The first mecp2-null zebrafish model shows altered motor behaviors

Frontiers in Neural Circuits

Volumn , Issue JUL, 2013, Pages

  Pietri, Thomas ^a,b,c   Roman, Angel Carlos ^d   Guyon, Nicolas ^a,b,c   Romano, Sebastián A ^a,b,c   Washbourne, Philip ^e   Moens, Cecilia B ^f   de Polavieja, Gonzalo G ^d   Sumbre, Germán ^a,b,c  

^a PSL RESEARCH UNIVERSITY   (France)

^b INSERM   (France)

^c CNRS   (France)

^d INSTITUTO CAJAL   (Spain)

^e UNIVERSITY OF OREGON   (United States)

^f Fred Hutchinson Cancer Research Center   (United States)

Author keywords

Early development; Mecp2; Motor behavior; Rett syndrome; Thigmotaxis; Zebrafish

Indexed keywords

METHYL CPG BINDING PROTEIN 2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY; ARTICLE; CONTROLLED STUDY; EMBRYO; GENE MUTATION; LARVA; LOCOMOTION; MECP2 GENE; MOTOR ACTIVITY; MOTOR DEVELOPMENT; MOTOR DYSFUNCTION; NONHUMAN; RETT SYNDROME; SWIMMING;

EID: 84880589894     PISSN: 16625110     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncir.2013.00118     Document Type: Article

References (69)

1. Amir, R. E., Van den Veyver, I. B., Wan, M., Tran, C. Q., Francke, U., and 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. doi: 10.1038/13810
2. Anichtchik, O. V., Kaslin, J., Peitsaro, N., Scheinin, M., and Panula, P. (2004). Neurochemical and behavioural changes in zebrafish Danio rerio after systemic administration of 6-hydroxydopamine and 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. J. Neurochem. 88, 443-453. doi: 10.1111/j.1471-4159.2004.02190.x
3. Ballas, N., Lioy, D. T., Grunseich, C., and Mandel, G. (2009). Non-cell autonomous influence of MeCP2-deficient glia on neuronal dendritic morphology. Nat. Neurosci. 12, 311-317. doi: 10.1038/nn.2275
4. Beattie, C. E., Carrel, T. L., and McWhorter, M. L. (2007). Fishing for a mechanism: using zebrafish to understand spinal muscular atrophy. J. Child Neurol. 22, 995-1003. doi: 10.1177/0883073807305671
5. Belmonte, M. K., Cook, E. H. Jr., Anderson, G. M., Rubenstein, J. L., Greenough, W. T., Beckel-Mitchener, A., et al. (2004). Autism as a disorder of neural information processing: directions for research and targets for therapy. Mol. Psychiatry 9, 646-663.
6. Blue, M. E., Kaufmann, W. E., Bressler, J., Eyring, C., O'Driscoll, C., Naidu, S., et al. (2011). Temporal and regional alterations in NMDA receptor expression in MeCP2-null mice. Anat. Rec. (Hoboken) 294, 1624-1634. doi: 10.1002/ar.21380
7. Brennan, C. H. (2011). Zebrafish behavioural assays of translational relevance for the study of psychiatric disease. Rev. Neurosci. 22, 37-48. doi: 10.1515/rns.2011.006
8. Chahrour, M., Jung, S. Y., Shaw, C., Zhou, X., Wong, S. T. C., Qin, J., et al. (2008). MeCP2, a key contributor to neurological disease, activates and represses transcription. Science 320, 1224-1229. doi: 10.1126/science.1153252
9. Chao, H., Zoghbi, H. Y., and Rosenmund, C. (2007). MeCP2 controls excitatory synaptic strength by regulating glutamatergic synapse number. Neuron 56, 58-65. doi: 10.1016/j.neuron.2007.08.018
10. Chao, H., Chen, H., Samaco, R. C., Xue, M., Chahrour, M., Yoo, J., et al. (2010). Dysfunction in GABA signaling mediates autism-like stereotypies and Rett syndrome phenotypes. Nature 468, 263-269. doi: 10.1038/nature09582
11. Chen, R. Z., Akbarian, S., Tudor, M., and Jaenisch, R. (2001). Deficiency of methyl-CpC binding protein-2 in CNS neurons results in a Rett-like phenotype in mice. Nat. Genet. 27, 327-331. doi: 10.1038/85906
12. Colwill, R. M., and Creton, R. (2011) Locomotor behaviors in zebrafish (Danio rerio) larvae. Behav. Processes. 86, 222-229. doi: 10.1016/j.beproc.2010.12.003
13. Coverdale, L. E., Martyniuk C.J., Trudeau V.L., and Martin, C. C. (2004). Differential expression of the methyl-cytosine binding protein 2 gene in embryonic and adult brain of zebrafish. Brain Res. Dev. Brain Res. 153, 281-287. doi: 10.1016/j.devbrainres.2004.08.009
14. Cox, J. A., Kucenas, S., and Voigt, M. M. (2005) Molecular characterization and embryonic expression of the family of N-methyl-D-aspartate receptor subunit genes in the zebrafish. Dev. Dyn. 234, 756-766. doi: 10.1002/dvdy.20532
15. Curado, S., Anderson, R. M., Jungblut, B., Mumm, J., Schroeter, E., and Stainier, D. Y. R. (2007). Conditional targeted cell ablation in zebrafish: a new tool for regeneration studies. Dev. Dyn. 236, 1025-1035. doi: 10.1002/ dvdy.21100
16. Dani, V. S., Chang, Q., Maffei, A., Turrigiano, G. G., Jaenisch, R., and Nelson, S. B. (2005). Reduced cortical activity due to a shift in the balance between excitation and inhibition in a mouse model of Rett syndrome. Proc. Natl. Acad. Sci. U.S.A. 102, 12560-12565. doi: 10.1073/pnas.0506071102
17. Dichter, G. S., Damiano, C. A., and Allen, J. A. (2012). Reward circuitry dysfunction in psychiatric and neurodevelopmental disorders and genetic syndromes: animal models and clinical findings. J. Neurodev. Disord. 4:19. doi: 10.1186/1866-1955-4-19
18. Draper, B. W., McCallum, C. M., Stout, J. L., Slade, A. J., and Moens, C. B. (2004). A high-throughput method for identifying N-ethyl-N-nitrosourea (ENU)-induced point mutations in zebrafish. Methods Cell Biol. 77, 91-112. doi: 10.1016/S0091-679X (04)77005-3
19. Faure, P., Neumeister, H., Faber, D. S., and Korn, H. (2003). Symbolic analysis of swimming trajectories reveals scale invariance and provides a model for fish locomotion. Fractals 11, 233-243. doi: 10.1142/S0218348X03002166
20. Fetcho, J. R., and Faber, D. S. (1988). Identification of motoneurons and interneurons in the spinal network for escapes initiated by the mauthner cell in goldfish. J. Neurosci. 8, 4192-4213.
21. Gahtan, E., Sankrithi, N., Campos, J. B., and O'Malley, D. M. (2002). Evidence for a widespread brain stem escape network in larval zebrafish. J. Neurophysiol. 87, 608-614.
22. Gantz, S. C., Ford, C. P., Neve, K. A., and Williams, J. T. (2011). Loss of MeCP2 in substantia nigra dopamine neurons compromises the nigrostriatal pathway. J. Neurosci. 31, 12629-12637. doi: 10.1523/JNEUROSCI.0684-11.2011
23. Guy, J., Gan, J., Selfridge, J., Cobb, S., and Bird, A. (2007). Reversal of neurological defects in a mouse model of Rett syndrome. Science 315, 1143-1147. doi: 10.1126/science.1138389
24. Guy, J., Hendrich, B., Holmes, M., Martin, J. E., and Bird, A. (2001). A mouse MeCP2-null mutation causes neurological symptoms that mimic Rett syndrome. Nat. Genet. 27, 322-326. doi: 10.1038/85899
25. Harnos, A., Horvath, G., Lawrence, A. B., and Vattay, G. (2000). Scaling and intermittency in animal behavior. Physica A 286, 312-320. doi: 10.1016/S0378-4371(00)00332-0
26. Higashijima, S., Mandel, G., and Fetcho, J. (2004). Distribution of prospective glutamatergic, glycinergic, and GABAergic neurons in embryonic and larval zebrafish. J. Comp. Neurol. 480, 1-18. doi: 10.1002/cne.20278
27. Huang, P., Xiao, A., Zhou, M., Zhu, Z., Lin, S., and Zhang, B. (2011). Heritable gene targeting in zebrafish using customized TALENS. Nat. Biotechnol. 29, 699-700. doi: 10.1038/nbt.1939
28. Kabashi, E., Brustein, E., Champagne, N., and Drapeau, P. (2011). Zebrafish models for the functional genomics of neurogenetic disorders. Biochim. Biophys. Acta 1812, 335-345. doi: 10.1016/j.bbadis. 2010.09.011
29. Kimmel, C. B., Hatta, K., and Metcalfe, W. K. (1990). Early axonal contacts during development of an identified dendrite in the brain of the zebrafish. Neuron 4, 535-545. doi: 10.1016/0896-6273(90)90111
30. R Kron, M., Howell, C. J., Adams, I. T., Ransbottom, M., Christian, D., Ogier, M., et al. (2012). Brain activity mapping in MeCP2 mutant mice reveals functional deficits in forebrain circuits, including key nodes in the default mode network, that are reversed with ketamine treatment. J. Neurosci. 32, 13860-13872. doi: 10.1523/JNEUROSCI.2159-12.2012
31. Kuwada, J. Y., Bernhardt, R. R., and Nguyen, N. (1990). Development of spinal neurons and tracts in the zebrafish embryo. J. Comp. Neurol. 302, 617-628. doi: 10.1002/cne.903020316
32. Lewis, J. D., Meehan, R. R., Henzel, W. J., Maurer-Fogy, I., Jeppesen, P., Klein, F., et al. (1992). Purification, sequence, and cellular localization of a novel chromosomal protein that binds to methylated DNA. Cell 69, 905-914. doi: 10.1016/0092-8674(92)90610-O
33. Lioy, D. T., Garg, S. K., Monaghan, C. E., Raber, J., Foust, K. D., Kaspar, B. K., et al. (2011). A role for glia in the progression of Rett's syndrome. Nature 475, 497-500. doi: 10.1038/nature10214
34. Liu, K. S., and Fetcho, J. R. (1999). Laser ablations reveal functional relationships of segmental hind-brain neurons in zebrafish. Neuron 23, 325-335. doi: 10.1016/S0896-6273(00)80783-7
35. Liu, Y., Bailey, I., and Hale, M. E. (2012). Alternative startle motor patterns and behaviors in the larval zebrafish (Danio rerio). J. Comp. Physiol. A Neuroethol. Sens. Neural. Behav. Physiol. 198, 11-24. doi: 10.1007/s00359-011-0682-1
36. Matsuishi, T., Yamashita, Y., Takahashi, T., and Nagamitsu, S. (2011). Rett syndrome: the state of clinical and basic research, and future perspectives. Brain Dev. 33, 627-631. doi: 10.1016/j.braindev.2010.12.007
37. Medrihan, L., Tantalaki, E., Aramuni, G., Sargsyan, V., Dudanova, I., Missler, M., et al. (2008). Early defects of GABAergic synapses in the brain stem of a MeCP2 mouse model of Rett syndrome. J. Neurophysiol. 99, 112-121. doi: 10.1152/jn.00826.2007
38. Moretti, P., Bouwknecht, J. A., Teague, R., Paylor, R., and Zoghbi, H. Y. (2005). Abnormalities of social interactions and home-cage behavior in a mouse model of Rett syndrome. Hum. Mol. Genet. 14, 205-220. doi: 10.1093/ hmg/ddi016
39. Moretti, P., Levenson, J. M., Battaglia, F., Atkinson, R., Teague, R., Antalffy, B., et al. (2006). Learning and memory and synaptic plasticity are impaired in a mouse model of Rett syndrome. J. Neurosci. 26, 319-327. doi: 10.1523/JNEUROSCI.2623-05.2006
40. Morris, J. A. (2009). Zebrafish: a model system to examine the neurodevelopmental basis of schizophrenia. Prog. Brain Res. 179, 97-106. doi: 10.1016/S0079-6123 (09)17911-6
41. Ng, H. H., Zhang, Y., Hendrich, B., Johnson, C. A., Turner, B. M., Erdjument-Bromage, H., et al. (1999). MBD2 is a transcriptional repressor belonging to the MeCP1 histone deacetylase complex. Nat. Genet. 23, 58-61. doi: 10.1038/12659
42. O'Malley, D. M., Kao, Y.-H, and Fetcho, J. R. (1996). Imaging the functional organization of zebrafish hindbrain segments during escape behaviors. Neuron 17, 1145-1155. doi: 10.1016/S0896-6273(00)80246-9
43. Panayotis, N., Ghata, A., Villard, L., and Roux, J. C. (2011). Biogenic amines and their metabolites are differentially affected in the MeCP2-deficient mouse brain. BMC Neurosci. 12:47. doi: 10.1186/1471-2202-12-47
44. Panula, P., Sallinen, V., Sundvik, M., Kolehmainen, J., Torkko, V., Tiittula, A., et al. (2006). Modulatory neurotransmitter systems and behavior: towards zebrafish models of neurodegenerative diseases. Zebrafish 3, 235-247. doi: 10.1089/zeb.2006.3.235
45. Paylor, R., Nguyen, M., Crawley, J. N., Patrick, J., Beaudet, A., and Orr-Urtreger, A. (1998). Alpha7 nicotinic receptor subunits are not necessary for hippocampal-dependent learning or sensorimotor gating: a behavioral characterization of Acra7-deficient mice. Learn Mem. 5, 302-316.
46. Picker, J. D., Yang, R., Ricceri, L., and Berger-Sweeney, J. (2006). An altered neonatal behavioral phenotype in mecp2 mutant mice. Neuroreport 17, 541-544. doi: 10.1097/01.wnr.0000208995. 38695.2f
47. Pietri, T., Manalo, E., Ryan, J., Saint-Amant, L., and Washbourne, P. (2009). Glutamate drives the touch response through a rostral loop in the spinal cord of zebrafish embryos. Dev. Neurobiol. 69, 780-795. doi: 10.1002/dneu.20741
48. Peitsaro, N., Kaslin, J., Anichtchik, O. V., and Panula, P. (2003). Modulation of the histaminergic system and behaviour by alphafluoromethylhistidine in zebrafish. J. Neurochem. 86, 432-441. doi: 10.1046/j.1471-4159.2003.01850.x
49. Postlethwait, J., Amores, A., Cresko, W., Singer, A., and Yan, Y. L. (2004). Subfunction partitioning, the teleost radiation and the annotation of the human genome. Trends Genet. 20, 481-490. doi: 10.1016/j.tig.2004.08.001
50. Saint-Amant, L. (2010). Development of motor rhythms in zebrafish embryos. Prog. Brain Res. 187, 47-61. doi: 10.1016/B978-0-44453613-6.00004-6
51. Saint-Amant, L., and Drapeau, P. (1998). Time course of the development of motor behaviors in the zebrafish embryo. J. Neurobiol. 37, 622-632.
52. Saint-Amant, L., and Drapeau, P. (2000). Motoneuron activity patterns related to the earliest behavior of the zebrafish embryo. J. Neurosci. 20, 3964-3972.
53. Saint-Amant, L., and Drapeau, P. (2001). Synchronization of an embryonic network of identified spinal interneurons solely by electrical coupling. Neuron 31, 1035-1046. doi: 10.1016/S0896-6273(01)00416-0
54. Samaco, R. C., Mandel-Brehm, C., Chao, H. T., Ward, C. S., Fyffe-Maricich, S. L., Ren, J., et al. (2009). Loss of MeCP2 in aminergic neurons causes cell-autonomous defects in neurotransmitter synthesis and specific behavioral abnormalities. Proc. Natl. Acad. Sci. U.S.A. 106, 21966-21971. doi: 10.1073/pnas.0912257106
55. Santos, M., Silva-Fernandes, A., Oliveira, P., Sousa, N., and Maciel, P. (2007). Evidence for abnormal early development in a mouse model of Rett syndrome. Genes Brain Behav. 6, 277-286. doi: 10.1111/j.1601-183X.2006.00258.x
56. Scott-Van Zeeland, A. A., Dapretto, M., Ghahremani, D. G., Poldrack, R. A., and Bookheimer, S. Y. (2010). Reward processing in autism. Autism Res. 3, 53-67.
57. Shahbazian, M. D., Antalffy, B., Armstrong, D. L., and Zoghbi, H. Y. (2002a). Insight into Rett syndrome: MeCP2 levels display tissue-and cell-specific differences and correlate with neuronal maturation. Hum. Mol. Genet. 11, 115-124. doi: 10.1093/hmg/11.2.115
58. Shahbazian, M. D., Young, J., Yuva-Paylor, L., Spencer, C., Antalffy, B., Noebels, J., et al. (2002b). Mice with truncated MeCP2 recapitulate many Rett syndrome features and display hyperacetylation of histone H3. Neuron 35, 243-254. doi: 10.1016/S0896-6273(02)00768-7
59. Skene, P. J., Illingworth, R. S., Webb, S., Kerr, A. R. W., James, K. D., Turner, D. J., et al. (2010). Neuronal MeCP2 is expressed at near histone-octamer levels and globally alters the chromatin state. Mol. Cell 37, 457-468. doi: 10.1016/j.molcel.2010.01.030
60. Schnorr, S. J., Steenbergen, P. J., Richardson, M. K., and Champagne, D. L. (2012). Measuring thigmotaxis in larval zebrafish. Behav. Brain Res. 228, 367-374. doi: 10.1016/j.bbr.2011.12.016
61. Stearns, N. A., Schaevitz, L. R., Bowling, H., Nag, N., Berger, U. V., and Berger-Sweeney, J. (2007). Behavioral and anatomical abnormalities in mecp2 mutant mice: a model for Rett syndrome. Neuroscience 146, 907-921. doi: 10.1016/j.neuroscience.2007.02.009
62. Steenbergen, P. J., Richardson, M. K., and Champagne, D. L. (2011). The use of the zebrafish model in stress research. Prog. Neuropsychopharmacol. Biol. Psychiatry 35, 1432-1451. doi: 10.1016/j.pnpbp.2010.10.010
63. Thirumalai, V., and Cline, H. T. (2008). Endogenous dopamine suppresses initiation of swimming in prefeeding zebrafish larvae. J. Neurophysiol. 100, 1635-1648. doi: 10.1152/jn.90568.2008
64. Westerfield, M. (2000). The Zebrafish Book a Guide for the Laboratory Use of Zebrafish Danio (Brachydanio) rerio. 4th edn. Eugene, OR: University of Oregon Press.
65. Wood, S. J., and Toth, M. (2001). Molecular pathways of anxiety revealed by knockout mice. Mol. Neurobiol. 2, 101-119.
66. Xi, Y., Noble, S., and Ekker, M. (2011). Modeling neurodegeneration in zebrafish. Curr. Neurol. Neurosci. Rep. 11, 274-282. doi: 10.1007/s11910-011-0182-2
67. Yasui, D. H., Peddada, S., Bieda, M. C., Vallero, R. O., Hogart, A., Nagarajan, R. P., et al. (2007). Integrated epigenomic analyses of neuronal MeCP2 reveal a role for long-range interaction with active genes. Proc. Natl. Acad. Sci. U.S.A. 104, 19416-19421. doi: 10.1073/pnas.0707442104
68. Young, J. I., Hong, E. P., Castle, J. C., Crespo-Barreto, J., Bowman, A. B., Rose, M. F., et al. (2005). Regulation of RNA splicing by the methylation-dependent transcriptional repressor methyl-CpG binding protein 2. Proc. Natl. Acad. Sci. U.S.A. 102, 17551-17558. doi: 10.1073/pnas.0507856102
69. Zupanc, G. K. H. (2008). Adult neurogenesis and neuronal regeneration in the brain of teleost fish. J. Physiol. Paris 102, 357-373. doi: 10.1016/j.jphysparis.2008.10.007