Lactococcus lactis as a live vector: Heterologous protein production and DNA delivery systems

Protein Expression and Purification

Volumn 79, Issue 2, 2011, Pages 165-175

  Pontes, Daniela Santos ^a   De Azevedo, Marcela Santiago Pacheco ^a   Chatel, Jean Marc ^b   Langella, Philippe ^b   Azevedo, Vasco ^a   Miyoshi, Anderson ^a  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^b UMR1319 MICALIS   (France)

Author keywords

Delivery systems; Heterologous expression; Lactic acid bacteria; Lactococcus lactis; Vaccines

Indexed keywords

BACTERIAL PROTEIN; BACTERIAL VACCINE; DNA; DNA VACCINE;

ANIMAL; BACTERIAL INFECTION; CELL WALL; CHEMISTRY; CYTOSOL; DRUG DELIVERY SYSTEM; EXTRACELLULAR SPACE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE VECTOR; GENETICS; HUMAN; IMMUNIZATION; IMMUNOLOGY; LACTOCOCCUS LACTIS; METABOLISM; METHODOLOGY; MICROBIOLOGY; MOUSE; MUCOSA; MUCOSAL IMMUNITY; PROTEIN ENGINEERING; REVIEW; VIROLOGY; VIRUS INFECTION;

ANIMALS; BACTERIAL INFECTIONS; BACTERIAL PROTEINS; BACTERIAL VACCINES; CELL WALL; CYTOSOL; DNA; DRUG DELIVERY SYSTEMS; EXTRACELLULAR SPACE; GENE EXPRESSION; GENE EXPRESSION REGULATION, BACTERIAL; GENETIC VECTORS; HUMANS; IMMUNITY, MUCOSAL; IMMUNIZATION; LACTOCOCCUS LACTIS; MICE; MUCOUS MEMBRANE; PROTEIN ENGINEERING; VACCINES, DNA; VIRUS DISEASES;

ANIMALIA; BACTERIA (MICROORGANISMS); EUKARYOTA; LACTOCOCCUS LACTIS;

EID: 80051590424     PISSN: 10465928     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pep.2011.06.005     Document Type: Review

References (110)

1. M. de Vrese, A. Stegelmann, B. Richter, S. Fenselau, C. Laue, and J. Schrezenmeir Probiotics - compensation for lactase insufficiency Am. J. Clin. Nutr. 73 2001 421S 429S (Pubitemid 32113266)
2. J.F. Seegers Lactobacilli as live vaccine delivery vectors: progress and prospects Trends Biotechnol. 20 2002 508 515 (Pubitemid 35356405)
3. S. Drouault, G. Corthier, S.D. Ehrlich, and P. Renault Expression of the Staphylococcus hyicus lipase in Lactococcus lactis Appl. Environ. Microbiol. 66 2000 588 598 (Pubitemid 30082745)
4. S. Drouault, C. Juste, P. Marteau, P. Renault, and G. Corthier Oral treatment with Lactococcus lactis expressing Staphylococcus hyicus lipase enhances lipid digestion in pigs with induced pancreatic insufficiency Appl. Environ. Microbiol. 68 2002 3166 3168 (Pubitemid 34602050)
5. J.M. Wells, P.W. Wilson, P.M. Norton, M.J. Gasson, and R.W. Le Page Lactococcus lactis: high-level expression of tetanus toxin fragment C and protection against lethal challenge Mol. Microbiol. 8 1993 1155 1162 (Pubitemid 23187034)
6. P.M. Norton, R.W. Le Page, and J.M. Wells Progress in the development of Lactococcus lactis as a recombinant mucosal vaccine delivery system Folia Microbiol. (Praha) 40 1995 225 230
7. Y. Le Loir, S. Nouaille, J. Commissaire, L. Bretigny, A. Gruss, and P. Langella Signal peptide and propeptide optimization for heterologous protein secretion in Lactococcus lactis Appl. Environ. Microbiol. 67 2001 4119 4127 (Pubitemid 33641707)
8. P.D. Becker, M. Noerder, and C.A. Guzman Genetic immunization: bacteria as DNA vaccine delivery vehicles Hum Vaccin 4 2008 189 202
9. J.M. Chatel, L. Pothelune, S. Ah-Leung, G. Corthier, J.M. Wal, and P. Langella In vivo transfer of plasmid from food-grade transiting lactococci to murine epithelial cells Gene Ther. 15 2008 1184 1190
10. V.D. Guimaraes, S. Innocentin, F. Lefevre, V. Azevedo, J.M. Wal, P. Langella, and J.M. Chatel Use of native lactococci as vehicles for delivery of DNA into mammalian epithelial cells Appl. Environ. Microbiol. 72 2006 7091 7097 (Pubitemid 44748422)
11. M.E. Stiles, and W.H. Holzapfel Lactic acid bacteria of foods and their current taxonomy Int. J. Food Microbiol. 36 1997 1 29 (Pubitemid 27198916)
12. F.J. Carr, D. Chill, and N. Maida The lactic acid bacteria: a literature survey Crit. Rev. Microbiol. 28 2002 281 370 (Pubitemid 36106334)
13. P. Tailliez Mini-revue: les bactéries lactiques, ces êtres vivants apparus il y a prs de 3 milliards d'annés Lait 81 2001 1 11 (Pubitemid 33589294)
14. M. van de Guchte, S.D. Ehrlich, and E. Maguin Production of growth-inhibiting factors by Lactobacillus delbrueckii J. Appl. Microbiol. 91 2001 147 153 (Pubitemid 32623360)
15. R. Fuller, and G.R. Gibson Modification of the intestinal microflora using probiotics and prebiotics Scand. J. Gastroenterol. Suppl. 222 1997 28 31 (Pubitemid 27196256)
16. A.C. Ouwehand, S. Salminen, and E. Isolauri Probiotics: an overview of beneficial effects Antonie Van Leeuwenhoek 82 2002 279 289
17. S. Amdekar, D. Dwivedi, P. Roy, S. Kushwah, and V. Singh Probiotics: multifarious oral vaccine against infectious traumas FEMS Immunol. Med. Microbiol. 58 2010 299 306
18. M.B. Roberfroid Prebiotics and probiotics: are they functional foods? Am. J. Clin. Nutr. 71 2000 1682S 1687S (discussion 1688S-1690S)
19. H.N. Brahmbhatt, A.A. Lindberg, and K.N. Timmis Shigella lipopolysaccharide: structure, genetics, and vaccine development Curr. Top. Microbiol. Immunol. 180 1992 45 64
20. A. Stevenson, and M. Roberts Use of Bordetella bronchiseptica and Bordetella pertussis as live vaccines and vectors for heterologous antigens FEMS Immunol. Med. Microbiol. 37 2003 121 128 (Pubitemid 36776493)
21. E. Medina, and C.A. Guzman Use of live bacterial vaccine vectors for antigen delivery: potential and limitations Vaccine 19 2001 1573 1580 (Pubitemid 32175714)
22. G. Vassaux, J. Nitcheu, S. Jezzard, and N.R. Lemoine Bacterial gene therapy strategies J. Pathol. 208 2006 290 298 (Pubitemid 43126121)
23. S. Stahl, P. Samuelson, M. Hansson, C. Andréoni, L. Goetsch, C. Libon, S. Liljeqvist, E. Gunneriusson, H. Binz, T.N. Nguyen, and M. Uhlén Development of non-pathogenic staphylococci as vaccine delivery vehicles G.J.M.a.P. Wells, Recombinant Gram-positive Bacteria as Vaccine Vehicles for Mucosal 1997 R.G. Landes Biomedical Publishers New York 61 81
24. S.F. Lee Oral colonization and immune responses to Streptococcus gordonii: potential use as a vector to induce antibodies against respiratory pathogens Curr. Opin. Infect. Dis. 16 2003 231 235 (Pubitemid 36677317)
25. S. Salminen, A. von Wright, L. Morelli, P. Marteau, D. Brassart, W.M. de Vos, R. Fonden, M. Saxelin, K. Collins, G. Mogensen, S.E. Birkeland, and T. Mattila-Sandholm Demonstration of safety of probiotics - a review Int. J. Food Microbiol. 44 1998 93 106 (Pubitemid 28486945)
26. A. Mercenier Lactic acid bacteria as live vaccines G. Tannock, Probiotics: A Critical Review 1999 Horizon Scientific Press Wymondham 113 127
27. D. Medaglini, C.M. Rush, P. Sestini, and G. Pozzi Commensal bacteria as vectors for mucosal vaccines against sexually transmitted diseases: vaginal colonization with recombinant streptococci induces local and systemic antibodies in mice Vaccine 15 1997 1330 1337 (Pubitemid 27397808)
28. J.M. Chatel, P. Langella, K. Adel-Patient, J. Commissaire, J.M. Wal, and G. Corthier Induction of mucosal immune response after intranasal or oral inoculation of mice with Lactococcus lactis producing bovine beta-lactoglobulin Clin. Diagn. Lab. Immunol. 8 2001 545 551 (Pubitemid 32428878)
29. N. Reveneau, M.C. Geoffroy, C. Locht, P. Chagnaud, and A. Mercenier Comparison of the immune responses induced by local immunizations with recombinant Lactobacillus plantarum producing tetanus toxin fragment C in different cellular locations Vaccine 20 2002 1769 1777 (Pubitemid 34242832)
30. L. Steidler, K. Robinson, L. Chamberlain, K.M. Schofield, E. Remaut, R.W. Le Page, and J.M. Wells Mucosal delivery of murine interleukin-2 (IL-2) and IL-6 by recombinant strains of Lactococcus lactis coexpressing antigen and cytokine Infect. Immun. 66 1998 3183 3189 (Pubitemid 28303115)
31. M. Medina, J. Villena, S. Salva, E. Vintini, P. Langella, and S. Alvarez Nasal administration of Lactococcus lactis improves local and systemic immune responses against Streptococcus pneumoniae Microbiol. Immunol. 52 2008 399 409
32. J.M. Wells, and A. Mercenier Mucosal delivery of therapeutic and prophylactic molecules using lactic acid bacteria Nat. Rev. Microbiol. 6 2008 349 362 (Pubitemid 351552656)
33. L. Tao, S.I. Pavlova, X. Ji, L. Jin, and G. Spear A novel plasmid for delivering genes into mammalian cells with noninvasive food and commensal lactic acid bacteria Plasmid 65 2011 8 14
34. J. Glenting, and S. Wessels Ensuring safety of DNA vaccines Microb Cell Fact 4 2005 26
35. A. Bolotin, S. Mauger, K. Malarme, S.D. Ehrlich, and A. Sorokin Low-redundancy sequencing of the entire Lactococcus lactis IL1403 genome Antonie Van Leeuwenhoek 76 1999 27 76 (Pubitemid 29440720)
36. W.M. de Vos Gene expression systems for lactic acid bacteria Curr. Opin. Microbiol. 2 1999 289 295 (Pubitemid 29260149)
37. L. Jannire, A. Gruss, and D. Ehrlich Plasmids A.L. Sonenshein, J.A. Hoch, R. Losick, Bacillus subtilis and Other Gram-positive Bacteria: Biochemistry, Physiology and Molecular Genetics 1993 American Society for Microbiology Washington DC 625 644
38. D. Simon, and A. Chopin Construction of a vector plasmid family and its use for molecular cloning in Streptococcus lactis Biochimie 70 1988 559 566
39. J. Kok, J.M. van der Vossen, and G. Venema Construction of plasmid cloning vectors for lactic streptococci which also replicate in Bacillus subtilis and Escherichia coli Appl. Environ. Microbiol. 48 1984 726 731 (Pubitemid 14010837)
40. A. Nauta, D. van Sinderen, H. Karsens, E. Smit, G. Venema, and J. Kok Inducible gene expression mediated by a repressor-operator system isolated from Lactococcus lactis bacteriophage r1t Mol. Microbiol. 19 1996 1331 1341 (Pubitemid 26111504)
41. O.P. Kuipers, M.M. Beerthuyzen, R.J. Siezen, and W.M. De Vos Characterization of the nisin gene cluster nisABTCIPR of Lactococcus lactis. Requirement of expression of the nisA and nisI genes for development of immunity Eur. J. Biochem. 216 1993 281 291 (Pubitemid 23255198)
42. P.G. de Ruyter, O.P. Kuipers, and W.M. de Vos Controlled gene expression systems for Lactococcus lactis with the food-grade inducer nisin Appl. Environ. Microbiol. 62 1996 3662 3667 (Pubitemid 26329592)
43. O.P. Kuipers, P.G. De Ruyter, M. Kleerebezem, and W.M. de Vos Quorum sensing controlled gene expression in lactic acid bacteria Biotechnology 64 1998 15 21 (Pubitemid 29027781)
44. Z. Eichenbaum, M.J. Federle, D. Marra, W.M. de Vos, O.P. Kuipers, M. Kleerebezem, and J.R. Scott Use of the lactococcal nisA promoter to regulate gene expression in gram-positive bacteria: comparison of induction level and promoter strength Appl. Environ. Microbiol. 64 1998 2763 2769 (Pubitemid 28363139)
45. S. Pavan, P. Hols, J. Delcour, M.C. Geoffroy, C. Grangette, M. Kleerebezem, and A. Mercenier Adaptation of the nisin-controlled expression system in Lactobacillus plantarum: a tool to study in vivo biological effects Appl. Environ. Microbiol. 66 2000 4427 4432
46. M. Kleerebezem, M.M. Beerthuyzen, E.E. Vaughan, W.M. De Vos, and O.P. Kuipers Controlled gene expression systems for lactic acid bacteria: transferable nisin-inducible expression cassettes for Lactococcus, Leuconostoc, and Lactobacillus spp Appl. Environ. Microbiol. 63 1997 4581 4584 (Pubitemid 27485794)
47. G.M. Oddone, D.A. Mills, and D.E. Block Incorporation of nisI-mediated nisin immunity improves vector-based nisin-controlled gene expression in lactic acid bacteria Plasmid 61 2009 151 158
48. L. Bredmose, S.M. Madsen, A. Vrang, P. Ravn, M.G. Johnsen, J. Glenting, and H. Israelsen Development of a heterologous gene expression system for use in Lactococcus lactis: a novel Gram-positive expression system O.-W. Merten, D. Mattanovich, C. Lang, G. Larsson, P. Neubauer, D. Porro, P. Postma, J. Teixeira de Mattos, J.A. Cole, Recombinant Protein Production with Prokaryotic and Eukaryotic Cells - A Comparative View on Host Physiology 2001 Kluwer Academic Publishers Dordrecht 270 272
49. S.M. Madsen, J. Arnau, A. Vrang, M. Givskov, and H. Israelsen Molecular characterization of the pH-inducible and growth phase-dependent promoter P170 of Lactococcus lactis Mol. Microbiol. 32 1999 75 87 (Pubitemid 29164135)
50. D. Shortle A genetic system for analysis of staphylococcal nuclease Gene 22 1983 181 189 (Pubitemid 13099594)
51. H. Israelsen, S.M. Madsen, A. Vrang, E.B. Hansen, and E. Johansen Cloning and partial characterization of regulated promoters from Lactococcus lactis Tn917-lacZ integrants with the new promoter probe vector, pAK80 Appl. Environ. Microbiol. 61 1995 2540 2547
52. G.M. Djordjevic, and T.R. Klaenhammer Inducible gene expression systems in Lactococcus lactis Mol. Biotechnol. 9 1998 127 139 (Pubitemid 28414967)
53. M. Simonen, and I. Palva Protein secretion in Bacillus species Microbiol. Rev. 57 1993 109 137 (Pubitemid 23078439)
54. H. Ton-That, G. Liu, S.K. Mazmanian, K.F. Faull, and O. Schneewind Purification and characterization of sortase, the transpeptidase that cleaves surface proteins of Staphylococcus aureus at the LPXTG motif. Proc. Natl. Acad. Sci. USA 96 1999 12424 12429 (Pubitemid 29513518)
55. V.A. Fischetti, V. Pancholi, and O. Schneewind Conservation of a hexapeptide sequence in the anchor region of surface proteins from gram-positive cocci Mol. Microbiol. 4 1990 1603 1605
56. M. van Asseldonk, G. Rutten, M. Oteman, R.J. Siezen, W.M. de Vos, and G. Simons Cloning of usp45, a gene encoding a secreted protein from Lactococcus lactis subsp. lactis MG1363 Gene 95 1990 155 160
57. Y. Le Loir, A. Gruss, S.D. Ehrlich, and P. Langella Direct screening of recombinants in gram-positive bacteria using the secreted staphylococcal nuclease as a reporter J. Bacteriol. 176 1994 5135 5139 (Pubitemid 24253758)
58. J.C. Piard, I. Hautefort, V.A. Fischetti, S.D. Ehrlich, M. Fons, and A. Gruss Cell wall anchoring of the Streptococcus pyogenes M6 protein in various lactic acid bacteria J. Bacteriol. 179 1997 3068 3072 (Pubitemid 27194463)
59. J.M. Wells, P.W. Wilson, P.M. Norton, and R.W. Le Page A model system for the investigation of heterologous protein secretion pathways in Lactococcus lactis Appl. Environ. Microbiol. 59 1993 3954 3959 (Pubitemid 23327609)
60. Y. Dieye, S. Usai, F. Clier, A. Gruss, and J.C. Piard Design of a protein-targeting system for lactic acid bacteria J. Bacteriol. 183 2001 4157 4166 (Pubitemid 32568066)
61. I. Poquet, V. Saint, E. Seznec, N. Simoes, A. Bolotin, and A. Gruss HtrA is the unique surface housekeeping protease in Lactococcus lactis and is required for natural protein processing Mol. Microbiol. 35 2000 1042 1051 (Pubitemid 30137774)
62. Y. Le Loir, A. Gruss, S.D. Ehrlich, and P. Langella A nine-residue synthetic propeptide enhances secretion efficiency of heterologous proteins in Lactococcus lactis J. Bacteriol. 180 1998 1895 1903 (Pubitemid 28173072)
63. Y. Le Loir, V. Azevedo, S.C. Oliveira, D.A. Freitas, A. Miyoshi, L.G. Bermudez-Humaran, S. Nouaille, L.A. Ribeiro, S. Leclercq, J.E. Gabriel, V.D. Guimaraes, M.N. Oliveira, C. Charlier, M. Gautier, and P. Langella Protein secretion in Lactococcus lactis: an efficient way to increase the overall heterologous protein production Microb. Cell Fact. 4 2005 2
64. S. Nouaille, L.A. Ribeiro, A. Miyoshi, D. Pontes, Y. Le Loir, S.C. Oliveira, P. Langella, and V. Azevedo Heterologous protein production and delivery systems for Lactococcus lactis Genet. Mol. Res. 2 2003 102 111 (Pubitemid 38846553)
65. E. Jamet Etude de l'Expression et de la Régulation des Gnes Impliqués Dans le Métabolisme Carboné Chez Lactococcus lactis 2001 Institut National Agronomique de Paris-Grignon Grignon
66. A. Miyoshi, E. Jamet, J. Commissaire, P. Renault, P. Langella, and V. Azevedo A xylose-inducible expression system for Lactococcus lactis FEMS Microbiol. Lett. 239 2004 205 212 (Pubitemid 39346126)
67. D. Llull, and I. Poquet New expression system tightly controlled by zinc availability in Lactococcus lactis Appl. Environ. Microbiol. 70 2004 5398 5406 (Pubitemid 39279616)
68. E. Morello, L.G. Bermudez-Humaran, D. Llull, V. Sole, N. Miraglio, P. Langella, and I. Poquet Lactococcus lactis, an efficient cell factory for recombinant protein production and secretion J. Mol. Microbiol. Biotechnol. 14 2008 48 58 (Pubitemid 350022332)
69. S. Gottesman Proteases and their targets in Escherichia coli Annu. Rev. Genet. 30 1996 465 506 (Pubitemid 27014475)
70. C.M. Henriksen, D. Nilsson, S. Hansen, E. Johansen, and Industrial applications of genetically modified microorganisms: gene technology at Chr. Hansen A/S Int. Dairy J. 9 1999 17 23
71. F. Dickely, D. Nilsson, E.B. Hansen, and E. Johansen Isolation of Lactococcus lactis nonsense suppressors and construction of a food-grade cloning vector Mol. Microbiol. 15 1995 839 847
72. K.I. Sorensen, R. Larsen, A. Kibenich, M.P. Junge, and E. Johansen A food-grade cloning system for industrial strains of Lactococcus lactis Appl. Environ. Microbiol. 66 2000 1253 1258 (Pubitemid 30185586)
73. J. Glenting, S.M. Madsen, A. Vrang, A. Fomsgaard, and H. Israelsen A plasmid selection system in Lactococcus lactis and its use for gene expression in L. lactis and human kidney fibroblasts Appl. Environ. Microbiol. 68 2002 5051 5056 (Pubitemid 35154817)
74. V.D. Guimaraes, J.E. Gabriel, F. Lefevre, D. Cabanes, A. Gruss, P. Cossart, V. Azevedo, and P. Langella Internalin-expressing Lactococcus lactis is able to invade small intestine of guinea pigs and deliver DNA into mammalian epithelial cells Microb. Infect. 7 2005 836 844 (Pubitemid 40826649)
75. S. Innocentin, V. Guimaraes, A. Miyoshi, V. Azevedo, P. Langella, J.M. Chatel, and F. Lefevre Lactococcus lactis expressing either Staphylococcus aureus fibronectin-binding protein A or Listeria monocytogenes internalin A can efficiently internalize and deliver DNA in human epithelial cells Appl. Environ. Microbiol. 75 2009 4870 4878
76. K. Robinson, L.M. Chamberlain, K.M. Schofield, J.M. Wells, and R.W. Le Page Oral vaccination of mice against tetanus with recombinant Lactococcus lactis Nat. Biotechnol. 15 1997 653 657 (Pubitemid 27291166)
77. T.L. Chang, C.H. Chang, D.A. Simpson, Q. Xu, P.K. Martin, L.A. Lagenaur, G.K. Schoolnik, D.D. Ho, S.L. Hillier, M. Holodniy, J.A. Lewicki, and P.P. Lee Inhibition of HIV infectivity by a natural human isolate of Lactobacillus jensenii engineered to express functional two-domain CD4 Proc. Natl. Acad. Sci. USA 100 2003 11672 11677 (Pubitemid 37205993)
78. M. Iwaki, N. Okahashi, I. Takahashi, T. Kanamoto, Y. Sugita-Konishi, K. Aibara, and T. Koga Oral immunization with recombinant Streptococcus lactis carrying the Streptococcus mutans surface protein antigen gene Infect. Immun. 58 1990 2929 2934 (Pubitemid 20267682)
79. C. Grangette, H. Muller-Alouf, D. Goudercourt, M.C. Geoffroy, M. Turneer, and A. Mercenier Mucosal immune responses and protection against tetanus toxin after intranasal immunization with recombinant Lactobacillus plantarum Infect. Immun. 69 2001 1547 1553 (Pubitemid 32187607)
80. N.G. Cortes-Perez, F. Lefevre, G. Corthier, K. Adel-Patient, P. Langella, and L.G. Bermudez-Humaran 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 2007 6581 6588 (Pubitemid 47224988)
81. C. Daniel, F. Sebbane, S. Poiret, D. Goudercourt, J. Dewulf, C. Mullet, M. Simonet, and B. Pot Protection against Yersinia pseudotuberculosis infection conferred by a Lactococcus lactis mucosal delivery vector secreting LcrV Vaccine 27 2009 1141 1144
82. L.G. Bermudez-Humaran, N.G. Cortes-Perez, F. Lefevre, V. Guimaraes, S. Rabot, J.M. Alcocer-Gonzalez, J.J. Gratadoux, C. Rodriguez-Padilla, R.S. Tamez-Guerra, G. Corthier, A. Gruss, and P. Langella 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 2005 7297 7302 (Pubitemid 41713425)
83. N.G. Cortes-Perez, P. Kharrat, P. Langella, and L.G. Bermudez-Humaran Heterologous production of human papillomavirus type-16 L1 protein by a lactic acid bacterium BMC Res Notes 2 2009 167
84. L. Steidler, W. Hans, L. Schotte, S. Neirynck, F. Obermeier, W. Falk, W. Fiers, and E. Remaut Treatment of murine colitis by Lactococcus lactis secreting interleukin-10 Science 289 2000 1352 1355 (Pubitemid 30656052)
85. L. Steidler, S. Neirynck, N. Huyghebaert, V. Snoeck, A. Vermeire, B. Goddeeris, E. Cox, J.P. Remon, and E. Remaut Biological containment of genetically modified Lactococcus lactis for intestinal delivery of human interleukin 10 Nat. Biotechnol. 21 2003 785 789 (Pubitemid 36791397)
86. H. Braat, P. Rottiers, D.W. Hommes, N. Huyghebaert, E. Remaut, J.P. Remon, S.J. van Deventer, S. Neirynck, M.P. Peppelenbosch, and L. Steidler A phase I trial with transgenic bacteria expressing interleukin-10 in Crohn's disease Clin. Gastroenterol. Hepatol. 4 2006 754 759 (Pubitemid 43841860)
87. K.Q. Xin, Y. Hoshino, Y. Toda, S. Igimi, Y. Kojima, N. Jounai, K. Ohba, A. Kushiro, M. Kiwaki, K. Hamajima, D. Klinman, and K. Okuda Immunogenicity and protective efficacy of orally administered recombinant Lactococcus lactis expressing surface-bound HIV Env. Blood 102 2003 223 228 (Pubitemid 36759658)
88. K. Robinson, L.M. Chamberlain, M.C. Lopez, C.M. Rush, H. Marcotte, R.W. Le Page, and J.M. Wells Mucosal and cellular immune responses elicited by recombinant Lactococcus lactis strains expressing tetanus toxin fragment C Infect. Immun. 72 2004 2753 2761 (Pubitemid 38542403)
89. M.A. Kutzler, and D.B. Weiner DNA vaccines: ready for prime time? Nat. Rev. Genet. 9 2008 776 788
90. H. Sung, and M.R. Schleiss Update on the current status of cytomegalovirus vaccines Expert Rev. Vaccines 9 2010 1303 1314
91. V. Guimaraes, S. Innocentin, J.M. Chatel, F. Lefevre, P. Langella, V. Azevedo, and A. Miyoshi A new plasmid vector for DNA delivery using lactococci Genet. Vaccines Ther. 7 2009 4
92. M.I. Masood, M.I. Qadir, J.H. Shirazi, and I.U. Khan Beneficial effects of lactic acid bacteria on human beings Crit. Rev. Microbiol. 37 2011 91 98
93. J. Mengaud, H. Ohayon, P. Gounon, R.M. Mege, and P. Cossart E-cadherin is the receptor for internalin, a surface protein required for entry of L. monocytogenes into epithelial cells Cell 84 1996 923 932 (Pubitemid 26106861)
94. M. Lecuit, S. Vandormael-Pournin, J. Lefort, M. Huerre, P. Gounon, C. Dupuy, C. Babinet, and P. Cossart A transgenic model for listeriosis: role of internalin in crossing the intestinal barrier Science 292 2001 1722 1725 (Pubitemid 32506246)
95. B.E. Menzies The role of fibronectin binding proteins in the pathogenesis of Staphylococcus aureus infections Curr. Opin. Infect. Dis. 16 2003 225 229 (Pubitemid 36677316)
96. N.A. Meenan, L. Visai, V. Valtulina, U. Schwarz-Linek, N.C. Norris, S. Gurusiddappa, M. Hook, P. Speziale, and J.R. Potts The tandem beta-zipper model defines high affinity fibronectin-binding repeats within Staphylococcus aureus FnBPA J. Biol. Chem. 282 2007 25893 25902 (Pubitemid 47372812)
97. R.C. Massey, M.N. Kantzanou, T. Fowler, N.P. Day, K. Schofield, E.R. Wann, A.R. Berendt, M. Hook, and S.J. Peacock Fibronectin-binding protein A of Staphylococcus aureus has multiple substituting, binding regions that mediate adherence to fibronectin and invasion of endothelial cells. Cell. Microbiol. 3 2001 839 851 (Pubitemid 33133479)
98. Y.A. Que, J.A. Haefliger, L. Piroth, P. Francois, E. Widmer, J.M. Entenza, B. Sinha, M. Herrmann, P. Francioli, P. Vaudaux, and P. Moreillon Fibrinogen and fibronectin binding cooperate for valve infection and invasion in Staphylococcus aureus experimental endocarditis J. Exp. Med. 201 2005 1627 1635 (Pubitemid 40721006)
99. P. Rottiers, T. De Smedt, and L. Steidler Modulation of gut-associated lymphoid tissue functions with genetically modified Lactococcus lactis Int. Rev. Immunol. 28 2009 465 486
100. Y.S. Huang, M. Fisher, Z. Nasrawi, and Z. Eichenbaum Defense from the group a streptococcus by active and passive vaccination with the streptococcal hemoprotein receptor J. Infect. Dis. 203 2011 1595 1601
101. B. Marelli, A.R. Perez, C. Banchio, D. de Mendoza, and C. Magni Oral immunization with live Lactococcus lactis expressing rotavirus VP8 subunit induces specific immune response in mice J. Virol. Method 175 2011 28 37
102. H. Jing, L. Yong, L. Haiyan, M. Yanjun, X. Yun, Z. Yu, L. Taiming, C. Rongyue, J. Liang, W. Jie, Z. Li, and L. Jingjing Oral administration of Lactococcus lactis delivered heat shock protein 65 attenuates atherosclerosis in low-density lipoprotein receptor-deficient mice Vaccine 29 2011 4102 4109
103. llena, M. Medina, S. Racedo, and S. Alvarez Resistance of young mice to pneumococcal infection can be improved by oral vaccination with recombinant Lactococcus lactis J. Microbiol. Immunol. Infect. 43 2010 1 10
104. Q. Gu, D. Song, and M. Zhu Oral vaccination of mice against Helicobacter pylori with recombinant Lactococcus lactis expressing urease subunit B FEMS Immunol. Med. Microbiol. 56 2009 197 203
105. S.B. Hanniffy, A.T. Carter, E. Hitchin, and J.M. Wells Mucosal delivery of a pneumococcal vaccine using Lactococcus lactis affords protection against respiratory infection J. Infect. Dis. 195 2007 185 193 (Pubitemid 46080050)
106. P. Mannam, K.F. Jones, and B.L. Geller Mucosal vaccine made from live, recombinant Lactococcus lactis protects mice against pharyngeal infection with Streptococcus pyogenes Infect. Immun. 72 2004 3444 3450 (Pubitemid 38697770)
107. H.I. Cheun, K. Kawamoto, M. Hiramatsu, H. Tamaoki, T. Shirahata, S. Igimi, and S.I. Makino Protective immunity of SpaA-antigen producing Lactococcus lactis against Erysipelothrix rhusiopathiae infection J. Appl. Microbiol. 96 2004 1347 1353 (Pubitemid 38703616)
108. C.A. Perez, C. Eichwald, O. Burrone, and D. Mendoza Rotavirus vp7 antigen produced by Lactococcus lactis induces neutralizing antibodies in mice J. Appl. Microbiol. 99 2005 1158 1164 (Pubitemid 41531306)
109. S. Buccato, D. Maione, C.D. Rinaudo, G. Volpini, A.R. Taddei, R. Rosini, J.L. Telford, G. Grandi, and I. Margarit Use of Lactococcus lactis expressing pili from group B Streptococcus as a broad-coverage vaccine against streptococcal disease J. Infect. Dis. 194 2006 331 340 (Pubitemid 44116975)
110. D.S. Pontes, F.A. Dorella, L.A. Ribeiro, A. Miyoshi, Y. Le Loir, A. Gruss, S.C. Oliveira, P. Langella, and V. Azevedo Induction of partial protection in mice after oral administration of Lactococcus lactis producing Brucella abortus L7/L12 antigen J. Drug Target. 11 2003 489 493 (Pubitemid 38519158)