Multifaceted Defense against Listeria monocytogenes in the Gastro-Intestinal Lumen
Abstract
:1. Introduction
2. A Brief Overview of In Vivo Colonization by L. monocytogenes
3. Defense against Listeria monocytogenes in the Gastro-Intestinal Lumen
3.1. Host-Derived Factors
3.1.1. Host Physical and Chemical (Non-Immune) Defenses
3.1.2. Host Immune Defenses
3.2. Gut Microbiota
3.2.1. Evidences for a Role of Gut Microbiota in Protection against Listeria monocytogenes
3.2.2. Possible Mechanisms Involved in Microbiota-Mediated Colonization Resistance against Listeria monocytogenes
4. Conclusions
Acknowledgments
Conflicts of Interest
References
- Swaminathan, B.; Gerner-Smidt, P. The epidemiology of human listeriosis. Microbes Infect. Inst. Pasteur 2007, 9, 1236–1243. [Google Scholar] [CrossRef] [PubMed]
- Vazquez-Boland, J.A.; Kuhn, M.; Berche, P.; Chakraborty, T.; Dominguez-Bernal, G.; Goebel, W.; Gonzalez-Zorn, B.; Wehland, J.; Kreft, J. Listeria pathogenesis and molecular virulence determinants. Clin. Microbiol. Rev. 2001, 14, 584–640. [Google Scholar] [CrossRef] [PubMed]
- Centers for Disease Control and Prevention (CDC). Listeria Outbreaks. Available online: http://www.cdc.gov/listeria/outbreaks/index.html (accessed on 21 December 2017).
- Lecuit, M. Understanding how listeria monocytogenes targets and crosses host barriers. Clin. Microbiol. Infect. 2005, 11, 430–436. [Google Scholar] [CrossRef] [PubMed]
- Marco, A.J.; Altimira, J.; Prats, N.; Lopez, S.; Dominguez, L.; Domingo, M.; Briones, V. Penetration of listeria monocytogenes in mice infected by the oral route. Microb. Pathog. 1997, 23, 255–263. [Google Scholar] [CrossRef] [PubMed]
- Pron, B.; Boumaila, C.; Jaubert, F.; Sarnacki, S.; Monnet, J.P.; Berche, P.; Gaillard, J.L. Comprehensive study of the intestinal stage of listeriosis in a rat ligated ileal loop system. Infect. Immun. 1998, 66, 747–755. [Google Scholar] [PubMed]
- MacDonald, T.T.; Carter, P.B. Cell-mediated immunity to intestinal infection. Infect. Immun. 1980, 28, 516–523. [Google Scholar] [PubMed]
- Corr, S.; Hill, C.; Gahan, C.G. An in vitro cell-culture model demonstrates internalin- and hemolysin-independent translocation of listeria monocytogenes across m cells. Microb. Pathog. 2006, 41, 241–250. [Google Scholar] [CrossRef] [PubMed]
- Chiba, S.; Nagai, T.; Hayashi, T.; Baba, Y.; Nagai, S.; Koyasu, S. Listerial invasion protein internalin b promotes entry into ileal peyer’s patches in vivo. Microbiol. Immunol. 2011, 55, 123–129. [Google Scholar] [CrossRef] [PubMed]
- Bou Ghanem, E.N.; Jones, G.S.; Myers-Morales, T.; Patil, P.D.; Hidayatullah, A.N.; D’Orazio, S.E. Inla promotes dissemination of listeria monocytogenes to the mesenteric lymph nodes during food borne infection of mice. PLoS Pathog. 2012, 8, e1003015. [Google Scholar] [CrossRef] [PubMed]
- Jensen, V.B.; Harty, J.T.; Jones, B.D. Interactions of the invasive pathogens salmonella typhimurium, listeria monocytogenes, and shigella flexneri with m cells and murine peyer’s patches. Infect. Immun. 1998, 66, 3758–3766. [Google Scholar] [PubMed]
- Dalton, C.B.; Austin, C.C.; Sobel, J.; Hayes, P.S.; Bibb, W.F.; Graves, L.M.; Swaminathan, B.; Proctor, M.E.; Griffin, P.M. An outbreak of gastroenteritis and fever due to listeria monocytogenes in milk. N. Engl. J. Med. 1997, 336, 100–105. [Google Scholar] [CrossRef] [PubMed]
- Aureli, P.; Fiorucci, G.C.; Caroli, D.; Marchiaro, G.; Novara, O.; Leone, L.; Salmaso, S. An outbreak of febrile gastroenteritis associated with corn contaminated by listeria monocytogenes. N. Engl. J. Med. 2000, 342, 1236–1241. [Google Scholar] [CrossRef] [PubMed]
- Esteban, J.I.; Oporto, B.; Aduriz, G.; Juste, R.A.; Hurtado, A. Faecal shedding and strain diversity of listeria monocytogenes in healthy ruminants and swine in northern spain. BMC Vet. Res. 2009, 5, 2. [Google Scholar] [CrossRef] [PubMed]
- Iida, T.; Kanzaki, M.; Nakama, A.; Kokubo, Y.; Maruyama, T.; Kaneuchi, C. Detection of listeria monocytogenes in humans, animals and foods. J. Vet. Med. Sci. 1998, 60, 1341–1343. [Google Scholar] [CrossRef] [PubMed]
- Yokoyama, E.; Saitoh, T.; Maruyama, S.; Katsube, Y. The marked increase of listeria monocytogenes isolation from contents of swine cecum. Comp. Immunol. Microbiol. Infect. Dis. 2005, 28, 259–268. [Google Scholar] [CrossRef] [PubMed]
- Garrec, N.; Picard-Bonnaud, F.; Pourcher, A.M. Occurrence oflisteriasp. Andl. Monocytogenesin sewage sludge used for land application: Effect of dewatering, liming and storage in tank on survival oflisteriaspecies. FEMS Immunol. Med. Microbiol. 2003, 35, 275–283. [Google Scholar] [CrossRef]
- Kampelmacher, E.H.; van Noorle Jansen, L.M. Isolation of listeria monocytogenes from faeces of clinically healthy humans and animals. Zent. Bakteriol. Orig. 1969, 211, 353–359. [Google Scholar]
- Cobb, C.A.; Curtis, G.D.; Bansi, D.S.; Slade, E.; Mehal, W.; Mitchell, R.G.; Chapman, R.W. Increased prevalence of listeria monocytogenes in the faeces of patients receiving long-term H2-antagonists. Eur. J. Gastroenterol. Hepatol. 1996, 8, 1071–1074. [Google Scholar] [CrossRef] [PubMed]
- Grif, K.; Patscheider, G.; Dierich, M.P.; Allerberger, F. Incidence of fecal carriage of listeria monocytogenes in three healthy volunteers: A one-year prospective stool survey. Eur. J. Clin. Microbiol. Infect. Dis. 2003, 22, 16–20. [Google Scholar] [PubMed]
- MacGowan, A.P.; Bowker, K.; McLauchlin, J.; Bennett, P.M.; Reeves, D.S. The occurrence and seasonal changes in the isolation of listeria spp. In shop bought food stuffs, human faeces, sewage and soil from urban sources. Int. J. Food Microbiol. 1994, 21, 325–334. [Google Scholar] [CrossRef]
- Pinner, R.W.; Schuchat, A.; Swaminathan, B.; Hayes, P.S.; Deaver, K.A.; Weaver, R.E.; Plikaytis, B.D.; Reeves, M.; Broome, C.V.; Wenger, J.D. Role of foods in sporadic listeriosis. Ii. Microbiologic and epidemiologic investigation. The listeria study group. JAMA 1992, 267, 2046–2050. [Google Scholar] [CrossRef] [PubMed]
- Schuchat, A.; Deaver, K.A.; Wenger, J.D.; Plikaytis, B.D.; Mascola, L.; Pinner, R.W.; Reingold, A.L.; Broome, C.V. Role of foods in sporadic listeriosis. I. Case-control study of dietary risk factors. The listeria study group. JAMA 1992, 267, 2041–2045. [Google Scholar] [CrossRef] [PubMed]
- Ooi, S.T.; Lorber, B. Gastroenteritis due to listeria monocytogenes. Clin. Infect. Dis. 2005, 40, 1327–1332. [Google Scholar] [CrossRef] [PubMed]
- Barbuddhe, S.B.; Chakraborty, T. Listeria as an enteroinvasive gastrointestinal pathogen. Curr. Top. Microbiol. Immunol. 2009, 337, 173–195. [Google Scholar] [PubMed]
- Zhang, T.; Abel, S.; Abel Zur Wiesch, P.; Sasabe, J.; Davis, B.M.; Higgins, D.E.; Waldor, M.K. Deciphering the landscape of host barriers to listeria monocytogenes infection. Proc. Natl. Acad. Sci. USA 2017, 114, 6334–6339. [Google Scholar] [CrossRef] [PubMed]
- Melton-Witt, J.A.; Rafelski, S.M.; Portnoy, D.A.; Bakardjiev, A.I. Oral infection with signature-tagged listeria monocytogenes reveals organ-specific growth and dissemination routes in guinea pigs. Infect. Immun. 2012, 80, 720–732. [Google Scholar] [CrossRef] [PubMed]
- Becattini, S.; Littmann, E.R.; Carter, R.A.; Kim, S.G.; Morjaria, S.M.; Ling, L.; Gyaltshen, Y.; Fontana, E.; Taur, Y.; Leiner, I.M.; et al. Commensal microbes provide first line defense against listeria monocytogenes infection. J. Exp. Med. 2017, 214, 1973–1989. [Google Scholar] [CrossRef] [PubMed]
- Havell, E.A.; Beretich, G.R.; Carter, P.B. The mucosal phase of listeria infection. Immunobiology 1999, 201, 164–177. [Google Scholar] [CrossRef]
- Bailey, J.S.; Fletcher, D.L.; Cox, N.A. Listeria monocytogenes colonization of broiler chickens. Poult. Sci. 1990, 69, 457–461. [Google Scholar] [CrossRef] [PubMed]
- Nikitas, G.; Deschamps, C.; Disson, O.; Niault, T.; Cossart, P.; Lecuit, M. Transcytosis of listeria monocytogenes across the intestinal barrier upon specific targeting of goblet cell accessible e-cadherin. J. Exp. Med. 2011, 208, 2263–2277. [Google Scholar] [CrossRef] [PubMed]
- Nishikawa, S.; Hirasue, M.; Miura, T.; Yamada, K.; Sasaki, S.; Nakane, A. Systemic dissemination by intrarectal infection with listeria monocytogenes in mice. Microbiol. Immunol. 1998, 42, 325–327. [Google Scholar] [CrossRef] [PubMed]
- Marco, A.J.; Prats, N.; Ramos, J.A.; Briones, V.; Blanco, M.; Dominguez, L.; Domingo, M. A microbiological, histopathological and immunohistological study of the intragastric inoculation of listeria monocytogenes in mice. J. Comp. Pathol. 1992, 107, 1–9. [Google Scholar] [CrossRef]
- Gahan, C.G.; Hill, C. Gastrointestinal phase of listeria monocytogenes infection. J. Appl. Microbiol. 2005, 98, 1345–1353. [Google Scholar] [CrossRef] [PubMed]
- Toledo-Arana, A.; Dussurget, O.; Nikitas, G.; Sesto, N.; Guet-Revillet, H.; Balestrino, D.; Loh, E.; Gripenland, J.; Tiensuu, T.; Vaitkevicius, K.; et al. The listeria transcriptional landscape from saprophytism to virulence. Nature 2009, 459, 950–956. [Google Scholar] [CrossRef] [PubMed]
- Jiang, L.; Olesen, I.; Andersen, T.; Fang, W.; Jespersen, L. Survival of listeria monocytogenes in simulated gastrointestinal system and transcriptional profiling of stress- and adhesion-related genes. Foodborne Pathog. Dis. 2010, 7, 267–274. [Google Scholar] [CrossRef] [PubMed]
- Ho, J.L.; Shands, K.N.; Friedland, G.; Eckind, P.; Fraser, D.W. An outbreak of type 4b listeria monocytogenes infection involving patients from eight boston hospitals. Arch. Intern. Med. 1986, 146, 520–524. [Google Scholar] [CrossRef] [PubMed]
- Schlech, W.F., 3rd; Chase, D.P.; Badley, A. A model of food-borne listeria monocytogenes infection in the sprague-dawley rat using gastric inoculation: Development and effect of gastric acidity on infective dose. Int. J. Food Microbiol. 1993, 18, 15–24. [Google Scholar] [CrossRef]
- Brandl, K.; Plitas, G.; Schnabl, B.; DeMatteo, R.P.; Pamer, E.G. MyD88-mediated signals induce the bactericidal lectin regiii gamma and protect mice against intestinal listeria monocytogenes infection. J. Exp. Med. 2007, 204, 1891–1900. [Google Scholar] [CrossRef] [PubMed]
- Saklani-Jusforgues, H.; Fontan, E.; Goossens, P.L. Effect of acid-adaptation on listeria monocytogenes survival and translocation in a murine intragastric infection model. FEMS Microbiol. Lett. 2000, 193, 155–159. [Google Scholar] [CrossRef] [PubMed]
- Sue, D.; Fink, D.; Wiedmann, M.; Boor, K.J. Sigmab-dependent gene induction and expression in listeria monocytogenes during osmotic and acid stress conditions simulating the intestinal environment. Microbiology 2004, 150, 3843–3855. [Google Scholar] [CrossRef] [PubMed]
- Barmpalia-Davis, I.M.; Geornaras, I.; Kendall, P.A.; Sofos, J.N. Differences in survival among 13 listeria monocytogenes strains in a dynamic model of the stomach and small intestine. Appl. Environ. Microbiol. 2008, 74, 5563–5567. [Google Scholar] [CrossRef] [PubMed]
- Sleator, R.D.; Wouters, J.; Gahan, C.G.; Abee, T.; Hill, C. Analysis of the role of opuc, an osmolyte transport system, in salt tolerance and virulence potential of listeria monocytogenes. Appl. Environ. Microbiol. 2001, 67, 2692–2698. [Google Scholar] [CrossRef] [PubMed]
- Buffie, C.G.; Bucci, V.; Stein, R.R.; McKenney, P.T.; Ling, L.; Gobourne, A.; No, D.; Liu, H.; Kinnebrew, M.; Viale, A.; et al. Precision microbiome reconstitution restores bile acid mediated resistance to clostridium difficile. Nature 2015, 517, 205–208. [Google Scholar] [CrossRef] [PubMed]
- Gunn, J.S. Mechanisms of bacterial resistance and response to bile. Microb. Infect. Inst. Pasteur 2000, 2, 907–913. [Google Scholar] [CrossRef]
- Hofmann, A.F.; Eckmann, L. How bile acids confer gut mucosal protection against bacteria. Proc. Natl Acad. Sci. USA 2006, 103, 4333–4334. [Google Scholar] [CrossRef] [PubMed]
- Hardy, J.; Francis, K.P.; DeBoer, M.; Chu, P.; Gibbs, K.; Contag, C.H. Extracellular replication of listeria monocytogenes in the murine gall bladder. Science 2004, 303, 851–853. [Google Scholar] [CrossRef] [PubMed]
- Hardy, J.; Margolis, J.J.; Contag, C.H. Induced biliary excretion of listeria monocytogenes. Infect. Immun. 2006, 74, 1819–1827. [Google Scholar] [CrossRef] [PubMed]
- Dussurget, O.; Cabanes, D.; Dehoux, P.; Lecuit, M.; Buchrieser, C.; Glaser, P.; Cossart, P.; European Listeria Genome, C. Listeria monocytogenes bile salt hydrolase is a prfa-regulated virulence factor involved in the intestinal and hepatic phases of listeriosis. Mol. Microbiol. 2002, 45, 1095–1106. [Google Scholar] [CrossRef] [PubMed]
- Begley, M.; Gahan, C.G.M.; Hill, C. Bile stress response in listeria monocytogenes lo28: Adaptation, cross-protection, and identification of genetic loci involved in bile resistance. Appl. Environ. Microbiol. 2002, 68, 6005–6012. [Google Scholar] [CrossRef] [PubMed]
- Begley, M.; Sleator, R.D.; Gahan, C.G.; Hill, C. Contribution of three bile-associated loci, bsh, pva, and btlb, to gastrointestinal persistence and bile tolerance of listeria monocytogenes. Infect. Immun. 2005, 73, 894–904. [Google Scholar] [CrossRef] [PubMed]
- Sleator, R.D.; Wemekamp-Kamphuis, H.H.; Gahan, C.G.; Abee, T.; Hill, C. A prfa-regulated bile exclusion system (bile) is a novel virulence factor in listeria monocytogenes. Mol. Microbiol. 2005, 55, 1183–1195. [Google Scholar] [CrossRef] [PubMed]
- Watson, D.; Sleator, R.D.; Casey, P.G.; Hill, C.; Gahan, C.G. Specific osmolyte transporters mediate bile tolerance in listeria monocytogenes. Infect. Immun. 2009, 77, 4895–4904. [Google Scholar] [CrossRef] [PubMed]
- Travier, L.; Guadagnini, S.; Gouin, E.; Dufour, A.; Chenal-Francisque, V.; Cossart, P.; Olivo-Marin, J.C.; Ghigo, J.M.; Disson, O.; Lecuit, M. Acta promotes listeria monocytogenes aggregation, intestinal colonization and carriage. PLoS Pathog. 2013, 9, e1003131. [Google Scholar] [CrossRef] [PubMed]
- Jaradat, Z.W.; Bhunia, A.K. Glucose and nutrient concentrations affect the expression of a 104-kilodalton listeria adhesion protein in listeria monocytogenes. Appl. Environ. Microbiol. 2002, 68, 4876–4883. [Google Scholar] [CrossRef] [PubMed]
- Johansson, M.E.; Hansson, G.C. Immunological aspects of intestinal mucus and mucins. Nat. Rev. Immunol. 2016, 16, 639–649. [Google Scholar] [CrossRef] [PubMed]
- Mariscotti, J.F.; Quereda, J.J.; Garcia-Del Portillo, F.; Pucciarelli, M.G. The listeria monocytogenes lpxtg surface protein LMO1413 is an invasin with capacity to bind mucin. Int. J. Med. Microbiol. 2014, 304, 393–404. [Google Scholar] [CrossRef] [PubMed]
- Popowska, M.; Krawczyk-Balska, A.; Ostrowski, R.; Desvaux, M. Inll from listeria monocytogenes is involved in biofilm formation and adhesion to mucin. Front. Microbiol. 2017, 8, 660. [Google Scholar] [CrossRef] [PubMed]
- Linden, S.K.; Bierne, H.; Sabet, C.; Png, C.W.; Florin, T.H.; McGuckin, M.A.; Cossart, P. Listeria monocytogenes internalins bind to the human intestinal mucin MUC2. Arch. Microbiol. 2008, 190, 101–104. [Google Scholar] [CrossRef] [PubMed]
- Richter, J.F.; Gitter, A.H.; Gunzel, D.; Weiss, S.; Mohamed, W.; Chakraborty, T.; Fromm, M.; Schulzke, J.D. Listeriolysin O affects barrier function and induces chloride secretion in HT-29/B6 colon epithelial cells. Am. J. Physiol. Gastrointest. Liver Physiol. 2009, 296, G1350–G1359. [Google Scholar] [CrossRef] [PubMed]
- Lievin-Le Moal, V.; Servin, A.L.; Coconnier-Polter, M.H. The increase in mucin exocytosis and the upregulation of muc genes encoding for membrane-bound mucins induced by the thiol-activated exotoxin listeriolysin O is a host cell defence response that inhibits the cell-entry of listeria monocytogenes. Cell. Microbiol. 2005, 7, 1035–1048. [Google Scholar] [CrossRef] [PubMed]
- Coconnier, M.H.; Dlissi, E.; Robard, M.; Laboisse, C.L.; Gaillard, J.L.; Servin, A.L. Listeria monocytogenes stimulates mucus exocytosis in cultured human polarized mucosecreting intestinal cells through action of listeriolysin O. Infect. Immun. 1998, 66, 3673–3681. [Google Scholar] [PubMed]
- Neudeck, B.L.; Loeb, J.M.; Faith, N.G.; Czuprynski, C.J. Intestinal P glycoprotein acts as a natural defense mechanism against listeria monocytogenes. Infect. Immun. 2004, 72, 3849–3854. [Google Scholar] [CrossRef] [PubMed]
- Manohar, M.; Baumann, D.O.; Bos, N.A.; Cebra, J.J. Gut colonization of mice with acta-negative mutant of listeria monocytogenes can stimulate a humoral mucosal immune response. Infect. Immun. 2001, 69, 3542–3549. [Google Scholar] [CrossRef] [PubMed]
- Kinnebrew, M.A.; Buffie, C.G.; Diehl, G.E.; Zenewicz, L.A.; Leiner, I.; Hohl, T.M.; Flavell, R.A.; Littman, D.R.; Pamer, E.G. Interleukin 23 production by intestinal CD103(+)CD11b(+) dendritic cells in response to bacterial flagellin enhances mucosal innate immune defense. Immunity 2012, 36, 276–287. [Google Scholar] [CrossRef] [PubMed]
- Mukherjee, S.; Zheng, H.; Derebe, M.G.; Callenberg, K.M.; Partch, C.L.; Rollins, D.; Propheter, D.C.; Rizo, J.; Grabe, M.; Jiang, Q.X.; et al. Antibacterial membrane attack by a pore-forming intestinal C-type lectin. Nature 2014, 505, 103–107. [Google Scholar] [CrossRef] [PubMed]
- Kobayashi, K.S.; Chamaillard, M.; Ogura, Y.; Henegariu, O.; Inohara, N.; Nunez, G.; Flavell, R.A. NOD2-dependent regulation of innate and adaptive immunity in the intestinal tract. Science 2005, 307, 731–734. [Google Scholar] [CrossRef] [PubMed]
- Veldhuizen, E.J.; Rijnders, M.; Claassen, E.A.; van Dijk, A.; Haagsman, H.P. Porcine beta-defensin 2 displays broad antimicrobial activity against pathogenic intestinal bacteria. Mol. Immunol. 2008, 45, 386–394. [Google Scholar] [CrossRef] [PubMed]
- Harwig, S.S.; Tan, L.; Qu, X.D.; Cho, Y.; Eisenhauer, P.B.; Lehrer, R.I. Bactericidal properties of murine intestinal phospholipase A2. J. Clin. Investig. 1995, 95, 603–610. [Google Scholar] [CrossRef] [PubMed]
- Menard, S.; Forster, V.; Lotz, M.; Gutle, D.; Duerr, C.U.; Gallo, R.L.; Henriques-Normark, B.; Putsep, K.; Andersson, M.; Glocker, E.O.; et al. Developmental switch of intestinal antimicrobial peptide expression. J. Exp. Med. 2008, 205, 183–193. [Google Scholar] [CrossRef] [PubMed]
- Meyer-Hoffert, U.; Hornef, M.W.; Henriques-Normark, B.; Axelsson, L.G.; Midtvedt, T.; Putsep, K.; Andersson, M. Secreted enteric antimicrobial activity localises to the mucus surface layer. Gut 2008, 57, 764–771. [Google Scholar] [CrossRef] [PubMed]
- Johansson, M.E.; Jakobsson, H.E.; Holmen-Larsson, J.; Schutte, A.; Ermund, A.; Rodriguez-Pineiro, A.M.; Arike, L.; Wising, C.; Svensson, F.; Backhed, F.; et al. Normalization of host intestinal mucus layers requires long-term microbial colonization. Cell Host Microbe 2015, 18, 582–592. [Google Scholar] [CrossRef] [PubMed]
- Brandl, K.; Plitas, G.; Mihu, C.N.; Ubeda, C.; Jia, T.; Fleisher, M.; Schnabl, B.; DeMatteo, R.P.; Pamer, E.G. Vancomycin-resistant enterococci exploit antibiotic-induced innate immune deficits. Nature 2008, 455, 804–807. [Google Scholar] [CrossRef] [PubMed]
- Long, S.L.; Gahan, C.G.M.; Joyce, S.A. Interactions between gut bacteria and bile in health and disease. Mol. Aspects Med. 2017, 56, 54–65. [Google Scholar] [CrossRef] [PubMed]
- Khosravi, A.; Yanez, A.; Price, J.G.; Chow, A.; Merad, M.; Goodridge, H.S.; Mazmanian, S.K. Gut microbiota promote hematopoiesis to control bacterial infection. Cell Host Microbe 2014, 15, 374–381. [Google Scholar] [CrossRef] [PubMed]
- Abt, M.C.; Osborne, L.C.; Monticelli, L.A.; Doering, T.A.; Alenghat, T.; Sonnenberg, G.F.; Paley, M.A.; Antenus, M.; Williams, K.L.; Erikson, J.; et al. Commensal bacteria calibrate the activation threshold of innate antiviral immunity. Immunity 2012, 37, 158–170. [Google Scholar] [CrossRef] [PubMed]
- Becattini, S.; Taur, Y.; Pamer, E.G. Antibiotic-induced changes in the intestinal microbiota and disease. Trends Mol. Med. 2016, 22, 458–478. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Q.; Pan, Y.; Yan, R.; Zeng, B.; Wang, H.; Zhang, X.; Li, W.; Wei, H.; Liu, Z. Commensal bacteria direct selective cargo sorting to promote symbiosis. Nat. Immunol. 2015, 16, 918–926. [Google Scholar] [CrossRef] [PubMed]
- Cabinian, A.; Sinsimer, D.; Tang, M.; Jang, Y.; Choi, B.; Laouar, Y.; Laouar, A. Gut symbiotic microbes imprint intestinal immune cells with the innate receptor SLAMF4 which contributes to gut immune protection against enteric pathogens. Gut 2017. [Google Scholar] [CrossRef] [PubMed]
- Archambaud, C.; Nahori, M.A.; Soubigou, G.; Becavin, C.; Laval, L.; Lechat, P.; Smokvina, T.; Langella, P.; Lecuit, M.; Cossart, P. Impact of lactobacilli on orally acquired listeriosis. Proc. Natl. Acad. Sci. USA 2012, 109, 16684–16689. [Google Scholar] [CrossRef] [PubMed]
- Corr, S.C.; Gahan, C.G.; Hill, C. Impact of selected lactobacillus and bifidobacterium species on listeria monocytogenes infection and the mucosal immune response. FEMS Immunol. Med. Microbiol. 2007, 50, 380–388. [Google Scholar] [CrossRef] [PubMed]
- Pamer, E.G. Resurrecting the intestinal microbiota to combat antibiotic-resistant pathogens. Science 2016, 352, 535–538. [Google Scholar] [CrossRef] [PubMed]
- Bohnhoff, M.; Drake, B.L.; Miller, C.P. Effect of streptomycin on susceptibility of intestinal tract to experimental salmonella infection. Proc. Soc. Exp. Biol. Med. 1954, 86, 132–137. [Google Scholar] [CrossRef] [PubMed]
- Lewis, B.B.; Buffie, C.G.; Carter, R.A.; Leiner, I.; Toussaint, N.C.; Miller, L.C.; Gobourne, A.; Ling, L.; Pamer, E.G. Loss of microbiota-mediated colonization resistance to clostridium difficile infection with oral vancomycin compared with metronidazole. J. Infect. Dis. 2015, 212, 1656–1665. [Google Scholar] [CrossRef] [PubMed]
- Zachar, Z.; Savage, D.C. Microbial interference and colonization of the murine gastrointestinal tract by listeria monocytogenes. Infect. Immun. 1979, 23, 168–174. [Google Scholar] [PubMed]
- Czuprynski, C.J.; Balish, E. Pathogenesis of listeria monocytogenes for gnotobiotic rats. Infect. Immun. 1981, 32, 323–331. [Google Scholar] [PubMed]
- Round, J.L.; Mazmanian, S.K. The gut microbiota shapes intestinal immune responses during health and disease. Nat. Rev. Immunol. 2009, 9, 313–323. [Google Scholar] [CrossRef] [PubMed]
- Schlech, W.F., 3rd. An animal model of foodborne listeria monocytogenes virulence: Effect of alterations in local and systemic immunity on invasive infection. Clin. Investig. Med. 1993, 16, 219–225. [Google Scholar]
- Okamoto, M.; Nakane, A.; Minagawa, T. Host resistance to an intragastric infection with listeria monocytogenes in mice depends on cellular immunity and intestinal bacterial flora. Infect. Immun. 1994, 62, 3080–3085. [Google Scholar] [PubMed]
- Vijayakumar, P.P.; Muriana, P.M. A microplate growth inhibition assay for screening bacteriocins against listeria monocytogenes to differentiate their mode-of-action. Biomolecules 2015, 5, 1178–1194. [Google Scholar] [CrossRef] [PubMed]
- Zhu, W.M.; Liu, W.; Wu, D.Q. Isolation and characterization of a new bacteriocin from lactobacillus gasseri kt7. J. Appl. Microbiol. 2000, 88, 877–886. [Google Scholar] [CrossRef] [PubMed]
- Allende, A.; Martinez, B.; Selma, V.; Gil, M.I.; Suarez, J.E.; Rodriguez, A. Growth and bacteriocin production by lactic acid bacteria in vegetable broth and their effectiveness at reducing listeria monocytogenes in vitro and in fresh-cut lettuce. Food Microbiol. 2007, 24, 759–766. [Google Scholar] [CrossRef] [PubMed]
- Gibson, G.R.; Wang, X. Regulatory effects of bifidobacteria on the growth of other colonic bacteria. J. Appl. Bacteriol. 1994, 77, 412–420. [Google Scholar] [CrossRef] [PubMed]
- Yang, D.; Wu, X.; Yu, X.; He, L.; Shah, N.P.; Xu, F. Mutual growth-promoting effect between bifidobacterium bifidum wbbi03 and listeria monocytogenes cmcc 54001. J. Dairy Sci. 2017, 100, 3448–3462. [Google Scholar] [CrossRef] [PubMed]
- Odamaki, T.; Kato, K.; Sugahara, H.; Hashikura, N.; Takahashi, S.; Xiao, J.Z.; Abe, F.; Osawa, R. Age-related changes in gut microbiota composition from newborn to centenarian: A cross-sectional study. BMC Microbiol. 2016, 16, 90. [Google Scholar] [CrossRef] [PubMed]
- Yatsunenko, T.; Rey, F.E.; Manary, M.J.; Trehan, I.; Dominguez-Bello, M.G.; Contreras, M.; Magris, M.; Hidalgo, G.; Baldassano, R.N.; Anokhin, A.P.; et al. Human gut microbiome viewed across age and geography. Nature 2012, 486, 222–227. [Google Scholar] [CrossRef] [PubMed]
- Koren, O.; Goodrich, J.K.; Cullender, T.C.; Spor, A.; Laitinen, K.; Backhed, H.K.; Gonzalez, A.; Werner, J.J.; Angenent, L.T.; Knight, R.; et al. Host remodeling of the gut microbiome and metabolic changes during pregnancy. Cell 2012, 150, 470–480. [Google Scholar] [CrossRef] [PubMed]
- Lozupone, C.A.; Stombaugh, J.I.; Gordon, J.I.; Jansson, J.K.; Knight, R. Diversity, stability and resilience of the human gut microbiota. Nature 2012, 489, 220–230. [Google Scholar] [CrossRef] [PubMed]
- Menudier, A.; Bosgiraud, C.; Nicolas, J.A. Virulence of listeria monocytogenes in pregnant mice. Pathol. Biol. 1994, 42, 510–515. [Google Scholar] [PubMed]
- Kerr, A.K.; Farrar, A.M.; Waddell, L.A.; Wilkins, W.; Wilhelm, B.J.; Bucher, O.; Wills, R.W.; Bailey, R.H.; Varga, C.; McEwen, S.A.; et al. A systematic review-meta-analysis and meta-regression on the effect of selected competitive exclusion products on salmonella spp. Prevalence and concentration in broiler chickens. Prev. Vet. Med. 2013, 111, 112–125. [Google Scholar] [CrossRef] [PubMed]
- Wagner, R.D.; Holland, M.; Cerniglia, C.E. An in vitro assay to evaluate competitive exclusion products for poultry. J. Food Prot. 2002, 65, 746–751. [Google Scholar] [CrossRef] [PubMed]
- Hume, M.E.; Byrd, J.A.; Stanker, L.H.; Ziprin, R.L. Reduction of caecal listeria monocytogenes in leghorn chicks following treatment with a competitive exclusion culture (preempt). Lett. Appl. Microbiol. 1998, 26, 432–436. [Google Scholar] [CrossRef] [PubMed]
- Cotter, P.D.; Hill, C.; Ross, R.P. Bacteriocins: Developing innate immunity for food. Nat. Rev. Microbiol. 2005, 3, 777–788. [Google Scholar] [CrossRef] [PubMed]
- Turgis, M.; Vu, K.D.; Lacroix, M. Partial characterization of bacteriocins produced by two new enterococcus faecium isolated from human intestine. Probiotics Antimicrob. Proteins 2013, 5, 110–120. [Google Scholar] [CrossRef] [PubMed]
- Lakshminarayanan, B.; Guinane, C.M.; O’Connor, P.M.; Coakley, M.; Hill, C.; Stanton, C.; O’Toole, P.W.; Ross, R.P. Isolation and characterization of bacteriocin-producing bacteria from the intestinal microbiota of elderly irish subjects. J. Appl. Microbiol. 2013, 114, 886–898. [Google Scholar] [CrossRef] [PubMed]
- Millette, M.; Dupont, C.; Shareck, F.; Ruiz, M.T.; Archambault, D.; Lacroix, M. Purification and identification of the pediocin produced by pediococcus acidilactici MM33, a new human intestinal strain. J. Appl. Microbiol. 2008, 104, 269–275. [Google Scholar] [CrossRef] [PubMed]
- Le Blay, G.; Hammami, R.; Lacroix, C.; Fliss, I. Stability and inhibitory activity of pediocin pa-1 against listeria sp. In simulated physiological conditions of the human terminal ileum. Probiotics Antimicrob. Proteins 2012, 4, 250–258. [Google Scholar] [CrossRef] [PubMed]
- Guinane, C.M.; Cotter, P.D.; Hill, C.; Ross, R.P. Microbial solutions to microbial problems; lactococcal bacteriocins for the control of undesirable biota in food. J. Appl. Microbiol. 2005, 98, 1316–1325. [Google Scholar] [CrossRef] [PubMed]
- Campion, A.; Casey, P.G.; Field, D.; Cotter, P.D.; Hill, C.; Ross, R.P. In vivo activity of nisin a and nisin v against listeria monocytogenes in mice. BMC Microbiol. 2013, 13, 23. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Field, D.; Quigley, L.; O’Connor, P.M.; Rea, M.C.; Daly, K.; Cotter, P.D.; Hill, C.; Ross, R.P. Studies with bioengineered nisin peptides highlight the broad-spectrum potency of nisin v. Microb. Biotechnol. 2010, 3, 473–486. [Google Scholar] [CrossRef] [PubMed]
- Benkerroum, N.; Sandine, W.E. Inhibitory action of nisin against listeria monocytogenes. J. Dairy Sci. 1988, 71, 3237–3245. [Google Scholar] [CrossRef]
- Collins, F.W.; O’Connor, P.M.; O’Sullivan, O.; Rea, M.C.; Hill, C.; Ross, R.P. Formicin—A novel broad-spectrum two-component lantibiotic produced by bacillus paralicheniformis APC 1576. Microbiology 2016, 162, 1662–1671. [Google Scholar] [CrossRef] [PubMed]
- Corr, S.C.; Li, Y.; Riedel, C.U.; O’Toole, P.W.; Hill, C.; Gahan, C.G. Bacteriocin production as a mechanism for the antiinfective activity of lactobacillus salivarius ucc118. Proc. Natl. Acad. Sci. USA 2007, 104, 7617–7621. [Google Scholar] [CrossRef] [PubMed]
- Altenhoefer, A.; Oswald, S.; Sonnenborn, U.; Enders, C.; Schulze, J.; Hacker, J.; Oelschlaeger, T.A. The probioticescherichia colistrain nissle 1917 interferes with invasion of human intestinal epithelial cells by different enteroinvasive bacterial pathogens. FEMS Immunol. Med. Microbiol. 2004, 40, 223–229. [Google Scholar] [CrossRef]
- Blom, H.; Nerbrink, E.; Dainty, R.; Hagtvedt, T.; Borch, E.; Nissen, H.; Nesbakken, T. Addition of 2.5% lactate and 0.25% acetate controls growth of listeria monocytogenes in vacuum-packed, sensory-acceptable servelat sausage and cooked ham stored at 4 degrees C. Int. J. Food Microbiol. 1997, 38, 71–76. [Google Scholar] [CrossRef]
- Hinton, A., Jr.; Hume, M.E. Research note: In vitro inhibition of listeria monocytogenes growth by veillonellae cultures grown on tartrate media. J. Appl. Microbiol. 1997, 82, 780–782. [Google Scholar] [CrossRef] [PubMed]
- Aoki, S.K.; Diner, E.J.; de Roodenbeke, C.T.; Burgess, B.R.; Poole, S.J.; Braaten, B.A.; Jones, A.M.; Webb, J.S.; Hayes, C.S.; Cotter, P.A.; et al. A widespread family of polymorphic contact-dependent toxin delivery systems in bacteria. Nature 2010, 468, 439–442. [Google Scholar] [CrossRef] [PubMed]
- Aoki, S.K.; Pamma, R.; Hernday, A.D.; Bickham, J.E.; Braaten, B.A.; Low, D.A. Contact-dependent inhibition of growth in escherichia coli. Science 2005, 309, 1245–1248. [Google Scholar] [CrossRef] [PubMed]
- Saraoui, T.; Fall, P.A.; Leroi, F.; Antignac, J.P.; Chereau, S.; Pilet, M.F. Inhibition mechanism of listeria monocytogenes by a bioprotective bacteria lactococcus piscium cncm i-4031. Food Microbiol. 2016, 53, 70–78. [Google Scholar] [CrossRef] [PubMed]
- Zilelidou, E.A.; Rychli, K.; Manthou, E.; Ciolacu, L.; Wagner, M.; Skandamis, P.N. Highly invasive listeria monocytogenes strains have growth and invasion advantages in strain competition. PLoS ONE 2015, 10, e0141617. [Google Scholar] [CrossRef] [PubMed]
- Whitney, J.C.; Peterson, S.B.; Kim, J.; Pazos, M.; Verster, A.J.; Radey, M.C.; Kulasekara, H.D.; Ching, M.Q.; Bullen, N.P.; Bryant, D.; et al. A broadly distributed toxin family mediates contact-dependent antagonism between gram-positive bacteria. Elife 2017, 6, e26938. [Google Scholar] [CrossRef] [PubMed]
- Quereda, J.J.; Dussurget, O.; Nahori, M.A.; Ghozlane, A.; Volant, S.; Dillies, M.A.; Regnault, B.; Kennedy, S.; Mondot, S.; Villoing, B.; et al. Bacteriocin from epidemic listeria strains alters the host intestinal microbiota to favor infection. Proc. Natl. Acad. Sci. USA 2016, 113, 5706–5711. [Google Scholar] [CrossRef] [PubMed]
© 2017 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Becattini, S.; Pamer, E.G. Multifaceted Defense against Listeria monocytogenes in the Gastro-Intestinal Lumen. Pathogens 2018, 7, 1. https://doi.org/10.3390/pathogens7010001
Becattini S, Pamer EG. Multifaceted Defense against Listeria monocytogenes in the Gastro-Intestinal Lumen. Pathogens. 2018; 7(1):1. https://doi.org/10.3390/pathogens7010001
Chicago/Turabian StyleBecattini, Simone, and Eric G. Pamer. 2018. "Multifaceted Defense against Listeria monocytogenes in the Gastro-Intestinal Lumen" Pathogens 7, no. 1: 1. https://doi.org/10.3390/pathogens7010001