C-kit+ cardiac progenitors exhibit mesenchymal markers and preferential cardiovascular commitment

Cardiovascular Research

Volumn 89, Issue 2, 2011, Pages 362-373

  Gambini, Elisa ^a,b   Pompilio, Giulio ^a,b,c   Biondi, Andrea ^d   Alamanni, Francesco ^b,c   Capogrossi, Maurizio C ^e   Agrifoglio, Marco ^b,c   Pesce, Maurizio ^a  

^a Laboratorio di Biologia Vascolare e Medicina Rigenerativa   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

^c CENTRO CARDIOLOGICO MONZINO   (Italy)

^d UNIVERSITY OF MILANO BICOCCA   (Italy)

^e LABORATORIO DI PATOLOGIA VASCOLARE   (Italy)

Author keywords

C kit; Cardiac MSC; Cardiac progenitor; Differentiation

Indexed keywords

BIOLOGICAL MARKER; STEM CELL FACTOR;

ADIPOCYTE; AGING; ARTICLE; BONE MARROW; CARDIAC PROGENITOR; CELL DIFFERENTIATION; CELL LINEAGE; CONTROLLED STUDY; ENDOTHELIUM CELL; FIBROBLAST; FLOW CYTOMETRY; HEART INFARCTION; HOMEOSTASIS; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE; IN VITRO STUDY; IN VIVO STUDY; MESENCHYMAL STEM CELL; MULTIPOTENT STEM CELL; OSTEOBLAST; PHENOTYPE; PRIORITY JOURNAL; STEM CELL; STRESS; VASCULAR ENDOTHELIUM; VASCULAR SMOOTH MUSCLE;

ADIPOCYTES; BIOLOGICAL MARKERS; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; CELL SEPARATION; CELLS, CULTURED; COCULTURE TECHNIQUES; ENDOTHELIAL CELLS; FIBROBLASTS; FLOW CYTOMETRY; HUMANS; IMMUNOHISTOCHEMISTRY; MESENCHYMAL STEM CELLS; MYOCARDIUM; MYOCYTES, SMOOTH MUSCLE; OSTEOBLASTS; PHENOTYPE; PROTO-ONCOGENE PROTEINS C-KIT;

EID: 78751538785     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvq292     Document Type: Article

References (50)

1. Beltrami AP, Urbanek K, Kajstura J, Yan SM, Finato N, Bussani R et al. Evidence that human cardiac myocytes divide after myocardial infarction. N Engl J Med 2001;344: 1750-1757.
2. Bergmann O, Bhardwaj RD, Bernard S, Zdunek S, Barnabe-Heider F, Walsh S et al. Evidence for cardiomyocyte renewal in humans. Science 2009;324:98-102.
3. Kajstura J, Urbanek K, Perl S, Hosoda T, Zheng H, Ogorek B et al. Cardiomyogenesis in the adult human heart. Circ Res 2010;107:305-315.
4. Oh H, Bradfute SB, Gallardo TD, Nakamura T, Gaussin V, Mishina Y et al. Cardiac progenitor cells from adult myocardium: homing, differentiation, and fusion after infarction. Proc Natl Acad Sci USA 2003;100:12313-12318.
5. Matsuura K, Nagai T, Nishigaki N, Oyama T, Nishi J, Wada H et al. Adult cardiac Sca-1-positive cells differentiate into beating cardiomyocytes. J Biol Chem 2004;279: 11384-11391.
6. Smits AM, van Vliet P, Metz CH, Korfage T, Sluijter JP, Doevendans PA et al. Human cardiomyocyte progenitor cells differentiate into functional mature cardiomyocytes: an in vitro model for studying human cardiac physiology and pathophysiology. Nat Protoc 2009;4:232-243.
7. Smith RR, Barile L, Cho HC, Leppo MK, Hare JM, Messina E et al. Regenerative potential of cardiosphere-derived cells expanded from percutaneous endomyocardial biopsy specimens. Circulation 2007;115:896-908.
8. Messina E, De Angelis L, Frati G, Morrone S, Chimenti S, Fiordaliso F et al. Isolation and expansion of adult cardiac stem cells from human and murine heart. Circ Res 2004; 95:911-921.
9. Laugwitz KL, Moretti A, Lam J, Gruber P, Chen Y, Woodard S et al. Postnatal isl1+ cardioblasts enter fully differentiated cardiomyocyte lineages. Nature 2005;433: 647-653.
10. Moretti A, Caron L, Nakano A, Lam JT, Bernshausen A, Chen Y et al. Multipotent embryonic isl1+ progenitor cells lead to cardiac, smooth muscle, and endothelial cell diversification. Cell 2006;127:1151-1165.
11. Limana F, Zacheo A, Mocini D, Mangoni A, Borsellino G, Diamantini A et al. Identifi- cation of myocardial and vascular precursor cells in human and mouse epicardium. Circ Res 2007;101:1255-1265.
12. BeltramiAP, Barlucchi L,TorellaD, Baker M, Limana F, Chimenti S et al.Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell 2003;114:763-776.
13. Bearzi C, Rota M, Hosoda T, Tillmanns J, Nascimbene A, De Angelis A et al. Human cardiac stem cells. Proc Natl Acad Sci USA 2007;104:14068-14073.
14. Bearzi C, Leri A, Lo Monaco F, Rota M, Gonzalez A, Hosoda T et al. Identification of a coronary vascular progenitor cell in the human heart. Proc Natl Acad Sci USA 2009; 106:15885-15890.
15. Garcia-Castro J, Trigueros C, Madrenas J, Perez-Simon JA, Rodriguez R, Menendez P. Mesenchymal stem cells and their use as cell replacement therapy and disease modelling tool. J Cell Mol Med 2008;12:2552-2565.
16. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006;8:315-317.
17. Amado LC, Saliaris AP, Schuleri KH, St John M, Xie JS, Cattaneo S et al. Cardiac repair with intramyocardial injection of allogeneic mesenchymal stem cells after myocardial infarction. Proc Natl Acad Sci USA 2005;102:11474-11479.
18. Silva GV, Litovsky S, Assad JA, Sousa AL, Martin BJ, VelaD et al. Mesenchymal stem cells differentiate into an endothelial phenotype, enhance vascular density, and improve heart function in a canine chronic ischemia model. Circulation 2005;111:150-156.
19. Gnecchi M, He H, Liang OD, Melo LG, Morello F, Mu H et al. Paracrine action accounts for marked protection of ischemic heart by Akt-modified mesenchymal stem cells. Nat Med 2005;11:367-368.
20. Makino S, Fukuda K, Miyoshi S, Konishi F, Kodama H, Pan J et al. Cardiomyocytes can be generated from marrow stromal cells in vitro. J Clin Invest 1999;103:697-705.
21. Quevedo HC, Hatzistergos KE, Oskouei BN, Feigenbaum GS, Rodriguez JE, Valdes D et al. Allogeneic mesenchymal stem cells restore cardiac function in chronic ischemic cardiomyopathy via trilineage differentiating capacity. Proc Natl Acad Sci USA 2009;106: 14022-14027.
22. Hatzistergos KE, Quevedo H, Oskouei BN, Hu Q, Feigenbaum GS, Margitich IS et al. Bone marrow mesenchymal stem cells stimulate cardiac stem cell proliferation and differentiation. Circ Res 2010.
23. Yoon YS, Park JS, Tkebuchava T, Luedeman C, Losordo DW. Unexpected severe calcification after transplantation of bone marrow cells in acute myocardial infarction. Circulation 2004;109:3154-3157.
24. Breitbach M, Bostani T, Roell W, Xia Y, Dewald O, Nygren JM et al. Potential risks of bone marrow cell transplantation into infarcted hearts. Blood 2007;110:1362-1369.
25. Joggerst SJ, Hatzopoulos AK. Stem cell therapy for cardiac repair: benefits and barriers. Expert Rev Mol Med 2009;11:e20.
26. Hare JM, Traverse JH, Henry TD, Dib N, Strumpf RK, Schulman SP et al. A randomized, double-blind, placebo-controlled, dose-escalation study of intravenous adult human mesenchymal stem cells (prochymal) after acute myocardial infarction. J Am Coll Cardiol 2009;54:2277-2286.
27. Davis DR, Kizana E, Terrovitis J, Barth AS, Zhang Y, Smith RR et al. Isolation and expansion of functionally-competent cardiac progenitor cells directly from heart biopsies. J Mol Cell Cardiol 2010;49:312-321.
28. Davis DR, Zhang Y, Smith RR, Cheng K, Terrovitis J, Malliaras K et al. Validation of the cardiosphere method to culture cardiac progenitor cells from myocardial tissue. PLoS One 2009;4:e7195.
29. Itzhaki-Alfia A, Leor J, Raanani E, Sternik L, Spiegelstein D, Netser S et al. Patient characteristics and cell source determine the number of isolated human cardiac progenitor cells. Circulation 2009;120:2559-2566.
30. Urbanek K, Cesselli D, Rota M, Nascimbene A, De Angelis A, Hosoda T et al. Stem cell niches in the adult mouse heart. Proc Natl Acad Sci USA 2006;103:9226-9231.
31. Davis DR, Smith RR, Marban E. Human cardiospheres are a source of stem cells with cardiomyogenic potential. Stem Cells 2010;28:903-904.
32. Sensebe L, Bourin P. Mesenchymal stem cells for therapeutic purposes. Transplantation 2009;87:S49-S53.
33. Rossini A, Zacheo A, Mocini D, Totta P, Facchiano A, Castoldi R et al. HMGB1-stimulated human primary cardiac fibroblasts exert a paracrine action on human and murine cardiac stem cells. J Mol Cell Cardiol 2008;44:683-693.
34. Takeuchi JK, Bruneau BG. Directed transdifferentiation of mouse mesoderm to heart tissue by defined factors. Nature 2009;459:708-711.
35. Lee OK, Kuo TK, Chen WM, Lee KD, Hsieh SL, Chen TH. Isolation of multipotent mesenchymal stem cells from umbilical cord blood. Blood 2004;103:1669-1675.
36. Cappuzzello C, Melchionna R, Mangoni A, Tripodi G, Ferrari P, Torielli L et al. Role of rat a adducin in angiogenesis: null effect of the F316Y polymorphism. Cardiovasc Res 2007;75:608-617.
37. Ventura C, Maioli M, Asara Y, Santoni D, Scarlata I, Cantoni S et al. Butyric and retinoic mixed ester of hyaluronan. A novel differentiating glycoconjugate affording a high throughput of cardiogenesis in embryonic stem cells. J Biol Chem 2004;279:23574-23579.
38. Anversa P, Kajstura J, Leri A, Bolli R. Life and death of cardiac stem cells: a paradigm shift in cardiac biology. Circulation 2006;113:1451-1463.
39. Souders CA, Bowers SL, Baudino TA. Cardiac fibroblast: the renaissance cell. Circ Res 2009;105:1164-1176.
40. Tateishi K, Ashihara E, Takehara N, Nomura T, Honsho S, Nakagami T et al. Clonally amplified cardiac stem cells are regulated by Sca-1 signaling for efficient cardiovascular regeneration. J Cell Sci 2007;120:1791-1800.
41. Matsuura K, Honda A, Nagai T, Fukushima N, Iwanaga K, Tokunaga M et al. Transplantation of cardiac progenitor cells ameliorates cardiac dysfunction after myocardial infarction in mice. J Clin Invest 2009;119:2204-2217.
42. Tateishi K, Ashihara E, Honsho S, Takehara N, Nomura T, Takahashi T et al. Human cardiac stem cells exhibit mesenchymal features and are maintained through Akt/ GSK-3b signaling. Biochem Biophys Res Commun 2007;352:635-641.
43. Goumans MJ, de Boer TP, Smits AM, van Laake LW, van Vliet P, Metz CH et al. TGF-beta1 induces efficient differentiation of human cardiomyocyte progenitor cells into functional cardiomyocytes in vitro. Stem Cell Res 2007;1:138-149.
44. Tallini YN, Greene KS, Craven M, Spealman A, Breitbach M, Smith J et al. c-kit expression identifies cardiovascular precursors in the neonatal heart. Proc Natl Acad Sci USA 2009;106:1808-1813.
45. Rossini A, Frati C, Lagrasta C, Graiani G, Scopece A, Cavalli S et al. Abstract 3230: cardiac stromal-derived cells reveal higher proficiency to myocardial regeneration than bone marrow mesenchymal cells with identical genetic background. Circulation 2009;120:S766.
46. Rossini A, Vecellio M, Scopece A, Di Rocco G, Pompilio G, Capogrossi MC et al. Abstract 3224: MicroRNA profiling of cardiac and bone marrow stromal cells with identical genetic background reveals distinctive signatures unmodulated by differentiation stimuli. Circulation 2009;120:S764-b.
47. Boni A, Urbanek K, Nascimbene A, Hosoda T, Zheng H, Delucchi F et al. Notch1 regulates the fate of cardiac progenitor cells. Proc Natl Acad Sci USA 2008;105: 15529-15534.
48. Collesi C, Zentilin L, Sinagra G, Giacca M. Notch1 signaling stimulates proliferation of immature cardiomyocytes. J Cell Biol 2008;183:117-128.
49. Gude NA, Emmanuel G, Wu W, Cottage CT, Fischer K, Quijada P et al. Activation of Notch-mediated protective signaling in the myocardium. Circ Res 2008;102:1025-1035.
50. Rossini A, Frati C, Lagrasta C, Graiani G, Scopece A, Cavalli S et al. Human cardiac and bone marrow stromal cells exhibit distinctive properties related to their origin. Cardiovasc Res 2010;doi:10.1093/cvr/cvq290. Published online ahead of print 10 September 2010.