Transforming growth factor-β induces loss of epithelial character and smooth muscle cell differentiation in epicardial cells

Developmental Dynamics

Volumn 235, Issue 1, 2006, Pages 82-93

  Compton, Leigh A ^a   Potash, Dru A ^a   Mundell, Nathan A ^a   Barnett, Joey V ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Chick; Development; Epicardium; Epithelial mesenchymal transformation; Smooth muscle; Transforming growth factor beta receptors

Indexed keywords

CALDESMON; CALPONIN; CYTOKERATIN; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN P160; RHO KINASE; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1; TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR BETA2; ACTIVIN RECEPTOR 1; CALMODULIN BINDING PROTEIN; PROTEIN SERINE THREONINE KINASE; RHO-ASSOCIATED KINASE; SIGNAL PEPTIDE; TGF BETA TYPE I RECEPTOR; TGF-BETA TYPE I RECEPTOR; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL INVASION; CELL LOSS; CELL STIMULATION; CELL STRUCTURE; CELL TRANSFORMATION; CONTROLLED STUDY; EPICARDIUM; EPITHELIUM CELL; GENE OVEREXPRESSION; MESENCHYME CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; SMOOTH MUSCLE FIBER; ANIMAL; BIOSYNTHESIS; CHICK EMBRYO; CYTOLOGY; ENZYMOLOGY; EPITHELIUM; GENETICS; METABOLISM; ORGAN CULTURE TECHNIQUE; PERICARDIUM; PHYSIOLOGY;

ACTIVIN RECEPTORS, TYPE I; ANIMALS; CALMODULIN-BINDING PROTEINS; CELL DIFFERENTIATION; CHICK EMBRYO; EPITHELIUM; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MYOCYTES, SMOOTH MUSCLE; ORGAN CULTURE TECHNIQUES; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PERICARDIUM; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA;

EID: 33644975212     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.20629     Document Type: Article

References (68)

1. Akhurst RJ, Lehnert SA, Faissner A, Duffle E. 1990. TGF beta in murine morphogenetic processes: the early embryo and cardiogenesis. Development 108:645-656.
2. Annes JP, Munger JS, Rifkin DB. 2003. Making sense of latent TGFbeta activation. J Cell Sci 116:217-224.
3. Bakin AV, Tomlinson AK, Bhowmick NA, Moses HL, Arteaga CL. 2000. Phosphatidylinositol 3-kinase function is required for transforming growth factor beta-mediated epithelial to mesenchymal transition and cell migration. J Biol Chem 275:36803-36810.
4. Bakin AV, Rinehart C, Tomlinson AK, Arteaga CL. 2002. p38 mitogen-activated protein kinase is required for TGFbeta-mediated fibroblastic transdifferentiation and cell migration. J Cell Sci 115:3193-3206.
5. Barnett JV, Moustakas A, Lin W, Wang XF, Lin HY, Galper JB, Maas RL. 1994. Cloning and developmental expression of the chick type II and type III TGF beta receptors. Dev Dyn 199:12-27.
6. Bhowmick NA, Ghiassi M, Bakin A, Aakre M, Lundquist CA, Engel ME, Arteaga CL, Moses HL. 2001a. Transforming growth factor-beta1 mediates epithelial to mesenchymal transdifferentiation through a RhoA-dependent mechanism. Mol Biol Cell 12:27-36.
7. Bhowmick NA, Zent R, Ghiassi M, McDonnell M, Moses HL. 2001b. Integrin beta 1 signaling is necessary for transforming growth factor-beta activation of p38MAPK and epithelial plasticity. J Biol Chem 276:46707-46713.
8. Bhowmick NA, Ghiassi M, Aakre M, Brown K, Singh V, Moses HL. 2003. TGF-beta-induced RhoA and p160ROCK activation is involved in the inhibition of Cdc25A with resultant cell-cycle arrest. Proc Natl Acad Sci U S A 100:15548-15553.
9. Chen S, Lechleider RJ. 2004. Transforming growth factor-beta-induced differentiation of smooth muscle from a neural crest stem cell line. Circ Res 94:1195-1202.
10. Crispino JD, Lodish MB, Thurberg BL, Litovsky SH, Collins T, Molkentin JD, Orkin SH. 2001. Proper coronary vascular development and heart morphogenesis depend on interaction of GATA-4 with FOG cofactors. Genes Dev 15:839-844.
11. Darland DC, D'Amore PA. 2001. TGF beta is required for the formation of capillary-like structures in three-dimensional co-cultures of 10T1/2 and endothelial cells. Angiogenesis 4:11-20.
12. Deaton RA, Su C, Valencia TG, Grant SR. 2005. Transforming growth factor-beta 1-induced expression of smooth muscle marker genes involves activation of PKN and p38 MAP kinase. J Biol Chem 280:31172-31181.
13. Desgrosellier JS, Mundell NA, McDonnell MA, Moses HL, Barnett JV. 2005. Activin receptor-like kinase 2 and Smad6 regulate epithelial-mesenchymal transformation during cardiac valve formation. Dev Biol 280:201-210.
14. Dettman RW, Denetclaw W Jr, Ordahl CP, Bristow J. 1998. Common epicardial origin of coronary vascular smooth muscle, perivascular fibroblasts, and intermyocardial fibroblasts in the avian heart. Dev Biol 193:169-181.
15. Dickson MC, Slager HG, Duffie E, Mummery CL, Akhurst RJ. 1993. RNA and protein localisations of TGF beta 2 in the early mouse embryo suggest an involvement in cardiac development. Development 117:625-639.
16. Edlund S, Landstrom M, Heldin CH, Aspenstrom P. 2002. Transforming growth factor-beta-induced mobilization of actin cytoskeleton requires signaling by small GTPases Cdc42 and RhoA. Mol Biol Cell 13:902-914.
17. Furumatsu T, Tsuda M, Taniguchi N, Tajima Y, Asahara H. 2005. Smad3 induces chondrogenesis through the activation of SOX9 via CREB-binding protein/p300 recruitment. J Biol Chem 280:8343-8350.
18. Ghosh S, Brauer PR. 1996. Latent transforming growth factor-beta is present in the extracellular matrix of embryonic hearts in situ. Dev Dyn 205:126-134.
19. Goumans MJ, Valdimarsdottir G, Itoh S, Lebrin F, Larsson J, Mummery C, Karlsson S, ten Dijke P. 2003. Activin receptor-like kinase (ALK)1 is an antagonistic mediator of lateral TGFbeta/ALK5 signaling. Mol Cell 12:817-828.
20. Grainger DJ, Metcalfe JC, Grace AA, Mosedale DE. 1998. Transforming growth factor-beta dynamically regulates vascular smooth muscle differentiation in vivo. J Cell Sci 111(Pt 19):2977-2988.
21. Hamburger V, Hamilton HL. 1992. A series of normal stages in the development of the chick embryo. 1951. Dev Dyn 195:231-272.
22. Hayashi K, Takahashi M, Kimura K, Nishida W, Saga H, Sobue K. 1999. 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.
23. Hayashi K, Takahashi M, Nishida W, Yoshida K, Ohkawa Y, Kitabatake A, Aoki J, Arai H, Sobue K. 2001. Phenotypic modulation of vascular smooth muscle cells induced by unsaturated lysophosphatidic acids. Circ Res 89:251-258.
24. He WW, Gustafson ML, Hirobe S, Donahoe PK. 1993. Developmental expression of four novel serine/threonine kinase receptors homologous to the activin/transforming growth factor-beta type II receptor family. Dev Dyn 196:133-142.
25. Hellstrom M, Kalen M, Lindahl P, Abramsson A, Betsholtz C. 1999. 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.
26. Hirschi KK, Rohovsky SA, D'Amore PA. 1998. 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.
27. Hirschi KK, Lai L, Belaguli NS, Dean DA, Schwartz RJ, Zimmer WE. 2002. Transforming growth factor-beta induction of smooth muscle cell phenotype requires transcriptional and post-transcriptional control of serum response factor. J Biol Chem 277:6287-6295.
28. Ho E, Shimada Y. 1978. Formation of the epicardium studied with the scanning electron microscope. Dev Biol 66:579-585.
29. Holifield JS, Arlen AM, Runyan RB, Tomanek RJ. 2004. TGF-beta1, -beta2 and -beta3 cooperate to facilitate tubulogenesis in the explanted quail heart. J Vasc Res 41:491-498.
30. Iseki S, Osumi-Yamashita N, Miyazono K, Franzen P, Ichijo H, Ohtani H, Hayashi Y, Eto K. 1995. Localization of transforming growth factor-beta type I and type II receptors in mouse development. Exp Cell Res 219:339-347.
31. Ishizaki T, Maekawa M, Fujisawa K, Okawa K, Iwamatsu A, Fujita A, Watanabe N, Saito Y, Kakizuka A, Morii N, Narumiya S. 1996. The small GTP-binding protein Rho binds to and activates a 160 kDa Ser/Thr protein kinase homologous to myotonic dystrophy kinase. EMBO J 15:1885-1893.
32. Jakowlew SB, Ciment G, Tuan RS, Sporn MB, Roberts AB. 1994. Expression of transforming growth factor-beta 2 and beta 3 mRNAs and proteins in the developing chicken embryo. Differentiation 55:105-118.
33. Kakiuchi R, Inui M, Morimoto K, Kanda K, Sobue K, Kakiuchi S. 1983. Caldesmon, a calmodulin-binding, F actin-interacting protein, is present in aorta, uterus and platelets. FEBS Lett 154:351-356.
34. Kalluri R, Neilson EG. 2003. Epithelial-mesenchymal transition and its implications for fibrosis. J Clin Invest 112:1776-1784.
35. Kaplan-Albuquerque N, Garat C, Desseva C, Jones PL, Nemenoff RA. 2003. Platelet-derived growth factor-BB-mediated activation of Akt suppresses smooth muscle-specific gene expression through inhibition of mitogen-activated protein kinase and redistribution of serum response factor. J Biol Chem 278:39830-39838.
36. Komiyama M, Ito K, Shimada Y. 1987. Origin and development of the epicardium in the mouse embryo. Anat Embryol (Berl) 176:183-189.
37. Kretzschmar M, Massague J. 1998. SMADs: mediators and regulators of TGF-beta signaling. Curr Opin Genet Dev 8:103-111.
38. Kwee L, Baldwin HS, Shen HM, Stewart CL, Buck C, Buck CA, Labow MA. 1995. Defective development of the embryonic and extraembryonic circulatory systems in vascular cell adhesion molecule (VCAM-1) deficient mice. Development 121:489-503.
39. Lavine KJ, Yu K, White AC, Zhang X, Smith C, Partanen J, Ornitz DM. 2005. Endocardial and epicardial derived FGF signals regulate myocardial proliferation and differentiation in vivo. Dev Cell 8:85-95.
40. Lu J, Landerholm TE, Wei JS, Dong XR, Wu SP, Liu X, Nagata K, Inagaki M, Majesky MW. 2001. Coronary smooth muscle differentiation from proepicardial cells requires rhoA-mediated actin reorganization and p160 rho-kinase activity. Dev Biol 240:404-418.
41. Mack CP, Somlyo AV, Hautmann M, Somlyo AP, Owens GK. 2001. Smooth muscle differentiation marker gene expression is regulated by RhoA-mediated actin polymerization. J Biol Chem 276:341-347.
42. Manner J. 1993. Experimental study on the formation of the epicardium in chick embryos. Anat Embryol (Berl) 187:281-289.
43. Masszi A, Di Ciano C, Sirokmany G, Arthur WT, Rotstein OD, Wang J, McCulloch CA, Rosivall L, Mucsi I, Kapus A. 2003. Central role for Rho in TGF-beta1-induced alpha-smooth muscle actin expression during epithelial-mesenchymal transition. Am J Physiol Renal Physiol 284:F911-F924.
44. Mikawa T, Fischman DA. 1992. Retroviral analysis of cardiac morphogenesis: discontinuous formation of coronary vessels. Proc Natl Acad Sci U S A 89:9504-9508.
45. Mikawa T, Gourdie RG. 1996. Pericardial mesoderm generates a population of coronary smooth muscle cells migrating into the heart along with ingrowth of the epicardial organ. Dev Biol 174:221-232.
46. Molin DG, Bartram U, Van der Heiden K, Van Iperen L, Speer CP, Hierck BP, Poelmann RE, Gittenberger-de-Groot AC. 2003. Expression patterns of Tgf-beta1-3 associate with myocardialisation of the outflow tract and the development of the epicardium and the fibrous heart skeleton. Dev Dyn 227:431-444.
47. Moore AW, McInnes L, Kreidberg J, Hastie ND, Schedl A. 1999. YAC complementation shows a requirement for Wt1 in the development of epicardium, adrenal gland and throughout nephrogenesis. Development 126:1845-1857.
48. Morabito CJ, Dettman RW, Kattan J, Collier JM, Bristow J. 2001. Positive and negative regulation of epicardial-mesenchymal transformation during avian heart development. Dev Biol 234:204-215.
49. Owens GK, Kumar MS, Wamhoff BR. 2004. Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol Rev 84:767-801.
50. Ozdamar B, Bose R, Barrios-Rodiles M, Wang HR, Zhang Y, Wrana JL. 2005. Regulation of the polarity protein Par6 by TGFbeta receptors controls epithelial cell plasticity. Science 307:1603-1609.
51. Pelton RW, Saxena B, Jones M, Moses HL, Gold LI. 1991. Immunohistochemical localization of TGF beta 1, TGF beta 2, and TGF beta 3 in the mouse embryo: expression patterns suggest multiple roles during embryonic development. J Cell Biol 115:1091-1105.
52. Perez-Pomares JM, Macias D, Garcia-Garrido L, Munoz-Chapuli R. 1997. Contribution of the primitive epicardium to the subepicardial mesenchyme in hamster and chick embryos. Dev Dyn 210:96-105.
53. Poelmann RE, Gittenberger-de Groot AC, Mentink MM, Bokenkamp R, Hogers B. 1993. Development of the cardiac coronary vascular endothelium, studied with antiendothelial antibodies, in chicken-quail chimeras. Circ Res 73:559-568.
54. Ryan DH, Nuccie BL, Abboud CN, Winslow JM. 1991. Vascular cell adhesion molecule-1 and the integrin VLA-4 mediate adhesion of human B cell precursors to cultured bone marrow adherent cells. J Clin Invest 88:995-1004.
55. Sengbusch JK, He W, Pinco KA, Yang JT. 2002. Dual functions of α4β1 integrin in epicardial development: initial migration and long-term attachment. J Cell Biol 157:873-882.
56. Shi Y, Massague J. 2003. Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 113:685-700.
57. Sinha S, Hoofnagle MH, Kingston PA, McCanna ME, Owens GK. 2004. Transforming growth factor-beta1 signaling contributes to development of smooth muscle cells from embryonic stem cells. Am J Physiol Cell Physiol 287:C1560-C1568.
58. Stevenson BR, Anderson JM, Bullivant S. 1988. The epithelial tight junction: structure, function and preliminary biochemical characterization. Mol Cell Biochem 83:129-145.
59. Takahashi K, Hiwada K, Kokubu T. 1988. Vascular smooth muscle calponin. A novel troponin T-like protein. Hypertension 11:620-626.
60. Tevosian SG, Deconinck AE, Tanaka M, Schinke M, Litovsky SH, Izumo S, Fujiwara Y, Orkin SH. 2000. FOG-2, a cofactor for GATA transcription factors, is essential for heart morphogenesis and development of coronary vessels from epicardium. Cell 101:729-739.
61. Tock J, Van Putten V, Stenmark KR, Nemenoff RA. 2003. Induction of SM-alpha-actin expression by mechanical strain in adult vascular smooth muscle cells is mediated through activation of JNK and p38 MAP kinase. Biochem Biophys Res Commun 301:1116-1121.
62. Tomanek RJ, Ratajska A, Kitten GT, Yue X, Sandra A. 1999. Vascular endothelial growth factor expression coincides with coronary vasculogenesis and angiogenesis. Dev Dyn 215:54-61.
63. Van Den Akker NM, Lie-Venema H, Maas S, Eralp I, Deruiter MC, Poelmann RE, Gittenberger-De Groot AC. 2005. Platelet-derived growth factors in the developing avian heart and maturating coronary vasculature. Dev Dyn 233:1579-1588.
64. Vijayachandra K, Lee J, Glick AB. 2003. Smad3 regulates senescence and malignant conversion in a mouse multistage skin carcinogenesis model. Cancer Res 63:3447-3452.
65. Viragh S, Challice CE. 1981. The origin of the epicardium and the embryonic myocardial circulation in the mouse. Anat Rec 201:157-168.
66. Ward SM, Gadbut AP, Tang D, Papageorge AG, Wu L, Li G, Barnett JV, Galper JB. 2002. TGFbeta regulates the expression of G alpha(i2) via an effect on the localization of ras. J Mol Cell Cardiol 34:1217-1226.
67. Xie L, Law BK, Chytil AM, Brown KA, Aakre ME, Moses HL. 2004. Activation of the Erk pathway is required for TGF-beta1-induced EMT in vitro. Neoplasia 6:603-610.
68. Yang JT, Rayburn H, Hynes RO. 1995. Cell adhesion events mediated by alpha 4 integrins are essential in placental and cardiac development. Development 121: 549-560.