Cholera Toxin: Mechanism of Action and Potential Use in Vaccine Development

Bacterial Toxins: Tools in Cell Biology and Pharmacology

Volumn , Issue , 2008, Pages 1-13

  Zhang, G F ^a   Patton, W A ^a   Moss, J ^a   Vaughan, M ^a  

^a NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

Enterotoxins; Mammalian; Nicotinamide; Nucleotide binding; Pathogenic

Indexed keywords

EID: 84954206388     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/9783527614615.ch1     Document Type: Chapter

References (125)

1. Abood ME, Hurley JB, Pappone M-C, et al. (1982): Functional homology between signal-coupling proteins. In J. Biol. Chem. 257:10540-10543.
2. Aitken R, Hirst TR (1995): Bacterial toxins as novel antigen delivery systems. In Livestock Prod. Sci. 42:163-172.
3. Albert MJ, Siddique AK, Islam MS, et al. (1993): Large outbreak of clinical cholera due to Vibrio cholerae non-O1 in Bangladesh. In Lancet 341:704.
4. Beubler E, Kollar G, Saria A, et al. (1989): Involvement of 5-hydroxytryptamine, prostaglandin E2, and cyclic adenosine monophosphate in cholera toxin-induced fluid secretion in the small intestine of rat in vivo. In Gastroenter. 96:368-376.
5. Bokoch GM, Katada T, Northup JK, et al. (1983): Identification of the predominant substrate for ADP-ribosylation by islet activating protein. In J. Biol. Chem. 258:2072-2075.
6. Bokoch GM, Katada T, Northup JK, et al. (1984): Purification and properties of the inhibitory guanine nucleotide-binding regulatory component of adenylate cyclase. In J. Biol. Chem. 259:3560-3567.
7. Brown HA, Gutowski S, Moomaw CR, et al. (1993): ADP-ribosylation factor, a small GTP-dependent regulatory protein, stimulates phosphase D activity. In Cell 75:1137-1144.
8. Buckley NE, Su Y, Milstein S, et al. (1995): The role of calcium influx in cellular proliferation induced by interaction of endogenous ganglioside GM1 with the B subunit of cholera toxin. In Biochim. Biophys. Acta 1256:275-283.
9. Burnette WN (1994): AB5 ADP-ribosylating toxins: Comparative anatomy and physiology. In Structure 2:151-158.
10. Burnette WN, Mar VL, Platler BW, et al. (1991): Site-specific mutagenesis of the catalytic subunit of cholera toxin: Substituting lysine for arginine 7 causes loss of activity. In Infect. Immun. 59:4266-4270.
11. Casey PJ, Gilman AG (1988): G protein involvement in receptor-effector coupling. In J. Biol. Chem. 263:2577-2580.
12. Cassel D, Selinger Z (1977): Mechanism of adenylate cyclase activation by cholera toxin: Inhibition of GTP hydrolysis at the regulatory site. In Proc. Natl. Acad. Sci. USA 74:3307-3311.
13. Chongsa-nguan M, Chaicumpa W, Moolasart P, et al. (1993): Vibrio cholerae O139 Bengal in Bangkok. In Lancet 342:430-431.
14. Clemens JD, Sack DA, Harris JR, et al. (1986): Field trial of oral cholera vaccines in Bangladesh. In Lancet 2 (8499): 124-127.
15. Clemens JD, Sack DA, Harris JR, et al. (1990): Field trial of oral cholera vaccines in Bangladesh: Results from three-year follow-up. In Lancet 335 (8684):270-273.
16. Cockcroft S, Thomas GMH, Fensome A, et al. (1994): Phospholipase D: A downstream effector of ARF in granulocytes. In Science 263:523-526.
17. Czerkinsky C, Russell MW, Lycke N, et al. (1989): Oral adminstration of a streptococcal antigen coupled to cholera toxin B subunit evokes strong antibody responses in salivary glands and extramucosal tissues. In Infect. Immun. 57:1072-1077.
18. Davis R, Spencer CM (1995): Live oral cholera vaccine: A preliminary review of its pharmacology and clinical potential in providing protective immunity against cholera. In Clin. Immunother. 4:235-247.
19. De SN (1959): Enterotoxicity of bacteria-free culture filtrate of Vibrio cholerae. In Nature 183:1533-1534.
20. Dertzbaugh MT, Elson CO, (1991) Cholera toxin as a mucosal adjuvant. In Topics in Vaccine Adjuvant Research, (Spriggs D, Koff W) CRC Press, Boca Raton, FL,119-132.
21. Dertzbaugh MT, Macrina FL (1989): Plasmid vectors for constructing translational fusions to the B subunit of cholera toxin. In Gene 82:335-342.
22. Dertzbaugh MT, Peterson DL, Macrina FL (1990): Cholera toxin B-subunit gene fusion: Structural and functional analysis of the chimeric protein. In Infect. Immun. 58:70-79.
23. Dixon SJ, Stewart D, Grinstein S, et al. (1987): Transmembrane signalling by the B subunit of cholera toxin: Increased cytoplasmic free calcium in rat lymphocytes. In J. Cell Biol. 105:1153-1161.
24. Douce G, Turcotte C, Cropley I, et al. (1995): Mutants of Escherichia coli heat-labile toxin lacking ADP-ribosyltransferase activity act as nontoxic, mucosal adjuvants. In Proc. Natl. Acad. Sci. USA 92:1644-1648.
25. Dutta NK, Panse MW, Kulkarni DR (1959): Role of cholera toxin in experimental cholera. In J. Bacteriol. 78:594-595.
26. Eklund S, Cassuto J, Jodal M, et al. (1984): The involvement of the enteric nervous system in the intestinal secretion evoked by cyclic adenosine 3', 5'-monophosphate. In Acta. Physiol. Scand. 120:311-316.
27. Elson CO, Ealding W (1984): Generalized systemic and mucosal immunity in mice after mucosal stimulation with cholera toxin. In J. Immunol. 132:27-36.
28. Elson CO, Hollard SP, Dertzbaugh MT, et al. (1995): Morphologic and functional alterations of mucosal T cells by cholera toxin and its B subunits. In J. Immunol. 154:1032-1040.
29. Enomoto K, Gill DM (1979): Requirement for guanosine triphosphate in the activation of adenylate cyclase by cholera toxin. In J. Supramol. Struct. 10:51-60.
30. Enomoto K, Gill DM (1980): Cholera toxin activation of adenylate cyclase. In J. Biol. Chem. 255:1252-1258.
31. Field M (1971): Intestinal secretion: Effect of cyclic AMP and its role in cholera. In N. Engl. J. Med. 284:1137-1144.
32. Finkelstein RA, LoSpalluto JJ (1969): Pathogenesis of experimental cholera: Preparation and isolation of choleragen and choleragenoid. In J. Exp. Med. 130:185-202.
33. Fishman PH (1982): Role of membrane gangliosides in the binding and action of bacterial toxins. In J. Membr. Biol. 69:85-97.
34. Fontana MR, Manetti R, Giannelli V, et al. (1995): Construction of nontoxic derivatives of cholera toxin and characterization of the immunological response against the A subunit. In Infect. Immun. 63:2356-2360.
35. Gill DM, Coburn J (1987): ADP-ribosylation by cholera toxin: Functional analysis of a cellular system that stimulates the enzymatic activity of cholera toxin fragment Al. In Biochemistry 26:6364-6371.
36. Gill DM, Meren R (1978): ADP-ribosylation of membrane proteins catalyzed by cholera toxin: Basis of the activation of adenylate cyclase. In Proc. Natl. Acad. Sci. USA 75:3050-3054.
37. Harokopakis E, Cholders NK, Michalek SM, et al. (1995): Conjugation of cholera toxin or its B subunit to liposomes for targeted delivery of antigens. In J. Immunolog. Meth. 185:31-42.
38. Ho Y-K, Hingorani VN, Navon SE, et al. (1989): Transducin: A signalling switch regulated by guanine nucleotides. In Curr. Top. Cell. Regul. 30:171-202.
39. Holmgren J, Czerkinsky C, Lycke N, et al. (1994): Strategies for the induction of immune responses at mucosal surfaces making use of cholera toxin B subunit as immunogen, carrier, and adjuvant. In Am. J. Trop. Med. Hyg. 50:42-54.
40. Jobling MG, Holmes RK (1992): Fusion proteins containing the A2 domain of cholera toxin assemble with B polypeptides of cholera toxin to form immunoreactive and functional holotoxin-like chimeras. In Infect. Immun. 60:4915-4924.
41. Johnson GL, Kaslow HR, Bourne HR (1978): Genetic evidence that cholera toxin substrates are regulatory components of adenylate cyclase. In J. Biol. Chem. 253:7120-7123.
42. Joseph KC, Kim SU, Strieber A, et al. (1978): Endocytosis of cholera toxin into neuronal GERL. In Proc. Natl. Acad. Sci. USA 75:2815-2819.
43. Kahn RA, Gilman AG (1984a): ADP-ribosylation of Gs promotes the dissociation of its α and β subunits. In J. Biol. Chem. 259:6235-6240.
44. Kahn RA, Gilman AG (1984b): Purification of a protein cofactor required for ADP-ribosylation of the stimulatory regulatory component of adenylate cyclase by cholera toxin. In J. Biol. Chem. 259:6228-6234.
45. Kahn RA, Gilman AG (1986): The protein cofactor necessary for ADP-ribosylation of Gs by cholera toxin is itself a GTP-binding protein. In J. Biol. Chem. 261:7906-7911.
46. Kaper JB, Levine MM (1990): Recombinant attenuated Vibrio cholerae strains used as live oral vaccines. In Res. Microbiol. 141:901-906.
47. Kaper JB, Morris JG, Levine MM (1995): Cholera. In Clin. Microbiol. Rev. 8:48-86.
48. Kaslow HR, Johnson GL, Brothers VM, et al. (1980): A regulatory component of adenylate cyclase from human erythrocyte membranes. In J. Biol. Chem. 255:3736-3741.
49. Knoop FC, Thomas DD (1984): Effect of cholera enterotoxin on calcium uptake and cyclic AMP accumulation in rat basophilic leukemia cells. In Int. J. Biochem. 16:275-280.
50. Koch R (1884): An address on cholera and its bacillus. In Brit. Med. J August 30:403-407;453-459.
51. Ktistakis NT, Brown HA, Sternweis PC, et al. (1995): Phospholipase D is present on Golgi-enriched membranes and its activation by ADP-ribosylation factor is sensitive to brefeldin A. In J. Biol. Chem. 92:4952-4956.
52. Larew JS-A, Peterson JE, Graves DJ (1991): Determination of the kinetic mechanism of arginine-specific ADP-ribosyltransferases using a high performance liquid chromatographic assay. In J. Biol. Chem. 266:52-57.
53. Lebens M, Holmgren J (1994): Mucosal vaccines based on the use of cholera toxin B subunit as immunogen and antigen carrier. In Dev. Biol. Stand. 82:215-227.
54. Lencer WI, de Almeida JB, Moe S, et al. (1993): Entry of cholera toxin into polarized human intestinal epithelial cells: Identification of an early brefeldin A-sensitive event required for A1-peptide generation. In J. Clin. Invest. 92:2941-2951.
55. Lencer WI, Moe S, Rufo PA, et al. (1995): Transcytosis of cholera toxin subunits across model human intestinal epithelia. In Proc. Natl. Acad. Sci. USA 92:10094-10098.
56. LeVine H, Cuatrecasas P (1981): Activation of pigeon erythrocyte adenylate cyclase by cholera toxin. In Biochim. Biophys. Acta 672:248-261.
57. Levine MM, Kaper JB, Herrington D, et al. (1988): Volunteer studies of deletion mutants of Vibrio cholerae O1 prepared by recombinant techniques. In Infect. Immun. 56:161-167.
58. Lin MC, Welton AF, Berman MF (1978): Essential role of GTP in the expression of adenylate cyclase activity after cholera toxin treatment. In J. Cycl. Nuc. Res. 4:159-168.
59. Lippincott-Schwartz J, Donaldson JG, Schweizer A, et al. (1990): Microtubule-dependent retrograde transport of proteins into the ER in the presence of brefeldin A suggests an ER recycling pathway. In Cell 60:821-836.
60. Lippincott-Schwartz J, Yuan LC, Bonifacino JS, et al. (1989): Rapid redistribution of Golgi proteins into the ER in cells treated with brefeldin A: Evidence for membrane cycling from the Golgi to the ER. In Cell 56:801-813.
61. Maenz DD, Forsyth GW (1986): Cholera toxin facilitates calcium transport in jejunal brush border vesicles. In Can. J. Physiol. Pharmacol. 64:568-574.
62. McKenzie SJ, Halsey JF (1984): Cholera toxin B subunit as a carrier protein to stimulate a mucosal immune response. In J. Immunol. 133:1818-1824.
63. Mekalanos JJ (1994): Live bacterial vaccines: Environmental aspects. In Curr. Opin. Biotech. 5:312-319.
64. Mekalanos JJ, Collier RJ, Romig WR (1979): Enzymatic activity of cholera toxin: II. Relationships to proteolytic processing, disulfide bond reduction, and subunit composition. In J. Biol. Chem. 254:5855-5861.
65. Mekalanos JJ, Sadoff JC (1994): Cholera vaccines: Fighting an ancient scourge. In Science 265:1387-1389.
66. Merritt EA, Hol WG (1995): AB5 toxins. In Curr. Opin. Struct. Biol. 5:165-171.
67. Merritt EA, Pronk SE, Sixma TK, et al. (1994a): Structure of partially-activated E coli heat-labile enterotoxin (LT) at 2.6 Å resolution. In FEBS Let. 337:88-92.
68. Merritt EA, Sarfaty S, Pizza M, et al. (1995): Mutation of a buried residue causes loss of activity, but no conformational change in the heat-labile enterotoxin of Escherichia coli. In Struct. Biol. 2:269-272.
69. Merritt EA, Sarfaty S, Van Den Akker F, et al. (1994c): Crystal structure of cholera toxin B-pentamer bound to receptor GMl pentasaccharide. In Prot. Sci. 3:166-175.
70. Merritt EA, Sixma TK, Kalk KH, et al. (1994b): Galactose-binding site in Escherichia coli heat-labile enterotoxin (LT) and cholera toxin (CT). In Mol. Microbiol. 13:745-753.
71. Moss J, Garrison S, Oppenheimer NJ, et al. (1979b): NAD-dependent ADP-ribosylation of arginine and proteins by Escherichia coli heat-labile enterotoxin. In J. Biol. Chem. 254:6270-6272.
72. Moss J, Manganiello VC, Vaughan M (1976): Hydrolysis of nicotinamide adenine dinucleotide by choleragen and its A protomer: Possible role in the activation of adenylate cyclase. In Proc. Natl. Acad. Sci. USA 73:4424-4427.
73. Moss J, Stanley, SJ (1981): Histone-dependent and histone-independent forms of an ADP-ribosyltransferase from human and turkey erythrocytes. In Proc. Natl. Acad. Sci. USA 78:4809-4812.
74. Moss J, Stanley SJ, Oppenheimer NJ (1979a): Substrate specificity and partial purification of a stereospecific NAD- and guanidine-dependent ADP-ribosyltransferase from avian erythrocytes . In J. Biol. Chem. 255:7835-7837.
75. Moss J, Stanley SJ, Watkins PA, et al. (1980): ADP-ribosyltransferase activity of mono- and multi-(ADP-ribosylated) choleragen. In J. Biol. Chem. 255:7835-7837.
76. Moss J, Vaughan M (1977a): Mechanism of action of choleragen: Evidence for ADP-ribosyltransferase activity with arginine as an acceptor. In J. Biol. Chem. 252:2455-2457.
77. Moss J, Vaughan M (1977b): Choleragen activation of solubilized adenylate cyclase: Requirement for GTP and protein activator for demonstration of enzymatic activity. In Proc. Natl. Acad. Sci. USA 74:4396-4400.
78. Moss J, Vaughan M (1978): Isolation of an avian erythrocyte protein possessing ADP-ribosyltransferase activity and capable of activating adenylate cyclase. In Proc. Natl. Acad. Sci. USA 75:3621-3624.
79. Moss J, Vaughan M, (1988a): Mechanism of action of choleragen (cholera toxin) and E coli heat-labile enterotoxins. In Bacterial Toxins (Handbook of Natural Toxins), 4, (Tu AT, Hardegree MC) Dekker, New York.
80. Moss J, Vaughan M (1988b): ADP-ribosylation of guanyl nucleotide-binding regulatory proteins by bacterial toxins. In Adv. Enzym. 61:303-379.
81. Moss J, Vaughan M (1993): ADP-ribosylation factors, 20,000 Mr guanine nucleotide-binding protein activators of cholera toxin and components of intracellular vesicular transport systems. In Cell. Signalling 5:367-379.
82. Moss J, Vaughan M (1995): Structure and function of ARF proteins: Activators of cholera toxin and critical components of intracellular vesicular transport processes. In J. Biol. Chem. 270:12327-12330.
83. Nakaya S, Moss J, Vaughan M (1980): Effects of nucleoside triphosphates on choleragen-activated brain adenylate cyclase. In Biochemistry 19:4871-4874.
84. Nambiar MP, Oda T, Chen C, et al. (1993): Involvement of the Golgi region in the intracellular trafficking of cholera toxin. In J. Cell. Physiol. 154:222-228.
85. Navon SE, Fung BK (1984): Characterization of transducin from bovine retinal rod outer segments. Mechanism and effects of cholera toxin-catalyzed ADP-ribosylation. In J. Biol. Chem. 259:6686-6693.
86. Nilsson O, Cassuto J, Larsson L-I, et al. (1983): 5-hydroxytryptamine and cholera secretion: A histochemical and physiological study in cats. In Gut 24:543-548.
87. Noda M, Tsai S-C, Adamik R, et al. (1990): Mechanism of cholera toxin activation by a guanine nucleotide-dependent 19-kDa protein. In Biochim. Biophys. Acta 1034:195-199.
88. Northup JK, Sternweis PC, Smigel MD, et al. (1980): Purification of the regulatory component of adenylate cyclase. In Proc. Natl. Acad. Sci. USA 77:6516-6520.
89. Ohtomo N, Muraoka T, Tashiro A, et al. (1976): Size and structure of the cholera toxin molecule and its subunits. In J. Infect. Dis. 133:S31-S40.
90. Oppenheimer NJ (1978): Structural determination and sterospecificity of the choleragen-catalyzed reaction of NAD+ with guanidines. In J. Biol. Chem. 253:4907-4910.
91. Orlandi PA, Curran PK, Fishman PH (1993): Brefeldin A blocks the response of cultured cells to cholera toxin. In J. Biol. Chem. 268:12010-12016.
92. Osborne JC Jr, Stanley SJ, Moss J (1985): Kinetic mechanisms of two NAD:arginine ADP-ribosyltransferases: The soluble, salt-stimulated transferase from turkey erythrocytes and choleragen, a toxin from Vibrio cholerae. In Biochemistry 24:5235-5240.
93. Peterson JW, Jackson CA, Reitmeyer JC (1990): Synthesis of prostaglandins in cholera toxin-treated Chinese hamster ovary cells. In Microb. Pathogen. 9:345-353.
94. Peterson JW, Lu Y, Duncan S, et al. (1994): interactions of intestinal mediators in the mode of action of cholera toxin. In J. Med. Microbiol. 41:3-9.
95. Peterson JW, Ochoa LG (1989): Role of prostaglandins and cAMP in the secretory effects of cholera toxin. In Science 245:857-859.
96. Picking WD (1993): Interaction of pyrene-labeled monosialoganglioside GM1 micelles with cholera toxin. In Biochem. Biophys. Res. Comm. 195:1153-1158.
97. Picking WL, Moon H, Wu H, et al. (1995): Fluorescence analysis of the interaction between ganglioside GM1-containing phospholipid vesicles and the B subunit of cholera toxin. In Biochim. Biophys. Acta 1247:65-73.
98. Pinkett MO, Anderson WB (1982): Plasma membrane-associated component(s) that confer(s) cholera toxin sensitivity to adenylate cyclase. In Biochim. Biophys. Acta. 714:337-343.
99. Pizza M, Domenighini M, Hol W, et al. (1994): Probing the structure-activity relationship of Escherichia coli LT-A by site-directed mutagenesis. In Mol. Microbiol. 14:51-60.
100. Quiding M, Nordström I, Kilander A, et al. (1991): Intestinal immune responses in humans. Oral cholera vaccination induces strong intestinal antibody responses and interferon-γ production and evokes local immunological memory. In J. Clin. Invest. 88:143-148.
101. Ramamurthy T, Garg S, Sharma R, et al. (1993): Emergence of novel strain of Vibrio cholerae with epidemic potential in southern and eastern India. In Lancet 341:703-704.
102. Reitmeyer JC, Peterson JW (1990): Stimulatory effects of cholera toxin on arachidonic acid metabolism in Chinese hamster ovary cells (43022). In Proc. Soc. Exper. Biol. Med. 193:181-184.
103. Robishaw JD, Russell DW, Harris BA, et al. (1986): Deduced primary structure of the α subunit of the GTP-binding stimulatory protein of adenylate cyclase. In Proc. Natl. Acad. Sci. USA 83:1251 -1255.
104. Sanchez J, Johansson S, Löwenadler B, et al. (1990): Recombinant cholera toxin B subunit and gene fusion proteins for oral vaccination. In Res. Microbiol. 141:971-979.
105. Schleifer LS, Kahn RA, Hanski E, et al. (1982): Requirements for cholera toxin-dependent ADP-ribosylation of the purified regulatory component of adenylate cyclase. In J. Biol. Chem. 257:20-23.
106. Sixma TK, Kalk KH, van Zanten BAM, et al. (1993): Refined structure of Escherichia coli heat-labile enterotoxin, a close relative of cholera toxin. In J. Mol. Biol. 230:890-918.
107. Sixma TK, Pronk SE, Kalk KH, et al. (1991): Crystal structure of a cholera toxin-related heat-labile enterotoxin from E. coli. In Nature 351:371-377.
108. Spangler BD (1992): Structure and function of cholera toxin and the related Escherichia coli heat-labile enterotoxin. In Microbiol. Rev. 56:622-647.
109. Sun J-B, Holmgren J, Czerkinsky C (1994): Cholera toxin B subunit: An efficient transmucosal carrier-delivery system for induction of peripheral immunological tolerance. In Proc. Natl. Acad. Sci. USA 91:10795-10799.
110. Svennerholm A-M, Jertborn M, Gothefors L, et al. (1984): Mucosal antitoxic and antibacterial immunity after cholera disease and after immunization with a combined B subunit-whole cell vaccine. In J. Infect. Dis. 149:884-893.
111. Svennerholm A-M, Lange S, Holmgren J (1978): Correlation between intestinal synthesis of specific immunoglobulin A and protection against experimental cholera in mice. In Infect. Immun. 21:1-6.
112. Taussig R, Gilman AG (1995): Mammalian membrane-bound adenylyl cyclases. In J. Biol. Chem. 270:1-4.
113. Tomasi M, Battistini A, Araco A, et al. (1979): The role of the reactive disulfide bond in the interaction of cholera-toxin functional regions. In Eur. J. Biochem. 93:621-627.
114. Trepel JB, Chuang D-M, Neff NH (1977): Transfer of ADP-ribose from NAD to choleragen: A subunit acts as catalyst and acceptor protein. In Proc. Natl. Acad. Sci. USA 74:5440-5442.
115. Tsai S-C, Adamik R, Haun RS, et al. (1992): Differential interaction of ADP-ribosylation factors 1, 3, and 5 with rat brain Golgi membranes. In Proc. Natl. Acad. Sci. USA 89:9272-9276.
116. Tsai S-C, Noda M, Adamik R, et al. (1987): Enhancement of choleragen ADP-ribosyltransferase activities by guanyl nucleotides and a 19-kDa membrane protein. In Proc. Natl. Acad. Sci. USA 84:5139-5142.
117. Tsai S-C, Noda M, Adamik R, et al. (1988): Stimulation of choleragen enzymatic activities by GTP and two soluble proteins purified from bovine brain. In J. Biol. Chem. 263:1768-1772.
118. Uwiera RE, Romancyia DA, Wong JP, et al. (1992): Effect of covalent modification on the binding of cholera toxin B subunit to ileal brush border surfaces. In Anal. Biochem. 204:244-249.
119. Van Dop C,Tsubokawa M, Bourne HR, et al. (1984): Amino acid sequence of retinal transducin at the site ADP-ribosylated by cholera toxin. In J. Biol. Chem. 259:696-698.
120. Waldor MK, Mekalanos JJ (1994): Emergence of a new cholera pandemic: Molecular analysis of virulence determinants in Vibrio cholerae and O139 and development of a live vaccine prototype. In J. Infect. Dis. 170:278-283.
121. West RE Jr, Moss J, Vaughan M et al. (1985): Pertussis toxin-catalyzed ADP-ribosylation of transducin. Cysteine 347 is the ADP-ribose acceptor site. In J. Biol. Chem. 260:14428-14430.
122. Wilson BA, Collier RJ (1992): Diphtheria toxin and Pseudomonas aeruginosa exotoxin A: Active-site structure and enzymatic mechanism. In Curr. Top. Microbiol. & Immunol. 175:27-41.
123. Zhang R-G, Scott DL, Westbrook ML, et al. (1995a): The three-dimensional crystal structure of cholera toxin. In J. Mol. Biol. 251:563-573.
124. Zhang R-G, Westbrook ML, Westbrook EM, et al. (1995b): The 2.4 Å crystal structure of cholera toxin B subunit pentamer: Choleragenoid. In J. Mol. Biol. 251:550-562.
125. Zolkiewska A, Okasaki IJ, Moss J (1994): Vertebrate mono-ADP-ribosyl-transferases. In Mol. Cell. Biochem. 138:107-112.