Reverse gyrase has heat-protective DNA chaperone activity independent of supercoiling

Nucleic Acids Research
Martin Kampmann, Daniela Stock

Abstract

Hyperthermophilic organisms must protect their constituent macromolecules from heat-induced degradation. A general mechanism for thermoprotection of DNA in active cells is unknown. We show that reverse gyrase, the only protein that is both specific and common to all hyperthermophiles, reduces the rate of double-stranded DNA breakage approximately 8-fold at 90 degrees C. This activity does not require ATP hydrolysis and is independent of the positive supercoiling activity of the enzyme. Reverse gyrase has a minor nonspecific effect on the rate of depurination, and a major specific effect on the rate of double-strand breakage. Using electron microscopy, we show that reverse gyrase recognizes nicked DNA and recruits a protein coat to the site of damage through cooperative binding. Analogously to molecular chaperones that assist unfolded proteins, we found that reverse gyrase prevents inappropriate aggregation of denatured DNA regions and promotes correct annealing. We propose a model for a targeted protection mechanism in vivo in which reverse gyrase detects damaged DNA and acts as a molecular splint to prevent DNA breakage in the vicinity of the lesion, thus maintaining damaged DNA in a conformation that is amenable to repair.

References

Sep 1, 1990·Mutation Research·P W Doetsch, R P Cunningham
Sep 9, 1982·Nature·A Stasiak, E Di Capua
May 11, 1994·Nucleic Acids Research·E Marguet, P Forterre
Sep 26, 1997·The Journal of Biological Chemistry·G Chu
May 1, 1998·FEBS Letters·C C Wang, C L Tsou
Jul 29, 1998·Molecular Microbiology·D W Grogan
Dec 23, 1998·Proceedings of the National Academy of Sciences of the United States of America·S D BellS P Jackson
Jun 22, 1999·FEBS Letters·K O Stetter
Oct 16, 1999·Proceedings of the National Academy of Sciences of the United States of America·M MachiusJ Deisenhofer
Apr 15, 2000·Cellular and Molecular Life Sciences : CMLS·R M Daniel, D A Cowan
Sep 1, 2000·Frontiers in Bioscience : a Journal and Virtual Library·S V AlbersW N Konings
Nov 1, 2001·The Journal of Biological Chemistry·Milan SkorvagaBennett Van Houten
Feb 2, 2002·The EMBO Journal·A Chapin Rodríguez, Daniela Stock
Oct 3, 2002·Biochemical and Biophysical Research Communications·Kyoko MatobaKosuke Morikawa
Sep 1, 1954·The Journal of Histochemistry and Cytochemistry : Official Journal of the Histochemistry Society·M R McDONALD, B P KAUFMANN

❮ Previous
Next ❯

Citations

Feb 15, 2011·Extremophiles : Life Under Extreme Conditions·Jie LiHua Xiang
Jun 27, 2009·The Journal of Microbiology·Michelle Heine, Sathees B C Chandra
Aug 30, 2008·Quarterly Reviews of Biophysics·Allyn J Schoeffler, James M Berger
Feb 26, 2011·Physical Chemistry Chemical Physics : PCCP·Yoandris del Toro Duany, Dagmar Klostermeier
Sep 21, 2010·The Journal of Biological Chemistry·Anna ValentiMaria Ciaramella
Oct 12, 2010·The Journal of Biological Chemistry·Christopher CappTao-Shih Hsieh
Sep 4, 2009·The Journal of Biological Chemistry·Jody Plank, Tao-shih Hsieh
Jan 28, 2005·Nucleic Acids Research·Alessandra NapoliMaria Ciaramella
Sep 18, 2008·Nucleic Acids Research·Yoandris del Toro DuanyDagmar Klostermeier
May 29, 2013·Extremophiles : Life Under Extreme Conditions·Marleen van WolferenSonja-Verena Albers
Aug 12, 2014·Extremophiles : Life Under Extreme Conditions·Antonella VettoneMaria Ciaramella
Sep 27, 2014·International Journal of Molecular Sciences·Valeria VisoneMaria Ciaramella
Mar 26, 2011·Journal of Molecular Biology·Anna BizardMarc Nadal
Jun 15, 2007·Journal of Molecular Biology·Stefan P Jungblut, Dagmar Klostermeier
Dec 5, 2006·Biochimie·Thierry Viard, Claire Bouthier de la Tour
Nov 30, 2005·Molecular Microbiology·Paras Jain, Valakunja Nagaraja
Feb 1, 2005·Trends in Microbiology·Maria CiaramellaMosè Rossi
Nov 14, 2012·Current Opinion in Biotechnology·Anna LewinSvein Valla
Nov 6, 2012·Journal of Molecular Biology·Agneyo GangulyDagmar Klostermeier
Jul 12, 2014·Nucleic Acids Research·Pavel Lulchev, Dagmar Klostermeier
Jun 24, 2017·International Journal of Molecular Sciences·Wenyuan HanQunxin She
Mar 25, 2005·The Journal of Biological Chemistry·Tao-shih Hsieh, Christopher Capp
Jul 11, 2008·The Journal of Biological Chemistry·Claire Bouthier de la TourMichel Duguet
Jan 16, 2009·Biochemical Society Transactions·Giuseppe PeruginoMaria Ciaramella
Nov 24, 2018·Extremophiles : Life Under Extreme Conditions·A GorlasP Forterre
May 7, 2020·Proceedings of the National Academy of Sciences of the United States of America·Xi YangMarc Nadal
Jun 28, 2020·Journal of Molecular Biology·Frederic CollinDagmar Klostermeier
Jun 12, 2021·Frontiers in Microbiology·Florence GarnierMarc Nadal

❮ Previous
Next ❯

Related Concepts

Related Feeds

Researcher Network:CZI Neurodegeneration Challenge

The Neurodegeneration Challenge Network aims to provide funding for and to bring together researchers studying neurodegenerative diseases. Find the latest research from the NDCN grantees here.

BioHub - Researcher Network

The Chan-Zuckerberg Biohub aims to support the fundamental research and develop the technologies that will enable physicians to cure, prevent, or manage all diseases in our childrens' lifetimes. The CZ Biohub brings together researchers from UC Berkeley, Stanford, and UCSF. Find the latest research from the CZ Biohub researcher network here.