Rab3 interacting molecule 3 mutations associated with autism alter regulation of voltage-dependent Ca2+ channels

Cell Calcium

Volumn 58, Issue 3, 2015, Pages 296-306

  Takada, Yoshinori ^a   Hirano, Mitsuru ^a   Kiyonaka, Shigeki ^a   Ueda, Yoshifumi ^a   Yamaguchi, Kazuma ^a   Nakahara, Keiko ^a   Mori, Masayuki X ^a   Mori, Yasuo ^a  

^a KYOTO UNIVERSITY   (Japan)

Author keywords

Autism; Calcium; Neurotransmitter release; Rab3 interacting molecule; Voltage dependent calcium channel

Indexed keywords

RAB PROTEIN; VOLTAGE GATED CALCIUM CHANNEL; CALCIUM CHANNEL; RABIN3 PROTEIN, RAT; SIGNAL PEPTIDE;

ACETYLCHOLINE RELEASE; ANIMAL CELL; ARTICLE; AUTISM; CALCIUM SIGNALING; CONTROLLED STUDY; GENE; GENE MUTATION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MEMBRANE DEPOLARIZATION; MOLECULAR CLONING; MYELINATION; NEUROTRANSMISSION; NEUROTRANSMITTER RELEASE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; RAT; RIM3 GENE; ANIMAL; GENETICS; HEK293 CELL LINE; METABOLISM; MOUSE; MUTATION; NERVE CELL; PC12 CELL LINE; PHYSIOLOGY;

RATTUS;

ANIMALS; AUTISTIC DISORDER; CALCIUM CHANNELS; CALCIUM SIGNALING; HEK293 CELLS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MUTATION; NEURONS; PC12 CELLS; RATS;

EID: 84938738094     PISSN: 01434160     EISSN: 15321991     Source Type: Journal    
DOI: 10.1016/j.ceca.2015.06.007     Document Type: Article

References (65)

1. Miller R.J. Calcium signaling in neurons. Trends Neuorsci. 1988, 11:415-419.
2. Berridge M.J., Lipp P., Bootman M.D. The versatility and universality of calcium signaling. Nat. Rev. Mol. Cell Biol. 2000, 1:11-21.
3. Autism and Developmental Disabilities Monitoring, Network Surveillance Year 2008 Principal Investigators, Prevalence of autism spectrum disorders-autism and developmental disabilities monitoring network, 14 sites, United States, 2008, MMWR Surveill Summ. 61 (2012) 1-19.
4. Johnson M.H. Functional brain development in humans. Nat. Rev. Neurosci. 2001, 2:475-483.
5. Abrahams B.S., Geschwind D.H. Advances in autism genetics: on the threshold of a new neurobiology. Nat. Rev. Genet. 2008, 9:341-355.
6. Jamain S., Quach H., Betancur C., et al. Mutations of the X-linked genes encoding neuroligins NLGN3 and NLGN4 are associated with autism. Nat. Genet. 2003, 34:27-29.
7. Durand C.M., Betancur C., Boeckers T.M., et al. Mutations in the gene encoding the synaptic scaffolding protein SHANK3 are associated with autism spectrum disorders. Nat. Genet. 2007, 39:25-27.
8. Malhotra D., Sebat J. CNVs: harbingers of a rare variant revolution in psychiatric genetics. Cell 2012, 148:1223-1241.
9. Südhof T.C. The presynaptic active zone. Neuron 2012, 75:11-25.
10. Wang Y., Südhof T.C. Genomic definition of RIM proteins: evolutionary amplification of a family of synaptic regulatory proteins. Genomics 2003, 81:126-137.
11. Koushika S.P., Richmond J.E., Hadwiger G., Weimer R.M., Jorgensen E.M., Nonet M.L. A post docking role for active zone protein Rim. Nat. Neurosci. 2001, 4:997-1005.
12. Schoch S., Castillo P.E., Jo T., et al. RIM1α forms a protein scaffold for regulating neurotransmitter release at the active zone. Nature 2002, 415:321-326.
13. Gracheva E.O., Hadwiger G., Nonet M.L., Richmond J.E. Direct interactions between C. elegans RAB-3 and Rime provide a mechanism to target vesicles to the presynaptic density. Neurosci. Lett. 2008, 444:137-142.
14. 2+ channels to presynaptic active zone via a direct PDZ-domain interaction. Cell 2011, 144:282-295.
15. Deng L., Kaeser P.S., Xu W., Südhof T.C. RIM proteins activate vesicle priming by reversing autoinhibitory homodimerization of Munc13. Neuron 2011, 69:317-331.
16. 2+ channel density and vesicle docking at the presynaptic active zone. Neuron 2011, 69:304-316.
17. Castillo P.E., Schoch S., Schmitz F., Südhof T.C., Malenka R.C. RIM1alpha is required for presynaptic long-term potentiation. Nature 2002, 415:327-330.
18. 2+ channels. Nat. Neurosci. 2007, 10:691-701.
19. 2+ channels in insulin release. J. Biol. Chem. 2011, 286:15757-15765.
20. 2+ channels. J. Biol. Chem. 2010, 285:21750-21767.
21. Alvarez-Baron E., Michel K., Mittelstaedt T., et al. RIM3γ and RIM4γ are key regulators of neuronal arborization. J. Neurosci. 2013, 33:824-839.
22. Liang F., Zhang B., Tang J., et al. RIM3γ is a postsynaptic protein in the rat central nervous system. J. Comp. Neurol. 2007, 503:501-510.
23. Kumar R.A., Sudi J., Babatz T.D., et al. A de novo 1p34.2 microdeletion identifies the synaptic vesicle gene RIMS3 as a novel candidate for autism. J. Med. Genet. 2010, 47:81-90.
24. Guex N., Peitsch M.C. SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 1997, 18:2714-2723.
25. Arnold K., Bordoli L., Kopp J., Schwede T. The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 2006, 22:195-201.
26. Bordoli L., Kiefer F., Arnold K., Benkert P., Battey J., Schwede T. Protein structure homology modeling using SWISS-MODEL workspace. Nat. Protoc. 2009, 4:1-13.
27. Guan R., Dai H., Tomchick D.R., et al. Crystal structure of the RIM1alpha C2B domain at 1.7 A resolution. Biochemistry 2007, 46:8988-8998.
28. Mc Nicholas S., Potterton E., Wilson K.S., Noble M.E. Presenting your structures: the CCP4mg molecular-graphics software. Acta Crystallogr. D Biol. Crystallogr. 2011, 67:386-394.
29. Niidome T., Teramoto T., Murata Y., et al. Stable expression of the neuronal BI (class A) calcium channel in baby hamster kidney cells. Biochem. Biophys. Res. Commun. 1994, 203:1821-1827.
30. Kang M.G., Chen C.C., Wakamori M., Hara Y., Mori Y., Campbell K.P. A functional AMPA receptor-calcium channel complex in the postsynaptic membrane. Proc. Natl. Acad. Sci. USA 2006, 103:5561-5566.
31. Wakamori M., Yamazaki K., Matsunodaira H., et al. Single tottering mutations responsible for the neuropathic phenotype of the P-type calcium channel. J. Biol. Chem. 1998, 273:34857-34867.
32. Itakura M., Misawa H., Sekiguchi M., Takahashi S., Takahashi M. Transfection analysis of functional roles of complexin I and II in the exocytosis of two different types of secretory vesicles. Biochem. Biophys. Res. Commun. 1999, 265:691-696.
33. 2-terminal kinase activity and DNA fragmentation in a calcium-dependent manner in rat myoblast cell line H9c2. Biochem. Biophys. Res. Commun. 1999, 262:350-354.
34. 2+ channels. Trends Pharmacol. Sci. 1991, 12:349-354.
35. Mori Y., Friedrich T., Kim M.S., et al. Primary structure and functional expression from complementary DNA of a brain calcium channel. Nature 1991, 350:398-402.
36. Zoghbi H.Y. Postnatal neurodevelopmental disorders: Meeting at the synapse?. Science 2003, 302:826-830.
37. Sheng Z.H., Rettig J., Takahashi M., Catterall W.A. Identification of a syntaxin-binding site on N-type calcium channels. Neuron 1994, 13:1303-1313.
38. Bezprozvanny I., Scheller R.H., Tsien R.W. Functional impact of syntaxin on gating of N-type and Q-type calcium channels. Nature 1995, 378:623-626.
39. 2+ channels. EMBO J. 1996, 15:4100-4110.
40. 2+ channels by SNAP-25, syntaxin and synaptotagmin. Nat. Neurosci. 1999, 2:939-941.
41. Chen J., Billings S.E., Nishimune H. Calcium channels link the muscle-derived synapse organizer laminin β2 to Bassoon and CAST/Erc2 to organize presynaptic active zones. J. Neurosci. 2011, 31:512-525.
42. 2+ channel subunit β4 interact and colocalize at cerebellar synapses. Neuroreport 2012, 23:49-54.
43. 2+ channel. J. Biochem. 2012, 152:149-159.
44. 2+ channels, SNAP-25, and synaptotagmin. J. Biol. Chem. 2001, 276:32756-32762.
45. Hussman J.P. Suppressed GABAergic inhibition as a common factor in suspected etiologies of autism. J. Autism Dev. Disord. 2001, 31:247-248.
46. Rubenstein J.L., Merzenich M.M. Model of autism: increased ration of excitation/inhibition in key neural systems. Genes Brain Behav. 2003, 2:255-267.
47. Meir A., Ginsburg S., Butkevich A., et al. Ion channels in presynaptic nerve terminals and control of transmitter release. Physiol. Rev. 1999, 79:1019-1088.
48. Poncer J.C., Mc Kinney R.A., Gähwiler B.H., Thompson S.M. Either N- or P-type calcium channels mediate GABA release at distinct hippocampal inhibitory synapses. Neuron 1997, 18:463-472.
49. Stephens G.J., Morris N.P., Fyffe R.E., Robertson B. The Cav2.1/alpha1A (P/Q-type) voltage-dependent calcium channel mediates inhibitory neurotransmission onto mouse cerebellar Purkinje cells. Eur. J. Neurosci. 2001, 13:1902-1912.
50. 2+ transients. Nature 1995, 375:784-787.
51. Solem M., Mc Mahon T., Messing R.O. Depolarization-induced neurite outgrowth in PC12 cells requires permissive, low level NGF receptor stimulation and activation of calcium/calmodulin-dependent protein kinase. J. Neurosci. 1995, 15:5966-5975.
52. Boeckers T.M., Bockmann J., Kreutz M.R., Gundelfinger E.D. ProSAP/Shank proteins-a family of higher order organizing molecules of the postsynaptic density with an emerging role in human neurological disease. J. Neurochem. 2002, 81:903-910.
53. Arons M.H., Thynne C.J., Grabrucker A.M., et al. Autism-associated mutations in ProSAP2/Shank3 impair synaptic transmission and Neurexin-Neuroligin-mediated transsynaptic signaling. J. Neurosci. 2012, 32:14966-14978.
54. 2+ signaling. Curr. Opin. Neurobiol. 2007, 17:112-119.
55. Aamodt S.M., Constantine-Paton M. The role of neural activity in synaptic development and its implications for adult brain function. Adv. Neurol. 1999, 79:133-144.
56. Cline H.T. Dendritic arbor development and synaptogenesis. Curr. Opin. Neurobiol. 2001, 11:118-126.
57. 2+ spikes specify transmitter choice. Trends Neurosci. 2004, 27:415-421.
58. DiCicco-Bloom E., Lord C., Zwaigenbaum L., et al. The developmental neurobiology of autism spectrum disorder. J. Neurosci. 2006, 26:6897-6906.
59. Splawski I., Timothy K.W., Sharpe L.M., et al. Cav1.2 calcium channel dysfunction causes a multisystem disorder including arrhythmia and autism. Cell 2004, 119:19-31.
60. Splawski I., Yoo D.S., Stotz S.C., Cherry A., Clapham D.E., Keating M.T. CACNA1H mutations in autism spectrum disorders. J. Biol. Chem. 2006, 281:22085-22091.
61. Hemara-Wahanui A., Berjukow S., Hope C.I., et al. A CACNA1F mutation identified in an X-linked retinal disorder shifts the voltage dependence of Cav1.4 channel activation. Proc. Natl. Acad. Sci. USA 2005, 102:7553-7558.
62. Laumonnier F., Roger S., Guerin P., et al. Association of a functional deficit of the BKCa channel, a synaptic regulator of neuronal excitability, with autism and mental retardation. Am. J. Psychiatry 2006, 163:1622-1629.
63. Weidenhofer J., Bowden N.A., Scott R.J., Tooney P.A. Altered gene expression in the amygdala in schizophrenia: up-regulation of genes located in the cytomatrix active zone. Mol. Cell. Neurosci. 2006, 31:243-250.
64. Weidenhofer J., Scott R.J., Tooney P.A. Investigation of the expression of genes affecting cytomatrix active zone function in the amygdala in schizophrenia: effects of antipsychotic drugs. J. Psychiatr. Res. 2009, 43:282-290.
65. Guerini F.R., Bolognesi E., Chiappedi M., et al. SNAP-25 single nucleotide polymorphisms are associated with hyperactivity in autism spectrum disorders. Pharmacol. Res. 2011, 64:283-288.