Genome-wide association study identifies variants at CLU and CR1 associated with Alzheimer's disease
Open accessAbstract
The gene encoding apolipoprotein E (APOE) on chromosome 19 is the only confirmed susceptibility locus for late-onset Alzheimer's disease. To identify other risk loci, we conducted a large genome-wide association study of 2,032 individuals from France with Alzheimer's disease (cases) and 5,328 controls. Markers outside APOE with suggestive evidence of association (P < 10(-5)) were examined in collections from Belgium, Finland, Italy and Spain totaling 3,978 Alzheimer's disease cases and 3,297 controls. Two loci gave replicated evidence of association: one within CLU (also called APOJ), encoding clusterin or apolipoprotein J, on chromosome 8 (rs11136000, OR = 0.86, 95% CI 0.81-0.90, P = 7.5 x 10(-9) for combined data) and the other within CR1, encoding the complement component (3b/4b) receptor 1, on chromosome 1 (rs6656401, OR = 1.21, 95% CI 1.14-1.29, P = 3.7 x 10(-9) for combined data). Previous biological studies support roles of CLU and CR1 in the clearance of beta amyloid (Abeta) peptide, the principal constituent of amyloid plaques, which are one of the major brain lesions of individuals with Alzheimer's disease.
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Nearly 30 late-onset Alzheimer's disease susceptibility loci are known, and risk is significantly polygenic.
“Nearly 30 LOAD susceptibility loci2-12 are known, and risk is significantly polygenic13.”
From Rare coding variants in PLCG2, ABI3, and TREM2 implicate microglial-mediated innate immunity in Alzheimer's disease (2017) · cites this paper as [4]
The paper reports genome-wide significant associations for CLU and PICALM, supporting its use among citations for late-onset Alzheimer’s susceptibility loci. It does not establish that nearly 30 loci were known; it says only APOE had previously been established unequivocally. The separate citation 13, not this paper, is attached to the polygenic-risk clause. (LLM, conf=0.83)
Experimental — accuracy not yet measuredGWAS have identified multiple loci associated with AD, including variants in PICALM, CLU, ABCA7, SORL1, CR1, TREM2, and BIN1.
“Genome-wide association studies (GWAS) have identified multiple loci associated with AD including to name a few, variants in PICALM , CLU , ATP-binding cassette transporter A7 ( ABCA7 ), sortilin related receptor-1 ( SORL1 ), complement receptor 1 ( CR1 ), triggering receptor expressed on myeloid cells 2 ( TREM2 ), and bridging integrator 1 ( BIN1 ) genes (219, 236, 254, 300, 343, 344, 528, 543).”
From Blood-Brain Barrier: From Physiology to Disease and Back (2019) · cites this paper as [343]
The paper’s Abstract reports genome-wide significant AD associations at CLU and PICALM, and suggestive associations at CR1 and BIN1. It does not support the sentence’s additional named loci—ABCA7, SORL1, and TREM2—from this source. (LLM, conf=0.88)
Experimental — accuracy not yet measuredSeveral GWAS studies have identified CLU as a significant genetic risk factor for sporadic AD.
“Several GWAS studies have identified CLU as a significant genetic risk factor for sporadic AD (94, 119, 236, 343).”
From Blood-Brain Barrier: From Physiology to Disease and Back (2019) · cites this paper as [343]
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 [83]
Among 149 identified familial AD and GWAS locus genes, 74 genes (49%) were differentially expressed for at least one cell type.
“We found that 74 genes (49%) were differentially expressed for at least one cell type, and multiple genes showed region-specific expression, including the lipid transporter ABCA7 (enriched in thalamus), the zinc-finger protein ZNF655 (EC) and the complement receptor CR1 (neocortex)56 (Extended Data Fig. 10).”
From Single-cell multiregion dissection of Alzheimer’s disease (2024) · cites this paper as [56]
CR1 is predominantly expressed by erythrocytes.
“CR1 is predominantly expressed by erythrocytes (343, 344) and A 𝛃 -C3b-CR1-mediated interactions sequester A 𝛃 42 to promote clearance to periphery (180, 338), suggesting that CR1 variants can increase free blood A 𝛃 levels (343), which in turn can promote RAGE-mediated A 𝛃 re-entry across the BBB into the brain.”
From Blood-Brain Barrier: From Physiology to Disease and Back (2019) · cites this paper as [343]
Our copy discusses CR1 in relation to Alzheimer’s disease genetic association (Abstract; page unavailable), but the retrieved passages do not describe where CR1 is expressed. Searches for erythrocytes, red blood cells, and CR1 expression did not find support for the claim. (LLM, conf=0.73)
Experimental — accuracy not yet measuredNeuroinflammation is a common feature of Alzheimer's disease, and GWAS have associated several immune-related genes with AD, including ABCA7, CD33, CLU, CR1, MS4A, and TREM2.
“Neuroinflammation is a common feature of AD9 and GWAS have associated several immune-related genes with AD including ABCA7, CD33, CLU, CR1, MS4A10, 11 and recently TREM2.12, 13”
From Whole-genome sequencing suggests a chemokine gene cluster that modifies age at onset in familial Alzheimer's disease (2015) · cites this paper as [11]
Stage 1 discovery meta-analysis produced 12 loci with genome-wide significance (P ≤ 5 × 10−8), all previously described.
“The Stage 1 discovery meta-analysis produced 12 loci with genome-wide significance (P ≤ 5 × 10−8) (Table 1), all of which are previously described1,4–11.”
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 [11]
The CLU intronic variant rs11136000 is associated with Alzheimer's disease.
“Two independent genome-wide association studies (GWAS) in 2009 found rs11136000, an intronic variant in CLU, associated with AD (Lambert et al, p=3.7×10−9 and Harold et al, p=8.5×10−10) (Harold, et al., 2009,Lambert, et al., 2009)”
From A potential endophenotype for Alzheimer's disease: cerebrospinal fluid clusterin (2016) · cites this paper as Lambert, et al., 2009
Polymorphisms in CLU are linked to Alzheimer's disease.
“polymorphisms in CLU are linked to AD19,20”
From Exercise plasma boosts memory and dampens brain inflammation via clusterin (2021) · cites this paper as [20]
CR1 variants are associated with increased risk for Alzheimer disease.
“the identification of CR1 variants associated with an increased risk for AD”
From Microglia Function in the Central Nervous System During Health and Neurodegeneration (2017) · cites this paper as [110]
Microglial expression of complement receptor CR1 has been linked to late-onset AD and may reflect microglial phagocytosis of synapses proposed to contribute to AD pathogenesis.
“microglial expression of the complement receptor CR1 has been linked to late-onset AD137,138 and may reflect the microglial phagocytosis of synapses that has been proposed to contribute to AD pathogenesis.”
From Microglial signatures and their role in health and disease (2018) · cites this paper as [138]
The 10 loci identified to date account for ~20% of the total variation in risk or ~33% of the risk attributable to genetic effects, with the major contribution being from APOE.
“the 10 loci identified to date account for ~20% of the total variation in risk or ~33% of the risk attributable to genetic effects, with the major contribution being from APOE”
From Genetic architectures of psychiatric disorders: the emerging picture and its implications (2012) · cites this paper as [34]
Multiple familial AD and GWAS locus genes showed region-specific expression, including ABCA7 enriched in thalamus, ZNF655 in EC, and CR1 in neocortex.
“We found that 74 genes (49%) were differentially expressed for at least one cell type, and multiple genes showed region-specific expression, including the lipid transporter ABCA7 (enriched in thalamus), the zinc-finger protein ZNF655 (EC) and the complement receptor CR1 (neocortex)56 (Extended Data Fig. 10).”
From Single-cell multiregion dissection of Alzheimer’s disease (2024) · cites this paper as [56]
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- Authors
- the European Alzheimer's Disease Initiative Investigators, Lambert, J.-C., Heath, S., Even, G., Campion, D., Sleegers, K., Hiltunen, M., Combarros, O., Zelenika, D., Bullido, M. J., Tavernier, B., Letenneur, L., Bettens, K., Berr, C., Pasquier, F., Fiévet, N., Barberger-Gateau, P., Engelborghs, S., De Deyn, P., Mateo, I., Franck, A., Helisalmi, S., Porcellini, E., Hanon, O., de Pancorbo, M. M., Lendon, C., Dufouil, C., Jaillard, C., Leveillard, T., Alvarez, V., Bosco, P., Mancuso, M., Panza, F., Nacmias, B., Bossù, P., Piccardi, P., Annoni, G., Seripa, D., Galimberti, D., Hannequin, D., Licastro, F., Soininen, H., Ritchie, K., Blanché, H., Dartigues, J.-F., Tzourio, C., Gut, I., Van Broeckhoven, C., Alpérovitch, A., Lathrop, M., & Amouyel, P.
- Affiliations
- Inserm (FR)
- University of Antwerp (BE)
- Universidad de Cantabria (ES)
- Consejo Superior de Investigaciones Científicas (ES)
- Institut Pasteur de Lille (FR)
- Hospital Universitario La Paz (ES)
- Kuopio University Hospital (FI)
- Institut de la Vision (FR)
- University of Pisa (IT)
- University of Florence (IT)
- Fondazione Santa Lucia (IT)
- University of Cagliari (IT)
- Casa Sollievo della Sofferenza (IT)
- University of Milan (IT)
- Commissariat à l'Énergie Atomique et aux Énergies Alternatives (FR)
- Corresponding author
- Amouyel, Philippe
- ORCID
- Lambert, Jean-Charles
- Heath, Simon
- Campion, Dominique
- Sleegers, Kristel
- Hiltunen, Mikko
- Bullido, Maria J
- Letenneur, Luc
- Berr, Claudine
- Pasquier, Florence
- Engelborghs, Sebastiaan
- Helisalmi, Seppo
- Porcellini, Elisa
- Hanon, Olivier
- Dufouil, Carole
- Jaillard, Céline
- Bosco, Paolo
- Mancuso, Michelangelo
- Panza, Francesco
- Nacmias, Benedetta
- Bossù, Paola
- Annoni, Giorgio
- Seripa, Davide
- Galimberti, Daniela
- Hannequin, Didier
- Soininen, Hilkka
- Ritchie, Karen
- Blanché, Hélène
- Dartigues, Jean-François
- Tzourio, Christophe
- Gut, Ivo
- Lathrop, Mark
- Amouyel, Philippe
- Venue
- Nature Genetics
- Published
- 2009-09-06
- Volume
- 41
- Issue
- 10
- Pages
- 1094-1099
- ISSN
- 1061-4036 (ISSN-L)
- 1546-1718
- OpenAlex
- W3214092816
- Cited by
- 2,234
- References
- 41
- Citations by year
- 2026: 47 · 2025: 58 · 2024: 100 · 2023: 106 · 2022: 106 · 2021: 145 · 2020: 155 · 2019: 120 · 2018: 135 · 2017: 146 · 2016: 145 · 2015: 152 · 2014: 162 · 2013: 141 · 2012: 178
- FWCI
- 112.24
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Genetics (publishedVersion)
- BOA (University of Milano-Bicocca) (submittedVersion, other-oa)
- CINECA IRIS Institutial research information system (University of Pisa) (submittedVersion)
- Archivio istituzionale della ricerca (Alma Mater Studiorum Università di Bologna) (submittedVersion)
- Florence Research (University of Florence) (submittedVersion)
- VUBIR (Vrije Universiteit Brussel) (submittedVersion)
- Funders
- U.S. Department of Health and Human Services (Z01 AG000950-06)
- Juvenile Diabetes Research Foundation International
- Wellcome Trust
- Alzheimer's Society
- Alzheimer's Research Trust
- Motor Neurone Disease Association
- University College London
- Cardiff University
- Bundesministerium für Bildung und Forschung
- Belgian Federal Science Policy Office
- Alfried Krupp von Bohlen und Halbach-Stiftung
- Universiteit Antwerpen
- Vlaamse regering
- H. Lundbeck A/S
- Instituut Born-Bunge
- Heinz Nixdorf Stiftung
- National Institutes of Health
- Medical Research Council
- Bijzonder Onderzoeksfonds UGent
- Helmholtz Zentrum München
- National Institute on Aging (Z01AG000950)
- National Institute of Allergy and Infectious Diseases
- National Institute of Diabetes and Digestive and Kidney Diseases
- National Institute of Child Health and Human Development
- 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, late-onset Alzheimer's disease, genetic susceptibility, clusterin, complement receptor 1, apolipoprotein E, amyloid-beta clearance, amyloid plaques, genetic susceptibility loci
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 ›
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