Roles of kringle domain-containing serine proteases in epithelial-mesenchymal transitions during embryonic development

Cells Tissues Organs

Volumn 156, Issue 3, 1996, Pages 162-172

  Thery C ^a   Stern, C D ^a  

^a College of Physicians and Surgeons of Columbia University ^*  (United States)

Author keywords

Epithelial mesenchymal transitions; Hepatocyte growth factor scatter factor; HGF like macrophage stirnulating protein; Kringle domains; Plasminogen; Plasminogen activators; Proteases; Tyrosine kinase receptors

Indexed keywords

PLASMINOGEN; PLASMINOGEN ACTIVATOR; PROTEINASE; SCATTER FACTOR; TYROSINE KINASE RECEPTOR;

EMBRYO; EMBRYO DEVELOPMENT; EPITHELIUM; KRINGLE DOMAIN; MESENCHYME; NONHUMAN; PRIORITY JOURNAL; REVIEW;

ANIMALS; EMBRYONIC AND FETAL DEVELOPMENT; EPITHELIUM; HEPATOCYTE GROWTH FACTOR; HUMANS; KRINGLES; MESODERM; RECEPTOR PROTEIN-TYROSINE KINASES; SERINE ENDOPEPTIDASES;

EID: 0030450542     PISSN: 14226405     EISSN: 14226421     Source Type: Journal    
DOI: 10.1159/000147844     Document Type: Article

References (98)

1. Andennarcher, H., M.A. Surani, E. Gherardi (submitted) Distinct patterns of expression of die IIGF/SF and e-mct genes during early and late mouse embryogenesis.
2. Axelrod. H R. (1985) Altered troplioblast functions in implantation-defective mouse embryos. Dev Biol 108; 185-190.
3. Bar-Shavit, R., A. Kahn, G. Wilner, J.L. Fenton (1983) Monocyte chemotaxis; stimulation by specific exositc region in thrombin. Science 220; 728-731.
4. Bellusci, S., G. Moens, G. Gaudino, P. Comoglio, T. Nakamura, J.-P. Thiery, J. Jouanneau (1994) Creation of an hepatocyte growth factor/ scatter factor autocrine loop in carcinoma cells induces invasive properties associated with increased tuntorigenicity. Oncogene 9; 1091-1099.
5. Bezerra, J.A., S. Han, M.J.S. Damon, S.J.F. Degcn (1993) Are hepatocyte growth factor-like protein and macrophage stimulating protein the same protein? Protein Sci 2;666-668.
6. Blasi, F. (1993) Urokinase anil urokinase receptor; A paracrine/autocrine system regulating cell migration and invasiveness. BioEssays 15; 105-111.
7. Bottaro, D.P., J.S. Rubin, D.L. Faletto, A.M.-L. Chan, T.E. Kmiecick, G.F. Vatule Woude, S.A. Aaronson (1991) Identification of the hepatocyte growth factor receptor as the c-met protooncogene product. Science 251;802-804.
8. Blatter, P.R., J.A. Yce (1993) Cranial neural crest cells synthesize and secrete a latent form of transforming growth factor β that can be activated bv neural crest cell proteolvsis. Dev Biol 155;281-285.
9. Bu, G., S. Williams, D.K. Strickland, A.L. Schwartz (1992) Identification and partial characterization by chemical cross-linking of a binding protein for tissue-type plasminogen activator on rat hepatoma cells. J Biol Client 267; 15595-15602.
10. Basso, N., S.K. Masur, D. Lazega, S. Waxmun, L. Ossowski (1994) Induction of cell migration by pro-urokinase binding to its receptor; Possible mechanism for signal transduction in human epithelial cells. J Cell Biol 126;259-270.
11. Bussolino, F., M.F. Di Renzo, M. Ziclte, E. Boc-chietto, M. Olivero, L. Naldini, G. Gaudino, L. Tamagnonc, A. Coffer, P.M. Comoglio (1992) Hepatocyte growth factor is a potent angiogenic factor which stimulates endothelial cell motility and growth. J Cell Biol 119;629-641.
12. Carroll, P.M., W.G. Richards, A.L. Darrow, J.M. Wells, S. Strickland (1993) Preimplantation mouse embryos express a cell surface receptor for tissue-plasminogen activator. Development 119; 191-198.
13. Chen, L., J. Buchanan (1975) Mitogenic activity of blood components; Thrombin and prothrombin. Proc Nall Acad Sci USA 72. 1321-1325.
14. Clark, P. (1994) Modulation of scatter lactor/hepa-locyte growth factor activity by cell substratum adhesion. J Cell Sci 107; 1265-1275.
15. Cohn, M.J., J.-C. lzpisua-Belmonte, C. Tickle (1995) FGF2 application can induce additional limb formation from the Hank of the chick embryo. Cell 80; 739-746.
16. Cool, DE., C.-J.S. Edgell, G.V. Louie, M.J. Zoller, G.D. Brayer, R.T.A. MacGillivray (1985)Char-acterization of human blood coagulation factor XII cDNA; Prediction of the primary structure of factor XII and the tertiary structure of 13-factor XIla. J Biol Chcm 260; 13666-13676.
17. Degen, S.J.F., E.W. Davie (1987) Nucleotide sequence of the gene for human prothrombin. Biochemistry 26. 6165-6177.
18. Degen, S.J.F., L.A. Sluart, S. Han, C.S. Jamison (1991) Characterization of the mouse cDNA and gene coding for a hcpalocytc growth factor-like protein; Expression during development. Biochemistry 30; 9781-9791.
19. Delannct, M., J.-L. Duband (1992) Transforming growth factor p control of cell-substratum adhesion during avian neural crest cell emigration in vitro. Development 116;275-287.
20. Del Rosso, M., E. Anichini, N. Pedersen, F. Blasi, G. Fibbi, M. Pucci, M. Ruggiero (1993) Urokinase-urokinase receptor interaction; Nonmito-genic signal transduction in human epidermal cells. Biochem Biophys Res Commun 190; 347-352.
21. Duband, J.-L., F. Monicr, M. Delannet, D. New-green (1995) Epithelium-mesenchyme transition during neural crest development. Acta Anat 154;63-78.
22. Erickson, C.A., R.R. Isscrroff (1989) Plasminogen activator activity is associated with neural crest cell motility in tissue culture. J Exp Zool 251; 123-133.
23. Fazleabas, A.T., R.D. Geisert, P.W. Bazer, R.M. Roberts (1983) Relationship between release of plasminogen activator and estrogen by blastocysts and secretion of plasmin inhibitor by uterine endometrium in the pregnant pig. Biol Reprod 29; 225-238.
24. Fibbi, G., M. Hidle, L. Morbidelli, L. Magnelli, M. Del Rosso (1988) Interaction of urokinase w ith specific receptors stimulates mobilization of bovine adrenal capillary endothelial cells. Exp Cell Res 179;385-395.
25. Finlay, T.H., J. Katz, L. Kirsch, M. Levitz, S.A. Nathoo, S. Seiler (1983) Estrogen-stimulated uptake of plasminogen by the mouse uterus. Endocrinology 112; 856-861.
26. Galimi, F., M.F. Brizzi, P.M. Comoglio (1993) The hcpalocytc growth factor and its receptor. Stem Cell 11; 22-30.
27. Gaudino, G., A. Follenzi, L. Naldini, C. Collesi, M. Santoro, K.A. Gallo, P.J. Godowski, P.M. Comoglio (1994) Ron is a hctcrodimcric tyrosine kinase receptor activated by the HGF Itomo-loguc MSP. EMBO J 15;3524-3532.
28. Giordano, S., Z. Then, E. Medico, G. Gaudino, F. Galimi, P.M. Comoglio (1993) Transfer of mo-togenic and invasive response to scatter fac-tor/hepatocyte growth factor by transfection of human MET protooncogcne. Proc Natl Acad Sei USA 90; 649-653.
29. Grant, D.S., H.K. Kleinman, I.D. Goldberg, M.M. Bhargava, B.J. Nickoloff, J.L. Kinsella, P. Polvcrini, E.M. Rosen (1993) Scatter factor induces blood vessel formation in vivo. Proc Natl Acad Sci USA 90; 1937-1941.
30. Gudcwicz, P.W., N. Gilboa (1987) Human urokinase-type plasminogen activator stimulates chemotaxis of human neutrophils. Biochem Biophys Res Commun 147; 1176-1181
31. Hajjar, K.A. (1991) The endothelial cell tissue plasminogen activator. J Biol Chem 266; 21962-21970.
32. Han, S., L.A. Stuart, S.J.F. Degen (1991) Characterization of the DNFI582 locus on human chromosome 3; Identification of a gene coding for four kringle domains with homology to hepatocyte growth factor. Biochemistry 50; 9768-9780.
33. Hay, E.D. (1995) An overview of cpithelio-mesenchymal transformation. Acta Anat 154 8-20.
34. Huff, J., M.A. Jelinek, C.A. Borgman, T.J. Lansing, J.T. Parsons (1993) The protoncogenc c-sett encodes a transmembrane receptor protein tyrosine kinase related to the Met/hcpatocyte growth faetor/scatter factor receptor. Proc Natl Acad Sci USA 90;6140-6144.
35. Jamison, C.S., S.J.F. Degen (1991) Prenatal and postnatal expression of mRNA coding for rat prothrombin. Biochim Biophys Acta 1088; 208-216.
36. Karp, S.L., A. Ortiz, Arduan, S. Li, E.G. Neilson (1994) Epithelial differentiation of metaneph-ric mesenchymal cells after stimulation with hepatocyte growth factor or embryonic spinal cord. Proc Natl Acad Sci USA 91;5286-5290.
37. Kryslosek, A., N.W. Seeds (1981) Plasminogen activator secretion by granule neurons in cultures of developing cerebellum. Proc Natl Acad Sci USA 700; 7810-7814.
38. Kuho, H., A. Spindle, R.A. Pedersen (1981) Inhibition of mouse blastocyst attachment and outgrowth by protease inhibitors. J Exp Zool 2/6; 445-451.
39. Leonard, E.J., A. Skcel (1976) A serum protein that stimulates macrophage movement, chemotaxis and spreading. Exp Ceil Res 102; 434-138.
40. Littlefield, B.A. (1991) Plasminogen activators in endometrial physiology and embryo implantation; A review. Ann NY Acad Sci 622; 167-175.
41. Lyons, R.M., L.E. Gentry, A.F. Purchio, HL. Moses (1990) Mechanism of activation of la-lent recombinant transforming growth factor βl by plasmin. J Cell Biol 110; 1361-1367.
42. Markwald, R.R., T.P. Fitzharris, F.J. Manasek (1977) Structural analysis of endocardial cushion development. Am J Anal 148; 85-120.
43. Malsumoto, K., K. Hashimoto, K. Yoshikawa, T. Nakamura (1991) Marked stimulation of growth and motility of human keratinocytes by hepatocyte growth factor. Exp Cell Res 199; 114-120.
44. McGuire, P.G., S.M. Alexander (1993) Inhibition of urokinase synthesis and cell surface binding alters the motile behavior of embryonic endocardial-derived mesenchymal cells in vitro. Development 118;931-939.
45. McGuire, P.G., N.W. Seeds (1990) Degradation of underlying extracellular matrix by sensory neurons during neurite outgrowth. Neuron 4; 633-642.
46. McLean, J.W., J.E. Tomlinson, W.-J. Kuang, D.L. Eaton, E.Y. Chen, G.M. Fless, A.M. Scanu, R.M. Lawn (1987) cDNA sequence of human apolipoprotein(a) is homologous to plasminogen. Nature 380; 132-137.
47. McNamara, C., I. Sarembok, I. Gimplc, J.W. Fenton II, S.R. Coughlin, G. Owens (1992) Thrombin stimulation of smooth muscle cell proliferation is mediated by a proteolytic receptor-mediated mechanism. J Clin Invest 91; 94-98.
48. Menoud, P.A., S. Debrot, J. Schowing (1989) Mouse neural crest cells secrete both urokinase-type and tissue-type plasminogen activators in vitro. Development 109;685-690.
49. Miles, L.A., C.M. Dahlbcrg, J. Plescia, J. Fclcz, K. Kato, F. Plow (1991) Role of cell-surface lysines in plasminogen binding to cells; Identification of alpha-enolase as a candidate plasminogen receptor. Biochemistry 30; 1682-1691.
50. Miyazawa, K., T. Shimomura, A. Kitamura, J. Kondo, Y. Morimoto, N. Kitamura (1993) Molecular cloning and sequence analysis of the cDNA fora human serine protease responsible for activation of hepatocyte growth factor; Structural similarity of the protease precursor to blood coagulation factor XII. J Biol Client 298;10024-10028.
51. Montesano, R., K. Matsumoto, T. Nakamura, L. Orei (1991) Identification of a fibroblast-derived epithelial morphogen as hepatocyte growth factor. Cell 67;901-908.
52. Naidu, Y.M., E.M. Rosen, R. Zitnick, I. Goldberg, M. Park, M. Naujokas, P.J. Polvcrini, B.J. Nickoloff (1994) Role of scatter factor in the pathogenesis of AIDS-related Kaposi sarcoma. Proc Natl Acad Sci USA 91;5281-5285.
53. Nakamura, T., K. Nawa, A. Ichihara (1984) Partial purification and characterization of a hepatocyte growth factor from serum of hepatec-tomized rat. Biochem Biophys Res Commun 122;1450-1459.
54. Nakamura, T., T. Nishizawa, M. Hagiya, T. Seki, M. Shimonishi, A. Sugimara, K. Tashiro, S. Shimizu (1989) Molecular cloning and expression of human hepatocyte growth factor. Nature 342;440-443.
55. Naldini, I., E. Vigna, R.P. Narsimhan, G. Gaudino, R. Zamegar, G.K. Michalopoulos, P.M. Comoglio (1991a) Hepatocyte growth factor (HGF) stimulates the tyrosine kinase activity of the receptor encoded by the proto-oncogene c-met. Oncogene 6;501-504.
56. Naldini, L., K.M. Weidner, E. Vigna, G. Gaudino, A. Bardelli, C. Ponzetto, R.P. Narsimhan, G. Hartmann, R. Zamegar, G.K. Michalopoulos, W. Birchmeier, P. Comoglio (1991b) Scatter factor and hepatocyte growth factor are indistinguishable ligands for the MET receptor. EMBO J 10;2867-2878.
57. Novokhatny, V.V., S.A. Kudinov, P.L. Privalov (1984) Domains in human plasminogen. J Mol Biol 179;215-232.
58. Ny, T., F. Elgh, B. Lund (1984) The structure of the human tissue-type plasminogen activator gene; correlation of intron and exon structures to functional and structural domains. Proc Nall Acad Sci USA 81;5355-5359.
59. Pepper, M.S., K. Matsumoto, T. Nakamura, L. Orci, R. Montesano (1992) Hepatocyte growth factor increases urokinase-type plasminogen activator (u-PA) and u-PA receptor expression in Madin-Darby canine kidney epithelial cells. J Biol Chem 297;20493-20496.
60. Plow, E.F., D.E. Freaney, J. Plescia, L.A. Miles (1986) The plasminogen system and cell surfaces; Evidence for plasminogen and urokinase receptors on the same cell type. J Cell Biol 103; 1411-1420.
61. Potts, J.D, J.M. Dagle, J.A. Wakler, D.L. Weeks, R.B. Runyan (1991) Epithelial-mesenchymal transformation of embryonic cardiac endothelial cells is inhibited by a modified antisense oligodeosynucleotide to transforming growth factor 53 Proc Natl Acad Sci USA 88; 1516-1520.
62. Quigley, J.P., L. Gold, R. Schwimmcr, I. Sullivan (1987) Limited cleavage of cellular fibronectin by plasminogen activator purified from transformed cells. Proc Nall Acad Sci USA 84; 2776-2780.
63. Riddle, R.D., R.I. Johnson, E. Lauler, CJ. Tabin (1993) Sonic hedgehog mediates the polarizing activity of the ZPA. Cell 75- 1401-1418.
64. Roelink, H., A. Augsburgcr, J. Heemskerk, V. Korzh, S. Norlin, A. Ruiz i Altaba, Y. Tanabe, M. Placzck, T. Edlund, T.M. Jessell, T. Dodd (1994) Floor plate and motor neuron induction by vhh-1, a vertebrate homologue of hedgehog expressed by the notochord. Cell 76; 761-775.
65. Rogers, S.L., P.J. Gegick, S.M. Alexander, P.G. McGuire (1992) Transforming growth factor-β alters differentiation in cultures of avian neural crest-derived cells; Effects on cell morphology. proliferation, fibronectin expression, and melanogencsis. Dev Biol 151; 192- 203.
66. Roldan, A.L., M.V. Cubellis, M.T. Masucci, N. Behrendt, L.R. Lund, K. Dancv, E. Appelhi, F. Blasi (1990) Cloning ¡ind expression of the receptor for human urokinase plasminogen activator, a central molecule in cell surface, plasmin dependent proteolysis, F.MBO J 9; 467-474.
67. Rong, S., S. Segal, M. Anver, J.H. Resau, G.F. Vatule Woude (1994) Invasiveness and metastasis of Nil I 3T3 cells induced by Mel-hepalo-cyte growth factor/scatter factor autocrine stimulation. Proc Natl Acad Sci USA 91; 4731-4735.
68. Russell, W.E., J.A. McGowan, N.R.L. Bucher (1984) Partial characterization of a hepatocyte growth factor from rat platelets. J Cell Physiol 119; 183-192.
69. Sanders, E.J., S. Prasad (1989) Evidence that plasminogen activator is not involved in basement membrane penetration at avian gastrulation. Exp Cell Res 185;394-398.
70. Santos, O.F.P., E.J.G. Barros, X.-M. Yang, K. Mal-sumoto, T. Nakamura, M. Park, S.K. Nigam (1994) Involvement of hepatocyte growth factor in kidney development. Dev Biol 163; 525-529.
71. Santos, O.F.P., S.K. Nigam (1993) HGF-induced tubulogcnesis and branching of epithelial cells is modulated by extracellular matrix and TGP'P. Dev Biol 160;293-302.
72. Sappino, A.-P., J. Huarte, D. Bclin, J.-D. Vas-salli (1989) Plasminogen activators in tissue remodeling and invasion; mRNA localization in mouse ovaries and implanting embryos. J Cell Biol 109; 2471-2479.
73. Schmidt, C., F. Bladt, S. Goedecke, V. Brinkmann, W. Zschiesche, M. Sharpe, E. Gherardi, C. Birchmeier (1995) Scatter factor/lrepatocyte growth factor is essential for liver development. Nature 373;699-702.
74. Seeds, N.W., S. Haffke, K. Christensen, J. Schoomaker (1990) Cerebellar granule cell migration involves proteolysis. Adv Exp Med Biol 265;169-178.
75. Seeds, N.W., S. Verrall, G. Friedman, S. Hayden, D. Gadotti, S. Haffke, K. Christensen, B. Gardner, P. McGuire, A. Krystosek (1992) Plasminogen activators and plasminogen activator inhibitors in neural development. Ann NY Acad Sci 667; 32-40.
76. Shimamoto, A., T. Kimura, K. Matsumoto, T. Nakamura (1993) Hepatocyte growth factorlike protein is identical to macrophage stimulating protein. FEBS Lett 333; 61-64.
77. Skeel, A., E.J. Leonard (1994) Action and target cell specificity of human macrophage-stimulating protein (MSP). J Immunol 152; 4618-4623.
78. Skeel, A., T. Yoshimura, S.D. Showaltzer, S. Tanaka, E. Appella, E.J. Leonard (1991) Macrophage stimulating protein; Purification, partial amino acid sequence, and cellular activity. J Exp Med 173; 1227-1234.
79. Soifer SI., K G Peters, I O'Keefe, S R. Coughlin (1994) Disparate temporal expression of the prothrombin and thrombin receptor genes during mouse development. Am J Pathol 144; 60-69.
80. Sonnenbcrg, E., D. Meyer, K.M. Weidner, C. Birchmeier (1993) Scatter factor/hepatocyte growth factor and its receptor, the c-met tyrosine kinase. can mediate a signal exchange between mesenchyme and epithelia during mouse development. J Cell Biol 123; 223-235.
81. Stern, C.D. (1984) A simple model for early morphogenesis. J Thcor Biol 107; 229-242.
82. Stem, C.D., G.W. Ireland, S.E. Herrick, E. Gherardi, J. Gray, M. Perryman, M. Stoker (1990) Epithelial scatter factor and development of the chick embryonic axis. Development 110; 1271-1284.
83. Stoker, M., E. Gherardi, M. Perryman, J. Gray (1987) Scatter factor is a fibroblast-derived modulator of epithelial cell mobility. Nature 327; 239-242.
84. Stoker, M., M. Perryman (1985) An epithelial scatter factor released bv embryo fibroblasts. J Cell Sci 77;209-213.
85. Streit, A., C.D. Stern, C. Théry, G. Ireland, S. Aparicio, M.J. Sharpe, E. Gherardi (1995) A role for IHGF/SF in neural induction and its expression in Henscn's node during gastrulation. Development 121;813-824.
86. Suidan, H.S., S.R. Stone, B.A. Hemmings, D. Monard (1992) Thrombin causes neurite retraction in neuronal cells through activation of cell surface receptors. Neuron 8;363-375.
87. Théry, C, M.J. Sharpe, S.J. Batley, C.D. Stern, E. Gherardi (1995) Expression of HGF/SF. HGFI/MSP and e-tnel suggests new functions during early chick development. Dev Genet 17;90-101.
88. Tsarfaty, I., S. Rong, J.H. Resau, S. Rulong, P. Pinto da Silva, G.F. Vande Woude (1994) The Met proto-oncogene mesenchymal to epithelial cell conversion. Science 263;98-101.
89. Uehara, Y., N. Kitamura (1992) Expression of a human hepatocyte growth factor/scatter factor cDNA in MDCK epithelial cells influences cell morphology, motility, and anchorage-independent growth. J Cell Biol 117; 889-894.
90. Uehara, Y., O. Minowa, C. Mort, K. Shiota, J. Kuno, T. Noda, N. Kitamura (1995) Placental defect and embryonic lethality in mice lacking hepatocyte growth factor/scatter factor. Nature 373;702-705.
91. Valinsky, J.E., N.M. Le Douarin (1985) Production of plasminogen activator by migrating cephalic neural crest cells. EMBO J 4; 1403-1406.
92. Valinsky, J.E., E. Reich (1981) Plasminogen in the chick embryo; Transport and biosynthesis. J Biol Client 256. 12470-12475.
93. Vassalli, J.-D, A.-P. Sappino, D. Belin (1991) The plasminogen aclivator/plasmin system. J Clin Invest 88; 1067-1072.
94. Vertle, P., H.P. Stoppelli, P Galeffi, P. Di Noccra, F. Blasi (1984) Identification and primary sequence of an unspliced human urokinase polv(A)+RNA. Proc Nall Acad Sci USA 81; 4727-4731.
95. Vu, T.-K.H., D.T. Hung, V.l. Wheaton, S.R. Coughlin (1991) Molecular cloning of a functional thrombin receptor reveals a novel proteolytic mechanism of receptor activation. Cell 64; 1057-1068.
96. Wang, M.H., C. Ronsin, M.-C. Gesnel, L. Coupey, A. Skeel, E.J. Leonard, R. Breathnach (1994) Identification of the Ron gene product as the receptor for the human macrophage stimulating protein. Science 266; 117-119.
97. Weidner, K.M., N. Arakaki, G. Hartmann, I. Van-derkerckhovc, S. Weingart, H. Rieder, C. Fonatsch, H. Tsubouchi, T. Hishida, Y. Dai-kuhara, W. Birchmeier (1991) Evidence for the identity of human scatter factor and human hepatocyte growth factor. Proc Natl Acad Sci USA 88; 7001-7005.
98. Yoshimura, T., N. Yuhki, M.-H. Wang, A. Skeel, E.J. Leonard (1993) Cloning, sequencing and expression of human macrophage stimulating protein (MSP. MSTI) confirms MSP as a member of the family of kringle proteins and locates the MSP gene on chromosome 3. J Biol Chem 268;15461-15468.