Chapter 14 : Animal Models in Cholera Research

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Our current knowledge of cholera and the highly effective oral treatment of the disease could not have been attained without the use of animal models and human volunteers. Ever since the discovery of the etiologic agent of cholera, there have been attempts to develop suitable animal models for studying the interactions of with its accidental human niche. The major animal models that have been employed in cholera research and some examples of the valuable information provided by these models have been discussed in this chapter. Finkelstein clearly demonstrated the presence of classical exo-enterotoxin (CT) (choleragen) and proceeded to work on purification of the material from Syncase medium, using infant rabbits as his biological assay. Concomitant with toxin purification, attempts were made to derive mutants of that would produce altered toxins or natural toxoids. Colonization studies are largely dependent on animal models, because the complex interactions between the two dynamic living systems are impossible to duplicate in vitro. The standard measure of vaccine efficacy was usually determined by the mouse protection assay. For all of the remarkable advances that have been made in cholera research at the bench, the real answers will have to be provided by in its normal environmental niche and in its transient home away from home, the intestines of humans and experimental animals.

Citation: Richardson S. 1994. Animal Models in Cholera Research, p 203-226. In Wachsmuth I, Blake P, Olsvik Ø (ed), and Cholera. ASM Press, Washington, DC. doi: 10.1128/9781555818364.ch14
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1. Aziz, K. M. S.,, A. K. M. Mohsin,, W. K. Hare,, and R. A. Phillips. 1968. Using the rat as a cholera "model." Nature (London) 220: 814 815.
2. Barua, D.,, and W. B. Greenough III (ed.). 1992. Cholera. Plenum Medical Book Co., New York.
3. Baselski, V. S.,, S. Upchurch,, and C. D. Parker. 1978. Isolation and phenotypic characterization of virulence deficient mutants of Vibrio cholerae. Infect. Immun. 22: 181 188.
4. Basu, S.,, R. L. Robinson,, and M. J. Pickett. 1970. Preliminary studies on the bioassay of anticholera vaccines in chinchillas. J. Infect. Dis. 121: S56 S57.
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: 428 434.
6. Betley, M. J.,, V. L. Miller,, and J. J. Mekalanos. 1986. Genetics of bacterial enterotoxins. Annu. Rev. Microbiol. 40: 577 605.
7. Bromander, A.,, J. Holmgren,, and N. Lycke. 1991. Cholera toxin stimulates IL-1 production and enhances antigen presentation by macrophages in vitro. J. Immunol. 146: 2908 2914.
8. Burnet, F. M.,, and J. D. Stone. 1947. Desquamation of intestinal epithelium by V. cholerae filtrates. Characterization of mucinase and tissue disintegrating enzymes. Aust. J. Exp. Biol. Med. Sci. 25: 219 226.
8a. Bushnell, O. A.,, and C. S. Brookhyer (ed.). 1965. Proceedings of the Cholera Research Symposium, Honolulu, 1965. U.S. Public Health Service publication no. 1328. U.S. Government Printing Office, Washington, D.C.
9. Callahan, L. T., III,, and S. H. Richardson. 1973. Biochemistry of Vibrio cholerae virulence, III. Nutritional requirements for toxin production and the effects of pH on toxin elaboration in chemically defined media. Infect. Immun. 7: 567 572.
10. Callahan, L. T., III,, R. C. Ryder,, and S. H. Richardson. 1971. Biochemistry of Vibrio cholerae virulence. II. Skin permeability factor-cholera enterotoxin production in a chemically defined medium. Infect. Immun. 4: 611 618.
11. Chedid, M.,, and S. B. Mizel. 1990. Involvement of cyclic AMP-dependent protein kinases in the signal transduction pathway for interleukin-1. Mol. Cell. Biol. 10: 3824 3827.
12. Chisari, F. V.,, and R. S. Northrup. 1974. Pathophysiologic effects of lethal and immunoregula-tory doses of cholera enterotoxin in the mouse. J. Immunol. 113: 740 749.
13. Chisari, F. V.,, R. S. Northrup,, and L. C. Chen. 1974. The modulating effect of cholera enterotoxin on the immune response. J. Immunol. 113: 729 739.
14. Colwell, R. R.,, and W. M. Spira,. 1992. The ecology of Vibrio cholerae, p. 107 127. In D. Barua, and W. B. Greenough III, (ed.), Cholera. Plenum Medical Book Co., New York.
15. 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: 614 616.
16. Craig, J. P., 1965. The effect of cholera stool and culture filtrates on the skin of guinea pigs and rabbits, p. 153 158. In O. A. Bushnell, and C. S. Brookhyer (ed.), Proceedings of the Cholera Research Symposium, Honolulu, 1965. U.S. Public Health Service publication no. 1328. U.S. Government Printing Office, Washington D.C.
17. Craig, J. P., 1971. Cholera toxins, p. 189 254. In S. Kadis,, T. C. Montie,, and S. J. Ajl (éd.), Microbial Toxins, vol. IIA. Academic Press, New York.
18. De, S.N. 1959. Enterotoxicity of bacteria-free culture-filtrate of Vibrio cholerae. Nature (London) 183: 1533 1534.
19. De, S.N. 1959. False reaction in ligated loop of rabbit intestine. Indian J. Pathol. Bacteriol. 2: 121 128.
20. De, S. N.,, M. L. Ghose,, and J. Chandra. 1962. Further observations on choiera enterotoxin. Trans. R. Soc. Trop. Med. Hyg. 3: 241 245.
21. De, S. N.,, M. L. Ghose,, and A. Sen. 1960. Activities of bacteria-free preparations from Vibrio cholerae. J. Pathol. Bacteriol. 79: 373 380.
22. DiRita, V. J. 1992. Co-ordinate expression of virulence genes by ToxR in Vibrio cholerae. Mol. Microbiol. 6: 451 458.
23. Donta, S. T.,, and M. King. 1973. Induction of steroidogenesis in tissue culture by cholera enterotoxin. Nature (London) 243: 246 247.
24. Dragunsky, E. M.,, E. Rivera,, W. Aaronson,, T. M. Dolgaya,, H. D. Hochstein,, W. H. Habig,, and I. S. Levenbook. 1992. Experimental evaluation of antitoxic protective effect of new cholera vaccines in mice. Vaccine 10: 735 736.
25. Dutta, N. K.,, and M. K. Habbu. 1955. Experimental cholera in infant rabbits: a method for che-motherapeutic investigation. Br. J. Pharmacol. Chemother. 10: 153 159.
26. Dutta, N. K.,, M. V. Panse,, and D. R. Kulkarni. 1959. Role of cholera toxin in experimental cholera. J. Bacteriol. 78: 594 595.
27. Elson, C. O.,, and W. Ealding. 1984. Generalized systemic and mucosal immunity in mice after mucosal stimulation with cholera toxin. J. Immunol. 132: 2736 2741.
28. Evans, D. J. 1968. Characterization of an ion translocase inhibitor from Vibrio cholerae, p. 1 172. Ph.D. dissertation, Wake Forest University, Winston-Salem, N.C.
29. Evans, D. J., Jr.,, and S. H. Richardson. 1968. ta vitro production of choleragen and vascular permeability factor by Vibrio cholerae. J. Bacteriol. 96: 126 130.
30. 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: 5242 5246.
31. Feeley, J. C.,, and M. Pittman. 1962. A mouse protection test for assay of cholera vaccine, p. 92 94. In SEATO Conference on Cholera. Post Publishing Co., Bangkok, Thailand.
32. Field, M. 1971. Intestinal secretion: effect of cyclic AMP and its role in cholera. N. Engl. J. Med. 284: 1137 1144.
33. Field, M.,, G. R. Piotkin,, and W. Silen. 1968. Effects of vasopressin, theophylline and cyclic adenosine monophosphate on short-circuit current across isolated rabbit ileal mucosa. Nature (London) 217: 469 471.
34. Finkeistein, R. A. 1970. Monospecific equine antiserum against cholera exo-enterotoxin. Infect. Immun. 2: 691 697.
35. Finkeistein, R. A. 1973. Cholera. Crit. Rev. Microbiol. 2: 553 623.
36. Finkeistein, R. A., 1976. Progress in the study of cholera and related enterotoxins, p. 53 84. In A. Bernheimer (ed.), Mechanisms in Bacterial Toxicology. John Wiley & Sons, New York.
37. Finkeistein, R. A., 1988. Structure of the cholera enterotoxin (choleragen) and the immunologically related ADP-ribosylating heat-labile enterotoxins, p. 1 38. In M. C. Hardegree,, W. H. Habig,, and A. Tu (ed.), Handbook of Natural Toxins, vol. II. Bacterial Toxins. Marcel Dekker, Inc., New York.
38. Finkeistein, R. A., 1988. Cholera, the cholera enterotoxins, and the cholera enterotoxin-related enterotoxin family, p. 85 101. In P. Owen, and T. J. Foster (ed.), Immunochemical and Molecular Genetic Analysis of Bacterial Pathogens. Elsevier/North Holland Science Publishing, Amsterdam.
39. Finkeistein, R. A., 1992. Cholera enterotoxin (choleragen): a historical perspective, p. 155 187. In D. Barua, and W. G. Greenough III (ed.), Cholera. Plenum Medical Book Co., New York.
40. Finkeistein, R. A.,, M. Boesman,, S. H. Neon,, M. K. LaRue,, and R. Delaney. 1974. Dissociation and recombinations of the subunits of the cholera enterotoxin (choleragen). J. Immunol. 113: 145 150.
41. Finkeistein, R. A.,, and C. E. Lankford. 1955. Nutrient requirements of Vibrio cholerae, p. 49. Bacteriol. Proc. 1955.
42. Finkeistein, R. A.,, and J. J. LoSpalluto. 1969. Pathogenesis of experimental cholera: preparation and isolation of choleragen and choleragenoid. J. Exp. Med. 130: 185 202.
43. Finkeistein, R. A.,, J. J. LoSpaUuto. 1970. Production of highly purified choleragen and choleragenoid. J. Infect. Dis. 121:( Suppl): S63 S72.
44. Finkeistein, R. A.,, and S. Mukerjee. 1963. Hemagglutination: a rapid method for differentiating Vibrio cholerae and El Tor vibrios. Proc. Soc. Exp. Biol. Med. 112: 355 359.
45. Finkeistein, R. A.,, M. L. Vasil,, and R. K. Holmes. 1974. Studies on toxinogenesis in Vibrio cholerae. I. Isolation of mutants with altered toxinogenicity. J. Infect. Dis. 129: 117 123.
46. Formal, S. B.,, D. Kundel,, H. Schneider,, N. Kunev,, and H. Sprinz. 1961. Studies with Vibrio cholerae in the ligated loop of the rabbit intestine. Br. J. Exp. Pathol. 42: 504 510.
47. Fréter, R. 1956. Coproantibody and bacterial antagonism as protective factors in experimental enteric cholera. J. Exp. Med. 104: 419 426.
48. Fréter, R. 1974. Interactions between mechanisms controlling the intestinal flora. Am. J. Clin. Nutr. 27: 1409 1416.
49. Fréter, R.,, and P. C. M. O'Brien. 1981. Role of chemotaxis in the association of motile bacteria with intestinal mucosa: fitness and virulence of nonche-motactic Vibrio cholerae mutants in infant mice. Infect. Immun. 34: 222 233.
50. Fréter, R.,, P. C. M. O'Brien,, and M. S. Macsal. 1981. Role of chemotaxis in the association of motile bacteria with intestinal mucosa: in vivo studies. Infect. Immun. 34: 234 240.
51. Fujita, K.,, and R. A. Finkelstein. 1972. Antitoxic immunity in experimental cholera: comparison of immunity induced perorally and parenterally in mice. J. Infect. Dis. 125: 647 655.
52. Galen, J.,, A. Fasano,, J. Ketley,, and S. Richardson. 1990. The role of neuraminidase in Vibrio cholerae pathogenesis, p. 41. Abstr. Annu. Meet. Am. Soc. Microbiol. 1990.
52a. Galen, J.,, and J. Kaper. Personal communication.
53. Galen, J. E.,, J. M. Ketley,, A. Fasano,, S. H. Richardson,, S. S. Wasserman,, and J. B. Kaper. 1992. Role of Vibrio cholerae neuraminidase in the function of cholera toxin. Infect. Immun. 60: 406 415.
54. Gill, D. M. 1976. The arrangement of subunits in cholera toxin. Biochemistry 15: 1242 1248.
55. Goldberg, M. B.,, V. J. DiRita,, and S. B. Calder-wood. 1990. Identification of an iron-regulated virulence determinant in Vibrio cholerae, using TnphoA mutagenesis. Infect. Immun. 58: 55 60.
56. Greenough, W. B., III,, N. F. Pierce,, and M. Vaughn. 1970. Titration of cholera enterotoxin and antitoxin in isolated fat cells. J. Infect. Dis. 121: S111 S113.
57. Guerrant, R. L.,, L. L. Brunton,, T. C. Schnait-man,, L. I. Rebbun,, 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: 320 327.
58. Guptka, R. K.,, S. C. Szu,, R. A. Finkelstein,, and J. B. Robbins. 1992. Synthesis characterization, and some immunological properties of conjugates composed of the detoxified lipopolysaccharide of Vibrio cholera Ol serotype Inaba bound to cholera toxin. Infect. Immun. 60: 3201 3208.
59. Hill, S. J.,, and J. L. Ebersole. 1991. Cholera toxin synergizes LPS and IL-1 beta-induced PGE2 release: potential amplification systems in cholera. Lymphokine Cytokine Res. 10: 445 449.
60. Hochstein, H. D.,, J. C. Feeley,, and S. H. Richardson. 1970. Titration of cholera antitoxin levels by passive hemagglutination tests using fresh and formalinized sheep erythrocytes. Proc. Soc. Exp. Biol. Med. 133: 120 124.
61. Holmgren, J.,, I. Lonnroth,, and L. Svennerholm. 1973. Tissue receptor for cholera exotoxin: postulated structure from studies with GM 1 ganglioside and related glycolipids. Infect. Immun. 8: 208 214.
62. Honda, T.,, and R. A. Finkelstein. 1979. Selection and characteristics of a novel Vibrio cholerae mutant lacking the A (ADP-ribosylating) portion of the cholera enterotoxin. Proc. Natl. Acad. Sci. USA 76: 2052 2056.
63. Huber, G. S.,, and R. A. Phillips. 1962. Cholera and the sodium pump, p. 37 40. In SEATO Conference on Cholera. Post Publishing Co., Bangkok, Thailand.
64. Jenkin, C. R.,, and D. Rowley. 1959. Possible factors in the pathogenesis of cholera. Br. J. Exp. Pathol. 40: 474 482.
65. Kaper, J. B.,, and M. M. Levine. 1990. Recombinant attenuated Vibrio cholerae strains used as live oral vaccines. Res. Microbiol. 141: 901 906.
66. Kennedy, J. R.,, and S. H. Richardson. 1969. Fine structure of Vibrio cholerae during toxin production. J. Bacteriol. 100: 1393 1401.
67. Kennedy, J. R.,, and S. H. Richardson. 1972. Effects of cholera permeability factor on guinea pig skin. An electron microscopic study. Lab. Invest. 26: 409 418.
68. King, C. A.,, and W. E. van Heyningen. 1973. Deactivation of cholera toxin by a sialidase-resistant monosialosyl ganglioside. J. Infect. Dis. 127: 639 647.
69. Koonìn, E. V. 1992. The second cholera toxin, Zot, and its plasmid-encoded and phage-encoded homologues constitute a group of putative ATPases with an altered purine NTP-binding motif. FEBS Lett. 312: 3 6.
70. Kothary, M. H.,, E. E Claverie,, J. M. Madden,, and S. H. Richardson. 1991. Purification and characterization of a Vibrio hollisae toxin which elongates chínese hamster ovary cells, p. 53 58. Proc. 27th Joint Conf. Cholera Related Diarrheal Dis.
71. Kothary, M. H.,, and S. H. Richardson. 1987. Fluid accumulation in infant mice caused by Vibrio hollisae and its extracellular enterotoxin. Infect. Immun. 55: 626 630.
72. Kuhn, R. E.,, and S. H. Richardson. 1984. A study on the genetic and cellular basis of sensitivity to cholera toxin in the SAM model, p. 221. Abstr. Joint Meet. R. Am. Soc. Trop. Med. Hyg.
73. LaBrec, E. H.,, H. Sprinz,, H. Schneider,, and S. Formal,. 1965. Localization of vibrios in experimental cholera: a fluorescent antibody study in guinea pigs, p. 272 276. In O. A. Bushnell, and C. S. Brookhyer (ed.), Proceedings of the Cholera Research Symposium, Honolulu, 1965. U.S. Public Health Service publication no. 1328. U.S. Government Printing Office, Washington, D.C.
74. Lange, S.,, I. Lonnroth,, and H. Nygren. 1984. Intestinal resistance to cholera toxin in mouse. Antitoxic antibodies and desensitization of adenylate cyclase. Int. Arch. Allergy Appi. Immunol. 74: 221 225.
75. Lankford, C. E. 1960. Factors of virulence of Vibrio cholerae. Ann. N.Y.Acad. Sci. 88: 1203 1212.
76. Lankford, C. E.,, and U. Legsomburana,. 1965. Virulence factors of choleragenic vibrios, p. 109 120. In O. A. Bushnell, and C. S. Brookhyer (ed.), Proceedings of the Cholera Research Symposium, Honolulu, 1965. U.S. Public Health Service publication no. 1328. U.S. Government Printing Office, Washington, D.C.
77. Leitch, G. J. 1988. Cholera enterotoxin-induced mucus secretion and increase in the mucus blanket of the rabbit ileum in vivo. Infect. Immun. 56: 2871 2875.
78. Levine, M. M.,, and J. B.. Kaper. 1993. Live oral vaccines against cholera: an update. Vaccine 11: 207 212.
79. Levine, M. M.,, J. B. Kaper,, R. E. Black,, and M. L. Clements. 1983. New knowledge on pathogenesis of bacterial enteric infection as applied to vaccine development. Microbiol. Rev. 47: 510 550.
80. Levine, M. M.,, and N. F. Pierce,. 1992. Immunity and vaccine development, p. 285 327. In D. Barua, and W. B. Greenough III (ed.), Cholera. Plenum Medical Book Co., New York.
81. Lewis, A. C.,, and S. H. Richardson. 1974. Properties of cholera enterotoxin from chemically defined media, p. 82 92. In Proceedings of the Ninth Joint Cholera Conference. Department of State publication no. 8762. U.S. Government Printing Office, Washington, D.C.
82. Lewis, A. C.,, S. H. Richardson,, and B. Sheridan. 1976. Biochemistry of Vibrio cholerae virulence: purification of cholera enterotoxin by preparative disc electrophoresis. Appl. Environ. Microbiol. 32: 288 293.
83. Lockwood, D.,, S. H. Richardson,, and M. Aiken. 1982. In vivo biologic activities of Vibrio fluvialis and its toxic products, p. 31. Abstr. Annu. Meet. Am. Soc. Microbiol. 1982.
84. Lockwood, D. E.,, A. S. Kreger,, and S. H. Richardson. 1982. Detection of toxins produced by Vibrio fluvialis. Infect. Immun. 35: 702 708.
85. Lönnroth, I.,, and J. Holmgren. 1973. Subunit structure of cholera toxin. J. Gen. Microbiol. 76: 417 427.
86. Lycke, N.,, A. K. Bromander,, L. Ekman,, U. Karlsson,, and J. Holmgren. 1989. Cellular basis of immunomodulation by cholera toxin in vitro with possible association to the adjuvant function in vivo. J. Immunol. 142: 20 27.
87. Manan, M. J.,, J. M. Slauch,, and J. J. Mekalanos. 1993. Selection of bacterial virulence genes that are specifically induced in host tissues. Science 259: 686 688.
88. Mekalanos, J. J. 1985. Cholera toxin: genetic analysis, regulation and role in pathogenesis. Curr. Top. Microbiol. Immunol. 118: 97 118.
89. Mekalanos, J. J. 1992. Environmental signals controlling expression of virulence determinants in bacteria. J. Bacteriol. 174: 1 7.
90. Mekalanos, J. J.,, R. J. Collier,, and W. R. Romig. 1978. Purification of cholera toxin and its sub-units: new methods of preparation and the use of hypertoxinogenic mutants. Infect. Immun. 20: 552 558.
91. Mekalanos, J. J.,, R. J. Collier,, and W. R. Romig. 1978. Affinity filters, a new approach to the isolation of tox mutants of Vibrio cholerae. Proc. Natl. Acad. Sci. USA 75: 941 945.
91a. Mekalanos, J. J.,, and M. H. Kothary. Personal communication.
92. Mekalanos, J. J.,, S. L. Moseley,, J. R. Murphy,, and S. Falkow. 1982. Isolation of enterotoxin structural gene deletion mutations in Vibrio cholerae induced by two mutagenic vibriophages. Proc. Natl. Acad. Sci. USA. 79: 151 155.
93. Miller, J. F.,, J. J. Mekalanos,, and S. Falkow. 1989. Coordinate regulation and sensory transduction in the control of bacterial virulence. Science 243: 916 922.
94. Miller, V. L.,, R. K. Taylor,, and J. J. Mekalanos. 1987. Cholera toxin transcriptional activator ToxR is a transmembrane DNA binding protein. Cell 48: 271 279.
95. Moyenuddin, M.,, K. Wachsmuth,, S. H. Richardson,, and W. L. Cook. 1992. Enteropatho-genicity of non-toxigenic Vibrio cholerae Ol for adult mice. Microb. Pathog. 12: 451 458.
96. Nelson, E. T.,, J. D. Clements,, and R. A. Finkeistein. 1976. Vibrio cholerae adherence and colonization in experimental cholera: electron microscopic studies. Infect. Immun. 14: 527 547.
97. Northrup, R. S.,, and F. V. Chisari. 1972. Response of monkeys to immunization with cholera toxoid, toxin, and vaccine: reversion of cholera toxoid. J. Infect. Dis. 125: 471 479.
98. Northrup, R. S.,, and A. S. Fauci. 1972. Adjuvant effect of cholera enterotoxin on the immune response of the mouse to sheep red blood cells. J. Infect. Dis. 125: 672 673.
99. Ohtomo, N.,, T. Muraoka,, A. Tashiro,, Y. Zin-naka,, and K. Amako. 1976. Size and structure of the cholera toxin molecule and its subunits. J. Infect. Dis. 133( Suppl): S31 S40.
100. Osek, J.,, A. M. Svennerholm,, and J. Holmgren. 1992. Protection against Vibrio cholerae El Tor infection by specific antibodies against mannose-binding hemagglutinin pili. Infect. Immun. 60: 4961 4964.
101. Owen, R. L.,, N. F. Pierce,, R. T. Apple,, and W. C. Cray, Jr. 1986. M cell transport of Vibrio cholerae from the intestinal lumen into Peyer's patches: a mechanism for antigen sampling and for microbial transepithelial migration. J. Infect. Dis. 153: 1108 1118.
102. Parker, C.,, D. Gauthier,, A. Tate,, K. Richardson,, and W. R. Romig. 1979. Extended linkage map of Vibrio cholerae. Genetics 91: 191 214.
103. Parsot, C.,, and J. J. Mekalanos. 1991. Expression of ToxR, the transcriptional activator of the virulence factors in Vibrio cholerae, is modulated by the heat shock response. Proc. Natl. Acad. Sci. USA 87: 9898 9902.
104. Patel, P.,, C. F. Marrs,, J. S. Mattick,, W. M. Ruehl,, R. K. Taylor,, and M. Koomey. 1991. Shared antigenicity and immunogenicity of type 4 pilins expressed by Pseudomonas aeruginosa, Mor-axella bovis, Neisseria gonorrhoeae, Dichelobacter nodosus, and Vibrio cholerae. Infect. Immun. 59: 4674 4676.
105. Pearson, G. D. N.,, V. J. DiRita,, M. B. Goldberg,, S. A. Boyko,, S. B. Calderwood,, and J. J. Mekalanos. 1990. New attenuated derivatives of Vibrio cholerae. Res. Microbiol. 14: 893 899.
106. Peterson, J. W.,, J. J. LoSpalluto,, and R. A. Finkelstein. 1972. Localization of cholera toxin in vivo. J. Infect. Dis. 126: 617 628.
107. Peterson, J. W.,, and L. G. Ochoa. 1989. Role of prostaglandins and cAMP in the secretory effects of cholera toxin. Science 245: 857 859.
108. Peterson, K. M.,, and J. J. Mekalanos. 1988. Characterization of the Vibrio cholerae ToxR regulen: identification of novel genes involved in intestinal colonization. Infect. Immun. 56: 2822 2829.
109. Phillips, R. A., 1965. Pathophysiology of cholera, p. 82 84. In O. A. Bushnell, and C. S. Brookhyer (ed.), Proceedings of the Cholera Research Symposium, Honolulu, 1965. U.S. Public Health Service publication no. 1328. U.S. Government Printing Office, Washington, D.C.
110. 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: 1009 1023.
111. Pierce, N. F. 1978. The role of antigen form and function in the primary and secondary intestinal immune responses to cholera toxin and toxoid in rats. J. Exp. Med. 145: 195 206.
112. Pierce, N. F.,, and J. L. Gowans. 1975. Cellular kinetics of the intestinal immune response to cholera toxoid in rats. J. Exp. Med. 142: 1550 1563.
113. Pierce, N. E.,, J. B. Kaper,, J. J. Mekalanos,, and W. C. Cray, Jr. 1985. Role of cholera toxin in enteric colonization by Vibrio cholerae Ol in rabbits. Infect. Immun. 50: 813 816.
114. PolUtzer, R. 1959. Cholera. Monograph no. 43. World Health Organization, Geneva.
115. Rappaport, R. S.,, and G. Bonde. 1981. Development of a vaccine against experimental cholera and Escherichia coli diarrheal disease. Infect. Immun. 32: 534 542.
116. Rappaport, R. S.,, G., Bonde,, T. McCann, B. A. Rubin, and H. Tint. 1974. Development of a purified cholera toxoid. II. Preparation of a stable, antigenic toxoid by reaction of purified toxin with glu-taraldehyde. Infect. Immun. 9: 304 317.
117. Rappaport, R. S.,, B. A. Rubin,, and H. Tint. 1974. Development of a purified cholera toxoid. I Purification of toxin. Infect. Immun. 9: 294 303.
118. Richardson, K. 1991. Roles of motility and flagellar structure in pathogenity of Vibrio cholerae: analysis of motility mutants in three animal models. Infect. Immun. 59: 2727 2736.
119. Richardson, S. H. 1966. Inhibition of intestinal ion translocase enzymes by culture filtrates of Vibrio cholerae. J. Bacteriol. 91: 1384 1386.
120. Richardson, S. H. 1968. An ion translocase system from rabbit intestinal mucosa. Preparation and properties of the (Na+K+)-activated ATPase. Bio-chim. Biophys. Acta 150: 572 577.
121. Richardson, S. H. 1969. Factors influencing in vitro skin permeability factor production by Vibrio cholera. J. Bacteriol. 100: 27 34.
122. Richardson, S. H.,, and D. J. Evans, Jr., 1965. The effects of Vibrio cholerae extracts on membrane transport mechanisms, p. 139 144. In O.A. Bushnell, and C. S. Brookhyer (ed.), Proceedings of the Cholera Research Symposium, Honolulu, 1965. U.S. Public Health Service publication no. 1328. U.S. Government Printing Office, Washington, D.C.
123. Richardson, S. H.,, and D. J. Evans, Jr. 1968. Isolation of cholera toxins by dextran sulfate precipitation. J. Bacteriol. 96: 1443 1445.
124. Richardson, S. H.,, J. Giles,, and K. S. Kruger. 1983. H-2 modulation of cholera enterotoxin effects in SAM (sealed adult mice), p. 28 Abstr. Anna. Meet. Am. Soc. Microbiol. 1983.
125. Richardson, S. H.,, J. C. Giles,, and K. S. Kruger. 1984. Sealed adult mice: new model for enterotoxin evaluation. Infect. Immun. 43: 482 486.
126. Richardson, S. H.,, and R. E. Kuhn. 1986. Studies on the genetic and cellular control of sensitivity to enterotoxins in the sealed adult mouse model. Infect. Immun. 54: 522 528.
127. Richardson, S. H.,, W. McKenzie,, E. Daves,, D. J. Evans,, and D. G. Evans,. 1975. Trans-missibility of the plasmid controlling vascular permeability factor (PF) and heat labile enterotoxin (LT) in E. coli from patients with "cholera-like" diarrhea, p. 37 44. In H. Fukumi, and M. Ohashi (ed.), Symposium on Cholera Kyoto 1974. Japanese Cholera Panel, Tokyo.
128. Richardson, S. H.,, and K. A. Noftie. 1970. Purification and properties of permeability factor/cholera enterotoxin from complex and synthetic media. J. Infect. Dis. 121: S73 S79.
129. Roomi, N.,, M. Laburthe,, N. Fleming,, R. Crovrther,, and J. Forstner. 1984. Cholera-induced mucin secretion from rat intestine: lack of effect of cAMP, cycloheximide, VIP and colchicine. Am. J. Physiol. 247: G140 G148.
130. Sack, R. B.,, C. C. J. Carpenter,, R. W. Steenburg,, and N. F. Pierce. 1966. Experimental cholera: a canine model. Lancet 7456: 206 207.
131. Sack, R. B.,, and C. E. Miller. 1969. Progressive changes of vibrio serotypes in germ-free mice infected with Vibrio cholerae. J. Bacteriol. 99: 688 695.
132. Savage, D. C. 1978. Factors involved in colonization of the gut epithelial surface. Am. J. Clin. Nutr. 31: S131 S135.
133. Savage, D. C., 1980. Adherence of normal flora to mucosal surfaces, p. 33 59. In E. H. Beachey (ed.), Bacterial Adherence. Chapman & Hall, London.
134. Schrank, G. D.,, and W. F. Verwey. 1976. Distribution of cholera organisms in experimental Vibrio cholerae infections: proposed mechanisms of pathogenesis and antibacterial immunity. Infect. Immun. 13: 195 203.
135. Sciortino, C. V. 1989. Protection against infection with Vibrio cholerae by passive transfer of monoclonal antibodies to outer membrane antigens. J. Infect. Dis. 160: 248 252.
136. Sengupta, D. K.,, T. K. Sengupta,, and S. C. Ghose. 1992. Major outer membrane proteins of Vibrio cholerae and their role in induction of protective immunity through inhibition of intestinal colonization. Infect. Immun. 60: 4848 4855.
137. Spangier, B. D. 1992. Structure and function of cholera toxin and the related Escherichia coli heat-labile enterotoxin. Microbiol. Rev. 56: 622 647.
138. Spira, W. M.,, and P. J. Fedorka-Cray. 1984. Purification of enterotoxins from Vibrio mimicus that appear to be identical to cholera toxin. Infect. Immun. 45: 679 684.
139. 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: 739 747.
140. Spyrides, G. J.,, and J. C. Feeley. 1970. Concentration and purification of cholera exotoxin by absorption on aluminum compound gels. J. Infect. Dis. 121( Suppl): S96 S99.
141. Sun, D.,, J. J. Mekalanos,, and R. K. Taylor. 1990. Antibodies directed against the toxin-co-regulated pilus isolated from Vibrio cholerae provide protection in the infant mouse experimental cholera model. J. Infect. Dis. 161: 1231 1236.
142. Sun, D.,, J. M. Seyer,, J. Kovari,, R. A. Sumrada,, and R. K. Taylor. 1991. Localization of protective epitopes within the pilin subunit of the Vibrio cholerae toxin-coregulated pilus. Infect. Immun. 59: 114 118.
143. Svennerholm, A. M.,, and J. Holmgren. 1976. Synergistic protective effect in rabbits of immunization with Vibrio cholerae lipopolysaccharide and toxin/toxoid. Infect. Immun. 13: 735 740.
144. Tannenbaum, C. S.,, and T. A. Hamilton. 1989. Lipopolysaccharide-induced gene expression in murine peritoneal macrophages is selectively suppressed by agents that elevate intracellular cAMP. J. Immunol. 142: 1274 1280.
145. Taylor, R. K.,, V. L. Miller,, D. B. Furlong,, and J. J. Mekalanos. 1987. Use of phoA gene fusions to identify a pilus colonization factor coordinately regulated with cholera toxin. Proc. Natl. Acad. Sci. USA 84: 2833 2837.
146. Trucksis, M.,, J. E. Galen,, J. Michalski,, A. Fasano,, and J. B. Kaper. 1993. Accessory cholera enterotoxin (Ace), the third member of a Vibrio cholerae virulence cassette. Proc. Natl. Acad. Sci. USA 90: 5267 5271.
147. Ujiiye, A.,, A. Nakatomi,, K. Utsunomiya,, K. Mitsui,, S. Segarne,, M. Iwanaga,, and K. Kobari. 1968. Experimental cholera in mice. I. First report on the oral infection. Trop. Med. (Nagasaki University) 10: 65 71.
148. van Heyningen, W. E. Personal communication.
149. van Heyningen, W. E.,, C. C. J. Carpenter,, N. F. Pierce,, and W. B. Greenough III. 1971. Deactivation of cholera toxin by ganglioside. J. Infect. Dis. 124: 415 418.
150. van Heyningen, W. E.,, and J. R. Seal. 1983. Cholera. The American Scientific Experience 1947-80. Westview Press, Boulder, Colo.
151. Vasil, J. L.,, R. K. Holmes,, and R. A. Finkeistein. 1975. Conjugal transfer of a chromosomal gene determining production of enterotoxin in Vibrio cholerae. Science 187: 849 850.
152. Vaughan, M.,, N. F. Pierce,, and W. B. Greenough III. 1970. Stimulation of glycerol production in fat cells by cholera toxin. Nature (London) 226: 658 659.
153. Weston, L.,, H. Drexler,, and S. H. Richardson. 1973. Characterization of vibriophage VA-1 J. Gen. Virol. 21: 155 158.
154. Winner, L. III,, J. Mack,, R. Weltzin,, J. J. Mekalanos,, J. Kraehenbuhl,, and M. Neutra. 1991. New model for analysis of mucosal immunity: intestinal secretion of specific monoclonal immunoglobulin A from hybridoma tumors protects against Vibrio cholerae infection. Infect. Immun. 59: 977 982.
155. Yamamoto, T.,, and T. Yokota. 1989. Vibrio cholerae Ol adherence to human small intestinal cells in vitro. 7. Infect. Dis. 160: 168 169.


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Table 1

Major animal models in cholera research

Citation: Richardson S. 1994. Animal Models in Cholera Research, p 203-226. In Wachsmuth I, Blake P, Olsvik Ø (ed), and Cholera. ASM Press, Washington, DC. doi: 10.1128/9781555818364.ch14

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