The identification of different endothelial cell populations within the mouse proepicardium

Developmental Dynamics

Volumn 240, Issue 10, 2011, Pages 2344-2353

  Cossette, Stephanie ^a   Misra, Ravi ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

Coronary vasculogenesis; Endothelial cells; Liver bud; Proepicardium; Sinus venosus

Indexed keywords

CELL MARKER;

ANIMAL TISSUE; ARTICLE; CELL POPULATION; CELLULAR DISTRIBUTION; EMBRYO; EMBRYONIC STRUCTURES; ENDOTHELIUM CELL; EPICARDIUM; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROEPICARDIUM; SINUS VENOSUS;

ANIMALS; ANTIGENS, CD31; BIOLOGICAL MARKERS; EMBRYO, MAMMALIAN; ENDOTHELIAL CELLS; FEMALE; HEART; MICE; MORPHOGENESIS; PERICARDIUM;

EID: 80052964970     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.22724     Document Type: Article

References (43)

1. Baldwin H, Shen H, Yan H, DeLisser H, Chung A, Mickanin C, Trask T, Kirschbaum N, Newman P, Albelda S, et al. 1994. Platelet endothelial cell adhesion molecule-1 (PECAM-1/CD31): alternatively spliced, functionally distinct isoforms expressed during mammalian cardiovascular development. Development 120: 2539-2553.
2. Battle M, Konopka G, Parviz F, Gaggl A, Yang C, Sladek F, Duncan S. 2006. Hepatocyte nuclear factor 4alpha orchestrates expression of cell adhesion proteins during the epithelial transformation of the developing liver. Proc Natl Acad Sci U S A 103: 8419-8424.
3. Burke Z, Oliver G. 2002. Prox1 is an early specific marker for the developing liver and pancreas in the mammalian foregut endoderm. Mech Dev 118: 147-155.
4. Cai C, Martin J, Sun Y, Cui L, Wang L, Ouyang K, Yang L, Bu L, Liang X, Zhang X, Stallcup W, Denton C, McCulloch A, Chen J, Evans S. 2008. A myocardial lineage derives from Tbx18 epicardial cells. Nature 454: 104-108.
5. del Monte G, Casanova J, Guadix J, MacGrogan D, Burch J, Perez-Pomares J, de la Pompa J. 2011. Differential Notch signaling in the epicardium is required for cardiac inflow development and coronary vessel morphogenesis. Circ Res 108: 824-836.
6. Dettman R, Denetclaw WJ, Ordahl C, Bristow J. 1998. Common epicardial origin of coronary vascular smooth muscle, perivascular fibroblasts, and intermyocardial fibroblasts in the avian heart. Dev Biol 193: 169-181.
7. Drake C, Fleming P. 2000. Vasculogenesis in the day 6.5 to 9.5 mouse embryo. Blood 95: 1671-1679.
8. Ferguson Jr, Kelley R, Patterson C. 2005. Mechanisms of endothelial differentiation in embryonic vasculogenesis. Arterioscler Thromb Vasc Biol 25: 2246-2254.
9. Gittenberger-de Groot A, Vrancken Peeters M, Mentink M, Gourdie R, Poelmann R. 1998. Epicardium-derived cells contribute a novel population to the myocardial wall and the atrioventricular cushions. Circ Res 82: 1043-1052.
10. Gittenberger-de Groot AC, Vrancken Peeters MP, Bergwerff M, Mentink MM, Poelmann RE. 2000. Epicardial outgrowth inhibition leads to compensatory mesothelial outflow tract collar and abnormal cardiac septation and coronary formation. Circ Res 87: 969-971.
11. Guadix J, Carmona R, Munoz-Chapuli R, Perez-Pomares J. 2006. In vivo and in vitro analysis of the vasculogenic potential of avian proepicardial and epicardial cells. Dev Dyn 235: 1014-1026.
12. Holtz ML, Misra RP. 2008. Endothelial-specific ablation of Serum Response Factor causes hemorrhaging, yolk sac vascular failure, and embryonic lethality. BMC Dev Biol 8: 65.
13. Kraus F, Haenig B, Kispert A. 2001. Cloning and expression analysis of the mouse T-box gene Tbx18. Mech Dev 100: 83-86.
14. Lampugnani M, Resnati M, Raiteri M, Pigott R, Pisacane A, Houen G, Ruco L, Dejana E. 1992. A novel endothelial-specific membrane protein is a marker of cell-cell contacts. J Cell Biol 118: 1511-1522.
15. Li J, Ning G, Duncan S. 2000. Mammalian hepatocyte differentiation requires the transcription factor HNF-4alpha. Genes Dev 14: 464-474.
16. Lie-Venema H, Eralp I, Maas S, Gittenberger-De Groot A, Poelmann R, DeRuiter M. 2005. Myocardial heterogeneity in permissiveness for epicardium-derived cells and endothelial precursor cells along the developing heart tube at the onset of coronary vascularization. Anat Rec A Discov Mol Cell Evol Biol 282: 120-129.
17. Manner J, Schlueter J, Brand T. 2005. Experimental analyses of the function of the proepicardium using a new microsurgical procedure to induce loss-of-proepicardial-function in chick embryos. Dev Dyn 233: 1454-1463.
18. McLaughlin F, Ludbrook V, Cox J, von Carlowitz I, Brown S, Randi A. 2001. Combined genomic and antisense analysis reveals that the transcription factor Erg is implicated in endothelial cell differentiation. Blood 98: 3332-3339.
19. Mikawa T, Fischman D. 1992. Retroviral analysis of cardiac morphogenesis: discontinuous formation of coronary vessels. Proc Natl Acad Sci U S A 89: 9504-9508.
20. Mikawa T, Gourdie RG. 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.
21. Millauer B, Wizigmann-Voos S, Schnurch H, Martinez R, Moller N, Risau W, Ullrich A. 1993. High affinity VEGF binding and developmental expression suggest Flk-1 as a major regulator of vasculogenesis and angiogenesis. Cell 72: 835-846.
22. Mohamed A, Tan S, Mikhalkevich N, Ponniah S, Vasioukhin V, Bieberich C, Sesterhenn I, Dobi A, Srivastava S, Sreenath T. 2010. Ets family protein, erg expression in developing and adult mouse tissues by a highly specific monoclonal antibody. J Cancer 1: 197-208.
23. Moore AW, McInnes L, Kreidberg J, Hastie ND, Schedl A. 1999. YAC complementation shows a requirement for Wt1 in the development of epicardium, adrenal gland and throughout nephrogenesis. Development 126: 1845-1857.
24. Perez-Pomares JM, Macias D, Garcia-Garrido L, Munoz-Chapuli R. 1998a. Immunolocalization of the vascular endothelial growth factor receptor-2 in the subepicardial mesenchyme of hamster embryos: identification of the coronary vessel precursors. Histochem J 30: 627-634.
25. Perez-Pomares JM, Macias D, Garcia-Garrido L, Munoz-Chapuli R. 1998b. The origin of the subepicardial mesenchyme in the avian embryo: an immunohistochemical and quail-chick chimera study. Dev Biol 200: 57-68.
26. Perez-Pomares J, Carmona R, Gonzalez-Iriarte M, Atencia G, Wessels A, Munoz-Chapuli R. 2002a. Origin of coronary endothelial cells from epicardial mesothelium in avian embryos. Int J Dev Biol 46: 1005-1013.
27. Perez-Pomares JM, Phelps A, Sedmerova M, Carmona R, Gonzalez-Iriarte M, Munoz-Chapuli R, Wessels A. 2002b. 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 247: 307-326.
28. Perez-Pomares J, Carmona R, Gonzalez-Iriarte M, Macias D, Guadix J, Munoz-Chapuli R. 2004. Contribution of mesothelium-derived cells to liver sinusoids in avian embryos. Dev Dyn 229: 465-474.
29. Poelmann R, Gittenberger-de Groot A, Mentink M, Bokenkamp R, Hogers B. 1993. Development of the cardiac coronary vascular endothelium, studied with antiendothelial antibodies, in chicken-quail chimeras. Circ Res 73: 559-568.
30. Red-Horse K, Ueno H, Weissman I, Krasnow M. 2010. Coronary arteries form by developmental reprogramming of venous cells. Nature 464: 549-553.
31. Tevosian S, Deconinck A, Tanaka M, Schinke M, Litovsky S, Izumo S, Fujiwara Y, Orkin S. 2000. FOG-2, a cofactor for GATA transcription factors, is essential for heart morphogenesis and development of coronary vessels from epicardium. Cell 101: 729-739.
32. Tremblay K, Zaret K. 2005. Distinct populations of endoderm cells converge to generate the embryonic liver bud and ventral foregut tissues. Dev Biol 280: 87-99.
33. Viragh S, Challice CE. 1981. The origin of the epicardium and the embryonic myocardial circulation in the mouse. Anat Rec 201: 157-168.
34. Viragh S, Gittenberger-de Groot AC, Poelmann RE, Kalman F. 1993. Early development of quail heart epicardium and associated vascular and glandular structures. Anat Embryol (Berl) 188: 381-393.
35. Vittet D, Prandini M, Berthier R, Schweitzer A, Martin-Sisteron H, Uzan G, Dejana E. 1996. Embryonic stem cells differentiate in vitro to endothelial cells through successive maturation steps. Blood 88: 3424-3431.
36. Vlaeminck-Guillem V, Carrere S, Dewitte F, Stehelin D, Desbiens X, Duterque-Coquillaud M. 2000. The Ets family member Erg gene is expressed in mesodermal tissues and neural crests at fundamental steps during mouse embryogenesis. Mech Dev 91: 331-335.
37. Vrancken Peeters M, Gittenberger-de Groot A, Mentink M, Hungerford J, Little C, Poelmann R. 1997. The development of the coronary vessels and their differentiation into arteries and veins in the embryonic quail heart. Dev Dyn 208: 338-348.
38. Vrancken Peeters M, Gittenberger-de Groot A, Mentink M, Poelmann R. 1999. Smooth muscle cells and fibroblasts of the coronary arteries derive from epithelial-mesenchymal transformation of the epicardium. Anat Embryol (Berl) 199: 367-378.
39. Watanabe N, Nakagawa M, Hanato T, Takeuchi Y, Hara M, Yoshida T, Imanaka-Yoshida K. 2006. In vitro model for mouse coronary vasculogenesis. Anat Rec A Discov Mol Cell Evol Biol 288: 714-722.
40. Yamaguchi TP, Dumont DJ, Conlon RA, Breitman ML, Rossant J. 1993. flk-1, an flt-related receptor tyrosine kinase is an early marker for endothelial cell precursors. Development 118: 489-498.
41. Yang J, Rayburn H, Hynes R. 1995. Cell adhesion events mediated by alpha 4 integrins are essential in placental and cardiac development. Development 121: 549-560.
42. Zhou B, Ma Q, Rajagopal S, Wu S, Domian I, Rivera-Feliciano J, Jiang D, von Gise A, Ikeda S, Chien K, Pu W. 2008. Epicardial progenitors contribute to the cardiomyocyte lineage in the developing heart. Nature 454: 109-113.
43. Zhou B, von Gise A, Ma Q, Hu Y, Pu W. 2010. Genetic fate mapping demonstrates contribution of epicardium-derived cells to the annulus fibrosis of the mammalian heart. Dev Biol 338: 251-261.