Skip to main content
Top
Published in: Malaria Journal 1/2016

Open Access 01-12-2016 | Research

Limited genetic diversity in the PvK12 Kelch protein in Plasmodium vivax isolates from Southeast Asia

Authors: Meilian Wang, Faiza Amber Siddiqui, Qi Fan, Enjie Luo, Yaming Cao, Liwang Cui

Published in: Malaria Journal | Issue 1/2016

Login to get access

Abstract

Background

Artemisinin resistance in Plasmodium falciparum has emerged as a major threat for malaria control and elimination worldwide. Mutations in the Kelch propeller domain of PfK13 are the only known molecular markers for artemisinin resistance in this parasite. Over 100 non-synonymous mutations have been identified in PfK13 from various malaria endemic regions. This study aimed to investigate the genetic diversity of PvK12, the Plasmodium vivax ortholog of PfK13, in parasite populations from Southeast Asia, where artemisinin resistance in P. falciparum has emerged.

Methods

The PvK12 sequences in 120 P. vivax isolates collected from Thailand (22), Myanmar (32) and China (66) between 2004 and 2008 were obtained and 353 PvK12 sequences from worldwide populations were retrieved for further analysis.

Results

These PvK12 sequences revealed a very low level of genetic diversity (π = 0.00003) with only three single nucleotide polymorphisms (SNPs). Of these three SNPs, only G581R is nonsynonymous. The synonymous mutation S88S is present in 3% (1/32) of the Myanmar samples, while G704G and G581R are present in 1.5% (1/66) and 3% (2/66) of the samples from China, respectively. None of the mutations observed in the P. vivax samples were associated with artemisinin resistance in P. falciparum. Furthermore, analysis of 473 PvK12 sequences from twelve worldwide P. vivax populations confirmed the very limited polymorphism in this gene and detected only five distinct haplotypes.

Conclusions

The PvK12 sequences from global P. vivax populations displayed very limited genetic diversity indicating low levels of baseline polymorphisms of PvK12 in these areas.
Appendix
Available only for authorised users
Literature
1.
go back to reference Delacollette C, D’Souza C, Christophel E, Thimasarn K, Abdur R, Bell D, et al. Malaria trends and challenges in the Greater Mekong Subregion. Southeast Asian J Trop Med Public Health. 2009;40:674–91.PubMed Delacollette C, D’Souza C, Christophel E, Thimasarn K, Abdur R, Bell D, et al. Malaria trends and challenges in the Greater Mekong Subregion. Southeast Asian J Trop Med Public Health. 2009;40:674–91.PubMed
2.
go back to reference Noedl H, Se Y, Schaecher K, Smith BL, Socheat D, Fukuda MM, et al. Evidence of artemisinin-resistant malaria in western Cambodia. N Engl J Med. 2008;359:2619–20.CrossRefPubMed Noedl H, Se Y, Schaecher K, Smith BL, Socheat D, Fukuda MM, et al. Evidence of artemisinin-resistant malaria in western Cambodia. N Engl J Med. 2008;359:2619–20.CrossRefPubMed
3.
go back to reference Dondorp AM, Nosten F, Yi P, Das D, Phyo AP, Tarning J, et al. Artemisinin resistance in Plasmodium falciparum malaria. N Engl J Med. 2009;361:455–67.CrossRefPubMedPubMedCentral Dondorp AM, Nosten F, Yi P, Das D, Phyo AP, Tarning J, et al. Artemisinin resistance in Plasmodium falciparum malaria. N Engl J Med. 2009;361:455–67.CrossRefPubMedPubMedCentral
4.
go back to reference Phyo AP, Nkhoma S, Stepniewska K, Ashley EA, Nair S, McGready R, et al. Emergence of artemisinin-resistant malaria on the western border of Thailand: a longitudinal study. Lancet. 2012;379:1960–6.CrossRefPubMedPubMedCentral Phyo AP, Nkhoma S, Stepniewska K, Ashley EA, Nair S, McGready R, et al. Emergence of artemisinin-resistant malaria on the western border of Thailand: a longitudinal study. Lancet. 2012;379:1960–6.CrossRefPubMedPubMedCentral
5.
go back to reference Hien TT, Thuy-Nhien NT, Phu NH, Boni MF, Thanh NV, Nha-Ca NT, et al. In vivo susceptibility of Plasmodium falciparum to artesunate in Binh Phuoc Province Vietnam. Malar J. 2012;11:355.CrossRefPubMedPubMedCentral Hien TT, Thuy-Nhien NT, Phu NH, Boni MF, Thanh NV, Nha-Ca NT, et al. In vivo susceptibility of Plasmodium falciparum to artesunate in Binh Phuoc Province Vietnam. Malar J. 2012;11:355.CrossRefPubMedPubMedCentral
6.
go back to reference Kyaw MP, Nyunt MH, Chit K, Aye MM, Aye KH, Aye MM, et al. Reduced susceptibility of Plasmodium falciparum to artesunate in southern Myanmar. PLoS ONE. 2013;8:e57689.CrossRefPubMedPubMedCentral Kyaw MP, Nyunt MH, Chit K, Aye MM, Aye KH, Aye MM, et al. Reduced susceptibility of Plasmodium falciparum to artesunate in southern Myanmar. PLoS ONE. 2013;8:e57689.CrossRefPubMedPubMedCentral
7.
go back to reference Ariey F, Witkowski B, Amaratunga C, Beghain J, Langlois AC, Khim N, et al. A molecular marker of artemisinin-resistant Plasmodium falciparum malaria. Nature. 2014;505:50–5.CrossRefPubMed Ariey F, Witkowski B, Amaratunga C, Beghain J, Langlois AC, Khim N, et al. A molecular marker of artemisinin-resistant Plasmodium falciparum malaria. Nature. 2014;505:50–5.CrossRefPubMed
8.
go back to reference Adams J, Kelso R, Cooley L. The kelch repeat superfamily of proteins: propellers of cell function. Trends Cell Biol. 2000;10:17–24.CrossRefPubMed Adams J, Kelso R, Cooley L. The kelch repeat superfamily of proteins: propellers of cell function. Trends Cell Biol. 2000;10:17–24.CrossRefPubMed
10.
go back to reference Mok S, Ashley EA, Ferreira PE, Zhu L, Lin Z, Yeo T, et al. Drug resistance. Population transcriptomics of human malaria parasites reveals the mechanism of artemisinin resistance. Science. 2015;347:431–5.CrossRefPubMed Mok S, Ashley EA, Ferreira PE, Zhu L, Lin Z, Yeo T, et al. Drug resistance. Population transcriptomics of human malaria parasites reveals the mechanism of artemisinin resistance. Science. 2015;347:431–5.CrossRefPubMed
11.
go back to reference 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:e1002132.CrossRefPubMedPubMedCentral 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:e1002132.CrossRefPubMedPubMedCentral
12.
go back to reference 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;520:683–7.CrossRefPubMedPubMedCentral 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;520:683–7.CrossRefPubMedPubMedCentral
13.
go back to reference Straimer J, Gnadig NF, Witkowski B, Amaratunga C, Duru V, Ramadani AP, et al. Drug resistance. K13-propeller mutations confer artemisinin resistance in Plasmodium falciparum clinical isolates. Science. 2015;347:428–31.CrossRefPubMed Straimer J, Gnadig NF, Witkowski B, Amaratunga C, Duru V, Ramadani AP, et al. Drug resistance. K13-propeller mutations confer artemisinin resistance in Plasmodium falciparum clinical isolates. Science. 2015;347:428–31.CrossRefPubMed
14.
go back to reference Wang Z, Wang Y, Cabrera M, Zhang Y, Gupta B, Wu Y, et al. Artemisinin resistance at the China-Myanmar border and association with mutations in the K13 propeller gene. Antimicrob Agents Chemother. 2015;59:6952–9.CrossRefPubMedPubMedCentral Wang Z, Wang Y, Cabrera M, Zhang Y, Gupta B, Wu Y, et al. Artemisinin resistance at the China-Myanmar border and association with mutations in the K13 propeller gene. Antimicrob Agents Chemother. 2015;59:6952–9.CrossRefPubMedPubMedCentral
15.
go back to reference Leang R, Taylor WR, Bouth DM, Song L, Tarning J, Char MC, et al. Evidence of Plasmodium falciparum malaria multidrug resistance to artemisinin and piperaquine in Western Cambodia: dihydroartemisinin–piperaquine open-label multicenter clinical assessment. Antimicrob Agents Chemother. 2015;59:4719–26.CrossRefPubMedPubMedCentral Leang R, Taylor WR, Bouth DM, Song L, Tarning J, Char MC, et al. Evidence of Plasmodium falciparum malaria multidrug resistance to artemisinin and piperaquine in Western Cambodia: dihydroartemisinin–piperaquine open-label multicenter clinical assessment. Antimicrob Agents Chemother. 2015;59:4719–26.CrossRefPubMedPubMedCentral
16.
go back to reference Win AA, Imwong M, Kyaw MP, Woodrow CJ, Chotivanich K, Hanboonkunupakarn B, et al. K13 mutations and pfmdr1 copy number variation in Plasmodium falciparum malaria in Myanmar. Malar J. 2016;15:110.CrossRefPubMedPubMedCentral Win AA, Imwong M, Kyaw MP, Woodrow CJ, Chotivanich K, Hanboonkunupakarn B, et al. K13 mutations and pfmdr1 copy number variation in Plasmodium falciparum malaria in Myanmar. Malar J. 2016;15:110.CrossRefPubMedPubMedCentral
17.
go back to reference Nyunt MH, Hlaing T, Oo HW, Tin-Oo LL, Phway HP, Wang B, et al. Molecular assessment of artemisinin resistance markers, polymorphisms in the k13 propeller, and a multidrug-resistance gene in the eastern and western border areas of Myanmar. Clin Infect Dis. 2015;60:1208–15.CrossRefPubMed Nyunt MH, Hlaing T, Oo HW, Tin-Oo LL, Phway HP, Wang B, et al. Molecular assessment of artemisinin resistance markers, polymorphisms in the k13 propeller, and a multidrug-resistance gene in the eastern and western border areas of Myanmar. Clin Infect Dis. 2015;60:1208–15.CrossRefPubMed
18.
go back to reference Thriemer K, Hong NV, Rosanas-Urgell A, Phuc BQ, Ha M, Pockele E, et al. Delayed parasite clearance after treatment with dihydroartemisinin–piperaquine in Plasmodium falciparum malaria patients in central Vietnam. Antimicrob Agents Chemother. 2014;58:7049–55.CrossRefPubMedPubMedCentral Thriemer K, Hong NV, Rosanas-Urgell A, Phuc BQ, Ha M, Pockele E, et al. Delayed parasite clearance after treatment with dihydroartemisinin–piperaquine in Plasmodium falciparum malaria patients in central Vietnam. Antimicrob Agents Chemother. 2014;58:7049–55.CrossRefPubMedPubMedCentral
19.
go back to reference Putaporntip C, Kuamsab N, Kosuwin R, Tantiwattanasub W, Vejakama P, Sueblinvong T, et al. Natural selection of K13 mutants of Plasmodium falciparum in response to artemisinin combination therapies in Thailand. Clin Microbiol Infect. 2016;22:285.CrossRefPubMed Putaporntip C, Kuamsab N, Kosuwin R, Tantiwattanasub W, Vejakama P, Sueblinvong T, et al. Natural selection of K13 mutants of Plasmodium falciparum in response to artemisinin combination therapies in Thailand. Clin Microbiol Infect. 2016;22:285.CrossRefPubMed
20.
go back to reference Isozumi R, Uemura H, Kimata I, Ichinose Y, Logedi J, Omar AH, et al. Novel mutations in K13 propeller gene of artemisinin-resistant Plasmodium falciparum. Emerg Infect Dis. 2015;21:490–2.CrossRefPubMedPubMedCentral Isozumi R, Uemura H, Kimata I, Ichinose Y, Logedi J, Omar AH, et al. Novel mutations in K13 propeller gene of artemisinin-resistant Plasmodium falciparum. Emerg Infect Dis. 2015;21:490–2.CrossRefPubMedPubMedCentral
21.
go back to reference Talundzic E, Okoth SA, Congpuong K, Plucinski MM, Morton L, Goldman IF. Selection and spread of artemisinin-resistant alleles in Thailand prior to the global artemisinin resistance containment campaign. PLoS Pathog. 2015;11:1004789.CrossRef Talundzic E, Okoth SA, Congpuong K, Plucinski MM, Morton L, Goldman IF. Selection and spread of artemisinin-resistant alleles in Thailand prior to the global artemisinin resistance containment campaign. PLoS Pathog. 2015;11:1004789.CrossRef
22.
go back to reference Ashley EA, Dhorda M, Fairhurst RM, Amaratunga C, Lim P, Suon S, et al. Spread of artemisinin resistance in Plasmodium falciparum malaria. N Engl J Med. 2014;371:411–23.CrossRefPubMedPubMedCentral Ashley EA, Dhorda M, Fairhurst RM, Amaratunga C, Lim P, Suon S, et al. Spread of artemisinin resistance in Plasmodium falciparum malaria. N Engl J Med. 2014;371:411–23.CrossRefPubMedPubMedCentral
23.
go back to reference Menard D, Khim N, Beghain J, Adegnika AA, Shafiul-Alam M, Amodu O, et al. A worldwide map of Plasmodium falciparum K13-Propeller polymorphisms. N Engl J Med. 2016;374:2453–64.CrossRefPubMed Menard D, Khim N, Beghain J, Adegnika AA, Shafiul-Alam M, Amodu O, et al. A worldwide map of Plasmodium falciparum K13-Propeller polymorphisms. N Engl J Med. 2016;374:2453–64.CrossRefPubMed
24.
go back to reference Conrad MD, Bigira V, Kapisi J, Muhindo M, Kamya MR, Havlir DV, et al. Polymorphisms in K13 and falcipain-2 associated with artemisinin resistance are not prevalent in Plasmodium falciparum isolated from Ugandan children. PLoS ONE. 2014;9:e105690.CrossRefPubMedPubMedCentral Conrad MD, Bigira V, Kapisi J, Muhindo M, Kamya MR, Havlir DV, et al. Polymorphisms in K13 and falcipain-2 associated with artemisinin resistance are not prevalent in Plasmodium falciparum isolated from Ugandan children. PLoS ONE. 2014;9:e105690.CrossRefPubMedPubMedCentral
25.
go back to reference Kamau E, Campino S, Amenga-Etego L, Drury E, Ishengoma D, Johnson K, et al. K13-propeller polymorphisms in Plasmodium falciparum parasites from sub-Saharan Africa. J Infect Dis. 2015;211:1352–5.PubMed Kamau E, Campino S, Amenga-Etego L, Drury E, Ishengoma D, Johnson K, et al. K13-propeller polymorphisms in Plasmodium falciparum parasites from sub-Saharan Africa. J Infect Dis. 2015;211:1352–5.PubMed
26.
go back to reference Taylor SM, Parobek CM, DeConti DK, Kayentao K, Coulibaly SO, Greenwood BM, et al. Absence of putative artemisinin resistance mutations among Plasmodium falciparum in sub-Saharan Africa: a molecular epidemiologic study. J Infect Dis. 2015;211:680–8.CrossRefPubMed Taylor SM, Parobek CM, DeConti DK, Kayentao K, Coulibaly SO, Greenwood BM, et al. Absence of putative artemisinin resistance mutations among Plasmodium falciparum in sub-Saharan Africa: a molecular epidemiologic study. J Infect Dis. 2015;211:680–8.CrossRefPubMed
29.
go back to reference Snounou G, Viriyakosol S, Jarra W, Thaithong S, Brown KN. Identification of the four human malaria parasite species in field samples by the polymerase chain reaction and detection of a high prevalence of mixed infections. Mol Biochem Parasitol. 1993;58:283–92.CrossRefPubMed Snounou G, Viriyakosol S, Jarra W, Thaithong S, Brown KN. Identification of the four human malaria parasite species in field samples by the polymerase chain reaction and detection of a high prevalence of mixed infections. Mol Biochem Parasitol. 1993;58:283–92.CrossRefPubMed
30.
31.
go back to reference Gogtay N, Kannan S, Thatte UM, Olliaro PL, Sinclair D. Artemisinin-based combination therapy for treating uncomplicated Plasmodium vivax malaria. Cochrane Database Syst Rev. 2013;10:008492. Gogtay N, Kannan S, Thatte UM, Olliaro PL, Sinclair D. Artemisinin-based combination therapy for treating uncomplicated Plasmodium vivax malaria. Cochrane Database Syst Rev. 2013;10:008492.
32.
go back to reference Imwong M, Pukrittakayamee S, Looareesuwan S, Pasvol G, Poirreiz J, White NJ, et al. Association of genetic mutations in P. vivax dhfr with resistance to sulfadoxine-pyrimethamine: geographical and clinical correlates. Antimicrob Agents Chemother. 2001;45:3122–7.CrossRefPubMedPubMedCentral Imwong M, Pukrittakayamee S, Looareesuwan S, Pasvol G, Poirreiz J, White NJ, et al. Association of genetic mutations in P. vivax dhfr with resistance to sulfadoxine-pyrimethamine: geographical and clinical correlates. Antimicrob Agents Chemother. 2001;45:3122–7.CrossRefPubMedPubMedCentral
33.
go back to reference Barnadas C, Musset L, Legrand E, Tichit M, Briolant S, Fusai T, et al. High prevalence and fixation of Plasmodium vivax dhfr/dhps mutations related to sulfadoxine/pyrimethamine resistance in French Guiana. Am J Trop Med Hyg. 2009;81:19–22.PubMed Barnadas C, Musset L, Legrand E, Tichit M, Briolant S, Fusai T, et al. High prevalence and fixation of Plasmodium vivax dhfr/dhps mutations related to sulfadoxine/pyrimethamine resistance in French Guiana. Am J Trop Med Hyg. 2009;81:19–22.PubMed
34.
go back to reference Sidhu AB, Uhlemann AC, Valderramos SG, Valderramos JC, Krishna S, Fidock DA. Decreasing pfmdr1 copy number in Plasmodium falciparum malaria heightens susceptibility to mefloquine, lumefantrine, halofantrine, quinine, and artemisinin. J Infect Dis. 2006;15(194):528–35.CrossRef Sidhu AB, Uhlemann AC, Valderramos SG, Valderramos JC, Krishna S, Fidock DA. Decreasing pfmdr1 copy number in Plasmodium falciparum malaria heightens susceptibility to mefloquine, lumefantrine, halofantrine, quinine, and artemisinin. J Infect Dis. 2006;15(194):528–35.CrossRef
35.
go back to reference Popovici J, Kao S, Eal L, Bin S, Kim S, Menard D. Reduced polymorphism in the Kelch propeller domain in Plasmodium vivax isolates from Cambodia. Antimicrob Agents Chemother. 2015;59:730–3.CrossRefPubMed Popovici J, Kao S, Eal L, Bin S, Kim S, Menard D. Reduced polymorphism in the Kelch propeller domain in Plasmodium vivax isolates from Cambodia. Antimicrob Agents Chemother. 2015;59:730–3.CrossRefPubMed
36.
go back to reference Wongsrichanalai C, Prajakwong S, Meshnick SR, Shanks GD, Thimasarn K. Mefloquine–its 20 years in the Thai Malaria Control Program. Southeast Asian J Trop Med Public Health. 2004;35:300–8.PubMed Wongsrichanalai C, Prajakwong S, Meshnick SR, Shanks GD, Thimasarn K. Mefloquine–its 20 years in the Thai Malaria Control Program. Southeast Asian J Trop Med Public Health. 2004;35:300–8.PubMed
37.
go back to reference Nosten F, Luxemburger C, ter Kuile FO, Woodrow C, Eh JP, Chongsuphajaisiddhi T, et al. Treatment of multidrug-resistant Plasmodium falciparum malaria with 3-day artesunate–mefloquine combination. J Infect Dis. 1994;170:971–7.CrossRefPubMed Nosten F, Luxemburger C, ter Kuile FO, Woodrow C, Eh JP, Chongsuphajaisiddhi T, et al. Treatment of multidrug-resistant Plasmodium falciparum malaria with 3-day artesunate–mefloquine combination. J Infect Dis. 1994;170:971–7.CrossRefPubMed
39.
go back to reference Marchler-Bauer A, Derbyshire MK, Gonzales NR, Lu S, Chitsaz F, Geer LY, et al. CDD: NCBI’s conserved domain database. Nucleic Acids Res. 2015;43:D222–6.CrossRefPubMed Marchler-Bauer A, Derbyshire MK, Gonzales NR, Lu S, Chitsaz F, Geer LY, et al. CDD: NCBI’s conserved domain database. Nucleic Acids Res. 2015;43:D222–6.CrossRefPubMed
40.
42.
go back to reference Bandelt HJ, Forster P, Rohl A. Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol. 1999;16:37–48.CrossRefPubMed Bandelt HJ, Forster P, Rohl A. Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol. 1999;16:37–48.CrossRefPubMed
43.
go back to reference Nei M, Gojobori T. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol. 1986;3:418–26.PubMed Nei M, Gojobori T. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol. 1986;3:418–26.PubMed
44.
go back to reference Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics. 1989;123:585–95.PubMedPubMedCentral Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics. 1989;123:585–95.PubMedPubMedCentral
45.
go back to reference McDonald JH, Kreitman M. Adaptive protein evolution at the Adh locus in Drosophila. Nature. 1991;351:652–4.CrossRefPubMed McDonald JH, Kreitman M. Adaptive protein evolution at the Adh locus in Drosophila. Nature. 1991;351:652–4.CrossRefPubMed
46.
go back to reference Wellinger RE, Prado F, Aguilera A. Replication fork progression is impaired by transcription in hyperrecombinant yeast cells lacking a functional THO complex. Mol Cell Biol. 2006;26:3327–34.CrossRefPubMedPubMedCentral Wellinger RE, Prado F, Aguilera A. Replication fork progression is impaired by transcription in hyperrecombinant yeast cells lacking a functional THO complex. Mol Cell Biol. 2006;26:3327–34.CrossRefPubMedPubMedCentral
47.
go back to reference Garcia-Rubio M, Chavez S, Huertas P, Tous C, Jimeno S, Luna R. Different physiological relevance of yeast THO/TREX subunits in gene expression and genome integrity. Mol Genet Genomics. 2008;279:123–32.CrossRefPubMed Garcia-Rubio M, Chavez S, Huertas P, Tous C, Jimeno S, Luna R. Different physiological relevance of yeast THO/TREX subunits in gene expression and genome integrity. Mol Genet Genomics. 2008;279:123–32.CrossRefPubMed
48.
go back to reference Escalante AA, Freeland DE, Collins WE, Lal AA. The evolution of primate malaria parasites based on the gene encoding cytochrome b from the linear mitochondrial genome. Proc Natl Acad Sci USA. 1998;95:8124–9.CrossRefPubMedPubMedCentral Escalante AA, Freeland DE, Collins WE, Lal AA. The evolution of primate malaria parasites based on the gene encoding cytochrome b from the linear mitochondrial genome. Proc Natl Acad Sci USA. 1998;95:8124–9.CrossRefPubMedPubMedCentral
49.
go back to reference Zhang DD, 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. 2003;23:8137–51.CrossRefPubMedPubMedCentral Zhang DD, 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. 2003;23:8137–51.CrossRefPubMedPubMedCentral
50.
go back to reference Abed DA, Goldstein M, Albanyan H, Jin H, Hu L. Discovery of direct inhibitors of Keap1-Nrf2 protein–protein interaction as potential therapeutic and preventive agents. Acta Pharm Sin B. 2015;5:285–99.CrossRefPubMedPubMedCentral Abed DA, Goldstein M, Albanyan H, Jin H, Hu L. Discovery of direct inhibitors of Keap1-Nrf2 protein–protein interaction as potential therapeutic and preventive agents. Acta Pharm Sin B. 2015;5:285–99.CrossRefPubMedPubMedCentral
51.
go back to reference Rijken MJ, Boel ME, Russell B, Imwong M, Leimanis ML, Phyo AP. Chloroquine resistant vivax malaria in a pregnant woman on the western border of Thailand. Malar J. 2011;10:113.CrossRefPubMedPubMedCentral Rijken MJ, Boel ME, Russell B, Imwong M, Leimanis ML, Phyo AP. Chloroquine resistant vivax malaria in a pregnant woman on the western border of Thailand. Malar J. 2011;10:113.CrossRefPubMedPubMedCentral
52.
go back to reference Guthmann JP, Pittet A, Lesage A, Imwong M, Lindegardh N, Min Lwin M. Plasmodium vivax resistance to chloroquine in Dawei, southern Myanmar. Trop Med Int Health. 2008;13:91–8.CrossRefPubMed Guthmann JP, Pittet A, Lesage A, Imwong M, Lindegardh N, Min Lwin M. Plasmodium vivax resistance to chloroquine in Dawei, southern Myanmar. Trop Med Int Health. 2008;13:91–8.CrossRefPubMed
53.
go back to reference Yuan L, Wang Y, Parker DM, Gupta B, Yang Z, Liu H. Therapeutic responses of Plasmodium vivax malaria to chloroquine and primaquine treatment in northeastern Myanmar. Antimicrob Agents Chemother. 2015;59:1230–5.CrossRefPubMedPubMedCentral Yuan L, Wang Y, Parker DM, Gupta B, Yang Z, Liu H. Therapeutic responses of Plasmodium vivax malaria to chloroquine and primaquine treatment in northeastern Myanmar. Antimicrob Agents Chemother. 2015;59:1230–5.CrossRefPubMedPubMedCentral
54.
go back to reference Zhang DD, Lo SC, Cross JV, Templeton DJ, Hannink M. Keap1 is a redox-regulated substrate adaptor protein for a Cul3-dependent ubiquitin ligase complex. Mol Cell Biol. 2004;24:10941–53.CrossRefPubMedPubMedCentral Zhang DD, Lo SC, Cross JV, Templeton DJ, Hannink M. Keap1 is a redox-regulated substrate adaptor protein for a Cul3-dependent ubiquitin ligase complex. Mol Cell Biol. 2004;24:10941–53.CrossRefPubMedPubMedCentral
55.
go back to reference Nguyen T, Sherratt PJ, Pickett CB. Regulatory mechanisms controlling gene expression mediated by the antioxidant response element. Annu Rev Pharmacol Toxicol. 2003;43:233–60.CrossRefPubMed Nguyen T, Sherratt PJ, Pickett CB. Regulatory mechanisms controlling gene expression mediated by the antioxidant response element. Annu Rev Pharmacol Toxicol. 2003;43:233–60.CrossRefPubMed
56.
go back to reference Strasser K, Masuda S, Mason P, Pfannstiel J, Oppizzi M, Rodriguez-Navarro S, et al. TREX is a conserved complex coupling transcription with messenger RNA export. Nature. 2002;417:304–8.CrossRefPubMed Strasser K, Masuda S, Mason P, Pfannstiel J, Oppizzi M, Rodriguez-Navarro S, et al. TREX is a conserved complex coupling transcription with messenger RNA export. Nature. 2002;417:304–8.CrossRefPubMed
57.
go back to reference Turnbull EL, Martin IV, Fantes PA. Cdc37 maintains cellular viability in Schizosaccharomyces pombe independently of interactions with heat-shock protein 90. FEBS J. 2005;272:4129–40.CrossRefPubMed Turnbull EL, Martin IV, Fantes PA. Cdc37 maintains cellular viability in Schizosaccharomyces pombe independently of interactions with heat-shock protein 90. FEBS J. 2005;272:4129–40.CrossRefPubMed
58.
go back to reference Ouattara A, Kone A, Adams M, Fofana B, Maiga AW, Hampton S, et al. Polymorphisms in the K13-propeller gene in artemisinin-susceptible Plasmodium falciparum parasites from Bougoula-Hameau and Bandiagara, Mali. Am J Trop Med Hyg. 2015;92:1202–6.CrossRefPubMedPubMedCentral Ouattara A, Kone A, Adams M, Fofana B, Maiga AW, Hampton S, et al. Polymorphisms in the K13-propeller gene in artemisinin-susceptible Plasmodium falciparum parasites from Bougoula-Hameau and Bandiagara, Mali. Am J Trop Med Hyg. 2015;92:1202–6.CrossRefPubMedPubMedCentral
59.
go back to reference Mita T, Culleton R, Takahashi N, Nakamura M, Tsukahara T, Hunja CW, et al. Little polymorphism at the K13 propeller locus in worldwide Plasmodium falciparum populations prior to the introduction of artemisinin combination therapies. Antimicrob Agents Chemother. 2016;60:3340–7.CrossRefPubMed Mita T, Culleton R, Takahashi N, Nakamura M, Tsukahara T, Hunja CW, et al. Little polymorphism at the K13 propeller locus in worldwide Plasmodium falciparum populations prior to the introduction of artemisinin combination therapies. Antimicrob Agents Chemother. 2016;60:3340–7.CrossRefPubMed
Metadata
Title
Limited genetic diversity in the PvK12 Kelch protein in Plasmodium vivax isolates from Southeast Asia
Authors
Meilian Wang
Faiza Amber Siddiqui
Qi Fan
Enjie Luo
Yaming Cao
Liwang Cui
Publication date
01-12-2016
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2016
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-016-1583-0

Other articles of this Issue 1/2016

Malaria Journal 1/2016 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.