DISC1 Ser704Cys impacts thalamic-prefrontal connectivity

Brain Structure and Function

Volumn 220, Issue 1, 2015, Pages 91-100

  Liu, Bing ^a,b   Fan, Lingzhong ^a   Cui, Yue ^a,b   Zhang, Xiaolong ^a   Hou, Bing ^a,b   Li, Yonghui ^c   Qin, Wen ^d   Wang, Dawei ^d   Yu, Chunshui ^d   Jiang, Tianzi ^a,b,c,e  

^a INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^b INSTITUTE OF AUTOMATION   (China)

^c UNIVERSITY OF QUEENSLAND   (Australia)

^d TIANJIN MEDICAL UNIVERSITY   (China)

^e UNIVERSITY OF ELECTRONIC SCIENCE AND TECHNOLOGY OF CHINA   (China)

Author keywords

Anatomical connectivity; DISC1; Functional connectivity density; Thalamic prefrontal circuit; Thalamus

Indexed keywords

CYSTEINE; DISC1 PROTEIN, HUMAN; NERVE PROTEIN; OXYGEN; SERINE;

ADOLESCENT; ADULT; ANATOMY AND HISTOLOGY; BLOOD; BRAIN MAPPING; CHI SQUARE DISTRIBUTION; FEMALE; GENETICS; HUMAN; MALE; NUCLEAR MAGNETIC RESONANCE IMAGING; PREFRONTAL CORTEX; SENSORY NERVE; THALAMUS; THREE DIMENSIONAL IMAGING; VASCULARIZATION; YOUNG ADULT;

ADOLESCENT; ADULT; AFFERENT PATHWAYS; BRAIN MAPPING; CHI-SQUARE DISTRIBUTION; CYSTEINE; FEMALE; HUMANS; IMAGING, THREE-DIMENSIONAL; MAGNETIC RESONANCE IMAGING; MALE; NERVE TISSUE PROTEINS; OXYGEN; PREFRONTAL CORTEX; SERINE; THALAMUS; YOUNG ADULT;

EID: 84885556819     PISSN: 18632653     EISSN: 18632661     Source Type: Journal    
DOI: 10.1007/s00429-013-0640-5     Document Type: Article

References (62)

1. Adriano F, Spoletini I, Caltagirone C, Spalletta G (2010) Updated meta-analyses reveal thalamus volume reduction in patients with first-episode and chronic schizophrenia. Schizophr Res 123(1):1–14. doi:10.1016/j.schres.2010.07.007
2. Andreasen NC (1997) The role of the thalamus in schizophrenia. Can J Psychiatry 42(1):27–33
3. Barnes A, Isohanni M, Barnett JH, Pietilainen O, Veijola J, Miettunen J, Paunio T, Tanskanen P, Ridler K, Suckling J, Bullmore ET, Jones PB, Murray GK (2012) Neuregulin-1 genotype is associated with structural differences in the normal human brain. Neuroimage 59(3):2057–2061. doi:10.1016/j.neuroimage.2011.10.007
4. Behrens TE, Woolrich MW, Jenkinson M, Johansen-Berg H, Nunes RG, Clare S, Matthews PM, Brady JM, Smith SM (2003) Characterization and propagation of uncertainty in diffusion-weighted MR imaging. Magn Reson Med 50(5):1077–1088. doi:10.1002/mrm.10609
5. Behrens TE, Berg HJ, Jbabdi S, Rushworth MF, Woolrich MW (2007) Probabilistic diffusion tractography with multiple fibre orientations: what can we gain? Neuroimage 34(1):144–155. doi:10.1016/j.neuroimage.2006.09.018
6. Blackwood DH, Fordyce A, Walker MT, St Clair DM, Porteous DJ, Muir WJ (2001) Schizophrenia and affective disorders–cosegregation with a translocation at chromosome 1q42 that directly disrupts brain-expressed genes: clinical and P300 findings in a family. Am J Hum Genet 69(2):428–433 S0002-9297(07)61088-X
7. Bora E, Fornito A, Radua J, Walterfang M, Seal M, Wood SJ, Yucel M, Velakoulis D, Pantelis C (2011) Neuroanatomical abnormalities in schizophrenia: a multimodal voxelwise meta-analysis and meta-regression analysis. Schizophr Res 127(1–3):46–57. doi:10.1016/j.schres.2010.12.020
8. Bradshaw NJ, Porteous DJ (2012) DISC1-binding proteins in neural development, signalling and schizophrenia. Neuropharmacology 62(3):1230–1241. doi:10.1016/j.neuropharm.2010.12.027
9. Brandon NJ, Sawa A (2011) Linking neurodevelopmental and synaptic theories of mental illness through DISC1. Nat Rev Neurosci 12(12):707–722. doi:10.1038/nrn3120
10. Brandon NJ, Millar JK, Korth C, Sive H, Singh KK, Sawa A (2009) Understanding the role of DISC1 in psychiatric disease and during normal development. J Neurosci 29(41):12768–12775. doi:10.1523/JNEUROSCI.3355-09.2009
11. Briggs F, Usrey WM (2008) Emerging views of corticothalamic function. Curr Opin Neurobiol 18(4):403–407. doi:10.1016/j.conb.2008.09.002
12. Byne W, Hazlett EA, Buchsbaum MS, Kemether E (2009) The thalamus and schizophrenia: current status of research. Acta Neuropathol 117(4):347–368. doi:10.1007/s00401-008-0404-0
13. Callicott JH, Straub RE, Pezawas L, Egan MF, Mattay VS, Hariri AR, Verchinski BA, Meyer-Lindenberg A, Balkissoon R, Kolachana B, Goldberg TE, Weinberger DR (2005) Variation in DISC1 affects hippocampal structure and function and increases risk for schizophrenia. Proc Natl Acad Sci USA 102(24):8627–8632. doi:10.1073/pnas.0500515102
14. Chubb JE, Bradshaw NJ, Soares DC, Porteous DJ, Millar JK (2008) The DISC locus in psychiatric illness. Mol Psychiatry 13(1):36–64. doi:10.1038/sj.mp.4002106
15. Clapcote SJ, Lipina TV, Millar JK, Mackie S, Christie S, Ogawa F, Lerch JP, Trimble K, Uchiyama M, Sakuraba Y, Kaneda H, Shiroishi T, Houslay MD, Henkelman RM, Sled JG, Gondo Y, Porteous DJ, Roder JC (2007) Behavioral phenotypes of Disc1 missense mutations in mice. Neuron 54(3):387–402. doi:10.1016/j.neuron.2007.04.015
16. Cronenwett WJ, Csernansky J (2010) Thalamic pathology in schizophrenia. Curr Top Behav Neurosci 4:509–528
17. DeRosse P, Hodgkinson CA, Lencz T, Burdick KE, Kane JM, Goldman D, Malhotra AK (2007) Disrupted in schizophrenia 1 genotype and positive symptoms in schizophrenia. Biol Psychiatry 61(10):1208–1210. doi:10.1016/j.biopsych.2006.07.023
18. Di Giorgio A, Blasi G, Sambataro F, Rampino A, Papazacharias A, Gambi F, Romano R, Caforio G, Rizzo M, Latorre V, Popolizio T, Kolachana B, Callicott JH, Nardini M, Weinberger DR, Bertolino A (2008) Association of the SerCys DISC1 polymorphism with human hippocampal formation gray matter and function during memory encoding. Eur J Neurosci 28(10):2129–2136. doi:10.1111/j.1460-9568.2008.06482.x
19. Duan X, Chang JH, Ge S, Faulkner RL, Kim JY, Kitabatake Y, Liu XB, Yang CH, Jordan JD, Ma DK, Liu CY, Ganesan S, Cheng HJ, Ming GL, Lu B, Song H (2007) Disrupted-In-Schizophrenia 1 regulates integration of newly generated neurons in the adult brain. Cell 130(6):1146–1158. doi:10.1016/j.cell.2007.07.010
20. Ellison-Wright I, Bullmore E (2009) Meta-analysis of diffusion tensor imaging studies in schizophrenia. Schizophr Res 108(1–3):3–10. doi:10.1016/j.schres.2008.11.021
21. Fornito A, Zalesky A, Pantelis C, Bullmore ET (2012) Schizophrenia, neuroimaging and connectomics. Neuroimage 62(4):2296–2314. doi:10.1016/j.neuroimage.2011.12.090
22. Hashimoto R, Numakawa T, Ohnishi T, Kumamaru E, Yagasaki Y, Ishimoto T, Mori T, Nemoto K, Adachi N, Izumi A, Chiba S, Noguchi H, Suzuki T, Iwata N, Ozaki N, Taguchi T, Kamiya A, Kosuga A, Tatsumi M, Kamijima K, Weinberger DR, Sawa A, Kunugi H (2006) Impact of the DISC1 Ser704Cys polymorphism on risk for major depression, brain morphology and ERK signaling. Hum Mol Genet 15(20):3024–3033. doi:10.1093/hmg/ddl244
23. Hulvershorn LA, Cullen K, Anand A (2011) Toward dysfunctional connectivity: a review of neuroimaging findings in pediatric major depressive disorder. Brain Imaging Behav 5(4):307–328. doi:10.1007/s11682-011-9134-3
24. Johnstone M, Thomson PA, Hall J, McIntosh AM, Lawrie SM, Porteous DJ (2011) DISC1 in schizophrenia: genetic mouse models and human genomic imaging. Schizophr Bull 37(1):14–20. doi:10.1093/schbul/sbq135
25. Kim HJ, Park HJ, Jung KH, Ban JY, Ra J, Kim JW, Park JK, Choe BK, Yim SV, Kwon YK, Chung JH (2008) Association study of polymorphisms between DISC1 and schizophrenia in a Korean population. Neurosci Lett 430(1):60–63. doi:10.1016/j.neulet.2007.10.010
26. Kim JY, Duan X, Liu CY, Jang MH, Guo JU, Pow-anpongkul N, Kang E, Song H, Ming GL (2009) DISC1 regulates new neuron development in the adult brain via modulation of AKT-mTOR signaling through KIAA1212. Neuron 63(6):761–773. doi:10.1016/j.neuron.2009.08.008
27. Lehrer DS, Christian BT, Mantil J, Murray AC, Buchsbaum BR, Oakes TR, Byne W, Kemether EM, Buchsbaum MS (2005) Thalamic and prefrontal FDG uptake in never medicated patients with schizophrenia. Am J Psychiatry 162(5):931–938. doi:10.1176/appi.ajp.162.5.931
28. Lewis DA (2000) Is there a neuropathology of schizophrenia? Recent findings converge on altered thalamic-prefrontal cortical connectivity. Neuroscientist 6(3):208–218. doi:10.1177/107385840000600311
29. Li Y, Liu B, Hou B, Qin W, Wang D, Yu C, Jiang T (2013) Less efficient information transfer in Cys-allele carriers of DISC1: a brain network study based on diffusion MRI. Cereb Cortex 23(7):1715–1723. doi:10.1093/cercor/bhs167
30. Mamah D, Conturo TE, Harms MP, Akbudak E, Wang L, McMichael AR, Gado MH, Barch DM, Csernansky JG (2010) Anterior thalamic radiation integrity in schizophrenia: a diffusion-tensor imaging study. Psychiatry Res 183(2):144–150. doi:10.1016/j.pscychresns.2010.04.013
31. Marenco S, Stein JL, Savostyanova AA, Sambataro F, Tan HY, Goldman AL, Verchinski BA, Barnett AS, Dickinson D, Apud JA, Callicott JH, Meyer-Lindenberg A, Weinberger DR (2012) Investigation of anatomical thalamo-cortical connectivity and FMRI activation in schizophrenia. Neuropsychopharmacology 37(2):499–507. doi:10.1038/npp.2011.215
32. Mathieson I, Munafo MR, Flint J (2012) Meta-analysis indicates that common variants at the DISC1 locus are not associated with schizophrenia. Mol Psychiatry 17(6):634–641. doi:10.1038/mp.2011.41
33. McIntosh AM, Munoz Maniega S, Lymer GK, McKirdy J, Hall J, Sussmann JE, Bastin ME, Clayden JD, Johnstone EC, Lawrie SM (2008) White matter tractography in bipolar disorder and schizophrenia. Biol Psychiatry 64(12):1088–1092. doi:10.1016/j.biopsych.2008.07.026
34. Millar JK, Wilson-Annan JC, Anderson S, Christie S, Taylor MS, Semple CA, Devon RS, St Clair DM, Muir WJ, Blackwood DH, Porteous DJ (2000) Disruption of two novel genes by a translocation co-segregating with schizophrenia. Hum Mol Genet 9(9):1415–1423
35. Ming GL, Song H (2009) DISC1 partners with GSK3beta in neurogenesis. Cell 136(6):990–992. doi:10.1016/j.cell.2009.03.005
36. Mori S, Zhang J (2006) Principles of diffusion tensor imaging and its applications to basic neuroscience research. Neuron 51(5):527–539. doi:10.1016/j.neuron.2006.08.012
37. Narayanan S, Arthanari H, Wolfe MS, Wagner G (2011) Molecular characterization of disrupted in schizophrenia-1 risk variant S704C reveals the formation of altered oligomeric assembly. J Biol Chem 286(51):44266–44276. doi:10.1074/jbc.M111.271593
38. Pakkenberg B, Scheel-Kruger J, Kristiansen LV (2009) Schizophrenia; from structure to function with special focus on the mediodorsal thalamic prefrontal loop. Acta Psychiatr Scand 120(5):345–354. doi:10.1111/j.1600-0447.2009.01447.x
39. Palo OM, Antila M, Silander K, Hennah W, Kilpinen H, Soronen P, Tuulio-Henriksson A, Kieseppa T, Partonen T, Lonnqvist J, Peltonen L, Paunio T (2007) Association of distinct allelic haplotypes of DISC1 with psychotic and bipolar spectrum disorders and with underlying cognitive impairments. Hum Mol Genet 16(20):2517–2528. doi:10.1093/hmg/ddm207
40. Perez-Iglesias R, Tordesillas-Gutierrez D, Barker GJ, McGuire PK, Roiz-Santianez R, Mata I, de Lucas EM, Quintana F, Vazquez-Barquero JL, Crespo-Facorro B (2010) White matter defects in first episode psychosis patients: a voxelwise analysis of diffusion tensor imaging. Neuroimage 49(1):199–204. doi:10.1016/j.neuroimage.2009.07.016
41. Prata DP, Mechelli A, Fu CH, Picchioni M, Kane F, Kalidindi S, McDonald C, Kravariti E, Toulopoulou T, Miorelli A, Murray R, Collier DA, McGuire PK (2008) Effect of disrupted-in-schizophrenia-1 on pre-frontal cortical function. Mol Psychiatry 13 (10):915–917, 909. doi:10.1038/mp.2008.76
42. Qu M, Tang F, Yue W, Ruan Y, Lu T, Liu Z, Zhang H, Han Y, Zhang D, Wang F (2007) Positive association of the Disrupted-in-Schizophrenia-1 gene (DISC1) with schizophrenia in the Chinese Han population. Am J Med Genet B Neuropsychiatr Genet 144B(3):266–270. doi:10.1002/ajmg.b.30322
43. Raznahan A, Lee Y, Long R, Greenstein D, Clasen L, Addington A, Rapoport JL, Giedd JN (2011) Common functional polymorphisms of DISC1 and cortical maturation in typically developing children and adolescents. Mol Psychiatry 16(9):917–926. doi:10.1038/mp.2010.72
44. Rosazza C, Minati L (2011) Resting-state brain networks: literature review and clinical applications. Neurol Sci 32(5):773–785. doi:10.1007/s10072-011-0636-y
45. Rose SE, Chalk JB, Janke AL, Strudwick MW, Windus LC, Hannah DE, McGrath JJ, Pantelis C, Wood SJ, Mowry BJ (2006) Evidence of altered prefrontal-thalamic circuitry in schizophrenia: an optimized diffusion MRI study. Neuroimage 32(1):16–22. doi:10.1016/j.neuroimage.2006.03.003
46. Schurov IL, Handford EJ, Brandon NJ, Whiting PJ (2004) Expression of disrupted in schizophrenia 1 (DISC1) protein in the adult and developing mouse brain indicates its role in neurodevelopment. Mol Psychiatry 9(12):1100–1110. doi:10.1038/sj.mp.4001574
47. Singh KK, De Rienzo G, Drane L, Mao Y, Flood Z, Madison J, Ferreira M, Bergen S, King C, Sklar P, Sive H, Tsai LH (2011) Common DISC1 polymorphisms disrupt Wnt/GSK3beta signaling and brain development. Neuron 72(4):545–558. doi:10.1016/j.neuron.2011.09.030
48. Skudlarski P, Jagannathan K, Anderson K, Stevens MC, Calhoun VD, Skudlarska BA, Pearlson G (2010) Brain connectivity is not only lower but different in schizophrenia: a combined anatomical and functional approach. Biol Psychiatry 68(1):61–69. doi:10.1016/j.biopsych.2010.03.035
49. Sprooten E, Lymer GK, Munoz Maniega S, McKirdy J, Clayden JD, Bastin ME, Porteous D, Johnstone EC, Lawrie SM, Hall J, McIntosh AM (2009) The relationship of anterior thalamic radiation integrity to psychosis risk associated neuregulin-1 variants. Mol Psychiatry 14(3):237–238, 233. doi:10.1038/mp.2008.136
50. Sprooten E, Sussmann JE, Moorhead TW, Whalley HC, Ffrench-Constant C, Blumberg HP, Bastin ME, Hall J, Lawrie SM, McIntosh AM (2011) Association of white matter integrity with genetic variation in an exonic DISC1 SNP. Mol Psychiatry 16(7):685, 688–689. doi:10.1038/mp.2011.15
51. Strakowski SM, Delbello MP, Adler CM (2005) The functional neuroanatomy of bipolar disorder: a review of neuroimaging findings. Mol Psychiatry 10(1):105–116. doi:10.1038/sj.mp.4001585
52. Takahashi T, Suzuki M, Tsunoda M, Maeno N, Kawasaki Y, Zhou SY, Hagino H, Niu L, Tsuneki H, Kobayashi S, Sasaoka T, Seto H, Kurachi M, Ozaki N (2009) The Disrupted-in-Schizophrenia-1 Ser704Cys polymorphism and brain morphology in schizophrenia. Psychiatry Res 172(2):128–135. doi:10.1016/j.pscychresns.2009.01.005
53. Tomasi D, Volkow ND (2010a) Functional connectivity density mapping. Proc Natl Acad Sci USA 107(21):9885–9890. doi:10.1073/pnas.1001414107
54. Tomasi D, Volkow ND (2010b) Ultrafast method for mapping local functional connectivity hubs in the human brain. Conf Proc IEEE Eng Med Biol Soc 2010:4274–4277. doi:10.1109/IEMBS.2010.5626180
55. Tomasi D, Volkow ND (2011) Aging and functional brain networks. Mol Psychiatry 17(5):549–558. doi:10.1038/mp.2011.81
56. Tomita K, Kubo K, Ishii K, Nakajima K (2011) Disrupted-in-Schizophrenia-1 (Disc1) is necessary for migration of the pyramidal neurons during mouse hippocampal development. Hum Mol Genet 20(14):2834–2845. doi:10.1093/hmg/ddr194
57. Trost S, Platz B, Usher J, Scherk H, Wobrock T, Ekawardhani S, Meyer J, Reith W, Falkai P, Gruber O (2013) DISC1 (disrupted-in-schizophrenia 1) is associated with cortical grey matter volumes in the human brain: a voxel-based morphometry (VBM) study. J Psychiatr Res 47(2):188–196. doi:10.1016/j.jpsychires.2012.10.006
58. van den Heuvel MP, Hulshoff Pol HE (2010) Exploring the brain network: a review on resting-state fMRI functional connectivity. Eur Neuropsychopharmacol 20(8):519–534. doi:10.1016/j.euroneuro.2010.03.008
59. Wang J, Fan L, Zhang Y, Liu Y, Jiang D, Yu C, Jiang T (2012) Tractography-based parcellation of the human left inferior parietal lobule. Neuroimage 63(2):641–652. doi:10.1016/j.neuroimage.2012.07.045
60. Wei SM, Eisenberg DP, Kohn PD, Kippenhan JS, Kolachana BS, Weinberger DR, Berman KF (2012) Brain-derived neurotrophic factor Val(6)(6)Met polymorphism affects resting regional cerebral blood flow and functional connectivity differentially in women versus men. J Neurosci 32(20):7074–7081. doi:10.1523/JNEUROSCI.5375-11.2012
61. Woodward ND, Karbasforoushan H, Heckers S (2012) Thalamocortical dysconnectivity in schizophrenia. Am J Psychiatry 169(10):1092–1099. doi:10.1176/appi.ajp.2012.12010056
62. Zhang Y, Fan L, Wang J, Zhu M, Yu C, Jiang T (2012) Connectivity-based parcellation of the human posteromedial cortex. Cereb Cortex. doi:10.1093/cercor/bhs353