microRNA-210 is upregulated in hypoxic cardiomyocytes through Akt- and p53-dependent pathways and exerts cytoprotective effects

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 301, Issue 4, 2011, Pages

  Mutharasan, R Kannan ^a   Nagpal, Varun ^a   Ichikawa, Yoshihiko ^a   Ardehali, Hossein ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Cell death; Hypoxia; Microribonucleic acid; Reactive oxygen species

Indexed keywords

ANTIMYCIN A1; APOPTOSIS INDUCING FACTOR; APOPTOSIS INDUCING FACTOR MITOCHONDRION ASSOCIATED 3; HYDROGEN PEROXIDE; HYPOXIA INDUCIBLE FACTOR; HYPOXIA INDUCIBLE FACTOR 1BETA; MICRORNA; MICRORNA 210; PROTEIN KINASE B; PROTEIN P53; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL DEATH; CELL FUNCTION; CELL HYPOXIA; CELL PROTECTION; CELL VIABILITY; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; FIBROBLAST; HEART MUSCLE CELL; HUMAN; HUMAN CELL; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REGULATORY MECHANISM; REOXYGENATION; UPREGULATION; WILD TYPE;

ADENOVIRIDAE; ANIMALS; BLOTTING, WESTERN; CARDIOTONIC AGENTS; CELL DEATH; CELL HYPOXIA; CELLS, CULTURED; FLOW CYTOMETRY; HEK293 CELLS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; LUCIFERASES; MEMBRANE POTENTIALS; MICE; MICRORNAS; MITOCHONDRIA, HEART; MYOCYTES, CARDIAC; ONCOGENE PROTEIN V-AKT; PLASMIDS; REACTIVE OXYGEN SPECIES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRANSFECTION; TUMOR SUPPRESSOR PROTEIN P53; UP-REGULATION;

EID: 80053259947     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.01080.2010     Document Type: Article

References (42)

1. Ardehali H, O'Rourke B, Marban E. Cardioprotective role of the mitochondrial ATP-binding cassette protein 1. Circ Res 97: 740-742, 2005.
2. Bartel DP, Chen CZ. Micromanagers of gene expression: the potentially widespread influence of metazoan microRNAs. Nat Rev Genet 5: 396-400, 2004.
3. Beitner-Johnson D, Rust RT, Hsieh TC, Millhorn DE. Hypoxia activates Akt and induces phosphorylation of GSK-3 in PC12 cells. Cell Signal 13: 23-27, 2001.
4. Berger JA, Hautaniemi S, Jarvinen AK, Edgren H, Mitra SK, Astola J. Optimized LOWESS normalization parameter selection for DNA microarray data (Abstract). BMC Bioinformatics 5: 194, 2004.
5. Brunelle JK, Bell EL, Quesada NM, Vercauteren K, Tiranti V, Zeviani M, Scarpulla RC, Chandel NS. Oxygen sensing requires mitochondrial ROS but not oxidative phosphorylation. Cell Metab 1: 409-414, 2005.
6. Budinger GR, Chandel N, Shao ZH, Li CQ, Melmed A, Becker LB, Schumacker PT. Cellular energy utilization and supply during hypoxia in embryonic cardiac myocytes. Am J Physiol Lung Cell Mol Physiol 270: L44-L53, 1996.
7. Camps C, Buffa FM, Colella S, Moore J, Sotiriou C, Sheldon H, Harris AL, Gleadle JM, Ragoussis J. hsa-miR-210 Is induced by hypoxia and is an independent prognostic factor in breast cancer. Clin Cancer Res 14: 1340-1348, 2008.
8. Ceci M, Ross J Jr, Condorelli G. Molecular determinants of the physiological adaptation to stress in the cardiomyocyte: a focus on AKT. J Mol Cell Cardiol 37: 905-912, 2004.
9. 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 10: 273-284, 2009.
10. Chen Z, Li Y, Zhang H, Huang P, Luthra R. Hypoxia-regulated microRNA-210 modulates mitochondrial function and decreases ISCU and COX10 expression. Oncogene 29: 4362-4368, 2010.
11. Cordes KR, Srivastava D. MicroRNA regulation of cardiovascular development. Circ Res 104: 724-732, 2009.
12. Crosby ME, Kulshreshtha R, Ivan M, Glazer PM. MicroRNA regulation of DNA repair gene expression in hypoxic stress. Cancer Res 69: 1221-1229, 2009.
13. Daubman S. MicroRNAs in angiogenesis and vascular smooth muscle cell function. Circ Res 106: 423-425, 2010.
14. 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 283: 15878-15883, 2008.
15. Favaro E, Ramachandran A, McCormick R, Gee H, Blancher C, Crosby M, Devlin C, Blick C, Buffa F, Li JL, Vojnovic B, Pires das Neves R, Glazer P, Iborra F, Ivan M, Ragoussis J, Harris AL. MicroRNA-210 regulates mitochondrial free radical response to hypoxia and krebs cycle in cancer cells by targeting iron sulfur cluster protein ISCU. PLoS One 5: e10345, 2010.
16. Filipowicz W, Bhattacharyya SN, Sonenberg N. Mechanisms of posttranscriptional regulation by microRNAs: are the answers in sight? Nat Rev Genet 9: 102-114, 2008.
17. Friedman RC, Farh KK, Burge CB, Bartel DP. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 19: 92-105, 2009.
18. Frost RJ, van Rooij E. miRNAs as therapeutic targets in ischemic heart disease. J Cardiovasc Transl Res 3: 280-289, 2010.
19. Guzy RD, Hoyos B, Robin E, Chen H, Liu L, Mansfield KD, Simon MC, Hammerling U, Schumacker PT. Mitochondrial complex III is required for hypoxia-induced ROS production and cellular oxygen sensing. Cell Metab 1: 401-408, 2005.
20. Hammond EM, Giaccia AJ. The role of p53 in hypoxia-induced apoptosis. Biochem Biophys Res Commun 331: 718-725, 2005.
21. 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 122: S124-131, 2010.
22. Huang X, Ding L, Bennewith KL, Tong RT, Welford SM, Ang KK, Story M, Le QT, Giaccia AJ. Hypoxia-inducible mir-210 regulates normoxic gene expression involved in tumor initiation. Mol Cell 35: 856-867, 2009.
23. Huss JM, Levy FH, Kelly DP. Hypoxia inhibits the peroxisome proliferator-activated receptor alpha/retinoid X receptor gene regulatory pathway in cardiac myocytes: a mechanism for O2-dependent modulation of mitochondrial fatty acid oxidation. J Biol Chem 276: 27605-27612, 2001.
24. Jacobson J, Duchen MR, Heales SJ. Intracellular distribution of the fluorescent dye nonyl acridine orange responds to the mitochondrial membrane potential: implications for assays of cardiolipin and mitochondrial mass. J Neurochem 82: 224-233, 2002.
25. Jung SH, Bang H, Young S. Sample size calculation for multiple testing in microarray data analysis. Biostatistics 6: 157-169, 2005.
26. Kim HW, Haider HK, Jiang S, Ashraf M. Ischemic preconditioning augments survival of stem cells via miR-210 expression by targeting caspase-8-associated protein 2. J Biol Chem 284: 33161-33168, 2009.
27. Kubasiak LA, Hernandez OM, Bishopric NH, Webster KA. Hypoxia and acidosis activate cardiac myocyte death through the Bcl-2 family protein BNIP3. Proc Natl Acad Sci USA 99: 12825-12830, 2002.
28. Kulshreshtha R, Ferracin M, Wojcik SE, Garzon R, Alder H, Agosto- Perez FJ, Davuluri R, Liu CG, Croce CM, Negrini M, Calin GA, Ivan M. A microRNA signature of hypoxia. Mol Cell Biol 27: 1859-1867, 2007.
29. Matsui T, Li L, del Monte F, Fukui Y, Franke TF, Hajjar RJ, Rosenzweig A. Adenoviral gene transfer of activated phosphatidylinositol 3'-kinase and Akt inhibits apoptosis of hypoxic cardiomyocytes in vitro. Circulation 100: 2373-2379, 1999.
30. Maynard MA, Evans AJ, Shi W, Kim WY, Liu FF, Ohh M. Dominantnegative HIF-3 alpha 4 suppresses VHL-null renal cell carcinoma progression. Cell Cycle 6: 2810-2816, 2007.
31. Miyamoto S, Murphy AN, Brown JH. Akt mediated mitochondrial protection in the heart: metabolic and survival pathways to the rescue. J Bioenerg Biomembr 41: 169-180, 2009.
32. 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 18: 465-478, 2011.
33. Silverman HS, Wei S, Haigney MC, Ocampo CJ, Stern MD. Myocyte adaptation to chronic hypoxia and development of tolerance to subsequent acute severe hypoxia. Circ Res 80: 699-707, 1997.
34. Suzuki HI, Yamagata K, Sugimoto K, Iwamoto T, Kato S, Miyazono K. Modulation of microRNA processing by p53. Nature 460: 529-533, 2009.
35. Tanaka T, Wiesener M, Bernhardt W, Eckardt KU, Warnecke C. The human HIF (hypoxia-inducible factor)-3alpha gene is a HIF-1 target gene and may modulate hypoxic gene induction. Biochem J 424: 143-151, 2009.
36. Topkara VK, Mann DL. Role of microRNAs in cardiac remodeling and heart failure. Cardiovasc Drugs Ther 25: 171-182, 2011.
37. Tsai CA, Chen YJ, Chen JJ. Testing for differentially expressed genes with microarray data. Nucleic Acids Res 31: e52, 2003.
38. Tsuchiya S, Fujiwara T, Sato F, Shimada Y, Tanaka E, Sakai Y, Shimizu K, Tsujimoto G. MicroRNA-210 regulates cancer cell proliferation through targeting fibroblast growth factor receptor-like 1 (FGFRL1). J Biol Chem 286: 420-428, 2011.
39. Wang N, Zhou Z, Liao X, Zhang T. Role of microRNAs in cardiac hypertrophy and heart failure. IUBMB Life 61: 566-571, 2009.
40. Xie Q, Lin T, Zhang Y, Zheng J, Bonanno JA. Molecular cloning and characterization of a human AIF-like gene with ability to induce apoptosis. J Biol Chem 280: 19673-19681, 2005.
41. Zhang Z, Sun H, Dai H, Walsh RM, Imakura M, Schelter J, Burchard J, Dai X, Chang AN, Diaz RL, Marszalek JR, Bartz SR, Carleton M, Cleary MA, Linsley PS, Grandori C. MicroRNA miR-210 modulates cellular response to hypoxia through the MYC antagonist MNT. Cell Cycle 8: 2756-2768, 2009.
42. Zhou BP, Hu MC, Miller SA, Yu Z, Xia W, Lin SY, Hung MC. HER-2/neu blocks tumor necrosis factor-induced apoptosis via the Akt/ NF-kappaB pathway. J Biol Chem 275: 8027-8031, 2000.