Activation of chaperone-mediated autophagy during oxidative stress

Molecular Biology of the Cell

Volumn 15, Issue 11, 2004, Pages 4829-4840

  Kiffin, Roberta ^a   Christian, Christopher ^a   Knecht, Erwin ^b   Cuervo, Ana Maria ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b CENTRO DE INVESTIGACIÓN PRÍNCIPE FELIPE   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

LYSOSOMAL MEMBRANE PROTEIN 2A; MEMBRANE PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTOPHAGY; IMMUNOCYTOCHEMISTRY; LIVER LYSOSOME; MALE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PROTEIN INTERACTION; RAT; SIGNAL TRANSDUCTION;

ANIMALS; AUTOPHAGY; CYTOSOL; FIBROBLASTS; IMMUNOHISTOCHEMISTRY; LIVER; LYSOSOMES; MALE; MICE; MICROSCOPY, FLUORESCENCE; MOLECULAR CHAPERONES; OXIDATIVE STRESS; OXYGEN; RATS; RATS, WISTAR; RIBONUCLEASE, PANCREATIC; RNA, MESSENGER; TIME FACTORS; TRANSCRIPTION, GENETIC; UP-REGULATION;

ANIMALIA;

EID: 6344275803     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E04-06-0477     Document Type: Article

References (79)

1. Agarraberes, F.A., and Dice, J.F. (2001). A molecular chaperone complex at the Iysosomal membrane is required for protein translocation. J. Cell Sci. 114, 2491-2499.
2. Agarraberes, F., Terlecky, S.R., and Dice, J.F. (1997). An intralysosomal hsp70 is required for a selective pathway of lysosomal protein degradation. J. Cell Biol. 137, 825-834.
3. Aniento, F., Roche, E., Cuervo, A.M., and Knecht, E. (1993). Uptake and degradation of glyceraldehyde-3-phosphate dehydrogenase by rat liver lysosomes. J. Biol. Chem. 268, 10463-10470.
4. Brunk, U.T., Zhang, H., Dalen, H., and Ollinger, K. (1995). Exposure of cells to nonlethal concentrations of hydrogen peroxide induces degeneration-repair mechanisms involving lysosomal destabilization. Free Radic. Biol. Med. 19, 813-822.
5. Carr, A.C. (2001). Hypochlorous acid-modified low-density lipoprotein inactivates the lysosomal protease cathepsin B: protection by ascorbic and lipoic acids. Redox Rep. 6, 343-349.
6. Carrard, G., Bulteau, A.L., Petropoulos, I., and Friguet, B. (2002). Impairment of proteasome structure and function in aging. Int. J. Biochem. Cell Biol. 34, 1461-1474.
7. Chiang, H.L., and Dice, J.F. (1988). Peptide sequences that target proteins for enhanced degradation during serum withdrawal. J. Biol. Chem. 262, 6797-6805.
8. Chiang, H.L., Terlecky, S.R., Plant, C.P., and Dice, J.F. (1989). A role for a 70-kilodalton heat shock protein in lysosomal degradation of intracellular proteins. Science 246, 382-385.
9. Crabb, J.W., O'Neil, J., Miyagi, M., West, K., and Hoff, H.F. (2002). Hydroxynonenal inactivates cathepsin B by forming Michael adducts with active site residues. Protein Sci. 11, 831-840.
10. Cuervo, A.M. (2004a). Autophagy: in sickness and in health. Trends Cell Biol. 14, 70-77.
11. Cuervo, A.M. (2004b). Autophagy: many paths to the same end. Mol. Cell. Biochem. 263, 55-72
12. Cuervo, A.M., and Dice, J.F. (1996). A receptor for the selective uptake and degradation of proteins by lysosomes. Science 273, 501-503.
13. Cuervo, A.M., and Dice, J.F. (1998a). How do intracellular proteolytic systems change with age? Front. Biosci. 3, 25-43.
14. Cuervo, A.M., and Dice, J.F. (1998b). Lysosomes, a meeting point of proteins, chaperones, and proteases. J. Mol. Med. 76, 6-12.
15. Cuervo, A.M., and Dice, J.F. (2000a). Age-related decline in chaperone-mediated autophagy. J. Biol. Chem. 275, 31505-31513.
16. Cuervo, A.M., and Dice, J.F. (2000b). Regulation of lamp2a levels in the lysosomal membrane. Traffic 1, 570-583.
17. Cuervo, A.M., and Dice, J.F. (2000c). Unique properties of lamp2a compared to other lamp2 isoforms. J. Cell Sci. 113, 4441-4450.
18. Cuervo, A.M., Dice, J.F., and Knecht, E. (1997). A population of rat liver lysosomes responsible for the selective uptake and degradation of cytosolic proteins. J. Biol. Chem. 272, 5606-5615.
19. Cuervo, A.M., Hildebrand, H., Bombard, E.M., and Dice, J.F. (1999). Direct lysosomal uptake of alpha2-microglobulin contributes to chemically induced nephropathy. Kidney Int. 55, 529-545.
20. Cuervo, A.M., Hu, W., Lim, B., and Dice, J.F. (1998). IkB is a substrate for a selective pathway of lysosomal proteolysis. Mol. Biol. Cell 9, 1995-2010.
21. Cuervo, A.M., Knecht, E., Terlecky, S.R., and Dice, J.F. (1995). Activation of a selective pathway of lysosomal proteolysis in rat liver by prolonged starvation. Am. J. Physiol. 269, C1200-C1208.
22. Cuervo, A. M., Mann, L., Bonten, E., d'Azzo, A., and Dice, J. (2003). Cathepsin A regulates chaperone-mediated autophagy through cleavage of the lysosomal receptor. EMBO J. 22, 12-19.
23. Cuervo, A.M., Terlecky, S.R., Dice, J.F., and Knecht, E. (1994). Selective binding and uptake of ribonuclease A and glyceraldehyde-3-phosphate dehydrogenase by rat liver lysosomes. J. Biol. Chem. 269, 26374-26380.
24. Davies, K.J. (2001). Degradation of oxidized proteins by the 20S proteasome. Biochimie 83, 301-310.
25. Demasi, M., and Davies, K.J. (2003). Proteasome inhibitors induce intracellular protein aggregation and cell death by an oxygen-dependent mechanism. FEBS Lett. 542, 89-94.
26. Dice, J., Finn, P., Majeski, A., Mesieres, N., and Cuervo, A. (2003). Chaperone-mediated autophagy. In: Autophagy, ed. D.J. Klionsky, Georgetown, TX: Landes Bioscience, 158-177.
27. Dice, J.F. (2000). Lysosomal Pathways of Protein Degradation, Austin, TX: Landes Bioscience.
28. Ding, Q., Dimayuga, E., Martin, S., Bruce-Keller, A.J., Nukala, V., Cuervo, A.M., and Keller, J.N. (2003). Characterization of chronic low-level proteasome inhibition on neural homeostasis. J. Neurochem. 86, 489-497.
29. Donati, A., Cavallini, G., Paradiso, C., Vittorini, S., Pollera, M., Gori, Z., and Bergamini, E. (2001). Age-related changes in the autophagic proteolysis of rat isolated liver cells: effects of antiaging dietary restrictions. J. Gerontol. 56, B375-B383.
30. Dunlop, R.A., Rodgers, K.J., and Dean, R.T. (2002). Recent developments in the intracellular degradation of oxidized proteins. Free Radic. Biol. Med. 33, 894-906.
31. Franch, H.A., Sooparb, S., Du, J., and Brown, N.S. (2001). A mechanism regulating proteolysis of specific proteins during renal tubular cell growth. J. Biol. Chem. 276, 19126-19131.
32. Friguet, B. (2002). Protein repair and degradation during aging. Sci. World J. 2, 248-254.
33. Friguet, B., Bulteau, A.L., Chondrogianni, N., Conconi, M., and Petropoulos, I. (2000). Protein degradation by the proteasome and its implications in aging. Ann. N.Y. Acad. Sci. 908, 143-154.
34. Fuertes, G., Martin de Llano, J., Villarroya, A., Rivett, A.J., and Knecht, E. (2003). 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, 75-86.
35. Gomes-Marcondes, M., and Tisdale, M. (2002). Induction of protein catabolism and the ubiquitin-proteasome pathway by mild oxidative stress. Cancer Lett. 180, 69-74.
36. Gracy, R., Talent, J., and Zvaigzne, A. (1998). Molecular wear and tear leads to terminal marking and the unstable isoforms of aging. J. Exp. Zool. 282, 18-27.
37. Grune, T. (2000). Oxidative stress, aging and the proteasomal system. Biogerontology 1, 31-40.
38. Grune, T., and Davies, K.J. (1997). Breakdown of oxidized proteins as a part of secondary antioxidant defenses in mammalian cells. Biofactors 6, 165-172.
39. Grune, T., Klotz, L.O., Gieche, J., Rudeck, M., and Sies, H. (2001). Protein oxidation and proteolysis by the nonradical oxidants singlet oxygen or peroxynitrite. Free Radic. Biol. Med. 30, 1243-1253.
40. Grune, T., Reinheckel, T., and Davies, K.J. (1997). Degradation of oxidized proteins in mammalian cells. FASEB J. 11, 526-534.
41. Grune, T., Reinheckel, T., Joshi, M., and Davies, K.J. (1995). Proteolysis in cultured liver epithelial cells during oxidative stress. Role of the multicatalytic proteinase complex, proteasome. J. Biol. Chem. 270, 2344-2351.
42. Grune, T., Reinheckel, T., Li, R., North, J.A., and Davies, K.J. (2002a). Proteasome-dependent turnover of protein disulfide isomerase in oxidatively stressed cells. Arch. Biochem. Biophys. 397, 407-413.
43. Grune, T., Stolzing, A., Jakstadt, M., McLaren, J.S., Speakman, J.R., and Szweda, P.A. (2002b). Proteolysis, free radicals, and aging. Free Radic. Biol. Med. 33, 259-265.
44. Haly, T. (1979). Review of the toxicity of paraquat. Clin. Toxicol. 14, 1-46.
45. Hoff, H.F., Zyromski, N., Armstrong, D., and O'Neil, J. (1993). Aggregation as well as chemical modification of LDL during oxidation is responsible for poor processing in macrophages. J Lipid Res. 34, 1919-1929.
46. Hosler, M.R., Wang-Su, S.T., and Wagner, B.J. (2003). Targeted disruption of specific steps of the ubiquitin-proteasome pathway by oxidation in lens epithelial cells. Int. J Biochem. Cell Biol. 35, 685-697.
47. Imai, J., Yashiroda, H., Maruya, M., Yahara, I., and Tanaka, K. (2003). Proteasomes and molecular chaperones: cellular machinery responsible for folding and destruction of unfolded proteins. Cell Cycle 2, 585-590.
48. Jentoft, N., and Dearborn, D. (1983). Protein labeling by reductive alkylation. Methods Enzymol. 91, 570-579.
49. Keller, J.N., Gee, J., and Ding, Q. (2002). The proteasome in brain aging. Age Res Rev. 3, 279-293.
50. Laemmli, U. (1970). Cleavage of structural proteins during the assembly of the head of the bacteriophage T4. Nature 227, 680-685.
51. Lemasters, J.J., Qian, T., He, L., Kim, J.S., Elmore, S.P., Cascio, W.E., and Brenner, D.A. (2002). Role of mitochondrial inner membrane permeabilization in necrotic cell death, apoptosis, and autophagy. Antioxid. Redox Signal. 4, 769-781.
52. Lenk, S.E., Susan, P.P., Hickson, I., Jasionowski, T., and Dunn, W.A., Jr. (1999). Ubiquitinated aldolase B accumulates during starvation-induced lysosomal proteolysis. J. Cell Physiol. 178, 17-27.
53. Lowry, O.H., Rosebrough, N.J., Farr, A.L., and Randall, R.J. (1951). Protein measurement with the Polin phenol reagent. J. Biol. Chem. 193, 265-275.
54. Martin, A., Joseph, J.A., and Cuervo, A.M. (2002). Stimulatory effect of vitamin C on autophagy in glial cells. J. Neurochem. 82, 538-549.
55. Massey, A., Kiffin, R., and Cuervo, A.M. (2004). Pathophysiology of chaperone-mediated autophagy. Int. J. Biochem. Cell Biol. 36, 2420-2434.
56. Mehlhase, J., and Grune, T. (2002). Proteolytic response to oxidative stress in mammalian cells. Biol. Chem. 383, 559-567.
57. Merker, K., and Grune, T. (2000). Proteolysis of oxidised proteins and cellular senescence. Exp. Gerontol. 35, 779-786.
58. Merker, K., Stolzing, A., and Grune, T. (2001). Proteolysis, caloric restriction and aging. Mech. Ageing Dev. 122, 595-615.
59. Ohsumi, Y., Ishikawa, T., and Kato, K. (1983). A rapid and simplified method for the preparation of lysosomal membranes from rat liver. J. Biochem. 93, 547-556.
60. Ollinger, K., and Brunk, U.T. (1995). Cellular injury induced by oxidative stress is mediated through lysosomal damage. Free Radic. Biol. Med. 19, 565-574.
61. O'Neil, J., Hoppe, G., Sayre, L.M., and Hoff, H.F. (1997). Inactivation of cathepsin B by oxidized LDL involves complex formation induced by binding of putative reactive sites exposed at low pH to thiols on the enzyme. Free Radic. Biol. Med. 23, 215-225.
62. Reggiori, F., and Klionsky, D.J. (2002). Autophagy in the eukaryotic cell. Eukaryot. Cell 1, 11-21.
63. Rivett, A., and Levine, R. (1990). Metal-catalyzed oxidation of Escherichia coli glutamine synthetase: correlation of structural and functional changes. Arch. Biochem. Biophys. 278, 26-34.
64. Rivett, A.J. (1985). Preferential degradation of the oxidatively modified form of glutamine synthetase by intracellular mammalian proteases. J. Biol. Chem. 260, 300-305.
65. Salvador, N., Aguado, C., Horst, M., and Knecht, E. (2000). Import of a cytosolic protein into lysosomes by chaperone-mediated autophagy depends on its folding state. J. Biol. Chem. 275, 27447-27456.
66. Shringarpure, R., Grune, T., Mehlhase, J., and Davies, KJ. (2003). Ubiquitin conjugation is not required for the degradation of oxidized proteins by proteasome. J. Biol. Chem. 278, 311-318.
67. Sitte, N., Merker, K., Von Zglinicki, T., Davies, K.J., and Grune, T. (2000a). Protein oxidation and degradation during cellular senescence of human BJ fibroblasts: part II-aging of nondividing cells. FASEB J. 14, 2503-2510.
68. Sitte, N., Merker, K., Von Zglinicki, T., Grune, T., and Davies, K.J. (2000b). Protein oxidation and degradation during cellular senescence of human BJ fibroblasts: part I-effects of proliferative senescence. FASEB J. 14, 2495-2502.
69. Stadtman, E.R. (2001). Protein oxidation in aging and age-related diseases. Ann. N.Y. Acad. Sci. 928, 22-38.
70. Storrie, B., and Madden, E. (1990). Isolation of subcellular organelles. Methods Enzymol. 182, 203-225.
71. Szweda, P.A., Friguet, B., and Szweda, L.I. (2002). Proteolysis, free radicals, and aging. Free Radic. Biol. Med. 33, 29-36.
72. Terlecky, S., and Dice, J.F. (1993). Polypeptide import and degradation by isolated lysosomes. J. Biol. Chem. 268, 23490-23495.
73. Terman, A. (1995). The effect of age on formation and elimination of autophagic vacuoles in mouse hepatocytes. Gerontology 41 (suppl 2), 319-326.
74. Towbin, H., Staehelin, T., and Gordon, J. (1979). Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedures and some applications. Proc. Natl. Acad. Sci. USA 76, 4350-4353.
75. Vittorini, S., Paradiso, C., Donati, A., Cavallini, G., Masini, M., Gori, Z., Pollera, M., and Bergamini, E. (1999). The age-related accumulation of protein carbonyl in rat liver correlates with the age-related decline in liver proteolytic activities. J. Gerontol. A Biol. Sci. Med. Sci. 54, B318-B323.
76. Wang, C.W., and Klionsky, D.J. (2003). The molecular mechanism of autophagy. Mol. Med. 9, 65-76.
77. Ward, W.F. (2002). Protein degradation in the aging organism. Prog. Mol. Subcell. Biol. 29, 35-42.
78. Wattiaux, R., Wattiaux-De Coninck, S., Ronveaux-Dupal, M.F., and Dubois, F. (1978). Isolation of rat liver lysosomes by isopycnic centrifugation in a metrizamide gradient. J. Cell Biol. 78, 349-368.
79. Wing, S.S., Chiang, H.L., Goldberg, A.L., and Dice, J.F. (1991). Proteins containing peptide sequences related to KFERQ are selectively depleted in liver and heart, but not skeletal muscle, of fasted rats. Biochem. J. 275, 165-169.