Evidence of human thrombomodulin domain as a novel angiogenic factor

Circulation

Volumn 111, Issue 13, 2005, Pages 1627-1636

  Shi, Chung Sheng ^a   Shi, Guey Yueh ^a   Chang, Yi Sheng ^a   Han, Huai Song ^a   Kuo, Cheng Hsiang ^a   Liu, Che ^a   Huang, Huey Chun ^a   Chang, Yu Jia ^a   Chen, Pin Shern ^a   Wu, Hua Lin ^a  

^a NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

Author keywords

Angiogenesis; Endothelium; Glycoproteins

Indexed keywords

ANGIOGENIC FACTOR; ENDOTHELIAL NITRIC OXIDE SYNTHASE; EPIDERMAL GROWTH FACTOR; HEPARIN; MATRIGEL; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN C; PROTEIN KINASE B; SERINE; THREONINE; THROMBOMODULIN;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL CULTURE; CELL INVASION; CORNEA; CORNEA LIMBUS; CORNEA NEOVASCULARIZATION; DNA SYNTHESIS; ENDOTHELIUM CELL; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; NUDE MOUSE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; UMBILICAL VEIN;

ANGIOGENESIS INDUCING AGENTS; ANIMALS; CELL PROLIFERATION; CELLS, CULTURED; CHEMOTAXIS; CORNEA; ENDOTHELIUM, VASCULAR; EPIDERMAL GROWTH FACTOR; HUMANS; MICE; NEOVASCULARIZATION, PATHOLOGIC; NEOVASCULARIZATION, PHYSIOLOGIC; PHOSPHORYLATION; PROTEIN BIOSYNTHESIS; PROTEIN C; PROTEIN STRUCTURE, TERTIARY; RATS; RECOMBINANT PROTEINS; THROMBOMODULIN;

EID: 20244382267     PISSN: 00097322     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.CIR.0000160364.05405.B5     Document Type: Article

References (43)

1. Esmon NL, Owen WG, Esmon CT. Isolation of a membrane-bound cofactor for thrombin-catalyzed activation of protein C. J Biol Chem. 1982;257:859-864.
2. Suzuki K, Kusumoto S, Deyashiki Y, Nishioka J, Maruyama I, Zushi M, Kawahara S, Honda G, Yamamoto S, Horiguchi S. Structure and expression of human TM, a thrombin receptor on endothelium acting as a cofactor for protein C activation. EMBO J. 1987;6:1891-1897.
3. Boffa MC, Burke B, Haudenschild CC. Preservation of thrombomodulin antigen on vascular and extravascular surfaces. J Histochem Cytochem. 1987;35:1267-1276.
4. Healy AM, Rayburn HB, Rosenberg RD, Weiler H. Absence of the blood-clotting regulator thrombomodulin causes embryonic lethality in mice before development of a functional cardiovascular system. Proc Natl Acad Sci U S A. 1995;92:850-854.
5. Takano S, Kimura S, Ohdama S, Aoki N. Plasma thrombomodulin in health and diseases. Blood. 1990;76:2024-2029.
6. Yamamoto S, MIizoguchi T, Tamaki T, Ohkuchi M, Kimura S, Aoki N. Urinary thrombomodulin, its isolation and characterization. J Biochem (Tokyo). 1993;113:433-440.
7. Boehme MWJ, Galle P, Stremmel W. Kinetics of thrombomodulin release and endothelial cell injury by neutrophil-derived proteases and oxygen radicals. Immunology. 2002;107:340-349.
8. Salomaa V, Matei C, Aleksic N, Sansores-Garcia L, Folsom AR, Juneja H, Chambless LE, Wu KK. Soluble thrombomodulin as a predictor of incident coronary heart disease and symptom less carotid artery atherosclerosis in the Atherosclerosis Risk in Communities (ARIC) study: a case-cohort study. Lancet. 1999;353:1729-1734.
9. Hamada H, Ishii H, Sakyo K, Horie S, Nishiki K, Kazama M. The epidermal growth factor-like domain of recombinant human thrombomodulin exhibits mitogenic activity for Swiss 3T3 cells. Blood. 1995;86:225-233.
10. Conway EM, Van de Wouwer M, Pollefeyt S, Jurk K, Van Aken H, De Vriese A, Weitz JI, Weiler H, Hellings PW, Schaeffer P, Herbert JM, Collen D, Theilmeier G. The lectin-like domain of thrombomodulin confers protection from neutrophil-mediated tissue damage by suppressing adhesion molecule expression via nuclear factor kB and mitogen-activated protein kinase pathways. J Exp Med. 2002;196:565-577.
11. Huang HC, Shi GY, Jiang SJ, Shi CS, Wu CM, Yang HY, Wu HL. Thrombomodulin-mediated cell adhesion: involvement of its lectin-like domain. J Biol Chem. 2003;278:46750-46759.
12. Han HS, Wu HL, Lin BT, Shi CS, Shi GY. Effect of thrombomodulin on plasminogen activation. Fibrinolysis Proteolysis. 2000;14:221-228.
13. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970;227:680-685.
14. Shi GY, Hau JS, Wang SJ, Wu IS, Chang BI, Lin MT, Chow YH, Chang WC, Wing LYC, Jen CJ, Wu HL. Plasmin and the regulation of tissue-type plasminogen activator biosynthesis in human endothelial cells. J Biol Chem. 1992;267:19363-19368.
15. Lee OH, Bae SK, Bae MH, Lee YM, Moon EJ, Cha HJ, Kwon YG, Kim KW. Identification of angiogenic properties of insulin-like growth factor II in in vitro angiogenesis models. Br J Cancer. 2000;82:385-391.
16. Kenyon BM, Voest EE, Chen CC, Flynn E, Folkman J, D'Amato RJ. A model of angiogenesis in the mouse cornea. Invest Ophthalmol Vis Sci. 1996;37:1625-1632.
17. Passaniti A, Taylor RM, Pili R, Guo Y, Long PV, Haney JA, Pauly RR, Grant DS, Martin GR. A simple quantitative method for assessing angiogenesis and antiangiogenic agents using reconstituted basement membrane, heparin, and fibroblast growth factor. Lab Invest. 1992;67:519-528.
18. Shirai T, Shiojiri S, Ito H, Yamamoto S, Kusumoto H, Deyashiki Y, Maruyama I, Suzuki K. Gene structure of human thrombomodulin, a cofactor for thrombin-catalyzed activation of protein C. J Biochem. 1988;103:281-285.
19. Rousseau S, Houle F, Landry J, Huot J. p38 MAP kinase activation by vascular endothelial growth factor mediates actin reorganization and cell migration in human endothelial cells. Oncogene. 1997;15:2169-2177.
20. Kawasaki K, Smith RS, Hsieh CM, Sun J, Chao J, Liao JK. Activation of the phosphatidylinositol 3-kinase/protein kinase Akt pathway mediates nitric oxide-induced endothelial cell migration and angiogenesis. Mol Cell Biol. 2003;23:5726-5737.
21. Pepper MS. Role of the matrix metalloproteinase and plasminogen activator-plasmin systems in angiogenesis. Arterioscler Thromb Vasc Biol. 2001;21:1104-1117.
22. Kumar R, Yoneda J, Bucana CD, Fidler IJ. Regulation of distinct steps of angiogenesis by different angiogenic molecules. Int J Oncol. 1998;12:749-757.
23. Pepper MS, Rosnoblet C, Di Sanza C, Kruithof EK. Synergistic induction of t-PA by vascular endothelial growth factor and basic fibroblast growth factor and localization of t-PA to Weibel-Palade bodies in bovine microvascular endothelial cells. Thromb Haemost. 2001;86:702-709.
24. Kurosawa S, Aoki N. Preparation of thrombomodulin from human placenta. Thromb Res. 1985;37:353-364.
25. Suzuki K, Kusumoto H, Hashimoto S. Isolation and characterization of thrombomodulin from bovine lung. Biochim Biophys Acta. 1986;882:343-352.
26. Carmeliet P. Angiogenesis in health and disease. Nat Med. 2003;9:653-660.
27. Folkman J, Shing Y. Angiogenesis. J Biol Chem. 1992;267:10931-10934.
28. Yancopoulos GD, Davis S, Gale NW, Rudge JS, Wiegand SJ, Holash J. Vascular-specific growth factors and blood vessel formation. Nature. 2000;407:242-248.
29. Cao R, Wu HL, Veitonmaki N, Linden P, Farnebo J, Shi GY, Cao Y. Suppression of angiogenesis and tumor growth by the inhibitor K1-5 generated by plasmin-mediated proteolysis. Proc Natl Acad Sci U S A. 1999;96:5728-5733.
30. Jimenez B, Volpert OV, Crawford SE, Febbraio M, Silverstein RL, Bouck N. Signals leading to apoptosis-dependent inhibition of neovascularization by thrombospondin-J. Nat Med. 2000;6:41-48.
31. O'Reilly MS, Boehm T, Shing Y, Fukai N, Vasios G, Lane WS, Flynn E, Birkhead JR, Olsen BR, Folkman J. Endostatin: an endogenous inhibitor of angiogenesis and tumor growth. Cell. 1997;88:277-285.
32. Corbacho AM, Martinez de la Escalera G, Clapp C. Roles of prolactin and related members of the prolactin/growth hormone/placental lactogen family in angiogenesis. J Endocrinol. 2002;173:219-238.
33. Bourin MC, Lundgren AE, Lindahl U. Isolation and characterization of the glycosaminoglycan component of rabbit thrombomodulin proteoglycan. J Biol Chem. 1990;265:15424-15431.
34. Bechard D, Gentina T, Delehedde M, Scherpereel A, Lyon M, Aumercier M, Vazeux R, Richet C, Degand P, Jude B, Janin A, Fernig DG, Tonnel AB, Lassalle P. Endocan is a novel chondroitin sulfate/dermatan sulfate proteoglycan that promotes hepatocyte growth factor/scatter factor mitogenic activity. J Biol Chem. 2001;276:48341-48349.
35. Tapon-Bretaudiere J, Chabut D, Zierer M, Matou S, Helley D, Bros A, Mourao PAS, Fischer AM. A fucosylated chondroitin sulfate from echinoderm modulates in vitro fibroblast growth factor 2-dependent angiogenesis. Mol Cancer Res. 2002;1:96-102.
36. Pieper JS, Hafmans T, van Wachem PB, van Luyn MJA, Brouwer LA, Veerkamp JH, van Kuppeveit TH. Loading of collagen-heparin sulfate matrices with bFGF promotes angiogenesis and tissue generation in rats. J Biomed Mater Res. 2002;62:185-194.
37. Horowitz A, Tkachenko E, Simons M. Fibroblast growth factor-specific modulation of cellular response by syndecan-4. J Cell Biol. 2004;157:715-725.
38. Miettinen M, Sarlomo-Rikala M. Expression of calretinin, thrombomodulin, keratin 5, and mesothelin in lung carcinomas of different types: an immunohistochemical analysis of 596 tumors in comparison with epithelioid mesotheliomas of the pleura. Am J Surg Pathol 2003;27:150-158.
39. Tezuka Y, Yonezswa S, Marayama I, Matsushita Y, Shimizu T, Obama H, Sagara M, Shirao K, Kusano C, Natsugoe S, Yoshinaka H, Baba M, Fukumoto T, Aikou T, Sato E. Expression of thrombomodulin in esophageal squamous cell carcinoma and its relationship to lymph node metastasis. Cancer Res. 1995;55:4196-4200.
40. Wilhelm S, Schmitt M, Parkinson J, Kuhn W, Graeff H, Wilhelm OG. Thrombomodulin, a receptor for the serine protease thrombin, is decreased in primary tumors and metastases but increased in ascitic fluids of patients with advanced ovarian cancer FIGO IIIc. Int J Oncol. 1998;13:645-651.
41. Ishii H, Majerus PW. Thrombomodulin is present in human plasma and urine. J Clin Invest. 1985;76:2178-2181.
42. Boehme MW, Deng Y, Raeth U, Bierhaus A, Ziegler R, Stremmel W, Nawroth PP. Release of thrombomodulin from endothelial cells by concerted action of TNF-alpha and neutrophils: in vivo and in vitro studies. Immunology. 1996;87:134-140.
43. Lohi O, Urban S, Freeman M. Diverse substrate recognition mechanisms for rhomboids; thrombomodulin is cleaved by mammalian rhomboids. Curr Biol. 2004;14:236-241.