Transcriptional regulation of SM22α by Wnt3a: Convergence with TGFβ1/Smad signaling at a novel regulatory element

Journal of Molecular and Cellular Cardiology

Volumn 46, Issue 5, 2009, Pages 621-635

  Shafer, Shawn L ^a   Towler, Dwight A ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

catenin; Msx2; Myofibroblast; Type II diabetes; Vascular calcification; Wnt

Indexed keywords

ANTIBODY; BETA CATENIN; BINDING PROTEIN; BONE MORPHOGENETIC PROTEIN 2; DEOXYRIBONUCLEOPROTEIN; DNA BINDING PROTEIN; HISTONE; HISTONE H3; LUCIFERASE; NUCLEOTIDE; SMAD2 PROTEIN; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA1; TRANSGELIN; WNT3A PROTEIN; ACTIN BINDING PROTEIN; MESSENGER RNA; MUSCLE PROTEIN; SMAD PROTEIN; SMAD2 PROTEIN, MOUSE; SMAD3 PROTEIN, MOUSE; SMALL INTERFERING RNA; TCF7 PROTEIN, MOUSE; TRANSCRIPTION FACTOR 7; WNT PROTEIN; WNT3 PROTEIN;

ACETYLATION; ANIMAL CELL; ARTICLE; BACTERIAL GENE; CHROMATIN IMMUNOPRECIPITATION; DISEASE ASSOCIATION; DNA PROTEIN COMPLEX; DNA TRANSCRIPTION; DRUG BINDING; GEL; GENE; GENETIC TRANSCRIPTION; GENOMICS; MEDIATOR; MESENCHYME CELL; MOLECULAR WEIGHT; MYOFIBROBLAST; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN MOTIF; REGULATORY SEQUENCE; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION REGULATION; ANIMAL; DOMINANT GENE; EXON; GENETICS; MESENCHYMAL STEM CELL; METABOLISM; MOLECULAR GENETICS; MOUSE; RNA INTERFERENCE; SIGNAL TRANSDUCTION; UPREGULATION;

RICE STRIPE VIRUS;

ANIMALS; EXONS; GENES, DOMINANT; LUCIFERASES; MESENCHYMAL STEM CELLS; MICE; MICROFILAMENT PROTEINS; MOLECULAR SEQUENCE DATA; MUSCLE PROTEINS; PROMOTER REGIONS, GENETIC; RNA INTERFERENCE; RNA, MESSENGER; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SMAD PROTEINS; SMAD2 PROTEIN; SMAD3 PROTEIN; T CELL TRANSCRIPTION FACTOR 1; TRANSCRIPTION, GENETIC; TRANSFORMING GROWTH FACTOR BETA1; UP-REGULATION; WNT PROTEINS;

EID: 63349111610     PISSN: 00222828     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2009.01.005     Document Type: Article

References (67)

1. Brohall G., Oden A., and Fagerberg B. Carotid artery intima-media thickness in patients with Type 2 diabetes mellitus and impaired glucose tolerance: a systematic review. Diabet. Med. 23 (2006) 609-616
2. Collett G.D., and Canfield A.E. Angiogenesis and pericytes in the initiation of ectopic calcification. Circ. Res. 96 (2005) 930-938
3. Jaffe I.Z., Tintut Y., Newfell B.G., Demer L.L., and Mendelsohn M.E. Mineralocorticoid receptor activation promotes vascular cell calcification. Arterioscler. Thromb. Vasc. Biol. 27 (2007) 799-805
4. Abedin M., Tintut Y., and Demer L.L. Mesenchymal stem cells and the artery wall. Circ. Res. 95 (2004) 671-676
5. Katz R., Wong N.D., Kronmal R., et al. Features of the metabolic syndrome and diabetes mellitus as predictors of aortic valve calcification in the Multi-Ethnic Study of Atherosclerosis. Circulation 113 (2006) 2113-2119
6. Mozes G., Keresztury G., Kadar A., et al. Atherosclerosis in amputated legs of patients with and without diabetes mellitus. Int. Angiol. 17 (1998) 282-286
7. Guzman R.J., Brinkley D.M., Schumacher P.M., Donahue R.M., Beavers H., and Qin X. Tibial artery calcification as a marker of amputation risk in patients with peripheral arterial disease. J. Am. Coll. Cardiol. 51 (2008) 1967-1974
8. Quasnichka H., Slater S.C., Beeching C.A., Boehm M., Sala-Newby G.B., and George S.J. Regulation of smooth muscle cell proliferation by beta-catenin/T-cell factor signaling involves modulation of cyclin D1 and p21 expression. Circ. Res. 99 (2006) 1329-1337
9. Kirton J.P., Crofts N.J., George S.J., Brennan K., and Canfield A.E. Wnt/beta-catenin signaling stimulates chondrogenic and inhibits adipogenic differentiation of pericytes: potential relevance to vascular disease?. Circ. Res. 101 (2007) 581-589
10. Shao J.S., Cai J., and Towler D.A. Molecular mechanisms of vascular calcification: lessons learned from the aorta. Arterioscler. Thromb. Vasc. Biol. 26 (2006) 1423-1430
11. Kalajzic Z., Li H., Wang L.P., et al. Use of an alpha-smooth muscle actin GFP reporter to identify an osteoprogenitor population. Bone 43 (2008) 501-510
12. Kalajzic I., Kalajzic Z., Wang L., et al. Pericyte/myofibroblast phenotype of osteoprogenitor cell. J. Musculoskelet. Neuronal. Interact. 7 (2007) 320-322
13. Hoppler S., and Kavanagh C.L. Wnt signalling: variety at the core. J. Cell. Sci. 120 (2007) 385-393
14. Shao J.S., Cheng S.L., Pingsterhaus J.M., Charlton-Kachigian N., Loewy A.P., and Towler D.A. Msx2 promotes cardiovascular calcification by activating paracrine Wnt signals. J. Clin. Invest. 115 (2005) 1210-1220
15. Al-Aly Z., Shao J.S., Lai C.F., et al. Aortic Msx2-Wnt calcification cascade is regulated by TNF-alpha-dependent signals in diabetic Ldlr-/-mice. Arterioscler. Thromb. Vasc. Biol. 27 (2007) 2589-2596
16. Goodwin A.M., Sullivan K.M., and D'Amore P.A. Cultured endothelial cells display endogenous activation of the canonical Wnt signaling pathway and express multiple ligands, receptors, and secreted modulators of Wnt signaling. Dev. Dyn. 235 (2006) 3110-3120
17. Satokata I., Ma L., Ohshima H., et al. Msx2 deficiency in mice causes pleiotropic defects in bone growth and ectodermal organ formation. Nat. Genet. 24 (2000) 391-395
18. Cheng S.L., Shao J.S., Charlton-Kachigian N., Loewy A.P., and Towler D.A. MSX2 promotes osteogenesis and suppresses adipogenic differentiation of multipotent mesenchymal progenitors. J. Biol. Chem. 278 (2003) 45969-45977
19. Hayashi K., Nakamura S., Nishida W., and Sobue K. Bone morphogenetic protein-induced MSX1 and MSX2 inhibit myocardin-dependent smooth muscle gene transcription. Mol. Cell. Biol. 26 (2006) 9456-9470
20. Cheng S.L., Shao J.S., Cai J., Sierra O.L., and Towler D.A. Msx2 exerts bone anabolism via canonical Wnt signaling. J. Biol. Chem. 283 (2008) 20505-20522
21. Lai C.F., Seshadri V., Huang K., et al. An osteopontin-NADPH oxidase signaling cascade promotes pro-matrix metalloproteinase 9 activation in aortic mesenchymal cells. Circ. Res. 98 (2006) 1479-1489
22. Bidder M., Shao J.S., Charlton-Kachigian N., Loewy A.P., Semenkovich C.F., and Towler D.A. Osteopontin transcription in aortic vascular smooth muscle cells is controlled by glucose-regulated upstream stimulatory factor and activator protein-1 activities. J. Biol. Chem. 277 (2002) 44485-44496
23. Newberry E.P., Latifi T., Battaile J.T., and Towler D.A. Structure-function analysis of Msx2-mediated transcriptional suppression. Biochemistry 36 (1997) 10451-10462
24. Sierra O.L., Cheng S.L., Loewy A.P., Charlton-Kachigian N., and Towler D.A. MINT, the Msx2 interacting nuclear matrix target, enhances Runx2-dependent activation of the osteocalcin fibroblast growth factor response element. J. Biol. Chem. 279 (2004) 32913-32923
25. Towler D.A., Bennett C.D., and Rodan G.A. Activity of the rat osteocalcin basal promoter in osteoblastic cells is dependent upon homeodomain and CP1 binding motifs. Mol. Endocrinol. 8 (1994) 614-624
26. Nelson J.D., Denisenko O., and Bomsztyk K. Protocol for the fast chromatin immunoprecipitation (ChIP) method. Nat. Protoc. 1 (2006) 179-185
27. Nelson J.D., Denisenko O., Sova P., and Bomsztyk K. Fast chromatin immunoprecipitation assay. Nucleic Acids Res. 34 (2006) e2
28. Solway J., Seltzer J., Samaha F.F., et al. Structure and expression of a smooth muscle cell-specific gene, SM22 alpha. J. Biol. Chem. 270 (1995) 13460-13469
29. Li L., Miano J.M., Cserjesi P., and Olson E.N. SM22 alpha, a marker of adult smooth muscle, is expressed in multiple myogenic lineages during embryogenesis. Circ. Res. 78 (1996) 188-195
30. Caverzasio J., and Manen D. Essential role of Wnt3a-mediated activation of mitogen-activated protein kinase p38 for the stimulation of alkaline phosphatase activity and matrix mineralization in C3H10T1/2 mesenchymal cells. Endocrinology 148 (2007) 5323-5330
31. Hirschi K.K., Rohovsky S.A., and D'Amore P.A. 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 (1998) 805-814
32. Kale S., Hanai J., Chan B., et al. Microarray analysis of in vitro pericyte differentiation reveals an angiogenic program of gene expression. Faseb J. 19 (2005) 270-271
33. Tomasek J.J., Gabbiani G., Hinz B., Chaponnier C., and Brown R.A. Myofibroblasts and mechano-regulation of connective tissue remodelling. Nat. Rev., Mol. Cell Biol. 3 (2002) 349-363
34. Yoshida T., and Owens G.K. Molecular determinants of vascular smooth muscle cell diversity. Circ. Res. 96 (2005) 280-291
35. Qiu P., Feng X.H., and Li L. Interaction of Smad3 and SRF-associated complex mediates TGF-beta1 signals to regulate SM22 transcription during myofibroblast differentiation. J. Mol. Cell. Cardiol. 35 (2003) 1407-1420
36. Faggin E., Puato M., Zardo L., et al. Smooth muscle-specific SM22 protein is expressed in the adventitial cells of balloon-injured rabbit carotid artery. Arterioscler Thromb Vasc Biol 19 (1999) 1393-1404
37. Kennard S., Liu H., and Lilly B. Transforming growth factor-beta (TGF-1) down-regulates Notch3 in fibroblasts to promote smooth muscle gene expression. J. Biol. Chem. 283 (2008) 1324-1333
38. Qiu P., Ritchie R.P., Gong X.Q., Hamamori Y., and Li L. Dynamic changes in chromatin acetylation and the expression of histone acetyltransferases and histone deacetylases regulate the SM22alpha transcription in response to Smad3-mediated TGFbeta1 signaling. Biochem. Biophys. Res. Commun. 348 (2006) 351-358
39. Owens G.K., Kumar M.S., and Wamhoff B.R. Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol. Rev. 84 (2004) 767-801
40. Brunelli S., and Cossu G. A role for MSX2 and necdin in smooth muscle differentiation of mesoangioblasts and other mesoderm progenitor cells. Trends Cardiovasc. Med. 15 (2005) 96-100
41. Ding R., Darland D.C., Parmacek M.S., and D'Amore P.A. Endothelial-mesenchymal interactions in vitro reveal molecular mechanisms of smooth muscle/pericyte differentiation. Stem Cells Dev. 13 (2004) 509-520
42. Gaur T., Lengner C.J., Hovhannisyan H., et al. Canonical WNT signaling promotes osteogenesis by directly stimulating Runx2 gene expression. J. Biol. Chem. 280 (2005) 33132-33140
43. Qiu P., Ritchie R.P., Fu Z., et al. Myocardin enhances Smad3-mediated transforming growth factor-beta1 signaling in a CArG box-independent manner: Smad-binding element is an important cis element for SM22alpha transcription in vivo. Circ. Res. 97 (2005) 983-991
44. Chen Y., Budd R.C., Kelm Jr. R.J., Sobel B.E., and Schneider D.J. Augmentation of proliferation of vascular smooth muscle cells by plasminogen activator inhibitor type 1. Arterioscler. Thromb. Vasc. Biol. 26 (2006) 1777-1783
45. Ross S., Cheung E., Petrakis T.G., Howell M., Kraus W.L., and Hill C.S. Smads orchestrate specific histone modifications and chromatin remodeling to activate transcription. Embo J. 25 (2006) 4490-4502
46. Massague J., Seoane J., and Wotton D. Smad transcription factors. Genes Dev. 19 (2005) 2783-2810
47. Clevers H., and van de Wetering M. TCF/LEF factor earn their wings. Trends Genet. 13 (1997) 485-489
48. Tago K., Nakamura T., Nishita M., et al. Inhibition of Wnt signaling by ICAT, a novel beta-catenin-interacting protein. Genes Dev. 14 (2000) 1741-1749
49. Dunn N.R., Koonce C.H., Anderson D.C., Islam A., Bikoff E.K., and Robertson E.J. Mice exclusively expressing the short isoform of Smad2 develop normally and are viable and fertile. Genes Dev. 19 (2005) 152-163
50. Kaps C., Hoffmann A., Zilberman Y., et al. Distinct roles of BMP receptors Type IA and IB in osteo-/chondrogenic differentiation in mesenchymal progenitors (C3H10T1/2). BioFactors 20 (2004) 71-84
51. Gan Q., Yoshida T., Li J., and Owens G.K. Smooth muscle cells and myofibroblasts use distinct transcriptional mechanisms for smooth muscle alpha-actin expression. Circ. Res. 101 (2007) 883-892
52. Xu R., Ho Y.S., Ritchie R.P., and Li L. Human SM22 alpha BAC encompasses regulatory sequences for expression in vascular and visceral smooth muscles at fetal and adult stages. Am. J. Physiol. Heart Circ. Physiol. 284 (2003) H1398-1407
53. Kim S., Ip H.S., Lu M.M., Clendenin C., and Parmacek M.S. A serum response factor-dependent transcriptional regulatory program identifies distinct smooth muscle cell sublineages. Mol. Cell. Biol. 17 (1997) 2266-2278
54. Oishi I., Suzuki H., Onishi N., et al. The receptor tyrosine kinase Ror2 is involved in non-canonical Wnt5a/JNK signalling pathway. Genes Cells 8 (2003) 645-654
55. Dennler S., Huet S., and Gauthier J.M. A short amino-acid sequence in MH1 domain is responsible for functional differences between Smad2 and Smad3. Oncogene 18 (1999) 1643-1648
56. Yagi K., Goto D., Hamamoto T., Takenoshita S., Kato M., and Miyazono K. Alternatively spliced variant of Smad2 lacking exon 3. Comparison with wild-type Smad2 and Smad3. J. Biol. Chem. 274 (1999) 703-709
57. Guo W., Flanagan J., Jasuja R., Kirkland J., Jiang L., and Bhasin S. The effects of myostatin on adipogenic differentiation of human bone marrow-derived mesenchymal stem cells are mediated through cross-communication between Smad3 and Wnt/{beta}-catenin signaling pathways. J. Biol. Chem. 283 (2008) 9136-9145
58. Caraci F., Gili E., Calafiore M., et al. TGF-beta1 targets the GSK-3beta/beta-catenin pathway via ERK activation in the transition of human lung fibroblasts into myofibroblasts. Pharmacol. Res. 57 (2008) 274-282
59. Carmon K.S., and Loose D.S. Secreted frizzled-related protein 4 regulates two wnt7a signaling pathways and inhibits proliferation in endometrial cancer cells. Mol. Cancer Res. 6 (2008) 1017-1028
60. Caricasole A., Ferraro T., Iacovelli L., et al. Functional characterization of WNT7A signaling in PC12 cells: interaction with A FZD5 × LRP6 receptor complex and modulation by Dickkopf proteins. J. Biol. Chem. 278 (2003) 37024-37031
61. Zhou H., Mak W., Zheng Y., Dunstan C.R., and Seibel M.J. Osteoblasts directly control lineage commitment of mesenchymal progenitor cells through Wnt signaling. J. Biol. Chem. 283 (2008) 1936-1945
62. Torsney E., Hu Y., and Xu Q. Adventitial progenitor cells contribute to arteriosclerosis. Trends Cardiovasc. Med. 15 (2005) 64-68
63. Hoshino A., Chiba H., Nagai K., Ishii G., and Ochiai A. Human vascular adventitial fibroblasts contain mesenchymal stem/progenitor cells. Biochem. Biophys. Res. Commun. 368 (2008) 305-310
64. Bostrom K., Zebboudj A.F., Yao Y., Lin T.S., and Torres A. Matrix GLA protein stimulates VEGF expression through increased transforming growth factor-beta1 activity in endothelial cells. J. Biol. Chem. 279 (2004) 52904-52913
65. Parmacek M.S. Myocardin-related transcription factors: critical coactivators regulating cardiovascular development and adaptation. Circ. Res. 100 (2007) 633-644
66. Yoshida T., Kaestner K.H., and Owens G.K. Conditional deletion of Kruppel-like factor 4 delays downregulation of smooth muscle cell differentiation markers but accelerates neointimal formation following vascular injury. Circ. Res. 102 (2008) 1548-1557
67. Liu Y., Sinha S., and Owens G. A transforming growth factor-beta control element required for SM alpha-actin expression in vivo also partially mediates GKLF-dependent transcriptional repression. J. Biol. Chem. 278 (2003) 48004-48011