Dysbindin-associated proteome in the P2 synaptosome fraction of mouse brain

Journal of Proteome Research

Volumn 13, Issue 11, 2014, Pages 4567-4580

  Han, Meng Hsuan J ^a,b   Hu, Zhonghua ^a   Chen, Cai Yun ^a   Chen, Yong ^c   Gucek, Marjan ^c   Li, Zheng ^a   Markey, Sanford P ^a  

^a NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^b CHILDREN'S NATIONAL MEDICAL CENTER   (United States)

^c NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

BAC transgenesis; Dysbindin; mass spectrometry; proteasome; protein complex; protein protein interaction; schizophrenia; synaptosome

Indexed keywords

BLOC 1 PROTEIN; DYSBINDIN; FAM91A1 PROTEIN; PALLIDIN; PROTEOME; PSMA4 PROTEIN; PSMD9 PROTEIN; SNAPIN; UNCLASSIFIED DRUG; WDR11 PROTEIN; CARRIER PROTEIN; DTNBP1 PROTEIN, MOUSE; DYSTROPHIN ASSOCIATED PROTEIN; ISOPROTEIN; LECTIN; MULTIPROTEIN COMPLEX; PLDN PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL FRACTIONATION; CONTROLLED STUDY; MASS SPECTROMETRY; MOUSE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN EXPRESSION; SYNAPTOSOME; TRANSGENIC MOUSE; ANIMAL; BRAIN; GENETICS; IMMUNOPRECIPITATION; ISOLATION AND PURIFICATION; METABOLISM; NERVE CELL PLASTICITY; PHYSIOLOGY; SCHIZOPHRENIA;

ANIMALS; BRAIN; CARRIER PROTEINS; DYSTROPHIN-ASSOCIATED PROTEINS; IMMUNOPRECIPITATION; LECTINS; MASS SPECTROMETRY; MICE; MICE, TRANSGENIC; MULTIPROTEIN COMPLEXES; NEURONAL PLASTICITY; PROTEIN ISOFORMS; PROTEOME; SCHIZOPHRENIA; SYNAPTOSOMES;

EID: 84908896599     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr500656z     Document Type: Article

References (66)

1. Tandon, R.; Keshavan, M. S.; Nasrallah, H. A. Schizophrenia, just the facts what we know in 2008. 2. Epidemiology and etiology Schizophr. Res. 2008, 102, 1-18
2. Sullivan, P. F.; Kendler, K. S.; Neale, M. C. Schizophrenia as a complex trait: evidence from a meta-analysis of twin studies Arch. Gen. Psychiatry 2003, 60, 1187-92
3. Sullivan, P. F. Schizophrenia genetics: the search for a hard lead Curr. Opin Psychiatry 2008, 21, 157-60
4. Cardno, A. G.; Gottesman, I. I. Twin studies of schizophrenia: from bow-and-arrow concordances to star wars Mx and functional genomics Am. J. Med. Genet. 2000, 97, 12-7
5. OTuathaigh, C. M.; Babovic, D.; OMeara, G.; Clifford, J. J.; Croke, D. T.; Waddington, J. L. Susceptibility genes for schizophrenia: characterisation of mutant mouse models at the level of phenotypic behaviour Neurosci. Biobehav. Rev. 2007, 31, 60-78
6. International Schizophrenia Consortium Rare chromosomal deletions and duplications increase risk of schizophrenia Nature 2008, 455, 237-41
7. Straub, R. E.; Jiang, Y.; MacLean, C. J.; Ma, Y.; Webb, B. T.; Myakishev, M. V.; Harris-Kerr, C.; Wormley, B.; Sadek, H.; Kadambi, B.; Cesare, A. J.; Gibberman, A.; Wang, X.; ONeill, F. A.; Walsh, D.; Kendler, K. S. 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, 337-48
8. Purcell, S. M.; Moran, J. L.; Fromer, M.; Ruderfer, D.; Solovieff, N.; Roussos, P.; ODushlaine, C.; Chambert, K.; Bergen, S. E.; Kahler, A.; Duncan, L.; Stahl, E.; Genovese, G.; Fernandez, E.; Collins, M. O.; Komiyama, N. H.; Choudhary, J. S.; Magnusson, P. K.; Banks, E.; Shakir, K.; Garimella, K.; Fennell, T.; DePristo, M.; Grant, S. G.; Haggarty, S. J.; Gabriel, S.; Scolnick, E. M.; Lander, E. S.; Hultman, C. M.; Sullivan, P. F.; McCarroll, S. A.; Sklar, P. A polygenic burden of rare disruptive mutations in schizophrenia Nature 2014, 506, 185-90
9. Purcell, S. M.; Wray, N. R.; Stone, J. L.; Visscher, P. M.; ODonovan, M. C.; Sullivan, P. F.; Sklar, P. Common polygenic variation contributes to risk of schizophrenia and bipolar disorder Nature 2009, 460, 748-52
10. Singh, S.; Kumar, A.; Agarwal, S.; Phadke, S. R.; Jaiswal, Y. Genetic insight of schizophrenia: past and future perspectives Gene 2014, 535, 97-100
11. Balu, D. T.; Coyle, J. T. Neuroplasticity signaling pathways linked to the pathophysiology of schizophrenia Neurosci. Biobehav. Rev. 2011, 35, 848-70
12. Ghiani, C. A.; DellAngelica, E. C. Dysbindin-containing complexes and their proposed functions in brain: from zero to (too) many in a decade ASN Neuro 2011, 3, 109-124
13. Sun, J.; Kuo, P. H.; Riley, B. P.; Kendler, K. S.; Zhao, Z. Candidate genes for schizophrenia: a survey of association studies and gene ranking Am. J. Med. Genet., Part B 2008, 147B, 1173-81
14. Allen, N. C.; Bagade, S.; McQueen, M. B.; Ioannidis, J. P.; Kavvoura, F. K.; Khoury, M. J.; Tanzi, R. E.; Bertram, L. Systematic meta-analyses and field synopsis of genetic association studies in schizophrenia: the SzGene database Nat. Genet. 2008, 40, 827-34
15. Sanders, A. R.; Duan, J.; Levinson, D. F.; Shi, J.; He, D.; Hou, C.; Burrell, G. J.; Rice, J. P.; Nertney, D. A.; Olincy, A.; Rozic, P.; Vinogradov, S.; Buccola, N. G.; Mowry, B. J.; Freedman, R.; Amin, F.; Black, D. W.; Silverman, J. M.; Byerley, W. F.; Crowe, R. R.; Cloninger, C. R.; Martinez, M.; Gejman, P. V. 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
16. Joo, E. J.; Lee, K. Y.; Jeong, S. H.; Ahn, Y. M.; Koo, Y. J.; Kim, Y. S. The dysbindin gene (DTNBP1) and schizophrenia: no support for an association in the Korean population Neurosci. Lett. 2006, 407, 101-6
17. Strohmaier, J.; Frank, J.; Wendland, J. R.; Schumacher, J.; Jamra, R. A.; Treutlein, J.; Nieratschker, V.; Breuer, R.; Mattheisen, M.; Herms, S.; Muhleisen, T. W.; Maier, W.; Nothen, M. M.; Cichon, S.; Rietschel, M.; Schulze, T. G. A reappraisal of the association between dysbindin (DTNBP1) and schizophrenia in a large combined case-control and family-based sample of German ancestry Schizophr. Res. 2010, 118, 98-105
18. Wirgenes, K. V.; Djurovic, S.; Agartz, I.; Jonsson, E. G.; Werge, T.; Melle, I.; Andreassen, O. A. Dysbindin and d-amino-acid-oxidase gene polymorphisms associated with positive and negative symptoms in schizophrenia Neuropsychobiology 2009, 60, 31-6
19. DeRosse, P.; Funke, B.; Burdick, K. E.; Lencz, T.; Ekholm, J. M.; Kane, J. M.; Kucherlapati, R.; Malhotra, A. K. Dysbindin genotype and negative symptoms in schizophrenia Am. J. Psychiatry 2006, 163, 532-4
20. Pae, C. U.; Drago, A.; Kim, J. J.; Patkar, A. A.; Jun, T. Y.; Lee, C.; Mandelli, L.; De Ronchi, D.; Paik, I. H.; Serretti, A. DTNBP1 haplotype influences baseline assessment scores of schizophrenic in-patients Neurosci. Lett. 2008, 440, 150-4
21. Talbot, K.; Eidem, W. L.; Tinsley, C. L.; Benson, M. A.; Thompson, E. W.; Smith, R. J.; Hahn, C. G.; Siegel, S. J.; Trojanowski, J. Q.; Gur, R. E.; Blake, D. J.; Arnold, S. E. Dysbindin-1 is reduced in intrinsic, glutamatergic terminals of the hippocampal formation in schizophrenia J. Clin. Invest. 2004, 113, 1353-63
22. 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. Human dysbindin (DTNBP1) gene expression in normal brain and in schizophrenic prefrontal cortex and midbrain Arch. Gen. Psychiatry 2004, 61, 544-55
23. Talbot, K.; Louneva, N.; Cohen, J. W.; Kazi, H.; Blake, D. J.; Arnold, S. E. Synaptic dysbindin-1 reductions in schizophrenia occur in an isoform-specific manner indicating their subsynaptic location PLoS One 2011, 6, e16886
24. Tang, J.; LeGros, R. P.; Louneva, N.; Yeh, L.; Cohen, J. W.; Hahn, C. G.; Blake, D. J.; Arnold, S. E.; Talbot, K. 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. 2009, 18, 3851-63
25. Bray, N. J.; Preece, A.; Williams, N. M.; Moskvina, V.; Buckland, P. R.; Owen, M. J.; ODonovan, M. C. Haplotypes at the dystrobrevin binding protein 1 (DTNBP1) gene locus mediate risk for schizophrenia through reduced DTNBP1 expression Hum. Mol. Genet. 2005, 14, 1947-54
26. Feng, Y. Q.; Zhou, Z. Y.; He, X.; Wang, H.; Guo, X. L.; Hao, C. J.; Guo, Y.; Zhen, X. C.; Li, W. Dysbindin deficiency in sandy mice causes reduction of snapin and displays behaviors related to schizophrenia Schizophr. Res. 2008, 106, 218-28
27. Talbot, K. The sandy (sdy) mouse: a dysbindin-1 mutant relevant to schizophrenia research Prog. Brain Res. 2009, 179, 87-94
28. Bhardwaj, S. K.; Baharnoori, M.; Sharif-Askari, B.; Kamath, A.; Williams, S.; Srivastava, L. K. Behavioral characterization of dysbindin-1 deficient sandy mice Behav. Brain Res. 2009, 197, 435-41
29. Benson, M. A.; Newey, S. E.; Martin-Rendon, E.; Hawkes, R.; Blake, D. J. Dysbindin, a novel coiled-coil-containing protein that interacts with the dystrobrevins in muscle and brain J. Biol. Chem. 2001, 276, 24232-41
30. Talbot, K.; Cho, D. S.; Ong, W. Y.; Benson, M. A.; Han, L. Y.; Kazi, H. A.; Kamins, J.; Hahn, C. G.; Blake, D. J.; Arnold, S. E. Dysbindin-1 is a synaptic and microtubular protein that binds brain snapin Hum. Mol. Genet. 2006, 15, 3041-54
31. Guo, A. Y.; Sun, J.; Riley, B. P.; Thiselton, D. L.; Kendler, K. S.; Zhao, Z. The dystrobrevin-binding protein 1 gene: features and networks Mol. Psychiatry 2009, 14, 18-29
32. Ghiani, C. A.; Starcevic, M.; Rodriguez-Fernandez, I. A.; Nazarian, R.; Cheli, V. T.; Chan, L. N.; Malvar, J. S.; de Vellis, J.; Sabatti, C.; DellAngelica, E. C. The dysbindin-containing complex (BLOC-1) in brain: developmental regulation, interaction with SNARE proteins and role in neurite outgrowth Mol. Psychiatry 2010, 15, 115 204-15.
33. Frankle, W. G.; Lerma, J.; Laruelle, M. The synaptic hypothesis of schizophrenia Neuron 2003, 39, 205-16
34. Li, W.; Zhang, Q.; Oiso, N.; Novak, E. K.; Gautam, R.; OBrien, E. P.; Tinsley, C. L.; Blake, D. J.; Spritz, R. A.; Copeland, N. G.; Jenkins, N. A.; Amato, D.; Roe, B. A.; Starcevic, M.; DellAngelica, E. C.; Elliott, R. W.; Mishra, V.; Kingsmore, S. F.; Paylor, R. E.; Swank, R. T. 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, 84-9
35. Breen, G.; Prata, D.; Osborne, S.; Munro, J.; Sinclair, M.; Li, T.; Staddon, S.; Dempster, D.; Sainz, R.; Arroyo, B.; Kerwin, R. W.; St. Clair, D.; Collier, D. Association of the dysbindin gene with bipolar affective disorder Am. J. Psychiatry 2006, 163, 1636-8
36. Sardiu, M. E.; Washburn, M. P. Building protein-protein interaction networks with proteomics and informatics tools J. Biol. Chem. 2011, 286, 23645-51
37. Camargo, L. M.; Collura, V.; Rain, J. C.; Mizuguchi, K.; Hermjakob, H.; Kerrien, S.; Bonnert, T. P.; Whiting, P. J.; Brandon, N. J. Disrupted in Schizophrenia 1 interactome: evidence for the close connectivity of risk genes and a potential synaptic basis for schizophrenia Mol. Psychiatry 2007, 12, 74-86
38. Mead, C. L.; Kuzyk, M. A.; Moradian, A.; Wilson, G. M.; Holt, R. A.; Morin, G. B. Cytosolic protein interactions of the schizophrenia susceptibility gene dysbindin J. Neurochem 2010, 113, 1491-503
39. Gokhale, A.; Larimore, J.; Werner, E.; So, L.; Moreno-De-Luca, A.; Lese-Martin, C.; Lupashin, V. V.; Smith, Y.; Faundez, V. Quantitative proteomic and genetic analyses of the schizophrenia susceptibility factor dysbindin identify novel roles of the biogenesis of lysosome-related organelles complex 1 J. Neurosci. 2012, 32, 3697-711
40. Pitre, S.; Alamgir, M.; Green, J. R.; Dumontier, M.; Dehne, F.; Golshani, A. Computational methods for predicting protein-protein interactions Adv. Biochem. Eng. Biotechnol. 2008, 110, 247-67
41. Whittaker, V. P. Thirty years of synaptosome research J. Neurocytol. 1993, 22, 735-42
42. Poser, I.; Sarov, M.; Hutchins, J. R.; Heriche, J. K.; Toyoda, Y.; Pozniakovsky, A.; Weigl, D.; Nitzsche, A.; Hegemann, B.; Bird, A. W.; Pelletier, L.; Kittler, R.; Hua, S.; Naumann, R.; Augsburg, M.; Sykora, M. M.; Hofemeister, H.; Zhang, Y.; Nasmyth, K.; White, K. P.; Dietzel, S.; Mechtler, K.; Durbin, R.; Stewart, A. F.; Peters, J. M.; Buchholz, F.; Hyman, A. A. BAC TransgeneOmics: a high-throughput method for exploration of protein function in mammals Nat. Methods 2008, 5, 409-15
43. Warming, S.; Costantino, N.; Court, D. L.; Jenkins, N. A.; Copeland, N. G. Simple and highly efficient BAC recombineering using galK selection Nucleic Acids Res. 2005, 33, e36
44. Han, M. H.; Lin, C.; Meng, S.; Wang, X. Proteomics analysis reveals overlapping functions of clustered protocadherins Mol. Cell. Proteomics 2010, 9, 71-83
45. Keller, A.; Nesvizhskii, A. I.; Kolker, E.; Aebersold, R. Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search Anal. Chem. 2002, 74, 5383-92
46. Nesvizhskii, A. I.; Keller, A.; Kolker, E.; Aebersold, R. A statistical model for identifying proteins by tandem mass spectrometry Anal. Chem. 2003, 75, 4646-58
47. Han, M. H.; Jiao, S.; Jia, J. M.; Chen, Y.; Chen, C. Y.; Gucek, M.; Markey, S. P.; Li, Z. The novel caspase-3 substrate Gap43 is involved in AMPA receptor endocytosis and long-term depression Mol. Cell. Proteomics 2013, 12, 3719-31
48. Strucksberg, K. H.; Tangavelou, K.; Schroder, R.; Clemen, C. S. Proteasomal activity in skeletal muscle: a matter of assay design, muscle type, and age Anal. Biochem. 2010, 399, 225-9
49. Salazar, G.; Zlatic, S.; Craige, B.; Peden, A. A.; Pohl, J.; Faundez, V. Hermansky-Pudlak syndrome protein complexes associate with phosphatidylinositol 4-kinase type II alpha in neuronal and non-neuronal cells J. Biol. Chem. 2009, 284, 1790-802
50. Zhang, L.; Rayner, S.; Katoku-Kikyo, N.; Romanova, L.; Kikyo, N. Successful co-immunoprecipitation of Oct4 and Nanog using cross-linking Biochem. Biophys. Res. Commun. 2007, 361, 611-4
51. Falcon-Perez, J. M.; Starcevic, M.; Gautam, R.; DellAngelica, E. C. 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, 28191-9
52. Hollenback, S. M.; Lyman, S.; Cheng, J. Recombineering-based procedure for creating BAC transgene constructs for animals and cell lines. Current Protocols in Molecular Biology; John Wiley & Sons: New York, 2011; Chapter 23, Unit 23 14.
53. Van Keuren, M. L.; Gavrilina, G. B.; Filipiak, W. E.; Zeidler, M. G.; Saunders, T. L. Generating transgenic mice from bacterial artificial chromosomes: transgenesis efficiency, integration and expression outcomes Transgenic Res. 2009, 18, 769-85
54. Chandler, K. J.; Chandler, R. L.; Broeckelmann, E. M.; Hou, Y.; Southard-Smith, E. M.; Mortlock, D. P. Relevance of BAC transgene copy number in mice: transgene copy number variation across multiple transgenic lines and correlations with transgene integrity and expression Mamm. Genome 2007, 18, 693-708
55. Nazarian, R.; Starcevic, M.; Spencer, M. J.; DellAngelica, E. C. Reinvestigation of the dysbindin subunit of BLOC-1 (biogenesis of lysosome-related organelles complex-1) as a dystrobrevin-binding protein Biochem. J. 2006, 395, 587-98
56. Wong, M. L.; Dong, C.; Andreev, V.; Arcos-Burgos, M.; Licinio, J. Prediction of susceptibility to major depression by a model of interactions of multiple functional genetic variants and environmental factors Mol. Psychiatry 2012, 17, 624-633
57. Gragnoli, C. Proteasome modulator 9 and depression in type 2 diabetes Curr. Med. Chem. 2012, 19, 5178-5180
58. Lee, Y. H.; Kim, J. H.; Song, G. G. Pathway analysis of a genome-wide association study in schizophrenia Gene 2013, 525, 107-15
59. Locke, M.; Tinsley, C. L.; Benson, M. A.; Blake, D. J. TRIM32 is an E3 ubiquitin ligase for dysbindin Hum. Mol. Genet. 2009, 18, 2344-58
60. Jarome, T. J.; Helmstetter, F. J. The ubiquitin-proteasome system as a critical regulator of synaptic plasticity and long-term memory formation Neurobiol. Learn. Mem. 2013, 105, 107-16
61. Lin, A. W.; Man, H. Y. Ubiquitination of neurotransmitter receptors and postsynaptic scaffolding proteins Neural Plast. 2013, 2013, 432057
62. Mabb, A. M.; Ehlers, M. D. Ubiquitination in postsynaptic function and plasticity Annu. Rev. Cell Dev. Biol. 2010, 26, 179-210
63. Tai, H. C.; Besche, H.; Goldberg, A. L.; Schuman, E. M. Characterization of the brain 26S proteasome and its interacting proteins Front Mol. Neurosci. 2010, 3, 1-19
64. Rigaut, G.; Shevchenko, A.; Rutz, B.; Wilm, M.; Mann, M.; Seraphin, B. A generic protein purification method for protein complex characterization and proteome exploration Nat. Biotechnol. 1999, 17, 1030-2
65. Hikita, T.; Taya, S.; Fujino, Y.; Taneichi-Kuroda, S.; Ohta, K.; Tsuboi, D.; Shinoda, T.; Kuroda, K.; Funahashi, Y.; Uraguchi-Asaki, J.; Hashimoto, R.; Kaibuchi, K. Proteomic analysis reveals novel binding partners of dysbindin, a schizophrenia-related protein J. Neurochem. 2009, 110, 1567-74
66. Kim, H. G.; Ahn, J. W.; Kurth, I.; Ullmann, R.; Kim, H. T.; Kulharya, A.; Ha, K. S.; Itokawa, Y.; Meliciani, I.; Wenzel, W.; Lee, D.; Rosenberger, G.; Ozata, M.; Bick, D. P.; Sherins, R. J.; Nagase, T.; Tekin, M.; Kim, S. H.; Kim, C. H.; Ropers, H. H.; Gusella, J. F.; Kalscheuer, V.; Choi, C. Y.; Layman, L. C. WDR11, a WD protein that interacts with transcription factor EMX1, is mutated in idiopathic hypogonadotropic hypogonadism and Kallmann syndrome Am. J. Hum. Genet. 2010, 87, 465-79