Probing small ribosomal subunit RNA helix 45 acetylation across eukaryotic evolution
NAT10 is an essential enzyme that catalyzes N4-acetylcytidine (ac4C) in eukaryotic transfer RNA and 18S ribosomal RNA. Recent studies suggested that rRNA acetylation is dependent on SNORD13, a box C/D small nucleolar RNA predicted to base-pair with 18S rRNA via two antisense elements. However, the s...
Gespeichert in:
| Veröffentlicht in: | Nucleic acids research 2022-06, Vol.50 (11), p.6284-6299 |
|---|---|
| Hauptverfasser: | , , , , , , , , , , , , |
| Format: | Artikel |
| Sprache: | eng |
| Schlagworte: | |
| Online-Zugang: | Volltext |
| Tags: |
Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
|
| container_end_page | 6299 |
|---|---|
| container_issue | 11 |
| container_start_page | 6284 |
| container_title | Nucleic acids research |
| container_volume | 50 |
| creator | Bortolin-Cavaillé, Marie-Line Quillien, Aurélie Thalalla Gamage, Supuni Thomas, Justin M Sas-Chen, Aldema Sharma, Sunny Plisson-Chastang, Célia Vandel, Laurence Blader, Patrick Lafontaine, Denis L J Schwartz, Schraga Meier, Jordan L Cavaillé, Jérôme |
| description | NAT10 is an essential enzyme that catalyzes N4-acetylcytidine (ac4C) in eukaryotic transfer RNA and 18S ribosomal RNA. Recent studies suggested that rRNA acetylation is dependent on SNORD13, a box C/D small nucleolar RNA predicted to base-pair with 18S rRNA via two antisense elements. However, the selectivity of SNORD13-dependent cytidine acetylation and its relationship to NAT10's essential function remain to be defined. Here, we demonstrate that SNORD13 is required for acetylation of a single cytidine of human and zebrafish 18S rRNA. In-depth characterization revealed that SNORD13-dependent ac4C is dispensable for human cell growth, ribosome biogenesis, translation and development. This loss of function analysis inspired a cross-evolutionary survey of the eukaryotic rRNA acetylation 'machinery' that led to the characterization of many novel metazoan SNORD13 genes. This includes an atypical SNORD13-like RNA in Drosophila melanogaster which guides ac4C to 18S rRNA helix 45 despite lacking one of the two rRNA antisense elements. Finally, we discover that Caenorhabditis elegans 18S rRNA is not acetylated despite the presence of an essential NAT10 homolog. Our findings shed light on the molecular mechanisms underlying SNORD13-mediated rRNA acetylation across eukaryotic evolution and raise new questions regarding the biological and evolutionary relevance of this highly conserved rRNA modification. |
| doi_str_mv | 10.1093/nar/gkac404 |
| format | Article |
| fullrecord | <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_9226516</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>2672319702</sourcerecordid><originalsourceid>FETCH-LOGICAL-c415t-6fd38dd9251ee1b8f7c4fb925a265601f15053978c7449e131ba41a8e39672283</originalsourceid><addsrcrecordid>eNpdkUtPAyEUhYnRaH2s3BuWGjPK5TUzG5PG-EoaNUbXhJkyLUoHhZlG_73UVqOuuHA_zj1wENoHcgKkZKetDqeTF11zwtfQAJikGS8lXUcDwojIgPBiC23H-EwIcBB8E20xIXnBWT5Aj_fBV7ad4DjTzuFgKx99KnHsq761HX64HeKpcfYdc4F1bboPpzvr21QHHyM2_YsOH76zNTZz7_pFbxdtNNpFs7dad9DT5cXj-XU2uru6OR-Osjr56DLZjFkxHpdUgDFQFU1e86ZKW02lkAQaEESwMi_qnPPSAINKc9CFYaXMKS3YDjpb6r721cyMa9N2QTv1GuwseVJeW_W309qpmvi5KmmaADIJHC0Fpv-uXQ9HanFGWC4KIvkcEnu4Ghb8W29ip2Y21sY53RrfR0WTJwZlTmhCj5fo1xcF0_xoA1GLzFTKTK0yS_TB71f8sN8hsU8Kv5OZ</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2672319702</pqid></control><display><type>article</type><title>Probing small ribosomal subunit RNA helix 45 acetylation across eukaryotic evolution</title><source>Oxford Journals Open Access Collection</source><source>MEDLINE</source><source>DOAJ Directory of Open Access Journals</source><source>PubMed Central</source><source>Free Full-Text Journals in Chemistry</source><creator>Bortolin-Cavaillé, Marie-Line ; Quillien, Aurélie ; Thalalla Gamage, Supuni ; Thomas, Justin M ; Sas-Chen, Aldema ; Sharma, Sunny ; Plisson-Chastang, Célia ; Vandel, Laurence ; Blader, Patrick ; Lafontaine, Denis L J ; Schwartz, Schraga ; Meier, Jordan L ; Cavaillé, Jérôme</creator><creatorcontrib>Bortolin-Cavaillé, Marie-Line ; Quillien, Aurélie ; Thalalla Gamage, Supuni ; Thomas, Justin M ; Sas-Chen, Aldema ; Sharma, Sunny ; Plisson-Chastang, Célia ; Vandel, Laurence ; Blader, Patrick ; Lafontaine, Denis L J ; Schwartz, Schraga ; Meier, Jordan L ; Cavaillé, Jérôme</creatorcontrib><description>NAT10 is an essential enzyme that catalyzes N4-acetylcytidine (ac4C) in eukaryotic transfer RNA and 18S ribosomal RNA. Recent studies suggested that rRNA acetylation is dependent on SNORD13, a box C/D small nucleolar RNA predicted to base-pair with 18S rRNA via two antisense elements. However, the selectivity of SNORD13-dependent cytidine acetylation and its relationship to NAT10's essential function remain to be defined. Here, we demonstrate that SNORD13 is required for acetylation of a single cytidine of human and zebrafish 18S rRNA. In-depth characterization revealed that SNORD13-dependent ac4C is dispensable for human cell growth, ribosome biogenesis, translation and development. This loss of function analysis inspired a cross-evolutionary survey of the eukaryotic rRNA acetylation 'machinery' that led to the characterization of many novel metazoan SNORD13 genes. This includes an atypical SNORD13-like RNA in Drosophila melanogaster which guides ac4C to 18S rRNA helix 45 despite lacking one of the two rRNA antisense elements. Finally, we discover that Caenorhabditis elegans 18S rRNA is not acetylated despite the presence of an essential NAT10 homolog. Our findings shed light on the molecular mechanisms underlying SNORD13-mediated rRNA acetylation across eukaryotic evolution and raise new questions regarding the biological and evolutionary relevance of this highly conserved rRNA modification.</description><identifier>ISSN: 0305-1048</identifier><identifier>EISSN: 1362-4962</identifier><identifier>DOI: 10.1093/nar/gkac404</identifier><identifier>PMID: 35648437</identifier><language>eng</language><publisher>England: Oxford University Press</publisher><subject>Acetylation ; Animals ; Biochemistry, Molecular Biology ; Eukaryota - genetics ; Eukaryota - metabolism ; Humans ; Life Sciences ; Molecular Biology ; Ribosome Subunits, Small - metabolism ; RNA, Ribosomal ; RNA, Ribosomal, 18S - metabolism ; RNA, Small Nucleolar - genetics ; RNA, Small Nucleolar - metabolism</subject><ispartof>Nucleic acids research, 2022-06, Vol.50 (11), p.6284-6299</ispartof><rights>The Author(s) 2022. Published by Oxford University Press on behalf of Nucleic Acids Research.</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><rights>The Author(s) 2022. Published by Oxford University Press on behalf of Nucleic Acids Research. 2022</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c415t-6fd38dd9251ee1b8f7c4fb925a265601f15053978c7449e131ba41a8e39672283</citedby><cites>FETCH-LOGICAL-c415t-6fd38dd9251ee1b8f7c4fb925a265601f15053978c7449e131ba41a8e39672283</cites><orcidid>0000-0003-2833-6836 ; 0000-0002-3671-9709 ; 0000-0002-4814-1895 ; 0000-0001-7295-6288 ; 0000-0002-3692-2942 ; 0000-0003-3299-6108 ; 0000-0002-8439-8428</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/PMC9226516/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC9226516/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,27901,27902,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/35648437$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-03758064$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Bortolin-Cavaillé, Marie-Line</creatorcontrib><creatorcontrib>Quillien, Aurélie</creatorcontrib><creatorcontrib>Thalalla Gamage, Supuni</creatorcontrib><creatorcontrib>Thomas, Justin M</creatorcontrib><creatorcontrib>Sas-Chen, Aldema</creatorcontrib><creatorcontrib>Sharma, Sunny</creatorcontrib><creatorcontrib>Plisson-Chastang, Célia</creatorcontrib><creatorcontrib>Vandel, Laurence</creatorcontrib><creatorcontrib>Blader, Patrick</creatorcontrib><creatorcontrib>Lafontaine, Denis L J</creatorcontrib><creatorcontrib>Schwartz, Schraga</creatorcontrib><creatorcontrib>Meier, Jordan L</creatorcontrib><creatorcontrib>Cavaillé, Jérôme</creatorcontrib><title>Probing small ribosomal subunit RNA helix 45 acetylation across eukaryotic evolution</title><title>Nucleic acids research</title><addtitle>Nucleic Acids Res</addtitle><description>NAT10 is an essential enzyme that catalyzes N4-acetylcytidine (ac4C) in eukaryotic transfer RNA and 18S ribosomal RNA. Recent studies suggested that rRNA acetylation is dependent on SNORD13, a box C/D small nucleolar RNA predicted to base-pair with 18S rRNA via two antisense elements. However, the selectivity of SNORD13-dependent cytidine acetylation and its relationship to NAT10's essential function remain to be defined. Here, we demonstrate that SNORD13 is required for acetylation of a single cytidine of human and zebrafish 18S rRNA. In-depth characterization revealed that SNORD13-dependent ac4C is dispensable for human cell growth, ribosome biogenesis, translation and development. This loss of function analysis inspired a cross-evolutionary survey of the eukaryotic rRNA acetylation 'machinery' that led to the characterization of many novel metazoan SNORD13 genes. This includes an atypical SNORD13-like RNA in Drosophila melanogaster which guides ac4C to 18S rRNA helix 45 despite lacking one of the two rRNA antisense elements. Finally, we discover that Caenorhabditis elegans 18S rRNA is not acetylated despite the presence of an essential NAT10 homolog. Our findings shed light on the molecular mechanisms underlying SNORD13-mediated rRNA acetylation across eukaryotic evolution and raise new questions regarding the biological and evolutionary relevance of this highly conserved rRNA modification.</description><subject>Acetylation</subject><subject>Animals</subject><subject>Biochemistry, Molecular Biology</subject><subject>Eukaryota - genetics</subject><subject>Eukaryota - metabolism</subject><subject>Humans</subject><subject>Life Sciences</subject><subject>Molecular Biology</subject><subject>Ribosome Subunits, Small - metabolism</subject><subject>RNA, Ribosomal</subject><subject>RNA, Ribosomal, 18S - metabolism</subject><subject>RNA, Small Nucleolar - genetics</subject><subject>RNA, Small Nucleolar - metabolism</subject><issn>0305-1048</issn><issn>1362-4962</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkUtPAyEUhYnRaH2s3BuWGjPK5TUzG5PG-EoaNUbXhJkyLUoHhZlG_73UVqOuuHA_zj1wENoHcgKkZKetDqeTF11zwtfQAJikGS8lXUcDwojIgPBiC23H-EwIcBB8E20xIXnBWT5Aj_fBV7ad4DjTzuFgKx99KnHsq761HX64HeKpcfYdc4F1bboPpzvr21QHHyM2_YsOH76zNTZz7_pFbxdtNNpFs7dad9DT5cXj-XU2uru6OR-Osjr56DLZjFkxHpdUgDFQFU1e86ZKW02lkAQaEESwMi_qnPPSAINKc9CFYaXMKS3YDjpb6r721cyMa9N2QTv1GuwseVJeW_W309qpmvi5KmmaADIJHC0Fpv-uXQ9HanFGWC4KIvkcEnu4Ghb8W29ip2Y21sY53RrfR0WTJwZlTmhCj5fo1xcF0_xoA1GLzFTKTK0yS_TB71f8sN8hsU8Kv5OZ</recordid><startdate>20220624</startdate><enddate>20220624</enddate><creator>Bortolin-Cavaillé, Marie-Line</creator><creator>Quillien, Aurélie</creator><creator>Thalalla Gamage, Supuni</creator><creator>Thomas, Justin M</creator><creator>Sas-Chen, Aldema</creator><creator>Sharma, Sunny</creator><creator>Plisson-Chastang, Célia</creator><creator>Vandel, Laurence</creator><creator>Blader, Patrick</creator><creator>Lafontaine, Denis L J</creator><creator>Schwartz, Schraga</creator><creator>Meier, Jordan L</creator><creator>Cavaillé, Jérôme</creator><general>Oxford University Press</general><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>7X8</scope><scope>1XC</scope><scope>VOOES</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-2833-6836</orcidid><orcidid>https://orcid.org/0000-0002-3671-9709</orcidid><orcidid>https://orcid.org/0000-0002-4814-1895</orcidid><orcidid>https://orcid.org/0000-0001-7295-6288</orcidid><orcidid>https://orcid.org/0000-0002-3692-2942</orcidid><orcidid>https://orcid.org/0000-0003-3299-6108</orcidid><orcidid>https://orcid.org/0000-0002-8439-8428</orcidid></search><sort><creationdate>20220624</creationdate><title>Probing small ribosomal subunit RNA helix 45 acetylation across eukaryotic evolution</title><author>Bortolin-Cavaillé, Marie-Line ; Quillien, Aurélie ; Thalalla Gamage, Supuni ; Thomas, Justin M ; Sas-Chen, Aldema ; Sharma, Sunny ; Plisson-Chastang, Célia ; Vandel, Laurence ; Blader, Patrick ; Lafontaine, Denis L J ; Schwartz, Schraga ; Meier, Jordan L ; Cavaillé, Jérôme</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c415t-6fd38dd9251ee1b8f7c4fb925a265601f15053978c7449e131ba41a8e39672283</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Acetylation</topic><topic>Animals</topic><topic>Biochemistry, Molecular Biology</topic><topic>Eukaryota - genetics</topic><topic>Eukaryota - metabolism</topic><topic>Humans</topic><topic>Life Sciences</topic><topic>Molecular Biology</topic><topic>Ribosome Subunits, Small - metabolism</topic><topic>RNA, Ribosomal</topic><topic>RNA, Ribosomal, 18S - metabolism</topic><topic>RNA, Small Nucleolar - genetics</topic><topic>RNA, Small Nucleolar - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Bortolin-Cavaillé, Marie-Line</creatorcontrib><creatorcontrib>Quillien, Aurélie</creatorcontrib><creatorcontrib>Thalalla Gamage, Supuni</creatorcontrib><creatorcontrib>Thomas, Justin M</creatorcontrib><creatorcontrib>Sas-Chen, Aldema</creatorcontrib><creatorcontrib>Sharma, Sunny</creatorcontrib><creatorcontrib>Plisson-Chastang, Célia</creatorcontrib><creatorcontrib>Vandel, Laurence</creatorcontrib><creatorcontrib>Blader, Patrick</creatorcontrib><creatorcontrib>Lafontaine, Denis L J</creatorcontrib><creatorcontrib>Schwartz, Schraga</creatorcontrib><creatorcontrib>Meier, Jordan L</creatorcontrib><creatorcontrib>Cavaillé, Jérôme</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Nucleic acids research</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Bortolin-Cavaillé, Marie-Line</au><au>Quillien, Aurélie</au><au>Thalalla Gamage, Supuni</au><au>Thomas, Justin M</au><au>Sas-Chen, Aldema</au><au>Sharma, Sunny</au><au>Plisson-Chastang, Célia</au><au>Vandel, Laurence</au><au>Blader, Patrick</au><au>Lafontaine, Denis L J</au><au>Schwartz, Schraga</au><au>Meier, Jordan L</au><au>Cavaillé, Jérôme</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Probing small ribosomal subunit RNA helix 45 acetylation across eukaryotic evolution</atitle><jtitle>Nucleic acids research</jtitle><addtitle>Nucleic Acids Res</addtitle><date>2022-06-24</date><risdate>2022</risdate><volume>50</volume><issue>11</issue><spage>6284</spage><epage>6299</epage><pages>6284-6299</pages><issn>0305-1048</issn><eissn>1362-4962</eissn><abstract>NAT10 is an essential enzyme that catalyzes N4-acetylcytidine (ac4C) in eukaryotic transfer RNA and 18S ribosomal RNA. Recent studies suggested that rRNA acetylation is dependent on SNORD13, a box C/D small nucleolar RNA predicted to base-pair with 18S rRNA via two antisense elements. However, the selectivity of SNORD13-dependent cytidine acetylation and its relationship to NAT10's essential function remain to be defined. Here, we demonstrate that SNORD13 is required for acetylation of a single cytidine of human and zebrafish 18S rRNA. In-depth characterization revealed that SNORD13-dependent ac4C is dispensable for human cell growth, ribosome biogenesis, translation and development. This loss of function analysis inspired a cross-evolutionary survey of the eukaryotic rRNA acetylation 'machinery' that led to the characterization of many novel metazoan SNORD13 genes. This includes an atypical SNORD13-like RNA in Drosophila melanogaster which guides ac4C to 18S rRNA helix 45 despite lacking one of the two rRNA antisense elements. Finally, we discover that Caenorhabditis elegans 18S rRNA is not acetylated despite the presence of an essential NAT10 homolog. Our findings shed light on the molecular mechanisms underlying SNORD13-mediated rRNA acetylation across eukaryotic evolution and raise new questions regarding the biological and evolutionary relevance of this highly conserved rRNA modification.</abstract><cop>England</cop><pub>Oxford University Press</pub><pmid>35648437</pmid><doi>10.1093/nar/gkac404</doi><tpages>16</tpages><orcidid>https://orcid.org/0000-0003-2833-6836</orcidid><orcidid>https://orcid.org/0000-0002-3671-9709</orcidid><orcidid>https://orcid.org/0000-0002-4814-1895</orcidid><orcidid>https://orcid.org/0000-0001-7295-6288</orcidid><orcidid>https://orcid.org/0000-0002-3692-2942</orcidid><orcidid>https://orcid.org/0000-0003-3299-6108</orcidid><orcidid>https://orcid.org/0000-0002-8439-8428</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 0305-1048 |
| ispartof | Nucleic acids research, 2022-06, Vol.50 (11), p.6284-6299 |
| issn | 0305-1048 1362-4962 |
| language | eng |
| recordid | cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_9226516 |
| source | Oxford Journals Open Access Collection; MEDLINE; DOAJ Directory of Open Access Journals; PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Acetylation Animals Biochemistry, Molecular Biology Eukaryota - genetics Eukaryota - metabolism Humans Life Sciences Molecular Biology Ribosome Subunits, Small - metabolism RNA, Ribosomal RNA, Ribosomal, 18S - metabolism RNA, Small Nucleolar - genetics RNA, Small Nucleolar - metabolism |
| title | Probing small ribosomal subunit RNA helix 45 acetylation across eukaryotic evolution |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-29T04%3A40%3A17IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Probing%20small%20ribosomal%20subunit%20RNA%20helix%2045%20acetylation%20across%20eukaryotic%20evolution&rft.jtitle=Nucleic%20acids%20research&rft.au=Bortolin-Cavaill%C3%A9,%20Marie-Line&rft.date=2022-06-24&rft.volume=50&rft.issue=11&rft.spage=6284&rft.epage=6299&rft.pages=6284-6299&rft.issn=0305-1048&rft.eissn=1362-4962&rft_id=info:doi/10.1093/nar/gkac404&rft_dat=%3Cproquest_pubme%3E2672319702%3C/proquest_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2672319702&rft_id=info:pmid/35648437&rfr_iscdi=true |