Structural Characterization of the Mammalian Deoxynucleotide N-Hydrolase Rcl and Its Stabilizing Interactions with Two Inhibitors

Journal of Molecular Biology

Volumn 394, Issue 3, 2009, Pages 435-447

  Yang, Yinshan ^a,b,c,d   Padilla, André ^a,b,c,d   Zhang, Chi ^e   Labesse, Gilles ^a,b,c,d   Kaminski, P Alexandre ^e  

^a CENTRE DE BIOCHIMIE STRUCTURALE   (France)

^b INSERM   (France)

^c UNIV MONTPELLIER   (France)

^d Institut Pasteur ^*  (France)

^e INSTITUT PASTEUR   (France)

Author keywords

dimeric enzyme; directed mutagenesis; GMP; ligand induced fit; molecular modeling

Indexed keywords

ACICLOVIR; ALANINE; ASPARAGINE; ASPARTIC ACID; DIMER; GUANOSINE PHOSPHATE; LIGAND; ONCOPROTEIN; PURINE 2' DEOXYRIBONUCLEOSIDE 5' MONOPHOSPHATE N GLYCOSIDASE; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CONTROLLED STUDY; ENZYME STRUCTURE; LIGAND BINDING; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN INTERACTION; STRUCTURE ANALYSIS; WILD TYPE;

MAMMALIA;

5'-GUANYLIC ACID; ACYCLOVIR; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; BASE SEQUENCE; BINDING SITES; DIMERIZATION; DNA; ENZYME INHIBITORS; ENZYME STABILITY; GENETIC VARIATION; KINETICS; LIGANDS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; N-GLYCOSYL HYDROLASES; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY; RATS; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 70449519338     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2009.10.004     Document Type: Article

References (40)

1. Lewis B.C., Shim H., Li Q., Wu C.S., Lee L.A., Maity A., and Dang C.V. Identification of putative c-Myc-responsive genes: characterization of rcl, a novel growth-related gene. Mol. Cell. Biol. 17 (1997) 4967-4978
2. Rhodes D.R., Barrette T.R., Rubin M.A., Ghosh D., and Chinnaiyan A.M. Meta-analysis of microarrays: interstudy validation of gene expression profiles reveals pathway dysregulation in prostate cancer. Cancer Res. 62 (2002) 4427-4433
3. Shin S., Bosc D.G., Ingle J.N., Spelsberg T.C., and Janknecht R. Rcl is a novel ETV1/ER81 target gene upregulated in breast tumors. J. Cell. Biochem. 105 (2008) 866-874
4. Lewis B.C., Prescott J.E., Campbell S.E., Shim H., Orlowski R.Z., and Dang C.V. Tumor induction by the c-Myc target genes rcl and lactate dehydrogenase A. Cancer Res. 60 (2000) 6178-6183
5. Ludwig A., Dietel M., and Lage H. Identification of differentially expressed genes in classical and atypical multidrug-resistant gastric carcinoma cells. Anticancer Res. 22 (2002) 3213-3221
6. Almon R.R., DuBois D.C., and Jusko W.J. A microarray analysis of the temporal response of liver to methylprednisolone: a comparative analysis of two dosing regimens. Endocrinology 148 (2007) 2209-2225
7. Miki Y., Suzuki T., Tazawa C., Ishizuka M., Semba S., Gorai I., and Sasano H. Analysis of gene expression induced by diethylstilbestrol (DES) in human primitive Mullerian duct cells using microarray. Cancer Lett. 220 (2005) 197-210
8. Ghiorghi Y.K., Zeller K.I., Dang C.V., and Kaminski P.A. The c-Myc target gene Rcl (C6orf108) encodes a novel enzyme, deoxynucleoside 5′-monophosphate N-glycosidase. J. Biol. Chem. 282 (2007) 8150-8156
9. Brown N.S., and Bicknell R. Thymidine phosphorylase, 2-deoxy-d-ribose and angiogenesis. Biochem. J. 334 (1998) 1-8
10. Kaminski P.A. Functional cloning, heterologous expression, and purification of two different N-deoxyribosyltransferases from Lactobacillus helveticus. J. Biol. Chem. 277 (2002) 14400-14407
11. Armstrong S.R., Cook W.J., Short S.A., and Ealick S.E. Crystal structures of nucleoside 2-deoxyribosyltransferase in native and ligand-bound forms reveal architecture of the active site. Structure 4 (1996) 97-107
12. Cornilescu G., Delaglio F., and Bax A. Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J. Biomol. NMR 13 (1999) 289-302
13. Berjanskii M.V., Neal S., and Wishart D.S. PREDITOR: a web server for predicting protein torsion angle restraints. Nucleic Acids Res. 34 (2006) W63-W69
14. Lindhout D.A., Boyko R.F., Corson D.C., Li M.X., and Sykes B.D. The role of electrostatics in the interaction of the inhibitory region of troponin I with troponin C. Biochemistry 44 (2005) 14750-14759
15. Guntert P. Automated NMR structure calculation with CYANA. Methods Mol. Biol. 278 (2004) 353-378
16. 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 Crystallogr., Sect. D: Biol. Crystallogr. 54 (1998) 905-921
17. Dosset P., Hus J.C., Blackledge M., and Marion D. Efficient analysis of macromolecular rotational diffusion from heteronuclear relaxation data. J. Biomol. NMR 16 (2000) 23-28
18. Anand R., Kaminski P.A., and Ealick S.E. Structures of purine 2′-deoxyribosyltransferase, substrate complexes, and the ribosylated enzyme intermediate at 2.0 Å resolution. Biochemistry 43 (2004) 2384-2393
19. Bosch J., Robien M.A., Mehlin C., Boni E., Riechers A., Buckner F.S., et al. Using fragment cocktail crystallography to assist inhibitor design of Trypanosoma brucei nucleoside 2-deoxyribosyltransferase. J. Med. Chem. 49 (2006) 5939-5946
20. Danzin C., and Cardinaud R. Deoxyribosyl transfer catalysis with trans-N-deoxyribosylase. Kinetic studies of purine-to-purine trans-N-deoxyribosylase. Eur. J. Biochem. 48 (1974) 255-262
21. Porter D.J., Merrill B.M., and Short S.A. Identification of the active site nucleophile in nucleoside 2-deoxyribosyltransferase as glutamic acid 98. J. Biol. Chem. 270 (1995) 15551-15556
22. Short S.A., Armstrong S.R., Ealick S.E., and Porter D.J. Active site amino acids that participate in the catalytic mechanism of nucleoside 2′-deoxyribosyltransferase. J. Biol. Chem. 271 (1996) 4978-4987
23. Smar M., Short S.A., and Wolfenden R. Lyase activity of nucleoside 2-deoxyribosyltransferase: transient generation of ribal and its use in the synthesis of 2′-deoxynucleosides. Biochemistry 30 (1991) 7908-7912
24. Grochowski L.L., and Zabriskie T.M. Characterization of BlsM, a nucleotide hydrolase involved in cytosine production for the biosynthesis of blasticidin S. ChemBioChem 7 (2006) 957-964
25. Zhang Y., Cottet S.E., and Ealick S.E. Structure of Escherichia coli AMP nucleosidase reveals similarity to nucleoside phosphorylases. Structure 12 (2004) 1383-1394
26. Leung H.B., and Schramm V.L. Adenylate degradation in Escherichia coli. The role of AMP nucleosidase and properties of the purified enzyme. J. Biol. Chem. 255 (1980) 10867-10874
27. Hurwitz J., Heppel L.A., and Horecker B.L. The enzymatic cleavage of adenylic acid to adenine and ribose 5-phosphate. J. Biol. Chem. 226 (1957) 525-540
28. Miles R.W., Tyler P.C., Furneaux R.H., Bagdassarian C.K., and Schramm V.L. One-third-the-sites transition-state inhibitors for purine nucleoside phosphorylase. Biochemistry 37 (1998) 8615-8621
29. Li C.M., Tyler P.C., Furneaux R.H., Kicska G., Xu Y., Grubmeyer C., et al. Transition-state analogs as inhibitors of human and malarial hypoxanthine-guanine phosphoribosyltransferases. Nat. Struct. Biol. 6 (1999) 582-587
30. Kicska G.A., Long L., Horig H., Fairchild C., Tyler P.C., Furneaux R.H., et al. Immucillin H, a powerful transition-state analog inhibitor of purine nucleoside phosphorylase, selectively inhibits human T lymphocytes. Proc. Natl Acad. Sci. USA 98 (2001) 4593-4598
31. Galmarini C.M. Drug evaluation: forodesine-PNP inhibitor for the treatment of leukemia, lymphoma and solid tumor. IDrugs 9 (2006) 712-722
32. Korycka A., Blonski J.Z., and Robak T. Forodesine (BCX-1777, Immucillin H)-a new purine nucleoside analogue: mechanism of action and potential clinical application. Mini Rev. Med. Chem. 7 (2007) 976-983
33. Berti P.J., and McCann J.A. Toward a detailed understanding of base excision repair enzymes: transition state and mechanistic analyses of N-glycoside hydrolysis and N-glycoside transfer. Chem. Rev. 106 (2006) 506-555
34. Catherinot V., and Labesse G. ViTO: tool for refinement of protein sequence-structure alignments. Bioinformatics 20 (2004) 3694-3696
35. Canutescu A.A., Shelenkov A.A., and Dunbrack Jr. R.L. A graph-theory algorithm for rapid protein side-chain prediction. Protein Sci. 12 (2003) 2001-2014
36. Sali A., and Blundell T.L. Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234 (1993) 779-815
37. Svergun D.I., Petoukhov M.V., and Koch M.H. Determination of domain structure of proteins from X-ray solution scattering. Biophys. J. 80 (2001) 2946-2953
38. Barthe P., Chiche L., Declerck N., Delsuc M.A., Lefevre J.F., Malliavin T., et al. Refined solution structure and backbone dynamics of 15-->N-labeled C12A-p8MTCP1 studied by NMR relaxation. J. Biomol. NMR 15 (1999) 271-288
39. Malliavin T.E., Pons J.L., and Delsuc M.A. An NMR assignment module implemented in the Gifa NMR processing program. Bioinformatics 14 (1998) 624-631
40. 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. Crystallogr. 26P (1993) 283-291