CHOP deficiency prevents methylglyoxal-induced myocyte apoptosis and cardiac dysfunction

Journal of Molecular and Cellular Cardiology

Volumn 85, Issue , 2015, Pages 168-177

  Nam, Dae Hwan ^a   Han, Jung Hwa ^a   Lee, Tae Jin ^a   Shishido, Tetsuro ^b   Lim, Jae Hyang ^c   Kim, Geun Young ^d   Woo, Chang Hoon ^a  

^a Yeungnam University College of Medicine   (South Korea)

^b YAMAGATA UNIVERSITY   (Japan)

^c Ewha Womans University School of Medicine   (South Korea)

^d Korea National Institute of Health   (South Korea)

Author keywords

Cardiac dysfunction; CHOP; Diabetes; ER stress; Methylglyoxal

Indexed keywords

CASPASE 3; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; METHYLGLYOXAL; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; SMALL INTERFERING RNA; DDIT3 PROTEIN, RAT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DIABETES MELLITUS; EMBRYO; GENE INACTIVATION; HEART DISEASE; HEART MUSCLE CELL; IMPAIRED GLUCOSE TOLERANCE; IN VIVO STUDY; INFLAMMATION; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; RAT; UNFOLDED PROTEIN RESPONSE; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; CARDIAC MUSCLE CELL; CELL CULTURE; DRUG EFFECTS; ENDOPLASMIC RETICULUM STRESS; GENE SILENCING; GENETICS; HEART STROKE VOLUME; KNOCKOUT MOUSE; METABOLISM; MYOCARDITIS; PATHOPHYSIOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

MUS; RATTUS;

ANIMALS; APOPTOSIS; CELLS, CULTURED; ENDOPLASMIC RETICULUM STRESS; GENE KNOCKDOWN TECHNIQUES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYOCARDITIS; MYOCYTES, CARDIAC; PYRUVALDEHYDE; RATS, SPRAGUE-DAWLEY; STROKE VOLUME; TRANSCRIPTION FACTOR CHOP; UNFOLDED PROTEIN RESPONSE;

EID: 84931262390     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2015.05.016     Document Type: Article

References (64)

1. Haffner S.M., Lehto S., Ronnemaa T., Pyorala K., Laakso M. Mortality from coronary heart disease in subjects with type 2 diabetes and in nondiabetic subjects with and without prior myocardial infarction. N Engl J Med 1998, 339:229-234.
2. Domanski M., Krause-Steinrauf H., Deedwania P., Follmann D., Ghali J.K., Gilbert E., et al. The effect of diabetes on outcomes of patients with advanced heart failure in the BEST trial. J Am Coll Cardiol 2003, 42:914-922.
3. Ozcan U., Cao Q., Yilmaz E., Lee A.H., Iwakoshi N.N., Ozdelen E., et al. Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science 2004, 306:457-461.
4. Back S.H., Kaufman R.J. Endoplasmic reticulum stress and type 2 diabetes. Annu Rev Biochem 2012, 81:767-793.
5. McLellan A.C., Thornalley P.J., Benn J., Sonksen P.H. Glyoxalase system in clinical diabetes mellitus and correlation with diabetic complications. Clin Sci (Lond) 1994, 87:21-29.
6. Ramasamy R., Yan S.F., Schmidt A.M. Methylglyoxal comes of AGE. Cell 2006, 124:258-260.
7. Randell E.W., Vasdev S., Gill V. Measurement of methylglyoxal in rat tissues by electrospray ionization mass spectrometry and liquid chromatography. J Pharmacol Toxicol Methods 2005, 51:153-157.
8. Thornalley P.J., Langborg A., Minhas H.S. Formation of glyoxal, methylglyoxal and 3-deoxyglucosone in the glycation of proteins by glucose. Biochem J 1999, 344(Pt 1):109-116.
9. Yamawaki H., Saito K., Okada M., Hara Y. Methylglyoxal mediates vascular inflammation via JNK and p38 in human endothelial cells. Am J Physiol Cell Physiol 2008, 295:C1510-C1517.
10. Bourajjaj M., Stehouwer C.D., van Hinsbergh V.W., Schalkwijk C.G. Role of methylglyoxal adducts in the development of vascular complications in diabetes mellitus. Biochem Soc Trans 2003, 31:1400-1402.
11. Dhar A., Desai K., Liu J., Wu L. Methylglyoxal, protein binding and biological samples: are we getting the true measure?. J Chromatogr B Analyt Technol Biomed Life Sci 2009, 877:1093-1100.
12. Mao W., Iwai C., Liu J., Sheu S.S., Fu M., Liang C.S. Darbepoetin alfa exerts a cardioprotective effect in autoimmune cardiomyopathy via reduction of ER stress and activation of the PI3K/Akt and STAT3 pathways. J Mol Cell Cardiol 2008, 45:250-260.
13. Xu J., Zhou Q., Xu W., Cai L. Endoplasmic reticulum stress and diabetic cardiomyopathy. Exp Diabetes Res 2012, 2012:827971.
14. Schroder M., Kaufman R.J. ER stress and the unfolded protein response. Mutat Res 2005, 569:29-63.
15. Oyadomari S., Mori M. Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ 2004, 11:381-389.
16. Szegezdi E., Logue S.E., Gorman A.M., Samali A. Mediators of endoplasmic reticulum stress-induced apoptosis. EMBO Rep 2006, 7:880-885.
17. Minamino T., Kitakaze M. ER stress in cardiovascular disease. J Mol Cell Cardiol 2010, 48:1105-1110.
18. Wu T., Dong Z., Geng J., Sun Y., Liu G., Kang W., et al. Valsartan protects against ER stress-induced myocardial apoptosis via CHOP/Puma signaling pathway in streptozotocin-induced diabetic rats. Eur J Pharm Sci 2011, 42:496-502.
19. Hamada H., Suzuki M., Yuasa S., Mimura N., Shinozuka N., Takada Y. Dilated cardiomyopathy caused by aberrant endoplasmic reticulum quality control in mutant KDEL receptor transgenic mice. Mol Cell Biol 2004, 24:8007-8017.
20. Shen M., Wang L., Yang G., Gao L., Wang B., Guo X., et al. Baicalin protects the cardiomyocytes from ER stress-induced apoptosis: inhibition of CHOP through induction of endothelial nitric oxide synthase. PLoS One 2014, 9:e88389.
21. Pirot P., Ortis F., Cnop M., Ma Y., Hendershot L.M., Eizirik D.L., et al. Transcriptional regulation of the endoplasmic reticulum stress gene chop in pancreatic insulin-producing cells. Diabetes 2007, 56:1069-1077.
22. Chikka M.R., McCabe D.D., Tyra H.M., Rutkowski D.T. C/EBP homologous protein (CHOP) contributes to suppression of metabolic genes during endoplasmic reticulum stress in the liver. J Biol Chem 2013, 288:4405-4415.
23. Oyadomari S., Koizumi A., Takeda K., Gotoh T., Akira S., Araki E., et al. Targeted disruption of the Chop gene delays endoplasmic reticulum stress-mediated diabetes. J Clin Invest 2002, 109:525-532.
24. Song B., Scheuner D., Ron D., Pennathur S., Kaufman R.J. Chop deletion reduces oxidative stress, improves beta cell function, and promotes cell survival in multiple mouse models of diabetes. J Clin Invest 2008, 118:3378-3389.
25. Tamaki N., Hatano E., Taura K., Tada M., Kodama Y., Nitta T., et al. CHOP deficiency attenuates cholestasis-induced liver fibrosis by reduction of hepatocyte injury. Am J Physiol Gastrointest Liver Physiol 2008, 294:G498-G505.
26. Toriguchi K., Hatano E., Tanabe K., Takemoto K., Nakamura K., Koyama Y., et al. Attenuation of steatohepatitis, fibrosis, and carcinogenesis in mice fed a methionine-choline deficient diet by CCAAT/enhancer-binding protein homologous protein deficiency. J Gastroenterol Hepatol 2014, 29:1109-1118.
27. Chlopcikova S., Psotova J., Miketova P. Neonatal rat cardiomyocytes - a model for the study of morphological, biochemical and electrophysiological characteristics of the heart. Biomedical papers of the Medical Faculty of the University Palacky, Olomouc. Czechoslovakia 2001, 145:49-55.
28. White S.M., Constantin P.E., Claycomb W.C. 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 2004, 286:H823-H829.
29. Woo C.H., Le N.T., Shishido T., Chang E., Lee H., Heo K.S., et al. Novel role of C terminus of Hsc70-interacting protein (CHIP) ubiquitin ligase on inhibiting cardiac apoptosis and dysfunction via regulating ERK5-mediated degradation of inducible cAMP early repressor. FASEB J 2010, 24:4917-4928.
30. He Z., Ostrowski R.P., Sun X., Ma Q., Tang J., Zhang J.H. Targeting C/EBP homologous protein with siRNA attenuates cerebral vasospasm after experimental subarachnoid hemorrhage. Exp Neurol 2012, 238:218-224.
31. Kumagai T., Nangaku M., Kojima I., Nagai R., Ingelfinger J.R., Miyata T., et al. Glyoxalase I overexpression ameliorates renal ischemia-reperfusion injury in rats. Am J Physiol Renal Physiol 2009, 296:F912-F921.
32. Nigro P., Abe J., Woo C.H., Satoh K., McClain C., O'Dell M.R., et al. PKCzeta decreases eNOS protein stability via inhibitory phosphorylation of ERK5. Blood 2010, 116:1971-1979.
33. Liu Z.W., Zhu H.T., Chen K.L., Dong X., Wei J., Qiu C., et al. Protein kinase RNA-like endoplasmic reticulum kinase (PERK) signaling pathway plays a major role in reactive oxygen species (ROS)-mediated endoplasmic reticulum stress-induced apoptosis in diabetic cardiomyopathy. Cardiovasc Diabetol 2013, 12:158.
34. Thornalley P.J. Pharmacology of methylglyoxal: formation, modification of proteins and nucleic acids, and enzymatic detoxification - a role in pathogenesis and antiproliferative chemotherapy. Gen Pharmacol 1996, 27:565-573.
35. Miller A.G., Smith D.G., Bhat M., Nagaraj R.H. Glyoxalase I is critical for human retinal capillary pericyte survival under hyperglycemic conditions. J Biol Chem 2006, 281:11864-11871.
36. Ma H., Li S.Y., Xu P., Babcock S.A., Dolence E.K., Brownlee M., et al. Advanced glycation endproduct (AGE) accumulation and AGE receptor (RAGE) up-regulation contribute to the onset of diabetic cardiomyopathy. J Cell Mol Med 2009, 13:1751-1764.
37. Malhi H., Kropp E.M., Clavo V.F., Kobrossi C.R., Han J., Mauer A.S., et al. C/EBP homologous protein-induced macrophage apoptosis protects mice from steatohepatitis. J Biol Chem 2013, 288:18624-18642.
38. Dhar A., Dhar I., Jiang B., Desai K.M., Wu L. Chronic methylglyoxal infusion by minipump causes pancreatic beta-cell dysfunction and induces type 2 diabetes in Sprague-Dawley rats. Diabetes 2011, 60:899-908.
39. Endo M., Mori M., Akira S., Gotoh T. C/EBP homologous protein (CHOP) is crucial for the induction of caspase-11 and the pathogenesis of lipopolysaccharide-induced inflammation. J Immunol 2006, 176:6245-6253.
40. Urano F., Wang X., Bertolotti A., Zhang Y., Chung P., Harding H.P., et al. Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science (New York, NY) 2000, 287:664-666.
41. Doroudgar S., Glembotski C.C. New concepts of endoplasmic reticulum function in the heart: programmed to conserve. J Mol Cell Cardiol 2013, 55:85-91.
42. Li S.Y., Sigmon V.K., Babcock S.A., Ren J. Advanced glycation endproduct induces ROS accumulation, apoptosis, MAP kinase activation and nuclear O-GlcNAcylation in human cardiac myocytes. Life Sci 2007, 80:1051-1056.
43. Dhar I., Dhar A., Wu L., Desai K.M. Methylglyoxal, a reactive glucose metabolite, increases renin angiotensin aldosterone and blood pressure in male Sprague-Dawley rats. Am J Hypertens 2014, 27:308-316.
44. Mukohda M., Okada M., Hara Y., Yamawaki H. Exploring mechanisms of diabetes-related macrovascular complications: role of methylglyoxal, a metabolite of glucose on regulation of vascular contractility. J Pharmacol Sci 2012, 118:303-310.
45. Kolattukudy P.E., Niu J. Inflammation, endoplasmic reticulum stress, autophagy, and the monocyte chemoattractant protein-1/CCR2 pathway. Circ Res 2012, 110:174-189.
46. Wang H., Meng Q.H., Gordon J.R., Khandwala H., Wu L. Proinflammatory and proapoptotic effects of methylglyoxal on neutrophils from patients with type 2 diabetes mellitus. Clin Biochem 2007, 40:1232-1239.
47. Hwang I.S., Ho H., Hoffman B.B., Reaven G.M. Fructose-induced insulin resistance and hypertension in rats. Hypertension 1987, 10:512-516.
48. Dhar A., Desai K.M., Wu L. Alagebrium attenuates acute methylglyoxal-induced glucose intolerance in Sprague-Dawley rats. Br J Pharmacol 2010, 159:166-175.
49. Dhar A., Desai K., Kazachmov M., Yu P., Wu L. Methylglyoxal production in vascular smooth muscle cells from different metabolic precursors. Metab Clin Exp 2008, 57:1211-1220.
50. Shinohara M., Thornalley P.J., Giardino I., Beisswenger P., Thorpe S.R., Onorato J., et al. Overexpression of glyoxalase-I in bovine endothelial cells inhibits intracellular advanced glycation endproduct formation and prevents hyperglycemia-induced increases in macromolecular endocytosis. J Clin Invest 1998, 101:1142-1147.
51. Ramasamy R., Vannucci S.J., Yan S.S., Herold K., Yan S.F., Schmidt A.M. Advanced glycation end products and RAGE: a common thread in aging, diabetes, neurodegeneration, and inflammation. Glycobiology 2005, 15:16r-28r.
52. Sorci G., Riuzzi F., Agneletti A.L., Marchetti C., Donato R. S100B causes apoptosis in a myoblast cell line in a RAGE-independent manner. J Cell Physiol 2004, 199:274-283.
53. Liu R., Wu C.X., Zhou D., Yang F., Tian S., Zhang L., et al. Pinocembrin protects against beta-amyloid-induced toxicity in neurons through inhibiting receptor for advanced glycation end products (RAGE)-independent signaling pathways and regulating mitochondrion-mediated apoptosis. BMC Med 2012, 10:105.
54. Ghavami S., Kerkhoff C., Chazin W.J., Kadkhoda K., Xiao W., Zuse A., et al. S100A8/9 induces cell death via a novel, RAGE-independent pathway that involves selective release of Smac/DIABLO and Omi/HtrA2. Biochim Biophys Acta 1783, 2008:297-311.
55. Vulesevic B., Milne R.W., Suuronen E.J. Reducing methylglyoxal as a therapeutic target for diabetic heart disease. Biochem Soc Trans 2014, 42:523-527.
56. Brouwers O., Niessen P.M., Ferreira I., Miyata T., Scheffer P.G., Teerlink T., et al. Overexpression of glyoxalase-I reduces hyperglycemia-induced levels of advanced glycation end products and oxidative stress in diabetic rats. J Biol Chem 2011, 286:1374-1380.
57. Vulesevic B., McNeill B., Geoffrion M., Kuraitis D., McBane J.E., Lochhead M., et al. Glyoxalase-1 overexpression in bone marrow cells reverses defective neovascularization in STZ-induced diabetic mice. Cardiovasc Res 2014, 101:306-316.
58. Hammadi M., Oulidi A., Gackiere F., Katsogiannou M., Slomianny C., Roudbaraki M., et al. Modulation of ER stress and apoptosis by endoplasmic reticulum calcium leak via translocon during unfolded protein response: involvement of GRP78. FASEB J 2013, 27:1600-1609.
59. Orrenius S., Zhivotovsky B., Nicotera P. Regulation of cell death: the calcium-apoptosis link. Nat Rev Mol Cell Biol 2003, 4:552-565.
60. Jan C.R., Chen C.H., Wang S.C., Kuo S.Y. Effect of methylglyoxal on intracellular calcium levels and viability in renal tubular cells. Cell Signal 2005, 17:847-855.
61. Palsamy P., Bidasee K.R., Ayaki M., Augusteyn R.C., Chan J.Y., Shinohara T. Methylglyoxal induces endoplasmic reticulum stress and DNA demethylation in the Keap1 promoter of human lens epithelial cells and age-related cataracts. Free Radic Biol Med 2014, 72:134-148.
62. Higa A., Chevet E. Redox signaling loops in the unfolded protein response. Cell Signal 2012, 24:1548-1555.
63. Thornalley P.J. Protein and nucleotide damage by glyoxal and methylglyoxal in physiological systems - role in ageing and disease. Drug Metabol Drug Interact 2008, 23:125-150.
64. Bento C.F., Marques F., Fernandes R., Pereira P. Methylglyoxal alters the function and stability of critical components of the protein quality control. PLoS One 2010, 5:e13007.