Interplay of LRRK2 with chaperone-mediated autophagy

Nature Neuroscience

Volumn 16, Issue 4, 2013, Pages 394-406

  Orenstein, Samantha J ^a   Kuo, Sheng Han ^b   Tasset, Inmaculada ^a   Arias, Esperanza ^a   Koga, Hiroshi ^a   Fernandez Carasa, Irene ^c   Cortes, Etty ^b,d   Honig, Lawrence S ^b,d   Dauer, William ^e   Consiglio, Antonella ^c,f   Raya, Angel ^g,h,i   Sulzer, David ^b,d   Cuervo, Ana Maria ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b H Houston Merritt Center   (United States)

^c UNIVERSITY OF BARCELONA   (Spain)

^d Columbia University Medical School ^*  (United States)

^e UNIVERSITY OF MICHIGAN   (United States)

^f UNIVERSITY OF BRESCIA   (Italy)

^g INSTITUTE FOR BIOENGINEERING OF CATALONIA IBEC   (Spain)

^h INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

ⁱ BIOMATERIALES Y NANOMEDICINA CIBER BBN   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

LEUCINE RICH REPEAT KINASE 2; MUTANT PROTEIN;

ARTICLE; CHAPERONE-MEDIATED AUTOPHAGY; DOPAMINERGIC NERVE CELL; GENE MUTATION; LYSOSOME; NERVE CELL CULTURE; PARKINSON DISEASE; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN DEGRADATION; WILD TYPE;

AGED, 80 AND OVER; ANIMALS; ANIMALS, NEWBORN; AUTOPHAGY; BRAIN CHEMISTRY; CELLS, CULTURED; FEMALE; HEK293 CELLS; HUMANS; MALE; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; MIDDLE AGED; MOLECULAR CHAPERONES; MUTATION; PROTEIN BINDING; PROTEIN-SERINE-THREONINE KINASES; RATS; RATS, WISTAR;

EID: 84875640261     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.3350     Document Type: Article

References (54)

1. Spillantini, M.G. et al. Alpha-synuclein in Lewy bodies. Nature 388, 839-840 (1997).
2. West, A.B. et al. Parkinson's disease-associated mutations in leucine-rich repeat kinase 2 augment kinase activity. Proc. Natl. Acad. Sci. USA 102, 16842-16847 (2005). (Pubitemid 41688864)
3. Balch, W.E., Morimoto, R.I., Dillin, A. & Kelly, J.W. Adapting proteostasis for disease intervention. Science 319, 916-919 (2008). (Pubitemid 351263754)
4. Anglade, P. et al. Apoptosis and autophagy in nigral neurons of patients with Parkinson's disease. Histol. Histopathol. 12, 25-31 (1997). (Pubitemid 27106916)
5. Zhu, J.H., Guo, F., Shelburne, J., Watkins, S. & Chu, C.T. Localization of phosphorylated ERK/MAP kinases to mitochondria and autophagosomes in Lewy body diseases. Brain Pathol. 13, 473-481 (2003). (Pubitemid 37420692)
6. Stefanis, L., Larsen, K., Rideout, H., Sulzer, D. & Greene, L. Expression of A53T mutant but not wild-type alpha-synuclein in PC12 cells induces alterations of the ubiquitin-dependent degradation system, loss of dopamine release, and autophagic cell death. J. Neurosci. 21, 9549-9560 (2001). (Pubitemid 34184043)
7. Martinez-Vicente, M. et al. Dopamine-modified alpha-synuclein blocks chaperone-mediated autophagy. J. Clin. Invest. 118, 777-788 (2008).
8. Cuervo, A.M., Stefanis, L., Fredenburg, R., Lansbury, P.T. & Sulzer, D. Impaired degradation of mutant alpha-synuclein by chaperone-mediated autophagy. Science 305, 1292-1295 (2004). (Pubitemid 39129234)
9. Mizushima, N., Levine, B., Cuervo, A. & Klionsky, D. Autophagy fights disease through cellular self-digestion. Nature 451, 1069-1075 (2008). (Pubitemid 351317450)
10. Gómez-Suaga, P. et al. Leucine-rich repeat kinase 2 regulates autophagy through a calcium-dependent pathway involving NAADP. Hum. Mol. Genet. 21, 511-525 (2012).
11. Biskup, S. et al. Localization of LRRK2 to membranous and vesicular structures in mammalian brain. Ann. Neurol. 60, 557-569 (2006). (Pubitemid 44871798)
12. Alegre-Abarrategui, J. et al. LRRK2 regulates autophagic activity and localizes to specific membrane microdomains in a novel human genomic reporter cellular model. Hum. Mol. Genet. 18, 4022-4034 (2009).
13. Ramonet, D. et al. Dopaminergic neuronal loss, reduced neurite complexity and autophagic abnormalities in transgenic mice expressing G2019S mutant LRRK2. PLoS ONE 6, e18568 (2011).
14. Plowey, E.D., Cherra, S.J. III, Liu, Y.J. & Chu, C.T. Role of autophagy in G2019S-LRRK2-associated neurite shortening in differentiated SH-SY5Y cells. J. Neurochem. 105, 1048-1056 (2008). (Pubitemid 351565713)
15. Tong, Y. et al. Loss of leucine-rich repeat kinase 2 causes impairment of protein degradation pathways, accumulation of alpha-synuclein, and apoptotic cell death in aged mice. Proc. Natl. Acad. Sci. USA 107, 9879-9884 (2010).
16. Orenstein, S.J. & Cuervo, A.M. Chaperone-mediated autophagy: molecular mechanisms and physiological relevance. Semin. Cell Dev. Biol. 21, 719-726 (2010).
17. Cuervo, A.M. Chaperone-mediated autophagy: selectivity pays off. Trends Endocrinol. Metab. 21, 142-150 (2010).
18. Chiang, H.L. & Dice, J.F. Peptide sequences that target proteins for enhanced degradation during serum withdrawal. J. Biol. Chem. 263, 6797-6805 (1988).
19. Chiang, H.L., Terlecky, S.R., Plant, C.P. & Dice, J.F. A role for a 70-kilodalton heat shock protein in lysosomal degradation of intracellular proteins. Science 246, 382-385 (1989).
20. Cuervo, A.M. & Dice, J. A receptor for the selective uptake and degradation of proteins by lysosomes. Science 273, 501-503 (1996). (Pubitemid 26286451)
21. Bandyopadhyay, U., Kaushik, S., Vartikovsky, L. & Cuervo, A.M. Dynamic organization of the receptor for chaperone-mediated autophagy at the lysosomal membrane. Mol. Cell Biol. 28, 5747-5763 (2008).
22. Cuervo, A.M., Mann, L., Bonten, E., d'Azzo, A. & Dice, J. Cathepsin A regulates chaperone-mediated autophagy through cleavage of the lysosomal receptor. EMBO J. 22, 47-59 (2003). (Pubitemid 36091268)
23. Kaushik, S., Massey, A.C. & Cuervo, A.M. Lysosome membrane lipid microdomains: novel regulators of chaperone-mediated autophagy. EMBO J. 25, 3921-3933 (2006). (Pubitemid 44338735)
24. 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. 283, 23542-23556 (2008).
25. Kabuta, T., Furuta, A., Aoki, S., Furuta, K. & Wada, K. Aberrant interaction between Parkinson disease-associated mutant UCH-L1 and the lysosomal receptor for chaperone-mediated autophagy. J. Biol. Chem. 283, 23731-23738 (2008).
26. Alvarez-Erviti, L. et al. Chaperone-mediated autophagy markers in Parkinson disease brains. Arch. Neurol. 67, 1464-1472 (2010).
27. Ko, H.S. et al. CHIP regulates leucine-rich repeat kinase-2 ubiquitination, degradation, and toxicity. Proc. Natl. Acad. Sci. USA 106, 2897-2902 (2009).
28. Dice, J.F. Peptide sequences that target cytosolic proteins for lysosomal proteolysis. Trends Biochem. Sci. 15, 305-309 (1990). (Pubitemid 20223216)
29. Kaushik, S. & Cuervo, A.M. Methods to monitor chaperone-mediated autophagy. Methods Enzymol. 452, 297-324 (2009).
30. Cuervo, A.M., Terlecky, S.R., Dice, J.F. & Knecht, E. Selective binding and uptake of ribonuclease A and glyceraldehyde-3-phosphate dehydrogenase by isolated rat liver lysosomes. J. Biol. Chem. 269, 26374-26380 (1994).
31. Kett, L.R. et al. LRRK2 Parkinson disease mutations enhance its microtubule association. Hum. Mol. Genet. 21, 890-899 (2012).
32. Tanida, I., Minematsu-Ikeguchi, N., Ueno, T. & Kominami, E. Lysosomal turnover, but not a cellular level, of endogenous LC3 is a marker for autophagy. Autophagy 1, 84-91 (2005).
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. 2, 386 (2011).
34. Dodson, M.W., Zhang, T., Jiang, C., Chen, S. & Guo, M. Roles of the Drosophila LRRK2 homolog in Rab7-dependent lysosomal positioning. Hum. Mol. Genet. 21, 1350-1363 (2012).
35. Mak, S.K., McCormack, A.L., Manning-Bog, A.B., Cuervo, A.M. & Di Monte, D.A. Lysosomal degradation of alpha-synuclein in vivo. J. Biol. Chem. 285, 13621-13629 (2010).
36. Zhang, C. & Cuervo, A.M. Restoration of chaperone-mediated autophagy in aging liver improves cellular maintenance and hepatic function. Nat. Med. 14, 959-965 (2008).
37. 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. USA 103, 5805-5810 (2006).
38. Blake, R.A. et al. SU6656, a selective src family kinase inhibitor, used to probe growth factor signaling. Mol. Cell Biol. 20, 9018-9027 (2000). (Pubitemid 32245931)
39. Wang, Y. et al. Tau fragmentation, aggregation and clearance: the dual role of lysosomal processing. Hum. Mol. Genet. 18, 4153-4170 (2009).
40. Greggio, E. et al. The Parkinson disease-associated leucine-rich repeat kinase 2 (LRRK2) is a dimer that undergoes intramolecular autophosphorylation. J. Biol. Chem. 283, 16906-16914 (2008).
41. Greggio, E. et al. Kinase activity is required for the toxic effects of mutant LRRK2/dardarin. Neurobiol. Dis. 23, 329-341 (2006). (Pubitemid 44097032)
42. Sulzer, D. & Surmeier, D.J. Neuronal vulnerability, pathogenesis, and Parkinson's disease. Mov. Disord. doi:10.1002/mds.25095 (12 July 2012).
43. Sen, S., Webber, P.J. & West, A.B. Dependence of leucine-rich repeat kinase 2 (LRRK2) kinase activity on dimerization. J. Biol. Chem. 284, 36346-36356 (2009).
44. Sánchez-Dánes, A. et al. Disease-specific phenotypes in dopamine neurons from human iPS-based models of genetic and sporadic Parkinson's disease. EMBO Mol. Med. 4, 380-395 (2012).
45. Kon, M. et al. Chaperone-mediated autophagy is required for tumor growth. Sci. Transl. Med. 3, 109ra117 (2011).
46. Berger, Z., Smith, K.A. & Lavoie, M.J. Membrane localization of LRRK2 is associated with increased formation of the highly active LRRK2 dimer and changes in its phosphorylation. Biochemistry 49, 5511-5523 (2010).
47. Cuervo, A.M. & Dice, J.F. Regulation of lamp2a levels in the lysosomal membrane. Traffic 1, 570-583 (2000).
48. Li, Y. et al. Mutant LRRK2(R1441G) BAC transgenic mice recapitulate cardinal features of Parkinson's disease. Nat. Neurosci. 12, 826-828 (2009).
49. Staal, R.G.W., Rayport, S. & Sulzer, D. Amperometric detection of dopamine exocytosis from synaptic terminals. in Electrochemical Methods for Neuroscience (eds. Michael, A.C. & Borland, L.M.) Ch. 16 (CRC, Boca Raton, Florida, USA, 2007).
50. Poulopoulos, M. et al. Clinical and pathological characteristics of LRRK2 G2019S patients with PD. J. Mol. Neurosci. 47, 139-143 (2012).
51. Storrie, B. & Madden, E. Isolation of subcellular organelles. Methods Enzymol. 182, 203-225 (1990). (Pubitemid 20154389)
52. Rubinsztein, D.C. et al. In search of an "autophagomometer". Autophagy 5, 585-589 (2009).
53. Lowry, C.C., Kraeft, N.H. & Hughes, F.A. Jr. Blastomycosis of the lung. Am. J. Surg. 81, 676-679 (1951).
54. Towbin, H., Staehelin, T. & Gordon, J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA 76, 4350-4354 (1979). (Pubitemid 9256559)