IA3, An Aspartic Proteinase Inhibitor from Saccharomyces cerevisiae, Is Intrinsically Unstructured in Solution

Biochemistry

Volumn 43, Issue 14, 2004, Pages 4071-4081

  Green, Terry B ^a   Ganesh, Omjoy ^a   Perry, Kyle ^a   Smith, Leif ^a   Phylip, Lowri H ^b   Logan, Timothy M ^c,d   Hagen, Stephen J ^e   Dunn, Ben M ^a   Edison, Arthur S ^a,d  

^a UNIVERSITY OF FLORIDA   (United States)

^b CARDIFF UNIVERSITY   (United Kingdom)

^c FLORIDA STATE UNIVERSITY   (United States)

^d FLORIDA STATE UNIVERSITY   (United States)

^e NONE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CALORIMETRY; DATA ACQUISITION; DECOMPOSITION; ENTHALPY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; POLYPEPTIDES; PROTEINS; SPECTRUM ANALYSIS; X RAY ANALYSIS; YEAST;

CIRCULAR DICHROISM (CD); SINGULAR-VALUE DECOMPOSITION (SVD);

ENZYME INHIBITION;

AMINO ACID DERIVATIVE; ASPARTIC PROTEINASE INHIBITOR; BINDING PROTEIN; FUNGAL PROTEIN; POLYPEPTIDE; PROTEIN IA3; PROTEIN YPRA; UNCLASSIFIED DRUG; ASPARTIC PROTEINASE; ASPARTIC PROTEINASE A; LIGAND; PAI3 PROTEIN, S CEREVISIAE; PROTEINASE INHIBITOR; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; CALORIMETRY; CIRCULAR DICHROISM; CRYSTAL STRUCTURE; ENTHALPY; NITROGEN NUCLEAR MAGNETIC RESONANCE; NONHUMAN; NUCLEAR OVERHAUSER EFFECT; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; SACCHAROMYCES CEREVISIAE; X RAY CRYSTALLOGRAPHY; AMINO ACID SEQUENCE; CHEMISTRY; DRUG ANTAGONISM; ENZYME SPECIFICITY; METABOLISM; MOLECULAR GENETICS; NUCLEAR MAGNETIC RESONANCE; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN SECONDARY STRUCTURE; SOLUTION AND SOLUBILITY; THERMODYNAMICS;

SACCHAROMYCES; SACCHAROMYCES CEREVISIAE;

AMINO ACID SEQUENCE; ASPARTIC ENDOPEPTIDASES; CIRCULAR DICHROISM; LIGANDS; MOLECULAR SEQUENCE DATA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEASE INHIBITORS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY; SACCHAROMYCES CEREVISIAE PROTEINS; SOLUTIONS; SUBSTRATE SPECIFICITY; THERMODYNAMICS;

EID: 1842531458     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi034823n     Document Type: Article

References (54)

1. Dreyer, T., Valler, M. J., Kay, J., Charlton, P., and Dunn, B. M. (1985) The selectivity of action of the aspartic-proteinase inhibitor IA3 from yeast (Saccharomyces cerevisiae), Biochem. J. 231, 777-779.
2. Phylip, L. H., Lees, W. E., Brownsey, B. G., Bur, D., Dunn, B. M., Winther, J. R., Gustchina, A., Li, M., Copeland, T., Wlodawer, A., and Kay, J. (2001) The potency and specificity of the interaction between the IA3 inhibitor and its target aspartic proteinase from Saccharomyces cerevisiae, J. Biol. Chem. 276, 2023-2030.
3. Li, M., Phylip, L. H., Lees, W. E., Winther, J. R., Dunn, B. M., Wlodawer, A., Kay, J., and Gustchina, A. (2000) The aspartic proteinase from Saccharomyces cerevisiae folds its own inhibitor into a helix, Nat. Struct. Biol. 7, 113-117.
4. Takahashi, S., Takahashi, K., Kaneko, T., Ogasawara, H., Shindo, S., Saito, K., and Kobayashi, M. (1999) Identification of cysteine-380 as the essential residue for the human N-acetyl-D-glucosamine 2-epimerase (renin binding protein), J. Biochem. 126, 639-642.
5. Kageyama, T. (1998) Molecular cloning, expression and characterization of an Ascaris inhibitor for pepsin and cathepsin E, Eur. J. Biochem. 253, 804-809.
6. Kreft, S., Ravnikar, M., Mesko, P., Pungercar, J., Umek, A., Kregar, I., and Strukelj, B. (1997) Jasmonic acid inducible aspartic proteinase inhibitors from potato, Phytochemistry 44, 1001-1006.
7. Christeller, J. T., Farley, P. C., Ramsay, R. J., Sullivan, P. A., and Laing, W. A. (1998) Purification, characterization and cloning of an aspartic proteinase inhibitor from squash phloem exudate, Eur. J. Biochem. 254, 160-167.
8. Lenarcic, B., and Turk, V. (1999) Thyroglobulin type-1 domains in equistatin inhibit both papain-like cysteine proteinases and cathepsin D, J. Biol. Chem. 274, 563-566.
9. Ng, K. K., Petersen, J. F., Cherney, M. M., Garen, C., Zalatoris, J. J., Rao-Naik, C., Dunn, B. M., Martzen, M. R., Peanasky, R. J., and James, M. N. (2000) Structural basis for the inhibition of procine pepsin by Ascaris pepsin inhibitor-3, Nat. Struct. Biol. 7, 653-657.
10. Wright, P. E., and Dyson, H. J. (1999) Intrinsically unstructured proteins: re-assessing the protein structure-function paradigm, J. Mol. Biol. 293, 321-331.
11. Dunn, B. M., Scarborough, P. E., Davenport, R., and Swietnicki, W. (1994) Analysis of proteinase specificity by studies of peptide substrates. The use of UV and fluorescence spectroscopy to quantitate rates of enzymatic cleavage, Methods Mol. Biol. 36, 225-243.
12. Henry, E. R., and Hofrichter, J. (1992) Singular value decomposition: Application to analysis of experimental data, Methods Enzymol. 210, 129-192.
13. 15N random coil NMR chemical shifts of the common amino acids. Investigations of nearest-neighbor effects, J. Biomol. NMR 5, 67-81.
14. Schwarzinger, S., Kroon, G. J., Foss, T. R., Wright, P. E., and Dyson, H. J. (2000) Random coil chemical shifts in acidic 8 M urea: implementation of random coil shift data in NMR View, J. Biomol. NMR 18, 43-48.
15. Schwarzinger, S., Kroon, G. J., Foss, T. R., Chung, J., Wright, P. E., and Dyson, H. J. (2001) Sequence-dependent correction of random coil NMR chemical shifts, J. Am. Chem. Soc. 123, 2970-2978.
16. Piotto, M., Saudek, V., and Sklenar, V. (1992) Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions, J. Biomol. NMR 2, 661-665.
17. Bodenhausen, G., and Ruben, D. J. (1980) Natural abundance N-15 NMR by enhanced heteronuclear spectroscopy, Chem. Phys. Lett. 69, 185-189.
18. 15N NMR relaxation, Biochemistry 33, 5984-6003.
19. Marion, D., Ikura, M., Tschudin, R., and Bax, A. (1989) Rapid recording of 2D NMR spectra without phase cycling. Application to the study of hydrogen exchange in proteins, J. Magn. Reson. 85, 393-399.
20. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes, J. Biomol. NMR 6, 277-293.
21. Johnson, B. A., and Bax, A. (1994) NMR View: A computer program for the visualization and analysis of NMR data, J. Biomol. NMR 4, 603-614.
22. Grzesiek, S., and Bax, A. (1992) Improved 3D triple-resonance NMR techniques applied to a 31-kDa protein, J. Magn. Reson. 96, 432-440.
23. Kay, L. E., Ikura, M., Tschudin, R., and Bax, A. (1990) Three-dimensional triple-resonance NMR spectroscopy of isotopically enriched proteins, J. Magn. Reson. 89, 496-514.
24. Grzesiek, S., and Bax, A. (1992) Correlating backbone amide and side-chain resonances in larger proteins by multiple relayed triple resonance NMR, J. Am. Chem. Soc. 114, 6291-6293.
25. Grzesiek, S., and Bax, A. (1992) An efficient experiment for sequential backbone assignment of medium-sized isotopically enriched proteins, J. Magn. Reson. 99, 201-207.
26. 15N Hartmann-Hahn-multiple quantum coherence and nuclear Over-hauser-multiple quantum coherence spectroscopy: application to interleukin-1β, Biochemistry 28, 6150-6156.
27. Palmer, A. G., Cavanagh, J., Wright, P. E., and Rance, M. (1991) Sensitivity improvement in proton-detected two-dimensional heteronuclear correlation NMR spectroscopy, J. Magn. Reson. 93, 151-170.
28. Lyons, B. A., and Montelione, G. T. (1993) An HCCNH triple-resonance experiment using C-13 isotropic mixing for correlating backbone amide and side-chain aliphatic resonances in isotopically enriched proteins, J. Magn. Reson., Ser. B 101, 206-209.
29. Logan, T. M., Olejniczak, E. T., Xu, R. X., and Fesik, S. W. (1993) A general method for assigning NMR spectra of denatured proteins using 3D HC(CO)NH-TOCSY triple resonance experiments, J. Biomol. NMR 3, 225-231.
30. Pervushin, K., Riek, R., Wider, G., and Wuthrich, K. (1997) Attenuated T-2 relaxation by mutual cancellation of dipole-dipole coupling and chemical shift anisotropy indicates an avenue to NMR structures of very large biological macromolecules in solution, Proc. Natl. Acad. Sci. U.S.A. 94, 12366-12371.
31. Pierce, M. M., Raman, C. S., and Nall, B. T. (1999) Isothermal titration calorimetry of protein-protein interactions, Methods 19, 213-221.
32. Jelesarov, I., and Bosshard, H. R. (1999) Isothermal titration calorimetry and differential scanning calorimetry as complementary tools to investigate the energetics of biomolecular recognition, J. Mol. Recognit. 12, 3-18.
33. Holdgate, G. A. (2001) Making cool drugs hot: Isothermal titration calorimetry as a tool to study binding energetics, Drug Discovery and Genomic Technologies, BioTechniques 31, 164-186.
34. Woody, R. W. (1995) Circular dichroism, Methods Enzymol. 246, 34-71.
35. Buck, M. (1998) Trifluoroethanol and colleagues: cosolvents come of age. Recent studies with peptides and proteins, Q. Rev. Biophys. 31, 297-355.
36. Sreerama, N., and Woody, R. W. (2000) Estimation of protein secondary structure from circular dichroism spectra: comparison of CONTIN, SELCON, and CDSSTR methods with an expanded reference set, Anal. Biochem. 287, 252-260.
37. Wishart, D. S., and Sykes, B. D. (1994) Chemical shifts as a tool for structure determination, Methods Enzymol. 239, 363-392.
38. Garnier, J., Gibrat, J. F., and Robson, B. (1996) GOR method for predicting protein secondary structure from amino acid sequence, Methods Enzymol. 266, 540-553.
39. Munoz, V., and Serrano, L. (1995) Elucidating the folding problem of helical peptides using empirical parameters. III. Temperature and pH dependence, J. Mol. Biol. 245, 297-308.
40. Munoz, V., and Serrano, L. (1995) Elucidating the folding problem of helical peptides using empirical parameters. II. Helix macrodipole effects and rational modification of the helical content of natural peptides, J. Mol. Biol. 245, 275-296.
41. Farrow, N. A., Zhang, O., Forman-Kay, J. D., and Kay, L. E. (1997) Characterization of the backbone dynamics of folded and denatured states of an SH3 domain, Biochemistry 36, 2390-2402.
42. Dyson, H. J., and Wright, P. E. (2002) Coupling of binding and folding for unstructured proteins, Curr. Opin. Struct. Biol. 12, 54-60.
43. Tompa, P. (2002) Intrinsically unstructured proteins, Trends Biochem. Sci. 27, 527-533.
44. Dunker, A. K., Brown, C. J., Lawson, J. D., Iakoucheva, L. M., and Obradovic, Z. (2002) Intrinsic disorder and protein function, Biochemistry 41, 6573-6582.
45. Dunker, A. K., Obradovic, Z., Romero, P., Garner, E. C., and Brown, C. J. (2000) Intrinsic protein disorder in complete genomes, Genome Inf. Ser. 11, 161-171.
46. Parker, D., Rivera, M., Zor, T., Henrion-Caude, A., Radhakrishnan, I., Kumar, A., Shapiro, L. H., Wright, P. E., Montminy, M., and Brindle, P. K. (1999) Role of secondary structure in discrimination between constitutive and inducible activators, Mol. Cell. Biol. 19, 5601-5607.
47. Daughdrill, G. W., Chadsey, M. S., Karlinsey, J. E., Hughes, K. T., and Dahlquist, F. W. (1997) The C-terminal half of the anti-sigma factor, FlgM, becomes structured when bound to its target, sigma 28, Nat. Struct. Biol. 4, 285-291.
48. Fletcher, C. M., and Wagner, G. (1998) The interaction of eIF4E with 4E-BP1 is an induced fit to a completely disordered protein, Protein Sci. 7, 1639-1642.
49. Kim, A. S., Kakalis, L. T., Abdul-Manan, N., Liu, G. A., and Rosen, M. K. (2000) Autoinhibition and activation mechanisms of the Wiskott-Aldrich syndrome protein, Nature 404, 151-158.
50. He, X. L., Chow, D. C., Martick, M. M., and Garcia, K. C. (2001) Allosteric activation of a spring-loaded natriuretic peptide receptor dimer by hormone, Science 293, 1657-1662.
51. Pfander, R., Neumann, L., Zweckstetter, M., Seger, C., Holak, T. A., and Tampe, R. (1999) Structure of the active domain of the herpes simplex virus protein ICP47 in water/sodium dodecyl sulfate solution determined by nuclear magnetic resonance spectroscopy, Biochemistry 38, 13692-13698.
52. Kriwacki, R. W., Hengst, L., Tennant, L., Reed, S. I., and Wright, P. E. (1996) Structural studies of p21Waf1/Cip1/Sdi1 in the free and Cdk2-bound state: conformational disorder mediates binding diversity, Proc. Natl. Acad. Sci. U.S.A. 93, 11504-11509.
53. Adkins, J. N., and Lumb, K. J. (2002) Intrinsic structural disorder and sequence features of the cell cycle inhibitor p57Kip2, Proteins 46, 1-7.
54. Bienkiewicz, E. A., Adkins, J. N., and Lumb, K. J. (2002) Functional consequences of preorganized helical structure in the intrinsically disordered cell-cycle inhibitor p27(Kip1), Biochemistry 41, 752-759.