Comparison of histidine recognition in human and trypanosomatid histidyl-tRNA synthetases

Biochimie

Volumn 106, Issue , 2014, Pages 111-120

  Koh, Cho Yeow ^a   Wetzel, Allan B ^a   De Van Der Schueren, Will J ^a   Hol, Wim G J ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

Chagas disease; Drug design; Histidyl tRNA synthetase; Sleeping sickness; Trypanosome

Indexed keywords

AMINO ACID; CARBOXYLIC ACID DERIVATIVE; HISTIDINE; HISTIDINE TRANSFER RNA LIGASE; HYDROGEN; IMIDAZOLE; LIGAND; ENZYME INHIBITOR; PROTEIN BINDING; PROTOZOAL PROTEIN;

AMINOACYLATION; ANIMAL CELL; ARTICLE; CHEMICAL ANALYSIS; CONTROLLED STUDY; CRYSTAL STRUCTURE; CYTOSOL; ENZYME ACTIVE SITE; ENZYME CONFORMATION; ENZYME SUBSTRATE; HYDROGEN BOND; KINETOPLASTIDA; MOLECULAR RECOGNITION; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; TRYPANOSOMA BRUCEI; AMINO ACID SEQUENCE; BINDING SITE; BIOCATALYSIS; CHEMICAL STRUCTURE; CHEMISTRY; COMPARATIVE STUDY; DRUG DESIGN; DRUG EFFECTS; ENZYME SPECIFICITY; ENZYMOLOGY; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; PROTEIN CONFORMATION; PROTEIN TERTIARY STRUCTURE; SEQUENCE HOMOLOGY; TRYPANOSOMA BRUCEI BRUCEI; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; BINDING SITES; BIOCATALYSIS; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; DRUG DESIGN; ENZYME INHIBITORS; HISTIDINE; HISTIDINE-TRNA LIGASE; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; PROTOZOAN PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SUBSTRATE SPECIFICITY; TRYPANOSOMA BRUCEI BRUCEI;

EID: 84908017455     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2014.08.005     Document Type: Article

References (53)

1. M. Ibba, and D. Soll Aminoacyl-tRNA synthesis Annu. Rev. Biochem. 69 2000 617 650
2. S. Shibata, J.R. Gillespie, A.M. Kelley, A.J. Napuli, Z. Zhang, K.V. Kovzun, R.M. Pefley, J. Lam, F.H. Zucker, W.C. Van Voorhis, E.A. Merritt, W.G. Hol, C.L. Verlinde, E. Fan, and F.S. Buckner Selective inhibitors of methionyl-tRNA synthetase have potent activity against Trypanosoma brucei infection in mice Antimicrob. Agents Chemother. 55 2011 1982 1989
3. G.H. Vondenhoff, and A. Van Aerschot Aminoacyl-tRNA synthetase inhibitors as potential antibiotics Eur. J. Med. Chem. 46 2011 5227 5236
4. S. Kalidas, I. Cestari, S. Monnerat, Q. Li, S. Regmi, N. Hasle, M. Labaied, M. Parsons, K. Stuart, and M.A. Phillips Genetic validation of aminoacyl-tRNA synthetases as drug targets in Trypanosoma brucei Eukaryot. Cell 13 2014 504 516
5. J.S. Pham, K.L. Dawson, K.E. Jackson, E.E. Lim, C.F. Pasaje, K.E. Turner, and S.A. Ralph Aminoacyl-tRNA synthetases as drug targets in eukaryotic parasites Int. J. Parasitol. Drugs Drug Resist. 4 2014 1 13
6. S. Shibata, J.R. Gillespie, R.M. Ranade, C.Y. Koh, J.E. Kim, J.U. Laydbak, F.H. Zucker, W.G. Hol, C.L. Verlinde, F.S. Buckner, and E. Fan Urea-based inhibitors of Trypanosoma brucei methionyl-tRNA synthetase: selectivity and in vivo characterization J. Med. Chem. 55 2012 6342 6351
7. C.Y. Koh, J.E. Kim, S. Shibata, R.M. Ranade, M. Yu, J. Liu, J.R. Gillespie, F.S. Buckner, C.L. Verlinde, E. Fan, and W.G. Hol Distinct states of methionyl-tRNA synthetase indicate inhibitor binding by conformational selection Structure 20 2012 1681 1691
8. E.T. Larson, J.E. Kim, F.H. Zucker, A. Kelley, N. Mueller, A.J. Napuli, C.L. Verlinde, E. Fan, F.S. Buckner, W.C. Van Voorhis, E.A. Merritt, and W.G. Hol Structure of Leishmania major methionyl-tRNA synthetase in complex with intermediate products methionyladenylate and pyrophosphate Biochimie 93 2011 570 582
9. H. Ingvarsson, and T. Unge Flexibility and communication within the structure of the Mycobacterium smegmatis methionyl-tRNA synthetase FEBS J. 277 2010 3947 3962
10. L. Serre, G. Verdon, T. Choinowski, N. Hervouet, J.L. Risler, and C. Zelwer How methionyl-tRNA synthetase creates its amino acid recognition pocket upon L-methionine binding J. Mol. Biol. 306 2001 863 876
11. Y. Mechulam, E. Schmitt, L. Maveyraud, C. Zelwer, O. Nureki, S. Yokoyama, M. Konno, and S. Blanquet Crystal structure of Escherichia coli methionyl-tRNA synthetase highlights species-specific features J. Mol. Biol. 294 1999 1287 1297
12. V.A. Ilyin, B. Temple, M. Hu, G. Li, Y. Yin, P. Vachette, and C.W. Carter Jr. 2.9 A crystal structure of ligand-free tryptophanyl-tRNA synthetase: domain movements fragment the adenine nucleotide binding site Protein Sci. 9 2000 218 231
13. P. Retailleau, X. Huang, Y. Yin, M. Hu, V. Weinreb, P. Vachette, C. Vonrhein, G. Bricogne, P. Roversi, V. Ilyin, and C.W. Carter Jr. Interconversion of ATP binding and conformational free energies by tryptophanyl-tRNA synthetase: structures of ATP bound to open and closed, pre-transition-state conformations J. Mol. Biol. 325 2003 39 63
14. P. Laowanapiban, M. Kapustina, C. Vonrhein, M. Delarue, P. Koehl, and C.W. Carter Jr. Independent saturation of three TrpRS subsites generates a partially assembled state similar to those observed in molecular simulations Proc. Natl. Acad. Sci. U. S. A. 106 2009 1790 1795
15. N. Shen, M. Zhou, B. Yang, Y. Yu, X. Dong, and J. Ding Catalytic mechanism of the tryptophan activation reaction revealed by crystal structures of human tryptophanyl-tRNA synthetase in different enzymatic states Nucleic Acids Res. 36 2008 1288 1299
16. N. Shen, L. Guo, B. Yang, Y. Jin, and J. Ding Structure of human tryptophanyl-tRNA synthetase in complex with tRNATrp reveals the molecular basis of tRNA recognition and specificity Nucleic Acids Res. 34 2006 3246 3258
17. X.L. Yang, F.J. Otero, K.L. Ewalt, J. Liu, M.A. Swairjo, C. Kohrer, U.L. RajBhandary, R.J. Skene, D.E. McRee, and P. Schimmel Two conformations of a crystalline human tRNA synthetase-tRNA complex: implications for protein synthesis EMBO J. 25 2006 2919 2929
18. C.Y. Koh, J.E. Kim, A.J. Napoli, C.L. Verlinde, E. Fan, F.S. Buckner, W.C. Van Voorhis, and W.G. Hol Crystal structures of Plasmodium falciparum cytosolic tryptophanyl-tRNA synthetase and its potential as a target for structure-guided drug design Mol. Biochem. Parasitol. 189 2013 26 32
19. G. Eriani, M. Delarue, O. Poch, J. Gangloff, and D. Moras Partition of tRNA synthetases into two classes based on mutually exclusive sets of sequence motifs Nature 347 1990 203 206
20. S. Cusack Eleven down and nine to go Nat. Struct. Biol. 2 1995 824 831
21. J.G. Arnez, D.C. Harris, A. Mitschler, B. Rees, C.S. Francklyn, and D. Moras Crystal structure of histidyl-tRNA synthetase from Escherichia coli complexed with histidyl-adenylate EMBO J. 14 1995 4143 4155
22. E.A. Merritt, T.L. Arakaki, J.R. Gillespie, E.T. Larson, A. Kelley, N. Mueller, A.J. Napuli, J. Kim, L. Zhang, C.L. Verlinde, E. Fan, F. Zucker, F.S. Buckner, W.C. van Voorhis, and W.G. Hol Crystal structures of trypanosomal histidyl-tRNA synthetase illuminate differences between eukaryotic and prokaryotic homologs J. Mol. Biol. 397 2010 481 494
23. Z. Xu, Z. Wei, J.J. Zhou, F. Ye, W.S. Lo, F. Wang, C.F. Lau, J. Wu, L.A. Nangle, K.P. Chiang, X.L. Yang, M. Zhang, and P. Schimmel Internally deleted human tRNA synthetase suggests evolutionary pressure for repurposing Structure 20 2012 1470 1477
24. Y.I. Wolf, L. Aravind, N.V. Grishin, and E.V. Koonin Evolution of aminoacyl-tRNA synthetases-analysis of unique domain architectures and phylogenetic trees reveals a complex history of horizontal gene transfer events Genome Res. 9 1999 689 710
25. T.P. O'Hanlon, and F.W. Miller Genomic organization, transcriptional mapping, and evolutionary implications of the human bi-directional histidyl-tRNA synthetase locus (HARS/HARSL) Biochem. Biophys. Res. Commun. 294 2002 609 614
26. X. Qiu, C.A. Janson, M.N. Blackburn, I.K. Chhohan, M. Hibbs, and S.S. Abdel-Meguid Cooperative structural dynamics and a novel fidelity mechanism in histidyl-tRNA synthetases Biochemistry 38 1999 12296 12304
27. A. Yaremchuk, M. Tukalo, M. Grotli, and S. Cusack A succession of substrate induced conformational changes ensures the amino acid specificity of Thermus thermophilus prolyl-tRNA synthetase: comparison with histidyl-tRNA synthetase J. Mol. Biol. 309 2001 989 1002
28. A. Aberg, A. Yaremchuk, M. Tukalo, B. Rasmussen, and S. Cusack Crystal structure analysis of the activation of histidine by Thermus thermophilus histidyl-tRNA synthetase Biochemistry 36 1997 3084 3094
29. J.G. Arnez, J.G. Augustine, D. Moras, and C.S. Francklyn The first step of aminoacylation at the atomic level in histidyl-tRNA synthetase Proc. Natl. Acad. Sci. U. S. A. 94 1997 7144 7149
30. L. Baugh, L.A. Gallagher, R. Patrapuvich, M.C. Clifton, A.S. Gardberg, T.E. Edwards, B. Armour, D.W. Begley, S.H. Dieterich, D.M. Dranow, J. Abendroth, J.W. Fairman, D. Fox 3rd, B.L. Staker, I. Phan, A. Gillespie, R. Choi, S. Nakazawa-Hewitt, M.T. Nguyen, A. Napuli, L. Barrett, G.W. Buchko, R. Stacy, P.J. Myler, L.J. Stewart, C. Manoil, and W.C. Van Voorhis Combining functional and structural genomics to sample the essential Burkholderia structome PLoS One 8 2013 e53851
31. C.Y. Koh, J.E. Kim, A.B. Wetzel, W.J. de van der Schueren, S. Shibata, R.M. Ranade, J. Liu, Z. Zhang, J.R. Gillespie, F.S. Buckner, C.L. Verlinde, E. Fan, and W.G. Hol Structures of Trypanosoma brucei methionyl-tRNA synthetase with urea-based inhibitors provide guidance for drug design against sleeping sickness PLoS Negl. Trop. Dis. 8 2014 e2775
32. E.T. Larson, J.E. Kim, L.J. Castaneda, A.J. Napuli, Z. Zhang, E. Fan, F.H. Zucker, C.L. Verlinde, F.S. Buckner, W.C. Van Voorhis, W.G. Hol, and E.A. Merritt The double-length tyrosyl-tRNA synthetase from the eukaryote Leishmania major forms an intrinsically asymmetric pseudo-dimer J. Mol. Biol. 409 2011 159 176
33. C. Mehlin, E. Boni, F.S. Buckner, L. Engel, T. Feist, M.H. Gelb, L. Haji, D. Kim, C. Liu, N. Mueller, P.J. Myler, J.T. Reddy, J.N. Sampson, E. Subramanian, W.C. Van Voorhis, E. Worthey, F. Zucker, and W.G. Hol Heterologous expression of proteins from Plasmodium falciparum: results from 1000 genes Mol. Biochem. Parasitol. 148 2006 144 160
34. R. Choi, A. Kelley, D. Leibly, S.N. Hewitt, A. Napuli, and W. Van Voorhis Immobilized metal-affinity chromatography protein-recovery screening is predictive of crystallographic structure success Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 67 2011 998 1005
35. F.W. Studier Protein production by auto-induction in high density shaking cultures Protein Expr. Purif. 41 2005 207 234
36. W. Kabsch XDS Acta Crystallogr. D Biol. Crystallogr. 66 2010 125 132
37. M.D. Winn, C.C. Ballard, K.D. Cowtan, E.J. Dodson, P. Emsley, P.R. Evans, R.M. Keegan, E.B. Krissinel, A.G. Leslie, A. McCoy, S.J. McNicholas, G.N. Murshudov, N.S. Pannu, E.A. Potterton, H.R. Powell, R.J. Read, A. Vagin, and K.S. Wilson Overview of the CCP4 suite and current developments Acta Crystallogr. D Biol. Crystallogr. 67 2011 235 242
38. E. Krissinel, and K. Henrick Inference of macromolecular assemblies from crystalline state J. Mol. Biol. 372 2007 774 797
39. N. Stein CHAINSAW: a program for mutating PDB files used as templates in molecular replacement J. Appl. Crystallogr. 41 2008 641 643
40. A.J. McCoy, R.W. Grosse-Kunstleve, P.D. Adams, M.D. Winn, L.C. Storoni, and R.J. Read Phaser crystallographic software J. Appl. Crystallogr. 40 2007 658 674
41. P. Emsley, and K. Cowtan Coot: model-building tools for molecular graphics Acta Crystallogr. D Biol. Crystallogr. 60 2004 2126 2132
42. G.N. Murshudov, A.A. Vagin, and E.J. Dodson Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallogr. D Biol. Crystallogr. 53 1997 240 255
43. J. Painter, and E.A. Merritt TLSMD web server for the generation of multi-group TLS models J. Appl. Cryst. 39 2006 109 111
44. V.B. Chen, W.B. Arendall 3rd, J.J. Headd, D.A. Keedy, R.M. Immormino, G.J. Kapral, L.W. Murray, J.S. Richardson, and D.C. Richardson MolProbity: all-atom structure validation for macromolecular crystallography Acta Crystallogr. D Biol. Crystallogr. 66 2010 12 21
45. W. DeLano The PyMOL Molecular Graphics System 2002 http://www.pymol.org
46. E. Krissinel, and K. Henrick Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions Acta Crystallogr. D Biol. Crystallogr. 60 2004 2256 2268
47. S. Hayward, and H.J. Berendsen Systematic analysis of domain motions in proteins from conformational change: new results on citrate synthase and T4 lysozyme Proteins 30 1998 144 154
48. J.J. Perona, and I. Gruic-Sovulj Synthetic and editing mechanisms of aminoacyl-tRNA synthetases Top. Curr. Chem. 344 2014 1 41
49. I.H. Gilbert Drug discovery for neglected diseases: molecular target-based and phenotypic approaches J. Med. Chem. 56 2013 7719 7726
50. T. Nakama, O. Nureki, and S. Yokoyama Structural basis for the recognition of isoleucyl-adenylate and an antibiotic, mupirocin, by isoleucyl-tRNA synthetase J. Biol. Chem. 276 2001 47387 47393
51. M. Teng, M.T. Hilgers, M.L. Cunningham, A. Borchardt, J.B. Locke, S. Abraham, G. Haley, B.P. Kwan, C. Hall, G.W. Hough, K.J. Shaw, and J. Finn Identification of bacteria-selective threonyl-tRNA synthetase substrate inhibitors by structure-based design J. Med. Chem. 56 2013 1748 1760
52. F. Sievers, A. Wilm, D. Dineen, T.J. Gibson, K. Karplus, W. Li, R. Lopez, H. McWilliam, M. Remmert, J. Soding, J.D. Thompson, and D.G. Higgins Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega Mol. Syst. Biol. 7 2011 539
53. P. Gouet, X. Robert, and E. Courcelle ESPript/ENDscript: extracting and rendering sequence and 3D information from atomic structures of proteins Nucleic Acids Res. 31 2003 3320 3323