Ligand-specific function of transforming growth factor beta in epithelial-mesenchymal transition in heart development

Developmental Dynamics

Volumn 238, Issue 2, 2009, Pages 431-442

  Azhar, Mohamad ^a,c   Runyan, Raymond B ^a   Gard, Connie ^a   Sanford, L Philip ^a   Miller, Marian L ^b   Andringa, Anastasia ^b   Pawlowski, Sharon ^b   Rajan, Sudarsan ^b   Doetschman, Thomas ^a,c  

^a UNIVERSITY OF ARIZONA   (United States)

^b UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^c NONE   (United States)

Author keywords

Epithelial mesenchymal transformation; Heart development; Transforming growth factor beta; Valvulogenesis

Indexed keywords

CELL MARKER; COLLAGEN GEL; TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR BETA2;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ATRIOVENTRICULAR CANAL; CELL ULTRASTRUCTURE; CONTROLLED STUDY; EMBRYO CELL; EPITHELIUM CELL; GENE TARGETING; HEART DEVELOPMENT; HISTOPATHOLOGY; IN VITRO STUDY; IN VIVO STUDY; MESENCHYME CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION;

ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; ENDOTHELIAL CELLS; EPITHELIAL CELLS; HEART; LIGANDS; MESODERM; MICE; MICE, KNOCKOUT; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR BETA2; TRANSFORMING GROWTH FACTOR BETA3;

MUS;

EID: 59649115469     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.21854     Document Type: Article

References (55)

1. Abdelwahid E, Pelliniemi LJ, Jokinen E. 2002. Cell death and differentiation in the development of the endocardial cushion of the embryonic heart. Microsc Res Tech 58:395-403.
2. Ahmed S, Nawshad A. 2007. Complexity in interpretation of embryonic epithelial-mesenchymal transition in response to transforming growth factor-beta signaling. Cells Tissues Organs 185:131-145.
3. Armstrong EJ, Bischoff J. 2004. Heart valve development: endothelial cell signaling and differentiation. Circ Res 95: 459-470.
4. Azhar M, Schultz JE, Grupp I, Dorn GW, Meneton P, Molin DG, Gittenberger-de Groot AC, Doetschman T. 2003. Transforming growth factor beta in cardiovascular development and function. Cytokine Growth Factor Rev 14:391-407.
5. Barnett JV, Desgrosellier JS. 2003. Early events in valvulogenesis: a signaling perspective. Birth Defects Res C Embryo Today 69:58-72.
6. Bartram U, Bartelings MM, Kramer HH, Gittenberger-de Groot AC. 2001a. Congenital polyvalvular disease: a review. Pediatr Cardiol 22:93-101.
7. Bartram U, Molin DG, Wisse LJ, Mohamad A, Sanford LP, Doetschman T, Speer CP, Poelmann RE, Gittenberger-de GA. 2001b. Double-outlet right ventricle and overriding tricuspid valve reflect disturbances of looping, myocardialization, endocardial cushion differentiation, and apoptosis in Tgfb2 knockout mice. Circulation 103:2745-2752.
8. Bharathy S, Xie W, Yingling JM, Reiss M. 2008. Cancer-associated transforming growth factor beta type II receptor gene mutant causes activation of bone morphogenic protein-Smads and invasive phenotype. Cancer Res 68:1656-1666.
9. Bommireddy R, Pathak LJ, Martin J, Ormsby I, Engle SJ, Boivin GP, Babcock GF, Eriksson AU, Singh RR, Doetschman T. 2006. Self-antigen recognition by TGFbeta1-deficient T cells causes their activation and systemic inflammation. Lab Invest 86:1008-1019.
10. Boyer AS, Ayerinskas II, Vincent EB, McKinney LA, Weeks DL, Runyan RB. 1999. TGFbeta2 and TGFbeta3 have separate and sequential activities during epithelial-mesenchymal cell transformation in the embryonic heart. Dev Biol 208:530-545.
11. Brown CB, Boyer AS, Runyan RB, Barnett JV. 1999. Requirement of type III TGF-beta receptor for endocardial cell transformation in the heart. Science 283:2080-2082.
12. Butcher JT, Markwald RR. 2007. Valvulogenesis: the moving target. Phil Trans R Soc Lond B Biol Sci 362:1489-1503.
13. Camenisch TD, Molin DG, Person A, Runyan RB, Gittenberger-de Groot AC, McDonald JA, Klewer SE. 2002. Temporal and distinct TGFbeta ligand requirements during mouse and avian endocardial cushion morphogenesis. Dev Biol 248:170-181.
14. Camenisch TD, Spicer AP, Brehm-Gibson T, Biesterfeldt J, Augustine ML, Calabro AJ, Kubalak S, Klewer SE, McDonald JA. 2000. Disruption of hyaluronan synthase-2 abrogates normal cardiac morphogenesis and hyaluronan-mediated transformation of epithelium to mesenchyme. J Clin Invest 106:349-360.
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. Diebold RJ, Eis MJ, Yin M, Ormsby I, Boivin GP, Darrow BJ, Saffitz JE, Doetschman T. 1995. Early-onset multifocal inflammation in the transforming growth factor beta 1-null mouse is lymphocyte mediated. Proc Natl Acad Sci USA 92:12215-12219.
17. Enciso JM, Gratzinger D, Camenisch TD, Canosa S, Pinter E, Madri JA. 2003. Elevated glucose inhibits VEGF-A-mediated endocardial cushion formation: modulation by PECAM-1 and MMP-2. J Cell Biol 160:605-615.
18. Gaussin V, Morley GE, Cox L, Zwijsen A, Vance KM, Emile L, Tian Y, Liu J, Hong C, Myers D, Conway SJ, Depre C, Mishina Y, Behringer RR, Hanks MC, Schneider MD, Huylebroeck D, Fishman GI, Burch JB, Vatner SF. 2005. Alk3/ Bmpr1a receptor is required for development of the atrioventricular canal into valves and annulus fibrosus. Circ Res 97:219-226.
19. Gitler AD, Zhu Y, Ismat FA, Lu MM, Yamauchi Y, Parada LF, Epstein JA. 2003. Nf1 has an essential role in endothelial cells. Nat Genet 33:75-79.
20. Grazia LM, Zanetti A, Corada M, Takahashi T, Balconi G, Breviario F, Orsenigo F, Cattelino A, Kemler R, Daniel TO, Dejana E. 2003. Contact inhibition of VEGF-induced proliferation requires vascular endothelial cadherin, beta-catenin, and the phosphatase DEP-1/CD148. J Cell Biol 161:793-804.
21. Jiao K, Langworthy M, Batts L, Brown CB, Moses HL, Baldwin HS. 2006. Tgfbeta signaling is required for atrioventricular cushion mesenchyme remodeling during in vivo cardiac development. Development 133:4585-4593.
22. Kaartinen V, Voncken JW, Shuler C, Warburton D, Bu D, Heisterkamp N, Groffen J. 1995. Abnormal lung development and cleft palate in mice lacking TGF-beta 3 indicates defects of epithelial-mesenchymal interaction. Nat Genet 11:415-421.
23. Kirkbride KC, Townsend TA, Bruinsma MW, Barnett JV, Blobe GC. 2008. Bone morphogenetic proteins signal through the transforming growth factor-beta type III receptor. J Biol Chem 283:7628-7637.
24. Kulkarni AB, Huh CG, Becker D, Geiser A, Lyght M, Flanders KC, Roberts AB, Sporn MB, Ward JM, Karlsson S. 1993. Transforming growth factor beta 1 null mutation in mice causes excessive inflammatory response and early death. Proc Natl Acad Sci USA 90:770-774.
25. Lakkis MM, Epstein JA. 1998. Neurofibromin modulation of ras activity is required for normal endocardial-mesenchymal transformation in the developing heart. Development 125:4359-4367.
26. Lan Y, Liu B, Yao H, Li F, Weng T, Yang G, Li W, Cheng X, Mao N, Yang X. 2007. Essential role of endothelial Smad4 in vascular remodeling and integrity. Mol Cell Biol 27:7683-7692.
27. Ma L, Lu MF, Schwartz RJ, Martin JF. 2005. Bmp2 is essential for cardiac cushion epithelial-mesenchymal transition and myocardial patterning. Development 132: 5601-5611.
28. Markwald RR, Fitzharris TP, Smith WN. 1975. Sturctural analysis of endocardial cytodifferentiation. Dev Biol 42:160-180.
29. Markwald RR, Fitzharris TP, Manasek FJ. 1977. Structural development of endocardial cushions. Am J Anat 148:85-119.
30. Massague J, Gomis RR. 2006. The logic of TGFbeta signaling. FEBS Lett 580:2811-2820.
31. Mercado-Pimentel ME, Runyan RB. 2007. Multiple transforming growth factor-beta isoforms and receptors function during epithelial-mesenchymal cell transformation in the embryonic heart. Cells Tissues Organs 185:146-156.
32. Mercado-Pimentel ME, Hubbard AD, Runyan RB. 2007. Endoglin and Alk5 regulate epithelial-mesenchymal transformation during cardiac valve formation. Dev Biol 304:420-432.
33. Millan FA, Denhez F, Kondaiah P, Akhurst RJ. 1991. Embryonic gene expression patterns of TGF beta 1, beta 2 and beta 3 suggest different developmental functions in vivo. Development 111:131-143.
34. Molin DG, Bartram U, Van der HK, Van Iperen L, Speer CP, Hierck BP, Poelmann RE, Gittenberger-de-Groot AC. 2003. Expression patterns of Tgfbeta1-3 associate with myocardialisation of the outflow tract and the development of the epicardium and the fibrous heart skeleton. Dev Dyn 227:431-444.
35. Nakajima Y, Krug EL, Markwald RR. 1994. Myocardial regulation of transforming growth factor-beta expression by outflow tract endothelium in the early embryonic chick heart. Dev Biol 165: 615-626.
36. Okunade GW, Miller ML, Azhar M, Andringa A, Sanford LP, Doetschman T, Prasad V, Shull GE. 2007. Loss of the Atp2c1 secretory pathway Ca(2+)-ATPase (SPCA1) in mice causes Golgi stress, apoptosis, and midgestational death in homozygous embryos and squamous cell tumors in adult heterozygotes. J Biol Chem 282:26517-26527.
37. Paruchuri S, Yang JH, Aikawa E, Melero-Martin JM, Khan ZA, Loukogeorgakis S, Schoen FJ, Bischoff J. 2006. Human pulmonary valve progenitor cells exhibit endothelial/ mesenchymal plasticity in response to vascular endothelial growth factor-A and transforming growth factor-beta2. Circ Res 99:861-869.
38. Person AD, Klewer SE, Runyan RB. 2005. Cell biology of cardiac cushion development. Int Rev Cytol 243:287-335.
39. Pfaffl MW. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45.
40. Pierpont ME, Basson CT, Benson DW, Jr., Gelb BD, Giglia TM, Goldmuntz E, Mc-Gee G, Sable CA, Srivastava D, Webb CL. 2007. Genetic basis for congenital heart defects: current knowledge: a scientific statement from the American Heart Association Congenital Cardiac Defects Committee, Council on Cardiovascular Disease in the Young, endorsed by the American Academy of Pediatrics. Circulation 115:3015-3038.
41. Potts JD, Runyan RB. 1989. Epithelial-mesenchymal cell transformation in the embryonic heart can be mediated, in part, by transforming growth factor beta. Dev Biol 134:392-401.
42. Potts JD, Vincent EB, Runyan RB, Weeks DL. 1992. Sense and antisense TGF beta 3 mRNA levels correlate with cardiac valve induction. Dev Dyn 193:340-345.
43. Prasad V, Boivin GP, Miller ML, Liu LH, Erwin CR, Warner BW, Shull GE. 2005. Haploinsufficiency of Atp2a2, encoding the sarco(endo)plasmic reticulum Ca2+-ATPase isoform 2 Ca2+ pump, predisposes mice to squamous cell tumors via a novel mode of cancer susceptibility. Cancer Res 65:8655-8661.
44. Proetzel G, Pawlowski SA, Wiles MV, Yin M, Boivin GP, Howles PN, Ding J, Ferguson MW, Doetschman T. 1995. Transforming growth factor-beta 3 is required for secondary palate fusion. Nat Genet 11:409-414.
45. Rajan S, Williams SS, Jagatheesan G, Ahmed RP, Fuller-Bicer G, Schwartz A, Aronow BJ, Wieczorek DF. 2006. Microarray analysis of gene expression during early stages of mild and severe cardiac hypertrophy. Physiol Genomics 27: 309-317.
46. Rivera-Feliciano J, Tabin CJ. 2006. Bmp2 instructs cardiac progenitors to form the heart-valve-inducing field. Dev Biol 295: 580-588.
47. Rudini N, Felici A, Giampietro C, Lampugnani M, Corada M, Swirsding K, Garre M, Liebner S, Letarte M, ten Dijke P, Dejana E. 2008. VE-cadherin is a critical endothelial regulator of TGF-beta signalling. EMBO J 27:993-1004.
48. Sanford LP, Ormsby I, Gittenberger-de GA, Sariola H, Friedman R, Boivin GP, Cardell EL, Doetschman T. 1997. TGF-beta2 knockout mice have multiple developmental defects that are non-overlapping with other TGFbeta knockout phenotypes. Development 124:2659-2670.
49. Shull MM, Ormsby I, Kier AB, Pawlowski S, Diebold RJ, Yin M, Allen R, Sidman C, Proetzel G, Calvin D, Doetschman T. 1992. Targeted disruption of the mouse transforming growth factor-beta 1 gene results in multifocal inflammatory disease. Nature 359:693-699.
50. Sridurongrit S, Larsson J, Schwartz R, Ruiz-Lozano P, Kaartinen V. 2008. Signaling via the Tgf-beta type I receptor Alk5 in heart development. Dev Biol 322:208-218.
51. Supino PG, Borer JS, Yin A, Dillingham E, McClymont W. 2004. The epidemiology of valvular heart diseases: the problem is growing. Adv Cardiol 41:9-15.
52. Timmerman LA, Grego-Bessa J, Raya A, Bertran E, Perez-Pomares JM, Diez J, Aranda S, Palomo S, McCormick F, Izpisua-Belmonte JC, de la Pompa JL. 2004. Notch promotes epithelial-mesenchymal transition during cardiac development and oncogenic transformation. Genes Dev 18:99-115.
53. Wang J, Sridurongrit S, Dudas M, Thomas P, Nagy A, Schneider MD, Epstein JA, Kaartinen V. 2005. Atrioventricular cushion transformation is mediated by ALK2 in the developing mouse heart. Dev Biol 286:299-310.
54. Yamagishi T, Nakajima Y, Miyazono K, Nakamura H. 1999. Bone morphogenetic protein-2 acts synergistically with transforming growth factor-beta3 during endothelial-mesenchymal transformation in the developing chick heart. J Cell Physiol 180:35-45.
55. Yang JH, Wylie-Sears J, Bischoff J. 2008. Opposing actions of Notch1 and VEGF in postnatal cardiac valve endothelial cells. Biochem Biophys Res Commun 374:512-516.