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l-Glutamine and Physical Exercise Prevent Intestinal Inflammation and Oxidative Stress Without Improving Gastric Dysmotility in Rats with Ulcerative Colitis

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Abstract

The aim of this study was to evaluate the effects of glutamine supplementation or exercise on gastric emptying and intestinal inflammation in rats with ulcerative colitis (UC). Strength exercise consisted of jump training 4 × 10 repetitions/5 days a week/8 weeks with progressive overload. Endurance exercise consisted of swimming without overload for a period of 1 h a day/5 days a week/8 weeks. Another group (sedentary) of animals was supplemented with l-glutamine (1 g/kg of body weight) orally for 8 weeks before induction of UC. Colitis was induced by intra-colonic administration of 1 mL of 4% acetic acid. We assessed gastric emptying, macroscopic and microscopic scoring, oxidative stress markers, and IL-1β, IL-6, and (TNF-α) levels. The UC significantly increased (p < 0.05) the gastric emptying compared with the saline control group. We observed a significantly decrease (p < 0.05) in body weight gain in UC rats compared with the control groups. Both exercise interventions and l-glutamine supplementation significantly prevented (p < 0.05) weight loss compared with the UC group. Strength and endurance exercises significantly prevented (p < 0.05) the increase of microscopic scores and oxidative stress (p < 0.05). l-glutamine supplementation in UC rats prevented hemorrhagic damage and improved oxidative stress markers (p < 0.05). Strength and endurance exercises and glutamine decreased the concentrations of inflammatory cytokines IL-1β, IL-6, and TNF-α compared with the UC group (p < 0.05). Strength and endurance exercises and l-glutamine supplementation prevented intestinal inflammation and improved cytokines and oxidative stress levels without altering gastric dysmotility in rats with UC.

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Data Availability

The datasets used and/or analyzed during the current study are available from the corresponding author (MTBS) on reasonable request.

Abbreviations

CNS:

Central nervous system

GLP-1:

Glucagon-like peptide 1

IL:

Interleukin

MDA:

Malondialdehyde

MPO:

Myeloperoxidase

Nox:

Nitrite plus nitrate

NTS:

Nucleus tractus solitarius

SAL:

Saline

SOD:

Superoxide dismutase

TBARS:

Thiobarbituric acid reactive substances

TLRs:

Toll-like receptors

TNBS:

2,4,6-trinitrobenzenesulfonic acid

TNF-α:

Tumor necrosis factor alpha

UC:

Ulcerative colitis

References

  1. Yu, Y.R., and J.R. Rodriguez. 2017. Clinical presentation of Crohn’s, ulcerative colitis, and indeterminate colitis: symptoms, extraintestinal manifestations, and diseases phenotypes. Seminars in Pediatric Surgery 26: 349–355.

    PubMed  Google Scholar 

  2. Ordás, I., L. Eckmann, M. Talamini, D.C. Baumgart, and W.J. Sandborn. 2012. Ulcerative colitis. Lancet. 380: 1606–1619.

    PubMed  Google Scholar 

  3. Victoria, C.R., L.Y. Sassaki, and H.R.C. Nunes. 2009. Incidência e prevalência das doenças inflamatórias intestinais na região centro-oeste do Estado de São Paulo. Arquivos de Gastroenterologia 46 (1): 20–25.

    PubMed  Google Scholar 

  4. Araújo, G.L.S., A.M.S. Telles, F.E.A. Lima, N.T.P. Filho, and M.C.F.P. Machado. 2009. Histological and histochemical analysis of prognostic factors in patients with ulcerative colitis. Revista Brasilera de Coloproctologia 29: 1–8.

    Google Scholar 

  5. Ciesielczyk, K., A. Furgala, L. Dobrek, K. Juszczak, and P. Thor. 2015. Altered sympathovagal balance and pain hypersensitivity in TNBS-induced colitis. Archives of Medical Science 1: 246–255.

    Google Scholar 

  6. Feuerstein, J.D., and A.S. Cheifetz. 2014. Ulcerative colitis: epidemiology, diagnosis, and management. Mayo Clinic Proceedings 89 (11): 1553–1563.

    PubMed  Google Scholar 

  7. Hashash, J.G., and D.G. Binion. 2017. Exercise and inflammatory bowel disease: insights into etiopathogenesis and modification of clinical course. Gastroenterology Clinics of North America 46: 895–905.

    PubMed  Google Scholar 

  8. Jeong, S.Y., Y.N. Im, J.Y. Youm, H.K. Lee, and S.Y. Im. 2018. l-glutamine attenuates DSS-induced colitis via induction of MAPK phosphatase-1. Nutrients 10: 288.

    PubMed Central  Google Scholar 

  9. Cruzat, V., M. Macedo Rogero, K. Noel Keane, R. Curi, and P. Newsholme. 2018. Glutamine: metabolism and immune function, supplementation and clinical translation. Nutrients. 10 (11): 1564.

    PubMed Central  Google Scholar 

  10. Achamrah, N., P. Déchelotte, and M. Coëffier. 2017. Glutamine and the regulation of intestinal permeability: from bench to bedside. Current Opinion in Clinical Nutrition and Metabolic Care 20: 86–91.

    PubMed  CAS  Google Scholar 

  11. Kim, M.H., and H.Y. Kim. 2017. The roles of glutamine in the intestine and its implication in intestinal diseases. International Journal of Molecular Sciences 18 (5): 1051.

    PubMed Central  Google Scholar 

  12. Roggenbuck, C., F. Lammert, H. Berthold, T. Giese, A. Stallmach, et al. 2014. High-dose oral supplementation of antioxidants and glutamine improves the antioxidant status in patients with Crohn’s disease: a pilot study. European Journal of Clinical Nutrition and Metabolism 3 (1): 246–253.

    Google Scholar 

  13. Benjamin, J., G. Makharia, V. Ahuja, K.D. Anand Rajan, M. Kalaivani, S.D. Gupta, and Y.K. Joshi. 2012. Glutamine and whey protein improve intestinal permeability and morphology in patients with Crohn’s disease: a randomized controlled trial. Digestive Diseases and Sciences 57 (4): 1000–1012.

    PubMed  CAS  Google Scholar 

  14. Chen, Q.H., Y. Yang, H.L. He, J.F. Xie, S.X. Cai, et al. 2014. The effect of glutamine therapy on outcomes in critically ill patients: a meta-analysis of randomized controlled trials. Critical Care 18: 2–13.

    Google Scholar 

  15. Pedersen, B.K., and L. Hoffman-Goetz. 2000. Exercise and the immune system: regulation, integration, and adaptation. Physiological Reviews 80 (3): 1055–1081.

    PubMed  CAS  Google Scholar 

  16. Petersen, A.M., and B.K. Pedersen. 2005. The anti-inflammatory effect of exercise. Journal of Applied Physiology (Bethesda, MD: 1985) 98 (4): 1154–1162.

    CAS  Google Scholar 

  17. Souza, A.C., L.C. Magalhães, and L.F. Teixeira-Salmela. 2011. Adaptação transcultural e análise das propriedades psicométricas da versão brasileira do perfil de atividade humana. Cad Saúde Pública. 22 (12): 2623–2636.

    Google Scholar 

  18. Gomarasca, M., G. Banfi, and G. Lombardi. 2020. Myokines: the endocrine coupling of skeletal muscle and bone. Advances in Clinical Chemistry 94: 155–218.

    PubMed  CAS  Google Scholar 

  19. Değer, C., Y. Erbil, M. Giriş, B.T. Yanik, F. Tunca, V. Olgaç, S.D. Abbasoğlu, S. Öztezcan, and G. Toker. 2006. The effect of glutamine on pancreatic damage in TNBS-induced colitis. Digestive Diseases and Sciences 51 (10): 1841–1846.

    PubMed  Google Scholar 

  20. Bilski, J., A. Mazur-Bialy, D. Wojcik, M. Magierowski, M. Surmiak, et al. 2019. Effect of forced physical activity on the severity of experimental colitis in normal weight and obese mice. Involvement of Oxidative Stress and Proinflammatory Biomarkers. Nutrients 11 (5): E1127.

    PubMed  Google Scholar 

  21. Giriş M, Erbil, Y. Doğru-Abbasoğlu, S. Yanik, B.T. Aliş, H. Olgaç, V. Toker, G.A. 2007. The effect of heme oxygenase-1 induction by glutamine on TNBS-induced colitis. The effect of glutamine on TNBS colitis. International Journal of Colorectal Disease 22 (6): 591–599.

  22. Bilski, J., A.I. Mazur-Bialy, B. Brzozowski, M. Magierowski, K. Jasnos, et al. 2015. Moderate exercise training attenuates the severity of experimental rodent colitis: the importance of crosstalk between adipose tissue and skeletal muscles. Mediators of Inflammation 60: 50–71.

    Google Scholar 

  23. Mazur-Bialy, A.I., J. Bilski, D. Wojcik, B. Brzozowski, H. Surmiak, et al. 2017. Beneficial effect of voluntary exercise on experimental colitis in mice fed a high-fat diet: the role of irisin, adiponectin and proinflammatory biomarkers. Nutrients 9 (4): 410.

    PubMed Central  Google Scholar 

  24. Bento-Silva, M.T., M.C.C. Martins, F.L. Torres-Leal, T.L. Barros, I.L.N.F. Carvalho, et al. 2010. Effects of administering testosterone undecanoate in rats subjected to physical exercise: effects on the estrous cycle, motor behavior and morphology of the liver and kidney. Brazilian Journal of Pharmaceutical Sciences 46 (1): 79–89.

    Google Scholar 

  25. Lima, E.B.S., L.C.S. Oliveira, G.S. Cardoso, P.V.N. Telles, L.C. Lima, et al. 2018. Moderate-intensity exercise renin angiotensin system blockade improve the renovascular hypertension (2K1C)-induced gastric dysmotility in rats. Journal Life Sciences 210: 55–64.

    Google Scholar 

  26. Felix, A.C.S., A.C. Gastaldi, S.G.V. Dutra, A.C.S. de Freitas, S.V. Philbois, T. de Paula Facioli, V.J.D. da Silva, T.H. Fares, and H.C.D. de Souza. 2019. Early ovarian hormone deprivation increases cardiac contractility in old female rats-role of physical training. Autonomic Neuroscience 218: 1–9.

    PubMed  CAS  Google Scholar 

  27. Felix, A.C.S., S.G.V. Dutra, A.C. Gastaldi, P.C. Bonfim, S. Vieira, and H.C.D. de Souza. 2018. Physical training promotes similar effects to the blockade of angiotensin-converting enzyme on the cardiac morphology and function in old female rats subjected to premature ovarian failure. Experimental Gerontology 109: 90–98.

    PubMed  CAS  Google Scholar 

  28. Tezini, G.C., D.P. Dias, and H.C. Souza. 2013. Aerobic physical training has little effect on cardiovascular autonomic control in aging rats subjected to early menopause. Experimental Gerontology 48 (2): 147–153.

    PubMed  Google Scholar 

  29. Tezini, G.C., L.C. Silveira, P.G. Villa-Clé Jr., C.P. Jacinto, T.H. Di Sacco, et al. 2009. The effect of aerobic physical training on cardiac autonomic control of rats submitted to ovariectomy. Menopause. 16 (1): 110–116.

    PubMed  Google Scholar 

  30. de Souza, C.F., A.F. Machado, S.J. Bonatto, F.C. Grando, C. Pessini, et al. 2008. Neutrophil response of anaerobic jump trained diabetic rats. European Journal of Applied Physiology 104 (6): 1079–1086.

    PubMed  Google Scholar 

  31. Aguiar, A.F., L.B. Agati, S.S. Mulleer, O.C. Pereira, and M. Dal-Pai-Silva. 2010. Effects of physical training on the mechanical resistance of rat femur proximal thirds. Acta Ortopedica Brasileira 18: 245–249.

    Google Scholar 

  32. Aguiar, A.F., R.W. de Souza, D.H. Aguiar, R.C. Aguiar, I.J. Vechetti Jr., et al. 2011. Creatine does not promote hypertrophy in skeletal muscle in supplemented compared with nonsupplemented rats subjected to a similar workload. Nutrition Research 31 (8): 652–657.

    PubMed  CAS  Google Scholar 

  33. Rogero, M.M., J.O. Tirapegui, R.G. Pedrosa, I.A. Castro, and I.S.O. Pires. 2006. Effect of L-alanyl-L-glutamine supplementation on the plasma and tissue concentrations of glutamine in rats submitted to exhaustive exercise. Nutrition 22: 564–567.

    PubMed  CAS  Google Scholar 

  34. Rogero, M.M., J.O. Tirapegui, R.G. Pedrosa, I.S.O. Pires, and I.A. Castro. 2004. Plasma and tissue glutamine response to acute and chronic supplementation with L-glutamine and L-alanyl-L-glutamine in rats. Nutrition Research 24: 261–270.

    Google Scholar 

  35. Petry, E.R., V.F. Cruzat, T.G. Heck, J.S.M. Leite, P.I. Homem de Bittencourt Jr., and J. Tirapegui. 2014. Alanyl-glutamine and glutamine plus alanine supplements improve skeletal redox status in trained rats: involvement of heat shock protein pathways. Life Sciences 94 (2): 130–136.

    PubMed  CAS  Google Scholar 

  36. Cruzat, V., M. Rogero, and J. Tirapegui. 2010. Effects of supplementation with free glutamine and the dipeptide alanyl-glutamine on parameters of muscle damage and inflammation in rats submitted to prolonged exercise. Cell Biochemistry and Function 28: 24–30.

    PubMed  CAS  Google Scholar 

  37. Cruzat, V., and J. Tirapegui. 2009. Effects of oral supplementation with glutamine and alanyl-glutamine on glutamine, glutamate, and glutathione status in trained rats and subjected to long-duration exercise. Nutrition. 25 (4): 428–435. https://doi.org/10.1016/j.nut.2008.09.014.

    Article  PubMed  CAS  Google Scholar 

  38. Çakir, B., A. Bozkurt, F. Erkan, and B.C. Yegen. 2004. The anti-inflammatory effect of leptin on experimental colitis: involvement of endogenous glucocorticoids. Peptides. 25 (1): 95–104.

    PubMed  Google Scholar 

  39. Kasimay, O., E. Güzel, A. Gemici, A. Abdyli, A. Sulovari, et al. 2006. Colitis-induced oxidative damage of the colon and skeletal muscle is ameliorated by regular exercise in rats: the anxiolytic role of exercise. Experimental Physiology 91 (5): 897–906.

    PubMed  CAS  Google Scholar 

  40. Babitha, S., K. Bindu, T. Nageena, and V.P. Veerapur. 2019. Fresh fruit juice of Opuntia dillenii Haw. Attenuates acetic acid-induced ulcerative colitis in rats. Journal of Dietary Supplements 16 (4): 431–442.

    PubMed  CAS  Google Scholar 

  41. Bell, C.J., D.G. Gall, and J.L. Wallace. 1995. Disruption of colonic electrolyte transport inexperimental colitis. The American Journal of Physiology 268: 622–630.

    Google Scholar 

  42. Mard, S.A., I. Ahmadi, A. Ahangarpour, M.K. Gharib-Naseri, and M. Badavi. 2016. Delayed gastric emptying in diabetic rats caused by decreased expression. Of cystathionine gamma lyase and H2 S synthesis: in vitro and in vivo studies. Neurogastroenterology and Motility 28 (11): 1677–1689.

    PubMed  CAS  Google Scholar 

  43. Brito, T.V., G.J.D. Júnior, J.S.C. Júnior, R.O. Silva, C.E.S. Monteiro, A.X. Franco, D.F.P. Vasconcelos, J.S. Oliveira, D.V.S. Costa, T.B. Carneiro, A.S.G. Duarte, M.H.L.P. Souza, P.M.G. Soares, and A.L.R. Barbosa. 2020. Gabapentin attenuates intestinal inflammation: role of PPAR-gamma receptor. European Journal of Pharmacology 873: 172974. https://doi.org/10.1016/j.ejphar.2020.172974.

    Article  PubMed  CAS  Google Scholar 

  44. Oliveira, G.A.L., C.A. Lastra, M.Á. Rosillo, M.L.C. Martinez, M. Sánchez-Hidalgo, J.V.R. Medeiros, and I. Villegas. 2019. Preventive effect of bergenin against the development of TNBS-induced acute colitis in rats is associated with inflammatory mediators inhibition and NLRP3/ASC inflammasome signaling pathways. Chemico-Biological Interactions 297: 25–33. https://doi.org/10.1016/j.cbi.2018.10.020.

    Article  CAS  Google Scholar 

  45. Brito, T.V., J.P.R.P.N.S. Prudêncio, J.A. Batista, J.S.C.J. Silva, O. Renan, A.X. Franco, K.S. Aragão, P.M.G. Soares, M.H.L.P. Souza, L.S. Chaves, A.L.P. Freitas, J.V.R. Medeiros, and A.L.R. Barbosa. 2014. Ulfated-polysaccharide fraction extracted from red algae Gracilaria birdiae ameliorates trinitrobenzenesulfonic acid-induced colitis in rats. The Journal of Pharmacy and Pharmacology 66 (8): 1161–1170. https://doi.org/10.1111/jphp.12231.

    Article  PubMed  CAS  Google Scholar 

  46. Green, L.C., D.A. Wagner, J. Glogowski, P.L. Skipper, J.S. Wishnok, and S.R. Tannenbaum. 1982. Analysis of nitrate, nitrite, and [15N]nitrate in biological fluids. Analytical Biochemistry 126 (1): 131–138.

    PubMed  CAS  Google Scholar 

  47. Mihara, M., and M. Uchiyama. 1978. Determination of malonaldehyde precursor in tissues by thiobarbituric acid test. Analytical Biochemistry 86 (1): 271–278.

    PubMed  CAS  Google Scholar 

  48. Cunha, F.Q., M.A. Boukili, J.I. Motta, B.B. Vargaftig, and S.H. Ferreira. 1993. Blockade by fenspiride of endotoxin-induced neutrophil migration in the rat. European Journal of Pharmacology 238 (1): 47–52.

    PubMed  CAS  Google Scholar 

  49. Bradley, P.P., R.D. Christensen, and G. Rothstein. 1982. Cellular and extracellular myeloperoxidase in pyogenic inflammation. Blood. 60 (3): 618–622.

    PubMed  CAS  Google Scholar 

  50. De Schepper, H.U., J.G. De Man, L. Van Nassauw, J.P. Timmermans, A.G. Herman, et al. 2007. Acute distal colitis impairs gastric emptying in rats via an extrinsic neuronal reflex pathway involving the pelvic nerve. Gut 56 (2): 195–202.

    PubMed  Google Scholar 

  51. Keller, J., C. Beglinger, J.J. Holst, V. Andresen, and P. Layer. 2009. Mechanisms of gastric emptying disturbances in chronic and acute inflammation of the distal gastrointestinal tract. American Journal of Physiology. Gastrointestinal and Liver Physiology 297 (5): G861–G868.

    PubMed  CAS  Google Scholar 

  52. Keller, J., U. Binnewies, M. Rösch, J. Juul Holst, C. Beglinger, V. Andresen, and P. Layer. 2015. Gastric emptying and disease activity in inflammatory bowel disease. European Journal of Clinical Investigation 45 (12): 1234–1242.

    PubMed  CAS  Google Scholar 

  53. Jung, J.Y., J.B. Jeong, J.W. Kim, S.H. Kim, S.J. Koh, B.G. Kim, and K.L. Lee. 2015. Circulating ghrelin levels and obestatin/ghrelin ratio as a marker of activity in ulcerative colitis. Intestinal Research 13 (1): 68–73.

    PubMed  PubMed Central  Google Scholar 

  54. Matsuzaki, J., H. Suzuki, T. Masaoka, K. Tanaka, H. Mori, and T. Kanai. 2016. Influence of regular exercise on gastric emptying in healthy men: a pilot study. Journal of Clinical Biochemistry and Nutrition 59 (2): 130–133.

    PubMed  PubMed Central  CAS  Google Scholar 

  55. Hellström, P.M., P. Grybäck, and H. Jacobsson. 2006. The physiology of gastric emptying. Best Practice & Research. Clinical Anaesthesiology 20 (3): 397–407.

    Google Scholar 

  56. Parkman, H.P., and M.P. Jones. 2009. Tests of gastric neuromuscular function. Gastroenterology. 136 (5): 1526–1543.

    PubMed  Google Scholar 

  57. Meerveld, B.G., A.C. Johnson, and D. Grundy. 2017. Gastrointestinal physiology and function. Handbook of Experimental Pharmacology 239: 1–16.

    Google Scholar 

  58. Travagli, R.A., and L. Anselmi. 2016. Vagal neurocircuitry and its influence on gastric motility. Nature Reviews. Gastroenterology & Hepatology 13 (7): 389–401.

    CAS  Google Scholar 

  59. Goyal, R.K., Y. Guo, and H. Mashimo. 2019. Advances in the physiology of gastric emptying. Neurogastroenterology and Motility 31 (4): e13546.

    PubMed  PubMed Central  Google Scholar 

  60. Bonaz, B.L., and C.N. Bernstein. 2013. Brain-gut interactions in inflammatory bowel disease. Gastroenterology. 144 (1): 36–49.

    PubMed  Google Scholar 

  61. Swain, M.G., P.A. Blennerhassett, and S.M. Collins. 1991. Impaired sympathetic nerve function in the inflamed rat intestine. Gastroenterology. 100 (3): 675–682.

    PubMed  CAS  Google Scholar 

  62. Aube, A.C., C. Cherbut, M. Barbier, J.H. Xing, C. Roze, et al. 1999. Altered myoelectrical activity in noninflamed ileum of rats with colitis induced by trinitrobenzene sulphonic acid. Neurogastroenterology and Motility 11 (1): 55–62.

    PubMed  CAS  Google Scholar 

  63. Jacobson, K., K. McHugh, and S.M. Collins. 1995. Experimental colitis alters myenteric nerve function at inflamed and noninflamed sites in the rat. Gastroenterology. 109 (3): 718–722.

    PubMed  CAS  Google Scholar 

  64. Mourad, F.H., K.A. Barada, N.A. Bou Rached, C.I. Khoury, N.E. Saadé, and C.F. Nassar. 2006. Inhibitory effect of experimental colitis on fluid absorption in rat jejunum: role of the enteric nervous system, VIP, and nitric oxide. American Journal of Physiology. Gastrointestinal and Liver Physiology 290 (2): G262–G268.

    PubMed  CAS  Google Scholar 

  65. da Silva, M.V., A.R. Marosti, C.E. Mendes, K. Palombit, and P. Castelucci. 2015. Differential effects of experimental ulcerative colitis on P2X7 receptor expression in enteric neurons. Histochemistry and Cell Biology 143 (2): 171–184.

    PubMed  Google Scholar 

  66. Macpherson, B.R., and C.J. Pfeiffer. 1978. Experimental production of diffuse colitis in rats. Digestion. 17 (2): 35–150.

    Google Scholar 

  67. Evans, G.H., P. Watson, S.M. Shirreffs, and R.J. Maughan. 2016. Effect of exercise intensity on subsequent gastric emptying rate in humans. International Journal of Sport Nutrition and Exercise Metabolism 26: 128–134.

    PubMed  Google Scholar 

  68. Horner, K.M., M.M. Schubert, B. Desbrow, N.M. Byrne, and N.A. King. 2015. Acute exercise and gastric emptying: a meta-analysis and implications for appetite control. Sports Medicine 45: 659–678.

    PubMed  Google Scholar 

  69. Ikeo, K., T. Oshima, H. Sei, T. Kondo, H. Fukui, J. Watari, and H. Miwa. 2017. Acotiamide improves stress-induced impaired gastric accommodation. Neurogastroenterology and Motility 29: e12991.

    Google Scholar 

  70. Cavalcante, A.K.M., R.C.L. Siqueira, V.N. Feitosa, C.R. Andrade, A.A. Santos, et al. 2018. Acute exercise inhibits gastric emptying of liquids in rats: influence of the NO-cGMP pathway. Brazilian Journal of Medical and Biological Research 51 (11): e7541.

    PubMed  PubMed Central  CAS  Google Scholar 

  71. Costa, R.J.S., R.M.J. Snipe, C.M. Kitic, and P.R. Gibson. 2017. Systematic review: exercise-induced gastrointestinal syndrome-implications for health and intestinal disease. Alimentary Pharmacology & Therapeutics 46 (3): 246–265.

    CAS  Google Scholar 

  72. Uchida, M., O. Kobayashi, and C. Saito. 2017. Correlation between gastric emptying and gastric adaptive relaxation influenced by amino acids. Journal of Neurogastroenterology and Motility 23: 400–408.

    PubMed  PubMed Central  Google Scholar 

  73. Gu, P., L. Zhu, Y. Liu, L. Zhang, J. Liu, and H. Shen. 2017. Protective effects of paeoniflorin on TNBS-induced ulcerative colitis through inhibiting NF-kappaB pathway and apoptosis in mice. International Immunopharmacology 50: 152–160.

    PubMed  CAS  Google Scholar 

  74. Ghasemi-Pirbaluti, M., E. Motaghi, A. Najafi, and M.J. Hosseini. 2017. The effect of theophylline on acetic acid induced ulcerative colitis in rats. Biomedicine & Pharmacotherapy 90: 153–159.

    CAS  Google Scholar 

  75. Liu, W.X., F. Zhou, Y. Wang, T. Wang, J.W. Xing, S. Zhang, L.X. Sang, S.Z. Gu, and H.L. Wang. 2015. Voluntary exercise protects against ulcerative colitis by up-regulating glucocorticoid-mediated PPAR-γ activity in the colon in mice. Acta Physiologica (Oxford, England) 215 (1): 24–36.

    CAS  Google Scholar 

  76. Lacey, J.M., and D.W. Wilmore. 1990. Is glutamine a conditionally essential amino acid? Nutrition Reviews 48 (8): 297–309.

    PubMed  CAS  Google Scholar 

  77. Neu, J., W.A. Mihatsch, J. Zegarra, S. Supapannachart, Z.Y. Ding, and T. Murguía-Peniche. 2013. Intestinal mucosal defense system, Part 1. Consensus recommendations for immunonutrients. The Journal of Pediatrics 162 (3 Suppl): 56–63.

    Google Scholar 

  78. Bilski, J., A. Mazur-Bialy, B. Brzozowski, M. Magierowski, J. Zahradnik-Bilska, D. Wójcik, K. Magierowska, S. Kwiecien, T. Mach, and T. Brzozowski. 2016. Can exercise affect the course of inflammatory bowel disease? Experimental and clinical evidence. Pharmacological Reports 68 (4): 827–836.

    PubMed  Google Scholar 

  79. Filmann, H., N.A. Kretzmann, B. San-Miguel, S. Llesuy, N. Marroni, et al. 2007. Glutamine inhibits over-expression of pro-inflammatory genes and down-regulates the nuclear factor kappaB pathway in an experimental model of colitis in the rat. Toxicology. 236: 217–226.

    Google Scholar 

  80. Crespo, I., B. San-Miguel, C. Prause, N. Marroni, M.J. Cuevas, et al. 2012. Glutamine treatment attenuates endoplasmic reticulum stress and apoptosis in TNBS-induced colitis. PLoS One 7 (11): 312–322.

    Google Scholar 

  81. Fatani, A.J., K.A. Hosaini, M.M. Ahmed, H.M. Abuohashish, M.Y. Parmar, et al. 2015. Carvedilol attenuates inflammatory biomarkers and oxidative stress in a rat model of ulcerative colitis. Drug Development Research 76 (4): 204–214.

    PubMed  CAS  Google Scholar 

  82. Behera, J.P., B. Mohanty, Y.R. Ramani, B. Rath, and S. Pradhan. 2012. Effect of aqueous extract of Aegle marmelos unripe fruit on inflammatory bowel disease. Indian Journal of Pharmacology 44 (5): 614–618.

    PubMed  PubMed Central  Google Scholar 

  83. Powers, S.K., and M.J. Jackson. 2008. Exercise-induced oxidative stress: cellular mechanisms and impact on muscle force production. Physiological Reviews 88 (4): 1243–1276.

    PubMed  PubMed Central  CAS  Google Scholar 

  84. Lambertucci, R.H., A.C. Levada-Pires, L.V. Rossoni, R. Curi, and T.C. Pithon-Curi. 2007. Effects of aerobic exercise training on antioxidant enzyme activities and mRNA levels in soleus muscle from young and aged rats. Mechanisms of Ageing and Development 128: 267–275.

    PubMed  CAS  Google Scholar 

  85. Hellsten, Y., F.S. Apple, and B. Sjodin. 1996. Effect of sprint cycle training on activities of antioxidant enzymes in human skeletal muscle. Journal of Applied Physiology 81: 1484–1487.

    PubMed  CAS  Google Scholar 

  86. Alessio, H.M., and A.H. Goldfarb. 1988. Lipid peroxidation and scavenger enzymes during exercise: adaptive response to training. Journal of Applied Physiology 64: 1333–1336.

    PubMed  CAS  Google Scholar 

  87. Lawler, J.M., H.B. Kwak, W. Song, and J.L. Parker. 2006. Exercise training reverses downregulation of HSP70 and antioxidant enzymes in porcine skeletal muscle after chronic coronary artery occlusion. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 291: R1756–R1763.

    PubMed  CAS  Google Scholar 

  88. Oh-ishi, S., T. Kizaki, J. Nagasawa, T. Izawa, T. Komabayashi, N. Nagata, K. Suzuki, N. Taniguchi, and H. Ohno. 1997. Effects of endurance training on superoxide dismutase activity, content and mRNA expression in rat muscle. Clinical and Experimental Pharmacology & Physiology 24: 326–332.

    CAS  Google Scholar 

  89. Higuchi, M., L.J. Cartier, M. Chen, and J.O. Holloszy. 1985. Superoxide dismutase and catalase in skeletal muscle: adaptive response to exercise. Journal of Gerontology 40: 281–286.

    PubMed  CAS  Google Scholar 

  90. Belviranlı, M., and N. Okudan. 2018. Effect of coenzyme Q10 alone and in combination with exercise training on oxidative stress biomarkers in rats. International Journal for Vitamin and Nutrition Research 88 (3-4): 126–136.

    PubMed  Google Scholar 

  91. Chang, S.P., Y.H. Chen, W.C. Chang, I.M. Liu, and J.T. Cheng. 2004. Increase of anti-oxidation by exercise in the liver of obese Zucker rats. Clinical and Experimental Pharmacology & Physiology 31 (8): 506–511.

    CAS  Google Scholar 

  92. Qin, L., Z. Yao, Q. Chang, Y. Zhao, N. Liu, X.S. Zhu, Q.Q. Liu, L.F. Wang, A.G. Yang, C.F. Gao, and J.T. Li. 2017. Swimming attenuates inflammation, oxidative stress, and apoptosis in a rat model of dextran sulfate sodium-induced chronic colitis. Oncotarget. 8 (5): 7391–7404.

    PubMed  Google Scholar 

  93. Randhawa, P.K., K. Singh, N. Singh, and A.S. Jaggi. 2012. A review on chemical-induced inflammatory bowel disease models in rodents. The Korean Journal of Physiology & Pharmacology 18 (4): 279–288.

    Google Scholar 

  94. Pedersen, B.K., and B. Saltin. 2006. Evidence for prescribing exercise as therapy in chronic disease. Scandinavian Journal of Medicine & Science in Sports 16: S5–S65.

    Google Scholar 

  95. Suzuki, K., S. Nakaji, M. Yamada, M. Totsuka, K. Sato, and K. Sugawara. 2002. Systemic inflammatory response to exhaustive exercise. Exercise Immunology Review 8: 6–48.

    PubMed  Google Scholar 

  96. Febbraio, M.A., and B.K. Pedersen. 2002. Muscle-derived interleukin-6: mechanisms for activation and possible biological roles. The FASEB Journal 16: 1335–1347.

    PubMed  CAS  Google Scholar 

  97. Steensberg, A. 2003. The role of IL-6 in exercise-induced immune changes and metabolism. Exercise Immunology Review 9: 40–47.

    PubMed  Google Scholar 

  98. Sumi, K., K. Ashida, and K. Nakazato. 2020. Resistance exercise with anti-inflammatory foods attenuates skeletal muscle atrophy induced by chronic inflammation. Journal of Applied Physiology (Bethesda, MD: 1985) 128 (1): 197–211.

    CAS  Google Scholar 

  99. Szpetnar, M., D. Luchowska-Kocot, A. Boguszewska-Czubara, and J. Kurzepa. 2016. The influence of manganese and glutamine intake on antioxidants and neurotransmitter amino acids levels in rats’ brain. Neurochemical Research 41 (8): 2129–2139.

    PubMed  PubMed Central  CAS  Google Scholar 

  100. San-Miguel, B., I. Crespo, N.A. Kretzmann, J.L. Mauriz, N. Marroni, et al. 2010. Glutamine prevents fibrosis development in rats with colitis induced by 2,4,6-trinitrobenzene sulfonic acid. The Journal of Nutrition 140 (6): 1065–1071.

    PubMed  CAS  Google Scholar 

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Authors’ Information

This study was part of a MsC dissertation on Food and Nutrition presented by Dr. Raisa de Oliveira Santos to the Department of Nutrition, Federal University of Piaui, Brazil.

Funding

This work was supported by grants from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Conselho Nacional de Pesquisas (CNPq), and Fundação Cearense de Apoio ao Desenvolvimento Científico e Tecnológico (FUNCAP). In addition, we thank Ajinomoto® of Brazil for donating the l-glutamine used in this study.

Author information

Authors and Affiliations

  1. Graduate Program in Food and Nutrition, Federal University of Piauí, Teresina, PI, Brazil

    Raisa de Oliveira Santos, Juliana Soares Severo & Moisés Tolentino

  2. Laboratory of Exercise and Gastrointestinal Tract – Department of Physical Education, Center for Health Sciences, Federal University of Piauí, Teresina, PI, 64049-550, Brazil

    Geovane da Silva Cardoso, Lara da Costa Lima & Moisés Tolentino

  3. Graduate Program in Pharmacology, Federal University of Piauí, Teresina, PI, Brazil

    Mickael Laudrup de Sousa Cavalcante, Mariana Sousa Silva, Jand Venes Rolim Medeiros & Moisés Tolentino

  4. Department of Physiology and Pharmacology, School of Medicine, Federal University of Ceará, Fortaleza, CE, Brazil

    Ana Karolina Martins Cavalcante, Lívia Maria Soares Nobre, Roberto Cesar Lima-Junior & Armênio Aguiar dos Santos

  5. Graduate Program in Biotechnology, Federal University of Piauí, Parnaiba, PI, Brazil

    Francisca Beatriz de Melo Sousa, Gabriella Pacheco & Even Herlany Pereira Alves

Authors
  1. Raisa de Oliveira Santos
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  2. Geovane da Silva Cardoso
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  3. Lara da Costa Lima
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  7. Juliana Soares Severo
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  11. Lívia Maria Soares Nobre
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  12. Jand Venes Rolim Medeiros
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  13. Roberto Cesar Lima-Junior
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  14. Armênio Aguiar dos Santos
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  15. Moisés Tolentino
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Contributions

ROS, GSC, LCL, MLSC, MSS, AKMC, JSS, FBMS, GP, and LMSN analyzed and interpreted the experimental protocols. JVRM, RCL, and AAS provided some analysis and are majors’ contributors in writing the manuscript. MTBS had supervised the paper and participated in the redaction and the review of the paper. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Moisés Tolentino.

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All treatments and procedures were performed according to ethical standards of the National Council of Animal Experimentation (CONCEA) and were approved by the local ethics committee (Protocol N° 403/17).

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The authors declare that they have no conflicts of interest.

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de Oliveira Santos, R., da Silva Cardoso, G., da Costa Lima, L. et al. l-Glutamine and Physical Exercise Prevent Intestinal Inflammation and Oxidative Stress Without Improving Gastric Dysmotility in Rats with Ulcerative Colitis. Inflammation 44, 617–632 (2021). https://doi.org/10.1007/s10753-020-01361-3

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  • DOI: https://doi.org/10.1007/s10753-020-01361-3

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