Analysis of the Putative Role of CR1 in Alzheimer's Disease: Genetic Association, Expression and Function

Chronic activation of the complement system and induced inflammation are associated with neuropathology in Alzheimer's disease (AD). Recent large genome wide association studies (GWAS) have identified single nucleotide polymorphisms (SNPs) in the C3b/C4b receptor (CR1 or CD35) that are associat...

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Published inPloS one Vol. 11; no. 2; p. e0149792
Main Authors Fonseca, Maria I, Chu, Shuhui, Pierce, Aimee L, Brubaker, William D, Hauhart, Richard E, Mastroeni, Diego, Clarke, Elizabeth V, Rogers, Joseph, Atkinson, John P, Tenner, Andrea J
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 25.02.2016
Public Library of Science (PLoS)
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Abstract Chronic activation of the complement system and induced inflammation are associated with neuropathology in Alzheimer's disease (AD). Recent large genome wide association studies (GWAS) have identified single nucleotide polymorphisms (SNPs) in the C3b/C4b receptor (CR1 or CD35) that are associated with late onset AD. Here, anti-CR1 antibodies (Abs) directed against different epitopes of the receptor, were used to localize CR1 in brain, and relative binding affinities of the CR1 ligands, C1q and C3b, were assessed by ELISA. Most Abs tested stained red blood cells in blood vessels but showed no staining in brain parenchyma. However, two monoclonal anti-CR1 Abs labeled astrocytes in all of the cases tested, and this reactivity was preabsorbed by purified recombinant human CR1. Human brain-derived astrocyte cultures were also reactive with both mAbs. The amount of astrocyte staining varied among the samples, but no consistent difference was conferred by diagnosis or the GWAS-identified SNPs rs4844609 or rs6656401. Plasma levels of soluble CR1 did not correlate with diagnosis but a slight increase was observed with rs4844609 and rs6656401 SNP. There was also a modest but statistically significant increase in relative binding activity of C1q to CR1 with the rs4844609 SNP compared to CR1 without the SNP, and of C3b to CR1 in the CR1 genotypes containing the rs6656401 SNP (also associated with the larger isoform of CR1) regardless of clinical diagnosis. These results suggest that it is unlikely that astrocyte CR1 expression levels or C1q or C3b binding activity are the cause of the GWAS identified association of CR1 variants with AD. Further careful functional studies are needed to determine if the variant-dictated number of CR1 expressed on red blood cells contributes to the role of this receptor in the progression of AD, or if another mechanism is involved.
AbstractList Chronic activation of the complement system and induced inflammation are associated with neuropathology in Alzheimer's disease (AD). Recent large genome wide association studies (GWAS) have identified single nucleotide polymorphisms (SNPs) in the C3b/C4b receptor (CR1 or CD35) that are associated with late onset AD. Here, anti-CR1 antibodies (Abs) directed against different epitopes of the receptor, were used to localize CR1 in brain, and relative binding affinities of the CR1 ligands, C1q and C3b, were assessed by ELISA. Most Abs tested stained red blood cells in blood vessels but showed no staining in brain parenchyma. However, two monoclonal anti-CR1 Abs labeled astrocytes in all of the cases tested, and this reactivity was preabsorbed by purified recombinant human CR1. Human brain-derived astrocyte cultures were also reactive with both mAbs. The amount of astrocyte staining varied among the samples, but no consistent difference was conferred by diagnosis or the GWAS-identified SNPs rs4844609 or rs6656401. Plasma levels of soluble CR1 did not correlate with diagnosis but a slight increase was observed with rs4844609 and rs6656401 SNP. There was also a modest but statistically significant increase in relative binding activity of C1q to CR1 with the rs4844609 SNP compared to CR1 without the SNP, and of C3b to CR1 in the CR1 genotypes containing the rs6656401 SNP (also associated with the larger isoform of CR1) regardless of clinical diagnosis. These results suggest that it is unlikely that astrocyte CR1 expression levels or C1q or C3b binding activity are the cause of the GWAS identified association of CR1 variants with AD. Further careful functional studies are needed to determine if the variant-dictated number of CR1 expressed on red blood cells contributes to the role of this receptor in the progression of AD, or if another mechanism is involved.
Audience Academic
Author Atkinson, John P
Brubaker, William D
Mastroeni, Diego
Chu, Shuhui
Hauhart, Richard E
Tenner, Andrea J
Fonseca, Maria I
Rogers, Joseph
Clarke, Elizabeth V
Pierce, Aimee L
AuthorAffiliation 7 School for Mental Health and Neuroscience (MHeNS), Department of Psychiatry and Neuropsychology, Faculty of Health, Medicine and Life Sciences, European Graduate School of Neuroscience (EURON), Maastricht University Medical Centre, Maastricht, The Netherlands
6 Banner Sun Health Research Institute, Sun City, Arizona, 85351, United States of America
4 SRI International, Menlo Park, California, 94025, United States of America
3 UCI Institute for Memory Impairment and Neurological Disorders, University of California Irvine, Irvine, California, 92697, United States of America
5 Division of Rheumatology, Department of Medicine, Washington University School of Medicine, St. Louis, Missouri, 63110, United States of America
1 Department of Molecular Biology and Biochemistry, University of California Irvine, Irvine, California, 92697, United States of America
2 Department of Neurology, University of California Irvine, Irvine, California, 92697, United States of America
Colorado State University, Col
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/26914463$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright COPYRIGHT 2016 Public Library of Science
2016 Fonseca et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
2016 Fonseca et al 2016 Fonseca et al
Copyright_xml – notice: COPYRIGHT 2016 Public Library of Science
– notice: 2016 Fonseca et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
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content type line 23
Current address: Department of Neurology, Oregon Health and Sciences University, Portland, Oregon, 97239, United States of America
Competing Interests: The authors have declared that no competing interests exist.
Current address: The Biodesign Institute, Neurodegenerative Disease Research Center (NDRC) Arizona State University, Tempe, Arizona, 85287, United States of America
Conceived and designed the experiments: MIF SC WDB REH EVC JR JPA AJT. Performed the experiments: MIF SC WDB EVC DM REH. Analyzed the data: MIF SC WDB EVC REH JR JPA AJT. Contributed reagents/materials/analysis tools: ALP JPA JR. Wrote the paper: MIF SC JR DM JPA REH AJT. Patient evaluation: ALP.
OpenAccessLink https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4767815/
PMID 26914463
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Snippet Chronic activation of the complement system and induced inflammation are associated with neuropathology in Alzheimer's disease (AD). Recent large genome wide...
Chronic activation of the complement system and induced inflammation are associated with neuropathology in Alzheimer’s disease (AD). Recent large genome wide...
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SubjectTerms Aged
Aged, 80 and over
Alzheimer Disease - blood
Alzheimer Disease - genetics
Alzheimer Disease - metabolism
Alzheimer's disease
Alzheimers disease
Analysis
Antibodies
Astrocytes
Astrocytes - metabolism
Binding
Biochemistry
Biology and Life Sciences
Blood
Blood cells
Blood vessels
Brain
Brain - pathology
Brain research
Cell receptors
Complement activation
Complement C1q - metabolism
Complement C3b - metabolism
Complement component C1q
Complement component C3b
Development and progression
Diagnosis
Enzyme-linked immunosorbent assay
Epitopes
Erythrocytes
Erythrocytes - metabolism
Female
Gene Expression Regulation
Genetic aspects
Genetic Predisposition to Disease - genetics
Genomes
Genotypes
Humans
Immune system
Male
Medicine
Medicine and Health Sciences
Molecular biology
Neurodegenerative diseases
Neurological disorders
Neurosciences
Parenchyma
Physical Sciences
Physiological aspects
Plasma levels
Polymorphism, Single Nucleotide
Protein Transport
Proteins
Receptors, Complement 3b - blood
Receptors, Complement 3b - genetics
Receptors, Complement 3b - metabolism
Red blood cells
Research and Analysis Methods
Rheumatology
Single nucleotide polymorphisms
Single-nucleotide polymorphism
Staining
Statistical analysis
Statistical methods
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Title Analysis of the Putative Role of CR1 in Alzheimer's Disease: Genetic Association, Expression and Function
URI https://www.ncbi.nlm.nih.gov/pubmed/26914463
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http://dx.doi.org/10.1371/journal.pone.0149792
Volume 11
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