The serine protease inhibitor camostat inhibits influenza virus replication and cytokine production in primary cultures of human tracheal epithelial cells

Pulmonary Pharmacology and Therapeutics

Volumn 33, Issue , 2015, Pages 66-74

  Yamaya, Mutsuo ^a   Shimotai, Yoshitaka ^b   Hatachi, Yukimasa ^c,d   Lusamba Kalonji, Nadine ^a   Tando, Yukiko ^a   Kitajima, Yasuo ^a   Matsuo, Kaori ^a   Kubo, Hiroshi ^a   Nagatomi, Ryoichi ^a   Hongo, Seiji ^b   Homma, Morio ^e   Nishimura, Hidekazu ^e  

^a TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b YAMAGATA UNIVERSITY   (Japan)

^c KOBE CITY MEDICAL CENTER GENERAL HOSPITAL   (Japan)

^d KYOTO UNIVERSITY   (Japan)

^e SENDAI CITY MEDICAL CENTER   (Japan)

Author keywords

Airway epithelial cell; Camostat; Cell culture; Influenza; Interleukin; Serine protease

Indexed keywords

APROTININ; CAMOSTAT; GABEXATE; SIVELESTAT; VIRUS RNA; SERINE PROTEINASE INHIBITOR;

ANIMAL CELL; ARTICLE; CYTOKINE PRODUCTION; CYTOKINE RELEASE; EPITHELIUM CELL; HUMAN; HUMAN CELL; INFLUENZA VIRUS; INFLUENZA VIRUS A H1N1; INFLUENZA VIRUS A H3N2; MDCK CELL LINE; NONHUMAN; PRIMARY CULTURE; PRIORITY JOURNAL; RNA REPLICATION; SCANNING ELECTRON MICROSCOPY; TRACHEA MUCOSA; VIRUS REPLICATION; WESTERN BLOTTING; AGED; ANALOGS AND DERIVATIVES; ANIMAL; CELL CULTURE; CYTOLOGY; DOG; DRUG EFFECTS; FEMALE; INFLUENZA A VIRUS (H1N1); INFLUENZA A VIRUS (H3N2); INFLUENZA, HUMAN; ISOLATION AND PURIFICATION; MALE; METABOLISM; MIDDLE AGED; TRACHEA; VIROLOGY;

AGED; ANIMALS; APROTININ; CELLS, CULTURED; DOGS; EPITHELIAL CELLS; FEMALE; GABEXATE; HUMANS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA A VIRUS, H3N2 SUBTYPE; INFLUENZA, HUMAN; MADIN DARBY CANINE KIDNEY CELLS; MALE; MIDDLE AGED; RNA, VIRAL; SERINE PROTEINASE INHIBITORS; TRACHEA; VIRUS REPLICATION;

EID: 84938519998     PISSN: 10945539     EISSN: 15229629     Source Type: Journal    
DOI: 10.1016/j.pupt.2015.07.001     Document Type: Article

References (54)

1. Hayden F.G., Gwaltney J.M. Viral infections. Textbook of Respiratory Medicine 1988, 748-802. Saunders Co, Philadelphia. J. Murray, J.A. Nadel (Eds.).
2. Perez-Padilla R., de la Rosa-Zamboni D., Ponce de Leon S., Hernandez M., Quinones-Falconi F., Bautista E., et al. INER Working Group on influenza, Pneumonia and respiratory failure from swine-origin influenza A (H1N1) in Mexico. N.Engl. J. Med. 2009, 361:680-689.
3. Minor T.E., Dick E.C., Baker J.W., Ouellette J.J., Cohen M., Reed C.E. Rhinovirus and influenza type A infections as precipitants of asthma. Am. Rev. Respir. Dis. 1976, 113:149-153.
4. Rohde G., Wiethege A., Borg I., Kauth M., Bauer T.T., Gillissen A., et al. Respiratory viruses in exacerbations of chronic obstructive pulmonary disease requiring hospitalisation: a case-control study. Thorax 2003, 58:37-42.
5. Nichol K.L., Margolis K.L., Wuorenma J., Von Sternberg T. The efficacy and cost effectiveness of vaccination against influenza among elderly persons living in the community. N.Engl. J. Med. 1994, 331:778-784.
6. Glezen W.P. Asthma, influenza, and vaccination. J.Allergy Clin. Immunol. 2006, 118:1199-1206.
7. Puig-Barbera J., Arnedo-Pena A., Pardo-Serrano F., Tirado-Balaguer M.D., Perez-Vilar S., Silvestre-Silvestre E., et al. Surveillance and Vaccine Evaluation Group during the autumn 2009 H1N1 pandemic wave in Castellon, Spain, Effectiveness of seasonal 2008-2009, 2009-2010 and pandemic vaccines, to prevent influenza hospitalizations during the autumn 2009 influenza pandemic wave in Castellon, Spain. A test-negative, hospital-based, case-control study. Vaccine 2010, 28:7460-7467.
8. Treanor J.J., Hayden F.G., Vrooman P.S., Barbarash R., Bettis R., Riff D., et al. Efficacy and safety of the oral neuraminidase inhibitor oseltamivir in treating acute influenza: a randomized controlled trial. US Oral Neuraminidase Study Group. JAMA 2000, 283:1016-1024.
9. Kumar A. Early versus late oseltamivir treatment in severely ill patients with 2009 pandemic influenza A (H1N1): speed is life. J.Antimicrob. Chemother. 2011, 66:959-963.
10. de Jong M.D., Simmons C.P., Thanh T.T., Hien V.M., Smith G.J., Chau T.N., et al. Fatal outcome of human influenza A (H5N1) is associated with high viral load and hypercytokinemia. Nat. Med. 2006, 12:1203-1207.
11. Paquette S.G., Banner D., Zhao Z., Fang Y., Huang S.S., Leon A.J., et al. Interleukin-6 is a potential biomarker for severe pandemic H1N1 influenza A infection. PLoS One 2012, 7:e38214.
12. Gooskens J., Jonges M., Claas E.C., Meijer A., van den Broek P.J., Kroes A.M. Morbidity and mortality associated with nosocomial transmission of oseltamivir-resistant influenza A (H1N1) virus. JAMA 2009, 301:1042-1046.
13. Homma M. Trypsin action on the growth of Sendai virus in tissue culture cells. I. Restoration of the infectivity for L cells by direct action of trypsin on L cell-borne Sendai virus. J.Virol. 1971, 8:619-629.
14. Ohuchi M., Homma M. Trypsin action on the growth of Sendai virus in tissue culture cells. IV. Evidence for activation of sendai virus by cleavage of a glycoprotein. J.Virol. 1976, 18:1147-1150.
15. Nagai Y. Protease-dependent virus tropism and pathogenicity. Trends Microbiol. 1993, 1:81-87.
16. Klenk H.D., Garten W. Host cell protease controlling virus pathogenicity. Trends Microbiol. 1994, 2:39-43.
17. Klenk H.D., Rott R., Orlich M., Blödorn J. Activation of influenza A viruses by trypsin treatment. Virology 1975, 68:426-439.
18. Böttcher E., Matrosovich T., Beyerle M., Klenk H.D., Garten W., Matrosovich M. Proteolytic activation of influenza viruses by serine proteases TMPRSS2 and HAT from human airway epithelium. J.Virol. 2006, 80:9896-9898.
19. Zhirnov O.P., Klenk H.D., Wright P.F. Aprotinin and similar protease inhibitors as drugs against influenza. Antivir. Res. 2011, 92:27-36.
20. Hosoya M., Matsuyama S., Baba M., Suzuki H., Shigeta S. Effects of protease inhibitors on replication of various myxoviruses. Antimicrob. Agents Chemother. 1992, 36:1432-1436.
21. Lee M.G., Kim K.H., Park K.Y., Kim J.S. Evaluation of anti-influenza effects of camostat in mice infected with non-adapted human influenza viruses. Arch. Virol. 1996, 141:1979-1989.
22. Zhirnov O.P., Ikizler M.R., Wright P. Cleavage of influenza A virus hemagglutinin in human respiratory epithelium is cell-associated and sensitive to exogenous antiproteases. J.Virol. 2002, 76:8682-8689.
23. Hayakawa M., Katabami K., Wada T., Sugano M., Hoshino H., Sawamura A., et al. Sivelestat (selective neutrophil elastase inhibitor) improves the mortality rate of sepsis associated with both respiratory distress syndrome and disseminated intravascular coagulation patients. Shock 2010, 33:14-18.
24. Yamaya M., Finkbeiner W.E., Chun S.Y., Widdicombe J.H. Differentiated structure and function of cultures from human tracheal epithelium. Am. J. Physiol. 1992, 262:L713-L724.
25. Yamaya M., Shinya K., Hatachi Y., Kubo H., Asada M., Yasuda H., et al. Clarithromycin inhibits type A seasonal influenza virus infection in human airway epithelial cells. J.Pharmacol. Exp. Ther. 2010, 333:81-90.
26. Numazaki Y., Oshima T., Ohmi A., Tanaka A., Oizumi Y., Komatsu S., et al. Amicroplate method for isolation of viruses from infants and children with acute respiratory infections. Microbiol. Immunol. 1987, 31:1085-1095.
27. Condit R.C. Principles of virology. Fields Virology 2006, vol 1:25-57. Lippincott Williams & Wilkins Inc, Philadelphia. fifth ed.
28. Lorusso A., Faaberg K.S., Killian M.L., Koster L., Vincent A.L. One-step real-time RT-PCR for pandemic influenza A virus (H1N1) 2009 matrix gene detection in swine samples. J.Virol. Methods 2010, 164:83-87.
29. Yamaya M., Lusamba N., Ota C., Kubo H., Makiguchi T., Nagatomi R., et al. Magnitude of influenza virus replication and cell damage is associated with interleukin-6 production in primary cultures of human tracheal epithelium. Respir. Physiol. Neurobiol. 2014, 202:16-23.
30. Peitsch C., Klenk H.D., Garten W., Böttcher-Friebertshauser E. Activation of influenza A viruses by host proteases from swine airway epithelium. J.Virol. 2014, 88:282-291.
31. Bertram S., Glowacka I., Blazejewska P., Soilleux E., Allen P., Danisch S., et al. TMPRSS2 and TMPRSS4 facilitate trypsin-independent spread of influenza virus in Caco-2 cells. J.Virol. 2010, 84:10016-10025.
32. Bertram S., Dijkman R., Habjan M., Heurich A., Gierer S., Glowacka I., et al. TMPRSS2 activates the human coronavirus 229E for cathepsin-independent host cell entry and is expressed in viral target cells in the respiratory epithelium. J.Virol. 2013, 87:6150-6160.
33. Hiraku S., Muryobayashi K., Ito H., Inagawa T., Tuboshima M. Absorption and excretion of camostat (FOY-305) orally administered to male rabbit and healthy subjects (English Abstract). Iyaku Kenkyu 1982, 13:756-765.
34. Lin B., Ferguson C., White J.T., Wang S., Vessella R., True L.D., et al. Prostate-localized and androgen-regulated expression of the membrane-bound serine protease TMPRSS2. Cancer Res. 1999, 59:4180-4184.
35. Donaldson S.H., Hirsh A., Li D.C., Holloway G., Chao J., Boucher R.C., et al. Regulation of the epithelial sodium channel by serine proteases in human airways. J.Biol. Chem. 2002, 277:8338-8345.
36. Yamaoka K., Masuda K., Ogawa H., Takagi K., Umemoto N., Yasuoka S. Cloning and characterization of the cDNA for human airway trypsin-like protease. J.Biol. Chem. 1998, 273:11895-11901.
37. Ohler A., Becker-Pauly C. TMPRSS4 is a type II transmembrane serine protease involved in cancer and viral infections. Biol. Chem. 2012, 393:907-914.
38. Chokki M., Yamamura S., Eguchi H., Masegi T., Horiuchi H., Tanabe H., et al. Human airway trypsin-like protease increases mucin gene expression in airway epithelial cells. Am. J. Respir. Cell Mol. Biol. 2004, 30:470-478.
39. Coote K., Atherton-Watson H.C., Sugar R., Young A., MacKenzie-Beevor A., Gosling M., et al. Camostat attenuates airway epithelial sodium channel function invivo through the inhibition of a channel-activating protease. J.Pharmacol. Exp. Ther. 2009, 329:764-774.
40. Kawase M., Shirato K., van der Hoek L., Taguchi F., Matsuyama S. Simultaneous treatment of human bronchial epithelial cells with serine and cysteine protease inhibitors prevents severe acute respiratory syndrome coronavirus entry. J.Virol. 2012, 86:6537-6545.
41. Sieczkarski S.B., Brown H.A., Whittaker G.R. Role of protein kinase C βII in influenza virus entry via late endosomes. J.Virol. 2003, 77:460-469.
42. Matsuyama S., Nagata N., Shirato K., Kawase M., Takeda M., Taguchi F. Efficient activation of the severe acute respiratory syndrome coronavirus spike protein by the transmembrane protease TMPRSS2. J.Virol. 2010, 84:12658-12664.
43. Tumurkhuu G., Koide N., Hiwasa T., Ookoshi M., Dagvadorj J., Abu Shadat Mohammod Noman, et al. ONO 3403, a synthetic serine protease inhibitor, inhibits lipopolysaccharide-induced tumor necrosis factor-α and nitric oxide production and protects mice from lethal endotoxic shock. Innate Immun. 2011, 17:97-105.
44. Kosai K., Seki M., Yanagihara K., Nakamura S., Kurihara S., Izumikawa K., et al. Gabexate mesilate suppresses influenza pneumonia in mice through inhibition of cytokines. J.Int. Med. Res. 2008, 36:322-328.
45. Asimakopoulos G., Lidington E.A., Mason J., Haskard D.O., Taylor K.M., Landis R.C. Effect of aprotinin on endothelial cell activation. J.Thorac. Cardiovasc. Surg. 2001, 122:123-128.
46. Buerke M., Pruefer D., Sankat D., Carter J.M., Buerke U., Russ M., et al. Effects of aprotinin on gene expression and protein synthesis after ischemia and reperfusion in rats. Circulation 2007, 116(Suppl I):I121-I126.
47. Hayden F.G., Fritz R., Lobo M.C., Alvord W., Strober W., Straus S.E. Local and systemic cytokine responses during experimental human influenza A virus infection. Relation to symptom formation and host defense. J.Clin. Invest. 1998, 101:643-649.
48. Iwadou H., Morimoto Y., Iwagaki H., Sinoura S., Chouda Y., Kodama M., et al. Differential cytokine response in host defence mechanisms triggered by gram-negative and gram-positive bacteria, and the roles of gabexate mesilate, a synthetic protease inhibitor. J.Intern. Med. Res. 2002, 30:99-108.
49. Kawabata K., Suzuki M., Sugitani M., Imaki K., Toda M., Miyamoto T. ONO-5046, a novel inhibitor of human neutrophil elastase. Biochem. Biophys. Res. Commun. 1991, 177:814-820.
50. Tamura Y., Hirado M., Okamura K., Minato Y., Fujii S. Synthetic inhibitors of trypsin, plasmin, kallikrein, thrombin, C1r-, and C1 esterase. Biochim. Biophys. Acta 1977, 484:417-422.
51. Nakatani K., Takeshita S., Tsujimoto H., Kawamura Y., Sekine I. Inhibitory effect of serine protease inhibitors on neutrophil-mediated endothelial cell injury. J.Leukoc. Biol. 2001, 69:241-247.
52. Fritz H., Wunderer G. Biochemistry and applications of aprotinin, the kallikrein inhibitor from bovine organs. Arzneimittelforschung 1983, 33:479-494.
53. Böttcher E., Freuer C., Steinmetzer T., Klenk H.D., Garten W. MDCK cells that express proteases TMPRSS2 and HAT provide a cell system to propagate influenza viruses in the absence of trypsin and to study cleavage of HA and its inhibition. Vaccine 2009, 27:6324-6329.
54. Sai J.K., Suyama M., Kubokawa Y., Matsumura Y., Inami K., Watanabe S. Efficacy of camostat mesilate against dyspepsia associated with non-alcoholic mild pancreatic disease. J.Gastroenterol. 2010, 45:335-341.