The proteolytic activation of (H3N2) influenza A virus hemagglutinin is facilitated by different type II transmembrane serine proteases

Journal of Virology

Volumn 90, Issue 9, 2016, Pages 4298-4307

  Kühn, Nora ^a   Bergmann, Silke ^b   Kösterke, Nadine ^c   Lambertz, Ruth L O ^a   Keppner, Anna ^d   Van Den Brand, Judith M A ^e   Pöhlmann, Stefan ^f   Weiß, Siegfried ^c   Hummler, Edith ^d   Hatesuer, Bastian ^a   Schughart, Klaus ^a,b  

^a UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

^b UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^c HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^d UNIVERSITY OF LAUSANNE   (Switzerland)

^e ERASMUS MEDICAL CENTER   (Netherlands)

^f GERMAN PRIMATE CENTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS HEMAGGLUTININ; CHEMOKINE; CYTOKINE; INFLUENZA VIRUS HEMAGGLUTININ; MEMBRANE PROTEIN; SERINE PROTEINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; GENE INACTIVATION; IN VITRO STUDY; IN VIVO STUDY; INFLUENZA A (H1N1); INFLUENZA A (H3N2); INFLUENZA A VIRUS (H1N1); INFLUENZA A VIRUS (H3N2); MORTALITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; TMPRSS2 GENE; TMPRSS4 GENE; VIRUS ACTIVATION; VIRUS CELL INTERACTION; VIRUS GENE; VIRUS LOAD; VIRUS PATHOGENESIS; VIRUS REPLICATION; WEIGHT REDUCTION; ANIMAL; BRONCHUS; DISEASE MODEL; DISEASE PREDISPOSITION; ENZYME ACTIVATION; GENE DELETION; GENE EXPRESSION; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; KNOCKOUT MOUSE; LUNG ALVEOLUS; METABOLISM; ORTHOMYXOVIRUS INFECTION; PHYSIOLOGY; PROTEIN DEGRADATION; VIROLOGY;

ANIMALS; BRONCHI; CHEMOKINES; CYTOKINES; DISEASE MODELS, ANIMAL; DISEASE SUSCEPTIBILITY; ENZYME ACTIVATION; FEMALE; GENE DELETION; GENE EXPRESSION; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HOST-PATHOGEN INTERACTIONS; INFLUENZA A VIRUS, H3N2 SUBTYPE; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; ORTHOMYXOVIRIDAE INFECTIONS; PROTEOLYSIS; PULMONARY ALVEOLI; SERINE ENDOPEPTIDASES; VIRAL LOAD; VIRUS REPLICATION;

EID: 84964989185     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02693-15     Document Type: Article

References (45)

1. Cox NJ, Subbarao K. 2000. Global epidemiology of influenza: past and present. Annu Rev Med 51:407-421. http://dx.doi.org/10.1146/annurev.med.51.1.407.
2. Loregian A, Mercorelli B, Nannetti G, Compagnin C, Palu G. 2014. Antiviral strategies against influenza virus: towards new therapeutic approaches. Cell Mol Life Sci 71:3659-3683. http://dx.doi.org/10.1007/s00018-014-1615-2.
3. Klenk HD, Rott R, Orlich M, Blodorn J. 1975. Activation of influenza A viruses by trypsin treatment. Virology 68:426-439. http://dx.doi.org/10.1016/0042-6822(75)90284-6.
4. Lazarowitz SG, Choppin PW. 1975. Enhancement of the infectivity of influenza A and B viruses by proteolytic cleavage of the hemagglutinin polypeptide. Virology 68:440-454. http://dx.doi.org/10.1016/0042-6822(75)90285-8.
5. Kido H, Okumura Y, Yamada H, Le TQ, Yano M. 2007. Proteases essential for human influenza virus entry into cells and their inhibitors as potential therapeutic agents. Curr Pharm Des 13:405-414. http://dx.doi.org/10.2174/138161207780162971.
6. Murakami M, Towatari T, Ohuchi M, Shiota M, Akao M, Okumura Y, Parry MA, Kido H. 2001. Mini-plasmin found in the epithelial cells of bronchioles triggers infection by broad-spectrum influenza A viruses and Sendai virus. Eur J Biochem 268:2847-2855. http://dx.doi.org/10.1046/j.1432-1327.2001.02166.x.
7. Steinhauer DA. 1999. Role of hemagglutinin cleavage for the pathogenicity of influenza virus. Virology 258:1-20. http://dx.doi.org/10.1006/viro.1999.9716.
8. Towatari T, Ide M, Ohba K, Chiba Y, Murakami M, Shiota M, Kawachi M, Yamada H, Kido H. 2002. Identification of ectopic anionic trypsin I in rat lungs potentiating pneumotropic virus infectivity and increased enzyme level after virus infection. Eur J Biochem 269:2613-2621. http://dx.doi.org/10.1046/j.1432-1033.2002.02937.x.
9. Zhirnov OP, Ikizler MR, Wright PF. 2002. Cleavage of influenza A virus hemagglutinin in human respiratory epithelium is cell associated and sensitive to exogenous antiproteases. J Virol 76:8682-8689. http://dx.doi.org/10.1128/JVI.76.17.8682-8689.2002.
10. Bertram S, Glowacka I, Blazejewska P, Soilleux E, Allen P, Danisch S, Steffen I, Choi SY, Park Y, Schneider H, Schughart K, Pohlmann S. 2010. TMPRSS2 and TMPRSS4 facilitate trypsin-independent spread of influenza virus in Caco-2 cells. J Virol 84:10016-10025. http://dx.doi.org/10.1128/JVI.00239-10.
11. Böttcher E, Matrosovich T, Beyerle M, Klenk HD, Garten W, Matrosovich M. 2006. Proteolytic activation of influenza viruses by serine proteases TMPRSS2 and HAT from human airway epithelium. J Virol 80: 9896-9898. http://dx.doi.org/10.1128/JVI.01118-06.
12. Böttcher-Friebertshauser E, Stein DA, Klenk HD, Garten W. 2011. Inhibition of influenza virus infection in human airway cell cultures by an antisense peptide-conjugated morpholino oligomer targeting the hemagglutinin-activating protease TMPRSS2. J Virol 85:1554-1562. http://dx.doi.org/10.1128/JVI.01294-10.
13. Hatesuer B, Bertram S, Mehnert N, Bahgat MM, Nelson PS, Pohlman S, Schughart K. 2013. Tmprss2 is essential for influenza H1N1 virus pathogenesis in mice. PLoS Pathog 9:e1003774. http://dx.doi.org/10.1371/journal.ppat.1003774.
14. Tarnow C, Engels G, Arendt A, Schwalm F, Sediri H, Preuss A, Nelson PS, Garten W, Klenk HD, Gabriel G, Bottcher-Friebertshauser E. 2014. TMPRSS2 is a host factor that is essential for pneumotropism and pathogenicity of H7N9 influenza A virus in mice. J Virol 88:4744-4751. http://dx.doi.org/10.1128/JVI.03799-13.
15. Sakai K, Ami Y, Tahara M, Kubota T, Anraku M, Abe M, Nakajima N, Sekizuka T, Shirato K, Suzaki Y, Ainai A, Nakatsu Y, Kanou K, Nakamura K, Suzuki T, Komase K, Nobusawa E, Maenaka K, Kuroda M, Hasegawa H, Kawaoka Y, Tashiro M, Takeda M. 2014. The host protease TMPRSS2 plays a major role in in vivo replication of emerging H7N9 and seasonal influenza viruses. J Virol 88:5608-5616. http://dx.doi.org/10.1128/JVI.03677-13.
16. Gabriel G, Dauber B, Wolff T, Planz O, Klenk HD, Stech J. 2005. The viral polymerase mediates adaptation of an avian influenza virus to a mammalian host. Proc Natl Acad Sci U S A 102:18590-18595. http://dx.doi.org/10.1073/pnas.0507415102.
17. Haller O, Arnheiter H, Lindenmann J. 1979. Natural, genetically determined resistance toward influenza virus in hemopoietic mouse chimeras. Role of mononuclear phagocytes. J Exp Med 150:117-126.
18. Blazejewska P, Koscinski L, Viegas N, Anhlan D, Ludwig S, Schughart K. 2011. Pathogenicity of different PR8 influenza A virus variants in mice is determined by both viral and host factors. Virology 412:36-45. http://dx.doi.org/10.1016/j.virol.2010.12.047.
19. Keppner A, Andreasen D, Merillat AM, Bapst J, Ansermet C, Wang Q, Maillard M, Malsure S, Nobile A, Hummler E. 2015. Epithelial sodium channel-mediated sodium transport is not dependent on the membranebound serine protease CAP2/Tmprss4. PLoS One 10:e0135224. http://dx.doi.org/10.1371/journal.pone.0135224.
20. Kim TS, Heinlein C, Hackman RC, Nelson PS. 2006. Phenotypic analysis of mice lacking the Tmprss2-encoded protease. Mol Cell Biol 26:965-975. http://dx.doi.org/10.1128/MCB.26.3.965-975.2006.
21. Wilk E, Schughart K. 2012. The mouse as model system to study hostpathogen interactions in influenza A infections. Curr Protoc Mouse Biol 2:177-205. http://dx.doi.org/10.1002/9780470942390.mo110173.
22. 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.
23. van den Brand JM, Stittelaar KJ, van Amerongen G, Rimmelzwaan GF, Simon J, de Wit E, Munster V, Bestebroer T, Fouchier RA, Kuiken T, Osterhaus AD. 2010. Severity of pneumonia due to new H1N1 influenza virus in ferrets is intermediate between that due to seasonal H1N1 virus and highly pathogenic avian influenza H5N1 virus. J Infect Dis 201:993-999. http://dx.doi.org/10.1086/651132.
24. Bertram S, Heurich A, Lavender H, Gierer S, Danisch S, Perin P, Lucas JM, Nelson PS, Pohlmann S, Soilleux EJ. 2012. Influenza and SARScoronavirus activating proteases TMPRSS2 and HAT are expressed at multiple sites in human respiratory and gastrointestinal tracts. PLoS One 7:e35876. http://dx.doi.org/10.1371/journal.pone.0035876.
25. Weinheimer VK, Becher A, Tonnies M, Holland G, Knepper J, Bauer TT, Schneider P, Neudecker J, Ruckert JC, Szymanski K, Temmesfeld-Wollbrueck B, Gruber AD, Bannert N, Suttorp N, Hippenstiel S, Wolff T, Hocke AC. 2012. Influenza A viruses target type II pneumocytes in the human lung. J Infect Dis 206:1685-1694. http://dx.doi.org/10.1093/infdis/jis455.
26. Koerner I, Matrosovich MN, Haller O, Staeheli P, Kochs G. 2012. Altered receptor specificity and fusion activity of the haemagglutinin contribute to high virulence of a mouse-adapted influenzaAvirus. J Gen Virol 93:970-979. http://dx.doi.org/10.1099/vir.0.035782-0.
27. Chaipan C, Kobasa D, Bertram S, Glowacka I, Steffen I, Tsegaye TS, Takeda M, Bugge TH, Kim S, Park Y, Marzi A, Pohlmann S. 2009. Proteolytic activation of the 1918 influenza virus hemagglutinin. J Virol 83:3200-3211. http://dx.doi.org/10.1128/JVI.02205-08.
28. Dengler L, Kuhn N, Shin DL, Hatesuer B, Schughart K, Wilk E. 2014. Cellular changes in blood indicate severe respiratory disease during influenza infections in mice. PLoS One 9:e103149. http://dx.doi.org/10.1371/journal.pone.0103149.
29. Hamilton BS, Gludish DW, Whittaker GR. 2012. Cleavage activation of the human-adapted influenza virus subtypes by matriptase reveals both subtype and strain specificities. J Virol 86:10579-10586. http://dx.doi.org/10.1128/JVI.00306-12.
30. Hamilton BS, Whittaker GR. 2013. Cleavage activation of humanadapted influenza virus subtypes by kallikrein-related peptidases 5 and 12. J Biol Chem 288:17399-17407. http://dx.doi.org/10.1074/jbc.M112.440362.
31. Zmora P, Blazejewska P, Moldenhauer AS, Welsch K, Nehlmeier I, Wu Q, Schneider H, Pohlmann S, Bertram S. 2014. DESC1 and MSPL activate influenza A viruses and emerging coronaviruses for host cell entry. J Virol 88:12087-12097. http://dx.doi.org/10.1128/JVI.01427-14.
32. Cheng Z, Zhou J, To KK, Chu H, Li C, Wang D, Yang D, Zheng S, Hao K, Bosse Y, Obeidat M, Brandsma CA, Song YQ, Chen Y, Zheng BJ, Li L, Yuen KY. 2015. Identification of TMPRSS2 as a susceptibility gene for severe 2009 pandemic A(H1N1) influenza and A(H7N9) influenza. J Infect Dis 212:1214-1221. http://dx.doi.org/10.1093/infdis/jiv246.
33. Böttcher-Friebertshauser E, Freuer C, Sielaff F, Schmidt S, Eickmann M, Uhlendorff J, Steinmetzer T, Klenk HD, Garten W. 2010. Cleavage of influenza virus hemagglutinin by airway proteases TMPRSS2 and HAT differs in subcellular localization and susceptibility to protease inhibitors. J Virol 84:5605-5614. http://dx.doi.org/10.1128/JVI.00140-10.
34. Min HJ, Lee MK, Lee JW, Kim S. 2014. TMPRSS4 induces cancer cell invasion through pro-uPA processing. Biochem Biophys Res Commun 446:1-7. http://dx.doi.org/10.1016/j.bbrc.2014.01.013.
35. Passero CJ, Mueller GM, Myerburg MM, Carattino MD, Hughey RP, Kleyman TR. 2012. TMPRSS4-dependent activation of the epithelial sodium channel requires cleavage of the gamma-subunit distal to the furin cleavage site. Am J Physiol Renal Physiol 302:F1-F8. http://dx.doi.org/10.1152/ajprenal.00330.2011.
36. de Aberasturi AL, Calvo A. 2015. TMPRSS4: an emerging potential therapeutic target in cancer. Br J Cancer 112:4-8. http://dx.doi.org/10.1038/bjc.2014.403.
37. Planes C, Leyvraz C, Uchida T, Angelova MA, Vuagniaux G, Hummler E, Matthay M, Clerici C, Rossier B. 2005. In vitro and in vivo regulation of transepithelial lung alveolar sodium transport by serine proteases.AmJ Physiol Lung Cell Mol Physiol 288:L1099-L1109. http://dx.doi.org/10.1152/ajplung.00332.2004.
38. Wallrapp C, Hahnel S, Muller-Pillasch F, Burghardt B, Iwamura T, Ruthenburger M, Lerch MM, Adler G, Gress TM. 2000. A novel transmembrane serine protease (TMPRSS3) overexpressed in pancreatic cancer. Cancer Res 60:2602-2606.
39. Hansen IA, Fassnacht M, Hahner S, Hammer F, Schammann M, Meyer SR, Bicknell AB, Allolio B. 2004. The adrenal secretory serine protease AsP is a short secretory isoform of the transmembrane airway trypsin-like protease. Endocrinology 145:1898-1905. http://dx.doi.org/10.1210/en.2003-0930.
40. Sales KU, Hobson JP, Wagenaar-Miller R, Szabo R, Rasmussen AL, Bey A, Shah MF, Molinolo AA, Bugge TH. 2011. Expression and genetic loss of function analysis of the HAT/DESC cluster proteases TMPRSS11A and HAT. PLoS One 6:e23261. http://dx.doi.org/10.1371/journal.pone.0023261.
41. Bahgat MM, Blazejewska P, Schughart K. 2011. Inhibition of lung serine proteases in mice: a potentially new approach to control influenza infection. Virol J 8:27. http://dx.doi.org/10.1186/1743-422X-8-27.
42. Ovcharenko AV, Zhirnov OP. 1994. Aprotinin aerosol treatment of influenza and paramyxovirus bronchopneumonia of mice. Antiviral Res 23:107-118.
43. Zhirnov OP, Ovcharenko AV, Bukrinskaya AG. 1984. Suppression of influenza virus replication in infected mice by protease inhibitors. J Gen Virol 65:191-196. http://dx.doi.org/10.1099/0022-1317-65-1-191.
44. Zhirnov OP. 1987. High protection of animals lethally infected with influenza virus by aprotinin-rimantadine combination. J Med Virol 21:161-167. http://dx.doi.org/10.1002/jmv.1890210208.
45. Zhirnov OP, Klenk HD, Wright PF. 2011. Aprotinin and similar protease inhibitors as drugs against influenza. Antiviral Res 92:27-36. http://dx.doi.org/10.1016/j.antiviral.2011.07.014.