#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Adaptation of H3N2 canine influenza virus to feline cell culture


Autoři: Haruhiko Kamiki aff001;  Hiromichi Matsugo aff001;  Hiroho Ishida aff001;  Tomoya Kobayashi-Kitamura aff001;  Wataru Sekine aff001;  Akiko Takenaka-Uema aff001;  Shin Murakami aff001;  Taisuke Horimoto aff001
Působiště autorů: Department of Veterinary Microbiology, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Bunkyo-ku, Tokyo, Japan aff001
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0223507

Souhrn

H3N2 canine influenza viruses are prevalent in Asian and North American countries. During circulation of the viruses in dogs, these viruses are occasionally transmitted to cats. If this canine virus causes an epidemic in cats too, sporadic infections may occur in humans because of the close contact between these companion animals and humans, possibly triggering an emergence of mutant viruses with a pandemic potential. In this study, we aimed to gain an insight into the mutations responsible for inter-species transmission of H3N2 virus from dogs to cats. We found that feline CRFK cell-adapted viruses acquired several mutations in multiple genome segments. Among them, HA1-K299R, HA2-T107I, NA-L35R, and M2-W41C mutations individually increased virus growth in CRFK cells. With a combination of these mutations, virus growth further increased not only in CRFK cells but also in other feline fcwf-4 cells. Both HA1-K299R and HA2-T107I mutations increased thermal resistance of the viruses. In addition, HA2-T107I increased the pH requirement for membrane fusion. These findings suggest that the mutations, especially the two HA mutations, identified in this study, might be responsible for adaptation of H3N2 canine influenza viruses in cats.

Klíčová slova:

Cats – Dogs – Microbial mutation – Plasmid construction – Respiratory infections – RNA viruses – Viral transmission and infection – Membrane fusion


Zdroje

1. Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y. Evolution and ecology of influenza A viruses. Microbiol Rev. 1992;56: 152–179. 1579108

2. Joseph U, Su YCF, Vijaykrishna D, Smith GJD. The ecology and adaptive evolution of influenza A interspecies transmission. Influenza Other Respi Viruses. 2017;11: 74–84. doi: 10.1111/irv.12412 27426214

3. Hinshaw VS, Webster RG, Easterday BC, Bean WJ. Replication of avian influenza A viruses in mammals. Infect Immun. 1981;34: 354–361. 7309229

4. Songserm T, Amonsin A, Jam-on R, Sae-Heng N, Pariyothorn N, Payungporn S, et al. Fatal avian influenza A H5N1 in a dog. Emerg Infect Dis. 2006;12: 1744–1747. doi: 10.3201/eid1211.060542 17283627

5. Dundon WG, De Benedictis P, Viale E, Capua I. Serologic evidence of pandemic (H1N1) 2009 infection in dogs, Italy. Emerg Infect Dis. 2010;16: 2019–2021. doi: 10.3201/eid1612.100514 21122255

6. Kuiken T, Rimmelzwaan G, van Riel D, van Amerongen G, Baars M, Fouchier R, et al. Avian H5N1 influenza in cats. Science. 2004;306: 241–241. doi: 10.1126/science.1102287 15345779

7. ProMED-mail. 2007 Mar 8 [cited 7 Mar 2019]. In: ProMED-mail [Internet]. Available: https://www.promedmail.org/post/20070308.0826

8. Horimoto T, Gen F, Murakami S, Iwatsuki-Horimoto K, Kato K, Hisasue M, et al. Cats as a potential source of emerging influenza virus infections. Virol Sin. 2015;30: 221–223. doi: 10.1007/s12250-015-3580-9 25953615

9. Horimoto T, Gen F, Murakami S, Iwatsuki-Horimoto K, Kato K, Akashi H, et al. Serological evidence of infection of dogs with human influenza viruses in Japan. Vet Rec. 2014;174: 96.2–96. doi: 10.1136/vr.101929 24336761

10. Crawford PC, Dubovi EJ, Castleman WL, Stephenson I, Gibbs EPJ, Chen L, et al. Transmission of equine influenza virus to dogs. Science. 2005;310: 482–485. doi: 10.1126/science.1117950 16186182

11. Song D, Kang B, Lee C, Jung K, Ha G, Kang D, et al. Transmission of avian influenza virus (H3N2) to dogs. Emerg Infect Dis. 2008;14: 741–746. doi: 10.3201/eid1405.071471 18439355

12. Li S, Shi Z, Jiao P, Zhang G, Zhong Z, Tian W, et al. Avian-origin H3N2 canine influenza A viruses in Southern China. Infect Genet Evol. 2010;10: 1286–1288. doi: 10.1016/j.meegid.2010.08.010 20732458

13. Lee Y-N, Lee D-H, Lee H-JJ, Park J-K, Yuk S-S, Sung H-J, et al. Evidence of H3N2 canine influenza virus infection before 2007. Vet Rec. 2012;171: 477.1–477. doi: 10.1136/vr.100718 22952134

14. Bunpapong N, Nonthabenjawan N, Chaiwong S, Tangwangvivat R, Boonyapisitsopa S, Jairak W, et al. Genetic characterization of canine influenza A virus (H3N2) in Thailand. Virus Genes. 2014;48: 56–63. doi: 10.1007/s11262-013-0978-z 24101341

15. Newbury S, Godhardt-Cooper J, Poulsen KP, Cigel F, Balanoff L, Toohey-Kurth K. Prolonged intermittent virus shedding during an outbreak of canine influenza A H3N2 virus infection in dogs in three Chicago area shelters: 16 cases (March to May 2015). J Am Vet Med Assoc. 2016;248: 1022–1026. doi: 10.2460/javma.248.9.1022 27074610

16. Voorhees IEH, Glaser AL, Toohey-Kurth K, Newbury S, Dalziel BD, Dubovi EJ, et al. Spread of canine influenza A(H3N2) virus, United States. Emerg Infect Dis. 2017;23: 1950–1957. doi: 10.3201/eid2312.170246 28858604

17. Lin H-T, Wang C-H, Chueh L-L, Su B-L, Wang L-C. Influenza A(H6N1) virus in dogs, Taiwan. Emerg Infect Dis. 2015;21: 2154–2157. doi: 10.3201/eid2112.141229 26583707

18. Guang-jian Z, Zong-shuai L, Yan-li Z, Shi-jin J, Zhi-jing X. Genetic characterization of a novel influenza A virus H5N2 isolated from a dog in China. Vet Microbiol. 2012;155: 409–416. doi: 10.1016/j.vetmic.2011.08.017 22033043

19. Sun X, Xu X, Liu Q, Liang D, Li C, He Q, et al. Evidence of avian-like H9N2 influenza A virus among dogs in Guangxi, China. Infect Genet Evol. 2013;20: 471–475. doi: 10.1016/j.meegid.2013.10.012 24161411

20. Chen Y, Trovão NS, Wang G, Zhao W, He P, Zhou H, et al. Emergence and evolution of novel reassortant influenza A viruses in canines in Southern China. MBio. 2018;9: e00909–18. doi: 10.1128/mBio.00909-18 29871917

21. Zhang X, Shen Y, Du L, Wang R, Jiang B, Sun H, et al. Serological survey of canine H3N2, pandemic H1N1/09, and human seasonal H3N2 influenza viruses in cats in northern China, 2010–2014. Virol J. 2015;12: 50. doi: 10.1186/s12985-015-0285-5 25889762

22. Ali A, Daniels JB, Zhang Y, Rodriguez-Palacios A, Hayes-Ozello K, Mathes L, et al. Pandemic and seasonal human influenza virus infections in domestic cats: prevalence, association with respiratory disease, and seasonality patterns. J Clin Microbiol. 2011;49: 4101–4105. doi: 10.1128/JCM.05415-11 21956989

23. Fiorentini L, Taddei R, Moreno A, Gelmetti D, Barbieri I, De Marco MA, et al. Influenza A pandemic (H1N1) 2009 virus outbreak in a cat colony in Italy. Zoonoses Public Health. 2011;58: 573–581. doi: 10.1111/j.1863-2378.2011.01406.x 21824359

24. Songserm T, Amonsin A, Jam-on R, Sae-Heng N, Meemak N, Pariyothorn N, et al. Avian influenza H5N1 in naturally infected domestic cat. Emerg Infect Dis. 2006;12: 681–683. doi: 10.3201/eid1204.051396 16704821

25. Belser JA, Pulit-Penaloza JA, Sun X, Brock N, Pappas C, Creager HM, et al. A novel A(H7N2) influenza virus isolated from a veterinarian caring for cats in a New York City animal shelter causes mild disease and transmits poorly in the ferret model. J Virol. 2017; JVI.00672-17. doi: 10.1128/JVI.00672-17 28515300

26. Paniker CK, Nair CM. Infection with A2 Hong Kong influenza virus in domestic cats. Bull World Health Organ. 1970;43: 859–862. 5314017

27. Paniker CK, Nair CM. Experimental infection of animals with influenzavirus types A and B. Bull World Health Organ. 1972;47: 461–463. 4196340

28. Jeoung H-Y, Lim S-I, Shin B-H, Lim J-A, Song J-Y, Song D-S, et al. A novel canine influenza H3N2 virus isolated from cats in an animal shelter. Vet Microbiol. 2013;165: 281–286. doi: 10.1016/j.vetmic.2013.03.021 23618838

29. Song DS, An DJ, Moon HJ, Yeom MJ, Jeong HY, Jeong WS, et al. Interspecies transmission of the canine influenza H3N2 virus to domestic cats in South Korea, 2010. J Gen Virol. 2011;92: 2350–2355. doi: 10.1099/vir.0.033522-0 21715595

30. Neumann G, Noda T, Kawaoka Y. Emergence and pandemic potential of swine-origin H1N1 influenza virus. Nature. 2009;459: 931–939. doi: 10.1038/nature08157 19525932

31. Song D, Moon H-J, An D-J, Jeoung H-Y, Kim H, Yeom M-J, et al. A novel reassortant canine H3N1 influenza virus between pandemic H1N1 and canine H3N2 influenza viruses in Korea. J Gen Virol. 2012;93: 551–554. doi: 10.1099/vir.0.037739-0 22131311

32. Hoffmann E, Stech J, Guan Y, Webster RG, Perez DR. Universal primer set for the full-length amplification of all influenza A viruses. Arch Virol. 2001;146: 2275–2289. doi: 10.1007/s007050170002 11811679

33. Neumann G, Watanabe T, Ito H, Watanabe S, Goto H, Gao P, et al. Generation of influenza A viruses entirely from cloned cDNAs. Proc Natl Acad Sci USA. 1999;96: 9345–9350. doi: 10.1073/pnas.96.16.9345 10430945

34. Murakami S, Horimoto T, Ito M, Takano R, Katsura H, Shimojima M, et al. Enhanced growth of influenza vaccine seed viruses in vero cells mediated by broadening the optimal pH range for virus membrane fusion. J Virol. 2012;86: 1405–1410. doi: 10.1128/JVI.06009-11 22090129

35. Hanson A, Imai M, Hatta M, McBride R, Imai H, Taft A, et al. Identification of stabilizing mutations in an H5 hemagglutinin influenza virus protein. J Virol. 2015;90: 2981–2992. doi: 10.1128/JVI.02790-15 26719265

36. Neumann G, Kawaoka Y. Transmission of influenza A viruses. Virology. 2015;479–480: 234–246. doi: 10.1016/j.virol.2015.03.009 25812763

37. Sang X, Wang A, Ding J, Kong H, Gao X, Li L, et al. Adaptation of H9N2 AIV in guinea pigs enables efficient transmission by direct contact and inefficient transmission by respiratory droplets. Sci Rep. 2015;5: 15928. doi: 10.1038/srep15928 26552719

38. Klein EY, Blumenkrantz D, Serohijos A, Shakhnovich E, Choi JM, Rodrigues JV, et al. Stability of the influenza virus hemagglutinin protein correlates with evolutionary dynamics. mSphere. 2018;3: e00554–17, doi: 10.1128/mSphereDirect.00554-17 29299534

39. Singanayagam A, Zambon M, Barclay WS. Influenza virus with increased pH of hemagglutinin activation has improved replication in cell culture but at the cost of infectivity in human airway epithelium. J Virol. 2019;93: e00058–19. doi: 10.1128/JVI.00058-19 31189708

40. Rachakonda PS, Veit M, Korte T, Ludwig K, Böttcher C, Huang Q, et al. The relevance of salt bridges for the stability of the influenza virus hemagglutinin. FASEB J. 2007;21: 995–1002. doi: 10.1096/fj.06-7052hyp 17218542

41. Sauter NK, Hanson JE, Glick GD, Brown JH, Crowther RL, Park SJ, et al. Binding of influenza virus hemagglutinin to analogs of its cell-surface receptor, sialic acid: analysis by proton nuclear magnetic resonance spectroscopy and x-ray crystallography. Biochemistry. 1992;31: 9609–9621. doi: 10.1021/bi00155a013 1327122

42. Thoennes S, Li Z-N, Lee B-J, Langley WA, Skehel JJ, Russell RJ, et al. Analysis of residues near the fusion peptide in the influenza hemagglutinin structure for roles in triggering membrane fusion. Virology. 2008;370: 403–414. doi: 10.1016/j.virol.2007.08.035 17936324

43. Daniels RS, Downie JC, Hay AJ, Knossow M, Skehel JJ, Wang ML, et al. Fusion mutants of the influenza virus hemagglutinin glycoprotein. Cell. 1985;40: 431–439. doi: 10.1016/0092-8674(85)90157-6 3967299

44. Reed ML, Yen H-L, DuBois RM, Bridges OA, Salomon R, Webster RG, et al. Amino acid residues in the fusion peptide pocket regulate the pH of activation of the H5N1 influenza virus hemagglutinin protein. J Virol. 2009;83: 3568–3580. doi: 10.1128/JVI.02238-08 19193808

45. Barman S, Nayak DP. Analysis of the transmembrane domain of influenza virus neuraminidase, a type II transmembrane glycoprotein, for apical sorting and raft association. J Virol. 2000;74: 6538–6545. doi: 10.1128/jvi.74.14.6538-6545.2000 10864667

46. Wang C, Lamb RA, Pinto LH. Activation of the M2 ion channel of influenza virus: a role for the transmembrane domain histidine residue. Biophys J. 1995;69: 1363–1371. doi: 10.1016/S0006-3495(95)80003-2 8534806

47. Schnell JR, Chou JJ. Structure and mechanism of the M2 proton channel of influenza A virus. Nature. 2008;451: 591–595. doi: 10.1038/nature06531 18235503

48. Venkataraman P, Lamb RA, Pinto LH. Chemical rescue of histidine selectivity filter mutants of the M2 ion channel of influenza A virus. J Biol Chem. 2005;280: 21463–21472. doi: 10.1074/jbc.M412406200 15784624

49. Tang Y, Zaitseva F, Lamb RA, Pinto LH. The gate of the influenza virus M2 proton channel is formed by a single tryptophan residue. J Biol Chem. 2002;277: 39880–39886. doi: 10.1074/jbc.M206582200 12183461


Článek vyšel v časopise

PLOS One


2019 Číslo 10
Nejčtenější tento týden
Nejčtenější v tomto čísle
Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

KOST
Koncepce osteologické péče pro gynekology a praktické lékaře
nový kurz
Autoři: MUDr. František Šenk

Sekvenční léčba schizofrenie
Autoři: MUDr. Jana Hořínková

Hypertenze a hypercholesterolémie – synergický efekt léčby
Autoři: prof. MUDr. Hana Rosolová, DrSc.

Svět praktické medicíny 5/2023 (znalostní test z časopisu)

Imunopatologie? … a co my s tím???
Autoři: doc. MUDr. Helena Lahoda Brodská, Ph.D.

Všechny kurzy
Kurzy Podcasty Doporučená témata Časopisy
Přihlášení
Zapomenuté heslo

Zadejte e-mailovou adresu, se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

#ADS_BOTTOM_SCRIPTS#