{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,18]],"date-time":"2026-08-18T04:37:51Z","timestamp":1787027871299,"version":"build-2736575974"},"reference-count":71,"publisher":"MDPI AG","issue":"21","license":[{"start":{"date-parts":[[2025,11,6]],"date-time":"2025-11-06T00:00:00Z","timestamp":1762387200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100000268","name":"Biotechnology and Biological Sciences Research Council, UK","doi-asserted-by":"publisher","award":["BB\/T020954\/2"],"award-info":[{"award-number":["BB\/T020954\/2"]}],"id":[{"id":"10.13039\/501100000268","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000268","name":"Biotechnology and Biological Sciences Research Council, UK","doi-asserted-by":"publisher","award":["BB\/T020954\/1"],"award-info":[{"award-number":["BB\/T020954\/1"]}],"id":[{"id":"10.13039\/501100000268","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000268","name":"Biotechnology and Biological Sciences Research Council, UK","doi-asserted-by":"publisher","award":["BB\/S01506X\/1"],"award-info":[{"award-number":["BB\/S01506X\/1"]}],"id":[{"id":"10.13039\/501100000268","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000268","name":"Biotechnology and Biological Sciences Research Council, UK","doi-asserted-by":"publisher","award":["BBS\/E\/I\/00007030"],"award-info":[{"award-number":["BBS\/E\/I\/00007030"]}],"id":[{"id":"10.13039\/501100000268","id-type":"DOI","asserted-by":"publisher"}]},{"name":"The British Egg Marketing Research and Education Trust, UK"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Cells"],"abstract":"<jats:p>Sodium butyrate has been documented to support gut function and help control pathogens in the gastrointestinal tract. However, the precise mechanisms of dietary sodium butyrate\u2019s control over enteric pathogens in chickens remain unclear. Our study demonstrated that priming chicken bone marrow-derived macrophages (BMDMs) or the HD11 cell line with 1 mM sodium butyrate significantly enhanced their antimicrobial capacity against key bacterial pathogens (Escherichia coli, Salmonella Typhimurium, Pseudomonas aeruginosa, and Staphylococcus aureus) in gentamicin protection assays (p &lt; 0.05; \u22651 log reduction in CFU\/mL). This in vitro enhancement was associated with increased production of reactive oxygen species (ROS), as detected by DCFH-DA assays, showing approximately a 30% increase in HD11 cells and a 12% increase in BMDMs. Butyrate priming was observed to result in autophagy activation, potentially through mTOR pathway inhibition, evidenced by changes in related gene expression using RT-qPCR assay and a 2.5-fold increase in GFP-LC3B accumulation. Supporting this, pharmacological inhibition of ROS using the ROS scavenger N-acetyl-L-cystine (NAC) or autophagy with chloroquine reduced the butyrate-enhanced bacterial clearance. Furthermore, the mTOR inhibitor rapamycin synergized with butyrate priming, whereas the mTOR activator L-leucine counteracted enhanced antimicrobial activity. These findings offer crucial insights for improving host defence against bacterial infections and developing novel therapeutic strategies in chickens.<\/jats:p>","DOI":"10.3390\/cells14211742","type":"journal-article","created":{"date-parts":[[2025,11,6]],"date-time":"2025-11-06T17:51:43Z","timestamp":1762451503000},"page":"1742","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":3,"title":["Butyrate Enhances Antimicrobial Defence in Chicken Macrophages Through Reactive Oxygen Species Generation and Autophagy Activation"],"prefix":"10.3390","volume":"14","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-3415-2999","authenticated-orcid":false,"given":"James R. G.","family":"Adams","sequence":"first","affiliation":[{"name":"Discipline of Veterinary Clinical Sciences, School of Veterinary Medicine, Faculty of Health and Medical Sciences, University of Surrey, Guildford GU2 7AL, UK"},{"name":"The Pirbright Institute, Pirbright, Woking GU24 0NE, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Faisal R.","family":"Anjum","sequence":"additional","affiliation":[{"name":"Bristol Veterinary School, University of Bristol, Langford BS40 5DU, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9563-6348","authenticated-orcid":false,"given":"Jai W.","family":"Mehat","sequence":"additional","affiliation":[{"name":"Discipline of Microbes, Infection and Immunity, School of Biosciences, Faculty of Health and Medical Sciences, University of Surrey, Guildford GU2 7XH, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Roberto M.","family":"La Ragione","sequence":"additional","affiliation":[{"name":"Discipline of Microbes, Infection and Immunity, School of Biosciences, Faculty of Health and Medical Sciences, University of Surrey, Guildford GU2 7XH, UK"},{"name":"Discipline of Comparative Biomedical Sciences, School of Veterinary Medicine, Faculty of Health and Medical Sciences, University of Surrey, Guildford GU2 7AL, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shahriar","family":"Behboudi","sequence":"additional","affiliation":[{"name":"The Pirbright Institute, Pirbright, Woking GU24 0NE, UK"},{"name":"Bristol Veterinary School, University of Bristol, Langford BS40 5DU, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2025,11,6]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Hirayama, D., Iida, T., and Nakase, H. (2017). The Phagocytic Function of Macrophage-Enforcing Innate Immunity and Tissue Homeostasis. Int. J. Mol. Sci., 19.","DOI":"10.3390\/ijms19010092"},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Amamou, A., O\u2019mahony, C., Leboutte, M., Savoye, G., Ghosh, S., and Marion-Letellier, R. (2022). Gut Microbiota, Macrophages and Diet: An Intriguing New Triangle in Intestinal Fibrosis. Microorganisms, 10.","DOI":"10.3390\/microorganisms10030490"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"2","DOI":"10.1038\/s41590-020-00845-6","article-title":"Trained immunity, tolerance, priming and differentiation: Distinct immunological processes","volume":"22","author":"Divangahi","year":"2021","journal-title":"Nat. Immunol."},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Goonewardene, K.B., Karu, N., Ahmed, K.A., Popowich, S., Chow-Lockerbie, B., Ayalew, L.E., Karunarathna, R., Gunawardana, T., Liu, M., and Tikoo, S.K. (2021). CpG-ODN induced antimicrobial immunity in neonatal chicks involves a substantial shift in serum metabolic profiles. Sci. Rep., 11.","DOI":"10.1038\/s41598-021-88386-2"},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"Verwoolde, M.B., van den Biggelaar, R.H.G.A., van Baal, J., Jansen, C.A., and Lammers, A. (2020). Training of Primary Chicken Monocytes Results in Enhanced Pro-Inflammatory Responses. Vet. Sci., 7.","DOI":"10.20944\/preprints202007.0618.v1"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1869","DOI":"10.1093\/infdis\/jiz692","article-title":"Trained Immunity Confers Broad-Spectrum Protection Against Bacterial Infections","volume":"222","author":"Ciarlo","year":"2020","journal-title":"J. Infect. Dis."},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Funes, S.C., Rios, M., Fern\u00e1ndez-Fierro, A., Di Genaro, M.S., and Kalergis, A.M. (2022). Trained Immunity Contribution to Autoimmune and Inflammatory Disorders. Front. Immunol., 13.","DOI":"10.3389\/fimmu.2022.868343"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"232","DOI":"10.1080\/03079457.2023.2201169","article-title":"Broiler performance correlates with gut morphology and intestinal inflammation under field conditions","volume":"52","author":"Rysman","year":"2023","journal-title":"Avian Pathol."},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Singh, V., Lee, G., Son, H., Koh, H., Kim, E.S., Unno, T., and Shin, J.-H. (2022). Butyrate producers, \u201cThe Sentinel of Gut\u201d: Their intestinal significance with and beyond butyrate, and prospective use as microbial therapeutics. Front. Microbiol., 13.","DOI":"10.3389\/fmicb.2022.1103836"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"265","DOI":"10.1017\/S0043933916000210","article-title":"Sodium butyrate in chicken nutrition: The dynamics of performance, gut microbiota, gut morphology, and immunity","volume":"72","author":"Ahsan","year":"2016","journal-title":"World\u2019s Poult. Sci. J."},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Sunkara, L.T., Achanta, M., Schreiber, N.B., Bommineni, Y.R., Dai, G., Jiang, W., Lamont, S., Lillehoj, H.S., Beker, A., and Teeter, R.G. (2011). Butyrate Enhances Disease Resistance of Chickens by Inducing Antimicrobial Host Defense Peptide Gene Expression. PLoS ONE, 6.","DOI":"10.1371\/journal.pone.0027225"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1026","DOI":"10.5713\/ajas.2009.80298","article-title":"Effect of Butyric Acid on Performance, Gastrointestinal Tract Health and Carcass Characteristics in Broiler Chickens","volume":"22","author":"Panda","year":"2009","journal-title":"Asian-Australas. J. Anim. Sci."},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Aribi, M., Meziane, W., Habi, S., Boulatika, Y., Marchandin, H., and Aymeric, J.-L. (2015). Macrophage Bactericidal Activities against Staphylococcus aureus Are Enhanced In Vivo by Selenium Supplementation in a Dose-Dependent Manner. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0135515"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"2485S","DOI":"10.1093\/jn\/133.7.2485S","article-title":"Inhibition of Histone Deacetylase Activity by Butyrate","volume":"133","author":"Davie","year":"2003","journal-title":"J. Nutr."},{"key":"ref_15","first-page":"1701","article-title":"The histone deacetylase inhibitor sodium butyrate induces breast cancer cell apoptosis through diverse cytotoxic actions including glutathione depletion and oxidative stress","volume":"25","author":"Louis","year":"2004","journal-title":"Int. J. Oncol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"128","DOI":"10.1016\/j.immuni.2013.12.007","article-title":"Activation of Gpr109a, Receptor for niacin and the commensal metabolite butyrate, suppresses colonic inflammation and carcinogenesis","volume":"40","author":"Singh","year":"2014","journal-title":"Immunity"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"11312","DOI":"10.1074\/jbc.M211609200","article-title":"The Orphan G Protein-coupled Receptors GPR41 and GPR43 Are Activated by Propionate and Other Short Chain Carboxylic Acids","volume":"278","author":"Brown","year":"2003","journal-title":"J. Biol. Chem."},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Guabiraba, R., and Schouler, C. (2015). Avian colibacillosis: Still many black holes. FEMS Microbiol. Lett., 362.","DOI":"10.1093\/femsle\/fnv118"},{"key":"ref_19","unstructured":"Kabir, S.M.L., Sikder, D.M., Alam, J., Neogi, S., and Yamasaki, S. (2017). Colibacillosis and Its Impact on Egg Production, Academic Press."},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Kathayat, D., Lokesh, D., Ranjit, S., and Rajashekara, G. (2021). Avian Pathogenic Escherichia coli (APEC): An Overview of Virulence and Pathogenesis Factors, Zoonotic Potential, and Control Strategies. Pathogens, 10.","DOI":"10.3390\/pathogens10040467"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"3987","DOI":"10.1128\/JCM.00816-08","article-title":"Identification of Minimal Predictors of Avian Pathogenic Escherichia coli Virulence for Use as a Rapid Diagnostic Tool","volume":"46","author":"Johnson","year":"2008","journal-title":"J. Clin. Microbiol."},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Nhung, N.T., Chansiripornchai, N., and Carrique-Mas, J.J. (2017). Antimicrobial Resistance in Bacterial Poultry Pathogens: A Review. Front. Vet. Sci., 4.","DOI":"10.3389\/fvets.2017.00126"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"2","DOI":"10.1186\/s13620-019-0154-4","article-title":"European perspectives on efforts to reduce antimicrobial usage in food animal production","volume":"73","author":"More","year":"2020","journal-title":"Ir. Vet. J."},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Balhuizen, M.D., Veldhuizen, E.J.A., and Haagsman, H.P. (2021). Outer Membrane Vesicle Induction and Isolation for Vaccine Development. Front. Microbiol., 12.","DOI":"10.3389\/fmicb.2021.629090"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1016\/j.vetmic.2014.04.019","article-title":"Advances in vaccination against avian pathogenic Escherichia coli respiratory disease: Potentials and limitations","volume":"172","author":"Ghunaim","year":"2014","journal-title":"Vet. Microbiol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"275","DOI":"10.1016\/j.vetimm.2007.03.002","article-title":"In vivo priming heterophil innate immune functions and increasing resistance to Salmonella enteritidis infection in neonatal chickens by immune stimulatory CpG oligodeoxynucleotides","volume":"117","author":"He","year":"2007","journal-title":"Vet. Immunol. Immunopathol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"732","DOI":"10.1017\/S002217240001158X","article-title":"The estimation of the bactericidal power of the blood","volume":"38","author":"Miles","year":"1938","journal-title":"Epidemiol. Infect."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"375","DOI":"10.1016\/0092-8674(79)90057-6","article-title":"Chicken hematopoietic cells transformed by seven strains of defective avian leukemia viruses display three distinct phenotypes of differentiation","volume":"18","author":"Beug","year":"1979","journal-title":"Cell"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"432","DOI":"10.1016\/j.immuni.2018.12.018","article-title":"The Short Chain Fatty Acid Butyrate Imprints an Antimicrobial Program in Macrophages","volume":"50","author":"Schulthess","year":"2019","journal-title":"Immunity"},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"L\u00e1zaro-D\u00edez, M., Chapartegui-Gonz\u00e1lez, I., Redondo-Salvo, S., Leigh, C., Merino, D., Segundo, D.S., Fern\u00e1ndez, A., Navas, J., Icardo, J.M., and Acosta, F. (2017). Human neutrophils phagocytose and kill Acinetobacter baumannii and A. pittii. Sci. Rep., 7.","DOI":"10.1038\/s41598-017-04870-8"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"496","DOI":"10.4161\/auto.23465","article-title":"Visualizing the autophagy pathway in avian cells and its application to studying infectious bronchitis virus","volume":"9","author":"Maier","year":"2013","journal-title":"Autophagy"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"402","DOI":"10.1006\/meth.2001.1262","article-title":"Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2\u2212\u0394\u0394CT Method","volume":"25","author":"Livak","year":"2001","journal-title":"Methods"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"114","DOI":"10.3382\/ps.2013-03287","article-title":"Activation of mammalian target of rapamycin signaling in skeletal muscle of neonatal chicks: Effects of dietary leucine and age","volume":"93","author":"Deng","year":"2014","journal-title":"Poult. Sci."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"14","DOI":"10.1186\/s13567-021-00896-z","article-title":"Analysis of chicken macrophage functions and gene expressions following infectious bronchitis virus M41 infection","volume":"52","author":"Sun","year":"2021","journal-title":"Vet. Res."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1186\/s13567-023-01174-w","article-title":"NDV-induced autophagy enhances inflammation through NLRP3\/Caspase-1 inflammasomes and the p38\/MAPK pathway","volume":"54","author":"Cai","year":"2023","journal-title":"Vet. Res."},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"McKight, P.E., and Najab, J. (2010). Kruskal-Wallis Test. The Corsini Encyclopedia of Psychology, Wiley.","DOI":"10.1002\/9780470479216.corpsy0491"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"292","DOI":"10.1177\/1536867X1501500117","article-title":"Nonparametric Pairwise Multiple Comparisons in Independent Groups using Dunn\u2019s Test","volume":"15","author":"Dinno","year":"2015","journal-title":"Stata J. Promot. Commun. Stat. Stata"},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Redza-Dutordoir, M., and Averill-Bates, D.A. (2021). Interactions between reactive oxygen species and autophagy: Special issue: Death mechanisms in cellular homeostasis. Biochim. Biophys. Acta (BBA) Mol. Cell Res., 1868.","DOI":"10.1016\/j.bbamcr.2021.119041"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"151","DOI":"10.1016\/j.aninu.2017.08.010","article-title":"Implications of butyrate and its derivatives for gut health and animal production","volume":"4","author":"Bedford","year":"2018","journal-title":"Anim. Nutr."},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Adams, J.R.G., Mehat, J., La Ragione, R., and Behboudi, S. (2023). Preventing bacterial disease in poultry in the post-antibiotic era: A case for innate immunity modulation as an alternative to antibiotic use. Front. Immunol., 14.","DOI":"10.3389\/fimmu.2023.1205869"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"e15","DOI":"10.4110\/in.2020.20.e15","article-title":"The Role of Butyrate in Attenuating Pathobiont-Induced Hyperinflammation","volume":"20","author":"Chen","year":"2020","journal-title":"Immune Netw."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1016\/j.clnu.2022.10.024","article-title":"Butyrate\u2019s role in human health and the current progress towards its clinical application to treat gastrointestinal disease","volume":"42","author":"Hodgkinson","year":"2023","journal-title":"Clin. Nutr."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"685","DOI":"10.1016\/j.immuni.2014.10.015","article-title":"The Macrophage Paradox","volume":"41","author":"Price","year":"2014","journal-title":"Immunity"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"612","DOI":"10.1016\/j.molcel.2012.08.033","article-title":"The warburg effect dictates the mechanism of butyrate-mediated histone acetylation and cell proliferation","volume":"48","author":"Donohoe","year":"2012","journal-title":"Mol. Cell"},{"key":"ref_45","doi-asserted-by":"crossref","unstructured":"Chen, W., Ma, Q., Li, Y., Wei, L., Zhang, Z., Khan, A., Khan, M.Z., and Wang, C. (2025). Butyrate Supplementation Improves Intestinal Health and Growth Performance in Livestock: A Review. Biomolecules, 15.","DOI":"10.3390\/biom15010085"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"92","DOI":"10.1038\/s41577-024-01080-y","article-title":"Inducible antibacterial responses in macrophages","volume":"25","author":"Sweet","year":"2025","journal-title":"Nat. Rev. Immunol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"1469","DOI":"10.1016\/j.cellsig.2010.05.015","article-title":"Multi-mechanisms are involved in reactive oxygen species regulation of mTORC1 signaling","volume":"22","author":"Li","year":"2010","journal-title":"Cell. Signal."},{"key":"ref_48","doi-asserted-by":"crossref","unstructured":"Redweik, G.A.J., Kogut, M.H., Arsenault, R.J., Lyte, M., and Mellata, M. (2021). Reserpine improves Enterobacteriaceae resistance in chicken intestine via neuro-immunometabolic signaling and MEK1\/2 activation. Commun. Biol., 4.","DOI":"10.1038\/s42003-021-02888-3"},{"key":"ref_49","doi-asserted-by":"crossref","unstructured":"Peng, Y., Wang, Y., Zhou, C., Mei, W., and Zeng, C. (2022). PI3K\/Akt\/mTOR Pathway and Its Role in Cancer Therapeutics: Are We Making Headway?. Front. Oncol., 12.","DOI":"10.3389\/fonc.2022.819128"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1083\/jcb.200906094","article-title":"Keratins regulate protein biosynthesis through localization of GLUT1 and -3 upstream of AMP kinase and Raptor","volume":"187","author":"Vijayaraj","year":"2009","journal-title":"J. Cell Biol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"120805","DOI":"10.1016\/j.lfs.2022.120805","article-title":"Role of AMPK\/mTOR, mitochondria, and ROS in the pathogenesis of endometriosis","volume":"306","author":"Assaf","year":"2022","journal-title":"Life Sci."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"22","DOI":"10.3390\/oxygen1010004","article-title":"Comprehension of the Relationship between Autophagy and Reactive Oxygen Species for Superior Cancer Therapy with Histone Deacetylase Inhibitors","volume":"1","author":"Ikeda","year":"2021","journal-title":"Oxygen"},{"key":"ref_53","doi-asserted-by":"crossref","unstructured":"Bah, A., and Vergne, I. (2017). Macrophage Autophagy and Bacterial Infections. Front. Immunol., 8.","DOI":"10.3389\/fimmu.2017.01483"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"329","DOI":"10.1016\/j.immuni.2010.02.009","article-title":"Delivery of cytosolic components by autophagic adaptor protein p62 endows autophagosomes with unique antimicrobial properties","volume":"32","author":"Ponpuak","year":"2010","journal-title":"Immunity"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"6031","DOI":"10.1073\/pnas.0700036104","article-title":"Lysosomal killing of Mycobacterium mediated by ubiquitin-derived peptides is enhanced by autophagy","volume":"104","author":"Alonso","year":"2007","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"24","DOI":"10.1016\/j.vetimm.2014.09.002","article-title":"Effect of butyrate on immune response of a chicken macrophage cell line","volume":"162","author":"Zhou","year":"2014","journal-title":"Vet. Immunol. Immunopathol."},{"key":"ref_57","doi-asserted-by":"crossref","unstructured":"Yang, Q., Burkardt, A.C., Sunkara, L.T., Xiao, K., and Zhang, G. (2022). Natural Cyclooxygenase-2 Inhibitors Synergize With Butyrate to Augment Chicken Host Defense Peptide Gene Expression. Front. Immunol., 13.","DOI":"10.3389\/fimmu.2022.819222"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"2422","DOI":"10.1073\/pnas.0304455101","article-title":"Interplay between antibacterial effectors: A macrophage antimicrobial peptide impairs intracellular Salmonella replication","volume":"101","author":"Rosenberger","year":"2004","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"1082","DOI":"10.1136\/gutjnl-2014-307436","article-title":"Intestinal epithelial vitamin D receptor deletion leads to defective autophagy in colitis","volume":"64","author":"Wu","year":"2015","journal-title":"Gut"},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"18","DOI":"10.4161\/derm.3.1.14616","article-title":"Impact of vitamin D3 on cutaneous immunity and antimicrobial peptide expression","volume":"3","author":"Antal","year":"2011","journal-title":"Derm. Endocrinol."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"629","DOI":"10.1111\/j.0022-202X.2005.23856.x","article-title":"Old Meets New: The Interaction Between Innate and Adaptive Immunity","volume":"125","author":"Clark","year":"2005","journal-title":"J. Investig. Dermatol."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"461","DOI":"10.1038\/s41575-019-0157-3","article-title":"The role of short-chain fatty acids in microbiota\u2013gut\u2013brain communication","volume":"16","author":"Dalile","year":"2019","journal-title":"Nat. Rev. Gastroenterol. Hepatol."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"120","DOI":"10.1080\/21623945.2020.1738791","article-title":"Low and high concentrations of butyrate regulate fat accumulation in chicken adipocytes via different mechanisms","volume":"9","author":"Zhao","year":"2020","journal-title":"Adipocyte"},{"key":"ref_64","doi-asserted-by":"crossref","unstructured":"Meyers, G.R., Samouda, H., and Bohn, T. (2022). Short Chain Fatty Acid Metabolism in Relation to Gut Microbiota and Genetic Variability. Nutrients, 14.","DOI":"10.3390\/nu14245361"},{"key":"ref_65","doi-asserted-by":"crossref","unstructured":"Garceau, V., Balic, A., Garcia-Morales, C., Sauter, K.A., McGrew, M.J., Smith, J., Vervelde, L., Sherman, A., Fuller, T.E., and Oliphant, T. (2015). The development and maintenance of the mononuclear phagocyte system of the chick is controlled by signals from the macrophage colony-stimulating factor receptor. BMC Biol., 13.","DOI":"10.1186\/s12915-015-0121-9"},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"1116","DOI":"10.1016\/j.immuni.2018.10.013","article-title":"The Microbial Metabolite Butyrate Stimulates Bone Formation via T Regulatory Cell-Mediated Regulation of WNT10B Expression","volume":"49","author":"Tyagi","year":"2018","journal-title":"Immunity"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1038\/s41467-017-02490-4","article-title":"Short-chain fatty acids regulate systemic bone mass and protect from pathological bone loss","volume":"9","author":"Lucas","year":"2018","journal-title":"Nat. Commun."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"8817421","DOI":"10.1155\/2021\/8817421","article-title":"Butyrate Inhibits Osteoclast Activity In Vitro and Regulates Systemic Inflammation and Bone Healing in a Murine Osteotomy Model Compared to Antibiotic-Treated Mice","volume":"2021","author":"Wallimann","year":"2021","journal-title":"Mediat. Inflamm."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"24","DOI":"10.1016\/j.cbi.2014.07.004","article-title":"Spiruchostatin A and B, novel histone deacetylase inhibitors, induce apoptosis through reactive oxygen species-mitochondria pathway in human lymphoma U937 cells","volume":"221","author":"Rehman","year":"2014","journal-title":"Chem. Biol. Interact."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"1521","DOI":"10.1128\/AAC.01876-15","article-title":"Histone Deacetylase Inhibitors Promote Mitochondrial Reactive Oxygen Species Production and Bacterial Clearance by Human Macrophages","volume":"60","author":"Ariffin","year":"2015","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"16191","DOI":"10.1074\/jbc.M908066199","article-title":"N-terminal Region, C-terminal Region, Nuclear Export Signal, and Deacetylation Activity of Histone Deacetylase-3 Are Essential for the Viability of the DT40 Chicken B Cell Line","volume":"275","author":"Takami","year":"2000","journal-title":"J. Biol. 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