Physiologically relevant reconstitution of iron-sulfur cluster biosynthesis uncovers persulfide-processing functions of ferredoxin-2 and frataxin.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
08 08 2019
Historique:
received: 14 02 2019
accepted: 04 07 2019
entrez: 10 8 2019
pubmed: 10 8 2019
medline: 8 1 2020
Statut: epublish

Résumé

Iron-sulfur (Fe-S) clusters are essential protein cofactors whose biosynthetic defects lead to severe diseases among which is Friedreich's ataxia caused by impaired expression of frataxin (FXN). Fe-S clusters are biosynthesized on the scaffold protein ISCU, with cysteine desulfurase NFS1 providing sulfur as persulfide and ferredoxin FDX2 supplying electrons, in a process stimulated by FXN but not clearly understood. Here, we report the breakdown of this process, made possible by removing a zinc ion in ISCU that hinders iron insertion and promotes non-physiological Fe-S cluster synthesis from free sulfide in vitro. By binding zinc-free ISCU, iron drives persulfide uptake from NFS1 and allows persulfide reduction into sulfide by FDX2, thereby coordinating sulfide production with its availability to generate Fe-S clusters. FXN stimulates the whole process by accelerating persulfide transfer. We propose that this reconstitution recapitulates physiological conditions which provides a model for Fe-S cluster biosynthesis, clarifies the roles of FDX2 and FXN and may help develop Friedreich's ataxia therapies.

Identifiants

pubmed: 31395877
doi: 10.1038/s41467-019-11470-9
pii: 10.1038/s41467-019-11470-9
pmc: PMC6687725
doi:

Substances chimiques

FDX2 protein, human 0
Ferredoxins 0
ISCU protein, human 0
Iron-Binding Proteins 0
Iron-Sulfur Proteins 0
IscU protein, mouse 0
Recombinant Proteins 0
Sulfides 0
persulfides 0
Iron E1UOL152H7
Carbon-Sulfur Lyases EC 4.4.-
NFS1 protein, human EC 4.4.1.-
Nfs1 protein, mouse EC 4.4.1.-
Zinc J41CSQ7QDS

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

3566

Références

Biochim Biophys Acta. 2010 Jun;1802(6):531-8
pubmed: 20307653
J Am Chem Soc. 2012 Dec 5;134(48):19746-57
pubmed: 23167247
Front Pharmacol. 2014 Jun 03;5:130
pubmed: 24917819
Biochemistry. 2007 Jun 12;46(23):6804-11
pubmed: 17506525
J Mol Biol. 2004 Nov 19;344(2):567-83
pubmed: 15522305
J Am Chem Soc. 2001 Nov 7;123(44):11103-4
pubmed: 11686732
J Am Chem Soc. 2014 Sep 3;136(35):12337-44
pubmed: 25082811
Biochemistry. 2009 Jul 7;48(26):6062-71
pubmed: 19492851
J Am Chem Soc. 2013 Jan 16;135(2):733-40
pubmed: 23265191
Angew Chem Int Ed Engl. 2012 May 29;51(22):5439-42
pubmed: 22511353
Biochemistry. 2014 Jan 14;53(1):152-60
pubmed: 24321018
Nat Struct Mol Biol. 2009 Apr;16(4):390-6
pubmed: 19305405
Mol Microbiol. 2015 Feb;95(4):605-23
pubmed: 25430730
Metallomics. 2017 Jan 25;9(1):48-60
pubmed: 27738674
J Biol Chem. 2017 Aug 4;292(31):12754-12763
pubmed: 28615445
Nat Commun. 2014 Oct 31;5:5013
pubmed: 25358379
J Biol Chem. 2008 Jan 11;283(2):908-18
pubmed: 18003617
Biometals. 2015 Jun;28(3):567-76
pubmed: 25782577
Biochim Biophys Acta. 2015 Jun;1853(6):1253-71
pubmed: 25655665
J Natl Cancer Inst. 2016 Jan;108(1):
pubmed: 26719882
Nat Commun. 2017 Jan 04;8:13932
pubmed: 28051091
Proteins. 2005 Jun 1;59(4):875-81
pubmed: 15815978
Eur J Biochem. 2004 Jun;271(11):2093-100
pubmed: 15153099
J Am Chem Soc. 2002 Jul 31;124(30):8774-5
pubmed: 12137512
Biochim Biophys Acta. 2013 Mar;1827(3):455-69
pubmed: 23298813
Biochem J. 2014 Apr 1;459(1):71-81
pubmed: 24433162
Nat Commun. 2015 Jan 19;6:5686
pubmed: 25597503
Biochimie. 2018 Sep;152:211-218
pubmed: 30031876
Biochemistry. 2015 Jun 30;54(25):3871-9
pubmed: 26016389
Proc Natl Acad Sci U S A. 2017 Jul 3;114(27):E5325-E5334
pubmed: 28634302
FASEB J. 2013 Mar;27(3):1074-83
pubmed: 23193175
Biochemistry. 2010 Nov 2;49(43):9132-9
pubmed: 20873749
Nature. 2017 Nov 30;551(7682):639-643
pubmed: 29168506
PLoS One. 2011;6(7):e21992
pubmed: 21799759
J Biol Inorg Chem. 2018 Jun;23(4):545-566
pubmed: 29349662
J Mol Biol. 2008 Oct 31;383(1):133-43
pubmed: 18723024
J Biol Chem. 2017 Aug 4;292(31):12744-12753
pubmed: 28615439
Nat Commun. 2017 Nov 3;8(1):1287
pubmed: 29097656
Proc Natl Acad Sci U S A. 2010 Jun 29;107(26):11775-80
pubmed: 20547883
J Biol Chem. 2011 Dec 2;286(48):41205-16
pubmed: 21987576
Nat Commun. 2017 May 11;8:15124
pubmed: 28492233
Biochemistry. 2011 Nov 8;50(44):9641-50
pubmed: 21977977
J Biol Chem. 2001 Nov 30;276(48):44521-6
pubmed: 11577100
Biometals. 2009 Dec;22(6):1051-61
pubmed: 19649569
Metallomics. 2018 Jan 24;10(1):49-72
pubmed: 29219157
Biochemistry. 2014 Aug 5;53(30):4904-13
pubmed: 24971490
J Neurochem. 2013 Aug;126 Suppl 1:43-52
pubmed: 23859340
Protein Sci. 2014 Sep;23(9):1208-19
pubmed: 24917298
J Biol Inorg Chem. 2018 Jun;23(4):509-520
pubmed: 29511832
Science. 2013 Jun 28;340(6140):1583-7
pubmed: 23812717
Proc Natl Acad Sci U S A. 2000 Feb 1;97(3):1050-5
pubmed: 10655482
Biochemistry. 2000 Jul 11;39(27):7856-62
pubmed: 10891064
J Biol Chem. 2013 Dec 27;288(52):36773-86
pubmed: 24217246
EMBO Rep. 2004 Nov;5(11):1096-101
pubmed: 15472712
Biochimie. 2014 May;100:61-77
pubmed: 24462711

Auteurs

Sylvain Gervason (S)

Institute for Integrative Biology of the Cell (I2BC), CEA, CNRS, Univ. Paris-Sud, Université Paris-Saclay, 91198, Gif-sur-Yvette cedex, France.

Djabir Larkem (D)

Institute for Integrative Biology of the Cell (I2BC), CEA, CNRS, Univ. Paris-Sud, Université Paris-Saclay, 91198, Gif-sur-Yvette cedex, France.

Amir Ben Mansour (AB)

Institute for Integrative Biology of the Cell (I2BC), CEA, CNRS, Univ. Paris-Sud, Université Paris-Saclay, 91198, Gif-sur-Yvette cedex, France.

Thomas Botzanowski (T)

Laboratoire de Spectrométrie de Masse BioOrganique, Université de Strasbourg, CNRS, IPHC UMR 7178, 67000, Strasbourg, France.

Christina S Müller (CS)

Fachbreich Physik, Technische Universität Kaiserslautern, Erwin-Schrödinger-Str. 56, 67663, Kaiserslautern, Germany.

Ludovic Pecqueur (L)

Laboratoire de Chimie des Processus Biologiques, Collège de France, Sorbonne Université, CNRS UMR 8229, PSL Research University, 11 place Marcelin Berthelot, 75005, Paris, France.

Gwenaelle Le Pavec (G)

Institute for Integrative Biology of the Cell (I2BC), CEA, CNRS, Univ. Paris-Sud, Université Paris-Saclay, 91198, Gif-sur-Yvette cedex, France.

Agnès Delaunay-Moisan (A)

Institute for Integrative Biology of the Cell (I2BC), CEA, CNRS, Univ. Paris-Sud, Université Paris-Saclay, 91198, Gif-sur-Yvette cedex, France.

Omar Brun (O)

Departament de Química Orgànica i IBUB, Facultat de Química, Universitat de Barcelona, Martí i Franquès 1-11, E-08028, Barcelona, Spain.

Jordi Agramunt (J)

Departament de Química Orgànica i IBUB, Facultat de Química, Universitat de Barcelona, Martí i Franquès 1-11, E-08028, Barcelona, Spain.

Anna Grandas (A)

Departament de Química Orgànica i IBUB, Facultat de Química, Universitat de Barcelona, Martí i Franquès 1-11, E-08028, Barcelona, Spain.

Marc Fontecave (M)

Laboratoire de Chimie des Processus Biologiques, Collège de France, Sorbonne Université, CNRS UMR 8229, PSL Research University, 11 place Marcelin Berthelot, 75005, Paris, France.

Volker Schünemann (V)

Fachbreich Physik, Technische Universität Kaiserslautern, Erwin-Schrödinger-Str. 56, 67663, Kaiserslautern, Germany.

Sarah Cianférani (S)

Laboratoire de Spectrométrie de Masse BioOrganique, Université de Strasbourg, CNRS, IPHC UMR 7178, 67000, Strasbourg, France.

Christina Sizun (C)

Institut de Chimie des Substances Naturelles, CNRS, Université Paris Saclay, 91190, Gif-sur-Yvette, France.

Michel B Tolédano (MB)

Institute for Integrative Biology of the Cell (I2BC), CEA, CNRS, Univ. Paris-Sud, Université Paris-Saclay, 91198, Gif-sur-Yvette cedex, France.

Benoit D'Autréaux (B)

Institute for Integrative Biology of the Cell (I2BC), CEA, CNRS, Univ. Paris-Sud, Université Paris-Saclay, 91198, Gif-sur-Yvette cedex, France. benoit.dautreaux@i2bc.paris-saclay.fr.

Articles similaires

Psoriasis Humans Magnesium Zinc Trace Elements

A molecular mechanism for bright color variation in parrots.

Roberto Arbore, Soraia Barbosa, Jindich Brejcha et al.
1.00
Animals Feathers Pigmentation Parrots Aldehyde Dehydrogenase
Osteosarcoma Animals Glutathione Oxidation-Reduction Mice

Classifications MeSH