Insolubility of disrupted-in-schizophrenia 1 disrupts oligomer-dependent interactions with nuclear distribution element 1 and is associated with sporadic mental disease

Journal of Neuroscience

Volumn 28, Issue 15, 2008, Pages 3839-3845

  Leliveld, S Rutger ^a,b   Bader, Verian ^a   Hendriks, Philipp ^a   Prikulis, Ingrid ^a   Sajnani, Gustavo ^c   Requena, Jesús R ^c   Korth, Carsten ^a  

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b FORSCHUNGSZENTRUM JÜLICH   (Germany)

^c UNIVERSITY OF SANTIAGO DE COMPOSTELA   (Spain)

Author keywords

Bipolar disorder; Depression; Multimerization; Protein aggregation; Protein conformational disease; Psychiatric disease

Indexed keywords

DIMER; DISRUPTED IN SCHIZOPHRENIA 1 PROTEIN; LIGAND; NUCLEAR DISTRIBUTION ELEMENT LIKE PROTEIN; OLIGOMER; POLYMER; PROTEIN; UNCLASSIFIED DRUG; CARRIER PROTEIN; DISC1 PROTEIN, HUMAN; NDEL1 PROTEIN, HUMAN; NERVE PROTEIN; PROTEOME; RECOMBINANT PROTEIN;

ANIMAL TISSUE; ARTICLE; AUTOPSY; CONTROLLED STUDY; ESCHERICHIA COLI; GENE EXPRESSION; HUMAN; HUMAN CELL; LIGAND BINDING; MENTAL DISEASE; MOLECULAR GENETICS; MOLECULAR INTERACTION; MOLECULAR WEIGHT; MOOD DISORDER; MOUSE; NEUROBLASTOMA CELL; NONHUMAN; OLIGOMERIZATION; PHENOTYPE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN EXPRESSION; RECOMBINANT GENE; SCHIZOPHRENIA; SOLUBILITY; ANIMAL; BRAIN LEVEL; CADAVER; CHEMISTRY; DRUG INTERACTION; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; TRANSGENIC MOUSE; TUMOR CELL LINE;

ANIMALS; BRAIN CHEMISTRY; CADAVER; CARRIER PROTEINS; CELL LINE, TUMOR; DRUG INTERACTIONS; ESCHERICHIA COLI; HUMANS; LIGANDS; MICE; MICE, TRANSGENIC; MOOD DISORDERS; NERVE TISSUE PROTEINS; PHENOTYPE; PROTEOME; RECOMBINANT PROTEINS; SCHIZOPHRENIA; SOLUBILITY;

EID: 43049167463     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5389-07.2008     Document Type: Article

References (42)

1. an der Heiden W, Hafner H (2000) The epidemiology of onset and course of schizophrenia. Eur Arch Psych Clin Neurosci 250:292-303.
2. Berrettini W (2003) Evidence for shared susceptibility in bipolar disorder and schizophrenia. Am J Med Genet 123:59-64.
3. Blackwood DH, Muir WJ (2004) Clinical phenotypes associated with DISC1, a candidate gene for schizophrenia. Neurotox Res 6:35-41.
4. Blackwood DH, Fordyce A, Walker MT, St Clair DM, Porteous DJ, Muir WJ (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.
5. Chua SE, McKenna PJ (2000) A skeptical view of the neuropathology of schizophrenia. In: The neuropathology of schizophrenia (Harrison PJ, Roberts GW, eds), pp 291-337. Oxford: Oxford UP.
6. Chubb JE, Bradshaw NJ, Soares DC, Porteous DJ, Millar JK (2008) The DISC locus in psychiatric illness. Mol Psychiatry 13:36-64.
7. Cohen E, Bieschke J, Perciavalle RM, Kelly JW, Dillin A (2006) Opposing activities protect against age-onset proteotoxicity. Science 313:1604-1610.
8. Craddock N, Owen MJ (2007) Rethinking psychosis: the disadvantages of a dichotomous classification now outweigh the advantages. World Psychiatry 6:20-27.
9. Duan X, Chang JH, Ge S, Faulkner RL, Kim JY, Kitabatake Y, Liu XB, Yang CH, Jordan JD, Ma DK, Liu CY, Ganesan S, Cheng HJ, Ming GL, Lu B, Song H (2007) Disrupted-in-schizophrenia 1 regulates integration of newly generated neurons in the adult brain. Cell 130:1146-1158.
10. Franzen B, Yang Y, Sunnemark D, Wickman M, Ottervald J, Oppermann M, Sandberg K (2003) Dihydropyrimidinase related protein-2 as a biomarker for temperature and time dependent post mortem changes in the mouse brain proteome. Proteomics 3:1920-1929.
11. Green EK, Norton N, Peirce T, Grozeva D, Kirov G, Owen MJ, O'Donovan MC, Craddock N (2006) Evidence that a DISC1 frame-shift deletion associated with psychosis in a single family may not be a pathogenic mutation. Mol Psychiatry 11:798-799.
12. Gutekunst CA, Li SH, Yi H, Mulroy JS, Kuemmerle S, Jones R, Rye D, Ferrante RJ, Hersch SM, Li XJ (1999) Nuclear and neuropil aggregates in Huntington's disease: relationship to neuropathology. J Neurosci 19:2522-2534.
13. Harrison PJ, Weinberger DR (2005) Schizophrenia genes, gene expression, and neuropathology: on the matter of their convergence. Mol Psychiatry 10:40-68, image 45.
14. Hikida T, Jaaro-Peled H, Seshadri S, Oishi K, Hookway C, Kong S, Wu D, Xue R, Andrade M, Tankou S, Mori S, Gallagher M, Ishizuka K, Pletnikov M, Kida S, Sawa A (2007) Dominant-negative DISC1 transgenic mice display schizophrenia-associated phenotypes detected by measures translatable to humans. Proc Natl Acad Sci USA 104:14501-14506.
15. Hulshoff Pol HE, Schnack HG, Mandl RC, van Haren NE, Koning H, Collins DL, Evans AC, Kahn RS (2001) Focal gray matter density changes in schizophrenia. Arch Gen Psychiatry 58:1118-1125.
16. Ishizuka K, Paek M, Kamiya A, Sawa A (2006) A review of disrupted-inschizophrenia-1 (DISC1): neurodevelopment, cognition, and mental conditions. Biol Psychiatry 59:1189-1197.
17. James R, Adams RR, Christie S, Buchanan SR, Porteous DJ, Millar JK (2004) Disrupted in schizophrenia 1 (DISC1) is a multicompartmentalized protein that predominantly localizes to mitochondria. Mol Cell Neurosci 26:112-122.
18. Kamiya A, Kubo K, Tomoda T, Takaki M, Youn R, Ozeki Y, Sawamura N, Park U, Kudo C, Okawa M, Ross CA, Hatten ME, Nakajima K, Sawa A (2005) A schizophrenia-associated mutation of DISC1 perturbs cerebral cortex development. Nat Cell Biol 7:1167-1178.
19. Katsel P, Davis KL, Gorman JM, Haroutunian V (2005) Variations in differential gene expression patterns across multiple brain regions in schizophrenia. Schizophr Res 77:241-252.
20. Kuemmerle S, Gutekunst CA, Klein AM, Li XJ, Li SH, Beal MF, Hersch SM, Ferrante RJ (1999) Huntington aggregates may not predict neuronal death in Huntington's disease. Ann Neurol 46:842-849.
21. Law AJ, Shannon Weickert C, Hyde TM, Kleinman JE, Harrison PJ (2004) Neuregulin-1 (NRG-1) mRNA and protein in the adult human brain. Neuroscience 127:125-136.
22. Li W, Zhou Y, Jentsch JD, Brown RA, Tian X, Ehninger D, Hennah W, Peltonen L, Lonnqvist J, Huttunen MO, Kaprio J, Trachtenberg JT, Silva AJ, Cannon TD (2007) Specific developmental disruption of disruptedin-schizophrenia- 1 function results in schizophrenia-related phenotypes in mice. Proc Natl Acad Sci USA 104:18280-18285.
23. Li XJ, Li SH, Sharp AH, Nucifora Jr FC, Schilling G, Lanahan A, Worley P, Snyder SH, Ross CA (1995) A huntingtin-associated protein enriched in brain with implications for pathology. Nature 378:398-402.
24. Mangiarini L, Sathasivam K, Seller M, Cozens B, Harper A, Hetherington C, Lawton M, Trottier Y, Lehrach H, Davies SW, Bates GP (1996) Exon 1 of the HD gene with an expanded CAG repeat is sufficient to cause a progressive neurological phenotype in transgenic mice. Cell 87:493-506.
25. McDonald C, Bullmore ET, Sham PC, Chitnis X, Wickham H, Bramon E, Murray RM (2004) Association of genetic risks for schizophrenia and bipolar disorder with specific and generic brain structural endophenotypes. Arch Gen Psychiatry 61:974-984.
26. Millar JK, Wilson-Annan JC, Anderson S, Christie S, Taylor MS, Semple CA, Devon RS, Clair DM, Muir WJ, Blackwood DH, Porteous DJ (2000) Disruption of two novel genes by a translocation co-segregating with schizophrenia. Hum Mol Genet 9:1415-1423.
27. Millar JK, Pickard BS, Mackie S, James R, Christie S, Buchanan SR, Malloy MP, Chubb JE, Huston E, Baillie GS, Thomson PA, Hill EV, Brandon NJ, Rain JC, Camargo LM, Whiting PJ, Houslay MD, Blackwood DH, Muir WJ, Porteous DJ (2005) DISC1 and PDE4B are interacting genetic factors in schizophrenia that regulate cAMP signaling. Science 310:1187-1191.
28. Narr KL, Toga AW, Szeszko P, Thompson PM, Woods RP, Robinson D, Sevy S, Wang Y, Schrock K, Bilder RM (2005) Cortical thinning in cingulate and occipital cortices in first episode schizophrenia. Biol Psychiatry 58:32-40.
29. Nguyen MD, Shu T, Sanada K, Lariviere RC, Tseng HC, Park SK, Julien JP, Tsai LH (2004) A NUDEL-dependent mechanism of neurofilament assembly regulates the integrity of CNS neurons. Nat Cell Biol 6:595-608.
30. Owen MJ, Craddock N, Jablensky A (2007) The genetic deconstruction of psychosis. Schizophr Bull 33:905-911.
31. Ozeki Y, Tomoda T, Kleiderlein J, Kamiya A, Bord L, Fujii K, Okawa M, Yamada N, Hatten ME, Snyder SH, Ross CA, Sawa A (2003) Disruptedin- schizophrenia-1 (DISC-1): mutant truncation prevents binding to NudE-like (NUDEL) and inhibits neurite outgrowth. Proc Natl Acad Sci USA 100:289-294.
32. Pletnikov MV, Ayhan Y, Nikolskaia O, Xu Y, Ovanesov MV, Huang H, Mori S, Moran TH, Ross CA (2008) Inducible expression of mutant human DISC1 in mice is associated with brain and behavioral abnormalities reminiscent of schizophrenia. Mol Psychiatry 13:173-186.
33. Prusiner SB (2001) Shattuck lecture-neurodegenerative diseases and prions. N Engl J Med 344:1516-1526.
34. Ross CA, Margolis RL, Reading SA, Pletnikov M, Coyle JT (2006) Neurobiology of schizophrenia. Neuron 52:139-153.
35. Sachs NA, Sawa A, Holmes SE, Ross CA, DeLisi LE, Margolis RL (2005) A frameshift mutation in disrupted in schizophrenia 1 in an American family with schizophrenia and schizoaffective disorder. Mol Psychiatry 10:758-764.
36. Sawamura N, Sawamura-Yamamoto T, Ozeki Y, Ross CA, Sawa A (2005) A form of DISC1 enriched in nucleus: altered subcellular distribution in orbitofrontal cortex in psychosis and substance/alcohol abuse. Proc Natl Acad Sci USA 102:1187-1192.
37. Scherzinger E, Lurz R, Turmaine M, Mangiarini L, Hollenbach B, Hasenbank R, Bates GP, Davies SW, Lehrach H, Wanker EE (1997) Huntingtin-encoded polyglutamine expansions form amyloid-like protein aggregates in vitro and in vivo. Cell 90:549-558.
38. St Clair D, Blackwood D, Muir W, Carothers A, Walker M, Spowart G, Gosden C, Evans HJ (1990) Association within a family of a balanced autosomal translocation with major mental illness. Lancet 336:13-16.
39. Stefansson H, Sigurdsson E, Steinthorsdottir V, Bjornsdottir S, Sigmundsson T, Ghosh S, Brynjolfsson J, Gunnarsdottir S, Ivarsson O, Chou TT, Hjaltason O, Birgisdottir B, Jonsson H, Gudnadottir VG, Gudmundsdottir E, Bjornsson A, Ingvarsson B, Ingason A, Sigfusson S, Hardardottir H, et al. (2002) Neuregulin 1 and susceptibility to schizophrenia. Am J Hum Genet 71:877-892.
40. Taylor JP, Hardy J, Fischbeck KH (2002) Toxic proteins in neurodegenerative disease. Science 296:1991-1995.
41. Torrey EF, Webster M, Knable M, Johnston N, Yolken RH (2000) The Stanley foundation brain collection and neuropathology consortium. Schizophr Res 44:151-155.
42. Trottier Y, Lutz Y, Stevanin G, Imbert G, Devys D, Cancel G, Saudou F, Weber C, David G, Tora L, Agid Y, Brice A, Mandel J-L (1995) Polyglutamine expansion as a pathological epitope in Huntington's disease and four dominant cerebellar ataxias. Nature 378:403-406.