Hand factors as regulators of cardiac morphogenesis and implications for congenital heart defects

Birth Defects Research Part A - Clinical and Molecular Teratology

Volumn 91, Issue 6, 2011, Pages 485-494

  Vincentz, Joshua W ^a   Barnes, Ralston M ^a   Firulli, Anthony B ^a  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Basic helix loop helix; Cardiogenesis; Congenital heart defect; Dimerization; DNA binding; HAND1; HAND2; Heart development; Transcription

Indexed keywords

DNA; MESSENGER RNA; MICRORNA; THYMOSIN BETA4; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR HAND1; TRANSCRIPTION FACTOR HAND2; UNCLASSIFIED DRUG;

CELL DIFFERENTIATION; CELL MATURATION; CONGENITAL HEART DISEASE; DOWN REGULATION; EMBRYO DEATH; EMBRYO DEVELOPMENT; ENDOCARDIUM; EPICARDIUM; GAIN OF FUNCTION MUTATION; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; GENE TARGETING; HEART DEVELOPMENT; HUMAN; MUSCLE CELL; NEURAL CREST CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; ZEBRA FISH;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEART; HEART DEFECTS, CONGENITAL; HUMANS; MORPHOGENESIS; MYOCARDIUM;

ANIMALIA;

EID: 79958130975     PISSN: 15420752     EISSN: 15420760     Source Type: Journal    
DOI: 10.1002/bdra.20796     Document Type: Review

References (86)

1. Ambros V. 2004. The functions of animal microRNAs. Nature 431: 350-355.
2. Baek D, Villen J, Shin C, et al. 2008. The impact of microRNAs on protein output. Nature 455: 64-71.
3. Barbosa AC, Funato N, Chapman S, et al. 2007. Hand transcription factors cooperatively regulate development of the distal midline mesenchyme. Dev Biol 310: 154-168.
4. Barnes RM, Firulli AB. 2009. A twist of insight-the role of Twist-family bHLH factors in development. Int J Dev Biol 53: 909-924.
5. Barnes RM, Firulli BA, Conway SJ, et al. 2010. Analysis of the Hand1 cell lineage reveals novel contributions to cardiovascular, neural crest, extra-embryonic, and lateral mesoderm derivatives. Dev Dyn 239: 3086-3097.
6. Borochowitz Z, Shalev SA, Yehudai I, et al. 1997. Deletion (4)(q33 -> qter): a case report and review of the literature. J Child Neurol 12: 335-337.
7. Breckenridge RA, Zuberi Z, Gomes J, et al. 2009. Overexpression of the transcription factor Hand1 causes predisposition towards arrhythmia in mice. J Mol Cell Cardiol 47: 133-141.
8. Byatt SA, Baker E, Richards RI, et al. 1997. Unbalanced t(4;11)(q32;q23) in a 34-year-old man with manifestations of distal monosomy 11q and trisomy 4q syndromes. Am J Med Genet 70: 357-360.
9. Chin TK, Perloff JK, Williams RG, et al. 1990. Isolated noncompaction of left ventricular myocardium. A study of eight cases. Circulation 82: 507-513.
10. Conway SJ, Firulli B, Firulli AB, et al. 2010. A bHLH code for cardiac morphogenesis. Pediatr Cardiol 31: 318-324.
11. Cserjesi P, Brown D, Lyons GE, et al. 1995. Expression of the novel basic helix-loop-helix gene eHAND in neural crest derivatives and extraembryonic membranes during mouse development. Dev Biol 170: 664-678.
12. Dupont E, Matsushita T, Kaba RA, et al. 2001. Altered connexin expression in human congestive heart failure. J Mol Cell Cardiol 33: 359-371.
13. Firulli AB. 2003. A HANDful of questions: the molecular biology of the heart and neural crest derivatives (HAND)-subclass of basic helix-loop-helix transcription factors. Gene 312: 27-40.
14. Firulli AB, McFadden DG, Lin Q, et al. 1998. Heart and extra-embryonic mesodermal defects in mouse embryos lacking the bHLH transcription factor Hand1. Nat Genet 18: 266-270.
15. Firulli BA, Hadzic DB, McDaid JR, et al. 2000. The basic helix-loop-helix transcription factors dHAND and eHAND exhibit dimerization characteristics that suggest complex regulation of function. J Biol Chem 275: 33567-33573.
16. Firulli BA, Howard MJ, McDaid JR, et al. 2003. PKA, PKC, and the protein phosphatase 2A influence HAND factor function: a mechanism for tissue-specific transcriptional regulation Mol Cell 12: 1225-1237.
17. Firulli BA, Krawchuk D, Centonze VE, et al. 2005. Altered Twist1 and Hand2 dimerization is associated with Saethre-Chotzen syndrome and limb abnormalities. Nat Genet 37: 373-381.
18. Firulli BA, McConville DP, Byers JS, et al. 2010. Analysis of a Hand1 hypomorphic allele reveals a critical threshold for embryonic viability. Dev Dyn 239: 2748-2760.
19. Firulli BA, Redick BA, Conway SJ, et al. 2007. Mutations within helix I of Twist1 result in distinct limb defects and variation of DNA binding affinities. J Biol Chem 282: 27536-27546.
20. Garavito-Aguilar ZV, Riley HE, Yelon D, et al. 2010. Hand2 ensures an appropriate environment for cardiac fusion by limiting Fibronectin function. Development 137: 3215-3220.
21. Gutstein DE, Morley GE, Vaidya D, et al. 2001. Heterogeneous expression of Gap junction channels in the heart leads to conduction defects and ventricular dysfunction. Circulation 104: 1194-1199.
22. Hendershot TJ, Liu H, Sarkar AA, et al. 2007. Expression of Hand2 is sufficient for neurogenesis and cell type-specific gene expression in the enteric nervous system. Dev Dyn 236: 93-105.
23. Holler KL, Hendershot TJ, Troy SE, et al. 2010. Targeted deletion of Hand2 in cardiac neural crest-derived cells influences cardiac gene expression and outflow tract development. Dev Biol 341: 291-304.
24. Huang J, Bridges LC, White JM, et al. 2005. Selective modulation of integrin-mediated cell migration by distinct ADAM family members. Mol Biol Cell 16: 4982-4991.
25. Ichida F, Hamamichi Y, Miyawaki T, et al. 1999. Clinical features of isolated noncompaction of the ventricular myocardium: long-term clinical course, hemodynamic properties, and genetic background. J Am Coll Cardiol 34: 233-240.
26. Kenny D, Hares D, Uzun O, et al. 2007. Ventricular non-compaction in the setting of double-outlet right ventricle (tetralogy of Fallot type) with doubly committed subarterial ventricular septal defect. Heart 93: 647.
27. Kloosterman WP, Plasterk RH. 2006. The diverse functions of microRNAs in animal development and disease. Dev Cell 11: 441-450.
28. Kostin S, Dammer S, Hein S, et al. 2004. Connexin 43 expression and distribution in compensated and decompensated cardiac hypertrophy in patients with aortic stenosis. Cardiovasc Res 62: 426-436.
29. Lie-Venema H, van den Akker NM, Bax NA, et al. 2007. Origin, fate, and function of epicardium-derived cells (EPDCs) in normal and abnormal cardiac development. ScientificWorldJournal 7: 1777-1798.
30. Lim KC, Lakshmanan G, Crawford SE, et al. 2000. Gata3 loss leads to embryonic lethality due to noradrenaline deficiency of the sympathetic nervous system. Nat Genet 25: 209-212.
31. Litchenberg WH, Norman LW, Holwell AK, et al. 2000. The rate and anisotropy of impulse propagation in the postnatal terminal crest are correlated with remodeling of Cx43 gap junction pattern. Cardiovasc Res 45: 379-387.
32. Liu J, Stainier DYR. 2010. Tbx5 and Bmp signaling are essential for proepicardium specification in zebrafish. Circ Res 106: 1818-1828.
33. Liu N, Barbosa AC, Chapman SL, et al. 2009. DNA binding-dependent and -independent functions of the Hand2 transcription factor during mouse embryogenesis. Development 136: 933-942.
34. Lo PC, Zaffran S, Senatore S, et al. 2007. The Drosophila Hand gene is required for remodeling of the developing adult heart and midgut during metamorphosis. Dev Biol 311: 287-296.
35. Martindill DM, Risebro CA, Smart N, et al. 2007. Nucleolar release of Hand1 acts as a molecular switch to determine cell fate. Nat Cell Biol 9: 1131-1141.
36. Masuelli L, Bei R, Sacchetti P, et al. 2003. Beta-catenin accumulates in intercalated disks of hypertrophic cardiomyopathic hearts. Cardiovasc Res 60: 376-387.
37. Maves L, Tyler A, Moens CB, et al. 2009. Pbx acts with Hand2 in early myocardial differentiation. Dev Biol 333: 409-418.
38. McFadden DG, Barbosa AC, Richardson JA, et al. 2005. The Hand1 and Hand2 transcription factors regulate expansion of the embryonic cardiac ventricles in a gene dosage-dependent manner. Development 132(1): 189-201.
39. McFadden DG, Charite J, Richardson JA, et al. 2000. A GATA-dependent right ventricular enhancer controls dHAND transcription in the developing heart. Development 127: 5331-5341.
40. Mitchell ME, Sander TL, Klinkner DB, et al. 2007. The molecular basis of congenital heart disease. Semin Thorac Cardiovasc Surg 19: 228-237.
41. Morikawa Y, Cserjesi P. 2004. Extra-embryonic vasculature development is regulated by the transcription factor HAND1. Development 131: 2195-2204.
42. Morikawa Y, Cserjesi P. 2008. Cardiac neural crest expression of Hand2 regulates outflow and second heart field development. Circ Res 103: 1422-1429.
43. Morikawa Y, D'Autreaux F, Gershon MD, et al. 2007. Hand2 determines the noradrenergic phenotype in the mouse sympathetic nervous system. Dev Biol 307: 114-126.
44. Morrison-Graham K, Schatteman GC, Bork T, et al. 1992. A PDGF receptor mutation in the mouse (Patch) perturbs the development of a non-neuronal subset of neural crest-derived cells. Development 115: 133-142.
45. Obler D, Juraszek AL, Smoot LB, et al. 2008. Double outlet right ventricle: aetiologies and associations. J Med Genet 45: 481-497.
46. Orr-Urtreger A, Lonai P. 1992. Platelet-derived growth factor-A and its receptor are expressed in separate, but adjacent cell layers of the mouse embryo. Development 115: 1045-1058.
47. Pinco KA, Liu S, Yang JT, et al. 2001. alpha4 integrin is expressed in a subset of cranial neural crest cells and in epicardial progenitor cells during early mouse development. Mech Dev 100: 99-103.
48. Reamon-Buettner SM, Ciribilli Y, Inga A, Borlak J. 2008. A loss-of-function mutation in the binding domain of HAND1 predicts hypoplasia of the human hearts. Human Molecular Genetics 17: 1397-1405.
49. Riley P, Anson-Cartwright L, Cross JC, et al. 1998. The Hand1 bHLH transcription factor is essential for placentation and cardiac morphogenesis. Nat Genet 18: 271-275.
50. Risebro CA, Smart N, Dupays L, et al. 2006. Hand1 regulates cardiomyocyte proliferation versus differentiation in the developing heart. Development 133: 4595-4606.
51. Ritter O, Haase H, Schulte HD, et al. 1999. Remodeling of the hypertrophied human myocardium by cardiac bHLH transcription factors. J Cell Biochem 74: 551-561.
52. Rychlik JL, Gerbasi V, Lewis EJ, et al. 2003. The interaction between dHAND and Arix at the dopamine beta-hydroxylase promoter region is independent of direct dHAND binding to DNA. J Biol Chem 278: 49652-49660.
53. Schoenebeck JJ, Keegan BR, Yelon D, et al. 2007. Vessel and blood specification override cardiac potential in anterior mesoderm. Dev Cell 13: 254-267.
54. Scholl AM, Kirby ML. 2009. Signals controlling neural crest contributions to the heart. Wiley Interdiscip Rev Syst Biol Med 1: 220-227.
55. Selbach M, Schwanhausser B, Thierfelder N, et al. 2008. Widespread changes in protein synthesis induced by microRNAs. Nature 455: 58-63.
56. Sepp R, Severs NJ, Gourdie RG, et al. 1996. Altered patterns of cardiac intercellular junction distribution in hypertrophic cardiomyopathy. Heart 76: 412-417.
57. Shen L, Li XF, Shen AD, et al. 2010. Transcription factor HAND2 mutations in sporadic Chinese patients with congenital heart disease. Chin Med J (Engl) 123: 1623-1627.
58. Sheppard AM, Onken MD, Rosen GD, et al. 1994. Expanding roles for alpha 4 integrin and its ligands in development. Cell Adhes Commun 2: 27-43.
59. Shrivastava S, Srivastava D, Olson EN, et al. 2010. Thymosin beta4 and cardiac repair. Ann N Y Acad Sci 1194: 87-96.
60. Smart N, Dube KN, Riley PR, et al. 2010. Identification of Thymosin beta4 as an effector of Hand1-mediated vascular development. Nat Commun 1: 1-10.
61. Smart N, Hill AA, Cross JC, et al. 2002. A differential screen for putative targets of the bHLH transcription factor Hand1 in cardiac morphogenesis. Gene Expr Patterns 2: 61-67.
62. Snarr BS, Kern CB, Wessels A, et al. 2008. Origin and fate of cardiac mesenchyme. Dev Dyn 237: 2804-2819.
63. Srivastava D, Cserjesi P, Olson EN, et al. 1995. A subclass of bHLH proteins required for cardiac morphogenesis. Science 270: 1995-1999.
64. Srivastava D, Olson EN. 2000. A genetic blueprint for cardiac development. Nature 407: 221-226.
65. Srivastava D, Thomas T, Lin Q, et al. 1997. Regulation of cardiac mesodermal and neural crest development by the bHLH transcription factor, dHAND. Nat Genet 16: 154-160.
66. Stoller JZ, Epstein JA. 2005. Cardiac neural crest. Semin Cell Dev Biol 16: 704-715.
67. Talner CN. 1998. Report of the New England Regional Infant Cardiac Program, by Donald C. Fyler, MD, Pediatrics, 1980;65(suppl):375-461. Pediatrics 102(1 Pt 2): 258-259.
68. Thattaliyath BD, Firulli BA, Firulli AB, et al. 2002. The basic-helix-loop-helix transcription factor HAND2 directly regulates transcription of the atrial naturetic peptide gene. J Mol Cell Cardiol 34: 1335-1344.
69. Thomas T, Kurihara H, Yamagishi H, et al. 1998. A signaling cascade involving endothelin-1, dHAND and msx1 regulates development of neural-crest-derived branchial arch mesenchyme. Development 125: 3005-3014.
70. Togi K, Kawamoto T, Yamauchi R, et al. 2004. Role of Hand1/eHAND in the dorso-ventral patterning and interventricular septum formation in the embryonic heart. Mol Cell Biol 24: 4627-4635.
71. Trinh LA, Stainier DY. 2004. Fibronectin regulates epithelial organization during myocardial migration in zebrafish. Dev Cell 6: 371-382.
72. Trinh LA, Yelon D, Stainier DY, et al. 2005. Hand2 regulates epithelial formation during myocardial diferentiation. Curr Biol 15: 441-446.
73. Vincentz JW, Barnes RM, Rodgers R, et al. 2008. An absence of Twist1 results in aberrant cardiac neural crest morphogenesis. Dev Biol 320: 131-139.
74. Waldo K, Miyagawa-Tomita S, Kumiski D, et al. 1998. Cardiac neural crest cells provide new insight into septation of the cardiac outflow tract: aortic sac to ventricular septal closure. Dev Biol 196: 129-144.
75. Weiford BC, Subbarao VD, Mulhern KM, et al. 2004. Noncompaction of the ventricular myocardium. Circulation 109: 2965-2971.
76. Wills AA, Holdway JE, Major RJ, et al. 2008. Regulated addition of new myocardial and epicardial cells fosters homeostatic cardiac growth and maintenance in adult zebrafish. Development 135: 183-192.
77. Xu H, Firulli AB, Zhang X, et al. 2003. HAND2 synergistically enhances transcription of dopamine-beta-hydroxylase in the presence of Phox2a. Dev Biol 262: 183-193.
78. Yamada KM. 2000. Fibronectin peptides in cell migration and wound repair. J Clin Invest 105: 1507-1509.
79. Yamagishi H, Garg V, Matsuoka R, et al. 1999. A molecular pathway revealing a genetic basis for human cardiac and craniofacial defects. Science 283: 1158-1161.
80. Yamagishi H, Olson EN, Srivastava D, et al. 2000. The basic helix-loop-helix transcription factor, dHAND, is required for vascular development. J Clin Invest 105: 261-270.
81. Yelon D, Ticho B, Halpern ME, et al. 2000. The bHLH transcription factor hand2 plays parallel roles in zebrafish heart and pectoral fin development. Development 127: 2573-2582.
82. Yeo GH, Cheah FS, Winkler C, et al. 2009. Phylogenetic and evolutionary relationships and developmental expression patterns of the zebrafish twist gene family. Dev Genes Evol 219: 289-300.
83. Young BA, Taooka Y, Liu S, et al. 2001. The cytoplasmic domain of the integrin alpha9 subunit requires the adaptor protein paxillin to inhibit cell spreading but promotes cell migration in a paxillin-independent manner. Mol Biol Cell 12: 3214-3225.
84. Zhao Y, Ransom JF, Li A, et al. 2007. Dysregulation of cardiogenesis, cardiac conduction, and cell cycle in mice lacking miRNA-1-2. Cell 129: 303-317.
85. Zhao Y, Samal E, Srivastava D, et al. 2005. Serum response factor regulates a muscle-specific microRNA that targets Hand2 during cardiogenesis. Nature 436: 214-220.
86. Zhao Y, Srivastava D. 2007. A developmental view of microRNA function. Trends Biochem Sci 32: 189-197.