Both asymmetric mitotic segregation and cell-to-cell invasion are required for stable germline transmission of Wolbachia in filarial nematodes
Identifieur interne : 003B87 ( Pmc/Curation ); précédent : 003B86; suivant : 003B88Both asymmetric mitotic segregation and cell-to-cell invasion are required for stable germline transmission of Wolbachia in filarial nematodes
Auteurs : Frédéric Landmann [États-Unis] ; Odile Bain [France] ; Coralie Martin [France] ; Shigehiko Uni [Malaisie] ; Mark J. Taylor [Royaume-Uni] ; William Sullivan [États-Unis]Source :
- Biology Open [ 2046-6390 ] ; 2012.
Abstract
Parasitic filarial nematodes that belong to the Onchocercidae family live in mutualism with
Url:
DOI: 10.1242/bio.2012737
PubMed: 23213446
PubMed Central: 3509449
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Both asymmetric mitotic segregation and cell-to-cell invasion are required for stable germline transmission of <italic>Wolbachia</italic> in filarial nematodes</title><author><name sortKey="Landmann, Frederic" sort="Landmann, Frederic" uniqKey="Landmann F" first="Frédéric" last="Landmann">Frédéric Landmann</name><affiliation wicri:level="1"><nlm:aff id="aff1"><institution>Department of Molecular, Cell and Developmental Biology, Sinsheimer Laboratories, University of California</institution>,<addr-line>Santa Cruz, CA 95064</addr-line>,<country>USA</country></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Bain, Odile" sort="Bain, Odile" uniqKey="Bain O" first="Odile" last="Bain">Odile Bain</name><affiliation wicri:level="1"><nlm:aff id="aff2"><institution>UMR 7205 OSEB MNHN CNRS and UMR 7245 MCAM MNHN CNRS, Muséum National d'Histoire Naturelle</institution>,<addr-line>61 rue Buffon, CP52, 75231 Paris Cedex 05</addr-line>,<country>France</country></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Martin, Coralie" sort="Martin, Coralie" uniqKey="Martin C" first="Coralie" last="Martin">Coralie Martin</name><affiliation wicri:level="1"><nlm:aff id="aff2"><institution>UMR 7205 OSEB MNHN CNRS and UMR 7245 MCAM MNHN CNRS, Muséum National d'Histoire Naturelle</institution>,<addr-line>61 rue Buffon, CP52, 75231 Paris Cedex 05</addr-line>,<country>France</country></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Uni, Shigehiko" sort="Uni, Shigehiko" uniqKey="Uni S" first="Shigehiko" last="Uni">Shigehiko Uni</name><affiliation wicri:level="1"><nlm:aff id="aff3"><institution>Institute of Biological Sciences, Faculty of Science, University of Malaya</institution>,<addr-line>50603 Kuala Lumpur</addr-line>,<country>Malaysia</country></nlm:aff><country xml:lang="fr">Malaisie</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Taylor, Mark J" sort="Taylor, Mark J" uniqKey="Taylor M" first="Mark J." last="Taylor">Mark J. Taylor</name><affiliation wicri:level="1"><nlm:aff id="aff4"><institution>Molecular and Biochemical Parasitology, Liverpool School of Tropical Medicine</institution>,<addr-line>Liverpool L3 5QA</addr-line>,<country>UK</country></nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Sullivan, William" sort="Sullivan, William" uniqKey="Sullivan W" first="William" last="Sullivan">William Sullivan</name><affiliation wicri:level="1"><nlm:aff id="aff1"><institution>Department of Molecular, Cell and Developmental Biology, Sinsheimer Laboratories, University of California</institution>,<addr-line>Santa Cruz, CA 95064</addr-line>,<country>USA</country></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">23213446</idno><idno type="pmc">3509449</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3509449</idno><idno type="RBID">PMC:3509449</idno><idno type="doi">10.1242/bio.2012737</idno><date when="2012">2012</date><idno type="wicri:Area/Pmc/Corpus">003B88</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">003B88</idno><idno type="wicri:Area/Pmc/Curation">003B87</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">003B87</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Both asymmetric mitotic segregation and cell-to-cell invasion are required for stable germline transmission of <italic>Wolbachia</italic> in filarial nematodes</title><author><name sortKey="Landmann, Frederic" sort="Landmann, Frederic" uniqKey="Landmann F" first="Frédéric" last="Landmann">Frédéric Landmann</name><affiliation wicri:level="1"><nlm:aff id="aff1"><institution>Department of Molecular, Cell and Developmental Biology, Sinsheimer Laboratories, University of California</institution>,<addr-line>Santa Cruz, CA 95064</addr-line>,<country>USA</country></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Bain, Odile" sort="Bain, Odile" uniqKey="Bain O" first="Odile" last="Bain">Odile Bain</name><affiliation wicri:level="1"><nlm:aff id="aff2"><institution>UMR 7205 OSEB MNHN CNRS and UMR 7245 MCAM MNHN CNRS, Muséum National d'Histoire Naturelle</institution>,<addr-line>61 rue Buffon, CP52, 75231 Paris Cedex 05</addr-line>,<country>France</country></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Martin, Coralie" sort="Martin, Coralie" uniqKey="Martin C" first="Coralie" last="Martin">Coralie Martin</name><affiliation wicri:level="1"><nlm:aff id="aff2"><institution>UMR 7205 OSEB MNHN CNRS and UMR 7245 MCAM MNHN CNRS, Muséum National d'Histoire Naturelle</institution>,<addr-line>61 rue Buffon, CP52, 75231 Paris Cedex 05</addr-line>,<country>France</country></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Uni, Shigehiko" sort="Uni, Shigehiko" uniqKey="Uni S" first="Shigehiko" last="Uni">Shigehiko Uni</name><affiliation wicri:level="1"><nlm:aff id="aff3"><institution>Institute of Biological Sciences, Faculty of Science, University of Malaya</institution>,<addr-line>50603 Kuala Lumpur</addr-line>,<country>Malaysia</country></nlm:aff><country xml:lang="fr">Malaisie</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Taylor, Mark J" sort="Taylor, Mark J" uniqKey="Taylor M" first="Mark J." last="Taylor">Mark J. Taylor</name><affiliation wicri:level="1"><nlm:aff id="aff4"><institution>Molecular and Biochemical Parasitology, Liverpool School of Tropical Medicine</institution>,<addr-line>Liverpool L3 5QA</addr-line>,<country>UK</country></nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Sullivan, William" sort="Sullivan, William" uniqKey="Sullivan W" first="William" last="Sullivan">William Sullivan</name><affiliation wicri:level="1"><nlm:aff id="aff1"><institution>Department of Molecular, Cell and Developmental Biology, Sinsheimer Laboratories, University of California</institution>,<addr-line>Santa Cruz, CA 95064</addr-line>,<country>USA</country></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author></analytic><series><title level="j">Biology Open</title><idno type="eISSN">2046-6390</idno><imprint><date when="2012">2012</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><title>Summary</title><p>Parasitic filarial nematodes that belong to the Onchocercidae family live in mutualism with <italic>Wolbachia</italic> endosymbionts. We developed whole-mount techniques to follow the segregation patterns of <italic>Wolbachia</italic> through the somatic and germline lineages of four filarial species. These studies reveal multiple evolutionarily conserved mechanisms that are required for <italic>Wolbachia</italic> localization to the germline. During the initial embryonic divisions, <italic>Wolbachia</italic> segregate asymmetrically such that they concentrate in the posteriorly localized P<sub>2</sub> blastomere, a precursor to the adult germline and hypodermal lineages. Surprisingly, in the next division they are excluded from the germline precursor lineage. Rather, they preferentially segregate to the C blastomere, a source of posterior hypodermal cells. Localization to the germline is accomplished by a distinct mechanism in which <italic>Wolbachia</italic> invade first the somatic gonadal cells close to the ovarian distal tip cell, the nematode stem cell niche, from the hypodermis. This tropism is associated with a cortical F-actin disruption, suggesting an active engulfment. Significantly, germline invasion occurs only in females, explaining the lack of <italic>Wolbachia</italic> in the male germline. Once in the syncytial environment of the ovaries, <italic>Wolbachia</italic> rely on the rachis to multiply and disperse into the germ cells. The utilization of cell-to-cell invasion for germline colonization may indicate an ancestral mode of horizontal transfer that preceded the acquisition of the mutualism.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Abi Rached, M" uniqKey="Abi Rached M">M. Abi-Rached</name></author><author><name sortKey="Brun, J" uniqKey="Brun J">J. Brun</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Alper, S" uniqKey="Alper S">S. Alper</name></author><author><name sortKey="Podbilewicz, B" uniqKey="Podbilewicz B">B. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Biol Open</journal-id><journal-id journal-id-type="iso-abbrev">Biol Open</journal-id><journal-id journal-id-type="hwp">biolopen</journal-id><journal-id journal-id-type="publisher-id">bio</journal-id><journal-title-group><journal-title>Biology Open</journal-title></journal-title-group><issn pub-type="epub">2046-6390</issn><publisher><publisher-name>The Company of Biologists</publisher-name><publisher-loc>Bidder Building, 140 Cowley Road, Cambridge, CB4 0DL, UK</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">23213446</article-id><article-id pub-id-type="pmc">3509449</article-id><article-id pub-id-type="publisher-id">BIO2012737</article-id><article-id pub-id-type="doi">10.1242/bio.2012737</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group></article-categories><title-group><article-title>Both asymmetric mitotic segregation and cell-to-cell invasion are required for stable germline transmission of <italic>Wolbachia</italic> in filarial nematodes</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Landmann</surname><given-names>Frédéric</given-names></name><xref ref-type="aff" rid="aff1">1</xref><xref ref-type="corresp" rid="cor1">*</xref></contrib><contrib contrib-type="author"><name><surname>Bain</surname><given-names>Odile</given-names></name><xref ref-type="aff" rid="aff2">2</xref></contrib><contrib contrib-type="author"><name><surname>Martin</surname><given-names>Coralie</given-names></name><xref ref-type="aff" rid="aff2">2</xref></contrib><contrib contrib-type="author"><name><surname>Uni</surname><given-names>Shigehiko</given-names></name><xref ref-type="aff" rid="aff3">3</xref></contrib><contrib contrib-type="author"><name><surname>Taylor</surname><given-names>Mark J.</given-names></name><xref ref-type="aff" rid="aff4">4</xref></contrib><contrib contrib-type="author"><name><surname>Sullivan</surname><given-names>William</given-names></name><xref ref-type="aff" rid="aff1">1</xref></contrib></contrib-group><aff id="aff1"><label>1</label><institution>Department of Molecular, Cell and Developmental Biology, Sinsheimer Laboratories, University of California</institution>,<addr-line>Santa Cruz, CA 95064</addr-line>,<country>USA</country></aff><aff id="aff2"><label>2</label><institution>UMR 7205 OSEB MNHN CNRS and UMR 7245 MCAM MNHN CNRS, Muséum National d'Histoire Naturelle</institution>,<addr-line>61 rue Buffon, CP52, 75231 Paris Cedex 05</addr-line>,<country>France</country></aff><aff id="aff3"><label>3</label><institution>Institute of Biological Sciences, Faculty of Science, University of Malaya</institution>,<addr-line>50603 Kuala Lumpur</addr-line>,<country>Malaysia</country></aff><aff id="aff4"><label>4</label><institution>Molecular and Biochemical Parasitology, Liverpool School of Tropical Medicine</institution>,<addr-line>Liverpool L3 5QA</addr-line>,<country>UK</country></aff><author-notes><corresp id="cor1"><label>*</label>Author for correspondence (<email>landmann@biology.ucsc.edu</email>)</corresp></author-notes><pub-date pub-type="collection"><day>15</day><month>6</month><year>2012</year></pub-date><pub-date pub-type="epub"><day>18</day><month>4</month><year>2012</year></pub-date><volume>1</volume><issue>6</issue><fpage>536</fpage><lpage>547</lpage><permissions><copyright-statement>© 2012. Published by The Company of Biologists Ltd</copyright-statement><copyright-year>2012</copyright-year><license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by-nc-sa/3.0"><license-p>This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial Share Alike License (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by-nc-sa/3.0/">http://creativecommons.org/licenses/by-nc-sa/3.0/</ext-link>).</license-p></license></permissions><abstract><title>Summary</title><p>Parasitic filarial nematodes that belong to the Onchocercidae family live in mutualism with <italic>Wolbachia</italic> endosymbionts. We developed whole-mount techniques to follow the segregation patterns of <italic>Wolbachia</italic> through the somatic and germline lineages of four filarial species. These studies reveal multiple evolutionarily conserved mechanisms that are required for <italic>Wolbachia</italic> localization to the germline. During the initial embryonic divisions, <italic>Wolbachia</italic> segregate asymmetrically such that they concentrate in the posteriorly localized P<sub>2</sub> blastomere, a precursor to the adult germline and hypodermal lineages. Surprisingly, in the next division they are excluded from the germline precursor lineage. Rather, they preferentially segregate to the C blastomere, a source of posterior hypodermal cells. Localization to the germline is accomplished by a distinct mechanism in which <italic>Wolbachia</italic> invade first the somatic gonadal cells close to the ovarian distal tip cell, the nematode stem cell niche, from the hypodermis. This tropism is associated with a cortical F-actin disruption, suggesting an active engulfment. Significantly, germline invasion occurs only in females, explaining the lack of <italic>Wolbachia</italic> in the male germline. Once in the syncytial environment of the ovaries, <italic>Wolbachia</italic> rely on the rachis to multiply and disperse into the germ cells. The utilization of cell-to-cell invasion for germline colonization may indicate an ancestral mode of horizontal transfer that preceded the acquisition of the mutualism.</p></abstract><kwd-group><kwd><italic>Wolbachia</italic></kwd><kwd>Bacteria</kwd><kwd>Filarial nematodes</kwd><kwd>Mutualism</kwd><kwd>Parasite</kwd><kwd>Symbiosis</kwd></kwd-group></article-meta></front></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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