Fish Oil Attenuates Omega-6 Polyunsaturated Fatty Acid-Induced Dysbiosis and Infectious Colitis but Impairs LPS Dephosphorylation Activity Causing Sepsis
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{"title"=>"Fish Oil Attenuates Omega-6 Polyunsaturated Fatty Acid-Induced Dysbiosis and Infectious Colitis but Impairs LPS Dephosphorylation Activity Causing Sepsis", "type"=>"journal", "authors"=>[{"first_name"=>"Sanjoy", "last_name"=>"Ghosh", "scopus_author_id"=>"55478976400"}, {"first_name"=>"Daniella", "last_name"=>"DeCoffe", "scopus_author_id"=>"55378318500"}, {"first_name"=>"Kirsty", "last_name"=>"Brown", "scopus_author_id"=>"55508192000"}, {"first_name"=>"Ethendhar", "last_name"=>"Rajendiran", "scopus_author_id"=>"24485569500"}, {"first_name"=>"Mehrbod", "last_name"=>"Estaki", "scopus_author_id"=>"55585493000"}, {"first_name"=>"Chuanbin", "last_name"=>"Dai", "scopus_author_id"=>"55166339200"}, {"first_name"=>"Ashley", "last_name"=>"Yip", "scopus_author_id"=>"55377872300"}, {"first_name"=>"Deanna L.", "last_name"=>"Gibson", "scopus_author_id"=>"14123289800"}], "year"=>2013, "source"=>"PLoS ONE", "identifiers"=>{"scopus"=>"2-s2.0-84873563309", "sgr"=>"84873563309", "issn"=>"19326203", "doi"=>"10.1371/journal.pone.0055468", "pmid"=>"23405155", "isbn"=>"1932-6203", "pui"=>"368304373"}, "id"=>"0c9bc1f6-1b27-3aef-87bd-26632cde8cbe", "abstract"=>"Clinically, excessive ω-6 polyunsaturated fatty acid (PUFA) and inadequate ω-3 PUFA have been associated with enhanced risks for developing ulcerative colitis. In rodent models, ω-3 PUFAs have been shown to either attenuate or exacerbate colitis in different studies. We hypothesized that a high ω-6: ω-3 PUFA ratio would increase colitis susceptibility through the microbe-immunity nexus. To address this, we fed post-weaned mice diets rich in ω-6 PUFA (corn oil) and diets supplemented with ω-3 PUFA (corn oil+fish oil) for 5 weeks. We evaluated the intestinal microbiota, induced colitis with Citrobacter rodentium and followed disease progression. We found that ω-6 PUFA enriched the microbiota with Enterobacteriaceae, Segmented Filamentous Bacteria and Clostridia spp., all known to induce inflammation. During infection-induced colitis, ω-6 PUFA fed mice had exacerbated intestinal damage, immune cell infiltration, prostaglandin E2 expression and C. rodentium translocation across the intestinal mucosae. Addition of ω-3 PUFA on a high ω-6 PUFA diet, reversed inflammatory-inducing microbial blooms and enriched beneficial microbes like Lactobacillus and Bifidobacteria, reduced immune cell infiltration and impaired cytokine/chemokine induction during infection. While, ω-3 PUFA supplementation protected against severe colitis, these mice suffered greater mortality associated with sepsis-related serum factors such as LPS binding protein, IL-15 and TNF-α. These mice also demonstrated decreased expression of intestinal alkaline phosphatase and an inability to dephosphorylate LPS. Thus, the colonic microbiota is altered differentially through varying PUFA composition, conferring altered susceptibility to colitis. Overall, ω-6 PUFA enriches pro-inflammatory microbes and augments colitis; but prevents infection-induced systemic inflammation. In contrast, ω-3 PUFA supplementation reverses the effects of the ω-6 PUFA diet but impairs infection-induced responses resulting in sepsis. We conclude that as an anti-inflammatory agent, ω-3 PUFA supplementation during infection may prove detrimental when host inflammatory responses are critical for survival.", "link"=>"http://www.mendeley.com/research/fish-oil-attenuates-omega6-polyunsaturated-fatty-acidinduced-dysbiosis-infectious-colitis-impairs-lp", "reader_count"=>106, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>6, "Researcher"=>25, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>20, "Student > Postgraduate"=>7, "Other"=>8, "Student > Master"=>16, "Student > Bachelor"=>18, "Lecturer > Senior Lecturer"=>2, "Professor"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>6, "Researcher"=>25, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>20, "Student > Postgraduate"=>7, "Other"=>8, "Student > Master"=>16, "Student > Bachelor"=>18, "Lecturer > Senior Lecturer"=>2, "Professor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>8, "Agricultural and Biological Sciences"=>41, "Veterinary Science and Veterinary Medicine"=>1, "Chemistry"=>2, "Computer Science"=>1, "Earth and Planetary Sciences"=>1, "Nursing and Health Professions"=>9, "Biochemistry, Genetics and Molecular Biology"=>6, "Materials Science"=>1, "Medicine and Dentistry"=>25, "Sports and Recreations"=>1, "Psychology"=>3, "Immunology and Microbiology"=>7}, "reader_count_by_subdiscipline"=>{"Materials Science"=>{"Materials Science"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>25}, "Sports and Recreations"=>{"Sports and Recreations"=>1}, "Psychology"=>{"Psychology"=>3}, "Unspecified"=>{"Unspecified"=>8}, "Chemistry"=>{"Chemistry"=>2}, "Earth and Planetary Sciences"=>{"Earth and Planetary Sciences"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>7}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>41}, "Computer Science"=>{"Computer Science"=>1}, "Nursing and Health Professions"=>{"Nursing and Health Professions"=>9}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>6}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>1}}, "reader_count_by_country"=>{"Netherlands"=>1, "United States"=>3, "United Kingdom"=>3, "South Africa"=>1}, "group_count"=>7}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/494147"], "description"=>"<p>LPS binding protein, TNF-α and IL-15 were measured in sera from in mice that had been fed the various diets both before and after infection with <i>C. rodentium</i>. (*, <i>P</i><0.05).</p>", "links"=>[], "tags"=>["pufa", "diets", "resulted", "induction", "lps", "binding", "was", "supplemented", "induced", "infection-induced", "septic"], "article_id"=>164645, "categories"=>["Microbiology", "Chemistry", "Infectious Diseases", "Immunology"], "users"=>["Sanjoy Ghosh", "Daniella DeCoffe", "Kirsty Brown", "Ethendhar Rajendiran", "Mehrbod Estaki", "Chuanbin Dai", "Ashley Yip", "Deanna L. Gibson"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0055468.g006", "stats"=>{"downloads"=>1, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_While_969_6_PUFA_rich_diets_resulted_in_the_induction_of_LPS_binding_protein_prior_to_infection_it_was_the_969_3_PUFA_supplemented_diet_that_induced_infection_induced_septic_responses_/164645", "title"=>"While ω-6 PUFA rich diets resulted in the induction of LPS binding protein prior to infection, it was the ω-3 PUFA supplemented diet that induced infection-induced septic responses.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-19 15:51:31"}
  • {"files"=>["https://ndownloader.figshare.com/files/493530"], "description"=>"<p>A) C57BL/6 mice fed ω-6 PUFA rich diets supplemented with ω-3 PUFA suffered increased mortality during infection with <i>C. rodentium</i>. 30% of mice fed ω-3 PUFA required euthanization by 6–8 days p.i., in contrast to the low or high-fat ω-6 PUFA groups. B) While both low or high-fat ω-6 PUFA diets result in similar weight changes during infection with <i>C. rodentium</i>, the ω-3 PUFA supplemented group suffered significantly increased cachexia throughout days 5–10 p.i. C) Mice fed ω-6 PUFA rich diets had the highest induction of histopathologic severity during <i>C. rodentium</i>-induced colitis while ω-3 PUFA supplementation reduced this. D) Representative colon sections from diet groups were taken at 100× magnification and stitched together using Metamorph software (black scale bar = 46.5 µm) or 200× magnification (white scale bar = 20.7 µm). E) Colonic tissue sections were stained for TUNEL-positive cells. Colons from mice fed low and high-fat ω-6 PUFA diets showed increased cell death compared to mice fed diets supplemented with ω-3 PUFA. (*, <i>P</i><0.05).</p>", "links"=>[], "tags"=>["pufa", "supplementation", "prevents", "induced", "histopathologic", "mice", "suffered", "morbidity"], "article_id"=>164039, "categories"=>["Microbiology", "Chemistry", "Infectious Diseases", "Immunology"], "users"=>["Sanjoy Ghosh", "Daniella DeCoffe", "Kirsty Brown", "Ethendhar Rajendiran", "Mehrbod Estaki", "Chuanbin Dai", "Ashley Yip", "Deanna L. Gibson"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0055468.g002", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_While_3_PUFA_supplementation_prevents_6_PUFA_induced_histopathologic_severity_these_mice_suffered_increased_mortality_and_morbidity_during_C_rodentium_infection_/164039", "title"=>"While ω-3 PUFA supplementation prevents ω-6 PUFA induced histopathologic severity, these mice suffered increased mortality and morbidity during <i>C. rodentium</i> infection.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-19 15:48:13"}
  • {"files"=>["https://ndownloader.figshare.com/files/493822"], "description"=>"<p>qPCR analysis of colonic tissues revealed that both high and low ω-6 PUFA diets were relatively similar where infection induced cytokine and the chemokine Relm-β responses. However, the ω-3 PUFA supplemented diet had impaired IFN-γ, TNF-α, IL-17A, IL-22 and IL-23, as well as the Relm-β responses evident by the lack of their induction during infection. (*, <i>P</i><0.05; **, <i>P</i><0.005).</p>", "links"=>[], "tags"=>["pufa", "supplementation", "diets", "impairs", "infection-induced", "cytokine", "chemokine"], "article_id"=>164328, "categories"=>["Microbiology", "Chemistry", "Infectious Diseases", "Immunology"], "users"=>["Sanjoy Ghosh", "Daniella DeCoffe", "Kirsty Brown", "Ethendhar Rajendiran", "Mehrbod Estaki", "Chuanbin Dai", "Ashley Yip", "Deanna L. Gibson"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0055468.g004", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_969_3_PUFA_supplementation_to_969_6_PUFA_rich_diets_impairs_infection_induced_cytokine_and_chemokine_responses_/164328", "title"=>"ω-3 PUFA supplementation to ω-6 PUFA rich diets impairs infection-induced cytokine and chemokine responses.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-19 15:49:49"}
  • {"files"=>["https://ndownloader.figshare.com/files/494360"], "description"=>"<p>Major fatty acid compositions of dietary oil used in preparing high-fat diets.</p>", "links"=>[], "tags"=>["fatty", "compositions", "dietary", "preparing", "high-fat"], "article_id"=>164873, "categories"=>["Microbiology", "Chemistry", "Infectious Diseases", "Immunology"], "users"=>["Sanjoy Ghosh", "Daniella DeCoffe", "Kirsty Brown", "Ethendhar Rajendiran", "Mehrbod Estaki", "Chuanbin Dai", "Ashley Yip", "Deanna L. Gibson"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0055468.t001", "stats"=>{"downloads"=>1, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Major_fatty_acid_compositions_of_dietary_oil_used_in_preparing_high_fat_diets_/164873", "title"=>"Major fatty acid compositions of dietary oil used in preparing high-fat diets.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-02-19 15:52:39"}
  • {"files"=>["https://ndownloader.figshare.com/files/494249"], "description"=>"<p>A) IAP+ cells were highest in ω-6 PUFA rich diet groups during infection and ω-3 PUFA supplementation impaired this response. Colon sections were stained for the presence of IAP+ cells and quantified. Representative immunofluorescence images are shown at 200× magnification (scale bar = 13.6 µm). B) While both the low and high ω-6 PUFA rich diet groups showed an induction of LPS-dephosphorylating activity during infection induced colitis, theω-3 PUFA supplementation fed mice were unable to dephosphorylate LPS in response to infection. Colonic tissues were homogenized, supernatant collected and LPS incubated with each diet group for 2 hours. A colorimetric malachite green solution was used to measure absorbance at 620 nm and the LPS-dephosphorylating activity/mg of protein was determined for each diet group. (*, <i>P</i><0.05; **, <i>P</i><0.005).</p>", "links"=>[], "tags"=>["pufa", "supplementation", "diets", "resulted", "impaired", "infection-induced", "intestinal", "alkaline", "phosphatase"], "article_id"=>164752, "categories"=>["Microbiology", "Chemistry", "Infectious Diseases", "Immunology"], "users"=>["Sanjoy Ghosh", "Daniella DeCoffe", "Kirsty Brown", "Ethendhar Rajendiran", "Mehrbod Estaki", "Chuanbin Dai", "Ashley Yip", "Deanna L. Gibson"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0055468.g007", "stats"=>{"downloads"=>1, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_969_3_PUFA_supplementation_to_969_6_PUFA_rich_diets_resulted_in_impaired_infection_induced_intestinal_alkaline_phosphatase_activity_/164752", "title"=>"ω-3 PUFA supplementation to ω-6 PUFA rich diets resulted in impaired infection-induced intestinal alkaline phosphatase activity.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-19 15:52:05"}
  • {"files"=>["https://ndownloader.figshare.com/files/493700"], "description"=>"<p>While ω-6 PUFA rich diets induced the infiltration of macrophages, neutrophils and PGE2 inflammatory cells, ω-3 PUFA supplementation prevented the enhanced infiltration during infection. Colon sections were stained for the presence of submucosal A) F4/80+ macrophages B) MPO+ neutrophils and C) PGE2+ cells and quantified. Representative immunofluorescence images are shown at 200× magnification. (scale bar = 13.6 µm; *, <i>P</i><0.05).</p>", "links"=>[], "tags"=>["pufa", "supplementation", "diets", "impairs", "intestinal", "inflammatory", "infiltration"], "article_id"=>164209, "categories"=>["Microbiology", "Chemistry", "Infectious Diseases", "Immunology"], "users"=>["Sanjoy Ghosh", "Daniella DeCoffe", "Kirsty Brown", "Ethendhar Rajendiran", "Mehrbod Estaki", "Chuanbin Dai", "Ashley Yip", "Deanna L. Gibson"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0055468.g003", "stats"=>{"downloads"=>0, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_3_PUFA_supplementation_to_6_PUFA_rich_diets_impairs_intestinal_inflammatory_cell_infiltration_during_C_rodentium_induced_colitis_/164209", "title"=>"ω-3 PUFA supplementation to ω-6 PUFA rich diets impairs intestinal inflammatory cell infiltration during <i>C. rodentium-</i>induced colitis.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-19 15:49:10"}
  • {"files"=>["https://ndownloader.figshare.com/files/493989"], "description"=>"<p>A) Colonic tissue sections were hybridized with a γ-Proteobacteria probe (green) and the nuclei stained with DAPI (blue) to examine the locations of Enterobacteriaceae. These Gram-negative microbes were found in the submucosae (600× magnification scale bar = 14.2 µm) prior to infection in the colons of mice fed ω-6 PUFA rich diets. During infection with <i>C. rodentium</i>, a member of Enterobacteriaceae, the pathogen was found deep into the crypts (100× magnification, scale bar = 85.4 µm; upper panel) and in the submucosae (600× magnification scale bar = 14.2 µm) in the colons of mice fed ω-6 PUFA rich diets. B) Colony forming units (CFU) recovered from the spleen and mesenteric lymph nodes (MLN) were highest from mice fed ω-6 PUFA rich diets after 10 days of <i>C. rodentium</i> infection. CFU were enumerated from tissues removed from mice fed various diets and were homogenized followed by plating in serial dilutions on Lb agar. (*, <i>P</i><0.05).</p>", "links"=>[], "tags"=>["pufa", "diets", "resulted", "translocation", "microbes", "enterobacteriacea", "intestinal"], "article_id"=>164497, "categories"=>["Microbiology", "Chemistry", "Infectious Diseases", "Immunology"], "users"=>["Sanjoy Ghosh", "Daniella DeCoffe", "Kirsty Brown", "Ethendhar Rajendiran", "Mehrbod Estaki", "Chuanbin Dai", "Ashley Yip", "Deanna L. Gibson"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0055468.g005", "stats"=>{"downloads"=>2, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_969_6_PUFA_rich_diets_resulted_in_increased_translocation_of_microbes_from_Enterobacteriacea_across_the_intestinal_mucosae_/164497", "title"=>"ω-6 PUFA rich diets resulted in increased translocation of microbes from Enterobacteriacea across the intestinal mucosae.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-19 15:50:42"}
  • {"files"=>["https://ndownloader.figshare.com/files/494406"], "description"=>"1<p>Mineral mix (mg/g): di calcium phosphate 500, magnesium oxide 24; potassium citrate 220, potassium sulfate 52; sodium chloride 74, chromium KSO<sub>4</sub> 12H<sub>2</sub>0 0.55; cupric carbonate 0.3, potassium iodate 0.01; ferric citrate 6, manganous carbonate 3.5, sodium selenite 0.01, zinc carbonate 1.6; sucrose 118.03.</p>2<p>Vitamin Mix (mg/g): vitamin A 0.8; vitamin D<sub>3</sub> 1; vitamin E 10; menadione sodium bisulfite 0.08; nicotinic acid 3; calcium pantothenate 1.6; pyridoxine HCl 0.7; riboflavin 0.6; thiamin 0.6; sucrose 978.42.</p>3<p>Added to meet essential fatty acid requirements for all groups.</p>", "links"=>[], "tags"=>["high-fat"], "article_id"=>164924, "categories"=>["Microbiology", "Chemistry", "Infectious Diseases", "Immunology"], "users"=>["Sanjoy Ghosh", "Daniella DeCoffe", "Kirsty Brown", "Ethendhar Rajendiran", "Mehrbod Estaki", "Chuanbin Dai", "Ashley Yip", "Deanna L. Gibson"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0055468.t002", "stats"=>{"downloads"=>5, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Composition_of_high_fat_diets_/164924", "title"=>"Composition of high-fat diets.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-02-19 15:52:52"}
  • {"files"=>["https://ndownloader.figshare.com/files/493316"], "description"=>"<p>A) ω-6 PUFA rich diets promote a microbiota enriched with Enterobacteriacea, Segmented Filamentous Bacteria (SFB) and microbes from the <i>Clostridia coccoides</i> group and ω-3 supplementation reverses this and B) enriches <i>Bifidobacteria</i> spp., <i>Lactobacillus</i> spp. and <i>Enterococcus faecium</i>. C) High-fat diet groups resulted in decreased <i>Bacteroides</i> spp. and <i>Enterococcus faecalis</i>. Expression is relative to the low ω-6 PUFA group. (*, <i>P</i><0.05).</p>", "links"=>[], "tags"=>["pufa", "diets", "induce", "dysbiosis", "supplementation", "reverses", "blooms", "enriching", "beneficial"], "article_id"=>163805, "categories"=>["Microbiology", "Chemistry", "Infectious Diseases", "Immunology"], "users"=>["Sanjoy Ghosh", "Daniella DeCoffe", "Kirsty Brown", "Ethendhar Rajendiran", "Mehrbod Estaki", "Chuanbin Dai", "Ashley Yip", "Deanna L. Gibson"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0055468.g001", "stats"=>{"downloads"=>2, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_969_6_PUFA_rich_diets_induce_dysbiosis_and_969_3_PUFA_supplementation_reverses_these_blooms_while_enriching_beneficial_microbes_/163805", "title"=>"ω-6 PUFA rich diets induce dysbiosis and ω-3 PUFA supplementation reverses these blooms while enriching beneficial microbes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-19 15:46:59"}

PMC Usage Stats | Further Information

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Relative Metric

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