Disrupted in schizophrenia 1 and synaptic function in the mammalian central nervous system

European Journal of Neuroscience

Volumn 39, Issue 7, 2014, Pages 1068-1073

  Randall, Andrew D ^a,b   Kurihara, Mai ^a   Brandon, Nicholas J ^c   Brown, Jon T ^b  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b UNIVERSITY OF EXETER   (United Kingdom)

^c ASTRAZENECA   (United Kingdom)

Author keywords

Elecrtophysiology; Neurophysiology; Psychiatric genetics; Synaptic physiology; Synaptic plasticity

Indexed keywords

DISRUPTED IN SCHIZOPHRENIA 1 PROTEIN; DISC1 PROTEIN, HUMAN; NERVE PROTEIN;

ANIMAL BEHAVIOR; ARTICLE; CENTRAL NERVOUS SYSTEM; CHROMOSOME TRANSLOCATION; GENE FUNCTION; HUMAN; MAMMAL; MENTAL DISEASE; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN ASSEMBLY; SYNAPSE; ANIMAL; BRAIN CORTEX; GENETICS; HIPPOCAMPUS; METABOLISM; SYNAPTIC TRANSMISSION;

ANIMALS; CEREBRAL CORTEX; HIPPOCAMPUS; HUMANS; MENTAL DISORDERS; NERVE TISSUE PROTEINS; SYNAPTIC TRANSMISSION;

EID: 84898732566     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.12500     Document Type: Article

References (61)

1. Arenkiel, B.R. & Ehlers, M.D. (2009) Molecular genetics and imaging technologies for circuit-based neuroanatomy. Nature, 461, 900-907.
2. Atkin, T.A., MacAskill, A.F., Brandon, N.J. & Kittler, J.T. (2011) Disrupted in Schizophrenia-1 regulates intracellular trafficking of mitochondria in neurons. Mol. Psychiatr., 16, 122-124, 121.
3. Austin, C.P., Ky, B., Ma, L., Morris, J.A. & Shughrue, P.J. (2004) Expression of Disrupted-In-Schizophrenia-1, a schizophrenia-associated gene, is prominent in the mouse hippocampus throughout brain development. Neuroscience, 124, 3-10.
4. Blackwood, D.H., Fordyce, A., Walker, M.T., St Clair, D.M., Porteous, D.J. & Muir, W.J. (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. Booth, C.A., Brown, J.T. & Randall, A.D. (2014) Neurophysiological modification of CA1 pyramidal neurons in a transgenic mouse expressing a truncated form of disrupted-in-schizophrenia 1. Eur. J. Neurosci., 39, 1074-1090.
6. Brandon, N.J. (2007) Dissecting DISC1 function through protein-protein interactions. Biochem. Soc. T., 35, 1283-1286.
7. Brandon, N.J. & Sawa, A. (2011) Linking neurodevelopmental and synaptic theories of mental illness through DISC1. Nat. Rev. Neurosci., 12, 707-722.
8. Brandon, N.J., Handford, E.J., Schurov, I., Rain, J.C., Pelling, M., Duran-Jimeniz, B., Camargo, L.M., Oliver, K.R., Beher, D., Shearman, M.S. & Whiting, P.J. (2004) Disrupted in Schizophrenia 1 and Nudel form a neurodevelopmentally regulated protein complex: implications for schizophrenia and other major neurological disorders. Mol. Cell. Neurosci., 25, 42-55.
9. Camargo, L.M., Collura, V., Rain, J.C., Mizuguchi, K., Hermjakob, H., Kerrien, S., Bonnert, T.P., Whiting, P.J. & Brandon, N.J. (2007) Disrupted in Schizophrenia 1 Interactome: evidence for the close connectivity of risk genes and a potential synaptic basis for schizophrenia. Mol. Psychiatr., 12, 74-86.
10. Carlisle, H.J., Luong, T.N., Medina-Marino, A., Schenker, L., Khorosheva, E., Indersmitten, T., Gunapala, K.M., Steele, A.D., O'Dell, T.J., Patterson, P.H. & Kennedy, M.B. (2011) Deletion of densin-180 results in abnormal behaviors associated with mental illness and reduces mGluR5 and DISC1 in the postsynaptic density fraction. J. Neurosci., 31, 16194-16207.
11. Clapcote, S.J. & Roder, J.C. (2006) Deletion polymorphism of Disc1 is common to all 129 mouse substrains: implications for gene-targeting studies of brain function. Genetics, 173, 2407-2410.
12. Clapcote, S.J., Lipina, T.V., Millar, J.K., Mackie, S., Christie, S., Ogawa, F., Lerch, J.P., Trimble, K., Uchiyama, M., Sakuraba, Y., Kaneda, H., Shiroishi, T., Houslay, M.D., Henkelman, R.M., Sled, J.G., Gondo, Y., Porteous, D.J. & Roder, J.C. (2007) Behavioral phenotypes of Disc1 missense mutations in mice. Neuron, 54, 387-402.
13. Cuthbert, B. & Insel, T. (2010) The data of diagnosis: new approaches to psychiatric classification. Psychiatry, 73, 311-314.
14. Duan, X., Chang, J.H., Ge, S., Faulkner, R.L., Kim, J.Y., Kitabatake, Y., Liu, X.B., Yang, C.H., Jordan, J.D., Ma, D.K., Liu, C.Y., Ganesan, S., Cheng, H.J., Ming, G.L., Lu, B. & Song, H. (2007) Disrupted-In-Schizophrenia 1 regulates integration of newly generated neurons in the adult brain. Cell, 130, 1146-1158.
15. Enomoto, A., Asai, N., Namba, T., Wang, Y., Kato, T., Tanaka, M., Tatsumi, H., Taya, S., Tsuboi, D., Kuroda, K., Kaneko, N., Sawamoto, K., Miyamoto, R., Jijiwa, M., Murakumo, Y., Sokabe, M., Seki, T., Kaibuchi, K. & Takahashi, M. (2009) Roles of disrupted-in-schizophrenia 1-interacting protein girdin in postnatal development of the dentate gyrus. Neuron, 63, 774-787.
16. Eykelenboom, J.E., Briggs, G.J., Bradshaw, N.J., Soares, D.C., Ogawa, F., Christie, S., Malavasi, E.L., Makedonopoulou, P., Mackie, S., Malloy, M.P., Wear, M.A., Blackburn, E.A., Bramham, J., McIntosh, A.M., Blackwood, D.H., Muir, W.J., Porteous, D.J. & Millar, J.K. (2012) A t(1;11) translocation linked to schizophrenia and affective disorders gives rise to aberrant chimeric DISC1 transcripts that encode structurally altered, deleterious mitochondrial proteins. Hum. Mol. Genet., 21, 3374-3386.
17. Faulkner, R.L., Jang, M.H., Liu, X.B., Duan, X., Sailor, K.A., Kim, J.Y., Ge, S., Jones, E.G., Ming, G.L., Song, H. & Cheng, H.J. (2008) Development of hippocampal mossy fiber synaptic outputs by new neurons in the adult brain. Proc. Natl. Acad. Sci. USA, 105, 14157-14162.
18. Flores, R. 3rd, Hirota, Y., Armstrong, B., Sawa, A. & Tomoda, T. (2011) DISC1 regulates synaptic vesicle transport via a lithium-sensitive pathway. Neurosci. Res., 71, 71-77.
19. Hayashi-Takagi, A., Takaki, M., Graziane, N., Seshadri, S., Murdoch, H., Dunlop, A.J., Makino, Y., Seshadri, A.J., Ishizuka, K., Srivastava, D.P., Xie, Z., Baraban, J.M., Houslay, M.D., Tomoda, T., Brandon, N.J., Kamiya, A., Yan, Z., Penzes, P. & Sawa, A. (2010) Disrupted-in-Schizophrenia 1 (DISC1) regulates spines of the glutamate synapse via Rac1. Nat. Neurosci., 13, 327-332.
20. 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.
21. Holley, S.M., Wang, E.A., Cepeda, C., Jentsch, J.D., Ross, C.A., Pletnikov, M.V. & Levine, M.S. (2013) Frontal cortical synaptic communication is abnormal in Disc1 genetic mouse models of schizophrenia. Schizophr. Res., 146, 264-272.
22. Jacobs, P.A., Aitken, J., Frackiewicz, A., Law, P., Newton, M.S. & Smith, P.G. (1970) The inheritance of translocations in man: data from families ascertained through a balanced heterozygote. Ann. Hum. Genet., 34, 119-136.
23. Kamiya, A., Kubo, K., Tomoda, T., Takaki, M., Youn, R., Ozeki, Y., Sawamura, N., Park, U., Kudo, C., Okawa, M., Ross, C.A., Hatten, M.E., Nakajima, K. & Sawa, A. (2005) A schizophrenia-associated mutation of DISC1 perturbs cerebral cortex development. Nat. Cell Biol., 7, 1167-1178.
24. Kang, E., Burdick, K.E., Kim, J.Y., Duan, X., Guo, J.U., Sailor, K.A., Jung, D.E., Ganesan, S., Choi, S., Pradhan, D., Lu, B., Avramopoulos, D., Christian, K., Malhotra, A.K., Song, H. & Ming, G.L. (2011) Interaction between FEZ1 and DISC1 in regulation of neuronal development and risk for schizophrenia. Neuron, 72, 559-571.
25. Katsel, P., Tan, W., Abazyan, B., Davis, K.L., Ross, C., Pletnikov, M. & Haroutunian, V. (2011) Expression of mutant human DISC1 in mice supports abnormalities in differentiation of oligodendrocytes. Schizophr. Res., 130, 238-249.
26. Kim, J.Y., Duan, X., Liu, C.Y., Jang, M.H., Guo, J.U., Pow-anpongkul, N., Kang, E., Song, H. & Ming, G.L. (2009) DISC1 regulates new neuron development in the adult brain via modulation of AKT-mTOR signaling through KIAA1212. Neuron, 63, 761-773.
27. Kirkpatrick, B., Xu, L., Cascella, N., Ozeki, Y., Sawa, A. & Roberts, R.C. (2006) DISC1 immunoreactivity at the light and ultrastructural level in the human neocortex. J. Comp. Neurol., 497, 436-450.
28. Koike, H., Arguello, P.A., Kvajo, M., Karayiorgou, M. & Gogos, J.A. (2006) Disc1 is mutated in the 129S6/SvEv strain and modulates working memory in mice. Proc. Natl. Acad. Sci. USA, 103, 3693-3697.
29. Korth, C. (2012) Aggregated proteins in schizophrenia and other chronic mental illnesses: DISCopathies. Prion, 6, 134-141.
30. Kubo, K., Tomita, K., Uto, A., Kuroda, K., Seshadri, S., Cohen, J., Kaibuchi, K., Kamiya, A. & Nakajima, K. (2010) Migration defects by DISC1 knockdown in C57BL/6, 129X1/SvJ, and ICR strains via in utero gene transfer and virus-mediated RNAi. Biochem. Bioph. Res. Co., 400, 631-637.
31. Kuroda, K., Yamada, S., Tanaka, M., Iizuka, M., Yano, H., Mori, D., Tsuboi, D., Nishioka, T., Namba, T., Iizuka, Y., Kubota, S., Nagai, T., Ibi, D., Wang, R., Enomoto, A., Isotani-Sakakibara, M., Asai, N., Kimura, K., Kiyonari, H., Abe, T., Mizoguchi, A., Sokabe, M., Takahashi, M., Yamada, K. & Kaibuchi, K. (2011) Behavioral alterations associated with targeted disruption of exons 2 and 3 of the Disc1 gene in the mouse. Hum. Mol. Genet., 20, 4666-4683.
32. Kvajo, M., McKellar, H., Arguello, P.A., Drew, L.J., Moore, H., MacDermott, A.B., Karayiorgou, M. & Gogos, J.A. (2008) A mutation in mouse Disc1 that models a schizophrenia risk allele leads to specific alterations in neuronal architecture and cognition. Proc. Natl. Acad. Sci. USA, 105, 7076-7081.
33. Kvajo, M., McKellar, H., Drew, L.J., Lepagnol-Bestel, A.M., Xiao, L., Levy, R.J., Blazeski, R., Arguello, P.A., Lacefield, C.O., Mason, C.A., Simonneau, M., O'Donnell, J.M., MacDermott, A.B., Karayiorgou, M. & Gogos, J.A. (2011) Altered axonal targeting and short-term plasticity in the hippocampus of Disc1 mutant mice. Proc. Natl. Acad. Sci. USA, 108, E1349-E1358.
34. Li, W., Zhou, Y., Jentsch, J.D., Brown, R.A., Tian, X., Ehninger, D., Hennah, W., Peltonen, L., Lonnqvist, J., Huttunen, M.O., Kaprio, J., Trachtenberg, J.T., Silva, A.J. & Cannon, T.D. (2007) Specific developmental disruption of disrupted-in-schizophrenia-1 function results in schizophrenia-related phenotypes in mice. Proc. Natl. Acad. Sci. USA, 104, 18280-18285.
35. Ma, T.M., Abazyan, S., Abazyan, B., Nomura, J., Yang, C., Seshadri, S., Sawa, A., Snyder, S.H. & Pletnikov, M.V. (2013) Pathogenic disruption of DISC1-serine racemase binding elicits schizophrenia-like behavior via D-serine depletion. Mol. Psychiatr., 18, 557-567.
36. MacLaren, E.J., Charlesworth, P., Coba, M.P. & Grant, S.G. (2011) Knockdown of mental disorder susceptibility genes disrupts neuronal network physiology in vitro. Mol. Cell. Neurosci., 47, 93-99.
37. Maher, B.J. & LoTurco, J.J. (2012) Disrupted-in-schizophrenia (DISC1) functions presynaptically at glutamatergic synapses. PLoS One, 7, e34053.
38. Meyer, K.D. & Morris, J.A. (2009) Disc1 regulates granule cell migration in the developing hippocampus. Hum. Mol. Genet., 18, 3286-3297.
39. Millar, J.K., Wilson-Annan, J.C., Anderson, S., Christie, S., Taylor, M.S., Semple, C.A., Devon, R.S., St Clair, D.M., Muir, W.J., Blackwood, D.H. & Porteous, D.J. (2000) Disruption of two novel genes by a translocation co-segregating with schizophrenia. Hum. Mol. Genet., 9, 1415-1423.
40. Moffitt, T.E., Caspi, A. & Rutter, M. (2005) Strategy for investigating interactions between measured genes and measured environments. Arch. Gen. Psychiat., 62, 473-481.
41. Muir, W.J., Pickard, B.S. & Blackwood, D.H. (2008) Disrupted-in-Schizophrenia-1. Curr. Psychiatry Rep., 10, 140-147.
42. Nakata, K., Lipska, B.K., Hyde, T.M., Ye, T., Newburn, E.N., Morita, Y., Vakkalanka, R., Barenboim, M., Sei, Y., Weinberger, D.R. & Kleinman, J.E. (2009) DISC1 splice variants are upregulated in schizophrenia and associated with risk polymorphisms. Proc. Natl. Acad. Sci. USA, 106, 15873-15878.
43. Narayanan, S., Arthanari, H., Wolfe, M.S. & Wagner, G. (2011) Molecular characterization of disrupted in schizophrenia-1 risk variant S704C reveals the formation of altered oligomeric assembly. J. Biol. Chem., 286, 44266-44276.
44. Niwa, M., Kamiya, A., Murai, R., Kubo, K., Gruber, A.J., Tomita, K., Lu, L., Tomisato, S., Jaaro-Peled, H., Seshadri, S., Hiyama, H., Huang, B., Kohda, K., Noda, Y., O'Donnell, P., Nakajima, K., Sawa, A. & Nabeshima, T. (2010) Knockdown of DISC1 by in utero gene transfer disturbs postnatal dopaminergic maturation in the frontal cortex and leads to adult behavioral deficits. Neuron, 65, 480-489.
45. van Os, J., Kenis, G. & Rutten, B.P. (2010) The environment and schizophrenia. Nature, 468, 203-212.
46. Owen, M.J., Craddock, N. & Jablensky, A. (2007) The genetic deconstruction of psychosis. Schizophrenia Bull., 33, 905-911.
47. Owen, M.J., O'Donovan, M.C., Thapar, A. & Craddock, N. (2011) Neurodevelopmental hypothesis of schizophrenia. Brit. J. Psychiat., 198, 173-175.
48. Paspalas, C.D., Wang, M. & Arnsten, A.F. (2013) Constellation of HCN channels and cAMP regulating proteins in dendritic spines of the primate prefrontal cortex: potential substrate for working memory deficits in schizophrenia. Cereb. Cortex, 23, 1643-1654.
49. Pletnikov, M.V., Ayhan, Y., Nikolskaia, O., Xu, Y., Ovanesov, M.V., Huang, H., Mori, S., Moran, T.H. & Ross, C.A. (2008) Inducible expression of mutant human DISC1 in mice is associated with brain and behavioral abnormalities reminiscent of schizophrenia. Mol. Psychiatr., 13, 173-186, 115.
50. Ritchie, D.J. & Clapcote, S.J. (2013) Disc1 deletion is present in Swiss-derived inbred mouse strains: implications for transgenic studies of learning and memory. Lab Animal, 47, 162-167.
51. Schurov, I.L., Handford, E.J., Brandon, N.J. & Whiting, P.J. (2004) Expression of disrupted in schizophrenia 1 (DISC1) protein in the adult and developing mouse brain indicates its role in neurodevelopment. Mol. Psychiatr., 9, 1100-1110.
52. Seshadri, S., Kamiya, A., Yokota, Y., Prikulis, I., Kano, S., Hayashi-Takagi, A., Stanco, A., Eom, T.Y., Rao, S., Ishizuka, K., Wong, P., Korth, C., Anton, E.S. & Sawa, A. (2010) Disrupted-in-Schizophrenia-1 expression is regulated by beta-site amyloid precursor protein cleaving enzyme-1-neuregulin cascade. Proc. Natl. Acad. Sci. USA, 107, 5622-5627.
53. Shen, S., Lang, B., Nakamoto, C., Zhang, F., Pu, J., Kuan, S.L., Chatzi, C., He, S., Mackie, I., Brandon, N.J., Marquis, K.L., Day, M., Hurko, O., McCaig, C.D., Riedel, G. & St Clair, D. (2008) Schizophrenia-related neural and behavioral phenotypes in transgenic mice expressing truncated Disc1. J. Neurosci., 28, 10893-10904.
54. St Clair, D., Blackwood, D., Muir, W., Carothers, A., Walker, M., Spowart, G., Gosden, C. & Evans, H.J. (1990) Association within a family of a balanced autosomal translocation with major mental illness. Lancet, 336, 13-16.
55. Taya, S., Shinoda, T., Tsuboi, D., Asaki, J., Nagai, K., Hikita, T., Kuroda, S., Kuroda, K., Shimizu, M., Hirotsune, S., Iwamatsu, A. & Kaibuchi, K. (2007) DISC1 regulates the transport of the NUDEL/LIS1/14-3-3epsilon complex through kinesin-1. J. Neurosci., 27, 15-26.
56. Thomson, P.A., Malavasi, E.L., Grunewald, E., Soares, D.C., Borkowska, M. & Millar, J.K. (2013) DISC1 genetics, biology and psychiatric illness. Front. Biol., 8, 1-31.
57. Tomita, K., Kubo, K., Ishii, K. & Nakajima, K. (2011) Disrupted-in-Schizophrenia-1 (Disc1) is necessary for migration of the pyramidal neurons during mouse hippocampal development. Hum. Mol. Genet., 20, 2834-2845.
58. Tsuang, M. (2000) Schizophrenia: genes and environment. Biol. Psychiat., 47, 210-220.
59. Wang, Q., Charych, E.I., Pulito, V.L., Lee, J.B., Graziane, N.M., Crozier, R.A., Revilla-Sanchez, R., Kelly, M.P., Dunlop, A.J., Murdoch, H., Taylor, N., Xie, Y., Pausch, M., Hayashi-Takagi, A., Ishizuka, K., Seshadri, S., Bates, B., Kariya, K., Sawa, A., Weinberg, R.J., Moss, S.J., Houslay, M.D., Yan, Z. & Brandon, N.J. (2011) The psychiatric disease risk factors DISC1 and TNIK interact to regulate synapse composition and function. Mol. Psychiatr., 16, 1006-1023.
60. Wei, J., Graziane, N.M., Wang, H., Zhong, P., Wang, Q., Liu, W., Hayashi-Takagi, A., Korth, C., Sawa, A., Brandon, N.J. & Yan, Z. (2014) Regulation of N-methyl-D-aspartate receptors by Disrupted-in-Schizophrenia-1. Biol. Psychiat., 75, 414-424.
61. Williams, H.J., Owen, M.J. & O'Donovan, M.C. (2009) Schizophrenia genetics: new insights from new approaches. Brit. Med. Bull., 91, 61-74.