Heat-stable enterotoxin of enterotoxigenic Escherichia coli as a vaccine target

Infection and Immunity

Volumn 78, Issue 5, 2010, Pages 1824-1831

  Taxt, Arne ^a   Aasland, Rein ^a,b   Sommerfelt, Halvor ^a,c   Nataro, James ^a,d   Puntervoll, Pål ^a,b  

^a UNIVERSITY OF BERGEN   (Norway)

^b BCCS   (Norway)

^c NORWEGIAN INSTITUTE OF PUBLIC HEALTH   (Norway)

^d UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENTEROTOXIN; ESCHERICHIA COLI ENTEROTOXIN; GUANYLATE CYCLASE; GUANYLATE CYCLASE C RECEPTOR; GUANYLIN; UNCLASSIFIED DRUG; UROGUANYLIN; VACCINE;

ANTIGENICITY; BACTERIAL COLONIZATION; CROSS REACTION; DIARRHEA; HUMAN; IMMUNE RESPONSE; IMMUNOGENICITY; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; SHORT SURVEY; SMALL INTESTINE; THERMOSTABILITY;

AMINO ACID SEQUENCE; BACTERIAL TOXINS; ENTEROTOXIGENIC ESCHERICHIA COLI; ENTEROTOXINS; ESCHERICHIA COLI VACCINES; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, TERTIARY;

EID: 77951221998     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01397-09     Document Type: Short Survey

References (74)

1. Aimoto, S. S., H. H. Watanabe, H. H. Ikemura, Y. Y. Shimonishi, T. T. Takeda, Y. Y. Takeda, and T. T. Miwatani. 1983. Chemical synthesis of a highly potent and heat-stable analog of an enterotoxin produced by a human strain of enterotoxigenic Escherichia coli. Biochem. Biophys. Res. Commun. 112:320-326.
2. Batisson, I., and M. D. Vartanian. 2000. Contribution of defined amino acid residues to the immunogenicity of recombinant Escherichia coli heat-stable enterotoxin fusion proteins. FEMS Microbiol. Lett. 192:223-229.
3. Batisson, I., M. D. Vartanian, B. Gaillard-Martinie, and M. Contrepois. 2000. Full capacity of recombinant Escherichia coli heat-stable enterotoxin fusion proteins for extracellular secretion, antigenicity, disulfide bond formation, and activity. Infect. Immun. 68:4064-4074.
4. Cárdenas, L., and J. D. Clements. 1993. Development of mucosal protection against the heat-stable enterotoxin (ST) of Escherichia coli by oral immunization with a genetic fusion delivered by a bacterial vector. Infect. Immun. 61:4629-4636.
5. Chan, S. K., and R. A. Giannella. 1981. Amino acid sequence of heat-stable enterotoxin produced by Escherichia coli pathogenic for man. J. Biol. Chem. 256:7744-7746.
6. Clemens, J. D., J. R. Harris, D. A. Sack, J. Chakraborty, F. Ahmed, B. F. Stanton, M. U. Khan, B. A. Kay, N. Huda, M. R. Khan, et al. 1988. Field trial of oral cholera vaccines in Bangladesh: results of one year of follow-up. J. Infect. Dis. 158:60-69.
7. Clemens, J. D., D. A. Sack, J. R. Harris, J. Chakraborty, M. R. Khan, B. F. Stanton, B. A. Kay, M. U. Khan, M. Yunus, W. Atkinson, et al. 1986. Field trial of oral cholera vaccines in Bangladesh. Lancet ii:124-127.
8. Clemens, J. D., D. A. Sack, J. R. Harris, J. Chakraborty, P. K. Neogy, B. Stanton, N. Huda, M. U. Khan, B. A. Kay, M. R. Khan, et al. 1988. Cross-protection by B subunit-whole cell cholera vaccine against diarrhea associated with heat-labile toxin-producing enterotoxigenic Escherichia coli: results of a large-scale field trial. J. Infect. Dis. 158:372-377.
9. Clements, J. D. 1990. Construction of a nontoxic fusion peptide for immunization against Escherichia coli strains that produce heat-labile and heatstable enterotoxins. Infect. Immun. 58:1159-1166.
10. Crane, M. R., M. Hugues, P. D. O'Hanley, and S. A. Waldman. 1992. Identification of two affinity states of low affinity receptors for Escherichia coli heat-stable enterotoxin: correlation of occupation of lower affinity state with guanylate cyclase activation. Mol. Pharmacol. 41:1073-1080.
11. Gaastra, W., and A. M. Svennerholm. 1996. Colonization factors of human enterotoxigenic Escherichia coli (ETEC). Trends Microbiol. 4:444-452. (Pubitemid 26373242)
12. Giannella, R. A. 1976. Suckling mouse model for detection of heat-stable Escherichia coli enterotoxin: characteristics of the model. Infect. Immun. 14:95-99.
13. Glenn, G. M., S. A. Frech, R. T. Kenney, and L. R. Ellingsworth. 2005. Transcutaneous immunization: antigen and adjuvant delivery to the skin. Drugs Pharm. Sci. 155:769-788.
14. Guzman-Verduzco, L. M., and Y. M. Kupersztoch. 1987. Fusion of Escherichia coli heat-stable enterotoxin and heat-labile enterotoxin B subunit. J. Bacteriol. 169:5201-5208.
15. Hasegawa, M., and Y. Shimonishi. 2005. Recognition and signal transduction mechanism of Escherichia coli heat-stable enterotoxin and its receptor, guanylate cyclase C. J. Pept. Res. 65:261-271.
16. Houghten, R. A., J. M. Ostresh, and F. A. Klipstein. 1984. Chemical synthesis of an octadecapeptide with the biological and immunological properties of human heat-stable Escherichia coli enterotoxin. Eur. J. Biochem. 145:157-162.
17. Kauffman, P. E. 1981. Production and evaluation of antibody to the heat-stable enterotoxin from a human strain of enterotoxigenic Escherichia coli. Appl. Environ. Microbiol. 42:611-614.
18. Kennedy, D. J., R. N. Greenberg, J. A. Dunn, R. Abernathy, J. S. Ryerse, and R. L. Guerrant. 1984. Effects of Escherichia coli heat-stable enterotoxin STb on intestines of mice, rats, rabbits, and piglets. Infect. Immun. 46:639-643.
19. Klipstein, F. A., and R. F. Engert. 1979. Protective effect of active immunization with purified Escherichia coli heat-labile enterotoxin in rats. Infect. Immun. 23:592-599.
20. Klipstein, F. A., R. F. Engert, and J. D. Clements. 1982. Development of a vaccine of cross-linked heat-stable and heat-labile enterotoxins that protects against Escherichia coli producing either enterotoxin. Infect. Immun. 37:550-557.
21. Klipstein, F. A., R. F. Engert, and J. D. Clements. 1981. Protection in rats immunized with Escherichia coli heat-stable enterotoxin. Infect. Immun. 34:637-639.
22. Klipstein, F. A., R. F. Engert, J. D. Clements, and R. A. Houghten. 1983. Protection against human and porcine enterotoxigenic strains of Escherichia coli in rats immunized with a cross-linked toxoid vaccine. Infect. Immun. 40:924-929.
23. Klipstein, F. A., R. F. Engert, J. D. Clements, and R. A. Houghten. 1983. Vaccine for enterotoxigenic Escherichia coli based on synthetic heat-stable toxin crossed-linked to the B subunit of heat-labile toxin. J. Infect. Dis. 147:318-326.
24. Klipstein, F. A., R. F. Engert, and R. A. Houghten. 1986. Immunisation of volunteers with a synthetic peptide vaccine for enterotoxigenic Escherichia coli. Lancet i:471-472.
25. Klipstein, F. A., R. F. Engert, and R. A. Houghten. 1985. Mucosal antitoxin response in volunteers to immunization with a synthetic peptide of Escherichia coli heat-stable enterotoxin. Infect. Immun. 50:328-332.
26. Klipstein, F. A., R. F. Engert, and R. A. Houghten. 1984. Properties of cross-linked toxoid vaccines made with hyperantigenic forms of synthetic Escherichia coli heat-stable toxin. Infect. Immun. 44:268-273.
27. Klipstein, F. A., R. F. Engert, and R. A. Houghten. 1983. Properties of synthetically produced Escherichia coli heat-stable enterotoxin. Infect. Immun. 39:117-121.
28. Lowenadler, B. 1991. A recombinant Escherichia coli heat-stable enterotoxin (STa) fusion protein eliciting anti-STa neutralizing antibodies. FEMS Microbiol. Lett. 82:271.
29. Marx, U. C., J. Klodt, M. Meyer, H. Gerlach, P. Rosch, W. G. Forssmann, and K. Adermann. 1998. One peptide, two topologies: structure and interconversion dynamics of human uroguanylin isomers. J. Pept. Res. 52:229-240.
30. Moss, J., J. C. Osborne, P. H. Fishman, S. Nakaya, and D. C. Robertson. 1981. Escherichia coli heat-labile enterotoxin. Ganglioside specificity and ADP-ribosyltransferase activity. J. Biol. Chem. 256:2861-2865.
31. Okamoto, K., K. Okamoto, J. Yukitake, Y. Kawamoto, and A. Miyama. 1987. Substitutions of cysteine residues of Escherichia coli heat-stable enterotoxin by oligonucleotide-directed mutagenesis. Infect. Immun. 55:2121-2125.
32. Okamoto, K., K. Okamoto, J. Yukitake, and A. Miyama. 1988. Reduction of enterotoxic activity of Escherichia coli heat-stable enterotoxin by substitution for an asparagine residue. Infect. Immun. 56:2144-2148.
33. Okamoto, K., and M. Takahara. 1990. Synthesis of Escherichia coli heat-stable enterotoxin STp as a pre-pro form and role of the pro sequence in secretion. J. Bacteriol. 172:5260-5265. (Pubitemid 20281979)
34. Ozaki, H., T. Sato, H. Kubota, Y. Hata, Y. Katsube, and Y. Shimonishi. 1991. Molecular structure of the toxin domain of heat-stable enterotoxin produced by a pathogenic strain of Escherichia coli. A putative binding site for a binding protein on rat intestinal epithelial cell membranes. J. Biol. Chem. 266:5934-5941.
35. Pereira, C. M., B. E. Guth, M. E. Sbrogio-Almeida, and B. A. Castilho. 2001. Antibody response against Escherichia coli heat-stable enterotoxin expressed as fusions to flagellin. Microbiology 147:861-867. (Pubitemid 32401326)
36. Rasheed, J. K., L. M. Guzman-Verduzco, and Y. M. Kupersztoch. 1990. Two precursors of the heat-stable enterotoxin of Escherichia coli: evidence of extracellular processing. Mol. Microbiol. 4:265-273.
37. Rosales-Mendoza, S., A. G. Alpuche-Solis, R. E. Soria-Guerra, L. Moreno-Fierros, L. Martinez-Gonzalez, A. Herrera-Diaz, and S. S. Korban. 2009. Expression of an Escherichia coli antigenic fusion protein comprising the heat labile toxin B subunit and the heat stable toxin, and its assembly as a functional oligomer in transplastomic tobacco plants. Plant J. 57:45-54.
38. Saarilahti, H. T., E. T. Palva, J. Holmgren, and J. Sanchez. 1989. Fusion of genes encoding Escherichia coli heat-stable enterotoxin and outer membrane protein OmpC. Infect. Immun. 57:3663-3665.
39. Sanchez, J., S. Johansson, B. Lowenadler, A. M. Svennerholm, and J. Holmgren. 1990. Recombinant cholera toxin B subunit and gene fusion proteins for oral vaccination. Res. Microbiol. 141:971-979.
40. Sanchez, J., A. M. Svennerholm, and J. Holmgren. 1988. Genetic fusion of a non-toxic heat-stable enterotoxin-related decapeptide antigen to cholera toxin B-subunit. FEBS Lett. 241:110-114. (Pubitemid 19004990)
41. Sanchez, J., B. E. Uhlin, T. Grundstrom, J. Holmgren, and T. R. Hirst. 1986. Immunoactive chimeric ST-LT enterotoxins of Escherichia coli generated by in vitro gene fusion. FEBS Lett. 208:194-198. (Pubitemid 17206194)
42. Sato, T., H. Ozaki, Y. Hata, Y. Kitagawa, Y. Katsube, and Y. Shimonishi. 1994. Structural characteristics for biological activity of heat-stable enterotoxin produced by enterotoxigenic Escherichia coli: X-ray crystallography of weakly toxic and nontoxic analogs. Biochemistry 33:8641-8650. (Pubitemid 2122459)
43. Schulz, S., C. K. Green, P. S. Yuen, and D. L. Garbers. 1990. Guanylyl cyclase is a heat-stable enterotoxin receptor. Cell 63:941-948. (Pubitemid 120034935)
44. Schulz, S., M. J. Lopez, M. Kuhn, and D. L. Garbers. 1997. Disruption of the guanylyl cyclase-C gene leads to a paradoxical phenotype of viable but heat-stable enterotoxin-resistant mice. J. Clin. Invest. 100:1590-1595.
45. Sizemore, D. R., K. L. Roland, and U. S. Ryan. 2004. Enterotoxigenic Escherichia coli virulence factors and vaccine approaches. Expert Rev. Vaccines 3:585-595. (Pubitemid 39440833)
46. Sjoling, A., F. Qadri, M. Nicklasson, Y. A. Begum, G. Wiklund, and A. M. Svennerholm. 2006. In vivo expression of the heat stable (estA) and heat labile (eltB) toxin genes of enterotoxigenic Escherichia coli (ETEC). Microbes Infect. 8:2797-2802.
47. So, M., and B. J. McCarthy. 1980. Nucleotide sequence of the bacterial transposon Tn1681 encoding a heat-stable (ST) toxin and its identification in enterotoxigenic Escherichia coli strains. Proc. Natl. Acad. Sci. U. S. A. 77:4011-4015.
48. Svennerholm, A.-M., and J. Tobias. 2008. Vaccines against enterotoxigenic Escherichia coli. Expert Rev. Vaccines 7:795-804.
49. Svennerholm, A. M., C. Åhren, and M. Jertborn. 1997. Oral inactivated vaccines against enterotoxigenic Escherichia coli, p. 865-873. In M. M. Levine, G. C. Woodrow, J. B. Kaper, and G. S. Cobon (ed.), New generation vaccines. Marcel Dekker, Inc., New York, NY.
50. Svennerholm, A. M., and J. J. Holmgren. 1995. Oral vaccines against cholera and enterotoxigenic Escherichia coli diarrhea. Adv. Exp. Med. Biol. 371B:1623-1628.
51. Svennerholm, A. M., M. Lindblad, B. Svennerholm, and J. Holmgren. 1988. Synthesis of nontoxic, antibody-binding Escherichia coli heat-stable enterotoxin (ST (a)) peptides. FEMS Microbiol. Lett. 55:23-28.
52. Svennerholm, A. M., M. Wikstrom, M. Lindblad, and J. Holmgren. 1986. Monoclonal antibodies against Escherichia coli heat-stable toxin (STa) and their use in a diagnostic ST ganglioside GM1-enzyme-linked immunosorbent assay. J. Clin. Microbiol. 24:585-590.
53. Takeda, T., G. B. Nair, K. Suzuki, H. X. Zhe, Y. Yokoo, P. D. Mol, W. Hemelhof, J. P. Butzler, Y. Takeda, and Y. Shimonishi. 1993. Epitope mapping and characterization of antigenic determinants of heat-stable enterotoxin (STh) of enterotoxigenic Escherichia coli by using monoclonal antibodies. Infect. Immun. 61:289-294.
54. Thompson, M. R., and R. A. Giannella. 1985. Revised amino acid sequence for a heat-stable enterotoxin produced by an Escherichia coli strain (18D) that is pathogenic for humans. Infect. Immun. 47:834-836.
55. Turner, S. M., R. R. Chaudhuri, Z. D. Jiang, H. DuPont, C. Gyles, C. W. Penn, M. J. Pallen, and I. R. Henderson. 2006. Phylogenetic comparisons reveal multiple acquisitions of the toxin genes by enterotoxigenic Escherichia coli strains of different evolutionary lineages. J. Clin. Microbiol. 44:4528-4536.
56. Uzzau, S., and A. Fasano. 2000. Cross-talk between enteric pathogens and the intestine. Cell. Microbiol. 2:83-89.
57. Vaandrager, A. B. 2002. Structure and function of the heat-stable enterotoxin receptor/guanylyl cyclase C. Mol. Cell. Biochem. 230:73-83.
58. Valentiner-Branth, P., H. Steinsland, T. K. Fischer, M. Perch, F. Scheutz, F. Dias, P. Aaby, K. Mølbak, and H. Sommerfelt. 2003. Cohort study of Guinean children: incidence, pathogenicity, conferred protection, and attributable risk for enteropathogens during the first 2 years of life. J. Clin. Microbiol. 41:4238-4245.
59. van Loon, F. P. L., J. D. Clemens, J. Chakraborty, M. R. Rao, B. A. Kay, D. A. Sack, M. Yunus, M. Ali, A. M. Svennerholm, and J. Holmgren. 1996. Field trial of inactivated oral cholera vaccines in Bangladesh: results from 5 years of follow-up. Vaccine 14:162-166.
60. Waldman, S. A., and P. O'Hanley. 1989. Influence of a glycine or proline substitution on the functional properties of a 14-amino-acid analog of Escherichia coli heat-stable enterotoxin. Infect. Immun. 57:2420-2424.
61. Walker, R. I., D. Steele, T. Aguado, and the Ad Hoc ETEC Technical Expert Committee. 2007. Analysis of strategies to successfully vaccinate infants in developing countries against enterotoxigenic E. coli (ETEC) disease. Vaccine 25:2545-2566.
62. Wolf, M. K. 1997. Occurrence, distribution, and associations of O and H serogroups, colonization factor antigens, and toxins of enterotoxigenic Escherichia coli. Clin. Microbiol. Rev. 10:569-584.
63. World Health Organization. 2006. Future directions for research on enterotoxigenic Escherichia coli vaccines for developing countries. Wkly. Epidemiol. Rec. 81:97.
64. Wraith, D. C., M. Goldman, and P. H. Lambert. 2003. Vaccination and autoimmune disease: what is the evidence? Lancet 362:1659-1666.
65. Wu, C.-M., and T.-C. Chung. 2007. Mice protected by oral immunization with Lactobacillus reuteri secreting fusion protein of Escherichia coli enterotoxin subunit protein. FEMS Immunol. Med. Microbiol. 50:354-365.
66. Yamanaka, H., M. Kameyama, T. Baba, Y. Fujii, and K. Okamoto. 1994. Maturation pathway of Escherichia coli heat-stable enterotoxin I: requirement of DsbA for disulfide bond formation. J. Bacteriol. 176:2906-2913. (Pubitemid 24152936)
67. Yamanaka, H., T. Nomura, Y. Fujii, and K. Okamoto. 1997. Extracellular secretion of Escherichia coli heat-stable enterotoxin I across the outer membrane. J. Bacteriol. 179:3383-3390. (Pubitemid 27232971)
68. Yamanaka, H., T. Nomura, Y. Fujii, and K. Okamoto. 1998. Need for TolC, an Escherichia coli outer membrane protein, in the secretion of heat-stable enterotoxin I across the outer membrane. Microb. Pathog. 25:111-120.
69. Yamanaka, H., T. Nomura, and K. Okamoto. 1998. Involvement of glutamic acid residue at position 7 in the formation of the intramolecular disulfide bond of Escherichia coli heat-stable enterotoxin Ip in vivo. Microb. Pathog. 24:145-154.
70. Yamanaka, H., and K. Okamoto. 2000. Mutation of aromatic amino acid residues located at the amino- and carboxy-termini of Escherichia coli heat-stable enterotoxin Ip reduces the efficiency of the toxin to cross the outer membrane. Microbiol. Immunol. 44:481-488.
71. Yamasaki, S., T. Sato, Y. Hidaka, H. Ozaki, H. Ito, T. Hirayama, Y. Takeda, T. Sugimura, A. Tai, and Y. Shimonishi. 1990. Structure-activity relationship of Escherichia coli heat-stable enterotoxin: role of Ala residue at position 14 in toxin-receptor interaction. Bull. Chem. Soc. Jpn. 63:2063-2070.
72. Yoshimura, S., H. Ikemura, H. Watanabe, S. Aimoto, Y. Shimonishi, S. Hara, T. Takeda, T. Miwatani, and Y. Takeda. 1985. Essential structure for full enterotoxigenic activity of heat-stable enterotoxin produced by enterotoxigenic Escherichia coli. FEBS Lett. 181:138-142. (Pubitemid 15127989)
73. Zhang, W., C. Zhang, D. H. Francis, Y. Fang, D. Knudsen, J. P. Nataro, and D. C. Robertson. 2010. Genetic fusions of LTAB and STa toxoids of porcine enterotoxigenic Escherichia coli (ETEC) elicited neutralizing anti-LT and anti-STa antibodies. Infect. Immun. 78:316-325.
74. Zheng, J. P., Z. S. Zhang, S. Q. Li, X. X. Liu, S. L. Yuan, P. Wang, D. W. Zhan, L. C. Wang, and C. F. Huang. 2005. Construction of a novel Shigella live-vector strain coexpressing CS3 and LTB/STm of enterotoxigenic E.coli. World J. Gastroenterol. 11:3411-3418.