Abstract
CTXphi is a filamentous bacteriophage that encodes cholera toxin, the principal virulence factor of Vibrio cholerae. CTXphi is unusual among filamentous phages because it encodes a repressor and forms lysogens. CTXphi can infect the existing live-attenuated V. cholerae vaccine strains derived from either the El Tor or classical V. cholerae biotypes and result in vaccine reversion to toxinogenicity. Intraintestinal CTXphi transduction assays were used to demonstrate that El Tor biotype strains of V. cholerae are immune to infection with the El Tor-derived CTXphi, whereas classical strains are not. The El Tor CTXphi repressor, RstR, was sufficient to render classical strains immune to infection with the El Tor CTXphi. The DNA sequences of the classical and El Tor CTXphi repressors and their presumed cognate operators are highly diverged, whereas the sequences that surround this "immunity" region are nearly identical. Transcriptional fusion studies revealed that the El Tor RstR mediated repression of an El Tor rstA-lacZ fusion but did not repress a classical rstA-lacZ fusion. Likewise, the classical RstR only repressed a classical rstA-lacZ fusion. Thus, similar to the mechanistic basis for heteroimmunity among lambdoid phages, the specificity of CTXphi immunity is based on the divergence of the sequences of repressors and their operators. Expression of the El Tor rstR in either El Tor or classical live-attenuated V. cholerae vaccine strains effectively protected these vaccines from CTXphi infection. Introduction of rstR into V. cholerae vaccine strains should enhance their biosafety.
MeSH Terms
Bacteriophages/genetics,immunology
Cholera Toxin/genetics,immunology
Cholera Vaccines/genetics,immunology
Genes, Viral
Molecular Sequence Data
Plasmids
Vibrio cholerae/immunology
Chemicals
Cholera Vaccines
Cholera Toxin
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Kimsey H H
Division of Geographic Medicine and Infectious Diseases, Tupper Research Institute, Tufts-New England Medical Center 041, 750 Washington Street, Boston, MA 02111, USA.
Waldor M K
References (18)
18 references, click to expand
-
Construction and characterization of new cloning vehicles. II. A multipurpose cloning system.
Gene. 1977;2(2):95-113
PMID: 344137
-
Regulation, replication, and integration functions of the Vibrio cholerae CTXphi are encoded by region RS2.
Mol Microbiol. 1997 Jun;24(5):917-26
PMID: 9220000
-
Duplication and amplification of toxin genes in Vibrio cholerae.
Cell. 1983 Nov;35(1):253-63
PMID: 6627396
-
Cholera toxin genes: nucleotide sequence, deletion analysis and vaccine development.
Nature. 1983 Dec 8-14;306(5943):551-7
PMID: 6646234
-
New knowledge on pathogenesis of bacterial enteric infections as applied to vaccine development.
Microbiol Rev. 1983 Dec;47(4):510-50
PMID: 6363898
-
TnphoA: a transposon probe for protein export signals.
Proc Natl Acad Sci U S A. 1985 Dec;82(23):8129-33
PMID: 2999794
-
Promoter-probe vectors for the analysis of divergently arranged promoters.
Gene. 1986;42(1):37-48
PMID: 3087817
-
Use of phoA gene fusions to identify a pilus colonization factor coordinately regulated with cholera toxin.
Proc Natl Acad Sci U S A. 1987 May;84(9):2833-7
PMID: 2883655
-
Toxin, toxin-coregulated pili, and the toxR regulon are essential for Vibrio cholerae pathogenesis in humans.
J Exp Med. 1988 Oct 1;168(4):1487-92
PMID: 2902187
-
Basic local alignment search tool.
J Mol Biol. 1990 Oct 5;215(3):403-10
PMID: 2231712
-
CTX genetic element encodes a site-specific recombination system and an intestinal colonization factor.
Proc Natl Acad Sci U S A. 1993 Apr 15;90(8):3750-4
PMID: 8475125
-
ToxR regulates virulence gene expression in non-O1 strains of Vibrio cholerae that cause epidemic cholera.
Infect Immun. 1994 Jan;62(1):72-8
PMID: 7903285
-
Cholera vaccines: fighting an ancient scourge.
Science. 1994 Sep 2;265(5177):1387-9
PMID: 8073279
-
The sixth and seventh cholera pandemics are due to independent clones separately derived from environmental, nontoxigenic, non-O1 Vibrio cholerae.
J Bacteriol. 1995 Jun;177(11):3191-8
PMID: 7768818
-
Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter.
J Bacteriol. 1995 Jul;177(14):4121-30
PMID: 7608087
-
Lysogenic conversion by a filamentous phage encoding cholera toxin.
Science. 1996 Jun 28;272(5270):1910-4
PMID: 8658163
-
Enteric bacterial toxins: mechanisms of action and linkage to intestinal secretion.
Microbiol Rev. 1996 Mar;60(1):167-215
PMID: 8852900
-
Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid.
J Bacteriol. 1978 Jun;134(3):1141-56
PMID: 149110