Modified Heat-stable toxins (hSTa) of enterotoxigenic Escherichia coli lose toxicity but display antigenicity after being genetically fused to heat-labile toxoid LT(R192G)

Toxins

Volumn 3, Issue 9, 2011, Pages 1146-1162

  Liu, Mei ^a   Zhang, Chengxian ^a   Mateo, Kristy ^a   Nataro, James P ^b   Robertson, Donald C ^c   Zhang, Weiping ^a  

^a SOUTH DAKOTA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

^c KANSAS STATE UNIVERSITY   (United States)

Author keywords

Diarrhea; ETEC; LT STa toxoid fusion; STa toxin; Toxoid; Vaccine

Indexed keywords

BACTERIUM ANTIBODY; ESCHERICHIA COLI ENTEROTOXIN; ESCHERICHIA COLI VACCINE; HEAT LABILE ENTEROTOXIN; HEAT LABILE HEAT STABLE TOXOID FUSION; HEAT STABLE ENTEROTOXIN; HYBRID PROTEIN; IMMUNOGLOBULIN G ANTIBODY; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ANIMAL EXPERIMENT; ANTIBODY BLOOD LEVEL; ANTIBODY TITER; ANTIGENICITY; ARTICLE; BACTERIAL STRAIN; CONTROLLED STUDY; ENTEROTOXIGENIC ESCHERICHIA COLI; GENE FUSION; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN STRUCTURE; STRUCTURAL HOMOLOGY; TOXICITY;

ANIMALS; ANTIBODIES; ANTIGENS; BACTERIAL TOXINS; ENTEROTOXIGENIC ESCHERICHIA COLI; ENTEROTOXINS; ESCHERICHIA COLI INFECTIONS; ESCHERICHIA COLI PROTEINS; ESCHERICHIA COLI VACCINES; FEMALE; INTESTINES; MICE; MICE, INBRED BALB C; PEPTIDES; RECOMBINANT FUSION PROTEINS; SWINE;

ANIMALIA; ESCHERICHIA COLI; MUS; SUS;

EID: 80053181078     PISSN: None     EISSN: 20726651     Source Type: Journal    
DOI: 10.3390/toxins3091146     Document Type: Article

References (51)

1. Black, R.E.; Cousens, S.; Johnson, H.L.; Lawn, J.E.; Rudan, I.; Bassani, D.G.; Jha, P.; Campbell, H.; Walker, C.F.; Cibulskis, R.; et al. Global, regional, and national causes of child mortality in 2008: A systematic analysis. Lancet 2010, 375, 1969-1987.
2. Wardlaw, T.; Salama, P.; Brocklehurst, C.; Chopra, M.; Mason, E. Diarrhoea: Why children are still dying and what can be done. Lancet 2010, 376, 63-67.
3. World Health Organization (WHO). Diarrhoeal Diseases; WHO: Geneva, Switzerland, Updated February 2009.
4. Black, E. Epidemiology of travelers, diarrhea and relative importance of various pathogens. Rev. Infect. Dis. 1990, 1, S73-S79.
5. Northey, G.; Evans, M.R.; Sarvotham, T.S.; Thomas, D.R.; Howard, T.J. Sentinel surveillance for travellers' diarrhoea in primary care. BMC Infect. Dis. 2007, 7, 126.
6. Alexander, T.J.L. Neonatal Diarrhoea in Pigs. In Escherichia coli in Domestic Animals and Humans; Gyles, C.L., Ed.; CAB International: Oxon, UK, 1994; pp. 151-170.
7. Moon, H.W. Colonization factor antigens of enterotoxigenic Escherichia coli in animals. Curr. Topics Microbiol. Immunol. 1990, 151, 147-165.
8. Moon, H.W.; Bunn, T.O. Vaccines for preventing enterotoxigenic Escherichia coli infections in farm animals. Vaccine 1993, 11, 213-220.
9. Smith, H.W.; Linggood, M.A. Observation on the pathogenic properties of the K88, HIY and ENT plasmids of Escherichia coli with particular reference to porcine diarrhea. J. Med. Microbiol. 1971, 4, 467-485.
10. Nataro, J.P.; Kaper, J.B. Diarrheagenic Escherichia coli. Clin. Microbiol. Rev. 1998, 11, 142-201.
11. Berberov, E.M.; Zhou, Y.; Francis, D.H.; Scott, M.A.; Kachman, S.D.; Moxley, R.A. Relative importance of heat labile enterotoxin in the causation of severe diarrheal disease in the gnotobiotic piglet model by a strain of enterotoxigenic Escherichia coli that produces multiple enterotoxins. Infect. Immun. 2004, 72, 3914-3924.
12. Zhang, W.; Berberov, E.M.; Freeling, J.; He, D.; Moxley, R.A.; Francis, D.H. Significance of heat-stable and heat-labile enterotoxins in porcine colibacillosis, in an additive model for pathogenicity studies. Infect. Immun. 2006, 76, 3107-3114.
13. Hughs, J.M.; Murad, F.; Chang, B.; Guerrant, R.L. Role of cyclic GMP in the action of heat-stable enterotoxin of Escherichia coli. Nature 1978, 271, 755-756.
14. Moon, H.W. Mechanisms in the pathogenesis of diarrhea: A review. J. Am. Vet. Med. Assoc. 1978, 172, 443-448.
15. Wolf, M.K. Occurrence, distribution, and associations of O and H serogroups, colonization factor antigens, and toxin of enterotoxigenic Escherichia coli. Clin. Microbiol. Rev. 1997, 10, 569-584.
16. Girard, M.P.; Steele, D.; Chaignat, C.L.; Kieny, M.P. A review of vaccine research and development: Human enteric infections. Vaccine 2006, 24, 2732-2750.
17. Zhang, W.; Robertson, D.C.; Zhang, C.; Bai, W.; Zhao, M.; Francis, D.H. Escherichia coli constructs expressing human or porcine enterotoxins induce identical diarrheal diseases in a piglet infection model. Appl. Environ. Microbiol. 2008, 74, 5832-5837.
18. Boedeker, E.C. Vaccines for enterotoxigenic Escherichia coli: Current status. Curr. Opin. Gastroenterol. 2005, 21, 15-19.
19. Walker, R.I. Considerations for development of whole cell bacterial vaccines to prevent diarrheal diseases in children in developing countries. Vaccine 2005, 23, 3369-3385.
20. Walker, R.I.; Steele, D.; Aguado, T. The Ad Hoc ETEC Technical Expert Committee. Analysis of strategies to successfully vaccinate infants in developing countries against enterotoxigenic E. coli (ETEC) disease. Vaccine 2007, 25, 2545-2566.
21. Taxt, A.; Aasland, R.; Sommerfelt, H.; Nataro, J.; Puntervoll, P. Heat-stable enterotoxin of enterotoxigenic Escherichia coli as a vaccine target. Infect. Immun. 2010, 78, 1824-1831.
22. Franz, J.C.; Mellencamp, M.W. Production and Testing of Escherichia coli (LTb) Toxoid. In Proceedings of Fourth International Symposium on Neonatal Diarrhea, Saskatchewan, S.K., Canada, 3-5 October 1983; Acres, S., Ed.; pp. 500-517.
23. Frantz, J.C.; Robertson, D.C. Immunological properties of Escherichia coli heat-stable enterotoxins: development of a radioimmunoassay specific for heat-stable enterotoxins with suckling mouse activity. Infect. Immun. 1981, 33, 193-198.
24. Clements, J.D. Construction of a nontoxic fusion peptide for immunization against Escherichia coli strains that produce heat-labile and heat-stable enterotoxins. Infect. Immun. 1990, 58, 1159-1166.
25. Chong, C.; Frigerg, M.; Clements, J.D. LT(R192G), a non-toxic mutant of the heat-labile enterotoxin of Escherichia coli, elicits enhanced humeral and cellular immune responses associated with protection against lethal oral challenge with Salmonella spp. Vaccine 1998, 16, 732-740.
26. 192) and heat-stable toxin b (STb) of porcine enterotoxigenic Escherichia coli elicit protective anti-LT and anti-STb antibodies. Clin. Vaccine Immun. 2010, 17, 1223-1231.
27. Cardenase-Freytag, L.; Cheng, E.; Mayeux, P.; Domer, J.E.; Clements, J.D. Effectiveness of a vaccine composed of heat-killed Candida albicans and a novel mucosal adjuvant, LT(R192G), against systemic candidiasis. Infect. Immun. 1999, 67, 826-833.
28. Lemere, C.A.; Spooner, E.T.; Leverone, J.F.; Mori, C.; Clements, J.D. Intranasal immunotherapy for the treatment of Alzheimer's disease: Escherichia coli LT and LT(R192G) as mucosal adjuvants. Neurobiol. Ageing 2002, 23, 991-1000.
29. Van Cott, J.L.; Prada, A.E.; McNeal, M.M.; Stone, S.C.; Basu, M.; Huffer, B., Jr.; Smiley, K.L.; Shao, M.; Bean, J.A.; Clements, J.D.; et al. Mice develop effective but delayed protective immune responses when immunized as neonates either intranasally with nonliving VP6/LT(R192G) or orally with live Rhesus rotavirus vaccine candidates. J. Virol. 2006, 80, 4949-4961.
30. Choi, A.H.; Smiley, C.K.; Basu, M.; McNeal, M.M.; Shao, M.; Bean, J.A.; Clements, J.D.; Stout, R.R.; Ward, R.L. Protection of mice against rotavirus challenge following intradermal DNA immunization by biojector needle-free injection. Vaccine 2007, 25, 3215-3218.
31. Smiley, K.L.; McNeal, M.M.; Basu, M.; Choi, A.H.; Clements, J.D.; Ward, R.L. Association of Gamma interferon and interleukin-17 production in intestinal CD4 T cells with protection against rotavirus shedding in mice intranasally immunized with VP6 and the adjuvant LT(R192G). J. Virol. 2007, 81, 3740-3748.
32. McNeal, M.M.; Basu, M.; Bean, J.A.; Clements, J.D.; Lycke, N.Y.; Ramme, A.; Lowenadler, B.; Choi, A.H.; Ward, R.L. Intrarectal immunization of mice with VP6 and either LT(R192G) or CTA1-DD as adjuvant protects against fecal rotavirus shedding after EDIM challenge. Vaccine 2007, 25, 6224-6231.
33. Yamasaki, S.; Ito, H.; Hirayama, T.; Takeda, Y.; Shimonishi, Y. Effects on the Activity of Amino Acids Replacement at Positions 12, 13, and 14 Heat-Stable Enterotoxin (STh) by Chemical Synthesis. In Proceedings of 24th Joint Conference U.S.-Japan Cooperative Medical Science Program on Cholera and Related Diarrheal Disease Panel, Tokyo, Japan, 1988; p. 42.
34. Hirayama, T. Heat-Stable Enterotoxin of Escherichia coli. In Bacterial Toxins and Virulence Factors in Disease; Moss, J., Iglewski, B., Vaughan, M., Tu, A.T., Eds.; Marcel Dekker, Inc.: New York, NY, USA, 1995; pp. 281-296.
35. Zhang, W.; Zhang, C.; Francis, D.H.; Fang, Y.; Knudsen, D.; Nataro, J.P.; Robertson, D.C. 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, 316-325.
36. Zhang, C.; Zhang, W. Escherichia coli K88ac fimbriae expressing heat-labile and heat-stable toxin epitopes elicit antibodies that neutralize cholera toxin and STa toxin and inhibit adherence of K88ac fimbrial E. coli. Clin. Vaccine Immunol. 2010, 17, 1859-1867.
37. Osaki, H.; Sato, T.; Kubata, H.; Hata, Y.; Katsube, Y.; Shimonishi, Y. Moleuclar 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. 1991, 266, 5934-5941.
38. Ausubel, F.M.; Brent, R.; Kingston, R.K.; Moore, D.D.; Seidman, J.G.; Smith, J.A.; Struhl, K. Short Protocols in Molecular Biology, 4th ed.; John Wiley & Sons, Inc.: New York, NY, USA, 1999; pp. 1-29.
39. Lockwood, D.E.; Robertson, D.C. Development of a competitive enzyme-linked immunosorbent assay (ELISA) for Escherichia coli heat-stable enterotoxin (STa). J. Immunol. Meth. 1984, 75, 293-307.
40. National Research Council. Guide for the Care and Use of Laboratory Animals; National Academy Press: Washington, DC, USA, 1996.
41. Sanchez, J.; Uhlin, B.E.; Grundstrom, T.; Holmgren, J.; Hirst, T.R. Immunoactive chimeric ST-LT enterotoxins of Escherichia coli generated by in vitro gene fusion. FEBS Lett. 1986, 8, 194-198.
42. Stevens, L.A.; Moss, J.; Vaughan, M.; Pizza, M.; Rappuoli, R. Effects of site-directed mutagenesis of Escherichia coli heat-labile enterotoxin on ADP-ribosyltranferase activity and interaction with ADP-ribosylation factors. Infect. Immun. 1999, 67, 259-265.
43. Svennerholm, A.M.; Holmgren, J. Immunity to Enterotoxin-Producing Bacteria. In Immunology of Gastrointestinal Disease; MacDonald, T.T., Ed.; Kluwer Academic Publishers: Dordrecht, the Netherlands, 1992; pp. 227-246.
44. Guidry, J.J.; Cardenas, L.; Cheng, E.; Clements, J.D. Role of receptor binding in toxicity, immunogenicity, and adjuvanticity of Escherichia coli heat-labile enterotoxin. Infect. Immun. 1997, 65, 4943-4950.
45. Stevens, L.A.; Moss, J.; Vaughan, M.; Pizza, M.; Rappuoli, R. Effects of site-directed mutagenesis of Escherichia coli heat-labile enterotoxin on ADP-ribosyltranferase activity and interaction with ADP-ribosylation factors. Infect. Immun. 1999, 67, 259-265.
46. Ryan, E.J.; McNeela, E.; Murphy, G.A.; Stewart, H.; O'Hagan, D.; Pizza, M.; Rappuoli, R.; Mills, K.H. Mutants of Escherichia coli heat-labile toxin act as effective mucosal adjuvants for nasal delivery of an cellular pertussis vaccine: Differential effects of the nontoxic AB complex and enzyme activity on Th1 and Th2 cells. Infect. Immun. 1999, 67, 6270-6280.
47. Sato, T.; Shimonishi, Y. Structural features of Escherichia coli heat-stable enterotoxin that activates membrane-associated guanylyl cyclase. J. Peptide Res. 2004, 63, 200-206.
48. Okamoto, K.; Okamoto, K.; Yukitake, J.; Kawamoto, Y.; Miyama, A. Substitutions of cycteine residues of Escherichia coli heat-stable enterotoxin by oligonucleotide-directed mutagenesis. Infect. Immun. 1987, 55, 2121-2125.
49. Svennerholm, A.M.; Lindblad, M.; Svennerholm, B.; Holmgren, J. Synthesis of nontoxic, antibody binding Escherichia coli heat-stable enterotoxin (STa) peptide. FEMS Microbiol. Lett. 1988, 55, 23-28.
50. Kubota, H.; Hidaka, Y.; Ozaki, H.; Ito, H.; Hirayama, T.; Takeda, Y.L.; Shimonishi, Y. A long acting heat-stable enterotoxin of ETEC with a single D-amino acid. Biochem. Biophys. Res. Commun. 1989, 161, 229-235.
51. Wolf, H.R.; Waldman, S.A. A comparative molecular field analysis (COMFA) of the structural of heat-stable enterotoxins mediating activation of guanylye cyclase C. J. Med. Chem. 2002, 45, 1731-1734.