Selective molecular alterations in the autophagy pathway in patients with lewy body disease and in models of α-synucleinopathy

PLoS ONE

Volumn 5, Issue 2, 2010, Pages

  Crews, Leslie ^a   Spencer, Brian ^b   Desplats, Paula ^b   Patrick, Christina ^b   Paulino, Amy ^b   Rockenstein, Edward ^b   Hansen, Lawrence ^a,b   Adame, Anthony ^b   Galasko, Douglas ^b   Masliah, Eliezer ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SYNUCLEIN; ATG 10 PROTEIN; ATG 12 PROTEIN; ATG 5 PROTEIN; ATG 7 PROTEIN; BECLIN 1; LENTIVIRUS VECTOR; PROTEIN; RAPAMYCIN; UNCLASSIFIED DRUG; ATG7 PROTEIN, HUMAN; UBIQUITIN PROTEIN LIGASE;

AGED; ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOPHAGY; CLINICAL ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DIFFUSE LEWY BODY DISEASE; FEMALE; HUMAN; IMMUNOBLOTTING; IN VITRO STUDY; LYSOSOME; MALE; MOUSE; NERVE CELL; NEUROPATHOLOGY; NONHUMAN; PROTEIN EXPRESSION; TRANSGENIC MOUSE; ANIMAL; BRAIN; CELL LINE; CONFOCAL MICROSCOPY; DISEASE MODEL; ELECTRON MICROSCOPY; GENETICS; METABOLISM; NERVE DEGENERATION; PATHOLOGY; PYRAMIDAL NERVE CELL; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TUMOR CELL LINE; ULTRASTRUCTURE; WESTERN BLOTTING;

MUS MUSCULUS;

AGED; AGED, 80 AND OVER; ALPHA-SYNUCLEIN; ALZHEIMER DISEASE; ANIMALS; AUTOPHAGY; BLOTTING, WESTERN; BRAIN; CELL LINE; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; LEWY BODY DISEASE; MALE; MICE; MICE, TRANSGENIC; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON; NERVE DEGENERATION; PYRAMIDAL CELLS; RNA INTERFERENCE; SIGNAL TRANSDUCTION; UBIQUITIN-ACTIVATING ENZYMES;

EID: 77949504405     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0009313     Document Type: Article

References (89)

1. Dauer W, Kholodilov N, Vila M, Trillat AC, Goodchild R, et al. (2002) Resistance of alpha -synuclein null mice to the parkinsonian neurotoxin MPTP. Proc Natl Acad Sci U S A 99: 14524-14529.
2. Dauer W, Przedborski S (2003) Parkinson's disease: mechanisms and models. Neuron 39: 889-909.
3. Walsh DM, Selkoe DJ (2004) Oligomers on the brain: the emerging role of soluble protein aggregates in neurodegeneration. Protein Pept Lett 11: 213-228.
4. Klein WL, Krafft GA, Finch CE (2001) Targeting small Abeta oligomers: the solution to an Alzheimer's disease conundrum? Trends Neurosci 24: 219-224.
5. Hashimoto M, Rockenstein E, Crews L, Masliah E (2003) Role of protein aggregation in mitochondrial dysfunction and neurodegeneration in Alzheimer's and Parkinson's diseases. Neuromolecular Med 4: 21-36.
6. Lee M, Hyun D, Halliwell B, Jenner P (2001) Effect of the overexpression of wild-type or mutant alpha-synuclein on cell susceptibility to insult. J Neurochem 76: 998-1009.
7. Giasson BI, Duda JE, Murray IV, Chen Q, Souza JM, et al. (2000) Oxidative damage linked to neurodegeneration by selective alpha-synuclein nitration in synucleinopathy lesions. Science 290: 985-989.
8. Lashuel HA, Petre BM, Wall J, Simon M, Nowak RJ, et al. (2002) Alphasynuclein, especially the Parkinson's disease-associated mutants, forms pore-like annular and tubular protofibrils. J Mol Biol 322: 1089-1102.
9. Lashuel HA, Hartley D, Petre BM, Walz T, Lansbury PT, Jr. (2002) Neurodegenerative disease: amyloid pores from pathogenic mutations. Nature 418: 291.
10. Lippa CF, Duda JE, Grossman M, Hurtig HI, Aarsland D, et al. (2007) DLB and PDD boundary issues: diagnosis, treatment, molecular pathology, and biomarkers. Neurology 68: 812-819.
11. McKeith IG (2000) Spectrum of Parkinson's disease, Parkinson's dementia, and Lewy body dementia. Neurol Clin 18: 865-902.
12. McKeith IG, Galasko D, Kosaka K, Perry EK, Dickson DW, et al. (1996) Consensus guidelines for the clinical and pathologic diagnosis of dementia with Lewy bodies (DLB): report of the consortium on DLB international workshop. Neurology 47: 1113-1124.
13. Burn DJ (2006) Cortical Lewy body disease and Parkinson's disease dementia. Curr Opin Neurol 19: 572-579.
14. Aarsland D, Ballard CG, Halliday G (2004) Are Parkinson's disease with dementia and dementia with Lewy bodies the same entity? J Geriatr Psychiatry Neurol 17: 137-145.
15. Jellinger KA, Attems J (2006) Does striatal pathology distinguish Parkinson disease with dementia and dementia with Lewy bodies? Acta Neuropathol (Berl) 112: 253-260.
16. Litvan I, MacIntyre A, Goetz CG, Wenning GK, Jellinger K, et al. (1998) Accuracy of the clinical diagnoses of Lewy body disease, Parkinson disease, and dementia with Lewy bodies: a clinicopathologic study. Arch Neurol 55: 969-978.
17. Janvin CC, Larsen JP, Salmon DP, Galasko D, Hugdahl K, et al. (2006) Cognitive profiles of individual patients with Parkinson's disease and dementia: comparison with dementia with lewy bodies and Alzheimer's disease. Mov Disord 21: 337-342.
18. McKeith IG, Dickson DW, Lowe J, Emre M, O'Brien JT, et al. (2005) Diagnosis and management of dementia with Lewy bodies: third report of the DLB Consortium. Neurology 65: 1863-1872.
19. Masliah E, Rockenstein E, Veinbergs I, Sagara Y, Mallory M, et al. (2001) betaamyloid peptides enhance alpha-synuclein accumulation and neuronal deficits in a transgenic mouse model linking Alzheimer's disease and Parkinson's disease. Proc Natl Acad Sci U S A 98: 12245-12250.
20. Mandal PK, Pettegrew JW, Masliah E, Hamilton RL, Mandal R (2006) Interaction between Abeta peptide and alpha synuclein: molecular mechanisms in overlapping pathology of Alzheimer's and Parkinson's in dementia with Lewy body disease. Neurochem Res 31: 1153-1162.
21. Tsigelny IF, Crews L, Desplats P, Shaked GM, Sharikov Y, et al. (2008) Mechanisms of hybrid oligomer formation in the pathogenesis of combined Alzheimer's and Parkinson's diseases. PLoS ONE 3: e3135.
22. Crews L, Tsigelny I, Hashimoto M, Masliah E (2009) Role of synucleins in Alzheimer's disease. Neurotox Res 16: 306-317.
23. Cuervo AM, Stefanis L, Fredenburg R, Lansbury PT, Sulzer D (2004) Impaired degradation of mutant alpha-synuclein by chaperone-mediated autophagy. Science 305: 1292-1295.
24. Bendiske J, Bahr BA (2003) Lysosomal activation is a compensatory response against protein accumulation and associated synaptopathogenesis-an approach for slowing Alzheimer disease? J Neuropathol Exp Neurol 62: 451-463.
25. Klionsky DJ, Emr SD (2000) Autophagy as a regulated pathway of cellular degradation. Science 290: 1717-1721.
26. Levine B (2005) Eating oneself and uninvited guests: autophagy-related pathways in cellular defense. Cell 120: 159-162.
27. Cuervo AM (2004) Autophagy: in sickness and in health. Trends Cell Biol 14: 70-77.
28. Larsen KE, Sulzer D (2002) Autophagy in neurons: a review. Histol Histopathol 17: 897-908.
29. Chu CT (2006) Autophagic stress in neuronal injury and disease. J Neuropathol Exp Neurol 65: 423-432.
30. Edinger AL, Thompson CB (2004) Death by design: apoptosis, necrosis and autophagy. Curr Opin Cell Biol 16: 663-669.
31. Bahr BA, Bendiske J (2002) The neuropathogenic contributions of lysosomal dysfunction. J Neurochem 83: 481-489.
32. Nixon RA, Wegiel J, Kumar A, Yu WH, Peterhoff C, et al. (2005) Extensive involvement of autophagy in Alzheimer disease: an immuno-electron microscopy study. J Neuropathol Exp Neurol 64: 113-122.
33. Nixon RA, Cataldo AM (2006) Lysosomal system pathways: genes to neurodegeneration in Alzheimer's disease. J Alzheimers Dis 9: 277-289.
34. Pickford F, Masliah E, Britschgi M, Lucin K, Narasimhan R, et al. (2008) The autophagy-related protein beclin 1 shows reduced expression in early Alzheimer disease and regulates amyloid beta accumulation in mice. J Clin Invest 118: 2190-2199.
35. Rockenstein E, Schwach G, Ingolic E, Adame A, Crews L, et al. (2005) Lysosomal pathology associated with alpha-synuclein accumulation in transgenic models using an eGFP fusion protein. J Neurosci Res 80: 247-259.
36. Rideout HJ, Lang-Rollin I, Stefanis L (2004) Involvement of macroautophagy in the dissolution of neuronal inclusions. Int J Biochem Cell Biol 36: 2551-2562.
37. Nakajima T, Takauchi S, Ohara K, Kokai M, Nishii R, et al. (2005) Alphasynuclein-positive structures induced in leupeptin-infused rats. Brain Res 1040: 73-80.
38. Meredith GE, Totterdell S, Petroske E, Santa Cruz K, Callison RC, Jr., et al. (2002) Lysosomal malfunction accompanies alpha-synuclein aggregation in a progressive mouse model of Parkinson's disease. Brain Res 956: 156-165.
39. Stefanis L, Larsen KE, Rideout HJ, Sulzer D, Greene LA (2001) 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.
40. Martinez-Vicente M, Talloczy Z, Kaushik S, Massey AC, Mazzulli J, et al. (2008) Dopamine-modified alpha-synuclein blocks chaperone-mediated autophagy. J Clin Invest 118: 777-788.
41. Xilouri M, Vogiatzi T, Vekrellis K, Park D, Stefanis L (2009) Abberant alphasynuclein confers toxicity to neurons in part through inhibition of chaperonemediated autophagy. PLoS ONE 4: e5515.
42. Spencer B, Potkar R, Trejo M, Rockenstein E, Patrick C, 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: 13578-13588.
43. Varkonyi J, Rosenbaum H, Baumann N, MacKenzie JJ, Simon Z, et al. (2003) Gaucher disease associated with parkinsonism: four further case reports. Am J Med Genet A 116: 348-351.
44. Tayebi N, Callahan M, Madike V, Stubblefield BK, Orvisky E, et al. (2001) Gaucher disease and parkinsonism: a phenotypic and genotypic characterization. Mol Genet Metab 73: 313-321.
45. Saito Y, Suzuki K, Hulette C, Murayama S (2004) Aberrant phosphorylation of alpha-synuclein in human Niemann-Pick type C1 disease. J Neuropathol Exp Neurol 63: 323-328.
46. Uchikado H, Lin WL, DeLucia MW, Dickson DW (2006) Alzheimer disease with amygdala Lewy bodies: a distinct form of alpha-synucleinopathy. J Neuropathol Exp Neurol 65: 685-697.
47. Hansen L (1997) The Lewy body variant of Alzheimer disease. JNeural Transm 51: 111-121.
48. Braak H, Braak E (2000) Pathoanatomy of Parkinson's disease. J Neurol 247 Suppl 2: II3-10.
49. Dickson DW (2001) Alpha-synuclein and the Lewy body disorders. Curr Opin Neurol 14: 423-432.
50. Hansen L, Daniel S, Wilcock G, Lowe S (1998) Neocortical synaptophysin in Lewy body disease: relationship to Alzheimer's disease and dementia. JNeurolNeurosurgPsych.
51. Hansen L, Masliah E, Quijada-Fawcett S, Rexin D (1991) Entorhinal neurofibrillary tangles in Alzheimer disease with Lewy bodies. NeurosciLett 129: 269-272.
52. Braak H, Braak E (1991) Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 82: 239-259.
53. McKeith IG (2006) Consensus guidelines for the clinical and pathologic diagnosis of dementia with Lewy bodies (DLB): report of the Consortium on DLB International Workshop. J Alzheimers Dis 9: 417-423.
54. Jellinger KA, Bancher C (1998) Neuropathology of Alzheimer's disease: a critical update. J Neural Transm Suppl 54: 77-95.
55. Masliah E, Rockenstein E, Veinbergs I, Mallory M, Hashimoto M, et al. (2000) Dopaminergic loss and inclusion body formation in alpha-synuclein mice: Implications for neurodegenerative disorders. Science 287: 1265-1269.
56. Rockenstein E, Mallory M, Hashimoto M, Song D, Shults CW, et al. (2002) Differential neuropathological alterations in transgenic mice expressing alphasynuclein from the platelet-derived growth factor and Thy-1 promoters. J Neurosci Res 68: 568-578.
57. Masliah E, Rockenstein E, Adame A, Alford M, Crews L, et al. (2005) Effects of alpha-Synuclein Immunization in a Mouse Model of Parkinson's Disease. Neuron 46: 857-868.
58. Mucke L, Masliah E, Yu GQ, Mallory M, Rockenstein EM, et al. (2000) Highlevel neuronal expression of abeta 1-42 in wild-type human amyloid protein precursor transgenic mice: synaptotoxicity without plaque formation. J Neurosci 20: 4050-4058.
59. Veinbergs I, Van Uden E, Mallory M, Alford M, McGiffert C, et al. (2001) Role of apolipoprotein E receptors in regulating the differential in vivo neurotrophic effects of apolipoprotein E. Exp Neurol 170: 15-26.
60. Naldini L, Blomer U, Gallay P, Ory D, Mulligan R, et al. (1996) In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science 272: 263-267.
61. Tiscornia G, Singer O, Verma IM (2006) Design and cloning of lentiviral vectors expressing small interfering RNAs. Nat Protoc 1: 234-240.
62. Marr RA, Rockenstein E, Mukherjee A, Kindy MS, Hersh LB, et al. (2003) Neprilysin gene transfer reduces human amyloid pathology in transgenic mice. J Neurosci 23: 1992-1996.
63. Takenouchi T, Hashimoto M, Hsu L, Mackowski B, Rockenstein E, et al. (2001) Reduced neuritic outgrowth and cell adhesion in neuronal cells transfected with human a-synuclein. MolCell Neurosci 17: 141-150.
64. Hashimoto M, Takenouchi T, Rockenstein E, Masliah E (2003) Alpha-synuclein up-regulates expression of caveolin-1 and down-regulates extracellular signalregulated kinase activity in B103 neuroblastoma cells: role in the pathogenesis of Parkinson's disease. J Neurochem 85: 1468-1479.
65. Masliah E, Alford M, Adame A, Rockenstein E, Galasko D, et al. (2003) Abeta1-42 promotes cholinergic sprouting in patients with AD and Lewy body variant of AD. Neurology 61: 206-211.
66. Mucke L, Abraham C, Ruppe M, Rockenstein E, Toggas S, et al. (1995) Protection against HIV-1 gp120-induced brain damage by neuronal overexpression of human amyloid precursor protein (hAPP). JExpMed 181: 1551-1556.
67. Toggas S, Masliah E, Rockenstein E, Mucke L (1994) Central nervous system damage produced by expression of the HIV-1 coat protein gp120 in transgenic mice. Nature 367: 188-193.
68. Hashimoto M, Sagara Y, Everall IP, Mallory M, Everson A, et al. (2002) Fibroblast growth factor 1 regulates signaling via the GSK3{beta} pathway: implications for neuroprotection. J Biol Chem 277: 32985-32991.
69. van Kats JP, van Meegen JR, Verdouw PD, Duncker DJ, Schalekamp MA, et al. (2001) Subcellular localization of angiotensin II in kidney and adrenal. J Hypertens 19: 583-589.
70. Rockenstein E, Hansen LA, Mallory M, Trojanowski JQ, Galasko D, et al. (2001) Altered expression of the synuclein family mRNA in Lewy body and Alzheimer's disease. Brain Res 914: 48-56.
71. Blommaart EF, Krause U, Schellens JP, Vreeling-Sindelarova H, Meijer AJ (1997) The phosphatidylinositol 3-kinase inhibitors wortmannin and LY294002 inhibit autophagy in isolated rat hepatocytes. Eur J Biochem 243: 240-246.
72. Chang YY, Juhasz G, Goraksha-Hicks P, Arsham AM, Mallin DR, et al. (2009) Nutrient-dependent regulation of autophagy through the target of rapamycin pathway. Biochem Soc Trans 37: 232-236.
73. Kawamata T, Kamada Y, Kabeya Y, Sekito T, Ohsumi Y (2008) Organization of the pre-autophagosomal structure responsible for autophagosome formation. Mol Biol Cell 19: 2039-2050.
74. 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: 25009-25013.
75. Williams A, Jahreiss L, Sarkar S, Saiki S, Menzies FM, et al. (2006) Aggregateprone proteins are cleared from the cytosol by autophagy: therapeutic implications. Curr Top Dev Biol 76: 89-101.
76. Ravikumar B, Duden R, Rubinsztein DC (2002) Aggregate-prone proteins with polyglutamine and polyalanine expansions are degraded by autophagy. Hum Mol Genet 11: 1107-1117.
77. Pan T, Kondo S, Zhu W, Xie W, Jankovic J, et al. (2008) Neuroprotection of rapamycin in lactacystin-induced neurodegeneration via autophagy enhancement. Neurobiol Dis 32: 16-25.
78. Boland B, Kumar A, Lee S, Platt FM, Wegiel J, et al. (2008) Autophagy induction and autophagosome clearance in neurons: relationship to autophagic pathology in Alzheimer's disease. J Neurosci 28: 6926-6937.
79. Sarkar S, Rubinsztein DC (2008) Small molecule enhancers of autophagy for neurodegenerative diseases. Mol Biosyst 4: 895-901.
80. Ravikumar B, Vacher C, Berger Z, Davies JE, Luo S, 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: 585-595.
81. Tain LS, Mortiboys H, Tao RN, Ziviani E, Bandmann O, et al. (2009) Rapamycin activation of 4E-BP prevents parkinsonian dopaminergic neuron loss. Nat Neurosci 12: 1129-1135.
82. Zhu JH, Horbinski C, Guo F, Watkins S, Uchiyama Y, et al. (2007) Regulation of autophagy by extracellular signal-regulated protein kinases during 1-methyl-4-phenylpyridinium-induced cell death. Am J Pathol 170: 75-86.
83. Chu Y, Dodiya H, Aebischer P, Olanow CW, Kordower JH (2009) Alterations in lysosomal and proteasomal markers in Parkinson's disease: relationship to alpha-synuclein inclusions. Neurobiol Dis 35: 385-398.
84. Sevlever D, Jiang P, Yen SH (2008) Cathepsin D is the main lysosomal enzyme involved in the degradation of alpha-synuclein and generation of its carboxyterminally truncated species. Biochemistry 47: 9678-9687.
85. Cullen V, Lindfors M, Ng J, Paetau A, Swinton E, et al. (2009) Cathepsin D expression level affects alpha-synuclein processing, aggregation, and toxicity in vivo. Mol Brain 2: 5.
86. Lee JA, Gao FB (2009) Inhibition of autophagy induction delays neuronal cell loss caused by dysfunctional ESCRT-III in frontotemporal dementia. J Neurosci 29: 8506-8511.
87. Skibinski G, Parkinson NJ, Brown JM, Chakrabarti L, Lloyd SL, et al. (2005) Mutations in the endosomal ESCRTIII-complex subunit CHMP2B in frontotemporal dementia. Nat Genet 37: 806-808.
88. Parkinson N, Ince PG, Smith MO, Highley R, Skibinski G, et al. (2006) ALS phenotypes with mutations in CHMP2B (charged multivesicular body protein 2B). Neurology 67: 1074-1077.
89. Komatsu M, Waguri S, Chiba T, Murata S, Iwata J, et al. (2006) Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature 441: 880-884.