The ionization of a buried glutamic acid is thermodynamically linked to the stability of Leishmania mexicana triose phosphate isomerase

European Journal of Biochemistry

Volumn 267, Issue 9, 2000, Pages 2516-2524

  Lambeir, Anne Marie ^a   Backmann, Jan ^b   Ruiz Sanz, Javier ^d   Filimonov, Vladimir ^d   Nielsen, Jens Erik ^c   Kursula, Inari ^d   Norledge, Brian V ^d   Wierenga, Rik K ^d  

^a UNIVERSITY OF ANTWERP   (Belgium)

^b VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^d NONE

Author keywords

Leishmania mexicana; PK(a) calculations; Stability; Triose phosphate isomerase

Indexed keywords

GLUTAMIC ACID; TRIOSEPHOSPHATE ISOMERASE;

ARTICLE; CRYSTAL STRUCTURE; ENZYME ACTIVITY; LEISHMANIA; LEISHMANIA MEXICANA; MOLECULAR CLONING; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; SITE DIRECTED MUTAGENESIS; THERMODYNAMICS; X RAY CRYSTALLOGRAPHY;

ANIMALS; CRYSTALLOGRAPHY, X-RAY; DIMERIZATION; ENZYME STABILITY; GLUTAMIC ACID; GUANIDINE; HYDROGEN-ION CONCENTRATION; IONS; LEISHMANIA MEXICANA; MUTAGENESIS, SITE-DIRECTED; PROTEIN DENATURATION; THERMODYNAMICS; TRIOSE-PHOSPHATE ISOMERASE;

LEISHMANIA MEXICANA; PROTOZOA;

EID: 0034111423     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1432-1327.2000.01254.x     Document Type: Article

References (44)

1. a shifts for aspartic acid: relevance to protein mechanisms. Biopolymers 34, 889-896.
2. 2. Stites, W.E., Gittis, A.G., Lattman, E.E. & Shortle, D. (1991) In a staphylococcal nuclease mutant the side-chain of a lysine replacing valine 66 is fully buried in the hydrophobic core. J. Mol. Biol. 221, 7-14.
3. a of 7.5. Its titration produces a related shift in global stability. Biochemistry 30, 7603-7609.
4. a. Biochemistry 30, 7609-7614.
5. 5. Qasim, M.A., Ranjbar, M.R., Wynn, R., Anderson, S. & Laskowski, M. Jr (1995) Ionizable P1 residues in serine proteinase inhibitors undergo large pK shifts on complex formation. J. Biol. Chem. 270, 27419-27422.
6. 6. Garcia-Moreno, B.E., Dwyer, J.J., Gittis, A.G., Lattman, E.E., Spencer, D.S. & Stites, W.E. (1997) Experimental measurement of the effective dielectric in the hydrophobic core of a protein. Biophys. Chem. 64, 211-224.
7. 7. Quirk, D.J., Park, C., Thompson, J.E. & Raines, R.T. (1998) His**Asp catalytic dyad of ribonuclease A: conformational stability of the wild-type, D121N, D121A, and H119A enzymes. Biochemistry 37, 17958-17964.
8. 8. Kohl, L., Callens, M., Wierenga, R.K., Opperdoes, F.R. & Michels, P.A.M. (1994) Triose-phosphate isomerase of Leishmania mexicana mexicana. Cloning and characterisation of the gene, overexpression in Escherichia coli and analysis of the protein. Eur. J. Biochem. 220, 331-338.
9. 9. Wierenga, R.K., Kalk, K.H. & Hol, W.G.J. (1987) Structure determination of the glycosomal triosephosphate isomerase from Trypanosoma brucei at 2.4 Å resolution. J. Mol. Biol. 198, 109-121.
10. 10. Wierenga, R.K., Noble, M.E.M., Vriend, G., Nauche, S. & Hol, W.G.J. (1991) Refined 1.83 A structure of trypanosomal triosephosphate isomerase crystallized in the presence of 2.4 M-ammonium sulphate. A comparison with the structure of the trypanosomal triosephosphate isomerase-glycerol-3-phosphate complex. J. Mol. Biol. 220, 995-1015.
11. 11. Williams, J.C., Zeelen, J.P., Neubauer, G., Vriend, G., Backman, J., Michels, P.A.M., Lambeir, A.M. & Wierenga, R.K. (1999) Structural and mutagenesis studies of leishmania triosephosphate isomerase: a point mutation can convert a mesophilic enzyme into a superstable enzyme without loosing catalytic power. Protein Eng. 12, 243-250.
12. 12. Borchert, T.V., Radha Kishan, K.V., Zeelen, J.Ph., Schliebs, W., Thanki, N., Abagyan, R., Jaenicke, R. & Wierenga, R.K. (1995) Three new crystal structures of point mutation variants of monoTIM: conformational flexibility of loop-1, loop-4 and loop-8. Structure 3, 669-679.
13. 13. Backes, H., Berens, C., Helbl, V., Walter, S., Schmid, F.X. & Hillen, W. (1997) Combinations of the α-helix-turn-α-helix motif of tetR with respective residues from LacI or 434Cro: DNA recognition, inducer binding, and urea dependent denaturation. Biochemistry 36, 5311-5322.
14. 14. Otwinowski, Z. & Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326.
15. 15. Collaborative Computational Project, 4. (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D50, 760-763.
16. 16. Jones, T.A., Zou, J.-Y., Cowan, S.W. & Kjeldgaard, M. (1991) Improved methods for the building of protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A47, 110-119.
17. 17. Murshudov, G.N., Vagin, A.A. & Dodson, E.J. (1997) Refinement of macromolecular structures by the maximum likelihood method. Acta Crystallogr. D53, 240-255.
18. 18. Noble, M.E.M., Zeelen, J.P. & Wierenga, R.K. (1993) Structure of triosephosphate isomerase from Escherichia coli determined at 2.6 Å resolution. Acta Crystallogr. D 49, 403-417.
19. 19. Vriend, G. (1990) WHAT IF: a molecular modeling and drug design program. J. Mol. Graphics 8, 52-56.
20. 20. Hooft, R.W., Sander, C. & Vriend, G. (1996) Positioning hydrogen atoms by optimizing hydrogen bonds. Proteins 26, 263-376.
21. 21. Nielsen, J.E., Andersen, K.V., Honig, B.H., Hooft, R.W.W., Klebe, G., Vriend, G. & Wade, R.C. (1999) Improving Macromolecular electrostatics calculations. Protein Eng. 12, 657-662.
22. 22. Tanford, C. (1970) Protein denaturation (Part C), theoretical models for the mechanism of denaturation. Adv. Protein Chem. 25, 1-95.
23. 23. Yang, A.S. & Honig, B. (1993) On the pH dependence of protein stability. J. Mol. Biol. 231, 459-474.
24. 28. Pfeil, N. (1998) Stability and co-operative properties of partially folded proteins. Biochemistry (Moscow) 63, 294-302.
25. 29. Sun, A.-Q., Yuksel, K.U. & Gracy, R.W. (1993) Limited proteolysis of triose-phosphate isomerase and characterization of the catalytically active peptide complex. J. Biol. Chem. 268, 26872-26878.
26. 30. Rietveld, A.W.M. & Ferreira, S.T. (1998) Kinetics and energetics of subunit dissociation/unfolding of TIM: the importance of oligomerisation for conformational persistence and chemical stability of proteins. Biochemistry 37, 933-937.
27. 31. Gokhale, R.S., Ray, S.S., Balaram, H. & Balaram, P. (1999) Unfolding of Plasmodium falciparum triosephosphate isomerase in urea and guanidinium chloride: evidence for a novel disulfide exchange reaction in a covalently cross-linked mutant. Biochemistry 38, 423-431.
28. 32. Myers, J.K., Pace, C.N. & 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.
29. 33. Maes, D., Zeelen, J.Ph., Thanki, N., Beaucamp, N., Alvarez, M., Dao Thi, M.H., Backman, J., Martial, J., Weyns, L., Jeanicke, R. & Wierenga, R.K. (1999) The crystal structure of triosephosphate isomerase (TIM) from Thermotoga maritime: a comparative thermostability structural analysis of ten different TIM structures. Proteins 37, 441-453.
30. 34. Mainfroid, V., Terpstra, P., Beauregard, M., Frere, J.-M., Mande, S.C., Hol, W.G.J., Martial, J.A. & Goraj, K. (1996) Three hTIM mutants that provide new insights on why TIM is a dimer. J. Mol. Biol. 257, 441-456.
31. 35. Zabori, S., Rudolph, R. & Jaenicke, R. (1980) Folding and association of triosephosphate isomerase from rabbit muscle. Z. Naturforsch. [C] 35, 999-1004.
32. 24. Schellmann, J.A. (1975) Macromolecular binding. Biopolymers 14, 999-1018.
33. 25. Yang, A.S. & Honig, B. (1992) Electrostatic effects on protein stability. Curr. Opin. Struct. Biol. 2, 40-45.
34. 36. Alber, T., Dao-pin, S., Wilson, K., Wozniak, J.A., Cook, S.P. & Matthews, B.W. (1987) Contributions of hydrogen bonds of Thr157 to the thermodynamic stability of phage T4 lysozyme. Nature (London) 330, 41-46.
35. 37. Baker, E.N. & Hubbard, R.E. (1984) Hydrogen bonding in globular proteins. Progr. Biophys. Mol. Biol. 44, 97-179.
36. 38. Fersht, A.R. (1987) The hydrogen bond in molecular recognition. Trends Biochem. Sci. 12, 301-305.
37. 39. Fersht, A.R., Shi, J.-P., Knill-Jones, J., Lowe, D.M., Wilkinson, A.J., Blow, D.M., Brick, P., Carter, P., Waye, M.M.Y. & Winter, G. (1985) Hydrogen bonding and biological specificity analysed by protein engineering. Nature (London) 314, 235-238.
38. 40. Shirley, B.A., Stanssens, P., Hahn, U. & Pace, C.N. (1992) Contribution of hydrogen bonding to the conformational stability of ribonuclease T1. Biochemistry 31, 725-732.
39. 41. Williams, M.A., Goodfellow, J.M. & Thornton, J.M. (1994) Buried waters and internal cavities in monomeric proteins. Protein Sci. 3, 1224-1235.
40. 42. Schliebs, W., Thanki, N., Eritja, R. & Wierenga, R. (1996) Active site properties of monomeric triosephosphate isomerase (monoTIM) as deduced from mutational and structural studies. Protein Sci. 5, 229-239.
41. 43. Neet, K.E. & Timm, D.E. (1994) Conformational stability of dimeric proteins: quantitative studies by equilibrium denaturation. Protein Sci. 3, 2167-2174.
42. 44. Janin, J. (1995) Principles of protein-protein recognition from structure to thermodynamics. Biochimie 77, 497-505.
43. 26. Antosiewicz, J., McCammon, J.A. & Gilson, M.K. (1994) Prediction of pH-dependent properties of proteins. J. Mol. Biol. 238, 415-436.
44. 27. Sham, Y.Y., Muegge, I. & Warshel, A. (1998) The effect of protein relaxation on charge - charge interactions and dielectric constants of proteins. Biophys. J. 74, 1744-1753.