The dysbindin-containing complex (BLOC-1) in brain: Developmental regulation, interaction with SNARE proteins and role in neurite outgrowth

Molecular Psychiatry

Volumn 15, Issue 2, 2010, Pages 204-215

  Ghiani, C A ^a,b   Starcevic, M ^b   Rodriguez Fernandez, I A ^a,b   Nazarian, R ^b   Cheli, V T ^a,b   Chan, L N ^b,c   Malvar, J S ^a   De Vellis, J ^a,b   Sabatti, C ^b   Dell'Angelica, E C ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Biological plausibility; DTNBP1; Neurite extension; Pallidin; Schizophrenia; Synaptosomal associated protein

Indexed keywords

BIOGENESIS OF LYSOSOME RELATED ORGANELLE COMPLEX 1; DYSBINDIN; SNARE PROTEIN; SYNAPTOSOMAL ASSOCIATED PROTEIN 25; SYNTAXIN; SYNTAXIN 13; UNCLASSIFIED DRUG; BLOC1S1 PROTEIN, HUMAN; CARRIER PROTEIN; DTNBP1 PROTEIN, MOUSE; NERVE PROTEIN; RECOMBINANT PROTEIN; SYNAPTOBREVIN 2; VESICLE ASSOCIATED MEMBRANE PROTEIN 2, MOUSE; VESICLE-ASSOCIATED MEMBRANE PROTEIN 2, MOUSE;

ADULTHOOD; ALLELE; ANIMAL CELL; ARTICLE; BIOCHEMISTRY; BIOGENESIS; BRAIN; BRAIN NERVE CELL; CELL MIGRATION; CELL ORGANELLE; CONTROLLED STUDY; DISEASE MODEL; GENETIC VARIABILITY; HIPPOCAMPUS; INTRACELLULAR MEMBRANE; MEMBRANE FUSION; MOUSE; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; NEWBORN; NONHUMAN; OBSERVATIONAL STUDY; PATHOGENESIS; PERINATAL PERIOD; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN INTERACTION; SCHIZOPHRENIA; ANALYSIS OF VARIANCE; ANIMAL; ANIMAL EMBRYO; C57BL MOUSE; CATTLE; CELL CULTURE; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOUSE MUTANT; MUTATION; NERVE CELL; NEURITE; PHYSIOLOGY; PRENATAL DEVELOPMENT; PROTEIN BINDING; PROTEIN TRANSPORT;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; CARRIER PROTEINS; CATTLE; CELLS, CULTURED; EMBRYO, MAMMALIAN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HIPPOCAMPUS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUTATION; NERVE TISSUE PROTEINS; NEURITES; NEURONS; PROTEIN BINDING; PROTEIN TRANSPORT; QA-SNARE PROTEINS; RECOMBINANT PROTEINS; SNARE PROTEINS; SYNAPTOSOMAL-ASSOCIATED PROTEIN 25; VESICLE-ASSOCIATED MEMBRANE PROTEIN 2;

EID: 75549089372     PISSN: 13594184     EISSN: 14765578     Source Type: Journal    
DOI: 10.1038/mp.2009.58     Document Type: Article

References (65)

1. Ross CA, Margolis RL, Reading SA, Pletnikov M, Coyle JT. Neurobiology of schizophrenia. Neuron 2006; 52: 139-153.
2. Burmeister M, McInnis MG, Zöllner S. Psychiatric genetics: progress amid controversy. Nat Rev Genet 2008; 9: 527-540.
3. Benson MA, Newey SE, Martin-Rendon E, Hawkes R, Blake DJ. Dysbindin, a novel coiled-coil-containing protein that interacts with the dystrobrevins in muscle and brain. J Biol Chem 2001; 276: 24232-24241.
4. Guo AY, Sun J, Riley BP, Thiselton DL, Kendler KS, Zhao Z. The dystrobrevin-binding protein 1 gene: features and networks. Mol Psychiatry 2009; 14: 18-29.
5. Straub RE, Jiang Y, MacLean CJ, Ma Y, Webb BT, Myakishev MVet al. Genetic variation in the 6p22.3 gene DTNBP1, the human ortholog of the mouse dysbindin gene, is associated with schizophrenia. Am J Hum Genet 2002; 71: 337-348.
6. Allen NC, Bagade S, McQueen MB, Ioannidis JP, Kavvoura FK, Khoury MJ et al. Systematic meta-analyses and field synopsis of genetic association studies in schizophrenia: the SzGene database. Nat Genet 2008; 40: 827-834.
7. Shi J, Gershon ES, Liu C. Genetic associations with schizophrenia: meta-analyses of 12 candidate genes. Schizophr Res 2008; 104: 96-107.
8. Mutsuddi M, Morris DW, Waggoner SG, Daly MJ, Scolnick EM, Sklar P. Analysis of high-resolution HapMap of DTNBP1 (Dysbindin) suggests no consistency between reported common variant associations and schizophrenia. Am J Hum Genet 2006; 79: 903-909.
9. Sanders AR, Duan J, Levinson DF, Shi J, He D, Hou C et al. No significant association of 14 candidate genes with schizophrenia in a large European ancestry sample: implications for psychiatric genetics. Am J Psychiatry 2008; 165: 497-506.
10. Kirov G, Ivanov D, Williams NM, Preece A, Nikolov I, Milev R et al. Strong evidence for association between the dystrobrevin binding protein 1 gene (DTNBP1) and schizophrenia in 488 parent-offspring trios from Bulgaria. Biol Psychiatry 2004; 55: 971-975.
11. Gornick MC, Addington AM, Sporn A, Gogtay N, Greenstein D, Lenane M et al. Dysbindin (DTNBP1, 6p22.3) is associated with childhood-onset psychosis and endophenotypes measured by the Premorbid Adjustment Scale (PAS). J Autism Dev Disord 2005; 35: 831-838.
12. Weickert CS, Straub RE, McClintock BW, Matsumoto M, Hashimoto R, Hyde TM et al. Human dysbindin (DTNBP1) gene expression in normal brain and in schizophrenic prefrontal cortex and midbrain. Arch Gen Psychiatry 2004; 61: 544-555.
13. Bray NJ, Preece A, Williams NM, Moskvina V, Buckland PR, Owen MJ et al. Haplotypes at the dystrobrevin binding protein 1 (DTNBP1) gene locus mediate risk for schizophrenia through reduced DTNBP1 expression. Hum Mol Genet 2005; 14: 1947-1954.
14. Weickert CS, Rothmond DA, Hyde TM, Kleinman JE, Straub RE. Reduced DTNBP1 (dysbindin-1) mRNA in the hippocampal formation of schizophrenia patients. Schizophr Res 2008; 98: 105-110.
15. Talbot K, Eidem WL, Tinsley CL, Benson MA, Thompson EW, Smith RJ et al. Dysbindin-1 is reduced in intrinsic, glutamatergic terminals of the hippocampal formation in schizophrenia. J Clin Invest 2004; 113: 1353-1363.
16. Li W, Zhang Q, Oiso N, Novak EK, Gautam R, O'Brien EP et al. 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 2003; 35: 84-89.
17. Hattori S, Murotani T, Matsuzaki S, Ishizuka T, Kumamoto N, Takeda M et al. Behavioral abnormalities and dopamine reductions in sdy mutant mice with a deletion in Dtnbp1, a susceptibility gene for schizophrenia. Biochem Biophys Res Commun 2008; 373: 298-302.
18. Feng YQ, Zhou ZY, He X, Wang H, Guo XL, Hao CJ et al. Dysbindin deficiency in sandy mice causes reduction of snapin and displays behaviors related to schizophrenia. Schizophr Res 2008; 106: 218-222.
19. Takao K, Toyama K, Nakanishi K, Hattori S, Takamura H, Takeda M et al. Impaired long-term memory retention and working memory in sdy mutant mice with a deletion in Dtnbp1, a susceptibility gene for schizophrenia. Mol Brain 2008; 1: 11.
20. Bhardwaj SK, Baharnoori M, Sharif-Askari B, Kamath A, Williams S, Srivastava LK. Behavioral characterization of dysbindin-1 deficient sandy mice. Behav Brain Res 2009; 197: 435-441.
21. Cox MM, Tucker AM, Tang J, Talbot K, Richer DC, Yeh L et al. Neurobehavioral abnormalities in the dysbindin-1 mutant, sandy, on a C57BL/6J genetic background. Genes Brain Behav 2009; 8: 390-397.
22. Chen XW, Feng YQ, Hao CJ, Guo XL, He X, Zhou ZY et al. DTNBP1, a schizophrenia susceptibility gene, affects kinetics of transmitter release. J Cell Biol 2008; 181: 791-801.
23. Nazarian R, Starcevic M, Spencer MJ, Dell'Angelica EC. Reinves-tigation of the dysbindin subunit of BLOC-1 (biogenesis of lysosome-related organelles complex-1) as a dystrobrevin-binding protein. Biochem J 2006; 395: 587-598.
24. Numakawa T, Yagasaki Y, Ishimoto T, Okada T, Suzuki T, Iwata N et al. Evidence of novel neuronal functions of dysbindin, a susceptibility gene for schizophrenia. Hum Mol Genet 2004; 13: 2699-2708.
25. Kumamoto N, Matsuzaki S, Inoue K, Hattori T, Shimizu S, Hashimoto R et al. Hyperactivation of midbrain dopaminergic system in schizophrenia could be attributed to the down-regulation of dysbindin. Biochem Biophys Res Commun 2006; 345: 904-909.
26. Talbot K, Cho D-S, Ong W-Y, Benson MA, Han L-Y, Kazi HA et al. Dysbindin-1 is a synaptic and microtubular protein that binds brain snapin. Hum Mol Genet 2006; 15: 3041-3054.
27. Newell-Litwa K, Seong E, Burmeister M, Faundez V. Neuronal and non-neuronal functions of the AP-3 sorting machinery. J Cell Sci 2007; 120: 531-541.
28. Frankle WG, Lerma J, Laruelle M. The synaptic hypothesis of schizophrenia. Neuron 2003; 39: 205-216.
29. Rapoport JL, Addington AM, Frangou S, Psych MR. The neurodevelopmental model of schizophrenia: update 2005. Mol Psychiatry 2005; 10: 434-449.
30. Karlsgodt KH, Sun D, Jimenez AM, Lutkenhoff ES, Willhite R, van Erp TG et al. Developmental disruptions in neural connectivity in the pathophysiology of schizophrenia. Dev Psychopathol 2008; 20: 1297-1327.
31. Falcón-Pérez JM, Starcevic M, Gautam R, Dell'Angelica EC. BLOC-1, a novel complex containing the pallidin and muted proteins involved in the biogenesis of melanosomes and platelet dense granules. J Biol Chem 2002; 277: 28191-28199.
32. Moriyama K, Bonifacino JS. Pallidin is a component of a multi-protein complex involved in the biogenesis of lysosome-related organelles. Traffic 2002; 3: 666-677.
33. Starcevic M, Dell'Angelica EC. Identification of snapin and three novel proteins (BLOS1, BLOS2, and BLOS3/reduced pigmentation) as subunits of biogenesis of lysosome-related organelles complex-1 (BLOC-1). J Biol Chem 2004; 279: 28393-28401.
34. Di Pietro SM, Falcón-Pérez JM, Tenza D, Setty SRG, Marks MS, Raposo G et al. BLOC-1 interacts with BLOC-2 and AP-3 to facilitate protein trafficking on endosomes. Mol Biol Cell 2006; 17: 4027-4038.
35. Salazar G, Craige B, Styers ML, Newell-Litwa KA, Doucette MM, Wainer BH et al. BLOC-1 complex deficiency alters the targeting of adaptor protein complex-3 cargoes. Mol Biol Cell 2006; 17: 4014-4026.
36. Setty SR, Tenza D, Truschel ST, Chou E, Sviderskaya EV, Theos AC et al. BLOC-1 is required for cargo-specific sorting from vacuolar early endosomes toward lysosome-related organelles. Mol Biol Cell 2007; 18: 768-780.
37. Setty SR, Tenza D, Sviderskaya EV, Bennett DC, Raposo G, Marks MS. Cell-specific ATP7A transport sustains copper-dependent tyrosinase activity in melanosomes. Nature 2008; 454: 1142-1146.
38. Jahn R, Scheller RH. SNAREs-engines for membrane fusion. Nat Rev Mol Cell Biol 2006; 7: 631-643.
39. Ghiani CA, Ying Z, de Vellis J, Gomez-Pinilla F. Exercise decreases myelin-associated glycoprotein expression in the spinal cord and positively modulates neuronal growth. Glia 2007; 55: 966-975.
40. Ciciotte SL, Gwynn B, Moriyama K, Huizing M, Gahl WA, Bonifacino JS et al. Cappuccino, a mouse model of Hermansky-Pudlak syndrome, encodes a novel protein that is part of the pallidin-muted complex (BLOC-1). Blood 2003; 101: 4402-4407.
41. Gwynn B, Martina JA, Bonifacino JS, Sviderskaya EV, Lamoreux ML, Bennett DC et al. Reduced pigmentation (rp), a mouse model of Hermansky-Pudlak syndrome, encodes a novel component of the BLOC-1 complex. Blood 2004; 104: 3181-3189.
42. Huang L, Kuo Y-M, Gitschier J. The pallid gene encodes a novel, syntaxin 13-interacting protein involved in platelet storage pool deficiency. Nat Genet 1999; 23: 329-332.
43. Yin H, Laguna KA, Kuret J. Dysbindin structural homologue CK1BP is an isoform-selective binding partner of human casein kinase-1. Biochemistry 2006; 45: 5297-5308.
44. Washbourne P, Thompson PM, Carta M, Costa ET, Mathews JR, Lopez-Benditó G et al. Genetic ablation of the t-SNARE SNAP-25 distinguishes mechanisms of neuroexocytosis. Nat Neurosci 2002; 5: 19-26.
45. Osen-Sand A, Catsicas M, Staple JK, Jones KA, Ayala G, Knowles J et al. Inhibition of axonal growth by SNAP-25 antisense oligonucleotides in vitro and in vivo. Nature 1993; 364: 445-448.
46. Delgado-Martínez I, Nehring RB, Sørensen JB. Differential abilities of SNAP-25 homologs to support neuronal function. J Neurosci 2007; 27: 9380-9391.
47. Aikawa Y, Lynch KL, Boswell KL, Martin TF. A second SNARE role for exocytic SNAP25 in endosome fusion. Mol Biol Cell 2006; 17: 2113-2124.
48. Hirling H, Steiner P, Chaperon C, Marsault R, Regazzi R, Catsicas S. Syntaxin 13 is a developmentally regulated SNARE involved in neurite outgrowth and endosomal trafficking. Eur J Neurosci 2000; 12: 1913-1923.
49. Akum BF, Chen M, Gunderson SI, Riefler GM, Scerri-Hansen MM, Firestein BL. Cypin regulates dendrite patterning in hippocampal neurons by promoting microtubule assembly. Nat Neurosci 2004; 7: 145-152.
50. Ilardi JM, Mochida S, Sheng ZH. Snapin: a SNARE-associated protein implicated in synaptic transmission. Nat Neurosci 1999; 2: 119-124.
51. Chen M, Lucas KG, Akum BF, Balasingam G, Stawicki TM, Provost JM et al. A novel role for snapin in dendrite patterning: interaction with cypin. Mol Biol Cell 2005; 16: 5103-5114.
52. Buxton P, Zhang XM, Walsh B, Sriratana A, Schenberg I, Manickam E et al. Identification and characterization of snapin as a ubiquitously expressed SNARE-binding protein that interacts with SNAP23 in non-neuronal cells. Biochem J 2003; 375: 433-440.
53. Hunt RA, Edris W, Chanda PK, Nieuwenhuijsen B, Young KH. Snapin interacts with the N-terminus of regulator of G protein signaling 7. Biochem Biophys Res Commun 2003; 303: 594-599.
54. Levitt P, Ebert P, Mirnics K, Nimgaonkar VL, Lewis DA. Making the case for a candidate vulnerability gene in schizophrenia: convergent evidence for regulator of G-protein signaling 4 (RGS4). Biol Psychiatry 2006; 60: 534-537.
55. Dulubova I, Sugita S, Hill S, Hosaka M, Fernandez I, Südhof TC et al. A conformational switch in syntaxin during exocytosis: role of munc18. EMBO J 1999; 18: 4372-4382.
56. Prekeris R, Klumperman J, Chen YA, Scheller RH. Syntaxin 13 mediates cycling of plasma membrane proteins via tubulovesicu-lar recycling endosomes. J Cell Biol 1998; 143: 957-971.
57. Chua CE, Tang BL. Syntaxin 16 is enriched in neuronal dendrites and may have a role in neurite outgrowth. Mol Membr Biol 2008; 25: 35-45.
58. Ozeki Y, Tomoda T, Kleiderlein J, Kamiya A, Bord L, Fujii K et al. Disrupted-in-Schizophrenia-1 (DISC-1): mutant truncation prevents binding to NudE-like (NUDEL) and inhibits neurite outgrowth. Proc Natl Acad Sci USA 2003; 100: 289-294.
59. Miyoshi K, Honda A, Baba K, Taniguchi M, Oono K, Fujita T et al. Disrupted-In-Schizophrenia 1, a candidate gene for schizophrenia, participates in neurite outgrowth. Mol Psychiatry 2003; 8: 685-694.
60. Bellon A. New genes associated with schizophrenia in neurite formation: a review of cell culture experiments. Mol Psychiatry 2007; 12: 620-629.
61. Morris DW, Murphy K, Kenny N, Purcell SM, McGhee KA, Schwaiger S et al. 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 2008; 63: 24-31.
62. Rodriguez-Fernandez IA, Dell'Angelica EC. 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 2009; 32: 190-203.
63. Holt M, Varoqueaux F, Wiederhold K, Takamori S, Urlaub H, Fasshauer D et al. Identification of SNAP-47, a novel Qbc-SNARE with ubiquitous expression. J Biol Chem 2006; 281: 17076-17083.
64. Alberts P, Galli T. The cell outgrowth secretory endosome (COSE): a specialized compartment involved in neuronal morphogenesis. Biol Cell 2003; 95: 419-424.
65. Prekeris R, Foletti DL, Scheller RH. Dynamics of tubulovesicular recycling endosomes in hippocampal neurons. J Neurosci 1999; 19: 10324-10337.