Resequencing and association analysis of Six PSD-95-related genes as possible susceptibility genes for schizophrenia and autism spectrum disorders

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Xing, Jingrui ^a   Kimura, Hiroki ^a   Wang, Chenyao ^a   Ishizuka, Kanako ^a   Kushima, Itaru ^a,b   Arioka, Yuko ^a   Yoshimi, Akira ^a   Nakamura, Yukako ^a   Shiino, Tomoko ^a   Oya Ito, Tomoko ^a   Takasaki, Yuto ^a   Uno, Yota ^a   Okada, Takashi ^a   Iidaka, Tetsuya ^a   Aleksic, Branko ^a   Mori, Daisuke ^a   Ozaki, Norio ^a  

^a NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b NAGOYA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

DISKS LARGE HOMOLOG 4;

ADOLESCENT; ADULT; AUTISM; CASE CONTROL STUDY; CHILD; FEMALE; GENETIC PREDISPOSITION; GENETICS; HUMAN; MALE; MIDDLE AGED; MISSENSE MUTATION; SCHIZOPHRENIA;

ADOLESCENT; ADULT; AUTISM SPECTRUM DISORDER; CASE-CONTROL STUDIES; CHILD; DISKS LARGE HOMOLOG 4 PROTEIN; FEMALE; GENETIC PREDISPOSITION TO DISEASE; HUMANS; MALE; MIDDLE AGED; MUTATION, MISSENSE; SCHIZOPHRENIA;

EID: 84976394852     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep27491     Document Type: Article

References (72)

1. Sullivan, P. F., Kendler, K. S. & Neale, M. C. Schizophrenia as a complex trait: evidence from a meta-Analysis of twin studies. Arch Gen Psychiatry 60, 1187-1192 (2003).
2. Purcell, S. M. et al. A polygenic burden of rare disruptive mutations in schizophrenia. Nature 506, 185-190 (2014).
3. Schizophrenia Working Group of the Psychiatric Genomics, C. Biological insights from 108 schizophrenia-Associated genetic loci. Nature 511, 421-427 (2014).
4. Sullivan, P. F., Daly, M. J. & O'Donovan, M. Genetic architectures of psychiatric disorders: the emerging picture and its implications. Nat Rev Genet 13, 537-551 (2012).
5. Okabe, S. Molecular anatomy of the postsynaptic density. Mol Cell Neurosci 34, 503-518 (2007).
6. Verpelli, C., Schmeisser, M. J., Sala, C. & Boeckers, T. M. Scaffold proteins at the postsynaptic density. Adv Exp Med Biol 970, 29-61 (2012).
7. Elias, G. M. & Nicoll, R. A. Synaptic trafficking of glutamate receptors by MAGUK scaffolding proteins. Trends Cell Biol 17, 343-352 (2007).
8. Cheng, M. C. et al. Genetic and functional analysis of the DLG4 gene encoding the post-synaptic density protein 95 in schizophrenia. PLoS One 5, e15107 (2010).
9. Kristiansen, L. V., Beneyto, M., Haroutunian, V. & Meador-Woodruff, J. H. Changes in NMDA receptor subunits and interacting PSD proteins in dorsolateral prefrontal and anterior cingulate cortex indicate abnormal regional expression in schizophrenia. Mol Psychiatry 11, 737-747, 705 (2006).
10. Funk, A. J., Rumbaugh, G., Harotunian, V., McCullumsmith, R. E. & Meador-Woodruff, J. H. Decreased expression of NMDA receptor-Associated proteins in frontal cortex of elderly patients with schizophrenia. Neuroreport 20, 1019-1022 (2009).
11. Kristiansen, L. V. & Meador-Woodruff, J. H. Abnormal striatal expression of transcripts encoding NMDA interacting PSD proteins in schizophrenia, bipolar disorder and major depression. Schizophr Res 78, 87-93 (2005).
12. Toro, C. & Deakin, J. F. NMDA receptor subunit NRI and postsynaptic protein PSD-95 in hippocampus and orbitofrontal cortex in schizophrenia and mood disorder. Schizophr Res 80, 323-330 (2005).
13. Clinton, S. M. & Meador-Woodruff, J. H. Abnormalities of the NMDA Receptor and Associated Intracellular Molecules in the Thalamus in Schizophrenia and Bipolar Disorder. Neuropsychopharmacology 29, 1353-1362 (2004).
14. Ohnuma, T. et al. Gene expression of PSD95 in prefrontal cortex and hippocampus in schizophrenia. Neuroreport 11, 3133-3137 (2000).
15. Mulle, J. G. et al. Microdeletions of 3q29 confer high risk for schizophrenia. Am J Hum Genet 87, 229-236 (2010).
16. Sato, J., Shimazu, D., Yamamoto, N. & Nishikawa, T. An association analysis of synapse-Associated protein 97 (SAP97) gene in schizophrenia. J Neural Transm 115, 1355-1365 (2008).
17. Uezato, A. et al. Further evidence for a male-selective genetic association of synapse-Associated protein 97 (SAP97) gene with schizophrenia. Behav Brain Funct 8, 2 (2012).
18. Toyooka, K. et al. Selective reduction of a PDZ protein, SAP-97, in the prefrontal cortex of patients with chronic schizophrenia. J Neurochem 83, 797-806 (2002).
19. Dracheva, S., McGurk, S. R. & Haroutunian, V. mRNA expression of AMPA receptors and AMPA receptor binding proteins in the cerebral cortex of elderly schizophrenics. J Neurosci Res 79, 868-878 (2005).
20. MacLaren, E. J., Charlesworth, P., Coba, M. P. & Grant, S. G. Knockdown of mental disorder susceptibility genes disrupts neuronal network physiology in vitro. Mol Cell Neurosci 47, 93-99 (2011).
21. Kim, E. et al. GKAP, a novel synaptic protein that interacts with the guanylate kinase-like domain of the PSD-95/SAP90 family of channel clustering molecules. J Cell Biol 136, 669-678 (1997).
22. Takeuchi, M. et al. SAPAPs. A family of PSD-95/SAP90-Associated proteins localized at postsynaptic density. J Biol Chem 272, 11943-11951 (1997).
23. Li, J. M. et al. Genetic analysis of the DLGAP1 gene as a candidate gene for schizophrenia. Psychiatry Res 205, 13-17 (2013).
24. Li, J. M. et al. Role of the DLGAP2 gene encoding the SAP90/PSD-95-Associated protein 2 in schizophrenia. PLoS One 9, e85373 (2014).
25. Sodhi, M. S., Simmons, M., McCullumsmith, R., Haroutunian, V. & Meador-Woodruff, J. H. Glutamatergic gene expression is specifically reduced in thalamocortical projecting relay neurons in schizophrenia. Biol Psychiatry 70, 646-654 (2011).
26. Guo, X. et al. Reduced expression of the NMDA receptor-interacting protein SynGAP causes behavioral abnormalities that model symptoms of Schizophrenia. Neuropsychopharmacology 34, 1659-1672 (2009).
27. Kirov, G. et al. De novo CNV analysis implicates specific abnormalities of postsynaptic signalling complexes in the pathogenesis of schizophrenia. Mol Psychiatry 17, 142-153 (2012).
28. Szatkiewicz, J. P. et al. Copy number variation in schizophrenia in Sweden. Mol Psychiatry 19, 762-773 (2014).
29. Arlington, V. American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders. 5thed. American Psychiatric Publishing (2013).
30. Moreno-De-Luca, A. et al. Developmental brain dysfunction: revival and expansion of old concepts based on new genetic evidence. The Lancet. Neurology 12, 406-414 (2013).
31. Reiss, A. L. Childhood developmental disorders: an academic and clinical convergence point for psychiatry, neurology, psychology and pediatrics. Journal of child psychology and psychiatry, and allied disciplines 50, 87-98 (2009).
32. Capute & Accardo's 3e Vol II,The Spectrum of Neurodevelopmental Disabilities,Capute & Accardo's Neurodevelopmental Disabilities in Infancy and Childhood: Neurodevelopmental Diagnosis and Treatment. 61-104 (2008).
33. Crespi, B. J. & Crofts, H. J. Association testing of copy number variants in schizophrenia and autism spectrum disorders. J Neurodev Disord 4, 15 (2012).
34. Ku, C. S. et al. A new paradigm emerges from the study of de novo mutations in the context of neurodevelopmental disease. Mol Psychiatry 18, 141-153 (2013).
35. Martin, J. et al. Biological Overlap of Attention-Deficit/Hyperactivity Disorder and Autism Spectrum Disorder: Evidence From Copy Number Variants. J Am Acad Child Psy 53, 761-770 (2014).
36. McCarthy, S. E. et al. De novo mutations in schizophrenia implicate chromatin remodeling and support a genetic overlap with autism and intellectual disability. Mol Psychiatr 19, 652-658 (2014).
37. Daniel Moreno-De-Luca, A. M.-D.-L., Joseph F. Cubells, Stephan & J. Sanders. Cross-Disorder Comparison of Four Neuropsychiatric CNV Loci. Current Genetic Medicine Reports 2, 151-161 (2014).
38. Krumm, N., O'Roak, B. J., Shendure, J. & Eichler, E. E. A de novo convergence of autism genetics and molecular neuroscience. Trends Neurosci 37, 95-105 (2014).
39. Gilman, S. R. et al. Rare de novo variants associated with autism implicate a large functional network of genes involved in formation and function of synapses. Neuron 70, 898-907 (2011).
40. Pinto, D. et al. Functional impact of global rare copy number variation in autism spectrum disorders. Nature 466, 368-372 (2010).
41. Chien, W. H. et al. Deep exon resequencing of DLGAP2 as a candidate gene of autism spectrum disorders. Mol Autism 4, 26 (2013).
42. Lo-Castro, A. & Curatolo, P. Epilepsy associated with autism and attention deficit hyperactivity disorder: is there a genetic link? Brain Dev 36, 185-193 (2014).
43. Berryer, M. H. et al. Mutations in SYNGAP1 cause intellectual disability, autism, and a specific form of epilepsy by inducing haploinsufficiency. Hum Mutat 34, 385-394 (2013).
44. Hamdan, F. F. et al. De novo SYNGAP1 mutations in nonsyndromic intellectual disability and autism. Biol Psychiatry 69, 898-901 (2011).
45. Cook, E. H., Jr. De novo autosomal dominant mutation in SYNGAP1. Autism Res 4, 155-156 (2011).
46. Willatt, L. et al. 3q29 microdeletion syndrome: clinical and molecular characterization of a new syndrome. Am J Hum Genet 77, 154-160 (2005).
47. Quintero-Rivera, F., Sharifi-Hannauer, P. & Martinez-Agosto, J. A. Autistic and psychiatric findings associated with the 3q29 microdeletion syndrome: case report and review. Am J Med Genet A 152A, 2459-2467 (2010).
48. Egger, G. et al. Identification of risk genes for autism spectrum disorder through copy number variation analysis in Austrian families. Neurogenetics 15, 117-127 (2014).
49. Feyder, M. et al. Association of mouse Dlg4 (PSD-95) gene deletion and human DLG4 gene variation with phenotypes relevant to autism spectrum disorders and Williams' syndrome. Am J Psychiatry 167, 1508-1517 (2010).
50. Leonard, A. S., Davare, M. A., Horne, M. C., Garner, C. C. & Hell, J. W. SAP97 is associated with the alpha-Amino-3-hydroxy-5-methylisoxazole-4-propionic acid receptor GluR1 subunit. J Biol Chem 273, 19518-19524 (1998).
51. Cai, C., Coleman, S. K., Niemi, K. & Keinanen, K. Selective binding of synapse-Associated protein 97 to GluR-A alpha-Amino-5-hydroxy-3-methyl-4-isoxazole propionate receptor subunit is determined by a novel sequence motif. J Biol Chem 277, 31484-31490 (2002).
52. Kim, E. et al. Plasma membrane Ca2+ ATPase isoform 4b binds to membrane-Associated guanylate kinase (MAGUK) proteins via their PDZ (PSD-95/Dlg/ZO-1) domains. J Biol Chem 273, 1591-1595 (1998).
53. Zhang, L. et al. Structure-function analysis of SAP97, a modular scaffolding protein that drives dendrite growth. Mol Cell Neurosci 65, 31-44 (2015).
54. Hong, X., Avetisyan, M., Ronilo, M. & Standley, S. SAP97 blocks the RXR ER retention signal of NMDA receptor subunit GluN1-3 through its SH3 domain. Biochim Biophys Acta 1853, 489-499 (2015).
55. Zhu, J. et al. Guanylate kinase domains of the MAGUK family scaffold proteins as specific phospho-protein-binding modules. EMBO J 30, 4986-4997 (2011).
56. Wu, H. et al. Intramolecular interactions regulate SAP97 binding to GKAP. EMBO J 19, 5740-5751 (2000).
57. Niethammer, M., Kim, E. & Sheng, M. Interaction between the C terminus of NMDA receptor subunits and multiple members of the PSD-95 family of membrane-Associated guanylate kinases. J Neurosci 16, 2157-2163 (1996).
58. Cousins, S. L., Kenny, A. V. & Stephenson, F. A. Delineation of additional PSD-95 binding domains within NMDA receptor NR2 subunits reveals differences between NR2A/PSD-95 and NR2B/PSD-95 association. Neuroscience 158, 89-95 (2009).
59. Tong, J., Yang, H., Eom, S. H., Chun, C. & Im, Y. J. Structure of the GH1 domain of guanylate kinase-Associated protein from Rattus norvegicus. Biochem Biophys Res Commun 452, 130-135 (2014).
60. Loohuis, L. M. et al. Genome-wide burden of deleterious coding variants increased in schizophrenia. Nat Commun 6, 7501 (2015).
61. De Rubeis, S. & Buxbaum, J. D. Recent advances in the genetics of autism spectrum disorder. Curr Neurol Neurosci Rep 15, 36 (2015).
62. Griswold, A. J. et al. Targeted massively parallel sequencing of autism spectrum disorder-Associated genes in a case control cohort reveals rare loss-of-function risk variants. Mol Autism 6, 43 (2015).
63. De Rubeis, S. et al. Synaptic, transcriptional and chromatin genes disrupted in autism. Nature 515, 209-215 (2014).
64. von Ossowski, I. et al. Crystal structure of the second PDZ domain of SAP97 in complex with a GluR-A C-terminal peptide. FEBS J 273, 5219-5229 (2006).
65. Dunn, H. A., Walther, C., Godin, C. M., Hall, R. A. & Ferguson, S. S. Role of SAP97 protein in the regulation of corticotropinreleasing factor receptor 1 endocytosis and extracellular signal-regulated kinase 1/2 signaling. J Biol Chem 288, 15023-15034 (2013).
66. Yokomaku, D. et al. ErbB1 receptor ligands attenuate the expression of synaptic scaffolding proteins, GRIP1 and SAP97, in developing neocortex. Neuroscience 136, 1037-1047 (2005).
67. Nonaka, M., Doi, T., Fujiyoshi, Y., Takemoto-Kimura, S. & Bito, H. Essential contribution of the ligand-binding beta B/beta C loop of PDZ1 and PDZ2 in the regulation of postsynaptic clustering, scaffolding, and localization of postsynaptic density-95. J Neurosci 26, 763-774 (2006).
68. Nagura, H. et al. Impaired synaptic clustering of postsynaptic density proteins and altered signal transmission in hippocampal neurons, and disrupted learning behavior in PDZ1 and PDZ2 ligand binding-deficient PSD-95 knockin mice. Mol Brain 5, 43 (2012).
69. Cao, C. et al. Impairment of TrkB-PSD-95 signaling in Angelman syndrome. PLoS Biol 11, e1001478 (2013).
70. Cohen, F. E. General-Principles of Protein-Structure. Journal of the American Society of Nephrology 5, 1842-1842 (1995).
71. Ptitsyn, O. B. Physical Principles of Protein-Structure and Protein Folding. Journal of Biosciences 8, 1-13 (1985).
72. Hong, E. P. & Park, J. W. Sample size and statistical power calculation in genetic association studies. Genomics Inform 10, 117-122 (2012).