The essential role of mitochondria in the biogenesis of cellular iron-sulfur proteins

Biological Chemistry

Volumn 380, Issue 10, 1999, Pages 1157-1166

  Lill, Roland ^a   Diekert, Kerstin ^a   Kaut, Anita ^a   Lange, Heike ^a   Pelzer, Winfried ^a   Prohl, Corinna ^a   Kispal, Gyula ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

ABC transporter; Chaperone; Ferredoxin; Iron sulfur cluster; Mitochondria; Sideroblastic anemia

Indexed keywords

ABC TRANSPORTER; CHAPERONE; CYSTATHIONINE GAMMA LYASE; FERREDOXIN; IRON; IRON SULFUR PROTEIN; MITOCHONDRIAL ENZYME; SULFUR;

HEMOSIDEROSIS; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; REVIEW;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; CELL NUCLEUS; CYTOSOL; HUMANS; INTRACELLULAR MEMBRANES; IRON-SULFUR PROTEINS; MITOCHONDRIA; SACCHAROMYCES CEREVISIAE;

EUKARYOTA; PROKARYOTA;

EID: 0032746009     PISSN: 14316730     EISSN: None     Source Type: Journal    
DOI: 10.1515/BC.1999.147     Document Type: Review

References (57)

1. Allen, R.M., Chatterjee, R., Ludden, P.W., and Shah, V.K. (1995). Incorporation of iron and sulfur from NifB cofactor into the iron-molybdenum cofactor of dinitrogenase. J. Biol. Chem. 270, 26890-26896.
2. 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.
3. Andersson, S.G., Zomorodipour, A., Andersson, J.O., Sicheritz-Ponten, T., Alsmark, U.C., Podowski, R.M., Naslund, A.K., Eriksson, A.S., Winkler, H.H., and Kurland, C.G. (1998). The genome sequence of Rickettsia prowazekii and the origin of mitochondria. Nature 396, 133-140.
4. Attardi, G., and Schatz, G. (1988). The biogenesis of mitochondria. Annu. Rev. Cell Biol. 4, 289-333.
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. Barros, M.H., and Nobrega, F.G. (1999). YAH1 of Saccharomyces cerevisiae: a new essential gene that codes for a protein homologous to human adrenodoxin. Gene 233, 197-203.
7. Beinert, H., Holm, R.H., and Münck, E. (1997). Iron-sulfur clusters: Nature's modular, multipurpose structures. Science 277, 653-659.
8. Cammack, R. (1992). Iron-sulfur clusters in enzymes: Themes and variations. In Iron-sulfur proteins, R. Cammack, ed. (San Diego, USA: Academic Press), pp. 281-322.
9. Campuzano, V., Montermini, L. Molto, M. D., Pianese, L., Cossee, M., Cavalcanti, F., Monros, E., Rodius, F., Duclos, F., Monticelli, A., Zara, F., Canizares, J., Koutnikova, H., Bidichandani, S., Gellera, C., Brice, A., Trouillas, P., DeMichele, G., Filla, A., deFrutos, R., Palau, F., Patel, P.I., DiDonato, S., Mandel, J.L, Cocozza, S., Koenig, M., and Pandolfo, M. (1996). Friedreich's ataxia: autosomal recessive disease caused by an intronic GAA triplet repeat expansion. Science 271, 1423-1427.
10. Cheng, M.Y., Hartl, F.-U., and Horwich, A.L. (1990). The mitochondrial chaperonin hsp60 is required for its own assembly. Nature 348, 455-458.
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. Dalbey, R. E., and Robinson, C. (1999). Protein translocation into and across the bacterial plasma membrane and the plant thylakoid membrane. Trends Biochem. Sci. 24, 17-22.
13. De Winde, J.H., and Grivell, L.A. (1993). Global regulation of mitochondrial biogenesis in Saccharomyces cerevisiae. Prog. Nucleic Acid Res. Mol. Biol. 46, 51-91.
14. Dean, D.R., Bolin, J.T., and Zheng, L. (1993). Nitrogenase metalloclusters: structures, organization, and synthesis. J. Bacteriol. 175, 6737-6744.
15. Dickinson, J.R. (1999). Nitrogen metabolism. In: The metabolism and molecular physiology of Saccharomyces cerevisiae., J.R. Dickinson and M. Schweizer, eds. (London, UK: Taylor and Francis Ltd.), pp. 57-77.
16. El Moualij, B., Duyckaerts, C., Lamotte-Brasseur, J., and Sluse, F.E. (1997). Phylogenetic classification of the mitochondrial carrier family of Saccharomyces cerevisiae. Yeast 13, 573-581.
17. 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.
18. Fu, W., Jack, R.F., Morgan, T.V., Dean, D.R., and Johnson, M.K. (1994). nifU gene product from Azotobacter vinelandii is a homodimer that contains two identical [2Fe-2S] clusters. Biochemistry 33, 13455-13463.
19. Grivell, L.A., Artal-Sanz, M., Hakkaart, G., de Jong, L., Nijtmans, L.G., van Oosterum, K., Siep, M., and van der Spek, H. (1999). Mitochondrial assembly in yeast. FEBS Letters 452, 57-60.
20. 0 state) restores growth of a manganese-superoxide dismutase-deficient Saccharomyces cerevisiae in hyperoxia. Evidence for electron transport as a major source of superoxide generation in vivo. J. Biol. Chem. 268, 26699-26703.
21. 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.
22. Hermann, G.J., and Shaw, J.M. (1998). Mitochondrial dynamics in yeast. Annu. Rev. Cell Dev. Biol. 14, 265-303.
23. Higgins, C.F. (1992). ABC transporters: From microorganisms to man. Annu. Rev. Cell Biol. 8, 67-113.
24. Hinnebusch, A.G. (1992). General and pathway-specific regulatory mechanisms controlling the synthesis of amino acid biosynthetic enzymes in Saccharomyces cerevisiae. In: The molecular and cellular biology of the yeast Saccharomyces. Vol. II: Gene expression., E.W. Jones, J.R. Pringle and J.R. Broach, eds. (Cold Spring Harbor, USA: CSH Laboratory Press), pp. 319-414.
25. Johnson, M.K. (1998). Iron-sulfur proteins: new roles for old clusters. Curr. Opin. Chem. Biol. 2, 173-181.
26. Kispal, G., Csere, P., Guiard, B., and Lill, R. (1997). The ABC transporter Atm1p is required for mitochondrial iron homeostasis. FEBS Lett. 418, 346-350.
27. Kispal, G., Csere, P., Prohl, C., and Lill, R. (1999). The mitochondrial proteins Atm1p and Nfs1p are required for biogenesis of cytosolic Fe/S proteins. EMBO J. 18, 3981-3989.
28. 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.
29. 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.
30. Kohlhaw, G. B. (1988). Isopropylmalate dehydratase from yeast. Methods Enzymol. 166, 423-429.
31. Kolman, C., and Soll, D. (1993). SPL1-1, a Saccharomyces cerevisiae mutation affecting tRNA splicing. J. Bacteriol. 175, 1433-1442.
32. 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.
33. 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.
34. Lange, H., Kispal, G., and Lill, R. (1999). Mechanism of iron transport to the site of heme synthesis inside yeast mitochondria. J. Biol. Chem. 274, 18989-18996.
35. 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.
36. Lill, R., Nargang, F.E., and Neupert, W. (1996). Biogenesis of mitochondrial proteins. Curr. Opin. Cell Biol. 8, 505-512.
37. Manzella, L., Barros, M.H., and Nobrega, F.G. (1998). ARH1 of Saccharomyces cerevisiae: a new essential gene that codes for a protein homologous to the human adrenodoxin reductase. Yeast 14, 839-846.
38. Matsubara, H., and Saeki, K. (1992). Structural and functional diversity of ferredoxins and related proteins. In Iron-sulfur proteins, R. Cammack, ed. (San Diego, USA: Academic Press), pp. 223-280.
39. 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.
40. Neupert, W. (1997). Protein import into mitochondria. Ann. Rev. Biochem. 66, 861-915.
41. Peters, J.W., Fisher, K., and Dean, D.R. (1995). Nitrogenase structure and function: a biochemical-genetic perspective. Annu. Rev. Microbiol. 49, 335-366.
42. Pfanner, N., Craig, E.A., and Honlinger, A. (1997). Mitochondrial preprotein translocase. Annu. Rev. Cell. Dev. Biol. 13, 25-51.
43. Pon, L., and Schatz, G. (1991). Biogenesis of yeast mitochondria. In: The molecular and cellular biology of the yeast Saccharomyces: Vol. I: Genome dynamics, protein synthesis, and energetics., J. R. Broach, J. R. Pringle and E. W. Jones, eds. (Cold Spring Harbor, USA: CSH Laboratory Press), pp. 333-406.
44. Prohl, C., Kispal, G., and Lill, R. (1999). Branched-chain amino acid transaminases of the yeast Saccharomyces cerevisiae. Methods Enzymol. in press.
45. Roll, J.T., Shah, V.K., Dean, D.R., and Roberts, G.P. (1995). Characteristics of NIFNE in Azotobacter vinelandii strains. Implications for the synthesis of the iron-molybdenum cofactor of dinitrogenase. J. Biol. Chem. 270, 4432-4437.
46. Rotig, A., de Lonlay, P., Chretien, D., Foury, F., Koenig, M., Sidi, D., Munnich, A., and Rustin, P. (1997). Aconitase and mitochondrial iron-sulphur protein deficiency in Friedreich ataxia. Nat. Genetics 17, 215-217.
47. Rouault, T.A., and Klausner, R.D. (1996). Iron-sulfur clusters as biosensors of oxidants and iron. Trends Biochem. Sci. 21, 174-177.
48. Rowley, N., Prip-Buus, C., Westermann, B., Brown, C., Schwarz, E., Barrell, B., and Neupert, W. (1994). Mdj1p, a novel chaper-one of the DnaJ family, is involved in mitochondrial biogenesis and protein folding. Cell 77, 249-259.
49. Scharfe, C., Zaccaria, P., Hoertnagel, K., Jaksch, M., Klopstock, T., Lill, R., Prokisch, H., Gerbitz, K. D., Mewes, H. W., and Meitinger, T. (1999). MITOP: database for mitochondria-related proteins, genes and diseases. Nucleic Acids Res. 27, 153-155.
50. Schatz, G., and Dobberstein, B. (1996). Common principles of protein translocation across membranes. Science 271, 1519-1526.
51. Schilke, B., Forster, J., Davis, J., James, P., Walter, W., Laloraya, S., Johnson, J., Miao, B., and Craig, E. (1996). The cold sensitivity of a mutant of Saccharomyces cerevisiae lacking a mitochondrial heat shock protein 70 is suppressed by loss of mitochondrial DNA. J. Cell Biol. 134, 603-613.
52. 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.
53. Westermann, B., and Neupert, W. (1997). Mdj2p, a novel DnaJ homolog in the mitochondrial inner membrane of the yeast Saccharomyces cerevisiae. J. Mol. Biol. 272, 477-483.
54. 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.
55. 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.
56. Zheng, L., and Dean, D.R. (1994). Catalytic formation of a nitrogenase iron-sulfur cluster. J. Biol. Chem. 269, 18723-18726.
57. Zheng, L., White, R.H., Cash, V.L., Jack, R.F., and Dean, D.R. (1993). Cysteine desulfurase acitivity indicates a role for NifS in metallocluster biosynthesis. Proc. Natl. Acad. Sci. USA. 90, 2754-2758.