Proteostasis, oxidative stress and aging

Redox Biology

Volumn 13, Issue , 2017, Pages 550-567

  Korovila, Ioanna ^a   Hugo, Martín ^a   Castro, José Pedro ^a,b,e,f   Weber, Daniela ^a,d   Höhn, Annika ^a,b   Grune, Tilman ^a,b,c,d   Jung, Tobias ^a,c  

^a GERMAN INSTITUTE OF HUMAN NUTRITION   (Germany)

^b GERMAN CENTER FOR DIABETES RESEARCH DZD   (Germany)

^c DZHK GERMAN CENTRE FOR CARDIOVASCULAR RESEARCH   (Germany)

^d NutriAct Competence Cluster for Nutritional Sciences Berlin Potsdam   (Germany)

^e University of Porto   (Portugal)

^f UNIVERSITY OF PORTO   (Portugal)

Author keywords

Autophagy; Lysosome; Oxidative stress; Proteasome; Redox shift

Indexed keywords

11S REGULATOR PROTEIN; 19S REGULATOR PROTEIN; 20S PROTEASOME; 26S PROTEASOME; ADVANCED GLYCATION END PRODUCT; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IMMUNOPROTEASOME; LIPOFUSCIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; PA200 PROTEIN; PROTEASOME; REGULATOR PROTEIN; TRANSCRIPTION FACTOR NRF1; TRANSCRIPTION FACTOR NRF2; UBIQUITIN; UNCLASSIFIED DRUG;

AGING; AUTOPHAGY; CHAPERONE-MEDIATED AUTOPHAGY; DETOXIFICATION; DNA REPAIR; ENDOCYTOSIS; ENZYME SPECIFICITY; HUMAN; IMMUNE RESPONSE; LYSOSOME; MACROAUTOPHAGY; MICROAUTOPHAGY; NONHUMAN; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN HOMEOSTASIS; PROTEIN MODIFICATION; PROTEIN UNFOLDING; REVIEW; SPERMATOGENESIS; UBIQUITIN PROTEASOMAL SYSTEM; UBIQUITINATION; UNFOLDED PROTEIN RESPONSE; ANIMAL; METABOLISM;

AGING; ANIMALS; AUTOPHAGY; GLYCATION END PRODUCTS, ADVANCED; HUMANS; LIPOFUSCIN; OXIDATIVE STRESS; PROTEOSTASIS;

EID: 85026547975     PISSN: 22132317     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.redox.2017.07.008     Document Type: Review

References (199)

1. Sautin, Y.Y., Johnson, R.J., Uric acid: the oxidant-antioxidant paradox. Nucleosides Nucleotides Nucleic Acids 27 (2008), 608–619.
2. Schafer, F.Q., Buettner, G.R., Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radic. Biol. Med. 30 (2001), 1191–1212.
3. Valko, M., Jomova, K., Rhodes, C.J., Kuca, K., Musilek, K., Redox- and non-redox-metal-induced formation of free radicals and their role in human disease. Arch. Toxicol. 90 (2016), 1–37.
4. La Penna, G., Hureau, C., Andreussi, O., Faller, P., Identifying, by first-principles simulations, Cu[amyloid-beta] species making Fenton-type reactions in Alzheimer's disease. J. Phys. Chem. B 117 (2013), 16455–16467.
5. Rock, K.L., Gramm, C., Rothstein, L., Clark, K., Stein, R., Dick, L., Hwang, D., Goldberg, A.L., 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.
6. Hoshi, T., Heinemann, S., Regulation of cell function by methionine oxidation and reduction. J. Physiol. 531 (2001), 1–11.
7. Suzuki, S., Kodera, Y., Saito, T., Fujimoto, K., Momozono, A., Hayashi, A., Kamata, Y., Shichiri, M., Methionine sulfoxides in serum proteins as potential clinical biomarkers of oxidative stress. Sci. Rep., 6, 2016, 38299.
8. Stadtman, E.R., Van Remmen, H., Richardson, A., Wehr, N.B., Levine, R.L., Methionine oxidation and aging. Biochim. Biophys. Acta 1703 (2005), 135–140.
9. Stadtman, E.R., Protein oxidation and aging. Free Radic. Res. 40 (2006), 1250–1258.
10. Jonsson, T.J., Lowther, W.T., The peroxiredoxin repair proteins. Subcell. Biochem. 44 (2007), 115–141.
11. Perkins, A., Nelson, K.J., Parsonage, D., Poole, L.B., Karplus, P.A., Peroxiredoxins: guardians against oxidative stress and modulators of peroxide signaling. Trends Biochem. Sci. 40 (2015), 435–445.
12. Huh, J.Y., Kim, Y., Jeong, J., Park, J., Kim, I., Huh, K.H., Kim, Y.S., Woo, H.A., Rhee, S.G., Lee, K.J., Ha, H., Peroxiredoxin 3 is a key molecule regulating adipocyte oxidative stress, mitochondrial biogenesis, and adipokine expression. Antioxid. Redox Signal 16 (2012), 229–243.
13. Handy, D.E., Loscalzo, J., Redox regulation of mitochondrial function. Antioxid. Redox Signal 16 (2012), 1323–1367.
14. Poole, L.B., The basics of thiols and cysteines in redox biology and chemistry. Free Radic. Biol. Med. 80 (2015), 148–157.
15. Kalinina, E.V., Chernov, N.N., Novichkova, M.D., Role of glutathione, glutathione transferase, and glutaredoxin in regulation of redox-dependent processes. Biochemistry 79 (2014), 1562–1583.
16. Mailloux, R.J., Willmore, W.G., S-glutathionylation reactions in mitochondrial function and disease. Front. Cell Dev. Biol., 2, 2014, 68.
17. Jung, T., Catalgol, B., Grune, T., The proteasomal system. Mol. Asp. Med. 30 (2009), 191–296.
18. Levine, R.L., Berlett, B.S., Moskovitz, J., Mosoni, L., Stadtman, E.R., Methionine residues may protect proteins from critical oxidative damage. Mech. Ageing Dev. 107 (1999), 323–332.
19. Levine, R.L., Mosoni, L., Berlett, B.S., Stadtman, E.R., Methionine residues as endogenous antioxidants in proteins. Proc. Natl. Acad. Sci. USA 93 (1996), 15036–15040.
20. Lilienbaum, A., Relationship between the proteasomal system and autophagy. Int. J. Biochem. Mol. Biol. 4 (2013), 1–26.
21. Jung, T., Engels, M., Kaiser, B., Poppek, D., Grune, T., Intracellular distribution of oxidized proteins and proteasome in HT22 cells during oxidative stress. Free Radic. Biol. Med. 40 (2006), 1303–1312.
22. Jung, T., Grune, T., The proteasome and the degradation of oxidized proteins: Part I-structure of proteasomes. Redox Biol. 1 (2013), 178–182.
23. Arendt, C.S., Hochstrasser, M., Identification of the yeast 20S proteasome catalytic centers and subunit interactions required for active-site formation. Proc. Natl. Acad. Sci. USA 94 (1997), 7156–7161.
24. Jager, S., Groll, M., Huber, R., Wolf, D.H., Heinemeyer, W., Proteasome beta-type subunits: unequal roles of propeptides in core particle maturation and a hierarchy of active site function. J. Mol. Biol. 291 (1999), 997–1013.
25. Orlowski, M., Wilk, S., Catalytic activities of the 20 S proteasome, a multicatalytic proteinase complex. Arch. Biochem. Biophys. 383 (2000), 1–16.
26. Groll, M., Bajorek, M., Kohler, A., Moroder, L., Rubin, D.M., Huber, R., Glickman, M.H., Finley, D., A gated channel into the proteasome core particle. Nat. Struct. Biol. 7 (2000), 1062–1067.
27. Wenzel, T., Baumeister, W., Conformational constraints in protein degradation by the 20S proteasome. Nat. Struct. Biol. 2 (1995), 199–204.
28. Pacifici, R.E., Salo, D.C., Davies, K.J., Macroxyproteinase (M.O.P.): a 670 kDa proteinase complex that degrades oxidatively denatured proteins in red blood cells. Free Radic. Biol. Med 7 (1989), 521–536.
29. Lasch, P., Petras, T., Ullrich, O., Backmann, J., Naumann, D., Grune, T., Hydrogen peroxide-induced structural alterations of RNAse A. J. Biol. Chem. 276 (2001), 9492–9502.
30. Reeg, S., Jung, T., Castro, J.P., Davies, K.J., Henze, A., Grune, T., The molecular chaperone Hsp70 promotes the proteolytic removal of oxidatively damaged proteins by the proteasome. Free Radic. Biol. Med. 99 (2016), 153–166.
31. Karademir, B., Bozaykut, P., Kartal Ozer, N., Heat shock proteins and proteasomal degradation in normal and tumor cells. Free Radic. Biol. Med, 75(Suppl 1), 2014, S35.
32. Rabl, J., Smith, D.M., Yu, Y., Chang, S.C., Goldberg, A.L., Cheng, Y., Mechanism of gate opening in the 20S proteasome by the proteasomal ATPases. Mol. Cell 30 (2008), 360–368.
33. Luciani, F., Kesmir, C., Mishto, M., Or-Guil, M., de Boer, R.J., A mathematical model of protein degradation by the proteasome. Biophys. J. 88 (2005), 2422–2432.
34. Kish-Trier, E., Hill, C.P., Structural biology of the proteasome. Annu. Rev. Biophys. 42 (2013), 29–49.
35. Wehmer, M., Sakata, E., Recent advances in the structural biology of the 26S proteasome. Int. J. Biochem. Cell Biol. 79 (2016), 437–442.
36. Bedford, L., Paine, S., Sheppard, P.W., Mayer, R.J., Roelofs, J., Assembly, structure, and function of the 26S proteasome. Trends Cell Biol. 20 (2010), 391–401.
37. Aizawa, H., Kawahara, H., Tanaka, K., Yokosawa, H., Activation of the proteasome during Xenopus egg activation implies a link between proteasome activation and intracellular calcium release. Biochem. Biophys. Res. Commun. 218 (1996), 224–228.
38. Cascio, P., Call, M., Petre, B.M., Walz, T., Goldberg, A.L., Properties of the hybrid form of the 26S proteasome containing both 19S and PA28 complexes. EMBO J. 21 (2002), 2636–2645.
39. Hohn, A., Konig, J., Jung, T., Metabolic Syndrome, Redox State, and the Proteasomal System. Antioxid. Redox Signal 25 (2016), 902–917.
40. Tsvetkov, P., Myers, N., Eliav, R., Adamovich, Y., Hagai, T., Adler, J., Navon, A., Shaul, Y., NADH binds and stabilizes the 26S proteasomes independent of ATP. J. Biol. Chem. 289 (2014), 11272–11281.
41. Clague, M.J., Heride, C., Urbe, S., The demographics of the ubiquitin system. Trends Cell Biol. 25 (2015), 417–426.
42. Tai, H.C., Schuman, E.M., Ubiquitin, the proteasome and protein degradation in neuronal function and dysfunction. Nat. Rev. Neurosci. 9 (2008), 826–838.
43. Schulman, B.A., Harper, J.W., Ubiquitin-like protein activation by E1 enzymes: the apex for downstream signalling pathways. Nat. Rev. Mol. Cell Biol. 10 (2009), 319–331.
44. Ristic, G., Tsou, W.L., Todi, S.V., An optimal ubiquitin-proteasome pathway in the nervous system: the role of deubiquitinating enzymes. Front. Mol. Neurosci., 7, 2014, 72.
45. Metzger, M.B., Pruneda, J.N., Klevit, R.E., Weissman, A.M., RING-type E3 ligases: master manipulators of E2 ubiquitin-conjugating enzymes and ubiquitination. Biochim. Biophys. Acta 1843 (2014), 47–60.
46. Ashizawa, A., Higashi, C., Masuda, K., Ohga, R., Taira, T., Fujimuro, M., The ubiquitin system and Kaposi's sarcoma-associated Herpesvirus. Front. Microbiol., 3, 2012, 66.
47. Zhao, S., Ulrich, H.D., Distinct consequences of posttranslational modification by linear versus K63-linked polyubiquitin chains. Proc. Natl. Acad. Sci. USA 107 (2010), 7704–7709.
48. Kravtsova-Ivantsiv, Y., Ciechanover, A., Non-canonical ubiquitin-based signals for proteasomal degradation. J. Cell Sci. 125 (2012), 539–548.
49. Stewart, D.P., Koss, B., Bathina, M., Perciavalle, R.M., Bisanz, K., Opferman, J.T., Ubiquitin-independent degradation of antiapoptotic MCL-1. Mol. Cell. Biol. 30 (2010), 3099–3110.
50. Zhou, S., Dewille, J.W., Proteasome-mediated CCAAT/enhancer-binding protein delta (C/EBPdelta) degradation is ubiquitin-independent. Biochem. J. 405 (2007), 341–349.
51. Murakami, Y., Matsufuji, S., Kameji, T., Hayashi, S., Igarashi, K., Tamura, T., Tanaka, K., Ichihara, A., Ornithine decarboxylase is degraded by the 26S proteasome without ubiquitination. Nature 360 (1992), 597–599.
52. Schwartz, A.L., Ciechanover, A., Targeting proteins for destruction by the ubiquitin system: implications for human pathobiology. Annu Rev. Pharmacol. Toxicol. 49 (2009), 73–96.
53. Wolberger, C., Mechanisms for regulating deubiquitinating enzymes. Protein Sci. 23 (2014), 344–353.
54. Urbe, S., Liu, H., Hayes, S.D., Heride, C., Rigden, D.J., Clague, M.J., Systematic survey of deubiquitinase localization identifies USP21 as a regulator of centrosome- and microtubule-associated functions. Mol. Biol. Cell 23 (2012), 1095–1103.
55. Desvergne, A., Ugarte, N., Petropoulos, I., Friguet, B., Circadian modulation of proteasome activities and removal of carbonylated proteins. Free Radic. Biol. Med., 75(Suppl 1), 2014, S18.
56. Vriend, J., Reiter, R.J., Melatonin feedback on clock genes: a theory involving the proteasome. J. Pineal Res. 58 (2015), 1–11.
57. Diaz-Villanueva, J.F., Diaz-Molina, R., Garcia-Gonzalez, V., Protein folding and mechanisms of proteostasis. Int. J. Mol. Sci. 16 (2015), 17193–17230.
58. Mao, I., Liu, J., Li, X., Luo, H., REGgamma, a proteasome activator and beyond?. Cell Mol. Life Sci. 65 (2008), 3971–3980.
59. Zanker, D., Waithman, J., Yewdell, J.W., Chen, W., Mixed proteasomes function to increase viral peptide diversity and broaden antiviral CD8+ T cell responses. J. Immunol. 191 (2013), 52–59.
60. Mishto, M., Liepe, J., Textoris-Taube, K., Keller, C., Henklein, P., Weberruss, M., Dahlmann, B., Enenkel, C., Voigt, A., Kuckelkorn, U., Stumpf, M.P., Kloetzel, P.M., Proteasome isoforms exhibit only quantitative differences in cleavage and epitope generation. Eur. J. Immunol. 44 (2014), 3508–3521.
61. Hulpke, S., Tampe, R., The MHC I loading complex: a multitasking machinery in adaptive immunity. Trends Biochem. Sci. 38 (2013), 412–420.
62. Zanker, D., Chen, W., Standard and immunoproteasomes show similar peptide degradation specificities. Eur. J. Immunol. 44 (2014), 3500–3503.
63. Dubiel, W., Pratt, G., Ferrell, K., Rechsteiner, M., Purification of an 11 S regulator of the multicatalytic protease. J. Biol. Chem. 267 (1992), 22369–22377.
64. Di Cola, D., Human erythrocyte contains a factor that stimulates the peptidase activities of multicatalytic proteinase complex. Ital. J. Biochem. 41 (1992), 213–224.
65. Kuehn, L., Dahlmann, B., Proteasome activator PA28 and its interaction with 20 S proteasomes. Arch. Biochem. Biophys. 329 (1996), 87–96.
66. Ferrington, D.A., Gregerson, D.S., Immunoproteasomes: structure, function, and antigen presentation. Prog. Mol. Biol. Transl. Sci. 109 (2012), 75–112.
67. Caniard, A., Ballweg, K., Lukas, C., Yildirim, A.O., Eickelberg, O., Meiners, S., Proteasome function is not impaired in healthy aging of the lung. Aging 7 (2015), 776–792.
68. McCarthy, M.K., Weinberg, J.B., The immunoproteasome and viral infection: a complex regulator of inflammation. Front. Microbiol., 6, 2015, 21.
69. van Deventer, S., Neefjes, J., The immunoproteasome cleans up after inflammation. Cell 142 (2010), 517–518.
70. Johnston-Carey, H.K., Pomatto, L.C., Davies, K.J., The Immunoproteasome in oxidative stress, aging, and disease. Crit. Rev. Biochem. Mol. Biol. 51 (2015), 268–281.
71. Agarwal, A.K., Xing, C., Demartino, G.N., Mizrachi, D., Hernandez, M.D., Sousa, A.B., Martinez, d., V., dos Santos, H.G., Garg, A., PSMB8 encoding the beta5i proteasome subunit is mutated in joint contractures, muscle atrophy, microcytic anemia, and panniculitis-induced lipodystrophy syndrome. Am. J. Hum. Genet. 87 (2010), 866–872.
72. Kunimoto, K., Kimura, A., Uede, K., Okuda, M., Aoyagi, N., Furukawa, F., Kanazawa, N., A new infant case of Nakajo-Nishimura syndrome with a genetic mutation in the immunoproteasome subunit: an overlapping entity with JMP and CANDLE syndrome related to PSMB8 mutations. Dermatology 227 (2013), 26–30.
73. Arima, K., Kinoshita, A., Mishima, H., Kanazawa, N., Kaneko, T., Mizushima, T., Ichinose, K., Nakamura, H., Tsujino, A., Kawakami, A., Matsunaka, M., Kasagi, S., Kawano, S., Kumagai, S., Ohmura, K., Mimori, T., Hirano, M., Ueno, S., Tanaka, K., Tanaka, M., Toyoshima, I., Sugino, H., Yamakawa, A., Tanaka, K., Niikawa, N., Furukawa, F., Murata, S., Eguchi, K., Ida, H., Yoshiura, K., Proteasome assembly defect due to a proteasome subunit beta type 8 (PSMB8) mutation causes the autoinflammatory disorder, Nakajo-Nishimura syndrome. Proc. Natl. Acad. Sci. USA 108 (2011), 14914–14919.
74. Pickering, A.M., Lehr, M., Miller, R.A., Lifespan of mice and primates correlates with immunoproteasome expression. J. Clin. Investig. 125 (2015), 2059–2068.
75. Gavilan, M.P., Castano, A., Torres, M., Portavella, M., Caballero, C., Jimenez, S., Garcia-Martinez, A., Parrado, J., Vitorica, J., Ruano, D., Age-related increase in the immunoproteasome content in rat hippocampus: molecular and functional aspects. J. Neurochem. 108 (2009), 260–272.
76. Stratford, F.L., Chondrogianni, N., Trougakos, I.P., Gonos, E.S., Rivett, A.J., Proteasome response to interferon-gamma is altered in senescent human fibroblasts. FEBS Lett. 580 (2006), 3989–3994.
77. Pickering, A.M., Linder, R.A., Zhang, H., Forman, H.J., Davies, K.J., Nrf2-dependent induction of proteasome and Pa28alphabeta regulator are required for adaptation to oxidative stress. J. Biol. Chem. 287 (2012), 10021–10031.
78. Wright, K.L., White, L.C., Kelly, A., Beck, S., Trowsdale, J., Ting, J.P., Coordinate regulation of the human TAP1 and LMP2 genes from a shared bidirectional promoter. J. Exp. Med. 181 (1995), 1459–1471.
79. Nitta, T., Murata, S., Sasaki, K., Fujii, H., Ripen, A.M., Ishimaru, N., Koyasu, S., Tanaka, K., Takahama, Y., Thymoproteasome shapes immunocompetent repertoire of CD8+ T cells. Immunity 32 (2010), 29–40.
80. Xing, Y., Jameson, S.C., Hogquist, K.A., Thymoproteasome subunit-beta5T generates peptide-MHC complexes specialized for positive selection. Proc. Natl. Acad. Sci. USA 110 (2013), 6979–6984.
81. Murata, S., Sasaki, K., Kishimoto, T., Niwa, S., Hayashi, H., Takahama, Y., Tanaka, K., Regulation of CD8+ T cell development by thymus-specific proteasomes. Science 316 (2007), 1349–1353.
82. 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.
83. Fort, P., Kajava, A.V., Delsuc, F., Coux, O., Evolution of proteasome regulators in eukaryotes. Genome Biol. Evol. 7 (2015), 1363–1379.
84. Henderson, A., Erales, J., Hoyt, M.A., Coffino, P., Dependence of proteasome processing rate on substrate unfolding. J. Biol. Chem. 286 (2011), 17495–17502.
85. Liepe, J., Holzhutter, H.G., Bellavista, E., Kloetzel, P.M., Stumpf, M.P., Mishto, M., Quantitative time-resolved analysis reveals intricate, differential regulation of standard- and immuno-proteasomes. Elife, 4, 2015, e07545.
86. Demasi, M., Shringarpure, R., Davies, K.J., Glutathiolation of the proteasome is enhanced by proteolytic inhibitors. Arch. Biochem. Biophys. 389 (2001), 254–263.
87. Zmijewski, J.W., Banerjee, S., Abraham, E., S-glutathionylation of the Rpn2 regulatory subunit inhibits 26 S proteasomal function. J. Biol. Chem. 284 (2009), 22213–22221.
88. Silva, G.M., Netto, L.E., Discola, K.F., Piassa-Filho, G.M., Pimenta, D.C., Barcena, J.A., Demasi, M., Role of glutaredoxin 2 and cytosolic thioredoxins in cysteinyl-based redox modification of the 20S proteasome. FEBS J. 275 (2008), 2942–2955.
89. Hohn, T.J., Grune, T., The proteasome and the degradation of oxidized proteins: part III-Redox regulation of the proteasomal system. Redox Biol. 2 (2014), 388–394.
90. Ullrich, O., Reinheckel, T., Sitte, N., Hass, R., Grune, T., Davies, K.J., Poly-ADP ribose polymerase activates nuclear proteasome to degrade oxidatively damaged histones. Proc. Natl. Acad. Sci. USA 96 (1999), 6223–6228.
91. Szabo, E., Kovacs, I., Grune, T., Haczku, A., Virag, L., PARP-1: a new player in the asthma field?. Allergy 66 (2011), 811–814.
92. Jung, T., Hohn, A., Grune, T., The proteasome and the degradation of oxidized proteins: Part II - protein oxidation and proteasomal degradation. Redox Biol. 2 (2014), 99–104.
93. Shang, F., Taylor, A., Ubiquitin-proteasome pathway and cellular responses to oxidative stress. Free Radic. Biol. Med. 51 (2011), 5–16.
94. Pickering, A.M., Davies, K.J., Differential roles of proteasome and immunoproteasome regulators Pa28alphabeta, Pa28gamma and Pa200 in the degradation of oxidized proteins. Arch. Biochem. Biophys. 523 (2012), 181–190.
95. Davies, K.J., Adaptive homeostasis. Mol. Asp. Med. 49 (2016), 1–7.
96. Settembre, C., Fraldi, A., Medina, D.L., Ballabio, A., Signals from the lysosome: a control centre for cellular clearance and energy metabolism. Nat. Rev. Mol. Cell Biol. 14 (2013), 283–296.
97. Piao, S., Amaravadi, R.K., Targeting the lysosome in cancer. Ann. N.Y. Acad. Sci. 1371 (2016), 45–54.
98. Mony, V.K., Benjamin, S., O'Rourke, E.J., A lysosome-centered view of nutrient homeostasis. Autophagy 12 (2016), 619–631.
99. Tsukamoto, S., Hara, T., Yamamoto, A., Ohta, Y., Wada, A., Ishida, Y., Kito, S., Nishikawa, T., Minami, N., Sato, K., Kokubo, T., Functional analysis of lysosomes during mouse preimplantation embryo development. J. Reprod. Dev. 59 (2013), 33–39.
100. Li, W., Yang, Q., Mao, Z., Chaperone-mediated autophagy: machinery, regulation and biological consequences. Cell Mol. Life Sci. 68 (2011), 749–763.
101. Stoka, V., Turk, V., Turk, B., Lysosomal cathepsins and their regulation in aging and neurodegeneration. Ageing Res. Rev., 2016.
102. Konig, J., Besoke, F., Stuetz, W., Malarski, A., Jahreis, G., Grune, T., Hohn, A., Quantification of age-related changes of alpha-tocopherol in lysosomal membranes in murine tissues and human fibroblasts. Biofactors 42 (2016), 307–315.
103. De Duve, C., The lysosome. Sci. Am. 208 (1963), 64–72.
104. Feng, Y., He, D., Yao, Z., Klionsky, D.J., The machinery of macroautophagy. Cell Res. 24 (2014), 24–41.
105. Esclatine, A., Chaumorcel, M., Codogno, P., Macroautophagy signaling and regulation. Curr. Top. Microbiol. Immunol. 335 (2009), 33–70.
106. Gallagher, L.E., Williamson, L.E., Chan, E.Y., Advances in autophagy regulatory mechanisms. Cells, 5, 2016.
107. Svenning, S., Johansen, T., Selective autophagy. Essays Biochem. 55 (2013), 79–92.
108. Lemasters, J.J., Selective mitochondrial autophagy, or mitophagy, as a targeted defense against oxidative stress, mitochondrial dysfunction, and aging. Rejuvenation Res. 8 (2005), 3–5.
109. Shaik, A., Schiavi, A., Ventura, N., Mitochondrial autophagy promotes healthy aging. Cell Cycle 15 (2016), 1805–1806.
110. Bauckman, K.A., Owusu-Boaitey, N., Mysorekar, I.U., Selective autophagy: xenophagy. Methods 75 (2015), 120–127.
111. Cheong, H., Klionsky, D.J., mTORC1 maintains metabolic balance. Cell Res. 25 (2015), 1085–1086.
112. Gallagher, L.E., Chan, E.Y., Early signalling events of autophagy. Essays Biochem. 55 (2013), 1–15.
113. Kim, J., Kim, Y.C., Fang, C., Russell, R.C., Kim, J.H., Fan, W., Liu, R., Zhong, Q., Guan, K.L., Differential regulation of distinct Vps34 complexes by AMPK in nutrient stress and autophagy. Cell 152 (2013), 290–303.
114. Huber, L.A., Teis, D., Lysosomal signaling in control of degradation pathways. Curr. Opin. Cell Biol. 39 (2016), 8–14.
115. Klionsky, D.J., Eskelinen, E.L., Deretic, V., Autophagosomes, phagosomes, autolysosomes, phagolysosomes, autophagolysosomes.. wait, I'm confused. Autophagy 10 (2014), 549–551.
116. Xilouri, M., Stefanis, L., Chaperone mediated autophagy in aging: starve to prosper. Ageing Res. Rev., 2016.
117. Morozova, K., Clement, C.C., Kaushik, S., Stiller, B., Arias, E., Ahmad, A., Rauch, J.N., Chatterjee, V., Melis, C., Scharf, B., Gestwicki, J.E., Cuervo, A.M., Zuiderweg, E.R., Santambrogio, L., Structural and biological interaction of hsc-70 protein with phosphatidylserine in endosomal microautophagy. J. Biol. Chem. 291 (2016), 18096–18106.
118. Li, W.W., Li, J., Bao, J.K., Microautophagy: lesser-known self-eating. Cell Mol. Life Sci. 69 (2012), 1125–1136.
119. Cuervo, A.M., Wong, E., Chaperone-mediated autophagy: roles in disease and aging. Cell Res. 24 (2014), 92–104.
120. Kaushik, S., Cuervo, A.M., Chaperones in autophagy. Pharmacol. Res. 66 (2012), 484–493.
121. Stricher, F., Macri, C., Ruff, M., Muller, S., HSPA8/HSC70 chaperone protein: structure, function, and chemical targeting. Autophagy 9 (2013), 1937–1954.
122. 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.
123. Sahu, R., Kaushik, S., Clement, C.C., Cannizzo, E.S., Scharf, B., Follenzi, A., Potolicchio, I., Nieves, E., Cuervo, A.M., Santambrogio, L., Microautophagy of cytosolic proteins by late endosomes. Dev. Cell 20 (2011), 131–139.
124. Yuan, Y., Pan, S.S., Shen, Y.J., Cardioprotection of exercise preconditioning involving heat shock protein 70 and concurrent autophagy: a potential chaperone-assisted selective macroautophagy effect. J. Physiol. Sci., 2016.
125. Ulbricht, A., Gehlert, S., Leciejewski, B., Schiffer, T., Bloch, W., Hohfeld, J., Induction and adaptation of chaperone-assisted selective autophagy CASA in response to resistance exercise in human skeletal muscle. Autophagy 11 (2015), 538–546.
126. Jadhav, T.S., Wooten, M.W., Wooten, M.C., Mining the TRAF6/p62 interactome for a selective ubiquitination motif. BMC Proc., 5(Suppl 2), 2011, S4.
127. Phadwal, K., Analyzing the colocalization of MAP1LC3 and lysosomal markers in primary cells. Cold Spring Harb. Protoc., 2015, 2015 (2015:pdb prot086272).
128. Kansanen, E., Kuosmanen, S.M., Leinonen, H., Levonen, A.L., The Keap1-Nrf2 pathway: mechanisms of activation and dysregulation in cancer. Redox Biol. 1 (2013), 45–49.
129. Bryan, H.K., Olayanju, A., Goldring, C.E., Park, B.K., The Nrf2 cell defence pathway: Keap1-dependent and -independent mechanisms of regulation. Biochem. Pharmacol. 85 (2013), 705–717.
130. Huang, Y., Li, W., Su, Z.Y., Kong, A.N., The complexity of the Nrf2 pathway: beyond the antioxidant response. J. Nutr. Biochem. 26 (2015), 1401–1413.
131. Theodore, M., Kawai, Y., Yang, J., Kleshchenko, Y., Reddy, S.P., Villalta, F., Arinze, I.J., Multiple nuclear localization signals function in the nuclear import of the transcription factor Nrf2. J. Biol. Chem. 283 (2008), 8984–8994.
132. Li, W., Khor, T.O., Xu, C., Shen, G., Jeong, W.S., Yu, S., Kong, A.N., Activation of Nrf2-antioxidant signaling attenuates NFkappaB-inflammatory response and elicits apoptosis. Biochem. Pharmacol. 76 (2008), 1485–1489.
133. Salazar, M., Rojo, A.I., Velasco, D., de Sagarra, R.M., Cuadrado, A., Glycogen synthase kinase-3beta inhibits the xenobiotic and antioxidant cell response by direct phosphorylation and nuclear exclusion of the transcription factor Nrf2. J. Biol. Chem. 281 (2006), 14841–14851.
134. Rada, P., Rojo, A.I., Chowdhry, S., McMahon, M., Hayes, J.D., Cuadrado, A., SCF/{beta}-TrCP promotes glycogen synthase kinase 3-dependent degradation of the Nrf2 transcription factor in a Keap1-independent manner. Mol. Cell Biol. 31 (2011), 1121–1133.
135. Pickering, A.M., Linder, R.A., Zhang, H., Forman, H.J., Davies, K.J., Nrf2-dependent induction of proteasome and Pa28alphabeta regulator are required for adaptation to oxidative stress. J. Biol. Chem. 287 (2012), 10021–10031.
136. 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.
137. Kapeta, S., Chondrogianni, N., Gonos, E.S., Nuclear erythroid factor 2-mediated proteasome activation delays senescence in human fibroblasts. J. Biol. Chem. 285 (2010), 8171–8184.
138. Jang, J., Wang, Y., Kim, H.S., Lalli, M.A., Kosik, K.S., Nrf2, a regulator of the proteasome, controls self-renewal and pluripotency in human embryonic stem cells. Stem Cells 32 (2014), 2616–2625.
139. Wardyn, J.D., Ponsford, A.H., Sanderson, C.M., Dissecting molecular cross-talk between Nrf2 and NF-kappaB response pathways. Biochem. Soc. Trans. 43 (2015), 621–626.
140. Israel, A., The IKK complex, a central regulator of NF-kappaB activation. Cold Spring Harb. Perspect. Biol., 2, 2010, a000158.
141. Sen, R., Baltimore, D., Inducibility of kappa immunoglobulin enhancer-binding protein Nf-kappa B by a posttranslational mechanism. Cell 47 (1986), 921–928.
142. Mauro, C., Leow, S.C., Anso, E., Rocha, S., Thotakura, A.K., Tornatore, L., Moretti, M., De Smaele, E., Beg, A.A., Tergaonkar, V., Chandel, N.S., Franzoso, G., NF-kappaB controls energy homeostasis and metabolic adaptation by upregulating mitochondrial respiration. Nat. Cell Biol. 13 (2011), 1272–1279.
143. Manea, A., Manea, S.A., Gafencu, A.V., Raicu, M., Regulation of NADPH oxidase subunit p22(phox) by NF-kB in human aortic smooth muscle cells. Arch. Physiol. Biochem. 113 (2007), 163–172.
144. Rom, O., Reznick, A.Z., The role of E3 ubiquitin-ligases MuRF-1 and MAFbx in loss of skeletal muscle mass. Free Radic. Biol. Med. 98 (2016), 218–230.
145. Liu, G.H., Qu, J., Shen, X., NF-kappaB/p65 antagonizes Nrf2-ARE pathway by depriving CBP from Nrf2 and facilitating recruitment of HDAC3 to MafK. Biochim. Biophys. Acta 1783 (2008), 713–727.
146. Ben-Neriah, Y., Karin, M., Inflammation meets cancer, with NF-kappaB as the matchmaker. Nat. Immunol. 12 (2011), 715–723.
147. Kim, J.E., You, D.J., Lee, C., Ahn, C., Seong, J.Y., Hwang, J.I., Suppression of NF-kappaB signaling by KEAP1 regulation of IKKbeta activity through autophagic degradation and inhibition of phosphorylation. Cell. Signal. 22 (2010), 1645–1654.
148. Schultz, M.A., Abdel-Mageed, A.B., Mondal, D., The nrf1 and nrf2 balance in oxidative stress regulation and androgen signaling in prostate cancer cells. Cancers 2 (2010), 1354–1378.
149. 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.
150. Radhakrishnan, S.K., den Besten, W., Deshaies, R.J., p97-dependent retrotranslocation and proteolytic processing govern formation of active Nrf1 upon proteasome inhibition. Elife, 3, 2014, e01856.
151. Vangala, J.R., Sotzny, F., Kruger, E., Deshaies, R.J., Radhakrishnan, S.K., Nrf1 can be processed and activated in a proteasome-independent manner. Curr. Biol. 26 (2016), R834–835.
152. Hetz, C., The unfolded protein response: controlling cell fate decisions under ER stress and beyond. Nat. Rev. Mol. Cell Biol. 13 (2012), 89–102.
153. 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.
154. Steffen, J., Seeger, M., Koch, A., Kruger, E., Proteasomal degradation is transcriptionally controlled by TCF11 via an ERAD-dependent feedback loop. Mol. Cell 40 (2010), 147–158.
155. Ullrich, O., Reinheckel, T., Sitte, N., Hass, R., Grune, T., Davies, K.J., Poly-ADP ribose polymerase activates nuclear proteasome to degrade oxidatively damaged histones. Proc. Natl. Acad. Sci. USA 96 (1999), 6223–6228.
156. Merker, K., Sitte, N., Grune, T., Hydrogen peroxide-mediated protein oxidation in young and old human MRC-5 fibroblasts. Arch. Biochem. Biophys. 375 (2000), 50–54.
157. Merker, K., Ullrich, O., Schmidt, H., Sitte, N., Grune, T., Stability of the nuclear protein turnover during cellular senescence of human fibroblasts. FASEB J. 17 (2003), 1963–1965.
158. Bakondi, E., Catalgol, B., Bak, I., Jung, T., Bozaykut, P., Bayramicli, M., Ozer, N.K., Grune, T., Age-related loss of stress-induced nuclear proteasome activation is due to low PARP-1 activity. Free Radic. Biol. Med. 50 (2011), 86–92.
159. Catalgol, B., Wendt, B., Grimm, S., Breusing, N., Ozer, N.K., Grune, T., Chromatin repair after oxidative stress: role of PARP-mediated proteasome activation. Free Radic. Biol. Med. 48 (2010), 673–680.
160. Hohn, A., Sittig, A., Jung, T., Grimm, S., Grune, T., Lipofuscin is formed independently of macroautophagy and lysosomal activity in stress-induced prematurely senescent human fibroblasts. Free Radic. Biol. Med. 53 (2012), 1760–1769.
161. Hohn, A., Jung, T., Grimm, S., Catalgol, B., Weber, D., Grune, T., Lipofuscin inhibits the proteasome by binding to surface motifs. Free Radic. Biol. Med. 50 (2011), 585–591.
162. Yin, D., Biochemical basis of lipofuscin, ceroid, and age pigment-like fluorophores. Free Radic. Biol. Med. 21 (1996), 871–888.
163. Baraibar, M.A., Friguet, B., Changes of the proteasomal system during the aging process. Prog. Mol. Biol. Transl. Sci. 109 (2012), 249–275.
164. Schmidt, M., Finley, D., Regulation of proteasome activity in health and disease. Biochim. Biophys. Acta 1843 (2014), 13–25.
165. Ferrington, D.A., Kapphahn, R.J., Catalytic site-specific inhibition of the 20S proteasome by 4-hydroxynonenal. FEBS Lett. 578 (2004), 217–223.
166. Demasi, M., Netto, L.E., Silva, G.M., Hand, A., de Oliveira, C.L., Bicev, R.N., Gozzo, F., Barros, M.H., Leme, J.M., Ohara, E., Redox regulation of the proteasome via S-glutathionylation. Redox Biol. 2 (2013), 44–51.
167. Bulteau, A.L., Szweda, L.I., Friguet, B., Age-dependent declines in proteasome activity in the heart. Arch. Biochem. Biophys. 397 (2002), 298–304.
168. Konig, J., Ott, C., Hugo, M., Jung, T., Bulteau, A.L., Grune, T., Hohn, A., Mitochondrial contribution to lipofuscin formation. Redox Biol. 11 (2017), 673–681.
169. Hohn, A., Grune, T., Lipofuscin: formation, effects and role of macroautophagy. Redox Biol. 1 (2013), 140–144.
170. Ott, C., Konig, J., Hohn, A., Jung, T., Grune, T., Macroautophagy is impaired in old murine brain tissue as well as in senescent human fibroblasts. Redox Biol. 10 (2016), 266–273.
171. Husom, A.D., Peters, E.A., Kolling, E.A., Fugere, N.A., Thompson, L.V., Ferrington, D.A., Altered proteasome function and subunit composition in aged muscle. Arch. Biochem. Biophys. 421 (2004), 67–76.
172. Altun, M., Besche, H.C., Overkleeft, H.S., Piccirillo, R., Edelmann, M.J., Kessler, B.M., Goldberg, A.L., Ulfhake, B., Muscle wasting in aged, sarcopenic rats is associated with enhanced activity of the ubiquitin proteasome pathway. J. Biol. Chem. 285 (2010), 39597–39608.
173. Hayashi, T., Goto, S., Age-related changes in the 20S and 26S proteasome activities in the liver of male F344 rats. Mech. Ageing Dev. 102 (1998), 55–66.
174. Sitte, N., Merker, K., Von Zglinicki, T., Davies, K.J., Grune, T., Protein oxidation and degradation during cellular senescence of human BJ fibroblasts: Part II–aging of nondividing cells. FASEB J.: Off. Publ. Fed. Am. Soc. Exp. Biol. 14 (2000), 2503–2510.
175. Sitte, N., Merker, K., Von Zglinicki, T., Grune, T., Davies, K.J., Protein oxidation and degradation during cellular senescence of human BJ fibroblasts: Part I–effects of proliferative senescence. FASEB J.: Off. Publ. Fed. Am. Soc. Exp. Biol. 14 (2000), 2495–2502.
176. Chondrogianni, N., Stratford, F.L., Trougakos, I.P., Friguet, B., Rivett, A.J., Gonos, E.S., Central role of the proteasome in senescence and survival of human fibroblasts: induction of a senescence-like phenotype upon its inhibition and resistance to stress upon its activation. J. Biol. Chem. 278 (2003), 28026–28037.
177. Kapphahn, R.J., Bigelow, E.J., Ferrington, D.A., Age-dependent inhibition of proteasome chymotrypsin-like activity in the retina. Exp. Eye Res. 84 (2007), 646–654.
178. Jung, T., Hohn, A., Catalgol, B., Grune, T., Age-related differences in oxidative protein-damage in young and senescent fibroblasts. Arch. Biochem. Biophys. 483 (2009), 127–135.
179. Carroll, B., Hewitt, G., Korolchuk, V.I., Autophagy and ageing: implications for age-related neurodegenerative diseases. Essays Biochem. 55 (2013), 119–131.
180. Zhang, C., Cuervo, A.M., Restoration of chaperone-mediated autophagy in aging liver improves cellular maintenance and hepatic function. Nat. Med. 14 (2008), 959–965.
181. Kiffin, R., Kaushik, S., Zeng, M., Bandyopadhyay, U., Zhang, C., Massey, A.C., Martinez-Vicente, M., Cuervo, A.M., Altered dynamics of the lysosomal receptor for chaperone-mediated autophagy with age. J. Cell Sci. 120 (2007), 782–791.
182. Ott, C., Konig, J., Hohn, A., Jung, T., Grune, T., Reduced autophagy leads to an impaired ferritin turnover in senescent fibroblasts. Free Radic. Biol. Med. 101 (2016), 325–333.
183. Kaushik, S., Massey, A.C., Mizushima, N., Cuervo, A.M., Constitutive activation of chaperone-mediated autophagy in cells with impaired macroautophagy. Mol. Biol. Cell 19 (2008), 2179–2192.
184. Korolchuk, V.I., Menzies, F.M., Rubinsztein, D.C., Mechanisms of cross-talk between the ubiquitin-proteasome and autophagy-lysosome systems. FEBS Lett. 584 (2010), 1393–1398.
185. Chondrogianni, N., Georgila, K., Kourtis, N., Tavernarakis, N., Gonos, E.S., 20S proteasome activation promotes life span extension and resistance to proteotoxicity in Caenorhabditis elegans. FASEB J.: Off. Publ. Fed. Am. Soc. Exp. Biol. 29 (2015), 611–622.
186. Chondrogianni, N., Tzavelas, C., Pemberton, A.J., Nezis, I.P., Rivett, A.J., Gonos, E.S., Overexpression of proteasome beta5 assembled subunit increases the amount of proteasome and confers ameliorated response to oxidative stress and higher survival rates. J. Biol. Chem. 280 (2005), 11840–11850.
187. Yun, C., Stanhill, A., Yang, Y., Zhang, Y., Haynes, C.M., Xu, C.F., Neubert, T.A., Mor, A., Philips, M.R., Ron, D., Proteasomal adaptation to environmental stress links resistance to proteotoxicity with longevity in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 105 (2008), 7094–7099.
188. Vilchez, D., Morantte, I., Liu, Z., Douglas, P.M., Merkwirth, C., Rodrigues, A.P., Manning, G., Dillin, A., RPN-6 determines C. elegans longevity under proteotoxic stress conditions. Nature 489 (2012), 263–268.
189. Tonoki, A., Kuranaga, E., Tomioka, T., Hamazaki, J., Murata, S., Tanaka, K., Miura, M., Genetic evidence linking age-dependent attenuation of the 26S proteasome with the aging process. Mol. Cell Biol. 29 (2009), 1095–1106.
190. Chondrogianni, N., Petropoulos, I., Franceschi, C., Friguet, B., Gonos, E.S., Fibroblast cultures from healthy centenarians have an active proteasome. Exp. Gerontol. 35 (2000), 721–728.
191. Katsiki, M., Chondrogianni, N., Chinou, I., Rivett, A.J., Gonos, E.S., The olive constituent oleuropein exhibits proteasome stimulatory properties in vitro and confers life span extension of human embryonic fibroblasts. Rejuvenation Res. 10 (2007), 157–172.
192. Papaevgeniou, N., Sakellari, M., Jha, S., Tavernarakis, N., Holmberg, C.I., Gonos, E.S., Chondrogianni, N., 18alpha-glycyrrhetinic acid proteasome activator decelerates aging and alzheimer's disease progression in caenorhabditis elegans and neuronal cultures. Antioxid. Redox Signal. 25 (2016), 855–869.
193. Madeo, F., Zimmermann, A., Maiuri, M.C., Kroemer, G., Essential role for autophagy in life span extension. J. Clin. Investig. 125 (2015), 85–93.
194. Eisenberg, T., Knauer, H., Schauer, A., Buttner, S., Ruckenstuhl, C., Carmona-Gutierrez, D., Ring, J., Schroeder, S., Magnes, C., Antonacci, L., Fussi, H., Deszcz, L., Hartl, R., Schraml, E., Criollo, A., Megalou, E., Weiskopf, D., Laun, P., Heeren, G., Breitenbach, M., Grubeck-Loebenstein, B., Herker, E., Fahrenkrog, B., Frohlich, K.U., Sinner, F., Tavernarakis, N., Minois, N., Kroemer, G., Madeo, F., Induction of autophagy by spermidine promotes longevity. Nat. Cell Biol. 11 (2009), 1305–1314.
195. Seah, N.E., de Magalhaes Filho, C.D., Petrashen, A.P., Henderson, H.R., Laguer, J., Gonzalez, J., Dillin, A., Hansen, M., Lapierre, L.R., Autophagy-mediated longevity is modulated by lipoprotein biogenesis. Autophagy 12 (2016), 261–272.
196. Lapierre, L.R., Kumsta, C., Sandri, M., Ballabio, A., Hansen, M., Transcriptional and epigenetic regulation of autophagy in aging. Autophagy 11 (2015), 867–880.
197. Unno, M., Mizushima, T., Morimoto, Y., Tomisugi, Y., Tanaka, K., Yasuoka, N., Tsukihara, T., The structure of the mammalian 20S proteasome at 2.75 A resolution. Structure 10 (2002), 609–618.
198. Kastle, M., Reeg, S., Rogowska-Wrzesinska, A., Grune, T., Chaperones, but not oxidized proteins, are ubiquitinated after oxidative stress. Free Radic. Biol. Med. 53 (2012), 1468–1477.
199. Kastle, M., Grune, T., Proteins bearing oxidation-induced carbonyl groups are not preferentially ubiquitinated. Biochimie 93 (2011), 1076–1079.