Structure and dynamics in solution of the complex of Lactobacillus casei dihydrofolate reductase with the new lipophilic antifolate drug trimetrexate

Protein Science

Volumn 8, Issue 3, 1999, Pages 467-481

  Polshakov, Vladimir I ^a,b   Birdsall, Berry ^a   Frenkiel, Thomas A ^a   Gargaro, Angelo R ^a   Feeney, James ^a  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^b Center for Drug Chemistry   (Russian Federation)

Author keywords

15N relaxation; Dihydrofolate reductase; Dynamics; NMR; Protein ligand interactions; Ring flipping; Structure determination; Trimetrexate

Indexed keywords

DIHYDROFOLATE REDUCTASE; FOLIC ACID ANTAGONIST; TRIMETREXATE;

ANTINEOPLASTIC ACTIVITY; ARTICLE; COMPLEX FORMATION; DRUG EFFECT; ENZYME STRUCTURE; LACTOBACILLUS CASEI; LIGAND BINDING; LIPOPHILICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN PROTEIN INTERACTION; PROTON NUCLEAR MAGNETIC RESONANCE; STRUCTURE ANALYSIS;

BACTERIA (MICROORGANISMS); LACTOBACILLUS CASEI;

EID: 0033019040     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1110/ps.8.3.467     Document Type: Article

References (70)

1. Andrews J, Clore GM, Davies RW, Gronenborn AM, Gronenborn B, Kalderon D, Papadopoulos PC, Schafer S, Sims PFG, Stancombe R. 1985. Nucleotide sequence of the dihydrofolate reductase gene of methotrexate-resistant Lactobacillus casei. Gene 35:217-222.
2. 1H NMR study of the role of the glutamate moiety in the binding of methotrexate to dihydrofolate reductase. Brit J Pharmacol 81:309-315.
3. Baccanari DP, Kuyper LF. 1993. Basis of selectivity of antibacterial diaminopyrimidines. J Chemother 5:393-399.
4. Bertino JR, Sawicki WL, Moroson BA, Cashmore AR, Elslager EF. 1979. 24-Diamino-5-methyl-6-[3,4,5]-trimethoxyanilino-methyl]quinazoline trimetrexate a potent non-classical folate antagonist inhibitor: I. Effect of dihydrofolate reductase and growth of rodent tumours in vitro and in vivo. Biochemical Pharmacol 28:1983-1987.
5. 15N NMR studies of protonation and hydrogen-bonding in the binding of trimethoprim to dihydrofolate reductase. Eur Biophys J 11:211-218.
6. Birdsall B, Andrews J, Ostler G, Tendler SJB, Feeney J, Roberts GCK, Davies RW, Cheung HTA. 1989b. NMR studies of the differences in the conformations and dynamics of ligand complexes formed with mutant dihydrofolate reductases. Biochemistry 28:1353-1362.
7. Birdsall B, Burgen ASV, Hyde EI, Roberts GCK, Feeney J. 1981. Negative cooperativity between folinic acid and coenzyme in their binding to L. casei dihydrofolate reductase. Biochemistry 20:186-7195.
8. Birdsall B, Burgen ASV, Roberts GCK. 1980. Binding of coenzyme analogues to L. casei dihydrofolate reductase: Binary and ternary complexes. Biochemistry 19:3723-3731.
9. Birdsall B, Cassarotto MG, Cheung HTA, Basran J, Roberts GCK, Feeney J. 1997. The influence of aspartate 26 on the tautomeric forms of folate bound to Lactobacillus casei dihydrofolate reductase. FEBS Lett 402:157-161.
10. 1H study of the interactions and conformations of rationally designed brodimoprim analogues in complexes with Lactobacillus casei dihydrofolate reductase. J Med Chem 23:1672-1676.
11. Birdsall B, Feeney J, Tendler SJB, Hammond SJ, Roberts GCK. 1989a. Dihydrofolate reductase: Multiple conformations and alternative modes of substrate binding. Biochemistry 28:2297-2305.
12. Birdsall B, Gronenborn AM, Hyde EI, Clore GM, Roberts GCK, Feeney J, Burgen ASV. 1982. Hydrogen-1, carbon-13 and phosphorus-31 nuclear magnetic resonance studies of the dihydrofolate reductase-nicotinamide adenine dinucleotide phosphate-folate complex: Characterization of three coexisting conformational states. Biochemistry 21:5831-5838.
13. Birdsall B, Tendler SJB, Arnold JRP, Feeney J, Griffin RJ, Carr MD, Thomas JA, Roberts GCK, Stevens MFG. 1990. NMR studies of multiple conformations in complexes of L. casei dihydrofolate reductase with analogues of pyrimethamine. Biochemistry 29:9660-9667.
14. Blakley RL. 1985. Dihydrofolate reductase in folates and pterins, Vol 1, Chapter 5. In: Blakley RL, Benkovic SJ, eds. New York, NY: J. Wiley. pp 191-253.
15. Bolin JT, Filman DJ, Matthews DA, Hamlin RC, Kraut J. 1982. Crystal structures of E. coli and L. casei dihydrofolate reductase refined to 1.7 Å resolution: I. General features and binding of methotrexate. J Biol Chem 257:13650-13662.
16. Brünger AT. 1992. X-PLOR 3.1: A system for X-ray crystallography and NMR. New Haven, CT: Yale University Press.
17. Carr MD, Birdsall B, Frenkiel TA, Bauer CJ, Jimenez-Barbero J, Polshakov VI, McCormick JE, Feeney J, Roberts GCK. 1991. Dihydrofolate reductase: Sequential resonance assignments using 2D and 3D NMR and secondary structure determination in solution. Biochemistry 30:6330-6341.
18. 13C NMR determination of the tautomeric and ionization states of folate in its complexes with Lactobacillus casei dihydrofolate reductase. Biochemistry 32:6846-6854.
19. 1H NMR spectroscopy. Biochemistry 29:7387-7401.
20. 19F-NMR studies of 3′,5′-difluoromethotrexate binding to Lactobacillus casei dihydrofolate reductase. Molecular motion and coenzyme-induced conformational changes. Biochem J 217:659-666.
21. Clore GM, Szabo A, Bax A, Kay LE, Driscoll PC, Gronenborn AM. 1990b. Deviations from the simple two-parameter model-free approach to the interpretation of nitrogen-15 nuclear magnetic relaxation in proteins. J Am Chem Soc 112:4989-4991.
22. Cocco L, Roth B, Temple C, Montgomery JA, London RE, Blakley RL. 1981. Protonated state of methotrexate trimethoprim and pyrimethamine bound to dihydrofolate reductase. Arch Biochem Biophys 226:567-577.
23. Dann JG, Ostler G, Bjur RA, King RW, Scudder P, Turner PC, Roberts GCK, Burgen ASV, Harding NGL. 1976. Large scale purification and characterization of dihydrofolate reductase from a methotrexate-resistant strain of Lactobacillus casei. Biochem J 157: 559-571.
24. Elslager EF, Johnson JL, Werbel LM. 1983. Folate antagonists. 20. Synthesis and anti-tumor and anti-malarial properties of trimetrexate and related 6-[(phenylamino)methyl]-2,4-quinazolinediamines. J Med Chem 26:1753-1760.
25. Epstein DM, Benkovic SJ, Wright PE. 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.
26. 13C resonance assignments secondary structure and the conformation of substrate in the binary folate complex of Escherichia coli dihydrofolate reductase. J Biomol NMR 4:349-366.
27. 15N NMR relaxation. Biochemistry 33:5984-6003.
28. Feeney J. 1986. NMR studies of drug receptor complexes: Antifolate drugs binding to dihydrofolate reductase. NATO Advanced Study Inst Ser C 164:347-366.
29. Feeney J. 1990. NMR studies of interactions of ligands with dihydrofolate reductase. Biochem Pharm 40:141-152.
30. Feeney J. 1996. NMR studies of ligand binding to dihydrofolate reductase and their application in drug design. In: Craik D. ed. NMR in drug design. Boca Raton, New York, London, Tokyo: CRC Press.
31. Feeney J, Birdsall B. 1993. NMR studies of protein-ligand interactions. In: Roberts GCK, ed. NMR of biological macromolecules: A practical approach. Oxford, New York, Tokyo: Oxford University Press.
32. Freisheim JH, Matthews DA. 1984. In: Sirotnak FM, Burchill JJ, Ensminger WD, Montgomery JA, eds. Folate antagonists as therapeutic agents, Vol 1. New York: Academic Press Inc. pp 69-131.
33. Gangjee A, Elzain E, Kothare M, Vasudevan A. 1996. Classical and nonclassical antifolates as a potential antitumor antipneumocystis and antitoxoplasma agents. Current Pharmaceutical Design 2:263-280.
34. Gangjee A, Zaveri N, Kothare M, Queener SF. 1995. Nonclassical 2,4-diamino-6-aminomethyl-5,6,7,8-tetrahydroquinazoline antifolates: Syntheses and biological activities. J Med Chem 38:3660-3668.
35. Gargaro AR, Frenkiel TA, Nieto PM, Birdsall B, Polshakov VI, Morgan WD, Feeney J. 1996. NMR detection of arginine-ligand interactions in complexes of Lactobacillus casei dihydrofolate reductase. Euro J Biochem 238:435-439.
36. Gargaro AR, Soteriou A, Frenkiel TA, Bauer CJ, Birdsall B, Polshakov VI, Barsukov IL, Roberts GCK, Feeney J. 1998. The solution structure of the complex of Lactobacillus casei dihydrofolate reductase with methotrexate. J Mol Biol 277:119-134.
37. 31P solid-state NMR measurements used to detect interactions between NADPH and water and to determine the ionization state of NADPH in a protein-ligand complex subjected to low-level hydration. Euro J Biochem 235:262-266.
38. Gronenborn A, Birdsall B, Hyde EI, Roberts GCK, Feeney J, Burgen ASV. 1981. Direct observation by NMR of two coexisting conformations of an enzyme-ligand complex in solution. Nature 290:273-274.
39. 1H resonance assignments and coenzyme-induced conformational changes. J Mol Biol 188:81-97.
40. Hempel A, Camerman N. 1988. Trimetrexate: Molecular structures and conformational similarities in two crystal forms. Cancer Biochem Biophys 10:25-30.
41. Jackson RC, Fry DW, Boritzki TJ, Besserer JA, Leopold WR, Sloan BJ, Elslager EF. 1984. Biochemical pharmacology of the lipophilic antifolate trimetrexate. Advances in Enzyme Regulation 22:187-206.
42. Johnson JM, Meiering EM, Wright JE, Pardo J, Rosowsky A, Wagner G. 1997. NMR solution structure of the anti tumor compound PT523 and NADPH in the ternary complex with human dihydrofolate reductase. Biochemistry 36:4399-4411.
43. 2 values in proteins: Pulse sequences for the removal of such effects. J Magn Reson 97:359-375.
44. 15N inverse detected heteronuclear NMR spectroscopy: Application to staphylococcal nuclease. Biochemistry 28:8972-8979.
45. Laskowski RA, MacArthur MW, Moss DS, Thornton JM. 1993. PROCHECK: A program to check the stereochemical quality of protein structures. J Appl Cryst 26:283-291.
46. Laskowski RA, Rullmann JAC, MacArthur MW, Kaptein R, Thornton JM. 1996. AQUA and PROCHECK-NMR: Programs for checking the quality of protein structures solved by NMR. J Biomol NMR 8:477-486.
47. Lin JT, Bertino JR. 1987. Trimetrexate - A 2nd generation folate antagonist in clinical-trial. J Clin Oncol 5:2032-2040.
48. Lin JT, Bertino JR. 1991. Update on trimetrexate a folate antagonist with antineoplastic and antiprotozal properties. Cancer Invest 9:159-172.
49. Lipari G, Szabo A. 1982. Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules: 1. Theory and range of validity. J Am Chem Soc 104:4546-4559.
50. 15N NMR via proton detected multiquantum coherences: Studies of large peptides. J Am Chem Soc 106:1939-1941.
51. Martorell G, Gradwell MJ, Birdsall B, Bauer CJ, Frenkiel TA, Cheung HTA, Polshakov VI, Kuyper L, Feeney J. 1994. Solution structure of bound trimethoprim in its complex with Lactobacillus casei dihydrofolate reductase. Biochemistry 33:12416-12426.
52. Matthews DA, Bolin JT, Burridge JM, Filman DJ, Volz KW, Kaufman BT, Beddell CR, Champness JN, Stammers DK, Kraut J. 1985a. Refined crystal structures of Escherichia coli and chicken liver dihydrofolate reductase containing hound trimethoprim. J Biol Chem 260:381-391.
53. Matthews DA, Bolin JT, Burridge JM, Filman DJ, Volz KW, Kraut J. 1985b. Dihydrofolate reductase - The stereochemistry of inhibitor selectivity. J Biol Chem 260:392-399.
54. Morgan WD, Birdsall B, Polshakov VI, Sali D, Kompis I, Feeney J. 1995. Solution structure of a brodimoprim analogue in its complex with Lactobacillus casei dihydrofolate reductase. Biochemistry 34:11690-11702.
55. Nicholls A, Sharp KA, Honig B. 1991. Protein folding and association: Insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins Struct Funct Genet 11:281-296.
56. Nieto PM, Birdsall B, Morgan WD, Frenkiel TA, Gargaro AR, Feeney J. 1997. Correlated bond rotations in interactions of arginine residues with ligand carboxylate groups in protein ligand complexes. FEBS Lett 405:16-20.
57. Nilges M. 1995. Calculation of protein structures with ambiguous distance constraints: Automated assignment of ambiguous NOE crosspeaks and disulphide connectivities. J Mol Biol 245:645-660.
58. Nilges M, Gronenborn AM, Brünger AT, Clore GM. 1988. The determination of three-dimensional structures of proteins by simulated annealing with interproton distance restraints - Application to crambin potato carboxypeptidase inhibitor and barley serine proteinase inhibitor-2. Protein Eng 2:27-38.
59. Nilges M, Kuszewski J, Brünger AT. 1991. In: Hoch JC, ed. Computational aspects of the study of biological macromolecules by NMR. New York: Plenum Press.
60. Polshakov VI, Birdsall B, Gradwell MJ, Feeney J. 1995a. The use of PM3 SCF MO quantum mechanical calculations to refine NMR-determined structures of complexes of antifolate drugs with dihydrofolate reductase in solution. J Mol Struct (Theochem) 357:207-216.
61. Polshakov VI, Frenkiel TA, Birdsall B, Soteriou A, Feeney J. 1995b. Determination of stereospecific assignments torsion-angle constraints and rotamer populations in proteins using the program AngleSearch. J Magn Reson Series B 108:31-43.
62. Press WH, Teukolsky SA, Vetterling WT, Flannery BP. 1992. Numerical recipes in FORTRAN. The art of scientific computing, Second ed. Cambridge, UK: Cambridge University Press. pp 409-413; 564-570.
63. Robert F. 1988. Trimetrexate as a single agent in patients with advanced head and neck-cancer. Seminars in Oncol 15:22-26.
64. Roberts GCK. 1983. The interaction of substrates and inhibitors with dihydrofolate reductase. In: Blair JA, ed. Chemistry and biology of pteridines. Berlin: W. de Gruyter. pp 197-214.
65. Roth B, Cheng CC. 1982. Recent progress in the medicinal chemistry of 2,4-diaminopyrimidines. Prog Med Chem 19:1-58.
66. Ryckaert JP, Ciccotti G, Berendsen HJC. 1977. Numerical-integration of cartesian equations of motion of a system with constraints: Molecular dynamics of N-alkanes. J Comput Phys 23:327-341.
67. Sawaya MR, Kraut J. 1997. Loop and subdomain movements in the mechanism of E. coli dihydrofolate reductase: Crystallographic evidence. Biochemistry 36:586-603.
68. Searle MS, Forster MJ, Birdsall B, Roberts GCK, Feeney J, Cheung HTA, Kompis I, Geddes AJ. 1988. Dynamics of trimethoprim bound to dihydrofolate reductase. Proc Nat Acad Sci USA 85:3787-3791.
69. 1H NMR-based assignments for side-chain resonances of Lactobacillus casei dihydrofolate reductase. Evidence for similarities between the solution and crystal structures of the enzyme. J Biomol NMR 3:535-546.
70. 15N chemical shift referencing in biomolecular NMR. J Biomol NMR 6:135-140.