Unique roles of iron and zinc binding to the yeast Fe-S cluster scaffold assembly protein "Isu1".


Journal

Metallomics : integrated biometal science
ISSN: 1756-591X
Titre abrégé: Metallomics
Pays: England
ID NLM: 101478346

Informations de publication

Date de publication:
01 11 2019
Historique:
pubmed: 19 9 2019
medline: 20 6 2020
entrez: 19 9 2019
Statut: ppublish

Résumé

Mitochondrial Fe-S cluster biosynthesis is accomplished within yeast utilizing the biophysical attributes of the "Isu1" scaffold assembly protein. As a member of a highly homologous protein family, Isu1 has sequence conservation between orthologs and a conserved ability to assemble [2Fe-2S] clusters. Regardless of species, scaffold orthologs have been shown to exist in both "disordered" and "structured" conformations, a structural architecture that is directly related to conformations utilized during Fe-S cluster assembly. During assembly, the scaffold helps direct the delivery and utilization of Fe(ii) and persulfide substrates to produce [2Fe-2S] clusters, however Zn(ii) binding alters the activity of the scaffold while at the same time stabilizes the protein in its structured state. Additional studies confirm Zn binds to the scaffold's Cys rich active site, and has an impact on the protein's ability to make Fe-S clusters. Understanding the interplay between Fe(ii) and Zn(ii) binding to Isu1 in vitro may help clarify metal loading events that occur during Fe-S cluster assembly in vivo. Here we determine the metal : protein stoichiometry for Isu1 Zn and Fe binding to be 1 : 1 and 2 : 1, respectively. As expected, while Zn binding shifts the Isu1 to its structured state, folding is not influenced by Fe(ii) binding. X-ray absorption spectroscopy (XAS) confirms Zn(ii) binds to the scaffold's cysteine rich active site but Fe(ii) binds at a location distinct from the active site. XAS results show Isu1 binding initially of either Fe(ii) or Zn(ii) does not significantly perturb the metal site structure of alternate metal. XAS confirmed that four scaffold orthologs bind iron as high-spin Fe(ii) at a site composed of ca. 6 oxygen and nitrogen nearest neighbor ligands. Finally, in our report Zn binding dramatically reduces the Fe-S cluster assembly activity of Isu1 even in the presence of frataxin. Given the Fe-binding activity we report for Isu1 and its orthologs here, a possible mechanism involving Fe(ii) transport to the scaffold's active site during cluster assembly has been considered.

Identifiants

pubmed: 31532427
doi: 10.1039/c9mt00172g
pmc: PMC6854292
mid: NIHMS1051259
doi:

Substances chimiques

ISU1 protein, S cerevisiae 0
Iron-Sulfur Proteins 0
Mitochondrial Proteins 0
Saccharomyces cerevisiae Proteins 0
Iron E1UOL152H7
Zinc J41CSQ7QDS

Types de publication

Journal Article Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

1820-1835

Subventions

Organisme : NIBIB NIH HHS
ID : P30 EB009998
Pays : United States
Organisme : NIDDK NIH HHS
ID : R01 DK068139
Pays : United States
Organisme : NHLBI NIH HHS
ID : T32 HL120822
Pays : United States

Références

EMBO J. 2006 Jan 11;25(1):174-83
pubmed: 16341090
EMBO Rep. 2007 Feb;8(2):194-9
pubmed: 17186026
Nat Struct Mol Biol. 2009 Apr;16(4):390-6
pubmed: 19305405
PLoS Genet. 2015 May 21;11(5):e1005135
pubmed: 25996596
J Inorg Biochem. 2019 Oct 29;203:110882
pubmed: 31683123
Biochemistry. 2004 Dec 28;43(51):16254-62
pubmed: 15610019
Nat Commun. 2019 May 17;10(1):2210
pubmed: 31101807
Front Mol Biosci. 2018 Nov 19;5:97
pubmed: 30510932
Metallomics. 2017 Jan 25;9(1):48-60
pubmed: 27738674
Appl Environ Microbiol. 2019 Apr 18;85(9):null
pubmed: 30824435
J Biol Chem. 2017 Aug 4;292(31):12754-12763
pubmed: 28615445
Biochemistry. 2006 Jun 27;45(25):7767-77
pubmed: 16784228
Biometals. 2015 Jun;28(3):567-76
pubmed: 25782577
J Biol Chem. 2008 May 2;283(18):12674-9
pubmed: 18319250
Nat Protoc. 2010 Apr;5(4):725-38
pubmed: 20360767
EMBO Rep. 2003 Sep;4(9):906-11
pubmed: 12947415
Met Ions Life Sci. 2013;12:1-13
pubmed: 23595668
J Synchrotron Radiat. 2001 Mar 1;8(Pt 2):61-5
pubmed: 11512868
Methods Enzymol. 2004;383:318-51
pubmed: 15063656
Proc Natl Acad Sci U S A. 2016 Apr 26;113(17):4700-5
pubmed: 27071088
Nat Commun. 2019 Aug 8;10(1):3566
pubmed: 31395877
Biochemistry. 2010 Oct 12;49(40):8756-65
pubmed: 20815377
Nat Chem Biol. 2015 Sep;11(9):678-84
pubmed: 26192600
J Biol Chem. 2003 Aug 15;278(33):31340-51
pubmed: 12732649
Proteins. 2005 Jun 1;59(4):875-81
pubmed: 15815978
J Am Chem Soc. 2002 Jul 31;124(30):8774-5
pubmed: 12137512
Biochim Biophys Acta. 2015 Jun;1853(6):1251-2
pubmed: 25746719
Biochimie. 2018 Sep;152:211-218
pubmed: 30031876
J Mol Biol. 2004 Nov 19;344(2):567-83
pubmed: 15522305
J Mol Biol. 2004 Aug 6;341(2):605-15
pubmed: 15276847
Biochemistry. 2015 Jun 30;54(25):3871-9
pubmed: 26016389
Met Ions Life Sci. 2019 Jan 14;19:
pubmed: 30855105
Acc Chem Res. 2004 Sep;37(9):719-25
pubmed: 15379587
ACS Chem Biol. 2018 Mar 16;13(3):591-599
pubmed: 29210568
Proc Natl Acad Sci U S A. 2017 Jul 3;114(27):E5325-E5334
pubmed: 28634302
Biochemistry. 2010 Nov 2;49(43):9132-9
pubmed: 20873749
Acta Crystallogr B Struct Sci Cryst Eng Mater. 2016 Apr;72(Pt 2):171-9
pubmed: 27048719
J Biol Inorg Chem. 2008 Jun;13(5):825-36
pubmed: 18425540
PLoS One. 2011 Jan 26;6(1):e16199
pubmed: 21298097
J Mol Biol. 2008 Oct 31;383(1):133-43
pubmed: 18723024
Biochemistry. 2018 Feb 6;57(5):672-683
pubmed: 29228768
J Biol Chem. 2003 May 30;278(22):20225-34
pubmed: 12644454
Metallomics. 2018 Jan 24;10(1):9-29
pubmed: 29019354
Nat Commun. 2017 Nov 3;8(1):1287
pubmed: 29097656
Biochem Soc Trans. 2008 Dec;36(Pt 6):1112-9
pubmed: 19021507
Proc Natl Acad Sci U S A. 2010 Jun 29;107(26):11775-80
pubmed: 20547883
Protein Sci. 2018 Jan;27(1):135-145
pubmed: 28884485
Biochemistry. 2001 Jul 10;40(27):8138-45
pubmed: 11434783
Biol Trace Elem Res. 2007 Nov;119(2):166-74
pubmed: 17916939
Methods Enzymol. 2018;599:265-292
pubmed: 29746243
Mol Cell Biol. 2004 Jun;24(11):4848-57
pubmed: 15143178
Biochemistry. 2014 Aug 5;53(30):4904-13
pubmed: 24971490
Biochemistry. 2012 Jul 17;51(28):5557-63
pubmed: 22734684
J Biol Chem. 2007 Aug 31;282(35):25950-9
pubmed: 17609202
Arch Biochem Biophys. 2016 Feb 15;592:60-75
pubmed: 26785297
Biochemistry. 2015 Jun 9;54(22):3442-53
pubmed: 26018429
EMBO J. 2006 Jan 11;25(1):184-95
pubmed: 16341089
Protein Sci. 2014 Sep;23(9):1208-19
pubmed: 24917298
Anal Biochem. 1996 Jun 1;237(2):260-73
pubmed: 8660575
Chembiochem. 2014 Jul 21;15(11):1682-6
pubmed: 25044349
FEBS Lett. 2004 Jan 16;557(1-3):215-20
pubmed: 14741370
Curr Protoc Bioinformatics. 2015 Dec 17;52:5.8.1-15
pubmed: 26678386
Science. 1997 Jun 13;276(5319):1709-12
pubmed: 9180083
Biochemistry. 2010 May 18;49(19):4227-34
pubmed: 20408527
J Biol Chem. 2013 Dec 27;288(52):36773-86
pubmed: 24217246
Biochemistry. 2009 Jul 7;48(26):6062-71
pubmed: 19492851
Biochemistry. 2018 Mar 6;57(9):1491-1500
pubmed: 29406711
Elife. 2016 Aug 19;5:
pubmed: 27540631
FEBS Lett. 2013 Apr 17;587(8):1172-9
pubmed: 23333622

Auteurs

Brianne E Lewis (BE)

Department of Pharmaceutical Science, Wayne State University, Detroit, MI 48201, USA. timothy.stemmler@wayne.edu.

Zachary Mason (Z)

Department of Pharmaceutical Science, Wayne State University, Detroit, MI 48201, USA. timothy.stemmler@wayne.edu.

Andria V Rodrigues (AV)

Department of Pharmaceutical Science, Wayne State University, Detroit, MI 48201, USA. timothy.stemmler@wayne.edu.

Manunya Nuth (M)

Department of Chemistry, The Ohio State University, Columbus, OH 43210, USA.

Eric Dizin (E)

Department of Chemistry, The Ohio State University, Columbus, OH 43210, USA.

J A Cowan (JA)

Department of Chemistry, The Ohio State University, Columbus, OH 43210, USA.

Timothy L Stemmler (TL)

Department of Pharmaceutical Science, Wayne State University, Detroit, MI 48201, USA. timothy.stemmler@wayne.edu.

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Classifications MeSH