Chaperone-mediated autophagy in the kidney: The road more traveled

Seminars in Nephrology

Volumn 34, Issue 1, 2014, Pages 72-83

  Franch, Harold A ^a,b  

^a ATLANTA VA MEDICAL CENTER   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cancer; Diabetes; Hypertrophy; Starvation

Indexed keywords

CARRIER PROTEIN; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 2; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 2A; UNCLASSIFIED DRUG;

AGING; AMINO ACID SEQUENCE; CHAPERONE-MEDIATED AUTOPHAGY; DEGENERATIVE DISEASE; DIABETES MELLITUS; HUMAN; KIDNEY DISEASE; KIDNEY HYPERTROPHY; KIDNEY PROXIMAL TUBULE; LYSOSOME MEMBRANE; MACROAUTOPHAGY; MALIGNANT NEOPLASTIC DISEASE; METABOLIC REGULATION; MOLECULAR RECOGNITION; NONHUMAN; OXIDATION; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN DEGRADATION; PROTEIN METABOLISM; REVIEW; SIGNAL TRANSDUCTION; STARVATION;

CANCER; DIABETES; HYPERTROPHY; STARVATION;

AGING; ANIMALS; AUTOPHAGY; DIABETES MELLITUS; HUMANS; KIDNEY; KIDNEY TUBULES; LYSOSOMAL-ASSOCIATED MEMBRANE PROTEIN 2; MOLECULAR CHAPERONES; NEOPLASMS; OXIDATIVE STRESS;

EID: 84893399524     PISSN: 02709295     EISSN: 15584488     Source Type: Journal    
DOI: 10.1016/j.semnephrol.2013.11.010     Document Type: Review

References (100)

1. Klionsky D.J., Baehrecke E.H., Brumell J.H., Chu C.T., Codogno P., Cuervo A.M., et al. A comprehensive glossary of autophagy-related molecules and processes (2nd edition). Autophagy 2011, 7:1273-1294.
2. Kaushik S., Cuervo A.M. Chaperone-mediated autophagy: a unique way to enter the lysosome world. Trends Cell Biol 2012, 22:407-417.
3. Wing S.S., Chiang H.L., Goldberg A.L., Dice J.F. Proteins containing peptide sequences related to Lys-Phe-Glu-Arg-Gln are selectively depleted in liver and heart, but not skeletal-muscle, of fasted rats. Biochem J 1991, 275:165-169.
4. Huber T.B., Edelstein C.L., Hartleben B., Inoki K., Jiang M., Koya D., et al. Emerging role of autophagy in kidney function, diseases and aging. Autophagy 2012, 8:1009-1031.
5. Franch H.A. Pathways of proteolysis affecting renal cell growth. Curr Opin Nephrol Hypertens 2002, 11:445-450.
6. Sridhar S., Botbol Y., Macian F., Cuervo A.M. Autophagy and disease: always two sides to a problem. J Pathol 2012, 226:255-273.
7. Dice J.F., Finn P.F. Proteolytic and lipolytic responses to starvation. Nutrition 2006, 22:830-844.
8. Cuervo A.M. Chaperone-mediated autophagy: Dice's 'wild' idea about lysosomal selectivity. Nat Rev Mol Cell Biol 2011, 12:535-541.
9. Dice J.F., Terlecky S.R. Targeting of cytosolic proteins to lysosomes for degradation. Crit Rev Ther Drug Carrier Sys 1990, 7:211-233.
10. Olson T.S., Terlecky S.R., Dice J.F. Targeting specific proteins for lysosomal proteolysis. Biomed Biochim Acta 1991, 50:393-397.
11. Dice J.F. Selective degradation of cytosolic proteins by lysosomes. Ann N Y Acad Sci 1992, 674:58-64.
12. Isenman L.D., Dice J.F. Secretion of intact proteins and peptide-fragments by lysosomal pathways of protein-degradation. J Biol Chem 1989, 264:21591-21596.
13. Hayes S.A., Dice J.F. Roles of molecular chaperones in protein degradation. J Cell Biol 1996, 132:255-258.
14. Kaushik S., Bandyopadhyay U., Sridhar S., Kiffin R., Martinez-Vicente M., Kon M., et al. Chaperone-mediated autophagy at a glance. J Cell Sci 2011, 124:495-499.
15. Cuervo A.M., Dice J.F., Knecht E. A population of rat liver lysosomes responsible for the selective uptake and degradation of cytosolic proteins. J Biol Chem 1997, 272:5606-5615.
16. Agarraberes F.A., Terlecky S.R., Dice J.F. An intralysosomal hsp70 is required for a selective pathway of lysosomal protein degradation. J Cell Biol 1997, 137:825-834.
17. Cuervo A.M., Dice J.F. Lysosomes, a meeting point of proteins, chaperones, and proteases. J Mol Med 1998, 76:6-12.
18. Agarraberes F.A., Dice J.F. A molecular chaperone complex at the lysosomal membrane is required for protein translocation. JCell Sci 2001, 114:2491-2499.
19. Cuervo A.M., Dice J.F. A receptor for the selective uptake and degradation of proteins by the lysosome. Science 1996, 273:501-503.
20. Cuervo A.M., Dice J.F. Unique properties of lamp2a compared to other lamp2 isoforms. J Cell Sci 2000, 113:4441-4450.
21. Massey A.C., Kaushik S., Sovak G., Kiffin R., Cuervo A.M. Consequences of the selective blockage of chaperone-mediated autophagy. Proc Natl Acad Sci U S A 2006, 103:5805-5810.
22. Cuervo A.M., Dice J.F. Regulation of lamp2a levels in the lysosomal membrane. Trafficking 2000, 1:572-580.
23. Fukuda M. Lysosomal membrane glycoproteins. Structure, biosynthesis, and intracellular trafficking. J Biol Chem 1991, 266:21327-21330.
24. Eskelinen Eeva L., Illert A.L., Tanaka Y., Schwarzmann G., Blanz J., von Figura K., et al. Role of LAMP-2 in lysosome biogenesis and autophagy. Mol Biol Cell 2002, 13:3355-3368.
25. Orenstein S.J., Cuervo A.M. Chaperone-mediated autophagy: molecular mechanisms and physiological relevance. Semin Cell Dev Biol 2010, 21:719-726.
26. Bandyopadhyay U., Sridhar S., Kaushik S., Kiffin R., Cuervo A.M. Identification of regulators of chaperone-mediated autophagy. Mol Cell 2010, 39:535-547.
27. Park C., Cuervo A.M. Selective autophagy: talking with the UPS. Cell Biochem Biophys 2013, 6:3-13.
28. Franch H.A., Sooparb S., Du J. A mechanism regulating proteolysis of specific proteins during renal tubular cell hypertrophy. J Biol Chem 2001, 276:19126-19131.
29. Sooparb S., Price S.R., Shaoguang J., Franch H.A. Suppression of chaperone-mediated autophagy in the renal cortex during acute diabetes mellitus. Kidney Int 2004, 65:2135-2144.
30. Cuervo A.M., Mann L., Bonten E.J., d'Azzo A., Dice J.F. Cathepsin A regulates chaperone-mediated autophagy through cleavage of the lysosomal receptor. EMBO J. 2003, 22:47-59.
31. Kaushik S., Massey A.C., Cuervo A.M. Lysosome membrane lipid microdomains: novel regulators of chaperone-mediated autophagy. EMBO J. 2006, 25:3921-3933.
32. Kaushik S., Cuervo A.M. Methods to monitor chaperone-mediated autophagy. Methods Enzymol 2009, 452:297-324.
33. Koga H., Martinez-Vicente M., Macian F., Verkhusha V.V., Cuervo A.M. A photoconvertible fluorescent reporter to track chaperone-mediated autophagy. Nat Commun 2011, 2:386.
34. Shen W., Brown N.S., Finn P.F., Dice J.F., Franch H.A. Akt and mammalian target of rapamycin regulate separate systems of proteolysis in renal tubular cells. J Am Soc Nephrol 2006, 17:2414-2423.
35. May R.C., Logue B., Edwards B., Patel S. An in vitro method for the determination of protein turnover in incubated proximal tubule segments. Kidney Int 1993, 43:1156-1159.
36. Dice J.F. Chaperone-mediated autophagy. Autophagy 2007, 3:295-299.
37. De Duve C., De Barsy T., Poole B., Trouet A., Tulkens P., Van Hoof F. Commentary: lysosomotropic agents. Biochem Pharmacol 1974, 23:2495-2531.
38. Poole B., Ohkuma S. Effect of weak bases on the intralysosomal pH in mouse peritoneal macrophages. J Cell Biol 1981, 90:665-669.
39. +-ATPase, inhibits acidification and protein degradation in lysosomes of cultured cells. J Biol Chem 1991, 266:17707-17712.
40. Franch H.A., Preisig P.A. NH4 Cl-induced hypertrophy is mediated by weak base effects and is independent of cell cycle processes. Am J Physiol (Cell Physiol) 1996, 270:C932-8.
41. Rabkin R., Palathumpat M., Tsao T. Ammonium chloride alters renal tubular cell growth and protein turnover. Lab Invest 1993, 68:427-438.
42. Nath K.A., Hostetter M.K., Hostetter T.H. Pathophysiology of chronic tubulo-interstitial disease in rats. Interactions of dietary acid load, ammonia, and complement component C3. J Clin Invest 1985, 76:667-675.
43. Preisig P.A., Franch H.A. Renal epithelial cell hyperplasia and hypertrophy. Semin Nephrol 1995, 15:327-340.
44. Finn P.F., Dice J.F. Ketone bodies stimulate chaperone-mediated autophagy. J Biol Chem 2005, 280:25864-25870.
45. Finn P.E., Mesires N.T., Vine M., Dice J.F. Effects of small molecules on chaperone-mediated autophagy. Autophagy 2005, 1:141-145.
46. Dice J.F., Terlecky S.R. Selective degredation of cytosolic proteins by lysosomes. Cellular proteolytic systems 1994, 55-64. Wiley-Liss, New York. A.J. Ciechanover, A.L. Schwartz (Eds.).
47. Dice J.F., Cuervo A.M. Age-related decline in chaperone-mediated autophagy. J Biol Chem 2000, 275:31505-31513.
48. Franch H.A., Wang X., Sooparb S., Brown N.S., Du J. Phoshatidylinositol 3-kinase activity is required for epidermal growth factor to suppress proteolysis. J Am Soc Nephrol 2002, 13:903-908.
49. Franch H.A., Curtis P.V., Mitch W.E. Mechanisms of renal tubular cell hypertrophy: mitogen-induced suppression of proteolysis. Am J Physiol (Cell Physiol) 1997, 273:C843-C851.
50. Shechter P., Boner G., Rabkin R. Tubular cell protein degredation in early diabetic renal hypertrophy. J Am Soc Nephrol 1994, 4:1582-1587.
51. Moghal N., Sternberg P.W. Multiple positive and negative regulators of signalling by the EGF receptor. Curr Opin Cell Biol 1999, 11:190-196.
52. Schrier R.W., Harris D.C.H., Chan L., Shapiro J.I., Caramelo C. Tubular hypermetabolism as a factor in the progression of chronic renal failure. Am J Kidney Dis 1988, 12:243-249.
53. Nakae J., Kitamura T., Silver D.L., Accili D. The forkhead transcription factor Foxo1 (Fkhr) confers insulin sensitivity onto glucose-6-phosphatase expression. J Clin Invest 2001, 108:1359-1367.
54. Brunet A., Bonni A., Zigmond M.J., Lin M.Z., Juo P. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 1999, 96:857.
55. Brazil D.P., Yang Z.Z., Hemmings B.A. Advances in protein kinase B signalling: AKTion on multiple fronts. Trends Biochem Sci 2004, 29:233-242.
56. Zhao J., Brault J.J., Schild A., Cao P., Sandri M. FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells. Cell Metab 2007, 6:472.
57. Vidal R.L., Figueroa A., Court F.A., Thielen P., Molina C., Wirth C., et al. Targeting the UPR transcription factor XBP1 protects against Huntington's disease through the regulation of FoxO1 and autophagy. Hum Mol Genet 2012, 21:2245-2262.
58. Singh R., Cuervo A.M. Autophagy in the cellular energetic balance. Cell Metab 2011, 13:495-504.
59. Kon M., Kiffin R., Koga H., Chapochnick J., Macian F., Varticovski L., et al. Chaperone-mediated autophagy is required for tumor growth. Sci Transl Med 2011, 3:109-117.
60. Rodriguez-Navarro J.A., Cuervo A.M. Autophagy and lipids: tightening the knot. Semin Immunopathol 2010, 32:343-353.
61. Rodriguez-Navarro J.A., Kaushik S., Koga H., Dall'Armi C., Shui G., Wenk M.R., et al. Inhibitory effect of dietary lipids on chaperone-mediated autophagy. Proc Natl Acad Sci U S A 2012, 109:E705-E714.
62. Choudhury D., Tuncel M., Levi M. Disorders of lipid metabolism and chronic kidney disease in the elderly. Semin Nephrol 2009, 29:610-620.
63. Massey A.C., Kaushik S., Cuervo A.M. Lysosomal chat maintains the balance. Autophagy 2006, 2:325-327.
64. Koga H., Cuervo A.M. Chaperone-mediated autophagy dysfunction in the pathogenesis of neurodegeneration. Neurobiol Dis 2011, 43:29-37.
65. Levine B., Kroemer G. Autophagy in the pathogenesis of disease. Cell 2008, 132:27-42.
66. Kiffin R., Christian C., Knecht E., Cuervo A.M. Activation of chaperone-mediated autophagy during oxidative stress. Mol Biol Cell 2004, 15:4829-4840.
67. Kaushik S., Cuervo A.M. Autophagy as a cell-repair mechanism: activation of chaperone-mediated autophagy during oxidative stress. Mol Aspects Med 2006, 27:444-454.
68. Kon M., Cuervo A.M. Chaperone-mediated autophagy in health and disease. FEBS Lett 2010, 584:1399-1404.
69. Anguiano J., Garner T.P., Mahalingam M., Das B.C., Gavathiotis E., Cuervo A.M. Chemical modulation of chaperone-mediated autophagy by retinoic acid derivatives. Nat Chem Biol 2013, 9:374-382.
70. Duong V., Rochette-Egly C. The molecular physiology of nuclear retinoic acid receptors. From health to disease. Biochim Biophys Acta 2011, 1812:1023-1031.
71. Knecht E., Cuervo A.M., Dice J.F. A lysosomal pathway for the selective degradation of cytosolic proteins in rat liver. Biom Health Rep 1997, 13:402-410.
72. Carrero J.J., Stenvinkel P., Cuppari L., Ikizler T.A., Kalantar-Zadeh K., Kaysen G., et al. Etiology of the protein-energy wasting syndrome in chronic kidney disease: a consensus statement from the International Society of Renal Nutrition and Metabolism (ISRNM). J Ren Nutr 2013, 23:77-90.
73. Fine L.G., Norman J. Cellular events in renal hypertrophy. Ann Rev Physiol 1989, 15:19-32.
74. Chen J.K., Chen J., Neilson E.G., Harris R.C. Role of mammalian target of rapamycin signaling in compensatory renal hypertrophy. J Am Soc Nephrol 2005, 16:1384-1391.
75. Lotspeich W.D. Renal hypertrophy in metabolic acidosis and its relation to ammonia excretion. Am J Physiol 1965, 208:1135-1142.
76. Seyer-Hansen K., Hansen J., Gunderson H.J.G. Renal hypertrophy in experimental diabetes. Diabetologia 1980, 18:501-505.
77. Eskelinen E.L., Prescott A.R., Cooper J., Brachmann S.M., Wang L., Tang X., et al. Inhibition of autophagy in mitotic animal cells. Traffic 2002, 3:878-893.
78. Chang Y.Y., Juhász G., Goraksha-Hicks P., Arsham A.M., Mallin D.R., Muller L.K., et al. Nutrient-dependent regulation of autophagy through the target of rapamycin pathway. Biochem Soc Trans 2009, 37:232-236.
79. Huber T.B., Walz G., Kuehn E.W. mTOR and rapamycin in the kidney: signaling and therapeutic implications beyond immunosuppression. Kidney Int 2011, 79:502-511.
80. Massey A., Kiffin R., Cuervo A.M. Pathophysiology of chaperone-mediated autophagy. Int J Biochem Cell Biol 2004, 36:2420-2434.
81. Wing S.S., Chiang H.L., Goldberg A.L., Dice J.F. Proteins containing peptide sequences related to lys-phe-glu-arg-gln are selectively depleted in liver and heart, but not skeletal muscle, of fasted rats. Biochem J 1991, 275:165-169.
82. Hubbi M.E., Hu H., Kshitiz Ahmed I, Levchenko A., Semenza G.L. Chaperone-mediated autophagy targets hypoxia-inducible factor-1α (HIF-1α) for lysosomal degradation. J Biol Chem 2013, 288:10703-10714.
83. Franch H.A. Kidney growth during catabolic illness: what it does not destroy makes it grow stronger. J Ren Nutr 2007, 17:167-172.
84. Kaushik S., Singh R., Cuervo A.M. Autophagic pathways and metabolic stress. Diabetes Obes Metab 2010, 12(Suppl 2):4-14.
85. Maxwell P.H., Wiesener M.S., Chang G.W., Clifford S.C., Vaux E.C., Cockman M.E., et al. The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 1999, 399:271-275.
86. Welsch T., Younsi A., Disanza A., Rodriguez J.A., Cuervo A.M., Scita G., et al. Eps8 is recruited to lysosomes and subjected to chaperone-mediated autophagy in cancer cells. Exp Cell Res 2010, 316:1914-1924.
87. Cuervo A.M., Dice J.F. Age-related decline in chaperone-mediated autophagy. J Biol Chem 2000, 275:31305-31313.
88. Martinez-Vicente M., Sovak G., Cuervo A.M. Protein degradation and aging. Exp Gerontol 2005, 40:622-633.
89. Franch H.A., Mitch W.E. Navigating between the Scylla and Charybdis of prescribing dietary protein for chronic kidney diseases. Annu Rev Nutr 2009, 29:341-364.
90. Cuervo A.M., Dice J.F. When lysosomes get old. Exp Gerontol 2000, 35:119-131.
91. Kiffin R., Kaushik S., Zeng M., Bandyopadhyay U., Zhang C., Massey A.C., et al. Altered dynamics of the lysosomal receptor for chaperone-mediated autophagy with age. J Cell Sci 2007, 120:782-791.
92. Cui J., Bai X.Y., Shi S.Z., Cui S.Y., Hong Q., Cai G.Y., et al. Age-related changes in the function of autophagy in rat kidneys. Age 2012, 34:329-339.
93. Zhang C., Cuervo A.M. Restoration of chaperone-mediated autophagy in aging liver improves cellular maintenance and hepatic function. Nat Med 2008, 14:959-965.
94. Read N.G. The role of lysosomes in hyaline droplet nephropathy induced by a variety of pharmacological agents in the male rat. Histochem J 1991, 23:436-443.
95. Cuervo A.M., Hildebrand H., Bomhard E.M., Dice J.F. Direct lysosomal uptake of alpha 2-microglobulin contributes to chemically induced nephropathy. Kidney Int 1999, 55:529-545.
96. Lieberman A.P., Puertollano R., Raben N., Slaugenhaupt S., Walkley S.U., Ballabio A. Autophagy in lysosomal storage disorders. Autophagy 2012, 8:719-730.
97. Venugopal B., Mesires N.T., Kennedy J.C., Curcio-Morelli C., LaPlante J.M., Dice J.F., et al. Chaperone-mediated autophagy is defective in mucolipidosis type IV. J Cell Physiol 2009, 219:344-353.
98. d'Azzo A., Andria G., Strisciuglio P., Galjaard H. Galactosialidosis. The metabolic and molecular bases of inherited disease 2001, 3811-3826. McGraw-Hill Publishing Co, New York. C. Scriver, A. Beaudet, W. Sly, D. Valle (Eds.).
99. Shimmoto M., Fukuhara Y., Itoh K., Oshima A., Sakuraba H., Suzuki Y. Protective protein gene mutations in galactosialidosis. J Clin Invest 1993, 91:2393-2398.
100. Eccles M.R., Wallis J.L., Fidler A.E., Spurr N.K., Goodfellow P.J., Reeve A.E. Expression of the PAX2 gene in fetal kidney and in Wilm's tumor. Cell Growth Differ 1992, 3:279-289.