MicroRNA-539 is up-regulated in failing heart, and suppresses O-GlcNAcase expression

Journal of Biological Chemistry

Volumn 289, Issue 43, 2014, Pages 29665-29676

  Muthusamy, Senthilkumar ^a   DeMartino, Angelica M ^a   Watson, Lewis J ^a   Brittian, Kenneth R ^a   Zafir, Ayesha ^a   Dassanayaka, Sujith ^a   Hong, Kyung U ^a   Jones, Steven P ^a  

^a University of Louisville School of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARDIOLOGY; DNA; ENZYMES; METABOLISM; PROTEINS; RNA;

CYTOPLASMIC PROTEINS; MICROARRAY ANALYSIS; MOLECULAR MECHANISM; N-ACETYLGLUCOSAMINE; NEONATAL RAT CARDIOMYOCYTES; POST-TRANSLATIONAL MODIFICATIONS; PROTEIN EXPRESSIONS; THERAPEUTIC TARGETS;

HEART;

ACETYLGLUCOSAMINIDASE; MICRORNA; MICRORNA 539; UNCLASSIFIED DRUG; 3' UNTRANSLATED REGION; BETA N ACETYLHEXOSAMINIDASE; HEXOSAMINIDASE C; OXYGEN;

3' UNTRANSLATED REGION; ACYLATION; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME REPRESSION; GENE OVEREXPRESSION; HEART FAILURE; HEART FUNCTION; HEART INFARCTION; HEART MUSCLE CELL; METABOLIC DISORDER; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMID; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROCESSING; RAT; TRANSCRIPTION REGULATION; UPREGULATION; ANIMAL; C57BL MOUSE; CELL HYPOXIA; DOWN REGULATION; GENETICS; GLYCOSYLATION; HEART FUNCTION TEST; HEART MUSCLE; HEK293 CELL LINE; HUMAN; METABOLISM; MOLECULAR GENETICS; PATHOLOGY; PATHOPHYSIOLOGY; SPRAGUE DAWLEY RAT;

3' UNTRANSLATED REGIONS; ANIMALS; BASE SEQUENCE; BETA-N-ACETYLHEXOSAMINIDASES; CELL HYPOXIA; DOWN-REGULATION; GLYCOSYLATION; HEART FAILURE; HEART FUNCTION TESTS; HEK293 CELLS; HUMANS; MICE, INBRED C57BL; MICRORNAS; MOLECULAR SEQUENCE DATA; MYOCARDIAL INFARCTION; MYOCARDIUM; MYOCYTES, CARDIAC; OXYGEN; RATS, SPRAGUE-DAWLEY; UP-REGULATION;

EID: 84908462087     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.578682     Document Type: Article

References (52)

1. Mudd, J. O., and Kass, D. A. (2008) Tackling heart failure in the twenty-first century. Nature 451, 919-928
2. Ngoh, G. A., and Jones, S. P. (2008) New insights into metabolic signaling and cell survival: the role of β-O-linkage of N-acetylglucosamine. J. Pharmacol. Exp. Ther. 327, 602-609
3. Zachara, N. E., and Hart, G. W. (2006) Cell signaling, the essential role of O-GlcNAc!. Biochim. Biophys. Acta 1761, 599-617
4. Jones, S. P., Zachara, N. E., Ngoh, G. A., Hill, B. G., Teshima, Y., Bhatnagar, A., Hart, G. W., and Marbán, E. (2008) Cardioprotection by N-acetylglucosamine linkage to cellular proteins. Circulation 117, 1172-1182
5. Laczy, B. (2009) Protein O-GlcNAcylation: a new signaling paradigm for the cardiovascular system. Am. J. Physiol. Heart Circ. Physiol. 296, H13-H28
6. Hart, G. W., Slawson, C., Ramirez-Correa, G., and Lagerlof, O. (2011) Cross talk between O-GlcNAcylation and phosphorylation: roles in signaling, transcription, and chronic disease. Annu. Rev. Biochem. 80, 825-858
7. Zachara, N. E., O'Donnell, N., Cheung, W. D., Mercer, J. J., Marth, J. D., and Hart, G. W. (2004) Dynamic O-GlcNAc modification of nucleocytoplasmic proteins in response to stress. A survival response of mammalian cells. J. Biol. Chem. 279, 30133-30142
8. Champattanachai, V., Marchase, R. B., and Chatham, J. C. (2007) Glucosamine protects neonatal cardiomyocytes from ischemia-reperfusion injury via increased proteinassociated O-GlcNAc. Am. J. Physiol. Cell Physiol. 292, C178-C187
9. Zafir, A., Readnower, R., Long, B. W., McCracken, J., Aird, A., Alvarez, A., Cummins, T. D., Li, Q., Hill, B. G., Bhatnagar, A., Prabhu, S. D., Bolli, R., and Jones, S. P. (2013) Protein O-GlcNAcylation is a novel cytoprotective signal in cardiac stem cells. Stem Cells 31, 765-775
10. Ngoh, G. A., Facundo, H. T., Zafir, A., and Jones, S. P. (2010) O-GlcNAc signaling in the cardiovascular system. Circ. Res. 107, 171-185
11. Watson, L. J., Facundo, H. T., Ngoh, G. A., Ameen, M., Brainard, R. E., Lemma, K. M., Long, B. W., Prabhu, S. D., Xuan, Y. T., and Jones, S. P. (2010) O-Linked β-N-acetylglucosamine transferase is indispensable in the failing heart. Proc. Natl. Acad. Sci. U.S.A. 107, 17797-17802
12. Small, E. M., and Olson, E. N. (2011) Pervasive roles of microRNAs in cardiovascular biology. Nature 469, 336-342
13. D'Alessandra, Y., Devanna, P., Limana, F., Straino, S., Di Carlo, A., Brambilla, P. G., Rubino, M., Carena, M. C., Spazzafumo, L., De Simone, M., Micheli, B., Biglioli, P., Achilli, F., Martelli, F., Maggiolini, S., Marenzi, G., Pompilio, G., and Capogrossi, M. C. (2010) Circulating microRNAs are new and sensitive biomarkers of myocardial infarction. Eur. Heart J. 31, 2765-2773
14. Divakaran, V., and Mann, D. L. (2008) The emerging role of microRNAs in cardiac remodeling and heart failure. Circ. Res. 103, 1072-1083
15. Dong, S., Cheng, Y., Yang, J., Li, J., Liu, X., Wang, X., Wang, D., Krall, T. J., Delphin, E. S., and Zhang, C. (2009) MicroRNA expression signature and the role of microRNA-21 in the early phase of acute myocardial infarction. J. Biol. Chem. 284, 29514-29525
16. Brainard, R. E., Watson, L. J., Demartino, A. M., Brittian, K. R., Readnower, R. D., Boakye, A. A., Zhang, D., Hoetker, J. D., Bhatnagar, A., Baba, S. P., and Jones, S. P. (2013) High fat feeding in mice is insufficient to induce cardiac dysfunction and does not exacerbate heart failure. PloS One 8, e83174
17. Jones, S. P., Greer, J. J., van Haperen, R., Duncker, D. J., de Crom, R., and Lefer, D. J. (2003) Endothelial nitric oxide synthase overexpression attenuates congestive heart failure in mice. Proc. Natl. Acad. Sci. U.S.A. 100, 4891-4896
18. Jones, S. P., and Lefer, D. J. (2001) Cardioprotective actions of acute HMG-CoA reductase inhibition in the setting of myocardial infarction. Acta Physiol. Scand. 173, 139-143
19. Greer, J. J., Kakkar, A. K., Elrod, J. W., Watson, L. J., Jones, S. P., and Lefer, D. J. (2006) Low-dose simvastatin improves survival and ventricular function via eNOS in congestive heart failure. Am. J. Physiol. Heart Circ. Physiol. 291, H2743-H2751
20. Jones, S. P., Greer, J. J., Ware, P. D., Yang, J., Walsh, K., and Lefer, D. J. (2005) Deficiency of iNOS does not attenuate severe congestive heart failure in mice. Am. J. Physiol. Heart Circ. Physiol. 288, H365-H370
21. Watson, L. J., Long, B. W., DeMartino, A. M., Brittian, K. R., Readnower, R. D., Brainard, R. E., Cummins, T. D., Annamalai, L., Hill, B. G., and Jones, S. P. (2014) Cardiomyocyte Ogt is essential for postnatal viability. Am. J. Physiol. Heart Circ. Physiol. 306, H142-H153
22. Sansbury, B. E., DeMartino, A. M., Xie, Z., Brooks, A. C., Brainard, R. E., Watson, L. J., DeFilippis, A. P., Cummins, T. D., Harbeson, M. A., Brittian, K. R., Prabhu, S. D., Bhatnagar, A., Jones, S. P., and Hill, B. G. (2014) Metabolomic analysis of pressure-overloaded and infarcted mouse hearts. Circulation 7, 634-642
23. Jones, S. P., Teshima, Y., Akao, M., and Marbán, E. (2003) Simvastatin attenuates oxidant-induced mitochondrial dysfunction in cardiac myocytes. Circ. Res. 93, 697-699
24. Facundo, H. T., Brainard, R. E., Watson, L. J., Ngoh, G. A., Hamid, T., Prabhu, S. D., and Jones, S. P. (2012) O-GlcNAc signaling is essential for NFAT-mediated transcriptional reprogramming during cardiomyocyte hypertrophy. Am. J. Physiol. Heart Circ. Physiol. 302, H2122-H2130
25. Obernosterer, G., Martinez, J., and Alenius, M. (2007) Locked nucleic acid-based in situ detection of microRNAs in mouse tissue sections. Nat. Protoc. 2, 1508-1514
26. Lewis, B. P., Burge, C. B., and Bartel, D. P. (2005) Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120, 15-20
27. Ozcan, S., Andrali, S. S., and Cantrell, J. E. (2010) Modulation of transcription factor function by O-GlcNAc modification. Biochim. Biophys. Acta 1799, 353-364
28. Hart, G. W., Housley, M. P., and Slawson, C. (2007) Cycling of O-linked β-N-acetylglucosamine on nucleocytoplasmic proteins. Nature 446, 1017-1022
29. Housley, M. P., Rodgers, J. T., Udeshi, N. D., Kelly, T. J., Shabanowitz, J., Hunt, D. F., Puigserver, P., and Hart, G. W. (2008) O-GlcNAc regulates FoxO activation in response to glucose. J. Biol. Chem. 283, 16283-16292
30. Slawson, C., Zachara, N. E., Vosseller, K., Cheung, W. D., Lane, M. D., and Hart, G. W. (2005) Perturbations in O-linked β-N-acetylglucosamine protein modification cause severe defects in mitotic progression and cytokinesis. J. Biol. Chem. 280, 32944-32956
31. Groves, J. A., Lee, A., Yildirir, G., and Zachara, N. E. (2013) Dynamic O-GlcNAcylation and its roles in the cellular stress response and homeostasis. Cell Stress Chaperones 18, 535-558
32. Ngoh, G. A., Hamid, T., Prabhu, S. D., and Jones, S. P. (2009) O-GlcNAc signaling attenuates ER stress-induced cardiomyocyte death. Am. J. Physiol. Heart Circ. Physiol. 297, H1711-H1719
33. Ngoh, G. A., Watson, L. J., Facundo, H. T., and Jones, S. P. (2011) Augmented O-GlcNAc signaling attenuates oxidative stress and calcium overload in cardiomyocytes. Amino Acids 40, 895-911
34. Thum, T., Gross, C., Fiedler, J., Fischer, T., Kissler, S., Bussen, M., Galuppo, P., Just, S., Rottbauer, W., Frantz, S., Castoldi, M., Soutschek, J., Koteliansky, V., Rosenwald, A., Basson, M. A., Licht, J. D., Pena, J. T., Rouhanifard, S. H., Muckenthaler, M. U., Tuschl, T., Martin, G. R., Bauersachs, J., and Engelhardt, S. (2008) MicroRNA-21 contributes to myocardial disease by stimulating MAP kinase signalling in fibroblasts. Nature 456, 980-984
35. van Rooij, E., Sutherland, L. B., Thatcher, J. E., DiMaio, J. M., Naseem, R. H., Marshall, W. S., Hill, J. A., and Olson, E. N. (2008) Dysregulation of microRNAs after myocardial infarction reveals a role of miR-29 in cardiac fibrosis. Proc. Natl. Acad. Sci. U.S.A. 105, 13027-13032
36. Callis, T. E., Pandya, K., Seok, H. Y., Tang, R. H., Tatsuguchi, M., Huang, Z. P., Chen, J. F., Deng, Z., Gunn, B., Shumate, J., Willis, M. S., Selzman, C. H., and Wang, D. Z. (2009) MicroRNA-208a is a regulator of cardiac hypertrophy and conduction in mice. J. Clin. Invest. 119, 2772-2786
37. van Rooij, E., Sutherland, L. B., Qi, X., Richardson, J. A., Hill, J., and Olson, E. N. (2007) Control of stress-dependent cardiac growth and gene expression by a microRNA. Science 316, 575-579
38. Carè, A., Catalucci, D., Felicetti, F., Bonci, D., Addario, A., Gallo, P., Bang, M. L., Segnalini, P., Gu, Y., Dalton, N. D., Elia, L., Latronico, M. V., Høydal, M., Autore, C., Russo, M. A., Dorn, G. W., 2nd, Ellingsen, O., Ruiz-Lozano, P., Peterson, K. L., Croce, C. M., Peschle, C., and Condorelli, G. (2007) MicroRNA-133 controls cardiac hypertrophy. Nat. Med. 13, 613-618
39. Najafi-Shoushtari, S. H., Kristo, F., Li, Y., Shioda, T., Cohen, D. E., Gerszten, R. E., and Näär, A. M. (2010) MicroRNA-33 and the SREBP host genes cooperate to control cholesterol homeostasis. Science 328, 1566-1569
40. Esau, C., Davis, S., Murray, S. F., Yu, X. X., Pandey, S. K., Pear, M., Watts, L., Booten, S. L., Graham, M., McKay, R., Subramaniam, A., Propp, S., Lollo, B. A., Freier, S., Bennett, C. F., Bhanot, S., and Monia, B. P. (2006) miR-122 regulation of lipid metabolism revealed by in vivo antisense targeting. Cell Metab. 3, 87-98
41. Milosevic, J., Pandit, K., Magister, M., Rabinovich, E., Ellwanger, D. C., Yu, G., Vuga, L. J., Weksler, B., Benos, P. V., Gibson, K. F., McMillan, M., Kahn, M., and Kaminski, N. (2012) Profibrotic role of miR-154 in pulmonary fibrosis. Am. J. Respir. Cell Mol. Biol. 47, 879-887
42. Wang, K., Long, B., Zhou, L. Y., Liu, F., Zhou, Q. Y., Liu, C. Y., Fan, Y. Y., and Li, P. F. (2014) CARL lncRNA inhibits anoxia-induced mitochondrial fission and apoptosis in cardiomyocytes by impairing miR-539-dependent PHB2 down-regulation. Nat. Commun. 5, 3596
43. Lee, Y. N., Brandal, S., Noel, P., Wentzel, E., Mendell, J. T., McDevitt, M. A., Kapur, R., Carter, M., Metcalfe, D. D., and Takemoto, C. M. (2011) KIT signaling regulates MITF expression through miRNAs in normal and malignant mast cell proliferation. Blood 117, 3629-3640
44. Rodríguez-Meléndez, R., Cano, S., Méndez, S. T., and Velázquez, A. (2001) Biotin regulates the genetic expression of holocarboxylase synthetase and mitochondrial carboxylases in rats. J. Nutr. 131, 1909-1913
45. Lima, V. V., Giachini, F. R., Choi, H., Carneiro, F. S., Carneiro, Z. N., Fortes, Z. B., Carvalho, M. H., Webb, R. C., and Tostes, R. C. (2009) Impaired vasodilator activity in deoxycorticosterone acetate-salt hypertension is associated with increased protein O-GlcNAcylation. Hypertension 53, 166-174
46. Laczy, B., Marsh, S. A., Brocks, C. A., Wittmann, I., and Chatham, J. C. (2010) Inhibition of O-GlcNAcase in perfused rat hearts by NAG-thiazolines at the time of reperfusion is cardioprotective in an O-GlcNAc-dependent manner. Am. J. Physiol. Heart Circ. Physiol. 299, H1715-H1727
47. Marsh, S. A., Dell'Italia, L. J., and Chatham, J. C. (2011) Activation of the hexosamine biosynthesis pathway and protein O-GlcNAcylation modulate hypertrophic and cell signaling pathways in cardiomyocytes from diabetic mice. Amino Acids 40, 819-828
48. Deng, Y., Li, B., Liu, Y., Iqbal, K., Grundke-Iqbal, I., and Gong, C. X. (2009) Dysregulation of insulin signaling, glucose transporters, O-GlcNAcylation, and phosphorylation of tau and neurofilaments in the brain: implication for Alzheimer's disease. Am. J. Pathol. 175, 2089-2098
49. Yuzwa, S. A., Macauley, M. S., Heinonen, J. E., Shan, X., Dennis, R. J., He, Y., Whitworth, G. E., Stubbs, K. A., McEachern, E. J., Davies, G. J., and Vocadlo, D. J. (2008) A potent mechanism-inspired O-GlcNAcase inhibitor that blocks phosphorylation of Tau in vivo. Nat. Chem. Biol. 4, 483-490
50. Jacobsen, K. T., and Iverfeldt, K. (2011) O-GlcNAcylation increases non-amyloidogenic processing of the amyloid-β precursor protein (APP). Biochem. Biophys. Res. Commun. 404, 882-886
51. Ma, Z., and Vosseller, K. (2013) O-GlcNAc in cancer biology. Amino Acids 45, 719-733
52. Mi, W., Gu, Y., Han, C., Liu, H., Fan, Q., Zhang, X., Cong, Q., and Yu, W. (2011) O-GlcNAcylation is a novel regulator of lung and colon cancer malignancy. Biochim. Biophys. Acta 1812, 514-519