A Parallel G Quadruplex-Binding Protein Regulates the Boundaries of DNA Elimination Events of Tetrahymena thermophila
Guanine (G)-rich DNA readily forms four-stranded quadruplexes in vitro, but evidence for their participation in genome regulation is limited. We have identified a quadruplex-binding protein, Lia3, that controls the boundaries of germline-limited, internal eliminated sequences (IESs) of Tetrahymena t...
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| description | Guanine (G)-rich DNA readily forms four-stranded quadruplexes in vitro, but evidence for their participation in genome regulation is limited. We have identified a quadruplex-binding protein, Lia3, that controls the boundaries of germline-limited, internal eliminated sequences (IESs) of Tetrahymena thermophila. Differentiation of this ciliate's somatic genome requires excision of thousands of IESs, targeted for removal by small-RNA-directed heterochromatin formation. In cells lacking LIA3 (ΔLIA3), the excision of IESs bounded by specific G-rich polypurine tracts was impaired and imprecise, whereas the removal of IESs without such controlling sequences was unaffected. We found that oligonucleotides containing these polypurine tracts formed parallel G-quadruplex structures that are specifically bound by Lia3. The discovery that Lia3 binds G-quadruplex DNA and controls the accuracy of DNA elimination at loci with specific G-tracts uncovers an unrecognized potential of quadruplex structures to regulate chromosome organization. |
| doi_str_mv | 10.1371/journal.pgen.1005842 |
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We have identified a quadruplex-binding protein, Lia3, that controls the boundaries of germline-limited, internal eliminated sequences (IESs) of Tetrahymena thermophila. Differentiation of this ciliate's somatic genome requires excision of thousands of IESs, targeted for removal by small-RNA-directed heterochromatin formation. In cells lacking LIA3 (ΔLIA3), the excision of IESs bounded by specific G-rich polypurine tracts was impaired and imprecise, whereas the removal of IESs without such controlling sequences was unaffected. We found that oligonucleotides containing these polypurine tracts formed parallel G-quadruplex structures that are specifically bound by Lia3. The discovery that Lia3 binds G-quadruplex DNA and controls the accuracy of DNA elimination at loci with specific G-tracts uncovers an unrecognized potential of quadruplex structures to regulate chromosome organization.</description><identifier>ISSN: 1553-7404</identifier><identifier>ISSN: 1553-7390</identifier><identifier>EISSN: 1553-7404</identifier><identifier>DOI: 10.1371/journal.pgen.1005842</identifier><identifier>PMID: 26950070</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Binding proteins ; Biology and life sciences ; Boundaries ; Chromosomes - genetics ; Deoxyribonucleic acid ; DNA ; DNA methylation ; DNA sequencing ; DNA-Binding Proteins - genetics ; DNA-Binding Proteins - metabolism ; G-Quadruplexes ; Gene expression ; Genetic aspects ; Genome ; Genomes ; Laboratories ; Methods ; Oligonucleotides - genetics ; Physical Sciences ; Physiological aspects ; Protein Binding ; Proteins ; Protozoan Proteins - genetics ; Research and Analysis Methods ; Sequence Analysis, DNA ; Telomere - genetics ; Tetrahymena thermophila ; Tetrahymena thermophila - genetics ; Thermophiles</subject><ispartof>PLoS genetics, 2016-03, Vol.12 (3), p.e1005842</ispartof><rights>COPYRIGHT 2016 Public Library of Science</rights><rights>2016 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: . PLoS Genet 12(3): e1005842. doi:10.1371/journal.pgen.1005842</rights><rights>2016 Carle et al 2016 Carle et al</rights><rights>2016 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: . 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We have identified a quadruplex-binding protein, Lia3, that controls the boundaries of germline-limited, internal eliminated sequences (IESs) of Tetrahymena thermophila. Differentiation of this ciliate's somatic genome requires excision of thousands of IESs, targeted for removal by small-RNA-directed heterochromatin formation. In cells lacking LIA3 (ΔLIA3), the excision of IESs bounded by specific G-rich polypurine tracts was impaired and imprecise, whereas the removal of IESs without such controlling sequences was unaffected. We found that oligonucleotides containing these polypurine tracts formed parallel G-quadruplex structures that are specifically bound by Lia3. The discovery that Lia3 binds G-quadruplex DNA and controls the accuracy of DNA elimination at loci with specific G-tracts uncovers an unrecognized potential of quadruplex structures to regulate chromosome organization.</description><subject>Binding proteins</subject><subject>Biology and life sciences</subject><subject>Boundaries</subject><subject>Chromosomes - genetics</subject><subject>Deoxyribonucleic acid</subject><subject>DNA</subject><subject>DNA methylation</subject><subject>DNA sequencing</subject><subject>DNA-Binding Proteins - genetics</subject><subject>DNA-Binding Proteins - metabolism</subject><subject>G-Quadruplexes</subject><subject>Gene expression</subject><subject>Genetic aspects</subject><subject>Genome</subject><subject>Genomes</subject><subject>Laboratories</subject><subject>Methods</subject><subject>Oligonucleotides - genetics</subject><subject>Physical Sciences</subject><subject>Physiological aspects</subject><subject>Protein Binding</subject><subject>Proteins</subject><subject>Protozoan Proteins - genetics</subject><subject>Research and Analysis Methods</subject><subject>Sequence Analysis, DNA</subject><subject>Telomere - genetics</subject><subject>Tetrahymena thermophila</subject><subject>Tetrahymena thermophila - genetics</subject><subject>Thermophiles</subject><issn>1553-7404</issn><issn>1553-7390</issn><issn>1553-7404</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNqVk1Fv0zAUhSMEYqPwDxBEQkLw0GLHcZ28TOpGGZWmbYzBq-XaN6krxy52Mm3_HqftphbtYSgPie3vnNjn-ibJW4xGmDD8Zek6b4UZrWqwI4wQLfLsWXKIKSVDlqP8-c73QfIqhCVChBYle5kcZOOSIsTQYdJN0kvhhTFg0tP0RyeU71YGbofH2ipt6_TSuxa0Ta-g7oxoIaTtAtJj11klvI5DV6Vfzyfp1OhGW9FqZ9PpDdh2vXINrReLuwas6HW-cauFNuJ18qISJsCb7XuQ_Po2vT75Pjy7OJ2dTM6GktGyHRYShMIZK-eQEZXLUsC4QBRKXGVUYiIzgjJQUCFVqpJQFU83r-ayYqCwIAUZJO83vivjAt8mFjhmBSZlFvOIxGxDKCeWfOV1I_wdd0Lz9YTzNRe-1dIAp-OqEgzkHGSZK5gXhCKgLGdIFlWR59HraPu3bt6AkjGEmOye6f6K1QteuxuesyIWozf4tDXw7k8HoeWNDhKMERZct943K8fjIkNPQBlmWU5J7_rhH_TxILZULeJZta1c3KLsTfkkZyUljMbbNEhGj1DxUdBo6SxUOs7vCT7vCSLTwm1biy4EPvt59R_s-dPZi9_77McddgHCtIvgTNff1bAP5htQeheCh-qhdhjxvunuk-N90_Ft00XZu926P4juu4z8BfN7Jxc</recordid><startdate>20160307</startdate><enddate>20160307</enddate><creator>Carle, Christine M</creator><creator>Zaher, Hani S</creator><creator>Chalker, Douglas L</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</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>IOV</scope><scope>ISN</scope><scope>ISR</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>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20160307</creationdate><title>A Parallel G Quadruplex-Binding Protein Regulates the Boundaries of DNA Elimination Events of Tetrahymena thermophila</title><author>Carle, Christine M ; Zaher, Hani S ; Chalker, Douglas L</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c759t-8cead1279be23d4c9ae6805e91f25c13c2302edef0d9d935d897bfbcf7ed1a383</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Binding proteins</topic><topic>Biology and life sciences</topic><topic>Boundaries</topic><topic>Chromosomes - genetics</topic><topic>Deoxyribonucleic acid</topic><topic>DNA</topic><topic>DNA methylation</topic><topic>DNA sequencing</topic><topic>DNA-Binding Proteins - genetics</topic><topic>DNA-Binding Proteins - metabolism</topic><topic>G-Quadruplexes</topic><topic>Gene expression</topic><topic>Genetic aspects</topic><topic>Genome</topic><topic>Genomes</topic><topic>Laboratories</topic><topic>Methods</topic><topic>Oligonucleotides - genetics</topic><topic>Physical Sciences</topic><topic>Physiological aspects</topic><topic>Protein Binding</topic><topic>Proteins</topic><topic>Protozoan Proteins - genetics</topic><topic>Research and Analysis Methods</topic><topic>Sequence Analysis, DNA</topic><topic>Telomere - genetics</topic><topic>Tetrahymena thermophila</topic><topic>Tetrahymena thermophila - genetics</topic><topic>Thermophiles</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Carle, Christine M</creatorcontrib><creatorcontrib>Zaher, Hani S</creatorcontrib><creatorcontrib>Chalker, Douglas L</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Opposing Viewpoints</collection><collection>Gale In Context: Canada</collection><collection>Gale In Context: Science</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>MEDLINE - Academic</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>Carle, Christine M</au><au>Zaher, Hani S</au><au>Chalker, Douglas L</au><au>Mochizuki, Kazufumi</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>A Parallel G Quadruplex-Binding Protein Regulates the Boundaries of DNA Elimination Events of Tetrahymena thermophila</atitle><jtitle>PLoS genetics</jtitle><addtitle>PLoS Genet</addtitle><date>2016-03-07</date><risdate>2016</risdate><volume>12</volume><issue>3</issue><spage>e1005842</spage><pages>e1005842-</pages><issn>1553-7404</issn><issn>1553-7390</issn><eissn>1553-7404</eissn><abstract>Guanine (G)-rich DNA readily forms four-stranded quadruplexes in vitro, but evidence for their participation in genome regulation is limited. We have identified a quadruplex-binding protein, Lia3, that controls the boundaries of germline-limited, internal eliminated sequences (IESs) of Tetrahymena thermophila. Differentiation of this ciliate's somatic genome requires excision of thousands of IESs, targeted for removal by small-RNA-directed heterochromatin formation. In cells lacking LIA3 (ΔLIA3), the excision of IESs bounded by specific G-rich polypurine tracts was impaired and imprecise, whereas the removal of IESs without such controlling sequences was unaffected. We found that oligonucleotides containing these polypurine tracts formed parallel G-quadruplex structures that are specifically bound by Lia3. The discovery that Lia3 binds G-quadruplex DNA and controls the accuracy of DNA elimination at loci with specific G-tracts uncovers an unrecognized potential of quadruplex structures to regulate chromosome organization.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>26950070</pmid><doi>10.1371/journal.pgen.1005842</doi><oa>free_for_read</oa></addata></record> |
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| subjects | Binding proteins Biology and life sciences Boundaries Chromosomes - genetics Deoxyribonucleic acid DNA DNA methylation DNA sequencing DNA-Binding Proteins - genetics DNA-Binding Proteins - metabolism G-Quadruplexes Gene expression Genetic aspects Genome Genomes Laboratories Methods Oligonucleotides - genetics Physical Sciences Physiological aspects Protein Binding Proteins Protozoan Proteins - genetics Research and Analysis Methods Sequence Analysis, DNA Telomere - genetics Tetrahymena thermophila Tetrahymena thermophila - genetics Thermophiles |
| title | A Parallel G Quadruplex-Binding Protein Regulates the Boundaries of DNA Elimination Events of Tetrahymena thermophila |
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