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The Cfd1–Nbp35 complex acts as a scaffold for iron-sulfur protein assembly in the yeast cytosol - Nature Chemical Biology

  • ️Lill, Roland
  • ️Sun Apr 01 2007

References

  1. Beinert, H., Holm, R.H. & Münck, E. Iron-sulfur clusters: nature's modular, multipurpose structures. Science 277, 653–659 (1997).

    Article  CAS  Google Scholar 

  2. Beinert, H., Meyer, J. & Lill, R. in Encyclopedia of Biological Chemistry Vol. 2 (eds. Lennarz, W.J. & Lane, M.D.) 482–489 (Academic, Amsterdam, 2004).

    Book  Google Scholar 

  3. Barras, F., Loiseau, L. & Py, B. How Escherichia coli and Saccharomyces cerevisiae build Fe/S proteins. Adv. Microb. Physiol. 50, 41–101 (2005).

    Article  CAS  Google Scholar 

  4. 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, 247–281 (2005).

    Article  CAS  Google Scholar 

  5. Fontecave, M., Choudens, S.O., Py, B. & Barras, F. Mechanisms of iron-sulfur cluster assembly: the SUF machinery. J. Biol. Inorg. Chem. 10, 713–721 (2005).

    Article  CAS  Google Scholar 

  6. Balk, J. & Lobreaux, S. Biogenesis of iron-sulfur proteins in plants. Trends Plant Sci. 10, 324–331 (2005).

    Article  CAS  Google Scholar 

  7. Rubio, L.M. & Ludden, P.W. Maturation of nitrogenase: a biochemical puzzle. J. Bacteriol. 187, 405–414 (2005).

    Article  CAS  Google Scholar 

  8. Lill, R. & Mühlenhoff, U. Iron-sulfur protein biogenesis in eukaryotes. Trends Biochem. Sci. 30, 133–141 (2005).

    Article  CAS  Google Scholar 

  9. Lill, R. & Mühlenhoff, U. Iron-sulfur protein biogenesis in eukaryotes: components and mechanisms. Annu. Rev. Cell Dev. Biol. 22, 457–486 (2006).

    Article  CAS  Google Scholar 

  10. Rouault, T.A. & Tong, W.H. Iron-sulphur cluster biogenesis and mitochondrial iron homeostasis. Nat. Rev. Mol. Cell Biol. 6, 345–351 (2005).

    Article  CAS  Google Scholar 

  11. Roy, A., Solodovnikova, N., Nicholson, T., Antholine, W. & Walden, W.E. A novel eukaryotic factor for cytosolic Fe-S cluster assembly. EMBO J. 22, 4826–4835 (2003).

    Article  CAS  Google Scholar 

  12. Balk, J., Pierik, A.J., Aguilar Netz, D., Mühlenhoff, U. & Lill, R. The hydrogenase-like Nar1p is essential for maturation of cytosolic and nuclear iron-sulphur proteins. EMBO J. 23, 2105–2115 (2004).

    Article  CAS  Google Scholar 

  13. Hausmann, A. et al. The eukaryotic P-loop NTPase Nbp35: an essential component of the cytosolic and nuclear iron-sulfur protein assembly machinery. Proc. Natl. Acad. Sci. USA 102, 3266–3271 (2005).

    Article  CAS  Google Scholar 

  14. Balk, J., Aguilar Netz, D.J., Tepper, K., Pierik, A.J. & Lill, R. The essential WD40 protein Cia1 is involved in a late step of cytosolic and nuclear iron-sulfur protein assembly. Mol. Cell. Biol. 25, 10833–10841 (2005).

    Article  CAS  Google Scholar 

  15. Kispal, G., Csere, P., Prohl, C. & Lill, R. The mitochondrial proteins Atm1p and Nfs1p are required for biogenesis of cytosolic Fe/S proteins. EMBO J. 18, 3981–3989 (1999).

    Article  CAS  Google Scholar 

  16. Lange, H., Kispal, G., Kaut, A. & Lill, R. A mitochondrial ferredoxin is essential for biogenesis of intra- and extra-mitochondrial Fe/S proteins. Proc. Natl. Acad. Sci. USA 97, 1050–1055 (2000).

    Article  CAS  Google Scholar 

  17. Li, J., Saxena, S., Pain, D. & Dancis, A. Adrenodoxin reductase homolog (Arh1p) of yeast mitochondria required for iron homeostasis. J. Biol. Chem. 276, 1503–1509 (2001).

    Article  CAS  Google Scholar 

  18. Gerber, J., Neumann, K., Prohl, C., Mühlenhoff, U. & Lill, R. The yeast scaffold proteins Isu1p and Isu2p are required inside mitochondria for maturation of cytosolic Fe/S proteins. Mol. Cell. Biol. 24, 4848–4857 (2004).

    Article  CAS  Google Scholar 

  19. Pondarre, C. et al. The mitochondrial ATP-binding cassette transporter Abcb7 is essential in mice and participates in cytosolic iron-sulphur cluster biogenesis. Hum. Mol. Genet. 15, 953–964 (2006).

    Article  CAS  Google Scholar 

  20. Mühlenhoff, U. et al. Functional characterization of the eukaryotic cysteine desulfurase Nfs1p from Saccharomyces cerevisiae. J. Biol. Chem. 279, 36906–36915 (2004).

    Article  Google Scholar 

  21. Biederbick, A. et al. Role of human mitochondrial Nfs1 in cytosolic iron-sulfur protein biogenesis and iron regulation. Mol. Cell. Biol. 26, 5675–5687 (2006).

    Article  CAS  Google Scholar 

  22. Fosset, C. et al. RNA silencing of mitochondrial m-Nfs1 reduces Fe-S enzyme activity both in mitochondria and cytosol of mammalian cells. J. Biol. Chem. 281, 25398–25406 (2006).

    Article  CAS  Google Scholar 

  23. Ghaemmaghami, S. et al. Global analysis of protein expression in yeast. Nature 425, 737–741 (2003).

    Article  CAS  Google Scholar 

  24. Puig, O. et al. The tandem affinity purification (TAP) method: a general procedure of protein complex purification. Methods 24, 218–229 (2001).

    Article  CAS  Google Scholar 

  25. Skerra, A. & Schmidt, T.G. Use of the Strep-Tag and streptavidin for detection and purification of recombinant proteins. Methods Enzymol. 326, 271–304 (2000).

    Article  CAS  Google Scholar 

  26. Orme-Johnson, W.H. & Orme-Johnson, N.R. Overview of iron-sulfur proteins. Methods Enzymol. 53, 259–268 (1978).

    Article  CAS  Google Scholar 

  27. Agar, J.N. et al. IscU as a scaffold for iron-sulfur cluster biosynthesis: sequential assembly of [2Fe-2S] and [4Fe-4S] clusters in IscU. Biochemistry 39, 7856–7862 (2000).

    Article  CAS  Google Scholar 

  28. Yuvaniyama, P., Agar, J.N., Cash, V.L., Johnson, M.K. & Dean, D.R. NifS-directed assembly of a transient [2Fe-2S] cluster within the NifU protein. Proc. Natl. Acad. Sci. USA 97, 599–604 (2000).

    Article  CAS  Google Scholar 

  29. Mühlenhoff, U., Gerber, J., Richhardt, N. & Lill, R. Components involved in assembly and dislocation of iron-sulfur clusters on the scaffold protein Isu1p. EMBO J. 22, 4815–4825 (2003).

    Article  Google Scholar 

  30. Bonomi, F., Iametti, S., Ta, D. & Vickery, L.E. Multiple turnover transfer of [2Fe2S] clusters by the iron-sulfur cluster assembly scaffold proteins IscU and IscA. J. Biol. Chem. 280, 29513–29518 (2005).

    Article  CAS  Google Scholar 

  31. Smith, A.D. et al. NifS-mediated assembly of [4Fe-4S] clusters in the N- and C-terminal domains of the NifU scaffold protein. Biochemistry 44, 12955–12969 (2005).

    Article  CAS  Google Scholar 

  32. Dutkiewicz, R. et al. The Hsp70 chaperone Ssq1p is dispensable for iron-sulfur cluster formation on the scaffold protein Isu1p. J. Biol. Chem. 281, 7801–7808 (2006).

    Article  CAS  Google Scholar 

  33. Chandramouli, K. & Johnson, M.K. HscA and HscB stimulate [2Fe-2S] cluster transfer from IscU to apoferredoxin in an ATP-dependent reaction. Biochemistry 45, 11087–11095 (2006).

    Article  CAS  Google Scholar 

  34. Chen, O.S. et al. Transcription of the yeast iron regulon responds not directly to iron but rather to iron-sulfur cluster biosynthesis. J. Biol. Chem. 279, 29513–29518 (2004).

    Article  CAS  Google Scholar 

  35. Leipe, D.D., Wolf, Y.I., Koonin, E.V. & Aravind, L. Classification and evolution of P-loop GTPases and related ATPases. J. Mol. Biol. 317, 41–72 (2002).

    Article  CAS  Google Scholar 

  36. Skovran, E. & Downs, D.M. Lack of the ApbC or ApbE protein results in a defect in Fe-S cluster metabolism in Salmonella enterica serovar Typhimurium. J. Bacteriol. 185, 98–106 (2003).

    Article  CAS  Google Scholar 

  37. 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. 37, 174–185 (2004).

    Article  CAS  Google Scholar 

  38. Stockel, J. & Oelmuller, R. A novel protein for photosystem I biogenesis. J. Biol. Chem. 279, 10243–10251 (2004).

    Article  Google Scholar 

  39. Lill, R. & Kispal, G. Maturation of cellular Fe/S proteins: the essential function of mitochondria. Trends Biochem. Sci. 25, 352–356 (2000).

    Article  CAS  Google Scholar 

  40. Gerber, J., Mühlenhoff, U. & Lill, R. An interaction between frataxin and Isu1/Nfs1 that is crucial for Fe/S cluster synthesis on Isu1. EMBO Rep. 4, 906–911 (2003).

    Article  CAS  Google Scholar 

  41. Yoon, T. & Cowan, J.A. Frataxin-mediated iron delivery to ferrochelatase in the final step of heme biosynthesis. J. Biol. Chem. 279, 25943–25946 (2004).

    Article  CAS  Google Scholar 

  42. Bencze, K.Z. et al. The structure and function of frataxin. Crit. Rev. Biochem. Mol. Biol. 41, 269–291 (2006).

    Article  CAS  Google Scholar 

  43. Puccio, H. & Koenig, M. Friedreich ataxia: a paradigm for mitochondrial diseases. Curr. Opin. Genet. Dev. 12, 272–277 (2002).

    Article  CAS  Google Scholar 

  44. Bekri, S. et al. Human ABC7 transporter: gene structure and mutation causing X-linked sideroblastic anemia with ataxia (XLSA/A) with disruption of cytosolic iron-sulfur protein maturation. Blood 96, 3256–3264 (2000).

    CAS  PubMed  Google Scholar 

  45. Rudolf, J., Makrantoni, V., Ingledew, W.J., Stark, M.J. & White, M.F. The DNA repair helicases XPD and FancJ have essential iron-sulfur domains. Mol. Cell 23, 801–808 (2006).

    Article  CAS  Google Scholar 

  46. Mühlenhoff, U., Richhardt, N., Ristow, M., Kispal, G. & Lill, R. The yeast frataxin homologue Yfh1p plays a specific role in the maturation of cellular Fe/S proteins. Hum. Mol. Genet. 11, 2025–2036 (2002).

    Article  Google Scholar 

  47. Kerner, M.J. et al. Proteome-wide analysis of chaperonin-dependent protein folding in Escherichia coli. Cell 122, 209–220 (2005).

    Article  CAS  Google Scholar 

  48. Takahashi, Y. & Nakamura, M. Functional assignment of the ORF2-iscS-iscU-iscA-hscB-hscA-fdx-ORF3 gene cluster involved in the assembly of Fe-S clusters in Escherichia coli. J. Biochem. 126, 917–926 (1999).

    Article  CAS  Google Scholar 

  49. Floss, B., Igloi, G.L., Cassier-Chauvat, C. & Mühlenhoff, U. Molecular characterization and overexpression of the petF gene from Synechococcus elongatus: evidence for a second site of electrostatic interaction between ferredoxin and the PS I-D subunit. Photosynth. Res. 54, 63–71 (1997).

    Article  CAS  Google Scholar 

  50. Jungermann, K., Thauer, R.K., Rupprecht, E., Ohrloff, C. & Decker, K. Ferredoxin mediated hydrogen formation from NADPH in a cell-free system of Clostridium kluyveri. FEBS Lett. 3, 144–146 (1969).

    Article  CAS  Google Scholar 

  51. Mumberg, D., Müller, R. & Funk, M. Regulatable promoters of Saccharomyces cerevisiae: comparison of transcriptional activity and their use for heterologous expression. Nucleic Acids Res. 22, 5767–5768 (1994).

    Article  CAS  Google Scholar 

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