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Systemic infection modifies the neuroinflammatory response in late stage Alzheimer’s disease

Systemic infection modifies the neuroinflammatory response in late stage Alzheimer’s disease
Systemic infection modifies the neuroinflammatory response in late stage Alzheimer’s disease
Clinical studies indicate that systemic infections accelerate cognitive decline in Alzheimer’s disease. Animal models suggest that this may be due to enhanced pro-inflammatory changes in the brain.
We have performed a post-mortem human study to determine whether systemic infection modifies the neuropathology and in particular, neuroinflammation, in the late-stage of the disease.
Sections of cerebral cortex and underlying white matter from controls and Alzheimer's patients who died with or without a terminal systemic infection were immunolabelled and quantified for: (i) Aβ and phosphorylated-tau; (ii) the inflammation-related proteins Iba1, CD68, HLA-DR, FcγRs (CD64, CD32a, CD32b, CD16), CHIL3L1, IL4R and CCR2; and (iii) T-cell marker CD3. In Alzheimer's disease, the synaptic proteins synaptophysin and PSD-95 were quantified by ELISA, and the inflammatory proteins and mRNAs by MesoScale Discovery Multiplex Assays and qPCR, respectively.
Systemic infection in Alzheimers' disease was associated with decreased CD16 (p = 0.027, grey matter) and CD68 (p= 0.015, white matter); increased CD64 (p = 0.017, white matter) as well as increased protein expression of IL6 (p = 0.047) and decreased IL5 (p = 0.007), IL7 (p = 0.002), IL12/IL23p40 (p = 0.001), IL15 (p =0.008), IL16 (p < 0.001) and IL17A (p < 0.001). Increased expression of anti-inflammatory genes CHI3L1 (p = 0.012) and IL4R (p = 0.004) were detected in this group. T-cell recruitment to the brain was reduced when systemic infection was present. However, exposure to systemic infection did not modify the pathology. In Alzheimer's disease, CD68 (p = 0.026), CD64 (p = 0.002), CHI3L1 (p = 0.016), IL4R (p = 0.005) and CCR2 (p = 0.010) were increased independently of systemic infection.
Our findings suggest that systemic infections modify neuroinflammatory processes in Alzheimer's disease. However, rather than promoting pro-inflammatory changes, as observed in experimental models, they seem to promote an anti-inflammatory, potentially immunosuppressive, environment in the human brain.
2051-5960
Rakic, Sonja
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Hung, Yat M.A.
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Smith, Matthew
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So, Denise
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Tayler, Hannah
bf6131b7-357f-4d30-bf91-a73d3baf85e6
Varney, William
f1acc3e1-116d-4edf-8e03-b21c67f5a5e2
Wild, Joe
d6f248d8-d5d9-4f90-ace2-e0b3b04f41e7
Harris, Scott
19ea097b-df15-4f0f-be19-8ac42c190028
Holmes, Clive
ada5abf3-8459-4cf7-be40-3f4e9391cc96
Love, Seth
c8c00a86-ecf8-4f61-8377-254305bdbc02
Stewart, William
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Nicoll, James
88c0685f-000e-4eb7-8f72-f36b4985e8ed
Boche, Delphine
bdcca10e-6302-4dd0-919f-67218f7e0d61
Rakic, Sonja
a6631393-7e52-4df4-a936-00cd2df5b6d4
Hung, Yat M.A.
5d05d4fb-5b91-4b03-941e-4758d32932f1
Smith, Matthew
a8ab8043-8bf9-4f6c-bfea-28c68ce02ce7
So, Denise
cb0836b5-056f-44df-8a5b-fb4621671b8c
Tayler, Hannah
bf6131b7-357f-4d30-bf91-a73d3baf85e6
Varney, William
f1acc3e1-116d-4edf-8e03-b21c67f5a5e2
Wild, Joe
d6f248d8-d5d9-4f90-ace2-e0b3b04f41e7
Harris, Scott
19ea097b-df15-4f0f-be19-8ac42c190028
Holmes, Clive
ada5abf3-8459-4cf7-be40-3f4e9391cc96
Love, Seth
c8c00a86-ecf8-4f61-8377-254305bdbc02
Stewart, William
18382d6a-f1dc-418f-81ee-25886304e250
Nicoll, James
88c0685f-000e-4eb7-8f72-f36b4985e8ed
Boche, Delphine
bdcca10e-6302-4dd0-919f-67218f7e0d61

Rakic, Sonja, Hung, Yat M.A., Smith, Matthew, So, Denise, Tayler, Hannah, Varney, William, Wild, Joe, Harris, Scott, Holmes, Clive, Love, Seth, Stewart, William, Nicoll, James and Boche, Delphine (2018) Systemic infection modifies the neuroinflammatory response in late stage Alzheimer’s disease. Acta Neuropathologica Communications, 6 (88). (doi:10.1186/s40478-018-0592-3).

Record type: Article

Abstract

Clinical studies indicate that systemic infections accelerate cognitive decline in Alzheimer’s disease. Animal models suggest that this may be due to enhanced pro-inflammatory changes in the brain.
We have performed a post-mortem human study to determine whether systemic infection modifies the neuropathology and in particular, neuroinflammation, in the late-stage of the disease.
Sections of cerebral cortex and underlying white matter from controls and Alzheimer's patients who died with or without a terminal systemic infection were immunolabelled and quantified for: (i) Aβ and phosphorylated-tau; (ii) the inflammation-related proteins Iba1, CD68, HLA-DR, FcγRs (CD64, CD32a, CD32b, CD16), CHIL3L1, IL4R and CCR2; and (iii) T-cell marker CD3. In Alzheimer's disease, the synaptic proteins synaptophysin and PSD-95 were quantified by ELISA, and the inflammatory proteins and mRNAs by MesoScale Discovery Multiplex Assays and qPCR, respectively.
Systemic infection in Alzheimers' disease was associated with decreased CD16 (p = 0.027, grey matter) and CD68 (p= 0.015, white matter); increased CD64 (p = 0.017, white matter) as well as increased protein expression of IL6 (p = 0.047) and decreased IL5 (p = 0.007), IL7 (p = 0.002), IL12/IL23p40 (p = 0.001), IL15 (p =0.008), IL16 (p < 0.001) and IL17A (p < 0.001). Increased expression of anti-inflammatory genes CHI3L1 (p = 0.012) and IL4R (p = 0.004) were detected in this group. T-cell recruitment to the brain was reduced when systemic infection was present. However, exposure to systemic infection did not modify the pathology. In Alzheimer's disease, CD68 (p = 0.026), CD64 (p = 0.002), CHI3L1 (p = 0.016), IL4R (p = 0.005) and CCR2 (p = 0.010) were increased independently of systemic infection.
Our findings suggest that systemic infections modify neuroinflammatory processes in Alzheimer's disease. However, rather than promoting pro-inflammatory changes, as observed in experimental models, they seem to promote an anti-inflammatory, potentially immunosuppressive, environment in the human brain.

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Accepted/In Press date: 30 August 2018
e-pub ahead of print date: 7 September 2018

Identifiers

Local EPrints ID: 424359
URI: http://eprints.soton.ac.uk/id/eprint/424359
ISSN: 2051-5960
PURE UUID: 2eace2e2-4b74-4ee5-bc95-871031a1c2b5
ORCID for Clive Holmes: ORCID iD orcid.org/0000-0003-1999-6912
ORCID for James Nicoll: ORCID iD orcid.org/0000-0002-9444-7246
ORCID for Delphine Boche: ORCID iD orcid.org/0000-0002-5884-130X

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Date deposited: 05 Oct 2018 11:36
Last modified: 16 Mar 2024 03:26

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Contributors

Author: Sonja Rakic
Author: Yat M.A. Hung
Author: Matthew Smith
Author: Denise So
Author: Hannah Tayler
Author: William Varney
Author: Joe Wild
Author: Scott Harris
Author: Clive Holmes ORCID iD
Author: Seth Love
Author: William Stewart
Author: James Nicoll ORCID iD
Author: Delphine Boche ORCID iD

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