Redox activation of ATM enhances GSNOR translation to sustain mitophagy and tolerance to oxidative stress.


Journal

EMBO reports
ISSN: 1469-3178
Titre abrégé: EMBO Rep
Pays: England
ID NLM: 100963049

Informations de publication

Date de publication:
07 01 2021
Historique:
received: 24 03 2020
revised: 01 10 2020
accepted: 14 10 2020
pubmed: 28 11 2020
medline: 1 6 2021
entrez: 27 11 2020
Statut: ppublish

Résumé

The denitrosylase S-nitrosoglutathione reductase (GSNOR) has been suggested to sustain mitochondrial removal by autophagy (mitophagy), functionally linking S-nitrosylation to cell senescence and aging. In this study, we provide evidence that GSNOR is induced at the translational level in response to hydrogen peroxide and mitochondrial ROS. The use of selective pharmacological inhibitors and siRNA demonstrates that GSNOR induction is an event downstream of the redox-mediated activation of ATM, which in turn phosphorylates and activates CHK2 and p53 as intermediate players of this signaling cascade. The modulation of ATM/GSNOR axis, or the expression of a redox-insensitive ATM mutant influences cell sensitivity to nitrosative and oxidative stress, impairs mitophagy and affects cell survival. Remarkably, this interplay modulates T-cell activation, supporting the conclusion that GSNOR is a key molecular effector of the antioxidant function of ATM and providing new clues to comprehend the pleiotropic effects of ATM in the context of immune function.

Identifiants

pubmed: 33245190
doi: 10.15252/embr.202050500
pmc: PMC7788447
doi:

Substances chimiques

Aldehyde Oxidoreductases EC 1.2.-

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e50500

Subventions

Organisme : NHLBI NIH HHS
ID : P01 HL128192
Pays : United States

Informations de copyright

© 2020 The Authors. Published under the terms of the CC BY 4.0 license.

Références

Nat Cell Biol. 2015 Oct;17(10):1259-1269
pubmed: 26344566
J Immunol. 2010 Dec 1;185(11):6664-9
pubmed: 20980633
J Immunol. 2012 Nov 1;189(9):4405-16
pubmed: 23024271
Autophagy. 2018;14(8):1435-1455
pubmed: 29940786
Philos Trans R Soc Lond B Biol Sci. 1985 Dec 17;311(1152):617-31
pubmed: 2869521
Nat Methods. 2009 Apr;6(4):275-7
pubmed: 19305406
Sci Signal. 2018 Jul 10;11(538):
pubmed: 29991649
Cell Cycle. 2015;14(12):1908-24
pubmed: 25970706
Cytometry A. 2011 Aug;79(8):646-52
pubmed: 21695774
Science. 2016 Jan 29;351(6272):aad3867
pubmed: 26823435
FASEB J. 2001 May;15(7):1132-8
pubmed: 11344081
Antioxid Redox Signal. 2014 Aug 1;21(4):570-87
pubmed: 24684653
Autophagy. 2018;14(7):1285-1287
pubmed: 30029585
Trends Biochem Sci. 2012 Jan;37(1):15-22
pubmed: 22079189
J Clin Invest. 2004 Jun;113(12):1734-42
pubmed: 15199408
Science. 2010 Oct 22;330(6003):517-21
pubmed: 20966255
Mol Cell. 2010 Oct 22;40(2):228-37
pubmed: 20965418
Biochem Pharmacol. 2020 Jun;176:113885
pubmed: 32112881
Arch Biochem Biophys. 2001 Feb 15;386(2):163-71
pubmed: 11368338
Annu Rev Biochem. 2017 Jun 20;86:715-748
pubmed: 28441057
Mech Ageing Dev. 1991 Feb;57(2):187-202
pubmed: 1904965
Environ Mol Mutagen. 1994;24(2):103-11
pubmed: 7925323
Proc Natl Acad Sci U S A. 2018 Apr 10;115(15):E3388-E3397
pubmed: 29581312
J Vis Exp. 2014 May 17;(87):
pubmed: 24893926
J Biol Chem. 1999 Nov 26;274(48):34277-82
pubmed: 10567403
Nat Immunol. 2004 Aug;5(8):818-27
pubmed: 15258578
Sci Rep. 2017 Mar 03;7:43598
pubmed: 28256581
J Immunol. 2010 May 1;184(9):4827-41
pubmed: 20335530
Nature. 2001 Mar 22;410(6827):490-4
pubmed: 11260719
Proc Natl Acad Sci U S A. 2013 Jun 25;110(26):10592-7
pubmed: 23754435
J Biochem. 2014 Aug;156(2):85-95
pubmed: 24682951
Blood. 2012 Feb 9;119(6):1490-500
pubmed: 22144182
Nucleic Acids Res. 2018 Jan 9;46(1):e3
pubmed: 29069469
Trends Immunol. 2015 Mar;36(3):161-78
pubmed: 25687683
Cancer Lett. 1990 Oct 8;54(1-2):43-50
pubmed: 2208088
Nat Methods. 2012 Jun 28;9(7):676-82
pubmed: 22743772
Cancers (Basel). 2018 May 21;10(5):
pubmed: 29883412
Sci Signal. 2018 Jan 09;11(512):
pubmed: 29317520
Biochim Biophys Acta. 1996 Mar 18;1242(3):181-4
pubmed: 8603071
J Biomed Sci. 2015 Oct 15;22:85
pubmed: 26471060
J Pediatr. 2004 Apr;144(4):505-11
pubmed: 15069401
DNA Repair (Amst). 2002 Jan 22;1(1):3-25
pubmed: 12509294
J Immunol. 1998 Dec 15;161(12):6526-31
pubmed: 9862677
Biochim Biophys Acta. 2012 Dec;1823(12):2297-310
pubmed: 22917578
Proc Natl Acad Sci U S A. 2016 Nov 15;113(46):13063-13068
pubmed: 27799543
Cell Death Differ. 2014 Oct;21(10):1522-34
pubmed: 24926617
Redox Biol. 2020 May;32:101511
pubmed: 32244177
Cell. 2005 Feb 25;120(4):483-95
pubmed: 15734681
Cell. 2004 Feb 20;116(4):617-28
pubmed: 14980227
Ann Neurol. 2001 May;49(5):627-35
pubmed: 11357953
Cancer Res. 1987 Sep 1;47(17):4576-81
pubmed: 3621155
Ann Rheum Dis. 2006 Nov;65 Suppl 3:iii37-40
pubmed: 17038470
Free Radic Biol Med. 2012 Feb 1;52(3):539-555
pubmed: 22080087
Nat Immunol. 2014 Mar;15(3):275-82
pubmed: 24441790
J Clin Invest. 2007 Sep;117(9):2723-34
pubmed: 17786248
Cancer Res. 2001 Mar 1;61(5):1849-54
pubmed: 11280737
EMBO J. 2020 May 18;39(10):e103111
pubmed: 32187724
Genome Res. 2017 Oct;27(10):1645-1657
pubmed: 28904012
J Biol Chem. 2003 Apr 25;278(17):14806-11
pubmed: 12588868
J Biol Chem. 1951 Nov;193(1):265-75
pubmed: 14907713
Nucleic Acids Res. 2010 Jan;38(3):778-88
pubmed: 19934254
Free Radic Biol Med. 1995 Jan;18(1):125-6
pubmed: 7896166
Free Radic Biol Med. 2017 Sep;110:19-30
pubmed: 28533171
Mediators Inflamm. 2015;2015:536238
pubmed: 26491229

Auteurs

Claudia Cirotti (C)

Department of Biology, Tor Vergata University, Rome, Italy.
Laboratory of Cell Signaling, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) Fondazione Santa Lucia, Rome, Italy.

Salvatore Rizza (S)

Redox Signaling and Oxidative Stress Group, Danish Cancer Society Research Center, Copenhagen, Denmark.

Paola Giglio (P)

Department of Biology, Tor Vergata University, Rome, Italy.

Noemi Poerio (N)

Department of Biology, Tor Vergata University, Rome, Italy.

Maria Francesca Allega (MF)

Redox Signaling and Oxidative Stress Group, Danish Cancer Society Research Center, Copenhagen, Denmark.

Giuseppina Claps (G)

INSERM, U981, Villejuif, France.

Chiara Pecorari (C)

Redox Signaling and Oxidative Stress Group, Danish Cancer Society Research Center, Copenhagen, Denmark.

Ji-Hoon Lee (JH)

Department of Molecular Biosciences, The University of Texas at Austin, Austin, TX, USA.

Barbara Benassi (B)

Division of Health Protection Technologies, ENEA-Casaccia, Rome, Italy.

Daniela Barilà (D)

Department of Biology, Tor Vergata University, Rome, Italy.
Laboratory of Cell Signaling, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) Fondazione Santa Lucia, Rome, Italy.

Caroline Robert (C)

INSERM, U981, Villejuif, France.
Université Paris Sud, Université Paris-Saclay, Kremlin-Bicêtre, France.
Oncology Department, Gustave Roussy, Université Paris-Saclay, Villejuif, France.

Jonathan S Stamler (JS)

Institute for Transformative Molecular Medicine, Case Western Reserve University and Harrington Discovery Institute, University Hospitals Case Medical Center, Cleveland, OH, USA.

Francesco Cecconi (F)

Department of Biology, Tor Vergata University, Rome, Italy.
Cell Stress and Survival Unit, Danish Cancer Society Research Center, Copenhagen, Denmark.
Department of Pediatric Hematology and Oncology, IRCCS Bambino Gesù Children's Hospital, Rome, Italy.

Maurizio Fraziano (M)

Department of Biology, Tor Vergata University, Rome, Italy.

Tanya T Paull (TT)

Department of Molecular Biosciences, The University of Texas at Austin, Austin, TX, USA.

Giuseppe Filomeni (G)

Department of Biology, Tor Vergata University, Rome, Italy.
Redox Signaling and Oxidative Stress Group, Danish Cancer Society Research Center, Copenhagen, Denmark.
Center for Healthy Aging, Copenhagen University, Copenhagen, Denmark.

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Classifications MeSH