Thrombomodulin promotes focal adhesion kinase activation and contributes to angiogenesis by binding to fibronectin

Oncotarget

Volumn 7, Issue 42, 2016, Pages 68122-68139

  Hsu, Yun Yan ^a   Shi, Guey Yueh ^a   Wang, Kuan Chieh ^a   Ma, Chih Yuan ^a   Cheng, Tsung Lin ^b   Wu, Hua Lin ^a  

^a NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^b KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

Author keywords

Angiogenesis; Endothelial cells; Fibronectin; Thrombomodulin; VEGF

Indexed keywords

FIBRONECTIN; FOCAL ADHESION KINASE; GELATINASE B; THROMBOMODULIN; VASCULOTROPIN; PROTEIN BINDING; VASCULOTROPIN A;

A2058 CELL LINE; AMINO TERMINAL SEQUENCE; ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B16-BL6 CELL LINE; BINDING SITE; CELL ADHESION; CELL INVASION; CELL MIGRATION; CONTROLLED STUDY; DRUG TARGETING; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; ENZYME SYNTHESIS; GENE KNOCKDOWN; HUMAN; HUMAN CELL; HUVEC CELL LINE; IMMUNOFLUORESCENCE; MOUSE; NONHUMAN; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; RNA INTERFERENCE; TUMOR VASCULARIZATION; UPREGULATION; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL MOTION; DRUG EFFECTS; EXPERIMENTAL MELANOMA; GENETICS; METABOLISM; PATHOLOGY; TUMOR CELL LINE;

ANIMALS; CELL ADHESION; CELL LINE, TUMOR; CELL MOVEMENT; CELLS, CULTURED; ENZYME ACTIVATION; FIBRONECTINS; FOCAL ADHESION PROTEIN-TYROSINE KINASES; HUMANS; MELANOMA, EXPERIMENTAL; MICE, INBRED C57BL; NEOVASCULARIZATION, PHYSIOLOGIC; PROTEIN BINDING; RNA INTERFERENCE; THROMBOMODULIN; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 85035094459     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/ONCOTARGET.11828     Document Type: Article

References (46)

1. Geiger B, Bershadsky A, Pankov R, Yamada KM. Transmembrane crosstalk between the extracellular matrix-cytoskeleton crosstalk. Nat Rev Mol Cell Biol. 2001; 2:793-805
2. Avraamides CJ, Garmy-Susini B, Varner JA. Integrins in angiogenesis and lymphangiogenesis. Nat Rev Cancer. 2008; 8:604-617
3. Guo W, Giancotti FG. Integrin signalling during tumour progression. Nat Rev Mol Cell Biol. 2004; 5:816-826
4. Larsen M, Artym VV, Green JA, Yamada KM. The matrix reorganized: extracellular matrix remodeling and integrin signaling. Curr Opin Cell Biol. 2006; 18:463-471
5. Mitra SK, Hanson DA, Schlaepfer DD. Focal adhesion kinase: in command and control of cell motility. Nat Rev Mol Cell Biol. 2005; 6:56-68
6. Morgan MR, Humphries MJ, Bass MD. Synergistic control of cell adhesion by integrins and syndecans. Nat Rev Mol Cell Biol. 2007; 8:957-969
7. Ponta H, Sherman L, Herrlich PA. CD44: from adhesion molecules to signalling regulators. Nat Rev Mol Cell Biol. 2003; 4:33-45
8. Conway EM. Thrombomodulin and its role in inflammation. Semin Immunopathol. 2012; 34:107-125
9. 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 USA. 1995; 92:850-854
10. Cheng TL, Wu YT, Lai CH, Kao YC, Kuo CH, Liu SL, Hsu YY, Chen PK, Cho CF, Wang KC, Lin WL, Chang BI, Chen CM, et al. Thrombomodulin regulates keratinocyte differentiation and promotes wound healing. J Invest Dermatol. 2013; 133:1638-1645
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. Wang KC, Li YH, Shi GY, Tsai HW, Luo CY, Cheng MH, Ma CY, Hsu YY, Cheng TL, Chang BI, Lai CH, Wu HL. Membrane-Bound Thrombomodulin Regulates Macrophage Inflammation in Abdominal Aortic Aneurysm. Arterioscler Thromb Vasc Biol. 2015; 35:2412-2422
13. Hsu YY, Shi GY, Kuo CH, Liu SL, Wu CM, Ma CY, Lin FY, Yang HY, Wu HL. Thrombomodulin is an ezrin-interacting protein that controls epithelial morphology and promotes collective cell migration. FASEB J. 2012; 26:3440-3452
14. Shi CS, Shi GY, Chang YS, Han HS, Kuo CH, Liu C, Huang HC, Chang YJ, Chen PS, Wu HL. Evidence of human thrombomodulin domain as a novel angiogenic factor. Circulation. 2005; 111:1627-1636
15. Kuo CH, Chen PK, Chang BI, Sung MC, Shi CS, Lee JS, Chang CF, Shi GY, Wu HL. The recombinant lectinlike domain of thrombomodulin inhibits angiogenesis through interaction with Lewis Y antigen. Blood. 2012; 119:1302-1313
16. Kim S, Bell K, Mousa SA, Varner JA. Regulation of angiogenesis in vivo by ligation of integrin alpha5beta1 with the central cell-binding domain of fibronectin. Am J Pathol. 2000; 156:1345-1362
17. Singh P, Carraher C, Schwarzbauer JE. Assembly of fibronectin extracellular matrix. Annu Rev Cell Dev Biol. 2010; 26:397-419
18. Sen T, Dutta A, Maity G, Chatterjee A. Fibronectin induces matrix metalloproteinase-9 (MMP-9) in human laryngeal carcinoma cells by involving multiple signaling pathways. Biochimie. 2010; 92:1422-1434
19. Toth M, Fridman R. Assessment of Gelatinases (MMP-2 and MMP-9 by Gelatin Zymography. Methods Mol Med. 2001; 57:163-174
20. Hirokawa K, Aoki N. Up-regulation of thrombomodulin in human umbilical vein endothelial cells in vitro. J Biochem. 1990; 108:839-845
21. Hirokawa K, Aoki N. Up-regulation of thrombomodulin by activation of histamine H1-receptors in human umbilical-vein endothelial cells in vitro. Biochem J. 1991; 276:739-743
22. Horie S, Kizaki K, Ishii H, Kazama M. Retinoic acid stimulates expression of thrombomodulin, a cell surface anticoagulant glycoprotein, on human endothelial cells. Differences between up-regulation of thrombomodulin by retinoic acid and cyclic AMP. Biochem J. 1992; 281:149-154
23. Calnek DS, Grinnell BW. Thrombomodulin-dependent anticoagulant activity is regulated by vascular endothelial growth factor. Exp Cell Res. 1998; 238:294-298
24. Ruoslahti E. RGD and other recognition sequences for integrins. Annu Rev Cell Dev Biol. 1996; 12:697-715
25. Chen N, Chen CC, Lau LF. Adhesion of human skin fibroblasts to Cyr61 is mediated through integrin alpha 6beta 1 and cell surface heparan sulfate proteoglycans. J Biol Chem. 2000; 275:24953-24961
26. Soderberg O, Gullberg M, Jarvius M, Ridderstrale K, Leuchowius KJ, Jarvius J, Wester K, Hydbring P, Bahram F, Larsson LG, Landegren U. Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat Methods. 2006; 3:995-1000
27. Lo IC, Lin TM, Chou LH, Liu SL, Wu LW, Shi GY, Wu HL, Jiang MJ. Ets-1 mediates platelet-derived growth factor-BB-induced thrombomodulin expression in human vascular smooth muscle cells. Cardiovasc Res. 2009; 81:771-779
28. Huang YH, I CC, Kuo CH, Hsu YY, Lee FT, Shi GY, Tseng SH, Wu HL. Thrombomodulin promotes corneal epithelial wound healing. PLoS One. 2015; 10:e0122491
29. Tomkowicz B, Rybinski K, Foley B, Ebel W, Kline B, Routhier E, Sass P, Nicolaides NC, Grasso L, Zhou Y. Interaction of endosialin/TEM1 with extracellular matrix proteins mediates cell adhesion and migration. Proc Natl Acad Sci USA. 2007; 104:17965-17970
30. Van Obberghen-Schilling E, Tucker RP, Saupe F, Gasser I, Cseh B, Orend G. Fibronectin and tenascin-C: accomplices in vascular morphogenesis during development and tumor growth. Int J Dev Biol. 2011; 55:511-525
31. Vu TH, Shipley JM, Bergers G, Berger JE, Helms JA, Hanahan D, Shapiro SD, Senior RM, Werb Z. MMP-9/gelatinase B is a key regulator of growth plate angiogenesis and apoptosis of hypertrophic chondrocytes. Cell. 1998; 93:411-422
32. Das S, Banerji A, Frei E, Chatterjee A. Rapid expression and activation of MMP-2 and MMP-9 upon exposure of human breast cancer cells (MCF-7) to fibronectin in serum free medium. Life Sci. 2008; 82:467-476
33. Esparza J, Vilardell C, Calvo J, Juan M, Vives J, Urbano-Marquez A, Yague J, Cid MC. Fibronectin upregulates gelatinase B (MMP-9) and induces coordinated expression of gelatinase A (MMP-2) and its activator MT1-MMP (MMP-14) by human T lymphocyte cell lines. A process repressed through RAS/MAP kinase signaling pathways. Blood. 1999; 94:2754-2766
34. Shibata K, Kikkawa F, Nawa A, Thant AA, Naruse K, Mizutani S, Hamaguchi M. Both focal adhesion kinase and c-Ras are required for the enhanced matrix metalloproteinase 9 secretion by fibronectin in ovarian cancer cells. Cancer Res. 1998; 58:900-903
35. Park MJ, Kim MS, Park IC, Kang HS, Yoo H, Park SH, Rhee CH, Hong SI, Lee SH. PTEN suppresses hyaluronic acid-induced matrix metalloproteinase-9 expression in U87MG glioblastoma cells through focal adhesion kinase dephosphorylation. Cancer Res. 2002; 62:6318-6322
36. Cho CF, Chen PK, Chang PC, Wu HL, Shi GY. Human plasminogen kringle 1-5 inhibits angiogenesis and induces thrombomodulin degradation in a protein kinase A-dependent manner. J Mol Cell Cardiol. 2013; 63:79-88
37. Sumagin R, Robin AZ, Nusrat A, Parkos CA. Activation of PKCbetaII by PMA facilitates enhanced epithelial wound repair through increased cell spreading and migration. PLoS One. 2013; 8:e55775
38. Besson A, Davy A, Robbins SM, Yong VW. Differential activation of ERKs to focal adhesions by PKC epsilon is required for PMA-induced adhesion and migration of human glioma cells. Oncogene. 2001; 20:7398-7407
39. Shen TL, Park AY, Alcaraz A, Peng X, Jang I, Koni P, Flavell RA, Gu H, Guan JL. Conditional knockout of focal adhesion kinase in endothelial cells reveals its role in angiogenesis and vascular development in late embryogenesis. J Cell Biol. 2005; 169:941-952
40. Peng X, Ueda H, Zhou H, Stokol T, Shen TL, Alcaraz A, Nagy T, Vassalli JD, Guan JL. Overexpression of focal adhesion kinase in vascular endothelial cells promotes angiogenesis in transgenic mice. Cardiovasc Res. 2004; 64:421-430
41. Zhou X, Rowe RG, Hiraoka N, George JP, Wirtz D, Mosher DF, Virtanen I, Chernousov MA, Weiss SJ. Fibronectin fibrillogenesis regulates three-dimensional neovessel formation. Genes Dev. 2008; 22:1231-1243
42. Langenkamp E, Zhang L, Lugano R, Huang H, Elhassan TE, Georganaki M, Bazzar W, Loof J, Trendelenburg G, Essand M, Ponten F, Smits A, Dimberg A. Elevated Expression of the C-Type Lectin CD93 in the Glioblastoma Vasculature Regulates Cytoskeletal Rearrangements That Enhance Vessel Function and Reduce Host Survival. Cancer Res. 2015; 75:4504-4516
43. Orlandini M, Galvagni F, Bardelli M, Rocchigiani M, Lentucci C, Anselmi F, Zippo A, Bini L, Oliviero S. The characterization of a novel monoclonal antibody against CD93 unveils a new antiangiogenic target. Oncotarget. 2014; 5:2750-2760. doi: 10.18632/oncotarget.1887
44. Chung AS, Lee J, Ferrara N. Targeting the tumour vasculature: insights from physiological angiogenesis. Nat Rev Cancer. 2010; 10:505-514
45. Samant RS, Shevde LA. Recent advances in anti-angiogenic therapy of cancer. Oncotarget. 2011; 2:122-134. doi: 10.18632/oncotarget.234
46. Guba M, von Breitenbuch P, Steinbauer M, Koehl G, Flegel S, Hornung M, Bruns CJ, Zuelke C, Farkas S, Anthuber M, Jauch KW, Geissler EK. Rapamycin inhibits primary and metastatic tumor growth by antiangiogenesis: involvement of vascular endothelial growth factor. Nat Med. 2002; 8:128-135