Epicardial lineages and cardiac repair

Journal of Developmental Biology

Volumn 1, Issue 2, 2013, Pages 141-158

  Singh, Manvendra K ^a   Epstein, Jonathan A ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Cardiac regeneration; Epicardium; Epithelial to mesenchymal transition (EMT); Proepicardium

Indexed keywords

EID: 84975813991     PISSN: None     EISSN: 22213759     Source Type: Journal    
DOI: 10.3390/jdb1020141     Document Type: Review

References (105)

1. Mikawa, T.; Gourdie, R.G. 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.
2. 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.
3. Gittenberger-de Groot, A.C.; Vrancken Peeters, M.P.; Mentink, M.M.; Gourdie, R.G.; Poelmann, R.E. Epicardium-derived cells contribute a novel population to the myocardial wall and the atrioventricular cushions. Circ. Res. 1998, 82, 1043-1052.
4. Mikawa, T.; Fischman, D.A. Retroviral analysis of cardiac morphogenesis: discontinuous formation of coronary vessels. Proc. Natl. Acad. Sci. USA 1992, 89, 9504-9508.
5. Lie-Venema, H.; van den Akker, N.M.; Bax, N.A.; Winter, E.M.; Maas, S.; Kekarainen, T.; Hoeben, R.C.; deRuiter, M.C.; Poelmann, R.E.; Gittenberger-de Groot, A.C. Origin, fate, and function of epicardium-derived cells (EPDCs) in normal and abnormal cardiac development. Sci. World J. 2007, 7, 1777-1798.
6. von Gise, A.; Pu, W.T. Endocardial and epicardial epithelial to mesenchymal transitions in heart development and disease. Circ. Res. 2012, 110, 1628-1645.
7. Epstein, J.A. Franklin, H. Epstein Lecture. Cardiac development and implications for heart disease. N. Engl. J. Med. 2010, 363, 1638-1647.
8. Degenhardt, K.; Singh, M.K.; Epstein, J.A. New approaches under development: Cardiovascular embryology applied to heart disease. J. Clin. Invest. 2013, 123, 71-74.
9. Singh, M.K.; Lu, M.M.; Massera, D.; Epstein, J.A. MicroRNA-processing enzyme Dicer is required in epicardium for coronary vasculature development. J. Biol. Chem. 2011, 286, 41036-41045.
10. Limana, F.; Capogrossi, M.C.; Germani, A. The epicardium in cardiac repair: From the stem cell view. Pharmacol. Ther. 2011, 129, 82-96.
11. Kwee, L.; Baldwin, H.S.; Shen, H.M.; Stewart, C.L.; Buck, C.; Buck, C.A.; Labow, M.A. Defective development of the embryonic and extraembryonic circulatory systems in vascular cell adhesion molecule (VCAM-1) deficient mice. Development 1995, 121, 489-503.
12. Yang, J.T.; Rayburn, H.; Hynes, R.O. Cell adhesion events mediated by alpha 4 integrins are essential in placental and cardiac development. Development 1995, 121, 549-560.
13. Sengbusch, J.K.; He, W.; Pinco, K.A.; Yang, J.T. Dual functions of [alpha]4[beta]1 integrin in epicardial development: Initial migration and long-term attachment. J. Cell. Biol. 2002, 157, 873-882.
14. Mahtab, E.A.; Wijffels, M.C.; Van Den Akker, N.M.; Hahurij, N.D.; Lie-Venema, H.; Wisse, L.J.; Deruiter, M.C.; Uhrin, P.; Zaujec, J.; Binder, B.R.; Schalij, M.J.; Poelmann, R.E.; Gittenberger-De Groot, A.C. Cardiac malformations and myocardial abnormalities in podoplanin knockout mouse embryos: Correlation with abnormal epicardial development. Dev. Dyn. 2008, 237, 847-857.
15. von Gise, A.; Zhou, B.; Honor, L.B.; Ma, Q.; Petryk, A.; Pu, W.T. WT1 regulates epicardial epithelial to mesenchymal transition through beta-catenin and retinoic acid signaling pathways. Dev. Biol. 2011, 356, 421-431.
16. Guadix, J.A.; Ruiz-Villalba, A.; Lettice, L.; Velecela, V.; Muñoz-Chápuli, R.; Hastie, N.D.; Pérez-Pomares, J.M.; Martínez-Estrada, O.M. Wt1 controls retinoic acid signalling in embryonic epicardium through transcriptional activation of Raldh2. Development 2011, 138, 1093-1097.
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. 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; discussion E9-E10.
19. Greulich, F.; Farin, H.F.; Schuster-Gossler, K.; Kispert, A. Tbx18 function in epicardial development. Cardiovasc. Res. 2012, 96, 476-483.
20. Combs, M.D.; Braitsch, C.M.; Lange, A.W.; James, J.F.; Yutzey, K.E. NFATC1 promotes epicardium-derived cell invasion into myocardium. Development 2011, 138, 1747-1757.
21. Baek, S.T.; Tallquist, M.D. Nf1 limits epicardial derivative expansion by regulating epithelial to mesenchymal transition and proliferation. Development 2012, 139, 2040-2049.
22. Winter, E.M.; Gittenberger-de Groot, A.C. Epicardium-derived cells in cardiogenesis and cardiac regeneration. Cell. Mol. Life Sci. 2007, 64, 692-703.
23. 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.; McCulloch, A.; Chen, J.; Evans, S.M. A myocardial lineage derives from Tbx18 epicardial cells. Nature 2008, 454, 104-108.
24. Zhou, B.; Ma, Q.; Rajagopal, S.; Wu, S.M.; Domian, I.; Rivera-Feliciano, J.; Jiang, D.; von Gise, 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.
25. Katz, T.C.; Singh, M.K.; Degenhardt, K.; Rivera-Feliciano, J.; Johnson, R.L.; Epstein, J.A.; Tabin, C.J. Distinct compartments of the proepicardial organ give rise to coronary vascular endothelial cells. Dev. Cell 2012, 22, 639-650.
26. 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.
27. 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, Av.; Zhou, P.; Hu, Y.W.; Wang, G.; Zhang, B.; Wang, L.; Hall, J.L.; Moses, M.A.; McGowan, F.X.; Pu, W.T. Adult mouse epicardium modulates myocardial injury by secreting paracrine factors. J. Clin. Invest. 2011, 121, 1894-1904.
28. Lavine, K.J.; Lavine, K.J.; Yu, K.; White, A.C.; Zhang, X.; Smith, C.; Partanen, J.; Ornitz, D.M. Endocardial and epicardial derived FGF signals regulate myocardial proliferation and differentiation in vivo. Dev. Cell. 2005, 8, 85-95.
29. Tian, Y.; Morrisey, E.E. Importance of myocyte-nonmyocyte interactions in cardiac development and disease. Circ. Res. 2012, 110, 1023-1034.
30. Choi, W.Y.; Poss, K.D. Cardiac regeneration. Curr. Top. Dev. Biol. 2012, 100, 319-344.
31. Laflamme, M.A.; Murry, C.E. Heart regeneration. Nature 2011, 473, 326-335.
32. Laugwitz, K.L.; Moretti, A.; Caron, L.; Nakano, A.; Chien, K.R. Islet1 cardiovascular progenitors: a single source for heart lineages-Development 2008, 135, 193-205.
33. Wu, S.M.; Fujiwara, Y.; Cibulsky, S.M.; Clapham, D.E.; Lien, C.L.; Schultheiss, T.M.; Orkin, S.H. Developmental origin of a bipotential myocardial and smooth muscle cell precursor in the mammalian heart. Cell 2006, 127, 1137-1150.
34. Zhou, B.; von Gise, A.; Ma, Q.; Rivera-Feliciano, J.; Pu, W.T. Nkx2-5- and Isl1-expressing cardiac progenitors contribute to proepicardium. Biochem. Biophys. Res. Commun. 2008, 375, 450-453.
35. Manner, J. Does the subepicardial mesenchyme contribute myocardioblasts to the myocardium of the chick embryo heart-A quail-chick chimera study tracing the fate of the epicardial primordium. Anat. Rec. 1999, 255, 212-226.
36. Gourdie, R.G.; Cheng, G.; Thompson, R.P.; Mikawa, T. Retroviral cell lineage analysis in the developing chick heart. Meth. Mol. Biol 2000, 135, 297-304.
37. Perez-Pomares, J.M.; Carmona, R.; González-Iriarte, M.; Atencia, G.; Wessels, A.; Muñoz-Chápuli, R. Origin of coronary endothelial cells from epicardial mesothelium in avian embryos. Int. J. Dev. Biol. 2002, 46, 1005-1013.
38. Guadix, J.A.; Carmona, R.; Munoz-Chapuli, R.; Perez-Pomares, J.M. In vivo and in vitro analysis of the vasculogenic potential of avian proepicardial and epicardial cells. Dev. Dyn. 2006, 235, 1014-1026.
39. Parmacek, M.S.; Epstein, J.A. Cardiomyocyte renewal. N. Engl. J. Med. 2009, 361, 86-88.
40. Nag, A.C. Study of non-muscle cells of the adult mammalian heart: a fine structural analysis and distribution. Cytobios 1980, 28, 41-61.
41. Souders, C.A.; Bowers, S.L.; Baudino, T.A. Cardiac fibroblast: the renaissance cell. Circ. Res. 2009, 105, 1164-1176.
42. Zeisberg, E.M.; Kalluri, R. Origins of cardiac fibroblasts. Circ. Res. 2010, 107, 1304-1312.
43. Van den Akker, N.M.; Winkel, L.C.; Nisancioglu, M.H.; Maas, S.; Wisse, L.J.; Armulik, A.; Poelmann, R.E.; Lie-Venema, H.; Betsholtz, C.; Gittenberger-de Groot, A.C. PDGF-B signaling is important for murine cardiac development: its role in developing atrioventricular valves, coronaries, and cardiac innervation. Dev. Dyn. 2008, 237, 494-503.
44. Van Den Akker, N.M.; Lie-Venema, H.; Maas, S.; Eralp, I.; DeRuiter, M.C.; Poelmann, R.E.; Gittenberger-De Groot, A.C. Platelet-derived growth factors in the developing avian heart and maturating coronary vasculature. Dev. Dyn. 2005, 233, 1579-1588.
45. Mellgren, A.M.; 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.
46. Smith, C.L.; Baek, S.T.; Sung, C.Y.; Tallquist, M.D. Epicardial-derived cell epithelial-tomesenchymal transition and fate specification require PDGF receptor signaling. Circ. Res. 2011, 108, e15-e26.
47. Acharya, A.; Baek, S.T.; Huang, G.; Eskiocak, B.; Goetsch, S.; Sung, C.Y.; Banfi, S.; Sauer, M.F.; Olsen, G.S.; Duffield, J.S.; Olson, E.N.; Tallquist, M.D. The bHLH transcription factor Tcf21 is required for lineage-specific EMT of cardiac fibroblast progenitors. Development 2012, 139, 2139-2149.
48. van Wijk, B.; Gunst, Q.D.; Moorman, A.F.; van den Hoff, M.J. Cardiac regeneration from activated epicardium. PLoS One 2012, 7, e44692.
49. Huang, G.N.; Thatcher, J.E.; McAnally, J.; Kong, Y.; Qi, X.; Tan, W.; DiMaio, J.M.; Amatruda, J.F.; Gerard, R.D.; Hill, J.A.; Bassel-Duby, R.; Olson, E.N. C/EBP transcription factors mediate epicardial activation during heart development and injury. Science 2012, 338, 1599-1603.
50. Manner, J. Experimental study on the formation of the epicardium in chick embryos. Anat. Embryol. (Berl.) 1993, 187, 281-289.
51. Manner, J.; Schlueter, J.; Brand, T. Experimental analyses of the function of the proepicardium using a new microsurgical procedure to induce loss-of-proepicardial-function in chick embryos. Dev. Dyn. 2005, 233, 1454-1463.
52. Pennisi, D.J.; Ballard, V.L.; Mikawa, T. Epicardium is required for the full rate of myocyte proliferation and levels of expression of myocyte mitogenic factors FGF2 and its receptor, FGFR-1, but not for transmural myocardial patterning in the embryonic chick heart. Dev. Dyn. 2003, 228, 161-172.
53. Niederreither, K.; Subbarayan, V.; Dolle, P.; Chambon, P. Embryonic retinoic acid synthesis is essential for early mouse post-implantation development. Nat. Genet. 1999, 21, 444-448.
54. Merki, E.; Zamora, M.; Raya, A.; Kawakami, Y.; Wang, J.; Zhang, X.; Burch, J.; Kubalak, S.W.; Kaliman, P.; Izpisua 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.
55. Stuckmann, I.; Evans, S.; Lassar, A.B. Erythropoietin and retinoic acid, secreted from the epicardium, are required for cardiac myocyte proliferation. Dev. Biol 2003, 255, 334-349.
56. Chen, J.; Kubalak, S.W.; Chien, K.R. Ventricular muscle-restricted targeting of the RXRalpha gene reveals a non-cell-autonomous requirement in cardiac chamber morphogenesis. Development 1998, 125, 1943-1949.
57. Brade, T.; Kumar, S.; Cunningham, T.J.; Chatzi, C.; Zhao, X.; Cavallero, S.; Li, P.; Sucov, H.M.; Ruiz-Lozano, P.; Duester, G. Retinoic acid stimulates myocardial expansion by induction of hepatic erythropoietin which activates epicardial Igf2. Development 2011, 138, 139-148.
58. Li, P.; Cavallero, S.; Gu, Y.; Chen, T.H.; Hughes, J.; Hassan, A.B.; Brüning, J.C.; Pashmforoush, M.; Sucov, H.M. IGF signaling directs ventricular cardiomyocyte proliferation during embryonic heart development. Development 2011, 138, 1795-1805.
59. Duan, J.; Gherghe, C.; Liu, D.; Hamlett, E.; Srikantha, L.; Rodgers, L.; Regan, J.N.; Rojas, M.; Willis, M.; Leask, A.; Majesky, M.; Deb, A. Wnt1/betacatenin injury response activates the epicardium and cardiac fibroblasts to promote cardiac repair. EMBO J. 2012, 31, 429-442.
60. 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.
61. Chen, T.; 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 acidinducible trophic factor. Dev. Biol. 2002, 250, 198-207.
62. Morabito, C.J.; Dettman, R.W.; Kattan, J.; Collier, J.M.; Bristow, J. Positive and negative regulation of epicardial-mesenchymal transformation during avian heart development. Dev. Biol. 2001, 234, 204-215.
63. Vega-Hernandez, M.; Kovacs, A.; De Langhe, S.; Ornitz, D.M. FGF10/FGFR2b signaling is essential for cardiac fibroblast development and growth of the myocardium. Development 2011, 138, 3331-3340.
64. Bock-Marquette, I.; Saxena, A.; White, M.D.; Dimaio, J.M.; Srivastava, D. Thymosin beta4 activates integrin-linked kinase and promotes cardiac cell migration, survival and cardiac repair. Nature 2004, 432, 466-472.
65. 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.
66. 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. Mol. Cell. Cardiol. 2009, 46, 728- 738.
67. Banerjee, I.; Zhang, J.; Moore-Morris, T.; Lange, S.; Shen, T.; Dalton, N.D.; Gu, Y.; Peterson, K.L.; Evans, S.M.; Chen, J. Thymosin beta 4 is dispensable for murine cardiac development and function. Circ. Res. 2012, 110, 456-464.
68. Banerjee, I.; Morris, T.M.; Evans, S.M.; Chen, J. Thymosin beta4 is not required for embryonic viability or vascular development. Circ. Res. 2013, 112, e25-e28.
69. Becker, R.O.; Chapin, S.; Sherry, R. Regeneration of the ventricular myocardium in amphibians. Nature 1974, 248, 145-147.
70. Neff, A.W.; Dent, A.E.; Armstrong, J.B. Heart development and regeneration in urodeles. Int. J. Dev. Biol. 1996, 40, 719-725.
71. Poss, K.D.; Wilson, L.G.; Keating, M.T. Heart regeneration in zebrafish. Science 2002, 298, 2188-2190.
72. Flink, I.L. Cell cycle reentry of ventricular and atrial cardiomyocytes and cells within the epicardium following amputation of the ventricular apex in the axolotl, Amblystoma mexicanum: Confocal microscopic immunofluorescent image analysis of bromodeoxyuridine-labeled nuclei. Anat. Embryol. (Berl.) 2002, 205, 235-244.
73. 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.
74. 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.
75. Jopling, C.; Sleep, E.; Raya, M.; Martí, M.; Raya, A.; Izpisúa Belmonte, J.C. Zebrafish heart regeneration occurs by cardiomyocyte dedifferentiation and proliferation. Nature 2010, 464, 606-609.
76. 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.
77. Chablais, F.; Veit, J.; Rainer, G.; Jazwinska, A. The zebrafish heart regenerates after cryoinjuryinduced myocardial infarction. BMC Dev. Biol. 2011, 11, 21.
78. 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.
79. Schnabel, K.; Wu, C.C.; Kurth, T.; Weidinger, G. Regeneration of cryoinjury induced necrotic heart lesions in zebrafish is associated with epicardial activation and cardiomyocyte proliferation. PLoS One 2011, 6, e18503.
80. Wang, J.; Panáková, D.; Kikuchi, K.; Holdway, J.E.; Gemberling, M.; Burris, J.S.; Singh, S.P.; Dickson, A.L.; Lin, Y.F.; Sabeh, M.K.; Werdich, A.A.; Yelon, D.; Macrae, C.A.; Poss, K.D. The regenerative capacity of zebrafish reverses cardiac failure caused by genetic cardiomyocyte depletion. Development 2011, 138, 3421-3430.
81. 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.
82. Bergmann, O.; Bhardwaj, R.D.; Bernard, S.; Zdunek, S.; Barnabé-Heider, F.; Walsh, S.; Zupicich, J.; Alkass, K.; Buchholz, B.A.; Druid, H.; Jovinge, S.; Frisén, J. Evidence for cardiomyocyte renewal in humans. Science 2009, 324, 98-102.
83. Senyo, S.E.; Steinhauser, M.L.; Pizzimenti, C.L.; Yang, V.K.; Cai, L.; Wang, M.; Wu, T.D.; Guerquin-Kern, J.L.; Lechene, C.P.; Lee, R.T. Mammalian heart renewal by pre-existing cardiomyocytes. Nature 2013, 493, 433-436.
84. Mummery, C.L.; Lee, R.T. Is heart regeneration on the right track-Nat. Med. 2013, 19, 412-413.
85. Hsieh, P.C.; Segers, V.F.; Davis, M.E.; MacGillivray, C.; Gannon, J.; Molkentin, J.D.; Robbins, J.; Lee, R.T. Evidence from a genetic fate-mapping study that stem cells refresh adult mammalian cardiomyocytes after injury. Nat. Med. 2007, 13, 970-974.
86. 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.
87. Smart, N.; Bollini, S.; Dubé, 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.
88. Zhou, B.; Honor, L.B.; Ma, Q.; Oh, J.H.; Lin, R.Z.; Melero-Martin, J.M.; von Gise, A.; Zhou, P.; Hu, T.; He, L.; Wu, K.H.; Zhang, H.; Zhang, Y.; Pu, W.T. Thymosin beta 4 treatment after myocardial infarction does not reprogram epicardial cells into cardiomyocytes. J. Mol. Cell. Cardiol. 2012, 52, 43-47.
89. Kispert, A. No muscle for a damaged heart: thymosin beta 4 treatment after myocardial infarction does not induce myocardial differentiation of epicardial cells. J. Mol. Cell. Cardiol. 2012, 52, 10-12.
90. Chong, J.J.; Chandrakanthan, V.; Xaymardan, M.; Asli, N.S.; Li, J.; Ahmed, I.; Heffernan, C.; Menon, M.K.; Scarlett, C.J.; Rashidianfar, A.; Biben, C.; Zoellner, H.; Colvin, E.K.; Pimanda, J.E.; Biankin, A.V.; Zhou, B.; Pu, W.T.; Prall, O.W.; Harvey, R.P. Adult cardiac-resident MSClike stem cells with a proepicardial origin. Cell Stem Cell 2011, 9, 527-540.
91. Singh, M.K.; Epstein, J.A. Epicardium-derived cardiac mesenchymal stem cells: expanding the outer limit of heart repair. Circ. Res. 2012, 110, 904-906.
92. Fujita, M.; Ikemoto, M.; Kishishita, M.; Otani, H.; Nohara, R.; Tanaka, T.; Tamaki, S.; Yamazato, A.; Sasayama, S. Elevated basic fibroblast growth factor in pericardial fluid of patients with unstable angina. Circulation 1996, 94, 610-613.
93. 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.
94. 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.
95. Kubota, T.; Namiki, A.; Fukazawa, M.; Ishikawa, M.; Moroi, M.; Ebine, K.; Yamaguchi, T. Concentrations of hepatocyte growth factor, basic fibroblast growth factor, and vascular endothelial growth factor in pericardial fluid and plasma. Jpn. Heart J. 2004, 45, 989-998.
96. Limana, F.; Bertolami, C.; Mangoni, A.; Di Carlo, A.; Avitabile, D.; Mocini, D.; Iannelli, P.; De Mori, R.; Marchetti, C.; Pozzoli, O.; Gentili, C.; Zacheo, A.; Germani, A.; Capogrossi, M.C. Myocardial infarction induces embryonic reprogramming of epicardial c-kit(+) cells: role of the pericardial fluid. J. Mol. Cell. Cardiol. 2010, 48, 609-618.
97. Ikemoto, M.; Hasegawa, K.; Kihara, Y.; Iwakura, A.; Komeda, M.; Yamazato, A.; Fujita, M. Development of enzyme-linked immunosorbent assay for acidic fibroblast growth factor and its clinical application. Clin. Chim. Acta. 1999, 283, 171-182.
98. Abe, N.; Matsunaga, T.; Kameda, K.; Tomita, H.; Fujiwara, T.; Ishizaka, H.; Hanada, H.; Fukui, K.; Fukuda, I.; Osanai, T.; Okumura, K. Increased level of pericardial insulin-like growth factor- 1 in patients with left ventricular dysfunction and advanced heart failure. J. Am. Coll. Cardiol. 2006, 48, 1387-1395.
99. Matsunaga, T.; Chilian, W.M.; March, K. Angiostatin is negatively associated with coronary collateral growth in patients with coronary artery disease. Am. J. Physiol. Heart Circ. Physiol. 2005, 288, H2042-H2046.
100. Namiki, A.; Kubota, T.; Fukazawa, M.; Ishikawa, M.; Moroi, M.; Aikawa, J.; Ebine, K.; Yamaguchi, T. Endothelin-1 concentrations in pericardial fluid are more elevated in patients with ischemic heart disease than in patients with nonischemic heart disease. Jpn. Heart J. 2003, 44, 633-644.
101. Oyama, J.; Shimokawa, H.; Morita, S.; Yasui, H.; Takeshita, A. Elevated interleukin-1beta in pericardial fluid of patients with ischemic heart disease. Coron. Artery Dis. 2001, 12, 567-571.
102. Ege, T.; Canbaz, S.; Yuksel, V.; Duran, E. Effect of pericardial fluid pro-inflammatory cytokines on hemodynamic parameters. Cytokine 2003, 23, 47-51.
103. Urbanek, K.; Rota, M.; Cascapera, S.; Bearzi, C.; Nascimbene, A.; De Angelis, A.; Hosoda, T.; Chimenti, S.; Baker, M.; Limana, F.; Nurzynska, D.; Torella, D.; Rotatori, F.; Rastaldo, R.; Musso, E.; Quaini, F.; Leri, A.; Kajstura, J.; Anversa, P. Cardiac stem cells possess growth factor-receptor systems that after activation regenerate the infarcted myocardium, improving ventricular function and long-term survival. Circ. Res. 2005, 97, 663-673.
104. Limana, F.; Germani, A.; Zacheo, A.; Kajstura, J.; Di Carlo, A.; Borsellino, G.; Leoni, O.; Palumbo, R.; Battistini, L.; Rastaldo, R.; Müller, S.; Pompilio, G.; Anversa, P.; Bianchi, M.E.; Capogrossi, M.C. Exogenous high-mobility group box 1 protein induces myocardial regeneration after infarction via enhanced cardiac C-kit+ cell proliferation and differentiation. Circ. Res. 2005, 97, e73-e83.
105. Linke, A.; Müller, P.; Nurzynska, D.; Casarsa, C.; Torella, D.; Nascimbene, A.; Castaldo, C.; Cascapera, S.; Böhm, M.; Quaini, F.; Urbanek, K.; Leri, A.; Hintze, T.H.; Kajstura, J.; Anversa, P. Stem cells in the dog heart are self-renewing, clonogenic, and multipotent and regenerate infarcted myocardium, improving cardiac function. Proc. Natl. Acad. Sci. USA 2005, 102, 8966-8971.