Haem-activated promiscuous targeting of artemisinin in Plasmodium falciparum.

Article Details

Citation

Wang J, Zhang CJ, Chia WN, Loh CC, Li Z, Lee YM, He Y, Yuan LX, Lim TK, Liu M, Liew CX, Lee YQ, Zhang J, Lu N, Lim CT, Hua ZC, Liu B, Shen HM, Tan KS, Lin Q

Haem-activated promiscuous targeting of artemisinin in Plasmodium falciparum.

Nat Commun. 2015 Dec 22;6:10111. doi: 10.1038/ncomms10111.

PubMed ID
26694030 [ View in PubMed
]
Abstract

The mechanism of action of artemisinin and its derivatives, the most potent of the anti-malarial drugs, is not completely understood. Here we present an unbiased chemical proteomics analysis to directly explore this mechanism in Plasmodium falciparum. We use an alkyne-tagged artemisinin analogue coupled with biotin to identify 124 artemisinin covalent binding protein targets, many of which are involved in the essential biological processes of the parasite. Such a broad targeting spectrum disrupts the biochemical landscape of the parasite and causes its death. Furthermore, using alkyne-tagged artemisinin coupled with a fluorescent dye to monitor protein binding, we show that haem, rather than free ferrous iron, is predominantly responsible for artemisinin activation. The haem derives primarily from the parasite's haem biosynthesis pathway at the early ring stage and from haemoglobin digestion at the latter stages. Our results support a unifying model to explain the action and specificity of artemisinin in parasite killing.

DrugBank Data that Cites this Article

Drugs
Drug Targets
DrugTargetKindOrganismPharmacological ActionActions
Artenimol14-3-3 proteinProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
Artenimol40S ribosomal protein S19ProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
Artenimol40S ribosomal protein S21ProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
Artenimol40S ribosomal protein S3ProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
Artenimol40S ribosomal protein S3aProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
Artenimol40S ribosomal protein S5, putativeProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
Artenimol60S ribosomal protein L10, putativeProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
Artenimol60S ribosomal protein L14, putativeProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
Artenimol60S ribosomal protein L17, putativeProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
Artenimol60S ribosomal protein L2ProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
Artenimol60S ribosomal protein L21ProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
Artenimol60S ribosomal protein L23ProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
Artenimol60S ribosomal protein L24, putativeProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
Artenimol60S ribosomal protein L27ProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
Artenimol60S ribosomal protein L3ProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
Artenimol60S ribosomal protein L30e, putativeProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
Artenimol60S ribosomal protein L4ProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolActin-1ProteinPlasmodium falciparum (isolate HB3)
Unknown
Ligand
Details
ArtenimolAcyl-CoA synthetaseProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolAdenosine deaminaseProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolAdenosylhomocysteinaseProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolAnamorsin homologProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolAspartate carbamoyltransferaseProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolATP-dependent RNA helicase UAP56ProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolAutophagy-related protein 18, putativeProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolCalcium-dependent protein kinase 4ProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolCalcium-transporting ATPaseProteinPlasmodium falciparum (isolate K1 / Thailand)
Unknown
Ligand
Details
ArtenimolcAMP-dependent protein kinase regulatory subunitProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolCarbamoyl phosphate synthetaseProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolCasein kinase 2, alpha subunitProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolCell division cycle protein 48 homologue,putativeProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolChaperone, putativeProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolChloroquine resistance transporterProteinPlasmodium falciparum
Unknown
Ligand
Details
ArtenimolCoatomer alpha subunit, putativeProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolConserved Plasmodium membrane proteinProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolDipeptidyl aminopeptidase 1ProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolDnaJ protein, putativeProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolElongation factor 1-alphaProteinPlasmodium falciparum (isolate K1 / Thailand)
Unknown
Ligand
Details
ArtenimolElongation factor 1-gamma, putativeProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolElongation factor 2ProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolEndoplasmin homolog, putativeProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolEnolaseProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolEukaryotic initiation factor 4AProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolEukaryotic translation initiation factor 3 subunit CProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolFructose-bisphosphate aldolaseProteinPlasmodium falciparum
Unknown
Ligand
Details
ArtenimolGlutamate dehydrogenaseProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolGlutamate--tRNA ligaseProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolGlutamine synthetase, putativeProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolGlyceraldehyde-3-phosphate dehydrogenaseProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolGlycophorin-binding proteinProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolGTP-binding nuclear protein RanProteinPlasmodium falciparum
Unknown
Ligand
Details
ArtenimolHaloacid dehalogenase-like hydrolaseProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolHAP proteinProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolHeat shock protein 110, putativeProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolHeat shock protein 90ProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolHexokinaseProteinPlasmodium falciparum
Unknown
Ligand
Details
ArtenimolHigh molecular weight rhoptry protein 2ProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolHSP40, subfamily A, putativeProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolHypoxanthine-guanine-xanthine phosphoribosyltransferaseProteinPlasmodium falciparum (isolate FCR-3 / Gambia)
Unknown
Ligand
Details
ArtenimolImportin subunit alphaProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolImportin-7, putativeProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolInner membrane complex sub-compartment protein 3ProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolInsulinase, putativeProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolIsoleucine--tRNA ligase, putativeProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolKnob-associated histidine-rich proteinProteinPlasmodium falciparum
Unknown
Ligand
Details
ArtenimolL-lactate dehydrogenaseProteinPlasmodium falciparum (isolate CDC / Honduras)
Unknown
Ligand
Details
ArtenimolLysophospholipase, putativeProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolMature parasite-infected erythrocyte surface antigenProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolMerozoite surface protein 1ProteinPlasmodium falciparum (isolate CDC / Honduras)
Unknown
Ligand
Details
ArtenimolMethionine--tRNA ligaseProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolMultidrug resistance proteinProteinPlasmodium falciparum (isolate FC27 / Papua New Guinea)
Unknown
Ligand
Details
ArtenimolNon-SERCA-type Ca2+-transporting P-ATPaseProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolNucleoside transporter 2ProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolOrnithine aminotransferaseProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolParasite-infected erythrocyte surface proteinProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolPeptidyl-prolyl cis-trans isomeraseProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolPhosphoethanolamine N-methyltransferaseProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolPhosphoribosylpyrophosphate synthetaseProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolPlasmepsin IVProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolPlasmepsin-1ProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolPlasmepsin-2ProteinPlasmodium falciparum
Unknown
Ligand
Details
ArtenimolPlasmodium exported proteinProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolPolyadenylate-binding proteinProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolProbable ATP-dependent 6-phosphofructokinaseProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolProteasome subunit alpha typeProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolProtein disulfide-isomeraseProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolProtein transport protein SEC31ProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolPurine nucleotide phosphorylase, putativeProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolPyridoxal 5'-phosphate synthase subunit Pdx1ProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolPyruvate kinaseProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolRhoptry neck protein 3ProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolRing-infected erythrocyte surface antigenProteinPlasmodium falciparum (isolate FC27 / Papua New Guinea)
Unknown
Ligand
Details
ArtenimolS-adenosylmethionine synthaseProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolSec62, putativeProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolSerine repeat antigen 5ProteinPlasmodium falciparum
Unknown
Ligand
Details
ArtenimolSignal recognition particle receptor, beta subunitProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolSkeleton-binding protein 1ProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolSpermidine synthaseProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolT-complex protein 1 subunit etaProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolThioredoxin peroxidase 1ProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolThioredoxin-like proteinProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolThioredoxin-related protein, putativeProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolThreonine--tRNA ligaseProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolTubulin alpha chainProteinPlasmodium falciparum (isolate K1 / Thailand)
Unknown
Ligand
Details
ArtenimolTubulin beta chainProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolUbiquitin-60S ribosomal protein L40ProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolUbiquitin-conjugating enzyme E2ProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolV-type H(+)-translocating pyrophosphatase, putativeProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details
ArtenimolV-type proton ATPase catalytic subunit AProteinPlasmodium falciparum (isolate 3D7)
Unknown
Ligand
Details