Cited by 336

The DOI matches its Crossref record; 22 of the 22 references it cites were found in a registry or an index.

Tau degradation: the ubiquitin-proteasome system versus the autophagy-lysosome system

Lee, Min Jae, Lee, Jung Hoon, Rubinsztein, David C.·2013·Progress in Neurobiology

Abstract

The ubiquitin-proteasome system (UPS) and the autophagy-lysosome system are two major protein quality control mechanisms in eukaryotic cells. While the UPS has been considered for decades as the critical regulator in the degradation of various aggregate-prone proteins, autophagy has more recently been shown to be an important pathway implicated in neuronal health and disease. The two hallmark lesions of Alzheimer's disease (AD) are extracellular β-amyloid plaques and intracellular tau tangles. It has been suggested that tau accumulation is pathologically more relevant to the development of neurodegeneration and cognitive decline in AD patients than β-amyloid plaques. Here, we review the UPS and autophagy-mediated tau clearance mechanisms and outline the biochemical connections between these two processes. In addition, we discuss pharmacological methods that target these degradation systems for the treatment and prevention of AD.

Overview

Integrity signals

Registry

Crossref · 10.1016/j.pneurobio.2013.03.001

Cites

22 of 22 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Verification

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Citations

Cites

Flagged first, then by citations

Research works printed but not linked: 95

  1. Aisen, 2009, Alzheimer's disease therapeutic research: the path forward, Alzheimer's Research and Therapy, 1, 2, 10.1186/alzrt2 · DOI
  2. Babu, 2008, Genetic inactivation of p62 leads to accumulation of hyperphosphorylated tau and neurodegeneration, Journal of Neurochemistry, 106, 107, 10.1111/j.1471-4159.2008.05340.x · DOI · Paper page
  3. Bednarski, 1996, Cytosolic proteolysis of tau by cathepsin D in hippocampus following suppression of cathepsins B and L, Journal of Neurochemistry, 67, 1846, 10.1046/j.1471-4159.1996.67051846.x · DOI
  4. Bence, 2001, Impairment of the ubiquitin–proteasome system by protein aggregation, Science, 292, 1552, 10.1126/science.292.5521.1552 · DOI
  5. Berger, 2006, Rapamycin alleviates toxicity of different aggregate-prone proteins, Human Molecular Genetics, 15, 433, 10.1093/hmg/ddi458 · DOI · Paper page
  6. Bernassola, 2008, The HECT family of E3 ubiquitin ligases: multiple players in cancer development, Cancer Cell, 14, 10, 10.1016/j.ccr.2008.06.001 · DOI · Paper page
  7. Besche, 2009, Isolation of mammalian 26S proteasomes and p97/VCP complexes using the ubiquitin-like domain from HHR23B reveals novel proteasome-associated proteins, Biochemistry, 48, 2538, 10.1021/bi802198q · DOI
  8. Brown, 2005, Proteasome or calpain inhibition does not alter cellular tau levels in neuroblastoma cells or primary neurons, Journal of Alzheimer's Disease, 7, 15, 10.3233/JAD-2005-7103 · DOI
  9. Cardozo, 2002, Proteasome-mediated degradation of tau proteins occurs independently of the chymotrypsin-like activity by a nonprocessive pathway, Archives of Biochemistry and Biophysics, 408, 103, 10.1016/S0003-9861(02)00493-9 · DOI
  10. Cripps, 2006, Alzheimer disease-specific conformation of hyperphosphorylated paired helical filament-Tau is polyubiquitinated through Lys-48, Lys-11, and Lys-6 ubiquitin conjugation, Journal of Biological Chemistry, 281, 10825, 10.1074/jbc.M512786200 · DOI · Paper page
  11. David, 2002, Proteasomal degradation of tau protein, Journal of Neurochemistry, 83, 176, 10.1046/j.1471-4159.2002.01137.x · DOI · Paper page
  12. de Vrij, 2004, Protein quality control in Alzheimer's disease by the ubiquitin proteasome system, Progress in Neurobiology, 74, 249, 10.1016/j.pneurobio.2004.10.001 · DOI
  13. Ding, 2001, Proteasome inhibition in oxidative stress neurotoxicity: implications for heat shock proteins, Journal of Neurochemistry, 77, 1010, 10.1046/j.1471-4159.2001.00302.x · DOI
  14. Ding, 2007, Linking of autophagy to ubiquitin–proteasome system is important for the regulation of endoplasmic reticulum stress and cell viability, American Journal of Pathology, 171, 513, 10.2353/ajpath.2007.070188 · DOI · Paper page
  15. Dolan, 2010, A caspase cleaved form of tau is preferentially degraded through the autophagy pathway, Journal of Biological Chemistry, 285, 21978, 10.1074/jbc.M110.110940 · DOI
  16. Egan, 2011, Phosphorylation of ULK1 (hATG1) by AMP-activated protein kinase connects energy sensing to mitophagy, Science, 331, 456, 10.1126/science.1196371 · DOI · Paper page
  17. Ethell, 2010, An amyloid-notch hypothesis for Alzheimer's disease, Neuroscientist, 16, 614, 10.1177/1073858410366162 · DOI
  18. Feuillette, 2005, Tau is not normally degraded by the proteasome, Journal of Neuroscience Research, 80, 400, 10.1002/jnr.20414 · DOI
  19. Finley, 2009, Recognition and processing of ubiquitin-protein conjugates by the proteasome, Annual Review of Biochemistry, 78, 477, 10.1146/annurev.biochem.78.081507.101607 · DOI · Paper page
  20. Giannakopoulos, 2003, Tangle and neuron numbers, but not amyloid load, predict cognitive status in Alzheimer's disease, Neurology, 60, 1495, 10.1212/01.WNL.0000063311.58879.01 · DOI · Paper page
  21. Glickman, 2002, The ubiquitin–proteasome proteolytic pathway: destruction for the sake of construction, Physiological Reviews, 82, 373, 10.1152/physrev.00027.2001 · DOI
  22. Gotz, 2001, Formation of neurofibrillary tangles in P301l tau transgenic mice induced by Abeta 42 fibrils, Science, 293, 1491, 10.1126/science.1062097 · DOI · Paper page
  23. Groll, 2000, A gated channel into the proteasome core particle, Natural Structural Biology, 7, 1062, 10.1038/80992 · DOI
  24. Hailey, 2010, Mitochondria supply membranes for autophagosome biogenesis during starvation, Cell, 141, 656, 10.1016/j.cell.2010.04.009 · DOI
  25. Hamano, 2008, Autophagic-lysosomal perturbation enhances tau aggregation in transfectants with induced wild-type tau expression, European Journal of Neuroscience, 27, 1119, 10.1111/j.1460-9568.2008.06084.x · DOI · Paper page
  26. Hayashi-Nishino, 2010, Electron tomography reveals the endoplasmic reticulum as a membrane source for autophagosome formation, Autophagy, 6, 301, 10.4161/auto.6.2.11134 · DOI
  27. Healy, 2006, UCHL-1 is not a Parkinson's disease susceptibility gene, Annals of Neurology, 59, 627, 10.1002/ana.20757 · DOI
  28. Hernandez, 2007, Tauopathies, Cellular and Molecular Life Sciences, 64, 2219, 10.1007/s00018-007-7220-x · DOI
  29. Hutter, 2008, Lack of evidence for an association between UCHL1 S18Y and Parkinson's disease, European Journal of Neurology, 15, 134, 10.1111/j.1468-1331.2007.02012.x · DOI
  30. Inoue, 2012, Macroautophagy deficiency mediates age-dependent neurodegeneration through a phospho-tau pathway, Molecular Neurodegeneration, 7, 48, 10.1186/1750-1326-7-48 · DOI · Paper page
  31. Jin, 2012, Usp14 deficiency increases tau phosphorylation without altering tau degradation or causing tau-dependent deficits, PLoS ONE, 7, e47884, 10.1371/journal.pone.0047884 · DOI
  32. Jinwal, 2010, Hsp70 ATPase modulators as therapeutics for Alzheimer's and other neurodegenerative diseases, Molecular and Cellular Pharmacology, 2, 43
  33. Khandelwal, 2011, Parkin mediates beclin-dependent autophagic clearance of defective mitochondria and ubiquitinated Abeta in AD models, Human Molecular Genetics, 20, 2091, 10.1093/hmg/ddr091 · DOI
  34. Kawaguchi, 1994, CAG expansions in a novel gene for Machado-Joseph disease at chromosome 14q32.1, Nature Genetics, 8, 221, 10.1038/ng1194-221 · DOI
  35. Keck, 2003, Proteasome inhibition by paired helical filament-tau in brains of patients with Alzheimer's disease, Journal of Neurochemistry, 85, 115, 10.1046/j.1471-4159.2003.01642.x · DOI · Paper page
  36. Keller, 2000, Impaired proteasome function in Alzheimer's disease, Journal of Neurochemistry, 75, 436, 10.1046/j.1471-4159.2000.0750436.x · DOI · Paper page
  37. Kimura, 2010, Regulatory mechanisms involved in the control of ubiquitin homeostasis, Journal of Biochemistry, 147, 793, 10.1093/jb/mvq044 · DOI
  38. King, 2006, Tau-dependent microtubule disassembly initiated by prefibrillar beta-amyloid, Journal of Cell Biology, 175, 541, 10.1083/jcb.200605187 · DOI
  39. Kisselev, 1999, Proteasome active sites allosterically regulate each other, suggesting a cyclical bite-chew mechanism for protein breakdown, Molecular Cell, 4, 395, 10.1016/S1097-2765(00)80341-X · DOI
  40. Kisselev, 2006, Importance of the different proteolytic sites of the proteasome and the efficacy of inhibitors varies with the protein substrate, Journal of Biological Chemistry, 281, 8582, 10.1074/jbc.M509043200 · DOI
  41. Komander, 2009, The emerging complexity of protein ubiquitination, Biochemical Society Transactions, 37, 937, 10.1042/BST0370937 · DOI · Paper page
  42. Komatsu, 2006, Loss of autophagy in the central nervous system causes neurodegeneration in mice, Nature, 441, 880, 10.1038/nature04723 · DOI · Paper page
  43. Korolchuk, 2009, Autophagy inhibition compromises degradation of ubiquitin–proteasome pathway substrates, Molecular Cell, 33, 517, 10.1016/j.molcel.2009.01.021 · DOI · Paper page
  44. Kruger, 2012, Autophagic degradation of tau in primary neurons and its enhancement by trehalose, Neurobiology of Aging, 33, 2291, 10.1016/j.neurobiolaging.2011.11.009 · DOI · Paper page
  45. Kudo, 1994, Alzheimer disease: correlation of cerebro-spinal fluid and brain ubiquitin levels, Brain Research, 639, 1, 10.1016/0006-8993(94)91757-4 · DOI
  46. Lam, 2000, Inhibition of the ubiquitin–proteasome system in Alzheimer's disease, Proceedings of the National Academy of Sciences of the United States of America, 97, 9902, 10.1073/pnas.170173897 · DOI
  47. Lee, 2010, Enhancement of proteasome activity by a small-molecule inhibitor of Usp14, Nature, 467, 179, 10.1038/nature09299 · DOI · Paper page
  48. Lee, 2011, Trimming of ubiquitin chains by proteasome-associated deubiquitinating enzymes, Molecular and Cellular Proteomics, 10, 10.1074/mcp.R110.003871 · DOI
  49. Lopez Salon, 2000, Defective ubiquitination of cerebral proteins in Alzheimer's disease, Journal of Neuroscience Research, 62, 302, 10.1002/1097-4547(20001015)62:2<302::AID-JNR15>3.0.CO;2-L · DOI
  50. Loring, 2001, A gene expression profile of Alzheimer's disease, DNA and Cell Biology, 20, 683, 10.1089/10445490152717541 · DOI
  51. Luo, 2012, Bim Inhibits Autophagy by Recruiting Beclin 1 to Microtubules, Molecular Cell, 47, 359, 10.1016/j.molcel.2012.05.040 · DOI
  52. Majumder, 2011, Inducing autophagy by rapamycin before, but not after, the formation of plaques and tangles ameliorates cognitive deficits, PLoS ONE, 6, e25416, 10.1371/journal.pone.0025416 · DOI · Paper page
  53. Matsumoto, 2010, K11-linked polyubiquitination in cell cycle control revealed by a K11 linkage-specific antibody, Molecular Cell, 39, 477, 10.1016/j.molcel.2010.07.001 · DOI
  54. Mishto, 2006, Immunoproteasome and LMP2 polymorphism in aged and Alzheimer's disease brains, Neurobiology of Aging, 27, 54, 10.1016/j.neurobiolaging.2004.12.004 · DOI
  55. Mizushima, 2010, Methods in mammalian autophagy research, Cell, 140, 313, 10.1016/j.cell.2010.01.028 · DOI · Paper page
  56. Moreau, 2012, Arf6 promotes autophagosome formation via effects on phosphatidylinositol 4,5-bisphosphate and phospholipase D, Journal of Cell Biology, 196, 483, 10.1083/jcb.201110114 · DOI
  57. Moreau, 2011, Autophagosome precursor maturation requires homotypic fusion, Cell, 146, 303, 10.1016/j.cell.2011.06.023 · DOI
  58. Nandi, 2006, The ubiquitin–proteasome system, Journal of Biosciences, 31, 137, 10.1007/BF02705243 · DOI
  59. Nijman, 2005, A genomic and functional inventory of deubiquitinating enzymes, Cell, 123, 773, 10.1016/j.cell.2005.11.007 · DOI · Paper page
  60. Nixon, 2011, Autophagy failure in Alzheimer's disease--locating the primary defect, Neurobiology of Disease, 43, 38, 10.1016/j.nbd.2011.01.021 · DOI · Paper page
  61. Nussbaum, 1998, Cleavage motifs of the yeast 20S proteasome beta subunits deduced from digests of enolase 1, Proceedings of the National Academy of Sciences of the United States of America, 95, 12504, 10.1073/pnas.95.21.12504 · DOI
  62. Pickart, 2001, Mechanisms underlying ubiquitination, Annual Review of Biochemistry, 70, 503, 10.1146/annurev.biochem.70.1.503 · DOI · Paper page
  63. Pickart, 2004, Proteasomes and their kin: proteases in the machine age, Nature Reviews Molecular Cell Biology, 5, 177, 10.1038/nrm1336 · DOI
  64. Ravikumar, 2010, Regulation of mammalian autophagy in physiology and pathophysiology, Physiological Reviews, 90, 1383, 10.1152/physrev.00030.2009 · DOI
  65. Reggiori, 2005, Autophagosomes: biogenesis from scratch?, Current Opinion in Cell Biology, 17, 415, 10.1016/j.ceb.2005.06.007 · DOI
  66. Roberson, 2007, Reducing endogenous tau ameliorates amyloid beta-induced deficits in an Alzheimer's disease mouse model, Science, 316, 750, 10.1126/science.1141736 · DOI · Paper page
  67. Rodriguez-Navarro, 2010, Trehalose ameliorates dopaminergic and tau pathology in parkin deleted/tau overexpressing mice through autophagy activation, Neurobiology of Disease, 39, 423, 10.1016/j.nbd.2010.05.014 · DOI · Paper page
  68. Rubinsztein, 2012, Autophagy modulation as a potential therapeutic target for diverse diseases, Nature Reviews Drug Discovery, 11, 709, 10.1038/nrd3802 · DOI
  69. Sakamoto, 2001, Protacs: chimeric molecules that target proteins to the Skp1-Cullin-F box complex for ubiquitination and degradation, Proceedings of the National Academy of Sciences of the United States of America, 98, 8554, 10.1073/pnas.141230798 · DOI · Paper page
  70. Sarkar, 2007, Trehalose, a novel mTOR-independent autophagy enhancer, accelerates the clearance of mutant huntingtin and alpha-synuclein, Journal of Biological Chemistry, 282, 5641, 10.1074/jbc.M609532200 · DOI · Paper page
  71. Schulman, 2009, Ubiquitin-like protein activation by E1 enzymes: the apex for downstream signalling pathways, Nature Reviews Molecular Cell Biology, 10, 319, 10.1038/nrm2673 · DOI
  72. See, 2010, Genetic causes of frontotemporal degeneration, Journal of Geriatric Psychiatry and Neurology, 23, 260, 10.1177/0891988710383574 · DOI
  73. Selkoe, 2001, Alzheimer's disease: genes, proteins, and therapy, Physiological Reviews, 81, 741, 10.1152/physrev.2001.81.2.741 · DOI · Paper page
  74. Shimada, 2012, Long-term oral lithium treatment attenuates motor disturbance in tauopathy model mice: implications of autophagy promotion, Neurobiology of Disease, 46, 101, 10.1016/j.nbd.2011.12.050 · DOI
  75. Shimura, 2004, CHIP-Hsc70 complex ubiquitinates phosphorylated tau and enhances cell survival, Journal of Biological Chemistry, 279, 4869, 10.1074/jbc.M305838200 · DOI
  76. Simonsen, 2008, Promoting basal levels of autophagy in the nervous system enhances longevity and oxidant resistance in adult Drosophila, Autophagy, 4, 176, 10.4161/auto.5269 · DOI · Paper page
  77. Small, 2008, Linking Abeta and tau in late-onset Alzheimer's disease: a dual pathway hypothesis, Neuron, 60, 534, 10.1016/j.neuron.2008.11.007 · DOI · Paper page
  78. Tai, 2008, Ubiquitin, the proteasome and protein degradation in neuronal function and dysfunction, Nature Reviews Neuroscience, 9, 826, 10.1038/nrn2499 · DOI · Paper page
  79. Tan, 2008, Lysine 63-linked ubiquitination promotes the formation and autophagic clearance of protein inclusions associated with neurodegenerative diseases, Human Molecular Genetics, 17, 431, 10.1093/hmg/ddm320 · DOI
  80. Tan, 2007, Mutant ubiquitin found in Alzheimer's disease causes neuritic beading of mitochondria in association with neuronal degeneration, Cell Death and Differentiation, 14, 1721, 10.1038/sj.cdd.4402180 · DOI
  81. Tseng, 2008, Abeta inhibits the proteasome and enhances amyloid and tau accumulation, Neurobiology of Aging, 29, 1607, 10.1016/j.neurobiolaging.2007.04.014 · DOI · Paper page
  82. van Leeuwen, 1998, Frameshift mutants of beta amyloid precursor protein and ubiquitin-B in Alzheimer's and Down patients, Science, 279, 242, 10.1126/science.279.5348.242 · DOI
  83. von Bergen, 2000, Assembly of tau protein into Alzheimer paired helical filaments depends on a local sequence motif ((306)VQIVYK(311)) forming beta structure, Proceedings of the National Academy of Sciences of the United States of America, 97, 5129, 10.1073/pnas.97.10.5129 · DOI · Paper page
  84. Vossel, 2010, Tau reduction prevents Abeta-induced defects in axonal transport, Science, 330, 198, 10.1126/science.1194653 · DOI · Paper page
  85. Wang, 2010, Proteolytic processing of tau, Biochemical Society Transactions, 38, 955, 10.1042/BST0380955 · DOI
  86. Wang, 2010, Synergy and antagonism of macroautophagy and chaperone-mediated autophagy in a cell model of pathological tau aggregation, Autophagy, 6, 182, 10.4161/auto.6.1.10815 · DOI · Paper page
  87. Wei, 2008, JNK1-mediated phosphorylation of Bcl-2 regulates starvation-induced autophagy, Molecular Cell, 30, 678, 10.1016/j.molcel.2008.06.001 · DOI · Paper page
  88. Wray, 2009, Linking amyloid and tau pathology in Alzheimer's disease: the role of membrane cholesterol in Abeta-mediated tau toxicity, Journal of Neuroscience, 29, 9665, 10.1523/JNEUROSCI.2234-09.2009 · DOI
  89. Ye, 2009, Building ubiquitin chains: E2 enzymes at work, Nature Reviews Molecular Cell Biology, 10, 755, 10.1038/nrm2780 · DOI · Paper page
  90. Yorimitsu, 2005, Autophagy: molecular machinery for self-eating, Cell Death and Differentiation, 12, 1542, 10.1038/sj.cdd.4401765 · DOI
  91. Zhang, 2005, Microtubule-associated protein tau is a substrate of ATP/Mg(2+)-dependent proteasome protease system, Journal of Neural Transmission, 112, 547, 10.1007/s00702-004-0196-x · DOI
  92. Zhao, 2007, FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells, Cell Metabolism, 6, 472, 10.1016/j.cmet.2007.11.004 · DOI · Paper page
  93. Zheng, 2009, Interplay between the ubiquitin–proteasome system and autophagy in proteinopathies, International Journal of Physiology, Pathophysiology and Pharmacology, 1, 127
  94. Zhu, 2010, Proteasome inhibitors activate autophagy as a cytoprotective response in human prostate cancer cells, Oncogene, 29, 451, 10.1038/onc.2009.343 · DOI · Paper page
  95. Zhu, 2004, Oxidative stress signalling in Alzheimer's disease, Brain Research, 1000, 32, 10.1016/j.brainres.2004.01.012 · DOI

Cited by

Sorted by citations

Metadata

Authors
Lee, M. J., Lee, J. H., & Rubinsztein, D. C.
Venue
Progress in Neurobiology
Publisher
Elsevier BV
Published
2013-06
Volume
105
Pages
49-59
ISSN
0301-0082
Cited by
336
References
22
Language
en
Funders
  • Tau Consortium
  • Medical Research Council
  • Ministry of Health and Welfare (A111227)
  • National Research Foundation of Korea
  • Ministry of Education, Science and Technology (2012-0003217, 2012-0009484, 2012R1A6A3A01039788)
  • Wellcome Trust

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review