Millisecond dynamics in the allosteric enzyme imidazole glycerol phosphate synthase (IGPS) from Thermotoga maritima

Journal of Biomolecular NMR

Volumn 45, Issue 1-2, 2009, Pages 73-84

  Lipchock, James ^a   Loria, J Patrick ^a  

^a YALE UNIVERSITY   (United States)

Author keywords

Allostery; IGP synthase; Millisecond motions; Protein dynamics

Indexed keywords

BACTERIAL PROTEIN; HETERODIMER; IMIDAZOLE GLYCEROL PHOSPHATE SYNTHASE; PROTEIN HISF; PROTEIN HISH; SYNTHETASE; UNCLASSIFIED DRUG;

ALLOSTERISM; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ANALYSIS; ENZYME BINDING; ENZYME STRUCTURE; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; THERMOTOGA MARITIMA;

ALLOSTERIC REGULATION; AMINOHYDROLASES; CATALYTIC DOMAIN; MODELS, BIOLOGICAL; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN CONFORMATION; THERMOTOGA MARITIMA;

THERMOTOGA MARITIMA;

EID: 69249222534     PISSN: 09252738     EISSN: 15735001     Source Type: Journal    
DOI: 10.1007/s10858-009-9337-8     Document Type: Article

References (43)

1. Amaro RE, Myers RS, Davisson VJ, Luthey-Schulten ZA (2005) Structural elements in IGP synthase exclude water to optimize ammonia transfer. Biophys J 89:475-487
2. Amaro RE, Sethi A, Myers RS, Davisson VJ, Luthey-Schulten ZA (2007) A network of conserved interactions regulates the allosteric signal in a glutamine amidotransferase. Biochemistry 46:2156-2173
3. Beach H, Cole R, Gill M, Loria JP (2005) Conservation of μs-ms enzyme motions in the apo- and substrate-mimicked state. J Am Chem Soc 127:9167-9176
4. Bhattacharya A, Kurochkin AV, Yip GN, Zhang Y, Bertelsen EB, Zuiderweg ER (2009) Allostery in Hsp70 chaperones is transduced by subdomain rotations. J Mol Biol 388:475-490
5. 13C relaxation: Expanding perturbation mapping of the rigidifying core mutation, V54A, in eglin c. Biochemistry 47:4876-4886
6. Bruschweiler S, Schanda P, Kloiber K, Brutscher B, Kontaxis G, Konrat R, Tollinger M (2009) Direct observation of the dynamic process underlying allosteric signal transmission. J Am Chem Soc 131:3063-3068
7. Chaudhuri BN, Lange SC, Myers RS, Chittur SV, Davisson VJ, Smith JL (2001) Crystal structure of imidazole glycerol phosphate synthase: A tunnel through a (beta/alpha)8 barrel joins two active sites. Structure 9:987-997
8. Chittur SV, Chen Y, Davisson VJ (2000) Expression and purification of imidazole glycerol phosphate synthase from Saccharomyces cerevisiae. Protein Expr Purif 18:366-377
9. Chittur SV, Klem TJ, Shafer CM, Davisson VJ (2001) Mechanism for acivicin inactivation of triad glutamine amidotransferases. Biochemistry 40:876-887
10. Delaglio F, Grzesiek S, Vuister G, Zhu G, Pfeifer J, Bax A (1995) NMRPipe: A multidimensional spectral processing system based on UNIX pipes. J Biomol NMR 6:277-293
11. DeLano WL (2005) MacPyMOL: A PyMOL-based molecular graphics application for MacOS X. DeLano Scientific LLC, South San Francisco, CA, USA
12. Douangamath A, Walker M, Beismann-Driemeyer S, Vega-Fernandez MC, Sterner R, Wilmanns M (2002) Structural evidence for ammonia tunneling across the (beta alpha)(8) barrel of the imidazole glycerol phosphate synthase bienzyme complex. Structure 10:185-193
13. Eaton WA, Henry ER, Hofrichter J, Mozzarelli A (1999) Is cooperative oxygen binding by hemoglobin really understood? Nat Struct Biol 6:351-358
14. Grzesiek S, Stahl SJ, Wingfield PT, Bax A (1996) The CD4 determinant for downregulation by HIV-1 Nef directly binds to Nef. Mapping of the Nef binding surface by NMR. Biochemistry 35:10256-10261
15. Kimmel JL, Reinhart GD (2000) Reevaluation of the accepted allosteric mechanism of phosphofructokinase from Bacillus stearothermophilus. Proc Natl Acad Sci U S A 97:3844-3849
16. Klem TJ, Davisson VJ (1993) Imidazole glycerol phosphate synthase - the glutamine amidotransferase in histidine biosynthesis. Biochemistry 32:5177-5186
17. Klem TJ, Chen Y, Davisson VJ (2001) Subunit interactions and glutamine utilization by Escherichia coli imidazole glycerol phosphate synthase. J Bacteriol 183:989-996
18. Kneller DG, Kuntz ID (1993) Ucsf sparky - an Nmr display, annotation and assignment tool. J Cell Biochem 25:4-254
19. Koshland DE, Nemethy G, Filmer D (1966) Comparison of experimental binding data and theoretical models in proteins containing subunits. Biochemistry 5:365-385
20. Krahn JM, Kim JH, Burns MR, Parry RJ, Zalkin H, Smith JL (1997) Coupled formation of an amidotransferase interdomain ammonia channel and a phosphoribosyltransferase active site. Biochemistry 36:11061-11068
21. Kuenzler M, Balmelli T, Egli CM, Paravicini G, Braus GH (1993) Cloning, primary structure, and regulation of the HIS7 gene encoding a bifunctional glutamine amidotransferase: Cyclase from Saccharomyces cerevisiae. J Bacteriol 175:5548-5558
22. Lang D, Thoma R, Henn-Sax M, Sterner R, Wilmanns M (2000) Structural evidence for evolution of the beta/alpha barrel scaffold by gene duplication and fusion. Science 289:1546-1550
23. 13C resonance assignment of imidazole glycerol phosphate (IGP) synthase protein HisF from Thermotoga maritima. Biomol NMR Assign 2:219-221
24. Loria JP, Rance M, Palmer AG (1999a) A relaxation-compensated Carr-Purcell-Meiboom-Gill sequence for characterizing chemical exchange by NMR spectroscopy. J Am Chem Soc 121:2331-2332
25. Loria JP, Rance M, Palmer AG (1999b) A TROSY CPMG sequence for characterizing chemical exchange in large proteins. J Biomol NMR 15:151-155
26. Luz Z, Meiboom S (1963) Nuclear magnetic resonance study of the protolysis of trimethylammonium ion in aqueous solution - order of the reaction with respect to solvent. J Chem Phys 39:366-370
27. Massi F, Wang C, Palmer AG 3rd (2006) Solution NMR and computer simulation studies of active site loop motion in triosephosphate isomerase. Biochemistry 45:10787-10794
28. Massiere F, Badet-Denisot MA (1998) The mechanism of glutamine-dependent amidotransferases. Cell Mol Life Sci 54:205-222
29. Monod J, Wyman J, Changeux J-P (1965) On the nature of allosteric transitions: A plausible model. J Mol Biol 12:88-118
30. Mulder FA, Skrynnikov NR, Hon B, Dahlquist FW, Kay LE (2001) Measurement of slow (micros-ms) time scale dynamics in protein side chains by (15)N relaxation dispersion NMR spectroscopy: Application to Asn and Gln residues in a cavity mutant of T4 lysozyme. J Am Chem Soc 123:967-975
31. Myers RS, Jensen JR, Deras IL, Smith JL, Davisson VJ (2003) Substrate-induced changes in the ammonia channel for imidazole glycerol phosphate synthase. Biochemistry 42:7013-7022
32. Omi R, Mizuguchi H, Goto M, Miyahara I, Hayashi H, Kagamiyama H, Hirotsu K (2002) Structure of imidazole glycerol phosphate synthase from Thermus thermophilus HB8: Open-closed conformational change and ammonia tunneling. J Biochem 132:759-765
33. Pervushin K, Riek R, Wider G, Wuthrich K (1997) Attenuated T2 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
34. Rudolph J, Stubbe J (1995) Investigation of the mechanism of phosphoribosylamine transfer from glutamine phosphoribosylpyrophosphate amidotransferase to glycinamide ribonucleotide synthetase. Biochemistry 34:2241-2250
35. Schachman HK (1988) Can a simple model account for the allosteric transition of aspartate transcarbamoylase? J Biol Chem 263:18583-18586
36. Sinha SC, Chaudhuri BN, Burgner JW, Yakovleva G, Davisson VJ, Smith JL (2004) Crystal structure of imidazole glycerol-phosphate dehydratase: duplication of an unusual fold. J Biol Chem 279:15491-15498
37. Stevens SY, Sanker S, Kent C, Zuiderweg ER (2001) Delineation of the allosteric mechanism of a cytidylyltransferase exhibiting negative cooperativity. Nat Struct Biol 8:947-952
38. Thoden JB, Holden HM, Wesenberg G, Raushel FM, Rayment I (1997) Structure of carbamoyl phosphate synthetase: A journey of 96 A from substrate to product. Biochemistry 36:6305-6316
39. Velyvis A, Yang YR, Schachman HK, Kay LE (2007) A solution NMR study showing that active site ligands and nucleotides directly perturb the allosteric equilibrium in aspartate transcarbamoylase. Proc Natl Acad Sci U S A 104:8815-8820
40. Volkman BF, Lipson D, Wemmer DE, Kern D (2001) Two-state allosteric behavior in a single-domain signaling protein. Science 291:2429-2433
41. Yu EW, Koshland DE Jr (2001) Propagating conformational changes over long (and short) distances in proteins. Proc Natl Acad Sci U S A 98:9517-9520
42. Zalkin H, Smith JL (1998) Enzymes utilizing glutamine as an amide donor. Adv Enzymol Relat Areas Mol Biol 72:87-144
43. Zhu G, Xia Y, Nicholson LK, Sze KH (2000) Protein dynamics measurements by TROSY-based NMR experiments. J Magn Reson 143:423-426