Exosomes secreted from GATA-4 overexpressing mesenchymal stem cells serve as a reservoir of anti-apoptotic microRNAs for cardioprotection

International Journal of Cardiology

Volumn 182, Issue C, 2015, Pages 349-360

  Yu, Bin ^a   Kim, Ha Won ^a   Gong, Min ^a   Wang, Jingcai ^a   Millard, Ronald W ^a   Wang, Yigang ^a   Ashraf, Muhammad ^a,b   Xu, Meifeng ^a  

^a UNIVERSITY OF CINCINNATI MEDICAL CENTER   (United States)

^b UNIVERSITY OF ILLINOIS   (United States)

Author keywords

Bone marrow stem cells; Cardioprotection; Exosomes; GATA 4; MiR transfer; Target proteins

Indexed keywords

MICRORNA; RNA; TRANSCRIPTION FACTOR GATA 4;

ANIMAL; APOPTOSIS; BIOSYNTHESIS; CARDIAC MUSCLE CELL; CELL CULTURE; CELL SURVIVAL; CYTOLOGY; EXOSOME; GENE EXPRESSION REGULATION; GENETICS; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMA CELL; METABOLISM; MYOCARDIAL INFARCTION; PATHOLOGY; PROCEDURES; RAT; REAL TIME POLYMERASE CHAIN REACTION;

ANIMALS; APOPTOSIS; CELL SURVIVAL; CELLS, CULTURED; EXOSOMES; GATA4 TRANSCRIPTION FACTOR; GENE EXPRESSION REGULATION; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; MICRORNAS; MYOCARDIAL INFARCTION; MYOCYTES, CARDIAC; RATS; REAL-TIME POLYMERASE CHAIN REACTION; RNA;

EID: 84947201437     PISSN: 01675273     EISSN: 18741754     Source Type: Journal    
DOI: 10.1016/j.ijcard.2014.12.043     Document Type: Article

References (39)

1. A.B. Mathiasen, M. Haack-Sorensen, E. Jorgensen, J. Kastrup, Autotransplantation of mesenchymal stromal cells from bone-marrow to heart in patients with severe stable coronary artery disease and refractory angina - final 3-year follow-up, Int. J. Cardiol. 170 (2013) 246-251.
2. E.C. Perin, G.V. Silva, T.D. Henry, M.G. Cabreira-Hansen, W.H. Moore, S.A. Coulter, et al., A randomized study of transendocardial injection of autologous bone marrow mononuclear cells and cell function analysis in ischemic heart failure (FOCUS-HF), Am. Heart J. 161 (2011) 1078-1087 e3.
3. R. Uemura, M. Xu, N. Ahmad, M. Ashraf, Bone marrow stem cells prevent left ventricular remodeling of ischemic heart through paracrine signaling, Circ. Res. 98 (2006) 1414-1421.
4. J.H. Houtgraaf, R. de Jong, K. Kazemi, D. de Groot, T.I. van der Spoel, F. Arslan, et al., Intracoronary infusion of allogeneic mesenchymal precursor cells directly after experimental acute myocardial infarction reduces infarct size, abrogates adverse remodeling, and improves cardiac function, Circ. Res. 113 (2013) 153-166.
5. D.S. Nascimento, D. Mosqueira, L.M. Sousa, M. Teixeira, M. Filipe, T.P. Resende, et al., Human umbilical cord tissue-derived mesenchymal stromal cells attenuate remodeling following myocardial infarction by pro-angiogenic, anti-apoptotic and endogenous cell activation mechanisms, Stem Cell Res. Ther. 5 (2014) 5.
6. H. Li, S. Zuo, Z. Pasha, B. Yu, Z. He, Y. Wang, et al., GATA-4 promotes myocardial transdifferentiation of mesenchymal stromal cells via up-regulating IGFBP-4, Cytotherapy 13 (2011) 1057-1065.
7. H. Li, S. Zuo, Z. He, Y. Yang, Z. Pasha, Y. Wang, et al., Paracrine factors released by GATA-4 overexpressed mesenchymal stem cells increase angiogenesis and cell survival, Am. J. Physiol. Heart Circ. Physiol. 299 (2010) H1772-H1781.
8. B. Yu, M. Gong, Z. He, Y.G. Wang, R.W. Millard, M. Ashraf, et al., Enhanced mesenchymal stem cell survival induced by GATA-4 overexpression is partially mediated by regulation of the miR-15 family, Int. J. Biochem. Cell Biol. 45 (2013) 2724-2735.
9. B. Yu, M. Gong, Y. Wang, R.W. Millard, Z. Pasha, Y. Yang, et al., Cardiomyocyte protection by GATA-4 gene engineered mesenchymal stem cells is partially mediated by translocation of miR-221 in microvesicles, PLoS One 8 (2013) e73304.
10. D. Orlic, Adult bone marrow stem cells regenerate myocardium in ischemic heart disease, Ann. N. Y. Acad. Sci. 996 (2003) 152-157.
11. J. DeSantiago, D.J. Bare, I. Semenov, R.D. Minshall, D.L. Geenen, B.M. Wolska, et al., Excitation-contraction coupling in ventricular myocytes is enhanced by paracrine signaling from mesenchymal stem cells, J. Mol. Cell. Cardiol. 52 (2012) 1249-1256.
12. D. Angoulvant, F. Ivanes, R. Ferrera, P.G. Matthews, S. Nataf, M. Ovize, Mesenchymal stem cell conditioned media attenuates in vitro and ex vivo myocardial reperfusion injury, J. Heart Lung Transplant. Off. Publ. Int. Soc. Heart Transpl. 30 (2011) 95-102.
13. A.I. Caplan, J.E. Dennis, Mesenchymal stem cells as trophic mediators, J. Cell. Biochem. 98 (2006) 1076-1084.
14. F. Arslan, R.C. Lai, M.B. Smeets, L. Akeroyd, A. Choo, E.N. Aguor, et al., Mesenchymal stem cell-derived exosomes increase ATP levels, decrease oxidative stress and activate PI3K/Akt pathway to enhance myocardial viability and prevent adverse remodeling after myocardial ischemia/reperfusion injury, Stem Cell Res. 10 (2013) 301-312.
15. R.C. Lai, F. Arslan, M.M. Lee, N.S. Sze, A. Choo, T.S. Chen, et al., Exosome secreted by MSC reduces myocardial ischemia/reperfusion injury, Stem Cell Res. 4 (2010) 214-222.
16. L. Chen, Y. Wang, Y. Pan, L. Zhang, C. Shen, G. Qin, et al., Cardiac progenitor-derived exosomes protect ischemic myocardium from acute ischemia/reperfusion injury, Biochem. Biophys. Res. Commun. 431 (2013) 566-571.
17. T.S. Chen, R.C. Lai, M.M. Lee, A.B. Choo, C.N. Lee, S.K. Lim, Mesenchymal stem cell secretes microparticles enriched in pre-microRNAs, Nucleic Acids Res. 38 (2010) 215-224.
18. W. Stoorvogel, Functional transfer of microRNA by exosomes, Blood 119 (2012) 646-648.
19. H. Valadi, K. Ekstrom, A. Bossios, M. Sjostrand, J.J. Lee, J.O. Lotvall, Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells, Nat. Cell Biol. 9 (2007) 654-659.
20. S.S. Luo, O. Ishibashi, G. Ishikawa, T. Ishikawa, A. Katayama, T. Mishima, et al., Human villous trophoblasts express and secrete placenta-specific microRNAs into maternal circulation via exosomes, Biol. Reprod. 81 (2009) 717-729.
21. M. Mittelbrunn, C. Gutierrez-Vazquez, C. Villarroya-Beltri, S. Gonzalez, F. Sanchez-Cabo, M.A. Gonzalez, et al., Unidirectional transfer of microRNA-loaded exosomes from T cells to antigen-presenting cells, Nat. Commun. 2 (2011) 282.
22. H. Xin, Y. Li, B. Buller, M. Katakowski, Y. Zhang, X. Wang, et al., Exosome-mediated transfer of miR-133b from multipotent mesenchymal stromal cells to neural cells contributes to neurite outgrowth, Stem Cells 30 (2012) 1556-1564.
23. M. Xu, M. Wani, Y.S. Dai, J. Wang, M. Yan, A. Ayub, et al., Differentiation of bone marrow stromal cells into the cardiac phenotype requires intercellular communication with myocytes, Circulation 110 (2004) 2658-2665.
24. I. Parolini, C. Federici, C. Raggi, L. Lugini, S. Palleschi, A. De Milito, et al., Microenvironmental pH is a key factor for exosome traffic in tumor cells, J. Biol. Chem. 284 (2009) 34211-34222.
25. J. Schrader, Mechanisms of ischemic injury in the heart, Basic Res. Cardiol. 80 (Suppl. 2) (1985) 135-139.
26. A. Montecalvo, A.T. Larregina, A.E. Morelli, Methods of analysis of dendritic cell-derived exosome-shuttle microRNA and its horizontal propagation between dendritic cells, Methods Mol. Biol. 1024 (2013) 19-40.
27. Z. Pasha, Y. Wang, R. Sheikh, D. Zhang, T. Zhao, M. Ashraf, Preconditioning enhances cell survival and differentiation of stem cells during transplantation in infarcted myocardium, Cardiovasc. Res. 77 (2008) 134-142.
28. Y. Feng, W. Huang, M. Wani, X. Yu, M. Ashraf, Ischemic preconditioning potentiates the protective effect of stem cells through secretion of exosomes by targeting Mecp2 via miR-22, PLoS One 9 (2014) e88685.
29. A.R. Mackie, E. Klyachko, T. Thorne, K.M. Schultz, M. Millay, A. Ito, et al., Sonic hedgehog-modified human CD34+ cells preserve cardiac function after acute myocardial infarction, Circ. Res. 111 (2012) 312-321.
30. L.S. Danielson, D.S. Park, N. Rotllan, A. Chamorro-Jorganes, M.V. Guijarro, C. Fernandez-Hernando, et al., Cardiovascular dysregulation of miR-17-92 causes a lethal hypertrophic cardiomyopathy and arrhythmogenesis, FASEB J. 27 (2013) 1460-1467.
31. J. Chen, Z.P. Huang, H.Y. Seok, J. Ding, M. Kataoka, Z. Zhang, et al., mir-17-92 cluster is required for and sufficient to induce cardiomyocyte proliferation in postnatal and adult hearts, Circ. Res. 112 (2013) 1557-1566.
32. Y. Cao, S.L. Yu, Y. Wang, G.Y. Guo, Q. Ding, R.H. An, MicroRNA-dependent regulation of PTEN after arsenic trioxide treatment in bladder cancer cell line T24, Tumour Biol. 32 (2011) 179-188.
33. S. Choorapoikayil, R. Kers, P. Herbomel, K. Kissa, J. den Hertog, Pivotal role of Pten in the balance between proliferation and differentiation of hematopoietic stem cells in zebrafish, Blood 123 (2014) 184-190.
34. B. Yan, R.D. Singla, L.S. Abdelli, P.K. Singal, D.K. Singla, Regulation of PTEN/Akt pathway enhances cardiomyogenesis and attenuates adverse left ventricular remodeling following thymosin beta4 overexpressing embryonic stem cell transplantation in the infarcted heart, PLoS One 8 (2013) e75580.
35. C. Skurk, Y. Izumiya, H. Maatz, P. Razeghi, I. Shiojima, M. Sandri, et al., The FOXO3a transcription factor regulates cardiac myocyte size downstream of AKT signaling, J. Biol. Chem. 280 (2005) 20814-20823.
36. P. Bouillet, J.F. Purton, D.I. Godfrey, L.C. Zhang, L. Coultas, H. Puthalakath, et al., BH3-only Bcl-2 family member Bim is required for apoptosis of autoreactive thymocytes, Nature 415 (2002) 922-926.
37. X. Zhang, X. Wang, H. Zhu, C. Zhu, Y. Wang, W.T. Pu, et al., Synergistic effects of the GATA-4-mediated miR-144/451 cluster in protection against simulated ischemia/reperfusion-induced cardiomyocyte death, J. Mol. Cell. Cardiol. 49 (2010) 841-850.
38. C.Z. Zhang, J.X. Zhang, A.L. Zhang, Z.D. Shi, L. Han, Z.F. Jia, et al., MiR-221 and miR-222 target PUMA to induce cell survival in glioblastoma, Mol. Cancer 9 (2010) 229.
39. A.D. Sharma, N. Narain, E.M. Handel, M. Iken, N. Singhal, T. Cathomen, et al., MicroRNA-221 regulates FAS-induced fulminant liver failure, Hepatology 53 (2011) 1651-1661.