Quantitative proteomic and genetic analyses of the schizophrenia susceptibility factor dysbindin identify novel roles of the Biogenesis of Lysosome-Related Organelles Complex 1

Journal of Neuroscience

Volumn 32, Issue 11, 2012, Pages 3697-3711

  Gokhale, Avanti ^a   Larimore, Jennifer ^a   Werner, Erica ^a   So, Lomon ^a   Moreno De Luca, Andres ^a,c   Lese Martin, Christa ^a   Lupashin, Vladimir V ^d   Smith, Yoland ^a,b   Faundez, Victor ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b EMORY UNIVERSITY   (United States)

^c GEISINGER HEALTH SYSTEM   (United States)

^d UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 AMINO 3 PHOSPHONOPROPIONIC ACID; ALPHA CATENIN; BIOGENESIS OF LYSOSOME RELATED ORGANELLES COMPLEX 1; CELL PROTEIN; CLATHRIN HEAVY CHAIN; COLLAPSIN RESPONSE MEDIATOR PROTEIN; DYSBINDIN; HISTONE H2A; HISTONE H2B; IMMUNOGLOBULIN KAPPA CHAIN; MICROTUBULE ASSOCIATED PROTEIN 4; PEROXIREDOXIN 1; PEROXIREDOXIN 2; POTASSIUM CHANNEL KCNQ5; SEPTIN; SERINE PROTEINASE; SNARE PROTEIN; SORTING NEXIN; SYNAPTOPHYSIN; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DISEASE PREDISPOSITION; FEMALE; FLOW CYTOMETRY; GENE LOCUS; GENETIC ANALYSIS; HIPPOCAMPUS; HUMAN; HUMAN CELL; IMMUNOAFFINITY CHROMATOGRAPHY; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEOMICS; SCHIZOPHRENIA;

ANIMALS; CARRIER PROTEINS; CELL LINE, TUMOR; GENETIC ASSOCIATION STUDIES; GENETIC PREDISPOSITION TO DISEASE; HEK293 CELLS; HUMANS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; PROTEOMICS; SCHIZOPHRENIA;

EID: 84858022403     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5640-11.2012     Document Type: Article

References (70)

1. Allen NC, Bagade S, McQueen MB, Ioannidis JP, Kavvoura FK, Khoury MJ, Tanzi RE, Bertram L (2008) Systematic meta-analyses and field synopsis of genetic association studies in schizophrenia: the SzGene database. Nat Genet 40:827-834.
2. Baust T, Anitei M, Czupalla C, Parshyna I, Bourel L, Thiele C, Krause E, Hoflack B (2008) Protein networks supporting AP-3 function in targeting lysosomal membrane proteins. Mol Biol Cell 19:1942-1951.
3. Bell KF, Hardingham GE (2011) CNS peroxiredoxins and their regulation in health and disease. Antioxid Redox Signal 14:1467-1477.
4. Bhardwaj SK, Baharnoori M, Sharif-Askari B, Kamath A, Williams S, Srivastava LK (2009) Behavioral characterization of dysbindin-1 deficient sandy mice. Behav Brain Res 197:435-441.
5. Borner GH, Harbour M, Hester S, Lilley KS, Robinson MS (2006) Comparative proteomics of clathrin-coated vesicles. J Cell Biol 175:571-578.
6. Buizer-Voskamp JE, Muntjewerff JW, Strengman E, Sabatti C, Stefansson H, Vorstman JA, Ophoff RA (2011) Genome-wide analysis shows increased frequency of copy number variation deletions in Dutch schizophrenia patients. Biol Psychiatry 70:655-662.
7. Cheli VT, Daniels RW, Godoy R, Hoyle DJ, Kandachar V, Starcevic M, Martinez-Agosto JA, Poole S, DiAntonio A, Lloyd VK, Chang HC, Krantz DE, Dell'Angelica EC (2010) Genetic modifiers of abnormal organelle biogenesis in a Drosophila model of BLOC-1 deficiency. Hum Mol Genet 19:861-878.
8. Cossarizza A, Ferraresi R, Troiano L, Roat E, Gibellini L, Bertoncelli L, Nasi M, Pinti M (2009) Simultaneous analysis of reactive oxygen species and reduced glutathione content in living cells by polychromatic flow cytometry. Nat Protoc 4:1790-1797.
9. Cox MM, Tucker AM, Tang J, Talbot K, Richer DC, Yeh L, Arnold SE (2009) Neurobehavioral abnormalities in the dysbindin-1 mutant, sandy, on a C57BL/6J genetic background. Genes Brain Behav 8:390-397.
10. Craige B, Salazar G, Faundez V (2008) Phosphatidylinositol-4-kinase type II alpha contains an AP-3-sorting motif and a kinase domain that are both required for endosome traffic. Mol Biol Cell 19:1415-1426.
11. Dell'Angelica EC (2009) AP-3-dependent trafficking and disease: the first decade. Curr Opin Cell Biol 21:552-559.
12. Dell'Angelica EC, Klumperman J, Stoorvogel W, Bonifacino JS (1998) Association of the AP-3 adaptor complex with clathrin. Science 280: 431-434.
13. Dickman DK, Davis GW (2009) The schizophrenia susceptibility gene dysbindin controls synaptic homeostasis. Science 326:1127-1130.
14. Di Pietro SM, Dell'Angelica EC (2005) The cell biology of Hermansky- Pudlak syndrome: recent advances. Traffic 6:525-533.
15. Di Pietro SM, Falcón-Pérez JM, Tenza D, Setty SR, Marks MS, Raposo G, Dell'Angelica EC (2006) BLOC-1 interacts with BLOC-2 and the AP-3 complex to facilitate protein trafficking on endosomes. Mol Biol Cell 17:4027-4038.
16. Finkel T (2011) Signal transduction by reactive oxygen species. J Cell Biol 194:7-15.
17. Föcking M, Dicker P, English JA, Schubert KO, Dunn MJ, Cotter DR (2011) Common proteomic changes in the hippocampus in schizophrenia and bipolar disorder and particular evidence for involvement of cornu ammonis regions 2 and 3. Arch Gen Psychiatry 68:477-488.
18. Ghiani CA, Dell'Angelica EC (2011) Dysbindin-containing complexes and their proposed functions in brain: from zero to (too) many in a decade. ASN Neuro 3:e00058.
19. Gillingham AK, Pfeifer AC, Munro S (2002) CASP, the alternatively spliced product of the gene encoding the CCAAT-displacement protein transcription factor, is a Golgi membrane protein related to giantin. Mol Biol Cell 13:3761-3774.
20. Hattori S, Murotani T, Matsuzaki S, Ishizuka T, Kumamoto N, Takeda M, Tohyama M, Yamatodani A, Kunugi H, Hashimoto R (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.
21. Iizuka Y, Sei Y, Weinberger DR, Straub RE (2007) Evidence that the BLOC-1 protein dysbindin modulates dopamine D2 receptor internalization and signaling but not D1 internalization. J Neurosci 27:12390-12395.
22. International Schizophrenia Consortium (2008) Rare chromosomal deletions and duplications increase risk of schizophrenia. Nature 455: 237-241.
23. Ji Y, Yang F, Papaleo F, Wang HX, Gao WJ, Weinberger DR, Lu B (2009) Role of dysbindin in dopamine receptor trafficking and cortical GABA function. Proc Natl Acad Sci U S A 106:19593-19598.
24. Karayiorgou M, Simon TJ, Gogos JA (2010) 22q11.2 microdeletions: linkingDNAstructural variation to brain dysfunction and schizophrenia. Nat Rev Neurosci 11:402-416.
25. Larimore J, Tornieri K, Ryder PV, Gokhale A, Zlatic SA, Craige B, Lee JD, Talbot K, Pare JF, Smith Y, Faundez V (2011) The schizophrenia susceptibility factor dysbindin and its associated complex sort cargoes from cell bodies to the synapse. Mol Biol Cell 22:4854-4867.
26. Lee HH, Nemecek D, Schindler C, Smith WJ, Ghirlando R, Steven AC, Bonifacino JS, Hurley JH (2011) Assembly and architecture of the biogenesis of lysosome-related organelles complex-1 (BLOC-1). J Biol Chem doi:10.1074/jbc.M111.325746.
27. Lees JA, Yip CK, Walz T, Hughson FM (2010) Molecular organization of the COG vesicle tethering complex. Nat Struct Mol Biol 17:1292-1297.
28. Li W, Zhang Q, Oiso N, Novak EK, Gautam R, O'Brien EP, Tinsley CL, Blake DJ, Spritz RA, Copeland NG, Jenkins NA, Amato D, Roe BA, Starcevic M, Dell'Angelica EC, Elliott RW, Mishra V, Kingsmore SF, Paylor RE, Swank RT (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.
29. Li W, Rusiniak ME, Chintala S, Gautam R, Novak EK, Swank RT (2004) Murine Hermansky-Pudlak syndrome genes: regulators of lysosomerelated organelles. Bioessays 26:616-628.
30. Lomant AJ, Fairbanks G (1976) Chemical probes of extended biological structures: synthesis and properties of the cleavable protein cross-linking reagent [35S]dithiobis(succinimidyl propionate). J Mol Biol 104:243-261.
31. Malhotra D, McCarthy S, Michaelson JJ, Vacic V, Burdick KE, Yoon S, Cichon S, Corvin A, Gary S, Gershon ES, Gill M, Karayiorgou M, Kelsoe JR, Krastoshevsky O, Krause V, Leibenluft E, Levy DL, Makarov V, Bhandari A, Malhotra AK, et al. (2011) High Frequencies of De Novo CNVs in Bipolar Disorder and Schizophrenia. Neuron 72:951-963.
32. Mann M (2006) Functional and quantitative proteomics using SILAC. Nat Rev Mol Cell Biol 7:952-958.
33. Marley A, von Zastrow M (2010) Dysbindin promotes the post-endocytic sorting of G protein-coupled receptors to lysosomes. PLoS ONE 5:e9325.
34. Martins-de-Souza D, Harris LW, Guest PC, Bahn S (2011) The role of energy metabolism dysfunction and oxidative stress in schizophrenia revealed by proteomics. Antioxid Redox Signal 15:2067-2079.
35. Mead CL, Kuzyk MA, Moradian A, Wilson GM, Holt RA, Morin GB (2010) Cytosolic protein interactions of the schizophrenia susceptibility gene dysbindin. J Neurochem 113:1491-1503.
36. Mullin AP, Gokhale A, Larimore J, Faundez V (2011) Cell biology of the BLOC-1 complex subunit dysbindin, a schizophrenia susceptibility gene. Mol Neurobiol 44:53-64.
37. Myhre O, Andersen JM, Aarnes H, Fonnum F (2003) Evaluation of the probes 2',7'-dichlorofluorescin diacetate, luminol, and lucigenin as indicators of reactive species formation. Biochem Pharmacol 65:1575-1582.
38. Nakahira M, Macedo JN, Seraphim TV, Cavalcante N, Souza TA, Damalio JC, Reyes LF, Assmann EM, Alborghetti MR, Garratt RC, Araujo AP, Zanchin NI, Barbosa JA, Kobarg J (2010) A draft of the human septin interactome. PLoS ONE 5:e13799.
39. Neumann CA, Cao J, Manevich Y (2009) Peroxiredoxin 1 and its role in cell signaling. Cell Cycle 8:4072-4078.
40. Newell-Litwa K, Salazar G, Smith Y, Faundez V (2009) Roles of BLOC-1 and AP-3 Complexes in Cargo Sorting to Synaptic Vesicles. Mol Biol Cell 20:1441-1453.
41. Newell-Litwa K, Chintala S, Jenkins S, Pare JF, McGaha L, Smith Y, Faundez V (2010) Hermansky-Pudlak protein complexes, AP-3 and BLOC-1, differentially regulate presynaptic composition in the striatum and hippocampus. J Neurosci 30:820-831.
42. Oka T, Ungar D, Hughson FM, Krieger M (2004) TheCOGand COPI complexes interact to control the abundance of GEARs, a subset of Golgi integral membrane proteins. Mol Biol Cell 15:2423-2435.
43. Ong SE, Mann M (2006) A practical recipe for stable isotope labeling by amino acids in cell culture (SILAC). Nat Protoc 1:2650-2660.
44. Ong SE, Blagoev B, Kratchmarova I, Kristensen DB, Steen H, Pandey A, Mann M (2002) Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol Cell Proteomics 1:376-386.
45. Papaleo F, Yang F, Garcia S, Chen J, Lu B, Crawley JN, Weinberger DR (2012) Dysbindin-1 modulates prefrontal cortical activity and schizophrenia-like behaviors via dopamine/D2 pathways. Mol Psychiatry 17:85-98.
46. Raposo G, Marks MS (2007) Melanosomes-dark organelles enlighten endosomal membrane transport. Nat Rev Mol Cell Biol 8:786-797.
47. Ross CA, Margolis RL, Reading SA, Pletnikov M, Coyle JT (2006) Neurobiology of schizophrenia. Neuron 52:139-153.
48. Salazar G, Zlatic S, Craige B, Peden AA, Pohl J, Faundez V (2009) Hermansky-Pudlak syndrome protein complexes associate with phosphatidylinositol 4-kinase type II alpha in neuronal and non-neuronal cells. J Biol Chem 284:1790-1802.
49. Schmidt EF, Strittmatter SM (2007) The CRMP family of proteins and their role in Sema3A signaling. Adv Exp Med Biol 600:1-11.
50. Setty SR, Tenza D, Truschel ST, Chou E, Sviderskaya EV, Theos AC, Lamoreux ML, Di Pietro SM, Starcevic M, Bennett DC, Dell'Angelica EC, Raposo G, Marks MS (2007) BLOC-1 is required for cargo-specific sorting from vacuolar early endosomes toward lysosome-related organelles. Mol Biol Cell 18:768-780.
51. Shestakova A, Zolov S, Lupashin V (2006) COG complex-mediated recycling of Golgi glycosyltransferases is essential for normal protein glycosylation. Traffic 7:191-204.
52. Smith RD, Lupashin VV (2008) Role of the conserved oligomeric Golgi (COG) complex in protein glycosylation. Carbohydr Res 343:2024-2031.
53. Smith RD, Willett R, Kudlyk T, Pokrovskaya I, Paton AW, Paton JC, Lupashin VV (2009) The COG complex, Rab6 and COPI define a novel Golgi retrograde trafficking pathway that is exploited by SubAB toxin. Traffic 10:1502-1517.
54. Starcevic M, Dell'Angelica EC (2004) 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 279:28393-28401.
55. Sun J, Kuo PH, Riley BP, Kendler KS, Zhao Z (2008) Candidate genes for schizophrenia: a survey of association studies and gene ranking. AmJMed Genet B Neuropsychiatr Genet 147B:1173-1181.
56. Suzuki SC, Takeichi M (2008) Cadherins in neuronal morphogenesis and function. Dev Growth Differ 50 [Suppl 1]:S119-S130.
57. Talbot K (2009) The sandy (sdy) mouse: a dysbindin-1 mutant relevant to schizophrenia research. Prog Brain Res 179:87-94
58. Talbot K, Eidem WL, Tinsley CL, Benson MA, Thompson EW, Smith RJ, Hahn CG, Siegel SJ, Trojanowski JQ, Gur RE, Blake DJ, Arnold SE (2004) Dysbindin-1 is reduced in intrinsic, glutamatergic terminals of the hippocampal formation in schizophrenia. J Clin Invest 113:1353-1363.
59. Talbot K, Cho DS, Ong WY, Benson MA, Han LY, Kazi HA, Kamins J, Hahn CG, Blake DJ, Arnold SE (2006) Dysbindin-1 is a synaptic and microtubular protein that binds brain snapin. Hum Mol Genet 15:3041-3054.
60. Talbot K, Ong WY, Blake DJ, Tang D, Louneva N, Carlson GC, Arnold SE (2009) Dysbindin-1 and its protein family, with special attention to the potential role of dysbindin-1 in neuronal functions and the pathophysiology of schizophrenia. In: Handbook of neurochemistry and molecular neurobiology (Kantrowitz J, ed), pp 107-241. New York: Springer Science.
61. Talbot K, Louneva N, Cohen JW, Kazi H, Blake DJ, Arnold SE (2011) Synaptic dysbindin-1 reductions in schizophrenia occur in an isoform-specific manner indicating their subsynaptic location. PLoS ONE 6:e16886.
62. Tandon R, Keshavan MS, Nasrallah HA (2008) Schizophrenia, "just the facts" what we know in 2008. 2. Epidemiology and etiology. Schizophr Res 102:1-18.
63. Tang J, LeGros RP, Louneva N, Yeh L, Cohen JW, Hahn CG, Blake DJ, Arnold SE, Talbot K (2009a) Dysbindin-1 in dorsolateral prefrontal cortex of schizophrenia cases is reduced in an isoform-specific manner unrelated to dysbindin-1 mRNA expression. Hum Mol Genet 18:3851-3863.
64. Tang TT, Yang F, Chen BS, Lu Y, Ji Y, Roche KW, Lu B (2009b) Dysbindin regulates hippocampal LTP by controlling NMDA receptor surface expression. Proc Natl Acad Sci U S A 106:21395-21400.
65. Trinkle-Mulcahy L, Boulon S, Lam YW, Urcia R, Boisvert FM, Vandermoere F, Morrice NA, Swift S, Rothbauer U, Leonhardt H, Lamond A (2008) Identifying specific protein interaction partners using quantitative mass spectrometry and bead proteomes. J Cell Biol 183:223-239.
66. Ungar D, Oka T, Brittle EE, Vasile E, Lupashin VV, Chatterton JE, Heuser JE, Krieger M, Waters MG (2002) Characterization of a mammalian Golgilocalized protein complex, COG, that is required for normal Golgi morphology and function. J Cell Biol 157:405-415.
67. Ungar D, Oka T, Krieger M, Hughson FM (2006) Retrograde transport on the COG railway. Trends Cell Biol 16:113-120.
68. Wei ML (2006) Hermansky-Pudlak syndrome: a disease of protein trafficking and organelle function. Pigment Cell Res 19:19-42.
69. Zhang Q, Li W, Novak EK, Karim A, Mishra VS, Kingsmore SF, Roe BA, Suzuki T, Swank RT (2002) The gene for the muted (mu) mouse, a model for Hermansky-Pudlak syndrome, defines a novel protein which regulates vesicle trafficking. Hum Mol Genet 11:697-706.
70. Zlatic SA, Ryder PV, Salazar G, Faundez V (2010) Isolation of labile multiprotein complexes by in vivo controlled cellular cross-linking and immunomagnetic affinity chromatography. J Vis Exp doi:10.3791/1855