Voluntary Exercise Increases Oligodendrogenesis in Spinal Cord

REFERENCES

• Aberg, M. A., Aberg, N. D., Hedbacker, H., Oscarsson, J., &Eriksson, P. S. (2000). Peripheral infusion of IGF-I selectively induces neurogenesis in the adult rat hippocampus. The Journal of Neuroscience, 20(8), 2896–2903.
   PubMed Web of Science ®Google Scholar
• Aberg, M. A., Aberg, N. D., Palmer, T. D., Alborn, A. M., Carlsson-Skwirut, C., Bang, P., (2003). IGF-I has a direct proliferative effect in adult hippocampal progenitor cells. Molecular and Cellular Neurosciences, 24(1), 23–40.
   PubMed Web of Science ®Google Scholar
• Ang, E. T., & Gomez-Pinilla, F. (2007). Potential therapeutic effects of exercise to the brain. Current Medicinal Chemistry, 14(24), 2564–2571.
   PubMed Web of Science ®Google Scholar
• Bansal, R., Magge, S., & Winkler, S. (2003). Specific inhibitor of FGF receptor signaling: FGF-2-mediated effects on proliferation, differentiation, and MAPK activation are inhibited by PD173074 in oligodendrocyte-line-age cells. Journal of Neuroscience Research, 74(4), 486–493.
   Google Scholar
• Baron-Van, E. A., Olichon-Berthe, C., Kowalski, A., Visciano, G., & Van Obberghen, E. (1991). Expression of IGF-I and insulin receptor genes in the rat central nervous system: A developmental, regional and cellular analysis. Journal of Neuroscience Research, 28(2), 244–253.
   Google Scholar
• Biebl, M., Copper, C. M., Winkler, J., & Kuhn, H. G. (2000). Analysis of neurogenesis and programmed cell death reveals a self-renewing capacity in the adult rat brain. Neuroscience Letters, 291(1), 333–340.
   Google Scholar
• Calver, A. R., Hall, A. C., Yu, W. P., Walsh, F. S., Heath, J. K.,Betsholtz, C., (1998). Oligodendrocyte population dynamics and the role of PDGF in vivo. Neuron, 20(5), 869–882.
   Google Scholar
• Carro, E., Nunez, A., Busiguina, S., & Torres-Aleman, I. (2000). Circulating insulin-like growth factor I mediates effects of exercise on the brain. The Journal of Neuroscience, 20(8), 2926–2933.
   PubMed Web of Science ®Google Scholar
• Carro, E., Trejo, J. L., Busiguina, S., & Torres-Aleman, I. (2001). Circulation insulin-like growth factor I mediates the protective effects of physical exercise against brain insults of different etiology and anatomy. The Journal of Neuroscience, 21(15), 5678–5684.
   PubMed Web of Science ®Google Scholar
• Carson, M. J., Behiringer, R. R., Brinster, R. L., & McMorris, F. A. (1993). Insulin-like growth factor I increases brain growth and central nervous system myelination in transgenic mice. Neuron, 10(4), 729–740.
   Google Scholar
• Cotman, C. W., & Gerchtold, N. C. (2002). Exercise: A behavioral intervention to enhance brain health and plasticity. Trends in Neurosciences, 25(6), 295–301.
   PubMed Web of Science ®Google Scholar
• Craig, C. G., Tropepe, V., Morshead, C. M., Reynolds, B. A., Weiss, S., & Van Der Kooy, D. (1996). In vivo growth factor expansion of endogenous subependymal neural precursor cell populations in the adult mouse brain. The Journal of Neuroscience, 16(8), 2649–2658.
   Google Scholar
• de Castro, F., & Brian, A. (2005). The molecular orchestra of the migration of oligodendrocyte precursors during development. Journal of Brain Research Reviews, 49(2), 227–241.
   Google Scholar
• Ding, Y. H., Luan, X., Li, J., Rafols, J. A., Guthikonda, M., Diaz, F. G., (2004). Exercise-induced overexpression of angiogenic factors and reduction of ischemia/repercussion injury in stroke. Current Neurovascular Research, 1(5), 411–420.
   PubMed Web of Science ®Google Scholar
• Droste, S. K., Gesing, A., Ulbricht, S., Muller, M. B., Linthorst, A. C., & Teul, J. M. (2003). Effects of long-term voluntary exercise on the mouse hypothalamic-pituitary-adrenocortical axis. Endocrinology, 144(7), 3012–3023.
   PubMed Web of Science ®Google Scholar
• Dunn, A. L., Reigle, T. G., Youngstedt, S. D., Armstrong, R. B., & Dishman, R. K. (1996). Brain norepinephrine and metabolites after treadmill training and wheel running in rats. Medicine and Science in Sports and Exercise, 28(2), 204–209.
   Google Scholar
• Engesser-Cesar, C., Anderson, A. J., & Cotman, C. W. (2007). Wheel running and fluoxetine antidepressant treatment have differential effects in the hippocampus and the spinal cord. Neuroscience, 144(3), 1033–1044.
   Google Scholar
• Espinosa-Jeffrey, A., Zhao, P., Awosika, W., Wo, N., Macias, F., Cepeda, C., (2006). Activation, proliferation and commitment of endogenous stem/progenitor cells to the oligodendrocyte lineage by TS1 in a rat model of dysmyelination. Developmental Neuroscience, 28(6), 488–498.
   Google Scholar
• Filippov, V., Kronenberg, G., Pivneva, T., Reuter, K., Steiner, B., Wang, L. P., (2003). Subpopulation of nestin-expressing progenitor cells in the adult murine hippocampus shows electrophysiological and morphological characteristics of astrocytes. Molecular and Cellular Neurosciences, 23(3), 373–82.
   PubMed Web of Science ®Google Scholar
• Fruttiger, M., Karlsson, L., Hall, A. C., Abramsson, A., Calver, A. R., Bostrom, H., (1999). Defective oligodendrocyte development and severe hypomyelination in PDGF-A knockout mice. Development, 126(3), 457–467.
   Google Scholar
• Ghiani, C. A., Ying, Z., de Vellis, J., & Gomez-Pinilla, F. (2007). Exercise decreases myelin-associated glycoprotein expression in the spinal cord and positively modulates neuronal growth. Glia, 55(9), 966–975.
   PubMed Web of Science ®Google Scholar
• Gibney, S. M., & McDermott, K. W. (2007). Differentiation of oligodendrocytes in neurospheres derived from embryonic rat brain using growth and differentiation factors. Journal of Neuroscience Research, 85(9), 1912–1920.
   Google Scholar
• Gomez-Pinilla, F., Daw, L., & So, V. (1997). Physical exercise induces FGF-2 and its mRNA in the hippocampus. Brain Research, 764(1–2), 1–8.
   Google Scholar
• Gomez-Pinilla, F., Huie, J. R., Ying, Z., Ferguson, A. R., Crown, E. D., Baumbauer, K. M., (2007). BDNF and learning: Evidence that instrumental training promotes learning within the spinal cord by up-regulating BDNF expression. Neuroscience, 148(4), 893–906.
   PubMed Web of Science ®Google Scholar
• Gomez-Pinilla, F., Ying, Z., Opaza, P., Roy, R. R., & Edgerton, V. R. (2001). Differential regulation by exercise of BDNF and NT-3 in rat spinal cord and skeletal muscle. The European Journal of Neuroscience, 13(6), 1078–1084.
   PubMed Web of Science ®Google Scholar
• Gomez-Pinilla, F., Ying, Z., Roy, R. R., Molteni, R., & Edgerton, V. R. (2002). Voluntary exercise induces a BDNF-mediated mechanism that promotes neuroplasticity. Journal of Neurophysiology, 88(5), 2187–2195.
   PubMed Web of Science ®Google Scholar
• Horner, P. J., Power, A. E., Kempermann, G., Kuhn, H. G., Palmer, T. D., Winkler, J., (2000). Proliferation and differentiation of progenitor cells throughout the intact adult rat spinal cord. The Journal of Neuroscience, 20(6), 2218–2228.
   PubMed Web of Science ®Google Scholar
• Hsieh, J., Bimone, J. B., Kaspar, B. K., Kuwabara, T., Nakashima, K., & Gage, F. H. (2004). IGF-I instructs multipotent adult neural progenitor cells to become oligodendrocytes. The Journal of Cell Biology, 164(1), 111–122.
   Google Scholar
• Jin, K., Zhu, Y., Sun, Y., Mao, X. O., Xie, L., & Greenberg, D. A. (2002). Vascular endothelial growth factor (VEGF) stimulates neurogenesis in vitro and in vivo. Proceedings of the National Academy of Sciences of the United States of America, 99(18), 11946–11950.
   PubMed Web of Science ®Google Scholar
• Kronenberg, G., Bick-Sander, A., Bunk, E., Wolf, C., Ehninger, D., & Kempermann, G. (2006). Physical exercise prevents age-related decline in precursor cell activity in the mouse dentate gyrus. Neurobiology of Aging, 27(10), 1505–1513.
   PubMed Web of Science ®Google Scholar
• Kronenberg, G., Reuter, K., Steiner, B., Brandt, M. D., Jessbetger, S., Yamaguchi, M., (2003). Subpopulations of proliferating cells of the adult hippocampus respond differently to physiologic neurogenic stimuli. The Journal of Comparative Neurology, 467(4), 455–463.
   PubMed Web of Science ®Google Scholar
• Kuhn, H. G., Winkler, J., Kempermann, G., Thal, L. J., & Gage, F. H. (1997). Epidermal growth factor and fibroblast growth factor-2 have different effects on neural progenitors in the adult rat brain. The Journal of Neuroscience, 17(15), 5820–5829.
   PubMed Web of Science ®Google Scholar
• Kulbatski, I., Mothe, A. J., Keating, A., Hakamata, Y., Kobayashi, E., & Tator, C. H. (2007). Oligodendrocytes and radial glia derived from adult rat spinal cord progenitors: Morphological and immunocytochemical characterization. The Journal of Histochemistry and Cytochemistry, 55(3), 209–222.
   Google Scholar
• Li, J., Ding, Y. H., Rafols, J. A., Lai, Q., McAllister, II, J. P., & Ding, Y. (2005). Increased astrocyte proliferation in rats after running exercise. Neuroscience Letters, 386(3), 160–164.
   PubMed Web of Science ®Google Scholar
• McKinnon, R. D., Matsui, T., Dubois-Dalcq, M., & Aaronson, S. A. (1990). FGF modulates the PDGF-driven pathway of oligodendrocyte development. Neuron, 5(5), 603–614.
   Google Scholar
• McMorris, F. A., & Dubois-Dalcq, M. (1988). Insulin-like growth factor I promotes cell proliferation and oligodendroglial commitment in rat glial progenitor cells developing in vitro. Journal of Neuroscience Research, 21(2–4), 199–209.
   Google Scholar
• McTigue, D. M., Horner, P. J., Stokes, B. T., & Gage, F. H. (1998). Neurotrophin-3 and brain-derived neurotrophic factor induce oligodendrocyte proliferation and myelination of regenerating axons in the contused adult rat spinal cord. The Journal of Neuroscience, 18(14), 5354–5365.
   PubMed Web of Science ®Google Scholar
• Miller, R. H. (1996). Oligodendrocyte origins. Trends in Neurosciences, 19(3), 92–96.
   Google Scholar
• Morshead, C. M., Reynolds, B. A., Craig, C. G., McBurney, M. W., Staines, W. A., Morassutti, D., (1994). Neural stem cells in the adult mammalian forebrain: A relatively quiescent subpopulation of subependymal cells. Neuron, 13(5), 1071–1082.
   PubMed Web of Science ®Google Scholar
• Munehiro, U., Minenori, I., Katsuya, K., & Mitsuhiko, M. (2006). Effects of chronic treadmill running on neurogenesis in the dentate gyrus of the hippocampus of adult rat. Journal of Brain Research, 1104(1), 64–72.
   Google Scholar
• Naylor, A. S., Persson, A. I., Eriksson, P. S., Jonsdottir, I. H., &Thorlin, T. (2005). Extended voluntary running inhibits exercise-induced adult hippocampal progenitor proliferation in spontaneously hypertensive rat. Journal of Neurophysiology, 93(5), 2406–2414.
   Google Scholar
• Neeper, S. A., Gomez-Pinilla, F., Choi, J., & Cotman, C. W. (1995). Exercise and brain neurotrophins [letter]. Nature, 373(6510), 109.
   PubMed Web of Science ®Google Scholar
• Neeper, S. A., Gomez-Pinilla, F., Choi, J., & Cotman, C. W. (1996). Physical activity increases mRNA for brain-derived neurotrophic factor and nerve growth factor in rat brain. Brain Research, 726(1–2), 49–56.
   PubMed Web of Science ®Google Scholar
• Perreau, W. M., Paul, A. A., Anderson, A. J., & Cotman, C. W. (2005). Exercise-induced gene expression changes in the rat spinal cord. Gene Expression, 12(2), 107–121.
   Google Scholar
• Rao, M. A. (1999). Multipotent and restricted precursors in the central nervous system. The Anatomical Record, 257(4), 137–148.
   Google Scholar
• Reynolds, B. A., & Weiss, S. (1992). Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science, 255(5052), 1707–1710.
   PubMed Web of Science ®Google Scholar
• Richardson, W. E., Pringle, N., Mosely, M. J., Westermark, B., & Dubois-Dalcq, M. (1988). A role of platelet-derived growth factor in normal gliogenesis in the central nervous system. Cell, 53(2), 309–319.
   Google Scholar
• Scarisbrick, I. A., Asakura, K., & Rodriguez, M. (2000). Neurotrophin-4/5 promotes proliferation of oligodendrocyte-type-2 astrocytes (O-2A). Developmental Brain Research, 123(1), 87–90.
   Google Scholar
• Skup, M., Dwornik, A., Macias, M., Sulejczak, D., Wiater, M., & Czarkowska-Bauch, J. (2002). Long-term locomotor training up-regulates TrkB receptor-like proteins, brain-derived neurotrophic factor, and neurotrophin 4 with different topographies of expression in oligodendroglia and neurons in the spinal cord. Experimental Neurology, 176(2), 289–307.
   Google Scholar
• Tropepe, V., Craig, C. G., Morshead, C. M., & Van Der Kooy, D. (1997). Transforming growth factor-alpha null and senescent mice show decreased neural progenitor cell proliferation in the forebrain sub ependyma. The Journal of Neuroscience, 17(20), 7850–7859.
   Google Scholar
• van Praag, H., Christie, B. R., Sejnowski, T. J., & Gage, F. H. (1999b). Running enhances neurogenesis, learning and long-term potentiation in mice. Proceedings of the National Academy of Sciences of the United States of America, 96(23), 13427–13431.
   PubMed Web of Science ®Google Scholar
• van Praag, H., Kempermann, G., & Gage, F. H. (1999a). Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nature Neuroscience, 2(3), 266–270.
   PubMed Web of Science ®Google Scholar
• Vick, R. S., Collins, J. M., & de Vries, G. H. (1992). Cell cycle and proliferation dynamics of adult rat oligodendrocytes. Journal of Neuroscience Research, 33(1), 75–81.
   Google Scholar
• Weiss, S., Dunne, C., Hewson, J., Wohl, C., Wheatley, M., Peterson, A. C., (1996). Multipotent CNS stem cells are present in the adult mammalian spinal cord and ventricular neuroaxis. The Journal of Neuroscience, 16(23), 7599–7609.
   PubMedGoogle Scholar
• Yamaguchi, M., Saito, H., Suzuki, M., & Mori, K. (2000). Visualization of neurogenesis in the central nervous system using nestin promoter-GFP transgenic mice. Neuroreport, 11(9), 1991– 1996.
   Google Scholar
• Yeh, H. J., Ruit, K. G., Wang, Y. X., Parks, W. C., Snider, W. D., & Deuel, T. F. (1991). PDGF A-chain gene is expressed by mammalian neurons during development and in maturity. Cell, 64(1), 201–216.
   Google Scholar
• Ying, Z., Roy, R. R., Edgerton, V. R., & Gomez-Pinilla, F. (2003). Voluntary exercise increases neurotrophin-3 and its receptor TrkC in spinal cord. Brain Research, 987(1), 93–99.
   Google Scholar
• Ying, Z., Roy, R. R., Edgerton, V. R., & Gomez-Pinilla, F. (2005). Exercise restores levels of neurotrophins and synaptic plasticity following spinal cord injury. Experimental Neurology, 193(2), 411–419.
   PubMed Web of Science ®Google Scholar