Comparison of solution structures and stabilities of native, partially unfolded and partially refolded pepsin

Biochemistry

Volumn 45, Issue 47, 2006, Pages 13982-13992

  Dee, Derek ^a   Pencer, Jeremy ^b,c   Nieh, Mu Ping ^b   Krueger, Susan ^d   Katsaras, John ^a,b   Yada, Rickey Y ^a  

^a UNIVERSITY OF GUELPH   (Canada)

^b NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^c ST FRANCIS XAVIER UNIVERSITY   (Canada)

^d NATIONAL INSTITUTE OF STANDARDS AND TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CONFORMATIONS; DATA REDUCTION; DIFFERENTIAL SCANNING CALORIMETRY; NEUTRON SCATTERING; THERMODYNAMICS;

PEPSIN; PROTEIN CONCENTRATION; SMALL ANGLE NEUTRON SCATTERING (SANS); TERTIARY STRUCTURES;

PROTEINS;

PEPSIN A;

ARTICLE; CIRCULAR DICHROISM; CONFORMATIONAL TRANSITION; DIFFERENTIAL SCANNING CALORIMETRY; NEUTRON SCATTERING; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY; PROTEIN STRUCTURE; THERMODYNAMICS;

ANIMALS; CALORIMETRY, DIFFERENTIAL SCANNING; CIRCULAR DICHROISM; DEUTERIUM OXIDE; MODELS, MOLECULAR; NEUTRONS; PEPSIN A; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN FOLDING; SCATTERING, RADIATION; SWINE; WATER;

SUIDAE;

EID: 33751558596     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi061270i     Document Type: Article

References (61)

1. Jackson, S. E. (1998) How do small single-domain proteins fold? Folding Des. 3, R81-R91.
2. Daggett, V., and Fersht, A., R. (2003) Is there a unifying mechanism for protein folding? Trends Biochem. Sci. 28, 18-25.
3. Radford, S. (2000) Protein folding: progress made and promise ahead, Trends Biochem. Sci. 25, 611-618.
4. Anfinsen, C. B. (1973) Principles that govern the folding of protein chains, Science 181, 223-230.
5. Brown, E. D., and Yada, R. Y. (1991) A kinetic and equilibrium study of the denaturation of aspartic proteinases from the fungi, Endothia parasitica and Mucor miehei, Biochim. Biophys. Acta. 1076, 406-415.
6. Song, J., Xu, P., Xiang, H., Su, Z., Storer, A. C., and Ni, F. (2000) The active-site residue cys-29 is responsible for the neutral-pH inactivation and the refolding barrier of human cathepsin B, FEBS Lett. 475, 157-162.
7. Beldarrain, A., Acosta, N., Montesinos, R., Mata, M., and Cremata, J. (2000) Characterization of Mucor pusillus rennin expressed in Pichia pastoris: enzymic, spectroscopic and calorimetric studies, Biotechnol. Appl. Biochem. 31, 77-84.
8. Solís-Mendiola, S., Gutiérrez-González, L. H., Arroyo-Reyna, A., Padilla-Zúñiga, J., Rojo-Domínguez, A., and Hernández-Arana, A. (1998) pH dependence of the activation parameters for chymopapain unfolding: influence of ion pairs on the kinetic stability of proteins, Biochim. Biophys. Acta. 1388, 363-372.
9. Baker, D., Shiau, A. K., and Agard, D. A. (1993) The role of pro regions in protein folding, Curr. Opin. Cell Biol. 5, 966-970.
10. Dunn, B. M. (2002) Structure and mechanism of the pepsin-like family of aspartic peptidases, Chem. Rev. 102, 4431-4458.
11. Richter, C., Tanaka, T., and Yada, R. Y. (1998) Mechanism of activation of the gastric aspartic proteinases: pepsinogen, progastricsin and prochymosin, Biochem. J. 335, 481-490.
12. Lin, X., Wong, R. N. S., and Tang, J. (1989) Synthesis, purification, and active site mutagenesis of recombinant porcine pepsinogen, J. Biol. Chem. 264, 4482-4489.
13. Sielecki, A. R., Fedorov, A. A., Boodhoo, A., Andreeva, N. S., and James, M. N. G. (1990) Molecular and crystal structures of monoclinic porcine pepsin refined at 1.8 A resolution, J. Mol. Biol. 214, 143-170.
14. Ahmad, F., and McPhie, P. (1978) Thermodynamics of the denaturation of pepsinogen by urea, Biochemistry 17, 241-246.
15. Frattali, V., Steiner, R. F., and Edelhoch, H. (1965) Native and unfolded states of pepsinogen. I. The molecular conformation in water and in urea, J. Biol. Chem. 240, 112-121.
16. Ahmad, F., and McPhie, P. (1978) The denaturation of covalently inhibited swine pepsin, Int. J. Pept. Protein Res. 12, 155-163.
17. McPhie, P. (1989) A reversible unfolding reaction of swine pepsin; implications for pepsinogen's folding mechanism, Biochem. Biophys. Res. Commun. 158, 115-119.
18. Privalov, P. L., Mateo, P. L., Khechinashvili, N. N., Stepanov, V. M., and Revina, L. P. (1981) Comparative thermodynamic study of pepsinogen and pepsin structure, J. Mol. Biol. 152, 445-464.
19. Lin, X. L., Loy, J. A., Sussman, F., and Tang, J. (1993) Conformational instability of the N- and C-terminal lobes of porcine pepsin in neutral and alkaline solutions, Protein Sci. 2, 1383-1390.
20. Tanaka, T., and Yada, R. Y. (2001) N-terminal portion acts as an initiator of the inactivation of pepsin at neutral pH, Protein Eng. 14, 669-674.
21. Konno, T., Kamatari, Y. O., Tanaka, N., Kamikubo, H., Dobson, C. M., and Nagayama, K. (2000) A partially unfolded structure of the alkaline-denatured state of pepsin and its implication for stability of the zymogen-derived protein, Biochemistry 39, 4182-4190.
22. Kamatari, Y. O., Dobson, C. M., and Konno, T. (2003) Structural dissection of alkaline-denatured pepsin, Protein Sci. 12, 717-724.
23. Yada, R. Y., and Nakai, S. (1986) Secondary structure of some aspartyl proteinases, J. Food Biochem. 10, 155-183.
24. Favilla, R., Parisoli, A., and Mazzini, A. (1997) Alkaline denaturation and partial refolding of pepsin investigated with DAPI as an extrinsic probe, Biophys. Chem. 67, 75-83.
25. Dunn, B. M., Jimenez, M., Parten, B. F., Valler, M. J., Rolph, C. E., and Kay, J. (1986) A systematic series of synthetic chromophoric substrates for aspartic proteinases, Biochem. J. 237, 899-906.
26. Svergun, D., Richard, S., Koch, M., Sayers, Z., Kuprin, S., and Zaccai, G. (1998) Protein hydration in solution: experimental observation by X-ray and neutron scattering, Proc. Natl. Acad. Sci. U.S.A. 95, 2267-2272.
27. Svergun, D. I. (1999) Restoring low resolution structure of biological macromolecules from solution scattering using simulated annealing, Biophys. J. 76, 2879-2886.
28. Svergun, D. I. (1992) Determination of the regularization parameter in indirect-transform methods using perceptual criteria, J. Appl. Crystallogr. 25, 495-503.
29. Svergun, D. I., Volkov, V. V., Kozin, M. B., and Stuhrmann, H. B. (1996) New developments in direct shape determination from small-angle scattering. II. Uniqueness, Acta. Crystallogr., Sect. A 52, 419-426.
30. Kratky, O., Leopold, H., and Stabinger, H. (1973) The determination of the partial specific volume of proteins by the mechanical oscillator technique, Methods Enzymol. 27, 98-110.
31. Epand, R. M., and Epand, R. F. (1980) Studies of thermotropic phospholipid phase transitions using scanning densitometry, Chem. Phys. Lipids 27, 139-150.
32. 2O, J. Protein Chem. 17, 479-484.
33. 2O, FEBS Lett. 421, 273-276.
34. Chakrabarti, G., Kim, S., Gupta, M. L., Barton, J. S., and Himes, R. H. (1999) Stabilization of tubulin by deuterium oxide, Biochemistry 38, 3067-3072.
35. Russo, D., Durand, D., Calmettes, P., and Desmadril, M. (2001) Characterization of the denatured states distribution of neocarzinostatin by small-angle neutron scattering and differential scanning calorimetry, Biochemistry 40, 3958-3966.
36. Bonnete, F., Madern, D., and Zaccai, G. (1994) Stability against denaturation mechanisms in halophilic malate dehydrogenase adapt to solvent conditions, J. Mol. Biol. 244, 436-447.
37. Pederson, J. S., Hansen, S., and Bauer, R. (1994) The aggregation behavior of zinc-free insulin studied by small-angle neutron scattering, Eur. Biophys. J. 22, 379-389.
38. Tuinier, R., and Brûlet, A. (2003) On the long-range attraction between proteins due to nonadsorbing polysaccharide, Biomacromolecules 4, 28-31.
39. Glatter, O. (1979) The interpretation of real-space information from small-angle scattering experiments, J. Appl. Crystallogr. 12, 166-175.
40. Horn, D., and Heuck, C. (1983) Charge determination of proteins with polyelectrolyte titration, J. Biol Chem. 258, 1665-1670.
41. Glatter, O. (1982) Interpretation, in Small-Angle X-ray Scattering (Glatter, O., and Kratky, O., Eds.) pp 167-196, Academic Press: New York.
42. Glatter, O. (1977) A new method for the evaluation of small-angle scattering data, J. Appl. Crystallogr. 10, 415-421.
43. Kanjilal, S., Taulier, N., Le Huerou, J.-Y., Gindre, M., Urbach, W., and Waks, M. (2003) Ultrasonic studies of alcohol-induced transconformation in β-lactoglobulin: the intermediate state, Biophys. J. 85, 3928-3934.
44. Sreerema, N., and Woody, R. W. (1993) A self-consistent method for the analysis of protein secondary structure from circular dichroism, Anal. Biochem. 209, 32-44.
45. Van Stokkum, I. H. M., Spoelder, H. J. W., Bloemendal, M., Van Grondelle, R., and Groen, F. C. A. (1990) Estimation of protein secondary structure and error analysis from CD spectra, Anal. Biochem. 191, 110-118.
46. Manavalan, P., and Johnson, W. C., Jr. (1987) Variable selection method improves the prediction of protein secondary structure from circular dichroism spectra, Anal. Biochem. 167, 76-85.
47. Whitmore, L., and Wallace, B. A. (2004) DICHROWEB, an online server for protein secondary structure analyses from circular dichroism spectroscopic data, Nucleic Acids Res. 32, W668-W673.
48. Lobley, A., Whitmore, L., and Wallace, B. A. (2002) DICHROWEB: an interactive website for the analysis of protein secondary structure from circular dichroism spectra, Bioinformatics 18, 211-212.
49. Kelly, S. M., Jess, T. J., and Price, N. C. (2005) How to study proteins by circular dichroism, Biochim. Biophys. Acta. 1751, 119-139.
50. Lakowicz, J. R. (2000) Topics in Fluorescence Spectroscopy: Protein Fluorescence. Kluwer Academic/Plenum Publishers, New York.
51. Burstein, E. A., Vedenkina, N. S., and Ivkova, M. N. (1973) Fluorescence and the location of tryptophan residues in protein molecules, Photochem. Photobiol. 18, 263-279.
52. Privalov, P. L., and Potekhin, S. A. (1986) Scanning microcalorimetry in studying temperature-induced changes in proteins, Methods Enzymol. 131, 4-51.
53. Yoshimasu, M. A., Tanaka, T., Ahn, J.- K., and Yada, R. Y. (2004) Effect of N-linked glycosylation on the aspartic proteinase porcine pepsin expressed from Pichia pastoris, Glycobiology 14, 417-429.
54. O'Brian, R., and Haq, I. (2004) Applications of Biocalorimetry: Binding, Stability and Enzyme Kinetics, in Biocalorimetry II: Applications of Calorimetry in the Biological Sciences (Ladbury, J. E., and Doyle, M. L., Eds.) pp 1-34, John Wiley & Sons, Ltd., West Sussex, England.
55. Baker, D., and Agard, D. A. (1994) Kinetics versus thermodynamics in protein folding, Biochemistry 33, 7505-7509.
56. Jaswal, S. S., Truhlar, S. M., Dill, K. A., and Agard, D. A. (2005) Comprehensive analysis of protein folding activation thermodynamics reveals a universal behavior violated by kinetically stable proteases, J. Mol. Biol. 347, 355-366.
57. Sohl, J. L., Jaswal, S. S., and Agard, D. A. (1998) Unfolded conformations of alpha-lytic protease are more stable than its native state, Nature 395, 817-819.
58. Baker, D., Sohl, J. L., and Agard, D. A. (1992) A protein-folding reaction under kinetic control, Nature 356, 263-265.
59. Truhlar, S. M. E., Cunningham, E. L., and Agard, D. A. (2004) The folding landscape of Streptomyces griseus protease B reveals the energetic costs and benefits associated with evolving kinetic stability, Protein Sci. 13, 381-390.
60. Eder, J., Rheinnecker, M., and Fersht, A. R. (1993) Folding of subtilisin BPN′: characterization of a folding intermediate, Biochemistry 32, 18-26.
61. Kurimoto, E., Harada, T., Akiyama, A., Sakai, T., and Kato, K. (2001) In vitro refolding of porcine pepsin immobilized on agarose beads, J. Biochem. 130, 295-297.