#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

The effect of mutations derived from mouse-adapted H3N2 seasonal influenza A virus to pathogenicity and host adaptation


Autoři: Eun-Ji Choi aff001;  Young Jae Lee aff001;  Jin-Moo Lee aff001;  Yeon-Jung Kim aff001;  Jang-Hoon Choi aff001;  Byeongwoo Ahn aff002;  Kisoon Kim aff001;  Myung Guk Han aff001
Působiště autorů: Division of Viral Disease Research, Center for Infectious Diseases Research, National Institute of Health, Korea Centers for Disease Control and Prevention, Osong, Republic of Korea aff001;  College of Veterinary Medicine, Chungbuk National University, Cheongju, Republic of Korea aff002
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0227516

Souhrn

Elucidating the genetic basis of influenza A viruses (IAVs) is important to understand which mutations will determine the virulence and the host range of mammals. Here, seasonal H3N2 influenza was adapted in mice by serial passage and four mutants, each carrying amino acid substitutions related to mouse adaptation in either the PB2, HA, NP, or NA protein, were generated. To confirm the contribution of each gene to enhanced pathogenicity and mouse adaptation, mice were inoculated with the respective variants, and virulence, replication, histopathology, and infectivity were examined. The virus harboring HA mutations displayed increased infection efficiency and replication competence, resulting in higher mortality in mice relative to those infected with wild-type virus. By contrast, the NP D34N mutation caused rapid and widespread infection in multiple organs without presenting virulent symptoms. Additionally, the PB2 F323L mutation presented delayed but elevated replication competence in the respiratory tract, whereas the S331R mutation in NA showed no considerable effects on mouse adaptation. These results suggested that mouse-adapted changes in HA are major factors in increased pathogenicity and that mutations in NP and PB2 also contribute to cross-species adaptability. Our findings offer a better understanding of the molecular basis for IAV pathogenicity and adaptation in a new host.

Klíčová slova:

Death rates – Influenza A virus – Microbial mutation – Mouse models – Pathogenesis – Substitution mutation – Viral pathogens – Viral replication


Zdroje

1. Iuliano AD, Roguski KM, Chang HH, Muscatello DJ, Palekar R, Tempia S, et al. Estimates of global seasonal influenza-associated respiratory mortality: a modelling study. Lancet. 2018;391(10127):1285–300. Epub 2017/12/19. doi: 10.1016/S0140-6736(17)33293-2 29248255.

2. Nicholson KG, Wood JM, Zambon M. Influenza. Lancet. 2003;362(9397):1733–45. Epub 2003/12/04. doi: 10.1016/S0140-6736(03)14854-4 14643124.

3. Pu Z, Xiang D, Li X, Luo T, Shen X, Murphy RW, et al. Potential Pandemic of H7N9 Avian Influenza A Virus in Human. Front Cell Infect Microbiol. 2018;8:414. Epub 2018/12/12. doi: 10.3389/fcimb.2018.00414 30533399.

4. Webster RG, Shortridge KF, Kawaoka Y. Influenza: interspecies transmission and emergence of new pandemics. FEMS Immunol Med Microbiol. 1997;18(4):275–9. Epub 1997/08/01. doi: 10.1111/j.1574-695X.1997.tb01056.x 9348163.

5. Taubenberger JK, Morens DM. 1918 influenza: the mother of all pandemics. Emerging Infectious Diseases. 2006;12(1):15–22. doi: 10.3201/eid1201.050979 16494711

6. Subbarao EK, London W, Murphy BR. A single amino acid in the PB2 gene of influenza A virus is a determinant of host range. J Virol. 1993;67(4):1761–4. Epub 1993/04/01. 8445709.

7. Brown EG, Liu H, Kit LC, Baird S, Nesrallah M. Pattern of mutation in the genome of influenza A virus on adaptation to increased virulence in the mouse lung: identification of functional themes. Proc Natl Acad Sci U S A. 2001;98(12):6883–8. Epub 2001/05/24. doi: 10.1073/pnas.111165798 11371620.

8. Gabriel G, Dauber B, Wolff T, Planz O, Klenk HD, Stech J. The viral polymerase mediates adaptation of an avian influenza virus to a mammalian host. Proceedings of the National Academy of Sciences of the United States of America. 2005;102(51):18590–5. Epub 2005/12/13. doi: 10.1073/pnas.0507415102 16339318.

9. Ping J, Dankar SK, Forbes NE, Keleta L, Zhou Y, Tyler S, et al. PB2 and hemagglutinin mutations are major determinants of host range and virulence in mouse-adapted influenza A virus. J Virol. 2010;84(20):10606–18. Epub 2010/08/13. doi: 10.1128/JVI.01187-10 20702632.

10. Keleta L, Ibricevic A, Bovin NV, Brody SL, Brown EG. Experimental evolution of human influenza virus H3 hemagglutinin in the mouse lung identifies adaptive regions in HA1 and HA2. J Virol. 2008;82(23):11599–608. Epub 2008/10/03. doi: 10.1128/JVI.01393-08 18829764.

11. Pepin KM, Lass S, Pulliam JR, Read AF, Lloyd-Smith JO. Identifying genetic markers of adaptation for surveillance of viral host jumps. Nat Rev Microbiol. 2010;8(11):802–13. Epub 2010/10/13. doi: 10.1038/nrmicro2440 20938453.

12. Rudneva IA, Kaverin NV, Varich NL, Gitelman AK, Makhov AM, Klimenko SM, et al. Studies on the genetic determinants of influenza virus pathogenicity for mice with the use of reassortants between mouse-adapted and non-adapted variants of the same virus strain. Arch Virol. 1986;90(3–4):237–48. Epub 1986/01/01. doi: 10.1007/bf01317373 3729728.

13. Kobasa D, Takada A, Shinya K, Hatta M, Halfmann P, Theriault S, et al. Enhanced virulence of influenza A viruses with the haemagglutinin of the 1918 pandemic virus. Nature. 2004;431(7009):703–7. Epub 2004/10/08. doi: 10.1038/nature02951 15470432.

14. Brown EG. Increased virulence of a mouse-adapted variant of influenza A/FM/1/47 virus is controlled by mutations in genome segments 4, 5, 7, and 8. J Virol. 1990;64(9):4523–33. Epub 1990/09/01. 2117072.

15. Ilyushina NA, Khalenkov AM, Seiler JP, Forrest HL, Bovin NV, Marjuki H, et al. Adaptation of pandemic H1N1 influenza viruses in mice. J Virol. 2010;84(17):8607–16. Epub 2010/07/02. doi: 10.1128/JVI.00159-10 20592084.

16. Shilov AA, Sinitsyn BV. [Changes in its hemagglutinin during the adaptation of the influenza virus to mice and their role in the acquisition of virulent properties and resistance to serum inhibitors]. Vopr Virusol. 1994;39(4):153–7. Epub 1994/07/01. 7998391.

17. Chen H, Bright RA, Subbarao K, Smith C, Cox NJ, Katz JM, et al. Polygenic virulence factors involved in pathogenesis of 1997 Hong Kong H5N1 influenza viruses in mice. Virus Res. 2007;128(1–2):159–63. Epub 2007/05/25. doi: 10.1016/j.virusres.2007.04.017 17521765.

18. Gabriel G, Herwig A, Klenk HD. Interaction of polymerase subunit PB2 and NP with importin alpha1 is a determinant of host range of influenza A virus. PLoS Pathog. 2008;4(2):e11. Epub 2008/02/06. doi: 10.1371/journal.ppat.0040011 18248089.

19. de Jong RM, Stockhofe-Zurwieden N, Verheij ES, de Boer-Luijtze EA, Ruiter SJ, de Leeuw OS, et al. Rapid emergence of a virulent PB2 E627K variant during adaptation of highly pathogenic avian influenza H7N7 virus to mice. Virol J. 2013;10:276. Epub 2013/09/07. doi: 10.1186/1743-422X-10-276 24007444.

20. Wang J, Sun Y, Xu Q, Tan Y, Pu J, Yang H, et al. Mouse-adapted H9N2 influenza A virus PB2 protein M147L and E627K mutations are critical for high virulence. PLoS One. 2012;7(7):e40752. Epub 2012/07/19. doi: 10.1371/journal.pone.0040752 22808250.

21. Broberg E, Snacken R, Adlhoch C, Beaute J, Galinska M, Pereyaslov D, et al. Start of the 2014/15 influenza season in Europe: drifted influenza A(H3N2) viruses circulate as dominant subtype. Euro Surveill. 2015;20(4). Epub 2015/02/07. doi: 10.2807/1560-7917.es2015.20.4.21023 25655052.

22. Chambers BS, Parkhouse K, Ross TM, Alby K, Hensley SE. Identification of Hemagglutinin Residues Responsible for H3N2 Antigenic Drift during the 2014–2015 Influenza Season. Cell Rep. 2015;12(1):1–6. Epub 2015/06/30. doi: 10.1016/j.celrep.2015.06.005 26119736.

23. Flannery B, Clippard J, Zimmerman RK, Nowalk MP, Jackson ML, Jackson LA, et al. Early estimates of seasonal influenza vaccine effectiveness—United States, January 2015. MMWR Morb Mortal Wkly Rep. 2015;64(1):10–5. Epub 2015/01/16. 25590680.

24. Pebody RG, Warburton F, Ellis J, Andrews N, Thompson C, von Wissmann B, et al. Low effectiveness of seasonal influenza vaccine in preventing laboratory-confirmed influenza in primary care in the United Kingdom: 2014/15 mid-season results. Euro Surveill. 2015;20(5):21025. Epub 2015/02/14. 25677050.

25. D’Mello T, Brammer L, Blanton L, Kniss K, Smith S, Mustaquim D, et al. Update: Influenza activity—United States, September 28, 2014-February 21, 2015. MMWR Morb Mortal Wkly Rep. 2015;64(8):206–12. Epub 2015/03/06. 25742380.

26. Morens DM, Taubenberger JK, Fauci AS. The 2009 H1N1 pandemic influenza virus: what next? MBio. 2010;1(4). Epub 2010/09/30. doi: 10.1128/mBio.00211-10 20877580.

27. Prokopyeva EA, Sobolev IA, Prokopyev MV, Shestopalov AM. Adaptation of influenza A(H1N1)pdm09 virus in experimental mouse models. Infect Genet Evol. 2016;39:265–71. doi: 10.1016/j.meegid.2016.01.022 26829383.

28. Eisfeld AJ, Neumann G, Kawaoka Y. Influenza A virus isolation, culture and identification. Nat Protoc. 2014;9(11):2663–81. Epub 2014/10/17. doi: 10.1038/nprot.2014.180 25321410.

29. Hoffmann E, Neumann G, Kawaoka Y, Hobom G, Webster RG. A DNA transfection system for generation of influenza A virus from eight plasmids. Proceedings of the National Academy of Sciences of the United States of America. 2000;97(11):6108–13. doi: 10.1073/pnas.100133697 10801978.

30. REED LJ, MUENCH H. A SIMPLE METHOD OF ESTIMATING FIFTY PER CENT ENDPOINTS12. American Journal of Epidemiology. 1938;27(3):493–7. doi: 10.1093/oxfordjournals.aje.a118408

31. Kim HM, Kim CK, Lee NJ, Chu H, Kang C, Kim K, et al. Pathogenesis of novel reassortant avian influenza virus A (H5N8) Isolates in the ferret. Virology. 2015;481:136–41. Epub 2015/03/18. doi: 10.1016/j.virol.2015.02.042 25776760.

32. Thangavel RR, Bouvier NM. Animal models for influenza virus pathogenesis, transmission, and immunology. J Immunol Methods. 2014;410:60–79. Epub 2014/04/09. doi: 10.1016/j.jim.2014.03.023 24709389.

33. Andrewes CH, Laidlaw PP, Smith W. THE SUSCEPTIBILITY OF MICE TO THE VIRUSES OF HUMAN AND SWINE INFLUENZA. The Lancet. 1934;224(5799):859–62. https://doi.org/10.1016/S0140-6736(00)74657-5

34. Hirst GK. Studies on the Mechanism of Adaptation of Influenza Virus to Mice. J Exp Med. 1947;86(5):357–66. Epub 1947/10/31. doi: 10.1084/jem.86.5.357 19871683.

35. Mononen I, Karjalainen E. Structural comparison of protein sequences around potential N-glycosylation sites. Biochimica et Biophysica Acta (BBA)—Protein Structure and Molecular Enzymology. 1984;788(3):364–7. https://doi.org/10.1016/0167-4838(84)90050-5

36. Deshpande KL, Fried VA, Ando M, Webster RG. Glycosylation affects cleavage of an H5N2 influenza virus hemagglutinin and regulates virulence. Proceedings of the National Academy of Sciences of the United States of America. 1987;84(1):36–40. Epub 1987/01/01. doi: 10.1073/pnas.84.1.36 3467357.

37. Reading PC, Morey LS, Crouch EC, Anders EM. Collectin-mediated antiviral host defense of the lung: evidence from influenza virus infection of mice. J Virol. 1997;71(11):8204–12. Epub 1997/10/29. 9343171.

38. Kamiki H, Matsugo H, Kobayashi T, Ishida H, Takenaka-Uema A, Murakami S, et al. A PB1-K577E Mutation in H9N2 Influenza Virus Increases Polymerase Activity and Pathogenicity in Mice. Viruses. 2018;10(11). Epub 2018/11/23. doi: 10.3390/v10110653 30463209.

39. Kamal RP, Katz JM, York IA. Molecular determinants of influenza virus pathogenesis in mice. Curr Top Microbiol Immunol. 2014;385:243–74. Epub 2014/07/21. doi: 10.1007/82_2014_388 25038937.

40. Ping J, Keleta L, Forbes NE, Dankar S, Stecho W, Tyler S, et al. Genomic and protein structural maps of adaptive evolution of human influenza A virus to increased virulence in the mouse. PLoS One. 2011;6(6):e21740. Epub 2011/07/09. doi: 10.1371/journal.pone.0021740 21738783.

41. Ping J, Lopes TJ, Nidom CA, Ghedin E, Macken CA, Fitch A, et al. Development of high-yield influenza A virus vaccine viruses. Nat Commun. 2015;6:8148. Epub 2015/09/04. doi: 10.1038/ncomms9148 26334134.

42. Hartley CA, Reading PC, Ward AC, Anders EM. Changes in the hemagglutinin molecule of influenza type A (H3N2) virus associated with increased virulence for mice. Arch Virol. 1997;142(1):75–88. Epub 1997/01/01. doi: 10.1007/s007050050060 9155874.

43. Perrone LA, Plowden JK, Garcia-Sastre A, Katz JM, Tumpey TM. H5N1 and 1918 pandemic influenza virus infection results in early and excessive infiltration of macrophages and neutrophils in the lungs of mice. PLoS Pathog. 2008;4(8):e1000115. Epub 2008/08/02. doi: 10.1371/journal.ppat.1000115 18670648.


Článek vyšel v časopise

PLOS One


2020 Číslo 1
Nejčtenější tento týden
Nejčtenější v tomto čísle
Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

Svět praktické medicíny 1/2024 (znalostní test z časopisu)
nový kurz

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

Sekvenční léčba schizofrenie
Autoři: MUDr. Jana Hořínková

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

Význam metforminu pro „udržitelnou“ terapii diabetu
Autoři: prof. MUDr. Milan Kvapil, CSc., MBA

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#