Bacterial ApbC Protein Has Two Biochemical Activities That Are Required for in Vivo Function

Overview

Journal J Biol Chem

Specialty Biochemistry

Date 2008 Nov 13

PMID 19001370

Citations 18

Authors

Jeffrey M Boyd

Jamie L Sondelski

Diana M Downs

Affiliations

Soon will be listed here.

Abstract

The ApbC protein has been shown previously to bind and rapidly transfer iron-sulfur ([Fe-S]) clusters to an apoprotein (Boyd, J. M., Pierik, A. J., Netz, D. J., Lill, R., and Downs, D. M. (2008) Biochemistry 47, 8195-8202. This study utilized both in vivo and in vitro assays to examine the function of variant ApbC proteins. The in vivo assays assessed the ability of ApbC proteins to function in pathways with low and high demand for [Fe-S] cluster proteins. Variant ApbC proteins were purified and assayed for the ability to hydrolyze ATP, bind [Fe-S] cluster, and transfer [Fe-S] cluster. This study details the first kinetic analysis of ATP hydrolysis for a member of the ParA subfamily of "deviant" Walker A proteins. Moreover, this study details the first functional analysis of mutant variants of the ever expanding family of ApbC/Nbp35 [Fe-S] cluster biosynthetic proteins. The results herein show that ApbC protein needs ATPase activity and the ability to bind and rapidly transfer [Fe-S] clusters for in vivo function.

Citing Articles

A-Type Carrier Proteins Are Involved in [4Fe-4S] Cluster Insertion into the Radical -Adenosylmethionine Protein MoaA for the Synthesis of Active Molybdoenzymes.

Hasnat M, Zupok A, Olas J, Mueller-Roeber B, Leimkuhler S J Bacteriol. 2021; 203(12):e0008621.

PMID: 33782054 PMC: 8316096. DOI: 10.1128/JB.00086-21.

Iron-Sulfur Cluster Biogenesis and Iron Homeostasis in Cyanobacteria.

Gao F Front Microbiol. 2020; 11:165.

PMID: 32184761 PMC: 7058544. DOI: 10.3389/fmicb.2020.00165.

The bacterial Mrp is a novel Mrp/NBP35 protein involved in iron-sulfur biogenesis.

Pardoux R, Fievet A, Carreira C, Brochier-Armanet C, Valette O, Dermoun Z Sci Rep. 2019; 9(1):712.

PMID: 30679587 PMC: 6345978. DOI: 10.1038/s41598-018-37021-8.

Rv1460, a SufR homologue, is a repressor of the suf operon in Mycobacterium tuberculosis.

Willemse D, Weber B, Masino L, Warren R, Adinolfi S, Pastore A PLoS One. 2018; 13(7):e0200145.

PMID: 29979728 PMC: 6034842. DOI: 10.1371/journal.pone.0200145.

A Small-Molecule Inhibitor of Iron-Sulfur Cluster Assembly Uncovers a Link between Virulence Regulation and Metabolism in Staphylococcus aureus.

Choby J, Mike L, Mashruwala A, Dutter B, Dunman P, Sulikowski G Cell Chem Biol. 2016; 23(11):1351-1361.

PMID: 27773628 PMC: 5117899. DOI: 10.1016/j.chembiol.2016.09.012.

References

Skovran E, Downs D . Lack of the ApbC or ApbE protein results in a defect in Fe-S cluster metabolism in Salmonella enterica serovar Typhimurium. J Bacteriol. 2002; 185(1):98-106. PMC: 141979. DOI: 10.1128/JB.185.1.98-106.2003. View

Lezhneva L, Amann K, Meurer J . The universally conserved HCF101 protein is involved in assembly of [4Fe-4S]-cluster-containing complexes in Arabidopsis thaliana chloroplasts. Plant J. 2003; 37(2):174-85. DOI: 10.1046/j.1365-313x.2003.01952.x. View

Lewis J, Escalante-Semerena J . The FAD-dependent tricarballylate dehydrogenase (TcuA) enzyme of Salmonella enterica converts tricarballylate into cis-aconitate. J Bacteriol. 2006; 188(15):5479-86. PMC: 1540016. DOI: 10.1128/JB.00514-06. View

Zhou H, Schulze R, Cox S, Saez C, Hu Z, Lutkenhaus J . Analysis of MinD mutations reveals residues required for MinE stimulation of the MinD ATPase and residues required for MinC interaction. J Bacteriol. 2005; 187(2):629-38. PMC: 543533. DOI: 10.1128/JB.187.2.629-638.2005. View

Skovran E, Lauhon C, Downs D . Lack of YggX results in chronic oxidative stress and uncovers subtle defects in Fe-S cluster metabolism in Salmonella enterica. J Bacteriol. 2004; 186(22):7626-34. PMC: 524902. DOI: 10.1128/JB.186.22.7626-7634.2004. View

Parsonage D, Senior A . Directed mutations of the strongly conserved lysine 155 in the catalytic nucleotide-binding domain of beta-subunit of F1-ATPase from Escherichia coli. J Biol Chem. 1988; 263(10):4740-4. View

Lutkenhaus J, Sundaramoorthy M . MinD and role of the deviant Walker A motif, dimerization and membrane binding in oscillation. Mol Microbiol. 2003; 48(2):295-303. DOI: 10.1046/j.1365-2958.2003.03427.x. View

Koo M, Lee J, Rah S, Yeo W, Lee J, Lee K . A reducing system of the superoxide sensor SoxR in Escherichia coli. EMBO J. 2003; 22(11):2614-22. PMC: 156749. DOI: 10.1093/emboj/cdg252. View

Raulfs E, OCarroll I, Dos Santos P, Unciuleac M, Dean D . In vivo iron-sulfur cluster formation. Proc Natl Acad Sci U S A. 2008; 105(25):8591-6. PMC: 2438426. DOI: 10.1073/pnas.0803173105. View

10.

Bates P, Kelley L, MacCallum R, STERNBERG M . Enhancement of protein modeling by human intervention in applying the automatic programs 3D-JIGSAW and 3D-PSSM. Proteins. 2002; Suppl 5:39-46. DOI: 10.1002/prot.1168. View

11.

Takahashi Y, Tokumoto U . A third bacterial system for the assembly of iron-sulfur clusters with homologs in archaea and plastids. J Biol Chem. 2002; 277(32):28380-3. DOI: 10.1074/jbc.C200365200. View

12.

Justino M, Almeida C, Goncalves V, Teixeira M, Saraiva L . Escherichia coli YtfE is a di-iron protein with an important function in assembly of iron-sulphur clusters. FEMS Microbiol Lett. 2006; 257(2):278-84. DOI: 10.1111/j.1574-6968.2006.00179.x. View

13.

Chan K, Delfert D, Junger K . A direct colorimetric assay for Ca2+ -stimulated ATPase activity. Anal Biochem. 1986; 157(2):375-80. DOI: 10.1016/0003-2697(86)90640-8. View

14.

Reinstein J, Schlichting I, Wittinghofer A . Structurally and catalytically important residues in the phosphate binding loop of adenylate kinase of Escherichia coli. Biochemistry. 1990; 29(32):7451-9. DOI: 10.1021/bi00484a014. View

15.

Lewis J, Horswill A, Schwem B, Escalante-Semerena J . The Tricarballylate utilization (tcuRABC) genes of Salmonella enterica serovar Typhimurium LT2. J Bacteriol. 2004; 186(6):1629-37. PMC: 355976. DOI: 10.1128/JB.186.6.1629-1637.2004. View

16.

Kreuzer K, Jongeneel C . Escherichia coli phage T4 topoisomerase. Methods Enzymol. 1983; 100:144-60. DOI: 10.1016/0076-6879(83)00051-8. View

17.

Antonkine M, Maes E, Czernuszewicz R, Breitenstein C, Bill E, Falzone C . Chemical rescue of a site-modified ligand to a [4Fe-4S] cluster in PsaC, a bacterial-like dicluster ferredoxin bound to Photosystem I. Biochim Biophys Acta. 2007; 1767(6):712-24. DOI: 10.1016/j.bbabio.2007.02.003. View

18.

Jin Z, Heinnickel M, Krebs C, Shen G, Golbeck J, Bryant D . Biogenesis of iron-sulfur clusters in photosystem I: holo-NfuA from the cyanobacterium Synechococcus sp. PCC 7002 rapidly and efficiently transfers [4Fe-4S] clusters to apo-PsaC in vitro. J Biol Chem. 2008; 283(42):28426-35. PMC: 2661401. DOI: 10.1074/jbc.M803395200. View

19.

Dos Santos P, Smith A, Frazzon J, Cash V, Johnson M, Dean D . Iron-sulfur cluster assembly: NifU-directed activation of the nitrogenase Fe protein. J Biol Chem. 2004; 279(19):19705-11. DOI: 10.1074/jbc.M400278200. View

20.

Lewis J, Escalante-Semerena J . Tricarballylate catabolism in Salmonella enterica. The TcuB protein uses 4Fe-4S clusters and heme to transfer electrons from FADH2 in the tricarballylate dehydrogenase (TcuA) enzyme to electron acceptors in the cell membrane. Biochemistry. 2007; 46(31):9107-15. DOI: 10.1021/bi7006564. View