Modulation of the respiratory supercomplexes in yeast: Enhanced formation of cytochrome oxidase increases the stability and abundance of respiratory supercomplexes

Journal of Biological Chemistry

Volumn 289, Issue 9, 2014, Pages 6133-6141

  Cui, Tie Zhong ^a   Conte, Annalea ^b   Fox, Jennifer L ^a,c   Zara, Vincenzo ^b   Winge, Dennis R ^a  

^a UNIVERSITY OF UTAH HEALTH SCIENCES CENTER   (United States)

^b UNIVERSITY OF SALENTO   (Italy)

^c Department of Teacher Education and Department of Sociology and Anthropology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARDIOLIPINS; CYTOCHROME OXIDASE; GLOBULAR DOMAINS; OVER-EXPRESSION; STABILIZATION FACTORS; SUPERCOMPLEX; TRANSLOCASES; UBIQUINOL-CYTOCHROME C REDUCTASE;

PHOSPHOLIPIDS; YEAST;

STABILIZATION;

BCS1 PROTEIN; CARDIOLIPIN; CARRIER PROTEIN; CYTOCHROME C OXIDASE; IRON SULFUR PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BIOACCUMULATION; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ASSAY; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STABILITY; YEAST;

BIOENERGETICS/ELECTRON TRANSFER COMPLEX; CARDIOLIPIN; CYTOCHROME OXIDASE; MITOCHONDRIA; MITOCHONDRIAL METABOLISM;

ELECTRON TRANSPORT; ELECTRON TRANSPORT COMPLEX IV; ENZYME STABILITY; MUTATION; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84896813914     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.523688     Document Type: Article

References (46)

1. Winge, D. R. (2012) Sealing the mitochondrial respirasome. Mol. Cell. Biol. 32, 2647-2652
2. Heinemeyer, J., Braun, H. P., Boekema, E. J., and Kouril, R. (2007) A structural model of the cytochrome c reductase/oxidase supercomplex from yeast mitochondria. J. Biol. Chem. 282, 12240-12248 (Pubitemid 47100694)
3. Schägger, H., and von Jagow, G. (1991) Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form. Anal. Biochem. 199, 223-231
4. Schagger, H. (2001) Respiratory chain supercomplexes. IUBMB Life 52, 119-128
5. 2 revealed by single particle cryo-electron microscopy. J. Biol. Chem. 287, 23095-23103
6. Dudkina, N. V., Kudryashev, M., Stahlberg, H., and Boekema, E. J. (2011) Interaction of complexes I, III, and IV within the bovine respirasome by single particle cryoelectron tomography. Proc. Natl. Acad. Sci. U.S.A. 108, 15196-15200
7. 1-COX supercomplex and the TIM23 machinery. Mol. Biol. Cell 19, 3934-3943
8. Claypool, S. M., Oktay, Y., Boontheung, P., Loo, J. A., and Koehler, C. M. (2008) Cardiolipin defines the interactome of the major ADP/ATP carrier protein of the mitochondrial inner membrane. J. Cell Biol. 182, 937-950
9. Strogolova, V., Furness, A., Robb-McGrath, M., Garlich, J., and Stuart, R. A. (2012) Rcf1 and Rcf2, members of the hypoxia-induced gene 1 protein family, are critical components of the mitochondrial cytochrome bc1-cytochrome c oxidase supercomplex. Mol. Cell. Biol. 32, 1363-1373
10. Chen, Y. C., Taylor, E. B., Dephoure, N., Heo, J. M., Tonhato, A., Papandreou, I., Nath, N., Denko, N. C., Gygi, S. P., and Rutter, J. (2012) Identification of a protein mediating respiratory supercomplex stability. Cell Metab. 15, 348-360
11. Vukotic, M., Oeljeklaus, S., Wiese, S., Vögtle, F. N., Meisinger, C., Meyer, H. E., Zieseniss, A., Katschinski, D. M., Jans, D. C., Jakobs, S., Warscheid, B., Rehling, P., and Deckers, M. (2012) Rcf1 mediates cytochrome oxidase assembly and respirasome formation, revealing heterogeneity of the enzyme complex. Cell Metab. 15, 336-347
12. 1 and cytochrome c oxidase complexes associate to form a single supracomplex in yeast mitochondria. J. Biol. Chem. 275, 18093-18098
13. Pfeiffer, K., Gohil, V., Stuart, R. A., Hunte, C., Brandt, U., Greenberg, M. L., and Schägger, H. (2003) Cardiolipin stabilizes respiratory chain super-complexes. J. Biol. Chem. 278, 52873-52880 (Pubitemid 38035887)
14. Bazán, S., Mileykovskaya, E., Mallampalli, V. K., Heacock, P., Sparagna, G. C., and Dowhan, W. (2013) Cardiolipin-dependent reconstitution of respiratory supercomplexes from purified Saccharomyces cerevisiae complexes III and IV. J. Biol. Chem. 288, 401-411
15. 1 complex from bovine heart mitochondria. Science 277, 60-66
16. Iwata, S., Lee, J. W., Okada, K., Lee, J. K., Iwata, M., Rasmussen, B., Link, T. A., Ramaswamy, S., and Jap, B. K. (1998) Complete structure of the 11-subunit bovine mitochondrial cytochrome bc1 complex. Science 281, 64-71 (Pubitemid 28354043)
17. 1 subunits. FEBS J. 274, 4526-4539
18. 1 complex involves the formation of a large core structure in the inner mitochondrial membrane. FEBS J. 276, 1900-1914
19. Crivellone, M. D., Wu, M. A., and Tzagoloff, A. (1988) Assembly of the mitochondrial membrane system. Analysis of structural mutants of the yeast coenzyme QH2-cytochrome c reductase complex. J. Biol. Chem. 263, 14323-14333
20. 1 complex assembly in yeast mitochondria. J. Cell Biol. 199, 137-150
21. 1 complex assembly in Saccharomyces cerevisiae. Curr. Genet. 47, 203-212
22. Gruschke, S., Kehrein, K., Römpler, K., Gröne, K., Israel, L., Imhof, A., Herrmann, J. M., and Ott, M. (2011) Cbp3-Cbp6 interacts with the yeast mitochondrial ribosomal tunnel exit and promotes cytochrome b synthesis and assembly. J. Cell Biol. 193, 1101-1114
23. Cruciat, C. M., Hell, K., Fölsch, H., Neupert, W., and Stuart, R. A. (1999) Bcs1p, an AAA-family member, is a chaperone for the assembly of the cytochrome bc1 complex. EMBO J. 18, 5226-5233 (Pubitemid 29465573)
24. Wagener, N., Ackermann, M., Funes, S., and Neupert, W. (2011) A pathway of protein translocation in mitochondria mediated by the AAA-ATPase Bcs1. Mol. Cell 44, 191-202
25. Mühlenhoff, U., Richter, N., Pines, O., Pierik, A. J., and Lill, R. (2011) Specialized function of yeast Isa1 and Isa2 proteins in the maturation of mitochondrial [4Fe-4S] proteins. J. Biol. Chem. 286, 41205-41216
26. Atkinson, A., Khalimonchuk, O., Smith, P., Sabic, H., Eide, D., and Winge, D. R. (2010) Mzm1 influences a labile pool of mitochondrial zinc important for respiratory function. J. Biol. Chem. 285, 19450-19459
27. Atkinson, A., Smith, P., Fox, J. L., Cui, T. Z., Khalimonchuk, O., and Winge, D. R. (2011) The LYR protein Mzm1 functions in the insertion of the Rieske Fe/S protein in yeast mitochondria. Mol. Cell. Biol. 31, 3988-3996
28. Cui, T. Z., Smith, P. M., Fox, J. L., Khalimonchuk, O., and Winge, D. R. (2012) Late-stage maturation of the Rieske Fe/S protein: Mzm1 stabilizes Rip1 but does not facilitate its translocation by the AAA ATPase Bcs1. Mol. Cell. Biol. 32, 4400-4409
29. Pierrel, F., Khalimonchuk, O., Cobine, P. A., Bestwick, M., and Winge, D. R. (2008) Coa2 is an assembly factor for yeast cytochrome c oxidase biogenesis facilitating the maturation of Cox1. Mol. Cell. Biol. 28, 4927-4939
30. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254
31. Capaldi, R. A., Marusich, M. F., and Taanman, J.-W. (1995) Mammalian cytochrome c oxidase: characterization of enzyme and immunological detection of subunits in tissue extracts and whole cells. Methods Enzymol. 260, 117-132
32. Ferramosca, A., Conte, A., Burri, L., Berge, K., De Nuccio, F., Giudetti, A. M., and Zara, V. (2012) A krill oil supplemented diet suppresses hepatic steatosis in high-fat fed rats. PLoS ONE 7, e38797
33. 1 complex. Biochim. Biophys. Acta 1793, 89-96
34. Williams, S. L., Valnot, I., Rustin, P., and Taanman, J.-W. (2004) Cytochrome c oxidase subassemblies in fibroblast cultures from patients carrying mutations in COX10, SCO1 or SURF1. J. Biol. Chem. 279, 7462-7469 (Pubitemid 38294623)
35. Mick, D. U., Wagner, K., van der Laan, M., Frazier, A. E., Perschil, I., Pawlas, M., Meyer, H. E., Warscheid, B., and Rehling, P. (2007) Shy1 couples Cox1 translational regulation to cytochrome c oxidase assembly. EMBO J. 26, 4347-4358 (Pubitemid 47587664)
36. McStay, G. P., Su, C. H., Thomas, S. M., Xu, J. T., and Tzagoloff, A. (2013) Characterization of Cox1p assembly intermediates in Saccharomyces cerevisiae. J. Biol. Chem. 288, 26546-26556
37. McStay, G. P., Su, C. H., and Tzagoloff, A. (2013) Modular assembly of yeast cytochrome oxidase. Mol. Biol. Cell 24, 440-452
38. 1 complex in S. cerevisiae may be involved in facilitating stability of the subcomplex with the Qcr8 protein and cytochrome b. Arch. Biochem. Biophys. 393, 215-221
39. Lapuente-Brun, E., Moreno-Loshuertos, R., Acín-Pérez, R., Latorre-Pellicer, A., Colás, C., Balsa, E., Perales-Clemente, E., Quirós, P. M., Calvo, E., Rodríguez-Hernández, M. A., Navas, P., Cruz, R., Carracedo, Á., López-Otín, C., Pérez-Martos, A., Fernández-Silva, P., Fernández-Vizarra, E., and Enríquez, J. A. (2013) Supercomplex assembly determines electron flux in the mitochondrial electron transport chain. Science 340, 1567-1570
40. Zhang, M., Mileykovskaya, E., and Dowhan, W. (2002) Cardiolipin is required for supercomplex formation in the inner mitochondrial membrane. J. Biol. Chem. 277, 43553-43556 (Pubitemid 36157767)
41. Lange, C., Nett, J. H., Trumpower, B. L., and Hunte, C. (2001) Specific roles of protein-phospholipid interactions in the yeast cytochrome bc1 complex structure. EMBO J. 20, 6591-6600 (Pubitemid 33134190)
42. Shinzawa-Itoh, K., Aoyama, H., Muramoto, K., Terada, H., Kurauchi, T., Tadehara, Y., Yamasaki, A., Sugimura, T., Kurono, S., Tsujimoto, K., Mizushima, T., Yamashita, E., Tsukihara, T., and Yoshikawa, S. (2007) Structures and physiological roles of 13 integral lipids of bovine heart cytochrome c oxidase. EMBO J. 26, 1713-1725 (Pubitemid 46480942)
43. 1 complex catalysis and supercomplex formation. Biochim. Biophys. Acta 1787, 609-616
44. Zhang, M., Su, X., Mileykovskaya, E., Amoscato, A. A., and Dowhan, W. (2003) Cardiolipin is not required to maintain mitochondrial DNA stability or cell viability for Saccharomyces cerevisiae grown at elevated temperatures. J. Biol. Chem. 278, 35204-35210 (Pubitemid 37102286)
45. Weraarpachai, W., Sasarman, F., Nishimura, T., Antonicka, H., Auré, K., Rötig, A., Lombès, A., and Shoubridge, E. A. (2012) Mutations in C12orf62, a factor that couplesCOXI synthesis with cytochrome c oxidase assembly, cause fatal neonatal lactic acidosis. Am. J. Hum. Genet. 90, 142-151
46. 1 complex with its bound substrate cytochrome c. Proc. Natl. Acad. Sci. U.S.A. 99, 2800-2805