The advances of cardiac stem cell for the treatment of cardiovascular disease_Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Authors：

LV Jingjing , SHI Guocheng ,  CHEN Huiwen

Department of Cardiothoracic Surgery, Shanghai Children’s Medical Center, Heart Center, Shanghai Jiaotong University School of Medicine, Shanghai, 200127, P.R.China;

Corresponding author：

CHEN Huiwen, Email: hwhwhc@hotmail.com

Keywords：

Cardiac stem cell; cell therapy; cardiomyocyte regeneration; cardiovascular disease

DOI：

10.7507/1007-4848.201608018

Video：

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With the discovery of cardiac stem cell, the conception of the heart considered to be a terminally differentiated organ was changed. Cardiac stem cells possess the common characteristics of self-renew, clone formation and differentiating into cardiomyocyte, smooth muscle cell, and endothelial cell. Because of the properties of tissue specificity and lineage commitment, cardiac stem cells are considered to have great advantages over other stem cells in the treatment of cardiovascular disease. However, the low rate of engraftment still remains a problem to be solved. In recent years, people attempted to combine stem cell therapy with other ways, such as tissue engineering, gene therapy, exosome therapy, to cure cardiovascular diseases, aiming at finding better ways to treat the cardiovascular disease. This article is mainly for the reviewing of the mechanisms underlying the stem cell therapy and the combinatory use of new technology emerged these years.

Citation： LV Jingjing, SHI Guocheng, CHEN Huiwen. The advances of cardiac stem cell for the treatment of cardiovascular disease. Chinese Journal of Clinical Thoracic and Cardiovascular Surgery, 2017, 24(12): 983-987. doi: 10.7507/1007-4848.201608018 Copy

1.	Beltrami AP, Barlucchi L, Torella D, et al. Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell, 2003, 114(6): 763-776.
2.	Messina E, De Angelis L, Frati G, et al. Isolation and expansion of adult cardiac stem cells from human and murine heart. Circ Res, 2004, 95(9): 911-921.
3.	Smith RR, Barile L, Cho HC, et al. Regenerative potential of cardiosphere-derived cells expanded from percutaneous endomyocardial biopsy specimens. Circulation, 2007, 115(7): 896-908.
4.	Ott HC, Matthiesen TS, Brechtken J, et al. The adult human heart as a source for stem cells: repair strategies with embryonic-like progenitor cells. Nat Clin Pract Cardiovasc Med, 2007, 4(Suppl 1): S27-S39.
5.	Matsuura K, Nagai T, Nishigaki N, et al. Adult cardiac Sca-1-positive cells differentiate into beating cardiomyocytes. J Biol Chem, 2004, 279(12): 11384-11391.
6.	Bu L, Jiang X, Martin-Puig S, et al. Human ISL1 heart progenitors generate diverse multipotent cardiovascular cell lineages. Nature, 2009, 460(7251): 113-117.
7.	Liang SX, Tan TY, Gaudry L, et al. Differentiation and migration of Sca1+/CD31- cardiac side population cells in a murine myocardial ischemic model. Inter J Cardiol, 2010, 138(1): 40-49.
8.	Carr CA, Stuckey DJ, Tan JJ, et al. Cardiosphere-derived cells improve function in the infarcted rat heart for at least 16 weeks--an MRI study. PloS One, 2011, 6(10): e25669.
9.	Davis DR, Ruckdeschel Smith R, Marban E. Human cardiospheres are a source of stem cells with cardiomyogenic potential. Stem Cells, 2010, 28(5): 903-904.
10.	Vieira JM, Riley PR. Epicardium-derived cells: a new source of regenerative capacity. Heart, 2011, 97(1): 15-19.
11.	Urbanek K, Cesselli D, Rota M, et al. Stem cell niches in the adult mouse heart. Proc Natl Acad Sci USA, 2006, 103(24): 9226-9231.
12.	Bearzi C, Rota M, Hosoda T, et al. Human cardiac stem cells. Proc Natl Acad Sci USA, 2007, 104(35): 14068-14073.
13.	Bollini S, Smart N, Riley PR. Resident cardiac progenitor cells: at the heart of regeneration. J Mol Cell Cardiol, 2011, 50(2): 296-303.
14.	van Vliet P, Roccio M, Smits AM, et al. Progenitor cells isolated from the human heart: a potential cell source for regenerative therapy. Neth Heart J, 2008, 16(5): 163-169.
15.	Limana F, Capogrossi MC, Germani A. The epicardium in cardiac repair: from the stem cell view. Pharmacol Ther, 2011, 129(1): 82-96.
16.	Garbade JA, Dhein M, Dhein S, et al. Distribution pattern of viable resident C-Kit positive cardiac stem cells in the human ischemic heart as a pool for cardiac regeneration. J Heart Lung Transplant, 2014, 33(4): 254.
17.	Itzhaki-Alfia A, Leor J, Raanani E, et al. Patient characteristics and cell source determine the number of isolated human cardiac progenitor cells. Circulation, 2009, 120(25): 2559-2566.
18.	Sandstedt J, Jonsson M, Dellgren G, et al. Human C-kit+CD45- cardiac stem cells are heterogeneous and display both cardiac and endothelial commitment by single-cell qPCR analysis. Biochem Biophys Res Commun, 2014, 443(1): 234-238.
19.	Ye J, Boyle A, Shih H, et al. Sca-1+ cardiosphere-derived cells are enriched for Isl1-expressing cardiac precursors and improve cardiac function after myocardial injury. PloS One, 2012, 7(1): e30329.
20.	Dawn B, Stein AB, Urbanek K, et al. Cardiac stem cells delivered intravascularly traverse the vessel barrier, regenerate infarcted myocardium, and improve cardiac function. Proc Natl Acad Sci USA, 2005, 102(10): 3766-3771.
21.	Li Q, Guo Y, Ou Q, et al. Intracoronary administration of cardiac stem cells in mice: a new, improved technique for cell therapy in murine models. Basic Res Cardiol, 2011, 106(5): 849-864.
22.	Tang XL, Rokosh G, Sanganalmath SK, et al. Intracoronary administration of cardiac progenitor cells alleviates left ventricular dysfunction in rats with a 30-day-old infarction. Circulation, 2010, 121(2): 293-305.
23.	Mirotsou M, Jayawardena TM, Schmeckpeper J, et al. Paracrine mechanisms of stem cell reparative and regenerative actions in the heart. J Mol Cell Cardiol, 2011, 50(2): 280-289.
24.	Chimenti I, Smith RR, Li TS, et al. Relative roles of direct regeneration versus paracrine effects of human cardiosphere-derived cells transplanted into infarcted mice. Circ Res, 2010, 106(5): 971-980.
25.	Stastna M, Chimenti I, Marban E, et al. Identification and functionality of proteomes secreted by rat cardiac stem cells and neonatal cardiomyocytes. Proteomics, 2010, 10(2): 245-253.
26.	Stastna M, Abraham MR, Van Eyk JE. Cardiac stem/progenitor cells, secreted proteins, and proteomics. FEBS Letters, 2009, 583(11): 1800-1807.
27.	Urbanek K, Rota M, Cascapera S, 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, 2005, 97(7): 663-673.
28.	Yeghiazarians Y, Zhang Y, Prasad M, et al. Injection of bone marrow cell extract into infarcted hearts results in functional improvement comparable to intact cell therapy. Mol Ther, 2009, 17(7): 1250-1256.
29.	Zhang YH, Zhang GW, Gu TX, et al. Exogenous basic fibroblast growth factor promotes cardiac stem cell-mediated myocardial regeneration after miniswine acute myocardial infarction. Coron Artery Dis, 2011, 22(4): 279-285.
30.	Ellison GM, Torella D, Dellegrottaglie S, et al. Endogenous cardiac stem cell activation by insulin-like growth factor-1/hepatocyte growth factor intracoronary injection fosters survival and regeneration of the infarcted pig heart. J Am Coll Cardiol, 2011, 58(9): 977-986.
31.	Linke A, Muller P, Nurzynska D, 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 USA, 2005, 102(25): 8966-8971.
32.	Rota M, Padin-Iruegas ME, Misao Y, et al. Local activation or implantation of cardiac progenitor cells rescues scarred infarcted myocardium improving cardiac function. Circ Res, 2008, 103(1): 107-116.
33.	Padin-Iruegas ME, Misao Y, Davis ME, et al. Cardiac progenitor cells and biotinylated insulin-like growth factor-1 nanofibers improve endogenous and exogenous myocardial regeneration after infarction. Circulation, 2009, 120(10): 876-887.
34.	Tan SC, Gomes RS, Yeoh KK, et al. Preconditioning of cardiosphere-derived cells with hypoxia or prolyl-4-hydroxylase inhibitors increases stemness and decreases reliance on oxidative metabolism. Cell Transplant, 2016, 25(1): 35-53.
35.	Hatzistergos KE, Quevedo H, Oskouei BN, et al. Bone marrow mesenchymal stem cells stimulate cardiac stem cell proliferation and differentiation. Circ Res, 2010, 107(7): 913-922.
36.	Williams AR, Hatzistergos KE, Addicott B, et al. Enhanced effect of combining human cardiac stem cells and bone marrow mesenchymal stem cells to reduce infarct size and to restore cardiac function after myocardial infarction. Circulation, 2013, 127(2): 213-223.
37.	Avolio E, Meloni M, Spencer HL, et al. Combined intramyocardial delivery of human pericytes and cardiac stem cells additively improves the healing of mouse infarcted hearts through stimulation of vascular and muscular repair. Circ Res, 2015, 116(10): e81-e94.
38.	Shimizu T, Yamato M, Kikuchi A, et al. Cell sheet engineering for myocardial tissue reconstruction. Biomaterials, 2003, 24(13): 2309-2316.
39.	Alshammary S, Fukushima S, Miyagawa S, et al. Impact of cardiac stem cell sheet transplantation on myocardial infarction. Surg Today, 2013, 43(9): 970-976.
40.	Soejima K, Negishi N, Nozaki M, et al. Effect of cultured endothelial cells on angiogenesis in vivo. Plast Reconstr Surg, 1998, 101(6): 1552-1560.
41.	Li Z, Guan J. Thermosensitive hydrogels for drug delivery. Expert Opin Drug Deliv, 2011, 8(8): 991-1007.
42.	Ou L, Li W, Zhang Y, et al. Intracardiac injection of matrigel induces stem cell recruitment and improves cardiac functions in a rat myocardial infarction model. J Cell Mol Med, 2011, 15(6): 1310-1318.
43.	Takehara N, Tsutsumi Y, Tateishi K, et al. Controlled delivery of basic fibroblast growth factor promotes human cardiosphere-derived cell engraftment to enhance cardiac repair for chronic myocardial infarction. J Am Coll Cardiol, 2008, 52(23): 1858-1865.
44.	Sun X, Nunes SS. Overview of hydrogel-based strategies for application in cardiac tissue regeneration. Biomed Mater, 2015, 10(3): 034005.
45.	Liu Q, Tian S, Zhao C, et al. Porous nanofibrous poly(L-lactic acid) scaffolds supporting cardiovascular progenitor cells for cardiac tissue engineering. Acta Biomater, 2015, 26: 105-114.
46.	Lee YS, Lim KS, Oh JE, et al. Development of porous PLGA/PEI1.8k biodegradable microspheres for the delivery of mesenchymal stem cells (MSCs). J Control Release, 2015, 205: 128-133.
47.	Yaniz-Galende E, Chen J, Chemaly E, et al. Stem cell factor gene transfer promotes cardiac repair after myocardial infarction via in situ recruitment and expansion of c-kit+ cells. Circ Res, 2012, 111(11): 1434-1445.
48.	Fischer KM, Cottage CT, Wu W, et al. Enhancement of myocardial regeneration through genetic engineering of cardiac progenitor cells expressing Pim-1 kinase. Circulation, 2009, 120(21): 2077-2087.
49.	Hu S, Huang M, Nguyen PK, et al. Novel microRNA prosurvival cocktail for improving engraftment and function of cardiac progenitor cell transplantation. Circulation, 2011, 124(11 Suppl): S27-S34.
50.	Lavu M, Gundewar S, Lefer DJ. Gene therapy for ischemic heart disease. J Mol Cell Cardiol, 2011, 50(5): 742-750.
51.	Yockman JW, Kastenmeier A, Erickson HM, et al. Novel polymer carriers and gene constructs for treatment of myocardial ischemia and infarction. J Control Release, 2008, 132(3): 260-266.
52.	Yi F, Wu H, Jia GL, et al. Effect of nanoparticle with vascular endothelial growth factor gene transferred into ischemic myocardium: experiment with rabbit. Zhonghua Yi Xue Za Zhi, 2006, 86(8): 510-514.
53.	Johnstone RM. Revisiting the road to the discovery of exosomes. Blood Cells Mol Dis, 2005, 34(3): 214-219.
54.	Ibrahim AG, Cheng K, Marban E. Exosomes as critical agents of cardiac regeneration triggered by cell therapy. Stem Cell Reports, 2014, 2(5): 606-619.
55.	Gray WD, French KM, Ghosh-Choudhary S, et al. Identification of therapeutic covariant microRNA clusters in hypoxia-treated cardiac progenitor cell exosomes using systems biology. Circ Res, 2015, 116(2): 255-263.
56.	Khan M, Nickoloff E, Abramova T, et al. Embryonic stem cell-derived exosomes promote endogenous repair mechanisms and enhance cardiac function following myocardial infarction. Circ Res, 2015, 117(1): 52-64.

1. Beltrami AP, Barlucchi L, Torella D, et al. Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell, 2003, 114(6): 763-776.
2. Messina E, De Angelis L, Frati G, et al. Isolation and expansion of adult cardiac stem cells from human and murine heart. Circ Res, 2004, 95(9): 911-921.
3. Smith RR, Barile L, Cho HC, et al. Regenerative potential of cardiosphere-derived cells expanded from percutaneous endomyocardial biopsy specimens. Circulation, 2007, 115(7): 896-908.
4. Ott HC, Matthiesen TS, Brechtken J, et al. The adult human heart as a source for stem cells: repair strategies with embryonic-like progenitor cells. Nat Clin Pract Cardiovasc Med, 2007, 4(Suppl 1): S27-S39.
5. Matsuura K, Nagai T, Nishigaki N, et al. Adult cardiac Sca-1-positive cells differentiate into beating cardiomyocytes. J Biol Chem, 2004, 279(12): 11384-11391.
6. Bu L, Jiang X, Martin-Puig S, et al. Human ISL1 heart progenitors generate diverse multipotent cardiovascular cell lineages. Nature, 2009, 460(7251): 113-117.
7. Liang SX, Tan TY, Gaudry L, et al. Differentiation and migration of Sca1+/CD31- cardiac side population cells in a murine myocardial ischemic model. Inter J Cardiol, 2010, 138(1): 40-49.
8. Carr CA, Stuckey DJ, Tan JJ, et al. Cardiosphere-derived cells improve function in the infarcted rat heart for at least 16 weeks--an MRI study. PloS One, 2011, 6(10): e25669.
9. Davis DR, Ruckdeschel Smith R, Marban E. Human cardiospheres are a source of stem cells with cardiomyogenic potential. Stem Cells, 2010, 28(5): 903-904.
10. Vieira JM, Riley PR. Epicardium-derived cells: a new source of regenerative capacity. Heart, 2011, 97(1): 15-19.
11. Urbanek K, Cesselli D, Rota M, et al. Stem cell niches in the adult mouse heart. Proc Natl Acad Sci USA, 2006, 103(24): 9226-9231.
12. Bearzi C, Rota M, Hosoda T, et al. Human cardiac stem cells. Proc Natl Acad Sci USA, 2007, 104(35): 14068-14073.
13. Bollini S, Smart N, Riley PR. Resident cardiac progenitor cells: at the heart of regeneration. J Mol Cell Cardiol, 2011, 50(2): 296-303.
14. van Vliet P, Roccio M, Smits AM, et al. Progenitor cells isolated from the human heart: a potential cell source for regenerative therapy. Neth Heart J, 2008, 16(5): 163-169.
15. Limana F, Capogrossi MC, Germani A. The epicardium in cardiac repair: from the stem cell view. Pharmacol Ther, 2011, 129(1): 82-96.
16. Garbade JA, Dhein M, Dhein S, et al. Distribution pattern of viable resident C-Kit positive cardiac stem cells in the human ischemic heart as a pool for cardiac regeneration. J Heart Lung Transplant, 2014, 33(4): 254.
17. Itzhaki-Alfia A, Leor J, Raanani E, et al. Patient characteristics and cell source determine the number of isolated human cardiac progenitor cells. Circulation, 2009, 120(25): 2559-2566.
18. Sandstedt J, Jonsson M, Dellgren G, et al. Human C-kit+CD45- cardiac stem cells are heterogeneous and display both cardiac and endothelial commitment by single-cell qPCR analysis. Biochem Biophys Res Commun, 2014, 443(1): 234-238.
19. Ye J, Boyle A, Shih H, et al. Sca-1+ cardiosphere-derived cells are enriched for Isl1-expressing cardiac precursors and improve cardiac function after myocardial injury. PloS One, 2012, 7(1): e30329.
20. Dawn B, Stein AB, Urbanek K, et al. Cardiac stem cells delivered intravascularly traverse the vessel barrier, regenerate infarcted myocardium, and improve cardiac function. Proc Natl Acad Sci USA, 2005, 102(10): 3766-3771.
21. Li Q, Guo Y, Ou Q, et al. Intracoronary administration of cardiac stem cells in mice: a new, improved technique for cell therapy in murine models. Basic Res Cardiol, 2011, 106(5): 849-864.
22. Tang XL, Rokosh G, Sanganalmath SK, et al. Intracoronary administration of cardiac progenitor cells alleviates left ventricular dysfunction in rats with a 30-day-old infarction. Circulation, 2010, 121(2): 293-305.
23. Mirotsou M, Jayawardena TM, Schmeckpeper J, et al. Paracrine mechanisms of stem cell reparative and regenerative actions in the heart. J Mol Cell Cardiol, 2011, 50(2): 280-289.
24. Chimenti I, Smith RR, Li TS, et al. Relative roles of direct regeneration versus paracrine effects of human cardiosphere-derived cells transplanted into infarcted mice. Circ Res, 2010, 106(5): 971-980.
25. Stastna M, Chimenti I, Marban E, et al. Identification and functionality of proteomes secreted by rat cardiac stem cells and neonatal cardiomyocytes. Proteomics, 2010, 10(2): 245-253.
26. Stastna M, Abraham MR, Van Eyk JE. Cardiac stem/progenitor cells, secreted proteins, and proteomics. FEBS Letters, 2009, 583(11): 1800-1807.
27. Urbanek K, Rota M, Cascapera S, 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, 2005, 97(7): 663-673.
28. Yeghiazarians Y, Zhang Y, Prasad M, et al. Injection of bone marrow cell extract into infarcted hearts results in functional improvement comparable to intact cell therapy. Mol Ther, 2009, 17(7): 1250-1256.
29. Zhang YH, Zhang GW, Gu TX, et al. Exogenous basic fibroblast growth factor promotes cardiac stem cell-mediated myocardial regeneration after miniswine acute myocardial infarction. Coron Artery Dis, 2011, 22(4): 279-285.
30. Ellison GM, Torella D, Dellegrottaglie S, et al. Endogenous cardiac stem cell activation by insulin-like growth factor-1/hepatocyte growth factor intracoronary injection fosters survival and regeneration of the infarcted pig heart. J Am Coll Cardiol, 2011, 58(9): 977-986.
31. Linke A, Muller P, Nurzynska D, 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 USA, 2005, 102(25): 8966-8971.
32. Rota M, Padin-Iruegas ME, Misao Y, et al. Local activation or implantation of cardiac progenitor cells rescues scarred infarcted myocardium improving cardiac function. Circ Res, 2008, 103(1): 107-116.
33. Padin-Iruegas ME, Misao Y, Davis ME, et al. Cardiac progenitor cells and biotinylated insulin-like growth factor-1 nanofibers improve endogenous and exogenous myocardial regeneration after infarction. Circulation, 2009, 120(10): 876-887.
34. Tan SC, Gomes RS, Yeoh KK, et al. Preconditioning of cardiosphere-derived cells with hypoxia or prolyl-4-hydroxylase inhibitors increases stemness and decreases reliance on oxidative metabolism. Cell Transplant, 2016, 25(1): 35-53.
35. Hatzistergos KE, Quevedo H, Oskouei BN, et al. Bone marrow mesenchymal stem cells stimulate cardiac stem cell proliferation and differentiation. Circ Res, 2010, 107(7): 913-922.
36. Williams AR, Hatzistergos KE, Addicott B, et al. Enhanced effect of combining human cardiac stem cells and bone marrow mesenchymal stem cells to reduce infarct size and to restore cardiac function after myocardial infarction. Circulation, 2013, 127(2): 213-223.
37. Avolio E, Meloni M, Spencer HL, et al. Combined intramyocardial delivery of human pericytes and cardiac stem cells additively improves the healing of mouse infarcted hearts through stimulation of vascular and muscular repair. Circ Res, 2015, 116(10): e81-e94.
38. Shimizu T, Yamato M, Kikuchi A, et al. Cell sheet engineering for myocardial tissue reconstruction. Biomaterials, 2003, 24(13): 2309-2316.
39. Alshammary S, Fukushima S, Miyagawa S, et al. Impact of cardiac stem cell sheet transplantation on myocardial infarction. Surg Today, 2013, 43(9): 970-976.
40. Soejima K, Negishi N, Nozaki M, et al. Effect of cultured endothelial cells on angiogenesis in vivo. Plast Reconstr Surg, 1998, 101(6): 1552-1560.
41. Li Z, Guan J. Thermosensitive hydrogels for drug delivery. Expert Opin Drug Deliv, 2011, 8(8): 991-1007.
42. Ou L, Li W, Zhang Y, et al. Intracardiac injection of matrigel induces stem cell recruitment and improves cardiac functions in a rat myocardial infarction model. J Cell Mol Med, 2011, 15(6): 1310-1318.
43. Takehara N, Tsutsumi Y, Tateishi K, et al. Controlled delivery of basic fibroblast growth factor promotes human cardiosphere-derived cell engraftment to enhance cardiac repair for chronic myocardial infarction. J Am Coll Cardiol, 2008, 52(23): 1858-1865.
44. Sun X, Nunes SS. Overview of hydrogel-based strategies for application in cardiac tissue regeneration. Biomed Mater, 2015, 10(3): 034005.
45. Liu Q, Tian S, Zhao C, et al. Porous nanofibrous poly(L-lactic acid) scaffolds supporting cardiovascular progenitor cells for cardiac tissue engineering. Acta Biomater, 2015, 26: 105-114.
46. Lee YS, Lim KS, Oh JE, et al. Development of porous PLGA/PEI1.8k biodegradable microspheres for the delivery of mesenchymal stem cells (MSCs). J Control Release, 2015, 205: 128-133.
47. Yaniz-Galende E, Chen J, Chemaly E, et al. Stem cell factor gene transfer promotes cardiac repair after myocardial infarction via in situ recruitment and expansion of c-kit+ cells. Circ Res, 2012, 111(11): 1434-1445.
48. Fischer KM, Cottage CT, Wu W, et al. Enhancement of myocardial regeneration through genetic engineering of cardiac progenitor cells expressing Pim-1 kinase. Circulation, 2009, 120(21): 2077-2087.
49. Hu S, Huang M, Nguyen PK, et al. Novel microRNA prosurvival cocktail for improving engraftment and function of cardiac progenitor cell transplantation. Circulation, 2011, 124(11 Suppl): S27-S34.
50. Lavu M, Gundewar S, Lefer DJ. Gene therapy for ischemic heart disease. J Mol Cell Cardiol, 2011, 50(5): 742-750.
51. Yockman JW, Kastenmeier A, Erickson HM, et al. Novel polymer carriers and gene constructs for treatment of myocardial ischemia and infarction. J Control Release, 2008, 132(3): 260-266.
52. Yi F, Wu H, Jia GL, et al. Effect of nanoparticle with vascular endothelial growth factor gene transferred into ischemic myocardium: experiment with rabbit. Zhonghua Yi Xue Za Zhi, 2006, 86(8): 510-514.
53. Johnstone RM. Revisiting the road to the discovery of exosomes. Blood Cells Mol Dis, 2005, 34(3): 214-219.
54. Ibrahim AG, Cheng K, Marban E. Exosomes as critical agents of cardiac regeneration triggered by cell therapy. Stem Cell Reports, 2014, 2(5): 606-619.
55. Gray WD, French KM, Ghosh-Choudhary S, et al. Identification of therapeutic covariant microRNA clusters in hypoxia-treated cardiac progenitor cell exosomes using systems biology. Circ Res, 2015, 116(2): 255-263.
56. Khan M, Nickoloff E, Abramova T, et al. Embryonic stem cell-derived exosomes promote endogenous repair mechanisms and enhance cardiac function following myocardial infarction. Circ Res, 2015, 117(1): 52-64.

Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

The advances of cardiac stem cell for the treatment of cardiovascular disease

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