Both asymmetric mitotic segregation and cell-to-cell invasion are required for stable germline transmission of Wolbachia in filarial nematodes
Identifieur interne : 000232 ( France/Analysis ); précédent : 000231; suivant : 000233Both 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
Affiliations:
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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><idno type="wicri:Area/Pmc/Checkpoint">002B43</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Checkpoint">002B43</idno><idno type="wicri:Area/Ncbi/Merge">005395</idno><idno type="wicri:Area/Ncbi/Curation">005395</idno><idno type="wicri:Area/Ncbi/Checkpoint">005395</idno><idno type="wicri:Area/Main/Merge">004510</idno><idno type="wicri:Area/Main/Curation">004489</idno><idno type="wicri:Area/Main/Exploration">004489</idno><idno type="wicri:Area/France/Extraction">000232</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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Labouesse</name></author></analytic></biblStruct></listBibl></div1></back></TEI><affiliations><list><country><li>France</li><li>Malaisie</li><li>Royaume-Uni</li><li>États-Unis</li></country></list><tree><country name="États-Unis"><noRegion><name sortKey="Landmann, Frederic" sort="Landmann, Frederic" uniqKey="Landmann F" first="Frédéric" last="Landmann">Frédéric Landmann</name></noRegion><name sortKey="Sullivan, William" sort="Sullivan, William" uniqKey="Sullivan W" first="William" last="Sullivan">William Sullivan</name></country><country name="France"><noRegion><name sortKey="Bain, Odile" sort="Bain, Odile" uniqKey="Bain O" first="Odile" last="Bain">Odile Bain</name></noRegion><name sortKey="Martin, Coralie" sort="Martin, Coralie" uniqKey="Martin C" first="Coralie" last="Martin">Coralie Martin</name></country><country name="Malaisie"><noRegion><name sortKey="Uni, Shigehiko" sort="Uni, Shigehiko" uniqKey="Uni S" first="Shigehiko" last="Uni">Shigehiko Uni</name></noRegion></country><country name="Royaume-Uni"><noRegion><name sortKey="Taylor, Mark J" sort="Taylor, Mark J" uniqKey="Taylor M" first="Mark J." last="Taylor">Mark J. 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