Epithelial integrity is maintained by a matriptase-dependent proteolytic pathway

American Journal of Pathology

Volumn 175, Issue 4, 2009, Pages 1453-1463

  List, Karin ^a,b   Kosa, Peter ^a   Szabo, Roman ^a   Bey, Alexandra L ^b   Wang, Chao Becky ^a   Molinolo, Alfredo ^a   Bugge, Thomas H ^a  

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

^b WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MATRIPTASE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ENZYME ANALYSIS; EPITHELIUM; FEMALE; GENE DELETION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; TIGHT JUNCTION;

EID: 73549091040     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2009.090240     Document Type: Article

References (44)

1. Quesada V, Ordonez GR, Sanchez LM, Puente XS, Lopez-Otin C: The Degradome database: mammalian proteases and diseases of proteolysis. Nucleic Acid Res 2009, 37:D239-D243
2. López-Otin C, Bond JS: Proteases: multifunctional enzymes in life and disease. J Biol Chem 2008, 283:30433-30437
3. 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, 170:487-496
4. Chin AC, Lee WY, Nusrat A, Vergnolle N, Parkos CA: Neutrophilmediated activation of epithelial protease-activated receptors-1 and -2 regulates barrier function and transepithelial migration. J Immunol 2008, 181:5702-5710
5. Cohen E, Talmon A, Faff O, Bacher A, Ben-Shaul Y: Formation of tight junctions in epithelial cells. I. Induction by proteases in a human colon carcinoma cell line. Exp Cell Res 1985, 156:103-116
6. Scudamore CL, Jepson MA, Hirst BH, Miller HR: The rat mucosal mast cell chymase. RMCP-II, alters epithelial cell monolayer permeability in association with altered distribution of the tight junction proteins ZO-1 and occludin. Eur J Cell Biol 1998, 75:321-330
7. Wang MH, Skeel A, Leonard EJ: Proteolytic cleavage and activation of pro-macrophage-stimulating protein by resident peritoneal macrophage membrane proteases. J Clin Invest 1996, 97:720-727
8. Wang MH, Yoshimura T, Skeel A, Leonard EJ: Proteolytic conversion of single chain precursor macrophage-stimulating protein to a biologically active heterodimer by contact enzymes of the coagulation cascade. J Biol Chem 1994, 269:3436-3440
9. Bhatt AS, Welm A, Farady CJ, Vasquez M, Wilson K, Craik CS: Coordinate expression and functional profiling identify an extracellular proteolytic signaling pathway. Proc Natl Acad Sci USA 2007, 104:5771-5776
10. Shimomura T, Kondo J, Ochiai M, Naka D, Miyazawa K, Morimoto Y, Kitamura N: Activation of the zymogen of hepatocyte growth factor activator by thrombin. J Biol Chem 1993, 268:22927-22932
11. Naldini L, Tamagnone L, Vigna E, Sachs M, Hartmann G, Birchmeier W, Daikuhara Y, Tsubouchi H, Blasi F, Comoglio PM: Extracellular proteolytic cleavage by urokinase is required for activation of hepatocyte growth factor/scatter factor. EMBO J 1992, 11:4825-4833
12. Wang MH, Gonias SL, Skeel A, Wolf BB, Yoshimura T, Leonard EJ: Proteolytic activation of single-chain precursor macrophage-stimulating protein by nerve growth factor-γ and epidermal growth factorbinding protein, members of the kallikrein family. J Biol Chem 1994, 269:13806-13810
13. Mizuno K, Tanoue Y, Okano I, Harano T, Takada K, Nakamura T: Purification and characterization of hepatocyte growth factor (HGF)-converting enzyme: activation of pro-HGF. Biochem Biophys Res Commun 1994, 198:1161-1169
14. Lee SL, Dickson RB, Lin CY: Activation of hepatocyte growth factor and urokinase/plasminogen activator by matriptase, an epithelial membrane serine protease. J Biol Chem 2000, 275:36720-36725
15. Picard N, Eladari D, El Moghrabi S, Planes C, Bourgeois S, Houillier P, Wang Q, Burnier M, Deschenes G, Knepper MA, Meneton P, Chambrey R: Defective ENaC processing and function in tissue kallikrein-deficient mice. J Biol Chem 2008, 283:4602-4611
16. Carattino MD, Hughey RP, Kleyman TR: Proteolytic processing of the epithelial sodium channel γ subunit has a dominant role in channel activation. J Biol Chem 2008, 283:25290-25295
17. Myerburg MM, Butterworth MB, McKenna EE, Peters KW, Frizzell RA, Kleyman TR, Pilewski JM: Airway surface liquid volume regulates ENaC by altering the serine protease-protease inhibitor balance: a mechanism for sodium hyperabsorption in cystic fibrosis. J Biol Chem 2006, 281:27942-27949
18. Vallet V, Chraibi A, Gaeggeler HP, Horisberger JD, Rossier BC: An epithelial serine protease activates the amiloride-sensitive sodium channel. Nature 1997, 389:607-610
19. Shin K, Fogg VC, Margolis B: Tight junctions and cell polarity. Annu Rev Cell Dev Biol 2006, 22:207-235
20. Gecse K, Róka R, Ferrier L, Leveque M, Eutamene H, Cartier C, Ait-Belgnaoui A, Rosztóczy A, Izbéki F, Fioramonti J, Wittmann T, Bueno L: Increased faecal serine protease activity in diarrhoeic IBS patients: a colonic lumenal factor impairing colonic permeability and sensitivity. Gut 2008, 57:591-599
21. McDermott JR, Bartram RE, Knight PA, Miller HR, Garrod DR, Grencis RK: Mast cells disrupt epithelial barrier function during enteric nematode infection, Proc Natl Acad Sci USA 2003,100:7761-7766
22. List K, Bugge TH, Szabo R: Matriptase: potent proteolysis on the cell surface. Mol Med 2006, 12:1-7
23. 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, Shohat M: Autosomal recessive ichthyosis with hypotrichosis caused by a mutation in ST14. Encoding type II transmembrane serine protease matriptase. Am J Hum Genet 2007, 80:467-477
24. 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, 163:901-910
25. Alef T, Torres S, Hausser I, Metze D, Tursen U, Lestringant GG, Hennies HC: Ichthyosis, follicular atrophoderma, and hypotrichosis caused by mutations in ST14 is associated with impaired profilaggrin processing. J Invest Dermatol 2009, 129:862-869
26. List K, Hobson JP, Molinolo A, Bugge TH: Co-localization of the channel activating protease prostasin/(CAP1/PRSS8) with its candidate activator, matriptase. J Cell Physiol 2007, 213:237-245
27. Oberst MD, Singh B, Ozdemirli M, Dickson RB, Johnson MD, Lin CY: Characterization of matriptase expression in normal human tissues. J Histochem Cytochem 2003, 51:1017-1025
28. Hayashi S, McMahon AP: Efficient recombination in diverse tissues by a tamoxifen-inducible form of Cre: a tool for temporally regulated gene activation/inactivation in the mouse. Dev Biol 2002, 244:305-318
29. Wagner KU, McAllister K, Ward T, Davis B, Wiseman R, Hennighausen L: Spatial and temporal expression of the Cre gene under the control of the MMTV-LTR in different lines of transgenic mice. Transgenic Res 2001, 10:545-553
30. Madison BB, Dunbar L, Qiao XT, Braunstein K, Braunstein E, Gumucio DL: Cis elements of the villin gene control expression in restricted domains of the vertical (crypt) and horizontal (duodenum, cecum) axes of the intestine. J Biol Chem 2002, 277:33275-33283
31. Wang Q, Fang CH, Hasselgren PO: Intestinal permeability is reduced and IL-10 levels are increased in septic IL-6 knockout mice. Am J Physiol Regul Integr Comp Physiol 1994, 281:R1013-R1023
32. Chen Y, Merzdorf C, Paul DL, Goodenough DA: COOH terminus of occludin is required for tight junction barrier function in early Xenopus embryos. J Cell Biol 1997, 138:891-899
33. List K, Szabo R, Molinolo A, Sriuranpong V, Redeye V, Murdock T, Burke B, Nielsen BS, Gutkind JS, Bugge TH: Deregulated matriptase causes ras-independent multistage carcinogenesis and promotes ras-mediated malignant transformation. Genes Dev 2005, 19:1934-1950
34. Cliffe LJ, Humphreys NE, Lane TE, Potten CS, Booth C, Grencis RK: Accelerated intestinal epithelial cell turnover: a new mechanism of parasite expulsion. Science 2005, 308:1463-1465
35. 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 2006, 168:1513-1525
36. 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, 21:3765-3779
37. Furuse M, Hata M, Furuse K, Yoshida Y, Haratake A, Sugitani Y, Noda T, Kubo A, Tsukita S: Claudin-based tight junctions are crucial for the mammalian epidermal barrier: a lesson from claudin-1-deficient mice. J Cell Biol 2002, 156:1099-1111
38. 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, 22:237-258
39. Szabo R, Molinolo A, List K, Bugge TH: Matriptase inhibition by hepatocyte growth factor activator inhibitor-1 is essential for placental development. Oncogene 2007, 26:1546-1556
40. Segre JA: Epidermal barrier formation and recovery in skin disorders. J Clin Invest 2006, 116:1150-1158
41. 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, 281:32941-32945
42. Avrahami L, Maas S, Pasmanik-Chor M, Rainshtein L, Magal N, Smitt J, van Marle J, Shohat M, Basel-Vanagaite L: Autosomal recessive ichthyosis with hypotrichosis syndrome: further delineation of the phenotype. Clin Genet 2008, 74:47-53
43. 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, 282:36714-36723
44. Schuster V, Hugle B, Tefs K: Plasminogen deficiency. J Thromb Haemost 2007, 5:2315-2322