Filamentation of asparagine synthetase in Saccharomyces cerevisiae
Asparagine synthetase (ASNS) and CTP synthase (CTPS) are two metabolic enzymes crucial for glutamine homeostasis. A genome-wide screening in Saccharomyces cerevisiae reveal that both ASNS and CTPS form filamentous structures termed cytoophidia. Although CTPS cytoophidia were well documented in recen...
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description | Asparagine synthetase (ASNS) and CTP synthase (CTPS) are two metabolic enzymes crucial for glutamine homeostasis. A genome-wide screening in Saccharomyces cerevisiae reveal that both ASNS and CTPS form filamentous structures termed cytoophidia. Although CTPS cytoophidia were well documented in recent years, the filamentation of ASNS is less studied. Using the budding yeast as a model system, here we confirm that two ASNS proteins, Asn1 and Asn2, are capable of forming cytoophidia in diauxic and stationary phases. We find that glucose deprivation induces ASNS filament formation. Although ASNS and CTPS form distinct cytoophidia with different lengths, both structures locate adjacently to each other in most cells. Moreover, we demonstrate that the Asn1 cytoophidia colocalize with the Asn2 cytoophidia, while Asn2 filament assembly is largely dependent on Asn1. In addition, we are able to alter Asn1 filamentation by mutagenizing key sites on the dimer interface. Finally, we show that ASN1D330V promotes filamentation. The ASN1D330V mutation impedes cell growth in an ASN2 knockout background, while growing normally in an ASN2 wild-type background. Together, this study reveals a connection between ASNS and CTPS cytoophidia and the differential filament-forming capability between two ASNS paralogs. |
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A genome-wide screening in Saccharomyces cerevisiae reveal that both ASNS and CTPS form filamentous structures termed cytoophidia. Although CTPS cytoophidia were well documented in recent years, the filamentation of ASNS is less studied. Using the budding yeast as a model system, here we confirm that two ASNS proteins, Asn1 and Asn2, are capable of forming cytoophidia in diauxic and stationary phases. We find that glucose deprivation induces ASNS filament formation. Although ASNS and CTPS form distinct cytoophidia with different lengths, both structures locate adjacently to each other in most cells. Moreover, we demonstrate that the Asn1 cytoophidia colocalize with the Asn2 cytoophidia, while Asn2 filament assembly is largely dependent on Asn1. In addition, we are able to alter Asn1 filamentation by mutagenizing key sites on the dimer interface. Finally, we show that ASN1D330V promotes filamentation. The ASN1D330V mutation impedes cell growth in an ASN2 knockout background, while growing normally in an ASN2 wild-type background. Together, this study reveals a connection between ASNS and CTPS cytoophidia and the differential filament-forming capability between two ASNS paralogs.</description><identifier>ISSN: 1553-7404</identifier><identifier>ISSN: 1553-7390</identifier><identifier>EISSN: 1553-7404</identifier><identifier>DOI: 10.1371/journal.pgen.1007737</identifier><identifier>PMID: 30365499</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Anatomy & physiology ; Asparagine ; Aspartate-ammonia ligase ; Biochemistry ; Biology and Life Sciences ; Carbon ; Cell cycle ; CTP synthase ; Cytoplasm ; Enzymes ; Filamentation ; Genes ; Genomes ; Genomics ; Glutamine ; Homeostasis ; Life sciences ; Melanoma ; Metabolism ; Mutation ; Physical Sciences ; Physiology ; Proteins ; Research and Analysis Methods ; Saccharomyces cerevisiae ; Yeast</subject><ispartof>PLoS genetics, 2018-10, Vol.14 (10), p.e1007737</ispartof><rights>2018 Zhang et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2018 Zhang et al 2018 Zhang et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c592t-f117037fd0eab531692a272c631fc67596d5b8c538575f8ef73a1d0ee102ae8d3</citedby><cites>FETCH-LOGICAL-c592t-f117037fd0eab531692a272c631fc67596d5b8c538575f8ef73a1d0ee102ae8d3</cites><orcidid>0000-0002-4834-8554</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6221361/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6221361/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79343,79344</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30365499$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Zhang, Shanshan</creatorcontrib><creatorcontrib>Ding, Kang</creatorcontrib><creatorcontrib>Shen, Qing-Ji</creatorcontrib><creatorcontrib>Zhao, Suwen</creatorcontrib><creatorcontrib>Liu, Ji-Long</creatorcontrib><title>Filamentation of asparagine synthetase in Saccharomyces cerevisiae</title><title>PLoS genetics</title><addtitle>PLoS Genet</addtitle><description>Asparagine synthetase (ASNS) and CTP synthase (CTPS) are two metabolic enzymes crucial for glutamine homeostasis. A genome-wide screening in Saccharomyces cerevisiae reveal that both ASNS and CTPS form filamentous structures termed cytoophidia. Although CTPS cytoophidia were well documented in recent years, the filamentation of ASNS is less studied. Using the budding yeast as a model system, here we confirm that two ASNS proteins, Asn1 and Asn2, are capable of forming cytoophidia in diauxic and stationary phases. We find that glucose deprivation induces ASNS filament formation. Although ASNS and CTPS form distinct cytoophidia with different lengths, both structures locate adjacently to each other in most cells. Moreover, we demonstrate that the Asn1 cytoophidia colocalize with the Asn2 cytoophidia, while Asn2 filament assembly is largely dependent on Asn1. In addition, we are able to alter Asn1 filamentation by mutagenizing key sites on the dimer interface. Finally, we show that ASN1D330V promotes filamentation. The ASN1D330V mutation impedes cell growth in an ASN2 knockout background, while growing normally in an ASN2 wild-type background. Together, this study reveals a connection between ASNS and CTPS cytoophidia and the differential filament-forming capability between two ASNS paralogs.</description><subject>Anatomy & physiology</subject><subject>Asparagine</subject><subject>Aspartate-ammonia ligase</subject><subject>Biochemistry</subject><subject>Biology and Life Sciences</subject><subject>Carbon</subject><subject>Cell cycle</subject><subject>CTP synthase</subject><subject>Cytoplasm</subject><subject>Enzymes</subject><subject>Filamentation</subject><subject>Genes</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Glutamine</subject><subject>Homeostasis</subject><subject>Life sciences</subject><subject>Melanoma</subject><subject>Metabolism</subject><subject>Mutation</subject><subject>Physical Sciences</subject><subject>Physiology</subject><subject>Proteins</subject><subject>Research and Analysis Methods</subject><subject>Saccharomyces cerevisiae</subject><subject>Yeast</subject><issn>1553-7404</issn><issn>1553-7390</issn><issn>1553-7404</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><sourceid>BENPR</sourceid><sourceid>DOA</sourceid><recordid>eNp1kUFvEzEQhS0Eom3gHyBYqecEj71eey9IULVQqRKHlrM1sceJo8062JtK-fdsm23VHjjZ8rz3zYwfY5-AL0Bq-LpJ-9xjt9itqF8A51pL_YadglJyrmtev31xP2FnpWw4l8q0-j07kVw2qm7bU_bjKna4pX7AIaa-SqHCssOMq9hTVQ79sKYBC1Wxr27RuTXmtD04KpWjTPexRKQP7F3ArtDH6ZyxP1eXdxe_5je_f15ffL-ZO9WKYR4ANJc6eE64VBKaVqDQwjUSgmu0ahuvlsYpaZRWwVDQEmEUE3CBZLycsS9H7q5LxU7rFyuEAg6mGeEzdn1U-IQbu8txi_lgE0b7-JDyymIeouvIIidNwnsja6oJnKlro72gEJbCq9aNrG9Tt_1yS96NX5SxewV9Xenj2q7SvW2EANnACDifADn93VMZ_jNyfVS5nErJFJ47ALcPOT-57EPOdsp5tH1-Od2z6SlY-Q_6qKd7</recordid><startdate>20181001</startdate><enddate>20181001</enddate><creator>Zhang, Shanshan</creator><creator>Ding, Kang</creator><creator>Shen, Qing-Ji</creator><creator>Zhao, Suwen</creator><creator>Liu, Ji-Long</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7QP</scope><scope>7QR</scope><scope>7SS</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</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>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>P64</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>RC3</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0002-4834-8554</orcidid></search><sort><creationdate>20181001</creationdate><title>Filamentation of asparagine synthetase in Saccharomyces cerevisiae</title><author>Zhang, Shanshan ; Ding, Kang ; Shen, Qing-Ji ; Zhao, Suwen ; Liu, Ji-Long</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c592t-f117037fd0eab531692a272c631fc67596d5b8c538575f8ef73a1d0ee102ae8d3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>Anatomy & physiology</topic><topic>Asparagine</topic><topic>Aspartate-ammonia ligase</topic><topic>Biochemistry</topic><topic>Biology and Life Sciences</topic><topic>Carbon</topic><topic>Cell cycle</topic><topic>CTP synthase</topic><topic>Cytoplasm</topic><topic>Enzymes</topic><topic>Filamentation</topic><topic>Genes</topic><topic>Genomes</topic><topic>Genomics</topic><topic>Glutamine</topic><topic>Homeostasis</topic><topic>Life sciences</topic><topic>Melanoma</topic><topic>Metabolism</topic><topic>Mutation</topic><topic>Physical Sciences</topic><topic>Physiology</topic><topic>Proteins</topic><topic>Research and Analysis Methods</topic><topic>Saccharomyces cerevisiae</topic><topic>Yeast</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Zhang, Shanshan</creatorcontrib><creatorcontrib>Ding, Kang</creatorcontrib><creatorcontrib>Shen, Qing-Ji</creatorcontrib><creatorcontrib>Zhao, Suwen</creatorcontrib><creatorcontrib>Liu, Ji-Long</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>Genetics Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS genetics</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Zhang, Shanshan</au><au>Ding, Kang</au><au>Shen, Qing-Ji</au><au>Zhao, Suwen</au><au>Liu, Ji-Long</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Filamentation of asparagine synthetase in Saccharomyces cerevisiae</atitle><jtitle>PLoS genetics</jtitle><addtitle>PLoS Genet</addtitle><date>2018-10-01</date><risdate>2018</risdate><volume>14</volume><issue>10</issue><spage>e1007737</spage><pages>e1007737-</pages><issn>1553-7404</issn><issn>1553-7390</issn><eissn>1553-7404</eissn><abstract>Asparagine synthetase (ASNS) and CTP synthase (CTPS) are two metabolic enzymes crucial for glutamine homeostasis. A genome-wide screening in Saccharomyces cerevisiae reveal that both ASNS and CTPS form filamentous structures termed cytoophidia. Although CTPS cytoophidia were well documented in recent years, the filamentation of ASNS is less studied. Using the budding yeast as a model system, here we confirm that two ASNS proteins, Asn1 and Asn2, are capable of forming cytoophidia in diauxic and stationary phases. We find that glucose deprivation induces ASNS filament formation. Although ASNS and CTPS form distinct cytoophidia with different lengths, both structures locate adjacently to each other in most cells. Moreover, we demonstrate that the Asn1 cytoophidia colocalize with the Asn2 cytoophidia, while Asn2 filament assembly is largely dependent on Asn1. In addition, we are able to alter Asn1 filamentation by mutagenizing key sites on the dimer interface. Finally, we show that ASN1D330V promotes filamentation. The ASN1D330V mutation impedes cell growth in an ASN2 knockout background, while growing normally in an ASN2 wild-type background. Together, this study reveals a connection between ASNS and CTPS cytoophidia and the differential filament-forming capability between two ASNS paralogs.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>30365499</pmid><doi>10.1371/journal.pgen.1007737</doi><orcidid>https://orcid.org/0000-0002-4834-8554</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Anatomy & physiology Asparagine Aspartate-ammonia ligase Biochemistry Biology and Life Sciences Carbon Cell cycle CTP synthase Cytoplasm Enzymes Filamentation Genes Genomes Genomics Glutamine Homeostasis Life sciences Melanoma Metabolism Mutation Physical Sciences Physiology Proteins Research and Analysis Methods Saccharomyces cerevisiae Yeast |
title | Filamentation of asparagine synthetase in Saccharomyces cerevisiae |
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