Chapter 4 : Detection of Toxins of O1 and Non-O1

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Although cellular components are involved in the pathogenesis of cholera in ways not yet clearly discerned, the pathogenicity of serovar O1 is largely due to the synthesis of an exotoxin that triggers the secretion of water and electrolytes into the small intestine. This chapter provides a historical and practical perspective on the variety of biological, tissue culture, immunologic, and enzymatic assays developed for detection of O1 and non-O1 toxins. The microtiter plate-based GM ganglioside enzyme-linked immunosorbent assay (ELISA) was developed to detect heat-labile enterotoxin (LT) and cholera toxin and was based on the specific binding of these toxins to polystyrene-adsorbed GM ganglioside and subsequently to enzyme to demonstrate the presence of the bound toxin by immunologic means. This assay could detect cholera toxin and other bacterial protein toxins within several hours in standard test tubes. The entero-toxin-binding effect of free gangliosides present in mucin found in stools is probably an important reason for the low or undetectable levels of enterotoxins in stools. Monoclonal antibodies against STh and STp are valuable and sensitive reagents used in the development of immunoassays for heat-stable enterotoxins. A variety of methods for detection of cholera toxin and other toxins elaborated by Ol and non-Ol strains have evolved over the last decades.

Citation: Nair G, Takeda Y. 1994. Detection of Toxins of O1 and Non-O1, p 53-67. In Wachsmuth I, Blake P, Olsvik Ø (ed), and Cholera. ASM Press, Washington, DC. doi: 10.1128/9781555818364.ch4

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Cholera Toxin
Heat-Labile Enterotoxin
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1. Aimoto, S.,, T. Takao,, Y. Shimonishi,, S. Hara,, T. Takeda,, Y. Takeda,, and T. Miwatani. 1982. Amino-acid sequence of a heat-stable enterotoxin produced by human enterotoxigenic Escherichia coli. Eur. J. Biochem. 129:257263.
2. Almeida, R. J.,, F. W. Hickman-Brenner,, E. G. Sowers,, N. D. Puhr,, J. J. Farmer m,, and I. K. Wachsmuth. 1990. Comparison of a latex agglutination assay and an enzyme-linked immunosorbent assay for detecting cholera toxin. J. Clin. Microbiol. 28:128130.
3. Arita, M.,, T. Takeda,, T. Honda,, and T. Miwatani. 1986. Purification and characterization of Vibrio cholerae non-Ol heat-stable enterotoxin. Infect. Immun. 52:4549.
4. Baselski, V.,, R. Briggs,, and C. Parker. 1977. Intestinal fluid accumulation induced by oral challenge with Vibrio cholerae or cholera toxin in infant mice. Infect. Immun. 15:704712.
5. Baudry, B.,, A. Fasano,, J. Ketley,, and J. B. Kaper. 1992. Cloning of a gene (zot) encoding a new toxin produced by Vibrio cholerae. Infect. Immun. 60:428434.
6. Bhadra, R. K.,, T. Biswas,, S. C. Pal,, T. Takeda,, and G. B. Nair. 1991. A polyclonal-monoclonal antibody based sensitive sandwich enzyme-linked immunosorbent assay for specific detection of cholera toxin. Zentralbl. Bakteriol. 275:467473.
7. Blachman, T. J.,, S. J. Goss,, and M. J. Pickett. 1974. Experimental cholera in the chinchilla. J. Infect. Dis. 129:376384.
8. Brill, B. M,, B. L. Wasilauskas,, and S. H. Richardson. 1979. Adaptation of the staphylococcal coagglutination technique for detection of heat-labile enterotoxin of Escherichia coli. J. Clin. Microbiol. 9:4955.
9. Ceska, M.,, F. Effenberger,, and F. Grossmiiller. 1978. Highly sensitive solid-phase radioimmunoassay suitable for determination of low amounts of cholera toxin and cholera toxin antibodies. J. Clin. Microbiol. 7:209213.
10. Chaicumpa, W.,, and D. Rowley. 1972. Experimental cholera in infant mice: protective effects of antibody. J. Infect. Dis. 125:480485.
11. Clements, J. D.,, and R. A. Finkelstein. 1979. Isolation and characterization of homogeneous heat-labile enterotoxins with high specific activity from Escherichia coli cultures. Infect. Immun. 24:760769.
12. Craig, J. P. 1965. A permeability factor (toxin) found in cholera stools and culture filtrates and its neutralization by convalescent cholera sera. Nature (London) 207:614616.
13. Craig, J. P. 1966. Preparation of the vascular permeability factor of Vibrio cholerae. J. Bacteriol. 92:793795.
14. Craig, J. P., 1985. The vibrio diseases in 1982: an overview, p. 1123. In Y. Takeda, and T. Miw-atani (ed.), Bacterial Diarrheal Diseases. KTK Scientific Publishers, Tokyo.
15. Craig, J. P.,, K. Yamamoto,, Y. Takeda,, and T. Miwatani. 1981. Production of cholera-like enterotoxin by a Vibrio cholerae non-O1 strain isolated from the environment. Infect. Immun. 34:9097.
16. Cuatrecasas, P. 1973. Gangliosides and membrane receptors for cholera toxin. Biochemistry 12:35583566.
17. De, S. N. 1959. Enterotoxicity of bacteria-free culture-filtrate of Vibrio cholerae. Nature (London) 183:15331534.
18. De, S. N.,, and D. N. Chatterje. 1953. An experimental study of the mechanism of action of Vibrio cholerae on the intestinal mucous membrane. J. Pathol. Bacteriol. 66:559562.
19. De, S. N.,, M. L. Ghose,, and A. Sen. 1960. Activities of bacteria-free preparations from Vibrio cholerae. J. Pathol. Bacteriol. 79:373380.
20. Dean, A. G.,, Y.-C. Ching,, R. G. Williams,, and L. B. Harden. 1972. Test for Escherichia coli enterotoxin using infant mice: application in a study of diarrhea in children in Honolulu. J. Infect. Dis. 125:407411.
21. DeMol, P.,, W. Hemelhof,, P. Retort,, T. Takeda,, T. Miwatani,, Y. Takeda,, and J. P. Butzler. 1985. A competitive immunosorbent assay for the detection of heat-stable enterotoxin of Escherichia coli. J. Med. Microbiol. 20:6974.
22. Donta, S. T.,, M. King,, and K. Sloper. 1973. Induction of steroidogenesis in tissue culture by cholera enterotoxin. Nature (London) New Biol. 243:246247.
23. Donta, S. T.,, H. W. Moon,, and S. C. Whipp. 1974. Detection of heat-labile Escherichia coli enterotoxin with the use of adrenal cells in tissue culture. Science 183:334336.
24. Donta, S. T.,, and D. M. Smith. 1974. Stimulation of steroidogenesis in tissue culture by enterotoxigenic Escherichia coli and its neutralization by specific antiserum. Infect. Immun. 9:500505.
25. Dubey, R. S.,, M. Lindblad,, and J. Holmgren. 1990. Purification of El Tore cholera enterotoxins and comparisons with classical toxin. J. Gen. Microbiol. 136:18391847.
26. Dutt, A. R. 1965. Enterotoxic activity in cholera stool. Indian J. Med. Res. 53:605609.
27. Dutta, N. K.,, and M. K. Habbu. 1955. Experimental cholera in infant rabbits: a method for che-motherapeutic investigation. Br. J. Pharmacol. Chemother. 10:153159.
28. Echeverria, P.,, L. Verheart,, C. V. Ulyanco,, and L. T. Santiago. 1978. Detection of heat-labile enterotoxin-like activity in stools of patients with cholera and Escherichia coli diarrhea. Infect. Immun. 19:343344.
29. Engvall, E.,, and P. Perlmann. 1972. Enzyme-linked immunosorbent assay, ELISA. III. Quantitation of specific antibodies by enzyme-labeled anti-immunoglobulin in antigen-coated tubes. J. Immunol. 109:129135.
30. Evans, D. J., Jr.,, and D. G. Evans. 1977. Direct serological assay for the heat-labile enterotoxin of Escherichia coli, using passive immune hemolysis. Infect. Immun. 16:604609.
31. Fasano, A.,, B. Baudry,, D. W. Pumplin,, S. S. Wasserman,, B. D. Tall,, J. M. Ketley,, and J. B. Kaper. 1991. Vibrio cholerae produces a second enterotoxin, which affects intestinal tight junctions. Proc. Natl. Acad. Sci. USA 88:52425246.
32. Felsenfeld, O.,, W. E. Greer,, and A. D. Felsen-feld. 1967. Cholera toxin neutralization and some cellular sites of immune globulin formation in Cercopithecus aethiops. Nature (London) 213:12491251.
33. Field, M.,, D. Fromm,, and I. McColl. 1971. Ion transport in rabbit ileal mucosa. I. Na and CI fluxes and short circuit current. Am. J. Physiol. 220:13881396.
34. Finkelstein, R. A.,, R Atthasampunna,, M. Chulasamaya,, and R Charunmethee. 1966. Pathogenesis of experimental cholera: biologic activities of purified procholeragen A. J. Immunol. 96:440449.
35. Finkelstein, R. A.,, and J. J. LoSpalluto. 1969. Pathogenesis of experimental cholera: preparation and isolation of choleragen and choleragenoid. J. Exp. Med. 130:185202.
36. Finkelstein, R. A.,, H. T. Norris,, and N. K. Dutta. 1964. Pathogenesis of experimental cholera in infant rabbits. I. Observations on the intra-intestinal infection and experimental cholera produced with cell-free products. J. Infect. Dis. 114:203216.
37. Finkelstein, R. A.,, and J. W. Peterson. 1970. In vitro detection of antibody to cholera enterotoxin in cholera patients and laboratory animals. Infect. Immun. 1:2129.
38. Germani, Y.,, E. Begaud,, J. L. Guesdon,, J. P. Moreau. 1987. Assay of Vibrio cholerae/Escherichia coli heat-labile enterotoxin by inhibition of erythroadsorption on the GM, ganglioside. Ann. Inst. Pasteur Microbiol. 138:223234.
39. Gorbach, S. L.,, and C. M. Khurana. 1972. Toxigenic Escherichia coli: a cause of infantile diarrhea in Chicago. N. Engl. J. Med. 287:791795.
40. Greenberg, H. B.,, D. A. Sack,, W. Rodriguez,, R. B. Sack,, R. G. Wyatt,, A. R. Kalica,, R. L. Horswood,, R. M. Chanock,, and A. Z. Ka-pikian. 1977. Microtiter solid-phase radioimmunoassay for detection of Escherichia coli heat-labile enterotoxin. Infect. Immun. 17:541545.
41. Guentzel, M. N.,, and L. J. Berry. 1975. Motility as a virulence factor for Vibrio cholerae. Infect. Immun. 11:890897.
42. Guerrant, R. L.,, L. L. Brunton,, T. C. Schnait-man,, L. I. Rebhun,, and A. G. Gilman. 1974. Cyclic adenosine monophosphate and alteration of Chinese hamster ovary cell morphology: a rapid, sensitive in vitro assay for the enterotoxins of Vibrio cholerae and Escherichia coli. Infect. Immun. 10:320327.
43. Guerrant, R. L.,, L. C. Chen,, and G. W. G. Sharp. 1972. Intestinal adenyl-cyclase activity in canine cholera: correlation with fluid accumulation. J. Infect. Dis. 125:377381.
44. Hejtmancik, K. E.,, J. W. Peterson,, D. E. Markel,, and A. Kurosky. 1977. Radioimmunoassay for the antigenic determinants of cholera toxin and its components. Infect. Immun. 17:621628.
45. Holmgren, J. 1973. Comparison of the tissue receptors for Vibrio cholerae and Escherichia coli enterotoxins by means of gangliosides and natural cholera toxoid. Infect. Immun. 8:851859.
46. Holmgren, J.,, I. Lonnroth,, and L. Sven-nerholm. 1973. Fixation and inactivation of cholera toxin by GM, ganglioside. Scand. J. Infect. Dis. 5:7778.
47. Holmgren, J.,, and A.-M. Svennerholm. 1973. Enzyme-linked immunosorbent assays for cholera serology. Infect. Immun. 7:759763.
48. Honda, T.,, and R. A. Finkelstein. 1979. Selection and characteristics of a Vibrio cholerae mutant lacking the A (ADP-ribosylating) portion of the cholera enterotoxin. Proc. Natl. Acad. Sci. USA 76:20522056.
49. Ichinose, Y.,, K. Yamamoto,, N. Nakasone,, M. J. Tanabe,, T. Takeda,, T. Miwatani,, and M. Iwanaga. 1987. Enterotoxicity of El Tor-like hemolysin of non-Ol Vibrio cholerae. Infect. Immun. 55:10901093.
50. Ishikawa, E.,, M. Imagawa,, and S. Hashida,. 1983. Ultrasensitive enzyme immunoassay using fluorogenic, luminogenic, radioactive and related substrates and factors to limit the sensitivity, p. 219232. In S. Avrameas,, P. Duret,, R. Mas-seyeff,, and G. Geldmann (ed.), Immunoenzymatic Techniques. Elsevier Science Publishers B. V., Amsterdam.
51. Ito, T.,, S. Kuwahara,, and T. Yokota. 1983. Automatic and manual latex agglutination tests for measurement of cholera toxin and heat-labile enterotoxin of Escherichia coli. J. Clin. Microbiol. 17:712.
52. Iwanaga, M.,, and T. Kuyyakanond. 1987. Large production of cholera toxin by Vibrio cholerae Ol in yeast extract peptone water. J. Clin. Microbiol. 25:23142316.
53. Iwanaga, M.,, and K. Yamamoto. 1985. New medium for the production of cholera toxin by Vibrio cholerae O1 biotype El Tor. J. Clin. Microbiol. 22:405408.
54. Iwanaga, M.,, K. Yamamoto,, N. Higa,, Y. Ichinose,, N. Nakasone,, and M. Tanabe. 1986. Culture conditions for stimulating cholera toxin production by Vibrio Cholerae O1 El Tor. Microbiol. Immunol. 30:10751083.
55. Johnson, J. A.,, J. G. Morris, Jr.,, and J. B. Kaper. 1993. Gene encoding zonula occludens toxin (zot) does not occur independently from cholera enterotoxin genes (etc) in Vibrio cholerae. J. Clin. Microbiol. 31:732733.
56. Kantor, H. S.,, P. Tao,, and S. L. Gorbach. 1974. Stimulation of intestinal adenyl cyclase by Escherichia coli enterotoxin: comparison of strains from an infant and an adult with diarrhea. J. Infect. Dis. 129:19.
57. Kaper, J. B.,, H. B. Bradford,, N. C. Roberts,, and S. Falkow. 1982. Molecular epidemiology and Vibrio cholerae in the U.S. gulf coast. J. Clin. Microbiol. 16:129134.
58. Kaper, J. B.,, H. Lockman,, M. M. Baldini,, and M. M. Levine. 1984. Recombinant live oral cholera vaccine. Bio/Technology 2:345349.
59. Kaper, J. B.,, H. Lockman,, M. M. Baldini,, and M. M. Levine. 1984. Recombinant nontox-inogenic Vibrio cholerae strains as attenuated cholera vaccines candidates. Nature (London) 308:655658.
60. Karasawa, T.,, T. Mihara,, H. Kurazono,, G. B. Nair,, S. Garg,, T. Ramamurthy,, and Y. Takeda. 1993. Distribution of the zot (zonula occludens toxin) gene among strains of Vibrio cholerae O1 and non-O1. FEMS Microbiol. Lett. 106:143146.
61. Kasai, G. J.,, and W. Burrows. 1966. The titration of cholera toxin and antitoxin in the rabbit ileal loop. J. Infect. Dis. 116:606614.
62. Koch, R. 1919. Erste Konferenz zur Eroterung derCholerafrage am 26 Juli 1884 in Berlin, p. 2060. In Gesammelte Werke von Robert Koch, 2er Band, lste Teil. Verlag von Georg Thieme, Leipzig, Gremany.
63. Kusama, H.,, and J. R Craig. 1970. Production of biologically active substances by two strains of Vibrio cholerae. Infect. Immun. 1:8087.
64. Levine, M. M.,, J. B. Kaper,, D. Herrington,, G. Losonsky,, J. G. Morris,, M. L. Clemets,, R. E. Black,, B. Tall,, and R. Hall. 1988. Volunteer studies of deletion mutants of Vibrio cholerae O1 prepared by recombinant techniques. Infect. Immun. 56:161167.
65. Levner, M.,, E. P. Wiener,, and B. A. Rubin. 1977. Induction of Escherichia coli and Vibrio cholerae enterotoxins by an inhibitor of protein synthesis. Infect. Immun. 15:132137.
66. Lindholm, L.,, J. Holmgren,, M. Wikstrdm,, U. Karlsson,, K. Andersson,, and N. Lycke. 1983. Monoclonal antibodies to cholera toxin with special references to cross-reactions with Escherichia coli heat-labile enterotoxin. Infect. Immun. 40:570576.
67. Maneval, D. R.,, R. R. Colwell,, S. W. Joseph,, R. Grays,, and S. T. Donta. 1980. A tissue culture method for the detection of bacterial enterotoxins. J. Tissue Culture Methods 6:8590.
68. Merson, M. H.,, R. H. Yolken,, R. B. Sack,, J. L. Froehlich,, H. B. Greenberg,, I. Huq,, and R. W. Black. 1980. Detection of Escherichia coli enterotoxins in stools. Infect. Immun. 29:108113.
69. Minami, A.,, S. Hashimoto,, H. Abe,, M. Arita,, T. Taniguchi,, T. Honda,, T. Miwatani,, and M. Nishibuchi. 1991. Cholera enterotoxin production in Vibrio cholerae O1 strains isolated from the environment and from humans in Japan. Appl. Environ. Microbiol. 57:21522157.
70. Morgan, D. R.,, H. L. DuPont,, L. V. Wood,, and C. D. Ericsson. 1983. Comparison of methods to detect Escherichia coli heat-labile enterotoxin in stool and cell-free culture superna-tants. J. Clin. Microbiol. 18:798802.
71. Morris, J. G., Jr.,, T. Takeda,, B. D. Tall,, G. A. Losonsky,, S. K. Bhattacharya,, B. D. Forrest,, B. A. Kay,, and M. Nishibuchi. 1990. Experimental non-O group 1 Vibrio cholerae gastroenteritis in humans. J. Clin. Invest. 85:697705.
72. Nair, G. B.,, S. K. Bhattacharya,, and T. Takeda. 1993. Identification of heat-stable en-terotoxin-producing strains of Yersinia enterocolitica and Vibrio cholerae non-Ol by a monoclonal antibody-based enzyme-linked immunosorbent assay. Microbiol. Immunol. 37:181186.
73. Nair, G. B.,, Y. Oku,, Y. Takeda,, A. Ghosh,, R. K. Ghosh,, S. Chattopadhyay,, S. C. Pal,, J. B. Kaper,, and T. Takeda. 1988. Toxin profiles of Vibrio cholerae non-O1 from environmental sources in Calcutta, India. Appl. Environ. Microbiol. 54:31803182.
74. Nair, G. B.,, A. Pal,, R. K. Bhadra,, S. Misra,, P. Das,, P. P. Chaudhuri,, and S. C. Pal. 1989. Production, subunit specificity and neutralizing activity of murine monoclonal antibodies to cholera toxin, p. 141145. In Proceedings of the Indo-U.K. Workshop on Diarrhoeal Diseases, Calcutta, India. National Institute of Cholera and Enteric Diseases, Indian Medical Council.
75. Narayanan, J.,, P. A. Hartman,, and D. J. Graves. 1989. Assay of heat-labile enterotoxins by their ADP-ribosyltransferase activities. J. Clin. Microbiol. 27:24142419.
76. Ohashi, M.,, T. Shimada,, and H. Fukumi. 1972. In vitro production of enterotoxin and hemorrhagic principle by Vibrio cholerae, NAG. Jpn. J. Med. Sci. Biol. 25:179194.
77. Oku, Y.,, Y. Uesaka,, T. Hirayama,, and Y. Takeda. 1988. Development of a highly sensitive bead-ELISA to detect bacterial protein toxins. Microbiol. Immunol. 32:807816.
78. Pierce, N. F. 1973. Differential inhibitory effects of cholera toxoids and ganglioside on the enterotoxins of Vibrio cholerae and Escherichia coli. J. Exp. Med. 137:10091023.
79. Pierce, N. E.,, W. B. Greenough III,, and C. C. J. Carpenter, Jr. 1971. Vibrio cholerae enterotoxin and its mode of action. Bacteriol. Rev. 35:113.
80. Pollitzer, R. 1959. Cholera. Monograph no. 43. World Health Organization, Geneva.
81. Ramamurthy, T.,, S. K. Bhattacharya,, Y. Uesaka,, K. Horigome,, M. Paul,, D. Sen,, S. C. Pal,, T. Takeda,, Y. Takeda,, and G. B. Nair. 1992. Evaluation of the bead enzyme-linked immunosorbent assay for detection of cholera toxin directly from stool specimens. J. Clin. Microbiol. 30:17831786.
82. Ramamurthy, T.,, A. Pal,, G. B. Nair,, S. C. Pal,, T. Takeda,, and Y. Takeda. 1990. Experience with toxin bead ELISA in cholera outbreak. Lancet ii:375376.
83. Remmers, E., E. R. R. Colwell,, and R. A. Goldsby. 1982. Production and characterization of monoclonal antibodies to cholera toxin. Infect. Immun. 37:7076.
84. Richardson, S. H. 1969. Factors influencing in vitro skin permeability factor production by Vibrio cholerae. J. Bacteriol. 100:2734.
85. Ruch, F. E., Jr.,, J. R. Murphy,, L. H. Graf,, and M. Field. 1978. Isolation of nontoxinogenic mutants of Vibrio cholerae in a colorimetric assay for cholera toxin using the S49 mouse lymphosarcoma cell line. J. Infect. Dis. 137:747755.
86. Sack, D. A.,, S. Huda,, P. K. B. Neogi,, R. R. Daniel,, and W. M. Spira. 1980. Microtiter ganglioside enzyme-linked immunosorbent assay for Vibrio and Escherichia coli heat-labile enterotoxins and antitoxin. J. Clin. Microbiol. 11:3540.
87. Sack, D. A.,, and R. B. Sack. 1975. Test for enterotoxigenic Escherichia coli using Y1 adrenal cells in miniculture. Infect. Immun. 11:334336.
88. Sack, R. B.,, and C. C. J. Carpenter. 1969. Experimental canine cholera. I. Development of the model. J. Infect. Dis. 119:138149.
89. Sack, R. B.,, and C. C. J. Carpenter. 1969. Experimental canine cholera. II. Production by cell-free culture filtrates of Vibrio cholerae. J. Infect. Dis. 119:150157.
90. Sack, R. B.,, S. L. Gorbach,, J. G. Banwell,, B. Jacobs,, B. D. Chatterjee,, and R. C. Mitra. 1971. Enterotoxigenic Escherichia coli isloated from patients with severe cholera-like disease. J. Infect. Dis. 123:378385.
91. Saha, S.,, and S. C. Sanyal. 1988. Cholera toxin gene-positive Vibrio cholerae Ol Ogawa and Inaba strains produce the new cholera toxin. FEMS Microbiol. Lett. 50:113116.
92. Saha, S.,, and S. C. Sanyal. 1989. Neutralization of the new cholera toxin by antiserum against crude enterotoxin of cholera toxin gene-positive Vibrio cholerae Ol in rabbit ileal loop model. Indian J. Med. Res. 89:117120.
93. Sanyal, S., C. K. Alam,, P. K. B. Neogi,, M. I. Huq,, and K. A. Al-Mahmud. 1983. A new cholera toxin. Lancet i:1337.
94. Sanyal, S. C,, P. K. B. Neogi,, K. Alam,, M. I. Huq,, and K. A. Al-Mahamud. 1984. A new enterotoxin produced by Vibrio cholerae Ol. J. Diarrhoea!Dis. Res. 2:312.
95. Shimamura, T. 1972. Immune response in germ-free mice orally immunized with Vibrio cholerae. KeioJ. Med. 21:113126.
96. Shimamura, T.,, S. Tazume,, K. Hashimoto,, and S. Sasaki. 1981. Experimental cholera in germfree suckling mice. Infect. Immun. 34:296298.
97. Shimamura, T.,, S. Watanabe,, and S. Sasaki. 1985. Enhancement of enterotoxin production by carbon dioxide in Vibrio cholerae. Infect. Immun. 49:455456.
98. Soman, G.,, J. Narayanan,, B. L. Martin,, and D. J. Graves. 1986. Use of substituted (ben-zylidineamino) guanidines in the study of gua-nidino group specific ADP-ribosyltransferase. Biochemistry 25:41134119.
99. Soman, G.,, K. B. Tomer,, and D. J. Graves. 1983. Assay of mono ADP-ribosyltransferase activity by using guanylhydrazones. Anal. Biochem. 134:101110.
100. Spira, W. M.,, R. B. Sack,, and J. L. Froehlich. 1981. Simple adult rabbit model for Vibrio cholerae and enterotoxigenic Escherichia coli diarrhea. Infect. Immun. 32:739747.
101. Strombeck, D. R.,, and D. Harrold. 1974. Binding of cholera toxin to mucins and inhibition by gastric mucin. Infect. Immun. 10:12661272.
102. Svennerholm, A.-M.,, and J. Holmgren. 1978. Identification of Escherichia coli heat-labile enterotoxin by means of a ganglioside immunosorbent assay (GM,-ELISA) procedure. Curr. Microbiol. 1:1923.
103. Svennerholm, A.-M.,, M. Wikstrom,, M. Lind-blad,, and J. Holmgren. 1986. Monoclonal antibodies to Escherichia coli heat-labile enterotoxins: neutralizing activity and differentiation of human and porcine LTs and cholera toxin. Med. Biol. 64:2330.
104. Svennerholm, A.-M.,, M. Wikstrom,, M. Lind-blad,, and J. Holmgren. 1986. Monoclonal antibodies against Escherichia coli heat-stable toxin (STa) and their use in a diagnostic ST ganglioside GM,-enzyme-linked immunosorbent assay. J. Clin. Microbiol. 24:585590.
105. Svennerholm, A.-M.,, M. Wikstrom,, L. Lind-holm,, and J. Holmgren,. 1986. Monoclonal antibodies and immunodetection methods for Vibrio cholerae and Escherichia coli enterotoxins, p. 7797. In A. J. Macario, and E. Conway de Macario (ed.), Monoclonal Antibodies against Bacteria, vol III. Academic Press, New York.
106. Takao, T.,, T. Hitouji,, S. Aimoto,, Y. Shim-onishi,, S. Hara,, T. Takeda,, Y. Takeda,, and T. Miwatani. 1983. Amino acid sequence of a heat-stable enterotoxin isolated from enterotoxigenic Escherichia coli strain 18D. FEBS Lett. 152: 15.
107. Takeda, T.,, G. B. Nair,, K. Suzuki,, and Y. Shimonishi. 1990. Production of a monoclonal antibody to Vibrio cholerae non-O1 heat-stable enterotoxin (ST) which is cross-reactive with Yersinia enterocolitica ST. Infect. Immun. 58:27552759.
108. Takeda, T.,, Y. Peina,, A. Ogawa,, S. Dohi,, H. Abe,, G. B. Nair,, and S. C. Pal. 1991. Detection of heat-stable enterotoxin in a cholera toxin gene positive strains of Vibrio cholerae O1. FEMS Microbiol. Lett. 80:2328.
109. Takeda, T.,, Y. Takeda,, T. Miwatani,, and N. Ohtomo. 1978. Detection of cholera enterotoxin activity in suckling hamsters. Infect. Immun. 19:752754.
110. Takeda, Y.,, T. Takeda,, T. Yano,, K. Yamamoto,, and T. Miwatani. 1979. Purification and partial characterization of heat-stable enterotoxin of enterotoxigenic Escherichia coli. Infect. Immun. 25:978985.
111. Thompson, M. R.,, H. Brandwein,, M. LaBine-Racke,, and R. A. Giannella. 1984. Simple and reliable enzyme-linked immunosorbent assay with monoclonal antibodies for detection of Escherichia coli heat-stable enterotoxins. J. Clin. Microbiol. 20:5964.
112. Tsukamoto, T.,, Y. Kinoshita,, S. Taga,, Y. Takeda,, and T. Miwatani. 1980. Value of passive immune hemolysis for detection of heat-labile enterotoxin produced by enterotoxigenic Escherichia coli. J. Clin. Microbiol. 12:768771.
113. Uesaka, Y.,, Y. Otsuka,, M. Kashida,, Y. Oku,, K. Horigome,, G. B. Nair,, S. C. Pal,, S. Yamasaki,, and Y. Takeda. 1992. Detection of cholera toxin by a highly sensitive bead-enzyme linked immunosorbent assay. Microbiol. Immunol. 36:4353.
114. Ujiiye, A.,, and K. Kobari. 1970. Protective effect on infections with Vibrio cholerae in suckling mice caused by the passive immunization with milk of immune mothers. J. Infect. Dis. 121(Suppl.):S50S55.
115. Yamamoto, K.,, Y. Takeda,, T. Miwatani,, and J. P. Craig. 1981. Stimulation by lincomycin of production of cholera-like enterotoxin in Vibrio cholerae non-Ol. FEMS Microbiol. Lett. 12:245248.
116. Yamamoto, K.,, Y. Takeda,, T. Miwatani,, and J. P. Craig. 1982. Purification and some properties of a non-Ol Vibrio cholerae enterotoxin that is identical to cholera enterotoxin. Infect. Immun. 39:11281135.
117. Yamamoto, K.,, Y. Takeda,, T. Miwatani,, and J. P. Craig. 1983. Evidence that a non-O1 Vibrio cholerae produces enterotoxin that is similar but not identical to cholera enterotoxin. Infect. Immun. 41:896901.
118. Yolken, R. H.,, H. B. Greenberg,, M. H. Mer-son,, R. B. Sack,, and A. Z. Kapikian. 1977. Enzyme-linked immunosorbent assay for detection of Escherichia coli heat-labile enterotoxin. J. Clin. Microbiol. 6:439444.
119. Yoshimura, S.,, T. Takao,, Y. Shimonishi,, M. Arita,, T. Takeda,, H. Imaishi,, T. Honda,, and T. Miwatani. 1986. A heat-stable enterotoxin of Vibrio cholerae non-Ol: chemical synthesis, and biological and physicochemical properties. Biopolymers 25:S69S83.
120. Zinnaka, Y.,, and C. C. J. Carpenter, Jr. 1972. An enterotoxin produced by non-cholera vibrios. Johns Hopkins Med. J. 131:403411.

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