Development and application of a high-throughput screening assay for identification of small molecule inhibitors of the P. falciparum reticulocyte binding-like homologue 5 protein

Brad E. Sleebs1,2, Kate E. Jarman1,2, Sonja Frolich3, Wilson Wong1,2, Julie Healer1,2, Weiwen Dai1, Isabelle S. Lucet1,2, Danny W. Wilson3, Alan F. Cowman1,2
1The Walter and Eliza Hall Institute of Medical Research Parkville, Victoria 3052, Australia
2Department of Medical Biology, The University of Melbourne, Parkville, Victoria, 3052, Australia
3Research Centre for Infectious Diseases, School of Biological Sciences, University of Adelaide, Adelaide, South Australia, 5005, Australia

Tài liệu tham khảo

Alanine, 2019, Human antibodies that slow erythrocyte invasion potentiate malaria-neutralizing antibodies, Cell, 178, 216, 10.1016/j.cell.2019.05.025 Ashton, 2019, The development process for discovery and clinical advancement of modern antimalarials, J. Med. Chem., 62, 10526, 10.1021/acs.jmedchem.9b00761 Baum, 2009, Reticulocyte-binding protein homologue 5 - an essential adhesin involved in invasion of human erythrocytes by Plasmodium falciparum, Int. J. Parasitol., 39, 371, 10.1016/j.ijpara.2008.10.006 Bejon, 2013, Efficacy of RTS,S malaria vaccines: individual-participant pooled analysis of phase 2 data, Lancet Infect. Dis., 13, 319, 10.1016/S1473-3099(13)70005-7 Boyle, 2010, Isolation of viable Plasmodium falciparum merozoites to define erythrocyte invasion events and advance vaccine and drug development, Proc. Natl. Acad. Sci. U. S. A., 107, 14378, 10.1073/pnas.1009198107 Burns, 2019, Targeting malaria parasite invasion of red blood cells as an antimalarial strategy, FEMS Microbiol. Rev., 43, 223, 10.1093/femsre/fuz005 Bustamante, 2013, A full-length recombinant Plasmodium falciparum PfRH5 protein induces inhibitory antibodies that are effective across common PfRH5 genetic variants, Vaccine, 31, 373, 10.1016/j.vaccine.2012.10.106 Calculator Plugins were used for structure property prediction and calculation Chen, 2011, An EGF-like protein forms a complex with PfRh5 and is required for invasion of human erythrocytes by Plasmodium falciparum, PLoS Pathog., 7, 10.1371/journal.ppat.1002199 Chen, 2014, Crystal structure of PfRh5, an essential P. falciparum ligand for invasion of human erythrocytes, Elife, 3, 10.7554/eLife.04187 Chiu, 2014, Association of antibodies to Plasmodium falciparum reticulocyte binding protein homologue 5 with protection from clinical malaria, Front. Microbiol., 5, 314, 10.3389/fmicb.2014.00314 Cimmperman, 2008, A quantitative model of thermal stabilization and destabilization of proteins by ligands, Biophys. J., 95, 3222, 10.1529/biophysj.108.134973 Coan, 2009, Promiscuous aggregate-based inhibitors promote enzyme unfolding, J. Med. Chem., 52, 2067, 10.1021/jm801605r Counihan, 2013, Plasmodium rhoptry proteins: why order is important, Trends Parasitol., 29, 228, 10.1016/j.pt.2013.03.003 Cowman, 2012, The cellular and molecular basis for malaria parasite invasion of the human red blood cell, J. Cell Biol., 198, 961, 10.1083/jcb.201206112 Crosnier, 2011, Basigin is a receptor essential for erythrocyte invasion by Plasmodium falciparum, Nature, 480, 534, 10.1038/nature10606 Doak, 2010, Colloid formation by drugs in simulated intestinal fluid, J. Med. Chem., 53, 4259, 10.1021/jm100254w Douglas, 2015, A PfRH5-based vaccine is efficacious against Heterologous strain blood-stage Plasmodium falciparum infection in aotus monkeys, Cell Host Microbe, 17, 130, 10.1016/j.chom.2014.11.017 Douglas, 2014, Neutralization of Plasmodium falciparum merozoites by antibodies against PfRH5, J. Immunol., 192, 245, 10.4049/jimmunol.1302045 Drew, 2015, PfRH5 as a candidate vaccine for Plasmodium falciparum malaria, Trends Parasitol., 31, 87, 10.1016/j.pt.2015.02.001 Gagaring, K., Borboa, R., Francek, C., Chen, Z., Buenviaje, J., Plouffe, D., Winzeler, E., Brinker, A., Diagana, T., Taylor, J., Glynne, R., Chatterjee, A., Kuhen, K., Novartis-GNF Malaria Box. Genomics Institute of the Novartis Research Foundation (GNF), 10675 John Jay Hopkins Drive, San Diego CA 92121, USA and Novartis Institute for Tropical Disease, 10 Biopolis Road, Chromos # 05-01, 138 670 Singapore. Gamo, 2010, Thousands of chemical starting points for antimalarial lead identification, Nature, 465, 305, 10.1038/nature09107 Geen, 2006, A direct and high yielding route to 2-(5-tetrazolyl) substituted benzopyran-4-ones: synthesis of pranlukast, Synth. Commun., 27, 1065, 10.1080/00397919708003052 Guiguemde, 2010, Chemical genetics of Plasmodium falciparum, Nature, 465, 311, 10.1038/nature09099 Hayton, 2008, Erythrocyte binding protein PfRH5 polymorphisms determine species-specific pathways of Plasmodium falciparum invasion, Cell Host Microbe, 4, 40, 10.1016/j.chom.2008.06.001 Healer, 2019, Neutralising antibodies block the function of Rh5/Ripr/CyRPA complex during invasion of Plasmodium falciparum into human erythrocytes, Cell Microbiol., 21, 10.1111/cmi.13030 Lessene, 2013, Structure-guided design of a selective BCL-X(L) inhibitor, Nat. Chem. Biol., 9, 390, 10.1038/nchembio.1246 Mbengue, 2012, Human erythrocyte remodelling during Plasmodium falciparum malaria parasite growth and egress, Br. J. Haematol., 157, 171, 10.1111/j.1365-2141.2012.09044.x Murphy, 2013, The pseudokinase MLKL mediates necroptosis via a molecular switch mechanism, Immunity, 39, 443, 10.1016/j.immuni.2013.06.018 Murphy, 2014, Insights into the evolution of divergent nucleotide-binding mechanisms among pseudokinases revealed by crystal structures of human and mouse MLKL, Biochem. J., 457, 369, 10.1042/BJ20131270 Murphy, 2014, A robust methodology to subclassify pseudokinases based on their nucleotide-binding properties, Biochem. J., 457, 323, 10.1042/BJ20131174 Park, 2008, Discovery of an orally bioavailable small molecule inhibitor of prosurvival B-cell lymphoma 2 proteins, J. Med. Chem., 51, 6902, 10.1021/jm800669s Patel, 2016, Biochemical and structural insights into doublecortin-like kinase domain 1, Structure, 24, 1550, 10.1016/j.str.2016.07.008 Payne, 2017, Human vaccination against RH5 induces neutralizing antimalarial antibodies that inhibit RH5 invasion complex interactions, JCI Insight, 2, 10.1172/jci.insight.96381 Pingaew, 2014, Design, synthesis and molecular docking studies of novel N-benzenesulfonyl-1,2,3,4-tetrahydroisoquinoline-based triazoles with potential anticancer activity, Eur. J. Med. Chem., 81, 192, 10.1016/j.ejmech.2014.05.019 Ragotte, 2020, The RH5-CyRPA-Ripr complex as a malaria vaccine target, Trends Parasitol., 36, 545, 10.1016/j.pt.2020.04.003 Raposo, 1996, Malonic acid receptors with decarboxylative activity, Tetrahedron, 52, 12323, 10.1016/0040-4020(96)00719-3 Reddy, 2015, Multiprotein complex between the GPI-anchored CyRPA with PfRH5 and PfRipr is crucial for Plasmodium falciparum erythrocyte invasion, Proc. Natl. Acad. Sci. U.S.A., 112, 1179, 10.1073/pnas.1415466112 Reddy, 2014, Bacterially expressed full-length recombinant Plasmodium falciparum RH5 protein binds erythrocytes and elicits potent strain-transcending parasite-neutralizing antibodies, Infect. Immun., 82, 152, 10.1128/IAI.00970-13 RTS, 2012, A phase 3 trial of RTS,S/AS01 malaria vaccine in african infants, N. Engl. J. Med., 367, 2284, 10.1056/NEJMoa1208394 Souers, 2013, ABT-199, a potent and selective BCL-2 inhibitor, achieves antitumor activity while sparing platelets, Nat. Med., 19, 202, 10.1038/nm.3048 Spangenberg, 2013, The open access malaria box: a drug discovery catalyst for neglected diseases, PloS One, 8, 10.1371/journal.pone.0062906 Trager, 1976, Human malaria parasites in continuous culture, Science, 193, 673, 10.1126/science.781840 Tran, 2014, Naturally acquired antibodies specific for Plasmodium falciparum reticulocyte-binding protein homologue 5 inhibit parasite growth and predict protection from malaria, J. Infect. Dis., 209, 789, 10.1093/infdis/jit553 Volz, 2016, Essential role of the PfRh5/PfRipr/CyRPA complex during Plasmodium falciparum invasion of erythrocytes, Cell Host Microbe, 20, 60, 10.1016/j.chom.2016.06.004 Weiss, 2015, Revealing the sequence and resulting cellular morphology of receptor-ligand interactions during Plasmodium falciparum invasion of erythrocytes, PLoS Pathog., 11, 10.1371/journal.ppat.1004670 Wilson, 2010, Development of fluorescent Plasmodium falciparum for in vitro growth inhibition assays, Malar. J., 9, 152, 10.1186/1475-2875-9-152 Wilson, 2015, Macrolides rapidly inhibit red blood cell invasion by the human malaria parasite, Plasmodium falciparum, BMC Biol., 13, 52, 10.1186/s12915-015-0162-0 Wilson, 2013, Defining the timing of action of antimalarial drugs against Plasmodium falciparum, Antimicrob. Agents Chemother., 57, 1455, 10.1128/AAC.01881-12 Wong, 2018, Structure of Plasmodium falciparum Rh5-CyRPA-Ripr invasion complex, Nature, 565, 118, 10.1038/s41586-018-0779-6 Xu, 2010, Crystal structure of the entire ectodomain of gp130: insights into the molecular assembly of the tall cytokine receptor complexes, J. Biol. Chem., 285, 21214, 10.1074/jbc.C110.129502 Yasgar, 2016, AlphaScreen-based assays: ultra-high-throughput screening for small-molecule inhibitors of challenging enzymes and protein-protein interactions, Methods Mol. Biol., 1439, 77, 10.1007/978-1-4939-3673-1_5