Dietary Enrichment with 20% Fish Oil Decreases Mucus Production and the Inflammatory Response in Mice with Ovalbumin-Induced Allergic Lung Inflammation

The prevalence of asthma has increased in recent decades, which may be related to higher dietary intake of (n-6) polyunsaturated fatty acids (PUFA) and lower intake of (n-3) PUFA, e.g., those contained in fish oil. The objective of this study was to determine if dietary PUFA enrichment decreases muc...

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Veröffentlicht in:PloS one 2016-09, Vol.11 (9), p.e0163819-e0163819
Hauptverfasser: Hall, Jean A, Hartman, Jaye, Skinner, Monica M, Schwindt, Adam R, Fischer, Kay A, Vorachek, William R, Bobe, Gerd, Valentine, Beth A
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container_issue 9
container_start_page e0163819
container_title PloS one
container_volume 11
creator Hall, Jean A
Hartman, Jaye
Skinner, Monica M
Schwindt, Adam R
Fischer, Kay A
Vorachek, William R
Bobe, Gerd
Valentine, Beth A
description The prevalence of asthma has increased in recent decades, which may be related to higher dietary intake of (n-6) polyunsaturated fatty acids (PUFA) and lower intake of (n-3) PUFA, e.g., those contained in fish oil. The objective of this study was to determine if dietary PUFA enrichment decreases mucus production or the inflammatory response associated with ovalbumin (OVA)-induced allergic lung inflammation. Mice (n = 10/group) were fed control, 20% fish oil, or 20% corn oil enriched diets for a total of 12 weeks. At 8 and 10 weeks, mice were given an intraperitoneal injection of saline (10 control-fed mice) or OVA (30 remaining mice). Once at 10 weeks and on 3 consecutive days during week 12, mice were challenged by nebulizing with saline or OVA. Mice were euthanized 24 hours after the last challenge and blood was collected for plasma FA analysis. Bronchoalveolar lavage (BAL) fluid was collected to determine cell composition and Th2-type cytokine (IL-4, IL-13) concentrations. Periodic acid-Schiff (PAS) + mucus-producing cells and CD45+ inflammatory cell infiltrates in lung tissue were quantified using morphometric analysis. Relative abundance of mRNA for mucin (Muc4, Muc5ac, and Muc5b) and Th2-type cytokine (IL-4, IL-5, and IL-13) genes were compared with ß-actin by qPCR. Supplementation with either corn oil or fish oil effectively altered plasma FA profiles towards more (n-6) FA or (n-3) FA, respectively (P < 0.0001). Sensitization and challenge with OVA increased the proportion of neutrophils, lymphocytes, and eosinophils, and decreased the proportion of macrophages and concentrations of IL-13 in BAL fluid; increased the percentage of PAS+ mucus-producing cells and CD45+ inflammatory cell infiltrates in lung tissue; and increased gene expression of mucins (Muc4, Muc5ac, and Muc5b) and Th2-type cytokines (IL-5 and IL-13) in lung tissue of control-fed mice. Dietary PUFA reversed the increase in PAS+ mucus-producing cells (P = 0.003). In addition, dietary enrichment with fish oil attenuated the percentage of CD45+ inflammatory cell infiltrates in lung tissue, and increased Muc4 and Muc 5b gene expression compared with OVA-sensitized and challenged control mice. In conclusion, dietary enrichment with either (n-3) or (n-6) PUFA decreased mucus production in lung tissues of OVA-sensitized and challenged mice. More specifically, enrichment with dietary (n-3) PUFA decreased CD45+ inflammatory cell infiltrates, thus inducing potentially beneficial changes in lung
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The objective of this study was to determine if dietary PUFA enrichment decreases mucus production or the inflammatory response associated with ovalbumin (OVA)-induced allergic lung inflammation. Mice (n = 10/group) were fed control, 20% fish oil, or 20% corn oil enriched diets for a total of 12 weeks. At 8 and 10 weeks, mice were given an intraperitoneal injection of saline (10 control-fed mice) or OVA (30 remaining mice). Once at 10 weeks and on 3 consecutive days during week 12, mice were challenged by nebulizing with saline or OVA. Mice were euthanized 24 hours after the last challenge and blood was collected for plasma FA analysis. Bronchoalveolar lavage (BAL) fluid was collected to determine cell composition and Th2-type cytokine (IL-4, IL-13) concentrations. Periodic acid-Schiff (PAS) + mucus-producing cells and CD45+ inflammatory cell infiltrates in lung tissue were quantified using morphometric analysis. Relative abundance of mRNA for mucin (Muc4, Muc5ac, and Muc5b) and Th2-type cytokine (IL-4, IL-5, and IL-13) genes were compared with ß-actin by qPCR. Supplementation with either corn oil or fish oil effectively altered plasma FA profiles towards more (n-6) FA or (n-3) FA, respectively (P &lt; 0.0001). Sensitization and challenge with OVA increased the proportion of neutrophils, lymphocytes, and eosinophils, and decreased the proportion of macrophages and concentrations of IL-13 in BAL fluid; increased the percentage of PAS+ mucus-producing cells and CD45+ inflammatory cell infiltrates in lung tissue; and increased gene expression of mucins (Muc4, Muc5ac, and Muc5b) and Th2-type cytokines (IL-5 and IL-13) in lung tissue of control-fed mice. Dietary PUFA reversed the increase in PAS+ mucus-producing cells (P = 0.003). In addition, dietary enrichment with fish oil attenuated the percentage of CD45+ inflammatory cell infiltrates in lung tissue, and increased Muc4 and Muc 5b gene expression compared with OVA-sensitized and challenged control mice. In conclusion, dietary enrichment with either (n-3) or (n-6) PUFA decreased mucus production in lung tissues of OVA-sensitized and challenged mice. More specifically, enrichment with dietary (n-3) PUFA decreased CD45+ inflammatory cell infiltrates, thus inducing potentially beneficial changes in lung tissue of OVA-sensitized and challenged mice.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0163819</identifier><identifier>PMID: 27669173</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Actin ; Albumin ; Alveoli ; Animal tissues ; Asthma ; B cells ; Biology and Life Sciences ; Bronchoalveolar lavage ; Bronchus ; CD45 antigen ; Corn ; Corn oil ; Cytokines ; Diet ; Dietary intake ; Dietary supplements ; Drug dosages ; Enrichment ; Eosinophils ; Fatty acids ; Fish ; Fish oils ; Gene expression ; Inflammation ; Inflammatory response ; Interleukin 13 ; Interleukin 4 ; Interleukin 5 ; Leukocytes (eosinophilic) ; Leukocytes (neutrophilic) ; Lungs ; Lymphocytes ; Lymphocytes T ; Macrophages ; Medicine and Health Sciences ; Metabolism ; Metabolites ; Mice ; Morphometry ; Mucin ; Mucins ; Mucus ; Oils &amp; fats ; Ovalbumin ; Polyunsaturated fatty acids ; Production management ; Relative abundance ; Rodents ; Statistics ; Supplementation ; Tissues ; Unsaturated fatty acids ; Vegetable oils ; Veterinary colleges ; Veterinary medicine</subject><ispartof>PloS one, 2016-09, Vol.11 (9), p.e0163819-e0163819</ispartof><rights>COPYRIGHT 2016 Public Library of Science</rights><rights>2016 Hall et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 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The objective of this study was to determine if dietary PUFA enrichment decreases mucus production or the inflammatory response associated with ovalbumin (OVA)-induced allergic lung inflammation. Mice (n = 10/group) were fed control, 20% fish oil, or 20% corn oil enriched diets for a total of 12 weeks. At 8 and 10 weeks, mice were given an intraperitoneal injection of saline (10 control-fed mice) or OVA (30 remaining mice). Once at 10 weeks and on 3 consecutive days during week 12, mice were challenged by nebulizing with saline or OVA. Mice were euthanized 24 hours after the last challenge and blood was collected for plasma FA analysis. Bronchoalveolar lavage (BAL) fluid was collected to determine cell composition and Th2-type cytokine (IL-4, IL-13) concentrations. Periodic acid-Schiff (PAS) + mucus-producing cells and CD45+ inflammatory cell infiltrates in lung tissue were quantified using morphometric analysis. Relative abundance of mRNA for mucin (Muc4, Muc5ac, and Muc5b) and Th2-type cytokine (IL-4, IL-5, and IL-13) genes were compared with ß-actin by qPCR. Supplementation with either corn oil or fish oil effectively altered plasma FA profiles towards more (n-6) FA or (n-3) FA, respectively (P &lt; 0.0001). Sensitization and challenge with OVA increased the proportion of neutrophils, lymphocytes, and eosinophils, and decreased the proportion of macrophages and concentrations of IL-13 in BAL fluid; increased the percentage of PAS+ mucus-producing cells and CD45+ inflammatory cell infiltrates in lung tissue; and increased gene expression of mucins (Muc4, Muc5ac, and Muc5b) and Th2-type cytokines (IL-5 and IL-13) in lung tissue of control-fed mice. Dietary PUFA reversed the increase in PAS+ mucus-producing cells (P = 0.003). In addition, dietary enrichment with fish oil attenuated the percentage of CD45+ inflammatory cell infiltrates in lung tissue, and increased Muc4 and Muc 5b gene expression compared with OVA-sensitized and challenged control mice. In conclusion, dietary enrichment with either (n-3) or (n-6) PUFA decreased mucus production in lung tissues of OVA-sensitized and challenged mice. More specifically, enrichment with dietary (n-3) PUFA decreased CD45+ inflammatory cell infiltrates, thus inducing potentially beneficial changes in lung tissue of OVA-sensitized and challenged mice.</description><subject>Actin</subject><subject>Albumin</subject><subject>Alveoli</subject><subject>Animal tissues</subject><subject>Asthma</subject><subject>B cells</subject><subject>Biology and Life Sciences</subject><subject>Bronchoalveolar lavage</subject><subject>Bronchus</subject><subject>CD45 antigen</subject><subject>Corn</subject><subject>Corn oil</subject><subject>Cytokines</subject><subject>Diet</subject><subject>Dietary intake</subject><subject>Dietary supplements</subject><subject>Drug dosages</subject><subject>Enrichment</subject><subject>Eosinophils</subject><subject>Fatty acids</subject><subject>Fish</subject><subject>Fish oils</subject><subject>Gene expression</subject><subject>Inflammation</subject><subject>Inflammatory response</subject><subject>Interleukin 13</subject><subject>Interleukin 4</subject><subject>Interleukin 5</subject><subject>Leukocytes (eosinophilic)</subject><subject>Leukocytes (neutrophilic)</subject><subject>Lungs</subject><subject>Lymphocytes</subject><subject>Lymphocytes T</subject><subject>Macrophages</subject><subject>Medicine and Health Sciences</subject><subject>Metabolism</subject><subject>Metabolites</subject><subject>Mice</subject><subject>Morphometry</subject><subject>Mucin</subject><subject>Mucins</subject><subject>Mucus</subject><subject>Oils &amp; fats</subject><subject>Ovalbumin</subject><subject>Polyunsaturated fatty acids</subject><subject>Production management</subject><subject>Relative abundance</subject><subject>Rodents</subject><subject>Statistics</subject><subject>Supplementation</subject><subject>Tissues</subject><subject>Unsaturated fatty acids</subject><subject>Vegetable oils</subject><subject>Veterinary colleges</subject><subject>Veterinary medicine</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNqNk1tvFCEYhidGY2v1HxglMRq92JXDAMONSdODbrLNmnq4JSzD7NAwUGGm6i_x78p0t3XX9KLhYibwvC8fL3xF8RzBKSIcvb8IQ_TKTS-DN1OIGKmQeFDsI0HwhGFIHm797xVPUrqAkJKKscfFHuaMCcTJfvHn2Jpexd_gxEer2874Hvy0fQswfA1ObWrBwjpwbHQ0KpkEzgY9JPA5hnrQvQ0eKF-DvjVg5hunuk71IZudm5TLSgZYD86sNmvLxZVyy6GzfjLzWW5qcOiciSurwXzwq38W2fdp8ahRLplnm-9B8e305OvRp8l88XF2dDifaI5pPxF0yZuSacGhEFBRrmiZR00JKjOgFWmWQitGIBfI1AaVotG6grRmhGlekoPi5dr30oUkN5kmiSpMSsxLwTIxWxN1UBfyMtouxyWDsvJ6IsSVVLG32hm5hBWtzVIzqllZIiUqVtFKaF5pbARqsteHzW7DsjO1zmlH5XZMd1e8beUqXEkKCePXxbzdGMTwYzCpl51N2jinvAnDWDehFAtC8T1QzAXGHI_oq__Qu4PYUCuVz2p9E3KJejSVhyVHAnLIR6_pHVQetemszm-1sXl-R_BuR5CZ3vzqV2pISc6-nN-fXXzfZd9ssa1Rrm9TcMP4utIuWK5BHUNK0TS394GgHFvtJg05tprctFqWvdi-y1vRTW-Rv4IdI0E</recordid><startdate>20160926</startdate><enddate>20160926</enddate><creator>Hall, Jean A</creator><creator>Hartman, Jaye</creator><creator>Skinner, Monica M</creator><creator>Schwindt, Adam R</creator><creator>Fischer, Kay A</creator><creator>Vorachek, William R</creator><creator>Bobe, Gerd</creator><creator>Valentine, Beth A</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20160926</creationdate><title>Dietary Enrichment with 20% Fish Oil Decreases Mucus Production and the Inflammatory Response in Mice with Ovalbumin-Induced Allergic Lung Inflammation</title><author>Hall, Jean A ; 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Medical Complete (Alumni)</collection><collection>Materials Science Database</collection><collection>Nursing &amp; Allied Health Database (Alumni Edition)</collection><collection>Meteorological &amp; Geoastrophysical Abstracts - Academic</collection><collection>ProQuest Engineering Collection</collection><collection>ProQuest Biological Science Collection</collection><collection>Agricultural Science Database</collection><collection>Health &amp; Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science Database</collection><collection>Engineering Database</collection><collection>Nursing &amp; Allied Health Premium</collection><collection>Advanced Technologies &amp; Aerospace Database</collection><collection>ProQuest Advanced Technologies &amp; Aerospace Collection</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environmental Science Database</collection><collection>Materials Science Collection</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>Engineering Collection</collection><collection>Environmental Science Collection</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Hall, Jean A</au><au>Hartman, Jaye</au><au>Skinner, Monica M</au><au>Schwindt, Adam R</au><au>Fischer, Kay A</au><au>Vorachek, William R</au><au>Bobe, Gerd</au><au>Valentine, Beth A</au><au>Aguila, Marcia B.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Dietary Enrichment with 20% Fish Oil Decreases Mucus Production and the Inflammatory Response in Mice with Ovalbumin-Induced Allergic Lung Inflammation</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2016-09-26</date><risdate>2016</risdate><volume>11</volume><issue>9</issue><spage>e0163819</spage><epage>e0163819</epage><pages>e0163819-e0163819</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>The prevalence of asthma has increased in recent decades, which may be related to higher dietary intake of (n-6) polyunsaturated fatty acids (PUFA) and lower intake of (n-3) PUFA, e.g., those contained in fish oil. The objective of this study was to determine if dietary PUFA enrichment decreases mucus production or the inflammatory response associated with ovalbumin (OVA)-induced allergic lung inflammation. Mice (n = 10/group) were fed control, 20% fish oil, or 20% corn oil enriched diets for a total of 12 weeks. At 8 and 10 weeks, mice were given an intraperitoneal injection of saline (10 control-fed mice) or OVA (30 remaining mice). Once at 10 weeks and on 3 consecutive days during week 12, mice were challenged by nebulizing with saline or OVA. Mice were euthanized 24 hours after the last challenge and blood was collected for plasma FA analysis. Bronchoalveolar lavage (BAL) fluid was collected to determine cell composition and Th2-type cytokine (IL-4, IL-13) concentrations. Periodic acid-Schiff (PAS) + mucus-producing cells and CD45+ inflammatory cell infiltrates in lung tissue were quantified using morphometric analysis. Relative abundance of mRNA for mucin (Muc4, Muc5ac, and Muc5b) and Th2-type cytokine (IL-4, IL-5, and IL-13) genes were compared with ß-actin by qPCR. Supplementation with either corn oil or fish oil effectively altered plasma FA profiles towards more (n-6) FA or (n-3) FA, respectively (P &lt; 0.0001). Sensitization and challenge with OVA increased the proportion of neutrophils, lymphocytes, and eosinophils, and decreased the proportion of macrophages and concentrations of IL-13 in BAL fluid; increased the percentage of PAS+ mucus-producing cells and CD45+ inflammatory cell infiltrates in lung tissue; and increased gene expression of mucins (Muc4, Muc5ac, and Muc5b) and Th2-type cytokines (IL-5 and IL-13) in lung tissue of control-fed mice. Dietary PUFA reversed the increase in PAS+ mucus-producing cells (P = 0.003). In addition, dietary enrichment with fish oil attenuated the percentage of CD45+ inflammatory cell infiltrates in lung tissue, and increased Muc4 and Muc 5b gene expression compared with OVA-sensitized and challenged control mice. In conclusion, dietary enrichment with either (n-3) or (n-6) PUFA decreased mucus production in lung tissues of OVA-sensitized and challenged mice. More specifically, enrichment with dietary (n-3) PUFA decreased CD45+ inflammatory cell infiltrates, thus inducing potentially beneficial changes in lung tissue of OVA-sensitized and challenged mice.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>27669173</pmid><doi>10.1371/journal.pone.0163819</doi><tpages>e0163819</tpages><oa>free_for_read</oa></addata></record>
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subjects Actin
Albumin
Alveoli
Animal tissues
Asthma
B cells
Biology and Life Sciences
Bronchoalveolar lavage
Bronchus
CD45 antigen
Corn
Corn oil
Cytokines
Diet
Dietary intake
Dietary supplements
Drug dosages
Enrichment
Eosinophils
Fatty acids
Fish
Fish oils
Gene expression
Inflammation
Inflammatory response
Interleukin 13
Interleukin 4
Interleukin 5
Leukocytes (eosinophilic)
Leukocytes (neutrophilic)
Lungs
Lymphocytes
Lymphocytes T
Macrophages
Medicine and Health Sciences
Metabolism
Metabolites
Mice
Morphometry
Mucin
Mucins
Mucus
Oils & fats
Ovalbumin
Polyunsaturated fatty acids
Production management
Relative abundance
Rodents
Statistics
Supplementation
Tissues
Unsaturated fatty acids
Vegetable oils
Veterinary colleges
Veterinary medicine
title Dietary Enrichment with 20% Fish Oil Decreases Mucus Production and the Inflammatory Response in Mice with Ovalbumin-Induced Allergic Lung Inflammation
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