Structural and Kinetic Studies of Induced Fit in Xylulose Kinase from Escherichia coli

Journal of Molecular Biology

Volumn 365, Issue 3, 2007, Pages 783-798

  Di Luccio, Eric ^a   Petschacher, Barbara ^b   Voegtli, Jennifer ^a   Chou, Hui Ting ^a   Stahlberg, Henning ^a   Nidetzky, Bernd ^b   Wilson, David K ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b GRAZ UNIVERSITY OF TECHNOLOGY   (Austria)

Author keywords

ATPase; FGGY kinase; mechanism; X ray structure; xylulokinase

Indexed keywords

ADENOSINE TRIPHOSPHATE; ADENOSINE TRIPHOSPHATE MAGNESIUM; BACTERIAL ENZYME; DNA; PROTEIN KINASE; UNCLASSIFIED DRUG; XYLULOKINASE; XYLULOSE;

ARTICLE; CATALYSIS; CRYOELECTRON MICROSCOPY; CRYSTAL STRUCTURE; DIMERIZATION; ENZYME KINETICS; ENZYME SPECIFICITY; ENZYME STRUCTURE; ENZYME SUBSTRATE; ESCHERICHIA COLI; HYDROLYSIS; IMAGE RECONSTRUCTION; LIGHT SCATTERING; MOLECULAR MODEL; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; SITE DIRECTED MUTAGENESIS; STEADY STATE; STRUCTURE ANALYSIS;

ESCHERICHIA COLI;

EID: 33845799646     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2006.10.068     Document Type: Article

References (55)

1. Hahn-Hägerdal B., Wahlbom C.F., Gardonyi M., van Zyl W.H., Cordero Otero R.R., and Jonsson L.J. Metabolic engineering of Saccharomyces cerevisiae for xylose utilization. Advan. Biochem. Eng. Biotechnol. 73 (2001) 53-84
2. Jeffries T.W., and Jin Y.S. Metabolic engineering for improved fermentation of pentoses by yeasts. Appl. Microbiol. Biotechnol. 63 (2004) 495-509
3. Lawlis V.B., Dennis M.S., Chen E.Y., Smith D.H., and Henner D.J. Cloning and sequencing of the xylose isomerase and xylulose kinase genes of Escherichia coli. Appl. Environ. Microbiol. 47 (1984) 15-21
4. Wungsintaweekul J., Herz S., Hecht S., Eisenreich W., Feicht R., Rohdich F., et al. Phosphorylation of 1-deoxy-d-xylulose by d-xylulokinase of Escherichia coli. Eur. J. Biochem. 268 (2001) 310-316
5. Eisenreich W., Schwarz M., Cartayrade A., Arigoni D., Zenk M.H., and Bacher. A. The deoxyxylulose phosphate pathway of terpenoid biosynthesis in plants and microorganisms. Chem. Biol. 5 (1998) R221-R233
6. David S., Estramareix B., Fischer J.-C., and Therisod M. 1-deoxy-d-threo-2-pentulose: the precursor of the five-carbon chain of the thiazole of thiamine. J. Am. Chem. Soc. 103 (1981) 7341-7342
7. Hill R.E., Sayer B.G., and Spenser J.D. Biosynthesis of vitamin B6: incorporation of d-1-deoxyxylulose. J. Am. Chem. Soc. 111 (1989) 1916-1917
8. Rodriguez-Pena J.M., Cid V.J., Arroyo J., and Nombela C. The YGR194c (XKS1) gene encodes the xylulokinase from the budding yeast Saccharomyces cerevisiae. FEMS Microbiol Letters 162 (1998) 155-160
9. Jin Y.S., Jones S., Shi N.Q., and Jeffries T.W. Molecular cloning of XYL3 (d-xylulokinase) from Pichia stipitis and characterization of its physiological function. Appl. Environ. Microbiol. 68 (2002) 1232-1239
10. Bork P., Sander C., and Valencia A. An ATPase domain common to prokaryotic cell cycle proteins, sugar kinases, actin, and hsp70 heat shock proteins. Proc. Natl Acad. Sci. USA 89 (1992) 7290-7294
11. Bennett Jr. W.S., and Steitz T.A. Glucose-induced conformational change in yeast hexokinase. Proc. Natl Acad. Sci. USA 75 (1978) 4848-4852
12. Flaherty K.M., McKay D.B., Kabsch W., and Holmes K.C. Similarity of the three-dimensional structures of actin and the ATPase fragment of a 70-kDa heat shock cognate protein. Proc. Natl Acad. Sci. USA 88 (1991) 5041-5045
13. Hurley J.H., Faber H.R., Worthylake D., Meadow N.D., Roseman S., Pettigrew D.W., and Remington S.J. Structure of the regulatory complex of Escherichia coli IIIGlc with glycerol kinase. Science 259 (1993) 673-677
14. Yeh J.I., Charrier V., Paulo J., Hou L., Darbon E., Claiborne A., et al. Structures of enterococcal glycerol kinase in the absence and presence of glycerol: correlation of conformation to substrate binding and a mechanism of activation by phosphorylation. Biochemistry 43 (2004) 362-373
15. Ormo M., Bystrom C.E., and Remington S.J. Crystal structure of a complex of Escherichia coli glycerol kinase and an allosteric effector fructose 1,6-bisphosphate. Biochemistry 37 (1998) 16565-16572
16. Flachner B., Varga A., Szabo J., Barna L., Hajdu I., Gyimesi G., et al. Substrate-assisted movement of the catalytic Lys 215 during domain closure: site-directed mutagenesis studies of human 3-phosphoglycerate kinase. Biochemistry 44 (2005) 16853-16865
17. Zecchinon L., Oriol A., Netzel U., Svennberg J., Gerardin-Otthiers N., and Feller G. Stability domains, substrate-induced conformational changes, and hinge-bending motions in a psychrophilic phosphoglycerate kinase. A microcalorimetric study. J. Biol. Chem. 280 (2005) 41307-41314
18. Laskowski R.A., MacArthur M.W., Moss D.S., and Thornton J.M. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallog. 26 (1993) 283-291
19. Panchenko A.R., and Bryant S.H. A comparison of position-specific score matrices based on sequence and structure alignments. Protein Sci. 11 (2002) 361-370
20. Bernstein B.E., Michels P.A., and Hol W.G. Synergistic effects of substrate-induced conformational changes in phosphoglycerate kinase activation. Nature 385 (1997) 275-278
21. Kuser P.R., Krauchenco S., Antunes O.A., and Polikarpov I. The high resolution crystal structure of yeast hexokinase PII with the correct primary sequence provides new insights into its mechanism of action. J. Biol. Chem. 275 (2000) 20814-20821
22. Liu J., Lou Y., Yokota H., Adams P.D., Kim R., and Kim S.H. Crystal structures of an NAD kinase from Archaeoglobus fulgidus in complex with ATP, NAD, or NADP. J. Mol. Biol. 354 (2005) 289-303
23. Feese M.D., Faber H.R., Bystrom C.E., Pettigrew D.W., and Remington S.J. Glycerol kinase from Escherichia coli and an Ala65 → Thr mutant: the crystal structures reveal conformational changes with implications for allosteric regulation. Structure 6 (1998) 1407-1418
24. Zhu X., Zhao X., Burkholder W.F., Gragerov A., Ogata C.M., Gottesman M.E., and Hendrickson W.A. Structural analysis of substrate binding by the molecular chaperone DnaK. Science 272 (1996) 1606-1614
25. Robinson R.C., Turbedsky K., Kaiser D.A., Marchand J.B., Higgs H.N., Choe S., and Pollard T.D. Crystal structure of Arp2/3 complex. Science 294 (2001) 1679-1684
26. Lee L.V., Gerratana B., and Cleland W.W. Substrate specificity and kinetic mechanism of Escherichia coli ribulokinase. Arch. Biochem. Biophys. 396 (2001) 219-224
27. Yang V.W., and Jeffries T.W. Regulation of phosphotransferases in glucose- and xylose-fermenting yeasts. Appl. Biochem. Biotechnol. 63-65 (1997) 97-108
28. Pettigrew D.W., Yu G.J., and Liu Y. Nucleotide regulation of Escherichia coli glycerol kinase: initial-velocity and substrate binding studies. Biochemistry 29 (1990) 8620-8627
29. Neuberger M.S., Hartley B.S., and Walker J.E. Purification and properties of d-ribulokinase and d-xylulokinase from Klebsiella aerogenes. Biochem. J. 193 (1981) 513-524
30. Bennett Jr. W.S., and Steitz T.A. Structure of a complex between yeast hexokinase A and glucose. II. Detailed comparisons of conformation and active site configuration with the native hexokinase B monomer and dimer. J. Mol. Biol. 140 (1980) 211-230
31. Kamata K., Mitsuya M., Nishimura T., Eiki J., and Nagata Y. Structural basis for allosteric regulation of the monomeric allosteric enzyme human glucokinase. Structure 12 (2004) 429-438
32. Pettigrew D.W., Smith G.B., Thomas K.P., and Dodds D.C. Conserved active site aspartates and domain-domain interactions in regulatory properties of the sugar kinase superfamily. Arch. Biochem. Biophys. 349 (1998) 236-245
33. Mayer G., Kulbe K.D., and Nidetzky B. Utilization of xylitol dehydrogenase in a combined microbial/enzymatic process for production of xylitol from d-glucose. Appl. Biochem. Biotechnol. 98-100 (2002) 577-589
34. Hadwiger P., Mayr P., Nidetzky B., Stütz A.E., and Tauss A. Synthesis of 5,6-di-modified open-chain d-fructose derivatives and their properties as substrates of bacterial polyol dehydrogenase. Tetrahedron: Asymmetry 11 (2002) 607-620
35. Wang W., and Malcolm B.A. Two-stage PCR protocol allowing introduction of multiple mutations, deletions and insertions using QuikChange site-directed mutagenesis. Biotechniques 26 (1999) 680-682
36. Otwinowski Z., and Minor W. Processing of X-Ray diffraction data collected in oscillation mode. Methods Enzymol. 276 (1997) 307-326
37. Collaborative Computational Project, Number 4. The CCP4 suite: programs for protein crystallography. Acta Crystallog. sect. D 50 (1994) 760-763
38. Brunger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallog. sect. D 54 (1998) 905-921
39. Emsley P., and Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallog. sect. D 60 (2004) 2126-2132
40. Murshudov G.N., Vagin A.A., and Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallog. sect. D 53 (1997) 240-255
41. Bystrom C.E., Pettigrew D.W., Branchaud B.P., O'Brien P., and Remington S.J. Crystal structures of Escherichia coli glycerol kinase variant S58 → W in complex with nonhydrolyzable ATP analogues reveal a putative active conformation of the enzyme as a result of domain motion. Biochemistry 38 (1999) 3508-3518
42. Krissinel E., and Henrick K. Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallog. sect. D 60 (2004) 2256-2268
43. Mao C., Ozer Z., Zhou M., and Uckun F.M. X-Ray structure of glycerol kinase complexed with an ATP analog implies a novel mechanism for the ATP-dependent glycerol phosphorylation by glycerol kinase. Biochem. Biophys. Res. Commun. 259 (1999) 640-644
44. Guex N., Diemand A., and Peitsch M.C. Protein modelling for all. Trends Biochem. Sci. 24 (1999) 364-367
45. Guex N., and Peitsch M.C. SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18 (1997) 2714-2723
46. Hayward S., and Berendsen H.J. Systematic analysis of domain motions in proteins from conformational change: new results on citrate synthase and T4 lysozyme. Proteins: Struct. Funct. Genet. 30 (1998) 144-154
47. Wriggers W., and Schulten K. Protein domain movements: detection of rigid domains and visualization of hinges in comparisons of atomic coordinates. Proteins: Struct. Funct. Genet. 29 (1997) 1-14
48. Humphrey, W., Dalke, A. & Schulten, K. (1996). VMD: visual molecular dynamics. J. Mol. Graph. 14, 27-8, 33-8.
49. Dubochet J., Adrian M., Chang J.J., Homo J.C., Lepault J., McDowall A.W., and Schultz P. Cryo-electron microscopy of vitrified specimens. Quart. Rev. Biophys. 21 (1988) 129-228
50. Ludtke S.J., Baldwin P.R., and Chiu W. EMAN: semiautomated software for high-resolution single-particle reconstructions. J. Struct. Biol. 128 (1999) 82-97
51. Frank J., Radermacher M., Penczek P., Zhu J., Li Y., Ladjadj M., and Leith A. SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields. J. Struct. Biol. 116 (1996) 190-199
52. Frank J. Multivariate Statistical Analysis and Classification of Images. In Three-dimensional Electron Microscopy of Macromolecular Assemblies. The Enzymes. 2nd edit. (2006), Oxford University Press, New York 145-192 chapt. 4
53. van Heel M. Similarity measures between images. Ultramicroscopy 21 (1987) 95-100
54. Unser M., Trus B.L., and Steven A.C. A new resolution criterion based on spectral signal-to-noise ratios. Ultramicroscopy 23 (1987) 39-52
55. Pettersen E.F., Goddard T.D., Huang C.C., Couch G.S., Greenblatt D.M., Meng E.C., and Ferrin T.E. UCSF Chimera - a visualization system for exploratory research and analysis. J. Comput. Chem. 25 (2004) 1605-1612