[en] Colibacillosis is one of the major health threats in the poultry industry worldwide. Understanding the pathogenic mechanisms involved in Escherichia coli-induced inflammatory response may lead to the development of new therapies to combat the disease. To address this, a total of 96 1-day-old male lean Pekin ducklings were employed and randomly allocated to two treatments, each with six replicates of eight ducks. Ducks in the experiment group (EG) and the control group (CG) were separately orally administered with 0.2 ml of pathogenic E. coli O88 (3 × 109 CFU/ml) or equivalent volumes of 0.9% sterile saline solution on day 7, two times with an 8-h interval. Serum and intestinal samples were collected on days 9, 14, and 28. Results showed that ducks challenged with E. coli had lower average daily gain and higher feed intake/weight gain during days 9-14 and overall (P < 0.05). Histopathological examination showed that E. coli decreased the villus height and the ratio of villus height/crypt depth in the jejunum (P < 0.05) on days 9 and 14. The intestinal barrier was disrupted, presenting in E. coli ducks having higher serum DAO and D-LA on days 9 and 14 (P < 0.05) and greater content of serum LPS on day 9 (P < 0.05). Escherichia coli infection also triggered a systemic inflammatory response including the decrease of the serum IgA, IgM, and jejunal sIgA on day 14 (P < 0.05). In addition to these, 1,062 differentially expressed genes were detected in the jejunum tissues of ducks by RNA-seq, consisting of 491 upregulated and 571 downregulated genes. Based on the KEGG database, oxidative phosphorylation and the ribosome pathway were the most enriched. These findings reveal the candidate pathways and genes that may be involved in E. coli infection, allow a better understanding of the molecular mechanisms of inflammation progression and may facilitate the genetic improvement of ducks, and provide further insights to tackle the drug sensitivity and animal welfare issues.
Disciplines :
Veterinary medicine & animal health
Author, co-author :
Li, Chong ; Université de Liège - ULiège > TERRA Research Centre ; Key Laboratory for Feed Biotechnology of the Ministry of Agriculture and Rural Affairs, Institute of Feed Research, Chinese Academy of Agriculture Sciences, Beijing, China
Li, Shuzhen; Key Laboratory for Feed Biotechnology of the Ministry of Agriculture and Rural Affairs, Institute of Feed Research, Chinese Academy of Agriculture Sciences, Beijing, China
Liu, Jinmei; Key Laboratory for Feed Biotechnology of the Ministry of Agriculture and Rural Affairs, Institute of Feed Research, Chinese Academy of Agriculture Sciences, Beijing, China
Cai, Huiyi; Key Laboratory for Feed Biotechnology of the Ministry of Agriculture and Rural Affairs, Institute of Feed Research, Chinese Academy of Agriculture Sciences, Beijing, China ; Research and Development Department, National Engineering Research Center of Biological Feed, Beijing, China
Liu, Guohua; Key Laboratory for Feed Biotechnology of the Ministry of Agriculture and Rural Affairs, Institute of Feed Research, Chinese Academy of Agriculture Sciences, Beijing, China
Deng, Xuejuan; Research and Development Department, National Engineering Research Center of Biological Feed, Beijing, China
Chang, Wenhuan; Key Laboratory for Feed Biotechnology of the Ministry of Agriculture and Rural Affairs, Institute of Feed Research, Chinese Academy of Agriculture Sciences, Beijing, China
Language :
English
Title :
Escherichia coli O88 induces intestinal damage and inflammatory response through the oxidative phosphorylation and ribosome pathway in Pekin ducks.
This research was funded by the Agricultural Science and Technology Innovation Program (ASTIP) and the Collaborative Innovation Task in Agricultural Science and Technology Innovation Program (CAAS-XTCX).
Alber A. Stevens M. P. Vervelde L. (2021). The bird’s immune response to avian pathogenic escherichia coli. Avian Pathol. 50, 382–391. doi: 10.1080/03079457.2021.1873246
Alhotan R. A. Al Sulaiman A. R. Alharthi A. S. Abudabos A. M. (2021). Protective influence of betaine on intestinal health by regulating inflammation and improving barrier function in broilers under heat stress. Poult. Sci. 100, 101337. doi: 10.1016/j.psj.2021.101337
Ashton T. M. Gillies McKenna W. Kunz-Schughart L. A. Higgins G. S. (2018). Oxidative phosphorylation as an emerging target in cancer therapy. Clin. Cancer Res. 24, 2482–2490. doi: 10.1158/1078-0432.CCR-17-3070
Berger C. N. Crepin V. F. Roumeliotis T. I. Wright J. C. Carson D. Pevsner-Fischer M. et al. (2017). Citrobacter rodentium subverts ATP flux and cholesterol homeostasis in intestinal epithelial cells In vivo. Cell Metab. 26, 738–752. doi: 10.1016/j.cmet.2017.09.003
Buck M. D. O’Sullivan D. Geltink R. I. K. Curtis J. D. Chang C. H. Sanin D. E. et al. (2017). Mitochondrial dynamics controls T cell fate through metabolic programming. Cell 166, 63–76. doi: 10.1016/j.cell.2016.05.035
Carrasco-Pozo C. Tan K. N. Avery V. M. (2020). Hemin prevents increased glycolysis in macrophages upon activation: Protection by microbiota-derived metabolites of polyphenols. Antioxidants 9, 1–21. doi: 10.3390/antiox9111109
Czarny P. Wigner P. Galecki P. Sliwinski T. (2018). The interplay between inflammation, oxidative stress, DNA damage, DNA repair and mitochondrial dysfunction in depression. Prog. Neuropsychopharmacol. Biol. Psychiatry 80, 309–321. doi: 10.1016/j.pnpbp.2017.06.036
Daneshmand A. Kermanshahi H. Sekhavati M. H. Javadmanesh A. Ahmadian M. (2019). Antimicrobial peptide, cLF36, affects performance and intestinal morphology, microflora, junctional proteins, and immune cells in broilers challenged with e. coli. Sci. Rep. 9, 1–9. doi: 10.1038/s41598-019-50511-7
Ducatelle R. Goossens E. De Meyer F. Eeckhaut V. Antonissen G. Haesebrouck F. et al. (2018). Biomarkers for monitoring intestinal health in poultry: Present status and future perspectives. Vet. Res. 49, 1–9. doi: 10.1186/s13567-018-0538-6
Dziva F. Stevens M. P. (2008). Colibacillosis in poultry: Unravelling the molecular basis of virulence of avian pathogenic escherichia coli in their natural hosts. Avian Pathol. 37, 355–366. doi: 10.1080/03079450802216652
Ekim B. Calik A. Ceylan A. Saçaklı P. (2020). Effects of paenibacillus xylanexedens on growth performance, intestinal histomorphology, intestinal microflora, and immune response in broiler chickens challenged with escherichia coli K88. Poult. Sci. 99, 214–223. doi: 10.3382/ps/pez460
Florea L. Song L. Salzberg S. L. (2013). Thousands of exon skipping events differentiate among splicing patterns in sixteen human tissues. F1000Research 2, 188. doi: 10.12688/f1000research.2-188.v2
Franciotti R. Pignatelli P. Carrarini C. Romei F. M. Mastrippolito M. Gentile A. et al. (2021). Exploring the connection between porphyromonas gingivalis and neurodegenerative diseases: A pilot quantitative study on the bacterium abundance in oral cavity and the amount of antibodies in serum. Biomolecules 11, 845. doi: 10.3390/biom11060845
Fujiwara H. Seike K. Brooks M. D. Mathew A. V. Kovalenko I. Pal A. et al. (2021). Mitochondrial complex II in intestinal epithelial cells regulates T cell-mediated immunopathology. Nat. Immunol. 22, 1440–1451. doi: 10.1038/s41590-021-01048-3
Guabiraba R. Schouler C. (2015). Avian colibacillosis: Still many black holes. FEMS Microbiol. Lett. 362, 1–8. doi: 10.1093/femsle/fnv118
Honzawa Y. Nakase H. Matsuura M. Chiba T. (2011). Clinical significance of serum diamine oxidase activity in inflammatory bowel disease: Importance of evaluation of small intestinal permeability. Inflamm. Bowel Dis. 17, 23–25. doi: 10.1002/ibd.21588
Inatomi T. Otomaru K. (2018). Effect of dietary probiotics on the semen traits and antioxidative activity of male broiler breeders. Sci. Rep. 8, 1–6. doi: 10.1038/s41598-018-24345-8
Ip W. K. E. Hoshi N. Shouval D. S. Snapper S. Medzhitov R. (2017). Anti-inflammatory effect of IL-10 mediated by metabolic reprogramming of macrophages. Science 356, 513–519. doi: 10.1126/science.aal3535
Kaper J. B. Nataro J. P. Mobley H. L. T. (2004). Pathogenic escherichia coli. Nat. Rev. Microbiol. 2, 123–140. doi: 10.1038/nrmicro818
Kilkenny C. Browne W. J. Cuthi I. Emerson M. Altman D. G. (2012). Improving bioscience research reporting: The ARRIVE guidelines for reporting animal research. Vet. Clin. Pathol. 41, 27–31. doi: 10.1111/j.1939-165X.2012.00418.x
Kim J. K. Lee K. E. Lee S. A. Jang H. M. Kim D. H. (2020). Interplay between human gut bacteria escherichia coli and lactobacillus mucosae in the occurrence of neuropsychiatric disorders in mice. Front. Immunol. 11. doi: 10.3389/fimmu.2020.00273
Kim H. J. Maiti P. Barrientos A. (2017). Mitochondrial ribosomes in cancer. Semin. Cancer Biol. 47, 67–81. doi: 10.1016/j.semcancer.2017.04.004
Leng Y. Yi M. Fan J. Bai Y. Ge Q. Yao G. (2016). Effects of acute intra-abdominal hypertension on multiple intestinal barrier functions in rats. Sci. Rep. 6, 1–9. doi: 10.1038/srep22814
Letsinger A. C. Menon R. Iyer A. R. Vellers H. L. Granados J. Z. Jayaraman A. et al. (2020). A high fat/high sugar diet alters the gastrointestinal metabolome in a sex dependentmanner. Metabolites 10, 1–10. doi: 10.3390/metabo10100421
Li Y. Jin L. Chen T. Pirozzi C. J. (2020). The effects of secretory IgA in the mucosal immune system. BioMed. Res. Int. 2020, 1-6. doi: 10.1155/2020/2032057
Lin Q. Zhao J. Xie K. Wang Y. Hu G. Jiang G. et al. (2017). Magnolol additive as a replacer of antibiotic enhances the growth performance of linwu ducks. Anim. Nutr. 3, 132–138. doi: 10.1016/j.aninu.2017.03.004
Liu J. Liu G. Chen Z. Zheng A. Cai H. Chang W. et al. (2020). Effects of glucose oxidase on growth performance, immune function, and intestinal barrier of ducks infected with escherichia coli O88. Poult. Sci. 99, 6549–6558. doi: 10.1016/j.psj.2020.09.038
Livak K. J. Schmittgen T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25, 402–408. doi: 10.1006/meth.2001.1262
Love M. I. Huber W. Anders S. (2014). Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 1–21. doi: 10.1186/s13059-014-0550-8
Luk G. D. Bayless T. M. Baylin S. B. (1980). Diamine oxidase (histaminase). a circulating marker for rat intestinal mucosal maturation and integrity. J. Clin. Invest. 66, 66–70. doi: 10.1172/JCI109836
Lutful Kabir S. M. (2010). Avian colibacillosis and salmonellosis: A closer look at epidemiology, pathogenesis, diagnosis, control and public health concerns. Int. J. Environ. Res. Public Health 7, 89–114. doi: 10.3390/ijerph7010089
Ministry of Agriculture of the People’s Republic of China (2012). Nutrient requirements of meat-type duck (NY/T 2122-2012). Beijing, China: Agriculture Standard Press.
Monternier P. A. Fongy A. Hervant F. Drai J. Collin-Chavagnac D. Rouanet J. L. et al. (2015). Skeletal muscle phenotype affects fasting-induced mitochondrial oxidative phosphorylation flexibility in cold-acclimated ducklings. J. Exp. Biol. 218, 2427–2434. doi: 10.1242/jeb.122671
National Research Council (1994). Nutrient requirements of poultry, 9th re-vised edition. Washington, DC, USA: National Academy Press.
O’Neill L. A. J. Pearce E. J. (2016). Immunometabolism governs dendritic cell and macrophage function. J. Exp. Med. 213, 15–23. doi: 10.1084/jem.20151570
Pédron T. Mulet C. Dauga C. Frangeul L. Chervaux C. Grompone G. et al. (2012). A crypt-specific core microbiota resides in the mouse colon. MBio. 3, 1–7. doi: 10.1128/mBio.00116-12
Peng L. Y. Yuan M. Wu Z. M. Song K. Zhang C. L. An Q. et al. (2019). Anti-bacterial activity of baicalin against APEC through inhibition of quorum sensing and inflammatory responses. Sci. Rep. 9, 1–11. doi: 10.1038/s41598-019-40684-6
Pi D. Liu Y. Shi H. Li S. Odle J. Lin X. et al. (2014). Dietary supplementation of aspartate enhances intestinal integrity and energy status in weanling piglets after lipopolysaccharide challenge. J. Nutr. Biochem. 25, 456–462. doi: 10.1016/j.jnutbio.2013.12.006
Qu L. Tan W. Yang J. Lai L. Liu S. Wu J. et al. (2020). Combination compositions composed of l-glutamine and Si-Jun-Zi-Tang might be a preferable choice for 5-Fluorouracil-Induced intestinal mucositis: An exploration in a mouse model. Front. Pharmacol. 11. doi: 10.3389/fphar.2020.00918
Rodríguez-Prados J.-C. Través P. G. Cuenca J. Rico D. Aragonés J. Martín-Sanz P. et al. (2010). Substrate fate in activated macrophages: A comparison between innate, classic, and alternative activation. J. Immunol. 185, 605–614. doi: 10.4049/jimmunol.0901698
Smith F. Clark J. E. Overman B. L. Tozel C. C. Huang J. H. Rivier J. E. F. et al. (2010). Early weaning stress impairs development of mucosal barrier function in the porcine intestine. Am. J. Physiol. - Gastrointest. Liver Physiol. 298, 352–363. doi: 10.1152/ajpgi.00081.2009
Stephens M. von der Weid P. Y. (2020). Lipopolysaccharides modulate intestinal epithelial permeability and inflammation in a species-specific manner. Gut Microbes 11, 421–432. doi: 10.1080/19490976.2019.1629235
Sun X. Q. Fu X. B. Zhang R. Lü Y. Deng Q. Jiang X. G. et al. (2001). Relationship between plasma d(-)-lactate and intestinal damage after severe injuries in rats. World J. Gastroenterol. 7, 555–558. doi: 10.3748/wjg.v7.i4.555
Sun L. Xu G. Dong Y. Li M. Yang L. Lu W. (2020). Quercetin protects against lipopolysaccharide-induced intestinal oxidative stress in broiler chickens through activation of Nrf2 pathway. Molecules 25, 1053. doi: 10.3390/molecules25051053
Tan K. Deng D. Ma X. Cui Y. Tian Z. (2020). Pediococcus acidilactici P25 protected caenorhabditis elegans against enterotoxigenic escherichia coli K88 infection and transcriptomic analysis of its potential mechanisms. BioMed. Res. Int. 2020, 7340312. doi: 10.1155/2020/7340312
Tomlinson J. E. Blikslager A. T. (2004). Interactions between lipopolysaccharide and the intestinal epithelium. J. Am. Vet. Med. Assoc. 224, 1446–1452. doi: 10.2460/javma.2004.224.1446
Vats D. Mukundan L. Odegaard J. I. Zhang L. Smith K. L. Morel C. R. et al. (2006). Oxidative metabolism and PGC-1β attenuate macrophage-mediated inflammation. Cell Metab. 4, 13–24. doi: 10.1016/j.cmet.2006.05.011
Watkins E. J. Butler P. J. Kenyon B. P. (2004). Posthatch growth of the digestive system in wild and domesticated ducks. Br. Poult. Sci. 45, 331–341. doi: 10.1080/00071660410001730824
Wu Z. Yang K. Zhang A. Chang W. Zheng A. Chen Z. et al. (2021). Effects of lactobacillus acidophilus on the growth performance, immune response, and intestinal barrier function of broiler chickens challenged with escherichia coli O157. Poult. Sci. 100, 101323. doi: 10.1016/j.psj.2021.101323
Xiong W. Wang R. Mao W. Wu Y. Wang D. Hu Y. et al. (2021). Icariin and its phosphorylated derivatives reduce duck hepatitis a virus serotype 1-induced oxidative stress and inflammatory damage in duck embryonic hepatocytes through mitochondrial regulation. Res. Vet. Sci. 139, 133–139. doi: 10.1016/j.rvsc.2021.07.014
Zhang J. Yang Y. Han H. Zhang L. Wang T. (2021). Bisdemethoxycurcumin protects small intestine from lipopolysaccharide-induced mitochondrial dysfunction via activating mitochondrial antioxidant systems and mitochondrial biogenesis in broiler chickens. Oxid. Med. Cell. Longev. 2021, 9927864. doi: 10.1155/2021/9927864