Genetic associations with brain cortical thickness in multiple sclerosis

Genes, Brain and Behavior

Volumn 14, Issue 2, 2015, Pages 217-227

  Matsushita, T ^a   Madireddy, L ^a   Sprenger, T ^b   Khankhanian, P ^a   Magon, S ^b   Naegelin, Y ^b   Caverzasi, E ^a   Lindberg, R L P ^b   Kappos, L ^b   Hauser, S L ^a   Oksenberg, J R ^a   Henry, R ^a   Pelletier, D ^c   Baranzini, S E ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY HOSPITAL BASEL   (Switzerland)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Brain; Cortical thickness; Data integration; Genetics; GWAS; MRI; Multiple sclerosis; Networks; Protein interactome; SNP

Indexed keywords

CAENORHABDITIS ELEGANS PROTEIN; CALCIUM CHANNEL; DROSOPHILA PROTEIN; PHOSPHOPROTEIN PHOSPHATASE; PROTEIN KINASE B; SMAD PROTEIN; CALCIUM;

ADULT; ARTICLE; CALCIUM CELL LEVEL; CINGULATE GYRUS; CONTROLLED STUDY; CORTICAL THICKNESS (BRAIN); EXPANDED DISABILITY STATUS SCALE; FEMALE; FRONTAL LOBE; GENETIC ASSOCIATION; HUMAN; INSULA; LEFT HEMISPHERE; LIMBIC SYSTEM; MAJOR CLINICAL STUDY; MALE; MULTIPLE SCLEROSIS; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SCANNER; OCCIPITAL LOBE; PARIETAL LOBE; PRECUNEUS; PRIORITY JOURNAL; PROTEIN INTERACTION; RIGHT HEMISPHERE; SINGLE NUCLEOTIDE POLYMORPHISM; SUPERIOR TEMPORAL SULCUS; TEMPORAL LOBE; AGED; BRAIN; GENETIC PREDISPOSITION; GENETICS; METABOLISM; MIDDLE AGED; NERVE CELL NETWORK; PATHOLOGY; PROCEDURES;

ADULT; AGED; BRAIN; CALCIUM; FEMALE; GENETIC PREDISPOSITION TO DISEASE; GENOME-WIDE ASSOCIATION STUDY; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; MULTIPLE SCLEROSIS; NERVE NET;

EID: 84925372255     PISSN: 16011848     EISSN: 1601183X     Source Type: Journal    
DOI: 10.1111/gbb.12190     Document Type: Article

References (61)

1. Achiron, A., Chapman, J., Tal, S., Bercovich, E. & Gil, H. (2013) Superior temporal gyrus thickness correlates with cognitive performance in multiple sclerosis. Brain Struct Funct 218, 943-950.
2. Baranzini, S.E., Galwey, N.W., Wang, J., Khankhanian, P., Lindberg, R., Pelletier, D., Wu, W., Uitdehaag, B.M., Kappos, L., Polman, C.H., Matthews, P.M., Hauser, S.L., Gibson, R.A., Oksenberg, J.R. & Barnes, M.R. (2009a) Pathway and network-based analysis of genome-wide association studies in multiple sclerosis. Hum Mol Genet 18, 2078-2090.
3. Baranzini, S.E., Wang, J., Gibson, R.A. et al. (2009b) Genome-wide association analysis of susceptibility and clinical phenotype in multiple sclerosis. Hum Mol Genet 18, 767-778.
4. Baranzini, S.E., Srinivasan, R., Khankhanian, P., Okuda, D.T., Nelson, S.J., Matthews, P.M., Hauser, S.L., Oksenberg, J.R. & Pelletier, D. (2010) Genetic variation influences glutamate concentrations in brains of patients with multiple sclerosis. Brain 133, 2603-2611.
5. Beecham, A.H., Patsopoulos, N.A., Xifara, D.K. et al. (2013) Analysis of immune-related loci identifies 48 new susceptibility variants for multiple sclerosis. Nat Genet 45, 1353-1360.
6. Bindea, G., Mlecnik, B., Hackl, H., Charoentong, P., Tosolini, M., Kirilovsky, A., Fridman, W.H., Pages, F., Trajanoski, Z. & Galon, J. (2009) ClueGO: a Cytoscape plug-in to decipher functionally grouped gene ontology and pathway annotation networks. Bioinformatics 25, 1091-1093.
7. Blum, D., Yonelinas, A.P., Luks, T., Newitt, D., Oh, J., Lu, Y., Nelson, S., Goodkin, D. & Pelletier, D. (2002) Dissociating perceptual and conceptual implicit memory in multiple sclerosis patients. Brain Cogn 50, 51-61.
8. Bo, L., Vedeler, C.A., Nyland, H.I., Trapp, B.D. & Mork, S.J. (2003) Subpial demyelination in the cerebral cortex of multiple sclerosis patients. J Neuropathol Exp Neurol 62, 723-732.
9. Bodmer, W. & Bonilla, C. (2008) Common and rare variants in multifactorial susceptibility to common diseases. Nat Genet 40, 695-701.
10. Calabrese, M., De Stefano, N., Atzori, M., Bernardi, V., Mattisi, I., Barachino, L., Morra, A., Rinaldi, L., Romualdi, C., Perini, P., Battistin, L. & Gallo, P. (2007) Detection of cortical inflammatory lesions by double inversion recovery magnetic resonance imaging in patients with multiple sclerosis. Arch Neurol 64, 1416-1422.
11. Calabrese, M., Rinaldi, F., Mattisi, I., Grossi, P., Favaretto, A., Atzori, M., Bernardi, V., Barachino, L., Romualdi, C., Rinaldi, L., Perini, P. & Gallo, P. (2010a) Widespread cortical thinning characterizes patients with MS with mild cognitive impairment. Neurology 74, 321-328.
12. Calabrese, M., Rocca, M.A., Atzori, M., Mattisi, I., Favaretto, A., Perini, P., Gallo, P. & Filippi, M. (2010b) A 3-year magnetic resonance imaging study of cortical lesions in relapse-onset multiple sclerosis. Ann Neurol 67, 376-383.
13. Calabrese, M., Rinaldi, F., Mattisi, I., Bernardi, V., Favaretto, A., Perini, P. & Gallo, P. (2011) The predictive value of gray matter atrophy in clinically isolated syndromes. Neurology 77, 257-263.
14. Calabrese, M., Seppi, D., Cocco, E., Poretto, V., Rinaldi, F., Perini, P. & Gallo, P. (2012) Cortical pathology in RRMS: taking a cue from four sisters. Mult Scler Int 2012, Article ID 760254, doi: 10.1155/2012/760254.
15. Chard, D.T., Griffin, C.M., Parker, G.J., Kapoor, R., Thompson, A.J. & Miller, D.H. (2002) Brain atrophy in clinically early relapsing-remitting multiple sclerosis. Brain 125, 327-337.
16. Chen, J.T., Narayanan, S., Collins, D.L., Smith, S.M., Matthews, P.M. & Arnold, D.L. (2004) Relating neocortical pathology to disability progression in multiple sclerosis using MRI. Neuroimage 23, 1168-1175.
17. Dale, A.M., Fischl, B. & Sereno, M.I. (1999) Cortical surface-based analysis. I Segmentation and surface reconstruction. Neuroimage 9, 179-194.
18. Dalton, C.M., Chard, D.T., Davies, G.R., Miszkiel, K.A., Altmann, D.R., Fernando, K., Plant, G.T., Thompson, A.J. & Miller, D.H. (2004) Early development of multiple sclerosis is associated with progressive grey matter atrophy in patients presenting with clinically isolated syndromes. Brain 127, 1101-1107.
19. De Stefano, N., Matthews, P.M., Filippi, M., Agosta, F., De Luca, M., Bartolozzi, M.L., Guidi, L., Ghezzi, A., Montanari, E., Cifelli, A., Federico, A. & Smith, S.M. (2003) Evidence of early cortical atrophy in MS: relevance to white matter changes and disability. Neurology 60, 1157-1162.
20. Desikan, R.S., Segonne, F., Fischl, B., Quinn, B.T., Dickerson, B.C., Blacker, D., Buckner, R.L., Dale, A.M., Maguire, R.P., Hyman, B.T., Albert, M.S. & Killiany, R.J. (2006) An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage 31, 968-980.
21. Eyler, L.T., Prom-Wormley, E., Panizzon, M.S. et al. (2011) Genetic and environmental contributions to regional cortical surface area in humans: a magnetic resonance imaging twin study. Cereb Cortex 21, 2313-2321.
22. Eyler, L.T., Chen, C.H., Panizzon, M.S., Fennema-Notestine, C., Neale, M.C., Jak, A., Jernigan, T.L., Fischl, B., Franz, C.E., Lyons, M.J., Grant, M., Prom-Wormley, E., Seidman, L.J., Tsuang, M.T., Fiecas, M.J., Dale, A.M. & Kremen, W.S. (2012) A comparison of heritability maps of cortical surface area and thickness and the influence of adjustment for whole brain measures: a magnetic resonance imaging twin study. Twin Res Hum Genet 15, 304-314.
23. Filippi, M., Rocca, M.A., Calabrese, M., Sormani, M.P., Rinaldi, F., Perini, P., Comi, G. & Gallo, P. (2010) Intracortical lesions: relevance for new MRI diagnostic criteria for multiple sclerosis. Neurology 75, 1988-1994.
24. Fischl, B., Sereno, M.I. & Dale, A.M. (1999) Cortical surface-based analysis. II: inflation, flattening, and a surface-based coordinate system. Neuroimage 9, 195-207.
25. Fischl, B., van der Kouwe, A., Destrieux, C., Halgren, E., Segonne, F., Salat, D.H., Busa, E., Seidman, L.J., Goldstein, J., Kennedy, D., Caviness, V., Makris, N., Rosen, B. & Dale, A.M. (2004) Automatically parcellating the human cerebral cortex. Cereb Cortex 14, 11-22.
26. Fisniku, L.K., Brex, P.A., Altmann, D.R., Miszkiel, K.A., Benton, C.E., Lanyon, R., Thompson, A.J. & Miller, D.H. (2008) Disability and T2 MRI lesions: a 20-year follow-up of patients with relapse onset of multiple sclerosis. Brain 131, 808-817.
27. Georgala, P.A., Carr, C.B. & Price, D.J. (2011) The role of Pax6 in forebrain development. Dev Neurobiol 71, 690-709.
28. Geurts, J.J., Pouwels, P.J., Uitdehaag, B.M., Polman, C.H., Barkhof, F. & Castelijns, J.A. (2005) Intracortical lesions in multiple sclerosis: improved detection with 3D double inversion-recovery MR imaging. Radiology 236, 254-260.
29. Giorgio, A., Stromillo, M.L., Rossi, F., Battaglini, M., Hakiki, B., Portaccio, E., Federico, A., Amato, M.P. & De Stefano, N. (2011) Cortical lesions in radiologically isolated syndrome. Neurology 77, 1896-1899.
30. Hauser, S.L. & Oksenberg, J.R. (2006) The neurobiology of multiple sclerosis: genes, inflammation, and neurodegeneration. Neuron 52, 61-76.
31. Henry, R.G., Shieh, M., Okuda, D.T., Evangelista, A., Gorno-Tempini, M.L. & Pelletier, D. (2008) Regional grey matter atrophy in clinically isolated syndromes at presentation. J Neurol Neurosurg Psychiatry 79, 1236-1244.
32. Ideker, T., Ozier, O., Schwikowski, B. & Siegel, A.F. (2002) Discovering regulatory and signalling circuits in molecular interaction networks. Bioinformatics 18(Suppl. 1), S233-S240.
33. IMSGC (2013) Network-based multiple sclerosis pathway analysis with GWAS data from 15, 000 cases and 30, 000 controls. Am J Hum Genet 92, 854-865.
34. IMSGC, Bush, W.S., Sawcer, S.J., de Jager, P.L., Oksenberg, J.R., McCauley, J.L., Pericak-Vance, M.A. & Haines, J.L. (2010) Evidence for polygenic susceptibility to multiple sclerosis--the shape of things to come. Am J Hum Genet 86, 621-625.
35. IMSGC, Sawcer, S., Hellenthal, G. et al. (2011) Genetic risk and a primary role for cell-mediated immune mechanisms in multiple sclerosis. Nature 476, 214-219.
36. Joshi, A.A., Lepore, N., Joshi, S.H., Lee, A.D., Barysheva, M., Stein, J.L., McMahon, K.L., Johnson, K., de Zubicaray, G.I., Martin, N.G., Wright, M.J., Toga, A.W. & Thompson, P.M. (2011) The contribution of genes to cortical thickness and volume. Neuroreport 22, 101-105.
37. Kochunov, P., Glahn, D.C., Lancaster, J., Thompson, P.M., Kochunov, V., Rogers, B., Fox, P., Blangero, J. & Williamson, D.E. (2011) Fractional anisotropy of cerebral white matter and thickness of cortical gray matter across the lifespan. Neuroimage 58, 41-49.
38. Kremen, W.S., Prom-Wormley, E., Panizzon, M.S., Eyler, L.T., Fischl, B., Neale, M.C., Franz, C.E., Lyons, M.J., Pacheco, J., Perry, M.E., Stevens, A., Schmitt, J.E., Grant, M.D., Seidman, L.J., Thermenos, H.W., Tsuang, M.T., Eisen, S.A., Dale, A.M. & Fennema-Notestine, C. (2010) Genetic and environmental influences on the size of specific brain regions in midlife: the VETSA MRI study. Neuroimage 49, 1213-1223.
39. Kurtzke, J.F. (1983) Rating neurologic impairment in multiple sclerosis: an expanded disability status scale (EDSS). Neurology 33, 1444-1452.
40. Kutzelnigg, A., Lucchinetti, C.F., Stadelmann, C., Bruck, W., Rauschka, H., Bergmann, M., Schmidbauer, M., Parisi, J.E. & Lassmann, H. (2005) Cortical demyelination and diffuse white matter injury in multiple sclerosis. Brain 128, 2705-2712.
41. Lavedan, C., Licamele, L., Volpi, S., Hamilton, J., Heaton, C., Mack, K., Lannan, R., Thompson, A., Wolfgang, C.D. & Polymeropoulos, M.H. (2009) Association of the NPAS3 gene and five other loci with response to the antipsychotic iloperidone identified in a whole genome association study. Mol Psychiatry 14, 804-819.
42. Liu, J.Z., McRae, A.F., Nyholt, D.R., Medland, S.E., Wray, N.R., Brown, K.M., Hayward, N.K., Montgomery, G.W., Visscher, P.M., Martin, N.G. & Macgregor, S. (2010) A versatile gene-based test for genome-wide association studies. Am J Hum Genet 87, 139-145.
43. Nakamura, K. & Fisher, E. (2009) Segmentation of brain magnetic resonance images for measurement of gray matter atrophy in multiple sclerosis patients. Neuroimage 44, 769-776.
44. Noseworthy, J.H., Lucchinetti, C., Rodriguez, M. & Weinshenker, B.G. (2000) Multiple sclerosis. N Engl J Med 343, 938-952.
45. Okuda, D.T., Srinivasan, R., Oksenberg, J.R., Goodin, D.S., Baranzini, S.E., Beheshtian, A., Waubant, E., Zamvil, S.S., Leppert, D., Qualley, P., Lincoln, R., Gomez, R., Caillier, S., George, M., Wang, J., Nelson, S.J., Cree, B.A., Hauser, S.L. & Pelletier, D. (2009) Genotype-phenotype correlations in multiple sclerosis: HLA genes influence disease severity inferred by 1HMR spectroscopy and MRI measures. Brain 132, 250-259.
46. Patenaude, B., Smith, S.M., Kennedy, D.N. & Jenkinson, M. (2011) A Bayesian model of shape and appearance for subcortical brain segmentation. Neuroimage 56, 907-922.
47. Patsopoulos, N.A., Esposito, F., Reischl, J. et al. (2011) Genome-wide meta-analysis identifies novel multiple sclerosis susceptibility loci. Ann Neurol 70, 897-912.
48. Pickard, B.S., Malloy, M.P., Porteous, D.J., Blackwood, D.H. & Muir, W.J. (2005) Disruption of a brain transcription factor, NPAS3, is associated with schizophrenia and learning disability. Am J Med Genet B Neuropsychiatr Genet 136B, 26-32.
49. Polman, C.H., Reingold, S.C., Edan, G., Filippi, M., Hartung, H.P., Kappos, L., Lublin, F.D., Metz, L.M., McFarland, H.F., O'Connor, P.W., Sandberg-Wollheim, M., Thompson, A.J., Weinshenker, B.G. & Wolinsky, J.S. (2005) Diagnostic criteria for multiple sclerosis: 2005 revisions to the "McDonald Criteria". Ann Neurol 58, 840-846.
50. 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. (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 81, 559-575.
51. Purcell, S.M., Wray, N.R., Stone, J.L., Visscher, P.M., O'Donovan, M.C., Sullivan, P.F. & Sklar, P. (2009) Common polygenic variation contributes to risk of schizophrenia and bipolar disorder. Nature 460, 748-752.
52. Razick, S., Magklaras, G. & Donaldson, I.M. (2008) iRefIndex: a consolidated protein interaction database with provenance. BMC Bioinformatics 9, 405-424.
53. Rimol, L.M., Panizzon, M.S., Fennema-Notestine, C., Eyler, L.T., Fischl, B., Franz, C.E., Hagler, D.J., Lyons, M.J., Neale, M.C., Pacheco, J., Perry, M.E., Schmitt, J.E., Grant, M.D., Seidman, L.J., Thermenos, H.W., Tsuang, M.T., Eisen, S.A., Kremen, W.S. & Dale, A.M. (2010) Cortical thickness is influenced by regionally specific genetic factors. Biol Psychiatry 67, 493-499.
54. Sailer, M., Fischl, B., Salat, D., Tempelmann, C., Schonfeld, M.A., Busa, E., Bodammer, N., Heinze, H.J. & Dale, A. (2003) Focal thinning of the cerebral cortex in multiple sclerosis. Brain 126, 1734-1744.
55. Shannon, P., Markiel, A., Ozier, O., Baliga, N.S., Wang, J.T., Ramage, D., Amin, N., Schwikowski, B. & Ideker, T. (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13, 2498-2504.
56. Stirling, D.P. & Stys, P.K. (2010) Mechanisms of axonal injury: internodal nanocomplexes and calcium deregulation. Trends Mol Med 16, 160-170.
57. Tiberio, M., Chard, D.T., Altmann, D.R., Davies, G., Griffin, C.M., Rashid, W., Sastre-Garriga, J., Thompson, A.J. & Miller, D.H. (2005) Gray and white matter volume changes in early RRMS: a 2-year longitudinal study. Neurology 64, 1001-1007.
58. Trapp, B.D. & Nave, K.A. (2008) Multiple sclerosis: an immune or neurodegenerative disorder? Annu Rev Neurosci 31, 247-269.
59. Tur, C., Ramagopalan, S., Altmann, D.R., Bodini, B., Cercignani, M., Khaleeli, Z., Miller, D.H., Thompson, A.J. & Ciccarelli, O. (2014) HLA-DRB1*15 influences the development of brain tissue damage in early PPMS. Neurology 83, 1712-1718.
60. Wegner, C., Esiri, M.M., Chance, S.A., Palace, J. & Matthews, P.M. (2006) Neocortical neuronal, synaptic, and glial loss in multiple sclerosis. Neurology 67, 960-967.
61. Yates, R.L., Esiri, M.M., Palace, J., Mittal, A. & DeLuca, G.C. (2014) The influence of HLA-DRB1*15 on motor cortical pathology in multiple sclerosis. Neuropathol Appl Neurobiol. doi: 10.1111/nan.12165. [Epub ahead of print]