Mitochondrial complex III Rieske Fe-S protein processing and assembly

References

• Iwata S, Lee JW, Okada K, et al. Complete structure of the 11-subunit bovine mitochondrial cytochrome bc1 complex. Science. 1998;281:64–71. doi:10.1126/science.281.5373.64. PMID:9651245
   PubMed Web of Science ®Google Scholar
• Berry EA, Huang LS, Zhang Z, et al. Structure of the avian mitochondrial cytochrome bc1 complex. J Bioenerg Biomem. 1999;31:177–190. doi:10.1023/A:1005459426843. PMID:10591524
   PubMed Web of Science ®Google Scholar
• Zhang Z, Huang L, Shulmeister VM, et al. Electron transfer by domain movement in cytochrome bc1. Nature. 1998;392:677–684. doi:10.1038/33612. PMID:9565029
   PubMed Web of Science ®Google Scholar
• Hunte C, Koepke J, Lange C, et al. Structure at 2.3 A resolution of the cytochrome bc(1) complex from the yeast Saccharomyces cerevisiae co-crystallized with an antibody Fv fragment. Structure. 2000;8:669–684. doi:10.1016/S0969-2126(00)00152-0. PMID:10873857
   PubMed Web of Science ®Google Scholar
• Guo R, Zong S, Wu M, et al. Architecture of Human Mitochondrial Respiratory Megacomplex I2III2IV2. Cell. 2017;170:1247–1257, e12.
   PubMed Web of Science ®Google Scholar
• Cramer WA, Hasan SS, Yamashita E. The Q cycle of cytochrome bc complexes: a structure perspective. Biochim Biophys Acta. 2011;1807:788–802. doi:10.1016/j.bbabio.2011.02.006. PMID:21352799
   PubMed Web of Science ®Google Scholar
• Crofts AR, Holland JT, Victoria D, et al. The Q-cycle reviewed: How well does a monomeric mechanism of the bc(1) complex account for the function of a dimeric complex? Biochim Biophys Acta. 2008;1777:1001–1019.
   PubMed Web of Science ®Google Scholar
• Iwata M, Bjorkman J, Iwata S. Conformational change of the Rieske [2Fe-2S] protein in cytochrome bc1 complex. J Bioenerg Biomem. 1999;31:169–175. doi:10.1023/A:1005407410005. PMID:10591523
   PubMed Web of Science ®Google Scholar
• Zara V, Conte L, Trumpower BL. Biogenesis of the yeast cytochrome bc1 complex. Biochim Biophys Acta. 2009;1793:89–96.
   PubMed Web of Science ®Google Scholar
• Smith PM, Fox JL, Winge DR. Biogenesis of the cytochrome bc(1) complex and role of assembly factors. Biochim Biophys Acta. 2012;1817:276–286. doi:10.1016/j.bbabio.2011.11.009. PMID:22138626
   PubMed Web of Science ®Google Scholar
• Fernandez-Vizarra E, Zeviani M. Nuclear gene mutations as the cause of mitochondrial complex III deficiency. Front Genet. 2015;6:134. doi:10.3389/fgene.2015.00134. PMID:25914718
   PubMed Web of Science ®Google Scholar
• Gruschke S, Kehrein K, Rompler K, et al. Cbp3-Cbp6 interacts with the yeast mitochondrial ribosomal tunnel exit and promotes cytochrome b synthesis and assembly. J Cell Biol. 2011;193:1101–1114. doi:10.1083/jcb.201103132. PMID:21670217
   PubMed Web of Science ®Google Scholar
• Gruschke S, Rompler K, Hildenbeutel M, et al. The Cbp3-Cbp6 complex coordinates cytochrome b synthesis with bc(1) complex assembly in yeast mitochondria. J Cell Biol. 2012;199:137–150. doi:10.1083/jcb.201206040. PMID:23007649
   PubMed Web of Science ®Google Scholar
• Hildenbeutel M, Hegg EL, Stephan K, et al. Assembly factors monitor sequential hemylation of cytochrome b to regulate mitochondrial translation. J Cell Biol. 2014;205:511–524. doi:10.1083/jcb.201401009. PMID:24841564
   PubMed Web of Science ®Google Scholar
• Tucker EJ, Wanschers BF, Szklarczyk R, et al. Mutations in the UQCC1-Interacting Protein, UQCC2, Cause Human Complex III Deficiency Associated with Perturbed Cytochrome b Protein Expression. PLos Genet. 2013;9:e1004034. doi:10.1371/journal.pgen.1004034. PMID:24385928
   PubMed Web of Science ®Google Scholar
• Wanschers BF, Szklarczyk R, van den Brand MA, et al. A mutation in the human CBP4 ortholog UQCC3 impairs complex III assembly, activity and cytochrome b stability. Hum Mol Genet. 2014;23:6356–6365. doi:10.1093/hmg/ddu357. PMID:25008109
   PubMed Web of Science ®Google Scholar
• Wasilewski M, Chojnacka K, Chacinska A. Protein trafficking at the crossroads to mitochondria. Biochim Biophys Acta. 2017;1864:125–137. doi:10.1016/j.bbamcr.2016.10.019. PMID:27810356
   PubMed Web of Science ®Google Scholar
• Atkinson A, Smith P, Fox JL, et al. The LYR Protein Mzm1 Functions in the Insertion of the Rieske Fe/S Protein in Yeast Mitochondria. Mol Cell Biol. 2011;31:3988–3996. doi:10.1128/MCB.05673–11. PMID:21807901
   PubMed Web of Science ®Google Scholar
• Cui TZ, Smith PM, Fox JL, et al. 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. 2012;32:4400–4409. doi:10.1128/MCB.00441-12. PMID:22927643
   PubMed Web of Science ®Google Scholar
• Sanchez E, Lobo T, Fox JL, et al. LYRM7/MZM1L is a UQCRFS1 chaperone involved in the last steps of mitochondrial Complex III assembly in human cells. Biochim Biophys Acta. 2013;1827:285–293. doi:10.1016/j.bbabio.2012.11.003. PMID:23168492
   PubMed Web of Science ®Google Scholar
• Maio N, Kim KS, Singh A, et al. A single adaptable cochaperone-scaffold complex delivers nascent iron-sulfur clusters to mammalian respiratory chain complexes I-III. Cell Metab. 2017;25:945–953, e6. doi:10.1016/j.cmet.2017.03.010. PMID:28380382
   PubMed Web of Science ®Google Scholar
• Maio N, Singh A, Uhrigshardt H, et al. Cochaperone binding to LYR motifs confers specificity of iron sulfur cluster delivery. Cell Metab. 2014;19:445–457. doi:10.1016/j.cmet.2014.01.015. PMID:24606901
   PubMed Web of Science ®Google Scholar
• Cruciat CM, Hell K, Folsch H, et al. Bcs1p, an AAA-family member, is a chaperone for the assembly of the cytochrome bc(1) complex. Embo J. 1999;18:5226–5233. doi:10.1093/emboj/18.19.5226. PMID:10508156
   PubMed Web of Science ®Google Scholar
• Wagener N, Ackermann M, Funes S, et al. A Pathway of protein translocation in mitochondria mediated by the AAA-ATPase Bcs1. Mol Cell. 2011;44:191–202. doi:10.1016/j.molcel.2011.07.036. PMID:22017868
   PubMed Web of Science ®Google Scholar
• Fernandez-Vizarra E, Bugiani M, Goffrini P, et al. Impaired complex III assembly associated with BCS1L gene mutations in isolated mitochondrial encephalopathy. Hum Mol Genet. 2007;16:1241–1252. doi:10.1093/hmg/ddm072. PMID:17403714
   PubMed Web of Science ®Google Scholar
• Invernizzi F, Tigano M, Dallabona C, et al. A homozygous mutation in LYRM7/MZM1L associated with early onset encephalopathy, lactic acidosis, and severe reduction of mitochondrial complex III activity. Hum Mutat. 2013;34:1619–1622. doi:10.1002/humu.22441. PMID:24014394
   PubMed Web of Science ®Google Scholar
• Dallabona C, Abbink TE, Carrozzo R, et al. LYRM7 mutations cause a multifocal cavitating leukoencephalopathy with distinct MRI appearance. Brain. 2016;139:782–794. doi:10.1093/brain/awv392. PMID:26912632
   PubMed Web of Science ®Google Scholar
• Kremer LS, L'Hermitte-Stead C, Lesimple P, et al. Severe respiratory complex III defect prevents liver adaptation to prolonged fasting. J Hepatol. 2016;65:377–385. doi:10.1016/j.jhep.2016.04.017. PMID:27151179
   PubMed Web of Science ®Google Scholar
• Hempel M, Kremer LS, Tsiakas K, et al. LYRM7 – associated complex III deficiency: a clinical, molecular genetic, MR tomographic, and biochemical study. Mitochondrion. 2017. doi:10.1016/j.mito.2017.07.001. PMID:28694194
   PubMed Web of Science ®Google Scholar
• Ghezzi D, Arzuffi P, Zordan M, et al. Mutations in TTC19 cause mitochondrial complex III deficiency and neurological impairment in humans and flies. Nat Genet. 2011;43:259–263. doi:10.1038/ng.761. PMID:21278747
   PubMed Web of Science ®Google Scholar
• Bottani E, Cerutti R, Harbour ME, et al. TTC19 plays a husbandry role on UQCRFS1 turnover in the biogenesis of mitochondrial respiratory complex III. Mol Cell. 2017;67:96–105, e4. doi:10.1016/j.molcel.2017.06.001. PMID:28673544
   PubMed Web of Science ®Google Scholar
• Borchart U, Machleidt W, Schagger H, et al. Isolation and amino acid sequence of the 8 kDa DCCD-binding protein of beef heart ubiquinol:cytochrome c reductase. FEBS Lett. 1985;191:125–130. doi:10.1016/0014-5793(85)81007-3. PMID:2996928
   PubMed Web of Science ®Google Scholar
• Schagger H, Link TA, Engel WD, et al. Isolation of the eleven protein subunits of the bc1 complex grom beef heart. Methods Enzymol. 1986;126:224–237. doi:10.1016/S0076-6879(86)26024-3. PMID:2856130
   PubMed Web of Science ®Google Scholar
• Brandt U, Yu L, Yu CA, et al. 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. J Biol Chem. 1993;268:8387–8390.
   PubMed Web of Science ®Google Scholar
• Chacinska A, Koehler CM, Milenkovic D, et al. Importing mitochondrial proteins: machineries and mechanisms. Cell. 2009;138:628–644. doi:10.1016/j.cell.2009.08.005. PMID:19703392
   PubMed Web of Science ®Google Scholar
• Teixeira PF, Glaser E. Processing peptidases in mitochondria and chloroplasts. Biochim Biophys Acta. 2013;1833:360–370. doi:10.1016/j.bbamcr.2012.03.012. PMID:22495024
   PubMed Web of Science ®Google Scholar
• Hartl FU, Schmidt B, Wachter E, et al. Transport into mitochondria and intramitochondrial sorting of the Fe/S protein of ubiquinol-cytochrome c reductase. Cell. 1986;47:939–951. doi:10.1016/0092-8674(86)90809-3. PMID:3022944
   PubMed Web of Science ®Google Scholar
• Graham LA, Brandt U, Trumpower BL. Protease maturation of the Rieske iron-sulphur protein after its insertion into the mitochondrial cytochrome bc1 complex of Saccharomyces cerevisiae. Biochem Soc Trans. 1994;22:188–191. doi:10.1042/bst0220188. PMID:8206223
   PubMed Web of Science ®Google Scholar
• Glaser E, Dessi P. Integration of the mitochondrial-processing peptidase into the cytochrome bc1 complex in plants. J Bioenergy Biomem. 1999;31:259–274. doi:10.1023/A:1005475930477. PMID:10591532
   PubMed Web of Science ®Google Scholar
• Deng K, Zhang L, Kachurin AM, et al. Activation of a matrix processing peptidase from the crystalline cytochrome bc1 complex of bovine heart mitochondria. J Biol Chem. 1998;273:20752–20757.
   PubMed Web of Science ®Google Scholar
• Deng K, Shenoy SK, Tso SC, et al. Reconstitution of mitochondrial processing peptidase from the core proteins (subunits I and II) of bovine heart mitochondrial cytochrome bc(1) complex. J Biol Chem. 2001;276:6499–6505. doi:10.1074/jbc.M007128200. PMID:11073949
   PubMed Web of Science ®Google Scholar
• Berry EA, De Bari H, Huang LS. Unanswered questions about the structure of cytochrome bc1 complexes. Biochim Biophys Acta. 2013;1827:1258–1277. doi:10.1016/j.bbabio.2013.04.006. PMID:23624176
   PubMed Web of Science ®Google Scholar
• Berman HM, Westbrook J, Feng Z, et al. The protein data bank. Nucleic Acids Res. 2000;28:235–242. doi:10.1093/nar/28.1.235. PMID:10592235
   PubMed Web of Science ®Google Scholar
• Ardissone A, Granata T, Legati A, et al. Mitochondrial complex III deficiency caused by TTC19 defects: report of a novel mutation and review of literature. JIMD Rep. 2015;22:115–120. doi:10.1007/8904_2015_419. PMID:25772319
   PubMedGoogle Scholar
• Mordaunt DA, Jolley A, Balasubramaniam S, et al. Phenotypic variation of TTC19-deficient mitochondrial complex III deficiency: a case report and literature review. Am J Med Genet A. 2015;167:1330–1336. doi:10.1002/ajmg.a.36968. PMID:25899669
   PubMed Web of Science ®Google Scholar
• Schagger H. Respiratory chain supercomplexes of mitochondria and bacteria. Biochim Biophys Acta. 2002;1555:154–159.
   PubMed Web of Science ®Google Scholar
• Wai T, Saita S, Nolte H, et al. The membrane scaffold SLP2 anchors a proteolytic hub in mitochondria containing PARL and the i-AAA protease YME1L. EMBO Rep. 2016;17:1844–1856. doi:10.15252/embr.201642698. PMID:27737933
   PubMed Web of Science ®Google Scholar
• Aro EM, Suorsa M, Rokka A, et al. Dynamics of photosystem II: a proteomic approach to thylakoid protein complexes. J Exp Bot. 2005;56:347–356. doi:10.1093/jxb/eri041. PMID:15569703
   PubMed Web of Science ®Google Scholar
• De Las Rivas J, Andersson B, Barber J. Two sites of primary degradation of the D1-protein induced by acceptor or donor side photo-inhibition in photosystem II core complexes. FEBS Lett. 1992;301:246–252. doi:10.1016/0014-5793(92)80250-K. PMID:1577160
   PubMed Web of Science ®Google Scholar
• Komayama K, Khatoon M, Takenaka D, et al. Quality control of photosystem II: cleavage and aggregation of heat-damaged D1 protein in spinach thylakoids. Biochim Biophys Acta. 2007;1767:838–846. doi:10.1016/j.bbabio.2007.05.001. PMID:17543883
   PubMed Web of Science ®Google Scholar
• Lazarou M, McKenzie M, Ohtake A, et al. Analysis of the assembly profiles for mitochondrial- and nuclear-DNA-encoded subunits into complex I. Mol Cell Biol. 2007;27:4228–4237.
   PubMed Web of Science ®Google Scholar
• Karunadharma PP, Basisty N, Chiao YA, et al. Respiratory chain protein turnover rates in mice are highly heterogeneous but strikingly conserved across tissues, ages, and treatments. FASEB J. 2015;29:3582–3592. doi:10.1096/fj.15-272666. PMID:25977255
   PubMed Web of Science ®Google Scholar
• Gao X, Wen X, Esser L, et al. Structural basis for the quinone reduction in the bc1 complex: a comparative analysis of crystal structures of mitochondrial cytochrome bc1 with bound substrate and inhibitors at the Qi site. Biochemistry. 2003;42:9067–9080. doi:10.1021/bi0341814. PMID:12885240
   PubMed Web of Science ®Google Scholar
• Gao X, Wen X, Yu C, et al. The crystal structure of mitochondrial cytochrome bc1 in complex with famoxadone: the role of aromatic-aromatic interaction in inhibition. Biochemistry. 2002;41:11692–11702. doi:10.1021/bi026252p. PMID:12269811
   PubMed Web of Science ®Google Scholar
• Esser L, Gong X, Yang S, et al. Surface-modulated motion switch: capture and release of iron-sulfur protein in the cytochrome bc1 complex. PNAS. 2006;103:13045–13050. doi:10.1073/pnas.0601149103. PMID:16924113
   PubMed Web of Science ®Google Scholar
• Esser L, Quinn B, Li YF, et al. Crystallographic studies of quinol oxidation site inhibitors: a modified classification of inhibitors for the cytochrome bc(1) complex. J Mol Biol. 2004;341:281–302. doi:10.1016/j.jmb.2004.05.065. PMID:15312779
   PubMed Web of Science ®Google Scholar
• Huang LS, Cobessi D, Tung EY, et al. Binding of the respiratory chain inhibitor antimycin to the mitochondrial bc1 complex: a new crystal structure reveals an altered intramolecular hydrogen-bonding pattern. J Mol Biol. 2005;351:573–597. doi:10.1016/j.jmb.2005.05.053. PMID:16024040
   PubMed Web of Science ®Google Scholar
• Xia D, Yu CA, Kim H, et al. Crystal structure of the cytochrome bc1 complex from bovine heart mitochondria. Science. 1997;277:60–66. doi:10.1126/science.277.5322.60. PMID:9204897
   PubMed Web of Science ®Google Scholar
• Capper MJ, O'Neill PM, Fisher N, et al. Antimalarial 4(1H)-pyridones bind to the Qi site of cytochrome bc1. PNAS. 2015;112:755–760. doi:10.1073/pnas.1416611112. PMID:25564664
   PubMed Web of Science ®Google Scholar
• Esser L, Zhou F, Zhou Y, et al. Hydrogen bonding to the substrate is not required for Rieske Iron-Sulfur Protein Docking to the Quinol Oxidation Site of Complex III. J Biol Chem. 2016;291:25019–25031. doi:10.1074/jbc.M116.744391. PMID:27758861
   PubMed Web of Science ®Google Scholar
• McPhillie M, Zhou Y, El Bissati K, et al. New paradigms for understanding and step changes in treating active and chronic, persistent apicomplexan infections. Sci Rep. 2016;6:29179. doi:10.1038/srep29179. PMID:27412848
   PubMed Web of Science ®Google Scholar
• Berry EA, Huang LS, Lee DW, et al. Ascochlorin is a novel, specific inhibitor of the mitochondrial cytochrome bc1 complex. Biochim Biophys Acta. 2010;1797:360–370. doi:10.1016/j.bbabio.2009.12.003. PMID:20025846
   PubMed Web of Science ®Google Scholar
• Crowley PJ, Berry EA, Cromartie T, et al. The role of molecular modeling in the design of analogues of the fungicidal natural products crocacins A and D. Bioorg Med Chem. 2008;16:10345–10355. doi:10.1016/j.bmc.2008.10.030. PMID:18996700
   PubMed Web of Science ®Google Scholar
• Hao G-F, Yang, S.-G., Huang, W., et al. Rational design of highly potent and slow-binding cytochrome bc1 inhibitor as fungicide by computational substitution optimization. To be published 2015.
   Google Scholar
• Hao GF, Wang F, Li H, et al. Computational discovery of picomolar Q(o) site inhibitors of cytochrome bc1 complex. J Am Chem Soc. 2012;134:11168–11176. doi:10.1021/ja3001908. PMID:22690928
   PubMed Web of Science ®Google Scholar
• Huang L, Berry, E.A. Famoxadone and related inhibitors bind like methoxy acrylate inhibitors in the Qo site of the BC1 compl and fix the rieske iron-sulfur protein in a positio close to but distinct from that seen with stigmatellin and other "distal" Qo inhibitors. To be published 2010.
   Google Scholar