A matriptase-prostasin reciprocal zymogen activation complex with unique features: Prostasin as a non-enzymatic co-factor for matriptase activation

Journal of Biological Chemistry

Volumn 288, Issue 26, 2013, Pages 19028-19039

  Friis, Stine ^a,c   Sales, Katiuchia Uzzun ^a,b   Godiksen, Sine ^a,c,d   Peters, Diane E ^a,e   Lin, Chen Yong ^f   Vogel, Lotte K ^c   Bugge, Thomas H ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b NATIONAL INSTITUTE OF DENTAL AND CRANIOFACIAL RESEARCH   (United States)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d UNIVERSITY OF COPENHAGEN   (Denmark)

^e TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f GEORGETOWN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURFACES; DOWNSTREAM TARGET; EPITHELIAL DEVELOPMENT; NON-ENZYMATIC; SERINE PROTEASE; TRANSGENIC MICE; UNIQUE FEATURES; ZYMOGEN ACTIVATION;

AMINO ACIDS; CELL MEMBRANES;

MAMMALS;

MATRIPTASE; PROSTASIN; PROTEINASE ACTIVATED RECEPTOR 2;

ALLOSTERISM; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CATALYSIS; CELL STRAIN HEK293; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; EPIDERMIS; EPITHELIUM CELL; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; TRANSGENIC MOUSE;

ALLOSTERIC CO-FACTOR; ENZYME MECHANISMS; EPITHELIAL CELL; MATRIPTASE; PROSTASIN; PROTEASE CASCADE; PROTEASE INHIBITOR; PROTEIN COMPLEXES; RECIPROCAL ZYMOGEN CONVERSION; SERINE PROTEASE;

ALLOSTERIC SITE; ANIMALS; BINDING SITES; CACO-2 CELLS; CATALYSIS; ENZYME ACTIVATION; ENZYME PRECURSORS; EPITHELIAL CELLS; FEMALE; HEK293 CELLS; HUMANS; MALE; MICE; MICE, TRANSGENIC; PEPTIDE HYDROLASES; PHENOTYPE; SERINE ENDOPEPTIDASES;

MUS MUSCULUS;

EID: 84879560367     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.469932     Document Type: Article

References (55)

1. Leyvraz, C., Charles, R. P., Rubera, I., Guitard, M., Rotman, S., Breiden, B., Sandhoff, K., and Hummler, E. (2005) The epidermal barrier function is dependent on the serine protease CAP1/Prss8. J. Cell Biol. 170, 487-496 (Pubitemid 41126947)
2. List, K., Hobson, J. P., Molinolo, A., and Bugge, T. H. (2007) Co-localization of the channel activating protease prostasin/(CAP1/PRSS8) with its candidate activator, matriptase. J. Cell. Physiol. 213, 237-245 (Pubitemid 47378812)
3. Spacek, D. V., Perez, A. F., Ferranti, K. M., Wu, L. K., Moy, D. M., Magnan, D. R., and King, T. R. (2010) The mouse frizzy (fr) and rat "hairless" (frCR) mutations are natural variants of protease serine S1 family member 8 (Prss8). Exp. Dermatol. 19, 527-532
4. List, K., Haudenschild, C. C., Szabo, R., Chen, W., Wahl, S. M., Swaim, W., Engelholm, L. H., Behrendt, N., and Bugge, T. H. (2002) Matriptase/MT-SP1 is required for postnatal survival, epidermal barrier function, hair follicle development, and thymic homeostasis. Oncogene 21, 3765-3779 (Pubitemid 34620539)
5. List, K., Kosa, P., Szabo, R., Bey, A. L., Wang, C. B., Molinolo, A., and Bugge, T. H. (2009) Epithelial integrity is maintained by a matriptase-dependent proteolytic pathway. Am. J. Pathol. 175, 1453-1463
6. List, K., Szabo, R., Wertz, P. W., Segre, J., Haudenschild, C. C., Kim, S. Y., and Bugge, T. H. (2003) Loss of proteolytically processed filaggrin caused by epidermal deletion of Matriptase/MT-SP1. J. Cell Biol. 163, 901-910 (Pubitemid 37517896)
7. Szabo, R., and Bugge, T. H. (2011) Membrane-anchored serine proteases in vertebrate cell and developmental biology. Annu. Rev. Cell. Dev. Biol. 27, 213-235
8. Lin, C. Y., Anders, J., Johnson, M., Sang, Q. A., and Dickson, R. B. (1999) Molecular cloning of cDNA for matriptase, a matrix-degrading serine protease with trypsin-like activity. J. Biol. Chem. 274, 18231-18236
9. Kim, M. G., Chen, C., Lyu, M. S., Cho, E. G., Park, D., Kozak, C., and Schwartz, R. H. (1999) Cloning and chromosomal mapping of a gene isolated from thymic stromal cells encoding a new mouse type II membrane serine protease, epithin, containing four LDL receptor modules and two CUB domains. Immunogenetics 49, 420-428 (Pubitemid 29178825)
10. Takeuchi, T., Harris, J. L., Huang, W., Yan, K. W., Coughlin, S. R., and Craik, C. S. (2000) Cellular localization of membrane-type serine protease 1 and identification of protease-activated receptor-2 and single-chain urokinase-type plasminogen activator as substrates. J. Biol. Chem. 275, 26333-26342
11. Macao, B., Johansson, D. G., Hansson, G. C., and Härd, T. (2006) Autoproteolysis coupled to protein folding in the SEA domain of the membrane-bound MUC1 mucin. Nat. Struct. Mol. Biol. 13, 71-76 (Pubitemid 43049405)
12. Oberst, M. D., Williams, C. A., Dickson, R. B., Johnson, M. D., and Lin, C. Y. (2003) The activation of matriptase requires its noncatalytic domains, serine protease domain, and its cognate inhibitor. J. Biol. Chem. 278, 26773-26779 (Pubitemid 36876825)
13. Cho, E. G., Kim, M. G., Kim, C., Kim, S. R., Seong, I. S., Chung, C., Schwartz, R. H., and Park, D. (2001) N-terminal processing is essential for release of epithin, a mouse type II membrane serine protease. J. Biol. Chem. 276, 44581-44589
14. Inouye, K., Yasumoto, M., Tsuzuki, S., Mochida, S., and Fushiki, T. (2010) The optimal activity of a pseudozymogen form of recombinant matriptase under the mildly acidic pH and low ionic strength conditions. J. Biochem. 147, 485-492
15. Takeuchi, T., Shuman, M. A., and Craik, C. S. (1999) Reverse biochemistry. Use of macromolecular protease inhibitors to dissect complex biological processes and identify a membrane-type serine protease in epithelial cancer and normal tissue. Proc. Natl. Acad. Sci. U.S.A. 96, 11054-11061 (Pubitemid 29487326)
16. Yu, J. X., Chao, L., and Chao, J. (1994) Prostasin is a novel human serine proteinase from seminal fluid. Purification, tissue distribution, and localization in prostate gland. J. Biol. Chem. 269, 18843-18848
17. Yu, J. X., Chao, L., and Chao, J. (1995) Molecular cloning, tissue-specific expression, and cellular localization of human prostasin mRNA. J. Biol. Chem. 270, 13483-13489
18. Shipway, A., Danahay, H., Williams, J. A., Tully, D. C., Backes, B. J., and Harris, J. L. (2004) Biochemical characterization of prostasin, a channel activating protease. Biochem. Biophys. Res. Commun. 324, 953-963 (Pubitemid 39359197)
19. Lin, C. Y., Anders, J., Johnson, M., and Dickson, R. B. (1999) Purification and characterization of a complex containing matriptase and a Kunitztype serine protease inhibitor from human milk. J. Biol. Chem. 274, 18237-18242
20. Tseng, I. C., Chou, F. P., Su, S. F., Oberst, M., Madayiputhiya, N., Lee, M. S., Wang, J. K., Sloane, D. E., Johnson, M., and Lin, C. Y. (2008) Purification from human milk of matriptase complexes with secreted serpins. Mechanism for inhibition of matriptase other than HAI-1. Am. J. Physiol. Cell Physiol. 295, C423-C431 (Pubitemid 352755786)
21. Szabo, R., Hobson, J. P., Christoph, K., Kosa, P., List, K., and Bugge, T. H. (2009) Regulation of cell surface protease matriptase by HAI2 is essential for placental development, neural tube closure and embryonic survival in mice. Development 136, 2653-2663
22. Szabo, R., Hobson, J. P., List, K., Molinolo, A., Lin, C. Y., and Bugge, T. H. (2008) Potent inhibition and global co-localization implicate the transmembrane Kunitz-type serine protease inhibitor hepatocyte growth factor activator inhibitor-2 in the regulation of epithelial matriptase activity. J. Biol. Chem. 283, 29495-29504
23. Szabo, R., Kosa, P., List, K., and Bugge, T. H. (2009) Loss of matriptase suppression underlies spint1 mutation-associated ichthyosis and postnatal lethality. Am. J. Pathol. 174, 2015-2022
24. Szabo, R., Molinolo, A., List, K., and Bugge, T. H. (2007) Matriptase inhibition by hepatocyte growth factor activator inhibitor-1 is essential for placental development. Oncogene 26, 1546-1556 (Pubitemid 46398747)
25. Szabo, R., Uzzun Sales, K., Kosa, P., Shylo, N. A., Godiksen, S., Hansen, K. K., Friis, S., Gutkind, J. S., Vogel, L. K., Hummler, E., Camerer, E., and Bugge, T. H. (2012) Reduced prostasin (CAP1/PRSS8) activity eliminates HAI-1 and HAI-2 deficiency-associated developmental defects by preventing matriptase activation. PLoS Genet. 8, e1002937
26. Chen, Y. W., Wang, J. K., Chou, F. P., Chen, C. Y., Rorke, E. A., Chen, L. M., Chai, K. X., Eckert, R. L., Johnson, M. D., and Lin, C. Y. (2010) Regulation of the matriptase-prostasin cell surface proteolytic cascade by hepatocyte growth factor activator inhibitor-1 during epidermal differentiation. J. Biol. Chem. 285, 31755-31762
27. Netzel-Arnett, S., Currie, B. M., Szabo, R., Lin, C. Y., Chen, L. M., Chai, K. X., Antalis, T. M., Bugge, T. H., and List, K. (2006) Evidence for a matriptase-prostasin proteolytic cascade regulating terminal epidermal differentiation. J. Biol. Chem. 281, 32941-32945 (Pubitemid 46036678)
28. Camerer, E., Barker, A., Duong, D. N., Ganesan, R., Kataoka, H., Cornelissen, I., Darragh, M. R., Hussain, A., Zheng, Y. W., Srinivasan, Y., Brown, C., Xu, S. M., Regard, J. B., Lin, C. Y., Craik, C. S., Kirchhofer, D., and Coughlin, S. R. (2010) Local protease signaling contributes to neural tube closure in the mouse embryo. Dev. Cell 18, 25-38
29. Buzza, M. S., Martin, E. W., Driesbaugh, K. H., Désilets, A., Leduc, R., and Antalis, T. M. (2013) Prostasin is required for matriptase activation in intestinal epithelial cells to regulate closure of the paracellular pathway. J. Biol. Chem. 288, 10328-10337
30. Bugge, T. H., Antalis, T. M., and Wu, Q. (2009) Type II transmembrane serine proteases. J. Biol. Chem. 284, 23177-23181
31. Friis, S., Godiksen, S., Bornholdt, J., Selzer-Plon, J., Rasmussen, H. B., Bugge, T. H., Lin, C. Y., and Vogel, L. K. (2011) Transport via the transcytotic pathway makes prostasin available as a substrate for matriptase. J. Biol. Chem. 286, 5793-5802
32. Lin, C. Y., Wang, J. K., Torri, J., Dou, L., Sang, Q. A., and Dickson, R. B. (1997) Characterization of a novel, membrane-bound, 80-kDa matrix-degrading protease from human breast cancer cells. Monoclonal antibody production, isolation, and localization. J. Biol. Chem. 272, 9147-9152 (Pubitemid 27154920)
33. Alam, J., and Cook, J. L. (1990) Reporter genes. Application to the study of mammalian gene transcription. Anal. Biochem. 188, 245-254 (Pubitemid 20265164)
34. Murillas, R., Larcher, F., Conti, C. J., Santos, M., Ullrich, A., and Jorcano, J. L. (1995) Expression of a dominant negative mutant of epidermal growth factor receptor in the epidermis of transgenic mice elicits striking alterations in hair follicle development and skin structure. EMBO J. 14, 5216-5223
35. List, K., Szabo, R., Molinolo, A., Sriuranpong, V., Redeye, V., Murdock, T., Burke, B., Nielsen, B. S., Gutkind, J. S., and Bugge, T. H. (2005) Deregulated matriptase causes ras-independent multistage carcinogenesis and promotes ras-mediated malignant transformation. Genes Dev. 19, 1934-1950 (Pubitemid 41186993)
36. Oberst, M. D., Chen, L. Y., Kiyomiya, K., Williams, C. A., Lee, M. S., Johnson, M. D., Dickson, R. B., and Lin, C. Y. (2005) HAI-1 regulates activation and expression of matriptase, a membrane-bound serine protease. Am. J. Physiol. Cell Physiol. 289, C462-C470 (Pubitemid 41008893)
37. List, K., Bugge, T. H., and Szabo, R. (2006) Matriptase. Potent proteolysis on the cell surface. Mol. Med. 12, 1-7 (Pubitemid 44128372)
38. Frateschi, S., Camerer, E., Crisante, G., Rieser, S., Membrez, M., Charles, R. P., Beermann, F., Stehle, J. C., Breiden, B., Sandhoff, K., Rotman, S., Haftek, M., Wilson, A., Ryser, S., Steinhoff, M., Coughlin, S. R., and Hummler, E. (2011) PAR2 absence completely rescues inflammation and ichthyosis caused by altered CAP1/Prss8 expression in mouse skin. Nat. Commun. 2, 161
39. Inouye, K., Tsuzuki, S., Yasumoto, M., Kojima, K., Mochida, S., and Fushiki, T. (2010) Identification of the matriptase second CUB domain as the secondary site for interaction with hepatocyte growth factor activator inhibitor type-1. J. Biol. Chem. 285, 33394-33403
40. Ellis, V., Behrendt, N., and Danø, K. (1991) Plasminogen activation by receptor-bound urokinase. A kinetic study with both cell-associated and isolated receptor. J. Biol. Chem. 266, 12752-12758 (Pubitemid 21907159)
41. Ellis, V., and Danø, K. (1993) Potentiation of plasminogen activation by an anti-urokinase monoclonal antibody due to ternary complex formation.A mechanistic model for receptor-mediated plasminogen activation. J. Biol. Chem. 268, 4806-4813
42. Bergum, C., Zoratti, G., Boerner, J., and List, K. (2012) Strong expression association between matriptase and its substrate prostasin in breast cancer. J. Cell. Physiol. 227, 1604-1609
43. Cheng, M. F., Jin, J. S., Wu, H. W., Chiang, P. C., Sheu, L. F., and Lee, H. S. (2007) Matriptase expression in the normal and neoplastic mast cells. Eur. J. Dermatol. 17, 375-380
44. Kilpatrick, L. M., Harris, R. L., Owen, K. A., Bass, R., Ghorayeb, C., Bar-Or, A., and Ellis, V. (2006) Initiation of plasminogen activation on the surface of monocytes expressing the type II transmembrane serine protease matriptase. Blood 108, 2616-2623
45. Firsov, D., Gautschi, I., Merillat, A. M., Rossier, B. C., and Schild, L. (1998) The heterotetrameric architecture of the epithelial sodium channel (ENaC). EMBO J. 17, 344-352 (Pubitemid 28045475)
46. Rossier, B. C., Pradervand, S., Schild, L., and Hummler, E. (2002) Epithelial sodium channel and the control of sodium balance. Interaction between genetic and environmental factors. Annu. Rev. Physiol. 64, 877-897 (Pubitemid 34259252)
47. Garty, H., and Palmer, L. G. (1997) Epithelial sodium channels. Function, structure, and regulation. Physiol. Rev. 77, 359-396 (Pubitemid 27184343)
48. Bruns, J. B., Carattino, M. D., Sheng, S., Maarouf, A. B., Weisz, O. A., Pilewski, J. M., Hughey, R. P., and Kleyman, T. R. (2007) Epithelial Na+ channels are fully activated by furin- and prostasin-dependent release of an inhibitory peptide from the γ-subunit. J. Biol. Chem. 282, 6153-6160 (Pubitemid 47100869)
49. Narikiyo, T., Kitamura, K., Adachi, M., Miyoshi, T., Iwashita, K., Shiraishi, N., Nonoguchi, H., Chen, L. M., Chai, K. X., Chao, J., and Tomita, K. (2002) Regulation of prostasin by aldosterone in the kidney. J. Clin. Invest. 109, 401-408 (Pubitemid 34141814)
50. Planès, C., Randrianarison, N. H., Charles, R.-P., Frateschi, S., Cluzeaud, F., Vuagniaux, G., Soler, P., Clerici, C., Rossier, B. C., and Hummler, E. (2010) ENaC-mediated alveolar fluid clearance and lung fluid balance depend on the channel-activating protease 1. EMBO Mol. Med. 2, 26-37
51. Tong, Z., Illek, B., Bhagwandin, V. J., Verghese, G. M., and Caughey, G. H. (2004) 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. 287, L928-L935 (Pubitemid 39391022)
52. 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, P. L., Kudoh, J., Shimizu, N., Scott, H. S., Antonarakis, S. E., and Rossier, B. C. (2002) The transmembrane serine protease (TMPRSS3) mutated in deafness DFNB8/10 activates the epithelial sodium channel (ENaC) in vitro. Hum. Mol. Genet. 11, 2829-2836 (Pubitemid 35331815)
53. Vuagniaux, G., Vallet, V., Jaeger, N. F., Hummler, E., and Rossier, B. C. (2002) 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. 120, 191-201 (Pubitemid 34857968)
54. Vallet, V., Chraibi, A., Gaeggeler, H. P., Horisberger, J. D., and Rossier, B. C. (1997) An epithelial serine protease activates the amiloride-sensitive sodium channel. Nature 389, 607-610 (Pubitemid 27446178)
55. Andreasen, D., Vuagniaux, G., Fowler-Jaeger, N., Hummler, E., and Rossier, B. C. (2006) 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. 17, 968-976