Exercise training enhanced myocardial endothelial nitric oxide synthase (eNOS) function in diabetic Goto-Kakizaki (GK) rats

Cardiovascular Diabetology

Volumn 7, Issue , 2008, Pages

  Grijalva, James ^a   Hicks, Steven ^a   Zhao, Xiangmin ^a   Medikayala, Sushma ^a   Kaminski, Pawel M ^a   Wolin, Michael S ^a   Edwards, John G ^a  

^a NEW YORK MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME C OXIDASE; DIMER; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GLYCOSYLATED HEMOGLOBIN; HEMOGLOBIN; MONOMER; NITRIC OXIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; SUPEROXIDE; TETRAHYDROBIOPTERIN; 5,6,7,8-TETRAHYDROBIOPTERIN; BIOPTERIN; DRUG DERIVATIVE; MESSENGER RNA; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIMERIZATION; ENZYME ACTIVITY; ENZYME GLYCOSYLATION; ENZYME SYNTHESIS; EXERCISE; GOTO KAKIZAKI RAT; HEART LEFT VENTRICLE; HEART MUSCLE; INSULIN SENSITIVITY; MALE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PLANTARIS MUSCLE; PROTEIN EXPRESSION; RAT; RUNNING; SITTING; ANIMAL; DISEASE MODEL; ENZYMOLOGY; METABOLISM; PHYSIOLOGY; RAT STRAIN;

ANIMALS; BIOPTERIN; DIABETES MELLITUS, TYPE 2; DISEASE MODELS, ANIMAL; MALE; MYOCARDIUM; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; PHYSICAL CONDITIONING, ANIMAL; RATS; RATS, INBRED STRAINS; REACTIVE OXYGEN SPECIES; RNA, MESSENGER; SUPEROXIDES;

EID: 58049140295     PISSN: None     EISSN: 14752840     Source Type: Journal    
DOI: 10.1186/1475-2840-7-34     Document Type: Article

References (63)

1. Walker K Jones J Piers L O'Dea K Putt R Effects of regular walking on cardiovascular risk factors and body composition in normoglycemic women and women with type 2 diabetes Diabetes Care 1999, 22:555-561. 10.2337/ diacare.22.4.555 10189531
2. Boule NG Kenny GP Haddad E Wells GA Sigal RJ Meta-analysis of the effect of structured exercise training on cardiorespiratory fitness in Type 2 diabetes mellitus Diabetologia 2003. 12856082
3. Laughlin MH Endothelium-mediated control of coronary vascular tone after chronic exercise training Med Sci Sports Exerc 1995, 27:1135-44. 7476057
4. Delp MD Effects of exercise training on endothelium-dependent peripheral vascular responsiveness Med Sci Sports Exerc 1995, 27:1152-7. 7476059
5. Sessa WC Pritchard K Seyedi N Wang J Hintze TH Chronic exercise in dogs increases coronary vascular nitric oxide production and endothelial cell nitric oxide synthase gene expression Circ Res 1994, 74:349-53. 7507417
6. Johnson LR Rush JW Turk JR Price EM Laughlin MH Short-term exercise training increases ACh-induced relaxation and eNOS protein in porcine pulmonary arteries J Appl Physiol 2001, 90:1102-10. 10.1063/1.1383260 11181626
7. Sun D Huang A Koller A Kaley G Adaptation of flow-induced dilation of arterioles to daily exercise Microvasc Res 1998, 56:54-61. 10.1006/ mvre.1998.2083 9683563
8. Xiao Z Xhang Z Diamond SL Shear Stress Induction of the Endothelial Nitric Oxide Synthase Gene is Calcium-Dependent But Not Calcium-Activated Jour of Cell Phys 1997, 171:205-211. 10.1002/ (SICI)1097-4652(199705)171:2<205::AID-JCP11>3.0.CO;2-C
9. Ziegler T Silacci P Harrison V Hayoz D Nitric oxide synthase expression in endothelial cells exposed to mechanical forces Hypertension 1998, 32(2):351-355. 9719066
10. Minami A Ishimura N Harada N Sakamoto S Niwa Y Nakaya Y Exercise training improves acetylcholine-induced endothelium-dependent hyperpolarization in type 2 diabetic rats, Otsuka Long-Evans Tokushima fatty rats Atherosclerosis 2002, 162:85-92. 10.1016/ S0021-9150(01)00685-2 11947901
11. Hamdy O Ledbury S Mullooly C Jarema C Porter S Ovalle K et al Lifestyle modification improves endothelial function in obese subjects with the insulin resistance syndrome Diabetes Care 2003, 26:2119-25. 10.2337/ diacare.26.7.2119 12832323
12. Radomski MW Palmer RM Moncada S The anti-aggregating properties of vascular endothelium: Interactions between prostacyclin and nitric oxide Br J Pharmacol 1987, 92:639-46. 1853691 3322462
13. Recchia FA Osorio JC Chandler MP Xu X Panchal AR Lopaschuk GD et al Reduced synthesis of NO causes marked alterations in myocardial substrate metabolism in conscious dogs Am J Physiol Endocrinol Metab 2002, 282:E197-206. 11739101
14. Alderton WK Cooper CE Knowles RG Nitric oxide synthases: Structure, function and inhibition Biochem J 2001, 357:593-615. 1221991 11463332 10.1042/0264-6021:3570593
15. Zou MH Shi C Cohen RA Oxidation of the zinc-thiolate complex and uncoupling of endothelial nitric oxide synthase by peroxynitrite J Clin Invest 2002, 109:817-26. 150913 11901190
16. Balligand JL Cannon PJ Nitric oxide synthases and cardiac muscle. Autocrine and paracrine influences Arterioscler Thromb Vasc Biol 1997, 17:1846-58. 9351345
17. Zhang QJ Li QX Zhang HF Zhang KR Guo WY Wang HC et al Swim training sensitizes myocardial response to insulin: Role of Akt-dependent eNOS activation Cardiovasc Res 2007, 75:369-80. 10.1016/ j.cardiores.2007.04.015 17537411
18. Zhao G Zhang X Smith CJ Xu X Ochoa M Greenhouse D et al Reduced coronary NO production in conscious dogs after the development of alloxan-induced diabetes Am J Physiol 1999, 277:H268-78. 10409206
19. Rabini RA Staffolani R Fumelli P Mutus B Curatola G Mazzanti L Decreased nitric oxide synthase activity in platelets from IDDM and NIDDM patients Diabetologia 1998, 41:101-4. 10.1007/s001250050873 9498637
20. Martina V Bruno GA Trucco F Zumpano E Tagliabue M Di Bisceglie C et al Platelet cNOS activity is reduced in patients with IDDM and NIDDM Thromb Haemost 1998, 79:520-2. 9531033
21. Rafalski K Abdourahman A Edwards JG Early adaptations to training: upregulation of alpha-myosin heavy chain gene expression Med Sci Sports Exerc 2007, 39:75-82. 10.1249/01.mss.0000240324.08406.3d 17218887
22. Misko TP Schilling RJ Salvemini D Moore WM Currie MG A fluorometric assay for the measurement of nitrite in biological samples Anal Biochem 1993, 214:11-6. 10.1006/abio.1993.1449 7504409
23. Ungvari Z Csiszar A Edwards JG Kaminski PM Wolin MS Kaley G et al Increased superoxide production in coronary arteries in hyperhomocysteinemia: Role of tumor necrosis factor-alpha, NAD(P)H oxidase, and inducible nitric oxide synthase Arterioscler Thromb Vasc Biol 2003, 23:418-24. 10.1161/01.ATV.0000061735.85377.40 12615666
24. Zhao H Kalivendi S Zhang H Joseph J Nithipatikom K Vasquez-Vivar J et al Superoxide reacts with hydroethidine but forms a fluorescent product that is distinctly different from ethidium: Potential implications in intracellular fluorescence detection of superoxide Free Radic Biol Med 2003, 34:1359-68. 10.1016/S0891-5849(03)00142-4 12757846
25. Matsuda M DeFronzo RA Insulin sensitivity indices obtained from oral glucose tolerance testing: Comparison with the euglycemic insulin clamp Diabetes Care 1999, 22:1462-70. 10.2337/diacare.22.9.1462 10480510
26. Witte K Jacke K Stahrenberg R Arlt G Reitenbach I Schilling L Dysfunction of soluble guanylyl cyclase in aorta and kidney of Goto-Kakizaki rats: Influence of age and diabetic state Nitric Oxide 2002, 6:85-95. 10.1006/niox.2001.0363 11829539
27. Oliveira PJ Rolo AP Seica R Sardao V Monteiro P Goncalves L Impact of diabetes on induction of the mitochondrial permeability transition Rev Port Cardiol 2002, 21:759-66. 12194377
28. Murakawa Y Zhang W Pierson CR Brismar T Ostenson CG Efendic S et al Impaired glucose tolerance and insulinopenia in the GK-rat causes peripheral neuropathy Diabetes Metab Res Rev 2002, 18:473-83. 10.1002/ dmrr.326 12469361
29. Phillips AO Baboolal K Riley S Grone H Janssen U Steadman R Association of prolonged hyperglycemia with glomerular hypertrophy and renal basement membrane thickening in the Goto Kakizaki model of non-insulin-dependent diabetes mellitus Am J Kidney Dis 2001, 37:400-10. 10.1053/ajkd.2001.21322 11157383
30. Kobayashi T Matsumoto T Ooishi K Kamata K Differential expression of alpha2D-adrenoceptor and eNOS in aortas from early and later stages of diabetes in Goto-Kakizaki rats Am J Physiol Heart Circ Physiol 2004, 287:H135-48. 10.1152/ajpheart.01074.2003 15130881
31. Cheng ZJ Vaskonen T Tikkanen I Nurminen K Ruskoaho H Vapaatalo H et al Endothelial dysfunction and salt-sensitive hypertension in spontaneously diabetic Goto-Kakizaki rats Hypertension 2001, 37:433-9. 11230314
32. Santos DL Palmeira CM Seica R Dias J Mesquita J Moreno AJ et al Diabetes and mitochondrial oxidative stress: A study using heart mitochondria from the diabetic Goto-Kakizaki rat Mol Cell Biochem 2003, 246:163-70. 10.1023/A:1023475022025 12841358
33. Woodman CR Muller JM Laughlin MH Price M Induction of nitric oxide synthase mRNA in coronary resistance arteries isolated from exercise-trained pigs Am J Physiol 1997, 273:H2575-9. 9435589
34. Lin MI Fulton D Babbitt R Fleming I Busse R Pritchard KA Jr et al Phosphorylation of threonine 497 in endothelial nitric-oxide synthase coordinates the coupling of L-arginine metabolism to efficient nitric oxide production J Biol Chem 2003, 278:44719-26. 10.1074/jbc.M302836200 12952971
35. Fulton D Fontana J Sowa G Gratton JP Lin M Li KX et al Localization of endothelial nitric-oxide synthase phosphorylated on serine 1179 and nitric oxide in Golgi and plasma membrane defines the existence of two pools of active enzyme J Biol Chem 2002, 277:4277-84. 10.1074/ jbc.M106302200 11729179
36. Robinson LJ Busconi L Michel T Agonist-modulated palmitoylation of endothelial nitric oxide synthase J Biol Chem 1995, 270:995-8. 10.1074/ jbc.270.46.27403 7530714
37. Shaul PW Smart EJ Robinson LJ German Z Yuhanna IS Ying Y et al Acylation targets emdothelial nitric-oxide synthase to plasmalemmal caveolae J Biol Chem 1996, 271:6518-22. 10.1074/jbc.271.11.6518 8626455
38. Gonzalez E Kou R Lin AJ Golan DE Michel T Subcellular targeting and agonist-induced site-specific phosphorylation of endothelial nitric-oxide synthase J Biol Chem 2002, 277:39554-60. 10.1074/ jbc.M207299200 12189156
39. Scott-Burden T Regulation of nitric oxide production by tetrahydrobiopterin Circulation 1995, 91:248-50. 7805211
40. Ihlemann N Rask-Madsen C Perner A Dominguez H Hermann T Kober L et al Tetrahydrobiopterin restores endothelial dysfunction induced by an oral glucose challenge in healthy subjects Am J Physiol Heart Circ Physiol 2003, 285:H875-82. 12730050
41. Heitzer T Krohn K Albers S Meinertz T Tetrahydrobiopterin improves endothelium-dependent vasodilation by increasing nitric oxide activity in patients with Type II diabetes mellitus Diabetologia 2000, 43:1435-8. 10.1007/s001250051551 11126415
42. Bagi Z Koller A Lack of nitric oxide mediation of flow-dependent arteriolar dilation in type I diabetes is restored by sepiapterin J Vasc Res 2003, 40:47-57. 10.1159/000068938 12644725
43. Cai S Alp NJ McDonald D Smith I Kay J Canevari L et al GTP cyclohydrolase I gene transfer augments intracellular tetrahydrobiopterin in human endothelial cells: Effects on nitric oxide synthase activity, protein levels and dimerisation Cardiovasc Res 2002, 55:838-49. 10.1016/S0008-6363(02)00460-1 12176133
44. Tiefenbacher CP Tetrahydrobiopterin: A critical cofactor for eNOS and a strategy in the treatment of endothelial dysfunction? Am J Physiol Heart Circ Physiol 2001, 280:H2484-8. 11356602
45. Mayer B Werner ER In search of a function for tetrahydrobiopterin in the biosynthesis of nitric oxide Naunyn Schmiedebergs Arch Pharmacol 1995, 351:453-63. 10.1007/BF00171035 7543976
46. Vasquez-Vivar J Kalyanaraman B Martasek P Hogg N Masters BS Karoui H et al Superoxide generation by endothelial nitric oxide synthase: The influence of cofactors Proc Natl Acad Sci USA 1998, 95:9220-5. 21319 9689061 10.1073/pnas.95.16.9220
47. Meininger CJ Marinos RS Hatakeyama K Martinez-Zaguilan R Rojas JD Kelly KA et al Impaired nitric oxide production in coronary endothelial cells of the spontaneously diabetic BB rat is due to tetrahydrobiopterin deficiency Biochem J 2000, 349:353-6. 1221156 10861247 10.1042/ 0264-6021:3490353
48. Bitar MS Wahid S Mustafa S Al-Saleh E Dhaunsi GS Al-Mulla F Nitric oxide dynamics and endothelial dysfunction in type II model of genetic diabetes Eur J Pharmacol 2005, 511:53-64. 10.1016/j.ejphar.2005.01.014 15777779
49. Eskurza I Myerburgh LA Kahn ZD Seals DR Tetrahydrobiopterin augments endothelium-dependent dilatation in sedentary but not in habitually exercising older adults J Physiol 2005, 568:1057-65. 1464176 16141271 10.1113/jphysiol.2005.092734
50. Simons JM Hart BA Ip Vai Ching TR van Dijk H Labadie RP Metabolic activation of natural phenols into selective oxidative burst agonists by activated human neutrophils Free Radic Biol Med 1990, 8:251-8. 10.1016/ 0891-5849(90)90070-Y 2160411
51. Heumuller S Wind S Barbosa-Sicard E Schmidt HH Busse R Schroder K et al Apocynin is not an inhibitor of vascular NADPH oxidases but an antioxidant Hypertension 2008, 51:211-7. 10.1161/ HYPERTENSIONAHA.107.100214 18086956
52. Ferriss JB O'Hare JA Kelleher CC Sullivan PA Cole MM Ross HF et al Diabetic control and the renin-angiotensin system, catecholamines, and blood pressure Hypertension 1985, 7:II58-63. 3935582
53. Lip PL Chatterjee S Caine GJ Hope-Ross M Gibson J Blann AD Plasma vascular endothelial growth factor, angiopoietin-2, and soluble angiopoietin receptor tie-2 in diabetic retinopathy: Effects of laser photocoagulation and angiotensin receptor blockade Br J Ophthalmol 2004, 88:1543-6. 1772428 15548809 10.1136/bjo.2004.048587
54. Taguchi K Kobayashi T Hayashi Y Matsumoto T Kamata K Enalapril improves impairment of SERCA-derived relaxation and enhancement of tyrosine nitration in diabetic rat aorta Eur J Pharmacol 2007, 556:121-8. 10.1016/ j.ejphar.2006.11.026 17196960
55. Hollenberg NK Stevanovic R Agarwal A Lansang MC Price DA Laffel LM et al Plasma aldosterone concentration in the patient with diabetes mellitus Kidney Int 2004, 65:1435-9. 10.1111/j.1523-1755.2004.00524.x 15086486
56. Hattori Y Akimoto K Gross SS Hattori S Kasai K Angiotensin-II-induced oxidative stress elicits hypoadiponectinaemia in rats Diabetologia 2005, 48:1066-74. 10.1007/s00125-005-1766-7 15864528
57. Laursen JB Somers M Kurz S McCann L Warnholtz A Freeman BA et al Endothelial regulation of vasomotion in apoE-deficient mice: implications for interactions between peroxynitrite and tetrahydrobiopterin Circulation 2001, 103:1282-8. 11238274
58. Cai S Khoo J Mussa S Alp NJ Channon KM Endothelial nitric oxide synthase dysfunction in diabetic mice: Importance of tetrahydrobiopterin in eNOS dimerisation Diabetologia 2005, 48:1933-40. 10.1007/s00125-005-1857-5 16034613
59. Ding QF Hayashi T Packiasamy AR Miyazaki A Fukatsu A Shiraishi H et al The effect of high glucose on NO and O2- through endothelial GTPCH1 and NADPH oxidase Life Sci 2004, 75:3185-94. 10.1016/j.lfs.2004.06.005 15488897
60. Drummond GR Cai H Davis ME Ramasamy S Harrison DG Transcriptional and posttranscriptional regulation of endothelial nitric oxide synthase expression by hydrogen peroxide Circ Res 2000, 86:347-54. 10679488
61. Brodsky SV Yamamoto T Tada T Kim B Chen J Kajiya F et al Endothelial dysfunction in ischemic acute renal failure: Rescue by transplanted endothelial cells Am J Physiol Renal Physiol 2002, 282:F1140-9. 11997331
62. Grumbach IM Chen W Mertens SA Harrison DG A negative feedback mechanism involving nitric oxide and nuclear factor kappa-B modulates endothelial nitric oxide synthase transcription J Mol Cell Cardiol 2005, 39:595-603. 10.1016/j.yjmcc.2005.06.012 16099468
63. Vaziri ND Wang XQ cGMP-mediated negative-feedback regulation of endothelial nitric oxide synthase expression by nitric oxide Hypertension 1999, 34:1237-41. 10601124