R G Webster

St. Jude Children's Research Hospital, Memphis, Tennessee, United States

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Publications (737)4026.35 Total impact

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    ABSTRACT: Compounds that target the cellular factors essential for influenza virus replication represent an innovative approach to antiviral therapy. Sp2CBMTD is a genetically engineered multivalent protein that masks sialic acid-containing cellular receptors on the respiratory epithelium, which are recognized by influenza viruses. Here, we evaluated the antiviral potential of Sp2CBMTD against lethal infection of mice with an emerging A/Anhui/1/2013(H7N9) influenza virus and addressed the mechanistic basis of its activity in vivo. Sp2CBMTD was administered to mice intranasally as a single or repeated dose (0.1, 1, 10, or 100 μg) before (day -7, -3, or/and -1) or after (6 or 24 h) H7N9 virus inoculation. A single Sp2CBMTD dose (10 or 100 μg) protected 80% to 100% of mice when administered 7 days before the H7N9 lethal challenge. Repeated Sp2CBMTD administration conferred the highest protection, resulting in 100% survival of mice even at the lowest dose tested (0.1 μg). When treatment began 24 h after exposure to the H7N9 virus, a single administration of 100 μg Sp2CBMTD protected 40% of mice from death. Administration of Sp2CBMTD induced pulmonary expression of proinflammatory mediators (IL-6, IL-1β, RANTES, MCP-1, MIP-1α, IP-10) and recruited neutrophils to the respiratory tract before H7N9 virus infection, which resulted in less pronounced inflammation and rapid virus clearance from mouse lungs. Sp2CBMTD administration did not affect the virus-specific adaptive immune response, which was sufficient to protect against reinfection with a higher dose of homologous H7N9 virus or heterologous H5N1 virus. Thus, Sp2CBMTD was effective in preventing H7N9 infections in a lethal mouse model and holds promise as a prophylaxis option against zoonotic influenza viruses. Copyright © 2014, American Society for Microbiology. All Rights Reserved.
    Antimicrobial Agents and Chemotherapy 12/2014; · 4.45 Impact Factor
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    ABSTRACT: In recent years, controversy has arisen regarding the risks and benefits of certain types of gain-of-function (GOF) studies involving avian influenza viruses. In this article, we provide specific examples of how different types of data, including information garnered from GOF studies, have helped to shape the influenza vaccine production process-from selection of candidate vaccine viruses (CVVs) to the manufacture and stockpiling of safe, high-yield prepandemic vaccines for the global community. The article is not written to support a specific pro- or anti-GOF stance but rather to inform the scientific community about factors involved in vaccine virus selection and the preparation of prepandemic influenza vaccines and the impact that some GOF information has had on this process. Copyright © 2014 Schultz-Cherry et al.
    mBio 12/2014; 5(6). · 6.88 Impact Factor
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    ABSTRACT: Most influenza pandemics have been caused by H1N1 viruses of purely or partially avian origin. Here, using Cox proportional hazard model, we attempt to identify the genetic variations in the whole genome of wild-type North American avian H1N1 influenza A viruses that are associated with their virulence in mice by residue variations, host origins of virus (Anseriformes-ducks or Charadriiformes-shorebirds), and host-residue interactions. In addition, through structural modeling, we predicted that several polymorphic sites associated with pathogenicity were located in structurally important sites, especially in the polymerase complex and NS genes. Our study introduces a new approach to identify pathogenic variations in wild-type viruses circulating in the natural reservoirs and ultimately to understand their infectious risks to humans as part of risk assessment efforts towards the emergence of future pandemic strains.
    Scientific Reports 12/2014; 4:7455. · 5.08 Impact Factor
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    The Journal of Infectious Diseases 10/2014; · 5.78 Impact Factor
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    ABSTRACT: Aquatic birds are the natural reservoir for avian influenza viruses (AIV). Habitats in Brazil provide stopover and wintering sites for water birds that migrate between North and South America. The current study was conducted to elucidate the possibility of the transport of influenza A viruses by birds that migrate annually between the Northern and Southern Hemispheres. In total, 556 orotracheal/cloacal swab samples were collected for influenza A virus screening using real-time RT-PCR (rRT-PCR). The influenza A virus-positive samples were subjected to viral isolation. Four samples were positive for the influenza A matrix gene by rRT-PCR. From these samples, three viruses were isolated, sequenced and characterized. All positive samples originated from a single bird species, the ruddy turnstone (Arenaria interpres), that was caught in the Amazon region at Caeté Bay, Northeast Pará, at Ilha de Canelas. To our knowledge, this is the first isolation of H11N9 in the ruddy turnstone in South America.
    PLoS ONE 10/2014; 9(10):e110141. · 3.53 Impact Factor
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    ABSTRACT: A novel avian-origin H3N2 canine influenza A virus (CIV) that showed high sequence similarities in hemagglutinin and neuraminidase genes with those of non-pathogenic avian influenza viruses was isolated in our routine surveillance program in South Korea. We previously reported that the pathogenicity of this strain could be reproduced in dogs and cats. In the present study, the host tropism of H3N2 CIV was examined by experimental inoculation into several host species, including chickens, pigs, mice, guinea pigs, and ferrets. The CIV infection resulted in no overt symptoms of disease in these host species. However, sero-conversion, virus shedding, and gross and histopathologic lung lesions were observed in guinea pig and ferrets but not in pigs, or mice. Based on the genetic similarity of our H3N2 CIV with currently circulating avian influenza viruses and the presence of α-2,3-linked rather than α-2,6-linked sialic acid receptors in the respiratory tract of dogs, we believed that this strain of CIV would have avian virus-like receptor specificity, but that seems to be contrary to our findings in the present study. Further studies are needed to determine the co-receptors of hemagglutinin or post-attachment factors related to virus internalization or pathogenesis in other animals.
    Virus Research 09/2014; · 2.83 Impact Factor
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    ABSTRACT: Genetic and phylogenetic analyses suggest that the pandemic H1N1/2009 virus was derived from well-established swine influenza lineages; however, there is no convincing evidence that the pandemic virus was generated from a direct precursor in pigs. Furthermore, the evolutionary dynamics of influenza virus in pigs have not been well documented. Here, we subjected a recombinant virus (rH1N1) with the same constellation makeup as the pandemic H1N1/2009 virus to nine serial passages in pigs. Severity of infection sequentially increased with each passage. Deep sequencing of viral quasi-species from the ninth passage found five consensus amino acid mutations: PB1 A469T, PA 1129T, NA N329D, NS1 N205K and NEP T48N. Mutations in the HA protein, however, differed greatly between the upper and lower respiratory tracts. Three representative viral clones with the five consensus mutations were selected for functional evaluation. Relative to the parental virus, the three viral clones showed enhanced replication and polymerase activity in vitro, and enhanced replication, pathogenicity and transmissibility in pigs, guinea pigs and ferrets in vivo. Specifically, two mutants of rH1N1 (PB1 A469T, and combined NS1 N205K and NEP T48N) were identified as determinants of transmissibility in guinea pigs. Crucially, one mutant viral clone with the five consensus mutations, which also carried D187E, K211E and S289N mutations in its hemagglutinin (HA), was additionally able to infect ferrets by airborne transmission as effectively the pandemic virus. Our findings demonstrate that influenza virus can acquire viral characteristics that are similar to those of the pandemic virus after limited serial passages in pigs.
    Journal of Virology 08/2014; · 4.65 Impact Factor
  • Sun-Woo Yoon, Richard J Webby, Robert G Webster
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    ABSTRACT: Wild aquatic bird populations have long been considered the natural reservoir for influenza A viruses with virus transmission from these birds seeding other avian and mammalian hosts. While most evidence still supports this dogma, recent studies in bats have suggested other reservoir species may also exist. Extensive surveillance studies coupled with an enhanced awareness in response to H5N1 and pandemic 2009 H1N1 outbreaks is also revealing a growing list of animals susceptible to infection with influenza A viruses. Although in a relatively stable host-pathogen interaction in aquatic birds, antigenic, and genetic evolution of influenza A viruses often accompanies interspecies transmission as the virus adapts to a new host. The evolutionary changes in the new hosts result from a number of processes including mutation, reassortment, and recombination. Depending on host and virus these changes can be accompanied by disease outbreaks impacting wildlife, veterinary, and public health.
    Current topics in microbiology and immunology 07/2014; · 3.47 Impact Factor
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    ABSTRACT: SUMMARY After an outbreak of pandemic influenza A/H1N1 (pH1N1) virus, we had previously reported the emergence of a recombinant canine influenza virus (CIV) between the pH1N1 virus and the classic H3N2 CIV. Our ongoing routine surveillance isolated another reassortant H3N2 CIV carrying the matrix gene of the pH1N1 virus from 2012. The infection dynamics of this H3N2 CIV variant (CIV/H3N2mv) were investigated in dogs and ferrets via experimental infection and transmission. The CIV/H3N2mv-infected dogs and ferrets produced typical symptoms of respiratory disease, virus shedding, seroconversion, and direct-contact transmissions. Although indirect exposure was not presented for ferrets, CIV/H3N2mv presented higher viral replication in MDCK cells and more efficient transmission was observed in ferrets compared to classic CIV H3N2. This study demonstrates the effect of reassortment of the M gene of pH1N1 in CIV H3N2.
    Epidemiology and Infection 06/2014; · 2.49 Impact Factor
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    ABSTRACT: The H7N9 influenza virus caused significant mortality and morbidity in infected humans during an outbreak in China in 2013 stimulating vaccine development efforts. As previous H7-based vaccines have been poorly immunogenic in humans we sought to determine the immunogenic and protective properties of an inactivated whole virus vaccine derived from a 2013 H7N9 virus in ferrets. As whole virus vaccine preparations have been shown to be more immunogenic in humans, but less likely to be used, than split or surface antigen formulations, we vaccinated ferrets with a single dose of 15, 30, or 50μg of the vaccine and subsequently challenged with wild-type A/Anhui/1/2013 (H7N9) either by direct instillation or by contact with infected animals. Although ferrets vaccinated with higher doses of vaccine had higher serum hemagglutinin inhibition (HI) titers, the titers were still low. During subsequent instillation challenge, however, ferrets vaccinated with 50μg of vaccine showed no illness and shed significantly less virus than mock vaccinated controls. All vaccinated ferrets had lower virus loads in their lungs as compared to controls. In a separate study where unvaccinated-infected ferrets were placed in the same cage with vaccinated-uninfected ferrets, vaccination did not prevent infection in the contact ferrets, although they showed a trend of lower viral load. Overall, we conclude that inactivated whole-virus H7N9 vaccine was able to reduce the severity of infection and viral load, despite the lack of hemagglutinin-inhibiting antibodies.
    Vaccine 06/2014; · 3.49 Impact Factor
  • Robert G Webster, Elena A Govorkova
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    ABSTRACT: Influenza is an acute respiratory disease in mammals and domestic poultry that emerges from zoonotic reservoirs in aquatic birds and bats. Although influenza viruses are among the most intensively studied pathogens, existing control options require further improvement. Influenza vaccines must be regularly updated because of continuous antigenic drift and sporadic antigenic shifts in the viral surface glycoproteins. Currently, influenza therapeutics are limited to neuraminidase inhibitors; novel drugs and vaccine approaches are therefore urgently needed. Advances in vaccinology and structural analysis have revealed common antigenic epitopes on hemagglutinins across all influenza viruses and suggest that a universal influenza vaccine is possible. In addition, various immunomodulatory agents and signaling pathway inhibitors are undergoing preclinical development. Continuing challenges in influenza include the emergence of pandemic H1N1 influenza in 2009, human infections with avian H7N9 influenza in 2013, and sporadic human cases of highly pathogenic avian H5N1 influenza. Here, we review the challenges facing influenza scientists and veterinary and human public health officials; we also discuss the exciting possibility of achieving the ultimate goal of controlling influenza's ability to change its antigenicity.
    Annals of the New York Academy of Sciences 05/2014; · 4.38 Impact Factor
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    ABSTRACT: There is a need for new approaches for the control of influenza given the burden caused by annual seasonal outbreaks, the emergence of viruses with pandemic potential, and the development of resistance to current antiviral drugs. We show that multivalent biologics, engineered using carbohydrate-binding modules specific for sialic acid, mask the cell-surface receptor recognized by the influenza virus and protect mice from a lethal challenge with 2009 pandemic H1N1 influenza virus. The most promising biologic protects mice when given as a single 1-μg intranasal dose 7 d in advance of viral challenge. There also is sufficient virus replication to establish an immune response, potentially protecting the animal from future exposure to the virus. Furthermore, the biologics appear to stimulate inflammatory mediators, and this stimulation may contribute to their protective ability. Our results suggest that this host-targeted approach could provide a front-line prophylactic that has the potential to protect against any current and future influenza virus and possibly against other respiratory pathogens that use sialic acid as a receptor.
    Proceedings of the National Academy of Sciences 04/2014; · 9.81 Impact Factor
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    ABSTRACT: Wild birds are an important but to some extent under-studied reservoir for emerging pathogens. We used unbiased sequencing methods for virus discovery in shorebird samples from the Delaware Bay, USA; an important feeding ground for thousands of migratory birds. Analysis of shorebird fecal samples indicated the presence of a novel astrovirus and coronavirus. A sanderling sample yielded sequences with distant homology to avian nephritis virus 1, an astrovirus associated with acute nephritis in poultry. A ruddy turnstone sample yielded sequences with homology to deltacoronaviruses. Our findings highlight shorebirds as a virus reservoir and the need to closely monitor wild bird populations for the emergence of novel virus variants.
    PLoS ONE 04/2014; 9(4):e93395. · 3.53 Impact Factor
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    ABSTRACT: Continuous circulation of influenza A(H5N1) virus among poultry in Egypt has created an epicenter in which the viruses evolve into newer subclades and continue to cause disease in humans. To detect influenza viruses in Egypt, since 2009 we have actively surveyed various regions and poultry production sectors. From August 2010 through January 2013, >11,000 swab samples were collected; 10% were positive by matrix gene reverse transcription PCR. During this period, subtype H9N2 viruses emerged, cocirculated with subtype H5N1 viruses, and frequently co-infected the same avian host. Genetic and antigenic analyses of viruses revealed that influenza A(H5N1) clade 2.2.1 viruses are dominant and that all subtype H9N2 viruses are G1-like. Cocirculation of different subtypes poses concern for potential reassortment. Avian influenza continues to threaten public and animal health in Egypt, and continuous surveillance for avian influenza virus is needed.
    Emerging Infectious Diseases 04/2014; 20(4):542-51. · 7.33 Impact Factor
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    ABSTRACT: Avian-origin influenza A(H7N9) recently emerged in China, causing severe human disease. Several subtype H7N9 isolates contain influenza genes previously identified in viruses from finch-like birds. Because wild and domestic songbirds interact with humans and poultry, we investigated the susceptibility and transmissibility of subtype H7N9 in these species. Finches, sparrows, and parakeets supported replication of a human subtype H7N9 isolate, shed high titers through the oropharyngeal route, and showed few disease signs. Virus was shed into water troughs, and several contact animals seroconverted, although they shed little virus. Our study demonstrates that a human isolate can replicate in and be shed by such songbirds and parakeets into their environment. This finding has implications for these birds' potential as intermediate hosts with the ability to facilitate transmission and dissemination of A(H7N9) virus.
    Emerging Infectious Diseases 03/2014; 20(3). · 7.33 Impact Factor
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    ABSTRACT: Avian influenza viruses may cause severe disease in a variety of domestic animal species worldwide, with high mortality in chickens and turkeys. To reduce the information gap about prevalence of these viruses in animals in Uganda, this study was undertaken. Influenza A virus prevalence by RT-PCR was 1.1% (45/4,052) while seroprevalence by ELISA was 0.8% (24/2,970). Virus prevalence was highest in domestic ducks (2.7%, 17/629) and turkeys (2.6%, 2/76), followed by free-living waterfowl (1.3%, 12/929) and swine (1.4%, 7/511). A lower proportion of chicken samples (0.4%, 7/1,865) tested positive. No influenza A virus was isolated. A seasonal prevalence of these viruses in waterfowl was 0.7% (4/561) for the dry and 2.2% (8/368) for the wet season. In poultry, prevalence was 0.2% (2/863) for the dry and 1.4% (24/1,713) for the wet season, while that of swine was 0.0% (0/159) and 2.0% (7/352) in the two seasons, respectively. Of the 45 RT-PCR positive samples, 13 (28.9%) of them were H5 but none was H7. The 19 swine sera positive for influenza antibodies by ELISA were positive for H1 antibodies by HAI assay, but the subtype(s) of ELISA positive poultry sera could not be determined. Antibodies in the poultry sera could have been those against subtypes not included in the HAI test panel. The study has demonstrated occurrence of influenza A viruses in animals in Uganda. The results suggest that increase in volumes of migratory waterfowl in the country could be associated with increased prevalence of these viruses in free-living waterfowl and poultry.
    BMC Veterinary Research 02/2014; 10(1):50. · 1.74 Impact Factor
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    ABSTRACT: Influenza B viruses cause annual outbreaks of respiratory illness in humans and are increasingly recognized as a major cause of influenza-associated pediatric mortality. Neuraminidase (NA) inhibitors (NAIs) are the only available therapy for patients infected with influenza B viruses and the potential emergence of NAI-resistant viruses is a public health concern. The NA substitutions located within enzyme active site could not only reduce NAI susceptibility of influenza B virus but also affect virus fitness. In this study we investigated the effect of single NA substitutions on fitness of influenza B/Yamanashi/166/1998 viruses (Yamagata lineage). We generated recombinant viruses containing either WT NA or NA with a substitution in the catalytic (R371K) or framework residues (E119A, D198E, D198Y, I222T, H274Y, N294S). We assessed NAI susceptibility, NA biochemical properties, NA protein expression, and virus replication in vitro and in differentiated normal human bronchial epithelial (NHBE) cells. Our results showed that four NA substitutions (D198E, I222T, H274Y, and N294S) conferred reduced inhibition by oseltamivir and 3 (E119A, D198Y, and R371K) conferred highly reduced inhibition by oseltamivir, zanamivir, and peramivir. All NA substitutions, except for D198Y and R371K, were genetically stable after 7 passages in MDCK cells. Cell surface NA protein expression was significantly increased by H274Y and N294S substitutions. Viruses with E119A, I222T, H274Y, or N294S substitutions were not attenuated in replication efficiency in vitro or in NHBE cells. Overall, viruses with E119A or H274Y NA substitutions possess fitness comparable to NAI-susceptible virus and their acquisition by influenza B viruses should be closely monitored.
    Antimicrobial Agents and Chemotherapy 02/2014; · 4.57 Impact Factor
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    ABSTRACT: Toll-like receptors (TLRs) play key roles in innate immune recognition of pathogen-associated molecular patterns of invading microbes. Among the 10 TLR family members identified in humans, TLR10 remains an orphan receptor without known agonist or function. TLR10 is a pseudogene in mice and mouse models are noninformative in this regard. Using influenza virus infection in primary human peripheral blood monocyte-derived macrophages and a human monocytic cell line, we now provide previously unidentified evidence that TLR10 plays a role in innate immune responses following viral infection. Influenza virus infection increased TLR10 expression and TLR10 contributed to innate immune sensing of viral infection leading to cytokine induction, including proinflammatory cytokines and interferons. TLR10 induction is more pronounced following infection with highly pathogenic avian influenza H5N1 virus compared with a low pathogenic H1N1 virus. Induction of TLR10 by virus infection requires active virus replication and de novo protein synthesis. Culture supernatants of virus-infected cells modestly up-regulate TLR10 expression in nonvirus-infected cells. Signaling via TLR10 was activated by the functional RNA-protein complex of influenza virus leading to robust induction of cytokine expression. Taken together, our findings identify TLR10 as an important innate immune sensor of viral infection and its role in innate immune defense and immunopathology following viral and bacterial pathogens deserves attention.
    Proceedings of the National Academy of Sciences 02/2014; · 9.81 Impact Factor
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    ABSTRACT: The divergence of the hemagglutinin gene of A/goose/Guangdong/1/1996-lineage H5N1 viruses during 2011 and 2012 (807 new sequences collected through December 31, 2012) was analyzed by phylogenetic and p-distance methods to define new clades using the pre-established nomenclature system. Eight new clade designations were recommended based on division of clade 1.1 (Mekong River Delta), (Indonesia), 2.2.2 (India/Bangladesh), (Egypt/Israel), and (Asia). A simplification to the previously defined criteria, which adds a letter rather than number to the right-most digit of fifth-order clades, was proposed to facilitate this and future updates.
    Influenza and Other Respiratory Viruses 01/2014; · 1.90 Impact Factor
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    ABSTRACT: H6 subtype influenza viruses are commonly isolated from wild aquatic birds. However, limited information is available regarding H6 influenza virus isolated from chickens. We compared the viral genome segment between A/chicken/Hong Kong/W312/97 (H6N1), which was able to grow in chicken trachea, and A/duck/Shantou/5540/01 (H6N2), which was isolated from wild aquatic duck, to explore the factors for effective replication in chicken. When chickens were inoculated with 7 + 1 reassortants (W312 background), the replication of viruses with PB2 and M genes derived from the duck strain was significantly reduced. Chimeras of PB2 and M proteins, encoding the C-terminal region of the PB2 protein and the M2 protein from W312, were required for efficient replication in canine-derived (MDCK) cells and in chicken trachea. These results indicate that host range may be determined by some types of internal proteins such as PB2 and M2, as well as by surface glycoprotein like hemagglutinin.
    Influenza research and treatment. 01/2014; 2014:547839.

Publication Stats

44k Citations
4,026.35 Total Impact Points


  • 1971–2014
    • St. Jude Children's Research Hospital
      • Department of Infectious Diseases
      Memphis, Tennessee, United States
  • 2013
    • United Arab Emirates University
      • Veterinary Research Laboratory
      Al ‘Ayn, Abu Zaby, United Arab Emirates
    • University of Oklahoma Health Sciences Center
      Oklahoma City, Oklahoma, United States
  • 2012–2013
    • Erasmus MC
      • Department of Virology
      Rotterdam, South Holland, Netherlands
    • The Scripps Research Institute
      La Jolla, California, United States
    • University of Georgia
      • Department of Population Health
      Athens, GA, United States
    • United States Geological Survey
      Reston, Virginia, United States
  • 2005–2013
    • Chungbuk National University
      • • Department of Microbiology
      • • College of Medicine and Medical Research Institute
      Tyundyu, North Chungcheong, South Korea
    • Centers for Disease Control and Prevention
      Atlanta, Michigan, United States
    • National Institute of Veterinary Research, Vietnam
      Hà Nội, Ha Nội, Vietnam
  • 1996–2013
    • The University of Hong Kong
      • • Centre of Influenza Research
      • • Department of Microbiology
      • • Li Ka Shing Faculty of Medicine
      Hong Kong, Hong Kong
  • 2010–2012
    • Mahidol University
      • Faculty of Veterinary Science
      Bangkok, Bangkok, Thailand
    • University of Alberta
      • Department of Biological Sciences
      Edmonton, Alberta, Canada
    • Korea Research Institute of Bioscience and Biotechnology KRIBB
      Anzan, Gyeonggi Province, South Korea
    • University of Bologna
      • School of Agriculture and Veterinary Medicine
      Bologna, Emilia-Romagna, Italy
  • 2003–2012
    • Shantou University
      • • International Institute of Infection and Immunity
      • • Department of Microbiology and Immunology
      Swatow, Guangdong, China
    • Chumakov Institute of Poliomyelitis and Viral Encephalitides
      Moskva, Moscow, Russia
  • 2002–2012
    • Ivanovsky Institute of Virology
      Moskva, Moscow, Russia
    • Philipps-Universität Marburg
      • Institut für Virologie
      Marburg, Hesse, Germany
  • 1993–2009
    • University of Tennessee
      • • Department of Pathology
      • • Division of Biostatistics and Epidemiology
      Knoxville, Tennessee, United States
    • Le ministère de l'Agriculture, des Pêcheries et de l'Alimentation du Québec
      Québec, Quebec, Canada
  • 2007
    • National Veterinary Research Quarantine Service
      Sŏul, Seoul, South Korea
  • 2006
    • University of Michigan
      • Department of Epidemiology
      Ann Arbor, Michigan, United States
  • 2004
    • Chungnam National University
      • College of Veterinary Medicine
      Seongnam, Gyeonggi, South Korea
    • Tai Lung Veterinary Laboratory
      Hong Kong, Hong Kong
  • 1997–2004
    • Istituto Superiore di Sanità
      Roma, Latium, Italy
  • 1980–2004
    • MRC National Institute for Medical Research
      Londinium, England, United Kingdom
  • 1966–2000
    • Australian National University
      Canberra, Australian Capital Territory, Australia
  • 1999
    • Emory University
      Atlanta, Georgia, United States
    • Queen Mary Hospital
      Hong Kong, Hong Kong
    • University of Wisconsin, Madison
      • Department of Pathobiological Sciences
      Mississippi, United States
  • 1998
    • University of Virginia
      • Division of Maternal Fetal Medicine
      Charlottesville, Virginia, United States
  • 1994–1998
    • Erasmus Universiteit Rotterdam
      • Department of Virology
      Rotterdam, South Holland, Netherlands
  • 1986–1998
    • Hokkaido University
      • • Laboratory of Microbiology
      • • Graduate School of Veterinary Medicine
      • • Laboratory of Radiation Biology
      Sapporo-shi, Hokkaido, Japan
  • 1992–1997
    • University of Massachusetts Medical School
      • Department of Pathology
      Worcester, MA, United States
  • 1990–1993
    • University of Otago
      • Virus Research Unit
      Taieri, Otago Region, New Zealand
  • 1991
    • University of Melbourne
      • Department of Microbiology and Immunology
      Melbourne, Victoria, Australia
  • 1985–1991
    • University of Alabama at Birmingham
      • Department of Microbiology
      Birmingham, AL, United States
  • 1988
    • University of Louisville
      • Department of Microbiology and Immunology
      Louisville, KY, United States
  • 1987
    • Georgia Poultry Laboratory Network
      Georgia, United States
  • 1981
    • University of Guelph
      Guelph, Ontario, Canada
  • 1972
    • National Institutes of Health
      Maryland, United States