Structure of prolyl-tRNA synthetase-halofuginone complex provides basis for development of drugs against malaria and toxoplasmosis

Structure

Volumn 23, Issue 5, 2015, Pages 819-829

  Jain, Vitul ^a   Yogavel, Manickam ^a   Oshima, Yoshiteru ^b   Kikuchi, Haruhisa ^b   Touquet, Bastien ^c,d   Hakimi, Mohamed Ali ^c,d   Sharma, Amit ^a  

^a INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

^b TOHOKU UNIVERSITY   (Japan)

^c CNRS   (France)

^d UNIV GRENOBLE ALPES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID TRANSFER RNA LIGASE; ANTIMALARIAL AGENT; HALOFUGINONE; MULTIPROTEIN COMPLEX; PIPERIDINE DERIVATIVE; PROLYL T RNA SYNTHETASE; PROTOZOAL PROTEIN; QUINAZOLINONE DERIVATIVE;

CHEMICAL STRUCTURE; CHEMISTRY; CRYSTALLOGRAPHY; DRUG EFFECTS; ENZYME ACTIVE SITE; ENZYMOLOGY; HUMAN; METABOLISM; PLASMODIUM FALCIPARUM; STRUCTURE ACTIVITY RELATION; TOXOPLASMA;

AMINO ACYL-TRNA SYNTHETASES; ANTIMALARIALS; CATALYTIC DOMAIN; CRYSTALLOGRAPHY; HUMANS; MODELS, MOLECULAR; MULTIPROTEIN COMPLEXES; PIPERIDINES; PLASMODIUM FALCIPARUM; PROTOZOAN PROTEINS; QUINAZOLINONES; STRUCTURE-ACTIVITY RELATIONSHIP; TOXOPLASMA;

EID: 84930190688     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2015.02.011     Document Type: Article

References (53)

1. P.D. Adams, P.V. Afonine, G. Bunkoczi, V.B. Chen, I.W. Davis, N. Echols, J.J. Headd, L.W. Hung, G.J. Kapral, and R.W. Grosse-Kunstleve PHENIX: a comprehensive Python-based system for macromolecular structure solution Acta Crystallogr. D Biol. Crystallogr. 66 2010 213 221
2. A.A. Baykov, O.A. Evtushenko, and S.M. Avaeva A malachite green procedure for orthophosphate determination and its use in alkaline phosphatase-based enzyme immunoassay Anal. Biochem. 171 1988 266 270
3. T.K. Bhatt, C. Kapil, S. Khan, M.A. Jairajpuri, V. Sharma, D. Santoni, F. Silvestrini, E. Pizzi, and A. Sharma A genomic glimpse of aminoacyl-tRNA synthetases in malaria parasite Plasmodium falciparum BMC Genomics 10 2009 644
4. T.K. Bhatt, S. Khan, V.P. Dwivedi, M.M. Banday, A. Sharma, A. Chandele, N. Camacho, L. Ribas de Pouplana, Y. Wu, and A.G. Craig Malaria parasite tyrosyl-tRNA synthetase secretion triggers pro-inflammatory responses Nat. Commun. 2 2011 530
5. I. Cestari, and K. Stuart A spectrophotometric assay for quantitative measurement of aminoacyl-tRNA synthetase activity J. Biomol. Screen. 18 2013 490 497
6. B.R. Chandra, A. Olivieri, F. Silvestrini, P. Alano, and A. Sharma Biochemical characterization of the two nucleosome assembly proteins from Plasmodium falciparum Mol. Biochem. Parasitol. 142 2005 237 247
7. 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
8. G.R. Coatney, W.C. Cooper, W.B. Culwell, W.C. White, and C.A. Imboden Jr. Studies in human malaria. XXV. Trial of febrifugine, an alkaloid obtained from Dichroa febrifuga Lour., against the Chesson strain of Plasmodium vivax J. Natl. Malar. Soc. 9 1950 183 186
9. E.R. Derbyshire, R. Mazitschek, and J. Clardy Characterization of Plasmodium liver stage inhibition by halofuginone ChemMedChem 7 2012 844 849
10. M. Elkin, I. Ariel, H.Q. Miao, A. Nagler, M. Pines, N. de-Groot, A. Hochberg, and I. Vlodavsky Inhibition of bladder carcinoma angiogenesis, stromal support, and tumor growth by halofuginone Cancer Res. 59 1999 4111 4118
11. P. Emsley, and K. Cowtan Coot: model-building tools for molecular graphics Acta Crystallogr. D Biol. Crystallogr. 60 2004 2126 2132
12. T.G. Geary, A.A. Divo, and J.B. Jensen An in vitro assay system for the identification of potential antimalarial drugs J. Parasitol. 69 1983 577 583
13. J. Gill, M. Yogavel, A. Kumar, H. Belrhali, S.K. Jain, M. Rug, M. Brown, A.G. Maier, and A. Sharma Crystal structure of malaria parasite nucleosome assembly protein: distinct modes of protein localization and histone recognition J. Biol. Chem. 284 2009 10076 10087
14. O. Halevy, A. Nagler, F. Levi-Schaffer, O. Genina, and M. Pines Inhibition of collagen type I synthesis by skin fibroblasts of graft versus host disease and scleroderma patients: effect of halofuginone Biochemical Pharmacol. 52 1996 1057 1063
15. R.I. Hewitt, W.S. Wallace, E.R. Gill, and J.H. Williams An antimalarial alkaloid from Hydrangea. XIII. The effects of various synthetic quinazolones against Plasmodium lophurae in ducks Am. J. Trop. Med. Hyg. 1 1952 768 772
16. R. Hoen, E.M. Novoa, A. Lopez, N. Camacho, L. Cubells, P. Vieira, M. Santos, P. Marin-Garcia, J.M. Bautista, and A. Cortes Selective inhibition of an apicoplastic aminoacyl-tRNA synthetase from Plasmodium falciparum ChemBioChem 14 2013 499 509
17. D. Hoepfner, C.W. McNamara, C.S. Lim, C. Studer, R. Riedl, T. Aust, S.L. McCormack, D.M. Plouffe, S. Meister, and S. Schuierer Selective and specific inhibition of the Plasmodium falciparum lysyl-tRNA synthetase by the fungal secondary metabolite cladosporin Cell Host Microbe 11 2012 654 663
18. M. Ibba, and D. Soll Aminoacyl-tRNA synthesis Annu. Rev. Biochem. 69 2000 617 650
19. E.S. Istvan, N.V. Dharia, S.E. Bopp, I. Gluzman, E.A. Winzeler, and D.E. Goldberg Validation of isoleucine utilization targets in Plasmodium falciparum Proc. Natl. Acad. Sci. USA 108 2011 1627 1632
20. K.E. Jackson, S. Habib, M. Frugier, R. Hoen, S. Khan, J.S. Pham, L. Ribas de Pouplana, M. Royo, M.A. Santos, and A. Sharma Protein translation in Plasmodium parasites Trends Parasitol. 27 2011 467 476
21. V. Jain, H. Kikuchi, Y. Oshima, A. Sharma, and M. Yogavel Structural and functional analysis of the anti-malarial drug target prolyl-tRNA synthetase J. Struct. Funct. Genomics 15 2014 181 190
22. T.L. Keller, D. Zocco, M.S. Sundrud, M. Hendrick, M. Edenius, J. Yum, Y.J. Kim, H.K. Lee, J.F. Cortese, and D.F. Wirth Halofuginone and other febrifugine derivatives inhibit prolyl-tRNA synthetase Nat. Chem. Biol. 8 2012 311 317
23. S. Khan, A. Sharma, A. Jamwal, V. Sharma, A.K. Pole, K.K. Thakur, and A. Sharma Uneven spread of cis- and trans-editing aminoacyl-tRNA synthetase domains within translational compartments of P. falciparum Sci. Rep. 1 2011 188
24. S. Khan, A. Garg, N. Camacho, J. Van Rooyen, A. Kumar Pole, H. Belrhali, L. Ribas de Pouplana, V. Sharma, and A. Sharma Structural analysis of malaria-parasite lysyl-tRNA synthetase provides a platform for drug development Acta Crystallogr. D Biol. Crystallogr. 69 2013 785 795
25. S. Khan, A. Garg, A. Sharma, N. Camacho, D. Picchioni, A. Saint-Leger, L. Ribas de Pouplana, M. Yogavel, and A. Sharma An appended domain results in an unusual architecture for malaria parasite tryptophanyl-tRNA synthetase PLoS One 8 2013 e66224
26. S. Khan, A. Sharma, H. Belrhali, M. Yogavel, and A. Sharma Structural basis of malaria parasite lysyl-tRNA synthetase inhibition by cladosporin J. Struct. Funct. Genomics 15 2014 63 71
27. H. Kikuchi, K. Yamamoto, S. Horoiwa, S. Hirai, R. Kasahara, N. Hariguchi, M. Matsumoto, and Y. Oshima Exploration of a new type of antimalarial compounds based on febrifugine J. Med. Chem. 49 2006 4698 4706
28. H. Kikuchi, S. Horoiwa, R. Kasahara, N. Hariguchi, M. Matsumoto, and Y. Oshima Synthesis of febrifugine derivatives and development of an effective and safe tetrahydroquinazoline-type antimalarial Eur. J. Med. Chem. 76 2014 10 19
29. J.B. Koepfli, J.F. Mead, and J.A. Brockman Jr. An alkaloid with high antimalarial activity from Dichroa febrifuga J. Am. Chem. Soc. 69 1947 1837
30. C.Y. Koh, J.E. Kim, S. Shibata, R.M. Ranade, M. Yu, J. Liu, J.R. Gillespie, F.S. Buckner, C.L. Verlinde, and E. Fan Distinct states of methionyl-tRNA synthetase indicate inhibitor binding by conformational selection Structure 20 2012 1681 1691
31. E. Krissinel, and K. Henrick Inference of macromolecular assemblies from crystalline state J. Mol. Biol. 372 2007 774 797
32. M.R. Linder, A.R. Heckeroth, M. Najdrowski, A. Daugschies, D. Schollmeyer, and C. Miculka (2R,3S)-(+)- and (2S,3R)-(-)-halofuginone lactate: synthesis, absolute configuration, and activity against Cryptosporidium parvum Bioorg. Med. Chem. Lett. 17 2007 4140 4143
33. S. Loewe The problem of synergism and antagonism of combined drugs Arzneimittelforschung 3 1953 285 290
34. D. Matulis, J.K. Kranz, F.R. Salemme, and M.J. Todd Thermodynamic stability of carbonic anhydrase: measurements of binding affinity and stoichiometry using ThermoFluor Biochemistry 44 2005 5258 5266
35. 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
36. T. McGaha, T. Kodera, R. Phelps, H. Spiera, M. Pines, and C. Bona Effect of halofuginone on the development of tight skin (TSK) syndrome Autoimmunity 35 2002 277 282
37. G.N. Murshudov, P. Skubak, A.A. Lebedev, N.S. Pannu, R.A. Steiner, R.A. Nicholls, M.D. Winn, F. Long, and A.A. Vagin REFMAC5 for the refinement of macromolecular crystal structures Acta Crystallogr. D Biol. Crystallogr. 67 2011 355 367
38. V.M. Navadgi, B.R. Chandra, P.C. Mishra, and A. Sharma The two Plasmodium falciparum nucleosome assembly proteins play distinct roles in histone transport and chromatin assembly J. Biol. Chem. 281 2006 16978 16984
39. E.F. Pettersen, T.D. Goddard, C.C. Huang, G.S. Couch, D.M. Greenblatt, E.C. Meng, and T.E. Ferrin UCSF Chimera - a visualization system for exploratory research and analysis J. Comput. Chem. 25 2004 1605 1612
40. 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
41. M. Pines, and A. Nagler Halofuginone: a novel antifibrotic therapy Gen. Pharmacol. 30 1998 445 450
42. M. Pines, D. Snyder, S. Yarkoni, and A. Nagler Halofuginone to treat fibrosis in chronic graft-versus-host disease and scleroderma Biol. Blood Marrow Transplant. 9 2003 417 425
43. J.F. Ryley, and M.J. Betts Chemotherapy of chicken coccidiosis Adv. Pharmacol. Chemother. 11 1973 221 293
44. J.F. Ryley, and R.G. Wilson Laboratory studies with some recent anticoccidials Parasitology 70 1975 203 222
45. A. Sharma, and A. Sharma Fatty acid induced remodeling within the human liver fatty acid-binding protein J. Biol. Chem. 286 2011 31924 31928
46. A. Sharma, M. Yogavel, R.R. Akhouri, J. Gill, and A. Sharma Crystal structure of soluble domain of malaria sporozoite protein UIS3 in complex with lipid J. Biol. Chem. 283 2008 24077 24088
47. M. Smilkstein, N. Sriwilaijaroen, J.X. Kelly, P. Wilairat, and M. Riscoe Simple and inexpensive fluorescence-based technique for high-throughput antimalarial drug screening Antimicrob. Agents Chemother. 48 2004 1803 1806
48. J. Son, E.H. Lee, M. Park, J.H. Kim, J. Kim, S. Kim, Y.H. Jeon, and K.Y. Hwang Conformational changes in human prolyl-tRNA synthetase upon binding of the substrates proline and ATP and the inhibitor halofuginone Acta Crystallogr. D Biol. Crystallogr. 69 2013 2136 2145
49. G.G. Steel, and M.J. Peckham Exploitable mechanisms in combined radiotherapy-chemotherapy: the concept of additivity Int. J. Radiat. Oncol. Biol. Phys. 5 1979 85 91
50. C.J. Tonkin, G.G. van Dooren, T.P. Spurck, N.S. Struck, R.T. Good, E. Handman, A.F. Cowman, and G.I. McFadden Localization of organellar proteins in Plasmodium falciparum using a novel set of transfection vectors and a new immunofluorescence fixation method Mol. Biochem. Parasitol. 137 2004 13 21
51. W. Trager, and J.B. Jensen Human malaria parasites in continuous culture J. Parasitol. 91 2005 484 486
52. 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, and A. McCoy Overview of the CCP4 suite and current developments Acta Crystallogr. D Biol. Crystallogr. 67 2011 235 242
53. H. Zhou, L. Sun, X.L. Yang, and P. Schimmel ATP-directed capture of bioactive herbal-based medicine on human tRNA synthetase Nature 494 2013 121 124