Crystal structures of the novel cytosolic 5′-nucleotidase IIIB explain its preference for m7GMP

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  Monecke, Thomas ^a   Buschmann, Juliane ^b   Neumann, Piotr ^a   Wahle, Elmar ^b   Ficner, Ralf ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

5' NUCLEOTIDASE; 7 METHYLGUANOSINE; AROMATIC AMINO ACID; CYTIDINE; CYTOSOLIC 5' NUCLEOTIDASE III LIKE PROTEIN; GUANOSINE PHOSPHATE; PURINE; PYRIMIDINE; TRYPTOPHAN; UNCLASSIFIED DRUG; 7-METHYLGUANINE; 7-METHYLGUANOSINE-5'-MONOPHOSPHATE; CAPPED RNA; GUANINE; ISOENZYME; RECOMBINANT PROTEIN;

ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLIZATION; DROSOPHILA MELANOGASTER; ENZYME ACTIVE SITE; ENZYME SPECIFICITY; MOLECULAR DOCKING; PROTEIN DEPHOSPHORYLATION; SITE DIRECTED MUTAGENESIS; AMINO ACID SEQUENCE; ANALOGS AND DERIVATIVES; ANIMAL; CHEMISTRY; ENZYMOLOGY; ESCHERICHIA COLI; GENE EXPRESSION; GENETICS; HUMAN; METABOLISM; MOLECULAR DYNAMICS; MOLECULAR GENETICS; MUTATION; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; THERMODYNAMICS; X RAY CRYSTALLOGRAPHY;

5'-NUCLEOTIDASE; AMINO ACID SEQUENCE; ANIMALS; CRYSTALLOGRAPHY, X-RAY; CYTIDINE; DROSOPHILA MELANOGASTER; ESCHERICHIA COLI; GENE EXPRESSION; GUANINE; HUMANS; ISOENZYMES; MOLECULAR DOCKING SIMULATION; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; RNA CAP ANALOGS; SUBSTRATE SPECIFICITY; THERMODYNAMICS;

EID: 84897446590     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0090915     Document Type: Article

References (50)

1. Bianchi V, Spychala J (2003) Mammalian 5′-nucleotidases. J Biol Chem 278: 46195-46198.
2. Rampazzo C, Miazzi C, Franzolin E, Pontarin G, Ferraro P, et al. (2010) Regulation by degradation, a cellular defense against deoxyribonucleotide pool imbalances. Mutat Res 703: 2-10.
3. Reaves ML, Young BD, Hosios AM, Xu Y-F, Rabinowitz JD (2013) Pyrimidine homeostasis is accomplished by directed overflow metabolism. Nature 500: 237-241.
4. Hunsucker SA, Mitchell BS, Spychala J (2005) The 5′-nucleotidases as regulators of nucleotide and drug metabolism. Pharmacol Ther 107: 1-30. (Pubitemid 40800406)
5. Rinaldo-Matthis A, Rampazzo C, Reichard P, Bianchi V, Nordlund P (2002) Crystal structure of a human mitochondrial deoxyribonucleotidase. Nat Struct Biol 9: 779-787.
6. Walldén K, Ruzzenente B, Rinaldo-Matthis A, Bianchi V, Nordlund P (2005) Structural basis for substrate specificity of the human mitochondrial deoxyribonucleotidase. Structure/Folding and Design 13: 1081-1088. (Pubitemid 40943338)
7. Walldén K, Rinaldo-Matthis A, Ruzzenente B, Rampazzo C, Bianchi V, et al. (2007) Crystal Structures of Human and Murine Deoxyribonucleotidases: Insights into Recognition of Substrates and Nucleotide Analogues. Biochemistry 46: 13809-13818. (Pubitemid 350223908)
8. Knapp K, Zebisch M, Pippel J, El-Tayeb A, Müller CE, et al. (2012) Crystal structure of the human ecto-5′-nucleotidase (CD73): insights into the regulation of purinergic signaling. Structure 20: 2161-2173.
9. Heuts DPHM, Weissenborn MJ, Olkhov RV, Shaw AM, Gummadova J, et al. (2012) Crystal structure of a soluble form of human CD73 with ecto-5′-nucleotidase activity. Chembiochem 13: 2384-2391.
10. Walldén K, Stenmark P, Nyman T, Flodin S, Gräslund S, et al. (2007) Crystal structure of human cytosolic 5′-nucleotidase II: insights into allosteric regulation and substrate recognition. J Biol Chem 282: 17828-17836. (Pubitemid 47100283)
11. Walldén K, Nordlund P (2011) Structural basis for the allosteric regulation and substrate recognition of human cytosolic 5′-nucleotidase II. J Mol Biol 408: 684-696.
12. Jordheim LP, Marton Z, Rhimi M, Cros-Perrial E, Lionne C, et al. (2013) Identification and characterization of inhibitors of cytoplasmic 5′-nucleotidase cN-II issued from virtual screening. Biochem Pharmacol 85: 497-506.
13. Bitto E, Bingman CA, Wesenberg GE, McCoy JG, Phillips GN (2006) Structure of pyrimidine 5′-nucleotidase type 1. Insight into mechanism of action and inhibition during lead poisoning. J Biol Chem 281: 20521-20529. (Pubitemid 44065824)
14. Grobosky CL, Lopez JB, Rennie S, Skopelitis DJ, Wiest AT, et al. (2012) Structural basis of substrate specificity and selectivity of murine cytosolic 5′-nucleotidase III. J Mol Biol 423: 540-554.
15. Burroughs AM, Allen KN, Dunaway-Mariano D, Aravind L (2006) Evolutionary genomics of the HAD superfamily: understanding the structural adaptations and catalytic diversity in a superfamily of phosphoesterases and allied enzymes. J Mol Biol 361: 1003-1034. (Pubitemid 44192587)
16. Allegrini S, Scaloni A, Careddu MG, Cuccu G, D'Ambrosio C, et al. (2004) Mechanistic studies on bovine cytosolic 5′-nucleotidase II, an enzyme belonging to the HAD superfamily. Eur J Biochem 271: 4881-4891. (Pubitemid 40065591)
17. Aravind L, Galperin MY, Koonin EV (1998) The catalytic domain of the P-type ATPase has the haloacid dehalogenase fold. Trends Biochem Sci 23: 127-129. (Pubitemid 28189521)
18. Allegrini S, Scaloni A, Ferrara L, Pesi R, Pinna P, et al. (2001) Bovine cytosolic 5′-nucleotidase acts through the formation of an aspartate 52-phosphoenzyme intermediate. J Biol Chem 276: 33526-33532.
19. Collet JF, Stroobant V, Pirard M, Delpierre G, Van Schaftingen E (1998) A new class of phosphotransferases phosphorylated on an aspartate residue in an amino-terminal DXDX(T/V) motif. J Biol Chem 273: 14107-14112. (Pubitemid 28319117)
20. Lahiri SD, Zhang G, Dunaway-Mariano D, Allen KN (2003) The pentacovalent phosphorus intermediate of a phosphoryl transfer reaction. Science 299: 2067-2071. (Pubitemid 36383733)
21. Buschmann J, Moritz B, Jeske M, Lilie H, Schierhorn A, et al. (2013) Identification of Drosophila and Human 7-Methyl GMP-specific Nucleotidases. J Biol Chem 288: 2441-2451.
22. Amici A, Magni G (2002) Human erythrocyte pyrimidine 5′- nucleotidase, PN-I. Arch Biochem Biophys 397: 184-190. (Pubitemid 34852279)
23. Rees DCD, Duley JAJ, Marinaki AMA (2003) Pyrimidine 5′ nucleotidase deficiency. Br J Haematol 120: 375-383.
24. Hokari S, Miyazaki T, Hasegawa M, Komoda T (1998) Enhanced activity of pyrimidine 5′-nucleotidase in rat red blood cells during erythropoiesis. Biol Chem 379: 329-333. (Pubitemid 28152097)
25. Valentine WNW, Fink KK, Paglia DED, Harris SRS, Adams WSW (1974) Hereditary hemolytic anemia with human erythrocyte pyrimidine 5′-nucleotidase deficiency. J Clin Invest 54: 866-879.
26. van Dijk EE, Cougot NN, Meyer SS, Babajko SS, Wahle EE, et al. (2002) Human Dcp2: a catalytically active mRNA decapping enzyme located in specific cytoplasmic structures. EMBO J 21: 6915-6924.
27. Wang Z, Jiao X, Carr-Schmid A, Kiledjian M (2002) The hDcp2 protein is a mammalian mRNA decapping enzyme. Proc Natl Acad Sci U S A 99: 12663-12668.
28. Song M-G, Bail S, Kiledjian M (2013) Multiple Nudix family proteins possess mRNA decapping activity. RNA 19: 390-399.
29. Machnicka MA, Milanowska K, Osman Oglou O, Purta E, Kurkowska M, et al. (2013) MODOMICS: a database of RNA modification pathways-2013 update. Nucleic Acids Res 41: D262-D267.
30. Wang ZZ, Kiledjian MM (2001) Functional Link between the Mammalian Exosome and mRNA Decapping. Cell 107: 12-12.
31. Hendler S, Fürer E, Srinivasan PR (1970) Synthesis and chemical properties of monomers and polymers containing 7-methylguanine and an investigation of their substrate or template properties for bacterial deoxyribonucleic acid or ribonucleic acid polymerases. Biochemistry 9: 4141-4153.
32. Reichard P (2010) Ribonucleotide reductases: Substrate specificity by allostery. Biochem Biophys Res Commun 396: 5-5.
33. Cliff MJ, Bowler MW, Varga A, Marston JP, Szabó J, et al. (2010) Transition state analogue structures of human phosphoglycerate kinase establish the importance of charge balance in catalysis. J Am Chem Soc 132: 6507-6516.
34. Baxter NJ, Blackburn GM, Marston JP, Hounslow AM, Cliff MJ, et al. (2008) Anionic charge is prioritized over geometry in aluminum and magnesium fluoride transition state analogs of phosphoryl transfer enzymes. J Am Chem Soc 130: 3952-3958. (Pubitemid 351429862)
35. Amici A, Ciccioli K, Naponelli V, Raffaelli N, Magni G (2005) Evidence for essential catalytic determinants for human erythrocyte pyrimidine 5′-nucleotidase. Cell Mol Life Sci 62: 1613-1620. (Pubitemid 41021583)
36. Ruszczynska K, Kamienska-Trela K, Wojcik J, Stepinski J, Darzynkiewicz E, et al. (2003) Charge distribution in 7-methylguanine regarding cation-pi interaction with protein factor eIF4E. Biophys J 85: 1450-1456. (Pubitemid 37052231)
37. Strasser A, Dickmanns A, Luhrmann R, Ficner R (2005) Structural basis for m3G-cap-mediated nuclear import of spliceosomal UsnRNPs by snurportin1. EMBO J 24: 2235-2243. (Pubitemid 41032577)
38. Hsu PC, Hodel MR, Thomas JW, Taylor LJ, Hagedorn CH, et al. (2000) Structural requirements for the specific recognition of an m7G mRNA cap. Biochemistry 39: 13730-13736.
39. Mueller U, Darowski N, Fuchs MR, Förster R, Hellmig M, et al. (2012) Facilities for macromolecular crystallography at the Helmholtz-Zentrum Berlin. J Synchrotron Radiat 19: 442-449.
40. Kabsch W (2010) XDS. Acta Crystallogr D Biol Crystallogr 66: 125-132.
41. Vagin A, Teplyakov A (2010) Molecular replacement with MOLREP. Acta Crystallogr D Biol Crystallogr 66: 22-25.
42. Winn MD, Ballard CC, Cowtan KD, Dodson EJ, Emsley P, et al. (2011) Overview of the CCP4 suite and current developments. Acta Crystallogr D Biol Crystallogr 67: 235-242.
43. Adams PD, Afonine PV, Bunkóczi G, Chen VB, Davis IW, et al. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66: 213-221.
44. Emsley P, Lohkamp B, Scott WG, Cowtan K (2010) Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66: 486-501.
45. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, et al. (2004) UCSF Chimera-a visualization system for exploratory research and analysis. J Comput Chem 25: 1605-1612.
46. Bosse-Doenecke E, Weininger U, Gopalswamy M, Balbach J, Knudsen SM, et al. (2008) High yield production of recombinant native and modified peptides exemplified by ligands for G-protein coupled receptors. Protein Expr Purif 58: 114-121.
47. Sambrook JJ, Russell DDW (2001) Molecular cloning. CSHL Press. 1 pp.
48. Mossessova E, Lima CD (2000) Ulp1-SUMO crystal structure and genetic analysis reveal conserved interactions and a regulatory element essential for cell growth in yeast. Mol Cell 5: 865-876.
49. Sanner MF (1999) Python: a programming language for software integration and development. J Mol Graph Model 17: 57-61.
50. Trott O, Olson AJ (2010) AutoDock Vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. J Comput Chem 31: 455-461.