Novel avian-origin influenza A (H7N9) virus attachment to the respiratory tract of five animal models

Journal of Virology

Volumn 88, Issue 8, 2014, Pages 4595-4599

  Siegers, Jurre Y ^a   Short, Kirsty R ^a   Leijten, Lonneke M E ^a   de Graaf, Miranda ^a   Spronken, Monique I J ^a   Schrauwen, Eefje J A ^a   Marshall, Nicolle ^b   Lowen, Anice C ^b   Gabriel, Gülsah ^c   Osterhaus, Albert D M E ^a   Kuiken, Thijs ^a   van Riel, Debby ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c LEIBNIZ INSTITUTE FOR EXPERIMENTAL VIROLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AVIAN INFLUENZA VIRUS; C57BL 6 MOUSE; COMPARATIVE STUDY; CONTROLLED STUDY; DISEASE MODEL; FERRET; GUINEA PIG; HUMAN; INFLUENZA A; INFLUENZA VIRUS A H1N1; INFLUENZA VIRUS A H3N2; INFLUENZA VIRUS A H5N1; INFLUENZA VIRUS A H7N7; INFLUENZA VIRUS A H7N9; MACACA; MOUSE; NONHUMAN; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL (TOPIC); SWINE; TISSUE DISTRIBUTION; VIRUS ATTACHMENT; VIRUS PATHOGENESIS; VIRUS STRAIN;

ANIMALS; CHINA; DISEASE MODELS, ANIMAL; FEMALE; FERRETS; GUINEA PIGS; HUMANS; INFLUENZA A VIRUS, H7N9 SUBTYPE; INFLUENZA, HUMAN; MACACA; MALE; MICE; RESPIRATORY SYSTEM; SWINE; VIRUS ATTACHMENT;

EID: 84896963937     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03190-13     Document Type: Article

References (34)

1. 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 influenzaA(H7N9) virus. N. Engl. J. Med. 368:1888-1897. http://dx.doi.org/10.1056/NEJMoa1304459.
2. 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. 18 September 2013. Avian-origin influenza A(H7N9) infection in influenza A(H7N9)-affected areas of China: a serological study. J. Infect. Dis. http://dx.doi.org/10.1093/infdis/jit430.
3. World Health Organization. 25 October 2013. Number of confirmed human cases of avian influenza A(H7N9) reported to WHO. World Health Organization, Geneva, Switzerland. http://www.who.int/influe nza/human_animal_interface/influenza_h7n9/Data_Reports/en/inde x.html.
4. Li Q, Zhou L, Zhou M, Chen Z, Li F, Wu H, Xiang N, Chen E, Tang F, Wang D, Meng L, Hong Z, Tu W, Cao Y, Li L, Ding F, Liu B, Wang M, Xie R, Gao R, Li X, Bai T, Zou S, He J, Hu J, Xu Y, Chai C, Wang S, Gao Y, Jin L, Zhang Y, Luo H, Yu H, Gao L, Pang X, Liu G, Shu Y, Yang W, Uyeki TM, Wang Y, Wu F, Feng Z. 24 April 2013. Preliminary report: epidemiology of the avian influenzaA(H7N9) outbreak in China. N. Engl. J. Med. http://dx.doi.org/10.1056/NEJMoa1304617.
5. Qi X, Qian YH, Bao CJ, Guo XL, Cui LB, Tang FY, Ji H, Huang Y, Cai PQ, Lu B, Xu K, Shi C, Zhu FC, Zhou MH, Wang H. 2013. Probable person to person transmission of novel avian influenza A (H7N9) virus in Eastern China, 2013: epidemiological investigation. Br. Med. J. 347:f4752. http://dx.doi.org/10.1136/bmj.f4752.
6. Shi J, Xie J, He Z, Hu Y, He Y, Huang Q, Leng B, He W, Sheng Y, Li F, Song Y, Bai C, Gu Y, Jie Z. 2013. A detailed epidemiological and clinical description of 6 human cases of avian-origin influenza A (H7N9) virus infection in Shanghai. PLoS One 8:e77651. http://dx.doi.org/10.1371/journal.pone.0077651.
7. van Riel D, Leijten LM, de Graaf M, Siegers JY, Short KR, Spronken MI, Schrauwen EJ, Fouchier RA, Osterhaus AD, Kuiken T. 2013. Novel Avian-Origin Influenza A (H7N9) Virus Attaches to Epithelium in Both Upper and Lower Respiratory Tract of Humans. Am. J. Pathol. 183:1137-1143. http://dx.doi.org/10.1016/j.ajpath.2013.06.011.
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. 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. http://dx.doi.org/10.1038/nature12476.
10. Xu L, Bao L, Deng W, Dong L, 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, Li X, Huang W, Zhao X, Lan Y, Guo J, Yong W, Wei Q, Chen H, Zhang L, Qin C. 2013. Novel avian-origin human influenza A(H7N9) can be transmitted between ferrets via respiratory droplets. J. Infect. Dis. 209:551-556. http://dx.doi.org/10.1093/infdis/jit474.
11. 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.
12. Zhu H, Wang D, Kelvin DJ, Li L, Zheng Z, Yoon SW, Wong SS, Farooqui A, Wang J, Banner D, Chen R, Zheng R, Zhou J, Zhang Y, Hong W, Dong W, Cai Q, Roehrl MH, Huang SS, Kelvin AA, Yao T, Zhou B, Chen X, Leung GM, Poon LL, Webster RG, Webby RJ, Peiris JS, Guan Y, Shu Y. 2013. Infectivity, transmission, and pathology of human-isolated H7N9 influenza virus in ferrets and pigs. Science 341: 183-186. http://dx.doi.org/10.1126/science.1239844.
13. Belser JA, Gustin KM, Pearce MB, Maines TR, Zeng H, Pappas C, Sun X, Carney PJ, Villanueva JM, Stevens J, Katz JM, Tumpey TM. 2013. Pathogenesis and transmission of avian influenza A (H7N9) virus in ferrets and mice. Nature 501:556-559. http://dx.doi.org/10.1038/nature12391.
14. Mok CK, Lee HH, Chan MC, Sia SF, Lestra M, Nicholls JM, Zhu H, Guan Y, Peiris JM. 2013. Pathogenicity of the novel A/H7N9 influenza virus in mice. mBio 4:e0032-13. http://dx.doi.org/10.1128/mBio.003 62-13.
15. Kreijtz JH, Kroeze EJ, Stittelaar KJ, de Waal L, van Amerongen G, van Trierum S, van Run P, Bestebroer T, Kuiken T, Fouchier RA, Rimmelzwaan GF, Osterhaus AD. 2013. Low pathogenic avian influenza A(H7N9) virus causes high mortality in ferrets upon intratracheal challenge: a model to study intervention strategies. Vaccine 31:4995-4999. http://dx.doi.org/10.1016/j.vaccine.2013.06.071.
16. 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. http://dx.doi.org/10.1126/science.1240532.
17. van Riel D, Munster VJ, de Wit E, Rimmelzwaan GF, Fouchier RA, Osterhaus AD, Kuiken T. 2007. Human and avian influenza viruses target different cells in the lower respiratory tract of humans and other mammals. Am. J. Pathol. 171:1215-1223. http://dx.doi.org/10.2353/ajpath.2007.070248.
18. van Riel D, den Bakker MA, Leijten LM, Chutinimitkul S, Munster VJ, de Wit E, Rimmelzwaan GF, Fouchier RA, Osterhaus AD, Kuiken T. 2010. Seasonal and pandemic human influenza viruses attach better to human upper respiratory tract epithelium than avian influenza viruses. Am. J. Pathol. 176:1614-1618. http://dx.doi.org/10.2353/ajpath.2010.090949.
19. van Riel D, Munster VJ, de Wit E, Rimmelzwaan GF, Fouchier RA, Osterhaus AD, Kuiken T. 2006. H5N1 virus attachment to lower respiratory tract. Science 312:399. http://dx.doi.org/10.1126/science.1125548.
20. Xiong X, Martin SR, Haire LF, Wharton SA, Daniels RS, Bennett MS, McCauley JW, Collins PJ, Walker PA, Skehel JJ, Gamblin SJ. 2013. Receptor binding by an H7N9 influenza virus from humans. Nature 499: 496-499. http://dx.doi.org/10.1038/nature12372.
21. Yang H, Carney PJ, Chang JC, Villanueva JM, Stevens J. 2013. Structural analysis of the hemagglutinin from the recent 2013 H7N9 influenza virus. J. Virol. 87:12433-12446. http://dx.doi.org/10.1128/JVI.01854-13.
22. Tharakaraman K, Jayaraman A, Raman R, Viswanathan K, Stebbins NW, Johnson D, Shriver Z, Sasisekharan V, Sasisekharan R. 2013. Glycan receptor binding of the influenza A virus H7N9 hemagglutinin. Cell 153:1486-1493. http://dx.doi.org/10.1016/j.cell.2013.05.034.
23. Xu R, de Vries RP, Zhu X, Nycholat CM, McBride R, Yu W, Paulson JC, Wilson IA. 2013. Preferential recognition of avian-like receptors in human influenza A H7N9 viruses. Science 342:1230-1235. http://dx.doi.org/10.1126/science.1243761.
24. Chutinimitkul S, van Riel D, Munster VJ, van den Brand JM, Rimmelzwaan GF, Kuiken T, Osterhaus AD, Fouchier RA, de Wit E. 2010. In vitro assessment of attachment pattern and replication efficiency of H5N1 influenza A viruses with altered receptor specificity. J. Virol. 84:6825-6833. http://dx.doi.org/10.1128/JVI.02737-09.
25. Herfst S, Schrauwen EJ, Linster M, Chutinimitkul S, de Wit E, Munster VJ, Sorrell EM, Bestebroer TM, Burke DF, Smith DJ, Rimmelzwaan GF, Osterhaus AD, Fouchier RA. 2012. Airborne transmission of influenza A/H5N1 virus between ferrets. Science 336:1534-1541. http://dx.doi.org/10.1126/science.1213362.
26. Imai M, Watanabe T, Hatta M, Das SC, Ozawa M, Shinya K, Zhong G, Hanson A, Katsura H, Watanabe S, Li C, Kawakami E, Yamada S, Kiso M, Suzuki Y, Maher EA, Neumann G, Kawaoka Y. 2012. Experimental adaptation of an influenza H5 HA confers respiratory droplet transmission to a reassortant H5 HA/H1N1 virus in ferrets. Nature 486:420-428. http://dx.doi.org/10.1038/nature10831.
27. Kageyama T, Fujisaki S, Takashita E, Xu H, Yamada S, Uchida Y, Neumann G, Saito T, Kawaoka Y, Tashiro M. 2013. Genetic analysis of novel avian A(H7N9) influenza viruses isolated from patients in China, February to April 2013. Euro Surveill. 18:20453.
28. Nidom CA, Takano R, Yamada S, Sakai-Tagawa Y, Daulay S, Aswadi D, Suzuki T, Suzuki Y, Shinya K, Iwatsuki-Horimoto K, Muramoto Y, Kawaoka Y. 2010. Influenza A (H5N1) viruses from pigs, Indonesia. Emerg. Infect. Dis. 16:1515-1523. http://dx.doi.org/10.3201/eid1610.100 508.
29. Chan MCW, Chan RWY, Chan LLY, Mok CKP, Hui KPY, Fong JHM, Tao KP, Poon LLM, Nicholls JM, Guan Y, Peiris JSM. 2013. Tropism and innate host responses of a novel avian influenza A H7N9 virus: an analysis of ex-vivo and in-vitro cultures of the human respiratory tract. Lancet Respir. Med. 1:534-542. http://dx.doi.org/10.1016/S2213-2600 (13)70138-3.
30. Jones JC, Baranovich T, Zaraket H, Guan Y, Shu Y, Webby RJ, Webster RG. 2013. Human H7N9 influenza A viruses replicate in swine respiratory tissue explants. J. Virol. 87:12496-12498. http://dx.doi.org/10.1128/JVI.02499-13.
31. van den Brand JM, Stittelaar KJ, van Amerongen G, Reperant L, de Waal L, Osterhaus AD, Kuiken T. 2012. Comparison of temporal and spatial dynamics of seasonal H3N2, pandemic H1N1 and highly pathogenic avian influenza H5N1 virus infections in ferrets. PLoS One 7:e42343. http://dx.doi.org/10.1371/journal.pone.0042343.
32. Rimmelzwaan GF, Kuiken T, van Amerongen G, Bestebroer TM, Fouchier RA, Osterhaus AD. 2001. Pathogenesis of influenza A (H5N1) virus infection in a primate model. J. Virol. 75:6687-6691. http://dx.doi.org/10.1128/JVI.75.14.6687-6691.2001.
33. Korteweg C, Gu J. 2008. Pathology, molecular biology, and pathogenesis of avian influenza A (H5N1) infection in humans. Am. J. Pathol. 172: 1155-1170. http://dx.doi.org/10.2353/ajpath.2008.070791.
34. van Riel D, Rimmelzwaan GF, van Amerongen G, Osterhaus AD, Kuiken T. 2010. Highly pathogenic avian influenza virus H7N7 isolated from a fatal human case causes respiratory disease in cats but does not spread systemically. Am. J. Pathol. 177:2185-2190. http://dx.doi.org/10.2353/ajpath.2010.100401.