Article Dans Une Revue Science Année : 2023

Visualizing the DNA repair process by a photolyase at atomic resolution

Manuel Maestre-Reyna (1, 2) , Po-Hsun Wang (1) , Eriko Nango (3, 4) , Yuhei Hosokawa (1, 2, 5) , Martin Saft (6) , Antonia Furrer (7) , Cheng-Han Yang (1) , Eka Putra Gusti Ngurah Putu (1) , Wen-Jin Wu (1) , Hans-Joachim Emmerich (6) , Nicolas Caramello (8, 9) , Sophie Franz-Badur (6) , Chao Yang (10) , Sylvain Engilberge (8, 11) , Maximilian Wranik (7) , Hannah Louise Glover (7) , Tobias Weinert (7) , Hsiang-Yi Wu (1) , Cheng-Chung Lee (1) , Wei-Cheng Huang (1) , Kai-Fa Huang (1) , Yao-Kai Chang (1) , Jiahn-Haur Liao (1) , Jui-Hung Weng (1) , Wael Gad (1) , Chiung-Wen Chang (1) , Allan Pang (1) , Kai-Chun Yang (2) , Wei-Ting Lin (2) , Yu-Chen Chang (2) , Dardan Gashi (7) , Emma Beale (7) , Dmitry Ozerov (7) , Karol Nass (7) , Gregor Knopp (7) , Philip Johnson (7) , Claudio Cirelli (7) , Chris Milne (7) , Camila Bacellar (7) , Michihiro Sugahara (3) , Shigeki Owada (3) , Yasumasa Joti (3) , Ayumi Yamashita (3) , Rie Tanaka (3) , Tomoyuki Tanaka (3) , Fangjia Luo (12) , Kensuke Tono (3) , Wiktoria Zarzycka (13, 14) , Pavel Müller (13, 14) , Maisa Alkheder Alahmad (6) , Filipp Bezold (6) , Valerie Fuchs (6) , Petra Gnau (6) , Stephan Kiontke (6) , Lukas Korf (6) , Viktoria Reithofer (6) , Christian Joshua Rosner (6) , Elisa Marie Seiler (6) , Mohamed Watad (6) , Laura Werel (6) , Roberta Spadaccini (6, 15) , Junpei Yamamoto (5) , So Iwata (3) , Dongping Zhong (10, 16, 17) , Jörg Standfuss (7) , Antoine Royant (8, 11) , Yoshitaka Bessho (1, 3) , Lars-Oliver Essen (6) , Ming-Daw Tsai (1, 18)
1 IBC Sinica - Institute of Biological Chemistry [Tapei]
2 Department of Chemistry, National Taiwan University, 1, Roosevelt Rd. Sec. 4, Taipei 106, Taiwan.
3 RIKEN RSC - RIKEN SPring-8 Center [Hyogo]
4 IMRAM - Institute of Multidisciplinary Research for Advanced Materials [Tohoku University]
5 Department of Chemistry - Graduate School of Engineering Science, Osaka University
6 Department of Chemistry, Philipps University Marburg, Hans-Meerwein Strasse 4, Marburg 35032, Germany.
7 PSI - Paul Scherrer Institute
8 ESRF - European Synchrotron Radiation Facility [Grenoble]
9 Hamburg Centre for Ultrafast Imaging [Universität Hamburg]
10 OSU - Department of Physics [Ohio State University]
11 IBS - UMR 5075 - Institut de biologie structurale
12 JASRI - Japan Synchrotron Radiation Research Institute [Hyogo]
13 I2BC - Institut de Biologie Intégrative de la Cellule
14 B3S - Département Biochimie, Biophysique et Biologie Structurale
15 Dipartimento di Scienze e Tecnologie, Università degli Studi del Sannio, Benevento
16 OSU - Department of Chemistry and Biochemistry [Ohio State University]
17 Shangaï Jiao Tong University [Shangaï]
18 Institute of Biochemical Sciences
Manuel Maestre-Reyna
IBC Sinica - Institute of Biological Chemistry [Tapei]
Department of Chemistry, National Taiwan University, 1, Roosevelt Rd. Sec. 4, Taipei 106, Taiwan.
Po-Hsun Wang
IBC Sinica - Institute of Biological Chemistry [Tapei]
Eriko Nango
RIKEN RSC - RIKEN SPring-8 Center [Hyogo]
IMRAM - Institute of Multidisciplinary Research for Advanced Materials [Tohoku University]
Yuhei Hosokawa
IBC Sinica - Institute of Biological Chemistry [Tapei]
Department of Chemistry, National Taiwan University, 1, Roosevelt Rd. Sec. 4, Taipei 106, Taiwan.
Department of Chemistry - Graduate School of Engineering Science, Osaka University
Martin Saft
Department of Chemistry, Philipps University Marburg, Hans-Meerwein Strasse 4, Marburg 35032, Germany.
Antonia Furrer
PSI - Paul Scherrer Institute
Cheng-Han Yang
IBC Sinica - Institute of Biological Chemistry [Tapei]
Eka Putra Gusti Ngurah Putu
IBC Sinica - Institute of Biological Chemistry [Tapei]
Wen-Jin Wu
IBC Sinica - Institute of Biological Chemistry [Tapei]
Hans-Joachim Emmerich
Department of Chemistry, Philipps University Marburg, Hans-Meerwein Strasse 4, Marburg 35032, Germany.
Nicolas Caramello
ESRF - European Synchrotron Radiation Facility [Grenoble]
Hamburg Centre for Ultrafast Imaging [Universität Hamburg]
CV
Sophie Franz-Badur
Department of Chemistry, Philipps University Marburg, Hans-Meerwein Strasse 4, Marburg 35032, Germany.
Chao Yang
OSU - Department of Physics [Ohio State University]
Sylvain Engilberge
ESRF - European Synchrotron Radiation Facility [Grenoble]
IBS - UMR 5075 - Institut de biologie structurale
Maximilian Wranik
PSI - Paul Scherrer Institute
Hannah Louise Glover
PSI - Paul Scherrer Institute
Tobias Weinert
PSI - Paul Scherrer Institute
Hsiang-Yi Wu
IBC Sinica - Institute of Biological Chemistry [Tapei]
Cheng-Chung Lee
IBC Sinica - Institute of Biological Chemistry [Tapei]
Wei-Cheng Huang
IBC Sinica - Institute of Biological Chemistry [Tapei]
Kai-Fa Huang
IBC Sinica - Institute of Biological Chemistry [Tapei]
Yao-Kai Chang
IBC Sinica - Institute of Biological Chemistry [Tapei]
Jiahn-Haur Liao
IBC Sinica - Institute of Biological Chemistry [Tapei]
Jui-Hung Weng
IBC Sinica - Institute of Biological Chemistry [Tapei]
Wael Gad
IBC Sinica - Institute of Biological Chemistry [Tapei]
Chiung-Wen Chang
  • Fonction : Auteur
IBC Sinica - Institute of Biological Chemistry [Tapei]
Allan Pang
IBC Sinica - Institute of Biological Chemistry [Tapei]
Kai-Chun Yang
  • Fonction : Auteur
Department of Chemistry, National Taiwan University, 1, Roosevelt Rd. Sec. 4, Taipei 106, Taiwan.
Wei-Ting Lin
Department of Chemistry, National Taiwan University, 1, Roosevelt Rd. Sec. 4, Taipei 106, Taiwan.
Yu-Chen Chang
Department of Chemistry, National Taiwan University, 1, Roosevelt Rd. Sec. 4, Taipei 106, Taiwan.
Dardan Gashi
  • Fonction : Auteur
PSI - Paul Scherrer Institute
Emma Beale
PSI - Paul Scherrer Institute
Dmitry Ozerov
PSI - Paul Scherrer Institute
Karol Nass
PSI - Paul Scherrer Institute
Gregor Knopp
PSI - Paul Scherrer Institute
Philip Johnson
PSI - Paul Scherrer Institute
Claudio Cirelli
PSI - Paul Scherrer Institute
Chris Milne
PSI - Paul Scherrer Institute
Camila Bacellar
PSI - Paul Scherrer Institute
Michihiro Sugahara
  • Fonction : Auteur
RIKEN RSC - RIKEN SPring-8 Center [Hyogo]
Shigeki Owada
RIKEN RSC - RIKEN SPring-8 Center [Hyogo]
Yasumasa Joti
RIKEN RSC - RIKEN SPring-8 Center [Hyogo]
Ayumi Yamashita
RIKEN RSC - RIKEN SPring-8 Center [Hyogo]
Rie Tanaka
RIKEN RSC - RIKEN SPring-8 Center [Hyogo]
Tomoyuki Tanaka
  • Fonction : Auteur
RIKEN RSC - RIKEN SPring-8 Center [Hyogo]
Fangjia Luo
JASRI - Japan Synchrotron Radiation Research Institute [Hyogo]
Kensuke Tono
RIKEN RSC - RIKEN SPring-8 Center [Hyogo]
Wiktoria Zarzycka
  • Fonction : Auteur
I2BC - Institut de Biologie Intégrative de la Cellule
B3S - Département Biochimie, Biophysique et Biologie Structurale
Pavel Müller
I2BC - Institut de Biologie Intégrative de la Cellule
B3S - Département Biochimie, Biophysique et Biologie Structurale
CV
Maisa Alkheder Alahmad
Department of Chemistry, Philipps University Marburg, Hans-Meerwein Strasse 4, Marburg 35032, Germany.
Filipp Bezold
Department of Chemistry, Philipps University Marburg, Hans-Meerwein Strasse 4, Marburg 35032, Germany.
Valerie Fuchs
Department of Chemistry, Philipps University Marburg, Hans-Meerwein Strasse 4, Marburg 35032, Germany.
Petra Gnau
  • Fonction : Auteur
Department of Chemistry, Philipps University Marburg, Hans-Meerwein Strasse 4, Marburg 35032, Germany.
Stephan Kiontke
Department of Chemistry, Philipps University Marburg, Hans-Meerwein Strasse 4, Marburg 35032, Germany.
Lukas Korf
Department of Chemistry, Philipps University Marburg, Hans-Meerwein Strasse 4, Marburg 35032, Germany.
Viktoria Reithofer
Department of Chemistry, Philipps University Marburg, Hans-Meerwein Strasse 4, Marburg 35032, Germany.
Christian Joshua Rosner
  • Fonction : Auteur
Department of Chemistry, Philipps University Marburg, Hans-Meerwein Strasse 4, Marburg 35032, Germany.
Elisa Marie Seiler
Department of Chemistry, Philipps University Marburg, Hans-Meerwein Strasse 4, Marburg 35032, Germany.
Mohamed Watad
  • Fonction : Auteur
Department of Chemistry, Philipps University Marburg, Hans-Meerwein Strasse 4, Marburg 35032, Germany.
Laura Werel
  • Fonction : Auteur
Department of Chemistry, Philipps University Marburg, Hans-Meerwein Strasse 4, Marburg 35032, Germany.
Roberta Spadaccini
Department of Chemistry, Philipps University Marburg, Hans-Meerwein Strasse 4, Marburg 35032, Germany.
Dipartimento di Scienze e Tecnologie, Università degli Studi del Sannio, Benevento
Junpei Yamamoto
Department of Chemistry - Graduate School of Engineering Science, Osaka University
So Iwata
RIKEN RSC - RIKEN SPring-8 Center [Hyogo]
Dongping Zhong
OSU - Department of Physics [Ohio State University]
OSU - Department of Chemistry and Biochemistry [Ohio State University]
Shangaï Jiao Tong University [Shangaï]
Jörg Standfuss
PSI - Paul Scherrer Institute
Antoine Royant
ESRF - European Synchrotron Radiation Facility [Grenoble]
IBS - UMR 5075 - Institut de biologie structurale
Yoshitaka Bessho
IBC Sinica - Institute of Biological Chemistry [Tapei]
RIKEN RSC - RIKEN SPring-8 Center [Hyogo]
Lars-Oliver Essen
Department of Chemistry, Philipps University Marburg, Hans-Meerwein Strasse 4, Marburg 35032, Germany.
Ming-Daw Tsai
IBC Sinica - Institute of Biological Chemistry [Tapei]
Institute of Biochemical Sciences

Résumé

Photolyases, a ubiquitous class of flavoproteins, use blue light to repair DNA photolesions. In this work, we determined the structural mechanism of the photolyase-catalyzed repair of a cyclobutane pyrimidine dimer (CPD) lesion using time-resolved serial femtosecond crystallography (TR-SFX). We obtained 18 snapshots that show time-dependent changes in four reaction loci. We used these results to create a movie that depicts the repair of CPD lesions in the picosecond-to-nanosecond range, followed by the recovery of the enzymatic moieties involved in catalysis, completing the formation of the fully reduced enzyme-product complex at 500 nanoseconds. Finally, back-flip intermediates of the thymine bases to reanneal the DNA were captured at 25 to 200 microseconds. Our data cover the complete molecular mechanism of a photolyase and, importantly, its chemistry and enzymatic catalysis at work across a wide timescale and at atomic resolution.

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Soumis le : jeudi 10 octobre 2024-16:28:33

Dernière modification le : vendredi 3 avril 2026-16:40:05

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hal-04334937 , version 1 (10-10-2024)

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Manuel Maestre-Reyna, Po-Hsun Wang, Eriko Nango, Yuhei Hosokawa, Martin Saft, et al.. Visualizing the DNA repair process by a photolyase at atomic resolution. Science, 2023, 382 (6674), ⟨10.1126/science.add7795⟩. ⟨hal-04334937⟩

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