Hrd1 facilitates tau degradation and promotes neuron survival

Current Molecular Medicine

Volumn 12, Issue 2, 2012, Pages 138-152

  Shen, Y X ^a,b   Sun, A M ^b   Fang, S ^b,c   Feng, L J ^b   Li, Q ^b   Hou, H L ^a   Liu, C ^b   Wang, H P ^b   Shen, J L ^b   Luo, J ^d   Zhou, J N ^a,e  

^a UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^b ANHUI MEDICAL UNIVERSITY   (China)

^c UNIVERSITY OF MARYLAND BIOTECHNOLOGY INSTITUTE   (United States)

^d UNIVERSITY OF KENTUCKY   (United States)

^e UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

Author keywords

Alzheimer's disease; Hrd1; Tau; Ubiquitin proteasome pathway

Indexed keywords

ENDOPLASMIC RETICULUM MEMBRANE UBIQUITIN LIGASE E3; PROTEASOME; SMALL INTERFERING RNA; TAU PROTEIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ARTICLE; CELL STRUCTURE; CELL SURVIVAL; CONTROLLED STUDY; CYTOTOXICITY; ENZYME ACTIVITY; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA2 REGION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; MOLECULAR MECHANICS; NERVE CELL; NEUROPROTECTION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; UBIQUITINATION;

ALZHEIMER DISEASE; ANIMALS; CELL LINE; CELL SURVIVAL; HIPPOCAMPUS; HUMANS; NEURONS; PHOSPHORYLATION; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN BINDING; RATS; RATS, SPRAGUE-DAWLEY; TAU PROTEINS; UBIQUITIN-PROTEIN LIGASES;

EID: 84862910337     PISSN: 15665240     EISSN: 18755666     Source Type: Journal    
DOI: 10.2174/156652412798889009     Document Type: Article

References (65)

1. Boekhoorn K, Terwel D, Biemans B, et al. Improved longterm potentiation and memory in young tau-P301L transgenic mice before onset of hyperphosphorylation and tauopathy. J Neurosci 2006; 26: 3514-23.
2. Barghorn S, Davies P, Mandelkow E. Tau paired helical filaments from Alzheimer's disease brain and assembled in vitro are based on beta-structure in the core domain. Biochemistry 2004; 43: 1694-703.
3. Berriman J, Serpell LC, Oberg KA, et al. Tau filaments from human brain and from in vitro assembly of recombinant protein show cross-beta structure. Proc Natl Acad Sci USA 2003; 10: 9034-8.
4. Hutton M, Lendon CL, Rizzu P, et al. Association of missense and 5'-splice-site mutations in tau with the inherited dementia FTDP-17. Nature 1998; 393: 702-5.
5. Spillantini MG, Murrell JR, Goedert M, et al. Mutation in the tau gene in familial multiple system tauopathy with presenile dementia. Proc Natl Acad Sci USA 1998; 95: 7737-41.
6. Menendez J, Rodriguez-Navarro JA, Solano RM, et al. Suppression of Parkin enhances nigrostriatal and motor neuron lesion in mice over-expressing human-mutated tau protein. Hum Mol Genet 2006; 15: 2045-58.
7. Keller JN, Gee J, Ding Q. The proteasome in brain aging. Ageing Res Rev 2002; 1: 279-93.
8. Ciechanover A, Brundin P. The ubiquitin proteasome system in neurodegenerative diseases: sometimes the chicken, sometimes the egg. Neuron 2003; 40: 427-46.
9. Mori H, Kondo J, Ihara Y. Ubiquitin is a component of paired helical filaments in Alzheimer's disease. Science 1987; 235: 1641-4.
10. Goldbaum O, Oppermann M, Handschuh M, et al. Proteasome inhibition stabilizes tau inclusions in oligodendroglial cells that occur after treatment with okadaic acid. J Neurosci 2003; 23: 8872-80.
11. Cripps D, Thomas SN, Jeng Y, et al. Alzheimer diseasespecific conformation of hyperphosphorylated paired helical filament-Tau is polyubiquitinated through Lys-48, Lys-11, and Lys-6 ubiquitin conjugation. J Biol Chem 2006; 281: 10825-38.
12. Shimura H, Schwartz D, Gygi SP, Kosik KS. CHIP-Hsc70 complex ubiquitinates phosphorylated tau and enhances cell survival. J Biol Chem 2004; 279: 4869-76.
13. Petrucelli L, Dickson D, Kehoe K, et al. CHIP and Hsp70 regulate tau ubiquitination, degradation and aggregation. Hum Mol Genet 2004; 13: 703-14.
14. Babu JR, Geetha T, Wooten MW. Sequestosome 1/p62 shuttles polyubiquitinated tau for proteasomal degradation. J Neurochem 2005; 9: 192-203.
15. Dorval V, Fraser PE. Small ubiquitin-like modifier (SUMO) modification of natively unfolded proteins tau and alphasynuclein. J Biol Chem 2006; 281: 9919-24.
16. Gong CX, Grundke-Iqbal I, Iqbal K. Targeting tau protein in Alzheimer's disease. Drugs Aging 2010; 27: 351-65.
17. Schuberth C, Buchberger A. Membrane-bound Ubx2 recruits Cdc48 to ubiquitin ligases and their substrates to ensure efficient ER-associated protein degradation. Nat Cell Biol 2005; 7: 999-1006.
18. Neuber O, Jarosch E, Volkwein C, et al. Ubx2 links the Cdc48 complex to ER-associated protein degradation. Nat Cell Biol 2005; 7: 993-8.
19. Gauss R, Jarosch E, Sommer T, Hirsch C. A complex of Yos9p and the HRD ligase integrates endoplasmic reticulum quality control into the degradation machinery. Nat Cell Biol 2006; 8: 849-54.
20. Denic V, Quan EM, Weissman JS. A luminal surveillance complex that selects misfolded glycoproteins for ERassociated degradation. Cell 2006; 126: 349-59.
21. Carvalho P, Goder V, Rapoport TA. Distinct ubiquitin-ligase complexes define convergent pathways for the degradation of ER proteins. Cell. 2006; 126: 361-73.
22. Kaneko M, Ishiguro M, Niinuma Y, et al. Human HRD1 protects against ER stress-induced apoptosis through ERassociated degradation. FEBS Lett 2002; 532: 147-52.
23. Lindholm D, Wootz H, Korhonen L. ER stress and neurodegenerative diseases. Cell Death Differ 2006; 13: 385-92.
24. Uehara T, Nakamura T, Yao D, et al. S-nitrosylated proteindisulphide isomerase links protein misfolding to neurodegeneration. Nature 2006; 441: 513-7.
25. Hou HL, Shen YX, Zhu HY, et al. Alterations of hHrd1 expression are related to hyperphosphorylated tau in the hippocampus in Alzheimer's disease. J Neurosci Res 2006; 84: 1862-70.
26. Kaneko M, Koike H, Saito R, et al. Loss of HRD1-mediated protein degradation causes amyloid precursor protein accumulation and amyloid-beta generation. J Neurosci 2010; 30: 3924-32.
27. Saito R, Kaneko M, Okuma Y, Nomura Y. Correlation between decrease in protein levels of ubiquitin ligase HRD1 and amyloid-beta production. J Pharmacol Sci 2010; 113: 285-8.
28. Maeda T, Marutani T, Zou K, et al. An E3 ubiquitin ligase, Synoviolin, is involved in the degradation of immature nicastrin, and regulates the production of amyloid betaprotein. FEBS J 2009; 276: 5832-40.
29. Yang H, Zhong X, Ballar P, et al. Ubiquitin ligase Hrd1 enhances the degradation and suppresses the toxicity of polyglutamine-expanded huntingtin. Exp Cell Res 2007; 313: 538-50.
30. Zhong X, Shen Y, Ballar P, et al. AAA ATPase p97/valosincontaining protein interacts with gp78, a ubiquitin ligase for endoplasmic reticulum-associated degradation. J Biol Chem 2004; 279: 45676-84.
31. Chen G, Bower KA, Ma C, et al. Glycogen synthase kinase 3beta (GSK3beta) mediates 6-hydroxydopamine-induced neuronal death. FASEB J 2004; 18: 1162-4.
32. Salehi A, Van de Nes JA, Hofman MA, et al. Early cytoskeletal changes as shown by Alz-50 are not accompanied by decreased neuronal activity. Brain Res 1995; 678: 28-39.
33. McKhann G, Drachman D, Folstein M, et al. Clinical diagnosis of Alzheimer's disease: report of the NINCDSADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer's Disease. Neurology 1984; 34: 939-44.
34. Fang S, Ferrone M, Yang C, et al. The tumor autocrine motility factor receptor, gp78, is a ubiquitin protein ligase implicated in degradation from the endoplasmic reticulum. Proc Natl Acad Sci USA 2001; 98: 14422-7.
35. Wang H, Li Q, Shen Y, et al. The ubiquitin ligase Hrd1 promotes degradation of the Z variant alpha 1-antitrypsin and increases its solubility. Mol Cell Biochem 2010; 346: 137-45.
36. Keck S, Nitsch R, Grune T, Ullrich O. Proteasome inhibition by paired helical filament-tau in brains of patients with Alzheimer's disease. J Neurochem 2003; 85: 115-22.
37. Ueda K, Masliah E, Saitoh T, et al. Alz-50 recognizes a phosphorylated epitope of tau protein. J Neurosci 1990; 10: 3295-304.
38. McBain CJ, Traynelis SF, Dingledine R. Regional variation of extracellular space in the hippocampus. Science 1990; 249: 674-7.
39. Kuan CY, Schloemer AJ, Lu A, et al. Hypoxia-ischemia induces DNA synthesis without cell proliferation in dying neurons in adult rodent brain. J Neurosci 2004; 24: 10763-72.
40. Ding Q, Markesbery WR, Chen Q, et al. Ribosome dysfunction is an early event in Alzheimer's disease. J Neurosci 2005; 25: 9171-5.
41. Ando H, Watabe H, Valencia JC, et al. Fatty acids regulate pigmentation via proteasomal degradation of tyrosinase: a new aspect of ubiquitin-proteasome function. J Biol Chem 2004; 279: 15427-33.
42. Sharma M, Pampinella F, Nemes C, et al. Misfolding diverts CFTR from recycling to degradation: quality control at early endosomes. J Cell Biol. 2004; 164: 923-33.
43. Morales-Corraliza J, Mazzella MJ, Berger JD, et al. In vivo turnover of tau and APP metabolites in the brains of wild-type and Tg2576 mice: greater stability of sAPP in the betaamyloid depositing mice. PLoS One 2009; 4: e7134.
44. Oddo S, Billings L, Kesslak JP, et al. Abeta immunotherapy leads to clearance of early, but not late, hyperphosphorylated tau aggregates via the proteasome. Neuron 2004; 43: 321-32.
45. Yamada S, Niwa J, Ishigaki S, et al. Archaeal proteasomes effectively degrade aggregation-prone proteins and reduce cellular toxicities in mammalian cells. J Biol Chem 2006; 281: 23842-51.
46. Dickey CA, Kamal A, Lundgren K, et al. The high-affinity HSP90-CHIP complex recognizes and selectively degrades phosphorylated tau client proteins. J Clin Invest 2007; 117: 648-58.
47. Chau KW, Chan WY, Shaw PC, Chan HY. Biochemical investigation of Tau protein phosphorylation status and its solubility properties in Drosophila. Biochem Biophys Res Commun 2006; 346: 150-9.
48. Terwel D, Muyllaert D, Dewachter I, et al. Amyloid activates GSK-3beta to aggravate neuronal tauopathy in bigenic mice. Am J Pathol 2008; 172: 786-98.
49. Godemann R, Biernat J, Mandelkow E, Mandelkow EM. Phosphorylation of tau protein by recombinant GSK-3beta: pronounced phosphorylation at select Ser/Thr-Pro motifs but no phosphorylation at Ser262 in the repeat domain. FEBS Lett 1999; (454): 157-64.
50. Chatterjee S, Sang TK, Lawless GM, Jackson GR. Dissociation of Tau Toxicity and Phosphorylation: Role of GSK-3{beta}, MARK, and Cdk5 in a Drosophila Model. Hum Mol Genet 2009; 18: 164-77.
51. Kikkert M, Doolman R, Dai M, et al. Human HRD1 is an E3 ubiquitin ligase involved in degradation of proteins from the endoplasmic reticulum. J Biol Chem 2004; 279: 3525-34.
52. Hassink G, Kikkert M, van Voorden S, et al. TEB4 is a C4HC3 RING finger-containing ubiquitin ligase of the endoplasmic reticulum. Biochem J 2005; 388: 647-55.
53. Bays NW, Gardner RG, Seelig LP, et al. Hrd1p/Der3p is a membrane-anchored ubiquitin ligase required for ERassociated degradation. Nat Cell Biol 2001; 3: 24-9.
54. Swanson R, Locher M, Hochstrasser M. A conserved ubiquitin ligase of the nuclear envelope/endoplasmic reticulum that functions in both ER-associated and Matalpha2 repressor degradation. Genes Dev 2001; 15: 2660-74.
55. Ravid T, Kreft SG, Hochstrasser M. Membrane and soluble substrates of the Doa10 ubiquitin ligase are degraded by distinct pathways. EMBO J 2006; 25: 533-43.
56. Kadowaki H, Nishitoh H, Ichijo H. Survival and apoptosis signals in ER stress: the role of protein kinases. J Chem Neuroanat. 2004; 28: 93-100.
57. Shen Y, Ballar P, Apostolou A, et al. ER stress differentially regulates the stabilities of ERAD ubiquitin ligases and their substrates. Biochem Biophys Res Commun 2007; 352: 919-24.
58. Santacruz K, Lewis J, Spires T, et al. Tau suppression in a neurodegenerative mouse model improves memory function. Science. 2005; 309: 476-81.
59. Braak E, Braak H, Mandelkow EM. A sequence of cytoskeleton changes related to the formation of neurofibrillary tangles and neuropil threads. Acta Neuropathol 1994; 87: 554-67.
60. Luna-Munoz J, Chavez-Macias L, Garcia-Sierra F, Mena R. Earliest stages of tau conformational changes are related to the appearance of a sequence of specific phosphodependent tau epitopes in Alzheimer's disease. J Alzheimers Dis 2007; 12: 365-75.
61. Sahara N, Murayama M, Mizoroki T, et al. In vivo evidence of CHIP up-regulation attenuating tau aggregation. J Neurochem 2005; 94: 1254-63.
62. Bandyopadhyay B, Li G, Yin H, Kuret J. Tau aggregation and toxicity in a cell culture model of tauopathy. J Biol Chem 2007; 282: 16454-64.
63. Terwel D, Lasrado R, Snauwaert J, et al. Changed conformation of mutant Tau-P301L underlies the moribund tauopathy, absent in progressive, nonlethal axonopathy of Tau-4R/2N transgenic mice. J Biol Chem 2005; 280: 3963-73.
64. Thies E, Mandelkow EM. Missorting of tau in neurons causes degeneration of synapses that can be rescued by the kinase MARK2/Par-1. J Neurosci 2007; 27: 2896-907.
65. Park SY, Ferreira A. The generation of a 17 kDa neurotoxic fragment: an alternative mechanism by which tau mediates beta-amyloid-induced neurodegeneration. J Neurosci 2005; 25: 5365-75.