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Telomere-specific regulation of TERRA and its impact on telomere stability
TERRA is a class of telomeric repeat-containing RNAs that are expressed from telomeres in multiple organisms. TERRA transcripts play key roles in telomere maintenance and their physiological levels are essential to maintain the integrity of telomeric DNA. Indeed, deregulated TERRA expression or its...
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| Published in: | Seminars in cell & developmental biology 2024-04, Vol.157, p.3-23 |
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| container_title | Seminars in cell & developmental biology |
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| creator | Rivosecchi, Julieta Jurikova, Katarina Cusanelli, Emilio |
| description | TERRA is a class of telomeric repeat-containing RNAs that are expressed from telomeres in multiple organisms. TERRA transcripts play key roles in telomere maintenance and their physiological levels are essential to maintain the integrity of telomeric DNA. Indeed, deregulated TERRA expression or its altered localization can impact telomere stability by multiple mechanisms including fueling transcription-replication conflicts, promoting resection of chromosome ends, altering the telomeric chromatin, and supporting homologous recombination. Therefore, a fine-tuned control of TERRA is important to maintain the integrity of the genome. Several studies have reported that different cell lines express substantially different levels of TERRA. Most importantly, TERRA levels markedly vary among telomeres of a given cell type, indicating the existence of telomere-specific regulatory mechanisms which may help coordinate TERRA functions. TERRA molecules contain distinct subtelomeric sequences, depending on their telomere of origin, which may instruct specific post-transcriptional modifications or mediate distinct functions. In addition, all TERRA transcripts share a repetitive G-rich sequence at their 3′ end which can form DNA:RNA hybrids and fold into G-quadruplex structures. Both structures are involved in TERRA functions and can critically affect telomere stability. In this review, we examine the mechanisms controlling TERRA levels and the impact of their telomere-specific regulation on telomere stability. We compare evidence obtained in different model organisms, discussing recent advances as well as controversies in the field. Furthermore, we discuss the importance of DNA:RNA hybrids and G-quadruplex structures in the context of TERRA biology and telomere maintenance.
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•Transcription of telomeric repeats contributes to telomere function and stability.•TERRA expression is regulated in a telomere-specific manner in various organisms.•Transcriptional control and RNA decay mechanisms coordinate TERRA expression regulation.•Altered TERRA levels can precipitate telomere dysfunction and genome instability.•Telomeric R-loops and RNA G quadruplexes contribute to TERRA functions. |
| doi_str_mv | 10.1016/j.semcdb.2023.11.001 |
| format | article |
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[Display omitted]
•Transcription of telomeric repeats contributes to telomere function and stability.•TERRA expression is regulated in a telomere-specific manner in various organisms.•Transcriptional control and RNA decay mechanisms coordinate TERRA expression regulation.•Altered TERRA levels can precipitate telomere dysfunction and genome instability.•Telomeric R-loops and RNA G quadruplexes contribute to TERRA functions.</description><identifier>ISSN: 1084-9521</identifier><identifier>EISSN: 1096-3634</identifier><identifier>DOI: 10.1016/j.semcdb.2023.11.001</identifier><identifier>PMID: 38088000</identifier><language>eng</language><publisher>England: Elsevier Ltd</publisher><subject>G-quadruplex ; R-loop ; RNA decay ; telomere ; TERRA ; transcription</subject><ispartof>Seminars in cell & developmental biology, 2024-04, Vol.157, p.3-23</ispartof><rights>2023 The Authors</rights><rights>Copyright © 2023 The Authors. Published by Elsevier Ltd.. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c408t-145f23765d22f10fc33bfadc129da56b373349e80bd2a45a509174a0833ec0db3</citedby><cites>FETCH-LOGICAL-c408t-145f23765d22f10fc33bfadc129da56b373349e80bd2a45a509174a0833ec0db3</cites><orcidid>0000-0002-7683-8542</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>315,786,790,27957,27958</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38088000$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Rivosecchi, Julieta</creatorcontrib><creatorcontrib>Jurikova, Katarina</creatorcontrib><creatorcontrib>Cusanelli, Emilio</creatorcontrib><title>Telomere-specific regulation of TERRA and its impact on telomere stability</title><title>Seminars in cell & developmental biology</title><addtitle>Semin Cell Dev Biol</addtitle><description>TERRA is a class of telomeric repeat-containing RNAs that are expressed from telomeres in multiple organisms. TERRA transcripts play key roles in telomere maintenance and their physiological levels are essential to maintain the integrity of telomeric DNA. Indeed, deregulated TERRA expression or its altered localization can impact telomere stability by multiple mechanisms including fueling transcription-replication conflicts, promoting resection of chromosome ends, altering the telomeric chromatin, and supporting homologous recombination. Therefore, a fine-tuned control of TERRA is important to maintain the integrity of the genome. Several studies have reported that different cell lines express substantially different levels of TERRA. Most importantly, TERRA levels markedly vary among telomeres of a given cell type, indicating the existence of telomere-specific regulatory mechanisms which may help coordinate TERRA functions. TERRA molecules contain distinct subtelomeric sequences, depending on their telomere of origin, which may instruct specific post-transcriptional modifications or mediate distinct functions. In addition, all TERRA transcripts share a repetitive G-rich sequence at their 3′ end which can form DNA:RNA hybrids and fold into G-quadruplex structures. Both structures are involved in TERRA functions and can critically affect telomere stability. In this review, we examine the mechanisms controlling TERRA levels and the impact of their telomere-specific regulation on telomere stability. We compare evidence obtained in different model organisms, discussing recent advances as well as controversies in the field. Furthermore, we discuss the importance of DNA:RNA hybrids and G-quadruplex structures in the context of TERRA biology and telomere maintenance.
[Display omitted]
•Transcription of telomeric repeats contributes to telomere function and stability.•TERRA expression is regulated in a telomere-specific manner in various organisms.•Transcriptional control and RNA decay mechanisms coordinate TERRA expression regulation.•Altered TERRA levels can precipitate telomere dysfunction and genome instability.•Telomeric R-loops and RNA G quadruplexes contribute to TERRA functions.</description><subject>G-quadruplex</subject><subject>R-loop</subject><subject>RNA decay</subject><subject>telomere</subject><subject>TERRA</subject><subject>transcription</subject><issn>1084-9521</issn><issn>1096-3634</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><recordid>eNp9kFtLw0AQhRdRbK3-A5E8-pI4e0mavAil1BsFodTnZbM7kS25ubsR-u9NafXRp5lhzpnDfITcUkgo0Oxhl3hstCkTBownlCYA9IxMKRRZzDMuzg99LuIiZXRCrrzfAYAoWHZJJjyHPB_HKXnbYt016DD2PWpbWR05_BxqFWzXRl0VbVebzSJSrYls8JFteqVDNK7CyRf5oEpb27C_JheVqj3enOqMfDyttsuXeP3-_LpcrGMtIA8xFWnF-DxLDWMVhUpzXlbKaMoKo9Ks5HPORYE5lIYpkaoUCjoXCnLOUYMp-YzcH-_2rvsa0AfZWK-xrlWL3eAlK4AVggmRj1JxlGrXee-wkr2zjXJ7SUEeKMqdPFKUB4qSUjlSHG13p4ShbND8mX6xjYLHowDHP78tOum1xVajsQ51kKaz_yf8AIwkg_c</recordid><startdate>202404</startdate><enddate>202404</enddate><creator>Rivosecchi, Julieta</creator><creator>Jurikova, Katarina</creator><creator>Cusanelli, Emilio</creator><general>Elsevier Ltd</general><scope>6I.</scope><scope>AAFTH</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-7683-8542</orcidid></search><sort><creationdate>202404</creationdate><title>Telomere-specific regulation of TERRA and its impact on telomere stability</title><author>Rivosecchi, Julieta ; Jurikova, Katarina ; Cusanelli, Emilio</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c408t-145f23765d22f10fc33bfadc129da56b373349e80bd2a45a509174a0833ec0db3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>G-quadruplex</topic><topic>R-loop</topic><topic>RNA decay</topic><topic>telomere</topic><topic>TERRA</topic><topic>transcription</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Rivosecchi, Julieta</creatorcontrib><creatorcontrib>Jurikova, Katarina</creatorcontrib><creatorcontrib>Cusanelli, Emilio</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Seminars in cell & developmental biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Rivosecchi, Julieta</au><au>Jurikova, Katarina</au><au>Cusanelli, Emilio</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Telomere-specific regulation of TERRA and its impact on telomere stability</atitle><jtitle>Seminars in cell & developmental biology</jtitle><addtitle>Semin Cell Dev Biol</addtitle><date>2024-04</date><risdate>2024</risdate><volume>157</volume><spage>3</spage><epage>23</epage><pages>3-23</pages><issn>1084-9521</issn><eissn>1096-3634</eissn><notes>ObjectType-Article-2</notes><notes>SourceType-Scholarly Journals-1</notes><notes>ObjectType-Feature-3</notes><notes>content type line 23</notes><notes>ObjectType-Review-1</notes><abstract>TERRA is a class of telomeric repeat-containing RNAs that are expressed from telomeres in multiple organisms. TERRA transcripts play key roles in telomere maintenance and their physiological levels are essential to maintain the integrity of telomeric DNA. Indeed, deregulated TERRA expression or its altered localization can impact telomere stability by multiple mechanisms including fueling transcription-replication conflicts, promoting resection of chromosome ends, altering the telomeric chromatin, and supporting homologous recombination. Therefore, a fine-tuned control of TERRA is important to maintain the integrity of the genome. Several studies have reported that different cell lines express substantially different levels of TERRA. Most importantly, TERRA levels markedly vary among telomeres of a given cell type, indicating the existence of telomere-specific regulatory mechanisms which may help coordinate TERRA functions. TERRA molecules contain distinct subtelomeric sequences, depending on their telomere of origin, which may instruct specific post-transcriptional modifications or mediate distinct functions. In addition, all TERRA transcripts share a repetitive G-rich sequence at their 3′ end which can form DNA:RNA hybrids and fold into G-quadruplex structures. Both structures are involved in TERRA functions and can critically affect telomere stability. In this review, we examine the mechanisms controlling TERRA levels and the impact of their telomere-specific regulation on telomere stability. We compare evidence obtained in different model organisms, discussing recent advances as well as controversies in the field. Furthermore, we discuss the importance of DNA:RNA hybrids and G-quadruplex structures in the context of TERRA biology and telomere maintenance.
[Display omitted]
•Transcription of telomeric repeats contributes to telomere function and stability.•TERRA expression is regulated in a telomere-specific manner in various organisms.•Transcriptional control and RNA decay mechanisms coordinate TERRA expression regulation.•Altered TERRA levels can precipitate telomere dysfunction and genome instability.•Telomeric R-loops and RNA G quadruplexes contribute to TERRA functions.</abstract><cop>England</cop><pub>Elsevier Ltd</pub><pmid>38088000</pmid><doi>10.1016/j.semcdb.2023.11.001</doi><tpages>21</tpages><orcidid>https://orcid.org/0000-0002-7683-8542</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | G-quadruplex R-loop RNA decay telomere TERRA transcription |
| title | Telomere-specific regulation of TERRA and its impact on telomere stability |
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