MitomiRs Keep the Heart Beating

  • Samarjit Das
  • Hannah R. Vasanthi
  • Ramesh Parjapath
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 982)

Abstract

In this chapter, we focus on the microRNAs (miRNAs or miRs) that have been found in the mitochondrial compartment, and target either mitochondrial or nuclear encoded genes present in mitochondria, leading to an alteration of mitochondrial function. We term this subset of miRNAs as “MitomiRs”.

Keywords

Electron Transport Chain Fetal Heart Diabetic Cardiomyopathy Beating Heart Mitochondrial Fission 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

This work was supported by a Scientist Development Grant from the American Heart Association 14SDG18890049 (S.D.).

References

  1. 1.
    Rottiers V, Naar AM. MicroRNAs in metabolism and metabolic disorders. Nat Rev Mol Cell Biol. 2012;13:239–50.PubMedPubMedCentralCrossRefGoogle Scholar
  2. 2.
    Wronska A, Kurkowska-Jastrzebska I, Santulli G. Application of microRNAs in diagnosis and treatment of cardiovascular disease. Acta Physiol (Oxford). 2015;213:60–83.CrossRefGoogle Scholar
  3. 3.
    Hulsmans M, Holvoet P. MicroRNAs as early biomarkers in obesity and related metabolic and cardiovascular diseases. Curr Pharm Des. 2013;19:5704–17.PubMedCrossRefGoogle Scholar
  4. 4.
    Novak J, Kruzliak P, Bienertova-Vasku J, Slaby O, Novak M. MicroRNA-206: a promising theranostic marker. Theranostics. 2014;4:119–33.PubMedPubMedCentralCrossRefGoogle Scholar
  5. 5.
    Sayed D, Rane S, Abdellatif M. MicroRNAs challenge the status quo of therapeutic targeting. J Cardiovasc Transl Res. 2009;2:100–7.PubMedCrossRefGoogle Scholar
  6. 6.
    Ambros V. The functions of animal microRNAs. Nature. 2004;431:350–5.PubMedCrossRefGoogle Scholar
  7. 7.
    Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 2004;116:281–97.PubMedCrossRefGoogle Scholar
  8. 8.
    Hwang HW, Wentzel EA, Mendell JT. A hexanucleotide element directs microRNA nuclear import. Science. 2007;315:97–100.PubMedCrossRefGoogle Scholar
  9. 9.
    Ha M, Kim VN. Regulation of microRNA biogenesis. Nat Rev Mol Cell Biol. 2014;15:509–24.PubMedCrossRefGoogle Scholar
  10. 10.
    Bruneau BG. Signaling and transcriptional networks in heart development and regeneration. Cold Spring Harb Perspect Biol. 2013;5:a008292.PubMedPubMedCentralCrossRefGoogle Scholar
  11. 11.
    Lopaschuk GD, Collins-Nakai RL, Itoi T. Developmental changes in energy substrate use by the heart. Cardiovasc Res. 1992;26:1172–80.PubMedCrossRefGoogle Scholar
  12. 12.
    Thum T, Galuppo P, Wolf C, Fiedler J, Kneitz S, van Laake LW, Doevendans PA, Mummery CL, Borlak J, Haverich A, Gross C, Engelhardt S, Ertl G, Bauersachs J. MicroRNAs in the human heart. A clue to fetal gene reprogramming in heart failure. Circulation. 2007;116:258–67.Google Scholar
  13. 13.
    Chistiakov DA, Orekhov AN, Bobryshev YV. Cardiac-specific miRNA in cardiogenesis, heart function, and cardiac pathology (with focus on myocardial infarction). J Mol Cell Cardiol. 2016;94:107–21.PubMedCrossRefGoogle Scholar
  14. 14.
    Romaine SP, Tomaszewski M, Condorelli G, Samani NJ. MicroRNAs in cardiovascular disease: an introduction for clinicians. Heart. 2015;101:921–8.PubMedPubMedCentralCrossRefGoogle Scholar
  15. 15.
    Xin M, Olson EN, Bassel-Duby R. Mending broken hearts: cardiac development as a basis for adult heart regeneration and repair. Nat Rev Mol Cell Biol. 2013;14:529–41.PubMedPubMedCentralCrossRefGoogle Scholar
  16. 16.
    Tirziu D, Giordano FJ, Simons M. Cell communications in the heart. Circulation. 2010;122:928–37.PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    Santulli G. MicroRNAs and endothelial (dys)function. J Cell Physiol. 2016;231:1638–44.PubMedCrossRefGoogle Scholar
  18. 18.
    Santulli G, Nakashima R, Yuan Q, Marks AR. Intracellular calcium release channels: an update. J Physiol. 2017 (in press). doi:  10.1113/JP272781.
  19. 19.
    Marín-García J, Goldenthal MJ. The mitochondrial organelle and the heart. Rev Esp Cardiol. 2002;55:1293–310.PubMedCrossRefGoogle Scholar
  20. 20.
    Sack MN, Harrington LS, Jonassen AK, Mjøs OD, Yellon DM. Coordinate regulation of metabolic enzyme encoding genes during cardiac development and following carvedilol therapy in spontaneously hypertensive rats. Cardiovasc Drugs Ther. 2000;14:31–9.PubMedCrossRefGoogle Scholar
  21. 21.
    Tiivel T, Kadaya L, Kuznetsov A, Käämbre T, Peet N, Sikk P, Braun U, Ventura-Clapier R, Saks V, Seppet EK. Developmental changes in regulation of mitochondrial respiration by ADP and creatine in rat heart in vivo. Mol Cell Biochem. 2000;208:119–28.PubMedCrossRefGoogle Scholar
  22. 22.
    Hoerter JA, Kuznetsov A, Ventura-Clapier R. Functional development of the creatine kinase system in perinatal rabbit heart. Circ Res. 1991;69:665–76.PubMedCrossRefGoogle Scholar
  23. 23.
    Dröse S, Brandt U. Molecular mechanisms of superoxide production by the mitochondrial respiratory chain. Adv Exp Med Biol. Mitochondrial Oxidative Phosphorylation: Springer. 2012;748:145–69.Google Scholar
  24. 24.
    Marín-García J. Heart failure: bench to bedside. New York: Humana Press; 2010.CrossRefGoogle Scholar
  25. 25.
    Nulton-Persson AC, Szweda LI. Modulation of mitochondrial function by hydrogen peroxide. J Biol Chem. 2001;276:23357–61.PubMedCrossRefGoogle Scholar
  26. 26.
    Wang JX, Jiao JQ, Li Q, Long B, Wang K, Liu JP, Li YR, Li PF. miR-499 regulates mitochondrial dynamics by targeting calcineurin and dynamin-related protein-1. Nat Med. 2011;17:71–8.PubMedCrossRefGoogle Scholar
  27. 27.
    Li J, Donath S, Li Y, Qin D, Prabhakar BS, Li P. miR-30 regulates mitochondrial fission through targeting p53 and the dynamin-related protein-1 pathway. PLoS Genet. 2010;6:e1000795.PubMedPubMedCentralCrossRefGoogle Scholar
  28. 28.
    Long B, Wang K, Li N, Murtaza I, Xiao JY, Fan YY, Liu CY, Li WH, Cheng Z, Li P. miR-761 regulates the mitochondrial network by targeting mitochondrial fission factor. Free Radic Biol Med. 2013;65:371–9.PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    Li J, Li Y, Jiao J, Wang J, Li Y, Qin D, Li P. Mitofusin 1 is negatively regulated by microRNA 140 in cardiomyocyte apoptosis. Mol Cell Biol. 2014;34:1788–99.PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    Das S, Ferlito M, Kent OA, Fox-Talbot K, Wang R, Liu D, Raghavachari N, Yang Y, Wheelan SJ, Murphy E, Steenbergen C. Nuclear miRNA regulates the mitochondrial genome in the heart. Circ Res. 2012;110:1596–603.PubMedPubMedCentralCrossRefGoogle Scholar
  31. 31.
    Barrey E, Saint-Auret G, Bonnamy B, Damas D, Boyer O, Gidrol X. Pre-microRNA and mature microRNA in human mitochondria. PLoS ONE. 2011;6:e20220.PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Das S, Bedja D, Campbell N, Dunkerly B, Chenna V, Maitra A, Steenbergen C. miR-181c regulates the mitochondrial genome, bioenergetics, and propensity for heart failure in vivo. PLoS ONE. 2014;9:e96820.PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    Dasgupta N, Peng Y, Tan Z, Ciraolo G, Wang D, Li R. miRNAs in mtDNA-less cell mitochondria. Cell Death Discov. 2015;1:15004.PubMedPubMedCentralCrossRefGoogle Scholar
  34. 34.
    Jagannathan R, Thapa D, Nichols CE, Shepherd DL, Stricker JC, Croston TL, Baseler WA, Lewis SE, Martinez I, Hollander JM. Translational regulation of the mitochondrial genome following redistribution of mitochondrial microRNA in the diabetic heart. Circ Cardiovasc Genet. 2015;8:785–802.PubMedPubMedCentralCrossRefGoogle Scholar
  35. 35.
    Srinivasan H, Das S. Mitochondrial miRNA (MitomiR): a new player in cardiovascular health. Can J Physiol Pharmacol. 2015;93:855–61.PubMedCrossRefGoogle Scholar
  36. 36.
    Zhang X, Zuo X, Yang B, Li Z, Xue Y, Zhou Y, Huang J, Zhao X, Zhou J, Yan Y, Zhang H, Guo P, Sun H, Guo L, Zhang Y, Fu XD. MicroRNA directly enhances mitochondrial translation during muscle differentiation. Cell. 2014;158:607–19.PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Li H, Zhang X, Wang F, Zhou L, Yin Z, Fan J, Nie X, Wang P, Fu XD, Chen C, Wang DW. MicroRNA-21 lowers blood pressure in spontaneous hypertensive rats by upregulating mitochondrial translation. Circulation. 2016;134:734–51.PubMedCrossRefGoogle Scholar
  38. 38.
    Beitzinger M, Peters L, Zhu JY, Kremmer E, Meister G. Identification of human microRNA targets from isolated argonaute protein complexes. RNA Biol. 2007;4:76–84.PubMedCrossRefGoogle Scholar
  39. 39.
    Hock J, Weinmann L, Ender C, Rudel S, Kremmer E, Raabe M, Urlaub H, Meister G. Proteomic and functional analysis of argonaute-containing mRNA-protein complexes in human cells. EMBO Rep. 2007;8:1052–60.PubMedPubMedCentralCrossRefGoogle Scholar
  40. 40.
    Maniataki E, Mourelatos Z. Human mitochondrial tRNAMet is exported to the cytoplasm and associates with the argonaute 2 protein. RNA. 2005;11:849–52.PubMedPubMedCentralCrossRefGoogle Scholar
  41. 41.
    Ventura A, Young AG, Winslow MM, Lintault L, Meissner A, Erkeland SJ, Newman J, Bronson RT, Crowley D, Stone JR, Jaenisch R, Sharp PA, Jacks T. Targeted deletion reveals essential and overlapping functions of the miR-17 through 92 family of miRNA clusters. Cell. 2008;132:875–86.PubMedPubMedCentralCrossRefGoogle Scholar
  42. 42.
    Kuhn DE, Nuovo GJ, Martin MM, Malana GE, Pleister AP, Jiang J, Schmittgen TD, Terry Jr AV, Gardiner K, Head E, Feldman DS, Elton TS. Human chromosome 21-derived miRNAs are overexpressed in down syndrome brains and hearts. Biochem Biophys Res Commun. 2008;370:473–7.PubMedPubMedCentralCrossRefGoogle Scholar
  43. 43.
    Zhao Y, Ransom JF, Li A, Vedantham V, von Drehle M, Muth AN, Tsuchihashi T, McManus MT, Schwartz RJ, Srivastava D. Dysregulation of cardiogenesis, cardiac conduction, and cell cycle in mice lacking miRNA-1-2. Cell. 2007;129:303–17.PubMedCrossRefGoogle Scholar
  44. 44.
    Moreadith RW, Batshaw ML, Ohnishi T, Kerr D, Knox B, Jackson D, Hruban R, Olson J, Reynafarje B, Lehninger AL. Deficiency of the iron-sulfur clusters of mitochondrial reduced nicotinamide-adenine dinucleotide-ubiquinone oxidoreductase (complex I) in an infant with congenital lactic acidosis. J Clin Invest. 1984;74:685–97.PubMedPubMedCentralCrossRefGoogle Scholar
  45. 45.
    Feinberg MW, Moore KJ. MicroRNA regulation of atherosclerosis. Circ Res. 2016;118:703–20.PubMedPubMedCentralCrossRefGoogle Scholar
  46. 46.
    Novak J, Olejnickova V, Tkacova N, Santulli G. Mechanistic role of microRNAs in coupling lipid metabolism and atherosclerosis. Adv Exp Med Biol. 2015;887:79–100.PubMedPubMedCentralCrossRefGoogle Scholar
  47. 47.
    Najafi-Shoushtari SH, Kristo F, Li Y, Shioda T, Cohen DE, Gerszten RE, Naar AM. MicroRNA-33 and the SREBP host genes cooperate to control cholesterol homeostasis. Science. 2010;328:1566–9.PubMedCrossRefGoogle Scholar
  48. 48.
    Ramirez CM, Davalos A, Goedeke L, Salerno AG, Warrier N, Cirera-Salinas D, Suarez Y, Fernandez-Hernando C. MicroRNA-758 regulates cholesterol efflux through posttranscriptional repression of ATP-binding cassette transporter A1. Arterioscler Thromb Vasc Biol. 2011;31:2707–14.PubMedPubMedCentralCrossRefGoogle Scholar
  49. 49.
    Kim J, Yoon H, Ramirez CM, Lee SM, Hoe HS, Fernandez-Hernando C, Kim J. MiR-106b impairs cholesterol efflux and increases Abeta levels by repressing ABCA1 expression. Exp Neurol. 2012;235:476–83.PubMedCrossRefGoogle Scholar
  50. 50.
    de Aguiar Vallim TQ, Tarling EJ, Kim T, Civelek M, Baldan A, Esau C, Edwards PA. MicroRNA-144 regulates hepatic ATP binding cassette transporter A1 and plasma high-density lipoprotein after activation of the nuclear receptor farnesoid X receptor. Circ Res. 2013;112:1602–12.PubMedPubMedCentralCrossRefGoogle Scholar
  51. 51.
    Ramirez CM, Goedeke L, Rotllan N, Yoon JH, Cirera-Salinas D, Mattison JA, Suarez Y, de Cabo R, Gorospe M, Fernandez-Hernando C. MicroRNA 33 regulates glucose metabolism. Mol Cell Biol. 2013;33:2891–902.PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    Goedeke L, Rotllan N, Canfran-Duque A, Aranda JF, Ramirez CM, Araldi E, Lin CS, Anderson NN, Wagschal A, de Cabo R, Horton JD, Lasuncion MA, Naar AM, Suarez Y, Fernandez-Hernando C. MicroRNA-148a regulates LDL receptor and ABCA1 expression to control circulating lipoprotein levels. Nat Med. 2015;21:1280–9.PubMedPubMedCentralCrossRefGoogle Scholar
  53. 53.
    Meiler S, Baumer Y, Toulmin E, Seng K, Boisvert WA. MicroRNA 302a is a novel modulator of cholesterol homeostasis and atherosclerosis. Arterioscler Thromb Vasc Biol. 2015;35:323–31.PubMedCrossRefGoogle Scholar
  54. 54.
    Rayner KJ, Suarez Y, Davalos A, Parathath S, Fitzgerald ML, Tamehiro N, Fisher EA, Moore KJ, Fernandez-Hernando C. MiR-33 contributes to the regulation of cholesterol homeostasis. Science. 2010;328:1570–3.PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    Marquart TJ, Allen RM, Ory DS, Baldan A. miR-33 links SREBP-2 induction to repression of sterol transporters. Proc Natl Acad Sci U S A. 2010;107:12228–32.PubMedPubMedCentralCrossRefGoogle Scholar
  56. 56.
    Gerin I, Clerbaux LA, Haumont O, Lanthier N, Das AK, Burant CF, Leclercq IA, MacDougald OA, Bommer GT. Expression of miR-33 from an SREBP2 intron inhibits cholesterol export and fatty acid oxidation. J Biol Chem. 2010;285:33652–61.PubMedPubMedCentralCrossRefGoogle Scholar
  57. 57.
    Bommer GT, MacDougald OA. Regulation of lipid homeostasis by the bifunctional SREBF2-miR33a locus. Cell Metab. 2011;13:241–7.PubMedPubMedCentralCrossRefGoogle Scholar
  58. 58.
    Xu X, So JS, Park JG, Lee AH. Transcriptional control of hepatic lipid metabolism by SREBP and ChREBP. Semin Liver Dis. 2013;33:301–11.PubMedPubMedCentralCrossRefGoogle Scholar
  59. 59.
    Goedeke L, Vales-Lara FM, Fenstermaker M, Cirera-Salinas D, Chamorro-Jorganes A, Ramirez CM, Mattison JA, de Cabo R, Suarez Y, Fernandez-Hernando C. A regulatory role for microRNA 33* in controlling lipid metabolism gene expression. Mol Cell Biol. 2013;33:2339–52.PubMedPubMedCentralCrossRefGoogle Scholar
  60. 60.
    Tibiche C, Wang E. MicroRNA regulatory patterns on the human metabolic network. Open Syst Biol J. 2008;1:1–8.CrossRefGoogle Scholar
  61. 61.
    Murry CE, Jennings RB, Reimer KA. Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation. 1986;74:1124–36.PubMedCrossRefGoogle Scholar
  62. 62.
    Murry CE, Richard VJ, Reimer KA, Jennings RB. Ischemic preconditioning slows energy metabolism and delays ultrastructural damage during a sustained ischemic episode. Circ Res. 1990;66:913–31.PubMedCrossRefGoogle Scholar
  63. 63.
    Steenbergen C, Perlman ME, London RE, Murphy E. Mechanism of preconditioning. Ionic alterations. Circ Res. 1993;72:112–25.PubMedCrossRefGoogle Scholar
  64. 64.
    He B, Xiao J, Ren AJ, Zhang YF, Zhang H, Chen M, Xie B, Gao XG, Wang YW. Role of miR-1 and miR-133a in myocardial ischemic postconditioning. J Biomed Sci. 2011;18:22.PubMedPubMedCentralCrossRefGoogle Scholar
  65. 65.
    Zhu WS, Guo W, Zhu JN, Tang CM, Fu YH, Lin QX, Tan N, Shan ZX. Hsp90aa1: a novel target gene of miR-1 in cardiac ischemia/reperfusion injury. Sci Rep. 2016;6:24498.PubMedPubMedCentralCrossRefGoogle Scholar
  66. 66.
    Murphy E, Steenbergen C. Mechanisms underlying acute protection from cardiac ischemia-reperfusion injury. Physiol Rev. 2008;88:581–609.PubMedPubMedCentralCrossRefGoogle Scholar
  67. 67.
    Steenbergen C, Das S, Su J, Wong R, Murphy E. Cardioprotection and altered mitochondrial adenine nucleotide transport. Basic Res Cardiol. 2009;104:149–56.PubMedPubMedCentralCrossRefGoogle Scholar
  68. 68.
    Luo R, Wang Y, Xu P, Cao G, Zhao Y, Shao X, Li YX, Chang C, Peng C, Wang YL. Hypoxia-inducible miR-210 contributes to preeclampsia via targeting thrombospondin type I domain containing 7A. Sci Rep. 2016;6:19588.PubMedPubMedCentralCrossRefGoogle Scholar
  69. 69.
    Fasanaro P, D’Alessandra Y, Di Stefano V, Melchionna R, Romani S, Pompilio G, Capogrossi MC, Martelli F. MicroRNA-210 modulates endothelial cell response to hypoxia and inhibits the receptor tyrosine kinase ligand Ephrin-A3. J Biol Chem. 2008;283:15878–83.PubMedPubMedCentralCrossRefGoogle Scholar
  70. 70.
    Hu S, Huang M, Li Z, Jia F, Ghosh Z, Lijkwan MA, Fasanaro P, Sun N, Wang X, Martelli F, Robbins RC, Wu JC. MicroRNA-210 as a novel therapy for treatment of ischemic heart disease. Circulation. 2010;122:S124–31.PubMedPubMedCentralCrossRefGoogle Scholar
  71. 71.
    Mutharasan RK, Nagpal V, Ichikawa Y, Ardehali H. microRNA-210 is upregulated in hypoxic cardiomyocytes through Akt- and p53-dependent pathways and exerts cytoprotective effects. Am J Physiol Heart Circ Physiol. 2011;301:H1519–30.PubMedPubMedCentralCrossRefGoogle Scholar
  72. 72.
    Chen Z, Li Y, Zhang H, Huang P, Luthra R. Hypoxia-regulated microRNA-210 modulates mitochondrial function and decreases ISCU and COX10 expression. Oncogene. 2010;29:4362–8.PubMedCrossRefGoogle Scholar
  73. 73.
    Colleoni F, Padmanabhan N, Yung HW, Watson ED, Cetin I, Tissot van Patot MC, Burton GJ, Murray AJ. Suppression of mitochondrial electron transport chain function in the hypoxic human placenta: a role for miRNA-210 and protein synthesis inhibition. PLoS ONE. 2013;8:e55194.PubMedPubMedCentralCrossRefGoogle Scholar
  74. 74.
    Bienertova-Vasku J, Sana J, Slaby O. The role of microRNAs in mitochondria in cancer. Cancer Lett. 2013;336:1–7.PubMedCrossRefGoogle Scholar
  75. 75.
    Wang P, Liang J, Li Y, Li J, Yang X, Zhang X, Han S, Li S, Li J. Down-regulation of miRNA-30a alleviates cerebral ischemic injury through enhancing beclin 1-mediated autophagy. Neurochem Res. 2014;39:1279–91.PubMedCrossRefGoogle Scholar
  76. 76.
    Li W, Zhang X, Zhuang H, Chen HG, Chen Y, Tian W, Wu W, Li Y, Wang S, Zhang L, Chen Y, Li L, Zhao B, Sui S, Hu Z, Feng D. MicroRNA-137 is a novel hypoxia-responsive microRNA that inhibits mitophagy via regulation of two mitophagy receptors FUNDC1 and NIX. J Biol Chem. 2014;289:10691–701.PubMedPubMedCentralCrossRefGoogle Scholar
  77. 77.
    Li RC, Tao J, Guo YB, Wu HD, Liu RF, Bai Y, Lv ZZ, Luo GZ, Li LL, Wang M, Yang HQ, Gao W, Han QD, Zhang YY, Wang XJ, Xu M, Wang SQ. In vivo suppression of microRNA-24 prevents the transition toward decompensated hypertrophy in aortic-constricted mice. Circ Res. 2013;112:601–5.PubMedPubMedCentralCrossRefGoogle Scholar
  78. 78.
    Qian L, Van Laake LW, Huang Y, Liu S, Wendland MF, Srivastava D. miR-24 inhibits apoptosis and represses Bim in mouse cardiomyocytes. J Exp Med. 2011;208:549–60.PubMedPubMedCentralCrossRefGoogle Scholar
  79. 79.
    van Rooij E, Sutherland LB, Liu N, Williams AH, McAnally J, Gerard RD, Richardson JA, Olson EN. A signature pattern of stress-responsive microRNAs that can evoke cardiac hypertrophy and heart failure. Proc Natl Acad Sci U S A. 2006;103:18255–60.PubMedPubMedCentralCrossRefGoogle Scholar
  80. 80.
    Li DF, Tian J, Guo X, Huang LM, Xu Y, Wang CC, Wang JF, Ren AJ, Yuan WJ, Lin L. Induction of microRNA-24 by HIF-1 protects against ischemic injury in rat cardiomyocytes. Physiol Res. 2012;61:555–65.PubMedGoogle Scholar
  81. 81.
    Gao P, Tchernyshyov I, Chang TC, Lee YS, Kita K, Ochi T, Zeller KI, De Marzo AM, Van Eyk JE, Mendell JT, Dang CV. c-Myc suppression of miR-23a/b enhances mitochondrial glutaminase expression and glutamine metabolism. Nature. 2009;458:762–5.PubMedPubMedCentralCrossRefGoogle Scholar
  82. 82.
    Meloni M, Marchetti M, Garner K, Littlejohns B, Sala-Newby G, Xenophontos N, Floris I, Suleiman MS, Madeddu P, Caporali A, Emanueli C. Local inhibition of microRNA-24 improves reparative angiogenesis and left ventricle remodeling and function in mice with myocardial infarction. Mol Ther. 2013;21:1390–402.PubMedPubMedCentralCrossRefGoogle Scholar
  83. 83.
    Fiedler J, Jazbutyte V, Kirchmaier BC, Gupta SK, Lorenzen J, Hartmann D, Galuppo P, Kneitz S, Pena JT, Sohn-Lee C, Loyer X, Soutschek J, Brand T, Tuschl T, Heineke J, Martin U, Schulte-Merker S, Ertl G, Engelhardt S, Bauersachs J, Thum T. MicroRNA-24 regulates vascularity after myocardial infarction. Circulation. 2011;124:720–30.PubMedCrossRefGoogle Scholar
  84. 84.
    Yang KC, Bonini MG, Dudley Jr SC. Mitochondria and arrhythmias. Free Radic Biol Med. 2014;71:351–61.PubMedPubMedCentralCrossRefGoogle Scholar
  85. 85.
    Tong WH, Rouault T. Distinct iron-sulfur cluster assembly complexes exist in the cytosol and mitochondria of human cells. EMBO J. 2000;19:5692–700.PubMedPubMedCentralCrossRefGoogle Scholar
  86. 86.
    Chan SY, Zhang YY, Hemann C, Mahoney CE, Zweier JL, Loscalzo J. MicroRNA-210 controls mitochondrial metabolism during hypoxia by repressing the iron-sulfur cluster assembly proteins ISCU1/2. Cell Metab. 2009;10:273–84.PubMedPubMedCentralCrossRefGoogle Scholar
  87. 87.
    Puissegur MP, Mazure NM, Bertero T, Pradelli L, Grosso S, Robbe-Sermesant K, Maurin T, Lebrigand K, Cardinaud B, Hofman V, Fourre S, Magnone V, Ricci JE, Pouyssegur J, Gounon P, Hofman P, Barbry P, Mari B. miR-210 is overexpressed in late stages of lung cancer and mediates mitochondrial alterations associated with modulation of HIF-1 activity. Cell Death Differ. 2011;18:465–78.PubMedCrossRefGoogle Scholar
  88. 88.
    Li Y, Park JS, Deng JH, Bai Y. Cytochrome c oxidase subunit IV is essential for assembly and respiratory function of the enzyme complex. J Bioenerg Biomembr. 2006;38:283–91.PubMedPubMedCentralCrossRefGoogle Scholar
  89. 89.
    Aschrafi A, Schwechter AD, Mameza MG, Natera-Naranjo O, Gioio AE, Kaplan BB. MicroRNA-338 regulates local cytochrome c oxidase IV mRNA levels and oxidative phosphorylation in the axons of sympathetic neurons. J Neurosci. 2008;28:12581–90.PubMedPubMedCentralCrossRefGoogle Scholar
  90. 90.
    Zheng SQ, Li YX, Zhang Y, Li X, Tang H. MiR-101 regulates HSV-1 replication by targeting ATP5B. Antivir Res. 2011;89:219–26.PubMedCrossRefGoogle Scholar
  91. 91.
    Willers IM, Martinez-Reyes I, Martinez-Diez M, Cuezva JM. miR-127-5p targets the 3′UTR of human beta-F1-ATPase mRNA and inhibits its translation. Biochim Biophys Acta. 2012;1817:838–48.PubMedCrossRefGoogle Scholar
  92. 92.
    Meng C, Jin X, Xia L, Shen SM, Wang XL, Cai J, Chen GQ, Wang LS, Fang NY. Alterations of mitochondrial enzymes contribute to cardiac hypertrophy before hypertension development in spontaneously hypertensive rats. J Proteome Res. 2009;8:2463–75.PubMedCrossRefGoogle Scholar
  93. 93.
    Jullig M, Hickey AJ, Chai CC, Skea GL, Middleditch MJ, Costa S, Choong SY, Philips AR, Cooper GJ. Is the failing heart out of fuel or a worn engine running rich? A study of mitochondria in old spontaneously hypertensive rats. Proteomics. 2008;8:2556–72.PubMedCrossRefGoogle Scholar
  94. 94.
    Ding Y, Xia B, Yu J, Leng J, Huang J. Mitochondrial DNA mutations and essential hypertension (review). Int J Mol Med. 2013;32:768–74.PubMedGoogle Scholar
  95. 95.
    Meyers DE, Basha HI, Koenig MK. Mitochondrial cardiomyopathy: pathophysiology, diagnosis, and management. Tex Heart Inst J. 2013;40:385–94.PubMedPubMedCentralGoogle Scholar
  96. 96.
    Casademont J, Miro O. Electron transport chain defects in heart failure. Heart Fail Rev. 2002;7:131–9.PubMedCrossRefGoogle Scholar
  97. 97.
    Marin-Garcia J, Goldenthal MJ. Understanding the impact of mitochondrial defects in cardiovascular disease: a review. J Card Fail. 2002;8:347–61.PubMedCrossRefGoogle Scholar
  98. 98.
    Wijnen WJ, van der Made I, van den Oever S, Hiller M, de Boer BA, Picavet DI, Chatzispyrou IA, Houtkooper RH, Tijsen AJ, Hagoort J, van Veen H, Everts V, Ruijter JM, Pinto YM, Creemers EE. Cardiomyocyte-specific miRNA-30c over-expression causes dilated cardiomyopathy. PLoS ONE. 2014;9:e96290.PubMedPubMedCentralCrossRefGoogle Scholar
  99. 99.
    Duisters RF, Tijsen AJ, Schroen B, Leenders JJ, Lentink V, van der Made I, Herias V, van Leeuwen RE, Schellings MW, Barenbrug P, Maessen JG, Heymans S, Pinto YM, Creemers EE. miR-133 and miR-30 regulate connective tissue growth factor: implications for a role of microRNAs in myocardial matrix remodeling. Circ Res. 2009;104:170–8. 6p following 178PubMedCrossRefGoogle Scholar
  100. 100.
    Leptidis S, El Azzouzi H, Lok SI, de Weger R, Olieslagers S, Kisters N, Silva GJ, Heymans S, Cuppen E, Berezikov E, De Windt LJ, da Costa Martins P. A deep sequencing approach to uncover the miRNOME in the human heart. PLoS ONE. 2013;8:e57800.PubMedPubMedCentralCrossRefGoogle Scholar
  101. 101.
    Thum T, Galuppo P, Wolf C, Fiedler J, Kneitz S, van Laake LW, Doevendans PA, Mummery CL, Borlak J, Haverich A, Gross C, Engelhardt S, Ertl G, Bauersachs J. MicroRNAs in the human heart: a clue to fetal gene reprogramming in heart failure. Circulation. 2007;116:258–67.PubMedCrossRefGoogle Scholar
  102. 102.
    Soh J, Iqbal J, Queiroz J, Fernandez-Hernando C, Hussain MM. MicroRNA-30c reduces hyperlipidemia and atherosclerosis in mice by decreasing lipid synthesis and lipoprotein secretion. Nat Med. 2013;19:892–900.PubMedPubMedCentralCrossRefGoogle Scholar
  103. 103.
    Poggesi C, Ho CY. Muscle dysfunction in hypertrophic cardiomyopathy: what is needed to move to translation? J Muscle Res Cell Motil. 2014;35:37–45.PubMedPubMedCentralCrossRefGoogle Scholar
  104. 104.
    Guclu A, Germans T, Witjas-Paalberends ER, Stienen GJ, Brouwer WP, Harms HJ, Marcus JT, Vonk AB, Stooker W, Yilmaz A, Klein P, Ten Berg JM, Kluin J, Asselbergs FW, Lammertsma AA, Knaapen P, van Rossum AC, van der Velden J. ENerGetIcs in hypertrophic cardiomyopathy: traNslation between MRI, PET and cardiac myofilament function (ENGINE study). Neth Heart J. 2013;21:567–71.PubMedPubMedCentralCrossRefGoogle Scholar
  105. 105.
    Song L, Su M, Wang S, Zou Y, Wang X, Wang Y, Cui H, Zhao P, Hui R, Wang J. MiR-451 is decreased in hypertrophic cardiomyopathy and regulates autophagy by targeting TSC1. J Cell Mol Med. 2014;18:2266–74.PubMedPubMedCentralCrossRefGoogle Scholar
  106. 106.
    Bagnall RD, Tsoutsman T, Shephard RE, Ritchie W, Semsarian C. Global microRNA profiling of the mouse ventricles during development of severe hypertrophic cardiomyopathy and heart failure. PLoS ONE. 2012;7:e44744.PubMedPubMedCentralCrossRefGoogle Scholar
  107. 107.
    Soni MS, Rabaglia ME, Bhatnagar S, Shang J, Ilkayeva O, Mynatt R, Zhou YP, Schadt EE, Thornberry NA, Muoio DM, Keller MP, Attie AD. Downregulation of carnitine acyl-carnitine translocase by miRNAs 132 and 212 amplifies glucose-stimulated insulin secretion. Diabetes. 2014;63:3805–14.PubMedPubMedCentralCrossRefGoogle Scholar
  108. 108.
    Morita S, Horii T, Kimura M, Hatada I. MiR-184 regulates insulin secretion through repression of Slc25a22. Peer J. 2013;1:e162.PubMedPubMedCentralCrossRefGoogle Scholar
  109. 109.
    Barath R HJ, Hollander JM, Das S. Mitochondrial miRNAs in diabetes: just the tip of the iceberg. Can J Physiol Pharmacol. 2017. (in press).Google Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • Samarjit Das
    • 1
  • Hannah R. Vasanthi
    • 2
  • Ramesh Parjapath
    • 2
  1. 1.Department of Pathology, Cardiovascular DivisionJohns Hopkins UniversityBaltimoreUSA
  2. 2.Department of BiotechnologyPondicherry UniversityPuducherryIndia

Personalised recommendations