Human cardiac stem cells isolated from atrial appendages stably express c-kit

PLoS ONE

Volumn 6, Issue 11, 2011, Pages

  He, Jia Qiang ^a   Vu, Duc Minh ^a   Hunt, Greg ^a   Chugh, Atul ^a   Bhatnagar, Aruni ^a   Bolli, Roberto ^a  

^a University of Louisville School of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD133 ANTIGEN; CD31 ANTIGEN; CD34 ANTIGEN; CD45 ANTIGEN; STEM CELL FACTOR; VASCULOTROPIN RECEPTOR 2; AZACITIDINE; BIOLOGICAL MARKER; STEM CELL FACTOR RECEPTOR; TRANSCRIPTION FACTOR;

ARTICLE; CELL DIFFERENTIATION; CELL ISOLATION; CELL LINEAGE; CELL SELECTION; CONTROLLED STUDY; DISSOCIATION; HEART ATRIUM APPENDAGE; HEART INFARCTION; HEART MUSCLE CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; STEM CELL; ANTIBODY SPECIFICITY; CELL SEPARATION; CYTOLOGY; DRUG EFFECT; ENDOTHELIUM CELL; FIBROBLAST; FLOW CYTOMETRY; HEART MUSCLE; HEMATOPOIETIC STEM CELL; MAGNETISM; MAST CELL; METABOLISM; METHODOLOGY; STAINING;

ANTIBODY SPECIFICITY; ATRIAL APPENDAGE; AZACITIDINE; BIOLOGICAL MARKERS; CELL DIFFERENTIATION; CELL LINEAGE; CELL SEPARATION; ENDOTHELIAL CELLS; FIBROBLASTS; FLOW CYTOMETRY; HEMATOPOIETIC STEM CELLS; HUMANS; MAGNETICS; MAST CELLS; MYOCARDIUM; PROTO-ONCOGENE PROTEINS C-KIT; STAINING AND LABELING; STEM CELLS; TRANSCRIPTION FACTORS;

EID: 82155181992     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0027719     Document Type: Article

References (72)

1. Beltrami AP, Barlucchi L, Torella D, Baker M, Limana F, et al. (2003) Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell 114: 763-776.
2. Matsuura K, Yoshioka S, Tosha T, Hori H, Ishimori K, et al. (2005) Structural diversities of active site in clinical azole-bound forms between sterol 14alpha-demethylases (CYP51s) from human and Mycobacterium tuberculosis. J Biol Chem 280: 9088-9096.
3. Matsuura K, Nagai T, Nishigaki N, Oyama T, Nishi J, et al. (2004) Adult cardiac Sca-1-positive cells differentiate into beating cardiomyocytes. J Biol Chem 279: 11384-11391.
4. Oh H, Bradfute SB, Gallardo TD, Nakamura T, Gaussin V, et al. (2003) Cardiac progenitor cells from adult myocardium: homing, differentiation, and fusion after infarction. Proc Natl Acad Sci U S A 100: 12313-12318.
5. Laugwitz KL, Moretti A, Lam J, Gruber P, Chen Y, et al. (2005) Postnatal isl1+ cardioblasts enter fully differentiated cardiomyocyte lineages. Nature 433: 647-653.
6. Bu L, Jiang X, Martin-Puig S, Caron L, Zhu S, et al. (2009) Human ISL1 heart progenitors generate diverse multipotent cardiovascular cell lineages. Nature 460: 113-117.
7. Pfister O, Mouquet F, Jain M, Summer R, Helmes M, et al. (2005) CD31- but Not CD31+ cardiac side population cells exhibit functional cardiomyogenic differentiation. Circ Res 97: 52-61.
8. Hierlihy AM, Seale P, Lobe CG, Rudnicki MA, Megeney LA, (2002) The post-natal heart contains a myocardial stem cell population. FEBS Lett 530: 239-243.
9. Messina E, De AL, Frati G, Morrone S, Chimenti S, et al. (2004) Isolation and expansion of adult cardiac stem cells from human and murine heart. Circ Res 95: 911-921.
10. Johnston PV, Sasano T, Mills K, Evers R, Lee ST, et al. (2009) Engraftment, differentiation, and functional benefits of autologous cardiosphere-derived cells in porcine ischemic cardiomyopathy. Circulation 120: 1075-1083.
11. Li TS, Cheng K, Lee ST, Matsushita S, Davis D, et al. (2010) Cardiospheres recapitulate a niche-like microenvironment rich in stemness and cell-matrix interactions, rationalizing their enhanced functional potency for myocardial repair. Stem Cells 28: 2088-2098.
12. Bearzi C, Rota M, Hosoda T, Tillmanns J, Nascimbene A, et al. (2007) Human cardiac stem cells. Proc Natl Acad Sci U S A 104: 14068-14073.
13. Barile L, Chimenti I, Gaetani R, Forte E, Miraldi F, et al. (2007) Cardiac stem cells: isolation, expansion and experimental use for myocardial regeneration. Nat Clin Pract Cardiovasc Med 4 (Suppl 1): S9-S14.
14. Bolli P, Chaudhry HW, (2010) Molecular physiology of cardiac regeneration. Ann N Y Acad Sci 1211: 113-126.
15. Bollini S, Smart N, Riley PR, (2011) Resident cardiac progenitor cells: At the heart of regeneration. J Mol Cell Cardiol 50: 296-303.
16. Kuhn EN, Wu SM, (2010) Origin of cardiac progenitor cells in the developing and postnatal heart. J Cell Physiol 225: 321-325.
17. Cai CL, Martin JC, Sun Y, Cui L, Wang L, et al. (2008) A myocardial lineage derives from Tbx18 epicardial cells. Nature 454: 104-108.
18. Kostin S, Popescu LM, (2009) A distinct type of cell in myocardium: interstitial Cajal-like cells (ICLCs). J Cell Mol Med 13: 295-308.
19. Gittenberger-de Groot AC, Winter EM, Poelmann RE, (2010) Epicardium-derived cells (EPDCs) in development, cardiac disease and repair of ischemia. J Cell Mol Med 14: 1056-1060.
20. Ellison GM, Galuppo V, Vicinanza C, Aquila I, Waring CD, et al. (2010) Cardiac stem and progenitor cell identification: different markers for the same cell? Front Biosci (Schol Ed) 2: 641-652.
21. Bollini S, Smart N, Riley PR, (2010) Resident Cardiac Progenitor Cells: At the Heart of Regeneration. J Mol Cell Cardiol 50: 296-303.
22. Itzhaki-Alfia A, Leor J, Raanani E, Sternik L, Spiegelstein D, et al. (2009) Patient characteristics and cell source determine the number of isolated human cardiac progenitor cells. Circulation 120: 2559-2566.
23. Mishra R, Vijayan K, Colletti EJ, Harrington DA, Matthiesen TS, et al. (2011) Characterization and functionality of cardiac progenitor cells in congenital heart patients. Circulation 123: 364-373.
24. Smith RR, Barile L, Cho HC, Leppo MK, Hare JM, et al. (2007) Regenerative potential of cardiosphere-derived cells expanded from percutaneous endomyocardial biopsy specimens. Circulation 115: 896-908.
25. Chimenti I, Gaetani R, Barile L, Frati G, Messina E, et al. (2009) c-kit cardiac progenitor cells: what is their potential? Proc Natl Acad Sci U S A 106: E78.
26. Tang XL, Rokosh G, Sanganalmath SK, Yuan F, Sato H, et al. (2010) Intracoronary administration of cardiac progenitor cells alleviates left ventricular dysfunction in rats with a 30-day-old infarction. Circulation 121: 293-305.
27. Lovell MJ, Mathur A, (2010) Cardiac stem cell therapy: progress from the bench to bedside. Heart 96: 1531-1537.
28. Guan K, Hasenfuss G, (2007) Do stem cells in the heart truly differentiate into cardiomyocytes? J Mol Cell Cardiol 43: 377-387.
29. Davis DR, Zhang Y, Smith RR, Cheng K, Terrovitis J, et al. (2009) Validation of the cardiosphere method to culture cardiac progenitor cells from myocardial tissue. PLoS One 4: e7195-e7122.
30. Andersen DC, Andersen P, Schneider M, Jensen HB, Sheikh SP, (2009) Murine "cardiospheres" are not a source of stem cells with cardiomyogenic potential. Stem Cells 27: 1571-1581.
31. Katayama N, Shih JP, Nishikawa S, Kina T, Clark SC, et al. (1993) Stage-specific expression of c-kit protein by murine hematopoietic progenitors. Blood 82: 2353-2360.
32. Sandstedt J, Jonsson M, Lindahl A, Jeppsson A, Asp J, (2010) C-kit+ CD45- cells found in the adult human heart represent a population of endothelial progenitor cells. Basic Res Cardiol 105: 545-556.
33. Sperr WR, Bankl HC, Mundigler G, Klappacher G, Grossschmidt K, et al. (1994) The human cardiac mast cell: localization, isolation, phenotype, and functional characterization. Blood 84: 3876-3884.
34. Zhou Y, Pan P, Yao L, Su M, He P, et al. (2010) CD117-positive cells of the heart: progenitor cells or mast cells? J Histochem Cytochem 58: 309-316.
35. Boni A, Urbanek K, Nascimbene A, Hosoda T, Zheng H, et al. (2008) Notch1 regulates the fate of cardiac progenitor cells. Proc Natl Acad Sci U S A 105: 15529-15534.
36. D'Amario D, Fiorini C, Campbell PM, Goichberg P, Sanada F, et al. (2011) Functionally competent cardiac stem cells can be isolated from endomyocardial biopsies of patients with advanced cardiomyopathies. Circ Res 108: 857-861.
37. Smits AM, van VP, Metz CH, Korfage T, Sluijter JP, et al. (2009) Human cardiomyocyte progenitor cells differentiate into functional mature cardiomyocytes: an in vitro model for studying human cardiac physiology and pathophysiology. Nat Protoc 4: 232-243.
38. Kondo M, Weissman IL, Akashi K, (1997) Identification of clonogenic common lymphoid progenitors in mouse bone marrow. Cell 91: 661-672.
39. Fajtova M, Babusikova O, (2010) Immunophenotype characterization of hematopoietic stem cells, progenitor cells restricted to myeloid lineage and their leukemia counterparts. Neoplasma 57: 392-400.
40. Zeisberg EM, Kalluri R, (2010) Origins of cardiac fibroblasts. Circ Res 107: 1304-1312.
41. Singer KH, Scearce RM, Tuck DT, Whichard LP, Denning SM, et al. (1989) Removal of fibroblasts from human epithelial cell cultures with use of a complement fixing monoclonal antibody reactive with human fibroblasts and monocytes/macrophages. J Invest Dermatol 92: 166-170.
42. Esterre P, Melin M, Serrar M, Grimaud JA, (1992) New specific markers of human and mouse fibroblasts. Cell Mol Biol 38: 297-301.
43. Ronnov-Jessen L, Celis JE, Van DB, Petersen OW, (1992) A fibroblast-associated antigen: characterization in fibroblasts and immunoreactivity in smooth muscle differentiated stromal cells. J Histochem Cytochem 40: 475-486.
44. Strutz F, Okada H, Lo CW, Danoff T, Carone RL, et al. (1995) Identification and characterization of a fibroblast marker: FSP1. J Cell Biol 130: 393-405.
45. Genovese A, Rossi FW, Spadaro G, Galdiero MR, Marone G, (2010) Human cardiac mast cells in anaphylaxis. Chem Immunol Allergy 95: 98-109.
46. Reid AC, Silver RB, Levi R, (2007) Renin: at the heart of the mast cell. Immunol Rev 217: 123-140.
47. van VP, Sluijter JP, Doevendans PA, Goumans MJ, (2007) Isolation and expansion of resident cardiac progenitor cells. Expert Rev Cardiovasc Ther 5: 33-43.
48. Camelliti P, Borg TK, Kohl P, (2005) Structural and functional characterisation of cardiac fibroblasts. Cardiovasc Res 65: 40-51.
49. Anversa P, Kajstura J, Leri A, Bolli R, (2006) Life and death of cardiac stem cells: a paradigm shift in cardiac biology. Circulation 113: 1451-1463.
50. D'Alessandro DA, Kajstura J, Hosoda T, Gatti A, Bello R, et al. (2009) Progenitor cells from the explanted heart generate immunocompatible myocardium within the transplanted donor heart. Circ Res 105: 1128-1140.
51. Barile L, Messina E, Giacomello A, Marban E, (2007) Endogenous cardiac stem cells. Prog Cardiovasc Dis 50: 31-48.
52. Smith RR, Barile L, Messina E, Marban E, (2008) Stem cells in the heart: what's the buzz all about? Part 2: Arrhythmic risks and clinical studies. Heart Rhythm 5: 880-887.
53. Smith RR, Barile L, Messina E, Marban E, (2008) Stem cells in the heart: what's the buzz all about?-Part 1: preclinical considerations. Heart Rhythm 5: 749-757.
54. Wu JC, Abraham MR, Kraitchman DL, (2010) Current perspectives on imaging cardiac stem cell therapy. J Nucl Med 51 (Suppl 1): 128S-136S.
55. Davis DR, Kizana E, Terrovitis J, Barth AS, Zhang Y, et al. (2010) Isolation and expansion of functionally-competent cardiac progenitor cells directly from heart biopsies. J Mol Cell Cardiol 49: 312-321.
56. Muta K, Krantz SB, Bondurant MC, Dai CH, (1995) Stem cell factor retards differentiation of normal human erythroid progenitor cells while stimulating proliferation. Blood 86: 572-580.
57. Kashiwakura I, Takahashi TA, (2003) Basic fibroblast growth factor-stimulated ex vivo expansion of haematopoietic progenitor cells from human placental and umbilical cord blood. Br J Haematol 122: 479-488.
58. Yeoh JS, de HG, (2007) Fibroblast growth factors as regulators of stem cell self-renewal and aging. Mech Ageing Dev 128: 17-24.
59. Bailey B, Izarra A, Alvarez R, Fischer KM, Cottage CT, et al. (2009) Cardiac stem cell genetic engineering using the alphaMHC promoter. Regen Med 4: 823-833.
60. Cottage CT, Bailey B, Fischer KM, Avitable D, Collins B, et al. (2010) Cardiac progenitor cell cycling stimulated by pim-1 kinase. Circ Res 106: 891-901.
61. Linke A, Muller P, Nurzynska D, Casarsa C, Torella D, et al. (2005) 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: 8966-8971.
62. Hatzistergos KE, Quevedo H, Oskouei BN, Hu Q, Feigenbaum GS, et al. (2010) Bone Marrow Mesenchymal Stem Cells Stimulate Cardiac Stem Cell Proliferation and Differentiation. Circ Res 107: 913-922.
63. Orlic D, Fischer R, Nishikawa S, Nienhuis AW, Bodine DM, (1993) Purification and characterization of heterogeneous pluripotent hematopoietic stem cell populations expressing high levels of c-kit receptor. Blood 82: 762-770.
64. Orlic D, Kajstura J, Chimenti S, Bodine DM, Leri A, et al. (2001) Transplanted adult bone marrow cells repair myocardial infarcts in mice. Ann N Y Acad Sci 938: 221-229.
65. Monsel G, Ortonne N, Bagot M, Bensussan A, Dumaz N, (2010) c-Kit mutants require hypoxia-inducible factor 1alpha to transform melanocytes. Oncogene 29: 227-236.
66. Leong KG, Wang BE, Johnson L, Gao WQ, (2008) Generation of a prostate from a single adult stem cell. Nature 456: 804-808.
67. Miettinen M, Lasota J, (2005) KIT (CD117): a review on expression in normal and neoplastic tissues, and mutations and their clinicopathologic correlation. Appl Immunohistochem Mol Morphol 13: 205-220.
68. Meuser-Batista M, Correa JR, Soares MJ, Henriques-Pons A, (2008) Isolation of cardiac mast cells in experimental Trypanosoma cruzi infection. Tissue Cell 40: 309-316.
69. Mouquet F, Pfister O, Jain M, Oikonomopoulos A, Ngoy S, et al. (2005) Restoration of cardiac progenitor cells after myocardial infarction by self-proliferation and selective homing of bone marrow-derived stem cells. Circ Res 97: 1090-1092.
70. Pfister O, Oikonomopoulos A, Sereti KI, Sohn RL, Cullen D, et al. (2008) Role of the ATP-binding cassette transporter Abcg2 in the phenotype and function of cardiac side population cells. Circ Res 103: 825-835.
71. Rota M, Lecapitaine N, Hosoda T, Boni A, De AA, et al. (2006) Diabetes promotes cardiac stem cell aging and heart failure, which are prevented by deletion of the p66shc gene. Circ Res 99: 42-52.
72. Bearzi C, Leri A, Lo MF, Rota M, Gonzalez A, et al. (2009) Identification of a coronary vascular progenitor cell in the human heart. Proc Natl Acad Sci U S A 106: 15885-15890.