Supergenomic network compression and the discovery of exp1 as a glutathione transferase inhibited by artesunate

Cell

Volumn 158, Issue 4, 2014, Pages 916-928

  Lisewski, Andreas Martin ^a   Quiros, Joel P ^a   Ng, Caroline L ^b   Adikesavan, Anbu Karani ^a   Miura, Kazutoyo ^c   Putluri, Nagireddy ^a   Eastman, Richard T ^b,c   Scanfeld, Daniel ^b   Regenbogen, Sam J ^a   Altenhofen, Lindsey ^d,e   Llinás, Manuel ^d,e   Sreekumar, Arun ^a   Long, Carole ^c   Fidock, David A ^b   Lichtarge, Olivier ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b Department of Medicine   (United States)

^c NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^d PRINCETON UNIVERSITY   (United States)

^e PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTESUNATE; EXP1 PROTEIN; GLUTATHIONE TRANSFERASE; HEMATIN; MEMBRANE ANTIGEN; UNCLASSIFIED DRUG; DIHYDROARTEMISININ; ANTIMALARIAL AGENT; ARTEMISININ DERIVATIVE; HEMIN; PARASITE ANTIGEN; QF116 ANTIGEN, PLASMODIUM FALCIPARUM;

ARTICLE; CELL STRESS; COMPRESSION; CONTROLLED STUDY; DRUG METABOLISM; DRUG SENSITIVITY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME SUBSTRATE; ERYTHROCYTE; NONHUMAN; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN METABOLISM; PROTOZOAL GENETICS; ANIMAL CELL; CYTOTOXICITY; DRUG DEGRADATION; DRUG INHIBITION; DRUG POTENCY; GENE FUNCTION; GENE REGULATORY NETWORK; GENOME; IC50; IN VITRO STUDY; MOLECULAR BIOLOGY; OXIDATIVE STRESS; PREDICTION; BIOLOGICAL MODEL; CHEMISTRY; ENZYMOLOGY; GENETICS; GENOMICS; INFORMATION PROCESSING; ISOLATION AND PURIFICATION; METABOLISM; PROCEDURES;

ANTIGENS, PROTOZOAN; ANTIMALARIALS; ARTEMISININS; CATALYTIC DOMAIN; DATA COMPRESSION; GENOMICS; HEMIN; MODELS, GENETIC; PLASMODIUM FALCIPARUM;

EID: 84908399993     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2014.07.011     Document Type: Article

References (78)

1. N. Abu Bakar, N. Klonis, E. Hanssen, C. Chan, and L. Tilley Digestive-vacuole genesis and endocytic processes in the early intraerythrocytic stages of Plasmodium falciparum J. Cell Sci. 123 2010 441 450
2. S.F. Altschul, T.L. Madden, A.A. Schäffer, J. Zhang, Z. Zhang, W. Miller, and D.J. Lipman Gapped BLAST and PSI-BLAST: a new generation of protein database search programs Nucleic Acids Res. 25 1997 3389 3402
3. C. Andersson, F. Piemonte, E. Mosialou, R. Weinander, T.H. Sun, G. Lundqvist, A.E. Adang, and R. Morgenstern Kinetic studies on rat liver microsomal glutathione transferase: consequences of activation Biochim. Biophys. Acta 1247 1995 277 283
4. F. Ariey, B. Witkowski, C. Amaratunga, J. Beghain, A.C. Langlois, N. Khim, S. Kim, V. Duru, C. Bouchier, and L. Ma et al. A molecular marker of artemisinin-resistant Plasmodium falciparum malaria Nature 505 2014 50 55
5. H. Atamna, and H. Ginsburg Heme degradation in the presence of glutathione. A proposed mechanism to account for the high levels of non-heme iron found in the membranes of hemoglobinopathic red blood cells J. Biol. Chem. 270 1995 24876 24883
6. C. Aurrecoechea, J. Brestelli, B.P. Brunk, J. Dommer, S. Fischer, B. Gajria, X. Gao, A. Gingle, G. Grant, and O.S. Harb et al. PlasmoDB: a functional genomic database for malaria parasites Nucleic Acids Res. 37 Database issue 2009 D539 D543
7. A.L. Barabasi, and R. Albert Emergence of scaling in random networks Science 286 1999 509 512
8. K. Becker, L. Tilley, J.L. Vennerstrom, D. Roberts, S. Rogerson, and H. Ginsburg Oxidative stress in malaria parasite-infected erythrocytes: host-parasite interactions Int. J. Parasitol. 34 2004 163 189
9. Z. Bozdech, M. Llinás, B.L. Pulliam, E.D. Wong, J. Zhu, and J.L. DeRisi The transcriptome of the intraerythrocytic developmental cycle of Plasmodium falciparum PLoS Biol. 1 2003 E5
10. D. Cardi, A. Pozza, B. Arnou, E. Marchal, J.D. Clausen, J.P. Andersen, S. Krishna, J.V. Møller, M. le Maire, and C. Jaxel Purified E255L mutant SERCA1a and purified PfATP6 are sensitive to SERCA-type inhibitors but insensitive to artemisinins J. Biol. Chem. 285 2010 26406 26416
11. P. Caspers, H. Etlinger, H. Matile, J.R. Pink, D. Stüber, and B. Takács A Plasmodium falciparum malaria vaccine candidate which contains epitopes from the circumsporozoite protein and a blood stage antigen, 5.1 Mol. Biochem. Parasitol. 47 1991 143 150
12. I.H. Cheeseman, B.A. Miller, S. Nair, S. Nkhoma, A. Tan, J.C. Tan, S. Al Saai, A.P. Phyo, C.L. Moo, and K.M. Lwin et al. A major genome region underlying artemisinin resistance in malaria Science 336 2012 79 82
13. H.N. Chua, W.K. Sung, and L. Wong Exploiting indirect neighbours and topological weight to predict protein function from protein-protein interactions Bioinformatics 22 2006 1623 1630
14. M. Chugh, V. Sundararaman, S. Kumar, V.S. Reddy, W.A. Siddiqui, K.D. Stuart, and P. Malhotra Protein complex directs hemoglobin-to-hemozoin formation in Plasmodium falciparum Proc. Natl. Acad. Sci. USA 110 2013 5392 5397
15. M. Deponte, and K. Becker Glutathione S-transferase from malarial parasites: structural and functional aspects Methods Enzymol. 401 2005 241 253
16. D. Eppstein, M. Loffler, and D. Strash Listing all maximal cliques in sparse graphs in near-optimal time Proceedings of the 21st International Symposium on Algorithms and Computation (ISAAC 2010) 6506 2010 403 413
17. S. Erdin, A.M. Lisewski, and O. Lichtarge Protein function prediction: towards integration of similarity metrics Curr. Opin. Struct. Biol. 21 2011 180 188
18. O. Famin, M. Krugliak, and H. Ginsburg Kinetics of inhibition of glutathione-mediated degradation of ferriprotoporphyrin IX by antimalarial drugs Biochem. Pharmacol. 58 1999 59 68
19. M. Fry, and M. Pudney Site of action of the antimalarial hydroxynaphthoquinone, 2-[trans-4-(4′-chlorophenyl) cyclohexyl]-3-hydroxy- 1,4-naphthoquinone (566C80) Biochem. Pharmacol. 43 1992 1545 1553
20. M.J. Gardner, N. Hall, E. Fung, O. White, M. Berriman, R.W. Hyman, J.M. Carlton, A. Pain, K.E. Nelson, and S. Bowman et al. Genome sequence of the human malaria parasite Plasmodium falciparum Nature 419 2002 498 511
21. H. Ginsburg, O. Famin, J. Zhang, and M. Krugliak Inhibition of glutathione-dependent degradation of heme by chloroquine and amodiaquine as a possible basis for their antimalarial mode of action Biochem. Pharmacol. 56 1998 1305 1313
22. M. Gribskov, and N.L. Robinson Use of receiver operating characteristic (ROC) analysis to evaluate sequence matching Comput. Chem. 20 1996 25 33
23. C. Grüring, A. Heiber, F. Kruse, J. Ungefehr, T.W. Gilberger, and T. Spielmann Development and host cell modifications of Plasmodium falciparum blood stages in four dimensions Nat Commun 2 2011 165
24. M. Habig, A. Blechschmidt, S. Dressler, B. Hess, V. Patel, A. Billich, C. Ostermeier, D. Beer, and M. Klumpp Efficient elimination of nonstoichiometric enzyme inhibitors from HTS hit lists J. Biomol. Screen. 14 2009 679 689
25. N. Hiller, K. Fritz-Wolf, M. Deponte, W. Wende, H. Zimmermann, and K. Becker Plasmodium falciparum glutathione S-transferase - structural and mechanistic studies on ligand binding and enzyme inhibition Protein Sci. 15 2006 281 289
26. P.J. Holm, P. Bhakat, C. Jegerschöld, N. Gyobu, K. Mitsuoka, Y. Fujiyoshi, R. Morgenstern, and H. Hebert Structural basis for detoxification and oxidative stress protection in membranes J. Mol. Biol. 360 2006 934 945
27. I.A. Hope, R. Hall, D.L. Simmons, J.E. Hyde, and J.G. Scaife Evidence for immunological cross-reaction between sporozoites and blood stages of a human malaria parasite Nature 308 1984 191 194
28. I.A. Hope, M. Mackay, J.E. Hyde, M. Goman, and J. Scaife The gene for an exported antigen of the malaria parasite Plasmodium falciparum cloned and expressed in Escherichia coli Nucleic Acids Res. 13 1985 369 379
29. T. Ideker, and R. Sharan Protein networks in disease Genome Res. 18 2008 644 652
30. P.J. Jakobsson, R. Morgenstern, J. Mancini, A. Ford-Hutchinson, and B. Persson Common structural features of MAPEG - a widespread superfamily of membrane associated proteins with highly divergent functions in eicosanoid and glutathione metabolism Protein Sci. 8 1999 689 692
31. N. Klonis, M.P. Crespo-Ortiz, I. Bottova, N. Abu-Bakar, S. Kenny, P.J. Rosenthal, and L. Tilley Artemisinin activity against Plasmodium falciparum requires hemoglobin uptake and digestion Proc. Natl. Acad. Sci. USA 108 2011 11405 11410
32. N. Klonis, D.J. Creek, and L. Tilley Iron and heme metabolism in Plasmodium falciparum and the mechanism of action of artemisinins Curr. Opin. Microbiol. 16 2013 722 727
33. N. Klonis, S.C. Xie, J.M. McCaw, M.P. Crespo-Ortiz, S.G. Zaloumis, J.A. Simpson, and L. Tilley Altered temporal response of malaria parasites determines differential sensitivity to artemisinin Proc. Natl. Acad. Sci. USA 110 2013 5157 5162
34. B.K. Lam, J.F. Penrose, K. Xu, M.H. Baldasaro, and K.F. Austen Site-directed mutagenesis of human leukotriene C4 synthase J. Biol. Chem. 272 1997 13923 13928
35. K.G. Le Roch, J.R. Johnson, L. Florens, Y. Zhou, A. Santrosyan, M. Grainger, S.F. Yan, K.C. Williamson, A.A. Holder, and D.J. Carucci et al. Global analysis of transcript and protein levels across the Plasmodium falciparum life cycle Genome Res. 14 2004 2308 2318
36. A.G. Maier, M. Rug, M.T. O'Neill, M. Brown, S. Chakravorty, T. Szestak, J. Chesson, Y. Wu, K. Hughes, and R.L. Coppel et al. Exported proteins required for virulence and rigidity of Plasmodium falciparum-infected human erythrocytes Cell 134 2008 48 61
37. I. Melvin, J. Weston, C. Leslie, and W.S. Noble RANKPROP: a web server for protein remote homology detection Bioinformatics 25 2009 121 122
38. V. Meraldi, I. Nebié, A.B. Tiono, D. Diallo, E. Sanogo, M. Theisen, P. Druilhe, G. Corradin, R. Moret, and B.S. Sirima Natural antibody response to Plasmodium falciparum Exp-1, MSP-3 and GLURP long synthetic peptides and association with protection Parasite Immunol. 26 2004 265 272
39. I. Mihalek, I. Res, and O. Lichtarge A family of evolution-entropy hybrid methods for ranking protein residues by importance J. Mol. Biol. 336 2004 1265 1282
40. R. Morgenstern, J. Zhang, and K. Johansson Microsomal glutathione transferase 1: mechanism and functional roles Drug Metab. Rev. 43 2011 300 306
41. S. Mukanganyama, Y.S. Naik, M. Widersten, B. Mannervik, and J.A. Hasler Proposed reductive metabolism of artemisinin by glutathione transferases in vitro Free Radic. Res. 35 2001 427 434
42. M.E.J. Newman Power laws, Pareto distributions and Zipf's law Contemp. Phys. 46 2005 323 351
43. P.M. O'Neill, V.E. Barton, and S.A. Ward The molecular mechanism of action of artemisinin - the debate continues Molecules 15 2010 1705 1721
44. A. Ochoa, M. Llinás, and M. Singh Using context to improve protein domain identification BMC Bioinformatics 12 2011 90
45. K. Oexle Data compressibility, physical entropy, and evolutionary a priori relation between observer and object Phys. Rev. E 51 1995 2651 2653
46. D.J. Park, A.K. Lukens, D.E. Neafsey, S.F. Schaffner, H.H. Chang, C. Valim, U. Ribacke, D. Van Tyne, K. Galinsky, and M. Galligan et al. Sequence-based association and selection scans identify drug resistance loci in the Plasmodium falciparum malaria parasite Proc. Natl. Acad. Sci. USA 109 2012 13052 13057
47. P. Radivojac, W.T. Clark, T.R. Oron, A.M. Schnoes, T. Wittkop, A. Sokolov, K. Graim, C. Funk, K. Verspoor, and A. Ben-Hur et al. A large-scale evaluation of computational protein function prediction Nat. Methods 10 2013 221 227
48. R. Sharan, I. Ulitsky, and R. Shamir Network-based prediction of protein function Mol. Syst. Biol. 3 2007 88
49. D. Simmons, G. Woollett, M. Bergin-Cartwright, D. Kay, and J. Scaife A malaria protein exported into a new compartment within the host erythrocyte EMBO J. 6 1987 485 491
50. V.A. Simossis, J. Kleinjung, and J. Heringa Homology-extended sequence alignment Nucleic Acids Res. 33 2005 816 824
51. T. Spielmann, D.L. Gardiner, H.P. Beck, K.R. Trenholme, and D.J. Kemp Organization of ETRAMPs and EXP-1 at the parasite-host cell interface of malaria parasites Mol. Microbiol. 59 2006 779 794
52. S. Takala-Harrison, T.G. Clark, C.G. Jacob, M.P. Cummings, O. Miotto, A.M. Dondorp, M.M. Fukuda, F. Nosten, H. Noedl, and M. Imwong et al. Genetic loci associated with delayed clearance of Plasmodium falciparum following artemisinin treatment in Southeast Asia Proc. Natl. Acad. Sci. USA 110 2013 240 245
53. R.L. Tatusov, E.V. Koonin, and D.J. Lipman A genomic perspective on protein families Science 278 1997 631 637
54. F. Teuscher, N. Chen, D.E. Kyle, M.L. Gatton, and Q. Cheng Phenotypic changes in artemisinin-resistant Plasmodium falciparum lines in vitro: evidence for decreased sensitivity to dormancy and growth inhibition Antimicrob. Agents Chemother. 56 2012 428 431
55. UniProt Consortium The Universal Protein Resource (UniProt) in 2010 Nucleic Acids Res. 38 Database issue 2010 D142 D148
56. A. Vazquez, A. Flammini, A. Maritan, and A. Vespignani Global protein function prediction from protein-protein interaction networks Nat. Biotechnol. 21 2003 697 700
57. E. Venner, A.M. Lisewski, S. Erdin, R.M. Ward, S.R. Amin, and O. Lichtarge Accurate protein structure annotation through competitive diffusion of enzymatic functions over a network of local evolutionary similarities PLoS ONE 5 2010 e14286
58. C. von Mering, L.J. Jensen, M. Kuhn, S. Chaffron, T. Doerks, B. Krüger, B. Snel, and P. Bork STRING 7 - recent developments in the integration and prediction of protein interactions Nucleic Acids Res. 35 Database issue 2007 D358 D362
59. B. Wang, X.-h. Yang, and W.-l. Wang A novel scale-free network model based on clique growth J Cent South Univ Technol 16 2009 474 477
60. B. Witkowski, J. Lelièvre, M.J. Barragán, V. Laurent, X.Z. Su, A. Berry, and F. Benoit-Vical Increased tolerance to artemisinin in Plasmodium falciparum is mediated by a quiescence mechanism Antimicrob. Agents Chemother. 54 2010 1872 1877
61. B. Witkowski, J. Lelièvre, M.L. Nicolau-Travers, X. Iriart, P. Njomnang Soh, F. Bousejra-Elgarah, B. Meunier, A. Berry, and F. Benoit-Vical Evidence for the contribution of the hemozoin synthesis pathway of the murine Plasmodium yoelii to the resistance to artemisinin-related drugs PLoS ONE 7 2012 e32620
62. World Health Organization (WHO) Section 8.4.1. In Guidelines for the Treatment of Malaria, 2nd edition - Rev. 1 2011 World Health Organization
63. G.U. Yule A mathematical theory of evolution based on the conclusions of Dr. J. C. Willis Philos. Trans. R. Soc. Lond. B 213 1925 21 87
64. J. Aach, and G.M. Church Aligning gene expression time series with time warping algorithms Bioinformatics 17 2001 495 508
65. C. Falls, B. Powell, and J. Snoeyink Computing high-stringency COGs using Turan-type graphs CiteSeerX 2004 http://citeseerx.ist.psu.edu/viewdoc/summary? doi=10.1.1.107.8589
66. D.A. Fidock, T. Nomura, and T.E. Wellems Cycloguanil and its parent compound proguanil demonstrate distinct activities against Plasmodium falciparum malaria parasites transformed with human dihydrofolate reductase Mol. Pharmacol. 54 1998 1140 1147
67. D.A. Fidock, T. Nomura, A.K. Talley, R.A. Cooper, S.M. Dzekunov, M.T. Ferdig, L.M. Ursos, A.B. Sidhu, B. Naudé, and K.W. Deitsch et al. Mutations in the P. falciparum digestive vacuole transmembrane protein PfCRT and evidence for their role in chloroquine resistance Mol. Cell 6 2000 861 871
68. L.J. Jensen, P. Julien, M. Kuhn, C. von Mering, J. Muller, T. Doerks, and P. Bork eggNOG: automated construction and annotation of orthologous groups of genes Nucleic Acids Res. 36 Database issue 2008 D250 D254
69. S. Koncarevic, R. Bogumil, and K. Becker SELDI-TOF-MS analysis of chloroquine resistant and sensitive Plasmodium falciparum strains Proteomics 7 2007 711 721
70. S. Kyes, R. Pinches, and C. Newbold A simple RNA analysis method shows var and rif multigene family expression patterns in Plasmodium falciparum Mol. Biochem. Parasitol. 105 2000 311 315
71. A.M. Lisewski, and O. Lichtarge Untangling complex networks: risk minimization in financial markets through accessible spin glass ground states Physica A 389 2010 3250 3253
72. M. Llinás, Z. Bozdech, E.D. Wong, A.T. Adai, and J.L. DeRisi Comparative whole genome transcriptome analysis of three Plasmodium falciparum strains Nucleic Acids Res. 34 2006 1166 1173
73. J.S. McBride, D. Walliker, and G. Morgan Antigenic diversity in the human malaria parasite Plasmodium falciparum Science 217 1982 254 257
74. S. Mohseni-Zadeh, P. Brézellec, and J. Risler Cluster-C, an algorithm for the large-scale clustering of protein sequences based on the extraction of maximal cliques Comput. Biol. Chem. 28 2004 211 218
75. M.G. Montague, and C.A. Hutchison III Gene content phylogeny of herpesviruses Proc. Natl. Acad. Sci. USA 97 2000 5334 5339
76. S. Mostafavi, D. Ray, D. Warde-Farley, C. Grouios, and Q. Morris GeneMANIA: a real-time multiple association network integration algorithm for predicting gene function Genome Biol. 9 Suppl 1 2008 S4
77. H.J. Painter, L.M. Altenhofen, B.F.C. Kafsack, and M. Llinás Whole-genome analysis of Plasmodium spp. utilizing a new Agilent Technologies DNA microarray platform Malaria: Methods and Protocols 2nd edition 2013 Humana Press New York
78. K. Tsuda, H. Shin, and B. Schölkopf Fast protein classification with multiple networks Bioinformatics 21 Suppl 2 2005 ii59 ii65