Ubiquitin activation is essential for schizont maturation in Plasmodium falciparum blood-stage development
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Judith L. Green aff001; Yang Wu aff001; Vesela Encheva aff002; Edwin Lasonder aff003; Adchara Prommaban aff001; Simone Kunzelmann aff005; Evangelos Christodoulou aff005; Munira Grainger aff001; Ngoc Truongvan aff006; Sebastian Bothe aff007; Vikram Sharma aff003; Wei Song aff008; Irene Pinzuti aff008; Chairat Uthaipibull aff009; Somdet Srichairatanakool aff004; Veronique Birault aff010; Gordon Langsley aff011; Hermann Schindelin aff006; Benjamin Stieglitz aff008; Ambrosius P. Snijders aff002; Anthony A. Holder aff001
Působiště autorů:
Malaria Parasitology Laboratory, The Francis Crick Institute, London, United Kingdom
aff001; Mass Spectrometry Proteomics, The Francis Crick Institute, London, United Kingdom
aff002; School of Biomedical Science, University of Plymouth, Plymouth, United Kingdom
aff003; Department of Biochemistry, Chiang Mai University, Chiang Mai, Thailand
aff004; Structural Biology Science Technology Platform, The Francis Crick Institute, London, United Kingdom
aff005; Rudolf Virchow Center for Experimental Biomedicine, Universität Würzburg, Würzburg, Germany
aff006; Department of Chemistry and Pharmacy, University of Würzburg, Würzburg, Germany
aff007; School of Biological and Chemical Sciences, Queen Mary University of London, London, United Kingdom
aff008; National Center for Genetic Engineering and Biotechnology, Khlong Luang, Thailand
aff009; Translation, The Francis Crick Institute, London, United Kingdom
aff010; Laboratoire de Biologie Cellulaire Comparative des Apicomplexes, Institut Cochin, Université Paris Descartes, Paris, France
aff011
Vyšlo v časopise:
Ubiquitin activation is essential for schizont maturation in Plasmodium falciparum blood-stage development. PLoS Pathog 16(6): e32767. doi:10.1371/journal.ppat.1008640
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.ppat.1008640
Souhrn
Ubiquitylation is a common post translational modification of eukaryotic proteins and in the human malaria parasite, Plasmodium falciparum (Pf) overall ubiquitylation increases in the transition from intracellular schizont to extracellular merozoite stages in the asexual blood stage cycle. Here, we identify specific ubiquitylation sites of protein substrates in three intraerythrocytic parasite stages and extracellular merozoites; a total of 1464 sites in 546 proteins were identified (data available via ProteomeXchange with identifier PXD014998). 469 ubiquitylated proteins were identified in merozoites compared with only 160 in the preceding intracellular schizont stage, suggesting a large increase in protein ubiquitylation associated with merozoite maturation. Following merozoite invasion of erythrocytes, few ubiquitylated proteins were detected in the first intracellular ring stage but as parasites matured through trophozoite to schizont stages the apparent extent of ubiquitylation increased. We identified commonly used ubiquitylation motifs and groups of ubiquitylated proteins in specific areas of cellular function, for example merozoite pellicle proteins involved in erythrocyte invasion, exported proteins, and histones. To investigate the importance of ubiquitylation we screened ubiquitin pathway inhibitors in a parasite growth assay and identified the ubiquitin activating enzyme (UBA1 or E1) inhibitor MLN7243 (TAK-243) to be particularly effective. This small molecule was shown to be a potent inhibitor of recombinant PfUBA1, and a structural homology model of MLN7243 bound to the parasite enzyme highlights avenues for the development of P. falciparum specific inhibitors. We created a genetically modified parasite with a rapamycin-inducible functional deletion of uba1; addition of either MLN7243 or rapamycin to the recombinant parasite line resulted in the same phenotype, with parasite development blocked at the schizont stage. Nuclear division and formation of intracellular structures was interrupted. These results indicate that the intracellular target of MLN7243 is UBA1, and this activity is essential for the final differentiation of schizonts to merozoites.
Klíčová slova:
Malaria – Malarial parasites – Merozoites – Parasitic diseases – Parasitic life cycles – Plasmodium – Red blood cells – Sequence motif analysis
Zdroje
1. Lasonder E, Green JL, Camarda G, Talabani H, Holder AA, Langsley G, et al. The Plasmodium falciparum schizont phosphoproteome reveals extensive phosphatidylinositol and cAMP-protein kinase A signaling. J Proteome Res. 2012;11(11):5323–37. Epub 2012/10/03. doi: 10.1021/pr300557m 23025827.
2. Lasonder E, Green JL, Grainger M, Langsley G, Holder AA. Extensive differential protein phosphorylation as intraerythrocytic Plasmodium falciparum schizonts develop into extracellular invasive merozoites. Proteomics. 2015;15(15):2716–29. Epub 2015/04/18. doi: 10.1002/pmic.201400508 25886026.
3. Xie X, Kang H, Liu W, Wang GL. Comprehensive profiling of the rice ubiquitome reveals the significance of lysine ubiquitination in young leaves. J Proteome Res. 2015;14(5):2017–25. Epub 2015/03/10. doi: 10.1021/pr5009724 25751157.
4. Kim W, Bennett EJ, Huttlin EL, Guo A, Li J, Possemato A, et al. Systematic and quantitative assessment of the ubiquitin-modified proteome. Mol Cell. 2011;44(2):325–40. Epub 2011/09/13. doi: 10.1016/j.molcel.2011.08.025 21906983; PubMed Central PMCID: PMC3200427.
5. Silmon de Monerri NC, Yakubu RR, Chen AL, Bradley PJ, Nieves E, Weiss LM, et al. The Ubiquitin Proteome of Toxoplasma gondii Reveals Roles for Protein Ubiquitination in Cell-Cycle Transitions. Cell Host Microbe. 2015;18(5):621–33. Epub 2015/11/17. doi: 10.1016/j.chom.2015.10.014 26567513; PubMed Central PMCID: PMC4968887.
6. Aminake MN, Arndt HD, Pradel G. The proteasome of malaria parasites: A multi-stage drug target for chemotherapeutic intervention? Int J Parasitol Drugs Drug Resist. 2012;2:1–10. Epub 2012/12/01. doi: 10.1016/j.ijpddr.2011.12.001 24533266; PubMed Central PMCID: PMC3862440.
7. Hamilton MJ, Lee M, Le Roch KG. The ubiquitin system: an essential component to unlocking the secrets of malaria parasite biology. Mol Biosyst. 2014;10(4):715–23. Epub 2014/02/01. doi: 10.1039/c3mb70506d 24481176; PubMed Central PMCID: PMC3990246.
8. Ponts N, Yang J, Chung DW, Prudhomme J, Girke T, Horrocks P, et al. Deciphering the ubiquitin-mediated pathway in apicomplexan parasites: a potential strategy to interfere with parasite virulence. PLoS One. 2008;3(6):e2386. Epub 2008/06/12. doi: 10.1371/journal.pone.0002386 18545708; PubMed Central PMCID: PMC2408969.
9. Agrawal S, Chung DW, Ponts N, van Dooren GG, Prudhomme J, Brooks CF, et al. An apicoplast localized ubiquitylation system is required for the import of nuclear-encoded plastid proteins. PLoS Pathog. 2013;9(6):e1003426. Epub 2013/06/21. doi: 10.1371/journal.ppat.1003426 23785288; PubMed Central PMCID: PMC3681736.
10. Spork S, Hiss JA, Mandel K, Sommer M, Kooij TW, Chu T, et al. An unusual ERAD-like complex is targeted to the apicoplast of Plasmodium falciparum. Eukaryot Cell. 2009;8(8):1134–45. Epub 2009/06/09. doi: 10.1128/EC.00083-09 19502583; PubMed Central PMCID: PMC2725561.
11. Ponts N, Saraf A, Chung DW, Harris A, Prudhomme J, Washburn MP, et al. Unraveling the ubiquitome of the human malaria parasite. J Biol Chem. 2011;286(46):40320–30. Epub 2011/09/21. doi: 10.1074/jbc.M111.238790 21930698; PubMed Central PMCID: PMC3220526.
12. Mata-Cantero L, Azkargorta M, Aillet F, Xolalpa W, LaFuente MJ, Elortza F, et al. New insights into host-parasite ubiquitin proteome dynamics in P. falciparum infected red blood cells using a TUBEs-MS approach. J Proteomics. 2016;139:45–59. Epub 2016/03/15. doi: 10.1016/j.jprot.2016.03.004 26972027.
13. Mata-Cantero L, Cid C, Gomez-Lorenzo MG, Xolalpa W, Aillet F, Martin JJ, et al. Development of two novel high-throughput assays to quantify ubiquitylated proteins in cell lysates: application to screening of new anti-malarials. Malar J. 2015;14:200. Epub 2015/05/15. doi: 10.1186/s12936-015-0708-1 25968882; PubMed Central PMCID: PMC4440562.
14. Horrocks P, Newbold CI. Intraerythrocytic polyubiquitin expression in Plasmodium falciparum is subjected to developmental and heat-shock control. Mol Biochem Parasitol. 2000;105(1):115–25. Epub 1999/12/29. doi: 10.1016/s0166-6851(99)00174-7 10613704.
15. Gonzalez-Lopez L, Carballar-Lejarazu R, Arrevillaga Boni G, Cortes-Martinez L, Cazares-Raga FE, Trujillo-Ocampo A, et al. Lys48 ubiquitination during the intraerythrocytic cycle of the rodent malaria parasite, Plasmodium chabaudi. PLoS One. 2017;12(6):e0176533. Epub 2017/06/13. doi: 10.1371/journal.pone.0176533 28604779; PubMed Central PMCID: PMC5467854.
16. Ng CL, Fidock DA, Bogyo M. Protein Degradation Systems as Antimalarial Therapeutic Targets. Trends Parasitol. 2017;33(9):731–43. Epub 2017/07/10. doi: 10.1016/j.pt.2017.05.009 28688800; PubMed Central PMCID: PMC5656264.
17. Bridgford JL, Xie SC, Cobbold SA, Pasaje CFA, Herrmann S, Yang T, et al. Artemisinin kills malaria parasites by damaging proteins and inhibiting the proteasome. Nat Commun. 2018;9(1):3801. Epub 2018/09/20. doi: 10.1038/s41467-018-06221-1 30228310; PubMed Central PMCID: PMC6143634.
18. Sanchez CP, Liu CH, Mayer S, Nurhasanah A, Cyrklaff M, Mu J, et al. A HECT ubiquitin-protein ligase as a novel candidate gene for altered quinine and quinidine responses in Plasmodium falciparum. PLoS Genet. 2014;10(5):e1004382. Epub 2014/05/17. doi: 10.1371/journal.pgen.1004382 24830312; PubMed Central PMCID: PMC4022464.
19. Hyer ML, Milhollen MA, Ciavarri J, Fleming P, Traore T, Sappal D, et al. A small-molecule inhibitor of the ubiquitin activating enzyme for cancer treatment. Nat Med. 2018;24(2):186–93. Epub 2018/01/16. doi: 10.1038/nm.4474 29334375.
20. Misra M, Kuhn M, Lobel M, An H, Statsyuk AV, Sotriffer C, et al. Dissecting the Specificity of Adenosyl Sulfamate Inhibitors Targeting the Ubiquitin-Activating Enzyme. Structure. 2017;25(7):1120–9 e3. Epub 2017/06/06. doi: 10.1016/j.str.2017.05.001 28578874.
21. Schafer A, Kuhn M, Schindelin H. Structure of the ubiquitin-activating enzyme loaded with two ubiquitin molecules. Acta Crystallogr D Biol Crystallogr. 2014;70(Pt 5):1311–20. Epub 2014/05/13. doi: 10.1107/S1399004714002910 24816100.
22. Jain J, Jain SK, Walker LA, Tekwani BL. Inhibitors of ubiquitin E3 ligase as potential new antimalarial drug leads. BMC Pharmacol Toxicol. 2017;18(1):40. Epub 2017/06/04. doi: 10.1186/s40360-017-0147-4 28577368; PubMed Central PMCID: PMC5457628.
23. Collins CR, Das S, Wong EH, Andenmatten N, Stallmach R, Hackett F, et al. Robust inducible Cre recombinase activity in the human malaria parasite Plasmodium falciparum enables efficient gene deletion within a single asexual erythrocytic growth cycle. Mol Microbiol. 2013;88(4):687–701. Epub 2013/03/16. doi: 10.1111/mmi.12206 23489321; PubMed Central PMCID: PMC3708112.
24. Jones ML, Das S, Belda H, Collins CR, Blackman MJ, Treeck M. A versatile strategy for rapid conditional genome engineering using loxP sites in a small synthetic intron in Plasmodium falciparum. Sci Rep. 2016;6:21800. Epub 2016/02/20. doi: 10.1038/srep21800 26892670; PubMed Central PMCID: PMC4759600.
25. Knuepfer E, Napiorkowska M, van Ooij C, Holder AA. Generating conditional gene knockouts in Plasmodium—a toolkit to produce stable DiCre recombinase-expressing parasite lines using CRISPR/Cas9. Sci Rep. 2017;7(1):3881. Epub 2017/06/22. doi: 10.1038/s41598-017-03984-3 28634346; PubMed Central PMCID: PMC5478596.
26. Schlott AC, Mayclin S, Reers AR, Coburn-Flynn O, Bell AS, Green JL, et al. Structure-guided identification of resistance breaking antimalarial N Myristoyltransferase inhibitors. Cell Chemical Biology. 2019; 26(7):991–1000 e7. Epub 2019/05/14. doi: 10.1016/j.chembiol.2019.03.015 31080074; PubMed Central PMCID: PMC6658617.
27. Cox J, Matic I, Hilger M, Nagaraj N, Selbach M, Olsen JV, et al. A practical guide to the MaxQuant computational platform for SILAC-based quantitative proteomics. Nat Protoc. 2009;4(5):698–705. Epub 2009/04/18. doi: 10.1038/nprot.2009.36 19373234.
28. Boeing S, Williamson L, Encheva V, Gori I, Saunders RE, Instrell R, et al. Multiomic Analysis of the UV-Induced DNA Damage Response. Cell Rep. 2016;15(7):1597–610. Epub 2016/05/18. doi: 10.1016/j.celrep.2016.04.047 27184836; PubMed Central PMCID: PMC4893159.
29. Ginsburg H. Progress in in silico functional genomics: the malaria Metabolic Pathways database. Trends Parasitol. 2006;22(6):238–40. Epub 2006/05/19. doi: 10.1016/j.pt.2006.04.008 16707276.
30. Green JL, Wall RJ, Vahokoski J, Yusuf NA, Ridzuan MAM, Stanway RR, et al. Compositional and expression analyses of the glideosome during the Plasmodium life cycle reveal an additional myosin light chain required for maximum motility. J Biol Chem. 2017;292(43):17857–75. Epub 2017/09/13. doi: 10.1074/jbc.M117.802769 28893907; PubMed Central PMCID: PMC5663884.
31. Saini E, Zeeshan M, Brady D, Pandey R, Kaiser G, Koreny L, et al. Photosensitized INA-Labelled protein 1 (PhIL1) is novel component of the inner membrane complex and is required for Plasmodium parasite development. Sci Rep. 2017;7(1):15577. Epub 2017/11/16. doi: 10.1038/s41598-017-15781-z 29138437; PubMed Central PMCID: PMC5686188.
32. Marti M, Good RT, Rug M, Knuepfer E, Cowman AF. Targeting malaria virulence and remodeling proteins to the host erythrocyte. Science. 2004;306(5703):1930–3. Epub 2004/12/14. doi: 10.1126/science.1102452 15591202.
33. Hiller NL, Bhattacharjee S, van Ooij C, Liolios K, Harrison T, Lopez-Estrano C, et al. A host-targeting signal in virulence proteins reveals a secretome in malarial infection. Science. 2004;306(5703):1934–7. Epub 2004/12/14. doi: 10.1126/science.1102737 15591203.
34. Heiber A, Kruse F, Pick C, Gruring C, Flemming S, Oberli A, et al. Identification of new PNEPs indicates a substantial non-PEXEL exportome and underpins common features in Plasmodium falciparum protein export. PLoS Pathog. 2013;9(8):e1003546. Epub 2013/08/21. doi: 10.1371/journal.ppat.1003546 23950716; PubMed Central PMCID: PMC3738491.
35. Gruring C, Heiber A, Kruse F, Flemming S, Franci G, Colombo SF, et al. Uncovering common principles in protein export of malaria parasites. Cell Host Microbe. 2012;12(5):717–29. Epub 2012/11/20. doi: 10.1016/j.chom.2012.09.010 23159060.
36. Vernot-Hernandez JP, Heidrich HG. Time-course of synthesis, transport and incorporation of a protein identified in purified membranes of host erythrocytes infected with a knob-forming strain of Plasmodium falciparum. Mol Biochem Parasitol. 1984;12(3):337–50. Epub 1984/07/01. doi: 10.1016/0166-6851(84)90090-2 6384777.
37. Hawthorne PL, Trenholme KR, Skinner-Adams TS, Spielmann T, Fischer K, Dixon MW, et al. A novel Plasmodium falciparum ring stage protein, REX, is located in Maurer's clefts. Mol Biochem Parasitol. 2004;136(2):181–9. Epub 2004/10/16. doi: 10.1016/j.molbiopara.2004.03.013 15481109.
38. Coppel RL, Lustigman S, Murray L, Anders RF. MESA is a Plasmodium falciparum phosphoprotein associated with the erythrocyte membrane skeleton. Mol Biochem Parasitol. 1988;31(3):223–31. Epub 1988/12/01. doi: 10.1016/0166-6851(88)90152-1 3065643.
39. Pasloske BL, Baruch DI, van Schravendijk MR, Handunnetti SM, Aikawa M, Fujioka H, et al. Cloning and characterization of a Plasmodium falciparum gene encoding a novel high-molecular weight host membrane-associated protein, PfEMP3. Mol Biochem Parasitol. 1993;59(1):59–72. Epub 1993/05/01. doi: 10.1016/0166-6851(93)90007-k 8515784.
40. Oberli A, Slater LM, Cutts E, Brand F, Mundwiler-Pachlatko E, Rusch S, et al. A Plasmodium falciparum PHIST protein binds the virulence factor PfEMP1 and comigrates to knobs on the host cell surface. FASEB J. 2014;28(10):4420–33. Epub 2014/07/02. doi: 10.1096/fj.14-256057 24983468; PubMed Central PMCID: PMC4202109.
41. Parish LA, Mai DW, Jones ML, Kitson EL, Rayner JC. A member of the Plasmodium falciparum PHIST family binds to the erythrocyte cytoskeleton component band 4.1. Malar J. 2013;12:160. Epub 2013/05/15. doi: 10.1186/1475-2875-12-160 23663475; PubMed Central PMCID: PMC3658886.
42. Maier AG, Rug M, O'Neill MT, Brown M, Chakravorty S, Szestak T, et al. Exported proteins required for virulence and rigidity of Plasmodium falciparum-infected human erythrocytes. Cell. 2008;134(1):48–61. Epub 2008/07/11. doi: 10.1016/j.cell.2008.04.051 18614010; PubMed Central PMCID: PMC2568870.
43. Sargeant TJ, Marti M, Caler E, Carlton JM, Simpson K, Speed TP, et al. Lineage-specific expansion of proteins exported to erythrocytes in malaria parasites. Genome Biol. 2006;7(2):R12. Epub 2006/03/02. doi: 10.1186/gb-2006-7-2-r12 16507167; PubMed Central PMCID: PMC1431722.
44. Mbengue A, Audiger N, Vialla E, Dubremetz JF, Braun-Breton C. Novel Plasmodium falciparum Maurer's clefts protein families implicated in the release of infectious merozoites. Mol Microbiol. 2013;88(2):425–42. Epub 2013/03/23. doi: 10.1111/mmi.12193 23517413.
45. Zuegge J, Ralph S, Schmuker M, McFadden GI, Schneider G. Deciphering apicoplast targeting signals—feature extraction from nuclear-encoded precursors of Plasmodium falciparum apicoplast proteins. Gene. 2001;280(1–2):19–26. Epub 2001/12/12. doi: 10.1016/s0378-1119(01)00776-4 11738814.
46. Boucher MJ, Ghosh S, Zhang L, Lal A, Jang SW, Ju A, et al. Integrative proteomics and bioinformatic prediction enable a high-confidence apicoplast proteome in malaria parasites. PLoS Biol. 2018;16(9):e2005895. Epub 2018/09/14. doi: 10.1371/journal.pbio.2005895 30212465; PubMed Central PMCID: PMC6155542.
47. Saraf A, Cervantes S, Bunnik EM, Ponts N, Sardiu ME, Chung DW, et al. Dynamic and Combinatorial Landscape of Histone Modifications during the Intraerythrocytic Developmental Cycle of the Malaria Parasite. J Proteome Res. 2016;15(8):2787–801. Epub 2016/06/14. doi: 10.1021/acs.jproteome.6b00366 27291344; PubMed Central PMCID: PMC5905347.
48. Trelle MB, Salcedo-Amaya AM, Cohen AM, Stunnenberg HG, Jensen ON. Global histone analysis by mass spectrometry reveals a high content of acetylated lysine residues in the malaria parasite Plasmodium falciparum. J Proteome Res. 2009;8(7):3439–50. Epub 2009/04/09. doi: 10.1021/pr9000898 19351122.
49. Brownell JE, Sintchak MD, Gavin JM, Liao H, Bruzzese FJ, Bump NJ, et al. Substrate-assisted inhibition of ubiquitin-like protein-activating enzymes: the NEDD8 E1 inhibitor MLN4924 forms a NEDD8-AMP mimetic in situ. Mol Cell. 2010;37(1):102–11. Epub 2010/02/05. doi: 10.1016/j.molcel.2009.12.024 20129059.
50. Enchev RI, Schulman BA, Peter M. Protein neddylation: beyond cullin-RING ligases. Nat Rev Mol Cell Biol. 2015;16(1):30–44. Epub 2014/12/23. doi: 10.1038/nrm3919 25531226; PubMed Central PMCID: PMC5131867.
51. Bryk AH, Wisniewski JR. Quantitative Analysis of Human Red Blood Cell Proteome. J Proteome Res. 2017;16(8):2752–61. Epub 2017/07/12. doi: 10.1021/acs.jproteome.7b00025 28689405.
52. Longhurst HJ, Holder AA. The histones of Plasmodium falciparum: identification, purification and a possible role in the pathology of malaria. Parasitology. 1997;114 (Pt 5):413–9. Epub 1997/05/01. doi: 10.1017/s0031182096008621 9149412.
53. Chen JJ, Tsu CA, Gavin JM, Milhollen MA, Bruzzese FJ, Mallender WD, et al. Mechanistic studies of substrate-assisted inhibition of ubiquitin-activating enzyme by adenosine sulfamate analogues. J Biol Chem. 2011;286(47):40867–77. Epub 2011/10/05. doi: 10.1074/jbc.M111.279984 21969368; PubMed Central PMCID: PMC3220466.
54. Artavanis-Tsakonas K, Weihofen WA, Antos JM, Coleman BI, Comeaux CA, Duraisingh MT, et al. Characterization and structural studies of the Plasmodium falciparum ubiquitin and Nedd8 hydrolase UCHL3. J Biol Chem. 2010;285(9):6857–66. Epub 2010/01/01. doi: 10.1074/jbc.M109.072405 20042598; PubMed Central PMCID: PMC2825479.
55. Barghout SH, Patel PS, Wang X, Xu GW, Kavanagh S, Halgas O, et al. Preclinical evaluation of the selective small-molecule UBA1 inhibitor, TAK-243, in acute myeloid leukemia. Leukemia. 2019;33(1):37–51. Epub 2018/06/10. doi: 10.1038/s41375-018-0167-0 29884901.
56. Burrows JN, Duparc S, Gutteridge WE, Hooft van Huijsduijnen R, Kaszubska W, Macintyre F, et al. New developments in anti-malarial target candidate and product profiles. Malar J. 2017;16(1):26. Epub 2017/01/15. doi: 10.1186/s12936-016-1675-x 28086874; PubMed Central PMCID: PMC5237200.
57. Li H, O'Donoghue AJ, van der Linden WA, Xie SC, Yoo E, Foe IT, et al. Structure- and function-based design of Plasmodium-selective proteasome inhibitors. Nature. 2016;530(7589):233–6. Epub 2016/02/13. doi: 10.1038/nature16936 26863983; PubMed Central PMCID: PMC4755332.
58. Stokes BH, Yoo E, Murithi JM, Luth MR, Afanasyev P, da Fonseca PCA, et al. Covalent Plasmodium falciparum-selective proteasome inhibitors exhibit a low propensity for generating resistance in vitro and synergize with multiple antimalarial agents. PLoS Pathog. 2019;15(6):e1007722. Epub 2019/06/07. doi: 10.1371/journal.ppat.1007722 31170268; PubMed Central PMCID: PMC6553790.
59. Xie SC, Gillett DL, Spillman NJ, Tsu C, Luth MR, Ottilie S, et al. Target Validation and Identification of Novel Boronate Inhibitors of the Plasmodium falciparum Proteasome. J Med Chem. 2018;61(22):10053–66. Epub 2018/10/31. doi: 10.1021/acs.jmedchem.8b01161 30373366; PubMed Central PMCID: PMC6257627.
60. Dogovski C, Xie SC, Burgio G, Bridgford J, Mok S, McCaw JM, et al. Targeting the cell stress response of Plasmodium falciparum to overcome artemisinin resistance. PLoS Biol. 2015;13(4):e1002132. Epub 2015/04/23. doi: 10.1371/journal.pbio.1002132 25901609; PubMed Central PMCID: PMC4406523.
61. Tilley L, Straimer J, Gnadig NF, Ralph SA, Fidock DA. Artemisinin Action and Resistance in Plasmodium falciparum. Trends Parasitol. 2016;32(9):682–96. Epub 2016/06/13. doi: 10.1016/j.pt.2016.05.010 27289273; PubMed Central PMCID: PMC5007624.
62. Mbengue A, Bhattacharjee S, Pandharkar T, Liu H, Estiu G, Stahelin RV, et al. A molecular mechanism of artemisinin resistance in Plasmodium falciparum malaria. Nature. 2015;520(7549):683–7. Epub 2015/04/16. doi: 10.1038/nature14412 25874676; PubMed Central PMCID: PMC4417027.
63. Bhattacharjee S, Coppens I, Mbengue A, Suresh N, Ghorbal M, Slouka Z, et al. Remodeling of the malaria parasite and host human red cell by vesicle amplification that induces artemisinin resistance. Blood. 2018;131(11):1234–47. Epub 2018/01/25. doi: 10.1182/blood-2017-11-814665 29363540; PubMed Central PMCID: PMC5855022.
64. Suresh N, Haldar K. Mechanisms of artemisinin resistance in Plasmodium falciparum malaria. Curr Opin Pharmacol. 2018;42:46–54. Epub 2018/08/05. doi: 10.1016/j.coph.2018.06.003 30077118; PubMed Central PMCID: PMC6314025.
65. Taylor HM, Grainger M, Holder AA. Variation in the expression of a Plasmodium falciparum protein family implicated in erythrocyte invasion. Infect Immun. 2002;70(10):5779–89. Epub 2002/09/14. doi: 10.1128/iai.70.10.5779-5789.2002 12228308; PubMed Central PMCID: PMC128319.
66. Lambros C, Vanderberg JP. Synchronization of Plasmodium falciparum erythrocytic stages in culture. J Parasitol. 1979;65(3):418–20. Epub 1979/06/01. 383936.
67. Blackman MJ. Purification of Plasmodium falciparum merozoites for analysis of the processing of merozoite surface protein-1. Methods Cell Biol. 1994;45:213–20. Epub 1994/01/01. doi: 10.1016/s0091-679x(08)61853-1 7707987.
68. Green JL, Moon RW, Whalley D, Bowyer PW, Wallace C, Rochani A, et al. Imidazopyridazine Inhibitors of Plasmodium falciparum Calcium-Dependent Protein Kinase 1 Also Target Cyclic GMP-Dependent Protein Kinase and Heat Shock Protein 90 To Kill the Parasite at Different Stages of Intracellular Development. Antimicrob Agents Chemother. 2015;60(3):1464–75. Epub 2015/12/30. doi: 10.1128/AAC.01748-15 26711771; PubMed Central PMCID: PMC4775997.
69. MacPherson CR, Scherf A. Flexible guide-RNA design for CRISPR applications using Protospacer Workbench. Nat Biotechnol. 2015;33(8):805–6. Epub 2015/06/30. doi: 10.1038/nbt.3291 26121414.
70. Cox J, Neuhauser N, Michalski A, Scheltema RA, Olsen JV, Mann M. Andromeda: a peptide search engine integrated into the MaxQuant environment. J Proteome Res. 2011;10(4):1794–805. Epub 2011/01/25. doi: 10.1021/pr101065j 21254760.
71. Chou MF, Schwartz D. Biological sequence motif discovery using motif-x. Curr Protoc Bioinformatics. 2011;Chapter 13:Unit 13 5–24. Epub 2011/09/09. doi: 10.1002/0471250953.bi1315s35 21901740.
72. Bauer S, Grossmann S, Vingron M, Robinson PN. Ontologizer 2.0—a multifunctional tool for GO term enrichment analysis and data exploration. Bioinformatics. 2008;24(14):1650–1. Epub 2008/05/31. doi: 10.1093/bioinformatics/btn250 18511468.
73. Merico D, Isserlin R, Stueker O, Emili A, Bader GD. Enrichment map: a network-based method for gene-set enrichment visualization and interpretation. PLoS One. 2010;5(11):e13984. Epub 2010/11/19. doi: 10.1371/journal.pone.0013984 21085593; PubMed Central PMCID: PMC2981572.
74. Laskowski RA, MacArthur MW, Moss DS, Thornton JM. PROCHECK: a program to check the stereochemical quality of protein structures. Journal of Applied Crystallography. 1993;26(2):283–91. doi: 10.1107/s0021889892009944
75. Stieglitz B, Morris-Davies AC, Koliopoulos MG, Christodoulou E, Rittinger K. LUBAC synthesizes linear ubiquitin chains via a thioester intermediate. EMBO Rep. 2012;13(9):840–6. Epub 2012/07/14. doi: 10.1038/embor.2012.105 22791023; PubMed Central PMCID: PMC3432797.
76. Dove KK, Stieglitz B, Duncan ED, Rittinger K, Klevit RE. Molecular insights into RBR E3 ligase ubiquitin transfer mechanisms. EMBO Rep. 2016;17(8):1221–35. Epub 2016/06/18. doi: 10.15252/embr.201642641 27312108; PubMed Central PMCID: PMC4967960.
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