Nonadditive effects of double mutations at the flexible loops, glycine-67 and glycine-121, of Escherichia coli dihydrofolate reductase on its stability and function

Journal of Biochemistry

Volumn 123, Issue 1, 1998, Pages 33-41

  Ohmae, Eiji ^a   Iriyama, Koji ^b   Ichihara, Shigeyuki ^b   Gekko, Kunihiko ^a  

^a HIROSHIMA UNIVERSITY   (Japan)

^b NAGOYA UNIVERSITY   (Japan)

Author keywords

Dihydrofolate reductase; Double mutants; Flexible loops; Long range interactions; Stability and function

Indexed keywords

DIHYDROFOLATE REDUCTASE; GLYCINE;

AMINO ACID SUBSTITUTION; ARTICLE; CIRCULAR DICHROISM; ENZYME ACTIVITY; ENZYME STABILITY; ENZYME STRUCTURE; ESCHERICHIA COLI; MUTATION; NONHUMAN; POINT MUTATION; STEADY STATE;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; FELIS CATUS;

EID: 0031937819     PISSN: 0021924X     EISSN: None     Source Type: Journal    
DOI: 10.1093/oxfordjournals.jbchem.a021913     Document Type: Article

References (44)

1. Bolin, J.T., Filman, D.J., Matthews, D.A., Hamlin, R.C., and Kraut, J. (1982) Crystal structures of Escherichia coli and Lactobacillus casei dihydrofolate reductase refined at 1.7 Å resolution. J. Biol. Chem. 257, 13650-13662
2. + ternary complex. Substrate binding and a model for the transition state. Biochemistry 29, 3263-3277
3. Bystroff, C. and Kraut, J. (1991) Crystal structure of unliganded Escherichia coli dihydrofolate reductase: Ligand-induced conformational changes and cooperativity in binding. Biochemistry 30, 2227-2239
4. Epstein, D.M., Benkovic, S.J., and Wright, P.E. (1995) Dynamics of the dihydrofolate reductase-folate complex: catalytic sites and regions known to undergo conformational change exhibit diverse dynamical features. Biochemistry 34, 11037-11048
5. Gekko, K., Yamagami, K., Kunori, Y., Ichihara, S., Kodama, M., and Iwakura, M. (1993) Effects of point mutations in a flexible loop on the stability and enzymatic function of Escherichia coli dihydrofolate reductase. J. Biochem. 113, 74-80
6. Gekko, K., Kunori, Y., Takeuchi, H., Ichihara, S., and Kodama, M. (1994) Point mutations at glycine-121 of Escherichia coli dihydrofolate reductase: Important roles of a flexible loop in the stability and function. J. Biochem. 116, 34-41
7. Ohmae, E., Iriyama, K., Ichihara, S., and Gekko, K. (1996) Effects of point mutations at the flexible loop glycine-67 of Escherichia coli dihydrofolate reductase on its stability and function. J. Biochem. 119, 703-710
8. Shortle, D. and Meeker, A.K. (1986) Mutant forms of staphylococcal nuclease with altered patterns of guanidine hydrochloride and urea denaturation. Proteins: Struct. Funct. Genet. 1, 81-89
9. Hecht, M.H., Sturtevant, J.M., and Sauer, R.T. (1986) Stabilization of lambda repressor against thermal denaturation by site-directed Gly→Ala changes in alpha-helix 3. Proteins: Struct. Funct. Genet. 1, 43-46
10. Hurle, M.R., Tweedy, N.B., and Matthews, C.R. (1986) Synergism in folding of a double mutant of the alpha subunit of tryptophan synthase. Biochemistry 25, 6356-6360
11. Wetzel, R., Perry, L.J., Baase, W.A., and Becktel, W.J. (1988) Disulfide bonds and thermal stability in T4 lysozyme. Proc. Natl. Acad. Sci. USA 85, 401-405
12. Sandberg, W.S. and Terwilliger, T.C. (1993) Engineering multiple properties of a protein by combinatorial mutagenesis. Proc. Natl. Acad. Sci. USA 90, 8367-8371
13. Akasako, A., Haruki, M., Oobatake, M., and Kanaya, S. (1995) High resistance of Escherichia coli ribonuclease HI variant with quintuple thermostabilizing mutations to thermal denaturation, acid denaturation, and proteolytic degradation. Biochemistry 34, 8115-8122
14. Goldman, E.R., Dall'Acqua, W., Braden, B.C., and Mariuzza, R.A. (1997) Analysis of binding interactions in an idiotope-anti-idiotope protein-protein complex by double mutant cycles. Biochemistry 36, 49-56
15. Serrano, L., Horovitz, A., Avron, B., Bycroft, M., and Fersht, A.R. (1990) Estimating the contribution of engineered surface electrostatic interactions to protein stability by using double-mutant cycles. Biochemistry 29, 9343-9352
16. Green, S.M. and Shortle, D. (1993) Patterns of nonadditivity between pairs of stability mutations in staphylococcal nuclease. Biochemistry 32, 10131-10139
17. Blaber, M., Baase, W.A., Gassner, N., and Matthews, B.W. (1995) Alanine scanning mutagenesis of the alpha-helix 115-123 of phage T4 lysozyme: Effects on structure, stability and the binding of solvent. J. Mol. Biol. 246, 317-330
18. Perry, K.M., Onuffer, J.J., Gittelman, M.S., Barmat, L., and Matthews, C.R. (1989) Long-range electrostatic interactions can influence the folding, stability, and cooperativity of dihydrofolate reductase. Biochemistry 28, 7961-7968
19. Texter, F.L., Spencer, D.B., Rosenstein, R., and Matthews, C.R. (1992) Intramolecular catalysis of a proline isomerization reaction in the folding of dihydrofolate reductase. Biochemistry 31, 5687-5691
20. Dion, A., Linn, C.E., Bradrick, T.D., Georghiou, S., and Howell, E.E. (1993) How do mutations at phenylalanine-153 and isoleucine-155 partially suppress the effects of the aspartate-27→ serine mutation in Escherichia coli dihydrofolate reductase? Biochemistry 32, 3479-3487
21. Iwakura, M. and Tanaka, T. (1992) Dihydrofolate reductase gene as a versatile expression marker. J. Biochem. 111, 31-36
22. Sanger, F., Nicklen, S., and Coulson, A.R. (1977) DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA 74, 5463-5467
23. Singer, S., Ferone, R., Walton, L., and Elwell, L. (1985) Isolation of a dihydrofolate reductase-deficient mutant of Escherichia coli. J. Bacteriol. 164, 470-472
24. Fierke, C.A., Johnson, K.A., and Benkovic, S.J. (1987) Construction and evaluation of the kinetic scheme associated with dihydrofolate reductase from Escherichia coli. Biochemistry 26, 4085-4092
25. Nakagawa, T. and Oyanagi, Y. (1980) Program system SALS for nonlinear least-squares fitting in experimental sciences in Recent Developments in Statistical Inference and Data Analysis (Matsushita, K., ed.) pp. 221-225, North Holland Publishing Company, Amsterdam
26. Pace, C.N. (1985) Determination and analysis of urea and guanidine hydrochloride denaturation curves in Methods in Enzymology (Hirs, C.H.W. and Timasheff, S.N., eds.) Vol. 131, pp. 267-280, Academic Press, New York
27. Williams, J.W., Morrison, J.F., and Duggleby, R.G. (1979) Methotrexate, a high-affinity pseudosubstrate of dihydrofolate reductase. Biochemistry 18, 2567-2573
28. Penner, M.H. and Frieden, C. (1985) Substrate-induced hysteresis in the activity of Escherichia coli dihydrofolate reductase. J. Biol. Chem. 260, 5366-5369
29. Stone, S.R. and Morrison, J.F. (1982) Kinetic mechanism of the reaction catalyzed by dihydrofolate reductase from Escherichia coli. Biochemistry 21, 3757-3765
30. Kuwajima, K., Garvey, E.P., Finn, B.E., Matthews, C.R., and Sugai, S. (1991) Transient intermediates in the folding of dihydrofolate reductase as detected by far-ultraviolet circular dichroism spectroscopy. Biochemistry 30, 7693-7703
31. Touchette, N.A., Perry, K.M., and Matthews, C.R. (1986) Folding of dihydrofolate reductase from Escherichia coli. Biochemistry 25, 5445-5452
32. Perry, K.M., Onuffer, J.J., Touchette, N.A., Herndon, C.S., Gittelman, M.S., Matthews, C.R., Chen, J.T., Mayer, R.J., Taira, K., Benkovic, S.J., Howell, E.E., and Kraut, J. (1987) Effect for single amino acid replacements on the folding and stability of dihydrofolate reductase from Escherichia coli. Biochemistry 26, 2674-2682
33. Garvey, E.P. and Matthews, C.R. (1989) Effects of multiple replacements at a single position on the folding and stability of dihydrofolate reductase from Escherichia coli. Biochemistry 28, 2083-2093
34. Jennings, P.A., Finn, B.E., Jones, B.E., and Matthews, C.R. (1993) A reexamination of the folding mechanism of dihydrofolate reductase from Escherichia coli: Verification and refinement of a four-channel model. Biochemistry 32, 3783-3789
35. Iwakura, M., Jones, B.E., Falzone, C.J., and Matthews, C.R. (1993) Collapse of parallel folding channels in dihydrofolate reductase from Escherichia coli by site-directed mutagenesis. Biochemistry 32, 13566-13574
36. David, C.L., Howell, E.E., Farnum, M.F., Villafranca, J.E., Oatley, S.J., and Kraut, J. (1992) Structure and function of alternative proton-relay mutants of dihydrofolate reductase. Biochemistry 31, 9813-9822
37. Chen, J.-T., Taira, K., Tu, C.-P.D., and Benkovic, S.J. (1987) Probing the functional role of phenylalanine-31 of Escherichia coli dihydrofolate reductase by site-directed mutagenesis. Biochemistry 26, 4093-4100
38. Howell, E.E., Warren, M.S., Booth, C.L., Villafranca, J.E., and Kraut, J. (1987) Construction of an altered proton donation mechanism in Escherichia coli dihydrofolate reductase. Biochemistry 26, 8591-8598
39. Warren, M.S., Brown, K.A., Farnum, M.F., Howell, E.E., and Kraut, J. (1991) Investigation of the functional role of tryptophan-22 in Escherichia coli dihydrofolate reductase by site-directed mutagenesis. Biochemistry 30, 11092-11103
40. Wilkinson, A.J., Fersht, A.R., Blow, D.M., and Winter, G. (1983) Site-directed mutagenesis as a probe of enzyme structure and catalysis: tyrosyl-tRNA synthetase cysteine-35 to glycine-35 mutation. Biochemistry 22, 3581-3586
41. Wells, J.A. (1990) Additivity of mutational effects in proteins. Biochemistry 29, 8509-8517
42. Nozaki, Y. and Tanford, C. (1971) The solubility of amino acids and two glycine peptides in aqueous ethanol and dioxane solutions. J. Biol. Chem. 246, 2211-2217
43. Zamyatnin, A.A. (1984) Amino acid, peptide, and protein volume in solution. Annu. Rev. Biophys. Bioeng. 13, 145-165
44. Miller, S., Janin, J., Lesk, A.M., and Chothia, C. (1987) Interior and surface of monomeric proteins. J. Mol. Biol. 196, 641-656