Suppression of Induced microRNA-15b Prevents Rapid Loss of Cardiac Function in a Dicer Depleted Model of Cardiac Dysfunction

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Roy, Sashwati ^a   Banerjee, Jaideep ^a   Gnyawali, Surya C ^a   Khanna, Savita ^a   He, Guanglong ^a   Pfeiffer, Douglas ^a   Zweier, Jay L ^a   Sen, Chandan K ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DICER; LOCKED NUCLEIC ACID; MICRORNA 15B; PROTEIN KINASE PIM 1; RNA ANTIBODY; DEAD BOX PROTEIN; DICER1 PROTEIN, MOUSE; MICRORNA; MIRN15 MICRORNA, MOUSE; PIM1 PROTEIN, MOUSE; RIBONUCLEASE III;

ADULT ANIMAL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DICER GENE; DISORDERS OF MITOCHONDRIAL FUNCTIONS; GENE DELETION; GENE REPRESSION; GENE SILENCING; HEART FAILURE; HEART HYPERTROPHY; HEART PROTECTION; IN VITRO STUDY; IN VIVO STUDY; MALE; MITOCHONDRIAL MEMBRANE POTENTIAL; MOUSE; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PROTEIN EXPRESSION; ANIMAL; CELL LINE; DISEASE MODEL; ECHOCARDIOGRAPHY; GENE EXPRESSION REGULATION; GENETICS; HEART DISEASE; HEART FUNCTION TEST; MITOCHONDRION; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; PHYSIOLOGY; TRANSGENIC MOUSE;

MURINAE;

ANIMALS; CELL LINE; DEAD-BOX RNA HELICASES; DISEASE MODELS, ANIMAL; ECHOCARDIOGRAPHY; GENE EXPRESSION REGULATION; HEART DISEASES; HEART FUNCTION TESTS; MAGNETIC RESONANCE IMAGING; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MICE, TRANSGENIC; MICRORNAS; MITOCHONDRIA; OXIDATIVE STRESS; PROTO-ONCOGENE PROTEINS C-PIM-1; RIBONUCLEASE III;

EID: 84879242259     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0066789     Document Type: Article

References (72)

1. Zhao Y, Ransom JF, Li A, Vedantham V, von Drehle M, et al. (2007) Dysregulation of cardiogenesis, cardiac conduction, and cell cycle in mice lacking miRNA-1-2. Cell 129: 303-317.
2. Saxena A, Tabin CJ, (2010) miRNA-processing enzyme Dicer is necessary for cardiac outflow tract alignment and chamber septation. Proc Natl Acad Sci U S A 107: 87-91.
3. da Costa Martins PA, Bourajjaj M, Gladka M, Kortland M, van Oort RJ, et al. (2008) Conditional dicer gene deletion in the postnatal myocardium provokes spontaneous cardiac remodeling. Circulation 118: 1567-1576.
4. Chen JF, Murchison EP, Tang R, Callis TE, Tatsuguchi M, et al. (2008) Targeted deletion of Dicer in the heart leads to dilated cardiomyopathy and heart failure. Proc Natl Acad Sci U S A 105: 2111-2116.
5. Small EM, Frost RJ, Olson EN, (2010) MicroRNAs add a new dimension to cardiovascular disease. Circulation 121: 1022-1032.
6. Divakaran V, Mann DL, (2008) The emerging role of microRNAs in cardiac remodeling and heart failure. Circ Res 103: 1072-1083.
7. Gnyawali SC, Roy S, McCoy M, Biswas S, Sen CK, (2009) Remodeling of the ischemia-reperfused murine heart: 11.7-T cardiac magnetic resonance imaging of contrast-enhanced infarct patches and transmurality. Antioxid Redox Signal 11: 1829-1839.
8. Gnyawali SC, Roy S, Driggs J, Khanna S, Ryan T, et al. (2010) High-frequency high-resolution echocardiography: first evidence on non-invasive repeated measure of myocardial strain, contractility, and mitral regurgitation in the ischemia-reperfused murine heart. J Vis Exp.
9. Zhu X, Zuo L, Cardounel AJ, Zweier JL, He G, (2007) Characterization of in vivo tissue redox status, oxygenation, and formation of reactive oxygen species in postischemic myocardium. Antioxid Redox Signal 9: 447-455.
10. Khanna S, Roy S, Ryu H, Bahadduri P, Swaan PW, et al. (2003) Molecular basis of vitamin E action: tocotrienol modulates 12-lipoxygenase, a key mediator of glutamate-induced neurodegeneration. J Biol Chem 278: 43508-43515.
11. Khanna S, Roy S, Slivka A, Craft TK, Chaki S, et al. (2005) Neuroprotective properties of the natural vitamin E alpha-tocotrienol. Stroke 36: 2258-2264.
12. Sen CK, Khanna S, Babior BM, Hunt TK, Ellison EC, et al. (2002) Oxidant-induced vascular endothelial growth factor expression in human keratinocytes and cutaneous wound healing. J Biol Chem 277: 33284-33290.
13. Sen CK, Khanna S, Roy S, Packer L, (2000) Molecular basis of vitamin E action. Tocotrienol potently inhibits glutamate-induced pp60(c-Src) kinase activation and death of HT4 neuronal cells. J Biol Chem 275: 13049-13055.
14. Crouser ED, Julian MW, Blaho DV, Pfeiffer DR, (2002) Endotoxin-induced mitochondrial damage correlates with impaired respiratory activity. Crit Care Med 30: 276-284.
15. Claycomb WC, Lanson NA Jr, Stallworth BS, Egeland DB, Delcarpio JB, et al. (1998) HL-1 cells: a cardiac muscle cell line that contracts and retains phenotypic characteristics of the adult cardiomyocyte. Proc Natl Acad Sci U S A 95: 2979-2984.
16. Shilo S, Roy S, Khanna S, Sen CK, (2008) Evidence for the involvement of miRNA in redox regulated angiogenic response of human microvascular endothelial cells. Arterioscler Thromb Vasc Biol 28: 471-477.
17. Hussain SR, Lucas DM, Johnson AJ, Lin TS, Bakaletz AP, et al. (2008) Flavopiridol causes early mitochondrial damage in chronic lymphocytic leukemia cells with impaired oxygen consumption and mobilization of intracellular calcium. Blood 111: 3190-3199.
18. Reid AB, Kurten RC, McCullough SS, Brock RW, Hinson JA, (2005) Mechanisms of acetaminophen-induced hepatotoxicity: role of oxidative stress and mitochondrial permeability transition in freshly isolated mouse hepatocytes. J Pharmacol Exp Ther 312: 509-516.
19. Khanna S, Roy S, Parinandi NL, Maurer M, Sen CK, (2006) Characterization of the potent neuroprotective properties of the natural vitamin E alpha-tocotrienol. J Neurochem 98: 1474-1486.
20. Du H, Guo L, Fang F, Chen D, Sosunov AA, et al. (2008) Cyclophilin D deficiency attenuates mitochondrial and neuronal perturbation and ameliorates learning and memory in Alzheimer's disease. Nat Med 14: 1097-1105.
21. Kuhn DE, Roy S, Radtke J, Gupta S, Sen CK, (2006) Laser microdissection and pressure-catapulting technique to study gene expression in the reoxygenated myocardium. Am J Physiol Heart Circ Physiol 290: H2625-2632.
22. Kuhn DE, Roy S, Radtke J, Khanna S, Sen CK, (2007) Laser microdissection and capture of pure cardiomyocytes and fibroblasts from infarcted heart regions: perceived hyperoxia induces p21 in peri-infarct myocytes. Am J Physiol Heart Circ Physiol 292: H1245-1253.
23. Bernstein E, Kim SY, Carmell MA, Murchison EP, Alcorn H, et al. (2003) Dicer is essential for mouse development. Nat Genet 35: 215-217.
24. Yang WJ, Yang DD, Na S, Sandusky GE, Zhang Q, et al. (2005) Dicer is required for embryonic angiogenesis during mouse development. J Biol Chem 280: 9330-9335.
25. Sohal DS, Nghiem M, Crackower MA, Witt SA, Kimball TR, et al. (2001) Temporally regulated and tissue-specific gene manipulations in the adult and embryonic heart using a tamoxifen-inducible Cre protein. Circ Res 89: 20-25.
26. Dhalla AK, Hill MF, Singal PK, (1996) Role of oxidative stress in transition of hypertrophy to heart failure. J Am Coll Cardiol 28: 506-514.
27. Seddon M, Looi YH, Shah AM, (2007) Oxidative stress and redox signalling in cardiac hypertrophy and heart failure. Heart 93: 903-907.
28. Tsutsui H, Ide T, Kinugawa S, (2006) Mitochondrial oxidative stress, DNA damage, and heart failure. Antioxid Redox Signal 8: 1737-1744.
29. Narula N, Zaragoza MV, Sengupta PP, Li P, Haider N, et al. (2011) Adenine nucleotide translocase 1 deficiency results in dilated cardiomyopathy with defects in myocardial mechanics, histopathological alterations, and activation of apoptosis. JACC Cardiovasc Imaging 4: 1-10.
30. Miyamoto S, Murphy AN, Brown JH, (2008) Akt mediates mitochondrial protection in cardiomyocytes through phosphorylation of mitochondrial hexokinase-II. Cell Death Differ 15: 521-529.
31. White SM, Constantin PE, Claycomb WC, (2004) Cardiac physiology at the cellular level: use of cultured HL-1 cardiomyocytes for studies of cardiac muscle cell structure and function. Am J Physiol Heart Circ Physiol 286: H823-829.
32. Thum T, (2008) Cardiac dissonance without conductors: how dicer depletion provokes chaos in the heart. Circulation 118: 1524-1527.
33. van Rooij E, Sutherland LB, Qi X, Richardson JA, Hill J, et al. (2007) Control of stress-dependent cardiac growth and gene expression by a microRNA. Science 316: 575-579.
34. Rainer J, Ploner C, Jesacher S, Ploner A, Eduardoff M, et al. (2009) Glucocorticoid-regulated microRNAs and mirtrons in acute lymphoblastic leukemia. Leukemia 23: 746-752.
35. Gantier MP, McCoy CE, Rusinova I, Saulep D, Wang D, et al. (2011) Analysis of microRNA turnover in mammalian cells following Dicer1 ablation. Nucleic Acids Res 39: 5692-5703.
36. Kai ZS, Pasquinelli AE, (2010) MicroRNA assassins: factors that regulate the disappearance of miRNAs. Nat Struct Mol Biol 17: 5-10.
37. Rissland OS, Hong SJ, Bartel DP, (2011) MicroRNA destabilization enables dynamic regulation of the miR-16 family in response to cell-cycle changes. Mol Cell 43: 993-1004.
38. Bail S, Swerdel M, Liu H, Jiao X, Goff LA, et al. (2010) Differential regulation of microRNA stability. RNA 16: 1032-1039.
39. Kosaka N, Iguchi H, Yoshioka Y, Takeshita F, Matsuki Y, et al. (2010) Secretory mechanisms and intercellular transfer of microRNAs in living cells. J Biol Chem 285: 17442-17452.
40. Montecalvo A, Larregina AT, Shufesky WJ, Beer Stolz D, Sullivan ML, et al. (2011) Mechanism of transfer of functional microRNAs between mouse dendritic cells via exosomes. Blood.
41. Katakowski M, Buller B, Wang X, Rogers T, Chopp M, (2010) Functional microRNA is transferred between glioma cells. Cancer Res 70: 8259-8263.
42. Roy S, Khanna S, Rink T, Radtke J, Williams WT, et al. (2007) P21waf1/cip1/sdi1 as a central regulator of inducible smooth muscle actin expression and differentiation of cardiac fibroblasts to myofibroblasts. Mol Biol Cell 18: 4837-4846.
43. Roy S, Khanna S, Hussain SR, Biswas S, Azad A, et al. (2009) MicroRNA expression in response to murine myocardial infarction: miR-21 regulates fibroblast metalloprotease-2 via phosphatase and tensin homologue. Cardiovasc Res 82: 21-29.
44. Roy S, Khanna S, Azad A, Schnitt R, He G, et al. (2010) Fra-2 mediates oxygen-sensitive induction of transforming growth factor beta in cardiac fibroblasts. Cardiovasc Res 87: 647-655.
45. Muraski JA, Rota M, Misao Y, Fransioli J, Cottage C, et al. (2007) Pim-1 regulates cardiomyocyte survival downstream of Akt. Nat Med 13: 1467-1475.
46. Fischer KM, Cottage CT, Wu W, Din S, Gude NA, et al. (2009) Enhancement of myocardial regeneration through genetic engineering of cardiac progenitor cells expressing Pim-1 kinase. Circulation 120: 2077-2087.
47. Cottage CT, Bailey B, Fischer KM, Avitable D, Collins B, et al. (2010) Cardiac progenitor cell cycling stimulated by pim-1 kinase. Circ Res 106: 891-901.
48. Borillo GA, Mason M, Quijada P, Volkers M, Cottage C, et al. (2010) Pim-1 Kinase Protects Mitochondrial Integrity in Cardiomyocytes. Circ Res.
49. Muraski JA, Fischer KM, Wu W, Cottage CT, Quijada P, et al. (2008) Pim-1 kinase antagonizes aspects of myocardial hypertrophy and compensation to pathological pressure overload. Proc Natl Acad Sci U S A 105: 13889-13894.
50. Sussman MA, (2009) Mitochondrial integrity: preservation through Akt/Pim-1 kinase signaling in the cardiomyocyte. Expert Rev Cardiovasc Ther 7: 929-938.
51. Lilly M, Sandholm J, Cooper JJ, Koskinen PJ, Kraft A, (1999) The PIM-1 serine kinase prolongs survival and inhibits apoptosis-related mitochondrial dysfunction in part through a bcl-2-dependent pathway. Oncogene 18: 4022-4031.
52. Li S, Xi Y, Zhang H, Wang Y, Wang X, et al. (2010) A pivotal role for Pim-1 kinase in esophageal squamous cell carcinoma involving cell apoptosis induced by reducing Akt phosphorylation. Oncol Rep 24: 997-1004.
53. Nishi H, Ono K, Iwanaga Y, Horie T, Nagao K, et al. (2010) MicroRNA-15b modulates cellular ATP levels and degenerates mitochondria via Arl2 in neonatal rat cardiac myocytes. J Biol Chem 285: 4920-4930.
54. Paradkar PN, Zumbrennen KB, Paw BH, Ward DM, Kaplan J, (2009) Regulation of mitochondrial iron import through differential turnover of mitoferrin 1 and mitoferrin 2. Mol Cell Biol 29: 1007-1016.
55. Scorrano L, Ashiya M, Buttle K, Weiler S, Oakes SA, et al. (2002) A distinct pathway remodels mitochondrial cristae and mobilizes cytochrome c during apoptosis. Dev Cell 2: 55-67.
56. Singh MK, Lu MM, Massera D, Epstein JA, (2011) MicroRNA-processing enzyme Dicer is required in epicardium for coronary vasculature development. J Biol Chem 286: 41036-41045.
57. Humphreys DT, Hynes CJ, Patel HR, Wei GH, Cannon L, et al. (2012) Complexity of murine cardiomyocyte miRNA biogenesis, sequence variant expression and function. PLoS One 7: e30933.
58. Carlson DL, Lightfoot E Jr, Bryant DD, Haudek SB, Maass D, et al. (2002) Burn plasma mediates cardiac myocyte apoptosis via endotoxin. Am J Physiol Heart Circ Physiol 282: H1907-1914.
59. Fryer RM, Hsu AK, Nagase H, Gross GJ, (2000) Opioid-induced cardioprotection against myocardial infarction and arrhythmias: mitochondrial versus sarcolemmal ATP-sensitive potassium channels. J Pharmacol Exp Ther 294: 451-457.
60. George CH, Higgs GV, Lai FA, (2003) Ryanodine receptor mutations associated with stress-induced ventricular tachycardia mediate increased calcium release in stimulated cardiomyocytes. Circ Res 93: 531-540.
61. Gonzalez-Juanatey JR, Iglesias MJ, Alcaide C, Pineiro R, Lago F, (2003) Doxazosin induces apoptosis in cardiomyocytes cultured in vitro by a mechanism that is independent of alpha1-adrenergic blockade. Circulation 107: 127-131.
62. Akhavan A, Atanasiu R, Shrier A, (2003) Identification of a COOH-terminal segment involved in maturation and stability of human ether-a-go-go-related gene potassium channels. J Biol Chem 278: 40105-40112.
63. Lanson NA Jr, Glembotski CC, Steinhelper ME, Field LJ, Claycomb WC, (1992) Gene expression and atrial natriuretic factor processing and secretion in cultured AT-1 cardiac myocytes. Circulation 85: 1835-1841.
64. Sartiani L, Bochet P, Cerbai E, Mugelli A, Fischmeister R, (2002) Functional expression of the hyperpolarization-activated, non-selective cation current I(f) in immortalized HL-1 cardiomyocytes. J Physiol 545: 81-92.
65. Kitta K, Clement SA, Remeika J, Blumberg JB, Suzuki YJ, (2001) Endothelin-1 induces phosphorylation of GATA-4 transcription factor in the HL-1 atrial-muscle cell line. Biochem J 359: 375-380.
66. Kitta K, Day RM, Ikeda T, Suzuki YJ, (2001) Hepatocyte growth factor protects cardiac myocytes against oxidative stress-induced apoptosis. Free Radic Biol Med 31: 902-910.
67. Nguyen SV, Claycomb WC, (1999) Hypoxia regulates the expression of the adrenomedullin and HIF-1 genes in cultured HL-1 cardiomyocytes. Biochem Biophys Res Commun 265: 382-386.
68. Sanders DB, Larson DF, Hunter K, Gorman M, Yang B, (2001) Comparison of tumor necrosis factor-alpha effect on the expression of iNOS in macrophage and cardiac myocytes. Perfusion 16: 67-74.
69. Seymour EM, Wu SY, Kovach MA, Romano MA, Traynor JR, et al. (2003) HL-1 myocytes exhibit PKC and K(ATP) channel-dependent delta opioid preconditioning. J Surg Res 114: 187-194.
70. Dai B, Saada N, Echetebu C, Dettbarn C, Palade P, (2002) A new promoter for alpha1C subunit of human L-type cardiac calcium channel Ca(V)1.2. Biochem Biophys Res Commun 296: 429-433.
71. Watanabe E, Smith DM Jr, Delcarpio JB, Sun J, Smart FW, et al. (1998) Cardiomyocyte transplantation in a porcine myocardial infarction model. Cell Transplant 7: 239-246.
72. Hullinger TG, Montgomery RL, Seto AG, Dickinson BA, Semus HM, et al. (2011) Inhibition of miR-15 Protects Against Cardiac Ischemic Injury. Circ Res.