Poly(ADP-ribose) polymerases covalently modify strand break termini in DNA fragments in vitro
Poly(ADP-ribose) polymerases (PARPs/ARTDs) use nicotinamide adenine dinucleotide (NAD ) to catalyse the synthesis of a long branched poly(ADP-ribose) polymer (PAR) attached to the acceptor amino acid residues of nuclear proteins. PARPs act on single- and double-stranded DNA breaks by recruiting DNA...
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| Veröffentlicht in: | Nucleic acids research 2016-11, Vol.44 (19), p.9279-9295 |
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| creator | Talhaoui, Ibtissam Lebedeva, Natalia A Zarkovic, Gabriella Saint-Pierre, Christine Kutuzov, Mikhail M Sukhanova, Maria V Matkarimov, Bakhyt T Gasparutto, Didier Saparbaev, Murat K Lavrik, Olga I Ishchenko, Alexander A |
| description | Poly(ADP-ribose) polymerases (PARPs/ARTDs) use nicotinamide adenine dinucleotide (NAD
) to catalyse the synthesis of a long branched poly(ADP-ribose) polymer (PAR) attached to the acceptor amino acid residues of nuclear proteins. PARPs act on single- and double-stranded DNA breaks by recruiting DNA repair factors. Here, in in vitro biochemical experiments, we found that the mammalian PARP1 and PARP2 proteins can directly ADP-ribosylate the termini of DNA oligonucleotides. PARP1 preferentially catalysed covalent attachment of ADP-ribose units to the ends of recessed DNA duplexes containing 3'-cordycepin, 5'- and 3'-phosphate and also to 5'-phosphate of a single-stranded oligonucleotide. PARP2 preferentially ADP-ribosylated the nicked/gapped DNA duplexes containing 5'-phosphate at the double-stranded termini. PAR glycohydrolase (PARG) restored native DNA structure by hydrolysing PAR-DNA adducts generated by PARP1 and PARP2. Biochemical and mass spectrometry analyses of the adducts suggested that PARPs utilise DNA termini as an alternative to 2'-hydroxyl of ADP-ribose and protein acceptor residues to catalyse PAR chain initiation either via the 2',1″-O-glycosidic ribose-ribose bond or via phosphodiester bond formation between C1' of ADP-ribose and the phosphate of a terminal deoxyribonucleotide. This new type of post-replicative modification of DNA provides novel insights into the molecular mechanisms underlying biological phenomena of ADP-ribosylation mediated by PARPs. |
| doi_str_mv | 10.1093/nar/gkw675 |
| format | Article |
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) to catalyse the synthesis of a long branched poly(ADP-ribose) polymer (PAR) attached to the acceptor amino acid residues of nuclear proteins. PARPs act on single- and double-stranded DNA breaks by recruiting DNA repair factors. Here, in in vitro biochemical experiments, we found that the mammalian PARP1 and PARP2 proteins can directly ADP-ribosylate the termini of DNA oligonucleotides. PARP1 preferentially catalysed covalent attachment of ADP-ribose units to the ends of recessed DNA duplexes containing 3'-cordycepin, 5'- and 3'-phosphate and also to 5'-phosphate of a single-stranded oligonucleotide. PARP2 preferentially ADP-ribosylated the nicked/gapped DNA duplexes containing 5'-phosphate at the double-stranded termini. PAR glycohydrolase (PARG) restored native DNA structure by hydrolysing PAR-DNA adducts generated by PARP1 and PARP2. Biochemical and mass spectrometry analyses of the adducts suggested that PARPs utilise DNA termini as an alternative to 2'-hydroxyl of ADP-ribose and protein acceptor residues to catalyse PAR chain initiation either via the 2',1″-O-glycosidic ribose-ribose bond or via phosphodiester bond formation between C1' of ADP-ribose and the phosphate of a terminal deoxyribonucleotide. This new type of post-replicative modification of DNA provides novel insights into the molecular mechanisms underlying biological phenomena of ADP-ribosylation mediated by PARPs.</description><identifier>ISSN: 0305-1048</identifier><identifier>EISSN: 1362-4962</identifier><identifier>DOI: 10.1093/nar/gkw675</identifier><identifier>PMID: 27471034</identifier><language>eng</language><publisher>England: Oxford University Press</publisher><subject>Animals ; Biochemistry, Molecular Biology ; Catalysis ; DNA - genetics ; DNA - metabolism ; DNA Adducts ; DNA Breaks, Double-Stranded ; Genome Integrity, Repair and ; Genomics ; Humans ; Hydrolysis ; Life Sciences ; Mice ; NAD - metabolism ; Poly (ADP-Ribose) Polymerase-1 - metabolism ; Poly(ADP-ribose) Polymerases - metabolism ; Protein Binding ; Substrate Specificity</subject><ispartof>Nucleic acids research, 2016-11, Vol.44 (19), p.9279-9295</ispartof><rights>The Author(s) 2016. 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) 2016. Published by Oxford University Press on behalf of Nucleic Acids Research. 2016</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c376t-15945ad0a21f17631230d0819ef7502c8202aed229df3fa10ec9907b8bb43f853</citedby><cites>FETCH-LOGICAL-c376t-15945ad0a21f17631230d0819ef7502c8202aed229df3fa10ec9907b8bb43f853</cites><orcidid>0000-0002-1563-9208 ; 0000-0002-0488-8858 ; 0000-0002-7984-6177</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/PMC5100588/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5100588/$$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/27471034$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-03419285$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Talhaoui, Ibtissam</creatorcontrib><creatorcontrib>Lebedeva, Natalia A</creatorcontrib><creatorcontrib>Zarkovic, Gabriella</creatorcontrib><creatorcontrib>Saint-Pierre, Christine</creatorcontrib><creatorcontrib>Kutuzov, Mikhail M</creatorcontrib><creatorcontrib>Sukhanova, Maria V</creatorcontrib><creatorcontrib>Matkarimov, Bakhyt T</creatorcontrib><creatorcontrib>Gasparutto, Didier</creatorcontrib><creatorcontrib>Saparbaev, Murat K</creatorcontrib><creatorcontrib>Lavrik, Olga I</creatorcontrib><creatorcontrib>Ishchenko, Alexander A</creatorcontrib><title>Poly(ADP-ribose) polymerases covalently modify strand break termini in DNA fragments in vitro</title><title>Nucleic acids research</title><addtitle>Nucleic Acids Res</addtitle><description>Poly(ADP-ribose) polymerases (PARPs/ARTDs) use nicotinamide adenine dinucleotide (NAD
) to catalyse the synthesis of a long branched poly(ADP-ribose) polymer (PAR) attached to the acceptor amino acid residues of nuclear proteins. PARPs act on single- and double-stranded DNA breaks by recruiting DNA repair factors. Here, in in vitro biochemical experiments, we found that the mammalian PARP1 and PARP2 proteins can directly ADP-ribosylate the termini of DNA oligonucleotides. PARP1 preferentially catalysed covalent attachment of ADP-ribose units to the ends of recessed DNA duplexes containing 3'-cordycepin, 5'- and 3'-phosphate and also to 5'-phosphate of a single-stranded oligonucleotide. PARP2 preferentially ADP-ribosylated the nicked/gapped DNA duplexes containing 5'-phosphate at the double-stranded termini. PAR glycohydrolase (PARG) restored native DNA structure by hydrolysing PAR-DNA adducts generated by PARP1 and PARP2. Biochemical and mass spectrometry analyses of the adducts suggested that PARPs utilise DNA termini as an alternative to 2'-hydroxyl of ADP-ribose and protein acceptor residues to catalyse PAR chain initiation either via the 2',1″-O-glycosidic ribose-ribose bond or via phosphodiester bond formation between C1' of ADP-ribose and the phosphate of a terminal deoxyribonucleotide. This new type of post-replicative modification of DNA provides novel insights into the molecular mechanisms underlying biological phenomena of ADP-ribosylation mediated by PARPs.</description><subject>Animals</subject><subject>Biochemistry, Molecular Biology</subject><subject>Catalysis</subject><subject>DNA - genetics</subject><subject>DNA - metabolism</subject><subject>DNA Adducts</subject><subject>DNA Breaks, Double-Stranded</subject><subject>Genome Integrity, Repair and</subject><subject>Genomics</subject><subject>Humans</subject><subject>Hydrolysis</subject><subject>Life Sciences</subject><subject>Mice</subject><subject>NAD - metabolism</subject><subject>Poly (ADP-Ribose) Polymerase-1 - metabolism</subject><subject>Poly(ADP-ribose) Polymerases - metabolism</subject><subject>Protein Binding</subject><subject>Substrate Specificity</subject><issn>0305-1048</issn><issn>1362-4962</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkV1P2zAUhq1paBS2m_2AyZeAFHqOHSfOzaQKxodUsV5sl5PlJHbxSOJip53673FVQIwrS68fP_bxS8hXhHOEik8HHabLh39FKT6QCfKCZXlVsI9kAhxEhpDLQ3IU418AzFHkn8ghK_MSgecT8mfhu-3J7HKRBVf7aE7pKgW9CTqaSBu_0Z0Zxm5Le986u6VxDHpoaR2MfqCjCb0bHHUDvbybURv0sk903AUbNwb_mRxY3UXz5Xk9Jr-vfvy6uMnmP69vL2bzrOFlMWYoqlzoFjRDi2XBkXFoQWJlbCmANZIB06ZlrGottxrBNFUFZS3rOudWCn5Mvu-9q3Xdm7ZJjwi6U6vgeh22ymun_t8Z3L1a-o0SCCCkTILTveD-3bGb2VztsvRZWDEpNpjYk-fLgn9cmziq3sXGdJ0ejF9HhZIVJU8j7bRne7QJPsZg7KsbQe26U6k7te8uwd_eDvGKvpTFnwAl1pX8</recordid><startdate>20161102</startdate><enddate>20161102</enddate><creator>Talhaoui, Ibtissam</creator><creator>Lebedeva, Natalia A</creator><creator>Zarkovic, Gabriella</creator><creator>Saint-Pierre, Christine</creator><creator>Kutuzov, Mikhail M</creator><creator>Sukhanova, Maria V</creator><creator>Matkarimov, Bakhyt T</creator><creator>Gasparutto, Didier</creator><creator>Saparbaev, Murat K</creator><creator>Lavrik, Olga I</creator><creator>Ishchenko, Alexander A</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/0000-0002-1563-9208</orcidid><orcidid>https://orcid.org/0000-0002-0488-8858</orcidid><orcidid>https://orcid.org/0000-0002-7984-6177</orcidid></search><sort><creationdate>20161102</creationdate><title>Poly(ADP-ribose) polymerases covalently modify strand break termini in DNA fragments in vitro</title><author>Talhaoui, Ibtissam ; Lebedeva, Natalia A ; Zarkovic, Gabriella ; Saint-Pierre, Christine ; Kutuzov, Mikhail M ; Sukhanova, Maria V ; Matkarimov, Bakhyt T ; Gasparutto, Didier ; Saparbaev, Murat K ; Lavrik, Olga I ; Ishchenko, Alexander A</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c376t-15945ad0a21f17631230d0819ef7502c8202aed229df3fa10ec9907b8bb43f853</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Animals</topic><topic>Biochemistry, Molecular Biology</topic><topic>Catalysis</topic><topic>DNA - genetics</topic><topic>DNA - metabolism</topic><topic>DNA Adducts</topic><topic>DNA Breaks, Double-Stranded</topic><topic>Genome Integrity, Repair and</topic><topic>Genomics</topic><topic>Humans</topic><topic>Hydrolysis</topic><topic>Life Sciences</topic><topic>Mice</topic><topic>NAD - metabolism</topic><topic>Poly (ADP-Ribose) Polymerase-1 - metabolism</topic><topic>Poly(ADP-ribose) Polymerases - metabolism</topic><topic>Protein Binding</topic><topic>Substrate Specificity</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Talhaoui, Ibtissam</creatorcontrib><creatorcontrib>Lebedeva, Natalia A</creatorcontrib><creatorcontrib>Zarkovic, Gabriella</creatorcontrib><creatorcontrib>Saint-Pierre, Christine</creatorcontrib><creatorcontrib>Kutuzov, Mikhail M</creatorcontrib><creatorcontrib>Sukhanova, Maria V</creatorcontrib><creatorcontrib>Matkarimov, Bakhyt T</creatorcontrib><creatorcontrib>Gasparutto, Didier</creatorcontrib><creatorcontrib>Saparbaev, Murat K</creatorcontrib><creatorcontrib>Lavrik, Olga I</creatorcontrib><creatorcontrib>Ishchenko, Alexander A</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>Talhaoui, Ibtissam</au><au>Lebedeva, Natalia A</au><au>Zarkovic, Gabriella</au><au>Saint-Pierre, Christine</au><au>Kutuzov, Mikhail M</au><au>Sukhanova, Maria V</au><au>Matkarimov, Bakhyt T</au><au>Gasparutto, Didier</au><au>Saparbaev, Murat K</au><au>Lavrik, Olga I</au><au>Ishchenko, Alexander A</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Poly(ADP-ribose) polymerases covalently modify strand break termini in DNA fragments in vitro</atitle><jtitle>Nucleic acids research</jtitle><addtitle>Nucleic Acids Res</addtitle><date>2016-11-02</date><risdate>2016</risdate><volume>44</volume><issue>19</issue><spage>9279</spage><epage>9295</epage><pages>9279-9295</pages><issn>0305-1048</issn><eissn>1362-4962</eissn><abstract>Poly(ADP-ribose) polymerases (PARPs/ARTDs) use nicotinamide adenine dinucleotide (NAD
) to catalyse the synthesis of a long branched poly(ADP-ribose) polymer (PAR) attached to the acceptor amino acid residues of nuclear proteins. PARPs act on single- and double-stranded DNA breaks by recruiting DNA repair factors. Here, in in vitro biochemical experiments, we found that the mammalian PARP1 and PARP2 proteins can directly ADP-ribosylate the termini of DNA oligonucleotides. PARP1 preferentially catalysed covalent attachment of ADP-ribose units to the ends of recessed DNA duplexes containing 3'-cordycepin, 5'- and 3'-phosphate and also to 5'-phosphate of a single-stranded oligonucleotide. PARP2 preferentially ADP-ribosylated the nicked/gapped DNA duplexes containing 5'-phosphate at the double-stranded termini. PAR glycohydrolase (PARG) restored native DNA structure by hydrolysing PAR-DNA adducts generated by PARP1 and PARP2. Biochemical and mass spectrometry analyses of the adducts suggested that PARPs utilise DNA termini as an alternative to 2'-hydroxyl of ADP-ribose and protein acceptor residues to catalyse PAR chain initiation either via the 2',1″-O-glycosidic ribose-ribose bond or via phosphodiester bond formation between C1' of ADP-ribose and the phosphate of a terminal deoxyribonucleotide. This new type of post-replicative modification of DNA provides novel insights into the molecular mechanisms underlying biological phenomena of ADP-ribosylation mediated by PARPs.</abstract><cop>England</cop><pub>Oxford University Press</pub><pmid>27471034</pmid><doi>10.1093/nar/gkw675</doi><tpages>17</tpages><orcidid>https://orcid.org/0000-0002-1563-9208</orcidid><orcidid>https://orcid.org/0000-0002-0488-8858</orcidid><orcidid>https://orcid.org/0000-0002-7984-6177</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Animals Biochemistry, Molecular Biology Catalysis DNA - genetics DNA - metabolism DNA Adducts DNA Breaks, Double-Stranded Genome Integrity, Repair and Genomics Humans Hydrolysis Life Sciences Mice NAD - metabolism Poly (ADP-Ribose) Polymerase-1 - metabolism Poly(ADP-ribose) Polymerases - metabolism Protein Binding Substrate Specificity |
| title | Poly(ADP-ribose) polymerases covalently modify strand break termini in DNA fragments in vitro |
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