Exercise does not protect against MPTP-induced neurotoxicity in BDNF happloinsufficent mice

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Gerecke, Kim M ^a   Jiao, Yun ^b   Pagala, Viswajeeth ^b   Smeyne, Richard J ^b  

^a RHODES COLLEGE   (United States)

^b ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; BRAIN DERIVED NEUROTROPHIC FACTOR;

ANIMAL TISSUE; ARTICLE; CELL LOSS; CELL MIGRATION; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINERGIC NERVE CELL; ENERGY METABOLISM; EXERCISE; FEMALE; HAPLOINSUFFICIENCY; HETEROZYGOSITY; INTRACELLULAR SIGNALING; MALE; MOUSE; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; PROTEIN EXPRESSION; PROTEOMICS; RUNNING; SUBSTANTIA NIGRA PARS COMPACTA;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; DNA PRIMERS; DOPAMINERGIC NEURONS; ELECTROPHORESIS, AGAR GEL; GENOTYPE; HAPLOINSUFFICIENCY; IMMUNOHISTOCHEMISTRY; MICE; MPTP POISONING; PHYSICAL CONDITIONING, ANIMAL; PROTEOMICS; SUBSTANTIA NIGRA; TANDEM MASS SPECTROMETRY;

EID: 84865092868     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0043250     Document Type: Article

References (134)

1. Colcombe SJ, Kramer AF, Erickson KI, Scalf P, McAuley E, et al. (2004) Cardiovascular fitness, cortical plasticity, and aging. Proc Natl Acad Sci U S A 101: 3316-3321.
2. Berkman LF, Seeman TE, Albert M, Blazer D, Kahn R, et al. (1993) High, usual and impaired functioning in community-dwelling older men and women: findings from the MacArthur Foundation Research Network on Successful Aging. J Clin Epidemiol 46: 1129-1140.
3. Blomquist KB, Danner F, (1987) Effects of physical conditioning on information-processing efficiency. Percept Mot Skills 65: 175-186.
4. Evans DA, Beckett LA, Albert MS, Hebert LE, Scherr PA, et al. (1993) Level of education and change in cognitive function in a community population of older persons. Ann Epidemiol 3: 71-77. 1047-2797(93)90012-S [pii].
5. Rogers RL, Meyer JS, Mortel KF, (1990) After reaching retirement age physical activity sustains cerebral perfusion and cognition. J Am Geriatr Soc 38: 123-128.
6. Friedland RP, Fritsch T, Smyth KA, Koss E, Lerner AJ, et al. (2001) Patients with Alzheimer's disease have reduced activities in midlife compared with healthy control-group members. Proc Natl Acad Sci U S A 98: 3440-3445. 10.1073/pnas.061002998 [doi];061002998 [pii].
7. Laurin D, Verreault R, Lindsay J, MacPherson K, Rockwood K (2001) Physical activity and risk of cognitive impairment and dementia in elderly persons. Arch Neurol 58: 498-504. noc00302 [pii].
8. Chen H, Zhang SM, Schwarzschild MA, Hernan MA, Ascherio A, (2005) Physical activity and the risk of Parkinson disease. Neurology 64: 664-669.
9. Goodwin VA, Richards SH, Taylor RS, Taylor AH, Campbell JL (2008) The effectiveness of exercise interventions for people with Parkinson's disease: a systematic review and meta-analysis. Mov Disord 23: 631-640. 10.1002/mds.21922 [doi].
10. Zigmond MJ, Cameron JL, Hoffer BJ, Smeyne RJ (2012) Neurorestoration by physical exercise: moving forward. Parkinsonism Relat Disord 18 Suppl 1: S147-S150. S1353-8020(11)70046-3 [pii];10.1016/S1353-8020(11)70046-3 [doi].
11. Fisher BE, Petzinger GM, Nixon K, Hogg E, Bremmer S, et al. (2004) Exercise-induced behavioral recovery and neuroplasticity in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-lesioned mouse basal ganglia. J Neurosci Res 77: 378-390.
12. Smith BA, Goldberg NR, Meshul CK (2011) Effects of treadmill exercise on behavioral recovery and neural changes in the substantia nigra and striatum of the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-lesioned mouse. Brain Res 1386: 70-80. S0006-8993(11)00251-4 [pii];10.1016/j.brainres.2011.02.003 [doi].
13. Tillerson JL, Cohen AD, Philhower J, Miller GW, Zigmond MJ, et al. (2001) Forced limb-use effects on the behavioral and neurochemical effects of 6-hydroxydopamine. J Neurosci 21: 4427-4435. 21/12/4427 [pii].
14. Tillerson JL, Caudle WM, Reveron ME, Miller GW, (2003) Exercise induces behavioral recovery and attenuates neurochemical deficits in rodent models of Parkinson's disease. Neuroscience 119: 899-911.
15. Faherty CJ, Raviie SK, Herasimtschuk A, Smeyne RJ, (2005) Environmental enrichment in adulthood eliminates neuronal death in experimental Parkinsonism. Brain Res Mol Brain Res 134: 170-179.
16. Gerecke KM, Jiao Y, Pani A, Pagala V, Smeyne RJ, (2010) Exercise protects against MPTP-induced neurotoxicity in mice. Brain Res 1341: 72-83.
17. Zigmond MJ, Cameron JL, Leak RK, Mirnics K, Russell VA, et al. (2009) Triggering endogenous neuroprotective processes through exercise in models of dopamine deficiency. Parkinsonism Relat Disord 15 Suppl 3: S42-S45. S1353-8020(09)70778-3 [pii];10.1016/S1353-8020(09)70778-3 [doi].
18. Mabandla MV, Russell VA (2010) Voluntary exercise reduces the neurotoxic effects of 6-hydroxydopamine in maternally separated rats. Behav Brain Res 211: 16-22. S0166-4328(10)00169-5 [pii];10.1016/j.bbr.2010.02.045 [doi].
19. Wu SY, Wang TF, Yu L, Jen CJ, Chuang JI, et al. (2011) Running exercise protects the substantia nigra dopaminergic neurons against inflammation-induced degeneration via the activation of BDNF signaling pathway. Brain Behav Immun 25: 135-146. S0889-1591(10)00464-2 [pii];10.1016/j.bbi.2010.09.006 [doi].
20. Ransom BR, Kunis DM, Irwin I, Langston JW, (1987) Astrocytes convert the parkinsonism inducing neurotoxin, MPTP, to its active metabolite, MPP+. Neurosci Lett 75: 323-328.
21. Nicklas WJ, Youngster SK, Kindt MV, Heikkila RE, (1987) MPTP, MPP+ and mitochondrial function. Life Sci 40: 721-729.
22. Annepu J, Ravindranath V (2000) 1-Methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced complex I inhibition is reversed by disulfide reductant, dithiothreitol in mouse brain. Neurosci Lett 289: 209-212. S0304394000013008 [pii].
23. Kopin IJ, (1992) Features of the dopaminergic neurotoxin MPTP. Ann N Y Acad Sci 648: 96-104.
24. Smeyne RJ, Jackson-Lewis V (2005) The MPTP model of Parkinson's disease. Brain Res Mol Brain Res 134: 57-66. S0169-328X(04)00455-3 [pii];10.1016/j.molbrainres.2004.09.017 [doi].
25. McGeer PL, Itagaki S, Boyes BE, McGeer EG, (1988) Reactive microglia are positive for HLA-DR in the substantia nigra of Parkinson's and Alzheimer's disease brains. Neurology 38: 1285-1291.
26. Kohutnicka M, Lewandowska E, Kurkowska-Jastrzebska I, Czlonkowski A, Czlonkowska A (1998) Microglial and astrocytic involvement in a murine model of Parkinson's disease induced by 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP). Immunopharmacology 39: 167-180. S0162310998000228 [pii].
27. Sugama S, Yang L, Cho BP, DeGiorgio LA, Lorenzl S, et al. (2003) Age-related microglial activation in 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-induced dopaminergic neurodegeneration in C57BL/6 mice. Brain Res 964: 288-294.
28. Riederer P, Sofic E, Rausch WD, Schmidt B, Reynolds GP, et al. (1989) Transition metals, ferritin, glutathione, and ascorbic acid in parkinsonian brains. J Neurochem 52: 515-520.
29. Zang LY, Misra HP, (1993) Generation of reactive oxygen species during the monoamine oxidase-catalyzed oxidation of the neurotoxicant, 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. J Biol Chem 268: 16504-16512.
30. Jenner P, (1998) Oxidative mechanisms in nigral cell death in Parkinson's disease. Mov Disord 13 Suppl 1: 24-34.
31. Neeper SA, Gomez-Pinilla F, Choi J, Cotman C, (1995) Exercise and brain neurotrophins. Nature 373: 109.
32. Neeper SA, Gomez-Pinilla F, Choi J, Cotman CW, (1996) Physical activity increases mRNA for brain-derived neurotrophic factor and nerve growth factor in rat brain. Brain Res 726: 49-56.
33. Kesslak JP, So V, Choi J, Cotman CW, Gomez-Pinilla F, (1998) Learning upregulates brain-derived neurotrophic factor messenger ribonucleic acid: a mechanism to facilitate encoding and circuit maintenance? Behav Neurosci 112: 1012-1019.
34. Garza AA, Ha TG, Garcia C, Chen MJ, Russo-Neustadt AA, (2004) Exercise, antidepressant treatment, and BDNF mRNA expression in the aging brain. Pharmacol Biochem Behav 77: 209-220.
35. Russo-Neustadt AA, Beard RC, Huang YM, Cotman CW, (2000) Physical activity and antidepressant treatment potentiate the expression of specific brain-derived neurotrophic factor transcripts in the rat hippocampus. Neuroscience 101: 305-312.
36. Knusel B, Hefti F, (1991) Trophic actions of IGF-I, IGF-II and insulin on cholinergic and dopaminergic brain neurons. Adv Exp Med Biol 293: 351-360.
37. Spina MB, Squinto SP, Miller J, Lindsay RM, Hyman C, (1992) Brain-derived neurotrophic factor protects dopamine neurons against 6-hydroxydopamine and N-methyl-4-phenylpyridinium ion toxicity: involvement of the glutathione system. J Neurochem 59: 99-106.
38. Petersen AA, Larsen KE, Behr GG, Romero N, Przedborski S, et al. (2001) Brain-derived neurotrophic factor inhibits apoptosis and dopamine-induced free radical production in striatal neurons but does not prevent cell death. Brain Res Bull 56: 331-335. S0361923001005809 [pii].
39. Radak Z, Kumagai S, Taylor AW, Naito H, Goto S (2007) Effects of exercise on brain function: role of free radicals. Appl Physiol Nutr Metab 32: 942-946. h07-081 [pii];10.1139/H07-081 [doi].
40. Bloomer RJ, Schilling BK, Karlage RE, Ledoux MS, Pfeiffer RF, et al. (2008) Effect of resistance training on blood oxidative stress in Parkinson disease. Med Sci Sports Exerc 40: 1385-1389. 10.1249/MSS.0b013e31816f1550 [doi].
41. Ernfors P, Lee KF, Jaenisch R, (1994) Mice lacking brain-derived neurotrophic factor develop with sensory deficits. Nature 368: 147-150.
42. Chourbaji S, Hellweg R, Brandis D, Zorner B, Zacher C, et al. (2004) Mice with reduced brain-derived neurotrophic factor expression show decreased choline acetyltransferase activity, but regular brain monoamine levels and unaltered emotional behavior. Brain Res Mol Brain Res 121: 28-36.
43. Hill RA, van den Buuse M (2011) Sex-dependent and region-specific changes in TrkB signaling in BDNF heterozygous mice. Brain Res 1384: 51-60. S0006-8993(11)00144-2 [pii];10.1016/j.brainres.2011.01.060 [doi].
44. Baker SA, Stanford LE, Brown RE, Hagg T, (2005) Maturation but not survival of dopaminergic nigrostriatal neurons is affected in developing and aging BDNF-deficient mice. Brain Res 1039: 177-188.
45. Grosse G, Djalali S, Deng DR, Holtje M, Hinz B, et al. (2005) Area-specific effects of brain-derived neurotrophic factor (BDNF) genetic ablation on various neuronal subtypes of the mouse brain. Brain Res Dev Brain Res 156: 111-126. S0165-3806(05)00076-3 [pii];10.1016/j.devbrainres.2004.12.012 [doi].
46. Boger HA, Mannangatti P, Samuvel DJ, Saylor AJ, Bender TS, et al. (2011) Effects of brain-derived neurotrophic factor on dopaminergic function and motor behavior during aging. Genes Brain Behav 10: 186-198. 10.1111/j.1601-183X.2010.00654.x [doi].
47. Dluzen DE, Gao X, Story GM, Anderson LI, Kucera J, et al. (2001) Evaluation of nigrostriatal dopaminergic function in adult +/+ and +/- BDNF mutant mice. Exp Neurol 170: 121-128.
48. MacQueen GM, Ramakrishnan K, Croll SD, Siuciak JA, Yu G, et al. (2001) Performance of heterozygous brain-derived neurotrophic factor knockout mice on behavioral analogues of anxiety, nociception, and depression. Behav Neurosci 115: 1145-1153.
49. Duman CH, Schlesinger L, Russell DS, Duman RS (2008) Voluntary exercise produces antidepressant and anxiolytic behavioral effects in mice. Brain Res 1199: 148-158. S0006-8993(07)03068-5 [pii];10.1016/j.brainres.2007.12.047 [doi].
50. Smeyne M, Goloubeva O, Smeyne RJ (2001) Strain-dependent susceptibility to MPTP and MPP(+)-induced parkinsonism is determined by glia. Glia 34: 73-80. 10.1002/glia.1042 [pii].
51. Moy LY, Albers DS, Sonsalla PK (1998) Lowering ambient or core body temperature elevates striatal MPP+ levels and enhances toxicity to dopamine neurons in MPTP-treated mice. Brain Res 790: 264-269. S0006-8993(98)00069-9 [pii].
52. Jackson-Lewis V, Jakowec M, Burke RE, Przedborski S, (1995) Time course and morphology of dopaminergic neuronal death caused by the neurotoxin 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. Neurodegeneration 4: 257-269.
53. Boyd JD, Jang H, Shepherd KR, Faherty C, Slack S, Jia Y, et al. (2007) Response to 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) differs in mouse strains and reveals a divergence in JNK signaling and COX-2 induction prior to loss of neurons in the substantia nigra pars compacta. Brain Res 1175: 107-116.
54. Cook R, Lu L, Gu J, Williams RW, Smeyne RJ (2003) Identification of a single QTL, Mptp1, for susceptibility to MPTP-induced substantia nigra pars compacta neuron loss in mice. Brain Res Mol Brain Res 110: 279-288. S0169328X02006599 [pii].
55. Baquet ZC, Williams D, Brody J, Smeyne RJ (2009) A comparison of model-based (2D) and design-based (3D) stereological methods for estimating cell number in the substantia nigra pars compacta (SNpc) of the C57BL/6J mouse. Neuroscience 161: 1082-1090. S0306-4522(09)00637-X [pii];10.1016/j.neuroscience.2009.04.031 [doi].
56. Jiao Y, Lu L, Williams RW, Smeyne RJ (2012) Genetic dissection of strain dependent paraquat-induced neurodegeneration in the substantia nigra pars compacta. PLoS One 7: e29447. 10.1371/journal.pone.0029447 [doi];PONE-D-11-19803 [pii].
57. Rieker C, Schober A, Bilbao A, Schutz G, Parkitna JR (2012) Ablation of serum response factor in dopaminergic neurons exacerbates susceptibility towards MPTP-induced oxidative stress. Eur J Neurosci 35: 735-741. 10.1111/j.1460-9568.2012.08003.x [doi].
58. Sterky FH, Hoffman AF, Milenkovic D, Bao B, Paganelli A, et al. (2012) Altered dopamine metabolism and increased vulnerability to MPTP in mice with partial deficiency of mitochondrial complex I in dopamine neurons. Hum Mol Genet 21: 1078-1089. ddr537 [pii];10.1093/hmg/ddr537 [doi].
59. Chung YC, Kim SR, Park JY, Chung ES, Park KW, et al. (2011) Fluoxetine prevents MPTP-induced loss of dopaminergic neurons by inhibiting microglial activation. Neuropharmacology 60: 963-974. S0028-3908(11)00054-2 [pii];10.1016/j.neuropharm.2011.01.043 [doi].
60. Ding YX, Xia Y, Jiao XY, Duan L, Yu J, et al. (2011) The TrkB-positive dopaminergic neurons are less sensitive to MPTP insult in the substantia nigra of adult C57/BL mice. Neurochem Res 36: 1759-1766. 10.1007/s11064-011-0491-5 [doi].
61. Hutter-Saunders JA, Kosloski LM, McMillan JM, Yotam N, Rinat T, et al. (2011) BL-1023 improves behavior and neuronal survival in 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-intoxicated mice. Neuroscience 180: 293-304. S0306-4522(11)00156-4 [pii];10.1016/j.neuroscience.2011.02.015 [doi].
62. Ito T, Uchida K, Nakayama H (2011) Neuronal or inducible nitric oxide synthase (NOS) expression level is not involved in the different susceptibility to nigro-striatal dopaminergic neurotoxicity induced by 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) between C57BL/6 and BALB/c mice. Exp Toxicol Pathol. S0940-2993(11)00094-7 [pii];10.1016/j.etp.2011.06.009 [doi].
63. Coban A, Filipov NM (2007) Dopaminergic toxicity associated with oral exposure to the herbicide atrazine in juvenile male C57BL/6 mice. J Neurochem 100: 1177-1187. JNC4294 [pii];10.1111/j.1471-4159.2006.04294.x [doi].
64. McCormack AL, Atienza JG, Langston JW, Di Monte DA (2006) Decreased susceptibility to oxidative stress underlies the resistance of specific dopaminergic cell populations to paraquat-induced degeneration. Neuroscience 141: 929-937. S0306-4522(06)00438-6 [pii];10.1016/j.neuroscience.2006.03.069 [doi].
65. McCormack AL, Atienza JG, Johnston LC, Andersen JK, Vu S, et al. (2005) Role of oxidative stress in paraquat-induced dopaminergic cell degeneration. J Neurochem 93: 1030-1037. JNC3088 [pii];10.1111/j.1471-4159.2005.03088.x [doi].
66. Zou L, Xu J, Jankovic J, He Y, Appel SH, et al. (2000) Pramipexole inhibits lipid peroxidation and reduces injury in the substantia nigra induced by the dopaminergic neurotoxin 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine in C57BL/6 mice. Neurosci Lett 281: 167-170. S0304394000008533 [pii].
67. Liberatore GT, Jackson-Lewis V, Vukosavic S, Mandir AS, Vila M, et al. (1999) Inducible nitric oxide synthase stimulates dopaminergic neurodegeneration in the MPTP model of Parkinson disease. Nat Med 5: 1403-1409.
68. Walters TL, Irwin I, Delfani K, Langston JW, Janson AM (1999) Diethyldithiocarbamate causes nigral cell loss and dopamine depletion with nontoxic doses of MPTP. Exp Neurol 156: 62-70. S0014-4886(98)96997-7 [pii];10.1006/exnr.1998.6997 [doi].
69. Muthane U, Ramsay KA, Jiang H, Jackson-Lewis V, Donaldson D, et al. (1994) Differences in nigral neuron number and sensitivity to 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine in C57/bl and CD-1 mice. Exp Neurol 126: 195-204. S0014-4886(84)71058-2 [pii];10.1006/exnr.1994.1058 [doi].
70. Sundstrom E, Luthman J, Goldstein M, Jonsson G (1988) Time course of MPTP-induced degeneration of the nigrostriatal dopamine system in C57 BL/6 mice. Brain Res Bull 21: 257-263. 0361-9230(88)90240-7 [pii].
71. Verhave PS, Jongsma MJ, Van Den Berg RM, Vanwersch RA, Smit AB, et al. (2012) Neuroprotective effects of riluzole in early phase Parkinson's disease on clinically relevant parameters in the marmoset MPTP model. Neuropharmacology 62: 1700-1707. S0028-3908(11)00495-3 [pii];10.1016/j.neuropharm.2011.11.016 [doi].
72. Meissner W, Prunier C, Guilloteau D, Chalon S, Gross CE, et al. (2003) Time-course of nigrostriatal degeneration in a progressive MPTP-lesioned macaque model of Parkinson's disease. Mol Neurobiol 28: 209-218.
73. Collier TJ, Sortwell CE, Elsworth JD, Taylor JR, Roth RH, et al. (2002) Embryonic ventral mesencephalic grafts to the substantia nigra of MPTP-treated monkeys: feasibility relevant to multiple-target grafting as a therapy for Parkinson's disease. J Comp Neurol 442: 320-330. 10.1002/cne.10108 [doi];10.1002/cne.10108 [pii].
74. Perez-Otano I, Oset C, Luquin MR, Herrero MT, Obeso JA, et al. (1994) MPTP-induced parkinsonism in primates: pattern of striatal dopamine loss following acute and chronic administration. Neurosci Lett 175: 121-125.
75. German DC, Manaye KF, Sonsalla PK, Brooks BA, (1992) Midbrain dopaminergic cell loss in Parkinson's disease and MPTP-induced parkinsonism: sparing of calbindin-D28k-containing cells. Ann N Y Acad Sci 648: 42-62.
76. Deutch AY, Elsworth JD, Goldstein M, Fuxe K, Redmond DE Jr, et al. (1986) Preferential vulnerability of A8 dopamine neurons in the primate to the neurotoxin 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. Neurosci Lett 68: 51-56.
77. Langston JW, Forno LS, Rebert CS, Irwin I, (1984) Selective nigral toxicity after systemic administration of 1-methyl-4-phenyl-1,2,5,6-tetrahydropyrine (MPTP) in the squirrel monkey. Brain Res 292: 390-394.
78. Conover JC, Erickson JT, Katz DM, Bianchi LM, Poueymirou WT, et al. (1995) Neuronal deficits, not involving motor neurons, in mice lacking BDNF and/or NT4. Nature 375: 235-238.
79. Brandt U (2006) Energy converting NADH:quinone oxidoreductase (complex I). Annu Rev Biochem 75: 69-92. 10.1146/annurev.biochem.75.103004.142539 [doi].
80. Monaco R, Friedman FK, Hyde MJ, Chen JM, Manolatus S, et al. (1999) Identification of a glutathione-S-transferase effector domain for inhibition of jun kinase, by molecular dynamics. J Protein Chem 18: 859-866.
81. Wang T, Arifoglu P, Ronai Z, Tew KD (2001) Glutathione S-transferase P1-1 (GSTP1-1) inhibits c-Jun N-terminal kinase (JNK1) signaling through interaction with the C terminus. J Biol Chem 276: 20999-21003. 10.1074/jbc.M101355200 [doi];M101355200 [pii].
82. Lau YS, Patki G, Das-Panja K, Le WD, Ahmad SO (2011) Neuroprotective effects and mechanisms of exercise in a chronic mouse model of Parkinson's disease with moderate neurodegeneration. Eur J Neurosci 33: 1264-1274. 10.1111/j.1460-9568.2011.07626.x [doi].
83. Frim DM, Wullner U, Beal MF, Isacson O (1994) Implanted NGF-producing fibroblasts induce catalase and modify ATP levels but do not affect glutamate receptor binding or NMDA receptor expression in the rat striatum. Exp Neurol 128: 172-180. S0014-4886(84)71125-3 [pii];10.1006/exnr.1994.1125 [doi].
84. Tsukahara T, Takeda M, Shimohama S, Ohara O, Hashimoto N, (1995) Effects of brain-derived neurotrophic factor on 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced parkinsonism in monkeys. Neurosurgery 37: 733-739.
85. Moraska A, Deak T, Spencer RL, Roth D, Fleshner M, (2000) Treadmill running produces both positive and negative physiological adaptations in Sprague-Dawley rats. Am J Physiol Regul Integr Comp Physiol 279: R1321-R1329.
86. Albeck DS, Sano K, Prewitt GE, Dalton L (2006) Mild forced treadmill exercise enhances spatial learning in the aged rat. Behav Brain Res 168: 345-348. S0166-4328(05)00487-0 [pii];10.1016/j.bbr.2005.11.008 [doi].
87. Ke Z, Yip SP, Li L, Zheng XX, Tong KY (2011) The effects of voluntary, involuntary, and forced exercises on brain-derived neurotrophic factor and motor function recovery: a rat brain ischemia model. PLoS One 6: e16643. 10.1371/journal.pone.0016643 [doi].
88. Schaaf MJ, Hoetelmans RW, de Kloet ER, Vreugdenhil E (1997) AID-JNR5&3.0.CO;2-C [pii].
89. Schaaf MJ, de JJ, de Kloet ER, Vreugdenhil E (1998) Downregulation of BDNF mRNA and protein in the rat hippocampus by corticosterone. Brain Res 813: 112-120. S0006-8993(98)01010-5 [pii].
90. Schaaf MJ, de Kloet ER, Vreugdenhil E (2000) Corticosterone effects on BDNF expression in the hippocampus. Implications for memory formation. Stress 3: 201-208. I405J991014 [pii].
91. van PH, Christie BR, Sejnowski TJ, Gage FH, (1999) Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc Natl Acad Sci U S A 96: 13427-13431.
92. Yanagita S, Amemiya S, Suzuki S, Kita I (2007) Effects of spontaneous and forced running on activation of hypothalamic corticotropin-releasing hormone neurons in rats. Life Sci 80: 356-363. S0024-3205(06)00741-7 [pii];10.1016/j.lfs.2006.09.027 [doi].
93. Russo-Neustadt A, Ha T, Ramirez R, Kesslak JP (2001) Physical activity-antidepressant treatment combination: impact on brain-derived neurotrophic factor and behavior in an animal model. Behav Brain Res 120: 87-95. S0166-4328(00)00364-8 [pii].
94. Bueler H (2009) Impaired mitochondrial dynamics and function in the pathogenesis of Parkinson's disease. Exp Neurol 218: 235-246. S0014-4886(09)00080-6 [pii];10.1016/j.expneurol.2009.03.006 [doi].
95. Ding Q, Vaynman S, Souda P, Whitelegge JP, Gomez-Pinilla F (2006) Exercise affects energy metabolism and neural plasticity-related proteins in the hippocampus as revealed by proteomic analysis. Eur J Neurosci 24: 1265-1276. EJN5026 [pii];10.1111/j.1460-9568.2006.05026.x [doi].
96. Calkins MJ, Johnson DA, Townsend JA, Vargas MR, Dowell JA, et al. (2009) The Nrf2/ARE pathway as a potential therapeutic target in neurodegenerative disease. Antioxid Redox Signal 11: 497-508. 10.1089/ARS.2008.2242 [doi].
97. Cechetti F, Fochesatto C, Scopel D, Nardin P, Goncalves CA, et al. (2008) Effect of a neuroprotective exercise protocol on oxidative state and BDNF levels in the rat hippocampus. Brain Res 1188: 182-188. S0006-8993(07)02460-2 [pii];10.1016/j.brainres.2007.10.012 [doi].
98. Chen S, Zhang X, Yang D, Du Y, Li L, et al. (2008) D2/D3 receptor agonist ropinirole protects dopaminergic cell line against rotenone-induced apoptosis through inhibition of caspase- and JNK-dependent pathways. FEBS Lett 582: 603-610. S0014-5793(08)00053-7 [pii];10.1016/j.febslet.2008.01.028 [doi].
99. Baranano DE, Rao M, Ferris CD, Snyder SH (2002) Biliverdin reductase: a major physiologic cytoprotectant. Proc Natl Acad Sci U S A 99: 16093-16098. 10.1073/pnas.252626999 [doi];252626999 [pii].
100. Castro-Caldas M, Neves CA, Peixeiro I, Rodrigues E, Lechner MC, et al. (2009) GSTpi expression in MPTP-induced dopaminergic neurodegeneration of C57BL/6 mouse midbrain and striatum. J Mol Neurosci 38: 114-127. 10.1007/s12031-008-9141-z [doi].
101. Smeyne M, Boyd J, Raviie SK, Jiao Y, Pond BB, et al. (2007) GSTpi expression mediates dopaminergic neuron sensitivity in experimental parkinsonism. Proc Natl Acad Sci U S A 104: 1977-1982. 0610978104 [pii];10.1073/pnas.0610978104 [doi].
102. Shi M, Bradner J, Bammler TK, Eaton DL, Zhang J, et al. (2009) Identification of glutathione S-transferase pi as a protein involved in Parkinson disease progression. Am J Pathol 175: 54-65. S0002-9440(10)60523-8 [pii];10.2353/ajpath.2009.081019 [doi].
103. Nagatsu T, Sawada M (2006) Molecular mechanism of the relation of monoamine oxidase B and its inhibitors to Parkinson's disease: possible implications of glial cells. J Neural Transm Suppl 53-65.
104. Sun L, Xu S, Zhou M, Wang C, Wu Y, et al. (2010) Effects of cysteamine on MPTP-induced dopaminergic neurodegeneration in mice. Brain Res 1335: 74-82. S0006-8993(10)00716-X [pii];10.1016/j.brainres.2010.03.079 [doi].
105. Van HC, Cayla X, Bosch M, Merlevede W, Goris J, (1994) The phosphotyrosyl phosphatase activator of protein phosphatase 2A. A novel purification method, immunological and enzymic characterization. Eur J Biochem 226: 899-907.
106. Zeevalk GD, Bernard LP, Manzino L, Sonsalla PK, (2001) Differential sensitivity of mesencephalic neurons to inhibition of phosphatase 2A. J Pharmacol Exp Ther 298: 925-933.
107. Peng X, Tehranian R, Dietrich P, Stefanis L, Perez RG (2005) Alpha-synuclein activation of protein phosphatase 2A reduces tyrosine hydroxylase phosphorylation in dopaminergic cells. J Cell Sci 118: 3523-3530. jcs.02481 [pii];10.1242/jcs.02481 [doi].
108. Deters N, Ittner LM, Gotz J (2009) Substrate-specific reduction of PP2A activity exaggerates tau pathology. Biochem Biophys Res Commun 379: 400-405. S0006-291X(08)02479-0 [pii];10.1016/j.bbrc.2008.12.140 [doi].
109. Lee KW, Chen W, Junn E, Im JY, Grosso H, et al. (2011) Enhanced phosphatase activity attenuates alpha-Synucleinopathy in a mouse model. J Neurosci 31: 6963-6971. 31/19/6963 [pii];10.1523/JNEUROSCI.6513-10.2011 [doi].
110. Dougherty MK, Morrison DK (2004) Unlocking the code of 14-3-3. J Cell Sci 117: 1875-1884. 10.1242/jcs.01171 [doi];117/10/1875 [pii].
111. Zhang Y, Yang Z, Cao Y, Zhang S, Li H, et al. (2008) The Hsp40 family chaperone protein DnaJB6 enhances Schlafen1 nuclear localization which is critical for promotion of cell-cycle arrest in T-cells. Biochem J 413: 239-250. BJ20071510 [pii];10.1042/BJ20071510 [doi].
112. Durrenberger PF, Filiou MD, Moran LB, Michael GJ, Novoselov S, et al. (2009) DnaJB6 is present in the core of Lewy bodies and is highly up-regulated in parkinsonian astrocytes. J Neurosci Res 87: 238-245. 10.1002/jnr.21819 [doi].
113. Michael GJ, Esmailzadeh S, Moran LB, Christian L, Pearce RK, et al. (2011) Up-regulation of metallothionein gene expression in Parkinsonian astrocytes. Neurogenetics 12: 295-305. 10.1007/s10048-011-0294-5 [doi].
114. Kurz A, May C, Schmidt O, Muller T, Stephan C, et al. (2012) A53T-alpha-synuclein-overexpression in the mouse nigrostriatal pathway leads to early increase of 14-3-3 epsilon and late increase of GFAP. J Neural Transm 119: 297-312. 10.1007/s00702-011-0717-3 [doi].
115. Watabe M, Nakaki T (2004) Rotenone induces apoptosis via activation of bad in human dopaminergic SH-SY5Y cells. J Pharmacol Exp Ther 311: 948-953. 10.1124/jpet.104.071381 [doi];jpet.104.071381 [pii].
116. Gerlach M, Riederer P, Przuntek H, Youdim MB, (1991) MPTP mechanisms of neurotoxicity and their implications for Parkinson's disease. Eur J Pharmacol 208: 273-286.
117. Schapira AH, Cooper JM, Dexter D, Clark JB, Jenner P, et al. (1990) Mitochondrial complex I deficiency in Parkinson's disease. J Neurochem 54: 823-827.
118. Satoh K, Nigro P, Berk BC (2010) Oxidative stress and vascular smooth muscle cell growth: a mechanistic linkage by cyclophilin A. Antioxid Redox Signal 12: 675-682. 10.1089/ars.2009.2875 [doi].
119. Schurr A, (2002) Lactate, glucose and energy metabolism in the ischemic brain (Review). Int J Mol Med 10: 131-136.
120. Gupta V, Bamezai RN (2010) Human pyruvate kinase M2: a multifunctional protein. Protein Sci 19: 2031-2044. 10.1002/pro.505 [doi].
121. Spoden GA, Rostek U, Lechner S, Mitterberger M, Mazurek S, Z,et al. (2009) Pyruvate kinase isoenzyme M2 is a glycolytic sensor differentially regulating cell proliferation, cell size and apoptotic cell death dependent on glucose supply. Exp Cell Res 315: 2765-2774. S0014-4827(09)00294-8 [pii];10.1016/j.yexcr.2009.06.024 [doi].
122. Takei N, Kondo J, Nagaike K, Ohsawa K, Kato K, Kohsaka S, (1991) Neuronal survival factor from bovine brain is identical to neuron-specific enolase. J Neurochem 57: 1178-1184.
123. Hattori T, Takei N, Mizuno Y, Kato K, Kohsaka S (1995) Neurotrophic and neuroprotective effects of neuron-specific enolase on cultured neurons from embryonic rat brain. Neurosci Res 21: 191-198. 0168-0102(94)00849-B [pii].
124. Poon HF, Frasier M, Shreve N, Calabrese V, Wolozin B, et al. (2005) Mitochondrial associated metabolic proteins are selectively oxidized in A30P alpha-synuclein transgenic mice-a model of familial Parkinson's disease. Neurobiol Dis 18: 492-498. S0969-9961(04)00320-1 [pii];10.1016/j.nbd.2004.12.009 [doi].
125. Mejias R, Villadiego J, Pintado CO, Vime PJ, Gao L, et al. (2006) Neuroprotection by transgenic expression of glucose-6-phosphate dehydrogenase in dopaminergic nigrostriatal neurons of mice. J Neurosci 26: 4500-4508. 26/17/4500 [pii];10.1523/JNEUROSCI.0122-06.2006 [doi].
126. Greenamyre JT, Sherer TB, Betarbet R, Panov AV (2001) Complex I and Parkinson's disease. IUBMB Life 52: 135-141. 10.1080/15216540152845939 [doi].
127. Chou JL, Shenoy DV, Thomas N, Choudhary PK, Laferla FM, et al. (2011) Early dysregulation of the mitochondrial proteome in a mouse model of Alzheimer's disease. J Proteomics 74: 466-479. S1874-3919(11)00017-0 [pii];10.1016/j.jprot.2010.12.012 [doi].
128. Swerdlow RH, Parks JK, Davis JN, Cassarino DS, Trimmer PA, et al. (1998) Matrilineal inheritance of complex I dysfunction in a multigenerational Parkinson's disease family. Ann Neurol 44: 873-881. 10.1002/ana.410440605 [doi].
129. Pacelli C, De RD, Signorile A, Grattagliano I, di TG, et al. (2011) Mitochondrial defect and PGC-1alpha dysfunction in parkin-associated familial Parkinson's disease. Biochim Biophys Acta 1812: 1041-1053. S0925-4439(10)00300-5 [pii];10.1016/j.bbadis.2010.12.022 [doi].
130. Nagahara AH, Tuszynski MH (2011) Potential therapeutic uses of BDNF in neurological and psychiatric disorders. Nat Rev Drug Discov 10: 209-219. nrd3366 [pii];10.1038/nrd3366 [doi].
131. Gold SM, Schulz KH, Hartmann S, Mladek M, Lang UE, et al. (2003) Basal serum levels and reactivity of nerve growth factor and brain-derived neurotrophic factor to standardized acute exercise in multiple sclerosis and controls. J Neuroimmunol 138: 99-105.
132. Rojas VS, Struder HK, Wahrmann BV, Bloch W, Hollmann W (2006) Bicarbonate reduces serum prolactin increase induced by exercise to exhaustion. Med Sci Sports Exerc 38: 675-680. 10.1249/01.mss.0000210195.94952.50 [doi];00005768-200604000-00010 [pii].
133. Ferris LT, Williams JS, Shen CL (2007) The effect of acute exercise on serum brain-derived neurotrophic factor levels and cognitive function. Med Sci Sports Exerc 39: 728-734. 10.1249/mss.0b013e31802f04c7 [doi];00005768-200704000-00020 [pii].
134. Gomez-Pinilla F, Zhuang Y, Feng J, Ying Z, Fan G (2011) Exercise impacts brain-derived neurotrophic factor plasticity by engaging mechanisms of epigenetic regulation. Eur J Neurosci 33: 383-390. 10.1111/j.1460-9568.2010.07508.x [doi].