Advanced search
Publication Cover
Expert Review of Vaccines Volume 12, 2013 - Issue 9
Submit an article Journal homepage
341
Views
42
CrossRef citations to date
0
Altmetric
Reviews

Salmonella as a vaccine delivery vehicle

Kenneth L RolandCorrespondence[email protected]
&
Karen E BrennemanThe Biodesign Institute, Arizona State University, 1001 S. McAllister Avenue, Tempe, AZ 85287-5401, USA
Pages 1033-1045 | Published online: 09 Jan 2014

References

  • de Jong HK, Parry CM, van der Poll T, Wiersinga WJ. Host-pathogen interaction in invasive Salmonellosis. PLoS. Pathog 8(10), e1002933 (2012).
  • Pasetti MF, Levine MM, Sztein MB. Animal models paving the way for clinical trials of attenuated Salmonella enterica serovar Typhi live oral vaccines and live vectors. Vaccine 21(5-6), 401–418 (2003).
  • Galen JE, Pasetti MF, Tennant S, Ruiz-Olvera P, Sztein MB, Levine MM. Salmonella enterica serovar Typhi live vector vaccines finally come of age. Immunol. Cell Biol. 87(5), 400–412 (2009).
  • Winter SE, Thiennimitr P, Winter MG et al. Gut inflammation provides a respiratory electron acceptor for Salmonella. Nature 467(7314), 426–429 (2010).
  • Thiennimitr P, Winter SE, Winter MG et al. Intestinal inflammation allows Salmonella to use ethanolamine to compete with the microbiota. Proc. Natl Acad. Sci. USA 108(42), 17480–17485 (2011).
  • Baumler AJ, Gilde AJ, Tsolis RM, van der Velden AW, Ahmer BM, Heffron F. Contribution of horizontal gene transfer and deletion events to development of distinctive patterns of fimbrial operons during evolution of Salmonella serotypes. J. Bacteriol. 179(2), 317–322 (1997).
  • Baumler AJ, Tsolis RM, Heffron F. Contribution of fimbrial operons to attachment to and invasion of epithelial cell lines by Salmonella typhimurium. Infect. Immun. 64(5), 1862–1865 (1996).
  • Folkesson A, Advani A, Sukupolvi S, Pfeifer JD, Normark S, Lofdahl S. Multiple insertions of fimbrial operons correlate with the evolution of Salmonella serovars responsible for human disease. Mol. Microbiol. 33(3), 612–622 (1999).
  • Forest C, Faucher SP, Poirier K, Houle S, Dozois CM, Daigle F. Contribution of the stg fimbrial operon of Salmonella enterica serovar Typhi during interaction with human cells. Infect. Immun. 75(11), 5264–5271 (2007).
  • Townsend SM, Kramer NE, Edwards R et al. Salmonella enterica serovar Typhi possesses a unique repertoire of fimbrial gene sequences. Infect Immun 69(5), 2894–2901 (2001).
  • Parkhill J, Dougan G, James KD et al. Complete genome sequence of a multiple drug resistant Salmonella enterica serovar Typhi CT18. Nature 413(6858), 848–852 (2001).
  • Bonilla CG, Mera EP, Quinonez AD, Yepez SH. Salmonella as live carrier of antigens in vaccine development. In: Salmonella - A Diversified Superbug. Kumar Y ( Ed.). In Tech, Rijeka, Croatia 309–326 (2012).
  • Curtiss R 3rd, Xin W, Li Y et al. New technologies in using recombinant attenuated Salmonella vaccine vectors. Crit. Rev. Immunol. 30(3), 255–270 (2010).
  • Hegazy WA, Hensel M. Salmonella enterica as a vaccine carrier. Future Microbiol. 7(1), 111–127 (2012).
  • Kong W, Clark-Curtiss J, Curtiss R 3rd. Utilizing Salmonella for antigen delivery: the aims and benefits of bacterial delivered vaccination. Expert Rev. Vaccines 12(4), 345–347 (2013).
  • Wang S, Li Y, Scarpellini G et al. Salmonella vaccine vectors displaying delayed antigen synthesis in vivo to enhance immunogenicity. Infect. Immun. 78(9), 3969–3980 (2010).
  • Zhang S, Walters N, Cao L, Robison A, Yang X. Recombinant Salmonella vaccination technology and its application to human bacterial pathogens. Curr. Pharm. Biotechnol. 14(2), 209–219 (2013).
  • Tran QT, Gomez G, Khare S et al. The Salmonella enterica serotype Typhi Vi capsular antigen is expressed after the bacterium enters the ileal mucosa. Infect. Immun. 78(1), 527–535 (2010).
  • Wilson RP, Raffatellu M, Chessa D, Winter SE, Tukel C, Baumler AJ. The Vi-capsule prevents Toll-like receptor 4 recognition of Salmonella. Cell Microbiol. 10(4), 876–890 (2008).
  • Winter SE, Raffatellu M, Wilson RP, Russmann H, Baumler AJ. The Salmonella enterica serotype Typhi regulator TviA reduces interleukin-8 production in intestinal epithelial cells by repressing flagellin secretion. Cell Microbiol. 10(1), 247–261 (2008).
  • Bishop A, House D, Perkins T, Baker S, Kingsley RA, Dougan G. Interaction of Salmonella enterica serovar Typhi with cultured epithelial cells: roles of surface structures in adhesion and invasion. Microbiology 154(Pt 7), 1914–1926 (2008).
  • Janis C, Grant AJ, McKinley TJ et al. In vivo regulation of the Vi antigen in Salmonella and induction of immune responses with an in vivo-inducible promoter. Infect. Immun. 79(6), 2481–2488 (2011).
  • Buckner MM, Croxen MA, Arena ET, Finlay BB. A comprehensive study of the contribution of Salmonella enterica serovar Typhimurium SPI2 effectors to bacterial colonization, survival, and replication in typhoid fever, macrophage, and epithelial cell infection models. Virulence 2(3), 208–216 (2011).
  • Forest CG, Ferraro E, Sabbagh SC, Daigle F. Intracellular survival of Salmonella enterica serovar Typhi in human macrophages is independent of Salmonella pathogenicity island (SPI)-2. Microbiology 156(Pt 12), 3689–3698 (2010).
  • Hoffmann C, Galle M, Dilling S et al. In macrophages, caspase-1 activation by SopE and the type III secretion system-1 of S. typhimurium can proceed in the absence of flagellin. PLoS. One 5(8), e12477 (2010).
  • Zhang S, Santos RL, Tsolis RM et al. The Salmonella enterica serotype Typhimurium effector proteins SipA, SopA, SopB, SopD, and SopE2 act in concert to induce diarrhea in calves. Infect. Immun. 70(7), 3843–3855 (2002).
  • Deng W, Liou SR, Plunkett G, 3rd et al. Comparative genomics of Salmonella enterica serovar Typhi strains Ty2 and CT18. J. Bacteriol. 185(7), 2330–2337 (2003).
  • Trombert AN, Rodas PI, Mora GC. Reduced invasion to human epithelial cell lines of Salmonella enterica serovar Typhi carrying S. Typhimurium sopD2. FEMS Microbiol. Lett. 322(2), 150–156 (2011).
  • Trombert AN, Berrocal L, Fuentes JA, Mora GC. S. Typhimurium sseJ gene decreases the S. Typhi cytotoxicity toward cultured epithelial cells. BMC Microbiol. 10, 312 (2010).
  • Morgan E, Campbell JD, Rowe SC et al. Identification of host-specific colonization factors of Salmonella enterica serovar Typhimurium. Mol. Microbiol. 54(4), 994–1010 (2004).
  • Retamal P, Castillo-Ruiz M, Mora GC. Characterization of MgtC, a virulence factor of Salmonella enterica serovar Typhi. PLoS. One 4(5), e5551 (2009).
  • Retamal P, Castillo-Ruiz M, Villagra NA, Morgado J, Mora GC. Modified intracellular-associated phenotypes in a recombinant Salmonella Typhi expressing S. Typhimurium SPI-3 sequences. PLoS. One 5(2), e9394 (2010).
  • Bueno SM, Gonzalez PA, Carreno LJ et al. The capacity of Salmonella to survive inside dendritic cells and prevent antigen presentation to T cells is host specific. Immunology 124(4), 522–533 (2008).
  • Xu T, Maloy S, McGuire KL. Macrophages influence Salmonella host-specificity in vivo. Microb. Pathog. 47(4), 212–222 (2009).
  • Spano S, Galan JE. A Rab32-dependent pathway contributes to Salmonella Typhi host restriction. Science 338(6109), 960–963 (2012).
  • Spano S, Liu X, Galan JE. Proteolytic targeting of Rab29 by an effector protein distinguishes the intracellular compartments of human-adapted and broad-host Salmonella. Proc. Natl Acad. Sci. USA 108(45), 18418–18423 (2011).
  • Galen JE, Gomez-Duarte OG, Losonsky GA et al. A murine model of intranasal immunization to assess the immunogenicity of attenuated Salmonella typhi live vector vaccines in stimulating serum antibody responses to expressed foreign antigens. Vaccine 15(6–7), 700–708 (1997).
  • Libby SJ, Brehm MA, Greiner DL et al. Humanized nonobese diabetic-scid IL2rγnull mice are susceptible to lethal Salmonella Typhi infection. Proc. Natl Acad. Sci. USA 107(35), 15589–15594 (2010).
  • Song J, Willinger T, Rongvaux A et al. A mouse model for the human pathogen Salmonella Typhi. Cell Host Microbe 8(4), 369–376 (2010).
  • Mian MF, Pek EA, Chenoweth MJ, Coombes BK, Ashkar AA. Humanized mice for Salmonella typhi infection: new tools for an old problem. Virulence 2(3), 248252 (2011).
  • Duthie MS, Windish HP, Fox CB, Reed SG. Use of defined TLR ligands as adjuvants within human vaccines. Immunol. Rev. 239(1), 178–196 (2011).
  • Mathur R, Oh H, Zhang D et al. A mouse model of Salmonella Typhi infection. Cell 151(3), 590–602 (2012).
  • Roland KL, Tinge SA, Kochi SK, Thomas LJ, Killeen KP. Reactogenicity and immunogenicity of live attenuated Salmonella enterica serovar Paratyphi A enteric fever vaccine candidates. Vaccine 28(21), 3679–3687 (2010).
  • Wang S, Kong Q, Curtiss R 3rd. New technologies in developing recombinant attenuated Salmonella vaccine vectors. Microb. Pathog 58, 17–28 (2012).
  • Curtiss R 3rd, Wanda SY, Gunn BM et al. Salmonella strains with regulated delayed attenuation in vivo. Infect. Immun. (2009).
  • Li Y, Wang S, Scarpellini G et al. Evaluation of new generation Salmonella enterica serovar Typhimurium vaccines with regulated delayed attenuation to induce immune responses against PspA. Proc. Natl Acad. Sci. USA 106(2), 593–598 (2009).
  • Wang S, Li Y, Shi H, Sun W, Roland KL, Curtiss R 3rd. Comparison of a regulated delayed antigen synthesis system with in vivo-inducible promoters for antigen delivery by live attenuated Salmonella vaccines. Infect. Immun. 79(2), 937–949 (2011).
  • Dunstan SJ, Simmons CP, Strugnell RA. Use of in vivo-regulated promoters to deliver antigens from attenuated Salmonella enterica var. Typhimurium. Infect. Immun. 67(10), 5133–5141 (1999).
  • Eswarappa SM, Karnam G, Nagarajan AG, Chakraborty S, Chakravortty D. lac repressor is an antivirulence factor of Salmonella enterica: its role in the evolution of virulence in Salmonella. PLoS. One 4(6), e5789 (2009).
  • Li Y, Wang S, Xin W et al. A sopB deletion mutation enhances the immunogenicity and protective efficacy of a heterologous antigen delivered by live attenuated Salmonella enterica vaccines. Infect. Immun. 76(11), 5238–5246 (2008).
  • Shi H, Santander J, Brenneman KE et al. Live recombinant Salmonella Typhi vaccines constructed to investigate the role of rpoS in eliciting immunity to a heterologous antigen. PLoS. One 5(6), e11142 (2010).
  • Kong W, Wanda SY, Zhang X et al. Regulated programmed lysis of recombinant Salmonella in host tissues to release protective antigens and confer biological containment. Proc. Natl Acad. Sci. USA 105(27), 9361–9366 (2008).
  • Kong W, Brovold M, Koeneman BA, Clark-Curtiss J, Curtiss R, 3rd. Turning self-destructing Salmonella into a universal DNA vaccine delivery platform. Proc. Natl Acad. Sci. USA 109(47), 19414–19419 (2012).
  • Kong Q, Six DA, Roland KL et al. Salmonella synthesizing 1-dephosphorylated [corrected] lipopolysaccharide exhibits low endotoxic activity while retaining its immunogenicity. J. Immunol. 187(1), 412–423 (2011).
  • Galen JE, Simon R, Ernst RK. Salmonella expressing detoxified lipopolysaccharide is immunogenic and protective both as an attenuated vaccine and for delivery of foreign antigens. Expert Rev. Vaccines 10(12), 1679–1682 (2011).
  • Hone DM, Harris AM, Levine MM. Adaptive acid tolerance response by Salmonella typhi and candidate live oral typhoid vaccine strains. Vaccine 12(10), 895–898 (1994).
  • McConnell EL, Basit AW, Murdan S. Measurements of rat and mouse gastrointestinal pH, fluid and lymphoid tissue, and implications for in-vivo experiments. J. Pharm. Pharmacol. 60(1), 63–70 (2008).
  • Verdu EF, Fraser R, Armstrong D, Blum AL. Effects of omeprazole and lansoprazole on 24-hour intragastric pH in Helicobacter pylori-positive volunteers. Scand. J. Gastroenterol. 29(12), 1065–1069 (1994).
  • Viala JP, Meresse S, Pocachard B, Guilhon AA, Aussel L, Barras F. Sensing and adaptation to low pH mediated by inducible amino acid decarboxylases in Salmonella. PLoS One 6(7), e22397 (2011).
  • Brenneman KE, Willingham C, Kong W, Curtiss R 3rd, Roland KL. Low-pH rescue of acid-sensitive Salmonella enterica serovar Typhi strains by a rhamnose-regulated arginine decarboxylase aystem. J. Bacteriol. 195(13), 3062–3072 (2013).
  • Galan JE, Nakayama K, Curtiss R 3rd. Cloning and characterization of the asd gene of Salmonella typhimurium: use in stable maintenance of recombinant plasmids in Salmonella vaccine strains. Gene 94(1), 29–35 (1990).
  • Morona R, Yeadon J, Considine A, Morona JK, Manning PA. Construction of plasmid vectors with a non-antibiotic selection system based on the Escherichia coli thyA+ gene: application to cholera vaccine development. Gene 107(1), 139–144 (1991).
  • Angelakopoulos H, Hohmann EL. Pilot study of phoP/phoQ-deleted Salmonella enterica serovar Typhimurium expressing Helicobacter pylori urease in adult volunteers. Infect. Immun. 68(4), 2135–2141. (2000).
  • Ryan ET, Crean TI, Kochi SK et al. Development of a ΔglnA balanced lethal plasmid system for expression of heterologous antigens by attenuated vaccine vector strains of Vibrio cholerae. Infect. Immun. 68(1), 221–226 (2000).
  • Garmory HS, Leckenby MW, Griffin KF et al. Antibiotic-free plasmid stabilization by operator-repressor titration for vaccine delivery by using live Salmonella enterica serovar Typhimurium. Infect. Immun. 73(4), 2005–2011 (2005).
  • Sizemore DR, Warner EA, Lawrence JA, Thomas LJ, Roland KL, Killeen KP. Construction and screening of attenuated ΔphoP/Q Salmonella typhimurium vectored plague vaccine candidates. Hum. Vaccin. Immunother. 8(3), 371–383 (2012).
  • Klose KE, Mekalanos JJ. Simultaneous prevention of glutamine synthesis and high-affinity transport attenuates Salmonella typhimurium virulence. Infect. Immun. 65(2), 587–596 (1997).
  • Galen JE, Wang JY, Chinchilla M et al. A new generation of stable, nonantibiotic, low-copy-number plasmids improves immune responses to foreign antigens in Salmonella enterica serovar Typhi live vectors. Infect. Immun. 78(1), 337–347 (2010).
  • Galen JE, Zhao L, Chinchilla M et al. Adaptation of the endogenous Salmonella enterica serovar Typhi clyA-encoded hemolysin for antigen export enhances the immunogenicity of anthrax protective antigen domain 4 expressed by the attenuated live-vector vaccine strain CVD 908-htrA. Infect. Immun. 72(12), 7096–7106 (2004).
  • Tacket CO, Levine MM. CVD 908, CVD 908-htrA, and CVD 909 live oral typhoid vaccines: a logical progression. Clin. Infect. Dis. 45 (Suppl. 1), S20–23 (2007).
  • Santander J, Roland KL, Curtiss R 3rd. Regulation of Vi capsular polysaccharide synthesis in Salmonella enterica serotype Typhi. J. Infect. Dev. Ctries 2(6), 412–420 (2008).
  • Wang JY, Noriega FR, Galen JE, Barry E, Levine MM. Constitutive expression of the Vi polysaccharide capsular antigen in attenuated Salmonella enterica serovar Typhi oral vaccine strain CVD 909. Infect. Immun. 68(8), 4647–4652 (2000).
  • Tacket CO, Pasetti MF, Sztein MB, Livio S, Levine MM. Immune responses to an oral typhoid vaccine strain that is modified to constitutively express Vi capsular polysaccharide. J. Infect. Dis. 190(3), 565–570 (2004).
  • Wahid R, Salerno-Goncalves R, Tacket CO, Levine MM, Sztein MB. Cell-mediated immune responses in humans after immunization with one or two doses of oral live attenuated typhoid vaccine CVD 909. Vaccine 25(8), 1416–1425 (2007).
  • Galen JE, Chinchilla M, Pasetti MF et al. Mucosal immunization with attenuated Salmonella enterica serovar Typhi expressing protective antigen of anthrax toxin (PA83) primes monkeys for accelerated serum antibody responses to parenteral PA83 vaccine. J. Infect. Dis. 199(3), 326–335 (2009).
  • Baillie LW, Rodriguez AL, Moore S et al. Towards a human oral vaccine for anthrax: the utility of a Salmonella Typhi Ty21a-based prime-boost immunization strategy. Vaccine 26(48), 6083–6091 (2008).
  • Wahid R, Pasetti MF, Maciel M Jr. et al. Oral priming with Salmonella Typhi vaccine strain CVD 909 followed by parenteral boost with the S. Typhi Vi capsular polysaccharide vaccine induces CD27+IgD-S. Typhi-specific IgA and IgG B memory cells in humans. Clin. Immunol. 138(2), 187–200 (2011).
  • Wahid R, Simon R, Zafar SJ, Levine MM, Sztein MB. Live oral typhoid vaccine Ty21a induces cross-reactive humoral immune responses against Salmonella enterica serovar Paratyphi A and S. Paratyphi B in humans. Clin. Vaccine Immunol. 19(6), 825–834 (2012).
  • Khan S, Chatfield S, Stratford R et al. 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(21), 4175–4182 (2007).
  • Stratford R, McKelvie ND, Hughes NJ et al. Optimization of Salmonella enterica serovar Typhi ΔaroC ΔssaV derivatives as vehicles for delivering heterologous antigens by chromosomal integration and in vivo inducible promoters. Infect. Immun. 73(1), 362–368 (2005).
  • Fang FC, Libby SJ, Buchmeier NA et al. The alternative sigma factor katF (rpoS) regulates Salmonella virulence. Proc. Natl Acad. Sci. USA 89(24), 11978–11982 (1992).
  • Pakkanen SH, Kantele JM, Kantele A. Cross-reactive gut-directed immune response against Salmonella enterica serovar Paratyphi A and B in typhoid fever and after oral Ty21a typhoid vaccination. Vaccine 30(42), 6047–6053 (2012).
  • Kantele A, Pakkanen SH, Siitonen A, Karttunen R, Kantele JM. Live oral typhoid vaccine Salmonella Typhi Ty21a - a surrogate vaccine against non-typhoid Salmonella? Vaccine 30(50), 7238–7245 (2012).
  • Osorio M, Wu Y, Singh S et al. Anthrax protective antigen delivered by Salmonella enterica serovar Typhi Ty21a protects mice from a lethal anthrax spore challenge. Infect. Immun. 77(4), 1475–1482 (2009).
  • Roszczenko P, Radomska KA, Wywial E, Collet JF, Jagusztyn-Krynicka EK. A novel insight into the oxidoreductase activity of Helicobacter pylori HP0231 protein. PLoS One 7(10), e46563 (2012).
  • Aebischer T, Bumann D, Epple HJ et al. 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(8), 1065–1072 (2008).
  • Bumann D, Behre C, Behre K et al. Systemic, nasal and oral live vaccines against Pseudomonas aeruginosa: a clinical trial of immunogenicity in lower airways of human volunteers. Vaccine 28(3), 707–713 (2010).
  • Knapp B, Hundt E, Lenz U et al. A recombinant hybrid outer membrane protein for vaccination against Pseudomonas aeruginosa. Vaccine 17(13–14), 1663-1666 (1999).
  • Niethammer AG, Lubenau H, Mikus G et al. Double-blind, placebo-controlled first in human study to investigate an oral vaccine aimed to elicit an immune reaction against the VEGF-receptor 2 in patients with stage IV and locally advanced pancreatic cancer. BMC Cancer 12, 361 (2012).
  • Niethammer AG, Xiang R, Becker JC et al. A DNA vaccine against VEGF receptor 2 prevents effective angiogenesis and inhibits tumor growth. Nat. Med. 8(12), 1369–1375 (2002).
  • Sorenson B, Banton K, Augustin L et al. Safety and immunogenicity of Salmonella typhimurium expressing C-terminal truncated human IL-2 in a murine model. Biologics 4, 61–73 (2010).
  • Sorenson BS, Banton KL, Augustin LB, Leonard AS, Saltzman DA. Antioxidant oils and Salmonella enterica Typhimurium reduce tumor in an experimental model of hepatic metastasis. Onco. Targets Ther. 4, 59–69 (2011).
  • Hindle Z, Chatfield SN, Phillimore J et al. Characterization of Salmonella enterica derivatives harboring defined aroC and Salmonella pathogenicity island 2 type III secretion system (ssaV) mutations by immunization of healthy volunteers. Infect Immun. 70(7), 3457–3467 (2002).
  • Tacket CO, Hone DM, Curtiss R 3rd et al. Comparison of the safety and immunogenicity of ΔaroC ΔaroD and Δcya Δcrp Salmonella typhi strains in adult volunteers. Infect. Immun. 60(2), 536–541 (1992).
  • Kirkpatrick BD, McKenzie R, O’Neill JP et al. Evaluation of Salmonella enterica serovar Typhi (Ty2 aroC-ssaV-) M01ZH09, with a defined mutation in the Salmonella pathogenicity island 2, as a live, oral typhoid vaccine in human volunteers. Vaccine 24(2), 116–123 (2006).
  • Lyon CE, Sadigh KS, Carmolli MP et al. In a randomized, double-blinded, placebo-controlled trial, the single oral dose typhoid vaccine, M01ZH09, is safe and immunogenic at doses up to 1.7 x 10(10) colony-forming units. Vaccine 28(20), 3602–3608 (2010).
  • Tran TH, Nguyen TD, Nguyen TT et al. A randomised trial evaluating the safety and immunogenicity of the novel single oral dose typhoid vaccine M01ZH09 in healthy Vietnamese children. PLoS. One 5(7), e11778 (2010).

Websites

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Order Reprints Request Corporate Permissions

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

Request Academic Permissions

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.

Related research

People also read lists articles that other readers of this article have read.

Recommended articles lists articles that we recommend and is powered by our AI driven recommendation engine.

Cited by lists all citing articles based on Crossref citations.
Articles with the Crossref icon will open in a new tab.