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Article ; Online: Strategies in Aggregation Tests for Rare Variants.

Rajabli, Farid / Kunkle, Brian W

Current protocols

2023 Volume 3, Issue 11, Page(s) e931

Abstract: Genome-wide association studies (GWAS) successfully identified numerous common variants involved in complex diseases, but only limited heritability was explained by these findings. Advances in high-throughput sequencing technology made it possible to ... ...

Abstract	Genome-wide association studies (GWAS) successfully identified numerous common variants involved in complex diseases, but only limited heritability was explained by these findings. Advances in high-throughput sequencing technology made it possible to assess the contribution of rare variants in common diseases. However, study of rare variants introduces challenges due to low frequency of rare variants. Well-established common variant methods were underpowered to identify the rare variants in GWAS. To address this challenge, several new methods have been developed to examine the role of rare variants in complex diseases. These approaches are based on testing the aggregate effect of multiple rare variants in a predefined genetic region. Provided here is an overview of statistical approaches and the protocols explaining step-by-step analysis of aggregations tests with the hands-on experience using R scripts in four categories: burden tests, adaptive burden tests, variance-component tests, and combined tests. Also explained are the concepts of rare variants, permutation tests, kernel methods, and genetic variant annotation. At the end we discuss relevant topics of bioinformatics tools for annotation, family-based design of rare-variant analysis, population stratification adjustment, and meta-analysis. © 2023 The Authors. Current Protocols published by Wiley Periodicals LLC.
MeSH term(s)	Genome-Wide Association Study/methods ; Disease/genetics ; Genetic Variation
Language	English
Publishing date	2023-11-21
Publishing country	United States
Document type	Journal Article
ISSN	2691-1299
ISSN (online)	2691-1299
DOI	10.1002/cpz1.931
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Article ; Online: An X Chromosome Transcriptome Wide Association Study Implicates ARMCX6 in Alzheimer's Disease.

Zhang, Xueyi / Gomez, Lissette / Below, Jennifer E / Naj, Adam C / Martin, Eden R / Kunkle, Brian W / Bush, William S

Journal of Alzheimer's disease : JAD

2024 Volume 98, Issue 3, Page(s) 1053–1067

Abstract: Background: The X chromosome is often omitted in disease association studies despite containing thousands of genes that may provide insight into well-known sex differences in the risk of Alzheimer's disease (AD).: Objective: To model the expression ... ...

Abstract	Background: The X chromosome is often omitted in disease association studies despite containing thousands of genes that may provide insight into well-known sex differences in the risk of Alzheimer's disease (AD). Objective: To model the expression of X chromosome genes and evaluate their impact on AD risk in a sex-stratified manner. Methods: Using elastic net, we evaluated multiple modeling strategies in a set of 175 whole blood samples and 126 brain cortex samples, with whole genome sequencing and RNA-seq data. SNPs (MAF > 0.05) within the cis-regulatory window were used to train tissue-specific models of each gene. We apply the best models in both tissues to sex-stratified summary statistics from a meta-analysis of Alzheimer's Disease Genetics Consortium (ADGC) studies to identify AD-related genes on the X chromosome. Results: Across different model parameters, sample sex, and tissue types, we modeled the expression of 217 genes (95 genes in blood and 135 genes in brain cortex). The average model R2 was 0.12 (range from 0.03 to 0.34). We also compared sex-stratified and sex-combined models on the X chromosome. We further investigated genes that escaped X chromosome inactivation (XCI) to determine if their genetic regulation patterns were distinct. We found ten genes associated with AD at p < 0.05, with only ARMCX6 in female brain cortex (p = 0.008) nearing the significance threshold after adjusting for multiple testing (α = 0.002). Conclusions: We optimized the expression prediction of X chromosome genes, applied these models to sex-stratified AD GWAS summary statistics, and identified one putative AD risk gene, ARMCX6.
MeSH term(s)	Humans ; Male ; Female ; Alzheimer Disease/genetics ; Transcriptome ; Genetic Predisposition to Disease/genetics ; X Chromosome ; Brain ; Polymorphism, Single Nucleotide/genetics ; Genome-Wide Association Study
Language	English
Publishing date	2024-03-14
Publishing country	Netherlands
Document type	Meta-Analysis ; Journal Article
ZDB-ID	1440127-7
ISSN	1875-8908 ; 1387-2877
ISSN (online)	1875-8908
ISSN	1387-2877
DOI	10.3233/JAD-231075
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Article: An X Chromosome Transcriptome Wide Association Study Implicates ARMCX6 in Alzheimer's Disease.

Zhang, Xueyi / Gomez, Lissette / Below, Jennifer / Naj, Adam / Martin, Eden / Kunkle, Brian / Bush, William S

bioRxiv : the preprint server for biology

2023

Abstract: Background: The X chromosome is often omitted in disease association studies despite containing thousands of genes which may provide insight into well-known sex differences in the risk of Alzheimer's Disease.: Objective: To model the expression of X ... ...

Abstract	Background: The X chromosome is often omitted in disease association studies despite containing thousands of genes which may provide insight into well-known sex differences in the risk of Alzheimer's Disease. Objective: To model the expression of X chromosome genes and evaluate their impact on Alzheimer's Disease risk in a sex-stratified manner. Methods: Using elastic net, we evaluated multiple modeling strategies in a set of 175 whole blood samples and 126 brain cortex samples, with whole genome sequencing and RNA-seq data. SNPs (MAF>0.05) within the Results: Across different model parameters, sample sex, and tissue types, we modeled the expression of 217 genes (95 genes in blood and 135 genes in brain cortex). The average model R Conclusions: We optimized the expression prediction of X chromosome genes, applied these models to sex-stratified AD GWAS summary statistics, and identified one putative AD risk gene,
Language	English
Publishing date	2023-10-05
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.06.06.543877
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Article ; Online: Critical evaluation of the reliability of DNA methylation probes on the Illumina MethylationEPIC v1.0 BeadChip microarrays.

Zhang, Wei / Young, Juan I / Gomez, Lissette / Schmidt, Michael A / Lukacsovich, David / Varma, Achintya / Chen, X Steven / Kunkle, Brian / Martin, Eden R / Wang, Lily

Epigenetics

2024 Volume 19, Issue 1, Page(s) 2333660

Abstract: DNA methylation (DNAm) plays a crucial role in a number of complex diseases. However, the reliability of DNAm levels measured using Illumina arrays varies across different probes. Previous research primarily assessed probe reliability by comparing ... ...

Abstract	DNA methylation (DNAm) plays a crucial role in a number of complex diseases. However, the reliability of DNAm levels measured using Illumina arrays varies across different probes. Previous research primarily assessed probe reliability by comparing duplicate samples between the 450k-450k or 450k-EPIC platforms, with limited investigations on Illumina EPIC v1.0 arrays. We conducted a comprehensive assessment of the EPIC v1.0 array probe reliability using 69 blood DNA samples, each measured twice, generated by the Alzheimer's Disease Neuroimaging Initiative study. We observed higher reliability in probes with average methylation beta values of 0.2 to 0.8, and lower reliability in type I probes or those within the promoter and CpG island regions. Importantly, we found that probe reliability has significant implications in the analyses of Epigenome-wide Association Studies (EWAS). Higher reliability is associated with more consistent effect sizes in different studies, the identification of differentially methylated regions (DMRs) and methylation quantitative trait locus (mQTLs), and significant correlations with downstream gene expression. Moreover, blood DNAm measurements obtained from probes with higher reliability are more likely to show concordance with brain DNAm measurements. Our findings, which provide crucial reliability information for probes on the EPIC v1.0 array, will serve as a valuable resource for future DNAm studies.
MeSH term(s)	DNA Methylation ; Oligonucleotide Array Sequence Analysis/methods ; Reproducibility of Results ; Quantitative Trait Loci ; CpG Islands
Language	English
Publishing date	2024-04-02
Publishing country	United States
Document type	Journal Article
ISSN	1559-2308
ISSN (online)	1559-2308
DOI	10.1080/15592294.2024.2333660
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Article: MIAMI-AD (Methylation in Aging and Methylation in AD): an integrative knowledgebase that facilitates explorations of DNA methylation across sex, aging, and Alzheimer's disease.

Lukacsovich, David / O'Shea, Deirdre / Huang, Hanchen / Zhang, Wei / Young, Juan I / Steven Chen, X / Dietrich, Sven-Thorsten / Kunkle, Brian / Martin, Eden R / Wang, Lily

medRxiv : the preprint server for health sciences

2023

Abstract: Alzheimer's disease (AD) is a common neurodegenerative disorder with a significant impact on aging populations. DNA methylation (DNAm) alterations have been implicated in both the aging processes and the development of AD. Given that AD affects more ... ...

Abstract	Alzheimer's disease (AD) is a common neurodegenerative disorder with a significant impact on aging populations. DNA methylation (DNAm) alterations have been implicated in both the aging processes and the development of AD. Given that AD affects more women than men, it is also important to explore DNAm changes that occur specifically in each sex. We created MIAMI-AD, a comprehensive knowledge base containing manually curated summary statistics from 97 published tables in 37 studies, all of which included at least 100 participants. MIAMI-AD enables easy browsing, querying, and downloading DNAm associations at multiple levels - at individual CpG, gene, genomic regions, or genome-wide, in one or multiple studies. Moreover, it also offers tools to perform integrative analyses, such as comparing DNAm associations across different phenotypes or tissues, as well as interactive visualizations. Using several use case examples, we demonstrated that MIAMI-AD facilitates our understanding of age-associated CpGs in AD and the sex-specific roles of DNAm in AD. This open-access resource is freely available to the research community, and all the underlying data can be downloaded. MIAMI-AD (https://miami-ad.org/) facilitates integrative explorations to better understand the interplay between DNAm across aging, sex, and AD.
Language	English
Publishing date	2023-12-05
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.12.04.23299412
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Article: Critical evaluation of the reliability of DNA methylation probes on the Illumina MethylationEPIC BeadChip microarrays.

Zhang, Wei / Young, Juan I / Gomez, Lissette / Schmidt, Michael A / Lukacsovich, David / Varma, Achintya / Chen, X Steven / Kunkle, Brian / Martin, Eden R / Wang, Lily

Research square

2023

Abstract	DNA methylation (DNAm) plays a crucial role in a number of complex diseases. However, the reliability of DNAm levels measured using Illumina arrays varies across different probes. Previous research primarily assessed probe reliability by comparing duplicate samples between the 450k-450k or 450k-EPIC platforms, with limited investigations on Illumina EPIC arrays. We conducted a comprehensive assessment of the EPIC array probe reliability using 138 duplicated blood DNAm samples generated by the Alzheimer's Disease Neuroimaging Initiative study. We introduced a novel statistical measure, the modified intraclass correlation, to better account for the disagreement in duplicate measurements. We observed higher reliability in probes with average methylation beta values of 0.2 to 0.8, and lower reliability in type I probes or those within the promoter and CpG island regions. Importantly, we found that probe reliability has significant implications in the analyses of Epigenome-wide Association Studies (EWAS). Higher reliability is associated with more consistent effect sizes in different studies, the identification of differentially methylated regions (DMRs) and methylation quantitative trait locus (mQTLs), and significant correlations with downstream gene expression. Moreover, blood DNAm measurements obtained from probes with higher reliability are more likely to show concordance with brain DNAm measurements. Our findings, which provide crucial reliable information for probes on the EPIC array, will serve as a valuable resource for future DNAm studies.
Language	English
Publishing date	2023-10-17
Publishing country	United States
Document type	Preprint
DOI	10.21203/rs.3.rs-3068938/v2
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Article: Professional and Amateur Pitchers' Perspective on the Ulnar Collateral Ligament Injury Risk.

Vance, Danica D / Alexander, Frank J / Kunkle, Brian W / Littlefield, Mark / Ahmad, Christopher S

Orthopaedic journal of sports medicine

2019 Volume 7, Issue 6, Page(s) 2325967119850777

Abstract: Background: Medial ulnar collateral ligament (UCL) injury is increasingly prevalent in professional baseball pitchers, and significant research has been devoted to understanding the risk factors and prevention strategies associated with it. To date, no ... ...

Abstract	Background: Medial ulnar collateral ligament (UCL) injury is increasingly prevalent in professional baseball pitchers, and significant research has been devoted to understanding the risk factors and prevention strategies associated with it. To date, no study has investigated what the players themselves believe causes and prevents the injury. Purpose: To evaluate the opinions of UCL injuries among pitchers, including professional athletes. Study design: Cross-sectional study. Methods: A total of 214 baseball pitchers (45 high school/college, 169 Major League Baseball [MLB]/Minor League Baseball) completed a 52-item questionnaire designed to evaluate their opinions on the cause of UCL injuries, injury prevention, and Tommy John surgery. Overall, 51 of the 214 pitchers had previously experienced a UCL injury. The frequency of the selection of each answer option was measured. Additionally, chi-square tests were used to compare (1) responses between professional and nonprofessional pitchers and (2) responses between pitchers with and without a previous UCL injury. Results: Only 45% of pitchers thought that UCL injuries are avoidable in MLB. Additionally, 55% of pitchers with a UCL injury had a history of elbow injuries as an adolescent/child, compared with 18% in the uninjured group ( Conclusion: Pitchers with a previous childhood elbow injury had a significantly higher incidence of UCL injuries during their adult career, suggesting possible predisposition to UCL injury and warranting further research. Fatigue and inadequate rest were of greatest concern among all pitchers for an increased risk of UCL injuries. Understanding and acknowledging the opinions that players have regarding UCL injuries are important to improve UCL education, prevention, and treatment.
Language	English
Publishing date	2019-06-20
Publishing country	United States
Document type	Journal Article
ZDB-ID	2706251-X
ISSN	2325-9671
ISSN	2325-9671
DOI	10.1177/2325967119850777
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Article ; Online: Genetic analyses in multiplex families confirms chromosome 5q35 as a risk locus for Alzheimer's Disease in individuals of African Ancestry.

Nuytemans, Karen / Rajabli, Farid / Jean-Francois, Melissa / Kurup, Jiji Thulaseedhara / Adams, Larry D / Starks, Takiyah D / Whitehead, Patrice L / Kunkle, Brian W / Caban-Holt, Allison / Haines, Jonathan L / Cuccaro, Michael L / Vance, Jeffery M / Byrd, Goldie S / Beecham, Gary W / Reitz, Christiane / Pericak-Vance, Margaret A

Neurobiology of aging

2023 Volume 133, Page(s) 125–133

Abstract: There is a paucity of genetic studies of Alzheimer Disease (AD) in individuals of African Ancestry, despite evidence suggesting increased risk of AD in the African American (AA) population. We performed whole-genome sequencing (WGS) and multipoint ... ...

Abstract	There is a paucity of genetic studies of Alzheimer Disease (AD) in individuals of African Ancestry, despite evidence suggesting increased risk of AD in the African American (AA) population. We performed whole-genome sequencing (WGS) and multipoint linkage analyses in 51 multi-generational AA AD families ascertained through the Research in African American Alzheimer Disease Initiative (REAAADI) and the National Institute on Aging Late Onset Alzheimer's disease (NIA-LOAD) Family Based Study. Variants were prioritized on minor allele frequency (<0.01), functional potential of coding and noncoding variants, co-segregation with AD and presence in multi-ancestry ADSP release 3 WGS data. We identified a significant linkage signal on chromosome 5q35 (HLOD=3.3) driven by nine families. Haplotype segregation analysis in the family with highest LOD score identified a 3'UTR variant in INSYN2B with the most functional evidence. Four other linked AA families harbor within-family shared variants located in INSYN2B's promoter or enhancer regions. This AA family-based finding shows the importance of diversifying population-level genetic data to better understand the genetic determinants of AD on a global scale.
MeSH term(s)	Humans ; Alzheimer Disease/genetics ; Alzheimer Disease/epidemiology ; Lod Score ; Genetic Linkage/genetics ; Haplotypes ; Chromosomes ; Genetic Predisposition to Disease/genetics
Language	English
Publishing date	2023-10-31
Publishing country	United States
Document type	Journal Article
ZDB-ID	604505-4
ISSN	1558-1497 ; 0197-4580
ISSN (online)	1558-1497
ISSN	0197-4580
DOI	10.1016/j.neurobiolaging.2023.10.010
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Article: INCREASED RISK OF CHILDHOOD BRAIN TUMORS AMONG CHILDREN WHOSE PARENTS HAD FARM-RELATED PESTICIDE EXPOSURES DURING PREGNANCY.

Kunkle, Brian / Bae, S / Singh, K P / Roy, D

JP journal of biostatistics

2015 Volume 11, Issue 2, Page(s) 89–101

Abstract: Malignant brain tumors rank second in both incidence and mortality by cancer in children, and they are the leading cause of cancer death in children. Relatively little is known about the etiology of childhood brain tumor (CBT). While there are several ... ...

Abstract	Malignant brain tumors rank second in both incidence and mortality by cancer in children, and they are the leading cause of cancer death in children. Relatively little is known about the etiology of childhood brain tumor (CBT). While there are several studies which link pesticide exposure to increased risk of CBT, findings have been inconsistent. We performed a meta-analysis on 15 published epidemiological studies to test that in utero exposure to pesticides may be involved in the development of brain cancer in children. Meta-analysis was performed using the general variance-based method and homogeneity was tested by means of the Q statistic. Summary relative risk (RR) estimates were calculated for childhood brain cancer from (1) paternal exposure to pesticides prior to conception, (2) both maternal and paternal exposure to pesticides during pregnancy, (3) maternal exposure during pregnancy to: (a) agricultural and (b) non-agricultural activities, and (4) childhood exposure to: (a) agricultural and (b) nonagricultural activities up to date of diagnosis with CBT. The comparative toxicogenomics database (CTD) was used to identify gene-pesticide-CBT interactions. Findings of meta-analyses revealed a significantly increased risk of CBT among children whose mothers had farm-related exposures during pregnancy (RR=1.48, 95% CI=1.18-1.84). A dose response was recognized when this risk estimate was compared to those for risk of CBT from maternal exposure to non-agricultural pesticides (e.g., home extermination, pest strips) during pregnancy (RR=1.36, 1.10-1.68), and risk of CBT among children exposed to agricultural activities (RR=1.32, 1.04-1.67). Three studies combined for the paternal exposure to pesticides during preconception produced a calculated summary risk estimate of odds ratio (OR) = 2.29 (95% CI: 1.39-3.78). Meta-analysis of five studies of paternal exposure to pesticides during pregnancy produced a final calculated summary risk estimate of OR = 1.63 (95% CI: 1.16-2.31). The search of the CTD databases revealed association between herbicide and astrocytoma and more than 300 genes are altered by exposure to herbicide, fungicide, insecticide or pesticides. In summary, comparing results from our categories of exposure, preconception and pregnancy exposure estimates were slightly higher than childhood exposure estimates, paternal exposures produced slightly higher risk estimates compared to maternal exposures, agricultural exposures produced slightly higher risk estimates compared to non-agricultural exposures and CTD search revealed potential genes-pesticides-astrocytoma interactions. Based on the collective results of these meta-analyses, it appears that pesticide exposure may increase risk of CBT, with preconception and prenatal exposures being especially important factors in increasing risk of its development. Interestingly, paternal exposure may be as important, if not more important than maternal exposures, particularly during the preconception period. Whether this is a result of paternal exposures being more prevalent than maternal exposures or the consequence of a biological process, is a question that deserves further attention in future investigations of CBT etiology.
Language	English
Publishing date	2015-07-31
Publishing country	India
Document type	Journal Article
ISSN	0973-5143
ISSN	0973-5143
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Article ; Online: Manifestations of Alzheimer's disease genetic risk in the blood are evident in a multiomic analysis in healthy adults aged 18 to 90.

Heath, Laura / Earls, John C / Magis, Andrew T / Kornilov, Sergey A / Lovejoy, Jennifer C / Funk, Cory C / Rappaport, Noa / Logsdon, Benjamin A / Mangravite, Lara M / Kunkle, Brian W / Martin, Eden R / Naj, Adam C / Ertekin-Taner, Nilüfer / Golde, Todd E / Hood, Leroy / Price, Nathan D

Scientific reports

2022 Volume 12, Issue 1, Page(s) 6117

Abstract: Genetics play an important role in late-onset Alzheimer's Disease (AD) etiology and dozens of genetic variants have been implicated in AD risk through large-scale GWAS meta-analyses. However, the precise mechanistic effects of most of these variants have ...

Abstract	Genetics play an important role in late-onset Alzheimer's Disease (AD) etiology and dozens of genetic variants have been implicated in AD risk through large-scale GWAS meta-analyses. However, the precise mechanistic effects of most of these variants have yet to be determined. Deeply phenotyped cohort data can reveal physiological changes associated with genetic risk for AD across an age spectrum that may provide clues to the biology of the disease. We utilized over 2000 high-quality quantitative measurements obtained from blood of 2831 cognitively normal adult clients of a consumer-based scientific wellness company, each with CLIA-certified whole-genome sequencing data. Measurements included: clinical laboratory blood tests, targeted chip-based proteomics, and metabolomics. We performed a phenome-wide association study utilizing this diverse blood marker data and 25 known AD genetic variants and an AD-specific polygenic risk score (PGRS), adjusting for sex, age, vendor (for clinical labs), and the first four genetic principal components; sex-SNP interactions were also assessed. We observed statistically significant SNP-analyte associations for five genetic variants after correction for multiple testing (for SNPs in or near NYAP1, ABCA7, INPP5D, and APOE), with effects detectable from early adulthood. The ABCA7 SNP and the APOE2 and APOE4 encoding alleles were associated with lipid variability, as seen in previous studies; in addition, six novel proteins were associated with the e2 allele. The most statistically significant finding was between the NYAP1 variant and PILRA and PILRB protein levels, supporting previous functional genomic studies in the identification of a putative causal variant within the PILRA gene. We did not observe associations between the PGRS and any analyte. Sex modified the effects of four genetic variants, with multiple interrelated immune-modulating effects associated with the PICALM variant. In post-hoc analysis, sex-stratified GWAS results from an independent AD case-control meta-analysis supported sex-specific disease effects of the PICALM variant, highlighting the importance of sex as a biological variable. Known AD genetic variation influenced lipid metabolism and immune response systems in a population of non-AD individuals, with associations observed from early adulthood onward. Further research is needed to determine whether and how these effects are implicated in early-stage biological pathways to AD. These analyses aim to complement ongoing work on the functional interpretation of AD-associated genetic variants.
MeSH term(s)	ATP-Binding Cassette Transporters/genetics ; Adult ; Alzheimer Disease/genetics ; Apolipoprotein E2/genetics ; Female ; Genetic Predisposition to Disease ; Genome-Wide Association Study ; Genomics ; Humans ; Male ; Polymorphism, Single Nucleotide
Chemical Substances	ATP-Binding Cassette Transporters ; Apolipoprotein E2
Language	English
Publishing date	2022-04-12
Publishing country	England
Document type	Journal Article ; Meta-Analysis ; Research Support, U.S. Gov't, Non-P.H.S. ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2615211-3
ISSN	2045-2322 ; 2045-2322
ISSN (online)	2045-2322
ISSN	2045-2322
DOI	10.1038/s41598-022-09825-2
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