Skip to main content
Log in

Detraining reverses exercise-induced improvement in blood pressure associated with decrements of oxidative stress in various tissues in spontaneously hypertensive rats

  • Published:
Molecular and Cellular Biochemistry Aims and scope Submit manuscript

Abstract

This study aimed to investigate the effects of moderate intensity swimming exercise (10 weeks) followed by detraining (for five and 10 weeks) on oxidative stress levels of heart, lung, kidney, and liver tissues and systolic blood pressure (SBP) of spontaneously hypertensive rats (SHR). SHR and control rats were randomized into sedentary, exercised, detrained (5 weeks) and late-detrained (10 weeks) groups. Corresponding sedentary rats were grouped as time 1-2-3. Exercise of 60 min, 5 days/week/10 weeks was applied. Detraining rats underwent the same training protocol and then discontinued training during next 5, 10 weeks. SBP was measured by tail-cuff method. Tissue total oxidant/antioxidant status was measured using a commercial kit and oxidative stress index (OSI) was calculated. Exercise training slightly decreased tissue OSI of SHR and reduced SBP of both groups. Tissue OSI of SHR were higher than WKY and aging resulted in increment of oxidants in groups. detraining yielded time-dependent increments in oxidative stress of all tissues and SBP of both rat groups. Although short-term cessations may be tolerated, our results emphasize the importance of exercising as a way of life for cardiovascular well-being in hypertensives or in individuals who are genetically under risk of hypertension.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig 3
Fig. 4

Similar content being viewed by others

References

  1. Agarwal D, Elks CM, Reed SD, Mariappan N, Majid DS, Francis J (2012) Chronic exercise preserves renal structure and hemodynamics in spontaneously hypertensive rats. Antioxid Redox Signal 6:139–152. doi:10.1089/ars.2011.3967

    Article  Google Scholar 

  2. Lassegue B, Griendling KK (2004) Reactive oxygen species in hypertension; an update. Am J Hypertens 17:852–860

    Article  PubMed  CAS  Google Scholar 

  3. Lee MY, Griendling KK (2008) Redox signaling, vascular function and hypertension. Antioxid Redox Signal 10:1045–1059. doi:10.1089/ars.2007.1986

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  4. Amenta F, Di Tullio MA, Tomassoni D (2003) Arterial hypertension and brain damage: evidence from animal models. Clin Exper Hypertens 25:359–380

    Article  Google Scholar 

  5. Ito H, Torii M, Suzuki T (1992) A comparative study on defense systems for lipid peroxidation by free radicals in spontaneously hypertensive and normotensive rat myocardium. Comp Biochem Physiol 103:37–40

    CAS  Google Scholar 

  6. De Craemer D, Lobe E, Pauwells M, Verbeelen D, Van Den Branden C (2001) Angiotensin II administration causes enhanced expression of glomerulosclerosis-related markers and decreased renal antioxidant enzyme activities in rats. Exp Nephrol 9:125–132

    Article  PubMed  Google Scholar 

  7. Pogan L, Garneau L, Bissonnette P, Wu L, Sauve R (2001) Abnormal Ca2+ signaling in vascular endothelial cells from spontaneously hypertensive rats: role of free radicals. J Hypertens 19:721–730

    Article  PubMed  CAS  Google Scholar 

  8. Ulker S, McMaster D, McKeown PP, Bayraktutan U (2003) Impaired activities of antioxidant enzymes elicit endothelial dysfunction in spontaneously hypertensive rats despite enhanced vascular nitric oxide generation. Cardiovasc Res 59:488–500

    Article  PubMed  CAS  Google Scholar 

  9. Whelton SP, Chin A, Xin X, He J (2002) Effect of aerobic exercise on blood pressure: a meta-analysis of randomized, controlled trials. Ann Intern Med 136:493–503

    Article  PubMed  Google Scholar 

  10. Powers SK, Ji LL, Leeuwenburgh C (1999) Exercise training-induced alterations in skeletal muscle antioxidant capacity: a brief review. Med Sci Sports Exer 31:987–997

    Article  CAS  Google Scholar 

  11. Pepe H, Balci SS, Revan S, Akalın PP, Kurtoglu F (2009) Comparison of oxidative stress and antioxidant capacity before and after running exercises in both sexes. Gend Med 6:587–595. doi:10.1016/j.genm.2009.10.001

    Article  PubMed  Google Scholar 

  12. Leeuwenburgh C, Hollander J, Leichtweis S, Griffiths M, Gore M, Ji LL (1997) Adaptations of glutathione antioxidant system to endurance training are tissue and muscle fiber specific. Am J Physiol 272:R363369

    Google Scholar 

  13. Agarwal D, Dange RB, Vila J, Otamendi AJ, Francis J (2012) Detraining differentially preserved beneficial effects of exercise on hypertension: effects on blood pressure, cardiac function, brain inflammatory cytokines and oxidative stress. PLoS ONE 7:e52569. doi:10.1371/journal.pone.0052569

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  14. Ahmed N, Abdul Khaliq M, Shah SH, Anwar W (2008) Compliance to antihypertensive drugs, salt restriction, exercise and control of systemic hypertension in hypertensive patients at Abbottabad. J Ayub Med Coll Abbottabad 20:66–69

    PubMed  Google Scholar 

  15. Erel O (2005) A new automated colorimetric method for measuring total oxidant status. Clin Biochem 38:1103–1111

    Article  PubMed  CAS  Google Scholar 

  16. Erel O (2004) A novel automated method to measure total antioxidant re-sponse against potent free radical reactions. Clin Biochem 37:112–119

    Article  PubMed  CAS  Google Scholar 

  17. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  18. Nelson DL, Cox MM (2001) Lehninger principles of biochemistry, 3rd edn. MacMillan Press Ltd., Hampshire

    Book  Google Scholar 

  19. Chance B, Sies H, Boveries A (1979) Hydroperoxide metabolism in mammalian organs. Physiol Rev 59:527–605

    PubMed  CAS  Google Scholar 

  20. Gómez-Amores L, Mate A, Revilla E, Santa-María C, Vázquez CM (2006) Antioxidant activity of propionyl-L-carnitine in liver and heart of spontaneously hypertensive rats. Life Sci 78(17):1945–1952

    Article  PubMed  Google Scholar 

  21. Wilson DO, Johnson P (2000) Exercise modulates antioxidant enzyme gene expression in rat myocardium and liver. J Appl Physiol 88(5):1791–1796

    PubMed  CAS  Google Scholar 

  22. Rahman I, MacNee W (2012) Antioxidant pharmacological therapies for COPD. Curr Opin Pharmacol 12(3):256–265

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  23. Husain-Syed F, McCullough PA, Birk HW, Renker M, Brocca A, Seeger W et al (2015) Cardio-pulmonary–renal interactions: a multidisciplinary approach. J Am Coll Cardiol 65(22):2433–2448. doi:10.1016/j.jacc.2015.04.024

    Article  PubMed  CAS  Google Scholar 

  24. Ogura S, Shimosawa T (2014) Oxidative stress and organ damages. Curr Hypertens Rep 16(8):452. doi:10.1007/s11906-014-0452-x

    Article  PubMed  Google Scholar 

  25. Arendshorst WJ, Chatziantoniou C, Daniels FH (1990) Role of angiotensin in the renal vasoconstriction observed during the development of genetic hypertension. Kidney Int Suppl 30:S92–96

    PubMed  CAS  Google Scholar 

  26. Rincón J, Correia D, Arcaya JL, Finol E, Fernández A, Pérez M et al (2015) Role of angiotensin II type 1 receptor on renal NAD(P)H oxidase, oxidative stress and inflammation in nitric oxide inhibition induced-hypertension. Life Sci 124:81–90. doi:10.1016/j.lfs.2015.01.005

    Article  PubMed  Google Scholar 

  27. Kosugi T, Sato W (2012) Midkine and the kidney: health and diseases. Nephrol Dial Transplant 27(1):16–21. doi:10.1093/ndt/gfr652

    Article  PubMed  CAS  Google Scholar 

  28. Lazaro A, Gallego-Delgado J, Justo P, Esteban V, Osende J, Mezzano S et al (2005) Long-term blood pressure control prevents oxidative renal injury. Antioxid Redox Signal 7:1285–1293

    Article  PubMed  CAS  Google Scholar 

  29. Nabha L, Garbern JC, Buller CL, Charpie JR (2005) Vascular oxidative stress precedes high blood pressure in spontaneously hypertensive rats. Clin Exp Hypertens 27:71–82

    Article  PubMed  CAS  Google Scholar 

  30. Agarwal D, Haque M, Sriramula S, Mariappan N, Pariaut R, Francis J (2009) Role of proinflammatory cytokines and redox homeostasis in exercise-induced delayed progression of hypertension in spontaneously hypertensive rats. Hypertens 6:1393–1400. doi:10.1161/HYPERTENSIONAHA.109.135459

    Article  Google Scholar 

  31. Graham D, Rush J (2004) Exercise training improves aortic endothelium dependent vasorelaxation and determinants of nitric oxide bioavailability in spontaneously hypertensive rats. J Appl Physiol 96:2088–2096

    Article  PubMed  CAS  Google Scholar 

  32. Bertagnolli M, Campos C, Schenkel PC, de Oliveira VL, De Angelis K, Belló-Klein A et al (2006) Baroreflex sensitivity improvement is associated with decreased oxidative stress in trained spontaneously hypertensive rat. J Hypertens 24:2437–2443

    Article  PubMed  CAS  Google Scholar 

  33. Kilic-Erkek O, Kilic-Toprak E, Kucukatay V, Bor-Kucukatay M (2014) Exercise training and detraining modify hemorheological parameters of spontaneously hypertensive rats. Biorheology 51:355–367. doi:10.3233/BIR-14030

    Article  PubMed  Google Scholar 

  34. Kakarla P, Vadluri G, Reddy KS, Leeuwenburgh C (2005) Vulnerability of the mid aged rat myocardium to the age-induced oxidative stress: influence of exercise training on antioxidant defense system. Free Radic Res 39:1211–1217

    Article  PubMed  CAS  Google Scholar 

  35. Maeda S, Miyauchi T, Kakiyama T (2001) Effects of exercise training of 8 weeks and detraining on plasma levels of endothelium-derived factors, endothelin-1 and nitric oxide, in healthy young humans. Life Sci 69:1005–1016

    Article  PubMed  CAS  Google Scholar 

  36. Roque FR, Briones AM, García-Redondo AB, Galán M, Martínez-Revelles S, Avendaño MS et al (2013) Aerobic exercise reduces oxidative stress and improves vascular changes of small mesenteric and coronary arteries in hypertension. Br J Pharmacol 168:686–703. doi:10.1111/j.1476-5381.2012.02224.x

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  37. Polidori MC, Mecocci P, Cherubini A (2000) Physical activity and oxidative stress during aging. Int J Sports Med 21:154–157

    Article  PubMed  CAS  Google Scholar 

  38. Gunduz F, Senturk UK, Kuru O, Aktekin B, Aktekin MR (2004) The effect of one year’s swimming exercise on oxidant stress and antioxidant capacity in aged rats. Physiol Res 53:171–176

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This study was supported by Pamukkale University Scientific Research Projects Coordination Unit through project numbers 2012ARŞ002, 2013SBE002, 2013SBE003, and 2015HZL010.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Melek Bor-Kucukatay.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kilic-Erkek, O., Kilic-Toprak, E., Caliskan, S. et al. Detraining reverses exercise-induced improvement in blood pressure associated with decrements of oxidative stress in various tissues in spontaneously hypertensive rats. Mol Cell Biochem 412, 209–219 (2016). https://doi.org/10.1007/s11010-015-2627-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11010-015-2627-4

Keywords

Navigation