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Cited by 297Alzheimer's disease research and treatmentsDementia and Cognitive Impairment ResearchGenetic Associations and Epidemiology

A novel Alzheimer disease locus located near the gene encoding tau protein

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Jun, G, Ibrahim-Verbaas, C A, Vronskaya, M, Lambert, J-C, Chung, J, Naj, A C, Kunkle, B W, Wang, L-S +422 more·2016·Molecular Psychiatry
DOI 10.1038/mp.2015.23PMC PMC4573764
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Abstract

APOE ɛ4, the most significant genetic risk factor for Alzheimer disease (AD), may mask effects of other loci. We re-analyzed genome-wide association study (GWAS) data from the International Genomics of Alzheimer's Project (IGAP) Consortium in APOE ɛ4+ (10 352 cases and 9207 controls) and APOE ɛ4- (7184 cases and 26 968 controls) subgroups as well as in the total sample testing for interaction between a single-nucleotide polymorphism (SNP) and APOE ɛ4 status. Suggestive associations (P<1 × 10(-4)) in stage 1 were evaluated in an independent sample (stage 2) containing 4203 subjects (APOE ɛ4+: 1250 cases and 536 controls; APOE ɛ4-: 718 cases and 1699 controls). Among APOE ɛ4- subjects, novel genome-wide significant (GWS) association was observed with 17 SNPs (all between KANSL1 and LRRC37A on chromosome 17 near MAPT) in a meta-analysis of the stage 1 and stage 2 data sets (best SNP, rs2732703, P=5·8 × 10(-9)). Conditional analysis revealed that rs2732703 accounted for association signals in the entire 100-kilobase region that includes MAPT. Except for previously identified AD loci showing stronger association in APOE ɛ4+ subjects (CR1 and CLU) or APOE ɛ4- subjects (MS4A6A/MS4A4A/MS4A6E), no other SNPs were significantly associated with AD in a specific APOE genotype subgroup. In addition, the finding in the stage 1 sample that AD risk is significantly influenced by the interaction of APOE with rs1595014 in TMEM106B (P=1·6 × 10(-7)) is noteworthy, because TMEM106B variants have previously been associated with risk of frontotemporal dementia. Expression quantitative trait locus analysis revealed that rs113986870, one of the GWS SNPs near rs2732703, is significantly associated with four KANSL1 probes that target transcription of the first translated exon and an untranslated exon in hippocampus (P ⩽ 1.3 × 10(-8)), frontal cortex (P ⩽ 1.3 × 10(-9)) and temporal cortex (P⩽1.2 × 10(-11)). Rs113986870 is also strongly associated with a MAPT probe that targets transcription of alternatively spliced exon 3 in frontal cortex (P=9.2 × 10(-6)) and temporal cortex (P=2.6 × 10(-6)). Our APOE-stratified GWAS is the first to show GWS association for AD with SNPs in the chromosome 17q21.31 region. Replication of this finding in independent samples is needed to verify that SNPs in this region have significantly stronger effects on AD risk in persons lacking APOE ɛ4 compared with persons carrying this allele, and if this is found to hold, further examination of this region and studies aimed at deciphering the mechanism(s) are warranted.

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  • When examining variants at the APOE locus, APOE-stratified analyses may provide better statistical power than standard APOE-adjusted models.

    “Recent work has suggested that when examining variants at the APOE locus, APOE-stratified analyses may provide better statistical power than standard APOE-adjusted models.26”

    From Association of African Ancestry–Specific <i>APOE</i> Missense Variant R145C With Risk of Alzheimer Disease (2023) · cites this paper as [26]

    The Discussion (page unavailable) says APOE-stratified analysis revealed an association at the chromosome 17q21.31/MAPT region that was not genome-wide significant without stratification. This supports the possibility that stratification can reveal otherwise obscured associations, but the paper does not establish greater statistical power for variants at the APOE locus or compare stratified analyses with standard APOE-adjusted models. (LLM, conf=0.84)

    Experimental — accuracy not yet measured

  • More than 30 loci of interest have been identified as associated with AD risk since the 2009 GWAS papers.

    “since the seminal GWAS papers published in 2009 [47, 83], more than 30 loci of interest have been identified to be associated with AD risk (Suppl. Table) [50, 59, 67, 76, 84, 97, 116, 120].”

    From The new genetic landscape of Alzheimer’s disease: from amyloid cascade to genetically driven synaptic failure hypothesis? (2019) · cites this paper as [67]

    The Results report a newly identified genome-wide significant AD risk locus near MAPT, so this paper supports one example among the cited discoveries. It does not state that more than 30 loci had been identified since the 2009 GWAS papers; the count is not supported by this source alone. (LLM, conf=0.84)

    Experimental — accuracy not yet measured

  • The study defined 39 signals in 33 loci already known to be associated with the risk of developing Alzheimer's disease and related dementias.

    “this approach enabled us to define 39 signals in 33 loci already known to be associated with the risk of developing ADD3,5–10”

    From New insights into the genetic etiology of Alzheimer’s disease and related dementias (2022) · cites this paper as [10]

  • Among APOEε4− subjects, several novel associations between Alzheimer's disease risk and SNPs near the MAPT locus were identified.

    “Among APOEε4− subjects, several novel associations between AD risk and SNPs near the MAPT locus were identified.”

    From Genetic architecture of Alzheimer's disease (2020) · cites this paper as [107]

  • Dysfunction of the Chd8 complex has been associated with autism, and H4K16 acetylation by this complex is associated with brain aging.

    “Dysfunction of this complex has been associated with autism33, and H4K16 acetylation by this complex is associated with brain aging34.”

    From Cell type-specific transcriptional programs in mouse prefrontal cortex during adolescence and addiction (2019) · cites this paper as [34]

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Research works printed but not linked: 1

  1. [31]Trabzuni D Wray S Vandrovcova J MAPT expression and splicing is differentially regulated by brain region: relation to genotype and implication for tauopathies Hum Mol Genet 2012 21 4094 4103 22723018 PMC3428157

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Jun, G., Ibrahim-Verbaas, C. A., Vronskaya, M., Lambert, J.-C., Chung, J., Naj, A. C., Kunkle, B. W., Wang, L.-S., Bis, J. C., Bellenguez, C., Harold, D., Lunetta, K. L., Destefano, A. L., Grenier-Boley, B., Sims, R., Beecham, G. W., Smith, A. V., Chouraki, V, Hamilton-Nelson, K. L., Ikram, M. A., Fievet, N., Denning, N., Martin, E. R., Schmidt, H., Kamatani, Y., Dunstan, M. L., Valladares, O., Laza, A. R., Zelenika, D., Ramirez, A., Foroud, T. M., Choi, S.-H., Boland, A., Becker, T., Kukull, W. A., van der Lee, S. J., Pasquier, F., Cruchaga, C., Beekly, D., Fitzpatrick, A. L., Hanon, O., Gill, M., Barber, R., Gudnason, V, Campion, D., Love, S., Bennett, D. A., Amin, N., Berr, C., Tsolaki, M., Buxbaum, J. D., Lopez, O. L., Deramecourt, V, Fox, N. C., Cantwell, L. B., Tárraga, L., Dufouil, C., Hardy, J., Crane, P. K., Eiriksdottir, G., Hannequin, D., Clarke, R., Evans, D., Mosley, T. H., Letenneur, L., Brayne, C., Maier, W., De Jager, P., Emilsson, V, Dartigues, J.-F., Hampel, H., Kamboh, M. I., de Bruijn, R. F. A. G., Tzourio, C., Pastor, P., Larson, E. B., Rotter, J. I., O'Donovan, M. C., Montine, T. J., Nalls, M. A., Mead, S., Reiman, E. M., Jonsson, P. V., Holmes, C., St George-Hyslop, P. H., Boada, M., Passmore, P., Wendland, J. R., Schmidt, R., Morgan, K., Winslow, A. R., Powell, J. F., Carasquillo, M., Younkin, S. G., Jakobsdóttir, J., Kauwe, J. S. K., Wilhelmsen, K. C., Rujescu, D., Nöthen, M. M., Hofman, A., Jones, L., IGAP Consortium, Adams, P. M., Albert, M. S., Albin, R. L., Apostolova, L. G., Arnold, S. E., Asthana, S., Atwood, C. S., Baldwin, C. T., Barmada, M. M., Barnes, L. L., Beach, T. G., Becker, J. T., Bigio, E. H., Bird, T. D., Blacker, D., Boeve, B. F., Bowen, J. D., Boxer, A., Burke, J. R., Cairns, N. J., Cao, C., Carlson, C. S., Carlsson, C. M., Carney, R. M., Carrasquillo, M. M., Carroll, S. L., Chui, H. C., Clark, D. G., Corneveaux, J., Cribbs, D. H., Crocco, E. A., Cruchaga, C., De Jager, P. L., DeCarli, C., DeKosky, S. T., Demirci, F. Y., Dick, M., Dickson, D. W., Doody, R. S., Duara, R., Ertekin-Taner, N., Faber, K. M., Fairchild, T. J., Fallon, K. B., Farlow, M. R., Ferris, S., Frosch, M. P., Galasko, D. R., Gearing, M., Geschwind, D. H., Ghetti, B., Gilbert, J. R., Glass, J. D., Graff-Radford, N. R., Green, R. C., Growdon, J. H., Hakonarson, H., Hamilton, R. L., Hardy, J., Harrell, L. E., Head, E., Honig, L. S., Huebinger, R. M., Huentelman, M. J., Hulette, C. M., Hyman, B. T., Jarvik, G. P., Jicha, G. A., Jin, L.-W., Karydas, A., Kauwe, J. S., Kaye, J. A., Kim, R., Koo, E. H., Kowall, N. W., Kramer, J. H., LaFerla, F. M., Lah, J. J., Leverenz, J. B., Levey, A. I., Li, G., Lieberman, A. P., Lin, C.-F., Lopez, O. L., Lyketsos, C. G., Mack, W. J., Marson, D. C., Martiniuk, F., Mash, D. C., Masliah, E., McCormick, W. C., McCurry, S. M., McDavid, A. N., McKee, A. C., Mesulam, M., Miller, B. L., Miller, C. A., Miller, J. W., Morris, J. C., Mukherjee, S., Murrell, J. R., Myers, A. J., O'Bryant, S., Olichney, J. M., Pankratz, V. S., Parisi, J. E., Partch, A., Paulson, H. L., Perry, W., Peskind, E., Petersen, R. C., Pierce, A., Poon, W. W., Potter, H., Quinn, J. F., Raj, A., Raskind, M., Reisberg, B., Reisch, J. S., Reitz, C., Ringman, J. M., Roberson, E. D., Rogaeva, E., Rosen, H. J., Rosenberg, R. N., Royall, D. R., Sager, M. A., Sano, M., Saykin, A. J., Schneider, J. A., Schneider, L. S., Seeley, W. W., Smith, A. G., Sonnen, J. A., Spina, S., Stern, R. A., Tanzi, R. E., Thornton-Wells, T. A., Trojanowski, J. Q., Troncoso, J. C., Tsuang, D. W., Van Deerlin, V. M., Van Eldik, L. J., Vardarajan, B. N., Vinters, H. V., Vonsattel, J. P., Weintraub, S., Welsh-Bohmer, K. A., Williamson, J., Wishnek, S., Woltjer, R. L., Wright, C. B., Wu, C.-K., Yu, C.-E., Yu, L., Au, R., Wolf, P. A., Beiser, A., Satizabal, C., Uitterlinden, A. G., Rivadeneira, F., Koudstaal, P. J., Longstreth Jr, W. T., Becker, J. T., Kuller, L. H., Lumley, T., Rice, K., Harris, T. B., Nalls, M., Marksteiner, J. J. M., Dal-Bianco, P., Töglhofer, A. M., Freudenberger, P., Ransmayr, G., Benke, T., Toeglhofer, A. M., Boerwinkle, E., Bressler, J., Fornage, M., Morón, F. J., Hernández, I., Roca, M. R., Mauleón, A., Alegret, M., Ramírez-Lorca, R., González-Perez, A., Alpérovitch, A., Alvarez, V., Barberger-Gateau, P., Bettens, K., Bossù, P., Brice, A., Bullido, M., Caffara, P., Clarimon, J., Combarros, O., Coto, E., Zampo, M. D., Delepine, M., Deniz Naranjo, M. C., Epelbaum, J., Fratiglioni, L., Galimberti, D., Graff, C., Hiltunen, M., Ingelsson, M., Keller, L., Lannfelt, L., Llèo, A., Mancuso, M., Mateo, I., Mecocci, P., Nacmias, B., Panza, F., Pilotto, A., Garcia, F. S., Scarpini, E., Seripa, D., Sleegers, K., Soininen, H., Sorbi, S., Spalletta, G., Wallon, D., Thomas, C., Gerrish, A., Chapman, J., Stretton, A., Morgan, A., Oldham, H., Owen, M. J., Kehoe, P. G., Medway, C., Brown, K., Lord, J., Turton, J., Hooper, N. M., Vardy, E., Warren, J. D., Schott, J. M., Uphill, J., Hollingworth, P., Psy, D., Ryan, N., Rossor, M., Collinge, J., Ben-Shlomo, Y., Makrina, D., Gkatzima, O., Lupton, M., Koutroumani, M., Avramidou, D., Germanou, A., Jessen, F., Riedel-Heller, S., Dichgans, M., Heun, R., Kölsch, H., Schürmann, B., Herold, C., Lacour, A., Drichel, D., Hoffmann, P., Kornhuber, J., Gu, W., Feulner, T., Mayhaus, M., Pichler, S., Riemenschneider, M., Bussche, H. V. D., Lawlor, B., Lynch, A., Mann, D., Smith, A. D., Warden, D., Wilcock, G., Heuser, I., Wiltfang, J., Frölich, L., Hüll, M., Mayo, K., Livingston, G., Bass, N. J., Gurling, H., McQuillin, A., Gwilliam, R., Deloukas, P., Al-Chalabi, A., Shaw, C. E., Singleton, A. B., Guerreiro, R., Russo, G., Jöckel, K.-H., Moebus, S., Klopp, N., Wichmann, H.-E., Dickson, D. W., Graff-Radford, N. R., Ma, L., Bisceglio, G., Fisher, E., Warner, N., Pickering-Brown, S., Craig, D., Johnston, J. A., McGuinness, B., Todd, S., Rubinsztein, D. C., Lovestone, S., Bayer, A., Gallacher, J., Proitsi, P., Ortega-Cubero, S., Haines, J. L., Psaty, B. M., Van Broeckhoven, C., Holmans, P., Launer, L. J., Mayeux, R., Lathrop, M., Goate, A. M., Escott-Price, V, Seshadri, S., Pericak-Vance, M. A., Amouyel, P., Williams, J., van Duijn, C. M., Schellenberg, G. D., & Farrer, L. A.
Affiliations
  • Boston University (US)
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Corresponding author
Farrer, L A
ORCID
Venue
Molecular Psychiatry
Publisher
Springer Science and Business Media LLC
Published
2015-03-17
Volume
21
Issue
1
Pages
108-117
ISSN
  • 1359-4184 (ISSN-L)
  • 1476-5578
DOI
10.1038/mp.2015.23
PMC
PMC4573764
OpenAlex
W2028546773
Cited by
297
References
47
Citations by year
2026: 14 · 2025: 28 · 2024: 22 · 2023: 17 · 2022: 25 · 2021: 42 · 2020: 37 · 2019: 27 · 2018: 26 · 2017: 25 · 2016: 22 · 2015: 11 · 2012: 1
FWCI
20.63
Type
journal article
Language
en
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  • Howard Hughes Medical Institute
  • U.S. Department of Veterans Affairs (UL1TR000124, U01 AG024904)
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  • Instituto de Salud Carlos III
  • Bijzonder Onderzoeksfonds UGent
  • National Institute on Aging (U01-AG-024904, N01-HC-55021, N01HC85081, R01AG017917, AG-028383, P01AG010491, P50 AG016575, AG 016976, AG05 128, P30AG010129, P30AG010133, R01AG019085, AG-16495, N01HC85079, N01-HC-85080, P30 AG 08051, U01‐AG10483, R01AG33193, P50 AG016576, R01AG030146, R01-AG-16495, N01-HC-85082, AG021547, U01AG049505, R01 AG30146, AG036535, AG03991, AG010491, R01‐AG17917, N01-AG12100, AG-010124, U24 AG026390, P30AG028383, R01 AG15819, N01-AG012100, P30AG012300, R01AG041718, AG-005133, AG 025688, AG-005136, P50AG016577, N02-HL-6-4278, P50AG005133, R01-AG027944, N01HC55222, AG 024904, AG 030,514, AG-034504, N01-HC-25195, HHSN268200800007C, P30AG028377, U01AG006781, R01AG031287, U01AG016976, P50AG005131, R01-AG019757, R01AG034504, R37-AG015473, P50AG005138, R01AG026390, AG041718, RF1AG015473, AG031287, R01AG048927, P50AG016570, K01AG030514, AG-005142, R01AG020098, AG036528, P50AG005128, P30AG010124, P50AG016573, R01-AG-15928, AG019757, R01AG021547, R01AG041232, R01AG030653, U01AG010483, R01 AG20098, R01AG015819, P30AG008017, N01-HC-85083, AG08122, P30AG010161, R01AG054076, AG019085, U01AG032984, N01-HC-55018, AG033193, RF1AG054023, R01AG033040, R01AG031581, P30AG008051, R01AG041797, P50AG016582, P50AG008702, R01AG016495, AG 033040, AG023501, AG032984, P50AG005681, P50AG005142, P50AG008671, P30AG019610, R01AG026916, P50AG005146, P01 AG0 3991, P01AG003991, AG019724, N01-HC-55015, U24AG026395, U01AG046139, P30AG013846, P50AG005136, RF1AG055477, P50AG005134, RC2AG036535, N01‐HC‐85086, R01AG023629, N01-HC-55019, N01-HC-55020, P30AG013854, R01AG025259, P50AG025688, N01-HC-55016, R01AG017173, RC2AG036528, R01AG033193, P01AG002219, RF1AG015819, AG021886, R01AG015928, P30 AG-10133, AG005681, R01AG027058, R01AG008122, HHSN268201200036C, U24AG056270, P01AG019724, U24AG041689, U24AG021886, P50AG023501, AG027944, R01AG020688, AG 030653, N01-HC-55022, P50AG016574, UO1-AG06781)
  • National Heart, Lung, and Blood Institute (N01-HC-85081, DK-063491, N01-HC55022, N01 HC085086, HC-55016, N01HC-85083, N01 HC055016, N01-HC-55018, HC25195, N01 HC 55020, N01 HC085079, R01-HL120393, N01 HC085083, N01‐HC25195, HC-55021, R01AG20098, HC-55018, N01 HC 55019, N01HC85082, AG08122, N01 HC85086, N01 HC085080, R01HL087652, R01HL103612, HC-55022, HHSN 268200800007C, N01 HC055020, N01HC85080, AG031287, HC-55019, N01-HC, N02- HL-64278, N01 HC055018, R01AG15928, N01 HC55222, HL-093029, HC-55015, HL 103010, HHSN268200625226C, HC-55020, N01-HC-025195, UC2HL103010, ­N01-HC55016, R01HL087641, N01 HC055022, HHSN268201200036C, K24HL038444, HL102419, R01HL093029, N01HC085082, R01HL105756, U01HL080295, N01 HC055019, N01 HC055222, AG16495, U01HL096917, HL-096917, AG033040, HL087641, N01 HC085081, AG033193, N01‐HC‐55015, N01-HC55021, N01 HC055021, N01 HC055015, RC2HL102419, N01-HC85079)
  • National Institute of Mental Health (U01 AG024904, MH60451, R01MH080295, HEALTH-F4-2007-201413, P50MH060451)
  • National Human Genome Research Institute (HG004402, U01HG004402, HHSN268200625226C, UO1 HG004610, U01HG004610, U01HG006375)
  • National Eye Institute
  • National Cancer Institute (R01CA129769, U54CA137788, U54CA132378)
  • National Institute on Deafness and Other Communication Disorders
  • National Institute of Diabetes and Digestive and Kidney Diseases (DK063491, P30DK063491)
  • National Institute of Neurological Disorders and Stroke (NS3 9764, R01 NS 17950, R01AG-15928, N01-HC-55019, N01-HC-55018, R01NS080820, N01-HC-55020, N01-HC-55021, R01NS059873, N01-HC-55016, R01AG20098, AG033193, NS17950, HHSN268200800007C, HL096917, N01-HC-85080, N01-HC-85083, N01‐HC‐25195, N01HC85082, N01-HC-55022, U54NS100693, DK063491, N01-HC-85081, N02-HL-6-4278, N01-HC-85086, N01 HC-55222, N01HC85079, HHSN268201200036C, MH60451, NIMH MH60451, P50NS039764, N01-HC-55015, FP7/2007-2013, R01NS017950)
  • National Institute of Environmental Health Sciences (P30ES013508)
  • National Institute of Biomedical Imaging and Bioengineering (U01 AG024904, AG024904)
  • National Center for Research Resources (MO1 RR000-96, UL1RR025005, UL1RR02777, UL1RR029893, M01RR000096)
  • National Center for Advancing Translational Sciences (DK063491)
Topics
  • Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
  • Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Associations and Epidemiology
Keywords
Alzheimer's disease, genetic susceptibility loci, APOE ε4, MAPT, tau protein, KANSL1, TMEM106B, gene-gene interaction, conditional analysis, expression quantitative trait loci, hippocampal gene expression
MeSH terms
Alzheimer Disease, Chromosomes, Human, Pair 17, Humans, tau Proteins, Polymorphism, Single Nucleotide, Apolipoprotein E4, Genome-Wide Association Study

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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

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