Artemisinin-resistant Plasmodium falciparum parasites exhibit altered patterns of development in infected erythrocytes

Antimicrobial Agents and Chemotherapy

Volumn 59, Issue 6, 2015, Pages 3156-3167

  Hott, Amanda ^a   Casandra, Debora ^b   Sparks, Kansas N ^b   Morton, Lindsay C ^b,c   Castanares, Geocel Grace ^b   Rutter, Amanda ^b,d   Kyle, Dennis E ^b  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

^b UNIVERSITY OF SOUTH FLORIDA   (United States)

^c UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^d FLORIDA HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTEMISININ; ANTIPROTOZOAL AGENT; ARTEMISININ DERIVATIVE; HYPOXANTHINE;

ANTIMALARIAL DRUG RESISTANCE; ARTICLE; CELL CYCLE REGULATION; CONTROLLED STUDY; CRYOPRESERVATION; DRUG EFFECT; DRUG EXPOSURE; DRUG SENSITIVITY; ERYTHROCYTE; GENE MUTATION; HALF LIFE TIME; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PARASITE CLEARANCE; PARASITE DEVELOPMENT; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; SCHIZONT; TROPHOZOITE; CELL CULTURE; DRUG EFFECTS; DRUG RESISTANCE; PARASITOLOGY; PATHOGENICITY; SINGLE NUCLEOTIDE POLYMORPHISM;

ANTIPROTOZOAL AGENTS; ARTEMISININS; CELLS, CULTURED; DRUG RESISTANCE; ERYTHROCYTES; HUMANS; HYPOXANTHINE; PARASITIC SENSITIVITY TESTS; PLASMODIUM FALCIPARUM; POLYMORPHISM, SINGLE NUCLEOTIDE;

EID: 84943782868     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.00197-15     Document Type: Article

References (27)

1. Ashley EA, Dhorda M, Fairhurst RM, Amaratunga C, Lim P, Suon S, Sreng S, Anderson JM, Mao S, Sam B, Sopha C, Chuor CM, Nguon C, Sovannaroth S, Pukrittayakamee S, Jittamala P, Chotivanich K, Chutasmit K, Suchatsoonthorn C, Runcharoen R, Hien TT, Thuy-Nhien NT, Thanh NV, Phu NH, Htut Y, Han KT, Aye KH, Mokuolu OA, Olaosebikan RR, Folaranmi OO, Mayxay M, Khanthavong M, Hongvanthong B, Newton PN, Onyamboko MA, Fanello CI, Tshefu AK, Mishra N, Valecha N, Phyo AP, Nosten F, Yi P, Tripura R, Borrmann S, Bashraheil M, Peshu J, Faiz MA, Ghose A, Hossain MA, Samad R, et al. 2014. Spread of artemisinin resistance in Plasmodium falciparum malaria. N Engl J Med 371:411-423. http://dx.doi.org/10.1056/NEJMoa1314981.
2. Ariey F, Witkowski B, Amaratunga C, Beghain J, Langlois AC, Khim N, Kim S, Duru V, Bouchier C, Ma L, Lim P, Leang R, Duong S, Sreng S, Suon S, Chuor CM, Bout DM, Menard S, Rogers WO, Genton B, Fandeur T, Miotto O, Ringwald P, Le Bras J, Berry A, Barale JC, Fairhurst RM, Benoit-Vical F, Mercereau-Puijalon O, Menard D. 2014. A molecular marker of artemisinin-resistant Plasmodium falciparum malaria. Nature 505:50-55. http://dx.doi.org/10.1038/nature12876.
3. Takala-Harrison S, Jacob CG, Arze C, Cummings MP, Silva JC, Dondorp AM, Fukuda MM, Hien TT, Mayxay M, Noedl H, Nosten F, Kyaw MP, Nhien NT, Imwong M, Bethell D, Se Y, Lon C, Tyner SD, Saunders DL, Ariey F, Mercereau-Puijalon O, Menard D, Newton PN, Khanthavong M, Hongvanthong B, Starzengruber P, Fuehrer HP, Swoboda P, Khan WA, Phyo AP, Nyunt MM, Nyunt MH, Brown TS, Adams M, Pepin CS, Bailey J, Tan JC, Ferdig MT, Clark TG, Miotto O, MacInnis B, Kwiatkowski DP, White NJ, Ringwald P, Plowe CV. 2014. Independent emergence of artemisinin resistance mutations among Plasmodium falciparum in southeast Asia. J Infect Dis http://dx.doi.org/10.1093/infdis/jiu491.
4. Wootton JC, Feng X, Ferdig MT, Cooper RA, Mu J, Baruch DI, Magill AJ, Su XZ. 2002. Genetic diversity and chloroquine selective sweeps in Plasmodium falciparum. Nature 418:320-323. http://dx.doi.org/10.1038/nature00813.
5. Roper C, Pearce R, Bredenkamp B, Gumede J, Drakeley C, Mosha F, Chandramohan D, Sharp B. 2003. Antifolate antimalarial resistance in southeast Africa: a population-based analysis. Lancet 361:1174-1181. http://dx.doi.org/10.1016/S0140-6736(03)12951-0.
6. Nair S, Williams JT, Brockman A, Paiphun L, Mayxay M, Newton PN, Guthmann JP, Smithuis FM, Hien TT, White NJ, Nosten F, Anderson TJ. 2003. A selective sweep driven by pyrimethamine treatment in southeast Asian malaria parasites. Mol Biol Evol 20:1526-1536. http://dx.doi.org/10.1093/molbev/msg162.
7. Dondorp AM, Nosten F, Yi P, Das D, Phyo AP, Tarning J, Lwin KM, Ariey F, Hanpithakpong W, Lee SJ, Ringwald P, Silamut K, Imwong M, Chotivanich K, Lim P, Herdman T, An SS, Yeung S, Singhasivanon P, Day NP, Lindegardh N, Socheat D, White NJ. 2009. Artemisinin resistance in Plasmodium falciparum malaria. N Engl J Med 361:455-467. http://dx.doi.org/10.1056/NEJMoa0808859.
8. Tucker MS, Mutka T, Sparks K, Patel J, Kyle DE. 2012. Phenotypic and genotypic analysis of in vitro-selected artemisinin-resistant progeny of Plasmodium falciparum. Antimicrob Agents Chemother 56:302-314. http://dx.doi.org/10.1128/AAC.05540-11.
9. Witkowski B, Khim N, Chim P, Kim S, Ke S, Kloeung N, Chy S, Duong S, Leang R, Ringwald P, Dondorp AM, Tripura R, Benoit-Vical F, Berry A, Gorgette O, Ariey F, Barale JC, Mercereau-Puijalon O, Menard D. 2013. Reduced artemisinin susceptibility of Plasmodium falciparum ring stages in western Cambodia. Antimicrob Agents Chemother 57:914-923. http://dx.doi.org/10.1128/AAC.01868-12.
10. Trager W, Jensen JB. 1976. Human malaria parasites in continuous culture. Science 193:673-675. http://dx.doi.org/10.1126/science.781840.
11. Rosario V. 1981. Cloning of naturally occurring mixed infections of malaria parasites. Science 212:1037-1038. http://dx.doi.org/10.1126/science.7015505.
12. Desjardins RE, Canfield CJ, Haynes JD, Chulay JD. 1979. Quantitative assessment of antimalarial activity in vitro by a semiautomated microdilution technique. Antimicrob Agents Chemother 16:710-718. http://dx.doi.org/10.1128/AAC.16.6.710.
13. Balu B, Singh N, Maher SP, Adams JH. 2010. A genetic screen for attenuated growth identifies genes crucial for intraerythrocytic development of Plasmodium falciparum. PLoS One 5:e13282. http://dx.doi.org/10.1371/journal.pone.0013282.
14. Sanz LM, Crespo B, De-Cozar C, Ding XC, Llergo JL, Burrows JN, Garcia-Bustos JF, Gamo FJ. 2012. P. falciparum in vitro killing rates allow to discriminate between different antimalarial mode-of-action. PLoS One 7:e30949. http://dx.doi.org/10.1371/journal.pone.0030949.
15. Rosenthal PJ. 2013. The interplay between drug resistance and fitness in malaria parasites. Mol Microbiol 89:1025-1038. http://dx.doi.org/10.1111/mmi.12349.
16. Chotivanich K, Tripura R, Das D, Yi P, Day NP, Pukrittayakamee S, Chuor CM, Socheat D, Dondorp AM, White NJ. 2014. Laboratory detection of artemisinin-resistant Plasmodium falciparum. Antimicrob Agents Chemother 58:3157-3161. http://dx.doi.org/10.1128/AAC.01924-13.
17. Cheeseman IH, Miller BA, Nair S, Nkhoma S, Tan A, Tan JC, Al Saai S, Phyo AP, Moo CL, Lwin KM, McGready R, Ashley E, Imwong M, Stepniewska K, Yi P, Dondorp AM, Mayxay M, Newton PN, White NJ, Nosten F, Ferdig MT, Anderson TJ. 2012. A major genome region underlying artemisinin resistance in malaria. Science 336:79-82. http://dx.doi.org/10.1126/science.1215966.
18. Takala-Harrison S, Clark TG, Jacob CG, Cummings MP, Miotto O, Dondorp AM, Fukuda MM, Nosten F, Noedl H, Imwong M, Bethell D, Se Y, Lon C, Tyner SD, Saunders DL, Socheat D, Ariey F, Phyo AP, Starzengruber P, Fuehrer HP, Swoboda P, Stepniewska K, Flegg J, Arze C, Cerqueira GC, Silva JC, Ricklefs SM, Porcella SF, Stephens RM, Adams M, Kenefic LJ, Campino S, Auburn S, MacInnis B, Kwiatkowski DP, Su XZ, White NJ, Ringwald P, Plowe CV. 2013. Genetic loci associated with delayed clearance of Plasmodium falciparum following artemisinin treatment in southeast Asia. Proc Natl Acad Sci U S A 110: 240-245. http://dx.doi.org/10.1073/pnas.1211205110.
19. Teuscher F, Chen N, Kyle DE, Gatton ML, Cheng Q. 2012. Phenotypic changes in artemisinin-resistant plasmodium falciparum lines in vitro: evidence for decreased sensitivity to dormancy and growth inhibition. Antimicrob Agents Chemother 56:428-431. http://dx.doi.org/10.1128/AAC.05456-11.
20. Miotto O, Almagro-Garcia J, Manske M, Macinnis B, Campino S, Rockett KA, Amaratunga C, Lim P, Suon S, Sreng S, Anderson JM, Duong S, Nguon C, Chuor CM, Saunders D, Se Y, Lon C, Fukuda MM, Amenga-Etego L, Hodgson AV, Asoala V, Imwong M, Takala-Harrison S, Nosten F, Su XZ, Ringwald P, Ariey F, Dolecek C, Hien TT, Boni MF, Thai CQ, Amambua-Ngwa A, Conway DJ, Djimde AA, Doumbo OK, Zongo I, Ouedraogo JB, Alcock D, Drury E, Auburn S, Koch O, Sanders M, Hubbart C, Maslen G, Ruano-Rubio V, Jyothi D, Miles A, O'Brien J, Gamble C, Oyola SO, Rayner JC, Newbold CI, Berriman M, Spencer CC, McVean G, Day NP, White NJ, Bethell D, Dondorp AM, Plowe CV, Fairhurst RM, Kwiatkowski DP. 2013. Multiple populations of artemisinin-resistant Plasmodium falciparum in Cambodia. Nat Genet 45:648-655. http://dx.doi.org/10.1038/ng.2624.
21. Hopperus Buma AP, van Thiel PP, Lobel HO, Ohrt C, van Ameijden EJ, Veltink RL, Tendeloo DC, van Gool T, Green MD, Todd GD, Kyle DE, Kager PA. 1996. Long-term malaria chemoprophylaxis with mefloquine in Dutch marines in Cambodia. J Infect Dis 173:1506-1509. http://dx.doi.org/10.1093/infdis/173.6.1506.
22. Klonis N, Xie SC, McCaw JM, Crespo-Ortiz MP, Zaloumis SG, Simpson JA, Tilley L. 2013. Altered temporal response of malaria parasites determines differential sensitivity to artemisinin. Proc Natl Acad SciUSA 110:5157-5162. http://dx.doi.org/10.1073/pnas.1217452110.
23. Mok S, Ashley EA, Ferreira PE, Zhu L, Lin Z, Yeo T, Chotivanich K, Imwong M, Pukrittayakamee S, Dhorda M, Nguon C, Lim P, Amaratunga C, Suon S, Hien TT, Htut Y, Faiz MA, Onyamboko MA, Mayxay M, Newton PN, Tripura R, Woodrow CJ, Miotto O, Kwiatkowski DP, Nosten F, Day NP, Preiser PR, White NJ, Dondorp AM, Fairhurst RM, Bozdech Z. 2014. Population transcriptomics of human malaria parasites reveals the mechanism of artemisinin resistance. Science 347:431-435. http://dx.doi.org/10.1126/science.1260403.
24. Witkowski B, Amaratunga C, Khim N, Sreng S, Chim P, Kim S, Lim P, Mao S, Sopha C, Sam B, Anderson JM, Duong S, Chuor CM, Taylor WR, Suon S, Mercereau-Puijalon O, Fairhurst RM, Menard D. 2013. Novel phenotypic assays for the detection of artemisinin-resistant Plasmodium falciparum malaria in Cambodia: in-vitro and ex-vivo drugresponse studies. Lancet Infect Dis 13:1043-1049. http://dx.doi.org/10.1016/S1473-3099(13)70252-4.
25. Straimer J, Gnadig NF, Witkowski B, Amaratunga C, Duru V, Ramadani AP, Dacheux M, Khim N, Zhang L, Lam S, Gregory PD, Urnov FD, Mercereau-Puijalon O, Benoit-Vical F, Fairhurst RM, Menard D, Fidock DA. 2014. K13-propeller mutations confer artemisinin resistance in Plasmodium falciparum clinical isolates. Science http://dx.doi.org/10.1126/science.1260867.
26. Ghorbal M, Gorman M, Macpherson CR, Martins RM, Scherf A, Lopez-Rubio JJ. 2014. Genome editing in the human malaria parasite Plasmodium falciparum using the CRISPR-Cas9 system. Nat Biotechnol 32:819-821. http://dx.doi.org/10.1038/nbt.2925.
27. Lim P, Wongsrichanalai C, Chim P, Khim N, Kim S, Chy S, Sem R, Nhem S, Yi P, Duong S, Bouth DM, Genton B, Beck HP, Gobert JG, Rogers WO, Coppee JY, Fandeur T, Mercereau-Puijalon O, Ringwald P, Le Bras J, Ariey F. 2010. Decreased in vitro susceptibility of Plasmodium falciparum isolates to artesunate, mefloquine, chloroquine, and quinine in Cambodia from 2001 to 2007. Antimicrob Agents Chemother 54:2135-2142. http://dx.doi.org/10.1128/AAC.01304-09.