Fragile X mice have robust mGluR5-dependent alterations of social behaviour in the Automated Tube Test

Neurobiology of Disease

Volumn 75, Issue , 2015, Pages 31-39

  de Esch, C E F ^a   van den Berg, W E ^a   Buijsen, R A M ^a   Jaafar, I A ^a   Nieuwenhuizen Bakker, I M ^a   Gasparini, F ^b   Kushner, S A ^a   Willemsen, R ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b NOVARTIS PHARMA AG   (Switzerland)

Author keywords

ERK; Fragile X; Glutamate receptor; Social behaviour; Tube

Indexed keywords

GLUTAMATE RECEPTOR 5; MAVOGLURANT; MITOGEN ACTIVATED PROTEIN KINASE 1; PLACEBO; AMINO ACID RECEPTOR BLOCKING AGENT; FMR1 PROTEIN, MOUSE; FRAGILE X MENTAL RETARDATION PROTEIN; GRM5 PROTEIN, MOUSE; INDOLE DERIVATIVE; METABOTROPIC RECEPTOR 5; PSYCHOTROPIC AGENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOMATED TUBE TEST; CONTROLLED STUDY; DISEASE MARKER; ENZYME PHOSPHORYLATION; FEMALE; FRAGILE X SYNDROME; FUNCTION TEST; GENE DELETION; KNOCKOUT MOUSE; MALE; MGLUR5 GENE; MOUSE; NONHUMAN; PATHOPHYSIOLOGY; PHENOTYPE; RECEPTOR BLOCKING; SOCIAL BEHAVIOR; SOCIAL DISABILITY; TREATMENT OUTCOME; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; DEFICIENCY; DISEASE MODEL; DRUG EFFECTS; GENETICS; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; PSYCHOLOGIC TEST; PSYCHOLOGY; SIGNAL TRANSDUCTION; SYNAPSE;

ANIMALS; DISEASE MODELS, ANIMAL; EXCITATORY AMINO ACID ANTAGONISTS; FRAGILE X MENTAL RETARDATION PROTEIN; FRAGILE X SYNDROME; INDOLES; MALE; MAP KINASE SIGNALING SYSTEM; MICE, INBRED C57BL; MICE, KNOCKOUT; PHENOTYPE; PHOSPHORYLATION; PSYCHOLOGICAL TESTS; PSYCHOTROPIC DRUGS; RECEPTOR, METABOTROPIC GLUTAMATE 5; SOCIAL BEHAVIOR; SYNAPSES;

EID: 84921326733     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2014.12.021     Document Type: Article

References (62)

1. Bagni C., Klann E. Molecular functions of the mammalian fragile X mental retardation protein: insights into mental retardation and synaptic plasticity. The Autisms 2012, 126-139. C.M. Powell, L.M. Monteggia (Eds.).
2. Bailey D.B., Hatton D.D., Skinner M., Mesibov G. Autistic behavior, FMR1 protein, and developmental trajectories in young males with fragile X syndrome. J. Autism Dev. Disord. 2001, 31(2):165-174.
3. Bakker C.E., Oostra B.A. Understanding fragile X syndrome: insights from animal models. Cytogenet. Genome Res. 2003, 100(1-4):111-123.
4. Bartolomucci A., Palanza P., Gaspani L., Limiroli E., Panerai A.E., Ceresini G., et al. Social status in mice: behavioral, endocrine and immune changes are context dependent. Physiol. Behav. 2001, 73(3):401-410.
5. Bear M.F., Huber K.M., Warren S.T. The mGluR theory of fragile X mental retardation. Trends Neurosci. 2004, 27(7):370-377.
6. Bernardet M., Crusio W.E. Fmr1 KO mice as a possible model of autistic features. ScientificWorldJournal 2006, 6:1164-1176.
7. Berry-Kravis E., Potanos K. Psychopharmacology in fragile X syndrome-present and future. Ment. Retard. Dev. Disabil. Res. Rev. 2004, 10(1):42-48.
8. Berry-Kravis E., Sumis A., Hervey C., Mathur S. Clinic-based retrospective analysis of psychopharmacology for behavior in fragile X syndrome. Int. J. Pediatr. 2012, 843016.
9. Bhattacharya A., Kaphzan H., Alvarez-Dieppa A.C., Murphy J.P., Pierre P., Klann E. Genetic removal of p70 S6 kinase 1 corrects molecular, synaptic, and behavioral phenotypes in fragile X syndrome mice. Neuron 2012, 76(2):325-337.
10. Brock M., Hatton D. Distinguishing features of autism in boys with fragile X syndrome. J. Intellect. Disabil. Res. 2010, 54:894-905.
11. Darnell J.C., Klann E. The translation of translational control by FMRP: therapeutic targets for FXS. Nat. Neurosci. 2013, 16(11):1530-1536.
12. Dobkin C., Rabe A., Dumas R., El Idrissi A., Haubenstock H., Ted Brown W. Fmr1 knockout mouse has a distinctive strain-specific learning impairment. Neuroscience 2000, 100:423-429.
13. Dolen G., Osterweil E., Rao B.S., Smith G.B., Auerbach B.D., Chattarji S., et al. Correction of fragile X syndrome in mice. Neuron 2007, 56(6):955-962.
14. Dyer-Friedman J., Glaser B., Hessl D., Johnston C., Huffman L.C., Taylor A., et al. Genetic and environmental influences on the cognitive outcomes of children with fragile X syndrome. J. Am. Acad. Child Adolesc. Psychiatry 2002, 41(3):237-244.
15. Errijgers V., Kooy R.F. Genetic modifiers in mice: the example of the fragile X mouse model. Cytogenet. Genome Res. 2004, 105(2-4):448-454.
16. Gantois I., Pop A.S., de Esch C.E., Buijsen R.A., Pooters T., Gomez-Mancilla B., et al. Chronic administration of AFQ056/mavoglurant restores social behaviour in Fmr1 knockout mice. Behav. Brain Res. 2013, 239:72-79.
17. Garber K.B., Visootsak J., Warren S.T. Fragile X syndrome. Eur. J. Hum. Genet. 2008, 16:666-672.
18. Glaser B., Hessl D., Dyer-Friedman J., Johnston C., Wisbeck J., Taylor A., et al. Biological and environmental contributions to adaptive behavior in fragile X syndrome. Am. J. Med. Genet. 2003, 117A(1):21-29.
19. Goebel-Goody S.M., Wilson-Wallis E.D., Royston S., Tagliatela S.M., Naegele J.R., Lombroso P.J. Genetic manipulation of STEP reverses behavioral abnormalities in a fragile X syndrome mouse model. Genes Brain Behav. 2012, 11:586-600.
20. Greenberg G.D., Howerton C.L., Trainor B.C. Fighting in the home cage: agonistic encounters and effects on neurobiological markers within the social decision-making network of house mice (Mus musculus). Neurosci. Lett. 2014, 566:151-155.
21. Greenough W.T., Klintsova A.Y., Irwin S.A., Galvez R., Bates K.E., Weiler I.J. Synaptic regulation of protein synthesis and the fragile X protein. Proc. Natl. Acad. Sci. U. S. A. 2001, 98(13):7101-7106.
22. Gross C., Nakamoto M., Yao X., Chan C.B., Yim S.Y., Ye K., et al. Excess phosphoinositide 3-kinase subunit synthesis and activity as a novel therapeutic target in fragile X syndrome. J. Neurosci. 2010, 30(32):10624-10638.
23. Gross C., Berry-Kravis E.M., Bassell G.J. Therapeutic strategies in fragile X syndrome: dysregulated mGluR signaling and beyond. Neuropsychopharmacology 2012, 37(1):178-195.
24. Hagerman R.J. The physical and behavioural phenotype. Fragile-X syndrome: diagnosis, treatment and research 2002, 3-109. The Johns Hopkins University Press, Baltimore. R.J. Hagerman, P. Hagerman (Eds.).
25. Hatton D.D., Sideris J., Skinner M., Mankowski J., Bailey D.B., Roberts J., et al. Autistic behavior in children with fragile X syndrome: prevalence, stability, and the impact of FMRP. Am. J. Med. Genet. A 2006, 140A:1804-1813.
26. Hessl D., Dyer-Friedman J., Glaser B., Wisbeck J., Barajas R.G., Taylor A., et al. The influence of environmental and genetic factors on behavior problems and autistic symptoms in boys and girls with fragile x syndrome. Pediatrics 2001, 108(5):E88.
27. Hou L., Antion M.D., Hu D., Spencer C.M., Paylor R., Klann E. Dynamic translational and proteasomal regulation of fragile X mental retardation protein controls mGluR-dependent long-term depression. Neuron 2006, 51(4):441-454.
28. Hu H., Qin Y., Bochorishvili G., Zhu Y., van Aelst L., Zhu J.J. Ras signaling mechanisms underlying impaired GluR1-dependent plasticity associated with fragile X syndrome. J. Neurosci. 2008, 28(31):7847-7862.
29. Iio W., Matsukawa N., Tsukahara T., Kohari D., Toyoda A. Effects of chronic social defeat stress on MAP kinase cascade. Neurosci. Lett. 2011, 504(3):281-284.
30. Kooy R.F., Dhooge R., Reyniers E., Bakker C.E., Nagels G., Deboulle K., et al. Transgenic mouse model for the fragile X syndrome. Am. J. Med. Genet. 1996, 64(2):241-245.
31. Lachiewicz A.M., Spiridigliozzi G.A., Gullion C.M., Ransford S.N., Rao K. Aberrant behaviors of young boys with fragile X syndrome. Am. J. Ment. Retard. 1994, 98(5):567-579.
32. Larson J., Kim D., Patel R.C., Floreani C. Olfactory discrimination learning in mice lacking the fragile X mental retardation protein. Neurobiol. Learn. Mem. 2008, 90(1):90-102.
33. Lindzey G., Winston H., Manosevitz M. Social dominance in inbred mouse strains. Nature 1961, 191:474-476.
34. Liu Z.H., Chuang D.M., Smith C.B. Lithium ameliorates phenotypic deficits in a mouse model of fragile X syndrome. Int. J. Neuropsychopharmacol. 2010, 1-13.
35. Mientjes E.J., Nieuwenhuizen I., Kirkpatrick L., Zu T., Hoogeveen-Westerveld M., Severijnen L., et al. The generation of a conditional Fmr1 knock out mouse model to study Fmrp function in vivo. Neurobiol. Dis. 2006, 21:549-555.
36. Mines M.A., Yuskaitis C.J., King M.K., Beurel E., Jope R.S. GSK3 influences social preference and anxiety-related behaviors during social interaction in a mouse model of fragile X syndrome and autism. PLoS ONE 2010, 5(3):e9706.
37. O'Connell L.A., Hofmann H.A. Evolution of a vertebrate social decision-making network. Science 2012, 336(6085):1154-1157.
38. Oostra B.A., Willemsen R. A fragile balance: FMR1 expression levels. Hum. Mol. Genet. 2003, 12(Suppl. 2):R249-R257.
39. Osterweil E.K., Krueger D.D., Reinhold K., Bear M.F. Hypersensitivity to mGluR5 and ERK1/2 leads to excessive protein synthesis in the hippocampus of a mouse model of fragile X syndrome. J. Neurosci. 2010, 30(46):15616-15627.
40. Palanza P., Gioiosa L., Parmigiani S. Social stress in mice: gender differences and effects of estrous cycle and social dominance. Physiol. Behav. 2001, 73(3):411-420.
41. Pietropaolo S., Guilleminot A., Martin B., D'Amato F.R., Crusio W.E. Genetic-background modulation of core and variable autistic-like symptoms in FMR1 knock-out mice. PLoS ONE 2011, 6(2):e17073.
42. Price T.J., Rashid M.H., Millecamps M., Sanoja R., Entrena J.M., Cervero F. Decreased nociceptive sensitization in mice lacking the fragile X mental retardation protein: role of mGluR1/5 and mTOR. J. Neurosci. 2007, 27(51):13958-13967.
43. Rodriguiz R.M., Chu R., Caron M.G., Wetsel W.C. Aberrant responses in social interaction of dopamine transporter knockout mice. Behav. Brain Res. 2004, 148(1-2):185-198.
44. Rogers S.J., Wehner E.A., Hagerman R. The behavioral phenotype in fragile X: symptoms of autism in very young children with fragile X syndrome, idiopathic autism, and other developmental disorders. J. Dev. Behav. Pediatr. 2001, 22(6):409-417.
45. Ronesi J.A., Huber K.M. Metabotropic glutamate receptors and fragile x mental retardation protein: partners in translational regulation at the synapse. Sci. Signal. 2008, 1(5):pe6.
46. Rushworth M.F., Mars R.B., Sallet J. Are there specialized circuits for social cognition and are they unique to humans?. Curr. Opin. Neurobiol. 2013, 23(3):436-442.
47. Sabaratnam M., Murthy N.V., Wijeratne A., Buckingham A., Payne S. Autistic-like behaviour profile and psychiatric morbidity in Fragile X Syndrome: a prospective ten-year follow-up study. Eur. Child Adolesc. Psychiatry 2003, 12(4):172-177.
48. Sapolsky R.M. The influence of social hierarchy on primate health. Science 2005, 308(5722):648-652.
49. Spencer C.M., Alekseyenko O., Serysheva E., Yuva-Paylor L.A., Paylor R. Altered anxiety-related and social behaviors in the Fmr1 knockout mouse model of fragile X syndrome. Genes Brain Behav. 2005, 4(7):420-430.
50. Spencer C.M., Alekseyenko O., Hamilton S.M., Thomas A.M., Serysheva E., Yuva-Paylor L.A., et al. Modifying behavioral phenotypes in Fmr1KO mice: genetic background differences reveal autistic-like responses. Autism Res. 2011, 4(1):40-56.
51. Thomas A.M., Bui N., Graham D., Perkins J.R., Yuva-Paylor L.A., Paylor R. Genetic reduction of group 1 metabotropic glutamate receptors alters select behaviors in a mouse model for fragile X syndrome. Behav. Brain Res. 2011, 223:310-321.
52. Till S.M., Wijetunge L.S., Seidel V.G., Harlow E., Wright A.K., Bagni C., et al. Altered maturation of the primary somatosensory cortex in a mouse model of fragile X syndrome. Hum. Mol. Genet. 2012, 21(10):2143-2156.
53. Timmer M., Cordero M.I., Sevelinges Y., Sandi C. Evidence for a role of oxytocin receptors in the long-term establishment of dominance hierarchies. Neuropsychopharmacology 2011, 36(11):2349-2356.
54. Tranfaglia M.R. The psychiatric presentation of fragile X: evolution of the diagnosis and treatment of the psychiatric comorbidities of fragile X syndrome. Dev. Neurosci. 2011, 33:337-348.
55. Turner G., Webb T., Wake S., Robinson H. Prevalence of fragile X syndrome. Am. J. Med. Genet. 1996, 64(1):196-197.
56. van den Berg W.E., Lamballais S., Kushner S.A. Sex-specific mechanism of social hierarchy in mice. Neuropsychopharmacology 2014, 10.1038/npp.2014.319.
57. van der Kooij M.A., Sandi C. Social memories in rodents: methods, mechanisms and modulation by stress. Neurosci. Biobehav. Rev. 2012, 36(7):1763-1772.
58. Verkerk A.J., Pieretti M., Sutcliffe J.S., Fu Y.H., Kuhl D.P., Pizzuti A., et al. Identification of a gene (FMR-1) containing a CGG repeat coincident with a breakpoint cluster region exhibiting length variation in fragile X syndrome. Cell 1991, 65(5):905-914.
59. Wang F., Zhu J., Zhu H., Zhang Q., Lin Z., Hu H. Bidirectional control of social hierarchy by synaptic efficacy in medial prefrontal cortex. Science 2011, 334(6056):693-697.
60. Wang X., Snape M., Klann E., Stone J.G., Singh A., Petersen R.B., et al. Activation of the extracellular signal-regulated kinase pathway contributes to the behavioral deficit of fragile x-syndrome. J. Neurochem. 2012, 121(4):672-679.
61. Weng N., Weiler I.J., Sumis A., Berry-Kravis E., Greenough W.T. Early-phase ERK activation as a biomarker for metabolic status in fragile X syndrome. Am. J. Med. Genet. B Neuropsychiatr. Genet. 2008, 147B:1253-1257.
62. Yeh S.R., Fricke R.A., Edwards D.H. The effect of social experience on serotonergic modulation of the escape circuit of crayfish. Science 1996, 271(5247):366-369.