The three-dimensional crystal structure of cholera toxin

Journal of Molecular Biology

Volumn 251, Issue 4, 1995, Pages 563-573

  Zhang, Rong Guang ^a   Westbrook, Mary L ^b   Nance, Sharon ^a   Spangler, Brenda D ^a   Westbrook, Edwin M ^a   Scott, David L ^c   Shipley, Graham ^a,d  

^a ARGONNE NATIONAL LABORATORY   (United States)

^b YALE UNIVERSITY   (United States)

^c BOSTON UNIVERSITY   (United States)

^d NORTHWESTERN UNIVERSITY   (United States)

Author keywords

ADP ribosylation; Cholera toxin; Choleragenoid; Crystal structure; Enterotoxins

Indexed keywords

EID: 0029161099     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1995.0456     Document Type: Article

References (69)

1. Allured, V. S., Collier, R. J., Carroll, S. F. & McKay, D. B. (1986). Structure of exotoxin A of Pseudomonas aeruginosa at 3.0 A resolution. Proc. Natl Acad. Sci. USA, 83, 1320-1324.
2. Brunger, A. T., Kuriyan, J. & Karplus, M. (1987). Crystallographic R-factor refinement by molecular dynamics. Science, 235, 458-460.
3. 5 ADP-ribosylating toxins: comparative anatomy and physiology. Structure, 2, 151-158.
4. Burnette, W. N., Mar, V. L., Plater, B. W., Schlotterbeck, J. D., McGinley M. D., Stoney K. S., Rohde, M. F. & Kaslow, H. R. (1991). Site-directed mutagenesis of the catalytic subunit of cholera toxin: substituting lysine for arginine 7 causes loss of activity Infect. Immunol. 59, 4266-4270.
5. Cabral-Lilly D., Sosinsky G. E., Reed, R. A., McDermott, M. R. & Shipley, G. G. (1994). Orientation of a cholera toxin bound to model membranes. Biophys. J. 66, 935-941.
6. Carroll, S. F. & Collier, R. J. (1987). Active site of Pseudomonas aeruginosa exotoxin A. J. Biol. Chem. 262, 8707-8711
7. Cassel D. & Pfeuffer T. (1978).Mechanismof cholera toxin action: covalent modification of the guanyl nucleotide-binding protein of the adenylate cyclase system. Proc. Natl Acad. Sci. USA, 75, 2669-2673.
8. Choe, S., Bennett, M. J., Fujii, G., Curmi, P. M. G., Kantardjieff, K. A., Collier, R.J. & Eisenberg, D. (1992). The crystal structure of diphtheria toxin. Nature, 357, 216-222.
9. Dallas, W. S. (1983). Conformity between heat-labile toxin genes from human and porcine enterotoxigenic Escherichia coli. Infect. Immun. 40, 647-652.
10. Dallas, W. S. & Falkow, S. (1980). Amino acid sequence homology between cholera toxin and Escherichia coli heat-labile toxin. Nature, 288, 499-501.
11. De, S. N. (1959). Enterotoxicity of bacteria-free culture-filtrate of Vibrio cholerae. Nature, 183, 1533-1534.
12. Dykes, C. W., Halliday I. J., Hobden, A. N., Read, M. J. & Harford, S. (1985). A comparison of the nucleotide sequence of the A subunit of heat-labile enterotoxin and cholera toxin. FEMS family. In Immunochemical and Molecular Genetic Analysis of Bacterial Pathogens (Owen, P. & Foster, T. J. eds), vol. 85, Elsevier Science Publishers, New York.
13. Finkelstein, R. A. (1988). Cholera, the cholera enterotoxins, and the cholera enterotoxin-related enterotoxin. In Immunochemical and Molecular Genetic Analysis of Bacterial Pathogens (Owens, P. & Foster, T. J., eds), chapt. 7, pp. 85-102, Elsevier Science Publishers, New York.
14. Finzel, B. C. (1987). Incorporation of fast Fourier transforms to speed restrained least-squares refinement of protein structures. J. Appl. Crystalog. 20, 53-55.
15. Fishman, P. H., Moss, J. & Osborne, J. C., Jr (1978). Interaction of choleragen with the oligosaccharide of ganglioside GM1: evidence for multiple oligosaccharide binding sites. Biochemistry, 17, 711-716.
16. Fitzgerald, P. M. D. (1988). MERLOT, an integrated package of computer programs for the determination of crystal structures by molecular replacement. J. Appl. Crystallog. 21, 273-278.
17. Foster, J. W. & Kinney D. M. (1985). ADP-ribosylating microbial toxins. CRC Crit. Rev. Microbiol. 11, 273-298.
18. Fraser, M. E., Chernaia, M. M., Kozlov, Y. V. & James, M. N. G. (1994). Crystal structure of the holotoxin from Shigella dysenteriae at 2.5 A resolution. Struct. Biol. 1, 59-64.
19. Galloway T. S. & van Heyningen, S. (1987). Binding of NAD+ by cholera toxin. Biochem. J. 244, 225-230.
20. Gill, D. M. (1975). Involvement of nicrotinamide adenine nucleotide in the action of cholera toxin in vitro. Proc. Natl Acad. Sci. USA, 72, 2064-2068.
21. 1. Biochemistry, 26, 6364-6371.
22. Harford, S. C., Dykes, W., Hobden, A. N., Read, H. J. & Halliday I. J. (1989). Inactivation of the Escherichia coli heat-labile enterotoxin by in-vitro mutagenesis of the A-subunit gene. Eur. J. Biochem. 183, 311-316.
23. Jacob, C. O., Sela, M., Pines, M., Hurwitz, S. & Arnon, R. (1984). Neutralization of heat-labile toxin of E. coli by antibodies to synthetic peptides derived from the B subunit of cholera toxin. Proc. Natl Acad. Sci. USA, 81, 7893-7896.
24. Janicot, M., Fouque, F. & Desbuqois, B. (1991). Activation of rat liver adenylate cyclase by cholera toxin requires toxin internalization and processing in endosomes. J. Biol. Chem. 266, 12858-12865.
25. Joseph, K. C., Kim, S. U., Steiber, A. & Gonatas, N. K. (1978). Endocytosis of cholera toxin into neuronal GerL. Proc. Natl Acad. Sci. USA, 75, 2815-2819.
26. Jospeh, K. C., Steiber, A. & Gonatas, N. K. (1979). Endocytosis of cholera toxin in GERL-like structures of murine neuroblastoma cells pretreated with GM1 ganglioside. J.Cell Biol. 81, 543-554.
27. Kassis, S., Hagmann, J., Fishman, P. H., Chang, P. P. & Moss, J. (1982). Mechanism of action of cholera toxin on intact cells. Generation of A1 peptide and activation of adenylate cyclase. J. Biol. Chem. 257, 12148-12152.
28. Kurosky A., Markel, D. E. & Peterson, J. W. (1977). Covalent structure of the B chain of cholera enterotoxin. J. Biol. Chem. 252, 7257-7264.
29. Lai, C.-Y, Xia, Q.-C. & Salotra, P. T. (1983). Location and amino acid sequence around the ADP-ribosylation site in the cholera toxin active subunit A1. Biochem. Biophys. Res. Commun. 116, 341-348.
30. Lewis, M. J. & Pelham, H. R. B. (1990). A human homologue of the yeast HDEL receptor. Nature, 348 162-163.
31. Lockman, H. & Kaper, J. B. (1983). Nucleotide sequence analysis of the A2 and the B subunits of Vibrio cholerae enterotoxin. J. Biol. Chem. 258, 13722-13726.
32. Ludwig, D. S., Ribi, H. O., Schoolnik G K. & Kornberg, R. D. (1986). Two-dimensional crystals of cholera toxin B-subunit-receptor complexes: projected structure at 17-A resolution. Proc. Natl Acad. Sci. USA, 83, 8585-8588.
33. 1. Biophys. J. 49, 94-96.
34. Mekalanos, J. J., Collier, R. J. & Romig, W. R. (1979). Enzymatic activity of cholera toxin. II. Relationships of proteolytic processing, disulfide bond reduction, and subunit composition. J. Biol. Chem. 254, 5855-5861.
35. Mekalanos, J. J., Swartz, D. J., Pearson, G. D. N., Harford, N., Groyne, F. & De Wilde, M. (1983). Cholera toxin genes: nucleotide sequence, deletion analysis and vaccine development. Nature, 306, 551-557.
36. Merritt, E. A., Sarfaty S., van den Akker, F., L’hoir, C. L., Martial, J. A. & Hol, W. G. J. (1994a). Crystal structure of cholera toxin B-pentamer bound to receptor GM1 pentasaccharide. Protein Sci. 3, 166-175.
37. Merritt, E. A., Pronk, S. E., Sixma, T. K., Kalk, K. H., van Zanten, B. A. & Hol, W. G., (1994b). Structure of partially-activated E. coli heat-labile enterotoxin (LT) at 2.6 A resolution. FEBS Letters 337, 88-92.
38. Moss, J. & Vaughan, M. (1988). ADP-ribosylation of guanyl nucleotide-binding regulatory proteins by bacterial toxins. Advan. Enzymol. 61, 303-379.
39. Moss, J. & Vaughan, M. (1991). Activation of cholera toxin and Escherichia coli heat-labile enterotoxins by ADP-ribosylation factors, a family of 20 kDA guanine nucleotide-binding proteins. Mol. Microbiol. 5, 2621-2627.
40. Moss, J., Manganiello, V. C. & Vaughan, M. (1976). Hydrolysis of nicotinamide adenine nucleotide by choleragen and its A promoter: possible role in activation of adenylate cyclase. Proc. Nat Acad. Sci. USA, 73, 4424-4427.
41. Moss, J., Tsai, S. C. & Vaughan, M. (1994). Activation of cholera toxin by ADP-ribosylation factors. Methods Enzymol. 235, 640-647.
42. Mosser, G., Mallouh, V. & Brisson, A. (1992). A 9A two-dimensional projected structure of cholera toxin B-subunit-GM1 complexes determined by electron crystallography. J. Mol. Biol. 226, 23-28.
43. Orlandi, P. A. & Fishman, P. H. (1993). Orientation of cholera toxin bound to target cells. J. Biol. Chem. 268, 17038-17044.
44. Otwinowski, Z. (1991). In Isomorphous Replacement and Anomalous Scattering: Proceedings of the CCP4 Study Weekend 25-26 January 1991 (Wolf, W., Evans, P. R. & Leslie, A. G. W., eds), pp. 80-86, SERC, Darebury Laboratory Warrington.
45. Peterson, W. J. & Ochoa, L. G. (1989). Role of prostaglandins and cAMP in the secretory effects of cholera toxin. Science, 245, 857-859.
46. Reed, R. A., Mattai, A. J. & Shipley G. G. (1987). Interaction of cholera toxin with ganglioside GM1 receptors in supported lipid monolayers. Biochemistry, 26, 824-832.
47. Ribi, H. O., Ludwig, D. S., Mercer, K. L., Schoolnik GK. & Kornberg, R. D. (1988). Three-dimensional structure of cholera toxin penetrating a lipid membrane. Science, 239, 1272-1276.
48. Richards, F. M. & Kundrot, C. E. (1988). DEFINEStruc-ture: a program for specification of secondary and first level supersecondary structure from alpha carbon coordinate list. Proteins: Struct. Funct. Genet. 3, 71-84.
49. Rothman, J. E. & Orci, L. (1992). Molecular dissection of the secretary pathway. Nature, 355, 409-415.
50. Sattler, J., Schwarzmann, G., Knack, I., Rohm, K.-H. & Wiegandt, H. (1978). Studies of ligand binding to cholera toxin III, cooperativity of oligosaccharide binding. Hoppe-Seyler's Z. Physiol. Chem. 359, 719-723.
51. Sigler, P. B., Druyan, M. E., Kiefer, H. C. & Finkelstein, R. (1977). Cholera toxin crystals suitable for X-ray diffraction studies. Science, 197, 1277-1279.
52. Sixma, T. K., Pronk, S. E., Kalk, K. H., Wartna, E. S., Van Zanten, B. A. M., Witholt, B. & Hol, W. G. J. (1991). Crystal structure of a cholera toxin-related heat-labile enterotoxin from E. coli. Nature, 351, 371-378.
53. 5 orientation. FEBS Letters, 305, 81-85.
54. Sixma, T. K., Pronk, S. E., Kalk, K. H., van Zenten, B. A. M., Berhuis, A. M. & Hol, W. J. G. (1992b). Lactose binding to heat-labile enterotoxin revealed by X-ray crystallography. Nature, 355, 561-564.
55. Sixma, T. K., Kalk, K. H., van Zanten, B. A. M., Dauter, Z., Kingma, J., Witholt, B. & Hol, W. G. J. (1993). Refined crystal structure of Escherichia coli heat-labile enterotoxin, a close relative of cholera toxin. J. Mol. Biol. 230, 890-918.
56. Spangler, B. D. (1992). Structure of function of cholera toxin and the related Escherichia coli heat-labile enterotoxin. Microbiol. Rev. 56, 622-647.
57. Spangler, B. D. & Westbrook, E. M. (1989). Crystallization of isoelectrically homogenous cholera toxin. Biochemistry, 28, 1333-1340.
58. Stein, P. E., Boodhoo, A., Tyrell, G. J., Brunton, J. L. & Read, R. J. (1992). Crystal structure of the cell-binding B oligomer of verotoxin-1 from E. coli. Nature, 355, 748-750.
59. Stein, P. E., Boodhoo, A., Armstrong, G. D., Cockle, S. A., Kelin, M. H. & Read, R. J. (1994). The crystal structure of pertussis toxin. Structure, 2, 45-57.
60. Streatfield, S. J., Sandkvist, M., Sixma, T. K., Bagdasarian, M., Hol, W. G. & Hirst, T. R. (1992). Intermolecular interactions between the A-subunit and B-subunit of heat-labile enterotoxins from Escherichia coli promote holotoxin assembly and stability in-vitro. Proc. Natl Acad. Sci, USA, 89, 12140-12144.
61. Surewicz, W. K., Leddy J. J. & Mantsch, H. H. (1990). Structure, stability and receptor interaction of cholera toxin as studied by Fourier-transform infrared spectroscopy. Biochemistry, 29, 8106-8111.
62. Tomasi, M., Battistini, A., Araco, A., Roda, L. G. & D’Agnolo, M. (1979). The role of the reactive disulfide bond in the interaction of cholera toxin functional regions. Eur. J. Biochem. 93, 621-627.
63. Tran, D., Carpentier, J.-L., Sawano, F., Gorden, P. & Orci, L. (1987). Ligands internalized through coated or non-coated invaginations follow a common intracellular pathway. Proc. Natl Acad. Sci. USA, 84, 7957-7961.
64. Tsuji, T., Honda, T., Miwatani, T., Wakabayashi, T. & Matsubara, H. (1984). The amino acid sequence of the B-subunit of porcine Escherichia coli enterotoxin. FEMS Microbiol. Letters, 25, 243-246.
65. Tsuji, T., Inoue, T., Miyama, A. & Noda, M. (1991). Glutamic acid-112 of the A subunit of heat-labile enterotoxin from enterotoxigenic Escherichia coli is important for ADP-ribosyltransferase. FEBS Letters, 291, 319-321.
66. van Heyningen, S. (1982). Conformational changes in subunit A of cholera toxin following the binding of ganglioside to subunit B. Eur. J. Biochem. 122, 333-337.
67. Wang, B.-C. (1985). Resolution of phase ambiguity in macromolecular crystallography. Methods Enzymol. 115, 90-117.
68. Yang, J., Tamm, L. K., Tillack, T. W. & Shao, Z. (1993). New approach for atomic force microscopy of membrane proteins. The imaging of cholera toxin. J. Mol. Biol. 229, 286-290.
69. Zhang, R.-G., Westbrook, M. L., Westbrook, E. M., Scott, D. L., Otwinowski, Z., Maulik, P. R., Reed, R. A. & Shipley G. G. (1995). The 2.4 A crystal structure of cholera toxin B subunit pentamer: choleragenoid. J. Mol. Biol. In the press.