Live bacterial vaccine vectors: An overview

Brazilian Journal of Microbiology

Volumn 45, Issue 4, 2014, Pages 1117-1129

  da Silva, Adilson José ^a   Zangirolami, Teresa Cristina ^a   Novo Mansur, Maria Teresa Marques ^a   de Campos Giordano, Roberto ^a   Martins, Elizabeth Angélica Leme ^b  

^a FEDERAL UNIVERSITY OF SÃO CARLOS   (Brazil)

^b INSTITUTO BUTANTAN   (Brazil)

Author keywords

Antigen presentation; Bacterial vector; Cancer vaccine; DNA vaccine; Vaccine delivery system

Indexed keywords

BACTERIA (MICROORGANISMS);

BACTERIAL VACCINE; DRUG CARRIER; LIVE VACCINE;

ANIMAL; BACTERIAL INFECTIONS; GENETICS; HUMAN; IMMUNOLOGY; NEOPLASMS; TRANSGENIC ORGANISM;

ANIMALS; BACTERIAL INFECTIONS; BACTERIAL VACCINES; DRUG CARRIERS; HUMANS; NEOPLASMS; ORGANISMS, GENETICALLY MODIFIED; VACCINES, ATTENUATED;

EID: 84923687711     PISSN: 15178382     EISSN: 16784405     Source Type: Journal    
DOI: 10.1590/s1517-83822014000400001     Document Type: Review

References (133)

1. Adachi K, Kawana K, Yokoyama T, Fujii T, Tomio A, Miura S, Tomio K, Kojima S, Oda K, Sewaki T et al. (2010) Oral immunization with a Lactobacillus casei vaccine expressing human papillomavirus (HPV) type 16 E7 is an effective strategy to induce mucosal cytotoxic lymphocytes against HPV16 E7. Vaccine 28:2810-2817.
2. Aebischer T, Bumann D, Epple HJ, Metzger W, Schneider T, Cherepnev G, Walduck AK, Kunkel D, Moos V, Loddenkemper C et al. (2008) Correlation of T cell response and bacterial clearance in human volunteers challenged with Helicobacter pylori revealed by randomised controlled vaccination with Ty21a-based Salmonella vaccines. Gut 57:1065-1072.
3. Alaniz RC, Deatherage BL, Lara JC, Cookson BT (2007) Membrane vesicles are immunogenic facsimiles of Salmonella typhimurium that potently activate dendritic cells, prime B and T cell responses, and stimulate protective immunity in vivo. J Immunol 179:7692-7701.
4. Ashraf S, Kong W, Wang S, Yang J, Curtiss R (2011) Protective cellular responses elicited by vaccination with influenza nucleoprotein delivered by a live recombinant attenuated Salmonella vaccine. Vaccine 29:3990-4002.
5. Bahey-El-Din M, Gahan CG (2011) Lactococcus lactis-based vaccines: current status and future perspectives. Hum Vaccin 7:106-109.
6. Baillie LW, Rodriguez AL, Moore S, Atkins HS, Feng C, Nataro JP, Pasetti MF (2008) Towards a human oral vaccine for anthrax: the utility of a Salmonella typhi Ty21a-based primeboost immunization strategy. Vaccine 26:6083-6091.
7. Bao JX, Clements JD (1991) Prior immunologic experience potentiates the subsequent antibody response when Salmonella strains are used as vaccine carriers. Infect Immun 59:3841-3845.
8. Barry EM, Wang J, Wu T, Davis T, Levine MM (2006) Immunogenicity of multivalent Shigella-ETEC candidate vaccine strains in a guinea pig model. Vaccine 24:3727-3734.
9. Bastos RG, Borsuk S, Seixas FK, Dellagostin OA (2009) Recombinant Mycobacterium bovis BCG. Vaccine 27:6495-6503.
10. Bereta M, Hayhurst A, Gajda M, Chorobik P, Targosz M, Marcinkiewicz J, Kaufman HL (2007) Improving tumor targeting and therapeutic potential of Salmonella VNP20009 by displaying cell surface CEA-specific antibodies. Vaccine 25:4183-4192.
11. Bermúdez-Humarán LG, Cortes-Perez NG, Lefèvre F, Guimarães V, Rabot S, Alcocer-Gonzalez JM, Gratadoux JJ, Rodriguez- Padilla C, Tamez-Guerra RS, Corthier G 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.
12. Bouvet JP, Fischetti VA (1999) Diversity of antibody-mediated immunity at the mucosal barrier. Infect Immun 67:2687-2691.
13. Braat H, Rottiers P, Hommes DW, Huyghebaert N, Remaut E, Remon JP, van Deventer SJ, Neirynck S, Peppelenbosch MP, Steidler L (2006) A phase I trial with transgenic bacteria expressing interleukin-10 in Crohn’s disease. Clin Gastroenterol Hepatol 4:754-759.
14. Brockstedt DG, Giedlin MA, Leong ML, Bahjat KS, Gao Y, Luckett W, Liu W, Cook DN, Portnoy DA, Dubensky TW (2004) Listeria-based cancer vaccines that segregate immunogenicity from toxicity. Proc Natl Acad Sci U S A 101:13832-13837.
15. Bruhn KW, Craft N, Miller JF (2007) Listeria as a vaccine vector. Microbes Infect 9:1226-1235.
16. Buddenborg C, Daudel D, Liebrecht S, Greune L, Humberg V, Schmidt MA (2008) Development of a tripartite vector system for live oral immunization using a gram-negative probiotic carrier. Int J Med Microbiol 298:105-114.
17. Bullifent HL, Griffin KF, Jones SM, Yates A, Harrington L, Titball RW (2000) Antibody responses to Yersinia pestis F1-antigen expressed in Salmonella typhimurium aroA from in vivo-inducible promoters. Vaccine 18:2668-2676.
18. Bumann D, Behre C, Behre K, Herz S, Gewecke B, Gessner JE, von Specht BU, Baumann U (2010) Systemic, nasal and oral live vaccines against Pseudomonas aeruginosa: a clinical trial of immunogenicity in lower airways of human volunteers. Vaccine 28:707-713.
19. Chabalgoity JA, Baz A, Rial A, Grille S (2007) The relevance of cytokines for development of protective immunity and rational design of vaccines. Cytokine Growth Factor Rev 18:195-207.
20. Cheminay C, Hensel M (2008) Rational design of Salmonella recombinant vaccines. Int J Med Microbiol 298:87-98.
21. Chorobik P, Marcinkiewicz J (2011) Therapeutic vaccines based on genetically modified Salmonella: a novel strategy in cancer immunotherapy. Pol Arch Med Wewn 121:461-466.
22. Cortes-Perez NG, Lefèvre F, Corthier G, Adel-Patient K, Langella P, Bermúdez-Humarán LG (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.
23. Curtiss R, Wanda SY, Gunn BM, Zhang X, Tinge SA, Ananthnarayan V, Mo H, Wang S, Kong W (2009) Salmonella enterica serovar Typhimurium strains with regulated delayed attenuation in vivo. Infect Immun 77:1071-1082.
24. Curtiss R, Xin W, Li Y, Kong W, Wanda SY, Gunn B, Wang S (2010) New technologies in using recombinant attenuated Salmonella vaccine vectors. Crit Rev Immunol 30:255-270.
25. Cárdenas L, Clements JD (1992) Oral immunization using live attenuated Salmonella spp. as carriers of foreign antigens. Clin Microbiol Rev 5:328-342.
26. Duc lH, Hong HA, Fairweather N, Ricca E, Cutting SM (2003) Bacterial spores as vaccine vehicles. Infect Immun 71:2810-2818.
27. Dunstan SJ, Simmons CP, Strugnell RA (1999) Use of in vivoregulated promoters to deliver antigens from attenuated Salmonella enterica var. Typhimurium. Infect Immun 67:5133-5141.
28. Epaulard O, Toussaint B, Quenee L, Derouazi M, Bosco N, Villiers C, Le Berre R, Guery B, Filopon D, Crombez L et al. (2006) Anti-tumor immunotherapy via antigen delivery from a live attenuated genetically engineered Pseudomonas aeruginosa type III secretion system-based vector. Mol Ther 14:656-661.
29. Feng Y, Wang S, Luo F, Ruan Y, Kang L, Xiang X, Chao T, Peng G, Zhu C, Mu Y et al. (2008) A novel recombinant bacterial vaccine strain expressing dual viral antigens induces multiple immune responses to the Gag and gp120 proteins of HIV-1 in immunized mice. Antiviral Res 80:272-279.
30. Ferreira LC, Ferreira RC, SchumannW(2005) Bacillus subtilis as a tool for vaccine development: from antigen factories to delivery vectors. An Acad Bras Cienc 77:113-124.
31. Feunou PF, Kammoun H, Debrie AS, Mielcarek N, Locht C (2010) Long-term immunity against pertussis induced by a single nasal administration of live attenuated B. pertussis BPZE1. Vaccine 28:7047-7053.
32. Flesch IE, Collins H, Hess J, Kaufmann SH (1998) Checkpoints in antibacterial immunity. Res Immunol 149:693-697.
33. Gahan ME, Webster DE, Wijburg OL, Wesselingh SL, Strugnell RA (2008). Impact of prior immunological exposure on vaccine delivery by Salmonella enterica serovar Typhimurium. Vaccine 26:6212-6220.
34. Galen JE, LevineMM(2001) Can a ‘flawless’ live vector vaccine strain be engineered? Trends Microbiol 9:372-376.
35. Galen JE, Pasetti MF, Tennant S, Ruiz-Olvera P, Sztein MB, Levine MM (2009) Salmonella enterica serovar Typhi live vector vaccines finally come of age. Immunol Cell Biol 87:400-412.
36. Gentschev I, Dietrich G, Goebel W (2002) The E. coli alphahemolysin secretion system and its use in vaccine development. Trends Microbiol 10:39-45.
37. Georgiou G, Stathopoulos C, Daugherty PS, Nayak AR, Iverson BL, Curtiss R (1997) Display of heterologous proteins on the surface of microorganisms: from the screening of combinatorial libraries to live recombinant vaccines. Nat Biotechnol 15:29-34.
38. Hernández-Luna MA, Luria-Pérez R, Huerta-Yépez S (2013) Therapeutic intervention alternatives in cancer, using attenuated live bacterial vectors: Salmonella enterica as a carrier of heterologous molecules. Rev Invest Clin 65:65-73.
39. Ho SY, Chua SQ, Foo DG, Locht C, Chow VT, Poh CL, Alonso S (2008) Highly attenuated Bordetella pertussis strain BPZE1 as a potential live vehicle for delivery of heterologous vaccine candidates. Infect Immun 76:111-119.
40. Hoft DF, Blazevic A, Abate G, Hanekom WA, Kaplan G, Soler JH, Weichold F, Geiter L, Sadoff JC, Horwitz MA (2008) A new recombinant bacille Calmette-Guérin vaccine safely induces significantly enhanced tuberculosis-specific immunity in human volunteers. J Infect Dis 198:1491-1501.
41. Husseiny MI, Hensel M (2008) Construction of highly attenuated Salmonella enterica serovar Typhimurium live vectors for delivering heterologous antigens by chromosomal integration. Microbiol Res 163:605-615.
42. Husseiny MI, Hensel M (2009) Evaluation of Salmonella live vaccines with chromosomal expression cassettes for translocated fusion proteins. Vaccine 27:3780-3787.
43. Isticato R, Cangiano G, Tran HT, Ciabattini A, Medaglini D, Oggioni MR, De Felice M, Pozzi G, Ricca E (2001) Surface display of recombinant proteins on Bacillus subtilis spores. J Bacteriol 183:6294-6301.
44. Jain V, Mekalanos JJ (2000) Use of lambda phage S and R gene products in an inducible lysis system for Vibrio cholerae and Salmonella enterica serovar Typhimurium-based DNA vaccine delivery systems. Infect Immun 68:986-989.
45. Janeway CA, Medzhitov R (2002) Innate immune recognition. Annu Rev Immunol 20:197-216.
46. Jiang S, Rasmussen RA, Nolan KM, Frankel FR, Lieberman J, McClure HM, Williams KM, Babu US, Raybourne RB, Strobert E et al. (2007) Live attenuated Listeria monocytogenes expressing HIV Gag: immunogenicity in rhesus monkeys. Vaccine 25:7470-7479.
47. Jones B, Pascopella L, Falkow S (1995) Entry of microbes into the host: using M cells to break the mucosal barrier. Curr Opin Immunol 7:474-478.
48. Juárez-Rodríguez MD, Yang J, Kader R, Alamuri P, Curtiss R, Clark-Curtiss JE (2012) Live attenuated Salmonella vaccines displaying regulated delayed lysis and delayed antigen synthesis to confer protection against Mycobacterium tuberculosis. Infect Immun 80:815-831.
49. Kaper JB, Levine MM. 1990. Recombinant attenuated Vibrio cholerae strains used as live oral vaccines. Res Microbiol 141:901-906.
50. Kaufmann SH, Hess J (1999) Impact of intracellular location of and antigen display by intracellular bacteria: implications for vaccine development. Immunol Lett 65:81-84.
51. Keller R, Hilton TD, Rios H, Boedeker EC, Kaper JB (2010) Development of a live oral attaching and effacing Escherichia coli vaccine candidate using Vibrio cholerae CVD 103-HgR as antigen vector. Microb Pathog 48:1-8.
52. Khan S, Chatfield S, Stratford R, Bedwell J, Bentley M, Sulsh S, Giemza R, Smith S, Bongard E, Cosgrove CA et al. (2007) Ability of SPI2 mutant of S. typhi to effectively induce antibody responses to the mucosal antigen enterotoxigenic E. coli heat labile toxin B subunit after oral delivery to humans. Vaccine 25:4175-4182.
53. Kong W, Wanda SY, Zhang X, Bollen W, Tinge SA, Roland KL, Curtiss R (2008) Regulated programmed lysis of recombinant Salmonella in host tissues to release protective antigens and confer biological containment. Proc Natl Acad Sci U S A 105:9361-9366.
54. Kotton CN, Hohmann EL (2004) Enteric pathogens as vaccine vectors for foreign antigen delivery. Infect Immun 72:5535-5547.
55. Kuballa P, Nolte WM, Castoreno AB, Xavier RJ (2012) Autophagy and the immune system. Annu Rev Immunol 30:611-646.
56. Lee SF (2003) Oral colonization and immune responses to Streptococcus gordonii: Potential use as a vector to induce antibodies against respiratory pathogens. Curr Opin Infect Dis 16:231-235.
57. Lee SF, Halperin SA, Wang H, MacArthur A (2002) Oral colonization and immune responses to Streptococcus gordonii expressing a pertussis toxin S1 fragment in mice. FEMS Microbiol Lett 208:175-178.
58. Leenhouts K, Buist G, Kok J (1999). Anchoring of proteins to lactic acid bacteria. Antonie Van Leeuwenhoek 76:367-376.
59. Leibiger R, Niedung K, Geginat G, Heesemann J, Trülzsch K (2008) Yersinia enterocolitica Yop mutants as oral live carrier vaccines. Vaccine 26:6664-6670.
60. Leong ML, Hampl J, Liu W, Mathur S, Bahjat KS, Luckett W, Dubensky TW, Brockstedt DG (2009) Impact of preexisting vector-specific immunity on vaccine potency: characterization of Listeria monocytogenes-specific humoral and cellular immunity in humans and modeling studies using recombinant vaccines in mice. Infect Immun 77:3958-3968.
61. Levine MM, Kaper JB, Herrington D, Ketley J, Losonsky G, Tacket CO, Tall B, Cryz S (1988) Safety, immunogenicity, and efficacy of recombinant live oral cholera vaccines, CVD 103 and CVD 103-HgR. Lancet 2(8609):467-470.
62. Li R, Lim A, Alonso S (2011) Attenuated Bordetella pertussis BPZE1 as a live vehicle for heterologous vaccine antigens delivery through the nasal route. Bioeng Bugs 2:315-319.
63. Li Y, Wang S, Scarpellini G, Gunn B, Xin W, Wanda SY, Roland KL, Curtiss R (2009) Evaluation of new generation Salmonella enterica serovar Typhimurium vaccines with regulated delayed attenuation to induce immune responses against PspA. Proc Natl Acad Sci U S A 106:593-598.
64. Liljeqvist S, Ståhl S (1999) Production of recombinant subunit vaccines: protein immunogens, live delivery systems and nucleic acid vaccines. J Biotechnol 73:1-33.
65. Locht C (2000) Live bacterial vectors for intranasal delivery of protective antigens. Pharm Sci Technol Today 3:121-128.
66. Loessner H, Weiss S (2004) Bacteria-mediated DNA transfer in gene therapy and vaccination. Expert Opin Biol Ther 4:157-168.
67. Lu S (2009) Heterologous prime-boost vaccination. Curr Opin Immunol 21:346-351.
68. Luo Y, Zhou H, Mizutani M, Mizutani N, Reisfeld RA, Xiang R (2003) Transcription factor Fos-related antigen 1 is an effective target for a breast cancer vaccine. Proc Natl Acad Sci U S A 100:8850-8855.
69. Lü L, Cao HD, Zeng HQ, Wang PL, Wang LJ, Liu SN, Xiang TX (2009) Recombinant Mycobacterium smegmatis mc(2)155 vaccine expressing outer membrane protein 26 kDa antigen affords therapeutic protection against Helicobacter pylori infection. Vaccine 27:972-978.
70. Maciag PC, Radulovic S, Rothman J (2009) The first clinical use of a live-attenuated Listeria monocytogenes vaccine: a Phase I safety study of Lm-LLO-E7 in patients with advanced carcinoma of the cervix. Vaccine 27:3975-3983.
71. Mastroeni P, Chabalgoity JA, Dunstan SJ, Maskell DJ, Dougan G (2001) Salmonella: immune responses and vaccines. Vet J 161:132-164.
72. McKelvie ND, Stratford R, Wu T, Bellaby T, Aldred E, Hughes NJ, Chatfield SN, Pickard D, Hale C, Dougan G et al. (2004) Expression of heterologous antigens in Salmonella typhimurium vaccine vectors using the in vivo-inducible, SPI-2 promoter, ssaG. Vaccine 22:3243-3255.
73. Medina E, Paglia P, Rohde M, Colombo MP, Guzmán CA (2000) Modulation of host immune responses stimulated by Salmonella vaccine carrier strains by using different promoters to drive the expression of the recombinant antigen. Eur J Immunol 30:768-777.
74. Meeusen EN, Walker J, Peters A, Pastoret PP, Jungersen G (2007) Current status of veterinary vaccines. Clin Microbiol Rev 20:489-510.
75. Miller VL, Beer KB, Loomis WP, Olson JA, Miller SI (1992) An unusual pagC::TnphoA mutation leads to an invasion- and virulence-defective phenotype in Salmonellae. Infect Immun 60:3763-3770.
76. Miyaji EN, Carvalho E, Oliveira ML, Raw I, Ho PL (2011) Trends in adjuvant development for vaccines: DAMPs and PAMPs as potential new adjuvants. Braz J Med Biol Res 44:500-513.
77. Moore RJ, Rothel L, Krywult J, Radford AJ, Lund K, Hodgson AL (1999) Foreign gene expression in Corynebacterium pseudotuberculosis: development of a live vaccine vector. Vaccine 18:487-497.
78. Muneta Y, Panicker IS, Kanci A, Craick D, Noormohammadi AH, Bean A, Browning GF, Markham PF (2008) Development and immunogenicity of recombinant Mycoplasma gallisepticum vaccine strain ts-11 expressing chicken IFN-gamma. Vaccine 26:5449-5454.
79. Muralinath M, Kuehn MJ, Roland KL, Curtiss R (2011) Immunization with Salmonella enterica serovar Typhimuriumderived outer membrane vesicles delivering the pneumococcal protein PspA confers protection against challenge with Streptococcus pneumoniae. Infect Immun 79:887-894.
80. Nasser Eddine A, Kaufmann SH (2005) Improved protection by recombinant BCG. Microbes Infect 7:939-946.
81. Netea MG, van der Meer JW (2011) Immunodeficiency and genetic defects of pattern-recognition receptors. N Engl J Med 364:60-70.
82. Nishikawa H, Sato E, Briones G, Chen LM, Matsuo M, Nagata Y, Ritter G, Jäger E, Nomura H, Kondo S et al., 2006.In vivo antigen delivery by a Salmonella typhimurium type III secretion system for therapeutic cancer vaccines. J Clin Invest 116:1946-1954.
83. Ogawa Y, Oishi E, Muneta Y, Sano A, Hikono H, Shibahara T, Yagi Y, Shimoji Y (2009) Oral vaccination against mycoplasmal pneumonia of swine using a live Erysipelothrix rhusiopathiae vaccine strain as a vector. Vaccine 27:4543-4550.
84. Oggioni MR, Manganelli R, Contorni M, Tommasino M, Pozzi G (1995) Immunization of mice by oral colonization with live recombinant commensal streptococci. Vaccine 13:775-779.
85. Oxer MD, Bentley CM, Doyle JG, Peakman TC, Charles IG, Makoff AJ (1991) High level heterologous expression in E. coli using the anaerobically-activated nirB promoter. Nucleic Acids Res 19:2889-2892.
86. Paccez JD, Nguyen HD, Luiz WB, Ferreira RC, Sbrogio-Almeida ME, Schuman W, Ferreira LC (2007) Evaluation of different promoter sequences and antigen sorting signals on the immunogenicity of Bacillus subtilis vaccine vehicles. Vaccine 25:4671-4680.
87. Pacheco LG, Mati VL, Castro TL, Dorella FA, Oliveira SC, Miyoshi A, de Melo AL, Azevedo V (2008) Oral immunization with Salmonella harboring a Sm14-based DNA vaccine does not protect mice against Schistosoma mansoni infection. Parasitol Int 57:506-508.
88. Pan Z, Zhang X, Geng S, Cheng N, Sun L, Liu B, Huang J, Jiao X (2009) Priming with a DNA vaccine delivered by attenuated Salmonella typhimurium and boosting with a killed vaccine confers protection of chickens against infection with the H9 subtype of avian influenza virus. Vaccine 27:1018-1023.
89. Panthel K, Meinel KM, Sevil Domènech VE, Trülzsch K, Rüssmann H (2008) Salmonella type III-mediated heterologous antigen delivery: a versatile oral vaccination strategy to induce cellular immunity against infectious agents and tumors. Int J Med Microbiol 298:99-103.
90. Pardoll D (2003) Does the immune system see tumors as foreign or self? Annu Rev Immunol 21:807-839.
91. Paterson Y, Guirnalda PD, Wood LM (2010) Listeria and Salmonella bacterial vectors of tumor-associated antigens for cancer immunotherapy. Semin Immunol 22:183-189.
92. Pavot V, Rochereau N, Genin C, Verrier B, Paul S (2012) New insights in mucosal vaccine development. Vaccine 30:142-154.
93. Perdigón G, de Macias ME, Alvarez S, Oliver G, de Ruiz Holgado AP (1988) Systemic augmentation of the immune response in mice by feeding fermented milks with Lactobacillus casei and Lactobacillus acidophilus. Immunology 63:17-23.
94. Pilgrim S, Stritzker J, Schoen C, Kolb-Mäurer A, Geginat G, Loessner MJ, Gentschev I, Goebel W (2003) Bactofection of mammalian cells by Listeria monocytogenes: improvement and mechanism of DNA delivery. Gene Ther 10:2036-2045.
95. Portnoy DA, Chakraborty T, Goebel W, Cossart P (1992) Molecular determinants of Listeria monocytogenes pathogenesis. Infect Immun 60:1263-1267.
96. 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.
97. Ramasamy R, Yasawardena S, Zomer A, Venema G, Kok J, Leenhouts K (2006) Immunogenicity of a malaria parasite antigen displayed by Lactococcus lactis in oral immunisations. Vaccine 24:3900-3908.
98. Rescigno M, Rotta G, Valzasina B, Ricciardi-Castagnoli P (2001) Dendritic cells shuttle microbes across gut epithelial monolayers. Immunobiology 204:572-581.
99. Roberts M, Li J, Bacon A, Chatfield S (1998) Oral vaccination against tetanus: comparison of the immunogenicities of Salmonella strains expressing fragment C from the nirB and htrA promoters. Infect Immun 66:3080-3087.
100. Roland KL, Cloninger C, Kochi SK, Thomas LJ, Tinge SA, Rouskey C, Killeen KP (2007) Construction and preclinical evaluation of recombinant Peru-15 expressing high levels of the cholera toxin B subunit as a vaccine against enterotoxigenic Escherichia coli. Vaccine 25:8574-8584.
101. Rosenkranz CD, Chiara D, Agorio C, Baz A, Pasetti MF, Schreiber F, Dematteis S, Martinez M, Sztein MB, Chabalgoity JA (2003) Towards new immunotherapies: targeting recombinant cytokines to the immune system using live attenuated Salmonella. Vaccine 21:798-801.
102. Rüssmann H, Shams H, Poblete F, Fu Y, Galán JE, Donis RO (1998) Delivery of epitopes by the Salmonella type III secretion system for vaccine development. Science 281(5376):565-8.
103. Schoen C, Kolb-Mäurer A, Geginat G, Löffler D, Bergmann B, Stritzker J, Szalay AA, Pilgrim S, Goebel W (2005) Bacterial delivery of functional messenger RNA to mammalian cells. Cell Microbiol 7:709-724.
104. Schoen C, Stritzker J, Goebel W, Pilgrim S (2004) Bacteria as DNA vaccine carriers for genetic immunization. Int J Med Microbiol 294:319-335.
105. Seegers JF (2002) Lactobacilli as live vaccine delivery vectors: progress and prospects. Trends Biotechnol 20:508-515.
106. Seo SU, Kim JJ, Yang H, Kwon HJ, Yang JY, Curtiss III R, Kweon MN (2012) Effective protection against secondary pneumococcal pneumonia by oral vaccination with attenuated Salmonella delivering PspA antigen in mice. Vaccine 30:6816-6823.
107. Sevil Domènech VE, Panthel K, Meinel KM, Winter SE, Rüssmann H (2007) Pre-existing anti-Salmonella vector immunity prevents the development of protective antigen-specific CD8 T-cell frequencies against murine listeriosis. Microbes Infect 9:1447-1453.
108. Sevil Domènech VE, Panthel K, Winter SE, Rüssmann H (2008) Heterologous prime-boost immunizations with different Salmonella serovars for enhanced antigen-specific CD8 T-cell induction. Vaccine 26:1879-1886.
109. Sewell DA, Shahabi V, Gunn GR, Pan ZK, Dominiecki ME, Paterson Y (2004) Recombinant Listeria vaccines containing PEST sequences are potent immune adjuvants for the tumor- associated antigen human papillomavirus-16 E7. Cancer Res 64:8821-8825.
110. Shata MT, Stevceva L, Agwale S, Lewis GK, Hone DM (2000) Recent advances with recombinant bacterial vaccine vectors. Mol Med Today 6:66-71.
111. Silva AJ, Eko FO, Benitez JA (2008) Exploiting cholera vaccines as a versatile antigen delivery platform. Biotechnol Lett 30:571-579.
112. Singh R, WallechaA(2011) Cancer immunotherapy using recombinant Listeria monocytogenes: transition from bench to clinic. Hum Vaccin 7:497-505.
113. Sizemore DR, Branstrom AA, Sadoff JC (1995) Attenuated Shigella as a DNA delivery vehicle for DNA-mediated immunization. Science 270(5234):299-302.
114. Soussi N, Saklani-Jusforgues H, Colle JH, Milon G, Glaichenhaus N, Goossens PL (2002) Effect of intragastric and intraperitoneal immunisation with attenuated and wild-type LACK-expressing Listeria monocytogenes on control of murine Leishmania major infection. Vaccine 20:2702-2712.
115. Spreng S, Dietrich G, Goebel W, Gentschev I (1999) The Escherichia coli haemolysin secretion apparatus: a potential universal antigen delivery system in gram-negative bacterial vaccine carriers. Mol Microbiol 31:1596-1598.
116. Spreng S, Dietrich G, Weidinger G (2006) Rational design of Salmonella- based vaccination strategies. Methods 38:133-143.
117. Starks H, Bruhn KW, Shen H, Barry RA, Dubensky TW, Brockstedt D, Hinrichs DJ, Higgins DE, Miller JF, Giedlin M et al. (2004) Listeria monocytogenes as a vaccine vector: virulence attenuation or existing antivector immunity does not diminish therapeutic efficacy. J Immunol 173:420-427.
118. Stevens R, Lavoy A, Nordone S, Burkhard M, Dean GA (2005) Pre-existing immunity to pathogenic Listeria monocytogenes does not prevent induction of immune responses to feline immunodeficiency virus by a novel recombinant Listeria monocytogenes vaccine. Vaccine 23:1479-1490.
119. Sun W, Roland KL, Kuang X, Branger CG, Curtiss R (2010) Yersinia pestis with regulated delayed attenuation as a vaccine candidate to induce protective immunity against plague. Infect Immun 78:1304-1313.
120. Tartz S, Rüssmann H, Kamanova J, Sebo P, Sturm A, Heussler V, Fleischer B, Jacobs T (2008) Complete protection against P. berghei malaria upon heterologous prime/boost immunization against circumsporozoite protein employing Salmonella type III secretion system and Bordetella adenylate cyclase toxoid. Vaccine 26:5935-5943.
121. Uyen NQ, Hong HA, Cutting SM (2007) Enhanced immunisation and expression strategies using bacterial spores as heat-stable vaccine delivery vehicles. Vaccine 25:356-365.
122. Vindurampulle CJ, Attridge SR (2003) Impact of vector priming on the immunogenicity of recombinant Salmonella vaccines. Infect Immun 71:287-297.
123. Weiss S (2003) Transfer of eukaryotic expression plasmids to mammalian hosts by attenuated Salmonella spp. Int J Med Microbiol 293:95-106.
124. Wells JM, Mercenier A (2008) Mucosal delivery of therapeutic and prophylactic molecules using lactic acid bacteria. Nat Rev Microbiol 6:349-362.
125. Wood LM, Guirnalda PD, Seavey MM, Paterson Y (2008) Cancer immunotherapy using Listeria monocytogenes and listerial virulence factors. Immunol Res 42:233-245.
126. Xiang R, Luo Y, Niethammer AG, Reisfeld RA (2008) Oral DNA vaccines target the tumor vasculature and microenvironment and suppress tumor growth and metastasis. Immunol Rev 222:117-128.
127. Xin W, Wanda SY, Li Y, Wang S, Mo H, Curtiss R (2008) Analysis of type II secretion of recombinant pneumococcal PspA and PspC in a Salmonella enterica serovar Typhimurium vaccine with regulated delayed antigen synthesis. Infect Immun 76:3241-3254.
128. Xu D, McSorley SJ, Tetley L, Chatfield S, Dougan G, Chan WL, Satoskar A, David JR, Liew FY (1998) Protective effect on Leishmania major infection of migration inhibitory factor, TNF-alpha, and IFN-gamma administered orally via attenuated Salmonella typhimurium. J Immunol 160:1285-1289.
129. Xu DQ, Cisar JO, Osorio M, Wai TT, Kopecko DJ (2007) Corelinked LPS expression of Shigella dysenteriae serotype 1 O-antigen in live Salmonella typhi vaccine vector Ty21a: preclinical evidence of immunogenicity and protection. Vaccine 25:6167-6175.
130. Yang H, Cao S, Huang X, Liu J, Tang Y, Wen X (2009) Intragastric administration of attenuated Salmonella typhimurium harbouring transmissible gastroenteritis virus (TGEV) DNA vaccine induced specific antibody production. Vaccine 27:5035-5040.
131. Yano T, Kurata S (2011) Intracellular recognition of pathogens and autophagy as an innate immune host defence. J Biochem 150:143-149.
132. Zhao X, Li Z, Gu B, Frankel FR (2005) Pathogenicity and immunogenicity of a vaccine strain of Listeria monocytogenes that relies on a suicide plasmid to supply an essential gene product. Infect Immun 73:5789-5798.
133. Zhou Z, Xia H, Hu X, Huang Y, Li Y, Li L, Ma C, Chen X, Hu F, Xu J et al. (2008) Oral administration of a Bacillus subtilis spore-based vaccine expressing Clonorchis sinensis tegumental protein 22.3 kDa confers protection against Clonorchis sinensis. Vaccine 26:1817-1825.