1,827
Views
15
CrossRef citations to date
0
Altmetric
Research Paper

Adjuvant effect of enterotoxigenic Escherichia coli (ETEC) double-mutant heat-labile toxin (dmLT) on systemic immunogenicity induced by the CFA/I/II/IV MEFA ETEC vaccine: Dose-related enhancement of antibody responses to seven ETEC adhesins (CFA/I, CS1-CS6)

, , ORCID Icon, , , & show all
Pages 419-425 | Received 04 Jun 2019, Accepted 23 Jul 2019, Published online: 23 Aug 2019

References

  • Lycke N, Holmgren J. Strong adjuvant properties of cholera toxin on gut mucosal immune responses to orally presented antigens. Immunology. 1986;59:301–08.
  • Clements JD, Hartzog NM, Lyon FL. Adjuvant activity of Escherichia coli heat-labile enterotoxin and effect on the induction of oral tolerance in mice to unrelated protein antigens. Vaccine. 1988;6(3):269–77. doi:10.1016/0264-410x(88)90223-x.
  • Lycke N. From toxin to adjuvant: basic mechanisms for the control of mucosal IgA immunity and tolerance. Immunol Lett. 2005;97(2):193–98. doi:10.1016/j.imlet.2004.12.008.
  • Freytag LC, Clements JD. Mucosal adjuvants. Vaccine. 2005;23(15):1804–13. doi:10.1016/j.vaccine.2004.11.010.
  • Spangler BD. Structure and function of cholera toxin and the related Escherichia coli heat-labile enterotoxin. Microbiol Rev. 1992;56:622–47.
  • Anosova NG, Chabot S, Shreedhar V, Borawski JA, Dickinson BL, Neutra MR. Cholera toxin, E. coli heat-labile toxin, and non-toxic derivatives induce dendritic cell migration into the follicle-associated epithelium of Peyer’s patches. Mucosal Immunol. 2008;1(1):59–67. doi:10.1038/mi.2007.7.
  • Lycke N. Recent progress in mucosal vaccine development: potential and limitations. Nat Rev Immunol. 2012;12(8):592–605. doi:10.1038/nri3251.
  • Levine MM, Black RE, Clements ML, Lanata C, Sears S, Honda T, Young CR, Finkelstein RA. Evaluation in humans of attenuated Vibrio cholerae El Tor Ogawa strain Texas Star-SR as a live oral vaccine. Infect Immun. 1984;43:515–22.
  • Gagliardi MC, De Magistris MT. Maturation of human dendritic cells induced by the adjuvant cholera toxin: role of cAMP on chemokine receptor expression. Vaccine. 2003;21(9–10):856–61. doi:10.1016/s0264-410x(02)00532-7.
  • Lewis DJ, Huo Z, Barnett S, Kromann I, Giemza R, Galiza E, Woodrow M, Thierry-Carstensen B, Andersen P, Novicki D, et al. Transient facial nerve paralysis (Bell’s palsy) following intranasal delivery of a genetically detoxified mutant of Escherichia coli heat labile toxin. PLoS One. 2009;4(9):e6999. doi:10.1371/journal.pone.0006999.
  • Yamamoto M, McGhee JR, Hagiwara Y, Otake S, Kiyono H. Genetically manipulated bacterial toxin as a new generation mucosal adjuvant. Scand J Immunol. 2001;53:211–17.
  • Lycke N. From toxin to adjuvant: the rational design of a vaccine adjuvant vector, CTA1-DD/ISCOM. Cell Microbiol. 2004;6:23–32.
  • Chong C, Friberg M, Clements JD. LT(R192G), a non-toxic mutant of the heat-labile enterotoxin of Escherichia coli, elicits enhanced humoral and cellular immune responses associated with protection against lethal oral challenge with Salmonella spp. Vaccine. 1998;16(7):732–40. doi:10.1016/s0264-410x(97)00255-7.
  • Norton EB, Lawson LB, Freytag LC, Clements JD. Characterization of a mutant Escherichia coli heat-labile toxin, LT(R192G/L211A), as a safe and effective oral adjuvant. Clin Vaccine Immunol. 2011;18(4):546–51. doi:10.1128/CVI.00538-10.
  • El-Kamary SS, Cohen MB, Bourgeois AL, Van De Verg L, Bauers N, Reymann M, Pasetti MF, Chen WH. Safety and immunogenicity of a single oral dose of recombinant double mutant heat-labile toxin derived from enterotoxigenic Escherichia coli. Clin Vaccine Immunol. 2013;20(11):1764–70. doi:10.1128/CVI.00464-13.
  • Norton EB, Lawson LB, Mahdi Z, Freytag LC, Clements JD. The A subunit of Escherichia coli heat-labile enterotoxin functions as a mucosal adjuvant and promotes IgG2a, IgA, and Th17 responses to vaccine antigens. Infect Immun. 2012;80(7):2426–35. doi:10.1128/IAI.00181-12.
  • Summerton NA, Welch RW, Bondoc L, Yang HH, Pleune B, Ramachandran N, Harris AM, Bland D, Jackson WJ, Park S, et al. Toward the development of a stable, freeze-dried formulation of Helicobacter pylori killed whole cell vaccine adjuvanted with a novel mutant of Escherichia coli heat-labile toxin. Vaccine. 2010;28(5):1404–11. doi:10.1016/j.vaccine.2009.10.147.
  • Leach S, Clements JD, Kaim J, Lundgren A, Giambartolomei GH. The adjuvant double mutant Escherichia coli heat labile toxin enhances IL-17A production in human T cells specific for bacterial vaccine antigens. PLoS One. 2012;7(12):e51718. doi:10.1371/journal.pone.0051718.
  • Holmgren J, Bourgeois L, Carlin N, Clements J, Gustafsson B, Lundgren A, Nygren E, Tobias J, Walker R, Svennerholm A-M. Development and preclinical evaluation of safety and immunogenicity of an oral ETEC vaccine containing inactivated E. coli bacteria overexpressing colonization factors CFA/I, CS3, CS5 and CS6 combined with a hybrid LT/CT B subunit antigen, administered alone and together with dmLT adjuvant. Vaccine. 2013;31(20):2457–64. doi:10.1016/j.vaccine.2013.03.027.
  • Sjökvist Ottsjö L, Flach CF, Clements J, Holmgren J, Raghavan S. A double mutant heat-labile toxin from Escherichia coli, LT(R192G/L211A), is an effective mucosal adjuvant for vaccination against Helicobacter pylori infection. Infect Immun. 2013;81(5):1532–40. doi:10.1128/IAI.01407-12.
  • Martinez-Becerra FJ, Chen X, Dickenson NE, Choudhari SP, Harrison K, Clements JD, Picking WD, Van De Verg LL, Walker RI, Picking WL. Characterization of a novel fusion protein from IpaB and IpaD of Shigella spp. and its potential as a pan-Shigella vaccine. Infect Immun. 2013;81(12):4470–77. doi:10.1128/IAI.00859-13.
  • Nandre R, Ruan X, Duan Q, Zhang W. Enterotoxigenic Escherichia coli heat-stable toxin and heat-labile toxin toxoid fusion 3xSTaN12S-dmLT induces neutralizing anti-STa antibodies in SC immunized mice. FEMS Microbiol Lett. 2016;363(21):1–6. doi:10.1093/femsle/fnw246.
  • Nandre R, Ruan X, Lu T, Duan Q, Sack D, Zhang W. Enterotoxigenic Escherichia coli adhesin-toxoid multiepitope fusion antigen CFA/I/II/IV-3xSTaN12S-mnLTG192G/L211A-derived antibodies inhibit adherence of seven adhesins, neutralize enterotoxicity of LT and STa toxins, and protect piglets against diarrhea. Infect Immun. 2018;86(3):e00550–17. doi:10.1128/IAI.00550-17.
  • Duan Q, Lu T, Garcia C, Yañez C, Nandre RM, Sack DA, Zhang W. Co-administered tag-less toxoid fusion 3xSTaN12S-mnLTR192G/L211A and CFA/I/II/IV MEFA (Multiepitope Fusion Antigen) induce neutralizing antibodies to 7 adhesins (CFA/I, CS1-CS6) and both enterotoxins (LT, STa) of enterotoxigenic Escherichia coli (ETEC). Front Microbiol. 2018;9:1198. doi:10.3389/fmicb.2018.01198.
  • Ruan X, Knudsen DE, Wollenberg KM, Sack DA, Zhang W. Multiepitope fusion antigen induces broadly protective antibodies that prevent adherence of Escherichia coli strains expressing colonization factor antigen I (CFA/I), CFA/ II,and CFA/IV. Clin Vaccine Immunol. 2014;21(2):243–49. doi:10.1128/CVI.00652-13.
  • Zhang W, Zhang C, Francis DH, Fang Y, Knudsen D, Nataro JP, Robertson DC. Genetic fusions of heat-labile (LT) and heat-stable (ST) toxoids of porcine enterotoxigenic Escherichia coli elicit neutralizing anti-LT and anti-STa antibodies. Infect Immun. 2010;78(1):316–25. doi:10.1128/IAI.00497-09.
  • Ruan X, Robertson DC, Nataro JP, Clements JD, Zhang W. STa toxoid vaccine consortium group. Characterization of heat-stable (STa) toxoids of enterotoxigenic Escherichia coli fused to a double mutant heat-labile toxin (dmLT) peptide in inducing neutralizing anti-STa antibodies. Infect Immun. 2014;82(5):1823–32. doi:10.1128/IAI.01394-13.
  • Duan Q, Huang J, Xiao N, Seo H, Zhang W. Neutralizing anti-STa antibodies derived from enterotoxigenic Escherichia coli (ETEC) toxoid fusions with heat-stable toxin (STa) mutant STaN12S, STaL9A/N12S or STaN12S/A14T show little cross-reactivity with guanylin or uroguanylin. Appl Environ Microbiol. 2018;84:e01737–17.
  • Nandre RM, Duan Q, Wang Y, Zhang W. Passive antibodies derived from intramuscularly immunized toxoid fusion 3xSTaN12S-dmLT protect against STa+ enterotoxigenic Escherichia coli (ETEC) diarrhea in a pig model. Vaccine. 2017;35(4):552–56. doi:10.1016/j.vaccine.2016.12.021.