Increased matriptase zymogen activation in inflammatory skin disorders

American Journal of Physiology - Cell Physiology

Volumn 300, Issue 3, 2011, Pages

  Chen, Cheng Jueng ^a   Wu, Bai Yao ^a   Tsao, Pai In ^a   Chen, Chi Yung ^b   Wu, Mei Hsuan ^b   Chan, Yee Lam E ^b   Lee, Herng Sheng ^a   Johnson, Michael D ^c   Eckert, Richard L ^d   Chen, Ya Wen ^d,e   Chou, Fengpai ^d,e   Wang, Jehng Kang ^b   Lin, Chen Yong ^d,e  

^a TRI SERVICE GENERAL HOSPITAL   (Taiwan)

^b NATIONAL DEFENSE MEDICAL CENTER   (Taiwan)

^c GEORGETOWN UNIVERSITY   (United States)

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

^e UNIVERSITY OF MARYLAND   (United States)

Author keywords

Hepatocyte growth factor activator inhibitor 1; Protease

Indexed keywords

ENZYME PRECURSOR; HEPATOCYTE GROWTH FACTOR ACTIVATOR INHIBITOR 1; HYDROGEN PEROXIDE; MATRIPTASE; REACTIVE OXYGEN METABOLITE; SERINE PROTEINASE INHIBITOR; UNCLASSIFIED DRUG;

ACTINIC KERATOSIS; ARTICLE; CELL JUNCTION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DRUG ERUPTION; ECZEMA; EPIDERMIS; EPIDERMOID CYST; FOLLICULITIS; GRANULOMA; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; KELOID; KERATINOCYTE; LYMPHOMA; NATURAL KILLER CELL LYMPHOMA; NEVUS; OXIDATIVE STRESS; PARAKERATOSIS; PH; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; SEBORRHEIC KERATOSIS; SKIN INFLAMMATION; SKIN METASTASIS; VERRUCA VULGARIS;

CELL LINE, TRANSFORMED; DERMATITIS; DOWN-REGULATION; ENZYME ACTIVATION; EPIDERMIS; EPITHELIAL CELLS; HUMANS; INFLAMMATION MEDIATORS; INTERCELLULAR JUNCTIONS; KERATINOCYTES; PROTEINASE INHIBITORY PROTEINS, SECRETORY; SERINE ENDOPEPTIDASES; SERINE PROTEINASE INHIBITORS; UP-REGULATION;

EID: 79952146534     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00403.2010     Document Type: Article

References (45)

1. 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 129: 862-869, 2009.
2. 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 74: 47-53, 2008. (Pubitemid 351833818)
3. Basel-Vanagaite L, Attia R, Ishida-Yamamoto A, Rainshtein L, Ben AD, 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 80: 467-477, 2007.
4. Benaud C, Dickson RB, Lin CY. Regulation of the activity of matriptase on epithelial cell surfaces by a blood-derived factor. Eur J Biochem 268: 1439-1447, 2001. (Pubitemid 32231898)
5. Benaud C, Oberst M, Hobson JP, Spiegel S, Dickson RB, Lin CY. Sphingosine 1-phosphate, present in serum-derived lipoproteins, activates matriptase. J Biol Chem 277: 10539-10546, 2002. (Pubitemid 34968177)
6. Bocheva G, Rattenholl A, Kempkes C, Goerge T, Lin CY, D'Andrea MR, Stander S, Steinhoff M. Role of matriptase and proteinase-activated receptor-2 in nonmelanoma skin cancer. J Invest Dermatol 129: 1816-1823, 2009.
7. Chavanas S, Bodemer C, Rochat A, Hamel-Teillac D, Ali M, Irvine AD, Bonafe JL, Wilkinson J, Taieb A, Barrandon Y, Harper JI, de Prost Y, Hovnanian A. Mutations in SPINK5, encoding a serine protease inhibitor, cause Netherton syndrome. Nat Genet 25: 141-142, 2000. (Pubitemid 30394980)
8. Chen YW, Wang JK, Chou FP, Chen CY, Rorke EA, Chen LM, Chai KX, Eckert RL, Johnson MD, Lin CY. Regulation of the matriptase-prostasin cell surface proteolytic cascade by hepatocyte growth factor activator inhibitor-1 (HAI-1) during epidermal differentiation. J Biol Chem 285: 31755-31762, 2010.
9. Demerjian M, Hachem JP, Tschachler E, Denecker G, Declercq W, Vandenabeele P, Mauro T, Hupe M, Crumrine D, Roelandt T, Houben E, Elias PM, Feingold KR. Acute modulations in permeability barrier function regulate epidermal cornification: role of caspase-14 and the protease-activated receptor type 2. Am J Pathol 172: 86-97, 2008. (Pubitemid 351186371)
10. Denecker G, Hoste E, Gilbert B, Hochepied T, Ovaere P, Lippens S, Van den Broecke C, Van Damme P, D'Herde K, Hachem JP, Borgonie G, Presland RB, Schoonjans L, Libert C, Vandekerckhove J, Gevaert K, Vandenabeele P, Declercq W. Caspase-14 protects against epidermal UVB photodamage and water loss. Nat Cell Biol 9: 666-674, 2007. (Pubitemid 47214729)
11. Eckert RL. Structure, function, and differentiation of the keratinocyte. Physiol Rev 69: 1316-1346, 1989. (Pubitemid 19255839)
12. Egberts F, Heinrich M, Jensen JM, Winoto-Morbach S, Pfeiffer S, Wickel M, Schunck M, Steude J, Saftig P, Proksch E, Schutze S. Cathepsin D is involved in the regulation of transglutaminase 1 and epidermal differentiation. J Cell Sci 117: 2295-2307, 2004. (Pubitemid 38807497)
13. Elias PM, Friend DS, McNutt NS. Epidermal permeability barrier: transformation of lamellar granule-disks into intercellular sheets by a membrane fusion process. J Invest Dermatol 88: 459-460, 1987.
14. Fan B, Wu TD, Li W, Kirchhofer D. Identification of hepatocyte growth factor activator inhibitor-1B as a potential physiological inhibitor of prostasin. J Biol Chem 280: 34513-34520, 2005. (Pubitemid 41504581)
15. Fawcett DW. Intercellular bridges. Exp Cell Res Suppl 8: 174-187, 1961.
16. Hart TC, Hart PS, Bowden DW, Michalec MD, Callison SA, Walker SJ, Zhang Y, Firatli E. Mutations of the cathepsin C gene are responsible for Papillon-Lefevre syndrome. J Med Genet 36: 881-887, 1999. (Pubitemid 30003843)
17. Kamata Y, Taniguchi A, Yamamoto M, Nomura J, Ishihara K, Takahara H, Hibino T, Takeda A. Neutral cysteine protease bleomycin hydrolase is essential for the breakdown of deiminated filaggrin into amino acids. J Biol Chem 284: 12829-12836, 2009.
18. Kiyomiya KI, Lee MS, Tseng IC, Zuo H, Barndt RJ, Johnson MD, Dickson RB, Lin CY. Matriptase activation and subsequent shedding with HAI-1 is induced by steroid sex hormones in human prostate cancer cells, but not in breast cancer cells. Am J Physiol Cell Physiol 291: C40-C49, 2006.
19. Lee MS, Tseng IC, Wang Y, Kiyomiya K, Johnson MD, Dickson RB, Lin CY. Autoactivation of matriptase in vitro: requirement for biomembrane and LDL receptor domain. Am J Physiol Cell Physiol 293: C95-C105, 2007. (Pubitemid 47105046)
20. Lee MS, Kiyomiya K, Benaud C, Dickson RB, Lin CY. Simultaneous activation and HAI-1-mediated inhibition of matriptase induced at activation foci in immortal human mammary epithelial cells. Am J Physiol Cell Physiol 288: C932-C941, 2005. (Pubitemid 40395072)
21. 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 170: 487-496, 2005. (Pubitemid 41126947)
22. Lin CY, Anders J, Johnson M, Dickson RB. Purification and characterization of a complex containing matriptase and a Kunitz-type serine protease inhibitor from human milk. J Biol Chem 274: 18237-18242, 1999.
23. Lin CY, Tseng IC, Chou FP, Su SF, Chen YW, Johnson MD, Dickson RB. Zymogen activation, inhibition, and ectodomain shedding of matriptase. Front Biosci 13: 621-635, 2008. (Pubitemid 351599772)
24. 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 21: 3765-3779, 2002. (Pubitemid 34620539)
25. 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 213: 237-245, 2007. (Pubitemid 47378812)
26. List K, Kosa P, Szabo R, Bey AL, Wang CB, Molinolo A, Bugge TH. Epithelial integrity is maintained by a matriptase-dependent proteolytic pathway. Am J Pathol 175: 1453-1463, 2009.
27. 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 163: 901-910, 2003. (Pubitemid 37517896)
28. 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 173: 1464-1475, 2008.
29. 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 281: 32941-32945, 2006. (Pubitemid 46036678)
30. Oberst MD, Singh B, Ossandon M, Dickson RB, Johnson MD, Lin CY. Characterization of matriptase expression in normal human tissues. J Histochem Cytochem 51: 1017-1025, 2003. (Pubitemid 36919979)
31. 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 278: 26773-26779, 2003. (Pubitemid 36876825)
32. Ovaere P, Lippens S, Vandenabeele P, Declercq W. The emerging roles of serine protease cascades in the epidermis. Trends Biochem Sci 34: 453-463, 2009.
33. Press AG, Hauptmann IA, Hauptmann L, Fuchs B, Fuchs M, Ewe K, Ramadori G. Gastrointestinal pH profiles in patients with inflammatory bowel disease. Aliment Pharmacol Ther 12: 673-678, 1998. (Pubitemid 28327965)
34. Rahman I, Macnee W. Oxidant/antioxidant imbalance in smokers and chronic obstructive pulmonary disease. Thorax 51: 348-350, 1996. (Pubitemid 26140195)
35. Rahman I, Morrison D, Donaldson K, Macnee W. Systemic oxidative stress in asthma, COPD, and smokers. Am J Respir Crit Care Med 154: 1055-1060, 1996.
36. Resing KA, Thulin C, Whiting K, al-Alawi N, Mostad S. Characterization of profilaggrin endoproteinase 1. A regulated cytoplasmic endoproteinase of epidermis. J Biol Chem 270: 28193-28198, 1995.
37. Roth W, Deussing J, Botchkarev VA, Pauly-Evers M, Saftig P, Hafner A, Schmidt P, Schmahl W, Scherer J, Anton-Lamprecht I, Von Figura K, Paus R, Peters C. Cathepsin L deficiency as molecular defect of furless: hyperproliferation of keratinocytes and perturbation of hair follicle cycling. FASEB J 14: 2075-2086, 2000.
38. Szabo R, Kosa P, List K, Bugge TH. Loss of matriptase suppression underlies spint1 mutation-associated ichthyosis and postnatal lethality. Am J Pathol 174: 2015-2022, 2009.
39. Toomes C, James J, Wood AJ, Wu CL, McCormick D, Lench N, Hewitt C, Moynihan L, Roberts E, Woods CG, Markham A, Wong M, Widmer R, Ghaffar KA, Pemberton M, Hussein IR, Temtamy SA, Davies R, Read AP, Sloan P, Dixon MJ, Thakker NS. Loss-of-function mutations in the cathepsin C gene result in periodontal disease and palmoplantar keratosis. Nat Genet 23: 421-424, 1999.
40. Tseng IC, Chou FP, Su SF, Oberst M, Madayiputhiya N, Lee MS, Wang JK, Sloane DE, Johnson M, Lin CY. 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, 2008. (Pubitemid 352755786)
41. Tseng IC, Xu H, Chou FP, Li G, Vazzano AP, Kao JP, Johnson MD, Lin CY. Matriptase activation, an early cellular response to acidosis. J Biol Chem 285: 3261-3270, 2010.
42. Wang JK, Lee MS, Tseng IC, Chou FP, Chen YW, Fulton A, Lee HS, Chen CJ, Johnson MD, Lin CY. Polarized epithelial cells secrete matriptase as a consequence of zymogen activation and HAI-1-mediated inhibition. Am J Physiol Cell Physiol 297: C459-C470, 2009.
43. Zeeuwen PL. Epidermal differentiation: the role of proteases and their inhibitors. Eur J Cell Biol 83: 761-773, 2004. (Pubitemid 40123840)
44. Zeeuwen PL, van Vlijmen-Willems IM, Hendriks W, Merkx GF, Schalkwijk J. A null mutation in the cystatin M/E gene of ichq mice causes juvenile lethality and defects in epidermal cornification. Hum Mol Genet 11: 2867-2875, 2002.
45. Zeeuwen PL, van Vlijmen-Willems IM, Olthuis D, Johansen HT, Hitomi K, Hara-Nishimura I, Powers JC, James KE, op den Camp HJ, Lemmens R, Schalkwijk J. Evidence that unrestricted legumain activity is involved in disturbed epidermal cornification in cystatin M/E deficient mice. Hum Mol Genet 13: 1069-1079, 2004. (Pubitemid 38702193)