The Novel Omega-6 Fatty Acid Docosapentaenoic Acid Positively Modulates Brain Innate Immune Response for Resolving Neuroinflammation at Early and Late Stages of Humanized APOE-Based Alzheimer's Disease Models

The Novel Omega-6 Fatty Acid Docosapentaenoic Acid Positively Modulates Brain Innate Immune Response for Resolving Neuroinflammation at Early and Late Stages of Humanized APOE-Based Alzheimer's Disease Models

Neuroinflammation plays a crucial role in the development and progression of Alzheimer's disease (AD), in which activated microglia are found to be associated with neurodegeneration. However, there is limited evidence showing how neuroinflammation and activated microglia are directly linked to...

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Published in:Frontiers in immunology Vol. 11; p. 558036
Main Authors: Ma, Qiu-Lan, Zhu, Cansheng, Morselli, Marco, Su, Trent, Pelligrini, Matteo, Lu, Zhengqi, Jones, Mychica, Denver, Paul, Castro, Daniel, Gu, Xuelin, Relampagos, Frances, Caoili, Kaitlin, Teter, Bruce, Frautschy, Sally A, Cole, Gregory M
Format: Journal Article
Language:English
Published: Switzerland Frontiers Media S.A 16-10-2020
Subjects:
Alzheimer Disease - etiology
Alzheimer Disease - metabolism
Alzheimer Disease - pathology
Alzheimer's disease
Animals
APOE
Apolipoproteins E - genetics
Apolipoproteins E - metabolism
Brain - immunology
Brain - metabolism
Cytokines - metabolism
Disease Models, Animal
Disease Susceptibility
docosapentaenoic acid
fatty acid
Fatty Acids, Omega-6 - metabolism
Fatty Acids, Unsaturated - metabolism
Immunity, Innate
Immunohistochemistry
Immunology
Inflammation Mediators - metabolism
linoleic acid
Mice
Mice, Transgenic
Microglia - immunology
Microglia - metabolism
Neurodegenerative Diseases
neuroinflammation
EFAD
neuroinflammation
docosapentaenoic acid
fatty acid
linoleic acid
APOE
Alzheimer's disease
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Abstract Neuroinflammation plays a crucial role in the development and progression of Alzheimer's disease (AD), in which activated microglia are found to be associated with neurodegeneration. However, there is limited evidence showing how neuroinflammation and activated microglia are directly linked to neurodegeneration . Besides, there are currently no effective anti-inflammatory drugs for AD. In this study, we report on an effective anti-inflammatory lipid, linoleic acid (LA) metabolite docosapentaenoic acid (DPAn-6) treatment of aged humanized EFAD mice with advanced AD pathology. We also report the associations of neuroinflammatory and/or activated microglial markers with neurodegeneration . First, we found that dietary LA reduced proinflammatory cytokines of IL1-β, IL-6, as well as mRNA expression of COX2 toward resolving neuroinflammation with an increase of IL-10 in adult AD models E3FAD and E4FAD mice. Brain fatty acid assays showed a five to six-fold increase in DPAn-6 by dietary LA, especially more in E4FAD mice, when compared to standard diet. Thus, we tested DPAn-6 in aged E4FAD mice. After DPAn-6 was administered to the E4FAD mice by oral gavage for three weeks, we found that DPAn-6 reduced microgliosis and mRNA expressions of inflammatory, microglial, and caspase markers. Further, DPAn-6 increased mRNA expressions of ADCYAP1, VGF, and neuronal pentraxin 2 in parallel, all of which were inversely correlated with inflammatory and microglial markers. Finally, both LA and DPAn-6 directly reduced mRNA expression of COX2 in amyloid-beta42 oligomer-challenged BV2 microglial cells. Together, these data indicated that DPAn-6 modulated neuroinflammatory responses toward resolution and improvement of neurodegeneration in the late stages of AD models.
AbstractList Neuroinflammation plays a crucial role in the development and progression of Alzheimer's disease (AD), in which activated microglia are found to be associated with neurodegeneration. However, there is limited evidence showing how neuroinflammation and activated microglia are directly linked to neurodegeneration . Besides, there are currently no effective anti-inflammatory drugs for AD. In this study, we report on an effective anti-inflammatory lipid, linoleic acid (LA) metabolite docosapentaenoic acid (DPAn-6) treatment of aged humanized EFAD mice with advanced AD pathology. We also report the associations of neuroinflammatory and/or activated microglial markers with neurodegeneration . First, we found that dietary LA reduced proinflammatory cytokines of IL1-β, IL-6, as well as mRNA expression of COX2 toward resolving neuroinflammation with an increase of IL-10 in adult AD models E3FAD and E4FAD mice. Brain fatty acid assays showed a five to six-fold increase in DPAn-6 by dietary LA, especially more in E4FAD mice, when compared to standard diet. Thus, we tested DPAn-6 in aged E4FAD mice. After DPAn-6 was administered to the E4FAD mice by oral gavage for three weeks, we found that DPAn-6 reduced microgliosis and mRNA expressions of inflammatory, microglial, and caspase markers. Further, DPAn-6 increased mRNA expressions of ADCYAP1, VGF, and neuronal pentraxin 2 in parallel, all of which were inversely correlated with inflammatory and microglial markers. Finally, both LA and DPAn-6 directly reduced mRNA expression of COX2 in amyloid-beta42 oligomer-challenged BV2 microglial cells. Together, these data indicated that DPAn-6 modulated neuroinflammatory responses toward resolution and improvement of neurodegeneration in the late stages of AD models.
Neuroinflammation plays a crucial role in the development and progression of Alzheimer's disease (AD), in which activated microglia are found to be associated with neurodegeneration. However, there is limited evidence showing how neuroinflammation and activated microglia are directly linked to neurodegeneration in vivo. Besides, there are currently no effective anti-inflammatory drugs for AD. In this study, we report on an effective anti-inflammatory lipid, linoleic acid (LA) metabolite docosapentaenoic acid (DPAn-6) treatment of aged humanized EFAD mice with advanced AD pathology. We also report the associations of neuroinflammatory and/or activated microglial markers with neurodegeneration in vivo. First, we found that dietary LA reduced proinflammatory cytokines of IL1-β, IL-6, as well as mRNA expression of COX2 toward resolving neuroinflammation with an increase of IL-10 in adult AD models E3FAD and E4FAD mice. Brain fatty acid assays showed a five to six-fold increase in DPAn-6 by dietary LA, especially more in E4FAD mice, when compared to standard diet. Thus, we tested DPAn-6 in aged E4FAD mice. After DPAn-6 was administered to the E4FAD mice by oral gavage for three weeks, we found that DPAn-6 reduced microgliosis and mRNA expressions of inflammatory, microglial, and caspase markers. Further, DPAn-6 increased mRNA expressions of ADCYAP1, VGF, and neuronal pentraxin 2 in parallel, all of which were inversely correlated with inflammatory and microglial markers. Finally, both LA and DPAn-6 directly reduced mRNA expression of COX2 in amyloid-beta42 oligomer-challenged BV2 microglial cells. Together, these data indicated that DPAn-6 modulated neuroinflammatory responses toward resolution and improvement of neurodegeneration in the late stages of AD models.
Neuroinflammation plays a crucial role in the development and progression of Alzheimer's disease (AD), in which activated microglia are found to be associated with neurodegeneration. However, there is limited evidence showing how neuroinflammation and activated microglia are directly linked to neurodegeneration in vivo . Besides, there are currently no effective anti-inflammatory drugs for AD. In this study, we report on an effective anti-inflammatory lipid, linoleic acid (LA) metabolite docosapentaenoic acid (DPAn-6) treatment of aged humanized EFAD mice with advanced AD pathology. We also report the associations of neuroinflammatory and/or activated microglial markers with neurodegeneration in vivo . First, we found that dietary LA reduced proinflammatory cytokines of IL1-β, IL-6, as well as mRNA expression of COX2 toward resolving neuroinflammation with an increase of IL-10 in adult AD models E3FAD and E4FAD mice. Brain fatty acid assays showed a five to six-fold increase in DPAn-6 by dietary LA, especially more in E4FAD mice, when compared to standard diet. Thus, we tested DPAn-6 in aged E4FAD mice. After DPAn-6 was administered to the E4FAD mice by oral gavage for three weeks, we found that DPAn-6 reduced microgliosis and mRNA expressions of inflammatory, microglial, and caspase markers. Further, DPAn-6 increased mRNA expressions of ADCYAP1, VGF, and neuronal pentraxin 2 in parallel, all of which were inversely correlated with inflammatory and microglial markers. Finally, both LA and DPAn-6 directly reduced mRNA expression of COX2 in amyloid-beta42 oligomer-challenged BV2 microglial cells. Together, these data indicated that DPAn-6 modulated neuroinflammatory responses toward resolution and improvement of neurodegeneration in the late stages of AD models.
Author Zhu, Cansheng
Castro, Daniel
Lu, Zhengqi
Gu, Xuelin
Cole, Gregory M
Jones, Mychica
Su, Trent
Pelligrini, Matteo
Denver, Paul
Ma, Qiu-Lan
Relampagos, Frances
Teter, Bruce
Morselli, Marco
Frautschy, Sally A
Caoili, Kaitlin
AuthorAffiliation 6 Institute for Quantitative and Computational Biology, University of California, Los Angeles , Los Angeles, CA , United States
2 Geriatric Research and Clinical Center, Greater Los Angeles Veterans Affairs Healthcare System, West Los Angeles VA Medical Center , Los Angeles, CA , United States
4 Department of Molecular, Cell and Developmental Biology, University of California, Los Angeles , Los Angeles, CA , United States
5 Institute for Genomics and Proteomics, University of California, Los Angeles , Los Angeles, CA , United States
8 Molecular Biology Institute, University of California, Los Angeles , Los Angeles, CA , United States
3 Department of Neurology, The Third Affiliated Hospital, Sun Yat-sen University , Guangzhou , China
7 Department of Biological Chemistry, University of California, Los Angeles , Los Angeles, CA , United States
1 Department of Neurology, University of California, Los Angeles , Los Angeles, CA , United States
9 Department of Medicine, University of California, Los
AuthorAffiliation_xml – name: 7 Department of Biological Chemistry, University of California, Los Angeles , Los Angeles, CA , United States
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– name: 2 Geriatric Research and Clinical Center, Greater Los Angeles Veterans Affairs Healthcare System, West Los Angeles VA Medical Center , Los Angeles, CA , United States
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Copyright Copyright © 2020 Ma, Zhu, Morselli, Su, Pelligrini, Lu, Jones, Denver, Castro, Gu, Relampagos, Caoili, Teter, Frautschy and Cole.
Copyright © 2020 Ma, Zhu, Morselli, Su, Pelligrini, Lu, Jones, Denver, Castro, Gu, Relampagos, Caoili, Teter, Frautschy and Cole. 2020 Ma, Zhu, Morselli, Su, Pelligrini, Lu, Jones, Denver, Castro, Gu, Relampagos, Caoili, Teter, Frautschy and Cole
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Keywords EFAD
neuroinflammation
docosapentaenoic acid
fatty acid
linoleic acid
APOE
Alzheimer's disease
Language English
License Copyright © 2020 Ma, Zhu, Morselli, Su, Pelligrini, Lu, Jones, Denver, Castro, Gu, Relampagos, Caoili, Teter, Frautschy and Cole.
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This article was submitted to Multiple Sclerosis and Neuroimmunology, a section of the journal Frontiers in Immunology
Edited by: Jorge Matias-Guiu, Complutense University of Madrid, Spain
Reviewed by: Maria F. Cano-Abad, Autonomous University of Madrid, Spain; Jorge Tolivia, University of Oviedo, Spain
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Snippet Neuroinflammation plays a crucial role in the development and progression of Alzheimer's disease (AD), in which activated microglia are found to be associated...
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SubjectTerms Alzheimer Disease - etiology
Alzheimer Disease - metabolism
Alzheimer Disease - pathology
Alzheimer's disease
Animals
APOE
Apolipoproteins E - genetics
Apolipoproteins E - metabolism
Brain - immunology
Brain - metabolism
Cytokines - metabolism
Disease Models, Animal
Disease Susceptibility
docosapentaenoic acid
fatty acid
Fatty Acids, Omega-6 - metabolism
Fatty Acids, Unsaturated - metabolism
Immunity, Innate
Immunohistochemistry
Immunology
Inflammation Mediators - metabolism
linoleic acid
Mice
Mice, Transgenic
Microglia - immunology
Microglia - metabolism
Neurodegenerative Diseases
neuroinflammation
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Title The Novel Omega-6 Fatty Acid Docosapentaenoic Acid Positively Modulates Brain Innate Immune Response for Resolving Neuroinflammation at Early and Late Stages of Humanized APOE-Based Alzheimer's Disease Models
URI https://www.ncbi.nlm.nih.gov/pubmed/33178186
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