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Aerobic Exercise Attenuates Kidney Injury, Improves Physical Performance, and Increases Antioxidant Defenses in Lungs of Adenine-Induced Chronic Kidney Disease Mice

Abstract

The association between chronic kidney disease (CKD) and pulmonary pathophysiological changes is well stablished. Nevertheless, the effects of aerobic exercise (AE) on lungs of CKD need further clarification. Thus, Swiss mice were divided in control, AE, CKD, and CKD + AE groups. CKD was induced by 0.2% adenine intake during 8 weeks (4 weeks of CKD induction and 4 weeks of AE). AE consisted in running on treadmill, at moderate intensity, 30 min/day, 5 days/week, during 4 weeks. Twenty-four hours after the last training day, functional capacity test was performed, and 48 h after the test, mice were euthanized. CKD mice showed a significant increase in urine output, serum urea, and creatinine concentrations, and decreased body weight and urine density, besides oxidative damage (p = 0.044), edema area (p < 0.001), leukocyte infiltration (p = 0.040), and collagen area in lung tissue (p = 0.004). AE resulted in an increase of distance traveled (p = 0.049) and maximum speed (p = 0.046), increased activity of catalase (p = 0.031) and glutathione peroxidase (p = 0.048) in lungs, increased levels of nitric oxide (NOx) in serum (p = 0.001) and bronchoalveolar lavage fluid (p = 0.047), and decreased kidney histological injury (p = 0.018) of CKD mice. However, AE also increased oxidative damage (p = 0.003) and did not change collagen content or perivascular edema in lungs (p > 0.05) of CKD mice. Therefore, AE attenuated kidney injury and improved antioxidants defenses in lungs. Despite no significant changes in pulmonary damage, AE significantly improved physical performance in CKD mice.

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AVAILABILITY OF DATA AND MATERIAL

The data underlying this article are available in the article and in its online Supplementary Information.

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References

  1. Askari, H., B. Seifi, and M. Kadkhodaee. 2016. Evaluation of renal-hepatic functional indices and blood pressure based on the progress of time in a rat model of chronic kidney disease. Nephro-Urology Monthly 8 (3).

  2. Levey, A.S., and J. Coresh. 2012. Chronic kidney disease. Lancet 379 (9811): 165–180. https://doi.org/10.1016/S0140-6736(11)60178-5.

    Article  PubMed  Google Scholar 

  3. Levin, A., P.E. Stevens, R.W. Bilous, J. Coresh, A.L.M. Francisco, De P.E. Jong, and De K. E. Griffith. 2013. Kidney disease: Improving global outcomes (KDIGO) CKD work group. KDIGO, et al 2012 clinical practice guideline for the evaluation and management of chronic kidney disease. Kidney International Supplements 3(1):1–150

  4. Webster, Angela C., Evi V. Nagler, Rachael L. Morton, and Philip Masson. 2017. Chronic kidney disease. The Lancet 389 (10075): 1238–1252. https://doi.org/10.1016/S0140-6736(16)32064-5.

    Article  Google Scholar 

  5. de Medeiros, A.I.C., H.K.B. Fuzari, C. Rattesa, D.C. Brandão, and P. de Melo Marinho. 2017. Inspiratory muscle training improves respiratory muscle strength, functional capacity and quality of life in patients with chronic kidney disease: A systematic review. Journal of Physiotherapy 63 (2): 76–83. https://doi.org/10.1016/j.jphys.2017.02.016.

    Article  PubMed  Google Scholar 

  6. Domenech, P., T. Perez, A. Saldarini, P. Uad, and C.G. Musso. 2017. Kidney-lung pathophysiological crosstalk: Its characteristics and importance. International Urology and Nephrology 49 (7): 1211–1215. https://doi.org/10.1007/s11255-017-1585-z.

    CAS  Article  PubMed  Google Scholar 

  7. Howden, E.J., J.S. Coombes, H. Strand, B. Douglas, K.L. Campbell, and N.M. Isbel. 2015. Exercise training in CKD: Efficacy, adherence, and safety. American Journal of Kidney Diseases 65 (4): 583–591. https://doi.org/10.1053/j.ajkd.2014.09.017.

    Article  PubMed  Google Scholar 

  8. Xavier, V.B., R.S. Roxo, L.A. Miorin, V.L. Dos Santos Alves, and Y.A. Dos Santos Sens. 2015. Impact of continuous positive airway pressure (CPAP) on the respiratory capacity of chronic kidney disease patients under hemodialysis treatment. International Urology and Nephrology 47 (6): 1011–1016. https://doi.org/10.1007/s11255-015-0988-y.

    CAS  Article  PubMed  Google Scholar 

  9. Afsar, B., D. Siriopol, G. Aslan, O.C. Eren, T. Dagel, U. Kilic, A. Kanbay, A. Burlacu, A. Covic, and M. Kanbay. 2018. The impact of exercise on physical function, cardiovascular outcomes and quality of life in chronic kidney disease patients: A systematic review. International Urology and Nephrology 50 (5): 885–904. https://doi.org/10.1007/s11255-018-1790-4.

    Article  PubMed  Google Scholar 

  10. Heiwe, S., and S.H. Jacobson. 2014. Exercise training in adults with CKD: A systematic review and meta-analysis. American Journal of Kidney Diseases 64 (3): 383–393. https://doi.org/10.1053/j.ajkd.2014.03.020.

    Article  PubMed  Google Scholar 

  11. Morishita, S., A. Tsubaki, and N. Shirai. 2017. Physical function was related to mortality in patients with chronic kidney disease and dialysis. Hemodialysis International 21 (4): 483–489. https://doi.org/10.1111/hdi.12564.

    Article  PubMed  Google Scholar 

  12. Roshanravan, B., J. Gamboa, and K. Wilund. 2017. Exercise and CKD: Skeletal muscle dysfunction and practical application of exercise to prevent and treat physical impairments in CKD. American Journal of Kidney Diseases 69 (6): 837–852. https://doi.org/10.1053/j.ajkd.2017.01.051.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Ali, B.H., T. Karaca, Y. Al Suleimani, M. Al Za’abi, J. Al Kalbani, M. Ashique, and A. Nemmar. 2017. The effect of swimming exercise on adenine-induced kidney disease in rats, and the influence of curcumin or lisinopril thereon. PLoS ONE 12 (4): e0176316. https://doi.org/10.1371/journal.pone.0176316.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  14. Coelho, B.L., L.G. Rocha, K.S. Scarabelot, D.L. Scheffer, M.M. Ronsani, P.C. Silveira, L.A. Silva, C.T. Souza, and R.A. Pinho. 2010. Physical exercise prevents the exacerbation of oxidative stress parameters in chronic kidney disease. Journal of Renal Nutrition 20 (3): 169–175. https://doi.org/10.1053/j.jrn.2009.10.007.

    CAS  Article  PubMed  Google Scholar 

  15. de Souza, P.S., L.G. da Rocha, C.B. Tromm, D.L. Scheffer, E.G. Victor, P.C. da Silveira, C.T. de Souza, L.A. Silva, and R.A. Pinho. 2012. Therapeutic action of physical exercise on markers of oxidative stress induced by chronic kidney disease. Life Sciences 91 (3–4): 132–136. https://doi.org/10.1016/j.lfs.2012.06.028.

    CAS  Article  PubMed  Google Scholar 

  16. Souza, M.K., R.V.P. Neves, T.S. Rosa, M.A. Cenedeze, S.C.A. Arias, C.K. Fujihara, R.F.P. Bacurau, N.O.S. Câmara, M.R. Moraes, and A. Pacheco E Silva Filho. 2018. Resistance training attenuates inflammation and the progression of renal fibrosis in chronic renal disease. Life Sciences 206: 93–97. https://doi.org/10.1016/j.lfs.2018.05.034.

    CAS  Article  PubMed  Google Scholar 

  17. Tamaki, M., K. Miyashita, A. Hagiwara, S. Wakino, H. Inoue, K. Fujii, C. Fujii, et al. 2017. Ghrelin treatment improves physical decline in sarcopenia model mice through muscular enhancement and mitochondrial activation. Journal of Endocrinology 64 (Suppl.):S47-S51. https://doi.org/10.1507/endocrj.64.S47.

  18. Nemmar, A., T. Karaca, S. Beegam, P. Yuvaraju, J. Yasin, and B.H. Ali. 2017. Lung oxidative stress, DNA damage, apoptosis, and fibrosis in adenine-induced chronic kidney disease in mice. Frontiers in Physiology 8: 896. https://doi.org/10.3389/fphys.2017.00896.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Kilkenny, C., W. Browne, I. C. Cuthill, M. Emerson, D. G. Altman, and NC3Rs Reporting Guidelines Working Group. 2010. Animal research: Reporting in vivo experiments: The ARRIVE guidelines. British Journal of Pharmacology 160 (7): 1577–1579. https://doi.org/10.1111/j.1476-5381.2010.00872.x.

    CAS  Article  Google Scholar 

  20. Ali, B.H., S. Al-Salam, M. Al Za’abi, M.I. Waly, A. Ramkumar, S. Beegam, I. Al-Lawati, S.A. Adham, and A. Nemmar. 2013. New model for adenine-induced chronic renal failure in mice, and the effect of gum acacia treatment thereon: Comparison with rats. Journal of Pharmacological and Toxicological Methods 68 (3): 384–393. https://doi.org/10.1016/j.vascn.2013.05.001.

    CAS  Article  PubMed  Google Scholar 

  21. Vieira, R.P., R.C. Claudino, A.C. Duarte, A.B. Santos, A. Perini, H.C. Faria Neto, T. Mauad, M.A. Martins, M. Dolhnikoff, and C.R. Carvalho. 2007. Aerobic exercise decreases chronic allergic lung inflammation and airway remodeling in mice. American Journal of Respiratory and Critical Care Medicine 176 (9): 871–877. https://doi.org/10.1164/rccm.200610-1567OC.

    Article  PubMed  Google Scholar 

  22. Camargo Hizume-Kunzler, D., F.R. Greiffo, B. Fortkamp, G. Ribeiro Freitas, J. Keller Nascimento, T. Regina Bruggemann, L. Melo Avila, et al. 2017. Aerobic exercise decreases lung inflammation by IgE decrement in an OVA mice model. International Journal of Sports Medicine 38 (6): 473–480. https://doi.org/10.1055/s-0042-121638.

    CAS  Article  PubMed  Google Scholar 

  23. Cardoso, G.H., D.M. Petry, J.J. Probst, L.F. de Souza, G. Ganguilhet, F. Bobinski, A.R.S. Santos, et al. 2018. High-intensity exercise prevents disturbances in lung inflammatory cytokines and antioxidant defenses induced by lipopolysaccharide. Inflammation 41 (6): 2060–2067. https://doi.org/10.1007/s10753-018-0849-9.

    CAS  Article  PubMed  Google Scholar 

  24. Granger, D.L., J.B. Hibbs, J.R. Perfect, and D.T. Durack. 1990. Metabolic fate of L-arginine in relation to microbiostatic capability of murine macrophages. The Journal of Clinical Investigation 85 (1): 264–273. https://doi.org/10.1172/JCI114422.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  25. Levine, R.L., D. Garland, C.N. Oliver, A. Amici, I. Climent, A.G. Lenz, B.W. Ahn, S. Shaltiel, and E.R. Stadtman. 1990. Determination of carbonyl content in oxidatively modified proteins. Methods in Enzymology 186: 464–478.

    CAS  Article  Google Scholar 

  26. Aebi, H. 1984. Catalase in vitro. Methods in Enzymology 105: 121–126. https://doi.org/10.1016/s0076-6879(84)05016-3.

    CAS  Article  PubMed  Google Scholar 

  27. Arnér, E.S., and A. Holmgren. 2000. Physiological functions of thioredoxin and thioredoxin reductase. European Journal of Biochemistry 267 (20): 6102–6109. https://doi.org/10.1046/j.1432-1327.2000.01701.x.

    Article  PubMed  Google Scholar 

  28. Carlberg, I., and B. Mannervik. 1985. Glutathione reductase. Methods in Enzymology 113: 484–490. https://doi.org/10.1016/s0076-6879(85)13062-4.

    CAS  Article  PubMed  Google Scholar 

  29. Paoletti, F., D. Aldinucci, A. Mocali, and A. Caparrini. 1986. A sensitive spectrophotometric method for the determination of superoxide dismutase activity in tissue extracts. Analytical Biochemistry 154 (2): 536–541. https://doi.org/10.1016/0003-2697(86)90026-6.

    CAS  Article  PubMed  Google Scholar 

  30. Wendel, A. 1981. Glutathione peroxidase. Methods in Enzymology 77: 325–333. https://doi.org/10.1016/s0076-6879(81)77046-0.

    CAS  Article  PubMed  Google Scholar 

  31. Dafre, A.L., A.E. Schmitz, and P. Maher. 2020. Rapid and persistent loss of TXNIP in HT22 neuronal cells under carbonyl and hyperosmotic stress. Neurochemistry International 132: 104585. https://doi.org/10.1016/j.neuint.2019.104585.

    CAS  Article  PubMed  Google Scholar 

  32. Weibel, E.R., G.S. Kistler, and W.F. Scherle. 1966. Practical stereological methods for morphometric cytology. Journal of Cell Biology 30 (1): 23–38. https://doi.org/10.1083/jcb.30.1.23.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  33. Suzuki, S., S. Takamura, J. Yoshida, Y. Shinzawa, O. Niwa, and R. Tamatani. 1995. Comparison of gentamicin nephrotoxicity between rats and mice. Comparative Biochemistry and Physiology Part C: Pharmacology Toxicology and Endocrinology 112 (1): 15–28.

    CAS  Article  Google Scholar 

  34. Santana, A.C., S. Degaspari, S. Catanozi, H. Dellê, L. de Sá Lima, C. Silva, P. Blanco, K. Solez, C. Scavone, and I.L. Noronha. 2013. Thalidomide suppresses inflammation in adenine-induced CKD with uraemia in mice. Nephrology, Dialysis, Transplantation 28 (5): 1140–1149. https://doi.org/10.1093/ndt/gfs569.

    CAS  Article  PubMed  Google Scholar 

  35. Zhang, L., Y. Wang, L. Xiong, Y. Luo, Z. Huang, and B. Yi. 2019. Exercise therapy improves eGFR, and reduces blood pressure and BMI in non-dialysis CKD patients: Evidence from a meta-analysis. BMC Nephrology 20 (1): 398. https://doi.org/10.1186/s12882-019-1586-5.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  36. Mingels, A., L. Jacobs, V. Kleijnen, W. Wodzig, and M. Dieijen-Visser. 2009. Cystatin C a marker for renal function after exercise. International Journal of Sports Medicine 30 (9): 668–671. https://doi.org/10.1055/s-0029-1220733.

    CAS  Article  PubMed  Google Scholar 

  37. Adams, G.R., and N.D. Vaziri. 2006. Skeletal muscle dysfunction in chronic renal failure: Effects of exercise. American Journal of Physiology. Renal Physiology 290 (4): F753-761. https://doi.org/10.1152/ajprenal.00296.2005.

    CAS  Article  PubMed  Google Scholar 

  38. Baria, Flavia, Maria Ayako Kamimura, Danilo Takashi Aoike, Adriano Ammirati, Mariana Leister Rocha, Marco Túlio de Mello, and Lilian Cuppari. 2014. Randomized controlled trial to evaluate the impact of aerobic exercise on visceral fat in overweight chronic kidney disease patients. Nephrology Dialysis Transplantation 29 (4): 857–864. https://doi.org/10.1093/ndt/gft529.

    CAS  Article  Google Scholar 

  39. Villanego, Florentino, Javier Naranjo, Luis Alberto Vigara, Juan Manuel Cazorla, Maria Elisa Montero, Teresa García, Julia Torrado, and Auxiliadora Mazuecos. 2020. Impact of physical exercise in patients with chronic kidney disease: Systematic review and meta-analysis. Nefrología (English Edition) 40 (3): 237–252. https://doi.org/10.1016/j.nefroe.2020.06.012.

    Article  Google Scholar 

  40. Wang, Xiaonan H., Du. Jie, Janet D. Klein, James L. Bailey, and William E. Mitch. 2009. Exercise ameliorates chronic kidney disease–induced defects in muscle protein metabolism and progenitor cell function. Kidney International 76 (7): 751–759. https://doi.org/10.1038/ki.2009.260.

    CAS  Article  PubMed  Google Scholar 

  41. Tani, T., H. Orimo, A. Shimizu, and S. Tsuruoka. 2017. Development of a novel chronic kidney disease mouse model to evaluate the progression of hyperphosphatemia and associated mineral bone disease. Science and Reports 7 (1): 2233. https://doi.org/10.1038/s41598-017-02351-6.

    CAS  Article  Google Scholar 

  42. De Moraes, W.M.A.M., P.R.M. de Souza, N.A. da Paixão, L.G.O. de Sousa, D.A. Ribeiro, A.G. Marshall, J. Prestes, M.C. Irigoyen, P.C. Brum, and A. Medeiros. 2018. Aerobic exercise training rescues protein quality control disruption on white skeletal muscle induced by chronic kidney disease in rats. Journal of Cellular and Molecular Medicine 22 (3): 1452–1463. https://doi.org/10.1111/jcmm.13374.

    CAS  Article  PubMed  Google Scholar 

  43. Clarkson, M.J., P.N. Bennett, S.F. Fraser, and S.A. Warmington. 2019. Exercise interventions for improving objective physical function in patients with end-stage kidney disease on dialysis: A systematic review and meta-analysis. American Journal of Physiology. Renal Physiology 316 (5): F856–F872. https://doi.org/10.1152/ajprenal.00317.2018.

    CAS  Article  PubMed  Google Scholar 

  44. Kuczmarski, J.M., M.D. Darocki, J.J. DuPont, R.A. Sikes, C.R. Cooper, W.B. Farquhar, and D.G. Edwards. 2011. Effect of moderate-to-severe chronic kidney disease on flow-mediated dilation and progenitor cells. Experimental Biology and Medicine (Maywood, N.J.) 236 (9): 1085–1092. https://doi.org/10.1258/ebm.2011.011008.

    CAS  Article  Google Scholar 

  45. Martens, C.R., D.L. Kirkman, and D.G. Edwards. 2016. The vascular endothelium in chronic kidney disease: A novel target for aerobic exercise. Exercise and Sport Sciences Reviews 44 (1): 12–19. https://doi.org/10.1249/JES.0000000000000065.

    Article  PubMed  PubMed Central  Google Scholar 

  46. Nosarev, A.V., L.V. Smagliy, Y. Anfinogenova, S.V. Popov, and L.V. Kapilevich. 2014. Exercise and NO production: Relevance and implications in the cardiopulmonary system. Frontiers in Cell and Developmental Biology 2: 73. https://doi.org/10.3389/fcell.2014.00073.

    Article  PubMed  Google Scholar 

  47. Tousoulis, D., A.M. Kampoli, C. Tentolouris, N. Papageorgiou, and C. Stefanadis. 2012. The role of nitric oxide on endothelial function. Current Vascular Pharmacology 10 (1): 4–18. https://doi.org/10.2174/157016112798829760.

    CAS  Article  PubMed  Google Scholar 

  48. Miyauchi, T., S. Maeda, M. Iemitsu, T. Kobayashi, Y. Kumagai, I. Yamaguchi, and M. Matsuda. 2003. Exercise causes a tissue-specific change of NO production in the kidney and lung. Journal of Applied Physiology (1985) 94 (1):60–68. https://doi.org/10.1152/japplphysiol.00269.2002.

  49. Chen, K.C., C.L. Hsieh, C.C. Peng, and R.Y. Peng. 2014. Exercise rescued chronic kidney disease by attenuating cardiac hypertrophy through the cardiotrophin-1 -> LIFR/gp 130 -> JAK/STAT3 pathway. European Journal of Preventive Cardiology 21 (4): 507–520. https://doi.org/10.1177/2047487312462827.

    Article  PubMed  Google Scholar 

  50. Ito, D., P. Cao, T. Kakihana, E. Sato, C. Suda, Y. Muroya, Y. Ogawa, et al. 2015. Chronic Running exercise alleviates early progression of nephropathy with upregulation of nitric oxide synthases and suppression of glycation in Zucker diabetic rats. PLoS ONE 10 (9): e0138037. https://doi.org/10.1371/journal.pone.0138037.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  51. Adams, G.R., C.D. Zhan, F. Haddad, and N.D. Vaziri. 2005. Voluntary exercise during chronic renal failure in rats. Medicine and Science in Sports and Exercise 37 (4): 557–562. https://doi.org/10.1249/01.mss.0000159006.87769.67.

    Article  PubMed  Google Scholar 

  52. Martens, C.R., J.M. Kuczmarski, J. Kim, J.J. Guers, M.B. Harris, S. Lennon-Edwards, and D.G. Edwards. 2014. Voluntary wheel running augments aortic l-arginine transport and endothelial function in rats with chronic kidney disease. American Journal of Physiology. Renal Physiology 307 (4): F418-426. https://doi.org/10.1152/ajprenal.00014.2014.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  53. Shelkovnikov, S., S.M. Summers, R. Elahimehr, G. Adams, R.E. Purdy, and N.D. Vaziri. 2008. Effect of exercise training on aortic tone in chronic renal insufficiency. American Journal of Hypertension 21 (5): 564–569. https://doi.org/10.1038/ajh.2008.24.

    Article  PubMed  Google Scholar 

  54. Green, D.J., A. Maiorana, G. O’Driscoll, and R. Taylor. 2004. Effect of exercise training on endothelium-derived nitric oxide function in humans. Journal of Physiology 561 (Pt 1): 1–25. https://doi.org/10.1113/jphysiol.2004.068197.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  55. Daenen, K., A. Andries, D. Mekahli, A. Van Schepdael, F. Jouret, and B. Bammens. 2019. Oxidative stress in chronic kidney disease. Pediatric Nephrology (Berlin, Germany) 34 (6): 975–991. https://doi.org/10.1007/s00467-018-4005-4.

    Article  Google Scholar 

  56. Honda, T., Y. Hirakawa, and M. Nangaku. 2019. The role of oxidative stress and hypoxia in renal disease. Kidney Research and Clinical Practice 38 (4):414–426. https://doi.org/10.23876/j.krcp.19.063.

  57. Boor, P., P. Celec, M. Behuliak, P. Grancic, A. Kebis, M. Kukan, N. Pronayová, T. Liptaj, T. Ostendorf, and K. Sebeková. 2009. Regular moderate exercise reduces advanced glycation and ameliorates early diabetic nephropathy in obese Zucker rats. Metabolism 58 (11): 1669–1677. https://doi.org/10.1016/j.metabol.2009.05.025.

    CAS  Article  PubMed  Google Scholar 

  58. Johansen, K.L. 2005. Exercise and chronic kidney disease: Current recommendations. Sports Medicine (Auckland, N. Z.) 35 (6): 485–499. https://doi.org/10.2165/00007256-200535060-00003.

    Article  Google Scholar 

  59. Esgalhado, M., M.B. Stockler-Pinto, L.F. de França Cardozo, C. Costa, J.E. Barboza, and D. Mafra. 2015. Effect of acute intradialytic strength physical exercise on oxidative stress and inflammatory responses in hemodialysis patients. Kidney Research and Clinical Practice 34 (1): 35–40. https://doi.org/10.1016/j.krcp.2015.02.004.

    Article  PubMed  PubMed Central  Google Scholar 

  60. Small, D.M., K.S. Beetham, E.J. Howden, D.R. Briskey, D.W. Johnson, N.M. Isbel, G.C. Gobe, and J.S. Coombes. 2017. Effects of exercise and lifestyle intervention on oxidative stress in chronic kidney disease. Redox Report 22 (3): 127–136. https://doi.org/10.1080/13510002.2016.1276314.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  61. Barančík, M., L. Grešová, M. Barteková, and I. Dovinová. 2016. Nrf2 as a key player of redox regulation in cardiovascular diseases. Physiology Research 65 (Suppl 1):S1-S10. https://doi.org/10.33549/physiolres.933403.

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Funding

This research was supported by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, Grant 88882.447369/2019–01) and Fundação de Amparo à Pesquisa e Inovação do Estado de Santa Catarina (FAPESC, Grant PAP-2019TR715). JAF laboratory is supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (Grant 306082/2014–4) and CAPES (Grant 1966/2016).

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D. M. P. M., G. H. C. M., K. C. B., and D. C. H. K.: study design; data collection, analysis and interpretation of data, and manuscript writing. T. C. G., M. G. L., M. B., B. S.: data collection and analysis. M. S. G. and D. S. C. V.: data analysis. J. A. F., A. R. S. S., L. D., and D. C. H. K.: technical support and supervision of the project. All authors have approved the final version of the article and agree to provide all clarifications to ensure the completeness and accuracy of the research.

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Correspondence to Deborah de Camargo Hizume Kunzler.

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This study was approved by the Ethics Committee on Animals Use (CEUA) at Universidade do Estado de Santa Catarina (Protocol number 2306201018) and Universidade Federal de Santa Catarina (Protocol number 9256210519).

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Moecke, D.M.P., Martins, G.H.C., Garlet, T.C. et al. Aerobic Exercise Attenuates Kidney Injury, Improves Physical Performance, and Increases Antioxidant Defenses in Lungs of Adenine-Induced Chronic Kidney Disease Mice. Inflammation (2022). https://doi.org/10.1007/s10753-022-01643-y

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KEY WORDS

  • renal failure
  • physical exercise
  • lung inflammation
  • oxidative damage
  • antioxidant enzymes