Haploinsufficiency of the autism candidate gene Neurobeachin induces autism-like behaviors and affects cellular and molecular processes of synaptic plasticity in mice

Neurobiology of Disease

Volumn 51, Issue , 2013, Pages 144-151

  Nuytens, Kim ^a   Gantois, Ilse ^a   Stijnen, Pieter ^a   Iscru, Emilia ^a   Laeremans, Annelies ^a   Serneels, Lutgarde ^a,e   Van Eylen, Lien ^a,b   Liebhaber, Stephen A ^c   Devriendt, Koen ^a,d   Balschun, Detlef ^a   Arckens, Lutgarde ^a   Creemers, John W M ^a   D'Hooge, Rudi ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^c UNIVERSITY HOSPITALS LEUVEN   (Belgium)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

^e UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

ASD; BDNF; Behavior; CREB; Mouse; Neurobeachin

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN A;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTISM; CONTROLLED STUDY; CORPUS STRIATUM; DORSOMEDIAL STRIATUM; EIF268 GENE; FEAR; FEMALE; GENE; GENE EXPRESSION; GENE MAPPING; GROOMING; HAPLOINSUFFICIENCY; HIPPOCAMPAL CA1 REGION; IMMEDIATE EARLY GENE; IN SITU HYBRIDIZATION; LONG TERM POTENTIATION; MOUSE; NERVE CELL PLASTICITY; NEUROBEACHIN; NONHUMAN; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SOCIAL BEHAVIOR; SPATIAL LEARNING; SPATIAL MEMORY;

ANIMALS; AUTISTIC DISORDER; BEHAVIOR, ANIMAL; BRAIN; CARRIER PROTEINS; CHILD; FEMALE; HAPLOINSUFFICIENCY; HUMANS; IMMUNOBLOTTING; IN SITU HYBRIDIZATION; LEARNING; LONG-TERM POTENTIATION; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; NEURONAL PLASTICITY; PHENOTYPE; SYNAPTIC TRANSMISSION;

EID: 84872821207     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2012.11.004     Document Type: Article

References (63)

1. Abrahams B., Geschwind D. Advances in autism genetics: on the threshold of a new neurobiology. Nat. Rev. Genet. 2008, 9:341-355.
2. Barco A., et al. Expression of constitutively active CREB protein facilitates the late phase of long-term potentiation by enhancing synaptic capture. Cell 2002, 108:689-703.
3. Barco A., et al. Gene expression profiling of facilitated L-LTP in VP16-CREB mice reveals that BDNF is critical for the maintenance of LTP and its synaptic capture. Neuron 2005, 48:123-137.
4. Berridge K.C. Progressive degradation of serial grooming chains by descending decerebration. Behav. Brain Res. 1989, 33:241-253.
5. Bozon B., et al. MAPK, CREB and zif268 are all required for the consolidation of recognition memory. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2003, 358:805-814.
6. Breidenbach M., Brunger A. New insights into clostridial neurotoxin-SNARE interactions. Trends Mol. Med. 2005, 11:377-381.
7. Burgess A., et al. A concanavalin A-like lectin domain in the CHS1/LYST protein, shared by members of the BEACH family. Bioinformatics 2009, 25:1219-1222.
8. Castermans D., et al. The neurobeachin gene is disrupted by a translocation in a patient with idiopathic autism. J. Med. Genet. 2003, 40:352-356.
9. Castermans D., et al. SCAMP5, NBEA and AMISYN: three candidate genes for autism involved in secretion of large dense-core vesicles. Hum. Mol. Genet. 2010, 19:1368-1378.
10. Corstens G.J., et al. The effects of disruption of A kinase anchoring protein-protein kinase A association on protein kinase A signalling in neuroendocrine melanotroph cells of Xenopus laevis. J. Neuroendocrinol. 2006, 18:477-483.
11. Crawley J.N., et al. Behavioral phenotypes of inbred mouse strains: implications and recommendations for molecular studies. Psychopharmacology (Berl) 1997, 132:107-124.
12. D'Hooge R., De Deyn P.P. Applications of the Morris water maze in the study of learning and memory. Brain Res. Brain Res. Rev. 2001, 36:60-90.
13. D'Hooge R., et al. Neurocognitive and psychotiform behavioral alterations and enhanced hippocampal long-term potentiation in transgenic mice displaying neuropathological features of human alpha-mannosidosis. J. Neurosci. 2005, 25:6539-6549.
14. Dillon G.M., et al. Excitotoxic lesions restricted to the dorsal CA1 field of the hippocampus impair spatial memory and extinction learning in C57BL/6 mice. Neurobiol. Learn. Mem. 2008, 90:426-433.
15. Fombonne E. Epidemiology of pervasive developmental disorders. Pediatr. Res. 2009, 65:591-598.
16. Franklin K.B., Paxinos G. The Mouse Brain in Stereotaxic Coordinates 2008, Academic Press, San Diego.
17. Gebauer D., et al. Crystal structure of the PH-BEACH domains of human LRBA/BGL. Biochemistry 2004, 43:14873-14880.
18. Goddyn H., et al. Differences in behavioural test battery performance between mice with hippocampal and cerebellar lesions. Behav. Brain Res. 2006, 173:138-147.
19. Gonzalez G.A., Montminy M.R. Cyclic AMP stimulates somatostatin gene transcription by phosphorylation of CREB at serine 133. Cell 1989, 59:675-680.
20. Guzowski J.F., et al. Experience-dependent gene expression in the rat hippocampus after spatial learning: a comparison of the immediate-early genes Arc, c-fos, and zif268. J. Neurosci. 2001, 21:5089-5098.
21. Ito W., et al. Enhanced generalization of auditory conditioned fear in juvenile mice. Learn. Mem. 2009, 16:187-192.
22. Iwaniuk K.M., et al. Network-like impact of MicroRNAs on neuronal lineage differentiation of unrestricted somatic stem cells from human cord blood (USSC). Stem Cells Dev. 2010.
23. Jogl G., et al. Crystal structure of the BEACH domain reveals an unusual fold and extensive association with a novel PH domain. EMBO J. 2002, 21:4785-4795.
24. Jolas T., et al. Long-term potentiation is increased in the CA1 area of the hippocampus of APP(swe/ind) CRND8 mice. Neurobiol. Dis. 2002, 11:394-409.
25. Jones M.W., et al. A requirement for the immediate early gene Zif268 in the expression of late LTP and long-term memories. Nat. Neurosci. 2001, 4:289-296.
26. Lee R., et al. Regulation of cell survival by secreted proneurotrophins. Science 2001, 294:1945-1948.
27. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25:402-408.
28. Lopez de Armentia M., et al. cAMP response element-binding protein-mediated gene expression increases the intrinsic excitability of CA1 pyramidal neurons. J. Neurosci. 2007, 27:13909-13918.
29. McCaffery P., Deutsch C.K. Macrocephaly and the control of brain growth in autistic disorders. Prog. Neurobiol. 2005, 77:38-56.
30. Medrihan L., et al. Neurobeachin, a protein implicated in membrane protein traffic and autism, is required for the formation and functioning of central synapses. J. Physiol. 2009.
31. Moy S.S., et al. Social approach in genetically engineered mouse lines relevant to autism. Genes Brain Behav. 2009, 8:129-142.
32. Nadler J.J., et al. Automated apparatus for quantitation of social approach behaviors in mice. Genes Brain Behav. 2004, 3:303-314.
33. Naert A., et al. Nocturnal hyperactivity, increased social novelty preference and delayed extinction of fear responses in post-weaning socially isolated mice. Brain Res. Bull. 2011, 85:354-362.
34. Nguyen P.V., et al. Strain-dependent differences in LTP and hippocampus-dependent memory in inbred mice. Learn. Mem. 2000, 7:170-179.
35. Nickl-Jockschat T., Michel T.M. The role of neurotrophic factors in autism. Mol. Psychiatry 2011, 16:478-490.
36. Niesmann K., et al. Dendritic spine formation and synaptic function require neurobeachin. Nat. Commun. 2011, 2:557.
37. Olszewski P.K., et al. Neurobeachin, a regulator of synaptic protein targeting, is associated with body fat mass and feeding behavior in mice and body-mass index in humans. PLoS Genet. 2012, 8:e1002568.
38. Paradee W., et al. Fragile X mouse: strain effects of knockout phenotype and evidence suggesting deficient amygdala function. Neuroscience 1999, 94:185-192.
39. Parent A., et al. Synaptic transmission and hippocampal long-term potentiation in transgenic mice expressing FAD-linked presenilin 1. Neurobiol. Dis. 1999, 6:56-62.
40. Perry W., et al. Sensorimotor gating deficits in adults with autism. Biol. Psychiatry 2007, 61:482-486.
41. Piccart E., et al. Impaired appetitively as well as aversively motivated behaviors and learning in PDE10A-deficient mice suggest a role for striatal signaling in evaluative salience attribution. Neurobiol. Learn. Mem. 2011, 95:260-269.
42. Porte Y., et al. Spatial memory in the Morris water maze and activation of cyclic AMP response element-binding (CREB) protein within the mouse hippocampus. Learn. Mem. 2008, 15:885-894.
43. Reddy K. Cytogenetic abnormalities and fragile-X syndrome in autism spectrum disorder. BMC Med. Genet. 2005, 6:3.
44. Renaudineau S., et al. Impaired long-term stability of CA1 place cell representation in mice lacking the transcription factor zif268/egr1. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:11771-11775.
45. Rietman M.L., et al. Candidate genes in ocular dominance plasticity. Front. Neurosci. 2012, 6:11.
46. Ritvo E., et al. Association of autism, retinoblastoma, and reduced esterase D activity. Arch. Gen. Psychiatry 1988, 45:600.
47. Robertson H.R., Feng G. Annual Research Review: transgenic mouse models of childhood-onset psychiatric disorders. J. Child Psychol. Psychiatry 2011, 52:442-475.
48. Segal D.G., et al. Craniofacial and acral growth responses in growth hormone-deficient children treated with growth hormone. J. Pediatr. 2004, 144:437-443.
49. Silverman J.L., et al. Behavioural phenotyping assays for mouse models of autism. Nat. Rev. Neurosci. 2010, 11:490-502.
50. Smith M., et al. Molecular genetic delineation of a deletion of chromosome 13q12→q13 in a patient with autism and auditory processing deficits. Cytogenet. Genome Res. 2002, 98:233-239.
51. Stigler K.A., et al. Structural and functional magnetic resonance imaging of autism spectrum disorders. Brain Res. 2011, 1380:146-161.
52. Su Y., et al. Neurobeachin is essential for neuromuscular synaptic transmission. J. Neurosci. 2004, 24:3627-3636.
53. Suzuki A., et al. Upregulation of CREB-mediated transcription enhances both short- and long-term memory. J. Neurosci. 2011, 31:8786-8802.
54. Taverna F.A., et al. Defective place cell activity in nociceptin receptor knockout mice with elevated NMDA receptor-dependent long-term potentiation. J. Physiol. 2005, 565:579-591.
55. van Brussel L., et al. Identification and localization of functional subdivisions in the visual cortex of the adult mouse. J. Comp. Neurol. 2009, 514:107-116.
56. Van Dam D., et al. Spatial learning, contextual fear conditioning and conditioned emotional response in Fmr1 knockout mice. Behav. Brain Res. 2000, 117:127-136.
57. Viosca J., et al. Chronic enhancement of CREB activity in the hippocampus interferes with the retrieval of spatial information. Learn. Mem. 2009, 16:198-209.
58. Volders K., et al. The autism candidate gene Neurobeachin encodes a scaffolding protein implicated in membrane trafficking and signaling. Curr. Mol. Med. 2011, 11:204-217.
59. Wang X., et al. Neurobeachin: A protein kinase A-anchoring, beige/Chediak-higashi protein homolog implicated in neuronal membrane traffic. J. Neurosci. 2000, 20:8551-8565.
60. Wang X., et al. Synaptic dysfunction and abnormal behaviors in mice lacking major isoforms of Shank3. Hum. Mol. Genet. 2011, 20:3093-3108.
61. Welch J.M., et al. Cortico-striatal synaptic defects and OCD-like behaviours in Sapap3-mutant mice. Nature 2007, 448:894-900.
62. Williams D.L., et al. Verbal and spatial working memory in autism. J. Autism Dev. Disord. 2005, 35:747-756.
63. Yang M., et al. Automated three-chambered social approach task for mice. Curr. Protoc. Neurosci. 2011, (Chapter 8, Unit 8 26).