Multipotent stem cells of the heart-do they have therapeutic promise?

Frontiers in Physiology

Volumn 6, Issue MAY, 2015, Pages

  Leite, Camila F ^a   Almeida, Thalles R ^a   Lopes, Carolina S ^a   Dias da Silva, Valdo J ^a  

^a Triangulo Mineiro Federal University   (Brazil)

Author keywords

Cardiac homeostasis; Cardiac remodeling; Cardiac stem cells; Cell therapy; Regenerative process

Indexed keywords

PLACEBO; STEM CELL ANTIGEN 1; STEM CELL FACTOR RECEPTOR;

ACUTE HEART FAILURE; CARDIAC STEM CELL; CARDIAC STEM CELL TRANSPLANTATION; CARDIOMYOPATHY; CARDIOSPHERE DERIVED STEM CELL; CARDIOSPHERE DERIVED STEM CELL TRANSPLANTATION; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CELL TRANSDIFFERENTIATION; ENDOTHELIUM CELL; HEART DEVELOPMENT; HEART FAILURE; HEART INFARCTION; HEART INJURY; HEMATOPOIETIC STEM CELL; HUMAN; ISCHEMIC CARDIOMYOPATHY; MESENCHYMAL STEM CELL; MESENCHYMAL STEM CELL TRANSPLANTATION; MULTIPOTENT STEM CELL; MUSCLE CELL; NONHUMAN; REVIEW; SIDE POPULATION CELL; SMOOTH MUSCLE FIBER; STEM CELL TRANSPLANTATION; THERAPY EFFECT; TISSUE REGENERATION;

EID: 84930658204     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphar.2015.00123     Document Type: Review

References (125)

1. Aicher, A., Rentsch, M., Sasaki, K., Ellwart, J. W., Fändrich, F., Siebert, R., et al. (2007). Nonbone marrow-derived circulating progenitor cells contribute to postnatal neovascularization following tissue ischemia. Circ. Res. 100, 581-589. doi: 10.1161/01.RES.0000259562.63718.35.
2. Allen, L. A., Stevenson, L. W., Grady, K. L., Goldstein, N. E., Matlock, D. D., Arnold, R. M., et al. (2012). Decision making in advanced heart failure: a scientific statement from the American Heart Association. Circulation 125, 1928-1952. doi: 10.1161/CIR.0b013e31824f2173.
3. Aminzadeh, M. A., Tseliou, E., Sun, B., Cheng, K., Malliaras, K., Makkar, R. R., et al. (2015). Therapeutic efficacy of cardiosphere-derived cells in a transgenic mouse model of non-ischaemic dilated cardiomyopathy. Eur. Heart J. 36, 751-762. doi: 10.1093/eurheartj/ehu196.
4. Angelini, A., Castellani, C., Tona, F., Gambino, A., Caforio, A. P., Feltrin, G., et al. (2007). Continuous engraftment and differentiation of male recipient Y-chromosome-positive cardiomyocytes in donor female human heart transplants. J. Heart Lung Transplant. 26, 1110-1118. doi: 10.1016/j.healun.2007.08.004.
5. Anversa, P., and Kajstura, J. (1998). Ventricular myocytes are not terminally differentiated in the adult mammalian heart. Circ. Res. 83, 1-14. doi: 10.1161/01.RES.83.1.1.
6. Bailey, B., Izarra, A., Alvarez, R., Fischer, K. M., Cottage, C. T., Quijada, P., et al. (2009). Cardiac stem cell genetic engineering using the alphaMHC promoter. Regen. Med. 4, 823-833. doi: 10.2217/rme.09.51.
7. Balsam, L. B., Wagers, A. J., and Christensen, J. L. (2004). Haematopoietic stem cells adopt mature haematopoietic fates in ischaemic myocardium. Nature 428, 668-673. doi: 10.1038/nature02460.
8. Barile, L., Messina, E., Giacomello, A., and Marbán, E. (2007). Endogenous cardiac stem cells. Prog. Cardiovasc. Dis. 50, 31-48. doi: 10.1016/j.pcad.2007.03.005.
9. Bearzi, C., Rota, M., Hosoda, T., Tillmanns, J., Nascimbene, A., De Angelis, A., et al. (2007). Human cardiac stem cells. Proc. Natl. Acad. Sci. U.S.A. 104, 14068-14073. doi: 10.1073/pnas.0706760104.
10. Beltrami, A. P., Barlucchi, L., Torella, D., Baker, M., Limana, F., Chimenti, S., et al. (2003). Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell 114, 763-776. doi: 10.1016/S0092-8674(03)00687-1.
11. Beltrami, A. P., Urbanek, K., Kajstura, J., Yan, S. M., Finato, N., Bussani, R., et al. (2001). Evidence that human cardiac myocytes divide after myocardial infarction. N. Engl. J. Med. 344, 1750-1757. doi: 10.1056/NEJM200106073442303.
12. Bergmann, O., Bhardwaj, R. D., Bernard, S., Zdunek, S., Barnabé-Heide, F., Walsh, S., et al. (2010). Evidence for cardiomyocyte renewal in humans. Science 324, 98-102. doi: 10.1126/science.1164680.
13. Bersell, K., Arab, S., Haring, B., and Kühn, B. (2009). Neuregulin1/ErbB4 signaling induces cardiomyocyte proliferation and repair of heart injury. Cell 138, 257-270. doi: 10.1016/j.cell.2009.04.060.
14. Bian, S., Zhang, L., Duan, L., Wang, X., Min, Y., and Yu, H. (2014). Extracellular vesicles derived from human bone marrow mesenchymal stem cells promote angiogenesis in a rat myocardial infarction model. J. Mol. Med. (Berl). 92, 387-397. doi: 10.1007/s00109-013-1110-5.
15. Biancone, L., Bruno, S., Deregibus, M. C., Tetta, C., and Camussi, G. (2012). Therapeutic potential of mesenchymal stem cell-derived microvesicles. Nephrol. Dial. Transplant. 27, 3037-3042. doi: 10.1093/ndt/gfs168.
16. Bolli, R., Chugh, A. R., D'Amario, D., Loughran, J. H., Stoddard, M. F., Ikram, S., et al. (2011). Cardiac stem cells in patients with ischaemic cardiomyopathy (SCIPIO): initial results of a randomised phase 1 trial. Lancet 378, 1847-1857. doi: 10.1016/S0140-6736(11)61590-0.
17. Cagavi, E., Bartulos, O., Suh, C. Y., Sun, B., Yue, Z., Jiang, Z., et al. (2014). Functional cardiomyocytes derived from Isl1 cardiac progenitors via Bmp4 stimulation. PLoS ONE 9:e110752. doi: 10.1371/journal.pone.0110752.
18. Cesselli, D., Beltrami, A. P., D'Aurizio, F., Marcon, P., Bergamin, N., Toffoletto, B., et al. (2011). Effects of age and heart failure on human cardiac stem cell function. Am. J. Pathol. 179, 349-366. doi: 10.1016/j.ajpath.2011.03.036.
19. Chan, S. S.-K., Shueh, Y.-Z., Liu, Y.-W., and Hsieh, P. C. H. (2009). Harnessing endogenous intra-and extra-cardiac stem cells for cardiac regeneration-hope or hype? Drug Discov. Today Ther. Strateg. 6, 127-133. doi: 10.1016/j.ddstr.2009.06.004.
20. Chen, Z., Pan, X., Yao, Y., Yan, F., Chen, L., Huang, R., et al. (2013). Epigenetic regulation of cardiac progenitor cells marker c-kit by stromal cell derived factor-1a. PLoS ONE 8:e69134. doi: 10.1371/journal.pone.0069134.
21. Cheng, K., Ibrahim, A., Hensley, M. T., Shen, D., Sun, B., Middleton, R., et al. (2014). Relative roles of CD90 and c-kit to the regenerative efficacy of cardiosphere-derived cells in humans and in a mouse model of myocardial infarction. J. Am. Heart Assoc. 3:e001260. doi: 10.1161/JAHA.114.001260.
22. Chimenti, C., Kajstura, J., Torella, D., Urbanek, K., Heleniak, H., Colussi, C., et al. (2003). Senescence and death of primitive cells and myocytes lead to premature cardiac aging and heart failure. Circ. Res. 93, 604-613. doi: 10.1161/01.RES.0000093985.76901.AF.
23. Cho, D.-I., Kim, M. R., Jeong, H., Jeong, H. C., Jeong, M. H., Yoon, S. H., et al. (2014). Mesenchymal stem cells reciprocally regulate the M1/M2 balance in mouse bone marrow-derived macrophages. Exp. Mol. Med. 46:e70. doi: 10.1038/emm.2013.135.
24. Cho, H.-J., Lee, N., Lee, J. Y., Choi, Y. J., Ii, M., Wecker, A., et al. (2007). Role of host tissues for sustained humoral effects after endothelial progenitor cell transplantation into the ischemic heart. J. Exp. Med. 204, 3257-3269. doi: 10.1084/jem.20070166.
25. Chong, J. J. H., Chandrakanthan, V., Xaymardan, M., Asli, N. S., Li, J., Ahmed, I., et al. (2011). Adult cardiac-resident MSC-like stem cells with a proepicardial origin. Cell Stem Cell 9, 527-540. doi: 10.1016/j.stem.2011.10.002.
26. Chugh, A. R., Beache, G. M., Loughran, J. H., Mewton, N., Elmore, J. B., Kajstura, J., et al. (2012). Administration of cardiac stem cells in patients with ischemic cardiomyopathy: the SCIPIO trial: surgical aspects and interim analysis of myocardial function and viability by magnetic resonance. Circulation 126, S54-S64. doi: 10.1161/CIRCULATIONAHA.112.092627.
27. Cieslik, K. A., Trial, J., Carlson, S., Taffet, G. E., and Entman, M. L. (2013). Aberrant differentiation of fibroblast progenitors contributes to fibrosis in the aged murine heart: role of elevated circulating insulin levels. FASEB J. 27, 1761-1771. doi: 10.1096/fj.12-220145.
28. Cieslik, K. A., Trial, J., and Entman, M. L. (2011). Defective myofibroblast formation from mesenchymal stem cells in the aging murine heart rescue by activation of the AMPK pathway. Am. J. Pathol. 179, 1792-1806. doi: 10.1016/j.ajpath.2011.06.022.
29. Crisostomo, V., Casado, J. G., Baez-Diaz, C., Blazquez, R., and Sanchez-Margallo, F. M. (2015). Allogeneic cardiac stem cell administration for acute myocardial infarction. Expert Rev. Cardiovasc. Ther. 13, 285-299. doi: 10.1586/14779072.2015.1011621.
30. Curtis, M. W., and Russell, B. (2010). Cardiac tissue engineering. J. Cardiovasc. Nurs. 24, 87-92. doi: 10.1097/01.JCN.0000343562.06614.49.
31. da Silva Meirelles, L., Chagastelles, P. C., and Nardi, N. B. (2006). Mesenchymal stem cells reside in virtually all post-natal organs and tissues. J. Cell Sci. 119, 2204-2213. doi: 10.1242/jcs.02932.
32. De Angelis, A., Piegari, E., Cappetta, D., Marino, L., Filippelli, A., Berrino, L., et al. (2010). Anthracycline cardiomyopathy is mediated by depletion of the cardiac stem cell pool and is rescued by restoration of progenitor cell function. Circulation 121, 276-292. doi: 10.1161/CIRCULATIONAHA.109.895771.
33. Delucchi, F., Berni, R., Frati, C., Cavalli, S., Graiani, G., Sala, R., et al. (2012). Resveratrol treatment reduces cardiac progenitor cell dysfunction and prevents morpho-functional ventricular remodeling in type-1 diabetic rats. PLoS ONE 7:e39836. doi: 10.1371/journal.pone.0039836.
34. Dey, D., Han, L., Bauer, M., Sanada, F., Oikonomopoulos, A., Hosoda, T., et al. (2013). Dissecting the molecular relationship among various cardiogenic progenitor cells. Circ. Res. 112, 1253-1262. doi: 10.1161/CIRCRESAHA.112.300779.
35. Di Felice, V., De Luca, A., Colorito, M. L., Montalbano, A., Ardizzone, N. M., Macaluso, F., et al. (2009). Cardiac stem cell research: an elephant in the room? Anat. Rec. (Hoboken). 292, 449-454. doi: 10.1002/ar.20858.
36. Dominici, M., Le Blanc, K., Mueller, I., Slaper-Cortenbach, I., Marini, F., Krause, D., et al. (2006). Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8, 315-317. doi: 10.1080/14653240600855905.
37. Eggenhofer, E., Luk, F., Dahlke, M. H., and Hoogduijn, M. J. (2014). The life and fate of mesenchymal stem cells. Front. Immunol. 5:148. doi: 10.3389/fimmu.2014.00148.
38. Ellison, G. M., Vicinanza, C., Smith, A. J., Aquila, I., Leone, A., Waring, C. D., et al. (2013). Adult c-kit(pos) cardiac stem cells are necessary and sufficient for functional cardiac regeneration and repair. Cell 154, 827-842. doi: 10.1016/j.cell.2013.07.039.
39. Ellison, G. M., Waring, C. D., Vicinanza, C., and Torella, D. (2012). Physiological cardiac remodelling in response to endurance exercise training: cellular and molecular mechanisms. Heart 98, 5-10. doi: 10.1136/heartjnl-2011-300639.
40. Fang, S., Wei, J., Pentinmikko, N., Leinonen, H., and Salven, P. (2012). Generation of functional blood vessels from a single c-kit+ adult vascular endothelial stem cell. PLoS Biol. 10:e1001407. doi: 10.1371/journal.pbio.1001407.
41. Fazel, S. S., Chen, L., Angoulvant, D., Li, S.-H., Weisel, R. D., Keating, A., et al. (2008). Activation of c-kit is necessary for mobilization of reparative bone marrow progenitor cells in response to cardiac injury. FASEB J. 22, 930-940. doi: 10.1096/fj.07-8636com.
42. Ferreira-Martins, J., Ogórek, B., Cappetta, D., Matsuda, A., Signore, S., D'Amario, D., et al. (2012). Cardiomyogenesis in the developing heart is regulated by c-kit-positive cardiac stem cells. Circ. Res. 110, 701-715. doi: 10.1161/01.res.0000437785.32637.a2.
43. Fioret, B. A., Heimfeld, J. D., Paik, D. T., and Hatzopoulos, A. K. (2014). Endothelial cells contribute to generation of adult ventricular myocytes during cardiac homeostasis. Cell Rep. 8, 229-241. doi: 10.1016/j.celrep.2014.06.004.
44. Friedenstein, A. J., Chailakhyan, R. K., Latsinik, N. V., Panasyuk, A. F., and Keiliss-Borok, I. V. (1974). Stromal cells responsible for transferring the microenvironment of the hemopoietic tissues. Cloning in vitro and retransplantation in vivo. Transplantation 17, 331-340. doi: 10.1097/00007890-197404000-00001.
45. Fuentes, T. I., Appleby, N., Tsay, E., Martinez, J. J., Bailey, L., Hasaniya, N., et al. (2013). Human neonatal cardiovascular progenitors: unlocking the secret to regenerative ability. PLoS ONE 8:e77464. doi: 10.1371/journal.pone.0077464.
46. Gaetani, R., Ledda, M., Barile, L., Chimenti, I., De Carlo, F., Forte, E., et al. (2009). Differentiation of human adult cardiac stem cells exposed to extremely low-frequency electromagnetic fields. Cardiovasc. Res. 82, 411-420. doi: 10.1093/cvr/cvp067.
47. Gambini, E., Pompilio, G., Biondi, A., Alamanni, F., Capogrossi, M. C., Agrifoglio, M., et al. (2011). C-kit+ cardiac progenitors exhibit mesenchymal markers and preferential cardiovascular commitment. Cardiovasc. Res. 89, 362-373. doi: 10.1093/cvr/cvq292.
48. Gnecchi, M., Zhang, Z., Ni, A., and Dzau, V. J. (2008). Paracrine mechanisms in adult stem cell signaling and therapy. Circ. Res. 103, 1204-1219. doi: 10.1161/CIRCRESAHA.108.176826.
49. Go, A. S., Mozaffarian, D., Roger, V. L., Benjamin, E. J., Berry, J. D., Blaha, M. J., et al. (2014). Heart disease and stroke statistics-2014 update: a report from the American Heart Association. Circulation 129, e28-e292. doi: 10.1161/01.cir.0000441139.02102.80.
50. Go, A. S., Mozaffarian, D., Roger, V. L., Benjamin, E. J., Berry, J. D., Borden, W. B., et al. (2013). Heart disease and stroke statistics-2013 update: a report from the American Heart Association. Circulation 127, e6-e245. doi: 10.1161/CIR.0b013e318282ab8f.
51. Gussoni, E., Soneoka, Y., Strickland, C. D., Buzney, E. A., Khan, M. K., Flint, A. F., et al. (1999). Dystrophin expression in the mdx mouse restored by stem cell transplantation. Nature 401, 390-394. doi: 10.1038/43919.
52. Hallas, C. N., Wray, J., Andreou, P., and Banner, N. R. (2011). Depression and perceptions about heart failure predict quality of life in patients with advanced heart failure. Heart Lung 40, 111-121. doi: 10.1016/j.hrtlng.2009.12.008.
53. Hare, J. M., Fishman, J. E., Gerstenblith, G., DiFede Velazquez, D. L., Zambrano, J. P., Suncion, V. Y., et al. (2012). Comparison of allogeneic vs autologous bone marrow-derived mesenchymal stem cells delivered by transendocardial injection in patients with ischemic cardiomyopathy: the POSEIDON randomized trial. JAMA 308, 2369-2379. doi: 10.1001/jama.2012.25321.
54. Hatzistergos, K. E., Quevedo, H., Oskouei, B. N., Hu, Q., Feigenbaum, G. S., Margitich, I. S., et al. (2010). Bone marrow mesenchymal stem cells stimulate cardiac stem cell proliferation and differentiation. Circ. Res. 107, 913-922. doi: 10.1161/CIRCRESAHA.110.222703.
55. Heissig, B., Hattori, K., Dias, S., Friedrich, M., Ferris, B., Hackett, N. R., et al. (2002). Recruitment of stem and progenitor cells from the bone marrow niche requires MMP-9 mediated release of kit-ligand. Cell 109, 625-637. doi: 10.1016/S0092-8674(02)00754-7.
56. Hellermann, J. P., Jacobsen, S. J., Gersh, B. J., Rodeheffer, R. J., Reeder, G. S., and Roger, V. L. (2002). Heart failure after myocardial infarction: a review. Am. J. Med. 113, 324-330. doi: 10.1016/S0002-9343(02)01185-3.
57. Hierlihy, A. M., Seale, P., Lobe, C. G., Rudnicki, M. A., and Megeney, L. A. (2002). The post-natal heart contains a myocardial stem cell population. FEBS Lett. 530, 239-243. doi: 10.1016/S0014-5793(02)03477-4.
58. Holmes, C., and Stanford, W. L. (2007). Concise review: stem cell antigen-1: expression, function, and enigma. Stem Cells 25, 1339-1347. doi: 10.1634/stemcells.2006-0644.
59. Hoshino, K., Ly, H. Q., Frangioni, J. V., and Hajjar, R. J. (2007). In vivo tracking in cardiac stem cell-based therapy. Prog. Cardiovasc. Dis. 49, 414-420. doi: 10.1016/j.pcad.2007.02.005.
60. Javazon, E. H., Beggs, K. J., and Flake, A. W. (2004). Mesenchymal stem cells: paradoxes of passaging. Exp. Hematol. 32, 414-425. doi: 10.1016/j.exphem.2004.02.004.
61. Jiang, X.-X., Zhang, Y., Liu, B., Zhang, S.-X., Wu, Y., Yu, X.-D., et al. (2005). Human mesenchymal stem cells inhibit differentiation and function of monocyte-derived dendritic cells. Blood 105, 4120-4126. doi: 10.1182/blood-2004-02-0586.
62. Kajstura, J., Gurusamy, N., Ogórek, B., Goichberg, P., Clavo-Rondon, C., Hosoda, T., et al. (2010a). Myocyte turnover in the aging human heart. Circ. Res. 107, 1374-1386. doi: 10.1161/CIRCRESAHA.110.231498.
63. Kajstura, J., Urbanek, K., Perl, S., Hosoda, T., Zheng, H., Ogórek, B., et al. (2010b). Cardiomyogenesis in the adult human heart. Circ. Res. 107, 305-315. doi: 10.1161/CIRCRESAHA.110.223024.
64. Kern, S., Eichler, H., Stoeve, J., Klüter, H., and Bieback, K. (2006). Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue. Stem Cells 24, 1294-1301. doi: 10.1634/stemcells.2005-0342.
65. Khan, M., Mohsin, S., Avitabile, D., Siddiqi, S., Nguyen, J., Wallach, K., et al. (2013). β-Adrenergic regulation of cardiac progenitor cell death versus survival and proliferation. Circ. Res. 112, 476-486. doi: 10.1161/CIRCRESAHA.112.280735.
66. Laflamme, M. A. (2002). Evidence for cardiomyocyte repopulation by extracardiac progenitors in transplanted human hearts. Circ. Res. 90, 634-640. doi: 10.1161/01.RES.0000014822.62629.EB.
67. Laugwitz, K.-L., Moretti, A., Lam, J., Gruber, P., Chen, Y., Woodard, S., et al. (2005). Postnatal isl1+ cardioblasts enter fully differentiated cardiomyocyte lineages. Nature 433, 647-653. doi: 10.1038/nature03215.
68. Le Blanc, K., and Ringdén, O. (2005). Immunobiology of human mesenchymal stem cells and future use in hematopoietic stem cell transplantation. Biol. Blood Marrow Transplant. 11, 321-334. doi: 10.1016/j.bbmt.2005.01.005.
69. Leri, A. (2009). Human cardiac stem cells: the heart of a truth. Circulation 120, 2515-2518. doi: 10.1161/CIRCULATIONAHA.109.911107.
70. Leri, A., Kajstura, J., and Anversa, P. (2005). Cardiac stem cells and mechanisms of myocardial regeneration. Physiol. Rev. 85, 1373-1416. doi: 10.1152/physrev.00013.2005.
71. Li, T.-S., Cheng, K., Lee, S.-T., Matsushita, S., Davis, D., Malliaras, K., 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. doi: 10.1002/stem.532.
72. Li, T.-S., Suzuki, R., Ueda, K., Murata, T., and Hamano, K. (2007). Analysis of the origin and population dynamics of cardiac progenitor cells in a donor heart model. Stem Cells 25, 911-917. doi: 10.1634/stemcells.2006-0497.
73. Loffredo, F. S., Steinhauser, M. L., Gannon, J., and Lee, R. T. (2011). Bone marrow-derived cell therapy stimulates endogenous cardiomyocyte progenitors and promotes cardiac repair. Cell Stem Cell 8, 389-398. doi: 10.1016/j.stem.2011.02.002.
74. Lovell, M. J., and Mathur, A. (2011). Republished review: cardiac stem cell therapy: progress from the bench to bedside. Postgrad. Med. J. 87, 558-564. doi: 10.1136/pgmj.2009.192385rep.
75. Lui, K. O., Zangi, L., Silva, E. A., Bu, L., Sahara, M., Li, R. A., et al. (2013). Driving vascular endothelial cell fate of human multipotent Isl1+ heart progenitors with VEGF modified mRNA. Cell Res. 23, 1172-1186. doi: 10.1038/cr.2013.112.
76. Makkar, R. R., Smith, R. R., Cheng, K., Malliaras, K., Thomson, L. E., Berman, D., et al. (2012). Intracoronary cardiosphere-derived cells for heart regeneration after myocardial infarction (CADUCEUS): a prospective, randomised phase 1 trial. Lancet 379, 895-904. doi: 10.1016/S0140-6736(12)60195-0.
77. Malliaras, K., Makkar, R. R., Smith, R. R., Cheng, K., Wu, E., Bonow, R. O., et al. (2014). Intracoronary cardiosphere-derived cells after myocardial infarction: evidence of therapeutic regeneration in the final 1-year results of the CADUCEUS trial (CArdiosphere-Derived aUtologous stem CElls to reverse ventricUlar dySfunction). J. Am. Coll. Cardiol. 63, 110-122. doi: 10.1016/j.jacc.2013.08.724.
78. Martin, C. M., Meeson, A. P., Robertson, S. M., Hawke, T. J., Richardson, J. A., Bates, S., et al. (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. doi: 10.1016/j.ydbio.2003.09.028.
79. Matsuura, K., Nagai, T., Nishigaki, N., Oyama, T., Nishi, J., Wada, H., et al. (2004). Adult cardiac Sca-1-positive cells differentiate into beating cardiomyocytes. J. Biol. Chem. 279, 11384-11391. doi: 10.1074/jbc. M310822200.
80. Messina, E., De Angelis, L., Frati, G., Morrone, S., Chimenti, S., Fiordaliso, F., et al. (2004). Isolation and expansion of adult cardiac stem cells from human and murine heart. Circ. Res. 95, 911-921. doi: 10.1161/01.RES.0000147315.71699.51.
81. Meyer, G. P., Wollert, K. C., Lotz, J., Steffens, J., Lippolt, P., Fichtner, S., et al. (2006). 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, 1287-1294. doi: 10.1161/CIRCULATIONAHA.105.575118.
82. Miyamoto, S., Kawaguchi, N., Ellison, G. M., Matsuoka, R., Shin'oka, T., and Kurosawa, H. (2010). Characterization of long-term cultured c-kit+ cardiac stem cells derived from adult rat hearts. Stem Cells Dev. 19, 105-116. doi: 10.1089/scd.2009.0041.
83. Morita, Y., Iseki, A., Okamura, S., Suzuki, S., Nakauchi, H., and Ema, H. (2011). Functional characterization of hematopoietic stem cells in the spleen. Exp. Hematol. 39, 351.e3-359.e3. doi: 10.1016/j.exphem.2010.12.008.
84. Murry, C. E., Soonpaa, M. H., Reinecke, H., Nakajima, H., Nakajima, H. O., Rubart, M., et al. (2004). Haematopoietic stem cells do not transdifferentiate into cardiac myocytes in myocardial infarcts. Nature 428, 13-15. doi: 10.1038/nature02446.
85. Nora, C. C., Camassola, M., Bellagamba, B., Ikuta, N., Christoff, A. P., Meirelles, L. D. S., et al. (2012). Molecular analysis of the differentiation potential of murine mesenchymal stem cells from tissues of endodermal or mesodermal origin. Stem Cells Dev. 21, 1761-1768. doi: 10.1089/scd.2011.0030.
86. Noseda, M., and Schneider, M. D. (2010). Previews. Unleashing cardiopoiesis: a novel role for G-CSF. Cell Stem Cell 6, 188-189. doi: 10.1016/j.stem.2010.02.005.
87. Oh, H., Bradfute, S. B., Gallardo, T. D., Nakamura, T., Gaussin, V., Mishina, Y., 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. doi: 10.1073/pnas.2132126100.
88. Orlic, D., Kajstura, J., Chimenti, S., Jakoniuk, I., Anderson, S. M., Li, B., et al. (2001). Bone marrow cells regenerate infarcted myocardium. 410, 701-705. doi: 10.1038/35070587.
89. Prezioso, L., Tanzi, S., Galaverna, F., Frati, C., Testa, B., Savi, M., et al. (2010). Cancer treatment-induced cardiotoxicity: a cardiac stem cell disease? Cardiovasc. Hematol. Agents Med. Chem. 8, 55-75. doi: 10.2174/187152510790796165.
90. Quaini, F., Urbanek, K., Beltrami, A. P., Finato, N., Beltrami, C. A., Nadal-Ginard, B., et al. (2002). Chimerism of the transplanted heart. N. Engl. J. Med. 346, 5-15. doi: 10.1056/NEJMoa012081.
91. Raff, M. (2003). Adult stem cell plasticity: fact or artifact? Annu. Rev. Cell Dev. Biol. 19, 1-22. doi: 10.1146/annurev.cellbio.19.111301.143037.
92. Rosenblatt-velin, N., Lepore, M. G., Cartoni, C., and Beermann, F. (2005). FGF-2 controls the differentiation of resident cardiac precursors into functional cardiomyocytes. J. Clin. Invest. 115, 1724-1733. doi: 10.1172/JCI23418.
93. Rossini, A., Frati, C., Lagrasta, C., Graiani, G., Scopece, A., Cavalli, S., et al. (2011). Human cardiac and bone marrow stromal cells exhibit distinctive properties related to their origin. Cardiovasc. Res. 89, 650-660. doi: 10.1093/cvr/cvq290.
94. Rota, M., Kajstura, J., Hosoda, T., Bearzi, C., Vitale, S., Esposito, G., et al. (2007). Bone marrow cells adopt the cardiomyogenic fate in vivo. Proc. Natl. Acad. Sci. U.S.A. 104, 17783-17788. doi: 10.1073/pnas.0706406104.
95. Rota, M., LeCapitaine, N., Hosoda, T., Boni, A., De Angelis, A., Padin-Iruegas, M. E., 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. doi: 10.1161/01.RES.0000231289.63468.08.
96. Ryzhov, S., Sung, B. H., Zhang, Q., Weaver, A., Gumina, R. J., Biaggioni, I., et al. (2014). Role of adenosine A2B receptor signaling in contribution of cardiac mesenchymal stem-like cells to myocardial scar formation. Purinergic Signal. 10, 477-486. doi: 10.1007/s11302-014-9410-y.
97. Sánchez, P. L., Sanz-Ruiz, R., Fernández-Santos, M. E., and Fernández-Avilés, F. (2010). Cultured and freshly isolated adipose tissue-derived cells: fat years for cardiac stem cell therapy. Eur. Heart J. 31, 394-397. doi: 10.1093/eurheartj/ehp403.
98. Schächinger, V., Erbs, S., Elsässer, A., Haberbosch, W., Hambrecht, R., Hölschermann, H., et al. (2006). Intracoronary bone marrow-derived progenitor cells in acute myocardial infarction. N. Engl. J. Med. 355, 1210-1221. doi: 10.1056/NEJMoa060186.
99. Shah, A. P., Youngquist, S. T., McClung, C. D., Tzvetkova, E., Hanif, M. A., Rosborough, J. P., et al. (2011). Markers of progenitor cell recruitment and differentiation rise early during ischemia and continue during resuscitation in a porcine acute ischemia model. J. Interferon Cytokine Res. 31, 509-513. doi: 10.1089/jir.2010.0133.
100. Smith, R. R., Barile, L., Messina, E., and Marbán, E. (2008a). Stem cells in the heart: what's the buzz all about? Part 2: arrhythmic risks and clinical studies. Heart Rhythm 5, 880-887. doi: 10.1016/j.hrthm.2008.02.011.
101. Smith, R. R., Barile, L., Messina, E., and Marbán, E. (2008b). Stem cells in the heart: what's the buzz all about?-Part 1: preclinical considerations. Heart Rhythm 5, 749-757. doi: 10.1016/j.hrthm.2008.02.010.
102. Takashima, S.-I., Tempel, D., and Duckers, H. J. (2013). Current outlook of cardiac stem cell therapy towards a clinical application. Heart 99, 1772-1784. doi: 10.1136/heartjnl-2012-303308.
103. Takemura, G., and Fujiwara, H. (2007). Doxorubicin-induced cardiomyopathy from the cardiotoxic mechanisms to management. Prog. Cardiovasc. Dis. 49, 330-352. doi: 10.1016/j.pcad.2006.10.002.
104. Tendera, M., Wojakowski, W., Ruzyllo, W., Chojnowska, L., Kepka, C., Tracz, W., et al. (2009). Intracoronary infusion of bone marrow-derived selected CD34+CXCR4+ cells and non-selected mononuclear cells in patients with acute STEMI and reduced left ventricular ejection fraction: results of randomized, multicentre Myocardial Regeneration by Intracor. Eur. Heart J. 30, 1313-1321. doi: 10.1093/eurheartj/ehp073.
105. Toma, J. G., McKenzie, I. A., Bagli, D., and Miller, F. D. (2005). Isolation and characterization of multipotent skin-derived precursors from human skin. Stem Cells 23, 727-737. doi: 10.1634/stemcells.2004-0134.
106. Torella, D., Ellison, G. M., Karakikes, I., and Nadal-Ginard, B. (2007). Resident cardiac stem cells. Cell. Mol. Life Sci. 64, 661-673. doi: 10.1007/s00018-007-6519-y.
107. Uchida, S., De Gaspari, P., Kostin, S., Jenniches, K., Kilic, A., Izumiya, Y., et al. (2013). Sca1-derived cells are a source of myocardial renewal in the murine adult heart. Stem Cell Reports 1, 397-410. doi: 10.1016/j.stemcr.2013.09.004.
108. Urbanek, K., Cesselli, D., Rota, M., Nascimbene, A., De Angelis, A., Hosoda, T., et al. (2006). Stem cell niches in the adult mouse heart. Proc. Natl. Acad. Sci. U.S.A. 103, 9226-9231. doi: 10.1073/pnas.0600635103.
109. Urbanek, K., Torella, D., Sheikh, F., De Angelis, A., Nurzynska, D., Silvestri, F., et al. (2005). Myocardial regeneration by activation of multipotent cardiac stem cells in ischemic heart failure. Proc. Natl. Acad. Sci. U.S.A. 102, 8692-8697. doi: 10.1073/pnas.0500169102.
110. van Berlo, J. H., Kanisicak, O., Maillet, M., Vagnozzi, R. J., Karch, J., Lin, S.-C. J., et al. (2014). C-Kit+ cells minimally contribute cardiomyocytes to the heart. Nature 509, 337-341. doi: 10.1038/nature13309.
111. Vecellio, M., Meraviglia, V., Nanni, S., Barbuti, A., Scavone, A., DiFrancesco, D., et al. (2012). In vitro epigenetic reprogramming of human cardiac mesenchymal stromal cells into functionally competent cardiovascular precursors. PLoS ONE 7:e51694. doi: 10.1371/journal.pone.0051694.
112. Wagers, A. J., Sherwood, R. I., Christensen, J. L., and Weissman, I. L. (2002). Little evidence for developmental plasticity of adult hematopoietic stem cells. Science 297, 2256-2259. doi: 10.1126/science.1074807.
113. Wang, H., Chen, H., Feng, B., Wang, X., He, X., Hu, R., et al. (2014). Isolation and characterization of a Sca-1+/CD31-progenitor cell lineage derived from mouse heart tissue. BMC Biotechnol. 14:75. doi: 10.1186/1472-6750-14-75.
114. Wang, K., Zhao, X., Kuang, C., Qian, D., Wang, H., Jiang, H., et al. (2012). Overexpression of SDF-1α enhanced migration and engraftment of cardiac stem cells and reduced infarcted size via CXCR4/PI3K pathway. PLoS ONE 7:e43922. doi: 10.1371/journal.pone.0043922.
115. Wang, X., Hu, Q., Nakamura, Y., Lee, J., Zhang, G., From, A. H. L., et al. (2006a). The role of the sca-1+/CD31-cardiac progenitor cell population in postinfarction left ventricular remodeling. Stem Cells 24, 1779-1788. doi: 10.1634/stemcells.2005-0386.
116. Wang, Y., Haider, H. K., Ahmad, N., Zhang, D., and Ashraf, M. (2006b). Evidence for ischemia induced host-derived bone marrow cell mobilization into cardiac allografts. J. Mol. Cell. Cardiol. 41, 478-487. doi: 10.1016/j.yjmcc.2006.06.074.
117. Waring, C. D., Vicinanza, C., Papalamprou, A., Smith, A. J., Purushothaman, S., Goldspink, D. F., et al. (2014). The adult heart responds to increased workload with physiologic hypertrophy, cardiac stem cell activation, and new myocyte formation. Eur. Heart J. 35, 2722-2731. doi: 10.1093/eurheartj/ehs338.
118. Welm, B. E., Tepera, S. B., Venezia, T., Graubert, T. A., Rosen, J. M., and Goodell, M. A. (2002). Sca-1(pos) cells in the mouse mammary gland represent an enriched progenitor cell population. Dev. Biol. 245, 42-56. doi: 10.1006/dbio.2002.0625.
119. Wright, D. E., Wagers, A. J., Gulati, A. P., Johnson, F. L., and Weissman, I. L. (2001). Physiological migration of hematopoietic stem and progenitor cells. Science 294, 1933-1936. doi: 10.1126/science.1064081.
120. Wulf, G. G., Luo, K.-L., Jackson, K. A., Brenner, M. K., and Goodell, M. A. (2003). Cells of the hepatic side population contribute to liver regeneration and can be replenished with bone marrow stem cells. Haematologica 88, 368-378.
121. Xin, L., Lawson, D. A., and Witte, O. N. (2005). The Sca-1 cell surface marker enriches for a prostate-regenerating cell subpopulation that can initiate prostate tumorigenesis. Proc. Natl. Acad. Sci. U.S.A. 102, 6942-6947. doi: 10.1073/pnas.0502320102.
122. Yan, F., Yao, Y., Chen, L., Li, Y., Sheng, Z., and Ma, G. (2012). Hypoxic preconditioning improves survival of cardiac progenitor cells: role of stromal cell derived factor-1α-CXCR4 axis. PLoS ONE 7:e37948. doi: 10.1371/journal.pone.0037948.
123. Zakharova, L., Mastroeni, D., Mutlu, N., Molina, M., Goldman, S., Diethrich, E., et al. (2010). Transplantation of cardiac progenitor cell sheet onto infarcted heart promotes cardiogenesis and improves function. Cardiovasc. Res. 87, 40-49. doi: 10.1093/cvr/cvq027.
124. Zhang, G., Nakamura, Y., Wang, X., Hu, Q., Suggs, L. J., and Zhang, J. (2007). Controlled release of stromal cell-derived factor-1 alpha in situ increases c-kit+ cell homing to the infarcted heart. Tissue Eng. 13, 2063-2071. doi: 10.1089/ten.2006.0013.
125. Zhang, N., Mustin, D., Reardon, W., De Almeida, A., Mozdziak, P., Mrug, M., et al. (2006). Blood-borne stem cells differentiate into vascular and cardiac lineages during normal development. Stem Cells Dev. 15, 17-28. doi: 10.1089/scd.2006.15.17.