Deletion of α-neurexin II results in autism-related behaviors in mice

Translational Psychiatry

Volumn 4, Issue 11, 2014, Pages

  Dachtler, J ^a   Glasper, J ^b   Cohen, R N ^a   Ivorra, J L ^a   Swiffen, D J ^a   Jackson, A J ^a   Harte, M K ^b   Rodgers, R J ^a   Clapcote, S J ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA NEUREXIN 2; AMPA RECEPTOR; GLUTAMATE DECARBOXYLASE 65; GLUTAMATE DECARBOXYLASE 67; MESSENGER RNA; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2A; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; NEUREXIN; NEUROLIGIN; PARVALBUMIN; POSTSYNAPTIC DENSITY PROTEIN 93; POSTSYNAPTIC DENSITY PROTEIN 95; PROTEIN; PROTEIN HOMER 1; SYNTAXIN BINDING PROTEIN 1; UNCLASSIFIED DRUG; VESICULAR GLUTAMATE TRANSPORTER; VESICULAR INHIBITORY AMINO ACID TRANSPORTER; NERVE PROTEIN; NEUREXIN II;

ADULT; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY; ARTICLE; AUTISM; BEHAVIOR ASSESSMENT; BEHAVIOR DISORDER; CLINICAL ASSESSMENT; COMPARATIVE STUDY; CONTROLLED STUDY; DISEASE TRANSMISSION; EXPLORATORY BEHAVIOR; FRONTAL CORTEX; GENE DELETION; GENE EXPRESSION; GENE MUTATION; GENETIC ANALYSIS; HIPPOCAMPUS; MAZE TEST; MOUSE; NONHUMAN; PASSIVE AVOIDANCE; PATHOGENESIS; PHENOTYPIC VARIATION; PREPULSE INHIBITION; PRESYNAPTIC MEMBRANE; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SOCIAL BEHAVIOR; SURVIVAL RATE; WILD TYPE; YOUNG ADULT; ANIMAL; AVOIDANCE BEHAVIOR; BRAIN CORTEX; C57BL MOUSE; GENETICS; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY; SYNAPTIC TRANSMISSION;

ANIMALS; ANXIETY; AUTISTIC DISORDER; AVOIDANCE LEARNING; BEHAVIOR, ANIMAL; CEREBRAL CORTEX; HIPPOCAMPUS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; PREPULSE INHIBITION; SOCIAL BEHAVIOR; SYNAPTIC TRANSMISSION;

EID: 84925355681     PISSN: None     EISSN: 21583188     Source Type: Journal    
DOI: 10.1038/tp.2014.123     Document Type: Article

References (50)

1. Rosenberg RE, Law JK, Yenokyan G, McGready J, Kaufmann WE, Law PA. Characteristics and concordance of autism spectrum disorders among 277 twin pairs. Arch Pediatr Adolesc Med 2009; 163: 907-914.
2. Li X, Zou H, Brown WT. Genes associated with autism spectrum disorder. Brain Res Bull 2012; 88: 543-552.
3. Pinto D, Pagnamenta AT, Klei L, Anney R, Merico D, Regan R et al. Functional impact of global rare copy number variation in autism spectrum disorders. Nature 2010; 466: 368-372.
4. Biederer T, Sudhof TC. Mints as adaptors. Direct binding to neurexins and recruitment of munc18. J Biol Chem 2000; 275: 39803-39806.
5. Grootjans JJ, Reekmans G, Ceulemans H, David G. Syntenin-syndecan binding requires syndecan-synteny and the co-operation of both PDZ domains of syntenin. J Biol Chem 2000; 275: 19933-19941.
6. Hata Y, Butz S, Sudhof TC. CASK: a novel dlg/PSD95 homolog with an N-terminal calmodulin-dependent protein kinase domain identified by interaction with neurexins. J Neurosci 1996; 16: 2488-2494.
7. Ylisaukko-oja T, Rehnstrom K, Auranen M, Vanhala R, Alen R, Kempas E et al. Analysis of four neuroligin genes as candidates for autism. Eur J Hum Genet 2005; 13: 1285-1292.
8. Chubykin AA, Atasoy D, Etherton MR, Brose N, Kavalali ET, Gibson JR et al. Activitydependent validation of excitatory versus inhibitory synapses by neuroligin-1 versus neuroligin-2. Neuron 2007; 54: 919-931.
9. Craig AM, Kang Y. Neurexin-neuroligin signaling in synapse development. Curr Opin Neurobiol 2007; 17: 43-52.
10. de Wit J, Sylwestrak E, O'Sullivan ML, Otto S, Tiglio K, Savas JN et al. LRRTM2 interacts with Neurexin1 and regulates excitatory synapse formation. Neuron 2009; 64: 799-806.
11. Rowen L, Young J, Birditt B, Kaur A, Madan A, Philipps DL et al. Analysis of the human neurexin genes: alternative splicing and the generation of protein diversity. Genomics 2002; 79: 587-597.
12. Gauthier J, Siddiqui TJ, Huashan P, Yokomaku D, Hamdan FF, Champagne N et al. Truncating mutations in NRXN2 and NRXN1 in autism spectrum disorders and schizophrenia. Hum Genet 2011; 130: 563-573.
13. Mohrmann I, Gillessen-Kaesbach G, Siebert R, Caliebe A, Hellenbroich Y. A de novo 0.57 Mb microdeletion in chromosome 11q13.1 in a patient with speech problems, autistic traits, dysmorphic features and multiple endocrine neoplasia type 1. Eur J Med Genet 2011; 54: e461-e464.
14. Missler M, Zhang W, Rohlmann A, Kattenstroth G, Hammer RE, Gottmann K et al. Alpha-neurexins couple Ca2+ channels to synaptic vesicle exocytosis. Nature 2003; 423: 939-948.
15. Dudanova I, Tabuchi K, Rohlmann A, Sudhof TC, Missler M. Deletion of alphaneurexins does not cause a major impairment of axonal pathfinding or synapse formation. J Comp Neurol 2007; 502: 261-274.
16. Andersen CL, Jensen JL, Orntoft TF. Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res 2004; 64: 5245-5250.
17. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001; 25: 402-408.
18. Rapin I, Tuchman RF. Autism: definition, neurobiology, screening, diagnosis. Pediatr Clin North Am 2008; 55: 1129-1146, viii.
19. Moy SS, Nadler JJ, Perez A, Barbaro RP, Johns JM, Magnuson TR et al. Sociability and preference for social novelty in five inbred strains: an approach to assess autistic-like behavior in mice. Genes Brain Behav 2004; 3: 287-302.
20. White SW, Oswald D, Ollendick T, Scahill L. Anxiety in children and adolescents with autism spectrum disorders. Clin Psychol Rev 2009; 29: 216-229.
21. South M, Dana J, White SE, Crowley MJ. Failure is not an option: Risk-taking is moderated by anxiety and also by cognitive ability in children and adolescents diagnosed with an autism spectrum disorder. J Autism Dev Disord 2011; 41: 55-65.
22. Simon P, Dupuis R, Costentin J. Thigmotaxis as an index of anxiety in mice. Influence of dopaminergic transmissions. Behav Brain Res 1994; 61: 59-64.
23. Pare WP, Tejani-Butt S, Kluczynski J. The emergence test: effects of psychotropic drugs on neophobic disposition in Wistar Kyoto (WKY) and Sprague Dawley rats. Prog Neuropsychopharmacol Biol Psychiatry 2001; 25: 1615-1628.
24. Belzung C, Berton F. Further pharmacological validation of the BALB/c neophobia in the free exploratory paradigm as an animal model of trait anxiety. Behav Pharmacol 1997; 8: 541-548.
25. Avgustinovich DF, Lipina TV, Bondar NP, Alekseyenko OV, Kudryavtseva NN. Features of the genetically defined anxiety in mice. Behav Genet 2000; 30: 101-109.
26. Kohl S, Heekeren K, Klosterkotter J, Kuhn J. Prepulse inhibition in psychiatric disorders-apart from schizophrenia. J Psychiatr Res 2013; 47: 445-452.
27. Oranje B, Lahuis B, van Engeland H, Jan van der Gaag R, Kemner C. Sensory and sensorimotor gating in children with multiple complex developmental disorders (MCDD) and autism. Psychiatry Res 2013; 206: 287-292.
28. Perry W, Minassian A, Lopez B, Maron L, Lincoln A. Sensorimotor gating deficits in adults with autism. Biol Psychiatry. 2007; 61: 482-486.
29. Fombonne E. Epidemiological surveys of autism and other pervasive developmental disorders: an update. J Autism Dev Disord 2003; 33: 365-382.
30. Baarendse PJ, van Grootheest G, Jansen RF, Pieneman AW, Ogren SO, Verhage M et al. Differential involvement of the dorsal hippocampus in passive avoidance in C57bl/6J and DBA/2J mice. Hippocampus 2008; 18: 11-19.
31. Blundell J, Blaiss CA, Etherton MR, Espinosa F, Tabuchi K, Walz C et al. Neuroligin-1 deletion results in impaired spatial memory and increased repetitive behavior. J Neurosci 2010; 30: 2115-2129.
32. Aylward EH, Minshew NJ, Goldstein G, Honeycutt NA, Augustine AM, Yates KO et al. MRI volumes of amygdala and hippocampus in non-mentally retarded autistic adolescents and adults. Neurology 1999; 53: 2145-2150.
33. Carper RA, Courchesne E. Localized enlargement of the frontal cortex in early autism. Biol Psychiatry 2005; 57: 126-133.
34. Rizo J, Sudhof TC. Snares and Munc18 in synaptic vesicle fusion. Nat Rev Neurosci 2002; 3: 641-653.
35. Reichelt AC, Rodgers RJ, Clapcote SJ. The role of neurexins in schizophrenia and autistic spectrum disorder. Neuropharmacology 2012; 62: 1519-1526.
36. Grayton HM, Missler M, Collier DA, Fernandes C. Altered social behaviours in neurexin 1alpha knockout mice resemble core symptoms in neurodevelopmental disorders. PLoS One 2013; 8: e67114.
37. Etherton MR, Blaiss CA, Powell CM, Sudhof TC. Mouse neurexin-1alpha deletion causes correlated electrophysiological and behavioral changes consistent with cognitive impairments. Proc Natl Acad Sci USA 2009; 106: 17998-18003.
38. Peca J, Feliciano C, Ting JT, Wang W, Wells MF, Venkatraman TN et al. Shank3 mutant mice display autistic-like behaviours and striatal dysfunction. Nature 2011; 472: 437-442.
39. Wang X, McCoy PA, Rodriguiz RM, Pan Y, Je HS, Roberts AC et al. Synaptic dysfunction and abnormal behaviors in mice lacking major isoforms of Shank3. Hum Mol Genet 2011; 20: 3093-3108.
40. Horev G, Ellegood J, Lerch JP, Son YE, Muthuswamy L, Vogel H et al. Dosagedependent phenotypes in models of 16p11.2 lesions found in autism. Proc Natl Acad Sci USA 2011; 108: 17076-17081.
41. Matson JL, Shoemaker M. Intellectual disability and its relationship to autism spectrum disorders. Res Dev Disabil 2009; 30: 1107-1114.
42. Ching MSL, Shen Y, Tan W-H, Jeste SS, Morrow EM, Chen X et al. Deletions of NRXN1 (Neurexin-1) predispose to a wide spectrum of developmental disorders. Am J Med Genet B Neuropsychiatr Genet 2010; 153B: 937-947.
43. Song JY, Ichtchenko K, Südhof TC, Brose N. Neuroligin 1 is a postsynaptic celladhesion molecule of excitatory synapses. Proc Natl Acad Sci USA 1999; 96: 1100-1105.
44. Muers M. Gene expression: transcriptome to proteome and back to genome. Nat Rev Genet 2011; 12: 518.
45. Schwanhaüsser B, Busse D, Li N, Dittmar G, Schuchhardt J, Wolf J et al. Global quantification of mammalian gene expression control. Nature 2011; 473: 337-342.
46. Glessner JT, Wang K, Cai G, Korvatska O, Kim CE, Wood S et al. Autism genomewide copy number variation reveals ubiquitin and neuronal genes. Nature 2009; 459: 569-573.
47. Verhage M, Maia AS, Plomp JJ, Brussaard AB, Heeroma JH, Vermeer H et al. Synaptic assembly of the brain in the absence of neurotransmitter secretion. Science 2000; 287: 864-869.
48. Weimer RM, Richmond JE, Davis WS, Hadwiger G, Nonet ML, Jorgensen EM. Defects in synaptic vesicle docking in unc-18 mutants. Nat Neurosci 2003; 6: 1023-1030.
49. Toonen RF, Wierda K, Sons MS, de Wit H, Cornelisse LN, Brussaard A et al. Munc18-1 expression l evels control synapse recovery by regulating readily releasable pool size. Proc Natl Acad Sci USA 2006; 103: 18332-18337.
50. Hager T, Maroteaux G, Pont PD, Julsing J, van Vliet R, Stiedl O. Munc18-1 haploinsufficiency results in enhanced anxiety-like behavior as determined by heart rate responses in mice. Behav Brain Res 2014; 260: 44-52.