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The Yeast Iron Regulatory Proteins Grx3/4 and Fra2 Form Heterodimeric Complexes Containing a [2Fe-2S] Cluster with Cysteinyl and Histidyl Ligation

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‡ Department of Chemistry and Biochemistry, University of South Carolina, Columbia, South Carolina 29208
§ Department of Chemistry and Center for Metalloenzyme Studies, University of Georgia, Athens, Georgia 30602
∥ Department of Physics, Emory University, Atlanta, Georgia 30322
⊥ Chemistry Department, Northwestern University, Evanston, Illinois 60208
# Department of Chemistry and Biochemistry, College of Charleston, Charleston, South Carolina 29424
*To whom correspondence should be addressed. C.E.O.: e-mail, [email protected]; tel, 803-777-8783; fax, 803-777-9521. M.K.J.: e-mail, [email protected]; tel, 706-542-9378; fax, 706-542-9454.
Cite this: Biochemistry 2009, 48, 40, 9569–9581
Publication Date (Web):August 28, 2009
https://doi.org/10.1021/bi901182w
Copyright © 2009 American Chemical Society
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    Abstract

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    The transcription of iron uptake and storage genes in Saccharomyces cerevisiae is primarily regulated by the transcription factor Aft1. Nucleocytoplasmic shuttling of Aft1 is dependent upon mitochondrial Fe-S cluster biosynthesis via a signaling pathway that includes the cytosolic monothiol glutaredoxins (Grx3 and Grx4) and the BolA homologue Fra2. However, the interactions between these proteins and the iron-dependent mechanism by which they control Aft1 localization are unclear. To reconstitute and characterize components of this signaling pathway in vitro, we have overexpressed yeast Fra2 and Grx3/4 in Escherichia coli. We have shown that coexpression of recombinant Fra2 with Grx3 or Grx4 allows purification of a stable [2Fe-2S]2+ cluster-containing Fra2-Grx3 or Fra2-Grx4 heterodimeric complex. Reconstitution of a [2Fe-2S] cluster on Grx3 or Grx4 without Fra2 produces a [2Fe-2S]-bridged homodimer. UV−visible absorption and CD, resonance Raman, EPR, ENDOR, Mössbauer, and EXAFS studies of [2Fe-2S] Grx3/4 homodimers and the [2Fe-2S] Fra2-Grx3/4 heterodimers indicate that inclusion of Fra2 in the Grx3/4 Fe-S complex causes a change in the cluster stability and coordination environment. Taken together, our analytical, spectroscopic, and mutagenesis data indicate that Grx3/4 and Fra2 form a Fe-S-bridged heterodimeric complex with Fe ligands provided by the active site cysteine of Grx3/4, glutathione, and a histidine residue. Overall, these results suggest that the ability of the Fra2-Grx3/4 complex to assemble a [2Fe-2S] cluster may act as a signal to control the iron regulon in response to cellular iron status in yeast.

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    One table showing the primers used for cloning and mutagenesis and two figures providing additional XAS data. This material is available free of charge via the Internet at http://pubs.acs.org.

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