De novo mutations from sporadic schizophrenia cases highlight important signaling genes in an independent sample

Schizophrenia Research

Volumn 166, Issue 1-3, 2015, Pages 119-124

  Kranz, Thorsten M ^a   Harroch, Sheila ^b   Manor, Orly ^c   Lichtenberg, Pesach ^d   Friedlander, Yechiel ^d   Seandel, Marco ^e   Harkavy Friedman, Jill ^f   Walsh Messinger, Julie ^g   Dolgalev, Igor ^h   Heguy, Adriana ^h   Chao, Moses V ^a   Malaspina, Dolores ^g,i  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b INSTITUT PASTEUR   (France)

^c HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

^d HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^e WEILL CORNELL MEDICAL COLLEGE   (United States)

^f American Foundation for Suicide Prevention   (United States)

^g NEW YORK UNIVERSITY   (United States)

^h NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

ⁱ Creedmoor Psychiatric Center   (United States)

Author keywords

De novo; Exome sequencing; Paternal age; PTPRG: rare variant; Schizophrenia

Indexed keywords

BRUTON TYROSINE KINASE; PTPRG PROTEIN, HUMAN; RECEPTOR LIKE PROTEIN TYROSINE PHOSPHATASE;

ARTICLE; BTK GENE; CDKN3 GENE; CLINICAL ARTICLE; CONTROLLED STUDY; ETHNICITY; FEMALE; GENE; GENE IDENTIFICATION; GENE SEQUENCE; GENETIC VARIABILITY; HUMAN; MALE; MISSENSE MUTATION; PATHOGENESIS; PRIORITY JOURNAL; PTPRG GENE; SCHIZOPHRENIA; SEQUENCE ALIGNMENT; SINGLE NUCLEOTIDE POLYMORPHISM; SINGLE NUCLEOTIDE VARIANT; SLC39A13 GENE; STOP CODON; TGM5 GENE; ADULT; CASE REPORT; DNA SEQUENCE; ETHNOLOGY; GENETIC PREDISPOSITION; GENETICS; INFORMATION PROCESSING; ISRAEL; MUTATION; NEW YORK; PARENT; PSYCHOSIS;

ADULT; DATASETS AS TOPIC; FEMALE; GENETIC PREDISPOSITION TO DISEASE; HUMANS; ISRAEL; MALE; MUTATION; NEW YORK; PARENTS; PSYCHOTIC DISORDERS; RECEPTOR-LIKE PROTEIN TYROSINE PHOSPHATASES, CLASS 5; SCHIZOPHRENIA; SEQUENCE ANALYSIS, DNA;

EID: 84955212306     PISSN: 09209964     EISSN: 15732509     Source Type: Journal    
DOI: 10.1016/j.schres.2015.05.042     Document Type: Article

References (39)

1. Alipour, A., Shojaee, S., Mohebali, M., Tehranidoost, M., Masoleh, F.A., Keshavarz, H., 2011. Toxoplasma infection in schizophrenia patients: a comparative study with control group. Iran. J. Parasitol. 6 (2), 31-37.
2. Bienvenu, O.J., Samuels, J.F., Riddle, M.A., Hoehn-Saric, R., Liang, K.Y., Cullen, B.A.M., Grados, M.A., Nestadt, G., 2000. The relationship of obsessive-compulsive disorder to possible spectrum disorders: results from a family study. Biol. Psychiatry 48 (4), 287-293.
3. Brown, A.S., Schaefer, C.A., Wyatt, R.J., Begg, M.D., Goetz, R., Bresnahan, M.A., Harkavy-Friedman, J., Gorman, J.M., Malaspina, D., Susser, E.S., 2002. Paternal age and risk of schizophrenia in adult offspring. Am. J. Psychiatry 159 (9), 1528-1533.
4. Byrne, M., Agerbo, E., Bennedsen, B., Eaton, W.W., Mortensen, P.B., 2007 Dec. Obstetric conditionsand risk of first admission with schizophrenia: a Danish national register based study. Schizophr. Res. 97 (1-3), 51-59 Epub 2007 Aug 31. PubMed PMID: 17764905.
5. Cascella, N.G., Schretlen, D.J., Sawa, A., 2009 Apr. Schizophrenia and epilepsy: is there a shared susceptibility? Neurosci. Res. 63 (4), 227-235 Review. PubMed PMID: 19367784; PubMed Central PMCID: PMC2768382.
6. Crow, J.F., 2000. The origins, patterns and implications of human spontaneous mutation. Nature reviews. Genetics 1 (1), 40-47.
7. Davies, A.M., Prywes, R., Tzur, B., Weiskopf, P., Sterk, V.V., 1969. The Jerusalem perinatal study. 1. Design and organization of a continuing, community-based, record-linked survey. Isr. J. Med. Sci. 5 (6), 1095-1106.
8. De Rubeis, S., He, X., Goldberg, A.P., Poultney, C.S., Samocha, K., Ercument Cicek, A., Kou, Y., Liu, L., Fromer, M., Walker, S., Singh, T., Klei, L., Kosmicki, J., Fu, S.-C., Aleksic, B., Biscaldi, M., Bolton, P.F., Brownfeld, J.M., Cai, J., Campbell, N.G., Carracedo, A., Chahrour, M.H., Chiocchetti, A.G., Coon, H., Crawford, E.L., Crooks, L., Curran, S.R., Dawson, G., Duketis, E., Fernandez, B.A., Gallagher, L., Geller, E., Guter, S.J., Sean Hill, R., Ionita-Laza, I., Jimenez Gonzalez, P., Kilpinen, H., Klauck, S.M., Kolevzon, A., Lee, I., Lei, J., Lehtimaki, T., Lin, C.-F., Ma/'ayan, A., Marshall, C.R., McInnes, A.L., Neale, B., Owen, M.J., Ozaki, N., Parellada, M., Parr, J.R., Purcell, S., Puura, K., Rajagopalan, D., Rehnstrom, K., Reichenberg, A., Sabo, A., Sachse, M., Sanders, S.J., Schafer, C., Schulte-Ruther, M., Skuse, D., Stevens, C., Szatmari, P., Tammimies, K., Valladares, O., Voran, A., Wang, L.-S., Weiss, L.A., Jeremy Willsey, A., Yu, T.W., Yuen, R.K.C., The, D.D.D.S., Homozygosity Mapping Collaborative for, A., Consortium, U.K., The Autism Sequencing, C., Cook, E.H., Freitag, C.M., Gill, M., Hultman, C.M., Lehner, T., Palotie, A., Schellenberg, G.D., Sklar, P., State, M.W., Sutcliffe, J.S., Walsh, C.A., Scherer, S.W., Zwick, M.E., Barrett, J.C., Cutler, D.J., Roeder, K., Devlin, B., Daly, M.J., Buxbaum, J.D., 2014. Synaptic, Transcriptional and Chromatin Genes Disrupted in Autism. Nature 515 (7526), 209-215.
9. Dong, S., Walker, Michael F., Carriero, Nicholas J., DiCola, M., Willsey, A.J., Ye, Adam Y., Waqar, Z., Gonzalez, Luis E., Overton, John D., Frahm, S., Iii, Keaney, John, F., Teran, Nicole A., Dea, J., Mandell, Jeffrey D., Hus Bal, V., Sullivan, Catherine A., DiLullo, Nicholas M., Khalil, Rehab O., Gockley, J., Yuksel, Z., Sertel, Sinem M., Ercan-Sencicek, A.G., Gupta, Abha R., Mane, Shrikant M., Sheldon, M., Brooks, Andrew I., Roeder, K., Devlin, B., State, Matthew W., Wei, L., Sanders, Stephan J., 2014. De novo insertions and deletions of predominantly paternal origin are associated with autism spectrum disorder. Cell Rep. 9 (1), 16-23.
10. Doody, G.A., Johnstone, E.C., Sanderson, T.L., Owens, D.G., Muir, W.J., 1998 Aug. 'Pfropfschizophrenie' revisited. Schizophrenia in people with mild learning disability. Br. J. Psychiatry. 173, 145-153 PubMed PMID: 9850227.
11. Doty, R.L., Shaman, P., Dann, M., 1984. Development of the University of Pennsylvania Smell Identification Test: a standardized microencapsulated test of olfactory function. Physiol. Behav. 32 (3), 489-502.
12. Fromer, M., Pocklington, A.J., Kavanagh, D.H., Williams, H.J., Dwyer, S., Gormley, P., Georgieva, L., Rees, E., Palta, P., Ruderfer, D.M., Carrera, N., Humphreys, I., Johnson, J.S., Roussos, P., Barker, D.D., Banks, E., Milanova, V., Grant, S.G., Hannon, E., Rose, S.A., Chambert, K., Mahajan, M., Scolnick, E.M., Moran, J.L., Kirov, G., Palotie, A., McCarroll, S.A., Holmans, P., Sklar, P., Owen, M.J., Purcell, S.M., O/'Donovan, M.C., 2014. De novo mutations in schizophrenia implicate synaptic networks. Nature 506 (7487), 179-184.
13. Fukada, T., Civic, N., Furuichi, T., Shimoda, S., Mishima, K., Higashiyama, H., Idaira, Y., Asada, Y., Kitamura, H., Yamasaki, S., Hojyo, S., Nakayama, M., Ohara, O., Koseki, H., dos Santos, H.G., Bonafe, L., Ha-Vinh, R., Zankl, A., Unger, S., Kraenzlin, M.E., Beckmann, J.S., Saito, I., Rivolta, C., Ikegawa, S., Superti-Furga, A., Hirano, T., 2008. The zinc transporter SLC39A13/ZIP13 is required for connective tissue development; its involvement in BMP/TGF-beta signaling pathways. Plos One 3 (11).
14. Goriely, A., McGrath, J.J., Hultman, C.M., Wilkie, A.O., Malaspina, D., 2013. "Selfish spermatogonial selection": a novel mechanism for the association between advanced paternal age and neurodevelopmental disorders. Am. J. Psychiatry 170 (6), 599-608.
15. Gyuris, J., Golemis, E., Chertkov, H., Brent, R., 1993. Cdi1, a human G1-phase and S-phase protein phosphatase that associates with Cdk2. Cell 75 (4), 791-803.
16. Harlap, S., Davies, A.M., Deutsch, L., Calderon-Margalit, R., Manor, O., Paltiel, O., Tiram, E., Yanetz, R., Perrin, M.C., Terry, M.B., Malaspina, D., Friedlander, Y., 2007. The Jerusalem Perinatal Study cohort, 1964-2005: methods and a review of the main results. Paediatr. Perinat. Epidemiol. 21 (3), 256-273.
17. Hyvonen, M., Saraste, M., 1997. Structure of the PH domain and Btk motif from Bruton's tyrosine kinase: molecular explanations for X-linked agammaglobulinaemia. Embo J. 16 (12), 3396-3404.
18. Jeste, D.V., Heaton, S.C., Paulsen, J.S., Ercoli, L., Harris, J., Heaton, R.K., 1996 Apr. Clinical andneuropsychological comparison of psychotic depression with nonpsychoticdepression and schizophrenia. Am. J. Psychiatry. 153 (4), 490-496 PubMed PMID: 8599396.
19. Lamprianou, S., Vacaresse, N., Suzuki, Y., Meziane, H., Buxbaum, J.D., Schlessinger, J., Harroch, S., 2006. Receptor protein tyrosine phosphatase gamma is a marker for pyramidal cells and sensory neurons in the nervous systemand is not necessary for normal development. Mol. Cell. Biol. 26 (13), 5106-5119.
20. Lee, S.W., Reimer, C.L., Fang, L., Iruela-Arispe, M.L., Aaronson, S.A., 2000. Overexpression of kinase-associated phosphatase (KAP) in breast and prostate cancer and inhibition of the transformed phenotype by antisense KAP expression. Mol. Cell. Biol. 20 (5), 1723-1732.
21. Lorenzetto, E., Moratti, E., Vezzalini, M., Harroch, S., Sorio, C., Buffelli, M., 2014. Distribution of different isoforms of receptor protein tyrosine phosphatase gamma (Ptprg-RPTP gamma) in adult mouse brain: upregulation during neuroinflammation. Brain Struct. Funct. 219 (3), 875-890.
22. Malaspina, D., 2001. Paternal factors and schizophrenia risk: de novo mutations and imprinting. Schizophr. Bull. 27 (3), 379-393.
23. Malaspina, D., Harlap, S., Fennig, S., Heiman, D., Nahon, D., Feldman, D., Susser, E.S., 2001. Advancing paternal age and the risk of schizophrenia. Arch. Gen. Psychiatry 58 (4), 361-367.
24. McCarroll, S.A., Feng, G., Hyman, S.E., 2014. Genome-scale neurogenetics: methodology and meaning. Nat. Neurosci. 17 (6), 756-763.
25. Milekic, M.H., Xin, Y., O'Donnell, A., Kumar, K.K., Bradley-Moore, M., Malaspina, D., Moore, H., Brunner, D., Ge, Y., Edwards, J., Paul, S., Haghighi, F.G., Gingrich, J.A., 2014. Agerelated sperm DNA methylation changes are transmitted to offspring and associated with abnormal behavior and dysregulated gene expression. Mol. Psychiatry [Epup ahead of print].
26. Network Pathway Analysis Subgroup of the Psychiatric Genomics, 2015. Psychiatric genome-wide association study analyses implicate neuronal, immune and histone pathways. Nat. Neurosci. 18 (2), 199-209.
27. Nurnberger Jr., J.I., Blehar, M.C., Kaufmann, C.A., York-Cooler, C., Simpson, S.G., Harkavy-Friedman, J., Severe, J.B., Malaspina, D., Reich, T., 1994. Diagnostic interviewfor genetic studies. Rationale, unique features, and training. NIMH Genetics Initiative. Arch. Gen. Psychiatry 51 (11), 849-859 (discussion 863-844).
28. Penrose, L.S., 1955. Parental age and mutation. Lancet 269 (6885), 312-313.
29. Pietersen, C.Y., Mauney, S.A., Kim, S.S., Lim, M.P., Rooney, R.J., Goldstein, J.M., Petryshen, T.L., Seidman, L.J., Shenton, M.E., McCarley, R.W., Sonntag, K.C., Woo, T.U.W., 2014. Molecular profiles of pyramidal neurons in the superior temporal cortex in schizophrenia. J. Neurogenet. 28 (1-2), 53-69.
30. Purcell, S.M., Moran, J.L., Fromer, M., Ruderfer, D., Solovieff, N., Roussos, P., O/'Dushlaine, C., Chambert, K., Bergen, S.E., Kahler, A., Duncan, L., Stahl, E., Genovese, G., Fernandez, E., Collins, M.O., Komiyama, N.H., Choudhary, J.S., Magnusson, P.K.E., Banks, E., Shakir, K., Garimella, K., Fennell, T., DePristo, M., Grant, S.G.N., Haggarty, S.J., Gabriel, S., Scolnick, E.M., Lander, E.S., Hultman, C.M., Sullivan, P.F., McCarroll, S.A., Sklar, P., 2014. A polygenic burden of rare disruptivemutations in schizophrenia. Nature 506 (7487), 185-190.
31. Sipos, A., Rasmussen, F., Harrison, G., Tynelius, P., Lewis, G., Leon, D.A., Gunnell, D., 2004. Paternal age and schizophrenia: a population based cohort study. BMJ 329 (7474), 1070.
32. Takata, A., Xu, B., Ionita-Laza, I., Roos, J.L., Gogos, J.A., Karayiorgou, M., 2014. Loss-of-function variants in schizophrenia risk and SETD1A as a candidate susceptibility gene. Neuron 82 (4), 773-780.
33. Tsuchiya, K.J., Takagai, S., Kawai, M., Matsumoto, H., Nakamura, K., Minabe, Y., Mori, N., Takei, N., 2005. Advanced paternal age associated with an elevated risk for schizophrenia in offspring in a Japanese population. Schizophr. Res. 76 (2-3), 337-342.
34. Vetrie, D., Vorechovsky, I., Sideras, P., Holland, J., Davies, A., Flinter, F., Hammarstrom, L., Kinnon, C., Levinsky, R., Bobrow, M., Smith, C.I.E., Bentley, D.R., 2012. The gene involved in X-linked agammaglobulinaemia is member of the src family of proteintyrosine kinases (reprinted from nature, vol 391, pg 226, 1993). J. Immunol. 188 (7), 2948-2955.
35. Wechsler, D.S., 1999. Wechsler Abbreviated Scale of Intelligence.
36. White, L., Harvey, P.D., Opler, L., Lindenmayer, J.P., 1997. Empirical assessment of the factorial structure of clinical symptoms in schizophrenia. A multisite, multimodel evaluation of the factorial structure of the Positive and Negative Syndrome Scale. The PANSS Study Group. Psychopathology 30 (5), 263-274.
37. Xu, B., Roos, J.L., Dexheimer, P., Boone, B., Plummer, B., Levy, S., Gogos, J.A., Karayiorgou, M., 2011. Exome sequencing supports a de novomutational paradigm for schizophrenia. Nat. Genet. 43 (9), 864-868.
38. Yang, J., Visscher, P.M., Wray, N.R., 2009. Sporadic cases are the norm for complex disease. Eur. J. Hum. Genet. 18 (9), 1039-1043. http://dx.doi.org/10.1038/ejhg.2009.177 Epub 2009 Oct 14. Erratum in: Eur. J. Hum. Genet. 2010 Sep;18 (9), 1044. PubMed PMID: 19826454; PubMed Central PMCID: PMC2987426.
39. Zammit, S., Allebeck, P., Dalman, C., Lundberg, I., Hemmingson, T., Owen, M.J., Lewis, G., 2003. Paternal age and risk for schizophrenia. Br. J. Psychiatry J. Ment. Sci. 183, 405-408.