Misassembly of full-length Disrupted-in-Schizophrenia 1 protein is linked to altered dopamine homeostasis and behavioral deficits

Molecular Psychiatry

Volumn 21, Issue 11, 2016, Pages 1561-1572

  Trossbach, S V ^a   Bader, V ^a   Hecher, L ^a   Pum, M E ^a   Masoud, S T ^b   Prikulis, I ^a   Schable S ^a   De Souza Silva, M A ^a   Su, P ^c   Boulat, B ^d   Chwiesko, C ^d   Poschmann, G ^a   Stuhler K ^a   Lohr, K M ^e   Stout, K A ^e   Oskamp, A ^f   Godsave, S F ^g   Muller Schiffmann A ^a   Bilzer, T ^a   Steiner, H ^h   Peters, P J ^g,j   Bauer, A ^f   Sauvage, M ^d   Ramsey, A J ^b   Miller, G W ^e   Liu, F ^c   Seeman, P ^b   Brandon, N J ⁱ   Huston, J P ^a   Korth, C ^a   more..

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b UNIVERSITY OF TORONTO   (Canada)

^c CENTRE FOR ADDICTION AND MENTAL HEALTH   (Canada)

^d RUHR UNIVERSITY BOCHUM   (Germany)

^e EMORY UNIVERSITY   (United States)

^f FORSCHUNGSZENTRUM JÜLICH   (Germany)

^g NETHERLANDS CANCER INSTITUTE   (Netherlands)

^h ROSALIND FRANKLIN UNIVERSITY OF MEDICINE AND SCIENCE   (United States)

ⁱ ASTRAZENECA   (United Kingdom)

^j MAASTRICHT UNIVERSITY   (Netherlands)

more..

Author keywords

[No Author keywords available]

Indexed keywords

AMPHETAMINE; DEXAMPHETAMINE; DISRUPTED IN SCHIZOPHRENIA 1 PROTEIN; DOPAMINE; DOPAMINE TRANSPORTER; DISC1 PROTEIN, HUMAN; DOPAMINE 2 RECEPTOR; NERVE PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYCLIC POTENTIOMETRY; DOPAMINERGIC TRANSMISSION; DORSAL STRIATUM; IN VITRO STUDY; MENTAL DISEASE; NEUROPATHOLOGY; NEUROTRANSMISSION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PHENOTYPE; PRIORITY JOURNAL; PROTEIN HOMEOSTASIS; RAT; SCHIZOPHRENIA; SUPERSENSITIVITY; SYNAPTIC MEMBRANE; TRANSGENE; TRANSGENIC RAT; WESTERN BLOTTING; ANIMAL; ANIMAL BEHAVIOR; BRAIN; C57BL MOUSE; DISEASE MODEL; GENETICS; HOMEOSTASIS; HUMAN; MALE; METABOLISM; MOUSE; NERVE CELL; PHYSIOLOGY; SPRAGUE DAWLEY RAT; SYNAPTIC TRANSMISSION; TRANSGENIC MOUSE;

AMPHETAMINE; ANIMALS; BEHAVIOR, ANIMAL; BRAIN; DISEASE MODELS, ANIMAL; DOPAMINE; DOPAMINE PLASMA MEMBRANE TRANSPORT PROTEINS; HOMEOSTASIS; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; RATS, TRANSGENIC; RECEPTORS, DOPAMINE D2; SCHIZOPHRENIA; SYNAPTIC TRANSMISSION;

EID: 84954498999     PISSN: 13594184     EISSN: 14765578     Source Type: Journal    
DOI: 10.1038/mp.2015.194     Document Type: Article

References (68)

1. Millar JK, Wilson-Annan JC, Anderson S, Christie S, Taylor MS, Semple CA et al. Disruption of two novel genes by a translocation co-segregating with schizophrenia. Hum Mol Genet 2000; 9: 1415-1423.
2. Blackwood DH, Fordyce A, Walker MT St, Clair DM, Porteous DJ, Muir WJ. 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 2001; 69: 428-433.
3. St Clair D, Blackwood D, Muir W, Carothers A, Walker M, Spowart G et al. Association within a family of a balanced autosomal translocation with major mental illness. Lancet 1990; 336: 13-16.
4. Chubb JE, Bradshaw NJ, Soares DC, Porteous DJ, Millar JK. The DISC locus in psychiatric illness. Mol Psychiatry 2008; 13: 36-64.
5. Bradshaw NJ, Porteous DJ. DISC1-binding proteins in neural development, signalling and schizophrenia. Neuropharmacology 2012; 62: 1230-1241.
6. Leliveld SR, Hendriks P, Michel M, Sajnani G, Bader V, Trossbach S et al. Oligomer assembly of the C-terminal DISC1 domain (640-854) is controlled by self-association motifs and disease-associated polymorphism S704C. Biochemistry 2009; 48: 7746-7755.
7. Narayanan S, Arthanari H, Wolfe MS, Wagner G. Molecular characterization of disrupted in schizophrenia-1 risk variant S704C reveals the formation of altered oligomeric assembly. J Biol Chem 2011; 286: 44266-44276.
8. Clapcote SJ, Lipina TV, Millar JK, Mackie S, Christie S, Ogawa F et al. Behavioral phenotypes of Disc1 missense mutations in mice. Neuron 2007; 54: 387-402.
9. Koike H, Arguello PA, Kvajo M, Karayiorgou M, Gogos JA. Disc1 is mutated in the 129S6/SvEv strain and modulates working memory in mice. Proc Natl Acad Sci USA 2006; 103: 3693-3697.
10. Shen S, Lang B, Nakamoto C, Zhang F, Pu J, Kuan SL et al. Schizophrenia-related neural and behavioral phenotypes in transgenic mice expressing truncated Disc1. J Neurosci 2008; 28: 10893-10904.
11. Kuroda K, Yamada S, Tanaka M, Iizuka M, Yano H, Mori D et al. Behavioral alterations associated with targeted disruption of exons 2 and 3 of the Disc1 gene in the mouse. Hum Mol Genet 2011; 20: 4666-4683.
12. Pletnikov MV, Ayhan Y, Nikolskaia O, Xu Y, Ovanesov MV, Huang H et al. Inducible expression of mutant human DISC1 in mice is associated with brain and behavioral abnormalities reminiscent of schizophrenia. Mol Psychiatry 2008; 13: 115.
13. Hikida T, Jaaro-Peled H, Seshadri S, Oishi K, Hookway C, Kong S et al. Dominant-negative DISC1 transgenic mice display schizophrenia-associated phenotypes detected by measures translatable to humans. Proc Natl Acad Sci USA 2007; 104: 14501-14506.
14. Brandon NJ, Sawa A. Linking neurodevelopmental and synaptic theories of mental illness through DISC1. Nat Rev Neurosci 2011; 12: 707-722.
15. Porteous DJ, Thomson PA, Millar JK, Evans KL, Hennah W, Soares DC et al. DISC1 as a genetic risk factor for schizophrenia and related major mental illness: response to Sullivan. Mol Psychiatry 2014; 19: 141-143.
16. Sullivan PF. Questions about DISC1 as a genetic risk factor for schizophrenia. Mol Psychiatry 2013; 18: 1050-1052.
17. Bertram L, Lill CM, Tanzi RE. The genetics of Alzheimer disease: back to the future. Neuron 2010; 68: 270-281.
18. Prusiner SB. Shattuck Lecture-neurodegenerative diseases and prions. N Engl J Med 2001; 344: 1516-1526.
19. Greenwald J, Riek R. Biology of amyloid: structure, function, and regulation. Structure 2010; 18: 1244-1260.
20. Leliveld SR, Bader V, Hendriks P, Prikulis I, Sajnani G, Requena JR et al. Insolubility of disrupted-in-schizophrenia 1 disrupts oligomer-dependent interactions with nuclear distribution element 1 and is associated with sporadic mental disease. J Neurosci 2008; 28: 3839-3845.
21. Ottis P, Bader V, Trossbach S, Kretzschmar H, Michel M, Leliveld SR et al. Convergence of two independent mental disease genes on the protein level: recruitment of dysbindin to cell invasive DISC1 aggresomes. Biol Psychiatry 2011; 70: 604-610.
22. Lipina TV, Roder JC. Disrupted-In-Schizophrenia-1 (DISC1) interactome and mental disorders: impact of mouse models. Neurosci Biobehav Rev 2014; 45: 271-294.
23. Lipina TV, Niwa M, Jaaro-Peled H, Fletcher PJ, Seeman P, Sawa A et al. Enhanced dopamine function in DISC1-L100P mutant mice: implications for schizophrenia. Genes Brain Behav 2010; 9: 777-789.
24. Jaaro-Peled H, Niwa M, Foss CA, Murai R, de Los Reyes S, Kamiya A et al. Sub-cortical dopaminergic deficits in a DISC1 mutant model: a study in direct reference to human molecular brain imaging. Hum Mol Genet 2013; 22: 1574-1580.
25. Niwa M, Kamiya A, Murai R, Kubo K, Gruber AJ, Tomita K et al. Knockdown of DISC1 by in utero gene transfer disturbs postnatal dopaminergic maturation in the frontal cortex and leads to adult behavioral deficits. Neuron 2010; 65: 480-489.
26. Ayhan Y, Abazyan B, Nomura J, Kim R, Ladenheim B, Krasnova IN et al. Differential effects of prenatal and postnatal expressions of mutant human DISC1 on neuro-behavioral phenotypes in transgenic mice: evidence for neurodevelopmental origin of major psychiatric disorders. Mol Psychiatry 2011; 16: 293-306.
27. Pogorelov VM, Nomura J, Kim J, Kannan G, Ayhan Y, Yang C et al. Mutant DISC1 affects methamphetamine-induced sensitization and conditioned place preference: a comorbidity model. Neuropharmacology 2012; 62: 1242-1251.
28. Nakai T, Nagai T, Wang R, Yamada S, Kuroda K, Kaibuchi K et al. Alterations of GABAergic and dopaminergic systems in mutant mice with disruption of exons 2 and 3 of the Disc1 gene. Neurochem Int 2014; 74: 74-83.
29. Su P, Li S, Chen S, Lipina TV, Wang M, Lai TK et al. A dopamine D2 receptor-DISC1 protein complex may contribute to antipsychotic-like effects. Neuron 2014; 84: 1302-1316.
30. Scott MR, Kohler R, Foster D, Prusiner SB. Chimeric prion protein expression in cultured cells and transgenic mice. Protein Sci 1992; 1: 986-997.
31. Masoud ST, Vecchio LM, Bergeron Y, Hossain MM, Nguyen LT, Bermejo MK et al. Increased expression of the dopamine transporter leads to loss of dopamine neurons, oxidative stress and l-DOPA reversible motor deficits. Neurobiol Dis 2015; 74: 66-75.
32. Salahpour A, Ramsey AJ, Medvedev IO, Kile B, Sotnikova TD, Holmstrand E et al. Increased amphetamine-induced hyperactivity and reward in mice overexpressing the dopamine transporter. Proc Natl Acad Sci USA 2008; 105: 4405-4410.
33. Caudle WM, Richardson JR, Wang MZ, Taylor TN, Guillot TS, McCormack AL et al. Reduced vesicular storage of dopamine causes progressive nigrostriatal neuro-degeneration. J Neurosci 2007; 27: 8138-8148.
34. Mooslehner KA, Chan PM, Xu W, Liu L, Smadja C, Humby T et al. Mice with very low expression of the vesicular monoamine transporter 2 gene survive into adulthood: potential mouse model for parkinsonism. Mol Cell Biol 2001; 21: 5321-5331.
35. Bermejo MK, Milenkovic M, Salahpour A, Ramsey AJ. Preparation of synaptic plasma membrane and postsynaptic density proteins using a discontinuous sucrose gradient. J Vis Exp 2014; 91: e51896.
36. Ramsey AJ, Milenkovic M, Oliveira AF, Escobedo-Lozoya Y, Seshadri S, Salahpour A et al. Impaired NMDA receptor transmission alters striatal synapses and DISC1 protein in an age-dependent manner. Proc Natl Acad Sci USA 2011; 108: 5795-5800.
37. Seeman P, Guan HC. Glutamate agonist LY404,039 for treating schizophrenia has affinity for the dopamine D2(High) receptor. Synapse 2009; 63: 935-939.
38. Shuto T, Seeman P, Kuroiwa M, Nishi A. Repeated administration of a dopamine D1 receptor agonist reverses the increased proportions of striatal dopamine D1High and D2High receptors in methamphetamine-sensitized rats. Eur J Neurosci 2008; 27: 2551-2557.
39. Pum ME, Schable S, Harooni HE, Topic B, De Souza Silva MA, Li JS et al. Effects of intranasally applied dopamine on behavioral asymmetries in rats with unilateral 6-hydroxydopamine lesions of the nigro-striatal tract. Neuroscience 2009; 162: 174-183.
40. Peters PJ, Bos E, Griekspoor A. Cryo-immunogold electron microscopy. Curr Protoc Cell Biol 2006; Chapter 4: Unit 47.
41. Wang Q, Charych EI, Pulito VL, Lee JB, Graziane NM, Crozier RA et al. The psychiatric disease risk factors DISC1 and TNIK interact to regulate synapse composition and function. Mol Psychiatry 2011; 16: 1006-1023.
42. Torrey EF, Webster M, Knable M, Johnston N, Yolken RH. The stanley foundation brain collection and neuropathology consortium. Schizophr Res 2000; 44: 151-155.
43. Johnstone M, Thomson PA, Hall J, McIntosh AM, Lawrie SM, Porteous DJ. DISC1 in schizophrenia: genetic mouse models and human genomic imaging. Schizophr Bull 2011; 37: 14-20.
44. Seshadri S, Kamiya A, Yokota Y, Prikulis I, Kano S, Hayashi-Takagi A et al. Disrupted-in-Schizophrenia-1 expression is regulated by beta-site amyloid precursor protein cleaving enzyme-1-neuregulin cascade. Proc Natl Acad Sci USA 2010; 107: 5622-5627.
45. Hsiao KK, Borchelt DR, Olson K, Johannsdottir R, Kitt C, Yunis W et al. Age-related CNS disorder and early death in transgenic FVB/N mice overexpressing Alzheimer amyloid precursor proteins. Neuron 1995; 15: 1203-1218.
46. Chishti MA, Yang DS, Janus C, Phinney AL, Horne P, Pearson J et al. Early-onset amyloid deposition and cognitive deficits in transgenic mice expressing a double mutant form of amyloid precursor protein 695. J Biol Chem 2001; 276: 21562-21570.
47. Manson J, West JD, Thomson V, McBride P, Kaufman MH, Hope J. The prion protein gene: a role in mouse embryogenesis? Development 1992; 115: 117-122.
48. Schurov IL, Handford EJ, Brandon NJ, Whiting PJ. Expression of disrupted in schizophrenia 1 (DISC1) protein in the adult and developing mouse brain indicates its role in neurodevelopment. Mol Psychiatry 2004; 9: 1100-1110.
49. Nakata K, Lipska BK, Hyde TM, Ye T, Newburn EN, Morita Y et al. DISC1 splice variants are upregulated in schizophrenia and associated with risk polymorphisms. Proc Natl Acad Sci USA 2009; 106: 15873-15878.
50. van Haren NE, Cahn W, Hulshoff Pol HE, Kahn RS. Schizophrenia as a progressive brain disease. Eur Psychiatry 2008; 23: 245-254.
51. Lieberman JA, Kane JM, Alvir J. Provocative tests with psychostimulant drugs in schizophrenia. Psychopharmacology (Berl) 1987; 91: 415-433.
52. Seeman P, Schwarz J, Chen JF, Szechtman H, Perreault M, McKnight GS et al. Psychosis pathways converge via D2high dopamine receptors. Synapse 2006; 60: 319-346.
53. Seeman P. Schizophrenia and dopamine receptors. Eur Neuropsychopharmacol 2013; 23: 999-1009.
54. Kopito RR. Aggresomes, inclusion bodies and protein aggregation. Trends Cell Biol 2000; 10: 524-530.
55. Levin EC, Acharya NK, Sedeyn JC, Venkataraman V, D'Andrea MR, Wang HY et al. Neuronal expression of vimentin in the Alzheimer's disease brain may be part of a generalized dendritic damage-response mechanism. Brain Res 2009; 1298: 194-207.
56. Soderberg O, Gullberg M, Jarvius M, Ridderstrale K, Leuchowius KJ, Jarvius J et al. Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat Methods 2006; 3: 995-1000.
57. Featherstone RE, Kapur S, Fletcher PJ. The amphetamine-induced sensitized state as a model of schizophrenia. Prog Neuropsychopharmacol Biol Psychiatry 2007; 31: 1556-1571.
58. Kahlig KM, Galli A. Regulation of dopamine transporter function and plasma membrane expression by dopamine, amphetamine, and cocaine. Eur J Pharmacol 2003; 479: 153-158.
59. Blancas-Mejia LM, Ramirez-Alvarado M. Systemic amyloidoses. Annu Rev Biochem 2013; 82: 745-774.
60. Si K, Choi YB, White-Grindley E, Majumdar A, Kandel ER. Aplysia CPEB can form prion-like multimers in sensory neurons that contribute to long-term facilitation. Cell 2010; 140: 421-435.
61. Korth C. DISCopathies: brain disorders related to DISC1 dysfunction. Rev Neurosci 2009; 20: 321-330.
62. Kravitz AV, Freeze BS, Parker PR, Kay K, Thwin MT, Deisseroth K et al. Regulation of parkinsonian motor behaviours by optogenetic control of basal ganglia circuitry. Nature 2010; 466: 622-626.
63. Calabresi P, Picconi B, Tozzi A, Ghiglieri V, Di Filippo M. Direct and indirect pathways of basal ganglia: a critical reappraisal. Nat Neurosci 2014; 17: 1022-1030.
64. Cazorla M, de Carvalho FD, Chohan MO, Shegda M, Chuhma N, Rayport S et al. Dopamine D2 receptors regulate the anatomical and functional balance of basal ganglia circuitry. Neuron 2014; 81: 153-164.
65. Surmeier DJ, Ding J, Day M, Wang Z, Shen W. D1 and D2 dopamine-receptor modulation of striatal glutamatergic signaling in striatal medium spiny neurons. Trends Neurosci 2007; 30: 228-235.
66. Simpson EH, Kellendonk C, Kandel E. A possible role for the striatum in the pathogenesis of the cognitive symptoms of schizophrenia. Neuron 2010; 65: 585-596.
67. Durieux PF, Schiffmann SN, de Kerchove d'Exaerde A. Differential regulation of motor control and response to dopaminergic drugs by D1R and D2R neurons in distinct dorsal striatum subregions. EMBO J 2012; 31: 640-653.
68. Sulzer D, Chen TK, Lau YY, Kristensen H, Rayport S, Ewing A. Amphetamine redistributes dopamine from synaptic vesicles to the cytosol and promotes reverse transport. J Neurosci 1995; 15: 4102-4108.