Novel type II transmembrane serine proteases, MSPL and TMPRSS13, proteolytically activate membrane fusion activity of the hemagglutinin of highly pathogenic avian influenza viruses and induce their multicycle replication

Journal of Virology

Volumn 84, Issue 10, 2010, Pages 5089-5096

  Okumura, Yuushi ^a   Takahashi, Etsuhisa ^a   Yano, Mihiro ^a   Ohuchi, Masanobu ^b   Daidoji, Tomo ^c   Nakaya, Takaaki ^c   Böttcher, Eva ^d   Garten, Wolfgang ^d   Klenk, Hans Dieter ^d   Kido, Hiroshi ^a  

^a UNIVERSITY OF TOKUSHIMA   (Japan)

^b KAWASAKI MEDICAL SCHOOL   (Japan)

^c OSAKA UNIVERSITY   (Japan)

^d PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; HEMAGGLUTININ; SERINE PROTEINASE; TRANSMEMBRANE SERINE PROTEASE 2; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DNA CLEAVAGE; FOWL; HUMAN; HUMAN CELL; INFLUENZA VIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; VIRUS REPLICATION;

CELL LINE; HEMAGGLUTININS, VIRAL; HOST-PATHOGEN INTERACTIONS; HUMANS; INFLUENZA A VIRUS; MEMBRANE PROTEINS; SERINE ENDOPEPTIDASES; VIRUS INTERNALIZATION; VIRUS REPLICATION;

AVIAN INFLUENZA VIRUS; ORTHOMYXOVIRIDAE;

EID: 77951433024     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02605-09     Document Type: Article

References (42)

1. Barr, P. J. 1991. Mammalian subtilisins: the long-sought dibasic processing endoproteases. Cell 66:1-3.
2. Basak, A., M. Zhong, J. S. Munzer, M. Chrétien, and N. G. Seidah. 2001. Implication of the proprotein convertases furin, PC5 and PC7 in the cleavage of surface glycoproteins of Hong Kong, Ebola and respiratory syncytial viruses: a comparative analysis with fluorogenic peptides. Biochem. J. 353: 537-545. (Pubitemid 32158322)
3. Basler, C. F., A. H. Reid, J. K. Dybing, T. A. Janczewski, T. G. Fanning, H. Zheng, M. Salvatore, M. L. Perdue, D. E. Swayne, A. García-Sastre, P. Palese, and J. K. Taubenberger. 2001. Sequence of the 1918 pandemic influenza virus nonstructural gene (NS) segment and characterization of recombinant viruses bearing the 1918 NS genes. Proc. Natl. Acad. Sci. U. S. A. 98:2746-2751.
4. Beppu, Y., Y. Imamura, M. Tashiro, T. Towatari, H. Ariga, and H. Kido. 1997. Human mucus protease inhibitor in airway fluids is a potential defensive compound against infection with influenza A and Sendai viruses. J. Biochem. 121:309-316. (Pubitemid 27096207)
5. Böttcher, E., T. Matrosovich, M. Beyerle, H. D. Klenk, W. Garten, and M. Matrosovich. 2006. Proteolytic activation of influenza viruses by serine proteases TMPRSS2 and HAT from human airway epithelium. J. Virol. 80: 9896-9898. (Pubitemid 44435664)
6. Chaipan, C., D. Kobasa, S. Bertram, I. Glowacka, I. Steffen, T. S. Tsegaye, M. Takeda, T. H. Bugge, S. Kim, Y. Park, A. Marzi, and S. Pöhlmann. 2009. Proteolytic activation of the 1918 influenza virus hemagglutinin. J. Virol. 83:3200-3211.
7. Daidoji, T., T. Koma, A. Du, C. S. Yang, M. Ueda, K. Ikuta, and T. Nakaya. 2008. H5N1 avian influenza virus induces apoptotic cell death in mammalian airway epithelial cells. J. Virol. 82:11294-11307.
8. Du, A., T. Daidoji, T. Koma, M. S. Ibrahim, S. Nakamura, U. C. de Silva, M. Ueda, C. S. Yang, T. Yasunaga, K. Ikuta, and T. Nakaya. 2009. Detection of circulating Asian H5N1 viruses by a newly established monoclonal antibody. Biochem. Biophys. Res. Commun. 378:197-202.
9. Feldmann, A., M. K. Schäfer, W. Garten, and H. D. Klenk. 2000. Targeted infection of endothelial cells by avian influenza virus A/FPV/Rostock/34 (H7N1) in chicken embryos. J. Virol. 74:8018-8027. (Pubitemid 30641647)
10. Fodor, E., L. Devenish, O. G. Engelhardt, P. Palese, G. G. Brownlee, and A. García-Sastre. 1999. Rescue of influenza A virus from recombinant DNA. J. Virol. 73:9679-9682. (Pubitemid 29487131)
11. Hallenberger, S., V. Bosch, H. Angliker, E. Shaw, H. D. Klenk, and W. Garten. 1992. Inhibition of furin-mediated cleavage activation of HIV-1 glycoprotein gp160. Nature 360:358-361. (Pubitemid 23000676)
12. Hatsuzawa, K., M. Nagahama, S. Takahashi, K. Takada, K. Murakami, and K. Nakayama. 1992. Purification and characterization of furin, a Kex2-like processing endoprotease, produced in Chinese hamster ovary cells. J. Biol. Chem. 267:16094-16099.
13. Horimoto, T., K. Nakayama, S. P. Smeekens, and Y. Kawaoka. 1994. Proprotein-processing endoproteases PC6 and furin both activate hemagglutinin of virulent avian influenza viruses. J. Virol. 68:6074-6078. (Pubitemid 24258628)
14. Hosaka, M., M. Nagahama, W. S. Kim, T. Watanabe, K. Hatsuzawa, J. Ikemizu, K. Murakami, and K. Nakayama. 1991. Arg-X-Lys/Arg-Arg motif as a signal for precursor cleavage catalyzed by furin within the constitutive secretory pathway. J. Biol. Chem. 266:12127-12130.
15. Jean, F., L. Thomas, S. S. Molloy, G. Liu, M. A. Jarvis, J. A. Nelson, and G. Thomas. 2000. A protein-based therapeutic for human cytomegalovirus infection. Proc. Natl. Acad. Sci. U. S. A. 97:2864-2869.
16. Kawaoka, Y., C. W. Naeve, and R. G. Webster. 1984. Is virulence of H5N2 influenza viruses in chickens associated with loss of carbohydrate from the hemagglutinin? Virology 139:303-316.
17. Kido, H., and Y. Okumura. 2008. MSPL/TMPRSS13. Front. Biosci. 13:754-758.
18. Kido, H., M. Murakami, K. Oba, Y. Chen, and T. Towatari. 1999. Cellular proteinases trigger the infectivity of influenza A and Sendai viruses. Mol. Cells 9:235-244. (Pubitemid 129555786)
19. Kido, H., Y. Yokogoshi, K. Sakai, M. Tashiro, Y. Kishino, A. Fukutomi, and N. Katunuma. 1992. Isolation and characterization of a novel trypsin-like protease found in rat bronchiolar epithelial Clara cells. A possible activator of the viral fusion glycoprotein. J. Biol. Chem. 267:13573-13579.
20. Kim, D. R., S. Sharmin, M. Inoue, and H. Kido. 2001. Cloning and expression of novel mosaic serine proteases with and without a transmembrane domain from human lung. Biochim. Biophys. Acta 1518:204-209.
21. Klenk, H. D., and W. Garten. 1994. Host cell proteases controlling virus pathogenicity. Trends Microbiol. 2:39-43.
22. Klenk, H. D., R. Rott, M. Orlich, and J. Blödorn. 1975. Activation of influenza A viruses by trypsin treatment. Virology 68:426-439.
23. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
24. Le, T. Q., M. Kawachi, H. Yamada, M. Shiota, Y. Okumura, and H. Kido. 2006. Identification of trypsin I as a candidate for influenza A virus and Sendai virus envelope glycoprotein processing protease in rat brain. Biol. Chem. 387:467-475.
25. Murakami, M., T. Towatari, M. Ohuchi, M. Shiota, M. Akao, Y. Okumura, M. A. Parry, and H. Kido. 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.
26. Netzel-Arnett, S., J. D. Hooper, R. Szabo, E. L. Madison, J. P. Quigley, T. H. Bugge, and T. M. Antalis. 2003. Membrane anchored serine proteases: a rapidly expanding group of cell surface proteolytic enzymes with potential roles in cancer. Cancer Metastasis Rev. 22:237-258. (Pubitemid 36561060)
27. Ohuchi, M., A. Cramer, M. Vey, R. Ohuchi, W. Garten, and H. D. Klenk. 1994. Rescue of vector-expressed fowl plague virus hemagglutinin in biologically active form by acidotropic agents and coexpressed M2 protein. J. Virol. 68:920-926. (Pubitemid 24022195)
28. Ohuchi, M., M. Orlich, R. Ohuchi, B. E. Simpson, W. Garten, H. D. Klenk, and R. Rott. 1989. Mutations at the cleavage site of the hemagglutinin alter the pathogenicity of influenza virus A/chick/Penn/83 (H5N2). Virology 168: 274-280. (Pubitemid 19073305)
29. Ohuchi, R., M. Ohuchi, W. Garten, and H. D. Klenk. 1991. Human influenza virus hemagglutinin with high sensitivity to proteolytic activation. J. Virol. 65:3530-3537.
30. Ohuchi, R., M. Ohuchi, W. Garten, and H. D. Klenk. 1997. Oligosaccharides in the stem region maintain the influenza virus hemagglutinin in the meta-stable form required for fusion activity. J. Virol. 71:3719-3725. (Pubitemid 27172384)
31. Okumura, Y., M. Hayama, E. Takahashi, M. Fujiuchi, A. Shimabukuro, M. Yano, and H. Kido. 2006. Serase-1B, a new splice variant of polyserase-1/ TMPRSS9, activates urokinase-type plasminogen activator and the proteolytic activation is negatively regulated by glycosaminoglycans. Biochem. J. 400:551-561. (Pubitemid 44974467)
32. Okumura, Y., H. Sato, M. Seiki, and H. Kido. 1997. Proteolytic activation of the precursor of membrane type 1 matrix metalloproteinase by human plasmin. A possible cell surface activator. FEBS Lett. 402:181-184.
33. Remacle, A. G., S. A. Shiryaev, E. S. Oh, P. Cieplak, A. Srinivasan, G. Wei, R. C. Liddington, B. I. Ratnikov, A. Parent, R. Desjardins, R. Day, J. W. Smith, M. Lebl, and A. Y. Strongin. 2008. Substrate cleavage analysis of furin and related proprotein convertases. A comparative study. J. Biol. Chem. 283:20897-20906.
34. Steiner, D. F. 1998. The proprotein convertases. Curr. Opin. Chem. Biol. 2:31-39.
35. Stieneke-Gröber, A., M. Vey, H. Angliker, E. Shaw, G. Thomas, C. Roberts, H. D. Klenk, and W. Garten. 1992. Influenza virus hemagglutinin with multibasic cleavage site is activated by furin, a subtilisin-like endoprotease. EMBO J. 11:2407-2414.
36. Szabo, R., and T. H. Bugge. 2008. Type II transmembrane serine proteases in development and disease. Int. J. Biochem. Cell Biol. 40:1297-1316.
37. Szabo, R., Q. Wu, R. B. Dickson, S. Netzel-Arnett, T. M. Antalis, and T. H. Bugge. 2003. Type II transmembrane serine proteases. Thromb. Haemost. 90:185-193.
38. Thomas, G. 2002. Furin at the cutting edge: from protein traffic to embryogenesis and disease. Nat. Rev. Mol. Cell Biol. 3:753-766.
39. Towatari, T., M. Ide, K. Ohba, Y. Chiba, M. Murakami, M. Shiota, M. Kawachi, H. Yamada, and H. Kido. 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.
40. Walker, J. A., S. S. Molloy, G. Thomas, T. Sakaguchi, T. Yoshida, T. M. Chambers, and Y. Kawaoka. 1994. Sequence specificity of furin, a proprotein-processing endoprotease, for the hemagglutinin of a virulent avian influenza virus. J. Virol. 68:1213-1218. (Pubitemid 24022230)
41. WHO/OIE/FAO H5N1 Evolution Working Group. 2008. Toward a unified nomenclature system for highly pathogenic avian influenza virus (H5N1). Emerg. Infect. Dis. 14:e1.
42. Zhirnov, O. P., M. R. Ikizler, and P. F. Wright. 2002. Cleavage of influenza A virus hemagglutinin in human respiratory epithelium is cell associated and sensitive to exogenous antiproteases. J. Virol. 76:8682-8689.