SWIMMING EXERCISE STIMULATES NEUROGENESIS IN THE SUBVENTRICULAR ZONE VIA INCREASE IN SYNAPSIN I AND NERVE GROWTH FACTOR LEVELS
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In this study, we investigated the effects of 8-weeks of swimming exercise on neurogenesis in the subventricular zone (SVZ) and on the levels of nerve growth factor (NGF) and synapsin I protein in the olfactory bulb (OB) of adult rats at a series of relevant time points (2 days, 1 week, 2 weeks, 4 weeks, 3 months, and 6 months). Ninety-six male Sprague Dawley rats were divided into 2 groups: (1) a control group (COG; n = 48, n = 8 for each time point) and (2) a swimming exercise group (SEG; total n = 48; n = 8 for each time point). SEG performed swimming exercise for 5 days per week over a period of 8 weeks. We found that the number of 5-bromo-2'-deoxyuridine-5'-monophosphate (BrdU)- and doublecortin (DCX)-positive cells was significantly higher in SEG than in COG at all time points (Day 2, Week 1, Week 2, Week 4, Month 3, and Month 6; p < 0.001). Furthermore, NGF and synapsin I protein levels were significantly higher in SEG on Day 2, and Weeks 1, 2, and 4 than in COG (p < 0.05 for each time point). Our findings suggest that regular swimming exercise in adult rats increases neurogenesis, neuronal survival, and neuronal maintenance in the SVZ; furthermore, swimming exercise increases the levels of NGF and synapsin I in the OB.
- 1. Alvarez–Buylla A, Garcia–Verdugo J. Neurogenesis in adult subventricular zone J Neurosci. 2002;22:629–634.
- 2. Carleton A, Petreanu LT, Lansford R, Alvarez–Buylla A, Lledo PM Becoming a new neuron in the adult olfactory bulb. Nat Neurosci. 2003;6:507–518
- 3. Song H, Stevens C, Gage F. Neural stem cells from adult hippocampus develop essential properties of functional CNS neurons. Nat Neurosci. 2002;5:438–445.
- 4. Gheusi G, Cremer H, McLean H, Chazal G, Vincent JD, Lledo PM Importance of newly generated neurons in the adult olfactory bulb for odor discriminationProc Natl Acad Sci USA. 2000;97:1823–1828
- 5. Dayer AG, Ford AA, Cleaver KM, Yassaee M, Cameron HA. Short-term and long-term survival of new neurons in the rat dentate gyrus. J Comp Neurol. 2003;460:563–572
- 6. Winner B, Cooper–Kuhn CM, Aigner R, Winkler J, Kuhn HG. Long-term survival and cell death of newly generated neurons in the adult rat olfactory bulb. Eur J Neurosci. 2002;16:1681–1689.
- 7. Brunjes PC. Unilateral naris closure and olfactory system development. Brain Res Brain Rev. 1994;19:146–160.
- 8. Cummings DM, Brunjes PC. The effects of variable periods of functional deprivation on olfactory bulb development in rats. Exp Neurol. 1997;148:360–366.
- 9. Corotto FS, Henegar JR, Maruniak JA. Odor deprivation leads to reduced neurogenesis and reduced neuronal survival in the olfactory bulb of the adult mouse. Neurosci. 1994;61:739–744.
- 10. Petreanu L, Alvarez-Buylla A.Maturation and death of adult-born olfactory bulb granule neurons:role of olfaction. J Neurosci. 2002;22:6106–6113.
- 11. Yamashita T, Tucker KL, Barde YA. Neurotrophin binding to the p 75 receptor modulates Rho activity and axonal outgrowth. Neuron. 1999;24:585–593.
- 12. Mobley WC, Rutkowski JL, Tennekoon GI, Buchanan K, Johnston MV. Choline acetyltransferase activity in stratum of neonatal rats increased by nerve growth factor. Science1985;229:284–287.
- 13. Cheng B, Mattson MP. NGF and bFGF protect rat hippocampal and human cortical neurons against hypoglycemic damage by stabilizing calcium homeostasis Neuron. 1991;7:1031– 1041.
- 14. Cheng B, Mattson MP. Glucose deprivation elicits neurofibrillary tangle-like antigenic change in hippocampal neurons:prevention by NGF and bFGF. Exp Neurol. 1992;117:114–123.
- 15. Nistico G, Ciriolo MR, Fiskin K, Iannone M, De MA, Rotilio G. NGF restores decrease in catalase activity and increases superoxide dismutase and glutathione peroxidase activity in the brain of aged rats. Free Radic Biol Med. 1992;12:1771–1781.
- 16. Radak Z, Kanebo T, Tahara S, Nakamoto H, Pucsok J, Sasvari M, Nyakas C, Goto S.Regular exercise improves cognitive function and decreases oxidative damage in rat brain. Neurochem Int. 2001;38:17–23
- 17. Uysal N, Tugyan K, Kayatekin BM, Acikgoz O, Bagriyanik HA, Gonenc S, Ozdemir D, Aksu I, Topcu A, Semin I.The effects of regular aerobic exercise in adolescent period on hippocampal neuron density, apoptosis and spatial memory Neurosci Letter. 2005;383:241–245.
- 18. Radak Z, Toldy A, Szabo Z, Siamilis S, Nyakas C, Silye G, Jakus J, Goto S.The effects of training and detraining on memory, neurotrophins and oxidative stress markers in rat brain. Neurochem Int. 2006;49:387–392.
- 19. Lee HC, Hong YP, Kim HT. Effects of exercise on nerve growth factor levels and neurogenesis, and cognitive function in the hippocampal dentate gyrus of adult rats. Kor J Sport2013;11:287– 299.
- 20. Kuhn HG, Dickinson-Anson H, Gage FH. Neurogenesis in the dentate gyrus of adult rat:age-related decrease of neuronal progenitor proliferation J Neurosci. 1996;16:2027–2033.
- 21. Ventura RE, Goldman JE. Dorsal radial glia generate olfactory bulb interneurons in the postnatal murine brain. J Neurosci2007;27:4297–4302.
- 22. Arvidsson A, Collin T, Kirik D, Kokaia Z, Lindvall O.Neuronal replacement from endogenous precursors in the adult brain after stroke Nature Med. 2002;8:963– 970.
- 23. Curtis MA, Penney EB, Pearson AG, van Roon-Mon WMC, Butterworth NJ, Dragunow M, Connor B, Faull RLM. Increased cell proliferation and neurogenesis in the adult human Huntington’s disease brain. Proc Natl Acad Sci USA. 2003;100:9023–9027.
- 24. van Praag H, Kempermann G, Gage FH. Running increase cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci. 1999;2:203–205.
- 25. Yasuhara T, Hara K, Maki M, Matsukawa N, Fujino H, Date I, Borlongan CV. Lack of exercise, via hindlimb suspension, impedes endogenous neurogenesis Neurosci. 2007;149:182–191.
- 26. Hicks AU, Hewlett K, Windle V, Chernenko G, Ploughman M, Jolkkonen J, Weiss S, Corbett D.Enriched environment enhances transplanted subventricular zone stem cell migration and functional recovery after stroke Neurosci. 2007;146:31–40.
- 27. Jizi J, Kang HM, Park C.Voluntary exercise enhances survival and migration of neural progenitor cells after intracerebral haemorrhage in mice. Brain Injury. 2010;8:533–540.
- 28. Enwere E, Shingo T, Gregg C, Fujikawa H, Ohta S, Weiss S.Aging results in reduced epidermal growth factor receptor signaling, diminished olfactory neurogenesis, and deficits in fine olfactory discrimination. J Neurosci. 2004;24:8354–8365.
- 29. Brown J, Cooper-Kuhn CM, Kempermann G, van Praag H, Winkler J, Gage FH, Kuhn HG. Enriched environment and physical activity stimulate hippocampal but not olfactory bulb neurogenesis. Eur J Neurosci. 2003;17:2042–2046.
- 30. Jin K, Sun Y, Xie L, Batteur S, Mao XO, Smelick C, Logvinova A, Greenberg DA. Neurogenesis and aging: FGF-2 and HB-EGF restore neurogenesis in hippocampus and subventricular zone of aged mice. Aging Cell. 2003;2:175– 183.
- 31. Chae CH, Kim HT. Forced, moderate- intensity treadmill exercise suppresses apoptosis by increasing the level of NGF and stimulating phosphatidylinositol 3-kinase signaling in the hippocampus of aging rats. Neurochem Int. 2009;55:208–213.
- 32. Li L, Chin LS, Shupliakov O, Brodin L, Sihra TS, Hvalby O, Jensen V, Zheng D, McNamara JO, Greengard P, Anderson P.Impairment of synaptic vesicle clustering and of synaptic transmission, and increased seizure propensity in synapsin I-deficient miceProc Natl Acad Sci USA. 1995;92:9235–9239.
- 33. Takei Y, Harada A, Takeda S, Kobayashi K, Terada S, Noda T, Taka Hirokawa N.Synapsin I deficiency results in the structural change in the presynaptic terminals in the murine nervous system. J Cell Biol1995;131:1789–1800.
- 34. Vaynman S, Ying Z, Gomez-Pinilla F.Exercise induces BDNF and synapsin I to specific hippocampal subfields. J Neurosci Res. 2004;76:356–362.
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