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Effect of 6-week Endurance Training on the Hippocampal Tissue in the Streptozotocin-Induced Diabetic Rats: A Histological Study

Document Type : Original Article

Authors

1 Department of Sport Physiology, Faculty of Sport Sciences, Shahid Chamran University of Ahvaz, Ahvaz, Iran

2 Department of Physical Education, Faculty of Literature and Human Sciences, Lorestan University, Iran

3 Department of Biochemistry and Molecular Biology, Faculty of Veterinary Medicine, Shahid Chamran University of Ahvaz, Ahvaz, Iran

Abstract

Background: Glial cells perform several critical functions and exercise can moderate many of these interventions, so a comprehensive study is needed to elucidate the mechanisms that influence brain function following diabetes and exercise. In this study, the quantitative histological changes of glial in the hippocampus of Streptozotocin (STZ)-induced diabetic rats following endurance training were investigated.
Methods: Twenty-four adult male Wistar Rats (aged 10 weeks with an average weight of 256 ± 11.8 g), were classified into four groups: Diabetic, diabetic trained, untreated control, and trained groups. Diabetes was induced by a single dose intraperitoneal injection of Streptozotocin (45 mg/kg). Then, moderate exercise was performed for 6 weeks (5 sessions in a week). Rats were anesthetized 48 hours after the last training session. Then, they were sacrificed and the hippocampal tissue was removed. Sections (5-6 µ) were prepared and stained with Hematoxylin and Eosin (H & E) staining method.
Results: Histological evaluations showed that the number of astrocyte and oligodendrocyte cells in different hippocampal regions in diabetic rats significantly decreased compared to the untreated control and trained rats. However, the number of microglia cells in diabetic rats was significantly higher than that in the untreated control and trained rats (P ˂ 0.05). In addition, the number of astrocytes and oligodendrocytes significantly increased in the dentate gyrus, Cornu Ammonis, and subiculum of the hippocampal tissue after endurance training compared to the control group, while the number of microglial cells significantly decreased (P < 0.05).
Conclusion: The findings of the present study confirmed the potential effects of moderate exercise on diabetes. Therefore, it seems that physical activity plays an essential role in improving the nervous complications in patients with diabetes.

Keywords

References
  1. Guven A, Yavuz O, Cam M, Comunoglu C, Sevi'nc O. Central nervous system complications of diabetes in streptozotocin-induced diabetic rats: a histopathological and immunohistochemical examination. Int J Neurosci 2009; 119(8):1155-69. doi: 10.1080/00207450902841723.
  2. Samimagham HR, Tamaddondar M, Kazemi jahromi M. The Association between Glycated Hemoglobin and Estimated Glomerular Filtration Rate in Patients with Type 2 Diabetes based on the Hemoglobin Status. Journal of Kerman University of Medical Sciences. 2021;28(1):69-80.
  3. Chen GQ, Mou CY, Yang YQ, Wang S, Zhao ZW. Exercise training has beneficial anti-atrophy effects by inhibiting oxidative stress-induced MuRF1 upregulation in rats with diabetes. Life Sci 2011; 89(1-2):44-9. doi: 10.1016/j.lfs.2011.04.018.
  4. Amin SN, Younan SM, Youssef MF, Rashed LA, Mohamady I. A histological and functional study on hippocampal formation of normal and diabetic rats. F1000Res 2013; 2:151. doi: 10.12688/f1000research.2-151.v1.
  5. Ho N, Sommers MS, Lucki I. Effects of diabetes on hippocampal neurogenesis: links to cognition and depression. Neurosci Biobehav Rev 2013; 37(8):1346-62. doi: 10.1016/j.neubiorev.2013.03.010.
  6. Francis GJ, Martinez JA, Liu WQ, Xu K, Ayer A, Fine J, et al. Intranasal insulin prevents cognitive decline, cerebral atrophy and white matter changes in murine type I diabetic encephalopathy. Brain 2008; 131(Pt 12):3311-34. doi: 10.1093/brain/awn288.
  7. Gajardo-Gómez R, Labra VC, Orellana JA. Connexins and pannexins: new insights into microglial functions and dysfunctions. Front Mol Neurosci 2016; 9:86. doi: 10.3389/fnmol.2016.00086.
  8. de Senna PN, Ilha J, Baptista PP, do Nascimento PS, Leite MC, Paim MF, et al. Effects of physical exercise on spatial memory and astroglial alterations in the hippocampus of diabetic rats. Metab Brain Dis 2011; 26(4):269-79. doi: 10.1007/s11011-011-9262-x.
  9. Ang ET, Tai YK, Lo SQ, Seet R, Soong TW. Neurodegenerative diseases: exercising toward neurogenesis and neuroregeneration. Front Aging Neurosci 2010; 2:25. doi: 10.3389/fnagi.2010.00025.
  10. Verdile G, Fuller SJ, Martins RN. The role of type 2 diabetes in neurodegeneration. Neurobiol Dis 2015; 84:22-38. doi: 10.1016/j.nbd.2015.04.008.
  11. Cotman CW, Berchtold NC, Christie LA. Exercise builds brain health: key roles of growth factor cascades and inflammation. Trends Neurosci 2007; 30(9):464-72. doi: 10.1016/j.tins.2007.06.011.
  12. Farmer J, Zhao X, van Praag H, Wodtke K, Gage FH, Christie BR. Effects of voluntary exercise on synaptic plasticity and gene expression in the dentate gyrus of adult male Sprague-Dawley rats in vivo. Neuroscience 2004; 124(1):71-9. doi: 10.1016/j.neuroscience.2003.09.029.
  13. Yoo DY, Chae J, Jung HY, Yim HS, Kim JW, Nam SM, et al. Treadmill exercise is associated with reduction of reactive microgliosis and pro-inflammatory cytokine levels in the hippocampus of type 2 diabetic rats. Neurol Res 2015; 37(8):732-8. doi: 10.1179/1743132815Y.0000000015.
  14. Li J, Ding YH, Rafols JA, Lai Q, McAllister JP 2nd, Ding Y. Increased astrocyte proliferation in rats after running exercise. Neurosci Lett 2005; 386(3):160-4. doi: 10.1016/j.neulet.2005.06.009.
  15. Beavers KM, Brinkley TE, Nicklas BJ. Effect of exercise training on chronic inflammation. Clin Chim Acta 2010; 411(11-12):785-93. doi: 10.1016/j.cca.2010.02.069. 
  16. Meek TH, Morton GJ. Leptin, diabetes, and the brain. Indian J Endocrinol Metab 2012; 16(Suppl 3):S534-42. doi: 10.4103/2230-8210.105568.
  17. Reagan LP. Insulin signaling effects on memory and mood. Curr Opin Pharmacol 2007; 7(6):633-7. doi: 10.1016/j.coph.2007.10.012.
  18. Ito D, Cao P, Kakihana T, Sato E, Suda C, Muroya Y, et al. Chronic running exercise alleviates early progression of nephropathy with upregulation of nitric oxide synthases and suppression of glycation in zucker diabetic rats. PLoS One 2015; 10(9):e0138037. doi: 10.1371/journal.pone.0138037.
  19. Szkudelski T. The mechanism of alloxan and streptozotocin action in B cells of the rat pancreas. Physiol Res 2001; 50(6):537-46.
  20. Chae CH, Jung SL, An SH, Jung CK, Nam SN, Kim HT. Treadmill exercise suppresses muscle cell apoptosis by increasing nerve growth factor levels and stimulating p-phosphatidylinositol 3-kinase activation in the soleus of diabetic rats. J Physiol Biochem 2011; 67(2):235-41. doi: 10.1007/s13105-010-0068-9.
  21. Labrousse VF, Costes L, Aubert A, Darnaudéry M, Ferreira G, Amédée T, et al. Impaired interleukin-1β and c-Fos expression in the hippocampus is associated with a spatial memory deficit in P2X7 receptor-deficient mice. PLoS One 2009; 4(6):e6006. doi: 10.1371/journal.pone.0006006.
  22. Bancroft JD, Bancroft M. Theory and Practice of Histological Techniques. 6th ed. UK: Churchill Livingstone; 2007.
  23. Cui D, Daley WP, Naftel JP, Haines DE, Lynch JC, Naftel JP, et al. Atlas of Histology: With Functional and Clinical Correlations. USA: Wolters Kluwer Health/Lippincott Williams & Wilkins; 2011.
  24. Mahmoodi MR, Khodabakhshi A. Association between Depression and Food Insecurity in Patients with Diabetes: a cross-sectional study. Journal of Kerman University of Medical Sciences. 2021;28(2):157-66  
  25. Saravia FE, Revsin Y, Gonzalez Deniselle MC, Gonzalez SL, Roig P, Lima A, et al. Increased astrocyte reactivity in the hippocampus of murine models of type 1 diabetes: the nonobese diabetic (NOD) and streptozotocin-treated mice. Brain Res 2002; 957(2):345-53. doi: 10.1016/s0006-8993(02)03675-2.
  26. Radák Z, Sasvári M, Nyakas C, Taylor AW, Ohno H, Nakamoto H, et al. Regular training modulates the accumulation of reactive carbonyl derivatives in mitochondrial and cytosolic fractions of rat skeletal muscle. Arch Biochem Biophys 2000; 383(1):114-8. doi: 10.1006/abbi.2000.2042.
  27. Osborn BA, Daar JT, Laddaga RA, Romano FD, Paulson DJ. Exercise training increases sarcolemmal GLUT-4 protein and mRNA content in diabetic heart. J Appl Physiol (1985) 1997; 82(3):828-34. doi: 10.1152/jappl.1997.82.3.828.
  28. Chen YW, Li YT, Chen YC, Li ZY, Hung CH. Exercise training attenuates neuropathic pain and cytokine expression after chronic constriction injury of rat sciatic nerve. Anesth Analg 2012; 114(6):1330-7. doi: 10.1213/ANE.0b013e31824c4ed4.
  29. Bertram S, Brixius K, Brinkmann C. Exercise for the diabetic brain: how physical training may help prevent dementia and Alzheimer’s disease in T2DM patients. Endocrine 2016; 53(2):350-63. doi: 10.1007/s12020-016-0976-8.
  30. Kim HB, Jang MH, Shin MC, Lim BV, Kim YP, Kim KJ, et al. Treadmill exercise increases cell proliferation in dentate gyrus of rats with streptozotocin-induced diabetes. J Diabetes Complicat 2003; 17(1):29-33. doi: 10.1016/s1056-8727(02)00186-1.
  31. Reisi P, Babri S, Alaei H, Sharifi MR, Mohaddes G, Noorbakhsh SM, et al. Treadmill running improves long-term potentiation (LTP) defects in streptozotocin-induced diabetes at dentate gyrus in rats. Pathophysiology 2010; 17(1):33-8. doi: 10.1016/j.pathophys.2009.06.001.
  32. Gomes da Silva S, Unsain N, Mascó DH, Toscano-Silva M, de Amorim HA, Silva Araújo BH, et al. Early exercise promotes positive hippocampal plasticity and improves spatial memory in the adult life of rats. Hippocampus 2012; 22(2):347-58. doi: 10.1002/hipo.20903.
  33. Stranahan AM, Lee K, Becker KG, Zhang Y, Maudsley S, Martin B, et al. Hippocampal gene expression patterns underlying the enhancement of memory by running in aged mice. Neurobiol Aging 2010; 31(11):1937-49. doi: 10.1016/j.neurobiolaging.2008.10.016.
  34. Alvarez EO, Beauquis J, Revsin Y, Banzan AM, Roig P, De Nicola AF, et al. Cognitive dysfunction and hippocampal changes in experimental type 1 diabetes. Behav Brain Res 2009; 198(1):224-30. doi: 10.1016/j.bbr.2008.11.001.
  35. Tuzcu M, Baydas G. Effect of melatonin and vitamin E on diabetes-induced learning and memory impairment in rats. Eur J Pharmacol 2006; 537(1-3):106-10. doi: 10.1016/j.ejphar.2006.03.024.
  36. Voskuhl RR, Peterson RS, Song B, Ao Y, Morales LB, Tiwari-Woodruff S, et al. Reactive astrocytes form scar-like perivascular barriers to leukocytes during adaptive immune inflammation of the CNS. J Neurosci 2009; 29(37):11511-22. doi: 10.1523/JNEUROSCI.1514-09.2009.
  37. Bachiller S, Jiménez-Ferrer I, Paulus A, Yang Y, Swanberg M, Deierborg T, et al. Microglia in neurological diseases: a road map to brain-disease dependent-inflammatory response. Front Cell Neurosci 2018; 12:488. doi: 10.3389/fncel.2018.00488.
  38. Orellana JA, Martinez AD, Retamal MA. Gap junction channels and hemichannels in the CNS: regulation by signaling molecules. Neuropharmacology 2013; 75:567-82. doi: 10.1016/j.neuropharm.2013.02.020.
  39. Orellana JA, Froger N, Ezan P, Jiang JX, Bennett MV, Naus CC, et al. ATP and glutamate released via astroglial connexin 43 hemichannels mediate neuronal death through activation of pannexin 1 hemichannels. J Neurochem 2011; 118(5):826-40. doi: 10.1111/j.1471-4159.2011.07210.x.
  40. van Dijk G, van Heijningen S, Reijne AC, Nyakas C, van der Zee EA, Eisel UL. Integrative neurobiology of metabolic diseases, neuroinflammation, and neurodegeneration. Front Neurosci 2015; 9:173. doi: 10.3389/fnins.2015.00173.

 

Journal of Kerman University of Medical Sciences
Volume 28, Issue 4
July and August 2021
Pages 347-357
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