Abstract
The effects of maltose on production and secretion of virulence factors of Vibrio cholerae in strain X28214, classical biotype, and in maltose-defective transposon mutants constructed from this strain were characterized. Maltose was found to inhibit secretion of cholera toxin and to reduce production of the mannose-sensitive hemagglutinin and the soluble hemagglutinin-protease. In contrast, the amount of toxin-coregulated pilus was increased in the presence of maltose. The maltose effect was apparently mediated by genes of the maltose regulon, since inactivation of the malQ or malF gene of V. cholerae by transposon insertion was found to affect production and secretion of the same virulence factors that were responsive to maltose. The malQ and malF mutants showed, in addition, reduced virulence in an infant-mouse model. These results suggest that maltose may have a significant regulatory role in the production of virulence factors and that an intact maltose regulon is needed for full virulence of V. cholerae.
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Selected References
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- Betley M. J., Miller V. L., Mekalanos J. J. Genetics of bacterial enterotoxins. Annu Rev Microbiol. 1986;40:577–605. doi: 10.1146/annurev.mi.40.100186.003045. [DOI] [PubMed] [Google Scholar]
- Clément J. M., Hofnung M. Gene sequence of the lambda receptor, an outer membrane protein of E. coli K12. Cell. 1981 Dec;27(3 Pt 2):507–514. doi: 10.1016/0092-8674(81)90392-5. [DOI] [PubMed] [Google Scholar]
- Crowther R. S., Roomi N. W., Fahim R. E., Forstner J. F. Vibrio cholerae metalloproteinase degrades intestinal mucin and facilitates enterotoxin-induced secretion from rat intestine. Biochim Biophys Acta. 1987 Jun 22;924(3):393–402. doi: 10.1016/0304-4165(87)90153-x. [DOI] [PubMed] [Google Scholar]
- Curtiss R., 3rd, Kelly S. M. Salmonella typhimurium deletion mutants lacking adenylate cyclase and cyclic AMP receptor protein are avirulent and immunogenic. Infect Immun. 1987 Dec;55(12):3035–3043. doi: 10.1128/iai.55.12.3035-3043.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Decker K., Peist R., Reidl J., Kossmann M., Brand B., Boos W. Maltose and maltotriose can be formed endogenously in Escherichia coli from glucose and glucose-1-phosphate independently of enzymes of the maltose system. J Bacteriol. 1993 Sep;175(17):5655–5665. doi: 10.1128/jb.175.17.5655-5665.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- DiRita V. J., Parsot C., Jander G., Mekalanos J. J. Regulatory cascade controls virulence in Vibrio cholerae. Proc Natl Acad Sci U S A. 1991 Jun 15;88(12):5403–5407. doi: 10.1073/pnas.88.12.5403. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Finkelstein R. A., Boesman-Finkelstein M., Chang Y., Häse C. C. Vibrio cholerae hemagglutinin/protease, colonial variation, virulence, and detachment. Infect Immun. 1992 Feb;60(2):472–478. doi: 10.1128/iai.60.2.472-478.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Finkelstein R. A., Boesman-Finkelstein M., Holt P. Vibrio cholerae hemagglutinin/lectin/protease hydrolyzes fibronectin and ovomucin: F.M. Burnet revisited. Proc Natl Acad Sci U S A. 1983 Feb;80(4):1092–1095. doi: 10.1073/pnas.80.4.1092. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Göransson M., Forsman P., Nilsson P., Uhlin B. E. Upstream activating sequences that are shared by two divergently transcribed operons mediate cAMP-CRP regulation of pilus-adhesin in Escherichia coli. Mol Microbiol. 1989 Nov;3(11):1557–1565. doi: 10.1111/j.1365-2958.1989.tb00141.x. [DOI] [PubMed] [Google Scholar]
- Hall R. H., Losonsky G., Silveira A. P., Taylor R. K., Mekalanos J. J., Witham N. D., Levine M. M. Immunogenicity of Vibrio cholerae O1 toxin-coregulated pili in experimental and clinical cholera. Infect Immun. 1991 Jul;59(7):2508–2512. doi: 10.1128/iai.59.7.2508-2512.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Herrington D. A., Hall R. H., Losonsky G., Mekalanos J. J., Taylor R. K., Levine M. M. Toxin, toxin-coregulated pili, and the toxR regulon are essential for Vibrio cholerae pathogenesis in humans. J Exp Med. 1988 Oct 1;168(4):1487–1492. doi: 10.1084/jem.168.4.1487. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hirst T. R., Holmgren J. Conformation of protein secreted across bacterial outer membranes: a study of enterotoxin translocation from Vibrio cholerae. Proc Natl Acad Sci U S A. 1987 Nov;84(21):7418–7422. doi: 10.1073/pnas.84.21.7418. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Holmgren J. Comparison of the tissue receptors for Vibrio cholerae and Escherichia coli enterotoxins by means of gangliosides and natural cholera toxoid. Infect Immun. 1973 Dec;8(6):851–859. doi: 10.1128/iai.8.6.851-859.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jonson G., Holmgren J., Svennerholm A. M. Analysis of expression of toxin-coregulated pili in classical and El Tor Vibrio cholerae O1 in vitro and in vivo. Infect Immun. 1992 Oct;60(10):4278–4284. doi: 10.1128/iai.60.10.4278-4284.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jonson G., Holmgren J., Svennerholm A. M. Epitope differences in toxin-coregulated pili produced by classical and El Tor Vibrio cholerae O1. Microb Pathog. 1991 Sep;11(3):179–188. doi: 10.1016/0882-4010(91)90048-f. [DOI] [PubMed] [Google Scholar]
- Jonson G., Holmgren J., Svennerholm A. M. Identification of a mannose-binding pilus on Vibrio cholerae El Tor. Microb Pathog. 1991 Dec;11(6):433–441. doi: 10.1016/0882-4010(91)90039-d. [DOI] [PubMed] [Google Scholar]
- Jonson G., Sanchez J., Svennerholm A. M. Expression and detection of different biotype-associated cell-bound haemagglutinins of Vibrio cholerae O1. J Gen Microbiol. 1989 Jan;135(1):111–120. doi: 10.1099/00221287-135-1-111. [DOI] [PubMed] [Google Scholar]
- Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
- Lång H. A., Jonson G., Svennerholm A. M., Palva E. T. The maltose-inducible 43 kDa major outer membrane protein in Vibrio cholerae is immunogenic and common to different isolates. Microb Pathog. 1988 Sep;5(3):169–175. doi: 10.1016/0882-4010(88)90019-8. [DOI] [PubMed] [Google Scholar]
- Lång H., Palva E. T. The ompS gene of Vibrio cholerae encodes a growth-phase-dependent maltoporin. Mol Microbiol. 1993 Nov;10(4):891–901. doi: 10.1111/j.1365-2958.1993.tb00960.x. [DOI] [PubMed] [Google Scholar]
- Miller V. L., DiRita V. J., Mekalanos J. J. Identification of toxS, a regulatory gene whose product enhances toxR-mediated activation of the cholera toxin promoter. J Bacteriol. 1989 Mar;171(3):1288–1293. doi: 10.1128/jb.171.3.1288-1293.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Miller V. L., Mekalanos J. J. A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR. J Bacteriol. 1988 Jun;170(6):2575–2583. doi: 10.1128/jb.170.6.2575-2583.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Osek J., Jonson G., Svennerholm A. M., Holmgren J. Enzyme-linked immunosorbent assay for determination of antibodies to Vibrio cholerae toxin-coregulated pili. APMIS. 1992 Nov;100(11):1027–1032. doi: 10.1111/j.1699-0463.1992.tb04036.x. [DOI] [PubMed] [Google Scholar]
- Osek J., Svennerholm A. M., Holmgren J. Protection against Vibrio cholerae El Tor infection by specific antibodies against mannose-binding hemagglutinin pili. Infect Immun. 1992 Nov;60(11):4961–4964. doi: 10.1128/iai.60.11.4961-4964.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Peek J. A., Taylor R. K. Characterization of a periplasmic thiol:disulfide interchange protein required for the functional maturation of secreted virulence factors of Vibrio cholerae. Proc Natl Acad Sci U S A. 1992 Jul 1;89(13):6210–6214. doi: 10.1073/pnas.89.13.6210. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Peterson K. M., Mekalanos J. J. Characterization of the Vibrio cholerae ToxR regulon: identification of novel genes involved in intestinal colonization. Infect Immun. 1988 Nov;56(11):2822–2829. doi: 10.1128/iai.56.11.2822-2829.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pugsley A. P. The complete general secretory pathway in gram-negative bacteria. Microbiol Rev. 1993 Mar;57(1):50–108. doi: 10.1128/mr.57.1.50-108.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pugsley A. P., d'Enfert C., Reyss I., Kornacker M. G. Genetics of extracellular protein secretion by gram-negative bacteria. Annu Rev Genet. 1990;24:67–90. doi: 10.1146/annurev.ge.24.120190.000435. [DOI] [PubMed] [Google Scholar]
- Raibaud O., Vidal-Ingigliardi D., Richet E. A complex nucleoprotein structure involved in activation of transcription of two divergent Escherichia coli promoters. J Mol Biol. 1989 Feb 5;205(3):471–485. doi: 10.1016/0022-2836(89)90218-0. [DOI] [PubMed] [Google Scholar]
- Sandkvist M., Morales V., Bagdasarian M. A protein required for secretion of cholera toxin through the outer membrane of Vibrio cholerae. Gene. 1993 Jan 15;123(1):81–86. doi: 10.1016/0378-1119(93)90543-c. [DOI] [PubMed] [Google Scholar]
- Sharma D. P., Stroeher U. H., Thomas C. J., Manning P. A., Attridge S. R. The toxin-coregulated pilus (TCP) of Vibrio cholerae: molecular cloning of genes involved in pilus biosynthesis and evaluation of TCP as a protective antigen in the infant mouse model. Microb Pathog. 1989 Dec;7(6):437–448. doi: 10.1016/0882-4010(89)90024-7. [DOI] [PubMed] [Google Scholar]
- Sharma D. P., Thomas C., Hall R. H., Levine M. M., Attridge S. R. Significance of toxin-coregulated pili as protective antigens of Vibrio cholerae in the infant mouse model. Vaccine. 1989 Oct;7(5):451–456. doi: 10.1016/0264-410x(89)90161-8. [DOI] [PubMed] [Google Scholar]
- Shuman H. A., Silhavy T. J. Identification of the malK gene product. A peripheral membrane component of the Escherichia coli maltose transport system. J Biol Chem. 1981 Jan 25;256(2):560–562. [PubMed] [Google Scholar]
- Stieglitz H., Cervantes L., Robledo R., Fonseca R., Covarrubias L., Bolivar F., Kupersztoch Y. M. Cloning, sequencing, and expression in Ficoll-generated minicells of an Escherichia coli heat-stable enterotoxin gene. Plasmid. 1988 Jul;20(1):42–53. doi: 10.1016/0147-619x(88)90006-6. [DOI] [PubMed] [Google Scholar]
- Sun D. X., Mekalanos J. J., Taylor R. K. Antibodies directed against the toxin-coregulated pilus isolated from Vibrio cholerae provide protection in the infant mouse experimental cholera model. J Infect Dis. 1990 Jun;161(6):1231–1236. doi: 10.1093/infdis/161.6.1231. [DOI] [PubMed] [Google Scholar]
- Taylor R. K., Miller V. L., Furlong D. B., Mekalanos J. J. 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):2833–2837. doi: 10.1073/pnas.84.9.2833. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Taylor R., Shaw C., Peterson K., Spears P., Mekalanos J. Safe, live Vibrio cholerae vaccines? Vaccine. 1988 Apr;6(2):151–154. doi: 10.1016/s0264-410x(88)80019-7. [DOI] [PubMed] [Google Scholar]
- Walker J. E., Saraste M., Runswick M. J., Gay N. J. Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J. 1982;1(8):945–951. doi: 10.1002/j.1460-2075.1982.tb01276.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yu J., Webb H., Hirst T. R. A homologue of the Escherichia coli DsbA protein involved in disulphide bond formation is required for enterotoxin biogenesis in Vibrio cholerae. Mol Microbiol. 1992 Jul;6(14):1949–1958. doi: 10.1111/j.1365-2958.1992.tb01368.x. [DOI] [PubMed] [Google Scholar]