Structural/Functional Properties of Human NFU1, an Intermediate [4Fe-4S] Carrier in Human Mitochondrial Iron-Sulfur Cluster Biogenesis

Structure

Volumn 24, Issue 12, 2016, Pages 2080-2091

  Cai, Kai ^a   Liu, Gaohua ^b   Frederick, Ronnie O ^a   Xiao, Rong ^b   Montelione, Gaetano T ^b,c   Markley, John L ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b RUTGERS UNIVERSITY   (United States)

^c RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

Author keywords

Fe S cluster transfer; iron sulfur protein biosynthesis; NMR spectroscopy; small angle X ray scattering

Indexed keywords

DIMER; IRON SULFUR PROTEIN; MONOMER; NFU1 PROTEIN; PROTEIN; PROTEOME; UNCLASSIFIED DRUG; CARRIER PROTEIN; IRON; NFU1 PROTEIN, HUMAN; SULFUR;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; BETA SHEET; BIOGENESIS; CARBOXY TERMINAL SEQUENCE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DISULFIDE BOND; ELECTRON SPIN RESONANCE; HETERONUCLEAR SINGLE QUANTUM COHERENCE; HUMAN; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEAR OVERHAUSER EFFECT; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; SIZE EXCLUSION CHROMATOGRAPHY; STRUCTURAL MODEL; ULTRAVIOLET SPECTROSCOPY; X RAY CRYSTALLOGRAPHY; CHEMISTRY; METABOLISM; MITOCHONDRION; MOLECULAR MODEL; NUCLEAR MAGNETIC RESONANCE; PROTEIN SECONDARY STRUCTURE; SMALL ANGLE SCATTERING; X RAY DIFFRACTION;

CARRIER PROTEINS; HUMANS; IRON; IRON-SULFUR PROTEINS; MITOCHONDRIA; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN STRUCTURE, SECONDARY; SCATTERING, SMALL ANGLE; SULFUR; X-RAY DIFFRACTION;

EID: 85001129913     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2016.08.020     Document Type: Article

References (60)

1. Acton, T.B., Xiao, R., Anderson, S., Aramini, J., Buchwald, W.A., Ciccosanti, C., Conover, K., Everett, J., Hamilton, K., Huang, Y.J., et al. Preparation of protein samples for NMR structure, function, and small-molecule screening studies. Methods Enzymol. 493 (2011), 21–60.
2. Andreini, C., Banci, L., Rosato, A., Exploiting bacterial operons to illuminate human iron-sulfur proteins. J. Proteome Res. 15 (2016), 1308–1322.
3. Aramini, J.M., Ma, L.C., Zhou, L., Schauder, C.M., Hamilton, K., Amer, B.R., Mack, T.R., Lee, H.W., Ciccosanti, C.T., Zhao, L., et al. Dimer interface of the effector domain of non-structural protein 1 from influenza A virus: an interface with multiple functions. J. Biol. Chem. 286 (2011), 26050–26060.
4. Bandyopadhyay, S., Naik, S.G., O'Carroll, I.P., Huynh, B.H., Dean, D.R., Johnson, M.K., Dos Santos, P.C., A proposed role for the Azotobacter vinelandii NfuA protein as an intermediate iron-sulfur cluster carrier. J. Biol. Chem. 283 (2008), 14092–14099.
5. Bartels, C., Xia, T.H., Billeter, M., Güntert, P., Wüthrich, K., The program XEASY for computer-supported NMR spectral-analysis of biological macromolecules. J. Biomol. NMR 5 (1995), 1–10.
6. Beinert, H., Iron-sulfur proteins: ancient structures, still full of surprises. J. Biol. Inorg. Chem. 5 (2000), 2–15.
7. Beinert, H., Kennedy, M.C., Stout, C.D., Aconitase as iron-sulfur protein, enzyme, and iron-regulatory protein. Chem. Rev. 96 (1996), 2335–2373.
8. Bhattacharya, A., Tejero, R., Montelione, G.T., Evaluating protein structures determined by structural genomics consortia. Proteins 66 (2007), 778–795.
9. Brünger, A.T., Adams, P.D., Clore, G.M., Delano, W.L., Gros, P., Grossekunstleve, R.W., Jiang, J.S., Kuszewski, J., Nilges, M., Pannu, N.S., et al. Crystallography and NMR system – a new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54 (1998), 905–921.
10. Cameron, J.M., Janer, A., Levandovskiy, V., Mackay, N., Rouault, T.A., Tong, W.H., Ogilvie, I., Shoubridge, E.A., Robinson, B.H., Mutations in iron-sulfur cluster scaffold genes NFU1 and BOLA3 cause a fatal deficiency of multiple respiratory chain and 2-oxoacid dehydrogenase enzymes. Am. J. Hum. Genet. 89 (2011), 486–495.
11. Chen, V.B., Arendall, W.B. 3rd, Headd, J.J., Keedy, D.A., Immormino, R.M., Kapral, G.J., Murray, L.W., Richardson, J.S., Richardson, D.C., MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 66 (2010), 12–21.
12. Crack, J.C., Green, J., Thomson, A.J., Le Brun, N.E., Iron-sulfur cluster sensor-regulators. Curr. Opin. Chem. Biol. 16 (2012), 35–44.
13. Delaglio, F., Grzesiek, S., Vuister, G.W., Zhu, G., Pfeifer, J., Bax, A., NMRPIPE – a multidimensional spectral processing system based on UNIX Pipes. J. Biomol. NMR 6 (1995), 277–293.
14. Eletsky, A., Jeong, M.Y., Kim, H., Lee, H.W., Xiao, R., Pagliarini, D.J., Prestegard, J.H., Winge, D.R., Montelione, G.T., Szyperski, T., Solution NMR structure of yeast succinate dehydrogenase flavinylation factor Sdh5 reveals a putative Sdh1 binding site. Biochemistry 51 (2012), 8475–8477.
15. Franke, D., Svergun, D.I., DAMMIF, a program for rapid ab-initio shape determination in small-angle scattering. J. Appl. Crystallogr. 42 (2009), 342–346.
16. Fushman, D., Weisemann, R., Thuring, H., Rüterjans, H., Backbone dynamics of ribonuclease T1 and its complex with 2'-GMP studied by two-dimensional heteronuclear NMR spectroscopy. J. Biomol. NMR 4 (1994), 61–78.
17. Gao, H., Subramanian, S., Couturier, J., Naik, S.G., Kim, S.K., Leustek, T., Knaff, D.B., Wu, H.C., Vignols, F., Huynh, B.H., et al. Arabidopsis thaliana Nfu2 accommodates [2Fe-2S] or [4Fe-4S] clusters and is competent for in vitro maturation of chloroplast [2Fe-2S] and [4Fe-4S] cluster-containing proteins. Biochemistry 52 (2013), 6633–6645.
18. Güntert, P., Automated NMR structure calculation with CYANA. Methods Mol. Biol. 278 (2004), 353–378.
19. He, L., Niemeyer, B., A novel correlation for protein diffusion coefficients based on molecular weight and radius of gyration. Biotechnol. Prog. 19 (2003), 544–548.
20. Huang, Y.J., Powers, R., Montelione, G.T., Protein NMR recall, precision, and F-measure scores (RPF scores): structure quality assessment measures based on information retrieval statistics. J. Am. Chem. Soc. 127 (2005), 1665–1674.
21. Huang, Y.J., Tejero, R., Powers, R., Montelione, G.T., A topology-constrained distance network algorithm for protein structure determination from NOESY data. Proteins 62 (2006), 587–603.
22. Huang, Y.J., Rosato, A., Singh, G., Montelione, G.T., RPF: a quality assessment tool for protein NMR structures. Nucleic Acids Res. 40 (2012), W542–W546.
23. 13C-enriched fusion proteins in Escherichia coli. J. Biomol. NMR 7 (1996), 131–141.
24. Johnson, D.C., Dean, D.R., Smith, A.D., Johnson, M.K., Structure, function, and formation of biological iron-sulfur clusters. Annu. Rev. Biochem. 74 (2005), 247–281.
25. 15N inverse detected heteronuclear NMR spectroscopy: application to staphylococcal nuclease. Biochemistry 28 (1989), 8972–8979.
26. Kim, J.H., Tonelli, M., Markley, J.L., Disordered form of the scaffold protein IscU is the substrate for iron-sulfur cluster assembly on cysteine desulfurase. Proc. Natl. Acad. Sci. USA 109 (2012), 454–459.
27. Koradi, R., Billeter, M., Wüthrich, K., MOLMOL – a program for display and analysis of macromolecular structures. J. Mol. Graph. 14 (1996), 51–55.
28. Laskowski, R.A., MacArthur, M.W., Moss, D.S., Thornton, J.M., PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26 (1993), 283–291.
29. Lee, W., Tonelli, M., Markley, J.L., NMRFAM-SPARKY: enhanced software for biomolecular NMR spectroscopy. Bioinformatics 31 (2014), 1325–1327.
30. Li, X., Romero, P., Rani, M., Dunker, A.K., Obradovic, Z., Predicting protein disorder for N-, C-, and internal regions. Genome Inform. Ser. Workshop Genome Inform. 10 (1999), 30–40.
31. Lill, R., Function and biogenesis of iron-sulphur proteins. Nature 460 (2009), 831–838.
32. Lill, R., Mühlenhoff, U., Iron-sulfur-protein biogenesis in eukaryotes. Trends Biochem. Sci. 30 (2005), 133–141.
33. Lill, R., Mühlenhoff, U., Iron-sulfur protein biogenesis in eukaryotes: components and mechanisms. Annu. Rev. Cell Dev. Biol. 22 (2006), 457–486.
34. Linge, J.P., Williams, M.A., Spronk, C.A., Bonvin, A.M., Nilges, M., Refinement of protein structures in explicit solvent. Proteins 50 (2003), 496–506.
35. Liu, G., Shen, Y., Atreya, H.S., Parish, D., Shao, Y., Sukumaran, D.K., Xiao, R., Yee, A., Lemak, A., Bhattacharya, A., et al. NMR data collection and analysis protocol for high-throughput protein structure determination. Proc. Natl. Acad. Sci. USA 102 (2005), 10487–10492.
36. Maio, N., Rouault, T.A., Iron-sulfur cluster biogenesis in mammalian cells: new insights into the molecular mechanisms of cluster delivery. Biochim. Biophys. Acta 1853 (2015), 1493–1512.
37. Maio, N., Singh, A., Uhrigshardt, H., Saxena, N., Tong, W.H., Rouault, T.A., Cochaperone binding to LYR motifs confers specificity of iron sulfur cluster delivery. Cell Metab. 19 (2014), 445–457.
38. Markley, J.L., Aceti, D.J., Bingman, C.A., Fox, B.G., Frederick, R.O., Makino, S., Nichols, K.W., Phillips, G.N. Jr., Primm, J.G., Sahu, S.C., et al. The center for eukaryotic structural genomics. J. Struct. Funct. Genomics 10 (2009), 165–179.
39. Mashruwala, A.A., Pang, Y.Y., Rosario-Cruz, Z., Chahal, H.K., Benson, M.A., Mike, L.A., Skaar, E.P., Torres, V.J., Nauseef, W.M., Boyd, J.M., Nfu facilitates the maturation of iron-sulfur proteins and participates in virulence in Staphylococcus aureus. Mol. Microbiol. 95 (2015), 383–409.
40. Moseley, H.N., Monleon, D., Montelione, G.T., Automatic determination of protein backbone resonance assignments from triple resonance nuclear magnetic resonance data. Methods Enzymol. 339 (2001), 91–108.
41. Navarro-Sastre, A., Tort, F., Stehling, O., Uzarska, M.A., Arranz, J.A., Del Toro, M., Labayru, M.T., Landa, J., Font, A., Garcia-Villoria, J., et al. A fatal mitochondrial disease is associated with defective NFU1 function in the maturation of a subset of mitochondrial Fe-S proteins. Am. J. Hum. Genet. 89 (2011), 656–667.
42. 13C labeling. Biochemistry 28 (1989), 7510–7516.
43. Petoukhov, M.V., Svergun, D.I., Global rigid body modeling of macromolecular complexes against small-angle scattering data. Biophys. J. 89 (2005), 1237–1250.
44. Petoukhov, M.V., Franke, D., Shkumatov, A.V., Tria, G., Kikhney, A.G., Gajda, M., Gorba, C., Mertens, H.D., Konarev, P.V., Svergun, D.I., New developments in the program package for small-angle scattering data analysis. J. Appl. Crystallogr. 45 (2012), 342–350.
45. Rambo, R.P., Tainer, J.A., Accurate assessment of mass, models and resolution by small-angle scattering. Nature 496 (2013), 477–481.
46. Rouault, T.A., Mammalian iron-sulphur proteins: novel insights into biogenesis and function. Nat. Rev. Mol. Cell Biol. 16 (2015), 45–55.
47. Sheftel, A.D., Wilbrecht, C., Stehling, O., Niggemeyer, B., Elsasser, H.P., Mühlenhoff, U., Lill, R., The human mitochondrial ISCA1, ISCA2, and IBA57 proteins are required for [4Fe-4S] protein maturation. Mol. Biol. Cell 23 (2012), 1157–1166.
48. Shen, Y., Atreya, H.S., Liu, G., Szyperski, T., G-matrix Fourier transform NOESY-based protocol for high-quality protein structure determination. J. Am. Chem. Soc. 127 (2005), 9085–9099.
49. Shen, Y., Delaglio, F., Cornilescu, G., Bax, A., TALOS+: a hybrid method for predicting protein backbone torsion angles from NMR chemical shifts. J. Biomol. NMR 44 (2009), 213–223.
50. Sippl, M.J., Recognition of errors in three-dimensional structures of proteins. Proteins 17 (1993), 355–362.
51. Stehling, O., Wilbrecht, C., Lill, R., Mitochondrial iron-sulfur protein biogenesis and human disease. Biochimie 100 (2014), 61–77.
52. Studier, F.W., Protein production by auto-induction in high-density shaking cultures. Protein Expr. Purif. 41 (2005), 207–234.
53. Svergun, D.I., Determination of the regularization parameter in indirect-transform methods using perceptual criteria. J. Appl. Crystallogr. 25 (1992), 495–503.
54. Svergun, D., Barberato, C., Koch, M.H.J., CRYSOL – a program to evaluate x-ray solution scattering of biological macromolecules from atomic coordinates. J. Appl. Crystallogr. 28 (1995), 768–773.
55. Tejero, R., Snyder, D., Mao, B., Aramini, J.M., Montelione, G.T., PDBStat: a universal restraint converter and restraint analysis software package for protein NMR. J. Biomol. NMR 56 (2013), 337–351.
56. 15N-enriched human ubiquitin resulting from relaxation interference and residual dipolar coupling. J. Am. Chem. Soc. 118 (1996), 6264–6272.
57. Tong, W.H., Jameson, G.N.L., Huynh, B.H., Rouault, T.A., Subcellular compartmentalization of human Nfu, an iron-sulfur cluster scaffold protein, and its ability to assemble a [4Fe-4S] cluster. Proc. Natl. Acad. Sci. USA 100 (2003), 9762–9767.
58. Unciuleac, M.C., Chandramouli, K., Naik, S., Mayer, S., Huynh, B.H., Johnson, M.K., Dean, D.R., In vitro activation of apo-aconitase using a [4Fe-4S] cluster-loaded form of the IscU [Fe-S] cluster scaffolding protein. Biochemistry 46 (2007), 6812–6821.
59. Yabe, T., Yamashita, E., Kikuchi, A., Morimoto, K., Nakagawa, A., Tsukihara, T., Nakai, M., Structural analysis of Arabidopsis CnfU protein: an iron-sulfur cluster biosynthetic scaffold in chloroplasts. J. Mol. Biol. 381 (2008), 160–173.
60. Yang, J., Yan, R., Roy, A., Xu, D., Poisson, J., Zhang, Y., The I-TASSER suite: protein structure and function prediction. Nat. Methods 12 (2015), 7–8.