High Glucose-induced repression of RAR/RXR in cardiomyocytes is mediated through oxidative stress/JNK signaling

Journal of Cellular Physiology

Volumn 227, Issue 6, 2012, Pages 2632-2644

  Singh, Amar B ^a   Guleria, Rakeshwar S ^a   Nizamutdinova, Irina T ^a   Baker, Kenneth M ^a   Pan, Jing ^a  

^a TEXAS A M COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; GLUCOSE; HYDROGEN PEROXIDE; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE P38; REACTIVE OXYGEN METABOLITE; RETINOIC ACID; RETINOIC ACID RECEPTOR ALPHA; RETINOID X RECEPTOR ALPHA; SERINE; STRESS ACTIVATED PROTEIN KINASE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; ENZYME INHIBITION; GENE ACTIVITY; GENE OVEREXPRESSION; GENE REPRESSION; GENE SILENCING; HEART MUSCLE CELL; HYPERGLYCEMIA; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RAT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION;

ANIMALS; ANIMALS, NEWBORN; APOPTOSIS; CYSTEINE PROTEINASE INHIBITORS; DOSE-RESPONSE RELATIONSHIP, DRUG; GLUCOSE; HEK293 CELLS; HUMANS; HYPERGLYCEMIA; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MAP KINASE KINASE 7; MAP KINASE KINASE KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MYOCYTES, CARDIAC; OXIDANTS; OXIDATIVE STRESS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; PROMOTER REGIONS, GENETIC; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN KINASE INHIBITORS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, RETINOIC ACID; RETINOID X RECEPTOR ALPHA; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSCRIPTIONAL ACTIVATION; TRANSFECTION; TRETINOIN;

EID: 84863393440     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.23005     Document Type: Article

References (61)

1. Adam-Stitah S, Penna L, Chambon P, Rochette-Egly C. 1999. Hyperphosphorylation of the retinoid X receptor alpha by activated c-Jun NH2-terminal kinases. J Biol Chem 274:18932-18941.
2. Aikawa R, Komuro I, Yamazaki T, Zou Y, Kudoh S, Tanaka M, Shiojima I, Hiroi Y, Yazaki Y. 1997. Oxidative stress activates extracellular signal-regulated kinases through Src and Ras in cultured cardiac myocytes of neonatal rats. J Clin Invest 100:1813-1821.
3. Altucci L, Leibowitz MD, Ogilvie KM, de Lera AR, Gronemeyer H. 2007. RAR and RXR modulation in cancer and metabolic disease. Nat Rev Drug Discov 6:793-810.
4. Baena RM, Campoy C, Bayes R, Blanca E, Fernandez JM, Molina-Font JA. 2002. Vitamin A, retinol binding protein and lipids in type 1 diabetes mellitus. Eur J Clin Nutr 56:44-50.
5. Bastien J, Rochette-Egly C. 2004. Nuclear retinoid receptors and the transcription of retinoid-target genes. Gene 328:1-16.
6. Basu TK, Tze WJ, Leichter J. 1989. Serum vitamin A and retinol-binding protein in patients with insulin-dependent diabetes mellitus. Am J Clin Nutr 50:329-331.
7. Basualdo CG, Wein EE, Basu TK. 1997. Vitamin A (retinol) status of first nation adults with non-insulin-dependent diabetes mellitus. J Am Coll Nutr 16:39-45.
8. Baynes JW. 1991. Role of oxidative stress in development of complications in diabetes. Diabetes 40:405-412.
9. Bour G, Gaillard E, Bruck N, Lalevee S, Plassat JL, Busso D, Samama JP, Rochette-Egly C. 2005. Cyclin H binding to the RARalpha activation function (AF)-2 domain directs phosphorylation of the AF-1 domain by cyclin-dependent kinase 7. Proc Natl Acad Sci USA 102:16608-16613.
10. Bour G, Lalevee S, Rochette-Egly C. 2007. Protein kinases and the proteasome join in the combinatorial control of transcription by nuclear retinoic acid receptors. Trends Cell Biol 17:302-309.
11. Bruck N, Bastien J, Bour G, Tarrade A, Plassat JL, Bauer A, Adam-Stitah S, Rochette-Egly C. 2005. Phosphorylation of the retinoid x receptor at the omega loop, modulates the expression of retinoic-acid-target genes with a promoter context specificity. Cell Signal 17:1229-1239.
12. Bruck N, Vitoux D, Ferry C, Duong V, Bauer A, de The H, Rochette-Egly C. 2009. A coordinated phosphorylation cascade initiated by p38MAPK/MSK1 directs RARalpha to target promoters. EMBO J 28:34-47.
13. Cai L, Wang Y, Zhou G, Chen T, Song Y, Li X, Kang YJ. 2006. Attenuation by metallothionein of early cardiac cell death via suppression of mitochondrial oxidative stress results in a prevention of diabetic cardiomyopathy. J Am Coll Cardiol 48:1688-1697.
14. Choi SW, Benzie IF, Ma SW, Strain JJ, Hannigan BM. 2008. Acute hyperglycemia and oxidative stress: Direct cause and effect? Free Radic Biol Med 44:1217-1231.
15. Choudhary R, Baker KM, Pan J. 2008a. All-trans retinoic acid prevents angiotensin II- and mechanical stretch-induced reactive oxygen species generation and cardiomyocyte apoptosis. J Cell Physiol 215:172-181.
16. Choudhary R, Palm-Leis A, Scott RC III, Guleria RS, Rachut E, Baker KM, Pan J. 2008b. All-trans retinoic acid prevents development of cardiac remodeling in aortic banded rats by inhibiting the renin-angiotensin system. Am J Physiol Heart Circ Physiol 294:H633-H644.
17. Clerk A, Fuller SJ, Michael A, Sugden PH. 1998. Stimulation of "stress-regulated" mitogen-activated protein kinases (stress-activated protein kinases/c-Jun N-terminal kinases and p38-mitogen-activated protein kinases) in perfused rat hearts by oxidative and other stresses. J Biol Chem 273:7228-7234.
18. Feingold K, Kim MS, Shigenaga J, Moser A, Grunfeld C. 2004. Altered expression of nuclear hormone receptors and coactivators in mouse heart during the acute-phase response. Am J Physiol Endocrinol Metab 286:E201-E207.
19. Fiordaliso F, Bianchi R, Staszewsky L, Cuccovillo I, Doni M, Laragione T, Salio M, Savino C, Melucci S, Santangelo F, Scanziani E, Masson S, Ghezzi P, Latini R. 2004. Antioxidant treatment attenuates hyperglycemia-induced cardiomyocyte death in rats. J Mol Cell Cardiol 37:959-968.
20. Giacco F, Brownlee M. 2010. Oxidative stress and diabetic complications. Circ Res 107:1058-1070.
21. Gianni M, Bauer A, Garattini E, Chambon P, Rochette-Egly C. 2002. Phosphorylation by p38MAPK and recruitment of SUG-1 are required for RA-induced RAR gamma degradation and transactivation. EMBO J 21:3760-3769.
22. Guleria RS, Choudhary R, Tanaka T, Baker KM, Pan J. 2011. Retinoic acid receptor-mediated signaling protects cardiomyocytes from hyperglycemia induced apoptosis: Role of the renin-angiotensin system. J Cell Physiol 226:1292-1307.
23. Gurusamy N, Watanabe K, Ma M, Zhang S, Muslin AJ, Kodama M, Aizawa Y. 2004. Dominant negative 14-3-3 promotes cardiomyocyte apoptosis in early stage of type I diabetes mellitus through activation of JNK. Biochem Biophys Res Commun 320:773-780.
24. Hirosumi J, Tuncman G, Chang L, Gorgun CZ, Uysal KT, Maeda K, Karin M, Hotamisligil GS. 2002. A central role for JNK in obesity and insulin resistance. Nature 420:333-336.
25. Ho KK, Pinsky JL, Kannel WB, Levy D. 1993. The epidemiology of heart failure: The Framingham Study. J Am Coll Cardiol 22:6A-13A.
26. Hoshikawa Y, Kanki K, Ashla AA, Arakaki Y, Azumi J, Yasui T, Tezuka Y, Matsumi Y, Tsuchiya H, Kurimasa A, Hisatome I, Hirano T, Fujimoto J, Kagechika H, Shomori K, Ito H, Shiota G. 2011. c-Jun N-terminal kinase activation by oxidative stress suppresses retinoid signaling through proteasomal degradation of RARalpha protein in hepatic cells. Cancer Sci 102:934-941.
27. Jacques PF, Hartz SC, Chylack LT, Jr., McGandy RB, Sadowski JA. 1988. Nutritional status in persons with and without senile cataract: Blood vitamin and mineral levels. Am J Clin Nutr 48:152-158.
28. Krempf M, Ranganathan S, Ritz P, Morin M, Charbonnel B. 1991. Plasma vitamin A and E in type 1 (insulin-dependent) and type 2 (non-insulin-dependent) adult diabetic patients. Int J Vitam Nutr Res 61:38-42.
29. Lee HY, Suh YA, Robinson MJ, Clifford JL, Hong WK, Woodgett JR, Cobb MH, Mangelsdorf DJ, Kurie JM. 2000. Stress pathway activation induces phosphorylation of retinoid X receptor. J Biol Chem 275:32193-32199.
30. Liang JL, Xiao DZ, Liu XY, Lin QX, Shan ZX, Zhu JN, Lin SG, Yu XY. 2010. High glucose induces apoptosis in AC16 human cardiomyocytes via macrophage migration inhibitory factor and c-Jun N-terminal kinase. Clin Exp Pharmacol Physiol 37:969-973.
31. Lu J, Dixon WT, Tsin AT, Basu TK. 2000. The metabolic availability of vitamin A is decreased at the onset of diabetes in BB rats. J Nutr 130:1958-1962.
32. Matsushima-Nishiwaki R, Okuno M, Adachi S, Sano T, Akita K, Moriwaki H, Friedman SL, Kojima S. 2001. Phosphorylation of retinoid X receptor alpha at serine 260 impairs its metabolism and function in human hepatocellular carcinoma. Cancer Res 61:7675-7682.
33. Minucci S, Ozato K. 1996. Retinoid receptors in transcriptional regulation. Curr Opin Genet Dev 6:567-574.
34. Monnier L, Mas E, Ginet C, Michel F, Villon L, Cristol JP, Colette C. 2006. Activation of oxidative stress by acute glucose fluctuations compared with sustained chronic hyperglycemia in patients with type 2 diabetes. JAMA 295:1681-1687.
35. Murarka S, Movahed MR. 2010. Diabetic cardiomyopathy. J Card Fail 16:971-979.
36. Napoli JL. 1986. Quantification of physiological levels of retinoic acid. Methods Enzymol 123:112-124.
37. Napoli JL. 1996. Biochemical pathways of retinoid transport, metabolism, and signal transduction. Clin Immunol Immunopathol 80:S52-S62.
38. Osorio JC, Stanley WC, Linke A, Castellari M, Diep QN, Panchal AR, Hintze TH, Lopaschuk GD, Recchia FA. 2002. Impaired myocardial fatty acid oxidation and reduced protein expression of retinoid X receptor-alpha in pacing-induced heart failure. Circulation 106:606-612.
39. Palm-Leis A, Singh US, Herbelin BS, Olsovsky GD, Baker KM, Pan J. 2004. Mitogen-activated protein kinases and mitogen-activated protein kinase phosphatases mediate the inhibitory effects of all-trans retinoic acid on the hypertrophic growth of cardiomyocytes. J Biol Chem 279:54905-54917.
40. Pan J, Fukuda K, Saito M, Matsuzaki J, Kodama H, Sano M, Takahashi T, Kato T, Ogawa S. 1999. Mechanical stretch activates the JAK/STAT pathway in rat cardiomyocytes. Circ Res 84:1127-1136.
41. Rochette-Egly C. 2003. Nuclear receptors: Integration of multiple signalling pathways through phosphorylation. Cell Signal 15:355-366.
42. Rochette-Egly C, Oulad-Abdelghani M, Staub A, Pfister V, Scheuer I, Chambon P, Gaub MP. 1995. Phosphorylation of the retinoic acid receptor-alpha by protein kinase A. Mol Endocrinol 9:860-871.
43. Rochette-Egly C, Adam S, Rossignol M, Egly JM, Chambon P. 1997. Stimulation of RAR alpha activation function AF-1 through binding to the general transcription factor TFIIH and phosphorylation by CDK7. Cell 90:97-107.
44. Sabio G, Kennedy NJ, Cavanagh-Kyros J, Jung DY, Ko HJ, Ong H, Barrett T, Kim JK, Davis RJ. 2010. Role of muscle c-Jun NH2-terminal kinase 1 in obesity-induced insulin resistance. Mol Cell Biol 30:106-115.
45. Salazar J, Guardiola M, Ferre R, Coll B, Alonso-Villaverde C, Winklhofer-Roob BM, Rock E, Fernandez-Ballart JD, Civeira F, Pocovi M, Masana L, Ribalta J. 2007. Association of a polymorphism in the promoter of the cellular retinoic acid-binding protein II gene (CRABP2) with increased circulating low-density lipoprotein cholesterol. Clin Chem Lab Med 45:615-620.
46. Solomon C, White JH, Kremer R. 1999. Mitogen-activated protein kinase inhibits 1, 25-dihydroxyvitamin D3-dependent signal transduction by phosphorylating human retinoid X receptor alpha. J Clin Invest 103:1729-1735.
47. Srinivas H, Juroske DM, Kalyankrishna S, Cody DD, Price RE, Xu XC, Narayanan R, Weigel NL, Kurie JM. 2005. c-Jun N-terminal kinase contributes to aberrant retinoid signaling in lung cancer cells by phosphorylating and inducing proteasomal degradation of retinoic acid receptor alpha. Mol Cell Biol 25:1054-1069.
48. Tang M, Zhang W, Lin H, Jiang H, Dai H, Zhang Y. 2007. High glucose promotes the production of collagen types I and III by cardiac fibroblasts through a pathway dependent on extracellular-signal-regulated kinase 1/2. Mol Cell Biochem 301:109-114.
49. Thandavarayan RA, Watanabe K, Ma M, Gurusamy N, Veeraveedu PT, Konishi T, Zhang S, Muslin AJ, Kodama M, Aizawa Y. 2009. Dominant-negative p38alpha mitogen-activated protein kinase prevents cardiac apoptosis and remodeling after streptozotocin-induced diabetes mellitus. Am J Physiol Heart Circ Physiol 297:H911-H919.
50. Tuitoek PJ, Ziari S, Tsin AT, Rajotte RV, Suh M, Basu TK. 1996. Streptozotocin-induced diabetes in rats is associated with impaired metabolic availability of vitamin A (retinol). Br J Nutr 75:615-622.
51. Turner NA, Xia F, Azhar G, Zhang X, Liu L, Wei JY. 1998. Oxidative stress induces DNA fragmentation and caspase activation via the c-Jun NH2-terminal kinase pathway in H9c2 cardiac muscle cells. J Mol Cell Cardiol 30:1789-1801.
52. Vallerie SN, Hotamisligil GS. 2010. The role of JNK proteins in metabolism. Sci Transl Med 2:6orv5.
53. Van YH, Lee WH, Ortiz S, Lee MH, Qin HJ, Liu CP. 2009. All-trans retinoic acid inhibits type 1 diabetes by T regulatory (Treg)-dependent suppression of interferon-gamma-producing T-cells without affecting Th17 cells. Diabetes 58:146-155.
54. Wang HJ, Zhu YC, Yao T. 2002. Effects of all-trans retinoic acid on angiotensin II-induced myocyte hypertrophy. J Appl Physiol 92:2162-2168.
55. Wu J, Garami M, Cheng T, Gardner DG. 1996. 1, 25(OH)2 vitamin D3, and retinoic acid antagonize endothelin-stimulated hypertrophy of neonatal rat cardiac myocytes. J Clin Invest 97:1577-1588.
56. Yamauchi T, Waki H, Kamon J, Murakami K, Motojima K, Komeda K, Miki H, Kubota N, Terauchi Y, Tsuchida A, Tsuboyama-Kasaoka N, Yamauchi N, Ide T, Hori W, Kato S, Fukayama M, Akanuma Y, Ezaki O, Itai A, Nagai R, Kimura S, Tobe K, Kagechika H, Shudo K, Kadowaki T. 2001. Inhibition of RXR and PPARgamma ameliorates diet-induced obesity and type 2 diabetes. J Clin Invest 108:1001-1013.
57. Yang Q, Graham TE, Mody N, Preitner F, Peroni OD, Zabolotny JM, Kotani K, Quadro L, Kahn BB. 2005. Serum retinol binding protein 4 contributes to insulin resistance in obesity and type 2 diabetes. Nature 436:356-362.
58. Zhou MD, Sucov HM, Evans RM, Chien KR. 1995. Retinoid-dependent pathways suppress myocardial cell hypertrophy. Proc Natl Acad Sci USA 92:7391-7395.
59. Zhou H, Li YJ, Wang M, Zhang LH, Guo BY, Zhao ZS, Meng FL, Deng YG, Wang RY. 2011. Involvement of RhoA/ROCK in myocardial fibrosis in a rat model of type 2 diabetes. Acta Pharmacol Sin 32:999-1008.
60. Zhu J, Gianni M, Kopf E, Honore N, Chelbi-Alix M, Koken M, Quignon F, Rochette-Egly C, de The H. 1999. Retinoic acid induces proteasome-dependent degradation of retinoic acid receptor alpha (RARalpha) and oncogenic RARalpha fusion proteins. Proc Natl Acad Sci USA 96:14807-14812.
61. Zizola CF, Frey SK, Jitngarmkusol S, Kadereit B, Yan N, Vogel S. 2010. Cellular retinol-binding protein type I (CRBP-I) regulates adipogenesis. Mol Cell Biol 30:3412-3420.