Prevention of enteric bacterial infections and modulation of gut microbiota with conjugated linoleic acids producing Lactobacillus in mice

References

• Tlaskalová-Hogenová H, Tpánková R, Kozáková H, Hudcovic T, Vannucci L, Tuková L, Rossmann P, Hrní T, Kverka M, Zákostelská Z, et al. The role of gut microbiota (commensal bacteria) and the mucosal barrier in the pathogenesis of inflammatory and autoimmune diseases and cancer: contribution of germ-free and gnotobiotic animal models of human diseases. Cell Mol Immunol. 2011;8:110–120. doi:10.1038/cmi.2010.67.
   Google Scholar
• Liu L, Chen X, Skogerbø G, Zhang P, Chen R, He S, Huang DW. The human microbiome: A hot spot of microbial horizontal gene transfer. Genomics. 2012;100:165–270. doi:10.1016/j.ygeno.2012.07.012.
   Google Scholar
• Fujimura KE, Slusher NAN, Cabana MD. Role of the gut microbiota in defining human health. Expert Rev Anti. 2010;8:435–454. Internet. http://www.expert-reviews.com/doi/abs/10.1586/eri.10.14.
   Google Scholar
• Simon JC, Marchesi JR, Mougel C, Selosse MA. Host-microbiota interactions: from holobiont theory to analysis. Microbiome. 2019;7:1–5. doi:10.1186/s40168-019-0619-4.
   Google Scholar
• Hillman ET, Lu H, Yao T, Nakatsu CH. Microbial Ecology along the Gastrointestinal Tract. Microbes Environ. 2017;32:300–313. doi:10.1264/jsme2.ME17017.
   Google Scholar
• Guarner F, Malagelada JR. Gut flora in health and disease. Lancet. 2003;361:512–519. doi:10.1016/S0140-6736(03)12489-0.
   Google Scholar
• Vedantam G, Hecht DW. Antibiotics and anaerobes of gut origin. Curr Opin Microbiol. 2003;6:457–461.
   Google Scholar
• Shreiner AB, Kao JY, Young VB. The gut microbiome in health and in disease. Curr Opin Gastroenterol. 2015;31:69–75. doi:10.1097/MOG.0000000000000139.
   Google Scholar
• Wexler HM. Bacteroides: the good, the bad, and the nitty-gritty. Clin Microbiol Rev. 2007;20:593–621. doi:10.1128/CMR.00008-07.
   Google Scholar
• Segal LN, Blaser MJ. A brave new world: the lung microbiota in an era of change. Ann Am Thorac Soc Vol 11, Supplement 1, pp S21–S27.
   Google Scholar
• Beaugerie L, Petit JC. Antibiotic-associated diarrhoea. Best Pract Res Clin Gastroenterol. 2004;18:337–352. doi:10.1016/j.bpg.2003.10.002.
   Google Scholar
• Peng M, Salaheen S, Buchanan RL, Biswas D. Alterations of Salmonella enterica Serovar Typhimurium Antibiotic Resistance under Environmental Pressure. Appl Environ Microbiol. 2018;84:e01173–18. Internet [accessed 2018 Sept 20]. http://www.ncbi.nlm.nih.gov/pubmed/30054356.
   Google Scholar
• Peng M, Salaheen S, Biswas D. Animal health: antibiotic global issues. In: Alfen NKV editor. Encyclopedia of Agriculture and Food Systems, Elsevier Inc. Press. 2014;346–357.
   Google Scholar
• Peng M, Salaheen S, Almario JA, Tesfaye B, Buchanan R, Biswas D. Prevalence and antibiotic resistance pattern of Salmonella serovars in integrated crop-livestock farms and their products sold in local markets. Environ Microbiol. 2016;18:1654–1665. doi:10.1111/1462-2920.13265.
   Google Scholar
• Coburn B, Sekirov I, Finlay BB. Type III secretion systems and disease. Clin Microbiol Rev. 2007;20:535–549. doi:10.1128/CMR.00013-07.
   Google Scholar
• Peng M, Biswas D. Short Chain and Polyunsaturated Fatty Acids in Host Gut Health and Foodborne Bacterial Pathogen Inhibition. Crit Rev Food Sci Nutr. 2017;57:3987–4002. Internet http://www.tandfonline.com/doi/full/10.1080/10408398.2016.1203286.
   Google Scholar
• Panos GZ, Betsi GI, Falagas ME. Systematic review: are antibiotics detrimental or beneficial for the treatment of patients with Escherichia coli O157: h7infection? Aliment Pharmacol Ther. 2006;24:731–742. doi:10.1111/apt.2006.24.issue-5.
   Google Scholar
• Goldwater PN, Bettelheim KA. Treatment of enterohemorrhagic Escherichia coli (EHEC) infection and hemolytic uremic syndrome (HUS). BMC Med. 2012;10:1–8. doi:10.1186/1741-7015-10-12.
   Google Scholar
• Salaheen S, Peng M, Biswas D. Replacement of conventional antimicrobials and preservatives in food production to improve consumer safety and enhance health benefits. In: Rai VR and Bai JA editors. Microbial Food Safety and Preservation Techniques. CRC press. 2014;305–328.
   Google Scholar
• Peng M, Patel P, Nagarajan V, Bernhardt C, Carrion M, Biswas D. Feasible options to control colonization of enteric pathogens with designed synbiotics. In: Watson R and Preedy V. Dietary Interventions in Gastrointestinal Diseases. Elsevier Inc. Press. 2019;135–149.
   Google Scholar
• Peng M, Aryal U, Cooper B, Biswas D. Metabolites produced during the growth of probiotics in cocoa supplementation and the limited role of cocoa in host-enteric bacterial pathogen interactions. Food Control. 2015;53:124–133. Internet. doi:10.1016/j.foodcont.2015.01.014.
   Google Scholar
• Peng M, Tabashsum Z, Patel P, Bernhardt C, Biswas D. Linoleic Acids Overproducing Lactobacillus casei Limits Growth, Survival, and Virulence of Salmonella Typhimurium and Enterohaemorrhagic Escherichia coli. Front Microbiol. 2018;9:2663. Internet [accessed 2018 Dec 17]. https://www.frontiersin.org/article/10.3389/fmicb.2018.02663/full.
   Google Scholar
• O’Shea EF, Cotter PD, Stanton C, Ross RP, Hill C. Production of bioactive substances by intestinal bacteria as a basis for explaining probiotic mechanisms: bacteriocins and conjugated linoleic acid. Int J Food Microbiol. 2012;152:189–205. doi:10.1016/j.ijfoodmicro.2011.05.025.
   Google Scholar
• Yang B, Chen H, Stanton C, Ross RP, Zhang H, Chen YQ, Chen W. Review of the roles of conjugated linoleic acid in health and disease. J Funct Foods. 2015;15:314–325. doi:10.1016/j.jff.2015.03.050.
   Google Scholar
• Byeon JI, Song HS, Oh TW, Kim YS, Choi BD, Kim HC, Kim JO, Shim KH, Ha YL. Growth inhibition of foodborne and pathogenic bacteria by conjugated linoleic acid. J Agric Food Chem. 2009;57:3164–3172. Internet. http://www.scopus.com/inward/record.url?eid=2-s2.0-65349162210&partnerID=40&md5=9610d56bb99211a5bae2b01378ad8ecd.
   Google Scholar
• Garner CD, Antonopoulos DA, Wagner B, Duhamel GE, Keresztes I, Ross DA, Young VB, Altier C. Perturbation of the small intestine microbial ecology by streptomycin alters pathology in a Salmonella enterica serovar typhimurium murine model of infection. Infect Immun. 2009;77:2691–2702. doi:10.1128/IAI.01570-08.
   Google Scholar
• Snel J, Born L, van der Meer R. Dietary fish oil impairs induction of gamma-interferon and delayed-type hypersensitivity during a systemic Salmonella enteritidis infection in rats. APMIS. 2010;118:578–584. doi:10.1111/j.1600-0463.2010.02655.x.
   Google Scholar
• Lee SM, Donaldson GP, Mikulski Z, Boyajian S, Ley K, Mazmanian SK. Bacterial colonization factors control specificity and stability of the gut microbiota. Nature. 2013;501:426–429. doi:10.1038/nature12447.
   Google Scholar
• Willamil J, Creus E, Francisco Pérez J, Mateu E, Martín-Orúe SM. Effect of a microencapsulated feed additive of lactic and formic acid on the prevalence of Salmonella in pigs arriving at the abattoir. Arch Anim Nutr. 2011;65:431–444. doi:10.1080/1745039X.2011.623047.
   Google Scholar
• Sunkara LT, Achanta M, Schreiber NB, Bommineni YR, Dai G, Jiang W, Lamont S, Lillehoj HS, Beker A, Teeter RG, et al. Butyrate enhances disease resistance of chickens by inducing antimicrobial host defense peptide gene expression. PLoS One. 2011;6:e27225. doi:10.1371/journal.pone.0027225.
   Google Scholar
• Sunkara LT, Jiang W, Zhang G. Modulation of Antimicrobial Host Defense Peptide Gene Expression by Free Fatty Acids. PLoS One. 2012;7:e49558. doi:10.1371/journal.pone.0049558.
   Google Scholar
• Hung CC, Garner CD, Slauch JM, Dwyer ZW, Lawhon SD, Frye JG, Mcclelland M, Ahmer BMM, Altier C. The intestinal fatty acid propionate inhibits Salmonella invasion through the post-translational control of HilD. Mol Microbiol. 2013;87:1045–1060. doi:10.1111/mmi.12149.
   Google Scholar
• Sun Y, O’Riordan MXD. Regulation of bacterial pathogenesis by intestinal short-chain fatty acids. Adv Appl Microbiol. 2013;85:92–118.
   Google Scholar
• McKenney PT, Pamer EG. From Hype to Hope: the Gut Microbiota in Enteric Infectious Disease. Cell. 2015;163:1326–1332. doi:10.1016/j.cell.2015.11.032.
   Google Scholar
• Buffie CG, Pamer EG. Microbiota-mediated colonization resistance against intestinal pathogens. Nat Rev Immunol. 2013;13:790–801. doi:10.1038/nri3535.
   Google Scholar
• Amalaradjou MAR, Bhunia AK. Modern Approaches in Probiotics Research to Control Foodborne Pathogens. Adv Food Nutr Res. 2012;67:185–239.
   Google Scholar
• Peng M, Reichmann G, Biswas D. Lactobacillus casei and its byproducts alter the virulence factors of foodborne bacterial pathogens. J Funct Foods. 2015;15:418–428. Internet. doi:10.1016/j.jff.2015.03.055.
   Google Scholar
• Peng M, Bitsko E, Biswas D. Functional properties of peanut fractions on the growth of probiotics and foodborne bacterial pathogens. J Food Sci. 2015;80:M635–41. doi:10.1111/1750-3841.12785.
   Google Scholar
• Meraz-Torres LS, Hernandez-Sanchez H. Conjugated Linoleic Acid in Dairy Products: A Review. Am J Food Technol. 2012;7:176–179. doi:10.3923/ajft.2012.176.179.
   Google Scholar
• Tabashsum Z, Peng M, Salaheen S, Comis C, Biswas D. Competitive elimination and virulence property alteration of Campylobacter jejuni by genetically engineered Lactobacillus casei. Food Control. 2018;85:283–291. doi:10.1016/j.foodcont.2017.10.010.
   Google Scholar
• Tabashsum Z, Peng M, Kahan E, Rahaman SO, Biswas D. Effect of Conjugated Linoleic Acid Overproducing Lactobacillus with Berry Pomace Phenolic Extracts on Campylobacter jejuni Pathogenesis. Food Funct. 2018;10:296–303. Internet [accessed 2018 Dec 17]. http://pubs.rsc.org/en/Content/ArticleLanding/2018/FO/C8FO01863D.
   Google Scholar
• Oracz G, Feleszko W, Golicka D, Maksymiuk J, Klonowska A, Szajewska H. Rapid Diagnosis of Acute Salmonella Gastrointestinal Infection. Clin Infect Dis. 2003;36:112–115. doi:10.1086/cid.2003.36.issue-1.
   Google Scholar
• Barba-Vidal E, Buttow Roll VF, Garcia Manzanilla E, Torrente C, Moreno Muñoz JA, Pérez JF, Martín-Orúe SM. Blood parameters as biomarkers in a Salmonella spp. disease model of weaning piglets. PLoS One. 2017;12:e0186781. doi:10.1371/journal.pone.0186781.
   Google Scholar
• Santos RL, Tsolis RM, Bäumler AJ, Adams LG. Hematologic and serum biochemical changes in Salmonella ser Typhimurium-infected calves. Am J Vet Res. 2002. doi:10.2460/ajvr.2002.63.1145.
   Google Scholar
• Ohland CL, MacNaughton WK. Probiotic bacteria and intestinal epithelial barrier function. AJP Gastrointest Liver Physiol. 2010;298:G807–19. doi:10.1152/ajpgi.00243.2009.
   Google Scholar
• Rugge M, Pennelli G, Pilozzi E, Fassan M, Ingravallo G, Russo VM, Di Mario F. Gastritis: the histology report. Dig Liver Dis. 2011;43:S373–84. doi:10.1016/S1590-8658(11)60593-8.
   Google Scholar
• Thursby E, Juge N. Introduction to the human gut microbiota. Biochem J. 2017;474:1823–1836. doi:10.1042/BCJ20160510.
   Google Scholar
• Viladomiu M, Hontecillas R, Yuan L, Lu P, Bassaganya-Riera J. Nutritional protective mechanisms against gut inflammation. J Nutr Biochem. 2013;24:929–939. doi:10.1016/j.jnutbio.2013.01.006.
   Google Scholar
• Bassaganya-Riera J, Viladomiu M, Pedragosa M, de Simone C, Carbo A, Shaykhutdinov R, Jobin C, Arthur JC, Corl BA, Vogel H, et al. Probiotic bacteria produce conjugated linoleic acid locally in the gut that targets macrophage PPAR γ to suppress colitis. PLoS One. 2012;7:e31238. doi:10.1371/journal.pone.0031238.
   Google Scholar
• Ubeda C, Djukovic A, Isaac S. Roles of the intestinal microbiota in pathogen protection. Clin Transl Immunol. 2017;6:e128. doi:10.1038/cti.2017.2.
   Google Scholar
• Iacob S, Iacob DG, Luminos LM. Intestinal Microbiota as a Host Defense Mechanism to Infectious Threats. Front Microbiol. 2019;9:1–9. Internet [accessed 2019 Feb 26]. https://www.frontiersin.org/article/10.3389/fmicb.2018.03328/full.
   Google Scholar
• Barman M, Unold D, Shifley K, Amir E, Hung K, Bos N, Salzman N. Enteric salmonellosis disrupts the microbial ecology of the murine gastrointestinal tract. Infect Immun. 2008;76:907–915. doi:10.1128/IAI.01432-07.
   Google Scholar
• Videnska P, Sisak F, Havlickova H, Faldynova M, Rychlik I. Influence of Salmonella enterica serovar Enteritidis infection on the composition of chicken cecal microbiota. BMC Vet Res. 2013;9:1–8. doi:10.1186/1746-6148-9-18.
   Google Scholar
• Argüello H, Estellé J, Zaldívar-López S, Jiménez-Marín Á, Carvajal A, López-Bascón MA, Crispie F, O’Sullivan O, Cotter PD, Priego-Capote F, et al. Early Salmonella Typhimurium infection in pigs disrupts Microbiome composition and functionality principally at the ileum mucosa. Sci Rep. 2018;8:1–12. doi:10.1038/s41598-018-26083-3.
   Google Scholar
• Kho ZY, Lal SK. The human gut microbiome - A potential controller of wellness and disease. Front Microbiol. 2018;9:1–23. doi:10.3389/fmicb.2018.01835.
   Google Scholar
• Marques TM, Wall R, O’Sullivan O, Fitzgerald GF, Shanahan F, Quigley EM, Cotter PD, Cryan JF, Dinan TG, Ross RP, et al. Dietary trans-10, cis-12-conjugated linoleic acid alters fatty acid metabolism and microbiota composition in mice. Br J Nutr. 2015;113:1–11. doi:10.1017/S0007114514004206.
   Google Scholar
• O’Neill I, Schofield Z, Hall LJ. Exploring the role of the microbiota member Bifidobacterium in modulating immune-linked diseases. Emerg Top Life Sci. 2017;1:333–349. doi:10.1042/ETLS20170058.
   Google Scholar
• Jandhyala SM, Talukdar R, Subramanyam C, Vuyyuru H, Sasikala M, Reddy DN. Role of the normal gut microbiota. World J Gastroenterol. 2015;21:8787–8803. doi:10.3748/wjg.v21.i10.2937.
   Google Scholar
• Mohawk KL, O’Brien AD. Mouse Models of Escherichia coli O157: h7Infection and Shiga Toxin Injection. J Biomed Biotechnol. 2011;2011:1–17. Internet http://www.hindawi.com/journals/bmri/2011/258185/.
   Google Scholar
• Isogai E, Isogai H, Takeshi K, Nishikawa T. Protective effect of Japanese green tea extract on gnotobiotic mice infected with an Escherichia coli O157: h7strain. Microbiol Immunol. 1998;42:125–128. doi:10.1111/j.1348-0421.1998.tb02260.x.
   Google Scholar
• Eaton KA, Friedman DI, Francis GJ, Tyler JS, Young VB, Haeger J, Abu-Ali G, Whittam TS. Pathogenesis of renal disease due to enterohemorrhagic Escherichia coli in germ-free mice. Infect Immun. 2008;76:3054–3063. doi:10.1128/IAI.01626-07.
   Google Scholar
• Karpman D, Council H, Svensson M, Scheutz F, Aim P, Svanborg C. The role of lipopolysaccharide and Shiga-like toxin in a mouse model of Escherichia coli O157: h7infection. J Infect Dis. 1997;175:611–620. doi:10.1086/516490.
   Google Scholar
• Brando RJF, Miliwebsky E, Bentancor L, Deza N, Baschkier A, Ramos MV, Fernández GC, Meiss R, Rivas M, Palermo MS. Renal damage and death in weaned mice after oral infection with Shiga toxin 2-producing Escherichia coli strains. Clin Exp Immunol. 2008;153:297–306. doi:10.1111/j.1365-2249.2008.03698.x.
   Google Scholar
• Conlan JW, Perry MB. Susceptibility of Three Strains of Conventional Adult Mice to Intestinal Colonization by an Isolate of _Escherichia coli_ O157:H7. Can J Microbiol. 1998;44:800–805.
   Google Scholar
• Nagano K, Taguchi K, Hara T, Yokoyama SI, Kawada K, Mori H. Adhesion and colonization of enterohemorrhagic Escherichia coli O157: h7in cecum of mice. Microbiol Immunol. 2003;47:125–132.
   Google Scholar
• Salaheen S, Jaiswal E, Joo J, Peng M, Ho R, OConnor D, Adlerz K, Aranda-Espinoza JH, Biswas D. Bioactive extracts from berry byproducts on the pathogenicity of Salmonella Typhimurium. Int J Food Microbiol. 2016;237:128–135. Internet. doi:10.1016/j.ijfoodmicro.2016.08.027.
   Google Scholar
• Peng M, Zhao X, Biswas D. Polyphenols and tri-terpenoids from Olea europaea L. in alleviation of enteric pathogen infections through limiting bacterial virulence and attenuating inflammation. J Funct Foods. 2017;36:132–143. Internet. doi:10.1016/j.jff.2017.06.059.
   Google Scholar
• Dann SM, Le C, Choudhury BK, Liu H, Saldarriaga O, Hanson EM, Cong Y, Eckmann L. Attenuation of Intestinal Inflammation in Interleukin-10-Deficient Mice Infected with Citrobacter rodentium. Infect Immun. 2014;81:1949–1958. doi:10.1128/IAI.00066-14.
   Google Scholar
• Li H-L, Lu L, Wang X-S, Qin L-Y, Wang P, Qiu S-P, Wu H, Huang F, Zhang -B-B, Shi H-L, et al. Alteration of Gut Microbiota and Inflammatory Cytokine/Chemokine Profiles in 5-Fluorouracil Induced Intestinal Mucositis. Front Cell Infect Microbiol. 2017;7:1–14. doi:10.3389/fcimb.2017.00517.
   Google Scholar
• Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2-delta-delta-CT Method. Methods. 2001;25:402–408. doi:10.1006/meth.2001.1262.
   Google Scholar