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BioMed Research International
Volume 2015, Article ID 105620, 15 pages
http://dx.doi.org/10.1155/2015/105620
Review Article

Update on the Pathogenic Implications and Clinical Potential of microRNAs in Cardiac Disease

1Center of Regenerative Medicine in Barcelona (CMRB), Barcelona Biomedical Research Park, Dr. Aiguader 88, 08003 Barcelona, Spain
2Center for Networked Biomedical Research on Bioengineering, Biomaterials and Nanomedicine (CIBER-BBN), Spain
3Control of Stem Cell Potency Group, Institute for Bioengineering of Catalonia (IBEC), Barcelona Science Park, Baldiri Reixac 15-21, 08028 Barcelona, Spain
4Institució Catalana de Recerca i Estudis Avançats (ICREA), Spain

Received 18 September 2014; Accepted 19 December 2014

Academic Editor: Chi-Hsiao Yeh

Copyright © 2015 Mario Notari et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. B. B. Kelly, J. Narula, and V. Fuster, “Recognizing global burden of cardiovascular disease and related chronic diseases,” The Mount Sinai Journal of Medicine, vol. 79, no. 6, pp. 632–640, 2012. View at Publisher · View at Google Scholar · View at Scopus
  2. L. H. Opie, P. J. Commerford, B. J. Gersh, and M. A. Pfeffer, “Controversies in ventricular remodelling,” The Lancet, vol. 367, no. 9507, pp. 356–367, 2006. View at Publisher · View at Google Scholar
  3. R. S. Whelan, V. Kaplinskiy, and R. N. Kitsis, “Cell death in the pathogenesis of heart disease: mechanisms and significance,” Annual Review of Physiology, vol. 72, pp. 19–44, 2010. View at Publisher · View at Google Scholar · View at Scopus
  4. A. P. Beltrami, K. Urbanek, J. Kajstura et al., “Evidence that human cardiac myocytes divide after myocardial infarction,” The New England Journal of Medicine, vol. 344, no. 23, pp. 1750–1757, 2001. View at Publisher · View at Google Scholar
  5. D. Fan, A. Takawale, J. Lee, and Z. Kassiri, “Cardiac fibroblasts, fibrosis and extracellular matrix remodeling in heart disease,” Fibrogenesis and Tissue Repair, vol. 5, article 15, 2012. View at Publisher · View at Google Scholar · View at Scopus
  6. A. S. Go, D. Mozaffarian, V. L. Roger et al., “Heart disease and stroke statistics—2014 update: a report from the American Heart Association,” Circulation, vol. 129, pp. e28–e292, 2014. View at Publisher · View at Google Scholar
  7. J. C. Garbern and R. T. Lee, “Cardiac stem cell therapy and the promise of heart regeneration,” Cell Stem Cell, vol. 12, no. 6, pp. 689–698, 2013. View at Publisher · View at Google Scholar · View at Scopus
  8. S. E. Senyo, R. T. Lee, and B. Kuhn, “Cardiac regeneration based on mechanisms of cardiomyocyte proliferation and differentiation,” Stem Cell Research, vol. 13, no. 3, pp. 532–541, 2014. View at Publisher · View at Google Scholar
  9. E. R. Porrello and E. N. Olson, “A neonatal blueprint for cardiac regeneration,” Stem Cell Research, vol. 13, no. 3, pp. 556–570, 2014. View at Publisher · View at Google Scholar
  10. F. B. Engel, M. Schebesta, M. T. Duong et al., “p38 MAP kinase inhibition enables proliferation of adult mammalian cardiomyocytes,” Genes & Development, vol. 19, no. 10, pp. 1175–1187, 2005. View at Publisher · View at Google Scholar · View at Scopus
  11. K. Bersell, S. Arab, B. Haring, and B. Kühn, “Neuregulin1/ErbB4 signaling induces cardiomyocyte proliferation and repair of heart injury,” Cell, vol. 138, no. 2, pp. 257–270, 2009. View at Publisher · View at Google Scholar · View at Scopus
  12. D. Srivastava and M. Ieda, “Critical factors for cardiac reprogramming,” Circulation research, vol. 111, no. 1, pp. 5–8, 2012. View at Publisher · View at Google Scholar · View at Scopus
  13. D. P. Bartel, “MicroRNAs: target recognition and regulatory functions,” Cell, vol. 136, no. 2, pp. 215–233, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. E. van Rooij, L. B. Sutherland, N. Liu et al., “A signature pattern of stress-responsive microRNAs that can evoke cardiac hypertrophy and heart failure,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 48, pp. 18255–18260, 2006. View at Publisher · View at Google Scholar · View at Scopus
  15. A. Bonauer, G. Carmona, M. Iwasaki et al., “MicroRNA-92a controls angiogenesis and functional recovery of ischemic tissues in Mice,” Science, vol. 324, no. 5935, pp. 1710–1713, 2009. View at Publisher · View at Google Scholar · View at Scopus
  16. E. van Rooij, L. B. Sutherland, J. E. Thatcher et al., “Dysregulation of microRNAs after myocardial infarction reveals a role of miR-29 in cardiac fibrosis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 35, pp. 13027–13032, 2008. View at Publisher · View at Google Scholar · View at Scopus
  17. T. Thum, P. Galuppo, C. Wolf et al., “MicroRNAs in the human heart: a clue to fetal gene reprogramming in heart failure,” Circulation, vol. 116, no. 3, pp. 258–267, 2007. View at Publisher · View at Google Scholar
  18. S. Ikeda, S. W. Kong, J. Lu et al., “Altered microRNA expression in human heart disease,” Physiological Genomics, vol. 31, no. 3, pp. 367–373, 2007. View at Publisher · View at Google Scholar
  19. E. van Rooij and E. N. Olson, “MicroRNA therapeutics for cardiovascular disease: opportunities and obstacles,” Nature Reviews Drug Discovery, vol. 11, no. 11, pp. 860–872, 2012. View at Publisher · View at Google Scholar · View at Scopus
  20. T. Thum, “MicroRNA therapeutics in cardiovascular medicine,” EMBO Molecular Medicine, vol. 4, no. 1, pp. 3–14, 2012. View at Publisher · View at Google Scholar · View at Scopus
  21. E. M. Small, R. J. A. Frost, and E. N. Olson, “MicroRNAs add a new dimension to cardiovascular disease,” Circulation, vol. 121, no. 8, pp. 1022–1032, 2010. View at Publisher · View at Google Scholar · View at Scopus
  22. A. J. Tijsen, Y. M. Pinto, and E. E. Creemers, “Circulating microRNAs as diagnostic biomarkers for cardiovascular diseases,” The American Journal of Physiology—Heart and Circulatory Physiology, vol. 303, no. 9, pp. H1085–H1095, 2012. View at Publisher · View at Google Scholar · View at Scopus
  23. Y. Tomari and P. D. Zamore, “MicroRNA biogenesis: drosha can't cut it without a partner,” Current Biology, vol. 15, no. 2, pp. R61–R64, 2005. View at Publisher · View at Google Scholar · View at Scopus
  24. E. Hergenreider, S. Heydt, K. Tréguer et al., “Atheroprotective communication between endothelial cells and smooth muscle cells through miRNAs,” Nature Cell Biology, vol. 14, pp. 249–256, 2012. View at Publisher · View at Google Scholar · View at Scopus
  25. L. Xu, B.-F. Yang, and J. Ai, “MicroRNA transport: a new way in cell communication,” Journal of Cellular Physiology, vol. 228, no. 8, pp. 1713–1719, 2013. View at Publisher · View at Google Scholar · View at Scopus
  26. C. Bang, S. Batkai, S. Dangwal et al., “Cardiac fibroblast-derived microRNA passenger strand-enriched exosomes mediate cardiomyocyte hypertrophy,” The Journal of Clinical Investigation, vol. 124, no. 5, pp. 2136–2146, 2014. View at Publisher · View at Google Scholar · View at Scopus
  27. J. Liu, M. A. Valencia-Sanchez, G. J. Hannon, and R. Parker, “MicroRNA-dependent localization of targeted mRNAs to mammalian P-bodies,” Nature Cell Biology, vol. 7, no. 7, pp. 719–723, 2005. View at Publisher · View at Google Scholar · View at Scopus
  28. M. Kulkarni, S. Ozgur, and G. Stoecklin, “On track with P-bodies,” Biochemical Society Transactions, vol. 38, no. 1, pp. 242–251, 2010. View at Publisher · View at Google Scholar · View at Scopus
  29. J. Winter, S. Jung, S. Keller, R. I. Gregory, and S. Diederichs, “Many roads to maturity: microRNA biogenesis pathways and their regulation,” Nature Cell Biology, vol. 11, no. 3, pp. 228–234, 2009. View at Publisher · View at Google Scholar · View at Scopus
  30. D. Baek, J. Villén, C. Shin, F. D. Camargo, S. P. Gygi, and D. P. Bartel, “The impact of microRNAs on protein output,” Nature, vol. 455, pp. 64–71, 2008. View at Publisher · View at Google Scholar
  31. M. Selbach, B. Schwanhäusser, N. Thierfelder, Z. Fang, R. Khanin, and N. Rajewsky, “Widespread changes in protein synthesis induced by microRNAs,” Nature, vol. 455, no. 7209, pp. 58–63, 2008. View at Publisher · View at Google Scholar · View at Scopus
  32. R. Yi and E. Fuchs, “MicroRNAs and their roles in mammalian stem cells,” Journal of Cell Science, vol. 124, pp. 1775–1783, 2011. View at Publisher · View at Google Scholar · View at Scopus
  33. J. Pulecio, E. Nivet, I. Sancho-Martinez et al., “Conversion of human fibroblasts into monocyte-like progenitor cells,” Stem Cells, vol. 32, no. 11, pp. 2923–2938, 2014. View at Publisher · View at Google Scholar
  34. A. Kozomara and S. Griffiths-Jones, “miRBase: integrating microRNA annotation and deep-sequencing data,” Nucleic Acids Research, vol. 39, no. 1, pp. D152–D157, 2011. View at Publisher · View at Google Scholar · View at Scopus
  35. A. Kozomara and S. Griffiths-Jones, “MiRBase: annotating high confidence microRNAs using deep sequencing data,” Nucleic Acids Research, vol. 42, no. 1, pp. D68–D73, 2014. View at Publisher · View at Google Scholar · View at Scopus
  36. I. Lyons, L. M. Parsons, L. Hartley et al., “Myogenic and morphogenetic defects in the heart tubes of murine embryos lacking the homeo box gene Nkx2-5,” Genes and Development, vol. 9, no. 13, pp. 1654–1666, 1995. View at Publisher · View at Google Scholar · View at Scopus
  37. Y. Zhao, J. F. Ransom, A. Li et al., “Dysregulation of cardiogenesis, cardiac conduction, and cell cycle in mice lacking miRNA-1-2,” Cell, vol. 129, no. 2, pp. 303–317, 2007. View at Publisher · View at Google Scholar · View at Scopus
  38. P. A. da Costa Martins, M. Bourajjaj, M. Gladka et al., “Conditional Dicer gene deletion in the postnatal myocardium provokes spontaneous cardiac remodeling,” Circulation, vol. 118, no. 15, pp. 1567–1576, 2008. View at Publisher · View at Google Scholar · View at Scopus
  39. Y. Zhao, E. Samal, and D. Srivastava, “Serum response factor regulates a muscle-specific microRNA that targets Hand2 during cardiogenesis,” Nature, vol. 436, no. 7048, pp. 214–220, 2005. View at Publisher · View at Google Scholar · View at Scopus
  40. J.-F. Chen, E. M. Mandel, J. M. Thomson et al., “The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation,” Nature Genetics, vol. 38, no. 2, pp. 228–233, 2006. View at Publisher · View at Google Scholar · View at Scopus
  41. K. N. Ivey, A. Muth, J. Arnold et al., “MicroRNA regulation of cell lineages in mouse and human embryonic stem cells,” Cell Stem Cell, vol. 2, no. 3, pp. 219–229, 2008. View at Publisher · View at Google Scholar · View at Scopus
  42. N. Liu, S. Bezprozvannaya, A. H. Williams et al., “microRNA-133a regulates cardiomyocyte proliferation and suppresses smooth muscle gene expression in the heart,” Genes & Development, vol. 22, no. 23, pp. 3242–3254, 2008. View at Publisher · View at Google Scholar · View at Scopus
  43. S.-Y. Lee, O. Ham, M.-J. Cha et al., “The promotion of cardiogenic differentiation of hMSCs by targeting epidermal growth factor receptor using microRNA-133a,” Biomaterials, vol. 34, no. 1, pp. 92–99, 2013. View at Publisher · View at Google Scholar · View at Scopus
  44. J. P. G. Sluijter, A. van Mil, P. van Vliet et al., “MicroRNA-1 and-499 regulate differentiation and proliferation in human-derived cardiomyocyte progenitor cells,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 30, no. 4, pp. 859–868, 2010. View at Publisher · View at Google Scholar · View at Scopus
  45. P. S. Mitchell, R. K. Parkin, E. M. Kroh et al., “Circulating microRNAs as stable blood-based markers for cancer detection,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 30, pp. 10513–10518, 2008. View at Publisher · View at Google Scholar · View at Scopus
  46. G. W. Dorn, S. J. Matkovich, W. H. Eschenbacher, and Y. Zhang, “A human 3′ miR-499 mutation alters cardiac mRNA targeting and function,” Circulation Research, vol. 110, no. 7, pp. 958–967, 2012. View at Publisher · View at Google Scholar · View at Scopus
  47. J. T. C. Shieh, Y. Huang, J. Gilmore, and D. Srivastava, “Elevated miR-499 levels blunt the cardiac stress response,” PLoS ONE, vol. 6, no. 5, Article ID e19481, 2011. View at Publisher · View at Google Scholar · View at Scopus
  48. A. Ventura, A. G. Young, M. M. Winslow et al., “Targeted deletion reveals essential and overlapping functions of the miR-17~92 family of miRNA clusters,” Cell, vol. 132, no. 5, pp. 875–886, 2008. View at Publisher · View at Google Scholar · View at Scopus
  49. J. Wang, S. B. Greene, M. Bonilla-Claudio et al., “Bmp signaling regulates myocardial differentiation from cardiac progenitors through a MicroRNA-mediated mechanism,” Developmental Cell, vol. 19, no. 6, pp. 903–912, 2010. View at Publisher · View at Google Scholar · View at Scopus
  50. P. Sirish, J. E. López, N. Li et al., “MicroRNA profiling predicts a variance in the proliferative potential of cardiac progenitor cells derived from neonatal and adult murine hearts,” Journal of Molecular and Cellular Cardiology, vol. 52, no. 1, pp. 264–272, 2012. View at Publisher · View at Google Scholar · View at Scopus
  51. T. Hosoda, H. Zheng, M. Cabral-da-Silva et al., “Human cardiac stem cell differentiation is regulated by a mircrine mechanism,” Circulation, vol. 123, pp. 1287–1296, 2011. View at Publisher · View at Google Scholar
  52. S. Hu, M. Huang, P. K. Nguyen et al., “Novel microRNA prosurvival cocktail for improving engraftment and function of cardiac progenitor cell transplantation,” Circulation, vol. 124, no. 11, pp. S27–S34, 2011. View at Publisher · View at Google Scholar · View at Scopus
  53. P. A. Tsonis, “Regeneration in vertebrates,” Developmental Biology, vol. 221, no. 2, pp. 273–284, 2000. View at Publisher · View at Google Scholar · View at Scopus
  54. R. O. Becker, S. Chapin, and R. Sherry, “Regeneration of the ventricular myocardium in amphibians,” Nature, vol. 248, no. 5444, pp. 145–147, 1974. View at Publisher · View at Google Scholar · View at Scopus
  55. J. P. Brockes, “Amphibian limb regeneration: rebuilding a complex structure,” Science, vol. 276, no. 5309, pp. 81–87, 1997. View at Publisher · View at Google Scholar · View at Scopus
  56. J. P. Brockes and A. Kumar, “Comparative aspects of animal regeneration,” Annual Review of Cell and Developmental Biology, vol. 24, pp. 525–549, 2008. View at Publisher · View at Google Scholar
  57. Á. Raya, A. Consiglio, Y. Kawakami, C. Rodriguez-Esteban, and J. C. Izpisúa-Belmonte, “The zebrafish as a model of heart regeneration,” Cloning and Stem Cells, vol. 6, no. 4, pp. 345–351, 2004. View at Publisher · View at Google Scholar · View at Scopus
  58. C. Jopling, E. Sleep, M. Raya, M. Martí, A. Raya, and J. C. I. Belmonte, “Zebrafish heart regeneration occurs by cardiomyocyte dedifferentiation and proliferation,” Nature, vol. 464, no. 7288, pp. 606–609, 2010. View at Publisher · View at Google Scholar · View at Scopus
  59. E. J. Thatcher, I. Paydar, K. K. Anderson, and J. G. Patton, “Regulation of zebrafish fin regeneration by microRNAs,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 47, pp. 18384–18389, 2008. View at Publisher · View at Google Scholar · View at Scopus
  60. E. R. Porrello, A. I. Mahmoud, E. Simpson et al., “Transient regenerative potential of the neonatal mouse heart,” Science, vol. 331, no. 6020, pp. 1078–1080, 2011. View at Publisher · View at Google Scholar · View at Scopus
  61. J. L. Whited and C. J. Tabin, “Regeneration review reprise,” Journal of Biology, vol. 9, no. 2, article 15, 2010. View at Publisher · View at Google Scholar · View at Scopus
  62. V. P. Yin, J. M. Thomson, R. Thummel, D. R. Hyde, S. M. Hammond, and K. D. Poss, “Fgf-dependent depletion of microRNA-133 promotes appendage regeneration in zebrafish,” Genes & Development, vol. 22, no. 6, pp. 728–733, 2008. View at Publisher · View at Google Scholar · View at Scopus
  63. S. U. Morton, P. J. Scherz, K. R. Cordes, K. N. Ivey, D. Y. R. Stainier, and D. Srivastava, “microRNA-138 modulates cardiac patterning during embryonic development,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 46, pp. 17830–17835, 2008. View at Publisher · View at Google Scholar · View at Scopus
  64. E. R. Porrello, B. A. Johnson, A. B. Aurora et al., “MiR-15 family regulates postnatal mitotic arrest of cardiomyocytes,” Circulation Research, vol. 109, no. 6, pp. 670–679, 2011. View at Publisher · View at Google Scholar · View at Scopus
  65. M. J. Bueno and M. Malumbres, “MicroRNAs and the cell cycle,” Biochimica et Biophysica Acta—Molecular Basis of Disease, vol. 1812, no. 5, pp. 592–601, 2011. View at Publisher · View at Google Scholar · View at Scopus
  66. T. G. Hullinger, R. L. Montgomery, A. G. Seto et al., “Inhibition of miR-15 protects against cardiac ischemic injury,” Circulation Research, vol. 110, pp. 71–81, 2012. View at Publisher · View at Google Scholar
  67. S. E. Senyo, M. L. Steinhauser, C. L. Pizzimenti et al., “Mammalian heart renewal by pre-existing cardiomyocytes,” Nature, vol. 493, no. 7432, pp. 433–436, 2013. View at Publisher · View at Google Scholar
  68. A. Eulalio, M. Mano, M. D. Ferro et al., “Functional screening identifies miRNAs inducing cardiac regeneration,” Nature, vol. 492, no. 7429, pp. 376–381, 2012. View at Publisher · View at Google Scholar · View at Scopus
  69. D. Cirera-Salinas, M. Pauta, R. M. Allen et al., “Mir-33 regulates cell proliferation and cell cycle progression,” Cell Cycle, vol. 11, no. 5, pp. 922–933, 2012. View at Publisher · View at Google Scholar · View at Scopus
  70. A. Dávalos, L. Goedeke, P. Smibert et al., “miR-33a/b contribute to the regulation of fatty acid metabolism and insulin signaling,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 22, pp. 9232–9237, 2011. View at Publisher · View at Google Scholar · View at Scopus
  71. H. el Azzouzi, S. Leptidis, E. Dirkx et al., “The hypoxia-inducible microRNA cluster miR-199a∼214 targets myocardial PPARδ and impairs mitochondrial fatty acid oxidation,” Cell metabolism, vol. 18, pp. 341–354, 2013. View at Publisher · View at Google Scholar
  72. J. Chen, Z.-P. Huang, H. Y. Seok et al., “Mir-17-92 cluster is required for and sufficient to induce cardiomyocyte proliferation in postnatal and adult hearts,” Circulation Research, vol. 112, no. 12, pp. 1557–1566, 2013. View at Publisher · View at Google Scholar · View at Scopus
  73. V. Olive, M. J. Bennett, J. C. Walker et al., “miR-19 is a key oncogenic component of mir-17-92,” Genes and Development, vol. 23, no. 24, pp. 2839–2849, 2009. View at Publisher · View at Google Scholar · View at Scopus
  74. Y. Cheng, R. Ji, J. Yue et al., “MicroRNAs are aberrantly expressed in hypertrophic heart: do they play a pole in cardiac hypertrophy?” The American Journal of Pathology, vol. 170, no. 6, pp. 1831–1840, 2007. View at Publisher · View at Google Scholar · View at Scopus
  75. P. K. Rao, Y. Toyama, R. Chiang et al., “Loss of cardiac microRNA-mediated regulation leads to dilated cardiomyopathy and heart failure,” Circulation Research, vol. 105, pp. 585–594, 2009. View at Publisher · View at Google Scholar
  76. S. J. Matkovich, D. J. van Booven, K. A. Youker et al., “Reciprocal regulation of myocardial microRNAs and messenger RNA in human cardiomyopathy and reversal of the microRNA signature by biomechanical support,” Circulation, vol. 119, no. 9, pp. 1263–1271, 2009. View at Publisher · View at Google Scholar · View at Scopus
  77. M. Vitaloni, J. Pulecio, J. Bilic, B. Kuebler, L. Laricchia-Robbio, and J. C. I. Belmonte, “MicroRNAs contribute to induced pluripotent stem cell somatic donor memory,” The Journal of Biological Chemistry, vol. 289, no. 4, pp. 2084–2098, 2014. View at Publisher · View at Google Scholar · View at Scopus
  78. C. E. Murry, R. B. Jennings, and K. A. Reimer, “Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium,” Circulation, vol. 74, no. 5, pp. 1124–1136, 1986. View at Publisher · View at Google Scholar · View at Scopus
  79. M. Chiong, Z. V. Wang, Z. Pedrozo et al., “Cardiomyocyte death: mechanisms and translational implications,” Cell Death & Disease, vol. 2, p. e244, 2011. View at Publisher · View at Google Scholar
  80. G. W. Dorn II, “Apoptotic and non-apoptotic programmed cardiomyocyte death in ventricular remodelling,” Cardiovascular Research, vol. 81, no. 3, pp. 465–473, 2009. View at Publisher · View at Google Scholar · View at Scopus
  81. A. B. Aurora, A. I. Mahmoud, X. Luo et al., “MicroRNA-214 protects the mouse heart from ischemic injury by controlling Ca2+ overload and cell death,” Journal of Clinical Investigation, vol. 122, no. 4, pp. 1222–1232, 2012. View at Publisher · View at Google Scholar · View at Scopus
  82. S. Dong, Y. Cheng, J. Yang et al., “MicroRNA expression signature and the role of microRNA-21 in the early phase of acute myocardial infarction,” Journal of Biological Chemistry, vol. 284, no. 43, pp. 29514–29525, 2009. View at Publisher · View at Google Scholar · View at Scopus
  83. T. A. Harris, M. Yamakuchi, M. Ferlito, J. T. Mendell, and C. J. Lowenstein, “MicroRNA-126 regulates endothelial expression of vascular cell adhesion molecule 1,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 5, pp. 1516–1521, 2008. View at Publisher · View at Google Scholar · View at Scopus
  84. A. Zernecke, K. Bidzhekov, H. Noels et al., “Delivery of microRNA-126 by apoptotic bodies induces CXCL12-dependent vascular protection,” Science Signaling, vol. 2, no. 100, article ra81, 2009. View at Publisher · View at Google Scholar · View at Scopus
  85. J.-X. Wang, J.-Q. Jiao, Q. Li et al., “MiR-499 regulates mitochondrial dynamics by targeting calcineurin and dynamin-related protein-1,” Nature Medicine, vol. 17, no. 1, pp. 71–78, 2011. View at Publisher · View at Google Scholar · View at Scopus
  86. L. Qian, L. W. Van Laake, Y. Huang, S. Liu, M. F. Wendland, and D. Srivastava, “miR-24 inhibits apoptosis and represses Bim in mouse cardiomyocytes,” The Journal of Experimental Medicine, vol. 208, no. 3, pp. 549–560, 2011. View at Publisher · View at Google Scholar · View at Scopus
  87. M. A. Konstam, D. G. Kramer, A. R. Patel, M. S. Maron, and J. E. Udelson, “Left ventricular remodeling in heart failure: current concepts in clinical significance and assessment,” JACC: Cardiovascular Imaging, vol. 4, no. 1, pp. 98–108, 2011. View at Publisher · View at Google Scholar · View at Scopus
  88. S. Roy, S. Khanna, S.-R. A. Hussain et al., “MicroRNA expression in response to murine myocardial infarction: miR-21 regulates fibroblast metalloprotease-2 via phosphatase and tensin homologue,” Cardiovascular Research, vol. 82, no. 1, pp. 21–29, 2009. View at Publisher · View at Google Scholar · View at Scopus
  89. F. G. Spinale, “Matrix metalloproteinases: regulation and dysregulation in the failing heart,” Circulation Research, vol. 90, no. 5, pp. 520–530, 2002. View at Publisher · View at Google Scholar · View at Scopus
  90. T. Thum, C. Gross, J. Fiedler et al., “MicroRNA-21 contributes to myocardial disease by stimulating MAP kinase signalling in fibroblasts,” Nature, vol. 456, no. 7224, pp. 980–984, 2008. View at Publisher · View at Google Scholar
  91. M. Tatsuguchi, H. Y. Seok, T. E. Callis et al., “Expression of microRNAs is dynamically regulated during cardiomyocyte hypertrophy,” Journal of Molecular and Cellular Cardiology, vol. 42, no. 6, pp. 1137–1141, 2007. View at Publisher · View at Google Scholar · View at Scopus
  92. D. Sayed, S. Rane, J. Lypowy et al., “MicroRNA-21 targets Sprouty2 and promotes cellular outgrowths,” Molecular Biology of the Cell, vol. 19, no. 8, pp. 3272–3282, 2008. View at Publisher · View at Google Scholar · View at Scopus
  93. Y. Cheng, X. Liu, S. Zhang, Y. Lin, J. Yang, and C. Zhang, “MicroRNA-21 protects against the H2O2-induced injury on cardiac myocytes via its target gene PDCD4,” Journal of Molecular and Cellular Cardiology, vol. 47, no. 1, pp. 5–14, 2009. View at Publisher · View at Google Scholar · View at Scopus
  94. L. Cushing, P. P. Kuang, J. Qian et al., “miR-29 is a major regulator of genes associated with pulmonary fibrosis,” American Journal of Respiratory Cell and Molecular Biology, vol. 45, no. 2, pp. 287–294, 2011. View at Publisher · View at Google Scholar
  95. E. van Rooij, L. B. Sutherland, X. Qi, J. A. Richardson, J. Hill, and E. N. Olson, “Control of stress-dependent cardiac growth and gene expression by a microRNA,” Science, vol. 316, no. 5824, pp. 575–579, 2007. View at Publisher · View at Google Scholar · View at Scopus
  96. M. Vanderheyden, W. Mullens, L. Delrue et al., “Myocardial gene expression in heart failure patients treated with cardiac resynchronization therapy: responders versus nonresponders,” Journal of the American College of Cardiology, vol. 51, no. 2, pp. 129–136, 2008. View at Publisher · View at Google Scholar · View at Scopus
  97. R. L. Montgomery, T. G. Hullinger, H. M. Semus et al., “Therapeutic inhibition of miR-208a improves cardiac function and survival during heart failure,” Circulation, vol. 124, no. 14, pp. 1537–1547, 2011. View at Publisher · View at Google Scholar · View at Scopus
  98. C. E. Grueter, E. van Rooij, B. A. Johnson et al., “A cardiac microRNA governs systemic energy homeostasis by regulation of MED13,” Cell, vol. 149, no. 3, pp. 671–683, 2012. View at Publisher · View at Google Scholar · View at Scopus
  99. F. Ahmad, J. G. Seidman, and C. E. Seidman, “The genetic basis for cardiac remodeling,” Annual Review of Genomics and Human Genetics, vol. 6, pp. 185–216, 2005. View at Publisher · View at Google Scholar · View at Scopus
  100. B. Yang, H. Lin, J. Xiao et al., “The muscle-specific microRNA miR-1 regulates cardiac arrhythmogenic potential by targeting GJA1 and KCNJ2,” Nature Medicine, vol. 13, no. 4, pp. 486–491, 2007. View at Publisher · View at Google Scholar · View at Scopus
  101. P. Richardson, R. W. McKenna, M. Bristow et al., “Report of the 1995 world health organization/international society and federation of cardiology task force on the definition and classification of cardiomyopathies,” Circulation, vol. 93, no. 5, pp. 841–842, 1996. View at Publisher · View at Google Scholar · View at Scopus
  102. B. H. Chew, S. S. Ghazali, M. Ismail, J. Haniff, and M. A. Bujang, “Age 60 years was an independent risk factor for diabetes-related complications despite good control of cardiovascular risk factors in patients with type 2 diabetes mellitus,” Experimental Gerontology, vol. 48, no. 5, pp. 485–491, 2013. View at Publisher · View at Google Scholar · View at Scopus
  103. S. Rawal, P. Manning, and R. Katare, “Cardiovascular microRNAs: as modulators and diagnostic biomarkers of diabetic heart disease,” Cardiovascular Diabetology, vol. 13, article 44, 2014. View at Publisher · View at Google Scholar · View at Scopus
  104. A. D. McClelland and P. Kantharidis, “microRNA in the development of diabetic complications,” Clinical Science, vol. 126, no. 2, pp. 95–110, 2014. View at Publisher · View at Google Scholar · View at Scopus
  105. K. C. Vickers, K.-A. Rye, and F. Tabet, “MicroRNAs in the onset and development of cardiovascular disease,” Clinical Science, vol. 126, no. 3, pp. 183–194, 2014. View at Publisher · View at Google Scholar · View at Scopus
  106. M. Jaguszewski, J. Osipova, J.-R. Ghadri et al., “A signature of circulating microRNAs differentiates takotsubo cardiomyopathy from acute myocardial infarction,” European Heart Journal, vol. 35, no. 15, pp. 999–1006, 2014. View at Publisher · View at Google Scholar · View at Scopus
  107. J.-F. Chen, E. P. Murchison, R. Tang et al., “Targeted deletion of Dicer in the heart leads to dilated cardiomyopathy and heart failure,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 6, pp. 2111–2116, 2008. View at Publisher · View at Google Scholar · View at Scopus
  108. M. S. Ebert and P. A. Sharp, “MicroRNA sponges: progress and possibilities,” RNA, vol. 16, no. 11, pp. 2043–2050, 2010. View at Publisher · View at Google Scholar · View at Scopus
  109. F. C. Tay, J. K. Lim, H. Zhu, L. C. Hin, and S. Wang, “Using artificial microRNA sponges to achieve microRNA loss-of-function in cancer cells,” Advanced Drug Delivery Reviews, vol. 81, pp. 117–127, 2018. View at Publisher · View at Google Scholar · View at Scopus
  110. M. P. Gantier, C. E. McCoy, I. Rusinova et al., “Analysis of microRNA turnover in mammalian cells following Dicer1 ablation,” Nucleic Acids Research, vol. 39, no. 13, pp. 5692–5703, 2011. View at Publisher · View at Google Scholar · View at Scopus
  111. K. Buyens, S. C. de Smedt, K. Braeckmans et al., “Liposome based systems for systemic siRNA delivery: stability in blood sets the requirements for optimal carrier design,” Journal of Controlled Release, vol. 158, no. 3, pp. 362–370, 2012. View at Publisher · View at Google Scholar · View at Scopus
  112. K. A. Whitehead, R. Langer, and D. G. Anderson, “Knocking down barriers: advances in siRNA delivery,” Nature Reviews Drug Discovery, vol. 8, pp. 129–138, 2009. View at Google Scholar
  113. N. Jiang, X. Zhang, X. Zheng et al., “A novel in vivo siRNA delivery system specifically targeting liver cells for protection of ConA-induced fulminant hepatitis,” PLoS ONE, vol. 7, no. 9, Article ID e44138, 2012. View at Publisher · View at Google Scholar · View at Scopus
  114. R. M. Schiffelers, A. Ansari, J. Xu et al., “Cancer siRNA therapy by tumor selective delivery with ligand-targeted sterically stabilized nanoparticle,” Nucleic Acids Research, vol. 32, no. 19, article e149, 2004. View at Publisher · View at Google Scholar
  115. D. Kim, J. Hong, H.-H. Moon et al., “Anti-apoptotic cardioprotective effects of SHP-1 gene silencing against ischemia-reperfusion injury: use of deoxycholic acid-modified low molecular weight polyethyleneimine as a cardiac siRNA-carrier,” Journal of Controlled Release, vol. 168, no. 2, pp. 125–134, 2013. View at Publisher · View at Google Scholar · View at Scopus
  116. A. Santel, M. Aleku, O. Keil et al., “A novel siRNA-lipoplex technology for RNA interference in the mouse vascular endothelium,” Gene Therapy, vol. 13, no. 16, pp. 1222–1234, 2006. View at Publisher · View at Google Scholar · View at Scopus
  117. E. E. Creemers, A. J. Tijsen, and Y. M. Pinto, “Circulating microRNAs: novel biomarkers and extracellular communicators in cardiovascular disease?” Circulation Research, vol. 110, no. 3, pp. 483–495, 2012. View at Publisher · View at Google Scholar · View at Scopus
  118. H. L. Janssen, H. W. Reesink, E. J. Lawitz et al., “Treatment of HCV infection by targeting microRNA,” The New England Journal of Medicine, vol. 368, pp. 1685–1694, 2013. View at Publisher · View at Google Scholar
  119. L. Qian, Y. Huang, C. I. Spencer et al., “In vivo reprogramming of murine cardiac fibroblasts into induced cardiomyocytes,” Nature, vol. 485, no. 7400, pp. 593–598, 2012. View at Publisher · View at Google Scholar · View at Scopus
  120. M. Ieda, “Heart regeneration using reprogramming technology,” Proceedings of the Japan Academy Series B: Physical and Biological Sciences, vol. 89, no. 3, pp. 118–128, 2013. View at Publisher · View at Google Scholar · View at Scopus
  121. K. Song, Y. J. Nam, X. Luo et al., “Heart repair by reprogramming non-myocytes with cardiac transcription factors,” Nature, vol. 485, no. 7400, pp. 599–604, 2012. View at Publisher · View at Google Scholar
  122. R. Parker and U. Sheth, “P bodies and the control of mRNA translation and degradation,” Molecular Cell, vol. 25, no. 5, pp. 635–646, 2007. View at Publisher · View at Google Scholar · View at Scopus