MiR-133a enhances the protective capacity of cardiac progenitors cells after myocardial infarction

Stem Cell Reports

Volumn 3, Issue 6, 2014, Pages 1029-1042

  Izarra, Alberto ^a,b   Moscoso, Isabel ^b,c   Levent, Elif ^d   Cañón, Susana ^a,b   Cerrada, Inmaculada ^e,f   Díez Juan, Antonio ^b,e   Blanca, Vanessa ^b   Núñez Gil, Iván J ^g   Valiente, Iñigo ^b   Ruíz Sauri, Amparo ^h   Sepúlveda, Pilar ^e   Tiburcy, Malte ^d   Zimmermann, Wolfram H ^d   Bernad, Antonio ^a,b  

^a CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

^b CENTRO NACIONAL DE INVESTIGACIONES CARDIOVASCULARES CNIC   (Spain)

^c University of Santiago de Compostela ^*  (Spain)

^d UNIVERSITY OF GÖTTINGEN   (Germany)

^e Instituto Universitario IVI INCLIVA   (Spain)

^f HOSPITAL UNIVERSITARIO LA FE   (Spain)

^g HOSPITAL CLÍNICO SAN CARLOS   (Spain)

^h UNIVERSITY OF VALENCIA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BASIC FIBROBLAST GROWTH FACTOR RECEPTOR; CASPASE 3; MICRORNA; MICRORNA 1; MICRORNA 133A; RETROVIRUS VECTOR; TRANSCRIPTION FACTOR NKX2.5; TROPONIN T; UNCLASSIFIED DRUG; VASCULOTROPIN; MESSENGER RNA; MIRN1 MICRORNA, RAT; MIRN133 MICRORNA, RAT;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BIOINFORMATICS; CARDIAC STEM CELL; CELL DEATH; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL PROTECTION; COMPARATIVE STUDY; CONTROLLED STUDY; DNA SYNTHESIS; ECHOCARDIOGRAPHY; EXOSOME; FLUORESCENCE ACTIVATED CELL SORTING; HEART FUNCTION; HEART INFARCTION; HEART MUSCLE CELL; HEART MUSCLE FIBROSIS; HEART VENTRICLE HYPERTROPHY; IN VITRO STUDY; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; VASCULARIZATION; ANIMAL; BIOLOGY; CARDIAC MYOBLAST; CARDIOMEGALY; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENETICS; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; RAT; RNA INTERFERENCE;

RATTUS;

ANIMALS; CARDIOMEGALY; COMPUTATIONAL BIOLOGY; GENE EXPRESSION; GENE EXPRESSION PROFILING; MICRORNAS; MYOBLASTS, CARDIAC; MYOCARDIAL INFARCTION; RATS; RNA INTERFERENCE; RNA, MESSENGER;

EID: 84923791608     PISSN: 22136711     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.stemcr.2014.10.010     Document Type: Article

References (58)

1. R.R. Alcendor, S. Gao, P. Zhai, D. Zablocki, E. Holle, X. Yu, B. Tian, T. Wagner, S.F. Vatner, and J. Sadoshima Sirt1 regulates aging and resistance to oxidative stress in the heart Circ. Res. 100 2007 1512 1521
2. C. Bang, S. Batkai, S. Dangwal, S.K. Gupta, A. Foinquinos, A. Holzmann, A. Just, J. Remke, K. Zimmer, and A. Zeug Cardiac fibroblast-derived microRNA passenger strand-enriched exosomes mediate cardiomyocyte hypertrophy J. Clin. Invest. 124 2014 2136 2146
3. L. Barile, V. Lionetti, E. Cervio, M. Matteucci, M. Gherghiceanu, L.M. Popescu, T. Torre, F. Siclari, T. Moccetti, and G. Vassalli Extracellular vesicles from human cardiac progenitor cells inhibit cardiomyocyte apoptosis and improve cardiac function after myocardial infarction Cardiovasc. Res. 103 2014 530 541
4. A.P. Beltrami, L. Barlucchi, D. Torella, M. Baker, F. Limana, S. Chimenti, H. Kasahara, M. Rota, E. Musso, and K. Urbanek Adult cardiac stem cells are multipotent and support myocardial regeneration Cell 114 2003 763 776
5. A. Carè, D. Catalucci, F. Felicetti, D. Bonci, A. Addario, P. Gallo, M.L. Bang, P. Segnalini, Y. Gu, and N.D. Dalton MicroRNA-133 controls cardiac hypertrophy Nat. Med. 13 2007 613 618
6. T. Chen, G. Ding, Z. Jin, M.B. Wagner, and Z. Yuan Insulin ameliorates miR-1-induced injury in H9c2 cells under oxidative stress via Akt activation Mol. Cell. Biochem. 369 2012 167 174
7. S. Chen, P. Puthanveetil, B. Feng, S.J. Matkovich, G.W. Dorn 2nd, and S. Chakrabarti Cardiac miR-133a overexpression prevents early cardiac fibrosis in diabetes J. Cell. Mol. Med. 18 2014 415 421
8. C. Cheng, Q. Wang, W. You, M. Chen, and J. Xia MiRNAs as biomarkers of myocardial infarction: a meta-analysis PLoS ONE 9 2014 e88566
9. A.R. Chugh, G.M. Beache, J.H. Loughran, N. Mewton, J.B. Elmore, J. Kajstura, P. Pappas, A. Tatooles, M.F. Stoddard, and J.A. Lima 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 11, Suppl 1 2012 S54 S64
10. S.N. Cilvik, J.I. Wang, K.J. Lavine, K. Uchida, A. Castro, C.M. Gierasch, C.J. Weinheimer, S.L. House, A. Kovacs, C.G. Nichols, and D.M. Ornitz Fibroblast growth factor receptor 1 signaling in adult cardiomyocytes increases contractility and results in a hypertrophic cardiomyopathy PLoS ONE 8 2013 e82979
11. F. Cottini, T. Hideshima, C. Xu, M. Sattler, M. Dori, L. Agnelli, E. ten Hacken, M.T. Bertilaccio, E. Antonini, and A. Neri Rescue of Hippo coactivator YAP1 triggers DNA damage-induced apoptosis in hematological cancers Nat. Med. 20 2014 599 606
12. N. Danowski, I. Manthey, H.G. Jakob, W. Siffert, J. Peters, and U.H. Frey Decreased expression of miR-133a but not of miR-1 is associated with signs of heart failure in patients undergoing coronary bypass surgery Cardiology 125 2013 125 130
13. D.P. Del Re, T. Matsuda, P. Zhai, Y. Maejima, M.R. Jain, T. Liu, H. Li, C.P. Hsu, and J. Sadoshima Mst1 promotes cardiac myocyte apoptosis through phosphorylation and inhibition of Bcl-xL Mol. Cell 54 2014 639 650
14. Z. Deng, J.F. Chen, and D.Z. Wang Transgenic overexpression of miR-133a in skeletal muscle BMC Musculoskelet. Disord. 12 2011 115
15. B.G. Galvez, M. Sampaolesi, A. Barbuti, A. Crespi, D. Covarello, S. Brunelli, A. Dellavalle, S. Crippa, G. Balconi, and I. Cuccovillo Cardiac mesoangioblasts are committed, self-renewable progenitors, associated with small vessels of juvenile mouse ventricle Cell Death Differ. 15 2008 1417 1428
16. S. Gao, M. Wassler, L. Zhang, Y. Li, J. Wang, Y. Zhang, H. Shelat, J. Williams, and Y.J. Geng MicroRNA-133a regulates insulin-like growth factor-1 receptor expression and vascular smooth muscle cell proliferation in murine atherosclerosis Atherosclerosis 232 2014 171 179
17. B. He, J. Xiao, A.J. Ren, Y.F. Zhang, H. Zhang, M. Chen, B. Xie, X.G. Gao, and Y.W. Wang Role of miR-1 and miR-133a in myocardial ischemic postconditioning J. Biomed. Sci. 18 2011 22
18. M. Hori, and K. Nishida Oxidative stress and left ventricular remodelling after myocardial infarction Cardiovasc. Res. 81 2009 457 464
19. S. Hu, M. Huang, P.K. Nguyen, Y. Gong, Z. Li, F. Jia, F. Lan, J. Liu, D. Nag, R.C. Robbins, and J.C. Wu Novel microRNA prosurvival cocktail for improving engraftment and function of cardiac progenitor cell transplantation Circulation 124 11, Suppl. 2011 S27 S34
20. T.G. Hullinger, R.L. Montgomery, A.G. Seto, B.A. Dickinson, H.M. Semus, J.M. Lynch, C.M. Dalby, K. Robinson, C. Stack, and P.A. Latimer Inhibition of miR-15 protects against cardiac ischemic injury Circ. Res. 110 2012 71 81
21. A.G. Ibrahim, K. Cheng, and E. Marbán Exosomes as critical agents of cardiac regeneration triggered by cell therapy Stem Cell Rep. 2 2014 606 619
22. K.N. Ivey, and D. Srivastava MicroRNAs as regulators of differentiation and cell fate decisions Cell Stem Cell 7 2010 36 41
23. K.N. Ivey, A. Muth, J. Arnold, F.W. King, R.F. Yeh, J.E. Fish, E.C. Hsiao, R.J. Schwartz, B.R. Conklin, H.S. Bernstein, and D. Srivastava MicroRNA regulation of cell lineages in mouse and human embryonic stem cells Cell Stem Cell 2 2008 219 229
24. Y. Jiang, M. Zhang, H. He, J. Chen, H. Zeng, J. Li, and R. Duan MicroRNA/mRNA profiling and regulatory network of intracranial aneurysm BMC Med. Genomics 6 2013 36
25. V. Labi, D. Bertele, C. Woess, D. Tischner, F.J. Bock, S. Schwemmers, H.L. Pahl, S. Geley, M. Kunze, and C.M. Niemeyer Haematopoietic stem cell survival and transplantation efficacy is limited by the BH3-only proteins Bim and Bmf EMBO Mol. Med. 5 2013 122 136
26. R. Lee, R. Feinbaum, and V. Ambros A short history of a short RNA Cell 116 2004 S89 92 1 p following S96
27. Z. Li, M.Q. Hassan, S. Volinia, A.J. van Wijnen, J.L. Stein, C.M. Croce, J.B. Lian, and G.S. Stein A microRNA signature for a BMP2-induced osteoblast lineage commitment program Proc. Natl. Acad. Sci. USA 105 2008 13906 13911
28. X.B. Liao, Z.Y. Zhang, K. Yuan, Y. Liu, X. Feng, R.R. Cui, Y.R. Hu, Z.S. Yuan, L. Gu, and S.J. Li MiR-133a modulates osteogenic differentiation of vascular smooth muscle cells Endocrinology 154 2013 3344 3352
29. N. Liu, S. Bezprozvannaya, A.H. Williams, X. Qi, J.A. Richardson, R. Bassel-Duby, and E.N. Olson microRNA-133a regulates cardiomyocyte proliferation and suppresses smooth muscle gene expression in the heart Genes Dev. 22 2008 3242 3254
30. K. Malliaras, T.S. Li, D. Luthringer, J. Terrovitis, K. Cheng, T. Chakravarty, G. Galang, Y. Zhang, F. Schoenhoff, and J. Van Eyk Safety and efficacy of allogeneic cell therapy in infarcted rats transplanted with mismatched cardiosphere-derived cells Circulation 125 2012 100 112
31. K. Malliaras, R.R. Makkar, R.R. Smith, K. Cheng, E. Wu, R.O. Bonow, L. Marbán, A. Mendizabal, E. Cingolani, and P.V. Johnston 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 2014 110 122
32. A. Martínez-Palacián, G. del Castillo, A. Suárez-Causado, M. García-Álvaro, D. de Morena-Frutos, M. Fernández, C. Roncero, I. Fabregat, B. Herrera, and A. Sánchez Mouse hepatic oval cells require Met-dependent PI3K to impair TGF-β-induced oxidative stress and apoptosis PLoS ONE 8 2013 e53108
33. S.J. Matkovich, W. Wang, Y. Tu, W.H. Eschenbacher, L.E. Dorn, G. Condorelli, A. Diwan, J.M. Nerbonne, and G.W. Dorn 2nd MicroRNA-133a protects against myocardial fibrosis and modulates electrical repolarization without affecting hypertrophy in pressure-overloaded adult hearts Circ. Res. 106 2010 166 175
34. I. Moscoso, N. Tejados, O. Barreiro, P. Sepúlveda, A. Izarra, E. Calvo, A. Dorronsoro, J.M. Salcedo, R. Sádaba, and A. Díez-Juan Podocalyxin-like protein 1 is a relevant marker for human c-kit(pos) cardiac stem cells J. Tissue Eng. Regen. Med. 2013 10.1002/term.1795 Published online July 30, 2013
35. N. Muraoka, H. Yamakawa, K. Miyamoto, T. Sadahiro, T. Umei, M. Isomi, H. Nakashima, M. Akiyama, R. Wada, and K. Inagawa MiR-133 promotes cardiac reprogramming by directly repressing Snai1 and silencing fibroblast signatures EMBO J. 33 2014 1565 1581
36. H. Naito, I. Melnychenko, M. Didié, K. Schneiderbanger, P. Schubert, S. Rosenkranz, T. Eschenhagen, and W.H. Zimmermann Optimizing engineered heart tissue for therapeutic applications as surrogate heart muscle Circulation 114 1 Suppl. 2006 I72 I78
37. H. Oh, S.B. Bradfute, T.D. Gallardo, T. Nakamura, V. Gaussin, Y. Mishina, J. Pocius, L.H. Michael, R.R. Behringer, and D.J. Garry Cardiac progenitor cells from adult myocardium: homing, differentiation, and fusion after infarction Proc. Natl. Acad. Sci. USA 100 2003 12313 12318
38. J.D. Piñon, V. Labi, A. Egle, and A. Villunger Bim and Bmf in tissue homeostasis and malignant disease Oncogene 27 Suppl 1 2008 S41 S52
39. P. Puthanveetil, A. Wan, and B. Rodrigues FoxO1 is crucial for sustaining cardiomyocyte metabolism and cell survival Cardiovasc. Res. 97 2013 393 403
40. T.E. Robey, M.K. Saiget, H. Reinecke, and C.E. Murry Systems approaches to preventing transplanted cell death in cardiac repair J. Mol. Cell. Cardiol. 45 2008 567 581
41. S.K. Sanganalmath, and R. Bolli Cell therapy for heart failure: a comprehensive overview of experimental and clinical studies, current challenges, and future directions Circ. Res. 113 2013 810 834
42. M. Schneider, S. Kostin, C.C. Strøm, M. Aplin, S. Lyngbaek, J. Theilade, M. Grigorian, C.B. Andersen, E. Lukanidin, J. Lerche Hansen, and S.P. Sheikh S100A4 is upregulated in injured myocardium and promotes growth and survival of cardiac myocytes Cardiovasc. Res. 75 2007 40 50
43. T. Takaya, K. Ono, T. Kawamura, R. Takanabe, S. Kaichi, T. Morimoto, H. Wada, T. Kita, A. Shimatsu, and K. Hasegawa MicroRNA-1 and MicroRNA-133 in spontaneous myocardial differentiation of mouse embryonic stem cells Circ. J. 73 2009 1492 1497
44. X.L. Tang, G. Rokosh, S.K. Sanganalmath, F. Yuan, H. Sato, J. Mu, S. Dai, C. Li, N. Chen, and Y. Peng Intracoronary administration of cardiac progenitor cells alleviates left ventricular dysfunction in rats with a 30-day-old infarction Circulation 121 2010 293 305
45. K. Tateishi, E. Ashihara, N. Takehara, T. Nomura, S. Honsho, T. Nakagami, S. Morikawa, T. Takahashi, T. Ueyama, H. Matsubara, and H. Oh Clonally amplified cardiac stem cells are regulated by Sca-1 signaling for efficient cardiovascular regeneration J. Cell Sci. 120 2007 1791 1800
46. M. Tiburcy, M. Didié, O. Boy, P. Christalla, S. Döker, H. Naito, B.C. Karikkineth, A. El-Armouche, M. Grimm, and M. Nose Terminal differentiation, advanced organotypic maturation, and modeling of hypertrophic growth in engineered heart tissue Circ. Res. 109 2011 1105 1114
47. W.H. Townley-Tilson, T.E. Callis, and D. Wang MicroRNAs 1, 133, and 206: critical factors of skeletal and cardiac muscle development, function, and disease Int. J. Biochem. Cell Biol. 42 2010 1252 1255
48. R. Troncoso, C. Ibarra, J.M. Vicencio, E. Jaimovich, and S. Lavandero New insights into IGF-1 signaling in the heart Trends Endocrinol. Metab. 25 2014 128 137
49. M. Vantler, B.C. Karikkineth, H. Naito, M. Tiburcy, M. Didié, M. Nose, S. Rosenkranz, and W.H. Zimmermann PDGF-BB protects cardiomyocytes from apoptosis and improves contractile function of engineered heart tissue J. Mol. Cell. Cardiol. 48 2010 1316 1323
50. X. Wang, T. Zhao, W. Huang, T. Wang, J. Qian, M. Xu, E.G. Kranias, Y. Wang, and G.C. Fan Hsp20-engineered mesenchymal stem cells are resistant to oxidative stress via enhanced activation of Akt and increased secretion of growth factors Stem Cells 27 2009 3021 3031
51. Y. Wang, L. Li, B.T. Moore, X.H. Peng, X. Fang, J.M. Lappe, R.R. Recker, and P. Xiao MiR-133a in human circulating monocytes: a potential biomarker associated with postmenopausal osteoporosis PLoS ONE 7 2012 e34641
52. X. Wang, Q. Li, Q. Hu, P. Suntharalingam, A.H. From, and J. Zhang Intra-myocardial injection of both growth factors and heart derived Sca-1+/CD31- cells attenuates post-MI LV remodeling more than does cell transplantation alone: neither intervention enhances functionally significant cardiomyocyte regeneration PLoS ONE 9 2014 e95247
53. S.S. Yildirim, D. Akman, D. Catalucci, and B. Turan Relationship between downregulation of miRNAs and increase of oxidative stress in the development of diabetic cardiac dysfunction: junctin as a target protein of miR-1 Cell Biochem. Biophys. 67 2013 1397 1408
54. L. Zentilin, U. Puligadda, V. Lionetti, S. Zacchigna, C. Collesi, L. Pattarini, G. Ruozi, S. Camporesi, G. Sinagra, and M. Pepe Cardiomyocyte VEGFR-1 activation by VEGF-B induces compensatory hypertrophy and preserves cardiac function after myocardial infarction FASEB J. 24 2010 1467 1478
55. Y. Zhao, E. Samal, and D. Srivastava Serum response factor regulates a muscle-specific microRNA that targets Hand2 during cardiogenesis Nature 436 2005 214 220
56. Y. Zhao, J.F. Ransom, A. Li, V. Vedantham, M. von Drehle, A.N. Muth, T. Tsuchihashi, M.T. McManus, R.J. Schwartz, and D. Srivastava Dysregulation of cardiogenesis, cardiac conduction, and cell cycle in mice lacking miRNA-1-2 Cell 129 2007 303 317
57. W.H. Zimmermann, C. Fink, D. Kralisch, U. Remmers, J. Weil, and T. Eschenhagen Three-dimensional engineered heart tissue from neonatal rat cardiac myocytes Biotechnol. Bioeng. 68 2000 106 114
58. W.H. Zimmermann, K. Schneiderbanger, P. Schubert, M. Didié, F. Münzel, J.F. Heubach, S. Kostin, W.L. Neuhuber, and T. Eschenhagen Tissue engineering of a differentiated cardiac muscle construct Circ. Res. 90 2002 223 230