An Epicardial Floor Plan for Building and Rebuilding the Mammalian Heart

Current Topics in Developmental Biology

Volumn 100, Issue , 2012, Pages 233-251

  Riley, Paul R ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Cardiomyocytes; Coronary vessels; Endothelial cells; Epicardium; Myocardial regeneration; Neovascularization; Proepicardial organ; Vascular smooth muscle cells

Indexed keywords

EID: 84858775764     PISSN: 00702153     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-387786-4.00007-5     Document Type: Chapter

References (58)

1. Bax N.A., Pijnappels D.A., van Oorschot A.A., Winter E.M., de Vries A.A., van T.J., Braun J., Maas S., Schalij M.J., Atsma D.E., Goumans M.J., Gittenberger-de Groot A.C. Epithelial-to-mesenchymal transformation alters electrical conductivity of human epicardial cells. J. Cell. Mol. Med. 2011, 15(12):2675-2683. DOI:10.1111/j.1582-4934.2011.01266.x. Epub ahead of print.
2. Bock-Marquette I., Shrivastava S., Pipes G.C., Thatcher J.E., Blystone A., Shelton J.M., Galindo C.L., Melegh B., Srivastava D., Olson E.N., Dimaio J.M. Thymosin beta4 mediated PKC activation is essential to initiate the embryonic coronary developmental program and epicardial progenitor cell activation in adult mice in vivo. J. Cell Mol. Cardiol. 2009, 46:728-738.
3. Cai C.L., Martin J.C., Sun Y., Cui L., Wang L., Ouyang K., Yang L., Bu L., Liang X., Zhang X., Stallcup W.B., Denton C.P., et al. A myocardial lineage derives from Tbx18 epicardial cells. Nature 2008, 454:104-108.
4. Chen T.H., Chang T.C., Kang J.O., Choudhary B., Makita T., Tran C.M., Burch J.B., Eid H., Sucov H.M. Epicardial induction of fetal cardiomyocyte proliferation via a retinoic acid-inducible trophic factor. Dev. Biol. 2002, 250:198-207.
5. Christoffels V.M., Grieskamp T., Norden J., Mommersteeg M.T., Rudat C., Kispert A. Tbx18 and the fate of epicardial progenitors. Nature 2009, 458:E8-E9.
6. Corda S., Mebazaa A., Gandolfini M.P., Fitting C., Marotte F., Peynet J., Charlemagne D., Cavaillon J.M., Payen D., Rappaport L., Samuel J.L. Trophic effect of human pericardial fluid on adult cardiac myocytes. Differential role of fibroblast growth factor-2 and factors related to ventricular hypertrophy. Circ. Res. 1997, 81:679-687.
7. Di Meglio F., Castaldo C., Nurzynska D., Romano V., Miraglia R., Montagnani S. Epicardial cells are missing from the surface of hearts with ischemic cardiomyopathy: A useful clue about the self-renewal potential of the adult human heart?. Int. J. Cardiol. 2009, 145:e44-e46.
8. Gonzalez-Rosa J.M., Martin V., Peralta M., Torres M., Mercader N. Extensive scar formation and regression during heart regeneration after cryoinjury in zebrafish. Development 2011, 138:1663-1674.
9. Grieskamp T., Rudat C., Ludtke T.H., Norden J., Kispert A. Notch signaling regulates smooth muscle differentiation of epicardium-derived cells. Circ. Res. 2011, 108:813-823.
10. Guadix J.A., Ruiz-Villalba A., Lettice L., Velecela V., Munoz-Chapuli R., Hastie N.D., Perez-Pomares J.M., Martinez-Estrada O.M. Wt1 controls retinoic acid signalling in embryonic epicardium through transcriptional activation of Raldh2. Development 2011, 138:1093-1097.
11. Iwakura A., Fujita M., Hasegawa K., Sawamura T., Nohara R., Sasayama S., Komeda M. Pericardial fluid from patients with unstable angina induces vascular endothelial cell apoptosis. J. Am. Coll. Cardiol. 2000, 35:1785-1790.
12. Jopling C., Sleep E., Raya M., Marti M., Raya A., Belmonte J.C. Zebrafish heart regeneration occurs by cardiomyocyte dedifferentiation and proliferation. Nature 2010, 464:606-609.
13. Kang J.O., Sucov H.M. Convergent proliferative response and divergent morphogenic pathways induced by epicardial and endocardial signaling in fetal heart development. Mech. Dev. 2005, 122:57-65.
14. Kikuchi K., Holdway J.E., Werdich A.A., Anderson R.M., Fang Y., Egnaczyk G.F., Evans T., Macrae C.A., Stainier D.Y., Poss K.D. Primary contribution to zebrafish heart regeneration by gata4(+) cardiomyocytes. Nature 2010, 464:601-605.
15. Kikuchi K., Gupta V., Wang J., Holdway J.E., Wills A.A., Fang Y., Poss K.D. tcf21+ epicardial cells adopt non-myocardial fates during zebrafish heart development and regeneration. Development 2011, 138:2895-2902.
16. Kikuchi K., Holdway J.E., Major R.J., Blum N., Dahn R.D., Begemann G., Poss K.D. Retinoic acid production by endocardium and epicardium is an injury response essential for zebrafish heart regeneration. Dev. Cell 2011, 20:397-404.
17. Kraus F., Haenig B., Kispert A. Cloning and expression analysis of the mouse T-box gene Tbx18. Mech. Dev. 2001, 100:83-86.
18. Kurkiewicz T. O histogenezie miesna sercowego zwierzat kregowych-Zur Histogenese des Herzmuskels der Wirbeltiere. Bull. Int. Acad. Sci. Cracovie 1909, 148-191.
19. Lee K.F., Simon H., Chen H., Bates B., Hung M.C., Hauser C. Requirement for neuregulin receptor erbB2 in neural and cardiac development. Nature 1995, 378:394-398.
20. Lepilina A., Coon A.N., Kikuchi K., Holdway J.E., Roberts R.W., Burns C.G., Poss K.D. A dynamic epicardial injury response supports progenitor cell activity during zebrafish heart regeneration. Cell 2006, 127:607-619.
21. Limana F., Zacheo A., Mocini D., Mangoni A., Borsellino G., Diamantini A., De M.R., Battistini L., Vigna E., Santini M., Loiaconi V., Pompilio G., et al. Identification of myocardial and vascular precursor cells in human and mouse epicardium. Circ. Res. 2007, 101:1255-1265.
22. Limana F., Bertolami C., Mangoni A., Di C.A., Avitabile D., Mocini D., Iannelli P., De M.R., Marchetti C., Pozzoli O., Gentili C., Zacheo A., et al. Myocardial infarction induces embryonic reprogramming of epicardial c-kit(+) cells: Role of the pericardial fluid. J. Mol. Cell. Cardiol. 2010, 48:609-618.
23. Manasek F.J. Embryonic development of the heart. II. Formation of the epicardium. J. Embryol. Exp. Morphol. 1969, 22:333-348.
24. Manner J., Perez-Pomares J.M., Macias D., Munoz-Chapuli R. The origin, formation and developmental significance of the epicardium: A review. Cells Tissues Organs 2001, 169:89-103.
25. Martinez-Estrada O.M., Lettice L.A., Essafi A., Guadix J.A., Slight J., Velecela V., Hall E., Reichmann J., Devenney P.S., Hohenstein P., Hosen N., Hill R.E., et al. Wt1 is required for cardiovascular progenitor cell formation through transcriptional control of Snail and E-cadherin. Nat. Genet. 2010, 42:89-93.
26. Mellgren A.M., Smith C.L., Olsen G.S., Eskiocak B., Zhou B., Kazi M.N., Ruiz F.R., Pu W.T., Tallquist M.D. Platelet-derived growth factor receptor beta signaling is required for efficient epicardial cell migration and development of two distinct coronary vascular smooth muscle cell populations. Circ. Res. 2008, 103:1393-1401.
27. Merki E., Zamora M., Raya A., Kawakami Y., Wang J., Zhang X., Burch J., Kubalak S.W., Kaliman P., Belmonte J.C., Chien K.R., Ruiz-Lozano P. Epicardial retinoid X receptor alpha is required for myocardial growth and coronary artery formation. Proc. Natl. Acad. Sci. USA 2005, 102:18455-18460.
28. Mollier S. Die erste anlage des herzens bei den wirbeltieren. Handbuch der vergleichenden und experimentellen Entwicklungslehre der Wirbeltiere 1906, 1:1026-1051. Gustav Fischer, Jena, Sect 1. O. Hertwig (Ed.).
29. Moore A.W., McInnes L., Kreidberg J., Hastie N.D., Schedl A. YAC complementation shows a requirement for Wt1 in the development of epicardium, adrenal gland and throughout nephrogenesis. Development 1999, 126:1845-1857.
30. Moss J.B., Xavier-Neto J., Shapiro M.D., Nayeem S.M., McCaffery P., Drager U.C., Rosenthal N. Dynamic patterns of retinoic acid synthesis and response in the developing mammalian heart. Dev. Biol. 1998, 199:55-71.
31. Olivey H.E., Svensson E.C. Epicardial-myocardial signaling directing coronary vasculogenesis. Circ. Res. 2010, 106:818-832.
32. Olivotto I., Cecchi F., Poggesi C., Yacoub M.H. Developmental origins of hypertrophic cardiomyopathy phenotypes: A unifying hypothesis. Nat. Rev. Cardiol. 2009, 6:317-321.
33. Pennisi D.J., Mikawa T. FGFR-1 is required by epicardium-derived cells for myocardial invasion and correct coronary vascular lineage differentiation. Dev. Biol. 2009, 328:148-159.
34. Perez-Pomares J.M., Carmona R., Gonzalez-Iriarte M., Atencia G., Wessels A., Munoz-Chapuli R. Origin of coronary endothelial cells from epicardial mesothelium in avian embryos. Int. J. Dev. Biol. 2002, 46:1005-1013.
35. Perez-Pomares J.M., Phelps A., Sedmerova M., Carmona R., Gonzalez-Iriarte M., Munoz-Chapuli R., Wessels A. Experimental studies on the spatiotemporal expression of WT1 and RALDH2 in the embryonic avian heart: A model for the regulation of myocardial and valvuloseptal development by epicardially derived cells (EPDCs). Dev. Biol. 2002, 247:307-326.
36. Phillips H.M., Hildreth V., Peat J.D., Murdoch J.N., Kobayashi K., Chaudhry B., Henderson D.J. Non-cell-autonomous roles for the planar cell polarity gene Vangl2 in development of the coronary circulation. Circ. Res. 2008, 102:615-623.
37. Poelmann R.E., Gittenberger-de Groot A.C., Mentink M.M., Bokenkamp R., Hogers B. Development of the cardiac coronary vascular endothelium, studied with antiendothelial antibodies, in chicken-quail chimeras. Circ. Res. 1993, 73:559-568.
38. Porrello E.R., Mahmoud A.I., Simpson E., Hill J.A., Richardson J.A., Olson E.N., Sadek H.A. Transient regenerative potential of the neonatal mouse heart. Science 2011, 331:1078-1080.
39. Red-Horse K., Ueno H., Weissman I.L., Krasnow M.A. Coronary arteries form by developmental reprogramming of venous cells. Nature 2010, 464:549-553.
40. Remak R. Untersuchungen über die entwicklung der wirbelthiere 1855, Reimer, Berlin.
41. Riley P.R., Smart N. Vascularizing the heart. Cardiovasc. Res. 2011, 91:260-268.
42. Serluca F.C. Development of the proepicardial organ in the zebrafish. Dev. Biol. 2008, 315:18-27.
43. Smart N., Risebro C.A., Melville A.A., Moses K., Schwartz R.J., Chien K.R., Riley P.R. Thymosin beta4 induces adult epicardial progenitor mobilization and neovascularization. Nature 2007, 445:177-182.
44. Smart N., Risebro C.A., Clark J.E., Ehler E., Miquerol L., Rossdeutsch A., Marber M.S., Riley P.R. Thymosin β4 facilitates epicardial neovascularization of the injured adult heart. Ann. N. Y. Acad. Sci. 2010, 1194:97-104.
45. Smart N., Bollini S., Dube K.N., Vieira J.M., Zhou B., Davidson S., Yellon D., Riegler J., Price A.N., Lythgoe M.F., Pu W.T., Riley P.R. De novo cardiomyocytes from within the activated adult heart after injury. Nature 2011, 474:640-644.
46. Sucov H.M., Gu Y., Thomas S., Li P., Pashmforoush M. Epicardial control of myocardial proliferation and morphogenesis. Pediatr. Cardiol. 2009, 30:617-625.
47. Tomanek R., Zheng W., Yue X. Growth factor activation in myocardial vascularization: Therapeutic implications. Mol. Cell. Biochem. 2004, 264:3-11.
48. Torlopp A., Schlueter J., Brand T. Role of fibroblast growth factor signaling during proepicardium formation in the chick embryo. Dev. Dyn. 2010, 239:2393-2403.
49. vanTuyn J., Atsma D.E., Winter E.M., van der Velde-van Dijke I., Pijnappels D.A., Bax N.A., Knaan-Shanzer S., Gittenberger-de Groot A.C., Poelmann R.E., van der L.A., van der Wall E.E., Schalij M.J., de Vries A.A. Epicardial cells of human adults can undergo an epithelial-to-mesenchymal transition and obtain characteristics of smooth muscle cells in vitro. Stem Cells 2006, 25:271-278.
50. van W.B., van den B.G., Bu-Issa R., Barnett P., van der Velden S., Schmidt M., Ruijter J.M., Kirby M.L., Moorman A.F., van den Hoff M.J. Epicardium and myocardium separate from a common precursor pool by crosstalk between bone morphogenetic protein- and fibroblast growth factor-signaling pathways. Circ. Res. 2009, 105:431-441.
51. Vincent S.D., Buckingham M.E. How to make a heart: The origin and regulation of cardiac progenitor cells. Curr. Top. Dev. Biol. 2010, 90:1-41.
52. Wagner K.D., Wagner N., Bondke A., Nafz B., Flemming B., Theres H., Scholz H. The Wilms' tumor suppressor Wt1 is expressed in the coronary vasculature after myocardial infarction. FASEB J. 2002, 16:1117-1119.
53. Wills A.A., Holdway J.E., Major R.J., Poss K.D. Regulated addition of new myocardial and epicardial cells fosters homeostatic cardiac growth and maintenance in adult zebrafish. Development 2008, 135:183-192.
54. Winter E.M., Grauss R.W., Hogers B., Van T.J., van der G.R., Lie-Venema H., Steijn R.V., Maas S., DeRuiter M.C., Devries A.A., Steendijk P., Doevendans P.A., et al. Preservation of left ventricular function and attenuation of remodeling after transplantation of human epicardium-derived cells into the infarcted mouse heart. Circulation 2007, 116:917-927.
55. Yoneda T., Fujita M., Kihara Y., Hasegawa K., Sawamura T., Tanaka T., Inanami M., Nohara R., Sasayama S. Pericardial fluid from patients with ischemic heart disease accelerates the growth of human vascular smooth muscle cells. Jpn. Circ. J. 2000, 64:495-498.
56. Zamora M., Manner J., Ruiz-Lozano P. Epicardium-derived progenitor cells require beta-catenin for coronary artery formation. Proc. Natl. Acad. Sci. USA 2007, 104:18109-18114.
57. Zhou B., Ma Q., Rajagopal S., Wu S.M., Domian I., Rivera-Feliciano J., Jiang D., von G.A., Ikeda S., Chien K.R., Pu W.T. Epicardial progenitors contribute to the cardiomyocyte lineage in the developing heart. Nature 2008, 454:109-113.
58. Zhou B., Honor L.B., He H., Ma Q., Oh J.H., Butterfield C., Lin R.Z., Melero-Martin J.M., Dolmatova E., Duffy H.S., Gise A., Zhou P., et al. Adult mouse epicardium modulates myocardial injury by secreting paracrine factors. J. Clin. Invest. 2011, 121:1894-1904.