Previous Exercise Training Has a Beneficial Effect on Renal and Cardiovascular Function in a Model of Diabetes

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

  Silva, Kleiton Augusto dos Santos ^a   Luiz, Rafael da Silva ^a   Rampaso, Rodolfo Rosseto ^a   de Abreu, Nayda Parísio ^a   Moreira, Édson Dias ^b   Mostarda, Cristiano Teixeira ^b   de Angelis, Kátia ^c   de Paulo Castro Teixeira, Vicente ^a   Irigoyen, Maria Cláudia ^b   Schor, Nestor ^a  

^a FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c Nove de Julho University   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ALBUMIN; CREATININE; STREPTOZOCIN;

ALBUMINURIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTONOMIC NERVOUS SYSTEM FUNCTION; BRADYCARDIA; CARDIOVASCULAR FUNCTION; CONTROLLED STUDY; CREATININE URINE LEVEL; DIABETES MELLITUS; DIABETIC CARDIOMYOPATHY; DIABETIC NEPHROPATHY; ECHOCARDIOGRAPHY; EXERCISE; FOLLOW UP; HEART EJECTION FRACTION; HEART PERFORMANCE; HEART RATE VARIABILITY; KIDNEY FUNCTION; MALE; NONHUMAN; PRESSORECEPTOR REFLEX; PROTEINURIA; RAT; SEDENTARY LIFESTYLE; STREPTOZOCIN DIABETES; SYMPATHETIC NERVE; TACHYCARDIA; TREATMENT DURATION;

ANIMALS; BAROREFLEX; BLOOD GLUCOSE; BODY WEIGHT; DIABETES MELLITUS, EXPERIMENTAL; DISEASE PROGRESSION; ECHOCARDIOGRAPHY; HEART; KIDNEY; MALE; PHYSICAL CONDITIONING, ANIMAL; RATS; RATS, WISTAR; TIME FACTORS;

ANIMALIA; BOVINE RESPIRATORY SYNCYTIAL VIRUS; RATTUS; RATTUS NORVEGICUS;

EID: 84868689390     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0048826     Document Type: Article

References (56)

1. Zimmet PZ, McCarty DJ, de Courten MP, (1997) The global epidemiology of non-insulin-dependent diabetes mellitus and the metabolic syndrome. J Diabetes Complications 11: 60-68.
2. Souza SB, Flues K, Paulini J, Mostarda C, Rodrigues B, et al. (2007) Role of exercise training in cardiovascular autonomic dysfunction and mortality in diabetic ovariectomized rats. Hypertension 50: 786-791.
3. Bardoux P, Martin H, Ahloulay M, Schmitt F, Bouby N, et al. (1999) Vasopressin contributes to hyperfiltration, albuminuria, and renal hypertrophy in diabetes mellitus: study in vasopressin-deficient Brattleboro rats. Proc Natl Acad Sci U S A 96: 10397-10402.
4. Lohmeier TE, (2003) Interactions between angiotensin II and baroreflexes in long-term regulation of renal sympathetic nerve activity. Circ Res 92: 1282-1284.
5. Gu H, Zhang ZH, Epstein PN, Li L, Harden SW, et al. (2009) Impaired baroreflex control of renal sympathetic nerve activity in type 1 diabetic mice (OVE26). Neuroscience 161: 78-85.
6. Schaan BD, Irigoyen MC, Bertoluci MC, Lima NG, Passaglia J, et al. (2005) Increased urinary TGF-beta1 and cortical renal GLUT1 and GLUT2 levels: additive effects of hypertension and diabetes. Nephron Physiol 100: p43-50.
7. Bell TD, DiBona GF, Wang Y, Brands MW, (2006) Mechanisms for renal blood flow control early in diabetes as revealed by chronic flow measurement and transfer function analysis. J Am Soc Nephrol 17: 2184-2192.
8. La Rovere MT, Bigger JT Jr, Marcus FI, Mortara A, Schwartz PJ, (1998) Baroreflex sensitivity and heart-rate variability in prediction of total cardiac mortality after myocardial infarction. ATRAMI (Autonomic Tone and Reflexes After Myocardial Infarction) Investigators. Lancet 351: 478-484.
9. Chandra P, Sands RL, Gillespie BW, Levin NW, Kotanko P, et al. (2012) Predictors of heart rate variability and its prognostic significance in chronic kidney disease. Nephrol Dial Transplant 27: 700-709.
10. Brotman DJ, Bash LD, Qayyum R, Crews D, Whitsel EA, et al. (2010) Heart rate variability predicts ESRD and CKD-related hospitalization. J Am Soc Nephrol 21: 1560-1570.
11. Johansen KL, (2005) Exercise and chronic kidney disease: current recommendations. Sports Med 35: 485-499.
12. Silva GJ, Brum PC, Negrao CE, Krieger EM, (1997) Acute and chronic effects of exercise on baroreflexes in spontaneously hypertensive rats. Hypertension 30: 714-719.
13. Winnick JJ, Sherman WM, Habash DL, Stout MB, Failla ML, et al. (2008) Short-term aerobic exercise training in obese humans with type 2 diabetes mellitus improves whole-body insulin sensitivity through gains in peripheral, not hepatic insulin sensitivity. J Clin Endocrinol Metab 93: 771-778.
14. Mostarda C, Rogow A, Silva IC, De La Fuente RN, Jorge L, et al. (2009) Benefits of exercise training in diabetic rats persist after three weeks of detraining. Auton Neurosci 145: 11-16.
15. Ramires PR, Forjaz CL, Strunz CM, Silva ME, Diament J, et al. (1997) Oral glucose ingestion increases endurance capacity in normal and diabetic (type I) humans. J Appl Physiol 83: 608-614.
16. Goodyear LJ, Kahn BB, (1998) Exercise, glucose transport, and insulin sensitivity. Annu Rev Med 49: 235-261.
17. Hayashi T, Wojtaszewski JF, Goodyear LJ, (1997) Exercise regulation of glucose transport in skeletal muscle. Am J Physiol 273: E1039-1051.
18. DiCarlo SE, Collins HL, Rodenbaugh DW, Smitha MR, Berger RD, et al. (2002) Daily exercise reduces measures of heart rate and blood pressure variability in hypertensive rats. Clin Exp Hypertens 24: 221-234.
19. Weston PJ, James MA, Panerai R, McNally PG, Potter JF, et al. (1996) Abnormal baroreceptor-cardiac reflex sensitivity is not detected by conventional tests of autonomic function in patients with insulin-dependent diabetes mellitus. Clin Sci (Lond) 91: 59-64.
20. Niebauer J, Maxwell AJ, Lin PS, Tsao PS, Kosek J, et al. (1999) Impaired aerobic capacity in hypercholesterolemic mice: partial reversal by exercise training. Am J Physiol 276: H1346-1354.
21. Zheng H, Li YF, Zucker IH, Patel KP, (2006) Exercise training improves renal excretory responses to acute volume expansion in rats with heart failure. Am J Physiol Renal Physiol 291: F1148-1156.
22. Mousa TM, Liu D, Cornish KG, Zucker IH, (2008) Exercise training enhances baroreflex sensitivity by an angiotensin II-dependent mechanism in chronic heart failure. J Appl Physiol 104: 616-624.
23. Colberg SR, Sigal RJ, Fernhall B, Regensteiner JG, Blissmer BJ,et al. Exercise and type 2 diabetes: the American College of Sports Medicine and the American Diabetes Association: joint position statement. Diabetes Care 33: e147-167.
24. el Midaoui A, Tancrede G, Nadeau A, (1996) Effect of physical training on mitochondrial function in skeletal muscle of normal and diabetic rats. Metabolism 45: 810-816.
25. Kivela R, Silvennoinen M, Lehti M, Jalava S, Vihko V, et al. (2008) Exercise-induced expression of angiogenic growth factors in skeletal muscle and in capillaries of healthy and diabetic mice. Cardiovasc Diabetol 7: 13.
26. Cheng SM, Ho TJ, Yang AL, Chen IJ, Kao CL, et al. (2012) Exercise training enhances cardiac IGFI-R/PI3K/Akt and Bcl-2 family associated pro-survival pathways in streptozotocin-induced diabetic rats. Int J Cardiol.
27. de Angelis KL, Oliveira AR, Dall'Ago P, Peixoto LR, Gadonski G, et al. (2000) Effects of exercise training on autonomic and myocardial dysfunction in streptozotocin-diabetic rats. Braz J Med Biol Res 33: 635-641.
28. de Angelis Lobo d'Avila K, Gadonski G, Fang J, Dall'Ago P, Albuquerque VL, et al. (1999) Exercise reverses peripheral insulin resistance in trained L-NAME-hypertensive rats. Hypertension 34: 768-772.
29. Nakai N, Miyazaki Y, Sato Y, Oshida Y, Nagasaki M, et al. (2002) Exercise training increases the activity of pyruvate dehydrogenase complex in skeletal muscle of diabetic rats. Endocr J 49: 547-554.
30. Bergamaschi CT, Boim MA, Moura LA, Picarro IC, Schor N, (1997) Effects of long-term training on the progression of chronic renal failure in rats. Med Sci Sports Exerc 29: 169-174.
31. Gunduz F, Kuru O, Senturk UK, (2003) Effect of nitric oxide on exercise-induced proteinuria in rats. J Appl Physiol 95: 1867-1872.
32. Cianflocco AJ, (1992) Renal complications of exercise. Clin Sports Med 11: 437-451.
33. Albright AL, Mahan JD, Ward KM, Sherman WM, Roehrig KL, et al. (1995) Diabetic nephropathy in an aerobically trained rat model of diabetes. Med Sci Sports Exerc 27: 1270-1277.
34. Rodrigues AM, Bergamaschi CT, Araujo RC, Mouro MG, Rosa TS, et al. (2011) Effects of training and nitric oxide on diabetic nephropathy progression in type I diabetic rats. Exp Biol Med (Maywood) 236: 1180-1187.
35. Agarwal D, Elks CM, Reed SD, Mariappan N, Majid DS, et al. (2012) Chronic exercise preserves renal structure and hemodynamics in spontaneously hypertensive rats. Antioxid Redox Signal 16: 139-152.
36. Luippold G, Beilharz M, Muhlbauer B, (2004) Chronic renal denervation prevents glomerular hyperfiltration in diabetic rats. Nephrol Dial Transplant 19: 342-347.
37. Matsuoka H, (1993) Protective role of renal nerves in the development of diabetic nephropathy. Diabetes Res 23: 19-29.
38. Schaan BD, Irigoyen MC, Lacchini S, Moreira ED, Schmid H, et al. (2005) Sympathetic modulation of the renal glucose transporter GLUT2 in diabetic rats. Auton Neurosci 117: 54-61.
39. Malfitano C, de Angelis K, Fernandes T, Wichi RB, Rosa K, et al. (2012) Low-dose enalapril reduces angiotensin II and attenuates diabetic-induced cardiac and autonomic dysfunctions. J Cardiovasc Pharmacol 59: 58-65.
40. Zhang Y, Babcock SA, Hu N, Maris JR, Wang H, et al. (2012) Mitochondrial aldehyde dehydrogenase (ALDH2) protects against streptozotocin-induced diabetic cardiomyopathy: role of GSK3beta and mitochondrial function. BMC Med 10: 40.
41. Akula A, Kota MK, Gopisetty SG, Chitrapu RV, Kalagara M, et al. (2003) Biochemical, histological and echocardiographic changes during experimental cardiomyopathy in STZ-induced diabetic rats. Pharmacol Res 48: 429-435.
42. Wichi R, Malfitano C, Rosa K, De Souza SB, Salemi V, et al. (2007) Noninvasive and invasive evaluation of cardiac dysfunction in experimental diabetes in rodents. Cardiovasc Diabetol 6: 14.
43. Mihm MJ, Seifert JL, Coyle CM, Bauer JA, (2001) Diabetes related cardiomyopathy time dependent echocardiographic evaluation in an experimental rat model. Life Sci 69: 527-542.
44. Bai SZ, Sun J, Wu H, Zhang N, Li HX, et al. (2012) Decrease in calcium-sensing receptor in the progress of diabetic cardiomyopathy. Diabetes Res Clin Pract 95: 378-385.
45. Mostarda C, Moraes-Silva IC, Moreira ED, Medeiros A, Piratello AC, et al. (2011) Baroreflex sensitivity impairment is associated with cardiac diastolic dysfunction in rats. J Card Fail 17: 519-525.
46. Jorge L, Rodrigues B, Rosa KT, Malfitano C, Loureiro TC, et al. (2011) Cardiac and peripheral adjustments induced by early exercise training intervention were associated with autonomic improvement in infarcted rats: role in functional capacity and mortality. Eur Heart J 32: 904-912.
47. Dall'ago P, D'Agord Schaan B, da Silva VO, Werner J, da Silva Soares PP, et al. (2007) Parasympathetic dysfunction is associated with baroreflex and chemoreflex impairment in streptozotocin-induced diabetes in rats. Auton Neurosci 131: 28-35.
48. Farah Vde M, de Angelis K, Joaquim LF, Candido GO, Bernardes N, et al. (2007) Autonomic modulation of arterial pressure and heart rate variability in hypertensive diabetic rats. Clinics (Sao Paulo) 62: 477-482.
49. Harthmann AD, de Angelis K, Costa LP, Senador D, Schaan BD, et al. (2007) Exercise training improves arterial baro- and chemoreflex in control and diabetic rats. Auton Neurosci 133: 115-120.
50. Dinh W, Futh R, Lankisch M, Bansemir L, Nickl W,et al. Cardiovascular autonomic neuropathy contributes to left ventricular diastolic dysfunction in subjects with Type 2 diabetes and impaired glucose tolerance undergoing coronary angiography. Diabet Med.
51. Moraes-Silva IC, De La Fuente RN, Mostarda C, Rosa K, Flues K, et al. (2010) Baroreflex deficit blunts exercise training-induced cardiovascular and autonomic adaptations in hypertensive rats. Clin Exp Pharmacol Physiol 37: e114-120.
52. Jorge L, da Pureza DY, da Silva Dias D, Conti FF, Irigoyen MC, et al. (2012) Dynamic aerobic exercise induces baroreflex improvement in diabetic rats. Exp Diabetes Res 2012: 108680.
53. Rodrigues B, Figueroa DM, Mostarda CT, Heeren MV, Irigoyen MC, et al. (2007) Maximal exercise test is a useful method for physical capacity and oxygen consumption determination in streptozotocin-diabetic rats. Cardiovasc Diabetol 6: 38.
54. Brooks GA, White TP, (1978) Determination of metabolic and heart rate responses of rats to treadmill exercise. J Appl Physiol 45: 1009-1015.
55. Soares PP, da Nobrega AC, Ushizima MR, Irigoyen MC, (2004) Cholinergic stimulation with pyridostigmine increases heart rate variability and baroreflex sensitivity in rats. Auton Neurosci 113: 24-31.
56. Lundin S, Ricksten SE, Thoren P, (1984) Renal sympathetic activity in spontaneously hypertensive rats and normotensive controls, as studied by three different methods. Acta Physiol Scand 120: 265-272.