Mouse models of Rett syndrome: From behavioural phenotyping to preclinical evaluation of new therapeutic approaches

Behavioural Pharmacology

Volumn 19, Issue 5-6, 2008, Pages 501-517

  Ricceri, Laura ^a   De Filippis, Bianca ^a   Laviola, Giovanni ^a  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

Author keywords

Behavioural development; Methyl CpG binding protein 2 gene; Mouse; Neurotrophins; Presymptomatic phase; Ultrasound vocalizations

Indexed keywords

1,4 BENZODIOXAN 6 CARBOXYLIC ACID PIPERIDIDE; BIOLOGICAL MARKER; DESIPRAMINE; METHYL CPG BINDING PROTEIN 2; ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; MECP2 PROTEIN, MOUSE; PSYCHOTROPIC AGENT; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; BEHAVIOR; CLINICAL FEATURE; DRUG MECHANISM; FEMALE; HUMAN; LIFESPAN; MOUSE; MOUSE MUTANT; MUTATION; NONHUMAN; PATHOPHYSIOLOGY; PHENOTYPE; RETT SYNDROME; REVIEW; SYMPTOM; ANIMAL; BRAIN; DISEASE MODEL; DRUG POTENTIATION; DRUG SCREENING; GENE THERAPY; GENETIC EPIGENESIS; GENETICS; METABOLISM; TRANSGENIC MOUSE;

ALPHA-AMINO-3-HYDROXY-5-METHYL-4-ISOXAZOLEPROPIONIC ACID; ANIMALS; BRAIN; DESIPRAMINE; DISEASE MODELS, ANIMAL; DRUG EVALUATION, PRECLINICAL; EPIGENESIS, GENETIC; FEMALE; GENE THERAPY; HUMANS; METHYL-CPG-BINDING PROTEIN 2; MICE; MICE, TRANSGENIC; PHENOTYPE; PSYCHOTROPIC DRUGS; RETT SYNDROME;

EID: 58149340280     PISSN: 09558810     EISSN: None     Source Type: Journal    
DOI: 10.1097/FBP.0b013e32830c3645     Document Type: Review

References (92)

1. Adachi M, Monteggia LM (2007). The effect of basolateral amygdala-specific loss of MeCP2 on behavioural phenotypes. In: Conference Book:54.13, Society for Neuroscience: San Diego. Alvarez-Saavedra M, Saez MA, Kang D, Zoghbi HY, Young JI (2007). Cell-specific expression of wild-type MeCP2 in mouse models of Rett syndrome yields insight about pathogenesis. Hum Mol Genet 16:2315-2325.
2. Amir RE, Van Den Veyver IB, Wan M, Tran CQ, Francke U, Zoghbi HY (1999). Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2. Nat Genet 23:185-188.
3. Asaka Y, Jugloff DG, Zhang L, Eubanks JH, Fitzsimonds RM (2006). Hippocampal synaptic plasticity is impaired in the Mecp2-null mouse model of Rett syndrome. Neurobiol Dis 21:217-227.
4. Belichenko NP, Belichenko PV, Li HH, Mobley WC, Francke U (2008). Comparative study of brain morphology in Mecp2 mutant mouse models of Rett syndrome. J Comp Neurol 508:184-195.
5. Bell MD, Fiszdon J, Bryson G, Wexler BE (2004). Effects of neurocognitive enhancement therapy in schizophrenia: normalisation of memory performance. Cogn Neuropsychiatry 9:199-211.
6. Bienvenu T, Chelly J (2006). Molecular genetics of Rett syndrome: when DNA methylation goes unrecognized. Nat Rev Genet 7:415-426.
7. Bignami G (1996). Economical test methods for developmental neurobehavioral toxicity. Environ Health Perspect 104 (Suppl 2):285-298.
8. Bissonnette JM, Knopp SJ (2006). Separate respiratory phenotypes in methyl-CpG-binding protein 2 (Mecp2) deficient mice. Pediatr Res 59:513-518.
9. Branchi I, Ricceri L (2002). Transgenic and knock-out mouse pups: the growing need for behavioral analysis. Genes Brain Behav 1:135-141.
10. Branchi I, D'Andrea I, Fiore M, Di Fausto V, Aloe L, Alleva E (2006). Early social enrichment shapes social behavior and nerve growth factor and brain-derived neurotrophic factor levels in the adult mouse brain. Biol Psychiatry 60:690-696
11. Chadwick LH, Wade PA (2007). MeCP2 in Rett syndrome: transcriptional repressor or chromatin architectural protein? Curr Opin Genet Dev 17:121-125.
12. Chahrour M, Zoghbi HY (2007). The story of Rett syndrome: from clinic to neurobiology. Neuron 56:422-437.
13. 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.
14. Chao HT, Zoghbi HY, Rosenmund C (2007). MeCP2 controls excitatory synaptic strength by regulating glutamatergic synapse number. Neuron 56:58-65.
15. Charman T, Cass H, Owen L, Wigram T, Slonims V, Weeks L, et al. (2002). Regression in individuals with Rett syndrome. Brain Dev 24:281-283.
16. Chen RZ, 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.
17. Chen WG, Chang Q, Lin Y, Meissner A, West AE, Griffith EC, et al. (2003). Derepression of BDNF transcription involves calcium-dependent phosphor-ylation of MeCP2. Science 302:885-889.
18. Collins AL, Levenson JM, Vilaythong AP, Richman R, Armstrong DL, Noebels JL, et al. (2004). Mild overexpression of MeCP2 causes a progressive neurological disorder in mice. Hum Mol Genet 13:2679-2689.
19. Crawley JN (2007). Mouse behavioral assays relevant to the symptoms of autism. Brain Pathol 17:448-459.
20. Dani VS, Chang Q, Maffei A, Turrigiano GG, Jaenisch R, Nelson SB (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.
21. Darnaudery M, Maccari S (2008). Epigenetic programming of the stress response in male and female rats by prenatal restraint stress. Brain Res Rev 57:571-585.
22. Deng V, Matagne V, Banine F, Frerking M, Ohliger P, Budden S, et al. (2007). FXYD1 is an MeCP2 target gene overexpressed in the brains of Rett syndrome patients and Mecp2-null mice. Hum Mol Genet 16:640-650.
23. Dragich J, Houwink-Manville I, Schanen C (2000). Rett syndrome: a surprising result of mutation in MECP2. Hum Mol Genet 9:2365-2375.
24. Einspieler C, Kerr AM, Prechtl HF (2005). Is the early development of girls with Rett disorder really normal? Pediatr Res 57:696-700.
25. Erlandson A, Hagberg B (2005). MECP2 abnormality phenotypes: clinicopatho-logic area with broad variability. J Child Neurol 20:727-732.
26. Fox WM (1965). Reflex-ontogeny and behavioral development of the mouse. Anim Behav 13:234-240.
27. Gemelli T, Berton O, Nelson ED, Perrotti LI, Jaenisch R, Monteggia LM (2006). Postnatal loss of methyl-CpG binding protein 2 in the forebrain is sufficient to mediate behavioral aspects of Rett syndrome in mice. Biol Psychiatry 59:468-476.
28. 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.
29. Guy J, Hendrich B, Holmes M, Martin JE, Bird A (2001). A mouse Mecp2-null mutation causes neurological symptoms that mimic Rett syndrome. Nat Genet 27:322-326.
30. 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.
31. Hagberg B (2002). Clinical manifestations and stages of Rett syndrome. Ment Retard Dev Disabil Res Rev 8:61-65.
32. Hoffbuhr KC, Moses LM, Jerdonek MA, Naidu S, Hoffman EP (2002). Associations between MeCP2 mutations, X-chromosome inactivation, and phenotype. Ment Retard Dev Disabil Res Rev 8:99-105.
33. Hogart A, Nagarajan RP, Patzel KA, Yasui DH, Lasalle JM (2007). 15q11-13 GABAA receptor genes are normally biallelically expressed in brain yet are subject to epigenetic dysregulation in autism-spectrum disorders. Hum Mol Genet 16:691-703.
34. Horike S, Cai S, Miyano M, Cheng JF, Kohwi-Shigematsu T (2005). Loss of silent-chromatin looping and impaired imprinting of DLX5 in Rett syndrome. Nat Genet 37:31-40.
35. Ide S, Itoh M, Goto Y (2005). Defect in normal developmental increase of the brain biogenic amine concentrations in the mecp2-null mouse. Neurosci Lett 386:14-17.
36. Jordan C, Francke U (2006). Ube3a expression is not altered in Mecp2 mutant mice. Hum Mol Genet 15:2210-2215.
37. Jorgensen HF, Bird A (2002). MeCP2 and other methyl-CpG binding proteins. Ment Retard Dev Disabil Res Rev 8:87-93.
38. Jugloff DG, Vandamme K, Logan R, Visanji NP, Brotchie JM, Eubanks JH (2008). Targeted delivery of an Mecp2 transgene to forebrain neurons improves the behavior of female Mecp2-deficient mice. Hum Mol Genet 17:1386-1396.
39. Kerr AM, Prescott RJ (2005). Predictive value of the early clinical signs in Rett disorder. Brain Dev 27 (Suppl 1):S20-S24.
40. Kerr AM, Montague J, Stephenson JB (1987). The hands, and the mind, pre- and post-regression, in Rett syndrome. Brain Dev 9:487-490.
41. Kerr AM, Armstrong DD, Prescott RJ, Doyle D, Kearney DL (1997). Rett syndrome: analysis of deaths in the British survey. Eur Child Adolesc Psychiatry 6 (Suppl 1):71-74.
42. LaSalle JM (2007). The Odyssey of MeCP2 and parental imprinting. Epigenetics 2:5-10.
43. Lauterborn JC, Lynch G, Vanderklish P, Arai A, Gall CM (2000). Positive modulation of AMPA receptors increases neurotrophin expression by hippocampal and cortical neurons. J Neurosci 20:8-21.
44. Laviola G, Rea M, Morley-Fletcher S, Di Carlo S, Bacosi A, De Simone R, et al. (2004). Beneficial effects of enriched environment on adolescent rats from stressed pregnancies. Eur J Neurosci 20:1655-1664.
45. Lawson A, Picker J, Tsai G, Lange N, Froimowitz M, Cataldo AM, Coyle JT (2007). Rett mice with MeCP2 mutation, R168X, have abnormal mitochondria. In: Conference Book: 799.23, Society for Neuroscience:
46. San Diego. Lawson-Yuen A, Liu D, Han L, Jiang ZI, Tsai GE, Basu AC, et al. (2007). Ube3a mRNA and protein expression are not decreased in Mecp2R168X mutant mice. Brain Res 1180:1-6.
47. Lotan M (2007a). Alternative therapeutic intervention for individuals with Rett syndrome. ScientificWorld J 7:698-714.
48. Lotan M (2007b). Assistive technology and supplementary treatment for individuals with Rett syndrome. ScientificWorld J 7:903-948.
49. Luikenhuis S, Giacometti E, Beard CF, Jaenisch R (2004). Expression of MeCP2 in postmitotic neurons rescues Rett syndrome in mice. Proc Natl Acad Sci U S A 101:6033-6038.
50. Makedonski K, Abuhatzira L, Kaufman Y, Razin A, Shemer R (2005). MeCP2 deficiency in Rett syndrome causes epigenetic aberrations at the PWS/AS imprinting center that affects UBE3A expression. Hum Mol Genet 14:1049-1058.
51. Martinowich K, Hattori D, Wu H, Fouse S, He F, Hu Y, et al. (2003). DNA methylation-related chromatin remodeling in activity-dependent BDNF gene regulation. Science 302:890-893.
52. McGill BE, Bundle SF, Yaylaoglu MB, Carson JP, Thaller C, Zoghbi HY (2006). Enhanced anxiety and stress-induced corticosterone release are associated with increased Crh expression in a mouse model of Rett syndrome. Proc Natl Acad Sci U S A 103:18267-18272.
53. McKinney WT (1984). Animal models of depression: an overview. Psychiatr Dev 2:77-96.
54. Medrihan L, Tantalaki E, Aramuni G, Sargsyan V, Dudanova I, Missler M, et al. (2007). Early defects of GABAergic synapses in the brainstem of a MeCP2 mouse model of Rett syndrome. J Neurophysiol 99:112-21.
55. Moretti P, Bouwknecht JA, Teague R, Paylor R, Zoghbi HY (2005). Abnormalities of social interactions and home-cage behavior in a mouse model of Rett syndrome. Hum Mol Genet 14:205-220.
56. Moretti P, Levenson JM, Battaglia F, Atkinson R, Antalffy B, Amstrong D, et al. (2006). Learning and memory and synaptic plasticity are impaired in a mouse model of Rett syndrome. J Neurosci 26:319-327.
57. Moriuchi J, Nag N, Berger-Sweeney JE (2007). Effects of environmental enrichment on a mouse model of Rett syndrome. In: Conference Book:54.2, Society for Neuroscience: San Diego. Morley-Fletcher S, Rea M, Maccari S, Laviola G (2003). Environmental enrichment during adolescence reverses the effects of prenatal stress on play behaviour and HPA axis reactivity in rats. Eur J Neurosci 18:3367-3374.
58. Mount RH, Hastings RP, Reilly S, Cass H, Charman T (2001). Behavioural and emotional features in Rett syndrome. Disabil Rehabil 23:129-138.
59. Moy SS, Nadler JJ (2008). Advances in behavioral genetics: mouse models of autism. Mol Psychiatry 13:4-26.
60. Nag N, Berger-Sweeney JE (2007). Postnatal dietary choline supplementation alters behavior in a mouse model of Rett syndrome. Neurobiol Dis 26:473-480.
61. Nagarajan N, Quast C, Boxall AR, Shahid M, Rosenmund C (2001). Mechanism and impact of allosteric AMPA receptor modulation by the ampakine CX546. Neuropharmacology 41:650-663.
62. Nan X, Hou J, Maclean A, Nasir J, Lafuente MJ, Shu X, et al. (2007). Interaction between chromatin proteins MECP2 and ATRX is disrupted by mutations that cause inherited mental retardation. Proc Natl Acad Sci U S A 104:2709-2714.
63. Nomura T, Kimura M, Horii T, Morita S, Soejima H, Kudo S, et al. (2008). MeCP2-dependent repression of an imprinted miR-184 released by depolarization. Hum Mol Genet 17:1192-1199.
64. Nuber UA, Kriaucionis S, Roloff TC, Guy J, Selfridge J, Steinhoff C, et al. (2005). Up-regulation of glucocorticoid-regulated genes in a mouse model of Rett syndrome. Hum Mol Genet 14:2247-2256.
65. Ogier M, Wang H, Hong E, Wang Q, Greenberg ME, Katz DM (2007). Brain-derived neurotrophic factor expression and respiratory function improve after ampakine treatment in a mouse model of Rett syndrome. J Neurosci 27:10912-10917.
66. Peddada S, Yasui DH, LaSalle JM (2006). Inhibitors of differentiation (ID1, ID2, ID3 and ID4) genes are neuronal targets of MeCP2 that are elevated in Rett syndrome. Hum Mol Genet 15:2003-2014.
67. Pelka GJ, Watson CM, Radziewic T, Hayward M, Lahooti H, Christodoulou J, et al. (2006). Mecp2 deficiency is associated with learning and cognitive deficits and altered gene activity in the hippocampal region of mice. Brain 129:887-898.
68. Picker JD, Yang R, Ricceri L, Berger-Sweeney J (2006). An altered neonatal behavioral phenotype in Mecp2 mutant mice. NeuroReport 17:541-544.
69. Pietropaolo S, Branchi I, Cirulli F, Chiarotti F, Aloe L, Alleva E (2004). Long-term effects of the periadolescent environment on exploratory activity and aggressive behaviour in mice: social versus physical enrichment. Physiol Behav 81:443-453.
70. Pizzorusso T, Lonetti G, Boggio E, Morando L, Putignano E, Pallotto M, et al. (2007). Environmental enrichment produces behavioural improvement prolonged life span and structural sinaptic plasticity in a mouse model of Rett's syndrome. In: Conference Book:172.2, Society for Neuroscience: San Diego. Portwood MM (2006). The role of dietary fatty acids in children's behaviour and learning. Nutr Health 18:233-247.
71. Rampon C, Jiang CH, Dong H, Tang YP, Lockhart DJ, Schultz PG, et al. (2000). Effects of environmental enrichment on gene expression in the brain. Proc Natl Acad Sci U S A 97:12880-12884.
72. Rex CS, Lauterborn JC, Lin CY, Kramar EA, Rogers GA, Gall CM, et al. (2006). Restoration of long-term potentiation in middle-aged hippocampus after induction of brain-derived neurotrophic factor. J Neurophysiol 96:677-685.
73. Ricceri L, De Filippis B, Laviola G. (2007). Behavioural phenotyping and assessment of non-pharmacological interventions in a transgenic mouse model of Rett syndrome. In: Conference Book, Eastern European Conference on Rare Disease: Plovdiv (Bulgaria) Roux JC, Dura E, Moncla A, Mancini J, Villard L (2007a). Treatment with desipramine improves breathing and survival in a mouse model for Rett syndrome. Eur J Neurosci 25:1915-1922.
74. Roux JC, Dura E, Moncla A, Mancini J, Shvarev L, Villard L. (2007b). Bioaminergic deficits in Rett syndrome: from pathophysiology to clinical trials. In: Conference Book:172.8, Society for Neuroscience: San Diego. Sale A, Cenni MC, Ciucci F, Putignano E, Chierzi S, Maffei L (2007). Maternal enrichment during pregnancy accelerates retinal development of the fetus. PLoS ONE 2:e1160.
75. Samaco RC, Hogart A, LaSalle JM (2005). Epigenetic overlap in autism-spectrum neurodevelopmental disorders: MECP2 deficiency causes reduced expression of UBE3A and GABRB3. Hum Mol Genet 14:483-492.
76. Santos M, Silva-Fernandes A, Oliveira P, Sousa N, Maciel P (2007). Evidence for abnormal early development in a mouse model of Rett syndrome. Genes Brain Behav 6:277-286.
77. Saywell V, Viola A, Confort-Gouny S, Le Fur Y, Villard L, Cozzone PJ (2006). Brain magnetic resonance study of Mecp2 deletion effects on anatomy and metabolism. Biochem Biophys Res Commun 340:776-783.
78. Scala E, Ariani F, Mari F, Caselli R, Pescucci C, Longo I, et al. (2005). CDKL5/STK9 is mutated in Rett syndrome variant with infantile spasms. J Med Genet 42:103-107.
79. Scala I, Granese B, Sellitto M, Salome S, Sammartino A, Pepe A, et al. (2006). Analysis of seven maternal polymorphisms of genes involved in homocysteine/ folate metabolism and risk of Down syndrome offspring. Genet Med 8:409-416.
80. Scattoni ML, Crawley J, Ricceri L (2008). Ultrasonic vocalizations: a tool for behavioural phenotyping of mutant mice. Neurosci Biobehav Rev (in press). Schanen NC (2006). Epigenetics of autism spectrum disorders. Hum Mol Genet 15:R138-R150.
81. Schule B, Li HH, Fisch-Kohl C, Purmann C, Francke U (2007). DLX5 and DLX6 expression is biallelic and not modulated by MeCP2 deficiency. Am J Hum Genet 81:492-506.
82. Shahbazian M, Young J, Yuva-Paylor L, Spencer C, Antalffy B, Noebels J, et al. (2002). Mice with truncated MeCP2 recapitulate many Rett syndrome features and display hyperacetylation of histone H3. Neuron 35:243-254.
83. Spear LP (1990). Neurobehavioral assessment during the early postnatal period. Neurotoxicol Teratol 12:489-495.
84. Stearns NA, Schaevitz LR, Bowling H, Nag N, Berger UV, Berger-Sweeney J (2007). Behavioral and anatomical abnormalities in Mecp2 mutant mice: a model for Rett syndrome. Neuroscience 146:907-921.
85. Stettner GM, Huppke P, Brendel C, Richter DW, Gartner J, Dutschmann M (2007). Breathing dysfunctions associated with impaired control of postinspiratory activity in Mecp2-/y knockout mice. J Physiol 579:863-876.
86. Tams-Little S, Holdgrafer G (1996). Early communication development in children with Rett syndrome. Brain Dev 18:376-378.
87. Tecott LH (2003). The genes and brains of mice and men. Am J Psychiatry 160:646-656.
88. Viemari JC, Roux JC, Tryba AK, Saywell V, Burnet H, Pena F, et al. (2005). Mecp2 deficiency disrupts norepinephrine and respiratory systems in mice. J Neurosci 25:11521-11530.
89. Ward BC, Huang L, Peitzman C, Berger-Sweeney JE, Kolodny N (2007). MRI analysis of the effects of environmental enrichment on brain development in a mouse model of Rett syndrome. In: Conference Book:54.1, Society for Neuroscience: San Diego. Young JI, Zoghbi HY (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.
90. Zanella S, Mebarek S, Lajard AM, Picard N, Dutschmann M, Hilaire G (2008). Oral treatment with desipramine improves breathing and life span in Rett syndrome mouse model. Respir Physiol Neurobiol 160:116-121.
91. Zeisel SH (2006). The fetal origins of memory: the role of dietary choline in optimal brain development. J Pediatr 149:S131-S136.
92. Zhu SW, Pham TM, Aberg E, Brene S, Winblad B, Mohammed AH, et al. (2006). Neurotrophin levels and behaviour in BALB/c mice: impact of intermittent exposure to individual housing and wheel running. Behav Brain Res 167:1-8.