Lactococcus lactis and Lactobacillus salivarius differently modulate early immunological response of Wistar rats co-administered with Listeria monocytogenes

Beneficial Microbes

Volumn 8, Issue 5, 2017, Pages 809-822

  Lukic, J ^a   Jancic, I ^a   Mirkovic, N ^a   Bufan, B ^a   Djokic, J ^a   Milenkovic, M ^a   Begovic, J ^a   Strahinic, I ^a   Lozo, J ^a  

^a UNIVERSITY OF BELGRADE   (Serbia)

Author keywords

CD14; CD69; Lactic acid bacteria; Listeriolysin

Indexed keywords

CD14 ANTIGEN; CD69 ANTIGEN; INTERLEUKIN 1BETA; LISTERIOLYSIN O; MESSENGER RNA; TUMOR NECROSIS FACTOR; IMMUNOLOGIC FACTOR; PROBIOTIC AGENT;

ADAPTIVE IMMUNITY; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTERIAL COUNT; BACTERIAL STRAIN; BACTERIUM DETECTION; CONTROLLED STUDY; ENZYME ACTIVATION; INNATE IMMUNITY; INTESTINE VILLUS; LACTOBACILLUS SALIVARIUS; LACTOCOCCUS LACTIS; LIMIT OF QUANTITATION; LISTERIA MONOCYTOGENES; LISTERIOSIS; MALE; MESENTERY LYMPH NODE; NONHUMAN; PATHOGENESIS; PEYER PATCH; PROTEIN EXPRESSION; PROTEIN RNA BINDING; RAT; ANIMAL; BACTERIAL LOAD; GENE EXPRESSION PROFILING; IMMUNOLOGY; INTESTINE; LYMPH NODE; MICROBIOLOGY; PATHOLOGY; SPLEEN; TREATMENT OUTCOME; WISTAR RAT;

ANIMALS; BACTERIAL LOAD; GENE EXPRESSION PROFILING; IMMUNITY, INNATE; IMMUNOLOGIC FACTORS; INTESTINES; LACTOBACILLUS SALIVARIUS; LACTOCOCCUS LACTIS; LISTERIA MONOCYTOGENES; LISTERIOSIS; LYMPH NODES; MALE; PROBIOTICS; RATS, WISTAR; SPLEEN; TREATMENT OUTCOME;

EID: 85031408529     PISSN: 18762883     EISSN: 18762891     Source Type: Journal    
DOI: 10.3920/BM2017.0007     Document Type: Article

References (53)

1. Anand, P.K., Tait, S.W., Lamkanfi, M., Amer, A.O., Nunez, G., Pagès, G., Pouysségur, J., McGargill, M.A., Green, D.R. and Kanneganti, T.D., 2011. TLR2 and RIP2 pathways mediate autophagy of Listeria monocytogenes via extracellular signal-regulated kinase (ERK) activation. Journal of Biological Chemistry 286: 42981-42991
2. Brenan, M. and Puklavec, M., 1992. The MRC OX-62 antigen: a useful marker in the purification of rat veiled cells with the biochemical properties of an integrin. Journal of Experimetal Medicine 75: 1457-1465
3. Brissette-Storkus, C.S., Kettel, J.C., Whitham, T.F., Giezeman-Smits, K.M., Villa, L.A., Potter, D.M. and Chambers, W.H., 2002. Flt-3 ligand (FL) drives differentiation of rat bone marrow-derived dendritic cells expressing OX62 and/or CD161 (NKR-P1). Journal of Leukocyte Biology 71: 941-949
4. Brzoza, K.L., Rockel, A.B. and Hiltbold, E.M., 2004. Cytoplasmic entry of Listeria monocytogenes enhances dendritic cell maturation and T cell differentiation and function. Journal of Immunology 173: 2641-2651
5. Busarcevic, M., Kojic, M., Dalgalarrondo, M., Chobert, J.M., Haertlé, T. and Topisirovic, L., 2008. Purification of bacteriocin LS1 produced by human oral isolate Lactobacillus salivarius BGHO1. Oral Microbiology and Immunology 23: 254-258
6. Chang, Q., Wang, W., Regev-Yochay, G., Lipsitch, M. and Hanage, W.P., 2015. Antibiotics in agriculture and the risk to human health: how worried should we be? Evolutionary Applications 8: 240-247
7. Chen, J., Shen, J., Ingvar Hellgren, L., Ruhdal Jensen, P. and Solem, C., 2015. Adaptation of Lactococcus lactis to high growth temperature leads to a dramatic increase in acidification rate. Scientific Reports 5: 14199
8. Choy, A. and Roy, C.R., 2013. Autophagy and bacterial infection: an evolving arms race. Trends in Microbiology 21: 451-456
9. Cirkovic, I., Bozic, D.D., Draganic, V., Lozo, J., Beric, T., Kojic, M., Arsic, B., Garalejic, E., Djukic, S. and Stankovic, S., 2016. Licheniocin 50.2 and bacteriocins from Lactococcus lactis subsp. lactis biovar. diacetylactis BGBU1-4 inhibit biofilms of coagulase negative Staphylococci and Listeria monocytogenes clinical isolates. PLoS ONE 11: e0167995
10. Corr, S.C., Li, Y., Riedel, C.U., O'Toole, P.W., Hill, C. and Gahan, C.G., 2007. Bacteriocin production as a mechanism for the antiinfective activity of Lactobacillus salivarius UCC118. Proceedings of the National Academy of Science of the USA 104: 7617-7621
11. Croswell, A., Amir, E., Teggatz, P., Barman, M. and Salzman, N.H., 2009. Prolonged impact of antibiotics on intestinal microbial ecology and susceptibility to enteric Salmonella infection. Infection and Immunity 77: 2741-2753
12. Dalziel, J.E., Young, W., Bercik, P., Spencer, N.J., Ryan, L.J., Dunstan, K.E., Lloyd-West, C.M., Gopal, P.K., Haggarty, N.W. and Roy, N.C., 2016. Tracking gastrointestinal transit of solids in aged rats as pharmacolological models of chronic dysmotility. Neurogastroenterology and Motility 28: 1241-1251
13. Dancz, C.E., Haraga, A., Portnoy, D.A. and Higgins, D.E., 2002. Inducible control of virulence gene expression in Listeria monocytogenes: temporal requirement of listeriolysin O during intracellular infection. Journal of Bacteriology 184: 5935-5945
14. Daniel, C., Poiret, S., Dennin, V., Boutillier, D. and Pot, B., 2013. Bioluminiscence imaging study of spatial and temporal persistence of Lactobacillus plantarum and Lactococcus lactis in living mice. Applied and Environmental Microbiology 79: 1086-1094
15. Daniel, C., Poiret, S., Goudercourt, D., Dennin, V., Leyer, G. and Pot, B., 2006. Selecting lactic acid bacteria for their safety and functionality by use of a mouse colitis model. Applied and Environmental Microbiology 72: 5799-5805
16. De Waard, R., Garssen, J., Bokken, G.C.A.M. and Vos, J.G., 2002. Antagonistic activity of Lactobacillus casei strain Shirota against gastrointestinal Listeria monocytogenes infection in rats. International Journal of Food Microbiology 73: 93-100
17. Eitel, J., Suttorp, N. and Opitz, B., 2011. Innate immune recognition and inflammasome activation in Listeria monocytogenes infection. Frontiers in Microbiology 1: 149
18. Elmore, S.A., 2006. Histopathology of the lymph nodes. Toxicology and Pathology 34: 425-454
19. Elsner, L., Flğge, P.F., Lozano, J., Muppala, V., Eiz-Vesper, B., Demiroglu, S.Y., Malzahn, D., Herrmann, T., Brunner, E., Bickeböller, H., Multhoff, G., Walter, L. and Dressel, R., 2010. The endogenous danger signals HSP70 and MICA cooperate in the activation of cytotoxic effector functions of NK cells. Journal of Cellular and Molecular Medicine 14: 992-1002
20. Feldman, A.T. and Wolfe, D., 2014. Tissue processing and hematoxylin and eosin staining. In: Day, C.E. (ed.) Histopathology-methods and protocols. Humana Press, New York, NY, USA, pp. 31-42
21. Ghanem, E.N.B., Jones, G.S., Myers-Morales, T., Patil, P.D., Hidayatullah, A.N. and D'Orazio, S.E.F., 2012. InlA promotes dissemination of Listeria monocytogenes to the mesenteric lymph nodes during food borne infection of mice. PLoS Pathology 8: e1003015
22. Glomski, I.J., Decatur, A.L. and Portnoy, D.A., 2003. Listeria monocytogenes mutants that fail to compartmentalize listerolysin O activity are cytotoxic, avirulent, and unable to evade host extracellular defenses. Infection and Immunology 71: 6754-6765
23. Grangette, C., Müller-Alouf, H., Hols, P., Goudercourt, D., Delcour, J., Turneer, M. and Mercenier, A., 2004. Enhanced mucosal delivery of antigen with cell wall mutants of lactic acid bacteria. Infection and Immunology 72: 2731-2737
24. Hadley, J.S., Wang, J.E., Foster, S.J., Thiemermann, C. and Hinds, C.J., 2005. Peptidoglycan of Staphylococcus aureus upregualtes monocyte expression of CD14, Toll-like receptor 2 (TLR2), and TLR4 in human blood: possible implications for priming of lipopolysaccharide signaling. Infection and Immunology 73: 7613-7619
25. Harty, J.T., Lenz, L.L. and Bevan, M.J., 1996. Primary and secondary immune responses to Listeria monocytogenes. Current Opinion in Immunology 8: 526-530
26. Hill, C., Guarner, F., Reid, G., Gibson, G.R., Merenstein, D.J., Pot, B., Morelli, L., Canani, R.B., Flint, H.J., Salminen, S., Calder, P.C. and Sanders, M.E., 2014. Expert consensus document. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nature Reviews Gastroenterology and Hepatology 11: 506-514
27. Janeway, Jr., C.A., Travers, P., Walport, M. and Schlomchik, M.J., 2001. B-cell activation by armed helper T cells. Immunobiology: the immune system in health and disease, 5th ed. Garland Science, New York, NY, USA
28. Jaradat, Z.W. and Bhunia, A.K., 2003. Adhesion, invasion, and translocation characteristics of Listeria monocytogenes serotypes in Caco-2 cell and mouse models. Applied and Environmental Microbiology 69: 3640-3645
29. Jounai, K., Ikado, K., Sugimura, T., Ano, Y., Braun, J. and Fujiwara, D., 2012. Spherical lactic acid bacteria activate plasmacyotid dendritic cells immunomodulatory function via TLR9-dependent crosstalk with myeloid dendritic cells. PLoS ONE 7: e32588
30. Knudsen, G.M., Fromberg, A., Ng, Y. and Gram, L., 2016. Sublethal concentrations of antibiotics cause shift to anaerobic metabolism in Listeria monocytogenes and induce phenotypes linked to antibiotic tolerance. Frontiers in Microbiology 7: 1091
31. Lukic, J., Strahinic, I., Milenkovic, M., Golic, N., Kojic, M., Topisirovic, L. and Begovic, J., 2013. Interaction of Lactobacillus fermentum BGHI14 with rat colonic mucosa: implications for colitis induction. Applied and Environmental Microbiology 79: 5735-5744
32. Lukic, J., Strahinic, I., Milenkovic, M., Nikolic, M., Tolinacki, M., Kojic, M. and Begovic, J., 2014. Aggregation factor as an inhibitor of bacterial binding to gut mucosa. Microbial Ecology 68: 633-644
33. Luzina, I.G., Atamas, S.P., Storrer, C.E., daSilva, L.C., Kelsoe, G., Papadimitriou, J.C. and Handwerger, B.S., 2001. Spontaneous formation of germinal centers in autoimmune mice. Journal of Leukocyte Biology 70: 578-584
34. Mousavi, S.A., Fønhus, M.S. and Berg, T., 2009. Up-regulation of uPARAP/ENDO180 during culture activation of rat hepatic stellate cells and its presence in hepatic stellate cell lines from differnet species. BMC Cell Biology 10: 39
35. Ogawa, M., Yoshikawa, Y., Mimuro, H., Hain, T., Chakraborty, T. and Sasakawa, C., 2011. Autophagy targeting of Listeria monocytogenes and the bacterial countermeasure. Autophagy 7: 310-314
36. Oka, M., 2001. Helicobacter pylori and N-methyl-N'-nitro-Nnitrosoguanidine induction of dendritic cell infiltration of the pyloric mucosa of Mongolian gerbils. In: Asakura, H., Aoyagi, Y. and Nakazawa, S. (ed.) Trends in gastroenterology and hepatology. Springer, Tokyo, Japan, pp. 160-166
37. Oliveira, M.L., Arêas, A.P., Campos, I.B., Monedero, V., Perez-Martínez, G., Miyaji, E.N., Leite, L.C., Aires, K.A. and Lee Ho, P., 2006. Induction of systemic and mucosal immune response and decrease in Streptococcus pneumonia colonization by nasal inoculation of mice with recombinant lactic acid bacteria expressing pneumococcal surface antigen A. Microbes and Infection 8: 1016-1024
38. Ooi, S.T. and Lorber, B., 2005. Gastroenteritis due to Listeria monocytogenes. Clinical Infectious Diseases 40: 1327-1332
39. Pang, Q., Ji, Y., Li, Y., Bermúdez-Humařn, L.G., Hu, G. and Zeng, Y., 2008. Intragastric administration with recombinant Lactococcus lactis producing heme oxygenase-1 prevents lipopolysaccharideinduced endotoxemia in rats. FEMS Microbiology Letters 283: 62-68
40. Pedersen, N.C., Dean, G.A., Bernales, J., Sukura, A. and Higgins, J., 1998. Listeria monocytogenes and Serratia marcescens infections as models for Th1/Th2 immunity in laboratory cats. Veterinary Immunology and Immunopathology 63: 83-103
41. Peinnequin, A., Mouret, C., Birot, O., Alonso, A., Mathieu, J., Clarençon, D., Agay, D., Chancerelle, Y. and Multon, E., 2004. Rat pro-inflammatory cytokine and cytokine related mRNA quantification by real-time polymerase chain reaction using SYBR green. BMC Immunology 5: 3
42. Pfister, H., Remer, K.A., Brcic, M., Fatzer, R., Christen, S., Leib, S., Jungi, T.W., 2002. Inducible nitric oxide synthase and nitrotyrosine in listeric encephalitis: a cross-species study in ruminants. Veterinary Pathology 39: 190-199
43. Pron, B., Boumalia, C., Jaubert, F., Sarnacki, S., Monnet, J.P., Berche, P. and Gaillard, J.L., 1998. Comprehensive study of the intestinal stage of listeriosis in a rat ligated ileal loop system. Infection and Immunology 66: 747-755
44. Py, B.F., Lipinski, M.M. and Yuan, J., 2007. Autophagy limits Listeria monocytogenes intracellular growth in the early phase of primary infection. Autophagy 3: 117-125
45. Scopes, R. and Smith, J.A., 2010. Analysis of proteins. Current Protocols in Molecular Biology 90: 10.0.1-10.0.23
46. Sharifi, M., Erin, E., Mowers, E.E., Drake, L.E., Kay, F. and Macleod, K.F., 2015. Measuring autophagy in stressed cells. Methods in Molecular Biology 1292: 129-150
47. Shaughnessy, L. and Swanson, J.A., 2007. The role of the activated macrophage in clearing Listeria monocytogenes infection. Frontiers in Biosciences 12: 2683-2692
48. Shen, A. and Higgins, D.E., 2005. The 5' untranslated region-mediated enhancement of intracellular listeriolysin O production is required for Listeria monocytogenes pathogenicity. Molecular Microbiology 57: 1460-1473
49. Strahinic, I., Lukic, J., Terzic-Vidojevic, A., Lozo, J., Kojic, M. and Topisirovic, L., 2013. Use of Lactobacillus helveticus BGRA43 for manufacturing fermented milk products. Food Technology and Biotechnology 51: 257-265
50. Tilleux, S., Berger, J. and Hermans, E., 2007. Induction of astrogliosis by activated microglia is associated with a down-regulation of metabotropic glutamate receptor 5. Journal of Neuroimmunology 189: 23-30
51. Vabulas, R.M., Ahmad-Nejad, P., Ghose, S., Kirschning, C.J., Issels, R.D. and Wagner, H., 2002. HSP70 as endogenous stimulus of the Toll/interleukin-1 receptor signal pathway. Journal of Biological Chemistry 277: 15107-15112
52. Vanek, O., Nálezkova, M., Kavan, D., Borovicková, I., Pompach, P., Novák, P., Kumar, V., Vannucci, L., Hudecek, J., Hofbauerová, K., Kopecký, V. Jr., Brynda, J., Kolenko, P., Dohnálek, J., Kaderávek, P., Chmelík, J., Gorcík, L., Zídek, L., Sklenár, V., Bezouska, K., 2008. Soluble recombinant CD69 receptors optimized to have an exceptional physical and chemical stability display prolonged circulation and remain intact in the blood of mice. FEBS Journal 275: 5589-5606
53. Wang, X., Xu, H., Alvarez, X., Pahar, B., Moroney-Rasmussen, T., Lackner, A.A. and Veazey, R.S., 2011. Distinct expression patterns of CD69 in mucosal and systemic lymphoid tissues in primary SIV infection of rhesus macaques. PLoS ONE 6: e27207