Modulation of Alzheimer's disease brain pathology in mice by gut bacterial depletion: the role of IL-17a

Gut Microbes. 2024 Jan-Dec;16(1):2363014. doi: 10.1080/19490976.2024.2363014. Epub 2024 Jun 21.

Abstract

Gut bacteria regulate brain pathology of Alzheimer's disease (AD) patients and animal models; however, the underlying mechanism remains unclear. In this study, 3-month-old APP-transgenic female mice with and without knock-out of Il-17a gene were treated with antibiotics-supplemented or normal drinking water for 2 months. The antibiotic treatment eradicated almost all intestinal bacteria, which led to a reduction in Il-17a-expressing CD4-positive T lymphocytes in the spleen and gut, and to a decrease in bacterial DNA in brain tissue. Depletion of gut bacteria inhibited inflammatory activation in both brain tissue and microglia, lowered cerebral Aβ levels, and promoted transcription of Arc gene in the brain of APP-transgenic mice, all of which effects were abolished by deficiency of Il-17a. As possible mechanisms regulating Aβ pathology, depletion of gut bacteria inhibited β-secretase activity and increased the expression of Abcb1 and Lrp1 in the brain or at the blood-brain barrier, which were also reversed by the absence of Il-17a. Interestingly, a crossbreeding experiment between APP-transgenic mice and Il-17a knockout mice further showed that deficiency of Il-17a had already increased Abcb1 and Lrp1 expression at the blood-brain barrier. Thus, depletion of gut bacteria attenuates inflammatory activation and amyloid pathology in APP-transgenic mice via Il-17a-involved signaling pathways. Our study contributes to a better understanding of the gut-brain axis in AD pathophysiology and highlights the therapeutic potential of Il-17a inhibition or specific depletion of gut bacteria that stimulate the development of Il-17a-expressing T cells.

Keywords: Alzheimer’s disease; amyloid pathology; and Il-17a; gut microbiome; microglia.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alzheimer Disease* / metabolism
  • Alzheimer Disease* / microbiology
  • Alzheimer Disease* / pathology
  • Amyloid Precursor Protein Secretases / genetics
  • Amyloid Precursor Protein Secretases / metabolism
  • Amyloid beta-Peptides / metabolism
  • Animals
  • Anti-Bacterial Agents / pharmacology
  • Blood-Brain Barrier / metabolism
  • Blood-Brain Barrier / microbiology
  • Brain* / metabolism
  • Brain* / pathology
  • CD4-Positive T-Lymphocytes / immunology
  • CD4-Positive T-Lymphocytes / metabolism
  • Disease Models, Animal
  • Female
  • Gastrointestinal Microbiome*
  • Humans
  • Interleukin-17* / genetics
  • Interleukin-17* / metabolism
  • Low Density Lipoprotein Receptor-Related Protein-1
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mice, Transgenic
  • Microglia / metabolism
  • Microglia / microbiology
  • Microglia / pathology

Substances

  • Amyloid beta-Peptides
  • Amyloid Precursor Protein Secretases
  • Anti-Bacterial Agents
  • Il17a protein, mouse
  • Interleukin-17
  • Low Density Lipoprotein Receptor-Related Protein-1
  • Lrp1 protein, mouse

Grants and funding

This work was supported by Alzheimer Forschung Initiative e.V. (Project #18009, and Publication Grant #P2405; to Y.L.), Saarland University through HOMFOR 2016 and 2019 (to Y.L.) and Anschubfinanzierung 2021 and 2023 (to Y.L.).