Diminished parkin solubility and Co-Localization with intraneuronal amyloid-β are associated with autophagic defects in Alzheimer's disease

Journal of Alzheimer's Disease

Volumn 33, Issue 1, 2013, Pages 231-247

  Lonskaya, Irina ^a   Shekoyan, Ashot R ^a   Hebron, Michaeline L ^a   Desforges, Nicole ^a   Algarzae, Norah K ^a   Moussa, Charbel E H ^a  

^a GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

amyloid ; autophagy; parkin; tau phosphorylation

Indexed keywords

AMYLOID BETA PROTEIN[1-42]; PARKIN; TAU PROTEIN;

ADULT; AGED; ALZHEIMER DISEASE; ANIMAL TISSUE; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; AUTOPSY; BRAIN CORTEX; CONTROLLED STUDY; FEMALE; GENE TRANSFER; HIPPOCAMPUS; HUMAN; HUMAN TISSUE; LYSOSOME; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSMISSION ELECTRON MICROSCOPY; WESTERN BLOTTING; WILD TYPE;

EID: 84872480032     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-2012-121141     Document Type: Article

References (72)

1. Hardy J, Selkoe DJ (2002) The amyloid hypothesis of Alzheimer's disease: Progress and problems on the road to therapeutics. Science 297, 353-356. (Pubitemid 34790756)
2. Haass C, Schlossmacher MG, Hung AY, Vigo-Pelfrey C, Mellon A, Ostaszewski BL, Lieberburg I, Koo EH, Schenk D, Teplow DB, et al. (1992) Amyloid beta-peptide is produced by cultured cells during normal metabolism. Nature 359, 322-325.
3. Koo EH, Squazzo SL (1994) Evidence that production and release of amyloid beta-protein involves the endocytic pathway. J Biol Chem 269, 17386-17389. (Pubitemid 24218009)
4. Cook DG, Forman MS, Sung JC, Leight S, Kolson DL, Iwatsubo T, Lee VM, Doms RW(1997) Alzheimer's A beta(1-42) is generated in the endoplasmic reticulum/intermediate compartment of NT2N cells. Nat Med 3, 1021-1023. (Pubitemid 27391958)
5. Greenfield JP, Tsai J, Gouras GK, Hai B, Thinakaran G, Checler F, Sisodia SS, Greengard P,XuH(1999) Endoplasmic reticulum and trans-Golgi network generate distinct populations of Alzheimer beta-amyloid peptides. Proc Natl Acad Sci U S A 96, 742-747. (Pubitemid 29061279)
6. Skovronsky DM, Doms RW, Lee VM (1998) Detection of a novel intraneuronal pool of insoluble amyloid beta protein that accumulates with time in culture. J Cell Biol 141, 1031-1039. (Pubitemid 28243969)
7. Xu H, SweeneyD,Wang R, Thinakaran G, LoAC, Sisodia SS, Greengard P, Gandy S (1997) Generation of Alzheimer betaamyloid protein in the trans-Golgi network in the apparent absence of vesicle formation. Proc Natl Acad Sci U S A 94, 3748-3752. (Pubitemid 27180444)
8. Gouras GK, Tsai J, Naslund J,Vincent B, Edgar M, Checler F, Greenfield JP, HaroutunianV, Buxbaum JD, Xu H, Greengard P, Relkin NR (2000) Intraneuronal Abeta42 accumulation in human brain. Am J Pathol 156, 15-20. (Pubitemid 30644433)
9. Wilson CA, Doms RW, Lee VM (1999) Intracellular APP processing and A beta production in Alzheimer disease. J Neuropathol Exp Neurol 58, 787-794. (Pubitemid 29372833)
10. Li M, Chen L, Lee DH, Yu LC, Zhang Y (2007) The role of intracellular amyloid beta in Alzheimer's disease. Prog Neurobiol 83, 131-139. (Pubitemid 47484046)
11. Oddo S, Caccamo A, Kitazawa M, Tseng BP, LaFerla FM (2003) Amyloid deposition precedes tangle formation in a triple transgenic model of Alzheimer's disease. Neurobiol Aging 24, 1063-1070. (Pubitemid 37487883)
12. Cataldo AM, Barnett JL, Pieroni C, Nixon RA (1997) Increased neuronal endocytosis and protease delivery to early endosomes in sporadic Alzheimer's disease: Neuropathologic evidence for a mechanism of increased beta-amyloidogenesis. J Neurosci 17, 6142-6151. (Pubitemid 27329890)
13. Cataldo AM, Peterhoff CM, Troncoso JC, Gomez-Isla T, Hyman BT, Nixon RA (2000) Endocytic pathway abnormalities precede amyloid beta deposition in sporadic Alzheimer's disease and Down syndrome: Differential effects of APOE genotype and presenilin mutations.AmJ Pathol 157, 277-286. (Pubitemid 30641743)
14. D'Andrea MR, Nagele RG, Wang HY, Peterson PA, Lee DH (2001) Evidence that neurones accumulating amyloid can undergo lysis to form amyloid plaques in Alzheimer's disease. Histopathology 38, 120-134. (Pubitemid 32193626)
15. Tampellini D, Rahman N, LinMT, Capetillo-Zarate E, Gouras GK (2011) Impaired beta-Amyloid Secretion in Alzheimer's Disease Pathogenesis. J Neurosci 31, 15384-15390.
16. Shimura H, Hattori N, Kubo S, Mizuno Y, Asakawa S, Minoshima S, Shimizu N, Iwai K, Chiba T, Tanaka K, Suzuki T (2000) Familial Parkinson disease gene product, parkin, is a ubiquitin-protein ligase. Nat Genet 25, 302-305. (Pubitemid 30437317)
17. Geisler S, Holmstrom KM, Skujat D, Fiesel FC, Rothfuss OC, Kahle PJ, Springer W (2010) PINK1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1. Nat Cell Biol 12, 119-131.
18. Narendra D, Tanaka A, Suen DF, Youle RJ (2008) Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J Cell Biol 183, 795-803.
19. Park J, Kim Y, Chung J (2009) Mitochondrial dysfunction and Parkinson's disease genes: Insights from Drosophila. Dis Model Mech 2, 336-340.
20. Vives-Bauza C, Zhou C, Huang Y, Cui M, de Vries RL, Kim J, May J, Tocilescu MA, Liu W, Ko HS, Magrane J, Moore DJ, Dawson VL, Grailhe R, Dawson TM, Li C, Tieu K, Przedborski S (2010) PINK1-dependent recruitment of Parkin to mitochondria in mitophagy. Proc Natl Acad Sci U S A 107, 378-383.
21. Orvedahl A, Sumpter R Jr, Xiao G, Ng A, Zou Z, Tang Y, Narimatsu M, Gilpin C, Sun Q, Roth M, Forst CV,Wrana JL, Zhang YE, Luby-Phelps K, Xavier RJ, XieY, LevineB(2011) Image-based genome-wide siRNA screen identifies selective autophagy factors. Nature 480, 113-117.
22. Kitada T, Asakawa S, Hattori N, Matsumine H, Yamamura Y, Minoshima S, Yokochi M, Mizuno Y, Shimizu N (1998) Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature 392, 605-608. (Pubitemid 28207717)
23. Lucking CB, Durr A, Bonifati V, Vaughan J, De Michele G, Gasser T, Harhangi BS, Meco G, Denefle P,Wood NW, Agid Y, Brice A (2000) Association between early-onset Parkinson's disease and mutations in the parkin gene. N Engl J Med 342, 1560-1567. (Pubitemid 30340501)
24. Rodriguez-Navarro JA, Gomez A, Rodal I, Perucho J, Martinez A, Furio V, Ampuero I, Casarejos MJ, Solano RM, de Yebenes JG, Mena MA (2008) Parkin deletion causes cerebral and systemic amyloidosis in human mutated tau over-Expressing mice. Hum Mol Genet 17, 3128-3143.
25. Perucho J, Casarejos MJ, Rubio I, Rodriguez-Navarro JA, Gomez A, Ampuero I, Rodal I, Solano RM, Carro E, Garcia de Yebenes J, MenaMA(2010) The effects of parkin suppression on the behaviour, amyloid processing, and cell survival inAPP mutant transgenic mice. Exp Neurol 221, 54-67.
26. Seglen PO (1987) Regulation of autophagic protein degradation in isolated liver cells. In Lysosomes: Their Role in Protein Breakdown, Glaumann H, Ballard FJ, eds. Academic Press, London, pp. 369-414.
27. de Duve C,Wattiaux R (1966) Functions of lysosomes. Annu Rev Physiol 28, 435-492.
28. Dunn WA Jr (1994) Autophagy and related mechanisms of lysosome-mediated protein degradation. Trends Cell Biol 4, 139-143. (Pubitemid 24107709)
29. Gordon PB, Seglen PO (1988) Prelysosomal convergence of autophagic and endocytic pathways. Biochem Biophys Res Commun 151, 40-47.
30. Boland B, Kumar A, Lee S, Platt FM, Wegiel J, Yu WH, Nixon RA (2008) Autophagy induction and autophagosome clearance in neurons: Relationship to autophagic pathology in Alzheimer's disease. J Neurosci 28, 6926-6937.
31. Kegel KB, Kim M, Sapp E, McIntyre C, Castano JG, Aronin N, DiFiglia M (2000) Huntingtin expression stimulates endosomal-lysosomal activity, endosome tubulation, and autophagy. J Neurosci 20, 7268-7278.
32. Nixon RA, Wegiel J, Kumar A, Yu WH, Peterhoff C, Cataldo A, Cuervo AM (2005) Extensive involvement of autophagy in Alzheimer disease: An immuno-Electron microscopy study. J Neuropathol Exp Neurol 64, 113-122. (Pubitemid 40349309)
33. Ravikumar B, Duden R, Rubinsztein DC (2002) Aggregateprone proteins with polyglutamine and polyalanine expansions are degraded by autophagy. Hum Mol Genet 11, 1107-1117. (Pubitemid 34521091)
34. Sabatini DM (2006) mTOR and cancer: Insights into a complex relationship. Nat Rev Cancer 6, 729-734. (Pubitemid 44286004)
35. Stefanis L, Larsen KE, Rideout HJ, Sulzer D, Greene LA (2001) Expression of A53T mutant but not wild-type alphasynuclein in PC12 cells induces alterations of the ubiquitindependent degradation system, loss of dopamine release, and autophagic cell death. J Neurosci 21, 9549-9560. (Pubitemid 34184043)
36. 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. (Pubitemid 37548663)
37. Yang Y, Fukui K, Koike T, Zheng X (2007) Induction of autophagy in neurite degeneration of mouse superior cervical ganglion neurons. Eur J Neurosci 26, 2979-2988. (Pubitemid 350115519)
38. Mizushima N, Levine B, Cuervo AM, Klionsky DJ (2008) Autophagy fights disease through cellular self-digestion. Nature 451, 1069-1075. (Pubitemid 351317450)
39. Nixon RA, Yang DS, Lee JH (2008) Neurodegenerative lysosomal disorders: A continuum from development to late age. Autophagy 4, 590-599.
40. Winslow AR, Rubinsztein DC (2008) Autophagy in neurodegeneration and development. Biochim Biophys Acta 1782, 723-729.
41. Rodriguez-Navarro JA, Rodriguez L, Casarejos MJ, Solano RM, Gomez A, Perucho J, Cuervo AM, Garcia de Yebenes J, MenaMA(2010)Trehalose ameliorates dopaminergic and tau pathology in parkin deleted/tau overexpressing mice through autophagy activation. Neurobiol Dis 39, 423-438.
42. Casarejos MJ, Solano RM, Rodriguez-Navarro JA, Gomez A, Perucho J, Castano JG, Garcia de Yebenes J, Mena MA (2009) Parkin deficiency increases the resistance of midbrain neurons and glia to mild proteasome inhibition: The role of autophagy and glutathione homeostasis. J Neurochem 110, 1523-1537.
43. Burns MP, Zhang L, Rebeck GW, Querfurth HW, Moussa CE(2009) Parkin promotes intracellular Abeta1-42 clearance. Hum Mol Genet 18, 3206-3216.
44. Khandelwal PJ, Herman AM, Hoe HS, Rebeck GW, Moussa CE (2011) Parkin mediates beclin-dependent autophagic clearance of defective mitochondria and ubiquitinated Abeta in AD models. Hum Mol Genet 20, 2091-2102.
45. Rebeck GW, Hoe HS, Moussa CE (2010) Beta-amyloid1-42 gene transfer model exhibits intraneuronal amyloid, gliosis, tau phosphorylation, and neuronal loss. J Biol Chem 285, 7440-7446.
46. Herman AM, Moussa CE (2011) The ubiquitin ligase parkin modulates the execution of autophagy. Autophagy 7, 919-921.
47. Khandelwal PJ, Dumanis SB, Feng LR, Maguire-Zeiss K, Rebeck G, Lashuel HA, Moussa CE (2010) Parkinson-related parkin reduces alpha-Synuclein phosphorylation in a gene transfer model. Mol Neurodegener 5, 47.
48. Marzella L, Ahlberg J, Glaumann H (1982) Isolation of autophagic vacuoles from rat liver: Morphological and biochemical characterization. J Cell Biol 93, 144-154. (Pubitemid 12117051)
49. Rosen KM, Moussa CE, Lee HK, Kumar P, Kitada T, Qin G, Fu Q, QuerfurthHW(2010) Parkin reverses intracellular betaamyloid accumulation and its negative effects on proteasome function. J Neurosci Res 88, 167-178.
50. RenY, Zhao J, Feng J (2003) Parkin binds to alpha/beta tubulin and increases their ubiquitination and degradation. J Neurosci 23, 3316-3324. (Pubitemid 36531973)
51. Staropoli JF, McDermott C, Martinat C, Schulman B, Demireva E, Abeliovich A (2003) Parkin is a component of an SCF-like ubiquitin ligase complex and protects postmitotic neurons from kainate excitotoxicity. Neuron 37, 735-749. (Pubitemid 36288547)
52. Feany MB, Pallanck LJ (2003) Parkin: A multipurpose neuroprotective agent? Neuron 38, 13-16. (Pubitemid 36423349)
53. Moore DJ, Zhang L, Troncoso J, Lee MK, Hattori N, Mizuno Y, Dawson TM, Dawson VL (2005) Association of DJ-1 and parkin mediated by pathogenic DJ-1 mutations and oxidative stress. Hum Mol Genet 14, 71-84. (Pubitemid 40123464)
54. Xiong H, Wang D, Chen L, Choo YS, Ma H, Tang C, Xia K, Jiang W, Ronai Z, Zhuang X, Zhang Z (2009) Parkin, PINK1, and DJ-1 form a ubiquitin E3 ligase complex promoting unfolded protein degradation. J Clin Invest 119, 650-660.
55. Gonzalez-Polo RA, Boya P, Pauleau AL, Jalil A, Larochette N, Souquere S, Eskelinen EL, Pierron G, Saftig P, Kroemer G (2005) The apoptosis/autophagy paradox: Autophagic vacuolization before apoptotic death. J Cell Sci 118, 3091-3102. (Pubitemid 41149913)
56. Lee JH, Yu WH, Kumar A, Lee S, Mohan PS, Peterhoff CM, Wolfe DM, Martinez-Vicente M, Massey AC, Sovak G, Uchiyama Y, Westaway D, Cuervo AM, Nixon RA (2010) Lysosomal proteolysis and autophagy require presenilin 1 and are disrupted by Alzheimer-related PS1 mutations. Cell 141, 1146-1158.
57. Yu WH, Cuervo AM, Kumar A, Peterhoff CM, Schmidt SD, Lee JH, Mohan PS, Mercken M, Farmery MR, Tjernberg LO, Jiang Y, Duff K, Uchiyama Y, Naslund J, Mathews PM, Cataldo AM, Nixon RA (2005) Macroautophagy - a novel Beta-amyloid peptide-generating pathway activated in Alzheimer's disease. J Cell Biol 171, 87-98. (Pubitemid 41434604)
58. Kaasik A, Rikk T, Piirsoo A, Zharkovsky T, Zharkovsky A (2005) Up-regulation of lysosomal cathepsin L and autophagy during neuronal death induced by reduced serum and potassium. Eur J Neurosci 22, 1023-1031. (Pubitemid 41395366)
59. Pickford F, Masliah E, Britschgi M, Lucin K, Narasimhan R, Jaeger PA, Small S, Spencer B, Rockenstein E, Levine B, Wyss-Coray T (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. (Pubitemid 351872337)
60. Chen D, Gao F, Li B, Wang H, Xu Y, Zhu C, Wang G (2010) Parkin mono-ubiquitinates Bcl-2 and regulates autophagy. J Biol Chem 285, 38214-38223.
61. Kirkin V, McEwan DG, Novak I, Dikic I (2009) A role for ubiquitin in selective autophagy. Mol Cell 34, 259-269.
62. Sutovsky P, Moreno RD, Ramalho-Santos J, Dominko T, Simerly C, Schatten G (1999) Ubiquitin tag for sperm mitochondria. Nature 402, 371-372. (Pubitemid 129544815)
63. Sarkar S, Ravikumar B, Rubinsztein DC (2009) Autophagic clearance of aggregate-prone proteins associated with neurodegeneration. Methods Enzymol 453, 83-110.
64. Iwata A, Riley BE, Johnston JA, Kopito RR (2005) HDAC6 and microtubules are required for autophagic degradation of aggregated huntingtin. J Biol Chem 280, 40282-40292. (Pubitemid 41779165)
65. Mizushima N, Yoshimori T (2007) How to interpret LC3 immunoblotting. Autophagy 3, 542-545. (Pubitemid 350060049)
66. Kov́acs AL, Reith A, Seglen PO (1982) Accumulation of autophagosomes after inhibition of hepatocytic protein degradation by vinblastine, leupeptin or a lysosomotropic amine. Exp Cell Res 137, 191-201. (Pubitemid 12146152)
67. He C, Klionsky DJ (2009) Regulation mechanisms and signaling pathways of autophagy. Annu Rev Genet 43, 67-93.
68. Perez M, Santa-Maria I, Gomez de Barreda E, Zhu X, Cuadros R, Cabrero JR, Sanchez-Madrid F, Dawson HN, Vitek MP, Perry G, Smith MA, Avila J (2009) Tau-an inhibitor of deacetylase HDAC6 function. J Neurochem 109, 1756-1766.
69. Ding H, Dolan PJ, Johnson GV (2008) Histone deacetylase 6 interacts with the microtubule-associated protein tau. J Neurochem 106, 2119-2130.
70. Hara T, Nakamura K, Matsui M, Yamamoto A, Nakahara Y, Suzuki-Migishima R, Yokoyama M, Mishima K, Saito I, Okano H, Mizushima N (2006) Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature 441, 885-889.
71. Komatsu M, Waguri S, Chiba T, Murata S, Iwata J, Tanida I, Ueno T, Koike M, Uchiyama Y, Kominami E, Tanaka K (2006) Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature 441, 880-884.
72. Ballatore C, Lee VM, Trojanowski JQ (2007) Tau-mediated neurodegeneration in Alzheimer's disease and related disorders. Nat Rev Neurosci 8, 663-672. (Pubitemid 47283144)