Immune response to Lactobacillus plantarum expressing Borrelia burgdorferi OspA is modulated by the lipid modification of the antigen

PLoS ONE

Volumn 5, Issue 6, 2010, Pages

  del Rio, Beatriz ^a   Seegers, Jos F M L ^b   Gomes Solecki, Maria ^a,c  

^a UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^b Lactrys Biopharmaceuticals BV   (Netherlands)

^c Biopeptides Corp   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ANTIGEN; BACTERIAL VACCINE; CYTOKINE; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2A; LIPID; OUTER SURFACE PROTEIN A; SIGNAL PEPTIDE; BACTERIUM ANTIBODY; INTERLEUKIN 8; LIPOPROTEIN; MEMBRANE ANTIGEN; OUTER MEMBRANE PROTEIN; RECOMBINANT PROTEIN;

ANIMAL EXPERIMENT; ANTIGEN EXPRESSION; ARTICLE; BACTERIAL MEMBRANE; BORRELIA BURGDORFERI; CELL STIMULATION; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOLOGICAL TOLERANCE; IMMUNOMODULATION; INTESTINE EPITHELIUM CELL; LACTIC ACID BACTERIUM; LACTOBACILLUS PLANTARUM; MOUSE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PROTEIN LOCALIZATION; PROTEIN TARGETING; PROTEIN TRANSPORT; TH1 CELL; TH2 CELL; BIOSYNTHESIS; CELL CULTURE; CHEMISTRY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLUORESCENCE MICROSCOPY; GENETICS; IMMUNOLOGY; METABOLISM;

BORRELIA BURGDORFERI; LACTOBACILLUS PLANTARUM;

ANTIBODIES, BACTERIAL; ANTIGENS, BACTERIAL; ANTIGENS, SURFACE; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL VACCINES; BORRELIA BURGDORFERI; CELLS, CULTURED; ENZYME-LINKED IMMUNOSORBENT ASSAY; HUMANS; INTERLEUKIN-8; LACTOBACILLUS PLANTARUM; LIPIDS; LIPOPROTEINS; MICROSCOPY, FLUORESCENCE; RECOMBINANT PROTEINS;

EID: 77955285114     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0011199     Document Type: Article

References (49)

1. Wells JM, Mercenier A (2008) Mucosal delivery of therapeutic and prophylactic molecules using lactic acid bacteria. Nat Rev Microbiol 6: 349-362.
2. Anderson R, Dougan G, Roberts M (1996) Delivery of the Pertactin/P.69 polypeptide of Bordetella pertussis using an attenuated Salmonella typhimurium vaccine strain: expression levels and immune response. Vaccine 14: 1384-1390.
3. Ascon MA, Hone DM, Walters N, Pascual DW (1998) Oral immunization with a Salmonella typhimurium vaccine vector expressing recombinant enterotoxigenic Escherichia coli K99 fimbriae elicits elevated antibody titers for protective immunity. Infect Immun 66: 5470-5476.
4. Kohler JJ, Pathangey L, Hasona A, Progulske-Fox A, Brown TA (2000) Longterm immunological memory induced by recombinant oral Salmonella vaccine vectors. Infect Immun 68: 4370-4373.
5. Peters C, Peng X, Douven D, Pan ZK, Paterson Y (2003) The induction of HIV Gag-specific CD8+ T cells in the spleen and gut-associated lymphoid tissue by parenteral or mucosal immunization with recombinant Listeria monocytogenes HIV Gag. J Immunol 170: 5176-5187.
6. Shata MT, Reitz MS, Jr., DeVico AL, Lewis GK, Hone DM (2001) Mucosal and systemic HIV-1 Env-specific CD8(+) T-cells develop after intragastric vaccination with a Salmonella Env DNA vaccine vector. Vaccine 20: 623-629.
7. Lee JS, Poo H, Han DP, Hong SP, Kim K, et al. (2006) Mucosal immunization with surface-displayed severe acute respiratory syndrome coronavirus spike protein on Lactobacillus casei induces neutralizing antibodies in mice. J Virol 80: 4079-4087.
8. Wu CM, Chung TC (2007) Mice protected by oral immunization with Lactobacillus reuteri secreting fusion protein of Escherichia coli enterotoxin subunit protein. FEMS Immunol Med Microbiol 50: 354-365.
9. Kajikawa A, Satoh E, Leer RJ, Yamamoto S, Igimi S (2007) Intragastric immunization with recombinant Lactobacillus casei expressing flagellar antigen confers antibody-independent protective immunity against Salmonella enterica serovar Enteritidis. Vaccine 25: 3599-3605.
10. Li YG, Tian FL, Gao FS, Tang XS, Xia C (2007) Immune responses generated by Lactobacillus as a carrier in DNA immunization against foot-and-mouth disease virus. Vaccine 25: 902-911.
11. Daniel C, Sebbane F, Poiret S, Goudercourt D, Dewulf J, et al. (2009) Protection against Yersinia pseudotuberculosis infection conferred by a Lactococcus lactis mucosal delivery vector secreting LcrV. Vaccine 27: 1141-1144.
12. del Rio B, Dattwyler RJ, Aroso M, Neves V, Meirelles L, et al. (2008) Oral immunization with recombinant lactobacillus plantarum induces a protective immune response in mice with Lyme disease. Clin Vaccine Immunol 15: 1429-1435.
13. Perdigon G, Alvarez S, Pesce de Ruiz Holgado A (1991) Immunoadjuvant activity of oral Lactobacillus casei: influence of dose on the secretory immune response and protective capacity in intestinal infections. J Dairy Res 58: 485-496.
14. Link-Amster H, Rochat F, Saudan KY, Mignot O, Aeschlimann JM (1994) Modulation of a specific humoral immune response and changes in intestinal flora mediated through fermented milk intake. FEMS Immunol Med Microbiol 10: 55-63.
15. Pouwels PH, Leer RJ, Boersma WJ (1996) The potential of Lactobacillus as a carrier for oral immunization: development and preliminary characterization of vector systems for targeted delivery of antigens. J Biotechnol 44: 183-192.
16. Maassen CB, Laman JD, den Bak-Glashouwer MJ, Tielen FJ, van Holten- Neelen JC, et al. (1999) Instruments for oral disease-intervention strategies: recombinant Lactobacillus casei expressing tetanus toxin fragment C for vaccination or myelin proteins for oral tolerance induction in multiple sclerosis. Vaccine 17: 2117-2128.
17. Bermudez-Humaran LG, Langella P, Commissaire J, Gilbert S, le Loir Y, et al. (2003) Controlled intra- or extracellular production of staphylococcal nuclease and ovine omega interferon in Lactococcus lactis. FEMS Microbiol Lett 224: 307-313.
18. Dieye Y, Hoekman AJ, Clier F, Juillard V, Boot HJ, et al. (2003) Ability of Lactococcus lactis to export viral capsid antigens: a crucial step for development of live vaccines. Appl Environ Microbiol 69: 7281-7288.
19. Navarre WW, Schneewind O (1999) Surface proteins of gram-positive bacteria and mechanisms of their targeting to the cell wall envelope. Microbiol Mol Biol Rev 63: 174-229.
20. Weis JJ, Ma Y, Erdile LF (1994) Biological activities of native and recombinant Borrelia burgdorferi outer surface protein A: dependence on lipid modification. Infect Immun 62: 4632-4636.
21. Sellati TJ, Bouis DA, Kitchens RL, Darveau RP, Pugin J, et al. (1998) Treponema pallidum and Borrelia burgdorferi lipoproteins and synthetic lipopeptides activate monocytic cells via a CD14-dependent pathway distinct from that used by lipopolysaccharide. J Immunol 160: 5455-5464.
22. Mowat AM, Viney JL (1997) The anatomical basis of intestinal immunity. Immunol Rev 156: 145-166.
23. Mowat AM (2003) Anatomical basis of tolerance and immunity to intestinal antigens. Nat Rev Immunol 3: 331-341.
24. Radolf JD, Chamberlain NR, Clausell A, Norgard MV (1988) Identification and localization of integral membrane proteins of virulent Treponema pallidum subsp. pallidum by phase partitioning with the nonionic detergent triton X-114. Infect Immun 56: 490-498.
25. Gomes-Solecki MJ, Brisson DR, Dattwyler RJ (2006) Oral vaccine that breaks the transmission cycle of the Lyme disease spirochete can be delivered via bait. Vaccine 24: 4440-4449.
26. Bermudez-Humaran LG, Cortes-Perez NG, Lefevre F, Guimaraes V, Rabot S, et al. (2005) A novel mucosal vaccine based on live Lactococci expressing E7 antigen and IL-12 induces systemic and mucosal immune responses and protects mice against human papillomavirus type 16-induced tumors. J Immunol 175: 7297-7302.
27. Cho HJ, Shin HJ, Han IK, Jung WW, Kim YB, et al. (2007) Induction of mucosal and systemic immune responses following oral immunization of mice with Lactococcus lactis expressing human papillomavirus type 16 L1. Vaccine 25: 8049-8057.
28. Scavone P, Miyoshi A, Rial A, Chabalgoity A, Langella P, et al. (2007) Intranasal immunisation with recombinant Lactococcus lactis displaying either anchored or secreted forms of Proteus mirabilis MrpA fimbrial protein confers specific immune response and induces a significant reduction of kidney bacterial colonisation in mice. Microbes Infect 9: 821-828.
29. Moorthy G, Ramasamy R (2007) Mucosal immunisation of mice with malaria protein on lactic acid bacterial cell walls. Vaccine 25: 3636-3645.
30. Medina M, Villena J, Vintini E, Hebert EM, Raya R, et al. (2008) Nasal immunization with Lactococcus lactis expressing the pneumococcal protective protein A induces protective immunity in mice. Infect Immun 76: 2696-2705.
31. Sim AC, Lin W, Tan GK, Sim MS, Chow VT, et al. (2008) Induction of neutralizing antibodies against dengue virus type 2 upon mucosal administration of a recombinant Lactococcus lactis strain expressing envelope domain III antigen. Vaccine 26: 1145-1154.
32. Yigang XU, Yijing LI (2008) Construction of recombinant Lactobacillus casei efficiently surface displayed and secreted porcine parvovirus VP2 protein and comparison of the immune responses induced by oral immunization. Immunology 124: 68-75.
33. Gu Q, Song D, Zhu M (2009) Oral vaccination of mice against Helicobacter pylori with recombinant Lactococcus lactis expressing urease subunit B. FEMS Immunol Med Microbiol 56: 197-203.
34. Mohamadzadeh M, Duong T, Sandwick SJ, Hoover T, Klaenhammer TR (2009) Dendritic cell targeting of Bacillus anthracis protective antigen expressed by Lactobacillus acidophilus protects mice from lethal challenge. Proc Natl Acad Sci USA 106: 4331-4336.
35. Erdile LF, Brandt MA, Warakomski DJ, Westrack GJ, Sadziene A, et al. (1993) Role of attached lipid in immunogenicity of Borrelia burgdorferi OspA. Infect Immun 61: 81-90.
36. Venema R, Tjalsma H, van Dijl JM, de Jong A, Leenhouts K, et al. (2003) Active lipoprotein precursors in the Gram-positive eubacterium Lactococcus lactis. J Biol Chem 278: 14739-14746.
37. Sansonetti PJ (2004) War and peace at mucosal surfaces. Nat Rev Immunol 4: 953-964.
38. Hamilton-Miller JM (2003) The role of probiotics in the treatment and prevention of Helicobacter pylori infection. Int J Antimicrob Agents 22: 360-366.
39. Skjolaas KA, Burkey TE, Dritz SS, Minton JE (2007) Effects of Salmonella enterica serovar Typhimurium, or serovar Choleraesuis, Lactobacillus reuteri and Bacillus licheniformis on chemokine and cytokine expression in the swine jejunal epithelial cell line, IPEC-J2. Vet Immunol Immunopathol 115: 299-308.
40. Spear GT, Zariffard MR, Cohen MH, Sha BE (2008) Vaginal IL-8 levels are positively associated with Candida albicans and inversely with lactobacilli in HIV-infected women. J Reprod Immunol 78: 76-79.
41. Khoo UY, Proctor IE, Macpherson AJ (1997) CD4+ T cell down-regulation in human intestinal mucosa: evidence for intestinal tolerance to luminal bacterial antigens. J Immunol 158: 3626-3634.
42. Rescigno M, Rotta G, Valzasina B, Ricciardi-Castagnoli P (2001) Dendritic cells shuttle microbes across gut epithelial monolayers. Immunobiology 204: 572-581.
43. Macpherson AJ, Harris NL (2004) Interactions between commensal intestinal bacteria and the immune system. Nat Rev Immunol 4: 478-485.
44. Gahery-Segard H, Pialoux G, Charmeteau B, Sermet S, Poncelet H, et al. (2000) Multiepitopic B- and T-cell responses induced in humans by a human immunodeficiency virus type 1 lipopeptide vaccine. J Virol 74: 1694-1703.
45. De BK, Sampson JS, Ades EW, Huebner RC, Jue DL, et al. (2000) Purification and characterization of Streptococcus pneumoniae palmitoylated pneumococcal surface adhesin A expressed in Escherichia coli. Vaccine 18: 1811-1821.
46. Hirschfeld M, Kirschning CJ, Schwandner R, Wesche H, Weis JH, et al. (1999) Cutting edge: inflammatory signaling by Borrelia burgdorferi lipoproteins is mediated by toll-like receptor 2. J Immunol 163: 2382-2386.
47. Wooten RM, Ma Y, Yoder RA, Brown JP, Weis JH, et al. (2002) Toll-like receptor 2 is required for innate, but not acquired, host defense to Borrelia burgdorferi. J Immunol 168: 348-355.
48. Mestecky J, Russell MW, Elson CO (2007) Perspectives on mucosal vaccines: is mucosal tolerance a barrier? J Immunol 179: 5633-5638.
49. Roy CR, Mocarski ES (2007) Pathogen subversion of cell-intrinsic innate immunity. Nat Immunol 8: 1179-1187.