The Effect of One-Time and Two-Times Endurance Training with the Same Volume on Glial Cell-Derived Neurotrophic Factor and Nuclear Factor-kB in Sensory Roots of Spinal Cord in Diabetic Neuropathic Rats

Document Type : Research Paper

Authors
Hasan Parsa Shkooh 1
Marziyeh Saghebjoo 2
Samad Nazemi 3
Mehdi Hedayati 4
1 Ph.D. in Exercise Physiology, University of Birjand
2 Associate Professor of Exercise Physiology, University of Birjand
3 Associate Professor of Physiology, Sabzevar University of Medical Sciences
4 Professor of Biochemistry, Cellular and Molecular Endocrine Research Center, Shahid Beheshti University of Medical Sciences
10.22089/spj.2018.4708.1632
Abstract
The Physical activity and exercise training are among the factors that reduce the complications of diabetes including diabetic neuropathy pain. The purpose of this study was to investigate the effect of six weeks endurance training with the same volume on the glial cell-derived neurotrophic factor (GDNF), nuclear factor- KB (NF-KB), and pain in sensoty roots of spinal cord in rats with diabetic neuropathy. The study sample was 40 Wistar rats (10-week-old and weighing 230-260 g). Ten rats were assigned in healthy control group and 30 other rats were diabetic by interperitoneally injection of Sterptozotocin (45 mg/kg, dissolved in citrate buffer, pH=4.5). After creating diabetic neuropathy, rats were randomly assigned to three groups: diabetic one-time training, diabetic two-times training, and diabetic control. Both training protocols were a six weeks aerobic training with 60- 70% VO2max on the treadmill. 48 h after the last training session, the sensory part of spinal cord sampled. Data were analyzed with one-way analysis of variance, Scheffe, Kruskal- Wallis, and Mann- Witney U tests (P<0.05). Results showed; GDNF levels did not have a significant difference between one-time (P = 0.146) and two-times (P = 0.131) training with the neuropathic control group. Also, there was no significant difference in the mean GDNF level between one-time and two-times training groups (P = 0.990). The mean NF-KB level in the one-time training (P = 0.022) and two-times training (P = 0.039) groups was significantly lower than the neuropathy control group, but there was no significant difference between the mean NF-KB level in one-time training and two-times training groups (P = 0.994). The results of pain behavioral tests showed that six weeks of one-time and two-times training significantly reduced neuropathic pain (P = 0.001), while there was no significant difference between the one-time and two-times training groups (P = 0.990). It seems, both one-time and two-times endurance training have a positive effect on NF-KB levels and pain, and reduce the complications of diabetic neuropathy, while not affecting GDNF levels.
Keywords
One-time Endurance Training
Two-times Endurance Training
Diabetic Neuropathy
Glial Cell-Derived Neurotrophic Factor
Nuclear Factor- kB

Main Subjects

  1. Siamilis S, Jakus J, Nyakas C, Costa A, Mihalik B, Falus A, et al. The effect of exercise and oxidant–antioxidant intervention on the levels of neurotrophins and free radicals in spinal cord of rats. Spinal Cord. 2009;47(6):453-57.
  2. Zuccato C, Cattaneo E. Brain-derived neurotrophic factor in neurodegenerative diseases. Nat. Rev. Neurol. 2009;5(6):311-22.
  3. Borzykh A, Kuzmin I, Mart’ianov A, Borovik A, Sharova A, Tarasova O, et al. Changes of rat respiratory and locomotory muscles during aerobic exercise training in continuous and interval regimens. Biophysics. 2012;57(5):684-9.
  4. Xue B, Jiao J, Zhang L, Li K R, Gong Y T, Xie J X, et al. Triptolide upregulates NGF synthesis in rat astrocyte cultures. Neurochem Res. 2007;32(7):1113-9.
  5. Russo-Neustadt A A, Alejandre H, Garcia C, Ivy A S, Chen M J. Hippocampal brain-derived neurotrophic factor expression following treatment with reboxetine, citalopram, and physical exercise. Neuropsychopharmacology. 2004;29(12):2189-99.
  6. Cayo A, Aline D, Ricardo K, Flaviane C, Maria Ida R, Andr, Queirozb T A, et al. Exercise therapy normalizes BDNF upregulation and glial hyperactivity in a mouse model of neuropathic pain. Pain. 2015;156:504-13.
  7. Sally E. Stringer, Margot Mayer-Proschel, Anjali Kalyanii, Mahendra Raoi, and John T. Gallagher. Heparin Is a Unique Marker of Progenitors in the
    Glial Cell Lineage. J. Biol. Chem. 1999, 274:25455-60.
  8. Deschenes MR, Tenny K A, Wilson M H. Increased and decreased activity elicits specific morphological adaptations of the neuromuscular junction. Neuroscience. 2006;137(4):1277-83.
  9. Chae CH, Lee H, Jung S, Kim T, Kim J, Kim N. Swimming exercise increases the level of nerve growth factor and stimulates neurogenesis in adult rat hippocampus. Neuroscience. 2012;212:30-7.
  10. Spielman LJ, Little JP, Klegeris A. Physical activity and exercise attenuate neuroinflammation in neurological diseases. Brain Res Bull. 2016;125:19-29.
  11. Nadi M, Mohammad S, Esfarjani F, Saleki M. The comparison between effects of 12 weeks combined training and vitamin d supplement on improvement of sensory-motor neuropathy in type 2 diabetic women. Biomed Res. 2017;6:55-62.
  12. Zoladz J, Majerczak J, Zeligowska E, Mencel J, Jaskolski A, Jaskolska A, et al. Moderate-intensity interval training increases serum brain-derived neurotrophic factor level and decreases inflammation in Parkinson’s disease patients. J Physiol Pharmacol. 2014;65(3):441-8.
  13. Cooper M A, Kluding P M, Wright D E. Emerging relationships between exercise, sensory nerves, and neuropathic pain. Front. Neurosci. 2016;10-9.
  14. Lee-Kubli C A, Mixcoatl-Zecuatl T, Jolivalt C G, Calcutt N A. Animal models of diabetes-induced neuropathic pain. Behav Neurosci: Springer; 2014.                   p. 147-70.
  15. Kowalski J, Okopien B, Madej A, Makowiecka K, Zielinski M, Kalina Z, et al. Levels of sICAM-1, sVCAM-1 and MCP-1 in patients with hyperlipoproteinemia IIa and-IIb. Int J Clin Pharmacol Ther. 2001;39(2):48-52.
  16. Rajasekar R, Rajasekaran N, Duraisamy G and Kanakasabapathi D. Effect of Alpinia calcarata on glucose uptake in diabetic rats-an in vitro and in vivo model. Journal of Diabetes & Metabolic Disorders. 2014;33(1):1-13.
  17. Shabkhiz F, Ravasi AA, Hassan ZM, Taghikhani M, Razav T. The effect of aerobic continuous and interval training and detraining on some indexes of the cellular immune system in female wistar rats. J. Sports Sci. 2008;1:17-26.
  18. López-Álvarez VM, Mòdol L, Navarro X, Cobianchi S. Early increasing-intensity treadmill exercise reduces neuropathic pain by preventing nociceptor collateral sprouting and disruption of chloride cotransporters homeostasis after peripheral nerve injury. Pain. 2015;156:1812-25.
  19. Boulton AJ, Vinik AI, Arezzo JC, Bril V, Feldman EL, Freeman R, et al. Diabetic neuropathies a statement by the American Diabetes Association. Diabetes care. 2005;28(4):956-62.
  20. Thomas C, Perrey S, Lambert K, Hugon G, Mornet D, Mercier J. Monocarboxylate transporters, blood lactate removal after supramaximal exercise, and fatigue indexes in humans. J Appl Physiol. 2005;98(3):804-9.
  21. Bigdeli Y, Heidarianpour A. Effect of regular exercise and vitamin C on pain threshold in diabetic rats. Arak Medical University Journal. 2012;14(4):10-7.
  22. Prodanov D, Feirabend HK. Morphometric analysis of the fiber populations of the rat sciatic nerve, its spinal roots, and its major branches. J Comp Neurol. 2007;503(1):85-100.
  23. Saavedra A, Baltazar G, Duarte EP. Driving GDNF expression: The green and the red traffic lights. Prog Neurobiol. 2008;86(3):186-215.
  24. Pereira B, Lucas G, da Rocha A, Pauli J, Ropelle E, Cintra D. Eccentric exercise leads to glial activation but not apoptosis in mice spinal cords. Int J Sports Med. 2015;36:378-85.
  25. Gyorkos A, McCullough M, Spitsbergen J. Glial cell line-derived neurotrophic factor (GDNF) expression and NMJ plasticity in skeletal muscle following endurance exercise. Neurosci Biobehav Rev. 2014;257:111-8.
  26. Pierson CR, Zhang W, Murakawa Y, Sima AA. Insulin deficiency rather than hyperglycemia accounts for impaired neurotrophic responses and nerve fiber regeneration in type 1 diabetic neuropathy. J Neuropathol Exp Neurol. 2003;62(3):260-71.
  27. Ying Z, Roy RR, Edgerton R, Gomez-Pinilla F. Voluntary exercise increases neurotrophin-3 and its receptor TrkC in the spinal cord. Brain Res Bull. 2003;987: 93-9.
  28. Ferraiuolo L, De Bono JP, Heath PR, Holden H, Kasher P, Channon KM, et al. Transcriptional response of the neuromuscular system to exercise training and potential implications for ALS. J Neurochem. 2009;109:1714-24.
  29. Engesser-Cesar C, Anderson AJ, Cotman CJ. Wheel running and fluoxetine antidepressant treatment have differential effects in the hippocampus and the spinal cord. Neurosci Biobehav Rev. 2007;144:1033-44.
  30. Molteni R, Zheng JQ, Ying Z, Gomez-Pinilla F, Twiss JL. Voluntary exercise increases axonal regeneration from sensory neurons. Proc Natl Acad Sci. 2004;101:8473-8.
  31. Soya H, Nakamura T, Deocaris CC, Kimpara AI, Fujikawa T, Chang HM. BDNF 20 current neuropharmacology, induction with mild exercise in the rat hippocampus. Biochem Biophys Res Commun. 2007;358(4):961-7.
  32. Aguiar AS, Tuon T, Pinho CA, Silva LA, Andreazza AC, Kapczinski F, et al Intense exercise induces mitochondrial dysfunction in mice brain. Nerochem Res. 2008;33(1):51-8.
  33. Pezet S, McMahon SB. Neurotrophins: Mediators and modulators of pain. Annu Rev Neurosci. 2006;29:507-38.
  34. Murase S, Terazawa E, Hirate K, Yamanaka H, Kanda H, Noguchi K, et al. Upregulated glial cell line-derived neurotrophic factor through cyclooxygenase-2 activation in the muscle is required for mechanical hyperalgesia after exercise in rats. J Physiol Lond. 2013;591(12):3035-48.
  35. Mostarda C, Rogow A, Silva I, De La Fuente R, Jorge L, Rodrigues B. Benefits of exercise training in diabetic rats persist after three weeks of detraining. Auton Neurosci. 2009;145(1):11-6.
  36. Monteiro-Junior R, Cevada T, Oliveira B, Lattari E, Portugal E, Carvalho P, et al. We need to move more: Neurobiological hypotheses of physical exercise as a treatment for Parkinson’s disease. Med Hypotheses. 2015;85(5):537-41.
  37. Weinberg L, Hasni A, Shinohara M, Duarte A. A single bout of resistance exercise can enhance episodic memory performance. Acta Psychol. 2014;13: 153-9.
  38. Zou Y, Tan J, Li N, Yang J, Yu B, Yu J, et al. Do physical exercise and reading reduce the risk of Parkinson’s disease? A cross-sectional study on factors associated with Parkinson’s disease in elderly Chinese veterans. Neuropsychiatr Dis Treat. 215;11:695-700.
  39. Pittenger G, Vinik A. Nerve growth factor and diabetic neuropathy. Exp. Diabetes Res. 2003;4(4):271-85.
  40. Sakamoto T, Watabe K, Ohashi T. Adenoviral vector-mediated GDNF gene transfer prevents death of adult facial motoneurons. NeuroReport. 2000;11:   1857-60.
  41. Bian F, Qi H, Ma P, Zhang L, Yoon KC, Pflugfelder SC, et al. An immunoprotective privilege of corneal epithelial stem cells against Th17 inflammatory stress by producing glial cell-derived neurotrophic factor. Stem Cells . 2010;28(12):2172-81.
Sport Physiology
Volume 11, Issue 43
Fall 2018
October 2019
Pages 75-90

  • Receive Date 29 August 2017
  • Revise Date 04 February 2018
  • Accept Date 13 February 2018