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

American Journal of Pathology

Volumn 173, Issue 5, 2008, Pages 1464-1475

  Nagaike, Koki ^a   Kawaguchi, Makiko ^a   Takeda, Naoki ^b   Fukushima, Tsuyoshi ^a   Sawaguchi, Akira ^a   Kohama, Kazuyo ^a   Setoyama, Mitsuru ^a   Kataoka, Hiroaki ^a  

^a UNIVERSITY OF MIYAZAKI   (Japan)

^b KUMAMOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

APROTININ; FILAGGRIN; PROFILAGGRIN; PROTEIN KINASE B; SCATTER FACTOR RECEPTOR; SERINE PROTEINASE INHIBITOR;

ACANTHOSIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLASTOCYST; CHIMERA; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; EMBRYOTOXICITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; EPIDERMIS; FEMALE; GENE DELETION; GROWTH RETARDATION; HAIR GROWTH; ICHTHYOSIS; IMMUNOBLOTTING; KERATINIZATION; KNOCKOUT MOUSE; LETHALITY; MALE; MOUSE; NEWBORN; NONHUMAN; PHENOTYPE; PLACENTA; PLACENTA DISORDER; PLACENTA FUNCTION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; TISSUE DIFFERENTIATION; XERODERMA;

EID: 55349099521     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2008.071142     Document Type: Article

References (42)

1. Shimomura T, Denda K, Kitamura A, Kawaguchi T, Kito M, Kondo J, Kagaya S, Qin L, Takata H, Miyazawa K, Kitamura K: Hepatocyte growth factor activator inhibitor, a novel Kunitz-type serine protease inhibitor. J Biol Chem 1997, 272:6370-6376
2. Kataoka H, Miyata S, Uchinokura S, Itoh H: Roles of hepatocyte growth factor (HGF) activator and HGF activator inhibitor in the pericellular activation of HGF/scatter factor. Cancer Metastasis Rev 2003, 22:223-236
3. Kataoka H, Suganuma T, Shimomura T, Itoh H, Kitamura N, Nabeshima K, Koono M: Distribution of hepatocyte growth factor activator inhibitor type 1 (HAI-1) in human tissues: cellular surface localization of HAI-1 in simple columnar epithelium and its modulated expression in injured and regenerative tissues. J Histochem Cytochem 1999, 47:673-682
4. Oberst M, Anders J, Xie B, Singh B, Ossandon M, Johnson M, Dickson RB, Lin CY: Matriptase and HAI-1 are expressed by normal and malignant epithelial cells in vitro and in vivo. Am J Pathol 2001, 158:1301-1311
5. Kataoka H, Meng JY, Itoh H, Hamasuna R, Shimomura T, Suganuma T, Koono M: Localization of hepatocyte growth factor activator inhibitor type 1 in Langhans' cells of human placenta. Histochem Cell Biol 2000, 114:469-475
6. Akiyama Y, Nagai M, Komaki W, Marutsuka K, Asada Y, Kataoka H: Expression of hepatocyte growth factor activator inhibitor type 1 in endothelial cells. Human Cell 2006, 19:91-97
7. Kataoka H, Shimomura T, Kawaguchi T, Hamasuna R, Itoh H, Kitamura N, Miyazawa K, Koono M: Hepatocyte growth factor activator inhibitor type 1 is a specific cell surface binding protein of hepatocyte growth factor activator (HGFA) and regulates HGFA activity in the pericellular microenvironment. J Biol Chem 2000, 275:40453-40462
8. Oberst MD, Chen LY, Kiyomiya KI, Williams CA, Lee MS, Johnson MD, Dickson RB, Lin CY: Hepatocyte growth factor activator inhibitor 1 (HAI-1) regulates activation and expression of matriptase, a membrane-bound serine protease. Am J Physiol 2005, 289:C462-C470
9. List K, Bugge TH, Szabo R: Matriptase: potent proteolysis on the cell surface. Mol Med 2006, 12:1-7
10. 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, 25:5687-5698
11. Denda K, Shimomura T, Kawaguchi T, Miyazawa K, Kitamura N: Functional characterization of Kunitz domains in hepatocyte growth factor activator inhibitor type 1. J Biol Chem 2002, 277:14053-14059
12. 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 1999, 274:18237-18242
13. 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 2005, 280:34513-34520
14. Kirchhofer D, Peek M, Lipari MT, Billeci K, Fan B, Moran P: Hepsin activates pro-hepatocyte growth factor and is inhibited by hepatocyte growth factor activator inhibitor-1B (HAI-1B) and HAI-2. FEBS Lett 2005, 579:1945-1950
15. Miyazawa K, Shimomura T, Kitamura A, Kondo J, Morimoto Y, Kitamura N: Molecular cloning and sequence analysis of the cDNA for a human serine protease responsible for activation of hepatocyte growth factor. Structural similarity of the protease precursor to blood coagulation factor XII. J Biol Chem 1993, 268:10024-10028
16. 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
17. 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
18. 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
19. 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
20. 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
21. Oberst MD, Johnson MD, Dickson RB, Lin CY, Singh B, Stewart M, Williams A, al-Nafussi A, Smyth JF, Gabra H, Sellar GC: Expression of the serine protease matriptase and its inhibitor HAI-1 in epithelial ovarian cancer: correlation with clinical outcome and tumor clinicopathological parameters. Clin Cancer Res 2002, 8:1101-1107
22. Klezovitch O, Chevillet J, Mirosevich J, Roberts RL, Matusik RJ, Vasioukhin V: Hepsin promotes prostate cancer progression and metastasis. Cancer Cell 2004, 6:185-195
23. Betsunoh H, Mukai S, Akiyama Y, Fukushima T, Minamiguchi N, Hasui Y, Osada Y, Kataoka H: Clinical relevance of hepsin and hepatocyte growth factor activator inhibitor type 2 expression in renal cell carcinoma. Cancer Sci 2007, 98:491-498
24. 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
25. Fan B, Brennan J, Grant D, Peale F, Rangell L, Kirchhofer D: Hepatocyte growth factor activator inhibitor-1 (HAI-1) is essential for the integrity of basement membranes in the developing placental labyrinth. Dev Biol 2007, 303:222-230
26. Nagaike K, Kohama K, Uchiyama S, Tanaka H, Chijiiwa K, Itoh H, Kataoka H: Paradoxically enhanced immunoreactivity of hepatocyte growth factor activator inhibitor type 1 (HAI-1) in cancer cells at the invasion front. Cancer Sci 2004, 95:728-735
27. Hager B, Bickenbach JR, Fleckman P: Long-term culture of murine epidermal keratinocytes. J Invest Dermatol 1999, 112:971-976
28. 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
29. 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
30. 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
31. Tam PPL, Rossant J: Mouse embryonic chimeras: tools for studying mammalian development. Development 2003, 130:6155-6163
32. Carney TJ, von der Hardt S, Sonntag C, Amsterdam A, Topczewski J, Hopkins N, Hammerschmidt M: Inactivation of serine protease matriptase 1a by its inhibitor Hai1 is required for epithelial integrity of the zebrafish epidermis. Development 2007, 134:3461-3471
33. Mathias JR, Dodd ME, Walters KB, Rhodes J, Kanki JP, Look AT, Huttenlocher A: Live imaging of chronic inflammation caused by mutation of zebrafish Hai1. J Cell Sci 2007, 120:3372-3383
34. 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
35. 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
36. Lee MS, Tseng IC, Wang Y, Kiyomiya KI, Johnson MD, Dickson RB, Lin CY: Autoactivation of matriptase in vitro: requirement for biomembrane and LDL receptor domain. Am J Physiol 2007, 293:C95-C105
37. Zeeuwen PLJM: Epidermal differentiation: the role of proteases and their inhibitors. Eur J Cell Biol 2004, 83:761-773
38. -/- mice. Genes Dev 2004, 18:2354-2358
39. Descargues P, Deraison C, Bonnart C, Kreft M, Kishibe M, Ishida-Yamamoto A, Elias P, Barrandon Y, Zambruno G, Sonnenberg A, Hovnanian A: Spink5-deficient mice mimic Netherton syndrome through degradation of desmoglein 1 by epidermal protease hyperactivity. Nat Genet 2005, 37:56-65
40. Fresno Vara JA, Casado E, de Castro J, Cejas P, Belda-Iniesta C, Gonzälez-Barön M: PI3K/Akt signalling pathway and cancer. Cancer Treat Rev 2004, 30:193-204
41. Suzuki A, Itami S, Ohishi M, Hamada K, Inoue T, Komazawa N, Senoo H, Sasaki T, Takeda J, Manabe M, Mak TW, Nakano T: Keratinocyte-specific Pten deficiency results in epidermal hyperplasia, accelerated hair follicle morphogenesis and tumor formation. Cancer Res 2003, 63:674-681
42. Wakabayashi N, Itoh K, Wakabayashi J, Motohashi H, Noda S, Takahashi S, Imakado S, Kotsuji T, Otsuka F, Roop DR, Harada T, Engel JD, Yamamoto M: Keap1-null mutation leads to postnatal lethality due to constitutive Nrf2 activation. Nat Genet 2003, 35:238-245