Prostasin is required for matriptase activation in intestinal epithelial cells to regulate closure of the paracellular pathway

Journal of Biological Chemistry

Volumn 288, Issue 15, 2013, Pages 10328-10337

  Marguerite S Buzza, ^a   Martin, Erik W ^a   Driesbaugh, Kathryn H ^a   Désilets, Antoine ^b   Leduc, Richard ^b   Antalis, Toni M ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF SHERBROOKE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CELL MEMBRANES;

BARRIER FORMATION; EPITHELIAL BARRIER; INTESTINAL EPITHELIAL CELLS; INTESTINAL EPITHELIUM; PROTEOLYTIC CASCADE; SERINE PROTEASE; STRATUM CORNEUM; TISSUE SPECIFICS;

CHEMICAL ACTIVATION;

ENZYME PRECURSOR; MATRIPTASE; PROSTASIN; PROTEINASE; RECOMBINANT PROTEIN; SMALL INTERFERING RNA;

ARTICLE; CELL FUNCTION; CELL POLARITY; CELL STRAIN CACO 2; CONTROLLED STUDY; DRUG ACTIVITY; ENZYME ACTIVATION; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; INTESTINE EPITHELIUM CELL; PERMEABILITY BARRIER; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SKIN; TIGHT JUNCTION;

EID: 84876247967     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.443432     Document Type: Article

References (58)

1. 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
2. Antalis, T. M., Buzza, M. S., Hodge, K. M., Hooper, J. D., and Netzel- Arnett, S. (2010) The cutting edge: membrane-anchored serine protease activities in the pericellular microenvironment. Biochem. J. 428, 325-346
3. Miller, G. S., and List, K. (2013) The matriptase-prostasin proteolytic cascade in epithelial development and pathology. Cell Tissue Res. 351, 245-253
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/MTSP1 is required for postnatal survival, epidermal barrier function, hair follicle development, and thymic homeostasis. Oncogene 21, 3765-3779
5. Basel-Vanagaite, L., Attia, R., Ishida-Yamamoto, A., Rainshtein, L., Ben Amitai, D., Lurie, R., Pasmanik-Chor, M., Indelman, M., Zvulunov, A., Saban, S., Magal, N., Sprecher, E., and Shohat, M. (2007) Autosomal recessive ichthyosis with hypotrichosis caused by a mutation in ST14, encoding type II transmembrane serine protease matriptase. Am. J. Hum. Genet. 80, 467-477
6. 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
7. 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
8. 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
9. Chen, M., Chen, L. M., Lin, C. Y., and Chai, K. X. (2010) Hepsin activates prostasin and cleaves the extracellular domain of the epidermal growth factor receptor. Mol. Cell Biochem. 337, 259-266
10. 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
11. 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
12. Frateschi, S., Keppner, A., Malsure, S., Iwaszkiewicz, J., Sergi, C., Merillat, A. M., Fowler-Jaeger, N., Randrianarison, N., Planès, C., and Hummler, E. (2012) Mutations of the serine protease CAP1/Prss8 lead to reduced embryonic viability, skin defects, and decreased ENaC activity. Am. J. Pathol. 181, 605-615
13. 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
14. 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
15. 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
16. 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
17. 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
18. List, K., Currie, B., Scharschmidt, T. C., Szabo, R., Shireman, J., Molinolo, A., Cravatt, B. F., Segre, J., and Bugge, T. H. (2007) Autosomal ichthyosis with hypotrichosis syndrome displays low matriptase proteolytic activity and is phenocopied in ST14 hypomorphic mice. J. Biol. Chem. 282, 36714-36723
19. Buzza, M. S., Netzel-Arnett, S., Shea-Donohue, T., Zhao, A., Lin, C. Y., List, K., Szabo, R., Fasano, A., Bugge, T. H., and Antalis, T. M. (2010) Membrane-anchored serine protease matriptase regulates epithelial barrier formation and permeability in the intestine. Proc. Natl. Acad. Sci. U.S.A. 107, 4200-4205
20. Kosa, P., Szabo, R., Molinolo, A. A., and Bugge, T. H. (2012) Suppression of Tumorigenicity-14, encoding matriptase, is a critical suppressor of colitis and colitis-associated colon carcinogenesis. Oncogene 31, 3679-3695
21. Netzel-Arnett, S., Buzza, M. S., Shea-Donohue, T., Désilets, A., Leduc, R., Fasano, A., Bugge, T. H., and Antalis, T. M. (2012) Matriptase protects against experimental colitis and promotes intestinal barrier recovery. In- flamm. Bowel Dis. 18, 1303-1314
22. Simons, K., and Fuller, S. D. (1985) Cell surface polarity in epithelia. Annu. Rev. Cell Biol. 1, 243-288
23. Cereijido, M., Meza, I., and Martínez-Palomo, A. (1981) Occluding junctions in cultured epithelial monolayers. Am. J. Physiol. 240, C96-102
24. Sambuy, Y., De Angelis, I., Ranaldi, G., Scarino, M. L., Stammati, A., and Zucco, F. (2005) The Caco-2 cell line as a model of the intestinal barrier: influence of cell and culture-related factors on Caco-2 cell functional characteristics. Cell Biol. Toxicol. 21, 1-26
25. Wang, J. K., Lee, M. S., Tseng, I. C., Chou, F. P., Chen, Y. W., Fulton, A., Lee, H. S., Chen, C. J., Johnson, M. D., and Lin, C. Y. (2009) Polarized epithelial cells secrete matriptase as a consequence of zymogen activation and HAI-1-mediated inhibition. Am. J. Physiol. Cell Physiol. 297, C459-470
26. 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
27. 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
28. 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
29. Sanders, S. E., Madara, J. L., McGuirk, D. K., Gelman, D. S., and Colgan, S. P. (1995) Assessment of inflammatory events in epithelial permeability: a rapid screening method using fluorescein dextrans. Epithelial Cell Biol. 4, 25-34
30. Désilets, A., Longpré, J. M., Beaulieu, M. E., and Leduc, R. (2006) Inhibition of human matriptase by eglin c variants. FEBS Lett. 580, 2227-2232
31. Désilets, A., Béliveau, F., Vandal, G., McDuff, F. O., Lavigne, P., and Leduc, R. (2008) Mutation G827R in matriptase causing autosomal recessive ichthyosis with hypotrichosis yields an inactive protease. J. Biol. Chem. 283, 10535-10542
32. Lin, C. Y., Tseng, I. C., Chou, F. P., Su, S. F., Chen, Y. W., Johnson, M. D., and Dickson, R. B. (2008) Zymogen activation, inhibition, and ectodomain shedding of matriptase. Front Biosci. 13, 621-635
33. 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
34. Vuagniaux, G., Vallet, V., Jaeger, N. F., Pfister, C., Bens, M., Farman, N., Courtois-Coutry, N., Vandewalle, A., Rossier, B. C., and Hummler, E. (2000) Activation of the amiloride-sensitive epithelial sodium channel by the serine protease mCAP1 expressed in a mouse cortical collecting duct cell line. J. Am. Soc. Nephrol. 11, 828-834
35. 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 -subunit. J. Biol. Chem. 282, 6153-6160
36. Mankertz, J., and Schulzke, J. D. (2007) Altered permeability in inflammatory bowel disease: pathophysiology and clinical implications. Curr. Opin. Gastroenterol. 23, 379-383
37. Salim, S. Y., and Söderholm, J. D. (2011) Importance of disrupted intestinal barrier in inflammatory bowel diseases. Inflamm. Bowel. Dis. 17, 362-381
38. Swystun, V. A., Renaux, B., Moreau, F., Wen, S., Peplowski, M. A., Hollenberg, M. D., and MacNaughton, W. K. (2009) Serine proteases decrease intestinal epithelial ion permeability by activation of protein kinase C. Am. J. Physiol. Gastrointest. Liver Physiol. 297, G60-70
39. Steensgaard, M., Svenningsen, P., Tinning, A. R., Nielsen, T. D., Jorgensen, F., Kjaersgaard, G., Madsen, K., and Jensen, B. L. (2010) Apical serine protease activity is necessary for assembly of a high-resistance renal collecting duct epithelium. Acta Physiol. (Oxf) 200, 347-359
40. Vetrano, S., Ploplis, V. A., Sala, E., Sandoval-Cooper, M., Donahue, D. L., Correale, C., Arena, V., Spinelli, A., Repici, A., Malesci, A., Castellino, F. J., and Danese, S. (2011) Unexpected role of anticoagulant protein C in controlling epithelial barrier integrity and intestinal inflammation. Proc. Natl. Acad. Sci. U.S.A. 108, 19830-19835
41. Shen, L., Weber, C. R., Raleigh, D. R., Yu, D., and Turner, J. R. (2011) Tight junction pore and leak pathways: a dynamic duo. Annu. Rev. Physiol. 73, 283-309
42. Anderson, J. M., and Van Itallie, C. M. (2009) Physiology and function of the tight junction. Cold Spring Harb. Perspect. Biol. 1, a002584
43. List, K., Szabo, R., Molinolo, A., Nielsen, B. S., and Bugge, T. H. (2006) Delineation of matriptase protein expression by enzymatic gene trapping suggests diverging roles in barrier function, hair formation, and squamous cell carcinogenesis. Am. J. Pathol. 168, 1513-1525
44. 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
45. Oberst, M. D., Singh, B., Ozdemirli, M., Dickson, R. B., Johnson, M. D., and Lin, C. Y. (2003) Characterization of matriptase expression in normal human tissues. J. Histochem. Cytochem. 51, 1017-1025
46. 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
47. Tsuzuki, S., Murai, N., Miyake, Y., Inouye, K., Hirayasu, H., Iwanaga, T., and Fushiki, T. (2005) Evidence for the occurrence of membrane-type serine protease 1/matriptase on the basolateral sides of enterocytes. Biochem. J. 388, 679-687
48. 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
49. Lee, M. S., Tseng, I. C., Wang, Y., Kiyomiya, K., Johnson, M. D., Dickson, R. B., and Lin, C. Y. (2007) Autoactivation of matriptase in vitro: requirement for biomembrane and LDL receptor domain. Am. J. Physiol. Cell Physiol. 293, C95-105
50. Lee, M. S., Kiyomiya, K., Benaud, C., Dickson, R. B., and Lin, C. Y. (2005) Simultaneous activation and hepatocyte growth factor activator inhibitor 1-mediated inhibition of matriptase induced at activation foci in human mammary epithelial cells. Am. J. Physiol. Cell Physiol. 288, C932-941
51. Inouye, K., Tomoishi, M., Yasumoto, M., Miyake, Y., Kojima, K., Tsuzuki, S., and Fushiki, T. (2013) Roles of CUB and LDL receptor class A domain repeats of a transmembrane serine protease matriptase in its zymogen activation. J. Biochem. 153, 51-61
52. Godiksen, S., Selzer-Plon, J., Pedersen, E. D., Abell, K., Rasmussen, H. B., Szabo, R., Bugge, T. H., and Vogel, L. K. (2008) Hepatocyte growth factor activator inhibitor-1 has a complex subcellular itinerary. Biochem. J. 413, 251-259
53. Fan, B., Wu, T. D., Li, W., and Kirchhofer, D. (2005) Identification of hepatocyte growth factor activator inhibitor-1B as a potential physiological inhibitor of prostasin. J. Biol. Chem. 280, 34513-34520
54. Verghese, G. M., Gutknecht, M. F., and Caughey, G. H. (2006) Prostasin regulates epithelial monolayer function: cell-specific Gpld1-mediated secretion and functional role for GPI anchor. Am. J. Physiol. Cell Physiol. 291, C1258-1270
55. Hooper, J. D., Clements, J. A., Quigley, J. P., and Antalis, T. M. (2001) Type II transmembrane serine proteases. Insights into an emerging class of cell surface proteolytic enzymes. J. Biol. Chem. 276, 857-860
56. Shen, L., Su, L., and Turner, J. R. (2009) Mechanisms and functional implications of intestinal barrier defects. Dig. Dis. 27, 443-449
57. Turner, J. R. (2009) Intestinal mucosal barrier function in health and disease. Nat. Rev. Immunol. 9, 799-809
58. Henderson, P., van Limbergen, J. E., Schwarze, J., and Wilson, D. C. (2011) Function of the intestinal epithelium and its dysregulation in inflammatory bowel disease. Inflamm. Bowel. Dis. 17, 382-395