Platelet-derived growth factor-BB and Ets-1 transcription factor negatively regulate transcription of multiple smooth muscle cell differentiation marker genes

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 286, Issue 6 55-6, 2004, Pages

  Dandré, Frédéric ^a   Owens, Gary K ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Cell density; Promoter; Signaling; Vascular injury

Indexed keywords

6,7 DIMETHYL 2 PHENYLQUINOXALINE; ALPHA ACTIN; MYOSIN HEAVY CHAIN; ORTHOVANADIC ACID; PLATELET DERIVED GROWTH FACTOR BB; PROTEIN C FOS; PROTEIN SM22ALPHA; RECOMBINANT PLATELET DERIVED GROWTH FACTOR BB; TRANSCRIPTION FACTOR ETS 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL INJURY; CELL DENSITY; CELL DIFFERENTIATION; CELL SPECIFICITY; CONTROLLED STUDY; ENZYME INHIBITION; ENZYME MECHANISM; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; GENETIC TRANSFECTION; MARKER GENE; MESENCHYME CELL; MITOGENESIS; MOLECULAR CLONING; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS; RAT; REGULATORY MECHANISM; REPRESSOR GENE; SMOOTH MUSCLE FIBER; TRANSCRIPTION REGULATION;

ACTINS; ANIMALS; ANTICOAGULANTS; AORTA, THORACIC; BIOLOGICAL MARKERS; CELL COUNT; CELL DIFFERENTIATION; CELLS, CULTURED; LUCIFERASES; MICROFILAMENT PROTEINS; MUSCLE PROTEINS; MUSCLE, SMOOTH, VASCULAR; MYOSIN HEAVY CHAINS; PLATELET-DERIVED GROWTH FACTOR; PROMOTER REGIONS (GENETICS); PROTO-ONCOGENE PROTEIN C-ETS-1; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-ETS; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; UP-REGULATION;

EID: 2542469732     PISSN: 03636135     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpheart.00625.2003     Document Type: Article

References (60)

1. Adam PJ, Regan CP, Hautmann MB, and Owens GK. Positive- and negative-acting Kruppel-like transcription factors bind a transforming growth factor-β control element required for expression of the smooth muscle cell differentiation marker SM22α in vivo. J Biol Chem 275: 37798-37806, 2000.
2. Banal S, Wolf Y, Golomb G, Pearle A, Waltenberger J, Fishbein I, Schneider A, Gazit A, Perez L, Huber R, Lazarovichi G, Rabinovich L, Levitzki A, and Gertz SD. PDGF-receptor tyrosine kinase blocker AG1295 selectively attenuates smooth muscle cell growth in vitro and reduces neointimal formation after balloon angioplasty in swine. Circulation 97: 1960-1969, 1998.
3. Bendeck MP, Zempo N, Clowes AW, Galardy RE, and Reidy MA. Smooth muscle cell migration and matrix metalloproteinase expression after arterial injury in the rat. Circ Res 75: 539-545, 1994.
4. Blank RS and 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.
5. Blank RS, Thompson MM, and Owens GK. Cell cycle versus density dependence of smooth muscle α-actin expression in cultured rat aortic smooth muscle cells. J Cell Biol 107: 299-306, 1988.
6. Bochaton-Piallat ML, Ropraz P, Gabbiani F, and Gabbiani G. Phenotypic heterogeneity of rat arterial smooth muscle cell clones. Implications for the development of experimental intimal thickening. Arterioscler Thromb Vasc Biol 16: 815-820, 1996.
7. Corjay MH, Blank RS, and Owens GK. Platelet-derived growth factor-induced destabilization of smooth muscle α-actin mRNA. J Cell Physiol 145: 391-397, 1990.
8. Corjay MH, Thompson MM, Lynch KR, and Owens GK. Differential effect of platelet-derived growth factor-versus serum-induced growth on smooth muscle α-actin and non-muscle β-actin mRNA expression in cultured rat aortic smooth muscle cells. J Biol Chem 264: 10501-10506, 1989.
9. Ferns GA, Raines EW, Sprugel KH, Motani AS, Reidy MA, and Ross R. Inhibition of neointimal smooth muscle accumulation after angioplasty by an antibody to PDGF. Science 253: 1129-1132, 1991.
10. Gilman MZ, Wilson RN, and Weinberg RA. Multiple protein-binding sites in the 5′-flanking region regulate c-fos expression. Mol Cell Biol 6: 4305-4316, 1986.
11. Goetze S, Kintscher U, Kaneshiro K, Meehan WP, Collins A, Fleck E, Hsueh WA, and Law RE. TNFα induces expression of transcription factors c-fos, Egr-1, and Ets-1 in vascular lesions through extracellular signal-regulated kinases 1/2. Atherosclerosis 159: 93-101, 2001.
12. Hautmann MB, Adam PJ, and Owens GK. Similarities and differences in smooth muscle α-actin induction by TGF-β in smooth muscle versus non-smooth muscle cells. Arterioscler Thromb Vasc Biol 19: 2049-2058, 1999.
13. Hayashi K, Takahashi M, Kimura K, Nishida W, Saga H, and Sobue K. Changes in the balance of phosphoinositide 3-kinase/protein kinase B (Akt) and the mitogen-activated protein kinases (ERK/p38MAPK) determine a phenotype of visceral and vascular smooth muscle cells. J Cell Biol 145: 727-740, 1999.
14. Heldin CH and Westermark B. Mechanism of action and in vivo role of platelet-derived growth factor. Physiol Rev 79: 1283-1316, 1999.
15. Holycross BJ, Blank RS, Thompson MM, Peach MJ, and Owens GK. Platelet-derived growth factor-BB-induced suppression of smooth muscle cell differentiation. Circ Res 71: 1525-1532, 1992.
16. Hultgardh-Nilsson A, Cercek B, Wang JW, Naito S, Lovdahl C, Sharifi B, Forrester JS, and Fagin JA. Regulated expression of the Ets-1 transcription factor in vascular smooth muscle cells in vivo and in vitro. Circ Res 78: 589-595, 1996.
17. Kim S, Ip HS, Lu MM, Clendenin C, and Parmacek MS. A serum response factor-dependent transcriptional regulatory program identifies distinct smooth muscle cell sublineages. Mol Cell Biol 17: 2266-2278, 1997.
18. Kitange G, Shibata S, Tokunaga Y, Yagi N, Yasunaga A, Kishikawa M, and Naito S. Ets-1 transcription factor-mediated urokinase-type plasminogen activator expression and invasion in glioma cells stimulated by serum and basic fibroblast growth factors. Lab Invest 79: 407-416, 1999.
19. Ko JH, Miyoshi E, Noda K, Ekuni A, Kang R, Ikeda Y, and Taniguchi N. Regulation of the GnT-V promoter by transcription factor Ets-1 in various cancer cell lines. J Biol Chem 274: 22941-22948, 1999.
20. Kocher O, Gabbiani F, Gabbiani G, Reidy MA, Cokay MS, Peters H, and Huttner I. Phenotypic features of smooth muscle cells during the evolution of experimental carotid artery intimal thickening. Biochemical and morphologic studies. Lab Invest 65: 459-470, 1991.
21. Kovalenko M, Gazit A, Bohmer A, Rorsman C, Ronnstrand L, Heldin CH, Waltenberger J, Bohmer FD, and Levitzki A. Selective platelet-derived growth factor receptor kinase blockers reverse cis-transformation. Cancer Res 54: 6106-6114, 1994.
22. Kumar MS and Owens GK. Combinatorial control of smooth muscle-specific gene expression. Arterioscler Thromb Vasc Biol 23: 737-747, 2003.
23. Kusuoka H and Hoffman JI. Advice on statistical analysis for circulation research. Circ Res 91: 662-671, 2002.
24. Layne MD, Endege WO, Jain MK, Yet SF, Hsieh CM, Chin MT, Perrella MA, Blanar MA, Haber E, and Lee ME. Aortic carboxypeptidase-like protein, a novel protein with discoidin and carboxypeptidase-like domains, is up-regulated during vascular smooth muscle cell differentiation. J Biol Chem 273: 15654-15660, 1998.
25. Layne MD, Yet SF, Maemura K, Hsieh CM, Liu X, Ith B, Lee ME, and Perrella MA. Characterization of the mouse aortic carboxypeptidase-like protein promoter reveals activity in differentiated and dedifferentiated vascular smooth muscle cells. Circ Res 90: 728-736, 2002.
26. Leveen P, Pekny M, Gebre-Medhin S, Swolin B, Larsson E, and Betsholtz C. Mice deficient for PDGF B show renal, cardiovascular, and hematological abnormalities. Genes Dev 8: 1875-1887, 1994.
27. Li L, Miano JM, Mercer B, and Olson EN. Expression of the SM22α promoter in transgenic mice provides evidence for distinct transcriptional regulatory programs in vascular and visceral smooth muscle cells. J Cell Biol 132: 849-859, 1996.
28. Lu J, Landerholm TE, Wei JS, Dong XR, Wu SP, Liu X, Nagata K, Inagaki M, and Majesky MW. Coronary smooth muscle differentiation from proepicardial cells requires RhoA-mediated actin reorganization and p 160 Rho-kinase activity. Dev Biol 240: 404-418, 2001.
29. Mack CP and Owens GK. Regulation of smooth muscle α-actin expression in vivo is dependent on CArG elements within the 5′ and first intron promoter regions. Circ Res 84: 852-861, 1999.
30. Mack CP, Thompson MM, Lawrenz-Smith S, and Owens GK. Smooth muscle α-actin CArG elements coordinate formation of a smooth muscle cell-selective, serum response factor-containing activation complex. Circ Res 86: 221-232, 2000.
31. Madsen CS, Regan CP, Hungerford JE, White SL, Manabe I, and Owens GK. Smooth muscle-specific expression of the smooth muscle myosin heavy chain gene in transgenic mice requires 5′-flanking and first intronic DNA sequence. Circ Res 82: 908-917, 1998.
32. Majesky MW, Reidy MA, Bowen-Pope DF, Hart CE, Wilcox JN, and Schwartz SM. PDGF ligand and receptor gene expression during repair of arterial injury. J Cell Biol 111: 2149-2158, 1990.
33. Manabe I and Owens GK. CArG elements control smooth muscle subtype-specific expression of smooth muscle myosin in vivo. J Clin Invest 107: 823-834, 2001.
34. Muthusamy N, Barton K, and Leiden JM. Defective activation and survival of T cells lacking the Ets-1 transcription factor. Nature 377: 639-642, 1995.
35. Naito S, Shimizu S, Maeda S, Wang J, Paul R, and Fagin JA. Ets-1 is an early response gene activated by ET-1 and PDGF-BB in vascular smooth muscle cells. Am J Physiol Cell Physiol 274: C472-C480, 1998.
36. Niwa H, Yamamura K, and Miyazaki J. Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108: 193-199, 1991.
37. Nye JA, Petersen JM, Gunther CV, Jonsen MD, and Graves BJ. Interaction of murine Ets-1 with GGA-binding sites establishes the ETS domain as a new DNA-binding motif. Genes Dev 6: 975-990, 1992.
38. Owens GK. Molecular control of vascular smooth muscle cell differentiation. Acta Physiol Scand 164: 623-635, 1998.
39. Owens GK, Loeb A, Gordon D, and Thompson MM. Expression of smooth muscle-specific α-isoactin in cultured vascular smooth muscle cells: relationship between growth and cytodifferentiation. J Cell Biol 102: 343-352, 1986.
40. Pallen CJ and Tong PH. Elevation of membrane tyrosine phosphatase activity in density-dependent growth-arrested fibroblasts. Proc Natl Acad Sci USA 88: 6996-7000, 1991.
41. Ranganna K and Yatsu FM. Inhibition of platelet-derived growth factor BB-induced expression of glyceraldehyde-3-phosphate dehydrogenase by sodium butyrate in rat vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 17: 3420-3427, 1997.
42. Regan CP, Adam PJ, Madsen CS, and Owens GK. Molecular mechanisms of decreased smooth muscle differentiation marker expression after vascular injury. J Clin Invest 106: 1139-1147, 2000.
43. Regan CP, Manabe I, and Owens GK. Development of a smooth muscle-targeted Cre recombinase mouse reveals novel insights regarding smooth muscle myosin heavy chain promoter regulation. Circ Res 87: 363-369, 2000.
44. Reusch HP, Zimmermann S, Schaefer M, Paul M, and Moelling K. Regulation of Raf by Akt controls growth and differentiation in vascular smooth muscle cells. J Biol Chem 276: 33630-33637, 2001.
45. Reusch P, Wagdy H, Reusch R, Wilson E, and Ives HE. Mechanical strain increases smooth muscle and decreases nonmuscle myosin expression in rat vascular smooth muscle cells. Circ Res 79: 1046-1053, 1996.
46. Ross R. The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature 362: 801-809, 1993.
47. Ross R, Masuda J, Raines EW, Gown AM, Katsuda S, Sasahara M, Malden LT, Masuko H, and Sato H. Localization of PDGF-B protein in macrophages in all phases of atherogenesis. Science 248: 1009-1012, 1990.
48. Saito Y, Haendeler J, Hojo Y, Yamamoto K, and Berk BC. Receptor heterodimerization: essential mechanism for platelet-derived growth factor-induced epidermal growth factor receptor transactivation. Mol Cell Biol 21: 6387-6394, 2001.
49. Salhany KE, Robinson-Benion C, Candia AF, Pledger WJ, and Holt JT. Differential induction of the c-fos promoter through distinct PDGF receptor-mediated signaling pathways. J Cell Physiol 150: 386-395, 1992.
50. Sano H, Sudo T, Yokode M, Murayama T, Kataoka H, Takakura N, Nishikawa S, Nishikawa SI, and Kita T. Functional blockade of platelet-derived growth factor receptor-β but not of receptor-α prevents vascular smooth muscle cell accumulation in fibrous cap lesions in apolipoprotein E-deficient mice. Circulation 103: 2955-2960, 2001.
51. Sato Y, Teruyama K, Nakano T, Oda N, Abe M, Tanaka K, and Iwasaka-Yagi C. Role of transcription factors in angiogenesis: Ets-1 promotes angiogenesis as well as endothelial apoptosis. Ann NY Acad Sci 947: 117-123, 2001.
52. Shimizu RT, Blank RS, Jervis R, Lawrenz-Smith SC, and Owens GK. The smooth muscle α-actin gene promoter is differentially regulated in smooth muscle versus non-smooth muscle cells. J Biol Chem 270: 7631-7643, 1995.
53. Shinbrot E, Peters KG, and Williams LT. Expression of the platelet-derived growth factor-β receptor during organogenesis and tissue differentiation in the mouse embryo. Dev Dyn 199: 169-175, 1994.
54. Somasundaram C, Kallmeier RC, and Babij P. Regulation of smooth muscle myosin heavy chain gene expression in cultured vascular smooth muscle cells by growth factors and contractile agonists. Basic Appl Myol 6: 31-36, 1996.
55. Sorby M and Ostman A. Protein-tyrosine phosphatase-mediated decrease of epidermal growth factor and platelet-derived growth factor receptor tyrosine phosphorylation in high cell density cultures. J Biol Chem 271: 10963-10966, 1996.
56. Soriano P. Abnormal kidney development and hematological disorders in PDGF β-receptor mutant mice. Genes Dev 8: 1888-1896, 1994.
57. Uchida K, Sasahara M, Morigami N, Hazama F, and Kinoshita M. Expression of platelet-derived growth factor-B chain in neointimal smooth muscle cells of balloon-injured rabbit femoral arteries. Atherosclerosis 124: 9-23, 1996.
58. Van Putten V, Li X, Maselli J, and Nemenoff RA. Regulation of smooth muscle α-actin promoter by vasopressin and platelet-derived growth factor in rat aortic vascular smooth muscle cells. Circ Res 75: 1126-1130, 1994.
59. Wilcox JN, Smith KM, Williams LT, Schwartz SM, and Gordon D. Platelet-derived growth factor mRNA detection in human atherosclerotic plaques by in situ hybridization. J Clin Invest 82: 1134-1143, 1988.
60. Yang JH, Briggs WH, Libby P, and Lee RT. Small mechanical strains selectively suppress matrix metalloproteinase-1 expression by human vascular smooth muscle cells. J Biol Chem 273: 6550-6555, 1998.