Effect of amino acid substitutions at the subunit interface on the stability and aggregation properties of a dimeric protein: Role of Arg 178 and Arg 218 at the dimer interface of thymidylate synthase

Proteins: Structure, Function and Genetics

Volumn 34, Issue 3, 1999, Pages 356-368

  Prasanna, Variath ^a,b   Gopal, B ^a   Murthy, M R N ^a   Santi, Daniel V ^c   Balaram, Padmanabhan ^a,b  

^a INDIAN INSTITUTE OF SCIENCE   (India)

^b JAWAHARLAL NEHRU CENTRE FOR ADVANCED SCIENTIFIC RESEARCH   (India)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Aggregation of multimeric enzymes; Arginine residues in protein protein interactions; Dimeric enzyme stability; Thymidylate synthase

Indexed keywords

AMINO ACID; ARGININE; GUANIDINE; PROTEIN; THYMIDYLATE SYNTHASE; UREA;

AMINO ACID SUBSTITUTION; ARTICLE; CIRCULAR DICHROISM; CRYSTAL STRUCTURE; ENZYME ACTIVITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTEIN QUATERNARY STRUCTURE; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE;

ARGININE; CIRCULAR DICHROISM; DIMERIZATION; ENZYME STABILITY; LACTOBACILLUS CASEI; MUTATION; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; TEMPERATURE; THYMIDYLATE SYNTHASE; X-RAY DIFFRACTION;

LACTOBACILLUS CASEI;

EID: 0033557264     PISSN: 08873585     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-0134(19990215)34:3<356::AID-PROT8>3.0.CO;2-O     Document Type: Article

References (63)

1. Neet KE, Timm DE. Conformational studies of dimeric proteins: Quantitative studies by equilibrium denaturation. Protein Sci 1994;3:2167-2174.
2. Janin J, Miller S, Chothia C. Surface, subunit interfaces and interior of oligomeric proteins. J Mol Biol 1988;204:155-164.
3. Jones S, Thornton JM. Protein-protein interactions: A review of protein dimer structures. Prog Biophys Mol Biol 1995;63:31-65.
4. Clackson T, Wells JA. A hot spot of binding energy in a hormone-receptor interface. Science 1995;267:383-386.
5. Milla ME, Sauer RT. Critical side-chain interactions at a subunit interface in the arc repressor dimer. Biochemistry 1995;34:3344-3351.
6. Murray AJ, Lewis SJ, Barclay AN, Brady RL. One sequence, two folds: A metastable structure of CD2. Proc Natl Acad Sci USA 1995;92:7337-7341.
7. Borchert TV, Abagyan R, Radha Kishen KV, Zeelen JP, Wierenga RK. The crystal structure of an engineered monomeric triosephosphate isomerase, mono TIM: The correct modelling of an eight residue loop. Structure 1993;1:205-213.
8. Horton N, Lewis M. Calculation of free energy of association for protein complexes. Protein Sci 1992;1:169-181.
9. Tsai C-J, Lin SL, Wolfson HJ, Nussinov R. Protein-protein interfaces: Architectures and interactions in protein-protein interfaces and in protein cores. Their similarities and differences. Crit Rev Biochem Mol Biol 1996;31:127-152.
10. Tsai CJ, Nussinov R. Hydrophobic folding units at protein-protein interfaces: Implications to protein folding and to protein-protein association. Protein Sci 1997;6:1426-1437.
11. Chothia C, Janin J. Principles of protein-protein recognition. Nature 1975;256:705-708.
12. Young L, Jernigan RL, Covell DG. A role for surface hydrophobicity in protein-protein recognition. Protein Sci 1994;3:717-729.
13. Bashir A, Perham RN, Scrutton NS, Berry A. Altering kinetic mechanism and enzyme stability by mutagenesis of the dimer interface of glutathione reductase. Biochem J 1995; 312:527-533.
14. Walker JE, Wonacott AJ, Harris JI. Heat stability of a tetrameric enzyme, D-Glyceraldehyde-3-Phosphate dehydrogenase. Eur J Biochem 1980;108:581-586.
15. Bucht G, Haggstrom B, Radic Z, Osterman A, Hjalmarsson K. Residues important for folding and dimerization of recombinant torpedo California acetylcholineesterase. Biochim Biophys Acta 1994;1209:265-273.
16. Fersht AR, Shi J-P, Knill-Jones J et al. Hydrogen bonding and biological specificity analyzed by protein engineering. Nature 1985:314:235-314.
17. Kornblatt JA, Kornblatt MJ, Hoa GH. Second derivative spectroscopy of enolase at high hydrostatic pressure: An approach in the study of macromolecular interactions. Biochemistry 1995;34:1218-1223.
18. Ladbury JE. Just add water! The effect of water on the specificity of protein-ligand binding sites and its potential application to drug design. Chem Biol 1996;3:973-980.
19. 1 crystal form of oxidized uteroglobin at 1.34 Å resolution. J Mol Biol 1987;194:725-739.
20. Davies DR, Cohen GH. Interactions of protein antigens with antibody. Proc Natl Acad Sci USA 1996;93:7-12.
21. Jones S, Thornton JM. Principles of protein-protein interactions. Proc Natl Acad Sci USA 1996:93:13-20.
22. Marshall GR. Three-dimensional structure of peptide-protein complexes: Implications for recognition. Curr Opin Struct Biol 1992;2:904-919.
23. Borders CL, Jr, Broadwater JA, Bekeny PA et al. A structural role for arginine in proteins: Multiple hydrogen bonds to backbone carbonyl oxygens. Protein Sci 1994:3:541-548.
24. Mrabet NT, Broeck AVD, Brande IVD et al. Arginine residues as stabilizing elements in proteins. Biochemistry 1992;31:2239-2253.
25. Hardy LW, Finer-Moore JS, Montfort WR, Jones MO, Santi DV, Stroud RM. Atomic structure of thymidylate synthase: Target for rational drug design. Science 1987;235:448-455.
26. Perry KM, Fauman EB, Finer-Moore JS et al. Plastic adaptation toward mutations in proteins: Structural comparison of thymidylate synthases. Proteins 1990;8:315-333.
27. Schiffer CA, Clifton IJ, Davisson VJ, Santi DV, Stroud RM. Crystal structure of human thymidylate synthase: A structural mechanism for guiding substrates into the active site. Biochemistry 1995;34:16279-16287.
28. Finer-Moore J, Maley GF, Maley F, Montfort WR, Stroud RM. Crystal structure of thymidylate synthase from T4 phage: Component of a deoxyribonucleoside triphosphate - synthesizing complex. Biochemistry 1994.33:15459-15468.
29. Carreras CW, Santi DV. The catalytic mechanism and the structure of thymidylate synthase. Ann Rev Biochem 1995;64:722-762.
30. Perry KM, Pookanjanatavip M, Zhao J, Santi DV, Stroud RA. Reversible dissociation and unfolding of the dimeric protein of thymidylate synthase. Protein Sci 1992;1:796-800.
31. Gokhale RS, Agarwalla S, Santi DV, Balaram P. Covalent reinforcement of a fragile region in the dimeric thymidylate synthase stabilizes the protein against chaotrope-induced unfolding. Biochemistry 1996;35:7150-7158.
32. Agarwalla S, Gokhale RS, Santi DV, Balaram P. Covalent tethering of the dimer interface annuls aggregation in thymidylate synthase. Protein Sci 1996;5:270-277.
33. Gokhale RS, Agarwalla S, Francis VS, Santi DV, Balaram P. Thermal stabilization of thymidylate synthase by engineering two disulfide bridges across the dimer interface. J Mol Biol 1994;235: 89-93.
34. Pogolotti Jr AL, Danenberg PV, Santi DV. Kinetics and mechanism of interaction of 10-Propargy-5,8-dideazafolate with thymidylate synthase. J Med Chem 1986;29:478-482.
35. Carreras CW, Climie SC, Santi DV. Thymidylate synthase with a C-terminal deletion catalyzes partial reactions but is unable to catalyze thymidylate formation. Biochemistry 1992,31:6038-6044.
36. Brunger AT. X-Plor, Version 3.1 A system for X-ray crystallography and NMR. New Haven, CT: Yale University Press; 1992.
37. Jones TA, Zou JY, Cowman SW. Improved methods for model building protein models in electron density maps and the location of errors in these models. Acta Crystallogr 1991; A47:110-119.
38. Lim WA, Farruggio DC, Sauer RT. Structural and energetic consequences of disruptive mutations in a protein core. Biochemistry 1992;31:4321-4333.
39. Monera OD, Kay CM, Hodges RS. Protein denaturation with guanidine hydrochloride or urea provides a different estimate of stability depending on the contributions of electrostatic interactions. Protein Sci 1994;3:1984-1991.
40. Morjana NA, McKeone BJ, Gilbert HF. Guanidine hydrochloride stabilization of a partially unfolded intermediate during the reversible denaturation of protein disulfide isomerase. Proc Natl Acad Sci USA 1993;90:2107-2111.
41. Finer-Moore J, Fauman EB, Foster PG, Perry KM, Santi DV, Stroud RM. Refined structures of substrate bound and phosphate bound thymidylate synthase from Lactobacillus casei. J Mol Biol 1993;232:1101-1116.
42. Green SM, Meeker AK, Shortle D. Contributions of the polar, uncharged amino acids to the stability of staphylococcal nuclease: Evidence for mutational effects on the free energy of denatured state. Biochemistry 1992;31:5717-5728.
43. LaPat-Polasko L, Maley G, Maley F. Properties of bacteriphage T4 thymidylate synthase following mutagenic changes in the active site and folate binding region. Biochemistry 1990; 29:9561-9572.
44. Brems DN, Plaisted SM, Kauffman EW, Havel HA. Characterization of an associated equilibrium folding intermediate of bovine growth hormone. Biochemistry 1986;25:6539-6543.
45. Dabrowski MJ, Bietze EC, Atkins WM. Engineering the aggregation properties of dodecameric glutamine synthetase: A single amino acid substitution controls 'salting out' Protein Eng 1996;9: 291-298.
46. Tevelev A, Byeon IJ, Selby T et al. Tumor supressor p16INK4A: Structural characterization of wild type and mutant proteins by NMR and circular dichroism. Biochemistry 1996;35:9475-9487.
47. Kim D, Yu MH. Folding pathway of human alpha 1-antitrypsin: Characterization of an intermediate that is active but prone to aggregation. Biochem Biophys Res Commun 1996; 226:378-384.
48. 1-antitrypsin suppress the folding defect of the Z-type variant. J Biol Chem 1995; 270:8597-8601.
49. Harrison PM, Bamborough P, Dagget B, Prusiner SB, Cohen FE. The prion folding problem. Curr Opin Struct Biol 1997;7:53-59.
50. Bychkova VE, Ptitsyn OB. Folding intermediates are involved in genetic diseases? FEBS Lett 1995;359:6-8.
51. Pace CN, Marshall HF. A comparison of the effectiveness of protein denaturants for β-lactoglobulin and ribonuclease. Arch Biochem Biophys 1980;199:270-276.
52. Havel HA, Kauffman EW, Plaisted SM, Brems DN. Reversible self-association of bovine growth hormone during equilibrium unfolding. Biochemistry 1986;25:6533-6538.
53. Horowitz PM, Criscimagna NL. Low concentrations of guanidinium chloride expose apolar surfaces and cause differential perturbation in catalytic intermediates of rhodanese. J Biol Chem 1986;261:15652-15658.
54. Jaenicke R. Protein Folding: Local structures, domains, subunits and assemblies. Biochemistry 1991;30:3147-3161.
55. Jones DH, McMillan AJ, Fersht AR, Winter G. Reversible dissociation of dimeric Tyrosyl-tRNA synthetase by mutagenesis at the subunit interface. Biochemistry 1985;24: 5852-5857.
56. Kotik M, Zuber H. Mutations that significantly change the stability, flexibility and quarternary structure of the L-lactate dehydrogenase from bacillus megaterium. Eur J Biochem 1993;211: 267-280.
57. Maley F, Pedersen-Lane J, Changchien L. Complete restoration of activity to inactive mutants of E.coli thymidylate synthase: Evidence that E.coli thymidylate synthase is a half the sites activity enzyme. Biochemistry 1995;34:1469-1474.
58. Prasanna V, Battacharjya S, Balaram P. Synthetic interface peptides as inactivators of multimeric enzymes: Inhibitory and conformational properties of three fragments from Lactobaccilus casei thymidylate synthase. Biochemistry 1997;37:6883-6893.
59. 1-antitrypsin accumulation in the liver. Nature 1992;357:605-607.
60. Mitraki A, Fane B, Haase-Pettingell C, Sturtevant J, King J. Global supression of protein folding defects and inclusion body formation. Science 1991;253:54-58.
61. Folcarelli S, Battistoni A, Carri MT et al. Effect of LysArg mutation in the thermal stability of Cu, Zn Superoxide dismutase: Influence on the monomer-dimer equilibrium. Protein Eng 1996;9: 323-325.
62. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970;277:680-685.
63. Kraulis PJ. MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J Appl Cryst 1991;24:946-950.