Enhanced cardiac protein glycosylation (O-GlcNAc) of selected mitochondrial proteins in rats artificially selected for low running capacity

Physiological Genomics

Volumn 45, Issue 1, 2013, Pages 17-25

  Johnsen, Virginia L ^a   Belke, Darrell D ^a   Hughey, Curtis C ^a   Hittel, Dustin S ^a   Hepple, Russell T ^a,b   Koch, Lauren G ^c   Britton, Steven L ^c,d   Shearer, Jane ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^d NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

Author keywords

Aerobic capacity; Clamp; Insulin resistance; Metabolism; Mitochondrial dysfunction; Type 2 diabetes

Indexed keywords

BETA N ACETYL GLUCOSAMINE; HORMONE; MITOCHONDRIAL PROTEIN; N ACETYLGLUCOSAMINE; THREONINE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EXERCISE; GLUCOSE METABOLISM; HYPERINSULINEMIA; INSULIN SENSITIVITY; MALE; NONHUMAN; NUTRIENT; PRIORITY JOURNAL; PROTEIN GLYCOSYLATION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; RAT; RUNNING; STRESS;

ABSORPTIOMETRY, PHOTON; ANALYSIS OF VARIANCE; ANIMALS; CARBON RADIOISOTOPES; CITRATE (SI)-SYNTHASE; FATTY ACIDS, NONESTERIFIED; GLUCOSE; GLUCOSE CLAMP TECHNIQUE; GLYCOSYLATION; IMMUNOBLOTTING; INSULIN RESISTANCE; KINETICS; MITOCHONDRIAL PROTEINS; MODELS, ANIMAL; MYOCARDIUM; N-ACETYLGLUCOSAMINYLTRANSFERASES; OXIDATIVE PHOSPHORYLATION; RATS; RATS, INBRED STRAINS; RUNNING;

ANIMALIA; RATTUS;

EID: 84872202540     PISSN: 10948341     EISSN: 15312267     Source Type: Journal    
DOI: 10.1152/physiolgenomics.00111.2012     Document Type: Article

References (58)

1. Anderwald C, Tura A, Grassi A, Krebs M, Szendroedi J, Roden M, Bischof MG, Luger A, Pacini G. Insulin infusion during normoglycemia modulates insulin secretion according to whole-body insulin sensitivity. Diabet Care 34: 437-441, 2011.
2. Andres-Bergos J, Tardio L, Larranaga-Vera A, Gomez R, Herrero-Beaumont G, Largo R. The increase in o-linked N-acetylglucosamine protein modification stimulates chondrogenic differentiation both in vitro and in vivo. J Biol Chem 287: 33615-33628, 2012.
3. Arias EB, Kim J, Cartee GD. Prolonged incubation in PUGNAc results in increased protein O-Linked glycosylation and insulin resistance in rat skeletal muscle. Diabetes 53: 921-930, 2004.
4. Armstrong RB, Phelps RO. Muscle fiber type composition of the rat hindlimb. Am J Anat 171: 259-272, 1984.
5. Belke DD. Swim-exercised mice show a decreased level of protein O-GlcNAcylation and expression of O-GlcNAc transferase in heart. J Appl Physiol 111: 157-162, 2011.
6. Bennett CE, Johnsen VL, Shearer J, Belke DD. Exercise training mitigates aberrant cardiac protein O-GlcNAcylation in streptozotocininduced diabetic mice. Life Sci [Epub ahead of print].
7. Brownlee M. Biochemistry and molecular cell biology of diabetic complications. Nature 414: 813-820, 2001.
8. Burniston JG, Kenyani J, Wastling JM, Burant CF, Qi NR, Koch LG, Britton SL. Proteomic analysis reveals perturbed energy metabolism and elevated oxidative stress in hearts of rats with inborn low aerobic capacity. Proteomics 11: 3369-3379, 2011.
9. Champattanachai V, Marchase RB, Chatham JC. Glucosamine protects neonatal cardiomyocytes from ischemia-reperfusion injury via increased protein-associated O-GlcNAc. Am J Physiol Cell Physiol 292: C178-C187, 2007.
10. Darley-Usmar VM, Ball LE, Chatham JC. Protein O-linked beta-Nacetylglucosamine: a novel effector of cardiomyocyte metabolism and function. J Mol Cell Cardiol 52: 538-1049, 2012.
11. DeMarco VG, Johnson MS, Ma L, Pulakat L, Mugerfeld I, Hayden MR, Garro M, Knight W, Britton SL, Koch LG, Sowers JR. Overweight female rats selectively breed for low aerobic capacity exhibit increased myocardial fibrosis and diastolic dysfunction. Am J Physiol Heart Circ Physiol 302: H1667-H1682, 2012.
12. Dias WB, Hart GW. O-GlcNAc modification in diabetes and Alzheimer's disease. Mol BioSyst 3: 766-772, 2007.
13. Du XL, Edelstein D, Rossetti L, Fantus IG, Goldberg H, Ziyadeh F, Wu J, Brownlee M. Hyperglycemia-induced mitochondrial superoxide overproduction activates the hexosamine pathway and induces plasminogen activator inhibitor-1 expression by increasing Sp1 glycosylation. Proc Natl Acad Sci USA 97: 12222-12226, 2000.
14. Fricovsky ES, Suarez J, Ihm SH, Scott BT, Suarez-Ramirez JA, Banerjee I, Torres-Gonzalez M, Wang H, Ellrott I, Maya-Ramos L, Villarreal FJ, Dillmann WH. Excess protein O-GlcNAcylation and the progression of diabetic cardiomyopathy. Am J Physiol Regul Integr Comp Physiol 303: R689-R699, 2012.
15. Fulop N, Feng W, Xing D, He K, Not LG, Brocks CA, Marchase RB, Miller AP, Chatham JC. Aging leads to increased levels of protein O-linked N-acetylglucosamine in heart, aorta, brain and skeletal muscle in Brown-Norway rats. Biogerontology 9: 139-151, 2008.
16. Gu Y, Ande SR, Mishra S. Altered O-GlcNAc modification and phosphorylation of mitochondrial proteins in myoblast cells exposed to high glucose. Arch Biochem Biophys 505: 98-104, 2011.
17. Hart GW, Housley MP, Slawson C. Cycling of O-linked beta-Nacetylglucosamine on nucleocytoplasmic proteins. Nature 446: 1017-1022, 2007.
18. Hart GW, Slawson C, Ramirez-Correa G, Lagerlof O. Cross talk between O-GlcNAcylation and phosphorylation: roles in signaling, transcription, and chronic disease. Annu Rev Biochem 80: 825-858, 2011.
19. Hawley JA, Spargo FJ. It's all in the genes, so pick your parents wisely. J Appl Physiol 100: 1751-1752, 2006.
20. Howlett RA, Gonzalez NC, Wagner HE, Fu Z, Britton SL, Koch LG, Wagner PD. Selected contribution: skeletal muscle capillarity and enzyme activity in rats selectively bred for running endurance. J Appl Physiol 94: 1682-1688, 2003.
21. Hu Y, Belke D, Suarez J, Swanson E, Clark R, Hoshijima M, Dillmann WH. Adenovirus-mediated overexpression of O-GlcNAcase improves contractile function in the diabetic heart. Circ Res 96: 1006-1013, 2005.
22. Hu Y, Suarez J, Fricovsky E, Wang H, Scott BT, Trauger SA, Han W, Hu Y, Oyeleye MO, Dillmann WH. Increased enzymatic O-GlcNAcylation of mitochondrial proteins impairs mitochondrial function in cardiac myocytes exposed to high glucose. J Biol Chem 284: 547-555, 2009.
23. Hughey CC, Hittel DS, Johnsen VL, Shearer J. Hyperinsulinemiceuglycemic clamp in the conscious rat. J Vis Exp: e2432, 2011.
24. Issad T, Kuo M. O-GlcNAc modification of transcription factors, glucose sensing and glucotoxicity. Trends Endocrinol Metab 19: 380-389, 2008.
25. Issad T, Masson E, Pagesy P. O-GlcNAc modification, insulin signaling and diabetic complications. Diabetes Metab 36: 423-435, 2010.
26. Jones SP, Zachara NE, Ngoh GA, Hill BG, Teshima Y, Bhatnagar A, Hart GW, Marban E. Cardioprotection by N-acetylglucosamine linkage to cellular proteins. Circulation 117: 1172-1182, 2008.
27. Kivela R, Silvennoinen M, Lehti M, Rinnankoski-Tuikka R, Purhonen T, Ketola T, Pullinen K, Vuento M, Mutanen N, Sartor MA, Reunanen H, Koch LG, Britton SL, Kainulainen H. Gene expression centroids that link with low intrinsic aerobic exercise capacity and complex disease risk. FASEB J 24: 4565-4574, 2010.
28. Koch LG, Britton SL. Artificial selection for intrinsic aerobic endurance running capacity in rats. Physiol Genomics 5: 45-52, 2001.
29. Koch LG, Britton SL, Wisloff U. A rat model system to study complex disease risks, fitness, aging, and longevity. Trends Cardiovasc Med 22: 29-34, 2012.
30. Kullo IJ, Hensrud DD, Allison TG. Relation of low cardiorespiratory fitness to the metabolic syndrome in middle-aged men. Am J Cardiol 90: 795-797, 2002.
31. Laczy B, Hill BG, Wang K, Paterson AJ, White CR, Xing D, Chen YF, Darley-Usmar V, Oparil S, Chatham JC. Protein O-GlcNAcylation: a new signaling paradigm for the cardiovascular system. Am J Physiol Heart Circ Physiol 296: H13-H28, 2009.
32. Lessard SJ, Rivas DA, Chen ZP, van Denderen BJ, Watt MJ, Koch LG, Britton SL, Kemp BE, Hawley JA. Impaired skeletal muscle beta-adrenergic activation and lipolysis are associated with whole-body insulin resistance in rats bred for low intrinsic exercise capacity. Endocrinology 150: 4883-4891, 2009.
33. Love DC, Krause MW, Hanover JA. O-GlcNAc cycling: emerging roles in development and epigenetics. Sem Cell Dev Biol 21: 646-654, 2010.
34. Lowell BB, Shulman GI. Mitochondrial dysfunction and type 2 diabetes. Science 307: 384-387, 2005.
35. Marsh SA, Chatham JC. The paradoxical world of protein O-GlcNAcylation: a novel effector of cardiovascular (dys)function. Cardiovasc Res 89: 487-488, 2011.
36. Ngoh GA, Facundo HT, Zafir A, Jones SP. O-GlcNAc signaling in the cardiovascular system. Circ Res 107: 171-185, 2010.
37. Noland RC, Thyfault JP, Henes ST, Whitfield BR, Woodlief TL, Evans JR, Lust JA, Britton SL, Koch LG, Dudek RW, Dohm GL, Cortright RN, Lust RM. Artificial selection for high-capacity endurance running is protective against high-fat diet-induced insulin resistance. Am J Physiol Endocrinol Metab 293: E31-E41, 2007.
38. Patti ME, Corvera S. The role of mitochondria in the pathogenesis of type 2 diabetes. Endocr Rev 31: 364-395, 2010.
39. Petersen HA, Fueger PT, Bracy DP, Wasserman DH, Halseth AE. Fiber type-specific determinants of Vmax for insulin-stimulated muscle glucose uptake in vivo. Am J Physiol Endocrinol Metab 284: E541-E548, 2003.
40. Petersen KF, Befroy D, Dufour S, Dziura J, Ariyan C, Rothman DL, DiPietro L, Cline GW, Shulman GI. Mitochondrial dysfunction in the elderly: possible role in insulin resistance. Science 300: 1140-1142, 2003.
41. Roquemore EP, Chou TY, Hart GW. Detection of O-linked N-acetylglucosamine (O-GlcNAc) on cytoplasmic and nuclear proteins. Methods Enzymol 230: 443-460, 1994.
42. Schwarzer M, Britton SL, Koch LG, Wisloff U, Doenst T. Low intrinsic aerobic exercise capacity and systemic insulin resistance are not associated with changes in myocardial substrate oxidation or insulin sensitivity. Basic Res Cardiol 105: 357-364, 2010.
43. Sena S, Hu P, Zhang D, Wang X, Wayment B, Olsen C, Avelar E, Abel ED, Litwin SE. Impaired insulin signaling accelerates cardiac mitochondrial dysfunction after myocardial infarction. J Mol Cell Cardiol 46: 910-918, 2009.
44. Shearer J, Fueger PT, Bracy DP, Wasserman DH, Rottman JN. Partial gene deletion of heart-type fatty acid-binding protein limits the severity of dietary-induced insulin resistance. Diabetes 54: 3133-3139, 2005.
45. Shearer J, Fueger PT, Rottman JN, Bracy DP, Binas B, Wasserman DH. Heart-type fatty acid-binding protein reciprocally regulates glucose and fatty acid utilization during exercise. Am J Physiol Endocrinol Metab 288: E292-E297, 2005.
46. Slawson C, Copeland RJ, Hart GW. O-GlcNAc signaling: a metabolic link between diabetes and cancer? Trends Biochem Sci 35: 547-555, 2010.
47. Stabelini Neto A, Sasaki JE, Mascarenhas LP, Boguszewski MC, Bozza R, Ulbrich AZ, da Silva SG, de Campos W. Physical activity, cardiorespiratory fitness, and metabolic syndrome in adolescents: a crosssectional study. BMC Publ Health 11: 674, 2011.
48. Swallow JG, Wroblewska AK, Waters RP, Renner KJ, Britton SL, Koch LG. Phenotypic and evolutionary plasticity of body composition in rats selectively bred for high endurance capacity. J Appl Physiol 109: 778-785, 2010.
49. Tweedie C, Romestaing C, Burelle Y, Safdar A, Tarnopolsky MA, Seadon S, Britton SL, Koch LG, Hepple RT. Lower oxidative DNA damage despite greater ROS production in muscles from rats selectively bred for high running capacity. Am J Physiol Regul Integr Comp Physiol 300: R544-R553, 2011.
50. Vosseller K. O-GlcNAc and aging: C. elegans as a genetic model to test O-GlcNAc roles in type II diabetic insulin resistance. Aging (Albany NY) 2: 749-751, 2010.
51. Walsh B, Hooks RB, Hornyak JE, Koch LG, Britton SL, Hogan MC. Enhanced mitochondrial sensitivity to creatine in rats bred for high aerobic capacity. J Appl Physiol 100: 1765-1769, 2006.
52. Watson LJ, Facundo HT, Ngoh GA, Ameen M, Brainard RE, Lemma KM, Long BW, Prabhu SD, Xuan YT, Jones SP. O-linked beta-Nacetylglucosamine transferase is indispensable in the failing heart. Proc Natl Acad Sci USA 107: 17797-17802, 2010.
53. Wisloff U, Najjar SM, Ellingsen O, Haram PM, Swoap S, Al-Share Q, Fernstrom M, Rezaei K, Lee SJ, Koch LG, Britton SL. Cardiovascular risk factors emerge after artificial selection for low aerobic capacity. Science 307: 418-420, 2005.
54. Wolfe RR. Radioactive and Stable Isotope Tracers in Biomedicine: Principles and Practice of Kinetic Analysis. New York: Wiley-Liss, 1992.
55. Zachara NE. The roles of O-linked beta-N-acetylglucosamine in cardiovascular physiology and disease. Am J Physiol Heart Circ Physiol 302: H1905-H1918, 2012.
56. Zachara NE, Hart GW. Cell signaling, the essential role of O-GlcNAc! Biochim Biophys Acta 1761: 599-617, 2006.
57. Zachara NE, Molina H, Wong KY, Pandey A, Hart GW. The dynamic stress-induced "O-GlcNAc-ome" highlights functions for O-GlcNAc in regulating DNA damage/repair and other cellular pathways. Amino Acids 40: 793-808, 2011.
58. Zachara NE, O'Donnell N, Cheung WD, Mercer JJ, Marth JD, Hart GW. Dynamic O-GlcNAc modification of nucleocytoplasmic proteins in response to stress. A survival response of mammalian cells. J Biol Chem 279: 30133-30142, 2004.