The mitochondrial proteins Atm1p and Nfs1p are essential for biogenesis of cytosolic Fe/S proteins

EMBO Journal

Volumn 18, Issue 14, 1999, Pages 3981-3989

  Kispal, Gyula ^a,b   Csere, Peter ^a   Prohl, Corinna ^a   Lill, Roland ^a  

^a Fachbereich Medizin der Universitat Marburg   (Germany)

^b UNIVERSITY OF PÉCS   (Hungary)

Author keywords

ABC transporter; Iron homeostasis; Iron sulfur protein; Mitochondria; Sideroblastic anemia

Indexed keywords

ABC TRANSPORTER; CELL PROTEIN; IRON SULFUR PROTEIN; MITOCHONDRIAL ENZYME; PROTEIN PRECURSOR; SULFUR;

ARTICLE; BIOGENESIS; CONTROLLED STUDY; ELECTRON TRANSPORT; EUKARYOTIC CELL; HOMEOSTASIS; IRON TRANSPORT; ISOTOPE LABELING; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS;

ANTIBODIES; APOPROTEINS; ATP-BINDING CASSETTE TRANSPORTERS; BIOLOGICAL TRANSPORT; CYTOSOL; FUNGAL PROTEINS; GENES, FUNGAL; INTRACELLULAR MEMBRANES; IRON-SULFUR PROTEINS; MEMBRANE POTENTIALS; MITOCHONDRIA; MODELS, BIOLOGICAL; MUTATION; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 0033565665     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/18.14.3981     Document Type: Article

References (54)

1. Allikmets, R., Raskind, W.H., Hutchinson, A., Schueck, N.D., Dean, M. and Koeller, D.M. (1999) Mutation of a putative mitochondrial iron transporter gene (ABC7) in X-linked sideroblastic anemia and ataxia (XLSA/A). Hum. Mol. Gen., 8, 743-749.
2. Andersson, S.G. et al. (1998) The genome sequence of Rickettsia prowazekii and the origin of mitochondria. Nature, 396, 133-140.
3. Askwith, C. and Kaplan, J. (1998) Iron and copper transport in yeast and its relevance to human disease. Trends Biochem. Sci., 23, 135-138.
4. Augeri, L., Lee, Y.M., Barton, A.B. and Doetsch, P.W. (1997) Purification, characterization, gene cloning and expression of Saccharomyces cerevisiae redoxyendonuclease, a homolog of Escherichia coli endonuclease III. Biochemistry, 36, 721-729.
5. Babcock, M., De Silva, D., Oaks, R., Davis-Kaplan, S., Jiralerspong, S., Montermini, L., Pandolfo, M. and Kaplan, J. (1997) Regulation of mitochondrial iron accumulation by Yfh1p, a putative homolog of frataxin. Science, 276, 1709-1712.
6. Beinert, H., Holm, R.H. and Münck, E. (1997) Iron-sulfur clusters: Nature's modular, multipurpose structures. Science, 277, 653-659.
7. Beltzer, J.P., Morris, S.R. and Kohlhaw, G.B. (1988) Yeast LEU4 encodes mitochondrial and nonmitochondrial forms of α-isopropylmalate synthase. J. Biol. Chem., 263, 368-374.
8. Bisbal, C., Martinand, C., Silhol, M., Lebleu, B. and Salehzada, T. (1995) Cloning and characterization of a RNase L inhibitor. A new component of the interferon-regulated 2-5A pathway. J. Biol. Chem., 270, 13308-13317.
9. Cammack, R. (1992) Iron-sulfur clusters in enzymes: themes and variations. In Cammack, R. (ed.), Iron-Sulfur Proteins. Vol. 38. Academic Press, San Diego, CA, pp. 281-322.
10. Campuzano, V. et al. (1996) Friedreich's ataxia: autosomal recessive disease caused by an intronic GAA triplet repeat expansion. Science, 271, 1423-1427.
11. Csere, P., Lill, R. and Kispal, G. (1998) Identification of a human mitochondrial ABC transporter, the functional orthologue of yeast Atm1p. FEBS Lett., 441, 266-270.
12. 2 and cytochrome c peroxidase are located in the intermembrane space of yeast mitochondria. J. Biol. Chem., 257, 13028-13033.
13. Foury, F. and Cazzalini, O. (1997) Deletion of the yeast homologue of the human gene associated with Friedreich's ataxia elicits iron accumulation in mitochondria. FEBS Lett., 411, 373-377.
14. Gietz, D., St Jean, A., Woods, R.A. and Schiestl, R.H. (1992) Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Res., 20, 1425.
15. Glick, B.S. (1995) Pathways and energetics of mitochondrial protein import in Saccharomyces cerevisiae. Methods Enzymol., 260, 224-231.
16. Hentze, M.W. and Kuhn, L.C. (1996) Molecular control of vertebrate iron metabolism: mRNA-based regulatory circuits operated by iron, nitric oxide and oxidative stress. Proc. Natl Acad. Sci. USA, 93, 8175-8182.
17. Hinnebusch, A.G. (1992) General and pathway-specific regulatory mechanisms controlling the synthesis of amino acid biosynthetic enzymes in Saccharomyces cerevisiae. In Jones, E.W., Pringle, J.R. and Broach, J.R. (eds) The Molecular and Cellular Biology of the Yeast Saccharomyces. Vol. 2: Gene Expression. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp. 319-414.
18. Johnson, M.K. (1998) Iron-sulfur proteins: new roles for old clusters. Curr. Opin. Chem. Biol., 2, 173-181.
19. Jones, E.W. and Fink, G.R. (1982) Regulation of amino acid and nucleotide biosynthesis in yeast. In Strathern, J.N., Jones, E.W. and Broach, J.R. (eds), The Molecular Biology of the Yeast Saccharomyces. Metabolism and Gene Expression. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp. 181-299.
20. Kispal, G., Steiner, H., Court, D.A., Rolinski, B. and Lill, R. (1996) Mitochondrial and cytosolic branched-chain amino acid transaminases from yeast, homologs of the myc oncogene-regulated Eca39 protein. J. Biol. Chem., 271, 24458-24464.
21. Kispal, G., Csere, P., Guiard, B. and Lill, R. (1997) The ABC transporter Atmlp is required for mitochondrial iron homeostasis. FEBS Lett., 418, 346-350.
22. Knight, S.A., Sepuri, N.B., Pain, D. and Dancis, A. (1998) Mt-Hsp70 homolog, Ssc2p, required for maturation of yeast frataxin and mitochondrial iron homeostasis. J. Biol. Chem., 273, 18389-18393.
23. Kohlhaw, G.B. (1988a) α-isopropylmalate synthase from yeast. Methods Enzymol., 166, 414-423.
24. Kohlhaw, G.B. (1988b) β-isopropylmalate dehydrogenase from yeast. Methods Enzymol., 166, 429-435.
25. Kohlhaw, G.B. (1988c) Isopropylmalate dehydratase from yeast. Methods Enzymol., 166, 423-429.
26. Lacour, T., Achstetter, T. and Dumas, B. (1998) Characterization of recombinant adrenodoxin reductase homologue (Arh1p) from yeast. Implication in in vitro cytochrome p45011 beta monooxygenase system. J. Biol. Chem., 273, 23984-23992.
27. Land, T. and Rouault, T.A. (1998) Targeting of a human iron-sulfur cluster assembly enzyme, nifs, to different subcellular compartments is regulated through alternative AUG utilization. Mol. Cell, 2, 807-815.
28. Leighton, J. and Schatz, G. (1995) An ABC transporter in the mitochondrial inner membrane is required for normal growth of yeast. EMBO J., 14, 188-195.
29. Lill, R., Nargang, F.E. and Neupert, W. (1996) Biogenesis of mitochondrial proteins. Curr. Opin. Cell Biol., 8, 505-512.
30. Lombardo, A., Carine, K. and Scheffler, I.E. (1990) Cloning and characterization of the iron-sulfur subunit gene of succinate dehydrogenase from Saccharomyces cerevisiae. J. Biol. Chem., 265, 10419-10423.
31. Nakai, Y., Yoshihara, Y., Hayashi, H. and Kagamiyama, H. (1998) cDNA cloning and characterization of mouse nifS-like protein, m-Nfs1: mitochondrial localization of eukaryotic NifS-like proteins. FEBS Lett., 433, 143-148.
32. Neupert, W. (1997) Protein import into mitochondria. Annu. Rev. Biochem., 66, 861-915.
33. Peters, J.W., Fisher, K. and Dean, D.R. (1995) Nitrogenase structure and function: a biochemical-genetic perspective. Annu. Rev. Microbiol., 49, 335-366.
34. Pfanner, N., Craig, E.A. and Honlinger, A. (1997) Mitochondrial preprotein translocase. Annu. Rev. Cell Dev. Biol., 13, 25-51.
35. Radisky, D.C., Babcock, M.C. and Kaplan, J. (1999) The yeast frataxin homologue mediates mitochondrial iron efflux. Evidence for a mitochondrial iron cycle. J. Biol. Chem., 274, 4497-4499.
36. Robinson, K.M. and Lemire, B.D. (1995) Flavinylation of succinate: ubiquinone oxidoreductase from Saccharomyces cerevisiae. Methods Enzymol., 260, 34-51.
37. Robinson, K.M., von Kieckebusch-Guck, A. and Lemire, B.D. (1991) Isolation and characterization of a Saccharomyces cerevisiae mutant disrupted for the succinate dehydrogenase flavoprotein subunit. J. Biol. Chem., 266, 21347-21350.
38. Rotig, A., de Lonlay, P., Chretien, D., Foury, F., Koenig, M., Sidi, D., Munnich, A. and Rustin, P. (1997) Aconitase and mitochondrial iron-sulfur protein deficiency in Friedreich ataxia. Nature Genet., 17, 215-217.
39. Rouault, T.A. and Klausner, R.D. (1996) Iron-sulfur clusters as biosensors of oxidants and iron. Trends Biochem. Sci., 21, 174-177.
40. Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. 2nd edn. Cold Spring Harbor Press, Cold Spring Harbor, NY.
41. Schatz, G. and Dobberstein, B. (1996) Common principles of protein translocation across membranes. Science, 271, 1519-1526.
42. Schlenstedt, G., Harris, S., Risse, B., Lill, R. and Silver, P.A. (1995) A yeast DnaJ homolog, Scj1p, can function in the endoplasmic reticulum with BiP/Kar2p via a conserved domain that specifies interactions with Hsp70s. J. Cell Biol., 129, 979-988.
43. Sherman, F. (1991) Getting started with yeast. Methods Enzymol., 194, 3-21.
44. Sirrenberg, C., Bauer, M.F., Guiard, B., Neupert, W. and Brunner, M. (1996) Import of carrier proteins into the mitochondrial inner membrane mediated by Tim22. Nature, 384, 582-585.
45. Steiner, H., Kispal, G., Zollner, A., Haid, A., Neupert, W. and Lill, R. (1996) Heme binding to a conserved CysProVal motif is crucial for the catalytic function of mitochondrial heme lyases. J. Biol. Chem., 271, 32605-32611.
46. Strain, J., Lorenz, C.R., Bode, J., Garland, S., Smolen, G.A., Ta, D.T., Vickery, L.E. and Culotta, V.C. (1998) Suppressors of superoxide dismutase (SOD1) deficiency in Saccharomyces cerevisiae. Identification of proteins predicted to mediate iron-sulfur cluster assembly. J. Biol. Chem., 273, 31138-31144.
47. Tangeras, A., Flatmark, T., Bäckström, D. and Ehrenberg, A. (1980) Mitochondrial iron not bound in heme and iron-sulfur centers. Estimation, compartmentation and redox state. Biochim. Biophys. Acta, 589, 162-175.
48. Wienhues, U., Becker, K., Schleyer, M., Guiard, B., Tropschug, M., Horwich, A.L., Pfanner, N. and Neupert, W. (1991) Protein folding causes an arrest of preprotein translocation in mitochondria in vivo. J. Cell Biol., 115, 1601-1609.
49. Woonter, M. and Jaehning, J.A. (1990) Accurate initiation by RNA polymerase II in whole cell extracts from Saccharomyces cerevisiae. J. Biol. Chem., 265, 8979-8982.
50. Yamaguchi-Iwai, Y., Stearman, R., Dancis, A. and Klausner, R.D. (1996) Iron-regulated DNA binding by the AFT1 protein controls the iron regulon in yeast. EMBO J., 15, 3377-3384.
51. Zheng, L. and Dean, D.R. (1994) Catalytic formation of a nitrogenase iron-sulfur cluster. J. Biol. Chem., 269, 18723-18726.
52. Zheng, L., White, R.H., Cash, V.L., Jack, R.F. and Dean, D.R. (1993) Cysteine desulfurase activity indicates a role for NifS in metallocluster biosynthesis. Proc. Natl Acad. Sci. USA, 90, 2754-2758.
53. Zheng, L., Cash, V.L., Flint, D.H. and Dean, D.R. (1998) Assembly of iron-sulfur clusters. Identification of an iscSUA-hscBA-fdx gene cluster from Azotobacter vinelandii. J. Biol. Chem., 273, 13264-13272.
54. 1 heme lyase. Eur. J. Biochem., 207, 1093-1100.