Molecular mechanisms controlling the coupled development of myocardium and coronary vasculature

Clinical Science

Volumn 111, Issue 1, 2006, Pages 35-46

  Bhattacharya, Shoumo ^a   MacDonald, Simon T ^a   Farthing, Cassandra R ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Endothelium; Heart failure; Mouse genetics; Myocardium; Neural crest; Proepicardial organ; Vasculature

Indexed keywords

BONE MORPHOGENETIC PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR 2; FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR RECEPTOR 1; FIBROBLAST GROWTH FACTOR RECEPTOR 2; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; STRUCTURAL PROTEIN; SYNAPTOPHYSIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GATA 4; TRANSCRIPTION FACTOR PAX3; VASCULOTROPIN; VASCULOTROPIN A; WT1 PROTEIN;

APOPTOSIS; CELL CYCLE; CELL DIVISION; CORONARY BLOOD VESSEL; EMBRYO DEVELOPMENT; ENERGY METABOLISM; EXPERIMENTAL MODEL; GENE DELETION; GENE MUTATION; HEART FAILURE; HEART MUSCLE; HEART MUSCLE CELL; HYPOXIA; ISCHEMIC HEART DISEASE; MUTATION; MYOCARDIAL DISEASE; NONHUMAN; PRIORITY JOURNAL; RECEPTOR BINDING; REVIEW;

ANIMALS; CORONARY VESSELS; FETAL DEVELOPMENT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEART; HEART FAILURE, CONGESTIVE; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; MUTATION; MYOCYTES, CARDIAC;

EID: 33745765249     PISSN: 01435221     EISSN: None     Source Type: Journal    
DOI: 10.1042/CS20060003     Document Type: Review

References (196)

1. Petersen, S., Rayner, M. and Wolstenholme, J. (2002) Coronary Heart Disease Statistics: Heart Failure Supplement, British Heart Foundation Statistics, London
2. McMurray, J. J. and Pfeffer, M. A. (2005) Heart failure. Lancet 365, 1877-1889
3. Colucci, W. S. and Braunwald, E. (2001) Pathophysiology of heart failure. In Heart Disease: a Textbook of Cardiovascular Medicine, 6th edn (Braunwald, E., Zipes, D. P. and Libby, P., eds.), pp. 503-533, W. B. Saunders, Philadelphia
4. Andersson, B. and Swedberg, K. (2003) Management of overt heart failure. In Evidence-Based Cardiology, 2nd edn (Yusuf, S., Cairns, J. A., Camm, A. J., Fallen, E. L. and Gersh, B. J., eds.), pp. 659-680, BMJ Books, London
5. Caplice, N. M. and Deb, A. (2004) Myocardial-cell replacement: the science, the clinic and the future. Nat. Clin. Pract. Cardiovasc. Med. 1, 90-95
6. Rumyantsev, P. P. (1977) Interrelations of the proliferation and differentiation processes during cardiac myogenesis and regeneration. Int. Rev. Cytol. 51, 186-273
7. Anversa, P. and Nadal-Ginard, B. (2002) Myocyte renewal and ventricular remodelling. Nature (London) 415, 240-243
8. Nadal-Ginard, B., Kajstura, J., Leri, A. and Anversa, P. (2003) Myocyte death, growth, and regeneration in cardiac hypertrophy and failure. Circ. Res. 92, 139-150
9. Mummery, C. L. (2005) Cardiology: solace for the broken-hearted? Nature (London) 433, 585-587
10. Murry, C. E., Soonpaa, M. H., Reinecke, H. et al. (2004) Haematopoietic stem cells do not transdifferentiate into cardiac myocytes in myocardial infarcts. Nature (London) 428, 664-668
11. Balsam, L. B., Wagers, A. J., Christensen, J. L., Kofidis, T., Weissman, I. L. and Robbins, R. C. (2004) Haematopoietic stem cells adopt mature haematopoietic fates in ischaemic myocardium. Nature (London) 428, 668-673
12. Chien, K. R. (2004) Stem cells: lost in translation. Nature (London) 428, 607-608
13. Pasumarthi, K. B. and Field, L. J. (2002) Cardiomyocyte cell cycle regulation. Circ. Res. 90, 1044-1054
14. Harvey, R. P. (2002) Patterning the vertebrate heart. Nat. Rev. Genet. 3, 544-556
15. Kelly, R. G. and Buckingham, M. E. (2002) The anterior heart-forming field: voyage to the arterial pole of the heart. Trends Genet. 18, 210-216
16. Solloway, M. J. and Harvey, R. P. (2003) Molecular pathways in myocardial development: a stem cell perspective. Cardiovasc. Res. 58, 264-277
17. Kelly, R. G., Brown, N. A. and Buckingham, M. E. (2001) The arterial pole of the mouse heart forms from Fgf10-expressing cells in pharyngeal mesoderm. Dev. Cell. 1, 435-440
18. Cai, C. L., Liang, X., Shi, Y. et al. (2003) Isl1 identifies a cardiac progenitor population that proliferates prior to differentiation and contributes a majority of cells to the heart. Dev. Cell. 5, 877-889
19. Zaffran, S., Kelly, R. G., Meilhac, S. M., Buckingham, M. E. and Brown, N. A. (2004) Right ventricular myocardium derives from the anterior heart field. Circ. Res. 95, 261-268
20. Sucov, H. M. (1998) Molecular insights into cardiac development. Annu. Rev. Physiol. 60, 287-308
21. Chen, T. H., Chang, T. C., Kang, J. O. et al. (2002) Epicardial induction of fetal cardiomyocyte proliferation via a retinoic acid-inducible trophic factor. Dev. Biol. 250, 198-207
22. Sedmera, D., Pexieder, T, Vuillemin, M., Thompson, R. P. and Anderson, R. H. (2000) Developmental patterning of the myocardium. Anat. Rec. 258, 319-337
23. Meilhac, S. M., Esner, M., Kelly, R. G., Nicolas, J. F. and Buckingham, M. E. (2004) The clonal origin of myocardial cells in different regions of the embryonic mouse heart. Dev. Cell. 6, 685-698
24. Meilhac, S. M., Kelly, R. G., Rocancourt, D., Eloy-Trinquet, S., Nicolas, J. F. and Buckingham, M. E. (2003) A retrospective clonal analysis of the myocardium reveals two phases of clonal growth in the developing mouse heart. Development 130, 3877-3889
25. Reese, D. E., Mikawa, T. and Bader, D. M. (2002) Development of the coronary vessel system. Circ. Res. 91, 761-768
26. Luttun, A. and Carmeliet, P. (2003) De novo vasculogenesis in the heart. Cardiovasc. Res. 58, 378-389
27. Moore, A. W., McInnes, L., Kreidberg, J., Hastie, N. D. and Schedl, A. (1999) YAC complementation shows a requirement for Wt1 in the development of epicardium, adrenal gland and throughout nephrogenesis. Development 126, 1845-1857
28. Merki, E., Zamora, M., Raya, A. et al. (2005) Epicardial retinoid X receptor a is required for myocardial growth and coronary artery formation. Proc. Natl. Acad. Sci. U.S.A. 102, 18455-18460
29. Mikawa, T. and Gourdie, R. G. (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
30. Viragh, S. and Challice, C. E. (1981) The origin of the epicardium and the embryonic myocardial circulation in the mouse. Anat. Rec. 201, 157-168
31. Balsam, L. B. and Robbins, R. C. (2005) Haematopoietic stem cells and repair of the ischaemic heart. Clin. Sci. 109, 483-492
32. Menasche, P. (2005) The potential of embryonic stem cells to treat heart disease. Curr. Opin. Mol. Ther. 7, 293-299
33. Zambrowicz, B. P. and Sands, A. T. (2003) Knockouts model the 100 best-selling drugs-will they model the next 100? Nat. Rev. Drug Discovery 2, 38-51
34. Ruiz-Lozano, P. and Chien, K. R. (2003) Cre-constructing the heart. Nat. Genet. 33, 8-9
35. Moses, K. A., DeMayo, F., Braun, R. M., Reecy, J. L. and Schwartz, R. J. (2001) Embryonic expression of an Nkx2-Nkx5/Cre gene using ROSA26 reporter mice. Genesis 31, 176-180
36. McFadden, D. G., Barbosa, A. G., Richardson, J. A., Schneider, M. D., Srivastava, D. and Olson, E. N. (2005) The Hand1 and Hand2 transcription factors regulate expansion of the embryonic cardiac ventricles in a gene dosage-dependent manner. Development 132, 189-201
37. Chen, J., Rubalak, S. W., Minamisawa, S. et al. (1998) Selective requirement of myosin light chain 2v in embryonic heart function. J. Biol. Chem. 273, 1252-1256
38. Wegener, J. W., Nawrath, H., Wolfsgruber, W. et al. (2002) cGMP-dependent protein kinase I mediates the negative inotropic effect of cGMP in the murine myocardium. Circ. Res. 90, 18-20
39. Parlakian, A., Tuil, D., Hamard, G. et al. (2004) Targeted inactivation of serum response factor in the developing heart results in myocardial defects and embryonic lethality. Mol. Cell. Biol. 24, 5281-5289
40. Agah, R., Frenkel, P. A., French, B. A., Michael, L. H., Overbeek, P. A. and Schneider, M. D. (1997) Gene recombination in postmitotic cells. Targeted expression of Cre recombinase provokes cardiac-restricted, site-specific rearrangement in adult ventricular muscle in vivo. J. Clin. Invest. 100, 169-179
41. Jiang, X., Rowitch, D. H., Soriano, P., McMahon, A. P. and Sucov, H. M. (2000) Fate of the mammalian cardiac neural crest. Development 127, 1607-1616
42. Kisanuki, Y. Y., Hammer, R. E., Miyazaki, J., Williams, S. C., Richardson, J. A. and Yanagisawa, M. (2001) Tie2-Cre transgemc mice: a new model for endothelial cell-lineage analysis in vivo. Dev. Biol. 230, 230-242
43. Barak, Y., Nelson, M. C., Ong, E. S. et al. (1999) PPAR gamma is required for placental, cardiac, and adipose tissue development. Mol. Cell 4, 585-595
44. May, S. R., Stewart, N. J., Chang, W. and Peterson, A. S. (2004) A Titin mutation defines roles for circulation in endothelial morphogenesis. Dev. Biol. 270, 31-46
45. Ozcelik, C., Erdmann, B., Pilz, B. et al. (2002) Conditional mutation of the ErbB2 (HER2) receptor in cardiomyocytes leads to dilated cardiomyopathy. Proc. Natl. Acad. Sci. U.S.A. 99, 8880-8885
46. Chen, J., Kubalak, S. W. and Chien, K. R. (1998) Ventricular muscle-restricted targeting of the RXRtα gene reveals a non-cell-autonomous requirement in cardiac chamber morphogenesis. Development 125, 1943-1949
47. Hirota, H., Chen, J., Betz, U. A. et al. (1999) Loss of a gp130 cardiac muscle cell survival pathway is a critical event in the onset of heart failure during biomechanical stress. Cell 97, 189-198
48. Gutstein, D. E., Morley, G. E., Tamaddon, H. et al. (2001) Conduction slowing and sudden arrhythmic death in mice with cardiac-restricted inactivation of connexin43. Circ. Res. 88, 333-339
49. Wettschureck, N., Rutten, H., Zywietz, A. et al. (2001) Absence of pressure overload induced myocardial hypertrophy after conditional inactivation of Gαq/Gα11 in cardiomyocytes. Nat. Med. 7, 1236-1240
50. Giordano, F. J., Gerber, H. P., Williams, S. P. et al. (2001) A cardiac myocyte vascular endothelial growth factor paracrine pathway is required to maintain cardiac function. Proc. Natl. Acad. Sci. U.S.A. 98, 5780-5785
51. Gaussin, V., Van De Putte, T., Mishina, Y. et al. (2002) Endocardial cushion and myocardial defects after cardiac myocyte-specific conditional deletion of the bone morphogenetic protein receptor ALK3. Proc. Natl. Acad. Sci. U.S.A. 99, 2878-2883
52. Lavine, K. J., Yu, K., White, A. C. et al. (2005) Endocardial and epicardial derived FGF signals regulate myocardial proliferation and differentiation in vivo. Dev. Cell. 8, 85-95
53. Zeisberg, E. M., Ma, Q., Juraszek, A. L. et al. (2005) Morphogenesis of the right ventricle requires myocardial expression of Gata4. J. Clin. Invest. 115, 1522-1531
54. Conrad, M., Jakupoglu, C., Moreno, S. G. et al. (2004) Essential role for mitochondrial thioredoxin reductase in hematopoiesis, heart development, and heart function. Mol. Cell. Biol. 24, 9414-9423
55. Wu, H., Lee, S. H., Gao, J., Liu, X. and Iruela-Arispe, M. L. (1999) Inactivation of erythropoietin leads to defects in cardiac morphogenesis. Development 126, 3597-3605
56. Pu, W. T., Ishiwata, T., Juraszek, A. L., Ma, Q. and Izumo, S. (2004) GATA4 is a dosage-sensitive regulator of cardiac morphogenesis. Dev. Biol. 275, 235-244
57. Nebigil, C. G., Choi, D. S., Dierich, A. et al. (2000) Serotonin 2B receptor is required for heart development. Proc. Natl. Acad. Sci. U.S.A. 97, 9508-9513
58. Koera, K., Nakamura, K., Nakao, K. et al. (1997) K-ras is essential for the development of the mouse embryo. Oncogene 15, 1151-1159
59. Wang, X., Merritt, A. J., Seyfried, J. et al. (2005) Targeted deletion of mek5 causes early embryonic death and defects in the extracellular signal-regulated kinase 5/myocyte enhancer factor 2 cell survival pathway. Mol. Cell. Biol. 25, 336-345
60. Tullio, A. N., Accili, D., Ferrans, V. J. et al. (1997) Nonmuscle myosin II-B is required for normal development of the mouse heart. Proc. Natl. Acad. Sci. U.S.A. 94, 12407-12412
61. Bushdid, P. B., Osinska, H., Waclaw, R. R., Molkentin, J. D. and Yutzey, K. E. (2003) NFATc3 and NFATc4 are required for cardiac development and mitochondrial function. Circ. Res. 92, 1305-1313
62. Cai, C. L., Zhou, W., Yang, E. et al. (2005) T-box genes coordinate regional rates of proliferation and regional specification during cardiogenesis. Development 132, 2475-2487
63. Engel, F. B., Schebesta, M., Duong, M. T. et al. (2005) p38 MAP kinase inhibition enables proliferation of adult mammalian cardiomyocytes. Genes Dev. 19, 1175-1187
64. Gitler, A. D., Zhu, Y., Ismat, F. A. et al. (2003) Nf1 has an essential role in endothelial cells. Nat. Genet. 33, 75-79
65. Hayashi, M., Kim, S.-W., Imanaka-Yoshida, K. et al. (2004) Targeted deletion of BMK1/ERK5 in adult mice perturbs vascular integrity and leads to endothelial failure. J. Clin. Invest. 113, 1138-1148
66. Gerety, S. S. and Anderson, D. J. (2002) Cardiovascular ephrinB2 function is essential for embryonic angiogenesis. Development 129, 1397-1410
67. Kang, T. B., Ben-Moshe, T, Varfolomeev, E. E. et al. (2004) Caspase-8 serves both apoptotic and nonapoptotic roles. J. Immunol. 173, 2976-2984
68. Tachibana, K., Jones, N., Dumont, D. J., Puri, M. C. and Bernstein, A. (2005) Selective role of a distinct tyrosine residue on Tie2 in heart development and early hematopoiesis. Mol. Cell. Biol. 25, 4693-4702
69. Dumont, D. J., Gradwohl, G., Fong, G. H. et al. (1994) Dominant-negative and targeted null mutations in the endothelial receptor tyrosine kinase, tek, reveal a critical role in vasculogenesis of the embryo. Genes Dev. 8, 1897-1909
70. Niederreither, K., Subbarayan, V., Dolle, P. and Chambon, P. (1999) Embryonic retinoic acid synthesis is essential for early mouse post-implantation development. Nat. Genet. 21, 444-448
71. Tevosian, S. G., Deconinck, A. E., Tanaka, M. et al. (2000) FOG-2, a cofactor for GATA transcription factors, is essential for heart morphogenesis and development ot coronary vessels from epicardium. Cell 101, 729-739
72. Stottmann, R. W., Choi, M., Mishina, Y., Meyers, E. N. and Klingensmith, J. (2004) BMP receptor IA is required in mammalian neural crest cells for development of the cardiac outflow tract and ventricular myocardium. Development 131, 2205-2218
73. Li, J., Liu, K. C., Jin, F., Lu, M. M. and Epstein, J. A. (1999) Transgenic rescue of congenital heart disease and spina bifida in Splotch mice. Development 126, 2495-2503
74. Ornitz, D. M., Xu, J., Colvin, J. S. et al. (1996) Receptor specificity of the fibroblast growth factor family. J. Biol. Chem. 271, 15292-15297
75. Mazerbourg, S., Sangkuhl, K., Luo, C. W., Sudo, S., Klein, C. and Hsueh, A. J. (2005) Identification of receptors and signaling pathways for orphan bone morphogenetic protein/growth differentiation factor ligands based on genomic analyses. J. Biol. Chem. 280, 32122-32132
76. Neuhaus, H., Rosen, V. and Thies, R. S. (1999) Heart specific expression of mouse BMP-10 a novel member of the TGF-β superfamily. Mech. Dev, 80, 181-184
77. Harris, A. L. (2002) Hypoxia: a key regulatory factor in tumour growth. Nat. Rev. Cancer 2, 38-47
78. Compernolle, V., Brusselmans, K., Franco, D. et al. (2003) Cardia bifida, defective heart development and abnormal neural crest migration in embryos lacking hypoxia-inducible factor-1α. Cardiovasc. Res. 60, 569-579
79. Cowden Dahl, K. D., Fryer, B. H., Mack, F. A. et al. (2005) Hypoxia-inducible factors 1α and 2α regulate trophoblast differentiation. Mol. Cell. Biol. 25, 10479-10491
80. Licht, A. H., Muller-Holtkamp, R, Flamme, I. and Breier, G. (2005) Inhibition of hypoxia-inducible factor activity in endothelial cells disrupts embryonic cardiovascular development. Blood 107, 584-590
81. Caron, K. M. and Smithies, O. (2001) Extreme hydrops fetalis and cardiovascular abnormalities in mice lacking a functional Adrenomedullin gene. Proc. Natl. Acad. Sci. U.S.A. 98, 615-619
82. Hopkins, A. L. and Groom, C. R. (2002) The druggable genome. Nat. Rev. Drug Discovery 1, 727-730
83. Pugh, C. W. and Ratcliffe, P. (2003) Regulation of angiogenesis by hypoxia: role of the HIF system. Nat. Med. 9, 677-684
84. Sari, Y. and Zhou, F. C. (2003) Serotonin and its transporter on proliferation of fetal heart cells. Int. J. Dev. Neurosci. 21, 417-424
85. Zhao, Y. Y., Sawyer, D. R., Baliga, R. R. et al. (1998) Neuregulins promote survival and growth of cardiac myocytes. Persistence of ErbB2 and ErbB4 expression in neonatal and adult ventricular myocytes. J. Biol. Chem. 273, 10261-10269
86. Stuckmann, I., Evans, S. and Lassar, A. B. (2003) Erythropoietin and retinoic acid, secreted from the epicardium, are required for cardiac myocyte proliferation. Dev. Biol. 255, 334-349
87. Wald, M. R., Borda, E. S. and Sterin-Borda, L. (1996) Mitogenic effect of erythropoietin on neonatal rat cardiomyocytes: signal transduction pathways. J. Cell Physiol. 167, 461-468
88. Crottogini, A., Meckert, P. C., Vera Janavel, G. et al. (2003) Arteriogenesis induced by intramyocardial vascular endothelial growth factor 165 gene transfer in chronically ischemic pigs. Hum. Gene Ther. 14, 1307-1318
89. Laguens, R., Cabeza Meckert, P., Vera Janavel, G. et al. (2002) Entrance in mitosis of adult cardiomyocytes in ischemic pig hearts after plasmid-mediated rhVEGF165 gene transfer. Gene Ther. 9, 1676-1681
90. Narmoneva, D. A., Vukmirovic, R., Davis, M. E., Kamm, R. D. and Lee, R. T. (2004) Endothelial cells promote cardiac myocyte survival and spatial reorganization: implications for cardiac regeneration. Circulation 110, 962-968
91. Camelliti, P., McCulloch, A. D. and Kohl, P. (2005) Microstructured cocultures of cardiac myocytes and fibroblasts: a two-dimensional in vitro model of cardiac tissue. Microsc. Microanal. 11, 249-259
92. Radisic, M., Park, H., Shing, H. et al. (2004) Functional assembly of engineered myocardium by electrical stimulation of cardiac myocytes cultured on scaffolds. Proc. Natl. Acad. Sci. U.S.A. 101, 18129-18134
93. Suri, C., Jones, P. F., Patan, S. et al. (1996) Requisite role of angiopoietin-1, a ligand for the TIE2 receptor, during embryonic angiogenesis. Cell 87, 1171-1180
94. Chen, H., Shi, S., Acosta, L. et al. (2004) BMP10 is essential for maintaining cardiac growth during murine cardiogenesis. Development 131, 2219-2231
95. Krebs, L. T., Shutter, J. R., Tanigaki, K., Honjo, T., Stark, K. L. and Gridley, T. (2004) Haploinsufficient lethality and formation of arteriovenous malformations in Notch pathway mutants. Genes Dev. 18, 2469-2473
96. Gale, N. W., Dominguez, M. G., Noguera, I. et al. (2004) Haploinsufficiency of delta-like 4 ligand results in embryonic lethality due to major defects in arterial and vascular development. Proc. Natl. Acad. Sci. U.S.A. 101, 15949-15954
97. Duarte, A., Hirashima, M., Benedito, R. et al. (2004) Dosage-sensitive requirement for mouse Dl14 in artery development. Genes Dev. 18, 2474-2478
98. Wang, H. U., Chen, Z. F. and Anderson, D. J. (1998) Molecular distinction and angiogenic interaction between embryonic arteries and veins revealed by ephrin-B2 and its receptor Eph-B4. Cell 93, 741-753
99. Colvin, J. S., White, A. C., Pratt, S. J. and Ornitz, D. M. (2001) Lung hypoplasia and neonatal death in Fgf9-null mice identify this gene as an essential regulator of lung mesenchyme. Development 128, 2095-2106
100. McCright, B., Gao, X., Shen, L. et al. (2001) Defects in development of the kidney, heart and eye vasculature in mice homozygous for a hypomorphic Notch2 mutation. Development 128, 491-502
101. McCright, B., Lozier, J. and Gridley, T. (2002) A mouse model of Alagille syndrome: Notch2 as a genetic modifier of Jag1 haploinsufficiency. Development 129, 1075-1082
102. Vincent, S. D., Norris, D. P., Ann Le Good, J., Constam, D. B. and Robertson, E. J. (2004) Asymmetric Nodal expression in the mouse is governed by the combinatorial activities of two distinct regulatory elements. Mech. Dev. 121, 1403-1415
103. Meyer, D. and Birchmeier, C. (1995) Multiple essential functions of neuregulin in development. Nature (London) 378, 386-390
104. Kramer, R., Bucay, N., Kane, D. J., Martin, L. E., Tarpley, J. E. and Theill, L. E. (1996) Neuregulins with an Ig-like domain are essential for mouse myocardial and neuronal development. Proc. Natl. Acad. Sci U.S.A. 93, 4833-4838
105. Jaber, M., Koch, W. J., Rockman, H. et al. (1996) Essential role of beta-adrenergic receptor kinase 1 in cardiac development and function. Proc. Natl. Acad. Sci. U.S.A. 93, 12974-12979
106. Urness, L. D., Sorensen, L. K. and Li, D. Y. (2000) Arteriovenous malformations in mice lacking activin receptor-like kinase-1. Nat. Genet. 26, 328-331
107. Sorensen, L. K., Brooke, B. S., Li, D. Y. and Urness, L. D. (2003) Loss of distinct arterial and venous boundaries in mice lacking endoglin, a vascular-specific TGFβ coreceptor. Dev. Biol. 261, 235-250
108. Dorner, A. A., Wegmann, F., Butz, S. et al. (2005) Coxsackievirus- adenovirus receptor (CAR) is essential for early embryonic cardiac development. J. Cell Sci. 118, 3509-3521
109. Asher, D. R., Cerny, A. M., Weiler, S. R. et al. (2005) Coxsackievirus and adenovirus receptor is essential for cardiomyocyte development. Genesis 42, 77-85
110. Lee, K. F., Simon, H., Chen, H., Bates, B., Hung, M. C. and Hauser, C. (1995) Requirement for neuregulin receptor erbB2 in neural and cardiac development. Nature (London) 378, 394-398
111. Erickson, S. L., O'Shea, K. S., Ghaboosi, N. et al. (1997) ErbB3 is required for normal cerebellar and cardiac development: a comparison with ErbB2- and heregulin-deficient mice. Development 124, 4999-5011
112. Gassmann, M., Casagranda, F., Orioli, D. et al. (1995) Aberrant neural and cardiac development in mice lacking the ErbB4 neuregulin receptor. Nature (London) 378, 390-394
113. Yoshida, K., Taga, T., Saito, M. et al. (1996) Targeted disruption of gp130, a common signal transducer for the interleukin 6 family of cytokines, leads to myocardial and hematological disorders. Proc. Natl. Acad. Sci. U.S.A. 93, 407-411
114. Price, R. L., Thielen, T. E., Borg, T. K. and Terracio, L. (2001) Cardiac defects associated with the absence of the platelet-derived growth factor a receptor in the patch mouse. Microsc. Microanal. 7, 56-65
115. Stenvers, K. L., Tursky, M. L., Harder, K. W. et al. (2003) Heart and liver defects and reduced transforming growth factor β2 sensitivity in transforming growth factor β type III receptor-deficient embryos. Mol. Cell. Biol. 23, 4371-4385
116. Shou, W., Aghdasi, B., Armstrong, D. L. et al. (1998) Cardiac defects and altered ryanodine receptor function in mice lacking FKBP12. Nature (London) 391, 489-492
117. Offermanns, S., Zhao, L. P., Gohla, A., Sarosi, I., Simon, M. I. and Wilkie, T. M. (1998) Embryonic cardiomyocyte hypoplasia and craniofacial defects in Gαq/Gα11-mutant mice. EMBO J. 17, 4304-4312
118. Yang, J., Boerm, M., McCarty, M. et al. (2000) Mekk3 is essential for early embryonic cardiovascular development. Nat. Genet. 24, 309-313
119. Tamura, K., Sudo, T., Senftleben, U., Dadak, A. M., Johnson, R. and Karin, M. (2000) Requirement for p38α in erythropoietin expression: a role for stress kinases in erythropoiesis. Cell 102, 221-231
120. Jacks, T., Shih, T. S., Schmitt, E. M., Bronson, R. T., Bernards, A. and Weinberg, R. A. (1994) Tumour predisposition in mice heterozygous for a targeted mutation in Nf1. Nat. Genet. 7, 353-361
121. Brannan, C. I., Perkins, A. S., Vogel, K. S. et al. (1994) Targeted disruption of the neurofibromatosis type-1 gene leads to developmental abnormalities in heart and various neural crest-derived tissues. Genes Dev. 8, 1019-1029
122. Qu, J., Li, X., Novitch, B. G. et al. (2003) PAK4 kinase is essential for embryonic viability and for proper neuronal development. Mol. Cell. Biol. 23, 7122-7133
123. Hamada, K., Sasaki, T., Koni, P. A. et al. (2005) The PTEN/PI3K pathway governs normal vascular development and tumor angiogenesis. Genes Dev. 19, 2054-2065
124. Araki, T., Mohi, M. G., Ismat, F. A. et al. (2004) Mouse-model of Noonan syndrome reveals cell type- and gene dosage-dependent effects of Ptpn11 mutation. Nat. Med. 10, 849-857
125. Yao, T. P., Oh, S. P., Fuchs, M. et al. (1998) Gene dosage-dependent embryonic development and proliferation defects in mice lacking the transcriptional integrator p300. Cell 93, 361-372
126. Hoyt, P. R., Bartholomew, C., Davis, A. J. et al. (1997) The Evi1 proto-oncogene is required at midgestation for neural, heart, and paraxial mescnchyme development. Mech. Dev. 65, 55-70
127. Kume, T., Jiang, H., Topczewska, J. M. and Hogan, B. L. (2001) The murine winged helix transcription factors. Foxc1 and Foxc2, arc both required for cardiovascular development and somitogenesis. Genes Dev. 15, 2470-2482
128. Winnier, G. E., Kume, T., Deng, K. et al. (1999) Roles for the winged helix transcription factors MF1 and MEH1 in cardiovascular development revealed by nonallelic noncomplementation of null alleles. Dev. Biol. 213, 418-431
129. Von Both, I., Silvestri, C., Erdemir, T. et al. (2004) Foxh1 is essential for development of the anterior heart field. Dev. Cell 7, 331-345
130. Korver, W., Schilham, M. W., Moerer, P. et al. (1998) Uncoupling of S phase and mitosis in cardiomyocytes and hepatocytes lacking the winged-helix transcription factor Trident. Curr. Biol. 8, 1327-1330
131. Wang, B., Weidenfeld, J., Lu, M. M. et al. (2004) Foxp1 regulates cardiac outflow tract, endocardial cushion morphogenesis and myocyte proliferation and maturation. Development 131, 4477-4487
132. Crispino, J. D., Lodish, M. B., Thurberg, B. L. et al. (2001) Proper coronary vascular development and heart morphogenesis depend on interaction of GATA-4 with FOG cofactors. Genes Dev. 15, 839-844
133. Watt, A. J., Battle, M. A., Li, J. and Duncan, S. A. (2004) GATA4 is essential for formation of the proepicardium and regulates cardiogenesis. Proc. Natl. Acad. Sci. U.S.A. 101, 12573-12578
134. Chang, S., McKinsey, T. A., Zhang, C. L., Richardson, J. A., Hill, J. A. and Olson, E. N. (2004) Histone deacetylases 5 and 9 govern responsiveness of the heart to a subset of stress signals and play redundant roles in heart development. Mol. Cell. Biol. 24, 8467-8476
135. Fischer, A., Schumacher, N., Maier, M., Sendtner, M. and Gessler, M. (2004) The Notch target genes Hey1 and Hey2 are required for embryonic vascular development. Genes Dev. 18, 901-911
136. Kokubo, H., Miyagawa-Tomita, S., Nakazawa, M., Saga, Y. and Johnson, R. L. (2005) Mouse hesr1 and hesr2 genes are redundantly required to mediate Notch signaling in the developing cardiovascular system. Dev. Biol. 278, 301-309
137. Shin, C. H., Liu, Z. P., Passier, R. et al. (2002) Modulation of cardiac growth and development by HOP, an unusual homeodomain protein. Cell 110, 725-735
138. Chen, F., Kook, H., Milewski, R. et al. (2002) Hop is an unusual homeobox gene that modulates cardiac development. Cell 110, 713-723
139. Lee, Y., Song, A. J., Baker, R., Micales, B., Conway, S. J. and Lyons, G. E. (2000) Jumonji, a nuclear protein that is necessary for normal heart development. Circ. Res. 86, 932-938
140. Bi, W., Drake, C. J. and Schwarz, J. J. (1999) The transcription factor MEF2C-null mouse exhibits complex vascular malformations and reduced cardiac expression of angiopoietin 1 and VEGF. Dev. Biol. 211, 255-267
141. Lin, Q., Schwarz, J., Bucana, C. and Olson, E. N. (1997) Control of mouse cardiac morphogenesis and myogenesis by transcription factor MEF2C. Science 276, 1404-1407
142. Lin, Q., Lu, J., Yanagisawa, H. et al. (1998) Requirement of the MADS-box transcription factor MEF2C for vascular development. Development 125, 4565-4574
143. Bertolino, P., Radovanovic, I., Casse, H., Aguzzi, A., Wang, Z. Q. and Zhang, C. X. (2003) Genetic ablation of the tumor suppressor menin causes lethality at mid-gestation with defects m multiple organs. Mech. Dev. 120, 549-560
144. Oh, J., Richardson, J. A. and Olson, E. N. (2005) Requirement of myocardin-related transcription factor-B for remodeling of branchial arch arteries and smooth muscle differentiation. Proc. Natl. Acad. Sci. U.S.A. 102, 15122-15127
145. Tominaga, K., Kirtane, B., Jackson, J. G. et al. (2005) MRG15 regulates embryonic development and cell proliferation. Mol. Cell. Biol. 25, 2924-2937
146. Nagy, A., Moens, C., Ivanyi, E. et al. (1998) Dissecting the role of N-myc in development using a single targeting vector to generate a series of alleles. Curr. Biol. 8, 661-664
147. Kuang, S. Q., Liao, L., Zhang, H. et al. (2002) Deletion of the cancer-amplified coactivator A1B3 results in defective placentation and embryonic lethality. J. Biol. Chem. 277, 45356-45360
148. Lyons, I., Parsons, L. M., Hartley, L. et al. (1995) Myogenic and morphogenetic defects in the heart tubes of murine embryos lacking the homeo box gene Nkx2-Nkx5. Genes Dev. 9, 1654-1666
149. Tanaka, M., Wechsler, S. B., Lee, I. W., Yamasaki, N., Lawitts, J. A. and Izumo, S. (1999) Complex modular cis-acting elements regulate expression of the cardiac specifying homeobox gene Csx/Nkx2.5. Development 126, 1439-1450
150. Pereira, F. A., Qiu, Y., Zhou, G., Tsai, M. J. and Tsai, S. Y. (1999) The orphan nuclear receptor COUP-TFII is required for angiogenesis and heart development. Genes Dev. 13, 1037-1049
151. Wang, Z., Zhai, W., Richardson, J. A. et al. (2004) Polybromo protein BAF180 functions in mammalian cardiac chamber maturation. Genes Dev. 18, 3106-3116
152. Takihara, Y., Tomotsune, D., Shirai, M. et al. (1997) Targeted disruption of the mouse homologue of the Drosophila polyhomeotic gene leads to altered anteroposterior patterning and neural crest defects. Development 124, 3673-3682
153. Shirai, M., Osugi, T., Koga, H. et al. (2002) The Polycomb-group gene Rae28 sustains Nkx2.5/Csx expression and is essential for cardiac morphogenesis. J. Clin. Invest. 110, 177-184
154. Lin, C. R., Kioussi, C., O'Connell, S. et al. (1999) Pitx2 regulates lung asymmetry, cardiac positioning and pituitary and tooth morphogenesis. Nature (London) 401, 279-282
155. Lu, M. F., Pressman, C., Dyer, R., Johnson, R. L. and Martin, J. F. (1999) Function of Rieger syndrome gene in left-right asymmetry and craniofacial development. Nature (London) 401, 276-278
156. Ryan, A. K., Blumberg, B., Rodriguez-Esteban, C. et al. (1998) Pitx2 determines left-right asymmetry of internal organs in vertebrates. Nature (London) 394, 545-551
157. Landles, C., Chalk, S., Steel, J. H. et al. (2003) The thyroid hormone receptor-associated protein TRAP220 Is required at distinct embryonic stages in placental, cardiac, and hepatic development. Mol. Endocrinol. 17, 2418-2435
158. Crawford, S. E., Qi, C., Misra, P. et al. (2002) Defects of the heart, eye, and megakaryocytes in peroxisome proliferator activator receptor-binding protein (PBP) null embryos implicate GATA family of transcription factors. J. Biol. Chem. 277, 3585-3592
159. Mendelsohn, C., Lohnes, D., Decimo, D. et al. (1994) Function of the retinoic acid receptors (RARs) during development (II). Multiple abnormalities at various stages of organogenesis in RAR double mutants. Development 120, 2749-2771
160. LeCouter, J. E., Kablar, B., Hardy, W. R. et al. (1998) Strain-dependent myeloid hyperplasia, growth deficiency, and accelerated cell cycle in mice lacking the Rb-related p107 gene. Mol. Cell. Biol. 18, 7455-7465
161. Lickert, H., Takeuchi, J. K., Von Both, I. et al. (2004) Baf60c is essential for function of BAF chromatin remodelling complexes in heart development. Nature (London) 432, 107-112
162. Gottlieb, P. D., Pierce, S. A., Sims, R. J. et al. (2002) Bop encodes a muscle-restricted protein containing MYND and SET domains and is essential for cardiac differentiation and morphogenesis. Nat. Genet. 31, 25-32
163. Stennard, F. A., Costa, M. W., Lai, D. et al. (2005) Murine T-box transcription factor Tbx20 acts as a repressor during heart development, and is essential for adult heart integrity, function and adaptation. Development 132, 2451-2462
164. Singh, M. K., Christoffels, V. M., Dias, J. M. et al. (2005) Tbx20 is essential for cardiac chamber differentiation and repression of Tbx2. Development 132, 2697-2707
165. Chen, Z., Friedrich, G. A. and Soriano, P. (1994) Transcriptional enhancer factor 1 disruption by a retroviral gene trap leads to heart defects and embryonic lethality in mice. Genes Dev. 8, 2293-2301
166. Ito, M.; Okano, H. J., Darnell, R. B. and Roeder, R. G. (2002) The TRAP100 component of the TRAP/Mediator complex is essential in broad transcriptional events and development. EMBO J. 21, 3464-3475
167. Parekh, V., McEwen, A., Barbour, V. et al. (2004) Defective extraembryonic angiogenesis in mice lacking LBP-1a, a member of the grainyhead family of transcription factors. Mol. Cell. Biol. 24, 7113-7129
168. Ackerman, K. G., Herron, B. J., Vargas, S. O. et al. (2005) Fog2 is required for normal diaphragm and lung development in mice and humans. PLoS Genet. 1, 58-65
169. Varfolomeev, E. E., Schuchmann, M., Luria, V. et al. (1998) Targeted disruption of the mouse caspase 8 gene ablates cell death induction by the TNF receptors, Fas/Apo1, and DR3 and is lethal prenatally. Immunity 9, 267-276
170. Kozar, K., Ciemerych, M. A., Rebel, V. I. et al. (2004) Mouse development and cell proliferation in the absence of D-cyclins. Cell 118, 477-491
171. Yeh, W. C., Itie, A., Elia, A. J. et al. (2000) Requirement for Casper (c-FLIP) in regulation of death receptor-induced apoptosis and embryonic development. Immunity 12, 633-642
172. McPherson, J. P., Tamblyn, L., Elia, A. et al. (2004) Lats2/Kpm is required for embryonic development, proliferation control and genomic integrity. EMBO J. 23, 3677-3688
173. Kumar, A., Crawford, K., Close, L. et al. (1997) Rescue of cardiac α-actin-deficient mice by enteric smooth muscle gamma-actin. Proc. Natl. Acad. Sci. U.S.A. 94, 4406-4411
174. Honda, H., Oda, H., Nakamoto, T. et al. (1998) Cardiovascular anomaly, impaired actin bundling and resistance to Src-induced transformation in mice lacking p130Cas. Nat. Genet. 19, 361-365
175. Muller, A. J., Baker, J. E, DuHadaway, J. B. et al. (2003) Targeted disruption of the murine Bin1/Amphiphysin II gene does not disable endocytosis but results in embryonic cardiomyopathy with aberrant myofibril formation. Mol. Cell. Biol. 23, 4295-4306
176. Mesaeli, N., Nakamura, K., Zvaritch, E. et al. (1999) Calreticulin is essential for cardiac development. J. Cell Biol. 144, 857-868
177. Rauch, F., Prud'homme, J., Arabian, A., Dedhar, S. and St-Arnaud, R. (2000) Heart, brain, and body wall defects in mice lacking calreticulin. Exp. Cell Res. 256, 105-111
178. Bader, B. L., Rayburn, H., Crowley, D. and Hynes, R. O. (1998) Extensive vasculogenesis, angiogenesis, and organogenesis precede lethality in mice lacking all αv integrins. Cell 95, 507-519
179. -/- mice analysis. J. Cell Biol. 145, 825-836
180. Pall, G. S., Wallis, J., Axton, R. et al. (2004) A novel transmembrane MSP-containing protein that plays a role in right ventricle development. Genomics 84, 1051-1059
181. Boulter, C., Mulroy, S., Webb, S., Fleming, S., Brindle, K. and Sandford, R. (2001) Cardiovascular, skeletal, and renal defects in mice with a targeted disruption of the Pkd1 gene. Proc. Natl. Acad. Sci. U.S.A. 98, 12174-12179
182. Lu, W., Peissel, B., Babakhanlou, H. et al. (1997) Perinatal lethality with kidney and pancreas defects in mice with a targetted Pkd1 mutation. Nat. Genet. 17, 179-181
183. Grossmann, K. S., Grund, C., Huelsken, J. et al. (2004) Requirement of plakophilin 2 for heart morphogenesis and cardiac junction formation. J. Cell Biol. 167, 149-160
184. Kwee, E., Baldwin, H. S., Shen, H. M. et al. (1995) Defective development of the embryonic and extraembryonic circulatory systems in vascular cell adhesion molecule (VCAM-1) deficient mice. Development 121, 489-503
185. Pederson, B. A., Chen, H., Schroeder, J. M., Shou, W., DePaoli-Roach, A. A. and Roach, P. J. (2004) Abnormal cardiac development in the absence of heart glycogen. Mol. Cell. Biol. 24, 7179-7187
186. Carry, D. J., Ordway, G. A., Lorenz, J. N. et al. (1998) Mice without myoglobin. Nature (London) 395, 905-908
187. Meeson, A. P., Radford, N., Shelton, J. M. et al. (2001) Adaptive mechanisms that preserve cardiac function in mice without myoglobin. Circ. Res. 88, 713-720
188. Kwon, Y. T., Kashina, A. S., Davydov, I. V. et al. (2002) An essential role of N-terminal arginylation in cardiovascular development. Science 297, 96-99
189. Yu, Q., Shen, Y., Chatterjee, B. et al. (2004) ENU induced mutations causing congenital cardiovascular anomalies. Development 131, 6211-6223
190. Camenisch, T. D., Spicer, A. P., Brehm-Gibson, T. et al. (2000) Disruption of hyaluronan synthase-2 abrogates normal cardiac morphogenesis and hyaluronan-mediated transformation of epithelium to mesenchyme. J. Clin. Invest. 106, 349-360
191. King, T., Bland, Y., Webb, S., Barton, S. and Brown, N. A. (2002) Expression of Peg1 (Mest) in the developing mouse heart: involvement in trabeculation. Dev. Dyn. 225, 212-215
192. Dai, Y. S. and Markham, B. E. (2001) p300 Functions as a coactivator of transcription factor GATA-4. J. Biol. Chem. 276, 37178-37185
193. Dai, Y. S., Cserjesi, P., Markham, B. E. and Molkentin, J. D. (2002) The transcription factors GATA4 and dHAND physically interact to synergistically activate cardiac gene expression through a p300-dependent mechanism. J. Biol. Chem. 277, 24390-24398
194. Hirai, M., Ono, K., Morimoto, T. et al. (2004) FOG-2 competes with GATA-4 for transcriptional coactivator p300 and represses hypertrophic responses in cardiac myocytes. J. Biol. Chem. 279, 37640-37650
195. Poizat, C., Puri, P. L., Bai, Y. and Kedes, L. (2005) Phosphorylation-dependent degradation of p300 by doxorubicin-activated p38 mitogen-activated protein kinase in cardiac cells. Mol. Cell. Biol. 25, 2673-2687
196. Heidenreich, O., Neininger, A., Schratt, G. et al. (1999) MAPKAP kinase 2 phosphorylates serum response factor in vitro and in vivo. J. Biol. Chem. 274, 14434-14443