A novel marker, ARM58, confers antimony resistance to Leishmania spp.☆
Identifieur interne : 000229 ( Ncbi/Merge ); précédent : 000228; suivant : 000230A novel marker, ARM58, confers antimony resistance to Leishmania spp.☆
Auteurs : Andrea Nühs [Allemagne] ; Carola Sch Fer [Allemagne] ; Dorothea Zander [Allemagne] ; Leona Trübe [Allemagne] ; Paloma Tejera Nevado [Allemagne] ; Sonja Schmidt [Allemagne] ; Jorge Arevalo [Pérou] ; Vanessa Adaui [Pérou] ; Louis Maes [Belgique] ; Jean-Claude Dujardin [Belgique] ; Joachim Clos [Allemagne]Source :
- International Journal for Parasitology: Drugs and Drug Resistance [ 2211-3207 ] ; 2013.
Abstract
Url:
DOI: 10.1016/j.ijpddr.2013.11.004
PubMed: 24596667
PubMed Central: 3940081
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<front><journal-meta><journal-id journal-id-type="nlm-ta">Int J Parasitol Drugs Drug Resist</journal-id><journal-id journal-id-type="iso-abbrev">Int J Parasitol Drugs Drug Resist</journal-id><journal-title-group><journal-title>International Journal for Parasitology: Drugs and Drug Resistance</journal-title></journal-title-group><issn pub-type="epub">2211-3207</issn><publisher><publisher-name>Elsevier</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">24596667</article-id><article-id pub-id-type="pmc">3940081</article-id><article-id pub-id-type="publisher-id">S2211-3207(13)00020-1</article-id><article-id pub-id-type="doi">10.1016/j.ijpddr.2013.11.004</article-id><article-categories><subj-group subj-group-type="heading"><subject>Article</subject></subj-group></article-categories><title-group><article-title>A novel marker, <italic>ARM58</italic>, confers antimony resistance to <italic>Leishmania</italic> spp.<sup><xref ref-type="fn" rid="d32e504">☆</xref></sup></article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Nühs</surname><given-names>Andrea</given-names></name><xref rid="af005" ref-type="aff">a</xref><xref rid="fn1" ref-type="fn">1</xref></contrib><contrib contrib-type="author"><name><surname>Schäfer</surname><given-names>Carola</given-names></name><xref rid="af005" ref-type="aff">a</xref><xref rid="fn2" ref-type="fn">2</xref></contrib><contrib contrib-type="author"><name><surname>Zander</surname><given-names>Dorothea</given-names></name><xref rid="af005" ref-type="aff">a</xref></contrib><contrib contrib-type="author"><name><surname>Trübe</surname><given-names>Leona</given-names></name><xref rid="af005" ref-type="aff">a</xref><xref rid="fn3" ref-type="fn">3</xref></contrib><contrib contrib-type="author"><name><surname>Tejera Nevado</surname><given-names>Paloma</given-names></name><xref rid="af005" ref-type="aff">a</xref></contrib><contrib contrib-type="author"><name><surname>Schmidt</surname><given-names>Sonja</given-names></name><xref rid="af005" ref-type="aff">a</xref><xref rid="fn4" ref-type="fn">4</xref></contrib><contrib contrib-type="author"><name><surname>Arevalo</surname><given-names>Jorge</given-names></name><xref rid="af010" ref-type="aff">b</xref></contrib><contrib contrib-type="author"><name><surname>Adaui</surname><given-names>Vanessa</given-names></name><xref rid="af010" ref-type="aff">b</xref></contrib><contrib contrib-type="author"><name><surname>Maes</surname><given-names>Louis</given-names></name><xref rid="af020" ref-type="aff">d</xref></contrib><contrib contrib-type="author"><name><surname>Dujardin</surname><given-names>Jean-Claude</given-names></name><xref rid="af015" ref-type="aff">c</xref><xref rid="af020" ref-type="aff">d</xref></contrib><contrib contrib-type="author"><name><surname>Clos</surname><given-names>Joachim</given-names></name><email>clos@bnitm.de</email><xref rid="af005" ref-type="aff">a</xref><xref rid="cor1" ref-type="corresp">⁎</xref></contrib></contrib-group><aff id="af005"><label>a</label>Bernhard Nocht Institute for Tropical Medicine, D20359 Hamburg, Germany</aff><aff id="af010"><label>b</label>Instituto de Medicina Tropical Alexander von Humboldt, Universidad Peruana Cayetano Heredia, Lima, Peru</aff><aff id="af015"><label>c</label>Instituut voor Tropische Geneeskunde, Antwerp, Belgium</aff><aff id="af020"><label>d</label>Department of Biomedical Sciences, Faculty of Pharmaceutical, Biomedical and Veterinary Sciences, University of Antwerp, Antwerp, Belgium</aff><author-notes><corresp id="cor1"><label>⁎</label>Corresponding author. Address: Bernhard Nocht Institute for Tropical Medicine, Bernhard Nocht St. 74, D20359 Hamburg, Germany. Tel.: +49 40 42818 481; fax: +49 42818 512. <email>clos@bnitm.de</email></corresp><fn id="fn1"><label>1</label><p>Present address: Drug Discovery Unit, Division of Biological Chemistry and Drug Discovery, University of Dundee, Dundee, UK.</p></fn><fn id="fn2"><label>2</label><p>Present address: Heinrich Pette Institute for Experimental Virology, Hamburg, Germany.</p></fn><fn id="fn3"><label>3</label><p>Present address: Institute for Medical Microbiology, Virology and Hygiene, Hamburg, Germany.</p></fn><fn id="fn4"><label>4</label><p>Present address: Euroimmun AG, Division Medical Scientific Information, Lübeck, Germany.</p></fn></author-notes><pub-date pub-type="pmc-release"><day>6</day><month>12</month><year>2013</year></pub-date><pmc-comment> PMC Release delay is 0 months and 0 days and was
based on .</pmc-comment>
<pub-date pub-type="epub"><day>6</day><month>12</month><year>2013</year></pub-date><pub-date pub-type="collection"><month>4</month><year>2014</year></pub-date><volume>4</volume><issue>1</issue><fpage>37</fpage><lpage>47</lpage><history><date date-type="received"><day>24</day><month>8</month><year>2013</year></date><date date-type="rev-recd"><day>22</day><month>11</month><year>2013</year></date><date date-type="accepted"><day>25</day><month>11</month><year>2013</year></date></history><permissions><copyright-statement>© 2013 The Authors</copyright-statement><copyright-year>2013</copyright-year><license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by-nc-nd/3.0/"><license-p>This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial-No Derivative Works License, which permits non-commercial use, distribution, and reproduction in any medium, provided the original author and source are credited.</license-p></license></permissions><abstract abstract-type="graphical"><title>Graphical abstract</title><fig id="f0025" position="anchor"><graphic xlink:href="fx1"></graphic></fig></abstract><abstract abstract-type="author-highlights"><title>Highlights</title><p><list list-type="simple"><list-item id="o0005"><label>•</label><p>Functional cloning identifies a <italic>Leishmania</italic>-specific 58 kD antimony resistance marker, ARM58.</p></list-item><list-item id="o0010"><label>•</label><p>ARM58 overexpression confers antimony resistance.</p></list-item><list-item id="o0015"><label>•</label><p>A neighbouring, structurally related gene lacks antimony resistance function.</p></list-item><list-item id="o0020"><label>•</label><p>ARM58 comprises 4 related domains of unknown function, classified as DUF1935.</p></list-item><list-item id="o0025"><label>•</label><p>Cosmid-based functional cloning is feasible in <italic>L. braziliensis</italic> in spite of RNAi.</p></list-item></list></p></abstract><abstract><p>Protozoa of the <italic>Leishmania</italic> genus cause a variety of disease forms that rank at the top of the list of neglected tropical diseases. Anti-leishmanial drugs based on pentavalent antimony have been the mainstay of therapy for over 60 years and resistance against them is increasingly encountered in the field. The biochemical basis for this is poorly understood and likely diverse. No stringent correlation between genetic markers and antimony resistance has so far been shown, prompting us to use a functional cloning approach to identify markers of resistance. Using gene libraries derived from drug-resistant and drug-sensitive <italic>Leishmania braziliensis</italic> clinical isolates in a functional cloning strategy, we repeatedly selected one gene locus located on chromosome 20 whose amplification confers increased antimony (III) resistance <italic>in vitro</italic> to an otherwise sensitive <italic>L. braziliensis</italic> clone. The gene responsible for the effect encodes a previously hypothetical protein that we dubbed LbrARM58. It comprises four repeats of a domain of unknown function, DUF1935, one of them harbouring a potential trans-membrane domain. The gene is so far unique to the <italic>Leishmania</italic> genus, while a structurally related gene without antimony resistance functionality is also found in <italic>Trypanosoma</italic> spp. Overexpression of LbrARM58 also confers antimony resistance to promastigotes and intracellular amastigotes of the related species <italic>Leishmania infantum</italic>, indicating a conserved function in Old World and New World <italic>Leishmania</italic> species. Our results also show that in spite of their RNAi system, <italic>L. braziliensis</italic> promastigotes can serve as acceptor cells for episomally propagated cosmid libraries, at least for the initial stages of functional cloning efforts.</p></abstract><kwd-group><title>Keywords</title><kwd><italic>Leishmania braziliensis</italic></kwd><kwd>Antimony</kwd><kwd>Resistance</kwd></kwd-group></article-meta></front><floats-group><fig id="f0005"><label>Fig. 1</label><caption><p>(A) Sequence alignment between the experimentally determined insert sequence of pcosC1.6 and <italic>L. braziliensis</italic> chromosome 20. The 5′ ∼15 kb of the insert align in reverse complimentary direction with the 5′ end of chromosome 20, whilst the C′-terminal 24 kb align in colinear fashion with chromosome 20 sequences between positions 56 and 80 kb. (B) Schematic representation of the overlapping genomic DNA inserts of cosmid C1.6, A3 and B1. Eight open reading frames (ORFs) are present in all three cosmid inserts. The four digit gene numbers correspond to the systematic numbers for chromosome 20 (LbrM20.____) derived from version 2 of the <italic>L. braziliensis</italic> genome project. The total length of each insert (to the right in [bp]) was derived from end-sequencing. Green boxes symbolise ORFs for hypothetical proteins, orange boxes stand for conserved hypothetical proteins, and yellow boxes signify coding regions for proteins with predicted functions. Hatched boxes stand for incomplete ORFs. Vertical dotted lines connect identical ORFs found in all 3 cosmids. Note that the sequence was incomplete in the genome project, causing the apparent non-linear numbering of gene candidates. (C) Truncation of cosmid insert C1.6. The inserts of seven deletion constructs derived from the cosmid pcosC1.6 are schematically shown. The deletions are represented by the dashed lines. The positions of <italic>Afl</italic>II, <italic>Bam</italic>HI, <italic>Bcl</italic>I, <italic>Spe</italic>I and <italic>Xba</italic>I restriction sites are shown on insert C1.6. (D) Recovery rates [%] of cosmid pcosC1.6 and its truncated derivatives after selection in <italic>L. infantum</italic>. Promastigotes transfected with pcosC1.6 and any of the truncated variants (pcos-a to pcos-e, pcos210, pcos220) were mixed at equal ratio (C<sub>0</sub>). Two control cultures cultivated without Sb<sup>III</sup> for 12 days (C<sub>12</sub>) or 21 days (C<sub>21</sub>) were analysed along with the cultures selected at 500 μM Sb<sup>III</sup> for 12 days (S<sub>12</sub>) or at 400 μM Sb<sup>III</sup> for 21 days (S<sub>21</sub>). Episomes from surviving parasites were isolated and used for transformation of <italic>E. coli</italic>. From each transformation, the cosmid DNAs from 50 bacterial colonies were characterised by RFLA, and the share [%] of each cosmid type is displayed.</p></caption><graphic xlink:href="gr1"></graphic></fig><fig id="f0010"><label>Fig. 2</label><caption><p>(A) Dose–effect of antimonyl tartrate (Sb<sup>III</sup>) on the growth of <italic>L. braziliensis</italic> strains PER104 and PER002 transfected with cosmid pcosTL or pcosC1.6 respectively. Growth at 0 μM Sb<sup>III</sup> was defined as 100%. The dashed arrows indicate the 50% inhibiting concentration (IC<sub>50</sub>). Significance (IC<sub>50</sub>): <italic>p</italic> = 0.002, <italic>n</italic> = 6. (B) Effect of pcosC1.6 in <italic>L. infantum</italic>. Empty vector pcosTL and cosmid pcosC1.6 were transfected into <italic>L. infantum</italic> and selected under G418. Cells of both recombinant populations (5 × 10<sup>5</sup> cells ml<sup>−1</sup>) were grown under the indicated Sb<sup>III</sup> concentrations for 72 h. The diagram shows the cell density after 72 h relative to the control culture (0 μM Sb<sup>III</sup>). Numerical IC<sub>50</sub> values are indicated. Significance (IC<sub>50</sub>) <italic>p</italic> = 0.016, <italic>n</italic> = 5. (C) Constructs pcos-210, pcos-220, and the empty vector pcosTL were transfected into <italic>L. infantum</italic> and selected under G418. Cells of each recombinant population (5 × 10<sup>5</sup> cells ml<sup>−1</sup>) were challenged with the indicated Sb<sup>III</sup> concentrations for 72 h. The diagram shows the cell density after 72 h relative to the control culture (0 μM Sb<sup>III</sup>). The bars indicate the mean error. Significance (IC<sub>50</sub>) <italic>p</italic> = 0.008, <italic>n</italic> = 5. (D) Control of LbrM20.0210 expression by qPCR. Expression mediated by cosmid pcosC1.6 was given the value 1. Note that <italic>L. infantum</italic> expresses a homologous gene that is not amplified by the species-specific primers. Thus, the degree of overexpression cannot be determined. (E) Quantification of LbrM20.0210 expression in <italic>L. braziliensis</italic> strains PER002[pcosTL] and PER002cl7[pcosC1.6]. Expression in the control strain PER002cl7[pcosTL] was assigned the value 1. <italic>n</italic> = 6. The standard error of means is depicted.</p></caption><graphic xlink:href="gr2"></graphic></fig><fig id="f0015"><label>Fig. 3</label><caption><p>(A) Infection rate in bone marrow-derived macrophages under Sb<sup>V</sup> challenge. BMMs were infected with stationary growth phase <italic>L. infantum</italic> transfected either with vector pcosTL or with pcos-210. After removal of free parasites, the infected macrophages were incubated in the absence or presence of 160 μg ml<sup>−1</sup> Pentostam®. After 72 h, the cells were fixed with ice–cold methanol, stained with DAPI, and subjected to fluorescence microscopy. For each dataset, 100 macrophages were examined for the presence of parasites. Experiments were performed in quadruplicate and on separate days. The median infection rates are indicated by horizontal bars. Significance (*<italic>p</italic> = 0.029) was tested using the Mann–Whitney ranking test. <italic>n</italic> = 4. (B) Basic expression rate of ARM58 in two clinical isolates of <italic>L. braziliensis</italic>, PER002 (Sb<sup>III</sup> sensitive) and PER104 (Sb<sup>III</sup> resistant), measured by qPCR. Experiments were done in duplicate, arbitrary units. (C) ARM58 RNA expression in <italic>L. braziliensis</italic> populations under various selective pressure. Clone PER002cl7[pcos-210] was subjected to <italic>in vitro</italic> passage for 4 weeks with twice-weekly medium changes. The populations were kept without selection (2), under 50 μg ml<sup>−1</sup> G418 (3), under 3 μM Sb<sup>III</sup> (4), or under 10 μM Sb<sup>III</sup> (5). The PER002cl7 wild type was used for normalisation (1). Cultures were grown in duplicate, qPCR was done in duplicate for each culture (<italic>n</italic> = 4). The bars indicate the medians. Asterisks indicate significance (<sup>∗</sup><italic>p</italic> ⩽ 0.05).</p></caption><graphic xlink:href="gr3"></graphic></fig><fig id="f0020"><label>Fig. 4</label><caption><p>(A) ORF maps of the region around LbrM20.0210 for 5 <italic>Leishmania</italic> species and <italic>Trypanosoma brucei</italic>. (B) Phylogeny tree for LbrM20.0210 and LbrM20.0200. UPGMA algorithm, bootstrap analysis (1000 reps), uncorrected. Gene numbers are underlaid with colours red (for LbrM20.0210 orthologs) or yellow (LbrM20.0200 orthologs). (C) Domain structures for LbrM20.0210 and -0200. DUF = domain of unknown function. Domains are numbered sequentially in Roman numerals (I–IV) from N terminus to C terminus. Sequence conservation for each domain is indicated (<italic>I</italic> = identity, <italic>S</italic> = side chain similarity). Length markers in [amino acids] are given below. (D) Transmembrane domain prediction for LbrM20.0210 using the TMpred algorithm (<ext-link ext-link-type="uri" xlink:href="http://www.ch.embnet.org/software/TMPRED_form.html" id="ir0020">http://www.ch.embnet.org/software/TMPRED_form.html</ext-link>). Note the peak (score 792/819 i>o/o>i) corresponding to domain DUF1935-III and exceeding the threshold score of 500.</p></caption><graphic xlink:href="gr4"></graphic></fig><table-wrap id="t0005" position="float"><label>Table 1</label><caption><p>Outcomes for 6 independent selection screens.</p></caption><table frame="hsides" rules="groups"><thead><tr><th>Selection</th><th>Acceptor strain</th><th>Donor strain</th><th>Sb<sup>III</sup> (μM)</th><th>Time (d)</th><th>Selected cosmids (%)</th><th>Chromosome/region</th></tr></thead><tbody><tr><td>S1.1</td><td>PER002</td><td>PER104</td><td align="char">25</td><td align="char">18</td><td>C1.6 (66)</td><td>20/903 984–946 647</td></tr><tr><td>S1.2</td><td>PER002</td><td>PER104</td><td align="char">90</td><td align="char">33</td><td>C1.6 (90)</td><td>20/903 984–946 647</td></tr><tr><td>S1.3</td><td>PER002</td><td>PER104</td><td align="char">90</td><td align="char">15</td><td>C1.6 (98)</td><td>20/903 984–946 647</td></tr><tr><td>S2.1</td><td>PER002</td><td>PER002</td><td align="char">75</td><td align="char">17</td><td>A3 (10)</td><td>20/913 015–951 701</td></tr><tr><td>S2.2</td><td>PER002</td><td>PER002</td><td align="char">75</td><td align="char">17</td><td>A3 (96)</td><td>20/913 015–951 701</td></tr><tr><td>S3</td><td><italic>L. peruviana</italic></td><td>PER104</td><td align="char">15</td><td align="char">30</td><td>B1 (40)</td><td>20/908 315–951 075</td></tr></tbody></table><table-wrap-foot><fn><p>Screens S1.1–S1.3 were performed using the Sb<sup>III</sup> sensitive strain PER002 and a cosmid library derived from the Sb<sup>III</sup> resistant strain PER104; screens S2.1.1 and S2.1.2 were consecutively performed using PER002 both as donor and acceptor, and screen 3 was performed using <italic>L. peruviana</italic> as receptor and strain PER104 as donor. Sb<sup>III</sup> concentrations (column 3) and selection time (column 4) varied depending on antimony batch variations. The dominant selected cosmids and their share of the overall recovered cosmids are given in column 5, while the corresponding chromosomal regions are given in column 6.</p></fn></table-wrap-foot></table-wrap></floats-group></pmc><affiliations><list><country><li>Allemagne</li><li>Belgique</li><li>Pérou</li></country><region><li>Province d'Anvers</li></region><settlement><li>Anvers</li></settlement><orgName><li>Université d'Anvers</li></orgName></list><tree><country name="Allemagne"><noRegion><name sortKey="Nuhs, Andrea" sort="Nuhs, Andrea" uniqKey="Nuhs A" first="Andrea" last="Nühs">Andrea Nühs</name></noRegion><name sortKey="Clos, Joachim" sort="Clos, Joachim" uniqKey="Clos J" first="Joachim" last="Clos">Joachim Clos</name><name sortKey="Sch Fer, Carola" sort="Sch Fer, Carola" uniqKey="Sch Fer C" first="Carola" last="Sch Fer">Carola Sch Fer</name><name sortKey="Schmidt, Sonja" sort="Schmidt, Sonja" uniqKey="Schmidt S" first="Sonja" last="Schmidt">Sonja Schmidt</name><name sortKey="Tejera Nevado, Paloma" sort="Tejera Nevado, Paloma" uniqKey="Tejera Nevado P" first="Paloma" last="Tejera Nevado">Paloma Tejera Nevado</name><name sortKey="Trube, Leona" sort="Trube, Leona" uniqKey="Trube L" first="Leona" last="Trübe">Leona Trübe</name><name sortKey="Zander, Dorothea" sort="Zander, Dorothea" uniqKey="Zander D" first="Dorothea" last="Zander">Dorothea Zander</name></country><country name="Pérou"><noRegion><name sortKey="Arevalo, Jorge" sort="Arevalo, Jorge" uniqKey="Arevalo J" first="Jorge" last="Arevalo">Jorge Arevalo</name></noRegion><name sortKey="Adaui, Vanessa" sort="Adaui, Vanessa" uniqKey="Adaui V" first="Vanessa" last="Adaui">Vanessa Adaui</name></country><country name="Belgique"><region name="Province d'Anvers"><name sortKey="Maes, Louis" sort="Maes, Louis" uniqKey="Maes L" first="Louis" last="Maes">Louis Maes</name></region><name sortKey="Dujardin, Jean Claude" sort="Dujardin, Jean Claude" uniqKey="Dujardin J" first="Jean-Claude" last="Dujardin">Jean-Claude Dujardin</name><name sortKey="Dujardin, Jean Claude" sort="Dujardin, Jean Claude" uniqKey="Dujardin J" first="Jean-Claude" last="Dujardin">Jean-Claude Dujardin</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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