Serine ADP-ribosylation in Drosophila provides insights into the evolution of reversible ADP-ribosylation signalling

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Serine ADP-ribosylation in Drosophila provides insights into the evolution of reversible ADP-ribosylation signalling. / Fontana, Pietro; Buch-Larsen, Sara C.; Suyari, Osamu; Smith, Rebecca; Suskiewicz, Marcin J.; Schützenhofer, Kira; Ariza, Antonio; Rack, Johannes Gregor Matthias; Nielsen, Michael L.; Ahel, Ivan.

In: Nature Communications, Vol. 14, No. 1, 3200, 2023.

Research output: Contribution to journal › Journal article › Research › peer-review

Harvard

Fontana, P, Buch-Larsen, SC, Suyari, O, Smith, R, Suskiewicz, MJ, Schützenhofer, K, Ariza, A, Rack, JGM, Nielsen, ML & Ahel, I 2023, 'Serine ADP-ribosylation in Drosophila provides insights into the evolution of reversible ADP-ribosylation signalling', Nature Communications, vol. 14, no. 1, 3200. https://doi.org/10.1038/s41467-023-38793-y

APA

Fontana, P., Buch-Larsen, S. C., Suyari, O., Smith, R., Suskiewicz, M. J., Schützenhofer, K., Ariza, A., Rack, J. G. M., Nielsen, M. L., & Ahel, I. (2023). Serine ADP-ribosylation in Drosophila provides insights into the evolution of reversible ADP-ribosylation signalling. Nature Communications, 14(1), [3200]. https://doi.org/10.1038/s41467-023-38793-y

Vancouver

Fontana P, Buch-Larsen SC, Suyari O, Smith R, Suskiewicz MJ, Schützenhofer K et al. Serine ADP-ribosylation in Drosophila provides insights into the evolution of reversible ADP-ribosylation signalling. Nature Communications. 2023;14(1). 3200. https://doi.org/10.1038/s41467-023-38793-y

Author

Fontana, Pietro ; Buch-Larsen, Sara C. ; Suyari, Osamu ; Smith, Rebecca ; Suskiewicz, Marcin J. ; Schützenhofer, Kira ; Ariza, Antonio ; Rack, Johannes Gregor Matthias ; Nielsen, Michael L. ; Ahel, Ivan. / Serine ADP-ribosylation in Drosophila provides insights into the evolution of reversible ADP-ribosylation signalling. In: Nature Communications. 2023 ; Vol. 14, No. 1.

Bibtex

@article{815c84e38978486e9ee5dea292f6cbfb,
title = "Serine ADP-ribosylation in Drosophila provides insights into the evolution of reversible ADP-ribosylation signalling",
abstract = "In the mammalian DNA damage response, ADP-ribosylation signalling is of crucial importance to mark sites of DNA damage as well as recruit and regulate repairs factors. Specifically, the PARP1:HPF1 complex recognises damaged DNA and catalyses the formation of serine-linked ADP-ribosylation marks (mono-Ser-ADPr), which are extended into ADP-ribose polymers (poly-Ser-ADPr) by PARP1 alone. Poly-Ser-ADPr is reversed by PARG, while the terminal mono-Ser-ADPr is removed by ARH3. Despite its significance and apparent evolutionary conservation, little is known about ADP-ribosylation signalling in non-mammalian Animalia. The presence of HPF1, but absence of ARH3, in some insect genomes, including Drosophila species, raises questions regarding the existence and reversal of serine-ADP-ribosylation in these species. Here we show by quantitative proteomics that Ser-ADPr is the major form of ADP-ribosylation in the DNA damage response of Drosophila melanogaster and is dependent on the dParp1:dHpf1 complex. Moreover, our structural and biochemical investigations uncover the mechanism of mono-Ser-ADPr removal by Drosophila Parg. Collectively, our data reveal PARP:HPF1-mediated Ser-ADPr as a defining feature of the DDR in Animalia. The striking conservation within this kingdom suggests that organisms that carry only a core set of ADP-ribosyl metabolising enzymes, such as Drosophila, are valuable model organisms to study the physiological role of Ser-ADPr signalling.",
author = "Pietro Fontana and Buch-Larsen, {Sara C.} and Osamu Suyari and Rebecca Smith and Suskiewicz, {Marcin J.} and Kira Sch{\"u}tzenhofer and Antonio Ariza and Rack, {Johannes Gregor Matthias} and Nielsen, {Michael L.} and Ivan Ahel",
note = "Publisher Copyright: {\textcopyright} 2023, The Author(s).",
year = "2023",
doi = "10.1038/s41467-023-38793-y",
language = "English",
volume = "14",
journal = "Nature Communications",
issn = "2041-1723",
publisher = "nature publishing group",
number = "1",

}

RIS

TY - JOUR

T1 - Serine ADP-ribosylation in Drosophila provides insights into the evolution of reversible ADP-ribosylation signalling

AU - Fontana, Pietro

AU - Buch-Larsen, Sara C.

AU - Suyari, Osamu

AU - Smith, Rebecca

AU - Suskiewicz, Marcin J.

AU - Schützenhofer, Kira

AU - Ariza, Antonio

AU - Rack, Johannes Gregor Matthias

AU - Nielsen, Michael L.

AU - Ahel, Ivan

N1 - Publisher Copyright: © 2023, The Author(s).

PY - 2023

Y1 - 2023

N2 - In the mammalian DNA damage response, ADP-ribosylation signalling is of crucial importance to mark sites of DNA damage as well as recruit and regulate repairs factors. Specifically, the PARP1:HPF1 complex recognises damaged DNA and catalyses the formation of serine-linked ADP-ribosylation marks (mono-Ser-ADPr), which are extended into ADP-ribose polymers (poly-Ser-ADPr) by PARP1 alone. Poly-Ser-ADPr is reversed by PARG, while the terminal mono-Ser-ADPr is removed by ARH3. Despite its significance and apparent evolutionary conservation, little is known about ADP-ribosylation signalling in non-mammalian Animalia. The presence of HPF1, but absence of ARH3, in some insect genomes, including Drosophila species, raises questions regarding the existence and reversal of serine-ADP-ribosylation in these species. Here we show by quantitative proteomics that Ser-ADPr is the major form of ADP-ribosylation in the DNA damage response of Drosophila melanogaster and is dependent on the dParp1:dHpf1 complex. Moreover, our structural and biochemical investigations uncover the mechanism of mono-Ser-ADPr removal by Drosophila Parg. Collectively, our data reveal PARP:HPF1-mediated Ser-ADPr as a defining feature of the DDR in Animalia. The striking conservation within this kingdom suggests that organisms that carry only a core set of ADP-ribosyl metabolising enzymes, such as Drosophila, are valuable model organisms to study the physiological role of Ser-ADPr signalling.

AB - In the mammalian DNA damage response, ADP-ribosylation signalling is of crucial importance to mark sites of DNA damage as well as recruit and regulate repairs factors. Specifically, the PARP1:HPF1 complex recognises damaged DNA and catalyses the formation of serine-linked ADP-ribosylation marks (mono-Ser-ADPr), which are extended into ADP-ribose polymers (poly-Ser-ADPr) by PARP1 alone. Poly-Ser-ADPr is reversed by PARG, while the terminal mono-Ser-ADPr is removed by ARH3. Despite its significance and apparent evolutionary conservation, little is known about ADP-ribosylation signalling in non-mammalian Animalia. The presence of HPF1, but absence of ARH3, in some insect genomes, including Drosophila species, raises questions regarding the existence and reversal of serine-ADP-ribosylation in these species. Here we show by quantitative proteomics that Ser-ADPr is the major form of ADP-ribosylation in the DNA damage response of Drosophila melanogaster and is dependent on the dParp1:dHpf1 complex. Moreover, our structural and biochemical investigations uncover the mechanism of mono-Ser-ADPr removal by Drosophila Parg. Collectively, our data reveal PARP:HPF1-mediated Ser-ADPr as a defining feature of the DDR in Animalia. The striking conservation within this kingdom suggests that organisms that carry only a core set of ADP-ribosyl metabolising enzymes, such as Drosophila, are valuable model organisms to study the physiological role of Ser-ADPr signalling.

U2 - 10.1038/s41467-023-38793-y

DO - 10.1038/s41467-023-38793-y

M3 - Journal article

C2 - 37268618

AN - SCOPUS:85160897386

VL - 14

JO - Nature Communications

JF - Nature Communications

SN - 2041-1723

IS - 1

M1 - 3200

ER -

ID: 357615671