TFEB-mediated autophagy rescues midbrain dopamine neurons from α-synuclein toxicity

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 19, 2013, Pages

  Decressac, Mickael ^a   Mattsson, Bengt ^a   Weikop, Pia ^b   Lundblad, Martin ^a   Jakobsson, Johan ^a   Björklund, Anders ^a  

^a LUND UNIVERSITY   (Sweden)

^b International Center for Research and Research Training in Endocrine Disruption of Male Reproduction and Child Health   (Denmark)

Author keywords

Adeno associated virus; Aggregates; Beclin; Synucleinopathy

Indexed keywords

ALPHA SYNUCLEIN; BECLIN 1; CATHEPSIN B; CATHEPSIN D; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; MAMMALIAN TARGET OF RAPAMYCIN; MICRORNA; OLIGOMER; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR EB; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOPHAGY; CELL FUNCTION; CELL LEVEL; CELL NUCLEUS; CONTROLLED STUDY; CYTOPLASM; DISEASE COURSE; DOPAMINERGIC NERVE CELL; DOWN REGULATION; FEMALE; GENE OVEREXPRESSION; GENE REPRESSION; HUMAN; HUMAN TISSUE; IN VIVO STUDY; LYSOSOME; MESENCEPHALON; NERVE DEGENERATION; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; PARKINSON DISEASE; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; SUBSTANTIA NIGRA;

ADENO-ASSOCIATED VIRUS; AGGREGATES; BECLIN; SYNUCLEINOPATHY;

ALPHA-SYNUCLEIN; ANIMALS; APOPTOSIS REGULATORY PROTEINS; AUTOPHAGY; BASIC HELIX-LOOP-HELIX LEUCINE ZIPPER TRANSCRIPTION FACTORS; BRAIN; BRAIN MAPPING; DEPENDOVIRUS; DOPAMINE; FEMALE; HEK293 CELLS; HUMANS; IMMUNOHISTOCHEMISTRY; LYSOSOMES; MESENCEPHALON; NEURONS; NEUROPROTECTIVE AGENTS; PARKINSON DISEASE; PROTEIN BINDING; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84877351078     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1305623110     Document Type: Article

References (60)

1. Levine B, Kroemer G (2008) Autophagy in the pathogenesis of disease. Cell 132(1): 27-42.
2. Rubinsztein DC (2006) The roles of intracellular protein-degradation pathways in neurodegeneration. Nature 443(7113): 780-786.
3. Rubinsztein DC, Mariño G, Kroemer G (2011) Autophagy and aging. Cell 146(5): 682-695.
4. Wong E, Cuervo AM (2010) Autophagy gone awry in neurodegenerative diseases. Nat Neurosci 13(7): 805-811.
5. Chu Y, Dodiya H, Aebischer P, Olanow CW, Kordower JH (2009) Alterations in lysosomal and proteasomal markers in Parkinson's disease: Relationship to alphasynuclein inclusions. Neurobiol Dis 35(3): 385-398.
6. Crews L, et al. (2010) Selective molecular alterations in the autophagy pathway in patients with Lewy body disease and in models of alpha- synucleinopathy. PLoS ONE 5(2):e9313.
7. Dehay B, et al. (2010) Pathogenic lysosomal depletion in Parkinson's disease. J Neurosci 30(37): 12535-12544.
8. Lee HJ, Khoshaghideh F, Patel S, Lee SJ (2004) Clearance of alpha-synuclein oligomeric intermediates via the lysosomal degradation pathway. J Neurosci 24(8): 1888-1896.
9. Vogiatzi T, Xilouri M, Vekrellis K, Stefanis L (2008) Wild type alpha-synuclein is degraded by chaperone-mediated autophagy and macroautophagy in neuronal cells. J Biol Chem 283(35): 23542-23556.
10. Webb JL, Ravikumar B, Atkins J, Skepper JN, Rubinsztein DC (2003) Alpha-Synuclein is degraded by both autophagy and the proteasome. J Biol Chem 278(27): 25009-25013.
11. Mak SK, McCormack AL, Manning-Bog AB, Cuervo AM, Di Monte DA (2010) Lysosomal degradation of alpha-synuclein in vivo. J Biol Chem 285(18): 13621-13629.
12. Xilouri M, Vogiatzi T, Vekrellis K, Park D, Stefanis L (2009) Abberant alpha-synuclein confers toxicity to neurons in part through inhibition of chaperone-mediated autophagy. PLoS ONE 4(5):e5515.
13. Cuervo AM, Stefanis L, Fredenburg R, Lansbury PT, Sulzer D (2004) Impaired degradation of mutant alpha-synuclein by chaperone-mediated autophagy. Science 305(5688): 1292-1295.
14. Ebrahimi-Fakhari D, et al. (2011) Distinct roles in vivo for the ubiquitin-proteasome system and the autophagy-lysosomal pathway in the degradation of α-synuclein. J Neurosci 31(41): 14508-14520.
15. Martinez-Vicente M, et al. (2008) Dopamine-modified alpha-synuclein blocks chaperone-mediated autophagy. J Clin Invest 118(2): 777-788.
16. Friedman LG, et al. (2012) Disrupted autophagy leads to dopaminergic axon and dendrite degeneration and promotes presynaptic accumulation of α-synuclein and LRRK2 in the brain. J Neurosci 32(22): 7585-7593.
17. Hara T, et al. (2006) Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature 441(7095): 885-889.
18. Komatsu M, et al. (2006) Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature 441(7095): 880-884.
19. Usenovic M, Tresse E, Mazzulli JR, Taylor JP, Krainc D (2012) Deficiency of ATP13A2 leads to lysosomal dysfunction, α-synuclein accumulation, and neurotoxicity. J Neurosci 32(12): 4240-4246.
20. Mazzulli JR, et al. (2011) Gaucher disease glucocerebrosidase and α-synuclein form a bidirectional pathogenic loop in synucleinopathies. Cell 146(1): 37-52.
21. Winder-Rhodes SE, et al. (2012) Genetic and pathological links between Parkinson's disease and the lysosomal disorder Sanfilippo syndrome. Mov Disord 27(2): 312-315.
22. Pang S, Chen D, Zhang A, Qin X, Yan B (2012) Genetic analysis of the LAMP-2 gene promoter in patients with sporadic Parkinson's disease. Neurosci Lett 526(1): 63-67.
23. Ramirez A, et al. (2006) Hereditary parkinsonism with dementia is caused by mutations in ATP13A2, encoding a lysosomal type 5 P-type ATPase. Nat Genet 38(10): 1184-1191.
24. Harris H, Rubinsztein DC (2012) Control of autophagy as a therapy for neurodegenerative disease. Nat Rev Neurol 8(2): 108-117.
25. Rubinsztein DC, Gestwicki JE, Murphy LO, Klionsky DJ (2007) Potential therapeutic applications of autophagy. Nat Rev Drug Discov 6(4): 304-312.
26. Nascimento-Ferreira I, et al. (2011) Overexpression of the autophagic Beclin-1 protein clears mutant ataxin-3 and alleviates Machado-Joseph disease. Brain 134(Pt 5): 1400-1415.
27. Shibata M, et al. (2006) Regulation of intracellular accumulation of mutant Huntingtin by Beclin 1. J Biol Chem 281(20): 14474-14485.
28. Spencer B, et al. (2009) Beclin 1 gene transfer activates autophagy and ameliorates the neurodegenerative pathology in alpha-synuclein models of Parkinson's and Lewy body diseases. J Neurosci 29(43): 13578-13588.
29. Bové J, Martínez-Vicente M, Vila M (2011) Fighting neurodegeneration with rapamycin: Mechanistic insights. Nat Rev Neurosci 12(8): 437-452.
30. Malagelada C, Jin ZH, Jackson-Lewis V, Przedborski S, Greene LA (2010) Rapamycin protects against neuron death in in vitro and in vivo models of Parkinson's disease. J Neurosci 30(3): 1166-1175.
31. Menzies FM, et al. (2010) Autophagy induction reduces mutant ataxin-3 levels and toxicity in a mouse model of spinocerebellar ataxia type 3. Brain 133(Pt 1): 93-104.
32. Ravikumar B, et al. (2004) Inhibition of mTOR induces autophagy and reduces toxicity of polyglutamine expansions in fly and mouse models of Huntington disease. Nat Genet 36(6): 585-595.
33. Spilman P, et al. (2010) Inhibition of mTOR by rapamycin abolishes cognitive deficits and reduces amyloid-beta levels in a mouse model of Alzheimer's disease. PLoS ONE 5(4):e9979.
34. Schaeffer V, et al. (2012) Stimulation of autophagy reduces neurodegeneration in a mouse model of human tauopathy. Brain 135(Pt 7): 2169-2177.
35. Sardiello M, et al. (2009) A gene network regulating lysosomal biogenesis and function. Science 325(5939): 473-477.
36. Settembre C, et al. (2011) TFEB links autophagy to lysosomal biogenesis. Science 332(6036): 1429-1433.
37. Peña-Llopis S, et al. (2011) Regulation of TFEB and V-ATPases by mTORC1. EMBO J 30(16): 3242-3258.
38. Roczniak-Ferguson A, et al. (2012) The transcription factor TFEB links mTORC1 signaling to transcriptional control of lysosome homeostasis. Sci Signal 5(228):ra42.
39. Settembre C, et al. (2012) A lysosome-to-nucleus signalling mechanism senses and regulates the lysosome via mTOR and TFEB. EMBO J 31(5): 1095-1108.
40. Tsunemi T, et al. (2012) PGC-1alpha rescues Huntington's Disease proteotoxicity by preventing oxidative stress and promoting TFEB function. Sci Transl Med 4(142): 142ra197.
41. Decressac M, Mattsson B, Björklund A (2012) Comparison of the behavioural and histological characteristics of the 6-OHDA and α-synuclein rat models of Parkinson's disease. Exp Neurol 235(1): 306-315.
42. Decressac M, Mattsson B, Lundblad M, Weikop P, Björklund A (2012) Progressive neurodegenerative and behavioural changes induced by AAV-mediated overexpression of α-synuclein in midbrain dopamine neurons. Neurobiol Dis 45(3): 939-953.
43. Kirik D, et al. (2002) Parkinson-like neurodegeneration induced by targeted overexpression of alpha-synuclein in the nigrostriatal system. J Neurosci 22(7): 2780-2791.
44. Winner B, et al. (2011) In vivo demonstration that alpha-synuclein oligomers are toxic. Proc Natl Acad Sci USA 108(10): 4194-4199.
45. Bjørkøy G, et al. (2009) Monitoring autophagic degradation of p62/SQSTM1. Methods Enzymol 452: 181-197.
46. Ostrerova N, et al. (1999) alpha-Synuclein shares physical and functional homology with 14-3-3 proteins. J Neurosci 19(14): 5782-5791.
47. Perez RG, et al. (2002) A role for alpha-synuclein in the regulation of dopamine biosynthesis. J Neurosci 22(8): 3090-3099.
48. Dehay B, et al. (2012) Loss of P-type ATPase ATP13A2/PARK9 function induces general lysosomal deficiency and leads to Parkinson disease neurodegeneration. Proc Natl Acad Sci USA 109(24): 9611-9616.
49. Hirsch E, Graybiel AM, Agid YA (1988) Melanized dopaminergic neurons are differentially susceptible to degeneration in Parkinson's disease. Nature 334(6180): 345-348.
50. Uhl GR, Hedreen JC, Price DL (1985) Parkinson's disease: Loss of neurons from the ventral tegmental area contralateral to therapeutic surgical lesions. Neurology 35(8): 1215-1218.
51. Maingay M, Romero-Ramos M, Kirik D (2005) Viral vector mediated overexpression of human alpha-synuclein in the nigrostriatal dopaminergic neurons: A new model for Parkinson's disease. CNS Spectr 10(3): 235-244.
52. Lin X, et al. (2012) Conditional expression of Parkinson's disease-related mutant α-synuclein in the midbrain dopaminergic neurons causes progressive neurodegeneration and degradation of transcription factor nuclear receptor related 1. J Neurosci 32(27): 9248-9264.
53. Ubl A, et al. (2002) 14-3-3 protein is a component of Lewy bodies in Parkinson's disease-mutation analysis and association studies of 14-3-3 eta. Brain Res Mol Brain Res 108(1-2): 33-39.
54. Souza JM, Giasson BI, Lee VM, Ischiropoulos H (2000) Chaperone-like activity of synucleins. FEBS Lett 474(1): 116-119.
55. Kawamoto Y, et al. (2002) 14-3-3 proteins in Lewy bodies in Parkinson disease and diffuse Lewy body disease brains. J Neuropathol Exp Neurol 61(3): 245-253.
56. Åkerblom M, et al. (2012) MicroRNA-124 is a subventricular zone neuronal fate determinant. J Neurosci 32(26): 8879-8889.
57. Grimm D (2002) Production methods for gene transfer vectors based on adenoassociated virus serotypes. Methods 28(2): 146-157.
58. Zolotukhin S, et al. (1999) Recombinant adeno-associated virus purification using novel methods improves infectious titer and yield. Gene Ther 6(6): 973-985.
59. Torres EM, et al. (2011) Increased efficacy of the 6-hydroxydopamine lesion of the median forebrain bundle in small rats, by modification of the stereotaxic coordinates. J Neurosci Methods 200(1): 29-35.
60. Paxinos G, Watson C (1986) The Rat Brain in Stereotaxic Coordinates. (Academic, San Diego).