MAPT H1 haplotype is associated with late-onset Alzheimer's disease risk in APOE ε 4 noncarriers: Results from the dementia genetics Spanish consortium

Journal of Alzheimer's Disease

Volumn 49, Issue 2, 2015, Pages 343-352

  Pastor, Pau ^a,b,c   Moreno, Fermín ^b,d   Clarimón, Jordi ^b,e   Ruiz, Agustín ^f   Combarros, Onofre ^b,g   Calero, Miguel ^b,f   De Munain, Adolfo López ^b,d,i   Bullido, Maria J ^b,j,k   De Pancorbo, Marian M ⁱ   Carro, Eva ^b,l   Antonell, Anna ^m   Coto, Eliecer ⁿ   Ortega Cubero, Sara ^a,b   Hernandez, Isabel ^f   Tárraga, Lluís ^f   Boada, Mercè ^f   Lleó, Alberto ^b,e   Dols Icardo, Oriol ^b,e   Kulisevsky, Jaime ^b,e,o   Vázquez Higuera, José Luis ^b,g   Infante, Jon ^b,g   Rábano, Alberto ^b,p   Fernández Blázquez, Miguel Ángel ^h   Valentí, Meritxell ^h   Indakoetxea, Begoña ^b,d   Barandiarán, Myriam ^b,d   Gorostidi, Ana ^b,i   Frank García, Ana ^b,k   Sastre, Isabel ^b,j,k   Lorenzo, Elena ^a,b   Pastor, María A ^a,b,q   Elcoroaristizabal, Xabier ⁱ   Lennarz, Martina ^r   Maier, Wolfang ^r,s   Rámirez, Alfredo ^r   Serrano Ríos, Manuel ^t   Lee, Suzee E ^u   Sánchez Juan, Pascual ^b,g   more..

^a UNIVERSITY OF NAVARRA   (Spain)

^b CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED SOBRE ENFERMEDADES NEURODEGENERATIVAS CIBERNED   (Spain)

^c HOSPITAL MÚTUA DE TERRASSA   (Spain)

^d HOSPITAL DONOSTIA   (Spain)

^e UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^f Institut Catala de Neurociencies Aplicades   (Spain)

^g HOSPITAL UNIVERSITARIO MARQUÉS DE VALDECILLA   (Spain)

^h INSTITUTO DE SALUD CARLOS III   (Spain)

ⁱ UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

^j CENTRO DE BIOLOGÍA MOLECULAR SEVERO OCHOA   (Spain)

^k HOSPITAL UNIVERSITARIO LA PAZ   (Spain)

^l Universidad Complutense   (Spain)

^m HOSPITAL CLÍNIC   (Spain)

ⁿ HOSPITAL UNIVERSITARIO CENTRAL DE ASTURIAS   (Spain)

^o UNIVERSITAT OBERTA DE CATALUNYA   (Spain)

^p Alzheimer Center Reina Sofia Foundation   (Spain)

^q UNIVERSITY CLINIC OF NAVARRA   (Spain)

^r UNIVERSITY OF BONN   (Germany)

^s GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^t HOSPITAL CLÍNICO SAN CARLOS   (Spain)

^u UNIVERSITY OF CALIFORNIA   (United States)

more..

Author keywords

A152T; Alzheimer's disease; frontotemporal dementia; genetic association; H1H2; MAPT

Indexed keywords

AGED; ALZHEIMER DISEASE; APOE EPSILON4 GENE; ARTICLE; CONTROLLED STUDY; FEMALE; FRONTOTEMPORAL DEMENTIA; GENE; GENE LINKAGE DISEQUILIBRIUM; GENETIC ASSOCIATION; GENETIC LINKAGE; GENETIC RISK; GENETIC VARIABILITY; GENOTYPE; HAPLOTYPE; HUMAN; MAJOR CLINICAL STUDY; MALE; MAPT GENE; ONSET AGE; PARKINSON DISEASE; PRIORITY JOURNAL; PROGRESSIVE SUPRANUCLEAR PALSY; SINGLE NUCLEOTIDE POLYMORPHISM; SPAIN; GENETIC PREDISPOSITION; GENETICS; MIDDLE AGED; STATISTICAL MODEL; VERY ELDERLY;

APOLIPOPROTEIN E4; MAPT PROTEIN, HUMAN; TAU PROTEIN;

AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; APOLIPOPROTEIN E4; FEMALE; FRONTOTEMPORAL DEMENTIA; GENETIC PREDISPOSITION TO DISEASE; HAPLOTYPES; HUMANS; LOGISTIC MODELS; MALE; MIDDLE AGED; POLYMORPHISM, SINGLE NUCLEOTIDE; SPAIN; TAU PROTEINS;

EID: 84948692958     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-150555     Document Type: Article

References (39)

1. Goedert M (2004) Tau protein and neurodegeneration. Semin Cell Dev Biol 15, 45-49.
2. Galpern WR, Lang AE (2006) Interface between tauopathies and synucleinopathies, a tale of two proteins. Ann Neurol 59, 449-458.
3. Rademakers R, Cruts M, van Broeckhoven C (2004) The role of tau (MAPT) in frontotemporal dementia and related tauopathies. Hum Mutat 24, 277-295.
4. Ishizawa T, Mattila P, Davies P, Wang D, Dickson DW(2003) Colocalization of tau and alpha-synuclein epitopes in Lewy bodies. J Neuropathol Exp Neurol 62, 389-397.
5. Baker M, Litvan I, Houlden H, Adamson J, Dickson D, Perez-Dur J, Hardy J, Lynch T, Bigio E, Hutton M (1999) Association of an extended haplotype in the tau gene with progressive supranuclear palsy. Hum Mol Genet 8, 711-715.
6. Conrad C, Andreadis A, Trojanowski JQ, Dickson DW, Kang D, Chen X, Wiederholt W, Hansen L, Masliah E, Thal LJ, Katzman R, Xia Y, Saitoh T (1997) Genetic evidence for the involvement of tau in progressive supranuclear palsy. Ann Neurol 41, 277-281.
7. Higgins JJ, Golbe LI, De Biase A, Jankovic J, Factor SA, Adler RL (2000) An extended 5'-Dau susceptibility haplotype in progressive supranuclear palsy. Neurology 55, 1364-1367.
8. Pastor P, Ezquerra M, Perez JC, Chakraverty S, Norton J, Racette BA, McKeel D, Perlmutter JS, Tolosa E, Goate AM (2004) Novel haplotypes in 17q21 are associated with progressive supranuclear palsy. Ann Neurol 56, 249-258.
9. Houlden H, Baker M, Morris HR, MacDonald N, Pickering-BrownS, Adamson J, Lees AJ, RossorMN, QuinnNP, Kertesz A, KhanMN, Hardy J, Lantos PL, St George-Hyslop P, Munoz DG, Mann D, Lang AE, Bergeron C, Bigio EH, Litvan I, Bhatia KP, Dickson D, Wood NW, HuttonM(2001) Corticobasal degeneration and progressive supranuclear palsy share a common tau haplotype. Neurology 56, 1702-1706.
10. Verpillat P, Camuzat A, Hannequin D, Thomas-Anterion C, Puel M, Belliard S, Dubois B, Didic M, MichelBF, Lacomblez L, Moreaud O, Sellal F, Golfier V, Campion D, Clerget-Darpoux F, Brice A (2002) Association between the extended tau haplotype and frontotemporal dementia. Arch Neurol 59, 935-939.
11. Martin ER, Scott WK, Nance MA, Watts RL, Hubble JP, Koller WC, Lyons K, Pahwa R, Stern MB, Colcher A, Hiner BC, Jankovic J, Ondo WG, Allen FH, Goetz CG, Small GW, Masterman D, Mastaglia F, Laing NG, Stajich JM, Ribble RC, BoozeMW, Rogala A, Hauser MA, Zhang F, Gibson RA, Middleton LT, Roses AD, Haines JL, Scott BL, Pericak-Vance MA, Vance JM (2001) Association of single-nucleotide polymorphisms of the tau gene with late-onset Parkinson disease. JAMA 286, 2245-2250.
12. Simon-Sanchez J, Schulte C, Bras JM, Sharma M, Gibbs JR, Berg D, Paisan-Ruiz C, Lichtner P, Scholz SW, Hernandez DG, Kruger R, Federoff M, Klein C, Goate A, Perlmutter J, Bonin M, Nalls MA, Illig T, Gieger C, Houlden H, Steffens M, Okun MS, Racette BA, Cookson MR, Foote KD, Fernandez HH, Traynor BJ, Schreiber S, Arepalli S, Zonozi R, Gwinn K, van der Brug M, Lopez G, Chanock SJ, Schatzkin A, Park Y, Hollenbeck A, Gao J, Huang X, Wood NW, Lorenz D, Deuschl G, Chen H, Riess O, Hardy JA, Singleton AB, Gasser T (2009) Genome-wide association study reveals genetic risk underlying Parkinson's disease. Nat Genet 41, 1308-1312.
13. Pastor P, Ezquerra M, Munoz E, MartiMJ, Blesa R, Tolosa E, Oliva R (2000) Significant association between the tau gene A0/A0 genotype and Parkinson's disease. Ann Neurol 47, 242-245.
14. Myers AJ, Kaleem M, Marlowe L, Pittman AM, Lees AJ, Fung HC, Duckworth J, Leung D, Gibson A, Morris CM, de Silva R, Hardy J (2005) The H1c haplotype at the MAPT locus is associated with Alzheimer's disease. Hum Mol Genet 14, 2399-2404.
15. AlzGene. http://www.alzgene.org/meta.asp?geneID=232. Last updated May 5, 2010, Accessed on August 12, 2014.
16. Lambert J-C, Ibrahim-Verbaas CA, Harold D, Naj AC, Sims R, Bellenguez C, DeStafano AL, Bis JC, Beecham GW, Grenier-BoleyB, Russo G, Thorton-Wells TA, Jones N, Smith AV, Chouraki V, Thomas C, Ikram MA, Zelenika D, Vardarajan BN, Kamatani Y, Lin CF, Gerrish A, Schmidt H, Kunkle B, Dunstan ML, Ruiz A, Bihoreau MT, Choi SH, Reitz C, Pasquier F, Cruchaga C (2013) Extended meta-Analysis of 74, 538 individuals identifies 11 new susceptibility loci for Alzheimer's disease. Nat Genet 45, 1452-1458.
17. Jun G, Ibrahim-Verbaas CA, Vronskaya M, Lambert JC, Chung J, Naj AC, Kunkle BW, Wang LS, Bis JC, Bellenguez C, Harold D, Lunetta KL, Destefano AL, Grenier-Boley B, Sims R, Beecham GW, Smith AV, Chouraki V, Hamilton-Nelson KL, Ikram MA, Fievet N, Denning N, Martin ER, Schmidt H, Kamatani Y, Dunstan ML, Valladares O, Laza AR, Zelenika D, Ramirez A, Foroud TM, Choi SH, Boland A, Becker T, Kukull WA, van der Lee SJ, Pasquier F, Cruchaga C, Beekly D, Fitzpatrick AL, Hanon O, Gill M, Barber R, Gudnason V, Campion D, Love S, Bennett DA, Amin N, Berr C, Tsolaki M, Buxbaum JD, Lopez OL, Deramecourt V, Fox NC, (2015) A novel Alzheimer disease locus located near the gene encoding tau protein. Mol Psychiatry, doi: 10.1038/mp.2015.23
18. Heutink P, Stevens M, Rizzu P, Bakker E, Kros JM, Tibben A, Niermeijer MF, van Duijn CM, Oostra BA, van Swieten JC (1997) Hereditary frontotemporal dementia is linked to chromosome 17q21-q22, a genetic and clinicopathological study of three Dutch families. Ann Neurol 41, 150-159.
19. Hutton M, Lendon CL, Rizzu P, Baker M, Froelich S, Houlden H, Pickering-Brown S, Chakraverty S, Isaacs A, Grover A, Hackett J, Adamson J, Lincoln S, Dickson D, Davies P, Petersen RC, Stevens M, de Graaff E, Wauters E, van Baren J, Hillebrand M, Joosse M, Kwon JM, Nowotny P, Che LK, Norton J, Morris JC, Reed LA, Trojanowski J, Basun H, Lannfelt L, Neystat M, Fahn S, Dark F, Tannenberg T, Dodd PR, Hayward N, Kwok JB, Schofield PR, Andreadis A, Snowden J, Craufurd D, Neary D, Owen F, Oostra BA, Hardy J, Goate A, van Swieten J, Mann D, Lynch T, Heutink P (1998) Association of missense and 5'-splice-site mutations in tau with the inherited dementia FTDP-17. Nature 393, 702-705.
20. Hong M, Zhukareva V, Vogelsberg-Ragaglia V, Wszolek Z, Reed L, Miller BI, Geschwind DH, Bird TD, McKeel D, Goate A, Morris JC, Wilhelmsen KC, Schellenberg GD, Trojanowski JQ, Lee VM (1998) Mutation-specific functional impairments in distinct tau isoforms of hereditary FTDP-17. Science 282, 1914-1917.
21. Murrell JR, Spillantini MG, Zolo P, Guazzelli M, Smith MJ, Hasegawa M, Redi F, Crowther RA, Pietrini P, Ghetti B, Goedert M (1999) Tau gene mutation G389R causes a tauopathy with abundant pick body-like inclusions and axonal deposits. J Neuropathol Exp Neurol 58, 1207-1226.
22. Pickering-Brown S, Baker M, Yen SH, Liu WK, Hasegawa M, Cairns N, Lantos PL, Rossor M, Iwatsubo T, Davies Y, Allsop D, Furlong R, Owen F, Hardy J, Mann D, Hutton M (2000) Pick's disease is associated with mutations in the tau gene. Ann Neurol 48, 859-867.
23. Clark LN, Poorkaj P, Wszolek Z, Geschwind DH, Nasreddine ZS, Miller B, Li D, Payami H, Awert F, Markopoulou K, Andreadis A, D'Souza I, Lee VM, Reed L, Trojanowski JQ, Zhukareva V, Bird T, Schellenberg G, Wilhelmsen KC (1998) Pathogenic implications of mutations in the tau gene in pallido-ponto-nigral degeneration and related neurodegenerative disorders linked to chromosome 17. Proc Natl Acad Sci U S A 95, 13103-13107.
24. Pastor P, Pastor E, Carnero C, Vela R, Garcia T, Amer G, Tolosa E, Oliva R (2001) Familial atypical progressive supranuclear palsy associated with homozigosity for the delN296 mutation in the tau gene. Ann Neurol 49, 263-267.
25. Coppola G, Chinnathambi S, Lee JJ, Dombroski BA, Baker MC, Soto-Ortolaza AI, Lee SE, Klein E, Huang AY, Sears R, Lane JR, Karydas AM, Kenet RO, Biernat J, Wang LS, Cotman CW, Decarli CS, Levey AI, Ringman JM, Mendez MF, Chui HC, Le Ber I, Brice A, Lupton MK, Preza E, Lovestone S, Powell J, Graff-Radford N, Petersen RC, Boeve BF, Lippa CF, Bigio EH, Mackenzie I, Finger E, Kertesz A, Caselli RJ, Gearing M, Juncos JL, Ghetti B, Spina S, Bordelon YM, Tourtellotte WW, Frosch MP, Vonsattel JP, Zarow C, Beach TG, Albin RL, Lieberman AP, Lee VM, Trojanowski JQ, Van Deerlin VM, Bird TD, Galasko DR, Masliah E, White CL, Troncoso JC, Hannequin D, Boxer AL, Geschwind MD, Kumar S, Mandelkow EM, Wszolek ZK, Uitti RJ, Dickson DW, Haines JL, Mayeux R, Pericak-Vance MA, Farrer LA, Alzheimer's Disease Genetics Consortium, Ross OA, Rademakers R, Schellenberg GD, Miller BL, Mandelkow E, Geschwind DH (2012) Evidence for a role of the rare p. A152T variant in MAPT in increasing the risk for FTD-spectrum and Alzheimer's diseases. Hum Mol Genet 21, 3500-3512.
26. Lee SE, Tartaglia MC, Yener G, Genc S, Seeley WW, Sanchez-Juan P, Moreno F, Mendez MF, Klein E, Rademakers R, Munain AL, Combarros O, Kramer JH, Kenet RO, Boxer AL, Geschwind MD, Gorno-Dempini ML, Karydas AM, Rabinovici GD, Coppola G, Geschwind DH, Miller BL (2013) Neurodegenerative disease phenotypes in carriers of MAPT p. A152T, a risk factor for frontotemporal dementia spectrum disorders and Alzheimer disease. Alzheimer Dis Assoc Disord 27, 302-309.
27. Kara E, Ling H, Pittman AM, Shaw K, de Silva R, Simone R, Holton JL, Warren JD, Rohrer JD, Xiromerisiou G, Lees A, Hardy J, Houlden H, Revesz T (2012) The MAPT p. A152T variant is a risk factor associated with tauopathies with atypical clinical and neuropathological features. Neurobiol Aging 33, 2231.e7-2231.e14.
28. McKhann G, Drachman D, Folstein M, Katzman R, Price D, Stadlan EM (1984) Clinical diagnosis of Alzheimer's disease, report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer's Disease. Neurology 34, 939-944.
29. Rascovsky K, Hodges JR, Knopman D, Mendez MF, Kramer JH, Neuhaus J, van Swieten JC, Seelaar H, Dopper EG, Onyike CU, Hillis AE, Josephs KA, Boeve BF, Kertesz A, Seeley WW, Rankin KP, Johnson JK, Gorno-Dempini ML, Rosen H, Prioleau-Latham CE, Lee A, Kipps CM, Lillo P, Piguet O, Rohrer JD, Rossor MN, Warren JD, Fox NC, Galasko D, Salmon DP, Black SE, Mesulam M, Weintraub S, Dickerson BC, Diehl-Schmid J, Pasquier F, Deramecourt V, Lebert F, PijnenburgY, ChowTW, Manes F, Grafman J, Cappa SF, Freedman M, Grossman M, Miller BL (2011) Sensitivity of revised diagnostic criteria for the behavioural variant of frontotemporal dementia. Brain 134, 2456-2477.
30. Litvan I, Agid Y, Calne D, Campbell G, Dubois B, Duvoisin RC, Goetz CG, Golbe LI, Grafman J, Growdon JH, Hallett M, Jankovic J, Quinn NP, Tolosa E, Zee DS (1996) Clinical research criteria for the diagnosis of progressive supranuclear palsy (Steele-Richardson-Olszewski syndrome), report of the NINDS-SPSP international workshop. Neurology 47, 1-9.
31. Hughes AJ, Daniel SE, Kilford L, Lees AJ (1992) Accuracy of clinical diagnosis of idiopathic Parkinson's disease, a clinico-pathological study of 100 cases. J Neurol Neurosurg Psychiatry 55, 181-184.
32. Moreno F, Indakoetxea B, Barandiaran M, Alzualde A, Gabilondo A, Estanga A, Ruiz J, Ruibal M, Bergareche A, Martý-Masso JF, Lopez de Munain A (2009) 'Frontotemporoparietal' dementia, clinical phenotype associated with the c.709-1G>A PGRN mutation. Neurology 73, 1367-1374.
33. Lopez de Munain A, Alzualde A, Gorostidi A, Otaegui D, Ruiz-Martinez J, Indakoetxea B, Ferrer I, Perez-Dur J, Saenz A, Bergareche A, Barandiaran M, Poza JJ, Zabalza R, Ruiz I, Urtasun M, Fernandez-Manchola I, Olasagasti B, Espinal JB, Olaskoaga J, Ruibal M, Moreno F, Carrera N, Marti Masso JF (2008) Mutations in progranulin gene, clinical, pathological, and ribonucleic acid expression findings. Biol Psychiatry 63, 946-952.
34. Barrett JC, Fry B, Maller J, Daly MJ (2005) Haploview, analysis and visualization of LD and haplotype maps. Bioinformatics 21, 263-265.
35. Zollner S, Pritchard JK (2007) Overcoming the winner's curse, estimating penetrance parameters from case-control data. Am J Hum Genet 80, 605-615.
36. Krstic D, Knuesel I (2013) Deciphering the mechanism underlying late-onset Alzheimer disease. Nat Rev Neurol 9, 25-34.
37. Samaranch L, Cervantes S, Barabash A, Alonso A, Cabranes JA, Lamet I, Ancin I, Lorenzo E, Martinez-Lage P, Marcos A, Clarimon J, Alcolea D, Lleo A, Blesa R, Gomez-Isla T, Pastor P (2010) The effect of MAPT H1 and APOE-4 on transition from mild cognitive impairment to dementia. J Alzheimers Dis 22, 1065-1071.
38. Allen M, Kachadoorian M, Quicksall Z, Zou F, Chai HS, Younkin C, Crook JE, Pankratz VS, Carrasquillo MM, Krishnan S, Nguyen T, Ma L, Malphrus K, Lincoln S, Bisceglio G, Kolbert CP, Jen J, Mukherjee S, Kauwe JK, Crane PK, Haines JL, Mayeux R, Pericak-Vance MA, Farrer LA, Schellenberg GD, Parisi JE, Petersen RC, Graff-Radford NR, Dickson DW, Younkin SG, Ertekin-Daner N (2014) Association of MAPT haplotypes with Alzheimer's disease risk and MAPT brain gene expression levels. Alzheimers Res Ther 6, 39.
39. Pastor P (2013) Comment, double mutants of frontotemporal dementia genes-Simple co-occurrence? Neurology 81, 1338.