Chaperone-mediated autophagy: Roles in disease and aging

Cell Research

Volumn 24, Issue 1, 2014, Pages 92-104

  Cuervo, Ana Maria ^a   Wong, Esther ^b  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; LAMP2 PROTEIN, HUMAN; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 2; MICRORNA;

AGING; AUTOPHAGY; DEGENERATIVE DISEASE; ENZYMOLOGY; GENETICS; HUMAN; LYSOSOME; METABOLISM; NEOPLASM; PATHOLOGY; PHYSIOLOGY; REVIEW;

AGING; AUTOPHAGY; HUMANS; LYSOSOMAL-ASSOCIATED MEMBRANE PROTEIN 2; LYSOSOMES; MICRORNAS; MOLECULAR CHAPERONES; NEOPLASMS; NEURODEGENERATIVE DISEASES;

EID: 84891741302     PISSN: 10010602     EISSN: 17487838     Source Type: Journal    
DOI: 10.1038/cr.2013.153     Document Type: Review

References (86)

1. van Oosten-Hawle P, Porter RS, Morimoto RI. Regulation of organismal proteostasis by transcellular chaperone signaling. Cell 2013; 153:1366-1378.
2. Roth DM, Balch WE. Modeling general proteostasis: proteome balance in health and disease. Curr Opin Cell Biol 2011; 23:126-134.
3. Mizushima N, Levine B, Cuervo AM, Klionsky DJ. Autophagy fights disease through cellular self-digestion. Nature 2008; 451:1069-1075.
4. Kaushik S, Cuervo AM. Chaperone-mediated autophagy: a unique way to enter the lysosome world. Trends Cell Biol 2012; 22:407-417.
5. Dice JF. Peptide sequences that target cytosolic proteins for lysosomal proteolysis. Trends Biochem Sci 1990; 15:305-309.
6. Dice JF, Walker CD, Byrne B, Cardiel A. General characteristics of protein degradation in diabetes and starvation. Proc Natl Acad Sci USA 1978; 75:2093-2097.
7. Auteri JS, Okada A, Bochaki V, Dice JF. Regulation of intracellular protein degradation in IMR-90 human diploid fibroblasts. J Cell Physiol 1983; 115:159-166.
8. Agarraberes FA, Dice JF. A molecular chaperone complex at the lysosomal membrane is required for protein translocation. J Cell Sci 2001; 114:2491-2499.
9. Backer JM, Bourret L, Dice JF. Regulation of catabolism of microinjected ribonuclease A requires the amino-terminal 20 amino acids. Proc Natl Acad Sci USA 1983; 80:2166-2170.
10. Backer J, Dice J. Covalent linkage of ribonuclease S-peptide to microinjected proteins causes their intracellular degradation to be enhanced by serum withdrawal. Proc Natl Acad Sci USA 1986; 83:5830-5834.
11. Chiang HI, Dice JF. Peptide sequences that target proteins for enhanced degradation during serum withdrawal. J Biol Chem 1988; 263:6797-6803.
12. Chiang H, Terlecky S, Plant C, Dice JF. A role for a 70-kilodalton heat shock protein in lysosomal degradation of intracellular proteins. Science 1989; 246:382-385.
13. Cuervo AM, Terlecky SR, Dice JF, Knecht E. Selective binding and uptake of ribonuclease A and glyceraldehyde-3-phosphate dehydrogenase by isolated rat liver lysosomes. J Biol Chem 1994; 269:26374-26380.
14. Terlecky SR, Chiang H-L, Olson TS, Dice JF. Protein and peptide binding and stimulation of in vitro lysosomal proteolysis by the 73-kDa heat shock cognate protein. J Biol Chem 1992; 267:9202-9209.
15. Cuervo AM, Knecht E, Terlecky SR, Dice JF. Activation of a selective pathway of lysosomal proteolysis in rat liver by prolonged starvation. Am J Physiol 1995; 269:C1200-C1208.
16. Cuervo AM, Dice JF. Age-related decline in chaperone-mediated autophagy. J Biol Chem 2000; 275:31505-31513.
17. Lv L, Li D, Zhao D, et al. Acetylation targets the M2 isoform of pyruvate kinase for degradation through chaperone-mediated autophagy and promotes tumor growth. Mol Cell 2011; 42:719-730.
18. Thompson LM, Aiken CT, Kaltenbach LS, et al. IKK phosphorylates Huntingtin and targets it for degradation by the proteasome and lysosome. J Cell Biol 2009; 187:1083-1099.
19. Cuervo AM, Dice JF. A receptor for the selective uptake and degradation of proteins by lysosomes. Science 1996; 273:501-503.
20. Bandyopadhyay U, Kaushik S, Varticovski L, Cuervo AM. The chaperone-mediated autophagy receptor organizes in dynamic protein complexes at the lysosomal membrane. Mol Cell Biol 2008; 28:5747-5763.
21. Salvador N, Aguado C, Horst M, Knecht E. Import of a cytosolic protein into lysosomes by chaperone-mediated autophagy depends on its folding state. J Biol Chem 2000; 275:27447-27456.
22. Bandyopadhyay U, Sridhar S, Kaushik S, Kiffin R, Cuervo AM. Identification of regulators of chaperone-mediated autophagy. Mol Cell 2010; 39:535-547.
23. Ali AB, Nin DS, Tam J, Khan M. Role of chaperone mediated autophagy (CMA) in the degradation of misfolded N-CoR protein in non-small cell lung cancer (NSCLC) cells. PLoS One 2011; 6:e25268.
24. Cuervo AM, Dice JF, 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.
25. Massey AC, Kaushik S, Sovak G, Kiffin R, Cuervo AM. Consequences of the selective blockage of chaperone-mediated autophagy. Proc Natl Acad Sci USA 2006; 103:5805-5810.
26. Kaushik S, Massey AC, Mizushima N, Cuervo AM. Constitutive activation of chaperone-mediated autophagy in cells with impaired macroautophagy. Mol Biol Cell 2008; 19:2179-2192.
27. Kaushik S, Massey AC, Cuervo AM. Lysosome membrane lipid microdomains: novel regulators of chaperone-mediated autophagy. EMBO J 2006; 25:3921-3933.
28. Kiffin R, Christian C, Knecht E, Cuervo AM. Activation of chaperone-mediated autophagy during oxidative stress. Mol Biol Cell 2004; 15:4829-4840.
29. Cuervo AM, Dice JF. Unique properties of lamp2a compared to other lamp2 isoforms. J Cell Sci 2000; 113 Pt 24:4441-4450.
30. Cuervo AM, Dice JF. Regulation of lamp2a levels in the lysosomal membrane. Traffic 2000; 1:570-583.
31. Anguiano J, Garner TP, Mahalingam M, Das BC, Gavathiotis E, Cuervo AM. Chemical modulation of chaperone-mediated autophagy by retinoic acid derivatives. Nat Chem Biol 2013; 9:374-382.
32. Sahu R, Kaushik S, Cannizzo E, et al. Microautophagy of cytosolic proteins by late endosomes. Develop Cell 2011; 20:131-139.
33. Kaushik S, Cuervo AM. Methods to monitor chaperone-mediated autophagy. Meth Enzymol 2009; 452:297-324.
34. Cuervo AM, Hu W, Lim B, Dice JF. IkappaB is a substrate for a selective pathway of lysosomal proteolysis. Mol Biol Cell 1998; 9:1995-2010.
35. Kon M, Kiffin R, Koga H, et al. Chaperone-mediated autophagy is required for tumor growth. Sci Transl Med 2011; 3:109ra117.
36. Cuervo AM, Palmer A, Rivett AJ, Knecht E. Degradation of proteasomes by lysosomes in rat liver. Eur J Biochem 1995; 227:792-800.
37. Metrailler S, Schorderet DF, Cottet S. Early apoptosis of rod photoreceptors in Rpe65(-/-) mice is associated with the upregulated expression of lysosomal-mediated autophagic genes. Exp Eye Res 2012; 96:70-81.
38. Dohi E, Tanaka S, Seki T, et al. Hypoxic stress activates chaperone-mediated autophagy and modulates neuronal cell survival. Neurochem Int 2012; 60:431-442.
39. Ferreira JV, Fofo H, Bejarano E, et al. STUB1/CHIP is required for HIF1A degradation by chaperone-mediated autophagy. Autophagy 2013; 9:1349-1366.
40. Franch HA, Sooparb S, Du J, Brown NS. A mechanism regulating proteolysis of specific proteins during renal tubular cell growth. J Biol Chem 2001; 276:19126-19131.
41. Sooparb S, Price SR, Shaoguang J, Franch HA. Suppression of chaperone-mediated autophagy in the renal cortex during acute diabetes mellitus. Kidney Int 2004; 65:2135-2144.
42. Yang Q, She H, Gearing M, et al. Regulation of neuronal survival factor MEF2D by chaperone-mediated autophagy. Science 2009; 323:124-127.
43. Zhou D, Li P, Lin Y, et al. Lamp-2a facilitates MHC class II presentation of cytoplasmic antigens. Immunity 2005; 22:571-581.
44. Finn PF, Mesires NT, Vine M, Dice JF. Effects of small molecules on chaperone-mediated autophagy. Autophagy 2005; 1:141-145.
45. Arias E, Cuervo AM. Chaperone-mediated autophagy in protein quality control. Curr Opin Cell Biol 2011; 23:184-189.
46. Koga H, Cuervo AM. Chaperone-mediated autophagy dysfunction in the pathogenesis of neurodegeneration. Neurobiol Dis 2011; 43:29-37.
47. Orenstein SJ, Cuervo AM. Chaperone-mediated autophagy: molecular mechanisms and physiological relevance. Semin Cell Dev Biol 2010; 21:719-726.
48. Morimoto RI, Driessen AJ, Hegde RS, Langer T. The life of proteins: the good, the mostly good and the ugly. Nat Struct Mol Biol 2011; 18:1-4.
49. Wong E, Cuervo AM. Neuronal autophagy gone awry: many fixings for the autophagic wrong-doing. Nat Neurosci 2010; 13:805-811.
50. Cuervo AM, Stefanis L, Fredenburg R, Lansbury PT, Sulzer D. Impaired degradation of mutant alpha-synuclein by chaperonemediated autophagy. Science 2004; 305:1292-1295.
51. Martinez-Vicente M, Talloczy Z, Kaushik S, et al. Dopaminemodified alpha-synuclein blocks chaperone-mediated autophagy. J Clin Invest 2008; 118:777-788.
52. Orenstein SJ, Kuo SH, Tasset I, et al. Interplay of LRRK2 with chaperone-mediated autophagy. Nat Neurosci 2013; 16:394-406.
53. Wang Y, Martinez-Vicente M, Kruger U, et al. Tau fragmentation, aggregation and clearance: the dual role of lysosomal processing. Hum Mol Genet 2009; 18:4153-4170.
54. Mak SK, McCormack AL, Manning-Bog AB, Cuervo AM, Di Monte DA. Lysosomal degradation of alpha-synuclein in vivo. J Biol Chem 2010; 285:13621-13629.
55. Vogiatzi T, Xilouri M, Vekrellis K, Stefanis L. Wild type alpha-synuclein is degraded by chaperone-mediated autophagy and macroautophagy in neuronal cells. J Biol Chem 2008; 283:23542-23556.
56. Kabuta T, Furuta A, Aoki S, Furuta K, Wada K. Aberrant interaction between Parkinsons disease-associated mutant UCH-L1 and the lysosomal receptor for chaperone-mediated autophagy. J Biol Chem 2008; 283:23731-23738.
57. Oueslati A, Fournier M, Lashuel HA. Role of post-translational modifications in modulating the structure, function and toxicity of alpha-synuclein: implications for Parkinsons disease pathogenesis and therapies. Prog Brain Res 2010; 183:115-145.
58. Alvarez-Erviti L, Rodriguez-Oroz MC, Cooper JM, et al. Chaperone-mediated autophagy markers in Parkinson disease brains. Arch Neurol 2010; 67:1464-1472.
59. Malkus KA, Ischiropoulos H. Regional deficiencies in chaperone- mediated autophagy underlie alpha-synuclein aggregation and neurodegeneration. Neurobiol Dis 2012; 46:732-744.
60. Alvarez-Erviti L, Seow Y, Schapira AH, Rodriguez-Oroz MC, Obeso JA, Cooper JM. Influence of microRNA deregulation on chaperone-mediated autophagy and alpha-synuclein pathology in Parkinsons disease. Cell Death Dis 2013; 4:e545.
61. Pang S, Chen D, Zhang A, Qin X, Yan B. Genetic analysis of the LAMP-2 gene promoter in patients with sporadic Parkinsons disease. Neurosci Lett 2012; 526:63-67.
62. Xilouri M, Brekk OR, Landeck N, et al. Boosting chaperonemediated autophagy in vivo mitigates alpha-synuclein-induced neurodegeneration. Brain 2013; 136:2130-2146.
63. Liu H, Wang P, Song W, Sun X. Degradation of regulator of calcineurin 1 (RCAN1) is mediated by both chaperone-mediated autophagy and ubiquitin proteasome pathways. FASEB J 2009; 23:3383-3392.
64. Saha T. LAMP2A overexpression in breast tumors promotes cancer cell survival via chaperone-mediated autophagy. Autophagy 2012; 8:1643-1656.
65. Vakifahmetoglu-Norberg H, Kim M, Xia HG, et al. Chaperone- mediated autophagy degrades mutant p53. Genes Dev 2013; 27:1718-1730.
66. Welsch T, Younsi A, Disanza A, et al. Eps8 is recruited to lysosomes and subjected to chaperone-mediated autophagy in cancer cells. Exp Cell Res 2010; 316:1914-1924.
67. Kiffin R, Kaushik S, Zeng M, et al. Altered dynamics of the lysosomal receptor for chaperone-mediated autophagy with age. J Cell Sci 2007; 120:782-791.
68. Rodriguez-Navarro JA, Kaushik S, Koga H, et al. Inhibitory effect of dietary lipids on chaperone-mediated autophagy. Proc Natl Acad Sci USA 2012; 109:E705-E714.
69. Massey AC, Kaushik S, Sovak G, Kiffin R, Cuervo AM. Consequences of the selective blockage of chaperone-mediated autophagy. Proc Natl Acad Sci USA 2006; 103:5905-5910.
70. Zhang C, Cuervo AM. Restoration of chaperone-mediated autophagy in aging liver improves cellular maintenance and hepatic function. Nat Med 2008; 14:959-965.
71. Wong E, Cuervo AM. Integration of clearance mechanisms: the proteasome and autophagy. Cold Spring Harb Perspect Biol 2010; 2:a006734.
72. Park C, Cuervo AM. Selective autophagy: talking with the UPS. Cell Biochem Biophys 2013; 67:3-13.
73. Kaushik S, Massey A, Mizushima N, Cuervo AM. Constitutive activation of chaperone-mediated autophagy in cells with impaired macroautophagy. Mol Biol Cell 2008; 19:2179-2192.
74. Koga H, Martinez-Vicente M, Macian F, Verkhusha VV, Cuervo AM. A photoconvertible fluorescent reporter to track chaperone-mediated autophagy. Nat Commun 2011; 2:386.
75. Massey AC, Follenzi A, Kiffin R, Zhang C, Cuervo AM. Early cellular changes after blockage of chaperone-mediated autophagy. Autophagy 2008; 4:442-456.
76. Cuervo AM, Palmer A, Rivett AJ, Knecht E. Degradation of proteasomes by lysosomes in rat liver. Eur J Biochem 1995; 227:792-800.
77. Koga H, Martinez-Vicente M, Arias E, Kaushik S, Sulzer D, Cuervo AM. Constitutive upregulation of chaperonemediated autophagy in Huntingtons disease. J Neurosci 2011; 31:18492-18505.
78. Ravikumar B, Duden R, Rubinsztein D. Aggregate-prone proteins with polyglutamine and polyalanine expansions are degraded by autophagy. Hum Mol Genet 2002; 11:1107-1117.
79. Martinez-Vicente M, Talloczy Z, Wong E, et al. Cargo recognition failure is responsible for inefficient autophagy in Huntingtons Disease. Nat Neurosci 2010; 13:567-576.
80. Hipp MS, Patel CN, Bersuker K, et al. Indirect inhibition of 26S proteasome activity in a cellular model of Huntingtons disease. J Cell Biol 2012; 196:573-587.
81. Wong ES, Tan JM, Soong WE, et al. Autophagy-mediated clearance of aggresomes is not a universal phenomenon. Hum Mol Genet 2008; 17:2570-2582.
82. Wong E, Bejarano E, Rakshit M, et al. Molecular determinants of selective clearance of protein inclusions by autophagy. Nat Commun 2012; 3:1240.
83. Webb JL, Ravikumar B, Atkins J, Skepper JN, Rubinsztein DC. Alpha-Synuclein is degraded by both autophagy and the proteasome. J Biol Chem 2003; 278:25009-25013.
84. Tan JM, Wong ES, Kirkpatrick DS, et al. Lysine 63-linked ubiquitination promotes the formation and autophagic clearance of protein inclusions associated with neurodegenerative diseases. Hum Mol Genet 2008; 17:431-439.
85. Bauer PO, Goswami A, Wong HK, et al. Harnessing chaperone- mediated autophagy for the selective degradation of mutant huntingtin protein. Nat Biotechnol 2010; 28:256-263.
86. Rodriguez-Muela N, Koga H, Garcia-Ledo L, et al. Balance between autophagic pathways preserves retinal homeostasis. Aging cell 2013; 12:478-488.