Cell autonomous requirement of endocardial Smad4 during atrioventricular cushion development in mouse embryos

Developmental Dynamics

Volumn 240, Issue 1, 2011, Pages 211-220

  Song, Langying ^a,d   Zhao, Mei ^a,e   Wu, Bingruo ^b   Zhou, Bin ^b   Wang, Qin ^c   Jiao, Kai ^a  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e CHINA MEDICAL UNIVERSITY   (China)

Author keywords

Atrioventricular cushion; BMP; Congenital heart disease; Smad4; Valvulogenesis

Indexed keywords

BONE MORPHOGENETIC PROTEIN; COLLAGEN GEL; SMAD4 PROTEIN;

ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL PROLIFERATION; EMBRYO; EMBRYO DEATH; EMBRYO DEVELOPMENT; ENDOCARDIUM; GENE EXPRESSION; GENE INACTIVATION; HEART ATRIOVENTRICULAR NODE; HEART DEVELOPMENT; MESENCHYME CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; CELL COMMUNICATION; CELL PROLIFERATION; CELL SURVIVAL; EMBRYO, MAMMALIAN; EMBRYONIC DEVELOPMENT; ENDOCARDIAL CUSHIONS; ENDOCARDIUM; FEMALE; GESTATIONAL AGE; HEART DEFECTS, CONGENITAL; MALE; MICE; MICE, TRANSGENIC; SMAD4 PROTEIN;

EID: 78650364001     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.22493     Document Type: Article

References (60)

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. Armstrong EJ, Bischoff J. 2004. Heart valve development: endothelial cell signaling and differentiation. Circ Res 95: 459-470.
3. Barnett JV, Desgrosellier JS. 2003. Early events in valvulogenesis: a signaling perspective. Birth Defects Res Part C Embryo Today 69: 58-72.
4. Bei M, Maas R. 1998. FGFs and BMP4 induce both Msx1-independent and Msx1-dependent signaling pathways in early tooth development. Development 125: 4325-4333.
5. Bei M, Kratochwil K, Maas RL. 2000. BMP4 rescues a non-cell-autonomous function of Msx1 in tooth development. Development 127: 4711-4718.
6. Bernanke DH, Markwald RR. 1982. Migratory behavior of cardiac cushion tissue cells in a collagen-lattice culture system. Dev Biol 91: 235-245.
7. Butcher JT, Markwald RR. 2007. Valvulogenesis: the moving target. Philos Trans R Soc Lond B Biol Sci 362: 1489-1503.
8. 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.
9. Chen YH, Ishii M, Sucov HM, Maxson RE Jr. 2008. Msx1 and Msx2 are required for endothelial-mesenchymal transformation of the atrioventricular cushions and patterning of the atrioventricular myocardium. BMC Dev Biol 8: 75.
10. Chu GC, Dunn NR, Anderson DC, Oxburgh L, Robertson EJ. 2004. Differential requirements for Smad4 in TGFbeta-dependent patterning of the early mouse embryo. Development 131: 3501-3512.
11. Clark KL, Yutzey KE, Benson DW. 2006. Transcription factors and congenital heart defects. Annu Rev Physiol 68: 97-121.
12. de Caestecker M. 2004. The transforming growth factor-beta superfamily of receptors. Cytokine Growth Factor Rev 15: 1-11.
13. de la Cruz MV, Markwald RR, Krug EL, Rumenoff L, Sanchez Gomez C, Sadowinski S, Galicia TD, Gomez F, Salazar Garcia M, Villavicencio Guzman L, Reyes Angeles L, Moreno-Rodriguez RA. 2001. Living morphogenesis of the ventricles and congenital pathology of their component parts. Cardiol Young 11: 588-600.
14. Eisenberg LM, Markwald RR. 1995. Molecular regulation of atrioventricular valvuloseptal morphogenesis. Circ Res 77: 1-6.
15. Feng XH, Derynck R. 2005. Specificity and versatility in tgf-beta signaling through Smads. Annu Rev Cell Dev Biol 21: 659-693.
16. 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.
17. Gaussin V, Van de Putte T, Mishina Y, Hanks MC, Zwijsen A, Huylebroeck D, Behringer RR, Schneider MD. 2002. Endocardial cushion and myocardial defects after cardiac myocyte- specific conditional deletion of the bone morphogenetic protein receptor ALK3. Proc Natl Acad Sci USA 99: 2878-2883.
18. Gautschi O, Tepper CG, Purnell PR, Izumiya Y, Evans CP, Green TP, Desprez PY, Lara PN, Gandara DR, Mack PC, Kung HJ. 2008. Regulation of Id1 expression by SRC: implications for targeting of the bone morphogenetic protein pathway in cancer. Cancer Res 68: 2250-2258.
19. Gitler AD, Lu MM, Jiang YQ, Epstein JA, Gruber PJ. 2003. Molecular markers of cardiac endocardial cushion development. Dev Dyn 228: 643-650.
20. Gittenberger-de Groot AC, Bartelings MM, Deruiter MC, Poelmann RE. 2005. Basics of cardiac development for the understanding of congenital heart malformations. Pediatr Res 57: 169-176.
21. Gustafsson E, Brakebusch C, Hietanen K, Fassler R. 2001. Tie-1-directed expression of Cre recombinase in endothelial cells of embryoid bodies and transgenic mice. J Cell Sci 114: 671-676.
22. Hoffman JI. 1995. Incidence of congenital heart disease: II. Prenatal incidence. Pediatr Cardiol 16: 155-165.
23. Hoffman JI, Kaplan S. 2002. The incidence of congenital heart disease. J Am Coll Cardiol 39: 1890-1900.
24. Hogan BL. 1996. Bone morphogenetic proteins: multifunctional regulators of vertebrate development. Genes Dev 10: 1580-1594.
25. Hussein SM, Duff EK, Sirard C. 2003. Smad4 and beta-catenin co-activators functionally interact with lymphoid-enhancing factor to regulate graded expression of Msx2. J Biol Chem 278: 48805-48814.
26. Inai K, Norris RA, Hoffman S, Markwald RR, Sugi Y. 2008. BMP-2 induces cell migration and periostin expression during atrioventricular valvulogenesis. Dev Biol 315: 383-396.
27. Jia Q, McDill BW, Li SZ, Deng C, Chang CP, Chen F. 2007. Smad signaling in the neural crest regulates cardiac outflow tract remodeling through cell autonomous and non-cell autonomous effects. Dev Biol 311: 172-184.
28. Jiao K, Zhou Y, Hogan BL. 2002. Identification of mZnf8, a mouse Kruppel-like transcriptional repressor, as a novel nuclear interaction partner of Smad1. Mol Cell Biol 22: 7633-7644.
29. Jiao K, Kulessa H, Tompkins K, Zhou Y, Batts L, Baldwin HS, Hogan BL. 2003. An essential role of Bmp4 in the atrioventricular septation of the mouse heart. Genes Dev 17: 2362-2367.
30. Kishigami S, Mishina Y. 2005. BMP signaling and early embryonic patterning. Cytokine Growth Factor Rev 16: 265-278.
31. Ko SO, Chung IH, Xu X, Oka S, Zhao H, Cho ES, Deng C, Chai Y. 2007. Smad4 is required to regulate the fate of cranial neural crest cells. Dev Biol 312: 435-447.
32. 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.
33. 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.
34. Mandel EM, Kaltenbrun E, Callis TE, Zeng XX, Marques SR, Yelon D, Wang DZ, Conlon FL. 2010. The BMP pathway acts to directly regulate Tbx20 in the developing heart. Development 137: 1919-1929.
35. Markwald RR, Krook JM, Kitten GT, Runyan RB. 1981. Endocardial cushion tissue development: structural analyses on the attachment of extracellular matrix to migrating mesenchymal cell surfaces. Scan Electron Microsc 261-274.
36. Massague J, Gomis RR. 2006. The logic of TGFbeta signaling. FEBS Lett 580: 2811-2820.
37. Massague J, Seoane J, Wotton D. 2005. Smad transcription factors. Genes Dev 19: 2783-2810.
38. Miyazono K, Kamiya Y, Morikawa M. 2010. Bone morphogenetic protein receptors and signal transduction. J Biochem 147: 35-51.
39. Moustakas A, Heldin CH. 2005. Non-Smad TGF-beta signals. J Cell Sci 118: 3573-3584.
40. Nie X, Deng CX, Wang Q, Jiao K. 2008. Disruption of Smad4 in neural crest cells leads to mid-gestation death with pharyngeal arch, craniofacial and cardiac defects. Dev Biol 316: 417-430.
41. Onuzo OC. 2006. How effectively can clinical examination pick up congenital heart disease at birth? Arch Dis Child Fetal Neonatal Ed 91: F236-237.
42. Park C, Lavine K, Mishina Y, Deng CX, Ornitz DM, Choi K. 2006. Bone morphogenetic protein receptor 1A signaling is dispensable for hematopoietic development but essential for vessel and atrioventricular endocardial cushion formation. Development 133: 3473-3484.
43. Person AD, Klewer SE, Runyan RB. 2005. Cell biology of cardiac cushion development. Int Rev Cytol 243: 287-335.
44. Qi X, Yang G, Yang L, Lan Y, Weng T, Wang J, Wu Z, Xu J, Gao X, Yang X. 2007. Essential role of Smad4 in maintaining cardiomyocyte proliferation during murine embryonic heart development. Dev Biol 311: 136-146.
45. Rivera-Feliciano J, Tabin CJ. 2006. Bmp2 instructs cardiac progenitors to form the heart-valve-inducing field. Dev Biol 295:580-588.
46. Rivera-Feliciano J, Lee KH, Kong SW, Rajagopal S, Ma Q, Springer Z, Izumo S, Tabin CJ, Pu WT. 2006. Development of heart valves requires Gata4 expression in endothelial-derived cells. Development 133: 3607-3618.
47. Schroeder JA, Jackson LF, Lee DC, Camenisch TD. 2003. Form and function of developing heart valves: coordination by extracellular matrix and growth factor signaling. J Mol Med 81: 392-403.
48. Shelton EL, Yutzey KE. 2007. Tbx20 regulation of endocardial cushion cell proliferation and extracellular matrix gene expression. Dev Biol 302: 376-388.
49. Sirard C, de la Pompa JL, Elia A, Itie A, Mirtsos C, Cheung A, Hahn S, Wakeham A, Schwartz L, Kern SE, Rossant J, Mak TW. 1998. The tumor suppressor gene Smad4/Dpc4 is required for gastrulation and later for anterior development of the mouse embryo. Genes Dev 12: 107-119.
50. Song L, Fassler R, Mishina Y, Jiao K, Baldwin HS. 2007a. Essential functions of Alk3 during AV cushion morphogenesis in mouse embryonic hearts. Dev Biol 301: 276-286.
51. Song L, Yan W, Chen X, Deng CX, Wang Q, Jiao K. 2007b. Myocardial Smad4 is essential for cardiogenesis in mouse embryos. Circ Res 101: 277-285.
52. Sugi Y, Yamamura H, Okagawa H, Markwald RR. 2004. Bone morphogenetic protein-2 can mediate myocardial regulation of atrioventricular cushion mesenchymal cell formation in mice. Dev Biol 269: 505-518.
53. Takaku K, Oshima M, Miyoshi H, Matsui M, Seldin MF, Taketo MM. 1998. Intestinal tumorigenesis in compound mutant mice of both Dpc4 (Smad4) and Apc genes. Cell 92: 645-656.
54. ten Dijke P, Hill CS. 2004. New insights into TGF-beta-Smad signalling. Trends Biochem Sci 29: 265-273.
55. von Bubnoff A, Cho KW. 2001. Intracellular BMP signaling regulation in vertebrates: pathway or network? Dev Biol 239: 1-14.
56. Wagner M, Siddiqui MA. 2007. Signal transduction in early heart development (II): ventricular chamber specification, trabeculation, and heart valve formation. Exp Biol Med (Maywood) 232: 866-880.
57. 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.
58. Yang X, Li C, Xu X, Deng C. 1998. The tumor suppressor SMAD4/DPC4 is essential for epiblast proliferation and mesoderm induction in mice. Proc Natl Acad Sci USA 95: 3667-3672.
59. Yang X, Li C, Herrera PL, Deng CX. 2002. Generation of Smad4/Dpc4 conditional knockout mice. Genesis 32: 80-81.
60. Zhou B, Wu B, Tompkins KL, Boyer KL, Grindley JC, Baldwin HS. 2005. Characterization of Nfatc1 regulation identifies an enhancer required for gene expression that is specific to pro-valve endocardial cells in the developing heart. Development 132: 1137-1146.