Mechanistic investigation of human maturation of Okazaki fragments reveals slow kinetics

The final steps of lagging strand synthesis induce maturation of Okazaki fragments via removal of the RNA primers and ligation. Iterative cycles between Polymerase δ (Polδ) and Flap endonuclease-1 (FEN1) remove the primer, with an intermediary nick structure generated for each cycle. Here, we show t...

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Published inNature communications Vol. 13; no. 1; pp. 6973 - 17
Main Authors Raducanu, Vlad-Stefan, Tehseen, Muhammad, Al-Amodi, Amani, Joudeh, Luay I., De Biasio, Alfredo, Hamdan, Samir M.
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 15.11.2022
Nature Publishing Group
Nature Portfolio
Subjects
631/45/147
631/45/173
Deoxyribonucleic acid
DNA
DNA - metabolism
DNA Polymerase III - genetics
DNA Polymerase III - metabolism
DNA repair
DNA Replication
Endonuclease
FEN1 protein
Flap Endonucleases - genetics
Flap Endonucleases - metabolism
Fragments
Humanities and Social Sciences
Humans
Maturation
multidisciplinary
Okazaki fragments
Recombination
Ribonuclease
Ribonucleic acid
RNA
RNA - metabolism
Science
Science (multidisciplinary)
Substrates
Yeast
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Abstract The final steps of lagging strand synthesis induce maturation of Okazaki fragments via removal of the RNA primers and ligation. Iterative cycles between Polymerase δ (Polδ) and Flap endonuclease-1 (FEN1) remove the primer, with an intermediary nick structure generated for each cycle. Here, we show that human Polδ is inefficient in releasing the nick product from FEN1, resulting in non-processive and remarkably slow RNA removal. Ligase 1 (Lig1) can release the nick from FEN1 and actively drive the reaction toward ligation. These mechanisms are coordinated by PCNA, which encircles DNA, and dynamically recruits Polδ, FEN1, and Lig1 to compete for their substrates. Our findings call for investigating additional pathways that may accelerate RNA removal in human cells, such as RNA pre-removal by RNase Hs, which, as demonstrated herein, enhances the maturation rate ~10-fold. They also suggest that FEN1 may attenuate the various activities of Polδ during DNA repair and recombination. Here, the authors investigate the maturation of Okazaki fragments with human proteins and reveal that initiator RNA removal occurs non-processively and slowly suggesting that additional pathways might exist to accelerate RNA removal in cells.
AbstractList The final steps of lagging strand synthesis induce maturation of Okazaki fragments via removal of the RNA primers and ligation. Iterative cycles between Polymerase δ (Polδ) and Flap endonuclease-1 (FEN1) remove the primer, with an intermediary nick structure generated for each cycle. Here, we show that human Polδ is inefficient in releasing the nick product from FEN1, resulting in non-processive and remarkably slow RNA removal. Ligase 1 (Lig1) can release the nick from FEN1 and actively drive the reaction toward ligation. These mechanisms are coordinated by PCNA, which encircles DNA, and dynamically recruits Polδ, FEN1, and Lig1 to compete for their substrates. Our findings call for investigating additional pathways that may accelerate RNA removal in human cells, such as RNA pre-removal by RNase Hs, which, as demonstrated herein, enhances the maturation rate ~10-fold. They also suggest that FEN1 may attenuate the various activities of Polδ during DNA repair and recombination.
The final steps of lagging strand synthesis induce maturation of Okazaki fragments via removal of the RNA primers and ligation. Iterative cycles between Polymerase δ (Polδ) and Flap endonuclease-1 (FEN1) remove the primer, with an intermediary nick structure generated for each cycle. Here, we show that human Polδ is inefficient in releasing the nick product from FEN1, resulting in non-processive and remarkably slow RNA removal. Ligase 1 (Lig1) can release the nick from FEN1 and actively drive the reaction toward ligation. These mechanisms are coordinated by PCNA, which encircles DNA, and dynamically recruits Polδ, FEN1, and Lig1 to compete for their substrates. Our findings call for investigating additional pathways that may accelerate RNA removal in human cells, such as RNA pre-removal by RNase Hs, which, as demonstrated herein, enhances the maturation rate ~10-fold. They also suggest that FEN1 may attenuate the various activities of Polδ during DNA repair and recombination. Here, the authors investigate the maturation of Okazaki fragments with human proteins and reveal that initiator RNA removal occurs non-processively and slowly suggesting that additional pathways might exist to accelerate RNA removal in cells.
The final steps of lagging strand synthesis induce maturation of Okazaki fragments via removal of the RNA primers and ligation. Iterative cycles between Polymerase δ (Polδ) and Flap endonuclease-1 (FEN1) remove the primer, with an intermediary nick structure generated for each cycle. Here, we show that human Polδ is inefficient in releasing the nick product from FEN1, resulting in non-processive and remarkably slow RNA removal. Ligase 1 (Lig1) can release the nick from FEN1 and actively drive the reaction toward ligation. These mechanisms are coordinated by PCNA, which encircles DNA, and dynamically recruits Polδ, FEN1, and Lig1 to compete for their substrates. Our findings call for investigating additional pathways that may accelerate RNA removal in human cells, such as RNA pre-removal by RNase Hs, which, as demonstrated herein, enhances the maturation rate ~10-fold. They also suggest that FEN1 may attenuate the various activities of Polδ during DNA repair and recombination.The final steps of lagging strand synthesis induce maturation of Okazaki fragments via removal of the RNA primers and ligation. Iterative cycles between Polymerase δ (Polδ) and Flap endonuclease-1 (FEN1) remove the primer, with an intermediary nick structure generated for each cycle. Here, we show that human Polδ is inefficient in releasing the nick product from FEN1, resulting in non-processive and remarkably slow RNA removal. Ligase 1 (Lig1) can release the nick from FEN1 and actively drive the reaction toward ligation. These mechanisms are coordinated by PCNA, which encircles DNA, and dynamically recruits Polδ, FEN1, and Lig1 to compete for their substrates. Our findings call for investigating additional pathways that may accelerate RNA removal in human cells, such as RNA pre-removal by RNase Hs, which, as demonstrated herein, enhances the maturation rate ~10-fold. They also suggest that FEN1 may attenuate the various activities of Polδ during DNA repair and recombination.
The final steps of lagging strand synthesis induce maturation of Okazaki fragments via removal of the RNA primers and ligation. Iterative cycles between Polymerase δ (Polδ) and Flap endonuclease-1 (FEN1) remove the primer, with an intermediary nick structure generated for each cycle. Here, we show that human Polδ is inefficient in releasing the nick product from FEN1, resulting in non-processive and remarkably slow RNA removal. Ligase 1 (Lig1) can release the nick from FEN1 and actively drive the reaction toward ligation. These mechanisms are coordinated by PCNA, which encircles DNA, and dynamically recruits Polδ, FEN1, and Lig1 to compete for their substrates. Our findings call for investigating additional pathways that may accelerate RNA removal in human cells, such as RNA pre-removal by RNase Hs, which, as demonstrated herein, enhances the maturation rate ~10-fold. They also suggest that FEN1 may attenuate the various activities of Polδ during DNA repair and recombination.Here, the authors investigate the maturation of Okazaki fragments with human proteins and reveal that initiator RNA removal occurs non-processively and slowly suggesting that additional pathways might exist to accelerate RNA removal in cells.
Here, the authors investigate the maturation of Okazaki fragments with human proteins and reveal that initiator RNA removal occurs non-processively and slowly suggesting that additional pathways might exist to accelerate RNA removal in cells.
ArticleNumber 6973
Author Hamdan, Samir M.
Raducanu, Vlad-Stefan
De Biasio, Alfredo
Al-Amodi, Amani
Joudeh, Luay I.
Tehseen, Muhammad
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/36379932$$D View this record in MEDLINE/PubMed
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PublicationPlace_xml – name: London
– name: England
PublicationTitle Nature communications
PublicationTitleAbbrev Nat Commun
PublicationTitleAlternate Nat Commun
PublicationYear 2022
Publisher Nature Publishing Group UK
Nature Publishing Group
Nature Portfolio
Publisher_xml – name: Nature Publishing Group UK
– name: Nature Publishing Group
– name: Nature Portfolio
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Snippet The final steps of lagging strand synthesis induce maturation of Okazaki fragments via removal of the RNA primers and ligation. Iterative cycles between...
Here, the authors investigate the maturation of Okazaki fragments with human proteins and reveal that initiator RNA removal occurs non-processively and slowly...
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SubjectTerms 631/45/147
631/45/173
Deoxyribonucleic acid
DNA
DNA - metabolism
DNA Polymerase III - genetics
DNA Polymerase III - metabolism
DNA repair
DNA Replication
Endonuclease
FEN1 protein
Flap Endonucleases - genetics
Flap Endonucleases - metabolism
Fragments
Humanities and Social Sciences
Humans
Maturation
multidisciplinary
Okazaki fragments
Recombination
Ribonuclease
Ribonucleic acid
RNA
RNA - metabolism
Science
Science (multidisciplinary)
Substrates
Yeast
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Title Mechanistic investigation of human maturation of Okazaki fragments reveals slow kinetics
URI https://link.springer.com/article/10.1038/s41467-022-34751-2
https://www.ncbi.nlm.nih.gov/pubmed/36379932
https://www.proquest.com/docview/2736504627
https://www.proquest.com/docview/2737118502
https://pubmed.ncbi.nlm.nih.gov/PMC9666535
https://doaj.org/article/ac250a7a603b45faab1879d0f65dbec0
Volume 13
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