Advertisement

Membrane-Anchored Serine Proteases: Host Cell Factors in Proteolytic Activation of Viral Glycoproteins

  • Eva Böttcher-Friebertshäuser
Chapter
First Online:

Abstract

Over one third of all known proteolytic enzymes are serine proteases. Among these, the trypsin-like serine proteases comprise one of the best characterized subfamilies due to their essential roles in blood coagulation, food digestion, fibrinolysis, or immunity. Trypsin-like serine proteases possess primary substrate specificity for basic amino acids. Most of the well-characterized trypsin-like proteases such as trypsin, plasmin, or urokinase are soluble proteases that are secreted into the extracellular environment. At the turn of the millennium, a number of novel trypsin-like serine proteases have been identified that are anchored in the cell membrane, either by a transmembrane domain at the N- or C-terminus or via a glycosylphosphatidylinositol (GPI) linkage. Meanwhile more than 20 membrane-anchored serine proteases (MASPs) have been identified in human and mouse, and some of them have emerged as key regulators of mammalian development and homeostasis. Thus, the MASP corin and TMPRSS6/matriptase-2 have been demonstrated to be the activators of the atrial natriuretic peptide (ANP) and key regulator of hepcidin expression, respectively. Furthermore, MASPs have been recognized as host cell factors activating respiratory viruses including influenza virus as well as severe acute respiratory syndrome (SARS) and Middle East respiratory syndrome (MERS) coronaviruses. In particular, transmembrane protease serine S1 member 2 (TMPRSS2) has been shown to be essential for proteolytic activation and consequently spread and pathogenesis of a number of influenza A viruses in mice and as a factor associated with severe influenza virus infection in humans.

This review gives an overview on the physiological functions of the fascinating and rapidly evolving group of MASPs and a summary of the current knowledge on their role in proteolytic activation of viral fusion proteins.

Keywords

Membrane-anchored serine proteases (MASPs) Type II transmembrane serine proteases (TTSPs) Proteolytic activation Trypsin-like serine proteases Host protease Influenza virus Hemagglutinin Coronavirus TMPRSS2 Human airway trypsin-like protease (HAT) Severe acute respiratory syndrome (SARS) and Middle East respiratory syndrome (MERS) Matriptase TMPRSS4 TMPRSS6 TMPRSS13 Corin Prostasin Testisin Enteropeptidase 
This is a preview of subscription content, log in to check access.

References

  1. Abe M, Tahara M, Sakai K, Yamaguchi H, Kanou K, Shirato K, Kawase M, Noda M, Kimura H, Matsuyama S, Fukuhara H, Mizuta K, Maenaka K, Ami Y, Esumi M, Kato A, Takeda M. TMPRSS2 is an activating protease for respiratory parainfluenza viruses. J Virol. 2013;87:11930–5.PubMedPubMedCentralCrossRefGoogle Scholar
  2. Afar DE, Vivanco I, Hubert RS, Kuo J, Chen E, Saffran DC, Raitano AB, Jakobovits A. Catalytic cleavage of the androgen-regulated TMPRSS2 protease results in its secretion by prostate and prostate cancer epithelia. Cancer Res. 2001;61:1686–92.PubMedPubMedCentralGoogle Scholar
  3. Aimes RT, Zijlstra A, Hooper JD, Ogbourne SM, Sit ML, Fuchs S, Gotley DC, Quigley JP, Antalis TM. Endothelial cell serine proteases expressed during vascular morphogenesis and angiogenesis. Thromb Haemost. 2003;89:561–72.PubMedCrossRefGoogle Scholar
  4. Andreasen D, Vuagniaux G, Fowler-Jaeger N, Hummler E, Rossier BC. Activation of epithelial sodium channels by mouse channel activating proteases (mCAP) expressed in Xenopus oocytes requires catalytic activity of mCAP3 and mCAP2 but not mCAP1. J Am Soc Nephrol. 2006;17:968–76.PubMedCrossRefGoogle Scholar
  5. Antalis TM, Bugge TH, Wu Q. Membrane-anchored serine proteases in health and disease. Prog Mol Biol Transl Sci. 2011;99:1–50.PubMedPubMedCentralGoogle Scholar
  6. Appel LF, Prout M, Abu-Shumays R, Hammonds A, Garbe JC, Fristrom D, Fristrom J. The Drosophila Stubble-stubbloid gene encodes an apparent transmembrane serine protease required for epithelial morphogenesis. Proc Natl Acad Sci U S A. 1993;90:4937–41.PubMedPubMedCentralCrossRefGoogle Scholar
  7. Baba T, Azuma S, Kashiwabara S, Toyoda Y. Sperm from mice carrying a targeted mutation of the acrosin gene can penetrate the oocyte zona pellucida and effect fertilization. J Biol Chem. 1994;269:31845–9.PubMedPubMedCentralGoogle Scholar
  8. Babitt JL, Huang FW, Wrighting DM, Xia Y, Sidis Y, Samad TA, Campagna JA, Chung RT, Schneyer AL, Woolf CJ, Andrews NC, Lin HY. Bone morphogenetic protein signaling by hemojuvelin regulates hepcidin expression. Nat Genet. 2006;38:531–9.PubMedCrossRefGoogle Scholar
  9. Bao Y, Li K, Guo Y, Wang Q, Li Z, Yang Y, Chen Z, Wang J, Zhao W, Zhang H, Chen J, Dong H, Shen K, Diamond AM, Yang W. Tumor suppressor PRSS8 targets Sphk1/S1P/Stat3/Akt signaling in colorectal cancer. Oncotarget. 2016;7:26780–92.PubMedPubMedCentralGoogle Scholar
  10. Baron J, Tarnow C, Mayoli-Nüssle D, Schilling E, Meyer D, Hammami M, Schwalm F, Steinmetzer T, Guan Y, Garten W, Klenk HD, Böttcher-Friebertshäuser E. Matriptase, HAT, and TMPRSS2 activate the hemagglutinin of H9N2 influenza A viruses. J Virol. 2013;87:1811–20.PubMedPubMedCentralCrossRefGoogle Scholar
  11. Beaulieu A, Gravel É, Cloutier A, Marois I, Colombo É, Désilets A, Verreault C, Leduc R, Marsault É, Richter MV. Matriptase proteolytically activates influenza virus and promotes multicycle replication in the human airway epithelium. J Virol. 2013;87:4237–51.PubMedPubMedCentralCrossRefGoogle Scholar
  12. Béliveau F, Brulé C, Désilets A, Zimmerman B, Laporte SA, Lavoie CL, Leduc R. Essential role of endocytosis of the type II transmembrane serine protease TMPRSS6 in regulating its functionality. J Biol Chem. 2011;286:29035–43.PubMedPubMedCentralCrossRefGoogle Scholar
  13. Ben-Yosef T, Wattenhofer M, Riazuddin S, Ahmed ZM, Scott HS, Kudoh J, Shibuya K, Antonarakis SE, Bonne-Tamir B, Radhakrishna U, Naz S, Ahmed Z, Riazuddin S, Pandya A, Nance WE, Wilcox ER, Friedman TB, Morell RJ. Novel mutations of TMPRSS3 in four DFNB8/B10 families segregating congenital autosomal recessive deafness. J Med Genet. 2001;38:396–400.PubMedPubMedCentralCrossRefGoogle Scholar
  14. Bertram S, Glowacka I, Blazejewska P, Soilleux E, Allen P, Danisch S, Steffen I, Choi SY, Park Y, Schneider H, Schughart K, Pöhlmann S. TMPRSS2 and TMPRSS4 facilitate trypsin-independent spread of influenza virus in Caco-2 cells. J Virol. 2010;84:10016–25.PubMedPubMedCentralCrossRefGoogle Scholar
  15. Bertram S, Glowacka I, Müller MA, Lavender H, Gnirss K, Nehlmeier I, Niemeyer D, He Y, Simmons G, Drosten C, Soilleux EJ, Jahn O, Steffen I, Pöhlmann S. Cleavage and activation of the severe acute respiratory syndrome coronavirus spike protein by human airway trypsin-like protease. J Virol. 2011;85:13363–72.PubMedPubMedCentralCrossRefGoogle Scholar
  16. Bertram S, Heurich A, Lavender H, Gierer S, Danisch S, Perin P, Lucas JM, Nelson PS, Pöhlmann S, Soilleux EJ. Influenza and SARS-coronavirus activating proteases TMPRSS2 and HAT are expressed at multiple sites in human respiratory and gastrointestinal tracts. PLoS One. 2012;7:e35876.PubMedPubMedCentralCrossRefGoogle Scholar
  17. Bertram S, Dijkman R, Habjan M, Heurich A, Gierer S, Glowacka I, Welsch K, Winkler M, Schneider H, Hofmann-Winkler H, Thiel V, Pöhlmann S. 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;87:6150–60.PubMedPubMedCentralCrossRefGoogle Scholar
  18. Bosch FX, Garten W, Klenk HD, Rott R. Proteolytic cleavage of influenza virus hemagglutinins: primary structure of the connecting peptide between HA1 and HA2 determines proteolytic cleavability and pathogenicity of Avian influenza viruses. Virology. 1981;113:725–35.CrossRefGoogle Scholar
  19. Böttcher E, Matrosovich T, Beyerle M, Klenk HD, Garten W, Matrosovich M. Proteolytic activation of influenza viruses by serine proteases TMPRSS2 and HAT from human airway epithelium. J Virol. 2006;80:9896–8.PubMedPubMedCentralCrossRefGoogle Scholar
  20. Böttcher E, Freuer C, Steinmetzer T, Klenk HD, 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;27:6324–9.CrossRefPubMedGoogle Scholar
  21. Böttcher-Friebertshäuser E, Freuer C, Sielaff F, Schmidt S, Eickmann M, Uhlendorff J, Steinmetzer T, Klenk HD, Garten W. Cleavage of influenza virus hemagglutinin by airway proteases TMPRSS2 and HAT differs in subcellular localization and susceptibility to protease inhibitors. J Virol. 2010;84:5605–14.PubMedPubMedCentralCrossRefGoogle Scholar
  22. Böttcher-Friebertshäuser E, Stein DA, Klenk HD, Garten W. 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. 2011;85:1554–62.CrossRefPubMedGoogle Scholar
  23. Böttcher-Friebertshäuser E, Lu Y, Meyer D, Sielaff F, Steinmetzer T, Klenk HD, Garten W. Hemagglutinin activating host cell proteases provide promising drug targets for the treatment of influenza A and B virus infections. Vaccine. 2012;30:7374–80.CrossRefPubMedGoogle Scholar
  24. Böttcher-Friebertshäuser E, Klenk HD, Garten W. Activation of influenza viruses by proteases from host cells and bacteria in the human airway epithelium. Pathog Dis. 2013;69:87–100.PubMedPubMedCentralCrossRefGoogle Scholar
  25. Boycott R, Klenk HD, Ohuchi M. Cell tropism of influenza virus mediated by hemagglutinin activation at the stage of virus entry. Virology. 1994;203:313–9.CrossRefPubMedGoogle Scholar
  26. Brunati M, Perucca S, Han L, Cattaneo A, Consolato F, Andolfo A, Schaeffer C, Olinger E, Peng J, Santambrogio S, Perrier R, Li S, Bokhove M, Bachi A, Hummler E, Devuyst O, Wu Q, Jovine L, Rampoldi L. The serine protease hepsin mediates urinary secretion and polymerisation of Zona Pellucida domain protein uromodulin. Elife. 2015;4:e08887.PubMedPubMedCentralCrossRefGoogle Scholar
  27. Bruns JB, Carattino MD, Sheng S, Maarouf AB, Weisz OA, Pilewski JM, Hughey RP, Kleyman TR. Epithelial Na+ channels are fully activated by furin- and prostasin-dependent release of an inhibitory peptide from the gamma-subunit. J Biol Chem. 2007;282:6153–60.PubMedCrossRefGoogle Scholar
  28. Bugge TH, Antalis TM, Wu Q. Type II transmembrane serine proteases. J Biol Chem. 2009;284:23177–81. Review.PubMedPubMedCentralCrossRefGoogle Scholar
  29. Burkard C, Verheije MH, Wicht O, van Kasteren SI, van Kuppeveld FJ, Haagmans BL, Pelkmans L, Rottier PJ, Bosch BJ, de Haan CA. Coronavirus cell entry occurs through the endo-/lysosomal pathway in a proteolysis-dependent manner. PLoS Pathog. 2014;10:e1004502.PubMedPubMedCentralCrossRefGoogle Scholar
  30. Buzza MS, Netzel-Arnett S, Shea-Donohue T, Zhao A, Lin CY, List K, Szabo R, Fasano A, Bugge TH, Antalis TM. Membrane-anchored serine protease matriptase regulates epithelial barrier formation and permeability in the intestine. Proc Natl Acad Sci U S A. 2010;107:4200–5.PubMedPubMedCentralCrossRefGoogle Scholar
  31. Buzza MS, Martin EW, Driesbaugh KH, Désilets A, Leduc R, Antalis TM. Prostasin is required for matriptase activation in intestinal epithelial cells to regulate closure of the paracellular pathway. J Biol Chem. 2013;288:10328–37.PubMedPubMedCentralCrossRefGoogle Scholar
  32. Cal S, Quesada V, Garabaya C, Lopez-Otin C. Polyserase-I, a human polyprotease with the ability to generate independent serine protease domains from a single translation product. Proc Natl Acad Sci U S A. 2003;100:9185–90.PubMedPubMedCentralCrossRefGoogle Scholar
  33. Chaipan C, Kobasa D, Bertram S, Glowacka I, Steffen I, Tsegaye TS, Takeda M, Bugge TH, Kim S, Park Y, Marzi A, Pöhlmann S. Proteolytic activation of the 1918 influenza virus hemagglutinin. J Virol. 2009;83:3200–11.PubMedPubMedCentralCrossRefGoogle Scholar
  34. Chan JC, Knudson O, Wu F, Morser J, Dole WP, Wu Q. Hypertension in mice lacking the proatrial natriuretic peptide convertase corin. Proc Natl Acad Sci U S A. 2005;102:785–90.PubMedPubMedCentralCrossRefGoogle Scholar
  35. Chen LM, Chai KX. Prostasin serine protease inhibits breast cancer invasiveness and is transcriptionally regulated by promoter DNA methylation. Int J Cancer. 2002;97:323–9.PubMedCrossRefGoogle Scholar
  36. Chen LM, Hodge GB, Guarda LA, Welch JL, Greenberg NM, Chai KX. Down-regulation of prostasin serine protease: a potential invasion suppressor in prostate cancer. Prostate. 2001a;48:93–103.PubMedCrossRefGoogle Scholar
  37. Chen LM, Skinner ML, Kauffman SW, Chao J, Chao L, Thaler CD, Chai KX. Prostasin is a glycosylphosphatidylinositol-anchored active serine protease. J Biol Chem. 2001b;276:21434–42. Epub 2001 Mar 26.PubMedCrossRefGoogle Scholar
  38. Chen YW, Lee MS, Lucht A, Chou FP, Huang W, Havighurst TC, Kim K, Wang JK, Antalis TM, Johnson MD, Lin CY. TMPRSS2, a serine protease expressed in the prostate on the apical surface of luminal epithelial cells and released into semen in prostasomes, is misregulated in prostate cancer cells. Am J Pathol. 2010;176:2986–96.PubMedPubMedCentralCrossRefGoogle Scholar
  39. Chen S, Cao P, Dong N, Peng J, Zhang C, Wang H, Zhou T, Yang J, Zhang Y, Martelli EE, Naga Prasad SV, Miller RE, Malfait AM, Zhou Y, Wu Q. PCSK6-mediated corin activation is essential for normal blood pressure. Nat Med. 2015;21:1048–53.PubMedPubMedCentralCrossRefGoogle Scholar
  40. Cheng H, Fukushima T, Takahashi N, Tanaka H, Kataoka H. Hepatocyte growth factor activator inhibitor type 1 regulates epithelial to mesenchymal transition through membrane-bound serine proteinases. Cancer Res. 2009;69:1828–35.PubMedCrossRefGoogle Scholar
  41. Cheng Z, Zhou J, To KK, Chu H, Li C, Wang D, Yang D, Zheng S, Hao K, Bossé Y, Obeidat M, Brandsma CA, Song YQ, Chen Y, Zheng BJ, Li L, Yuen KY. Identification of TMPRSS2 as a susceptibility gene for severe 2009 Pandemic A(H1N1) Influenza and A(H7N9) Influenza. J Infect Dis. 2015;212:1214–21.CrossRefPubMedGoogle Scholar
  42. Chokki M, Yamamura S, Eguchi H, Masegi T, Horiuchi H, Tanabe H, Kamimura T, Yasuoka S. Human airway trypsin-like protease increases mucin gene expression in airway epithelial cells. Am J Respir Cell Mol Biol. 2004;30:470–8.PubMedCrossRefGoogle Scholar
  43. Dhanasekaran SM, Barrette TR, Ghosh D, Shah R, Varambally S, Kurachi K, Pienta KJ, Rubin MA, Chinnaiyan AM. Delineation of prognostic biomarkers in prostate cancer. Nature. 2001;412:822–6.PubMedCrossRefGoogle Scholar
  44. Donaldson SH, Hirsh A, Li DC, Holloway G, Chao J, Boucher RC, Gabriel SE. Regulation of the epithelial sodium channel by serine proteases in human airways. J Biol Chem. 2002;277:8338–45.PubMedCrossRefGoogle Scholar
  45. Driesbaugh KH, Buzza MS, Martin EW, Conway GD, Kao JP, Antalis TM. Proteolytic activation of the protease-activated receptor (PAR)-2 by the glycosylphosphatidylinositol-anchored serine protease testisin. J Biol Chem. 2015;290:3529–41.PubMedCrossRefGoogle Scholar
  46. Du X, She E, Gelbart T, Truksa J, Lee P, Xia Y, Khovananth K, Mudd S, Mann N, Moresco EM, Beutler E, Beutler B. The serine protease TMPRSS6 is required to sense iron deficiency. Science. 2008;320:1088–92.PubMedPubMedCentralCrossRefGoogle Scholar
  47. Duhaime MJ, Page KO, Varela FA, Murray AS, Silverman ME, Zoratti GL, List K. Cell surface human airway trypsin-like protease is lost during squamous cell carcinogenesis. J Cell Physiol. 2016;231:1476–83.PubMedPubMedCentralCrossRefGoogle Scholar
  48. Enshell-Seijffers D, Lindon C, Morgan BA. The serine protease Corin is a novel modifier of the Agouti pathway. Development. 2008;135:217–25.PubMedCrossRefGoogle Scholar
  49. Fang C, Shen L, Dong L, Liu M, Shi S, Dong N, Wu Q. Reduced urinary corin levels in patients with chronic kidney disease. Clin Sci (Lond). 2013;124:709–17.CrossRefGoogle Scholar
  50. Fasquelle L, Scott HS, Lenoir M, Wang J, Rebillard G, Gaboyard S, Venteo S, François F, Mausset-Bonnefont AL, Antonarakis SE, Neidhart E, Chabbert C, Puel JL, Guipponi M, Delprat B. Tmprss3, a transmembrane serine protease deficient in human DFNB8/10 deafness, is critical for cochlear hair cell survival at the onset of hearing. J Biol Chem. 2011;286:17383–97.PubMedPubMedCentralCrossRefGoogle Scholar
  51. Ferrara F, Molesti E, Böttcher-Friebertshäuser E, Cattoli G, Corti D, Scott S, Temperton N. The human Transmembrane Protease Serine 2 is necessary for the production of Group 2 influenza A virus pseudotypes. J Mol Genet Med. 2013;7:309–14.PubMedCentralCrossRefGoogle Scholar
  52. Finberg KE, Heeney MM, Campagna DR, Aydinok Y, Pearson HA, Hartman KR, Mayo MM, Samuel SM, Strouse JJ, Markianos K, Andrews NC, Fleming MD. Mutations in TMPRSS6 cause iron-refractory iron deficiency anemia (IRIDA). Nat Genet. 2008;40:569–71.PubMedPubMedCentralCrossRefGoogle Scholar
  53. Finberg KE, Whittlesey RL, Fleming MD, Andrews NC. Down-regulation of Bmp/Smad signaling by Tmprss6 is required for maintenance of systemic iron homeostasis. Blood. 2010;115:3817–26.PubMedPubMedCentralCrossRefGoogle Scholar
  54. Frateschi S, Keppner A, Malsure S, Iwaszkiewicz J, Sergi C, Merillat AM, Fowler-Jaeger N, Randrianarison N, Planès C, Hummler E. Mutations of the serine protease CAP1/Prss8 lead to reduced embryonic viability, skin defects, and decreased ENaC activity. Am J Pathol. 2012;181:605–15.PubMedCrossRefGoogle Scholar
  55. Friedrich R, Fuentes-Prior P, Ong E, Coombs G, Hunter M, Oehler R, Pierson D, Gonzalez R, Huber R, Bode W, Madison EL. Catalytic domain structures of Mt-Sp1/Matriptase, a matrix-degrading transmembrane serine proteinase. J Biol Chem. 2002;277:2160.PubMedCrossRefGoogle Scholar
  56. Friis S, Uzzun Sales K, Godiksen S, Peters DE, Lin CY, Vogel LK, Bugge TH. A matriptase-prostasin reciprocal zymogen activation complex with unique features: prostasin as a non-enzymatic co-factor for matriptase activation. J Biol Chem. 2013;288:19028–39.PubMedPubMedCentralCrossRefGoogle Scholar
  57. Friis S, Madsen DH, Bugge TH. Distinct Developmental Functions of Prostasin (CAP1/PRSS8) Zymogen and Activated Prostasin. J Biol Chem. 2016;291:2577–82.PubMedCrossRefGoogle Scholar
  58. Galloway SE, Reed ML, Russell CJ, Steinhauer DA. Influenza HA subtypes demonstrate divergent phenotypes for cleavage activation and pH of fusion: implications for host range and adaptation. PLoS Pathog. 2013;9:e1003151.PubMedPubMedCentralCrossRefGoogle Scholar
  59. Ganz T, Nemeth E. Hepcidin and iron homeostasis. Biochim Biophys Acta. 2012;1823:1434–43.PubMedPubMedCentralCrossRefGoogle Scholar
  60. Gasi Tandefelt D, Boormans J, Hermans K, Trapman J. ETS fusion genes in prostate cancer. Endocr Relat Cancer. 2014;21:R143–52.PubMedCrossRefGoogle Scholar
  61. Gierer S, Bertram S, Kaup F, Wrensch F, Heurich A, Krämer-Kühl A, Welsch K, Winkler M, Meyer B, Drosten C, Dittmer U, von Hahn T, Simmons G, Hofmann H, Pöhlmann S. The spike protein of the emerging betacoronavirus EMC uses a novel coronavirus receptor for entry, can be activated by TMPRSS2, and is targeted by neutralizing antibodies. J Virol. 2013;87:5502–11.PubMedPubMedCentralCrossRefGoogle Scholar
  62. Gladysheva IP, King SM, Houng AK. N-glycosylation modulates the cell-surface expression and catalytic activity of corin. Biochem Biophys Res Commun. 2008;373:130–5.PubMedCrossRefGoogle Scholar
  63. Glowacka I, Bertram S, Müller MA, Allen P, Soilleux E, Pfefferle S, Steffen I, Tsegaye TS, He Y, Gnirss K, Niemeyer D, Schneider H, Drosten C, Pöhlmann S. Evidence that TMPRSS2 activates the severe acute respiratory syndrome coronavirus spike protein for membrane fusion and reduces viral control by the humoral immune response. J Virol. 2011;85:4122–34.PubMedPubMedCentralCrossRefGoogle Scholar
  64. Götze H, Adelson JW, Hadorn HB, Portmann R, Troesch V. Hormone-elicited enzyme release by the small intestinal wall. Gut. 1972;13(6):471.PubMedPubMedCentralCrossRefGoogle Scholar
  65. Guipponi M, Vuagniaux G, Wattenhofer M, Shibuya K, Vazquez M, Dougherty L, Scamuffa N, Guida E, Okui M, Rossier C, Hancock M, Buchet K, Reymond A, Hummler E, Marzella PL, Kudoh J, Shimizu N, Scott HS, Antonarakis SE, Rossier BC. The transmembrane serine protease (TMPRSS3) mutated in deafness DFNB8/10 activates the epithelial sodium channel (ENaC) in vitro. Hum Mol Genet. 2002;11:2829–36.PubMedCrossRefGoogle Scholar
  66. Guipponi M, Tan J, Cannon PZ, Donley L, Crewther P, Clarke M, Wu Q, Shepherd RK, Scott HS. Mice deficient for the type II transmembrane serine protease, TMPRSS1/hepsin, exhibit profound hearing loss. Am J Pathol. 2007;171:608–16.PubMedPubMedCentralCrossRefGoogle Scholar
  67. Guipponi M, Toh MY, Tan J, Park D, Hanson K, Ballana E, Kwong D, Cannon PZ, Wu Q, Gout A, Delorenzi M, Speed TP, Smith RJ, Dahl HH, Petersen M, Teasdale RD, Estivill X, Park WJ, Scott HS. An integrated genetic and functional analysis of the role of type II transmembrane serine proteases (TMPRSSs) in hearing loss. Hum Mutat. 2008;29:130–41.PubMedCrossRefGoogle Scholar
  68. Guo YJ, Krauss S, Senne DA, Mo IP, Lo KS, Xiong XP, Norwood M, Shortridge KF, Webster RG, Guan Y. Characterization of the pathogenicity of members of the newly established H9N2 influenza virus lineages in Asia. Virology. 2000;267:279–88.PubMedCrossRefGoogle Scholar
  69. Hadorn B, Tarlow MJ, Lloyd JK, Wolff OH. Intestinal enterokinase deficiency. Lancet. 1969;1:812–3.PubMedCrossRefGoogle Scholar
  70. Hamilton BS, Whittaker GR. Cleavage activation of human-adapted influenza virus subtypes by kallikrein-related peptidases 5 and 12. J Biol Chem. 2013;288:17399–407.PubMedPubMedCentralCrossRefGoogle Scholar
  71. Hamilton BS, Gludish DW, Whittaker GR. Cleavage activation of the human-adapted influenza virus subtypes by matriptase reveals both subtype and strain specificities. J Virol. 2012;86(19):10579–86.PubMedPubMedCentralCrossRefGoogle Scholar
  72. Hanifa S, Scott HS, Crewther P, Guipponi M, Tan J. Thyroxine treatments do not correct inner ear defects in tmprss1 mutant mice. Neuroreport. 2010;21:897–901.PubMedPubMedCentralCrossRefGoogle Scholar
  73. Hansbro PM, Hamilton MJ, Fricker M, Gellatly SL, Jarnicki AG, Zheng D, Frei SM, Wong GW, Hamadi S, Zhou S, Foster PS, Krilis SA, Stevens RL. Importance of mast cell Prss31/transmembrane tryptase/tryptase-γ in lung function and experimental chronic obstructive pulmonary disease and colitis. J Biol Chem. 2014;289:18214–27.PubMedPubMedCentralCrossRefGoogle Scholar
  74. Hansen IA, Fassnacht M, Hahner S, Hammer F, Schammann M, Meyer SR, Bicknell AB, Allolio B. The adrenal secretory serine protease AsP is a short secretory isoform of the transmembrane airway trypsin-like protease. Endocrinology. 2004;145:1898–905.PubMedCrossRefGoogle Scholar
  75. Hatesuer B, Bertram S, Mehnert N, Bahgat MM, Nelson PS, Pöhlmann S, Schughart K. Tmprss2 is essential for influenza H1N1 virus pathogenesis in mice. PLoS Pathog. 2013;9:e1003774.PubMedPubMedCentralCrossRefGoogle Scholar
  76. Hermon-Taylor J, Perrin J, Grant DA, Appleyard A, Bubel M, Magee AI. Immunofluorescent localisation of enterokinase in human small intestine. Gut. 1977;18:259–65.PubMedPubMedCentralCrossRefGoogle Scholar
  77. Heurich A, Hofmann-Winkler H, Gierer S, Liepold T, Jahn O, Pöhlmann S. TMPRSS2 and ADAM17 cleave ACE2 differentially and only proteolysis by TMPRSS2 augments entry driven by the severe acute respiratory syndrome coronavirus spike protein. J Virol. 2014;88:1293–307.PubMedPubMedCentralCrossRefGoogle Scholar
  78. Hildenbrand R, Gandhari M, Stroebel P, Marx A, Allgayer H, Arens N. The urokinase-system—role of cell proliferation and apoptosis. Histol Histopathol. 2008;23:227–36.PubMedPubMedCentralGoogle Scholar
  79. Hobson JP, Netzel-Arnett S, Szabo R, Réhault SM, Church FC, Strickland DK, Lawrence DA, Antalis TM, Bugge TH. Mouse DESC1 is located within a cluster of seven DESC1-like genes and encodes a type II transmembrane serine protease that forms serpin inhibitory complexes. J Biol Chem. 2004;279:46981–94.PubMedCrossRefGoogle Scholar
  80. Hoffmann M, Krüger N, Zmora P, Wrensch F, Herrler G, Pöhlmann S. The hemagglutinin of Bat-associated influenza viruses is activated by TMPRSS2 for pH-dependent entry into Bat but not human cells. PLoS One. 2016;11:e0152134.PubMedPubMedCentralCrossRefGoogle Scholar
  81. Holzinger A, Maier EM, Bück C, Mayerhofer PU, Kappler M, Haworth JC, Moroz SP, Hadorn HB, Sadler JE, Roscher AA. Mutations in the proenteropeptidase gene are the molecular cause of congenital enteropeptidase deficiency. Am J Hum Genet. 2002;70:20–5.PubMedCrossRefGoogle Scholar
  82. Homma M, Ohuchi M. Trypsin action on the growth of Sendai virus in tissue culture cells. III. Structural difference of Sendai viruses grown in eggs and tissue culture cells. J Virol. 1973;12:1457–65.PubMedPubMedCentralGoogle Scholar
  83. Honda A, Yamagata K, Sugiura S, Watanabe K, Baba T. A mouse serine protease TESP5 is selectively included into lipid rafts of sperm membrane presumably as a glycosylphosphatidylinositol-anchored protein. J Biol Chem. 2002;277:16976–84.PubMedCrossRefGoogle Scholar
  84. Hooper JD, Nicol DL, Dickinson JL, Eyre HJ, Scarman AL, Normyle JF, Stuttgen MA, Douglas ML, Loveland KA, Sutherland GR, Antalis TM. Testisin, a new human serine proteinase expressed by premeiotic testicular germ cells and lost in testicular germ cell tumors. Cancer Res. 1999;59:3199–205.PubMedPubMedCentralGoogle Scholar
  85. Hooper JD, Bowen N, Marshall H, Cullen LM, Sood R, Daniels R, Stuttgen MA, Normyle JF, Higgs DR, Kastner DL, Ogbourne SM, Pera MF, Jazwinska EC, TM. Localization, expression and genomic structure of the gene encoding the human serine protease testisin. Biochim Biophys Acta. 2000;1492:63–71.CrossRefGoogle Scholar
  86. Hooper JD, Clements JA, Quigley JP, Antalis TM. Type II transmembrane serine proteases. Insights into an emerging class of cell surface proteolytic enzymes. J Biol Chem. 2001;276:857–60. Review.CrossRefPubMedGoogle Scholar
  87. Hsu YC, Huang HP, Yu IS, Su KY, Lin SR, Lin WC, Wu HL, Shi GY, Tao MH, Kao CH, Wu YM, Martin PE, Lin SY, Yang PC, Lin SW. Serine protease hepsin regulates hepatocyte size and hemodynamic retention of tumor cells by hepatocyte growth factor signaling in mice. Hepatology. 2012;56:1913–23.PubMedCrossRefGoogle Scholar
  88. Hummler E, Dousse A, Rieder A, Stehle JC, Rubera I, Osterheld MC, Beermann F, Frateschi S, Charles RP. The channel-activating protease CAP1/Prss8 is required for placental labyrinth maturation. PLoS One. 2013;8:e55796.PubMedPubMedCentralCrossRefGoogle Scholar
  89. Inoue M, Kanbe N, Kurosawa M, Kido H. Cloning and tissue distribution of a novel serine protease esp-1 from human eosinophils. Biochem Biophys Res Commun. 1998;252:307–12.PubMedCrossRefGoogle Scholar
  90. Iwakiri K, Ghazizadeh M, Jin E, Fujiwara M, Takemura T, Takezaki S, Kawana S, Yasuoka S, Kawanami O. Human airway trypsin-like protease induces PAR-2-mediated IL-8 release in psoriasis vulgaris. J Invest Dermatol. 2004;122:937–44.PubMedCrossRefGoogle Scholar
  91. Jiang J, Wu S, Wang W, Chen S, Peng J, Zhang X, Wu Q. Ectodomain shedding and autocleavage of the cardiac membrane protease corin. J Biol Chem. 2011;286:10066–72.PubMedPubMedCentralCrossRefGoogle Scholar
  92. Jung H, Lee KP, Park SJ, Park JH, Jang YS, Choi SY, Jung JG, Jo K, Park DY, Yoon JH, Park JH, Lim DS, Hong GR, Choi C, Park YK, Lee JW, Hong HJ, Kim S, Park YW. TMPRSS4 promotes invasion, migration and metastasis of human tumor cells by facilitating an epithelial-mesenchymal transition. Oncogene. 2008;27:2635–47.PubMedCrossRefGoogle Scholar
  93. Kam YW, Okumura Y, Kido H, Ng LF, Bruzzone R, Altmeyer R. Cleavage of the SARS coronavirus spike glycoprotein by airway proteases enhances virus entry into human bronchial epithelial cells in vitro. PLoS One. 2009;4:e7870.PubMedPubMedCentralCrossRefGoogle Scholar
  94. Kato M, Hashimoto T, Shimomura T, Kataoka H, Ohi H, Kitamura N. Hepatocyte growth factor activator inhibitor type 1 inhibits protease activity and proteolytic activation of human airway trypsin-like protease. J Biochem. 2012;151:179–87.PubMedCrossRefGoogle Scholar
  95. Kawano N, Kang W, Yamashita M, Koga Y, Yamazaki T, Hata T, Miyado K, Baba T. Mice lacking two sperm serine proteases, ACR and PRSS21, are subfertile, but the mutant sperm are infertile in vitro. Biol Reprod. 2010;83:359–69.PubMedCrossRefGoogle Scholar
  96. Kawaoka Y, Naeve CW, Webster RG. Is virulence of H5N2 influenza viruses in chickens associated with loss of carbohydrate from the hemagglutinin? Virology. 1984;139:303–16.CrossRefPubMedGoogle Scholar
  97. Keppner A, Andreasen D, Mérillat AM, Bapst J, Ansermet C, Wang Q, Maillard M, Malsure S, Nobile A, Hummler E. Epithelial sodium channel-mediated sodium transport is not dependent on the membrane-bound serine protease CAP2/Tmprss4. PLoS One. 2015;10:e0135224.PubMedPubMedCentralCrossRefGoogle Scholar
  98. Kesic MJ, Meyer M, Bauer R, Jaspers I. Exposure to ozone modulates human airway protease/antiprotease balance contributing to increased influenza A infection. PLoS One. 2012;7:e35108.PubMedPubMedCentralCrossRefGoogle Scholar
  99. Kido H, Okumura Y, Takahashi E, Pan HY, Wang S, Chida J, Le TQ, Yano M. Host envelope glycoprotein processing proteases are indispensable for entry into human cells by seasonal and highly pathogenic avian influenza viruses. J Mol Genet Med. 2008;3:167–75.PubMedPubMedCentralGoogle Scholar
  100. Kim S, Lee JW. Membrane proteins involved in epithelial-mesenchymal transition and tumor invasion: studies on TMPRSS4 and TM4SF5. Genom Inform. 2014;12:12–20.CrossRefGoogle Scholar
  101. Kim DR, Sharmin S, Inoue M, Kido H. Cloning and expression of novel mosaic serine proteases with and without a transmembrane domain from human lung. Biochim Biophys Acta. 2001;1518:204–9.PubMedCrossRefGoogle Scholar
  102. Kim TS, Heinlein C, Hackman RC, Nelson PS. Phenotypic analysis of mice lacking the Tmprss2-encoded protease. Mol Cell Biol. 2006;26:965–75.PubMedPubMedCentralCrossRefGoogle Scholar
  103. Kim S, Kang HY, Nam EH, Choi MS, Zhao XF, Hong CS, Lee JW, Lee JH, Park YK. TMPRSS4 induces invasion and epithelial-mesenchymal transition through upregulation of integrin alpha5 and its signaling pathways. Carcinogenesis. 2010;31:597–606.PubMedCrossRefGoogle Scholar
  104. Kitamoto Y, Yuan X, Wu Q, McCourt DW, Sadler JE. Enterokinase, the initiator of intestinal digestion, is a mosaic protease composed of a distinctive assortment of domains. Proc Natl Acad Sci U S A. 1994;91:7588–92.PubMedPubMedCentralCrossRefGoogle Scholar
  105. Kitamoto Y, Veile RA, Donis-Keller H, Sadler JE. cDNA sequence and chromosomal localization of human enterokinase, the proteolytic activator of trypsinogen. Biochemistry. 1995;34:4562–8.PubMedCrossRefGoogle Scholar
  106. Klenk HD, Rott R, Orlich M, Blödorn J. Activation of influenza A viruses by trypsin treatment. Virology. 1975;68:426–39.CrossRefPubMedGoogle Scholar
  107. Klezovitch O, Chevillet J, Mirosevich J, Roberts RL, Matusik RJ, Vasioukhin V. Hepsin promotes prostate cancer progression and metastasis. Cancer Cell. 2004;6:185–95.PubMedCrossRefGoogle Scholar
  108. Ko CJ, Huang CC, Lin HY, Juan CP, Lan SW, Shyu HY, Wu SR, Hsiao PW, Huang HP, Shun CT, Lee MS. Androgen-induced TMPRSS2 activates Matriptase and promotes extracellular matrix degradation, prostate cancer cell invasion, tumor growth, and metastasis. Cancer Res. 2015;75:2949–60.PubMedCrossRefGoogle Scholar
  109. Kühn N, Bergmann S, Kösterke N, Lambertz RL, Keppner A, van den Brand JM, Pöhlmann S, Weiß S, Hummler E, Hatesuer B, Schughart K. The proteolytic activation of (H3N2) Influenza A virus hemagglutinin is facilitated by different type II transmembrane serine proteases. J Virol. 2016;90:4298–307.PubMedPubMedCentralCrossRefGoogle Scholar
  110. Kunitz M. Formation of trypsin from crystalline trypsinogen by means of enterokinase. J Gen Physiol. 1939;22:429–46.PubMedPubMedCentralCrossRefGoogle Scholar
  111. Kyrieleis OJ, Huber R, Ong E, Oehler R, Hunter M, Madison EL, Jacob U. Crystal structure of the catalytic domain of DESC1, a new member of the type II transmembrane serine proteinase family. FEBS J. 2007;274:2148–60.PubMedCrossRefGoogle Scholar
  112. Lang JC, Schuller DE. Differential expression of a novel serine protease homologue in squamous cell carcinoma of the head and neck. Br J Cancer. 2001;84:237–43.PubMedPubMedCentralCrossRefGoogle Scholar
  113. Larsen BR, Steffensen SD, Nielsen NV, Friis S, Godiksen S, Bornholdt J, Soendergaard C, Nonboe AW, Andersen MN, Poulsen SS, Szabo R, Bugge TH, Lin CY, Skovbjerg H, Jensen JK, Vogel LK. Hepatocyte growth factor activator inhibitor-2 prevents shedding of matriptase. Exp Cell Res. 2013;319:918–29.PubMedPubMedCentralCrossRefGoogle Scholar
  114. Lazarowitz SG, Choppin PW. Enhancement of the infectivity of influenza A and B viruses by proteolytic cleavage of the hemagglutinin polypeptide. Virology. 1975;68:440–54.CrossRefPubMedGoogle Scholar
  115. Lazarowitz SG, Goldberg AR, Choppin PW. Proteolytic cleavage by plasmin of the HA polypeptide of influenza virus: host cell activation of serum plasminogen. Virology. 1973;56:172–80.CrossRefPubMedGoogle Scholar
  116. Leshem O, Madar S, Kogan-Sakin I, Kamer I, Goldstein I, Brosh R, Cohen Y, Jacob-Hirsch J, Ehrlich M, Ben-Sasson S, Goldfinger N, Loewenthal R, Gazit E, Rotter V, Berger R. TMPRSS2/ERG promotes epithelial to mesenchymal transition through the ZEB1/ZEB2 axis in a prostate cancer model. PLoS One. 2011;6:e21650.PubMedPubMedCentralCrossRefGoogle Scholar
  117. Leytus SP, Loeb KR, Hagen FS, Kurachi K, Davie EW. A novel trypsin-like serine protease (hepsin) with a putative transmembrane domain expressed by human liver and hepatoma cells. Biochemistry. 1988;27:1067–74.PubMedCrossRefGoogle Scholar
  118. Leyvraz C, Charles RP, Rubera I, Guitard M, Rotman S, Breiden B, Sandhoff K, Hummler E. The epidermal barrier function is dependent on the serine protease CAP1/Prss8. J Cell Biol. 2005;170:487–96.PubMedPubMedCentralCrossRefGoogle Scholar
  119. Li Y, Zhang X, Huang G, Miao X, Guo L, Lin D, Lu SH. Identification of a novel polymorphism Arg290Gln of esophageal cancer related gene 1 (ECRG1) and its related risk to esophageal squamous cell carcinoma. Carcinogenesis. 2006;27:798–802.PubMedCrossRefGoogle Scholar
  120. Li X, Qi W, He J, Ning Z, Hu Y, Tian J, Jiao P, Xu C, Chen J, Richt J, Ma W, Liao M. Molecular basis of efficient replication and pathogenicity of H9N2 avian influenza viruses in mice. PLoS One. 2012;7:e40118.PubMedPubMedCentralCrossRefGoogle Scholar
  121. Li Y, Peng A, Ge S, Wang Q, Liu J. miR-204 suppresses cochlear spiral ganglion neuron survival in vitro by targeting TMPRSS3. Hear Res. 2014;314:60–4.PubMedCrossRefGoogle Scholar
  122. Li H, Zhang Y, Wu Q. Role of corin in the regulation of blood pressure. Curr Opin Nephrol Hypertens. 2017;26:67–73.PubMedPubMedCentralGoogle Scholar
  123. Liao X, Wang W, Chen S, Wu Q. Role of glycosylation in corin zymogen activation. J Biol Chem. 2007;282:27728–35.PubMedCrossRefGoogle Scholar
  124. Lin CY, Anders J, Johnson M, Sang QA, Dickson RB. Molecular cloning of cDNA for matriptase, a matrix-degrading serine protease with trypsin-like activity. J Biol Chem. 1999;274:18231–6.PubMedCrossRefGoogle Scholar
  125. List K, Haudenschild CC, Szabo R, Chen W, Wahl SM, Swaim W, Engelholm LH, Behrendt N, Bugge TH. Matriptase/MT-SP1 is required for postnatal survival, epidermal barrier function, hair follicle development, and thymic homeostasis. Oncogene. 2002;21:3765–79.PubMedCrossRefGoogle Scholar
  126. List K, Szabo R, Wertz PW, Segre J, Haudenschild CC, Kim SY, Bugge TH. Loss of proteolytically processed filaggrin caused by epidermal deletion of Matriptase/MT-SP1. J Cell Biol. 2003;163:901–10.PubMedPubMedCentralCrossRefGoogle Scholar
  127. List K, Bugge TH, Szabo R. Matriptase: potent proteolysis on the cell surface. Mol Med. 2006a;12:1–7. ReviewPubMedPubMedCentralCrossRefGoogle Scholar
  128. List K, Szabo R, Molinolo A, Nielsen BS, Bugge TH. Delineation of matriptase protein expression by enzymatic gene trapping suggests diverging roles in barrier function, hair formation, and squamous cell carcinogenesis. Am J Pathol. 2006b;168:1513–25.PubMedPubMedCentralCrossRefGoogle Scholar
  129. List K, Currie B, Scharschmidt TC, Szabo R, Shireman J, Molinolo A, Cravatt BF, Segre J, Bugge TH. Autosomal ichthyosis with hypotrichosis syndrome displays low matriptase proteolytic activity and is phenocopied in ST14 hypomorphic mice. J Biol Chem. 2007;282:36714–23.PubMedCrossRefGoogle Scholar
  130. Lu D, Yuan X, Zheng X, Sadler JE. Bovine proenteropeptidase is activated by trypsin, and the specificity of enteropeptidase depends on the heavy chain. J Biol Chem. 1997;272:31293–300.PubMedCrossRefGoogle Scholar
  131. Lu D, Fütterer K, Korolev S, Zheng X, Tan K, Waksman G, Sadler JE. Crystal structure of enteropeptidase light chain complexed with an analog of the trypsinogen activation peptide. J Mol Biol. 1999;292:361–73.PubMedCrossRefGoogle Scholar
  132. Lucas JM, True L, Hawley S, Matsumura M, Morrissey C, Vessella R, Nelson PS. The androgen-regulated type II serine protease TMPRSS2 is differentially expressed and mislocalized in prostate adenocarcinoma. J Pathol. 2008;215:118–25.PubMedCrossRefGoogle Scholar
  133. Lucas JM, Heinlein C, Kim T, Hernandez SA, Malik MS, True LD, Morrissey C, Corey E, Montgomery B, Mostaghel E, Clegg N, Coleman I, Brown CM, Schneider EL, Craik C, Simon JA, Bedalov A, Nelson PS. The androgen-regulated protease TMPRSS2 activates a proteolytic cascade involving components of the tumor microenvironment and promotes prostate cancer metastasis. Cancer Discov. 2014;4:1310–25.PubMedPubMedCentralCrossRefGoogle Scholar
  134. Madsen DH, Szabo R, Molinolo AA, Bugge TH. TMPRSS13 deficiency impairs stratum corneum formation and epidermal barrier acquisition. Biochem J. 2014;461:487–95.PubMedPubMedCentralCrossRefGoogle Scholar
  135. Masmoudi S, Antonarakis SE, Schwede T, Ghorbel AM, Gratri M, Pappasavas MP, Drira M, Elgaied-Boulila A, Wattenhofer M, Rossier C, Scott HS, Ayadi H, Guipponi M. Novel missense mutations of TMPRSS3 in two consanguineous Tunisian families with non-syndromic autosomal recessive deafness. Hum Mutat. 2001;18:101–8.PubMedCrossRefGoogle Scholar
  136. Matsushima M, Ichinose M, Yahagi N, Kakei N, Tsukada S, Miki K, Kurokawa K, Tashiro K, Shiokawa K, Shinomiya K, et al. Structural characterization of porcine enteropeptidase. J Biol Chem. 1994;269:19976–82.PubMedPubMedCentralGoogle Scholar
  137. Matsushima R, Takahashi A, Nakaya Y, Maezawa H, Miki M, Nakamura Y, Ohgushi F, Yasuoka S. Human airway trypsin-like protease stimulates human bronchial fibroblast proliferation in a protease-activated receptor-2-dependent pathway. Am J Physiol Lung Cell Mol Physiol. 2006;290:L385–95.PubMedCrossRefGoogle Scholar
  138. 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;84:12658–64.PubMedPubMedCentralCrossRefGoogle Scholar
  139. Miao J, Mu D, Ergel B, Singavarapu R, Duan Z, Powers S, Oliva E, Orsulic S. Hepsin colocalizes with desmosomes and induces progression of ovarian cancer in a mouse model. Int J Cancer. 2008;123:2041–7.PubMedPubMedCentralCrossRefGoogle Scholar
  140. Miller GS, List K. The matriptase-prostasin proteolytic cascade in epithelial development and pathology. Cell Tissue Res. 2013;351:245–53.PubMedCrossRefGoogle Scholar
  141. Miller GS, Zoratti GL, Murray AS, Bergum C, Tanabe LM, List K. HATL5: a cell surface serine protease differentially expressed in epithelial cancers. PLoS One. 2014;9:e87675.PubMedPubMedCentralCrossRefGoogle Scholar
  142. Millet JK, Whittaker GR. Host cell proteases: critical determinants of coronavirus tropism and pathogenesis. Virus Res. 2015;202:120–34.CrossRefGoogle Scholar
  143. Milner JM, Patel A, Davidson RK, Swingler TE, Desilets A, Young DA, Kelso EB, Donell ST, Cawston TE, Clark IM, Ferrell WR, Plevin R, Lockhart JC, Leduc R, Rowan AD. Matriptase is a novel initiator of cartilage matrix degradation in osteoarthritis. Arthritis Rheum. 2010;62:1955–66.PubMedPubMedCentralGoogle Scholar
  144. Min HJ, Lee MK, Lee JW, Kim S. TMPRSS4 induces cancer cell invasion through pro-uPA processing. Biochem Biophys Res Commun. 2014a;446:1–7.PubMedCrossRefGoogle Scholar
  145. Min HJ, Lee Y, Zhao XF, Park YK, Lee MK, Lee JW, Kim S. TMPRSS4 upregulates uPA gene expression through JNK signaling activation to induce cancer cell invasion. Cell Signal. 2014b;26:398–408.PubMedCrossRefGoogle Scholar
  146. Miyata H, Thaler CD, Haimo LT, Cardullo RA. Protease activation and the signal transduction pathway regulating motility in sperm from the water strider Aquarius remigis. Cytoskeleton (Hoboken). 2012;69:207–20.CrossRefGoogle Scholar
  147. Molina L, Fasquelle L, Nouvian R, Salvetat N, Scott HS, Guipponi M, Molina F, Puel JL, Delprat B. Tmprss3 loss of function impairs cochlear inner hair cell Kcnma1 channel membrane expression. Hum Mol Genet. 2013;22:1289–99.PubMedCrossRefGoogle Scholar
  148. Murray AS, Varela FA, List K. Type II transmembrane serine proteases as potential targets for cancer therapy. Biol Chem. 2016;397:815–26.PubMedPubMedCentralCrossRefGoogle Scholar
  149. Nagai Y, Klenk HD, Rott R. Proteolytic cleavage of the viral glycoproteins and its significance for the virulence of Newcastle disease virus. Virology. 1976;72:494–508.PubMedCrossRefGoogle Scholar
  150. Nagaike K, Kawaguchi M, Takeda N, Fukushima T, Sawaguchi A, Kohama K, Setoyama M, Kataoka H. Defect of hepatocyte growth factor activator inhibitor type 1/serine protease inhibitor, Kunitz type 1 (Hai-1/Spint1) leads to ichthyosis-like condition and abnormal hair development in mice. Am J Pathol. 2008;173:1464–75.PubMedPubMedCentralCrossRefGoogle Scholar
  151. Narikiyo T, Kitamura K, Adachi M, Miyoshi T, Iwashita K, Shiraishi N, Nonoguchi H, Chen LM, Chai KX, Chao J, Tomita K. Regulation of prostasin by aldosterone in the kidney. J Clin Invest. 2002;109:401–8.PubMedPubMedCentralCrossRefGoogle Scholar
  152. Netzel-Arnett S, Hooper JD, Szabo R, Madison EL, Quigley JP, Bugge TH, Antalis TM. Membrane anchored serine proteases: a rapidly expanding group of cell surface proteolytic enzymes with potential roles in cancer. Cancer Metastasis Rev. 2003;22:237–58. Review.PubMedCrossRefGoogle Scholar
  153. Netzel-Arnett S, Currie BM, Szabo R, Lin CY, Chen LM, Chai KX, Antalis TM, Bugge TH, List K. Evidence for a matriptase-prostasin proteolytic cascade regulating terminal epidermal differentiation. J Biol Chem. 2006;281:32941–5.PubMedCrossRefGoogle Scholar
  154. Netzel-Arnett S, Bugge TH, Hess RA, Carnes K, Stringer BW, Scarman AL, Hooper JD, Tonks ID, Kay GF, Antalis TM. The glycosylphosphatidylinositol-anchored serine protease PRSS21 (testisin) imparts murine epididymal sperm cell maturation and fertilizing ability. Biol Reprod. 2009;81:921–32.PubMedPubMedCentralCrossRefGoogle Scholar
  155. Netzel-Arnett S, Buzza MS, Shea-Donohue T, Désilets A, Leduc R, Fasano A, Bugge TH, Antalis TM. Matriptase protects against experimental colitis and promotes intestinal barrier recovery. Inflamm Bowel Dis. 2012;18:1303–14.PubMedCrossRefGoogle Scholar
  156. Ng HY, Ko JM, Yu VZ, Ip JC, Dai W, Cal S, Lung ML. DESC1, a novel tumor suppressor, sensitizes cells to apoptosis by downregulating the EGFR/AKT pathway in esophageal squamous cell carcinoma. Int J Cancer. 2016;138:2940–51.PubMedCrossRefGoogle Scholar
  157. Nonboe AW, Krigslund O, Soendergaard C, Skovbjerg S, Friis S, Andersen MN, Ellis V, Kawaguchi M, Kataoka H, Bugge TH, Vogel LK. HAI-2 stabilizes, inhibits and regulates SEA-cleavage-dependent secretory transport of matriptase. Traffic. 2017;18:378–91.PubMedCrossRefGoogle Scholar
  158. Oberst MD, Williams CA, Dickson RB, Johnson MD, Lin CY. The activation of matriptase requires its noncatalytic domains, serine protease domain, and its cognate inhibitor. J Biol Chem. 2003;278:26773–9.PubMedCrossRefGoogle Scholar
  159. Oberst MD, Chen LY, Kiyomiya K, Williams CA, Lee MS, Johnson MD, Dickson RB, Lin CY. HAI-1 regulates activation and expression of matriptase, a membrane-bound serine protease. Am J Physiol Cell Physiol. 2005;289:C462–70.PubMedCrossRefGoogle Scholar
  160. Ogiwara K, Takahashi T. Specificity of the medaka enteropeptidase serine protease and its usefulness as a biotechnological tool for fusion-protein cleavage. Proc Natl Acad Sci U S A. 2007;104:7021–6.PubMedPubMedCentralCrossRefGoogle Scholar
  161. Okumura Y, Hayama M, Takahashi E, Fujiuchi M, Shimabukuro A, Yano M, Kido H. 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. 2006;400:551–61.PubMedPubMedCentralCrossRefGoogle Scholar
  162. Okumura Y, Takahashi E, Yano M, Ohuchi M, Daidoji T, Nakaya T, Böttcher E, Garten W, Klenk HD, Kido H. 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. J Virol. 2010 May;84(10):5089–96.PubMedPubMedCentralCrossRefGoogle Scholar
  163. Paoloni-Giacobino A, Chen H, Peitsch MC, Rossier C, Antonarakis SE. Cloning of the TMPRSS2 gene, which encodes a novel serine protease with transmembrane, LDLRA, and SRCR domains and maps to 21q22.3. Genomics. 1997;44:309–20.PubMedCrossRefGoogle Scholar
  164. Park JE, Li K, Barlan A, Fehr AR, Perlman S, McCray PBJ, Gallagher T. Proteolytic processing of Middle East respiratory syndrome coronavirus spikes expands virus tropism. Proc Natl Acad Sci U S A. 2016;113(43):12262–7.PubMedPubMedCentralCrossRefGoogle Scholar
  165. Peitsch C, Klenk HD, Garten W, Böttcher-Friebertshäuser E. Activation of influenza A viruses by host proteases from swine airway epithelium. J Virol. 2014;88:282–91.PubMedPubMedCentralCrossRefGoogle Scholar
  166. Perona JJ, Craik CS. Structural basis of substrate specificity in the serine proteases. Protein Sci. 1995;4:337–60. Review.PubMedPubMedCentralCrossRefGoogle Scholar
  167. Peters DE, Szabo R, Friis S, Shylo NA, Uzzun Sales K, Holmbeck K, Bugge TH. The membrane-anchored serine protease prostasin (CAP1/PRSS8) supports epidermal development and postnatal homeostasis independent of its enzymatic activity. J Biol Chem. 2014;289:14740–9.PubMedPubMedCentralCrossRefGoogle Scholar
  168. Planès C, Randrianarison NH, Charles RP, Frateschi S, Cluzeaud F, Vuagniaux G, Soler P, Clerici C, Rossier BC, Hummler E. ENaC-mediated alveolar fluid clearance and lung fluid balance depend on the channel-activating protease 1. EMBO Mol Med. 2010;2:26–37.PubMedPubMedCentralCrossRefGoogle Scholar
  169. Polzin D, Kaminski HJ, Kastner C, Wang W, Krämer S, Gambaryan S, Russwurm M, Peters H, Wu Q, Vandewalle A, Bachmann S, Theilig F. Decreased renal corin expression contributes to sodium retention in proteinuric kidney diseases. Kidney Int. 2010;78:650–9.PubMedPubMedCentralCrossRefGoogle Scholar
  170. Ramsay AJ, Hooper JD, Folgueras AR, Velasco G, López-Otín C. Matriptase-2 (TMPRSS6): a proteolytic regulator of iron homeostasis. Haematologica. 2009;94:840–9.PubMedPubMedCentralCrossRefGoogle Scholar
  171. Rickert KW, Kelley P, Byrne NJ, Diehl RE, Hall DL, Montalvo AM, Reid JC, Shipman JM, Thomas BW, Munshi SK, Darke PL, Su HP. Structure of human prostasin, a target for the regulation of hypertension. J Biol Chem. 2008;283:34864–72.PubMedPubMedCentralCrossRefGoogle Scholar
  172. 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. The host protease TMPRSS2 plays a major role in in vivo replication of emerging H7N9 and seasonal influenza viruses. J Virol. 2014;88:5608–16.PubMedPubMedCentralCrossRefGoogle Scholar
  173. Sakai K, Sekizuka T, Ami Y, Nakajima N, Kitazawa M, Sato Y, Nakajima K, Anraku M, Kubota T, Komase K, Takehara K, Hasegawa H, Odagiri T, Tashiro M, Kuroda M, Takeda M. A mutant H3N2 influenza virus uses an alternative activation mechanism in TMPRSS2 knockout mice by loss of an oligosaccharide in the hemagglutinin stalk region. J Virol. 2015;89:5154–8.PubMedPubMedCentralCrossRefGoogle Scholar
  174. Sakai K, Ami Y, Nakajima N, Nakajima K, Kitazawa M, Anraku M, Takayama I, Sangsriratanakul N, Komura M, Sato Y, Asanuma H, Takashita E, Komase K, Takehara K, Tashiro M, Hasegawa H, Odagiri T, Takeda M. TMPRSS2 independency for haemagglutinin cleavage in vivo differentiates Influenza B virus from Influenza A virus. Sci Rep. 2016;6:29430.PubMedPubMedCentralCrossRefGoogle Scholar
  175. Sales KU, Hobson JP, Wagenaar-Miller R, Szabo R, Rasmussen AL, Bey A, Shah MF, Molinolo AA, Bugge TH. Expression and genetic loss of function analysis of the HAT/DESC cluster proteases TMPRSS11A and HAT. PLoS One. 2011;6:e23261.PubMedPubMedCentralCrossRefGoogle Scholar
  176. Scheiblauer H, Reinacher M, Tashiro M, Rott R. Interactions between bacteria and influenza A virus in the development of influenza pneumonia. J Infect Dis. 1992;166:783–91.CrossRefPubMedGoogle Scholar
  177. Scheid A, Choppin PW. Identification of biological activities of paramyxovirus glycoproteins. Activation of cell fusion, hemolysis, and infectivity of proteolytic cleavage of an inactive precursor protein of Sendai virus. Virology. 1974;57:475–90.PubMedCrossRefGoogle Scholar
  178. Schmidlin F, Amadesi S, Dabbagh K, Lewis DE, Knott P, Bunnett NW, Gater PR, Geppetti P, Bertrand C, Stevens ME. Protease-activated receptor 2 mediates eosinophil infiltration and hyperreactivity in allergic inflammation of the airway. J Immunol. 2002;169:5315–21.PubMedCrossRefGoogle Scholar
  179. Scott HS, Kudoh J, Wattenhofer M, Shibuya K, Berry A, Chrast R, Guipponi M, Wang J, Kawasaki K, Asakawa S, Minoshima S, Younus F, Mehdi SQ, Radhakrishna U, Papasavvas MP, Gehrig C, Rossier C, Korostishevsky M, Gal A, Shimizu N, Bonne-Tamir B, Antonarakis SE. Insertion of beta-satellite repeats identifies a transmembrane protease causing both congenital and childhood onset autosomal recessive deafness. Nat Genet. 2001;27:59–63.PubMedCrossRefGoogle Scholar
  180. Sedghizadeh PP, Mallery SR, Thompson SJ, Kresty L, Beck FM, Parkinson EK, Biancamano J, Lang JC. Expression of the serine protease DESC1 correlates directly with normal keratinocyte differentiation and inversely with head and neck squamous cell carcinoma progression. Head Neck. 2006;28:432–40.PubMedCrossRefGoogle Scholar
  181. Semenov AG, Tamm NN, Seferian KR, Postnikov AB, Karpova NS, Serebryanaya DV, Koshkina EV, Krasnoselsky MI, Katrukha AG. Processing of pro-B-type natriuretic peptide: furin and corin as candidate convertases. Clin Chem. 2010;56:1166–76.PubMedCrossRefGoogle Scholar
  182. Shi YE, Torri J, Yieh L, Wellstein A, Lippman ME, Dickson RB. Identification and characterization of a novel matrix-degrading protease from hormone-dependent human breast cancer cells. Cancer Res. 1993;53:1409–15.PubMedPubMedCentralGoogle Scholar
  183. Shi W, Fan W, Bai J, Tang Y, Wang L, Jiang Y, Tang L, Liu M, Cui W, Xu Y, Li Y. TMPRSS2 and MSPL facilitate trypsin-independent porcine epidemic diarrhea virus replication in vero cells. Virus 2017;9.Google Scholar
  184. Shigemasa K, Underwood LJ, Beard J, Tanimoto H, Ohama K, Parmley TH, O'Brien TJ. Overexpression of testisin, a serine protease expressed by testicular germ cells, in epithelial ovarian tumor cells. J Soc Gynecol Investig. 2000;7:358–62.PubMedPubMedCentralGoogle Scholar
  185. Shipway A, Danahay H, Williams JA, Tully DC, Backes BJ, Harris JL. Biochemical characterization of prostasin, a channel activating protease. Biochem Biophys Res Commun. 2004;324:953–63.PubMedCrossRefGoogle Scholar
  186. Shirato K, Kawase M, Matsuyama S. Middle East respiratory syndrome coronavirus infection mediated by the transmembrane serine protease TMPRSS2. J Virol. 2013;87:12552–61.PubMedPubMedCentralCrossRefGoogle Scholar
  187. Shirogane Y, Takeda M, Iwasaki M, Ishiguro N, Takeuchi H, Nakatsu Y, Tahara M, Kikuta H, Yanagi Y. Efficient multiplication of human metapneumovirus in Vero cells expressing the transmembrane serine protease TMPRSS2. J Virol. 2008;82:8942–6.PubMedPubMedCentralCrossRefGoogle Scholar
  188. Shulla A, Heald-Sargent T, Subramanya G, Zhao J, Perlman S, Gallagher T. A transmembrane serine protease is linked to the severe acute respiratory syndrome coronavirus receptor and activates virus entry. J Virol. 2011;85:873–82.CrossRefPubMedGoogle Scholar
  189. Silvestri L, Pagani A, Nai A, De Domenico I, Kaplan J, Camaschella C. The serine protease matriptase-2 (TMPRSS6) inhibits hepcidin activation by cleaving membrane hemojuvelin. Cell Metab. 2008;8:502–11.PubMedPubMedCentralCrossRefGoogle Scholar
  190. Somoza JR, Ho JD, Luong C, Ghate M, Sprengeler PA, Mortara K, Shrader WD, Sperandio D, Chan H, McGrath ME, Katz BA. The structure of the extracellular region of human hepsin reveals a serine protease domain and a novel scavenger receptor cysteine-rich (SRCR) domain. Structure. 2003;11:1123–31.PubMedCrossRefGoogle Scholar
  191. Spacek DV, Perez AF, Ferranti KM, Wu LK, Moy DM, Magnan DR, King TR. The mouse frizzy (fr) and rat ‘hairless’ (frCR) mutations are natural variants of protease serine S1 family member 8 (Prss8). Exp Dermatol. 2010;19:527–32.PubMedCrossRefGoogle Scholar
  192. Stefanska B, Huang J, Bhattacharyya B, Suderman M, Hallett M, Han ZG, Szyf M. Definition of the landscape of promoter DNA hypomethylation in liver cancer. Cancer Res. 2011;71:5891–903.PubMedCrossRefGoogle Scholar
  193. Stephan C, Yousef GM, Scorilas A, Jung K, Jung M, Kristiansen G, Hauptmann S, Kishi T, Nakamura T, Loening SA, Diamandis EP. Hepsin is highly over expressed in and a new candidate for a prognostic indicator in prostate cancer. J Urol. 2004;171:187–91.PubMedCrossRefGoogle Scholar
  194. Stieneke-Gröber A, Vey M, Angliker H, Shaw E, Thomas G, Roberts C, Klenk HD, Garten W. Influenza virus hemagglutinin with multibasic cleavage site is activated by furin, a subtilisin-like endoprotease. EMBO J. 1992;11:2407–14.PubMedPubMedCentralCrossRefGoogle Scholar
  195. Stirnberg M, Maurer E, Horstmeyer A, Kolp S, Frank S, Bald T, Arenz K, Janzer A, Prager K, Wunderlich P, Walter J, Gütschow M. Proteolytic processing of the serine protease matriptase-2: identification of the cleavage sites required for its autocatalytic release from the cell surface. Biochem J. 2010;430:87–95.PubMedCrossRefGoogle Scholar
  196. Szabo R, Bugge TH. Membrane-anchored serine proteases in vertebrate cell and developmental biology. Annu Rev Cell Dev Biol. 2011;27:213–35.PubMedPubMedCentralCrossRefGoogle Scholar
  197. Szabo R, Wu Q, Dickson RB, Netzel-Arnett S, Antalis TM, Bugge TH. Type II transmembrane serine proteases. Thromb Haemost. 2003;90:185–93. Review.PubMedPubMedCentralGoogle Scholar
  198. Szabo R, Netzel-Arnett S, Hobson JP, Antalis TM, Bugge TH. Matriptase-3 is a novel phylogenetically preserved membrane-anchored serine protease with broad serpin reactivity. Biochem J. 2005;390:231–42.PubMedPubMedCentralCrossRefGoogle Scholar
  199. Szabo R, Molinolo A, List K, Bugge TH. Matriptase inhibition by hepatocyte growth factor activator inhibitor-1 is essential for placental development. Oncogene. 2007;26:1546–56.PubMedCrossRefGoogle Scholar
  200. Szabo R, Hobson JP, Christoph K, Kosa P, List K, Bugge TH. Regulation of cell surface protease matriptase by HAI2 is essential for placental development, neural tube closure and embryonic survival in mice. Development. 2009;136:2653–63.PubMedPubMedCentralCrossRefGoogle Scholar
  201. Szabo R, Uzzun Sales K, Kosa P, Shylo NA, Godiksen S, Hansen KK, Friis S, Gutkind JS, Vogel LK, Hummler E, Camerer E, Bugge TH. Reduced prostasin (CAP1/PRSS8) activity eliminates HAI-1 and HAI-2 deficiency-associated developmental defects by preventing matriptase activation. PLoS Genet. 2012;8:e10029e37.CrossRefGoogle Scholar
  202. Szabo R, Lantsman T, Peters DE, Bugge TH. Delineation of proteolytic and non-proteolytic functions of the membrane-anchored serine protease prostasin. Development. 2016;143:2818–28.PubMedPubMedCentralCrossRefGoogle Scholar
  203. Takahashi M, Sano T, Yamaoka K, Kamimura T, Umemoto N, Nishitani H, Yasuoka S. Localization of human airway trypsin-like protease in the airway: an immunohistochemical study. Histochem Cell Biol. 2001;115:181–7.PubMedPubMedCentralGoogle Scholar
  204. Tanabe LM, List K. The role of type II transmembrane serine protease-mediated signaling in cancer. FEBS J. 2017;284:1421–36.PubMedCrossRefGoogle Scholar
  205. Tanaka H, Nagaike K, Takeda N, Itoh H, Kohama K, Fukushima T, Miyata S, Uchiyama S, Uchinokura S, Shimomura T, Miyazawa K, Kitamura N, Yamada G, Kataoka H. Hepatocyte growth factor activator inhibitor type 1 (HAI-1) is required for branching morphogenesis in the chorioallantoic placenta. Mol Cell Biol. 2005;25:5687–98.PubMedPubMedCentralCrossRefGoogle Scholar
  206. Tarnow C, Engels G, Arendt A, Schwalm F, Sediri H, Preuss A, Nelson PS, Garten W, Klenk HD, Gabriel G, Böttcher-Friebertshäuser E. TMPRSS2 is a host factor that is essential for pneumotropism and pathogenicity of H7N9 influenza A virus in mice. J Virol. 2014;88:4744–51.PubMedPubMedCentralCrossRefGoogle Scholar
  207. Tomlins SA, Rhodes DR, Perner S, Dhanasekaran SM, Mehra R, Sun XW, Varambally S, Cao X, Tchinda J, Kuefer R, Lee C, Montie JE, Shah RB, Pienta KJ, Rubin MA, Chinnaiyan AM. Recurrent fusion of TMPRSS2 and ETS transcription factor genes in prostate cancer. Science. 2005;310:644–8.PubMedCrossRefGoogle Scholar
  208. Tong Z, Illek B, Bhagwandin VJ, Verghese GM, Caughey GH. Prostasin, a membrane-anchored serine peptidase, regulates sodium currents in JME/CF15 cells, a cystic fibrosis airway epithelial cell line. Am J Physiol Lung Cell Mol Physiol. 2004;287:L928–35.PubMedCrossRefGoogle Scholar
  209. Tsuji A, Torres-Rosado A, Arai T, Le Beau MM, Lemons RS, Chou SH, Hepsin KK. a cell membrane-associated protease. Characterization, tissue distribution, and gene localization. J Biol Chem. 1991;266:16948–53.PubMedPubMedCentralGoogle Scholar
  210. Ujike M, Taguchi F. Incorporation of spike and membrane glycoproteins into coronavirus virions. Virus. 2015;7:1700–25. Review.CrossRefGoogle Scholar
  211. Underwood LJ, Shigemasa K, Tanimoto H, Beard JB, Schneider EN, Wang Y, Parmley TH, O'Brien TJ. Ovarian tumor cells express a novel multi-domain cell surface serine protease. Biochim Biophys Acta. 2000;1502:337–50.PubMedCrossRefGoogle Scholar
  212. Vallet V, Chraibi A, Gaeggeler HP, Horisberger JD, Rossier BC. An epithelial serine protease activates the amiloride-sensitive sodium channel. Nature. 1997;389:607–10.PubMedCrossRefGoogle Scholar
  213. Verghese GM, Gutknecht MF, Caughey GH. Prostasin regulates epithelial monolayer function: cell-specific Gpld1-mediated secretion and functional role for GPI anchor. Am J Physiol Cell Physiol. 2006;291:C1258–70.PubMedPubMedCentralCrossRefGoogle Scholar
  214. Verhelst J, Hulpiau P, Saelens X. Mx proteins: antiviral gatekeepers that restrain the uninvited. Microbiol Mol Biol Rev. 2013;77:551–66.PubMedPubMedCentralCrossRefGoogle Scholar
  215. Villalba M, Diaz-Lagares A, Redrado M, de Aberasturi AL, Segura V, Bodegas ME, Pajares MJ, Pio R, Freire J, Gomez-Roman J, Montuenga LM, Esteller M, Sandoval J, Calvo A. Epigenetic alterations leading to TMPRSS4 promoter hypomethylation and protein overexpression predict poor prognosis in squamous lung cancer patients. Oncotarget. 2016;7:22752–69.PubMedPubMedCentralCrossRefGoogle Scholar
  216. Vuagniaux G, Vallet V, Jaeger NF, Hummler E, Rossier BC. Synergistic activation of ENaC by three membrane-bound channel-activating serine proteases (mCAP1, mCAP2, and mCAP3) and serum- and glucocorticoid-regulated kinase (Sgk1) in Xenopus Oocytes. J Gen Physiol. 2002;120:191–201.PubMedPubMedCentralCrossRefGoogle Scholar
  217. Wallrapp C, Hähnel S, Müller-Pillasch F, Burghardt B, Iwamura T, Ruthenbürger M, Lerch MM, Adler G, Gress TMA. novel transmembrane serine protease (TMPRSS3) overexpressed in pancreatic cancer. Cancer Res. 2000;60:2602–6.PubMedPubMedCentralGoogle Scholar
  218. Wang CY, Meynard D, Lin HY. The role of TMPRSS6/matriptase-2 in iron regulation and anemia. Front Pharmacol. 2014;5:114.PubMedPubMedCentralGoogle Scholar
  219. Wang H, Zhou T, Peng J, Xu P, Dong N, Chen S, Wu Q. Distinct roles of N-glycosylation at different sites of corin in cell membrane targeting and ectodomain shedding. J Biol Chem. 2015;290:1654–63.PubMedCrossRefGoogle Scholar
  220. Wattenhofer M, Sahin-Calapoglu N, Andreasen D, Kalay E, Caylan R, Braillard B, Fowler-Jaeger N, Reymond A, Rossier BC, Karaguzel A, Antonarakis SE. A novel TMPRSS3 missense mutation in a DFNB8/10 family prevents proteolytic activation of the protein. Hum Genet. 2005;117:528–35.PubMedCrossRefGoogle Scholar
  221. Wilson S, Greer B, Hooper J, Zijlstra A, Walker B, Quigley J, Hawthorne S. The membrane-anchored serine protease, TMPRSS2, activates PAR-2 in prostate cancer cells. Biochem J. 2005;388:967–72.PubMedPubMedCentralCrossRefGoogle Scholar
  222. Wong GW, Tang Y, Feyfant E, Sali A, Li L, Li Y, Huang C, Friend DS, Krilis SA, Stevens RL. Identification of a new member of the tryptase family of mouse and human mast cell proteases which possesses a novel COOH-terminal hydrophobic extension. J Biol Chem. 1999;274:30784–93.PubMedCrossRefGoogle Scholar
  223. Wu Q, Yu D, Post J, Halks-Miller M, Sadler JE, Morser J. Generation and characterization of mice deficient in hepsin, a hepatic transmembrane serine protease. J Clin Invest. 1998;101:321–6.PubMedPubMedCentralCrossRefGoogle Scholar
  224. Wu C, Wu F, Pan J, Morser J, Wu Q. Furin-mediated processing of Pro-C-type natriuretic peptide. J Biol Chem. 2003;278:25847–52.PubMedCrossRefGoogle Scholar
  225. Yamaguchi N, Okui A, Yamada T, Nakazato H, Mitsui S. Spinesin/TMPRSS5, a novel transmembrane serine protease, cloned from human spinal cord. J Biol Chem. 2002;277:6806–12.PubMedCrossRefGoogle Scholar
  226. 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;273:11895–901.PubMedCrossRefGoogle Scholar
  227. Yan W, Sheng N, Seto M, Morser J, Wu Q. Corin, a mosaic transmembrane serine protease encoded by a novel cDNA from human heart. J Biol Chem. 1999;274(21):14926–35.PubMedCrossRefGoogle Scholar
  228. Yan W, Wu F, Morser J, Wu Q. Corin, a transmembrane cardiac serine protease, acts as a pro-atrial natriuretic peptide-converting enzyme. Proc Natl Acad Sci U S A. 2000;97:8525–9.PubMedPubMedCentralCrossRefGoogle Scholar
  229. Yasuoka S, Ohnishi T, Kawano S, Tsuchihashi S, Ogawara M, Masuda K, Yamaoka K, Takahashi M, Sano T. Purification, characterization, and localization of a novel trypsin-like protease found in the human airway. Am J Respir Cell Mol Biol. 1997;16:300–8.PubMedPubMedCentralCrossRefGoogle Scholar
  230. Yoshinaga S, Nakahori Y, Yasuoka S. Fibrinogenolytic activity of a novel trypsin-like enzyme found in human airway. J Med Invest. 1998;45:77–86.PubMedPubMedCentralGoogle Scholar
  231. Yu JX, Chao L, Chao J. Prostasin is a novel human serine proteinase from seminal fluid. Purification, tissue distribution, and localization in prostate gland. J Biol Chem. 1994;269:18843–8.PubMedPubMedCentralGoogle Scholar
  232. Yuan X, Zheng X, Lu D, Rubin DC, Pung CY, Sadler JE. Structure of murine enterokinase (enteropeptidase) and expression in small intestine during development. Am J Physiol. 1998;274:G342–9.PubMedPubMedCentralGoogle Scholar
  233. Yun B, Zhang Y, Liu Y, Guan X, Wang Y, Qi X, Cui H, Liu C, Zhang Y, Gao H, Gao L, Li K, Gao Y, Wang X. TMPRSS12 is an activating protease for Subtype B Avian Metapneumovirus. J Virol. 2016;90:11231–46.PubMedPubMedCentralCrossRefGoogle Scholar
  234. Zamolodchikova TS, Sokolova EA, Alexandrov SL, Mikhaleva II, Prudchenko IA, Morozov IA, Kononenko NV, Mirgorodskaya OA, Da U, Larionova NI, Pozdnev VF, Ghosh D, Duax WL, Vorotyntseva TI. Subcellular localization, substrate specificity and crystallization of duodenase, a potential activator of enteropeptidase. Eur J Biochem. 1997;249:612–21.PubMedCrossRefGoogle Scholar
  235. Zamolodchikova TS, Sokolova EA, Lu D, Sadler JE. Activation of recombinant proenteropeptidase by duodenase. FEBS Lett. 2000;466:295–9.PubMedCrossRefGoogle Scholar
  236. Zhang D, Qiu S, Wang Q, Zheng J. TMPRSS3 modulates ovarian cancer cell proliferation, invasion and metastasis. Oncol Rep. 2016;35:81–8.PubMedCrossRefGoogle Scholar
  237. Zhang Z, Hu Y, Yan R, Dong L, Jiang Y, Zhou Z, Liu M, Zhou T, Dong N, Wu Q. The transmembrane serine protease HAT-like 4 is important for epidermal barrier function to prevent body fluid loss. Sci Rep. 2017;7:45262.PubMedPubMedCentralCrossRefGoogle Scholar
  238. Zhao N, Wang J, Cui Y, Guo L, Lu SH. Induction of G1 cell cycle arrest and P15INK4b expression by ECRG1 through interaction with Miz-1. J Cell Biochem. 2004;92:65–76.PubMedCrossRefGoogle Scholar
  239. Zheng X, Sadler JE. Mucin-like domain of enteropeptidase directs apical targeting in Madin-Darby canine kidney cells. J Biol Chem. 2002;277:6858–63.PubMedCrossRefGoogle Scholar
  240. Zheng XL, Kitamoto Y, Sadler JE. Enteropeptidase, a type II transmembrane serine protease. Front Biosci (Elite Ed). 2009;1:242–9. Review.Google Scholar
  241. Zhirnov O, Klenk HD. Human influenza A viruses are proteolytically activated and do not induce apoptosis in CACO-2 cells. Virology. 2003;313(1):198–212.PubMedCrossRefGoogle Scholar
  242. Zhirnov OP, Ikizler MR, Wright PF. Cleavage of influenza a virus hemagglutinin in human respiratory epithelium is cell associated and sensitive to exogenous antiproteases. J Virol. 2002;76:8682–9.PubMedPubMedCentralCrossRefGoogle Scholar
  243. Zhou X, Chen J, Zhang Q, Shao J, Du K, Xu X, Kong Y. Prognostic value of plasma soluble corin in patients with acute myocardial infarction. J Am Coll Cardiol. 2016;67:2008–14.PubMedCrossRefGoogle Scholar
  244. Zmora P, Blazejewska P, Moldenhauer AS, Welsch K, Nehlmeier I, Wu Q, Schneider H, Pöhlmann S, Bertram S. DESC1 and MSPL activate influenza A viruses and emerging coronaviruses for host cell entry. J Virol. 2014;88:12087–97.PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Institute of VirologyPhilipps-University MarburgMarburgGermany

Personalised recommendations

Cite chapter

Buy options