Downregulation of MiR-199a derepresses hypoxia-inducible factor-1α and sirtuin 1 and recapitulates hypoxia preconditioning in cardiac myocytes

Circulation Research

Volumn 104, Issue 7, 2009, Pages 879-886

  Rane, Shweta ^a   He, Minzhen ^a   Sayed, Danish ^a   Vashistha, Himanshu ^a   Malhotra, Ashwani ^a   Sadoshima, Junichi ^a   Vatner, Dorothy E ^a   Vatner, Stephen F ^a   Abdellatif, Maha ^a  

^a RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

Author keywords

199a; Hif 1; MiR; Preconditioning; Sirt1

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; MICRORNA; MIR 199A; OXYGEN; OXYGENASE; PROLYL HYDROXYLASE 2; PROTEIN P53; SIRTUIN 1; UNCLASSIFIED DRUG; HIF1A PROTEIN, HUMAN; HIF1A PROTEIN, MOUSE; HIF1A PROTEIN, RAT; MIRN199A MICRORNA, MOUSE; PHD2 PROTEIN, RAT; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE; SIRT1 PROTEIN, RAT; SIRTUIN;

ANIMAL CELL; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL HYPOXIA; DOWN REGULATION; HEART MUSCLE CELL; LONGEVITY; MOUSE; NEWBORN; NONHUMAN; OXYGEN TENSION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; UPREGULATION; ANIMAL; C57BL MOUSE; CELL CULTURE; DISEASE MODEL; GENE SILENCING; GENETIC TRANSDUCTION; GENETICS; HEART INFARCTION PREVENTION; HEART MITOCHONDRION; HEART MUSCLE ISCHEMIA; HUMAN; METABOLISM; PATHOLOGY; REPERFUSION INJURY; SPRAGUE DAWLEY RAT; SWINE;

ANIMALS; ANIMALS, NEWBORN; APOPTOSIS; CELL HYPOXIA; CELLS, CULTURED; DISEASE MODELS, ANIMAL; DOWN-REGULATION; GENE KNOCKDOWN TECHNIQUES; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; ISCHEMIC PRECONDITIONING, MYOCARDIAL; MICE; MICE, INBRED C57BL; MICRORNAS; MITOCHONDRIA, HEART; MYOCARDIAL ISCHEMIA; MYOCYTES, CARDIAC; OXYGEN; PROCOLLAGEN-PROLINE DIOXYGENASE; RATS; RATS, SPRAGUE-DAWLEY; REPERFUSION INJURY; SIRTUINS; SWINE; TRANSDUCTION, GENETIC;

EID: 65249185780     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.108.193102     Document Type: Article

References (36)

1. Sayed D, Hong C, Chen IY, Lypowy J, Abdellatif M. MicroRNAs play an essential role in the development of cardiac hypertrophy. Circ Res. 2007;100:416-424.
2. John B, Enright AJ, Aravin A, Tuschl T, Sander C, Marks DS. Human MicroRNA targets. PLoS Biol. 2004;2:1862-1879.
3. Thomson JM, Newman M, Parker JS, Morin-Kensicki EM, Wright T, Hammond SM. Extensive post-transcriptional regulation of microRNAs and its implications for cancer. Genes Dev. 2006;20:2202-2207.
4. Newman MA, Thomson JM, Hammond SM. Lin-28 interaction with the Let-7 precursor loop mediates regulated microRNA processing. RNA. 2008;14:1539-1549.
5. Viswanathan SR, Daley GQ, Gregory RI. Selective blockade of microRNA processing by Lin28. Science. 2008;320:97-100.
6. Rowland RT, Meng X, Cleveland JC, Meldrum DR, Harken AH, Brown JM. Cardioadaptation induced by cyclic ischemic preconditioning is mediated by translational regulation of de novo protein synthesis. J Surg Res. 1997;71:155-160.
7. Murry CE, Jennings RB, Reimer KA. Preconditioning with ischemia: A delay of lethal cell injury in ischemic myocardium. Circulation. 1986; 74:1124-1136.
8. Downey JM, Davis AM, Cohen MV. Signaling pathways in ischemic preconditioning. Heart Fail Rev. 2007;12:181-188.
9. Javadov SA, Clarke S, Das M, Griffiths EJ, Lim KH, Halestrap AP. Ischaemic preconditioning inhibits opening of mitochondrial permeability transition pores in the reperfused rat heart. J Physiol. 2003;549:513-524.
10. Baines CP, Song CX, Zheng YT, Wang GW, Zhang J, Wang OL, Guo Y, Bolli R, Cardwell EM, Ping P. Protein kinase Cepsilon interacts with and inhibits the permeability transition pore in cardiac mitochondria. Circ Res. 2003;92:873-880.
11. Juhaszova M, Zorov DB, Kim SH, Pepe S, Fu Q, Fishbein KW, Ziman BD, Wang S, Ytrehus K, Antos CL, Olson EN, Sollott SJ. Glycogen synthase kinase-3beta mediates convergence of protection signaling to inhibit the mitochondrial permeability transition pore. J Clin Invest. 2004;113:1535-1549.
12. Wang GL, Semenza GL. General involvement of hypoxia-inducible factor 1 in transcriptional response to hypoxia. Proc Natl Acad Sci U S A. 1993;90:4304-4308.
13. Greijer AE, van der Groep P, Kemming D, Shvarts A, Semenza GL, Meijer GA, van de Wiel MA, Belien JA, van Diest PJ, van der Wall E. Up-regulation of gene expression by hypoxia is mediated predominantly by hypoxia-inducible factor 1 (HIF-1). J Pathol. 2005;206:291-304.
14. Kido M, Du L, Sullivan CC, Li X, Deutsch R, Jamieson SW, Thistlethwaite PA. Hypoxia-inducible factor 1-alpha reduces infarction and attenuates progression of cardiac dysfunction after myocardial infarction in the mouse. J Am Coll Cardiol. 2005;46:2116-2124.
15. Cai Z, Zhong H, Bosch-Marce M, Fox-Talbot K, Wang L, Wei C, Trush MA, Semenza GL. Complete loss of ischaemic preconditioning-induced cardioprotection in mice with partial deficiency of HIF-1{alpha}. Car-diovasc Res. 2008;77:463-470.
16. Eckle T, Kohler D, Lehmann R, El Kasmi K, Eltzschig HK. Hypoxia-inducible factor-1 is central to cardioprotection: A new paradigm for ischemic preconditioning. Circulation. 2008;118:166-175.
17. Abdellatif M, Mcllelan WR, Schneider MD. p21 Ras as a governer of global gene expression. J Biol Chem. 1994;269:15423-15426.
18. Malhotra A, Reich D, Reich D, Nakouzi A, Sanghi V, Geenen DL, Buttrick PM. Experimental diabetes is associated with functional activation of protein kinase C epsilon and phosphorylation of troponin I in the heart, which are prevented by angiotensin II receptor blockade. Circ Res. 1997;81:1027-1033.
19. Graham FL, Prevec L. Manipulation of adenovirus vectors. In: Murray EJ, ed. Methods in Molecular Biology. Vol 7. Clifton, NJ: Humana Press; 1991:109-128.
20. Sayed D, Rane S, Lypowy J, He M, Chen IY, Vashistha H, Yan L, Malhotra A, Vatner D, Abdellatif M. MicroRNA-21 targets Sprouty2 and promotes cellular outgrowths. Mol Biol Cell. 2008;18:3272-3282.
21. Shen YT, Depre C, Yan L, Park JY, Tian B, Jain K, Chen L, Zhang Y, Kudej RK, Zhao X, Sadoshima J, Vatner DE, Vatner SF. Repetitive ischemia by coronary stenosis induces a novel window of ischemic preconditioning. Circulation. 2008;118:1961-1969.
22. Lewis BP, Burge CB, Bartel DP. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell. 2005;120:15-20.
23. Carmeliet P, Dor Y, Herbert JM, Fukumura D, Brusselmans K, Dewerchin M, Neeman M, Bono F, Abramovitch R, Maxwell P, Koch CJ, Ratcliffe P, Moons L, Jain RK, Collen D, Keshert E. Role of HIF-1alpha in hypoxia-mediated apoptosis, cell proliferation and tumour angio-genesis. Nature. 1998;394:485-490.
24. An WG, Kanekal M, Simon MC, Maltepe E, Blagosklonny MV, Neckers LM. Stabilization of wild-type p53 by hypoxia-inducible factor 1alpha. Nature. 1998;392:405-408.
25. Haldar S, Jena N, Croce CM. Inactivation of Bcl-2 by phosphorylation. Proc Natl Acad Sci U S A. 1995;92:4507-4511.
26. Kitakaze M, Hori M, Takashima S, Sato H, Inoue M, Kamada T. Ische-mic preconditioning increases adenosine release and 5′-nucleotidase activity during myocardial ischemia and reperfusion in dogs. Implications for myocardial salvage. Circulation. 1993;87:208-215. (Pubitemid 23019352)
27. Urabe K, Miura T, Iwamoto T, Ogawa T, Goto M, Sakamoto J, Iimura O. Preconditioning enhances myocardial resistance to postischaemic myo-cardial stunning via adenosine receptor activation. Cardiovasc Res. 1993; 27:657-662.
28. Bruick RK, McKnight SL. A conserved family of prolyl-4-hydroxylases that modify HIF. Science. 2001;294:1337-1340.
29. Maxwell PH, Wiesener MS, Chang GW, Clifford SC, Vaux EC, Cockman ME, Wykoff CC, Pugh CW, Maher ER, Ratcliffe PJ. The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature. 1999;399:271-275.
30. Berra E, Benizri E, Ginouves A, Volmat V, Roux D, Pouyssegur J. HIF prolyl-hydroxylase 2 is the key oxygen sensor setting low steady-state levels of HIF-1alpha in normoxia. EMBO J. 2003;22:4082-4090.
31. Ray PS, Maulik G, Cordis GA, Bertelli AA, Bertelli A, Das DK. The red wine antioxidant resveratrol protects isolated rat hearts from ischemia reperfusion injury. Free Radic Biol Med. 1999;27:160-169.
32. Raval AP, Dave KR, Perez-Pinzon MA. Resveratrol mimics ischemic preconditioning in the brain. J Cereb Blood Flow Metab. 2006;26: 1141-1147.
33. Giovannini L, Migliori M, Longoni BM, Das DK, Bertelli AA, Panichi V, Filippi C, Bertelli A. Resveratrol, a polyphenol found in wine, reduces ischemia reperfusion injury in rat kidneys. J Cardiovasc Pharmacol. 2001;37:262-270.
34. Thornton J, Striplin S, Liu GS, Swafford A, Stanley AW, Van Winkle DM, Downey JM. Inhibition of protein synthesis does not block myo-cardial protection afforded by preconditioning. Am J Physiol. 1990;259: H1822-H1825.
35. Matsuyama N, Leavens JE, McKinnon D, Gaudette GR, Aksehirli TO, Krukenkamp IB. Ischemic but not pharmacological preconditioning requires protein synthesis. Circulation. 2000;102(suppl III):III-312-III-318.
36. Zhang H, Bosch-Marce M, Shimoda LA, Tan YS, Baek JH, Wesley JB, Gonzalez FJ, Semenza GL. Mitochondrial autophagy is an HIF-1-dependent adaptive metabolic response to hypoxia. J Biol Chem. 2008; 283:10892-10903.