Characterization of long-term cultured c-kit+ cardiac stem cells derived from adult rat hearts

Stem Cells and Development

Volumn 19, Issue 1, 2010, Pages 105-116

  Miyamoto, Shinka ^a,b   Kawaguchi, Nanako ^b   Ellison, Georgina M ^c   Matsuoka, Rumiko ^b   Shin'Oka, Toshiharu ^c   Kurosawa, Hiromi ^a  

^a TOKYO WOMEN'S MEDICAL UNIVERSITY   (Japan)

^b LIVERPOOL JOHN MOORES UNIVERSITY   (United Kingdom)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SOMATOMEDIN; STEM CELL FACTOR RECEPTOR; TRANSCRIPTION FACTOR GATA 4; VASCULOTROPIN;

ADIPOCYTE; ADULTHOOD; ANIMAL CELL; ARTICLE; CARDIAC STEM CELL; CELL CULTURE; CELL DIFFERENTIATION; CELL ISOLATION; CELL LINEAGE; CELL REGENERATION; CELL TRANSPLANTATION; CONTROLLED STUDY; CULTURE TECHNIQUE; ENDOTHELIUM CELL; HEART MUSCLE CELL; NONHUMAN; PRIORITY JOURNAL; RAT; SKELETAL MUSCLE; SMOOTH MUSCLE; STEM CELL;

ADIPOCYTES; ADULT STEM CELLS; AGE FACTORS; ANIMALS; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SEPARATION; CELLS, CULTURED; MUSCLE FIBERS, SKELETAL; MYOCARDIUM; MYOCYTES, CARDIAC; PROTO-ONCOGENE PROTEINS C-KIT; RATS; RATS, INBRED LEW; RATS, TRANSGENIC; RATS, WISTAR; TIME FACTORS;

MAMMALIA; RATTUS;

EID: 75749155371     PISSN: 15473287     EISSN: None     Source Type: Journal    
DOI: 10.1089/scd.2009.0041     Document Type: Article

References (58)

1. Braunwald E and M Bristow. (2000). Congestive heart failure: fifty years of progress. Circulation 102:IV14-IV23.
2. Braunwald E and M Pfeffer. (1991). Ventricular enlargement and remodeling following acute myocardial infarction: mechanisms and management. Am J Cardiol 68:1D-6D.
3. Olivetti G, R Abbi, F Quaini, J Kajstura, W Cheng, J Nitahara, E Quaini, C Di Loreto, C Beltrami, S Krajewski, J Reed and P Anversa. (1997). Apoptosis in the failing human heart. N Engl J Med 336:1131-1141.
4. Wencker D, M Chandra, K Nguyen, W Miao, S Garantziotis, S Factor, J Shirani, R Armstrong and R Kitsis. (2003). A mechanistic role for cardiac myocyte apoptosis in heart failure. J Clin Invest 111:1497-1504.
5. Bernecker O, F Huq, E Heist, B Podesser and R Hajjar. (2003). Apoptosis in heart failure and the senescent heart. Cardiovasc Toxicol 3:183-190.
6. Beltrami A, L Barlucchi, D Torella, M Baker, F Limana, S Chimenti, H Kasahara, M Rota, E Musso, K Urbanek, A Leri, J Kajstura, B Nadal-Ginard and P Anversa. (2003). Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell 114:763-776.
7. Ellison G, D Torella, I Karakikes, S Purushothaman, A Curcio, C Gasparri, C Indolfi, N Cable, D Goldspink and B Nadal-Ginard. (2007). Acute beta-adrenergic overload produces myocyte damage through calcium leakage from the ryanodine receptor 2 but spares cardiac stem cells. J Biol Chem 282:11397-11409.
8. Boheler K, J Czyz, D Tweedie, H Yang, S Anisimov and A Wobus. (2002). Differentiation of pluripotent embryonic stem cells into cardiomyocytes. Circ Res 91:189-201. (Pubitemid 34875673)
9. Hescheler J, B Fleischmann, S Lentini, V Maltsev, J Rohwedel, A Wobus and K Addicks. (1997). Embryonic stem cells: a model to study structural and functional properties in cardiomyogenesis. Cardiovasc Res 36:149-162.
10. Nussbaum J, E Minami, M Laflamme, J Virag, C Ware, A Masino, V Muskheli, L Pabon, H Reinecke and C Murry. (2007). Transplantation of undifferentiated murine embryonic stem cells in the heart: teratoma formation and immune response. FASEB J 21:1345-1357.
11. Takahashi K and S Yamanaka. (2006). Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126:663-676.
12. Takahashi K, K Tanabe, M Ohnuki, M Narita, T Ichisaka, K Tomoda and S Yamanaka. (2007). Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131:861-872.
13. Beltrami A, D Cesselli, N Bergamin, P Marcon, S Rigo, E Puppato, F D'Aurizio, R Verardo, S Piazza, A Pignatelli, A Poz, U Baccarani, D Damiani, R Fanin, L Mariuzzi, N Finato, P Masolini, S Burelli, O Belluzzi, C Schneider and C Beltrami. (2007). Multipotent cells can be generated in vitro from several adult human organs (heart, liver, and bone marrow). Blood 110:3438-3446.
14. Strauer B, M Brehm, T Zeus, M Kostering, A Hernandez, R Sorg, G Kogler and P Wernet. (2002). Repair of infarcted myocardium by autologous intracoronary mononuclear bone marrow cell transplantation in humans. Circulation 106:1913-1918.
15. Britten M, N Abolmaali, B Assmus, R Lehmann, J Honold, J Schmitt, T Vogl, H Martin, V Schachinger, S Dimmeler and A Zeiher. (2003). Infarct remodeling after intracoronary progenitor cell treatment in patients with acute myocardial infarction (TOPCARE-AMI): mechanistic insights from serial contrast-enhanced magnetic resonance imaging. Circulation 108:2212-2218.
16. Perin E, H Dohmann, R Borojevic, S Silva, A Sousa, C Mesquita, M Rossi, A Carvalho, H Dutra, H Dohmann, G Silva, L Belem, R Vivacqua, F Rangel, R Esporcatte, Y Geng, W Vaughn, J Assad, E Mesquita and J Willerson. (2003). Transendocardial, autologous bone marrow cell transplantation for severe, chronic ischemic heart failure. Circulation 107:2294-2302.
17. Stamm C, B Westphal, H Kleine, M Petzsch, C Kittner, H Klinge, C Schumichen, C Nienaber, M Freund and G Steinhoff. (2003). Autologous bone-marrow stem-cell transplantation for myocardial regeneration. Lancet 361:45-46.
18. Tse H, Y Kwong, J Chan, G Lo, C Ho and C Lau. (2003). Angiogenesis in ischaemic myocardium by intramyocardial autologous bone marrow mononuclear cell implantation. Lancet 361:47-49.
19. Nygren J, S Jovinge, M Breitbach, P Sawen, W Roll, J Hescheler, J Taneera, B Fleischmann and S Jacobsen. (2004). Bone marrowderived hematopoietic cells generate cardiomyocytes at a low frequency through cell fusion, but not transdifferentiation. Nat Med 10:494-501.
20. Jackson K, S Majka, H Wang, J Pocius, C Hartley, M Majesky, M Entman, L Michael, K Hirschi and M Goodell. (2001). Regeneration of ischemic cardiac muscle and vascular endothelium by adult stem cells. J Clin Invest 107:1395-1402.
21. Murry C, M Soonpaa, H Reinecke, H Nakajima, H Nakajima, M Rubart, K Pasumarthi, J Virag, S Bartelmez, V Poppa, G Bradford, J Dowell, D Williams and L Field. (2004). Haematopoietic stem cells do not transdifferentiate into cardiomyocytes in myocardial infarcts. Nature 428:664-668.
22. Orlic D, J Kajstura, S Chimenti, D Bodine, A Leri and P Anversa. (2001). Transplanted adult bone marrow cells repair myocardial infarcts in mice. Ann N Y Acad Sci 938:221-229.
23. Dawn B, A Stein, K Urbanek, M Rota, B Whang, R Rastaldo, D Torella, X Tang, A Rezazadeh, J Kajstura, A Leri, G Hunt, J Varma, S Prabhu, P Anversa and R Bolli. (2005). Cardiac stem cells delivered intravascularly traverse the vessel barrier, regenerate infarcted myocardium, and improve cardiac function. Proc Natl Acad Sci USA 102:3766-3771. (Pubitemid 40354686)
24. Bergmann O, RD Bhardwaj, S Bernard, S Zdunek, F Barnabe- Heider, S Walsh, J Zupicich, K Alkass, BA Buchholz, H Druid, S Jovinge and J Frisen. (2009). Evidence for cardiomyocyte renewal in humans. Science 324:98-102.
25. Colucci W. (1997). Molecular and cellular mechanisms of myocardial failure. Am J Cardiol 80:15L-25L.
26. Towbin J and N Bowles. (2002). The failing heart. Nature 415:227-233.
27. Oh H, S Bradfute, T Gallardo, T Nakamura, V Gaussin, Y Mishina, J Pocius, L Michael, R Behringer, D Garry, M Entman and M Schneider. (2003). Cardiac progenitor cells from adult myocardium: homing, differentiation, and fusion after infarction. Proc Natl Acad Sci USA 100:12313-12318.
28. Matsuura K, T Nagai, N Nishigaki, T Oyama, J Nishi, H Wada, M Sano, H Toko, H Akazawa, T Sato, H Nakaya, H Kasanuki and I Komuro. (2004). Adult cardiac Sca-1-positive cells differentiate into beating cardiomyocytes. J Biol Chem 279:11384-11391.
29. Smits A, L van Laake, K den Ouden, C Schreurs, K Szuhai, C van Echteld, C Mummery, P Doevendans and M Goumans. (2009). Human cardiomyocyte progenitor cell transplantation preserves long-term function of the infarcted mouse myocardium. Cardiovasc Res. May 9. [Epub ahead of print].
30. Martin C, A Meeson, S Robertson, T Hawke, J Richardson, S Bates, S Goetsch, T Gallardo and D Garry. (2004). Persistent expression of the ATP-binding cassette transporter, Abcg2, identifies cardiac SP cells in the developing and adult heart. Dev Biol 265:262-275.
31. Pfister O, F Mouquet, M Jain, R Summer, M Helmes, A Fine, WS Colucci and R Liao. (2005). CD31- but Not CD31+ cardiac side population cells exhibit functional cardiomyogenic differentiation. Circ Res. 97:52-61.
32. Tomita Y, K Matsumura, Y Wakamatsu, Y Matsuzaki, I Shibuya, H Kawaguchi, M Ieda, S Kanakubo, T Shimazaki, S Ogawa, N Osumi, H Okano and K Fukuda. (2005). Cardiac neural crest cells contribute to the dormant multipotent stem cell in the mammalian heart. J Cell Biol 170:1135-1146.
33. Messina E, L De Angelis, G Frati, S Morrone, S Chimenti, F Fiordaliso, M Salio, M Battaglia, M Latronico, M Coletta, E Vivarelli, L Frati, G Cossu and A Giacomello. (2004). Isolation and expansion of adult cardiac stem cells from human and murine heart. Circ Res 95:911-921.
34. Wu S, Y Fujiwara, S Cibulsky, D Clapham, C Lien, T Schultheiss and S Orkin. (2006). Developmental origin of a bipotential myocardial and smooth muscle cell precursor in the mammalian heart. Cell 127:1137-1150.
35. Linke A, P Muller, D Nurzynska, C Casarsa, D Torella, A Nascimbene, C Castaldo, S Cascapera, M Bohm, F Quaini, K Urbanek, A Leri, T Hintze, J Kajstura and P Anversa. (2005). Stem cells in the dog heart are self-renewing, clonogenic, and multipotent and regenerate infarcted myocardium, improving cardiac function. Proc Natl Acad Sci USA 102:8966-8971. (Pubitemid 40881062)
36. Torella D, G Ellison, S Mendez-Ferrer, B Ibanez and B Nadal- Ginard. (2006). Resident human cardiac stem cells: role in cardiac cellular homeostasis and potential for myocardial regeneration. Nat Clin Pract Cardiovasc Med 3(Suppl 1):S8-S13.
37. Laugwitz K, A Moretti, J Lam, P Gruber, Y Chen, S Woodard, L Lin, C Cai, M Lu, M Reth, O Platoshyn, J Yuan, S Evans and K Chien. (2005). Postnatal isl1+ cardioblasts enter fully differentiated cardiomyocyte lineages. Nature 433:647-653.
38. Torella D, C Indolfi, D Goldspink and G Ellison. (2008). Cardiac stem cell-based myocardial regeneration: towards a translational approach. Cardiovasc Hematol Agents Med Chem 6:53-59.
39. Ellison G, D Torella, I Karakikes and B Nadal-Ginard. (2007). Myocyte death and renewal: modern concepts of cardiac cellular homeostasis. Nat Clin Pract Cardiovasc Med 4(Suppl 1):S52-S59.
40. Potten C and M Loeffler. (1990). Stem cells: attributes, cycles, spirals, pitfalls and uncertainties. Lessons for and from the crypt. Development 110:1001-1020.
41. Torella D, GM Ellison, I Karakikes and B Nadal-Ginard. (2007). Resident cardiac stem cells. Cell Mol Life Sci. 64:661-673
42. Bearzi C, M Rota, T Hosoda, J Tillmanns, A Nascimbene, A De Angelis, S Yasuzawa-Amano, I Trofimova, R Siggins, N Lecapitaine, S Cascapera, A Beltrami, D D'Alessandro, E Zias, F Quaini, K Urbanek, R Michler, R Bolli, J Kajstura, A Leri and P Anversa. (2007). Human cardiac stem cells. Proc Natl Acad Sci USA 104:14068-14073.
43. Suslov O, V Kukekov, T Ignatova and D Steindler. (2002). Neural stem cell heterogeneity demonstrated by molecular phenotyping of clonal neurospheres. Proc Natl Acad Sci USA 99:14506-111451
44. Rosenblatt-Velin N, M Lepore, C Cartoni, F Beermann and T Pedrazzini. (2005). FGF-2 controls the differentiation of resident cardiac precursors into functional cardiomyocytes. J Clin Invest 115:1724-1733.
45. Pouly J, P Bruneval, C Mandet, S Proksch, S Peyrard, C Amrein, V Bousseaux, R Guillemain, A Deloche, J Fabiani and P Menasche. (2008). Cardiac stem cells in the real world. J Thorac Cardiovasc Surg 135:673-678
46. Kelley C, H Blumberg, L Zon and T Evans. (1993). GATA-4 is a novel transcription factor expressed in endocardium of the developing heart. Development 118:817-827.
47. Molkentin J, Q Lin, S Duncan and E Olson. (1997). Requirement of the transcription factor GATA4 for heart tube formation and ventral morphogenesis. Genes Dev 11:1061-1072.
48. Oka T, M Maillet, A Watt, R Schwartz, B Aronow, S Duncan and J Molkentin. (2006). Cardiac-specific deletion of Gata4 reveals its requirement for hypertrophy, compensation, and myocyte viability. Circ Res 98:837-845.
49. Smith R, L Barile, H Cho, M Leppo, J Hare, E Messina, A Giacomello, M Abraham and E Marban. (2007). Regenerative potential of cardiosphere-derived cells expanded from percutaneous endomyocardial biopsy specimens. Circulation 115:896-908.
50. Ott H, T Matthiesen, J Brechtken, S Grindle, S Goh, W Nelson and D Taylor. (2007). The adult human heart as a source for stem cells: repair strategies with embryonic-like progenitor cells. Nat Clin Pract Cardiovasc Med 4(Suppl 1):S27-S39.
51. Torella D, G Ellison, I Karakikes and B Nadal-Ginard. (2007). Growth-factor-mediated cardiac stem cell activation in myocardial regeneration. Nat Clin Pract Cardiovasc Med 4(Suppl 1):S46-S51.
52. Urbanek K, M Rota, S Cascapera, C Bearzi, A Nascimbene, A De Angelis, T Hosoda, S Chimenti, M Baker, F Limana, D Nurzynska, D Torella, F Rotatori, R Rastaldo, E Musso, F Quaini, A Leri, J Kajstura and P Anversa. (2005). Cardiac stem cells possess growth factor-receptor systems that after activation regenerate the infarcted myocardium, improving ventricular function and long-term survival. Circ Res 97:663-673.
53. Torella D, M Rota, D Nurzynska, E Musso, A Monsen, I Shiraishi, E Zias, K Walsh, A Rosenzweig, M Sussman, K Urbanek, B Nadal-Ginard, J Kajstura, P Anversa and A Leri. (2004). Cardiac stem cell and myocyte aging, heart failure, and insulin-like growth factor-1 overexpression. Circ Res 94:514-524.
54. Uemura R, M Xu, N Ahmad and M Ashraf. (2006). Bone marrow stem cells prevent left ventricular remodeling of ischemic heart through paracrine signaling. Circ Res 98:1414-1421.
55. Dimmeler S, J Burchfield and A Zeiher. (2008). Cell-based therapy of myocardial infarction. Arterioscler Thromb Vasc Biol 28:208-216.
56. Fazel S, M Cimini, L Chen, S Li, D Angoulvant, P Fedak, S Verma, R Weisel, A Keating and R Li. (2006). Cardioprotective c-kit+ cells are from the bone marrow and regulate the myocardial balance of angiogenic cytokines. J Clin Invest 116:1865-1877.
57. Sadat S, S Gehmert, Y Song, Y Yen, X Bai, S Gaiser, H Klein and E Alt. (2007). The cardioprotective effect of mesenchymal stem cells is mediated by IGF-I and VEGF. Biochem Biophys Res Commun 363:674-679.
58. Wagers A and I Weissman. (2004). Plasticity of adult stem cells. Cell 116:639-648.