Suboptimal Humoral Immune Response against Influenza A(H7N9) Virus Is Related to Its Internal Genes

Clinical and Vaccine Immunology

Volumn 22, Issue 12, 2015, Pages 1235-1243

  Lee, Andrew C Y ^a   Zhu, Houshun ^a   Zhang, Anna J X ^a   Li, Can ^b   Wang, Pui ^b   Li, Chuangen ^a   Chen, Honglin ^a   Hung, Ivan F N ^c   To, Kelvin K W ^c   Yuen, Kwok Yung ^a  

^a Department of Microbiology ^*  (Hong Kong)

^b THE UNIVERSITY OF HONG KONG   (Hong Kong)

^c UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANTIBODY BLOOD LEVEL; ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; CONTROLLED STUDY; EMBRYO; FEMALE; HEMAGGLUTINATION INHIBITION; HUMORAL IMMUNITY; INFLUENZA A VIRUS (H7N9); MICRONEUTRALIZATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; VIRUS NEUTRALIZATION; VIRUS VIRULENCE; ANIMAL; BLOOD; CROSS PROTECTION; GENETICS; HEMAGGLUTINATION INHIBITION TEST; HUMAN; IMMUNOLOGY; INFLUENZA; INFLUENZA A VIRUS (H1N1); ORTHOMYXOVIRUS INFECTION; PATHOGENICITY; VIROLOGY; VIRUS GENE;

MATRIX PROTEIN; NEUTRALIZING ANTIBODY; VIRUS ANTIBODY;

ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; CROSS PROTECTION; GENES, VIRAL; HEMAGGLUTINATION INHIBITION TESTS; HUMANS; IMMUNITY, HUMORAL; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA A VIRUS, H7N9 SUBTYPE; INFLUENZA, HUMAN; MICE; ORTHOMYXOVIRIDAE INFECTIONS; VIRAL MATRIX PROTEINS;

EID: 84948161300     PISSN: 15566811     EISSN: 1556679X     Source Type: Journal    
DOI: 10.1128/CVI.00443-15     Document Type: Article

References (35)

1. To KK, Chan JF, Yuen KY. 2014. Viral lung infections: epidemiology, virology, clinical features, and management of avian influenza A(H7N9). Curr Opin Pulm Med 20:225-232. http://dx.doi.org/10.1097/MCP .0000000000000047.
2. 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. http://dx.doi.org/10.1093/cid/cit541.
3. 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. http://dx.doi.org/10.1016/S1473-3099(13)70167-1.
4. 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. http://dx.doi.org/10.1016/S0140-6736(13)60903-4.
5. To KKW, Ng KHL, Que TL, Chan JMC, Tsang KY, Tsang AKL, Chen H, Yuen K-Y. 2012. Avian influenza A H5N1 virus: a continuous threat to humans. Emerg Microbes Infect 1:e25. http://dx.doi.org/10.1038/emi .2012.24.
6. World Health Organization. 2015. Influenza at the human-Animal interface. Summary and assessment as of 17 July 2015. World Health Organization, Geneva, Switzerland. http://www.who.int/influenza/human-Animal-interface/Influenza-Summary-IRA-HA-interface-17-July-2015.pdf?ua-1.
7. Morrison J, Josset L, Tchitchek N, Chang J, Belser JA, Swayne DE, Pantin-Jackwood MJ, Tumpey TM, Katze MG. 2014. H7N9 and other pathogenic avian influenza viruses elicit a three-pronged transcriptomic signature that is reminiscent of 1918 influenza virus and is associated with lethal outcome in mice. J Virol 88:10556-10568. http://dx.doi.org/10.1128/JVI.00570-14.
8. Watanabe T, Kiso M, Fukuyama S, Nakajima N, Imai M, Yamada S, Murakami S, Yamayoshi S, Iwatsuki-Horimoto K, Sakoda Y, Takashita E, McBride R, Noda T, Hatta M, Imai H, Zhao D, Kishida N, Shirakura M, de Vries RP, Shichinohe S, Okamatsu M, Tamura T, Tomita Y, Fujimoto N, Goto K, Katsura H, Kawakami E, Ishikawa I, Watanabe S, Ito M, Sakai-Tagawa Y, Sugita Y, Uraki R, Yamaji R, Eisfeld AJ, Zhong G, Fan S, Ping J, Maher EA, Hanson A, Uchida Y, Saito T, Ozawa M, Neumann G, Kida H, Odagiri T, Paulson JC, Hasegawa H, Tashiro M, Kawaoka Y. 2013. Characterization of H7N9 influenza A viruses isolated from humans. Nature 501:551-555. http://dx.doi.org/10.1038/nature12392.
9. Bi Y, Xie Q, Zhang S, Li Y, Xiao H, Jin T, Zheng W, Li J, Jia X, Sun L, Liu J, Qin C, Gao GF, Liu W. 2015. Assessment of the internal genes of influenza A (H7N9) virus contributing to high pathogenicity in mice. J Virol 89:2-13. http://dx.doi.org/10.1128/JVI.02390-14.
10. De Groot AS, Ardito M, Terry F, Levitz L, Ross T, Moise L, Martin W. 2013. Low immunogenicity predicted for emerging avian-origin H7N9: implication for influenza vaccine design. Hum Vaccin Immunother 9:950-956. http://dx.doi.org/10.4161/hv.24939.
11. De Groot AS, Moise L, Liu R, Gutierrez AH, Terry F, Koita OA, Ross TM, Martin W. 2014. Cross-conservation of T-cell epitopes: now even more relevant to (H7N9) influenza vaccine design. Hum Vaccin Immunother 10:256-262. http://dx.doi.org/10.4161/hv.28135.
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. http://dx.doi.org/10.1056/NEJMoa1304459.
13. Zheng B, Chan KH, Zhang AJ, Zhou J, Chan CC, Poon VK, Zhang K, Leung VH, Jin DY, Woo PC, Chan JF, To KK, Chen H, Yuen KY. 2010. D225G mutation in hemagglutinin of pandemic influenza H1N1 (2009) virus enhances virulence in mice. Exp Biol Med (Maywood) 235:981-988. http://dx.doi.org/10.1258/ebm.2010.010071.
14. To KK, Zhang AJ, Chan AS, Li C, Cai JP, Lau CC, Li CG, Jahan AS, Wu WL, Li L, Tsang AK, Chan KH, Chen H, Yuen KY. 2015. Recombinant influenza A virus hemagglutinin HA2 subunit protects mice against influenza A(H7N9) virus infection. Arch Virol 160:777-786. http://dx.doi.org/10.1007/s00705-014-2314-x.
15. Song W, Wang P, Mok BW, Lau SY, Huang X, Wu WL, Zheng M, Wen X, Yang S, Chen Y, Li L, Yuen KY, Chen H. 2014. The K526R substitution in viral protein PB2 enhances the effects of E627K on influenza virus replication. Nat Commun 5:5509. http://dx.doi.org/10.1038/ncomms6509.
16. Li C, Li C, Zhang AJ, To KK, Lee AC, Zhu H, Wu HW, Chan JF, Chen H, Hung IF, Li L, Yuen KY. 2014. Avian influenza A H7N9 virus induces severe pneumonia in mice without prior adaptation and responds to a combination of zanamivir and COX-2 inhibitor. PLoS One 9:e107966. http://dx.doi.org/10.1371/journal.pone.0107966.
17. Weldon WC, Zarnitsyn VG, Esser ES, Taherbhai MT, Koutsonanos DG, Vassilieva EV, Skountzou I, Prausnitz MR, Compans RW. 2012. Effect of adjuvants on responses to skin immunization by microneedles coated with influenza subunit vaccine. PLoS One 7:e41501. http://dx.doi.org/10.1371/journal.pone.0041501.
18. Chan KH, To KKW, Hung IFN, Zhang AJX, Chan JFW, Cheng VCC, Tse H, Che XY, Chen HL, 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. http://dx.doi.org/10.1128/CVI.00555-10.
19. Guo L, Zhang X, Ren L, Yu X, Chen L, Zhou H, Gao X, Teng Z, Li J, Hu J, Wu C, Xiao X, Zhu Y, Wang Q, Pang X, Jin Q, Wu F, Wang J. 2014. Human antibody responses to avian influenza A(H7N9) virus, 2013. Emerg Infect Dis 20:192-200. http://dx.doi.org/10.3201/eid2002.131094.
20. Buchy P, Vong S, Chu S, Garcia JM, Hien TT, Hien VM, Channa M, Ha do Q, Chau QNV, Simmons C, Farrar JJ, Peiris M, de Jong MD. 2010. Kinetics of neutralizing antibodies in patients naturally infected by H5N1 virus. PLoS One 5:e10864. http://dx.doi.org/10.1371/journal.pone.0010864.
21. Xu L, Bao L, Deng W, Zhu H, Chen T, Lv Q, Li F, Yuan J, Xiang Z, Gao K, Xu Y, Huang L, Li Y, Liu J, Yao Y, Yu P, Yong W, Wei Q, Zhang L, Qin C. 2013. The mouse and ferret models for studying the novel avianorigin human influenza A (H7N9) virus. Virol J 10:253. http://dx.doi.org/10.1186/1743-422X-10-253.
22. Steel J, Lowen AC, Pena L, Angel M, Solorzano A, Albrecht R, Perez DR, Garcia-Sastre A, Palese P. 2009. Live attenuated influenza viruses containing NS1 truncations as vaccine candidates against H5N1 highly pathogenic avian influenza. J Virol 83:1742-1753. http://dx.doi.org/10.1128/JVI.01920-08.
23. Mssler C, Groiss F, Wolzt M, Wolschek M, Seipelt J, Muster T. 2013. Phase I/II trial of a replication-deficient trivalent influenza virus vaccine lacking NS1. Vaccine 31:6194-6200. http://dx.doi.org/10.1016/j.vaccine.2013.10.061.
24. Richt JA, Garca-Sastre A. 2009. Attenuated influenza virus vaccines with modified NS1 proteins. Curr Top Microbiol Immunol 333:177-195.
25. Ayllon J, Garca-Sastre A. 2015. The NS1 protein: a multitasking virulence factor. Curr Top Microbiol Immunol 386:73-107.
26. Hung IF, To KK, Lee CK, Lee KL, Chan K, Yan WW, Liu R, Watt CL, Chan WM, Lai KY, Koo CK, Buckley T, Chow FL, Wong KK, Chan HS, Ching CK, Tang BS, Lau CC, Li IW, Liu SH, Chan KH, Lin CK, Yuen KY. 2011. Convalescent plasma treatment reduced mortality in patients with severe pandemic influenzaA(H1N1) 2009 virus infection. Clin Infect Dis 52:447-456. http://dx.doi.org/10.1093/cid/ciq106.
27. Hung IF, To KK, Lee CK, Lee KL, Yan WW, Chan K, Chan WM, Ngai CW, Law KI, Chow FL, Liu R, Lai KY, Lau CC, Liu SH, Chan KH, Lin CK, Yuen KY. 2013. Hyperimmune IV immunoglobulin treatment: a multicenter double-blind randomized controlled trial for patients with severe 2009 influenza A(H1N1) infection. Chest 144:464-473. http://dx.doi.org/10.1378/chest.12-2907.
28. Liu YV, Massare MJ, Pearce MB, Sun X, Belser JA, Maines TR, Creager HM, Glenn GM, Pushko P, Smith GE, Tumpey TM. 2015. Recombinant virus-like particles elicit protective immunity against avian influenza A(H7N9) virus infection in ferrets. Vaccine 33:2152-2158. http://dx.doi.org/10.1016/j.vaccine.2015.03.009.
29. Smith GE, Flyer DC, Raghunandan R, Liu Y, Wei Z, Wu Y, Kpamegan E, Courbron D, Fries LF,, Glenn GM. 2013. Development of influenza H7N9 virus like particle (VLP) vaccine: homologous A/Anhui/1/2013 (H7N9) protection and heterologous A/chicken/Jalisco/CPA1/2012 (H7N3) cross-protection in vaccinated mice challenged with H7N9 virus. Vaccine 31:4305-4313. http://dx.doi.org/10.1016/j.vaccine.2013.07.043.
30. Bart SA, Hohenboken M, Della Cioppa G, Narasimhan V, Dormitzer PR, Kanesa-Thasan N. 2014. A cell culture-derived MF59-Adjuvanted pandemic A/H7N9 vaccine is immunogenic in adults. Sci Transl Med 6:234ra255.
31. Fries LF, Smith GE, Glenn GM. 2013. A recombinant viruslike particle influenza A (H7N9) vaccine. N Engl J Med 369:2564-2566. http://dx.doi.org/10.1056/NEJMc1313186.
32. Mulligan MJ, Bernstein DI, Winokur P, Rupp R, Anderson E, Rouphael N, Dickey M, Stapleton JT, Edupuganti S, Spearman P, Ince D, Noah DL, Hill H, Bellamy AR, DMID 13-0032 H7N9 Vaccine Study Group. 2014. Serological responses to an avian influenza A/H7N9 vaccine mixed at the point-of-use with MF59 adjuvant: a randomized clinical trial. JAMA 312:1409-1419. http://dx.doi.org/10.1001/jama.2014.12854.
33. Chia MY, Hu AY, Tseng YF, Weng TC, Lai CC, Lin JY, Chen PL, Wang YF, Chao SR, Chang JY, Hwang YS, Yeh CT, Yu CP, Chen YC, Su IJ, Lee MS. 2015. Evaluation of MDCK cell-derived influenza H7N9 vaccine candidates in ferrets. PLoS One 10:e0120793. http://dx.doi.org/10.1371/journal.pone.0120793.
34. 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. http://dx.doi.org/10.1128/CVI .00816-13.
35. 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 59:1246-1255. http://dx.doi.org/10.1093/cid/ciu582.