Transforming growth factor-β1 signaling contributes to development of smooth muscle cells from embryonic stem cells

American Journal of Physiology - Cell Physiology

Volumn 287, Issue 6 56-6, 2004, Pages

  Sinha, Sanjay ^a   Hoofnagle, Mark H ^a   Kingston, Paul A ^b   McCanna, Mary E ^a   Owens, Gary K ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Embryoid body; Smad

Indexed keywords

ALPHA ACTIN; MYOSIN; MYOSIN HEAVY CHAIN; SMAD PROTEIN; SMAD2 PROTEIN; SMAD3 PROTEIN; SMALL INTERFERING RNA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL CELL; ANTIBODY SPECIFICITY; ARTICLE; CELL DIFFERENTIATION; CELL MATURATION; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION; GENE INDUCTION; HUMAN; HUMAN CELL; MARKER GENE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; SIGNAL TRANSDUCTION; SMOOTH MUSCLE CONTRACTION; SMOOTH MUSCLE FIBER; TOTIPOTENT STEM CELL;

ACTINS; ANIMALS; ANTIBODIES; BIOLOGICAL MARKERS; CELL DIFFERENTIATION; CELL LINEAGE; CELLS, CULTURED; DNA-BINDING PROTEINS; DOWN-REGULATION; ENDOTHELIUM; GENE EXPRESSION; MICE; MUTAGENESIS; MYOCYTES, SMOOTH MUSCLE; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SMAD2 PROTEIN; SMAD3 PROTEIN; TOTIPOTENT STEM CELLS; TRANS-ACTIVATORS; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA1; UP-REGULATION;

ADENOVIRIDAE; ANIMALIA;

EID: 8644264026     PISSN: 03636143     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpcell.00221.2004     Document Type: Article

References (36)

1. Aikawa M, Sivam PN, Kuro-o M, Kimura K, Nakahara K, Takewaki S, Ueda M, Yamaguchi H, Yazaki Y, and Periasamy M. Human smooth muscle myosin heavy chain isoforms as molecular markers for vascular development and atherosclerosis. Circ Res 73: 1000-1012, 1993.
2. Baldwin HS, Shen HM, Yan HC, DeLisser HM, Chung A, Mickanin C, Trask T, Kirschbaum NE, Newman PJ, Albelda SM, and Buck CA. Platelet endothelial cell adhesion molecule-1 (PECAM-1/CD31): alternatively spliced, functionally distinct isoforms expressed during mammalian cardiovascular development. Development 120: 2539-2553, 1994.
3. Bjorkerud S. Effects of transforming growth factor-beta 1 on human arterial smooth muscle cells in vitro. Arterioscler Thromb 11: 892-902, 1991.
4. Borrione AC, Zanellato AM, Scannapieco G, Pauletto P, and Sartore S. Myosin heavy-chain isoforms in adult and developing rabbit vascular smooth muscle. Eur J Biochem 183: 413-417, 1989.
5. Bourdeau A, Dumont DJ, and Letarte M. A murine model of hereditary hemorrhagic telangiectasia. J Clin Invest 104: 1343-1351, 1999.
6. Chang H, Huylebroeck D, Verschueren K, Guo Q, Matzuk MM, and Zwijsen A. Smad5 knockout mice die at mid-gestation due to multiple embryonic and extraembryonic defects. Development 126: 1631-1642, 1999.
7. Chen S, Kulik M, and Lechleider RJ. Smad proteins regulate transcriptional induction of the SM22α gene by TGF-β. Nucleic Acids Res 31: 1302-1310, 2003.
8. Chen S and Lechleider RJ. Transforming growth factor-β-induced differentiation of smooth muscle from a neural crest stem cell line. Circ Res 94: 1195-1202, 2004.
9. Datto MB, Frederick JP, Pan L, Borton AJ, Zhuang Y, and Wang XF. Targeted disruption of Smad3 reveals an essential role in transforming growth factor β-mediated signal transduction. Mol Cell Biol 19: 2495-2504, 1999.
10. Dickson MC, Martin JS, Cousins FM, Kulkarni AB, Karlsson S, and Akhurst RJ. Defective haematopoiesis and vasculogenesis in transforming growth factor-beta 1 knock out mice. Development 121: 1845-1854, 1995.
11. Drab M, Haller H, Bychkov R, Erdmann B, Lindschau C, Haase H, Morano I, Luft FC, and Wobus AM. From totipotent embryonic stem cells to spontaneously contracting smooth muscle cells: a retinoic acid and db-cAMP in vitro differentiation model. FASEB J 11: 905-915, 1997.
12. Groschel-Stewart U, Schreiber J, and Mahlmeister C. Production of specific antibodies to contractile proteins, and their use in immunofluorescence microscopy. I. Antibodies to smooth and striated chicken muscle myosins. Histochemistry 46: 229-236, 1976.
13. Gualandris A, Annes JP, Arese M, Noguera I, Jurukovski V, and Rifkin DB. The latent transforming growth factor-β-binding protein-1 promotes in vitro differentiation of embryonic stem cells into endothelium. Mol Biol Cell 11: 4295-4308, 2000.
14. Hautmann MB, Madsen CS, and Owens GK. A transforming growth factor β (TGF β) control element drives TGFβ-induced stimulation of smooth muscle α-actin gene expression in concert with two CArG elements. J Biol Chem 272: 10948-10956, 1997.
15. Hirschi KK, Rohovsky SA, and D'Amore PA. PDGF, TGF-β, 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.
16. Jain RK. Molecular regulation of vessel maturation. Nat Med 9: 685-693, 2003.
17. Kato S, Ueda S, Tamaki K, Fujii M, Miyazono K, ten Dijke P, Morimatsu M, and Okuda S. Ectopic expression of Smad7 inhibits transforming growth factor-beta responses in vascular smooth muscle cells. Life Sci 69: 2641-2652, 2001.
18. Kingston PA, Sinha S, David A, Castro MG, Lowenstein PR, and Heagerty AM. Adenovirus-mediated gene transfer of a secreted transforming growth factor-β type II receptor inhibits luminal loss and constrictive remodeling after coronary angioplasty and enhances adventitial collagen deposition. Circulation 104: 2595-2601, 2001.
19. Lan HY, Mu W, Tomita N, Huang XR, Li JH, Zhu HJ, Morishita R, and Johnson RJ. Inhibition of renal fibrosis by gene transfer of inducible Smad7 using ultrasound-microbubble system in rat UUO model. J Am Soc Nephrol 14: 1535-1548, 2003.
20. Li DY, Sorensen LK, Brooke BS, Urness LD, Davis EC, Taylor DG, Boak BB, and Wendel DP. Defective angiogenesis in mice lacking endoglin. Science 284: 1534-1537, 1999.
21. 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.
22. 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.
23. Massague J and Chen YG. Controlling TGF-β signaling. Genes Dev 14: 627-644, 2000.
24. Oh SP, Seki T, Goss KA, Imamura T, Yi Y, Donahoe PK, Li L, Miyazono K, ten Dijke P, Kim S, and Li E. Activin receptor-like kinase 1 modulates transforming growth factor-β1 signaling in the regulation of angiogenesis. Proc Natl Acad Sci USA 97: 2626-2631, 2000.
25. Oshima M, Oshima H, and Taketo MM. TGF-β receptor type II deficiency results in defects of yolk sac hematopoiesis and vasculogenesis. Dev Biol 179: 297-302, 1996.
26. Owens GK. Regulation of differentiation of vascular smooth muscle cells. Physiol Rev 75: 487-517, 1995.
27. Piek E, Ju WJ, Heyer J, Escalante-Alcalde D, Stewart CL, Weinstein M, Deng C, Kucherlapati R, Bottinger EP, and Roberts AB. Functional characterization of transforming growth factor β signaling in Smad2- and Smad3-deficient fibroblasts. J Biol Chem 276: 19945-19953, 2001.
28. Qiu P, Feng XH, and Li L. Interaction of Smad3 and SRF-associated complex mediates TGF-β1 signals to regulate SM22 transcription during myofibroblast differentiation. J Mol Cell Cardiol 35: 1407-1420, 2003.
29. Redick SD and Bautch VL. Developmental platelet endothelial cell adhesion molecule expression suggests multiple roles for a vascular adhesion molecule. Am J Pathol 154: 1137-1147, 1999.
30. Regan CP, Manabe I, and Owens GK. Development of a smooth muscle-targeted ere recombinase mouse reveals novel insights regarding smooth muscle myosin heavy chain promoter regulation. Circ Res 87: 363-369, 2000.
31. Resnick N, Yahav H, Shay-Salit A, Shushy M, Schubert S, Zilberman LC, and Wofovitz E. Fluid shear stress and the vascular endothelium: for better and for worse. Prog Biophys Mol Biol 81: 177-199, 2003.
32. Shah NM, Groves AK, and Anderson DJ. Alternative neural crest cell fates are instructively promoted by TGFbeta superfamily members. Cell 85: 331-343, 1996.
33. Urness LD, Sorensen LK, and Li DY. Arteriovenous malformations in mice lacking activin receptor-like kinase-1. Nat Genet 26: 328-331, 2000.
34. Yang X, Letterio JJ, Lechleider RJ, Chen L, Hayman R, Gu H, Roberts AB, and Deng C. Targeted disruption of SMAD3 results in impaired mucosal immunity and diminished T cell responsiveness to TGF-beta. EMBO J 18: 1280-1291, 1999.
35. Yoshida T, Sinha S, Dandre F, Wamhoff BR, Hoofnagle MH, Kremer BE, Wang DZ, Olson EN, and Owens GK. Myocardin is a key regulator of CArG-dependent transcription of multiple smooth muscle marker genes. Circ Res 92: 856-864, 2003.
36. Zanellato AM, Borrione AC, Giuriato L, Tonello M, Scannapieco G, Pauletto P, and Sartore S. Myosin isoforms and cell heterogeneity in vascular smooth muscle. I. Developing and adult bovine aorta. Dev Biol 141: 431-446, 1990.