Carbonylation contributes to SERCA2a activity loss and diastolic dysfunction in a rat model of type 1 diabetes

Diabetes

Volumn 60, Issue 3, 2011, Pages 947-959

  Shao, Chun Hong ^a   Capek, Haley L ^a   Patel, Kaushik P ^a   Wang, Mu ^b   Tang, Kang ^a   DeSouza, Cyrus ^c   Nagai, Ryoji ^d   Mayhan, William ^a   Periasamy, Muthu ^e   Bidasee, Keshore R ^a,f  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^d JAPAN WOMEN'S UNIVERSITY   (Japan)

^e THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

^f UNIVERSITY OF NEBRASKA LINCOLN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; INSULIN; PROTEIN SERCA2A; PYRIDOXAMINE; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; CONTROLLED STUDY; DIABETES MELLITUS; DIASTOLIC DYSFUNCTION; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME INACTIVATION; INSULIN DEPENDENT DIABETES MELLITUS; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CARBONYLATION; RAT; STREPTOZOCIN DIABETES;

ANIMALS; BLOTTING, WESTERN; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 1; DIASTOLE; HEART; MALE; MASS SPECTROMETRY; MICROSCOPY, CONFOCAL; MYOCARDIUM; PROTEIN CARBONYLATION; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY; SARCOPLASMIC RETICULUM CALCIUM-TRANSPORTING ATPASES;

EID: 79952384286     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db10-1145     Document Type: Article

References (51)

1. International Diabetes Federation. IDF diabetes atlas [article online]. Available from http://www.diabetesatlas.org/. Accessed 10 August 2010
2. Juvenile Diabetes Association. Fact sheet type 1 diabetes [article online]. Available from http://www.jdrf.org/index.cfm?page-id5102585. Accessed 20 January 2011
3. Park J-W, Ziegler AG, Janka HU, Doering W, Mehnert H. Left ventricular relaxation and filling pattern in diabetic heart muscle disease: an echocardiographic study. Klin Wochenschr 1988;66:773-778
4. Ruddy TD, Shumak SL, Liu PP, et al. The relationship of cardiac diastolic dysfunction to concurrent hormonal and metabolic status in type I diabetes mellitus. J Clin Endocrinol Metab 1988;66:113-118 (Pubitemid 18027738)
5. Koltin D, Daneman D. Dead-in-bed syndrome: a diabetes nightmare. Pediatr Diabetes 2008;9:504-507
6. Penpargkul S, Fein F, Sonnenblick EH, Scheuer J. Depressed cardiac sarcoplasmic reticular function from diabetic rats. J Mol Cell Cardiol 1981; 13:303-309 (Pubitemid 11155567)
7. Choi KM, Zhong Y, Hoit BD, et al. Defective intracellular Ca(2+) signaling contributes to cardiomyopathy in type 1 diabetic rats. Am J Physiol Heart Circ Physiol 2002;283:H1398-H1408
8. Clark RJ, McDonough PM, Swanson E, et al. Diabetes and the accompanying hyperglycemia impairs cardiomyocyte calcium cycling through increased nuclear O-GlcNAcylation. J Biol Chem 2003;278:44230-44237 (Pubitemid 37377167)
9. Machackova J, Barta J, Dhalla NS. Molecular defects in cardiac myofibrillar proteins due to thyroid hormone imbalance and diabetes. Can J Physiol Pharmacol 2005;83:1071-1091
10. Kahaly GJ, Dillmann WH. Thyroid hormone action in the heart. Endocr Rev 2005;26:704-728 (Pubitemid 41127279)
11. Kim HW, Ch YS, Lee HR, Park SY, Kim YH. Diabetic alterations in cardiac sarcoplasmic reticulum Ca2+-ATPase and phospholamban protein expression. Life Sci 2001;70:367-379 (Pubitemid 34017533)
12. Rastogi S, Sentex E, Elimban V, Dhalla NS, Netticadan T. Elevated levels of protein phosphatase 1 and phosphatase 2A may contribute to cardiac dysfunction in diabetes. Biochim Biophys Acta 2003;1638:273-277 (Pubitemid 37288966)
13. Zhong Y, Ahmed S, Grupp IL, Matlib MA. Altered SR protein expression associated with contractile dysfunction in diabetic rat hearts. Am J Physiol Heart Circ Physiol 2001;281:H1137-H1147
14. Tschöpe C, Spillmann F, Rehfeld U, et al. Improvement of defective sarcoplasmic reticulum Ca2+ transport in diabetic heart of transgenic rats expressing the human kallikrein-1 gene. FASEB J 2004;18:1967-1969 (Pubitemid 39602300)
15. Zhao XY, Hu SJ, Li J, Mou Y, Chen BP, Xia Q. Decreased cardiac sarcoplasmic reticulum Ca2+-ATPase activity contributes to cardiac dysfunction in streptozotocin-induced diabetic rats. J Physiol Biochem 2006;62:1-8 (Pubitemid 44102814)
16. Ligeti L, Szenczi O, Prestia CM, et al. Altered calcium handling is an early sign of streptozotocin-induced diabetic cardiomyopathy. Int J Mol Med 2006;17:1035-1043
17. Shao CH, Wehrens XH, Wyatt TA, et al. Exercise training during diabetes attenuates cardiac ryanodine receptor dysregulation. J Appl Physiol 2009; 106:1280-1292
18. Brownlee M, Cerami A, Vlassara H. Advanced glycosylation end products in tissue and the biochemical basis of diabetic complications. N Engl J Med 1988;318:1315-1321
19. Brownlee M. Biochemistry and molecular cell biology of diabetic complications. Nature 2001;414:813-820 (Pubitemid 34000785)
20. Deng Y, Yu PH. Simultaneous determination of formaldehyde and methylglyoxal in urine: involvement of semicarbazide-sensitive amine oxidasemediated deamination in diabetic complications. J Chromatogr Sci 1999; 37:317-322 (Pubitemid 129697312)
21. Hayes BE, Clarke DE. Elevation of serum benzylamine oxidase activity in diabetic rats. Proc West Pharmacol Soc 1983;26:119-122 (Pubitemid 13047206)
22. Stadtman ER. Protein oxidation and aging. Science 1992;257:1220-1224
23. Uchida K. Role of reactive aldehyde in cardiovascular diseases. Free Radic Biol Med 2000;28:1685-1696 (Pubitemid 30628655)
24. 2+-ATPase. Diabetes 2004;53:463-473
25. National Research Council. Guide for the Care and Use of Laboratory Animals. Washington, DC, National Academy Press, 1996
26. Voziyan PA, Hudson BG. Pyridoxamine: the many virtues of a maillard reaction inhibitor. Ann N Y Acad Sci 2005;1043:807-816 (Pubitemid 41123975)
27. Nagaraj RH, Sarkar P, Mally A, Biemel KM, Lederer MO, Padayatti PS. Effect of pyridoxamine on chemical modification of proteins by carbonyls in diabetic rats: characterization of a major product from the reaction of pyridoxamine and methylglyoxal. Arch Biochem Biophys 2002;402:110-119 (Pubitemid 34848300)
28. Shao CH, Rozanski GJ, Nagai R, et al. Carbonylation of myosin heavy chains in rat heart during diabetes. Biochem Pharmacol 2010;80:205-217
29. Thornalley PJ, Hooper NI, Jennings PE, et al. The human red blood cell glyoxalase system in diabetes mellitus. Diabetes Res Clin Pract 1989;7:115-120 (Pubitemid 19221706)
30. Andersen JP. Dissection of the functional domains of the sarcoplasmic reticulum Ca(2+)-ATPase by site-directed mutagenesis. Biosci Rep 1995; 15:243-261
31. Andersen JP. Functional consequences of alterations to amino acids at the M5S5 boundary of the Ca(2+)-ATPase of sarcoplasmic reticulum. Mutation Tyr763->.Gly uncouples ATP hydrolysis from Ca2+ transport. J Biol Chem 1995;270:908-914
32. Zhang Y, Cocklin RR, Bidasee KR, Wang M. Rapid determination of advanced glycation end products of proteins using MALDI-TOF-MS and PERL script peptide searching algorithm. J Biomol Tech 2003;14:224-230
33. Toyoshima C, Nomura H. Structural changes in the calcium pump accompanying the dissociation of calcium. Nature 2002;418:605-611
34. Toyoshima C, Nomura H, Tsuda T. Lumenal gating mechanism revealed in calcium pump crystal structures with phosphate analogues. Nature 2004; 432:361-368 (Pubitemid 39555518)
35. Yim HS, Kang SO, Hah YC, Chock PB, Yim MB. Free radicals generated during the glycation reaction of amino acids by methylglyoxal: a model study of protein-cross-linked free radicals. J Biol Chem 1995;270:28228-28233
36. Dode L, Andersen JP, Leslie N, Dhitavat J, Vilsen B, Hovnanian A. Dissection of the functional differences between sarco(endo)plasmic reticulum Ca2+-ATPase (SERCA) 1 and 2 isoforms and characterization of Darier disease (SERCA2) mutants by steady-state and transient kinetic analyses. J Biol Chem 2003;278:47877-47889 (Pubitemid 37523236)
37. Lapolla A, Flamini R, Dalla Vedova A, et al. Glyoxal and methylglyoxal levels in diabetic patients: quantitative determination by a new GC/MS method. Clin Chem Lab Med 2003;41:1166-1173 (Pubitemid 37265695)
38. Williams ME, Bolton WK, Khalifah RG, Degenhardt TP, Schotzinger RJ, McGill JB. Effects of pyridoxamine in combined phase 2 studies of patients with type 1 and type 2 diabetes and overt nephropathy. Am J Nephrol 2007; 27:605-614 (Pubitemid 350014947)
39. Adachi T, Weisbrod RM, Pimentel DR, et al. S-Glutathiolation by peroxynitrite activates SERCA during arterial relaxation by nitric oxide. Nat Med 2004;10:1200-1207 (Pubitemid 39540436)
40. Clausen JD, McIntosh DB, Vilsen B, Woolley DG, Andersen JP. Importance of conserved N-domain residues Thr441, Glu442, Lys515, Arg560, and Leu562 of sarcoplasmic reticulum Ca2+-ATPase for MgATP binding and subsequent catalytic steps: plasticity of the nucleotide-binding site. J Biol Chem 2003;278:20245-20258 (Pubitemid 36799223)
41. Marks AR, Priori S, Memmi M, Kontula K, Laitinen PJ. Involvement of the cardiac ryanodine receptor/calcium release channel in catecholaminergic polymorphic ventricular tachycardia. J Cell Physiol 2002;190:1-6
42. Terentyev D, Viatchenko-Karpinski S, Györke I, Volpe P, Williams SC, Györke S. Calsequestrin determines the functional size and stability of cardiac intracellular calcium stores: Mechanism for hereditary arrhythmia. Proc Natl Acad Sci USA 2003;100:11759-11764 (Pubitemid 37206008)
43. Ferrington DA, Krainev AG, Bigelow DJ. Altered turnover of calcium regulatory proteins of the sarcoplasmic reticulum in aged skeletal muscle. J Biol Chem 1998;273:5885-5891 (Pubitemid 28124067)
44. Dunkel P, Gelain A, Barlocco D, et al. Semicarbazide-sensitive amine oxidase/vascular adhesion protein 1: recent developments concerning substrates and inhibitors of a promising therapeutic target. Curr Med Chem 2008;15:1827-1839
45. Penckofer S, Schwertz D, Florczak K. Oxidative stress and cardiovascular disease in type 2 diabetes: the role of antioxidants and pro-oxidants. J Cardiovasc Nurs 2002;16:68-85
46. Kilhovd BK, Berg TJ, Birkeland KI, Thorsby P, Hanssen KF. Serum levels of advanced glycation end products are increased in patients with type 2 diabetes and coronary heart disease. Diabetes Care 1999;22:1543-1548 (Pubitemid 29418253)
47. Schalkwijk CG, Baidoshvili A, Stehouwer CD, van Hinsbergh VW, Niessen HW. Increased accumulation of the glycoxidation product Nepsilon-(carboxymethyl) lysine in hearts of diabetic patients: generation and characterisation of a monoclonal anti-CML antibody. Biochim Biophys Acta 2004;1636:82-89 (Pubitemid 38780784)
48. Koyama Y, Takeishi Y, Arimoto T, et al. High serum level of pentosidine, an advanced glycation end product (AGE), is a risk factor of patients with heart failure. J Card Fail 2007;13:199-206 (Pubitemid 46590033)
49. Boomsma F, van Veldhuisen DJ, de Kam PJ, et al. Plasma semicarbazidesensitive amine oxidase is elevated in patients with congestive heart failure. Cardiovasc Res 1997;33:387-391 (Pubitemid 27072644)
50. Miyata T, Inagi R, Kurokawa K. Diagnosis, pathogenesis, and treatment of dialysis-related amyloidosis. Miner Electrolyte Metab 1999;25:114-117 (Pubitemid 29196646)
51. Karakikes I, Kim M, Hadri L, et al. Gene remodeling in type 2 diabetic cardiomyopathy and its phenotypic rescue with SERCA2a. PLoS ONE 2009;4:e6474