Characterization of the human HSC20, an unusual DnaJ type III protein, involved in iron-sulfur cluster biogenesis

Human Molecular Genetics

Volumn 19, Issue 19, 2010, Pages 3816-3834

  Uhrigshardt, Helge ^a,b   Singh, Anamika ^a   Kovtunovych, Gennadiy ^a   Ghosh, Manik ^a   Rouault, Tracey A ^a  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA HOMOLOG; FUNGAL PROTEIN; HUMAN HEAT SHOCK COGNATE PROTEIN 20; IRON SULFUR PROTEIN; PROTEIN DNAJ; PROTEIN JAC1P; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; GENE OVEREXPRESSION; HELA CELL; HUMAN; HUMAN CELL; MITOCHONDRION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; RNA INTERFERENCE; SEQUENCE ALIGNMENT;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; CELL PROLIFERATION; CYSTEINE; GENETIC COMPLEMENTATION TEST; HELA CELLS; HSP40 HEAT-SHOCK PROTEINS; HUMANS; IRON-SULFUR PROTEINS; MITOCHONDRIA; MOLECULAR CHAPERONES; MOLECULAR SEQUENCE DATA; ORGAN SPECIFICITY; OXIDATIVE STRESS; PARAQUAT; PROTEIN BINDING; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; TIME FACTORS;

BACTERIA (MICROORGANISMS); FUNGI; MAMMALIA;

EID: 77956513437     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddq301     Document Type: Article

References (95)

1. Walsh, P., Bursac, D., Law, Y.C., Cyr, D. and Lithgow, T. (2004) The J-protein family: modulating protein assembly, disassembly and translocation. EMBO Rep., 5, 567-571.
2. Qiu, X.B., Shao, Y.M., Miao, S. and Wang, L. (2006) The diversity of the DnaJ/Hsp40 family, the crucial partners for Hsp70 chaperones. Cell. Mol. Life Sci., 63, 2560-2570.
3. Genevaux, P., Georgopoulos, C. and Kelley, W.L. (2007) The Hsp70 chaperone machines of Escherichia coli: a paradigm for the repartition of chaperone functions. Mol. Microbiol., 66, 840-857.
4. Cheetham, M.E. and Caplan, A.J. (1998) Structure, function and evolution of DnaJ: conservation and adaptation of chaperone function. Cell Stress Chaperones, 3, 28-36.
5. Fan, C.Y., Lee, S. and Cyr, D.M. (2003) Mechanisms for regulation of Hsp70 function by Hsp40. Cell Stress Chaperones, 8, 309-316.
6. Hennessy, F., Nicoll, W.S., Zimmermann, R., Cheetham, M.E. and Blatch, G.L. (2005) Not all J domains are created equal: implications for the specificity of Hsp40-Hsp70 interactions. Protein Sci., 14, 1697-1709.
7. Craig, E.A., Huang, P., Aron, R. and Andrew, A. (2006) The diverse roles of J-proteins, the obligate Hsp70 co-chaperone. Rev. Physiol. Biochem. Pharmacol., 156, 1-21.
8. Kelley, W.L. (1998) The J-domain family and the recruitment of chaperone power. Trends Biochem. Sci., 23, 222-227.
9. Vickery, L.E. and Cupp-Vickery, J.R. (2007) Molecular chaperones HscA/Ssq1 and HscB/Jac1 and their roles in iron-sulfur protein maturation. Crit. Rev. Biochem. Mol. Biol., 42, 95-111.
10. Craig, E.A. and Marszalek, J. (2002) A specialized mitochondrial molecular chaperone system: a role in formation of Fe/S centers. Cell. Mol. Life Sci., 59, 1658-1665.
11. Rouault, T.A. and Klausner, R.D. (1996) Iron-sulfur clusters as biosensors of oxidants and iron. Trends Biochem. Sci., 21, 174-177.
12. Johnson, M.K. (1998) Iron-sulfur proteins: new roles for old clusters. Curr. Opin. Chem. Biol., 2, 173-181.
13. Beinert, H. (2000) Iron-sulfur proteins: ancient structures, still full of surprises. J. Biol. Inorg. Chem., 5, 2-15.
14. Kiley, P.J. and Beinert, H. (2003) The role of Fe-S proteins in sensing and regulation in bacteria. Curr. Opin. Microbiol., 6, 181-185.
15. Imlay, J.A. (2006) Iron-sulphur clusters and the problem with oxygen. Mol. Microbiol., 59, 1073-1082.
16. Lill, R. and Muhlenhoff, U. (2008) Maturation of iron-sulfur proteins in eukaryotes: mechanisms, connected processes, and diseases. Annu. Rev. Biochem., 77, 669-700.
17. Rouault, T.A. and Tong, W.H. (2008) Iron-sulfur cluster biogenesis and human disease. Trends Genet., 24, 398-407.
18. Johnson, D.C., Dean, D.R., Smith, A.D. and Johnson, M.K. (2005) Structure, function, and formation of biological iron-sulfur clusters. Annu. Rev. Biochem., 74, 247-281.
19. Lill, R. and Muhlenhoff, U. (2006) Iron-sulfur protein biogenesis in eukaryotes: components and mechanisms. Annu. Rev. Cell. Dev. Biol., 22, 457-486.
20. Lill,R., Dutkiewicz, R.,Elsasser, H.P.,Hausmann, A.,Netz, D.J., Pierik, A.J., Stehling, O., Urzica, E. and Muhlenhoff, U. (2006) Mechanisms of iron-sulfur protein maturation in mitochondria, cytosol and nucleus of eukaryotes. Biochim. Biophys. Acta, 1763, 652-667.
21. 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.
22. Schilke, B., Voisine, C., Beinert, H. and Craig, E. (1999) Evidence for a conserved system for iron metabolism in the mitochondria of Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA, 96, 10206-10211.
23. Voisine, C., Cheng, Y.C., Ohlson, M., Schilke, B., Hoff, K., Beinert, H., Marszalek, J. and Craig, E.A. (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.
24. Kim, R., Saxena, S., Gordon, D.M., Pain, D. and Dancis, A. (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.
25. Lutz, T., Westermann, B., Neupert, W. and Herrmann, J.M. (2001) The mitochondrial proteins Ssq1 and Jac1 are required for the assembly of iron sulfur clusters in mitochondria. J. Mol. Biol., 307, 815-825.
26. Hoff, K.G., Cupp-Vickery, J.R. and Vickery, L.E. (2003) Contributions of the LPPVK motif of the iron-sulfur template protein IscU to interactions with the Hsc66-Hsc20 chaperone system. J. Biol. Chem., 278, 37582-37589.
27. Tokumoto, U., Nomura, S., Minami, Y., Mihara, H., Kato, S., Kurihara, T., Esaki, N., Kanazawa, H., Matsubara, H. and Takahashi, Y. (2002) Network of protein-protein interactions among iron-sulfur cluster assembly proteins in Escherichia coli. J. Biochem., 131, 713-719.
28. Knieszner, H., Schilke,B.,Dutkiewicz,R., D'Silva, P.,Cheng, S.,Ohlson,M., Craig, E.A. andMarszalek, J. (2005)Compensation for a defective interaction of the hsp70 ssq1 with the mitochondrial Fe-S cluster scaffold isu. J. Biol. Chem., 280, 28966-28972.
29. Dutkiewicz, R., Schilke, B., Cheng, S., Knieszner, H., Craig, E.A. and Marszalek, J. (2004) Sequence-specific interaction between mitochondrial Fe-S scaffold protein Isu and Hsp70 Ssq1 is essential for their in vivo function. J. Biol. Chem., 279, 29167-29174.
30. Dutkiewicz, R., Schilke, B., Knieszner, H., Walter, W., Craig, E.A. and Marszalek, J. (2003) Ssq1, a mitochondrial Hsp70 involved in iron-sulfur (Fe/S) center biogenesis. Similarities to and differences from its bacterial counterpart. J. Biol. Chem., 278, 29719-29727.
31. Muhlenhoff, U., Gerber, J., Richhardt, N. and Lill, R. (2003) Components involved in assembly and dislocation of iron-sulfur clusters on the scaffold protein Isu1p. EMBO J., 22, 4815-4825.
32. Dutkiewicz, R., Marszalek, J., Schilke, B., Craig, E.A., Lill, R. and Muehlenhoff, U. (2006) The Hsp70 chaperone Ssq1p is dispensable for iron-sulfur cluster formation on the scaffold protein Isu1p. J. Biol. Chem., 281, 7801-7808.
33. Bonomi, F., Iametti, S., Ta, D. and Vickery, L.E. (2005) Multiple turnover transfer of [2Fe2S] clusters by the iron-sulfur cluster assembly scaffold proteins IscU and IscA. J. Biol. Chem., 280, 29513-29518.
34. Chandramouli, K. and Johnson, M.K. (2006) HscA and HscB stimulate [2Fe-2S] cluster transfer from IscU to apoferredoxin in an ATP-dependent reaction. Biochemistry, 45, 11087-11095.
35. Unciuleac, M.C., Chandramouli, K., Naik, S., Mayer, S., Huynh, B.H., Johnson, M.K. and Dean, D.R. (2007) In vitro activation of apo-aconitase using a [4Fe-4S] cluster-loaded form of the IscU [Fe-S] cluster scaffolding protein. Biochemistry, 46, 6812-6821.
36. Johnson, D.C., Unciuleac, M.C. and Dean, D.R. (2006) Controlled expression and functional analysis of iron-sulfur cluster biosynthetic components within Azotobacter vinelandii. J. Bacteriol., 188, 7551-7561.
37. Rouault, T.A. and Tong, W.H. (2005) Opinion: iron-sulphur cluster biogenesis and mitochondrial iron homeostasis. Nat. Rev. Mol. Cell. Biol., 6, 345-351.
38. Huynen, M.A., Snel, B., Bork, P. and Gibson, T.J. (2001) The phylogenetic distribution of frataxin indicates a role in iron-sulfur cluster protein assembly. Hum. Mol. Genet., 10, 2463-2468.
39. Schilke, B.,Williams, B., Knieszner, H., Pukszta, S., D'Silva, P., Craig, E.A. and Marszalek, J. (2006) Evolution of mitochondrial chaperones utilized in Fe-S cluster biogenesis. Curr. Biol., 16, 1660-1665.
40. Wadhwa, R., Taira, K. and Kaul, S.C. (2002) An Hsp70 family chaperone, mortalin/mthsp70/PBP74/Grp75: what, when, and where? Cell Stress Chaperones, 7, 309-316.
41. Deocaris, C.C., Kaul, S.C. and Wadhwa, R. (2006) On the brotherhood of the mitochondrial chaperones mortalin and heat shock protein 60. Cell Stress Chaperones, 11, 116-128.
42. Sun, G., Gargus, J.J., Ta, D.T. and Vickery, L.E. (2003) Identification of a novel candidate gene in the iron-sulfur pathway implicated in ataxia-susceptibility: human gene encoding HscB, a J-type co-chaperone. J. Hum. Genet., 48, 415-419.
43. Bitto, E., Bingman, C.A., Bittova, L., Kondrashov, D.A., Bannen, R.M., Fox, B.G., Markley, J.L. and Phillips, G.N.J. (2008) Structure of human J-type co-chaperone HscB reveals a tetracysteine metal-binding domain. J. Biol. Chem., 283, 30184-30192.
44. Cupp-Vickery, J.R. and Vickery, L.E. (2000) Crystal structure of Hsc20, a J-type Co-chaperone from Escherichia coli. J. Mol. Biol., 304, 835-845.
45. Hoff, K.G., Ta, D.T., Tapley, T.L., Silberg, J.J. and Vickery, L.E. (2002) Hsc66 substrate specificity is directed toward a discrete region of the iron-sulfur cluster template protein IscU. J. Biol. Chem., 277, 27353-27359.
46. Andrew, A.J., Dutkiewicz, R., Knieszner, H., Craig, E.A. and Marszalek, J. (2006) Characterization of the interaction between the J-protein Jac1p and the scaffold for Fe-S cluster biogenesis, Isu1p. J. Biol. Chem., 281, 14580-14587.
47. Fuzery, A.K., Tonelli, M., Ta, D.T., Cornilescu, G., Vickery, L.E. and Markley, J.L. (2008) Solution structure of the iron-sulfur cluster cochaperone HscB and its binding surface for the iron-sulfur assembly scaffold protein IscU. Biochemistry, 47, 9394-9404.
48. Tong, W.H. and Rouault, T. (2000) Distinct iron-sulfur cluster assembly complexes exist in the cytosol and mitochondria of human cells. EMBO J., 19, 5692-5700.
49. Li, K., Tong, W.H., Hughes, R.M. and Rouault, T.A. (2006) Roles of the mammalian cytosolic cysteine desulfurase, ISCS, and scaffold protein, ISCU, in iron-sulfur cluster assembly. J. Biol. Chem., 281, 12344-12351.
50. Tong, W.H. and Rouault, T.A. (2006) Functions of mitochondrial ISCU and cytosolic ISCU in mammalian iron-sulfur cluster biogenesis and iron homeostasis. Cell Metab., 3, 199-210.
51. Hoff, K.G., Silberg, J.J. and Vickery, L.E. (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.
52. Silberg, J.J. and Vickery, L.E. (2000) Kinetic characterization of the ATPase cycle of the molecular chaperone Hsc66 from Escherichia coli. J. Biol. Chem., 275, 7779-7786.
53. Ye, H., Jeong, S.Y., Ghosh,M.C., Kovtunovych, G., Silvestri, L., Ortillo,D., Uchida, N., Tisdale, J., Camaschella, C. and Rouault, T.A. (2010) Glutaredoxin 5 deficiency causes sideroblastic anemia by specifically impairing heme biosynthesis and depleting cytosolic iron in human erythroblasts. J. Clin. Invest., 120, 1749-1761.
54. Ye, H. and Rouault, T.A. (2010) Human iron-sulfur cluster assembly, cellular iron homeostasis and disease. Biochemistry, 49, 4945-4956.
55. Stehling, O., Elsasser, H.P., Bruckel, B., Muhlenhoff, U. and Lill, R. (2004) Iron-sulfur protein maturation in human cells: evidence for a function of frataxin. Hum. Mol. Genet., 13, 3007-3015.
56. Fosset, C., Chauveau, M.J., Guillon, B., Canal, F., Drapier, J.C. and Bouton, C. (2006) 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.
57. Song, D., Tu, Z. and Lee, F.S. (2009) Human ISCA1 interacts with IOP1/NARFL and functions in both cytosolic and mitochondrial iron-sulfur protein biogenesis. J. Biol. Chem., 284, 35297-35307.
58. Beinert, H., Kennedy, M.C. and Stout, D.C. (1996) Aconitase as iron-sulfur protein, enzyme, and iron-regulatory protein. Chem. Rev., 96, 2335-2373.
59. Kennedy, M.C., Emptage, M.H., Dreyer, J.L. and Beinert, H. (1983) The role of iron in the activation-inactivation of aconitase. J. Biol. Chem., 258, 11098-11105.
60. Brown, N.M.,Kennedy,M.C.,Antholine,W.E.,Eisenstein, R.S. andWalden, W.E. (2002) Detection of a [3Fe-4S] cluster intermediate of cytosolic aconitase in yeast expressing iron regulatory protein 1. Insights into the mechanism of Fe-S cluster cycling. J. Biol. Chem., 277, 7246-7254.
61. Jang, S. and Imlay, J.A. (2007) Micromolar intracellular hydrogen peroxide disrupts metabolism by damaging iron-sulfur enzymes. J. Biol. Chem., 282, 929-937.
62. Rouault, T.A. (2006) The role of iron regulatory proteins in mammalian iron homeostasis and disease. Nat. Chem. Biol., 2, 406-414.
63. Starzynski, R.R., Lipinski, P., Drapier, J.C., Diet, A., Smuda, E., Bartlomiejczyk, T., Gralak, M.A. and Kruszewski, M. (2005) Down-regulation of iron regulatory protein 1 activities and expression in superoxide dismutase 1 knock-out mice is not associated with alterations in iron metabolism. J. Biol. Chem., 280, 4207-4212.
64. Linke, K., Wolfram, T., Bussemer, J. and Jakob, U. (2003) The roles of the two zinc binding sites in DnaJ. J. Biol. Chem., 278, 44457-44466.
65. Martinez-Yamout, M., Legge, G.B., Zhang, O., Wright, P.E. and Dyson, H.J. (2000) Solution structure of the cysteine-rich domain of the Escherichia coli chaperone protein DnaJ. J. Mol. Biol., 300, 805-818.
66. Zhai, P., Stanworth, C., Liu, S. and Silberg, J.J. (2008) The human escort protein Hep binds to the ATPase domain of mitochondrial hsp70 and regulates ATP hydrolysis. J. Biol. Chem., 283, 26098-26106.
67. Morgan, B., Ang, S.K., Yan, G. and Lu, H. (2009) Zinc can play chaperone-like and inhibitor roles during import of mitochondrial small Tim proteins. J. Biol. Chem., 284, 6818-6825.
68. Sanford, R.A., Cole, J.R. and Tiedje, J.M. (2002) Characterization and description of Anaeromyxobacter dehalogenans gen. nov., sp. nov., an aryl-halorespiring facultative anaerobic myxobacterium. Appl. Environ. Microbiol., 68, 893-900.
69. Parro, V. and Moreno-Paz, M. (2003) Gene function analysis in environmental isolates: the nif regulon of the strict iron oxidizing bacterium Leptospirillum ferrooxidans. Proc. Natl Acad. Sci. USA, 100, 7883-7888.
70. 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.
71. Condo, I., Ventura, N., Malisan, F., Tomassini, B. and Testi, R. (2006) A pool of extramitochondrial frataxin that promotes cell survival. J. Biol. Chem., 281, 16750-16756.
72. Biederbick, A., Stehling, O., Rosser, R., Niggemeyer, B., Nakai, Y., Elsasser, H.P. and Lill, R. (2006) Role of human mitochondrial Nfs1 in cytosolic iron-sulfur protein biogenesis and iron regulation. Mol. Cell. Biol., 26, 5675-5687.
73. Cavadini, P., Biasiotto, G., Poli, M., Levi, S., Verardi, R., Zanella, I., Derosas, M., Ingrassia, R., Corrado, M. and Arosio, P. (2007) RNA silencing of the mitochondrial ABCB7 transporter in HeLa cells causes an iron-deficient phenotype with mitochondrial iron overload. Blood, 109, 3552-3559.
74. Andrew, A.J., Song, J.Y., Schilke, B. and Craig, E.A. (2008) Posttranslational regulation of the scaffold for Fe-S cluster biogenesis, Isu. Mol. Biol. Cell., 19, 5259-5266.
75. Tong, W.H., Jameson, G.N., Huynh, B.H. and Rouault, T.A. (2003) 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, 9762-9767.
76. Pearce, L.L., Martinez-Bosch, S., Manzano, E.L., Winnica, D.E., Epperly, M.W. and Peterson, J. (2009) The resistance of electron-transport chain Fe-S clusters to oxidative damage during the reaction of peroxynitrite with mitochondrial complex II and rat-heart pericardium. Nitric Oxide, 20, 135-142.
77. Barbet, F., Hakiki, S., Orssaud, C., Gerber, S., Perrault, I., Hanein, S., Ducroq, D., Dufier, J.L., Munnich, A., Kaplan, J. and Rozet, J.M. (2005) A third locus for dominant optic atrophy on chromosome 22q. J. Med. Genet., 42, electronic letter e1.
78. Bazylinski, D.A. and Frankel, R.B. (2004) Magnetosome formation in prokaryotes. Nat. Rev. Microbiol., 2, 217-230.
79. Hiraishi, A., Kishimoto, N., Kosako, Y., Wakao, N. and Tano, T. (1995) Phylogenetic position of the menaquinone-containing acidophilic chemo-organotroph Acidobacterium capsulatum. FEMS Microbiol. Lett., 132, 91-94.
80. Fons, R.D., Bogert, B.A. and Hegde, R.S. (2003) Substrate-specific function of the translocon-associated protein complex during translocation across the ER membrane. J. Cell. Biol., 160, 529-539.
81. Kim, H.Y., LaVaute, T., Iwai, K., Klausner, R.D. and Rouault, T.A. (1996) Identification of a conserved and functional iron-responsive element in the 5'UTR of mammalian mitochondrial aconitase. J. Biol. Chem., 271, 24226-24230.
82. Meyron-Holtz, E.G., Ghosh, M.C., Iwai, K., LaVaute, T., Brazzolotto, X., Berger, U.V., Land, W., Ollivierre-Wilson, H., Grinberg, A., Love, P. and Rouault, T.A. (2004) Genetic ablations of iron regulatory proteins 1 and 2 reveal why iron regulatory protein 2 dominates iron homeostasis. EMBO J., 23, 386-395.
83. Parvin, R. and Atkinson, D.E. (1968) Purification and some properties of yeast citrate synthase. Arch. Biochem. Biophys., 128, 528-533.
84. Munujos, P., Coll-Canti, J., Gonzalez-Sastre, F. and Gella, F.J. (1993) Assay of succinate dehydrogenase activity by a colorimetric-continuous method using iodonitrotetrazolium chloride as electron acceptor. Anal. Biochem., 212, 506-509.
85. Mosmann, T. (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods, 65, 55-63.
86. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680-685.
87. Altschul, S.F., Madden, T.L., Schaffer,A.A., Zhang, J., Zhang, Z., Miller,W. and Lipman, D.J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res., 25, 3389-3402.
88. Emanuelsson, O., Brunak, S., von Heijne, G. and Nielsen, H. (2007) Locating proteins in the cell using TargetP, SignalP and related tools. Nat. Protoc., 2, 953-971.
89. Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F. and Higgins, D.G. (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res., 25, 4876-4882.
90. Guex, N. and Peitsch, M.C. (1997) SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis, 18, 2714-2723.
91. Mattera, R., Tsai, Y.C., Weissman, A.M. and Bonifacino, J.S. (2006) The Rab5 guanine nucleotide exchange factor Rabex-5 binds ubiquitin (Ub) and functions as a Ub ligase through an atypical Ub-interacting motif and a zinc-finger domain. J. Biol. Chem., 281, 6874-6883.
92. Meriin, A.B., Gabai, V.L., Yaglom, J., Shifrin, V.I. and Sherman, M.Y. (1998) Proteasome inhibitors activate stress kinases and induce Hsp72. Diverse effects on apoptosis. J. Biol. Chem., 273, 6373-6379.
93. Bihlmaier, K., Mesecke, N., Kloeppel, C. and Herrmann, J.M. (2008) The disulfide relay of the intermembrane space of mitochondria: an oxygen-sensing system? Ann. N Y Acad. Sci., 1147, 293-302.
94. Xu, X.M., Lin, H., Latijnhouwers, M. and Moller, S.G. (2009) Dual localized AtHscB involved in iron sulfur protein biogenesis in Arabidopsis. PLoS One, 4, e7662.
95. Acquaviva, F., De Biase, I., Nezi, L., Ruggiero, G., Tatangelo, F., Pisano, C., Monticelli, A., Garbi, C., Acquaviva, A.M. and Cocozza, S. (2005) Extra-mitochondrial localisation of frataxin and its association with IscU1 during enterocyte-like differentiation of the human colon adenocarcinoma cell line Caco-2. J. Cell. Sci., 118, 3917-3924.