Hepatocyte growth factor activator inhibitor-1 (HAI-1) is essential for the integrity of basement membranes in the developing placental labyrinth

Developmental Biology

Volumn 303, Issue 1, 2007, Pages 222-230

  Fan, Bin ^a   Brennan, Jane ^a   Grant, Deanna ^a   Peale, Franklin ^a   Rangell, Linda ^a   Kirchhofer, Daniel ^a  

^a GENENTECH INC   (United States)

Author keywords

Basement membrane; HAI 1; Matriptase; OmniBank; Placental development; Prostasin; Serine protease

Indexed keywords

COLLAGEN TYPE 4; HEPATOCYTE GROWTH FACTOR ACTIVATOR INHIBITOR 1; HEPSIN; LAMININ; MATRIPTASE; PROSTASIN; PROTEINASE; SERINE PROTEINASE; SERINE PROTEINASE INHIBITOR; UNCLASSIFIED DRUG;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASEMENT MEMBRANE; CARCINOGENESIS; CELL SURFACE; CHORION VILLUS; CONTROLLED STUDY; ELECTRON MICROSCOPY; ENZYME LOCALIZATION; FETUS DEATH; FETUS MEMBRANE; GENE; GENE EXPRESSION; IMMUNOFLUORESCENCE TEST; MEMBRANE DAMAGE; MOUSE; NONHUMAN; PLACENTA CIRCULATION; PLACENTA DEVELOPMENT; PLACENTA DISORDER; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; TISSUE REGENERATION; TROPHOBLAST; VASCULARIZATION; WILD TYPE;

MUS;

EID: 33846917477     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2006.11.005     Document Type: Article

References (45)

1. Adachi M., Kitamura K., Miyoshi T., Narikiyo T., Iwashita K., Shiraishi N., Nonoguchi H., and Tomita K. Activation of epithelial sodium channels by prostasin in Xenopus oocytes. J. Am. Soc. Nephrol. 12 (2001) 1114-1121
2. Anson-Cartwright L., Dawson K., Holmyard D., Fisher S.J., Lazzarini R.A., and Cross J.C. The glial cells missing-1 protein is essential for branching morphogenesis in the chorioallantoic placenta. Nat. Genet. 25 (2000) 311-314
3. Benaud C., Dickson R.B., and Lin C.Y. Regulation of the activity of matriptase on epithelial cell surfaces by a blood-derived factor. Eur. J. Biochem. 268 (2001) 1439-1447
4. Birchmeier C., Birchmeier W., Gherardi E., and Vande Woude G.F. Met, metastasis, motility and more. Nat. Rev., Mol. Cell Biol. 4 (2003) 915-925
5. Chen L.M., and Chai K.X. Prostasin serine protease inhibits breast cancer invasiveness and is transcriptionally regulated by promoter DNA methylation. Int. J. Cancer 97 (2002) 323-329
6. Denda K., Shimomura T., Kawaguchi T., Miyazawa K., and Kitamura N. Functional characterization of Kunitz domains in hepatocyte growth factor activator inhibitor type 1. J. Biol. Chem. 277 (2002) 14053-14059
7. Fan B., Wu T.D., Li W., and Kirchhofer D. Identification of hepatocyte growth factor activator inhibitor-1B as a potential physiological inhibitor of prostasin. J. Biol. Chem. 280 (2005) 34513-34520
8. Hallmann R., Horn N., Selg M., Wendler O., Pausch F., and Sorokin L.M. Expression and function of laminins in the embryonic and mature vasculature. Physiol. Rev. 85 (2005) 979-1000
9. Herter S., Piper D.E., Aaron W., Gabriele T., Cutler G., Cao P., Bhatt A.S., Choe Y., Craik C.S., Walker N., Meininger D., Hoey T., and Austin R.J. Hepatocyte growth factor is a preferred in vitro substrate for human Hepsin, a membrane-anchored serine protease implicated in prostate and ovarian cancers. Biochem. J. 390 (2005) 125-136
10. Itoh H., Kataoka H., Tomita M., Hamasuna R., Nawa Y., Kitamura N., and Koono M. Upregulation of HGF activator inhibitor type 1 but not type 2 along with regeneration of intestinal mucosa. Am. J. Physiol.: Gastrointest. Liver Physiol. 278 (2000) G635-G643
11. Itoh H., Naganuma S., Takeda N., Miyata S., Uchinokura S., Fukushima T., Uchiyama S., Tanaka H., Nagaike K., Shimomura T., Miyazawa K., Yamada G., Kitamura N., Koono M., and Kataoka H. Regeneration of injured intestinal mucosa is impaired in hepatocyte growth factor activator-deficient mice. Gastroenterology 127 (2004) 1423-1435
12. Kataoka H., Hamasuna R., Itoh H., Kitamura N., and Koono M. Activation of hepatocyte growth factor/scatter factor in colorectal carcinoma. Cancer Res. 60 (2000) 6148-6159
13. Kataoka H., Shimomura T., Kawaguchi T., Hamasuna R., Itoh H., Kitamura N., Miyazawa K., and 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. 275 (2000) 40453-40462
14. Kirchhofer D., Peek M., Li W., Stamos J., Eigenbrot C., Kadkhodayan S., Elliott J.M., Corpuz R.T., Lazarus R.A., and Moran P. Tissue expression, protease specificity, and Kunitz domain functions of hepatocyte growth factor activator inhibitor-1B (HAI-1B), a new splice variant of HAI-1. J. Biol. Chem. 278 (2003) 36341-36349
15. Kirchhofer D., Peek M., Lipari M.T., Billeci K., Fan B., and 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. 579 (2005) 1945-1950
16. Klezovitch O., Chevillet J., Mirosevich J., Roberts R.L., Matusik R.J., and Vasioukhin V. Hepsin promotes prostate cancer progression and metastasis. Cancer Cell 6 (2004) 185-195
17. Lee S.L., Dickson R.B., and Lin C.Y. Activation of hepatocyte growth factor and urokinase/plasminogen activator by matriptase, an epithelial membrane serine protease. J. Biol. Chem. 275 (2000) 36720-36725
18. Leyvraz C., Charles R.P., Rubera I., Guitard M., Rotman S., Breiden B., Sandhoff K., and Hummler E. The epidermal barrier function is dependent on the serine protease CAP1/Prss8. J. Cell Biol. 170 (2005) 487-496
19. Lin C.Y., Anders J., Johnson M., and Dickson R.B. Purification and characterization of a complex containing matriptase and a Kunitz-type serine protease inhibitor from human milk. J. Biol. Chem. 274 (1999) 18237-18242
20. List K., Haudenschild C.C., Szabo R., Chen W., Wahl S.M., Swaim W., Engelholm L.H., Behrendt N., and Bugge T.H. Matriptase/MT-SP1 is required for postnatal survival, epidermal barrier function, hair follicle development, and thymic homeostasis. Oncogene 21 (2002) 3765-3779
21. List K., Szabo R., Wertz P.W., Segre J., Haudenschild C.C., Kim S.Y., and Bugge T.H. Loss of proteolytically processed filaggrin caused by epidermal deletion of Matriptase/MT-SP1. J. Cell Biol. 163 (2003) 901-910
22. List K., Szabo R., Molinolo A., Sriuranpong V., Redeye V., Murdock T., Burke B., Nielsen B.S., Gutkind J.S., and Bugge T.H. Deregulated matriptase causes ras-independent multistage carcinogenesis and promotes ras-mediated malignant transformation. Genes Dev. 19 (2005) 1934-1950
23. Magee J.A., Araki T., Patil S., Ehrig T., True L., Humphrey P.A., Catalona W.J., Watson M.A., and Milbrandt J. Expression profiling reveals hepsin overexpression in prostate cancer. Cancer Res. 61 (2001) 5692-5696
24. Millauer B., Wizigmann-Voos S., Schnurch H., Martinez R., Moller N.P., Risau W., and Ullrich A. High affinity VEGF binding and developmental expression suggest Flk-1 as a major regulator of vasculogenesis and angiogenesis. Cell 72 (1993) 835-846
25. Miner J.H., Cunningham J., and Sanes J.R. Roles for laminin in embryogenesis: exencephaly, syndactyly, and placentopathy in mice lacking the laminin alpha5 chain. J. Cell Biol. 143 (1998) 1713-1723
26. Miyata S., Uchinokura S., Fukushima T., Hamasuna R., Itoh H., Akiyama Y., Nakano S., Wakisaka S., and Kataoka H. Diverse roles of hepatocyte growth factor activator inhibitor type 1 (HAI-1) in the growth of glioblastoma cells in vivo. Cancer Lett. 227 (2005) 83-93
27. Miyazawa K., Shimomura T., Kitamura A., Kondo J., Morimoto Y., and 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. 268 (1993) 10024-10028
28. Morasso M.I., Grinberg A., Robinson G., Sargent T.D., and Mahon K.A. Placental failure in mice lacking the homeobox gene Dlx3. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 162-167
29. Nagaike K., Kohama K., Uchiyama S., Tanaka H., Chijiiwa K., Itoh H., and Kataoka H. Paradoxically enhanced immunoreactivity of hepatocyte growth factor activator inhibitor type 1 (HAI-1) in cancer cells at the invasion front. Cancer Sci. 95 (2004) 728-735
30. Oberst M.D., Johnson M.D., Dickson R.B., Lin C.Y., Singh B., Stewart M., Williams A., al-Nafussi A., Smyth J.F., Gabra H., and Sellar G.C. 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. 8 (2002) 1101-1107
31. Oberst M.D., Chen L.Y., Kiyomiya K.I., Williams C.A., Lee M.S., Johnson M.D., Dickson R.B., and Lin C.Y. Hepatocyte growth factor activator inhibitor 1 (HAI-1) regulates activation and expression of matriptase, a membrane-bound serine protease. Am. J. Physiol.: Cell Physiol. 289 (2005) C462-C470
32. Poschl E., Schlotzer-Schrehardt U., Brachvogel B., Saito K., Ninomiya Y., and Mayer U. Collagen IV is essential for basement membrane stability but dispensable for initiation of its assembly during early development. Development 131 (2004) 1619-1628
33. Qureshi F., Yang Y., Jaques S.M., Johnson M.P., Naparstek Y., Ulmansky R., and Schuger L. Anti-DNA antibodies cross-reacting with laminin inhibit trophoblast attachment and migration: implications for recurrent pregnancy loss in SLE patients. Am. J. Reprod. Immunol. 44 (2000) 136-142
34. Riddick A.C., Shukla C.J., Pennington C.J., Bass R., Nuttall R.K., Hogan A., Sethia K.K., Ellis V., Collins A.T., Maitland N.J., Ball R.Y., and Edwards D.R. Identification of degradome components associated with prostate cancer progression by expression analysis of human prostatic tissues. Br. J. Cancer 92 (2005) 2171-2180
35. Romagnano L., and Babiarz B. Mechanisms of murine trophoblast interaction with laminin. Biol. Reprod. 49 (1993) 374-380
36. Rossant J., and Cross J.C. Placental development: lessons from mouse mutants. Nat. Rev., Genet. 2 (2001) 538-548
37. Shia S., Stamos J., Kirchhofer D., Fan B., Wu J., Corpuz R.T., Santell L., Lazarus R.A., and Eigenbrot C. Conformational lability in serine protease active sites: structures of hepatocyte growth factor activator (HGFA) alone and with the inhibitory domain from HGFA inhibitor-1B. J. Mol. Biol. 346 (2005) 1335-1349
38. Shimamura K., Hirano S., McMahon A.P., and Takeichi M. Wnt-1-dependent regulation of local E-cadherin and alpha N-catenin expression in the embryonic mouse brain. Development 120 (1994) 2225-2234
39. Shimomura T., Denda K., Kitamura A., Kawaguchi T., Kito M., Kondo J., Kagaya S., Qin L., Takata H., Miyazawa K., and Kitamura N. Hepatocyte growth factor activator inhibitor, a novel Kunitz-type serine protease inhibitor. J. Biol. Chem. 272 (1997) 6370-6376
40. Takeuchi T., Shuman M.A., and Craik C.S. 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 (1999) 11054-11061
41. Takeuchi T., Harris J.L., Huang W., Yan K.W., Coughlin S.R., and Craik C.S. 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 (2000) 26333-26342
42. 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., and Kataoka H. Hepatocyte growth factor activator inhibitor type 1 (HAI-1) is required for branching morphogenesis in the chorioallantoic placenta. Mol. Cell. Biol. 25 (2005) 5687-5698
43. Timpl R., and Brown J.C. Supramolecular assembly of basement membranes. BioEssays 18 (1996) 123-132
44. Tong Z., Illek B., Bhagwandin V.J., Verghese G.M., and Caughey G.H. 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 (2004) L928-L935
45. Zambrowicz B.P., Abuin A., Ramirez-Solis R., Richter L.J., Piggott J., BeltrandelRio H., Buxton E.C., Edwards J., Finch R.A., Friddle C.J., Gupta A., Hansen G., Hu Y., Huang W., Jaing C., Key Jr. B.W., Kipp P., Kohlhauff B., Ma Z.Q., Markesich D., Payne R., Potter D.G., Qian N., Shaw J., Schrick J., Shi Z.Z., Sparks M.J., Van Sligtenhorst I., Vogel P., Walke W., Xu N., Zhu Q., Person C., and Sands A.T. Wnk1 kinase deficiency lowers blood pressure in mice: a gene-trap screen to identify potential targets for therapeutic intervention. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 14109-14114