Enriched environment promotes similar neuronal and behavioral recovery in a young and aged mouse model of Parkinson's disease

Neuroscience

Volumn 172, Issue , 2011, Pages 443-452

  Goldberg, N R S ^a   Haack, A K ^a   Meshul, C K ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Aging; Dopamine; Enriched environment; MPTP; Neurorestoration; Parkinson's disease

Indexed keywords

1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; SODIUM CHLORIDE; TYROSINE 3 MONOOXYGENASE;

AGE DISTRIBUTION; AGED; AGING; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR CONTROL; BRAIN REGION; CELL LEVEL; CONTROLLED STUDY; DISEASE SEVERITY; ENVIRONMENTAL ENRICHMENT; LOCOMOTION; MALE; MOUSE; NERVE CELL; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SUBSTANTIA NIGRA PARS COMPACTA; TREATMENT DURATION; TREATMENT RESPONSE;

ANIMALS; BEHAVIOR, ANIMAL; DISEASE MODELS, ANIMAL; ENVIRONMENT; ENVIRONMENT, CONTROLLED; MALE; MICE; MICE, INBRED C57BL; NEURONS; PARKINSONIAN DISORDERS; PHYSICAL STIMULATION; RECOVERY OF FUNCTION; SUBSTANTIA NIGRA;

EID: 78650743184     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2010.09.062     Document Type: Article

References (68)

1. Alstott J., Timberlake W. Effects of rat sex-differences, lighting on locomotor exploration of a circular open field with free-standing central corners and without peripheral walls. Behav Brain Res 2009, 196(2):214-219.
2. Alves G., Wentzel-Larsen T., Aarsland D., Larsen J.P. Progression of motor impairment and disability in Parkinson disease: a population-based study. Neurology 2005, 65:1436-1441.
3. Anderson D.W., Bradbury K.A., Schneider J.S. Broad neuroprotectice profile of nicotinamide in different mouse models of MPTP-induced parkinsonism. Eur J Neurosci 2008, 28(3):610-617.
4. Baquet Z.C., Williams D., Brody J., Smeyne J. 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 2009, 161:1082-1090.
5. Benes F.M., Lange N. Two-dimensional versus three-dimensional cell counting: a practical perspective. Trends Neurosci 2001, 24:11-17.
6. Berendse H.W., Ponsen M.M. Diagnosing premotor Parkinson's disease using a two-step approach combining olfactory testing and DAT SPECT imaging. Parkinsonism Relat Disord 2009, 15(3):S26-S30.
7. Bezard E., Dovero S., Belin D., Duconger S., Jackson-Lewis V., Przedborski S., Piazza P.V., Gross C.E., Jaber M. Enriched environment confers resistance to 1-methyl-4-phenyl 1,2,3,6-tetrahydropyridine and cocaine: involvement of dopamine transporter and trophic factors. J Neurosci 2003, 23:10999-11007.
8. Bezard E., Dovero S., Bioulac B., Gross C.E. Kinetics of nigral degeneration in a chronic model of MPTP-treated mice. Neurosci Lett 1997, 234:47-50.
9. Burke S.N., Barnes C.A. Neural plasticity in the ageing brain. Nat Rev Neurosci 2006, 7:30-40.
10. Cao L., Liu X., Lin E.J.D., Wang C., Choi E.Y., Riban V., Lin B., During M. Environmental and genetic activation of a brain-adipocyte BDNF/Leptin axis causes cancer remission and inhibition. Cell 2010, 142:52-64.
11. Chesselet M.F., Fleming S., Mortazavi F., Meurers B. Strengths and limitations of genetic mouse models of Parkinson's disease. Parkinsonism Relat Disord 2008, 14:S84-S87.
12. Clarke P.G.H. How inaccurate is the Abercrombie correction factor for cell counts?. Trends Neurosci 1992, 15:211-212.
13. Cohen A.D., Tillerson J.L., Smith A.D., Schallert T., Zigmond M.J. Neuroprotective effects of prior limb use in 6-hydroxydopamine-treated rats: possible role of GDNF. J Neurochem 2003, 85:299-305.
14. Crawley J.N. Exploratory behavior models of anxiety in mice. Neurosci Biobehav Rev 1985, 9:37-44.
15. Crawley J.N., Hays S.E., Paul S.M., Goodwin F.K. Cholecystokinin reduces exploratory behavior in mice. Physiol Behav 1981, 27:407-411.
16. Date I., Yoshimoto Y., Takashi I., Yasuyuki M., Futura T., Asari S., Ohmoto T. Effect of host age upon the degree of nigrostriatal dopaminergic system recovery following cografts of adrenal medulla and pretransected peripheral nerve. Brain Res 1994, 637:50-56.
17. Faherty C.J., Shepherd K.R., Herasimtschuk A., Smeyne R.J. Environmental enrichment in adulthood eliminates neuronal death in experimental Parkinsonism. Brain Res Mol Brain Res 2005, 134:170-179.
18. Filipov N.M., Norwood A.B., Sistrunk S.C. Strain-specific sensitivity to MPTP of C57BL/6 and BALB/c mice is age dependent. Neuroreport 2009, 20(7):713-717.
19. Fornai F., Schulter O.M., Lenzi P., Gesi M., Ruffoli R., Ferrucci M., Lazzeri G., Busceti C.L., Pontarelli F., Battaglia G., Pellegrini A., Nicoletti F., Ruggieri S., Paprelli A., Sudhof T.C. Parkinson-like syndrome induced by continuous MPTP infusion: convergen roles of the ubiquitin-proteasome system and alpha-synuclein. Proc Natl Acad Sci U S A 2005, 102(9):3413-3418.
20. Frances H. New animals model of social behavioral deficit: reversal by drugs. Pharmacol Biochem Behav 1988, 29:467-470.
21. Freed C.R., Greene P.E., Breeze R.E., Tsai W.Y., DuMouchel W., Kao R. Transplantation of embryonic dopamine neurons for severe Parkinson's disease. N Engl J Med 2001, 344:710-719.
22. Geraerts M., Krylyshkina O., Debyser Z. Concise review: therapeutic strategies for Parkinson's disease based on the modulation of adult neurogenesis. Stem Cells 2007, 25(2):263-270.
23. Gerlach M., Riederer P., Przuntek H., Youdim B.H. MPTP mechanisms of neurotoxicity and their implications for Parkinson's disease. Eur J Pharmacol 1991, 208(4):273-286.
24. Gomez-Pinilla F., Dao L., So V. Physical exercise induces FGF-2 and its mRNA in the hippocampus. Brain Res 1997, 764:1-8.
25. Hawkes C.H., Tredici K.D., Braak H. A timeline for Parkinson's disease. Parkinsonism Relat Disord 2010, 16:79-84.
26. Ho A., Blum M. Induction of interleukin-1 associated with compensatory dopaminergic srpouting in the denerveated striatum of young mice: model of aging and neurodegenerative disease. J Neurosci 1998, 18(15):5614-5629.
27. Holmer H.K., Keyghobadi M., Moore C., Menashe R.A., Meshul C.K. Dietary restriction affects striatal glutamate in the MPTP-induced mouse model of nigrostriatal degeneration. Synapse 2005, 57:100-112.
28. Holmer H.K., Keyghobadi M., Moore C., Meshul C.K. L-dopa-induced reversal in striatal glutamate following partial depletion of nigrostriatal dopamine with MPTP. Neuroscience 2005, 136:333-341.
29. Irwin I., Finnegan K.T., Delanney L.E., Monte D.D., Langston J.W. The relationships between aging, monoamine oxidase, striatal dopamine and the effects of MPTP in C57BL/6 mice: a critical reassessment. Brain Res 1992, 572:224-231.
30. Jackson-Lewis V., Jakowec M., Burke R.E., Przedborski S. Time course and morphology of dopaminergic neuronal death caused by the neurotoxin 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. Neurodegeneration 1995, 4:257-269.
31. Jarvis M.F., Wagner G.C. Age-dependent effects of 1-methyl-4-phenyl-1,2,5,6-tetrahydropyridine (MPTP). Neuropharmacology 1985, 24(6):581-583.
32. Jenner P. Molecular mechanisms of L-DOPA-induced dyskinesia. Nat Rev Neurosci 2008, 9:665-677.
33. Kamens H.M., Crabbe J.C. The parallel rod floor test: a measure of ataxia in mice. Nat Protoc 2007, 2:277-281.
34. Li L., Tang B.L. Environmental enrichment and neurodegenerative diseases. Biochem Biophys Res Commun 2005, 334:293-297.
35. Lie D.C., Dziewczapolski G., Willhoite A.R., Kaspar B.K., Shults C.W., Gage F.H. The adult substantia nigra contains progenitor cells with neurogenic potential. J Neurosci 2002, 22(15):6639-6649.
36. Mayeux R., Stern Y., Rosenstein R., Marder K., Hauser A., Cote L., Fahn S. An estimate of the prevalence of dementia in idiopathic Parkinson's disease. Arch Neurol 1988, 45(3):260-262.
37. McNeill T.H., Koek L.L. Differential effects of advancing age on neurotransmitter cell loss in the substantia nigra and striatum of C57Bl/6N mice. Brain Res 1990, 521(12):107-117.
38. Mineur Y.S., Belzung C., Crusio W.E. Effects of unpredictable chronic mild stress on anxiety and depression-like behavior in mice. Behav Brain Res 2006, 175(1):43-50.
39. Mora F., Segovia G., del Arco A. Aging, plasticity and environmental enrichment: structural changes and neurotransmitter dynamics in several areas of the brain. Brain Res Rev 2007, 55(1):78-88.
40. Morellini F., Lepsveridze E., Kähler B., Dityatev A., Schachner M. Reduced reactivity to novelty, impaired social behavior, and enhanced basal synaptic excitatory activity in perforant path projections to the dentate gyrus in young adult mice deficient in the neural cell adhesion molecule CHL1. Mol Cell Neurosci 2007, 342:121-136.
41. Mori F., Nishie M., Kakita A., Yoshimoto M., Takahashi H., Wakabayashi K. Relationship among alpha-synuclein accumulation, dopamine synthesis, and neurodegeneration in substantia nigra. J Neuropathol Exp Neurol 2006, 65:808-815.
42. Ohashi S., Mori A., Kurihara N., Mitsumoto Y., Nakai M. Age-related severity of dopaminergic neurodegenerative neurotoxicity causes motor dysfunction in C57BL/6 mice. Neurosci Lett 2006, 401:183-187.
43. Oka H., Yoshioka M., Onouchi K., Morita M., Mochio S., Suzuki M., Hirai T., Ito Y., Inoue K. Characteristics of orthostatic hypotension in Parkinson's disease. Brain 2007, 130(Pt 9):2425-2432.
44. Olanow C.W., Goetz C.G., Kordower J.H., Stoessl A.J., Sossi V., Brin M.F., et al. A double-blind controlled trial of bilateral fetal nigral transplantation in Parkinson's disease. Ann Neurol 2003, 54:403-414.
45. O'Tuathaigh C.M.P., O'Connor A.M., O'Sullivan G.J., Lai D., Harvey R., Croke D.T., Waddington J.L. Disruption to social dyadic interactions but not emotional/anxiety-related behaviour in mice with heterozygous "knockout" of the schizophrenia risk gene neuregulin-1. Prog Neuropsychopharmacol Biol Psychiatry 2008, 32(2):462-466.
46. Pakkenberg B., Moller A., Gundersen H.J.G., Dam A.M., Pakkenberg H. The absolute number of nerve cells in substantia nigra in normal subjects and in patients with Parkinson's disease estimated with an unbiased stereological method. J Neurol Neurosurg Psychiatry 1991, 54:30-33.
47. Petroske E., Meredith G.E., Callen S., Totterdell S., Lau Y.S. Mouse model of Parkinsonism: a comparison between subacute MPTP and chronic MPTP/probenecid treatment. Neuroscience 2001, 106:589-601.
48. Piccini P., Brooks D.J., Bjorklund A., et al. Dopamine release from nigral transplants visualized in vivo in a Parkinson's patient. Nat Neurosci 1999, 12:1137-1140.
49. Quinn N., Critchely P., Marsden C.D. Young onset Parkinson's disease. Mov Disord 2004, 2(2):73-91.
50. Ricaurte G.A., DeLanney L.E., Irwin I., Langston J.W. Older dopaminergic neurons do not recover from the effects of MPTP. Neuropharmacology 1987, 26:97-99.
51. Ricaurte G.A., Irwin I., Forno L.S., DeLanney L.E., Langston E., Langston J.W. Aging and 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced degeneration of dopaminergic neurons in the substantia nigra. Brain Res 1987, 403:43-51.
52. Robinson S., Freeman P., Moore C., Touchon J.C., Krentz L., Meshul C.K. Acute and subchronic MPTP administration differentially affects striatal glutamate synaptic function. Exp Neurol 2003, 180:7-87.
53. Saitoh T., Niijima K., Mizuno Y. Long-term effect of 1-mthyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) on striatal dopamine content in young and mature mice. J Neurol Sci 1987, 77(23):229-235.
54. Schintu N., Frau L., Ibba M., Garau A., Carboni E., Carta A.R. Progressive dopaminergic degeneration in the chronic MPTPp mouse model of Parkinson's disease. Neurotox Res 2009, 16:127-139.
55. Schneider B., Zufferey R., Aebischer P. Viral vectors, animal models and new therapies for Parkinson's disease. Parkinsonism Relat Disord 2008, 2:S169-S171.
56. Schrag A., Schott J.M. Epidemiological, clinical and genetic characteristics of early-onset parkinsonism. Lancet Neurol 2006, 5:355-363.
57. Segovia G., Yague A.G., Garcia-Verdugo J.M., Mora F. Enrivonmental enrichment promotes neurogenesis and changes the extracellular concentrations of glutamate and GABA in the hippocampus of aged rats. Brain Res Bull 2006, 70(1):8-14.
58. Senard J.M., Lapeyre-Mestre M., Brefel C., Rascol O., Rascol A., Montastruc J.L. Prevalence of orthostatic hypotension in Parkinson's disease. J Neurol Neurosurg Psychiatry 1997, 63:584-589.
59. Shan X., Chi L., Bishop M., Luo C., Lien L., Zhang Z., Liu R. Enhanced de novo neurogenesis and dopaminergic neurogenesis in the substantia nigra of MPTP-induced Parkinson's disease-like mice. Stem Cells 2006, 24:1280-1287.
60. Smolen A.J., Wright L.L., Cunningham T.J. Neuron numbers in the superior cervical ganglion of the rat: a critical method of cell counting. J Neurocytol 1983, 12:739-750.
61. Steiner B., Winter C., Hosman K., Siebert E., Kempermann G., Petrus D.S., Kupsch A. Enriched environment induces cellular plasticity in the adult substantia nigra and improves motor behavior function in the 6-OHDA rat model of Parkinson's disease. Exp Neurol 2006, 199(2):291-300.
62. Tereshchenko Y., Brandewiede J., Schachner M., Irintchev A., Morellini F. Novelty-induced behavioral traits correlate with numbers of brainstem noradrenergic neurons and septal cholinergic neurons in C57BL/6J mice. Behav Brain Res 2008, 191(2):280-284.
63. Ünal-Çevik I., Kilinç M., Gürsoy-Özdemir Y., Gurer G., Dalkara T. Loss of NeuN immunoreactivity after cerebral ischemia does not indicate neuronal cell loss: a cautionary note. Brain Res 2004, 1015:169-174.
64. Van Kampen J.M., Eckman C.B. Dopamine D3 receptor agonist delivery to a model of Parkinson's disease restores the nigrostriatal pathway and improves locomotor behavior. J Neurosci 2006, 26(27):7272-7280.
65. Van Praag H., Kempermann G., Gage F.H. Neural consequences of environmental enrichment. Nat Rev Neurosci 2000, 1:191-198.
66. Xu Z., Cawthon D., McCastlain D.A., Slikker W., Ali S.F. Selective alterations of gene expression in mice induced by MPTP. Synapse 2005, 55:45-51.
67. Zhao M., Momma S., Delfani K., Carlen M., Cassidy R.M., Johansson C.B., Brismar H., Shupliakov O., Frisen J., Janson A.M. Evidence for neurogenesis in the adult mammalian substantia nigra. Proc Natl Acad Sci U S A 2003, 100:7925-7930.
68. Ziv Y., Ron N., Butovsky O., Landa G., Sudai E., Greenberg N., Cohen H., Kipnis J., Schwartz M. Immune cells contribute to the maintenance of neurogenesis and spatial learning abilities in adulthood. Nat Neurosci 2006, 9:268-275.