The ubiquitin-proteasome system and autophagy: Coordinated and independent activities

International Journal of Biochemistry and Cell Biology

Volumn 79, Issue , 2016, Pages 403-418

  Cohen Kaplan, Victoria ^a   Livneh, Ido ^a   Avni, Noa ^a   Cohen Rosenzweig, Chen ^a   Ciechanover, Aaron ^a  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

Autophagy; Ubiquitin Proteasome System

Indexed keywords

AUTOPHAGY LINKED FYVE PROTEIN; CALMODULIN; CBL PROTEIN; CYCLIN DEPENDENT KINASE; HEAT SHOCK COGNATE PROTEIN 70; HISTONE DEACETYLASE 6; I KAPPA B ALPHA; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; OPTINEURIN; OVALBUMIN; PROTEASOME; PROTEIN P62; PROTEIN P97; PROTEIN TOLLIP; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FUNDC1; TRANSCRIPTION FACTOR NBR1; TRANSCRIPTION FACTOR NCOA4; TRANSCRIPTION FACTOR NDP52; TRANSCRIPTION FACTOR NIX; TRANSCRIPTION FACTOR NRF1; TRANSCRIPTION FACTOR RPN10; TRANSCRIPTION FACTOR SMURF1; TRANSCRIPTION FACTOR TAX1BP; TRANSCRIPTION FACTOR TECPR1; TRIPARTITE MOTIF PROTEIN 5; TROPONIN C; UBIQUITIN; UNCLASSIFIED DRUG;

AGGRESOME; ANTIGEN PRESENTATION; APOPTOSIS; AUTOPHAGOSOME; AUTOPHAGY; CELL CYCLE REGULATION; CELL DIFFERENTIATION; CELL MATURATION; CELL SURVIVAL; CROSS PRESENTATION; ENZYME ACTIVITY; ENZYME ENGINEERING; ENZYME SUBSTRATE; HUMAN; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN HOMEOSTASIS; PROTEIN INTERACTION; REVIEW; UBIQUITINATION; XENOPHAGY; ANIMAL; METABOLISM;

ANIMALS; AUTOPHAGY; HUMANS; PROTEASOME ENDOPEPTIDASE COMPLEX; UBIQUITIN;

EID: 84979266913     PISSN: 13572725     EISSN: 18785875     Source Type: Journal    
DOI: 10.1016/j.biocel.2016.07.019     Document Type: Review

References (286)

1. Abada, A., Elazar, Z., Getting ready for building: signaling and autophagosome biogenesis. EMBO Rep. 15 (2014), 839–852, 10.15252/embr.201439076.
2. Agarraberes, F.A., Dice, J.F., A molecular chaperone complex at the lysosomal membrane is required for protein translocation. J. Cell Sci. 114 (2001), 2491–2499.
3. Aguzzi, A., O'Connor, T., Protein aggregation diseases: pathogenicity and therapeutic perspectives. Nat. Rev. Drug Discov. 9 (2010), 237–248, 10.1038/nrd3050.
4. Alkalay, I., Yaron, A., Hatzubai, A., Orian, A., Ciechanover, A., Ben-Neriah, Y., Stimulation-dependent I kappa B alpha phosphorylation marks the NF-kappa B inhibitor for degradation via the ubiquitin-proteasome pathway. Proc. Natl. Acad. Sci. U. S. A. 92 (1995), 10599–10603.
5. Apcher, S., Prado Martins, R., Fåhraeus, R., The source of MHC class I presented peptides and its implications. Curr. Opin. Immunol. 40 (2016), 117–122, 10.1016/j.coi.2016.04.002.
6. Arndt, V., Dick, N., Tawo, R., Dreiseidler, M., Wenzel, D., Hesse, M., et al. Chaperone-assisted selective autophagy is essential for muscle maintenance. Curr. Biol. 20 (2010), 143–148, 10.1016/j.cub.2009.11.022.
7. Arnold, J.E., Developmental changes of the 26 S proteasome in abdominal intersegmental muscles of Manduca sexta during programmed cell death. J. Biol. Chem. 270 (1995), 1850–1858, 10.1074/jbc.270.4.1850.
8. Arrasate, M., Mitra, S., Schweitzer, E.S., Segal, M.R., Finkbeiner, S., Inclusion body formation reduces levels of mutant huntingtin and the risk of neuronal death. Nature 431 (2004), 805–810, 10.1038/nature02998.
9. Babu, J.R., Geetha, T., Wooten, M.W., Sequestosome 1/p62 shuttles polyubiquitinated tau for proteasomal degradation. J. Neurochem. 94 (2005), 192–203, 10.1111/j.1471-4159.2005.03181.x.
10. Baerga, R., Zhang, Y., Chen, P.-H., Goldman, S., Jin, S., Targeted deletion of autophagy-related 5 (atg5) impairs adipogenesis in a cellular model and in mice. Autophagy 5 (2009), 1118–1130.
11. Baldassarre, G., Boccia, A., Bruni, P., Sandomenico, C., Barone, M., Pepe, V., et al. Retinoic acid induces neuronal differentiation of embryonal carcinoma cells by reducing proteasome-dependent proteolysis of the cyclin-dependent inhibitor p27. Cell Growth Differ. 11 (2000), 517–526.
12. Bandyopadhyay, U., Kaushik, S., Varticovski, L., Cuervo, A.M., The chaperone-mediated autophagy receptor organizes in dynamic protein complexes at the lysosomal membrane. Mol. Cell. Biol. 28 (2008), 5747–5763, 10.1128/MCB.02070-07.
13. Bandyopadhyay, U., Sridhar, S., Kaushik, S., Kiffin, R., Cuervo, A.M., Identification of regulators of chaperone-mediated autophagy. Mol. Cell 39 (2010), 535–547, 10.1016/j.molcel.2010.08.004.
14. Bar-Peled, L., Sabatini, D.M., Regulation of mTORC1 by amino acids. Trends Cell Biol. 24 (2014), 400–406, 10.1016/j.tcb.2014.03.003.
15. Baugh, J.M., Viktorova, E.G., Pilipenko, E.V., Proteasomes can degrade a significant proportion of cellular proteins independent of ubiquitination. J. Mol. Biol. 386 (2009), 814–827, 10.1016/j.jmb.2008.12.081.
16. Ben-Nissan, G., Sharon, M., Regulating the 20 S proteasome ubiquitin-independent degradation pathway. Biomolecules 4 (2014), 862–884, 10.3390/biom4030862.
17. Benaroudj, N., Tarcsa, E., Cascio, P., Goldberg, A.L., The unfolding of substrates and ubiquitin-independentprotein degradation by proteasomes. Biochimie 83 (2001), 311–318, 10.1016/S0300-9084(01)01244-5.
18. Bernardi, R., Liebermann, D.A., Hoffman, B., Cdc25A stability is controlled by the ubiquitin-proteasome pathway during cell cycle progression and terminal differentiation. Oncogene 19 (2000), 2447–2454, 10.1038/sj.onc.1203564.
19. Bersuker, K., Brandeis, M., Kopito, R.R., Protein misfolding specifies recruitment to cytoplasmic inclusion bodies. J. Cell Biol. 213 (2016), 229–241, 10.1083/jcb.201511024.
20. Bjørkøy, G., Lamark, T., Brech, A., Outzen, H., Perander, M., Overvatn, A., et al. p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J. Cell Biol. 171 (2005), 603–614, 10.1083/jcb.200507002.
21. Bonifacino, J.S., Suzuki, C.K., Lippincott-Schwartz, J., Weissman, A.M., Klausner, R.D., Pre-golgi degradation of newly synthesized T-cell antigen receptor chains: intrinsic sensitivity and the role of subunit assembly. J. Cell Biol. 109 (1989), 73–83.
22. Boutet, S.C., Disatnik, M.-H., Chan, L.S., Iori, K., Rando, T.A., Regulation of Pax3 by proteasomal degradation of monoubiquitinated protein in skeletal muscle progenitors. Cell 130 (2007), 349–362, 10.1016/j.cell.2007.05.044.
23. Bradley, M., Hayflick, L., Schimke, T., Protein degradation in human fibroblasts (WI-38). Effects of aging viral transformation, and amino acid analogs. J. Biol. Chem. 251 (1975), 3521–3529.
24. Braten, O., Livneh, I., Ziv, T., Admon, A., Kehat, I., Caspi, L.H., et al. Numerous proteins with unique characteristics are degraded by the 26 S proteasome following monoubiquitination. Proc. Natl. Acad. Sci., 2016, 10.1073/pnas.1608644113 201608644.
25. Breitschopf, K., Haendeler, J., Malchow, P., Zeiher, A.M., Dimmeler, S., Posttranslational modification of Bcl-2 facilitates its proteasome-dependent degradation: molecular characterization of the involved signaling pathway. Mol. Cell. Biol. 20 (2000), 1886–1896, 10.1128/MCB.20.5.1886-1896.2000.
26. Burnett, B.G., Pittman, R.N., The polyglutamine neurodegenerative protein ataxin 3 regulates aggresome formation. Proc. Natl. Acad. Sci. U. S. A. 102 (2005), 4330–4335, 10.1073/pnas.0407252102.
27. Canu, N., Barbato, C., Ciotti, M.T., Serafino, A., Dus, L., Calissano, P., Proteasome involvement and accumulation of ubiquitinated proteins in cerebellar granule neurons undergoing apoptosis. J. Neurosci. 20 (2000), 589–599.
28. Carvallo, L., Muñoz, R., Bustos, F., Escobedo, N., Carrasco, H., Olivares, G., et al. Non-canonical Wnt signaling induces ubiquitination and degradation of Syndecan4. J. Biol. Chem. 285 (2010), 29546–29555, 10.1074/jbc.M110.155812.
29. Catzavelos, C., Bhattacharya, N., Ung, Y.C., Wilson, J.A., Roncari, L., Sandhu, et al. Decreased levels of the cell-cycle inhibitor p27Kip1 protein: prognostic implications in primary breast cancer. Nat. Med. 3 (1997), 227–230, 10.1038/nm0297-227.
30. Chan, N.C., Salazar, A.M., Pham, A.H., Sweredoski, M.J., Kolawa, N.J., Graham, et al. Broad activation of the ubiquitin-proteasome system by Parkin is critical for mitophagy. Hum. Mol. Genet. 20 (2011), 1726–1737, 10.1093/hmg/ddr048.
31. Chen, D., Fan, W., Lu, Y., Ding, X., Chen, S., Zhong, Q., A mammalian autophagosome maturation mechanism mediated by TECPR1 and the Atg12-Atg5 conjugate. Mol. Cell 45 (2012), 629–641, 10.1016/j.molcel.2011.12.036.
32. Cheong, H., Lindsten, T., Wu, J., Lu, C., Thompson, C.B., Ammonia-induced autophagy is independent of ULK1/ULK2 kinases. Proc. Natl. Acad. Sci. U. S. A. 108 (2011), 11121–11126, 10.1073/pnas.1107969108.
33. Chew, K.C.M., Matsuda, N., Saisho, K., Lim, G.G.Y., Chai, C., Tan, et al. Parkin mediates apparent E2-independent monoubiquitination in vitro and contains an intrinsic activity that catalyzes polyubiquitination. PLoS One, 6, 2011, e19720, 10.1371/journal.pone.0019720.
34. Chiarle, R., Budel, L.M., Skolnik, J., Frizzera, G., Chilosi, M., Corato, A., et al. Increased proteasome degradation of cyclin-dependent kinase inhibitor p27 is associated with a decreased overall survival in mantle cell lymphoma. Blood 95 (2000), 619–626.
35. Choe, K.P., Przybysz, A.J., Strange, K., The WD40 repeat protein WDR-23 functions with the CUL4/DDB1 ubiquitin ligase to regulate nuclear abundance and activity of SKN-1 in Caenorhabditis elegans. Mol. Cell. Biol. 29 (2009), 2704–2715, 10.1128/MCB.01811-08.
36. Chondrogianni, N., Tzavelas, C., Pemberton, A.J., Nezis, I.P., Rivett, A.J., Gonos, E.S., Overexpression of proteasome β5 subunit increases the amount of assembled proteasome and confers ameliorated response to oxidative stress and higher survival rates. J. Biol. Chem. 280 (2005), 11840–11850, 10.1074/jbc.M413007200.
37. Ciechanover, A., The ubiquitin-proteasome proteolytic pathway. Cell 79 (1994), 13–21, 10.1016/0092-8674(94)90396-4.
38. Codogno, P., Mehrpour, M., Proikas-Cezanne, T., Canonical and non-canonical autophagy: variations on a common theme of self-eating?. Nat. Rev. Mol. Cell Biol., 13, 2011, 7, 10.1038/nrm3249.
39. Collins, C.A., De Mazière, A., van Dijk, S., Carlsson, F., Klumperman, J., Brown, E.J., Atg5-independent sequestration of ubiquitinated mycobacteria. PLoS Pathog., 5, 2009, e1000430, 10.1371/journal.ppat.1000430.
40. Cuervo, A.M., Dice, J.F., A receptor for the selective uptake and degradation of proteins by lysosomes. Science 273 (1996), 501–503.
41. Cuervo, A.M., Hu, W., Lim, B., Dice, J.F., IkappaB is a substrate for a selective pathway of lysosomal proteolysis. Mol. Biol. Cell 9 (1998), 1995–2010.
42. Dargemont, C., Ossareh-Nazari, B., Cdc48/p97, a key actor in the interplay between autophagy and ubiquitin/proteasome catabolic pathways. Biochim. Biophys. Acta 1823 (2012), 138–144, 10.1016/j.bbamcr.2011.07.011.
43. Davies, K.J., Degradation of oxidized proteins by the 20 S proteasome. Biochimie 83 (2001), 301–310.
44. Deosaran, E., Larsen, K.B., Hua, R., Sargent, G., Wang, Y., Kim, S., et al. NBR1 acts as an autophagy receptor for peroxisomes. J. Cell Sci. 126 (2013), 939–952, 10.1242/jcs.114819.
45. Desai, M., Fang, R., Sun, J., The role of autophagy in microbial infection and immunity. Immuno Targets Ther., Volume 4, 2015, 13, 10.2147/ITT.S76720.
46. Dice, J.F., Dehlinger, P.J., Schimke, R.T., Studies on the correlation between size and relative degradation rate of soluble proteins. J. Biol. Chem. 248 (1973), 4220–4228.
47. Dice, J.F., Selective degradation of cytosolic proteins by lysosomes. Ann. N. Y. Acad. Sci. 674 (1992), 58–64.
48. Dick, L.R., Aldrich, C., Jameson, S.C., Moomaw, C.R., Pramanik, B.C., Doyle, C.K., et al. Proteolytic processing of ovalbumin and beta-galactosidase by the proteasome to a yield antigenic peptides. J. Immunol. 152 (1994), 3884–3894.
49. Dimmeler, S., Breitschopf, K., Haendeler, J., Zeiher, A.M., Dephosphorylation targets Bcl-2 for ubiquitin-dependent degradation: a link between the apoptosome and the proteasome pathway. J. Exp. Med. 189 (1999), 1815–1822, 10.1084/jem.189.11.1815.
50. Ding, W.X., Yin, X.M., Sorting, recognition and activation of the misfolded protein degradation pathways through macroautophagy and the proteasome. Autophagy 4 (2008), 141–150, 10.4161/auto.5190.
51. Djavaheri-Mergny, M., Codogno, P., Autophagy joins the game to regulate NF-kappaB signaling pathways. Cell Res. 17 (2007), 576–577, 10.1038/cr.2007.58.
52. Dowdle, W.E., Nyfeler, B., Nagel, J., Elling, R.A., Liu, S., Triantafellow, E., et al. Selective VPS34 inhibitor blocks autophagy and uncovers a role for NCOA4 in ferritin degradation and iron homeostasis in vivo. Nat. Cell Biol. 16 (2014), 1069–1079, 10.1038/ncb3053.
53. Elsasser, S., Gali, R.R., Schwickart, M., Larsen, C.N., Leggett, D.S., Müller, et al. Proteasome subunit Rpn1 binds ubiquitin-like protein domains. Nat. Cell Biol. 4 (2002), 725–730, 10.1038/ncb845.
54. Essén, P., McNurlan, M., a Wernerman, J., Vinnars, E., Garlick, P.J., Uncomplicated surgery, but not general anesthesia, decreases muscle protein synthesis. Am. J. Physiol. 262 (1992), E253–60.
55. Evans, W.J., Skeletal muscle loss: cachexia, sarcopenia, and inactivity. Am. J. Clin. Nutr. 91 (2010), 1123–1127, 10.3945/ajcn.2010.28608A.
56. Felig, P., Amino acid metabolism in man. Annu. Rev. Biochem. 44 (1975), 933–955.
57. Filimonenko, M., Isakson, P., Finley, K.D., Anderson, M., Jeong, H., Melia, et al. The selective macroautophagic degradation of aggregated proteins requires the PI3P-binding protein Alfy. Mol. Cell 38 (2010), 265–279, 10.1016/j.molcel.2010.04.007.
58. Finley, D., Chen, X., Walters, K.J., Gates, channels, and switches: elements of the proteasome machine. Trends Biochem. Sci. 41 (2016), 77–93, 10.1016/j.tibs.2015.10.009.
59. Finley, D., Recognition and processing of ubiquitin-protein conjugates by the proteasome. Annu. Rev. Biochem. 78 (2009), 477–513, 10.1146/annurev.biochem.78.081507.101607.
60. Fortmann, K.T., Lewis, R.D., Ngo, K.A., Fagerlund, R., Hoffmann, A., A regulated, ubiquitin-independent degron in IκBα. J. Mol. Biol. 427 (2015), 2748–2756, 10.1016/j.jmb.2015.07.008.
61. Fribley, A., Wang, C.-Y., Proteasome inhibitor induces apoptosis through induction of endoplasmic reticulum stress. Cancer Biol. Ther. 5 (2006), 745–748.
62. Fu, H., Sadis, S., Rubin, D.M., Glickman, M., Van Nocker, S., Finley, D., et al. Multiubiquitin chain binding and protein degradation are mediated by distinct domains within the 26 S proteasome subunit Mcb1. J. Biol. Chem. 273 (1998), 1970–1981, 10.1074/jbc.273.4.1970.
63. Fuchs, Y., Steller, H., Programmed cell death in animal development and disease. Cell 147 (2011), 742–758, 10.1016/j.cell.2011.10.033.
64. Fuertes, G., Martín De Llano, J.J., Villarroya, A., Rivett, A.J., Knecht, E., Changes in the proteolytic activities of proteasomes and lysosomes in human fibroblasts produced by serum withdrawal, amino-acid deprivation and confluent conditions. Biochem. J. 375 (2003), 75–86, 10.1042/BJ20030282.
65. Fuertes, G., Villarroya, A., Knecht, E., Role of proteasomes in the degradation of short-lived proteins in human fibroblasts under various growth conditions. Int. J. Biochem. Cell Biol. 35 (2003), 651–664, 10.1016/S1357-2725(02)00382-5.
66. Funakoshi, M., Sasaki, T., Nishimoto, T., Kobayashi, H., Budding yeast Dsk2p is a polyubiquitin-binding protein that can interact with the proteasome. Proc. Natl. Acad. Sci. U. S. A. 99 (2002), 745–750, 10.1073/pnas.012585199.
67. Fusco, C., Micale, L., Egorov, M., Monti, M., D'Addetta, E.V., Augello, B., et al. The E3-ubiquitin ligase TRIM50 interacts with HDAC6 and p62, and promotes the sequestration and clearance of ubiquitinated proteins into the aggresome. PLoS One, 7, 2012, e40440, 10.1371/journal.pone.0040440.
68. Galan, J.M., Haguenauer-Tsapis, R., Ubiquitin lys63 is involved in ubiquitination of a yeast plasma membrane protein. EMBO J. 16 (1997), 5847–5854, 10.1093/emboj/16.19.5847.
69. Gallastegui, N., Groll, M., The 26 S proteasome: assembly and function of a destructive machine. Trends Biochem. Sci. 35 (2010), 634–642, 10.1016/j.tibs.2010.05.005.
70. Gamerdinger, M., Hajieva, P., Kaya, A.M., Wolfrum, U., Hartl, F.U., Behl, C., Protein quality control during aging involves recruitment of the macroautophagy pathway by BAG3. EMBO J. 28 (2009), 889–901, 10.1038/emboj.2009.29.
71. Gamerdinger, M., Carra, S., Behl, C., Emerging roles of molecular chaperones and co-chaperones in selective autophagy: focus on BAG proteins. J. Mol. Med. (Berl) 89 (2011), 1175–1182, 10.1007/s00109-011-0795-6.
72. Ganley, I.G., Lam, DuH., Wang, J., Ding, X., Chen, S., Jiang, X., ULK1. ATG13. FIP200 complex mediates mTOR signaling and is essential for autophagy. J. Biol. Chem., 2009, 12297–12305, 10.1074/jbc.M900573200.
73. García-Mata, R., Bebök, Z., Sorscher, E.J., Sztul, E.S., Characterization and dynamics of aggresome formation by a cytosolic GFP-chimera. J. Cell Biol. 146 (1999), 1239–1254.
74. 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. 12 (2010), 119–131, 10.1038/ncb2012.
75. Geng, J., Klionsky, D.J., The Atg8 and Atg12 ubiquitin-like conjugation systems in macroautophagy. Protein modifications: beyond the usual suspects review series. EMBO Rep. 9 (2008), 859–864, 10.1038/embor.2008.163.
76. Geng, J., Nair, U., Yasumura-Yorimitsu, K., Klionsky, D.J., Post-golgi Sec proteins are required for autophagy in saccharomyces cerevisiae. Mol. Biol. Cell 21 (2010), 2257–2269, 10.1091/mbc.E09-11-0969.
77. Grasso, D., Ropolo, A., Lo Ré, A., Boggio, V., Molejón, M.I., Iovanna, J.L., et al. Zymophagy, a novel selective autophagy pathway mediated by VMP1-USP9x-p62, prevents pancreatic cell death. J. Biol. Chem. 286 (2011), 8308–8324, 10.1074/jbc.M110.197301.
78. Grimm, L.M., Goldberg, A.L., Poirier, G.G., Schwartz, L.M., Osborne, B.A., Proteasomes play an essential role in thymocyte apoptosis. EMBO J. 15 (1996), 3835–3844.
79. Hanada, T., Noda, N.N., Satomi, Y., Ichimura, Y., Fujioka, Y., Takao, T., et al. The Atg12-Atg5 conjugate has a novel E3-like activity for protein lipidation in autophagy. J. Biol. Chem. 282 (2007), 37298–37302.
80. Hao, Q., Jiao, S., Shi, Z., Li, C., Meng, X., Zhang, Z., et al. A non-canonical role of the p97 complex in RIG-I antiviral signaling. EMBO J. 34 (2015), 2903–2920, 10.15252/embj.201591888.
81. Hara, T., Nakamura, K., Matsui, M., Yamamoto, A., Nakahara, Y., Suzuki-Migishima, R., et al. Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature 441 (2006), 885–889, 10.1038/nature04724.
82. Haracska, L., Udvardy, A., Mapping the ubiquitin-binding domains in the p54 regulatory complex subunit of the Drosophila 26 S protease. FEBS Lett. 412 (1997), 331–336, 10.1016/S0014-5793(97)00808-9.
83. Hartl, F.U., Molecular chaperones in cellular protein folding. Nature 381 (1996), 571–579, 10.1038/381571a0.
84. Hershko, A., Ciechanover, A., The ubiquitin system. Annu. Rev. Biochem. 67 (1998), 425–479, 10.1146/annurev.biochem.67.1.425.
85. Hirano, H., Kimura, Y., Kimura, A., Biological significance of co- and post-translational modifications of the yeast 26 S proteasome. J. Proteomics 134 (2015), 37–46, 10.1016/j.jprot.2015.11.016.
86. Hiyama, H., Yokoi, M., Masutani, C., Sugasawa, K., Maekawa, T., Tanaka, et al. Interaction of hHR23 with S5a. The ubiquitin-like domain of hHR23 mediates interaction with S5a subunit of 26 S proteasome. J. Biol. Chem. 274 (1999), 28019–28025.
87. Hofmann, R.M., Pickart, C.M., In vitro assembly and recognition of Lys-63 polyubiquitin chains. J. Biol. Chem. 276 (2001), 27936–27943, 10.1074/jbc.M103378200.
88. Hosokawa, N., Hara, T., Kaizuka, T., Kishi, C., Takamura, A., Miura, Y., et al. Nutrient-dependent mTORC1 association with the ULK1-Atg13-FIP200 complex required for autophagy. Mol. Biol. Cell 20 (2009), 1981–1991, 10.1091/mbc.E08-12-1248.
89. Hurle, M.R., Helms, L.R., Li, L., Chan, W., Wetzel, R., A role for destabilizing amino acid replacements in light-chain amyloidosis. Proc. Natl. Acad. Sci. U. S. A. 91 (1994), 5446–5450.
90. Husnjak, K., Elsasser, S., Zhang, N., Chen, X., Randles, L., Shi, Y., et al. Proteasome subunit Rpn13 is a novel ubiquitin receptor. Nature 453 (2008), 481–488, 10.1038/nature06926.
91. Hyttinen, J.M.T., Amadio, M., Viiri, J., Pascale, A., Salminen, A., Kaarniranta, K., Clearance of misfolded and aggregated proteins by aggrephagy and implications for aggregation diseases. Ageing Res. Rev. 18 (2014), 16–28, 10.1016/j.arr.2014.07.002.
92. Ikeda, F., Dikic, I., Atypical ubiquitin chains: new molecular signals. Protein modifications: beyond the usual suspects review series. EMBO Rep. 9 (2008), 536–542, 10.1038/embor.2008.93.
93. Jänen, S.B., Chaachouay, H., Richter-Landsberg, C., Autophagy is activated by proteasomal inhibition and involved in aggresome clearance in cultured astrocytes. Glia 58 (2010), 1766–1774, 10.1002/glia.21047.
94. Jia, L., Gopinathan, G., Sukumar, J.T., Gribben, J.G., Blocking autophagy prevents bortezomib-induced NF-κB activation by reducing I-κBα degradation in lymphoma cells. PLoS One, 7, 2012, e32584, 10.1371/journal.pone.0032584.
95. Joffre, O.P., Segura, E., Savina, A., Amigorena, S., Cross-presentation by dendritic cells. Nat. Rev. Immunol. 12 (2012), 557–569, 10.1038/nri3254.
96. Johnston, J.A., Ward, C.L., Kopito, R.R., Aggresomes: a cellular response to misfolded proteins. J. Cell Biol. 143 (1998), 1883–1898, 10.1083/jcb.143.7.1883.
97. Josefsberg, L.B., Kaufman, O., Galiani, D., Kovo, M., Dekel, N., Inactivation of M-phase promoting factor at exit from first embryonic mitosis in the rat is independent of cyclin B1 degradation. Biol. Reprod. 64 (2001), 871–878.
98. Josefsberg, L.B.-Y., The proteasome is involved in the first metaphase-to-anaphase transition of meiosis in rat oocytes. Biol. Reprod. 62 (2000), 1270–1277, 10.1095/biolreprod62.5.1270.
99. Ju, J.S., Weihl, C.C., p97/VCP at the intersection of the autophagy and the ubiquitin proteasome system. Autophagy 6 (2010), 283–285, 10.4161/auto.6.2.11063.
100. Jung, C., Jun, C., Ro, S., Kim, Y., Otto, N., Cao, J., et al. ULK-Atg13-FIP200 complexes mediate mTOR signaling to the autophagy machinery. Mol. Biol. Cell, 2009, 1992–2003, 10.1091/mbc.e08-12-1249.
101. Kabeya, Y., Mizushima, N., Ueno, T., Yamamoto, A., Kirisako, T., Noda, T., et al. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 19 (2000), 5720–5728, 10.1093/emboj/19.21.5720.
102. Kabuta, T., Suzuki, Y., Wada, K., Degradation of amyotrophic lateral sclerosis-linked mutant Cu, Zn-superoxide dismutase proteins by macroautophagy and the proteasome. J. Biol. Chem. 281 (2006), 30524–30533, 10.1074/jbc.M603337200.
103. Kaplun, L., Tzirkin, R., Bakhrat, A., Shabek, N., Ivantsiv, Y., Raveh, D., The DNA damage-inducible UbL-UbA protein Ddi1 participates in Mec1-mediated degradation of Ho endonuclease. Mol. Cell. Biol. 25 (2005), 5355–5362, 10.1128/MCB.25.13.5355-5362.2005.
104. Karin, M., Ben-Neriah, Y., Phosphorylation meets ubiquitination: the control of NF-[kappa]B activity. Annu. Rev. Immunol. 18 (2000), 621–663, 10.1146/annurev.immunol.18.1.621.
105. Karin, M., How NF-kappaB is activated: the role of the IkappaB kinase (IKK) complex. Oncogene 18 (1999), 6867–6874, 10.1038/sj.onc.1203219.
106. Kawahara, H., Philipova, R., Yokosawa, H., Patel, R., Tanaka, K., Whitaker, M., Inhibiting proteasome activity causes overreplication of DNA and blocks entry into mitosis in sea urchin embryos. J. Cell Sci. 113 (2000), 2659–2670.
107. Khaminets, A., Behl, C., Dikic, I., Ubiquitin-dependent and independent signals in selective autophagy. Trends Cell Biol. 26 (2016), 6–16, 10.1016/j.tcb.2015.08.010.
108. 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. U. S. A. 105 (2008), 20567–20574, 10.1073/pnas.0810611105.
109. Kim, J., Kundu, M., Viollet, B., Guan, K.-L., AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat. Cell Biol. 13 (2011), 132–141, 10.1038/ncb2152.
110. Kinnunen, P.K.J., Kaarniranta, K., Mahalka, A.K., Protein-oxidized phospholipid interactions in cellular signaling for cell death: from biophysics to clinical correlations. Biochim. Biophys. Acta 1818 (2012), 2446–2455, 10.1016/j.bbamem.2012.04.008.
111. Kirisako, T., Kamei, K., Murata, S., Kato, M., Fukumoto, H., Kanie, M., et al. A ubiquitin ligase complex assembles linear polyubiquitin chains. EMBO J. 25 (2006), 4877–4887, 10.1038/sj.emboj.7601360.
112. Kirkin, V., Lamark, T., Sou, Y.-S., Bjørkøy, G., Nunn, J.L., Bruun, J.-A., et al. A role for NBR1 in autophagosomal degradation of ubiquitinated substrates. Mol. Cell 33 (2009), 505–516, 10.1016/j.molcel.2009.01.020.
113. Kirkin, V., McEwan, D.G., Novak, I., Dikic, I., A role for ubiquitin in selective autophagy. Mol. Cell 34 (2009), 259–269, 10.1016/j.molcel.2009.04.026.
114. Knævelsrud, H., Søreng, K., Raiborg, C., Håberg, K., Rasmuson, F., Brech, A., et al. Membrane remodeling by the PX-BAR protein SNX18 promotes autophagosome formation. J. Cell Biol. 202 (2013), 331–349, 10.1083/jcb.201205129.
115. Koegl, M., Hoppe, T., Schlenker, S., Ulrich, H.D., Mayer, T.U., Jentsch, S., A novel ubiquitination factor E4, is involved in multiubiquitin chain assembly. Cell 96 (1999), 635–644, 10.1016/S0092-8674(00)80574-7.
116. Komatsu, M., Waguri, S., Koike, M., Sou, Y.-S., Ueno, T., Hara, T., et al. Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice. Cell 131 (2007), 1149–1163, 10.1016/j.cell.2007.10.035.
117. Korac, J., Schaeffer, V., Kovacevic, I., Clement, A.M., Jungblut, B., Behl, C., et al. Ubiquitin-independent function of optineurin in autophagic clearance of protein aggregates. J. Cell Sci. 126 (2013), 580–592, 10.1242/jcs.114926.
118. Kravtsova-Ivantsiv, Y., Cohen, S., Ciechanover, A., Modification by single ubiquitin moieties rather than polyubiquitination is sufficient for proteasomal processing of the p105 NF-kappaB precursor. Mol. Cell 33 (2009), 496–504, 10.1016/j.molcel.2009.01.023.
119. Kroemer, G., Mariño, G., Levine, B., Autophagy and the integrated stress response. Mol. Cell 40 (2010), 280–293, 10.1016/j.molcel.2010.09.023.
120. 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. 277 (2002), 18619–18625, 10.1074/jbc.M111889200.
121. Kuma, A., Hatano, M., Matsui, M., Yamamoto, A., Nakaya, H., Yoshimori, T., et al. The role of autophagy during the early neonatal starvation period. Nature 432 (2004), 1032–1036, 10.1038/nature03029.
122. Kwak, M.-K., Wakabayashi, N., Greenlaw, J.L., Yamamoto, M., Kensler, T.W., Antioxidants enhance mammalian proteasome expression through the Keap1-Nrf2 signaling pathway. Mol. Cell. Biol. 23 (2003), 8786–8794, 10.1128/MCB.23.23.8786-8794.2003.
123. Löw, P., Bussell, K., Dawson, S., Billett, M., Mayer, R., Reynolds, S., Expression of a 26 S proteasome ATPase subunit MS73, in muscles that undergo developmentally programmed cell death, and its control by ecdysteroid hormones in the insect Manduca sexta. FEBS Lett. 400 (1997), 345–349, 10.1016/S0014-5793(96)01413-5.
124. Lamark, T., Kirkin, V., Dikic, I., Johansen, T., NBR1 and p62 as cargo receptors for selective autophagy of ubiquitinated targets. Cell Cycle 8 (2009), 1986–1990.
125. Laplante, M., Sabatini, D.M., mTOR signaling in growth control and disease. Cell 149 (2013), 274–293, 10.1016/j.cell.2012.03.017.mTOR.
126. Lazarou, M., Sliter, D.A., Kane, L.A., Sarraf, S.A., Wang, C., Burman, J.L., et al. The ubiquitin kinase PINK1 recruits autophagy receptors to induce mitophagy. Nature 524 (2015), 309–314, 10.1038/nature14893.
127. Lecker, S., Jagoe, R., Gilbert, A., Gomes, M., Baracos, V., Bailey, J., et al. Multiple types of skeletal muscle atrophy involve a common program of changes in gene expression. FASEB J. 18 (2004), 39–51, 10.1096/fj.03-0610com.
128. Lecker, S.H., Goldberg, A.L., Mitch, W.E., Protein degradation by the ubiquitin-proteasome pathway in normal and disease States. J. Am. Soc. Nephrol. 17 (2006), 1807–1819, 10.1681/ASN.2006010083.
129. Lee, D.H., Goldberg, A.L., Selective inhibitors of the proteasome-dependent and vacuolar pathways of protein degradation in saccharomyces cerevisiae. J. Biol. Chem. 271 (1996), 27280–27284, 10.1074/jbc.271.44.27280.
130. Lee, H.-J., Shin, S.Y., Choi, C., Lee, Y.H., Lee, S.-J., Formation and removal of alpha-synuclein aggregates in cells exposed to mitochondrial inhibitors. J. Biol. Chem. 277 (2002), 5411–5417.
131. Lee, J.-Y., Koga, H., Kawaguchi, Y., Tang, W., Wong, E., Gao, Y.-S., et al. HDAC6 controls autophagosome maturation essential for ubiquitin-selective quality-control autophagy. EMBO J. 29 (2010), 969–980, 10.1038/emboj.2009.405.
132. Lee, J.-Y., Nagano, Y., Taylor, J.P., Lim, K.L., Yao, T.-P., Disease-causing mutations in parkin impair mitochondrial ubiquitination, aggregation, and HDAC6-dependent mitophagy. J. Cell Biol. 189 (2010), 671–679, 10.1083/jcb.201001039.
133. Lehmann, A., Niewienda, A., Jechow, K., Janek, K., Enenkel, C., Ecm29 fulfils quality control functions in proteasome assembly. Mol. Cell 38 (2010), 879–888, 10.1016/j.molcel.2010.06.016.
134. Li, B., Dou, Q.P., Bax degradation by the ubiquitin/proteasome-dependent pathway: involvement in tumor survival and progression. Proc. Natl. Acad. Sci. U. S. A. 97 (2000), 3850–3855, 10.1073/pnas.070047997.
135. Li, X., Matilainen, O., Jin, C., Glover-Cutter, K.M., Holmberg, C.I., Blackwell, T.K., Specific SKN-1/NrF stress responses to perturbations in translation elongation and proteasome activity. PLoS Genet. 7 (2011), 9–11, 10.1371/journal.pgen.1002119.
136. Liang, C.-C., Wang, C., Peng, X., Gan, B., Guan, J.-L., Neural-specific deletion of FIP200 leads to cerebellar degeneration caused by increased neuronal death and axon degeneration. J. Biol. Chem. 285 (2010), 3499–3509, 10.1074/jbc.M109.072389.
137. Liu, C.-W., Corboy, M.J., DeMartino, G.N., Thomas, P.J., Endoproteolytic activity of the proteasome. Science 299 (2003), 408–411.
138. Liu, L., Feng, D., Chen, G., Chen, M., Zheng, Q., Song, P., et al. Mitochondrial outer-membrane protein FUNDC1 mediates hypoxia-induced mitophagy in mammalian cells. Nat. Cell Biol. 14 (2012), 177–185, 10.1038/ncb2422.
139. Livneh, I., Cohen-kaplan, V., Cohen-rosenzweig, C., Avni, N., Ciechanover, A., The life cycle of the 26 S proteasome: from birth, through regulation and function, and onto its death. Cell Res., 2016, 10.1038/cr.2016 in press.
140. Lokireddy, S., Kukushkin, N.V., Goldberg, A.L., cAMP-induced phosphorylation of 26 S proteasomes on Rpn6/PSMD11 enhances their activity and the degradation of misfolded proteins. Proc. Natl. Acad. Sci. 112 (2015), E7176–E7185, 10.1073/pnas.1522332112.
141. Lopes, U.G., Erhardt, P., Yao, R., Cooper, G.M., p53-dependent induction of apoptosis by proteasome inhibitors. J. Biol. Chem. 272 (1997), 12893–12896, 10.1074/jbc.272.20.12893.
142. Lowe, E.D., Hasan, N., Trempe, J.F., Fonso, L., Noble, M.E.M., Endicott, J.A., et al. Structures of the Dsk2 UBL and UBA domains and their complex. Acta Crystallogr. D Biol. Crystallogr. 62 (2006), 177–188, 10.1107/S0907444905037777.
143. Lu, K., Psakhye, I., Jentsch, S., Autophagic clearance of polyQ proteins mediated by ubiquitin-Atg8 adaptors of the conserved CUET protein family. Cell 158 (2014), 549–563, 10.1016/j.cell.2014.05.048.
144. Münz, C., Antigen processing for MHC presentation by autophagy. F1000 Biol. Rep., 2, 2010, 61, 10.3410/B2-61.
145. Münz, C., Antigen processing for MHC Class II presentation via autophagy. Front. Immunol., 3, 2012, 9, 10.3389/fimmu.2012.00009.
146. Münz, C., Autophagy proteins in antigen processing for presentation on MHC molecules. Immunol. Rev. 272 (2016), 17–27, 10.1111/imr.12422.
147. Maiuri, M.C., Zalckvar, E., Kimchi, A., Kroemer, G., Self-eating and self-killing: crosstalk between autophagy and apoptosis. Nat. Rev. Mol. Cell Biol. 8 (2007), 741–752, 10.1038/nrm2239.
148. Maki, C.G., Huibregtse, J.M., Howley, P.M., In vivo ubiquitination and proteasome-mediated degradation of p53(1). Cancer Res. 56 (1996), 2649–2654.
149. Mammucari, C., Milan, G., Romanello, V., Masiero, E., Rudolf, R., Del Piccolo, P., et al. FoxO3 controls autophagy in skeletal muscle in vivo. Cell Metab. 6 (2007), 458–471, 10.1016/j.cmet.2007.11.001.
150. Mancias, J.D., Wang, X., Gygi, S.P., Harper, J.W., Kimmelman, A.C., Quantitative proteomics identifies NCOA4 as the cargo receptor mediating ferritinophagy. Nature 509 (2014), 105–109, 10.1038/nature13148.
151. Mancias, J.D., Pontano Vaites, L., Nissim, S., Biancur, D.E., Kim, A.J., Wang, X., et al. Ferritinophagy via NCOA4 is required for erythropoiesis and is regulated by iron dependent HERC2-mediated proteolysis. Elife, 4, 2015, 10.7554/eLife.10308.
152. Mandell, M.A., Jain, A., Arko-Mensah, J., Chauhan, S., Kimura, T., Dinkins, C., et al. TRIM proteins regulate autophagy and can target autophagic substrates by direct recognition. Dev. Cell 30 (2014), 394–409, 10.1016/j.devcel.2014.06.013.
153. Marambio, P., Toro, B., Sanhueza, C., Troncoso, R., Parra, V., Verdejo, H., et al. Glucose deprivation causes oxidative stress and stimulates aggresome formation and autophagy in cultured cardiac myocytes. Biochim. Biophys. Acta 1802 (2010), 509–518, 10.1016/j.bbadis.2010.02.002.
154. Mariño, G., Niso-Santano, M., Baehrecke, E.H., Kroemer, G., Self-consumption: the interplay of autophagy and apoptosis. Nat. Rev. Mol. Cell Biol. 15 (2014), 81–94, 10.1038/nrm3735.
155. Marques, C., Guo, W., Pereira, P., Taylor, A., Patterson, C., Evans, P.C., et al. The triage of damaged proteins: degradation by the ubiquitin-proteasome pathway or repair by molecular chaperones. FASEB J. 20 (2006), 741–743, 10.1096/fj.05-5080fje.
156. Marshall, R.S., Li, F., Gemperline, D.C., Book, A.J., Vierstra, R.D., Autophagic degradation of the 26 S proteasome is mediated by the dual ATG8/Ubiquitin receptor RPN10 in Arabidopsis. Mol. Cell 58 (2015), 1053–1066, 10.1016/j.molcel.2015.04.023.
157. Massey, A.C., Zhang, C., Cuervo, A.M., Chaperone-mediated autophagy in aging and disease. Curr. Top. Dev. Biol. 73 (2006), 205–235.
158. Mathes, E., Wang, L., Komives, E., Ghosh, G., Flexible regions within IκBα create the ubiquitin-independent degradation signal. J. Biol. Chem. 285 (2010), 32927–32936, 10.1074/jbc.M110.107326.
159. Mathew, R., Karp, C.M., Beaudoin, B., Vuong, N., Chen, G., Chen, H.-Y., et al. Autophagy suppresses tumorigenesis through elimination of p62. Cell 137 (2009), 1062–1075, 10.1016/j.cell.2009.03.048.
160. McClellan, A.J., Tam, S., Kaganovich, D., Frydman, J., Protein quality control: chaperones culling corrupt conformations. Nat. Cell Biol. 7 (2005), 736–741, 10.1038/ncb0805-736.
161. McKeon, J.E., Sha, D., Li, L., Chin, L.-S., Parkin-mediated K63-polyubiquitination targets ubiquitin C-terminal hydrolase L1 for degradation by the autophagy-lysosome system. Cell. Mol. Life Sci. 72 (2015), 1811–1824, 10.1007/s00018-014-1781-2.
162. Meyer, H., Bug, M., Bremer, S., Emerging functions of the VCP/p97 AAA-ATPase in the ubiquitin system. Nat. Cell Biol. 14 (2012), 117–123, 10.1038/ncb2407.
163. Mizushima, N., Klionsky, D.J., Protein turnover via autophagy: implications for metabolism. Annu. Rev. Nutr. 27 (2007), 19–40, 10.1146/annurev.nutr.27.061406.093749.
164. Mizushima, N., Levine, B., Autophagy in mammalian development and differentiation. Nat. Cell Biol. 12 (2010), 823–830, 10.1038/ncb0910-823.
165. Mizushima, N., Yoshimori, T., Levine, B., Methods in mammalian autophagy research. Cell 140 (2010), 313–326, 10.1016/j.cell.2010.01.028.
166. Moreau, K., Ravikumar, B., Renna, M., Puri, C., Rubinsztein, D.C., Autophagosome precursor maturation requires homotypic fusion. Cell 146 (2011), 303–317, 10.1016/j.cell.2011.06.023.
167. Mortimore, G.E., Pösö, A.R., Intracellular protein catabolism and its control during nutrient deprivation and supply. Annu. Rev. Nutr. 7 (1987), 539–564, 10.1146/annurev.nu.07.070187.002543.
168. Mortimore, G.E., Lardeux, B.R., Adams, C.E., Regulation of microautophagy and basal protein turnover in rat liver: effects of short-term starvation. J. Biol. Chem. 263 (1988), 2506–2512.
169. Murakami, Y., Matsufuji, S., Kameji, T., Hayashi, S., Igarashi, K., Tamura, T., et al. Ornithine decarboxylase is degraded by the 26 S proteasome without ubiquitination. Nature 360 (1992), 597–599, 10.1038/360597a0.
170. Murakami, Y., Tanaka, K., Matsufuji, S., Miyazaki, Y., Hayashi, S., Antizyme, a protein induced by polyamines, accelerates the degradation of ornithine decarboxylase in Chinese-hamster ovary-cell extracts. Biochem. J. 283 (1992), 661–664.
171. N'Diaye, E.-N., Kajihara, K.K., Hsieh, I., Morisaki, H., Debnath, J., Brown, E.J., PLIC proteins or ubiquilins regulate autophagy-dependent cell survival during nutrient starvation. EMBO Rep. 10 (2009), 173–179, 10.1038/embor.2008.238.
172. Nair, U., Jotwani, A., Geng, J., Gammoh, N., Richerson, D., Yen, W.-L., et al. SNARE proteins are required for macroautophagy. Cell 146 (2011), 290–302, 10.1016/j.cell.2011.06.022.
173. Nanduri, P., Hao, R., Fitzpatrick, T., Yao, T.P., Chaperone-mediated 26 S proteasome remodeling facilitates free K63 ubiquitin chain production and aggresome clearance. J. Biol. Chem. 290 (2015), 9455–9464, 10.1074/jbc.M114.627950.
174. Nathan, J.A., Kim, H.T., Ting, L., Gygi, S.P., Goldberg, A.L., Why do cellular proteins linked to K63-polyubiquitin chains not associate with proteasomes?. EMBO J. 32 (2013), 552–565, 10.1038/emboj.2012.354.
175. Naujokat, C., Hoffmann, S., Role and function of the 26 S proteasome in proliferation and apoptosis. Lab. Invest. 82 (2002), 965–980.
176. Naujokat, C., Sezer, O., Zinke, H., Leclere, A., Hauptmann, S., Possinger, K., Proteasome inhibitors induce caspase-dependent apoptosis and accumulationof p21WAF1/Cip1 in human immatureleukemic cells. Eur. J. Haematol. 65 (2000), 221–236, 10.1034/j.1600-0609.2000.065004221.x.
177. Nedjic, J., Aichinger, M., Emmerich, J., Mizushima, N., Klein, L., Autophagy in thymic epithelium shapes the T-cell repertoire and is essential for tolerance. Nature 455 (2008), 396–400, 10.1038/nature07208.
178. Neefjes, J., Jongsma, M.L.M., Paul, P., Bakke, O., Towards a systems understanding of MHC class I and MHC class II antigen presentation. Nat. Rev. Immunol. 11 (2011), 823–836, 10.1038/nri3084.
179. Negishi, Y., Ui, N., Nakajima, M., Kawashima, K., Maruyama, K., Takizawa, et al. p21Cip-1/SDI-1/WAF-1 gene is involved in chondrogenic differentiation of ATDC5 cells in vitro. J. Biol. Chem. 276 (2001), 33249–33256, 10.1074/jbc.M010127200.
180. Neufeld, T.P., Autophagy and cell growth-the yin and yang of nutrient responses. J. Cell Sci. 125 (2012), 2359–2368, 10.1242/jcs.103333.
181. Nezis, I.P., Shravage, B., Sagona, V., Lamark, A.P., Bjørkøy, T., Johansen, G., et al. Autophagic degradation of dBruce controls DNA fragmentation in nurse cells during late Drosophila melanogaster oogenesis. J. Cell Biol. 190 (2010), 523–531, 10.1083/jcb.201002035.
182. Ni, H., Ergin, M., Huang, Q., Qin, J.-Z., Amin, H.M., Martinez, et al. Analysis of expression of nuclear factor kappaB (NF-kappaB) in multiple myeloma: downregulation of NF-kappaB induces apoptosis. Br. J. Haematol. 115 (2001), 279–286, 10.1046/j.1365-2141.2001.03102.x.
183. Niida, M., Tanaka, M., Kamitani, T., Downregulation of active IKK beta by Ro52-mediated autophagy. Mol. Immunol. 47 (2010), 2378–2387, 10.1016/j.molimm.2010.05.004.
184. Novak, I., Kirkin, V., McEwan, D.G., Zhang, J., Wild, P., Rozenknop, A., et al. Nix is a selective autophagy receptor for mitochondrial clearance. EMBO Rep. 11 (2010), 45–51, 10.1038/embor.2009.256.
185. Ogawa, M., Sasakawa, C., The role of Tecpr1 in selective autophagy as a cargo receptor. Autophagy 7 (2011), 1389–1391, 10.4161/auto.7.11.17151.
186. Ogawa, M., Yoshikawa, Y., Kobayashi, T., Mimuro, H., Fukumatsu, M., Kiga, K., et al. A Tecpr1-dependent selective autophagy pathway targets bacterial pathogens. Cell Host Microbe 9 (2011), 376–389, 10.1016/j.chom.2011.04.010.
187. Olzmann, J.A., Li, L., Chudaev, M.V., Chen, J., Perez, F.A., Palmiter, R.D., et al. Parkin-mediated K63-linked polyubiquitination targets misfolded DJ-1 to aggresomes via binding to HDAC6. J. Cell Biol. 178 (2007), 1025–1038, 10.1083/jcb.200611128.
188. Onodera, J., Ohsumi, Y., Ald6p is a preferred target for autophagy in yeast, Saccharomyces cerevisiae. J. Biol. Chem. 279 (2004), 16071–16076, 10.1074/jbc.M312706200.
189. Onodera, J., Ohsumi, Y., Autophagy is required for maintenance of amino acid levels and protein synthesis under nitrogen starvation. J. Biol. Chem. 280 (2005), 31582–31586, 10.1074/jbc.M506736200.
190. Orvedahl, A., MacPherson, S., Sumpter, R., Tallóczy, Z., Zou, Z., Levine, B., Autophagy protects against Sindbis virus infection of the central nervous system. Cell Host Microbe 7 (2010), 115–127, 10.1016/j.chom.2010.01.007.
191. Orvedahl, A., Sumpter, R., Xiao, G., Ng, A., Zou, Z., Tang, Y., et al. Image-based genome-wide siRNA screen identifies selective autophagy factors. Nature 480 (2011), 113–117, 10.1038/nature10546.
192. Ouyang, H., Ali, Y.O., Ravichandran, M., Dong, A., Qiu, W., MacKenzie, F., et al. Protein aggregates are recruited to aggresome by histone deacetylase 6 via unanchored ubiquitin C termini. J. Biol. Chem. 287 (2012), 2317–2327, 10.1074/jbc.M111.273730.
193. Paludan, C., Schmid, D., Landthaler, M., Vockerodt, M., Kube, D., Tuschl, T., et al. Endogenous MHC class II processing of a viral nuclear antigen after autophagy. Science 307 (2005), 593–596, 10.1126/science.1104904.
194. Pankiv, S., Clausen, T.H., Lamark, T., Brech, A., Bruun, J.-A., Outzen, H., et al. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J. Biol. Chem. 282 (2007), 24131–24145, 10.1074/jbc.M702824200.
195. Paraskevopoulos, K., Kriegenburg, F., Tatham, M.H., Rösner, H.I., Medina, B., Larsen, I.B., et al. Dss1 is a 26 S proteasome ubiquitin receptor. Mol. Cell 56 (2014), 453–461, 10.1016/j.molcel.2014.09.008.
196. Periyasamy-Thandavan, S., Jiang, M., Schoenlein, P., Dong, Z., Autophagy: molecular machinery, regulation, and implications for renal pathophysiology. Am. J. Physiol. Renal Physiol. 297 (2009), F244–F256, 10.1152/ajprenal.00033.2009.
197. Piccirillo, R., Goldberg, A.L., The p97/VCP ATPase is critical in muscle atrophy and the accelerated degradation of muscle proteins. EMBO J. 31 (2012), 3334–3350, 10.1038/emboj.2012.178.
198. Pickart, C.M., Ubiquitin in chains. Trends Biochem. Sci. 25 (2000), 544–548.
199. Pickering, a. M., Staab, T. a., Tower, J., Sieburth, D.S., Davies, K.J. a., A conserved role for the 20 S proteasome and Nrf2 transcription factor in oxidative-stress adaptation in mammals, C. elegans and D. melanogaster. J. Exp. Biol. 216 (2013), 543–553, 10.1242/jeb.074757.
200. Pua, H.H., Guo, J., Komatsu, M., He, Y.-W., Autophagy is essential for mitochondrial clearance in mature T lymphocytes. J. Immunol. 182 (2009), 4046–4055, 10.4049/jimmunol.0801143.
201. Qing, G., Yan, P., Qu, Z., Liu, H., Xiao, G., Hsp90 regulates processing of NF-kappa B2 p100 involving protection of NF-kappa B-inducing kinase (NIK) from autophagy-mediated degradation. Cell Res. 17 (2007), 520–530, 10.1038/cr.2007.47.
202. Raasi, S., Varadan, R., Fushman, D., Pickart, C.M., Diverse polyubiquitin interaction properties of ubiquitin-associated domains. Nat. Struct. Mol. Biol. 12 (2005), 708–714, 10.1038/nsmb962.
203. Radhakrishnan, S.K., Lee, C.S., Young, P., Beskow, A., Chan, J.Y., Deshaies, R.J., Transcription factor Nrf1 mediates the proteasome recovery pathway after proteasome inhibition in mammalian cells. Mol. Cell 38 (2010), 17–28, 10.1016/j.molcel.2010.02.029.
204. Rao, H., Sastry, A., Recognition of specific ubiquitin conjugates is important for the proteolytic functions of the ubiquitin-associated domain proteins Dsk2 and Rad23. J. Biol. Chem. 277 (2002), 11691–11695, 10.1074/jbc.M200245200.
205. Rao, V., Guan, B., Mutton, L.N., Bieberich, C.J., Proline-mediated proteasomal degradation of the prostate-specific tumor suppressor NKX3.1. J. Biol. Chem. 287 (2012), 36331–36340, 10.1074/jbc.M112.352823.
206. Reeds, P.J., Fjeld, C.R., Jahoor, F., Do the differences in amion acid composition of acute phase and muscle proteins have a bearing on nitrogen loss in traumatic states?. J. Nutr. 124 (1994), 906–910.
207. Reverte, C.G., Ahearn, M.D., Hake, L.E., CPEB degradation during Xenopus oocyte maturation requires a PEST domain and the 26 S proteasome. Dev. Biol. 231 (2001), 447–458, 10.1006/dbio.2001.0153.
208. Rieber, M., Strasberg Rieber, M., Apoptosis-inducing levels of UV radiation and proteasome inhibitors produce opposite effects on p21(WAF1) in human melanoma cells. Int. J. Cancer 86 (2000), 462–467.
209. Rikihisa, Y., Glycogen autophagosomes in polymorphonuclear leukocytes induced by rickettsiae. Anat. Rec. 208 (1984), 319–327, 10.1002/ar.1092080302.
210. Riley, B.E., Kaiser, S.E., Shaler, T.A., Ng, A.C.Y., Hara, T., Hipp, M.S., 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. 191 (2010), 537–552, 10.1083/jcb.201005012.
211. Rock, K.L., Gramm, C., Rothstein, L., Clark, K., Stein, R., Dick, L., et al. Inhibitors of the proteasome block the degradation of most cell proteins and the generation of peptides presented on MHC class I molecules. Cell 78 (1994), 761–771, 10.1016/S0092-8674(94)90462-6.
212. Rock, K.L., Farfán-Arribas, D.J., Colbert, J.D., Goldberg, A.L., Re-examining class-I presentation and the DRiP hypothesis. Trends Immunol. 35 (2014), 144–152, 10.1016/j.it.2014.01.002.
213. Ross, C.A., Poirier, M.A., Protein aggregation and neurodegenerative disease. Nat. Med. 10:Suppl (2004), S10–S17, 10.1038/nm1066.
214. Rothenberg, C., Srinivasan, D., Mah, L., Kaushik, S., Peterhoff, C.M., Ugolino, J., et al. Ubiquilin functions in autophagy and is degraded by chaperone-mediated autophagy. Hum. Mol. Genet. 19 (2010), 3219–3232, 10.1093/hmg/ddq231.
215. Sadoul, R., Fernandez, P.A., Quiquerez, A.L., Martinou, I., Maki, M., Schröter, M., et al. Involvement of the proteasome in the programmed cell death of NGF-deprived sympathetic neurons. EMBO J. 15 (1996), 3845–3852.
216. Saeki, Y., Kudo, T., Sone, T., Kikuchi, Y., Yokosawa, H., Toh-e, A., et al. Lysine 63-linked polyubiquitin chain may serve as a targeting signal for the 26 S proteasome. EMBO J. 28 (2009), 359–371, 10.1038/emboj.2008.305.
217. Sakowski, E.T., Koster, S., Portal Celhay, C., Park, H.S., Shrestha, E., Hetzenecker, S.E., et al. Ubiquilin 1 promotes IFN-γ-Induced xenophagy of mycobacterium tuberculosis. PLoS Pathog., 11, 2015, e1005076, 10.1371/journal.ppat.1005076.
218. Sandilands, E., Serrels, B., McEwan, D.G., Morton, J.P., Macagno, J.P., McLeod, K., et al. Autophagic targeting of Src promotes cancer cell survival following reduced FAK signalling. Nat. Cell Biol. 14 (2012), 51–60, 10.1038/ncb2386.
219. Sarkar, S., Regulation of autophagy by mTOR-dependent and mTOR-independent pathways: autophagy dysfunction in neurodegenerative diseases and therapeutic application of autophagy enhancers. Biochem. Soc. Trans. 41 (2013), 1103–1130, 10.1042/BST20130134.
220. Sawada, M.T., Morinaga, C., Izumi, K., Sawada, H., The 26 S proteasome assembly is regulated by a maturation-inducing hormone in starfish oocytes. Biochem. Biophys. Res. Commun. 254 (1999), 338–344, 10.1006/bbrc.1998.9948.
221. Schröder, M., Kaufman, R.J., The mammalian unfolded protein response. Annu. Rev. Biochem. 74 (2005), 739–789, 10.1146/annurev.biochem.73.011303.074134.
222. Seibenhener, M.L., Babu, J.R., Geetha, T., Wong, H.C., Krishna, N.R., Wooten, M.W., Sequestosome 1/p62 is a polyubiquitin chain binding protein involved in ubiquitin proteasome degradation. Mol. Cell. Biol. 24 (2004), 8055–8068, 10.1128/MCB.24.18.8055-8068.2004.
223. Sha, Z., Goldberg, A.L., Proteasome-mediated processing of Nrf1 is essential for coordinate induction of all proteasome subunits and p97. Curr. Biol. 24 (2014), 1573–1583, 10.1016/j.cub.2014.06.004.
224. Sherr, C.J., Roberts, J.M., CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev. 13 (1999), 1501–1512, 10.1101/gad.13.12.1501.
225. Shi, Y., Chen, X., Elsasser, S., Stocks, B.B., Tian, G., Lee, B.-H., et al. Rpn1 provides adjacent receptor sites for substrate binding and deubiquitination by the proteasome. Science, 351, 2016, 10.1126/science.aad9421 aad9421.
226. Shibutani, S.T., Saitoh, T., Nowag, H., Münz, C., Yoshimori, T., Autophagy and autophagy-related proteins in the immune system. Nat. Immunol. 16 (2015), 1014–1024, 10.1038/ni.3273.
227. Shin, Y., Klucken, J., Patterson, C., Hyman, B.T., McLean, P.J., The co-chaperone carboxyl terminus of Hsp70-interacting protein (CHIP) mediates alpha-synuclein degradation decisions between proteasomal and lysosomal pathways. J. Biol. Chem. 280 (2005), 23727–23734, 10.1074/jbc.M503326200.
228. Siegel, J.H., Cerra, F.B., Coleman, B., Giovannini, I., Shetye, M., Border, J.R., et al. Physiological and metabolic correlations in human sepsis. Surgery 86 (1979), 163–193.
229. Singh, R., Xiang, Y., Wang, Y., Baikati, K., Cuervo, A.M., Luu, Y.K., et al. Autophagy regulates adipose mass and differentiation in mice. J. Clin. Invest. 119 (2009), 3329–3339, 10.1172/JCI39228.
230. Slobodkin, M.R., Elazar, Z., The Atg8 family: multifunctional ubiquitin-like key regulators of autophagy. Essays Biochem. 55 (2013), 51–64, 10.1042/bse0550051.
231. Song, P., Li, S., Wu, H., Gao, R., Rao, G., Wang, D., et al. Parkin promotes proteasomal degradation of p62: implication of selective vulnerability of neuronal cells in the pathogenesis of Parkinson's disease. Protein Cell 7 (2016), 114–129, 10.1007/s13238-015-0230-9.
232. Spinella, M.J., Freemantle, S.J., Sekula, D., Chang, J.H., Christie, A.J., Dmitrovsky, E., Retinoic acid promotes ubiquitination and proteolysis of cyclin D1 during induced tumor cell differentiation. J. Biol. Chem. 274 (1999), 22013–22018, 10.1074/jbc.274.31.22013.
233. Steffen, J., Seeger, M., Koch, A., Krüger, E., Proteasomal degradation is transcriptionally controlled by TCF11 via an ERAD-dependent feedback loop. Mol. Cell 40 (2010), 147–158, 10.1016/j.molcel.2010.09.012.
234. Stephenson, L.M., Miller, B.C., Ng, A., Eisenberg, J., Zhao, Z., Cadwell, K., et al. Identification of Atg5-dependent transcriptional changes and increases in mitochondrial mass in Atg5-deficient T lymphocytes. Autophagy 5 (2009), 625–635.
235. Suraweera, A., Münch, C., Hanssum, A., Bertolotti, A., Failure of amino acid homeostasis causes cell death following proteasome inhibition. Mol. Cell 48 (2012), 242–253, 10.1016/j.molcel.2012.08.003.
236. Suzuki, K., Ohsumi, Y., Molecular machinery of autophagosome formation in yeast, Saccharomyces cerevisiae. FEBS Lett. 581 (2007), 2156–2161, 10.1016/j.febslet.2007.01.096.
237. Suzuki, S.W., Onodera, J., Ohsumi, Y., Starvation induced cell death in autophagy-defective yeast mutants is caused by mitochondria dysfunction. PLoS One, 6, 2011, e17412, 10.1371/journal.pone.0017412.
238. Svenning, S., Lamark, T., Krause, K., Johansen, T., Plant NBR1 is a selective autophagy substrate and a functional hybrid of the mammalian autophagic adapters NBR1 and p62/SQSTM1. Autophagy 7 (2011), 993–1010.
239. Takasugi, T., Minegishi, S., Asada, A., Saito, T., Kawahara, H., Hisanaga, S.-I., Two degradation pathways of the p35 Cdk5 (cyclin-dependent kinase) activation subunit, dependent and independent of ubiquitination. J. Biol. Chem. 291 (2016), 4649–4657, 10.1074/jbc.M115.692871.
240. Tan, J.M.M., Wong, E.S.P., Kirkpatrick, D.S., Pletnikova, O., Ko, H.S., Tay, S.-P., et al. Lysine 63-linked ubiquitination promotes the formation and autophagic clearance of protein inclusions associated with neurodegenerative diseases. Hum. Mol. Genet. 17 (2008), 431–439, 10.1093/hmg/ddm320.
241. Tanida, I., Ueno, T., Kominami, E., Human light chain 3/MAP1LC3 B is cleaved at its carboxyl-terminal Met121 to expose Gly120 for lipidation and targeting to autophagosomal membranes. J. Biol. Chem. 279 (2004), 47704–47710.
242. Tattoli, I., Philpott, D.J., Girardin, S.E., The bacterial and cellular determinants controlling the recruitment of mTOR to the Salmonella-containing vacuole. Biol. Open 1 (2012), 1215–1225, 10.1242/bio.20122840.
243. Tattoli, I., Sorbara, M.T., Vuckovic, D., Ling, A., Soares, F., Carneiro, L.A.M., et al. Amino acid starvation induced by invasive bacterial pathogens triggers an innate host defense program. Cell Host Microbe 11 (2012), 563–575, 10.1016/j.chom.2012.04.012.
244. Tattoli, I., Sorbara, M.T., Yang, C., Tooze, S.A., Philpott, D.J., Girardin, S.E., Listeria phospholipases subvert host autophagic defenses by stalling pre-autophagosomal structures. EMBO J. 32 (2013), 3066–3078, 10.1038/emboj.2013.234.
245. Terrell, J., Shih, S., Dunn, R., Hicke, L., A function for monoubiquitination in the internalization of a G protein-coupled receptor. Mol. Cell 1 (1998), 193–202.
246. Thrower, J.S., Hoffman, L., Rechsteiner, M., Pickart, C.M., Recognition of the polyubiquitin proteolytic signal. EMBO J. 19 (2000), 94––102, 10.1093/emboj/19.1.94.
247. Thurston, T.L.M., Ryzhakov, G., Bloor, S., von Muhlinen, N., Randow, F., The TBK1 adaptor and autophagy receptor NDP52 restricts the proliferation of ubiquitin-coated bacteria. Nat. Immunol. 10 (2009), 1215–1221, 10.1038/ni.1800.
248. Thurston, T.L.M., Wandel, M.P., von Muhlinen, N., Foeglein, A., Randow, F., Galectin 8 targets damaged vesicles for autophagy to defend cells against bacterial invasion. Nature 482 (2012), 414–418, 10.1038/nature10744.
249. Tokumoto, T., Tokumoto, M., Seto, K., Horiguchi, R., Nagahama, Y., Yamada, S., et al. Disappearance of a novel protein component of the 26 S proteasome during Xenopus oocyte maturation. Exp. Cell Res. 247 (1999), 313–319, 10.1006/excr.1998.4357.
250. Tresse, E., Salomons, F.A., Vesa, J., Bott, L.C., Kimonis, V., Yao, T.-P., et al. VCP/p97 is essential for maturation of ubiquitin-containing autophagosomes and this function is impaired by mutations that cause IBMPFD. Autophagy 6 (2010), 217–227.
251. Tumbarello, D.A., Manna, P.T., Allen, M., Bycroft, M., Arden, S.D., Kendrick-Jones, J., et al. The autophagy receptor TAX1BP1 and the molecular motor myosin VI are required for clearance of Salmonella typhimurium by autophagy. PLoS Pathog., 11, 2015, e1005174, 10.1371/journal.ppat.1005174.
252. Urano, T., Yashiroda, H., Muraoka, M., Tanaka, K., Hosoi, T., Inoue, S., et al. p57Kip2 is degraded through the proteasome in osteoblasts stimulated to proliferation by transforming growth factor 1. J. Biol. Chem. 274 (1999), 12197–12200, 10.1074/jbc.274.18.12197.
253. Vabulas, R.M., Hartl, F.U., Protein synthesis upon acute nutrient restriction relies on proteasome function. Science 310 (2005), 1960–1963, 10.1126/science.1121925.
254. Vilchez, D., Boyer, L., Morantte, I., Lutz, M., Merkwirth, C., Joyce, D., et al. Increased proteasome activity in human embryonic stem cells is regulated by PSMD11. Nature 489 (2012), 304–308, 10.1038/nature11468.
255. Vilchez, D., Morantte, I., Liu, Z., Douglas, P.M., Merkwirth, C., Rodrigues, A.P.C., et al. RPN-6 determines C. elegans longevity under proteotoxic stress conditions. Nature 489 (2012), 263–268, 10.1038/nature11315.
256. Walters, K.J., Kleijnen, M.F., Goh, A.M., Wagner, G., Howley, P.M., Structural studies of the interaction between ubiquitin family proteins and proteasome subunit S5a. Biochemistry 41 (2002), 1767–1777.
257. Wang, C.-W., Klionsky, D.J., The molecular mechanism of autophagy. Mol. Med. 9 (2003), 65–76.
258. Wang, L., Mao, X., Ju, D., Xie, Y., Rpn4 is a physiological substrate of the Ubr2 ubiquitin ligase. J. Biol. Chem. 279 (2004), 55218–55223, 10.1074/jbc.M410085200.
259. Wang, Q., Young, P., Walters, K.J., Structure of S5a bound to monoubiquitin provides a model for polyubiquitin recognition. J. Mol. Biol. 348 (2005), 727–739, 10.1016/j.jmb.2005.03.007.
260. Wang, X., Yen, J., Kaiser, P., Huang, L., Regulation of the 26 S proteasome complex during oxidative stress. Sci. Signal., 3, 2010, 10.1126/scisignal.2001232 ra88.
261. Wang, H., Ying, Z., Wang, G., Ataxin-3 regulates aggresome formation of copper-zinc superoxide dismutase (SOD1) by editing K63-linked polyubiquitin chains. J. Biol. Chem. 287 (2012), 28576–28585, 10.1074/jbc.M111.299990.
262. Watanabe, Y., Tanaka, M., p62/SQSTM1 in autophagic clearance of a non-ubiquitylated substrate. J. Cell Sci. 124 (2011), 2692–2701, 10.1242/jcs.081232.
263. 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. 278 (2003), 25009–25013, 10.1074/jbc.M300227200.
264. Wetzel, R., Mutations and off-pathway aggregation of proteins. Trends Biotechnol. 12 (1994), 193–198.
265. Wickner, S., Posttranslational quality control: folding, refolding, and degrading proteins. Science 286 (1999), 1888–1893.
266. Wild, P., Farhan, H., McEwan, D.G., Wagner, S., Rogov, V., Brady, V., N.R, et al. Phosphorylation of the autophagy receptor optineurin restricts Salmonella growth. Science 333 (2011), 228–233, 10.1126/science.1205405.
267. 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. U. S. A. 111 (2014), E4439–E4448, 10.1073/pnas.1405752111.
268. Wooten, M.W., Geetha, T., Babu, J.R., Seibenhener, M.L., Peng, J., Cox, N., et al. Essential role of sequestosome 1/p62 in regulating accumulation of Lys63-ubiquitinated proteins. J. Biol. Chem. 283 (2008), 6783–6789, 10.1074/jbc.M709496200.
269. Xie, Y., Varshavsky, a, RPN4 is a ligand, substrate, and transcriptional regulator of the 26 S proteasome: a negative feedback circuit. Proc. Natl. Acad. Sci. U. S. A. 98 (2001), 3056–3061, 10.1073/pnas.071022298.
270. Xie, X., Li, F., Wang, Y., Wang, Y., Lin, Z., Cheng, X., et al. Molecular basis of ubiquitin recognition by the autophagy receptor CALCOCO2. Autophagy 11 (2015), 1775–1789, 10.1080/15548627.2015.1082025.
271. Xu, P., Duong, D.M., Seyfried, N.T., Cheng, D., Xie, Y., Robert, J., et al. Quantitative proteomics reveals the function of unconventional ubiquitin chains in proteasomal degradation. Cell 137 (2009), 133–145, 10.1016/j.cell.2009.01.041.
272. Yamamoto, A., Masaki, R., Tashiro, Y., Characterization of the isolation membranes and the limiting membranes of autophagosomes in rat hepatocytes by lectin cytochemistry. J. Histochem. Cytochem. 38 (1990), 573–580, 10.1177/38.4.2319125.
273. Yan, J., Seibenhener, M.L., Calderilla-Barbosa, L., Diaz-Meco, M.-T., Moscat, J., Jiang, et al. SQSTM1/p62 interacts with HDAC6 and regulates deacetylase activity. PLoS One, 8, 2013, e76016, 10.1371/journal.pone.0076016.
274. Yang, Y.L., Li, X.M., The IAP family: endogenous caspase inhibitors with multiple biological activities. Cell Res. 10 (2000), 169–177, 10.1038/sj.cr.7290046.
275. Ye, J., Palm, W., Peng, M., King, B., Lindsten, T., Li, M.O., et al. GCN2 sustains mTORC1 suppression upon amino acid deprivation by inducing Sestrin2. Genes Dev. 29 (2015), 2331–2336, 10.1101/gad.269324.115.
276. Young, P., Deveraux, Q., Beal, R.E., Pickart, C.M., Rechsteiner, M., Characterization of two polyubiquitin binding sites in the 26 s protease subunit 5a. J. Biol. Chem. 273 (1998), 5461–5467, 10.1074/jbc.273.10.5461.
277. Zaarur, N., Meriin, A.B., Bejarano, E., Xu, X., Gabai, V.L., Cuervo, A.M., et al. Proteasome failure promotes positioning of lysosomes around the aggresome via local block of microtubule-dependent transport. Mol. Cell. Biol. 34 (2014), 1336–1348, 10.1128/MCB.00103-14.
278. Zhang, Y., Goldman, S., Baerga, R., Zhao, Y., Komatsu, M., Jin, S., Adipose-specific deletion of autophagy-related gene 7 (atg7) in mice reveals a role in adipogenesis. Proc. Natl. Acad. Sci. U. S. A. 106 (2009), 19860–19865, 10.1073/pnas.0906048106.
279. Zhang, Y., Nicholatos, J., Dreier, J.R., Ricoult, S.J.H., Widenmaier, S.B., Hotamisligil, G.S., et al. Coordinated regulation of protein synthesis and degradation by mTORC1. Nature 513 (2014), 440–443, 10.1038/nature13492.
280. Zhao, J., Brault, J.J., Schild, A., Cao, P., Sandri, M., Schiaffino, S., et al. FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells. Cell Metab. 6 (2007), 472–483, 10.1016/j.cmet.2007.11.004.
281. Zhao, J., Brault, J.J., Schild, A., Goldberg, A.L., Coordinate activation of autophagy and the proteasome pathway by FoxO transcription factor. Autophagy 4 (2008), 378–380, 10.4161/auto.5633.
282. Zhao, J., Zhai, B., Gygi, S.P., Goldberg, A.L., mTOR inhibition activates overall protein degradation by the ubiquitin proteasome system as well as by autophagy. Proc. Natl. Acad. Sci. U. S. A. 112 (2015), 15790–15797, 10.1073/pnas.1521919112.
283. 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. 183 (2009), 5909–5916, 10.4049/jimmunol.0900441.
284. van Nocker, S., Deveraux, Q., Rechsteiner, M., Vierstra, R.D., Arabidopsis MBP1 gene encodes a conserved ubiquitin recognition component of the 26 S proteasome. Proc. Natl. Acad. Sci. U. S. A. 93 (1996), 856–860.
285. van Nocker, S., Sadis, S., Rubin, D.M., Glickman, M., Fu, H., Coux, O., et al. The multiubiquitin-chain-binding protein Mcb1 is a component of the 26 S proteasome in Saccharomyces cerevisiae and plays a nonessential, substrate-specific role in protein turnover. Mol. Cell. Biol. 16 (1996), 6020–6028.
286. von Muhlinen, N., Akutsu, M., Ravenhill, B.J., Foeglein, Á., Bloor, S., Rutherford, T.J., et al. LC3C, bound selectively by a noncanonical LIR motif in NDP52, is required for antibacterial autophagy. Mol. Cell 48 (2012), 329––342, 10.1016/j.molcel.2012.08.024.