Reduced axonal localization of a Caps2 splice variant impairs axonal release of BDNF and causes autistic-like behavior in mice

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 51, 2012, Pages 21104-21109

  Sadakata, Tetsushi ^a,b   Shinoda, Yo ^b,c   Oka, Megumi ^a   Sekine, Yukiko ^c   Sato, Yumi ^c   Saruta, Chihiro ^c   Miwa, Hideki ^d   Tanaka, Mika ^e   Itohara, Shigeyoshi ^e   Furuichi, Teiichi ^b,c  

^a GUNMA UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c TOKYO UNIVERSITY OF SCIENCE   (Japan)

^d GUNMA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^e RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

Author keywords

Dense core vesicle; Exocytosis; Mental disorder; Psychiatry

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN PROTEIN; CALCIUM DEPENDENT ACTIVATOR PROTEIN FOR SECRETION 2 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY DISORDER; ARTICLE; AUTISM; BRAIN DEVELOPMENT; CELL DENSITY; CONTROLLED STUDY; FEMALE; GENETIC VARIABILITY; GENOTYPE; HUMAN; INTERNEURON; MALE; MOUSE; NERVE FIBER; NEUROPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN SECRETION; SOCIOPATHY;

ALTERNATIVE SPLICING; ANIMALS; ANXIETY; AUTISTIC DISORDER; AXONS; BRAIN; BRAIN MAPPING; BRAIN-DERIVED NEUROTROPHIC FACTOR; CALCIUM-BINDING PROTEINS; CROSSES, GENETIC; EXOCYTOSIS; EXONS; GENE EXPRESSION REGULATION; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR; MICE; MODELS, GENETIC; MODELS, NEUROLOGICAL; NERVE TISSUE PROTEINS; NEURONS; RISK FACTORS; SOCIAL BEHAVIOR;

MUS;

EID: 84871372880     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1210055109     Document Type: Article

References (45)

1. Binda AV, Kabbani N, Levenson R (2005) Regulation of dense core vesicle release from PC12 cells by interaction between the D2 dopamine receptor and calcium-dependent activator protein for secretion (CAPS). Biochem Pharmacol 69(10):1451-1461.
2. Speidel D, et al. (2005) CAPS1 regulates catecholamine loading of large dense-core vesicles. Neuron 46(1):75-88.
3. Tandon A, et al. (1998) Differential regulation of exocytosis by calcium and CAPS in semi-intact synaptosomes. Neuron 21(1):147-154.
4. Grishanin RN, et al. (2004) CAPS acts at a prefusion step in dense-core vesicle exocytosis as a PIP2 binding protein. Neuron 43(4):551-562.
5. Sadakata T, et al. (2010) Interaction of calcium-dependent activator protein for secretion 1 (CAPS1) with the class II ADP-ribosylation factor small GTPases is required for dense-core vesicle trafficking in the trans-Golgi network. J Biol Chem 285(49):38710-38719.
6. Sadakata T, et al. (2004) The secretory granule-associated protein CAPS2 regulates neurotrophin release and cell survival. J Neurosci 24(1):43-52.
7. Sadakata T, et al. (2007) Impaired cerebellar development and function in mice lacking CAPS2, a protein involved in neurotrophin release. J Neurosci 27(10):2472-2482.
8. Sadakata T, et al. (2007) Autistic-like phenotypes in Cadps2-knockout mice and aberrant CADPS2 splicing in autistic patients. J Clin Invest 117(4):931-943.
9. 2+-dependent activator protein for secretion 2 (CAPS2) is involved in BDNF secretion and is associated with autism susceptibility. Cerebellum 8(3):312-322.
10. Eran A, et al. (2009) Comment on "Autistic-like phenotypes in Cadps2-knockout mice and aberrant CADPS2 splicing in autistic patients." J Clin Invest 119(4):679-680, author reply 680-671.
11. International Molecular Genetic Study of Autism Consortium (IMGSAC) (2001) Further characterization of the autism susceptibility locus AUTS1 on chromosome 7q. Hum Mol Genet 10(9):973-982.
12. 2+-dependent activator for secretion protein family. Genomics 81(3):279-291.
13. Okamoto N, Hatsukawa Y, Shimojima K, Yamamoto T (2011) Submicroscopic deletion in 7q31 encompassing CADPS2 and TSPAN12 in a child with autism spectrum disorder and PHPV. Am J Med Genet A 155A(7):1568-1573.
14. Christian SL, et al. (2008) Novel submicroscopic chromosomal abnormalities detected in autism spectrum disorder. Biol Psychiatry 63(12):1111-1117.
15. Szatmari P, et al.; Autism Genome Project Consortium (2007) Mapping autism risk loci using genetic linkage and chromosomal rearrangements. Nat Genet 39(3):319-328.
16. Voineagu I, et al. (2011) Transcriptomic analysis of autistic brain reveals convergent molecular pathology. Nature 474(7351):380-384.
17. Abrahams BS, Geschwind DH (2008) Advances in autism genetics: On the threshold of a new neurobiology. Nat Rev Genet 9(5):341-355.
18. Bangash MA, et al. (2011) Enhanced polyubiquitination of Shank3 and NMDA receptor in a mouse model of autism. Cell 145(5):758-772.
19. Durand CM, et al. (2007) Mutations in the gene encoding the synaptic scaffolding protein SHANK3 are associated with autism spectrum disorders. Nat Genet 39(1):25-27.
20. Bourgeron T (2009) A synaptic trek to autism. Curr Opin Neurobiol 19(2):231-234.
21. Peça J, et al. (2011) Shank3 mutant mice display autistic-like behaviours and striatal dysfunction. Nature 472(7344):437-442.
22. Tabuchi K, et al. (2007) A neuroligin-3 mutation implicated in autism increases inhibitory synaptic transmission in mice. Science 318(5847):71-76.
23. Berkel S, et al. (2010) Mutations in the SHANK2 synaptic scaffolding gene in autism spectrum disorder and mental retardation. Nat Genet 42(6):489-491.
24. Jamain S, et al.; Paris Autism Research International Sibpair Study (2003) Mutations of the X-linked genes encoding neuroligins NLGN3 and NLGN4 are associated with autism. Nat Genet 34(1):27-29.
25. Zoghbi HY (2003) Postnatal neurodevelopmental disorders: Meeting at the synapse? Science 302(5646):826-830.
26. Pinto D, et al. (2010) Functional impact of global rare copy number variation in autism spectrum disorders. Nature 466(7304):368-372.
27. Sadakata T, Washida M, Furuichi T (2007) Alternative splicing variations in mouse CAPS2: Differential expression and functional properties of splicing variants. BMC Neurosci 8:25.
28. 2+-dependent activator protein for secretion family proteins (CAPS2 and CAPS1) in the mouse brain. J Comp Neurol 495(6):735-753.
29. Kuczewski N, et al. (2008) Backpropagating action potentials trigger dendritic release of BDNF during spontaneous network activity. J Neurosci 28(27):7013-7023.
30. Fiorentino H, et al. (2009) GABA(B) receptor activation triggers BDNF release and promotes the maturation of GABAergic synapses. J Neurosci 29(37):11650-11661.
31. Shinoda Y, et al. (2011) Calcium-dependent activator protein for secretion 2 (CAPS2) promotes BDNF secretion and is critical for the development of GABAergic interneuron network. Proc Natl Acad Sci USA 108(1):373-378.
32. Casanova MF, Buxhoeveden D, Gomez J (2003) Disruption in the inhibitory architecture of the cell minicolumn: Implications for autisim. Neuroscientist 9(6):496-507.
33. Jones KR, Fariñas I, Backus C, Reichardt LF (1994) Targeted disruption of the BDNF gene perturbs brain and sensory neuron development but not motor neuron development. Cell 76(6):989-999.
34. Fiala JC, Spacek J, Harris KM (2002) Dendritic spine pathology: Cause or consequence of neurological disorders? Brain Res Brain Res Rev 39(1):29-54.
35. Alonso M, Medina JH, Pozzo-Miller L (2004) ERK1/2 activation is necessary for BDNF to increase dendritic spine density in hippocampal CA1 pyramidal neurons. Learn Mem 11(2):172-178.
36. World Health Organization (1992) The ICD-10 Classification of Mental and Behavioural Disorders: Clinical Descriptions and Diagnostic Guidelines (WHO, Geneva) pp XII, 362.
37. American Psychiatric Association Task Force on DSM-IV (1994) Diagnostic and Statistical Manual of Mental Disorders: DSM-IV (American Psychiatric Association, Washington, DC) 4th Ed pp XXVII, 886.
38. Nakatani J, et al. (2009) Abnormal behavior in a chromosome-engineered mouse model for human 15q11-13 duplication seen in autism. Cell 137(7):1235-1246.
39. Filipek PA, et al. (2000) Practice parameter: Screening and diagnosis of autism: report of the Quality Standards Subcommittee of the American Academy of Neurology and the Child Neurology Society. Neurology 55(4):468-479.
40. Richdale AL, Prior MR (1995) The sleep/wake rhythm in children with autism. Eur Child Adolesc Psychiatry 4(3):175-186.
41. Courchesne E, Pierce K (2005) Why the frontal cortex in autism might be talking only to itself: Local over-connectivity but long-distance disconnection. Curr Opin Neurobiol 15(2):225-230.
42. Zheng K, et al. (2011) TrkB signaling in parvalbumin-positive interneurons is critical for gamma-band network synchronization in hippocampus. Proc Natl Acad Sci USA 108(41):17201-17206.
43. Montgomery KC (1955) The relation between fear induced by novel stimulation and exploratory behavior. J Comp Physiol Psychol 48(4):254-260.
44. Chang Q, Khare G, Dani V, Nelson S, Jaenisch R (2006) The disease progression of Mecp2 mutant mice is affected by the level of BDNF expression. Neuron 49(3):341-348.
45. Chen WG, et al. (2003) Derepression of BDNF transcription involves calcium-dependent phosphorylation of MeCP2. Science 302(5646):885-889.