Structural studies of the Nudix hydrolase DR1025 from Deinococcus radiodurans and its ligand complexes

Journal of Molecular Biology

Volumn 339, Issue 1, 2004, Pages 103-116

  Ranatunga, Wasantha ^a   Hill, Emma E ^b   Mooster, Jana L ^a   Holbrook, Elizabeth L ^a,c   Schulze Gahmen, Ursula ^a   Xu, WenLian ^d   Bessman, Maurice J ^d   Brenner, Steven E ^a,b   Holbrook, Stephen R ^a  

^a LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Ap4A, P1,P4 di(adenosine 5 ) tetraphosphate; Deinococcus radiodurans; GMPPNP, GNP guanosine 5 , imido triphosphate; HMM, hidden Markov model; MutT like; Nudix hydrolase; X ray crystallography

Indexed keywords

ADENOSINE DERIVATIVE; ADENOSINE TRIPHOSPHATE; BACTERIAL PROTEIN; GUANOSINE TRIPHOSPHATE; HYDROLASE; LIGAND; MAGNESIUM; NUCLEOSIDE TRIPHOSPHATE; PROLINE; PROTEIN NUDIX; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CHEMICAL STRUCTURE; CRYSTAL STRUCTURE; CRYSTALLIZATION; DEINOCOCCUS RADIODURANS; ENZYME SUBSTRATE COMPLEX; HYDROLYSIS; METAL BINDING; MOLECULAR DYNAMICS; PRIORITY JOURNAL;

BACTERIA (MICROORGANISMS); DEINOCOCCUS; DEINOCOCCUS RADIODURANS;

EID: 2342644032     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2004.01.065     Document Type: Article

References (57)

1. Bessman M.J., Frick N., O'Handley S.F. The MutT proteins or "Nudix" hydrolases, a family of versatile, widely distributed, "Housecleaning" enzymes. J. Biol. Chem. 271:1996;25059-25062
2. Treffers H.P., Spinelli V., Belser N.O. A factor (or mutator gene) influencing mutation rates in Escherichia coli. Proc. Natl Acad. Sci. USA. 40:1954;1064-1071
3. Bhatnagar S.K., Bullions L.C., Bessman M.J. Characterization of the mutT nucleoside triphosphatase of Escherichia coli. J. Biol. Chem. 266:1991;9050-9054
4. Wang Z., Jiao X., Carr-Schmid A., Kiledjian M. The hDcp2 protein is a mammalian mRNA decapping enzyme. Proc. Natl Acad. Sci. USA. 99:2002;12663-12668
5. Perraud A.L., Fleig A., Dunn C.A., Bagley L.A., Launay P., Schmitz C., et al. ADP-ribose gating of the calcium-permeable LTRPC2 channel revealed by Nudix motif homology. Nature. 411:2001;595-599
6. Bessman M.J., Walsh J.D., Dunn C.A., Swaminathan J., Weldon J.E., Shen J. The gene ygdP, associated with the invasiveness of Escherichia coli K1, designates a Nudix hydrolase, Orf176, active on adenosine (5′)- pentaphospho-(5′)-adenosine (Ap5A). J. Biol. Chem. 276:2001;37834-37838
7. Conyers G.B., Bessman M.J. The gene, ialA, associated with the invasion of human erythrocytes by Bartonella bacilliformis, designates a nudix hydrolase active on dinucleoside 5′-polyphosphates. J. Biol. Chem. 274:1999;1203-1206
8. Gaywee J., Xu W., Radulovic S., Bessman M.J., Azad A.F. The Rickettsia prowazekii invasion gene homolog (invA) encodes a Nudix hydrolase active on adenosine (5′)-pentaphospho-(5′)-adenosine. Mol. Cell. Proteomics. 1:2002;179-185
9. Ismail T.M., Hart C.A., McLenna A.G. Regulation of dinucleoside polyphosphate pools by the YgdP and ApaH hydrolases is essential for the ability of Salmonella enterica serovar Typhimurium to invade cultured mammalian cells. J. Biol. Chem. 278:2003;32602-32607
10. Bateman A., Birney E., Cerruti L., Durbin R., Etwiller L., Eddy S.R., et al. The Pfam protein families database. Nucl. Acids Res. 30:2002;276-280
11. Safrany S.T., Caffrey J.J., Yang X., Bembenek M.E., Moyer M.B., Burkhart W.A., Shears S.B. A novel context for the "MutT" module, a guardian of cell integrity, in a diphosphoinositol polyphosphate phosphohydrolase. EMBO J. 17:1998;6599-6607
12. Fisher D.I., Safrany S.T., Strike P., McLennan A.G., Cartwright J.L. Nudix hydrolases that degrade dinucleoside and diphosphoinositol polyphosphates also have 5-phosphoribosyl 1-pyrophosphate (PRPP) pyrophosphatase activity that generates the glycolytic activator ribose 1, 5-bisphosphate. J. Biol. Chem. 277:2002;47313-47317
13. Murzin A.G., Brenner S.E., Hubbard T., Chothia C. SCOP: a structural classification of proteins database for the investigation of sequences and structures. J. Mol. Biol. 247:1995;536-540
14. Fletcher J.I., Swarbrick J.D., Maksel D., Gayler K.R., Gooley P.R. The structure of Ap(4)A hydrolase complexed with ATP-MgF(x) reveals the basis of substrate binding. Structure. 10:2002;205-213
15. Gabelli S.B., Bianchet M.A., Bessman M.J., Amzel L.M. The structure of ADP-ribose pyrophosphatase reveals the structural basis for the versatility of the Nudix family. Nature Struct. Biol. 8:2001;467-472
16. Kang L.W., Gabelli S.B., Cunningham J.E., O'Handley S.F., Amzel L.M. Structure and mechanism of MT-ADPRase, a nudix hydrolase from Mycobacterium tuberculosis. Structure (Camb). 11:2003;1015-1023
17. Shen B.W., Perraud A.L., Scharenberg A., Stoddard B.L. The crystal structure and mutational analysis of human NUDT9. J. Mol. Biol. 332:2003;385-398
18. Wang S., Mura C., Sawaya M.R., Cascio D., Eisenberg D. Structure of a Nudix protein from Pyrobaculum aerophilum reveals a dimer with two intersubunit beta-sheets. Acta Crystallog. sect. D. 58:2002;571-578
19. Mattimore V., Battista J.R. Radioresistance of Deinococcus radiodurans: functions necessary to survive ionizing radiation are also necessary to survive prolonged desiccation. J. Bacteriol. 178:1996;633-637
20. Makarova K.S., Aravind L., Daly M.J., Koonin E.V. Specific expansion of protein families in the radioresistant bacterium Deinococcus radiodurans. Genetica. 108:2000;25-34
21. White O., Eisen J.A., Heidelberg J.F., Hickey E.K., Peterson J.D., Dodson R.J., et al. Genome sequence of the radioresistant bacterium Deinococcus radiodurans R1. Science. 286:1999;1571-1577
22. Ivanova N., Sorokin A., Anderson I., Galleron N., Candelon B., Kapatral V., et al. Genome sequence of Bacillus cereus and comparative analysis with Bacillus anthracis. Nature. 423:2003;87-91
23. Read T.D., Peterson S.N., Tourasse N., Baillie L.W., Paulsen I.T., Nelson K.E., et al. The genome sequence of Bacillus anthracis Ames and comparison to closely related bacteria. Nature. 423:2003;81-86
24. Blattner F.R., Plunkett G. III, Bloch C.A., Perna N.T., Burland V., Riley M., et al. The complete genome sequence of Escherichia coli K-12. Science. 277:1997;1453-1474
25. Xu W., Shen J., Dunn C.A., Desai S., Bessman M.J. The Nudix hydrolases of Deinococcus radiodurans. Mol. Microbiol. 2001:2001;286-290
26. Xu W., Shen J., Dunn C.A., Bessman M.J. Substrate switching of the Nudix hydrolases of Deinococcus radiodurans. FASEB J. (Part 1 suppl.). 17:2003;A574
27. O'Handley S.F., Frick D.N., Bullions L.C., Mildvan A.S., Bessman M.J. Escherichia coli orf17 codes for a nucleoside triphosphate pyrophosphohydrolase member of the MutT family of proteins. Cloning, purification, and characterization of the enzyme. J. Biol. Chem. 271:1996;24649-24654
28. O'Handley S.F., Dunn C.A., Bessman M.J. Orf135 from Escherichia coli is a Nudix hydrolase specific for CTP, dCTP, and 5-methyl-dCTP. J. Biol. Chem. 276:2001;5421-5426
29. Xu W., Shen J., Dunn C.A., Bessman M.J. A new subfamily of the Nudix hydrolase superfamily active on 5-methyl-UTP (ribo-TTP) and UTP. J. Biol. Chem. 278:2003;37492-37496
30. Kang L.W., Gabelli S.B., Bianchet M.A., Xu W.L., Bessman M.J., Amzel L.M. Structure of a coenzyme A pyrophosphatase from Deinococcus radiodurans: a member of the Nudix family. J. Bacteriol. 185:2003;4110-4118
31. Holbrook E.L., Schulze-Gahmen U., Buchko G.W., Ni S., Kennedy M.A., Holbrook S.R. Crystallization and preliminary X-ray analysis of two nudix hydrolases from Deinococcus radiodurans. Acta Crystallog. sect. D. 59:2003;737-740
32. Nicholls A., Sharp K., Honig B. Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins: Struct. Funct. Genet. 11:1991;281-296
33. Altschul S.F., Madden T.L., Schaffer A.A., Zhang J., Zhang Z., Miller W., Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl. Acids Res, 25:1997;3389-3402
34. Berman H.M., Westbrook J., Feng Z., Gilliland G., Bhat T.N., Weissig H., et al. The Protein Data Bank. Nucl. Acids Res. 28:2000;235-242
35. Liu Y., Zhou J., Omelchenko M.V., Beliaev A.S., Venkateswaran A., Stair J., et al. Transcriptome dynamics of Deinococcus radiodurans recovering from ionizing radiation. Proc. Natl Acad. Sci. USA. 100:2003;4193-4196
36. Hill E.E., Morea V., Chothia C. Sequence conservation in families whose members have little or no sequence similarity: the four-helical cytokines and cytochromes. J. Mol. Biol. 322:2002;205-233
37. Otwinowski Z., Minor W. Processing of X-ray diffraction data collected in oscillation mode. Carter C.W., Sweet R.M. Methods in Enzymology. Methods in Enzymology. vol. 276A:1997;307-326 Academic Press, New York
38. Collaborative Computational Project Number 4. The CCP4 suite: programs for protein crystallography. Acta Crystallog. sect. D. 50:1994;760-763
39. 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
40. Perrakis A., Morris R., Lamzin V.S. Automated protein model building combined with iterative structure refinement. Nature Struct. Biol. 6:1999;458-463
41. Jones T.A., Zou J.Y., Cowan S.W., Kjeldgaard. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallog. sect. A. 47:1991;110-119
42. McDonald I.K., Thornton J.M. Satisfying hydrogen bonding potential in proteins. J. Mol. Biol. 238:1994;777-793
43. Lee B., Richards F.M. The interpretation of protein structures: estimation of static accessibility. J. Mol. Biol. 55:1971;379-400
44. McLachlan A.D. Rapid comparison of protein structures. Acta Crystallog. sect. A. 38:1982;871-873
45. Boeckmann B., Bairoch A., Apweiler R., Blatter M.C., Estreicher A., Gasteiger E., et al. The SWISS-PROT protein knowledgebase and its supplement TrEMBL in 2003. Nucl. Acids Res. 31:2003;365-370
46. Eddy S.R. Profile hidden Markov models. Bioinformatics. 14:1998;755-763
47. Abeygunawardana C., Weber D.J., Gittis A.G., Frick D.N., Lin J., Miller A.F., et al. Solution structure of the MutT enzyme, a nucleoside triphosphate pyrophosphohydrolase. Biochemistry. 34:1995;14997-15005
48. Lin J., Abeygunawardana C., Frick D.N., Bessman M.J., Mildvan A.S. Solution structure of the quaternary MutT∇M2+-AMPCPP-M2+complex and mechanism of its pyrophosphohydrolase action. Biochemistry. 36:1997;1199-1211
49. Massiah M.A., Saraswat V., Azurmendi H.F., Mildvan A.S. Solution structure and NH exchange studies of the MutT pyrophosphohydrolase complexed with Mg(2+) and 8-oxo-dGMP, a tightly bound product. Biochemistry. 42:2003;10140-10154
50. Gabelli S.B., Bianchet M.A., Ohnishi Y., Ichikawa Y., Bessman M.J., Amzel L.M. Mechanism of the Esherichia coli ADP-ribose pyrophosphatase, a Nudix hydrolase. Biochemistry. 41:2002;9279-9285
51. Swarbrick J.D., Bashtannyk T., Maksel D., Zhang X.R., Blackburn G.M., Gayler K.R., Gooley P.R. The three-dimensional structure of the Nudix enzyme diadenosine tetraphosphate hydrolase from Lupinus angustifolius L. J. Mol. Biol. 302:2000;1165-1177
52. Bailey S., Sedelnikova S.E., Blackburn G.M., Abdelghany H.M., Baker P.J., McLennan A.G., Rafferty J.B. The crystal structure of diadenosine tetraphosphate hydrolase from Caenorhabditis elegans in free and binary complex forms. Structure. 10:2002;589-600
53. Durbecq V., Sainz G., Oudjama Y., Clantin B., Bompard-Gilles C., Tricot C., Caillet J., et al. Crystal structure of isopentenyl diphosphate: dimethylallyl diphosphate isomerase. EMBO J. 20:2001;1530-1537
54. Bonanno J.B., Edo C., Eswar N., Pieper U., Romanowski M.J., Ilyin V., Gerchman S.E., et al. Structural genomics of enzymes involved in sterol/isoprenoid biosynthesis. Proc. Natl Acad. Sci. USA. 98:2001;12896-12901
55. Wouters J., Oudjama Y., Ghosh S., Stalon V., Droogmans L., Oldfield E. Structure and mechanism of action of isopentenylpyrophosphate- dimethylallylpyrophosphate isomerase. J. Am. Chem. Soc. 125:2003;3198-3199
56. Buchko G.W., Ni S., Holbrook S.R., Kennedy M.A. 1H, (13)C, and (15)N NMR assignments of the hypothetical Nudix protein DR0079 from the extremely radiation-resistant bacterium Deinococcus radiodurans. J. Biomol. NMR. 25:2003;169-170
57. Karp P.D., Riley M., Paley S.M., Pellegrini-Toole A., Krummenacker M. Eco Cyc: encyclopedia of Escherichia coli genes and metabolism. Nucl. Acids Res. 27:1999;55-58