Characterization of the protective immune response to Yersinia pseudotuberculosis infection in mice vaccinated with an LcrV-secreting strain of Lactococcus lactis

Vaccine

Volumn 34, Issue 47, 2016, Pages 5762-5767

  Daniel, Catherine ^a   Titecat, Marie ^a   Poiret, Sabine ^a   Cayet, Delphine ^a   Boutillier, Denise ^a   Simonet, Michel ^a   Sirard, Jean Claude ^a   Lemaître, Nadine ^a   Sebbane, Florent ^a  

^a UNIV LILLE   (France)

Author keywords

Lactococcus lactis; LcrV; Vaccination; Yersinia

Indexed keywords

BACTERIAL ANTIGEN; BACTERIAL VACCINE; CD4 ANTIGEN; CD8 ANTIGEN; INTERLEUKIN 2 RECEPTOR ALPHA; LOW CALCIUM RESPONSE V ANTIGEN; UNCLASSIFIED DRUG; LCRV PROTEIN, YERSINIA; PORE FORMING CYTOTOXIC PROTEIN; RECOMBINANT VACCINE;

ADOPTIVE TRANSFER; ANIMAL EXPERIMENT; ARTICLE; B LYMPHOCYTE; BACTERIAL COUNT; BACTERIAL STRAIN; BAGG ALBINO MOUSE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; DRUG RESPONSE; FEMALE; FLOW CYTOMETRY; FOLLOW UP; IMMUNE RESPONSE; IMMUNOHISTOCHEMISTRY; LACTOCOCCUS LACTIS; LIVER; LYMPHOID CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROCEDURES; SPLEEN; SURVIVAL RATE; VACCINATION; YERSINIA PSEUDOTUBERCULOSIS INFECTION; ACTIVE IMMUNIZATION; ANIMAL; BACTERIAL LOAD; GENETICS; HUMAN; IMMUNOLOGY; INTRANASAL DRUG ADMINISTRATION; INTRAVENOUS DRUG ADMINISTRATION; MICROBIOLOGY; NONPARAMETRIC TEST; PRIMARY CELL CULTURE; TIME FACTOR; YERSINIA PSEUDOTUBERCULOSIS;

ADMINISTRATION, INTRANASAL; ANIMALS; ANTIGENS, BACTERIAL; BACTERIAL LOAD; BACTERIAL VACCINES; CD4 ANTIGENS; CD8 ANTIGENS; FEMALE; HUMANS; IMMUNITY, ACTIVE; INJECTIONS, INTRAVENOUS; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; LACTOCOCCUS LACTIS; MICE; MICE, INBRED BALB C; PORE FORMING CYTOTOXIC PROTEINS; PRIMARY CELL CULTURE; SPLEEN; STATISTICS, NONPARAMETRIC; TIME FACTORS; VACCINATION; VACCINES, SYNTHETIC; YERSINIA PSEUDOTUBERCULOSIS; YERSINIA PSEUDOTUBERCULOSIS INFECTIONS;

EID: 84992554920     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2016.09.060     Document Type: Article

References (42)

1. [1] Callinan, R.B., Cook, R.W., Boulton, J.G., Fraser, G.C., Unger, D.B., Enterocolitis in cattle associated with Yersinia pseudotuberculosis infection. Aust Vet J 65 (1988), 8–11.
2. [2] Riet-Correa, F., Gil-Turnes, C., Reyes, J.C., Schild, A.L., Méndez, M.C., Yersinia pseudotuberculosis infection of buffaloes (Bubalus bubalis). J Vet Diagn Invest 2 (1990), 78–79.
3. [3] Sanford, S.E., Outbreaks of yersiniosis caused by Yersinia pseudotuberculosis in farmed cervids. J Vet Diagn Invest 7 (1995), 78–81.
4. [4] Slee, K.J., Skilbeck, N.W., Epidemiology of Yersinia pseudotuberculosis and Y. enterocolitica infections in sheep in Australia. J Clin Microbiol 30 (1992), 712–715.
5. [5] Baskin, G.B., Montali, R.J., Bush, M., Quan, T.J., Smith, E., Yersiniosis in captive exotic mammals. J Am Vet Med Assoc 171 (1977), 908–912.
6. [6] Kageruka, P., Mortelmans, J., Vercruysse, J., Beernaert-Declercq, C., Pseudotuberculosis in the Antwerp zoo. Acta Zool Pathol Antverp 66 (1976), 111–120.
7. [7] Bielli, M., Lauzi, S., Pratelli, A., Martini, M., Dall'Ara, P., Bonizzi, L., Pseudotuberculosis in marmosets, tamarins, and Goeldi's monkeys (Callithrichidae/Callimiconidae) housed at a European zoo. J Zoo Wildl Med 30 (1999), 532–536.
8. [8] Welsh, R.D., Ely, R.W., Holland, R.J., Epizootic of Yersinia pseudotuberculosis in a wildlife park. J Am Vet Med Assoc 201 (1992), 142–144.
9. [9] Gandolf, R., Weaver, G.V., Yersiniosis. Infectious diseases of concern to captive and free ranging wildlife in North America, 2nd ed., 2013, American Association of Zoo Veterinarians Infectious Disease Committee Manual.
10. [10] Quintard, B., Petit, T., Ruvoen, N., Carniel, E., Demeure, C.E., Efficacy of an oral vaccine for veterinary use against pseudotuberculosis. Comp Immunol Microbiol Infect Dis 33 (2010), e59–e65.
11. [11] Brubaker, R.R., Interleukin-10 and inhibition of innate immunity to yersiniae: roles of Yops and LcrV (V antigen). Infect Immun 71 (2003), 3673–3681.
12. [12] Cornelis, G.R., The type III secretion injectisome. Nat Rev Microbiol 4 (2006), 811–825.
13. [13] Mueller, C.A., Broz, P., Cornelis, G.R., The type III secretion system tip complex and translocon. Mol Microbiol 68 (2006), 1085–1095.
14. [14] Williamson, E.D., Oyston, P.C., Protecting against plague: towards a next-generation vaccine. Clin Exp Immunol 172 (2013), 1–8.
15. [15] Lavelle, E.C., O'Hagan, D.T., Delivery systems and adjuvants for oral vaccines. Expert Opin Drug Deliv 3 (2006), 747–762.
16. [16] Neutra, M.R., Kozlowski, P.A., Mucosal vaccines: the promise and the challenge. Nat Rev Immunol 6 (2006), 148–158.
17. [17] Daniel, C., Roussel, Y., Kleerebezem, M., Pot, B., Recombinant lactic acid bacteria as mucosal biotherapeutic agents. Trends Biotechnol 29 (2011), 499–508.
18. [18] Daniel, C., Sebbane, F., Poiret, S., Goudercourt, D., Dewulf, Mullet, C., et al. Protection against Yersinia pseudotuberculosis infection conferred by a Lactococcus lactis mucosal delivery vector secreting LcrV. Vaccine 27 (2009), 1141–1144.
19. [19] Sirard, J.C., Fayolle, C., de Chastellier, C., Mock, M., Leclerc, C., Berche, P., Intracytoplasmic delivery of listeriolysin O by a vaccinal strain of Bacillus anthracis induces CD8-mediated protection against Listeria monocytogenes. J Immunol 159 (1997), 4435–4443.
20. [20] Foligné, B., Zoumpopoulou, G., Dewulf, J., Ben Younes, A., Chareyre, F., Sirard, J.C., et al. A key role of dendritic cells in probiotic functionality. PLoS One, 2, 2007, e313.
21. [21] van Furth, R., Diesselhoff-den Dulk, M.M., Dual origin of mouse spleen macrophages. J Exp Med 160 (1984), 1273–1283.
22. [22] Li, P.Z., Li, J.Z., Li, M., Gong, J.P., He, K., An efficient method to isolate and culture mouse Kupffer cells. Immunol Lett 158 (2014), 52–56.
23. [23] Titus, J.A., Finkelman, F.D., Stephany, D.A., Jones, J.F., Segal, D.M., Quantitative analysis of Fc gamma receptors on murine spleen cell populations by using dual parameter flow cytometry. J Immunol 133 (1984), 556–561.
24. [24] Gregory, S.H., Wing, E.J., Neutrophil-Kupffer cell interaction: a critical component host defenses to systemic bacterial infections. J Leukoc Biol 72 (2002), 239–248.
25. [25] Rosenheinrich, M., Heine, W., Schmühl, C.M., Pisano, F., Dersch, P., Natural Killer cells mediate protection against Yersinia pseudotuberculosis in the mesenteric lymph nodes. PLoS One, 10, 2015, e0136290.
26. [26] Zhang, Y., Mena, P., Romanov, G., Lin, J.S., Smiley, S.T., Bliska, J.B., A protective epitope in type III effector YopE is a major CD8 T cell antigen during primary infection with Yersinia pseudotuberculosis. Infect Immun 80 (2012), 206–214.
27. + T cells restrict Yersinia pseudotuberculosis infection: bypass of anti-phagocytosis by targeting antigen-presenting cells. PLoS Pathog, 5, 2009, e1000573.
28. + T cells are generated in response to an immunodominant epitope in type III effector YopE during primary Yersinia pseudotuberculosis infection. Infect Immun 82 (2014), 3033–3044.
29. [29] Parent, M.A., Berggren, K.N., Mullarky, I.K., Szaba, F.M., Kummer, L.W., Adamovicz, J.J., et al. Yersinia pestis V protein epitopes recognized by CD4 T cells. Infect Immun 73 (2005), 2197–2204.
30. + T cell-mediated immune responses in LcrV DNA vaccine induced protection against Yersinia pestis challenge. Vaccine 29 (2011), 6802–6809.
31. + T-cell expression and IFN-, perforin secretion for B-T constructs of F1 and V antigens of Yersinia pestis. Int Immunopharmacol 12 (2012), 64–73.
32. [32] Ramirez, K., Ditamo, Y., Rodriguez, L., Picking, W.L., van Roosmalen, M.L., Leenhouts, K., et al. Neonatal mucosal immunization with a non-living, non-genetically modified Lactococcus lactis vaccine carrier induces systemic and local Th1-type immunity and protects against bacterial infection. Mucosal Immunol 3 (2010), 159–171.
33. [33] Shreewastav, R.K., Ali, R., Uppada, J.B., Rao, D.N., Cell-mediated immune response to epitopic MAP (multiple antigen peptide) construct of LcrV antigen of Yersinia pestis in murine model. Cell Immunol 278 (2012), 55–62.
34. [34] Derewenda, U., Mateja, A., Devedjiev, Y., Routzahn, K.M., Evdokimov, A.G., Derewenda, Z.S., et al. The structure of Yersinia pestis V-antigen, an essential virulence factor and mediator of immunity against plague. Structure 12 (2004), 301–306.
35. [35] Schmidt, A., Schaffelhofer, S., Müller, K., Röllinghoff, M., Beusher, H.U., Analysis of the Yersinia enterocolitica 0:8 V antigen for cross protectivity. Microb Pathog 26 (1999), 221–233.
36. [36] Roggenkamp, A., Geiger, A.M., Leitritz, L., Kessler, A., Heesemann, J., Passive immunity to infection with Yersinia spp. mediated by anti-recombinant V antigen is dependent on polymorphism of V antigen. Infect Immun 65 (1997), 446–451.
37. [37] Motin, V.L., Nakajima, R., Smirnov, G.B., Brubaker, R.R., Passive immunity to yersiniae mediated by anti-recombinant V antigen and protein A-V antigen fusion peptide. Infect Immun 62 (1994), 4192–4201.
38. [38] Liu, W.T., Hsu, H.L., Liang, C.C., Chuang, C.C., Lin, H.C., Liu, Y.T., A comparison of immunogenicity and protective immunity against experimental plague by intranasal and/or combined with oral immunization of mice with attenuated Salmonella serovar Typhimurium expressing secreted Yersinia pestis F1 and V antigen. FEMS Immunol Med Microbiol 51 (2007), 58–69.
39. [39] Chamcha, V., Jones, A., Quigley, B.R., Scott, J.R., Amara, R.R., Oral immunization with a recombinant Lactococcus lactis-expressing HIV-1 antigen on group A Streptococcus pilus induces strong mucosal immunity in the gut. J Immunol 195 (2015), 5025–5034.
40. + T cells against Listeria monocytogenes in the murine infection model. Vaccine 26 (2008), 5304–5314.
41. [41] Lee, P., Abdul-Wahid, A., Faubert, G.M., Comparison of the local immune response against Giardia lamblia cyst wall protein 2 induced by recombinant Lactococcus lactis and Streptococcus gordonii. Microbes Infect 11 (2009), 20–28.
42. [42] Hugentobler, F., Yam, K.K., Gillard, J., Mahbuba, R., Olivier, M., Cousineau, B., Immunization against Leishmania major infection using LACK-and IL-12-expressing Lactococcus lactis induces delay in footpad swelling. PLoS One, 7, 2012, e30945.