Diastereomeric Recognition of 5',8-cyclo-2'-Deoxyadenosine Lesions by Human Poly(ADP-ribose) Polymerase 1 in a Biomimetic Model.
Identifieur interne : 000602 ( PubMed/Checkpoint ); précédent : 000601; suivant : 000603Diastereomeric Recognition of 5',8-cyclo-2'-Deoxyadenosine Lesions by Human Poly(ADP-ribose) Polymerase 1 in a Biomimetic Model.
Auteurs : Annalisa Masi [Italie] ; Arianna Sabbia [Italie] ; Carla Ferreri [Italie] ; Francesco Manoli [Italie] ; Yanhao Lai [États-Unis] ; Eduardo Laverde [États-Unis] ; Yuan Liu [États-Unis] ; Marios G. Krokidis [Grèce] ; Chryssostomos Chatgilialoglu [Italie] ; Maria Rosaria Faraone Mennella [Italie]Source :
- Cells [ 2073-4409 ] ; 2019.
Descripteurs français
- KwdFr :
- MESH :
English descriptors
- KwdEn :
- MESH :
- chemical , chemistry : Deoxyadenosines.
- chemical , metabolism : Oligonucleotides, Poly (ADP-Ribose) Polymerase-1.
- Biomimetics, DNA Damage, Fluorescence, Humans, Models, Biological, Molecular Weight, Protein Binding, Stereoisomerism, Substrate Specificity, Temperature.
Abstract
5',8-Cyclo-2'-deoxyadenosine (cdA), in the 5'R and 5'Sdiastereomeric forms, are typical non strand-break oxidative DNA lesions, induced by hydroxyl radicals, with emerging importance as a molecular marker. These lesions are exclusively repaired by the nucleotide excision repair (NER) mechanism with a low efficiency, thus readily accumulating in the genome. Poly(ADP-ribose) polymerase1 (PARP1) acts as an early responder to DNA damage and plays a key role as a nick sensor in the maintenance of the integrity of the genome by recognizing nicked DNA. So far, it was unknown whether the two diastereomeric cdA lesions could induce specific PARP1 binding. Here, we provide the first evidence of PARP1 to selectively recognize the diastereomeric lesions of 5'S-cdA and 5'R-cdA in vitro as compared to deoxyadenosine in model DNA substrates (23-mers) by using circular dichroism, fluorescence spectroscopy, immunoblotting analysis, and gel mobility shift assay. Several features of the recognition of the damaged and undamaged oligonucleotides by PARP1 were characterized. Remarkably, PARP1 exhibits different affinities in binding to a double strand (ds) oligonucleotide, which incorporates cdA lesions in R and S diastereomeric form. In particular, PARP1 proved to bind oligonucleotides, including a 5'S-cdA, with a higher affinity constant for the 5'S lesion in a model of ds DNA than 5'R-cdA, showing different recognition patterns, also compared with undamaged dA. This new finding highlights the ability of PARP1 to recognize and differentiate the distorted DNA backbone in a biomimetic system caused by different diastereomeric forms of a cdA lesion.
DOI: 10.3390/cells8020116
PubMed: 30717407
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Krokidis</name><affiliation wicri:level="1"><nlm:affiliation>Institute of Nanoscience and Nanotechnology, NCSR Demokritos Agia Paraskevi, 15310 Athens, Greece. m.krokidis@inn.demokritos.gr.</nlm:affiliation><country xml:lang="fr">Grèce</country><wicri:regionArea>Institute of Nanoscience and Nanotechnology, NCSR Demokritos Agia Paraskevi, 15310 Athens</wicri:regionArea><placeName><settlement type="city">Athènes</settlement><region nuts="2" type="region">Attique (région)</region></placeName></affiliation></author><author><name sortKey="Chatgilialoglu, Chryssostomos" sort="Chatgilialoglu, Chryssostomos" uniqKey="Chatgilialoglu C" first="Chryssostomos" last="Chatgilialoglu">Chryssostomos Chatgilialoglu</name><affiliation wicri:level="1"><nlm:affiliation>Istituto per la Sintesi Organica e la Fotoreattività, Consiglio Nazionale delle Ricerche, 40129 Bologna, Italy. chrys@isof.cnr.it.</nlm:affiliation><country xml:lang="fr">Italie</country><wicri:regionArea>Istituto per la Sintesi Organica e 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xml:lang="fr">Italie</country><wicri:regionArea>Istituto per la Sintesi Organica e la Fotoreattività, Consiglio Nazionale delle Ricerche, 40129 Bologna</wicri:regionArea><wicri:noRegion>40129 Bologna</wicri:noRegion></affiliation></author><author><name sortKey="Sabbia, Arianna" sort="Sabbia, Arianna" uniqKey="Sabbia A" first="Arianna" last="Sabbia">Arianna Sabbia</name><affiliation wicri:level="1"><nlm:affiliation>Dipartimento di Biologia, Università di Napoli "Federico II", 80138 Napoli, Italy. ar.sabbia@studenti.unina.it.</nlm:affiliation><country xml:lang="fr">Italie</country><wicri:regionArea>Dipartimento di Biologia, Università di Napoli "Federico II", 80138 Napoli</wicri:regionArea><wicri:noRegion>80138 Napoli</wicri:noRegion></affiliation></author><author><name sortKey="Ferreri, Carla" sort="Ferreri, Carla" uniqKey="Ferreri C" first="Carla" last="Ferreri">Carla Ferreri</name><affiliation wicri:level="1"><nlm:affiliation>Istituto per la Sintesi Organica e la Fotoreattività, Consiglio Nazionale delle Ricerche, 40129 Bologna, Italy. carla.ferreri@isof.cnr.it.</nlm:affiliation><country xml:lang="fr">Italie</country><wicri:regionArea>Istituto per la Sintesi Organica e la Fotoreattività, Consiglio Nazionale delle Ricerche, 40129 Bologna</wicri:regionArea><wicri:noRegion>40129 Bologna</wicri:noRegion></affiliation></author><author><name sortKey="Manoli, Francesco" sort="Manoli, Francesco" uniqKey="Manoli F" first="Francesco" last="Manoli">Francesco Manoli</name><affiliation wicri:level="1"><nlm:affiliation>Istituto per la Sintesi Organica e la Fotoreattività, Consiglio Nazionale delle Ricerche, 40129 Bologna, Italy. francesco.manoli@isof.cnr.it.</nlm:affiliation><country xml:lang="fr">Italie</country><wicri:regionArea>Istituto per la Sintesi Organica e la Fotoreattività, Consiglio Nazionale delle Ricerche, 40129 Bologna</wicri:regionArea><wicri:noRegion>40129 Bologna</wicri:noRegion></affiliation></author><author><name sortKey="Lai, Yanhao" sort="Lai, Yanhao" uniqKey="Lai Y" first="Yanhao" last="Lai">Yanhao Lai</name><affiliation wicri:level="2"><nlm:affiliation>Department of Chemistry and Biochemistry, Florida International University, Miami, FL 33199, USA. yalai@fiu.edu.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Chemistry and Biochemistry, Florida International University, Miami, FL 33199</wicri:regionArea><placeName><region type="state">Floride</region></placeName></affiliation></author><author><name sortKey="Laverde, Eduardo" sort="Laverde, Eduardo" uniqKey="Laverde E" first="Eduardo" last="Laverde">Eduardo Laverde</name><affiliation wicri:level="2"><nlm:affiliation>Biochemistry Ph.D. Program, Florida International University, Miami, FL 33199, USA. elave006@fiu.edu.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Biochemistry Ph.D. Program, Florida International University, Miami, FL 33199</wicri:regionArea><placeName><region type="state">Floride</region></placeName></affiliation></author><author><name sortKey="Liu, Yuan" sort="Liu, Yuan" uniqKey="Liu Y" first="Yuan" last="Liu">Yuan Liu</name><affiliation wicri:level="2"><nlm:affiliation>Department of Chemistry and Biochemistry, Florida International University, Miami, FL 33199, USA. yualiu@fiu.edu.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Chemistry and Biochemistry, Florida International University, Miami, FL 33199</wicri:regionArea><placeName><region type="state">Floride</region></placeName></affiliation></author><author><name sortKey="Krokidis, Marios G" sort="Krokidis, Marios G" uniqKey="Krokidis M" first="Marios G" last="Krokidis">Marios G. Krokidis</name><affiliation wicri:level="1"><nlm:affiliation>Institute of Nanoscience and Nanotechnology, NCSR Demokritos Agia Paraskevi, 15310 Athens, Greece. m.krokidis@inn.demokritos.gr.</nlm:affiliation><country xml:lang="fr">Grèce</country><wicri:regionArea>Institute of Nanoscience and Nanotechnology, NCSR Demokritos Agia Paraskevi, 15310 Athens</wicri:regionArea><placeName><settlement type="city">Athènes</settlement><region nuts="2" type="region">Attique (région)</region></placeName></affiliation></author><author><name sortKey="Chatgilialoglu, Chryssostomos" sort="Chatgilialoglu, Chryssostomos" uniqKey="Chatgilialoglu C" first="Chryssostomos" last="Chatgilialoglu">Chryssostomos Chatgilialoglu</name><affiliation wicri:level="1"><nlm:affiliation>Istituto per la Sintesi Organica e la Fotoreattività, Consiglio Nazionale delle Ricerche, 40129 Bologna, Italy. chrys@isof.cnr.it.</nlm:affiliation><country xml:lang="fr">Italie</country><wicri:regionArea>Istituto per la Sintesi Organica e la Fotoreattività, Consiglio Nazionale delle Ricerche, 40129 Bologna</wicri:regionArea><wicri:noRegion>40129 Bologna</wicri:noRegion></affiliation></author><author><name sortKey="Faraone Mennella, Maria Rosaria" sort="Faraone Mennella, Maria Rosaria" uniqKey="Faraone Mennella M" first="Maria Rosaria" last="Faraone Mennella">Maria Rosaria Faraone Mennella</name><affiliation wicri:level="1"><nlm:affiliation>Dipartimento di Biologia, Università di Napoli "Federico II", 80138 Napoli, Italy. faraone@unina.it.</nlm:affiliation><country xml:lang="fr">Italie</country><wicri:regionArea>Dipartimento di Biologia, Università di Napoli "Federico II", 80138 Napoli</wicri:regionArea><wicri:noRegion>80138 Napoli</wicri:noRegion></affiliation></author></analytic><series><title level="j">Cells</title><idno type="ISSN">2073-4409</idno><imprint><date when="2019" type="published">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Biomimetics</term><term>DNA Damage</term><term>Deoxyadenosines (chemistry)</term><term>Fluorescence</term><term>Humans</term><term>Models, Biological</term><term>Molecular Weight</term><term>Oligonucleotides (metabolism)</term><term>Poly (ADP-Ribose) Polymerase-1 (metabolism)</term><term>Protein Binding</term><term>Stereoisomerism</term><term>Substrate Specificity</term><term>Temperature</term></keywords><keywords scheme="KwdFr" xml:lang="fr"><term>Altération de l'ADN</term><term>Biomimétique</term><term>Désoxyadénosine ()</term><term>Fluorescence</term><term>Humains</term><term>Liaison aux protéines</term><term>Masse moléculaire</term><term>Modèles biologiques</term><term>Oligonucléotides (métabolisme)</term><term>Poly (ADP-Ribose) polymerase-1 (métabolisme)</term><term>Spécificité du substrat</term><term>Stéréoisomérie</term><term>Température</term></keywords><keywords scheme="MESH" type="chemical" qualifier="chemistry" xml:lang="en"><term>Deoxyadenosines</term></keywords><keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>Oligonucleotides</term><term>Poly (ADP-Ribose) Polymerase-1</term></keywords><keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr"><term>Oligonucléotides</term><term>Poly (ADP-Ribose) polymerase-1</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Biomimetics</term><term>DNA Damage</term><term>Fluorescence</term><term>Humans</term><term>Models, Biological</term><term>Molecular Weight</term><term>Protein Binding</term><term>Stereoisomerism</term><term>Substrate Specificity</term><term>Temperature</term></keywords><keywords scheme="MESH" xml:lang="fr"><term>Altération de l'ADN</term><term>Biomimétique</term><term>Désoxyadénosine</term><term>Fluorescence</term><term>Humains</term><term>Liaison aux protéines</term><term>Masse moléculaire</term><term>Modèles biologiques</term><term>Spécificité du substrat</term><term>Stéréoisomérie</term><term>Température</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">5',8-Cyclo-2'-deoxyadenosine (cdA), in the 5'<i>R</i> and 5'<i>S</i>diastereomeric forms, are typical non strand-break oxidative DNA lesions, induced by hydroxyl radicals, with emerging importance as a molecular marker. These lesions are exclusively repaired by the nucleotide excision repair (NER) mechanism with a low efficiency, thus readily accumulating in the genome. Poly(ADP-ribose) polymerase1 (PARP1) acts as an early responder to DNA damage and plays a key role as a nick sensor in the maintenance of the integrity of the genome by recognizing nicked DNA. So far, it was unknown whether the two diastereomeric cdA lesions could induce specific PARP1 binding. Here, we provide the first evidence of PARP1 to selectively recognize the diastereomeric lesions of 5'<i>S</i>-cdA and 5'<i>R</i>-cdA in vitro as compared to deoxyadenosine in model DNA substrates (23-mers) by using circular dichroism, fluorescence spectroscopy, immunoblotting analysis, and gel mobility shift assay. Several features of the recognition of the damaged and undamaged oligonucleotides by PARP1 were characterized. Remarkably, PARP1 exhibits different affinities in binding to a double strand (ds) oligonucleotide, which incorporates cdA lesions in <i>R</i> and <i>S</i> diastereomeric form. In particular, PARP1 proved to bind oligonucleotides, including a 5'<i>S</i>-cdA, with a higher affinity constant for the 5'<i>S</i> lesion in a model of ds DNA than 5'<i>R</i>-cdA, showing different recognition patterns, also compared with undamaged dA. This new finding highlights the ability of PARP1 to recognize and differentiate the distorted DNA backbone in a biomimetic system caused by different diastereomeric forms of a cdA lesion.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">30717407</PMID><DateCompleted><Year>2019</Year><Month>12</Month><Day>03</Day></DateCompleted><DateRevised><Year>2020</Year><Month>03</Month><Day>09</Day></DateRevised><Article PubModel="Electronic"><Journal><ISSN IssnType="Print">2073-4409</ISSN><JournalIssue CitedMedium="Print"><Volume>8</Volume><Issue>2</Issue><PubDate><Year>2019</Year><Month>02</Month><Day>02</Day></PubDate></JournalIssue><Title>Cells</Title><ISOAbbreviation>Cells</ISOAbbreviation></Journal><ArticleTitle>Diastereomeric Recognition of 5',8-cyclo-2'-Deoxyadenosine Lesions by Human Poly(ADP-ribose) Polymerase 1 in a Biomimetic Model.</ArticleTitle><ELocationID EIdType="pii" ValidYN="Y">E116</ELocationID><ELocationID EIdType="doi" ValidYN="Y">10.3390/cells8020116</ELocationID><Abstract><AbstractText>5',8-Cyclo-2'-deoxyadenosine (cdA), in the 5'<i>R</i> and 5'<i>S</i>diastereomeric forms, are typical non strand-break oxidative DNA lesions, induced by hydroxyl radicals, with emerging importance as a molecular marker. These lesions are exclusively repaired by the nucleotide excision repair (NER) mechanism with a low efficiency, thus readily accumulating in the genome. Poly(ADP-ribose) polymerase1 (PARP1) acts as an early responder to DNA damage and plays a key role as a nick sensor in the maintenance of the integrity of the genome by recognizing nicked DNA. So far, it was unknown whether the two diastereomeric cdA lesions could induce specific PARP1 binding. Here, we provide the first evidence of PARP1 to selectively recognize the diastereomeric lesions of 5'<i>S</i>-cdA and 5'<i>R</i>-cdA in vitro as compared to deoxyadenosine in model DNA substrates (23-mers) by using circular dichroism, fluorescence spectroscopy, immunoblotting analysis, and gel mobility shift assay. Several features of the recognition of the damaged and undamaged oligonucleotides by PARP1 were characterized. Remarkably, PARP1 exhibits different affinities in binding to a double strand (ds) oligonucleotide, which incorporates cdA lesions in <i>R</i> and <i>S</i> diastereomeric form. In particular, PARP1 proved to bind oligonucleotides, including a 5'<i>S</i>-cdA, with a higher affinity constant for the 5'<i>S</i> lesion in a model of ds DNA than 5'<i>R</i>-cdA, showing different recognition patterns, also compared with undamaged dA. This new finding highlights the ability of PARP1 to recognize and differentiate the distorted DNA backbone in a biomimetic system caused by different diastereomeric forms of a cdA lesion.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Masi</LastName><ForeName>Annalisa</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Istituto per la Sintesi Organica e la Fotoreattività, Consiglio Nazionale delle Ricerche, 40129 Bologna, Italy. annalisa.masi@isof.cnr.it.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Sabbia</LastName><ForeName>Arianna</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Dipartimento di Biologia, Università di Napoli "Federico II", 80138 Napoli, Italy. ar.sabbia@studenti.unina.it.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Ferreri</LastName><ForeName>Carla</ForeName><Initials>C</Initials><Identifier Source="ORCID">0000-0002-1359-0869</Identifier><AffiliationInfo><Affiliation>Istituto per la Sintesi Organica e la Fotoreattività, Consiglio Nazionale delle Ricerche, 40129 Bologna, Italy. carla.ferreri@isof.cnr.it.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Manoli</LastName><ForeName>Francesco</ForeName><Initials>F</Initials><Identifier Source="ORCID">0000-0003-2734-1625</Identifier><AffiliationInfo><Affiliation>Istituto per la Sintesi Organica e la Fotoreattività, Consiglio Nazionale delle Ricerche, 40129 Bologna, Italy. francesco.manoli@isof.cnr.it.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Lai</LastName><ForeName>Yanhao</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>Department of Chemistry and Biochemistry, Florida International University, Miami, FL 33199, USA. yalai@fiu.edu.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Laverde</LastName><ForeName>Eduardo</ForeName><Initials>E</Initials><AffiliationInfo><Affiliation>Biochemistry Ph.D. Program, Florida International University, Miami, FL 33199, USA. elave006@fiu.edu.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Liu</LastName><ForeName>Yuan</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>Department of Chemistry and Biochemistry, Florida International University, Miami, FL 33199, USA. yualiu@fiu.edu.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Biochemistry Ph.D. Program, Florida International University, Miami, FL 33199, USA. yualiu@fiu.edu.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Biomolecular Sciences Institute, Florida International University, Miami, FL 33199, USA. yualiu@fiu.edu.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Krokidis</LastName><ForeName>Marios G</ForeName><Initials>MG</Initials><AffiliationInfo><Affiliation>Institute of Nanoscience and Nanotechnology, NCSR Demokritos Agia Paraskevi, 15310 Athens, Greece. m.krokidis@inn.demokritos.gr.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Chatgilialoglu</LastName><ForeName>Chryssostomos</ForeName><Initials>C</Initials><Identifier Source="ORCID">0000-0003-2626-2925</Identifier><AffiliationInfo><Affiliation>Istituto per la Sintesi Organica e la Fotoreattività, Consiglio Nazionale delle Ricerche, 40129 Bologna, Italy. chrys@isof.cnr.it.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Faraone Mennella</LastName><ForeName>Maria Rosaria</ForeName><Initials>MR</Initials><Identifier Source="ORCID">0000-0003-1947-4700</Identifier><AffiliationInfo><Affiliation>Dipartimento di Biologia, Università di Napoli "Federico II", 80138 Napoli, Italy. faraone@unina.it.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>R01 ES023569</GrantID><Acronym>ES</Acronym><Agency>NIEHS NIH HHS</Agency><Country>United States</Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D052061">Research Support, N.I.H., Extramural</PublicationType><PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2019</Year><Month>02</Month><Day>02</Day></ArticleDate></Article><MedlineJournalInfo><Country>Switzerland</Country><MedlineTA>Cells</MedlineTA><NlmUniqueID>101600052</NlmUniqueID><ISSNLinking>2073-4409</ISSNLinking></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D003839">Deoxyadenosines</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance 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MajorTopicYN="N">Fluorescence</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D006801" MajorTopicYN="N">Humans</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D008954" MajorTopicYN="Y">Models, Biological</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D008970" MajorTopicYN="N">Molecular Weight</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D009841" MajorTopicYN="N">Oligonucleotides</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D000071137" MajorTopicYN="N">Poly (ADP-Ribose) Polymerase-1</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D011485" MajorTopicYN="N">Protein Binding</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D013237" MajorTopicYN="N">Stereoisomerism</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D013379" 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