Butyrate Enhances Disease Resistance of Chickens by Inducing Antimicrobial Host Defense Peptide Gene Expression
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{"title"=>"Butyrate enhances disease resistance of chickens by inducing antimicrobial host defense peptide gene expression", "type"=>"journal", "authors"=>[{"first_name"=>"Lakshmi T.", "last_name"=>"Sunkara", "scopus_author_id"=>"35849315700"}, {"first_name"=>"Mallika", "last_name"=>"Achanta", "scopus_author_id"=>"35848086800"}, {"first_name"=>"Nicole B.", "last_name"=>"Schreiber", "scopus_author_id"=>"35767241900"}, {"first_name"=>"Yugendar R.", "last_name"=>"Bommineni", "scopus_author_id"=>"13402849700"}, {"first_name"=>"Gan", "last_name"=>"Dai", "scopus_author_id"=>"7202576785"}, {"first_name"=>"Weiyu", "last_name"=>"Jiang", "scopus_author_id"=>"55483649100"}, {"first_name"=>"Susan", "last_name"=>"Lamont", "scopus_author_id"=>"7006579349"}, {"first_name"=>"Hyun S.", "last_name"=>"Lillehoj", "scopus_author_id"=>"7005236112"}, {"first_name"=>"Ali", "last_name"=>"Beker", "scopus_author_id"=>"6603638269"}, {"first_name"=>"Robert G.", "last_name"=>"Teeter", "scopus_author_id"=>"7005832306"}, {"first_name"=>"Guolong", "last_name"=>"Zhang", "scopus_author_id"=>"7405270549"}], "year"=>2011, "source"=>"PLoS ONE", "identifiers"=>{"sgr"=>"80455149886", "doi"=>"10.1371/journal.pone.0027225", "pmid"=>"22073293", "issn"=>"19326203", "scopus"=>"2-s2.0-80455149886", "pui"=>"362874152"}, "id"=>"0f100fac-14cf-3bdd-8258-99b082d009f9", "abstract"=>"Host defense peptides (HDPs) constitute a large group of natural broad-spectrum antimicrobials and an important first line of immunity in virtually all forms of life. Specific augmentation of synthesis of endogenous HDPs may represent a promising antibiotic-alternative approach to disease control. In this study, we tested the hypothesis that exogenous administration of butyrate, a major type of short-chain fatty acids derived from bacterial fermentation of undigested dietary fiber, is capable of inducing HDPs and enhancing disease resistance in chickens. We have found that butyrate is a potent inducer of several, but not all, chicken HDPs in HD11 macrophages as well as in primary monocytes, bone marrow cells, and jejuna and cecal explants. In addition, butyrate treatment enhanced the antibacterial activity of chicken monocytes against Salmonella enteritidis, with a minimum impact on inflammatory cytokine production, phagocytosis, and oxidative burst capacities of the cells. Furthermore, feed supplementation with 0.1% butyrate led to a significant increase in HDP gene expression in the intestinal tract of chickens. More importantly, such a feeding strategy resulted in a nearly 10-fold reduction in the bacterial titer in the cecum following experimental infections with S. enteritidis. Collectively, the results indicated that butyrate-induced synthesis of endogenous HDPs is a phylogenetically conserved mechanism of innate host defense shared by mammals and aves, and that dietary supplementation of butyrate has potential for further development as a convenient antibiotic-alternative strategy to enhance host innate immunity and disease resistance.", "link"=>"http://www.mendeley.com/research/butyrate-enhances-disease-resistance-chickens-inducing-antimicrobial-host-defense-peptide-gene-expre", "reader_count"=>44, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Professor > Associate Professor"=>1, "Student > Doctoral Student"=>3, "Researcher"=>10, "Student > Ph. D. Student"=>12, "Student > Postgraduate"=>3, "Student > Master"=>9, "Other"=>1, "Student > Bachelor"=>1, "Lecturer > Senior Lecturer"=>1, "Professor"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Professor > Associate Professor"=>1, "Student > Doctoral Student"=>3, "Researcher"=>10, "Student > Ph. D. Student"=>12, "Student > Postgraduate"=>3, "Student > Master"=>9, "Other"=>1, "Student > Bachelor"=>1, "Lecturer > Senior Lecturer"=>1, "Professor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>2, "Engineering"=>1, "Environmental Science"=>1, "Biochemistry, Genetics and Molecular Biology"=>2, "Agricultural and Biological Sciences"=>23, "Medicine and Dentistry"=>6, "Pharmacology, Toxicology and Pharmaceutical Science"=>1, "Veterinary Science and Veterinary Medicine"=>2, "Chemistry"=>2, "Computer Science"=>1, "Immunology and Microbiology"=>3}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>6}, "Chemistry"=>{"Chemistry"=>2}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>3}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>23}, "Computer Science"=>{"Computer Science"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>2}, "Unspecified"=>{"Unspecified"=>2}, "Environmental Science"=>{"Environmental Science"=>1}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>2}}, "reader_count_by_country"=>{"Colombia"=>1, "United States"=>1, "Slovenia"=>1, "Switzerland"=>1}, "group_count"=>1}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/715988"], "description"=>"<p>In the phagocytosis assay, chicken HD11 macrophage cells were incubated with different concentrations of butyrate in duplicate for 24 h, followed by exposure to <i>S. enteritidis</i> phage type 13a for 30 min at 37°C in the presence of 5% chicken serum. Extracellular bacteria were then killed by gentamicin, and internalized bacteria were enumerated from lyzed HD11 cells by serial plating on Brilliant Green agar plates containing 20 µg/ml nalidixic acid overnight at 37°C. In the oxidative burst assay, HD11 cells were stimulated with indicated concentrations of butyrate for 24 h. The fluorescence was monitored at 485 nm excitation and 528 nm emission following 1 h incubation with 2′,7′-dichlorodihydrofluorescein diacetate (DCFA) in the presence or absence of phorbol 12-myristate 13-acetate (PMA). The results were normalized against protein concentrations of each sample. The bars represent means ± standard error of the data from two independent experiments.</p>", "links"=>[], "tags"=>["butyrate", "phagocytic", "oxidative", "activities", "hd11"], "article_id"=>386334, "categories"=>["Microbiology", "Infectious Diseases", "Immunology"], "users"=>["Lakshmi T. Sunkara", "Mallika Achanta", "Nicole B. Schreiber", "Yugendar R. Bommineni", "Gan Dai", "Weiyu Jiang", "Susan Lamont", "Hyun S. Lillehoj", "Ali Beker", "Robert G. Teeter", "Guolong Zhang"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0027225.g007", "stats"=>{"downloads"=>4, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_No_impact_of_butyrate_on_phagocytic_A_or_oxidative_burst_activities_B_of_HD11_cells_/386334", "title"=>"No impact of butyrate on phagocytic (A) or oxidative burst activities (B) of HD11 cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 11:59:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/716065"], "description"=>"<p>HD11 cells were incubated with 4 mM butyrate, 1 µg/ml LPS or left untreated for 24 h, followed by flow cytometric analysis of surface expression of MHC class I and II using fluorescein isothiocyanate (FITC)-conjugated anti-chicken MHC class I and R-phycoerythrin (R-PE)-conjugated anti-chicken MHC class II monoclonal antibodies. The data shown are representative of two independent experiments.</p>", "links"=>[], "tags"=>["activation", "hd11", "cells"], "article_id"=>386407, "categories"=>["Microbiology", "Infectious Diseases", "Immunology"], "users"=>["Lakshmi T. Sunkara", "Mallika Achanta", "Nicole B. Schreiber", "Yugendar R. Bommineni", "Gan Dai", "Weiyu Jiang", "Susan Lamont", "Hyun S. Lillehoj", "Ali Beker", "Robert G. Teeter", "Guolong Zhang"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0027225.g008", "stats"=>{"downloads"=>0, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_No_influence_on_the_activation_status_of_HD11_cells_by_butyrate_/386407", "title"=>"No influence on the activation status of HD11 cells by butyrate.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 11:59:47"}
  • {"files"=>["https://ndownloader.figshare.com/files/715493"], "description"=>"<p>HD11 macrophage cells were incubated in duplicate with 4 mM sodium butyrate for indicated time points (A) or indicated concentrations of butyrate for 24 h (B). Chicken primary monocytes (C) or bone marrow cells (D) were exposed to different concentrations of butyrate in duplicate for 24 h prior to isolation of total RNA. The <i>AvBD9</i> gene expression was analyzed by real-time RT-PCR, and the relative fold increase over the control group was calculated using the comparative ΔΔCt method and the <i>GAPDH</i> gene for normalization. The bars represent means ± standard error of the data from 2–3 independent experiments.</p>", "links"=>[], "tags"=>["immunology", "Infectious diseases", "microbiology"], "article_id"=>385832, "categories"=>["Microbiology", "Infectious Diseases", "Immunology"], "users"=>["Lakshmi T. Sunkara", "Mallika Achanta", "Nicole B. Schreiber", "Yugendar R. Bommineni", "Gan Dai", "Weiyu Jiang", "Susan Lamont", "Hyun S. Lillehoj", "Ali Beker", "Robert G. Teeter", "Guolong Zhang"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0027225.g001", "stats"=>{"downloads"=>1, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Butyrate_induced_expression_of_the_AvBD9_gene_in_different_chicken_cell_types_/385832", "title"=>"Butyrate-induced expression of the <i>AvBD9</i> gene in different chicken cell types.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 11:56:42"}
  • {"files"=>["https://ndownloader.figshare.com/files/715744"], "description"=>"<p>Two-day-old male Cornish Rock broilers were fed with standard ration with or without supplementation of 0.1% and 0.2% butyrate for 2 days. The crop, cecal tonsil, and cecum were collected from each chicken and the <i>AvBD9</i> gene expression was evaluated by real-time PCR. Each bar represents means ± standard error of the data from 6 different chickens. * P<0.05 by unpaired Student's <i>t</i>-test.</p>", "links"=>[], "tags"=>["vivo", "induction", "intestinal", "tract", "chickens"], "article_id"=>386087, "categories"=>["Microbiology", "Infectious Diseases", "Immunology"], "users"=>["Lakshmi T. Sunkara", "Mallika Achanta", "Nicole B. Schreiber", "Yugendar R. Bommineni", "Gan Dai", "Weiyu Jiang", "Susan Lamont", "Hyun S. Lillehoj", "Ali Beker", "Robert G. Teeter", "Guolong Zhang"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0027225.g004", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_In_vivo_induction_of_the_AvBD9_gene_expression_in_the_intestinal_tract_of_chickens_by_butyrate_/386087", "title"=>"In vivo induction of the <i>AvBD9</i> gene expression in the intestinal tract of chickens by butyrate.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 11:58:08"}
  • {"files"=>["https://ndownloader.figshare.com/files/715815"], "description"=>"<p>Chicken HD11 macrophage cells were incubated with indicated concentrations of butyrate or 1 µg/ml LPS in duplicate for 3 and 24 h, followed by real-time PCR analysis of the gene expressions of <i>IL-1β</i> (A), <i>IL-12p40</i> (B), and <i>IL-8</i> (C). The bars represent means ± standard error of the data from two independent experiments. Essentially no induction of <i>IL-1</i> and <i>IL-12p40</i> was observed at both 3 and 24 h after butyrate stimulation, with moderate induction of <i>IL-8</i> occurring only following butyrate treatment for 24 h.</p>", "links"=>[], "tags"=>["triggering", "proinflammatory", "cytokine", "synthesis", "hd11", "cells"], "article_id"=>386161, "categories"=>["Microbiology", "Infectious Diseases", "Immunology"], "users"=>["Lakshmi T. Sunkara", "Mallika Achanta", "Nicole B. Schreiber", "Yugendar R. Bommineni", "Gan Dai", "Weiyu Jiang", "Susan Lamont", "Hyun S. Lillehoj", "Ali Beker", "Robert G. Teeter", "Guolong Zhang"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0027225.g005", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Minimum_triggering_of_proinflammatory_cytokine_synthesis_in_HD11_cells_by_butyrate_/386161", "title"=>"Minimum triggering of proinflammatory cytokine synthesis in HD11 cells by butyrate.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 11:58:30"}
  • {"files"=>["https://ndownloader.figshare.com/files/715647"], "description"=>"<p>Chicken jejunum and cecal explants were obtained by culturing slices of 0.5 cm long segments, followed by incubation with indicated concentrations of butyrate in duplicate for 24 h. Real time RT-PCR was performed and the relative fold increase over the control group was calculated using the comparative ΔΔCt method and the <i>GAPDH</i> gene for normalization. The bars represent means ± standard error of the data from two independent experiments.</p>", "links"=>[], "tags"=>["hdps", "jejunal", "cecal", "explants"], "article_id"=>385999, "categories"=>["Microbiology", "Infectious Diseases", "Immunology"], "users"=>["Lakshmi T. Sunkara", "Mallika Achanta", "Nicole B. Schreiber", "Yugendar R. Bommineni", "Gan Dai", "Weiyu Jiang", "Susan Lamont", "Hyun S. Lillehoj", "Ali Beker", "Robert G. Teeter", "Guolong Zhang"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0027225.g003", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Up_regulation_of_three_representative_HDPs_in_chicken_jejunal_A_and_cecal_explants_B_by_butyrate_/385999", "title"=>"Up-regulation of three representative HDPs in chicken jejunal (A) and cecal explants (B) by butyrate.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 11:57:39"}
  • {"files"=>["https://ndownloader.figshare.com/files/716255"], "description"=>"a<p>Primers for AvBD4-13 and GAPDH are adopted from reference 14.</p>", "links"=>[], "tags"=>["sequences", "peptides", "cytokines"], "article_id"=>386600, "categories"=>["Microbiology", "Infectious Diseases", "Immunology"], "users"=>["Lakshmi T. Sunkara", "Mallika Achanta", "Nicole B. Schreiber", "Yugendar R. Bommineni", "Gan Dai", "Weiyu Jiang", "Susan Lamont", "Hyun S. Lillehoj", "Ali Beker", "Robert G. Teeter", "Guolong Zhang"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0027225.t001", "stats"=>{"downloads"=>1, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Primer_sequences_of_chicken_host_defense_peptides_and_cytokines_for_real_time_PCR_a_/386600", "title"=>"Primer sequences of chicken host defense peptides and cytokines for real time PCR<sup>a</sup>.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-02-20 12:00:46"}
  • {"files"=>["https://ndownloader.figshare.com/files/715582"], "description"=>"<p>Chicken HD11 macrophage cells and primary monocytes were incubated in duplicate with and without different concentrations of butyrate for 24 h, followed by RNA isolation and real-time RT-PCR analysis of all 14 chicken β-defensins (<i>AvBDs</i>) and 4 cathelicidins (<i>fowlicidins 1–3</i> and <i>cathelicidin B1</i>). The color elements represent average log<sub>2</sub> ratios of fold change from 2–3 independent experiments. Red indicates up-regulation, whereas black means no induction and green down-regulation. Gray areas are an indication of no data due to extremely low expression levels of certain HDPs in primary monocytes. Three groups of chicken HDPs, namely generally induced (I), non-regulatable (II), and generally down-regulated (III), can be classified according to their mode of modulation by butyrate. <i>AvBD11</i>, <i>AvBD12</i>, and <i>AvBD13</i> could not be reliably detected in either cell type, and therefore, were not shown. The heat map was generating by using MultiExperiment Viewer <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0027225#pone.0027225-Saeed1\" target=\"_blank\">[48]</a>.</p>", "links"=>[], "tags"=>["hdp", "hd11", "macrophages"], "article_id"=>385931, "categories"=>["Microbiology", "Infectious Diseases", "Immunology"], "users"=>["Lakshmi T. Sunkara", "Mallika Achanta", "Nicole B. Schreiber", "Yugendar R. Bommineni", "Gan Dai", "Weiyu Jiang", "Susan Lamont", "Hyun S. Lillehoj", "Ali Beker", "Robert G. Teeter", "Guolong Zhang"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0027225.g002", "stats"=>{"downloads"=>1, "page_views"=>23, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Induction_of_HDP_gene_expression_in_chicken_HD11_macrophages_and_primary_monocytes_/385931", "title"=>"Induction of HDP gene expression in chicken HD11 macrophages and primary monocytes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 11:57:16"}
  • {"files"=>["https://ndownloader.figshare.com/files/716141"], "description"=>"<p>In trial 1 (A), 5-day old male broilers were equally divided into two groups of 10 and fed with a standard antibiotic-free diet mixed with and without 0.2% sodium butyrate for 2 days. Birds were then inoculated with 1×10<sup>6</sup> CFU of <i>S. enteritidis</i> phage type 13a and continued with butyrate feeding for another 4 days. The <i>S. enteritidis</i> titer in the cecal content was quantitated from each animal by serial plating on Brilliant Green agar plates containing 20 µg/ml nalidixic acid. Trial 2 (B) was similarly conducted with an additional group of 10 broilers fed with 0.1% butyrate. Each dot represents the bacterial titer from a bird and the solid line represents the median value of each treatment. Brackets indicate the statistical significance of differences (*<i>P</i> = 0.03, unpaired Student's <i>t</i>-test).</p>", "links"=>[], "tags"=>["titer", "cecal", "contents", "chickens", "supplementation"], "article_id"=>386487, "categories"=>["Microbiology", "Infectious Diseases", "Immunology"], "users"=>["Lakshmi T. Sunkara", "Mallika Achanta", "Nicole B. Schreiber", "Yugendar R. Bommineni", "Gan Dai", "Weiyu Jiang", "Susan Lamont", "Hyun S. Lillehoj", "Ali Beker", "Robert G. Teeter", "Guolong Zhang"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0027225.g009", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Reduction_of_the_S_enteritidis_titer_in_the_cecal_contents_of_chickens_following_oral_supplementation_of_butyrate_/386487", "title"=>"Reduction of the <i>S. enteritidis</i> titer in the cecal contents of chickens following oral supplementation of butyrate.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 12:00:09"}
  • {"files"=>["https://ndownloader.figshare.com/files/715909"], "description"=>"<p>Chicken monocytes were treated with or without different concentrations of butyrate for 24 h. Cell lysates were then prepared and incubated with <i>S. enteritidis</i> (ATCC 13076) for 9 h at 37°C. Bacterial turbidity at OD<sub>590 nm</sub> was measured as an indication of the bacterial density. <i>S. enteritidis</i> was also directly incubated with different concentrations of butyrate in cell culture medium alone without monocytes as controls (white bars). The bars represent means ± standard error of the data from two independent experiments.</p>", "links"=>[], "tags"=>["antibacterial", "monocytes", "stimulation"], "article_id"=>386258, "categories"=>["Microbiology", "Infectious Diseases", "Immunology"], "users"=>["Lakshmi T. Sunkara", "Mallika Achanta", "Nicole B. Schreiber", "Yugendar R. Bommineni", "Gan Dai", "Weiyu Jiang", "Susan Lamont", "Hyun S. Lillehoj", "Ali Beker", "Robert G. Teeter", "Guolong Zhang"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0027225.g006", "stats"=>{"downloads"=>1, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Augmentation_of_the_antibacterial_activity_of_monocytes_following_stimulation_with_butyrate_/386258", "title"=>"Augmentation of the antibacterial activity of monocytes following stimulation with butyrate.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 11:59:00"}

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