Environmental enrichment ameliorates a motor coordination deficit in a mouse model of Rett syndrome - Mecp2 gene dosage effects and BDNF expression

European Journal of Neuroscience

Volumn 27, Issue 12, 2008, Pages 3342-3350

  Kondo, Mari ^a   Gray, Laura J ^a   Pelka, Gregory J ^b   Christodoulou, John ^c,d   Tam, Patrick P L ^b,e   Hannan, Anthony J ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b CHILDREN'S MEDICAL RESEARCH INSTITUTE   (Australia)

^c CHILDREN S HOSPITAL AT WESTMEAD   (Australia)

^d UNIVERSITY OF SYDNEY   (Australia)

^e University of Sydney   (Australia)

Author keywords

BDNF; Behaviour; Gene environment interactions; MeCP2; Rett syndrome

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; METHYL CPG BINDING PROTEIN 2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN LEVEL; CEREBELLUM; CONTROLLED STUDY; ENVIRONMENTAL ENRICHMENT; FEMALE; GENE DOSAGE; HETEROZYGOSITY; MALE; MOTOR COORDINATION; MOUSE; MUTANT; NONHUMAN; NULL ALLELE; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETT SYNDROME; ROTAROD TEST; TRAINING; WILD TYPE;

ANIMALS; BEHAVIOR, ANIMAL; BRAIN-DERIVED NEUROTROPHIC FACTOR; CEREBELLUM; CEREBRAL CORTEX; CONDITIONING (PSYCHOLOGY); CORPUS STRIATUM; DISEASE MODELS, ANIMAL; ENVIRONMENT; FEMALE; GENE DOSAGE; HIPPOCAMPUS; MALE; METHYL-CPG-BINDING PROTEIN 2; MICE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; MOTOR ACTIVITY; NEURONAL PLASTICITY; RETT SYNDROME;

EID: 45349089199     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2008.06305.x     Document Type: Article

References (48)

1. Amir, R.E., Van den Veyver, I.B., Wan, M., Tran, C.Q., Francke, U. Zoghbi, H.Y. (1999) Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2. Nat. Genet., 23, 185 188.
2. Arendash, G.W., Garcia, M.F., Costa, D.A., Cracchiolo, J.R., Wefes, I.M. Potter, H. (2004) Environmental enrichment improves cognition in aged Alzheimer's transgenic mice despite stable beta-amyloid deposition, Neuroreport. Neuroreport, 15, 1751 1754.
3. Bezard, E., Dovero, S., Belin, D., Duconger, S., Jackson-Lewis, V., Przedborski, S., Piazza, P.V., Gross, C.E. Jaber, M. (2003) 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., 23, 10999 11007.
4. Bienvenu, T. Chelly, J. (2006) Molecular genetics of Rett syndrome: when DNA methylation goes unrecognized, Nat Rev Genet, 7, 415 426.
5. Chahrour, M. Zoghbi, H.Y. (2007) The story of Rett syndrome: from clinic to neurobiology. Neuron, 56, 422 437.
6. Chang, Q., Khare, G., Dani, V., Nelson, S. Jaenisch, R. (2006) The disease progression of Mecp2 mutant mice is affected by the level of BDNF expression. Neuron, 49, 341 348.
7. Chao, H.T., Zoghbi, H.Y. Rosenmund, C. (2007) MeCP2 controls excitatory synaptic strength by regulating glutamatergic synapse number. Neuron, 56, 58 65.
8. Chen, R.Z., Akbarian, S., Tudor, M. Jaenisch, R. (2001) Deficiency of methyl-CpG binding protein-2 in CNS neurons results in a Rett-like phenotype in mice. Nat. Genet., 27, 327 331.
9. Chen, W.G., Chang, Q., Lin, Y., Meissner, A., West, A.E., Griffith, E.C., Jaenisch, R. Greenberg, M.E. (2003) Derepression of BDNF transcription involves calcium-dependent phosphorylation of MeCP2. Science, 302, 885 889.
10. Christodoulou, J. Weaving, L.S. (2003) MECP2 and beyond: phenotype-genotype correlations in Rett syndrome, J. Child Neurol., 18, 669 674.
11. Clarke, A., Schanen, C. Anvret, M. (2001) Toward the genetic basis of Rett syndrome. In Kerr, A. Witt-Engerström, I. (eds Rett Disorder and the Developing Brain. Oxford University Press, New York, pp. 27 55.
12. Collins, A.L., Levenson, J.M., Vilaythong, A.P., Richman, R., Armstrong, D.L., Noebels, J.L., David Sweatt, J. Zoghbi, H.Y. (2004) Mild overexpression of MeCP2 causes a progressive neurological disorder in mice. Hum. Mol. Genet., 13, 2679 2689.
13. Crawley, J.N. (2007) What's wrong with my mouse? : behavioral phenotyping of transgenic and knockout mice. Wiley-Interscience, Hoboken, N.J.
14. van Dellen, A., Blakemore, C., Deacon, R., York, D. Hannan, A.J. (2000) Delaying the onset of Huntington's in mice. Nature, 404, 721 722.
15. Giacometti, E., Luikenhuis, S., Beard, C. Jaenisch, R. (2007) Partial rescue of MeCP2 deficiency by postnatal activation of MeCP2. Proc. Natl Acad. Sci. U. S. A., 104, 1931 1936.
16. Guy, J., Hendrich, B., Holmes, M., Martin, J.E. Bird, A. (2001) A mouse Mecp2-null mutation causes neurological symptoms that mimic Rett syndrome. Nat. Genet., 27, 322 326.
17. Guy, J., Gan, J., Selfridge, J., Cobb, S. Bird, A. (2007) Reversal of neurological defects in a mouse model of Rett syndrome. Science, 315, 1143 1147.
18. Hockly, E., Cordery, P.M., Woodman, B., Mahal, A., van Dellen, A., Blakemore, C., Lewis, C.M., Hannan, A.J. Bates, G.P. (2002) Environmental enrichment slows disease progression in R6/2 Huntington's disease mice. Ann. Neurol., 51, 235 242.
19. Jankowsky, J.L., Melnikova, T., Fadale, D.J., Xu, G.M., Slunt, H.H., Gonzales, V., Younkin, L.H., Younkin, S.G., Borchelt, D.R. Savonenko, A.V. (2005) Environmental enrichment mitigates cognitive deficits in a mouse model of Alzheimer's disease. J. Neurosci., 25, 5217 5224.
20. Jugloff, D.G., Logan, R. Eubanks, J.H. (2006) Breeding and maintenance of an Mecp2-deficient mouse model of Rett syndrome. J. Neurosci. Methods, 154, 89 95.
21. Kempermann, G., Kuhn, H.G. Gage, F.H. (1997) More hippocampal neurons in adult mice living in an enriched environment. Nature, 386, 493 495.
22. Kishi, N. Macklis, J.D. (2004) MECP2 is progressively expressed in post-migratory neurons and is involved in neuronal maturation rather than cell fate decisions. Mol. Cell. Neurosci., 27, 306 321.
23. LaSalle, J.M. (2004) Paradoxical role of methyl-CpG-binding protein 2 in Rett syndrome. Curr. Top. Dev. Biol., 59, 61 86.
24. Lazarov, O., Robinson, J., Tang, Y.P., Hairston, I.S., Korade-Mirnics, Z., Lee, V.M., Hersh, L.B., Sapolsky, R.M., Mirnics, K. Sisodia, S.S. (2005) Environmental enrichment reduces Abeta levels and amyloid deposition in transgenic mice. Cell, 120, 701 713.
25. Martinez-Cue, C., Baamonde, C., Lumbreras, M., Paz, J., Davisson, M.T., Schmidt, C., Dierssen, M. Florez, J. (2002) Differential effects of environmental enrichment on behavior and learning of male and female Ts65Dn mice, a model for Down syndrome. Behav. Brain Res., 134, 185 200.
26. Martinowich, K., Hattori, D., Wu, H., Fouse, S., He, F., Hu, Y., Fan, G. Sun, Y.E. (2003) DNA methylation-related chromatin remodeling in activity-dependent BDNF gene regulation. Science, 302, 890 893.
27. McOmish, C.E., Burrows, E., Howard, M., Scarr, E., Kim, D., Shin, H.S., Dean, B., van den Buuse, M. Hannan, A.J. (2007) Phospholipase C-beta1 knockout mice exhibit endophenotypes modeling schizophrenia which are rescued by environmental enrichment and clozapine administration. Mol Psychiatry Epub 31 Jul 2007).
28. Migeon, B.R., Dunn, M.A., Thomas, G., Schmeckpeper, B.J. Naidu, S. (1995) Studies of X inactivation and isodisomy in twins provide further evidence that the X chromosome is not involved in Rett syndrome. Am. J. Hum. Genet., 56, 647 653.
29. Nan, X., Ng, H.H., Johnson, C.A., Laherty, C.D., Turner, B.M., Eisenman, R.N. Bird, A. (1998) Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature, 393, 386 389.
30. Nithianantharajah, J. Hannan, A.J. (2006) Enriched environments, experience-dependent plasticity and disorders of the nervous system. Nat Rev Neurosci, 7, 697 709.
31. Nithianantharajah, J., Barkus, C., Murphy, M. Hannan, A.J. (2008) Gene-environment interactions modulating cognitive function and molecular correlates of synaptic plasticity in Huntington's disease transgenic mice. Neurobiol Dis, 29, 490 504.
32. Ogawa, A., Mitsudome, A., Yasumoto, S. Matsumoto, T. (1997) Japanese monozygotic twins with Rett syndrome. Brain Dev., 19, 568 570.
33. Pang, T.Y., Stam, N.C., Nithianantharajah, J., Howard, M.L. Hannan, A.J. (2006) Differential effects of voluntary physical exercise on behavioral and brain-derived neurotrophic factor expression deficits in Huntington's disease transgenic mice. Neuroscience, 141, 569 584.
34. Pelka, G.J., Watson, C.M., Radziewic, T., Hayward, M., Lahooti, H., Christodoulou, J. Tam, P.P. (2006) Mecp2 deficiency is associated with learning and cognitive deficits and altered gene activity in the hippocampal region of mice. Brain, 129, 887 898.
35. van Praag, H., Kempermann, G. Gage, F.H. (2000) Neural consequences of environmental enrichment. Nat Rev Neurosci, 1, 191 198.
36. Rampon, C., Jiang, C.H., Dong, H., Tang, Y.P., Lockhart, D.J., Schultz, P.G., Tsien, J.Z. Hu, Y. (2000) Effects of environmental enrichment on gene expression in the brain. Proc. Natl Acad. Sci. U. S. A., 97, 12880 12884.
37. Restivo, L., Ferrari, F., Passino, E., Sgobio, C., Bock, J., Oostra, B.A., Bagni, C. Ammassari-Teule, M. (2005) Enriched environment promotes behavioral and morphological recovery in a mouse model for the fragile X syndrome. Proc. Natl Acad. Sci. U. S. A., 102, 11557 11562.
38. Scala, E., Longo, I., Ottimo, F., Speciale, C., Sampieri, K., Katzaki, E., Artuso, R., Mencarelli, M.A., D'Ambrogio, T., Vonella, G., Zappella, M., Hayek, G., Battaglia, A., Mari, F., Renieri, A. Ariani, F. (2007) MECP2 deletions and genotype-phenotype correlation in Rett syndrome. Am J Med Genet A, 143, 2775 2784.
39. Shahbazian, M., Young, J., Yuva-Paylor, L., Spencer, C., Antalffy, B., Noebels, J., Armstrong, D., Paylor, R. Zoghbi, H. (2002) Mice with truncated MeCP2 recapitulate many Rett syndrome features and display hyperacetylation of histone H3. Neuron, 35, 243 254.
40. Spires, T.L., Grote, H.E., Varshney, N.K., Cordery, P.M., van Dellen, A., Blakemore, C. Hannan, A.J. (2004) Environmental enrichment rescues protein deficits in a mouse model of Huntington's disease, indicating a possible disease mechanism. J. Neurosci., 24, 2270 2276.
41. Stearns, N.A., Schaevitz, L.R., Bowling, H., Nag, N., Berger, U.V. Berger-Sweeney, J. (2007) Behavioral and anatomical abnormalities in Mecp2 mutant mice: a model for Rett syndrome. Neuroscience, 146, 907 921.
42. Wang, H., Chan, S.A., Ogier, M., Hellard, D., Wang, Q., Smith, C. Katz, D.M. (2006) Dysregulation of brain-derived neurotrophic factor expression and neurosecretory function in Mecp2 null mice. J. Neurosci., 26, 10911 10915.
43. Watson, C.M., Pelka, G.J., Radziewic, T., Shahbazian, M.D., Christodoulou, J., Williamson, S.L. Tam, P.P. (2005) Reduced proportion of Purkinje cells expressing paternally derived mutant Mecp2308 allele in female mouse cerebellum is not due to a skewed primary pattern of X-chromosome inactivation. Hum. Mol. Genet., 14, 1851 1861.
44. Williamson, S.L. Christodoulou, J. (2006) Rett syndrome: new clinical and molecular insights. Eur. J. Hum. Genet., 14, 896 903.
45. Wolf, S.A., Kronenberg, G., Lehmann, K., Blankenship, A., Overall, R., Staufenbiel, M. Kempermann, G. (2006) Cognitive and physical activity differently modulate disease progression in the amyloid precursor protein (APP)-23 model of Alzheimer's disease. Biol. Psychiatry, 60, 1314 1323.
46. Wolfer, D.P., Crusio, W.E. Lipp, H.P. (2002) Knockout mice: simple solutions to the problems of genetic background and flanking genes. Trends Neurosci., 25, 336 340.
47. Young, J.I. Zoghbi, H.Y. (2004) X-chromosome inactivation patterns are unbalanced and affect the phenotypic outcome in a mouse model of rett syndrome. Am. J. Hum. Genet., 74, 511 520.
48. Zhou, Z., Hong, E.J., Cohen, S., Zhao, W.N., Ho, H.Y., Schmidt, L., Chen, W.G., Lin, Y., Savner, E., Griffith, E.C., Hu, L., Steen, J.A., Weitz, C.J. Greenberg, M.E. (2006) Brain-specific phosphorylation of MeCP2 regulates activity-dependent Bdnf transcription, dendritic growth, and spine maturation. Neuron, 52, 255 269.