Molecular landscape of the overlap between Alzheimer’s disease and somatic insulin-related diseases

Abstract Alzheimer’s disease (AD) is a multifactorial disease with both genetic and environmental factors contributing to its etiology. Previous evidence has implicated disturbed insulin signaling as a key mechanism that plays a role in both neurodegenerative diseases such as AD and comorbid somatic...

Full description

Saved in:
Bibliographic Details
Main Authors: I. Hyun Ruisch, Joanna Widomska, Ward De Witte, Nina R. Mota, Giuseppe Fanelli, Veerle Van Gils, Willemijn J. Jansen, Stephanie J. B. Vos, Abel Fóthi, Csaba Barta, Simone Berkel, Kazi A. Alam, Aurora Martinez, Jan Haavik, Aet O’Leary, David Slattery, Mairéad Sullivan, Jeffrey Glennon, Jan K. Buitelaar, Janita Bralten, Barbara Franke, Geert Poelmans
Format: Article
Language:English
Published: BMC 2024-10-01
Series:Alzheimer’s Research & Therapy
Online Access:https://doi.org/10.1186/s13195-024-01609-2
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850180006445056000
author I. Hyun Ruisch
Joanna Widomska
Ward De Witte
Nina R. Mota
Giuseppe Fanelli
Veerle Van Gils
Willemijn J. Jansen
Stephanie J. B. Vos
Abel Fóthi
Csaba Barta
Simone Berkel
Kazi A. Alam
Aurora Martinez
Jan Haavik
Aet O’Leary
David Slattery
Mairéad Sullivan
Jeffrey Glennon
Jan K. Buitelaar
Janita Bralten
Barbara Franke
Geert Poelmans
author_facet I. Hyun Ruisch
Joanna Widomska
Ward De Witte
Nina R. Mota
Giuseppe Fanelli
Veerle Van Gils
Willemijn J. Jansen
Stephanie J. B. Vos
Abel Fóthi
Csaba Barta
Simone Berkel
Kazi A. Alam
Aurora Martinez
Jan Haavik
Aet O’Leary
David Slattery
Mairéad Sullivan
Jeffrey Glennon
Jan K. Buitelaar
Janita Bralten
Barbara Franke
Geert Poelmans
author_sort I. Hyun Ruisch
collection DOAJ
description Abstract Alzheimer’s disease (AD) is a multifactorial disease with both genetic and environmental factors contributing to its etiology. Previous evidence has implicated disturbed insulin signaling as a key mechanism that plays a role in both neurodegenerative diseases such as AD and comorbid somatic diseases such as diabetes mellitus type 2 (DM2). In this study, we analysed available genome-wide association studies (GWASs) of AD and somatic insulin-related diseases and conditions (SID), i.e., DM2, metabolic syndrome and obesity, to identify genes associated with both AD and SID that could increase our insights into their molecular underpinnings. We then performed functional enrichment analyses of these genes. Subsequently, using (additional) GWAS data, we conducted shared genetic etiology analyses between AD and SID, on the one hand, and blood and cerebrospinal fluid (CSF) metabolite levels on the other hand. Further, integrating all these analysis results with elaborate literature searches, we built a molecular landscape of the overlap between AD and SID. From the landscape, multiple functional themes emerged, including insulin signaling, estrogen signaling, synaptic transmission, lipid metabolism and tau signaling. We also found shared genetic etiologies between AD/SID and the blood/CSF levels of multiple metabolites, pointing towards “energy metabolism” as a key metabolic pathway that is affected in both AD and SID. Lastly, the landscape provided leads for putative novel drug targets for AD (including MARK4, TMEM219, FKBP5, NDUFS3 and IL34) that could be further developed into new AD treatments.
format Article
id doaj-art-ec15a71192f24d8aaffafb95a2cae7a1
institution OA Journals
issn 1758-9193
language English
publishDate 2024-10-01
publisher BMC
record_format Article
series Alzheimer’s Research & Therapy
spelling doaj-art-ec15a71192f24d8aaffafb95a2cae7a12025-08-20T02:18:20ZengBMCAlzheimer’s Research & Therapy1758-91932024-10-0116111610.1186/s13195-024-01609-2Molecular landscape of the overlap between Alzheimer’s disease and somatic insulin-related diseasesI. Hyun Ruisch0Joanna Widomska1Ward De Witte2Nina R. Mota3Giuseppe Fanelli4Veerle Van Gils5Willemijn J. Jansen6Stephanie J. B. Vos7Abel Fóthi8Csaba Barta9Simone Berkel10Kazi A. Alam11Aurora Martinez12Jan Haavik13Aet O’Leary14David Slattery15Mairéad Sullivan16Jeffrey Glennon17Jan K. Buitelaar18Janita Bralten19Barbara Franke20Geert Poelmans21Department of Cognitive Neuroscience, Radboud University Medical CenterDepartment of Cognitive Neuroscience, Radboud University Medical CenterDepartment of Cognitive Neuroscience, Radboud University Medical CenterDepartment of Human Genetics, Radboud University Medical CenterDepartment of Human Genetics, Radboud University Medical CenterDepartment of Psychiatry & Neuropsychology, Alzheimer Center Limburg, School for Mental Health and Neuroscience, Maastricht UniversityDepartment of Psychiatry & Neuropsychology, Alzheimer Center Limburg, School for Mental Health and Neuroscience, Maastricht UniversityDepartment of Psychiatry & Neuropsychology, Alzheimer Center Limburg, School for Mental Health and Neuroscience, Maastricht UniversityDepartment of Molecular Biology, Institute of Biochemistry and Molecular Biology, Semmelweis UniversityDepartment of Molecular Biology, Institute of Biochemistry and Molecular Biology, Semmelweis UniversityInstitute of Human Genetics, Heidelberg UniversityDepartment of Biomedicine, University of BergenDepartment of Biomedicine, University of BergenDepartment of Biomedicine, University of BergenDepartment of Psychiatry, University HospitalDepartment of Psychiatry, Psychosomatics and Psychotherapy, Goethe-UniversitätConway Institute of Biomedical and Biomolecular Research, School of Medicine, University College DublinConway Institute of Biomedical and Biomolecular Research, School of Medicine, University College DublinDepartment of Cognitive Neuroscience, Radboud University Medical CenterDepartment of Human Genetics, Radboud University Medical CenterDepartment of Cognitive Neuroscience, Radboud University Medical CenterDepartment of Cognitive Neuroscience, Radboud University Medical CenterAbstract Alzheimer’s disease (AD) is a multifactorial disease with both genetic and environmental factors contributing to its etiology. Previous evidence has implicated disturbed insulin signaling as a key mechanism that plays a role in both neurodegenerative diseases such as AD and comorbid somatic diseases such as diabetes mellitus type 2 (DM2). In this study, we analysed available genome-wide association studies (GWASs) of AD and somatic insulin-related diseases and conditions (SID), i.e., DM2, metabolic syndrome and obesity, to identify genes associated with both AD and SID that could increase our insights into their molecular underpinnings. We then performed functional enrichment analyses of these genes. Subsequently, using (additional) GWAS data, we conducted shared genetic etiology analyses between AD and SID, on the one hand, and blood and cerebrospinal fluid (CSF) metabolite levels on the other hand. Further, integrating all these analysis results with elaborate literature searches, we built a molecular landscape of the overlap between AD and SID. From the landscape, multiple functional themes emerged, including insulin signaling, estrogen signaling, synaptic transmission, lipid metabolism and tau signaling. We also found shared genetic etiologies between AD/SID and the blood/CSF levels of multiple metabolites, pointing towards “energy metabolism” as a key metabolic pathway that is affected in both AD and SID. Lastly, the landscape provided leads for putative novel drug targets for AD (including MARK4, TMEM219, FKBP5, NDUFS3 and IL34) that could be further developed into new AD treatments.https://doi.org/10.1186/s13195-024-01609-2
spellingShingle I. Hyun Ruisch
Joanna Widomska
Ward De Witte
Nina R. Mota
Giuseppe Fanelli
Veerle Van Gils
Willemijn J. Jansen
Stephanie J. B. Vos
Abel Fóthi
Csaba Barta
Simone Berkel
Kazi A. Alam
Aurora Martinez
Jan Haavik
Aet O’Leary
David Slattery
Mairéad Sullivan
Jeffrey Glennon
Jan K. Buitelaar
Janita Bralten
Barbara Franke
Geert Poelmans
Molecular landscape of the overlap between Alzheimer’s disease and somatic insulin-related diseases
Alzheimer’s Research & Therapy
title Molecular landscape of the overlap between Alzheimer’s disease and somatic insulin-related diseases
title_full Molecular landscape of the overlap between Alzheimer’s disease and somatic insulin-related diseases
title_fullStr Molecular landscape of the overlap between Alzheimer’s disease and somatic insulin-related diseases
title_full_unstemmed Molecular landscape of the overlap between Alzheimer’s disease and somatic insulin-related diseases
title_short Molecular landscape of the overlap between Alzheimer’s disease and somatic insulin-related diseases
title_sort molecular landscape of the overlap between alzheimer s disease and somatic insulin related diseases
url https://doi.org/10.1186/s13195-024-01609-2
work_keys_str_mv AT ihyunruisch molecularlandscapeoftheoverlapbetweenalzheimersdiseaseandsomaticinsulinrelateddiseases
AT joannawidomska molecularlandscapeoftheoverlapbetweenalzheimersdiseaseandsomaticinsulinrelateddiseases
AT warddewitte molecularlandscapeoftheoverlapbetweenalzheimersdiseaseandsomaticinsulinrelateddiseases
AT ninarmota molecularlandscapeoftheoverlapbetweenalzheimersdiseaseandsomaticinsulinrelateddiseases
AT giuseppefanelli molecularlandscapeoftheoverlapbetweenalzheimersdiseaseandsomaticinsulinrelateddiseases
AT veerlevangils molecularlandscapeoftheoverlapbetweenalzheimersdiseaseandsomaticinsulinrelateddiseases
AT willemijnjjansen molecularlandscapeoftheoverlapbetweenalzheimersdiseaseandsomaticinsulinrelateddiseases
AT stephaniejbvos molecularlandscapeoftheoverlapbetweenalzheimersdiseaseandsomaticinsulinrelateddiseases
AT abelfothi molecularlandscapeoftheoverlapbetweenalzheimersdiseaseandsomaticinsulinrelateddiseases
AT csababarta molecularlandscapeoftheoverlapbetweenalzheimersdiseaseandsomaticinsulinrelateddiseases
AT simoneberkel molecularlandscapeoftheoverlapbetweenalzheimersdiseaseandsomaticinsulinrelateddiseases
AT kaziaalam molecularlandscapeoftheoverlapbetweenalzheimersdiseaseandsomaticinsulinrelateddiseases
AT auroramartinez molecularlandscapeoftheoverlapbetweenalzheimersdiseaseandsomaticinsulinrelateddiseases
AT janhaavik molecularlandscapeoftheoverlapbetweenalzheimersdiseaseandsomaticinsulinrelateddiseases
AT aetoleary molecularlandscapeoftheoverlapbetweenalzheimersdiseaseandsomaticinsulinrelateddiseases
AT davidslattery molecularlandscapeoftheoverlapbetweenalzheimersdiseaseandsomaticinsulinrelateddiseases
AT maireadsullivan molecularlandscapeoftheoverlapbetweenalzheimersdiseaseandsomaticinsulinrelateddiseases
AT jeffreyglennon molecularlandscapeoftheoverlapbetweenalzheimersdiseaseandsomaticinsulinrelateddiseases
AT jankbuitelaar molecularlandscapeoftheoverlapbetweenalzheimersdiseaseandsomaticinsulinrelateddiseases
AT janitabralten molecularlandscapeoftheoverlapbetweenalzheimersdiseaseandsomaticinsulinrelateddiseases
AT barbarafranke molecularlandscapeoftheoverlapbetweenalzheimersdiseaseandsomaticinsulinrelateddiseases
AT geertpoelmans molecularlandscapeoftheoverlapbetweenalzheimersdiseaseandsomaticinsulinrelateddiseases