A Single Residue Substitution in the Receptor-Binding Domain of H5N1 Hemagglutinin Is Critical for Packaging into Pseudotyped Lentiviral Particles

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

  Tang, Dong Jiang ^a,d   Lam, Yuen Man ^a   Siu, Yu Lam ^a   Lam, Chi Hong ^a   Chu, Shui Ling ^a   Peiris, J S Malik ^a   Buchy, Philippe ^b   Nal, Béatrice ^a,e   Bruzzone, Roberto ^a,c  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

^b INSTITUT PASTEUR DU CAMBODGE   (Cambodia)

^c INSTITUT PASTEUR   (France)

^d GUANGZHOU MEDICAL UNIVERSITY   (China)

^e BRUNEL UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84868332793     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0043596     Document Type: Article

References (43)

1. Kilpatrick AM, Chmura AA, Gibbons SW, Fleischer RC, Marra PP, et al. (2006) Predicting the global spread of H5N1 avian influenza. Proc Natl Acad Sci USA 103: 19368-19373.
2. Peiris JS, de Jong MD, Guan Y, (2007) Avian influenza virus (H5N1): a threat to human health. Clin Microbiol Rev 20: 243-267.
3. Webster RG, Govorkova EA, (2006) H5N1 influenza-continuing evolution and spread. N Engl J Med 355: 2174-2177.
4. WHO (2012) Available: http://www.who.int/en.
5. Chu VC, Whittaker GR, (2004) Influenza virus entry and infection require host cell N-linked glycoprotein. Proc Natl Acad Sci USA 101: 18153-18158.
6. Lakadamyali M, Rust MJ, Zhuang X, (2004) Endocytosis of influenza viruses. Microbes Infect 6: 929-936.
7. Suzuki Y, Ito T, Suzuki T, Holland RE Jr, Chambers TM, et al. (2000) Sialic acid species as a determinant of the host range of influenza A viruses. J Virol 74: 11825-11831.
8. Skehel JJ, Waterfield MD, (1975) Studies on the primary structure of the influenza virus hemagglutinin. Proc Natl Acad Sci USA 72: 93-97.
9. Horimoto T, Kawaoka Y, (1994) Reverse genetics provides direct evidence for a correlation of hemagglutinin cleavability and virulence of an avian influenza A virus. J Virol 68: 3120-3128.
10. Senne DA, Panigrahy B, Kawaoka Y, Pearson JE, Suss J, et al. (1996) Survey of the hemagglutinin (HA) cleavage site sequence of H5 and H7 avian influenza viruses: amino acid sequence at the HA cleavage site as a marker of pathogenicity potential. Avian Dis 40: 425-437.
11. Nayak DP, Hui EK, Barman S, (2004) Assembly and budding of influenza virus. Virus Res 106: 147-165.
12. Air GM, Laver WG, (1989) The neuraminidase of influenza virus. Proteins 6: 341-356.
13. Chen H, Smith GJD, Li KS, Wang J, Fan XH, et al. (2006) Establishment of multiple sublineages of H5N1 influenza virus in Asia: Implications for pandemic control. Proc Natl Acad Sci USA 103: 2845-2850.
14. WHO, OIE, FAO H5N1 Evolution Working Group (2008) Toward a unified nomenclature system for highly pathogenic avian influenza virus (H5N1). Emerg Infect Dis 14: e1 Available: http://wwwnc.cdc.gov/eid/article/14/7/07-1681_article.htm.
15. Writing Committee of the Second WHO Consultation on Clinical Aspects of Human Infection with Avian Influenza A (H5N1) Virus (2008) Abdel-Ghafar AN, Chotpitayasunondh T, Gao Z, Hayden FG, Nguyen DH, de Jong MD, et al. (2008) Update on avian influenza A (H5N1) virus infection in humans. N Engl J Med 358: 261-273.
16. Garcia JM, Lai JC, (2011) Production of influenza pseudotyped lentiviral particles and their use in influenza research and diagnosis: an update. Expert Rev Anti Infec Ther 9: 443-455.
17. McKay T, Patel M, Pickles RJ, Johnson LG, Olsen JC, (2006) Influenza M2 envelope protein augments avian influenza hemagglutinin pseudotyping of lentiviral vectors. Gene Ther 13: 715-724.
18. Nefkens I, Garcia JM, Ling LS, Lagarde N, Nicholls J, et al. (2007) Hemagglutinin pseudotyped lentiviral particles: characterization of a new method fo avian H5N1 influenza sero-diagnosis. J Clin Virol 36: 27-33.
19. Szecsi J, Boson B, Johnsson P, Dupeyrot-Lacas P, Matrosovich M, et al. (2006) Induction of neutralizing antibodies by virus-like particles harbouring surface proteins from highly pathogenic H5N1 and H7N1influenza viruses. Virol J 3: 70-79.
20. Tsai C, Caillet C, Hua H, Zhou F, Ding H, et al. (2009) Measurement of neutralizing antibody responses against H5N1 clades in immunized mice and ferrets using pseudotypes expressing influenza hemagglutinin and neuraminidase. Vaccine 27: 6777-6790.
21. Wang SY, Su CY, Lin M, Huang SY, Huang WYI, et al. (2009) HA-pseudotyped retroviral vectors for influenza antagonist screening. J Biomol Screen 14: 294-302.
22. Dung Nuyen T, Vinh Nguyen T, Vijaykrishna D, Webster RG, Guan Y, et al. (2008) Multiple sublineages of influenza A virus (H5N1), Vietnam, 2005-2007. Emerg Infect Dis 14: 632-636.
23. Klenk HD, Garten W, (1994) Host cell proteases controlling virus pathogenicity. Trends Microbiol 2: 39-43.
24. Steinhauer DA, (1999) Role of hemagglutinin cleavage for the pathogenicity of influenza virus. Virology 258: 1-20.
25. Barman S, Ali A, Hui EK, Adhikary L, Nayak DP, (2001) Transport of viral proteins to the apical membranes and interaction of matrix protein with glycoproteins in the assembly of influenza virus. Virus Res 77: 61-69.
26. Matrosovich M, Matrosovich T, Carr J, Roberts NA, Klenk HD, (2003) Overexpression of the a-2,6-sialyltransferase in MDCK cells increases influenza virus sensitivity to neuraminidase inhibitors. J Virol 77: 8418-8425.
27. Benaroch P, Billard E, Gaudin R, Schindler M, Jouve M, (2010) HIV-1 assembly in macrophages. Retrovirology 7: 29.
28. Houzet L, Gay B, Morichaud Z, Briant L, Mougel M, (2006) Intracellular assembly and budding of the Murine Leukemia Virus in infected cells. Retrovirology 3: 12.
29. Deutscher SL, Nuwayhid N, Stanley P, Briles EI, Hirschberg CB, (1984) Translocation across Golgi vesicle membranes: A CHO glycosylation mutant deficient in CMP-sialic acid transport. Cell 39: 295-299.
30. Naughtin M, Dyason JC, Mardy S, Sorn S, Itzstein M, et al. (2011) Neuraminidase inhibitor sensitivity and receptor-binding specificity of Cambodian Clade 1 highly pathogenic H5N1 influenza virus. Antimicrob Agents Chemother 55: 2004-2010.
31. Ao Z, Patel A, Tran K, Fowke K, Coombs K, et al. (2008) Characterization of a trypsin-dependent avian influenza H5N1-pseudotyped HIV vector system for high throughput screening of inhibitory molecules. Antiviral Res 79: 12-18.
32. Labrosse B, Tourdjman M, Porcher R, LeGoff J, de Lamballerie X, et al. (2010) Detection of extensive cross-neutralization between pandemic and seasonal A/H1N1 influenza viruses using a pseudotype neutralization assay. PLoS One 5: e11036.
33. Bosch V, Kramer B, Pfeiffer T, Starch L, Steinhauer DA, (2001) Inhibition of release of lentivirus particles with incorporated human influenza virus haemagglutinin by binding to sialic acid-containing cellular receptors. J Gen Virol 82: 2485-2494.
34. Yamada S, Suzuki Y, Suzuki T, Le MQ, Nidom CA, et al. (2006) Haemagglutinin mutations responsible for the binding of H5N1 influenza A viruses to human-type receptors. Nature 444: 378-382.
35. Auewarakul P, Suptawiwat O, Kongchanagul A, Sangma C, Suzuki Y, et al. (2007) An avian influenza H5N1 virus that binds to a human-type receptor. J Virol 81: 9950-9955.
36. Imai H, Shinya K, Takano R, Kiso M, Muramoto Y, et al. (2010) The HA and NS genes of human H5N1 influenza A Virus contribute to high virulence in ferrets. PLoS Pathog 6: 1-13.
37. Kayali G, Setterquist SF, Capuano AW, Myers KP, Gill JS, et al. (1999) Testing human sera for antibodies against avian influenza viruses: horse RBC hemagglutination inhibition vs. microneutralization assays. J Clin Virol 43: 73-78.
38. Rowe T, Abernathy RA, Hu-Primmer J, Thompson WW, Lu X, et al. (1999) Detection of antibody to avian influenza A (H5N1) virus inhuman serum by using a combination of serologic assays. J Clin Microbiol 37: 937-943.
39. Garcia JM, Lagarde N, Ma ES, de Jong MD, Peiris JS, (2010) Optimization and evaluation of an influenza A (H5) pseudotyped lentiviral particles-based serological assay. J Clin Virol 47: 29-33.
40. Sandbulte MR, Jimenez GS, Boon AC, Smith LR, Treanor JJ, et al. (2007) Cross-reactive neuraminidase antibodies afford partial protection against H5N1 in mice and are present in unexposed humans. PLoS Med 4: e59.
41. Moore JM, Dorfman T, Li W, Wong SK, Li Y, et al. (2004) Retroviruses pseudotyped with the severe acute respiratory syndrome coronavirus spike protein efficiently infect cells expressing angiotensin-converting enzyme 2. J Virol 78: 10628-10635.
42. de Vries RP, de Vries E, Bosch BJ, de Groot RJ, Rottier PJ, et al. (2010) The influenza A virus hemagglutinin glycosylation state affects receptor-binding specificity. Virology 403: 17-25.
43. WHO (2011) Manual for the laboratory diagnosis and virological surveillance of influenza. Available: http://whqlibdoc.who.int/publications/2011/9789241548090_eng.pdf.