Alzheimer's disease‐associated CD83(+) microglia are linked with increased immunoglobulin G4 and human cytomegalovirus in the gut, vagal nerve, and brain

INTRODUCTION While there may be microbial contributions to Alzheimer's disease (AD), findings have been inconclusive. We recently reported an AD‐associated CD83(+) microglia subtype associated with increased immunoglobulin G4 (IgG4) in the transverse colon (TC). METHODS We used immunohistochemi...

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Published inAlzheimer's & dementia Vol. 21; no. 1; pp. e14401 - n/a
Main Authors Readhead, Benjamin P., Mastroeni, Diego F., Wang, Qi, Sierra, Maria A., Ávila, Camila, Jimoh, Tajudeen O., Haure‐Mirande, Jean‐Vianney, Atanasoff, Kristina E., Nolz, Jennifer, Suazo, Crystal, Barton, Nathaniel J., Orszulak, Adrian R., Chigas, Samantha M., Tran, Khanh, Mirza, Anne, Ryon, Krista, Proszynski, Jacqueline, Najjar, Deena, Dudley, Joel T., Liu, Sean T. H., Gandy, Sam, Ehrlich, Michelle E., Alsop, Eric, Antone, Jerry, Reiman, Rebecca, Funk, Cory, Best, Rebecca L., Jhatro, Michael, Kamath, Kathy, Shon, John, Kowalik, Timothy F., Bennett, David A., Liang, Winnie S., Serrano, Geidy E., Beach, Thomas G., Van Keuren‐Jensen, Kendall, Mason, Christopher E., Chan, Yingleong, Lim, Elaine T., Tortorella, Domenico, Reiman, Eric M.
Format Journal Article
LanguageEnglish
Published United States John Wiley and Sons Inc 01.01.2025
Subjects
Aged
Aged, 80 and over
Alzheimer Disease - immunology
Alzheimer Disease - metabolism
Alzheimer Disease - pathology
Alzheimer Disease - virology
Alzheimer's disease
antibody epitope repertoire analysis
Antigens, CD - metabolism
Brain - immunology
Brain - metabolism
Brain - pathology
Brain - virology
CD83 Antigen
CD83(+) microglia
cerebrospinal fluid
Cytomegalovirus - immunology
Cytomegalovirus Infections - immunology
Female
human cytomegalovirus
Humans
Immunoglobulin G - cerebrospinal fluid
Immunoglobulin G - metabolism
immunoglobulin G4
Immunoglobulins - metabolism
immunohistochemistry
Male
Membrane Glycoproteins - metabolism
Microglia - immunology
Microglia - metabolism
prefrontal cortex
superior frontal gyrus
transverse colon
vagus nerve
Vagus Nerve - immunology
Vagus Nerve - metabolism
Vagus Nerve - virology
viral infection
transverse colon
vagus nerve
viral infection
CD83(+) microglia
prefrontal cortex
cerebrospinal fluid
antibody epitope repertoire analysis
immunohistochemistry
Alzheimer's disease
human cytomegalovirus
immunoglobulin G4
superior frontal gyrus
Online AccessGet full text
ISSN1552-5260
1552-5279
1552-5279
DOI10.1002/alz.14401

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Abstract INTRODUCTION While there may be microbial contributions to Alzheimer's disease (AD), findings have been inconclusive. We recently reported an AD‐associated CD83(+) microglia subtype associated with increased immunoglobulin G4 (IgG4) in the transverse colon (TC). METHODS We used immunohistochemistry (IHC), IgG4 repertoire profiling, and brain organoid experiments to explore this association. RESULTS CD83(+) microglia in the superior frontal gyrus (SFG) are associated with elevated IgG4 and human cytomegalovirus (HCMV) in the TC, anti‐HCMV IgG4 in cerebrospinal fluid, and both HCMV and IgG4 in the SFG and vagal nerve. This association was replicated in an independent AD cohort. HCMV‐infected cerebral organoids showed accelerated AD pathophysiological features (Aβ42 and pTau‐212) and neuronal death. DISCUSSION Findings indicate complex, cross‐tissue interactions between HCMV and the adaptive immune response associated with CD83(+) microglia in persons with AD. This may indicate an opportunity for antiviral therapy in persons with AD and biomarker evidence of HCMV, IgG4, or CD83(+) microglia. Highlights Cross‐tissue interaction between HCMV and the adaptive immune response in a subset of persons with AD. Presence of CD83(+) microglial associated with IgG4 and HCMV in the gut. CD83(+) microglia are also associated presence of HCMV and IgG4 in the cortex and vagal nerve. Replication of key association in an independent cohort of AD subjects. HCMV infection of cerebral organoids accelerates the production of AD neuropathological features.
AbstractList INTRODUCTION While there may be microbial contributions to Alzheimer's disease (AD), findings have been inconclusive. We recently reported an AD‐associated CD83(+) microglia subtype associated with increased immunoglobulin G4 (IgG4) in the transverse colon (TC). METHODS We used immunohistochemistry (IHC), IgG4 repertoire profiling, and brain organoid experiments to explore this association. RESULTS CD83(+) microglia in the superior frontal gyrus (SFG) are associated with elevated IgG4 and human cytomegalovirus (HCMV) in the TC, anti‐HCMV IgG4 in cerebrospinal fluid, and both HCMV and IgG4 in the SFG and vagal nerve. This association was replicated in an independent AD cohort. HCMV‐infected cerebral organoids showed accelerated AD pathophysiological features (Aβ42 and pTau‐212) and neuronal death. DISCUSSION Findings indicate complex, cross‐tissue interactions between HCMV and the adaptive immune response associated with CD83(+) microglia in persons with AD. This may indicate an opportunity for antiviral therapy in persons with AD and biomarker evidence of HCMV, IgG4, or CD83(+) microglia. Highlights Cross‐tissue interaction between HCMV and the adaptive immune response in a subset of persons with AD. Presence of CD83(+) microglial associated with IgG4 and HCMV in the gut. CD83(+) microglia are also associated presence of HCMV and IgG4 in the cortex and vagal nerve. Replication of key association in an independent cohort of AD subjects. HCMV infection of cerebral organoids accelerates the production of AD neuropathological features.
While there may be microbial contributions to Alzheimer's disease (AD), findings have been inconclusive. We recently reported an AD-associated CD83(+) microglia subtype associated with increased immunoglobulin G4 (IgG4) in the transverse colon (TC).INTRODUCTIONWhile there may be microbial contributions to Alzheimer's disease (AD), findings have been inconclusive. We recently reported an AD-associated CD83(+) microglia subtype associated with increased immunoglobulin G4 (IgG4) in the transverse colon (TC).We used immunohistochemistry (IHC), IgG4 repertoire profiling, and brain organoid experiments to explore this association.METHODSWe used immunohistochemistry (IHC), IgG4 repertoire profiling, and brain organoid experiments to explore this association.CD83(+) microglia in the superior frontal gyrus (SFG) are associated with elevated IgG4 and human cytomegalovirus (HCMV) in the TC, anti-HCMV IgG4 in cerebrospinal fluid, and both HCMV and IgG4 in the SFG and vagal nerve. This association was replicated in an independent AD cohort. HCMV-infected cerebral organoids showed accelerated AD pathophysiological features (Aβ42 and pTau-212) and neuronal death.RESULTSCD83(+) microglia in the superior frontal gyrus (SFG) are associated with elevated IgG4 and human cytomegalovirus (HCMV) in the TC, anti-HCMV IgG4 in cerebrospinal fluid, and both HCMV and IgG4 in the SFG and vagal nerve. This association was replicated in an independent AD cohort. HCMV-infected cerebral organoids showed accelerated AD pathophysiological features (Aβ42 and pTau-212) and neuronal death.Findings indicate complex, cross-tissue interactions between HCMV and the adaptive immune response associated with CD83(+) microglia in persons with AD. This may indicate an opportunity for antiviral therapy in persons with AD and biomarker evidence of HCMV, IgG4, or CD83(+) microglia.DISCUSSIONFindings indicate complex, cross-tissue interactions between HCMV and the adaptive immune response associated with CD83(+) microglia in persons with AD. This may indicate an opportunity for antiviral therapy in persons with AD and biomarker evidence of HCMV, IgG4, or CD83(+) microglia.Cross-tissue interaction between HCMV and the adaptive immune response in a subset of persons with AD. Presence of CD83(+) microglial associated with IgG4 and HCMV in the gut. CD83(+) microglia are also associated presence of HCMV and IgG4 in the cortex and vagal nerve. Replication of key association in an independent cohort of AD subjects. HCMV infection of cerebral organoids accelerates the production of AD neuropathological features.HIGHLIGHTSCross-tissue interaction between HCMV and the adaptive immune response in a subset of persons with AD. Presence of CD83(+) microglial associated with IgG4 and HCMV in the gut. CD83(+) microglia are also associated presence of HCMV and IgG4 in the cortex and vagal nerve. Replication of key association in an independent cohort of AD subjects. HCMV infection of cerebral organoids accelerates the production of AD neuropathological features.
While there may be microbial contributions to Alzheimer's disease (AD), findings have been inconclusive. We recently reported an AD-associated CD83(+) microglia subtype associated with increased immunoglobulin G4 (IgG4) in the transverse colon (TC). We used immunohistochemistry (IHC), IgG4 repertoire profiling, and brain organoid experiments to explore this association. CD83(+) microglia in the superior frontal gyrus (SFG) are associated with elevated IgG4 and human cytomegalovirus (HCMV) in the TC, anti-HCMV IgG4 in cerebrospinal fluid, and both HCMV and IgG4 in the SFG and vagal nerve. This association was replicated in an independent AD cohort. HCMV-infected cerebral organoids showed accelerated AD pathophysiological features (Aβ42 and pTau-212) and neuronal death. Findings indicate complex, cross-tissue interactions between HCMV and the adaptive immune response associated with CD83(+) microglia in persons with AD. This may indicate an opportunity for antiviral therapy in persons with AD and biomarker evidence of HCMV, IgG4, or CD83(+) microglia. Cross-tissue interaction between HCMV and the adaptive immune response in a subset of persons with AD. Presence of CD83(+) microglial associated with IgG4 and HCMV in the gut. CD83(+) microglia are also associated presence of HCMV and IgG4 in the cortex and vagal nerve. Replication of key association in an independent cohort of AD subjects. HCMV infection of cerebral organoids accelerates the production of AD neuropathological features.
Author Kamath, Kathy
Mastroeni, Diego F.
Best, Rebecca L.
Suazo, Crystal
Jimoh, Tajudeen O.
Gandy, Sam
Liang, Winnie S.
Atanasoff, Kristina E.
Serrano, Geidy E.
Jhatro, Michael
Chan, Yingleong
Reiman, Eric M.
Ávila, Camila
Ehrlich, Michelle E.
Sierra, Maria A.
Haure‐Mirande, Jean‐Vianney
Barton, Nathaniel J.
Shon, John
Orszulak, Adrian R.
Kowalik, Timothy F.
Funk, Cory
Proszynski, Jacqueline
Alsop, Eric
Reiman, Rebecca
Bennett, David A.
Mason, Christopher E.
Nolz, Jennifer
Tortorella, Domenico
Antone, Jerry
Liu, Sean T. H.
Mirza, Anne
Tran, Khanh
Van Keuren‐Jensen, Kendall
Ryon, Krista
Readhead, Benjamin P.
Wang, Qi
Najjar, Deena
Dudley, Joel T.
Beach, Thomas G.
Chigas, Samantha M.
Lim, Elaine T.
AuthorAffiliation 7 Department of Microbiology and Physiological Systems University of Massachusetts Chan Medical School Worcester Massachusetts USA
9 Division of Infectious Diseases Icahn School of Medicine at Mount Sinai New York New York USA
14 Civin Laboratory for Neuropathology Banner Sun Health Research Institute Sun City Arizona USA
12 Serimmune, Inc Goleta California USA
1 ASU‐Banner Neurodegenerative Disease Research Center Arizona State University Tempe Arizona USA
6 Department of Genomics and Computational Biology University of Massachusetts Chan Medical School Worcester Massachusetts USA
5 Department of Neurology University of Massachusetts Chan Medical School Worcester Massachusetts USA
16 Banner Alzheimer's Institute Phoenix Arizona USA
11 Institute for Systems Biology Seattle Washington USA
8 Department of Physiology and Biophysics Weill Cornell Medicine New York New York USA
13 Rush Alzheimer's Disease Center Rush University Medical Center Chicago Illinois USA
10 Division of Neurogenomics The Trans
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Copyright 2024 The Author(s). published by Wiley Periodicals LLC on behalf of Alzheimer's Association.
2024 The Author(s). Alzheimer's & Dementia published by Wiley Periodicals LLC on behalf of Alzheimer's Association.
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ID FETCH-LOGICAL-c3761-1fcad9781343e2636b4a8870423f8e2d17b0e787984f5b634d1a3526584862f33
IEDL.DBID 24P
ISSN 1552-5260
1552-5279
IngestDate Thu Aug 21 18:40:20 EDT 2025
Mon Jul 21 09:54:20 EDT 2025
Mon Jul 21 02:03:39 EDT 2025
Sun Jul 06 05:02:12 EDT 2025
Wed Feb 12 09:21:48 EST 2025
IsDoiOpenAccess true
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Issue 1
Keywords transverse colon
vagus nerve
viral infection
CD83(+) microglia
prefrontal cortex
cerebrospinal fluid
antibody epitope repertoire analysis
immunohistochemistry
Alzheimer's disease
human cytomegalovirus
immunoglobulin G4
superior frontal gyrus
Language English
License Attribution
2024 The Author(s). Alzheimer's & Dementia published by Wiley Periodicals LLC on behalf of Alzheimer's Association.
This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-c3761-1fcad9781343e2636b4a8870423f8e2d17b0e787984f5b634d1a3526584862f33
Notes Benjamin P. Readhead and Diego F. Mastroeni contributed equally
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content type line 23
OpenAccessLink https://onlinelibrary.wiley.com/doi/abs/10.1002%2Falz.14401
PMID 39698934
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PQPubID 23479
PageCount 12
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PublicationTitle Alzheimer's & dementia
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Snippet INTRODUCTION While there may be microbial contributions to Alzheimer's disease (AD), findings have been inconclusive. We recently reported an AD‐associated...
While there may be microbial contributions to Alzheimer's disease (AD), findings have been inconclusive. We recently reported an AD-associated CD83(+)...
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StartPage e14401
SubjectTerms Aged
Aged, 80 and over
Alzheimer Disease - immunology
Alzheimer Disease - metabolism
Alzheimer Disease - pathology
Alzheimer Disease - virology
Alzheimer's disease
antibody epitope repertoire analysis
Antigens, CD - metabolism
Brain - immunology
Brain - metabolism
Brain - pathology
Brain - virology
CD83 Antigen
CD83(+) microglia
cerebrospinal fluid
Cytomegalovirus - immunology
Cytomegalovirus Infections - immunology
Female
human cytomegalovirus
Humans
Immunoglobulin G - cerebrospinal fluid
Immunoglobulin G - metabolism
immunoglobulin G4
Immunoglobulins - metabolism
immunohistochemistry
Male
Membrane Glycoproteins - metabolism
Microglia - immunology
Microglia - metabolism
prefrontal cortex
superior frontal gyrus
transverse colon
vagus nerve
Vagus Nerve - immunology
Vagus Nerve - metabolism
Vagus Nerve - virology
viral infection
Title Alzheimer's disease‐associated CD83(+) microglia are linked with increased immunoglobulin G4 and human cytomegalovirus in the gut, vagal nerve, and brain
URI https://onlinelibrary.wiley.com/doi/abs/10.1002%2Falz.14401
https://www.ncbi.nlm.nih.gov/pubmed/39698934
https://www.proquest.com/docview/3147134631
https://pubmed.ncbi.nlm.nih.gov/PMC11772737
Volume 21
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