Proteomic analysis reveals novel binding partners of dysbindin, a schizophrenia-related protein

Journal of Neurochemistry

Volumn 110, Issue 5, 2009, Pages 1567-1574

  Hikita, Takao ^a,b   Taya, Shinichiro ^a,b   Fujino, Yasutaka ^a,b   Taneichi Kuroda, Setsuko ^a   Ohta, Kanae ^a   Tsuboi, Daisuke ^a,b   Shinoda, Tomoyasu ^a   Kuroda, Keisuke ^a,b   Funahashi, Yusuke ^a,b   Uraguchi Asaki, Junko ^a,b   Hashimoto, Ryota ^b,c   Kaibuchi, Kozo ^a,b  

^a NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Dysbindin; Munc18 1; Proteomics; Schizophrenia; Susceptibility gene

Indexed keywords

AMMONIUM SULFATE; DYSBINDIN; DYSTROBREVIN; MUNC18 1 PROTEIN; MUNC18 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING ASSAY; BRAIN NERVE CELL; CELL LYSATE; COLUMN CHROMATOGRAPHY; CONTROLLED STUDY; EXOCYTOSIS; FUNCTIONAL PROTEOMICS; GENETIC SUSCEPTIBILITY; HIPPOCAMPUS; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; IN VITRO STUDY; LIQUID CHROMATOGRAPHY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NERVE CELL CULTURE; NONHUMAN; PRECIPITATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RAT; SCHIZOPHRENIA; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION; TANDEM MASS SPECTROMETRY;

ANIMALS; CARRIER PROTEINS; EXOCYTOSIS; HIPPOCAMPUS; HUMANS; MICE; MICE, INBRED C57BL; MUNC18 PROTEINS; PROTEIN BINDING; PROTEOMICS; RATS; SCHIZOPHRENIA;

RATTUS;

EID: 68949221092     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2009.06257.x     Document Type: Article

References (50)

1. Benson M. A., Newey S. E., Martin-Rendon E., Hawkes R. Blake D. J. (2001) Dysbindin, a novel coiled-coil-containing protein that interacts with the dystrobrevins in muscle and brain. J. Biol. Chem. 276, 24232 24241.
2. Bilder R. M., Volavka J., Czobor P. et al. (2002) Neurocognitive correlates of the COMT Val(158)Met polymorphism in chronic schizophrenia. Biol. Psychiatry 52, 701 707.
3. Blackwood D. H., Fordyce A., Walker M. T., St Clair D. M., Porteous D. J. Muir W. J. (2001) Schizophrenia and affective disorders-cosegregation with a translocation at chromosome 1q42 that directly disrupts brain-expressed genes: clinical and P300 findings in a family. Am. J. Hum. Genet. 69, 428 433.
4. Cardno A. G. Gottesman II (2000) Twin studies of schizophrenia: from bow-and-arrow concordances to star wars Mx and functional genomics. Am. J. Med. Genet. 97, 12 17.
5. Chen X. W., Feng Y. Q., Hao C. J. et al. (2008) DTNBP1, a schizophrenia susceptibility gene, affects kinetics of transmitter release. J. Cell Biol. 181, 791 801.
6. Chumakov I., Blumenfeld M., Guerassimenko O. et al. (2002) Genetic and physiological data implicating the new human gene G72 and the gene for D-amino acid oxidase in schizophrenia. Proc. Natl. Acad. Sci. USA 99, 13675 13680.
7. Cohen P. Frame S. (2001) The renaissance of GSK3. Nat. Rev. Mol. Cell Biol. 2, 769 776.
8. Craddock N., O'Donovan M. C. Owen M. J. (2005) The genetics of schizophrenia and bipolar disorder: dissecting psychosis. J. Med. Genet. 42, 193 204.
9. Dell'Angelica E. C. (2004) The building BLOC(k)s of lysosomes and related organelles. Curr. Opin. Cell Biol. 16, 458 464.
10. Di Pietro S. M., Falcon-Perez J. M., Tenza D., Setty S. R., Marks M. S., Raposo G. Dell'Angelica E. C. (2006) BLOC-1 interacts with BLOC-2 and the AP-3 complex to facilitate protein trafficking on endosomes. Mol. Biol. Cell 17, 4027 4038.
11. Egan M. F., Goldberg T. E., Kolachana B. S., Callicott J. H., Mazzanti C. M., Straub R. E., Goldman D. Weinberger D. R. (2001) Effect of COMT Val108/158 Met genotype on frontal lobe function and risk for schizophrenia. Proc. Natl. Acad. Sci. USA 98, 6917 6922.
12. Forgac M. (2007) Vacuolar ATPases: rotary proton pumps in physiology and pathophysiology. Nat. Rev. Mol. Cell Biol. 8, 917 929.
13. Guo A. Y., Sun J., Riley B. P., Thiselton D. L., Kendler K. S. Zhao Z. (2009) The dystrobrevin-binding protein 1 gene: features and networks. Mol. Psychiatry 14, 18 29.
14. Harrison P. J. Weinberger D. R. (2005) Schizophrenia genes, gene expression, and neuropathology: on the matter of their convergence. Mol. Psychiatry 10, 40 68.
15. Hata Y., Slaughter C. A. Südhof T. C. (1993) Synaptic vesicle fusion complex contains unc-18 homologue bound to syntaxin. Nature 366, 347 351.
16. Hattori S., Murotani T., Matsuzaki S. et al. (2008) Behavioral abnormalities and dopamine reductions in sdy mutant mice with a deletion in Dtnbp1, a susceptibility gene for schizophrenia. Biochem. Biophys. Res. Commun. 373, 298 302.
17. Inagaki N., Chihara K., Arimura N., Menager C., Kawano Y., Matsuo N., Nishimura T., Amano M. Kaibuchi K. (2001) CRMP-2 induces axons in cultured hippocampal neurons. Nat. Neurosci. 4, 781 782.
18. Kanaho Y., Kobayashi-Nakano A. Yokozeki T. (2007) The phosphoinositide kinase PIP5K that produces the versatile signaling phospholipid PI4,5P(2). Biol. Pharm. Bull. 30, 1605 1609.
19. Kubota K., Kumamoto N., Matsuzaki S. et al. (2009) Dysbindin engages in c-Jun N-terminal kinase activity and cytoskeletal organization. Biochem. Biophys. Res. Commun. 379, 191 195.
20. Kumamoto N., Matsuzaki S., Inoue K., Hattori T., Shimizu S., Hashimoto R., Yamatodani A., Katayama T. Tohyama M. (2006) Hyperactivation of midbrain dopaminergic system in schizophrenia could be attributed to the down-regulation of dysbindin. Biochem. Biophys. Res. Commun. 345, 904 909.
21. Li W., Zhang Q., Oiso N. et al. (2003) Hermansky-Pudlak syndrome type 7 (HPS-7) results from mutant dysbindin, a member of the biogenesis of lysosome-related organelles complex 1 (BLOC-1). Nat. Genet. 35, 84 89.
22. Loijens J. C. Anderson R. A. (1996) Type I phosphatidylinositol-4- phosphate 5-kinases are distinct members of this novel lipid kinase family. J. Biol. Chem. 271, 32937 32943.
23. Millar J. K., Wilson-Annan J. C., Anderson S. et al. (2000) Disruption of two novel genes by a translocation co-segregating with schizophrenia. Hum. Mol. Genet. 9, 1415 1423.
24. Morris D. W., Murphy K., Kenny N. et al. (2008) Dysbindin (DTNBP1) and the biogenesis of lysosome-related organelles complex 1 (BLOC-1): main and epistatic gene effects are potential contributors to schizophrenia susceptibility. Biol. Psychiatry 63, 24 31.
25. Murotani T., Ishizuka T., Hattori S., Hashimoto R., Matsuzaki S. Yamatodani A. (2007) High dopamine turnover in the brains of Sandy mice. Neurosci. Lett. 421, 47 51.
26. Nave K. A. Trapp B. D. (2008) Axon-glial signaling and the glial support of axon function. Annu. Rev. Neurosci. 31, 535 561.
27. Newell-Litwa K., Seong E., Burmeister M. Faundez V. (2007) Neuronal and non-neuronal functions of the AP-3 sorting machinery. J. Cell Sci. 120, 531 541.
28. Numakawa T., Yagasaki Y., Ishimoto T. et al. (2004) Evidence of novel neuronal functions of dysbindin, a susceptibility gene for schizophrenia. Hum. Mol. Genet. 13, 2699 2708.
29. Odorizzi G., Cowles C. R. Emr S. D. (1998) The AP-3 complex: a coat of many colours. Trends Cell Biol. 8, 282 288.
30. Robinson M. S. Bonifacino J. S. (2001) Adaptor-related proteins. Curr. Opin. Cell Biol. 13, 444 453.
31. Rodriguez-Fernandez I. A. Dell'angelica E. C. (2009) A data-mining approach to rank candidate protein-binding partners-The case of biogenesis of lysosome-related organelles complex-1 (BLOC-1). J. Inherit. Metab. Dis. 32, 190 203.
32. Saitsu H., Kato M., Mizuguchi T. et al. (2008) De novo mutations in the gene encoding STXBP1 (MUNC18-1) cause early infantile epileptic encephalopathy. Nat. Genet. 40, 782 788.
33. Salazar G., Craige B., Wainer B. H., Guo J., De Camilli P. Faundez V. (2005) Phosphatidylinositol-4-kinase type II alpha is a component of adaptor protein-3-derived vesicles. Mol. Biol. Cell 16, 3692 3704.
34. Salazar G., Craige B., Styers M. L. et al. (2006) BLOC-1 complex deficiency alters the targeting of adaptor protein complex-3 cargoes. Mol. Biol. Cell 17, 4014 4026.
35. Setty S. R., Tenza D., Truschel S. T. et al. (2007) BLOC-1 is required for cargo-specific sorting from vacuolar early endosomes toward lysosome-related organelles. Mol. Biol. Cell 18, 768 \780.
36. Shen J., Tareste D. C., Paumet F., Rothman J. E. Melia T. J. (2007) Selective activation of cognate SNAREpins by Sec1/Munc18 proteins. Cell 128, 183 195.
37. Shifman S., Bronstein M., Sternfeld M. et al. (2002) A highly significant association between a COMT haplotype and schizophrenia. Am. J. Hum. Genet. 71, 1296 1302.
38. Stefansson H., Sigurdsson E., Steinthorsdottir V. et al. (2002) Neuregulin 1 and susceptibility to schizophrenia. Am. J. Hum. Genet. 71, 877 892.
39. Straub R. E., MacLean C. J., O'Neill F. A. et al. (1995) A potential vulnerability locus for schizophrenia on chromosome 6p24-22: evidence for genetic heterogeneity. Nat. Genet. 11, 287 293.
40. Südhof T. C. (2004) The synaptic vesicle cycle. Annu. Rev. Neurosci. 27, 509 547.
41. Takao K., Toyama K., Nakanishi K., Hattori S., Takamura H., Takeda M., Miyakawa T. Hashimoto R. (2008) Impaired long-term memory retention and working memory in sdy mutant mice with a deletion in Dtnbp1, a susceptibility gene for schizophrenia. Mol. Brain 1, 11.
42. Talbot K., Eidem W. L., Tinsley C. L. et al. (2004) Dysbindin-1 is reduced in intrinsic, glutamatergic terminals of the hippocampal formation in schizophrenia. J. Clin. Invest. 113, 1353 1363.
43. Talbot K., Cho D. S., Ong W. Y. et al. (2006) Dysbindin-1 is a synaptic and microtubular protein that binds brain snapin. Hum. Mol. Genet. 15, 3041 3054.
44. Taneichi-Kuroda S., Taya S., Hikita T., Fujino Y. Kaibuchi K. (2009) Direct interaction of Dysbindin with the AP-3 complex via its μ subunit. Neurochem. Int. 54, 431 438.
45. Taya S., Shinoda T., Tsuboi D. et al. (2007) DISC1 regulates the transport of the NUDEL/LIS1/14-3-3epsilon complex through kinesin-1. J. Neurosci. 27, 15 26.
46. Toonen R. F. Verhage M. (2007) Munc18-1 in secretion: lonely Munc joins SNARE team and takes control. Trends Neurosci. 30, 564 572.
47. Verhage M., Maia A. S., Plomp J. J. et al. (2000) Synaptic assembly of the brain in the absence of neurotransmitter secretion. Science 287, 864 869.
48. Wang S., Sun C. E., Walczak C. A., Ziegle J. S., Kipps B. R., Goldin L. R. Diehl S. R. (1995) Evidence for a susceptibility locus for schizophrenia on chromosome 6pter-p22. Nat. Genet. 10, 41 46.
49. Weickert C. S., Straub R. E., McClintock B. W., Matsumoto M., Hashimoto R., Hyde T. M., Herman M. M., Weinberger D. R. Kleinman J. E. (2004) Human dysbindin (DTNBP1) gene expression in normal brain and in schizophrenic prefrontal cortex and midbrain. Arch. Gen. Psychiatry 61, 544 555.
50. Weickert C. S., Rothmond D. A., Hyde T. M., Kleinman J. E. Straub R. E. (2008) Reduced DTNBP1 (dysbindin-1) mRNA in the hippocampal formation of schizophrenia patients. Schizophr. Res. 98, 105 110.