ABC TRANSPORTERS IN MITOCHONDRIA

ABC Proteins: from Bacteria to Man

Volumn , Issue , 2003, Pages 515-531

  Lill, Roland ^a   Kispal, Gyula ^b  

^a Fachbereich Medizin der Universitat Marburg   (Germany)

^b UNIVERSITY OF PÉCS   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 33746912629     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1016/B978-012352551-2/50026-3     Document Type: Chapter

References (93)

1. J. Adamec, F. Rusnak, W.G. Owen, S. Naylor, L.M. Benson, A.M. Gacy and G. Isaya (2000) Iron-dependent self-assembly of recombinant yeast frataxin: implications for Friedreich ataxia. Am. J. Hum. Genet. 67 549-562.
2. J.N. Agar, C. Krebs, J. Frazzon, B.H. Huynh, D.R. Dean and M.K. Johnson (2000) IscU as a scaffold for iron-sulfur cluster biosynthesis: sequential assembly of [2Fe-2S] and [4Fe-4S] clusters in IscU. Biochemistry 39 7856-7862.
3. J.N. Agar, P. Yuvaniyama, R.F. Jack, V.L. Cash, A.D. Smith, D.R. Dean and M.K. Johnson (2000) Modular organization and identification of a mononuclear iron-binding site within the NifU protein. J. Biol. Inorg. Chem. 5 167-177.
4. J.N. Agar, L. Zheng, V.L. Cash, D.R. Dean and M.K. Johnson (2000) Role of the IscU protein in iron-sulfur cluster biosynthesis: IscS-mediated assembly of a [Fe2S2] cluster in IscU. J. Am. Chem. Soc. 122 2136-2137.
5. R. Allikmets, W.H. Raskind, A. Hutchinson, N.D. Schueck, M. Dean and D.M. Koeller (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.
6. H. Arlt, R. Tauer, H. Feldmann, W. Neupert and T. Langer (1996) The YTA10-12 complex, an AAA protease with chaperone-like activity in the inner membrane of mitochondria. Cell 85 875-885.
7. M. Babcock, D. De Silva, R. Oaks, S. Davis-Kaplan, S. Jiralerspong, L. Montermini, M. Pandolfo and J. Kaplan (1997) Regulation of mitochondrial iron accumulation by Yfh1p, a putative homolog of frataxin. Science 276 1709-1712.
8. B.E. Bauer, H. Wolfger and K. Kuchler (1999) Inventory and function of yeast ABC proteins: about sex, stress, pleiotropic drug and heavy metal resistance. Biochim. Biophys. Acta 1461 217-236.
9. S. Bekri, G. Kispal, H. Lange, E. Fitzsimons, J. Tolmie, R. Lill and D.F. Bishop (2000) 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.
10. J.P. Beltzer, S.R. Morris and G.B. Kohlhaw (1988) Yeast LEU4 encodes mitochondrial and nonmitochondrial forms of alphaisopropylmalate synthase. J. Biol. Chem. 263 368-374.
11. E. Casalone, C. Barberio, D. Cavalieri and M. Polsinelli (2000) Identification by functional analysis of the gene encoding alpha-isopropylmalate synthase II (LEU9) in Saccharomyces cerevisiae. Yeast 16 539-545.
12. E.A. Graig, C. Voisine and B. Schilke (1999) Mitochondrial iron metabolism in the yeast Saccharomyces cerevisiae. Biol. Chem. 380 1167-1173.
13. P. Csere, R. Lill and G. Kispal (1998) Identification of a human mitochondrial ABC transporter, the functional orthologue of yeast Atm1p. FEBS Lett. 441 266-270.
14. R.E. Dalbey and A. Kuhn (2000) Evolutionarily related insertion pathways of bacterial, mitochondrial, and thylakoid. Annu. Rev. Cell Dev. Biol. 16 51-87.
15. M. Dean, R. Allikmets, B. Gerrard, C. Stewart, A. Kistler, B. Shafer, S. Michaelis and J. Strathern (1994) Mapping and sequencing of two yeast genes belonging to the ATP-binding cassette superfamily. Yeast 10 377-383.
16. A. Decottignies and A. Goffeau (1997) Complete inventory of the yeast ABC proteins. Nat. Genet. 15 137-145.
17. A. Eden, G. Simchen and N. Benvenisty (1996) Two yeast homologs of ECA39, a target for c-Myc regulation, code for cytosolic and mitochondrial branched-chain amino acid aminotransferases. J. Biol. Chem. 271 20242-20245.
18. B. El Moualij, C. Duyckaerts, J. Lamotte-Brasseur and F.E. Sluse (1997) Phylogenetic classification of the mitochondrial carrier family of Saccharomyces cerevisiae. Yeast 13 573-581.
19. T. Elliott (1997) Transporter associated with antigen processing. Adv. Immunol. 65 47-109.
20. S.E. Faivre-Nitschke, P. Nazoa, J.M. Gualberto, J.M. Grienenberger and G. Bonnard (2001) Wheat mitochondria ccmB encodes the membrane domain of a putative ABC transporter involved in cytochrome c biogenesis. Biochim. Biophys. Acta 1519 199-208.
21. F. Foury (1999) Low iron concentration and aconitase deficiency in a yeast frataxin homologue deficient strain. FEBS Lett. 456 281-284.
22. F. Foury and O. Cazzalini (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.
23. S.A. Garland, K. Hoff, L.E. Vickery and V.C. Culotta (1999) Saccharomyces cerevisiae ISU1 and ISU2: members of a well-conserved gene family for iron-sulfur cluster assembly. J. Mol. Biol. 294 897-907.
24. B.S. Goldman and R.G. Kranz (2001) ABC transporters associated with cytochrome c biogenesis. Res. Microbiol. 152 323-329.
25. B.S. Goldman, D.L. Beck, E.M. Monika and R.G. Kranz (1998) Transmembrane heme delivery systems. Proc. Natl Acad. Sci. USA 95 5003-5008.
26. C.F. Higgins (1992) ABC transporters: from microorganisms to man. Annu. Rev. Cell Biol. 8 67-113.
27. A.G. Hinnebusch (1992) General and pathway-specific regulatory mechanisms controlling the synthesis of amino acid biosynthetic enzymes in Saccharomyces cerevisiae. E.W. Jones, J.R. Pringle, J.R. Broach (Eds) The Molecular and Cellular Biology of the Yeast Saccharomyces: Vol. II: Gene Expression Cold Spring Harbor: CSH Laboratory Press 319-414.
28. K.G. Hoff, J.J. Silberg and L.E. Vickery (2000) Interaction of the iron-sulfur cluster assembly protein IscU with the Hsc66/Hsc20 molecular chaperone system of Escherichia coli. Proc. Natl Acad. Sci. USA 97 7790-7795.
29. D.L. Hogue, L. Liu and V. Ling (1999) Identification and characterization of a mammalian mitochondrial ATP-binding cassette membrane protein. J. Mol. Biol. 285 379-389.
30. L.T. Jensen and V.C. Culotta (2000) Role of Saccharomyces cerevisiae ISA1 and ISA2 in iron homeostasis. Mol. Cell. Biol. 20 3918-3927.
31. E.W. Jones and G.R. Fink (1982) Regulation of amino acid and nucleotide biosynthesis in yeast. J.N. Strathern, E.W. Jones, J.R. Broach (Eds) The Molecular Biology of the Yeast Saccharomyces. Metabolism and Gene Expression Cold Spring Harbor: CSH Laboratory Press 181-299.
32. B.A. Kaufman, S.M. Newman, R.L. Hallberg, C.A. Slaughter, P.S. Perlman and R.A. Butow (2000) In organello formaldehyde crosslinking of proteins to mtDNA: identification of bifunctional proteins. Proc. Natl Acad. Sci. USA 97 7772-7777.
33. A. Kaut, H. Lange, K. Diekert, G. Kispal and R. Lill (2000) Isa1p is a component of the mitochondrial machinery for maturation of cellular iron-sulfur proteins and requires conserved cysteine residues for function. J. Biol. Chem. 275 15955-15961.
34. R. Kim, S. Saxena, D.M. Gordon, D. Pain and A. Dancis (2001) J-domain protein, Jac1p, of yeast mitochondria required for iron homeostasis and activity of Fe−S cluster proteins. J. Biol. Chem. 276 17524-17532.
35. G. Kispal, H. Steiner, D.A. Court, B. Rolinski and R. Lill (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.
36. G. Kispal, P. Csere, B. Guiard and R. Lill (1997) The ABC transporter Atm1p is required for mitochondrial iron homeostasis. FEBS Lett. 418 346-350.
37. G. Kispal, P. Csere, C. Prohl and R. Lill (1999) The mitochondrial proteins Atm1p and Nfs1p are required for biogenesis of cytosolic Fe/S proteins. EMBO J. 18 3981-3989.
38. I. Klein, B. Sarkadi and A. Varadi (1999) An inventory of the human ABC proteins. Biochem. Biophys. Res. Commun. 1461 237-262.
39. G.B. Kohlhaw (1988) Beta-isopropylmalate dehydrogenase from yeast. Methods Enzymol. 166 429-435.
40. G.B. Kohlhaw (1988) Isopropylmalate dehydratase from yeast. Methods Enzymol. 166 423-429.
41. R. Kranz, R. Lill, B. Goldman, G. Bonnard and S. Merchant (1998) Molecular mechanisms of cytochrome c biogenesis: three distinct systems. Mol. Microbiol. 29 383-396.
42. C. Krebs, J.N. Agar, A.D. Smith, J. Frazzon, D.R. Dean, B.H. Huynh and M.K. Johnson (2001) IscA, an alternate scaffold for Fe−S cluster biosynthesis. Biochemistry 40 14069-14080.
43. K.P. Künkele, P. Juin, C. Pompa, F.E. Nargang, J.P. Henry, W. Neupert, R. Lill and M. Thieffry (1998) The isolated complex of the translocase of the outer membrane of mitochondria. Characterization of the cation-selective and voltage-gated preprotein-conducting pore. J. Biol. Chem. 273 31032-31039.
44. S. Kushnir, E. Babiychuck, S. Storozhenko, M.W. Davey, J. Papenbrock, R. De Rycke, et al. (2001) A mutation of the mitochondrial ABC transporter Sta1 leads to dwarfism and chlorosis in the Arabidopsis mutant starik. Plant Cell 13 89-100.
45. H. Lange, G. Kispal and R. Lill (1999) Mechanism of iron transport to the site of heme synthesis inside yeast mitochondria. J. Biol. Chem. 274 18989-18996.
46. H. Lange, G. Kispal, A. Kaut and R. Lill (2000) A mitochondrial ferredoxin is essential for biogenesis of intra- and extra-mitochondrial Fe/S proteins. Proc. Natl Acad. Sci. USA. 97 1050-1055.
47. H. Lange, T. Lisowsky, J. Gerber, U. Mühlenhoff, G. Kispal and R. Lill (2001) An essential function of the mitochondrial sulfhydryl oxidase Erv1p/ALR in the maturation of cytosolic Fe/S proteins. EMBO Rep. 2 715-720.
48. T. Langer (2000) AAA proteases: cellular machines for degrading membrane proteins. Trends Biochem. Sci. 25 247-251.
49. J.E. Lee, G. Hofhaus and T. Lisowsky (2000) Erv1p from Saccharomyces cerevisiae is a FAD-linked sulfhydryl oxidase. FEBS Lett. 477 62-66.
50. J. Leighton and G. Schatz (1995) An ABC transporter in the mitochondrial innermembrane is required for normal growth of yeast. EMBO J. 14 188-195.
51. J. Li, S. Saxena, D. Pain and A. Dancis (2001) Adrenodoxin reductase homolog (Arh1p) of yeast mitochondria required for iron homeostasis. J. Biol. Chem. 276 1503-1509.
52. Z.S. Li, M. Szczypka, Y.P. Lu, D.J. Thiele and P.A. Rea (1996) The yeast cadmium factor protein (YCF1) is a vacuolar glutathione S-conjugate pump. J. Biol. Chem. 271 6509-6517.
53. R. Lill and G. Kispal (2000) Maturation of cellular Fe/S proteins: The essential function of mitochondria. Trends Biochem. Sci. 25 352-356.
54. R. Lill, K. Diekert, A. Kaut, H. Lange, W. Pelzer, C. Prohl and G. Kispal (1999) The essential role of mitochondria in the biogenesis of cellular iron-sulfur proteins. Biol. Chem. 380 1157-1166.
55. K.J. Linton and C.F. Higgins (1998) The Escherichia coli ATP-binding cassette (ABC) proteins. Mol. Microbiol. 28 5-13.
56. T. Lisowsky (1992) Dual function of a new nuclear gene for oxidative phosphorylation and vegetative growth in yeast. Mol. Gen. Genet. 232 58-64.
57. T. Lutz, B. Westermann, W. Neupert and J.M. Herrmann (2001) The mitochondrial proteins Ssq1 and Jac1 are required for the assembly of iron sulfur clusters in mitochondria. J. Mol. Biol. 307 815-825.
58. M. Mao, G. Fu, J.S. Wu, Q.H. Zhang, J. Zhou, L.X. Kan, et al. (1998) Identification of genes expressed in human CD34(+) hematopoietic stem/progenitor cells by expressed sequence tags and efficient full-length cDNA cloning. Proc. Natl Acad. Sci. USA 95 8175-8180.
59. N. Mitsuhashi, T. Miki, H. Senbongi, N. Yokoi, H. Yano, M. Miyazaki, et al. (2000) MTABC3, a novel mitochondrial ATP-binding cassette protein involved in iron homeostasis. J. Biol. Chem. 275 17536-17540.
60. U. Mühlenhoff and R. Lill (2000) Biogenesis of iron-sulfur proteins in eukaryotes: a novel task of mitochondria that is inherited from bacteria. Biochim. Biophys. Acta 1459 370-382.
61. D.R. Nelson, C.M. Felix and J.M. Swanson (1998) Highly conserved charge-pair networks in the mitochondrial carrier family. J. Mol. Biol. 277 285-308.
62. W. Neupert (1997) Protein import into mitochondria. Ann. Rev. Biochem. 66 861-915.
63. S. Ollagnier-de-Choudens, T. Mattioli, Y. Takahashi and M. Fontecave (2001) Iron-sulfur cluster assembly: characterization of IscA and evidence for a specific and functional complex with ferredoxin. J. Biol. Chem. 276 22604-22607.
64. D.F. Ortiz, T. Ruscitti, K.F. McCue and D.W. Ow (1995) Transport of metal-binding peptides by HMT1, a fission yeast ABC-type vacuolar membrane protein. J. Biol. Chem. 270 4721-4728.
65. M.D. Page, Y. Sambongi and S.J. Ferguson (1998) Contrasting roufes of c-type cytochrome assembly in mitochondria, chloroplasts and bacteria. Trends Biochem. Sci. 23 103-108.
66. L. Palmieri, M.J. Runswick, G. Fiermonte, J.E. Walker and F. Palmieri (2000) Yeast mitochondrial carriers: bacterial expression, biochemical identification and metabolic significance. J. Bioenerg. Biomemb. 32 67-77.
67. W. Pelzer, U. Mühlenhoff, K. Diekert, K. Siegmund, G. Kispal and R. Lill (2000) Mitochondrial Isa2p plays a crucial role in the maturation of cellular iron-sulfur proteins. FEBS Lett. 476 134-139.
68. N. Pfanner and A. Geissler (2001) Versatility of the mitochondrial protein import machinery. Nature Rev. Mol. Cell Biol. 2 339-349.
69. C. Prohl, G. Kispal and R. Lill (2000) Branched-chain amino acid transaminases of yeast Saccharomyces cerevisiae. Methods Enzymol. 324 365-375.
70. C. Prohl, W. Pelzer, K. Diekert, H. Kmita, T. Bedekovics, G. Kispal and R. Lill (2001) The yeast mitochondrial carrier Leu5p and its human homologue Graves' disease protein are required for accumulation of coenzyme A in the matrix. Mol. Cell Biol. 21 1089-1097.
71. Q. Ren and L. Thony-Meyer (2001) Physical interaction of CcmC with heme and the heme chaperone CcmE during cytochrome c maturation. J. Biol. Chem. 276 32591-32596.
72. M. Rep, J.M. van Dijl, K. Suda, G. Schatz, L.A. Grivell and C.K. Suzuki (1996) Promotion of mitochondrial membrane complex assembly by a proteolytically inactive yeast Lon. Science 274 103-106.
73. U. Ritz and B. Seliger (2001) The transporter associated with antigen processing (TAP): structural integrity, expression, function, and its clinical relevance. Mol. Med. 7 149-158.
74. A. Rötig, P. de Lonlay, D. Chretien, F. Foury, M. Koenig, D. Sidi, A. Munnich and P. Rustin (1997) Aconitase and mitochondrial iron-sulphur protein deficiency in Friedreich ataxia. Nat. Genet. 17 215-217.
75. R. Sanchez-Fernandez, T.G. Davies, J.O. Coleman and P.A. Rea (2001) The Arabidopsis thaliana ABC protein superfamily, a complete inventory. J. Biol. Chem. 276 30231-30244.
76. B. Schilke, C. Voisine, H. Beinert and E. Craig (1999) Evidence for a conserved system for iron metabolism in the mitochondria of Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA 96 10206-10211.
77. H. Schulz, H. Hennecke and L. Thony-Meyer (1998) Prototype of a heme chaperone essential for cytochrome c maturation. Science 281 1197-1200.
78. H. Schulz, R.A. Fabianek, E.C. Pellicioli, H. Hennecke and L. Thony-Meyer (1999) Heme transfer to the heme chaperone CcmE during cytochrome c maturation requires the CcmC protein, which may function independently of the ABC-transporter CcmAB. Proc. Natl Acad. Sci. USA 96 6462-6467.
79. H. Senbongi, F. Ling and T. Shibata (1999) A mutation in a mitochondrial ABC transporter results in mitochondrial dysfunction through oxidative damage of mitochondrial DNA. Mol. Gen. Genet. 262 426-436.
80. Y. Shimada, S. Okuno, A. Kawai, H. Shinomiya, A. Saito, M. Suzuki, et al. (1998) Cloning and chromosomal mapping of a novel ABC transporter gene (hABC7), a candidate for X-linked sideroblastic anemia with spinocerebellar ataxia. J. Hum. Genet. 43 115-122.
81. O.S. Shirihai, T. Gregory, C. Yu, S.H. Orkin and M.J. Weiss (2000) ABC-me: a novel mitochondrial transporter induced by GATA-1 during erythroid differentiation. EMBO J. 19 2492-2502.
82. J.J. Silberg, K.G. Hoff, T.L. Tapley and L.E. Vickery (2000) The Fe/S assembly protein IscU behaves as a substrate for the molecular chaperone Hsc66 from Escherichia coli. J. Biol. Chem. 276 1696-1700.
83. J. Strain, C.R. Lorenz, J. Bode, S. Garland, G.A. Smolen, D.T. Ta, L.E. Vickery and V.C. Culotta (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.
84. D. Taglicht and S. Michaelis (1998) Saccharomyces cerevisiae ABC proteins and their relevance to human health and disease. Methods Enzymol. 292 130-162.
85. L. Thony-Meyer (2000) Haem-polypeptide interactions during cytochrome c maturation. Biochim. Biophys. Acta 1459 316-324.
86. C. Voisine, Y.C. Cheng, M. Ohlson, B. Schilke, K. Hoff, H. Beinert, J. Marszalek and E.A. Craig (2001) Jac1, a mitochondrial J-type chaperone, is involved in the biogenesis of Fe/S clusters in Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA 98 1483-1488.
87. L. Young, K. Leonhard, T. Tatsuta, J. Trowsdale and T. Langer (2001) Role of the ABC transporter Mdl1 in peptide export from mitochondria. Science 291 2135-2138.
88. P. Yuvaniyama, J.N. Agar, V.L. Cash, M.K. Johnson and D.R. Dean (2000) NifS-directed assembly of a transient [2Fe−2S] cluster within the NifU protein. Proc. Natl Acad. Sci. USA 97 599-604.
89. F. Zhang, D.L. Hogue, L. Liu, C.L. Fisher, D. Hui, S. Childs and V. Ling (2000) M-ABC2, a new human mitochondrial ATP-binding cassette membrane protein. FEBS Lett. 478 89-94.
90. F. Zhang, W. Zhang, L. Liu, C.L. Fisher, D. Hui, S. Childs, K. Dorovini-Zis and V. Ling (2000) Characterization of ABCB9, an ATP binding cassette protein associated with lysosomes. J. Biol. Chem. 275 23287-23294.
91. L. Zheng, R.H. White, V.L. Cash, R.F. Jack and D.R. Dean (1993) Cysteine desulfurase acitivity indicates a role for NifS in metallocluster biosynthesis. Proc. Natl Acad. Sci. USA 90 2754-2758.
92. L. Zheng, R.H. White, V.L. Cash and D.R. Dean (1994) Mechanism for the desulfurization of l-cysteine catalyzed by the nifS gene product. Biochemistry 33 4714-4720.
93. L. Zheng, V.L. Cash, D.H. Flint and D.R. Dean (1998) Assembly of iron-sulfur clusters. Identification of an iscSUA-hscBA-fdx gene cluster from Azotobacter vinelandii. J. Biol. Chem. 273 13264-13272.