Exercise promotes axon regeneration of newborn striatonigral and corticonigral projection neurons in rats after ischemic stroke

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Zhang, Qiu Wan ^a   Deng, Xu Xu ^a   Sun, Xiao ^a   Xu, Jin Xiu ^a   Sun, Feng Yan ^a,b  

^a FUDAN UNIVERSITY   (China)

^b Shanghai Key Laboratory of Traditional Chinese Clinical Medicine   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; FLUOROGOLD; GREEN FLUORESCENT PROTEIN; PROTEIN NOGO A; RETROVIRUS VECTOR; SYNAPSIN; TYROSINE 3 MONOOXYGENASE; VASCULOTROPIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN; BRAIN ISCHEMIA; CEREBROVASCULAR ACCIDENT; CONTROLLED STUDY; CORPUS STRIATUM; CORTICONIGRAL PROJECTION NEURON; DOWN REGULATION; IMMUNOHISTOCHEMISTRY; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; MOTOR PERFORMANCE; NERVE FIBER REGENERATION; NEWBORN; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; OUTCOME ASSESSMENT; PARIETAL CORTEX; PREFRONTAL CORTEX; RAT; ROTAROD TEST; SUBSTANTIA NIGRA; THALAMOCORTICAL TRACT; TREADMILL EXERCISE; UPREGULATION;

ANIMALS; AXONS; CORPUS STRIATUM; DOWN-REGULATION; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; ISCHEMIC ATTACK, TRANSIENT; MALE; MOTOR CORTEX; MYELIN PROTEINS; NEUROGENESIS; NEURONS; PHYSICAL CONDITIONING, ANIMAL; RATS; RATS, SPRAGUE-DAWLEY; RECOVERY OF FUNCTION; REGENERATION; STROKE; SUBSTANTIA NIGRA; UP-REGULATION;

EID: 84896710117     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0080139     Document Type: Article

References (52)

1. Nakayama H, Jorgensen HS, Raaschou HO, Olsen TS (1994) Recovery of upper extremity function in stroke patients: the Copenhagen Stroke Study. Arch Phys Med Rehabil 75: 394-398. (Pubitemid 24134114)
2. Cho HY, Kim JS, Lee GC (2012) Effects of motor imagery training on balance and gait abilities in post-stroke patients: a randomized controlled trial. Clin Rehabil.
3. Metrot J, Mottet D, Hauret I, van Dokkum L, Bonnin-Koang HY, et al. (2012) Changes in Bimanual Coordination During the First 6 Weeks After Moderate Hemiparetic Stroke. Neurorehabil Neural Repair.
4. Yang YR, Wang RY, Wang PS, Yu SM (2003) Treadmill training effects on neurological outcome after middle cerebral artery occlusion in rats. Can J Neurol Sci 30: 252-258. (Pubitemid 37064522)
5. Gage FH (2000) Mammalian neural stem cells. Science 287: 1433-1438.
6. van Praag H, Schinder AF, Christie BR, Toni N, Palmer TD, et al. (2002) Functional neurogenesis in the adult hippocampus. Nature 415: 1030-1034. (Pubitemid 34193451)
7. Lichtenwalner RJ, Parent JM (2006) Adult neurogenesis and the ischemic forebrain. J Cereb Blood Flow Metab 26: 1-20. (Pubitemid 41818065)
8. Darsalia V, Heldmann U, Lindvall O, Kokaia Z (2005) Stroke-induced neurogenesis in aged brain. Stroke 36: 1790-1795. (Pubitemid 41098780)
9. Kuge A, Takemura S, Kokubo Y, Sato S, Goto K, et al. (2009) Temporal profile of neurogenesis in the subventricular zone, dentate gyrus and cerebral cortex following transient focal cerebral ischemia. Neurol Res 31: 969-976.
10. Jin K, Wang X, Xie L, Mao XO, Zhu W, et al. (2006) Evidence for stroke-induced neurogenesis in the human brain. Proc Natl Acad Sci U S A 103: 13198-13202. (Pubitemid 44338939)
11. Macas J, Nern C, Plate KH, Momma S (2006) Increased generation of neuronal progenitors after ischemic injury in the aged adult human forebrain. J Neurosci 26: 13114-13119. (Pubitemid 44954629)
12. Minger SL, Ekonomou A, Carta EM, Chinoy A, Perry RH, et al. (2007) Endogenous neurogenesis in the human brain following cerebral infarction. Regen Med 2: 69-74. (Pubitemid 46824414)
13. Arvidsson A, Collin T, Kirik D, Kokaia Z, Lindvall O (2002) Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat Med 8: 963-970. (Pubitemid 35033700)
14. Wang YQ, Guo X, Qiu MH, Feng XY, Sun FY (2007) VEGF overexpression enhances striatal neurogenesis in brain of adult rat after a transient middle cerebral artery occlusion. J Neurosci Res 85: 73-82. (Pubitemid 46079798)
15. Hou SW, Wang YQ, Xu M, Shen DH, Wang JJ, et al. (2008) Functional integration of newly generated neurons into striatum after cerebral ischemia in the adult rat brain. Stroke 39: 2837-2844.
16. Yang SZ, Li KY, Wang YQ, Shen DH, Sun FY (2010) Functional contribution of neurogenesis in normal and stroke brain. In: Jin KL, editor. Adult Neurogenesis and Central Nervous System Diseases. Kerala, India: Transworld Research Network. pp. 91-125.
17. Sun X, Zhang QW, Xu M, Guo JJ, Shen SW, et al. (2012) New striatal neurons form projections to substantia nigra in adult rat brain after stroke. Neurobiol Dis 45: 601-609.
18. Martin AB, Fernandez-Espejo E, Ferrer B, Gorriti MA, Bilbao A, et al. (2008) Expression and function of CB1 receptor in the rat striatum: localization and effects on D1 and D2 dopamine receptor-mediated motor behaviors. Neuropsychopharmacology 33: 1667-1679. (Pubitemid 351684717)
19. Thompson LH, Grealish S, Kirik D, Bjorklund A (2009) Reconstruction of the nigrostriatal dopamine pathway in the adult mouse brain. Eur J Neurosci 30: 625-638.
20. Mallet N, Ballion B, Le Moine C, Gonon F (2006) Cortical inputs and GABA interneurons imbalance projection neurons in the striatum of parkinsonian rats. J Neurosci 26: 3875-3884.
21. Nakane M, Teraoka A, Asato R, Tamura A (1992) Degeneration of the ipsilateral substantia nigra following cerebral infarction in the striatum. Stroke 23: 328-332.
22. Tamura A, Kirino T, Sano K, Takagi K, Oka H (1990) Atrophy of the ipsilateral substantia nigra following middle cerebral artery occlusion in the rat. Brain Res 510: 154-157. (Pubitemid 20060819)
23. Speisman RB, Kumar A, Rani A, Foster TC, Ormerod BK (2012) Daily exercise improves memory, stimulates hippocampal neurogenesis and modulates immune and neuroimmune cytokines in aging rats. Brain Behav Immun.
24. Luo CX, Jiang J, Zhou QG, Zhu XJ, Wang W, et al. (2007) Voluntary exercise-induced neurogenesis in the postischemic dentate gyrus is associated with spatial memory recovery from stroke. J Neurosci Res 85: 1637-1646. (Pubitemid 46849611)
25. Leasure JL, Grider M (2010) The effect of mild post-stroke exercise on reactive neurogenesis and recovery of somatosensation in aged rats. Exp Neurol 226: 58-67.
26. Chytrova G, Ying Z, Gomez-Pinilla F (2008) Exercise normalizes levels of MAG and Nogo-A growth inhibitors after brain trauma. Eur J Neurosci 27: 1-11.
27. Weinmann O, Schnell L, Ghosh A, Montani L, Wiessner C, et al. (2006) Intrathecally infused antibodies against Nogo-A penetrate the CNS and downregulate the endogenous neurite growth inhibitor Nogo-A. Mol Cell Neurosci 32: 161-173. (Pubitemid 43868104)
28. Yang ZJ, Bao WL, Qiu MH, Zhang LM, Lu SD, et al. (2002) Role of vascular endothelial growth factor in neuronal DNA damage and repair in rat brain following a transient cerebral ischemia. J Neurosci Res 70: 140-149.
29. Ploughman M, Windle V, MacLellan CL, White N, Dore JJ, et al. (2009) Brain-derived neurotrophic factor contributes to recovery of skilled reaching after focal ischemia in rats. Stroke 40: 1490-1495.
30. Guo JJ, Liu F, Sun X, Huang JJ, Xu M, et al. (2012) Bcl-2 enhances the formation of newborn striatal long-projection neurons in adult rat brain after a transient ischemic stroke. Neurosci Bull 28: 669-679.
31. Longa EZ, Weinstein PR, Carlson S, Cummins R (1989) Reversible middle cerebral artery occlusion without craniectomy in rats. Stroke 20: 84-91. (Pubitemid 19040218)
32. Chen J, Sanberg PR, Li Y, Wang L, Lu M, et al. (2001) Intravenous administration of human umbilical cord blood reduces behavioral deficits after stroke in rats. Stroke 32: 2682-2688. (Pubitemid 33055324)
33. Wild AR, Akyol E, Brothwell SL, Kimkool P, Skepper JN, et al. (2013) Memantine block depends on agonist presentation at the NMDA receptor in substantia nigra pars compacta dopamine neurones. Neuropharmacology 73C: 138-146.
34. Amaral DG (2000) The Anatomical Organization of the Central Nervous System. In: Kandel ER, Schwartz JH, Jessell TM, editor. Principles of Neural Science. New York: McGraw Hill. pp. 317-336.
35. Haines DE (1995) Neuroanatomy: An Atlas of Structures, Sections, and System. In: Wilkins W, editor. Maryland. pp. 134-203.
36. Trushina E, Dyer RB, Badger JD, 2nd, Ure D, Eide L, et al. (2004) Mutant huntingtin impairs axonal trafficking in mammalian neurons in vivo and in vitro. Mol Cell Biol 24: 8195-8209. (Pubitemid 39167467)
37. Bramham CR, Messaoudi E (2005) BDNF function in adult synaptic plasticity: the synaptic consolidation hypothesis. Prog Neurobiol 76: 99-125. (Pubitemid 41242884)
38. Ding Q, Ying Z, Gomez-Pinilla F (2011) Exercise influences hippocampal plasticity by modulating brain-derived neurotrophic factor processing. Neuroscience 192: 773-780.
39. MacLellan CL, Keough MB, Granter-Button S, Chernenko GA, Butt S, et al. (2011) A critical threshold of rehabilitation involving brain-derived neurotrophic factor is required for poststroke recovery. Neurorehabil Neural Repair 25: 740-748.
40. Schabitz WR, Steigleder T, Cooper-Kuhn CM, Schwab S, Sommer C, et al. (2007) Intravenous brain-derived neurotrophic factor enhances poststroke sensorimotor recovery and stimulates neurogenesis. Stroke 38: 2165-2172. (Pubitemid 47012284)
41. Zhu JM, Zhao YY, Chen SD, Zhang WH, Lou L, et al. (2011) Functional recovery after transplantation of neural stem cells modified by brain-derived neurotrophic factor in rats with cerebral ischaemia. J Int Med Res 39: 488-498.
42. GrandPre T, Nakamura F, Vartanian T, Strittmatter SM (2000) Identification of the Nogo inhibitor of axon regeneration as a Reticulon protein. Nature 403: 439-444. (Pubitemid 30073094)
43. Kilic E, ElAli A, Kilic U, Guo Z, Ugur M, et al. (2010) Role of Nogo-A in neuronal survival in the reperfused ischemic brain. J Cereb Blood Flow Metab 30: 969-984.
44. Qiu MH, Zhang R, Sun FY (2003) Enhancement of ischemia-induced tyrosine phosphorylation of Kv1.2 by vascular endothelial growth factor via activation of phosphatidylinositol 3-kinase. J Neurochem 87: 1509-1517. (Pubitemid 38020584)
45. Jin K, Zhu Y, Sun Y, Mao XO, Xie L, et al. (2002) Vascular endothelial growth factor (VEGF) stimulates neurogenesis in vitro and in vivo. Proc Natl Acad Sci U S A 99: 11946-11950. (Pubitemid 34994504)
46. Wang YQ, Cui HR, Yang SZ, Sun HP, Qiu MH, et al. (2009) VEGF enhance cortical newborn neurons and their neurite development in adult rat brain after cerebral ischemia. Neurochem Int 55: 629-636.
47. Ma YY, Li KY, Wang JJ, Huang YL, Huang Y, et al. (2009) Vascular endothelial growth factor acutely reduces calcium influx via inhibition of the Ca2+ channels in rat hippocampal neurons. J Neurosci Res 87: 393-402.
48. Xu JY, Zheng P, Shen DH, Yang SZ, Zhang LM, et al. (2003) Vascular endothelial growth factor inhibits outward delayed-rectifier potassium currents in acutely isolated hippocampal neurons. Neuroscience 118: 59-67. (Pubitemid 36369530)
49. Sun FY, Guo X (2005) Molecular and cellular mechanisms of neuroprotection by vascular endothelial growth factor. J Neurosci Res 79: 180-184.
50. Zhang F, Wu Y, Jia J (2011) Exercise preconditioning and brain ischemic tolerance. Neuroscience 177: 170-176.
51. Zhang R, Xue YY, Lu SD, Wang Y, Zhang LM, et al. (2006) Bcl-2 enhances neurogenesis and inhibits apoptosis of newborn neurons in adult rat brain following a transient middle cerebral artery occlusion. Neurobiol Dis 24: 345- 356.
52. Mink JW (1999) Basal ganglia. In: Zigmond MJ, Bloom FE, Landis SC,Roberts JL, Squire LR, editor. Fundamental Neuroscience. California: Academic Press. pp. 951-972.