Molecular mechanisms of cardiomyocyte regeneration and therapeutic outlook

Trends in Molecular Medicine

Volumn 13, Issue 3, 2007, Pages 125-133

  Germani, Antonia ^a,b   Di Rocco, Giuliana ^a   Limana, Federica ^a   Martelli, Fabio ^c   Capogrossi, Maurizio C ^c  

^a CENTRO CARDIOLOGICO MONZINO   (Italy)

^b Laboratori di Ricerca Gruppo Bios   (Italy)

^c LABORATORIO DI PATOLOGIA VASCOLARE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ATAXIN 1; BREAST CANCER RESISTANCE PROTEIN; CD133 ANTIGEN; CD31 ANTIGEN; CD34 ANTIGEN; CYCLIN A; CYCLIN B; CYCLIN D1; CYCLIN D2; CYCLIN D3; CYCLIN DEPENDENT KINASE INHIBITOR 1; CYCLIN DEPENDENT KINASE INHIBITOR 1B; FIBROBLAST GROWTH FACTOR 2; HIGH MOBILITY GROUP B1 PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; MULTIDRUG RESISTANCE PROTEIN 1; NESTIN; NOTCH1 RECEPTOR; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN MDM2; PROTEIN P53; RETINOBLASTOMA PROTEIN; STEM CELL FACTOR; TRANSCRIPTION FACTOR GATA 4; TRANSCRIPTION FACTOR NKX2.5; TRANSFORMING GROWTH FACTOR BETA; UNINDEXED DRUG; VASCULOTROPIN RECEPTOR 2;

CELL CYCLE REGULATION; CELL DIFFERENTIATION; CELL PROLIFERATION; EMBRYONIC STEM CELL; HEART FAILURE; HEART FUNCTION; HEART INJURY; HEART MUSCLE CELL; HUMAN; MAMMAL; MESENCHYMAL STEM CELL; NONHUMAN; REGENERATION; REVIEW; STEM CELL TRANSPLANTATION; SYSTEMATIC REVIEW; VERTEBRATE;

ANIMALS; HEART FAILURE, CONGESTIVE; HEART INJURIES; HUMANS; MYOCYTES, CARDIAC; REGENERATION; STEM CELL TRANSPLANTATION; STEM CELLS;

MAMMALIA; VERTEBRATA;

EID: 33847409770     PISSN: 14714914     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molmed.2007.01.002     Document Type: Review

References (92)

1. Oberpriller J.O., et al. Stimulation of proliferative events in the adult amphibian cardiac myocyte. Ann. N. Y. Acad. Sci. 752 (1995) 30-46
2. 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.) 205 (2002) 235-244
3. Poss K.D., et al. Heart regeneration in zebrafish. Science 298 (2002) 2188-2190
4. Lepilina A., et al. A dynamic epicardial injury response supports progenitor cell activity during zebrafish heart regeneration. Cell 127 (2006) 607-619
5. Lien C.L., et al. Gene expression analysis of zebrafish heart regeneration. PLoS Biol. 4 (2006) e260
6. Ober E.A., et al. Vegfc is required for vascular development and endoderm morphogenesis in zebrafish. EMBO Rep. 5 (2004) 78-84
7. Bock-Marquette I., et al. Thymosin β4 activates integrin-linked kinase and promotes cardiac cell migration, survival and cardiac repair. Nature 432 (2004) 466-472
8. Smart N., et al. Thymosin β4 induces adult epicardial progenitor mobilization and neovascularization. Nature 445 (2006) 177-182
9. Vinarsky V., et al. Normal newt limb regeneration requires matrix metalloproteinase function. Dev. Biol. 279 (2005) 86-98
10. Raya A., et al. Activation of Notch signaling pathway precedes heart regeneration in zebrafish. Proc. Natl. Acad. Sci. U. S. A. 100 Suppl 1 (2003) 11889-11895
11. Beltrami A.P., et al. Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell 114 (2003) 763-776
12. Linke A., et al. Stem cells in the dog heart are self-renewing, clonogenic, and multipotent and regenerate infarcted myocardium, improving cardiac function. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 8966-8971
13. Urbanek K., et al. Myocardial regeneration by activation of multipotent cardiac stem cells in ischemic heart failure. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 8692-8697
14. Urbanek K., et al. Intense myocyte formation from cardiac stem cells in human cardiac hypertrophy. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 10440-10445
15. Hierlihy A.M., et al. The post-natal heart contains a myocardial stem cell population. FEBS Lett. 530 (2002) 239-243
16. Oh H., et al. Cardiac progenitor cells from adult myocardium: homing, differentiation, and fusion after infarction. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 12313-12318
17. Urbanek K., et al. Cardiac stem cells possess growth factor-receptor systems that after activation regenerate the infarcted myocardium, improving ventricular function and long-term survival. Circ. Res. 97 (2005) 663-673
18. Martin C.M., et al. 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
19. Messina E., et al. Isolation and expansion of adult cardiac stem cells from human and murine heart. Circ. Res. 95 (2004) 911-921
20. + cardiac side population cells exhibit functional cardiomyogenic differentiation. Circ. Res. 97 (2005) 52-61
21. + cardioblasts enter fully differentiated cardiomyocyte lineages. Nature 433 (2005) 647-653
22. Tomita Y., et al. Cardiac neural crest cells contribute to the dormant multipotent stem cell in the mammalian heart. J. Cell Biol. 170 (2005) 1135-1146
23. + progenitor cells lead to cardiac, smooth muscle, and endothelial cell Diversification. Cell 127 (2006) 1151-1165
24. + cell proliferation and differentiation. Circ. Res. 97 (2005) e73-e83
25. Chimenti C., et al. Senescence and death of primitive cells and myocytes lead to premature cardiac aging and heart failure. Circ. Res. 93 (2003) 604-613
26. Torella D., et al. Cardiac stem cell and myocyte aging, heart failure, and insulin-like growth factor-1 overexpression. Circ. Res. 94 (2004) 514-524
27. Rota M., et al. Diabetes promotes cardiac stem cell aging and heart failure, which are prevented by deletion of the p66shc gene. Circ. Res. 99 (2006) 42-52
28. Urbanek K., et al. Stem cell niches in the adult mouse heart. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 9226-9231
29. Rosenblatt-Velin N., et al. FGF-2 controls the differentiation of resident cardiac precursors into functional cardiomyocytes. J. Clin. Invest. 115 (2005) 1724-1733
30. Suzuki G., et al. Adenoviral gene transfer of FGF-5 to hibernating myocardium improves function and stimulates myocytes to hypertrophy and reenter the cell cycle. Circ. Res. 96 (2005) 767-775
31. Ferrarini M., et al. Adeno-associated virus-mediated transduction of VEGF165 improves cardiac tissue viability and functional recovery after permanent coronary occlusion in conscious dogs. Circ. Res. 98 (2006) 954-961
32. Vera Janavel G., et al. Plasmid-mediated VEGF gene transfer induces cardiomyogenesis and reduces myocardial infarct size in sheep. Gene Ther. 13 (2006) 1133-1142
33. Grunewald M., et al. VEGF-induced adult neovascularization: recruitment, retention, and role of accessory cells. Cell 124 (2006) 175-189
34. Abbott J.D., et al. Stromal cell-derived factor-1α plays a critical role in stem cell recruitment to the heart after myocardial infarction but is not sufficient to induce homing in the absence of injury. Circulation 110 (2004) 3300-3305
35. Dawn B., et al. Cardiac stem cells delivered intravascularly traverse the vessel barrier, regenerate infarcted myocardium, and improve cardiac function. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 3766-3771
36. Wei H., et al. Embryonic stem cells and cardiomyocyte differentiation: phenotypic and molecular analyses. J. Cell. Mol. Med. 9 (2005) 804-817
37. Illi B., et al. Epigenetic histone modification and cardiovascular lineage programming in mouse embryonic stem cells exposed to laminar shear stress. Circ. Res. 96 (2005) 501-508
38. Yuasa S., et al. Transient inhibition of BMP signaling by Noggin induces cardiomyocyte differentiation of mouse embryonic stem cells. Nat. Biotechnol. 23 (2005) 607-611
39. Nemir M., et al. Induction of cardiogenesis in embryonic stem cells via downregulation of Notch1 signaling. Circ. Res. 98 (2006) 1471-1478
40. Kluppel M., and Wrana J.L. Turning it up a Notch: cross-talk between TGF β and Notch signaling. Bioessays 27 (2005) 115-118
41. Klug M.G., et al. Genetically selected cardiomyocytes from differentiating embronic stem cells form stable intracardiac grafts. J. Clin. Invest. 98 (1996) 216-224
42. Kehat I., et al. Electromechanical integration of cardiomyocytes derived from human embryonic stem cells. Nat. Biotechnol. 22 (2004) 1282-1289
43. Menard C., et al. Transplantation of cardiac-committed mouse embryonic stem cells to infarcted sheep myocardium: a preclinical study. Lancet 366 (2005) 1005-1012
44. Rubart M., and Field L.J. Cardiac repair by embryonic stem-derived cells. Handb Exp Pharmacol. (2006) 73-100
45. van Tuyn J., et al. Activation of cardiac and smooth muscle-specific genes in primary human cells after forced expression of human myocardin. Cardiovasc. Res. 67 (2005) 245-255
46. Wollert K.C., and Drexler H. Clinical applications of stem cells for the heart. Circ. Res. 96 (2005) 151-163
47. Leri A., et al. Cardiac stem cells and mechanisms of myocardial regeneration. Physiol. Rev. 85 (2005) 1373-1416
48. Murry C.E., et al. Regeneration gaps: observations on stem cells and cardiac repair. J. Am. Coll. Cardiol. 47 (2006) 1777-1785
49. Orlic D., et al. Bone marrow cells regenerate infarcted myocardium. Nature 410 (2001) 701-705
50. Balsam L.B., et al. Haematopoietic stem cells adopt mature haematopoietic fates in ischaemic myocardium. Nature 428 (2004) 668-673
51. Murry C.E., et al. Haematopoietic stem cells do not transdifferentiate into cardiac myocytes in myocardial infarcts. Nature 428 (2004) 664-668
52. Alvarez-Dolado M., et al. Fusion of bone-marrow-derived cells with Purkinje neurons, cardiomyocytes and hepatocytes. Nature 425 (2003) 968-973
53. Vassilopoulos G., et al. Transplanted bone marrow regenerates liver by cell fusion. Nature 422 (2003) 901-904
54. Wang X., et al. Cell fusion is the principal source of bone-marrow-derived hepatocytes. Nature 422 (2003) 897-901
55. Nygren J.M., et al. Bone marrow-derived hematopoietic cells generate cardiomyocytes at a low frequency through cell fusion, but not transdifferentiation. Nat. Med. 10 (2004) 494-501
56. Pittenger M.F., and Martin B.J. Mesenchymal stem cells and their potential as cardiac therapeutics. Circ. Res. 95 (2004) 9-20
57. Shake J.G., et al. Mesenchymal stem cell implantation in a swine myocardial infarct model: engraftment and functional effects. Ann. Thorac. Surg. 73 (2002) 1919-1925
58. Kocher A.A., et al. Neovascularization of ischemic myocardium by human bone-marrow-derived angioblasts prevents cardiomyocyte apoptosis, reduces remodeling and improves cardiac function. Nat. Med. 7 (2001) 430-436
59. Kawamoto A., et al. Intramyocardial transplantation of autologous endothelial progenitor cells for therapeutic neovascularization of myocardial ischemia. Circulation 107 (2003) 461-468
60. + cells. FASEB J. 18 (2004) 1392-1394
61. Iwasaki H., et al. Dose-dependent contribution of CD34-positive cell transplantation to concurrent vasculogenesis and cardiomyogenesis for functional regenerative recovery after myocardial infarction. Circulation 113 (2006) 1311-1325
62. Zhang S., et al. Both cell fusion and transdifferentiation account for the transformation of human peripheral blood CD34-positive cells into cardiomyocytes in vivo. Circulation 110 (2004) 3803-3807
63. Kajstura J., et al. Bone marrow cells differentiate in cardiac cell lineages after infarction independently of cell fusion. Circ. Res. 96 (2005) 127-137
64. Ishikawa F., et al. Purified human hematopoietic stem cells contribute to the generation of cardiomyocytes through cell fusion. FASEB J. 20 (2006) 950-952
65. Yoon Y.S., et al. Clonally expanded novel multipotent stem cells from human bone marrow regenerate myocardium after myocardial infarction. J. Clin. Invest. 115 (2005) 326-338
66. Miyahara Y., et al. Monolayered mesenchymal stem cells repair scarred myocardium after myocardial infarction. Nat. Med. 12 (2006) 459-465
67. Caplan A.I., and Dennis J.E. Mesenchymal stem cells as trophic mediators. J. Cell. Biochem. 98 (2006) 1076-1084
68. Urbich C., et al. Soluble factors released by endothelial progenitor cells promote migration of endothelial cells and cardiac resident progenitor cells. J. Mol. Cell. Cardiol. 39 (2005) 733-742
69. + cells are from the bone marrow and regulate the myocardial balance of angiogenic cytokines. J. Clin. Invest. 116 (2006) 1865-1877
70. Gnecchi M., et al. Paracrine action accounts for marked protection of ischemic heart by Akt-modified mesenchymal stem cells. Nat. Med. 11 (2005) 367-368
71. Menasche P., et al. Routine delivery of myoblasts during coronary artery bypass surgery: why not?. Nat. Clin. Pract. Cardiovasc. Med. 3 Suppl 1 (2006) S90-S93
72. Siminiak T., et al. Postinfarction heart failure: surgical and trans-coronary-venous transplantation of autologous myoblasts. Nat Clin Pract Cardiovasc Med. 3 Suppl 1 (2006) S46-S51
73. Leobon B., et al. Myoblasts transplanted into rat infarcted myocardium are functionally isolated from their host. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 7808-7811
74. Rubart M., et al. Spontaneous and evoked intracellular calcium transients in donor-derived myocytes following intracardiac myoblast transplantation. J. Clin. Invest. 114 (2004) 775-783
75. Wollert K.C., and Drexler H. Cell-based therapy for heart failure. Curr. Opin. Cardiol. 21 (2006) 234-239
76. Schachinger V., et al. Intracoronary bone marrow-derived progenitor cells in acute myocardial infarction. N. Engl. J. Med. 355 (2006) 1210-1221
77. Assmus B., et al. Transcoronary transplantation of progenitor cells after myocardial infarction. N. Engl. J. Med. 355 (2006) 1222-1232
78. Lunde K., et al. Intracoronary injection of mononuclear bone marrow cells in acute myocardial infarction. N. Engl. J. Med. 355 (2006) 1199-1209
79. Regula K.M., et al. Therapeutic opportunities for cell cycle re-entry and cardiac regeneration. Cardiovasc. Res. 64 (2004) 395-401
80. Cobrinik D. Pocket proteins and cell cycle control. Oncogene 24 (2005) 2796-2809
81. Kirshenbaum L.A., et al. Human E2F-1 reactivates cell cycle progression in ventricular myocytes and represses cardiac gene transcription. Dev. Biol. 179 (1996) 402-411
82. Berk A.J. Recent lessons in gene expression, cell cycle control, and cell biology from adenovirus. Oncogene 24 (2005) 7673-7685
83. Pasumarthi K.B., et al. Targeted expression of cyclin D2 results in cardiomyocyte DNA synthesis and infarct regression in transgenic mice. Circ. Res. 96 (2005) 110-118
84. Nakajima H., et al. Expression of mutant p193 and p53 permits cardiomyocyte cell cycle reentry after myocardial infarction in transgenic mice. Circ. Res. 94 (2004) 1606-1614
85. MacLellan W.R., et al. Overlapping roles of pocket proteins in the myocardium are unmasked by germ line deletion of p130 plus heart-specific deletion of Rb. Mol. Cell. Biol. 25 (2005) 2486-2497
86. Soonpaa M.H., et al. Cyclin D1 overexpression promotes cardiomyocyte DNA synthesis and multinucleation in transgenic mice. J. Clin. Invest. 99 (1997) 2644-2654
87. Chaudhry H.W., et al. Cyclin A2 mediates cardiomyocyte mitosis in the postmitotic myocardium. J. Biol. Chem. 279 (2004) 35858-35866
88. Poolman R.A., et al. Altered expression of cell cycle proteins and prolonged duration of cardiac myocyte hyperplasia in p27KIP1 knockout mice. Circ. Res. 85 (1999) 117-127
89. Rota M., et al. Nuclear targeting of Akt enhances ventricular function and myocyte contractility. Circ. Res. 97 (2005) 1332-1341
90. Gude N., et al. Akt promotes increased cardiomyocyte cycling and expansion of the cardiac progenitor cell population. Circ. Res. 99 (2006) 381-388
91. Engel F.B., et al. p38 MAP kinase inhibition enables proliferation of adult mammalian cardiomyocytes. Genes Dev. 19 (2005) 1175-1187
92. Limana F., et al. Bcl-2 overexpression promotes myocyte proliferation. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 6257-6262