Genome-wide investigation of schizophrenia associated plasma Ndel1 enzyme activity

Schizophrenia Research

Volumn 172, Issue 1-3, 2016, Pages 60-67

  Gadelha, Ary ^a   Coleman, Jonathan ^b   Breen, Gerome ^b   Mazzoti, Diego Robles ^a   Yonamine, Camila M ^a   Pellegrino, Renata ^c   Ota, Vanessa Kiyomi ^a   Belangero, Sintia Iole ^a   Glessner, Joseph ^c   Sleiman, Patrick ^c,d   Hakonarson, Hakon ^c,d   Hayashi, Mirian A F ^a   Bressan, Rodrigo A ^a  

^a FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Biomarker; Enzyme activity; GWAS; Ndel1; Schizophrenia

Indexed keywords

BINDING PROTEIN; NUCLEAR DISTRIBUTION ELEMENT LIKE 1 PROTEIN; UNCLASSIFIED DRUG; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE I; CAMK1D PROTEIN, HUMAN; CARRIER PROTEIN; CELL CYCLE PROTEIN; DNA BINDING PROTEIN; MAD1L1 PROTEIN, HUMAN; MAGI2 PROTEIN, HUMAN; NDEL1 PROTEIN, HUMAN; NUCLEAR PROTEIN; TRANSCRIPTION FACTOR; ZFPM2 PROTEIN, HUMAN;

ADULT; ARTICLE; CAMK1D GENE; CCDC25 GENE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME BLOOD LEVEL; FEMALE; GABGR3 GENE; GENE; GENETIC ASSOCIATION; GENETIC VARIABILITY; GENOTYPE; HUMAN; MAD1L1 GENE; MAGI2 GENE; MAJOR CLINICAL STUDY; MALE; MOLECULAR PHYLOGENY; PRIORITY JOURNAL; SCHIZOPHRENIA; ZFPM2 GENE; BLOOD; EDUCATIONAL STATUS; ENZYMOLOGY; GENETICS; GENOME-WIDE ASSOCIATION STUDY; SINGLE NUCLEOTIDE POLYMORPHISM;

ADULT; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 1; CARRIER PROTEINS; CELL CYCLE PROTEINS; DNA-BINDING PROTEINS; EDUCATIONAL STATUS; FEMALE; GENOME-WIDE ASSOCIATION STUDY; HUMANS; MALE; NUCLEAR PROTEINS; POLYMORPHISM, SINGLE NUCLEOTIDE; SCHIZOPHRENIA; TRANSCRIPTION FACTORS;

EID: 84956607233     PISSN: 09209964     EISSN: 15732509     Source Type: Journal    
DOI: 10.1016/j.schres.2016.01.043     Document Type: Article

References (68)

1. Barrett A.J., Rawlings N.D. Oligopeptidases, and the emergence of the prolyl oligopeptidase family. Biol. Chem. Hoppe Seyler 1992, 373(7):353-360.
2. Bradshaw N.J., Christie S., Soares D.C., Carlyle B.C., Porteous D.J., Millar J.K. NDE1 and NDEL1: multimerisation, alternate splicing and DISC1 interaction. Neurosci. Lett. 2009, 449(3):228-233.
3. 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. Disrupted in Schizophrenia 1 and Nudel form a neurodevelopmentally regulated protein complex: implications for schizophrenia and other major neurological disorders. Mol. Cell. Neurosci. 2004, 25(1):42-55.
4. Burdick K.E., Kamiya A., Hodgkinson C.A., Lencz T., DeRosse P., Ishizuka K., Elashvili S., Arai H., Goldman D., Sawa A., Malhotra A.K. Elucidating the relationship between DISC1, NDEL1 and NDE1 and the risk for schizophrenia: evidence of epistasis and competitive binding. Hum. Mol. Genet. 2008, 17(16):2462-2473.
5. Camargo A.C., Caldo H., Reis M.L. Susceptibility of a peptide derived from bradykinin to hydrolysis by brain endo-oligopeptidases and pancreatic proteinases. J. Biol. Chem. 1979, 254(12):5304-5307.
6. Camargo L.M., Collura V., Rain J.C., Mizuguchi K., Hermjakob H., Kerrien S., Bonnert T.P., Whiting P.J., Brandon N.J. Disrupted in Schizophrenia 1 Interactome: evidence for the close connectivity of risk genes and a potential synaptic basis for schizophrenia. Mol. Psychiatry 2007, 12(1):74-86.
7. Chan M.K., Gottschalk M.G., Haenisch F., Tomasik J., Ruland T., Rahmoune H., Guest P.C., Bahn S. Applications of blood-based protein biomarker strategies in the study of psychiatric disorders. Prog. Neurobiol. 2014, 122:45-72.
8. Chin D., Means A.R. Calmodulin: a prototypical calcium sensor. Trends Cell Biol. 2000, 10(8):322-328.
9. Deng F., Price M.G., Davis C.F., Mori M., Burgess D.L. Stargazin and other transmembrane AMPA receptor regulating proteins interact with synaptic scaffolding protein MAGI-2 in brain. J. Neurosci. 2006, 26(30):7875-7884.
10. Derewenda U., Tarricone C., Choi W.C., Cooper D.R., Lukasik S., Perrina F., Tripathy A., Kim M.H., Cafiso D.S., Musacchio A., Derewenda Z.S. The structure of the coiled-coil domain of Ndel1 and the basis of its interaction with Lis1, the causal protein of Miller-Dieker lissencephaly. Structure 2007, 15(11):1467-1481.
11. 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. Disrupted-In-Schizophrenia 1 regulates integration of newly generated neurons in the adult brain. Cell 2007, 130(6):1146-1158.
12. Dudbridge F., Gusnanto A. Estimation of significance thresholds for genomewide association scans. Genet. Epidemiol. 2008, 32(3):227-234.
13. Emtage L., Chang H., Tiver R., Rongo C. MAGI-1 modulates AMPA receptor synaptic localization and behavioral plasticity in response to prior experience. PLoS One 2009, 4(2).
14. Fei E., Ma X., Zhu C., Xue T., Yan J., Xu Y., Zhou J., Wang G. Nucleocytoplasmic shuttling of dysbindin-1, a schizophrenia-related protein, regulates synapsin I expression. J. Biol. Chem. 2010, 285(49):38630-38640.
15. Gadelha A., Machado M.F., Yonamine C.M., Sato J.R., Juliano M.A., Oliveira V., Bressan R.A., Hayashi M.A. Plasma Ndel1 enzyme activity is reduced in patients with schizophrenia-a potential biomarker?. J. Psychiatr. Res. 2013, 47(5):657-663.
16. Gadelha A., Vendramini A.M., Yonamine C.M., Nering M., Berberian A., Suiama M.A., Oliveira V., Lima-Landman M.T., Breen G., Bressan R.A., Abilio V., Hayashi M.A. Convergent evidences from human and animal studies implicate angiotensin I-converting enzyme activity in cognitive performance in schizophrenia. Transl. Psychiatry 2015, 5.
17. Gadelha A., Yonamine C.M., Nering M., Rizzo L.B., Noto C., Cogo-Moreira H., Teixeira A.L., Bressan R., Maes M., Brietzke E., Hayashi M.A. Angiotensin converting enzyme activity is positively associated with IL-17a levels in patients with schizophrenia. Psychiatry Res. 2015, 229(3):702-707.
18. Girirajan S., Brkanac Z., Coe B.P., Baker C., Vives L., Vu T.H., Shafer N., Bernier R., Ferrero G.B., Silengo M., Warren S.T., Moreno C.S., Fichera M., Romano C., Raskind W.H., Eichler E.E. Relative burden of large CNVs on a range of neurodevelopmental phenotypes. PLoS Genet. 2011, 7(11).
19. Giusti-Rodriguez P., Sullivan P.F. The genomics of schizophrenia: update and implications. J. Clin. Invest. 2013, 123(11):4557-4563.
20. Grarup N., Andersen G., Krarup N.T., Albrechtsen A., Schmitz O., Jorgensen T., Borch-Johnsen K., Hansen T., Pedersen O. Association testing of novel type 2 diabetes risk alleles in the JAZF1, CDC123/CAMK1D, TSPAN8, THADA, ADAMTS9, and NOTCH2 loci with insulin release, insulin sensitivity, and obesity in a population-based sample of 4,516 glucose-tolerant middle-aged Danes. Diabetes 2008, 57(9):2534-2540.
21. Gratten J., Wray N.R., Keller M.C., Visscher P.M. Large-scale genomics unveils the genetic architecture of psychiatric disorders. Nat. Neurosci. 2014, 17(6):782-790.
22. Greenbaum L., Smith R.C., Lorberboym M., Alkelai A., Zozulinsky P., Lifschytz T., Kohn Y., Djaldetti R., Lerer B. Association of the ZFPM2 gene with antipsychotic-induced parkinsonism in schizophrenia patients. Psychopharmacology 2012, 220(3):519-528.
23. Guerreiro J.R., Winnischofer S.M., Bastos M.F., Portaro F.C., Sogayar M.C., de Camargo A.C., Hayashi M.A. Cloning and characterization of the human and rabbit NUDEL-oligopeptidase promoters and their negative regulation. Biochim. Biophys. Acta 2005, 1730(1):77-84.
24. Haney S., Zhao J., Tiwari S., Eng K., Guey L.T., Tien E. RNAi screening in primary human hepatocytes of genes implicated in genome-wide association studies for roles in type 2 diabetes identifies roles for CAMK1D and CDKAL1, among others, in hepatic glucose regulation. PLoS One 2013, 8(6).
25. Hayashi M.A., Portaro F.C., Tambourgi D.V., Sucupira M., Yamane T., Fernandes B.L., Ferro E.S., Reboucas N.A., de Camargo A.C. Molecular and immunochemical evidences demonstrate that endooligopeptidase A is the predominant cytosolic oligopeptidase of rabbit brain. Biochem. Biophys. Res. Commun. 2000, 269(1):7-13.
26. Hayashi M.A., Portaro F.C., Bastos M.F., Guerreiro J.R., Oliveira V., Gorrao S.S., Tambourgi D.V., Sant'Anna O.A., Whiting P.J., Camargo L.M., Konno K., Brandon N.J., Camargo A.C. Inhibition of NUDEL (nuclear distribution element-like)-oligopeptidase activity by disrupted-in-schizophrenia 1. Proc. Natl. Acad. Sci. U. S. A. 2005, 102(10):3828-3833.
27. Hayashi M.A., Guerreiro J.R., Charych E., Kamiya A., Barbosa R.L., Machado M.F., Campeiro J.D., Oliveira V., Sawa A., Camargo A.C., Brandon N.J. Assessing the role of endooligopeptidase activity of Ndel1 (nuclear-distribution gene E homolog like-1) in neurite outgrowth. Mol. Cell. Neurosci. 2010, 44(4):353-361.
28. Howie B.N., Donnelly P., Marchini J. A flexible and accurate genotype imputation method for the next generation of genome-wide association studies. PLoS Genet. 2009, 5(6).
29. Jia P., Wang L., Fanous A.H., Pato C.N., Edwards T.L., Zhao Z. Network-assisted investigation of combined causal signals from genome-wide association studies in schizophrenia. PLoS Comput. Biol. 2012, 8(7).
30. Kahler A.K., Djurovic S., Kulle B., Jonsson E.G., Agartz I., Hall H., Opjordsmoen S., Jakobsen K.D., Hansen T., Melle I., Werge T., Steen V.M., Andreassen O.A. Association analysis of schizophrenia on 18 genes involved in neuronal migration: MDGA1 as a new susceptibility gene. Am. J. Med. Genet. B Neuropsychiatr. Genet. 2008, 147B(7):1089-1100.
31. 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. A schizophrenia-associated mutation of DISC1 perturbs cerebral cortex development. Nat. Cell Biol. 2005, 7(12):1167-1178.
32. Kamiya A., Tomoda T., Chang J., Takaki M., Zhan C., Morita M., Cascio M.B., Elashvili S., Koizumi H., Takanezawa Y., Dickerson F., Yolken R., Arai H., Sawa A. DISC1-NDEL1/NUDEL protein interaction, an essential component for neurite outgrowth, is modulated by genetic variations of DISC1. Hum. Mol. Genet. 2006, 15(22):3313-3323.
33. Kang H.M., Sul J.H., Service S.K., Zaitlen N.A., Kong S.Y., Freimer N.B., Sabatti C., Eskin E. Variance component model to account for sample structure in genome-wide association studies. Nat. Genet. 2010, 42(4):348-354.
34. Kawanishi Y., Harada S., Tachikawa H., Okubo T., Shiraishi H. Novel variants in the promoter region of the CREB gene in schizophrenic patients. J. Hum. Genet. 1999, 44(6):428-430.
35. Kohannim O., Hibar D.P., Stein J.L., Jahanshad N., Hua X., Rajagopalan P., Toga A.W., Jack C.R., Weiner M.W., de Zubicaray G.I., McMahon K.L., Hansell N.K., Martin N.G., Wright M.J., Thompson P.M. Discovery and replication of gene influences on brain structure using LASSO regression. Front. Neurosci. 2012, 6:115.
36. Koide T., Banno M., Aleksic B., Yamashita S., Kikuchi T., Kohmura K., Adachi Y., Kawano N., Kushima I., Nakamura Y., Okada T., Ikeda M., Ohi K., Yasuda Y., Hashimoto R., Inada T., Ujike H., Iidaka T., Suzuki M., Takeda M., Iwata N., Ozaki N. Common variants in MAGI2 gene are associated with increased risk for cognitive impairment in schizophrenic patients. PLoS One 2012, 7(5).
37. Kuta A., Deng W., Morsi El-Kadi A., Banks G.T., Hafezparast M., Pfister K.K., Fisher E.M. Mouse cytoplasmic dynein intermediate chains: identification of new isoforms, alternative splicing and tissue distribution of transcripts. PLoS One 2010, 5(7).
38. Liao H.M., Chao Y.L., Huang A.L., Cheng M.C., Chen Y.J., Lee K.F., Fang J.S., Hsu C.H., Chen C.H. Identification and characterization of three inherited genomic copy number variations associated with familial schizophrenia. Schizophr. Res. 2012, 139(1-3):229-236.
39. Lipska B.K., Peters T., Hyde T.M., Halim N., Horowitz C., Mitkus S., Weickert C.S., Matsumoto M., Sawa A., Straub R.E., Vakkalanka R., Herman M.M., Weinberger D.R., Kleinman J.E. Expression of DISC1 binding partners is reduced in schizophrenia and associated with DISC1 SNPs. Hum. Mol. Genet. 2006, 15(8):1245-1258.
40. Lukusa T., Fryns J.P. Human chromosome fragility. Biochim. Biophys. Acta 2008, 1779(1):3-16.
41. 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. Disruption of two novel genes by a translocation co-segregating with schizophrenia. Hum. Mol. Genet. 2000, 9(9):1415-1423.
42. Murray R.M., Lewis S.W. Is schizophrenia a neurodevelopmental disorder?. Br. Med. J. (Clin. Res. Ed.) 1987, 295(6600):681-682.
43. Nairn A.C., Greengard P. Purification and characterization of Ca2+/calmodulin-dependent protein kinase I from bovine brain. J. Biol. Chem. 1987, 262(15):7273-7281.
44. Nicodemus K.K., Callicott J.H., Higier R.G., Luna A., Nixon D.C., Lipska B.K., Vakkalanka R., Giegling I., Rujescu D., St Clair D., Muglia P., Shugart Y.Y., Weinberger D.R. Evidence of statistical epistasis between DISC1, CIT and NDEL1 impacting risk for schizophrenia: biological validation with functional neuroimaging. Hum. Genet. 2010, 127(4):441-452.
45. Nyarko A., Song Y., Barbar E. Intrinsic disorder in dynein intermediate chain modulates its interactions with NudE and dynactin. J. Biol. Chem. 2012, 287(30):24884-24893.
46. Paik S.H., Betti F., Camargo A.C., de Oliveira E.S. Presence of endo-oligopeptidase (EC 3.4.22.19), a putative neuropeptide-metabolizing endopeptidase in cells of the immune system. J. Neuroimmunol. 1992, 38(1-2):35-44.
47. Pletnikov M.V., Ayhan Y., Nikolskaia O., Xu Y., Ovanesov M.V., Huang H., Mori S., Moran T.H., Ross C.A. Inducible expression of mutant human DISC1 in mice is associated with brain and behavioral abnormalities reminiscent of schizophrenia. Mol. Psychiatry 2008, 13(2):173-186. (115).
48. Price A.L., Zaitlen N.A., Reich D., Patterson N. New approaches to population stratification in genome-wide association studies. nature reviews. Genetics 2010, 11(7):459-463.
49. Purcell S., Neale B., Todd-Brown K., Thomas L., Ferreira M.A., Bender D., Maller J., Sklar P., de Bakker P.I., Daly M.J., Sham P.C. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am. J. Hum. Genet. 2007, 81(3):559-575.
50. Ribeiro-dos-Santos A.M., de Souza J.E., Almeida R., Alencar D.O., Barbosa M.S., Gusmao L., Silva W.A., de Souza S.J., Silva A., Ribeiro-dos-Santos A., Darnet S., Santos S. High-throughput sequencing of a South American Amerindian. PLoS One 2013, 8(12).
51. Ripke S., O'Dushlaine C., Chambert K., Moran J.L., Kahler A.K., Akterin S., Bergen S.E., Collins A.L., Crowley J.J., Fromer M., Kim Y., Lee S.H., Magnusson P.K., Sanchez N., Stahl E.A., Williams S., Wray N.R., Xia K., Bettella F., Borglum A.D., Bulik-Sullivan B.K., Cormican P., Craddock N., de Leeuw C., Durmishi N., Gill M., Golimbet V., Hamshere M.L., Holmans P., Hougaard D.M., Kendler K.S., Lin K., Morris D.W., Mors O., Mortensen P.B., Neale B.M., O'Neill F.A., Owen M.J., Milovancevic M.P., Posthuma D., Powell J., Richards A.L., Riley B.P., Ruderfer D., Rujescu D., Sigurdsson E., Silagadze T., Smit A.B., Stefansson H., Steinberg S., Suvisaari J., Tosato S., Verhage M., Walters J.T., Levinson D.F., Gejman P.V., Laurent C., Mowry B.J., O'Donovan M.C., Pulver A.E., Schwab S.G., Wildenauer D.B., Dudbridge F., Shi J., Albus M., Alexander M., Campion D., Cohen D., Dikeos D., Duan J., Eichhammer P., Godard S., Hansen M., Lerer F.B., Liang K.Y., Maier W., Mallet J., Nertney D.A., Nestadt G., Norton N., Papadimitriou G.N., Ribble R., Sanders A.R., Silverman J.M., Walsh D., Williams N.M., Wormley B., Arranz M.J., Bakker S., Bender S., Bramon E., Collier D., Crespo-Facorro B., Hall J., Iyegbe C., Jablensky A., Kahn R.S., Kalaydjieva L., Lawrie S., Lewis C.M., Linszen D.H., Mata I., McIntosh A., Murray R.M., Ophoff R.A., Van Os J., Walshe M., Weisbrod M., Wiersma D., Donnelly P., Barroso I., Blackwell J.M., Brown M.A., Casas J.P., Corvin A.P., Deloukas P., Duncanson A., Jankowski J., Markus H.S., Mathew C.G., Palmer C.N., Plomin R., Rautanen A., Sawcer S.J., Trembath R.C., Viswanathan A.C., Wood N.W., Spencer C.C., Band G., Bellenguez C., Freeman C., Hellenthal G., Giannoulatou E., Pirinen M., Pearson R.D., Strange A., Su Z., Vukcevic D., Langford C., Hunt S.E., Edkins S., Gwilliam R., Blackburn H., Bumpstead S.J., Dronov S., Gillman M., Gray E., Hammond N., Jayakumar A., McCann O.T., Liddle J., Potter S.C., Ravindrarajah R., Ricketts M., Tashakkori-Ghanbaria A., Waller M.J., Weston P., Widaa S., Whittaker P., McCarthy M.I., Stefansson K., Scolnick E., Purcell S., McCarroll S.A., Sklar P., Hultman C.M., Sullivan P.F. Genome-wide association analysis identifies 13 new risk loci for schizophrenia. Nat. Genet. 2013, 45(10):1150-1159.
52. Ruderfer D.M., Fanous A.H., Ripke S., McQuillin A., Amdur R.L., Gejman P.V., O'Donovan M.C., Andreassen O.A., Djurovic S., Hultman C.M., Kelsoe J.R., Jamain S., Landen M., Leboyer M., Nimgaonkar V., Nurnberger J., Smoller J.W., Craddock N., Corvin A., Sullivan P.F., Holmans P., Sklar P., Kendler K.S. Polygenic dissection of diagnosis and clinical dimensions of bipolar disorder and schizophrenia. Mol. Psychiatry 2014, 19(9):1017-1024.
53. Sasaki S., Mori D., Toyo-oka K., Chen A., Garrett-Beal L., Muramatsu M., Miyagawa S., Hiraiwa N., Yoshiki A., Wynshaw-Boris A., Hirotsune S. Complete loss of Ndel1 results in neuronal migration defects and early embryonic lethality. Mol. Cell. Biol. 2005, 25(17):7812-7827.
54. Sassoe-Pognetto M., Frola E., Pregno G., Briatore F., Patrizi A. Understanding the molecular diversity of GABAergic synapses. Front. Cell. Neurosci. 2011, 5:4.
55. Saviouk V., Moreau M.P., Tereshchenko I.V., Brzustowicz L.M. Association of synapsin 2 with schizophrenia in families of Northern European ancestry. Schizophr. Res. 2007, 96(1-3):100-111.
56. Schizophrenia Working Group of the Psychiatric Genomics Consortium Biological insights from 108 schizophrenia-associated genetic loci. Nature 2014, 511(7510):421-427.
57. Sheng M., Thompson M.A., Greenberg M.E. CREB: a Ca(2+)-regulated transcription factor phosphorylated by calmodulin-dependent kinases. Science 1991, 252(5011):1427-1430.
58. Stetak A., Horndli F., Maricq A.V., van den Heuvel S., Hajnal A. Neuron-specific regulation of associative learning and memory by MAGI-1 in C. elegans. PLoS One 2009, 4(6):e6019.
59. 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 2003, 60(12):1187-1192.
60. Terao C., Bayoumi N., McKenzie C.A., Zelenika D., Muro S., Mishima M., Connell J.M., Vickers M.A., Lathrop G.M., Farrall M., Matsuda F., Keavney B.D. Quantitative variation in plasma angiotensin-I converting enzyme activity shows allelic heterogeneity in the ABO blood group locus. Ann. Hum. Genet. 2013, 77(6):465-471.
61. Toba S., Hirotsune S. A unique role of dynein and nud family proteins in corticogenesis. Neuropathology 2012, 32(4):432-439.
62. Tomppo L., Hennah W., Lahermo P., Loukola A., Tuulio-Henriksson A., Suvisaari J., Partonen T., Ekelund J., Lonnqvist J., Peltonen L. Association between genes of disrupted in schizophrenia 1 (DISC1) interactors and schizophrenia supports the role of the DISC1 pathway in the etiology of major mental illnesses. Biol. Psychiatry 2009, 65(12):1055-1062.
63. Verploegen S., Lammers J.W., Koenderman L., Coffer P.J. Identification and characterization of CKLiK, a novel granulocyte Ca(++)/calmodulin-dependent kinase. Blood 2000, 96(9):3215-3223.
64. Wassef A., Baker J., Kochan L.D. GABA and schizophrenia: a review of basic science and clinical studies. J. Clin. Psychopharmacol. 2003, 23(6):601-640.
65. Weinberger D.R. Implications of normal brain development for the pathogenesis of schizophrenia. Arch. Gen. Psychiatry 1987, 44(7):660-669.
66. Yang J., Lee S.H., Goddard M.E., Visscher P.M. GCTA: a tool for genome-wide complex trait analysis. Am. J. Hum. Genet. 2011, 88(1):76-82.
67. Zeggini E., Scott L.J., Saxena R., Voight B.F., Marchini J.L., Hu T., de Bakker P.I., Abecasis G.R., Almgren P., Andersen G., Ardlie K., Bostrom K.B., Bergman R.N., Bonnycastle L.L., Borch-Johnsen K., Burtt N.P., Chen H., Chines P.S., Daly M.J., Deodhar P., Ding C.J., Doney A.S., Duren W.L., Elliott K.S., Erdos M.R., Frayling T.M., Freathy R.M., Gianniny L., Grallert H., Grarup N., Groves C.J., Guiducci C., Hansen T., Herder C., Hitman G.A., Hughes T.E., Isomaa B., Jackson A.U., Jorgensen T., Kong A., Kubalanza K., Kuruvilla F.G., Kuusisto J., Langenberg C., Lango H., Lauritzen T., Li Y., Lindgren C.M., Lyssenko V., Marvelle A.F., Meisinger C., Midthjell K., Mohlke K.L., Morken M.A., Morris A.D., Narisu N., Nilsson P., Owen K.R., Palmer C.N., Payne F., Perry J.R., Pettersen E., Platou C., Prokopenko I., Qi L., Qin L., Rayner N.W., Rees M., Roix J.J., Sandbaek A., Shields B., Sjogren M., Steinthorsdottir V., Stringham H.M., Swift A.J., Thorleifsson G., Thorsteinsdottir U., Timpson N.J., Tuomi T., Tuomilehto J., Walker M., Watanabe R.M., Weedon M.N., Willer C.J., Illig T., Hveem K., Hu F.B., Laakso M., Stefansson K., Pedersen O., Wareham N.J., Barroso I., Hattersley A.T., Collins F.S., Groop L., McCarthy M.I., Boehnke M., Altshuler D. Meta-analysis of genome-wide association data and large-scale replication identifies additional susceptibility loci for type 2 diabetes. Nat. Genet. 2008, 40(5):638-645.
68. Zylkiewicz E., Kijanska M., Choi W.C., Derewenda U., Derewenda Z.S., Stukenberg P.T. The N-terminal coiled-coil of Ndel1 is a regulated scaffold that recruits LIS1 to dynein. J. Cell Biol. 2011, 192(3):433-445.