Origin and Evolution of Sulfadoxine Resistant Plasmodium falciparum
Publication Date
March 26, 2010
Journal
PLOS Pathogens
Authors
Sumiti Vinayak, Md Tauqeer Alam, Tonya Mixson Hayden, Andrea M. Mc Collum, et al
Volume
6
Issue
3
Pages
e1000830
DOI
https://dx.plos.org/10.1371/journal.ppat.1000830
Publisher URL
http://journals.plos.org/plospathogens/article?id=10.1371%2Fjournal.ppat.1000830
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/20360965
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2847944
Europe PMC
http://europepmc.org/abstract/MED/20360965
Web of Science
000277720400038
Scopus
77950435762
Mendeley
http://www.mendeley.com/research/origin-evolution-sulfadoxine-resistant-plasmodium-falciparum
Events
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Mendeley | Further Information

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Previous studies have shown that chloroquine (CQ) and pyrimethamine resistance originated in this region and eventually spread to other Asian countries and Africa. However, there is a dearth in understanding the origin and evolution of dhps alleles associated with sulfadoxine resistance. The present study was designed to reveal the origin(s) of sulfadoxine resistance in Cambodia and its evolutionary relationship to African and South American dhps alleles. We sequenced 234 Cambodian Plasmodium falciparum isolates for the dhps codons S436A/F, A437G, K540E, A581G and A613S/T implicated in sulfadoxine resistance. We also genotyped 10 microsatellite loci around dhps to determine the genetic backgrounds of various alleles and compared them with the backgrounds of alleles prevalent in Africa and South America. In addition to previously known highly-resistant triple mutant dhps alleles SGEGA and AGEAA (codons 436, 437, 540, 581, 613 are sequentially indicated), a large proportion of the isolates (19.3%) contained a 540N mutation in association with 437G/581G yielding a previously unreported triple mutant allele, SGNGA. Microsatellite data strongly suggest the strength of selection was greater on triple mutant dhps alleles followed by the double and single mutants. We provide evidence for at least three independent origins for the double mutants, one each for the SGKGA, AGKAA and SGEAA alleles. Our data suggest that the triple mutant allele SGEGA and the novel allele SGNGA have common origin on the SGKGA background, whereas the AGEAA triple mutant was derived from AGKAA on multiple, albeit limited, genetic backgrounds. The SGEAA did not share haplotypes with any of the triple mutants. Comparative analysis of the microsatellite haplotypes flanking dhps alleles from Cambodia, Kenya, Cameroon and Venezuela revealed an independent origin of sulfadoxine resistant alleles in each of these regions.", "link"=>"http://www.mendeley.com/research/origin-evolution-sulfadoxine-resistant-plasmodium-falciparum", "reader_count"=>82, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Professor > Associate Professor"=>5, "Researcher"=>23, "Student > Doctoral Student"=>6, "Student > Ph. D. Student"=>19, "Student > Postgraduate"=>2, "Student > Master"=>14, "Other"=>3, "Student > Bachelor"=>4, "Lecturer"=>1, "Professor"=>3}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Professor > Associate Professor"=>5, "Researcher"=>23, "Student > Doctoral Student"=>6, "Student > Ph. D. 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CrossRef

Scopus | Further Information

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  • {"month"=>"12", "year"=>"2019", "pdf_views"=>"9", "xml_views"=>"0", "html_views"=>"8"}

Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/425804", "https://ndownloader.figshare.com/files/425853", "https://ndownloader.figshare.com/files/425897", "https://ndownloader.figshare.com/files/425957", "https://ndownloader.figshare.com/files/426016", "https://ndownloader.figshare.com/files/426073"], "description"=>"<div><p>The Thailand-Cambodia border is the epicenter for drug-resistant falciparum malaria. Previous studies have shown that chloroquine (CQ) and pyrimethamine resistance originated in this region and eventually spread to other Asian countries and Africa. However, there is a dearth in understanding the origin and evolution of <em>dhps</em> alleles associated with sulfadoxine resistance. The present study was designed to reveal the origin(s) of sulfadoxine resistance in Cambodia and its evolutionary relationship to African and South American <em>dhps</em> alleles. We sequenced 234 Cambodian <em>Plasmodium falciparum</em> isolates for the <em>dhps</em> codons S436A/F, A437G, K540E, A581G and A613S/T implicated in sulfadoxine resistance. We also genotyped 10 microsatellite loci around <em>dhps</em> to determine the genetic backgrounds of various alleles and compared them with the backgrounds of alleles prevalent in Africa and South America. In addition to previously known highly-resistant triple mutant <em>dhps</em> alleles S<u>GEG</u>A and <u>AGE</u>AA (codons 436, 437, 540, 581, 613 are sequentially indicated), a large proportion of the isolates (19.3%) contained a 540N mutation in association with 437G/581G yielding a previously unreported triple mutant allele, S<u>GNG</u>A. Microsatellite data strongly suggest the strength of selection was greater on triple mutant <em>dhps</em> alleles followed by the double and single mutants. We provide evidence for at least three independent origins for the double mutants, one each for the S<u>G</u>K<u>G</u>A, <u>AG</u>KAA and S<u>GE</u>AA alleles. Our data suggest that the triple mutant allele S<u>GEG</u>A and the novel allele S<u>GNG</u>A have common origin on the S<u>G</u>K<u>G</u>A background, whereas the <u>AGE</u>AA triple mutant was derived from <u>AG</u>KAA on multiple, albeit limited, genetic backgrounds. The S<u>GE</u>AA did not share haplotypes with any of the triple mutants. Comparative analysis of the microsatellite haplotypes flanking <em>dhps</em> alleles from Cambodia, Kenya, Cameroon and Venezuela revealed an independent origin of sulfadoxine resistant alleles in each of these regions.</p></div>", "links"=>[], "tags"=>["sulfadoxine", "resistant"], "article_id"=>144064, "categories"=>["Microbiology", "Evolutionary Biology", "Genetics", "Cancer"], "users"=>["Sumiti Vinayak", "Md Tauqeer Alam", "Tonya Mixson-Hayden", "Andrea M. McCollum", "Rithy Sem", "Naman K. Shah", "Pharath Lim", "Sinuon Muth", "William O. Rogers", "Thierry Fandeur", "John W. Barnwell", "Ananias A. Escalante", "Chansuda Wongsrichanalai", "Frederick Ariey", "Steven R. Meshnick", "Venkatachalam Udhayakumar"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1000830.s001", "https://dx.doi.org/10.1371/journal.ppat.1000830.s002", "https://dx.doi.org/10.1371/journal.ppat.1000830.s003", "https://dx.doi.org/10.1371/journal.ppat.1000830.s004", "https://dx.doi.org/10.1371/journal.ppat.1000830.s005", "https://dx.doi.org/10.1371/journal.ppat.1000830.s006"], "stats"=>{"downloads"=>21, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Origin_and_Evolution_of_Sulfadoxine_Resistant_Plasmodium_falciparum_/144064", "title"=>"Origin and Evolution of Sulfadoxine Resistant <em>Plasmodium falciparum</em>", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2010-03-26 01:07:44"}
  • {"files"=>["https://ndownloader.figshare.com/files/857631"], "description"=>"<p>An eBURST diagram showing major lineages for Cambodian <i>dhps</i> alleles. Two major lineages exist in Cameroon (S<u>G</u>KAA and <u>AG</u>KAA), one major lineage in Kenya (S<u>GE</u>AA), and one in Venezuela (S<u>G</u>K<u>G</u>A and S<u>GEG</u>A). Each lineage is distinct from the others, suggesting multiple, independent evolutionary histories.</p>", "links"=>[], "tags"=>["relationships", "alleles", "asia", "africa", "america"], "article_id"=>528069, "categories"=>["Microbiology", "Evolutionary Biology", "Genetics", "Virology"], "users"=>["Sumiti Vinayak", "Md Tauqeer Alam", "Tonya Mixson-Hayden", "Andrea M. McCollum", "Rithy Sem", "Naman K. Shah", "Pharath Lim", "Sinuon Muth", "William O. Rogers", "Thierry Fandeur", "John W. Barnwell", "Ananias A. Escalante", "Chansuda Wongsrichanalai", "Frederick Ariey", "Steven R. Meshnick", "Venkatachalam Udhayakumar"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000830.g005", "stats"=>{"downloads"=>1, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Genetic_relationships_among_the_dhps_alleles_of_Southeast_Asia_Cambodia_Africa_Kenya_and_Cameroon_and_South_America_Venezuela_/528069", "title"=>"Genetic relationships among the <i>dhps</i> alleles of Southeast Asia (Cambodia), Africa (Kenya and Cameroon) and South America (Venezuela).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-03-26 02:14:29"}
  • {"files"=>["https://ndownloader.figshare.com/files/857317"], "description"=>"<p>(<b>A</b>) Comparison of the wild type and three mutant (single, double and triple) groups. (<b>B</b>) Comparison of the single (S<u>G</u>KAA) and double mutant (<u>AG</u>KAA, S<u>GE</u>AA, S<u>G</u>K<u>G</u>A) <i>dhps</i> alleles. (<b>C</b>) Comparison of the three triple mutant (<u>AGE</u>AA, S<u>GEG</u>A, S<u>GNG</u>A) <i>dhps</i> alleles. The dashed line crossing the y-axis indicates the mean heterozygosity (<i>H<sub>e</sub></i>) at 8 neutral microsatellite loci on chromosomes 2 and 3. The error bars indicate ±1SD (standard deviation).</p>", "links"=>[], "tags"=>["sweeps", "alleles"], "article_id"=>527750, "categories"=>["Microbiology", "Evolutionary Biology", "Genetics", "Virology"], "users"=>["Sumiti Vinayak", "Md Tauqeer Alam", "Tonya Mixson-Hayden", "Andrea M. McCollum", "Rithy Sem", "Naman K. Shah", "Pharath Lim", "Sinuon Muth", "William O. Rogers", "Thierry Fandeur", "John W. Barnwell", "Ananias A. Escalante", "Chansuda Wongsrichanalai", "Frederick Ariey", "Steven R. Meshnick", "Venkatachalam Udhayakumar"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000830.g002", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Selective_sweeps_around_dhps_alleles_in_Cambodia_/527750", "title"=>"Selective sweeps around <i>dhps</i> alleles in Cambodia.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-03-26 02:09:10"}
  • {"files"=>["https://ndownloader.figshare.com/files/857501"], "description"=>"<p>(<b>A</b>) A median-joining network diagram depicting three independent origins for double mutant and two independent origins for triple mutant <i>dhps</i> alleles in Cambodia. The 141 <i>P. falciparum</i> isolates were classified into 85 haplotypes (H1 to H85; see individual haplotypes profiles in <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1000830#ppat.1000830.s005\" target=\"_blank\">Table S5</a>) based on the 10-loci microsatellite profile around <i>dhps</i> gene. The size of the circle is proportional to the number of isolates showing particular 10-loci microsatellite haplotype, the proportion of <i>dhps</i> alleles on that haplotype background are depicted by the pie charts. The red dots are hypothetical median vectors generated by the software to connect existing haplotypes within the network with maximum parsimony. Box 1, 2 and 3 indicate three major origins for <i>dhps</i> mutant alleles. (<b>B</b>) Scheme of plausible evolution of <i>dhps</i> alleles inferred from the microsatellite haplotypes data. Three major and independent lineages are proposed for the double mutants, one each for S<u>G</u>K<u>G</u>A, S<u>GE</u>AA and <u>AG</u>KAA. The S<u>G</u>K<u>G</u>A is the progenitor allele for S<u>GEG</u>A and S<u>GNG</u>A triple mutants, whereas <u>AG</u>KAA is the progenitor for <u>AGE</u>AA triple mutant. Most likely, the <u>AG</u>KAA double mutant could also be the progenitor of <u>AGN</u>AA triple mutant found on the Andaman and Nicobar Islands, given its wide occurrence on the islands.</p>", "links"=>[], "tags"=>["relationships", "alleles"], "article_id"=>527944, "categories"=>["Microbiology", "Evolutionary Biology", "Genetics", "Virology"], "users"=>["Sumiti Vinayak", "Md Tauqeer Alam", "Tonya Mixson-Hayden", "Andrea M. McCollum", "Rithy Sem", "Naman K. Shah", "Pharath Lim", "Sinuon Muth", "William O. Rogers", "Thierry Fandeur", "John W. Barnwell", "Ananias A. Escalante", "Chansuda Wongsrichanalai", "Frederick Ariey", "Steven R. Meshnick", "Venkatachalam Udhayakumar"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000830.g004", "stats"=>{"downloads"=>1, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Genetic_relationships_among_dhps_alleles_in_Cambodia_/527944", "title"=>"Genetic relationships among <i>dhps</i> alleles in Cambodia.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-03-26 02:12:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/857694"], "description"=>"<p>Note: The DHPS alleles are denoted by the single letter amino acid code for codons 436, 437, 540, 581 and 613. Mutated amino acids are boldfaced and underlined.</p>", "links"=>[], "tags"=>["mutations"], "article_id"=>528141, "categories"=>["Microbiology", "Evolutionary Biology", "Genetics", "Virology"], "users"=>["Sumiti Vinayak", "Md Tauqeer Alam", "Tonya Mixson-Hayden", "Andrea M. McCollum", "Rithy Sem", "Naman K. Shah", "Pharath Lim", "Sinuon Muth", "William O. Rogers", "Thierry Fandeur", "John W. Barnwell", "Ananias A. Escalante", "Chansuda Wongsrichanalai", "Frederick Ariey", "Steven R. Meshnick", "Venkatachalam Udhayakumar"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000830.t001", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Prevalence_of_dhps_mutations_in_Cambodia_/528141", "title"=>"Prevalence of <i>dhps</i> mutations in Cambodia.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2010-03-26 02:15:41"}
  • {"files"=>["https://ndownloader.figshare.com/files/857223"], "description"=>"<p>The pie-diagrams show the frequency distribution of the single, double, triple and quadruple mutant <i>dhps</i> alleles in Cambodia. PL, Pailin; KS, Kampong Seila; CK, Chumkiri; MM, Memut; RK, Rattanakiri.</p>", "links"=>[], "tags"=>["cambodia"], "article_id"=>527666, "categories"=>["Microbiology", "Evolutionary Biology", "Genetics", "Virology"], "users"=>["Sumiti Vinayak", "Md Tauqeer Alam", "Tonya Mixson-Hayden", "Andrea M. McCollum", "Rithy Sem", "Naman K. Shah", "Pharath Lim", "Sinuon Muth", "William O. Rogers", "Thierry Fandeur", "John W. Barnwell", "Ananias A. Escalante", "Chansuda Wongsrichanalai", "Frederick Ariey", "Steven R. Meshnick", "Venkatachalam Udhayakumar"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000830.g001", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_map_of_Cambodia_showing_study_sites_/527666", "title"=>"The map of Cambodia showing study sites.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-03-26 02:07:46"}
  • {"files"=>["https://ndownloader.figshare.com/files/857744"], "description"=>"<p>Note: Populations were defined according to geographic locations. Pailin: PL (n = 36); Chumkiri: CK (n = 50); Memut: MM, (n = 28); and Rattanakiri: RK (n = 27). Because there were only 7 singly-infected isolates from Kampong Seila these were combined with the PL population. F<sub>ST</sub> values calculated from 10 <i>dhps</i> loci are given below the diagonal while those above are calculated from the 8 neutral loci. The values in bold indicate significant F<sub>ST</sub> after Bonferroni correction (<i>P</i>≤0.008) for multiple comparisons. Overall F<sub>ST</sub> value for <i>dhps</i> after jackknifing over loci was 0.12±0.02 (95% CI obtained after 1000 bootstrapping over loci: 0.09–0.16) and for neutral loci F<sub>ST</sub> was 0.04±0.01 (95% CI: 0.024–0.060).</p>", "links"=>[], "tags"=>["comparisons", "populations"], "article_id"=>528184, "categories"=>["Microbiology", "Evolutionary Biology", "Genetics", "Virology"], "users"=>["Sumiti Vinayak", "Md Tauqeer Alam", "Tonya Mixson-Hayden", "Andrea M. McCollum", "Rithy Sem", "Naman K. Shah", "Pharath Lim", "Sinuon Muth", "William O. Rogers", "Thierry Fandeur", "John W. Barnwell", "Ananias A. Escalante", "Chansuda Wongsrichanalai", "Frederick Ariey", "Steven R. Meshnick", "Venkatachalam Udhayakumar"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000830.t002", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Pairwise_F_ST_comparisons_between_four_populations_in_Cambodia_/528184", "title"=>"Pairwise F<sub>ST</sub> comparisons between four populations in Cambodia.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2010-03-26 02:16:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/857424"], "description"=>"<p>(<b>A</b>) Histogram plotting F<sub>ST</sub> (±SD) values at 8 neutral (gray bars) and 10 <i>dhps</i> (black bars) microsatellite loci. Asterisk indicates significant values obtained after 1000 random permutations. Populations were defined according to their <i>dhps</i> genotype (i.e. wild type, single, double, or triple mutant) for calculations of the overall (global) F<sub>ST</sub>. The overall F<sub>ST</sub> for <i>dhps</i> after jackknifing over loci was 0.20 (95% CI: 0.15–0.26) whereas the overall F<sub>ST</sub> for 8 neutral loci was 0.01 (95% CI: 0.006–0.019). The difference between F<sub>ST</sub> values of <i>dhps</i> and neutral groups was highly significant as assessed by Mann-Whitney <i>U</i> test (Z = 3.55, <i>P</i> = 0.0003). (<b>B</b>) Plot of F<sub>ST</sub> versus <i>H<sub>e</sub></i> to disentangle selection on <i>dhps</i> and neutral loci. Black circles represent 10 <i>dhps</i> loci and white diamonds represent 8 neutral loci. The gray shading indicates the region of neutral expectations at a confidence level of 95%. The markers above the gray region are considered to be under directional selection while those inside the gray region are considered to be neutral. The <i>P</i> values (simulated F<sub>ST</sub>ST) for each locus are given as supporting information (<a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1000830#ppat.1000830.s004\" target=\"_blank\">Table S4</a>).</p>", "links"=>[], "tags"=>["unselected"], "article_id"=>527871, "categories"=>["Microbiology", "Evolutionary Biology", "Genetics", "Virology"], "users"=>["Sumiti Vinayak", "Md Tauqeer Alam", "Tonya Mixson-Hayden", "Andrea M. McCollum", "Rithy Sem", "Naman K. Shah", "Pharath Lim", "Sinuon Muth", "William O. Rogers", "Thierry Fandeur", "John W. Barnwell", "Ananias A. Escalante", "Chansuda Wongsrichanalai", "Frederick Ariey", "Steven R. Meshnick", "Venkatachalam Udhayakumar"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000830.g003", "stats"=>{"downloads"=>7, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Comparison_of_F_ST_across_selected_dhps_and_unselected_neutral_loci_/527871", "title"=>"Comparison of F<sub>ST</sub> across selected (<i>dhps</i>) and unselected (neutral) loci.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-03-26 02:11:11"}

PMC Usage Stats | Further Information

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  • {"unique-ip"=>"5", "full-text"=>"4", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"8"}
  • {"unique-ip"=>"11", "full-text"=>"8", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"9"}
  • {"unique-ip"=>"16", "full-text"=>"17", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2019", "month"=>"10"}
  • {"unique-ip"=>"6", "full-text"=>"2", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"12"}

Relative Metric

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