The crystal structure of ribonuclease a in complex with thymidine-3'-monophosphate provides further insight into ligand binding

Proteins: Structure, Function and Bioinformatics

Volumn 78, Issue 11, 2010, Pages 2459-2468

  Doucet, Nicolas ^a,c   Jayasundera, Thusitha B ^a,d   Simonović, Miljan ^b   Loria, J Patrick ^a  

^a YALE UNIVERSITY   (United States)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^c INSTITUT NATIONAL DE LA RECHERCHE SCIENTIFIQUE   (Canada)

^d ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

Crystal structure; Enzyme catalysis; Inhibitors; ITC; NMR; Nucleotides; Ribonuclease A; RNA cleavage

Indexed keywords

PYRIMIDINE; RIBONUCLEASE A; RIBOSE; THYMIDINE 3' MONOPHOSPHATE; THYMINE DERIVATIVE; UNCLASSIFIED DRUG; CYTIDINE PHOSPHATE; LIGAND; PANCREATIC RIBONUCLEASE; PROTEIN BINDING; THYMIDINE PHOSPHATE;

ARTICLE; BINDING AFFINITY; BINDING SITE; CRYSTAL STRUCTURE; FEMALE; LIGAND BINDING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; ANIMAL; BOVINAE; CHEMISTRY; HUMAN; METABOLISM; THERMODYNAMICS; X RAY CRYSTALLOGRAPHY;

BOVINAE;

ANIMALS; CATTLE; CRYSTALLOGRAPHY, X-RAY; CYTIDINE MONOPHOSPHATE; HUMANS; LIGANDS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN BINDING; RIBONUCLEASE, PANCREATIC; THERMODYNAMICS; THYMIDINE MONOPHOSPHATE;

EID: 77955824806     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.22754     Document Type: Article

References (55)

1. Marshall GR, Feng JA, Kuster DJ. Back to the future: ribonuclease A. Biopolymers 2008; 90:259-277.
2. Raines R. Ribonuclease A. Chem Rev 1998; 98:1045-1065.
3. Dyer KD, Rosenberg HF. The RNase A superfamily: generation of diversity and innate host defense. Mol Divers 2006; 10:585-597.
4. Pavel ME, Hassler G, Baum U, Hahn EG, Lohmann T, Schuppan D. Circulating levels of angiogenic cytokines can predict tumour progression and prognosis in neuroendocrine carcinomas. Clin Endocrinol 2005; 62:434-443.
5. Loverix S, Steyaert J. Ribonucleases: from prototypes to therapeutic targets? Curr Med Chem 2003; 10:779-785.
6. Schein CH. From housekeeper to microsurgeon: the diagnostic and therapeutic potential of ribonucleases. Nat Biotechnol 1997; 15:529-536.
7. Lehrer RI, Szklarek D, Barton A, Ganz T, Hamann KJ, Gleich GJ. Antibacterial properties of eosinophil major basic protein and eosinophil cationic protein. J Immunol 1989; 142:4428-4434.
8. Ye B, Skates S, Mok SC, Horick NK, Rosenberg HF, Vitonis A, Edwards D, Sluss P, Han WK, Berkowitz RS, Cramer DW. Proteomic-based discovery and characterization of glycosylated eosinophil-derived neurotoxin and COOH-terminal osteopontin fragments for ovarian cancer in urine. Clin Cancer Res 2006; 12:432-441.
9. Hidaka Y, Kimura M, Izumi Y, Takano T, Tatsumi KI, Amino N. Increased serum concentration of eosinophil-derived neurotoxin in patients with Graves' disease. Thyroid 2003; 13:129-132.
10. Riordan JF. Structure and function of angiogenin. In: D'Alessio G, Riordan JF, editors. Ribonucleases structures and functions. New York: Academic Press; 1997. pp 272-304.
11. Youle RJ, D'Alessio G. Antitumor RNases. In: D'Alessio G, Riordan JF, editors. Ribonucleases structures and functions. New York: Academic Press; 1997. pp 272-304.
12. Thompson JE, Venegas FD, Raines RT. Energetics of catalysis by ribonucleases: fate of the 20, 30-cyclic phosphodiester intermediate. Biochemistry 1994; 33:7408-7414.
13. Cuchillo CM, Pares X, Guasch A, Barman T, Travers F, Nogues MV. The role of 20, 30-cyclic phosphodiesters in the bovine pancreatic ribonuclease A catalysed cleavage of RNA: intermediates or products? FEBS Lett 1993; 333:207-210.
14. Park C, Raines RT. Catalysis by ribonuclease A is limited by the rate of substrate association. Biochemistry 2003; 42:3509-3518.
15. Bugg TD. The development of mechanistic enzymology in the 20th century. Nat Prod Rep 2001; 18:465-493.
16. Wolfenden R, Snider MJ. The depth of chemical time and the power of enzymes as catalysts. Acc Chem Res 2001; 34:938-945.
17. Russo A, Acharya KR, Shapiro R. Small molecule inhibitors of RNase A and related enzymes. Methods Enzymol 2001; 341:629-648.
18. Beach H, Cole R, Gill ML, Loria JP. Conservation of ls-ms enzyme motions in the apo-and substrate-mimicked state. J Am Chem Soc 2005; 127:9167-9176.
19. Kovrigin EL, Cole R, Loria JP. Temperature dependence of the backbone dynamics of ribonuclease A in the ground state and bound to the inhibitor 50-phosphothymidine (30-50) pyrophosphate adenosine 30-phosphate. Biochemistry 2003; 42:5279-5291.
20. Russo N, Shapiro R. Potent inhibition of mammalian ribonucleases by 30, 50-pyrophosphate-linked nucleotides. J Biol Chem 1999; 274:14902-14908.
21. Hatzopoulos GN, Leonidas DD, Kardakaris R, Kobe J, Oikonomakos NG. The binding of IMP to ribonuclease A. FEBS J 2005; 272:3988-4001.
22. Aguilar CF, Thomas PJ, Mills A, Moss DS, Palmer RA. Newly observed binding mode in pancreatic ribonuclease. J Mol Biol 1992; 224:265-267.
23. Zegers I, Maes D, Dao-Thi MH, Poortmans F, Palmer R, Wyns L. The structures of RNase A complexed with 30-CMP and d (CpA): active site conformation and conserved water molecules. Protein Sci 1994; 3:2322-2339.
24. Leonidas DD, Chavali GB, Oikonomakos NG, Chrysina ED, Kosmopoulou MN, Vlassi M, Frankling C, Acharya KR. High-resolution crystal structures of ribonuclease A complexed with adenylic and uridylic nucleotide inhibitors. Implications for structure-based design of ribonucleolytic inhibitors. Protein Sci 2003; 12:2559-2574.
25. Fisher BM, Schultz LW, Raines RT. Coulombic effects of remote subsites on the active site of ribonuclease A. Biochemistry 1998; 37:17386-17401.
26. Otwinowski Z, Minor W. Processing of x-ray diffraction data collected in oscillation mode. Method Enzymol 1997; 276:307-326.
27. Larson SB, Day JS, Cudney R, McPherson A. A new crystal form of bovine pancreatic RNase A in complex with 20-deoxyguanosine-50-monophosphate. Acta Crystallogr Sect F: Struct Biol Cryst Commun 2007; 63:728-733.
28. McCoy AJ, Grosse-Kunstleve RW, Storoni LC, Read RJ. Likelihoodenhanced fast translation functions. Acta Crystallogr D Biol Crystallogr 2005; 61:458-464.
29. Storoni LC, McCoy AJ, Read RJ. Likelihood-enhanced fast rotation functions. Acta Crystallogr D Biol Crystallogr 2004; 60:432-438.
30. Brunger AT, Adams PD, Clore GM, DeLano WL, Gros P, Grosse-Kunstleve RW, Jiang JS, Kuszewski J, Nilges M, Pannu NS, Read RJ, Rice LM, Simonson T, Warren GL. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr D Biol Crystallogr 1998; 54:905-921.
31. Brunger AT. Version 1.2 of the crystallography and NMR system. Nat Protoc 2007; 2:2728-2733.
32. MicroCal. ITC data analysis in Origin. Northampton, MA: Micro-Cal, Inc.; 1998. 81 p.
33. Jelesarov I, Bosshard HR. Isothermal titration calorimetry and differential scanning calorimetry as complementary tools to investigate the energetics of biomolecular recognition. J Mol Recognit 1999; 12:3-18.
34. Doucet N, Watt ED, Loria JP. The flexibility of a distant loop modulates active site motion and product release in ribonuclease A. Biochemistry 2009; 48:7160-7168.
35. delCardayré SB, Ribo M, Yokel EM, Quirk DJ, Rutter WJ, Raines RT. Engineering ribonuclease A: production, purification and characterization of wild-type enzyme and mutants at Gln11. Protein Eng 1995; 8:261-273.
36. Cavanagh J, Fairbrother WJ, Palmer AG, Rance M, Skelton NJ. Protein NMR spectroscopy: principles and practice. San Diego: Elsevier Academic; 2007.
37. Kovrigin EL, Loria JP. Enzyme dynamics along the reaction coordinate: critical role of a conserved residue. Biochemistry 2006; 45:2636-2647.
38. Wlodawer A, Svensson LA, Sjolin L, Gilliland GL. Structure of phosphate-free ribonuclease A refined at 1.26 Å. Biochemistry 1988; 27:2705-2717.
39. Watt ED, Shimada H, Kovrigin EL, Loria JP. The mechanism of rate-limiting motions in enzyme function. Proc Natl Acad Sci 2007; 104:11981-11986.
40. Santoro J, Gonzalez C, Bruix M, Neira JL, Nieto JL, Herranz J, Rico M. High-resolution three-dimensional structure of ribonuclease A in solution by nuclear magnetic resonance spectroscopy. J Mol Biol 1993; 229:722-734.
41. Berisio R, Lamzin VS, Sica F, Wilson KS, Zagari A, Mazzarella L. Protein titration in the crystal state. J Mol Biol 1999; 292:845-854.
42. Fedorov AA, Joseph-McCarthy D, Fedorov E, Sirakova D, Graf I, Almo SC. Ionic interactions in crystalline bovine pancreatic ribonuclease A. Biochemistry 1996; 35:15962-15979.
43. de Mel VSJ, Doscher MS, Martin PD, Edwards BFP. The occupancy of two distinct conformations by active-site histidine-119 in crystals of ribonuclease is modulated by pH. FEBS Lett 1994; 349:155-160.
44. Cuchillo C, Vilanova M, Nogués MV. Pancreatic ribonucleases. In: D'Alessio G, Riordan JF, editors. Ribonucleases structures and functions. New York: Academic Press; 1997. pp 272-304.
45. Gilliland GL, Dill J, Pechik I, Svensson LA, Sjolin L. The active site of bovine pancreatic ribonuclease: an example of solvent modulated specificity. Protein Pept Lett 1994; 1:60-65.
46. Lisgarten JN, Gupta V, Maes D, Wyns L, Zegers I, Palmer RA, Dealwis CG, Aguilar CF, Hemmings AM. Structure of the crystalline complex of cytidylic acid (2'-CMP) with ribonuclease at 1.6 Å resolution. Conservation of solvent sites in RNase-A high-resolution structures. Acta Crystallogr D Biol Crystallogr 1993; 49:541-547.
47. Moodie SL, Thornton JM. A study into the effects of protein binding on nucleotide conformation. Nucleic Acids Res 1993; 21:1369-1380.
48. Tsirkone VG, Dossi K, Drakou C, Zographos SE, Kontou M, Leonidas DD. Inhibitor design for ribonuclease A: the binding of two 5'-phosphate uridine analogues. Acta Crystallogr Sect F: Struct Biol Cryst Commun 2009; 65:671-677.
49. Ladner JE, Wladkowski BD, Svensson LA, Sjolin L, Gilliland GL. X-ray structure of a ribonuclease A-uridine vanadate complex at 1.3 Å resolution. Acta Crystallogr D Biol Crystallogr 1997; 53:290-301.
50. Vitagliano L, Merlino A, Zagari A, Mazzarella L. Productive and nonproductive binding to ribonuclease A: X-ray structure of two complexes with uridylyl (2', 5') guanosine. Protein Sci 2000; 9:1217-1225.
51. Listgarten JN, Maes D, Wyns L, Aguilar CF, Palmer RA. Structure of the crystalline complex of deoxycytidylyl-3', 5'-guanosine (3', 5'-dCpdG) cocrystallized with ribonuclease at 1.9 Å resolution. Acta Crystallogr D Biol Crystallogr 1995; 51:767-771.
52. Borah B, Chen CW, Egan W, Miller M, Wlodawer A, Cohen JS. Nuclear magnetic resonance and neutron diffraction studies of the complex of ribonuclease A with uridine vanadate, a transition-state analogue. Biochemistry 1985; 24:2058-2067.
53. Birdsall DL, McPherson A. Crystal structure disposition of thymidylic acid tetramer in complex with ribonuclease A. J Biol Chem 1992; 267:22230-22236.
54. Lee GM, Craik CS. Trapping moving targets with small molecules. Science 2009; 324:213-215.
55. Grzesiek S, Stahl SJ, Wingfield PT, Bax A. The CD4 determinant for downregulation by HIV-1 Nef directly binds to Nef. Mapping of the Nef binding surface by NMR. Biochemistry 1996; 35:10256-10261.