Applying the ethoexperimental approach to neurodevelopmental syndrome research reveals exaggerated defensive behavior in Mecp2 mutant mice

Physiology and Behavior

Volumn 146, Issue , 2015, Pages 98-104

  Pearson, Brandon L ^a,b   Defensor, Erwin B ^a,c   Caroline Blanchard, D ^a   Blanchard, Robert J ^a  

^a UNIVERSITY OF HAWAII   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Autism; Defense; Ethoexperimental approach; Fear; MECP2; Rett syndrome

Indexed keywords

METHYL CPG BINDING PROTEIN 2; MECP2 PROTEIN, HUMAN;

AGGRESSION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY DISORDER; ARTICLE; BODY POSTURE; CONTROLLED STUDY; DEFENSIVE BEHAVIOR; ELEVATED ZERO MAZE TEST; EMOTIONALITY; ESCAPE BEHAVIOR; FEAR; FEMALE; GENOTYPE; LOCOMOTION; MOUSE; MOUSE DEFENSE TEST BATTERY; MUTANT; NONHUMAN; PANIC; PRIORITY JOURNAL; RAT; RETT SYNDROME; RISK ASSESSMENT; THREAT; ANALYSIS OF VARIANCE; ANIMAL; ANXIETY; C57BL MOUSE; COMPLICATION; DISEASE MODEL; ETIOLOGY; GENETICS; MALE; MAZE TEST; MUTATION; PHYSIOLOGY; TRANSGENIC MOUSE;

AGGRESSION; ANALYSIS OF VARIANCE; ANIMALS; ANXIETY; DISEASE MODELS, ANIMAL; ESCAPE REACTION; LOCOMOTION; MALE; MAZE LEARNING; METHYL-CPG-BINDING PROTEIN 2; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MUTATION; RETT SYNDROME;

EID: 84937967382     PISSN: 00319384     EISSN: 1873507X     Source Type: Journal    
DOI: 10.1016/j.physbeh.2015.03.035     Document Type: Article

References (71)

1. Crawley J.N. Translational animal models of autism and neurodevelopmental disorders. Dialogues Clin. Neurosci. 2012, 14:293-305.
2. Blanchard D.C., Blanchard R.J. Ethoexperimental approaches to the biology of emotion. Annu. Rev. Psychol. 1988, 39:43-68.
3. Pobbe R.L., Pearson B.L., Defensor E.B., Bolivar V.J., Blanchard D.C., Blanchard R.J. Expression of social behaviors of C57BL/6J versus BTBR inbred mouse strains in the visible burrow system. Behav. Brain Res. 2010, 214:443-449.
4. Pobbe R.L., Defensor E.B., Pearson B.L., Bolivar V.J., Blanchard D.C., Blanchard R.J. General and social anxiety in the BTBR T+ tf/J mouse strain. Behav. Brain Res. 2011, 216:446-451.
5. Pearson B.L., Pobbe R.L.H., Defensor E.B., Oasey L., Bolivar V.J., Blanchard D.C., Blanchard R.J. Motor and cognitive stereotypies in the BTBR T+ tf/J mouse model of autism. Genes Brain Behav. 2011, 10:228-235.
6. Defensor E.B., Pearson B.L., Pobbe R.L.H., Bolivar V.J., Blanchard D.C., Blanchard R.J. A novel social proximity test suggests patterns of social avoidance and gaze aversion-like behavior in BTBR T+ tf/J mice. Behav. Brain Res. 2011, 217:302-308.
7. Pobbe R.L.H., Pearson B.L., Defensor E.B., Bolivar V.J., Young W.S., Blanchard D.C., Blanchard R.J. Oxytocin receptor knockout mice display deficits in the expression of autism-related behaviors. Horm. Behav. 2012, 61:436-444.
8. Pearson B.L., Defensor E.B., Pobbe R.L.H., Yamamoto L.H.L., Bolivar V.J., Blanchard D.C., Blanchard R.J. MeCP2 truncation in male mice promotes affiliative social behavior. Behav. Genet. 2012, 42:299-312.
9. Chahrour M., Jung S.Y., Shaw C., Zhou X., Wong S.T., Qin J., Zoghbi H.Y. MeCP2, a key contributor to neurological disease, activates and represses transcription. Science 2008, 320:1224-1229.
10. Jørgensen H.F., Bird A. MeCP2 and other methyl-CpG binding proteins. Ment. Retard. Dev. Disabil. Res. Rev. 2002, 8:87-93.
11. Lewis J.D., Meehan R.R., Henzel W.J., Maurer-Fogy I., Jeppesen P., Klein F., Bird A. Purification, sequence, and cellular localization of a novel chromosomal protein that binds to methylated DNA. Cell 1992, 69:905-914.
12. Samaco R.C., Mandel-Brehm C., Chao H.T., Ward C.S., Fyffe-Maricich S.L., Ren J., Hyland K., Thaller C., Maricich S.M., Humphreys P., Greer J.J., Percy A., Glaze D.G., Zoghbi H.Y., Neul J.L. Loss of MeCP2 in aminergic neurons causes cell-autonomous defects in neurotransmitter synthesis and specific behavioral abnormalities. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:21966-21971.
13. Wu H., Tao J., Chen P.J., Shahab A., Ge W., Hart R.P., Ruan X., Ruan Y., Sun Y.E. Genome-wide analysis reveals methyl-CpG-binding protein 2-dependent regulation of microRNAs in a mouse model of Rett syndrome. Proc Natl Acad Sci USA 2010, 107:18161-18166.
14. Young J.I., Hong E.P., Castle J.C., Crespo-Barreto J., Bowman A.B., Rose M.F., Kang D., Richman R., Johnson J.M., Berget S., Zoghbi H.Y. Regulation of RNA splicing by the methylation-dependent transcriptional repressor methyl-CpG binding protein 2. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:17551-17558.
15. Nan X., Ng H.H., Johnson C.A., Laherty C.D., Turner B.M., Eisenman R.N., Bird A. Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 1998, 393:386-389.
16. Amir R.E., Van den Veyver I.B., Wan M., Tran C.Q., Francke U., Zoghbi H.Y. Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2. Nat. Genet. 1999, 23:185-188.
17. Bienvenu T., Carrié A., de Roux N., Vinet M.C., Jonveaux P., Couvert P., Villard L., Arzimanoglou A., Beldjord C., Fontes M., Tardieu M., Chelly J. MECP2 mutations account for most cases of typical forms of Rett syndrome. Hum. Mol. Genet. 2000, 9:1377-1384.
18. Beyer K.S., Blasi F., Bacchelli E., Klauck S.M., Maestrini E., Poustka A. Mutation analysis of the coding sequence of the MECP2 gene in infantile autism. Hum. Genet. 2002, 111:305-309.
19. Carney R.M., Wolpert C.M., Ravan S.A., Shahbazian M., Ashley-Koch A., Cuccaro M.L., Vance J.M., Pericak-Vance M.A. Identification of MeCP2 mutations in a series of females with autistic disorder. Pediatr. Neurol. 2003, 28:205-211.
20. Nagarajan R.P., Hogart A.R., Gwye Y., Martin M.R., LaSalle J.M. Reduced MeCP2 expression is frequent in autism frontal cortex and correlates with aberrant MECP2 promoter methylation. Epigenetics 2006, 1:e1-e11.
21. Samaco R.C., Nagarajan R.P., Braunschweig D., LaSalle J.M. Multiple pathways regulate MeCP2 expression in normal brain development and exhibit defects in autism-spectrum disorders. Hum. Mol. Genet. 2004, 13:629-639.
22. Hammer S., Dorrani N., Dragich J., Kudo S., Schanen C. The phenotypic consequences of MECP2 mutations extend beyond Rett syndrome. Ment. Retard. Dev. Disabil. Res. Rev. 2002, 8:94-98.
23. Van Esch H., Bauters M., Ignatius J., Jansen M., Raynaud M., Hollanders K., Lugtenberg D., Bienvenu T., Jensen L.R., Gecz J., Moraine C., Marynen P., Fryns J.P., Froyen G. Duplication of the MECP2 region is a frequent cause of severe mental retardation and progressive neurological symptoms in males. Am. J. Hum. Genet. 2005, 77:442-453.
24. Hagberg B. Clinical manifestations and stages of Rett syndrome. Ment. Retard. Dev. Disabil. Res. Rev. 2002, 8:61-65.
25. Chen R.Z., Akbarian S., Tudor M., Jaenisch R. Deficiency of methyl-CpG binding protein-2 in CNS neurons results in a Rett-like phenotype in mice. Nat. Genet. 2001, 27:327-331.
26. Guy J., Hendrich B., Holmes M., Martin J.E., Bird A. A mouse Mecp2-null mutation causes neurological symptoms that mimic Rett syndrome. Nat. Genet. 2001, 27:322-326.
27. Cassel S., Carouge D., Gensburger C., Anglard P., Burgun C., Dietrich J., Aunis D., Zwiller J. Fluoxetine and cocaine induce the epigenetic factors MeCP2 and MBD1 in adult rat brain. Mol. Pharmacol. 2006, 70:487-492.
28. De Filippis B., Ricceri L., Laviola G. Early postnatal behavioral changes in the Mecp2-308 truncation mouse model of Rett syndrome. Genes Brain Behav. 2010, 9:213-223.
29. Deng J.V., Rodriguiz R.M., Hutchinson A.N., Kim I.H., Wetsel W.C., West A.E. MeCP2 in the nucleus accumbens contributes to neural and behavioral responses to psychostimulants. Nat. Neurosci. 2010, 13:1128-1136.
30. Gemelli T., Berton O., Nelson E.D., Perrotti L.I., Jaenisch R., Monteggia L.M. Postnatal loss of methyl-CpG binding protein 2 in the forebrain is sufficient to mediate behavioral aspects of Rett syndrome in mice. Biol. Psychiatry 2006, 59:468-476.
31. Im H.I., Hollander J.A., Bali P., Kenny P.J. MeCP2 controls BDNF expression and cocaine intake through homeostatic interactions with microRNA-212. Nat. Neurosci. 2010, 13:1120-1127.
32. McGill B.E., Bundle S.F., Yaylaoglu M.B., Carson J.P., Thaller C., Zoghbi H.Y. 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. 2006, 103:18267-18272.
33. Moretti P., Bouwknecht J.A., Teague R., Paylor R., Zoghbi H.Y. Abnormalities of social interactions and home-cage behavior in a mouse model of Rett syndrome. Hum. Mol. Genet. 2005, 14:205-220.
34. Moretti P., Levenson J.M., Battaglia F., Atkinson R., Teague R., Antalffy B., Amstrong D., Arancio O., Sweatt J.D., Zoghbi H.Y. Learning and memory and synaptic plasticity are impaired in a mouse model of Rett syndrome. J. Neurosci. 2006, 26:319-327.
35. Pelka G.J., Watson C.M., Radziewic T., Hayward M., Lahooti H., Christodoulou J., Tam P.P. Mecp2 deficiency is associated with learning and cognitive deficits and altered gene activity in the hippocampal region of mice. Brain 2006, 129:887-898.
36. Shahbazian M., Young J., Yuva-Paylor L., Spencer C., Antalffy B., Noebels J., Armstrong D., Paylor R., Zoghbi H. Mice with truncated MeCP2 recapitulate many Rett syndrome features and display hyperacetylation of histone H3. Neuron 2002, 35:243-254.
37. Stearns N.A., Schaevitz L.R., Bowling H., Nag N., Berger U.V., Berger-Sweeney J. Behavioral and anatomical abnormalities in Mecp2 mutant mice: a model for Rett syndrome. Neuroscience 2007, 146:907-921.
38. Su D., Cha Y.M., West A.E. Mutation of MeCP2 alters transcriptional regulation of select immediate-early genes. Epigenetics 2012, 7:146-154.
39. McGraw C.M., Samaco R.C., Zoghbi H.Y. Adult neural function requires MeCP2. Science 2011, 333:186.
40. Nguyen M.V., Du F., Felice C.A., Shan X., Nigam A., Mandel G., Robinson J.K., Ballas N. MeCP2 is critical for maintaining mature neuronal networks and global brain anatomy during late stages of postnatal brain development and in the mature adult brain. J. Neurosci. 2012, 32:10021-10034.
41. Kaufmann W.E., Johnston M.V., Blue M.E. MeCP2 expression and function during brain development: implications for Rett syndrome's pathogenesis and clinical evolution. Brain Dev. 2005, 27:S77-S87.
42. Asaka Y., Jugloff D.G., Zhang L., Eubanks J.H., Fitzsimonds R.M. Hippocampal synaptic plasticity is impaired in the Mecp2-null mouse model of Rett syndrome. Neurobiol. Dis. 2006, 21:217-227.
43. Gantz S.C., Ford C.P., Neve K.A., Williams J.T. Loss of Mecp2 in substantia nigra dopamine neurons compromises the nigrostriatal pathway. J. Neurosci. 2011, 31:12629-12637.
44. Kishi N., Macklis J.D. MeCP2 functions largely cell-autonomously, but also non-cell-autonomously, in neuronal maturation and dendritic arborization of cortical pyramidal neurons. Exp. Neurol. 2010, 222:51-58.
45. Roux J.C., Zala D., Panayotis N., Borges-Correia A., Saudou F., Villard L. Modification of the Mecp2 dosage alters axonal transport through the Huntingtin/Hap1 pathway. Neurobiol. Dis. 2012, 45:786-795.
46. Stuss D.P., Boyd J.D., Levin D.B., Delaney K.R. MeCP2 mutation results in compartment-specific reductions in dendritic branching and spine density in layer 5 motor cortical neurons of YFP-H mice. PLoS One 2012, 7:e31896.
47. Bauman M.L., Kemper T.L., Arin D.M. Microscopic observations of the brain in Rett syndrome. Neuropediatrics 1995, 26:105-108.
48. Belichenko P.V., Wright E.E., Belichenko N.P., Masliah E., Li H.H., Mobley W.C., Francke U. Widespread changes in dendritic and axonal morphology in Mecp2-mutant mouse models of Rett syndrome: evidence for disruption of neuronal networks. J. Comp. Neurol. 2009, 514:240-258.
49. Chapleau C.A., Calfa G.D., Lane M.C., Albertson A.J., Larimore J.L., Kudo S., Armstrong D.L., Percy A.K., Pozzo-Miller L. Dendritic spine pathologies in hippocampal pyramidal neurons from Rett syndrome brain and after expression of Rett-associated MECP2 mutations. Neurobiol. Dis. 2009, 35:219-233.
50. Dani V.S., Chang Q., Maffei A., Turrigiano G.G., Jaenisch R., Nelson S.B. 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. 2005, 102:12560-12565.
51. Farra N., Zhang W.B., Pasceri P., Eubanks J.H., Salter M.W., Ellis J. Rett syndrome induced pluripotent stem cell-derived neurons reveal novel neurophysiological alterations. Mol. Psychiatry 2012, 17:1261-1271.
52. Fukuda T., Itoh M., Ichikawa T., Washiyama K., Goto Y. Delayed maturation of neuronal architecture and synaptogenesis in cerebral cortex of Mecp2-deficient mice. J. Neuropathol. Exp. Neurol. 2005, 64:537-544.
53. Mount R.H., Charman T., Hastings R.P., Reilly S., Cass H. The Rett Syndrome Behavior Questionnaire (RSBQ): refining the behavioural phenotype of Rett syndrome. J. Child Psychol. Psychiatry 2002, 43:1099-1110.
54. Sansom D., Krishnan V.H., Corbett J., Kerr A. Emotional and behavioural aspects of Rett syndrome. Dev. Med. Child Neurol. 1993, 35:340-345.
55. Christodoulou J., Ho G. MECP2-related Disorders. Source: GeneReviews® [Internet] 2001, University of Washington, Seattle, Seattle (WA). R.A. Pagon, M.P. Adam, H.H. Ardinger, T.D. Bird, C.R. Dolan, C.T. Fong, R.J.H. Smith, K. Stephens (Eds.).
56. Olsson B., Rett A. Behavioral observations concerning differential diagnosis between the Rett syndrome and autism. Brain Dev. 1985, 7:281-289.
57. Ozonoff S., Goodlin-Jones B.L., Solomon M. Evidence-based assessment of autism spectrum disorders in children and adolescents. J. Clin. Child Adolesc. Psychol. 2005, 34:523-540.
58. Quest K.M., Byiers B.J., Payen A., Symons F.J. Rett syndrome: a preliminary analysis of stereotypy, stress, and negative affect. Res. Dev. Disabil. 2014, 35:1191-1197.
59. Lister R.G. The use of a plus-maze to measure anxiety in the mouse. Psychopharmacology (Berl) 1987, 92:180-185.
60. Blanchard D.C., Griebel G., Blanchard R.J. The mouse defense test battery: pharmacological and behavioral assays for anxiety and panic. Eur. J. Pharmacol. 2003, 463:97-116.
61. Blanchard D.C., Griebel G., Blanchard R.J. Mouse defensive behaviors: pharmacological and behavioral assays for anxiety and panic. Neurosci. Biobehav. Rev. 2001, 25:205-218.
62. Ricceri L., De Filippis B., Laviola G. Mouse models of Rett syndrome: from behavioural phenotyping to preclinical evaluation of new therapeutic approaches. Behav. Pharmacol. 2008, 19:501-517.
63. Tantra M., Hammer C., Kästner A., Dahm L., Begemann M., Bodda C., Hammerschmidt K., Giegling I., Stepniak B., Castillo Venzor A., Konte B., Erbaba B., Hartmann A., Tarami A., Schulz-Schaeffer W., Rujescu D., Mannan A.U., Ehrenreich H. Mild expression differences of MECP2 influencing aggressive social behavior. EMBO Mol. Med. 2014, 6:662-684.
64. Blanchard R.J., Griebel G., Henrie J.A., Blanchard D.C. Differentiation of anxiolytic and panicolytic drugs by effects on rat and mouse defense test batteries. Neurosci. Biobehav. Rev. 1997, 21:783-789.
65. Rosen J.B. The neurobiology of conditioned and unconditioned fear: a neurobehavioral system analysis of the amygdala. Behav. Cogn. Neurosci. Rev. 2004, 3:23-41.
66. Adachi M., Autry A.E., Covington H.E., Monteggia L.M. MeCP2-mediated transcription repression in the basolateral amygdala may underlie heightened anxiety in a mouse model of Rett syndrome. J. Neurosci. 2009, 29:4218-4227.
67. Samaco R.C., Mandel-Brehm C., McGraw C.M., Shaw C.A., McGill B.E., Zoghbi H.Y. Crh and Oprm1 mediate anxiety-related behavior and social approach in a mouse model of MECP2 duplication syndrome. Nat. Genet. 2012, 44:206-211.
68. Wither R.G., Lang M., Zhang L., Eubanks J.H. Regional MeCP2 expression levels in the female MeCP2-deficient mouse brain correlate with specific behavioral impairments. Exp. Neurol. 2013, 239:49-59.
69. Ren J., Ding X., Funk G.D., Greer J.J. Anxiety-related mechanisms of respiratory dysfunction in a mouse model of Rett syndrome. J. Neurosci. 2012, 32:17230-17240.
70. Olsson B., Rett A. Autism and Rett syndrome: behavioural investigations and differential diagnosis. Dev. Med. Child Neurol. 1987, 29:429-441.
71. Muris P., Steerneman P., Merckelbach H., Holdrinet I., Meesters C. Comorbid anxiety symptoms in children with pervasive developmental disorders. J. Anxiety Disord. 1998, 12:387-393.