Fine-mapping of the human leukocyte antigen locus as a risk factor for Alzheimer disease: A case–control study
Open accessAbstract
BACKGROUND: Alzheimer disease (AD) is a progressive disorder that affects cognitive function. There is increasing support for the role of neuroinflammation and aberrant immune regulation in the pathophysiology of AD. The immunoregulatory human leukocyte antigen (HLA) complex has been linked to susceptibility for a number of neurodegenerative diseases, including AD; however, studies to date have failed to consistently identify a risk HLA haplotype for AD. Contributing to this difficulty are the complex genetic organization of the HLA region, differences in sequencing and allelic imputation methods, and diversity across ethnic populations. METHODS AND FINDINGS: Building on prior work linking the HLA to AD, we used a robust imputation method on two separate case-control cohorts to examine the relationship between HLA haplotypes and AD risk in 309 individuals (191 AD, 118 cognitively normal [CN] controls) from the San Francisco-based University of California, San Francisco (UCSF) Memory and Aging Center (collected between 1999-2015) and 11,381 individuals (5,728 AD, 5,653 CN controls) from the Alzheimer's Disease Genetics Consortium (ADGC), a National Institute on Aging (NIA)-funded national data repository (reflecting samples collected between 1984-2012). We also examined cerebrospinal fluid (CSF) biomarker measures for patients seen between 2005-2007 and longitudinal cognitive data from the Alzheimer's Disease Neuroimaging Initiative (n = 346, mean follow-up 3.15 ± 2.04 y in AD individuals) to assess the clinical relevance of identified risk haplotypes. The strongest association with AD risk occurred with major histocompatibility complex (MHC) haplotype A*03:01~B*07:02~DRB1*15:01~DQA1*01:02~DQB1*06:02 (p = 9.6 x 10-4, odds ratio [OR] [95% confidence interval] = 1.21 [1.08-1.37]) in the combined UCSF + ADGC cohort. Secondary analysis suggested that this effect may be driven primarily by individuals who are negative for the established AD genetic risk factor, apolipoprotein E (APOE) ɛ4. Separate analyses of class I and II haplotypes further supported the role of class I haplotype A*03:01~B*07:02 (p = 0.03, OR = 1.11 [1.01-1.23]) and class II haplotype DRB1*15:01- DQA1*01:02- DQB1*06:02 (DR15) (p = 0.03, OR = 1.08 [1.01-1.15]) as risk factors for AD. We followed up these findings in the clinical dataset representing the spectrum of cognitively normal controls, individuals with mild cognitive impairment, and individuals with AD to assess their relevance to disease. Carrying A*03:01~B*07:02 was associated with higher CSF amyloid levels (p = 0.03, β ± standard error = 47.19 ± 21.78). We also found a dose-dependent association between the DR15 haplotype and greater rates of cognitive decline (greater impairment on the 11-item Alzheimer's Disease Assessment Scale cognitive subscale [ADAS11] over time [p = 0.03, β ± standard error = 0.7 ± 0.3]; worse forgetting score on the Rey Auditory Verbal Learning Test (RAVLT) over time [p = 0.02, β ± standard error = -0.2 ± 0.06]). In a subset of the same cohort, dose of DR15 was also associated with higher baseline levels of chemokine CC-4, a biomarker of inflammation (p = 0.005, β ± standard error = 0.08 ± 0.03). The main study limitations are that the results represent only individuals of European-ancestry and clinically diagnosed individuals, and that our study used imputed genotypes for a subset of HLA genes. CONCLUSIONS: We provide evidence that variation in the HLA locus-including risk haplotype DR15-contributes to AD risk. DR15 has also been associated with multiple sclerosis, and its component alleles have been implicated in Parkinson disease and narcolepsy. Our findings thus raise the possibility that DR15-associated mechanisms may contribute to pan-neuronal disease vulnerability.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Previous analyses in the ADGC have linked both HLA class I and II haplotypes with Alzheimer's disease risk.
“Previous analyses in the ADGC (5,728 Alzheimer’s disease cases and 5,653 controls) have linked both HLA class I and II haplotypes with Alzheimer’s disease risk106.”
From Genetic meta-analysis of diagnosed Alzheimer’s disease identifies new risk loci and implicates Aβ, tau, immunity and lipid processing (2019) · cites this paper as [106]
A specific class II HLA-DR haplotype, DR15, has been suggested to impart risk for both AD and MS.
“Beyond these findings, a specific class II human leukocyte antigen (HLA)-DR haplotype, DR15, has been suggested to impart risk for both AD and MS (7, 8).”
From The Transcriptional Landscape of Microglial Genes in Aging and Neurodegenerative Disease (2019) · cites this paper as [8]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Hirono, N., Mori, E., Ikejiri, Y., Imamura, T., Shimomura, T., Hashimoto, M., Yamashita, H., & Ikeda, M. (1997) · PubMed · Cited by 21,010 · see citing works
Kok, J. S., Berg, I. J., & Scherder, E. J. A. (2013) · Dementia and Geriatric Cognitive Disorders Extra · doi:10.1159/000353441 · Cited by 20,589 · see citing works
The Clinical Dementia Rating (CDR): Current version and scoring rules
Morris, J. C. (1993) · Neurology · doi:10.1212/wnl.43.11.2412-a · Cited by 9,882 · see citing works
A New Clinical Scale for the Staging of Dementia
Hughes, C. P., Berg, L., Danziger, W., Coben, L. A., & Martin, R. L. (1982) · British Journal of Psychiatry · doi:10.1192/bjp.140.6.566 · Cited by 7,056 · see citing works
Meta-Analysis of 74,046 Individuals Identifies 11 New Susceptibility Loci for Alzheimer’s Disease
(EADI), E. A. D. I., Lambert, J.-C., (GERAD), G. A. E. R. I. A. D., Alzheimer's Disease Genetic Consortium (ADGC), (CHARGE), C. F. H. A. A. R. I. G. E., Ibrahim-Verbaas, C. A., Harold, D., Naj, A. C., Sims, R., Bellenguez, C., et al. (2013) · Nature Genetics · doi:10.1038/ng.2802 · Cited by 4,336 · see citing works
Self-citationA new rating scale for Alzheimer's disease
(1984) · American Journal of Psychiatry · doi:10.1176/ajp.141.11.1356 · Cited by 4,175 · see citing works
Complement and microglia mediate early synapse loss in Alzheimer mouse models
Hong, S., Beja-Glasser, V. F., Nfonoyim, B. M., Frouin, A., Li, S., Ramakrishnan, S., Merry, K. M., Shi, Q., Rosenthal, A., Barres, B. A., et al. (2016) · Science · doi:10.1126/science.aad8373 · Cited by 3,343 · see citing works
Advancing research diagnostic criteria for Alzheimer's disease: the IWG-2 criteria
Dubois, B., Feldman, H. H., Jacova, C., Hampel, H., Molinuevo, J. L., Blennow, K., DeKosky, S. T., Gauthier, S., Selkoe, D., Bateman, R., et al. (2014) · The Lancet Neurology · doi:10.1016/s1474-4422(14)70090-0 · Cited by 3,321 · see citing works
<i>TREM2</i> Variants in Alzheimer's Disease
Guerreiro, R., Wojtas, A., Bras, J., Carrasquillo, M., Rogaeva, E., Majounie, E., Cruchaga, C., Sassi, C., Kauwe, J. S. K., Younkin, S., et al. (2013) · New England Journal of Medicine · doi:10.1056/nejmoa1211851 · Cited by 3,020 · see citing works
Self-citationGenetic risk and a primary role for cell-mediated immune mechanisms in multiple sclerosis
The International Multiple Sclerosis Genetics Consortium & The Wellcome Trust Case Control Consortium 2 (2011) · Nature · doi:10.1038/nature10251 · Cited by 2,697 · see citing works
Variant of <i>TREM2</i> Associated with the Risk of Alzheimer's Disease
Jonsson, T., Stefansson, H., Steinberg, S., Jonsdottir, I., Jonsson, P. V., Snaedal, J., Bjornsson, S., Huttenlocher, J., Levey, A. I., Lah, J. J., et al. (2013) · New England Journal of Medicine · doi:10.1056/nejmoa1211103 · Cited by 2,558 · see citing works
Cerebrospinal fluid biomarker signature in Alzheimer's disease neuroimaging initiative subjects
Shaw, L. M., Vanderstichele, H., Knapik‐Czajka, M., Clark, C. M., Aisen, P. S., Petersen, R. C., Blennow, K., Soares, H., Simon, A., Lewczuk, P., et al. (2009) · Annals of Neurology · doi:10.1002/ana.21610 · Cited by 2,065 · see citing works
Naj, A. C., Jun, G., Beecham, G. W., Wang, L.-S., Vardarajan, B. N., Buros, J., Gallins, P. J., Buxbaum, J. D., Jarvik, G. P., Crane, P. K., et al. (2011) · Nature Genetics · doi:10.1038/ng.801 · Cited by 1,901 · see citing works
Self-citationAlzheimer’s Disease Risk Genes and Mechanisms of Disease Pathogenesis
Karch, C. M., & Goate, A. M. (2015) · Biological Psychiatry · doi:10.1016/j.biopsych.2014.05.006 · Cited by 1,357 · see citing works
Nalls, M., Plagnol, V., Hernandez, D., Sharma, M., Sheerin, U., Saad, M., Simón-Sánchez, J., Schulte, C., Lesage, S., Sveinbjörnsdóttir, S., et al. (2011) · The Lancet · doi:10.1016/s0140-6736(10)62345-8 · Cited by 986 · see citing works
Early inflammation and dementia: A 25‐year follow‐up of the Honolulu‐Asia aging study
Schmidt, R., Schmidt, H., Curb, J. D., Masaki, K., White, L. R., & Launer, L. J. (2002) · Annals of Neurology · doi:10.1002/ana.10265 · Cited by 710 · see citing works
Common variants at 7p21 are associated with frontotemporal lobar degeneration with TDP-43 inclusions
Van Deerlin, V. M., Sleiman, P. M. A., Martinez-Lage, M., Chen-Plotkin, A., Wang, L.-S., Graff-Radford, N. R., Dickson, D. W., Rademakers, R., Boeve, B. F., Grossman, M., et al. (2010) · Nature Genetics · doi:10.1038/ng.536 · Cited by 579 · see citing works
Self-citationHigh-resolution HLA alleles and haplotypes in the United States population
Maiers, M. J., Gragert, L. A., & Klitz, W. (2007) · Human Immunology · doi:10.1016/j.humimm.2007.04.005 · Cited by 456 · see citing works
Saykin, A. J., Shen, L., Foroud, T. M., Potkin, S. G., Swaminathan, S., Kim, S., Risacher, S. L., Nho, K., Huentelman, M. J., Craig, D. W., et al. (2010) · Alzheimer's & Dementia · doi:10.1016/j.jalz.2010.03.013 · Cited by 442 · see citing works
HIBAG—HLA genotype imputation with attribute bagging
Zheng, X., Shen, J., Cox, C. J., Wakefield, J. C., Ehm, M. G., Nelson, M. R., & Weir, B. S. (2013) · The Pharmacogenomics Journal · doi:10.1038/tpj.2013.18 · Cited by 425 · see citing works
A Dramatic Increase of C1q Protein in the CNS during Normal Aging
Stephan, A. H., Madison, D. V., Mateos, J. M., Fraser, D. A., Lovelett, E. A., Coutellier, L., Kim, L., Tsai, H.-H., Huang, E. J., Rowitch, D. H., et al. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.1333-13.2013 · Cited by 423 · see citing works
HLA DQB1*0602 is Associated With Cataplexy in 509 Narcoleptic Patients
Mignot, E. J.-M., Hayduk, R., Black, J. E., Grumet, F. C., & Guilleminault, C. (1997) · SLEEP · doi:10.1093/sleep/20.11.1012 · Cited by 394 · see citing works
Complement<i>C3</i>-Deficient Mice Fail to Display Age-Related Hippocampal Decline
Shi, Q., Colodner, K. J., Matousek, S. B., Merry, K., Hong, S., Kenison, J. E., Frost, J. L., Le, K. X., Li, S., Dodart, J.-C., et al. (2015) · The Journal of Neuroscience · doi:10.1523/jneurosci.1698-15.2015 · Cited by 368 · see citing works
Patsopoulos, N. A., Barcellos, L. F., Hintzen, R. Q., Schaefer, C., van Duijn, C. M., Noble, J. A., Raj, T., IMSGC, ANZgene, Gourraud, P.-A., et al. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003926 · Cited by 312 · see citing works
Yu, L., Chibnik, L. B., Srivastava, G. P., Pochet, N., Yang, J., Xu, J., Kozubek, J., Obholzer, N., Leurgans, S. E., Schneider, J. A., et al. (2015) · JAMA Neurology · doi:10.1001/jamaneurol.2014.3049 · Cited by 290 · see citing works
Miretti, M. M., Walsh, E. C., Ke, X., Delgado, M., Griffiths, M. N. D., Hunt, S. E., Morrison, J., Whittaker, P., Lander, E. S., Cardon, L. R., et al. (2005) · The American Journal of Human Genetics · doi:10.1086/429393 · Cited by 258 · see citing works
Hensley, K. (2010) · Journal of Alzheimer s Disease · doi:10.3233/jad-2010-1414 · Cited by 250 · see citing works
Wood, J. A., Wood, P. L., Ryan, R., Graff-Radford, N. R., Pilapil, C., Robitaille, Y., & Quirion, R. (1993) · Brain Research · doi:10.1016/0006-8993(93)91327-o · Cited by 244 · see citing works
Coppola, G., Chinnathambi, S., Lee, J. J., Dombroski, B. A., Baker, M. C., Soto-Ortolaza, A. I., Lee, S. E., Klein, E., Huang, A. Y., Sears, R., et al. (2012) · Human Molecular Genetics · doi:10.1093/hmg/dds161 · Cited by 240 · see citing works
Self-citationHLA-DR15 Haplotype and Multiple Sclerosis: A HuGE Review
Schmidt, H., Williamson, D., & Ashley-Koch, A. (2007) · American Journal of Epidemiology · doi:10.1093/aje/kwk118 · Cited by 212 · see citing works
Multi-Population Classical HLA Type Imputation
Dilthey, A., Leslie, S., Moutsianas, L., Shen, J., Cox, C. J., Nelson, M. R., & McVean, G. (2013) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1002877 · Cited by 207 · see citing works
DQB1 Locus Alone Explains Most of the Risk and Protection in Narcolepsy with Cataplexy in Europe
Behalf of the European Narcolepsy Network (EU-NN), Tafti, M., Hor, H., Dauvilliers, Y. A., Lammers, G. J., Overeem, S., Mayer, G., Javidi, S., Iranzo, Á., Santamaría, J., et al. (2014) · SLEEP · doi:10.5665/sleep.3300 · Cited by 202 · see citing works
Hoffman, L. M., DeWire, M. D., Ryall, S. T., Buczkowicz, P., Leach, J., Miles, L., Ramani, A. K., Brudno, M., Kumar, S. S., Drissi, R., et al. (2016) · Acta Neuropathologica Communications · doi:10.1186/s40478-015-0269-0 · Cited by 196 · see citing works
Alzheimer's Disease Assessment Scale (ADAS).
Mohs, R. C., & Cohen, L. (1988) · PubMed · Cited by 195 · see citing works
Association of Parkinson Disease with Structural and Regulatory Variants in the HLA Region
Wissemann, W. T., Hill-Burns, E. M., Zabetian, C. P., Factor, S. A., Patsopoulos, N., Hoglund, B., Holcomb, C., Donahue, R. J., Thomson, G., Erlich, H., et al. (2013) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2013.10.009 · Cited by 189 · see citing works
APOE effect on Alzheimer's disease biomarkers in older adults with significant memory concern
Risacher, S. L., Kim, S., Nho, K. T., Foroud, T., Shen, L., Petersen, R. C., Jack, C. R., Beckett, L. A., Aisen, P. S. S., Koeppe, R. A., et al. (2015) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2015.03.003 · Cited by 186 · see citing works
Association between genetic traits for immune-mediated diseases and Alzheimer disease
Yokoyama, J. S., Wang, Y., Schork, A. J., Thompson, W. K., Karch, C. M., Cruchaga, C., McEvoy, L. K., Witoelar, A., Chen, C.-H., Holland, D., et al. (2016) · JAMA Neurology · doi:10.1001/jamaneurol.2016.0150 · Cited by 176 · see citing works
Self-citationWes, P. D., Holtman, I. R., Boddeke, E. W. G. M., Möller, T., & Eggen, B. J. L. (2016) · Glia · doi:10.1002/glia.22866 · Cited by 167 · see citing works
TREM2 is associated with the risk of Alzheimer's disease in Spanish population
Benitez, B. A., Cooper, B., Pastor, P., Jin, S.-C., Lorenzo, E., Cervantes, S., & Cruchaga, C. (2013) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2012.12.018 · Cited by 163 · see citing works
Potential Inflammatory biomarkers in Alzheimer's disease
Mrak, R. E., & Griffin, W. S. T. (2006) · Journal of Alzheimer s Disease · doi:10.3233/jad-2005-8406 · Cited by 135 · see citing works
Gan, L., Ye, S., Chu, A., Anton, K., Yi, S.-L., Vincent, V. A. M., von Schack, D., Chin, D. J., Murray, J. C., Lohr, S., et al. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m306183200 · Cited by 128 · see citing works
Farrer, L. A. (1997) · JAMA · doi:10.1001/jama.1997.03550160069041 · Cited by 124 · see citing works
Chabas, D., Taheri, S., Renier, C. M., & Mignot, E. J.-M. (2003) · Annual Review of Genomics and Human Genetics · doi:10.1146/annurev.genom.4.070802.110432 · Cited by 122 · see citing works
HLA-DQ Locus of the Human Leukocyte Antigen Complex and Type 1 Diabetes Mellitus: A HuGE Review
Dorman, J. S., & Bunker, C. H. (2000) · Epidemiologic Reviews · doi:10.1093/oxfordjournals.epirev.a018034 · Cited by 121 · see citing works
Tapiola, T., Pirttilä, T., Mehta, P., Alafuzoff, I., Lehtovirta, M., & Soininen, H. (2000) · Neurobiology of Aging · doi:10.1016/s0197-4580(00)00164-0 · Cited by 111 · see citing works
Eikelenboom, P., Hoozemans, J. J. M., Veerhuis, R., van Exel, E. R., Rozemüller, A. J. M., & van Gool, W. A. (2012) · Alzheimer s Research & Therapy · doi:10.1186/alzrt118 · Cited by 107 · see citing works
Alzheimer's Disease Assessment Scale (ADAS)
本間昭 (2003) · Medical Entomology and Zoology · Cited by 106 · see citing works
Association of HLA Genetic Risk Burden With Disease Phenotypes in Multiple Sclerosis
Isobe, N., Keshavan, A., Gourraud, P., Zhu, A. H., Datta, E., Schlaeger, R., Caillier, S. J., Santaniello, A., Lizée, A., Himmelstein, D. S., et al. (2016) · JAMA Neurology · doi:10.1001/jamaneurol.2016.0980 · Cited by 89 · see citing works
Self-citationPappas, D. J., Marin, W. M., Hollenbach, J. A., & Mack, S. J. (2015) · Human Immunology · doi:10.1016/j.humimm.2015.12.006 · Cited by 85 · see citing works
Self-citationEvidence for association of HLA-A2 allele with onset age of Alzheimer's disease
Payami, H., Schellenberg, G. D., Zareparsi, S., Kaye, J. A., Sexton, G. J., Head, M. A., Matsuyama, S. S., Jarvik, L. F., Miller, B. L., McManus, D. Q., et al. (1997) · Neurology · doi:10.1212/wnl.49.2.512 · Cited by 84 · see citing works
Self-citationKessler, H., Pajonk, F., Meisser, P., Schneider-Axmann, T., Hoffmann, K.-H., Supprian, T., Herrmann, W., Obeid, R., Multhaup, G., Falkai, P., et al. (2006) · Journal of Neural Transmission · doi:10.1007/s00702-006-0485-7 · Cited by 79 · see citing works
The Role of Clusterin in Amyloid-β–Associated Neurodegeneration
Desikan, R. S., Thompson, W. K., Holland, D., Hess, C. P., Brewer, J. B., Zetterberg, H., Blennow, K., Andreassen, O. A., McEvoy, L. K., Hyman, B. T., et al. (2014) · JAMA Neurology · doi:10.1001/jamaneurol.2013.4560 · Cited by 79 · see citing works
Self-citationLate-onset Alzheimer disease risk variants mark brain regulatory loci
Allen, M., Kachadoorian, M., Carrasquillo, M. M., Karhade, A., Manly, L., Burgess, J. D., Wang, C., Serie, D., Wang, X., Siuda, J., et al. (2015) · Neurology Genetics · doi:10.1212/nxg.0000000000000012 · Cited by 73 · see citing works
The relationship between complement factor C3, APOE ε4, amyloid and tau in Alzheimer’s disease
Initiative, A. D. N., Bonham, L. W., Desikan, R. S., & Yokoyama, J. S. (2016) · Acta Neuropathologica Communications · doi:10.1186/s40478-016-0339-y · Cited by 70 · see citing works
Self-citationZetzsche, T., Rujescu, D., Hardy, J., & Hampel, H. J. (2010) · Expert Review of Molecular Diagnostics · doi:10.1586/erm.10.48 · Cited by 61 · see citing works
Rare TREM2 variants associated with Alzheimer’s disease display reduced cell surface expression
Sirkis, D. W., Bonham, L. W., Aparicio, R. E., Geier, E. G., Ramos, E. M., Wang, Q., Karydas, A., Miller, Z. A., Miller, B. L., Coppola, G., et al. (2016) · Acta Neuropathologica Communications · doi:10.1186/s40478-016-0367-7 · Cited by 61 · see citing works
Self-citationHeart fatty acid binding protein and Aβ-associated Alzheimer’s neurodegeneration
Desikan, R. S., Thompson, W. K., Holland, D., Hess, C. P., Brewer, J. B., Zetterberg, H., Blennow, K., Andreassen, O. A., McEvoy, L. K., Hyman, B. T., et al. (2013) · Molecular Neurodegeneration · doi:10.1186/1750-1326-8-39 · Cited by 58 · see citing works
Self-citationKhor, S., Yang, W., Kawashima, M., Kamitsuji, S., Zheng, X., Nishida, N., Sawai, H., Toyoda, H., Miyagawa, T., Honda, M., et al. (2015) · The Pharmacogenomics Journal · doi:10.1038/tpj.2015.4 · Cited by 55 · see citing works
Murcia, J. D. G., Schmutz, C., Munger, C., Perkes, A. D., Gustin, A. J., Peterson, M., Ebbert, M., Norton, M. C., Tschanz, J. T., Munger, R. G., et al. (2013) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2013.06.004 · Cited by 54 · see citing works
Self-citationAlzheimer disease: evidence for susceptibility loci on chromosomes 6 and 14.
WEITKAMP, L. R., Nee, L. E., Keats, B. J. B., Polinsky, R. J., & Guttormsen, S. A. (1983) · PubMed · Cited by 51 · see citing works
Analytical Methods for Disease Association Studies with Immunogenetic Data
Hollenbach, J. A., Mack, S. J., Thomson, G. J., & Gourraud, P. (2012) · Methods in molecular biology · doi:10.1007/978-1-61779-842-9_14 · Cited by 36 · see citing works
Self-citationPayami, H., Kaye, J. A., Becker, W. C., Norman, D. J., & Wetzsteon, P. J. (1991) · Neurology · doi:10.1212/wnl.41.10.1544 · Cited by 34 · see citing works
Does Narcolepsy Symptom Severity Vary According to HLA-DQB1*0602 Allele Status?
Watson, N. F., Ton, T. G. N., Koepsell, T. D., Gersuk, V. H., & Longstreth, W. T. (2010) · SLEEP · doi:10.1093/sleep/33.1.29 · Cited by 31 · see citing works
Association of HLA-DR/DQ Polymorphism With Alzheimer’s Disease
Mansouri, L., Klai, S., Gritli, N., Fekih‐Mrissa, N., Messelmani, M., Bedoui, I., Derbali, H., & Mrissa, R. (2015) · The American Journal of the Medical Sciences · doi:10.1097/maj.0000000000000416 · Cited by 31 · see citing works
Association Between the HLA-A2 Allele and Alzheimer Disease
Listı̀, F., Candore, G., Balistreri, C. R., Grimaldi, M. P., Orlando, V., Vasto, S., Colonna‐Romano, G., Lio, D., Licastro, F., Franceschi, C., et al. (2006) · Rejuvenation Research · doi:10.1089/rej.2006.9.99 · Cited by 30 · see citing works
The Relationship of HLA Class I and II Alleles and Haplotypes with Autism: A Case Control Study
Alhakbany, M. A., Awadallah, S., & AL-Ayadhi, L. Y. (2014) · Autism Research and Treatment · doi:10.1155/2014/242048 · Cited by 30 · see citing works
Risk for Alzheimer's disease in older late-onset cases is associated with HLA-DRB1*03
Neill, D., Curran, M. D., Middleton, D., Mawhinney, H., Edwardson, J. A., McKeith, I. G., Ballard, C. G., Morris, C. M., Ince, P. G., Jaros, E., et al. (1999) · Neuroscience Letters · doi:10.1016/s0304-3940(99)00761-2 · Cited by 28 · see citing works
Association between HLA-A Alleles and Alzheimer’s Disease in a Southern Chinese Community
Ma, S. L., Tang, N. L. S., Tam, C. W. C., Lui, V. W.-C., Suen, E., Chiu, H. F. K., & LAM, L. C. W. (2008) · Dementia and Geriatric Cognitive Disorders · doi:10.1159/000164275 · Cited by 27 · see citing works
HLA class I, II & III genes in confirmed late-onset Alzheimer's disease
Lehmann, D. J. (2001) · Neurobiology of Aging · doi:10.1016/s0197-4580(00)00180-9 · Cited by 27 · see citing works
HLA-A2 homozygosity but not heterozygosity is associated with Alzheimer disease
Zareparsi, S., James, D., Kaye, J. A., Bird, T. D., Schellenberg, G. D., & Payami, H. (2002) · Neurology · doi:10.1212/wnl.58.6.973 · Cited by 26 · see citing works
Harris, J. M., Cumming, A., Craddock, N. J., Clair, D. S., & Lendon, C. L. (2000) · Neuroscience Letters · doi:10.1016/s0304-3940(00)01539-1 · Cited by 24 · see citing works
HLA-A*01 is Associated with Late Onset of Alzheimer's Disease in Italian Patients
Guerini, F. R., Tinelli, C., Calabrese, E., Agliardi, C., Zanzottera, M., SILVESTRI, A. D., Franceschi, M., Grimaldi, L. M. E., Nemni, R., & Clerici, M. (2009) · International Journal of Immunopathology and Pharmacology · doi:10.1177/039463200902200414 · Cited by 23 · see citing works
No association of the HLA-A2 allele with Alzheimer's disease
Goumidi, L., Lambert, J., Cottel, D., Amouyel, P., & Chartier‐Harlin, M. (2002) · Neuroscience Letters · doi:10.1016/s0304-3940(02)01057-1 · Cited by 23 · see citing works
No association between the HLA-A2 allele and Alzheimer disease
Small, G. W., Scott, W. K., Komo, S., Yamaoka, L. H., Farrer, L. A., Auerbach, S. H., Saunders, A. M., Roses, A. D., Haines, J. L., & Pericak‐Vance, M. A. (1999) · Neurogenetics · doi:10.1007/s100480050080 · Cited by 21 · see citing works
Combarros, O., Escribano, J., Sánchez‐Velasco, P., Leyva‐Cobián, F., Oterino, A., Leno, C., & Berciano, J. (2009) · Acta Neurologica Scandinavica · doi:10.1111/j.1600-0404.1998.tb01735.x · Cited by 21 · see citing works
Frequency of HLA-A and B alleles in early and late-onset Alzheimer's disease
Middleton, D., Mawhinney, H., Curran, M. D., Edwardson, J. A., Perry, R., McKeith, I. G., Morris, C. M., Ince, P. G., & Neill, D. (1999) · Neuroscience Letters · doi:10.1016/s0304-3940(99)00045-2 · Cited by 20 · see citing works
Variable association of HLA-A2 in men with early-onset Alzheimer disease☆
Small, G. W., Ebeling, S. B., Matsuyama, S. S., Heyman, A., Reisner, E. G., Renvoize, E. B., & Sulkava, R. O. (1991) · Neurobiology of Aging · doi:10.1016/0197-4580(91)90026-g · Cited by 12 · see citing works
Hsieh, A., Chang, S., Chen, P., Chu, C., Hsiao, C., Yang, W., Chang, C.-C., Wu, J., Chen, Y.-T., Chang, T., et al. (2014) · BMC Genomics · doi:10.1186/1471-2164-15-81 · Cited by 11 · see citing works
Association study of the HLA-A2 allele in Italian Alzheimer disease patients
Guerini, F. R., Calabrese, E., Agliardi, C., Zanzottera, M., Franceschi, M., Grimaldi, L. M. E., Nemni, R., & Ferrante, P. (2008) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2008.02.001 · Cited by 6 · see citing works
Human leucocyte antigen (HLA) class I and II typing in Belgian multiple sclerosis patients
Lysandropoulos, A. P., Racapé, J., Holovská, V., & Toungouz, M. (2016) · Acta Neurologica Belgica · doi:10.1007/s13760-016-0716-0 · Cited by 4 · see citing works
Price (1999) · doi:10.1002/1531-8249(199903)45:3
Flagged first, then by citations
1 of the 82 references couldn’t be matched to a known paper.
Research works printed but not linked: 1
- [63]Yokoyama JS, Wang Y, Schork AJ, Thompson WK, Karch CM, Cruchaga C, et al Association between genetic traits for immune-mediated diseases and Alzheimer disease. JAMA Neurol. 2016; 73. PMC4905783 27088644
Cited by
Sorted by citations
Alzheimer Disease Genetics Consortium (ADGC), Kunkle, B. W., The European Alzheimer’s Disease Initiative (EADI), Cohorts for Heart and Aging Research in Genomic Epidemiology Consortium (CHARGE), Genetic and Environmental Risk in AD/Defining Genetic, P. A. E. R. F. A. D. C. (., Grenier-Boley, B., Sims, R., Bis, J. C., Damotte, V., Naj, A. C., et al. (2019) · Nature Genetics · doi:10.1038/s41588-019-0358-2 · Cited by 2,946 · see citing works
Self-citationB cells in autoimmune and neurodegenerative central nervous system diseases
Sabatino, J. J., Pröbstel, A., & Zamvil, S. S. (2019) · Nature reviews. Neuroscience · doi:10.1038/s41583-019-0233-2 · Cited by 347 · see citing works
You, Y., Muraoka, S., Jedrychowski, M. P., Hu, J., McQuade, A., Young‐Pearse, T. L., Aslebagh, R., Shaffer, S. A., Gygi, S. P., Blurton-Jones, M. M., et al. (2022) · Journal of Extracellular Vesicles · doi:10.1002/jev2.12183 · Cited by 161 · see citing works
Dissecting the genetic relationship between cardiovascular risk factors and Alzheimer’s disease
Broce, I. J., Tan, C. H., Fan, C. C., Jansen, I., Savage, J. E., Witoelar, A., Wen, N., Hess, C. P., Dillon, W. P., Glastonbury, C. M., et al. (2019) · Acta Neuropathologica · doi:10.1007/s00401-018-1928-6 · Cited by 140 · see citing works
Self-citationThe role of innate immunity in Alzheimer's disease
Ennerfelt, H. E., & Lukens, J. R. (2020) · Immunological Reviews · doi:10.1111/imr.12896 · Cited by 121 · see citing works
Polygenic hazard score: an enrichment marker for Alzheimer’s associated amyloid and tau deposition
Initiative, A. D. N., Tan, C. H., Fan, C. C., Mormino, E. C., Sugrue, L. P., Broce, I., Hess, C. P., Dillon, W. P., Bonham, L. W., Yokoyama, J. S., et al. (2017) · Acta Neuropathologica · doi:10.1007/s00401-017-1789-4 · Cited by 95 · see citing works
Self-citationDementia and aging populations—A global priority for contextualized research and health policy
Brayne, C., & Miller, B. L. (2017) · PLoS Medicine · doi:10.1371/journal.pmed.1002275 · Cited by 89 · see citing works
Self-citationThe Transcriptional Landscape of Microglial Genes in Aging and Neurodegenerative Disease
Bonham, L. W., Sirkis, D. W., & Yokoyama, J. S. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.01170 · Cited by 83 · see citing works
Self-citationTau at the interface between neurodegeneration and neuroinflammation
Didonna, A. (2020) · Genes & Immunity · doi:10.1038/s41435-020-00113-5 · Cited by 82 · see citing works
Multi-ancestry meta-analysis and fine-mapping in Alzheimer’s disease
Lake, J., Solsberg, C. W., Kim, J. J., Acosta‐Uribe, J., Makarious, M. B., Li, Z., Levine, K. S., Heutink, P., Alvarado, C. X., Vitale, D., et al. (2023) · Molecular Psychiatry · doi:10.1038/s41380-023-02089-w · Cited by 81 · see citing works
Self-citationGermline risk of clonal haematopoiesis
Silver, A. J., Bick, A. G., & Savona, M. R. (2021) · Nature Reviews Genetics · doi:10.1038/s41576-021-00356-6 · Cited by 80 · see citing works
The immunogenetics of neurological disease
Misra, M. K., Damotte, V., & Hollenbach, J. A. (2018) · Immunology · doi:10.1111/imm.12869 · Cited by 74 · see citing works
Self-citationSun, Y., Zhu, J., Zhou, D., Canchi, S., Wu, C., Cox, N. J., Rissman, R. A., Gamazon, E. R., & Wu, L. (2021) · Genome Medicine · doi:10.1186/s13073-021-00959-y · Cited by 69 · see citing works
T Cells: A Growing Universe of Roles in Neurodegenerative Diseases
Dressman, D., & Elyaman, W. (2021) · The Neuroscientist · doi:10.1177/10738584211024907 · Cited by 56 · see citing works
Guen, Y. L., Luo, G., Ambati, A., Damotte, V., Jansen, I. E., Yu, E., Nicolas, A., de Rojas, I., Leal, T. P., Miyashita, A., et al. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2302720120 · Cited by 56 · see citing works
Self-citationThe aging immune system in Alzheimer’s and Parkinson’s diseases
Heavener, K. S., & Bradshaw, E. M. (2022) · Seminars in Immunopathology · doi:10.1007/s00281-022-00944-6 · Cited by 50 · see citing works
Patel, D., Zhang, X., Farrell, J. J., Chung, J., Stein, T. D., Lunetta, K. L., & Farrer, L. A. (2021) · Translational Psychiatry · doi:10.1038/s41398-021-01373-z · Cited by 49 · see citing works
HLA in Alzheimer’s Disease: Genetic Association and Possible Pathogenic Roles
Wang, Z., Wan, Q., & Xing, A. (2020) · NeuroMolecular Medicine · doi:10.1007/s12017-020-08612-4 · Cited by 48 · see citing works
Mishra, A., Wang, Y., Yin, F., Vitali, F., Rodgers, K. E., Soto, M., Mosconi, L., Wang, T., & Brinton, R. D. (2021) · Ageing Research Reviews · doi:10.1016/j.arr.2021.101542 · Cited by 44 · see citing works
PINK1 is a target of T cell responses in Parkinson’s disease
Williams, G. P., Freuchet, A., Michaelis, T., Frazier, A., Tran, N. K., Lima-Júnior, J. R., Phillips, E. J., Mallal, S. A., Litvan, I., Goldman, J. G., et al. (2024) · Journal of Clinical Investigation · doi:10.1172/jci180478 · Cited by 33 · see citing works
James, L. M., Christova, P. S., Lewis, S. M., Engdahl, B. E., Georgopoulos, A., & Georgopoulos, A. P. (2018) · EBioMedicine · doi:10.1016/j.ebiom.2018.02.005 · Cited by 31 · see citing works
HLA genetics in bipolar disorder
Tamouza, R., Oliveira, J., Étain, B., Bengoufa, D., Hamdani, N., Manier, C., Mariaselvam, C. M., Sundaresh, A., Bellivier, F., Henry, C., et al. (2018) · Acta Psychiatrica Scandinavica · doi:10.1111/acps.12912 · Cited by 31 · see citing works
Lokki, M., & Paakkanen, R. (2018) · HLA · doi:10.1111/tan.13429 · Cited by 31 · see citing works
Persistent Antigens Hypothesis: The Human Leukocyte Antigen (HLA) Connection
James, L. M., & Georgopoulos, A. P. (2018) · Journal of Neurology and Neuromedicine · doi:10.29245/2572.942x/2018/6.1235 · Cited by 28 · see citing works
James, L. M., & Georgopoulos, A. P. (2019) · Journal of Neurology and Neuromedicine · doi:10.29245/2572.942x/2019/5.1253 · Cited by 24 · see citing works
Analysis of shared underlying mechanism in neurodegenerative disease
Butler, R., Bradford, D. R., & Rodgers, K. E. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2022.1006089 · Cited by 23 · see citing works
James, L. M., Dolan, S., Leuthold, A. C., Engdahl, B. E., Georgopoulos, A., & Georgopoulos, A. P. (2018) · EBioMedicine · doi:10.1016/j.ebiom.2018.08.026 · Cited by 23 · see citing works
Initiative, A. D. N., Maxwell, T. J., Corcoran, C., Del‐Aguila, J. L., Budde, J., Deming, Y. K., Cruchaga, C., Goate, A., & Kauwe, J. S. K. (2018) · Alzheimer s Research & Therapy · doi:10.1186/s13195-018-0410-y · Cited by 22 · see citing works
Self-citationHsieh, L., Song, J., Tremoulet, A. H., Burns, J. C., & Franco, A. (2022) · Clinical & Experimental Immunology · doi:10.1093/cei/uxac046 · Cited by 22 · see citing works
CYP1B1-RMDN2 Alzheimer’s disease endophenotype locus identified for cerebral tau PET
Nho, K. T., Risacher, S. L., Apostolova, L. G., Bice, P. J., Brosch, J. R., Deardorff, R. L., Faber, K. M., Farlow, M. R., Foroud, T., Gao, S., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-52298-2 · Cited by 22 · see citing works
Shared Genetics of Multiple System Atrophy and Inflammatory Bowel Disease
Shadrin, A. A., Mucha, S., Ellinghaus, D., Makarious, M. B., Blauwendraat, C., Sreelatha, A. A. K., Heras‐Garvin, A., Ding, J., Hammer, M. B., Foubert‐Samier, A., et al. (2020) · Movement Disorders · doi:10.1002/mds.28338 · Cited by 21 · see citing works
James, L. M., & Georgopoulos, A. P. (2021) · Journal of Immunological Sciences · doi:10.29245/2578-3009/2021/2.1209 · Cited by 21 · see citing works
Protein degradation-associated mechanisms that are affected in Alzheimer´s disease
Tecalco-Cruz, Á. C., Pedraza‐Chaverrí, J., Briones‐Herrera, A., Cruz-Ramos, E., López‐Cánovas, L., & Zepeda–Cervantes, J. (2022) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-021-04334-8 · Cited by 21 · see citing works
Human Leukocyte Antigen as a Key Factor in Preventing Dementia and Associated Apolipoprotein E4 Risk
James, L. M., & Georgopoulos, A. P. (2019) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2019.00082 · Cited by 20 · see citing works
Alzheimer’s Disease Genetics: A Dampened Microglial Response?
Chatila, Z. K., & Bradshaw, E. M. (2021) · The Neuroscientist · doi:10.1177/10738584211024531 · Cited by 20 · see citing works
Setbacks in Alzheimer research demand new strategies, not surrender
Jobke, B., McBride, T. C., Nevin, L. M., Peiperl, L., Ross, A. J., Stone, C., Turner, R. C., & Editors, A. T. P. M. (2018) · PLoS Medicine · doi:10.1371/journal.pmed.1002518 · Cited by 20 · see citing works
Kuan, P. F., Clouston, S., Yang, X., Che, C., Gandy, S., Kotov, R., Bromet, E. J., & Luft, B. J. (2021) · Alzheimer s & Dementia Diagnosis Assessment & Disease Monitoring · doi:10.1002/dad2.12154 · Cited by 18 · see citing works
Sarri, C. A., Papadopoulos, G. E., Papa, A., Tsakris, A., Pervanidou, D., Baka, A., Politis, C., Billinis, C., Hadjichristodoulou, C. S., Mamuris, Z., et al. (2018) · PLoS ONE · doi:10.1371/journal.pone.0205557 · Cited by 16 · see citing works
Dissecting the limited genetic overlap of Parkinson's and Alzheimer's disease
Andersen, M. S., Tan, M. M. X., Holtman, I. R., Hardy, J., & Pihlstrøm, L. (2022) · Annals of Clinical and Translational Neurology · doi:10.1002/acn3.51606 · Cited by 15 · see citing works
Shigemizu, D., Fukunaga, K., Yamakawa, A., Suganuma, M., Fujita, K., Kimura, T., Watanabe, K., Mushiroda, T., Sakurai, T., Niida, S., et al. (2024) · npj Aging · doi:10.1038/s41514-023-00131-3 · Cited by 13 · see citing works
Association of HLA–DRB1, DQA1 and DQB1 alleles and haplotype in Parkinson’s disease from South India
Pandi, S., Chinniah, R., Sevak, V., Ravi, P. M., Raju, M., Vellaiappan, N. A., & Balakrishnan, K. (2021) · Neuroscience Letters · doi:10.1016/j.neulet.2021.136296 · Cited by 13 · see citing works
The relationship of early- and late-onset Alzheimer’s disease genes with COVID-19
Şirin, S., Dolanbay, S. N., & Aslım, B. (2022) · Journal of Neural Transmission · doi:10.1007/s00702-022-02499-0 · Cited by 13 · see citing works
The role of critical immune genes in brain disorders: insights from neuroimaging immunogenetics
Bian, B., Couvy‐Duchesne, B., Wray, N. R., & McRae, A. F. (2022) · Brain Communications · doi:10.1093/braincomms/fcac078 · Cited by 13 · see citing works
An Integrated Molecular Atlas of Alzheimer’s DiseasePreprint
Wörheide, M. A., Krumsiek, J., Nataf, S., Nho, K. T., Greenwood, A. K., Wiley, J. C., Willruth, L.-L., Wu, T., Bellur, O., Marella, B., et al. (2021) · medRxiv · doi:10.1101/2021.09.14.21263565 · Cited by 12 · see citing works
DNA methylation signature of a lifestyle-based resilience index for cognitive health
Zhang, W. Y., Lukacsovich, D., Young, J. I., Gomez, L., Schmidt, M. A., Martin, E. R., Kunkle, B. W., Chen, X. S., O’Shea, D. M., Galvin, J. E., et al. (2025) · Alzheimer s Research & Therapy · doi:10.1186/s13195-025-01733-7 · Cited by 11 · see citing works
Lin, Z., Xue, H., Malakhov, M. M., Knutson, K. A., & Pan, W. (2022) · Human Molecular Genetics · doi:10.1093/hmg/ddac015 · Cited by 10 · see citing works
Statistical power of transcriptome‐wide association studies
He, R., Xue, H., Pan, W., & Initiative, A. D. N. (2022) · Genetic Epidemiology · doi:10.1002/gepi.22491 · Cited by 10 · see citing works
Huang, P.-Y. S., Yang, Y., Chang, Y.-H., Chang, S.-L., Chou, M., Lai, C., Liu, C., & Chen, H. (2020) · Translational Psychiatry · doi:10.1038/s41398-020-0826-6 · Cited by 9 · see citing works
Dissecting the immune response of CD4+ T cells in Alzheimer’s disease
Kostić, M. S., Živković, N., Cvetanović, A., Bašić, J., & Stojanović, I. R. (2024) · Reviews in the Neurosciences · doi:10.1515/revneuro-2024-0090 · Cited by 8 · see citing works
Acquired immunity and Alzheimer's disease
Feng, W., Zhang, Y., Sun, P. G., & Xiao, M. (2022) · Journal of Biomedical Research · doi:10.7555/jbr.36.20220083 · Cited by 8 · see citing works
Rad, F. R., Akbari, M. G., Zamani, M., Bayat, S., & Zamani, M. (2021) · Molecular Neurobiology · doi:10.1007/s12035-021-02295-z · Cited by 7 · see citing works
Hsieh, L., Sidney, J., Burns, J. C., Boyle, D. L., Firestein, G. S., Altman, Y., Sette, A., & Franco, A. (2021) · The Journal of Immunology · doi:10.4049/jimmunol.2001009 · Cited by 7 · see citing works
Xie, H., Li, Y., Wu, X., Wang, R., Long, X., Su, M., Chen, Q., Li, L., Tian, R., & Jia, Z. (2023) · Quantitative Imaging in Medicine and Surgery · doi:10.21037/qims-23-268 · Cited by 6 · see citing works
Zhang, L., Wang, D.-Z., Wang, J., Guo, L., Li, B.-H., & Wang, J. (2023) · Journal of Alzheimer s Disease · doi:10.3233/jad-230007 · Cited by 6 · see citing works
Cătană, C.-S., Marta, M. M., Văleanu, M., Dican, L., & Crișan, C. A. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25158544 · Cited by 6 · see citing works
James, L. M., Charonis, S. A., & Georgopoulos, A. P. (2021) · Journal of Immunological Sciences · doi:10.29245/2578-3009/2021/3.1218 · Cited by 6 · see citing works
Rosewood, T. J., Nho, K. T., Risacher, S. L., Liu, S., Gao, S., Shen, L., Foroud, T., Saykin, A. J., & Initiative, A. D. N. (2024) · Alzheimer s & Dementia · doi:10.1002/alz.14308 · Cited by 5 · see citing works
Han, S., Cho, S.-A., Choi, W., Eilbeck, K. L., Coon, H. H., Nho, K. T., & Lee, Y. (2025) · BMC Genomics · doi:10.1186/s12864-025-11362-x · Cited by 5 · see citing works
C4d, a high-affinity LilrB2 ligand, is elevated in Alzheimer’s disease and mediates synapse pruning
Brott, B. K., Raissi, A. J., Micheva, K. D., Vielmetter, J., Mendes, M. S., Baccus, C. J., Huang, J., & Shatz, C. J. (2025) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2519253122 · Cited by 5 · see citing works
Cardoso, E. M., Lourenço‐Gomes, V., Esgalhado, A. J., Reste‐Ferreira, D., Oliveira, N., Amaral, A. S., Martinho, A., Gama, J. M. R., Verde, I., Lourenço, O. M., et al. (2023) · HLA · doi:10.1111/tan.15149 · Cited by 5 · see citing works
Investigation of the HLA locus in autopsy-confirmed progressive supranuclear palsy
Wang, J., Forrest, S. L., Dasari, S., Tanaka, H., Rogaeva, E. A., Tartaglia, M. C., Fox, S. H., Lang, A. E., Kalyaanamoorthy, S., & Kovács, G. G. (2025) · Immunobiology · doi:10.1016/j.imbio.2025.152892 · Cited by 5 · see citing works
James, L. M., Leuthold, A. C., & Georgopoulos, A. P. (2023) · Neuroscience Insights · doi:10.1177/26331055231159658 · Cited by 5 · see citing works
Kumar, V., Bhuiyan, P., Qi, J., Chen, Y., Zhang, J., Yang, F., & Li, J. (2023) · Bioinformatics and Biology Insights · doi:10.1177/11779322231167977 · Cited by 5 · see citing works
<i>HLA’s</i> hidden hand in Alzheimer’s disease—five research questions en route to an answer
Capitani, L., & Carpanini, S. M. (2025) · Brain Communications · doi:10.1093/braincomms/fcaf438 · Cited by 4 · see citing works
Contributions of vascular and Alzheimer's disease pathology to dementia
Strandberg, T. E., & Tienari, P. J. (2019) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2019.04.004 · Cited by 4 · see citing works
Rosewood, T. J., Nho, K. T., Risacher, S. L., Gao, S., Shen, L., Foroud, T., Saykin, A. J., & Initiative, O. B. O. T. A. D. N. (2023) · Genes · doi:10.3390/genes14112010 · Cited by 3 · see citing works
Mignot, E. J.-M., Guen, Y. L., Luo, G., Ambati, A., Damotte, V., Jansen, I. E., Yu, E., Nicolas, A., de Rojas, I., Leal, T. P., et al. (2022) · Research Square · doi:10.21203/rs.3.rs-1285855/v1 · Cited by 3 · see citing works
Self-citationDistinct neuroinflammatory profiles in progressive supranuclear palsy associated with HLA haplotypes
Forrest, S. L., Zaheer, S. S., Kim, A., Tanaka, H., Chasiotis, H., Li, J., Fox, S. H., Wang, J., Tartaglia, M. C., Lang, A. E., et al. (2026) · Brain Communications · doi:10.1093/braincomms/fcag084 · Cited by 2 · see citing works
Immunogenetic mechanism driving neurological and neurodegenerative disorders
Hajam, Y. A., Premlata, P., Rani, R., Sharma, R., Sharma, P., & Kumar, R. (2022) · Elsevier eBooks · doi:10.1016/b978-0-323-90250-2.00001-7 · Cited by 2 · see citing works
Lipid associated polygenic enrichment in Alzheimer’s diseasePreprint
Broce, I., Tan, C. H., Fan, C. C., Witoelar, A., Wen, N., Jansen, I. E., Hess, C. P., Dillon, W. P., Glastonbury, C. M., Glymour, M. M., et al. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/383844 · Cited by 2 · see citing works
Self-citationJacobson, T. Y., Nho, K. T., Risacher, S. L., Gao, S., Shen, L., Foroud, T., Saykin, A. J., & Initiative, A. D. N. (2021) · medRxiv · doi:10.1101/2021.08.13.21261887 · Cited by 2 · see citing works
Genetic Factors in Neuroimmune Diseases
Didonna, A. (2024) · Springer eBooks · doi:10.1007/978-3-031-24297-7_11-1 · Cited by 1 · see citing works
HLA-DRB1*15:01 is associated with a reduced likelihood of longevity in northern European men
Mejía, N. M., Kolbe, D., Özer, O., Dose, J., Torres, G. G., Franke, A., Nygaard, M., & Nebel, A. (2025) · Genome Medicine · doi:10.1186/s13073-025-01554-1 · Cited by 1 · see citing works
Xu, X., Fan, S.-S., Wu, H., Du, Y., Bo, Y., He, J., He, Y., Cheng, N., & Meng, X. (2026) · Translational Psychiatry · doi:10.1038/s41398-026-04280-3 · Cited by 1 · see citing works
James, L. M., Stratigopoulos, G., Leuthold, A. C., & Georgopoulos, A. P. (2026) · Scientific Reports · doi:10.1038/s41598-026-44894-7 · Cited by 1 · see citing works
HLA-DRB1*15:01 drives sex- and age-dependent microglial immune phenotypes and neuroimmune signaling
Reyes‐Reyes, E. M., Chinnasamy, D., Trial, M., Fernandez, F., Nguyen, V. D., He, Q., Leslie, A. C., Begay, J., Triplett, J., Bradford, D. R., et al. (2026) · Frontiers in Immunology · doi:10.3389/fimmu.2026.1796692 · Cited by 1 · see citing works
Gong, W. (2026) · npj Systems Biology and Applications · doi:10.1038/s41540-026-00797-x · Cited by 1 · see citing works
Genetic Factors in Neuroimmune Diseases
Didonna, A., & Cantó, E. (2019) · Contemporary clinical neuroscience · doi:10.1007/978-3-030-19515-1_11 · Cited by 1 · see citing works
Association of the HLA-DQB1*02 allele with lower tauopathy in Alzheimer's disease
Huda, T. I., Fawcett, T. J., Green, A. J., & Blanck, G. (2025) · Archives of Gerontology and Geriatrics · doi:10.1016/j.archger.2025.105802 · Cited by 1 · see citing works
Autoreactomes in Healthy Individuals Vary According to HLA Class II GenotypePreprint
Suseno, R., Boquett, J. A., Dandekar, R., Ituarte, T., Sharathchandra, A., Alvarenga, B. D., Vierra‐Green, C., Spellman, S. R., Maiers, M. J., DeRisi, J. L., et al. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.02.19.706904 · Cited by 1 · see citing works
Self-citationImmunogenetics of neurological disease
Jager, P. L. D. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-813955-4.00005-2
Immune Regulatory Functions of IgG in the Ontogeny of Human Natural Regulatory T Cells
Franco, A. (2022) · Critical Reviews in Immunology · doi:10.1615/critrevimmunol.2022045009
Immunogenetics of Alzheimer’s disease: the human leukocyte antigen
Costescu, C., Vică, L. M., Bâlici, Ș., Nicula, G. Z., Nemeş, B., Coman, H. G., & Matei, H. V. (2023) · Psihiatru ro · doi:10.26416/psih.75.4.2023.8928
Sun, Y., Zhu, J., Zhou, D., Canchi, S., Wu, C., Cox, N. J., Rissman, R. A., Gamazon, E. R., & Wu, L. (2021) · Figshare · doi:10.6084/m9.figshare.16557372
Sun, Y., Zhu, J., Zhou, D., Canchi, S., Wu, C., Cox, N. J., Rissman, R. A., Gamazon, E. R., & Wu, L. (2021) · Figshare · doi:10.6084/m9.figshare.16557345
Sun, Y., Zhu, J., Zhou, D., Canchi, S., Wu, C., Cox, N. J., Rissman, R. A., Gamazon, E. R., & Wu, L. (2021) · Figshare · doi:10.6084/m9.figshare.16557378
Sun, Y., Zhu, J., Zhou, D., Canchi, S., Wu, C., Cox, N. J., Rissman, R. A., Gamazon, E. R., & Wu, L. (2021) · Figshare · doi:10.6084/m9.figshare.16557333
Sun, Y., Zhu, J., Zhou, D., Canchi, S., Wu, C., Cox, N. J., Rissman, R. A., Gamazon, E. R., & Wu, L. (2021) · Figshare · doi:10.6084/m9.figshare.16557360
Sun, Y., Zhu, J., Zhou, D., Canchi, S., Wu, C., Cox, N. J., Rissman, R. A., Gamazon, E. R., & Wu, L. (2021) · Figshare · doi:10.6084/m9.figshare.16557354
Sun, Y., Zhu, J., Zhou, D., Canchi, S., Wu, C., Cox, N. J., Rissman, R. A., Gamazon, E. R., & Wu, L. (2021) · Figshare · doi:10.6084/m9.figshare.16557342
Sun, Y., Zhu, J., Zhou, D., Canchi, S., Wu, C., Cox, N. J., Rissman, R. A., Gamazon, E. R., & Wu, L. (2021) · Figshare · doi:10.6084/m9.figshare.16557357
Sun, Y., Zhu, J., Zhou, D., Canchi, S., Wu, C., Cox, N. J., Rissman, R. A., Gamazon, E. R., & Wu, L. (2021) · Figshare · doi:10.6084/m9.figshare.16557375
Sun, Y., Zhu, J., Zhou, D., Canchi, S., Wu, C., Cox, N. J., Rissman, R. A., Gamazon, E. R., & Wu, L. (2021) · Figshare · doi:10.6084/m9.figshare.16557348
Sun, Y., Zhu, J., Zhou, D., Canchi, S., Wu, C., Cox, N. J., Rissman, R. A., Gamazon, E. R., & Wu, L. (2021) · Figshare · doi:10.6084/m9.figshare.16557369
Sun, Y., Zhu, J., Zhou, D., Canchi, S., Wu, C., Cox, N. J., Rissman, R. A., Gamazon, E. R., & Wu, L. (2021) · Figshare · doi:10.6084/m9.figshare.16557336
Immunogenetics of neurological disease
Jager, P. L. D. (2024) · Elsevier eBooks · doi:10.1016/b978-0-443-19041-4.00075-3
Genetic Factors in Neuroimmune Diseases
Didonna, A. (2024) · Springer eBooks · doi:10.1007/978-3-031-60006-7_11
Sun, Y., Zhu, J., Zhou, D., Canchi, S., Wu, C., Cox, N. J., Rissman, R. A., Gamazon, E. R., & Wu, L. (2021) · Figshare · doi:10.6084/m9.figshare.16557339
Cruz, L. A., Liu, S., Miskimen, K. L. S., Bailey, J. N. C., Kinzy, T. G., Song, Y. E., Laux, R. A., Miron, P. L., Ogrocki, P. K., Lerner, A. J., et al. (2026) · Annals of Human Genetics · doi:10.64898/2026.01.25.26344754
Yang, X., Jiang, J., Li, W., Pan, R., & Li, Y. (2026) · The Journal of Prevention of Alzheimer s Disease · doi:10.1016/j.tjpad.2026.100509
- Authors
- Steele, N. Z. R., Carr, J. S., Bonham, L. W., Geier, E. G., Damotte, V., Miller, Z. A., Desikan, R. S., Boehme, K. L., Mukherjee, S., Crane, P. K., Kauwe, J. S. K., Kramer, J. H., Miller, B. L., Coppola, G., Hollenbach, J. A., Huang, Y., & Yokoyama, J. S.
- Affiliations
- University of California, San Francisco (US)
- Gladstone Institutes (US)
- Johns Hopkins University (US)
- Brigham Young University (US)
- University of Washington (US)
- University of California, Los Angeles (US)
- Corresponding author
- Yokoyama, Jennifer S.
- ORCID
- Venue
- PLOS Medicine
- Publisher
- Public Library of Science (PLoS)
- Published
- 2017-03-28
- Volume
- 14
- Issue
- 3
- Pages
- e1002272
- ISSN
- 1549-1277 (ISSN-L)
- 1549-1676
- PMC
- PMC5369701
- OpenAlex
- W2597790250
- Cited by
- 91
- References
- 82
- Citations by year
- 2026: 8 · 2025: 8 · 2024: 10 · 2023: 10 · 2022: 14 · 2021: 15 · 2020: 5 · 2019: 8 · 2018: 10 · 2017: 3
- FWCI
- 5.22
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- PLoS Medicine (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Funders
- Larry L. Hillblom Foundation (2016-A-005-SUP, Hillblom Aging Network)
- National Institute on Aging (AG049152, R01 AG048017, K23 AG048291, AG023501, AG1972403)
- Tau Consortium
- National Alzheimer's Coordinating Center (Junior Investigator Award)
- Foundation of the American Society of Neuroradiology (Alzheimer's Imaging Grant)
- National Institutes of Health (RC1 AG035610, R01 AG26938)
- The John Douglas French Alzheimer's Foundation
- Dr. Miriam and Sheldon G. Adelson Medical Research Foundation
- CHDI Foundation
- Takeda Pharmaceutical Company
- National Institute of Neurological Disorders and Stroke (P30 NS062691)
- 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, human leukocyte antigen, HLA haplotypes, major histocompatibility complex, genetic risk, neuroinflammation, APOE ε4, APOE ε2, APOE ε3, cerebrospinal fluid biomarkers, CSF tau, cognitive decline
- MeSH terms
- Aged, Aged, 80 and over, Alzheimer Disease, Chromosome Mapping, Female, Haplotypes, HLA Antigens, Humans, Male, Middle Aged, Risk Factors, San Francisco, United States, Case-Control Studies
About these checks
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.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
