Mast cell deficiency improves cognition and enhances disease-associated microglia in 5XFAD mice.

5XFAD Alzheimer's disease CP: Immunology CP: Neuroscience astrocyte behavior mast cell meninges microglia neuroimmune interaction

Journal

Cell reports
ISSN: 2211-1247
Titre abrégé: Cell Rep
Pays: United States
ID NLM: 101573691

Informations de publication

Date de publication:
26 09 2023
Historique:
received: 13 07 2022
revised: 20 06 2023
accepted: 30 08 2023
medline: 13 11 2023
pubmed: 15 9 2023
entrez: 15 9 2023
Statut: ppublish

Résumé

Emerging evidence suggests that peripheral immune cells contribute to Alzheimer's disease (AD) neuropathogenesis. Among these, mast cells are known for their functions in allergic reactions and neuroinflammation; however, little is known about their role in AD. Here, we crossed 5XFAD mice with mast cell-deficient strains and observed the effects on AD-related neuropathology and cognitive impairment. We found that mast cell depletion improved contextual fear conditioning in 5XFAD mice without affecting cued fear conditioning, anxiety-like behavior, or amyloid burden. Furthermore, mast cell depletion led to an upregulation of transcriptomic signatures for putatively protective disease-associated microglia and resulted in reduced markers indicative of reactive astrocytes. We hypothesize a system of bidirectional communication between dural mast cells and the brain, where mast cells respond to signals from the brain environment by expressing immune-regulatory mediators, impacting cognition and glial cell function. These findings highlight mast cells as potential therapeutic targets for AD.

Identifiants

pubmed: 37713312
pii: S2211-1247(23)01153-1
doi: 10.1016/j.celrep.2023.113141
pmc: PMC10634538
mid: NIHMS1933923
pii:
doi:

Substances chimiques

Immunologic Factors 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

113141

Subventions

Organisme : NIDDK NIH HHS
ID : P30 DK040561
Pays : United States
Organisme : NIA NIH HHS
ID : T32 AG000222
Pays : United States

Informations de copyright

Copyright © 2023 The Authors. Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests R.E.T. is a consultant to and shareholder in AZTherapeutics. R.I.S. is a shareholder in Feromics.

Références

Neurodegener Dis Manag. 2021 Aug;11(4):263-276
pubmed: 34412534
J Neurosci. 2017 Jun 21;37(25):6132-6148
pubmed: 28559377
Nat Rev Dis Primers. 2021 May 13;7(1):33
pubmed: 33986301
Proc Natl Acad Sci U S A. 1997 Feb 18;94(4):1550-5
pubmed: 9037091
Int J Mol Sci. 2021 Jan 22;22(3):
pubmed: 33499208
Int J Immunopathol Pharmacol. 2009 Apr-Jun;22(2):473-83
pubmed: 19505377
Nat Commun. 2019 Feb 11;10(1):706
pubmed: 30742008
Nat Neurosci. 2019 Jun;22(6):1021-1035
pubmed: 31061494
Cell Physiol Biochem. 2012;29(5-6):931-40
pubmed: 22613992
Ageing Res Rev. 2021 Jul;68:101335
pubmed: 33812051
Proc Natl Acad Sci U S A. 2008 Nov 18;105(46):18053-7
pubmed: 19004805
J Neurosci. 2015 Feb 11;35(6):2817-29
pubmed: 25673868
J Neurosci. 2012 Nov 14;32(46):16129-40
pubmed: 23152597
Cell. 2017 Jun 15;169(7):1276-1290.e17
pubmed: 28602351
Acta Neuropathol. 2013 May;125(5):637-50
pubmed: 23404369
Mol Neurobiol. 2017 Mar;54(2):997-1007
pubmed: 26797518
Lancet. 2017 Feb 11;389(10069):612-620
pubmed: 28069279
Int J Mol Sci. 2023 Jul 26;24(15):
pubmed: 37569378
Cell. 2018 May 17;173(5):1073-1081
pubmed: 29775591
Acta Neuropathol Commun. 2018 Oct 16;6(1):104
pubmed: 30322407
Immunity. 2011 Nov 23;35(5):832-44
pubmed: 22101159
Cancer Res. 2021 Jul 15;81(14):3791-3805
pubmed: 34035083
Sci Rep. 2018 Jan 18;8(1):1144
pubmed: 29348604
Nat Neurosci. 2015 Oct;18(10):1394-404
pubmed: 26404714
Dev Neurosci. 2007;29(4-5):373-84
pubmed: 17762205
Nat Rev Neurol. 2018 Mar;14(3):133-150
pubmed: 29377008
Nature. 2022 Dec;612(7940):417-429
pubmed: 36517712
Genome Med. 2023 Jan 26;15(1):6
pubmed: 36703235
Acta Neuropathol Commun. 2021 Apr 26;9(1):78
pubmed: 33902708
Neurobiol Aging. 2012 Jan;33(1):196.e29-40
pubmed: 20619937
Immunity. 2017 Sep 19;47(3):566-581.e9
pubmed: 28930663
Trends Immunol. 2012 Dec;33(12):613-25
pubmed: 23127755
Cell. 2021 Jun 24;184(13):3573-3587.e29
pubmed: 34062119
Front Immunol. 2015 May 18;6:238
pubmed: 26042121
PLoS One. 2013;8(3):e58963
pubmed: 23527056
Cell. 2021 Feb 18;184(4):1000-1016.e27
pubmed: 33508229
Immunity. 2022 Dec 13;55(12):2236-2254
pubmed: 36351425
Cell. 2005 Feb 25;120(4):545-55
pubmed: 15734686
Front Cell Neurosci. 2019 Feb 19;13:54
pubmed: 30837843
Mol Neurobiol. 2019 Mar;56(3):1681-1693
pubmed: 29916143
Mediators Inflamm. 2013;2013:140812
pubmed: 23818741
Neuron. 2022 Nov 2;110(21):3458-3483
pubmed: 36327895
J Alzheimers Dis. 2020;76(4):1339-1345
pubmed: 32623401
Nat Genet. 2003 Jul;34(3):267-73
pubmed: 12808457
J Neurosci. 2006 Oct 4;26(40):10129-40
pubmed: 17021169
Chest. 1971 Sep;60(3):210-3
pubmed: 4106050
J Neuroinflammation. 2016 May 31;13(1):127
pubmed: 27245661
Trends Neurosci. 2019 Jan;42(1):43-55
pubmed: 30293752
PLoS One. 2013 Oct 18;8(10):e78434
pubmed: 24205232
J Innate Immun. 2020;12(5):357-372
pubmed: 32498069
Annu Rev Immunol. 2020 Apr 26;38:597-620
pubmed: 32340575
Front Cell Neurosci. 2019 Apr 30;13:171
pubmed: 31133804
PLoS One. 2009 Sep 30;4(9):e7258
pubmed: 19789626
EMBO Mol Med. 2019 Feb;11(2):
pubmed: 30617153
J Immunol. 2010 Jun 15;184(12):6891-900
pubmed: 20488789
Front Pharmacol. 2020 Apr 14;11:443
pubmed: 32346366
Immunity. 2022 Aug 9;55(8):1448-1465.e6
pubmed: 35931085
Front Neurosci. 2021 Jul 14;15:680214
pubmed: 34335160
Mediators Inflamm. 2020 Feb 24;2020:8098439
pubmed: 32184702
Am J Pathol. 2014 Sep;184(9):2493-504
pubmed: 25134760
Nature. 2018 Oct;562(7727):367-372
pubmed: 30283141
Adv Clin Exp Med. 2016 Jul-Aug;25(4):781-7
pubmed: 27629855
Nat Commun. 2017 Jan 16;8:14049
pubmed: 28091601
Front Cell Neurosci. 2019 May 03;13:191
pubmed: 31130850
Nat Neurosci. 2018 Sep;21(9):1209-1217
pubmed: 30150661
Alzheimers Res Ther. 2023 Feb 28;15(1):39
pubmed: 36849969
Glia. 2021 Aug;69(8):1852-1881
pubmed: 33634529

Auteurs

Chih-Chung Jerry Lin (CJ)

Genetics and Aging Research Unit, Department of Neurology, Massachusetts General Hospital and Harvard Medical School, Charlestown, MA 02129, USA.

Fanny Herisson (F)

Genetics and Aging Research Unit, Department of Neurology, Massachusetts General Hospital and Harvard Medical School, Charlestown, MA 02129, USA.

Hoang Le (H)

Genetics and Aging Research Unit, Department of Neurology, Massachusetts General Hospital and Harvard Medical School, Charlestown, MA 02129, USA.

Nader Jaafar (N)

Genetics and Aging Research Unit, Department of Neurology, Massachusetts General Hospital and Harvard Medical School, Charlestown, MA 02129, USA.

Kashish Chetal (K)

Department of Molecular Biology, Massachusetts General Hospital, Boston, MA 02114, USA.

Mary K Oram (MK)

Genetics and Aging Research Unit, Department of Neurology, Massachusetts General Hospital and Harvard Medical School, Charlestown, MA 02129, USA.

Kelly L Flynn (KL)

Genetics and Aging Research Unit, Department of Neurology, Massachusetts General Hospital and Harvard Medical School, Charlestown, MA 02129, USA.

Evan P Gavrilles (EP)

Genetics and Aging Research Unit, Department of Neurology, Massachusetts General Hospital and Harvard Medical School, Charlestown, MA 02129, USA.

Ruslan I Sadreyev (RI)

Department of Molecular Biology, Massachusetts General Hospital, Boston, MA 02114, USA; Department of Pathology, Massachusetts General Hospital and Harvard Medical School, Boston, MA 02114, USA.

Felipe L Schiffino (FL)

Genetics and Aging Research Unit, Department of Neurology, Massachusetts General Hospital and Harvard Medical School, Charlestown, MA 02129, USA.

Rudolph E Tanzi (RE)

Genetics and Aging Research Unit, Department of Neurology, Massachusetts General Hospital and Harvard Medical School, Charlestown, MA 02129, USA; Henry and Allison McCance Center for Brain Health, Massachusetts General Hospital, Charlestown, MA 02129, USA. Electronic address: tanzi@helix.mgh.harvard.edu.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH