Crystal structures of Plasmodium falciparum cytosolic tryptophanyl-tRNA synthetase and its potential as a target for structure-guided drug design

Molecular and Biochemical Parasitology

Volumn 189, Issue 1-2, 2013, Pages 26-32

  Koh, Cho Yeow ^a   Kim, Jessica E ^a   Napoli, Alberto J ^b   Verlinde, Christophe L M J ^a   Fan, Erkang ^a   Buckner, Frederick S ^b   Van Voorhis, Wesley C ^b   Hol, Wim G J ^a  

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

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Conformational changes; Crystal structure; Drug design; Malaria; Plasmodium falciparum; Tryptophanyl tRNA synthetase

Indexed keywords

ADENOSINE PHOSPHATE; TRYPTOPHAN TRANSFER RNA LIGASE; TRYPTOPHANYL ADENYLATE; UNCLASSIFIED DRUG;

ARTICLE; CONFORMATIONAL TRANSITION; CRYPTOSPORIDIUM PARVUM; CRYSTAL STRUCTURE; CRYSTALLIZATION; DRUG DESIGN; NONHUMAN; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ADENOSINE MONOPHOSPHATE; AMINO ACID SEQUENCE; ANTIMALARIALS; CRYSTALLOGRAPHY, X-RAY; DRUG DESIGN; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PLASMODIUM FALCIPARUM; PROTEIN BINDING; PROTEIN CONFORMATION; SEQUENCE ALIGNMENT; TRYPTOPHAN; TRYPTOPHAN-TRNA LIGASE;

PLASMODIUM FALCIPARUM;

EID: 84878240065     PISSN: 01666851     EISSN: 18729428     Source Type: Journal    
DOI: 10.1016/j.molbiopara.2013.04.007     Document Type: Article

References (48)

1. C.J. Murray, L.C. Rosenfeld, S.S. Lim, K.G. Andrews, K.J. Foreman, and D. Haring Global malaria mortality between 1980 and 2010: a systematic analysis Lancet 379 2012 413 431
2. G. Vogel Global health. Disappointing results blunt hopes for malaria vaccine Science 338 2012 871 872
3. A.M. Dondorp, S. Yeung, L. White, C. Nguon, N.P. Day, and D. Socheat Artemisinin resistance: current status and scenarios for containment Nature Reviews. Microbiology 8 2010 272 280
4. M. Ibba, and D. Soll Aminoacyl-tRNA synthesis Annual Review of Biochemistry 69 2000 617 650
5. V.A. Ilyin, B. Temple, M. Hu, G. Li, Y. Yin, and P. Vachette 2.9 Å crystal structure of ligand-free tryptophanyl-tRNA synthetase: domain movements fragment the adenine nucleotide binding site Protein Science 9 2000 218 231
6. P. Retailleau, X. Huang, Y. Yin, M. Hu, V. Weinreb, and P. Vachette Interconversion of ATP binding and conformational free energies by tryptophanyl-tRNA synthetase: structures of ATP bound to open and closed, pre-transition-state conformations Journal of Molecular Biology 325 2003 39 63
7. 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 Proceedings of the National Academy of Sciences of the United States of America 106 2009 1790 1795
8. 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 Research 36 2008 1288 1299
9. 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 Research 34 2006 3246 3258
10. X.L. Yang, F.J. Otero, K.L. Ewalt, J. Liu, M.A. Swairjo, and C. Kohrer Two conformations of a crystalline human tRNA synthetase-tRNA complex: implications for protein synthesis EMBO Journal 25 2006 2919 2929
11. G.H. Vondenhoff, and A. Van Aerschot Aminoacyl-tRNA synthetase inhibitors as potential antibiotics European Journal of Medicinal Chemistry 46 2011 5227 5236
12. V. Hernandez, T. Crepin, A. Palencia, S. Cusack, T. Akama, and S.J. Baker Discovery of a novel class of boron-based antibacterials with activity against gram-negative bacteria Antimicrobial Agents and Chemotherapy 57 3 2013 1394 1403
13. S. Shibata, J.R. Gillespie, R.M. Ranade, C.Y. Koh, J.E. Kim, and J.U. Laydbak Urea-based inhibitors of Trypanosoma brucei methionyl-tRNA synthetase: selectivity and in vivo characterization Journal of Medicinal Chemistry 55 2012 6342 6351
14. C.Y. Koh, J.E. Kim, S. Shibata, R.M. Ranade, M. Yu, and J. Liu Distinct states of methionyl-tRNA synthetase indicate inhibitor binding by conformational selection Structure 20 2012 1681 1691
15. D. Hoepfner, C.W. McNamara, C.S. Lim, C. Studer, R. Riedl, and T. Aust Selective and specific inhibition of the Plasmodium falciparum lysyl-tRNA synthetase by the fungal secondary metabolite cladosporin Cell Host Microbe 11 2012 654 663
16. S. Shibata, J.R. Gillespie, A.M. Kelley, A.J. Napuli, Z. Zhang, and K.V. Kovzun Selective inhibitors of methionyl-tRNA synthetase have potent activity against Trypanosoma brucei infection in mice Antimicrobial Agents and Chemotherapy 55 2011 1982 1989
17. F.L. Rock, W. Mao, A. Yaremchuk, M. Tukalo, T. Crepin, and H. Zhou An antifungal agent inhibits an aminoacyl-tRNA synthetase by trapping tRNA in the editing site Science 316 2007 1759 1761
18. M. Teng, M. Hilgers, M. Cunningham, A. Borchardt, J. Locke, and S. Abraham Identification of bacteria selective threonyl tRNA synthetase (ThrRS) substrate inhibitors by structure-based design Journal of Medicinal Chemistry 2013 epub ahead of print
19. E.A. Merritt, T.L. Arakaki, E.T. Larson, A. Kelley, N. Mueller, and A.J. Napuli Crystal structure of the aspartyl-tRNA synthetase from Entamoeba histolytica Molecular and Biochemical Parasitology 169 2010 95 100
20. E.A. Merritt, T.L. Arakaki, J.R. Gillespie, E.T. Larson, A. Kelley, and N. Mueller Crystal structures of trypanosomal histidyl-tRNA synthetase illuminate differences between eukaryotic and prokaryotic homologs Journal of Molecular Biology 397 2010 481 494
21. T.L. Arakaki, M. Carter, A.J. Napuli, C.L. Verlinde, E. Fan, and F. Zucker The structure of tryptophanyl-tRNA synthetase from Giardia lamblia reveals divergence from eukaryotic homologs Journal of Structural Biology 171 2010 238 243
22. E.T. Larson, J.E. Kim, F.H. Zucker, A. Kelley, N. Mueller, and A.J. Napuli Structure of Leishmania major methionyl-tRNA synthetase in complex with intermediate products methionyladenylate and pyrophosphate Biochimie 93 2011 570 582
23. E.T. Larson, J.E. Kim, L.J. Castaneda, A.J. Napuli, Z. Zhang, and E. Fan The double-length tyrosyl-tRNA synthetase from the eukaryote Leishmania major forms an intrinsically asymmetric pseudo-dimer Journal of Molecular Biology 409 2011 159 176
24. E.T. Larson, J.E. Kim, A.J. Napuli, C.L. Verlinde, E. Fan, and F.H. Zucker Structure of the prolyl-tRNA synthetase from the eukaryotic pathogen Giardia lamblia Acta Crystallographica. Section D: Biological Crystallography 68 2012 1194 1200
25. E.A. Merritt, T.L. Arakaki, R. Gillespie, A.J. Napuli, J.E. Kim, and F.S. Buckner Crystal structures of three protozoan homologs of tryptophanyl-tRNA synthetase Molecular and Biochemical Parasitology 177 2011 20 28
26. K.E. Jackson, S. Habib, M. Frugier, R. Hoen, S. Khan, and J.S. Pham Protein translation in plasmodium parasites Trends in Parasitology 27 2011 467 476
27. C. Mehlin, E. Boni, F.S. Buckner, L. Engel, T. Feist, and M.H. Gelb Heterologous expression of proteins from Plasmodium falciparum: results from 1000 genes Molecular and Biochemical Parasitology 148 2006 144 160
28. Z. Otwinowski, and W. Minor Processing of X-ray diffraction data collected in oscillation mode C. Carter, R. Sweet, Macromolecular Crystallography, Part A 1997 Academic Press 307 326
29. A.J. McCoy, R.W. Grosse-Kunstleve, P.D. Adams, M.D. Winn, L.C. Storoni, and R.J. Read Phaser crystallographic software Journal of Applied Crystallography 40 2007 658 674
30. G. Langer, S.X. Cohen, V.S. Lamzin, and A. Perrakis Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7 Nature Protocols 3 2008 1171 1179
31. P. Emsley, and K. Cowtan Coot: model-building tools for molecular graphics Acta Crystallographica. Section D: Biological Crystallography 60 2004 2126 2132
32. G.N. Murshudov, A.A. Vagin, and E.J. Dodson Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallographica. Section D: Biological Crystallography 53 1997 240 255
33. J. Painter, and E.A. Merritt TLSMD web server for the generation of multi-group TLS models Journal of Applied Crystallography 39 2006 109 111
34. V.B. Chen, W.B. Arendall 3rd, J.J. Headd, D.A. Keedy, R.M. Immormino, and G.J. Kapral MolProbity: all-atom structure validation for macromolecular crystallography Acta Crystallographica. Section D: Biological Crystallography 66 2010 12 21
35. W. DeLano The PyMOL Molecular Graphics System 2002 http://www.pymol.org
36. W. Kabsch XDS Acta Crystallographica. Section D: Biological Crystallography 66 2010 125 132
37. Collaborative Computational Project Number 4. The CCP4 suite: programs for protein crystallography Acta Crystallographica. Section D: Biological Crystallography 50 1994 760 763
38. L. Holm, and P. Rosenstrom Dali server: conservation mapping in 3D Nucleic Acids Research 38 2010 W545 W549
39. J. Dundas, Z. Ouyang, J. Tseng, A. Binkowski, Y. Turpaz, and J. Liang CASTp: computed atlas of surface topography of proteins with structural and topographical mapping of functionally annotated residues Nucleic Acids Research 34 2006 W116 W118
40. X.L. Yang, F.J. Otero, R.J. Skene, D.E. McRee, P. Schimmel, and L. Ribas de Pouplana Crystal structures that suggest late development of genetic code components for differentiating aromatic side chains Proceedings of the National Academy of Sciences of the United States of America 100 2003 15376 15380
41. X.L. Yang, M. Guo, M. Kapoor, K.L. Ewalt, F.J. Otero, and R.J. Skene Functional and crystal structure analysis of active site adaptations of a potent anti-angiogenic human tRNA synthetase Structure 15 2007 793 805
42. Y. Yu, Y. Liu, N. Shen, X. Xu, F. Xu, and J. Jia Crystal structure of human tryptophanyl-tRNA synthetase catalytic fragment: insights into substrate recognition, tRNA binding, and angiogenesis activity The Journal of Biological Chemistry 279 2004 8378 8388
43. J.D. Bauman, D. Patel, C. Dharia, M. Fromer, S. Ahmed, and Y. Frenkel Detecting allosteric sites of HIV-1 reverse transcriptase by X-ray crystallographic fragment screening Journal of Medicinal Chemistry 56 7 2013 2738 2746
44. K. Das, P.J. Lewi, S.H. Hughes, and E. Arnold Crystallography and the design of anti-AIDS drugs: conformational flexibility and positional adaptability are important in the design of non-nucleoside HIV-1 reverse transcriptase inhibitors Progress in Biophysics and Molecular Biology 88 2005 209 231
45. C. Wiesmann, K.J. Barr, J. Kung, J. Zhu, D.A. Erlanson, and W. Shen Allosteric inhibition of protein tyrosine phosphatase 1B Nature Structural & Molecular Biology 11 2004 730 737
46. S.W. Wright, A.A. Carlo, M.D. Carty, D.E. Danley, D.L. Hageman, and G.A. Karam Anilinoquinazoline inhibitors of fructose 1,6-bisphosphatase bind at a novel allosteric site: synthesis, in vitro characterization, and X-ray crystallography Journal of Medicinal Chemistry 45 2002 3865 3877
47. P. Gouet, X. Robert, and E. Courcelle ESPript/ENDscript. Extracting and rendering sequence and 3D information from atomic structures of proteins Nucleic Acids Research 31 2003 3320 3323
48. E. Krissinel, and K. Henrick Inference of macromolecular assemblies from crystalline state Journal of Molecular Biology 372 2007 774 797