The Rieske iron-sulfur protein: Import and assembly into the cytochrome bc1 complex of yeast mitochondria

Bioinorganic Chemistry and Applications

Volumn 2011, Issue , 2011, Pages

  Zara, Vincenzo ^a   Conte, Laura ^a  

^a UNIVERSITY OF SALENTO   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 79959269374     PISSN: 15653633     EISSN: 1687479X     Source Type: Journal    
DOI: 10.1155/2011/363941     Document Type: Review

References (74)

1. Yang X. H., Trumpower B. L., Protonmotive Q cycle pathway of electron transfer and energy transduction in the three-subunit ubiquinol-cytochrome c oxidoreductase complex of Paracoccus denitrificans Journal of Biological Chemistry 1988 263 24 11962 11970
2. Trumpower B. L., Cytochrome bc1 complexes of microorganisms Microbiological Reviews 1990 54 2 101 129
3. Beckmann J. D., Ljungdahl P. O., Lopez J. L., Trumpower B. L., Isolation and characterization of the nuclear gene encoding the Rieske iron-sulfur protein (RIP1) from Saccharomyces cerevisiae Journal of Biological Chemistry 1987 262 18 8901 8909
4. Beckmann J. D., Ljungdahl P. O., Trumpower B. L., Mutational analysis of the mitochondrial Rieske iron-sulfur protein of Saccharomyces cerevisiae. I. Construction of a RIP1 deletion strain and isolation of temperature-sensitive mutants Journal of Biological Chemistry 1989 264 7 3713 3722 (Pubitemid 19072248)
5. Ljungdahl P. O., Beckmann J. D., Trumpower B. L., Mutational analysis of the mitochondrial Rieske iron-sulfur protein of Saccharomyces cerevisiae. II. Biochemical characterization of temperature-sensitive RIP1 mutations Journal of Biological Chemistry 1989 264 7 3723 3731 (Pubitemid 19072249)
6. Xia D., Yu C. A., Kim H., Xia J. Z., Kachurin A. M., Zhang L., Yu L., Deisenhofer J., Crystal structure of the cytochrome bc1 complex from bovine heart mitochondria Science 1997 277 5322 60 66 (Pubitemid 27450644)
7. Iwata S., Lee J. W., Okada K., Lee J. K., Iwata M., Rasmussen B., Link T. A., Ramaswamy S., Jap B. K., Complete structure of the 11-subunit bovine mitochondrial cytochrome bc1 complex Science 1998 281 5373 64 71 (Pubitemid 28354043)
8. Zhang Z., Huang L., Shulmeister V. M., Chi Y. I., Kim K. K., Hung L. W., Crofts A. R., Berry E. A., Kim S. H., Electron transfer by domain movement in cytochrome bc1 Nature 1998 392 6677 677 684 (Pubitemid 28207780)
9. Hunte C., Koepke J., Lange C., Rossmanith T., Michel H., Structure at 2.3 resolution of the cytochrome bc1 complex from the yeast Saccharomyces cerevisiae co-crystallized with an antibody Fv fragment Structure 2000 8 6 669 684 (Pubitemid 30409318)
10. Iwata S., Saynovits M., Link T. A., Michel H., Structure of a water soluble fragment of the Rieske iron-sulfur protein of the bovine heart mitochondrial cytochrome bc1 complex determined by MAD phasing at 1.5 resolution Structure 1996 4 5 567 579 (Pubitemid 126657550)
11. Gutierrez-Cirlos E. B., Merbitz-Zahradnik T., Trumpower B. L., Failure to insert the iron-sulfur cluster into the rieske iron-sulfur protein impairs both center N and center P of the cytochrome bc1 complex Journal of Biological Chemistry 2002 277 52 50703 50709 (Pubitemid 36042232)
12. Merbitz-Zahradnik T., Zwicker K., Nett J. H., Link T. A., Trumpower B. L., Elimination of the disulfide bridge in the Rieske iron-sulfur protein allows assembly of the [2Fe-2S] cluster into the Rieske protein but damages the ubiquinol oxidation site in the cytochrome bc1 complex Biochemistry 2003 42 46 13637 13645 (Pubitemid 37444914)
13. Miki T., Yu L., Yu C. A., Hematoporphyrin-promoted photoinactivation of mitochondrial ubiquinol-cytochrome c reductase: selective destruction of the histidine ligands of the iron-sulfur cluster and protective effect of ubiquinone Biochemistry 1991 30 1 230 238
14. Gurung B., Yu L., Xia D., Yu C. A., The iron-sulfur cluster of the rieske iron-sulfur protein functions as a proton-exiting gate in the cytochrome bc1 complex Journal of Biological Chemistry 2005 280 26 24895 24902 (Pubitemid 40934581)
15. Crofts A. R., Berry E. A., Structure and function of the cytochrome bc1 complex of mitochondria and photosynthetic bacteria Current Opinion in Structural Biology 1998 8 4 501 509 (Pubitemid 28409961)
16. Yu C. A., Xia D., Kim H., Deisenhofer J., Zhang L., Kachurin A. M., Yu L., Structural basis of functions of the mitochondrial cytochrome bc1 complex Biochimica et Biophysica Acta 1998 1365 1-2 151 158 (Pubitemid 29359252)
17. Beattie D. S., Wang Y., Obungu V. H., The role of various domains of the iron-sulfur protein in the assembly and activity of the cytochrome bc1 complex of yeast mitochondria Journal of Bioenergetics and Biomembranes 1999 31 3 215 224
18. Tian H., White S., Yu L., Yu C. A., Evidence for the head domain movement of the Rieske iron-sulfur protein in electron transfer reaction of the cytochrome bc1 complex Journal of Biological Chemistry 1999 274 11 7146 7152
19. Darrouzet E., Valkova-Valchanova M., Daldal F., Probing the role of the Fe-S subunit hinge region during Q(o) site catalysis in Rhodobacter capsulatus bc1 complex Biochemistry 2000 39 50 15475 15483 (Pubitemid 32002774)
20. Obungu V. H., Wang Y., Amyot S. M., Gocke C. B., Beattie D. S., Mutations in the tether region of the iron-sulfur protein affect the activity and assembly of the cytochrome bc1 complex of yeast mitochondria Biochimica et Biophysica Acta 2000 1457 1-2 36 44 (Pubitemid 30110728)
21. Xia K., Yu L., Yu C. A., Confirmation of the involvement of protein domain movement during the catalytic cycle of the cytochrome bc1 complex by the formation of an intersubunit disulfide bond between cytochrome b and the iron-sulfur protein Journal of Biological Chemistry 2000 275 49 38597 38604 (Pubitemid 32009188)
22. Ghosh M., Wang Y., Ebert C. E., Vadlamuri S., Beattie D. S., Substituting leucine for alanine-86 in the tether region of the iron-sulfur protein of the cytochrome bc1 complex affects the mobility of the [2Fe2S] domain Biochemistry 2001 40 2 327 335 (Pubitemid 32061980)
23. Darrouzet E., Valkova-Valchanova M., Moser C. C., Dutton P. L., Daldal F., Uncovering the [2Fe2S] domain movement in cytochrome bc1 and its implications for energy conversion Proceedings of the National Academy of Sciences of the United States of America 2000 97 9 4567 4572 (Pubitemid 30238598)
24. Nett J. H., Hunte C., Trumpower B. L., Changes to the length of the flexible linker region of the Rieske protein impair the interaction of ubiquinol with the cytochrome bc1 complex European Journal of Biochemistry 2000 267 18 5777 5782
25. Fisher N., Bourges I., Hill P., Brasseur G., Meunier B., Disruption of the interaction between the Rieske iron-sulfur protein and cytochrome b in the yeast bc1 complex owing to a human disease-associated mutation within cytochrome b European Journal of Biochemistry 2004 271 7 1292 1298 (Pubitemid 38519607)
26. Esser L., Gong X., Yang S., Yu L., Yu C. A., Xia D., Surface-modulated motion switch: capture and release of iron-sulfur protein in the cytochrome bc1 complex Proceedings of the National Academy of Sciences of the United States of America 2006 103 35 13045 13050 (Pubitemid 44338914)
27. Xia D., Esser L., Yu L., Yu C. A., Structural basis for the mechanism of electron bifurcation at the quinol oxidation site of the cytochrome bc1 complex Photosynthesis Research 2007 92 1 17 34 (Pubitemid 47101222)
28. Yu C. A., Cen X., Ma H. W., Yin Y., Yu L., Esser L., Xia D., Domain conformational switch of the iron-sulfur protein in cytochrome bc1 complex is induced by the electron transfer from cytochrome bL to bH Biochimica et Biophysica Acta 2008 1777 7-8 1038 1043
29. Neupert W., Herrmann J. M., Translocation of proteins into mitochondria Annual Review of Biochemistry 2007 76 723 749
30. Chacinska A., Koehler C. M., Milenkovic D., Lithgow T., Pfanner N., Importing mitochondrial proteins: machineries and mechanisms Cell 2009 138 4 628 644
31. Hartl F. U., Schmidt B., Wachter E., Weiss H., Neupert W., Transport into mitochondria and intramitochondrial sorting of the Fe/S protein of ubiquinol-cytochrome c reductase Cell 1986 47 6 939 951 (Pubitemid 17005067)
32. Fu W., Japa S., Beattie D. S., Import of the iron-sulfur protein of the cytochrome bc1 complex into yeast mitochondria Journal of Biological Chemistry 1990 265 27 16541 16547
33. Fu W., Beattie D. S., Assembly of the iron-sulfur protein into the cytochrome bc1 complex of yeast mitochondria Journal of Biological Chemistry 1991 266 24 16212 16218
34. Ramabadran R. S., Beattie D. S., Processing of the intermediate form of the iron-sulfur protein of the bc1 complex to the mature form after import into yeast mitochondria Archives of Biochemistry and Biophysics 1992 296 1 279 285
35. Brandt U., Yu L., Yu C. A., Trumpower B. L., The mitochondrial targeting presequence of the Rieske iron-sulfur protein is processed in a single step after insertion into the cytochrome bc1 complex in mammals and retained as a subunit in the complex Journal of Biological Chemistry 1993 268 12 8387 8390 (Pubitemid 23118608)
36. Nett J. H., Denke E., Trumpower B. L., Two-step processing is not essential for the import and assembly of functionally active iron-sulfur protein into the cytochrome bc1 complex in Saccharomyces cerevisiae Journal of Biological Chemistry 1997 272 4 2212 2217 (Pubitemid 27058502)
37. Graham L. A., Trumpower B. L., Mutational analysis of the mitochondrial Rieske iron-sulfur protein of Saccharomyces cerevisiae. III. Import, protease processing, and assembly into the cytochrome bc1 complex of iron-sulfur protein lacking the iron-sulfur cluster Journal of Biological Chemistry 1991 266 33 22485 22492 (Pubitemid 21908679)
38. Graham L. A., Brandt U., Sargent J. S., Trumpower B. L., Mutational analysis of assembly and function of the iron-sulfur protein of the cytochrome bc1 complex in Saccharomyces cerevisiae Journal of Bioenergetics and Biomembranes 1993 25 3 245 257 (Pubitemid 23177520)
39. Graham L. A., Brandt U., Trumpower B. L., Protease maturation of the Rieske iron-sulphur protein after its insertion into the mitochondrial cytochrome bc1 complex of Saccharomyces cerevisiae Biochemical Society Transactions 1994 22 1 188 191 (Pubitemid 24072416)
40. Nett J. H., Trumpower B. L., Intermediate length Rieske iron-sulfur protein is present and functionally active in the cytochrome bc1 complex of Saccharomyces cerevisiae Journal of Biological Chemistry 1999 274 14 9253 9257
41. Yang M., Trumpower B. L., Deletion of QCR6, the gene encoding subunit six of the mitochondrial cytochrome bc1 complex, blocks maturation of cytochrome c1, and causes temperature-sensitive petite growth in Saccharomyces cerevisiae Journal of Biological Chemistry 1994 269 2 1270 1275
42. Lill R., Mhlenhoff U., Maturation of iron-sulfur proteins in eukaryotes: mechanisms, connected processes, and diseases Annual Review of Biochemistry 2008 77 669 700
43. Lill R., Function and biogenesis of iron-sulphur proteins Nature 2009 460 7257 831 838
44. Mhlenhoff U., Gerber J., Richhardt N., Lill R., Components involved in assembly and dislocation of iron-sulfur clusters on the scaffold protein Isu1p The EMBO Journal 2003 22 18 4815 4825 (Pubitemid 37162917)
45. Dutkiewicz R., Marszalek J., Schilke B., Craig E. A., Lill R., Mhlenhoff U., The Hsp70 chaperone Ssq1p is dispensable for iron-sulfur cluster formation on the scaffold protein Isu1p Journal of Biological Chemistry 2006 281 12 7801 7808 (Pubitemid 43847394)
46. Gerber J., Mhlenhoff U., Lill R., An interaction between frataxin and Isu1/Nfs1 that is crucial for Fe/S cluster synthesis on Isu1 EMBO Reports 2003 4 9 906 911 (Pubitemid 37304409)
47. Bencze K. Z., Kondapalli K. C., Cook J. D., McMahon S., Milln-Pacheco C., Pastor N., Stemmler T. L., The structure and function of frataxin Critical Reviews in Biochemistry and Molecular Biology 2006 41 5 269 291 (Pubitemid 44261883)
48. Layer G., Ollagnier-de Choudens S., Sanakis Y., Fontecave M., Iron-sulfur cluster biosynthesis: characterization of Escherichia coli CYaY as an iron donor for the assembly of [2Fe-2S] clusters in the scaffold IscU Journal of Biological Chemistry 2006 281 24 16256 16263
49. Wang T., Craig E. A., Binding of yeast frataxin to the scaffold for Fe-S cluster biogenesis, Isu Journal of Biological Chemistry 2008 283 18 12674 12679
50. Craig E. A., Marszalek J., A specialized mitochondrial molecular chaperone system: a role in formation of Fe/S centers Cellular and Molecular Life Sciences 2002 59 10 1658 1665 (Pubitemid 35346969)
51. Rodrguez-Manzaneque M. T., Tamarit J., Bell G., Ros J., Herrero E., Grx5 is a mitochondrial glutaredoxin required for the activity of iron/sulfur enzymes Molecular Biology of the Cell 2002 13 4 1109 1121 (Pubitemid 34309609)
52. Dutkiewicz R., Schilke B., Knieszner H., Walter W., Craig E. A., Marszalek J., Ssq1, a mitochondrial Hsp70 involved in iron-sulfur (Fe/S) center biogenesis. Similarities to and differences from its bacterial counterpart Journal of Biological Chemistry 2003 278 32 29719 29727 (Pubitemid 36962358)
53. Dutkiewicz R., Schilke B., Cheng S., Knieszner H., Craig E. A., Marszalek J., Sequence-specific interaction between mitochondrial Fe-S scaffold protein Isu and Hsp70 Ssq1 is essential for their in vivo function Journal of Biological Chemistry 2004 279 28 29167 29174 (Pubitemid 38915790)
54. Andrew A. J., Dutkiewicz R., Knieszner H., Craig E. A., Marszalek J., Characterization of the interaction between the J-protein Jac1p and the scaffold for Fe-S cluster biogenesis, Isu1p Journal of Biological Chemistry 2006 281 21 14580 14587 (Pubitemid 43855161)
55. Vickery L. E., Cupp-Vickery J. R., Molecular chaperones HscA/Ssq1 and HscB/Jac1 and their roles in iron-sulfur protein maturation Critical Reviews in Biochemistry and Molecular Biology 2007 42 2 95 111 (Pubitemid 46598188)
56. Zara V., Conte L., Trumpower B. L., Biogenesis of the yeast cytochrome bc1 complex Biochimica et Biophysica Acta 2009 1793 1 89 96
57. Crivellone M. D., Wu M. A., Tzagoloff A., Assembly of the mitochondrial membrane system. Analysis of structural mutants of the yeast coenzyme QH2-cytochrome c reductase complex Journal of Biological Chemistry 1988 263 28 14323 14333
58. Berden J. A., Schoppink P. J., Grivell L. A., Palmieri F., Quagliariello E., A model for the assembly of ubiquinol: cytochrome c oxidoreductase in yeast Molecular Basis of Biomembrane Transport 1988 Amsterdam, The Netherlands Elsevier 195 208
59. Grivell L. A., Nucleo-mitochondrial interactions in yeast mitochondrial biogenesis European Journal of Biochemistry 1989 182 3 477 493 (Pubitemid 19169944)
60. Zara V., Palmisano I., Conte L., Trumpower B. L., Further insights into the assembly of the yeast cytochrome bc1 complex based on analysis of single and double deletion mutants lacking supernumerary subunits and cytochrome b European Journal of Biochemistry 2004 271 6 1209 1218 (Pubitemid 38373053)
61. Karlsson B., Hovmller S., Weiss H., Leonard K., Structural studies of cytochrome reductase. Subunit topography determined by electron microscopy of membrane crystals of a subcomplex Journal of Molecular Biology 1983 165 2 287 302
62. Brandt U., Uribe S., Schagger H., Trumpower B. L., Isolation and characterization of QCR10, the nuclear gene encoding the 8.5-kDa subunit 10 of the Saccharomyces cerevisiae cytochrome bc1 complex Journal of Biological Chemistry 1994 269 17 12947 12953 (Pubitemid 24202096)
63. Rep M., Grivell L. A., The role of protein degradation in mitochondrial function and biogenesis Current Genetics 1996 30 5 367 380 (Pubitemid 26402474)
64. Phillips J. D., Graham L. A., Trumpower B. L., Subunit 9 of the Saccharomyces cerevisiae cytochrome bc1 complex is required for insertion of EPR-detectable iron-sulfur cluster into the Rieske iron-sulfur protein Journal of Biological Chemistry 1993 268 16 11727 11736 (Pubitemid 23168123)
65. Schgger H., von Jagow G., Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form Analytical Biochemistry 1991 199 2 223 231
66. Zara V., Conte L., Trumpower B. L., Identification and characterization of cytochrome bc1 subcomplexes in mitochondria from yeast with single and double deletions of genes encoding cytochrome bc1 subunits FEBS Journal 2007 274 17 4526 4539 (Pubitemid 47301714)
67. Kim C. H., Balny C., King T. E., Role of the hinge protein in the electron transfer between cardiac cytochrome c1 and c. Equilibrium constants and kinetic probes Journal of Biological Chemistry 1987 262 17 8103 8108
68. Schoppink P. J., Hemrika W., Reynen J. M., Grivell L. A., Berden J. A., Yeast ubiquinol: cytochrome c oxidoreductase is still active after inactivation of the gene encoding the 17-kDa subunit VI European Journal of Biochemistry 1988 173 1 115 122
69. Zara V., Conte L., Trumpower B. L., Evidence that the assembly of the yeast cytochrome bc1 complex involves the formation of a large core structure in the inner mitochondrial membrane FEBS Journal 2009 276 7 1900 1914
70. Nobrega F. G., Nobrega M. P., Tzagoloff A., BCS1, a novel gene required for the expression of functional Rieske iron-sulfur protein in Saccharomyces cerevisiae The EMBO Journal 1992 11 11 3821 3829
71. Cruciat C. M., Hell K., Flsch H., Neupert W., Stuart R. A., Bcs1p, an AAA-family member, is a chaperone for the assembly of the cytochrome bc1 complex The EMBO Journal 1999 18 19 5226 5233 (Pubitemid 29465573)
72. Conte L., Trumpower B. L., Zara V., Bcs1p can rescue a large and productive cytochrome bc1 complex assembly intermediate in the inner membrane of yeast mitochondria Biochimica et Biophysica Acta 2011 1813 1 91 101
73. Cruciat C. M., Brunner S., Baumann F., Neupert W., Stuart R. A., The cytochrome bc1 and cytochrome c oxidase complexes associate to form a single supracomplex in yeast mitochondria Journal of Biological Chemistry 2000 275 24 18093 18098 (Pubitemid 30414758)
74. Schgger H., Pfeiffer K., Supercomplexes in the respiratory chains of yeast and mammalian mitochondria The EMBO Journal 2000 19 8 1777 1783 (Pubitemid 30204389)