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      Evaluation of the fatty acid-based erythrocyte membrane lipidome in cats with food responsive enteropathy, inflammatory bowel disease and low-grade intestinal T-cell lymphoma

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          Abstract

          Feline chronic enteropathies (FCE), include food-responsive-enteropathy (FRE), inflammatory bowel disease (IBD), and low-grade intestinal T-cell lymphoma (LGITL), and are common causes of chronic gastrointestinal signs in cats. Distinguishing between different subgroups of FCE can be challenging due to the frequent overlap of anamnestic, clinical, and laboratory data. While dysregulation in lipid metabolism has been reported in humans and dogs with chronic IBD, similar changes in cats are not yet completely understood. Assessing the fatty acid (FA) profile of red blood cell (RBC) membranes offers a valuable method for evaluating the quantity and quality of structural and functional molecular components in the membranes. Therefore, this study aimed to examine the FA composition of RBC membranes in FCE in comparison to healthy cats (HC). Gas-chromatography was used to quantitatively analyze a cluster of 11 FA, and based on these results, parameters of lipid homeostasis and enzyme activity indexes were calculated. A total of 41 FCE cats (17 FRE, 15 IBD, 9 LGITL) and 43 HC were enrolled. In FCE cats, the values of docosapentaenoic acid (p = 0.0002) and docosahexaenoic acid (p = 0.0246), were significantly higher, resulting in an overall increase in ω-3 polyunsaturated fatty acids (PUFA) (p = 0.006), and that of linoleic acid (p = 0.0026) was significantly lower. Additionally, FCE cats exhibited an increased PUFA balance (p = 0.0019) and Δ6-desaturase index (p = 0.0151), along with a decreased ω-6/ω-3 ratio (p = 0.0019). No differences were observed among cats affected by FRE, IBD and LGITL. Like humans and dogs, the results of this study indicate that FCE cats also display changes in their FA lipid profile at the level of the RBC membrane. The non-invasive analysis of RBC membrane shows promise as a potential tool for gaining a better understanding of lipid imbalances in this disease.

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          Resolvins in inflammation: emergence of the pro-resolving superfamily of mediators.

          Charles Serhan, Bruce Levy (2018)
          Countless times each day, the acute inflammatory response protects us from invading microbes, injuries, and insults from within, as in surgery-induced tissue injury. These challenges go unnoticed because they are self-limited and naturally resolve without progressing to chronic inflammation. Peripheral blood markers of inflammation are present in many common diseases, including inflammatory bowel disease, cardiovascular disease, neurodegenerative disease, and cancer. While acute inflammation is protective, excessive swarming of neutrophils amplifies collateral tissue damage and inflammation. Hence, understanding the mechanisms that control the resolution of acute inflammation provides insight into preventing and treating inflammatory diseases in multiple organs. This Review focuses on the resolution phase of inflammation with identification of specialized pro-resolving mediators (SPMs) that involve three separate biosynthetic and potent mediator families, which are defined using the first quantitative resolution indices to score this vital process. These are the resolvins, protectins, and maresins: bioactive metabolomes that each stimulate self-limited innate responses, enhance innate microbial killing and clearance, and are organ-protective. We briefly address biosynthesis of SPMs and their activation of endogenous resolution programs as terrain for new therapeutic approaches that are not, by definition, immunosuppressive, but rather new immunoresolvent therapies.
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            Omega-3 Fatty Acids and Inflammatory Processes

            Philip C. Calder (2010)
            Long chain fatty acids influence inflammation through a variety of mechanisms; many of these are mediated by, or at least associated with, changes in fatty acid composition of cell membranes. Changes in these compositions can modify membrane fluidity, cell signaling leading to altered gene expression, and the pattern of lipid mediator production. Cell involved in the inflammatory response are typically rich in the n-6 fatty acid arachidonic acid, but the contents of arachidonic acid and of the n-3 fatty acids eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA) can be altered through oral administration of EPA and DHA. Eicosanoids produced from arachidonic acid have roles in inflammation. EPA also gives rise to eicosanoids and these often have differing properties from those of arachidonic acid-derived eicosanoids. EPA and DHA give rise to newly discovered resolvins which are anti-inflammatory and inflammation resolving. Increased membrane content of EPA and DHA (and decreased arachidonic acid content) results in a changed pattern of production of eicosanoids and resolvins. Changing the fatty acid composition of cells involved in the inflammatory response also affects production of peptide mediators of inflammation (adhesion molecules, cytokines etc.). Thus, the fatty acid composition of cells involved in the inflammatory response influences their function; the contents of arachidonic acid, EPA and DHA appear to be especially important. The anti-inflammatory effects of marine n-3 PUFAs suggest that they may be useful as therapeutic agents in disorders with an inflammatory component.
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              The opposing effects of n-3 and n-6 fatty acids.

              Gerd Schmitz, Adrian Ecker (2008)
              Polyunsaturated fatty acids (PUFAs) can be classified in n-3 fatty acids and n-6 fatty acids, and in westernized diet the predominant dietary PUFAs are n-6 fatty acids. Both types of fatty acids are precursors of signaling molecules with opposing effects, that modulate membrane microdomain composition, receptor signaling and gene expression. The predominant n-6 fatty acid is arachidonic acid, which is converted to prostaglandins, leukotrienes and other lipoxygenase or cyclooxygenase products. These products are important regulators of cellular functions with inflammatory, atherogenic and prothrombotic effects. Typical n-3 fatty acids are docosahexaenoic acid and eicosapentaenoic acid, which are competitive substrates for the enzymes and products of arachidonic acid metabolism. Docosahexaenoic acid- and eicosapentaenoic acid-derived eicosanoids antagonize the pro-inflammatory effects of n-6 fatty acids. n-3 and n-6 fatty acids are ligands/modulators for the nuclear receptors NFkappaB, PPAR and SREBP-1c, which control various genes of inflammatory signaling and lipid metabolism. n-3 Fatty acids down-regulate inflammatory genes and lipid synthesis, and stimulate fatty acid degradation. In addition, the n-3/n-6 PUFA content of cell and organelle membranes, as well as membrane microdomains strongly influences membrane function and numerous cellular processes such as cell death and survival.
              Article 0 comments Cited 141 times – based on 0 reviews     Review now
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                Author and article information

                Contributors
                Paolo Emidio Crisi:
                ORCID: https://orcid.org/0000-0001-5993-0059
                Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: Writing – original draft
                Maria Veronica Giordano: Role: Data curationRole: Formal analysisRole: InvestigationRole: Writing – original draft
                Alessia Luciani: Role: InvestigationRole: Writing – review & editing
                Alessandro Gramenzi: Role: ConceptualizationRole: MethodologyRole: SupervisionRole: Writing – review & editing
                Paraskevi Prasinou: Role: ConceptualizationRole: Formal analysisRole: Investigation
                Anna Sansone: Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: Writing – review & editing
                Valentina Rinaldi: Role: InvestigationRole: Writing – review & editing
                Carla Ferreri: Role: ConceptualizationRole: InvestigationRole: MethodologyRole: SupervisionRole: Writing – review & editing
                Andrea Boari: Role: ConceptualizationRole: Data curationRole: MethodologyRole: SupervisionRole: ValidationRole: Writing – review & editing
                Juan J. Loor: Role: Editor
                Journal
                Journal ID (nlm-ta): PLoS One
                Journal ID (iso-abbrev): PLoS One
                Journal ID (publisher-id): plos
                Title: PLOS ONE
                Publisher: Public Library of Science (San Francisco, CA USA )
                ISSN (Electronic): 1932-6203
                Publication date (Electronic): 29 July 2024
                Publication date Collection: 2024
                Volume: 19
                Issue: 7
                Electronic Location Identifier: e0307757
                Affiliations
                [1 ] Department of Veterinary Medicine, Veterinary Teaching Hospital, University of Teramo, Teramo, Italy
                [2 ] Institute of Organic Synthesis and Photoreactivity, Consiglio Nazionale delle Ricerche, Bologna, Italy
                University of Illinois, UNITED STATES OF AMERICA
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Author information
                https://orcid.org/0000-0001-5993-0059
                Article
                Publisher ID: PONE-D-24-03902
                DOI: 10.1371/journal.pone.0307757
                PMC ID: 11285949
                PubMed ID: 39074116
                SO-VID: 42bac37c-4700-4086-8cab-15f3b215771b
                Copyright © © 2024 Crisi et al
                License:

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                Date received : 29 January 2024
                Date accepted : 10 July 2024
                Page count
                Figures: 4, Tables: 5, Pages: 18
                Funding
                The author(s) received no specific funding for this work.
                Categories
                Subject: Research Article
                Subject: Biology and Life Sciences
                Subject: Organisms
                Subject: Eukaryota
                Subject: Animals
                Subject: Vertebrates
                Subject: Amniotes
                Subject: Mammals
                Subject: Cats
                Subject: Biology and Life Sciences
                Subject: Zoology
                Subject: Animals
                Subject: Vertebrates
                Subject: Amniotes
                Subject: Mammals
                Subject: Cats
                Subject: Biology and Life Sciences
                Subject: Biochemistry
                Subject: Lipids
                Subject: Fatty Acids
                Subject: Medicine and Health Sciences
                Subject: Gastroenterology and Hepatology
                Subject: Inflammatory Bowel Disease
                Subject: Biology and Life Sciences
                Subject: Organisms
                Subject: Eukaryota
                Subject: Animals
                Subject: Vertebrates
                Subject: Amniotes
                Subject: Mammals
                Subject: Dogs
                Subject: Biology and Life Sciences
                Subject: Zoology
                Subject: Animals
                Subject: Vertebrates
                Subject: Amniotes
                Subject: Mammals
                Subject: Dogs
                Subject: Biology and Life Sciences
                Subject: Cell Biology
                Subject: Cellular Structures and Organelles
                Subject: Cell Membranes
                Subject: Medicine and Health Sciences
                Subject: Gastroenterology and Hepatology
                Subject: Enteropathies
                Subject: Biology and Life Sciences
                Subject: Organisms
                Subject: Eukaryota
                Subject: Animals
                Subject: Domestic Animals
                Subject: Biology and Life Sciences
                Subject: Zoology
                Subject: Animals
                Subject: Domestic Animals
                Subject: Biology and Life Sciences
                Subject: Nutrition
                Subject: Diet
                Subject: Medicine and Health Sciences
                Subject: Nutrition
                Subject: Diet
                Custom metadata
                Data Availability All relevant data are within the paper and its Supporting information files.

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