Thermodynamic analysis of the structural stability of the Shiga toxin B-subunit

Biochemistry

Volumn 42, Issue 31, 2003, Pages 9498-9506

  Pina, David G ^a   Gómez, Javier ^b   Villar, Enrique ^a   Johannes, Ludger ^c   Shnyrov, Valery L ^a  

^a UNIVERSITY OF SALAMANCA   (Spain)

^b MIGUEL HERNÁNDEZ UNIVERSITY   (Spain)

^c INSTITUT CURIE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

DIFFERENTIAL SCANNING CALORIMETRY; IONIZATION; MOLECULAR STRUCTURE; OLIGOMERS; PH EFFECTS; SOLVENTS; THERMODYNAMICS;

STRUCTURAL STABILITY;

PROTEINS;

PROTEIN SUBUNIT; SHIGA TOXIN; SHIGA TOXIN B SUBUNIT; SOLVENT; UNCLASSIFIED DRUG;

ARTICLE; CALCULATION; CIRCULAR DICHROISM; DIFFERENTIAL SCANNING CALORIMETRY; ENERGY; ESCHERICHIA COLI; MOLECULAR INTERACTION; NONHUMAN; OLIGOMERIZATION; PH; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN STABILITY; SHIGELLA DYSENTERIAE; THERMODYNAMICS;

AMINO ACID SEQUENCE; CALORIMETRY, DIFFERENTIAL SCANNING; CIRCULAR DICHROISM; HYDROGEN-ION CONCENTRATION; KINETICS; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN SUBUNITS; SHIGA TOXIN; TEMPERATURE; THERMODYNAMICS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; SHIGELLA DYSENTERIAE;

EID: 0042572519     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi034591s     Document Type: Article

References (48)

1. Falnes, P. O., and Sandvig, K. (2000) Penetration of protein toxins into cells, Curr. Opin. Cell Biol. 12, 407-413.
2. Sandvig, K., and van Deurs, B. (1996) Endocytosis, intracellular transport, and cytotoxic action of Shiga toxin and ricin, Physiol. Rev. 76, 949-966.
3. Donohue-Rolfe, A., Jacewicz, M., and Keusch, G. T. (1989) Isolation and characterization of functional Shiga toxin subunits and renatured holotoxin, Mol. Microbiol. 3, 1231-1236.
4. Nichols, B. J., Kenworthy, A. K., Polishchuk, R. S., Lodge, R., Roberts, T. H., Hirschberg, K., Phair, R. D., and Lippincott-Schwartz, J. (2001) Rapid cycling of lipid raft markers between the cell surface and Golgi complex, J. Cell Biol. 153, 529-541.
5. Sandvig, K., Olsnes, S., Brown, J. E., Petersen, O. W. and van Deurs, B. (1989) Endocytosis from coated pits of Shiga toxin: a glycolipid-binding protein from Shigella dysenteriae 1, J. Cell Biol. 108, 1331-1343.
6. Sandvig, K., Garred, O., Prydz, K., Kozlov, J. V., Hansen, S. H., and van Deurs, B. (1992) Retrograde transport of endocytosed Shiga toxin to the endoplasmic reticulum, Nature 358, 510-512.
7. Johannes, L., and Goud, B. (1998) Surfing on a retrograde wave: how does Shiga toxin reach the endoplasmic reticulum? Trends Cell Biol, 8, 158-162.
8. Johannes, L. (2002) The epithelial cell cytoskeleton and intracellular trafficking I. Shiga toxin B-subunit system: retrograde transport, intracellular vectorization, and more, Am. J. Physiol.: Gastrointest. Liver Physiol. 283, G1-G7.
9. Sandvig, K., and van Deurs, B. (2002) Transport of protein toxins into cells: pathways used by ricin, cholera toxin, and Shiga toxin, FEBS Lett. 529, 49-53.
10. Hazes, B., and Read, R. J. (1997) Accumulating evidence suggests that several AB-toxins subvert the endoplasmic reticulum-associated protein degradation pathway to enter target cells, Biochemistry 36, 11051-11054.
11. Wesche, J., Rapak, A., and Olsnes, S. (1999) Dependence of ricin toxicity on translocation of the ricin A-chain from the endoplasmic reticulum to the cytosol, J. Biol. Chem. 274, 34443-34449.
12. Haicheur, N., Bismuth, E., Bosset, S., Adotevi, O., Waier, O., Lacabanne, V., Regnault, A., Desaymard, C., Amigorena, S., Riccardi-Castagnoli, P., Goud, B., Fridman, W. H., Johannes, L., and Tartour, E. (2000) The B-subunit of Shiga toxin fused to a tumor antigen elicits CTL and targets dendritic cells to allow MHC class I restricted presentation of peptides derived from exogenous antigens, J. Immunol. 165, 3301-3308.
13. Stein, P. E., Boodhoo, A., Tyrell, G. J., Brunton, J. L., and Read, R. J. (1992) Crystal structure of the cell-binding B oligomer of verotoxin-1 from Escherichia coli, Nature 355, 748-750.
14. Richardson, J. M., Evans, P. D., Homans, S. W., and Donohue-Rolfe, A. (1997) Solution structure of the carbohydrate-binding B-subunit homopentamer of verotoxin VT-1 from Escherichia coli, Nat. Struct. Biol. 4, 190-193.
15. Fraser, M. E., Chernaya, M. M., Kozlov, Y. V., and James, M. N. (1994) Crystal structure of the holotoxin from Shigella dysenteriae at 2.5 Å resolution, Nat. Struct. Biol. 1, 59-64.
16. 3, Biochemistry 37, 1777-1788.
17. Shimizu, H., Field, R. A., Homans, S. W., and Donohue-Rolfe, A. (1998) Solution structure of the complex between the B-subunit homopentamer of verotoxin VT-1 from Escherichia coli and the trisaccharide moiety of globotriaosylceramide, Biochemistry 37, 11078-11082.
18. Privalov, P. L. (1979) Stability of proteins: small globular proteins, Adv. Protein Chem. 33, 167-239.
19. Freire, E. (1989) Statistical thermodynamic analysis of the heat capacity function associated with protein folding-unfolding transitions, Comm. Mol. Cell Biophys. 6, 123-140.
20. Freire, E. (1995) Thermal denaturation methods in the study of protein folding, Methods Enzymol. 259, 145-168.
21. Sanchez-Ruiz, J. M. (1995) Differential scanning calorimetry of proteins, in Subcellular Biochemistry 24. Proteins: structure, function and engineering (Biswas, B. B., and Siddhartha, R., Eds.) pp 133-166, Plenum Press, New York.
22. Gómez, J., and Freire, E. (1995) Thermodynamic mapping of the inhibitor binding site of the aspartic protease endothiapepsin, J. Mol. Biol. 252, 337-350.
23. Gómez, J., Hilser, V. J., Xie, D., and Freire, E. (1995) The heat capacity of proteins, Proteins: Struct., Funct., Genet. 22, 404-412.
24. Hilser, V. J., Gómez, J., and Freire, E. (1996) The enthalpy change in protein folding and binding: refinement of parameters for structure-based calculations, Proteins: Struct., Funct., Genet. 26, 123-133.
25. D'Aquino, J. A., Gómez, J., Hilser, V. J., Lee, K. H., Amzel, M. L., and Freire, E. (1996) The magnitude of the backbone conformational entropy change in protein folding, Proteins: Struct., Funct., Genet. 25, 143-156.
26. Johannes, L., Tenza, D., Antony, C., and Goud, B. (1997) Retrograde transport of KDEL-bearing B-fragment of Shiga toxin, J. Biol. Chem. 272, 19554-19561.
27. Saleh, M. T., and Gariepy, J. (1993) Local conformational change in the B-subunit of Shiga-like toxin 1 at endosomal pH, Biochemistry 32, 918-922.
28. Shnyrov, V. L., Villar, E., Zhadan, G. G., Sanchez-Ruiz, J. M., Quintas, A., Saraiva, M. J. M., and Brito, R. M. M. (2000) Comparative calorimetric study of nonamyloidogenic and amyloidogenic variants of the homotetrameric protein transthyretin, Biophys. Chem. 88, 61-67.
29. Murphy, K. P., and Freire, E. (1992) Thermodynamics of structural stability and cooperativity of folding behavior in proteins, Adv. Protein Chem. 43, 313-361.
30. Spolar, R. S., Livingstone, J. R., and Record, M. T., Jr. (1992) Use of liquid hydrocarbon and amide transfer data to estimate contributions to thermodynamic functions of protein folding from the removal of nonpolar and polar surface from water, Biochemistry 31, 3947-3955.
31. Baker, B. M., and Murphy, K. P. (1997) Prediction of binding energetics of a protein-protein interaction: The binding of ovomucoid third domain to elastase, J. Mol. Boil. 268, 557-569.
32. Baldwin, R. L. (1986) Temperature dependence of the hydrophobic interaction in protein folding, Proc. Natl. Acad. Sci. U.S.A. 83, 8069-8072.
33. Lee, K. H., Xie, D., Freire, E., and Amzel, L. M. (1994) Estimation of changes in side chain configurational entropy in binding and folding: general methods and application to helix formation, Proteins 20, 68-84.
34. Gurney, R. W. (1953) Ionic Processes in Solution, McGraw-Hill, New York.
35. Kauzman, W. (1959) Some factors in the interpretation of protein denaturation, Adv. Protein Chem. 14, 1-63.
36. Holtzer, A. (1995) The "cratic correction" and related fallacies, Biopolymers 35, 595-602.
37. Gilson, M. K., Given, J. A., Bus, B. L., and McCammon, J. A. (1997) The statistical-thermodynamic basis for computation of binding affinities: a critical review, Biophys J. 72, 1047-1069.
38. Tamura, A., and Privalov, P. L. (1997). The entropy of protein association, J. Mol. Biol. 273, 1048-1060.
39. Yu, Y., Lavigne, P., Kay, C. M., Hodges, R. S., and Privalov, P. L. (1998) Contribution of translational and rotational entropy to the unfolding of a dimeric coiled-coil, J. Phys. Chem. B 103, 2270-2278.
40. Amzel, L. M. (1996) Loss of translational entropy in binding, folding, and catalysis, Proteins: Struct., Funct., Genet. 29, 1-6.
41. Lee, B., and Richards, F. M. (1971) The interpretation of protein structures: estimation of static accessibility, J. Mol. Biol. 55, 379-400.
42. Venyaminov, S. Y., and Vasilenko, K. S. (1994) Determination of protein tertiary structure class from circular dichroism spectra, Anal. Biochem. 222, 176-184.
43. Wyman, J., and Gill, S. J. (1990) Binding and Linkage, pp 1-330, University Science Books, Mill Valley, CA.
44. Greene, R. F., and Pace, C. N. (1974) Urea and guanidine hydrochloride denaturation of ribonuclease, lysozyme, α-chymotrypsin, and β-lactoglobulin, J. Biol. Chem. 249, 5388-5393.
45. Myers, J. K., Pace, C. N., and Scholtz, J. M. (1995) Denaturant m values and heat capacity changes: Relation to changes in accessible surface areas of protein unfolding, Protein Sci. 4, 2138-2148.
46. Johnson, C. R., Morin, P. E., Arrowsmith, C. H., and Freire, E. (1995) Thermodynamic analysis of the structural stability of the tetrameric oligomerization domain of p53 tumor suppressor, Biochemistry 34, 5309-5316.
47. Kenar, K. T., García-Moreno, B., and Freire, E. (1995) A calorimetric characterization of the salt dependence of the stability of the GCN4 leucine zipper, Protein Sci. 4, 1934-1938.
48. Boudker, O., Todd, M. J., and Freire, E. (1997) The structural stability of the co-chaperonin GroES, J. Mol. Biol. 272, 770-779.