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Alexandra Marinina Bibliography Apa

A Cultural Window to the West


Abstract:
Perspectives on Russian television focus mainly on state controlled networks. Russia, however, also has several important commercial televisions stations to whom little attention has been given. The most important of these stations is the entertainment network STS. The station was founded in 1996 when a subscription station AMTV merged with Saint Petersburg based broadcaster Channel Six and several regional stations to form Russia’s fifth national broadcaster. After airing primarily Hollywood and Latin American series in the 1990s, the station began to produce Russian language series in 2003. Today the station is one of the most important entertainment brands in the former Soviet Union. This paper traces the history of STS and its importance in bringing new genres and production techniques to Russia. It also maps the network’s explosive growth in the 2000s and its relationship with major Hollywood studios, most notably Sony. The influence of the station’s two most important executives Alexander Rodanyansky and Vyacheslav Murugov is also examined. The paper then theorizes on what STS’ current strategy may yield and what its current programs suggest about the changing nature of the Russian television market in an increasingly politicized environment.

Keywords: Russia, Television, Sony, STS, Hybridity, Cultural Odourlessness, Localization

1 Introduction

The typical focus of academic and popular works that examine media, and particularly television in the Russian Federation has been on two main aspects, news programming and propaganda. These discourses frequently circulate in the popular press, but academics have also mostly focused on these types of analysis. 1 While these are both real and serious aspects of the Russian media environment and worthy of examination, the fact that scholars in the West focus on them almost exclusively means that the focus has been entirely on the relationship of television to the Putin-led Russian state. The narrow scope of accounts of the Russian media has obscured many of the trends that have taken place in the realm of popular fiction. In particular, it has overemphasized accounts of the Russian media that are heavily influenced by political economy and underplayed the impact of several aspects of globalization on Russian television, particularly in the creation of television fiction.

This paper examines the history of the television station STS and its relationship to the development of entertainment television in Russia. The story of the growth of STS in the post-Soviet period is an important one in many respects. The station and the programming that it produces are examples of how Western culture spread following the collapse of the USSR in 1991. The growth of the station and the shape that its programs ultimately took, speaks strongly in support of theories of cultural hybridity such as those of Marwan Kraidy that view the merging of local and global forms as the “cultural logic of globalization.” 2 While discourses around hybridity have progressed in recent years as online video platforms like Netflix have transformed how people consume content, STS’s story has more in common with earlier accounts of hybridity that emphasized the blending of textual elements than it does with newer articulations of the concept that have emerged as a result of technological change. This paper also examines the interaction of STS with the international television industry, which has been one of the keys to the station’s success. While many Hollywood studios have attempted to enter the Russian market in some form, they have often failed to gain a foothold in the market. STS has been the most consistent and useful partner for the Western majors. This interaction has involved complex cultural negotiations, often with the Russians in the dominant position. The experience of Hollywood companies in Russia speaks against the typical account of Western dominance and media imperialism that is often prevalent in the works of scholars such as Toby Miller. 3 These scholars, generally taking their starting point from unreconstructed Marxist understandings of media flows expect that powerful Western companies like Disney, Warner Brothers, and Sony would simply be able to impose their programming and production practices on culturally and economically weaker peripheral markets like Russia. 4 While the majors, and Sony in particular, have had a strong impact on the Russian market, this examination of STS shows that their power is much more circumscribed than typical accounts of cultural and media imperialism might suggest. This study, therefore, aligns with researchers from scholars like Albert Moran, Jean Chalaby and Silvio Waisbord whose studies of the international format trade noted that, despite the West’s dominant position in the creation and distribution of these texts, national context, local producers, and local tastes, mediate the way formats are adapted. This need for localization ultimately works against overt western dominance. 5 As Moran notes “TV formats continue to anchor their adaptations in the ongoing reality of the national.” 6

2 STS: From Regional Station to National Juggernaut

For primarily economic reasons, television production in Russia lagged in the 1990s and was limited to a few genres, most notably the police procedural. Production accelerated greatly in the early 2000s, with an increasing number of genres appearing on Russian television. These included war dramas, period costume dramas, and many literary adaptations. By 2006 Russian language programming had mostly displaced imported shows in prime time. The industry continued to grow rapidly through the late 2000s and 2010s, with new networks and production companies emerging. One of the stations to gain prominence during this period was the television channel Set’ Televizionnykh Stantsiy or STS. The station was founded on December first, 1996, when Moscow-based AMTV, Saint Petersburg’s Channel Six and several regional rebroadcasters merged to form Russia’s fifth national broadcaster. 7 The network’s early years were unremarkable, as it struggled to create a brand identity. Under its first two general directors, STS grew slowly relying mostly on American and European imports. In early 2002 Alexander Rodnyansky was appointed to head the network. The company moved its headquarters from Russia’s second city back to the capital which housed most of the country’s production spaces. Given the trend towards primetime being dominated by domestically produced programs, Rodnyansky decided that STS needed to produce its Russian language series. The first program that STS produced was a costume drama set in nineteenth century Saint Petersburg titled Bednaya Nastya ( Poor Anastasia) (2003-2004). It was very popular and marked the first time that STS had managed to reach a mass audience. The project was the station’s first collaboration with Sony Pictures Television. Initially, Sony provided consulting on the technical and writing aspects of the series to STS and its partners. In less than a year one hundred and twenty seven episodes were produced, and the series was one of the most successful on Russian television.

Starting with Poor Anastasia, the series that STS brought to the screen differed sharply from most of their Soviet and post-Soviet predecessors. In the Soviet period, two factors had sharply constrained television production. The budding media often had difficulty accessing studio space and supplying itself with film stock since both were controlled by the Soviet film industry which saw television as inferior and therefore often refused to share its resources. 8 As a result, most Soviet television series had a short duration, usually about a dozen episodes. Long running series were relatively unknown. Soviet series were restricted to genres acceptable to the Communist party. This control meant that, for the most part, police and espionage dramas were most common. When the Russian industry began to produce new television in greater volume at the end of the 1990s, they were mostly mini-series, and creators returned first to the genres that had succeeded in the USSR. The most popular programs of the late 1990s were police dramas like Ulitsy Razbitykh Fonarei ( Streets of Broken Lights ) a series set in Saint Petersburg and Kamenskaya based on a popular series of police procedural novels by Alexandra Marinina. According to Konstantin Klioutchkine, the creators of these series resisted Western cultural encroachment by creating series that were “baggy monsters.” 9 He notes that these series combined multiple loose stories, privileged dialogue over action and “rather than emulating the gloss of the Western television image, they emphasize the smudge of the Russian picture.” 10 These series were difficult to watch, appeared only sporadically and ultimately were poorly positioned to compete with relatively well-crafted series that emerged from the STS-Sony partnership. Younger audiences who were not steeped in style of Soviet entertainment quickly became STS’s core audience.

The successful partnership with Sony became one of the dominant aspects of the STS program schedule in the mid-2000s. Following the success of Poor Anastasia, STS commissioned forty episodes of an adaptation of the American sitcom The Nanny (1993-1999) which it purchased from Sony. The Russian series was called Moia Prekrasnaia Niania (My Fair Nanny) (2004-2009). The Nanny format had been successful globally, and because of its long duration on American television, it had over a hundred episodes which meant STS could proceed with a rapid production schedule. Certain aspects of the series needed to be changed to the Russian context, but most of these were surface alterations rather than changes to the core of the program. For example, the main character was changed from a Jewish American from Queens to a Ukrainian immigrant from the working-class Moscow suburb of Birulyova. Both the original and Russian adaptation emphasized social class as exemplified by dialect, Yiddish and Ukrainian slang in the respective versions. These types of distinctions between classes and ethnicities within a society are relatively universal and for a transnational adaptation to succeed they need only be localized by a partner who understands what will resonate with local audiences. The wager that STS and Sony made was that with the involvement of consultants from Sony, STS could successfully adapt American sitcoms for Russian audiences and overcome the unease that they had with the genre. 11

Their strategy was successful, and My Fair Nanny became one of the most-watched series on Russian television with nearly a quarter of Russian viewers tuning in four times a week. The lead actress, Anastasiya Zavorotnyuk, quickly rose through the ranks of the Russian star system and became the most popular female celebrity in the country. With some effort, the series overcame the stigma previously attached to the sitcom genre to become successful. Hostility to the situation comedy and its unfamiliarity to Russian audiences was so acute that the general director of STS Alexander Rodnyansky made media appearances trying to explain the norms of the genre to Russians. Most notably he appeared on an episode of a radio program Telekhranitel that focuses on the latest trends on Russian television on the culturally oriented station Ekho Moskvyi . On the program, Rodnyansky tried to explain the norms of the sitcom genre to the host Elena Afanaseeva and answered questions from listeners who phoned the station. 12 The efforts bore fruit and sitcoms are now a staple of STS’s program schedule.

My Fair Nanny’s success led to a long partnership between STS and the American studio. Eventually, they would produce five other hit programs. The relationship was not always frictionless. As is evident in the documentary Exporting Raymond (2010) about the American producer Phillip Rosenthal’s experience bringing Everybody Loves Raymond (1996-2005) to Russia, STS and the local producers frequently resisted the advice that they were given. The documentary is problematic since it highlights conflicts for the sake of entertainment and presents only the American perspective, thereby framing Rosenthal and Sony as protagonists opposed by uncomprehending Russians. It does, however, offer a rare glimpse of the negotiations that take place when adapting texts from one national context to another. While Exporting Raymond should be viewed critically, it is still extremely valuable in understanding the process of transnational cultural adaptation. For example, Rodnyansky rejected Rosenthal’s pick for the male lead simply to prove that he was in charge. Those types of conflicts permeate the documentary. Sony’s need to negotiate with its Russian partners and the fact that none of the other Western studios ever succeeded in Russia suggests that the models of political economy and cultural imperialism are inadequate to describe the complexities of transnational media transfers. Sony succeeded in Russia because it was willing to invest in the Russia market by placing personnel in the country for long periods of time to learn how to negotiate the cultural landscape and build relationships. Sony’s consultants were not present in the writing rooms or on the set to impose a cultural agenda set by Hollywood; they were there to guide and teach their Russian partners, thereby ensuring the success and profitability of their series. Sony’s role was much closer to a partnership with the Russians in the lead position than the type of center-margin account promulgated by a political economist. Sony exerted influence, rather than forcing its Russian partner into an American way of producing television or imposing a Western neo-liberal ideology.

3 STS Becomes the Market Leader

Sony’s success and their ability to help their Russian partners produce popular programs allowed STS and its major production partners to develop their in-house talent. Writers trained on co-productions with Sony went on to create original Russian programs that shared many characteristics with American sitcoms. The first of these programs was the original series Papiny Dochki ( Daddy’s Girls ) (2007-2013). The series was developed and produced by one of STS’s in-house studios. This sitcom is notable for several reasons. It is the first original Russian sitcom to be developed without any assistance from a Western company, and it quickly became one of the most popular series in the market. At its peak in 2008 and 2009, the series was drawing nearly a quarter of Russian viewers four nights a week. 13 The series resembles the Sony sitcoms in several ways, relying primarily on physical comedy and character stereotypes to drive the humor.

While the program was a landmark for the Russian industry and STS, it was not particularly innovative. A Russian producer who worked on the program suggested that “the whole concept by itself … it’s a good concept, but it’s nothing overwhelming… They are [Russian] stories dealing with Russian reality rather than adapted American reality.” 14 The Russian reality he refers to are problems either with the idiosyncratic school system, the Russian legal system, corruption, struggles with housing, or the outsized role of oligarchs in Russian society. Regardless of its conventional structure, the program represented one of the first successful comedies of the post-Soviet era that told Russian stories in a humorous and engaging way. Its similarity to sitcoms from America, supports Kevin Robins idea that transnational television becomes hybridized through “structures of common difference.” By this term, he means that as the media globalize, audiences across different national borders consume similar kinds of media products, but inflected with national or local variations. 15

Supported by Sony co-productions and an increasing number of original series, STS went from a distant fifth in the national ratings in Russia at the beginning of the Rodnyansky era, to consistently jockeying with state-controlled NTV for third place. It was also during this period that STS began expanding. Its parent company, STS Media Holdings, began purchasing smaller channels in Russia and parts of the former Soviet Union including two channels in Russia, a satellite station and channels in Moldova and Kazakhstan. This expansion meant that by the end of Rodnyansky’s tenure at STS, it had grown from a nearly irrelevant Russian channel to the premiere entertainment brand in the former Soviet Union. The firm was valued at approximately four billion dollars, making it one of the most valuable media holding companies in Europe at the time.

4 The Murugov Era: STS’s Global Cultural Ambition

On the twenty-fourth of June 2008, Alexander Rodnyansky ended his tenure as the head of STS and was replaced by well-known Russian producer Vyacheslav Murugov. The latter’s tenure is controversial. Under his leadership, STS launched several of their best rated, most celebrated programs and made major strides towards becoming a supplier of formats to the international market. At the same time, the station struggled to maintain its position in the Russian market, falling from fourth to sixth place. It came to rely on one production studio for most of its popular programs and passed up formats and genres that its rival TNT used to surpass it in the overall ratings.

Murugov, who as a producer had spent a great deal of time on the floor of trade fairs like MIPTV and MIPCOM, believed that there was an opportunity for Russian companies to create formats to supply an increasingly demanding transnational industry. In his opinion, much of the market for formats had by 2011 become stale and repetitive. To move forward as a producer of programming that would be appealing to audiences outside of Russia, STS had several problems to overcome related to what Joseph Straubhaar calls “cultural proximity.” By this, he essentially means that people prefer to consume media from a culture similar their own. This concept means that Russian cultural products would be successful in the countries with which it shares cultural ties but not elsewhere since Russian culture is somewhat distinct from those of Western nations. 16 The program that marks the movement toward being the producer of programs that appeal and sell in the international marketplace, and thus overcomes these problems, is Kukhnia ( The Kitchen ) (2012-2016).

The Kitchen is notable in several ways. It has the highest budget of any Russian sitcom ever produced at approximately two hundred thousand dollars per episode. 17 The large budget, at least by Russian standards, allowed them to produce a program which in many ways is visually comparable with Western, single camera situation comedies. Through the first three seasons, The Kitchen was a ratings success, outperforming other programs in its time slot and helping to reinvigorate the STS brand as a whole. 18 The finale of the third season set an all-time ratings record for a Russian series, attracting about thirty percent of viewers in Moscow and twenty-five percent in the rest of the country. 19 The series continued to generate strong ratings in its last three seasons, never falling below twenty percent of viewers nationally.

The Kitchen was created with the format market in mind. The removal of most of the cultural markers that would have signaled it as being Russian makes the series culturally odourless. Koichi Iwabuchi defines cultural odour as the elements which tie a cultural product “with widely disseminated symbolic images of the country of origin” often in a way that can be disconcerting to audiences outside the country of origin. 20 The Kitchen is designed to be a culturally odourless product. The setting is an important aspect of this cultural odourlessness. The series set in an upscale French Restaurant called Claude Monet, and though the series obviously takes place in Moscow, because of it takes place in a milieu common in the era of globalization it could easily be transferred to another city. The mise-en-scène used in the series depicted in Figures 1 and 2 is very generic. Far from resembling a Russian restaurant the expensive furniture of the dining room and white-tiled industrial kitchen could be a French Restaurant in any global city. The only significant cultural marker that appears in the restaurant are the head Chef’s fan paraphernalia, displayed in his office for his favorite sports club, FC Spartak Moscow ( Figure 3 ). As part of the localization of the program, these items could easily be changed to match the new context.

Figure 1. The dining room at the Claude Monet restaurant (Image capture from STS’ official Youtube channel).

Figure 2. The Kitchen at the Claude Monet restaurant (Image capture from STS’ official Youtube channel).

Figure 3. The Chef’s office complete with Spartak FC paraphernalia (Image capture from STS’ official Youtube channel).

The non-diegetic music the series uses is another element that suggests that it is aimed at audiences outside Russia. Typically, Russian series license non-diegetic music from Russian artists since it is less expensive than using music from well-known Western artists. The Kitchen, however, uses music almost exclusively from the cannon of global culture. Most prominently the program features songs from Beyoncé, Neon Trees, Enya, OK GO, and REM but virtually all the music used in the series comes from a host of English-speaking artists or the library of classical music. In fact, through the first sixty episodes of the series, non-diegetic Russian music is used in only three instances. As the effects of economic sanctions began to affect the Russian economy after 2014, the program used less known Western bands and more Russian popular music but still maintained its global flavor. For the most part, through all six seasons, the music used in the program is familiar to audiences outside the Russian-speaking world, adding to the odourlessness of the series’.

Most of the humor in the series revolves around conflicts that take place in the restaurant or relate to the romantic misadventures of the series’ philandering protagonist Max Lavrov (Mark Bogatyrev). The restaurant portion of the humor is primarily related to head chef Viktor Barinov’s (Dimitri Nazarov) alcoholism and gambling addictions, and the kitchen staff’s efforts to cover up their leader’s shortcomings. The video below shows a compilation of the Chef’s drunken escapades and exemplifies the humor that emerges from it. It was compiled by STS and posted on YouTube as part of a promotional campaign leading up to the sixth and final season of the program.

A recurring theme in the series are the practical jokes played by two chefs, Fedya and Senya on their peers. Again, some of these were compiled by STS as YouTube promotions.

Some comic situations also arise from the competition of the head chef with his counterpart at the Arcoboleno a competing high-end restaurant on the same block. The humor of the series is bound up in the everyday experiences of globalization, such as the increasing number of people working in contingent service industry jobs, the increased normalcy of work environments where men and women work together, creating the possibility of romance and the fact that several people working in the kitchen are illegal migrants.

For those familiar with the Russian market, the program is recognized as a landmark in production quality. A vice president of international programming at a US studio whose area includes Russia put it the most bluntly stating that “ The Kitchen has changed the game… It’s one of the first shows, it’s so bright and airy and not just mired down in dark, ashen Russia…. it could be shot anywhere. It feels like any country that I don’t understand the language. 21 When asked if they believed the program might be viable on the international market they answered “seeing The Kitchen , I could, but before that, I didn’t.” 22 The fact that the series has drawn the attention of media giants outside of Russia for its quality is a rare achievement for that industry and suggests that Murugov’s vision of STS supplying programs to the international audience could come to fruition.

The first step in the direction of becoming a provider of formats for the world market occurred on November 26 th , 2013 when STS announced that it had reached an agreement with the international arm of the American network CBS to distribute The Kitchen worldwide. 23 Under the agreement, the former Soviet Republics remain under STS’s control. CBS has the rights to the series’ format in all the markets outside of that zone excluding Israel. Obviously, this is a very important agreement from the Russian point of view. While CBS holds the right to The Kitchen, it has yet to commission a pilot for the program. The only sign of The Kitchen in the United States thus far is its availability for streaming on the internet based services Hulu and Amazon Prime. 24 Three adaptation of the program to date have appeared in Georgia, Estonia, and Greece. These productions may not be a significant achievement given that those countries have strong cultural and historic ties to Russia. 25 While the success of The Kitchen internationally remains somewhat unclear, this has not stopped STS from pushing forwards with further efforts to develop programs for the format market. The company created some other culturally odourless programs such as Posledniy iz Magikan (Last of the Magikans) and Angelika both of which use similar structures to remain culturally odourless. These series are part of an increasing number of international series structured around “universal” story elements that “in any given television series is what might enable its subsequent adaptations in different countries around the world.” 26 Neither Last of the Magikyans or Angelika have achieved the success of The Kitchen , but they point to the fact that STS’s broader ambitions are not isolated to one program. They continue to invest heavily in new programs with this goal in mind.

This attempt to gain international recognition is central to the future of STS, since the Russian market is becoming increasingly saturated and competitive. As a result, they have invested significant time and effort into the venture. Vyacheslav Murugov stated in an interview that reaching this agreement required a large investment from the Russian side including the creation of promotional materials in English, including a roughly six-minute trailer with subtitles and English narration and an information book that breaks down the program’s performance in Russia by market segment.

He also said:

It is impossible just to sit in a chair and hope that someone will call and say “Hey we want to purchase The Kitchen… we had to build huge displays in Cannes where we placed large billboards. It required a great deal of preparation. It seemed like the right moment to get into this market. The Americans and the whole world are waiting for new formats.27

Accounts like the one above, coming as they do from industry trade publications are somewhat problematic since they are often structured to promote a particular narrative, in this case that of STS’s growing global ambition. They do, however, reveal the discourses that Russian producers are themselves promulgating. They are, therefore, important sources of information despite their origin. The expense and effort to create promotional material for the series at industry trade shows reflects STS’s willingness to take its products to the international market and invest heavily in getting its programs adopted. It also reflects the serious ambitions of STS. The Kitchen is the result of a decade and a half of STS copying, hybridizing and experimenting with a Western genre, but also having a deep engagement with Western companies like Sony from which they learned how to create series for both domestic and international audiences. If The Kitchen is successful in the West or elsewhere, it would represent one of the first significant Russian contributions to international culture since the collapse of communism. It is a bold undertaking by STS that represents an intense desire by Russian producers and Russian companies to gain recognition as an important cultural player again.

5 Present and Future Challenges for STS

While STS has international ambitions, it remains a Russian company and as such its relationship to the state ultimately affects what is its representational practices and its future. Even though it is an entertainment only network and there is relatively little engagement with politics, STS is still clearly vulnerable to pressure from the state and actively works to keep itself from running foul of mandates coming from the Kremlin. For example, a gay character on The Kitchen was rewritten after the first season to comply with Russia’s 2013 law banning “gay propaganda.” STS has also had to restructure its ownership following the passage of new media ownership laws in Russia. The Putin government’s reaction to the protests that swept their allies out of power in Kyiv (Kiev) was to try to make such a revolt impossible in Russia by forcing foreign-owned media outlets to shut down or to transfer ownership to a Russian company. Though the media law did not target STS, it’s passage forced Sweden’s Modern Times Group to sell its forty percent stake in the network to a Russian consortium dominated by Putin allies and to delist from the NASDAQ. The Putin government has used numerous tactics to control the political content of the media. Both NTV and REN-TV, leading channels of anti-Putin dissent in the early 2000s were handed over to Kremlin allies after their owners were arrested on false charges. 28 Both the change in the types of representations possible on STS and the forced changes in its ownership structure point to some of the problems and trends that one finds in authoritarian capitalist states with regards to television and other media platforms. While, as Michael Idov noted, the Kremlin does not police fiction particularly carefully there is a fear among creators that a wrong move might lead the state to intervene. 29 As an international format consultant put it “the show runners and the people doing the show, we’ll self-censor. There’s no office at the network [or] at the production company who were looking at script… but simply, you have to be an idiot to take that chance, because, you know, they’ll just take your show away.” 30 The Russian government and its allies in the economic elite, the so-called oligarchs, currently own all major media outlets. If they must be shut down at some point, the decision can be made to seem at least somewhat legitimate. They can argue, as was the case with both NTV and REN-TV when they were brought under the control of Putin allies, that these were business decisions relating to debts owed or the will of a board of governors, rather than a directly political operation. 31 While these arguments rarely convince critics in the West, people in Russia seem to give such arguments at least some credence. The state, in Russia at least, leaves the semblance of a free market media system in place, for the most part forcing stations to fund their operations through advertising sales. It, however, wants to make certain that these media assets cannot ever be used against the state. Therefore, the state or its allies in the economic elites own and control all of the major media outlets. Even if they never produce programming that could be considered even remotely political, they are watched with a wary eye. Typically only people who are well connected both within the entertainment industry and the political establishment are allowed to manage the six national broadcasters. This arrangement is similar to those found in other authoritarian capitalist states like China, Vietnam and newly emerging authoritarian capitalist states like Hungary and Turkey. 32

For all its past successes, the future of STS is now unclear. It has fallen behind many of its competitors, and despite its best efforts the new programs that it has premiered have failed to attract the massive audience that its popular programs of the 2000s and early 2010s achieved routinely. The changes in Russian media laws forced the company to leave the NASDAQ and seek financing in Russia. Along with the new ownership restrictions, the damage done to the Russian economy is constraining STS’s ability to raise capital and create compelling original programming. The network has been forced to increase its percentage of foreign programming, particularly Hollywood films, to make up the difference. 33 The station’s gambit to become a provider of formats has yet to come to fruition, meaning that much of the programming produced with this goal in mind failed to find a large domestic audience or to expand STS’s revenue base by selling formats.

The station still has a good reputation and strong connections to television and media industries in the West. It remains well positioned to take advantage of the expansion of new platforms and the associated need that media companies in the West have of finding new sources of content that attract audiences. However, the station has tended to cater primarily to multi-generation family programming with broad appeal, which in certain senses runs against the grain of the “quality television” that new platforms and cable stations seem to prefer. Other Russian networks, like the state-owned Channel One, are better positioned to take advantage of the move towards so-called “narratively complex television.” 34 There are certainly Russian production companies that are beginning to produce these types of series, but it is uncertain whether the STS brand could accommodate television programs of this kind. It is also increasingly unclear what role the Russian state and its stringent regulations will play on STS. In the past, the network benefitted from the fact that the state broadly ignored entertainment programming. With renewed conflict with the West, this situation might change at any time, and because of the network’s close ties with Hollywood, it might suffer from those types of changes more than other Russian networks.

6 Conclusion

While STS is struggling more than it did a few years ago, its legacy within the Russian industry is clear. The network has been the greatest importer of genres and techniques from the West. The programs listed above are essential for understanding the slow but steady turn of the Russian industry to accepted international media standards. It is also essential for understanding the slow shift of Russian audiences towards genres that are, ultimately, Western in origin. STS has had the deepest and most sustained relationship with the West, primarily through its strong ties with Sony. This interaction with Western companies and especially the station’s ties with important Hollywood studios cannot, however be classified as cultural imperial or Western domination of the kind predicted by political economy. In fact, STS has shown its ability to resist Western corporations in co-productions and take what it learns from them to create Russian versions of Western genres. This phenomenon has put Russia at the cusp of reasserting itself as a cultural producer and competitor to Western media firms on the world stage for the first time since the end of the Cold War. Because of its experience with Western genres STS is clearly the network most likely to produce a program that might be widely exportable back to the West or other large television markets. It is, therefore, no exaggeration to suggest that STS is a cultural relay between Russian and the international television industry. STS and its programs represent the movement of Russians towards a culture more in line with international norms. Given the enormous popularity that its programs have sustained over the long term, the influence of STS’s westernizing impulse is only likely to continue to grow.

Biography

Jeffrey Brassard is a doctoral candidate in the Department of Sociology at the University of Alberta. He is the author of articles in the Journal of Popular Film and Television, Palabra Clave and a forthcoming publication in The Journal of Historical Fiction .

  1. Sarah Oates, Television Democracy Elections, Routledge, 2006; Stephen White and Sarah Oates, ‘Politics and the Media in Postcommunist Russia,’ Politics 23, 1, February 2003, 31–37; Olessia Koltsova, News Media and Power in Russia, Routledge, 2006; Stephen C. Hutchings, ‘Saint Petersburg 300: Television and the Invention of a Russian (Media) Tradition,’ Television & New Media, 9, 1, January 2008, 3–23.↑
  2. Marwan Kraidy, Hybridity: The Cultural Logic of Globalization, Temple University Press, 2005.↑
  3. Toby Miller et al., eds, Global Hollywood: No. 2, British Film Institute, 2004.↑
  4. Enrique Uribe-Jongbloed and Hernán David Espinosa-Medina, ‘A Clearer Picture: Towards a New Framework for the Study of Cultural Transduction in Audiovisual Market Trades,’ Observatorio (OBS*) 8, 1, January 2014, 26.↑
  5. Albert Moran, ‘Reasserting the National? Programme Formats, International Television and Domestic Culture,’ in Television Studies After TV: Understanding Television in the Post-Broadcast Era, Graeme Turner and Jinna Tay eds, Routledge, 2009, p. 149-158; Silvio Waisbord, ‘McTV Understanding the Global Popularity of Television Formats,’ Television & New Media 5, 4, November 2004, 359–83; Jean K. Chalaby, Transnational Television Worldwide: Towards a New Media Order, I. B. Tauris, 2005.↑
  6. Albert Moran, ‘Reasserting the National? Programme Formats, International Television and Domestic Culture,’ 158.↑
  7. Natalia Zavyalova, ‘Novye televizionnye gorizonty — STS [New Television Horizons – STS],’ Gazeta Komersant, 13 August1997, https://www.kommersant.ru/doc/182415↑
  8. Kristin Roth-Ey, Moscow Prime Time: How the Soviet Union Built the Media Empire That Lost the Cultural Cold War, Cornell University Press, 2011, p. 188.↑
  9. Konstantin Klioutchkine, ‘The Kamenskaia Television Series and the Conventions of Russian Television,’ Kino Kultura, January 2007.↑
  10. Ibid.↑
  11. Dana Heller, ‘Russian ‘Sitkom’ Adaptation: The Pushkin Principle,’ Journal of Popular Film and Television, 31, 2, 2003, 60–72.↑
  12. Alexander Rodnyansky, ‘Smeshit’ po-russki: fenomen fil’ma Moia Prekrasnaia Niania [Laughter in Russian: The My Fair Nanny Phenomenon],’ interview by Elena Afanaseeva, Radio, 16 January 2005, http://echo.msk.ru/programs/tv/34025/↑
  13. ‘Papiny Dochki Vernutsya Na Tv S Kino Klishe [Daddy’s Girl’s Returns to Television with Film Cliches],’ Variety Russia, 6 May 2012.↑
  14. Interview with Russian Producer, interview by Author, 17 October 2014.↑
  15. Kevin Robins, ‘What in the World’s Going On,’ in Production of Culture/Cultures of Production, Paul du Gay ed, SAGE, 1998, 11–66.↑
  16. Joe Straubhaar, ‘Global, Regional, Transnational, Translocal,’ Media Industries 1, 3, February 2015.↑
  17. ‘STS Vkladyvaet 8 Mln Dollarov v Serial, Dejstvie Kotorogo Proishodit Na Kuhne Restorana [STS Is Investing 8 Million Dollars on a Show Set in a Restaurant Kitchen],’ Broadcasting.ru, 9 July 2012, http://www.broadcasting.ru/newstext.php?news_id=85960↑
  18. ‘Kukhnya na STS Ponravilas Strane [The Kitchen on STS is the nation’s favorite],’ Variety Russia, 25 October 2012.↑
  19. ‘Tretiy Sezon Kukhni Zavershilsya s Rekordnymi Reytingami [Third Season of The Kitchen End with Record Ratings],’ Variety Russia, 4 April, 2014.↑
  20. Koichi Iwabuchi, Recentering Globalization: Popular Culture and Japanese Transnationalism, Duke University Press, 2002, 38.↑
  21. Interview with the VP of International Development and Programming at a US Studio, interview by Author, 17 July 2014.↑
  22. Ibid.↑
  23. Katerina Kitayeva, ‘Russkaya Kukhnya Dlya Amerikantsev [Russia’s The Kitchen for Americans],’ 26 November 2013, http://rbcdaily.ru/media/562949989726542↑
  24. Vladimir Kozlov, ‘Russian Broadcaster CTC Media Sells Content to Hulu,’ The Hollywood Reporter, 7 July 2014, http://www.hollywoodreporter.com/news/russian-broadcaster-ctc-media-sells-716978↑
  25. ‘Serial Kukhnia adaptiruyut dlya Gruzii [The Kitchen Gets a Georgian Adaptation],’ The Hollywood Reporter: Russian Edition, 10 July 2015, http://thr.ru/article/7134/↑
  26. Isadora Avis, ‘Adapting Landscape and Place in Transcultural Remakes: The Case of Bron/Broen, the Bridge and the Tunnel,’ International Journal of TV Serial Narratives, 1, 2, Winter 2015, 130.↑
  27. Ksenia Boletskaya, ‘Vyacheslav Murugov Televidenie-Eto Ne Kanaly Eto Khity [Vyacheslav Murugov – Television is Not About Channels it is About Hits]’, Variety Russia, 4 October 2014.↑
  28. Ben Judah, Fragile Empire: How Russia Fell In and Out of Love with Vladimir Putin, Yale University Press, 2014, 44.↑
  29. Michael Idov, ‘My Accidental Career as a Russian Screenwriter,’ The New York Times, 7 January 2016, https://www.nytimes.com/2016/01/10/magazine/my-accidental-career-as-a-russian-screenwriter.html↑
  30. Interview with international format consultant, interview by Author, 10 July 2014.↑
  31. Koltsova, News Media and Power in Russia.↑
  32. Bilge Yesil, Media in New Turkey: The Origins of an Authoritarian Neoliberal State, University of Illinois Press, 2016.↑
  33. Vladimir Kozlov, ‘Russia’s TV Network CTC Media Re-Ups with Hollywood Majors,’ The Hollywood Reporter, 14 April, 2016, http://www.hollywoodreporter.com/news/russia-s-tv-network-ctc-883910↑
  34. Jason Mittell, Complex TV: The Poetics of Contemporary Television Storytelling, New York University Press, 2015.↑

Journal of European Television History and Culture
Volume 6 Issue 11/2017
DOI: http://dx.doi.org/10.18146/2213-0969.2017.JETHC125
Publisher: Netherlands Institute for Sound and Vision in collaboration with Utrecht University, University of Luxembourg, and Royal Holloway University of London
Copyright: Each article is copyrighted © by its author(s) and is published under license from the author(s). When a paper is accepted for publication, authors will be requested to agree with the Creative Commons Attribution-Noncommercial-No Derivative Works 3.0 Netherlands License.

Abstract

Background

Influenza A viruses of domestic birds originate from the natural reservoir in aquatic birds as a result of interspecies transmission and adaptation to new host species. We previously noticed that influenza viruses isolated from distinct orders of aquatic and terrestrial birds may differ in their fine receptor-binding specificity by recognizing the structure of the inner parts of Neu5Acα2-3Gal-terminated sialyloligosaccharide receptors. To further characterize these differences, we studied receptor-binding properties of a large panel of influenza A viruses from wild aquatic birds, poultry, pigs and horses.

Results

Using a competitive solid-phase binding assay, we determined viral binding to polymeric conjugates of sialyloligosaccharides differing by the type of Neu5Acα-Gal linkage and by the structure of the more distant parts of the oligosaccharide chain. Influenza viruses isolated from terrestrial poultry differed from duck viruses by an enhanced binding to sulfated and/or fucosylated Neu5Acα2-3Gal-containing sialyloligosaccharides. Most of the poultry viruses tested shared a high binding affinity for the 6-sulfo sialyl Lewis X (Su-SLex). Efficient binding of poultry viruses to Su-SLex was often accompanied by their ability to bind to Neu5Acα2-6Gal-terminated (human-type) receptors. Such a dual receptor-binding specificity was demonstrated for the North American and Eurasian H7 viruses, H9N2 Eurasian poultry viruses, and H1, H3 and H9 avian-like virus isolates from pigs.

Conclusion

Influenza viruses of terrestrial poultry differ from ancestral duck viruses by enhanced binding to sulfated and/or fucosylated Neu5Acα2-3Gal-terminated receptors and, occasionally, by the ability to bind to Neu5Acα2-6Gal-terminated (human-type) receptors. These findings suggest that the adaptation to receptors in poultry can enhance the potential of an avian virus for avian-to-human transmission and pandemic spread.

Background

The recent pandemic threat caused by the widespread circulation of H5N1 avian influenza viruses and their occasional transmission to humans as well as human infections caused by chicken H9N2, H7N7 and H7N3 viruses highlighted the need for a detailed study of host restriction mechanisms of influenza viruses. Numerous studies support the concept that alteration of the receptor specificity of an avian virus is essential for its transmission into humans as well as for human-to-human transmission and pandemic spread (reviewed in ref. [1,2]).

The history of research into the receptor binding phenotypes of influenza viruses can be divided into two periods: before and after 1997 when first human infections with chicken H5N1 viruses were documented. Before 1997, it was established that human influenza viruses recognize Neu5Acα2-6Gal-terminated receptors, avian viruses recognize Neu5Acα2-3Gal-terminated receptors while swine viruses recognize both of them [3-8]. It was shown that the receptor-binding site (RBS) of the hemagglutinin (HA) of avian viruses is evolutionally very stable. In addition to eight amino acids forming the HA RBS, which are conserved in all influenza A viruses (positions 97, 98, 134, 139, 153, 183, 184 and 195; H3 numbering is used here and throughout the paper), there are six more amino acids conserved in HAs of duck viruses (positions 138, 190, 194, 225, 226 and 228), and these are positions where human HAs are different from duck viruses [7]. Virus receptor binding specificity was found to correlate with the level of expression of relevant sialic acids determinants on the target cells of different host species. Thus, epithelial cells of human airway epithelium were shown to express high amounts of Neu5Acα2-6Gal-terminated sialyloligosaccharides, duck intestinal epithelium predominantly contains Neu5Acα2-3Gal-terminated receptors while swine tracheal epithelium contains both receptor types [8,9]. It was hypothesized that alteration of receptor specificity of avian viruses in some intermediate host, such as swine, might facilitate their transmission to humans [10].

After 1997, it became clear that avian H5N1 viruses are capable of replicating in humans [11,12] despite their avian-virus-like preference for Neu5Acα2-3Gal-containing receptors and lack of binding to human-type receptors [13]. It was shown afterwards that human airway epithelial cells express 2-3-linked sialic acid receptors with a density sufficient for the entry and replication of avian viruses [14,15].

Furthermore, a Eurasian lineage of poultry H9N2 viruses was discovered, which recognized Neu5Acα2-6Gal-terminated sialyloligosaccharides, thus indicating that some avian influenza viruses may display a human-virus-like receptor specificity [16-18]. It was also demonstrated that chicken and quail intestinal cells contain both Neu5Acα2-3Gal and Neu5Acα2-6Gal sialyloligosaccharides, in contrast to duck cells that contain only Neu5Acα2-3Gal [19-23].

Although the Neu5Acα2-3Gal receptor specificity is shared by the majority of avian viruses, viruses adapted to different avian species can differ in their ability to recognize the third saccharide and more distant moieties of Neu5Acα2-3Gal-terminated receptors. For example, duck viruses of various subtypes preferentially bound to glycoprotein O-chain trisaccharide Neu5Acα2-3Galβ1-3GalNAcα, whereas H5N1 chicken viruses preferred receptors with inner β-N-acetylglucosamine moiety, Neu5Acα2-3Galβ1-4GlcNAcβ [20]. Sulfation of the saccharide core produced no effect on binding of duck viruses, whereas chicken and human viruses isolated in 1997 in Hong Kong demonstrated an extraordinarily high affinity for sulfated trisaccharide Neu5Acα2-3Galβ1-4(6-HSO3)GlcNAc (Su-3'SLN) [24,25].

In the present study, we characterized the receptor-binding specificity of a broad set of influenza A viruses from wild aquatic birds, poultry, pigs and horses.

Results

Receptor-binding specificity

To determine the receptor-binding specificity of avian and mammalian influenza viruses, we tested their binding to 9 distinct polymeric glycoconjugates (see Fig. ​1 and Table ​1 for structural formulas and abbreviations). One of the glycoconjugates harboured 6-linked sialyloligosaccharide, Neu5Acα2-6Galβ1-4GlcNAc (6'SLN). The oligosaccharide parts of the other glycopolymers shared the same terminal Neu5Acα2-3Gal moiety but differed: (i) by the type of the bond between galactose and the next sugar residue (β1–3 or β1–4), (ii) by the nature of this residue (GlcNAcβ or GalNAcα), and (iii) by constituents at different positions on the GlcNAc ring (fucose or/and sulfo group). All studied oligosaccharide structures have been found in natural glycoproteins or glycolipids [26]. Virus binding to glycoconjugates was determined in a competitive solid-phase assay and expressed in terms of binding affinity constants (Fig. ​2).

Figure 1

Molecular models of sialyloligosaccharides. The models depict sialyloligosaccharide parts of glycopolymers that were tested for their binding to influenza viruses. Corresponding structural formulas are given in the Table 1. The figures were generated...

Table 1

Structure of sialyloligosaccharide parts of glycopolymers

Figure 2

Binding affinity constants of virus complexes with sialylglycopolymers. The constants were determined as described in the Methods and were expressed in μM of sialic acid. Higher values of constants correspond to lower binding affinities. The data...

Each of the tested viruses bound SLec, Su-SLec and STF with the same affinity and none of the viruses discriminated between SLex and SLea. We, therefore, do not show here the binding data for Su-SLec, STF and SLea. The patterns of viral binding to the panel of receptor analogues varied significantly among viruses of different subtypes and host species (Fig. ​2), however, several distinctive groups of viruses with typical receptor binding phenotypes could be recognized as described below.

Viruses of various subtypes isolated from wild ducks

These viruses displayed the highest binding affinity for glycoconjugates with β(1–3) linkage between Neu5Acα2-3Gal disaccharide fragment and the next GlcNAc residue, i.e., SLec, Su-SLec and STF. Other characteristic features of duck viruses were their low affinity for fucosylated sialyloligosaccharides SLea and SLex, nearly equal affinity for sulfated and non-sulfated sialyloligosaccharides, and a lack of appreciable binding to 6'SLN.

Viruses with H6 HA

Five viruses with H6 HA tested in this study were isolated from different avian species (turkey, shearwater, teal, chicken and gull). Unlike typical duck viruses, all H6 viral isolates efficiently bound to fucosylated sialyloligosaccharides SLex and SLea.

Viruses with H7 HA

Viruses of H7 subtype from two evolutionary lineages were tested: 1) American avian H7N2 viruses and closely related human isolate A/New York/107/03 (H7N2) [27], and 2) Eurasian H7N7 human isolates that were transmitted to humans from infected poultry during the 2003 outbreak in the Netherlands [28]. Viruses from both lineages showed enhanced binding to sulfated sialyloligosaccharides with the Galβ1-4GlcNAcβ core. The American viruses displayed the highest affinity for Su-3'SLN, whereas the H7N7 viruses from the Netherlands had particularly high affinity for Su-SLex. It was found unexpectedly that all H7 viruses tested displayed moderate binding affinity for human-type receptor 6'SLN (Fig. ​2).

H9N2 viruses

The H9N2 viruses tested could be arbitrarily separated into three groups, North American viruses and distantly related virus A/Chicken/Korea/96323/96 [29] and two evolutionary lineages of poultry viruses from Southeast Asia, G1 and G9 [16-18].

Receptor-binding affinity of A/Goose/Minnesota/5773/80 and A/Turkey/Wisconsin/1/66 was similar to that of A/Duck/Primorie/3628/02 (H9N2) and duck viruses of other subtypes: they preferentially bound to SLec and bound poorly to fucosylated sialyloligosaccharides. Other North American viruses such as A/Chicken/New Jersey/12220/97 and A/Pheasant/Wisconsin/1780/88 showed high binding affinity for SLea, SLex and Su-SLex. A/Chicken/Korea/96323/96 had an increased affinity for sulfated sialyloligosaccharides Su-3'SLN and Su-SLex. None of these viruses bound 6'SLN.

In contrast to North American viruses, Asian isolates from G1- and G9- lineages bound to 6'SLN. The binding pattern of the human isolate A/Hong Kong/1073/99 (H9N2) resembled that of pandemic human viruses A/USSR/039/68 and A/Canada/228/68 (see Fig. ​2, bottom lines): all these three viruses strongly bound to 6'SLN and did not appreciably bind to Neu5Acα2-3Gal-containing oligosaccharides. A/Quail/Hong Kong/G1/97 demonstrated high affinity for 6'SLN, SLex and Su-SLex and did not bind to any of non-fucosylated Neu5Acα2-3Gal-containing receptors. All other Asian poultry viruses tested displayed moderate binding to 6'SLN, bound much stronger to sulfated receptors Su-3'SLN and Su-SLex and did not bind at all to 3'SLN, SLec, SLex, and Su-SLec.

Swine viruses

Four viruses isolated from pigs were tested. A/Swine/Hong Kong/9/98 belonged to the G9 clade of H9N2 viruses, A/Swine/Finistere/2899/82 and A/Swine/France/80 represented the European avian-like swine virus lineage and A/Swine/Kazakhstan/48/82 was a sporadic avian-like H3N6 isolate. A common feature of these viruses was their high affinity for Su-SLex and a moderate affinity for 6'SLN.

Equine viruses

Equine H3N8 viruses including the equine-like canine isolate A/Canine/Florida/43/2004 [30] showed a strong binding affinity for Neu5Acα2-3Gal receptors, preferring sulfated ones, Su-3'SLN or Su-SLex.

H5N1 Asian viruses

Viruses of this group were extensively analyzed in our previous studies [24,25]. Two typical chicken isolates were tested here for a comparison with other poultry viruses. Both A/Chicken/Hong Kong/220/97 and A/Chicken/Vietnam/NCVD11/03 revealed increased affinity for Su-3'SLN. The latter virus in addition showed a high affinity for Su-SLex.

Analysis of HA amino acid sequences and molecular modelling of the complexes of Su-SLex with H3, H7 and H9 HA

The characteristic feature of the duck viruses tested herein was their poor binding to fucosylated sialyloligosaccharides (Fig. ​2, upper part). This receptor-binding phenotype agreed with that described earlier for a variety of viruses from wild ducks [20,24,31]. In order to understand the molecular basis of this phenotype, we modelled a putative disposition of the fucosylated receptor Su-SLex in the receptor-binding site of the HA of Duck/Ukraine/1/63 (H3N8) [32]. The modelling predicted that the fucose moiety would come into a significant sterical conflict with the side chain of Trp222 (Fig ​3). We next compared the HA sequences of more than 400 duck influenza viruses of H1, H2, H3, H4, H5, H8, H9, H10, H11 and H14 subtypes available from the Genbank. All of these viruses had a bulky amino acids (Arg, Lys, Trp, Leu, or Gln) in position 222 of the HA. We suggest on this basis that partial overlap of the fucose moiety with the bulky amino acid in position 222 could be a universal mechanism that reduces the capability of duck viruses to bind fucosylated receptors.

Figure 3

Models of complexes of H3, H7 and H9 hemagglutinins with Su-SLex. The models were generated as described in the Methods using the crystal structures of the HAs of the viruses A/Duck/Ukraine/1/63 (H3N8) [32], A/Turkey/Italy/02 (H7N1) [33] and A/Swine/Hong...

Our analysis of 68 published H6 HA sequences revealed that 67 of them have Ala222. This finding suggests that a relatively good binding of H6 viruses to fucosylated sialyloligosaccharides SLex and SLea (Fig. ​2) could be explained by a lack of interference between the fucose moiety and the short side chain of the alanine in position 222 of the HA. Essential role of amino acid in position 222 in the binding of fucosylated receptors was also supported by the comparison of HA sequences of the H9N2 viruses, A/Goose/Minnesota/5773/80 and A/Chicken/New Jersey/12220/97 (Fig. ​2 and Fig. ​4). The latter virus had His222 and bound SLex 100-times better than the former virus (Leu222).

Figure 4

Partial HA amino acid sequences of H9N2 viruses. The sequences were obtained from GenBank. Differences with respect to the top sequence are shown. Amino acids in positions 190, 222, and 226 are highlighted. The figure was generated with GeneDoc 2.6 software...

The high binding affinity of H7 viruses to sulfated sialyloligosaccharides suggested that the sulfo group interacts with some charged amino acid residue in the receptor-binding site. To test this possibility, we modelled potential contacts of Su-SLex with the receptor-binding pocket of avian H3 and H7 HAs [32,33]. In the case of H3 duck virus, the sulfo group faced towards solution and did not form obvious direct contacts with the protein. However, in the case of the H7 HA, the sulfo group of Su-SLex was located in a close proximity to the side chain of Lys193, which is highly conserved among viruses with H7 HA (Fig ​3). This finding suggests that enhanced affinity of H7 viruses for Su-3'SLN and Su-SLex is due to favourable charged interactions between the sulfo group of the receptor and amino group of Lys193. The same mechanism is likely responsible for the high affinity for Su-3'SLN of H5N1 (Gambaryan et al., 2004, 2006) and H3N8 equine viruses (Fig. ​2) since viruses of both these groups have lysine in position 193.

South-eastern Asian H9N2 viruses have multiple amino acid substitutions in the receptor-binding region of the HA, most notably, the mutation Gln226Leu [34] (Fig. ​4). The typical human-virus-like receptor specificity of A/Hong Kong/1073/99 (H9N2) is in a good agreement with the notion that a single Gln226Leu replacement shifts the receptor specificity from recognition of Neu5Acα2-3Gal to recognition of Neu5Acα2-6Gal receptors [35,36]. A/Quail/Hong Kong/G1/97 (H9N2) differs from A/Hong Kong/1073/99 (H9N2) by the Gly225Asp substitution (Fig. ​4) that markedly enhances the affinity of this virus for fucosylated 3-linked receptors SLex and Su-SLex and leads to a rather an unusual receptor-binding phenotype (Fig. ​2).

The H9N2 viruses of G9-lineage harbour substitutions Gln226Leu and Glu190Ala/Thr/Val in the HA [18,34] (Fig. ​4). Viruses with Ala or Thr in position 190 bound Su-3'SLN and Su-SLex with the highest affinity and demonstrated moderate affinity for 6'SLN (Fig. ​2). As these viruses did not noticeably bind to Su-SLec, specific orientation of the sulfo group rather than its negative charge alone seems to be essential for the binding. We used the crystal structure of the HA of A/Swine/Hong Kong/9/98 (H9N2) (G9-lineage) in complex with 3-linked receptor [37] for the modelling of H9 HA interactions with Su-SLex (Fig. ​3). Due to the amino acid substitutions in positions 226 and 190 of the H9 HA, the conformation of 3-linked galactose in this complex differs from that in the H3 avian HA [32,37], leading to corresponding differences in the putative disposition of Su-SLex (compare H3 and H9 complexes in Fig. ​3). In the H9 HA, the fucose moiety shifts upwards resolving the steric interference with amino acid in position 222, whereas the sulfo group shifts downwards and fits into a cavity formed by amino acids in positions 190 and 186 and by the solvent water molecules bound to residues 98, 228 and 227 (PDB:1JSD[37]). This could explain why the substitutions Gln226Leu and Glu190Val in the H9 HA, that increased virus affinity for Neu5Acα2-6Gal, at the same time significantly enhanced its affinity for sulfated Neu5Acα2-3Gal-containing receptors, Su-3'SLN and Su-SLex.

Discussion

Although almost all avian viruses use the same terminal disaccharide Neu5Acα2-3Gal as receptor, the evolution of distinct virus lineages adapted to distinct avian species (wild ducks, gulls, or terrestrial poultry) has led to specialized abilities to recognize longer oligosaccharide chains. Thus, duck viruses have the highest affinity for SLec and STF (Neu5Acα2-3Galβ1-3GalNAcα). We demonstrated earlier that duck viruses bind strongly to gangliosides from duck intestine as well as to GD1a ganglioside, which is terminated by Neu5Acα2-3Galβ1-3GalNAcβ[7,19]. It is possible that gangliosides with this termination serve as functional receptors of influenza viruses in the duck intestine.

Our present study indicated that receptor specificity of viruses from different lineages adapted to quail and chicken differed from that of wild duck viruses. Sulfated and fucosylated 3'SLN is a suitable receptor for most of these poultry viruses. It was shown recently that bi-antennary a2-6/3 sialylated glycans with Galβ1-4GlcNAcβ core are major sialylated N-glycans expressed by intestinal epithelial tissues in both chicken and quail [23]. This fact is in accord with preferential binding of quail and chicken viruses to sialyloligosaccharides with Galβ1-4GlcNAcβ core.

Gull viruses appear to be adapted to fucosylated receptors, such as SLex [31]. We suggested earlier that the presence of glycine in HA position 222 of H13 and H16 viruses is essential for this binding phenotype [38]. In this study, we found that all tested H6 viruses, similarly to gull viruses, demonstrated enhanced affinity for SLea and SLex and that alanine in position 222 of the H6 HA is likely to play an essential role in this specificity. Since almost all sequenced H6 HA have Ala222, viruses of this subtype should be able to recognize receptor determinants that are optimal for duck (SLec), gull (SLex) and chicken (Su-SLex) viruses. This feature of H6 viruses would agree with their known promiscuous host range [39]. Some American H9 poultry viruses with substitution in position 222 showed receptor binding phenotype that was similar to that of H13, H16 and H6 viruses. It could be speculated that mutations in position 222 that improve sterical accommodation of the fucose moiety could represent one general pathway for adaptation of duck viruses to fucosylated receptors present in gulls and chickens.

Asian H5N1 viruses, H7 poultry viruses and equine H3N8 viruses realized another pathway of adaptation to recognition of the Su-SLex determinant via the favourable electrostatic interactions between the sulfo group and the amino group of Lys193.

One more pathway of viral adaptation to Su-SLex can be achieved through a substitution of conserved glutamic acid in the HA position 190. Importantly, this substitution that leads to enhanced binding to Su-SLex is often accompanied by the enhanced viral binding to the human-type receptor 6'SLN. Thus, high affinity for Su-SLex and moderate affinity for 6'SLN was detected in this study for G9-like H9N2 viruses, and previously for H1N1 swine [40] and human [41] viruses. H7 viruses with high affinity for Su-SLex also showed detectable binding to 6'SLN (Fig. ​2).

It is not clear whether the ability of H7 and H9 poultry viruses to bind to 6'SLN provides them with some evolutionary advantage. For example, the binding of these viruses to 6'SLN does correlate with the presence of 6'SLN-containing receptors in epithelial tissues of gallinaceous birds [19-23]. Alternatively, the ability of poultry viruses to bind to 6'SLN could be an accidental consequence of their adaptation for the binding to Su-SLex due to some sterical similarity between Su-SLex and 6'SLN in the regions of Neu5Ac-Gal glycosidic linkage and of the NAc-moiety of the GlcNAc residue (Fig. ​1).

The binding data (Fig. ​2) show that the receptor specificity of poultry H5, H7, and H9 viruses is similar to that of equine and avian-like swine viruses. If sulfated and fucosylated sialyloligosaccharides are present in the target cells of both terrestrial poultry and mammals, the adaptation of aquatic bird viruses to poultry could facilitate their replication in mammals, including humans.

Conclusion

It is generally believed that alteration of the receptor specificity is a prerequisite for the highly effective replication and human-to-human transmission which characterize pandemic influenza viruses [1,2,42]. Here we found that several independent lineages of poultry influenza viruses differ from their precursors in aquatic birds by enhanced binding to 6-sulfo sialyl Lewis X and that this binding specificity is accompanied by the ability of the virus to bind to human-type receptor 6'SLN. We therefore suggest that the adaptation to Su-Slex receptor in terrestrial poultry could enhance the potential of an avian virus for avian-to-human transmission and pandemic spread.

Methods

Materials

Oligosaccharides conjugated with polyacrylamide (~30 kDa) were synthesized from spacered sialyloligosaccharides (spacer = -OCH2CH2CH2NH2 or -NHCOCH2NH2) and poly(4-nitrophenylacrylate) having m.w. 30 kDa by the method described earlier [43,44]. Spacered oligosaccharides were synthesized as described previously [45-47].

Viruses

The majority of viruses in the study were from the repository of the Influenza Division, CDC, USA; some isolates were from the collection of the D.I. Ivanovsky Institute of Virology, Moscow. Viruses were grown in 9-day-old embryonated chicken eggs and were inactivated by treatment with beta-propiolactone as described previously [13]. The allantoic fluids were clarified by low-speed centrifugation; the viruses were pelleted by high-speed centrifugation, resuspended in 0.1 M NaCl, 0.02 M Tris buffer (pH 7.2) containing 50% glycerol, and stored at -20°C.

The binding affinity of influenza viruses for sialylglycoconjugates

Receptor specificity of influenza viruses was evaluated in a competitive assay based on the inhibition of binding to solid-phase immobilized virus with bovine fetuin labelled with horseradish peroxidase [48]. The competitive reaction was performed at 2–4 oC for 30 min in PBS with 0.01% of Tween-20; 0.05% of BSA and 3 μM of the sialidase inhibitor 4-amino-Neu5Ac-en. The data were expressed in terms of affinity constants (Kaff) formally equivalent to the dissociation constants of virus-receptor complexes. For the calculation of the constants, concentration of the sialic acid residues in the solution was used. Each set of experiments presented in the Fig. ​2 was repeated three-four times with similar results. Data were averaged from 3 sets of experiments.

Molecular models

Atomic coordinates of SLex (PDB:2KMB) [49], H7 HA (PDB:1TI8) [33], H9 HA (PDB:1JSD) [37] and H3 and H9 HA complexes with NeuAcα2-3Gal-containing pentasaccharide LSTa (PDB:1MQM and PDB:1JSH) [32,37] were obtained from Brookhaven Protein Data Bank. The molecular models were generated using DS ViewerPro 5.0 software (Accelrys Inc.).

The model of Su-SLex was constructed on the basis of SLex structure (PDB:2KMB), by replacing the hydrogen atom of the 6-OH group of GlcNAc by HSO3 group.

The models of Su-SLex in the receptor-binding sites of H3 and H9 HA were made by superimposing the galactose residue of the Su-SLex over the galactose residue of LSTa. The model of Su-SLex in the receptor-binding site of H7 HA was generated by superimposing the protein chain of the H3 HA complex with Su-SLex over the protein chain of H7 HA (PDB:1TI8). The OH groups of Tyr98, SG atoms of Cys139, CZ3 atoms of Trp153, CD atoms of Glu190 and CA atoms of Tyr 195 were used to align two proteins.

Competing interests

The authors declare that they have no competing interests.

Authors' contributions

Conception and design of the study, manuscript preparation (ASG, NVB, AIK, MNM); experimental work (ASG, ABT, GVP, JAD); co-ordination of the study (AIK, NVB).

Disclaimer

The findings and conclusions in the report are those of the authors and do not necessarily represent the views of the funding agencies.

Acknowledgements

We thank Dr. Svetlana Yamnikova (D.I. Ivanovsky Institute of Virology, Moscow, Russia) for providing us with duck influenza viruses and Dr. Michael Shaw (Influenza Division, Centers for Disease Control and Prevention, Atlanta, GA, USA) for critical review of the paper. This study was supported by research grants 05-04-48934 from the Russian Foundation for Basic Research, RAS Presidium program 'Molecular and Cell Biology', ISTC grant No:5 2464 and the European Commission projects FLUPATH, FLUINNATE and FLUVACC.

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