Mitochondrial Cysteine Desulfurase and ISD11 Coexpressed in Escherichia coli Yield Complex Containing Acyl Carrier Protein

ACS Chemical Biology

Volumn 12, Issue 4, 2017, Pages 918-921

  Cai, Kai ^a   Frederick, Ronnie O ^a   Tonelli, Marco ^a   Markley, John L ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACYL CARRIER PROTEIN; CYSTATHIONINE GAMMA LYASE; IRON; PROTEIN; PROTEIN ISD11; SULFUR; UNCLASSIFIED DRUG; IRON REGULATORY FACTOR; ISD11 PROTEIN, HUMAN; LYASE; RECOMBINANT PROTEIN;

AMINO ACID ANALYSIS; AMINO ACID COMPOSITION; ARTICLE; ESCHERICHIA COLI; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; STOICHIOMETRY; ENZYMOLOGY; GENETICS; METABOLISM; MITOCHONDRION; POLYACRYLAMIDE GEL ELECTROPHORESIS; SIZE EXCLUSION CHROMATOGRAPHY; SMALL ANGLE SCATTERING; TANDEM MASS SPECTROMETRY; X RAY DIFFRACTION;

ACYL CARRIER PROTEIN; CARBON-SULFUR LYASES; CHROMATOGRAPHY, GEL; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ESCHERICHIA COLI; IRON-REGULATORY PROTEINS; MITOCHONDRIA; RECOMBINANT PROTEINS; SCATTERING, SMALL ANGLE; TANDEM MASS SPECTROMETRY; X-RAY DIFFRACTION;

EID: 85018515708     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/acschembio.6b01005     Document Type: Article

References (27)

1. Marelja, Z., Stocklein, W., Nimtz, M., and Leimkuhler, S. (2008) A novel role for human Nfs1 in the cytoplasm: Nfs1 acts as a sulfur donor for MOCS3, a protein involved in molybdenum cofactor biosynthesis J. Biol. Chem. 283, 25178-25185 10.1074/jbc.M804064200
2. Tsai, C. L. and Barondeau, D. P. (2010) Human Frataxin Is an Allosteric Switch That Activates the Fe-S Cluster Biosynthetic Complex Biochemistry 49, 9132-9139 10.1021/bi1013062
3. Tsai, C. L., Bridwell-Rabb, J., and Barondeau, D. P. (2011) Friedreich's ataxia variants I154F and W155R diminish frataxin-based activation of the iron-sulfur cluster assembly complex Biochemistry 50, 6478-6487 10.1021/bi200666h
4. Bridwell-Rabb, J., Fox, N. G., Tsai, C. L., Winn, A. M., and Barondeau, D. P. (2014) Human frataxin activates fe-s cluster biosynthesis by facilitating sulfur transfer chemistry Biochemistry 53, 4904-4913 10.1021/bi500532e
5. Bridwell-Rabb, J., Iannuzzi, C., Pastore, A., and Barondeau, D. P. (2012) Effector role reversal during evolution: the case of frataxin in Fe-S cluster biosynthesis Biochemistry 51, 2506-2514 10.1021/bi201628j
6. Bridwell-Rabb, J., Winn, A. M., and Barondeau, D. P. (2011) Structure-function analysis of Friedreich's ataxia mutants reveals determinants of frataxin binding and activation of the Fe-S assembly complex Biochemistry 50, 7265-7274 10.1021/bi200895k
7. Cai, K., Frederick, R. O., Kim, J. H., Reinen, N. M., Tonelli, M., and Markley, J. L. (2013) Human mitochondrial chaperone (mtHSP70) and cysteine desulfurase (NFS1) bind preferentially to the disordered conformation, whereas co-chaperone (HSC20) binds to the structured conformation of the iron-sulfur cluster scaffold protein (ISCU) J. Biol. Chem. 288, 28755-28770 10.1074/jbc.M113.482042
8. Terali, K., Beavil, R. L., Pickersgill, R. W., and van der Giezen, M. (2013) The effect of the adaptor protein Isd11 on the quaternary structure of the eukaryotic cysteine desulphurase Nfs1 Biochem. Biophys. Res. Commun. 440, 235-240 10.1016/j.bbrc.2013.09.039
9. Webert, H., Freibert, S. A., Gallo, A., Heidenreich, T., Linne, U., Amlacher, S., Hurt, E., Muhlenhoff, U., Banci, L., and Lill, R. (2014) Functional reconstitution of mitochondrial Fe/S cluster synthesis on Isu1 reveals the involvement of ferredoxin Nat. Commun. 5, 5013 10.1038/ncomms6013
10. Fox, N. G., Chakrabarti, M., McCormick, S. P., Lindahl, P. A., and Barondeau, D. P. (2015) The Human Iron-Sulfur Assembly Complex Catalyzes the Synthesis of [2Fe-2S] Clusters on ISCU2 That Can Be Transferred to Acceptor Molecules Biochemistry 54, 3871-3879 10.1021/bi5014485
11. Fox, N. G., Das, D., Chakrabarti, M., Lindahl, P. A., and Barondeau, D. P. (2015) Frataxin Accelerates [2Fe-2S] Cluster Formation on the Human Fe-S Assembly Complex Biochemistry 54, 3880-3889 10.1021/bi5014497
12. Gakh, O., Ranatunga, W., Smith, D. Y. t., Ahlgren, E. C., Al-Karadaghi, S., Thompson, J. R., and Isaya, G. (2016) Architecture of the Human Mitochondrial Iron-Sulfur Cluster Assembly Machinery J. Biol. Chem. 291, 21296-21321 10.1074/jbc.M116.738542
13. Van Vranken, J. G., Jeong, M. Y., Wei, P., Chen, Y. C., Gygi, S. P., Winge, D. R., and Rutter, J. (2016) The mitochondrial acyl carrier protein (ACP) coordinates mitochondrial fatty acid synthesis with iron sulfur cluster biogenesis, eLife 5, DOI: 10.7554/eLife.17828.
14. Cai, K., Tonelli, M., Frederick, R. O., and Markley, J. L. (2017) Human Mitochondrial Ferredoxin 1 (FDX1) and Ferredoxin 2 (FDX2) 2 Both Bind Cysteine Desulfurase and Donate Electrons for Iron-Sulfur 3 Cluster Biosynthesis Biochemistry 56, 487-499 10.1021/acs.biochem.6b00447
15. Kim, J. H., Tonelli, M., and Markley, J. L. (2012) Disordered form of the scaffold protein IscU is the substrate for iron-sulfur cluster assembly on cysteine desulfurase Proc. Natl. Acad. Sci. U. S. A. 109, 454-459 10.1073/pnas.1114372109
16. Petoukhov, M. V., Franke, D., Shkumatov, A. V., Tria, G., Kikhney, A. G., Gajda, M., Gorba, C., Mertens, H. D., Konarev, P. V., and Svergun, D. I. (2012) New developments in the program package for small-angle scattering data analysis J. Appl. Crystallogr. 45, 342-350 10.1107/S0021889812007662
17. Svergun, D. I. (1992) Determination of the Regularization Parameter in Indirect-Transform Methods Using Perceptual Criteria J. Appl. Crystallogr. 25, 495-503 10.1107/S0021889892001663
18. Rambo, R. P. and Tainer, J. A. (2013) Accurate assessment of mass, models and resolution by small-angle scattering Nature 496, 477-481 10.1038/nature12070
19. Schmucker, S., Martelli, A., Colin, F., Page, A., Wattenhofer-Donze, M., Reutenauer, L., and Puccio, H. (2011) Mammalian frataxin: an essential function for cellular viability through an interaction with a preformed ISCU/NFS1/ISD11 iron-sulfur assembly complex PLoS One 6, e16199 10.1371/journal.pone.0016199
20. Gully, D., Moinier, D., Loiseau, L., and Bouveret, E. (2003) New partners of acyl carrier protein detected in Escherichia coli by tandem affinity purification FEBS Lett. 548, 90-96 10.1016/S0014-5793(03)00746-4
21. Flint, D. H. (1996) Escherichia coli contains a protein that is homologous in function and N-terminal sequence to the protein encoded by the nifS gene of Azotobacter vinelandii and that can participate in the synthesis of the Fe-S cluster of dihydroxy-acid dehydratase J. Biol. Chem. 271, 16068-16074
22. Kim, J. H., Frederick, R. O., Reinen, N. M., Troupis, A. T., and Markley, J. L. (2013) [2Fe-2S]-Ferredoxin binds directly to cysteine desulfurase and supplies an electron for iron-sulfur cluster assembly but is displaced by the scaffold protein or bacterial frataxin J. Am. Chem. Soc. 135, 8117-8120 10.1021/ja401950a
23. Cupp-Vickery, J. R., Urbina, H., and Vickery, L. E. (2003) Crystal structure of IscS, a cysteine desulfurase from Escherichia coli J. Mol. Biol. 330, 1049-1059 10.1016/S0022-2836(03)00690-9
24. Shi, R., Proteau, A., Villarroya, M., Moukadiri, I., Zhang, L. H., Trempe, J. F., Matte, A., Armengod, M. E., and Cygler, M. (2010) Structural Basis for Fe-S Cluster Assembly and tRNA Thiolation Mediated by IscS Protein-Protein Interactions PLoS Biol. 8, e1000354 10.1371/journal.pbio.1000354
25. Angerer, H., Radermacher, M., Mankowska, M., Steger, M., Zwicker, K., Heide, H., Wittig, I., Brandt, U., and Zickermann, V. (2014) The LYR protein subunit NB4M/NDUFA6 of mitochondrial complex I anchors an acyl carrier protein and is essential for catalytic activity Proc. Natl. Acad. Sci. U. S. A. 111, 5207-5212 10.1073/pnas.1322438111
26. Zhu, J., Vinothkumar, K. R., and Hirst, J. (2016) Structure of mammalian respiratory complex I Nature 536, 354-358 10.1038/nature19095
27. Fiedorczuk, K., Letts, J. A., Degliesposti, G., Kaszuba, K., Skehel, M., and Sazanov, L. A. (2016) Atomic structure of the entire mammalian mitochondrial complex I Nature 538, 406-410 10.1038/nature19794