Histone deacetylase gene variants predict brain volume changes in multiple sclerosis

Neurobiology of Aging

Volumn 34, Issue 1, 2013, Pages 238-247

  Inkster, Becky ^a,b   Strijbis, Eva M M ^c   Vounou, Maria ^b   Kappos, Ludwig ^d   Radue, Ernst Wilhelm ^d   Matthews, Paul M ^a   Uitdehaag, Bernard M J ^c   Barkhof, Frederik ^c   Polman, Chris H ^c   Montana, Giovanni ^b   Geurts, Jeroen J G ^c  

^a HAMMERSMITH HOSPITAL   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^d UNIVERSITY HOSPITAL BASEL   (Switzerland)

Author keywords

Brain volume; Histone deacetylase; Mitochondria; Multiple sclerosis; Multivariate regression; Sirtuin

Indexed keywords

HISTONE DEACETYLASE;

ADULT; AGED; ARTICLE; BRAIN SIZE; EPIGENETICS; FEMALE; GENETIC ASSOCIATION; HISTONE DEACETYLASE GENE; HUMAN; MAJOR CLINICAL STUDY; MALE; MULTIPLE SCLEROSIS; MUTATOR GENE; NEUROIMAGING; PREDICTIVE VALUE; PRIORITY JOURNAL; REGULATOR GENE; SINGLE NUCLEOTIDE POLYMORPHISM; VOLUMETRY;

ADULT; AGED; BRAIN; COHORT STUDIES; FEMALE; GENETIC VARIATION; GENOTYPE; HISTONE DEACETYLASES; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; MULTIPLE SCLEROSIS; POLYMORPHISM, SINGLE NUCLEOTIDE; PREDICTIVE VALUE OF TESTS; REGRESSION ANALYSIS; YOUNG ADULT;

EID: 84868005204     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2012.07.007     Document Type: Article

References (73)

1. Szymański P., Markowicz M., Janik A., Ciesielski M., Mikiciuk-Olasik E. Neuroimaging diagnosis in neurodegenerative diseases. Nucl. Med. Rev. Cent. East. Eur 2010, 13:23-31.
2. Albani D., Polito L., Signorini A., Forloni G. Neuroprotective properties of resveratrol in different neurodegenerative disorders. Biofactors 2010, 36:370-376.
3. Aljada A., Dong L., Mousa S.A. Sirtuin-targeting drugs: mechanisms of action and potential therapeutic applications. Curr. Opin. Investig. Drugs 2010, 11:1158-1168.
4. Arnold A.C. Evolving management of optic neuritis and multiple sclerosis. Am. J. Ophthalmol 2005, 139:1101-1108.
5. Ayers K.L., Cordell H.J. SNP selection in genome-wide and candidate gene studies via penalized logistic regression. Genet. Epidemiol 2010, 34:879-891.
6. 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. Pathway and network-based analysis of genome-wide association studies in multiple sclerosis. Hum. Mol. Genet 2009, 18:2078-2090. GeneMSA Consortium.
7. Baranzini S.E., Srinivasan R., Khankhanian P., Okuda D.T., Nelson S.J., Matthews P.M., Hauser S.L., Oksenberg J.R., Pelletier D. Genetic variation influences glutamate concentrations in brains of patients with multiple sclerosis. Brain 2010, 133:2603-2611.
8. Benjamini Y., Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. B Stat. Methodol 1995, 57:289-300.
9. Benjamini Y., Yekutieli D. The control of the false discovery rate in multiple testing under dependency. Ann. Statist 2001, 29:1165-1188.
10. Blander G., Guarente L. The Sir2 family of protein deacetylases. Annu. Rev. Biochem 2004, 73:417-435.
11. Bolger T.A., Yao T.P. Intracellular trafficking of histone deacetylase 4 regulates neuronal cell death. J. Neurosci 2005, 25:9544-9553.
12. Camelo S., Iglesias A.H., Hwang D., Due B., Ryu H., Smith K., Gray S.G., Imitola J., Duran G., Assaf B., Langley B., Khoury S.J., Stephanopoulos G., De Girolami U., Ratan R.R., Ferrante R.J., Dangond F. Transcriptional therapy with the histone deacetylase inhibitor trichostatin A ameliorates experimental autoimmune encephalomyelitis. J. Neuroimmunol 2005, 164:10-21.
13. Chuang D.M., Leng Y., Marinova Z., Kim H.J., Chiu C.T. Multiple roles of HDAC inhibition in neurodegenerative conditions. Trends Neurosci 2009, 32:591-601.
14. de Oliveira R.M., Pais T.F., Outeiro T.F. Sirtuins: common targets in aging and in neurodegeneration. Curr. Drug Targets 2010, 11:1270-1280.
15. Disanto G., Berlanga A.J., Handel A.E., Para A.E., Burrell A.M., Fries A., Handunnetthi L., De Luca G.C., Morahan J.M. Heterogeneity in multiple sclerosis: scratching the surface of a complex disease. J. Autoimmune Dis 2011, 2011:932351.
16. El-Maarri O., Kareta M.S., Mikeska T., Becker T., Diaz-Lacava A., Junen J., Nüsgen N., Behne F., Wienker T., Waha A., Oldenburg J., Chédin F. A systematic search for DNA methyltransferase polymorphisms reveals a rare DNMT3L variant associated with subtelomeric hypomethylation. Hum. Mol. Genet 2009, 18:1755-1768.
17. Filippi M., Rocca M.A., Barkhof F., Brück W., Chen J.T., Comi G., DeLuca G., De Stefano N., Erickson B.J., Evangelou N., Fazekas F., Geurts J.J., Lucchinetti C., Miller D.H., Pelletier D., Popescu B.F., Lassmann H. Association between pathological and MRI findings in multiple sclerosis. Lancet Neurol 2012, 11:349-360. Attendees of the Correlation between Pathological MRI findings in MS workshop.
18. Faraco G., Cavone L., Chiarugi A. The therapeutic potential of HDAC inhibitors in the treatment of multiple sclerosis. Mol. Med 2011, 17:442-447.
19. Geurts J.J., Wolswijk G., Bö L., Redeker S., Ramkema M., Troost D., Aronica E. Expression patterns of Group III metabotropic glutamate receptors mGluR4 and mGluR8 in multiple sclerosis lesions. J. Neuroimmunol 2005, 158:182-190.
20. Geurts J.J., Wolswijk G., Bö L., van der Valk P., Polman C.H., Troost D., Aronica E. Altered expression patterns of group I and II metabotropic glutamate receptors in multiple sclerosis. Brain 2003, 126:1755-1766.
21. Gray S.G., Dangond F. Rationale for the use of histone deacetylase inhibitors as a dual therapeutic modality in multiple sclerosis. Epigenetics 2006, 1:67-75.
22. Haigis M.C., Mostoslavsky R., Haigis K.M., Fahie K., Christodoulou D.C., Murphy A.J., Valenzuela D.M., Yancopoulos G.D., Karow M., Blander G., Wolberger C., Prolla T.A., Weindruch R., Alt F.W., Guarente L. SIRT4 inhibits glutamate dehydrogenase and opposes the effects of calorie restriction in pancreatic beta cells. Cell 2006, 126:941-954.
23. Hauser S.L., Goodkin D.E. Multiple sclerosis and other demyelinating diseases. Harrison's Principles of Internal Medicine 2001, 2452-2461. McGraw-Hill, New York. 15th ed. E. Braunwald, S.L. Hauser, A.S. Fauci, D.L. Longo, D.L. Kasper, J.L. Jameson (Eds.).
24. Hauser S.L., Oksenberg J.R. The neurobiology of multiple sclerosis: genes, inflammation, and neurodegeneration. Neuron 2006, 52:61-76.
25. Healy B.C., Liguori M., Tran D., Chitnis T., Glanz B., Wolfish C., Gauthier S., Buckle G., Houtchens M., Stazzone L., Khoury S., Hartzmann R., Fernandez-Vina M., Hafler D.A., Weiner H.L., Guttmann C.R., De Jager P.L. HLA B*44: protective effects in MS susceptibility and MRI outcome measures. Neurology 2010, 75:634-640.
26. Hickman S.J., Kapoor R., Jones S.J., Altmann D.R., Plant G.T., Miller D.H. Corticosteroids do not prevent optic nerve atrophy following optic neuritis. J. Neurol. Neurosurg. Psychiatry 2003, 74:1139-1141.
27. Hochberg Y., Tamhane A. Multiple Comparison Procedures 1987, Wiley Online Library, NJ, USA.
28. Horakova D., Zivadinov R., Weinstock-Guttman B., Havrdova E., Tamaño-Blanco M., Tyblova M., Hussein S., Bergsland N., Willis L., Krasensky J., Vaneckova M., Seidl Z., Lelkova P., Ramanathan M. HLA DRB1*1501 is only modestly associated with lesion burden at the first demyelinating event. J. Neuroimmunol 2011, 236:76-80.
29. Howitz K.T., Bitterman K.J., Cohen H.Y., Lamming D.W., Lavu S., Wood J.G., Zipkin R.E., Chung P., Kisielewski A., Zhang L.L., Scherer B., Sinclair D.A. Small molecule activators of sirtuins extend Saccharomyces cerevisiae lifespan. Nature 2003, 425:191-196.
30. Hsieh J., Nakashima K., Kuwabara T., Mejia E., Gage F.H. Histone deacetylase inhibition-mediated neuronal differentiation of multipotent adult neural progenitor cells. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:16659-16664.
31. Huang J.Y., Hirschey M.D., Shimazu T., Ho L., Verdin E. Mitochondrial sirtuins. Biochim. Biophys. Acta 2010, 1804:1645-1651.
32. Jastorff A.M., Haegler K., Maccarrone G., Holsboer F., Weber F., Ziemssen T., Turck C.W. Regulation of proteins mediating neurodegeneration in experimental autoimmune encephalomyelitis and multiple sclerosis. Proteomics Clin. Appl 2009, 3:1273-1287.
33. Jones P.A., Takai D. The role of DNA methylation in mammalian epigenetics. Science 2001, 293:1068-1070.
34. Kaneko S., Wang J., Kaneko M., Yiu G., Hurrell J.M., Chitnis T., Khoury S.J., He Z. Protecting axonal degeneration by increasing nicotinamide adenine dinucleotide levels in experimental autoimmune encephalomyelitis models. J. Neurosci 2006, 26:9794-9804.
35. Kazantsev A.G., Thompson L.M. Therapeutic application of histone deacetylase inhibitors for central nervous system disorders. Nat. Rev. Drug Discov 2008, 7:854-868.
36. Kelly G.S. A review of the sirtuin system, its clinical implications, and the potential role of dietary activators like resveratrol: part 2. Altern. Med. Rev 2010, 15:313-328.
37. Kim J.Y., Shen S., Dietz K., He Y., Howell O., Reynolds R., Casaccia P. HDAC1 nuclear export induced by pathological conditions is essential for the onset of axonal damage. Nat. Neurosci 2010, 13:180-189.
38. Kurtzke J.F. Rating neurologic impairment in multiple sclerosis: an expanded disability status scale (EDSS). Neurology 1983, 33:1444-1452.
39. Lassman H. The pathologic substrate of magnetic resonance alterations in multiple sclerosis. Neuroimaging Clin. N. Am 2008, 18:563-576.
40. Lauer K. Environmental risk factors in multiple sclerosis. Expert Rev. Neurother 2010, 10:421-440.
41. Lin M.T., Beal M.F. Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 2006, 443:787-795.
42. Lu F., Selak M., O'Connor J., Croul S., Lorenzana C., Butunoi C., Kalman B. Oxidative damage to mitochondrial DNA and activity of mitochondrial enzymes in chronic active lesions of multiple sclerosis. J. Neurol. Sci 2000, 177:95-103.
43. Mahad D., Lassmann H., Turnbull D. Review: mitochondria and disease progression in multiple sclerosis. Neuropathol. Appl. Neurobiol 2008, 34:577-589.
44. Mahad D.J., Ziabreva I., Campbell G., Lax N., White K., Hanson P.S., Lassmann H., Turnbull D.M. Mitochondrial changes within axons in multiple sclerosis. Brain 2009, 132:1161-1174.
45. Matute C., Alberdi E., Domercq M., Pérez-Cerdá F., Pérez-Samartín A., Sánchez-Gómez M.V. The link between excitotoxic oligodendroglial death and demyelinating diseases. Trends Neurosci 2001, 24:224-230.
46. Meinshausen N., Bühlmann P. Stability selection. J. R. Stat. Soc. B Stat. Methodol 2010, 72:417-473.
47. Miralvès J., Magdeleine E., Kaddoum L., Brun H., Peries S., Joly E. High levels of MeCP2 depress MHC class I expression in neuronal cells. PLoS One 2007, 2:e1354.
48. Oksenberg J.R., Baranzini S.E. Multiple sclerosis genetics-is the glass half full, or half empty?. Nat. Rev. Neurol 2010, 6:429-437.
49. 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. Genotype-Phenotype correlations in multiple sclerosis: HLA genes influence disease severity inferred by 1HMR spectroscopy and MRI measures. Brain 2009, 132:250-259.
50. Parry A., Corkill R., Blamire A.M., Palace J., Narayanan S., Arnold D., Styles P., Matthews P.M. β-Interferon treatment does not always slow the progression of axonal injury in multiple sclerosis. J. Neurol 2003, 250:171-178.
51. 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. Diagnostic criteria for multiple sclerosis: 2005 revisions to the "McDonald Criteria". Ann. Neurol 2005, 58:840-846.
52. Porcu M., Chiarugi A. The emerging therapeutic potential of sirtuin-interacting drugs: from cell death to lifespan extension. Trends Pharmacol. Sci 2005, 26:94-103.
53. Potkin S.G., Turner J.A., Fallon J.A., Lakatos A., Keator D.B., Guffanti G., Macciardi F. Gene discovery through imaging genetics: identification of two novel genes associated with schizophrenia. Mol. Psychiatry 2009, 14:416-428.
54. 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, 81:559-575.
55. Riccio P., Rossano R., Liuzzi G.M. May diet and dietary supplements improve the wellness of multiple sclerosis patients? A molecular approach. J. Autoimmune Dis 2011, 2010:249842.
56. Schalkwyk L.C., Meaburn E.L., Smith R., Dempster E.L., Jeffries A.R., Davies M.N., Plomin R., Mill J. Allelic skewing of DNA methylation is widespread across the genome. Am. J. Hum. Genet 2010, 86:196-212.
57. Shi G., Boerwinkle E., Morrison A.C., Gu C.C., Chakravarti A., Rao D.C. Mining gold dust under the genome wide significance level: a two-stage approach to analysis of GWAS. Genet. Epidemiol 2011, 35:111-118.
58. Shindler K.S., Ventura E., Dutt M., Elliott P., Fitzgerald D.C., Rostami A. Oral resveratrol reduces neuronal damage in a model of multiple sclerosis. J. Neuroophthalmol 2010, 30:328-339.
59. Shindler K.S., Ventura E., Rex T.S., Elliott P., Rostami A. SIRT1 activation confers neuroprotection in experimental optic neuritis. Invest. Ophthalmol. Vis. Sci 2007, 48:3602-3609.
60. Shoba B., Lwin Z.M., Ling L.S., Bay B.H., Yip G.W., Kumar S.D. Function of sirtuins in biological tissues. Anat. Rec. (Hoboken) 2009, 292:536-543.
61. Siebzehnrubl F.A., Buslei R., Eyupoglu I.Y., Seufert S., Hahnen E., Blumcke I. Histone deacetylase inhibitors increase neuronal differentiation in adult forebrain precursor cells. Exp. Brain Res 2007, 176:672-678.
62. Smith S.M., Zhang Y., Jenkinson M., Chen J., Matthews P.M., Federico A., De Stefano N. Accurate, robust, and automated longitudinal and cross-sectional brain change analysis. Neuroimage 2002, 17:479-489.
63. Sombekke M.H., Lukas C., Crusius J.B., Tejedor D., Killestein J., Arteta D., Martínez A., Uitdehaag B.M., Knol D.L., Peña A.S., Geurts J.J., De Jager P.L., Barkhof F., Vrenken H., Polman C.H. HLA-DRB1*1501 and spinal cord magnetic resonance imaging lesions in multiple sclerosis. Arch. Neurol 2009, 66:1531-1536.
64. Stein J.L., Hua X., Lee S., Ho A.J., Leow A.D., Toga A.W., Saykin A.J., Shen L., Foroud T., Pankratz N., Huentelman M.J., Craig D.W., Gerber J.D., Allen A.N., Corneveaux J.J., Dechairo B.M., Potkin S.G., Weiner M.W., Thompson P. Voxelwise genome-wide association study (vGWAS). NeuroImage 2010, 53:1160-1174. Alzheimer's Disease Neuroimaging Initiative.
65. Tibshirani R. Regression shrinkage and selection via the Lasso. J. R. Stat. Soc. B Stat. Methodol 1996, 58:267-288.
66. Urdinguio R.G., Sanchez-Mut J.V., Esteller M. Epigenetic mechanisms in neurological diseases: genes, syndromes, and therapies. Lancet Neurol 2009, 8:1056-1072.
67. Verdin E., Hirschey M.D., Finley L.W., Haigis M.C. Sirtuin regulation of mitochondria: energy production, apoptosis, and signaling. Trends Biochem. Sci 2010, 35:669-675.
68. Vounou M., Nichols T.E., Montana G. Discovering genetic associations with high-dimensional neuroimaging phenotypes: a sparse reduced-rank regression approach. Neuroimage 2010, 53:1147-1159. Alzheimer's Disease Neuroimaging Initiative.
69. Vukusic S., Confavreux C. Natural history of multiple sclerosis: risk factors and prognostic indicators. Curr. Opin. Neurol 2007, 20:269-274.
70. Werner P., Pitt D., Raine C.S. Multiple sclerosis: altered glutamate homeostasis in lesions correlates with oligodendrocyte and axonal damage. Ann. Neurol 2001, 50:169-180.
71. Witte M.E., Bø L., Rodenburg R.J., Belien J.A., Musters R., Hazes T., Wintjes L.T., Smeitink J.A., Geurts J.J., De Vries H.E., van der Valk P., van Horssen J. Enhanced number and activity of mitochondria in multiple sclerosis lesions. J. Pathol 2009, 219:193-204.
72. Witte M.E., Geurts J.J., de Vries H.E., van der Valk P., van Horssen J. Mitochondrial dysfunction: a potential link between neuroinflammation and neurodegeneration?. Mitochondrion 2010, 10:411-418.
73. Zivadinov R., Uxa L., Zacchi T., Nasuelli D., Ukmar M., Furlan C., Pozzi-Mucelli R., Tommasi M.A., Locatelli L., Ulivi S., Bratina A., Bosco A., Grop A., Cazzato G., Zorzon M. HLA genotypes and disease severity assessed by magnetic resonance imaging findings in patients with multiple sclerosis. J. Neurol 2003, 250:1099-1106.