Order-Disorder-Order Transitions Mediate the Activation of Cholera Toxin

Journal of Molecular Biology

Volumn 377, Issue 3, 2008, Pages 748-760

  Ampapathi, Ravi S ^a   Creath, Andrea L ^a   Lou, Dianne I ^a   Craft Jr , John W ^a   Blanke, Steven R ^b   Legge, Glen B ^a  

^a University of Houston   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

allostery; ARF6; cholera toxin; NMR; partial unfolding

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 6; CHOLERA TOXIN; GUANOSINE TRIPHOSPHATE; POLYPEPTIDE;

ALLOSTERISM; ARTICLE; BINDING AFFINITY; CIRCULAR DICHROISM; ENDOPLASMIC RETICULUM; FLUORESCENCE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; SPECTROSCOPY; TITRIMETRY;

EID: 40649098565     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.12.075     Document Type: Article

References (59)

1. D.A. Sack R.B. Sack G.B. Nair A.K. Siddique Cholera Lancet 363 2004 223 233
2. D.E. Stewart-Tull Vaba, Haiza, Kholera, Foklune or Cholera: in any language still the disease of seven pandemics J. Appl. Microbiol. 91 2001 580 591
3. D.M. Gill R. Meren ADP-ribosylation of membrane proteins catalyzed by cholera toxin: basis of the activation of adenylate cyclase Proc. Natl Acad. Sci. USA 75 1978 3050 3054
4. G.W. Sharp S. Hynie Stimulation of intestinal adenyl cyclase by cholera toxin Nature 229 1971 266 269
5. D.E. Schafer W.D. Lust B. Sircar N.D. Goldberg Elevated concentration of adenosine 3′:5′-cyclic monophosphate in intestinal mucosa after treatment with cholera toxin Proc. Natl Acad. Sci. USA 67 1970 851 856
6. s and ARF GTPase-activating protein J. Biol. Chem. 269 1994 29490 29494
7. E. Lemichez P. Boquet To be helped or not helped, that is the question J. Cell Biol. 160 2003 991 992
8. W.I. Lencer B. Tsai The intracellular voyage of cholera toxin: going retro Trends Biochem. Sci. 28 2003 639 645
9. J. Moss M. Vaughan Activation of toxin ADP-ribosyltransferases by eukaryotic ADP-ribosylation factors Mol. Cell. Biochem. 193 1999 153 157
10. R.G. Zhang D.L. Scott M.L. Westbrook S. Nance B.D. Spangler G.G. Shipley E.M. Westbrook The three-dimensional crystal structure of cholera toxin J. Mol. Biol. 251 1995 563 573
11. M.G. Jobling R.K. Holmes Identification of motifs in cholera toxin A1 polypeptide that are required for its interaction with human ADP-ribosylation factor 6 in a bacterial two-hybrid system Proc. Natl Acad. Sci. USA 97 2000 14662 14667
12. J.J. Mekalanos R.J. Collier W.R. Romig Enzymic activity of cholera toxin: II. Relationships to proteolytic processing, disulfide bond reduction, and subunit composition J. Biol. Chem. 254 1979 5855 5861
13. P.E. Stein A. Boodhoo G.D. Armstrong S.A. Cockle M.H. Klein R.J. Read The crystal structure of pertussis toxin Structure 2 1994 45 57
14. M.E. Fraser M. Fujinaga M.M. Cherney A.R. Melton-Celsa E.M. Twiddy A.D. O'Brien M.N. James Structure of Shiga toxin type 2 (Stx2) from Escherichia coli O157:H7 J. Biol. Chem. 279 2004 27511 27517
15. L. De Haan T.R. Hirst Cholera toxin: a paradigm for multi-functional engagement of cellular mechanisms (Review) Mol. Membr. Biol. 21 2004 77 92
16. K. Sandvig B. van Deurs Transport of protein toxins into cells: pathways used by ricin, cholera toxin and Shiga toxin FEBS Lett. 529 2002 49 53
17. B. Hazes R.J. Read Accumulating evidence suggests that several AB-toxins subvert the endoplasmic reticulum-associated protein degradation pathway to enter target cells Biochemistry 36 1997 11051 11054
18. K. Teter R.L. Allyn M.G. Jobling R.K. Holmes Transfer of the cholera toxin A1 polypeptide from the endoplasmic reticulum to the cytosol is a rapid process facilitated by the endoplasmic reticulum-associated degradation pathway Infect. Immun. 70 2002 6166 6171
19. B. Tsai Y. Ye T.A. Rapoport Retro-translocation of proteins from the endoplasmic reticulum into the cytosol Nat. Rev. Mol. Cell Biol. 3 2002 246 255
20. W.I. Lencer Retrograde transport of cholera toxin into the ER of host cells Int. J. Med. Microbiol. 293 2004 491 494
21. Y. Hagiwara Y.I. Kawamura K. Kataoka B. Rahima R.J. Jackson K. Komase A second generation of double mutant cholera toxin adjuvants: enhanced immunity without intracellular trafficking J. Immunol. 177 2006 3045 3054
22. A. Schmitz H. Herrgen A. Winkeler V. Herzog Cholera toxin is exported from microsomes by the Sec61p complex J. Cell Biol. 148 2000 1203 1212
23. K. Teter M.G. Jobling D. Sentz R.K. Holmes The cholera toxin A1(3) subdomain is essential for interaction with ADP-ribosylation factor 6 and full toxic activity but is not required for translocation from the endoplasmic reticulum to the cytosol Infect. Immun. 74 2006 2259 2267
24. C. Rodighiero B. Tsai T.A. Rapoport W.I. Lencer Role of ubiquitination in retro-translocation of cholera toxin and escape of cytosolic degradation EMBO Rep. 3 2002 1222 1227
25. s promotes the dissociation of its alpha and beta subunits J. Biol. Chem. 259 1984 6235 6240
26. J.C. Osborne Jr S.J. Stanley J. Moss Kinetic mechanisms of two NAD:arginine ADP-ribosyltransferases: the soluble, salt-stimulated transferase from turkey erythrocytes and choleragen, a toxin from Vibrio cholerae Biochemistry 24 1985 5235 5240
27. C.J. O'Neal M.G. Jobling R.K. Holmes W.G. Hol Structural basis for the activation of cholera toxin by human ARF6-GTP Science 309 2005 1093 1096
28. C.J. O'Neal E.I. Amaya M.G. Jobling R.K. Holmes W.G. Hol Crystal structures of an intrinsically active cholera toxin mutant yield insight into the toxin activation mechanism Biochemistry 43 2004 3772 3782
29. J.J. Mekalanos R.J. Collier W.R. Romig Purification of cholera toxin and its subunits: new methods of preparation and the use of hypertoxinogenic mutants Infect. Immun. 20 1978 552 558
30. s by cholera toxin is itself a GTP binding protein J. Biol. Chem. 261 1986 7906 7911
31. R.W. Woody Circular dichroism Methods Enzymol. 246 1995 34 71
32. P. LaPointe X. Wei J. Gariepy A role for the protease-sensitive loop region of Shiga-like toxin 1 in the retrotranslocation of its A1 domain from the endoplasmic reticulum lumen J. Biol. Chem. 280 2005 23310 23318
33. A.H. Pande P. Scaglione M. Taylor K.N. Nemec S. Tuthill D. Moe Conformational instability of the cholera toxin A1 polypeptide J. Mol. Biol. 374 2007 1114 1128
34. H.J. Dyson P.E. Wright Equilibrium NMR studies of unfolded and partially folded proteins Nat. Struct. Biol. 5 1998 499 503
35. 15N chemical shift referencing in biomolecular NMR J. Biomol. NMR 6 1995 135 140
36. C. Redfield Using nuclear magnetic resonance spectroscopy to study molten globule states of proteins Methods 34 2004 121 132
37. V.J. Hilser E.B. Thompson Intrinsic disorder as a mechanism to optimize allosteric coupling in proteins Proc. Natl Acad. Sci. USA 104 2007 8311 8315
38. A.L. Smoot M. Panda B.T. Brazil A.M. Buckle A.R. Fersht P.M. Horowitz The binding of bis-ANS to the isolated GroEL apical domain fragment induces the formation of a folding intermediate with increased hydrophobic surface not observed in tetradecameric GroEL Biochemistry 40 2001 4484 4492
39. S. Spera A. Bax Empirical correlation between protein backbone conformation and C-alpha and C-beta C-13 nuclear-magnetic-resonance chemical-shifts J. Am. Chem. Soc. 113 1991 5490 5492
40. 13C chemical-shift data J. Biomol. NMR 4 1994 171 180
41. Weighted CSI Program: http://nmr.uhnres.utoronto.ca/ikura/csi/
42. + by cholera toxin Biochem. J. 244 1987 225 230
43. K. Vamvaca B. Vogeli P. Kast K. Pervushin D. Hilvert An enzymatic molten globule: efficient coupling of folding and catalysis Proc. Natl Acad. Sci. USA 101 2004 12860 12864
44. N. Morinaga Y. Kaihou N. Vitale J. Moss M. Noda Involvement of ADP-ribosylation factor 1 in cholera toxin-induced morphological changes of Chinese hamster ovary cells J. Biol. Chem. 276 2001 22838 22843
45. J. Moss M. Vaughan Structure and function of ARF proteins: activators of cholera toxin and critical components of intracellular vesicular transport processes J. Biol. Chem. 270 1995 12327 12330
46. B.D. Spangler Structure and function of cholera toxin and the related Escherichia coli heat-labile enterotoxin Microbiol. Rev. 56 1992 622 647
47. X. Zhu E. Kim A.L. Boman A. Hodel W. Cieplak R.A. Kahn ARF binds the C-terminal region of the Escherichia coli heat-labile toxin (LTA1) and competes for the binding of LTA2 Biochemistry 40 2001 4560 4568
48. X. Zhu R.A. Kahn The Escherichia coli heat labile toxin binds to Golgi membranes and alters Golgi and cell morphologies using ADP-ribosylation factor-dependent processes J. Biol. Chem. 276 2001 25014 25021
49. Q. Guo Y. Shen Y.S. Lee C.S. Gibbs M. Mrksich W.J. Tang Structural basis for the interaction of Bordetella pertussis adenylyl cyclase toxin with calmodulin EMBO J. 24 2005 3190 3201
50. D. Ladant A. Ullmann Bordetella pertussis adenylate cyclase: a toxin with multiple talents Trends Microbiol. 7 1999 172 176
51. J.J. Love X. Li J. Chung H.J. Dyson P.E. Wright The LEF-1 high-mobility group domain undergoes a disorder–to–order transition upon formation of a complex with cognate DNA Biochemistry 43 2004 8725 8734
52. H.J. Dyson P.E. Wright Coupling of folding and binding for unstructured proteins Curr. Opin. Struct. Biol. 12 2002 54 60
53. H.J. Dyson P.E. Wright Intrinsically unstructured proteins and their functions Nat. Rev. Mol. Cell Biol. 6 2005 197 208
54. R. Kukreja B. Singh Biologically active novel conformational state of botulinum, the most poisonous poison J. Biol. Chem. 280 2005 39346 39352
55. M. Salzmann K. Pervushin G. Wider H. Senn K. Wuthrich TROSY in triple-resonance experiments: new perspectives for sequential NMR assignment of large proteins Proc. Natl Acad. Sci. USA 95 1998 13585 13590
56. M. Sattler J. Schleucher C. Griesinger Heteronuclear multidimensional NMR experiments for the structure determination of proteins in solution employing pulsed field gradients Prog. Nucl. Magn. Reson. Spectrosc. 34 1999 93 158
57. F. Delaglio S. Grzesiek G.W. Vuister G. Zhu J. Pfeifer A. Bax NMRPipe—a multidimensional spectral processing system based on UNIX pipes J. Biomol. NMR 6 1995 277 293
58. Goddard, T., & Kneller, D.G. (2006). SPARKY 3. University of California, San Francisco.
59. D.A. Hall C.W. Vander Kooi C.N. Stasik S.Y. Stevens E.R. Zuiderweg R.G. Matthews Mapping the interactions between flavodoxin and its physiological partners flavodoxin reductase and cobalamin-dependent methionine synthase Proc. Natl Acad. Sci. USA 98 2001 9521 9526