Genetic risk for schizophrenia: Convergence on synaptic pathways involved in plasticity

Biological Psychiatry

Volumn 77, Issue 1, 2015, Pages 52-58

  Hall, Jeremy ^a   Trent, Simon ^a   Thomas, Kerrie L ^a,b   O'Donovan, Michael C ^a   Owen, Michael J ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

^b CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

Actin; ARC; Genetics; NMDA; Schizophrenia; Synapse

Indexed keywords

FRAGILE X MENTAL RETARDATION PROTEIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; VOLTAGE GATED CALCIUM CHANNEL;

BINOCULAR CONVERGENCE; BIOLOGY; CHROMOSOME DELETION; CYTOSKELETON; EXOME; GENE MUTATION; GENETIC RISK; GENETICS; HUMAN; NERVE CELL PLASTICITY; PATHOGENESIS; POSTSYNAPTIC DENSITY; PRIORITY JOURNAL; REVIEW; SCHIZOPHRENIA; SYNAPSE; SYNAPTIC TRANSMISSION; ALLELE; BRAIN; COPY NUMBER VARIATION; GENETIC PREDISPOSITION; METABOLISM; MUTATION; NERVE CELL; RISK FACTOR; SIGNAL TRANSDUCTION;

ALLELES; BRAIN; DNA COPY NUMBER VARIATIONS; GENETIC PREDISPOSITION TO DISEASE; HUMANS; MUTATION; NEURONAL PLASTICITY; NEURONS; RECEPTORS, N-METHYL-D-ASPARTATE; RISK FACTORS; SCHIZOPHRENIA; SIGNAL TRANSDUCTION;

EID: 84920646061     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2014.07.011     Document Type: Review

References (85)

1. N.J. Bray, and M.J. Owen Searching for schizophrenia genes Trends Mol Med 7 2001 169 174
2. Gottesman II, and J. Shields A polygenic theory of schizophrenia Proc Natl Acad Sci U S A 58 1967 199 205
3. T.R. Insel Translating scientific opportunity into public health impact: A strategic plan for research on mental illness Arch Gen Psychiatry 66 2009 128 133
4. J.L. Doherty, M.C. O'Donovan, and M.J. Owen Recent genomic advances in schizophrenia Clin Genet 81 2012 103 109
5. Y. Kim, S. Zerwas, S.E. Trace, and P.F. Sullivan Schizophrenia genetics: Where next? Schizophr Bull 37 2011 456 463
6. B.J. Mowry, and J. Gratten The emerging spectrum of allelic variation in schizophrenia: Current evidence and strategies for the identification and functional characterization of common and rare variants Mol Psychiatry 18 2013 38 52
7. G. Kirov, A.J. Pocklington, P. Holmans, D. Ivanov, M. Ikeda, and D. Ruderfer De novo CNV analysis implicates specific abnormalities of postsynaptic signalling complexes in the pathogenesis of schizophrenia Mol Psychiatry 17 2012 142 153
8. D. Pinto, A.T. Pagnamenta, L. Klei, R. Anney, D. Merico, and R. Regan Functional impact of global rare copy number variation in autism spectrum disorders Nature 466 2010 368 372
9. E.M. Kenny, P. Cormican, S. Furlong, E. Heron, G. Kenny, and C. Fahey Excess of rare novel loss-of-function variants in synaptic genes in schizophrenia and autism spectrum disorders Mol Psychiatry 19 2014 872 879
10. International Schizophrenia Consortium S.M. Purcell, N.R. Wray, J.L. Stone, P.M. Visscher, and M.C. O'Donovan Common polygenic variation contributes to risk of schizophrenia and bipolar disorder Nature 460 2009 748 752
11. M.J. Owen, N. Craddock, and M.C. O'Donovan Suggestion of roles for both common and rare risk variants in genome-wide studies of schizophrenia Arch Gen Psychiatry 67 2010 667 673
12. M.C. O'Donovan, N. Craddock, N. Norton, H. Williams, T. Peirce, and V. Moskvina Identification of loci associated with schizophrenia by genome-wide association and follow-up Nat Genet 40 2008 1053 1055
13. J. Shi, D.F. Levinson, J. Duan, A.R. Sanders, Y. Zheng, and I. Pe'er Common variants on chromosome 6p22.1 are associated with schizophrenia Nature 460 2009 753 757
14. H. Stefansson, R.A. Ophoff, S. Steinberg, O.A. Andreassen, S. Cichon, and D. Rujescu Common variants conferring risk of schizophrenia Nature 460 2009 744 747
15. H.J. Williams, N. Craddock, G. Russo, M.L. Hamshere, V. Moskvina, and S. Dwyer Most genome-wide significant susceptibility loci for schizophrenia and bipolar disorder reported to date cross-traditional diagnostic boundaries Hum Mol Genet 20 2011 387 391
16. International Schizophrenia Consortium Rare chromosomal deletions and duplications increase risk of schizophrenia Nature 455 2008 237 241
17. H. Stefansson, D. Rujescu, S. Cichon, O.P. Pietilainen, A. Ingason, and S. Steinberg Large recurrent microdeletions associated with schizophrenia Nature 455 2008 232 236
18. G. Kirov, D. Grozeva, N. Norton, D. Ivanov, K.K. Mantripragada, and P. Holmans Support for the involvement of large copy number variants in the pathogenesis of schizophrenia Hum Mol Genet 18 2009 1497 1503
19. J. Sebat, B. Lakshmi, J. Troge, J. Alexander, J. Young, and P. Lundin Large-scale copy number polymorphism in the human genome Science 305 2004 525 528
20. E. Rees, V. Moskvina, M.J. Owen, M.C. O'Donovan, and G. Kirov De novo rates and selection of schizophrenia-associated copy number variants Biol Psychiatry 70 2011 1109 1114
21. Lee SH, DeCandia TR, Ripke S, Yang J, Schizophrenia Psychiatric Genome-Wide Association Study Consortium, International Schizophrenia Consortium, et al. (2012): Estimating the proportion of variation in susceptibility to schizophrenia captured by common SNPs. Nat Genet 44:247-250
22. E. Rees, G. Kirov, M.C. O'Donovan, and M.J. Owen De novo mutation in schizophrenia Schizophr Bull 38 2012 377 381
23. J.A. Veltman, and H.G. Brunner De novo mutations in human genetic disease Nat Rev Genet 13 2012 565 575
24. B.M. Neale, Y. Kou, L. Liu, A. Ma'ayan, K.E. Samocha, and A. Sabo Patterns and rates of exonic de novo mutations in autism spectrum disorders Nature 485 2012 242 245
25. B.J. O'Roak, L. Vives, S. Girirajan, E. Karakoc, N. Krumm, and B.P. Coe Sporadic autism exomes reveal a highly interconnected protein network of de novo mutations Nature 485 2012 246 250
26. A. Rauch, D. Wieczorek, E. Graf, T. Wieland, S. Endele, and T. Schwarzmayr Range of genetic mutations associated with severe non-syndromic sporadic intellectual disability: An exome sequencing study Lancet 380 2012 1674 1682
27. S.J. Sanders, M.T. Murtha, A.R. Gupta, J.D. Murdoch, M.J. Raubeson, and A.J. Willsey De novo mutations revealed by whole-exome sequencing are strongly associated with autism Nature 485 2012 237 241
28. S.L. Girard, J. Gauthier, A. Noreau, L. Xiong, S. Zhou, and L. Jouan Increased exonic de novo mutation rate in individuals with schizophrenia Nat Genet 43 2011 860 863
29. B. Xu, I. Ionita-Laza, J.L. Roos, B. Boone, S. Woodrick, and Y. Sun De novo gene mutations highlight patterns of genetic and neural complexity in schizophrenia Nat Genet 44 2012 1365 1369
30. M. Fromer, A.J. Pocklington, D.H. Kavanagh, H.J. Williams, S. Dwyer, and P. Gormley De novo mutations in schizophrenia implicate synaptic networks Nature 506 2014 179 184
31. S.M. Purcell, J.L. Moran, M. Fromer, D. Ruderfer, N. Solovieff, and P. Roussos A polygenic burden of rare disruptive mutations in schizophrenia Nature 506 2014 185 190
32. T. Walsh, J.M. McClellan, S.E. McCarthy, A.M. Addington, S.B. Pierce, and G.M. Cooper Rare structural variants disrupt multiple genes in neurodevelopmental pathways in schizophrenia Science 320 2008 539 543
33. R.D. Emes, A.J. Pocklington, C.N. Anderson, A. Bayes, M.O. Collins, and C.A. Vickers Evolutionary expansion and anatomical specialization of synapse proteome complexity Nat Neurosci 11 2008 799 806
34. A. Bayes, and S.G. Grant Neuroproteomics: Understanding the molecular organization and complexity of the brain Nat Rev Neurosci 10 2009 635 646
35. I. Napoli, V. Mercaldo, P.P. Boyl, B. Eleuteri, F. Zalfa, and S. De Rubeis The fragile X syndrome protein represses activity-dependent translation through CYFIP1, a new 4E-BP Cell 134 2008 1042 1054
36. E. Fernandez, N. Rajan, and C. Bagni The FMRP regulon: From targets to disease convergence Front Neurosci 7 2013 191
37. L.A. Cingolani, and Y. Goda Actin in action: The interplay between the actin cytoskeleton and synaptic efficacy Nat Rev Neurosci 9 2008 344 356
38. F. Casamassima, A.C. Hay, A. Benedetti, L. Lattanzi, G.B. Cassano, and R.H. Perlis L-type calcium channels and psychiatric disorders: A brief review Am J Med Genet B Neuropsychiatr Genet 153B 2010 1373 1390
39. Schizophrenia Psychiatric Genome-Wide Association Study Consortium Genome-wide association study identifies five new schizophrenia loci Nat Genet 43 2011 969 976
40. S. Bhat, D.T. Dao, C.E. Terrillion, M. Arad, R.J. Smith, N.M. Soldatov, and T.D. Gould CACNA1C (Cav1.2) in the pathophysiology of psychiatric disease Prog Neurobiol 99 2012 1 14
41. S. Ripke, C. O'Dushlaine, K. Chambert, J.L. Moran, A.K. Kahler, and S. Akterin Genome-wide association analysis identifies 13 new risk loci for schizophrenia Nat Genet 45 2013 1150 1159
42. S. Moosmang, N. Haider, N. Klugbauer, H. Adelsberger, N. Langwieser, and J. Muller Role of hippocampal Cav1.2 Ca2+ channels in NMDA receptor-independent synaptic plasticity and spatial memory J Neurosci 25 2005 9883 9892
43. V.R. Rao, and S. Finkbeiner NMDA and AMPA receptors: Old channels, new tricks Trends Neurosci 30 2007 284 291
44. H. Wang, Y. Hu, and J.Z. Tsien Molecular and systems mechanisms of memory consolidation and storage Prog Neurobiol 79 2006 123 135
45. S. Finkbeiner, and M.E. Greenberg Ca2+ channel-regulated neuronal gene expression J Neurobiol 37 1998 171 189
46. A.E. West, W.G. Chen, M.B. Dalva, R.E. Dolmetsch, J.M. Kornhauser, and A.J. Shaywitz Calcium regulation of neuronal gene expression Proc Natl Acad Sci U S A 98 2001 11024 11031
47. O. Steward, and P.F. Worley Selective targeting of newly synthesized Arc mRNA to active synapses requires NMDA receptor activation Neuron 30 2001 227 240
48. P. Vanhoutte, and H. Bading Opposing roles of synaptic and extrasynaptic NMDA receptors in neuronal calcium signalling and BDNF gene regulation Curr Opin Neurobiol 13 2003 366 371
49. O. Steward, C.S. Wallace, G.L. Lyford, and P.F. Worley Synaptic activation causes the mRNA for the IEG Arc to localize selectively near activated postsynaptic sites on dendrites Neuron 21 1998 741 751
50. Y. Yin, G.M. Edelman, and P.W. Vanderklish The brain-derived neurotrophic factor enhances synthesis of Arc in synaptoneurosomes Proc Natl Acad Sci U S A 99 2002 2368 2373
51. F. Huang, J.K. Chotiner, and O. Steward Actin polymerization and ERK phosphorylation are required for Arc/Arg3.1 mRNA targeting to activated synaptic sites on dendrites J Neurosci 27 2007 9054 9067
52. J.J. Rodriguez, H.A. Davies, A.T. Silva, I.E. De Souza, C.J. Peddie, and F.M. Colyer Long-term potentiation in the rat dentate gyrus is associated with enhanced Arc/Arg3.1 protein expression in spines, dendrites and glia Eur J Neurosci 21 2005 2384 2396
53. C.R. Bramham, M.N. Alme, M. Bittins, S.D. Kuipers, R.R. Nair, and B. Pai The Arc of synaptic memory Exp Brain Res 200 2010 125 140
54. J.F. Guzowski, G.L. Lyford, G.D. Stevenson, F.P. Houston, J.L. McGaugh, P.F. Worley, and C.A. Barnes Inhibition of activity-dependent arc protein expression in the rat hippocampus impairs the maintenance of long-term potentiation and the consolidation of long-term memory J Neurosci 20 2000 3993 4001
55. N. Plath, O. Ohana, B. Dammermann, M.L. Errington, D. Schmitz, and C. Gross Arc/Arg3.1 is essential for the consolidation of synaptic plasticity and memories Neuron 52 2006 437 444
56. E. Messaoudi, T. Kanhema, J. Soule, A. Tiron, G. Dagyte, and B. da Silva Sustained Arc/Arg3.1 synthesis controls long-term potentiation consolidation through regulation of local actin polymerization in the dentate gyrus in vivo J Neurosci 27 2007 10445 10455
57. S. Chowdhury, J.D. Shepherd, H. Okuno, G. Lyford, R.S. Petralia, and N. Plath Arc/Arg3.1 interacts with the endocytic machinery to regulate AMPA receptor trafficking Neuron 52 2006 445 459
58. R.L. Huganir, and R.A. Nicoll AMPARs and synaptic plasticity: The last 25 years Neuron 80 2013 704 717
59. C.L. Peebles, J. Yoo, M.T. Thwin, J.J. Palop, J.L. Noebels, and S. Finkbeiner Arc regulates spine morphology and maintains network stability in vivo Proc Natl Acad Sci U S A 107 2010 18173 18178
60. E.M. Rial Verde, J. Lee-Osbourne, P.F. Worley, R. Malinow, and H.T. Cline Increased expression of the immediate-early gene arc/arg3.1 reduces AMPA receptor-mediated synaptic transmission Neuron 52 2006 461 474
61. Y. Kim, J.Y. Sung, I. Ceglia, K.W. Lee, J.H. Ahn, and J.M. Halford Phosphorylation of WAVE1 regulates actin polymerization and dendritic spine morphology Nature 442 2006 814 817
62. J.D. Shepherd, G. Rumbaugh, J. Wu, S. Chowdhury, N. Plath, and D. Kuhl Arc/Arg3.1 mediates homeostatic synaptic scaling of AMPA receptors Neuron 52 2006 475 484
63. M.W. Waung, B.E. Pfeiffer, E.D. Nosyreva, J.A. Ronesi, and K.M. Huber Rapid translation of Arc/Arg3.1 selectively mediates mGluR-dependent LTD through persistent increases in AMPAR endocytosis rate Neuron 59 2008 84 97
64. E. Korb, C.L. Wilkinson, R.N. Delgado, K.L. Lovero, and S. Finkbeiner Arc in the nucleus regulates PML-dependent GluA1 transcription and homeostatic plasticity Nat Neurosci 16 2013 874 883
65. A. Routtenberg Lifetime memories from persistently supple synapses Hippocampus 23 2013 202 206
66. W.A. Catterall, and A.P. Few Calcium channel regulation and presynaptic plasticity Neuron 59 2008 882 901
67. T.C. Sudhof Neuroligins and neurexins link synaptic function to cognitive disease Nature 455 2008 903 911
68. P.F. Sullivan, M.J. Daly, and M. O'Donovan Genetic architectures of psychiatric disorders: The emerging picture and its implications Nat Rev Genet 13 2012 537 551
69. J. de Ligt, M.H. Willemsen, B.W. van Bon, T. Kleefstra, H.G. Yntema, and T. Kroes Diagnostic exome sequencing in persons with severe intellectual disability N Engl J Med 367 2012 1921 1929
70. D. Malhotra, and J. Sebat CNVs: Harbingers of a rare variant revolution in psychiatric genetics Cell 148 2012 1223 1241
71. N. Craddock, and M.J. Owen The Kraepelinian dichotomy - going, going. but still not gone Br J Psychiatry 196 2010 92 95
72. M.J. Owen Implications of genetic findings for understanding schizophrenia Schizophr Bull 38 2012 904 907
73. V.M. Ho, J.A. Lee, and K.C. Martin The cell biology of synaptic plasticity Science 334 2011 623 628
74. P.J. Nathan, S.R. Cobb, B. Lu, E.T. Bullmore, and C.H. Davies Studying synaptic plasticity in the human brain and opportunities for drug discovery Curr Opin Pharmacol 11 2011 540 548
75. P.R. Corlett, G.D. Honey, J.H. Krystal, and P.C. Fletcher Glutamatergic model psychoses: Prediction error, learning, and inference Neuropsychopharmacology 36 2011 294 315
76. P.W. Glimcher Understanding dopamine and reinforcement learning: The dopamine reward prediction error hypothesis Proc Natl Acad Sci U S A 108 suppl 3 2011 15647 15654
77. J. Hall, L. Romaniuk, A.M. McIntosh, J.D. Steele, E.C. Johnstone, and S.M. Lawrie Associative learning and the genetics of schizophrenia Trends Neurosci 32 2009 359 365
78. W. Schultz, and A. Dickinson Neuronal coding of prediction errors Annu Rev Neurosci 23 2000 473 500
79. O.D. Howes, and R.M. Murray Schizophrenia: An integrated sociodevelopmental-cognitive model Lancet 383 2014 1677 1687
80. J.E. Lisman, J.T. Coyle, R.W. Green, D.C. Javitt, F.M. Benes, S. Heckers, and A.A. Grace Circuit-based framework for understanding neurotransmitter and risk gene interactions in schizophrenia Trends Neurosci 31 2008 234 242
81. D.A. Lewis Cortical circuit dysfunction and cognitive deficits in schizophrenia - implications for preemptive interventions Eur J Neurosci 35 2012 1871 1878
82. A.S. Brown The environment and susceptibility to schizophrenia Prog Neurobiol 93 2011 23 58
83. G. Gonzalez-Burgos, and D.A. Lewis NMDA receptor hypofunction, parvalbumin-positive neurons, and cortical gamma oscillations in schizophrenia Schizophr Bull 38 2012 950 957
84. S. Park, J.M. Park, S. Kim, J.A. Kim, J.D. Shepherd, and C.L. Smith-Hicks Elongation factor 2 and fragile X mental retardation protein control the dynamic translation of Arc/Arg3.1 essential for mGluR-LTD Neuron 59 2008 70 83
85. J.D. Shepherd, and M.F. Bear New views of Arc, a master regulator of synaptic plasticity Nat Neurosci 14 2011 279 284