A molecular marker of artemisinin-resistant Plasmodium falciparum malaria

Nature - Tập 505 Số 7481 - Trang 50-55 - 2014
Frédéric Ariey1, Benoît Witkowski2, Chanaki Amaratunga3, Johann Beghain1, Anne-Claire Langlois1, Nimol Khim2, Saorin Kim2, Valentine Duru2, Christiane Bouchier4, Laurence Ma4, Pharath Lim2, Rithea Leang5, Duong Socheat5, Sokunthea Sreng5, Seila Suon5, Char Meng Chuor5, Denis Mey Bout6, Sandie Ménard7, William O. Rogers8, Blaise Genton9, Thierry Fandeur2, Olivo Miotto10, Pascal Ringwald11, Jacques Le Bras12, Antoine Berry7, Jean-Christophe Barale13, Rick M. Fairhurst3, Françoise Benoit‐Vical14, Odile Mercereau‐Puijalon13, Didier Ménard2
1Institut Pasteur, Parasite Molecular Immunology Unit, 75724 Paris Cedex 15, France ,
2Institut Pasteur du Cambodge, Malaria Molecular Epidemiology Unit, Phnom Penh, Cambodia ,
3Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, 20892, Maryland, USA
4Département Génomes et Génétique, Institut Pasteur, Plate-forme Génomique, 75724 Paris Cedex 15, France,
5National Center for Parasitology, Entomology and Malaria Control, Phnom Penh, Cambodia
6SSA WHO, Drug Monitoring in Cambodia, National Center for Parasitology, Entomology and Malaria Control, Phnom Penh, Cambodia ,
7Service de Parasitologie et Mycologie, Centre Hospitalier Universitaire de Toulouse, 31059 Toulouse Cedex 9, France ,
8Naval Medical Research Unit #2 Detachment, Phnom Penh, Cambodia ,
9Swiss Tropical and Public Health Institute, 4051 Basel, Switzerland
10MRC Centre for Genomics and Global Health, University of Oxford, Oxford OX3 7BN, UK ,
11Global Malaria Program, World Health Organization, 1211 Geneva, Switzerland ,
12Centre National de Référence du Paludisme, CHU Bichat-Claude Bernard, APHP, PRES Sorbonne Paris Cité, 75018 Paris, France ,
13Centre National de la Recherche Scientifique, Unité de Recherche Associée 2581, 75724 Paris Cedex 15, France ,
14Centre National de la Recherche Scientifique, Laboratoire de Chimie de Coordination UPR8241, 31077 Toulouse Cedex 4, France ,

Tóm tắt

Từ khóa


Tài liệu tham khảo

Dondorp, A. M. et al. Artemisinin resistance in Plasmodium falciparum malaria. N. Engl. J. Med. 361, 455–467 (2009)

World Health Organization. Global Report on Antimalarial Drug Efficacy and Drug Resistance: 2000–2010 (World Health Organization, 2010)

Mita, T. et al. Limited geographical origin and global spread of sulfadoxine-resistant dhps alleles in Plasmodium falciparum populations. J. Infect. Dis. 204, 1980–1988 (2011)

Roper, C. et al. Intercontinental spread of pyrimethamine-resistant malaria. Science 305, 1124 (2004)

Wootton, J. C. et al. Genetic diversity and chloroquine selective sweeps in Plasmodium falciparum . Nature 418, 320–323 (2002)

Amaratunga, C. et al. Artemisinin-resistant Plasmodium falciparum in Pursat province, western Cambodia: a parasite clearance rate study. Lancet Infect. Dis. 12, 851–858 (2012)

Kyaw, M. P. et al. Reduced susceptibility of Plasmodium falciparum to artesunate in southern Myanmar. PLoS ONE 8, e57689 (2013)

Noedl, H. et al. Evidence of artemisinin-resistant malaria in western Cambodia. N. Engl. J. Med. 359, 2619–2620 (2008)

Phyo, A. P. et al. Emergence of artemisinin-resistant malaria on the western border of Thailand: a longitudinal study. Lancet 379, 1960–1966 (2012)

Hien, T. T. et al. In vivo susceptibility of Plasmodium falciparum to artesunate in Binh Phuoc Province, Vietnam. Malar. J. 11, 355 (2012)

Flegg, J. A. et al. Standardizing the measurement of parasite clearance in falciparum malaria: the parasite clearance estimator. Malar. J. 10, 339 (2011)

White, N. J. The parasite clearance curve. Malar. J. 10, 278 (2011)

Witkowski, B. et al. Novel phenotypic assays for the detection of artemisinin-resistant Plasmodium falciparum malaria in Cambodia: in-vitro and ex-vivo drug-response studies. Lancet Infect. Dis. 13, 1043–1049 (2013)

Cheeseman, I. H. et al. A major genome region underlying artemisinin resistance in malaria. Science 336, 79–82 (2012)

Miotto, O. et al. Multiple populations of artemisinin-resistant Plasmodium falciparum in Cambodia. Nature Genet. 45, 648–655 (2013)

Takala-Harrison, S. et al. Genetic loci associated with delayed clearance of Plasmodium falciparum following artemisinin treatment in Southeast Asia. Proc. Natl Acad. Sci. USA 110, 240–245 (2013)

Lopera-Mesa, T. M. et al. Plasmodium falciparum clearance rates in response to artesunate in Malian children with malaria: effect of acquired immunity. J. Infect. Dis. 207, 1655–1663 (2013)

Witkowski, B. et al. Increased tolerance to artemisinin in Plasmodium falciparum is mediated by a quiescence mechanism. Antimicrob. Agents Chemother. 54, 1872–1877 (2010)

Klonis, N. et al. Artemisinin activity against Plasmodium falciparum requires hemoglobin uptake and digestion. Proc. Natl Acad. Sci. USA 108, 11405–11410 (2011)

Vigan-Womas, I. et al. An in vivo and in vitro model of Plasmodium falciparum rosetting and autoagglutination mediated by varO, a group A var gene encoding a frequent serotype. Infect. Immun. 76, 5565–5580 (2008)

Cui, L. et al. Mechanisms of in vitro resistance to dihydroartemisinin in Plasmodium falciparum . Mol. Microbiol. 86, 111–128 (2012)

Leang, R. et al. Efficacy of dihydroartemisinin-piperaquine for treatment of uncomplicated Plasmodium falciparum and Plasmodium vivax in Cambodia, 2008 to 2010. Antimicrob. Agents Chemother. 57, 818–826 (2013)

Sidhu, A. B. et al. Chloroquine resistance in Plasmodium falciparum malaria parasites conferred by pfcrt mutations. Science 298, 210–213 (2002)

Valderramos, S. G. et al. Identification of a mutant PfCRT-mediated chloroquine tolerance phenotype in Plasmodium falciparum . PLoS Pathog. 6, e1000887 (2010)

Bhisutthibhan, J. et al. The Plasmodium falciparum translationally controlled tumor protein homolog and its reaction with the antimalarial drug artemisinin. J. Biol. Chem. 273, 16192–16198 (1998)

Eichhorn, T. et al. Molecular interaction of artemisinin with translationally controlled tumor protein (TCTP) of Plasmodium falciparum . Biochem. Pharmacol. 85, 38–45 (2013)

Sanchez, C. P. et al. Polymorphisms within PfMDR1 alter the substrate specificity for anti-malarial drugs in Plasmodium falciparum . Mol. Microbiol. 70, 786–798 (2008)

Veiga, M. I. et al. Novel polymorphisms in Plasmodium falciparum ABC transporter genes are associated with major ACT antimalarial drug resistance. PLoS ONE 6, e20212 (2011)

Raj, D. K. et al. Disruption of a Plasmodium falciparum multidrug resistance-associated protein (PfMRP) alters its fitness and transport of antimalarial drugs and glutathione. J. Biol. Chem. 284, 7687–7696 (2009)

Anderson, T. J. et al. Are transporter genes other than the chloroquine resistance locus (pfcrt) and multidrug resistance gene (pfmdr) associated with antimalarial drug resistance? Antimicrob. Agents Chemother. 49, 2180–2188 (2005)

Jambou, R. et al. Resistance of Plasmodium falciparum field isolates to in-vitro artemether and point mutations of the SERCA-type PfATPase6. Lancet 366, 1960–1963 (2005)

Krishna, S. et al. Artemisinins and the biological basis for the PfATP6/SERCA hypothesis. Trends Parasitol. 26, 517–523 (2010)

Hunt, P. et al. Gene encoding a deubiquitinating enzyme is mutated in artesunate- and chloroquine-resistant rodent malaria parasites. Mol. Microbiol. 65, 27–40 (2007)

Hunt, P. et al. Experimental evolution, genetic analysis and genome re-sequencing reveal the mutation conferring artemisinin resistance in an isogenic lineage of malaria parasites. BMC Genomics 11, 499 (2010)

Borges, S. et al. Genome-wide scan reveals amplification of mdr1 as a common denominator of resistance to mefloquine, lumefantrine, and artemisinin in Plasmodium chabaudi malaria parasites. Antimicrob. Agents Chemother. 55, 4858–4865 (2011)

Chavchich, M. et al. Role of pfmdr1 amplification and expression in induction of resistance to artemisinin derivatives in Plasmodium falciparum . Antimicrob. Agents Chemother. 54, 2455–2464 (2010)

Chen, N. et al. Deamplification of pfmdr1-containing amplicon on chromosome 5 in Plasmodium falciparum is associated with reduced resistance to artelinic acid in vitro . Antimicrob. Agents Chemother. 54, 3395–3401 (2010)

Picot, S. et al. A systematic review and meta-analysis of evidence for correlation between molecular markers of parasite resistance and treatment outcome in falciparum malaria. Malar. J. 8, 89 (2009)

Price, R. N. et al. Mefloquine resistance in Plasmodium falciparum and increased pfmdr1 gene copy number. Lancet 364, 438–447 (2004)

Sidhu, A. B. et al. Decreasing pfmdr1 copy number in Plasmodium falciparum malaria heightens susceptibility to mefloquine, lumefantrine, halofantrine, quinine, and artemisinin. J. Infect. Dis. 194, 528–535 (2006)

Yuan, J. et al. Chemical genomic profiling for antimalarial therapies, response signatures, and molecular targets. Science 333, 724–729 (2011)

Amambua-Ngwa, A. et al. Population genomic scan for candidate signatures of balancing selection to guide antigen characterization in malaria parasites. PLoS Genet. 8, e1002992 (2012)

Adams, J. et al. The kelch repeat superfamily of proteins: propellers of cell function. Trends Cell Biol. 10, 17–24 (2000)

Prag, S. & Adams, J. C. Molecular phylogeny of the kelch-repeat superfamily reveals an expansion of BTB/kelch proteins in animals. BMC Bioinformatics 4, 42 (2003)

Witkowski, B. et al. Reduced artemisinin susceptibility of Plasmodium falciparum ring stages in western Cambodia. Antimicrob. Agents Chemother. 57, 914–923 (2013)

Padmanabhan, B. et al. Structural basis for defects of Keap1 activity provoked by its point mutations in lung cancer. Mol. Cell 21, 689–700 (2006)

Boyden, L. M. et al. Mutations in kelch-like 3 and cullin 3 cause hypertension and electrolyte abnormalities. Nature 482, 98–102 (2012)

Li, X., Zhang, D., Hannink, M. & Beamer, L. J. Crystal structure of the Kelch domain of human Keap1. J. Biol. Chem. 279, 54750–54758 (2004)

Itoh, K. et al. Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes Dev. 13, 76–86 (1999)

Zhang, D. D. & Hannink, M. Distinct cysteine residues in Keap1 are required for Keap1-dependent ubiquitination of Nrf2 and for stabilization of Nrf2 by chemopreventive agents and oxidative stress. Mol. Cell. Biol. 23, 8137–8152 (2003)

Bozdech, Z. & Ginsburg, H. Antioxidant defense in Plasmodium falciparum--data mining of the transcriptome. Malar. J. 3, 23 (2004)

Nesser, N. K., Peterson, D. O. & Hawley, D. K. RNA polymerase II subunit Rpb9 is important for transcriptional fidelity in vivo . Proc. Natl Acad. Sci. USA 103, 3268–3273 (2006)

Kettenberger, H., Armache, K. J. & Cramer, P. Architecture of the RNA polymerase II-TFIIS complex and implications for mRNA cleavage. Cell 114, 347–357 (2003)

Dorin-Semblat, D., Sicard, A., Doerig, C., Ranford-Cartwright, L. & Doerig, C. Disruption of the PfPK7 gene impairs schizogony and sporogony in the human malaria parasite Plasmodium falciparum . Eukaryot. Cell 7, 279–285 (2008)

Tewari, R. et al. The systematic functional analysis of Plasmodium protein kinases identifies essential regulators of mosquito transmission. Cell Host Microbe 8, 377–387 (2010)

Rosenthal, P. J., McKerrow, J. H., Aikawa, M., Nagasawa, H. & Leech, J. H. A malarial cysteine proteinase is necessary for hemoglobin degradation by Plasmodium falciparum . J. Clin. Invest. 82, 1560–1566 (1988)

Sijwali, P. S. et al. Plasmodium falciparum cysteine protease falcipain-1 is not essential in erythrocytic stage malaria parasites. Proc. Natl Acad. Sci. USA 101, 8721–8726 (2004)

Sijwali, P. S., Koo, J., Singh, N. & Rosenthal, P. J. Gene disruptions demonstrate independent roles for the four falcipain cysteine proteases of Plasmodium falciparum . Mol. Biochem. Parasitol. 150, 96–106 (2006)

Klonis, N. et al. Altered temporal response of malaria parasites determines differential sensitivity to artemisinin. Proc. Natl Acad. Sci. USA 110, 5157–5162 (2013)

Lobo, C. A., Fujioka, H., Aikawa, M. & Kumar, N. Disruption of the Pfg27 locus by homologous recombination leads to loss of the sexual phenotype in P. falciparum. Mol. Cell 3, 793–798 (1999)

Olivieri, A. et al. The Plasmodium falciparum protein Pfg27 is dispensable for gametocyte and gamete production, but contributes to cell integrity during gametocytogenesis. Mol. Microbiol. 73, 180–193 (2009)

Sharma, A., Sharma, I., Kogkasuriyachai, D. & Kumar, N. Structure of a gametocyte protein essential for sexual development in Plasmodium falciparum . Nature Struct. Biol. 10, 197–203 (2003)