Coronary vessel development is dependent on the type III transforming growth factor β receptor

Circulation Research

Volumn 101, Issue 8, 2007, Pages 784-791

  Compton, Leigh A ^a   Potash, Dru A ^a   Brown, Christopher B ^b   Barnett, Joey V ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Coronary vessels; Mice, null; Transforming growth factor reptor

Indexed keywords

TRANSFORMING GROWTH FACTOR BETA3; BETAGLYCAN; PROTEOGLYCAN; TRANSFORMING GROWTH FACTOR BETA RECEPTOR; UNCLASSIFIED DRUG;

ANALYTIC METHOD; ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; AORTA; ARTICLE; CONTROLLED STUDY; CORONARY ARTERY; CORONARY BLOOD VESSEL; DEVELOPMENTAL STAGE; EPICARDIUM; HEART MUSCLE; MESENCHYME; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; WILD TYPE; ANIMAL; BIOSYNTHESIS; COMPARATIVE STUDY; FEMALE; FETUS DEVELOPMENT; GENETICS; METABOLISM; MOUSE MUTANT; PATHOLOGY; PREGNANCY; PRENATAL DEVELOPMENT;

ANIMALS; CORONARY VESSELS; FEMALE; FETAL DEVELOPMENT; MICE; MICE, KNOCKOUT; PREGNANCY; PROTEOGLYCANS; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA;

EID: 35448946457     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.107.152082     Document Type: Article

References (59)

1. American Heart Association. Heart disease and stroke statistics - 2004 update. Dallas, Tex: American Heart Association; 2003.
2. Tomanek RJ. Formation of the coronary vasculature during development. Angiogenesis. 2005;8:273-284.
3. Olivey HE, Compton LA, Barnett JV. Coronary vessel development: the epicardium delivers. Trends Cardiovasc Med. 2004;14:247-251.
4. Azhar M, Schultz Jel J, Grupp I, Dorn GW 2nd, Meneton P, Molin DG, Gittenberger-de Groot AC, Doetschman T. Transforming growth factor beta in cardiovascular development and function. Cytokine Growth Factor Rev. 2003;14:391-407.
5. Muraoka-Cook RS, Dumont N, Arteaga CL. Dual role of transforming growth factor beta in mammary tumorigenesis and metastatic progression. Clin Cancer Res. 2005;11:937s-943s.
6. Roberts AB, Wakefield LM. The two faces of transforming growth factor beta in carcinogenesis. Proc Natl Acad Sci U S A. 2003;100:8621-8623.
7. Roberts AB, Sporn MB. The transforming growth factor-betas. In: Sporn MB, Roberts AB, eds. Peptide Growth Factors and Their Receptors. New York: Springer-Verlag; 1990;419-472.
8. Sanford LP, Ormsby I, Gittenberger-de Groot AC, Sariola H, Friedman R, Boivin GP, Cardell EL, Doetschman T. TGFbeta2 knockout mice have multiple developmental defects that are non-overlapping with other TGFbeta knockout phenotypes. Development. 1997;124:2659-2670.
9. Hu PP, Datto MB, Wang XF. Molecular mechanisms of transforming growth factor-beta signaling. Endocr Rev. 1998;19:349-363.
10. Lin HY, Wang XF, Ng-Eaton E, Weinberg RA, Lodish HF. Expression cloning of the TGF-beta type II receptor, a functional transmembrane serine/threonine kinase. Cell. 1992;68:775-785.
11. Ebner R, Chen RH, Shum L, Lawler S, Zioncheck TF, Lee A, Lopez AR, Derynck R. Cloning of a type I TGF-beta receptor and its effect on TGF-beta binding to the type II receptor. Science. 1993;260:1344-1348.
12. Bassing CH, Yingling JM, Howe DJ, Wang T, He WW, Gustafson ML, Shah P, Donahoe PK, Wang XF. A transforming growth factor beta type I receptor that signals to activate gene expression. Science. 1994;263:87-89.
13. Lin HY, Moustakas A. TGF-beta receptors: structure and function. Cell Mol Biol. 1994;40:337-349.
14. Wrana JL, Attisano L, Wieser R, Ventura F, Massague J. Mechanism of activation of the TGF-beta receptor. Nature. 1994;370:341-347.
15. Kretzschmar M, Massague J. SMADs: mediators and regulators of TGF-beta signaling. Curr Opin Genet Dev. 1998;8:103-111.
16. Lopez-Casillas F, Cheifetz S, Doody J, Andres JL, Lane WS, Massague J. Structure and expression of the membrane proteoglycan betaglycan, a component of the TGF-beta receptor system. Cell. 1991;67:785-795.
17. Wang XF, Lin HY, Ng-Eaton E, Downward J, Lodish HF, Weinberg RA. Expression cloning and characterization of the TGF-beta type III receptor. Cell. 1991;67:797-805.
18. Cheifetz S, Bellon T, Cales C, Vera S, Bernabeu C, Massague J, Letarte M. Endoglin is a component of the transforming growth factor-beta receptor system in human endothelial cells. J Biol Chem. 1992;267:19027-19030.
19. Pepper MS. Transforming growth factor-beta: vasculogenesis, angiogenesis, and vessel wall integrity. Cytokine Growth Factor Rev. 1997;8:21-43.
20. Lebrin F, Deckers M, Bertolino P, Ten Dijke P. TGF-beta receptor function in the endothelium. Cardiovasc Res. 2005;65:599-608.
21. Oshima M, Oshima H, Taketo MM. TGF-beta receptor type II deficiency results in defects of yolk sac hematopoiesis and vasculogenesis. Dev Biol. 1996;179:297-302.
22. Shull MM, Ormsby I, Kier AB, Pawlowski S, Diebold RJ, Yin M, Allen R, Sidman C, Proetzel G, Calvin D, Annunziata N, Doetschman T. Targeted disruption of the mouse transforming growth factor-beta 1 gene results in multifocal inflammatory disease. Nature. 1992;359:693-699.
23. Larsson J, Goumans MJ, Sjostrand LJ, van Rooijen MA, Ward D, Leveen P, Xu X, ten Dijke P, Mummery CL, Karlsson S. Abnormal angiogenesis but intact hematopoietic potential in TGF-beta type I receptor-deficient mice. EMBO J. 2001;20:1663-1673.
24. Oh SP, Seki T, Goss KA, Imamura T, Yi Y, Donahoe PK, Li L, Miyazono K, ten Dijke P, Kim S, Li E. Activin receptor-like kinase 1 modulates transforming growth factor-beta 1 signaling in the regulation of angiogenesis. Proc Natl Acad Sci U S A. 2000;97:2626-2631.
25. Li DY, Sorensen LK, Brooke BS, Urness LD, Davis EC, Taylor DG, Boak BB, Wendel DP. Defective angiogenesis in mice lacking endoglin. Science. 1999;284:1534-1537.
26. Chang H, Huylebroeck D, Verschueren K, Guo Q, Matzuk MM, Zwijsen A. Smad5 knockout mice die at mid-gestation due to multiple embryonic and extraembryonic defects. Development. 1999;126:1631-1642.
27. Yang X, Castilla LH, Xu X, Li C, Gotay J, Weinstein M, Liu PP, Deng CX. Angiogenesis defects and mesenchymal apoptosis in mice lacking SMAD5. Development. 1999;126:1571-1580.
28. Goumans MJ, Valdimarsdottir G, Itoh S, Rosendahl A, Sideras P, ten Dijke P. Balancing the activation state of the endothelium via two distinct TGF-beta type I receptors. EMBO J. 2002;21:1743-1753.
29. Goumans MJ, Valdimarsdottir G, Itoh S, Lebrin F, Larsson J, Mummery C, Karlsson S, ten Dijke P. Activin receptor-like kinase (ALK)1 is an antagonistic mediator of lateral TGFbeta/ALK5 signaling. Mol Cell. 2003;12:817-828.
30. Lebrin F, Goumans MJ, Jonker L, Carvalho RL, Valdimarsdottir G, Thorikay M, Mummery C, Arthur HM, ten Dijke P. Endoglin promotes endothelial cell proliferation and TGF-beta/ALK1 signal transduction. EMBO J. 2004;23:4018-4028.
31. Arthur HM, Ure J, Smith AJ, Renforth G, Wilson DI, Torsney E, Charlton R, Parums DV, Jowett T, Marchuk DA, Burn J, Diamond AG. Endoglin, an ancillary TGFbeta receptor, is required for extraembryonic angiogenesis and plays a key role in heart development. Dev Biol. 2000;217:42-53.
32. Bourdeau A, Dumont DJ, Letarte M. A murine model of hereditary hemorrhagic telangiectasia. J Clin Invest. 1999;104:1343-1351.
33. Bartram U, Molin DG, Wisse LJ, Mohamad A, Sanford LP, Doetschman T, Speer CP, Poelmann RE, Gittenberger-de Groot AC. Double-outlet right ventricle and overriding tricuspid valve reflect disturbances of looping, myocardialization, endocardial cushion differentiation, and apoptosis in TGF-beta(2)-knockout mice. Circulation. 2001;103:2745-2752.
34. Stenvers KL, Tursky ML, Harder KW, Kountouri N, Amatayakul-Chantler S, Grail D, Small C, Weinberg RA, Sizeland AM, Zhu HJ. Heart and liver defects and reduced transforming growth factor beta2 sensitivity in transforming growth factor beta type III receptor-deficient embryos. Mol Cell Biol. 2003;23:4371-4385.
35. 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. 1998;141:805-814.
36. Zhang JC, Kim S, Helmke BP, Yu WW, Du KL, Lu MM, Strobeck M, Yu Q, Parmacek MS. Analysis of SM22alpha-deficient mice reveals unanticipated insights into smooth muscle cell differentiation and function. Mol Cell Biol. 2001;21:1336-1344.
37. Mikawa T, Fischman DA. Retroviral analysis of cardiac morphogenesis: discontinuous formation of coronary vessels. Proc Natl Acad Sci U S A. 1992;89:9504-9508.
38. Mikawa T, Gourdie RG. Pericardial mesoderm generates a population of coronary smooth muscle cells migrating into the heart along with ingrowth of the epicardial organ. Dev Biol. 1996;174:221-232.
39. Chen TH-P, Chang T-C, Kang J-O, Choudhary B, Makita T, Tran CM, Burch JBE, Eid H, Sucov HM. Epicardial induction of fetal cardiomyocyte proliferation via a retinoic acid-inducible trophic factor. Dev Biol. 2002;250:198-207.
40. Kwee L, Baldwin HS, Shen HM, Stewart CL, Buck C, Buck CA, Labow MA. Defective development of the embryonic and extraembryonic circulatory systems in vascular cell adhesion molecule (VCAM-1) deficient mice. Development. 1995;121:489-503.
41. Kang JO, Sucov HM. Convergent proliferative response and divergent morphogenic pathways induced by epicardial and endocardial signaling in fetal heart development. Mech Dev. 2005;122:57-65.
42. Tevosian SG, Deconinck AE, Tanaka M, Schinke M, Litovsky SH, Izumo S, Fujiwara Y, Orkin SH. FOG-2, a cofactor for GATA transcription factors, is essential for heart morphogenesis and development of coronary vessels from epicardium. Cell. 2000;101:729-739.
43. Yang JT, Rayburn H, Hynes RO. Cell adhesion events mediated by alpha 4 integrins are essential in placental and cardiac development. Development. 1995;121:549-560.
44. Sengbusch JK, He W, Pinco KA, Yang JT. Dual functions of α4β1 integrin in epicardial development: initial migration and long-term attachment. J Cell Biol. 2002;157:873-882.
45. Kirschner KM, Wagner N, Wagner KD, Wellmann S, Scholz H. The Wilms tumor suppressor Wt1 promotes cell adhesion through transcriptional activation of the {alpha}4integrin gene. J Biol Chem. 2006;281:31930-31939.
46. Moore AW, McInnes L, Kreidberg J, Hastie ND, Schedl A. YAC complementation shows a requirement for Wt1 in the development of epicardium, adrenal gland and throughout nephrogenesis. Development. 1999;126:1845-1857.
47. Crispino JD, Lodish MB, Thurberg BL, Litovsky SH, Collins T, Molkentin JD, Orkin SH. Proper coronary vascular development and heart morphogenesis depend on interaction of GATA-4 with FOG cofactors. Genes Dev. 2001;15:839-844.
48. Li WE, Waldo K, Linask KL, Chen T, Wessels A, Parmacek MS, Kirby ML, Lo CW. An essential role for connexin43 gap junctions in mouse coronary artery development. Development. 2002;129:2031-2042.
49. Smart N, Risebro CA, Melville AA, Moses K, Schwartz RJ, Chien KR, Riley PR. Thymosin beta4 induces adult epicardial progenitor mobilization and neovascularization. Nature. 2007;445:177-182.
50. Ward NL, Van Slyke P, Sturk C, Cruz M, Dumont DJ. Angiopoietin 1 expression levels in the myocardium direct coronary vessel development. Dev Dyn. 2004;229:500-509.
51. Lavine KJ, Yu K, White AC, Zhang X, Smith C, Partanen J, Ornitz DM. Endocardial and epicardial derived FGF signals regulate myocardial proliferation and differentiation in vivo. Dev Cell. 2005;8:85-95.
52. Blobe GC, Liu X, Fang SJ, How T, Lodish HF. A novel mechanism for regulating transforming growth factor beta (TGF-beta) signaling. Functional modulation of type III TGF-beta receptor expression through interaction with the PDZ domain protein, GIPC. J Biol Chem. 2001;276: 39608-39617.
53. Chittenden TW, Claes F, Lanahan AA, Autiero M, Palac RT, Tkachenko EV, Elfenbein A, Ruiz de Almodovar C, Dedkov E, Tomanek R, Li W, Westmore M, Singh JP, Horowitz A, Mulligan-Kehoe MJ, Moodie KL, Zhuang ZW, Carmeliet P, Simons M. Selective regulation of arterial branching morphogenesis by synectin. Dev Cell. 2006;10:783-795.
54. Linhares Y, Gutkind JS. Plexin D1 signals to guide endothelial cells. 2005 Meeting of Medical Fellows, May 9-11, 2005. Chevy Chase, Md: Howard Hughes Medical Institute; 51.
55. Eralp I, Lie-Venema H, DeRuiter MC, van den Akker NM, Bogers AJ, Mentink MM, Poelmann RE, Gittenberger-de Groot AC. Coronary artery and orifice development is associated with proper timing of epicardial outgrowth and correlated fas ligand associated apoptosis patterns. Circ Res. 2005;96:526-534.
56. Velkey JM, Bernanke DH. Apoptosis during coronary artery orifice development in the chick embryo. Anat Rec. 2001;262:310-317.
57. 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 U S A. 1989;86:4544-4548.
58. Olivey H, Mundell NA, Austin AF, Barnett JV. Transforming growth factor beta stimulates epithelial-mesenchymal transformation in the proepicardium. Dev Dyn. 2006;235:50-59.
59. Compton LA, Potash DA, Mundell NA, Barnett JV. Transforming growth factor-beta induces loss of epithelial character and smooth muscle cell differentiation in epicardial cells. Dev Dyn. 2006;235:82-93.