Lives of a Heart Cell: Tracing the Origins of Cardiac Progenitors

Cell Stem Cell

Volumn 2, Issue 4, 2008, Pages 320-331

  Martin Puig, Silvia ^a   Wang, Zhong ^a   Chien, Kenneth R ^a,b,c  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c HARVARD STEM CELL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT STEM CELL; CELL ASSAY; CELL CLONING; CELL DIFFERENTIATION; CELL FATE; CELL FUNCTION; CELL ISOLATION; CELL LINEAGE; CELL MATURATION; CELL POPULATION; CELL PROLIFERATION; CELL RENEWAL; CELL STIMULATION; CELL SURVIVAL; CELL TYPE; CORONARY ARTERY BLOOD FLOW; CYTOLOGY; EMBRYONIC STEM CELL; ENDOTHELIUM CELL; EPICARDIUM; HEART CONTRACTION; HEART DEVELOPMENT; HEART DISEASE; HEART ELECTROPHYSIOLOGY; HEART FAILURE; HEART INFARCTION; HEART MUSCLE CELL; HEART MUSCLE CONDUCTION SYSTEM; HEMATOPOIETIC STEM CELL; HUMAN; MESENCHYMAL STEM CELL; MULTIPOTENT STEM CELL; MUSCLE CELL; NEURAL CREST CELL; NONHUMAN; PRIORITY JOURNAL; REVIEW; SKELETAL MUSCLE; STEM CELL; STEM CELL TRANSPLANTATION; TISSUE REGENERATION;

CARDIOVASCULAR DISEASES; HUMANS; MYOCARDIUM; REGENERATIVE MEDICINE; STEM CELLS;

EID: 41449094683     PISSN: 19345909     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.stem.2008.03.010     Document Type: Review

References (96)

1. Abu-Issa R., Waldo K., and Kirby M.L. Heart fields: one, two or more?. Dev. Biol. 272 (2004) 281-285
2. Ai D., Fu X., Wang J., Lu M.F., Chen L., Baldini A., Klein W.H., and Martin J.F. Canonical Wnt signaling functions in second heart field to promote right ventricular growth. Proc. Natl. Acad. Sci. USA 104 (2007) 9319-9324
3. Alvarez-Dolado M., Pardal R., Garcia-Verdugo J.M., Fike J.R., Lee H.O., Pfeffer K., Lois C., Morrison S.J., and Alvarez-Buylla A. Fusion of bone-marrow-derived cells with Purkinje neurons, cardiomyocytes and hepatocytes. Nature 425 (2003) 968-973
4. Baba S., Heike T., Umeda K., Iwasa T., Kaichi S., Hiraumi Y., Doi H., Yoshimoto M., Kanatsu-Shinohara M., Shinohara T., and Nakahata T. Generation of cardiac and endothelial cells from neonatal mouse testis-derived multipotent germline stem cells. Stem Cells 25 (2007) 1375-1383
5. Balsam L.B., Wagers A.J., Christensen J.L., Kofidis T., Weissman I.L., and Robbins R.C. Haematopoietic stem cells adopt mature haematopoietic fates in ischaemic myocardium. Nature 428 (2004) 668-673
6. Beltrami A.P., Barlucchi L., Torella D., Baker M., Limana F., Chimenti S., Kasahara H., Rota M., Musso E., Urbanek K., et al. Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell 114 (2003) 763-776
7. Bhattacharya S., Macdonald S.T., and Farthing C.R. Molecular mechanisms controlling the coupled development of myocardium and coronary vasculature. Clin. Sci. (Lond.) 111 (2006) 35-46
8. Buckingham M., Meilhac S., and Zaffran S. Building the mammalian heart from two sources of myocardial cells. Nat. Rev. Genet. 6 (2005) 826-835
9. Cai C.L., Liang X., Shi Y., Chu P.H., Pfaff S.L., Chen J., and Evans S. Isl1 identifies a cardiac progenitor population that proliferates prior to differentiation and contributes a majority of cells to the heart. Dev. Cell 5 (2003) 877-889
10. Chen H., Shi S., Acosta L., Li W., Lu J., Bao S., Chen Z., Yang Z., Schneider M.D., Chien K.R., et al. BMP10 is essential for maintaining cardiac growth during murine cardiogenesis. Development 131 (2004) 2219-2231
11. Chen H., Yong W., Ren S., Shen W., He Y., Cox K.A., Zhu W., Li W., Soonpaa M., Payne R.M., et al. Overexpression of bone morphogenetic protein 10 in myocardium disrupts cardiac postnatal hypertrophic growth. J. Biol. Chem. 281 (2006) 27481-27491
12. Chiavegato A., Bollini S., Pozzobon M., Callegari A., Gasparotto L., Taiani J., Piccoli M., Lenzini E., Gerosa G., Vendramin I., et al. Human amniotic fluid-derived stem cells are rejected after transplantation in the myocardium of normal, ischemic, immuno-suppressed or immuno-deficient rat. J. Mol. Cell. Cardiol. 42 (2007) 746-759
13. Chien K.R. Stem cells: lost in translation. Nature 428 (2004) 607-608
14. Chien K.R. Lost and found: cardiac stem cell therapy revisited. J. Clin. Invest. 116 (2006) 1838-1840
15. Chien K.R. Making a play at regrowing hearts. Scientist 20 (2006) 34-39
16. Chien K.R., and Karsenty G. Longevity and lineages: toward the integrative biology of degenerative diseases in heart, muscle, and bone. Cell 120 (2005) 533-544
17. Christoffels V.M., Burch J.B., and Moorman A.F. Architectural plan for the heart: early patterning and delineation of the chambers and the nodes. Trends Cardiovasc. Med. 14 (2004) 301-307
18. Cohen E.D., Wang Z., Lepore J.J., Lu M.M., Taketo M.M., Epstein D.J., and Morrisey E.E. Wnt/beta-catenin signaling promotes expansion of Isl-1-positive cardiac progenitor cells through regulation of FGF signaling. J. Clin. Invest. 117 (2007) 1794-1804
19. De Coppi P., Bartsch Jr. G., Siddiqui M.M., Xu T., Santos C.C., Perin L., Mostoslavsky G., Serre A.C., Snyder E.Y., Yoo J.J., et al. Isolation of amniotic stem cell lines with potential for therapy. Nat. Biotechnol. 25 (2007) 100-106
20. Dodou E., Verzi M.P., Anderson J.P., Xu S.M., and Black B.L. Mef2c is a direct transcriptional target of ISL1 and GATA factors in the anterior heart field during mouse embryonic development. Development 131 (2004) 3931-3942
21. Dunwoodie S.L. Combinatorial signaling in the heart orchestrates cardiac induction, lineage specification and chamber formation. Semin. Cell Dev. Biol. 18 (2007) 54-66
22. Echelard Y., Vassileva G., and McMahon A.P. Cis-acting regulatory sequences governing Wnt-1 expression in the developing mouse CNS. Development 120 (1994) 2213-2224
23. Evans S.M., Mummery C., and Doevendans P.A. Progenitor cells for cardiac repair. Semin. Cell Dev. Biol. 18 (2007) 153-160
24. Fazel S., Cimini M., Chen L., Li S., Angoulvant D., Fedak P., Verma S., Weisel R.D., Keating A., and Li R.K. Cardioprotective c-kit+ cells are from the bone marrow and regulate the myocardial balance of angiogenic cytokines. J. Clin. Invest. 116 (2006) 1865-1877
25. Fazel S.S., Chen L., Angoulvant D., Li S.H., Weisel R.D., Keating A., and Li R.K. Activation of c-kit is necessary for mobilization of reparative bone marrow progenitor cells in response to cardiac injury. FASEB J. 22 (2007) 930-940
26. Franco D., Moreno N., and Ruiz-Lozano P. Non-resident stem cell populations in regenerative cardiac medicine. Cell. Mol. Life Sci. 64 (2007) 683-691
27. Gassmann M., Casagranda F., Orioli D., Simon H., Lai C., Klein R., and Lemke G. Aberrant neural and cardiac development in mice lacking the ErbB4 neuregulin receptor. Nature 378 (1995) 390-394
28. Gaustad K.G., Boquest A.C., Anderson B.E., Gerdes A.M., and Collas P. Differentiation of human adipose tissue stem cells using extracts of rat cardiomyocytes. Biochem. Biophys. Res. Commun. 314 (2004) 420-427
29. Gourdie R.G., Kubalak S.W., O'Brien T.X., Chien K.R., and Mikawa T. Development of cardiac pacemaking and conduction system lineages. In: Chien K.R. (Ed). Molecular Basis of Cardiovascular Disease: A Companion to Braunwald's Heart Disease. Second Edition (2004), Saunders, Philadelphia 225-237
30. Grego-Bessa J., Luna-Zurita L., del Monte G., Bolos V., Melgar P., Arandilla A., Garratt A.N., Zang H., Mukouyama Y.S., Chen H., et al. Notch signaling is essential for ventricular chamber development. Dev. Cell 12 (2007) 415-429
31. Grunewald M., Avraham I., Dor Y., Bachar-Lustig E., Itin A., Jung S., Chimenti S., Landsman L., Abramovitch R., and Keshet E. VEGF-induced adult neovascularization: recruitment, retention, and role of accessory cells. Cell 124 (2006) 175-189
32. Guan K., Nayernia K., Maier L.S., Wagner S., Dressel R., Lee J.H., Nolte J., Wolf F., Li M., Engel W., and Hasenfuss G. Pluripotency of spermatogonial stem cells from adult mouse testis. Nature 440 (2006) 1199-1203
33. Harvey R.P. Patterning the vertebrate heart. Nat. Rev. Genet. 3 (2002) 544-556
34. Hoogaars W.M., Barnett P., Moorman A.F., and Christoffels V.M. T-box factors determine cardiac design. Cell. Mol. Life Sci. 64 (2007) 646-660
35. Ishii Y., Langberg J.D., Hurtado R., Lee S., and Mikawa T. Induction of proepicardial marker gene expression by the liver bud. Development 134 (2007) 3627-3637
36. Jackson K.A., Majka S.M., Wang H., Pocius J., Hartley C.J., Majesky M.W., Entman M.L., Michael L.H., Hirschi K.K., and Goodell M.A. Regeneration of ischemic cardiac muscle and vascular endothelium by adult stem cells. J. Clin. Invest. 107 (2001) 1395-1402
37. Jiang X., Rowitch D.H., Soriano P., McMahon A.P., and Sucov H.M. Fate of the mammalian cardiac neural crest. Development 127 (2000) 1607-1616
38. Kattman S.J., Huber T.L., and Keller G.M. Multipotent flk-1+ cardiovascular progenitor cells give rise to the cardiomyocyte, endothelial, and vascular smooth muscle lineages. Dev. Cell 11 (2006) 723-732
39. Kruithof B.P., van Wijk B., Somi S., Kruithof-de Julio M., Perez Pomares J.M., Weesie F., Wessels A., Moorman A.F., and van den Hoff M.J. BMP and FGF regulate the differentiation of multipotential pericardial mesoderm into the myocardial or epicardial lineage. Dev. Biol. 295 (2006) 507-522
40. Kwon C., Arnold J., Hsiao E.C., Taketo M.M., Conklin B.R., and Srivastava D. Canonical Wnt signaling is a positive regulator of mammalian cardiac progenitors. Proc. Natl. Acad. Sci. USA 104 (2007) 10894-10899
41. Laugwitz K.L., Moretti A., Lam J., Gruber P., Chen Y., Woodard S., Lin L.Z., Cai C.L., Lu M.M., Reth M., et al. Postnatal isl1+ cardioblasts enter fully differentiated cardiomyocyte lineages. Nature 433 (2005) 647-653
42. Laugwitz K.L., Moretti A., Caron L., Nakano A., and Chien K.R. Islet1 cardiovascular progenitors: a single source for heart lineages?. Development 135 (2008) 193-205
43. Lee K.F., Simon H., Chen H., Bates B., Hung M.C., and Hauser C. Requirement for neuregulin receptor erbB2 in neural and cardiac development. Nature 378 (1995) 394-398
44. Lepilina A., Coon A.N., Kikuchi K., Holdway J.E., Roberts R.W., Burns C.G., and Poss K.D. A dynamic epicardial injury response supports progenitor cell activity during zebrafish heart regeneration. Cell 127 (2006) 607-619
45. Li J., Liu K.C., Jin F., Lu M.M., and Epstein J.A. Transgenic rescue of congenital heart disease and spina bifida in Splotch mice. Development 126 (1999) 2495-2503
46. Li J., Chen F., and Epstein J.A. Neural crest expression of Cre recombinase directed by the proximal Pax3 promoter in transgenic mice. Genesis 26 (2000) 162-164
47. 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., and Gittenberger-de Groot A.C. Origin, fate, and function of epicardium-derived cells (EPCDs) in normal and abnormal cardiac development. ScientificWorldJournal 7 (2007) 1777-1798
48. Lin L., Cui L., Zhou W., Dufort D., Zhang X., Cai C.L., Bu L., Yang L., Martin J., Kemler R., et al. Beta-catenin directly regulates Islet1 expression in cardiovascular progenitors and is required for multiple aspects of cardiogenesis. Proc. Natl. Acad. Sci. USA 104 (2007) 9313-9318
49. Majesky M.W. Developmental basis of vascular smooth muscle diversity. Arterioscler. Thromb. Vasc. Biol. 27 (2007) 1248-1258
50. Makino S., Fukuda K., Miyoshi S., Konishi F., Kodama H., Pan J., Sano M., Takahashi T., Hori S., Abe H., et al. Cardiomyocytes can be generated from marrow stromal cells in vitro. J. Clin. Invest. 103 (1999) 697-705
51. Martin C.M., Meeson A.P., Robertson S.M., Hawke T.J., Richardson J.A., Bates S., Goetsch S.C., Gallardo T.D., and Garry D.J. Persistent expression of the ATP-binding cassette transporter, Abcg2, identifies cardiac SP cells in the developing and adult heart. Dev. Biol. 265 (2004) 262-275
52. Massberg S., Schaerli P., Knezevic-Maramica I., Kollnberger M., Tubo N., Moseman E.A., Huff I.V., Junt T., Wagers A.J., Mazo I.B., and von Andrian U.H. Immunosurveillance by hematopoietic progenitor cells trafficking through blood, lymph, and peripheral tissues. Cell 131 (2007) 994-1008
53. Menasche P. Skeletal muscle satellite cell transplantation. Cardiovasc. Res. 58 (2003) 351-357
54. Merki E., Zamora M., Raya A., Kawakami Y., Wang J., Zhang X., Burch J., Kubalak S.W., Kaliman P., Izpisua Belmonte J.C., et al. Epicardial retinoid X receptor {alpha} is required for myocardial growth and coronary artery formation. Proc. Natl. Acad. Sci. USA 102 (2005) 18455-18460
55. Messina E., De Angelis L., Frati G., Morrone S., Chimenti S., Fiordaliso F., Salio M., Battaglia M., Latronico M.V., Coletta M., et al. Isolation and expansion of adult cardiac stem cells from human and murine heart. Circ. Res. 95 (2004) 911-921
56. Meyer D., and Birchmeier C. Multiple essential functions of neuregulin in development. Nature 378 (1995) 386-390
57. Meyer G.P., Wollert K.C., Lotz J., Steffens J., Lippolt P., Fichtner S., Hecker H., Schaefer A., Arseniev L., Hertenstein B., et al. Intracoronary bone marrow cell transfer after myocardial infarction: eighteen months' follow-up data from the randomized, controlled BOOST (BOne marrOw transfer to enhance ST-elevation infarct regeneration) trial. Circulation 113 (2006) 1287-1294
58. Moorman A.F., and Christoffels V.M. Cardiac chamber formation: development, genes, and evolution. Physiol. Rev. 83 (2003) 1223-1267
59. Moretti A., Caron L., Nakano A., Lam J.T., Bernshausen A., Chen Y., Qyang Y., Bu L., Sasaki M., Martin-Puig S., et al. Multipotent embryonic isl1+ progenitor cells lead to cardiac, smooth muscle, and endothelial cell diversification. Cell 127 (2006) 1151-1165
60. Mu H., Ohashi R., Lin P., Yao Q., and Chen C. Cellular and molecular mechanisms of coronary vessel development. Vasc. Med. 10 (2005) 37-44
61. Mummery C. Cardiomyocytes from human embryonic stem cells: more than heart repair alone. Bioessays 29 (2007) 572-579
62. Murry C.E., Soonpaa M.H., Reinecke H., Nakajima H., Nakajima H.O., Rubart M., Pasumarthi K.B., Virag J.I., Bartelmez S.H., Poppa V., et al. Haematopoietic stem cells do not transdifferentiate into cardiac myocytes in myocardial infarcts. Nature 428 (2004) 664-668
63. Murry C.E., Field L.J., and Menasche P. Cell-based cardiac repair: reflections at the 10-year point. Circulation 112 (2005) 3174-3183
64. Nygren J.M., Jovinge S., Breitbach M., Sawen P., Roll W., Hescheler J., Taneera J., Fleischmann B.K., and Jacobsen S.E. Bone marrow-derived hematopoietic cells generate cardiomyocytes at a low frequency through cell fusion, but not transdifferentiation. Nat. Med. 10 (2004) 494-501
65. Oh H., Bradfute S.B., Gallardo T.D., Nakamura T., Gaussin V., Mishina Y., Pocius J., Michael L.H., Behringer R.R., Garry D.J., et al. Cardiac progenitor cells from adult myocardium: homing, differentiation, and fusion after infarction. Proc. Natl. Acad. Sci. USA 100 (2003) 12313-12318
66. Okamoto K., Miyoshi S., Toyoda M., Hida N., Ikegami Y., Makino H., Nishiyama N., Tsuji H., Cui C.H., Segawa K., et al. 'Working' cardiomyocytes exhibiting plateau action potentials from human placenta-derived extraembryonic mesodermal cells. Exp. Cell Res. 313 (2007) 2550-2562
67. Orlic D., Kajstura J., Chimenti S., Jakoniuk I., Anderson S.M., Li B., Pickel J., McKay R., Nadal-Ginard B., Bodine D.M., et al. Bone marrow cells regenerate infarcted myocardium. Nature 410 (2001) 701-705
68. Parmacek M.S., and Epstein J.A. Pursuing cardiac progenitors: regeneration redux. Cell 120 (2005) 295-298
69. Pashmforoush M., Lu J.T., Chen H., Amand T.S., Kondo R., Pradervand S., Evans S.M., Clark B., Feramisco J.R., Giles W., et al. Nkx2-5 pathways and congenital heart disease; loss of ventricular myocyte lineage specification leads to progressive cardiomyopathy and complete heart block. Cell 117 (2004) 373-386
70. Planat-Benard V., Menard C., Andre M., Puceat M., Perez A., Garcia-Verdugo J.M., Penicaud L., and Casteilla L. Spontaneous cardiomyocyte differentiation from adipose tissue stroma cells. Circ. Res. 94 (2004) 223-229
71. Pouly J., Bruneval P., Mandet C., Proksch S., Peyrard S., Amrein C., Bousseaux V., Guillemain R., Deloche A., Fabiani J., and Menasché P. Cardiac stem cells in the real world. J. Thorac. Cardiovasc. Surg. 135 (2008) 673-678
72. Prall O.W., Menon M.K., Solloway M.J., Watanabe Y., Zaffran S., Bajolle F., Biben C., McBride J.J., Robertson B.R., Chaulet H., et al. An Nkx2-5/Bmp2/Smad1 negative feedback loop controls heart progenitor specification and proliferation. Cell 128 (2007) 947-959
73. Qyang Y., Martin-Puig S., Chiravuri M., Chen S., Xu H., Bu L., Jiang X., Lin L., Granger A., Moretti A., et al. The renewal and differentiation of Isl1+ cardiovascular progenitors are controlled by a Wnt/β-catenin pathway. Cell Stem Cell 1 (2007) 165-179
74. Rangappa S., Fen C., Lee E.H., Bongso A., and Sim E.K. Transformation of adult mesenchymal stem cells isolated from the fatty tissue into cardiomyocytes. Ann. Thorac. Surg. 75 (2003) 775-779
75. Reese D.E., Mikawa T., and Bader D.M. Development of the coronary vessel system. Circ. Res. 91 (2002) 761-768
76. Reinecke H., MacDonald G.H., Hauschka S.D., and Murry C.E. Electromechanical coupling between skeletal and cardiac muscle. Implications for infarct repair. J. Cell Biol. 149 (2000) 731-740
77. Rosenzweig A. Cardiac cell therapy-mixed results from mixed cells. N. Engl. J. Med. 355 (2006) 1274-1277
78. Rota M., Kajstura J., Hosoda T., Bearzi C., Vitale S., Esposito G., Iaffaldano G., Padin-Iruegas M.E., Gonzalez A., Rizzi R., et al. Bone marrow cells adopt the cardiomyogenic fate in vivo. Proc. Natl. Acad. Sci. USA 104 (2007) 17783-17788
79. Sedmera D., Pexieder T., Vuillemin M., Thompson R.P., and Anderson R.H. Developmental patterning of the myocardium. Anat. Rec. 258 (2000) 319-337
80. Smart N., Risebro C.A., Melville A.A., Moses K., Schwartz R.J., Chien K.R., and Riley P.R. Thymosin beta4 induces adult epicardial progenitor mobilization and neovascularization. Nature 445 (2007) 177-182
81. Smith R.R., Barile L., Cho H.C., Leppo M.K., Hare J.M., Messina E., Giacomello A., Abraham M.R., and Marban E. Regenerative potential of cardiosphere-derived cells expanded from percutaneous endomyocardial biopsy specimens. Circulation 115 (2007) 896-908
82. Snider P., Olaopa M., Firulli A.B., and Conway S.J. Cardiovascular development and the colonizing cardiac neural crest lineage. ScientificWorldJournal 7 (2007) 1090-1113
83. Sun Y., Liang X., Najafi N., Cass M., Lin L., Cai C.L., Chen J., and Evans S.M. Islet 1 is expressed in distinct cardiovascular lineages, including pacemaker and coronary vascular cells. Dev. Biol. 304 (2007) 286-296
84. Tillmanns J., Rota M., Hosoda T., Misao Y., Esposito G., Gonzalez A., Vitale S., Parolin C., Yasuzawa-Amano S., Muraski J., et al. Formation of large coronary arteries by cardiac progenitor cells. Proc. Natl. Acad. Sci. USA 105 (2008) 1668-1673
85. Toma C., Pittenger M.F., Cahill K.S., Byrne B.J., and Kessler P.D. Human mesenchymal stem cells differentiate to a cardiomyocyte phenotype in the adult murine heart. Circulation 105 (2002) 93-98
86. Tzahor E. Wnt/beta-catenin signaling and cardiogenesis: timing does matter. Dev. Cell 13 (2007) 10-13
87. Ueno S., Weidinger G., Osugi T., Kohn A.D., Golob J.L., Pabon L., Reinecke H., Moon R.T., and Murry C.E. Biphasic role for Wnt/beta-catenin signaling in cardiac specification in zebrafish and embryonic stem cells. Proc. Natl. Acad. Sci. USA 104 (2007) 9685-9690
88. van Tuyn 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 Laarse A., et al. Epicardial cells of human adults can undergo an epithelial-to-mesenchymal transition and obtain characteristics of smooth muscle cells in vitro. Stem Cells 25 (2007) 271-278
89. Ventura C., Cantoni S., Bianchi F., Lionetti V., Cavallini C., Scarlata I., Foroni L., Maioli M., Bonsi L., Alviano F., et al. Hyaluronan mixed esters of butyric and retinoic acid drive cardiac and endothelial fate in term placenta human mesenchymal stem cells and enhance cardiac repair in infarcted rat hearts. J. Biol. Chem. 282 (2007) 14243-14252
90. Wada A.M., Smith T.K., Osler M.E., Reese D.E., and Bader D.M. Epicardial/mesothelial cell line retains vasculogenic potential of embryonic epicardium. Circ. Res. 92 (2003) 525-531
91. Wagner M., and Siddiqui M.A. Signal transduction in early heart development (II): ventricular chamber specification, trabeculation, and heart valve formation. Exp. Biol. Med. (Maywood) 232 (2007) 866-880
92. Wessels A., and Sedmera D. Developmental anatomy of the heart: a tale of mice and man. Physiol. Genomics 15 (2003) 165-176
93. Winitsky S.O., Gopal T.V., Hassanzadeh S., Takahashi H., Gryder D., Rogawski M.A., Takeda K., Yu Z.X., Xu Y.H., and Epstein N.D. Adult murine skeletal muscle contains cells that can differentiate into beating cardiomyocytes in vitro. PLoS Biol. 3 (2005) e87 10.1371/journal.pbio.0030087
94. Winter E.M., and Gittenberger-de Groot A.C. Epicardium-derived cells in cardiogenesis and cardiac regeneration. Cell. Mol. Life Sci. 64 (2007) 692-703
95. Wu S.M., Fujiwara Y., Cibulsky S.M., Clapham D.E., Lien C.L., Schultheiss T.M., and Orkin S.H. Developmental origin of a bipotential myocardial and smooth muscle cell precursor in the mammalian heart. Cell 127 (2006) 1137-1150
96. Wu S.M., Chien K.R., and Mummery C. Origins and fates of cardiovascular progenitor cells. Cell 132 (2008) 537-543