Riboswitches in eubacteria sense the second messenger c-di-AMP
Identifieur interne : 000271 ( Pmc/Checkpoint ); précédent : 000270; suivant : 000272Riboswitches in eubacteria sense the second messenger c-di-AMP
Auteurs : James W. Nelson [États-Unis] ; Narasimhan Sudarsan [États-Unis] ; Kazuhiro Furukawa [États-Unis] ; Zasha Weinberg [États-Unis] ; Joy X. Wang [États-Unis] ; Ronald R. Breaker [États-Unis]Source :
- Nature chemical biology [ 1552-4450 ] ; 2013.
Abstract
Cyclic di-adenosine monophosphate (c-di-AMP) is a recently discovered bacterial second messenger implicated in the control of cell wall metabolism, osmotic stress responses, and sporulation. However, the mechanisms by which c-di-AMP triggers these physiological responses have remained largely unknown. Intriguingly, a candidate riboswitch class called
Url:
DOI: 10.1038/nchembio.1363
PubMed: 24141192
PubMed Central: 3830699
Affiliations:
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Nelson</name><affiliation wicri:level="2"><nlm:aff id="A1">Department of Chemistry, Yale University, Box 208107, New Haven, CT 06520, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Chemistry, Yale University, Box 208107, New Haven, CT 06520</wicri:regionArea><placeName><region type="state">Connecticut</region></placeName></affiliation></author><author><name sortKey="Sudarsan, Narasimhan" sort="Sudarsan, Narasimhan" uniqKey="Sudarsan N" first="Narasimhan" last="Sudarsan">Narasimhan Sudarsan</name><affiliation wicri:level="2"><nlm:aff id="A2">Howard Hughes Medical Institute, Yale University, Box 208103, New Haven, CT 06520, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Howard Hughes Medical Institute, Yale University, Box 208103, New Haven, CT 06520</wicri:regionArea><placeName><region type="state">Connecticut</region></placeName></affiliation><affiliation wicri:level="2"><nlm:aff id="A3">Department of Molecular, Cellular and Developmental Biology, Yale University, Box 208103, New Haven, CT 06520, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Molecular, Cellular and Developmental Biology, Yale University, Box 208103, New Haven, CT 06520</wicri:regionArea><placeName><region type="state">Connecticut</region></placeName></affiliation></author><author><name sortKey="Furukawa, Kazuhiro" sort="Furukawa, Kazuhiro" uniqKey="Furukawa K" first="Kazuhiro" last="Furukawa">Kazuhiro Furukawa</name><affiliation wicri:level="2"><nlm:aff id="A3">Department of Molecular, Cellular and Developmental Biology, Yale University, Box 208103, New Haven, CT 06520, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Molecular, Cellular and Developmental Biology, Yale University, Box 208103, New Haven, CT 06520</wicri:regionArea><placeName><region type="state">Connecticut</region></placeName></affiliation></author><author><name sortKey="Weinberg, Zasha" sort="Weinberg, Zasha" uniqKey="Weinberg Z" first="Zasha" last="Weinberg">Zasha Weinberg</name><affiliation wicri:level="2"><nlm:aff id="A2">Howard Hughes Medical Institute, Yale University, Box 208103, New Haven, CT 06520, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Howard Hughes Medical Institute, Yale University, Box 208103, New Haven, CT 06520</wicri:regionArea><placeName><region type="state">Connecticut</region></placeName></affiliation><affiliation wicri:level="2"><nlm:aff id="A3">Department of Molecular, Cellular and Developmental Biology, Yale University, Box 208103, New Haven, CT 06520, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Molecular, Cellular and Developmental Biology, Yale University, Box 208103, New Haven, CT 06520</wicri:regionArea><placeName><region type="state">Connecticut</region></placeName></affiliation></author><author><name sortKey="Wang, Joy X" sort="Wang, Joy X" uniqKey="Wang J" first="Joy X." last="Wang">Joy X. Wang</name><affiliation wicri:level="2"><nlm:aff id="A3">Department of Molecular, Cellular and Developmental Biology, Yale University, Box 208103, New Haven, CT 06520, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Molecular, Cellular and Developmental Biology, Yale University, Box 208103, New Haven, CT 06520</wicri:regionArea><placeName><region type="state">Connecticut</region></placeName></affiliation></author><author><name sortKey="Breaker, Ronald R" sort="Breaker, Ronald R" uniqKey="Breaker R" first="Ronald R." last="Breaker">Ronald R. 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Nelson</name><affiliation wicri:level="2"><nlm:aff id="A1">Department of Chemistry, Yale University, Box 208107, New Haven, CT 06520, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Chemistry, Yale University, Box 208107, New Haven, CT 06520</wicri:regionArea><placeName><region type="state">Connecticut</region></placeName></affiliation></author><author><name sortKey="Sudarsan, Narasimhan" sort="Sudarsan, Narasimhan" uniqKey="Sudarsan N" first="Narasimhan" last="Sudarsan">Narasimhan Sudarsan</name><affiliation wicri:level="2"><nlm:aff id="A2">Howard Hughes Medical Institute, Yale University, Box 208103, New Haven, CT 06520, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Howard Hughes Medical Institute, Yale University, Box 208103, New Haven, CT 06520</wicri:regionArea><placeName><region type="state">Connecticut</region></placeName></affiliation><affiliation wicri:level="2"><nlm:aff id="A3">Department of Molecular, Cellular and Developmental Biology, Yale University, Box 208103, New Haven, CT 06520, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Molecular, Cellular and Developmental Biology, Yale University, Box 208103, New Haven, CT 06520</wicri:regionArea><placeName><region type="state">Connecticut</region></placeName></affiliation></author><author><name sortKey="Furukawa, Kazuhiro" sort="Furukawa, Kazuhiro" uniqKey="Furukawa K" first="Kazuhiro" last="Furukawa">Kazuhiro Furukawa</name><affiliation wicri:level="2"><nlm:aff id="A3">Department of Molecular, Cellular and Developmental Biology, Yale University, Box 208103, New Haven, CT 06520, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Molecular, Cellular and Developmental Biology, Yale University, Box 208103, New Haven, CT 06520</wicri:regionArea><placeName><region type="state">Connecticut</region></placeName></affiliation></author><author><name sortKey="Weinberg, Zasha" sort="Weinberg, Zasha" uniqKey="Weinberg Z" first="Zasha" last="Weinberg">Zasha Weinberg</name><affiliation wicri:level="2"><nlm:aff id="A2">Howard Hughes Medical Institute, Yale University, Box 208103, New Haven, CT 06520, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Howard Hughes Medical Institute, Yale University, Box 208103, New Haven, CT 06520</wicri:regionArea><placeName><region type="state">Connecticut</region></placeName></affiliation><affiliation wicri:level="2"><nlm:aff id="A3">Department of Molecular, Cellular and Developmental Biology, Yale University, Box 208103, New Haven, CT 06520, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Molecular, Cellular and Developmental Biology, Yale University, Box 208103, New Haven, CT 06520</wicri:regionArea><placeName><region type="state">Connecticut</region></placeName></affiliation></author><author><name sortKey="Wang, Joy X" sort="Wang, Joy X" uniqKey="Wang J" first="Joy X." last="Wang">Joy X. Wang</name><affiliation wicri:level="2"><nlm:aff id="A3">Department of Molecular, Cellular and Developmental Biology, Yale University, Box 208103, New Haven, CT 06520, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Molecular, Cellular and Developmental Biology, Yale University, Box 208103, New Haven, CT 06520</wicri:regionArea><placeName><region type="state">Connecticut</region></placeName></affiliation></author><author><name sortKey="Breaker, Ronald R" sort="Breaker, Ronald R" uniqKey="Breaker R" first="Ronald R." last="Breaker">Ronald R. Breaker</name><affiliation wicri:level="2"><nlm:aff id="A2">Howard Hughes Medical Institute, Yale University, Box 208103, New Haven, CT 06520, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Howard Hughes Medical Institute, Yale University, Box 208103, New Haven, CT 06520</wicri:regionArea><placeName><region type="state">Connecticut</region></placeName></affiliation><affiliation wicri:level="2"><nlm:aff id="A3">Department of Molecular, Cellular and Developmental Biology, Yale University, Box 208103, New Haven, CT 06520, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Molecular, Cellular and Developmental Biology, Yale University, Box 208103, New Haven, CT 06520</wicri:regionArea><placeName><region type="state">Connecticut</region></placeName></affiliation><affiliation wicri:level="2"><nlm:aff id="A4">Department of Molecular Biophysics and Biochemistry, Yale University, Box 208103, New Haven, CT 06520, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Molecular Biophysics and Biochemistry, Yale University, Box 208103, New Haven, CT 06520</wicri:regionArea><placeName><region type="state">Connecticut</region></placeName></affiliation></author></analytic><series><title level="j">Nature chemical biology</title><idno type="ISSN">1552-4450</idno><idno type="eISSN">1552-4469</idno><imprint><date when="2013">2013</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p id="P3">Cyclic di-adenosine monophosphate (c-di-AMP) is a recently discovered bacterial second messenger implicated in the control of cell wall metabolism, osmotic stress responses, and sporulation. However, the mechanisms by which c-di-AMP triggers these physiological responses have remained largely unknown. Intriguingly, a candidate riboswitch class called <italic>ydaO</italic> associates with numerous genes involved in these same processes. Although a representative <italic>ydaO</italic> motif RNA recently was reported to weakly bind ATP, we report that numerous members of this noncoding RNA class selectively respond to c-di-AMP with sub-nanomolar affinity. Our findings resolve the mystery regarding the primary ligand for this extremely common riboswitch class and expose a major portion of the super-regulon of genes that are controlled by the widespread bacterial second messenger c-di-AMP.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Romling, U" uniqKey="Romling U">U Römling</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Pesavento, C" uniqKey="Pesavento C">C Pesavento</name></author><author><name sortKey="Hengge, R" uniqKey="Hengge R">R Hengge</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Sondermann, H" uniqKey="Sondermann H">H Sondermann</name></author><author><name sortKey="Shikuma, Nj" uniqKey="Shikuma N">NJ Shikuma</name></author><author><name sortKey="Yildiz, Fh" uniqKey="Yildiz F">FH Yildiz</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Krasteva, Pv" 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<front><journal-meta><journal-id journal-id-type="nlm-journal-id">101231976</journal-id><journal-id journal-id-type="pubmed-jr-id">32624</journal-id><journal-id journal-id-type="nlm-ta">Nat Chem Biol</journal-id><journal-id journal-id-type="iso-abbrev">Nat. Chem. Biol.</journal-id><journal-title-group><journal-title>Nature chemical biology</journal-title></journal-title-group><issn pub-type="ppub">1552-4450</issn><issn pub-type="epub">1552-4469</issn></journal-meta><article-meta><article-id pub-id-type="pmid">24141192</article-id><article-id pub-id-type="pmc">3830699</article-id><article-id pub-id-type="doi">10.1038/nchembio.1363</article-id><article-id pub-id-type="manuscript">NIHMS523513</article-id><article-categories><subj-group subj-group-type="heading"><subject>Article</subject></subj-group></article-categories><title-group><article-title>Riboswitches in eubacteria sense the second messenger c-di-AMP</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Nelson</surname><given-names>James W.</given-names></name><xref ref-type="aff" rid="A1">1</xref></contrib><contrib contrib-type="author"><name><surname>Sudarsan</surname><given-names>Narasimhan</given-names></name><xref ref-type="aff" rid="A2">2</xref><xref ref-type="aff" rid="A3">3</xref></contrib><contrib contrib-type="author"><name><surname>Furukawa</surname><given-names>Kazuhiro</given-names></name><xref ref-type="aff" rid="A3">3</xref><xref ref-type="author-notes" rid="FN1">*</xref></contrib><contrib contrib-type="author"><name><surname>Weinberg</surname><given-names>Zasha</given-names></name><xref ref-type="aff" rid="A2">2</xref><xref ref-type="aff" rid="A3">3</xref></contrib><contrib contrib-type="author"><name><surname>Wang</surname><given-names>Joy X.</given-names></name><xref ref-type="aff" rid="A3">3</xref><xref ref-type="author-notes" rid="FN2">**</xref></contrib><contrib contrib-type="author"><name><surname>Breaker</surname><given-names>Ronald R.</given-names></name><xref ref-type="aff" rid="A2">2</xref><xref ref-type="aff" rid="A3">3</xref><xref ref-type="aff" rid="A4">4</xref><xref ref-type="corresp" rid="CR1">†</xref></contrib></contrib-group><aff id="A1"><label>1</label>Department of Chemistry, Yale University, Box 208107, New Haven, CT 06520, USA</aff><aff id="A2"><label>2</label>Howard Hughes Medical Institute, Yale University, Box 208103, New Haven, CT 06520, USA</aff><aff id="A3"><label>3</label>Department of Molecular, Cellular and Developmental Biology, Yale University, Box 208103, New Haven, CT 06520, USA</aff><aff id="A4"><label>4</label>Department of Molecular Biophysics and Biochemistry, Yale University, Box 208103, New Haven, CT 06520, USA</aff><author-notes><corresp id="CR1"><label>†</label>To whom correspondence should be addressed. Dr. Ronald R. Breaker, Tel: (203) 432-9389, Fax: (203) 432-0753, <email>ronald.breaker@yale.edu</email></corresp><fn fn-type="present-address" id="FN1"><label>*</label><p id="P1">Current address: Faculty of Pharmaceutical Sciences, The University of Tokushima, Tokushima, Japan</p></fn><fn fn-type="present-address" id="FN2"><label>**</label><p id="P2">Current address: Center for Clinical and Translational Metagenomics, Brigham and Women’s Hospital, Boston, MA 02115</p></fn></author-notes><pub-date pub-type="nihms-submitted"><day>28</day><month>10</month><year>2013</year></pub-date><pub-date pub-type="epub"><day>20</day><month>10</month><year>2013</year></pub-date><pub-date pub-type="ppub"><month>12</month><year>2013</year></pub-date><pub-date pub-type="pmc-release"><day>01</day><month>6</month><year>2014</year></pub-date><volume>9</volume><issue>12</issue><fpage>834</fpage><lpage>839</lpage><pmc-comment>elocation-id from pubmed: 10.1038/nchembio.1363</pmc-comment>
<permissions><license><license-p>Users may view, print, copy, download and text and data- mine the content in such documents, for the purposes of academic research, subject always to the full Conditions of use:
<uri xlink:type="simple" xlink:href="http://www.nature.com/authors/editorial_policies/license.html#terms">http://www.nature.com/authors/editorial_policies/license.html#terms</uri></license-p></license></permissions><abstract><p id="P3">Cyclic di-adenosine monophosphate (c-di-AMP) is a recently discovered bacterial second messenger implicated in the control of cell wall metabolism, osmotic stress responses, and sporulation. However, the mechanisms by which c-di-AMP triggers these physiological responses have remained largely unknown. Intriguingly, a candidate riboswitch class called <italic>ydaO</italic> associates with numerous genes involved in these same processes. Although a representative <italic>ydaO</italic> motif RNA recently was reported to weakly bind ATP, we report that numerous members of this noncoding RNA class selectively respond to c-di-AMP with sub-nanomolar affinity. Our findings resolve the mystery regarding the primary ligand for this extremely common riboswitch class and expose a major portion of the super-regulon of genes that are controlled by the widespread bacterial second messenger c-di-AMP.</p></abstract></article-meta></front><floats-group><fig id="F1" orientation="portrait" position="float"><label>Figure 1</label><caption><title>Binding of c-di-AMP by a <italic>ydaO</italic> motif RNA</title><p><bold>a,</bold> Chemical structure of c-di-AMP. <bold>b,</bold> Consensus sequence and secondary structure of <italic>ydaO</italic> motif RNAs derived from ~ 3,000 examples. Red, black and gray nucleotides, respectively, are present in greater than 97, 90 and 75% of the representatives. Predicted base-paired substructures are labeled P1 through P7, with one pseudoknot as indicated. Green shading indicates phylogenetic evidence of base pairing. Other annotations are as described previously<sup><xref rid="R19" ref-type="bibr">19</xref></sup>. <bold>c,</bold> Structural modulation of the WT 165 <italic>ydaO</italic> RNA from <italic>B. subtilis</italic>. Highlighted nucleotides indicate locations of changes in spontaneous cleavage upon addition of c-di-AMP, mapped using the data in <bold>d</bold> and <xref ref-type="supplementary-material" rid="SD1">Supplementary Fig. 3</xref>. <bold>d,</bold> Polyacrylamide gel electrophoresis (PAGE) analysis of an in-line probing assay with 165 <italic>ydaO</italic> RNA exposed to various concentrations of c-di-AMP (100 pM to 10 μM in half-log intervals) or ATP (17.8 μM to 3.16 mM in quarter-log intervals). NR, T1 and <sup>−</sup>OH, respectively, designate no reaction, partial digestion with either RNase T1 (cleaves after guanosine nucleotides) or hydroxide ions (cleaves after any nucleotide). Precursor RNA (Pre) and certain RNase T1 cleavage product bands are identified. Locations of spontaneous RNA cleavage changes brought about by c-di-AMP (regions 1 through 6) are identified by asterisks (see <xref ref-type="supplementary-material" rid="SD1">Supplementary Fig. 14</xref> for the full length gel). <bold>e,</bold> Plot of the fraction of riboswitch RNA bound to ligand versus the logarithm of the molar concentration of c-di-AMP as inferred from the modulation of spontaneous cleavage products in <bold>d</bold>.</p></caption><graphic xlink:href="nihms-523513-f0001"></graphic></fig><fig id="F2" orientation="portrait" position="float"><label>Figure 2</label><caption><title>Ligand binding characteristics of WT and variant 165 <italic>ydaO</italic> RNAs</title><p><bold>a,</bold> Plot of the <italic>K</italic><sub>D</sub> values for the binding of c-di-AMP analogs by WT 165 <italic>ydaO</italic> RNA. A 5′PS is adenosine 5′-phosphosulfate, IMP is inosine 5′-phosphate, c-pGpA is the cyclic dinucleotide composed of one GMP and one AMP (also called cGA), and c-di-dAMP is the DNA analog of c-di-AMP. Gray circle and arrow indicates that the compounds listed exhibit no detectable binding at this concentration. Open circle and arrow indicates the <italic>K</italic><sub>D</sub> for c-di-AMP is no poorer than this value. <bold>b,</bold> Various mutant constructs examined for ligand binding. Nucleotide changes made at the sites annotated M1 through M5 are boxed. Red letters identify highly conserved nucleotides. <bold>c,</bold> In-line probing analyses of WT and M1 through M4 RNAs as defined in b in the absence (−) or presence of 10 nM c-di-AMP. Gel images depict spontaneous RNA cleavage patterns encompassing sites 1 and 2 as defined in <xref ref-type="fig" rid="F1">Fig. 1c</xref> (see <xref ref-type="supplementary-material" rid="SD1">Supplementary Fig. 15</xref> for the full length gel<bold>)</bold>. <bold>d,</bold> In-line probing analysis of M5 in the absence (−) of ligand, or the presence of c-di-AMP (10, 32 or 100 nM), or ATP (1 mM). Gel images depict the region encompassing sites 1 through 6 with annotations as described for <xref ref-type="fig" rid="F1">Fig. 1d</xref>. The arrow identifies nucleotides in the loop region of P7 that become unstructured on ligand binding, as expected since their complementary sequences have been removed in this construct (see <xref ref-type="supplementary-material" rid="SD1">Supplementary Fig. 16</xref> for the full length gel<bold>)</bold>.</p></caption><graphic xlink:href="nihms-523513-f0002"></graphic></fig><fig id="F3" orientation="portrait" position="float"><label>Figure 3</label><caption><title>Riboswitch regulation of gene expression by c-di-AMP</title><p><bold>a</bold>, PAGE analysis of an <italic>in vitro</italic> transcription termination assay using the <italic>yuaA</italic> riboswitch from <italic>B. subtilis</italic>. T is the riboswitch-terminated RNA transcript and FL is the full-length run-off transcript. M is a marker lane comprising the transcription products from a similar DNA template encoding the riboswitch plus six additional nucleotides beyond the predicted terminator site (see <xref ref-type="supplementary-material" rid="SD1">Supplementary Fig. 17</xref> for the full length gel<bold>)</bold>. <bold>b,</bold> Reporter gene construct used to assess regulation by c-di-AMP riboswitches. P is the native <italic>ydaO</italic> promoter, <italic>lacZ</italic> is the reporter gene, and RBS is the ribosome binding site. The predicted intrinsic transcription terminator stem for the <italic>B. subtilis ydaO</italic> riboswitch is shown in detail. <bold>c,</bold> Plot of reporter gene expression for various riboswitch constructs and genetic backgrounds (normal is the YP79 strain of <italic>B. subtilis</italic>) normalized to the level of expression observed with the WT riboswitch construct. Error bars represent the standard deviation of three replicate experiments conducted on three different days.</p></caption><graphic xlink:href="nihms-523513-f0003"></graphic></fig><fig id="F4" orientation="portrait" position="float"><label>Figure 4</label><caption><title>The super-regulon for second messenger signaling through c-di-AMP riboswitches</title><p>Bacterial lineages presented are Actinobacteria (Act), Bacillales (Bac), Clostridia, (Clo) and Cyanobacteria (Cya).</p></caption><graphic xlink:href="nihms-523513-f0004"></graphic></fig></floats-group></pmc><affiliations><list><country><li>États-Unis</li></country><region><li>Connecticut</li></region></list><tree><country name="États-Unis"><region name="Connecticut"><name sortKey="Nelson, James W" sort="Nelson, James W" uniqKey="Nelson J" first="James W." last="Nelson">James W. Nelson</name></region><name sortKey="Breaker, Ronald R" sort="Breaker, Ronald R" uniqKey="Breaker R" first="Ronald R." last="Breaker">Ronald R. Breaker</name><name sortKey="Breaker, Ronald R" sort="Breaker, Ronald R" uniqKey="Breaker R" first="Ronald R." last="Breaker">Ronald R. Breaker</name><name sortKey="Breaker, Ronald R" sort="Breaker, Ronald R" uniqKey="Breaker R" first="Ronald R." last="Breaker">Ronald R. Breaker</name><name sortKey="Furukawa, Kazuhiro" sort="Furukawa, Kazuhiro" uniqKey="Furukawa K" first="Kazuhiro" last="Furukawa">Kazuhiro Furukawa</name><name sortKey="Sudarsan, Narasimhan" sort="Sudarsan, Narasimhan" uniqKey="Sudarsan N" first="Narasimhan" last="Sudarsan">Narasimhan Sudarsan</name><name sortKey="Sudarsan, Narasimhan" sort="Sudarsan, Narasimhan" uniqKey="Sudarsan N" first="Narasimhan" last="Sudarsan">Narasimhan Sudarsan</name><name sortKey="Wang, Joy X" sort="Wang, Joy X" uniqKey="Wang J" first="Joy X." last="Wang">Joy X. Wang</name><name sortKey="Weinberg, Zasha" sort="Weinberg, Zasha" uniqKey="Weinberg Z" first="Zasha" last="Weinberg">Zasha Weinberg</name><name sortKey="Weinberg, Zasha" sort="Weinberg, Zasha" uniqKey="Weinberg Z" first="Zasha" last="Weinberg">Zasha Weinberg</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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