Altered Social Behaviours in Neurexin 1α Knockout Mice Resemble Core Symptoms in Neurodevelopmental Disorders

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Grayton, Hannah Mary ^a   Missler, Markus ^b   Collier, David Andrew ^c   Fernandes, Cathy ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF MÜNSTER   (Germany)

^c ELI LILLY AND COMPANY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NEUREXIN; NEUREXIN 1 ALPHA; UNCLASSIFIED DRUG;

AGGRESSION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BEHAVIOR DISORDER; CONTROLLED STUDY; DEVELOPMENTAL DISORDER; FEMALE; GENE INACTIVATION; HOMOZYGOTE; LOCOMOTION; MALE; MOUSE; NEURODEVELOPMENTAL DISORDER; NEUROLOGIC DISEASE; NONHUMAN; SOCIAL BEHAVIOR; SYMPTOM;

AGGRESSION; ANIMALS; ANXIETY; DEVELOPMENTAL DISABILITIES; DISEASE MODELS, ANIMAL; FEMALE; GLYCOPROTEINS; HUMANS; MALE; MEMORY DISORDERS; MEMORY, EPISODIC; MENTAL DISORDERS; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; MOTOR ACTIVITY; NESTING BEHAVIOR; NEUROPEPTIDES; SOCIAL BEHAVIOR;

MUS;

EID: 84879522237     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0067114     Document Type: Article

References (70)

1. Ushkaryov YA, Petrenko AG, Geppert M, Sudhof TC, (1992) Neurexins: synaptic cell surface proteins related to the alpha-latrotoxin receptor and laminin. Science. 257: 50-56.
2. Ichtchenko K, Hata Y, Nguyen T, Ullrich B, Missler M, et al. (1995) Neuroligin 1: a splice site-specific ligand for beta-neurexins. Cell. 81: 435-443.
3. Reissner CRF, Missler M. Neurexins. Genome Biology. In press.
4. Missler M, Zhang W, Rohlmann A, Kattenstroth G, Hammer RE, et al. (2003) Alpha-neurexins couple Ca2+ channels to synaptic vesicle exocytosis. Nature. 423: 939-948.
5. Rozic G, Lupowitz Z, Piontkewitz Y, Zisapel N, (2011) Dynamic changes in neurexins' alternative splicing: role of Rho-associated protein kinases and relevance to memory formation. PloS one. 6: e18579.
6. Rozic-Kotliroff G, Zisapel N, (2007) Ca2+-dependent splicing of neurexin IIalpha. Biochemical and biophysical research communications. 352: 226-230.
7. Iijima T, Wu K, Witte H, Hanno-Iijima Y, Glatter T, et al. (2011) SAM68 regulates neuronal activity-dependent alternative splicing of neurexin-1. Cell. 147: 1601-1614.
8. Kattenstroth G, Tantalaki E, Sudhof TC, Gottmann K, Missler M, (2004) Postsynaptic N-methyl-D-aspartate receptor function requires alpha-neurexins. Proceedings of the National Academy of Sciences of the United States of America. 101: 2607-2612.
9. Zhang W, Rohlmann A, Sargsyan V, Aramuni G, Hammer RE, et al. (2005) Extracellular domains of alpha-neurexins participate in regulating synaptic transmission by selectively affecting N- and P/Q-type Ca2+ channels. The Journal of neuroscience: the official journal of the Society for Neuroscience. 25: 4330-4342.
10. Dudanova I, Sedej S, Ahmad M, Masius H, Sargsyan V, et al. (2006) Important contribution of alpha-neurexins to Ca2+-triggered exocytosis of secretory granules. The Journal of neuroscience: the official journal of the Society for Neuroscience. 26: 10599-10613.
11. Feng J, Schroer R, Yan J, Song W, Yang C, et al. (2006) High frequency of neurexin 1beta signal peptide structural variants in patients with autism. Neuroscience letters. 409: 10-13.
12. Zahir FR, Baross A, Delaney AD, Eydoux P, Fernandes ND, et al. (2008) A patient with vertebral, cognitive and behavioural abnormalities and a de novo deletion of NRXN1alpha. Journal of medical genetics. 45: 239-243.
13. Kirov G, Gumus D, Chen W, Norton N, Georgieva L, et al. (2008) Comparative genome hybridization suggests a role for NRXN1 and APBA2 in schizophrenia. Human molecular genetics. 17: 458-465.
14. Walsh T, McClellan JM, McCarthy SE, Addington AM, Pierce SB, et al. (2008) Rare structural variants disrupt multiple genes in neurodevelopmental pathways in schizophrenia. Science. 320: 539-543.
15. Rujescu D, Ingason A, Cichon S, Pietilainen OP, Barnes MR, et al. (2009) Disruption of the neurexin 1 gene is associated with schizophrenia. Human molecular genetics. 18: 988-996.
16. Ching MS, Shen Y, Tan WH, Jeste SS, Morrow EM, et al. (2010) Deletions of NRXN1 (neurexin-1) predispose to a wide spectrum of developmental disorders. American journal of medical genetics Part B, Neuropsychiatric genetics: the official publication of the International Society of Psychiatric Genetics. 153B: 937-947.
17. Gregor A, Albrecht B, Bader I, Bijlsma EK, Ekici AB, et al. (2011) Expanding the clinical spectrum associated with defects in CNTNAP2 and NRXN1. BMC medical genetics. 12: 106.
18. Zweier C, de Jong EK, Zweier M, Orrico A, Ousager LB, et al. (2009) CNTNAP2 and NRXN1 are mutated in autosomal-recessive Pitt-Hopkins-like mental retardation and determine the level of a common synaptic protein in Drosophila. American journal of human genetics. 85: 655-666.
19. Harrison V, Connell L, Hayesmoore J, McParland J, Pike MG, et al. (2011) Compound heterozygous deletion of NRXN1 causing severe developmental delay with early onset epilepsy in two sisters. American journal of medical genetics Part A. 155A: 2826-2831.
20. Schaaf CP, Boone PM, Sampath S, Williams C, Bader PI, et al. (2012) Phenotypic spectrum and genotype-phenotype correlations of NRXN1 exon deletions. European journal of human genetics: EJHG. 20: 1240-1247.
21. Etherton MR, Blaiss CA, Powell CM, Sudhof TC, (2009) Mouse neurexin-1alpha deletion causes correlated electrophysiological and behavioral changes consistent with cognitive impairments. Proceedings of the National Academy of Sciences of the United States of America. 106: 17998-18003.
22. Laarakker MC, Reinders NR, Bruining H, Ophoff RA, Kas MJ, (2012) Sex-dependent novelty response in neurexin-1alpha mutant mice. PloS one. 7: e31503.
23. Gerlai R, (1996) Gene-targeting studies of mammalian behavior: is it the mutation or the background genotype? Trends in neurosciences. 19: 177-181.
24. Wolfer DP, Crusio WE, Lipp HP, (2002) Knockout mice: simple solutions to the problems of genetic background and flanking genes. Trends in neurosciences. 25: 336-340.
25. Bucan M, Abel T, (2002) The mouse: genetics meets behaviour. Nature reviews Genetics. 3: 114-123.
26. Reichelt AC, Rodgers RJ, Clapcote SJ, (2012) The role of neurexins in schizophrenia and autistic spectrum disorder. Neuropharmacology. 62: 1519-1526.
27. Kas MJ, Fernandes C, Schalkwyk LC, Collier DA, (2007) Genetics of behavioural domains across the neuropsychiatric spectrum; of mice and men. Molecular psychiatry. 12: 324-330.
28. Lad HV, Liu L, Paya-Cano JL, Parsons MJ, Kember R, et al. (2010) Behavioural battery testing: evaluation and behavioural outcomes in 8 inbred mouse strains. Physiology & behavior. 99: 301-316.
29. Easton AC, Lucchesi W, Schumann G, Giese KP, Muller CP, et al. (2011) alphaCaMKII autophosphorylation controls exploratory activity to threatening novel stimuli. Neuropharmacology. 61: 1424-1431.
30. Fernandes C, Hoyle E, Dempster E, Schalkwyk LC, Collier DA, (2006) Performance deficit of alpha7 nicotinic receptor knockout mice in a delayed matching-to-place task suggests a mild impairment of working/episodic-like memory. Genes, brain, and behavior. 5: 433-440.
31. Yang M, Silverman JL, Crawley JN (2011) Automated three-chambered social approach task for mice. Current protocols in neuroscience/editorial board, Jacqueline N Crawley [et al]. Chapter 8: Unit 8 26.
32. Winslow JT (2003) Mouse social recognition and preference. Current protocols in neuroscience/editorial board, Jacqueline N Crawley [et al]. Chapter 8: Unit 8 16.
33. Yang M, Crawley JN (2009) Simple behavioral assessment of mouse olfaction. Current protocols in neuroscience/editorial board, Jacqueline N Crawley [et al]. Chapter 8: Unit 8 24.
34. Radyushkin K, Hammerschmidt K, Boretius S, Varoqueaux F, El-Kordi A, et al. (2009) Neuroligin-3-deficient mice: model of a monogenic heritable form of autism with an olfactory deficit. Genes, brain, and behavior. 8: 416-425.
35. Silverman JL, Yang M, Lord C, Crawley JN, (2010) Behavioural phenotyping assays for mouse models of autism. Nature reviews Neuroscience. 11: 490-502.
36. Blundell J, Tabuchi K, Bolliger MF, Blaiss CA, Brose N, et al. (2009) Increased anxiety-like behavior in mice lacking the inhibitory synapse cell adhesion molecule neuroligin 2. Genes, brain, and behavior. 8: 114-126.
37. Boucard AA, Chubykin AA, Comoletti D, Taylor P, Sudhof TC, (2005) A splice code for trans-synaptic cell adhesion mediated by binding of neuroligin 1 to alpha- and beta-neurexins. Neuron. 48: 229-236.
38. Reissner C, Klose M, Fairless R, Missler M, (2008) Mutational analysis of the neurexin/neuroligin complex reveals essential and regulatory components. Proceedings of the National Academy of Sciences of the United States of America. 105: 15124-15129.
39. Association AP (2000) Diagnostic and statistical manual of mental disorders. 4 ed. Washington, DC: Author.
40. Doty RL, (1986) Odor-guided behavior in mammals. Experientia. 42: 257-271.
41. Lijam N, Paylor R, McDonald MP, Crawley JN, Deng CX, et al. (1997) Social interaction and sensorimotor gating abnormalities in mice lacking Dvl1. Cell. 90: 895-905.
42. Peripato AC, Cheverud JM, (2002) Genetic influences on maternal care. The American naturalist. 160Suppl 6: S173-185.
43. Piskulic D, Olver JS, Norman TR, Maruff P, (2007) Behavioural studies of spatial working memory dysfunction in schizophrenia: a quantitative literature review. Psychiatry research. 150: 111-121.
44. Kim HG, Kishikawa S, Higgins AW, Seong IS, Donovan DJ, et al. (2008) Disruption of neurexin 1 associated with autism spectrum disorder. American journal of human genetics. 82: 199-207.
45. Elvevag B, Goldberg TE, (2000) Cognitive impairment in schizophrenia is the core of the disorder. Critical reviews in neurobiology. 14: 1-21.
46. Wing L, (1981) Language, social, and cognitive impairments in autism and severe mental retardation. Journal of autism and developmental disorders. 11: 31-44.
47. St John RD, Corning PA, (1973) Maternal aggression in mice. Behavioral biology. 9: 635-639.
48. vom Saal FS, Svare B, Gandelman R, (1976) Time of neonatal androgen exposure influences length of testosterone treatment required to induce aggression in adult male and female mice. Behavioral biology. 17: 391-397.
49. Parmigiani S, Ferrari PF, Palanza P, (1998) An evolutionary approach to behavioral pharmacology: using drugs to understand proximate and ultimate mechanisms of different forms of aggression in mice. Neuroscience and biobehavioral reviews. 23: 143-153.
50. Brown RZ, (1953) Social behaviour, reproduction and population changes in the house mouse. Ecol Monogr. 23: 23.
51. Mohn AR, Gainetdinov RR, Caron MG, Koller BH, (1999) Mice with reduced NMDA receptor expression display behaviors related to schizophrenia. Cell. 98: 427-436.
52. 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. Human molecular genetics. 14: 205-220.
53. Takao K, Kobayashi K, Hagihara H, Ohira K, Shoji H, et al. (2013) Deficiency of Schnurri-2, an MHC Enhancer Binding Protein, Induces Mild Chronic Inflammation in the Brain and Confers Molecular, Neuronal, and Behavioral Phenotypes Related to Schizophrenia. Neuropsychopharmacology: official publication of the American College of Neuropsychopharmacology.
54. Schneider CW, Chenoweth MB, (1970) Effects of hallucinogenic and other drugs on the nest-building behaviour of mice. Nature. 225: 1262-1263.
55. Davisson MT, (1997) Rules and guidelines for genetic nomenclature in mice: excerpted version. Committee on Standardized Genetic Nomenclature for Mice. Transgenic research. 6: 309-319.
56. Nielsen DM, Derber WJ, McClellan DA, Crnic LS, (2002) Alterations in the auditory startle response in Fmr1 targeted mutant mouse models of fragile X syndrome. Brain research. 927: 8-17.
57. Moy SS, Nadler JJ, Magnuson TR, Crawley JN, (2006) Mouse models of autism spectrum disorders: the challenge for behavioral genetics. American journal of medical genetics Part C, Seminars in medical genetics. 142C: 40-51.
58. Fernando AB, Robbins TW, (2011) Animal models of neuropsychiatric disorders. Annual review of clinical psychology. 7: 39-61.
59. Nestler EJ, Hyman SE, (2010) Animal models of neuropsychiatric disorders. Nature neuroscience. 13: 1161-1169.
60. Nomura J, Takumi T, (2012) Animal models of psychiatric disorders that reflect human copy number variation. Neural plasticity. 2012: 589524.
61. Sebat J, Lakshmi B, Malhotra D, Troge J, Lese-Martin C, et al. (2007) Strong association of de novo copy number mutations with autism. Science. 316: 445-449.
62. Marshall CR, Noor A, Vincent JB, Lionel AC, Feuk L, et al. (2008) Structural variation of chromosomes in autism spectrum disorder. American journal of human genetics. 82: 477-488.
63. Weiss LA, Shen Y, Korn JM, Arking DE, Miller DT, et al. (2008) Association between microdeletion and microduplication at 16p11.2 and autism. The New England journal of medicine. 358: 667-675.
64. Pinto D, Pagnamenta AT, Klei L, Anney R, Merico D, et al. (2010) Functional impact of global rare copy number variation in autism spectrum disorders. Nature. 466: 368-372.
65. Sharp AJ, Mefford HC, Li K, Baker C, Skinner C, et al. (2008) A recurrent 15q13.3 microdeletion syndrome associated with mental retardation and seizures. Nature genetics. 40: 322-328.
66. Stefansson H, Rujescu D, Cichon S, Pietilainen OP, Ingason A, et al. (2008) Large recurrent microdeletions associated with schizophrenia. Nature. 455: 232-236.
67. Ghebranious N, Giampietro PF, Wesbrook FP, Rezkalla SH, (2007) A novel microdeletion at 16p11.2 harbors candidate genes for aortic valve development, seizure disorder, and mild mental retardation. American journal of medical genetics Part A. 143A: 1462-1471.
68. Brunetti-Pierri N, Berg JS, Scaglia F, Belmont J, Bacino CA, et al. (2008) Recurrent reciprocal 1q21.1 deletions and duplications associated with microcephaly or macrocephaly and developmental and behavioral abnormalities. Nature genetics. 40: 1466-1471.
69. Grayton HM, Fernandes C, Rujescu D, Collier DA, (2012) Copy number variations in neurodevelopmental disorders. Progress in neurobiology. 99: 81-91.
70. Voineskos AN, Lett TA, Lerch JP, Tiwari AK, Ameis SH, et al. (2011) Neurexin-1 and frontal lobe white matter: an overlapping intermediate phenotype for schizophrenia and autism spectrum disorders. PloS one. 6: e20982.