Tbx5 is required for avian and mammalian epicardial formation and coronary vasculogenesis

Circulation Research

Volumn 115, Issue 10, 2014, Pages 834-844

  Diman, Nata Y S G ^a   Brooks, Gabriel ^a   Kruithof, Boudewijn P T ^a   Elemento, Olivier ^b   Seidman, J G ^c   Seidman, Christine E ^c   Basson, Craig T ^a,e   Hatcher, Cathy J ^a,d  

^a Greenberg Division of Cardiology   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d PHILADELPHIA COLLEGE OF OSTEOPATHIC MEDICINE   (United States)

^e NOVARTIS INSTITUTES FOR BIOMEDICAL RESEARCH   (United States)

Author keywords

Cell adhesion; Cell migration; Coronary vessels; Epicardium; Myocardium; Tbx5; Transcription factors

Indexed keywords

CD31 ANTIGEN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; TRANSCRIPTION FACTOR TBX5; T BOX TRANSCRIPTION FACTOR; T-BOX TRANSCRIPTION FACTOR 5;

ANGIOGENESIS; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; BIRD; CELL ADHESION; CELL DENSITY; CELL FUNCTION; CELL MIGRATION; CELL POLARITY; CELL PROLIFERATION; CONTROLLED STUDY; CORONARY BLOOD VESSEL; EMBRYO; ENDOTHELIUM CELL; FEMALE; FIBROBLAST; HEART DEVELOPMENT; HEART MUSCLE ISCHEMIA; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; UPREGULATION; VASCULAR SMOOTH MUSCLE; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CELL MOTION; CHICK EMBRYO; DEFICIENCY; EMBRYOLOGY; KNOCKOUT MOUSE; METABOLISM; ORGANOGENESIS; PERICARDIUM; PHYSIOLOGY; SPECIES DIFFERENCE; TRANSGENIC MOUSE;

ANIMALS; CELL MOVEMENT; CHICK EMBRYO; CORONARY VESSELS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; ORGANOGENESIS; PERICARDIUM; SPECIES SPECIFICITY; T-BOX DOMAIN PROTEINS;

EID: 84924847481     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.115.304379     Document Type: Article

References (47)

1. Olivey HE, Svensson EC. Epicardial-myocardial signaling directing coronary vasculogenesis. Circ Res. 2010;106:818-832.
2. Pérez-Pomares JM, de la Pompa JL. Signaling during epicardium and coronary vessel development. Circ Res. 2011;109:1429-1442.
3. Kovacic JC, Mercader N, Torres M, Boehm M, Fuster V. Epithelial-to-mesenchymal and endothelial-to-mesenchymal transition: from cardiovascular development to disease. Circulation. 2012;125:1795-1808.
4. Tian X, Hu T, Zhang H, et al. Subepicardial endothelial cells invade the embryonic ventricle wall to form coronary arteries. Cell Res. 2013;23:1075-1090.
5. Red-Horse K, Ueno H, Weissman IL, Krasnow MA. Coronary arteries form by developmental reprogramming of venous cells. Nature. 2010;464:549-553.
6. Wu B, Zhang Z, Lui W, Chen X, Wang Y, Chamberlain AA, Moreno-Rodriguez RA, Markwald RR, O'Rourke BP, Sharp DJ, Zheng D, Lenz J, Baldwin HS, Chang CP, Zhou B. Endocardial cells form the coronary arteries by angiogenesis through myocardial-endocardial VEGF signaling. Cell. 2012;151:1083-1096.
7. Katz TC, Singh MK, Degenhardt K, Rivera-Feliciano J, Johnson RL, Epstein JA, Tabin CJ. Distinct compartments of the proepicar-dial organ give rise to coronary vascular endothelial cells. Dev Cell. 2012;22:639-650.
8. Wessels A, van den Hoff MJ, Adamo RF, Phelps AL, Lockhart MM, Sauls K, Briggs LE, Norris RA, van Wijk B, Perez-Pomares JM, Dettman RW, Burch JB. Epicardially derived fbroblasts preferentially contribute to the parietal leafets of the atrioventricular valves in the murine heart. Dev Biol. 2012;366:111-124.
9. Christoffels VM, Grieskamp T, Norden J, Mommersteeg MT, Rudat C, Kispert A. Tbx18 and the fate of epicardial progenitors. Nature. 2009;458:E8-9; discussion E9.
10. Lockhart MM, Phelps AL, van den Hoff MJ, Wessels A. The epicardium and the development of the atrioventricular junction in the murine heart. J Dev Biol. 2014;2:1-17.
11. Choi WY, Poss KD. Cardiac regeneration. Curr Top Dev Biol. 2012;100:319-344.
12. Acharya A, Baek ST, Huang G, Eskiocak B, Goetsch S, Sung CY, Banf S, Sauer MF, Olsen GS, Duffeld JS, Olson EN, Tallquist MD. The bHLH transcription factor Tcf21 is required for lineage-specifc EMT of cardiac fbroblast progenitors. Development. 2012;139:2139-2149.
13. Braitsch CM, Combs MD, Quaggin SE, Yutzey KE. Pod1/Tcf21 is regulated by retinoic acid signaling and inhibits differentiation of epicardi-um-derived cells into smooth muscle in the developing heart. Dev Biol. 2012;368:345-357.
14. Baek ST, Tallquist MD. Nf1 limits epicardial derivative expansion by regulating epithelial to mesenchymal transition and proliferation. Development. 2012;139:2040-2049.
15. Wu SP, Dong XR, Regan JN, Su C, Majesky MW. Tbx18 regulates development of the epicardium and coronary vessels. Dev Biol. 2013;383:307-320.
16. Hatcher CJ, Diman NY, Kim MS, Pennisi D, Song Y, Goldstein MM, Mikawa T, Basson CT. A role for Tbx5 in proepicardial cell migration during cardiogenesis. Physiol Genomics. 2004;18:129-140.
17. Basson CT, Bachinsky DR, Lin RC, Levi T, Elkins JA, Soults J, Grayzel D, Kroumpouzou E, Traill TA, Leblanc-Straceski J, Renault B, Kucherlapati R, Seidman JG, Seidman CE. Mutations in human TBX5 [corrected] cause limb and cardiac malformation in Holt-Oram syndrome. Nat Genet. 1997;15:30-35.
18. Li QY, Newbury-Ecob RA, Terrett JA, et al. Holt-Oram syndrome is caused by mutations in tbx5, a member of the brachyury (t) gene family. Nat Genet. 1997;15:21-29.
19. Dias RR, Albuquerque JM, Pereira AC, Stolf NA, Krieger JE, Mady C, Oliveira SA. Holt-Oram syndrome presenting as agenesis of the left pericardium. Int J Cardiol. 2007;114:98-100.
20. Vianna CB, Miura N, Pereira AC, Jatene MB. Holt-Oram syndrome: novel TBX5 mutation and associated anomalous right coronary artery. Cardiol Young. 2011;21:351-353.
21. Bruneau BG, Nemer G, Schmitt JP, Charron F, Robitaille L, Caron S, Conner DA, Gessler M, Nemer M, Seidman CE, Seidman JG. A murine model of Holt-Oram syndrome defnes roles of the T-box transcription factor Tbx5 in cardiogenesis and disease. Cell. 2001;106:709-721.
22. del Monte G, Casanova JC, Guadix JA, MacGrogan D, Burch JB, Pérez-Pomares JM, de la Pompa JL. Differential Notch signaling in the epi-cardium is required for cardiac infow development and coronary vessel morphogenesis. Circ Res. 2011;108:824-836.
23. Bimber B, Dettman RW, Simon HG. Differential regulation of Tbx5 protein expression and sub-cellular localization during heart development. Dev Biol. 2007;302:230-242.
24. Bruneau BG, Logan M, Davis N, Levi T, Tabin CJ, Seidman JG, Seidman CE. Chamber-specifc cardiac expression of Tbx5 and heart defects in Holt-Oram syndrome. Dev Biol. 1999;211:100-108.
25. Hatcher CJ, Goldstein MM, Mah CS, Delia CS, Basson CT. Identifcation and localization of TBX5 transcription factor during human cardiac morphogenesis. Dev Dyn. 2000;219:90-95.
26. Mikawa T, Fischman DA, Dougherty JP, Brown AM. In vivo analysis of a new lacZ retrovirus vector suitable for cell lineage marking in avian and other species. Exp Cell Res. 1991;195:516-523.
27. Hatcher CJ, Kim MS, Mah CS, Goldstein MM, Wong B, Mikawa T, Basson CT. TBX5 transcription factor regulates cell proliferation during cardiogenesis. Dev Biol. 2001;230:177-188.
28. Hirose T, Karasawa M, Sugitani Y, Fujisawa M, Akimoto K, Ohno S, Noda T. PAR3 is essential for cyst-mediated epicardial development by establishing apical cortical domains. Development. 2006;133:1389-1398.
29. Barnes RM, Firulli BA, VanDusen NJ, Morikawa Y, Conway SJ, Cserjesi P, Vincentz JW, Firulli AB. Hand2 loss-of-function in Hand1-expressing cells reveals distinct roles in epicardial and coronary vessel development. Circ Res. 2011;108:940-949.
30. Wu M, Smith CL, Hall JA, Lee I, Luby-Phelps K, Tallquist MD. Epicardial spindle orientation controls cell entry into the myocardium. Dev Cell. 2010;19:114-125.
31. Martínez-Estrada OM, Lettice LA, Essaf A, Guadix JA, Slight J, Velecela V, Hall E, Reichmann J, Devenney PS, Hohenstein P, Hosen N, Hill RE, Muñoz-Chapuli R, Hastie ND. Wt1 is required for cardiovascular progenitor cell formation through transcriptional control of Snail and E-cadherin. Nat Genet. 2010;42:89-93.
32. von Gise A, Zhou B, Honor LB, Ma Q, Petryk A, Pu WT. WT1 regulates epicardial epithelial to mesenchymal transition through β-catenin and reti-noic acid signaling pathways. Dev Biol. 2011;356:421-431.
33. Hernandez OM, Szczesna-Cordary D, Knollmann BC, Miller T, Bell M, Zhao J, Sirenko SG, Diaz Z, Guzman G, Xu Y, Wang Y, Kerrick WG, Potter JD. F110I and R278C troponin T mutations that cause familial hypertrophic cardiomyopathy affect muscle contraction in transgenic mice and reconstituted human cardiac fbers. J Biol Chem. 2005;280:37183-37194.
34. Jenkins SJ, Hutson DR, Kubalak SW. Analysis of the proepicardium-epi-cardium transition during the malformation of the RXRalpha-/-epicar-dium. Dev Dyn. 2005;233:1091-1101.
35. Apte SS. A disintegrin-like and metalloprotease (reprolysin type) with thrombospondin type 1 motifs: the ADAMTS family. Int J Biochem Cell Biol. 2004;36:981-985.
36. Sengbusch JK, He W, Pinco KA, Yang JT. Dual functions of [alpha]4[beta]1 integrin in epicardial development: initial migration and long-term attachment. J Cell Biol. 2002;157:873-882.
37. Gross JC, Schreiner A, Engels K, Starzinski-Powitz A. E-cadherin surface levels in epithelial growth factor-stimulated cells depend on adherens junction protein shrew-1. Mol Biol Cell. 2009;20:3598-3607.
38. Petrou P, Pavlakis E, Dalezios Y, Chalepakis G. Basement membrane localization of Frem3 is independent of the Fras1/Frem1/Frem2 protein complex within the sublamina densa. Matrix Biol. 2007;26:652-658.
39. Sekine K, Kawauchi T, Kubo K, Honda T, Herz J, Hattori M, Kinashi T, Nakajima K. Reelin controls neuronal positioning by promoting cell-matrix adhesion via inside-out activation of integrin α5β1. Neuron. 2012;76:353-369.
40. Liu J, Stainier DY. Tbx5 and Bmp signaling are essential for proepicar-dium specifcation in zebrafsh. Circ Res. 2010;106:1818-1828.
41. Xie L, Hoffmann AD, Burnicka-Turek O, Friedland-Little JM, Zhang K, Moskowitz IP. Tbx5-hedgehog molecular networks are essential in the second heart feld for atrial septation. Dev Cell. 2012;23:280-291.
42. Singh MK, Lu MM, Massera D, Epstein JA. MicroRNA-processing enzyme Dicer is required in epicardium for coronary vasculature development. J Biol Chem. 2011;286:41036-41045.
43. Phillips HM, Hildreth V, Peat JD, Murdoch JN, Kobayashi K, Chaudhry B, Henderson DJ. Non-cell-autonomous roles for the planar cell polarity gene Vangl2 in development of the coronary circulation. Circ Res. 2008;102:615-623.
44. Rhee DY, Zhao XQ, Francis RJ, Huang GY, Mably JD, Lo CW. Connexin 43 regulates epicardial cell polarity and migration in coronary vascular development. Development. 2009;136:3185-3193.
45. Mikawa T, Gourdie RG. Pericardial mesoderm generates a population of coronary smooth muscle cells migrating into the heart along with ingrowth of the epicardial organ. Dev Biol. 1996;174:221-232.
46. Nadeau M, Georges RO, Laforest B, Yamak A, Lefebvre C, Beauregard J, Paradis P, Bruneau BG, Andelfnger G, Nemer M. An endocardial pathway involving Tbx5, Gata4, and Nos3 required for atrial septum formation. Proc Natl Acad Sci USA. 2010;107:19356-19361.
47. Zhu Y, Gramolini AO, Walsh MA, Zhou YQ, Slorach C, Friedberg MK, Takeuchi JK, Sun H, Henkelman RM, Backx PH, Redington AN, Maclennan DH, Bruneau BG. Tbx5-dependent pathway regulating dia-stolic function in congenital heart disease. Proc Natl Acad Sci USA. 2008;105:5519-5524.