Recombinant influenza A virus hemagglutinin HA2 subunit protects mice against influenza A(H7N9) virus infection

Archives of Virology

Volumn 160, Issue 3, 2015, Pages 777-786

  To, Kelvin K W ^a,b   Zhang, Anna J X ^a,b   Chan, Andy S F ^b   Li, Can ^b   Cai, Jian Piao ^b   Lau, Candy C Y ^b   Li, Chuan Gen ^b   Jahan, Akhee S ^b   Wu, Wai Lan ^b   Li, Lanjuan ^c,d   Tsang, Alan Ka Lun ^b   Chan, Kwok Hung ^b   Chen, Honglin ^a,b,c   Yuen, Kwok Yung ^a,b,c  

^a THE UNIVERSITY OF HONG KONG   (Hong Kong)

^b UNIVERSITY OF HONG KONG   (Hong Kong)

^c ZHEJIANG UNIVERSITY   (China)

^d ZHEJIANG UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AMINOQUINOLINE DERIVATIVE; IMIQUIMOD; IMMUNOGLOBULIN G; IMMUNOLOGICAL ADJUVANT; INFLUENZA VACCINE; INFLUENZA VIRUS HEMAGGLUTININ; NEUTRALIZING ANTIBODY; PROTEIN SUBUNIT; RECOMBINANT PROTEIN; RECOMBINANT VACCINE; SUBUNIT VACCINE; VIRUS ANTIBODY;

ANIMAL; BAGG ALBINO MOUSE; BLOOD; DISEASE MODEL; ESCHERICHIA COLI; GENE EXPRESSION; GENETICS; HEMAGGLUTINATION INHIBITION TEST; IMMUNOLOGY; INFLUENZA VIRUS A H7N9; INTRAPERITONEAL DRUG ADMINISTRATION; ORTHOMYXOVIRIDAE INFECTIONS; PROCEDURES; PROTEIN SUBUNIT; SERODIAGNOSIS; SURVIVAL; VACCINATION;

ADJUVANTS, IMMUNOLOGIC; AMINOQUINOLINES; ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; DISEASE MODELS, ANIMAL; ESCHERICHIA COLI; GENE EXPRESSION; HEMAGGLUTINATION INHIBITION TESTS; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; IMMUNOGLOBULIN G; INFLUENZA A VIRUS, H7N9 SUBTYPE; INFLUENZA VACCINES; INJECTIONS, INTRAPERITONEAL; MICE, INBRED BALB C; NEUTRALIZATION TESTS; ORTHOMYXOVIRIDAE INFECTIONS; PROTEIN SUBUNITS; RECOMBINANT PROTEINS; SURVIVAL ANALYSIS; VACCINATION; VACCINES, SUBUNIT; VACCINES, SYNTHETIC;

EID: 84925539772     PISSN: 03048608     EISSN: 14328798     Source Type: Journal    
DOI: 10.1007/s00705-014-2314-x     Document Type: Article

References (41)

1. Bommakanti G, Citron MP, Hepler RW, Callahan C, Heidecker GJ, Najar TA, Lu X, Joyce JG, Shiver JW, Casimiro DR, ter Meulen J, Liang X, Varadarajan R (2010) Design of an HA2-based Escherichia coli expressed influenza immunogen that protects mice from pathogenic challenge. Proc Natl Acad Sci USA 107:13701–13706
2. Chan KH, To KK, Hung IF, Zhang AJ, Chan JF, Cheng VC, Tse H, Che XY, Chen H, Yuen KY (2011) Differences in antibody responses of individuals with natural infection and those vaccinated against pandemic H1N1 2009 influenza. Clin Vaccine Immunol 18:867–873
3. Chan KH, Chan JF, Tse H, Chen H, Lau CC, Cai JP, Tsang AK, Xiao X, To KK, Lau SK, Woo PC, Zheng BJ, Wang M, Yuen KY (2013) Cross-reactive antibodies in convalescent SARS patients’ sera against the emerging novel human coronavirus EMC (2012) by both immunofluorescent and neutralizing antibody tests. J Infect 67:130–140
4. Chan KH, To KK, Chan JF, Li CP, Chen H, Yuen KY (2013) Analytical sensitivity of seven point-of-care influenza virus detection tests and two molecular tests for detection of avian origin H7N9 and swine origin H3N2 variant influenza A viruses. J Clin Microbiol 51:3160–3161
5. Chen Y, Liang W, Yang S, Wu N, Gao H, Sheng J, Yao H, Wo J, Fang Q, Cui D, Li Y, Yao X, Zhang Y, Wu H, Zheng S, Diao H, Xia S, Zhang Y, Chan KH, Tsoi HW, Teng JL, Song W, Wang P, Lau SY, Zheng M, Chan JF, To KK, Chen H, Li L, Yuen KY (2013) Human infections with the emerging avian influenza A H7N9 virus from wet market poultry: clinical analysis and characterisation of viral genome. Lancet 381:1916–1925
6. Cheng VC, To KK, Tse H, Hung IF, Yuen KY (2012) Two years after pandemic influenza A/2009/H1N1: what have we learned? Clin Microbiol Rev 25:223–263
7. DiLillo DJ, Tan GS, Palese P, Ravetch JV (2014) Broadly neutralizing hemagglutinin stalk-specific antibodies require FcgammaR interactions for protection against influenza virus in vivo. Nat Med 20:143–151
8. Ekiert DC, Bhabha G, Elsliger MA, Friesen RH, Jongeneelen M, Throsby M, Goudsmit J, Wilson IA (2009) Antibody recognition of a highly conserved influenza virus epitope. Science 324:246–251
9. Ekiert DC, Friesen RH, Bhabha G, Kwaks T, Jongeneelen M, Yu W, Ophorst C, Cox F, Korse HJ, Brandenburg B, Vogels R, Brakenhoff JP, Kompier R, Koldijk MH, Cornelissen LA, Poon LL, Peiris M, Koudstaal W, Wilson IA, Goudsmit J (2011) A highly conserved neutralizing epitope on group 2 influenza A viruses. Science 333:843–850
10. El Bakkouri K, Descamps F, De Filette M, Smet A, Festjens E, Birkett A, Van Rooijen N, Verbeek S, Fiers W, Saelens X (2011) Universal vaccine based on ectodomain of matrix protein 2 of influenza A: Fc receptors and alveolar macrophages mediate protection. J Immunol 186:1022–1031
11. Gao HN, Lu HZ, Cao B, Du B, Shang H, Gan JH, Lu SH, Yang YD, Fang Q, Shen YZ, Xi XM, Gu Q, Zhou XM, Qu HP, Yan Z, Li FM, Zhao W, Gao ZC, Wang GF, Ruan LX, Wang WH, Ye J, Cao HF, Li XW, Zhang WH, Fang XC, He J, Liang WF, Xie J, Zeng M, Wu XZ, Li J, Xia Q, Jin ZC, Chen Q, Tang C, Zhang ZY, Hou BM, Feng ZX, Sheng JF, Zhong NS, Li LJ (2013) Clinical findings in 111 cases of influenza A (H7N9) virus infection. N Engl J Med 368:2277–2285
12. Gao R, Cao B, Hu Y, Feng Z, Wang D, Hu W, Chen J, Jie Z, Qiu H, Xu K, Xu X, Lu H, Zhu W, Gao Z, Xiang N, Shen Y, He Z, Gu Y, Zhang Z, Yang Y, Zhao X, Zhou L, Li X, Zou S, Zhang Y, Li X, Yang L, Guo J, Dong J, Li Q, Dong L, Zhu Y, Bai T, Wang S, Hao P, Yang W, Zhang Y, Han J, Yu H, Li D, Gao GF, Wu G, Wang Y, Yuan Z, Shu Y (2013) Human infection with a novel avian-origin influenza A (H7N9) virus. N Engl J Med 368:1888–1897
13. Gocnik M, Fislova T, Mucha V, Sladkova T, Russ G, Kostolansky F, Vareckova E (2008) Antibodies induced by the HA2 glycopolypeptide of influenza virus haemagglutinin improve recovery from influenza A virus infection. J Gen Virol 89:958–967
14. Gomez Lorenzo MM, Fenton MJ (2013) Immunobiology of influenza vaccines. Chest 143:502–510
15. Hung IF, Levin Y, To KK, Chan KH, Zhang AJ, Li P, Li C, Xu T, Wong TY, Yuen KY (2012) Dose sparing intradermal trivalent influenza (2010/2011) vaccination overcomes reduced immunogenicity of the 2009 H1N1 strain. Vaccine 30:6427–6435
16. Hung IF, Zhang AJ, To KK, Chan JF, Li C, Zhu HS, Li P, Li C, Chan TC, Cheng VC, Chan KH, Yuen KY (2014) Immunogenicity of intradermal trivalent influenza vaccine with topical Imiquimod, a double blind randomized controlled trial. Clin Infect Dis. doi:10.1093/cid/ciu582
17. Janulikova J, Stanekova Z, Mucha V, Kostolansky F, Vareckova E (2012) Two distinct regions of HA2 glycopolypeptide of influenza virus hemagglutinin elicit cross-protective immunity against influenza. Acta Virol 56:169–176
18. Kawai T, Akira S (2010) The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol 11:373–384
19. Khurana S, Loving CL, Manischewitz J, King LR, Gauger PC, Henningson J, Vincent AL, Golding H (2013) Vaccine-induced anti-HA2 antibodies promote virus fusion and enhance influenza virus respiratory disease. Sci Transl Med 5:200ra114
20. Mallajosyula VV, Citron M, Ferrara F, Lu X, Callahan C, Heidecker GJ, Sarma SP, Flynn JA, Temperton NJ, Liang X, Varadarajan R (2014) Influenza hemagglutinin stem-fragment immunogen elicits broadly neutralizing antibodies and confers heterologous protection. Proc Natl Acad Sci USA 111:E2514–E2523
21. Manicassamy B, Medina RA, Hai R, Tsibane T, Stertz S, Nistal-Villan E, Palese P, Basler CF, Garcia-Sastre A (2010) Protection of mice against lethal challenge with 2009 H1N1 influenza A virus by 1918-like and classical swine H1N1 based vaccines. PLoS Pathog 6:e1000745
22. Margine I, Krammer F, Hai R, Heaton NS, Tan GS, Andrews SA, Runstadler JA, Wilson PC, Albrecht RA, Garcia-Sastre A, Palese P (2013) Hemagglutinin stalk-based universal vaccine constructs protect against group 2 influenza A viruses. J Virol 87:10435–10446
23. Neirynck S, Deroo T, Saelens X, Vanlandschoot P, Jou WM, Fiers W (1999) A universal influenza A vaccine based on the extracellular domain of the M2 protein. Nat Med 5:1157–1163
24. Richard M, Schrauwen EJ, de Graaf M, Bestebroer TM, Spronken MI, van Boheemen S, de Meulder D, Lexmond P, Linster M, Herfst S, Smith DJ, van den Brand JM, Burke DF, Kuiken T, Rimmelzwaan GF, Osterhaus AD, Fouchier RA (2013) Limited airborne transmission of H7N9 influenza A virus between ferrets. Nature 501:560–563
25. Schneemann A, Speir JA, Tan GS, Khayat R, Ekiert DC, Matsuoka Y, Wilson IA (2012) A virus-like particle that elicits cross-reactive antibodies to the conserved stem of influenza virus hemagglutinin. J Virol 86:11686–11697
26. Stanekova Z, Adkins I, Kosova M, Janulikova J, Sebo P, Vareckova E (2013) Heterosubtypic protection against influenza A induced by adenylate cyclase toxoids delivering conserved HA2 subunit of hemagglutinin. Antiviral Res 97:24–35
27. Steel J, Lowen AC, Wang TT, Yondola M, Gao Q, Haye K, Garcia-Sastre A, Palese P (2010) Influenza virus vaccine based on the conserved hemagglutinin stalk domain. mBio. doi:10.1128/mBio.00018-10
28. Tan GS, Krammer F, Eggink D, Kongchanagul A, Moran TM, Palese P (2012) A pan-H1 anti-hemagglutinin monoclonal antibody with potent broad-spectrum efficacy in vivo. J Virol 86:6179–6188
29. To KK, Zhang AJ, Hung IF, Xu T, Ip WC, Wong RT, Ng JC, Chan JF, Chan KH, Yuen KY (2012) High titer and avidity of nonneutralizing antibodies against influenza vaccine antigen are associated with severe influenza. Clin Vaccine Immunol 19:1012–1018
30. To KK, Chan JF, Chen H, Li L, Yuen KY (2013) The emergence of influenza A H7N9 in human beings 16 years after influenza A H5N1: a tale of two cities. Lancet Infect Dis 13:809–821
31. To KK, Song W, Lau SY, Que TL, Lung DC, Hung IF, Chen H, Yuen KY (2014) Unique reassortant of influenza A(H7N9) virus associated with severe disease emerging in Hong Kong. J Infect 69:60–68
32. Wong SS, Yuen KY (2005) Influenza vaccination: options and issues. Hong Kong Med J 11:381–390
33. Woo PC, Lau SK, Tsoi HW, Chen ZW, Wong BH, Zhang L, Chan JK, Wong LP, He W, Ma C, Chan KH, Ho DD, Yuen KY (2005) SARS coronavirus spike polypeptide DNA vaccine priming with recombinant spike polypeptide from Escherichia coli as booster induces high titer of neutralizing antibody against SARS coronavirus. Vaccine 23:4959–4968
34. World Health Organization Influenza at the human-animal interface. Summary and assessment as of 4 July 2013. Available at http://www.who.int/influenza/human_animal_interface/Influenza_Summary_IRA_HA_interface_03July13.pdf. Accessed on 15 Aug 2013
35. Yang S, Chen Y, Cui D, Yao H, Lou J, Huo Z, Xie G, Yu F, Zheng S, Yang Y, Zhu Y, Lu X, Liu X, Lau SY, Chan JF, To KK, Yuen KY, Chen H, Li L (2014) Avian-origin influenza A(H7N9) infection in influenza A(H7N9)-affected areas of China: a serological study. J Infect Dis 209:265–269
36. Yu L, Wang Z, Chen Y, Ding W, Jia H, Chan JF, To KK, Chen H, Yang Y, Liang W, Zheng S, Yao H, Yang S, Cao H, Dai X, Zhao H, Li J, Bao Q, Chen P, Hou X, Li L, Yuen KY (2013) Clinical, virological, and histopathological manifestations of fatal human infections by avian influenza A(H7N9) virus. Clin Infect Dis 57:1449–1457
37. Zhang AJ, To KK, Tse H, Chan KH, Guo KY, Li C, Hung IF, Chan JF, Chen H, Tam S, Yuen KY (2011) High incidence of severe influenza among individuals over 50 years of age. Clin Vaccine Immunol 18:1918–1924
38. Zhang AJ, To KK, Li C, Lau CC, Poon VK, Chan CC, Zheng BJ, Hung IF, Lam KS, Xu A, Yuen KY (2013) Leptin mediates the pathogenesis of severe 2009 pandemic influenza A(H1N1) infection associated with cytokine dysregulation in mice with diet-induced obesity. J Infect Dis 207:1270–1280
39. Zhang AJ, Li C, To KK, Zhu HS, Lee AC, Li CG, Chan JF, Hung IF, Yuen KY (2014) Toll-like receptor 7 agonist Imiquimod in combination with influenza vaccine expedites and augments humoral immune responses against influenza A(H1N1)pdm09 virus infection in BALB/c mice. Clin Vaccine Immunol 21:570–579
40. Zhang Q, Shi J, Deng G, Guo J, Zeng X, He X, Kong H, Gu C, Li X, Liu J, Wang G, Chen Y, Liu L, Liang L, Li Y, Fan J, Wang J, Li W, Guan L, Li Q, Yang H, Chen P, Jiang L, Guan Y, Xin X, Jiang Y, Tian G, Wang X, Qiao C, Li C, Bu Z, Chen H (2013) H7N9 influenza viruses are transmissible in ferrets by respiratory droplet. Science 341:410–414
41. Zheng BJ, Chan KW, Lin YP, Zhao GY, Chan C, Zhang HJ, Chen HL, Wong SS, Lau SK, Woo PC, Chan KH, Jin DY, Yuen KY (2008) Delayed antiviral plus immunomodulator treatment still reduces mortality in mice infected by high inoculum of influenza A/H5N1 virus. Proc Natl Acad Sci USA 105:8091–8096