Selective Autophagy by Close Encounters of the Ubiquitin Kind
Abstract
:1. Introduction
2. Ubiquitin
3. Autophagy
4. Selective Autophagy
5. Cargo Receptors
6. Mitophagy
7. Aggrephagy/Proteophagy
8. ER-Phagy/Reticulophagy
9. Ribophagy
10. Pexophagy
11. Lysophagy
12. Xenophagy
13. Lipophagy
14. Nucleophagy
Autophagy Receptor | Substrates | Function and Associated Pathologies | Refs |
---|---|---|---|
SQSTM1/p62 | General autophagy Protein aggregates Mitochondria Pathogens Lipids Peroxisomes Lysosomes | The most universal autophagy receptor, p62, is involved in cellular stress response and the clearance of protein aggregates, defective organelles as well as invading pathogens. Defects in p62 are associated with Paget disease of bone, amyotrophic lateral sclerosis, and frontotemporal lobar degeneration | [58,59,80,159,174,175] |
NBR1 | Protein aggregates Mitochondria Peroxisomes | NBR1 is involved in aggrephagy and mitophagy, but is the main receptor for pexophagy | [60,61,62,130,176] |
OPTN | General autophagy Protein aggregates Mitochondria Pathogens | OPTN acts as an autophagy receptor for several substrates. Its phosphorylation by TBK1 enhances its function thus facilitating the clearance of Salmonella; it acts as primary mitophagy receptor; mutations in OPTN were found to cause amyotrophic lateral sclerosis, and OPTN in present in protein inclusions found in several neurodegenerative diseases | [53,78,146] |
NDP52 | Mitochondria Pathogens | NDP52 interacts with LC3-C via noncanonical LIR motif and facilitates autophagosome maturation. It is the primary mitophagy receptor and collaborates with p62 for pathogen clearance | [62,158,177] |
TAX1BP1 | MitochondriaPathogens Lysosomes | Promotes autophagy flux in activated T cells, and is recruited to damaged lysosomes facilitating their elimination | [143,178] |
TOLLIP | Protein aggregates | Facilitates degradation of protein aggregates such as huntingtin-derived polyQ proteins | [95] |
15. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Schmidt, M.; Finley, D. Regulation of proteasome activity in health and disease. Biochim. Biophys. Acta Mol. Cell Res. 2014, 1843, 13–25. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Shintani, T.; Klionsky, D.J. Autophagy in health and disease: A double-edged sword. Science 2004, 306, 990–995. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kleiger, G.; Mayor, T. Perilous journey: A tour of the ubiquitin-proteasome system. Trends Cell Biol. 2014, 24, 352–359. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Papadopoulos, C.; Kirchner, P.; Bug, M.; Grum, D.; Koerver, L.; Schulze, N.; Poehler, R.; Dressler, A.; Fengler, S.; Arhzaouy, K.; et al. VCP/p97 cooperates with YOD 1, UBXD 1 and PLAA to drive clearance of ruptured lysosomes by autophagy. EMBO J. 2017, 36, 135–150. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Piccirillo, R.; Goldberg, A.L. The p97/VCP ATPase is critical in muscle atrophy and the accelerated degradation of muscle proteins. EMBO J. 2012, 31, 3334–3350. [Google Scholar] [PubMed] [Green Version]
- Kraft, C.; Peter, M.; Hofmann, K. Selective autophagy: Ubiquitin-mediated recognition and beyond. Nat. Cell Biol. 2010, 12, 836–841. [Google Scholar] [PubMed]
- Deshaies, R.J.; Joazeiro, C.A.P. RING domain E3 ubiquitin ligases. Annu. Rev. Biochem. 2009, 78, 399–434. [Google Scholar] [CrossRef]
- Wild, P.; McEwan, D.G.; Dikic, I. The LC3 interactome at a glance. J. Cell Sci. 2014, 127, 3–9. [Google Scholar] [CrossRef] [Green Version]
- Komander, D.; Clague, M.J.; Urbé, S. Breaking the chains: Structure and function of the deubiquitinases. Nat. Rev. Mol. Cell Biol. 2009, 10, 550–563. [Google Scholar]
- Riley, B.E.; Kaiser, S.E.; Shaler, T.A.; Ng, A.C.Y.; Hara, T.; Hipp, M.S.; Lage, K.; Xavier, R.J.; Ryu, K.-Y.; Taguchi, K.; et al. Ubiquitin accumulation in autophagy-deficient mice is dependent on the Nrf2-mediated stress response pathway: A potential role for protein aggregation in autophagic substrate selection. J. Cell Biol. 2010, 191, 537–552. [Google Scholar]
- Swatek, K.N.; Komander, D. Ubiquitin modifications. Cell Res. 2016, 26, 399–422. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tan, J.M.M.; Wong, E.S.P.; Kirkpatrick, D.S.; Pletnikova, O.; Ko, H.S.; Tay, S.P.; Ho, M.W.L.; Troncoso, J.; Gygi, S.P.; Lee, M.K.; et al. Lysine 63-linked ubiquitination promotes the formation and autophagic clearance of protein inclusions associated with neurodegenerative diseases. Hum. Mol. Genet. 2008, 17, 431–439. [Google Scholar] [CrossRef] [PubMed]
- Morimoto, D.; Walinda, E.; Fukada, H.; Sou, Y.S.; Kageyama, S.; Hoshino, M.; Fujii, T.; Tsuchiya, H.; Saeki, Y.; Arita, K.; et al. The unexpected role of polyubiquitin chains in the formation of fibrillar aggregates. Nat. Commun. 2015, 6, 1–10. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Paz, Y.; Elazar, Z.; Fass, D. Structure of GATE-16, Membrane Transport Modulator and Mammalian Ortholog of Autophagocytosis Factor Aut7p*. J. Biol Chem. 2000, 275, 25445–25450. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Suzuki, N.N.; Yoshimoto, K.; Fujioka, Y.; Ohsumi, Y.; Inagaki, F. The crystal structure of plant ATG12 and its biological implication in autophagy. Autophagy 2005, 1, 119–126. [Google Scholar] [CrossRef] [Green Version]
- Zhang, Y.; Thery, F.; Wu, N.C.; Luhmann, E.K.; Dussurget, O.; Foecke, M.; Bredow, C.; Jiménez-Fernández, D.; Leandro, K.; Beling, A.; et al. The in vivo ISGylome links ISG15 to metabolic pathways and autophagy upon Listeria monocytogenes infection. Nat. Commun. 2019, 10, 1–15. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nakka, V.P.; Mohammed, A.Q. A Critical Role for ISGylation, Ubiquitination and, SUMOylation in Brain Damage: Implications for Neuroprotection. Neurochem. Res. 2020, 45, 1975–1985. [Google Scholar] [CrossRef]
- Spinnenhirn, V.; Farhan, H.; Basler, M.; Aichem, A.; Canaan, A.; Groettrup, M. The ubiquitin-like modifier FAT10 decorates autophagy-targeted Salmonella and contributes to Salmonella resistance in mice. J. Cell Sci. 2014, 127, 4883–4893. [Google Scholar] [CrossRef] [Green Version]
- Hwang, S.P.; Lee, D.H. Autophagy mediates SUMO-induced degradation of a polyglutamine protein ataxin-3. Animal Cells Syst. 2017, 21, 169–176. [Google Scholar] [CrossRef]
- Glick, D.; Barth, S.; Macleod, K.F. Autophagy: Cellular and molecular mechanisms. J. Pathol. 2010, 221, 3–12. [Google Scholar] [CrossRef] [Green Version]
- Levine, B.; Kroemer, G. Biological Functions of Autophagy Genes: A Disease Perspective. Cell 2019, 176, 11–42. [Google Scholar] [CrossRef] [Green Version]
- Youle, R.J.; Narendra, D.P. Mechanisms of mitophagy. Nat. Rev. Mol. Cell Biol. 2011, 12, 9–14. [Google Scholar] [CrossRef] [PubMed]
- Kirkin, V.; Rogov, V.V. A Diversity of Selective Autophagy Receptors Determines the Specificity of the Autophagy Pathway. Mol. Cell 2019, 76, 268–285. [Google Scholar]
- Georgakopoulos, N.D.; Wells, G.; Campanella, M. The pharmacological regulation of cellular mitophagy. Nat. Chem. Biol. 2017, 13, 136–146. [Google Scholar] [CrossRef]
- Reggiori, F.; Komatsu, M.; Finley, K.; Simonsen, A. Autophagy: More than a nonselective pathway. Int. J. Cell Biol. 2012, 2012, 219625. [Google Scholar] [CrossRef] [PubMed]
- Ohsumi, Y.; Mizushima, N. Two ubiquitin-like conjugation systems essential for autophagy. Semin. Cell Dev. Biol. 2004, 15, 231–236. [Google Scholar] [CrossRef]
- Kabeya, Y.; Mizushima, N.; Ueno, T.; Yamamoto, A.; Kirisako, T.; Noda, T.; Kominami, E.; Ohsumi, Y.; Yoshimori, T. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 2000, 19, 5720–5728. [Google Scholar] [CrossRef]
- Ichimura, Y.; Kirisako, T.; Takao, T.; Satomi, Y.; Shimonishi, Y.; Ishihara, N.; Mizushima, N.; Tanida, I.; Kominami, E.; Ohsumi, M.; et al. A ubiquitin-like system mediates protein lipidation. Nature 2000, 408, 488–492. [Google Scholar] [CrossRef]
- Kuma, A.; Mizushima, N.; Ishihara, N.; Ohsumi, Y. Formation of the approximately 350-kDa Apg12-Apg5.Apg16 multimeric complex, mediated by Apg16 oligomerization, is essential for autophagy in yeast. J. Biol. Chem. 2002, 277, 18619–18625. [Google Scholar] [CrossRef] [Green Version]
- Ravikumar, B.; Moreau, K.; Jahreiss, L.; Puri, C.; Rubinsztein, D.C. Plasma membrane contributes to the formation of pre-autophagosomal structures. Nat. Cell Biol. 2010, 12, 747–757. [Google Scholar] [CrossRef]
- Satoo, K.; Noda, N.N.; Kumeta, H.; Fujioka, Y.; Mizushima, N.; Ohsumi, Y.; Inagaki, F. The structure of Atg4B-LC3 complex reveals the mechanism of LC3 processing and delipidation during autophagy. EMBO J. 2009, 28, 1341–1350. [Google Scholar] [CrossRef]
- Bellot, G.; Garcia-Medina, R.; Gounon, P.; Chiche, J.; Roux, D.; Pouysségur, J.; Mazure, N.M. Hypoxia-induced autophagy is mediated through hypoxia-inducible factor induction of BNIP3 and BNIP3L via their BH3 domains. Mol. Cell. Biol. 2009, 29, 2570–2581. [Google Scholar] [CrossRef] [Green Version]
- Jin, S.M.; Youle, R.J. The accumulation of misfolded proteins in the mitochondrial matrix is sensed by PINK1 to induce PARK2/Parkin-mediated mitophagy of polarized mitochondria. Autophagy 2013, 9, 1750–1757. [Google Scholar] [CrossRef] [Green Version]
- Novak, I.; Kirkin, V.; McEwan, D.G.; Zhang, J.; Wild, P.; Rozenknop, A.; Rogov, V.; Löhr, F.; Popovic, D.; Occhipinti, A.; et al. Nix is a selective autophagy receptor for mitochondrial clearance. EMBO Rep. 2010, 11, 45–51. [Google Scholar] [CrossRef] [Green Version]
- Kuchay, S.; Duan, S.; Schenkein, E.; Peschiaroli, A.; Saraf, A.; Florens, L.; Washburn, M.P.; Pagano, M. FBXL2- and PTPL1-mediated degradation of p110-free p85β regulatory subunit controls the PI(3)K signalling cascade. Nat. Cell Biol. 2013, 15, 472–480. [Google Scholar] [CrossRef] [Green Version]
- Abrahamsen, H.; Stenmark, H.; Platta, H.W. Ubiquitination and phosphorylation of Beclin 1 and its binding partners: Tuning class III phosphatidylinositol 3-kinase activity and tumor suppression. FEBS Lett. 2012, 586, 1584–1591. [Google Scholar] [CrossRef]
- Stolz, A.; Ernst, A.; Dikic, I. Cargo recognition and trafficking in selective autophagy. Nat. Cell Biol. 2014, 16, 495–501. [Google Scholar] [CrossRef]
- Shaid, S.; Brandts, C.H.; Serve, H.; Dikic, I. Ubiquitination and selective autophagy. Cell Death Differ. 2013, 20, 21–30. [Google Scholar] [CrossRef]
- Scrivo, A.; Bourdenx, M.; Pampliega, O.; Cuervo, A.M. Selective autophagy as a potential therapeutic target for neurodegenerative disorders. Lancet Neurol. 2018, 17, 802–815. [Google Scholar] [CrossRef]
- Dombi, E.; Mortiboys, H.; Poulton, J. Modulating Mitophagy in Mitochondrial Disease. Curr. Med. Chem. 2017, 25, 5597–5612. [Google Scholar] [CrossRef] [PubMed]
- Mizumura, K.; Cloonan, S.M.; Nakahira, K.; Bhashyam, A.R.; Cervo, M.; Kitada, T.; Glass, K.; Owen, C.A.; Mahmood, A.; Washko, G.R.; et al. Mitophagy-dependent necroptosis contributes to the pathogenesis of COPD. J. Clin. Investig. 2014, 124, 3987–4003. [Google Scholar] [PubMed] [Green Version]
- Mizumura, K.; Choi, A.M.K.; Ryter, S.W. Emerging role of selective autophagy in human diseases. Front. Pharmacol. 2014, 5, 244. [Google Scholar] [PubMed] [Green Version]
- Reggio, A.; Buonomo, V.; Grumati, P. Eating the unknown: Xenophagy and ER-phagy are cytoprotective defenses against pathogens. Exp. Cell Res. 2020, 396, 112276. [Google Scholar]
- Sharma, V.; Verma, S.; Seranova, E.; Sarkar, S.; Kumar, D. Selective autophagy and xenophagy in infection and disease. Front. Cell Dev. Biol. 2018, 6, 147. [Google Scholar] [PubMed] [Green Version]
- Dong, X.; Levine, B. Autophagy and viruses: Adversaries or allies? J. Innate Immun. 2013, 5, 480–493. [Google Scholar]
- Mijaljica, D.; Klionsky, D.J. Autophagy/virophagy: A “disposal strategy” to combat COVID-19. Autophagy 2020, 1–2. [Google Scholar] [CrossRef]
- Chiramel, A.I.; Dougherty, J.D.; Nair, V.; Robertson, S.J.; Best, S.M. FAM134B, the Selective Autophagy Receptor for Endoplasmic Reticulum Turnover, Inhibits Replication of Ebola Virus Strains Makona and Mayinga. J. Infect. Dis. 2016, 214, S319–S325. [Google Scholar]
- Lennemann, N.J.; Coyne, C.B. Dengue and Zika viruses subvert reticulophagy by NS2B3-mediated cleavage of FAM134B. Autophagy 2017, 13, 322–332. [Google Scholar]
- Nicot, A.S.; Lo Verso, F.; Ratti, F.; Pilot-Storck, F.; Streichenberger, N.; Sandri, M.; Schaeffer, L.; Goillot, E. Phosphorylation of NBR1 by GSK3 modulates protein aggregation. Autophagy 2014, 10, 1036–1053. [Google Scholar]
- Richter, B.; Sliter, D.A.; Herhaus, L.; Stolz, A.; Wang, C.; Beli, P.; Zaffagnini, G.; Wild, P.; Martens, S.; Wagner, S.A.; et al. Phosphorylation of OPTN by TBK1 enhances its binding to Ub chains and promotes selective autophagy of damaged mitochondria. Proc. Natl. Acad. Sci. USA 2016, 113, 4039–4044. [Google Scholar]
- Matsumoto, G.; Wada, K.; Okuno, M.; Kurosawa, M.; Nukina, N. Serine 403 phosphorylation of p62/SQSTM1 regulates selective autophagic clearance of ubiquitinated proteins. Mol. Cell 2011, 44, 279–289. [Google Scholar] [CrossRef] [PubMed]
- Noda, N.N.; Kumeta, H.; Nakatogawa, H.; Satoo, K.; Adachi, W.; Ishii, J.; Fujioka, Y.; Ohsumi, Y.; Inagaki, F. Structural basis of target recognition by Atg8/LC3 during selective autophagy. Genes Cells 2008, 13, 1211–1218. [Google Scholar] [CrossRef] [PubMed]
- Wild, P.; Farhan, H.; McEwan, D.G.; Wagner, S.; Rogov, V.V.; Brady, N.R.; Richter, B.; Korac, J.; Waidmann, O.; Choudhary, C.; et al. Phosphorylation of the autophagy receptor optineurin restricts Salmonella growth. Science 2011, 333, 228–233. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tumbarello, D.A.; Manna, P.T.; Allen, M.; Bycroft, M.; Arden, S.D.; Kendrick-Jones, J.; Buss, F. The Autophagy Receptor TAX1BP1 and the Molecular Motor Myosin VI Are Required for Clearance of Salmonella Typhimurium by Autophagy. PLoS Pathog. 2015, 11, e1005174. [Google Scholar]
- von Muhlinen, N.; Akutsu, M.; Ravenhill, B.J.; Foeglein, Á.; Bloor, S.; Rutherford, T.J.; Freund, S.M.V.; Komander, D.; Randow, F. LC3C, bound selectively by a noncanonical LIR motif in NDP52, is required for antibacterial autophagy. Mol. Cell 2012, 48, 329–342. [Google Scholar] [CrossRef] [Green Version]
- Marshall, R.S.; Hua, Z.; Mali, S.; McLoughlin, F.; Vierstra, R.D. ATG8-Binding UIM Proteins Define a New Class of Autophagy Adaptors and Receptors. Cell 2019, 177, 766–781.e24. [Google Scholar]
- Wurzer, B.; Zaffagnini, G.; Fracchiolla, D.; Turco, E.; Abert, C.; Romanov, J.; Martens, S. Oligomerization of p62 allows for selection of ubiquitinated cargo and isolation membrane during selective autophagy. Elife 2015, 4. [Google Scholar] [CrossRef]
- Zatloukal, K.; Stumptner, C.; Fuchsbichler, A.; Heid, H.; Schnoelzer, M.; Kenner, L.; Kleinert, R.; Prinz, M.; Aguzzi, A.; Denk, H. p62 is a common component of cytoplasmic inclusions in protein aggregation diseases. Am. J. Pathol. 2002, 160, 255–263. [Google Scholar] [CrossRef] [Green Version]
- Pankiv, S.; Clausen, T.H.; Lamark, T.; Brech, A.; Bruun, J.-A.; Outzen, H.; Øvervatn, A.; Bjørkøy, G.; Johansen, T. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J. Biol. Chem. 2007, 282, 24131–24145. [Google Scholar] [CrossRef] [Green Version]
- Zhou, J.; Wang, J.; Cheng, Y.; Chi, Y.-J.; Fan, B.; Yu, J.-Q.; Chen, Z. NBR1-Mediated Selective Autophagy Targets Insoluble Ubiquitinated Protein Aggregates in Plant Stress Responses. PLoS Genet. 2013, 9, e1003196. [Google Scholar] [CrossRef] [Green Version]
- Kirkin, V.; Lamark, T.; Sou, Y.-S.; Bjørkøy, G.; Nunn, J.L.; Bruun, J.-A.; Shvets, E.; McEwan, D.G.; Clausen, T.H.; Wild, P.; et al. A role for NBR1 in autophagosomal degradation of ubiquitinated substrates. Mol. Cell 2009, 33, 505–516. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Deosaran, E.; Larsen, K.B.; Hua, R.; Sargent, G.; Wang, Y.; Kim, S.; Lamark, T.; Jauregui, M.; Law, K.; Lippincott-Schwartz, J.; et al. NBR1 acts as an autophagy receptor for peroxisomes. J. Cell Sci. 2013, 126, 939–952. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Korac, J.; Schaeffer, V.; Kovacevic, I.; Clement, A.M.; Jungblut, B.; Behl, C.; Terzic, J.; Dikic, I. Ubiquitin-independent function of optineurin in autophagic clearance of protein aggregates. J. Cell Sci. 2013, 126, 580–592. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liu, Z.; Chen, P.; Gao, H.; Gu, Y.; Yang, J.; Peng, H.; Xu, X.; Wang, H.; Yang, M.; Liu, X.; et al. Ubiquitylation of Autophagy Receptor Optineurin by HACE1 Activates Selective Autophagy for Tumor Suppression. Cancer Cell 2014, 26, 106–120. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Menzies, R.A.; Gold, P.H. The Turnover of Mitochondria in a Variety of Tissues of Young Adult and Aged Rats. J. Biol. Chem. 1971, 246, 2425–2429. [Google Scholar]
- Sandoval, H.; Thiagarajan, P.; Dasgupta, S.K.; Schumacher, A.; Prchal, J.T.; Chen, M.; Wang, J. Essential role for Nix in autophagic maturation of erythroid cells. Nature 2008, 454, 232–235. [Google Scholar] [CrossRef]
- Sato, M.; Sato, K. Degradation of paternal mitochondria by fertilization-triggered autophagy in C. elegans embryos. Science 2011, 334, 1141–1144. [Google Scholar] [CrossRef]
- Al Rawi, S.; Louvet-Vallée, S.; Djeddi, A.; Sachse, M.; Culetto, E.; Hajjar, C.; Boyd, L.; Legouis, R.; Galy, V. Postfertilization autophagy of sperm organelles prevents paternal mitochondrial DNA transmission. Science 2011, 334, 1144–1147. [Google Scholar] [CrossRef]
- Melser, S.; Chatelain, E.H.; Lavie, J.; Mahfouf, W.; Jose, C.; Obre, E.; Goorden, S.; Priault, M.; Elgersma, Y.; Rezvani, H.R.; et al. Rheb regulates mitophagy induced by mitochondrial energetic status. Cell Metab. 2013, 17, 719–730. [Google Scholar] [CrossRef] [Green Version]
- Vives-Bauza, C.; Zhou, C.; Huang, Y.; Cui, M.; de Vries, R.L.A.; Kim, J.; May, J.; Tocilescu, M.A.; Liu, W.; Ko, H.S.; et al. PINK1-dependent recruitment of Parkin to mitochondria in mitophagy. Proc. Natl. Acad. Sci. USA 2010, 107, 378–383. [Google Scholar] [CrossRef] [Green Version]
- Kondapalli, C.; Kazlauskaite, A.; Zhang, N.; Woodroof, H.I.; Campbell, D.G.; Gourlay, R.; Burchell, L.; Walden, H.; Macartney, T.J.; Deak, M.; et al. PINK1 is activated by mitochondrial membrane potential depolarization and stimulates Parkin E3 ligase activity by phosphorylating Serine 65. Open Biol. 2012, 2, 120080. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Narendra, D.; Tanaka, A.; Suen, D.-F.; Youle, R.J. Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J. Cell Biol. 2008, 183, 795–803. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sarraf, S.A.; Raman, M.; Guarani-Pereira, V.; Sowa, M.E.; Huttlin, E.L.; Gygi, S.P.; Harper, J.W. Landscape of the PARKIN-dependent ubiquitylome in response to mitochondrial depolarization. Nature 2013, 496, 372–376. [Google Scholar] [CrossRef] [PubMed]
- Wang, X.; Winter, D.; Ashrafi, G.; Schlehe, J.; Wong, Y.L.; Selkoe, D.; Rice, S.; Steen, J.; LaVoie, M.J.; Schwarz, T.L. PINK1 and Parkin target Miro for phosphorylation and degradation to arrest mitochondrial motility. Cell 2011, 147, 893–906. [Google Scholar] [CrossRef] [Green Version]
- Fu, M.; St-Pierre, P.; Shankar, J.; Wang, P.T.C.C.; Joshi, B.; Nabi, I.R. Regulation of mitophagy by the Gp78 E3 ubiquitin ligase. Mol. Biol. Cell 2013, 24, 1153–1162. [Google Scholar] [CrossRef]
- Bingol, B.; Tea, J.S.; Phu, L.; Reichelt, M.; Bakalarski, C.E.; Song, Q.; Foreman, O.; Kirkpatrick, D.S.; Sheng, M. The mitochondrial deubiquitinase USP30 opposes parkin-mediated mitophagy. Nature 2014, 510, 370–375. [Google Scholar] [CrossRef]
- Geisler, S.; Holmström, K.M.; Skujat, D.; Fiesel, F.C.; Rothfuss, O.C.; Kahle, P.J.; Springer, W. PINK1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1. Nat. Cell Biol. 2010, 12, 119–131. [Google Scholar] [CrossRef]
- Wong, Y.C.; Holzbaur, E.L.F. Optineurin is an autophagy receptor for damaged mitochondria in parkin-mediated mitophagy that is disrupted by an ALS-linked mutation. Proc. Natl. Acad. Sci. USA 2014, 111, E4439–E4448. [Google Scholar] [CrossRef] [Green Version]
- Lazarou, M.; Sliter, D.A.; Kane, L.A.; Sarraf, S.A.; Wang, C.; Burman, J.L.; Sideris, D.P.; Fogel, A.I.; Youle, R.J. The ubiquitin kinase PINK1 recruits autophagy receptors to induce mitophagy. Nature 2015, 524, 309–314. [Google Scholar] [CrossRef] [Green Version]
- Narendra, D.; Kane, L.A.; Hauser, D.N.; Fearnley, I.M.; Youle, R.J. p62/SQSTM1 is required for Parkin-induced mitochondrial clustering but not mitophagy; VDAC1 is dispensable for both. Autophagy 2010, 6, 1090–1106. [Google Scholar] [CrossRef]
- Lamark, T.; Johansen, T. Aggrephagy: Selective disposal of protein aggregates by macroautophagy. Int. J. Cell Biol. 2012, 2012, 736905. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pickford, F.; Masliah, E.; Britschgi, M.; Lucin, K.; Narasimhan, R.; Jaeger, P.A.; Small, S.; Spencer, B.; Rockenstein, E.; Levine, B.; et al. The autophagy-related protein beclin 1 shows reduced expression in early Alzheimer disease and regulates amyloid β accumulation in mice. J. Clin. Investig. 2008, 118, 2190–2199. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Webb, J.L.; Ravikumar, B.; Atkins, J.; Skepper, J.N.; Rubinsztein, D.C. Alpha-Synuclein is degraded by both autophagy and the proteasome. J. Biol. Chem. 2003, 278, 25009–25013. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ravikumar, B.; Vacher, C.; Berger, Z.; Davies, J.E.; Luo, S.; Oroz, L.G.; Scaravilli, F.; Easton, D.F.; Duden, R.; O’Kane, C.J.; et al. Inhibition of mTOR induces autophagy and reduces toxicity of polyglutamine expansions in fly and mouse models of Huntington disease. Nat. Genet. 2004, 36, 585–595. [Google Scholar] [CrossRef] [Green Version]
- Winslow, A.R.; Chen, C.W.; Corrochano, S.; Acevedo-Arozena, A.; Gordon, D.E.; Peden, A.A.; Lichtenberg, M.; Menzies, F.M.; Ravikumar, B.; Imarisio, S.; et al. α-Synuclein impairs macroautophagy: Implications for Parkinson’s disease. J. Cell Biol. 2010, 190, 1023–1037. [Google Scholar] [CrossRef] [Green Version]
- Ciechanover, A.; Brundin, P. The ubiquitin proteasome system in neurodegenerative diseases: Sometimes the chicken, sometimes the egg. Neuron 2003, 40, 427–446. [Google Scholar] [CrossRef] [Green Version]
- Lee, Y.; Jonson, P.H.; Sarparanta, J.; Palmio, J.; Sarkar, M.; Vihola, A.; Evilä, A.; Suominen, T.; Penttilä, S.; Savarese, M.; et al. TIA1 variant drives myodegeneration in multisystem proteinopathy with SQSTM1 mutations. J. Clin. Investig. 2018, 128, 1164–1177. [Google Scholar] [CrossRef] [Green Version]
- Neumann, M.; Sampathu, D.M.; Kwong, L.K.; Truax, A.C.; Micsenyi, M.C.; Chou, T.T.; Bruce, J.; Schuck, T.; Grossman, M.; Clark, C.M.; et al. Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 2006, 314, 130–133. [Google Scholar] [CrossRef] [Green Version]
- Deng, H.X.; Chen, W.; Hong, S.T.; Boycott, K.M.; Gorrie, G.H.; Siddique, N.; Yang, Y.; Fecto, F.; Shi, Y.; Zhai, H.; et al. Mutations in UBQLN2 cause dominant X-linked juvenile and adult-onset ALS and ALS/dementia. Nature 2011, 477, 211–215. [Google Scholar] [CrossRef] [Green Version]
- Isakson, P.; Holland, P.; Simonsen, A. The role of ALFY in selective autophagy. Cell Death Differ. 2013, 20, 12–20. [Google Scholar] [CrossRef] [Green Version]
- Simonsen, A.; Birkeland, H.C.G.; Gillooly, D.J.; Mizushima, N.; Kuma, A.; Yoshimori, T.; Slagsvold, T.; Brech, A.; Stenmark, H. Alfy, a novel FYVE-domain-containing protein associated with protein granules and autophagic membranes. J. Cell Sci. 2004, 117, 4239–4251. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Marshall, R.S.; Li, F.; Gemperline, D.C.; Book, A.J.; Vierstra, R.D. Autophagic Degradation of the 26S Proteasome Is Mediated by the Dual ATG8/Ubiquitin Receptor RPN10 in Arabidopsis. Mol. Cell 2015, 58, 1053–1066. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Marshall, R.; McLoughlin, F.; Vierstra, R.D. Autophagic turnover of inactive 26S proteasomes in yeast is directed by the ubiquitin receptor Cue5 and the Hsp42 chaperone. Cell Rep. 2016, 16, 1717–1732. [Google Scholar] [CrossRef] [Green Version]
- Cohen-Kaplan, V.; Livneh, I.; Avni, N.; Fabre, B.; Ziv, T.; Kwon, Y.T.; Ciechanover, A. p62- and ubiquitin-dependent stress-induced autophagy of the mammalian 26S proteasome. Proc. Natl. Acad. Sci. USA 2016, 113, E7490–E7499. [Google Scholar] [CrossRef] [Green Version]
- Lu, K.; Psakhye, I.; Jentsch, S. Autophagic clearance of PolyQ proteins mediated by ubiquitin-Atg8 adaptors of the conserved CUET protein family. Cell 2014, 158, 549–563. [Google Scholar] [CrossRef] [Green Version]
- Cho, S.J.; Yun, S.M.; Jo, C.; Lee, D.H.; Choi, K.J.; Song, J.C.; Park, S.I.; Kim, Y.J.; Koh, Y.H. SUMO1 promotes Aβ production via the modulation of autophagy. Autophagy 2015, 11, 100–112. [Google Scholar] [CrossRef] [Green Version]
- Nagashima, Y.; Kowa, H.; Tsuji, S.; Iwata, A. FAT10 protein binds to polyglutamine proteins and modulates their solubility. J. Biol. Chem. 2011, 286, 29594–29600. [Google Scholar] [CrossRef] [Green Version]
- Kalveram, B.; Schmidtke, G.; Groettrup, M. The ubiquitin-like modifier FAT10 interacts with HDAC6 and localizes to aggresomes under proteasome inhibition. J. Cell Sci. 2008, 121, 4079–4088. [Google Scholar] [CrossRef] [Green Version]
- Nakashima, H.; Nguyen, T.; Goins, W.F.; Chiocca, E.A. Interferon-stimulated gene 15 (ISG15) and ISG15-linked proteins can associate with members of the selective autophagic process, histone deacetylase 6 (HDAC6) and SQSTM1/p62. J. Biol. Chem. 2015, 290, 1485–1495. [Google Scholar] [CrossRef] [Green Version]
- Ylä-Anttila, P.; Vihinen, H.; Jokitalo, E.; Eskelinen, E.L. 3D tomography reveals connections between the phagophore and endoplasmic reticulum. Autophagy 2009, 5, 1180–1185. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Axe, E.L.; Walker, S.A.; Manifava, M.; Chandra, P.; Roderick, H.L.; Habermann, A.; Griffiths, G.; Ktistakis, N.T. Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum. J. Cell Biol. 2008, 182, 685–701. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Matsunaga, K.; Morita, E.; Saitoh, T.; Akira, S.; Ktistakis, N.T.; Izumi, T.; Noda, T.; Yoshimori, T. Autophagy requires endoplasmic reticulum targeting of the PI3-kinase complex via Atg14L. J. Cell Biol. 2010, 190, 511–521. [Google Scholar] [CrossRef]
- Nixon-Abell, J.; Obara, C.J.; Weigel, A.V.; Li, D.; Legant, W.R.; Xu, C.S.; Pasolli, H.A.; Harvey, K.; Hess, H.F.; Betzig, E.; et al. Increased spatiotemporal resolution reveals highly dynamic dense tubular matrices in the peripheral ER. Science 2016, 354. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hetz, C. The unfolded protein response: Controlling cell fate decisions under ER stress and beyond. Nat. Rev. Mol. Cell Biol. 2012, 13, 89–102. [Google Scholar] [CrossRef] [PubMed]
- Grumati, P.; Dikic, I.; Stolz, A. ER-phagy at a glance. J. Cell Sci. 2018, 131. [Google Scholar] [CrossRef] [Green Version]
- Stolz, A.; Grumati, P. The various shades of ER-phagy. FEBS J. 2019, 286, 4642–4649. [Google Scholar] [CrossRef]
- Khaminets, A.; Heinrich, T.; Mari, M.; Grumati, P.; Huebner, A.K.; Akutsu, M.; Liebmann, L.; Stolz, A.; Nietzsche, S.; Koch, N.; et al. Regulation of endoplasmic reticulum turnover by selective autophagy. Nature 2015, 522, 354–358. [Google Scholar] [CrossRef] [PubMed]
- Fumagalli, F.; Noack, J.; Bergmann, T.J.; Presmanes, E.C.; Pisoni, G.B.; Fasana, E.; Fregno, I.; Galli, C.; Loi, M.; Soldà, T.; et al. Translocon component Sec62 acts in endoplasmic reticulum turnover during stress recovery. Nat. Cell Biol. 2016, 18, 1173–1184. [Google Scholar] [CrossRef] [Green Version]
- Grumati, P.; Morozzi, G.; Hölper, S.; Mari, M.; Harwardt, M.L.I.E.; Yan, R.; Müller, S.; Reggiori, F.; Heilemann, M.; Dikic, I. Full length RTN3 regulates turnover of tubular endoplasmic reticulum via selective autophagy. Elife 2017, 6. [Google Scholar] [CrossRef]
- Smith, M.D.; Harley, M.E.; Kemp, A.J.; Wills, J.; Lee, M.; Arends, M.; von Kriegsheim, A.; Behrends, C.; Wilkinson, S. CCPG1 Is a Non-canonical Autophagy Cargo Receptor Essential for ER-Phagy and Pancreatic ER Proteostasis. Dev. Cell 2018, 44, 217–232. [Google Scholar] [CrossRef]
- Chino, H.; Hatta, T.; Natsume, T.; Mizushima, N. Intrinsically Disordered Protein TEX264 Mediates ER-phagy Article Intrinsically Disordered Protein TEX264 Mediates ER-phagy. Mol. Cell 2019, 74, 909–921. [Google Scholar] [CrossRef]
- Chen, Q.; Xiao, Y.; Chai, P.; Zheng, P.; Teng, J.; Chen, J. ATL3 Is a Tubular ER-Phagy Receptor for GABARAP-Mediated Selective Autophagy. Curr. Biol. 2019, 29, 846–855. [Google Scholar] [CrossRef] [Green Version]
- An, H.; Ordureau, A.; Paulo, J.A.; Shoemaker, C.J.; Denic, V.; Harper, J.W. TEX264 Is an Endoplasmic Reticulum-Resident ATG8-Interacting Protein Critical for ER Remodeling during Nutrient Stress. Mol. Cell 2019, 74, 891–908. [Google Scholar] [CrossRef]
- Ji, C.H.; Kim, H.Y.; Heo, A.J.; Lee, S.H.; Lee, M.J.; Kim, S.B.; Srinivasrao, G.; Mun, S.R.; Cha-Molstad, H.; Ciechanover, A.; et al. The N-Degron Pathway Mediates ER-phagy. Mol. Cell 2019, 75, 1058–1072. [Google Scholar] [CrossRef]
- Tschurtschenthaler, M.; Adolph, T.E.; Ashcroft, J.W.; Niederreiter, L.; Bharti, R.; Saveljeva, S.; Bhattacharyya, J.; Flak, M.B.; Shih, D.Q.; Fuhler, G.M.; et al. Defective ATG16L1-mediated removal of IRE1α drives Crohn’s disease-like ileitis. J. Exp. Med. 2017, 214, 401–422. [Google Scholar] [CrossRef]
- Yang, H.; Ni, H.M.; Guo, F.; Ding, Y.; Shi, Y.H.; Lahiri, P.; Fröhlich, L.F.; Rülicke, T.; Smole, C.; Schmidt, V.C.; et al. Sequestosome 1/p62 protein is associated with autophagic removal of excess hepatic endoplasmic reticulum in mice. J. Biol. Chem. 2016, 291, 18663–18674. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kraft, C.; Deplazes, A.; Sohrmann, M.; Peter, M. Mature ribosomes are selectively degraded upon starvation by an autophagy pathway requiring the Ubp3p/Bre5p ubiquitin protease. Nat. Cell Biol. 2008, 10, 602–610. [Google Scholar] [CrossRef]
- Ossareh-Nazari, B.; Bonizec, M.; Cohen, M.; Dokudovskaya, S.; Delalande, F.; Schaeffer, C.; Van Dorsselaer, A.; Dargemont, C. Cdc48 and Ufd3, new partners of the ubiquitin protease Ubp3, are required for ribophagy. EMBO Rep. 2010, 11, 548–554. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- An, H.; Harper, J.W. Systematic analysis of ribophagy in human cells reveals bystander flux during selective autophagy. Nat. Cell Biol. 2018, 20, 135–143. [Google Scholar] [CrossRef]
- Wyant, G.A.; Abu-Remaileh, M.; Frenkel, E.M.; Laqtom, N.N.; Dharamdasani, V.; Lewis, C.A.; Chan, S.H.; Heinze, I.; Ori, A.; Sabatini, D.M. Nufip1 is a ribosome receptor for starvation-induced ribophagy. Science 2018, 360, 751–758. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- An, H.; Ordureau, A.; Körner, M.; Paulo, J.A.; Harper, J.W. Systematic quantitative analysis of ribosome inventory during nutrient stress. Nature 2020, 583, 303–309. [Google Scholar] [CrossRef]
- Garzia, A.; Jafarnejad, S.M.; Meyer, C.; Chapat, C.; Gogakos, T.; Morozov, P.; Amiri, M.; Shapiro, M.; Molina, H.; Tuschl, T.; et al. The E3 ubiquitin ligase and RNA-binding protein ZNF598 orchestrates ribosome quality control of premature polyadenylated mRNAs. Nat. Commun. 2017, 8, 1–10. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Silva, G.M.; Finley, D.; Vogel, C. K63 polyubiquitination is a new modulator of the oxidative stress response. Nat. Struct. Mol. Biol. 2015, 22, 116–123. [Google Scholar] [CrossRef] [Green Version]
- Higgins, R.; Gendron, J.M.; Rising, L.; Mak, R.; Webb, K.; Kaiser, S.E.; Zuzow, N.; Riviere, P.; Yang, B.; Fenech, E.; et al. The Unfolded Protein Response Triggers Site-Specific Regulatory Ubiquitylation of 40S Ribosomal Proteins. Mol. Cell 2015, 59, 35–49. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- An, H.; Harper, J.W. Ribosome Abundance Control Via the Ubiquitin–Proteasome System and Autophagy. J. Mol. Biol. 2020, 432, 170–184. [Google Scholar] [CrossRef]
- Sung, M.K.; Porras-Yakushi, T.R.; Reitsma, J.M.; Huber, F.M.; Sweredoski, M.J.; Hoelz, A.; Hess, S.; Deshaies, R.J. A conserved quality-control pathway that mediates degradation of unassembled ribosomal proteins. Elife 2016, 5. [Google Scholar] [CrossRef]
- Yanagitani, K.; Juszkiewicz, S.; Hegde, R.S. UBE2O is a quality control factor for orphans of multiprotein complexes. Science 2017, 357, 472–475. [Google Scholar] [CrossRef] [Green Version]
- Zhang, J.; Tripathi, D.N.; Jing, J.; Alexander, A.; Kim, J.; Powell, R.T.; Dere, R.; Tait-Mulder, J.; Lee, J.H.; Paull, T.T.; et al. ATM functions at the peroxisome to induce pexophagy in response to ROS. Nat. Cell Biol. 2015, 17, 1259–1269. [Google Scholar] [CrossRef] [Green Version]
- Nordgren, M.; Francisco, T.; Lismont, C.; Hennebel, L.; Brees, C.; Wang, B.; van Veldhoven, P.P.; Azevedo, J.E.; Fransen, M. Export-deficient monoubiquitinated PEX5 triggers peroxisome removal in SV40 large T antigen-transformed mouse embryonic fibroblasts. Autophagy 2015, 11, 1326–1340. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sargent, G.; van Zutphen, T.; Shatseva, T.; Zhang, L.; Di Giovanni, V.; Bandsma, R.; Kim, P.K. PEX2 is the E3 ubiquitin ligase required for pexophagy during starvation. J. Cell Biol. 2016, 214. [Google Scholar] [CrossRef]
- Yamashita, S.I.; Abe, K.; Tatemichi, Y.; Fujiki, Y. The membrane peroxin PEX3 induces peroxisome-ubiquitination-linked pexophagy. Autophagy 2014, 10, 1549–1564. [Google Scholar] [CrossRef] [Green Version]
- Kim, P.K.; Hailey, D.W.; Mullen, R.T.; Lippincott-Schwartz, J. Ubiquitin signals autophagic degradation of cytosolic proteins and peroxisomes. Proc. Natl. Acad. Sci. USA 2008, 105, 20567–20574. [Google Scholar] [CrossRef] [Green Version]
- Nazarko, T.Y.; Ozeki, K.; Till, A.; Ramakrishnan, G.; Lotfi, P.; Yan, M.; Subramani, S. Peroxisomal Atg37 binds Atg30 or palmitoyl-CoA to regulate phagophore formation during pexophagy. J. Cell Biol. 2014, 204, 541–557. [Google Scholar] [CrossRef] [Green Version]
- Settembre, C.; Zoncu, R.; Medina, D.L.; Vetrini, F.; Erdin, S.; Erdin, S.; Huynh, T.; Ferron, M.; Karsenty, G.; Vellard, M.C.; et al. A lysosome-to-nucleus signalling mechanism senses and regulates the lysosome via mTOR and TFEB. EMBO J. 2012, 31, 1095–1108. [Google Scholar] [CrossRef] [Green Version]
- de Duve, C. Lysosomes, a new group of cytoplasmic particles. Subcell. Part. 1959, 60, 128–159. [Google Scholar]
- Boya, P.; Kroemer, G. Lysosomal membrane permeabilization in cell death. Oncogene 2008, 27, 6434–6451. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Maejima, I.; Takahashi, A.; Omori, H.; Kimura, T.; Takabatake, Y.; Saitoh, T.; Yamamoto, A.; Hamasaki, M.; Noda, T.; Isaka, Y.; et al. Autophagy sequesters damaged lysosomes to control lysosomal biogenesis and kidney injury. EMBO J. 2013, 32, 2336–2347. [Google Scholar] [CrossRef] [Green Version]
- Yoshida, Y.; Yasuda, S.; Fujita, T.; Hamasaki, M.; Murakami, A.; Kawawaki, J.; Iwai, K.; Saeki, Y.; Yoshimori, T.; Matsuda, N.; et al. Ubiquitination of exposed glycoproteins by SCFFBXO27 directs damaged lysosomes for autophagy. Proc. Natl. Acad. Sci. USA. 2017, 114, 8574–8579. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fiskin, E.; Bionda, T.; Dikic, I.; Behrends, C. Global Analysis of Host and Bacterial Ubiquitinome in Response to Salmonella Typhimurium Infection. Mol. Cell 2016, 62, 967–981. [Google Scholar] [CrossRef] [Green Version]
- Chauhan, S.; Kumar, S.; Jain, A.; Ponpuak, M.; Mudd, M.H.; Kimura, T.; Choi, S.W.; Peters, R.; Mandell, M.; Bruun, J.A.; et al. TRIMs and Galectins Globally Cooperate and TRIM16 and Galectin-3 Co-direct Autophagy in Endomembrane Damage Homeostasis. Dev. Cell 2016, 39, 13–27. [Google Scholar] [CrossRef] [Green Version]
- Aits, S.; Kricker, J.; Liu, B.; Ellegaard, A.-M.; Hämälistö, S.; Tvingsholm, S.; Corcelle-Termeau, E.; Høgh, S.; Farkas, T.; Holm Jonassen, A.; et al. Sensitive detection of lysosomal membrane permeabilization by lysosomal galectin puncta assay. Autophagy 2015, 11, 1408–1424. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Thurston, T.L.M.; Wandel, M.P.; Von Muhlinen, N.; Foeglein, Á.; Randow, F. Galectin 8 targets damaged vesicles for autophagy to defend cells against bacterial invasion. Nature 2012, 482, 414–418. [Google Scholar] [CrossRef] [PubMed]
- Koerver, L.; Papadopoulos, C.; Liu, B.; Kravic, B.; Rota, G.; Brecht, L.; Veenendaal, T.; Polajnar, M.; Bluemke, A.; Ehrmann, M.; et al. The ubiquitin-conjugating enzyme UBE 2 QL 1 coordinates lysophagy in response to endolysosomal damage. EMBO Rep. 2019, 20. [Google Scholar] [CrossRef] [PubMed]
- Hung, Y.H.; Chen, L.M.W.; Yang, J.Y.; Yuan Yang, W. Spatiotemporally controlled induction of autophagy-mediated lysosome turnover. Nat. Commun. 2013, 4. [Google Scholar] [CrossRef] [Green Version]
- Fujita, N.; Morita, E.; Itoh, T.; Tanaka, A.; Nakaoka, M.; Osada, Y.; Umemoto, T.; Saitoh, T.; Nakatogawa, H.; Kobayashi, S.; et al. Recruitment of the autophagic machinery to endosomes during infection is mediated by ubiquitin. J. Cell Biol. 2013, 203, 115–128. [Google Scholar] [CrossRef] [Green Version]
- Bussi, C.; Peralta Ramos, J.M.; Arroyo, D.S.; Gallea, J.I.; Ronchi, P.; Kolovou, A.; Wang, J.M.; Florey, O.; Celej, M.S.; Schwab, Y.; et al. Alpha-synuclein fibrils recruit TBK1 and OPTN to lysosomal damage sites and induce autophagy in microglial cells. J. Cell Sci. 2018, 131. [Google Scholar] [CrossRef] [Green Version]
- Goebel, W.; Kuhn, M. Bacterial replication in the host cell cytosol. Curr. Opin. Microbiol. 2000, 3, 49–53. [Google Scholar] [CrossRef]
- Dupont, N.; Lacas-Gervais, S.; Bertout, J.; Paz, I.; Freche, B.; Van Nhieu, G.T.; van der Goot, F.G.; Sansonetti, P.J.; Lafont, F. Shigella Phagocytic Vacuolar Membrane Remnants Participate in the Cellular Response to Pathogen Invasion and Are Regulated by Autophagy. Cell Host Microbe 2009, 6, 137–149. [Google Scholar] [CrossRef] [Green Version]
- Gomes, L.C.; Dikic, I. Autophagy in antimicrobial immunity. Mol. Cell 2014, 54, 224–233. [Google Scholar] [CrossRef] [Green Version]
- Perrin, A.J.; Jiang, X.; Birmingham, C.L.; So, N.S.Y.; Brumell, J.H. Recognition of bacteria in the cytosol of mammalian cells by the ubiquitin system. Curr. Biol. 2004, 14, 806–811. [Google Scholar] [CrossRef] [Green Version]
- van Wijk, S.J.L.; Fiskin, E.; Putyrski, M.; Pampaloni, F.; Hou, J.; Wild, P.; Kensche, T.; Grecco, H.E.; Bastiaens, P.; Dikic, I. Fluorescence-Based Sensors to Monitor Localization and Functions of Linear and K63-Linked Ubiquitin Chains in Cells. Mol. Cell 2012, 47, 797–809. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Collins, C.A.; De Mazière, A.; Van Dijk, S.; Carlsson, F.; Klumperman, J.; Brown, E.J. Atg5-independent sequestration of ubiquitinated mycobacteria. PLoS Pathog. 2009, 5. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Polajnar, M.; Dietz, M.S.; Heilemann, M.; Behrends, C. Expanding the host cell ubiquitylation machinery targeting cytosolic Salmonella. EMBO Rep. 2017, 18, 1572–1585. [Google Scholar] [CrossRef] [PubMed]
- Huett, A.; Heath, R.J.; Begun, J.; Sassi, S.O.; Baxt, L.A.; Vyas, J.M.; Goldberg, M.B.; Xavier, R.J. The LRR and RING domain protein LRSAM1 is an E3 ligase crucial for ubiquitin-dependent autophagy of intracellular salmonella typhimurium. Cell Host Microbe 2012, 12, 778–790. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Noad, J.; Von Der Malsburg, A.; Pathe, C.; Michel, M.A.; Komander, D.; Randow, F. LUBAC-synthesized linear ubiquitin chains restrict cytosol-invading bacteria by activating autophagy and NF-κB. Nat. Microbiol. 2017, 2. [Google Scholar] [CrossRef] [Green Version]
- Van Wijk, S.J.L.; Fricke, F.; Herhaus, L.; Gupta, J.; Hötte, K.; Pampaloni, F.; Grumati, P.; Kaulich, M.; Sou, Y.S.; Komatsu, M.; et al. Linear ubiquitination of cytosolic Salmonella Typhimurium activates NF-κB and restricts bacterial proliferation. Nat. Microbiol. 2017, 2. [Google Scholar] [CrossRef]
- Manzanillo, P.S.; Ayres, J.S.; Watson, R.O.; Collins, A.C.; Souza, G.; Rae, C.S.; Schneider, D.S.; Nakamura, K.; Shiloh, M.U.; Cox, J.S. The ubiquitin ligase parkin mediates resistance to intracellular pathogens. Nature 2013, 501, 512–516. [Google Scholar] [CrossRef] [Green Version]
- Mostowy, S.; Sancho-Shimizu, V.; Hamon, M.A.; Simeone, R.; Brosch, R.; Johansen, T.; Cossart, P. p62 and NDP52 proteins target intracytosolic Shigella and Listeria to different autophagy pathways. J. Biol. Chem. 2011, 286, 26987–26995. [Google Scholar] [CrossRef] [Green Version]
- Zheng, Y.T.; Shahnazari, S.; Brech, A.; Lamark, T.; Johansen, T.; Brumell, J.H. The Adaptor Protein p62/SQSTM1 Targets Invading Bacteria to the Autophagy Pathway. J. Immunol. 2009, 183, 5909–5916. [Google Scholar] [CrossRef] [Green Version]
- Thurston, T.L.M. The tbk1 adaptor and autophagy receptor ndp52 restricts the proliferation of ubiquitin-coated bacteria. Nat. Immunol. 2009, 10, 1215–1222. [Google Scholar] [CrossRef]
- Bogunovic, D.; Byun, M.; Durfee, L.A.; Abhyankar, A.; Sanal, O.; Mansouri, D.; Salem, S.; Radovanovic, I.; Grant, A.V.; Adimi, P.; et al. Mycobacterial disease and impaired IFN-γ immunity in humans with inherited ISG15 deficiency. Science 2012, 337, 1684–1688. [Google Scholar] [CrossRef] [Green Version]
- Zhang, X.; Bogunovic, D.; Payelle-Brogard, B.; Francois-Newton, V.; Speer, S.D.; Yuan, C.; Volpi, S.; Li, Z.; Sanal, O.; Mansouri, D.; et al. Human intracellular ISG15 prevents interferon-α/β over-amplification and auto-inflammation. Nature 2015, 517, 89–93. [Google Scholar] [CrossRef]
- Singh, R.; Kaushik, S.; Wang, Y.; Xiang, Y.; Novak, I.; Komatsu, M.; Tanaka, K.; Cuervo, A.M.; Czaja, M.J. Autophagy regulates lipid metabolism. Nature 2009, 458, 1131–1135. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rui, Y.N.; Xu, Z.; Patel, B.; Chen, Z.; Chen, D.; Tito, A.; David, G.; Sun, Y.; Stimming, E.F.; Bellen, H.J.; et al. Huntingtin functions as a scaffold for selective macroautophagy. Nat. Cell Biol. 2015, 17, 262–275. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Spandl, J.; Lohmann, D.; Kuerschner, L.; Moessinger, C.; Thiele, C. Ancient ubiquitous protein 1 (AUP1) localizes to lipid droplets and binds the E2 ubiquitin conjugase G2 (Ube2g2) via its G2 binding region. J. Biol. Chem. 2011, 286, 5599–5606. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, L.; Zhou, J.; Yan, S.; Lei, G.; Lee, C.H.; Yin, X.M. Ethanol-triggered Lipophagy Requires SQSTM1 in AML12 Hepatic Cells. Sci. Rep. 2017, 7, 1–13. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Shoji, J.Y.; Kikuma, T.; Arioka, M.; Kitamoto, K. Macroautophagy-mediated degradation of whole nuclei in the filamentous fungus Aspergillus oryzae. PLoS ONE 2010, 5. [Google Scholar] [CrossRef] [Green Version]
- Papandreou, M.E.; Tavernarakis, N. Nucleophagy: From homeostasis to disease. Cell Death Differ. 2019, 26, 630–639. [Google Scholar] [CrossRef] [Green Version]
- Krick, R.; Muehe, Y.; Prick, T.; Bremer, S.; Schlotterhose, P.; Eskelinen, E.L.; Millen, J.; Goldfarb, D.S.; Thumm, M. Piecemeal microautophagy of the nucleus requires the core macroautophagy genes. Mol. Biol. Cell 2008, 19, 4492–4505. [Google Scholar] [CrossRef] [Green Version]
- Millen, J.I.; Krick, R.; Prick, T.; Thumm, M.; Goldfarb, D.S. Measuring piecemeal microautophagy of the nucleus in Saccharomyces cerevisiae. Autophagy 2009, 5, 75–81. [Google Scholar] [CrossRef] [Green Version]
- Mochida, K.; Oikawa, Y.; Kimura, Y.; Kirisako, H.; Hirano, H.; Ohsumi, Y.; Nakatogawa, H. Receptor-mediated selective autophagy degrades the endoplasmic reticulum and the nucleus. Nature 2015, 522, 359–362. [Google Scholar] [CrossRef] [PubMed]
- Akinduro, O.; Sully, K.; Patel, A.; Robinson, D.J.; Chikh, A.; McPhail, G.; Braun, K.M.; Philpott, M.P.; Harwood, C.A.; Byrne, C.; et al. Constitutive Autophagy and Nucleophagy during Epidermal Differentiation. J. Investig. Dermatol. 2016, 136, 1460–1470. [Google Scholar] [CrossRef] [Green Version]
- Li, Y.; Jiang, X.; Zhang, Y.; Gao, Z.; Liu, Y.; Hu, J.; Hu, X.; Li, L.; Shi, J.; Gao, N. Nuclear accumulation of UBC9 contributes to SUMOylation of lamin A/C and nucleophagy in response to DNA damage. J. Exp. Clin. Cancer Res. 2019, 38, 67. [Google Scholar] [CrossRef]
- Ji, C.H.; Kim, H.Y.; Heo, A.J.; Lee, M.J.; Park, D.Y.; Kim, D.H.; Kim, B.Y.; Kwon, Y.T. Regulation of reticulophagy by the N-degron pathway. Autophagy 2020, 16, 373–375. [Google Scholar] [CrossRef] [PubMed]
- Rea, S.L.; Majcher, V.; Searle, M.S.; Layfield, R. SQSTM1 mutations-Bridging Paget disease of bone and ALS/FTLD. Exp. Cell Res. 2014, 325, 27–37. [Google Scholar] [CrossRef] [PubMed]
- Fuqua, J.D.; Mere, C.P.; Kronemberger, A.; Blomme, J.; Bae, D.; Turner, K.D.; Harris, M.P.; Scudese, E.; Edwards, M.; Ebert, S.M.; et al. ULK2 is essential for degradation of ubiquitinated protein aggregates and homeostasis in skeletal muscle. FASEB J. 2019, 33, 11735–12745. [Google Scholar] [CrossRef] [Green Version]
- Verlhac, P.; Grégoire, I.P.; Azocar, O.; Petkova, D.S.; Baguet, J.; Viret, C.; Faure, M. Autophagy receptor NDP52 regulates pathogen-containing autophagosome maturation. Cell Host Microbe 2015, 17, 515–525. [Google Scholar] [CrossRef] [Green Version]
- Whang, M.I.; Tavares, R.M.; Benjamin, D.I.; Debnath, J.; Malynn, B.A.; Kattah, M.G.; Advincula, R.; Nomura, D.K.; Ma, A. The Ubiquitin Binding Protein TAX1BP1 Mediates Autophagosome Induction and the Metabolic Transition of Activated T Cells. Immunity 2017, 46, 405–420. [Google Scholar] [CrossRef] [Green Version]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Vainshtein, A.; Grumati, P. Selective Autophagy by Close Encounters of the Ubiquitin Kind. Cells 2020, 9, 2349. https://doi.org/10.3390/cells9112349
Vainshtein A, Grumati P. Selective Autophagy by Close Encounters of the Ubiquitin Kind. Cells. 2020; 9(11):2349. https://doi.org/10.3390/cells9112349
Chicago/Turabian StyleVainshtein, Anna, and Paolo Grumati. 2020. "Selective Autophagy by Close Encounters of the Ubiquitin Kind" Cells 9, no. 11: 2349. https://doi.org/10.3390/cells9112349