Hypoxia-inducible factor 1α modulates adhesion, migration, and FAK phosphorylation in vascular smooth muscle cells

Journal of Cellular Biochemistry

Volumn 96, Issue 5, 2005, Pages 971-985

  Corley, Katina M ^a   Taylor, Caroline J ^a   Lilly, Brenda ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

Adhesion; Focal adhesion kinase (FAK); Hypoxia; Hypoxia inducible factor 1 (HIF 1); Migration; Smooth muscle cells

Indexed keywords

COBALT CHLORIDE; FOCAL ADHESION KINASE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; VASCULOTROPIN; VINCULIN;

ANGIOGENESIS; ANIMAL CELL; AORTA MEDIA; ARTICLE; BASEMENT MEMBRANE; CELL ADHESION; CELL MIGRATION; CONTROLLED STUDY; CORONARY ARTERY; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PHOSPHORYLATION; SMOOTH MUSCLE FIBER; TRANSCRIPTION REGULATION; VASCULAR SMOOTH MUSCLE; VASCULARIZATION;

ADENOVIRIDAE; ANIMALS; ANOXIA; AORTA; BLOTTING, WESTERN; CATTLE; CELL ADHESION; CELL MOVEMENT; CELLS, CULTURED; COBALT; DNA, COMPLEMENTARY; ENDOTHELIUM, VASCULAR; FOCAL ADHESION PROTEIN-TYROSINE KINASES; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; IMMUNOBLOTTING; IMMUNOPRECIPITATION; LUCIFERASES; MICROSCOPY, FLUORESCENCE; MUSCLE, SMOOTH; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; NEOVASCULARIZATION, PATHOLOGIC; PHOSPHORYLATION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TIME FACTORS; TRANSFECTION; TYROSINE; VASCULAR ENDOTHELIAL GROWTH FACTOR A; WOUND HEALING;

ANIMALIA;

EID: 28044462434     PISSN: 07302312     EISSN: None     Source Type: Journal    
DOI: 10.1002/jcb.20559     Document Type: Article

References (62)

1. Andres V. 1998. Control of vascular smooth muscle cell growth and its implication in atherosclerosis and restenosis (review). Int J Mol Med 2:81-89.
2. Ausubel FM. 1995. Current protocols in molecular biology: Laboratory manual John Wiley and Sons, Inc.
3. Banai S, Shweiki D, Pinson A, Chandra M, Lazarovici G, Keshet E. 1994. Upregulation of vascular endothelial growth factor expression induced by myocardial ischaemia: Implications for coronary angiogenesis. Cardiovasc Res 28:1176-1179.
4. Benjamin LE, Hemo I, Keshet E. 1998. A plasticity window for blood vessel remodelling is defined by pericyte coverage of the preformed endothelial network and is regulated by PDGF-B and VEGF. Development 125:1591-1598.
5. Beviglia L, Kramer RH. 1999. HGF induces FAK activation and integrin-mediated adhesion in MTLn3 breast carcinoma cells. Int J Cancer 83:640-649.
6. Bou-Gharios G, Ponticos M, Rajkumar V, Abraham D. 2004. Extra-cellular matrix in vascular networks. Cell Prolif 37:207-220.
7. Bundy R, Marczin N, Chester AH, Yacoub M. 1999. Differential regulation of DNA synthesis by nitric oxide and hydroxyurea in vascular smooth muscle cells. Am J Physiol 277:H1799-H807.
8. Carmeliet P. 2000. Mechanisms of angiogenesis and arteriogenesis. Nat Med 6:389-395.
9. Carmeliet P, Jain RK. 2000. Angiogenesis in cancer and other diseases. Nature 407:249-257.
10. Casscells W. 1991. Smooth muscle cell growth factors. Prog Growth Factor Res 3:177-206.
11. Ceradini DJ, Kulkarni AR, Callaghan MJ, Tepper OM, Bastidas N, Kleinman ME, Capla JM, Galiano RD, Levine JP, Gurtner GC. 2004. Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nat Med 10:858-864.
12. D'Angelo G, Ladoux A, Frelin C. 2000. Hypoxia-induced transcriptional activation of vascular endothelial growth factor is inhibited by serum. Biochem Biophys Res Commun 267:334-338.
13. Detmar M, Brown LF, Schon MP, Elicker BM, Velasco P, Richard L, Fukumura D, Monsky W, Claffey KP, Jain RK. 1998. Increased microvascular density and enhanced leukocyte rolling and adhesion in the skin of VEGF transgenic mice. J Invest Dermatol 111:1-6.
14. Eliceiri BP, Puente XS, Hood JD, Stupack DG, Schlaepfer DD, Huang XZ, Sheppard D, Cheresh DA. 2002. Src-mediated coupling of focal adhesion kinase to integrin alpha(v)beta5 in vascular endothelial growth factor signaling. J Cell Biol 157:149-160.
15. Forsythe JA, Jiang BH, Iyer NV, Agani F, Leung SW, Koos RD, Semenza GL. 1996. Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol Cell Biol 16:4604-4613.
16. Friedman GB, Taylor CT, Parkos CA, Colgan SP. 1998. Epithelial permeability induced by neutrophil transmigration is potentiated by hypoxia: Role of intracellular cAMP. J Cell Physiol 176:76-84.
17. Gardner LB, Li Q, Park MS, Flanagan WM, Semenza GL, Dang CV. 2001. Hypoxia inhibits G1/S transition through regulation of p27 expression. J Biol Chem 276:7919-7926.
18. Gerthoffer WT, Gunst SJ. 2001. Invited review: Focal adhesion and small heat shock proteins in the regulation of actin remodeling and contractility in smooth muscle. J Appl Physiol 91:963-972.
19. Goda N, Ryan HE, Khadivi B, McNulty W, Rickert RC, Johnson RS. 2003. Hypoxia-inducible factor 1alpha is essential for cell cycle arrest during hypoxia. Mol Cell Biol 23:359-369.
20. Gorlach A, Diebold I, Schini-Kerth VB, Berchner-Pfannschmidt U, Roth U, Brandes RP, Kietzmann T, Busse R. 2001. Thrombin activates the hypoxia-inducible factor-1 signaling pathway in vascular smooth muscle cells: Role of the p22(phox)-containing NADPH oxidase. Circ Res 89:47-54.
21. Harlow E, Lane D. 1999. Using antibodies: A laboratory manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
22. He TC, Zhou S, da Costa LT, Yu J, Kinzler KW, Vogelstein B. 1998. A simplified system for generating recombinant adenoviruses. Proc Natl Acad Sci USA 95:2509-2514.
23. Ilic D, Furuta Y, Kanazawa S, Takeda N, Sobue K, Nakatsuji N, Nomura S, Fujimoto J, Okada M, Yamamoto T. 1995. Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature 377:539-544.
24. Kanaya K, Kamitani T. 2003. pVHL-independent ubiquitination of HIF1alpha and its stabilization by cobalt ion. Biochem Biophys Res Commun 306:750-755.
25. Kong T, Eltzschig HK, Karhausen J, Colgan SP, Shelley CS. 2004. Leukocyte adhesion during hypoxia is mediated by HIF-1-dependent induction of beta2 integrin gene expression. Proc Natl Acad Sci USA 101:10440-10445.
26. Koochekpour S, Jeffers M, Wang PH, Gong C, Taylor GA, Roessler LM, Stearman R, Vasselli JR, Stetler-Stevenson WG, Kaelin WG, Jr., Linehan WM, Klausner RD, Gnarra JR, Vande Woude GF. 1999. The von Hippel-Lindau tumor suppressor gene inhibits hepatocyte growth factor/scatter factor-induced invasion and branching morphogenesis in renal carcinoma cells. Mol Cell Biol 19:5902-5912.
27. Larcher F, Murillas R, Bolontrade M, Conti CJ, Jorcano JL. 1998. VEGF/VPF overexpression in skin of transgenic mice induces angiogenesis, vascular hyperpermeability and accelerated tumor development. Oncogene 17:303-311.
28. Le Boeuf F, Houle F, Huot J. 2004. Regulation of vascular endothelial growth factor receptor 2-mediated phosphorylation of focal adhesion kinase by heat shock protein 90 and Src kinase activities. J Biol Chem 279:39175-39185.
29. Lee RJ, Springer ML, Blanco-Bose WE, Shaw R, Ursell PC, Blau HM. 2000. VEGF gene delivery to myocardium: Deleterious effects of unregulated expression. Circulation 102:898-901.
30. Maulik G, Kijima T, Ma PC, Ghosh SK, Lin J, Shapiro GI, Schaefer E, Tibaldi E, Johnson BE, Salgia R. 2002. Modulation of the c-Met/hepatocyte growth factor pathway in small cell lung cancer. Clin Cancer Res 8:620-627.
31. Maxwell P, Salnikow K. 2004. HIF-1: An oxygen and metal responsive transcription factor. Cancer Biol Ther 3:29-35.
32. Moiseeva EP. 2001. Adhesion receptors of vascular smooth muscle cells and their functions. Cardiovasc Res 52:372-386.
33. Neville C, Rosenthal N, Hauschka S. 1998. DNA transfection of cultured muscle cells: "Methods in cell biology." San Diego: Academic Press.
34. Oh RR, Park JY, Lee JH, Shin MS, Kim HS, Lee SK, Kim YS, Lee SH, Lee SN, Yang YM, Yoo NJ, Lee JY, Park WS. 2002. Expression of HGF/SF and Met protein is associated with genetic alterations of VHL gene in primary renal cell carcinomas. Apmis 110:229-238.
35. Oliver MH, Harrison NK, Bishop JE, Cole PJ, Laurent GJ. 1989. A rapid and convenient assay for counting cells cultured in microwell plates: Application for assessment of growth factors. J Cell Sci 92(Pt 3):513-518.
36. Owens GK, Kumar MS, Wamhoff BR. 2004. Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol Rev 84:767-801.
37. Page EL, Robitaille GA, Pouyssegur J, Richard DE. 2002. Induction of hypoxia-inducible factor-1alpha by transcriptional and translational mechanisms. J Biol Chem 277:48403-48409.
38. Panetti TS. 2002. Tyrosine phosphorylation of paxillin, FAK, and p130CAS: Effects on cell spreading and migration. Front Biosci 7:d143-d150.
39. Paul SA, Simons JW, Mabjeesh NJ. 2004. HIF at the crossroads between ischemia and carcinogenesis. J Cell Physiol 200:20-30.
40. Pennacchietti S, Michieli P, Galluzzo M, Mazzone M, Giordano S, Comoglio PM. 2003. Hypoxia promotes invasive growth by transcriptional activation of the met protooncogene. Cancer Cell 3:347-361.
41. Pugh CW, Ratcliffe PJ. 2003. Regulation of angiogenesis by hypoxia: Role of the HIF system. Nat Med 9:677-684.
42. Richard DE, Berra E, Pouyssegur J. 2000. Nonhypoxic pathway mediates the induction of hypoxia-inducible factor 1alpha in vascular smooth muscle cells. J Biol Chem 275:26765-26771.
43. Rose F, Grimminger F, Appel J, Heller M, Pies V, Weissmann N, Fink L, Schmidt S, Krick S, Camenisch G, Gassmann M, Seeger W, Hanze J. 2002. Hypoxic pulmonary artery fibroblasts trigger proliferation of vascular smooth muscle cells: Role of hypoxia-inducible transcription factors. FASEB J 16:1660-1661.
44. Sabia PJ, Powers ER, Ragosta M, Sarembock IJ, Burwell LR, Kaul S. 1992. An association between collateral blood flow and myocardial viability in patients with recent myocardial infarction. N Engl J Med 327:1825-1831.
45. Schieffer B, Drexler H, Ling BN, Marrero MB. 1997. G protein-coupled receptors control vascular smooth muscle cell proliferation via pp60c-src and p21ras. Am J Physiol 272:C2019-C2030.
46. Schlaepfer DD, Mitra SK. 2004. Multiple connections link FAK to cell motility and invasion. Curr Opin Genet Dev 14:92-101.
47. Semenza GL. 2000. HIF-1 and human disease: One highly involved factor. Genes Dev 14:1983-1991.
48. Semenza GL. 2002. HIF-1 and tumor progression: Pathophysiology and therapeutics. Trends Mol Med 8:S62-S67.
49. Semenza GL. 2003. Angiogenesis in ischemic and neoplastic disorders. Annu Rev Med 54:17-28.
50. Semenza GL, Wang GL. 1992. A nuclear factor induced by hypoxia via de novo protein synthesis binds to the human erythropoietin gene enhancer at a site required for transcriptional activation. Mol Cell Biol 12:5447-5454.
51. Spector D, Goldman R, Leinwand L. 1998. Cells: A laboratory manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
52. Sultana C, Shen Y, Johnson C, Kalra VK. 1999. Cobalt chloride-induced signaling in endothelium leading to the augmented adherence of sickle red blood cells and transendothelial migration of monocyte-like HL-60 cells is blocked by PAF-receptor antagonist. J Cell Physiol 179:67-78.
53. Tang N, Wang L, Esko J, Giordano FJ, Huang Y, Gerber HP, Ferrara N, Johnson RS. 2004. Loss of HIF-1alpha in endothelial cells disrupts a hypoxia-driven VEGF autocrine loop necessary for tumorigenesis. Cancer Cell 6:485-495.
54. Tscheudschilsuren G, Aust G, Nieber K, Schilling N, Spanel-Borowski K. 2002. Microvascular endothelial cells differ in basal and hypoxia-regulated expression of angiogenic factors and their receptors. Microvasc Res 63:243-251.
55. Webb DJ, Parsons JT, Horwitz AF. 2002. Adhesion assembly, disassembly and turnover in migrating cells - over and over and over again. Nat Cell Biol 4:E97-E100.
56. Weis M, Schlichting CL, Engleman EG, Cooke JP. 2002. Endothelial determinants of dendritic cell adhesion and migration: New implications for vascular diseases. Arterioscler Thromb Vasc Biol 22:1817-1823.
57. White FC, Carroll SM, Magnet A, Bloor CM. 1992. Coronary collateral development in swine after coronary artery occlusion. Circ Res 71:1490-1500.
58. Xia YP, Li B, Hylton D, Detmar M, Yancopoulos GD, Rudge JS. 2003. Transgenic delivery of VEGF to mouse skin leads to an inflammatory condition resembling human psoriasis. Blood 102:161-168.
59. Xu W, Baribault H, Adamson ED. 1998. Vinculin knockout results in heart and brain defects during embryonic development. Development 125:327-337.
60. Yamakawa M, Liu LX, Date T, Belanger AJ, Vincent KA, Akita GY, Kuriyama T, Cheng SH, Gregory RJ, Jiang C. 2003. Hypoxia-inducible factor-1 mediates activation of cultured vascular endothelial cells by inducing multiple angiogenic factors. Circ Res 93:664-673.
61. Yarbro JW. 1992. Mechanism of action of hydroxyurea. Semin Oncol 19:1-10.
62. Yuan Y, Hilliard G, Ferguson T, Millhorn DE. 2003. Cobalt inhibits the interaction between hypoxia-inducible factor-alpha and von Hippel-Lindau protein by direct binding to hypoxia-inducible factor-alpha. J Biol Chem 278:15911-15916.