DISC1 variants 37W and 607F disrupt its nuclear targeting and regulatory role in ATF4-mediated transcription

Human Molecular Genetics

Volumn 21, Issue 12, 2012, Pages 2779-2792

  Malavasi, Elise L V ^a   Ogawa, Fumiaki ^a   Porteous, David J ^a   Millar, J Kirsty ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; CYCLIC AMP; DISRUPTED IN SCHIZOPHRENIA 1 PROTEIN;

AMINO ACID SUBSTITUTION; ARTICLE; BEHAVIOR; CELLULAR STRESS RESPONSE; COGNITION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; GENE EXPRESSION; GENETIC REGULATION; GENETIC VARIABILITY; HUMAN; HUMAN CELL; MEMORY CONSOLIDATION; MENTAL DISEASE; PREDICTION; PRIORITY JOURNAL; TRANSCRIPTION REGULATION; WILD TYPE;

ACTIVATING TRANSCRIPTION FACTOR 4; ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; BLOTTING, WESTERN; CELL LINE, TUMOR; CELL NUCLEUS; COS CELLS; HEK293 CELLS; HUMANS; HYBRID CELLS; IMMUNOPRECIPITATION; LUCIFERASES; MICROSCOPY, CONFOCAL; MUTATION; NERVE TISSUE PROTEINS; OLIGODENDROGLIA; PROTEIN BINDING; RHABDOMYOSARCOMA; TRANSCRIPTION, GENETIC; TRANSFECTION;

EID: 84861731674     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/dds106     Document Type: Article

References (79)

1. Chubb, J.E., Bradshaw, N.J., Soares, D.C., Porteous, D.J. and Millar, J.K. (2008) The DISC locus in psychiatric illness. Mol. Psychiatry, 13, 36-64.
2. Bradshaw, N.J. and Porteous, D.J. (2012) DISC1-binding proteins in neural development, signalling and schizophrenia. Neuropharmacology, 31, 9043-9054.
3. Sawamura, N., Ando, T., Maruyama, Y., Fujimuro, M., Mochizuki, H., Honjo, K., Shimoda, M., Toda, H., Sawamura-Yamamoto, T., Makuch, L.A. et al. (2008) Nuclear DISC1 regulates CRE-mediated gene transcription and sleep homeostasis in the fruit fly. Mol. Psychiatry, 13, 1138-1148, 1069.
4. Morris, J.A., Kandpal, G., Ma, L. and Austin, C.P. (2003) DISC1 (Disrupted-In-Schizophrenia 1) is a centrosome-associated protein that interacts with MAP1A, MIPT3, ATF4/5 and NUDEL: regulation and loss of interaction with mutation. Hum. Mol. Genet., 12, 1591-1608.
5. Ozeki, Y., Tomoda, T., Kleiderlein, J., Kamiya, A., Bord, L., Fujii, K., Okawa, M., Yamada, N., Hatten, M.E., Snyder, S.H. et al. (2003) Disrupted-in-Schizophrenia-1 (DISC-1): mutant truncation prevents binding to NudE-like (NUDEL) and inhibits neurite outgrowth. Proc. Natl Acad. Sci. USA, 100, 289-294.
6. Millar, J.K., Christie, S. and Porteous, D.J. (2003) Yeast two-hybrid screens implicate DISC1 in brain development and function. Biochem. Biophys. Res. Commun., 311, 1019-1025.
7. Ameri, K. and Harris, A.L. (2008) Activating transcription factor 4. Int. J. Biochem. Cell Biol., 40, 14-21.
8. Dey, S., Baird, T.D., Zhou, D., Palam, L.R., Spandau, D.F. and Wek, R.C. (2010) Both transcriptional regulation and translational control of ATF4 are central to the integrated stress response. J. Biol. Chem., 285, 33165-33174.
9. Fawcett, T.W., Martindale, J.L., Guyton, K.Z., Hai, T. and Holbrook, N.J. (1999) Complexes containing activating transcription factor (ATF)/cAMP-responsive-element-binding protein (CREB) interact with the CCAAT/enhancer-binding protein (C/EBP)-ATF composite site to regulate Gadd153 expression during the stress response. Biochem. J., 339, 135-141.
10. Ohoka, N., Yoshii, S., Hattori, T., Onozaki, K. and Hayashi, H. (2005) TRB3, a novel ER stress-inducible gene, is induced via ATF4-CHOP pathway and is involved in cell death. EMBO J., 24, 1243-1255.
11. Harding, H.P., Zhang, Y., Zeng, H., Novoa, I., Lu, P.D., Calfon, M., Sadri, N., Yun, C., Popko, B., Paules, R. et al. (2003) An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol. Cell, 11, 619-633.
12. Green, T.A., Alibhai, I.N., Unterberg, S., Neve, R.L., Ghose, S., Tamminga, C.A. and Nestler, E.J. (2008) Induction of activating transcription factors (ATFs) ATF2, ATF3, and ATF4 in the nucleus accumbens and their regulation of emotional behavior. J. Neurosci., 28, 2025-2032.
13. Costa-Mattioli, M., Gobert, D., Stern, E., Gamache, K., Colina, R., Cuello, C., Sossin, W., Kaufman, R., Pelletier, J., Rosenblum, K. et al. (2007) eIF2alpha phosphorylation bidirectionally regulates the switch from shortto long-term synaptic plasticity and memory. Cell, 129, 195-206.
14. Abel, T., Martin, K.C., Bartsch, D. and Kandel, E.R. (1998) Memory suppressor genes: inhibitory constraints on the storage of long-term memory. Science, 279, 338-341.
15. Chen, A., Muzzio, I.A., Malleret, G., Bartsch, D., Verbitsky, M., Pavlidis, P., Yonan, A.L., Vronskaya, S., Grody, M.B., Cepeda, I. et al. (2003) Inducible enhancement of memory storage and synaptic plasticity in transgenic mice expressing an inhibitor of ATF4 (CREB-2) and C/EBP proteins. Neuron, 39, 655-669.
16. Soares, D.C., Carlyle, B.C., Bradshaw, N.J. and Porteous, D.J. (2011) DISC1: structure, function, and therapeutic potential for major mental illness. ACS Chem. Neurosci., 2, 609-632.
17. Singh, K.K., De Rienzo, G., Drane, L., Mao, Y., Flood, Z., Madison, J., Ferreira, M., Bergen, S., King, C., Sklar, P. et al. (2011) Common DISC1 polymorphisms disrupt Wnt/GSK3beta signaling and brain development. Neuron, 72, 545-558.
18. Song, W., Li, W., Feng, J., Heston, L.L., Scaringe, W.A. and Sommer, S.S. (2008) Identification of high risk DISC1 structural variants with a 2% attributable risk for schizophrenia. Biochem. Biophys. Res. Commun., 367, 700-706.
19. Leliveld, S.R., Bader, V., Hendriks, P., Prikulis, I., Sajnani, G., Requena, J.R. and Korth, C. (2008) Insolubility of disrupted-inschizophrenia 1 disrupts oligomer-dependent interactions with nuclear distribution element 1 and is associated with sporadic mental disease. J. Neurosci., 28, 3839-3845.
20. Leliveld, S.R., Hendriks, P., Michel, M., Sajnani, G., Bader, V., Trossbach, S., Prikulis, I., Hartmann, R., Jonas, E., Willbold, D. et al. (2009) Oligomer assembly of the C-terminal DISC1 domain (640-854) is controlled by self-association motifs and disease-associated polymorphism S704C. Biochemistry, 48, 7746-7755.
21. Ottis, P., Bader, V., Trossbach, S.V., Kretzschmar, H., Michel, M., Leliveld, S.R. and Korth, C. (2011) Convergence of two independent mental disease genes on the protein level: recruitment of dysbindin to cell-invasive disrupted-in-schizophrenia 1 aggresomes. Biol. Psychiatry, 70, 604-610.
22. Narayanan, S., Arthanari, H., Wolfe, M.S. and 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.
23. Ord, D. and Ord, T. (2003) Mouse NIPK interacts with ATF4 and affects its transcriptional activity. Exp. Cell Res., 286, 308-320.
24. Liang, G. and Hai, T. (1997) Characterization of human activating transcription factor 4, a transcriptional activator that interacts with multiple domains of cAMP-responsive element-binding protein (CREB)-binding protein. J. Biol. Chem., 272, 24088-24095.
25. Vallejo, M., Ron, D., Miller, C.P. and Habener, J.F. (1993) C/ATF, a member of the activating transcription factor family of DNA-binding proteins, dimerizes with CAAT/enhancer-binding proteins and directs their binding to cAMP response elements. Proc. Natl Acad. Sci. USA, 90, 4679-4683.
26. Siu, F., Bain, P.J., LeBlanc-Chaffin, R., Chen, H. and Kilberg, M.S. (2002) ATF4 is a mediator of the nutrient-sensing response pathway that activates the human asparagine synthetase gene. J. Biol. Chem., 277, 24120-24127.
27. He, C.H., Gong, P., Hu, B., Stewart, D., Choi, M.E., Choi, A.M. and Alam, J. (2001) Identification of activating transcription factor 4 (ATF4) as an Nrf2-interacting protein. Implication for heme oxygenase-1 gene regulation. J. Biol. Chem., 276, 20858-20865.
28. Kilberg, M.S., Shan, J. and Su, N. (2009) ATF4-dependent transcription mediates signaling of amino acid limitation. Trends Endocrinol. Metab., 20, 436-443.
29. Ma, Y., Brewer, J.W., Diehl, J.A. and Hendershot, L.M. (2002) Two distinct stress signaling pathways converge upon the CHOP promoter during the mammalian unfolded protein response. J. Mol. Biol., 318, 1351-1365.
30. Shan, J., Ord, D., Ord, T. and Kilberg, M.S. (2009) Elevated ATF4 expression, in the absence of other signals, is sufficient for transcriptional induction via CCAAT enhancer-binding protein-activating transcription factor response elements. J. Biol. Chem., 284, 21241-21248.
31. Bruhat, A., Averous, J., Carraro, V., Zhong, C., Reimold, A.M., Kilberg, M.S. and Fafournoux, P. (2002) Differences in the molecular mechanisms involved in the transcriptional activation of the CHOP and asparagine synthetase genes in response to amino acid deprivation or activation of the unfolded protein response. J. Biol. Chem., 277, 48107-48114.
32. Luo, S., Baumeister, P., Yang, S., Abcouwer, S.F. and Lee, A.S. (2003) Induction of Grp78/BiP by translational block: activation of the Grp78 promoter by ATF4 through and upstream ATF/CRE site independent of the endoplasmic reticulum stress elements. J. Biol. Chem., 278, 37375-37385.
33. Vinson, C., Myakishev, M., Acharya, A., Mir, A.A., Moll, J.R. and Bonovich, M. (2002) Classification of human B-ZIP proteins based on dimerization properties. Mol. Cell Biol., 22, 6321-6335.
34. Park, Y.U., Jeong, J., Lee, H., Mun, J.Y., Kim, J.H., Lee, J.S., Nguyen, M.D., Han, S.S., Suh, P.G. and Park, S.K. (2010) Disrupted-in-schizophrenia 1 (DISC1) plays essential roles in mitochondria in collaboration with Mitofilin. Proc. Natl Acad. Sci. USA, 107, 17785-17790.
35. Millar, J.K., James, R., Christie, S. and Porteous, D.J. (2005) Disrupted in schizophrenia 1 (DISC1): subcellular targeting and induction of ring mitochondria. Mol. Cell Neurosci., 30, 477-484.
36. James, R., Adams, R.R., Christie, S., Buchanan, S.R., Porteous, D.J. and Millar, J.K. (2004) Disrupted in Schizophrenia 1 (DISC1) is a multicompartmentalized protein that predominantly localizes to mitochondria. Mol. Cell Neurosci., 26, 112-122.
37. Hodgkinson, C.A., Goldman, D., Jaeger, J., Persaud, S., Kane, J.M., Lipsky, R.H. and Malhotra, A.K. (2004) Disrupted in schizophrenia 1 (DISC1): association with schizophrenia, schizoaffective disorder, and bipolar disorder. Am. J. Hum. Genet., 75, 862-872.
38. Lepagnol-Bestel, A.M., Dubertret, C., Benmessaoud, D., Simonneau, M., Ades, J., Kacha, F., Hamdani, N., Gorwood, P. and Ramoz, N. (2010) Association of DISC1 gene with schizophrenia in families from two distinct French and Algerian populations. Psychiatr. Genet., 20, 298-303.
39. Schosser, A., Gaysina, D., Cohen-Woods, S., Chow, P.C., Martucci, L., Craddock, N., Farmer, A., Korszun, A., Gunasinghe, C., Gray, J. et al. (2009) Association of DISC1 and TSNAX genes and affective disorders in the depression case-control (DeCC) and bipolar affective case-control (BACCS) studies. Mol. Psychiatry, 15, 844-849.
40. Szeszko, P.R., Hodgkinson, C.A., Robinson, D.G., Derosse, P., Bilder, R.M., Lencz, T., Burdick, K.E., Napolitano, B., Betensky, J.D., Kane, J.M. et al. (2008) DISC1 is associated with prefrontal cortical gray matter and positive symptoms in schizophrenia. Biol. Psychol., 79, 103-110.
41. Shaikh, M., Hall, M.H., Schulze, K., Dutt, A., Li, K., Williams, I., Walshe, M., Constante, M., Broome, M., Picchioni, M. et al. (2011) Effect of DISC1 on the P300 waveform in psychosis. Schizophr. Bull. [Epub ahead of print]. doi: 10.1093/schbul/sbr101.
42. Cannon, T.D., Hennah, W., van Erp, T.G., Thompson, P.M., Lonnqvist, J., Huttunen, M., Gasperoni, T., Tuulio-Henriksson, A., Pirkola, T., Toga, A.W. et al. (2005) Association of DISC1/TRAX haplotypes with schizophrenia, reduced prefrontal gray matter, and impaired short- and long-term memory. Arch. Gen. Psychiatry, 62, 1205-1213.
43. Raznahan, A., Lee, Y., Long, R., Greenstein, D., Clasen, L., Addington, A., Rapoport, J.L. and Giedd, J.N. (2011) Common functional polymorphisms of DISC1 and cortical maturation in typically developing children and adolescents. Mol. Psychiatry, 16, 917-926.
44. Brauns, S., Gollub, R.L., Roffman, J.L., Yendiki, A., Ho, B.C., Wassink, T.H., Heinz, A. and Ehrlich, S. (2011) DISC1 is associated with cortical thickness and neural efficiency. Neuroimage, 57, 1591-1600.
45. Whalley, H.C., Sussmann, J.E., Johnstone, M., Romaniuk, L., Redpath, H., Chakirova, G., Mukherjee, P., Hall, J., Johnstone, E.C., Lawrie, S.M. et al. (2012) Effects of a mis-sense DISC1 variant on brain activation in two cohorts at high risk of bipolar disorder or schizophrenia. Am. J. Med. Genet. B Neuropsychiatr. Genet. [Epub ahead of print]. doi: 10.1002/ajmg.b.32035.
46. Hennah, W., Thomson, P., McQuillin, A., Bass, N., Loukola, A., Anjorin, A., Blackwood, D., Curtis, D., Deary, I.J., Harris, S.E. et al. (2009) DISC1 association, heterogeneity and interplay in schizophrenia and bipolar disorder. Mol. Psychiatry, 14, 865-873.
47. Kamiya, A., Kubo, K., Tomoda, T., Takaki, M., Youn, R., Ozeki, Y., Sawamura, N., Park, U., Kudo, C., Okawa, M. et al. (2005) A schizophrenia-associated mutation of DISC1 perturbs cerebral cortex development. Nat. Cell Biol., 7, 1167-1178.
48. 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. et al. (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.
49. Elefteriou, F., Ahn, J.D., Takeda, S., Starbuck, M., Yang, X., Liu, X., Kondo, H., Richards, W.G., Bannon, T.W., Noda, M. et al. (2005) Leptin regulation of bone resorption by the sympathetic nervous system and CART. Nature, 434, 514-520.
50. Lassot, I., Estrabaud, E., Emiliani, S., Benkirane, M., Benarous, R. and Margottin-Goguet, F. (2005) p300 modulates ATF4 stability and transcriptional activity independently of its acetyltransferase domain. J. Biol. Chem., 280, 41537-41545.
51. Yang, X., Matsuda, K., Bialek, P., Jacquot, S., Masuoka, H.C., Schinke, T., Li, L., Brancorsini, S., Sassone-Corsi, P., Townes, T.M. et al. (2004) ATF4 is a substrate of RSK2 and an essential regulator of osteoblast biology; implication for Coffin-Lowry Syndrome. Cell, 117, 387-398.
52. Dever, T.E. (2002) Gene-specific regulation by general translation factors. Cell, 108, 545-556.
53. Harding, H.P., Novoa, I., Zhang, Y., Zeng, H., Wek, R., Schapira, M. and Ron, D. (2000) Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol. Cell, 6, 1099-1108.
54. Vattem, K.M. and Wek, R.C. (2004) Reinitiation involving upstream ORFs regulates ATF4 mRNA translation in mammalian cells. Proc. Natl Acad. Sci. USA, 101, 11269-11274.
55. Lassot, I., Segeral, E., Berlioz-Torrent, C., Durand, H., Groussin, L., Hai, T., Benarous, R. and Margottin-Goguet, F. (2001) ATF4 degradation relies on a phosphorylation-dependent interaction with the SCF(betaTrCP) ubiquitin ligase. Mol. Cell Biol., 21, 2192-2202.
56. Pons, J., Evrard-Todeschi, N., Bertho, G., Gharbi-Benarous, J., Benarous, R. and Girault, J.P. (2007) Phosphorylation-dependent structure of ATF4 peptides derived from a human ATF4 protein, a member of the family of transcription factors. Peptides, 28, 2253-2267.
57. Frank, C.L., Ge, X., Xie, Z., Zhou, Y. and Tsai, L.H. (2010) Control of activating transcription factor 4 (ATF4) persistence by multisite phosphorylation impacts cell cycle progression and neurogenesis. J. Biol. Chem., 285, 33324-33337.
58. Gachon, F., Gaudray, G., Thebault, S., Basbous, J., Koffi, J.A., Devaux, C. and Mesnard, J. (2001) The cAMP response element binding protein-2 (CREB-2) can interact with the C/EBP-homologous protein (CHOP). FEBS Lett., 502, 57-62.
59. Karpinski, B.A., Morle, G.D., Huggenvik, J., Uhler, M.D. and Leiden, J.M. (1992) Molecular cloning of human CREB-2: an ATF/CREB transcription factor that can negatively regulate transcription from the cAMP response element. Proc. Natl Acad. Sci. USA, 89, 4820-4824.
60. Costa-Mattioli, M. and Sonenberg, N. (2006) Translational control of long-term synaptic plasticity and memory storage by eIF2alpha. Crit. Rev. Neurobiol., 18, 187-195.
61. Bartsch, D., Ghirardi, M., Skehel, P.A., Karl, K.A., Herder, S.P., Chen, M., Bailey, C.H. and Kandel, E.R. (1995) Aplysia CREB2 represses long-term facilitation: relief of repression converts transient facilitation into long-term functional and structural change. Cell, 83, 979-992.
62. Clapcote, S.J., Lipina, T.V., Millar, J.K., Mackie, S., Christie, S., Ogawa, F., Lerch, J.P., Trimble, K., Uchiyama, M., Sakuraba, Y. et al. (2007) Behavioral phenotypes of Disc1 missense mutations in mice. Neuron, 54, 387-402.
63. Shen, S., Lang, B., Nakamoto, C., Zhang, F., Pu, J., Kuan, S.L., Chatzi, C., He, S., Mackie, I., Brandon, N.J. et al. (2008) Schizophrenia-related neural and behavioral phenotypes in transgenic mice expressing truncated Disc1. J. Neurosci., 28, 10893-10904.
64. Hikida, T., Jaaro-Peled, H., Seshadri, S., Oishi, K., Hookway, C., Kong, S., Wu, D., Xue, R., Andrade, M., Tankou, S. et al. (2007) Dominant-negative DISC1 transgenic mice display schizophrenia-associated phenotypes detected by measures translatable to humans. Proc. Natl Acad. Sci. USA, 104, 14501-14506.
65. Li, W., Zhou, Y., Jentsch, J.D., Brown, R.A., Tian, X., Ehninger, D., Hennah, W., Peltonen, L., Lonnqvist, J., Huttunen, M.O. et al. (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.
66. Ayhan, Y., Abazyan, B., Nomura, J., Kim, R., Ladenheim, B., Krasnova, I.N., Sawa, A., Margolis, R.L., Cadet, J.L., Mori, S. et al. (2011) Differential effects of prenatal and postnatal expressions of mutant human DISC1 on neurobehavioral phenotypes in transgenic mice: evidence for neurodevelopmental origin of major psychiatric disorders. Mol. Psychiatry, 16, 293-306.
67. Mao, Y., Ge, X., Frank, C.L., Madison, J.M., Koehler, A.N., Doud, M.K., Tassa, C., Berry, E.M., Soda, T., Singh, K.K. et al. (2009) Disrupted in schizophrenia 1 regulates neuronal progenitor proliferation via modulation of GSK3beta/beta-catenin signaling. Cell, 136, 1017-1031.
68. Niwa, M., Kamiya, A., Murai, R., Kubo, K., Gruber, A.J., Tomita, K., Lu, L., Tomisato, S., Jaaro-Peled, H., Seshadri, S. et al. (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.
69. Lipina, T.V., Niwa, M., Jaaro-Peled, H., Fletcher, P.J., Seeman, P., Sawa, A. and Roder, J.C. (2010) Enhanced dopamine function in DISC1-L100P mutant mice: implications for schizophrenia. Genes Brain Behav., 9, 777-789.
70. Badiola, N., Penas, C., Minano-Molina, A., Barneda-Zahonero, B., Fado, R., Sanchez-Opazo, G., Comella, J.X., Sabria, J., Zhu, C., Blomgren, K. et al. (2011) Induction of ER stress in response to oxygen-glucose deprivation of cortical cultures involves the activation of the PERK and IRE-1 pathways and of caspase-12. Cell Death Dis., 2, e149.
71. Granberg, F., Svensson, C., Pettersson, U. and Zhao, H. (2006) Adenovirus-induced alterations in host cell gene expression prior to the onset of viral gene expression. Virology, 353, 1-5.
72. Lange, P.S., Chavez, J.C., Pinto, J.T., Coppola, G., Sun, C.W., Townes, T.M., Geschwind, D.H. and Ratan, R.R. (2008) ATF4 is an oxidative stress-inducible, prodeath transcription factor in neurons in vitro and in vivo. J. Exp. Med., 205, 1227-1242.
73. Silva, J.M., Wong, A., Carelli, V. and Cortopassi, G.A. (2009) Inhibition of mitochondrial function induces an integrated stress response in oligodendroglia. Neurobiol. Dis., 34, 357-365.
74. Brown, A.S. (2011) The environment and susceptibility to schizophrenia. Prog. Neurobiol., 93, 23-58.
75. Caspi, A., Moffitt, T.E., Cannon, M., McClay, J., Murray, R., Harrington, H., Taylor, A., Arseneault, L., Williams, B., Braithwaite, A. et al. (2005) Moderation of the effect of adolescent-onset cannabis use on adult psychosis by a functional polymorphism in the catechol-O-methyltransferase gene: longitudinal evidence of a gene X environment interaction. Biol. Psychiatry, 57, 1117-1127.
76. Ogawa, F., Kasai, M. and Akiyama, T. (2005) A functional link between Disrupted-In-Schizophrenia 1 and the eukaryotic translation initiation factor 3. Biochem. Biophys. Res. Commun., 338, 771-776.
77. McLaurin, J., Trudel, G.C., Shaw, I.T., Antel, J.P. and Cashman, N.R. (1995) A human glial hybrid cell line differentially expressing genes subserving oligodendrocyte and astrocyte phenotype. J. Neurobiol., 26, 283-293.
78. Ord, D., Meerits, K. and Ord, T. (2007)TRB3 protects cells against the growth inhibitory and cytotoxic effect of ATF4. Exp. Cell Res., 313, 3556-3567.
79. Bradshaw, N.J., Ogawa, F., Antolin-Fontes, B., Chubb, J.E., Carlyle, B.C., Christie, S., Claessens, A., Porteous, D.J. and Millar, J.K. (2008) DISC1, PDE4B, and NDE1 at the centrosome and synapse. Biochem. Biophys. Res. Commun., 377, 1091-1096.