Dysfunction of the autophagy/lysosomal degradation pathway is a shared feature of the genetic synucleinopathies

FASEB Journal

Volumn 27, Issue 9, 2013, Pages 3424-3429

  Manzoni, Claudia ^a   Lewis, Patrick A ^a,b  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF READING   (United Kingdom)

Author keywords

GBA; LRRK2; Parkinson's disease

Indexed keywords

ALPHA SYNUCLEIN; ATPASE 13A2; GLUCOSYLCERAMIDASE; LEUCINE RICH REPEAT KINASE 2; PHOSPHOTRANSFERASE; PROTEIN SERINE THREONINE KINASE; UNCLASSIFIED DRUG; VACUOLAR PROTEIN SORTING 35;

ARTICLE; ATP13A2 GENE; AUTOPHAGY; GBA GENE; GENE; HUMAN; LEWY BODY; LRRK2 GENE; LYSOSOME; NERVE DEGENERATION; NEUROPATHOLOGY; NONHUMAN; PARKINSON DISEASE; PARKINSONISM; PATHOGENESIS; POINT MUTATION; PRIORITY JOURNAL; SNCA GENE; VPS35 GENE;

GBA; LRRK2; PARKINSON'S DISEASE;

ALPHA-SYNUCLEIN; ANIMALS; AUTOPHAGY; HUMANS; LYSOSOMES; MODELS, BIOLOGICAL; NERVE DEGENERATION; PARKINSON DISEASE;

EID: 84883420073     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.12-223842     Document Type: Article

References (44)

1. Lees, A. J., Hardy, J., and Revesz, T. (2009) Parkinson's disease. Lancet 373, 2055-2066
2. Polymeropoulos, M. H., Lavedan, C., Leroy, E., Ide, S. E., Dehejia, A., Dutra, A., Pike, B., Root, H., Rubenstein, J., Boyer, R., Stenroos, E. S., Chandrasekharappa, S., Athanassiadou, A., Papapetropoulos, T., Johnson, W. G., Lazzarini, A. M., Duvoisin, R. C., Di Iorio, G., Golbe, L. I., and Nussbaum, R. L. (1997) Mutation in the alpha-synuclein gene identified in families with Parkinson's disease. Science 276, 2045-2047
3. Lashuel, H. A., Overk, C. R., Oueslati, A., and Masliah, E. (2013) The many faces of alpha-synuclein: from structure and toxicity to therapeutic target. Nat. Rev. Neurosci. 14, 38-48
4. Spillantini, M. G., Schmidt, M. L., Lee, V. M., Trojanowski, J. Q., Jakes, R., and Goedert, M. (1997) Alpha-synuclein in Lewy bodies. Nature 388, 839-840
5. Cookson, M. R. (2010) The role of leucine-rich repeat kinase 2 (LRRK2) in Parkinson's disease. Nat. Rev. Neurosci. 11, 791-797
6. Zimprich, A., Biskup, S., Leitner, P., Lichtner, P., Farrer, M., Lincoln, S., Kachergus, J., Hulihan, M., Uitti, R. J., Calne, D. B., Stoessl, A. J., Pfeiffer, R. F., Patenge, N., Carbajal, I. C., Vieregge, P., Asmus, F., Muller-Myhsok, B., Dickson, D. W., Meitinger, T., Strom, T. M., Wszolek, Z. K., and Gasser, T. (2004) Mutations in LRRK2 cause autosomal-dominant parkinsonism with pleomorphic pathology. Neuron 44, 601-607
7. Sidransky, E., and Lopez, G. (2012) The link between the GBA gene and parkinsonism. Lancet Neurol. 11, 986-998
8. Deas, E., Wood, N. W., and Plun-Favreau, H. (2011) Mitophagy and Parkinson's disease: the PINK1-parkin link. Biochim. Biophys. Acta 1813, 623-633
9. Kahle, P. J., Waak, J., and Gasser, T. (2009) DJ-1 and prevention of oxidative stress in Parkinson's disease and other age-related disorders. Free Rad. Biol. Med. 47, 1354-1361
10. Thomas, K. J., McCoy, M. K., Blackinton, J., Beilina, A., van der Brug, M., Sandebring, A., Miller, D., Maric, D., Cedazo-Minguez, A., and Cookson, M. R. (2010) DJ-1 acts in parallel to the PINK1/parkin pathway to control mitochondrial function and autophagy. Hum. Mol. Genet. 20, 40-50
11. Houlden, H., and Singleton, A. B. (2012) The genetics and neuropathology of Parkinson's disease. Acta Neuropathol. 124, 325-338
12. Doherty, K. M., Silveira-Moriyama, L., Parkkinen, L., Healy, D. G., Farrell, M., Mencacci, N. E., Ahmed, Z., Brett, F. M., Hardy, J., Quinn, N., Counihan, T. J., Lynch, T., Fox, Z. V., Revesz, T., Lees, A. J., and Holton, J. L. (2013) Parkin disease: a clinicopathologic entity? JAMA Neurol. 4, 1-9
13. Vilarino-Guell, C., Wider, C., Ross, O. A., Dachsel, J. C., Kachergus, J. M., Lincoln, S. J., Soto-Ortolaza, A. I., Cobb, S. A., Wilhoite, G. J., Bacon, J. A., Behrouz, B., Melrose, H. L., Hentati, E., Puschmann, A., Evans, D. M., Conibear, E., Wasserman, W. W., Aasly, J. O., Burkhard, P. R., Djaldetti, R., Ghika, J., Hentati, F., Krygowska-Wajs, A., Lynch, T., Melamed, E., Rajput, A., Rajput, A. H., Solida, A., Wu, R. M., Uitti, R. J., Wszolek, Z. K., Vingerhoets, F., and Farrer, M. J. (2011) VPS35 mutations in Parkinson disease. Am. J. Hum. Genet. 89, 162-167
14. Zimprich, A., Benet-Pages, A., Struhal, W., Graf, E., Eck, S. H., Offman, M. N., Haubenberger, D., Spielberger, S., Schulte, E. C., Lichtner, P., Rossle, S. C., Klopp, N., Wolf, E., Seppi, K., Pirker, W., Presslauer, S., Mollenhauer, B., Katzenschlager, R., Foki, T., Hotzy, C., Reinthaler, E., Harutyunyan, A., Kralovics, R., Peters, A., Zimprich, F., Brucke, T., Poewe, W., Auff, E., Trenkwalder, C., Rost, B., Ransmayr, G., Winkelmann, J., Meitinger, T., and Strom, T. M. (2011) A mutation in VPS35, encoding a subunit of the retromer complex, causes late-onset Parkinson disease. Am. J. Hum. Genet. 89, 168-175
15. Ramirez, A., Heimbach, A., Grundemann, J., Stiller, B., Hampshire, D., Cid, L. P., Goebel, I., Mubaidin, A. F., Wriekat, A. L., Roeper, J., Al-Din, A., Hillmer, A. M., Karsak, M., Liss, B., Woods, C. G., Behrens, M. I., and Kubisch, C. (2006) Hereditary parkinsonism with dementia is caused by mutations in ATP13A2, encoding a lysosomal type 5 P-type ATPase. Nat. Genet. 38, 1184-1191
16. Lichtenthaler, S. F., Haass, C., and Steiner, H. (2011) Regulated intramembrane proteolysis-lessons from amyloid precursor protein processing. J. Neurochem. 117, 779-796
17. Tofaris, G. K. (2012) Lysosome-dependent pathways as a unifying theme in Parkinson's disease. Mov. Disord. 27, 1364-1369
18. Winslow, A. R., Chen, C. W., Corrochano, S., Acevedo-Arozena, A., Gordon, D. E., Peden, A. A., Lichtenberg, M., Menzies, F. M., Ravikumar, B., Imarisio, S., Brown, S., O'Kane, C. J., and Rubinsztein, D. C. (2010) alpha-Synuclein impairs macroautophagy: implications for Parkinson's disease. J. Cell Biol. 190, 1023-1037
19. Cuervo, A. M., Stefanis, L., Fredenburg, R., Lansbury, P. T., and Sulzer, D. (2004) Impaired degradation of mutant alpha-synuclein by chaperone-mediated autophagy. Science 305, 1292- 1295
20. Vogiatzi, T., Xilouri, M., Vekrellis, K., and Stefanis, L. (2008) Wild type alpha-synuclein is degraded by chaperone-mediated autophagy and macroautophagy in neuronal cells. J. Biol. Chem. 283, 23542-23556
21. Burre, J., Sharma, M., Tsetsenis, T., Buchman, V., Etherton, M. R., and Sudhof, T. C. (2010) Alpha-synuclein promotes SNARE-complex assembly in vivo and in vitro. Science 329, 1663-1667
22. Nair, U., Jotwani, A., Geng, J., Gammoh, N., Richerson, D., Yen, W. L., Griffith, J., Nag, S., Wang, K., Moss, T., Baba, M., McNew, J. A., Jiang, X., Reggiori, F., Melia, T. J., and Klionsky, D. J. (2011) SNARE proteins are required for macroautophagy. Cell 146, 290-302
23. Burre, J., Sharma, M., and Sudhof, T. C. (2012) Systematic mutagenesis of alpha-synuclein reveals distinct sequence requirements for physiological and pathological activities. J. Neurosci. 32, 15227-15242
24. Young, M. M., Kester, M., and Wang, H. G. (2013) Sphingolipids: regulators of crosstalk between apoptosis and autophagy. J. Lipid Res. 54, 5-19
25. Alegre-Abarrategui, J., Christian, H., Lufino, M. M., Mutihac, R., Venda, L. L., Ansorge, O., and Wade-Martins, R. (2009) LRRK2 regulates autophagic activity and localizes to specific membrane microdomains in a novel human genomic reporter cellular model. Hum. Mol. Genet. 18, 4022-4034
26. Gomez-Suaga, P., Luzon-Toro, B., Churamani, D., Zhang, L., Bloor-Young, D., Patel, S., Woodman, P. G., Churchill, G. C., and Hilfiker, S. (2012) Leucine-rich repeat kinase 2 regulates autophagy through a calcium-dependent pathway involving NAADP. Hum. Mol. Genet. 21, 511-525
27. Tong, Y., Giaime, E., Yamaguchi, H., Ichimura, T., Liu, Y., Si, H., Cai, H., Bonventre, J. V., and Shen, J. (2012) Loss of leucine-rich repeat kinase 2 causes age-dependent bi-phasic alterations of the autophagy pathway. Mol. Neurodeg. 7, 2
28. Orenstein, S. J., Kuo, S. H., Tasset, I., Arias, E., Koga, H., Fernandez-Carasa, I., Cortes, E., Honig, L. S., Dauer, W., Consiglio, A., Raya, A., Sulzer, D., and Cuervo, A. M. (2013) Interplay of LRRK2 with chaperone-mediated autophagy. Nat. Neurosci. 16, 394-406
29. Arighi, C. N., Hartnell, L. M., Aguilar, R. C., Haft, C. R., and Bonifacino, J. S. (2004) Role of the mammalian retromer in sorting of the cation-independent mannose 6-phosphate receptor. J. Cell Biol. 165, 123-133
30. Park, J. S., Mehta, P., Cooper, A. A., Veivers, D., Heimbach, A., Stiller, B., Kubisch, C., Fung, V. S., Krainc, D., Mackay-Sim, A., and Sue, C. M. (2011) Pathogenic effects of novel mutations in the P-type ATPase ATP13A2 (PARK9) causing Kufor-Rakeb syndrome, a form of early-onset parkinsonism. Hum. Mutat. 32, 956-964
31. Dehay, B., Ramirez, A., Martinez-Vicente, M., Perier, C., Canron, M. H., Doudnikoff, E., Vital, A., Vila, M., Klein, C., and Bezard, E. (2012) Loss of P-type ATPase ATP13A2/PARK9 function induces general lysosomal deficiency and leads to Parkinson disease neurodegeneration. Proc. Natl. Acad. Sci. U. S. A. 109, 9611-9616
32. Bras, J., Verloes, A., Schneider, S. A., Mole, S. E., and Guerreiro, R. J. (2012) Mutation of the parkinsonism gene ATP13A2 causes neuronal ceroid-lipofuscinosis. Hum. Mol. Genet. 21, 2646-2650
33. Cullen, V., Sardi, S. P., Ng, J., Xu, Y. H., Sun, Y., Tomlinson, J. J., Kolodziej, P., Kahn, I., Saftig, P., Woulfe, J., Rochet, J. C., Glicksman, M. A., Cheng, S. H., Grabowski, G. A., Shihabuddin, L. S., and Schlossmacher, M. G. (2011) Acid beta-glucosidase mutants linked to Gaucher disease, Parkinson disease, and Lewy body dementia alter alpha-synuclein processing. Ann. Neurol. 69, 940-953
34. Mazzulli, J. R., Xu, Y. H., Sun, Y., Knight, A. L., McLean, P. J., Caldwell, G. A., Sidransky, E., Grabowski, G. A., and Krainc, D. (2011) Gaucher disease glucocerebrosidase and alpha-synuclein form a bidirectional pathogenic loop in synucleinopathies. Cell 146, 37-52
35. Yap, T. L., Gruschus, J. M., Velayati, A., Westbroek, W., Goldin, E., Moaven, N., Sidransky, E., and Lee, J. C. (2011) Alphasynuclein interacts with Glucocerebrosidase providing a molecular link between Parkinson and Gaucher diseases. J. Biol. Chem. 286, 28080-28088
36. Lin, X., Parisiadou, L., Gu, X. L., Wang, L., Shim, H., Sun, L., Xie, C., Long, C. X., Yang, W. J., Ding, J., Chen, Z. Z., Gallant, P. E., Tao-Cheng, J. H., Rudow, G., Troncoso, J. C., Liu, Z., Li, Z., and Cai, H. (2009) Leucine-rich repeat kinase 2 regulates the progression of neuropathology induced by Parkinson's-diseaserelated mutant alpha-synuclein. Neuron 64, 807-827
37. Yeger-Lotem, E., Riva, L., Su, L. J., Gitler, A. D., Cashikar, A. G., King, O. D., Auluck, P. K., Geddie, M. L., Valastyan, J. S., Karger, D. R., Lindquist, S., and Fraenkel, E. (2009) Bridging highthroughput genetic and transcriptional data reveals cellular responses to alpha-synuclein toxicity. Nat. Genet. 41, 316-323
38. Usenovic, M., Tresse, E., Mazzulli, J. R., Taylor, J. P., and Krainc, D. (2012) Deficiency of ATP13A2 leads to lysosomal dysfunction, alpha-synuclein accumulation, and neurotoxicity. J. Neurosci. 32, 4240-4246
39. Schultheis, P. J., Fleming, S. M., Clippinger, A. K., Lewis, J., Tsunemi, T., Giasson, B., Dickson, D. W., Mazzulli, J. R., Bardgett, M. E., Haik, K. L., Ekhator, O., Chava, A. K., Howard, J., Gannon, M., Hoffman, E., Chen, Y., Prasad, V., Linn, S. C., Tamargo, R. J., Westbroek, W., Sidransky, E., Krainc, D., and Shull, G. E. (2013) Atp13a2-deficient mice exhibit neuronal ceroid lipofuscinosis, limited alpha-synuclein accumulation and age-dependent sensorimotor deficits. Hum. Mol. Genet. 22, 2067-2082
40. Macleod, D. A., Rhinn, H., Kuwahara, T., Zolin, A., Di Paolo, G., Maccabe, B. D., Marder, K. S., Honig, L. S., Clark, L. N., Small, S. A., and Abeliovich, A. (2013) RAB7L1 Interacts with LRRK2 to modify intraneuronal protein sorting and Parkinson's disease risk. Neuron 77, 425-439
41. Ahmed, I., Liang, Y., Schools, S., Dawson, V. L., Dawson, T. M., and Savitt, J. M. (2012) Development and characterization of a new Parkinson's disease model resulting from impaired autophagy. J. Neurosci. 32, 16503-16509
42. Friedman, L. G., Lachenmayer, M. L., Wang, J., He, L., Poulose, S. M., Komatsu, M., Holstein, G. R., and Yue, Z. (2012) Disrupted autophagy leads to dopaminergic axon and dendrite degeneration and promotes presynaptic accumulation of alphasynuclein and LRRK2 in the brain. J. Neurosci. 32, 7585-7593
43. Chu, Y., Dodiya, H., Aebischer, P., Olanow, C. W., and Kordower, J. H. (2009) Alterations in lysosomal and proteasomal markers in Parkinson's disease: relationship to alpha-synuclein inclusions. Neurobiol. Dis. 35, 385-398
44. Alvarez-Erviti, L., Rodriguez-Oroz, M. C., Cooper, J. M., Caballero, C., Ferrer, I., Obeso, J. A., and Schapira, A. H. (2010) Chaperone-mediated autophagy markers in Parkinson disease brains. Arch. Neurol. 67, 1464-1472