Proteomic analysis of Plasmodium falciparum response to isocryptolepine derivative
Identifieur interne : 000895 ( Ncbi/Merge ); précédent : 000894; suivant : 000896Proteomic analysis of Plasmodium falciparum response to isocryptolepine derivative
Auteurs : Kitiya Rujimongkon [Thaïlande] ; Mathirut Mungthin [Thaïlande] ; Jumreang Tummatorn [Thaïlande] ; Sumate Ampawong [Thaïlande] ; Poom Adisakwattana [Thaïlande] ; Usa Boonyuen [Thaïlande] ; Onrapak Reamtong [Thaïlande]Source :
- PLoS ONE [ 1932-6203 ] ; 2019.
Abstract
Drug-resistant strains of malaria parasites have emerged for most of antimalarial medications. A new chemotherapeutic compound is needed for malarial therapy. Antimalarial activity against both drug-sensitive and drug-resistant
Url:
DOI: 10.1371/journal.pone.0220871
PubMed: 31393938
PubMed Central: 6687117
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id="aff002"><addr-line>Department of Pharmacology, Phramongkutklao College of Medicine, Bangkok, Thailand</addr-line></nlm:aff><country xml:lang="fr">Thaïlande</country><wicri:regionArea>Department of Pharmacology, Phramongkutklao College of Medicine, Bangkok</wicri:regionArea><wicri:noRegion>Bangkok</wicri:noRegion></affiliation></author><author><name sortKey="Tummatorn, Jumreang" sort="Tummatorn, Jumreang" uniqKey="Tummatorn J" first="Jumreang" last="Tummatorn">Jumreang Tummatorn</name><affiliation wicri:level="1"><nlm:aff id="aff003"><addr-line>Program on Chemical Biology, Chulabhorn Graduate Institute, Center of Excellence on Environmental Health and Toxicology, Ministry of Education, Bangkok, Thailand</addr-line></nlm:aff><country xml:lang="fr">Thaïlande</country><wicri:regionArea>Program on Chemical Biology, Chulabhorn Graduate Institute, Center of Excellence on Environmental Health and Toxicology, Ministry of Education, 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type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6687117</idno><idno type="RBID">PMC:6687117</idno><idno type="doi">10.1371/journal.pone.0220871</idno><date when="2019">2019</date><idno type="wicri:Area/Pmc/Corpus">000774</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000774</idno><idno type="wicri:Area/Pmc/Curation">000774</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">000774</idno><idno type="wicri:Area/Pmc/Checkpoint">000464</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Checkpoint">000464</idno><idno type="wicri:Area/Ncbi/Merge">000895</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Proteomic analysis of <italic>Plasmodium falciparum</italic> response to isocryptolepine derivative</title><author><name sortKey="Rujimongkon, Kitiya" sort="Rujimongkon, Kitiya" uniqKey="Rujimongkon K" first="Kitiya" last="Rujimongkon">Kitiya Rujimongkon</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>Department of Molecular Tropical Medicine and Genetics, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand</addr-line></nlm:aff><country xml:lang="fr">Thaïlande</country><wicri:regionArea>Department of Molecular Tropical Medicine and Genetics, Faculty of Tropical Medicine, Mahidol University, Bangkok</wicri:regionArea><wicri:noRegion>Bangkok</wicri:noRegion></affiliation></author><author><name sortKey="Mungthin, Mathirut" sort="Mungthin, Mathirut" uniqKey="Mungthin M" first="Mathirut" last="Mungthin">Mathirut Mungthin</name><affiliation wicri:level="1"><nlm:aff id="aff002"><addr-line>Department of Pharmacology, Phramongkutklao College of Medicine, Bangkok, Thailand</addr-line></nlm:aff><country xml:lang="fr">Thaïlande</country><wicri:regionArea>Department of Pharmacology, Phramongkutklao College of Medicine, Bangkok</wicri:regionArea><wicri:noRegion>Bangkok</wicri:noRegion></affiliation></author><author><name sortKey="Tummatorn, Jumreang" sort="Tummatorn, Jumreang" uniqKey="Tummatorn J" first="Jumreang" last="Tummatorn">Jumreang Tummatorn</name><affiliation wicri:level="1"><nlm:aff id="aff003"><addr-line>Program on Chemical Biology, Chulabhorn Graduate Institute, Center of Excellence on Environmental Health and Toxicology, Ministry of Education, Bangkok, Thailand</addr-line></nlm:aff><country xml:lang="fr">Thaïlande</country><wicri:regionArea>Program on Chemical Biology, Chulabhorn Graduate Institute, Center of Excellence on Environmental Health and Toxicology, Ministry of Education, Bangkok</wicri:regionArea><wicri:noRegion>Bangkok</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="aff004"><addr-line>Laboratory of Medicinal Chemistry, Chulabhorn Research Institute, Bangkok, Thailand</addr-line></nlm:aff><country xml:lang="fr">Thaïlande</country><wicri:regionArea>Laboratory of Medicinal Chemistry, Chulabhorn Research Institute, Bangkok</wicri:regionArea><wicri:noRegion>Bangkok</wicri:noRegion></affiliation></author><author><name sortKey="Ampawong, Sumate" sort="Ampawong, Sumate" uniqKey="Ampawong S" first="Sumate" last="Ampawong">Sumate Ampawong</name><affiliation wicri:level="1"><nlm:aff id="aff005"><addr-line>Department of Tropical Pathology, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand</addr-line></nlm:aff><country xml:lang="fr">Thaïlande</country><wicri:regionArea>Department of Tropical Pathology, Faculty of Tropical Medicine, Mahidol University, Bangkok</wicri:regionArea><wicri:noRegion>Bangkok</wicri:noRegion></affiliation></author><author><name sortKey="Adisakwattana, Poom" sort="Adisakwattana, Poom" uniqKey="Adisakwattana P" first="Poom" last="Adisakwattana">Poom Adisakwattana</name><affiliation wicri:level="1"><nlm:aff id="aff006"><addr-line>Department of Helminthology, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand</addr-line></nlm:aff><country xml:lang="fr">Thaïlande</country><wicri:regionArea>Department of Helminthology, Faculty of Tropical Medicine, Mahidol University, Bangkok</wicri:regionArea><wicri:noRegion>Bangkok</wicri:noRegion></affiliation></author><author><name sortKey="Boonyuen, Usa" sort="Boonyuen, Usa" uniqKey="Boonyuen U" first="Usa" last="Boonyuen">Usa Boonyuen</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>Department of Molecular Tropical Medicine and Genetics, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand</addr-line></nlm:aff><country xml:lang="fr">Thaïlande</country><wicri:regionArea>Department of Molecular Tropical Medicine and Genetics, Faculty of Tropical Medicine, Mahidol University, Bangkok</wicri:regionArea><wicri:noRegion>Bangkok</wicri:noRegion></affiliation></author><author><name sortKey="Reamtong, Onrapak" sort="Reamtong, Onrapak" uniqKey="Reamtong O" first="Onrapak" last="Reamtong">Onrapak Reamtong</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>Department of Molecular Tropical Medicine and Genetics, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand</addr-line></nlm:aff><country xml:lang="fr">Thaïlande</country><wicri:regionArea>Department of Molecular Tropical Medicine and Genetics, Faculty of Tropical Medicine, Mahidol University, Bangkok</wicri:regionArea><wicri:noRegion>Bangkok</wicri:noRegion></affiliation></author></analytic><series><title level="j">PLoS ONE</title><idno type="eISSN">1932-6203</idno><imprint><date when="2019">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Drug-resistant strains of malaria parasites have emerged for most of antimalarial medications. A new chemotherapeutic compound is needed for malarial therapy. Antimalarial activity against both drug-sensitive and drug-resistant <italic>P</italic>. <italic>falciparum</italic> has been reported for an isocryptolepine derivative, 8-bromo-2-fluoro-5-methyl-5H-indolo[3,2-c]quinoline (ICL-M), which also showed less toxicity to human cells. ICL-M has indoloquinoline as a core structure and its mode of action remains unclear. Here, we explored the mechanisms of ICL-M in <italic>P</italic>. <italic>falciparum</italic> by assessing the stage-specific activity, time-dependent effect, a proteomic analysis and morphology. Since human topo II activity inhibition has been reported as a function of isocryptolepine derivatives, malarial topo II activity inhibition of ICL-M was also examined in this study. The ICL-M exhibited antimalarial activity against both the ring and trophozoite stages of <italic>P</italic>. <italic>falciparum</italic>. Our proteomics analysis revealed that a total of 112 <italic>P</italic>. <italic>falciparum</italic> proteins were differentially expressed after ICL-M exposure; among these, 58 and 54 proteins were upregulated and downregulated, respectively. Proteins localized in the food vacuole, nucleus, and cytoplasm showed quantitative alterations after ICL-M treatment. A bioinformatic analysis revealed that pathways associated with ribosomes, proteasomes, metabolic pathways, amino acid biosynthesis, oxidative phosphorylation, and carbon metabolism were significantly different in <italic>P</italic>. <italic>falciparum</italic> treated with ICL-M. Moreover, a loss of ribosomes was clearly observed by transmission electron microscopy in the ICL-M-treated <italic>P</italic>. <italic>falciparum</italic>. This finding is in agreement with the proteomics data, which revealed downregulated levels of ribosomal proteins following ICL-M treatment. Our results provide important information about the mechanisms by which ICL-M affects the malaria parasite, which may facilitate the drug development of isocryptolepine derivatives.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct></biblStruct><biblStruct><analytic><author><name sortKey="Willcox, Ml" uniqKey="Willcox M">ML Willcox</name></author><author><name sortKey="Bodeker, G" uniqKey="Bodeker G">G Bodeker</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Grellier, P" uniqKey="Grellier P">P Grellier</name></author><author><name sortKey="Ramiaramanana, L" uniqKey="Ramiaramanana L">L Ramiaramanana</name></author><author><name sortKey="Millerioux, V" uniqKey="Millerioux V">V Millerioux</name></author><author><name sortKey="Deharo, E" uniqKey="Deharo E">E Deharo</name></author><author><name sortKey="Schrevel, J" uniqKey="Schrevel J">J Schrével</name></author><author><name sortKey="Frappier, F" uniqKey="Frappier F">F 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<front><journal-meta><journal-id journal-id-type="nlm-ta">PLoS One</journal-id><journal-id journal-id-type="iso-abbrev">PLoS ONE</journal-id><journal-id journal-id-type="publisher-id">plos</journal-id><journal-id journal-id-type="pmc">plosone</journal-id><journal-title-group><journal-title>PLoS ONE</journal-title></journal-title-group><issn pub-type="epub">1932-6203</issn><publisher><publisher-name>Public Library of Science</publisher-name><publisher-loc>San Francisco, CA USA</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">31393938</article-id><article-id pub-id-type="pmc">6687117</article-id><article-id pub-id-type="doi">10.1371/journal.pone.0220871</article-id><article-id pub-id-type="publisher-id">PONE-D-19-14810</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Parasitology</subject><subj-group><subject>Parasite Groups</subject><subj-group><subject>Apicomplexa</subject><subj-group><subject>Plasmodium</subject></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Biochemistry</subject><subj-group><subject>Proteins</subject><subj-group><subject>Antiport Proteins</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Cell Biology</subject><subj-group><subject>Cellular Structures and Organelles</subject><subj-group><subject>Cytoplasm</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject><subj-group><subject>Pharmacology</subject><subj-group><subject>Drugs</subject><subj-group><subject>Antimalarials</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Physical Sciences</subject><subj-group><subject>Physics</subject><subj-group><subject>Physical Laws and Principles</subject><subj-group><subject>Conservation of Mass</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Cell Biology</subject><subj-group><subject>Cellular Structures and Organelles</subject><subj-group><subject>Cell Membranes</subject><subj-group><subject>Membrane Proteins</subject><subj-group><subject>Eukaryotic Membrane Proteins</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Cell Biology</subject><subj-group><subject>Cell Physiology</subject><subj-group><subject>Membrane Trafficking</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Parasitology</subject><subj-group><subject>Parasite Groups</subject><subj-group><subject>Apicomplexa</subject><subj-group><subject>Trophozoites</subject></subj-group></subj-group></subj-group></subj-group></subj-group></article-categories><title-group><article-title>Proteomic analysis of <italic>Plasmodium falciparum</italic> response to isocryptolepine derivative</article-title><alt-title alt-title-type="running-head"><italic>Plasmodium falciparum</italic> proteins response to isocryptolepine derivative</alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Rujimongkon</surname><given-names>Kitiya</given-names></name><role content-type="http://credit.casrai.org/">Data curation</role><role content-type="http://credit.casrai.org/">Formal analysis</role><role content-type="http://credit.casrai.org/">Investigation</role><role content-type="http://credit.casrai.org/">Methodology</role><role content-type="http://credit.casrai.org/">Validation</role><role content-type="http://credit.casrai.org/">Writing – original draft</role><role content-type="http://credit.casrai.org/">Writing – review & editing</role><xref ref-type="aff" rid="aff001"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Mungthin</surname><given-names>Mathirut</given-names></name><role content-type="http://credit.casrai.org/">Methodology</role><role content-type="http://credit.casrai.org/">Resources</role><role content-type="http://credit.casrai.org/">Writing – review & editing</role><xref ref-type="aff" rid="aff002"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>Tummatorn</surname><given-names>Jumreang</given-names></name><role content-type="http://credit.casrai.org/">Methodology</role><xref ref-type="aff" rid="aff003"><sup>3</sup></xref><xref ref-type="aff" rid="aff004"><sup>4</sup></xref></contrib><contrib contrib-type="author"><name><surname>Ampawong</surname><given-names>Sumate</given-names></name><role content-type="http://credit.casrai.org/">Methodology</role><role content-type="http://credit.casrai.org/">Software</role><xref ref-type="aff" rid="aff005"><sup>5</sup></xref></contrib><contrib contrib-type="author"><name><surname>Adisakwattana</surname><given-names>Poom</given-names></name><role content-type="http://credit.casrai.org/">Supervision</role><role content-type="http://credit.casrai.org/">Writing – review & editing</role><xref ref-type="aff" rid="aff006"><sup>6</sup></xref></contrib><contrib contrib-type="author"><name><surname>Boonyuen</surname><given-names>Usa</given-names></name><role content-type="http://credit.casrai.org/">Supervision</role><xref ref-type="aff" rid="aff001"><sup>1</sup></xref></contrib><contrib contrib-type="author"><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0002-1154-6485</contrib-id><name><surname>Reamtong</surname><given-names>Onrapak</given-names></name><role content-type="http://credit.casrai.org/">Conceptualization</role><role content-type="http://credit.casrai.org/">Funding acquisition</role><role content-type="http://credit.casrai.org/">Resources</role><role content-type="http://credit.casrai.org/">Supervision</role><role content-type="http://credit.casrai.org/">Writing – original draft</role><role content-type="http://credit.casrai.org/">Writing – review & editing</role><xref ref-type="aff" rid="aff001"><sup>1</sup></xref><xref ref-type="corresp" rid="cor001">*</xref></contrib></contrib-group><aff id="aff001"><label>1</label><addr-line>Department of Molecular Tropical Medicine and Genetics, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand</addr-line></aff><aff id="aff002"><label>2</label><addr-line>Department of Pharmacology, Phramongkutklao College of Medicine, Bangkok, Thailand</addr-line></aff><aff id="aff003"><label>3</label><addr-line>Program on Chemical Biology, Chulabhorn Graduate Institute, Center of Excellence on Environmental Health and Toxicology, Ministry of Education, Bangkok, Thailand</addr-line></aff><aff id="aff004"><label>4</label><addr-line>Laboratory of Medicinal Chemistry, Chulabhorn Research Institute, Bangkok, Thailand</addr-line></aff><aff id="aff005"><label>5</label><addr-line>Department of Tropical Pathology, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand</addr-line></aff><aff id="aff006"><label>6</label><addr-line>Department of Helminthology, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand</addr-line></aff><contrib-group><contrib contrib-type="editor"><name><surname>Carvalho</surname><given-names>Luzia Helena</given-names></name><role>Editor</role><xref ref-type="aff" rid="edit1"></xref></contrib></contrib-group><aff id="edit1"><addr-line>Instituto Rene Rachou, BRAZIL</addr-line></aff><author-notes><fn fn-type="COI-statement" id="coi001"><p><bold>Competing Interests: </bold>The authors have declared that no competing interests exist.</p></fn><corresp id="cor001">* E-mail: <email>onrapak.rea@mahidol.ac.th</email></corresp></author-notes><pub-date pub-type="epub"><day>8</day><month>8</month><year>2019</year></pub-date><pub-date pub-type="collection"><year>2019</year></pub-date><volume>14</volume><issue>8</issue><elocation-id>e0220871</elocation-id><history><date date-type="received"><day>25</day><month>5</month><year>2019</year></date><date date-type="accepted"><day>24</day><month>7</month><year>2019</year></date></history><permissions><copyright-statement>© 2019 Rujimongkon et al</copyright-statement><copyright-year>2019</copyright-year><copyright-holder>Rujimongkon et al</copyright-holder><license xlink:href="http://creativecommons.org/licenses/by/4.0/"><license-p>This is an open access article distributed under the terms of the <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution License</ext-link>, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</license-p></license></permissions><self-uri content-type="pdf" xlink:href="pone.0220871.pdf"></self-uri><abstract><p>Drug-resistant strains of malaria parasites have emerged for most of antimalarial medications. A new chemotherapeutic compound is needed for malarial therapy. Antimalarial activity against both drug-sensitive and drug-resistant <italic>P</italic>. <italic>falciparum</italic> has been reported for an isocryptolepine derivative, 8-bromo-2-fluoro-5-methyl-5H-indolo[3,2-c]quinoline (ICL-M), which also showed less toxicity to human cells. ICL-M has indoloquinoline as a core structure and its mode of action remains unclear. Here, we explored the mechanisms of ICL-M in <italic>P</italic>. <italic>falciparum</italic> by assessing the stage-specific activity, time-dependent effect, a proteomic analysis and morphology. Since human topo II activity inhibition has been reported as a function of isocryptolepine derivatives, malarial topo II activity inhibition of ICL-M was also examined in this study. The ICL-M exhibited antimalarial activity against both the ring and trophozoite stages of <italic>P</italic>. <italic>falciparum</italic>. Our proteomics analysis revealed that a total of 112 <italic>P</italic>. <italic>falciparum</italic> proteins were differentially expressed after ICL-M exposure; among these, 58 and 54 proteins were upregulated and downregulated, respectively. Proteins localized in the food vacuole, nucleus, and cytoplasm showed quantitative alterations after ICL-M treatment. A bioinformatic analysis revealed that pathways associated with ribosomes, proteasomes, metabolic pathways, amino acid biosynthesis, oxidative phosphorylation, and carbon metabolism were significantly different in <italic>P</italic>. <italic>falciparum</italic> treated with ICL-M. Moreover, a loss of ribosomes was clearly observed by transmission electron microscopy in the ICL-M-treated <italic>P</italic>. <italic>falciparum</italic>. This finding is in agreement with the proteomics data, which revealed downregulated levels of ribosomal proteins following ICL-M treatment. Our results provide important information about the mechanisms by which ICL-M affects the malaria parasite, which may facilitate the drug development of isocryptolepine derivatives.</p></abstract><funding-group><award-group id="award001"><funding-source><institution-wrap><institution-id institution-id-type="funder-id">http://dx.doi.org/10.13039/501100006439</institution-id><institution>Faculty of Tropical Medicine, Mahidol University</institution></institution-wrap></funding-source><award-id>Fiscal Year 2013</award-id><principal-award-recipient><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0002-1154-6485</contrib-id><name><surname>Reamtong</surname><given-names>Onrapak</given-names></name></principal-award-recipient></award-group><award-group id="award002"><funding-source><institution-wrap><institution-id institution-id-type="funder-id">http://dx.doi.org/10.13039/100008966</institution-id><institution>Thailand Toray Science Foundation</institution></institution-wrap></funding-source><award-id>TTSF 2016</award-id><principal-award-recipient><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0002-1154-6485</contrib-id><name><surname>Reamtong</surname><given-names>Onrapak</given-names></name></principal-award-recipient></award-group><funding-statement>This study was supported by FTM2013 of Faculty of Tropical Medicine, Mahidol university and Thailand Toray Science Foundation.</funding-statement></funding-group><counts><fig-count count="9"></fig-count><table-count count="4"></table-count><page-count count="22"></page-count></counts><custom-meta-group><custom-meta id="data-availability"><meta-name>Data Availability</meta-name><meta-value>All relevant data are within the manuscript and its Supporting Information files.</meta-value></custom-meta></custom-meta-group></article-meta><notes><title>Data Availability</title><p>All relevant data are within the manuscript and its Supporting Information files.</p></notes></front></pmc><affiliations><list><country><li>Thaïlande</li></country></list><tree><country name="Thaïlande"><noRegion><name sortKey="Rujimongkon, Kitiya" sort="Rujimongkon, Kitiya" uniqKey="Rujimongkon K" first="Kitiya" last="Rujimongkon">Kitiya Rujimongkon</name></noRegion><name sortKey="Adisakwattana, Poom" sort="Adisakwattana, Poom" uniqKey="Adisakwattana P" first="Poom" last="Adisakwattana">Poom Adisakwattana</name><name sortKey="Ampawong, Sumate" sort="Ampawong, Sumate" uniqKey="Ampawong S" first="Sumate" last="Ampawong">Sumate Ampawong</name><name sortKey="Boonyuen, Usa" sort="Boonyuen, Usa" uniqKey="Boonyuen U" first="Usa" last="Boonyuen">Usa Boonyuen</name><name sortKey="Mungthin, Mathirut" sort="Mungthin, Mathirut" uniqKey="Mungthin M" first="Mathirut" last="Mungthin">Mathirut Mungthin</name><name sortKey="Reamtong, Onrapak" sort="Reamtong, Onrapak" uniqKey="Reamtong O" first="Onrapak" last="Reamtong">Onrapak Reamtong</name><name sortKey="Tummatorn, Jumreang" sort="Tummatorn, Jumreang" uniqKey="Tummatorn J" first="Jumreang" last="Tummatorn">Jumreang Tummatorn</name><name sortKey="Tummatorn, Jumreang" sort="Tummatorn, Jumreang" uniqKey="Tummatorn J" first="Jumreang" last="Tummatorn">Jumreang Tummatorn</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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