Gene expression, methylation and neuropathology correlations at progressive supranuclear palsy risk loci

Acta Neuropathologica

Volumn 132, Issue 2, 2016, Pages 197-211

  Allen, Mariet ^a   Burgess, Jeremy D ^a   Ballard, Travis ^a   Serie, Daniel ^b   Wang, Xue ^b   Younkin, Curtis S ^a   Sun, Zhifu ^c   Kouri, Naomi ^a   Baheti, Saurabh ^c   Wang, Chen ^c   Carrasquillo, Minerva M ^a   Nguyen, Thuy ^a   Lincoln, Sarah ^a   Malphrus, Kimberly ^a   Murray, Melissa ^a   Golde, Todd E ^d   Price, Nathan D ^e   Younkin, Steven G ^a   Schellenberg, Gerard D ^f   Asmann, Yan ^b   Ordog, Tamas ^a   Crook, Julia ^b   Dickson, Dennis ^a   Ertekin Taner, Nilüfer ^a,b   more..

^a MAYO GRADUATE SCHOOL   (United States)

^b MAYO CLINIC   (United States)

^c MAYO CLINIC   (United States)

^d UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^e INSTITUTE FOR SYSTEMS BIOLOGY   (United States)

^f UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Association; Brain tissue; Epigenetic; Genetic risk; Neuropathology traits; Progressive supranuclear palsy; Transcription

Indexed keywords

DNA; TAU PROTEIN;

AGED; ARL17A GENE; ARL17B GENE; ARTICLE; ASTROCYTE; AUTOPSY; COILED BODY; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; ENDOPHENOTYPE; FEMALE; GENE EXPRESSION; GENETIC RISK; GENOME-WIDE ASSOCIATION STUDY; HUMAN; HUMAN TISSUE; LRRC37A4 GENE; MALE; MAPT GENE; MOBP GENE; NEUROPATHOLOGY; PRIORITY JOURNAL; PROGRESSIVE SUPRANUCLEAR PALSY; QUANTITATIVE ANALYSIS; SINGLE NUCLEOTIDE POLYMORPHISM; TEMPORAL CORTEX; ALLELE; GENE LOCUS; GENETICS; METABOLISM; PHYSIOLOGY; PROCEDURES; RISK; VERY ELDERLY;

AGED; AGED, 80 AND OVER; ALLELES; DNA METHYLATION; FEMALE; GENE EXPRESSION; GENETIC LOCI; GENOME-WIDE ASSOCIATION STUDY; HUMANS; MALE; NEUROPATHOLOGY; POLYMORPHISM, SINGLE NUCLEOTIDE; RISK; SUPRANUCLEAR PALSY, PROGRESSIVE; TAU PROTEINS;

EID: 84964426521     PISSN: 00016322     EISSN: 14320533     Source Type: Journal    
DOI: 10.1007/s00401-016-1576-7     Document Type: Article

References (48)

1. Allen M, Kachadoorian M, Quicksall Z, Zou F, Chai HS, Younkin C et al (2014) Association of MAPT haplotypes with Alzheimer’s disease risk and MAPT brain gene expression levels. Alzheimers Res Ther 6:39. doi:10.1186/alzrt268
2. Allen M, Kachadoorian M, Carrasquillo MM, Karhade A, Manly L, Burgess JD et al (2015) Late-onset Alzheimer disease risk variants mark brain regulatory loci. Neurol Genet 1:e15
3. Bekpen C, Tastekin I, Siswara P, Akdis CA, Eichler EE (2012) Primate segmental duplication creates novel promoters for the LRRC37 gene family within the 17q21.31 inversion polymorphism region. Genome Res 22:1050–1058. doi:10.1101/gr.134098.111
4. Bennett DA, Yu L, Yang J, Srivastava GP, Aubin C, De Jager PL (2015) Epigenomics of Alzheimer’s disease. Transl Res 165:200–220. doi:10.1016/j.trsl.2014.05.006
5. Boettger LM, Handsaker RE, Zody MC, McCarroll SA (2012) Structural haplotypes and recent evolution of the human 17q21.31 region. Nat Genet 44:881–885. doi:10.1038/ng.2334
6. Bollen KA (2002) Latent variables in psychology and the social sciences. Annu Rev Psychol 53:605–634. doi:10.1146/annurev.psych.53.100901.135239
7. Carrasquillo MM, Zou F, Pankratz VS, Wilcox SL, Ma L, Walker LP et al (2009) Genetic variation in PCDH11X is associated with susceptibility to late-onset Alzheimer’s disease. Nat Genet 41:192–198. doi:10.1038/ng.305
8. Coupland KG, Mellick GD, Silburn PA, Mather K, Armstrong NJ, Sachdev PS et al (2014) DNA methylation of the MAPT gene in Parkinson’s disease cohorts and modulation by vitamin E in vitro. Mov Disord 29:1606–1614. doi:10.1002/mds.25784
9. De Jager PL, Srivastava G, Lunnon K, Burgess J, Schalkwyk LC, Yu L et al (2014) Alzheimer’s disease: early alterations in brain DNA methylation at ANK1, BIN1, RHBDF2 and other loci. Nat Neurosci 17:1156–1163. doi:10.1038/nn.3786
10. de Jong S, Chepelev I, Janson E, Strengman E, van den Berg LH, Veldink JH et al (2012) Common inversion polymorphism at 17q21.31 affects expression of multiple genes in tissue-specific manner. BMC Genom 13:458. doi:10.1186/1471-2164-13-458
11. Desikan RS, Schork AJ, Wang Y, Witoelar A, Sharma M, McEvoy LK et al (2015) Genetic overlap between Alzheimer’s disease and Parkinson’s disease at the MAPT locus. Mol Psychiatry 20:1588–1595. doi:10.1038/mp.2015.6
12. Dickson DW, Rademakers R, Hutton ML (2007) Progressive supranuclear palsy: pathology and genetics. Brain Pathol 17:74–82. doi:10.1111/j.1750-3639.2007.00054.x
13. Donker Kaat L, Boon AJ, Azmani A, Kamphorst W, Breteler MM, Anar B et al (2009) Familial aggregation of parkinsonism in progressive supranuclear palsy. Neurology 73:98–105. doi:10.1212/WNL.0b013e3181a92bcc
14. Du P, Kibbe WA, Lin SM (2008) lumi: a pipeline for processing Illumina microarray. Bioinformatics 24:1547–1548. doi:10.1093/bioinformatics/btn224
15. Ertekin-Taner N, De Jager PL, Yu L, Bennett DA (2013) Alternative approaches in gene discovery and characterization in Alzheimer’s disease. Curr Genet Med Rep 1:39–51. doi:10.1007/s40142-013-0007-5
16. Ferrari R, Ryten M, Simone R, Trabzuni D, Nicolaou N, Hondhamuni G et al (2014) Assessment of common variability and expression quantitative trait loci for genome-wide associations for progressive supranuclear palsy. Neurobiol Aging 35(1514):e1511–e1512. doi:10.1016/j.neurobiolaging.2014.01.010
17. Goedert M (2015) Neurodegeneration. Alzheimer’s and Parkinson’s diseases: the prion concept in relation to assembled Abeta, tau, and alpha-synuclein. Science 349:1255555. doi:10.1126/science.1255555
18. Hauw JJ, Daniel SE, Dickson D, Horoupian DS, Jellinger K, Lantos PL et al (1994) Preliminary NINDS neuropathologic criteria for Steele-Richardson-Olszewski syndrome (progressive supranuclear palsy). Neurology 44:2015–2019
19. Hoglinger GU, Melhem NM, Dickson DW, Sleiman PM, Wang LS, Klei L et al (2011) Identification of common variants influencing risk of the tauopathy progressive supranuclear palsy. Nat Genet 43:699–705. doi:10.1038/ng.859
20. Im SY, Kim YE, Kim YJ (2015) Genetics of progressive supranuclear palsy. J Mov Disord 8:122–129. doi:10.14802/jmd.15033
21. Iwata A, Nagata K, Hatsuta H, Takuma H, Bundo M, Iwamoto K et al (2014) Altered CpG methylation in sporadic Alzheimer’s disease is associated with APP and MAPT dysregulation. Hum Mol Genet 23:648–656. doi:10.1093/hmg/ddt451
22. Jowaed A, Schmitt I, Kaut O, Wullner U (2010) Methylation regulates alpha-synuclein expression and is decreased in Parkinson’s disease patients’ brains. J Neurosci 30:6355–6359. doi:10.1523/JNEUROSCI.6119-09.2010
23. Kett LR, Dauer WT (2012) Leucine-rich repeat kinase 2 for beginners: six key questions. Cold Spring Harb Perspect Med 2:a009407. doi:10.1101/cshperspect.a009407
24. Kouri N, Ross OA, Dombroski B, Younkin CS, Serie DJ, Soto-Ortolaza A et al (2015) Genome-wide association study of corticobasal degeneration identifies risk variants shared with progressive supranuclear palsy. Nat Commun 6:7247. doi:10.1038/ncomms8247
25. Li Y, Chen JA, Sears RL, Gao F, Klein ED, Karydas A et al (2014) An epigenetic signature in peripheral blood associated with the haplotype on 17q21.31, a risk factor for neurodegenerative tauopathy. PLoS Genet 10:e1004211. doi:10.1371/journal.pgen.1004211
26. Lincoln S, Allen M, Cox CL, Walker LP, Malphrus K, Qiu Y et al (2013) LRRTM3 interacts with APP and BACE1 and has variants associating with late-onset Alzheimer’s disease (LOAD). PLoS One 8:e64164. doi:10.1371/journal.pone.0064164
27. Lunnon K, Mill J (2013) Epigenetic studies in Alzheimer’s disease: current findings, caveats, and considerations for future studies. Am J Med Genet B Neuropsychiatr Genet 162B:789–799. doi:10.1002/ajmg.b.32201
28. Majercak J, Ray WJ, Espeseth A, Simon A, Shi XP, Wolffe C et al (2006) LRRTM3 promotes processing of amyloid-precursor protein by BACE1 and is a positional candidate gene for late-onset Alzheimer’s disease. Proc Natl Acad Sci 103:17967–17972. doi:10.1073/pnas.0605461103
29. Myers AJ, Pittman AM, Zhao AS, Rohrer K, Kaleem M, Marlowe L et al (2007) The MAPT H1c risk haplotype is associated with increased expression of tau and especially of 4 repeat containing transcripts. Neurobiol Dis 25:561–570. doi:10.1016/j.nbd.2006.10.018
30. Ng CW, Yildirim F, Yap YS, Dalin S, Matthews BJ, Velez PJ et al (2013) Extensive changes in DNA methylation are associated with expression of mutant huntingtin. Proc Natl Acad Sci 110:2354–2359. doi:10.1073/pnas.1221292110
31. Pastor P, Moreno F, Clarimon J, Ruiz A, Combarros O, Calero M et al (2015) MAPT H1 haplotype is associated with late-onset Alzheimer’s disease risk in APOEvarepsilon4 noncarriers: results from the Dementia Genetics Spanish Consortium. J Alzheimers Dis 49:343–352. doi:10.3233/JAD-150555
32. Patterson N, Price AL, Reich D (2006) Population structure and eigenanalysis. PLoS Genet 2:e190. doi:10.1371/journal.pgen.0020190
33. Pittman AM, Myers AJ, Abou-Sleiman P, Fung HC, Kaleem M, Marlowe L et al (2005) Linkage disequilibrium fine mapping and haplotype association analysis of the tau gene in progressive supranuclear palsy and corticobasal degeneration. J Med Genet 42:837–846. doi:10.1136/jmg.2005.031377
34. Price AL, Patterson NJ, Plenge RM, Weinblatt ME, Shadick NA, Reich D (2006) Principal components analysis corrects for stratification in genome-wide association studies. Nat Genet 38:904–909. doi:10.1038/ng1847
35. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, Bender D et al (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 81:559–575. doi:10.1086/519795
36. Rademakers R, Melquist S, Cruts M, Theuns J, Del-Favero J, Poorkaj P et al (2005) High-density SNP haplotyping suggests altered regulation of tau gene expression in progressive supranuclear palsy. Hum Mol Genet 14:3281–3292. doi:10.1093/hmg/ddi361
37. Rizopoulos D (2006) ltm: an R Package for latent variable modeling and item response theory analyses. J Stat Softw 17:1–25
38. Rojo A, Pernaute RS, Fontan A, Ruiz PG, Honnorat J, Lynch T et al (1999) Clinical genetics of familial progressive supranuclear palsy. Brain 122(Pt 7):1233–1245
39. Seixas E, Barros M, Seabra MC, Barral DC (2013) Rab and Arf proteins in genetic diseases. Traffic 14:871–885. doi:10.1111/tra.12072
40. Simon-Sanchez J, Schulte C, Bras JM, Sharma M, Gibbs JR, Berg D et al (2009) Genome-wide association study reveals genetic risk underlying Parkinson’s disease. Nat Genet 41:1308–1312. doi:10.1038/ng.487
41. Steinberg KM, Antonacci F, Sudmant PH, Kidd JM, Campbell CD, Vives L et al (2012) Structural diversity and African origin of the 17q21.31 inversion polymorphism. Nat Genet 44:872–880. doi:10.1038/ng.2335
42. Stranger BE, Forrest MS, Clark AG, Minichiello MJ, Deutsch S, Lyle R et al (2005) Genome-wide associations of gene expression variation in humans. PLoS Genet 1:e78. doi:10.1371/journal.pgen.0010078
43. Sun Z, Baheti S, Middha S, Kanwar R, Zhang Y, Li X et al (2012) SAAP-RRBS: streamlined analysis and annotation pipeline for reduced representation bisulfite sequencing. Bioinformatics 28:2180–2181. doi:10.1093/bioinformatics/bts337
44. Willer CJ, Li Y, Abecasis GR (2010) METAL: fast and efficient meta-analysis of genomewide association scans. Bioinformatics 26:2190–2191. doi:10.1093/bioinformatics/btq340
45. Yamamoto Y, Mizuno R, Nishimura T, Ogawa Y, Yoshikawa H, Fujimura H et al (1994) Cloning and expression of myelin-associated oligodendrocytic basic protein. A novel basic protein constituting the central nervous system myelin. J Biol Chem 269:31725–31730
46. Zhang H, Zhang YW, Chen Y, Huang X, Zhou F, Wang W et al (2012) Appoptosin is a novel pro-apoptotic protein and mediates cell death in neurodegeneration. J Neurosci 32:15565–15576. doi:10.1523/JNEUROSCI.3668-12.2012
47. Zhao Y, Tseng IC, Heyser CJ, Rockenstein E, Mante M, Adame A et al (2015) Appoptosin-mediated caspase cleavage of tau contributes to progressive supranuclear palsy pathogenesis. Neuron 87:963–975. doi:10.1016/j.neuron.2015.08.020
48. Zou F, Chai HS, Younkin CS, Allen M, Crook J, Pankratz VS et al (2012) Brain expression genome-wide association study (eGWAS) identifies human disease-associated variants. PLoS Genet 8:e1002707. doi:10.1371/journal.pgen.1002707