The Dynamics of P Granule Liquid Droplets Are Regulated by the Caenorhabditis elegans Germline RNA Helicase GLH-1 via Its ATP Hydrolysis Cycle
Abstract Germ granules, also known as P granules in Caenorhabditis elegans, are phase-separated cellular bodies that are frequently found at the perinuclear region of germ cell nuclei in various animals. However... P granules are phase-separated liquid droplets that play important roles in the maint...
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| Veröffentlicht in: | Genetics (Austin) 2020-06, Vol.215 (2), p.421-434 |
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| creator | Chen, Wenjun Hu, Yabing Lang, Charles F Brown, Jordan S Schwabach, Sierra Song, Xiaoyan Zhang, Ying Munro, Edwin Bennett, Karen Zhang, Donglei Lee, Heng-Chi |
| description | Abstract
Germ granules, also known as P granules in Caenorhabditis elegans, are phase-separated cellular bodies that are frequently found at the perinuclear region of germ cell nuclei in various animals. However...
P granules are phase-separated liquid droplets that play important roles in the maintenance of germ cell fate in Caenorhabditis elegans. Both the localization and formation of P granules are highly dynamic, but mechanisms that regulate such processes remain poorly understood. Here, we show evidence that the VASA-like germline RNA helicase GLH-1 couples distinct steps of its ATPase hydrolysis cycle to control the formation and disassembly of P granules. In addition, we found that the phenylalanine-glycine-glycine repeats in GLH-1 promote its localization at the perinucleus. Proteomic analyses of the GLH-1 complex with a GLH-1 mutation that interferes with P granule disassembly revealed transient interactions of GLH-1 with several Argonautes and RNA-binding proteins. Finally, we found that defects in recruiting the P granule component PRG-1 to perinuclear foci in the adult germline correlate with the fertility defects observed in various GLH-1 mutants. Together, our results highlight the versatile roles of an RNA helicase in controlling the formation of liquid droplets in space and time. |
| doi_str_mv | 10.1534/genetics.120.303052 |
| format | Article |
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Germ granules, also known as P granules in Caenorhabditis elegans, are phase-separated cellular bodies that are frequently found at the perinuclear region of germ cell nuclei in various animals. However...
P granules are phase-separated liquid droplets that play important roles in the maintenance of germ cell fate in Caenorhabditis elegans. Both the localization and formation of P granules are highly dynamic, but mechanisms that regulate such processes remain poorly understood. Here, we show evidence that the VASA-like germline RNA helicase GLH-1 couples distinct steps of its ATPase hydrolysis cycle to control the formation and disassembly of P granules. In addition, we found that the phenylalanine-glycine-glycine repeats in GLH-1 promote its localization at the perinucleus. Proteomic analyses of the GLH-1 complex with a GLH-1 mutation that interferes with P granule disassembly revealed transient interactions of GLH-1 with several Argonautes and RNA-binding proteins. Finally, we found that defects in recruiting the P granule component PRG-1 to perinuclear foci in the adult germline correlate with the fertility defects observed in various GLH-1 mutants. Together, our results highlight the versatile roles of an RNA helicase in controlling the formation of liquid droplets in space and time.</description><identifier>ISSN: 0016-6731</identifier><identifier>ISSN: 1943-2631</identifier><identifier>EISSN: 1943-2631</identifier><identifier>DOI: 10.1534/genetics.120.303052</identifier><identifier>PMID: 32245789</identifier><language>eng</language><publisher>CARY: Oxford University Press</publisher><subject>Adenosine triphosphatase ; Adenosine Triphosphate - metabolism ; Animals ; Caenorhabditis elegans ; Caenorhabditis elegans - genetics ; Caenorhabditis elegans - growth & development ; Caenorhabditis elegans - metabolism ; Caenorhabditis elegans Proteins - genetics ; Caenorhabditis elegans Proteins - metabolism ; Cell fate ; CRISPR ; Cytoplasmic Granules - metabolism ; DEAD-box RNA Helicases - genetics ; DEAD-box RNA Helicases - metabolism ; Defects ; Deoxyribonucleic acid ; Dismantling ; DNA ; DNA helicase ; Droplets ; Fertility ; Genetics ; Genetics & Heredity ; Glycine ; Granular materials ; Hydrolysis ; Investigations ; Life Sciences & Biomedicine ; Liquid Crystals - chemistry ; Localization ; Mutation ; Nematodes ; Phenylalanine ; Plasmids ; Proteins ; Proteomics ; RNA helicase ; RNA-binding protein ; Science & Technology ; Young adults</subject><ispartof>Genetics (Austin), 2020-06, Vol.215 (2), p.421-434</ispartof><rights>Genetics 2020 2020</rights><rights>Copyright © 2020 by the Genetics Society of America.</rights><rights>Copyright Genetics Society of America Jun 2020</rights><rights>Genetics 2020</rights><rights>Copyright © 2020 by the Genetics Society of America 2020</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>true</woscitedreferencessubscribed><woscitedreferencescount>19</woscitedreferencescount><woscitedreferencesoriginalsourcerecordid>wos000538153800011</woscitedreferencesoriginalsourcerecordid><citedby>FETCH-LOGICAL-c500t-955a45364b1cf7a41c3378b4791a9670a59bf062a80896ae0f558de1e3faadc43</citedby><cites>FETCH-LOGICAL-c500t-955a45364b1cf7a41c3378b4791a9670a59bf062a80896ae0f558de1e3faadc43</cites><orcidid>0000-0001-8154-906X ; 0000-0001-6428-3941 ; 0000-0002-2720-1414</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,315,782,786,887,27933,27934,28257</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32245789$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Chen, Wenjun</creatorcontrib><creatorcontrib>Hu, Yabing</creatorcontrib><creatorcontrib>Lang, Charles F</creatorcontrib><creatorcontrib>Brown, Jordan S</creatorcontrib><creatorcontrib>Schwabach, Sierra</creatorcontrib><creatorcontrib>Song, Xiaoyan</creatorcontrib><creatorcontrib>Zhang, Ying</creatorcontrib><creatorcontrib>Munro, Edwin</creatorcontrib><creatorcontrib>Bennett, Karen</creatorcontrib><creatorcontrib>Zhang, Donglei</creatorcontrib><creatorcontrib>Lee, Heng-Chi</creatorcontrib><title>The Dynamics of P Granule Liquid Droplets Are Regulated by the Caenorhabditis elegans Germline RNA Helicase GLH-1 via Its ATP Hydrolysis Cycle</title><title>Genetics (Austin)</title><addtitle>GENETICS</addtitle><addtitle>Genetics</addtitle><description>Abstract
Germ granules, also known as P granules in Caenorhabditis elegans, are phase-separated cellular bodies that are frequently found at the perinuclear region of germ cell nuclei in various animals. However...
P granules are phase-separated liquid droplets that play important roles in the maintenance of germ cell fate in Caenorhabditis elegans. Both the localization and formation of P granules are highly dynamic, but mechanisms that regulate such processes remain poorly understood. Here, we show evidence that the VASA-like germline RNA helicase GLH-1 couples distinct steps of its ATPase hydrolysis cycle to control the formation and disassembly of P granules. In addition, we found that the phenylalanine-glycine-glycine repeats in GLH-1 promote its localization at the perinucleus. Proteomic analyses of the GLH-1 complex with a GLH-1 mutation that interferes with P granule disassembly revealed transient interactions of GLH-1 with several Argonautes and RNA-binding proteins. Finally, we found that defects in recruiting the P granule component PRG-1 to perinuclear foci in the adult germline correlate with the fertility defects observed in various GLH-1 mutants. Together, our results highlight the versatile roles of an RNA helicase in controlling the formation of liquid droplets in space and time.</description><subject>Adenosine triphosphatase</subject><subject>Adenosine Triphosphate - metabolism</subject><subject>Animals</subject><subject>Caenorhabditis elegans</subject><subject>Caenorhabditis elegans - genetics</subject><subject>Caenorhabditis elegans - growth & development</subject><subject>Caenorhabditis elegans - metabolism</subject><subject>Caenorhabditis elegans Proteins - genetics</subject><subject>Caenorhabditis elegans Proteins - metabolism</subject><subject>Cell fate</subject><subject>CRISPR</subject><subject>Cytoplasmic Granules - metabolism</subject><subject>DEAD-box RNA Helicases - genetics</subject><subject>DEAD-box RNA Helicases - metabolism</subject><subject>Defects</subject><subject>Deoxyribonucleic acid</subject><subject>Dismantling</subject><subject>DNA</subject><subject>DNA helicase</subject><subject>Droplets</subject><subject>Fertility</subject><subject>Genetics</subject><subject>Genetics & Heredity</subject><subject>Glycine</subject><subject>Granular materials</subject><subject>Hydrolysis</subject><subject>Investigations</subject><subject>Life Sciences & Biomedicine</subject><subject>Liquid Crystals - chemistry</subject><subject>Localization</subject><subject>Mutation</subject><subject>Nematodes</subject><subject>Phenylalanine</subject><subject>Plasmids</subject><subject>Proteins</subject><subject>Proteomics</subject><subject>RNA helicase</subject><subject>RNA-binding protein</subject><subject>Science & Technology</subject><subject>Young adults</subject><issn>0016-6731</issn><issn>1943-2631</issn><issn>1943-2631</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>AOWDO</sourceid><sourceid>EIF</sourceid><sourceid>8G5</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>GUQSH</sourceid><sourceid>M2O</sourceid><recordid>eNqNkl1r2zAUhs3YWLNuv2AwBLspDGf6sGz5ZhDcLSmErYzsWsjycaKiSKlkd_hP7DdPJW3YdjF6pQN6npdz4M2ytwTPCWfFxy04GIyOc0LxnGGGOX2WzUhdsJyWjDzPZhiTMi8rRs6yVzHeYIzLmouX2RmjtOCVqGfZr80O0OXk1D4lId-ja7QMyo0W0NrcjqZDl8EfLAwRLQKg77AdrRqgQ-2EhqQ2CpwPO9V2ZjARgYWtchEtIeytcUn4ukArsEarCGi5XuUE3RmFru7zNtdoNXXB2ykmtZm0hdfZi17ZCG8e3vPsx5fPm2aVr78tr5rFOtcc4yGvOVcFZ2XREt1XqiCasUq0RVUTVZcVVrxue1xSJbCoSwW451x0QID1SnW6YOfZp2PuYWz30GlwQ1BWHoLZqzBJr4z8-8eZndz6O1nRUtSiTAEXDwHB344QB7k3UYO1yoEfo6RMlFTUjNCEvv8HvfFjcOk8SdMhicRM_JcqCOWYM1olih0pHXyMAfrTygTL-1bIx1bI1Ap5bEWy3v157cl5rEECPhyBn9D6PmoDTsMJS73hTKR0kSZCEi2eTjdmUIPxrvGjG5I6P6p-PDxp9d8SlePa</recordid><startdate>20200601</startdate><enddate>20200601</enddate><creator>Chen, Wenjun</creator><creator>Hu, Yabing</creator><creator>Lang, Charles F</creator><creator>Brown, Jordan S</creator><creator>Schwabach, Sierra</creator><creator>Song, Xiaoyan</creator><creator>Zhang, Ying</creator><creator>Munro, Edwin</creator><creator>Bennett, Karen</creator><creator>Zhang, Donglei</creator><creator>Lee, Heng-Chi</creator><general>Oxford University Press</general><general>Oxford Univ Press</general><general>Genetics Society of America</general><scope>AOWDO</scope><scope>BLEPL</scope><scope>DTL</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>4T-</scope><scope>4U-</scope><scope>7QP</scope><scope>7SS</scope><scope>7TK</scope><scope>7TM</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>88I</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>8G5</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>GUQSH</scope><scope>HCIFZ</scope><scope>K9-</scope><scope>K9.</scope><scope>LK8</scope><scope>M0K</scope><scope>M0R</scope><scope>M0S</scope><scope>M1P</scope><scope>M2O</scope><scope>M2P</scope><scope>M7N</scope><scope>M7P</scope><scope>MBDVC</scope><scope>P64</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>Q9U</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-8154-906X</orcidid><orcidid>https://orcid.org/0000-0001-6428-3941</orcidid><orcidid>https://orcid.org/0000-0002-2720-1414</orcidid></search><sort><creationdate>20200601</creationdate><title>The Dynamics of P Granule Liquid Droplets Are Regulated by the Caenorhabditis elegans Germline RNA Helicase GLH-1 via Its ATP Hydrolysis Cycle</title><author>Chen, Wenjun ; Hu, Yabing ; Lang, Charles F ; Brown, Jordan S ; Schwabach, Sierra ; Song, Xiaoyan ; Zhang, Ying ; Munro, Edwin ; Bennett, Karen ; Zhang, Donglei ; Lee, Heng-Chi</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c500t-955a45364b1cf7a41c3378b4791a9670a59bf062a80896ae0f558de1e3faadc43</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Adenosine triphosphatase</topic><topic>Adenosine Triphosphate - metabolism</topic><topic>Animals</topic><topic>Caenorhabditis elegans</topic><topic>Caenorhabditis elegans - genetics</topic><topic>Caenorhabditis elegans - growth & development</topic><topic>Caenorhabditis elegans - metabolism</topic><topic>Caenorhabditis elegans Proteins - genetics</topic><topic>Caenorhabditis elegans Proteins - metabolism</topic><topic>Cell fate</topic><topic>CRISPR</topic><topic>Cytoplasmic Granules - metabolism</topic><topic>DEAD-box RNA Helicases - genetics</topic><topic>DEAD-box RNA Helicases - metabolism</topic><topic>Defects</topic><topic>Deoxyribonucleic acid</topic><topic>Dismantling</topic><topic>DNA</topic><topic>DNA helicase</topic><topic>Droplets</topic><topic>Fertility</topic><topic>Genetics</topic><topic>Genetics & Heredity</topic><topic>Glycine</topic><topic>Granular materials</topic><topic>Hydrolysis</topic><topic>Investigations</topic><topic>Life Sciences & Biomedicine</topic><topic>Liquid Crystals - chemistry</topic><topic>Localization</topic><topic>Mutation</topic><topic>Nematodes</topic><topic>Phenylalanine</topic><topic>Plasmids</topic><topic>Proteins</topic><topic>Proteomics</topic><topic>RNA helicase</topic><topic>RNA-binding protein</topic><topic>Science & Technology</topic><topic>Young adults</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Chen, Wenjun</creatorcontrib><creatorcontrib>Hu, Yabing</creatorcontrib><creatorcontrib>Lang, Charles F</creatorcontrib><creatorcontrib>Brown, Jordan S</creatorcontrib><creatorcontrib>Schwabach, Sierra</creatorcontrib><creatorcontrib>Song, Xiaoyan</creatorcontrib><creatorcontrib>Zhang, Ying</creatorcontrib><creatorcontrib>Munro, Edwin</creatorcontrib><creatorcontrib>Bennett, Karen</creatorcontrib><creatorcontrib>Zhang, Donglei</creatorcontrib><creatorcontrib>Lee, Heng-Chi</creatorcontrib><collection>Web of Science - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Genetics (Austin)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Chen, Wenjun</au><au>Hu, Yabing</au><au>Lang, Charles F</au><au>Brown, Jordan S</au><au>Schwabach, Sierra</au><au>Song, Xiaoyan</au><au>Zhang, Ying</au><au>Munro, Edwin</au><au>Bennett, Karen</au><au>Zhang, Donglei</au><au>Lee, Heng-Chi</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The Dynamics of P Granule Liquid Droplets Are Regulated by the Caenorhabditis elegans Germline RNA Helicase GLH-1 via Its ATP Hydrolysis Cycle</atitle><jtitle>Genetics (Austin)</jtitle><stitle>GENETICS</stitle><addtitle>Genetics</addtitle><date>2020-06-01</date><risdate>2020</risdate><volume>215</volume><issue>2</issue><spage>421</spage><epage>434</epage><pages>421-434</pages><issn>0016-6731</issn><issn>1943-2631</issn><eissn>1943-2631</eissn><abstract>Abstract
Germ granules, also known as P granules in Caenorhabditis elegans, are phase-separated cellular bodies that are frequently found at the perinuclear region of germ cell nuclei in various animals. However...
P granules are phase-separated liquid droplets that play important roles in the maintenance of germ cell fate in Caenorhabditis elegans. Both the localization and formation of P granules are highly dynamic, but mechanisms that regulate such processes remain poorly understood. Here, we show evidence that the VASA-like germline RNA helicase GLH-1 couples distinct steps of its ATPase hydrolysis cycle to control the formation and disassembly of P granules. In addition, we found that the phenylalanine-glycine-glycine repeats in GLH-1 promote its localization at the perinucleus. Proteomic analyses of the GLH-1 complex with a GLH-1 mutation that interferes with P granule disassembly revealed transient interactions of GLH-1 with several Argonautes and RNA-binding proteins. Finally, we found that defects in recruiting the P granule component PRG-1 to perinuclear foci in the adult germline correlate with the fertility defects observed in various GLH-1 mutants. Together, our results highlight the versatile roles of an RNA helicase in controlling the formation of liquid droplets in space and time.</abstract><cop>CARY</cop><pub>Oxford University Press</pub><pmid>32245789</pmid><doi>10.1534/genetics.120.303052</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0001-8154-906X</orcidid><orcidid>https://orcid.org/0000-0001-6428-3941</orcidid><orcidid>https://orcid.org/0000-0002-2720-1414</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Adenosine triphosphatase Adenosine Triphosphate - metabolism Animals Caenorhabditis elegans Caenorhabditis elegans - genetics Caenorhabditis elegans - growth & development Caenorhabditis elegans - metabolism Caenorhabditis elegans Proteins - genetics Caenorhabditis elegans Proteins - metabolism Cell fate CRISPR Cytoplasmic Granules - metabolism DEAD-box RNA Helicases - genetics DEAD-box RNA Helicases - metabolism Defects Deoxyribonucleic acid Dismantling DNA DNA helicase Droplets Fertility Genetics Genetics & Heredity Glycine Granular materials Hydrolysis Investigations Life Sciences & Biomedicine Liquid Crystals - chemistry Localization Mutation Nematodes Phenylalanine Plasmids Proteins Proteomics RNA helicase RNA-binding protein Science & Technology Young adults |
| title | The Dynamics of P Granule Liquid Droplets Are Regulated by the Caenorhabditis elegans Germline RNA Helicase GLH-1 via Its ATP Hydrolysis Cycle |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-01T10%3A01%3A06IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_cross&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=The%20Dynamics%20of%20P%20Granule%20Liquid%20Droplets%20Are%20Regulated%20by%20the%20Caenorhabditis%20elegans%20Germline%20RNA%20Helicase%20GLH-1%20via%20Its%20ATP%20Hydrolysis%20Cycle&rft.jtitle=Genetics%20(Austin)&rft.au=Chen,%20Wenjun&rft.date=2020-06-01&rft.volume=215&rft.issue=2&rft.spage=421&rft.epage=434&rft.pages=421-434&rft.issn=0016-6731&rft.eissn=1943-2631&rft_id=info:doi/10.1534/genetics.120.303052&rft_dat=%3Cproquest_cross%3E2412505327%3C/proquest_cross%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2412505327&rft_id=info:pmid/32245789&rft_oup_id=10.1534/genetics.120.303052&rfr_iscdi=true |