Crosstalk between autophagy and proteasome protein degradation systems: Possible implications for cancer therapy

Folia Histochemica et Cytobiologica

Volumn 51, Issue 4, 2013, Pages 249-264

  Wojcik, Slawomir ^a  

^a MEDICAL UNIVERSITY OF GDANSK   (Poland)

Author keywords

Aggresomes; ATF4; Autophagy; Cancer; LC3; MTOR; Proteasome inhibitors; Ubiquitin Proteasomes System; Unfolded Protein Response

Indexed keywords

ANIMALS; AUTOPHAGY; HUMANS; NEOPLASMS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEASOME INHIBITORS; PROTEOLYSIS;

EID: 84893491874     PISSN: 02398508     EISSN: 18975631     Source Type: Journal    
DOI: 10.5603/FHC.2013.0036     Document Type: Review

References (144)

1. Hershko A, Ciechanover A. The ubiquitin pathway for the degradation of intracellular proteins. Prog Nucleic Acid Res Mol Biol. 1986;33:19-56.
2. Pickart CM, Eddins MJ. Ubiquitin: structures, functions, mechanisms. Biochim Biophys Acta. 2004;1695:55-72.
3. Sadowski M, Sarcevic B. Mechanisms of mono-and poly-ubiquitination: Ubiquitination specificity depends on compatibility between the E2 catalytic core and amino acid residues proximal to the lysine. Cell Div. 2010;5:19.
4. Herrmann J, Lerman LO, Lerman A. Ubiquitin and ubiquitin-like proteins in protein regulation. Circ Res. 2007;100:1276-1291.
5. Teixeira LK, Reed SI. Ubiquitin ligases and cell cycle control. Annu Rev Biochem. 2013;82:387-414.
6. Ciechanover A. Intracellular protein degradation: from a vague idea thru the lysosome and the ubiquitin-proteasome system and onto human diseases and drug targeting. Biochim Biophys Acta. 2012;1824:3-13.
7. Crews CM. Feeding the machine: mechanisms of proteasomecatalyzed degradation of ubiquitinated proteins. Curr Opin Chem Biol. 2003;7:534-539.
8. Groll M, Ditzel L, Lowe J et al. Structure of 20S proteasome from yeast at 2.4 A resolution. Nature. 1997;386:463-471.
9. Hartmann-Petersen R, Seeger M, Gordon C. Transferring substrates to the 26S proteasome. Trends Biochem Sci. 2003;28:26-31.
10. McNaught KS, Olanow W. The ubiquitin-proteasome system and models of Parkinson's disease. Movement Disorders. 2004;19:S2-S3.
11. Reinstein E, Ciechanover A. Narrative review: protein degradation and human diseases: the ubiquitin connection. Ann Intern Med. 2006;145:676-684.
12. Ardley HC, Robinson PA. E3 ubiquitin ligases. Essays Biochem. 2005;41:15-30.
13. Metzger MB, Hristova VA, Weissman AM. HECT and RING finger families of E3 ubiquitin ligases at a glance. J Cell Sci. 2012;125:531-537.
14. Micel LN, Tentler JJ, Smith PG et al. Role of ubiquitin ligases and the proteasome in oncogenesis: novel targets for anticancer therapies. J Clin Oncol. 2013;31:1231-1238.
15. Kamura T, Sato S, Iwai K et al. Activation of HIF1alpha ubiquitination by a reconstituted von Hippel-Lindau (VHL) tumor suppressor complex. Proc Natl Acad Sci U S A. 2000;97:10430-10435.
16. Tanimoto K, Makino Y, Pereira T et al. Mechanism of regulation of the hypoxia-inducible factor-1 alpha by the von Hippel-Lindau tumor suppressor protein. EMBO J. 2000;19:4298-4309.
17. Peters JM, Cejka Z, Harris JR et al. Structural features of the 26 S proteasome complex. J Mol Biol. 1993;234:932-937.
18. Vinitsky A, Michaud C, Powers JC et al. Inhibition of the chymotrypsin-like activity of the pituitary multicatalytic proteinase complex. Biochemistry. 1992;31:9421-9428.
19. Genin E, Reboud-Ravaux M, Vidal J. Proteasome inhibitors: recent advances and new perspectives in medicinal chemistry. Curr Top Med Chem. 2010;10:232-256.
20. Pellom ST Jr., Shanker A. Development of Proteasome Inhibitors as Therapeutic Drugs. J Clin Cell Immunol. 2012;S5:5.
21. Wu WK, Cho CH, Lee CW et al. Proteasome inhibition: a new therapeutic strategy to cancer treatment. Cancer Lett. 2010;293:15-22.
22. Furet P, Imbach P, Noorani M et al. Entry into a new class of potent proteasome inhibitors having high antiproliferative activity by structure-based design. J Med Chem. 2004;47:4810-4813.
23. Lawasut P, Chauhan D, Laubach J et al. New proteasome inhibitors in myeloma. Curr Hematol Malig Rep. 2012;7:258-266.
24. Selimovic D, Porzig BB, El-Khattouti A et al. Bortezomib/ proteasome inhibitor triggers both apoptosis and autophagy-dependent pathways in melanoma cells. Cell Signal. 2013;25:308-318.
25. Teicher BA, Ara G, Herbst R et al. The proteasome inhibitor PS-341 in cancer therapy. Clin Cancer Res. 1999;5:2638-2645.
26. Groll M, Berkers CR, Ploegh HL et al. Crystal structure of the boronic acid-based proteasome inhibitor bortezomib in complex with the yeast 20S proteasome. Structure. 2006;14:451-456.
27. Zhang J, Wu P, Hu Y. Clinical and marketed proteasome inhibitors for cancer treatment. Curr Med Chem. 2013;20:2537-2551.
28. Qureshi AA, Guan XQ, Reis JC et al. Inhibition of nitric oxide and inflammatory cytokines in LPS-stimulated murine macrophages by resveratrol, a potent proteasome inhibitor. Lipids Health Dis. 2012;11:76.
29. Shukla Y, Singh R. Resveratrol and cellular mechanisms of cancer prevention. Ann N Y Acad Sci. 2011;1215:1-8.
30. Cherniack EP. A berry thought-provoking idea: the potential role of plant polyphenols in the treatment of age-related cognitive disorders. Br J Nutr. 2012;108:794-800.
31. Chen RJ, Ho CT, Wang YJ. Pterostilbene induces autophagy and apoptosis in sensitive and chemoresistant human bladder cancer cells. Mol Nutr Food Res. 2010;54:1819-1832.
32. Li J, Qin Z, Liang Z. The prosurvival role of autophagy in Resveratrol-induced cytotoxicity in human U251 glioma cells. BMC Cancer. 2009;9:215.
33. Mauthe M, Jacob A, Freiberger S et al. Resveratrol-mediated autophagy requires WIPI-1-regulated LC3 lipidation in the absence of induced phagophore formation. Autophagy. 2011;7:1448-1461.
34. Yamamoto M, Suzuki SO, Himeno M. Resveratrol-induced autophagy in human U373 glioma cells. Oncol Lett. 2010;1:489-493.
35. Mizushima N, Levine B, Cuervo AM, Klionsky DJ. Autophagy fights disease through cellular self-digestion. Nature. 2008;451:1069-1075.
36. Todde V, Veenhuis M, van der Klei IJ. Autophagy: principles and significance in health and disease. Biochim Biophys Acta. 2009;1792:3-13.
37. Tooze SA, Schiavo G. Liaisons dangereuses: autophagy, neuronal survival and neurodegeneration. Curr Opin Neurobiol. 2008;18:504-515.
38. Grotemeier A, Alers S, Pfisterer SG et al. AMPK-independent induction of autophagy by cytosolic Ca2+ increase. Cell Signal. 2010;22:914-925.
39. Jung CH, Ro SH, Cao J et al. mTOR regulation of autophagy. FEBS Lett. 2010;584:1287-1295.
40. Whitney ML, Jefferson LS, Kimball SR. ATF4 is necessary and sufficient for ER stress-induced upregulation of REDD1 expression. Biochem Biophys Res Commun. 2009;379:451-455.
41. Hara K, Maruki Y, Long X et al. Raptor, a binding partner of target of rapamycin (TOR), mediates TOR action. Cell. 2002;110:177-189.
42. Vander Haar E, Lee SI, Bandhakavi S et al. Insulin signalling to mTOR mediated by the Akt/PKB substrate PRAS40. Nat Cell Biol. 2007;9:316-323.
43. Zhao J, Brault JJ, Schild A et al. FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells. Cell MeTable. 2007;6:472-483.
44. Pearce LR, Huang X, Boudeau J et al. Identification of Protor as a novel Rictor-binding component of mTOR complex-2. Biochem J. 2007;405:513-522.
45. Sarbassov DD, Ali SM, Kim DH et al. Rictor, a novel binding partner of mTOR, defines a rapamycin-insensitive and raptor-independent pathway that regulates the cytoskeleton. Curr Biol. 2004;14:1296-1302.
46. Jacinto E, Facchinetti V, Liu D et al. SIN1/MIP1 maintains rictor-mTOR complex integrity and regulates Akt phosphorylation and substrate specificity. Cell. 2006;127:125-137.
47. Oh WJ, Jacinto E. mTOR complex 2 signaling and functions. Cell Cycle. 2011;10:2305-2316.
48. Polson HE, de Lartigue J, Rigden DJ et al. Mammalian Atg18 (WIPI2) localizes to omegasome-anchored phagophores and positively regulates LC3 lipidation. Autophagy. 2010;6:506-522.
49. Korolchuk VI, Menzies FM, Rubinsztein DC. Mechanisms of cross-talk between the ubiquitin-proteasome and autophagy-lysosome systems. FEBS Lett. 2010;584:1393-1398.
50. Mizushima N. The role of the Atg1/ULK1 complex in autophagy regulation. Curr Opin Cell Biol. 2010;22:132-139.
51. Liang C, Feng P, Ku B et al. UVRAG: a new player in autophagy and tumor cell growth. Autophagy. 2007;3:69-71.
52. Kihara A, Noda T, Ishihara N et al. Two distinct Vps34 phosphatidylinositol 3-kinase complexes function in autophagy and carboxypeptidase Y sorting in Saccharomyces cerevisiae. J Cell Biol. 2001;152:519-530.
53. Webber JL, Tooze SA. New insights into the function of Atg9. FEBS Lett. 2010;584:1319-1326.
54. Nazio F, Cecconi F. mTOR, AMBRA1, and autophagy: an intricate relationship. Cell Cycle. 2013;12:2524-2525.
55. Hara T, Takamura A, Kishi C et al. FIP200, a ULK-interacting protein, is required for autophagosome formation in mammalian cells. J Cell Biol. 2008;181:497-510.
56. Tanida I. Autophagy basics. Microbiol Immunol. 2011;55:1-11.
57. Hosokawa N, Sasaki T, Iemura S et al. Atg101, a novel mammalian autophagy protein interacting with Atg13. Autophagy. 2009;5:973-979.
58. Hosokawa N, Hara T, Kaizuka T et al. Nutrient-dependent mTORC1 association with the ULK1-Atg13-FIP200 complex required for autophagy. Mol Biol Cell. 2009;20:1981-1991.
59. Koren I, Reem E, Kimchi A. DAP1, a novel substrate of mTOR, negatively regulates autophagy. Curr Biol. 2010;20:1093-1098.
60. Kabeya Y, Mizushima N, Ueno T et al. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 2000;19:5720-5728.
61. von Muhlinen N, Akutsu M, Ravenhill BJ et al. LC3C, bound selectively by a noncanonical LIR motif in NDP52, is required for antibacterial autophagy. Mol Cell. 2012;48:329-342.
62. Czyzyk-Krzeska MF, Meller J, Plas DR. Not all autophagy is equal. Autophagy. 2012;8:1155-1156.
63. Mikhaylova O, Stratton Y, Hall D et al. VHL-regulated MiR-204 suppresses tumor growth through inhibition of LC3B-mediated autophagy in renal clear cell carcinoma. Cancer Cell. 2012;21:532-546.
64. Dall'Armi C, Devereaux KA, Di Paolo G. The role of lipids in the control of autophagy. Curr Biol. 2013;23:R33-45.
65. Ganley IG. Autophagosome maturation and lysosomal fusion. Essays Biochem. 2013;55:65-78.
66. Wilde IB, Brack M, Winget JM et al. Proteomic characterization of aggregating proteins after the inhibition of the ubiquitin proteasome system. J Proteome Res. 2011;10:1062-1072.
67. Komatsu M, Waguri S, Koike M et al. Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice. Cell. 2007;131:1149-1163.
68. Gao Z, Gammoh N, Wong PM et al. Processing of autophagic protein LC3 by the 20S proteasome. Autophagy. 2010;6:126-137.
69. Richter-Landsberg C, Leyk J. Inclusion body formation, macroautophagy, and the role of HDAC6 in neurodegeneration. Acta Neuropathol. 2013;126:793-807.
70. Yan J, Seibenhener ML, Calderilla-Barbosa L et al. SQSTM1/ p62 Interacts with HDAC6 and Regulates Deacetylase Activity. PLoS One. 2013;8:e76016.
71. Inoue M, Zhai H, Sakazaki H et al. TMC-95A, a reversible proteasome inhibitor, induces neurite outgrowth in PC12 cells. Bioorg Med Chem Lett. 2004;14:663-665.
72. Stauch B, Simon B, Basile T et al. Elucidation of the structure and intermolecular interactions of a reversible cyclic-peptide inhibitor of the proteasome by NMR spectroscopy and molecular modeling. Angew Chem Int Ed Engl. 2010;49:3934-3938.
73. Yang H, Landis-Piwowar KR, Chen D et al. Natural compounds with proteasome inhibitory activity for cancer prevention and treatment. Curr Protein Pept Sci. 2008;9:227-239.
74. Zhang X, Li W, Wang C et al. Inhibition of autophagy enhances apoptosis induced by proteasome inhibitor bortezomib in human glioblastoma U87 and U251 cells. Mol Cell Biochem. 2014;385:265-275.
75. Ding WX, Ni HM, Gao W et al. Linking of autophagy to ubiquitin-proteasome system is important for the regulation of endoplasmic reticulum stress and cell viability. Am J Pathol. 2007;171:513-524.
76. Li C, Johnson DE. Bortezomib induces autophagy in head and neck squamous cell carcinoma cells via JNK activation. Cancer Lett. 2012;314:102-107.
77. Lou Z, Ren T, Peng X et al. Bortezomib induces apoptosis and autophagy in osteosarcoma cells through mitogen-activated protein kinase pathway in vitro. J Int Med Res. 2013;41:1505-1519.
78. Zhang HY, Du ZX, Meng X et al. Beclin 1 enhances proteasome inhibition-mediated cytotoxicity of thyroid cancer cells in macroautophagy-independent manner. J Clin Endocrinol MeTable. 2013;98:E217-226.
79. Wu WK, Wu YC, Yu L et al. Induction of autophagy by proteasome inhibitor is associated with proliferative arrest in colon cancer cells. Biochem Biophys Res Commun. 2008;374:258-263.
80. Wu WK, Volta V, Cho CH et al. Repression of protein translation and mTOR signaling by proteasome inhibitor in colon cancer cells. Biochem Biophys Res Commun. 2009;386:598-601.
81. Wu WK, Cho CH, Lee CW et al. Macroautophagy and ERK phosphorylation counteract the antiproliferative effect of proteasome inhibitor in gastric cancer cells. Autophagy. 2010;6:228-238.
82. Shen D, Coleman J, Chan E et al. Novel cell-and tissue-based assays for detecting misfolded and aggregated protein accumulation within aggresomes and inclusion bodies. Cell Biochem Biophys. 2011;60:173-185.
83. Xiong R, Siegel D, Ross D. The activation sequence of cellular protein handling systems after proteasomal inhibition in dopaminergic cells. Chem Biol Interact. 2013;204:116-124.
84. Zhu K, Dunner K, Jr., McConkey DJ. Proteasome inhibitors activate autophagy as a cytoprotective response in human prostate cancer cells. Oncogene. 2010;29:451-462.
85. Shen YF, Tang Y, Zhang XJ et al. Adaptive changes in autophagy after UPS impairment in Parkinson's disease. Acta Pharmacol Sin. 2013;34:667-673.
86. Gimenez-Xavier P, Francisco R, Santidrian AF et al. Effects of dopamine on LC3-II activation as a marker of autophagy in a neuroblastoma cell model. Neurotoxicology. 2009;30:658-665.
87. Jiang H, Sun J, Xu Q et al. Marchantin M: a novel inhibitor of proteasome induces autophagic cell death in prostate cancer cells. Cell Death Dis. 2013;4:e761.
88. Filippi-Chiela EC, Villodre ES, Zamin LL et al. Autophagy interplay with apoptosis and cell cycle regulation in the growth inhibiting effect of resveratrol in glioma cells. PLoS One. 2011;6:e20849.
89. Chakraborty A, Bodipati N, Demonacos MK et al. Long term induction by pterostilbene results in autophagy and cellular differentiation in MCF-7 cells via ROS dependent pathway. Mol Cell Endocrinol. 2012;355:25-40.
90. Wang Y, Ding L, Wang X et al. Pterostilbene simultaneously induces apoptosis, cell cycle arrest and cyto-protective autophagy in breast cancer cells. Am J Transl Res. 2012;4:44-51.
91. Hsieh MJ, Lin CW, Yang SF et al. A combination of pterostilbene with autophagy inhibitors exerts efficient apoptotic characteristics in both chemosensitive and chemoresistant lung cancer cells. Toxicol Sci. 2014;137:65-75.
92. Siedlecka-Kroplewska K, Jozwik A, Boguslawski W et al. Pterostilbene induces accumulation of autophagic vacuoles followed by cell death in HL60 human leukemia cells. J Physiol Pharmacol. 2013;64:545-556.
93. Tanida I, Ueno T, Kominami E. LC3 and Autophagy. Methods Mol Biol. 2008;445:77-88.
94. Ni HM, Bockus A, Wozniak AL et al. Dissecting the dynamic turnover of GFP-LC3 in the autolysosome. Autophagy. 2011;7:188-204.
95. Belloni D, Veschini L, Foglieni C et al. Bortezomib induces autophagic death in proliferating human endothelial cells. Exp Cell Res. 2010;316:1010-1018.
96. Archer CR, Koomoa DL, Mitsunaga EM et al. Syrbactin class proteasome inhibitor-induced apoptosis and autophagy occurs in association with p53 accumulation and Akt/PKB activation in neuroblastoma. Biochem Pharmacol. 2010;80:170-178.
97. Klappan AK, Hones S, Mylonas I et al. Proteasome inhibition by quercetin triggers macroautophagy and blocks mTOR activity. Histochem Cell Biol. 2012;137:25-36.
98. Williams JA, Hou Y, Ni HM et al. Role of intracellular calcium in proteasome inhibitor-induced endoplasmic reticulum stress, autophagy, and cell death. Pharm Res. 2013;30:2279-2289.
99. Back JH, Zhu Y, Calabro A et al. Resveratrol-mediated downregulation of Rictor attenuates autophagic process and suppresses UV-induced skin carcinogenesis. Photochem Photobiol. 2012;88:1165-1172.
100. Wu WK, Sakamoto KM, Milani M et al. Macroautophagy modulates cellular response to proteasome inhibitors in cancer therapy. Drug Resist Updat. 2010;13:87-92.
101. Davies C, Tournier C. Exploring the function of the JNK (c-Jun N-terminal kinase) signalling pathway in physiological and pathological processes to design novel therapeutic strategies. Biochem Soc Trans. 2012;40:85-89.
102. Sabapathy K. Role of the JNK pathway in human diseases. Prog Mol Biol Transl Sci. 2012;106:145-169.
103. Kim R, Emi M, Tanabe K et al. Role of the unfolded protein response in cell death. Apoptosis. 2006;11:5-13.
104. Pavitt GD, Ron D. New insights into translational regulation in the endoplasmic reticulum unfolded protein response. Cold Spring Harb Perspect Biol. 2012;4:a012278.
105. Wei Y, Pattingre S, Sinha S et al. JNK1-mediated phosphorylation of Bcl-2 regulates starvation-induced autophagy. Mol Cell. 2008;30:678-688.
106. You SA, Basu A, Haldar S. Potent antitumor agent proteasome inhibitors: a novel trigger for Bcl2 phosphorylation to induce apoptosis. Int J Oncol. 1999;15:625-628.
107. Basu A, Haldar S. Signal-induced site specific phosphorylation targets Bcl2 to the proteasome pathway. Int J Oncol. 2002;21:597-601.
108. Jiang HY, Wek RC. Phosphorylation of the alpha-subunit of the eukaryotic initiation factor-2 (eIF2alpha) reduces protein synthesis and enhances apoptosis in response to proteasome inhibition. J Biol Chem. 2005;280:14189-14202.
109. Acharya P, Engel JC, Correia MA. Hepatic CYP3A suppression by high concentrations of proteasomal inhibitors: a consequence of endoplasmic reticulum (ER) stress induction, activation of RNA-dependent protein kinase-like ER-bound eukaryotic initiation factor 2alpha (eIF2alpha)-kinase (PERK) and general control nonderepressible-2 eIF2alpha kinase (GCN2), and global translational shutoff. Mol Pharmacol. 2009;76:503-515.
110. Gavilan MP, Pintado C, Gavilan E et al. Dysfunction of the unfolded protein response increases neurodegeneration in aged rat hippocampus following proteasome inhibition. Aging Cell. 2009;8:654-665.
111. Rouschop KM, van den Beucken T, Dubois L et al. The unfolded protein response protects human tumor cells during hypoxia through regulation of the autophagy genes MAP1LC3B and ATG5. J Clin Invest. 2010;120:127-141.
112. Cusimano A, Azzolina A, Iovanna JL et al. Novel combination of celecoxib and proteasome inhibitor MG132 provides synergistic antiproliferative and proapoptotic effects in human liver tumor cells. Cell Cycle. 2010;9:1399-1410.
113. Hu J, Dang N, Menu E et al. Activation of ATF4 mediates unwanted Mcl-1 accumulation by proteasome inhibition. Blood. 2012;119:826-837.
114. Bardag-Gorce F. Proteasome inhibitor treatment in alcoholic liver disease. World J Gastroenterol. 2011;17:2558-2562.
115. Ohta K, Mizuno A, Ueda M et al. Autophagy impairment stimulates PS1 expression and gamma-secretase activity. Autophagy. 2010;6:345-352.
116. Suzuki T, Osumi N, Wakamatsu Y. Stabilization of ATF4 protein is required for the regulation of epithelial-mesenchymal transition of the avian neural crest. Dev Biol. 2010;344:658-668.
117. Milani M, Rzymski T, Mellor HR et al. The role of ATF4 stabilization and autophagy in resistance of breast cancer cells treated with Bortezomib. Cancer Res. 2009;69:4415-4423.
118. Lassot I, Segeral E, Berlioz-Torrent C et al. ATF4 degradation relies on a phosphorylation-dependent interaction with the SCF(betaTrCP) ubiquitin ligase. Mol Cell Biol. 2001;21:2192-2202.
119. Martelli AM, Evangelisti C, Chiarini F et al. The phosphatidylinositol 3-kinase/Akt/mTOR signaling network as a therapeutic target in acute myelogenous leukemia patients. Oncotarget. 2010;1:89-103.
120. Ikenoue T, Hong S, Inoki K. Monitoring mammalian target of rapamycin (mTOR) activity. Methods Enzymol. 2009;452:165-180.
121. Ghosh P, Wu M, Zhang H et al. mTORC1 signaling requires proteasomal function and the involvement of CUL4-DDB1 ubiquitin E3 ligase. Cell Cycle. 2008;7:373-381.
122. Bruning A, Rahmeh M, Friese K. Nelfinavir and bortezomib inhibit mTOR activity via ATF4-mediated sestrin-2 regulation. Mol Oncol. 2013;7:1012-1018.
123. Ben-Sahra I, Dirat B, Laurent K et al. Sestrin2 integrates Akt and mTOR signaling to protect cells against energetic stress-induced death. Cell Death Differ. 2013;20:611-619.
124. Maiuri MC, Malik SA, Morselli E et al. Stimulation of autophagy by the p53 target gene Sestrin2. Cell Cycle. 2009;8:1571-1576.
125. Lun M, Zhang PL, Siegelmann-Danieli N et al. Intracellular inhibitory effects of Velcade correlate with morphoproteomic expression of phosphorylated-nuclear factor-kappaB and p53 in breast cancer cell lines. Ann Clin Lab Sci. 2005;35:15-24.
126. Du Y, Yang D, Li L et al. An insight into the mechanistic role of p53-mediated autophagy induction in response to proteasomal inhibition-induced neurotoxicity. Autophagy. 2009;5:663-675.
127. Zhang XY, Wu XQ, Deng R et al. Upregulation of sestrin 2 expression via JNK pathway activation contributes to autophagy induction in cancer cells. Cell Signal. 2013;25:150-158.
128. Zhang L, Cui L, Zhou G et al. Pterostilbene, a natural small-molecular compound, promotes cytoprotective macroautophagy in vascular endothelial cells. J Nutr Biochem. 2013;24:903-911.
129. Kopito RR. Aggresomes, inclusion bodies and protein aggregation. Trends Cell Biol. 2000;10:524-530.
130. Kuusisto E, Suuronen T, Salminen A. Ubiquitin-binding protein p62 expression is induced during apoptosis and proteasomal inhibition in neuronal cells. Biochem Biophys Res Commun. 2001;280:223-228.
131. Myeku N, Figueiredo-Pereira ME. Dynamics of the degradation of ubiquitinated proteins by proteasomes and autophagy: association with sequestosome 1/p62. J Biol Chem. 2011;286:22426-22440.
132. Viiri J, Amadio M, Marchesi N et al. Autophagy activation clears ELAVL1/HuR-mediated accumulation of SQSTM1/ p62 during proteasomal inhibition in human retinal pigment epithelial cells. PLoS One. 2013;8:e69563.
133. Jaakkola PM, Pursiheimo JP. p62 degradation by autophagy: another way for cancer cells to survive under hypoxia. Autophagy. 2009;5:410-412.
134. Kawaguchi Y, Kovacs JJ, McLaurin A et al. The deacetylase HDAC6 regulates aggresome formation and cell viability in response to misfolded protein stress. Cell. 2003;115:727-738.
135. Pandey UB, Nie Z, Batlevi Y et al. HDAC6 rescues neurodegeneration and provides an essential link between autophagy and the UPS. Nature. 2007;447:859-863.
136. Kastle M, Woschee E, Grune T. Histone deacetylase 6 (HDAC6) plays a crucial role in p38MAPK-dependent induction of heme oxygenase-1 (HO-1) in response to proteasome inhibition. Free Radic Biol Med. 2012;53:2092-2101.
137. Anckar J, Sistonen L. Regulation of HSF1 function in the heat stress response: implications in aging and disease. Annu Rev Biochem. 2011;80:1089-1115.
138. Boyault C, Zhang Y, Fritah S et al. HDAC6 controls major cell response pathways to cytotoxic accumulation of protein aggregates. Genes Dev. 2007;21:2172-2181.
139. Bonelli P, Petrella A, Rosati A et al. BAG3 protein regulates stress-induced apoptosis in normal and neoplastic leukocytes. Leukemia. 2004;18:358-360.
140. Gamerdinger M, Kaya AM, Wolfrum U et al. BAG3 mediates chaperone-based aggresome-targeting and selective autophagy of misfolded proteins. EMBO Rep. 2011;12:149-156.
141. Behl C. BAG3 and friends: co-chaperones in selective autophagy during aging and disease. Autophagy. 2011;7:795-798.
142. Rapino F, Jung M, Fulda S. BAG3 induction is required to mitigate proteotoxicity via selective autophagy following inhibition of constitutive protein degradation pathways. Oncogene. 2013. DOI:10.1038/onc.2013.110. [Epub ahead of print].
143. Liu BQ, Du ZX, Zong ZH et al. BAG3-dependent noncanonical autophagy induced by proteasome inhibition in HepG2 cells. Autophagy. 2013;9:905-916.
144. Sakairi T, Hiromura K, Takahashi S et al. Effects of proteasome inhibitors on rat renal fibrosis in vitro and in vivo. Nephrology (Carlton). 2011;16:76-86.