Multi-omics and pathway analyses of genome-wide associations implicate regulation and immunity in verbal declarative memory performance
Abstract Background Uncovering the functional relevance underlying verbal declarative memory (VDM) genome-wide association study (GWAS) results may facilitate the development of interventions to reduce age-related memory decline and dementia. Methods We performed multi-omics and pathway enrichment a...
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| Format: | Article |
| Language: | English |
| Published: |
BMC
2024-01-01
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| Series: | Alzheimer’s Research & Therapy |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s13195-023-01376-6 |
| _version_ | 1797350056283602944 |
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| author | Hao Mei Jeannette Simino Lianna Li Fan Jiang Joshua C. Bis Gail Davies W David Hill Charley Xia Vilmundur Gudnason Qiong Yang Jari Lahti Jennifer A. Smith Mirna Kirin Philip De Jager Nicola J. Armstrong Mohsen Ghanbari Ivana Kolcic Christopher Moran Alexander Teumer Murali Sargurupremraj Shamsed Mahmud Myriam Fornage Wei Zhao Claudia L. Satizabal Ozren Polasek Katri Räikkönen David C. Liewald Georg Homuth Michele Callisaya Karen A. Mather B. Gwen Windham Tatijana Zemunik Aarno Palotie Alison Pattie Sandra van der Auwera Anbupalam Thalamuthu David S. Knopman Igor Rudan John M. Starr Katharina Wittfeld Nicole A. Kochan Michael E. Griswold Veronique Vitart Henry Brodaty Rebecca Gottesman Simon R. Cox Bruce M. Psaty Eric Boerwinkle Daniel I. Chasman Francine Grodstein Perminder S. Sachdev Velandai Srikanth Caroline Hayward James F. Wilson Johan G. Eriksson Sharon L. R. Kardia Hans J. Grabe David A. Bennett M. Arfan Ikram Ian J. Deary Cornelia M. van Duijn Lenore Launer Annette L. Fitzpatrick Sudha Seshadri Jan Bressler Stephanie Debette Thomas H. Mosley |
| author_facet | Hao Mei Jeannette Simino Lianna Li Fan Jiang Joshua C. Bis Gail Davies W David Hill Charley Xia Vilmundur Gudnason Qiong Yang Jari Lahti Jennifer A. Smith Mirna Kirin Philip De Jager Nicola J. Armstrong Mohsen Ghanbari Ivana Kolcic Christopher Moran Alexander Teumer Murali Sargurupremraj Shamsed Mahmud Myriam Fornage Wei Zhao Claudia L. Satizabal Ozren Polasek Katri Räikkönen David C. Liewald Georg Homuth Michele Callisaya Karen A. Mather B. Gwen Windham Tatijana Zemunik Aarno Palotie Alison Pattie Sandra van der Auwera Anbupalam Thalamuthu David S. Knopman Igor Rudan John M. Starr Katharina Wittfeld Nicole A. Kochan Michael E. Griswold Veronique Vitart Henry Brodaty Rebecca Gottesman Simon R. Cox Bruce M. Psaty Eric Boerwinkle Daniel I. Chasman Francine Grodstein Perminder S. Sachdev Velandai Srikanth Caroline Hayward James F. Wilson Johan G. Eriksson Sharon L. R. Kardia Hans J. Grabe David A. Bennett M. Arfan Ikram Ian J. Deary Cornelia M. van Duijn Lenore Launer Annette L. Fitzpatrick Sudha Seshadri Jan Bressler Stephanie Debette Thomas H. Mosley |
| author_sort | Hao Mei |
| collection | DOAJ |
| description | Abstract Background Uncovering the functional relevance underlying verbal declarative memory (VDM) genome-wide association study (GWAS) results may facilitate the development of interventions to reduce age-related memory decline and dementia. Methods We performed multi-omics and pathway enrichment analyses of paragraph (PAR-dr) and word list (WL-dr) delayed recall GWAS from 29,076 older non-demented individuals of European descent. We assessed the relationship between single-variant associations and expression quantitative trait loci (eQTLs) in 44 tissues and methylation quantitative trait loci (meQTLs) in the hippocampus. We determined the relationship between gene associations and transcript levels in 53 tissues, annotation as immune genes, and regulation by transcription factors (TFs) and microRNAs. To identify significant pathways, gene set enrichment was tested in each cohort and meta-analyzed across cohorts. Analyses of differential expression in brain tissues were conducted for pathway component genes. Results The single-variant associations of VDM showed significant linkage disequilibrium (LD) with eQTLs across all tissues and meQTLs within the hippocampus. Stronger WL-dr gene associations correlated with reduced expression in four brain tissues, including the hippocampus. More robust PAR-dr and/or WL-dr gene associations were intricately linked with immunity and were influenced by 31 TFs and 2 microRNAs. Six pathways, including type I diabetes, exhibited significant associations with both PAR-dr and WL-dr. These pathways included fifteen MHC genes intricately linked to VDM performance, showing diverse expression patterns based on cognitive status in brain tissues. Conclusions VDM genetic associations influence expression regulation via eQTLs and meQTLs. The involvement of TFs, microRNAs, MHC genes, and immune-related pathways contributes to VDM performance in older individuals. |
| first_indexed | 2024-03-08T12:39:18Z |
| format | Article |
| id | doaj.art-50a19bd7fce542089e5527e952a66f90 |
| institution | Directory Open Access Journal |
| issn | 1758-9193 |
| language | English |
| last_indexed | 2024-03-08T12:39:18Z |
| publishDate | 2024-01-01 |
| publisher | BMC |
| record_format | Article |
| series | Alzheimer’s Research & Therapy |
| spelling | doaj.art-50a19bd7fce542089e5527e952a66f902024-01-21T12:13:11ZengBMCAlzheimer’s Research & Therapy1758-91932024-01-0116111510.1186/s13195-023-01376-6Multi-omics and pathway analyses of genome-wide associations implicate regulation and immunity in verbal declarative memory performanceHao Mei0Jeannette Simino1Lianna Li2Fan Jiang3Joshua C. Bis4Gail Davies5W David Hill6Charley Xia7Vilmundur Gudnason8Qiong Yang9Jari Lahti10Jennifer A. Smith11Mirna Kirin12Philip De Jager13Nicola J. Armstrong14Mohsen Ghanbari15Ivana Kolcic16Christopher Moran17Alexander Teumer18Murali Sargurupremraj19Shamsed Mahmud20Myriam Fornage21Wei Zhao22Claudia L. Satizabal23Ozren Polasek24Katri Räikkönen25David C. Liewald26Georg Homuth27Michele Callisaya28Karen A. Mather29B. Gwen Windham30Tatijana Zemunik31Aarno Palotie32Alison Pattie33Sandra van der Auwera34Anbupalam Thalamuthu35David S. Knopman36Igor Rudan37John M. Starr38Katharina Wittfeld39Nicole A. Kochan40Michael E. Griswold41Veronique Vitart42Henry Brodaty43Rebecca Gottesman44Simon R. Cox45Bruce M. Psaty46Eric Boerwinkle47Daniel I. Chasman48Francine Grodstein49Perminder S. Sachdev50Velandai Srikanth51Caroline Hayward52James F. Wilson53Johan G. Eriksson54Sharon L. R. Kardia55Hans J. Grabe56David A. Bennett57M. Arfan Ikram58Ian J. Deary59Cornelia M. van Duijn60Lenore Launer61Annette L. Fitzpatrick62Sudha Seshadri63Jan Bressler64Stephanie Debette65Thomas H. Mosley66Department of Data Science, John D. Bower School of Population Health, University of Mississippi Medical CenterDepartment of Data Science, John D. Bower School of Population Health, University of Mississippi Medical CenterDepartment of Biology, Tougaloo CollegeShanghai Children’s Medical Center, Shanghai Jiao Tong University School of MedicineDepartment of Medicine, Cardiovascular Health Research Unit, University of WashingtonDepartment of Psychology, Lothian Birth Cohorts Group, University of EdinburghDepartment of Psychology, Lothian Birth Cohorts Group, University of EdinburghDepartment of Psychology, Lothian Birth Cohorts Group, University of EdinburghIcelandic Heart AssociationDepartment of Biostatistics, Boston University School of Public HealthTurku Institute for Advanced Research, University of TurkuDepartment of Epidemiology, School of Public Health, University of MichiganWork completed while at The University of EdinburghTaub Institute for Research On Alzheimer’s Disease and the Aging Brain, Columbia Irving University Medical CenterMathematics and Statistics, Curtin UniversityDepartment of Epidemiology, Erasmus Medical Center University Medical CenterSchool of Medicine, University of SplitDepartment of Geriatric Medicine, Frankston Hospital, Peninsula HealthInstitute for Community Medicine, University Medicine GreifswaldInserm, Bordeaux Population Health Research Center, Team VINTAGE, UMR 1219, University of BordeauxDepartment of Data Science, John D. Bower School of Population Health, University of Mississippi Medical CenterThe Brown Foundation Institute of Molecular Medicine for the Prevention of Human Diseases, McGovern Medical School, University of Texas Health Science Center at HoustonDepartment of Epidemiology, School of Public Health, University of MichiganThe University of Texas Health Science Center at San AntonioSchool of Medicine, University of SplitDepartment of Psychology and Logopedics, Faculty of Medicine, University of HelsinkiDepartment of Psychology, Lothian Birth Cohorts Group, University of EdinburghInterfaculty Institute for Genetics and Functional Genomics, University Medicine GreifswaldPeninsula Clinical School, Central Clinical School, Monash UniversityCentre for Healthy Brain Ageing, School of Psychiatry, University of New South WalesGertrude C. Ford Memory Impairment and Neurodegenerative Dementia (MIND) Center, University of Mississippi Medical CenterSchool of Medicine, University of SplitDepartment of Medicine, Department of Neurology and Department of Psychiatry, Analytic and Translational Genetics Unit, Massachusetts General HospitalDepartment of Psychology, Lothian Birth Cohorts Group, University of EdinburghDepartment of Psychiatry and Psychotherapy, University Medicine GreifswaldCentre for Healthy Brain Ageing, School of Psychiatry, University of New South WalesDepartment of Neurology, Mayo ClinicCentre for Global Health Research, Usher Institute, University of EdinburghDepartment of Psychology, Lothian Birth Cohorts Group, University of EdinburghDepartment of Psychiatry and Psychotherapy, University Medicine GreifswaldCentre for Healthy Brain Ageing, School of Psychiatry, University of New South WalesGertrude C. Ford Memory Impairment and Neurodegenerative Dementia (MIND) Center, University of Mississippi Medical CenterMedical Research Council Human Genetics Unit, Institute of Genetics and Cancer, University of EdinburghCentre for Healthy Brain Ageing, School of Psychiatry, University of New South WalesStroke, Cognition, and Neuroepidemiology (SCAN) Section, National Institute of Neurological Disorders and Stroke, National Institutes of HealthDepartment of Psychology, Lothian Birth Cohorts Group, University of EdinburghDepartment of Medicine, Cardiovascular Health Research Unit, University of WashingtonHuman Genetics Center, School of Public Health, University of Texas Health Science Center at HoustonHarvard Medical SchoolDepartment of Medicine, Channing Division of Network Medicine, Brigham and Women’s Hospital, Harvard Medical SchoolCentre for Healthy Brain Ageing, School of Psychiatry, University of New South WalesDepartment of Geriatric Medicine, Frankston Hospital, Peninsula HealthMedical Research Council Human Genetics Unit, Institute of Genetics and Cancer, University of EdinburghCentre for Global Health Research, Usher Institute, University of EdinburghDepartment of General Practice and Primary Health Care, University of Helsinki and Helsinki University HospitalDepartment of Epidemiology, School of Public Health, University of MichiganDepartment of Psychiatry and Psychotherapy, University Medicine GreifswaldRush Alzheimer’s Disease Center, Rush University Medical CenterDepartment of Epidemiology, Erasmus Medical Center University Medical CenterDepartment of Psychology, Lothian Birth Cohorts Group, University of EdinburghNuffield Department of Population Health, Medical Sciences Division, University of OxfordLaboratory of Epidemiology and Population Sciences, National Institute On AgingDepartment of Epidemiology, University of WashingtonThe National Heart Lung and Blood Institute’s Framingham Heart StudyHuman Genetics Center, School of Public Health, University of Texas Health Science Center at HoustonInserm, Bordeaux Population Health Research Center, Team VINTAGE, UMR 1219, University of BordeauxGertrude C. Ford Memory Impairment and Neurodegenerative Dementia (MIND) Center, University of Mississippi Medical CenterAbstract Background Uncovering the functional relevance underlying verbal declarative memory (VDM) genome-wide association study (GWAS) results may facilitate the development of interventions to reduce age-related memory decline and dementia. Methods We performed multi-omics and pathway enrichment analyses of paragraph (PAR-dr) and word list (WL-dr) delayed recall GWAS from 29,076 older non-demented individuals of European descent. We assessed the relationship between single-variant associations and expression quantitative trait loci (eQTLs) in 44 tissues and methylation quantitative trait loci (meQTLs) in the hippocampus. We determined the relationship between gene associations and transcript levels in 53 tissues, annotation as immune genes, and regulation by transcription factors (TFs) and microRNAs. To identify significant pathways, gene set enrichment was tested in each cohort and meta-analyzed across cohorts. Analyses of differential expression in brain tissues were conducted for pathway component genes. Results The single-variant associations of VDM showed significant linkage disequilibrium (LD) with eQTLs across all tissues and meQTLs within the hippocampus. Stronger WL-dr gene associations correlated with reduced expression in four brain tissues, including the hippocampus. More robust PAR-dr and/or WL-dr gene associations were intricately linked with immunity and were influenced by 31 TFs and 2 microRNAs. Six pathways, including type I diabetes, exhibited significant associations with both PAR-dr and WL-dr. These pathways included fifteen MHC genes intricately linked to VDM performance, showing diverse expression patterns based on cognitive status in brain tissues. Conclusions VDM genetic associations influence expression regulation via eQTLs and meQTLs. The involvement of TFs, microRNAs, MHC genes, and immune-related pathways contributes to VDM performance in older individuals.https://doi.org/10.1186/s13195-023-01376-6Genome-wide association studyMemoryExpressionImmunityMulti-omicsDelayed recall |
| spellingShingle | Hao Mei Jeannette Simino Lianna Li Fan Jiang Joshua C. Bis Gail Davies W David Hill Charley Xia Vilmundur Gudnason Qiong Yang Jari Lahti Jennifer A. Smith Mirna Kirin Philip De Jager Nicola J. Armstrong Mohsen Ghanbari Ivana Kolcic Christopher Moran Alexander Teumer Murali Sargurupremraj Shamsed Mahmud Myriam Fornage Wei Zhao Claudia L. Satizabal Ozren Polasek Katri Räikkönen David C. Liewald Georg Homuth Michele Callisaya Karen A. Mather B. Gwen Windham Tatijana Zemunik Aarno Palotie Alison Pattie Sandra van der Auwera Anbupalam Thalamuthu David S. Knopman Igor Rudan John M. Starr Katharina Wittfeld Nicole A. Kochan Michael E. Griswold Veronique Vitart Henry Brodaty Rebecca Gottesman Simon R. Cox Bruce M. Psaty Eric Boerwinkle Daniel I. Chasman Francine Grodstein Perminder S. Sachdev Velandai Srikanth Caroline Hayward James F. Wilson Johan G. Eriksson Sharon L. R. Kardia Hans J. Grabe David A. Bennett M. Arfan Ikram Ian J. Deary Cornelia M. van Duijn Lenore Launer Annette L. Fitzpatrick Sudha Seshadri Jan Bressler Stephanie Debette Thomas H. Mosley Multi-omics and pathway analyses of genome-wide associations implicate regulation and immunity in verbal declarative memory performance Alzheimer’s Research & Therapy Genome-wide association study Memory Expression Immunity Multi-omics Delayed recall |
| title | Multi-omics and pathway analyses of genome-wide associations implicate regulation and immunity in verbal declarative memory performance |
| title_full | Multi-omics and pathway analyses of genome-wide associations implicate regulation and immunity in verbal declarative memory performance |
| title_fullStr | Multi-omics and pathway analyses of genome-wide associations implicate regulation and immunity in verbal declarative memory performance |
| title_full_unstemmed | Multi-omics and pathway analyses of genome-wide associations implicate regulation and immunity in verbal declarative memory performance |
| title_short | Multi-omics and pathway analyses of genome-wide associations implicate regulation and immunity in verbal declarative memory performance |
| title_sort | multi omics and pathway analyses of genome wide associations implicate regulation and immunity in verbal declarative memory performance |
| topic | Genome-wide association study Memory Expression Immunity Multi-omics Delayed recall |
| url | https://doi.org/10.1186/s13195-023-01376-6 |
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