TGF-β suppresses the upregulation of MMP-2 by vascular smooth muscle cells in response to PDGF-BB

American Journal of Physiology - Cell Physiology

Volumn 298, Issue 1, 2010, Pages

  Risinger Jr , George M ^a   Updike, Dawn L ^a   Bullen, Elizabeth C ^a   Tomasek, James J ^a   Howard, Eric W ^a  

^a UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

Author keywords

F actin cytoskeleton; Phenotypic modulation; Platelet derived growth factor BB; Transforming growth factor

Indexed keywords

GELATINASE A; PLATELET DERIVED GROWTH FACTOR BB; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA2; TRANSFORMING GROWTH FACTOR BETA3;

ANIMAL CELL; ARTICLE; AUTOCRINE EFFECT; CELL DIFFERENTIATION; CELL LOSS; CONTROLLED STUDY; FOCAL ADHESION; HUMAN; HUMAN CELL; NONHUMAN; PHASE TRANSITION; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION; SMOOTH MUSCLE CONTRACTION; SMOOTH MUSCLE FIBER; STRESS FIBER; VASCULAR SMOOTH MUSCLE;

ACTINS; ANIMALS; DNA PRIMERS; DOWN-REGULATION; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENES, FOS; HUMANS; MACROPHAGE COLONY-STIMULATING FACTOR; MATRIX METALLOPROTEINASE 2; MUSCLE CONTRACTION; MUSCLE, SMOOTH, VASCULAR; PLATELET-DERIVED GROWTH FACTOR; POLYMERASE CHAIN REACTION; RATS; RATS, INBRED WKY; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; TISSUE INHIBITOR OF METALLOPROTEINASE-1; TISSUE INHIBITOR OF METALLOPROTEINASE-2; TRANSFORMING GROWTH FACTOR BETA1; UP-REGULATION;

EID: 73549104265     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00417.2008     Document Type: Article

References (83)

1. Abramsson A, Lindblom P, Betsholtz C. Endothelial and nonendothelial sources of PDGF-B regulate pericyte recruitment and influence vascular pattern formation in tumors. J Clin Invest 112: 1142-1151, 2003.
2. Agrotis A, Saltis J, Bobik A. Effect of transforming growth factor-beta 1 on platelet-derived growth factor receptor binding and gene expression in vascular smooth muscle cells from SHR and WKY rats. Clin Exp Pharmacol Physiol 21: 145-148, 1994.
3. Ailenberg M, Silverman M. Trichostatin A-histone deacetylase inhibitor with clinical therapeutic potential-is also a selective and potent inhibitor of gelatinase A expression. Biochem Biophys Res Commun 298: 110-115, 2002.
4. Antonelli-Orlidge A, Saunders KB, Smith SR, D'Amore PA. An activated form of transforming growth factor beta is produced by cocultures of endothelial cells and pericytes. Proc Natl Acad Sci USA 86: 4544-4548, 1989.
5. Armulik A, Abramsson A, Betsholtz C. Endothelial/pericyte interactions. Circ Res 97: 512-523, 2005.
6. Auge N, Maupas-Schwalm F, Elbaz M, Thiers JC, Waysbort A, Itohara S, Krell HW, Salvayre R, and Negre-Salvayre A. Role for matrix metalloproteinase-2 in oxidized low-density lipoprotein-induced activation of the sphingomyelin/ceramide pathway and smooth muscle cell proliferation. Circulation 110: 571-578, 2004.
7. Bae IH, Park MJ, Yoon SH, Kang SW, Lee SS, Choi KM, Um HD. Bcl-w promotes gastric cancer cell invasion by inducing matrix metalloproteinase-2 expression via phosphoinositide 3-kinase, Akt, and Sp1. Cancer Res 66: 4991-4995, 2006.
8. Battegay EJ, Raines EW, Seifert RA, Bowen-Pope DF, Ross R. TGF-beta induces bimodal proliferation of connective tissue cells via complex control of an autocrine PDGF loop. Cell 63: 515-524, 1990.
9. Benjamin LE, Golijanin D, Itin A, Pode D, Keshet E. Selective ablation of immature blood vessels in established human tumors follows vascular endothelial growth factor withdrawal. J Clin Invest 103: 159-165, 1999.
10. Betsholtz C. Role of platelet-derived growth factors in mouse development. Int J Dev Biol 39: 817-825, 1995.
11. Bjarnegard M, Enge M, Norlin J, Gustafsdottir S, Fredriksson S, Abramsson A, Takemoto M, Gustafsson E, Fassler R, Betsholtz C. Endothelium-specific ablation of PDGFB leads to pericyte loss and glomerular, cardiac and placental abnormalities. Development 131: 1847-1857, 2004.
12. Blank RS, Owens GK. Platelet-derived growth factor regulates actin isoform expression and growth state in cultured rat aortic smooth muscle cells. J Cell Physiol 142: 635-642, 1990.
13. Carmeliet P. Angiogenesis in health and disease. Nat Med 9: 653-660, 2003.
14. Carvalho RL, Jonker L, Goumans MJ, Larsson J, Bouwman P, Karlsson S, Dijke PT, Arthur HM, Mummery CL. Defective paracrine signalling by TGFbeta in yolk sac vasculature of endoglin mutant mice: a paradigm for hereditary haemorrhagic telangiectasia. Development 131: 6237-6247, 2004.
15. Chen XL, Chen ZS, Ding Z, Dong C, Guo H, Gong NQ. Antisense extracellular signal-regulated kinase-2 gene therapy inhibits platelet-derived growth factor-induced proliferation, migration and transforming growth factor-beta(1) expression in vascular smooth muscle cells and attenuates transplant vasculopathy. Transpl Int 21: 30-38, 2008.
16. Crocker DJ, Murad TM, Geer JC. Role of the pericyte in wound healing. An ultrastructural study. Exp Mol Pathol 13: 51-65, 1970.
17. DaCosta Byfield S, Major C, Laping NJ, Roberts AB. SB-505124 is a selective inhibitor of transforming growth factor-beta type I receptors ALK4, ALK5, and ALK7. Mol Pharmacol 65: 744-752, 2004.
18. Dickson MC, Martin JS, Cousins FM, Kulkarni AB, Karlsson S, Akhurst RJ. Defective haematopoiesis and vasculogenesis in transforming growth factor-beta 1 knock out mice. Development 121: 1845-1854, 1995.
19. Ding R, Darland DC, Parmacek MS, D'Amore PA. Endothelial- mesenchymal interactions in vitro reveal molecular mechanisms of smooth muscle/pericyte differentiation. Stem Cells Dev 13: 509-520, 2004.
20. Enge M, Bjarnegard M, Gerhardt H, Gustafsson E, Kalen M, Asker N, Hammes HP, Shani M, Fassler R, Betsholtz C. Endothelium-specific platelet-derived growth factor-B ablation mimics diabetic retinopathy. EMBO J 21: 4307-4316, 2002.
21. Engel L, Ryan U. TGF-beta 1 reverses PDGF-stimulated migration of human aortic smooth muscle cells in vitro. In Vitro Cell Dev Biol Anim 33: 443-451, 1997.
22. Fontenay M, Bryckaert M, Tobelem G. Transforming growth factorbeta 1 inhibitory effect of platelet-derived growth factor-induced signal transduction on human bone marrow fibroblasts: possible involvement of protein phosphatases. J Cell Physiol 152: 507-519, 1992.
23. Gariano RF, Gardner TW. Retinal angiogenesis in development and disease. Nature 438: 960-966, 2005.
24. Gerhardt H, Betsholtz C. Endothelial-pericyte interactions in angiogenesis. Cell Tissue Res 314: 15-23, 2003.
25. Ghosh Choudhury G, Kim YS, Simon M, Wozney J, Harris S, Ghosh-Choudhury N, Abboud HE. Bone morphogenetic protein 2 inhibits platelet-derived growth factor-induced c-fos gene transcription and DNA synthesis in mesangial cells. Involvement of mitogen-activated protein kinase. J Biol Chem 274: 10897-10902, 1999.
26. Gines P, Li X, Zamarripa JL, Brown SE, Wieder ED, Nakamura T, Guzelian PS, Schrier RW, Heasley LE, Nemenoff RA. Tyrosine kinase growth factor receptors but not seven-membrane-spanning receptors or phorbol esters activate mitogen-activated protein kinase in rat hepatocytes. Hepatology 22: 1296-1303, 1995.
27. Gingras D, Page M, Annabi B, Beliveau R. Rapid activation of matrix metalloproteinase-2 by glioma cells occurs through a posttranslational MT1-MMP-dependent mechanism. Biochim Biophys Acta 1497: 341-350, 2000.
28. Gohongi T, Fukumura D, Boucher Y, Yun CO, Soff GA, Compton C, Todoroki T, Jain RK. Tumor-host interactions in the gallbladder suppress distal angiogenesis and tumor growth: involvement of transforming growth factor beta1. Nat Med 5: 1203-1208, 1999.
29. Heldin CH, Ostman A, Ronnstrand L. Signal transduction via plateletderived growth factor receptors. Biochim Biophys Acta 1378: F79-113, 1998.
30. Heldin CH, Westermark B. Mechanism of action and in vivo role of platelet-derived growth factor. Physiol Rev 79: 1283-1316, 1999.
31. Hellstrom M, Gerhardt H, Kalen M, Li X, Eriksson U, Wolburg H, Betsholtz C. Lack of pericytes leads to endothelial hyperplasia and abnormal vascular morphogenesis. J Cell Biol 153: 543-553, 2001.
32. Hellstrom M, Kalen M, Lindahl P, Abramsson A, Betsholtz C. Role of PDGF-B and PDGFR-beta in recruitment of vascular smooth muscle cells and pericytes during embryonic blood vessel formation in the mouse. Development 126: 3047-3055, 1999.
33. Hirschi KK, Rohovsky SA, Beck LH, Smith SR, D'Amore PA. Endothelial cells modulate the proliferation of mural cell precursors via plateletderived growth factor-BB and heterotypic cell contact. Circ Res 84: 298-305, 1999.
34. Hirschi KK, Rohovsky SA, D'Amore PA. PDGF, TGF-beta, and heterotypic cell-cell interactions mediate endothelial cell-induced recruitment of 10T1/2 cells and their differentiation to a smooth muscle fate. J Cell Biol 141: 805-814, 1998.
35. Hung LM, Tsai CH, Chen JK. TGF-beta1 selectively suppresses PDGF receptor signaling pathways in MG-63 human osteosarcoma cell. Life Sci 61: 685-693, 1997.
36. Hwang DL, Latus LJ, and Lev-Ran A. Effects of platelet-contained growth factors (PDGF, EGF, IGF-I, and TGF-beta) on DNA synthesis in porcine aortic smooth muscle cells in culture. Exp Cell Res 200: 358-360, 1992.
37. Itoh F, Asao H, Sugamura K, Heldin CH, ten Dijke P, Itoh S. Promoting bone morphogenetic protein signaling through negative regulation of inhibitory Smads. EMBO J 20: 4132-4142, 2001.
38. Itoh T, Tanioka M, Yoshida H, Yoshioka T, Nishimoto H, Itohara S. Reduced angiogenesis and tumor progression in gelatinase A-deficient mice. Cancer Res 58: 1048-1051, 1998.
39. Jain RK. Molecular regulation of vessel maturation. Nat Med 9: 685-693, 2003.
40. Janat MF, Liau G. Transforming growth factor beta 1 is a powerful modulator of platelet-derived growth factor action in vascular smooth muscle cells. J Cell Physiol 150: 232-242, 1992.
41. Jonk LJ, Itoh S, Heldin CH, ten Dijke P, Kruijer W. Identification and functional characterization of a Smad binding element (SBE) in the JunB promoter that acts as a transforming growth factor-beta, activin, and bone morphogenetic protein-inducible enhancer. J Biol Chem 273: 21145-21152, 1998.
42. Kim TS, Kim YB. Correlation between expression of matrix metalloproteinase-2 (MMP-2), and matrix metalloproteinase-9 (MMP-9) and angiogenesis in colorectal adenocarcinoma. J Korean Med Sci 14: 263-270, 1999.
43. Ko FN, Yang YC, Huang SC, Ou JT. Coagulation factor Xa stimulates platelet-derived growth factor release and mitogenesis in cultured vascular smooth muscle cells of rat. J Clin Invest 98: 1493-1501, 1996.
44. Korchynskyi O, ten Dijke P. Identification and functional characterization of distinct critically important bone morphogenetic protein-specific response elements in the Id1 promoter. J Biol Chem 277: 4883-4891, 2002.
45. Kuzuya M, Nakamura K, Sasaki T, Cheng XW, Itohara S, Iguchi A. Effect of MMP-2 deficiency on atherosclerotic lesion formation in apoEdeficient mice. Arterioscler Thromb Vasc Biol 26: 1120-1125, 2006.
46. Lee SJ, Bae SS, Kim KH, Lee WS, Rhim BY, Hong KW, Kim CD. High glucose enhances MMP-2 production in adventitial fibroblasts via Akt1-dependent NF-kappaB pathway. FEBS Lett 581: 4189-4194, 2007.
47. Li DY, Sorensen LK, Brooke BS, Urness LD, Davis EC, Taylor DG, Boak BB, Wendel DP. Defective angiogenesis in mice lacking endoglin. Science 284: 1534-1537, 1999.
48. Liao J, Wolfman JC, Wolfman A. K-ras regulates the steady-state expression of matrix metalloproteinase 2 in fibroblasts. J Biol Chem 278: 31871-31878, 2003.
49. Mack CP, Somlyo AV, Hautmann M, Somlyo AP, Owens GK. Smooth muscle differentiation marker gene expression is regulated by RhoAmediated actin polymerization. J Biol Chem 276: 341-347, 2001.
50. Majack RA. Beta-type transforming growth factor specifies organizational behavior in vascular smooth muscle cell cultures. J Cell Biol 105: 465-471, 1987.
51. Majack RA, Majesky MW, Goodman LV. Role of PDGF-A expression in the control of vascular smooth muscle cell growth by transforming growth factor-beta. J Cell Biol 111: 239-247, 1990.
52. Mii S, Ware JA, Kent KC. Transforming growth factor-beta inhibits human vascular smooth muscle cell growth and migration. Surgery 114: 464-470, 1993.
53. Miralles F, Posern G, Zaromytidou AI, Treisman R. Actin dynamics control SRF activity by regulation of its coactivator MAL. Cell 113: 329-342, 2003.
54. Morisaki N, Kawano M, Koyama N, Koshikawa T, Umemiya K, Saito Y, Yoshida S. Effects of transforming growth factor-beta 1 on growth of aortic smooth muscle cells. Influences of interaction with growth factors, cell state, cell phenotype, and cell cycle. Atherosclerosis 88: 227-234, 1991.
55. Nishio E, Watanabe Y. Transforming growth factor beta is a modulator of platelet-derived growth factor action in vascular smooth muscle cells: a possible role for catalase activity and glutathione peroxidase activity. Biochem Biophys Res Commun 232: 1-4, 1997.
56. Ohno-Matsui K, Uetama T, Yoshida T, Hayano M, Itoh T, Morita I, Mochizuki M. Reduced retinal angiogenesis in MMP-2-deficient mice. Invest Ophthalmol Vis Sci 44: 5370-5375, 2003.
57. Owens GK. Regulation of differentiation of vascular smooth muscle cells. Physiol Rev 75: 487-517, 1995.
58. Owens GK, Kumar MS, Wamhoff BR. Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol Rev 84: 767-801, 2004.
59. Pan D, Yang J, Lu F, Xu D, Zhou L, Shi A, Cao K. Platelet-derived growth factor BB modulates PCNA protein synthesis partially through the transforming growth factor beta signalling pathway in vascular smooth muscle cells. Biochem Cell Biol 85: 606-615, 2007.
60. Pauly RR, Passaniti A, Bilato C, Monticone R, Cheng L, Papadopoulos N, Gluzband YA, Smith L, Weinstein C, Lakatta EG, and et al. Migration of cultured vascular smooth muscle cells through a basement membrane barrier requires type IV collagenase activity and is inhibited by cellular differentiation. Circ Res 75: 41-54, 1994.
61. Phelps ED, Updike DL, Bullen EC, Grammas P, Howard EW. Transcriptional and posttranscriptional regulation of angiopoietin-2 expression mediated by IGF and PDGF in vascular smooth muscle cells. Am J Physiol Cell Physiol 290: C352-C361, 2006.
62. Quarck R, Berrou E, Magnier C, Bobe R, Bredoux R, Tobelem G, Enouf J, Bryckaert M. Differential up-regulation of Rap1a and Rap1b proteins during smooth muscle cell cycle. Eur J Cell Biol 70: 269-277, 1996.
63. Ribatti D, Nico B, Vacca A, Iurlaro M, Roncali L. Temporal expression of the matrix metalloproteinase MMP-2 correlates with fibronectin immunoreactivity during the development of the vascular system in the chick embryo chorioallantoic membrane. J Anat 195: 39-44, 1999.
64. Risinger GM Jr, Hunt TS, Updike DL, Bullen EC, and Howard EW. Matrix metalloproteinase-2 expression by vascular smooth muscle cells is mediated by both stimulatory and inhibitory signals in response to growth factors. J Cell Biol 281: 25915-25925, 2006.
65. Saltis J, Agrotis A, Bobik A. Differential regulation by transforming growth factor-beta 1 of platelet-derived growth factor-stimulated proliferation of vascular smooth muscle cells from SHR and WKY rats. Clin Exp Pharmacol Physiol 19: 396-399, 1992.
66. Saltis J, Bobik A. Developmental regulation of transforming growth factor-beta 1 responses and vascular smooth muscle growth in spontaneously hypertensive rats. J Hypertens 13: 1441-1448, 1995.
67. Samolov B, Steen B, Seregard S, van der Ploeg I, Montan P, Kvanta A. Delayed inflammation-associated corneal neovascularization in MMP-2-deficient mice. Exp Eye Res 80: 159-166, 2005.
68. Sanka K, Maddala R, Epstein DL, Rao PV. Influence of actin cytoskeletal integrity on matrix metalloproteinase-2 activation in cultured human trabecular meshwork cells. Invest Ophthalmol Vis Sci 48: 2105-2114, 2007.
69. Seifert RA, Coats SA, Raines EW, Ross R, and Bowen-Pope DF. Platelet-derived growth factor (PDGF) receptor alpha-subunit mutant and reconstituted cell lines demonstrate that transforming growth factor-beta can be mitogenic through PDGF A-chain-dependent and -independent pathways. J Cell Biol 269: 13951-13955, 1994.
70. Staus DP, Blaker AL, Taylor JM, Mack CP. Diaphanous 1 and 2 regulate smooth muscle cell differentiation by activating the myocardinrelated transcription factors. Arterioscler Thromb Vasc Biol 27: 478-486, 2007.
71. Tomasek JJ, Halliday NL, Updike DL, Ahern-Moore JS, Vu TK, Liu RW, Howard EW. Gelatinase A activation is regulated by the organization of the polymerized actin cytoskeleton. J Cell Biol 272: 7482-7487, 1997.
72. Turner NA, Hall KT, Ball SG, Porter KE. Selective gene silencing of either MMP-2 or MMP-9 inhibits invasion of human saphenous vein smooth muscle cells. Atherosclerosis 193: 36-43, 2007.
73. Tziakas DN, Lazarides MK, Tentes IK, Georgiadis GS, Eleftheriadou E, Chalikias GK, Kortsaris A, Hatseras DI. Gelatinases [matrix metalloproteinase-2 (MMP-2) and MMP-9] induce carotid plaque instability but their systemic levels are not predictive of local events. Ann Vasc Surg 19: 529-533, 2005.
74. Uzui H, Lee JD, Shimizu H, Tsutani H, Ueda T. The role of proteintyrosine phosphorylation and gelatinase production in the migration and proliferation of smooth muscle cells. Atherosclerosis 149: 51-59, 2000.
75. Van Obberghen-Schilling E, Roche NS, Flanders KC, Sporn MB, Roberts AB. Transforming growth factor beta 1 positively regulates its own expression in normal and transformed cells. J Cell Biol 263: 7741-7746, 1988.
76. Vartiainen MK, Guettler S, Larijani B, Treisman R. Nuclear actin regulates dynamic subcellular localization and activity of the SRF cofactor MAL. Science 316: 1749-1752, 2007.
77. Villiger PM, Lotz M. Differential expression of TGF beta isoforms by human articular chondrocytes in response to growth factors. J Cell Physiol 151: 318-325, 1992.
78. Wang DZ, Olson EN. Control of smooth muscle development by the myocardin family of transcriptional coactivators. Curr Opin Genet Dev 14: 558-566, 2004.
79. Wipff PJ, Rifkin DB, Meister JJ, Hinz B. Myofibroblast contraction activates latent TGF-beta1 from the extracellular matrix. J Cell Biol 179: 1311-1323, 2007.
80. Wrenn RW, Raeuber CL, Herman LE, Walton WJ, Rosenquist TH. Transforming growth factor-beta: signal transduction via protein kinase C in cultured embryonic vascular smooth muscle cells. In Vitro Cell Dev Biol 29A: 73-78, 1993.
81. Zempo N, Kenagy RD, Au YP, Bendeck M, Clowes MM, Reidy MA, Clowes AW. Matrix metalloproteinases of vascular wall cells are increased in balloon-injured rat carotid artery. J Vasc Surg 20: 209-217, 1994.
82. Zhan Y, Kim S, Izumi Y, Izumiya Y, Nakao T, Miyazaki H, Iwao H. Role of JNK, p38, and ERK in platelet-derived growth factor-induced vascular proliferation, migration, and gene expression. Arterioscler Thromb Vasc Biol 23: 795-801, 2003.
83. Zhou Z, Apte SS, Soininen R, Cao R, Baaklini GY, Rauser RW, Wang J, Cao Y, Tryggvason K. Impaired endochondral ossification and angiogenesis in mice deficient in membrane-type matrix metalloproteinase I. Proc Natl Acad Sci USA 97: 4052-4057, 2000.