Immunization with r-Lactococcus lactis expressing outer membrane protein A of Shigella dysenteriae type-1: evaluation of oral and intranasal route of administration

Journal of Applied Microbiology

Volumn 122, Issue 2, 2017, Pages 493-505

  Yagnik, B ^a,b   Sharma, D ^a,b   Padh, H ^b   Desai, P ^a  

^a B V PATEL PHARMACEUTICAL EDUCATION AND RESEARCH DEVELOPMENT PERD CENTRE   (India)

^b SARDAR PATEL UNIVERSITY   (India)

Author keywords

Lactococcus lactis; mucosal immunization; oral route; outer membrane protein A; Shigella

Indexed keywords

ANTIBODIES; BIOLOGICAL MEMBRANES; CHEMICAL DETECTION; CLONING; ENZYMES; ESCHERICHIA COLI; IMMUNE SYSTEM; IMMUNIZATION; MAMMALS;

BALB/C MICE; ENZYME LINKED IMMUNOSORBENT ASSAY; FOOD GRADE; INTRANASAL; LACTOCOCCUS LACTIS; MUCOSAL IMMUNIZATION; ORAL ROUTE; OUTER MEMBRANE PROTEIN A; RESTRICTION ENZYMES; SHIGELLA;

AFFINITY CHROMATOGRAPHY;

IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; OUTER MEMBRANE PROTEIN A; EPITOPE; OMPA OUTER MEMBRANE PROTEINS; OUTER MEMBRANE PROTEIN; RECOMBINANT PROTEIN; SHIGELLA VACCINE;

ANTIBODY; BACTERIUM; BIOASSAY; ENZYME; ENZYME ACTIVITY; GENE EXPRESSION; IMMUNE RESPONSE; IMMUNIZATION; PROTEIN; RODENT; SERUM; VACCINE;

ANIMAL EXPERIMENT; ANTIBODY DETECTION; ARTICLE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; ESCHERICHIA COLI; FECES ANALYSIS; FEMALE; IMMOBILIZED METAL AFFINITY CHROMATOGRAPHY; IMMUNIZATION; IMMUNOBLOTTING; IMMUNOGENICITY; IMMUNOGLOBULIN BLOOD LEVEL; LACTOCOCCUS LACTIS; MOLECULAR CLONING; MOUSE; NONHUMAN; PROTEIN PURIFICATION; RECOMBINANT GENE; SHIGELLA DYSENTERIAE; ANIMAL; BAGG ALBINO MOUSE; BLOOD; CHEMISTRY; GENETICS; GERMFREE ANIMAL; IMMUNOLOGY; INTRANASAL DRUG ADMINISTRATION; MUCOSAL IMMUNITY; ORAL DRUG ADMINISTRATION;

ESCHERICHIA COLI; LACTOCOCCUS LACTIS; MUS; SHIGELLA; SHIGELLA DYSENTERIAE;

ADMINISTRATION, INTRANASAL; ADMINISTRATION, ORAL; ANIMALS; BACTERIAL OUTER MEMBRANE PROTEINS; EPITOPES; FEMALE; IMMUNITY, MUCOSAL; IMMUNOGLOBULIN G; LACTOCOCCUS LACTIS; MICE; MICE, INBRED BALB C; RECOMBINANT PROTEINS; SHIGELLA DYSENTERIAE; SHIGELLA VACCINES; SPECIFIC PATHOGEN-FREE ORGANISMS;

EID: 85007415289     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/jam.13353     Document Type: Article

References (43)

1. Ahmed, B., Loos, M., Vanrompay, D. and Cox, E. (2014) Oral immunization with Lactococcus lactis-expressing EspB induces protective immune responses against Escherichia coli O157: H7 in a murine model of colonization. Vaccine 32, 3909–3916.
2. Ambrosi, C., Pompili, M., Scribano, D., Zagaglia, C., Ripa, S. and Nicoletti, M. (2012) Outer membrane protein A (OmpA): a new player in Shigella flexneri protrusion formation and inter-cellular spreading. PLoS ONE 7, e49625.
3. Asensi, G.F., de Sales, N.F.F., Dutra, F.F., Feijó, D.F., Bozza, M.T., Ulrich, R.G. and Le Loir, Y. (2013) Oral immunization with Lactococcus lactis secreting attenuated recombinant staphylococcal enterotoxin B induces a protective immune response in a murine model. Microb Cell Fact 12, 1.
4. Audouy, S.A., van Selm, S., van Roosmalen, M.L., Post, E., Kanninga, R., Neef, J., Estevao, S., Nieuwenhuis, E.E. et al. (2007) Development of lactococcal GEM-based pneumococcal vaccines. Vaccine 25, 2497–2506.
5. Bahey-El-Din, M., Casey, P.G., Griffin, B.T. and Gahan, C.G. (2008) Lactococcus lactis-expressing listeriolysin O (LLO) provides protection and specific CD8 + T cells against Listeria monocytogenes in the murine infection model. Vaccine 26, 5304–5314.
6. Bermúdez-Humarán, L.G., Langella, P., Commissaire, J., Gilbert, S., Le Loir, Y., L'Haridon, R. and Corthier, G. (2003) Controlled intra-or extracellular production of staphylococcal nuclease and ovine omega interferon in Lactococcus lactis. FEMS Microbiol Lett 224, 307–313.
7. Bermúdez-Humarán, L.G., Kharrat, P., Chatel, J.M. and Langella, P. (2011) Lactococci and lactobacilli as mucosal delivery vectors for therapeutic proteins and DNA vaccines. Microb Cell Fact 10, 1.
8. Bhattacharya, D., Sugunan, A.P., Bhattacharjee, H., Thamizhmani, R., Sayi, D.S., Thanasekaran, K. and Roy, S. (2012) Antimicrobial resistance in Shigella-rapid increase and widening of spectrum in Andaman Islands, India. Indian J Med Res 135, 365.
9. Biswas, A., Banerjee, P. and Biswas, T. (2009) Porin of Shigella dysenteriae directly promotes toll-like receptor 2-mediated CD4 + T cell survival and effector function. Mol Immunol 46, 3076–3085.
10. Blutt, S.E., Miller, A.D., Salmon, S.L., Metzger, D.W. and Conner, M.E. (2012) IgA is important for clearance and critical for protection from rotavirus infection. Mucosal Immunol 5, 712–719.
11. Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72, 248–254.
12. Cervantes-Barragán, L., Gil-Cruz, C., Pastelin-Palacios, R., Lang, K.S., Isibasi, A., Ludewig, B. and López-Macías, C. (2009) TLR2 and TLR4 signaling shapes specific antibody responses to Salmonella typhi antigens. Eur J Immunol 39, 126–135.
13. Choi, C.H., Lee, J.S., Lee, Y.C., Park, T.I. and Lee, J.C. (2008) Acinetobacter baumannii invades epithelial cells and outer membrane protein A mediates interactions with epithelial cells. BMC Microbiol 8, 216.
14. Confer, A.W. and Ayalew, S. (2013) The OmpA family of proteins: roles in bacterial pathogenesis and immunity. Vet Microbial 163, 207–222.
15. Cortes-Perez, N.G., Lefèvre, F., Corthier, G., Adel-Patient, K., Langella, P. and Bermúdez-Humarán, L.G. (2007) Influence of the route of immunization and the nature of the bacterial vector on immunogenicity of mucosal vaccines based on lactic acid bacteria. Vaccine 25, 6581–6588.
16. De Ruyter, P.G., Kuipers, O.P. and De Vos, W.M. (1996) Controlled gene expression systems for Lactococcus lactis with the food-grade inducer nisin. Appl Environ Microbiol 62, 3662–3667.
17. Delcour, A.H. (2002) Structure and function of pore-forming b-barrels from bacteria. J Mol Microbiol Biotechnol 4, 1–10.
18. Frees, D. and Ingmer, H. (1999) ClpP participates in the degradation of misfolded protein in Lactococcus lactis. Mol Microbiol 31, 79–87.
19. González, C.R., Isibasi, A., Ortiz-Navarrete, V., Paniagua, J., García, J.A., Blanco, F. and Kumate, J. (1993) Lymphocytic proliferative response to outer-membrane proteins isolated from Salmonella. Microbiol Immunol 37, 793–799.
20. Heine, S.J., Franco-Mahecha, O.L., Chen, X., Choudhari, S., Blackwelder, W.C., van Roosmalen, M.L., Leenhouts, K., Picking, W.L. et al. (2015) Shigella IpaB and IpaD displayed on L. lactis bacterium-like particles induce protective immunity in adult and infant mice. Immunol Cell Biol 93, 641–652.
21. Hongying, F., Xianbo, W., Fang, Y., Yang, B. and Beiguo, L. (2014) Oral immunization with recombinant Lactobacillus acidophilus expressing the adhesin Hp0410 of Helicobacter pylori induces mucosal and systemic immune responses. Clin Vaccine Immunol 21, 126–132.
22. Jeannin, P., Magistrelli, G., Goetsch, L., Haeuw, J.F., Thieblemont, N., Bonnefoy, J.Y. and Delneste, Y. (2002) Outer membrane protein A (OmpA): a new pathogen-associated molecular pattern that interacts with antigen presenting cells—impact on vaccine strategies. Vaccine 20, A23–A27.
23. Kotloff, K.L., Winickoff, J.P., Ivanoff, B., Clemens, J.D., Swerdlow, D.L., Sansonetti, P.J. and Levine, M.M. (1999) Global burden of Shigella infections: implications for vaccine development and implementation of control strategies. Bull World Health Organ 77, 651–666.
24. Marreddy, R.K., Pinto, J.P., Wolters, J.C., Geertsma, E.R., Fusetti, F., Permentier, H.P. and Poolman, B. (2011) The response of Lactococcus lactis to membrane protein production. PLoS ONE 6, e24060.
25. Medina, M., Villena, J., Vintiñi, E., Hebert, E.M., Raya, R. and Alvarez, S. (2008) Nasal immunization with Lactococcus lactis expressing the pneumococcal protective protein A induces protective immunity in mice. Infect Immun 76, 2696–2705.
26. Mittal, R., Krishnan, S., Gonzalez-Gomez, I. and Prasadarao, N.V. (2011) Deciphering the roles of outer membrane protein A extracellular loops in the pathogenesis of Escherichia coli K1 meningitis. J Biol Chem 286, 2183–2193.
27. Nair, M.K.M. and Venkitanarayanan, K. (2007) Role of bacterial OmpA and host cytoskeleton in the invasion of human intestinal epithelial cells by Enterobacter sakazakii. Pediatr Res 62, 664–669.
28. Nouaille, S., Ribeiro, L.A., Miyoshi, A., Pontes, D., Le Loir, Y., Oliveira, S.C. and Azevedo, V. (2003) Heterologous protein production and delivery systems for Lactococcus lactis. Genet Mol Res 2, 102–111.
29. Perdigon, G., Vintini, E., Alvarez, S., Medina, M. and Medici, M. (1999) Study of the possible mechanisms involved in the mucosal immune system activation by lactic acid bacteria. J Dairy Sci 82, 1108–1114.
30. Perez, C.A., Eichwald, C., Burrone, O. and Mendoza, D. (2005) Rotavirus vp7 antigen produced by Lactococcus lactis induces neutralizing antibodies in mice. J Appl Microbiol 99, 1158–1164.
31. Pore, D. and Chakrabarti, M.K. (2013) Outer membrane protein A (OmpA) from Shigella flexneri 2a: a promising subunit vaccine candidate. Vaccine 31, 3644–3650.
32. Pore, D., Mahata, N., Pal, A. and Chakrabarti, M.K. (2011) Outer membrane protein A (OmpA) of Shigella flexneri 2a, induces protective immune response in a mouse model. PLoS ONE 6, e22663.
33. Pore, D., Mahata, N. and Chakrabarti, M.K. (2012) Outer membrane protein A (OmpA) of Shigella flexneri 2a links innate and adaptive immunity in a TLR2-dependent manner and involvement of IL-12 and nitric oxide. ‎J. Biol Chem 287, 12589–12601.
34. Ribeiro, L.A., Azevedo, V., Le Loir, Y., Oliveira, S.C., Dieye, Y., Piard, J.C., Gruss, A. and Langella, P. (2002) Production and targeting of the Brucella abortus antigen L7/L12 in Lactococcus lactis: a first step towards food-grade live vaccines against brucellosis. Appl Environ Microbiol 68, 910–916.
35. Seegers, J.F. (2002) Lactobacilli as live vaccine delivery vectors: progress and prospects. Trends Biotechnol 20, 508–515.
36. Sharma, D., Patel, S., Padh, H. and Desai, P. (2016a) Immunoinformatic identification of potential epitopes against Shigellosis. Int J Pept Res 22, 481–495.
37. Sharma, D., Yagnik, B., Baksi, R., Desai, N., Padh, H. and Desai, P. (2016b) Shigellosis murine model established by intraperitoneal and intranasal route of administration: a comparative comprehension overview. Microbes Infect. doi:10.1016/j.micinf.2016.09.002.
38. Smith, S.G., Mahon, V., Lambert, M.A. and Fagan, R.P. (2007) A molecular Swiss army knife: OmpA structure, function and expression. FEMS Microbiol Lett 273, 1–11.
39. Torres, A.G. (2004) Current aspects of Shigella pathogenesis. Rev Latinoam Microbiol 46, 89–97.
40. Waeytens, A., Ferdinande, L., Neirynck, S., Rottiers, P., De Vos, M., Steidler, L. and Cuvelier, C.A. (2008) Paracellular entry of interleukin-10 producing Lactococcus lactis in inflamed intestinal mucosa in mice. Inflamm Bowel Dis 14, 471–479.
41. Yagnik, B., Patel, S., Dave, M., Sharma, D., Padh, H. and Desai, P. (2016a) Factors affecting inducible expression of outer membrane protein A (OmpA) of Shigella dysenteriae type-1 in Lactococcus lactis using nisin inducible controlled expression (NICE). Indian J Microbiol 56, 80–87.
42. Yagnik, B., Padh, H. and Desai, P. (2016b) Construction of a new shuttle vector for DNA delivery into mammalian cells using non-invasive Lactococcus lactis. Microbes Infect 18, 237–244.
43. Yung-Hung, R.L., Ismail, A., Lim, T.S. and Choong, Y.S. (2011) A 35 kDa antigenic protein from Shigella flexneri: in silico structural and functional studies. Biochem Biophys Res Commun 415, 229–234.