Genetic variation in the G72 gene is associated with increased frontotemporal fiber tract integrity

European Archives of Psychiatry and Clinical Neuroscience

Volumn 265, Issue 4, 2015, Pages 291-301

  Nickl Jockschat, Thomas ^a,b   Stöcker, Tony ^b,c   Krug, Axel ^d   Markov, Valentin ^a   Maximov, Ivan I ^c   Huang, Ruiwang ^b,c   Schneider, Frank ^a,b   Habel, Ute ^a,b   Eickhoff, Simon B ^c,e   Zerres, Klaus ^a   Nöthen, Markus M ^f   Rietschel, Marcella ^g   Jon Shah, N ^b,c,h   Treutlein, Jens ^g   Kircher, Tilo ^d  

^a RWTH AACHEN UNIVERSITY   (Germany)

^b Juelich Aachen Research Alliance   (Germany)

^c FORSCHUNGSZENTRUM JÜLICH   (Germany)

^d PHILIPPS UNIVERSITY MARBURG   (Germany)

^e HEINRICH HEINE UNIVERSITY   (Germany)

^f UNIVERSITY OF BONN   (Germany)

^g CENTRAL INSTITUTE OF MENTAL HEALTH   (Germany)

^h UNIVERSITY HOSPITAL RWTH AACHEN   (Germany)

Author keywords

Bipolar I disorder; Genetics; Imaging; MRI; Schizophrenia

Indexed keywords

ADULT; ARTICLE; CONTROLLED STUDY; DIFFUSION TENSOR IMAGING; FEMALE; FIBER TRACT INTEGRITY; FRACTIONAL ANISOTROPY; FRONTAL LOBE; G72 GENE; GENE; GENETIC ASSOCIATION; GENETIC SUSCEPTIBILITY; GENETIC VARIABILITY; GENOTYPE; HAPLOTYPE; HUMAN; HUMAN EXPERIMENT; INFERIOR PARIETAL LOBULE; INSULA; MALE; NERVE FIBER; NERVOUS SYSTEM PARAMETERS; NORMAL HUMAN; PRIORITY JOURNAL; TEMPORAL LOBE; ADOLESCENT; ANATOMY AND HISTOLOGY; CAUCASIAN; GENETICS; IMAGE PROCESSING; MIDDLE AGED; NONPARAMETRIC TEST; PHYSIOLOGY; YOUNG ADULT;

CARRIER PROTEIN; DAOA PROTEIN, HUMAN;

ADOLESCENT; ADULT; CARRIER PROTEINS; DIFFUSION TENSOR IMAGING; EUROPEAN CONTINENTAL ANCESTRY GROUP; FEMALE; FRONTAL LOBE; GENOTYPE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MALE; MIDDLE AGED; NERVE FIBERS; STATISTICS, NONPARAMETRIC; TEMPORAL LOBE; YOUNG ADULT;

EID: 84939418183     PISSN: 09401334     EISSN: 14338491     Source Type: Journal    
DOI: 10.1007/s00406-014-0516-6     Document Type: Article

References (79)

1. Nöthen MM, Nieratschker V, Cichon S, Rietschel M (2011) New findings in the genetics of major psychoses. Dialogues Clin Neurosci 12:85–93
2. Cardno AG, Rijsdijk FV, Sham PC, Murray RM, McGuffin P (2002) A twin study of genetic relationships between psychotic symptoms. Am J Psychiatry 159:539–545
3. Mortensen PB, Pedersen CB, Melbye M, Mors O, Ewald H (2003) Individual and familial risk factors for bipolar affective disorders in Denmark. Arch Gen Psychiatry 60:1209–1215
4. Van Snellenberg JX, de Candia T (2009) Meta-analytic evidence for familial coaggregation of schizophrenia and bipolar disorder. Arch Gen Psychiatry 66:748–755
5. Lichtenstein P, Yip BH, Björk C, Pawitan Y, Cannon TD, Sullivan PF, Hultman CM (2009) Common genetic determinants of schizophrenia and bipolar disorder in Swedish families: a population-based study. Lancet 373:234–239
6. Chumakov I, Blumenfeld M, Guerassimenko O, Cavarec L, Palicio M, Abderrahim H, Bougueleret L, Barry C, Tanaka H, La Rosa P, Puech A, Tahri N, Cohen-Akenine A, Delabrosse S, Lissarrague S, Picard FP, Maurice K, Essioux L, Millasseau P, Grel P, Debailleul V, Simon AM, Caterina D, Dufaure I, Malekzadeh K, Belova M, Luan JJ, Bouillot M, Sambucy JL, Primas G, Saumier M, Boubkiri N, Martin-Saumier S, Nasroune M, Peixoto H, Delaye A, Pinchot V, Bastucci M, Guillou S, Chevillon M, Sainz-Fuertes R, Meguenni S, Aurich-Costa J, Cherif D, Gimalac A, Van Duijn C, Gauvreau D, Ouellette G, Fortier I, Raelson J, Sherbatich T, Riazanskaia N, Rogaev E, Raeymaekers P, Aerssens J, Konings F, Luyten W, Macciardi F, Sham PC, Straub RE, Weinberger DR, Cohen N, Cohen D (2002) Genetic and physiological data implicating the new human gene G72 and the gene for D-amino acid oxidase in schizophrenia. Proc Natl Acad Sci USA 99:13675–13680
7. Addington AM, Gornick M, Sporn AL, Gogtay N, Greenstein D, Lenane M, Gochman P, Baker N, Balkissoon R, Vakkalanka RK, Weinberger DR, Straub RE, Rapoport JL (2004) Polymorphisms in the 13q33.2 gene G72/G30 are associated with childhood-onset schizophrenia and psychosis not otherwise specified. Biol Psychiatry 55:976–980
8. Li D, He L (2007) G72/G30 genes and schizophrenia: a systematic meta-analysis of association studies. Genetics 175:917–922
9. Ma J, Sun J, Zhang H, Zhang R, Kang WH, Gao CG, Liu HS, Ma XH, Min ZX, Zhao WX, Ning QL, Wang SH, Zhang YC, Guo TW, Lu SM (2009) Evidence for transmission disequilibrium at the DAOA gene locus in a schizophrenia family sample. Neurosci Lett 462(2):105–108
10. Bass NJ, Datta SR, McQuillin A, Puri V, Choudhury K, Thirumalai S, Lawrence J, Quested D, Pimm J, Curtis D, Gurling HM (2009) Evidence for the association of the DAOA (G72) gene with schizophrenia and bipolar disorder but not for the association of the DAO gene with schizophrenia. Behav Brain Funct 5:28
11. Schulze TG, Ohlraun S, Czerski PM, Schumacher J, Kassem L, Deschner M, Gross M, Tullius M, Heidmann V, Kovalenko S, Jamra RA, Becker T, Leszczynska-Rodziewicz A, Hauser J, Illig T, Klopp N, Wellek S, Cichon S, Henn FA, McMahon FJ, Maier W, Propping P, Nöthen MM, Rietschel M (2005) Genotype-phenotype studies in bipolar disorder showing association between the DAOA/G30 locus and persecutory delusions: a first step toward a molecular genetic classification of psychiatric phenotypes. Am J Psychiatry 162:2101–2108
12. Rietschel M, Beckmann L, Strohmaier J, Georgi A, Karpushova A, Schirmbeck F, Boesshenz KV, Schmäl C, Bürger C, Jamra RA, Schumacher J, Höfels S, Kumsta R, Entringer S, Krug A, Markov V, Maier W, Propping P, Wüst S, Kircher T, Nöthen MM, Cichon S, Schulze TG (2008) G72 and its association with major depression and neuroticism in large population-based groups from Germany. Am J Psychiatry 165:753–762
13. Schumacher J, Abou Jamra R, Becker T, Klopp N, Franke P, Jacob C, Sand P, Fritze J, Ohlraun S, Schulze TG, Rietschel M, Illig T, Propping P, Cichon S, Deckert J, Nöthen MM (2005) Investigation of the DAOA/G30 locus in panic disorder. Mol Psychiatry 10:428–429
14. Wang KS, Liu XF, Aragam N (2010) A genome-wide meta-analysis identifies novel loci associated with schizophrenia and bipolar disorder Schizophr Res 124:192–199
15. Berenbaum H, Fujita F (1994) Schizophrenia and personality: exploring the boundaries and connections between vulnerability and outcome. J Abnorm Psychol 103:148–158
16. Dinzeo TJ, Docherty NM (2007) Normal personality characteristics in schizophrenia: a review of the literature involving the FFM. J Nerv Ment Dis 195:421–429
17. Kendler KS, Gatz M, Gardner CO, Pedersen NL (2006) Personality and major depression: a Swedish longitudinal, population-based twin study. Arch Gen Psychiatry 63:1113–1120
18. Detera-Wadleigh SD, McMahon FJ (2006) G72/G30 in schizophrenia and bipolar disorder: review and meta-analysis. Biol Psychiatry 60:106–114
19. Shi J, Badner JA, Gershon ES, Liu C (2008) Allelic association of G72/G30 with schizophrenia and bipolar disorder: a comprehensive meta-analysis. Schizophr Res 98:89–97
20. Seifuddin F, Mahon PB, Judy J, Pirooznia M, Jancic D, Taylor J, Goes FS, Potash JB, Zandi PP (2012) Meta-analysis of genetic association studies on bipolar disorder. Am J Med Genet B Neuropsychiatr Gene 159B:508–518
21. Mothet JP, Parent AT, Wolosker H, Brady RO Jr, Linden DJ, Ferris CD, Rogawski MA, Snyder SH (2000) d-serine is an endogenous ligand for the glycine site of the N-methyl-D-aspartate receptor. Proc Natl Acad Sci USA 97:4926–4931
22. Sacchi S, Cappelletti P, Giovannardi S, Pollegioni L (2011) Evidence for the interaction of D-amino acid oxidase with pLG72 in a glial cell line. Mol Cell Neurosci 48:20–28
23. Drews E, Otte DM, Zimmer A (2012) Involvement of the primate specific gene G72 in schizophrenia: From genetic studies to pathomechanisms. Neurosci Biobehav Rev. doi:10.1016/j.neubiorev.2012.10.009
24. Korostishevsky M, Kremer I, Kaganovich M, Cholostoy A, Murad I, Muhaheed M, Bannoura I, Rietschel M, Dobrusin M, Bening-Abu-Shach U, Belmaker RH, Maier W, Ebstein RP, Navon R (2006) Transmission disequilibrium and haplotype analyses of the G72/G30 locus: suggestive linkage to schizophrenia in Palestinian Arabs living in the North of Israel. Am J Med Genet B Neuropsychiatr Genet 141B(1):91–95
25. Andreou D, Saetre P, Werge T, Andreassen OA, Agartz I, Sedvall GC, Hall H, Terenius L, Jönsson EG (2012) D-amino acid oxidase activator gene (DAOA) variation affects cerebrospinal fluid homovanillic acid concentrations in healthy Caucasians. Eur Arch Psychiatry Clin Neurosci 262:549–556
26. Kvajo M, Dhilla A, Swor DE, Karayiorgou M, Gogos JA (2007) Evidence implicating the candidate schizophrenia/bipolar disorder susceptibility gene G72 in mitochondrial function. Mol Psychiatry 13:685–696
27. Chang DT, Reynolds IJ (2006) Differences in mitochondrial movement and morphology in young and mature primary cortical neurons in culture. Neuroscience 141:727–736
28. Otte DM, Sommersberg B, Kudin A, Guerrero C, Albayram O, Filiou MD, Frisch P, Yilmaz O, Drews E, Turck CW, Bilkei-Gorzó A, Kunz WS, Beck H, Zimmer A (2011) N-acetyl cysteine treatment rescues cognitive deficits induced by mitochondrial dysfunction in G72/G30 transgenic mice. Neuropsychopharmacology 36:2233–2243
29. Filiou MD, Teplytska L, Otte DM, Zimmer A, Turck CW (2012) Myelination and oxidative stress alterations in the cerebellum of the G72/G30 transgenic schizophrenia mouse model. J Psychiatr Res 46(10):1359–1365
30. Cheng L, Hattori E, Nakajima A, Woehrle NS, Opal MD, Zhang C, Grennan K, Dulawa SC, Tang YP, Gershon ES, Liu C (2013) Expression of the G72/G30 gene in transgenic mice induces behavioral changes. Mol Psychiatry. doi:10.1038/mp.2012.185
31. Schmitt A, Hasan A, Gruber O, Falkai P (2011) Schizophrenia as a disorder of disconnectivity. Eur Arch Psychiatry Clin Neurosci 261:S150–S154
32. Beaulieu C (2002) The basis of anisotropic water diffusion in the nervous system—a technical review. NMR Biomed 15:435–455
33. Ono J, Harada K, Takahashi M, Maeda M, Ikenaka K, Sakurai K, Sakai N, Kagawa T, Fritz-Zieroth B, Nagai T (1995) Differentiation between dysmyelination and demyelination using magnetic resonance diffusional anisotropy. Brain Res 671:141–148
34. Gulani V, Webb AG, Duncan ID, Lauterbur PC (2001) Apparent diffusion tensor measurements in myelin-deficient rat spinal cords. Magn Reson Med 45:191–195
35. Sakuma H, Nomura Y, Takeda K, Tagami T, Nakagawa T, Tamagawa Y, Ishii Y, Tsukamoto T (1991) Adult and neonatal human brain: diffusional anisotropy and myelination with diffusion-weighted MR imaging. Radiology 180:229–233
36. Ellison-Wright I, Bullmore E (2009) Meta-analysis of diffusion tensor imaging studies in schizophrenia. Schizophr Res 108:3–10
37. Ford JM, Mathalon DH, Whitfield S, Faustman WO, Roth WT (2002) Reduced communication between frontal and temporal lobes during talking in schizophrenia. Biol Psychiatry 51:485–492
38. Hubl D, Koenig T, Strik W, Federspiel A, Kreis R, Boesch C, Maier SE, Schroth G, Lovblad K, Dierks T (2004) Pathways that make voices: white matter changes in auditory hallucinations. Arch Gen Psychiatry 61:658–668
39. Bruno S, Cercignani M, Ron M (2008) White matter abnormalities in bipolar disorder: a voxel-based diffusion tensor imaging study. Bipolar Disord 10:460–468
40. Kafantaris V, Kingsley P, Ardekani B, Saito E, Lencz T, Lim K et al (2009) Lower orbital frontal white matter integrity in adolescents with bipolar I disorder. J Am Acad Child Adolesc Psychiatry 48:79–86
41. Versace A, Almeida JRC, Hassel S, Walsh ND, Novelli MKCR, Kupfer DJ et al (2008) Elevated left and reduced right orbitomedial prefrontal fractional anisotropy in adults with bipolar disorder revealed by tract-based spatial statistics. Arch Gen Psychiatry 65:1041–1052
42. Sussmann JE, Lymer GKS, Mckirdy J, Moorhead TWJ, Maniega SM, Job D et al (2009) White matter abnormalities in bipolar disorder and schizophrenia detected using diffusion tensor magnetic resonance imaging. Bipolar Disord 11:11–18
43. McDonald C, Bullmore E, Sham P, Chitnis X, Suckling J, MacCabe J, Walshe M, Murray RM (2005) Regional volume deviations of brain structure in schizophrenia and psychotic bipolar disorder: computational morphometry study. Br J Psychiatry 186:369–377
44. Ayalew M, Le-Niculescu H, Levey DF, Jain N, Changala B, Patel SD, Winiger E, Breier A, Shekhar A, Amdur R, Koller D, Nurnberger JI, Corvin A, Geyer M, Tsuang MT, Salomon D, Schork NJ, Fanous AH, O’Donovan MC, Niculescu AB (2012) Convergent functional genomics of schizophrenia: from comprehensive understanding to genetic risk prediction. Mol Psychiatry 17:887–905
45. Simon TJ, Ding L, Bish JP, McDonald-McGinn DM, Zackai EH, Gee J (2005) Volumetric, connective, and morphologic changes in the brains of children with chromosome 22q11.2 deletion syndrome: an integrative study. Neuroimage 25:169–180
46. Vangberg TR, Skranes J, Dale AM, Martinussen M, Brubakk AM, Haraldseth O (2006) Changes in white matter diffusion anisotropy in adolescents born prematurely. Neuroimage 32:1538–1548
47. Jones DK, Symms MR, Cercignani M, Howard RJ (2005) The effect of filter size on VBM analyses of DT-MRI data. The effect of filter size on VBM analyses of DT-MRI data. The effect of filter size on VBM analyses of DT-MRI data. Neuroimage 26:546–554
48. Smith SM, Jenkinson M, Johansen-Berg H, Rueckert D, Nichols TE, Mackay CE, Watkins KE, Ciccarelli O, Cader MZ, Matthews PM, Behrens TE (2006) Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage 31:1487–1505
49. Jbabdi S, Behrens TE, Smith SM (2010) Crossing fibres in tract-based spatial statistics. Neuroimage 49(1):249–256
50. Ennis DB, Kindlmann G (2006) Orthogonal tensor invariants and the analysis of diffusion tensor magnetic resonance images. Magn Reson Med 55(1):136–146
51. Krug A, Markov V, Leube D, Zerres K, Eggermann T, Nöthen MM, Skowronek MH, Rietschel M, Kircher T (2008) Genetic variation in the schizophrenia-risk gene neuregulin1 correlates with personality traits in healthy individuals. Eur Psychiatry 23(5):344–349
52. Griswold MA, Jakob PM, Heidemann RM, Nittka M, Jellus V, Wang J, Kiefer B, Haase A (2002) Generalized autocalibrating partially parallel acquisitions (GRAPPA). Magn Reson Med 47:1202–1210
53. Smith SM, Johansen-Berg H, Jenkinson M, Rueckert D, Nichols TE, Miller KL, Robson MD, Jones DK, Klein JC, Bartsch AJ, Behrens TE (2007) Acquisition and voxelwise analysis of multi-subject diffusion data with tract-based spatial statistics. Nat Protoc 2:499–503
54. Nichols TE, Holmes AP (2002) Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum Brain Mapp 15:1–25
55. Eickhoff SB, Stephan KE, Mohlberg H, Grefkes C, Fink GR, Amunts K, Zilles K (2005) A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. Neuroimage 25:1325–1335
56. Eickhoff SB, Paus T, Caspers S, Grosbras MH, Evans AC, Zilles K, Amunts K (2007) Assignment of functional activations to probabilistic cytoarchitectonic areas revisited. Neuroimage 36:511–521
57. Bürgel U, Amunts K, Hoemke L, Mohlberg H, Gilsbach JM, Zilles K (2006) White matter fiber tracts of the human brain: three-dimensional mapping at microscopic resolution, topography and intersubject variability. Neuroimage 29:1092–1105
58. Douaud G, Jbabdi S, Behrens TE, Menke RA, Gass A, Monsch AU, Rao A, Whitcher B, Kindlmann G, Matthews PM, Smith S (2011) DTI measures in crossing-fibre areas: increased diffusion anisotropy reveals early white matter alteration in MCI and mild Alzheimer’s disease. Neuroimage 55(3):880–890
59. Sexton CE, Mackay CE, Ebmeier KP (2009) A systematic review of diffusion tensor imaging studies in affective disorders. Biol Psychiatry 66:814–823
60. Nickl-Jockschat T, Schneider F, Pagel AD, Laird AR, Fox PT, Eickhoff SB (2011) Progressive pathology is functionally linked to the domains of language and emotion: meta-analysis of brain structure changes in schizophrenia patients. Eur Arch Psychiatry Clin Neurosci 261:S166–S171
61. Mechelli A, Allen P, Amaro E Jr, Fu CH, Williams SC, Brammer MJ, Johns LC, McGuire PK (2007) Misattribution of speech and impaired connectivity in patients with auditory verbal hallucinations. Hum Brain Mapp 28:1213–1222
62. Fletcher PC, Frith CD (2009) Perceiving is believing: a Bayesian approach to explaining the positive symptoms of schizophrenia. Nat Rev Neurosci 10:48–58
63. Strakowski SM, DelBello MP, Adler C, Cecil DM, Sax KW (2000) Neuroimaging in bipolar disorder. Bipolar Disord 2:148–164
64. Strakowski SM, Adler CM, Holland SK, Mills N, DelBello MP (2004) A preliminary FMRI study of sustained attention in euthymic, unmedicated bipolar disorder. Neuropsychopharmacology 29:1734–1740
65. Strakowski SM, Delbello MP, Adler CM (2005) The functional neuroanatomy of bipolar disorder: a review of neuroimaging findings. Mol Psychiatry 10:105–116
66. Yu K, Cheung C, Leung M, Li Q, Chua S, McAlonan G (2010) Are bipolar disorder and schizophrenia neuroanatomically distinct? An anatomical likelihood meta-analysis. Front Hum Neurosci 4:189
67. Nickl-Jockschat T, Stöcker T, Markov V, Krug A, Huang R, Schneider F, Habel U, Zerres K, Nöthen MM, Treutlein J, Rietschel M, Shah NJ, Kircher T (2012) The impact of a dysbindin schizophrenia susceptibility variant on fiber tract integrity in healthy individuals: a TBSS-based diffusion tensor imaging study. Neuroimage 60:847–853
68. Nickl-Jockschat T, Stöcker T, Markov V, Krug A, Huang R, Schneider F, Habel U, Zerres K, Nöthen MM, Treutlein J, Rietschel M, Shah NJ, Kircher T (2014) A Neuregulin-1 schizophrenia susceptibility variant causes perihippocampal fiber tract anomalies in healthy young subjects. Brain Behav 4(2):215–226
69. Grillon ML, Oppenheim C, Varoquaux G, Charbonneau F, Devauchelle AD, Krebs MO, Bayle F, Thirion B, Huron C (2012) Hyperfrontality and hypoconnectivity during refreshing in schizophrenia. Psychiatry Res. doi:10.1016/j.pscychresns.2012.09.001
70. van der Meer L, de Vos AE, Stiekema AP, Pijnenborg GH, van Tol MJ, Nolen WA, David AS, Aleman A (2012) Insight in schizophrenia: involvement of self-reflection networks? Schizophr Bull
71. Guo S, Kendrick KM, Yu R, Wang HL, Feng J (2012) Key functional circuitry altered in schizophrenia involves parietal regions associated with sense of self. Hum Brain Mapp. doi:10.1002/hbm.22162
72. Legrand D, Ruby P (2009) What is self-specific? Theoretical investigation and critical review of neuroimaging results. Psychol Rev 116:252–282
73. Fox MD, Raichle ME (2007) Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat Rev Neurosci 8:700–711
74. Kircher TT, Leube DT (2003) Self-consciousness, self-agency, and schizophrenia. Conscious Cogn 12:656–669
75. Liu CH, Ma X, Li F, Wang YJ, Tie CL, Li SF, Chen TL, Fan TT, Zhang Y, Dong J, Yao L, Wu X, Wang CY (2012) Regional homogeneity within the default mode network in bipolar depression: a resting-state functional magnetic resonance imaging study. PLoS ONE 7(11):e48181. doi:10.1371/journal.pone.0048181
76. Thomas LA, Brotman MA, Muhrer EJ, Rosen BH, Bones BL, Reynolds RC, Deveney CM, Pine DS, Leibenluft E (2012) Parametric modulation of neural activity by emotion in youth with bipolar disorder, youth with severe mood dysregulation, and healthy volunteers. Arch Gen Psychiatry 69:1257–1266
77. Mitchell RL, Crow TJ (2005) Right hemisphere language functions and schizophrenia: the forgotten hemisphere? Brain 128:963–978
78. Eickhoff SB, Laird AR, Grefkes C, Wang LE, Zilles K, Fox PT (2009) Coordinate-based activation likelihood estimation meta-analysis of neuroimaging data: a random-effects approach based on empirical estimates of spatial uncertainty. Hum Brain Mapp 30:2907–2926
79. Eickhoff SB, Bzdok D, Laird AR, Kurth F, Fox PT (2012) Activation likelihood estimation meta-analysis revisited. Neuroimage 59(3):2349–2361