DISC1 regulates synaptic vesicle transport via a lithium-sensitive pathway

Neuroscience Research

Volumn 71, Issue 1, 2011, Pages 71-77

  Flores, Rafael ^a   Hirota, Yuki ^a   Armstrong, Brian ^a   Sawa, Akira ^b,c   Tomoda, Toshifumi ^a  

^a CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Bipolar disorder; DISC1; FEZ1; Lithium; Motor cargo assembly; Vesicle transport

Indexed keywords

ADAPTOR PROTEIN; DISRUPTED IN SCHIZOPHRENIA 1 PROTEIN; FEZ1 PROTEIN; GLYCOGEN SYNTHASE KINASE 3; LITHIUM; SYNAPTOBREVIN 2; SYNAPTOTAGMIN I; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN CORTEX; CELL TRANSPORT; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; MICROTUBULE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; SYNAPSE VESICLE;

ANIMALS; AXONAL TRANSPORT; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; COS CELLS; FEMALE; LITHIUM COMPOUNDS; MICE; MICE, INBRED C57BL; MICROTUBULES; NERVE TISSUE PROTEINS; NEURONS; ORGANELLES; PREGNANCY; PRIMARY CELL CULTURE; SIGNAL TRANSDUCTION; SYNAPTIC VESICLES;

EID: 79960916466     PISSN: 01680102     EISSN: 18728111     Source Type: Journal    
DOI: 10.1016/j.neures.2011.05.014     Document Type: Article

References (39)

1. Atkin T.A., Macaskill A.F., Brandon N.J., Kittler J.T. The DISC1Cys607Phe polymorphism affects mitochondrial transport in neurons. Mol. Psychiatry 2011, 16:121.
2. Beaulieu J.M., Marion S., Rodriguiz R.M., Medvedev I.O., Sotnikova T.D., Ghisi V., Wetsel W.C., Lefkowitz R.J., Gainetdinov R.R., Caron M.G. A beta-arrestin 2 signaling complex mediates lithium action on behavior. Cell 2008, 132:125-136.
3. Berridge M.J., Downes C.P., Hanley M.R. Neural and developmental actions of lithium: a unifying hypothesis. Cell 1989, 59:411-419.
4. Blasius T.L., Cai D., Jih G.T., Toret C.P., Verhey K.J. Two binding partners cooperate to activate the molecular motor Kinesin-1. J. Cell Biol. 2007, 176:11-17.
5. Carter C.J. Multiple genes and factors associated with bipolar disorder converge on growth factor and stress activated kinase pathways controlling translation initiation: implications for oligodendrocyte viability. Neurochem. Int. 2007, 50:461-490.
6. Chuang D.M. The antiapoptotic actions of mood stabilizers: molecular mechanisms and therapeutic potentials. Ann. N. Y. Acad. Sci. 2005, 1053:195-204.
7. Colin E., Zala D., Liot G., Rangone H., Borrell-Pages M., Li X.J., Saudou F., Humbert S. Huntingtin phosphorylation acts as a molecular switch for anterograde/retrograde transport in neurons. EMBO J. 2008, 27:2124-2134.
8. Duan X., Chang J.H., Ge S., Faulkner R.L., Kim J.Y., Kitabatake Y., Liu X.B., Yang C.H., Jordan J.D., Ma D.K., et al. Disrupted-In-Schizophrenia 1 regulates integration of newly generated neurons in the adult brain. Cell 2007, 130:1146-1158.
9. Fatemi S.H., Reutiman T.J., Folsom T.D. The role of lithium in modulation of brain genes: relevance for aetiology and treatment of bipolar disorder. Biochem. Soc. Trans. 2009, 37:1090-1095.
10. Gindhart J.G., Chen J., Faulkner M., Gandhi R., Doerner K., Wisniewski T., Nandlestadt A. The kinesin-associated protein UNC-76 is required for axonal transport in the Drosophila nervous system. Mol. Biol. Cell 2003, 14:3356-3365.
11. Gong X., Bacchelli E., Blasi F., Toma C., Betancur C., Chaste P., Delorme R., Durand C.M., Fauchereau F., Botros H.G., et al. Analysis of X chromosome inactivation in autism spectrum disorders. Am. J. Med. Genet. B: Neuropsychiatr. Genet. 2008, 147B:830-835.
12. Guzik B.W., Goldstein L.S. Microtubule-dependent transport in neurons: steps towards an understanding of regulation, function and dysfunction. Curr. Opin. Cell Biol. 2004, 16:443-450.
13. Hashimoto R., Numakawa T., Ohnishi T., Kumamaru E., Yagasaki Y., Ishimoto T., Mori T., Nemoto K., Adachi N., Izumi A., et al. Impact of the DISC1 Ser704Cys polymorphism on risk for major depression, brain morphology and ERK signaling. Hum. Mol. Genet. 2006, 15:3024-3033.
14. Hayashi-Takagi A., Takaki M., Graziane N., Seshadri S., Murdoch H., Dunlop A.J., Makino Y., Seshadri A.J., Ishizuka K., Srivastava D.P., et al. Disrupted-in-Schizophrenia 1 (DISC1) regulates spines of the glutamate synapse via Rac1. Nat. Neurosci. 2010, 13:327-332.
15. Ishizuka K., Kamiya A., Oh E.C., Kanki H., Seshadri S., Robinson J.F., Murdoch H., Dunlop A.J., Kubo K.I., Furukori K., et al. DISC1-dependent switch from progenitor proliferation to migration in the developing cortex. Nature 2011, 473:92-96.
16. Kamiya A., Kubo K., Tomoda T., Takaki M., Youn R., Ozeki Y., Sawamura N., Park U., Kudo C., Okawa M., et al. A schizophrenia-associated mutation of DISC1 perturbs cerebral cortex development. Nat. Cell Biol. 2005, 7:1167-1178.
17. Kim J.Y., Duan X., Liu C.Y., Jang M.H., Guo J.U., Pow-anpongkul N., Kang E., Song H., Ming G.L. DISC1 regulates new neuron development in the adult brain via modulation of AKT-mTOR signaling through KIAA1212. Neuron 2009, 63:761-773.
18. Klein P.S., Melton D.A. A molecular mechanism for the effect of lithium on development. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:8455-8459.
19. Liou Y.J., Wang Y.C., Chen J.Y., Chen M.L., Chen T.T., Bai Y.M., Lin C.C., Liao D.L., Lai I.C. The coding-synonymous polymorphism rs1045280 (Ser280Ser) in beta-arrestin 2 (ARRB2) gene is associated with tardive dyskinesia in Chinese patients with schizophrenia. Eur. J. Neurol. 2008, 15:1406-1408.
20. Lohoff F.W., Weller A.E., Bloch P.J., Nall A.H., Ferraro T.N., Berrettini W.H. Association between polymorphisms in the vesicle-associated membrane protein-associated protein A (VAPA) gene on chromosome 18p and bipolar disorder. J. Neural Transm. 2008, 115:1339-1345.
21. Macgregor S., Visscher P.M., Knott S.A., Thomson P., Porteous D.J., Millar J.K., Devon R.S., Blackwood D., Muir W.J. A genome scan and follow-up study identify a bipolar disorder susceptibility locus on chromosome 1q42. Mol. Psychiatry 2004, 9:1083-1090.
22. Maeda K., Nwulia E., Chang J., Balkissoon R., Ishizuka K., Chen H., Zandi P., McInnis M.G., Sawa A. Differential expression of disrupted-in-schizophrenia (DISC1) in bipolar disorder. Biol. Psychiatry 2006, 60:929-935.
23. Mao Y., Ge X., Frank C.L., Madison J.M., Koehler A.N., Doud M.K., Tassa C., Berry E.M., Soda T., Singh K.K., et al. Disrupted in schizophrenia 1 regulates neuronal progenitor proliferation via modulation of GSK3beta/beta-catenin signaling. Cell 2009, 136:1017-1031.
24. McMahon F.J., Buervenich S., Charney D., Lipsky R., Rush A.J., Wilson A.F., Sorant A.J., Papanicolaou G.J., Laje G., Fava M., et al. Variation in the gene encoding the serotonin 2A receptor is associated with outcome of antidepressant treatment. Am. J. Hum. Genet. 2006, 78:804-814.
25. Michell R.H., Heath V.L., Lemmon M.A., Dove S.K. Phosphatidylinositol 3,5-bisphosphate: metabolism and cellular functions. Trends Biochem. Sci. 2006, 31:52-63.
26. Millar J.K., Pickard B.S., Mackie S., James R., Christie S., Buchanan S.R., Malloy M.P., Chubb J.E., Huston E., Baillie G.S., et al. DISC1 and PDE4B are interacting genetic factors in schizophrenia that regulate cAMP signaling. Science 2005, 310:1187-1191.
27. Millar J.K., Wilson-Annan J.C., Anderson S., Christie S., Taylor M.S., Semple C.A., Devon R.S., St Clair D.M., Muir W.J., Blackwood D.H., et al. Disruption of two novel genes by a translocation co-segregating with schizophrenia. Hum. Mol. Genet. 2000, 9:1415-1423.
28. Miyoshi K., Honda A., Baba K., Taniguchi M., Oono K., Fujita T., Kuroda S., Katayama T., Tohyama M. Disrupted-In-Schizophrenia 1, a candidate gene for schizophrenia, participates in neurite outgrowth. Mol. Psychiatry 2003, 8:685-694.
29. Morfini G., Szebenyi G., Elluru R., Ratner N., Brady S.T. Glycogen synthase kinase 3 phosphorylates kinesin light chains and negatively regulates kinesin-based motility. EMBO J. 2002, 21:281-293.
30. Ozeki Y., Tomoda T., Kleiderlein J., Kamiya A., Bord L., Fujii K., Okawa M., Yamada N., Hatten M.E., Snyder S.H., et al. Disrupted-in-Schizophrenia-1 (DISC-1): mutant truncation prevents binding to NudE-like (NUDEL) and inhibits neurite outgrowth. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:289-294.
31. Perlis R.H., Purcell S., Fagerness J., Kirby A., Petryshen T.L., Fan J., Sklar P. Family-based association study of lithium-related and other candidate genes in bipolar disorder. Arch. Gen. Psychiatry 2008, 65:53-61.
32. Prosser D.C., Tran D., Gougeon P.Y., Verly C., Ngsee J.K. FFAT rescues VAPA-mediated inhibition of ER-to-Golgi transport and VAPB-mediated ER aggregation. J. Cell Sci. 2008, 121:3052-3061.
33. Skehel P.A., Martin K.C., Kandel E.R., Bartsch D. A VAMP-binding protein from Aplysia required for neurotransmitter release. Science 1995, 269:1580-1583.
34. Taya S., Shinoda T., Tsuboi D., Asaki J., Nagai K., Hikita T., Kuroda S., Kuroda K., Shimizu M., Hirotsune S., et al. DISC1 regulates the transport of the NUDEL/LIS1/14-3-3epsilon complex through kinesin-1. J. Neurosci. 2007, 27:15-26.
35. Toda H., Mochizuki H., Flores R., Josowitz R., Krasieva T.B., Lamorte V.J., Suzuki E., Gindhart J.G., Furukubo-Tokunaga K., Tomoda T. UNC-51/ATG1 kinase regulates axonal transport by mediating motor-cargo assembly. Genes Dev. 2008, 22:3292-3307.
36. Tomoda T., Kim J.H., Zhan C., Hatten M.E. Role of Unc51.1 and its binding partners in CNS axon outgrowth. Genes Dev. 2004, 18:541-558.
37. Verhey K.J., Meyer D., Deehan R., Blenis J., Schnapp B.J., Rapoport T.A., Margolis B. Cargo of kinesin identified as JIP scaffolding proteins and associated signaling molecules. J. Cell Biol. 2001, 152:959-970.
38. Weir M.L., Klip A., Trimble W.S. Identification of a human homologue of the vesicle-associated membrane protein (VAMP)-associated protein of 33kDa (VAP-33): a broadly expressed protein that binds to VAMP. Biochem. J. 1998, 333(Pt 2):247-251.
39. Zala D., Colin E., Rangone H., Liot G., Humbert S., Saudou F. Phosphorylation of mutant huntingtin at S421 restores anterograde and retrograde transport in neurons. Hum. Mol. Genet. 2008, 17:3837-3846.