Small molecule binding, docking, and characterization of the interaction between Pth1 and peptidyl-tRNA

International Journal of Molecular Sciences

Volumn 14, Issue 11, 2013, Pages 22741-22752

  Hames, Mary C ^a   McFeeters, Hana ^a   Blake Holloway, W ^a   Stanley, Christopher B ^b   Urban, Volker S ^b   McFeeters, Robert L ^a  

^a University of Alabama in Huntsville   (United States)

^b OAK RIDGE NATIONAL LABORATORY   (United States)

Author keywords

Docking; Enzyme substrate complex; Inhibition; Peptidyl tRNA hydrolase; Small angle neutron scattering

Indexed keywords

BACTERIAL PROTEIN; PEPTIDE TRANSFER RIBONUCLEIC ACID; PIPERAZINE DERIVATIVE; PIPERONYLPIPERAZINE; PROTEIN PTH1; TRANSFER RNA; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; ENZYME ACTIVITY; ENZYME BINDING; ENZYME INHIBITION; ENZYME SUBSTRATE COMPLEX; ESCHERICHIA COLI; LIGHT SCATTERING; MOLECULAR DOCKING; NEUTRON SCATTERING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN CLEAVAGE; PROTEIN RNA BINDING;

ANTI-BACTERIAL AGENTS; CARBOXYLIC ESTER HYDROLASES; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; LIGANDS; MAGNETIC RESONANCE SPECTROSCOPY; MOLECULAR DOCKING SIMULATION; MULTIPROTEIN COMPLEXES; NEUTRONS; RNA, TRANSFER, AMINO ACYL; RNA-BINDING PROTEINS; SMALL MOLECULE LIBRARIES;

EID: 84887924167     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms141122741     Document Type: Article

References (43)

1. Jorgensen, F.; Kurland, C.G. Processivity errors of gene expression in Escherichia coli. J. Mol. Biol. 1990, 215, 511-521.
2. Manley, J.L. Synthesis and degradation of termination and premature-termination fragments of beta-galactosidase in vitro and in vivo. J. Mol. Biol. 1978, 125, 407-432.
3. Kurland, C.G.; Ehrenberg, M. Constraints on the accuracy of messenger RNA movement. Q. Rev. Biophys. 1985, 18, 423-450.
4. Heurgue-Hamard, V.; Karimi, R.; Mora, L.; MacDougall, J.; Leboeuf, C.; Grentzmann, G.; Ehrenberg, M.; Buckingham, R.H. Ribosome release factor RF4 and termination factor RF3 are involved in dissociation of peptidyl-tRNA from the ribosome. EMBO J. 1998, 17, 808-816.
5. Karimi, R.; Pavlov, M.Y.; Heurgue-Hamard, V.; Buckingham, R.H.; Ehrenberg, M. Initiation factors IF1 and IF2 synergistically remove peptidyl-tRNAs with short polypeptides from the P-site of translating Escherichia coli ribosomes. J. Mol. Biol. 1998, 281, 241-252.
6. Menninger, J.R. The accumulation as peptidyl-transfer RNA of isoaccepting transfer RNA families in Escherichia coli with temperature-sensitive peptidyl-transfer RNA hydrolase. J. Biol. Chem. 1978, 253, 6808-6813.
7. Cruz-Vera, L.R.; Hernandez-Ramon, E.; Perez-Zamorano, B.; Guarneros, G. The rate of peptidyl-tRNA dissociation from the ribosome during minigene expression depends on the nature of the last decoding interaction. J. Biol. Chem. 2003, 278, 26065-26070.
8. Hernandez-Sanchez, J.; Valadez, J.G.; Herrera, J.V.; Ontiveros, C.; Guarneros, G. Lambda bar minigene-mediated inhibition of protein synthesis involves accumulation of peptidyl-tRNA and starvation for tRNA. EMBO J. 1998, 17, 3758-3765.
9. Tenson, T.; Herrera, J.V.; Kloss, P.; Guarneros, G.; Mankin, A.S. Inhibition of translation and cell growth by minigene expression. J. Bacteriol. 1999, 181, 1617-1622.
10. Rosas-Sandoval, G.; Ambrogelly, A.; Rinehart, J.; Wei, D.; Cruz-Vera, L.R.; Graham, D.E.; Stetter, K.O.; Guarneros, G.; Soll, D. Orthologs of a novel archaeal and of the bacterial peptidyl-tRNA hydrolase are nonessential in yeast. Proc. Natl. Acad. Sci. USA 2002, 99, 16707-16712.
11. Gross, M.; Crow, P.; White, J. The site of hydrolysis by rabbit reticulocyte peptidyl-tRNA hydrolase is the 3'-AMP terminus of susceptible tRNA substrates. J. Biol. Chem. 1992, 267, 2080-2086.
12. Schulman, L.H.; Pelka, H. The structural basis for the resistance of Escherichia coli formylmethionyl transfer ribonucleic acid to cleavage by Escherichia coli peptidyl transfer ribonucleic acid hydrolase. J. Biol. Chem. 1975, 250, 542-547.
13. Dutka, S.; Meinnel, T.; Lazennec, C.; Mechulam, Y.; Blanquet, S. Role of the 1-72 base pair in tRNAs for the activity of Escherichia coli peptidyl-tRNA hydrolase. Nucleic Acids Res. 1993, 21, 4025-4030.
14. Fromant, M.; Schmitt, E.; Mechulam, Y.; Lazennec, C.; Plateau, P.; Blanquet, S. Crystal structure at 1.8 Å resolution and identification of active site residues of Sulfolobus solfataricus peptidyl-tRNA hydrolase. Biochemistry 2005, 44, 4294-4301.
15. Pulavarti, S.V.; Jain, A.; Pathak, P.P.; Mahmood, A.; Arora, A. Solution structure and dynamics of peptidyl-tRNA hydrolase from Mycobacterium tuberculosis H37Rv. J. Mol. Biol. 2008, 378, 165-177.
16. Selvaraj, M.; Roy, S.; Singh, N.S.; Sangeetha, R.; Varshney, U.; Vijayan, M. Structural plasticity and enzyme action: Crystal structures of Mycobacterium tuberculosis peptidyl-tRNA hydrolase. J. Mol. Biol. 2007, 372, 186-193.
17. Schmitt, E.; Fromant, M.; Plateau, P.; Mechulam, Y.; Blanquet, S. Crystallization and preliminary X-ray analysis of Escherichia coli peptidyl-tRNA hydrolase. Proteins 1997, 28, 135-136.
18. Hughes, R.C.; McFeeters, H.; Coates, L.; McFeeters, R.L. Recombinant production, crystallization and X-ray crystallographic structure determination of the peptidyl-tRNA hydrolase of Pseudomonas aeruginosa. Acta Crystallogr. F 2012, 68, 1472-1476.
19. Clarke, T.E.; Romanov, V.; Lam, R.; Gothe, S.A.; Peddi, S.R.; Razumova, E.B.; Lipman, R.S.; Branstrom, A.A.; Chirgadze, N.Y. Structure of Francisella tularensis peptidyl-tRNA hydrolase. Acta crystallogr. F 2011, 67, 446-449.
20. Giorgi, L.; Bontems, F.; Fromant, M.; Aubard, C.; Blanquet, S.; Plateau, P. RNA-binding site of Escherichia coli peptidyl-tRNA hydrolase. J. Biol. Chem. 2011, 286, 39585-39594.
21. Giorgi, L.; Plateau, P.; O'Mahony, G.; Aubard, C.; Fromant, M.; Thureau, A.; Grotli, M.; Blanquet, S.; Bontems, F. NMR-based substrate analog docking to Escherichia coli Peptidyl-tRNA hydrolase. J. Mol. Biol. 2011, 412, 619-633.
22. Ito, K.; Murakami, R.; Mochizuki, M.; Qi, H.; Shimizu, Y.; Miura, K.; Ueda, T.; Uchiumi, T. Structural basis for the substrate recognition and catalysis of peptidyl-tRNA hydrolase. Nucleic Acids Res. 2012, 40, 10521-10531.
23. Harris, S.M.; McFeeters, H.; Ogungbe, I.V.; Cruz-Vera, L.R.; Setzer, W.N.; Jackes, B.R.; McFeeters, R.L. Peptidyl-tRNA hydrolase screening combined with molecular docking reveals the antibiotic potential of Syzygium johnsonii bark extract. Nat. Prod. Commun. 2011, 6, 1421-1424.
24. McFeeters, H.; Gilbert, M.J.; Thompson, R.M.; Setzer, W.N.; Cruz-Vera, L.R.; McFeeters, R.L. Inhibition of essential bacterial peptidyl-tRNA hydrolase activity by tropical plant extracts. Nat. Prod. Commun. 2012, 7, 1107-1110.
25. Svergun, D. Determination of the regularization parameter in indirect-transform methods using perceptual criteria. J. Appl. Crystallogr. 1992, 25, 495-503.
26. Goodall, J.J.; Chen, G.J.; Page, M.G. Essential role of histidine 20 in the catalytic mechanism of Escherichia coli peptidyl-tRNA hydrolase. Biochemistry 2004, 43, 4583-4591.
27. Schmitt, E.; Mechulam, Y.; Fromant, M.; Plateau, P.; Blanquet, S. Crystal structure at 1.2 Å resolution and active site mapping of Escherichia coli peptidyl-tRNA hydrolase. EMBO J. 1997, 16, 4760-4769.
28. Kozin, M.B.; Svergun, D.I. Automated matching of high- and low-resolution structural models. J. Appl. Cryst. 2001, 34, 33-41.
29. Giege, R. Toward a more complete view of tRNA biology. Nat. Struct. Mol. Biol. 2008, 15, 1007-1014.
30. Alexander, R.W.; Eargle, J.; Luthey-Schulten, Z. Experimental and computational determination of tRNA dynamics. FEBS Lett. 2010, 584, 376-386.
31. Atherly, A.G.; Menninger, J.R. Mutant E. coli strain with temperature sensitive peptidyl-transfer RNA hydrolase. Nat. New Biol. 1972, 240, 245-246.
32. Cruz-Vera, L.R.; Toledo, I.; Hernandez-Sanchez, J.; Guarneros, G. Molecular basis for the temperature sensitivity of Escherichia coli pth(Ts). J. Bacteriol. 2000, 182, 1523-1528.
33. Varshney, U.; Lee, C.P.; RajBhandary, U.L. Direct analysis of aminoacylation levels of tRNAs in vivo. Application to studying recognition of Escherichia coli initiator tRNA mutants by glutaminyl-tRNA synthetase. J. Biol. Chem. 1991, 266, 24712-24718.
34. Wignall, G.D.; Bates, F.S. Absolute calibration of small-angle neutron scattering data. J. Appl. Crystallogr. 1987, 20, 28-40.
35. Guinier, A. La diffraction des rayons X aux tres petits angles: Applications a l'etude de phenomenes ultramicroscopiques. Annales de Physique 1939, 12.1939, 161-237.
36. Svergun, D.I. Restoring low resolution structure of biological macromolecules from solution scattering using simulated annealing. Biophys. J. 1999, 76, 2879-2886.
37. Trott, O.; Olson, A.J. AutoDock Vina: Improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. J. Comput. Chem. 2010, 31, 455-461.
38. Sanner, M.F. Python: A programming language for software integration and development. J. Mol. Graph. Model. 1999, 17, 57-61.
39. Pettersen, E.F.; Goddard, T.D.; Huang, C.C.; Couch, G.S.; Greenblatt, D.M.; Meng, E.C.; Ferrin, T.E. UCSF Chimera-A visualization system for exploratory research and analysis. J. Comput. Chem. 2004, 25, 1605-1612.
40. Falb, M.; Amata, I.; Gabel, F.; Simon, B.; Carlomagno, T. Structure of the K-turn U4 RNA: A combined NMR and SANS study. Nucleic Acids Res. 2010, 38, 6274-6285.
41. Grishaev, A.; Ying, J.; Canny, M.D.; Pardi, A.; Bax, A. Solution structure of tRNAVal from refinement of homology model against residual dipolar coupling and SAXS data. J. Biomol. NMR 2008, 42, 99-109.
42. Moroder, H.; Steger, J.; Graber, D.; Fauster, K.; Trappl, K.; Marquez, V.; Polacek, N.; Wilson, D.N.; Micura, R. Non-hydrolyzable RNA-peptide conjugates: A powerful advance in the synthesis of mimics for 3'-peptidyl tRNA termini. Angewandte Chemie 2009, 48, 4056-4060.
43. Geiermann, A.S.; Micura, R. Selective desulfurization significantly expands sequence variety of 3'-peptidyl-tRNA mimics obtained by native chemical ligation. Chembiochem Eur. J. Chem. Biol. 2012, 13, 1742-1745.