Controlling quality and amount of mitochondria by mitophagy: insights into the role of ubiquitination and deubiquitination

References

Al Rawi, S., Louvet-Vallee, S., Djeddi, A., Sachse, M., Culetto, E., Hajjar, C., Boyd, L., Legouis, R., and Galy, V. (2011). Postfertilization autophagy of sperm organelles prevents paternal mitochondrial DNA transmission. Science 334, 1144–1147.10.1126/science.1211878Search in Google Scholar PubMed

Aoki, Y., Kanki, T., Hirota, Y., Kurihara, Y., Saigusa, T., Uchiumi, T., and Kang, D. (2011). Phosphorylation of serine 114 on Atg32 mediates mitophagy. Mol. Biol. Cell 22, 3206–3217.10.1091/mbc.e11-02-0145Search in Google Scholar

Ashrafi, G. and Schwarz, T.L. (2013). The pathways of mitophagy for quality control and clearance of mitochondria. Cell Death Differ. 20, 31–42.10.1038/cdd.2012.81Search in Google Scholar PubMed PubMed Central

Baxter, B.K., Abeliovich, H., Zhang, X., Stirling, A.G., Burlingame, A.L., and Goldfarb, D.S. (2005). Atg19p ubiquitination and the cytoplasm to vacuole trafficking pathway in yeast. J. Biol. Chem. 280, 39067–39076.10.1074/jbc.M508064200Search in Google Scholar PubMed

Bertholet, A.M., Delerue, T., Millet, A.M., Moulis, M.F., David, C., Daloyau, M., Arnaune-Pelloquin, L., Davezac, N., Mils, V., Miquel, M.C., et al. (2016). Mitochondrial fusion/fission dynamics in neurodegeneration and neuronal plasticity. Neurobiol. Dis. 90, 3–19.10.1016/j.nbd.2015.10.011Search in Google Scholar PubMed

Cao, Y., Cheong, H., Song, H., and Klionsky, D.J. (2008). In vivo reconstitution of autophagy in Saccharomyces cerevisiae. J. Cell Biol. 182, 703–713.10.1083/jcb.200801035Search in Google Scholar PubMed PubMed Central

Castrejon-Jimenez, N.S., Leyva-Paredes, K., Hernandez-Gonzalez, J.C., Luna-Herrera, J., and Garcia-Perez, B.E. (2015). The role of autophagy in bacterial infections. Biosci. Trends 9, 149–159.10.5582/bst.2015.01035Search in Google Scholar PubMed

Chinnadurai, G., Vijayalingam, S., and Gibson, S.B. (2008). BNIP3 subfamily BH3-only proteins: mitochondrial stress sensors in normal and pathological functions. Oncogene 27 (Suppl 1), S114–S127.10.1038/onc.2009.49Search in Google Scholar PubMed PubMed Central

Cohen, M., Stutz, F., Belgareh, N., Haguenauer-Tsapis, R., and Dargemont, C. (2003). Ubp3 requires a cofactor, Bre5, to specifically de-ubiquitinate the COPII protein, Sec23. Nat. Cell Biol. 5, 661–667.10.1038/ncb1003Search in Google Scholar PubMed

Cornelissen, T., Haddad, D., Wauters, F., Van Humbeeck, C., Mandemakers, W., Koentjoro, B., Sue, C., Gevaert, K., De Strooper, B., Verstreken, P., et al. (2014). The deubiquitinase USP15 antagonizes Parkin-mediated mitochondrial ubiquitination and mitophagy. Hum. Mol. Genet. 23, 5227–5242.10.1093/hmg/ddu244Search in Google Scholar PubMed PubMed Central

Cunningham, C.N., Baughman, J.M., Phu, L., Tea, J.S., Yu, C., Coons, M., Kirkpatrick, D.S., Bingol, B., and Corn, J.E. (2015). USP30 and parkin homeostatically regulate atypical ubiquitin chains on mitochondria. Nat. Cell Biol. 17, 160–169.10.1038/ncb3097Search in Google Scholar PubMed

Ding, W.X. and Yin, X.M. (2012). Mitophagy: mechanisms, pathophysiological roles, and analysis. Biol. Chem. 393, 547–564.10.1515/hsz-2012-0119Search in Google Scholar PubMed PubMed Central

Duvezin-Caubet, S., Jagasia, R., Wagener, J., Hofmann, S., Trifunovic, A., Hansson, A., Chomyn, A., Bauer, M.F., Attardi, G., Larsson, N.G., et al. (2006). Proteolytic processing of OPA1 links mitochondrial dysfunction to alterations in mitochondrial morphology. J. Biol. Chem. 281, 37972–37979.10.1074/jbc.M606059200Search in Google Scholar PubMed

Ehses, S., Raschke, I., Mancuso, G., Bernacchia, A., Geimer, S., Tondera, D., Martinou, J.C., Westermann, B., Rugarli, E.I., and Langer, T. (2009). Regulation of OPA1 processing and mitochondrial fusion by m-AAA protease isoenzymes and OMA1. J. Cell Biol. 187, 1023–1036.10.1083/jcb.200906084Search in Google Scholar PubMed PubMed Central

Eiyama, A. and Okamoto, K. (2015). PINK1/Parkin-mediated mitophagy in mammalian cells. Curr. Opin. Cell Biol. 33, 95–101.10.1016/j.ceb.2015.01.002Search in Google Scholar PubMed

Feng, Y., He, D., Yao, Z., and Klionsky, D.J. (2014). The machinery of macroautophagy. Cell Res. 24, 24–41.10.1038/cr.2013.168Search in Google Scholar PubMed PubMed Central

Fu, M., St-Pierre, P., Shankar, J., Wang, P.T., Joshi, B., and Nabi, I.R. (2013). Regulation of mitophagy by the Gp78 E3 ubiquitin ligase. Mol. Biol. Cell 24, 1153–1162.10.1091/mbc.e12-08-0607Search in Google Scholar PubMed PubMed Central

Geisler, S., Holmstrom, K.M., Skujat, D., Fiesel, F.C., Rothfuss, O.C., Kahle, P.J., and Springer, W. (2010). PINK1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1. Nat. Cell Biol. 12, 119–131.10.1038/ncb2012Search in Google Scholar PubMed

Gomes, L.C. and Scorrano, L. (2013). Mitochondrial morphology in mitophagy and macroautophagy. Biochim. Biophys. Acta 1833, 205–212.10.1016/j.bbamcr.2012.02.012Search in Google Scholar PubMed

Head, B., Griparic, L., Amiri, M., Gandre-Babbe, S., and van der Bliek, A.M. (2009). Inducible proteolytic inactivation of OPA1 mediated by the OMA1 protease in mammalian cells. J. Cell Biol. 187, 959–966.10.1083/jcb.200906083Search in Google Scholar PubMed PubMed Central

Heo, J.M., Ordureau, A., Paulo, J.A., Rinehart, J., and Harper, J.W. (2015). The PINK1-PARKIN mitochondrial ubiquitylation pathway drives a program of OPTN/NDP52 recruitment and TBK1 activation to promote mitophagy. Mol. Cell 60, 7–20.10.1016/j.molcel.2015.08.016Search in Google Scholar PubMed PubMed Central

Herlan, M., Bornhövd, C., Hell, K., Neupert, W., and Reichert, A.S. (2004). Alternative topogenesis of Mgm1 and mitochondrial morphology depend on ATP and a functional import motor. J. Cell Biol. 165, 167–173.10.1083/jcb.200403022Search in Google Scholar PubMed PubMed Central

Ishihara, N., Fujita, Y., Oka, T., and Mihara, K. (2006). Regulation of mitochondrial morphology through proteolytic cleavage of OPA1. EMBO J. 25, 2966–2977.10.1038/sj.emboj.7601184Search in Google Scholar PubMed PubMed Central

Jacomin, A.C., Bescond, A., Soleilhac, E., Gallet, B., Schoehn, G., Fauvarque, M.O., and Taillebourg, E. (2015). The deubiquitinating enzyme UBPY is required for lysosomal biogenesis and productive autophagy in Drosophila. PLoS One 10, e0143078.10.1371/journal.pone.0143078Search in Google Scholar PubMed PubMed Central

Kanki, T., Wang, K., Cao, Y., Baba, M., and Klionsky, D.J. (2009). Atg32 is a mitochondrial protein that confers selectivity during mitophagy. Dev. Cell 17, 98–109.10.1016/j.devcel.2009.06.014Search in Google Scholar PubMed PubMed Central

Kanki, T., Kurihara, Y., Jin, X., Goda, T., Ono, Y., Aihara, M., Hirota, Y., Saigusa, T., Aoki, Y., Uchiumi, T., et al. (2013). Casein kinase 2 is essential for mitophagy. EMBO Rep. 14, 788–794.10.1038/embor.2013.114Search in Google Scholar PubMed PubMed Central

Kaushik, S. and Cuervo, A.M. (2012). Chaperone-mediated autophagy: a unique way to enter the lysosome world. Trends Cell Biol. 22, 407–417.10.1016/j.tcb.2012.05.006Search in Google Scholar PubMed PubMed Central

Kikuma, T. and Kitamoto, K. (2011). Analysis of autophagy in Aspergillus oryzae by disruption of Aoatg13, Aoatg4, and Aoatg15 genes. FEMS Microbiol. Lett. 316, 61–69.10.1111/j.1574-6968.2010.02192.xSearch in Google Scholar PubMed

Klionsky, D.J. and Emr, S.D. (2000). Autophagy as a regulated pathway of cellular degradation. Science 290, 1717–1721.10.1126/science.290.5497.1717Search in Google Scholar PubMed PubMed Central

Komander, D., Clague, M.J., and Urbe, S. (2009). Breaking the chains: structure and function of the deubiquitinases. Nat. Rev. Mol. Cell Biol. 10, 550–563.10.1038/nrm2731Search in Google Scholar PubMed

Kotoulas, O.B., Kalamidas, S.A., and Kondomerkos, D.J. (2006). Glycogen autophagy in glucose homeostasis. Pathol. Res. Pract. 202, 631–638.10.1016/j.prp.2006.04.001Search in Google Scholar PubMed

Kovacs, A.L. and Zhang, H. (2010). Role of autophagy in Caenorhabditis elegans. FEBS Lett. 584, 1335–1341.10.1016/j.febslet.2010.02.002Search in Google Scholar PubMed

Kraft, C., Deplazes, A., Sohrmann, M., and Peter, M. (2008). Mature ribosomes are selectively degraded upon starvation by an autophagy pathway requiring the Ubp3p/Bre5p ubiquitin protease. Nat. Cell Biol. 10, 602–610.10.1038/ncb1723Search in Google Scholar PubMed

Lazarou, M., Jin, S.M., Kane, L.A., and Youle, R.J. (2012). Role of PINK1 binding to the TOM complex and alternate intracellular membranes in recruitment and activation of the E3 ligase Parkin. Dev. Cell 22, 320–333.10.1016/j.devcel.2011.12.014Search in Google Scholar PubMed PubMed Central

Lazarou, M., Narendra, D.P., Jin, S.M., Tekle, E., Banerjee, S., and Youle, R.J. (2013). PINK1 drives Parkin self-association and HECT-like E3 activity upstream of mitochondrial binding. J. Cell Biol. 200, 163–172.10.1083/jcb.201210111Search in Google Scholar PubMed PubMed Central

Lemasters, J.J. (2005). Selective mitochondrial autophagy, or mitophagy, as a targeted defense against oxidative stress, mitochondrial dysfunction, and aging. Rejuvenation Res. 8, 3–5.10.1089/rej.2005.8.3Search in Google Scholar PubMed

Li, K., Zhao, K., Ossareh-Nazari, B., Da, G., Dargemont, C., and Marmorstein, R. (2005). Structural basis for interaction between the Ubp3 deubiquitinating enzyme and its Bre5 cofactor. J. Biol. Chem. 280, 29176–29185.10.1074/jbc.M502975200Search in Google Scholar PubMed

Lippai, M. and Low, P. (2014). The role of the selective adaptor p62 and ubiquitin-like proteins in autophagy. Biomed. Res. Int. 2014, 832704.10.1155/2014/832704Search in Google Scholar PubMed PubMed Central

Liu, L., Feng, D., Chen, G., Chen, M., Zheng, Q., Song, P., Ma, Q., Zhu, C., Wang, R., Qi, W., et al. (2012). Mitochondrial outer-membrane protein FUNDC1 mediates hypoxia-induced mitophagy in mammalian cells. Nat. Cell Biol. 14, 177–185.10.1038/ncb2422Search in Google Scholar PubMed

Margineantu, D.H., Emerson, C.B., Diaz, D., and Hockenbery, D.M. (2007). Hsp90 inhibition decreases mitochondrial protein turnover. PLoS One 2, e1066.10.1371/journal.pone.0001066Search in Google Scholar PubMed PubMed Central

Mehrpour, M., Esclatine, A., Beau, I., and Codogno, P. (2010). Overview of macroautophagy regulation in mammalian cells. Cell Res. 20, 748–762.10.1038/cr.2010.82Search in Google Scholar PubMed

Mendl, N., Occhipinti, A., Muller, M., Wild, P., Dikic, I., and Reichert, A.S. (2011). Mitophagy in yeast is independent of mitochondrial fission and requires the stress response gene WHI2. J. Cell Sci. 124, 1339–1350.10.1242/jcs.076406Search in Google Scholar PubMed

Mulakkal, N.C., Nagy, P., Takats, S., Tusco, R., Juhasz, G., and Nezis, I.P. (2014). Autophagy in Drosophila: from historical studies to current knowledge. Biomed. Res. Int. 2014, 1–24.10.1155/2014/273473Search in Google Scholar PubMed PubMed Central

Müller, M., Kotter, P., Behrendt, C., Walter, E., Scheckhuber, C.Q., Entian, K.D., and Reichert, A.S. (2015a). Synthetic quantitative array technology identifies the Ubp3-Bre5 deubiquitinase complex as a negative regulator of mitophagy. Cell Rep 10, 1215–1225.10.1016/j.celrep.2015.01.044Search in Google Scholar PubMed

Müller, M., Lu, K., and Reichert, A.S. (2015b). Mitophagy and mitochondrial dynamics in Saccharomyces cerevisiae. Biochim. Biophys. Acta 1853, 2766–2774.10.1016/j.bbamcr.2015.02.024Search in Google Scholar PubMed

Murakawa, T., Yamaguchi, O., Hashimoto, A., Hikoso, S., Takeda, T., Oka, T., Yasui, H., Ueda, H., Akazawa, Y., Nakayama, H., et al. (2015). Bcl-2-like protein 13 is a mammalian Atg32 homologue that mediates mitophagy and mitochondrial fragmentation. Nat. Commun. 6, 7527.10.1038/ncomms8527Search in Google Scholar PubMed PubMed Central

Narendra, D., Tanaka, A., Suen, D.F., and Youle, R.J. (2008). Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J. Cell Biol. 183, 795–803.10.1083/jcb.200809125Search in Google Scholar PubMed PubMed Central

Narendra, D., Kane, L.A., Hauser, D.N., Fearnley, I.M., and Youle, R.J. (2010). p62/SQSTM1 is required for Parkin-induced mitochondrial clustering but not mitophagy; VDAC1 is dispensable for both. Autophagy 6, 1090–1106.10.4161/auto.6.8.13426Search in Google Scholar PubMed PubMed Central

Noda, N.N., Kumeta, H., Nakatogawa, H., Satoo, K., Adachi, W., Ishii, J., Fujioka, Y., Ohsumi, Y., and Inagaki, F. (2008). Structural basis of target recognition by Atg8/LC3 during selective autophagy. Genes Cells 13, 1211–1218.10.1111/j.1365-2443.2008.01238.xSearch in Google Scholar PubMed

Novak, I., Kirkin, V., McEwan, D.G., Zhang, J., Wild, P., Rozenknop, A., Rogov, V., Lohr, F., Popovic, D., Occhipinti, A., et al. (2010). Nix is a selective autophagy receptor for mitochondrial clearance. EMBO Rep. 11, 45–51.10.1038/embor.2009.256Search in Google Scholar PubMed PubMed Central

Nowikovsky, K., Reipert, S., Devenish, R.J., and Schweyen, R.J. (2007). Mdm38 protein depletion causes loss of mitochondrial K⁺/H⁺ exchange activity, osmotic swelling and mitophagy. Cell Death Differ. 14, 1647–1656.10.1038/sj.cdd.4402167Search in Google Scholar PubMed

Okamoto, K., Kondo-Okamoto, N., and Ohsumi, Y. (2009). Mitochondria-anchored receptor Atg32 mediates degradation of mitochondria via selective autophagy. Dev. Cell 17, 87–97.10.1016/j.devcel.2009.06.013Search in Google Scholar PubMed

Orvedahl, A., Sumpter, R., Jr., Xiao, G., Ng, A., Zou, Z., Tang, Y., Narimatsu, M., Gilpin, C., Sun, Q., Roth, M., et al. (2011). Image-based genome-wide siRNA screen identifies selective autophagy factors. Nature 480, 113–117.10.1038/nature10546Search in Google Scholar PubMed PubMed Central

Palikaras, K., Lionaki, E., and Tavernarakis, N. (2015). Interfacing mitochondrial biogenesis and elimination to enhance host pathogen defense and longevity. Worm 4, e1071763.10.1080/21624054.2015.1071763Search in Google Scholar PubMed PubMed Central

Papaevgeniou, N. and Chondrogianni, N. (2014). The ubiquitin proteasome system in Caenorhabditis elegans and its regulation. Redox Biol. 2, 333–347.10.1016/j.redox.2014.01.007Search in Google Scholar PubMed PubMed Central

Pereira, C., Costa, V., Martins, L.M., and Saraiva, L. (2015). A yeast model of the Parkinson’s disease-associated protein Parkin. Exp. Cell Res. 333, 73–79.10.1016/j.yexcr.2015.02.018Search in Google Scholar PubMed

Pernas, L. and Scorrano, L. (2015). Mito-morphosis: mitochondrial fusion, fission, and cristae remodeling as key mediators of cellular function. Annu. Rev. Physiol. 78, 505–531.10.1146/annurev-physiol-021115-105011Search in Google Scholar PubMed

Priault, M., Salin, B., Schaeffer, J., Vallette, F.M., di Rago, J.P., and Martinou, J.C. (2005). Impairing the bioenergetic status and the biogenesis of mitochondria triggers mitophagy in yeast. Cell Death Differ. 12, 1613–1621.10.1038/sj.cdd.4401697Search in Google Scholar PubMed

Sandoval, H., Thiagarajan, P., Dasgupta, S.K., Schumacher, A., Prchal, J.T., Chen, M., and Wang, J. (2008). Essential role for Nix in autophagic maturation of erythroid cells. Nature 454, 232–235.10.1038/nature07006Search in Google Scholar PubMed PubMed Central

Schäfer, A. and Reichert, A.S. (2009). Emerging roles of mitochondrial membrane dynamics in health and disease. Biol. Chem. 390, 707–715.10.1515/BC.2009.086Search in Google Scholar PubMed

Scheibye-Knudsen, M., Fang, E.F., Croteau, D.L., Wilson, D.M. 3rd, and Bohr, V.A. (2015). Protecting the mitochondrial powerhouse. Trends Cell Biol. 25, 158–170.10.1016/j.tcb.2014.11.002Search in Google Scholar PubMed PubMed Central

Schuck, S., Gallagher, C.M., and Walter, P. (2014). ER-phagy mediates selective degradation of endoplasmic reticulum independently of the core autophagy machinery. J. Cell Sci. 127, 4078–4088.10.1242/jcs.154716Search in Google Scholar PubMed PubMed Central

Schweers, R.L., Zhang, J., Randall, M.S., Loyd, M.R., Li, W., Dorsey, F.C., Kundu, M., Opferman, J.T., Cleveland, J.L., Miller, J.L., et al. (2007). NIX is required for programmed mitochondrial clearance during reticulocyte maturation. Proc. Natl. Acad. Sci. USA 104, 19500–19505.10.1073/pnas.0708818104Search in Google Scholar PubMed PubMed Central

Smit, J.J. and Sixma, T.K. (2014). RBR E3-ligases at work. EMBO Rep. 15, 142–154.10.1002/embr.201338166Search in Google Scholar PubMed PubMed Central

Suliman, H.B. and Piantadosi, C.A. (2016). Mitochondrial quality control as a therapeutic target. Pharmacol. Rev. 68, 20–48.10.1124/pr.115.011502Search in Google Scholar PubMed

Sutovsky, P., Moreno, R.D., Ramalho-Santos, J., Dominko, T., Simerly, C., and Schatten, G. (1999). Ubiquitin tag for sperm mitochondria. Nature 402, 371–372.10.1038/46466Search in Google Scholar PubMed

Twig, G., Elorza, A., Molina, A.J., Mohamed, H., Wikstrom, J.D., Walzer, G., Stiles, L., Haigh, S.E., Katz, S., Las, G., et al. (2008). Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. EMBO J. 27, 433–446.10.1038/sj.emboj.7601963Search in Google Scholar PubMed PubMed Central

Vasquez-Trincado, C., Garcia-Carvajal, I., Pennanen, C., Parra, V., Hill, J.A., Rothermel, B.A., and Lavandero, S. (2016). Mitochondrial dynamics, mitophagy and cardiovascular disease. J. Physiol. 594, 509–525.10.1113/JP271301Search in Google Scholar PubMed PubMed Central

Wang, Y., Serricchio, M., Jauregui, M., Shanbhag, R., Stoltz, T., Di Paolo, C.T., Kim, P.K., and McQuibban, G.A. (2015). Deubiquitinating enzymes regulate PARK2-mediated mitophagy. Autophagy 11, 595–606.10.1080/15548627.2015.1034408Search in Google Scholar PubMed PubMed Central

Welter, E., Montino, M., Reinhold, R., Schlotterhose, P., Krick, R., Dudek, J., Rehling, P., and Thumm, M. (2013). Uth1 is a mitochondrial inner membrane protein dispensable for post-log-phase and rapamycin-induced mitophagy. FEBS J. 280, 4970–4982.10.1111/febs.12468Search in Google Scholar PubMed

Yamano, K. and Youle, R.J. (2013). PINK1 is degraded through the N-end rule pathway. Autophagy 9, 1758–1769.10.4161/auto.24633Search in Google Scholar PubMed PubMed Central

Yonashiro, R., Ishido, S., Kyo, S., Fukuda, T., Goto, E., Matsuki, Y., Ohmura-Hoshino, M., Sada, K., Hotta, H., Yamamura, H., et al. (2006). A novel mitochondrial ubiquitin ligase plays a critical role in mitochondrial dynamics. EMBO J. 25, 3618–3626.10.1038/sj.emboj.7601249Search in Google Scholar PubMed PubMed Central

Yorimitsu, T. and Klionsky, D.J. (2005). Atg11 links cargo to the vesicle-forming machinery in the cytoplasm to vacuole targeting pathway. Mol. Biol. Cell 16, 1593–1605.10.1091/mbc.e04-11-1035Search in Google Scholar PubMed PubMed Central