Proteasome Impairment Induces Recovery of Mitochondrial Membrane Potential and an Alternative Pathway of Mitochondrial Fusion

REFERENCES

• Hermann GJ, Shaw JM. 1998. Mitochondrial dynamics in yeast. Annu Rev Cell Dev Biol 14:265–303. http://dx.doi.org/10.1146/annurev.cellbio.14.1.265.
   PubMedGoogle Scholar
• Okamoto K, Shaw JM. 2005. Mitochondrial morphology and dynamics in yeast and multicellular eukaryotes. Annu Rev Genet 39:503–536. http://dx.doi.org/10.1146/annurev.genet.38.072902.093019.
   PubMed Web of Science ®Google Scholar
• Youle RJ, van der Bliek AM. 2012. Mitochondrial fission, fusion, and stress. Science 337:1062–1065. http://dx.doi.org/10.1126/science.1219855.
   PubMed Web of Science ®Google Scholar
• Hermann GJ, Thatcher JW, Mills JP, Hales KG, Fuller MT, Nunnari J, Shaw JM. 1998. Mitochondrial fusion in yeast requires the transmembrane GTPase Fzo1p. J Cell Biol 143:359–373. http://dx.doi.org/10.1083/jcb.143.2.359.
   PubMed Web of Science ®Google Scholar
• Wong ED, Wagner JA, Scott SV, Okreglak V, Holewinske TJ, Cassidy-Stone A, Nunnari J. 2003. The intramitochondrial dynamin-related GTPase, Mgm1p, is a component of a protein complex that mediates mitochondrial fusion. J Cell Biol 160:303–311. http://dx.doi.org/10.1083/jcb.200209015.
   PubMedGoogle Scholar
• Sesaki H, Jensen RE. 2004. Ugo1p links the Fzo1p and Mgm1p GTPases for mitochondrial fusion. J Biol Chem 279:28298–28303. http://dx.doi.org/10.1074/jbc.M401363200.
   PubMedGoogle Scholar
• Escobar-Henriques M, Anton F. 2013. Mechanistic perspective of mitochondrial fusion: tubulation vs. fragmentation. Biochim Biophys Acta 1833:162–175. http://dx.doi.org/10.1016/j.bbamcr.2012.07.016.
   PubMed Web of Science ®Google Scholar
• Rapaport D, Brunner M, Neupert W, Westermann B. 1998. Fzo1p is a mitochondrial outer membrane protein essential for the biogenesis of functional mitochondria in Saccharomyces cerevisiae. J Biol Chem 273:20150–20155. http://dx.doi.org/10.1074/jbc.273.32.20150.
   PubMed Web of Science ®Google Scholar
• Rinaldi T, Pick E, Gambadoro A, Zilli S, Maytal-Kivity V, Frontali L, Glickman MH. 2004. Participation of the proteasomal lid subunit Rpn11 in mitochondrial morphology and function is mapped to a distinct C-terminal domain. Biochem J 381:275–285. http://dx.doi.org/10.1042/BJ20040008.
   PubMedGoogle Scholar
• Rinaldi T, Hofmann L, Gambadoro A, Cossard R, Livnat-Levanon N, Glickman MH, Frontali L, Cedex O. 2008. Dissection of the carboxyl-terminal domain of the proteasomal subunit Rpn11 in maintenance of mitochondrial structure and function. Mol Biol Cell 19:1022–1031. http://dx.doi.org/10.1091/mbc.E07-07-0717.
   PubMed Web of Science ®Google Scholar
• Tar K, Dange T, Yang C, Yao Y, Bulteau A, Salcedo F, Braigen S, Finley D, Schmidt M, Fernandez Salcedo E, Bouillaud F. 2014. Proteasomes associated with the Blm10 activator protein antagonize mitochondrial fission through degradation of the fission protein Dnm1. J Biol Chem 289:12145–12156. http://dx.doi.org/10.1074/jbc.M114.554105.
   PubMedGoogle Scholar
• Cohen MM, Amiott EA, Day AR, Leboucher GP, Pryce EN, Glickman MH, McCaffery JM, Shaw JM, Weissman AM. 2011. Sequential requirements for the GTPase domain of the mitofusin Fzo1 and the ubiquitin ligase SCFMdm30 in mitochondrial outer membrane fusion. J Cell Sci 124:1403–1410. http://dx.doi.org/10.1242/jcs.079293.
   PubMed Web of Science ®Google Scholar
• Anton F, Fres JM, Schauss A, Pinson B, Praefcke GJK, Langer T, Escobar-Henriques M. 2011. Ugo1 and Mdm30 act sequentially during Fzo1-mediated mitochondrial outer membrane fusion. J Cell Sci 124:1126–1135. http://dx.doi.org/10.1242/jcs.073080.
   PubMedGoogle Scholar
• Anton F, Dittmar G, Langer T, Escobar-Henriques M. 2013. Two deubiquitylases act on mitofusin and regulate mitochondrial fusion along independent pathways. Mol Cell 49:487–498. http://dx.doi.org/10.1016/j.molcel.2012.12.003.
   PubMedGoogle Scholar
• Hershko A, Ciechanover A. 1998. The ubiquitin system. Annu Rev Biochem 67:425–479. http://dx.doi.org/10.1146/annurev.biochem.67.1.425.
   PubMed Web of Science ®Google Scholar
• Baumeister W, Walz J, Zühl F, Seemüller E. 1998. The proteasome: paradigm of a self-compartmentalizing protease. Cell 92:367–380. http://dx.doi.org/10.1016/S0092-8674(00)80929-0.
   PubMed Web of Science ®Google Scholar
• Qadota H, Ishii I, Fujiyama A, Ohya Y, Anraku Y. 1992. RHO gene products, putative small GTP-binding proteins, are important for activation of the CAL1/CDC43 gene product, a protein geranylgeranyltransferase in Saccharomyces cerevisiae. Yeast 8:735–741. http://dx.doi.org/10.1002/yea.320080906.
   PubMedGoogle Scholar
• Yashiroda H, Tanaka K. 2004. Hub1 is an essential ubiquitin-like protein without functioning as a typical modifier in fission yeast. Genes Cells 9:1189–1197. http://dx.doi.org/10.1111/j.1365-2443.2004.00807.x.
   PubMedGoogle Scholar
• Longtine MS, McKenzie A III, Demarini DJ, Shah NG, Wach A, Brachat A, Philippsen P, Pringle JR. 1998. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14:953–961.
   PubMed Web of Science ®Google Scholar
• Tong AHY, Boone C. 2007. High-throughput strain construction and systematic synthetic lethal screening in Saccharomyces cerevisiae. Methods Microbiol 36:369–386. http://dx.doi.org/10.1016/S0580-9517(06)36016-3.
   Google Scholar
• Okamoto K, Kondo-Okamoto N, Ohsumi Y. 2009. Mitochondria-anchored receptor Atg32 mediates degradation of mitochondria via selective autophagy. Dev Cell 17:87–97. http://dx.doi.org/10.1016/j.devcel.2009.06.013.
   PubMed Web of Science ®Google Scholar
• Yashiroda H, Mizushima T, Okamoto K, Kameyama T, Hayashi H, Kishimoto T, Niwa S, Kasahara M, Kurimoto E, Sakata E, Takagi K, Suzuki A, Hirano Y, Murata S, Kato K, Yamane T, Tanaka K. 2008. Crystal structure of a chaperone complex that contributes to the assembly of yeast 20S proteasomes. Nat Struct Mol Biol 15:228–236. http://dx.doi.org/10.1038/nsmb.1386.
   PubMedGoogle Scholar
• Gregg C, Kyryakov P, Titorenko VI. 24 August 2009. Purification of mitochondria from yeast cells. J Vis Exp http://dx.doi.org/10.3791/1417.
   Google Scholar
• Kimura Y, Koitabashi S, Kakizuka A, Fujita T. 2001. Initial process of polyglutamine aggregate formation in vivo. Genes Cells 6:887–897. http://dx.doi.org/10.1046/j.1365-2443.2001.00472.x.
   PubMedGoogle Scholar
• Ludovico P, Sansonetty F, Co M, Côrte-Real M. 2001. Assessment of mitochondrial membrane potential in yeast cell populations by flow cytometry. Microbiology 147:3335–3343. http://dx.doi.org/10.1099/00221287-147-12-3335.
   PubMedGoogle Scholar
• Velichutina I, Connerly PL, Arendt CS, Li X, Hochstrasser M. 2004. Plasticity in eucaryotic 20S proteasome ring assembly revealed by a subunit deletion in yeast. EMBO J 23:500–510. http://dx.doi.org/10.1038/sj.emboj.7600059.
   PubMedGoogle Scholar
• Glickman MH, Rubin DM, Coux O, Wefes I, Pfeifer G, Cjeka Z, Baumeister W, Fried VA, Finley D. 1998. A subcomplex of the proteasome regulatory particle required for ubiquitin-conjugate degradation and related to the COP9-signalosome and eIF3. Cell 94:615–623. http://dx.doi.org/10.1016/S0092-8674(00)81603-7.
   PubMed Web of Science ®Google Scholar
• Husnjak K, Elsasser S, Zhang N, Chen X, Randles L, Shi Y, Hofmann K, Walters KJ, Finley D, Dikic I. 2008. Proteasome subunit Rpn13 is a novel ubiquitin receptor. Nature 453:481–488. http://dx.doi.org/10.1038/nature06926.
   PubMed Web of Science ®Google Scholar
• Haarer B, Aggeli D, Viggiano S, Burke DJ, Amberg DC. 2011. Novel interactions between actin and the proteasome revealed by complex haploinsufficiency. PLoS Genet 7:e1002288. http://dx.doi.org/10.1371/journal.pgen.1002288.
   PubMedGoogle Scholar
• Chen XJ. 2004. Sal1p, a calcium-dependent carrier protein that suppresses an essential cellular function associated with the Aac2 isoform of ADP/ATP translocase in Saccharomyces cerevisiae. Genetics 167:607–617. http://dx.doi.org/10.1534/genetics.103.023655.
   PubMedGoogle Scholar
• Mokranjac D, Neupert W. 2009. Thirty years of protein translocation into mitochondria: unexpectedly complex and still puzzling. Biochim Biophys Acta 1793:33–41. http://dx.doi.org/10.1016/j.bbamcr.2008.06.021.
   PubMed Web of Science ®Google Scholar
• Chacinska A, Koehler CM, Milenkovic D, Lithgow T, Pfanner N. 2009. Importing mitochondrial proteins: machineries and mechanisms. Cell 138:628–644. http://dx.doi.org/10.1016/j.cell.2009.08.005.
   PubMed Web of Science ®Google Scholar
• Terziyska N, Lutz T, Kozany C, Mokranjac D, Mesecke N, Neupert W, Herrmann JM, Hell K. 2005. Mia40, a novel factor for protein import into the intermembrane space of mitochondria is able to bind metal ions. FEBS Lett 579:179–184. http://dx.doi.org/10.1016/j.febslet.2004.11.072.
   PubMed Web of Science ®Google Scholar
• Bragoszewski P, Gornicka AA, Sztolsztener ME, Chacinska A. 2013. The ubiquitin-proteasome system regulates mitochondrial intermembrane space proteins. Mol Cell Biol 33:2136–2148. http://dx.doi.org/10.1128/MCB.01579-12.
   PubMed Web of Science ®Google Scholar
• Sugioka R, Shimizu S, Tsujimoto Y. 2004. Fzo1, a protein involved in mitochondrial fusion, inhibits apoptosis. J Biol Chem 279:52726–52734. http://dx.doi.org/10.1074/jbc.M408910200.
   PubMed Web of Science ®Google Scholar
• Gerstenberger JP, Occhipinti P, Amy S, Gladfelter AS. 2012. Heterogeneity in mitochondrial morphology and membrane potential is independent of the nuclear division cycle in multinucleate fungal cells. Eukaryot Cell 11:353–367. http://dx.doi.org/10.1128/EC.05257-11.
   PubMedGoogle Scholar
• Thomas E, Roman E, Claypool S, Manzoor N, Pla J, Panwar SL. 2013. Mitochondria influence CDR1 efflux pump activity, Hog1-mediated oxidative stress pathway, iron homeostasis, and ergosterol levels in Candida albicans. Antimicrob Agents Chemother 57:5580–5599. http://dx.doi.org/10.1128/AAC.00889-13.
   PubMed Web of Science ®Google Scholar
• Chen XJ, Clark-Walker GD. 2000. The petite mutation in yeasts: 50 years on. Int Rev Cytol 194:197–238.
   PubMedGoogle Scholar
• Chen L. 1988. Mitochondrial membrane potential in living cells. Annu Rev Cell Biol 4:155–181. http://dx.doi.org/10.1146/annurev.cb.04.110188.001103.
   PubMedGoogle Scholar
• Allen S, Balabanidou V, Sideris DP, Lisowsky T, Tokatlidis K. 2005. Erv1 mediates the Mia40-dependent protein import pathway and provides a functional link to the respiratory chain by shuttling electrons to cytochrome c. J Mol Biol 353:937–944. http://dx.doi.org/10.1016/j.jmb.2005.08.049.
   PubMed Web of Science ®Google Scholar
• Dabir DV, Leverich EP, Kim S, Tsai FD, Hirasawa M, Knaff DB, Koehler CM. 2007. A role for cytochrome c and cytochrome c peroxidase in electron shuttling from Erv1. EMBO J 26:4801–4811. http://dx.doi.org/10.1038/sj.emboj.7601909.
   PubMedGoogle Scholar
• Bihlmaier K, Mesecke N, Terziyska N, Bien M, Hell K, Herrmann JM. 2007. The disulfide relay system of mitochondria is connected to the respiratory chain. J Cell Biol 179:389–395. http://dx.doi.org/10.1083/jcb.200707123.
   PubMed Web of Science ®Google Scholar
• Balaban RS, Nemoto S, Finkel T. 2005. Mitochondria, oxidants, and aging. Cell 120:483–495. http://dx.doi.org/10.1016/j.cell.2005.02.001.
   PubMed Web of Science ®Google Scholar
• Livnat-Levanon N, Kevei E, Kleifeld O, Krutauz D, Segref A, Rinaldi T, Erpapazoglou Z, Cohen M, Reis N, Hoppe T, Glickman MH. 2014. Reversible 26S proteasome disassembly upon mitochondrial stress. Cell Rep 7:1371–1380. http://dx.doi.org/10.1016/j.celrep.2014.04.030.
   PubMed Web of Science ®Google Scholar
• Brohem C, Massaro R, Tiago M, Marinho C, Jasiulionis M, de Almeida R, Rivelli D, Albuquerque R, de Oliveira T, de Melo Loureiro A, Okada S, Soengas M, de Moraes Barros S, Maria-Engler S. 2012. Proteasome inhibition and ROS generation by 4-nerolidylcatechol induces melanoma cell death. Pigment Cell Melanoma Res 25:354–369. http://dx.doi.org/10.1111/j.1755-148X.2012.00992.x.
   PubMed Web of Science ®Google Scholar
• Wang X, Yen J, Kaiser P, Huang L. 2010. Regulation of the 26S proteasome complex during oxidative stress. Sci Signal 3:ra88. http://dx.doi.org/10.1126/scisignal.2001232.
   PubMed Web of Science ®Google Scholar
• Mannhaupt G, Schnall R, Karpov V, Vetter I, Feldmann H. 1999. Rpn4p acts as a transcription factor by binding to PACE, a nonamer box found upstream of 26S proteasomal and other genes in yeast. FEBS Lett 450:27–34. http://dx.doi.org/10.1016/S0014-5793(99)00467-6.
   PubMed Web of Science ®Google Scholar
• Xie Y, Varshavsky A. 2001. RPN4 is a ligand, substrate, and transcriptional regulator of the 26S proteasome: a negative feedback circuit. Proc Natl Acad Sci USA 98:3056–3061. http://dx.doi.org/10.1073/pnas.071022298.
   PubMed Web of Science ®Google Scholar
• Kanki T, Klionsky DJ, Okamoto K. 2011. Mitochondria autophagy in yeast. Antioxid Redox Signal 14:1989–2001. http://dx.doi.org/10.1089/ars.2010.3762.
   PubMed Web of Science ®Google Scholar
• Priault M, Salin B, Schaeffer J, Vallette FM, di Rago J-P, Martinou J-C. 2005. Impairing the bioenergetic status and the biogenesis of mitochondria triggers mitophagy in yeast. Cell Death Differ 12:1613–1621. http://dx.doi.org/10.1038/sj.cdd.4401697.
   PubMed Web of Science ®Google Scholar
• Nowikovsky K, Reipert S, Devenish RJ, Schweyen RJ. 2007. Mdm38 protein depletion causes loss of mitochondrial K+/H+ exchange activity, osmotic swelling and mitophagy. Cell Death Differ 14:1647–1656. http://dx.doi.org/10.1038/sj.cdd.4402167.
   PubMed Web of Science ®Google Scholar
• Kanki T, Wang K, Cao Y, Baba M, Klionsky DJ. 2009. Atg32 is a mitochondrial protein that confers selectivity during mitophagy. Dev Cell 17:98–109. http://dx.doi.org/10.1016/j.devcel.2009.06.014.
   PubMed Web of Science ®Google Scholar
• Meeusen S, McCaffery JM, Nunnari J. 2004. Mitochondrial fusion intermediates revealed in vitro. Science 305:1747–1752. http://dx.doi.org/10.1126/science.1100612.
   PubMed Web of Science ®Google Scholar
• Wong ED, Wagner JA, Gorsich SW, McCaffery JM, Shaw JM, Nunnari J. 2000. The dynamin-related GTPase, Mgm1p, is an intermembrane space protein required for maintenance of fusion competent mitochondria. J Cell Biol 151:341–352. http://dx.doi.org/10.1083/jcb.151.2.341.
   PubMedGoogle Scholar
• Sesaki H, Southard SM, Yaffe MP, Jensen RE. 2003. Mgm1p, a dynamin-related GTPase, is essential for fusion of the mitochondrial outer membrane. Mol Biol Cell 14:2342–2356. http://dx.doi.org/10.1091/mbc.E02-12-0788.
   PubMed Web of Science ®Google Scholar
• Herlan M, Bornhövd C, Hell K, Neupert W, Reichert AS. 2004. Alternative topogenesis of Mgm1 and mitochondrial morphology depend on ATP and a functional import motor. J Cell Biol 165:167–173. http://dx.doi.org/10.1083/jcb.200403022.
   PubMedGoogle Scholar
• McQuibban GA, Saurya S, Freeman M. 2003. Mitochondrial membrane remodelling regulated by a conserved rhomboid protease. Nature 423:537–541. http://dx.doi.org/10.1038/nature01633.
   PubMedGoogle Scholar
• Harbauer AB, Zahedi RP, Sickmann A, Pfanner N, Meisinger C. 2014. The protein import machinery of mitochondria—a regulatory hub in metabolism, stress, and disease. Cell Metab 19:357–372. http://dx.doi.org/10.1016/j.cmet.2014.01.010.
   PubMed Web of Science ®Google Scholar
• Dunn CD, Lee MS, Spencer FA, Jensen RE. 2006. A genomewide screen for petite-negative yeast strains yields a new subunit of the i-AAA protease complex. Mol Biol Cell 17:213–226.
   PubMed Web of Science ®Google Scholar
• Badis G, Chan ET, van Bakel H, Pena-Castillo L, Tillo D, Tsui K, Carlson CD, Gossett AJ, Hasinoff MJ, Warren CL, Gebbia M, Talukder S, Yang A, Mnaimneh S, Terterov D, Coburn D, Li Yeo A, Yeo ZX, Clarke ND, Lieb JD, Ansari AZ, Nislow C, Hughes TR. 2008. A library of yeast transcription factor motifs reveals a widespread function for Rsc3 in targeting nucleosome exclusion at promoters. Mol Cell 32:878–887. http://dx.doi.org/10.1016/j.molcel.2008.11.020.
   PubMed Web of Science ®Google Scholar
• Zhu C, Byers KJ, McCord RP, Shi Z, Berger MF, Newburger DE, Saulrieta K, Smith Z, Shah MV, Radhakrishnan M, Philippakis AA, Hu Y, De Masi F, Pacek M, Rolfs A, Murthy T, Labaer J, Bulyk ML. 2009. High-resolution DNA-binding specificity analysis of yeast transcription factors. Genome Res 19:556–566. http://dx.doi.org/10.1101/gr.090233.108.
   PubMed Web of Science ®Google Scholar
• Shirozu R, Yashiroda H, Murata S. 2015. Identification of minimum Rpn4-responsive elements in genes related to proteasome functions. FEBS Lett 589:933–940. http://dx.doi.org/10.1016/j.febslet.2015.02.025.
   PubMed Web of Science ®Google Scholar
• Livnat-Levanon N, Glickman MH. 2011. Ubiquitin-proteasome system and mitochondria-reciprocity. Biochim Biophys Acta 1809:80–87. http://dx.doi.org/10.1016/j.bbagrm.2010.07.005.
   PubMed Web of Science ®Google Scholar
• Tatsuta T, Langer T. 2008. Quality control of mitochondria: protection against neurodegeneration and ageing. EMBO J 27:306–314. http://dx.doi.org/10.1038/sj.emboj.7601972.
   PubMed Web of Science ®Google Scholar
• Hoppins S, Nunnari J. 2009. The molecular mechanism of mitochondrial fusion. Biochim Biophys Acta 1793:20–26. http://dx.doi.org/10.1016/j.bbamcr.2008.07.005.
   PubMed Web of Science ®Google Scholar
• Chan DC. 2006. Mitochondrial fusion and fission in mammals. Annu Rev Cell Dev Biol 22:79–99. http://dx.doi.org/10.1146/annurev.cellbio.22.010305.104638.
   PubMed Web of Science ®Google Scholar
• Zick M, Duvezin-Caubet S, Schäfer A, Vogel F, Neupert W, Reichert AS. 2009. Distinct roles of the two isoforms of the dynamin-like GTPase Mgm1 in mitochondrial fusion. FEBS Lett 583:2237–2243. http://dx.doi.org/10.1016/j.febslet.2009.05.053.
   PubMedGoogle Scholar
• Santel A. 2006. Get the balance right: mitofusins roles in health and disease. Biochim Biophys Acta 1763:490–499. http://dx.doi.org/10.1016/j.bbamcr.2006.02.004.
   PubMedGoogle Scholar
• Archer SL. 2013. Mitochondrial dynamics—mitochondrial fission and fusion in human diseases. N Engl J Med 369:2236–2251. http://dx.doi.org/10.1056/NEJMra1215233.
   PubMed Web of Science ®Google Scholar
• Kondo-Okamoto N, Noda NN, Suzuki SW, Nakatogawa H, Takahashi I, Matsunami M, Hashimoto A, Inagaki F, Ohsumi Y, Okamoto K. 2012. Autophagy-related protein 32 acts as an autophagic degron and directly initiates mitophagy. J Biol Chem 287:10631–10638. http://dx.doi.org/10.1074/jbc.M111.299917.
   PubMed Web of Science ®Google Scholar
• Goldstein AL, McCusker JH. 1999. Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast 15:1541–1553.
   PubMed Web of Science ®Google Scholar
• Gietz R, Sugino A. 1988. New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites. Gene 74:527–534. http://dx.doi.org/10.1016/0378-1119(88)90185-0.
   PubMed Web of Science ®Google Scholar
• Sikorski R, Hieter P. 1989. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122:19–27.
   PubMed Web of Science ®Google Scholar