Molecular mechanism of ventricular trabeculation/compaction and the pathogenesis of the left ventricular noncompaction cardiomyopathy (LVNC)

American Journal of Medical Genetics, Part C: Seminars in Medical Genetics

Volumn 163, Issue 3, 2013, Pages 144-156

  Zhang, Wenjun ^a   Chen, Hanying ^a   Qu, Xiuxia ^a   Chang, Ching Pin ^a,b,c   Shou, Weinian ^a  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA ACTIN; ANGIOPOIETIN; ATRIAL NATRIURETIC FACTOR; BETA GALACTOSIDASE; BONE MORPHOGENETIC PROTEIN; EPHRIN B2; FIBROBLAST GROWTH FACTOR 16; FIBROBLAST GROWTH FACTOR RECEPTOR 1; FIBROBLAST GROWTH FACTOR RECEPTOR 2; LAMIN A; LAMIN C; MYOSIN HEAVY CHAIN BETA; NEU DIFFERENTIATION FACTOR; PLATELET DERIVED GROWTH FACTOR A; TRANSFORMING GROWTH FACTOR BETA; TROPONIN T; VASCULAR CELL ADHESION MOLECULE 1; VASCULOTROPIN; FK 506 BINDING PROTEIN;

ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CHROMATIN; ENDOCARDIUM; ENDODERM; EXTRACELLULAR MATRIX; GENE EXPRESSION; GENE MUTATION; GENETIC HETEROGENEITY; GENETIC VARIABILITY; HEART DEVELOPMENT; HEART MUSCLE; HEART VENTRICLE WALL; INTRACELLULAR SIGNALING; MESODERM; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; TRANSCRIPTION INITIATION; VENTRICULAR NONCOMPACTION; WNT SIGNALING PATHWAY; ANIMAL; DISEASE MODEL; GENETIC PREDISPOSITION; GENETICS; HEART VENTRICLE; HUMAN; METABOLISM; MOUSE; MUTATION; PATHOPHYSIOLOGY; TRANSGENIC MOUSE;

ANIMALS; DISEASE MODELS, ANIMAL; GENETIC PREDISPOSITION TO DISEASE; HEART VENTRICLES; HUMANS; ISOLATED NONCOMPACTION OF THE VENTRICULAR MYOCARDIUM; MICE; MICE, TRANSGENIC; MUTATION; TACROLIMUS BINDING PROTEIN 1A;

EID: 84880699781     PISSN: 15524868     EISSN: 15524876     Source Type: Journal    
DOI: 10.1002/ajmg.c.31369     Document Type: Article

References (104)

1. Anderson RH, Ho SY, Sanchez-Quintana D, Redmann K, Lunkenheimer PP. 2006. Heuristic problems in defining the three-dimensional arrangement of the ventricular myocytes. Anat Rec A Discov Mol Cell Evol Biol 288:579-586.
2. Anderson RH, Sanchez-Quintana D, Redmann K, Lunkenheimer PP. 2007. How are the myocytes aggregated so as to make up the ventricular mass? Semin Thorac Cardiovasc Surg Pediatr Card Surg Annu 10:76-86.
3. Anderson RH, Sanchez-Quintana D, Niederer P, Lunkenheimer PP. 2008. Structural-functional correlates of the 3-dimensional arrangement of the myocytes making up the ventricular walls. J Thorac Cardiovasc Surg 136:10-18.
4. Aras D, Tufekcioglu O, Ergun K, Ozeke O, Yildiz A, Topaloglu S, Deveci B, Sahin O, Kisacik HL, Korkmaz S. 2006. Clinical features of isolated ventricular noncompaction in adults long-term clinical course, echocardiographic properties, and predictors of left ventricular failure. J Card Fail 12:726-733.
5. Bao B, Zhang L, Hu H, Yin S, Liang Z. 2012. Deletion of a single-copy DAAM1 gene in congenital heart defect: A case report. BMC Med Genet 13:63.
6. Bartman T, Hove J. 2005. Mechanics and function in heart morphogenesis. Dev Dyn 233:373-381.
7. Besson A, Dowdy SF, Roberts JM. 2008. CDK inhibitors: Cell cycle regulators and beyond. Dev Cell 14:159-169.
8. Bierer BE, Mattila PS, Standaert RF, Herzenberg LA, Burakoff SJ, Crabtree G, Schreiber SL. 1990. Two distinct signal transmission pathways in T lymphocytes are inhibited by complexes formed between an immunophilin and either FK506 or rapamycin. Proc Natl Acad Sci USA 87:9231-9235.
9. Brutsaert DL, Andries LJ. 1992. The endocardial endothelium. Am J Physiol 263:H985-H1002.
10. Camenisch TD, Spicer AP, Brehm-Gibson T, Biesterfeldt J, Augustine ML, Calabro A Jr, 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.
11. Cameron AM, Steiner JP, Roskams AJ, Ali SM, Ronnett GV, Snyder SH. 1995a. Calcineurin associated with the inositol 1, 4, 5-trisphosphate receptor-FKBP12 complex modulates Ca2+ flux. Cell 83:463-472.
12. Cameron AM, Steiner JP, Sabatini DM, Kaplin AI, Walensky LD, Snyder SH. 1995b. Immunophilin FK506 binding protein associated with inositol 1, 4, 5-trisphosphate receptor modulates calcium flux. Proc Natl Acad Sci USA 92:1784-1788.
13. Cameron AM, Nucifora FC Jr, Fung ET, Livingston DJ, Aldape RA, Ross CA, Snyder SH. 1997. FKBP12 binds the inositol 1, 4, 5-trisphosphate receptor at leucine-proline (1400-1401) and anchors calcineurin to this FK506-like domain. J Biol Chem 272:27582-27588.
14. Chang B, Gorbea C, Lezin G, Li L, Shan L, Sakai N, Kogaki S, Otomo T, Okinaga T, Hamaoka A, Yu X, Hata Y, Nishida N, Yost HJ, Bowles NE, Brunelli L, Ichida F. 2013. 14-3-3epsilon Gene variants in a Japanese patient with left ventricular noncompaction and hypoplasia of the corpus callosum. Gene 515:173-180.
15. Chen H, Shi S, Acosta L, Li W, Lu J, Bao S, Chen Z, Yang Z, Schneider MD, Chien KR, Conway SJ, Yoder MC, Haneline LS, Franco D, Shou W. 2004. BMP10 is essential for maintaining cardiac growth during murine cardiogenesis. Development 131:2219-2231.
16. Chen H, Zhang W, Li D, Cordes TM, Mark Payne R, Shou W. 2009. Analysis of ventricular hypertrabeculation and noncompaction using genetically engineered mouse models. Pediatr Cardiol 30:626-634.
17. Chen H, Zhang W, Sun X, Yoshimoto M, Chen Z, Zhu W, Liu J, Shen Y, Yong W, Li D, Zhang J, Lin Y, Li B, Vandusen NJ, Snider P, Schwartz RJ, Conway SJ, Field LJ, Yoder MC, Firulli AB, Carlesso N, Towbin JA, Shou W. 2013. Fkbp1a controls ventricular myocardium trabeculation and compaction by regulating endocardial Notch1 activity. Development 140:1946-1957.
18. Christoffels VM, Keijser AG, Houweling AC, Clout DE, Moorman AF. 2000. Patterning the embryonic heart: Identification of five mouse Iroquois homeobox genes in the developing heart. Dev Biol 224:263-274.
19. Daubeney PE, Nugent AW, Chondros P, Carlin JB, Colan SD, Cheung M, Davis AM, Chow CW, Weintraub RG. 2006. Clinical features and outcomes of childhood dilated cardiomyopathy: Results from a national population-based study. Circulation 114:2671-2678.
20. Del Monte G, Grego-Bessa J, Gonzalez-Rajal A, Bolos V, De La Pompa JL. 2007. Monitoring Notch1 activity in development: Evidence for a feedback regulatory loop. Dev Dyn 236:2594-2614.
21. Dorri F, Niederer PF, Redmann K, Lunkenheimer PP, Cryer CW, Anderson RH. 2007. An analysis of the spatial arrangement of the myocardial aggregates making up the wall of the left ventricle. Eur J Cardiothorac Surg 31:430-437.
22. Dunaief JL, Strober BE, Guha S, Khavari PA, Alin K, Luban J, Begemann M, Crabtree GR, Goff SP. 1994. The retinoblastoma protein and BRG1 form a complex and cooperate to induce cell cycle arrest. Cell 79:119-130.
23. Ferrara N, Carver-Moore K, Chen H, Dowd M, Lu L, O'Shea KS, Powell-Braxton L, Hillan KJ, Moore MW. 1996. Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 380:439-442.
24. Freedom RM, Yoo SJ, Perrin D, Taylor G, Petersen S, Anderson RH. 2005. The morphological spectrum of ventricular noncompaction. Cardiol Young 15:345-364.
25. Gassmann M, Casagranda F, Orioli D, Simon H, Lai C, Klein R, Lemke G. 1995. Aberrant neural and cardiac development in mice lacking the ErbB4 neuregulin receptor. Nature 378:390-394.
26. Gourdie RG, Kubalak S, Mikawa T. 1999. Conducting the embryonic heart: Orchestrating development of specialized cardiac tissues. Trends Cardiovasc Med 9:18-26.
27. Grant RT. 1926. An unusual anomaly of the coronary vessels in the malformed heart of a child. Heart 13:273-283.
28. Grego-Bessa J, Luna-Zurita L, del Monte G, Bolos V, Melgar P, Arandilla A, Garratt AN, Zang H, Mukouyama YS, Chen H, Shou W, Ballestar E, Esteller M, Rojas A, Perez-Pomares JM, de la Pompa JL. 2007. Notch signaling is essential for ventricular chamber development. Dev Cell 12:415-429.
29. Henderson DJ, Chaudhry B. 2011. Getting to the heart of planar cell polarity signaling. Birth Defects Res A Clin Mol Teratol 91:460-467.
30. Hirschy A, Schatzmann F, Ehler E, Perriard JC. 2006. Establishment of cardiac cytoarchitecture in the developing mouse heart. Dev Biol 289:430-441.
31. Hoedemaekers YM, Caliskan K, Michels M, Frohn-Mulder I, van der Smagt JJ, Phefferkorn JE, Wessels MW, ten Cate FJ, Sijbrands EJ, Dooijes D, Majoor-Krakauer DF. 2010. The importance of genetic counseling, DNA diagnostics, and cardiologic family screening in left ventricular noncompaction cardiomyopathy. Circ Cardiovasc Genet 3:232-239.
32. Icardo JM. 1988. Heart anatomy and developmental biology. Experientia 44:910-919.
33. Icardo JM, Fernandez-Teran A. 1987. Morphologic study of ventricular trabeculation in the embryonic chick heart. Acta Anat (Basel) 130:264-274.
34. Jayaraman T, Brillantes AM, Timerman AP, Fleischer S, Erdjument-Bromage H, Tempst P, Marks AR. 1992. FK506 binding protein associated with the calcium release channel (ryanodine receptor). J Biol Chem 267:9474-9477.
35. Jenni R, Oechslin E, Schneider J, Attenhofer Jost C, Kaufmann PA. 2001. Echocardiographic and pathoanatomical characteristics of isolated left ventricular non-compaction: A step towards classification as a distinct cardiomyopathy. Heart 86:666-671.
36. Kaneda T, Naruse C, Kawashima A, Fujino N, Oshima T, Namura M, Nunoda S, Mori S, Konno T, Ino H, Yamagishi M, Asano M. 2008. A novel beta-myosin heavy chain gene mutation, p.Met531Arg, identified in isolated left ventricular non-compaction in humans, results in left ventricular hypertrophy that progresses to dilation in a mouse model. Clin Sci (Lond) 114:431-440.
37. Kang JO, Sucov HM. 2005. Convergent proliferative response and divergent morphogenic pathways induced by epicardial and endocardial signaling in fetal heart development. Mech Dev 122:57-65.
38. Klaassen S, Probst S, Oechslin E, Gerull B, Krings G, Schuler P, Greutmann M, Hurlimann D, Yegitbasi M, Pons L, Gramlich M, Drenckhahn JD, Heuser A, Berger F, Jenni R, Thierfelder L. 2008. Mutations in sarcomere protein genes in left ventricular noncompaction. Circulation 117:2893-2901.
39. Kochilas LK, Li J, Jin F, Buck CA, Epstein JA. 1999. p57Kip2 expression is enhanced during mid-cardiac murine development and is restricted to trabecular myocardium. Pediatr Res 45:635-642.
40. Komiyama M, Ito K, Shimada Y. 1987. Origin and development of the epicardium in the mouse embryo. Anat Embryol (Berl) 176:183-189.
41. Kosaka Y, Cieslik KA, Li L, Lezin G, Maguire CT, Saijoh Y, Toyo-Oka K, Gambello MJ, Vatta M, Wynshaw-Boris A, Baldini A, Yost HJ, Brunelli L. 2012. 14-3-3epsilon plays a role in cardiac ventricular compaction by regulating the cardiomyocyte cell cycle. Mol Cell Biol 32:5089-5102.
42. Kramer R, Bucay N, Kane DJ, Martin LE, Tarpley JE, Theill LE. 1996. Neuregulins with an Ig-like domain are essential for mouse myocardial and neuronal development. Proc Natl Acad Sci USA 93:4833-4838.
43. Kwee L, Baldwin HS, Shen HM, Stewart CL, Buck C, Buck CA, Labow MA. 1995. Defective development of the embryonic and extraembryonic circulatory systems in vascular cell adhesion molecule (VCAM-1) deficient mice. Development 121:489-503.
44. Lai D, Liu X, Forrai A, Wolstein O, Michalicek J, Ahmed I, Garratt AN, Birchmeier C, Zhou M, Hartley L, Robb L, Feneley MP, Fatkin D, Harvey RP. 2010. Neuregulin 1 sustains the gene regulatory network in both trabecular and nontrabecular myocardium. Circ Res 107:715-727.
45. Lavine KJ, Yu K, White AC, Zhang X, Smith C, Partanen J, Ornitz DM. 2005. Endocardial and epicardial derived FGF signals regulate myocardial proliferation and differentiation in vivo. Dev Cell 8:85-95.
46. Lee KF, Simon H, Chen H, Bates B, Hung MC, Hauser C. 1995. Requirement for neuregulin receptor erbB2 in neural and cardiac development. Nature 378:394-398.
47. Lee Y, Song AJ, Baker R, Micales B, Conway SJ, Lyons GE. 2000. Jumonji, a nuclear protein that is necessary for normal heart development. Circ Res 86:932-938.
48. Li D, Hallett MA, Zhu W, Rubart M, Liu Y, Yang Z, Chen H, Haneline LS, Chan RJ, Schwartz RJ, Field LJ, Atkinson SJ, Shou W. 2011. Dishevelled-associated activator of morphogenesis 1 (Daam1) is required for heart morphogenesis. Development 138:303-315.
49. Lickert H, Takeuchi JK, Von Both I, Walls JR, McAuliffe F, Adamson SL, Henkelman RM, Wrana JL, Rossant J, Bruneau BG. 2004. Baf60c is essential for function of BAF chromatin remodelling complexes in heart development. Nature 432:107-112.
50. Liu J, Bressan M, Hassel D, Huisken J, Staudt D, Kikuchi K, Poss KD, Mikawa T, Stainier DY. 2010. A dual role for ErbB2 signaling in cardiac trabeculation. Development 137:3867-3875.
51. Lu SY, Sheikh F, Sheppard PC, Fresnoza A, Duckworth ML, Detillieux KA, Cattini PA. 2008. FGF-16 is required for embryonic heart development. Biochem Biophys Res Commun 373:270-274.
52. Luedde M, Ehlermann P, Weichenhan D, Will R, Zeller R, Rupp S, Muller A, Steen H, Ivandic BT, Ulmer HE, Kern M, Katus HA, Frey N. 2010. Severe familial left ventricular non-compaction cardiomyopathy due to a novel troponin T (TNNT2) mutation. Cardiovasc Res 86:452-460.
53. Lunkenheimer PP, Redmann K, Kling N, Jiang X, Rothaus K, Cryer CW, Wubbeling F, Niederer P, Heitz PU, Ho SY, Anderson RH. 2006a. Three-dimensional architecture of the left ventricular myocardium. Anat Rec A Discov Mol Cell Evol Biol 288:565-578.
54. Lunkenheimer PP, Redmann K, Westermann P, Rothaus K, Cryer CW, Niederer P, Anderson RH. 2006b. The myocardium and its fibrous matrix working in concert as a spatially netted mesh: A critical review of the purported tertiary structure of the ventricular mass. Eur J Cardiothorac Surg 29:S41-S49.
55. Luxan G, Casanova JC, Martinez-Poveda B, Prados B, D'Amato G, MacGrogan D, Gonzalez-Rajal A, Dobarro D, Torroja C, Martinez F, Izquierdo-Garcia JL, Fernandez-Friera L, Sabater-Molina M, Kong YY, Pizarro G, Ibanez B, Medrano C, Garcia-Pavia P, Gimeno JR, Monserrat L, Jimenez-Borreguero LJ, de la Pompa JL. 2013. Mutations in the NOTCH pathway regulator MIB1 cause left ventricular noncompaction cardiomyopathy. Nat Med 19:193-201.
56. Manner J. 1993. Experimental study on the formation of the epicardium in chick embryos. Anat Embryol (Berl) 187:281-289.
57. Meilhac SM, Kelly RG, Rocancourt D, Eloy-Trinquet S, Nicolas JF, Buckingham ME. 2003. A retrospective clonal analysis of the myocardium reveals two phases of clonal growth in the developing mouse heart. Development 130:3877-3889.
58. Mikawa T, Borisov A, Brown AM, Fischman DA. 1992a. Clonal analysis of cardiac morphogenesis in the chicken embryo using a replication-defective retrovirus: I. Formation of the ventricular myocardium. Dev Dyn 193:11-23.
59. Mikawa T, Cohen-Gould L, Fischman DA. 1992b. Clonal analysis of cardiac morphogenesis in the chicken embryo using a replication-defective retrovirus. III: Polyclonal origin of adjacent ventricular myocytes. Dev Dyn 195:133-141.
60. Mjaatvedt CH, Yamamura H, Capehart AA, Turner D, Markwald RR. 1998. The Cspg2 gene, disrupted in the hdf mutant, is required for right cardiac chamber and endocardial cushion formation. Dev Biol 202:56-66.
61. Moorman AF, Christoffels VM, Anderson RH, van den Hoff MJ. 2007. The heart-forming fields: One or multiple? Philosophical Trans R Soc Lond Ser B Biol Sci 362:1257-1265.
62. Murdoch JN, Henderson DJ, Doudney K, Gaston-Massuet C, Phillips HM, Paternotte C, Arkell R, Stanier P, Copp AJ. 2003. Disruption of scribble (Scrb1) causes severe neural tube defects in the circletail mouse. Hum Mol Genet 12:87-98.
63. Mysliwiec MR, Bresnick EH, Lee Y. 2011. Endothelial Jarid2/Jumonji is required for normal cardiac development and proper Notch1 expression. J Biol Chem 286:17193-17204.
64. Mysliwiec MR, Carlson CD, Tietjen J, Hung H, Ansari AZ, Lee Y. 2012. Jarid2 (Jumonji, AT rich interactive domain 2) regulates NOTCH1 expression via histone modification in the developing heart. J Biol Chem 287:1235-1241.
65. Nakamura T, Colbert M, Krenz M, Molkentin JD, Hahn HS, Dorn GW II, Robbins J. 2007. Mediating ERK 1/2 signaling rescues congenital heart defects in a mouse model of Noonan syndrome. J Clin Invest 117:2123-2132.
66. Nugent AW, Daubeney PE, Chondros P, Carlin JB, Cheung M, Wilkinson LC, Davis AM, Kahler SG, Chow CW, Wilkinson JL, Weintraub RG. 2003. The epidemiology of childhood cardiomyopathy in Australia. N Engl J Med 348:1639-1646.
67. Nugent AW, Daubeney PE, Chondros P, Carlin JB, Colan SD, Cheung M, Davis AM, Chow CW, Weintraub RG. 2005. Clinical features and outcomes of childhood hypertrophic cardiomyopathy: Results from a national population-based study. Circulation 112:1332-1338.
68. Oechslin E, Jenni R. 2011. Left ventricular non-compaction revisited: A distinct phenotype with genetic heterogeneity? Eur Heart J 32:1446-1456.
69. Pashmforoush M, Lu JT, Chen H, Amand TS, Kondo R, Pradervand S, Evans SM, Clark B, Feramisco JR, Giles W, Ho SY, Benson DW, Silberbach M, Shou W, Chien KR. 2004. Nkx 2-5 pathways and congenital heart disease; loss of ventricular myocyte lineage specification leads to progressive cardiomyopathy and complete heart block. Cell 117:373-386.
70. Pasumarthi KB, Field LJ. 2002. Cardiomyocyte cell cycle regulation. Circ Res 90:1044-1054.
71. Phillips HM, Murdoch JN, Chaudhry B, Copp AJ, Henderson DJ. 2005. Vangl2 acts via RhoA signaling to regulate polarized cell movements during development of the proximal outflow tract. Circ Res 96:292-299.
72. Phillips HM, Rhee HJ, Murdoch JN, Hildreth V, Peat JD, Anderson RH, Copp AJ, Chaudhry B, Henderson DJ. 2007. Disruption of planar cell polarity signaling results in congenital heart defects and cardiomyopathy attributable to early cardiomyocyte disorganization. Circ Res 101:137-145.
73. Phillips HM, Hildreth V, Peat JD, Murdoch JN, Kobayashi K, Chaudhry B, Henderson DJ. 2008. Non-cell-autonomous roles for the planar cell polarity gene Vangl2 in development of the coronary circulation. Circ Res 102:615-623.
74. Phoon CK, Acehan D, Schlame M, Stokes DL, Edelman-Novemsky I, Yu D, Xu Y, Viswanathan N, Ren M. 2012. Tafazzin knockdown in mice leads to a developmental cardiomyopathy with early diastolic dysfunction preceding myocardial noncompaction. J Am Heart Assoc 1:jah3-e0004555 doi: 10.1161/JAHA.111.000455
75. Probst S, Oechslin E, Schuler P, Greutmann M, Boye P, Knirsch W, Berger F, Thierfelder L, Jenni R, Klaassen S. 2011. Sarcomere gene mutations in isolated left ventricular noncompaction cardiomyopathy do not predict clinical phenotype. Circ Cardiovasc Genet 4:367-374.
76. Risebro CA, Riley PR. 2006. Formation of the ventricles. Sci World J 6:1862-1880.
77. Ritter M, Oechslin E, Sutsch G, Attenhofer C, Schneider J, Jenni R. 1997. Isolated noncompaction of the myocardium in adults. Mayo Clin Proc 72:26-31.
78. Rumyantsev PP, Krylova MI. 1990. Ultrastructure of myofibers and cells synthesizing DNA in the developing and regenerating lymph-heart muscles. Int Rev Cytol 120:1-52.
79. Sandhu R, Finkelhor RS, Gunawardena DR, Bahler RC. 2008. Prevalence and characteristics of left ventricular noncompaction in a community hospital cohort of patients with systolic dysfunction. Echocardiography 25:8-12.
80. Sato TN, Tozawa Y, Deutsch U, Wolburg-Buchholz K, Fujiwara Y, Gendron-Maguire M, Gridley T, Wolburg H, Risau W, Qin Y. 1995. Distinct roles of the receptor tyrosine kinases Tie-1 and Tie-2 in blood vessel formation. Nature 376:70-74.
81. Schlame M, Towbin JA, Heerdt PM, Jehle R, DiMauro S, Blanck TJ. 2002. Deficiency of tetralinoleoyl-cardiolipin in Barth syndrome. Ann Neurol 51:634-637.
82. Schmid P, Lunkenheimer PP, Redmann K, Rothaus K, Jiang X, Cryer CW, Jaermann T, Niederer P, Boesiger P, Anderson RH. 2007. Statistical analysis of the angle of intrusion of porcine ventricular myocytes from epicardium to endocardium using diffusion tensor magnetic resonance imaging. Anat Rec (Hoboken) 290:1413-1423.
83. Schreiber SL, Crabtree GR. 1995. Immunophilins, ligands, and the control of signal transduction. Harvey Lect 91:99-114.
84. Sedmera D, Pexieder T, Vuillemin M, Thompson RP, Anderson RH. 2000. Developmental patterning of the myocardium. Anatom Rec 258:319-337.
85. Shou W, Aghdasi B, Armstrong DL, Guo Q, Bao S, Charng MJ, Mathews LM, Schneider MD, Hamilton SL, Matzuk MM. 1998. Cardiac defects and altered ryanodine receptor function in mice lacking FKBP12. Nature 391:489-492.
86. Simons M, Mlodzik M. 2008. Planar cell polarity signaling: From fly development to human disease. Annu Rev Genet 42:517-540.
87. Sinha T, Wang B, Evans S, Wynshaw-Boris A, Wang J. 2012. Disheveled mediated planar cell polarity signaling is required in the second heart field lineage for outflow tract morphogenesis. Dev Biol 370:135-144.
88. Stankunas K, Hang CT, Tsun ZY, Chen H, Lee NV, Wu JI, Shang C, Bayle JH, Shou W, Iruela-Arispe ML, Chang CP. 2008. Endocardial Brg1 represses ADAMTS1 to maintain the microenvironment for myocardial morphogenesis. Dev Cell 14:298-311.
89. Sucov HM, Gu Y, Thomas S, Li P, Pashmforoush M. 2009. Epicardial control of myocardial proliferation and morphogenesis. Pediatr Cardiol 30:617-625.
90. Suri C, Jones PF, Patan S, Bartunkova S, Maisonpierre PC, Davis S, Sato TN, Yancopoulos GD. 1996. Requisite role of angiopoietin-1, a ligand for the TIE2 receptor, during embryonic angiogenesis. Cell 87:1171-1180.
91. Taber LA. 1998. Mechanical aspects of cardiac development. Prog Biophys Mol Biol 69:237-255.
92. Terry RW, Kwee L, Baldwin HS, Labow MA. 1997. Cre-mediated generation of a VCAM-1 null allele in transgenic mice. Transgenic Res 6:349-356.
93. Torrent-Guasp F, Kocica MJ, Corno AF, Komeda M, Carreras-Costa F, Flotats A, Cosin-Aguillar J, Wen H. 2005. Towards new understanding of the heart structure and function. Eur J Cardiothorac Surg 27:191-201.
94. Towbin JA. 2010. Left ventricular noncompaction: A new form of heart failure. Heart Fail Clin 6:453-469; viii.
95. Viragh S, Challice CE. 1981. The origin of the epicardium and the embryonic myocardial circulation in the mouse. Anat Rec 201:157-168.
96. Wang Y, Nathans J. 2007. Tissue/planar cell polarity in vertebrates: New insights and new questions. Development 134:647-658.
97. Wang T, Li BY, Danielson PD, Shah PC, Rockwell S, Lechleider RJ, Martin J, Manganaro T, Donahoe PK. 1996. The immunophilin FKBP12 functions as a common inhibitor of the TGF beta family type I receptors. Cell 86:435-444.
98. Watanabe Y, Kokubo H, Miyagawa-Tomita S, Endo M, Igarashi K, Aisaki K, Kanno J, Saga Y. 2006. Activation of Notch1 signaling in cardiogenic mesoderm induces abnormal heart morphogenesis in mouse. Development 133:1625-1634.
99. Xing Y, Ichida F, Matsuoka T, Isobe T, Ikemoto Y, Higaki T, Tsuji T, Haneda N, Kuwabara A, Chen R, Futatani T, Tsubata S, Watanabe S, Watanabe K, Hirono K, Uese K, Miyawaki T, Bowles KR, Bowles NE, Towbin JA. 2006. Genetic analysis in patients with left ventricular noncompaction and evidence for genetic heterogeneity. Mol Genet Metab 88:71-77.
100. Xu Y, Condell M, Plesken H, Edelman-Novemsky I, Ma J, Ren M, Schlame M. 2006a. A Drosophila model of Barth syndrome. Proc Natl Acad Sci USA 103:11584-11588.
101. Xu Y, Malhotra A, Ren M, Schlame M. 2006b. The enzymatic function of tafazzin. J Biol Chem 281:39217-39224.
102. Yamamura H, Zhang M, Markwald RR, Mjaatvedt CH. 1997. A heart segmental defect in the anterior-posterior axis of a transgenic mutant mouse. Dev Biol 186:58-72.
103. Yang J, Bucker S, Jungblut B, Bottger T, Cinnamon Y, Tchorz J, Muller M, Bettler B, Harvey R, Sun QY, Schneider A, Braun T. 2012. Inhibition of Notch2 by Numb/Numblike controls myocardial compaction in the heart. Cardiovasc Res 96:276-285.
104. Zhang W, Chen H, Wang Y, Yong W, Zhu W, Liu Y, Wagner GR, Payne RM, Field LJ, Xin H, Cai CL, Shou W. 2011. Tbx20 a downstream mediator for bone morphogenetic protein 10 in regulating cardiac ventricular wall development and function. J Biol Chem 286:36820-36829.