Autophagy inhibition promotes defective neosynthesized proteins storage in ALIS, and induces redirection toward proteasome processing and MHCI-restricted presentation

References

• Kaganovich D, Kopito R, Frydman J. Misfolded proteins partition between two distinct quality control compartments. Nature 2008; 454:1088 - 95; http://dx.doi.org/10.1038/nature07195; PMID: 18756251
   PubMed Web of Science ®Google Scholar
• Yewdell JW, Nicchitta CV. The DRiP hypothesis decennial: support, controversy, refinement and extension. Trends Immunol 2006; 27:368 - 73; http://dx.doi.org/10.1016/j.it.2006.06.008; PMID: 16815756
   PubMed Web of Science ®Google Scholar
• Princiotta MF, Finzi D, Qian SB, Gibbs J, Schuchmann S, Buttgereit F, et al. Quantitating protein synthesis, degradation, and endogenous antigen processing. Immunity 2003; 18:343 - 54; http://dx.doi.org/10.1016/S1074-7613(03)00051-7; PMID: 12648452
   PubMed Web of Science ®Google Scholar
• Navon A, Ciechanover A. The 26 S proteasome: from basic mechanisms to drug targeting. J Biol Chem 2009; 284:33713 - 8; http://dx.doi.org/10.1074/jbc.R109.018481; PMID: 19812037
   PubMed Web of Science ®Google Scholar
• Young JC. Mechanisms of the Hsp70 chaperone system. Biochem Cell Biol 2010; 88:291 - 300; http://dx.doi.org/10.1139/O09-175; PMID: 20453930
   PubMed Web of Science ®Google Scholar
• McDonough H, Patterson C. CHIP: a link between the chaperone and proteasome systems. Cell Stress Chaperones 2003; 8:303 - 8; http://dx.doi.org/10.1379/1466-1268(2003)008<0303:CALBTC>2.0.CO;2; PMID: 15115282
   PubMed Web of Science ®Google Scholar
• Kabbage M, Dickman MB. The BAG proteins: a ubiquitous family of chaperone regulators. Cell Mol Life Sci 2008; 65:1390 - 402; http://dx.doi.org/10.1007/s00018-008-7535-2; PMID: 18264803
   PubMed Web of Science ®Google Scholar
• Yewdell JW. Plumbing the sources of endogenous MHC class I peptide ligands. Curr Opin Immunol 2007; 19:79 - 86; http://dx.doi.org/10.1016/j.coi.2006.11.010; PMID: 17140786
   PubMed Web of Science ®Google Scholar
• Khan S, de Giuli R, Schmidtke G, Bruns M, Buchmeier M, van den Broek M, et al. Cutting edge: neosynthesis is required for the presentation of a T cell epitope from a long-lived viral protein. J Immunol 2001; 167:4801 - 4; PMID: 11673482
   PubMed Web of Science ®Google Scholar
• Mehrpour M, Esclatine A, Beau I, Codogno P. Overview of macroautophagy regulation in mammalian cells. Cell Res 2010; 20:748 - 62; http://dx.doi.org/10.1038/cr.2010.82; PMID: 20548331
   PubMed Web of Science ®Google Scholar
• Kim PK, Hailey DW, Mullen RT, Lippincott-Schwartz J. Ubiquitin signals autophagic degradation of cytosolic proteins and peroxisomes. Proc Natl Acad Sci USA 2008; 105:20567 - 74; http://dx.doi.org/10.1073/pnas.0810611105; PMID: 19074260
   PubMed Web of Science ®Google Scholar
• Kirkin V, McEwan DG, Novak I, Dikic I. A role for ubiquitin in selective autophagy. Mol Cell 2009; 34:259 - 69; http://dx.doi.org/10.1016/j.molcel.2009.04.026; PMID: 19450525
   PubMed Web of Science ®Google Scholar
• Clausen TH, Lamark T, Isakson P, Finley K, Larsen KB, Brech A, et al. p62/SQSTM1 and ALFY interact to facilitate the formation of p62 bodies/ALIS and their degradation by autophagy. Autophagy 2010; 6:330 - 44; http://dx.doi.org/10.4161/auto.6.3.11226; PMID: 20168092
   PubMed Web of Science ®Google Scholar
• Thurston TL, 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 2009; 10:1215 - 21; http://dx.doi.org/10.1038/ni.1800; PMID: 19820708
   PubMed Web of Science ®Google Scholar
• Dikic I, Wakatsuki S, Walters KJ. Ubiquitin-binding domains - from structures to functions. Nat Rev Mol Cell Biol 2009; 10:659 - 71; http://dx.doi.org/10.1038/nrm2767; PMID: 19773779
   PubMed Web of Science ®Google Scholar
• Korolchuk VI, Mansilla A, Menzies FM, Rubinsztein DC. Autophagy inhibition compromises degradation of ubiquitin-proteasome pathway substrates. Mol Cell 2009; 33:517 - 27; http://dx.doi.org/10.1016/j.molcel.2009.01.021; PMID: 19250912
   PubMed Web of Science ®Google Scholar
• Pandey UB, Nie Z, Batlevi Y, McCray BA, Ritson GP, Nedelsky NB, et al. HDAC6 rescues neurodegeneration and provides an essential link between autophagy and the UPS. Nature 2007; 447:859 - 63; http://dx.doi.org/10.1038/nature05853; PMID: 17568747
   PubMed Web of Science ®Google Scholar
• Cuervo AM, Wong ES, Martinez-Vicente M. Protein degradation, aggregation, and misfolding. Mov Disord 2010; 25:Suppl 1 S49 - 54; http://dx.doi.org/10.1002/mds.22718; PMID: 20187257
   PubMedGoogle Scholar
• Yamamoto A, Cremona ML, Rothman JE. Autophagy-mediated clearance of huntingtin aggregates triggered by the insulin-signaling pathway. J Cell Biol 2006; 172:719 - 31; http://dx.doi.org/10.1083/jcb.200510065; PMID: 16505167
   PubMed Web of Science ®Google Scholar
• English L, Chemali M, Duron J, Rondeau C, Laplante A, Gingras D, et al. Autophagy enhances the presentation of endogenous viral antigens on MHC class I molecules during HSV-1 infection. Nat Immunol 2009; 10:480 - 7; http://dx.doi.org/10.1038/ni.1720; PMID: 19305394
   PubMed Web of Science ®Google Scholar
• Schmid D, Pypaert M, Munz C. Antigen-loading compartments for major histocompatibility complex class II molecules continuously receive input from autophagosomes. Immunity 2007; 26:79 - 92; http://dx.doi.org/10.1016/j.immuni.2006.10.018; PMID: 17182262
   PubMed Web of Science ®Google Scholar
• Dengjel J, Schoor O, Fischer R, Reich M, Kraus M, Muller M, et al. Autophagy promotes MHC class II presentation of peptides from intracellular source proteins. Proc Natl Acad Sci USA 2005; 102:7922 - 7; http://dx.doi.org/10.1073/pnas.0501190102; PMID: 15894616
   PubMed Web of Science ®Google Scholar
• Lee HK, Mattei LM, Steinberg BE, Alberts P, Lee YH, Chervonsky A, et al. In vivo requirement for Atg5 in antigen presentation by dendritic cells. Immunity 2010; 32:227 - 39; http://dx.doi.org/10.1016/j.immuni.2009.12.006; PMID: 20171125
   PubMed Web of Science ®Google Scholar
• Pierre P. Dendritic cells, DRiPs, and DALIS in the control of antigen processing. Immunol Rev 2005; 207:184 - 90; http://dx.doi.org/10.1111/j.0105-2896.2005.00300.x; PMID: 16181336
   PubMed Web of Science ®Google Scholar
• Szeto J, Kaniuk NA, Canadien V, Nisman R, Mizushima N, Yoshimori T, et al. ALIS are stress-induced protein storage compartments for substrates of the proteasome and autophagy. Autophagy 2006; 2:189 - 99; PMID: 16874109
   PubMed Web of Science ®Google Scholar
• 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 2005; 171:603 - 14; http://dx.doi.org/10.1083/jcb.200507002; PMID: 16286508
   PubMed Web of Science ®Google Scholar
• Lelouard H, Ferrand V, Marguet D, Bania J, Camosseto V, David A, et al. Dendritic cell aggresome-like induced structures are dedicated areas for ubiquitination and storage of newly synthesized defective proteins. J Cell Biol 2004; 164:667 - 75; http://dx.doi.org/10.1083/jcb.200312073; PMID: 14981091
   PubMed Web of Science ®Google Scholar
• Lelouard H, Gatti E, Cappello F, Gresser O, Camosseto V, Pierre P. Transient aggregation of ubiquitinated proteins during dendritic cell maturation. Nature 2002; 417:177 - 82; http://dx.doi.org/10.1038/417177a; PMID: 12000969
   PubMed Web of Science ®Google Scholar
• Kettern N, Rogon C, Limmer A, Schild H, Hohfeld J. The Hsc/Hsp70 co-chaperone network controls antigen aggregation and presentation during maturation of professional antigen presenting cells. PLoS ONE 2011; 6:e16398; http://dx.doi.org/10.1371/journal.pone.0016398; PMID: 21283720
   PubMed Web of Science ®Google Scholar
• Lamark T, Kirkin V, Dikic I, Johansen T. NBR1 and p62 as cargo receptors for selective autophagy of ubiquitinated targets. Cell Cycle 2009; 8:1986 - 90; http://dx.doi.org/10.4161/cc.8.13.8892; PMID: 19502794
   PubMed Web of Science ®Google Scholar
• Riley BE, Kaiser SE, Shaler TA, Ng AC, Hara T, Hipp MS, 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 - 52; http://dx.doi.org/10.1083/jcb.201005012; PMID: 21041446
   PubMed Web of Science ®Google Scholar
• Schmidt EK, Clavarino G, Ceppi M, Pierre P. SUnSET, a nonradioactive method to monitor protein synthesis. Nat Methods 2009; 6:275 - 7; http://dx.doi.org/10.1038/nmeth.1314; PMID: 19305406
   PubMed Web of Science ®Google Scholar
• Kirkin V, Lamark T, Sou YS, Bjorkoy G, Nunn JL, Bruun JA, et al. A role for NBR1 in autophagosomal degradation of ubiquitinated substrates. Mol Cell 2009; 33:505 - 16; http://dx.doi.org/10.1016/j.molcel.2009.01.020; PMID: 19250911
   PubMed Web of Science ®Google Scholar
• Lau A, Wang XJ, Zhao F, Villeneuve NF, Wu T, Jiang T, et al. A noncanonical mechanism of Nrf2 activation by autophagy deficiency: direct interaction between Keap1 and p62. Mol Cell Biol 2010; 30:3275 - 85; http://dx.doi.org/10.1128/MCB.00248-10; PMID: 20421418
   PubMed Web of Science ®Google Scholar
• Qian SB, Reits E, Neefjes J, Deslich JM, Bennink JR, Yewdell JW. Tight linkage between translation and MHC class I peptide ligand generation implies specialized antigen processing for defective ribosomal products. J Immunol 2006; 177:227 - 33; PMID: 16785518
   PubMed Web of Science ®Google Scholar
• Yewdell JW. Not such a dismal science: the economics of protein synthesis, folding, degradation and antigen processing. Trends Cell Biol 2001; 11:294 - 7; http://dx.doi.org/10.1016/S0962-8924(01)02030-X; PMID: 11413040
   PubMed Web of Science ®Google Scholar
• Kunisawa J, Shastri N. The group II chaperonin TRiC protects proteolytic intermediates from degradation in the MHC class I antigen processing pathway. Mol Cell 2003; 12:565 - 76; http://dx.doi.org/10.1016/j.molcel.2003.08.009; PMID: 14527404
   PubMed Web of Science ®Google Scholar
• Alberti S, Esser C, Hohfeld J. BAG-1–a nucleotide exchange factor of Hsc70 with multiple cellular functions. Cell Stress Chaperones 2003; 8:225 - 31; http://dx.doi.org/10.1379/1466-1268(2003)008<0225:BNEFOH>2.0.CO;2; PMID: 14984055
   PubMed Web of Science ®Google Scholar
• Gamerdinger M, Hajieva P, Kaya AM, Wolfrum U, Hartl FU, Behl C. Protein quality control during aging involves recruitment of the macroautophagy pathway by BAG3. EMBO J 2009; 28:889 - 901; http://dx.doi.org/10.1038/emboj.2009.29; PMID: 19229298
   PubMed Web of Science ®Google Scholar
• Gehring U. Biological activities of HAP46/BAG-1. The HAP46/BAG-1 protein: regulator of HSP70 chaperones, DNA-binding protein and stimulator of transcription. EMBO Rep 2004; 5:148 - 53; http://dx.doi.org/10.1038/sj.embor.7400083; PMID: 14755308
   PubMed Web of Science ®Google Scholar
• Minami R, Hayakawa A, Kagawa H, Yanagi Y, Yokosawa H, Kawahara H. BAG-6 is essential for selective elimination of defective proteasomal substrates. J Cell Biol 2010; 190:637 - 50; http://dx.doi.org/10.1083/jcb.200908092; PMID: 20713601
   PubMed Web of Science ®Google Scholar
• Rohde M, Daugaard M, Jensen MH, Helin K, Nylandsted J, Jaattela M. Members of the heat-shock protein 70 family promote cancer cell growth by distinct mechanisms. Genes Dev 2005; 19:570 - 82; http://dx.doi.org/10.1101/gad.305405; PMID: 15741319
   PubMed Web of Science ®Google Scholar
• Mayer MP, Bukau B. Hsp70 chaperones: cellular functions and molecular mechanism. Cell Mol Life Sci 2005; 62:670 - 84; http://dx.doi.org/10.1007/s00018-004-4464-6; PMID: 15770419
   PubMed Web of Science ®Google Scholar
• Seifert U, Bialy LP, Ebstein F, Bech-Otschir D, Voigt A, Schroter F, et al. Immunoproteasomes preserve protein homeostasis upon interferon-induced oxidative stress. Cell 2010; 142:613 - 24; http://dx.doi.org/10.1016/j.cell.2010.07.036; PMID: 20723761
   PubMed Web of Science ®Google Scholar
• Tyedmers J, Mogk A, Bukau B. Cellular strategies for controlling protein aggregation. Nat Rev Mol Cell Biol 2010; 11:777 - 88; http://dx.doi.org/10.1038/nrm2993; PMID: 20944667
   PubMed Web of Science ®Google Scholar
• Pankiv S, Clausen TH, Lamark T, Brech A, Bruun JA, Outzen H, et al. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J Biol Chem 2007; 282:24131 - 45; http://dx.doi.org/10.1074/jbc.M702824200; PMID: 17580304
   PubMed Web of Science ®Google Scholar
• Komatsu M, Waguri S, Koike M, Sou YS, Ueno T, Hara T, et al. Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice. Cell 2007; 131:1149 - 63; http://dx.doi.org/10.1016/j.cell.2007.10.035; PMID: 18083104
   PubMed Web of Science ®Google Scholar
• 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 2006; 441:885 - 9; http://dx.doi.org/10.1038/nature04724; PMID: 16625204
   PubMed Web of Science ®Google Scholar
• Itakura E, Mizushima N. p62 Targeting to the autophagosome formation site requires self-oligomerization but not LC3 binding. J Cell Biol 2011; 192:17 - 27; http://dx.doi.org/10.1083/jcb.201009067; PMID: 21220506
   PubMed Web of Science ®Google Scholar
• Sha Y, Pandit L, Zeng S, Eissa NT. A critical role for CHIP in the aggresome pathway. Mol Cell Biol 2009; 29:116 - 28; http://dx.doi.org/10.1128/MCB.00829-08; PMID: 18955503
   PubMed Web of Science ®Google Scholar
• Gutierrez MG, Master SS, Singh SB, Taylor GA, Colombo MI, Deretic V. Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 2004; 119:753 - 66; http://dx.doi.org/10.1016/j.cell.2004.11.038; PMID: 15607973
   PubMed Web of Science ®Google Scholar
• Heink S, Ludwig D, Kloetzel PM, Kruger E. IFN-gamma-induced immune adaptation of the proteasome system is an accelerated and transient response. Proc Natl Acad Sci USA 2005; 102:9241 - 6; http://dx.doi.org/10.1073/pnas.0501711102; PMID: 15944226
   PubMed Web of Science ®Google Scholar
• Imai Y, Soda M, Hatakeyama S, Akagi T, Hashikawa T, Nakayama KI, et al. CHIP is associated with Parkin, a gene responsible for familial Parkinson's disease, and enhances its ubiquitin ligase activity. Mol Cell 2002; 10:55 - 67; http://dx.doi.org/10.1016/S1097-2765(02)00583-X; PMID: 12150907
   PubMed Web of Science ®Google Scholar
• Ballinger CA, Connell P, Wu Y, Hu Z, Thompson LJ, Yin LY, et al. Identification of CHIP, a novel tetratricopeptide repeat-containing protein that interacts with heat shock proteins and negatively regulates chaperone functions. Mol Cell Biol 1999; 19:4535 - 45; PMID: 10330192
   PubMed Web of Science ®Google Scholar
• Hilton CJ, Dahl AM, Rock KL. Anti-peptide antibody blocks peptide binding to MHC class I molecules in the endoplasmic reticulum. J Immunol 2001; 166:3952 - 6; PMID: 11238640
   PubMed Web of Science ®Google Scholar
• Porgador A, Yewdell JW, Deng Y, Bennink JR, Germain RN. Localization, quantitation, and in situ detection of specific peptide-MHC class I complexes using a monoclonal antibody. Immunity 1997; 6:715 - 26; http://dx.doi.org/10.1016/S1074-7613(00)80447-1; PMID: 9208844
   PubMed Web of Science ®Google Scholar