Alzheimer's associated variant ubiquitin causes inhibition of the 26S proteasome and chaperone expression

Journal of Neurochemistry

Volumn 86, Issue 2, 2003, Pages 394-404

  Hope, Andrew D ^a   De Silva, Rohan ^a   Fischer, David F ^b   Hol, Elly M ^b   Van Leeuwen, Fred W ^b   Lees, Andrew J ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

Author keywords

Alzheimer's disease; Heat shock proteins; Oxidative stress; UBB+1; Ubiquitin

Indexed keywords

CHAPERONE; HEAT SHOCK PROTEIN; PROTEOME; TERT BUTYL HYDROPEROXIDE; UBIQUITIN;

ALZHEIMER DISEASE; ARTICLE; CELL ASSAY; CELL PROTECTION; CELL STRAIN; CONTROLLED STUDY; EXPERIMENTAL MODEL; HUMAN; HUMAN CELL; NEUROBLASTOMA CELL; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN SYNTHESIS INHIBITION;

ALZHEIMER DISEASE; CANAVANINE; CELL SURVIVAL; ENZYME INHIBITORS; GENE EXPRESSION REGULATION; GREEN FLUORESCENT PROTEINS; HEAT-SHOCK PROTEINS; HUMANS; LUMINESCENT PROTEINS; MOLECULAR CHAPERONES; NEUROBLASTOMA; OXIDATIVE STRESS; PEPTIDE HYDROLASES; PROTEASOME ENDOPEPTIDASE COMPLEX; RNA, MESSENGER; TRANSFECTION; TRANSGENES; TUMOR CELLS, CULTURED; UBIQUITIN;

EID: 0038155122     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.2003.01844.x     Document Type: Article

References (65)

1. Auluck P. K., Chan H. Y., Trojanowski J. Q., Lee V. M. and Bonini N. M. (2002) Chaperone suppression of α-synuclein toxicity in a Drosophila model for Parkinson's disease. Science 295, 865-868.
2. Benaroudj N., Lee D. H. and Goldberg A. L. (2001) Trehalose accumulation during cellular stress protects cells and cellular proteins from damage by oxygen radicals. J. Biol. Chem. 276, 24261-24267.
3. Bence N. F., Sampat R. M. and Kopito R. R. (2001) Impairment of the ubiquitin-proteasome system by protein aggregation. Science 292, 1552-1555.
4. Bercovich B., Stancovski I., Mayer A., Blumenfeld N., Laszlo A., Schwartz A. L. and Ciechanover A. (1997) Ubiquitin-dependent degradation of certain protein substrates in vitro requires the molecular chaperone Hsc70. J. Biol. Chem. 272, 9002-9010.
5. Bonini N. M. (2002) Chaperoning brain degeneration. Proc. Natl Acad. Sci. USA 99, 16407-16411.
6. Bukau B. and Horwich A. L. (1998) The Hsp70 and Hsp60 chaperone machines. Cell 92, 351-366.
7. Bush K. T., Goldberg A. L. and Nigam S. K. (1997) Proteasome inhibition leads to a heat-shock response, induction of endoplasmic reticulum chaperones, and thermotolerance. J. Biol. Chem. 272, 9086-9092.
8. Chan H. Y., Warrick J. M., Gray-Board G. L., Paulson H. L. and Bonini N. M. (2000) Mechanisms of chaperone suppression of polyglutamine disease: selectivity, synergy and modulation of protein solubility in Drosophila. Hum. Mol. Genet. 9, 2811-2820.
9. Ciechanover A., Orian A. and Schwartz A. L. (2000) Ubiquitin-mediated proteolysis: biological regulation via destruction. Bioessays 22, 442-451.
10. Cummings C. J., Sun Y., Opal P., Antalffy B., Mestril R., Orr H. T., Dillmann W. H. and Zoghbi H. Y. (2001) Overexpression of inducible HSP70 chaperone suppresses neuropathology and improves motor function in SCA1 mice. Hum. Mol. Genet. 10, 1511-1518.
11. Dantuma N. P., Lindsten K., Glas R., Jellne M. and Masucci M. G. (2000) Short-lived green fluorescent proteins for quantifying ubiquitin/proteasome-dependent proteolysis in living cells. Nat. Biotechnol. 18, 538-543.
12. De Vrij F. M., Sluijs J. A., Gregori L., Fischer D. F., Hermens W. T., Goldgaber D., Verhaagen J., Van Leeuwen F. W. and Hol E. M. (2001) Mutant ubiquitin expressed in Alzheimer's disease causes neuronal death. Faseb J. 15, 2680-2688.
13. Demand J., Alberti S., Patterson C. and Hohfeld J. (2001) Cooperation of a ubiquitin domain protein and an E3 ubiquitin ligase during chaperone/proteasome coupling. Curr. Biol. 11, 1569-1577.
14. Dou F., Netzer W. J., Tanemura K., Li F., Hartl F. U., Takashima A., Gouras G. K., Greengard P. and Xu H. (2003) Chaperones increase association of tau protein with microtubules. Proc. Natl Acad. Sci. USA 100, 721-726.
15. Fergusson J., Landon M., Lowe J., Ward L., van Leeuwen F. W. and Mayer R. J. (2000) Neurofibrillary tangles in progressive supranuclear palsy brains exhibit immunoreactivity to frameshift mutant ubiquitin-B protein. Neurosci. Lett. 279, 69-72.
16. Finley D., Sadis S., Monia B. P., Boucher P., Ecker D. J., Crooke S. T. and Chau V. (1994) Inhibition of proteolysis and cell cycle progression in a multiubiquitination-deficient yeast mutant. Mol. Cell. Biol. 14, 5501-5509.
17. French B. A., van Leeuwen F., Riley N. E., Yuan Q. X., Bardag-Gorce F., Gaal K., Lue Y. H., Marceau N. and French S. W. (2001) Aggresome formation in liver cells in response to different toxic mechanisms: role of the ubiquitin-proteasome pathway and the frameshift mutant of ubiquitin. Exp. Mol. Pathol. 71, 241-246.
18. Frydman J. and Hohfeld J. (1997) Chaperones get in touch: the Hip-Hop connection. Trends Biochem. Sci. 22, 87-92.
19. Gilon T., Chomsky O. and Kulka R. G. (1998) Degradation signals for ubiquitin system proteolysis in Saccharomyces cerevisiae. EMBO J. 17, 2759-2766.
20. Glickman M. H., Rubin D. M., Coux O., Wefes I., Pfeifer G., Cjeka Z., Baumeister W., Fried V. A. and Finley D. (1998) A subcomplex of the proteasome regulatory particle required for ubiquitin-conjugate degradation and related to the COP9-signalosome and eIF3. Cell 94, 615-623.
21. Grundke-Iqbal I., Iqbal K., Tung Y. C., Quinlan M., Wisniewski H. M. and Binder L. I. (1986) Abnormal phosphorylation of the microtubule-associated protein tau (tau) in Alzheimer cytoskeletal pathology. Proc. Natl Acad. Sci. USA 83, 4913-4917.
22. Hartl F. U. (1996) Molecular chaperones in cellular protein folding. Nature 381, 571-579.
23. Hohfeld J. (1998) Regulation of the heat shock conjugate Hsc70 in the mammalian cell: the characterization of the anti-apoptotic protein BAG-1 provides novel insights. Biol. Chem. 379, 269-274.
24. Huang H. C., Sherman M. Y., Kandror O. and Goldberg A. L. (2001) The molecular chaperone DnaJ is required for the degradation of a soluble abnormal protein in Escherichia coli. J. Biol. Chem. 276, 3920-3928.
25. Inai Y. and Nishikimi M. (2002) Increased degradation of oxidized proteins in yeast defective in 26 S proteasome assembly. Arch. Biochem. Biophys. 404, 279-284.
26. Iqbal K., Grundke-Iqbal I., Zaidi T., Merz P. A., Wen G. Y., Shaikh S. S., Wisniewski H. M., Alafuzoff I. and Winblad B. (1986) Defective brain microtubule assembly in Alzheimer's disease. Lancet 2, 421-426.
27. Johnston J. A., Ward C. L. and Kopito R. R. (1998) Aggresomes: a cellular response to misfolded proteins. J. Cell Biol. 143, 1883-1898.
28. Kawazoe Y., Nakai A., Tanabe M. and Nagata K. (1998) Proteasome inhibition leads to the activation of all members of the heat-shock-factor family. Eur. J. Biochem. 255, 356-362.
29. Keller J. N., Hanni K. B. and Markesbery W. R. (2000a) Impaired proteasome function in Alzheimer's disease. J. Neurochem. 75, 436-439.
30. Keller J. N., Huang F. F., Zhu H., Yu J., Ho Y. S. and Kindy T. S. (2000b) Oxidative stress-associated impairment of proteasome activity during ischemia-reperfusion injury. J. Cereb. Blood Flow Metab. 20, 1467-1473.
31. Kim D., Kim S. H. and Li G. C. (1999) Proteasome inhibitors MG132 and lactacystin hyperphosphorylate HSF1 and induce Hsp70 and Hsp27 expression. Biochem. Biophys. Res. Commun. 254, 264-268.
32. Lam Y. A., Pickart C. M., Alban A., Landon M., Jamieson C., Ramage R., Mayer R. J. and Layfield R. (2000) Inhibition of the ubiquitin-proteasome system in Alzheimer's disease. Proc. Natl Acad. Sci. USA 97, 9902-9906.
33. Lee D. H., Sherman M. Y. and Goldberg A. L. (1996) Involvement of the molecular chaperone Ydj1 in the ubiquitin-dependent degradation of short-lived and abnormal proteins in Saccharomyces cerevisiae. Mol. Cell. Biol. 16, 4773-4781.
34. Lee D. H. and Goldberg A. L. (1998) Proteasome inhibitors cause induction of heat shock proteins and trehalose, which together confer thermotolerance in Saccharomyces cerevisiae. Mol. Cell. Biol. 18, 30-38.
35. van Leeuwen F. W., de Kleijn D. P., van den Hurk H. H., Neubauer A., Sonnemans M. A., Sluijs J. A., Koycu S., Ramdjielal R. D., Salehi A., Martens G. J., Grosveld F. G., Peter J., Burbach H. and Hol E. M. (1998) Frameshift mutants of β-amyloid precursor protein and ubiquitin-B in Alzheimer's and Down's patients. Science 279, 242-247.
36. Lindsten K., De Vrij F. M., Verhoef L. G., Fischer D. F., Van Leeuwen F. W., Hol E. M., Masucci M. G. and Dantuma N. P. (2002) Mutant ubiquitin found in neurodegenerative disorders is a ubiquitin fusion degradation substrate that blocks proteasomal degradation. J. Cell Biol. 157, 417-427.
37. Lopez Salon M., Morelli L., Castano E. M., Soto E. F. and Pasquini J. M. (2000) Defective ubiquitination of cerebral proteins in Alzheimer's disease. J. Neurosci. Res. 62, 302-310.
38. Lovell M. A., Ehmann W. D., Butler S. M. and Markesbery W. R. (1995) Elevated thiobarbituric acid-reactive substances and antioxidant enzyme activity in the brain in Alzheimer's disease. Neurology 45, 1594-1601.
39. Luders J., Demand J. and Hohfeld J. (2000) The ubiquitin-related BAG-1 provides a link between the molecular chaperones Hsc70/Hsp70 and the proteasome. J. Biol. Chem. 275, 4613-4617.
40. McNaught K. S., Belizaire R., Jenner P., Olanow C. W. and Isacson O. (2002) Selective loss of 20S proteasome α-subunits in the substantia nigra pars compacta in Parkinson's disease. Neurosci. Lett. 326, 155-158.
41. McNaught K. S. and Jenner P. (2001) Proteasomal function is impaired in substantia nigra in Parkinson's disease. Neurosci. Lett. 297, 191-194.
42. McPhaul L. W., Wang J., Hol E. M., Sonnemans M. A., Riley N., Nguyen V., Yuan Q. X., Lue Y. H., Van Leeuwen F. W. and French S. W. (2002) Molecular misreading of the ubiquitin B gene and hepatic mallory body formation. Gastroenterology 122, 1878-1885.
43. Mecocci P., MacGarvey U. and Beal M. F. (1994) Oxidative damage to mitochondrial DNA is increased in Alzheimer's disease. Ann. Neurol. 36, 747-751.
44. Meriin A. B., Gabai V. L., Yaglom J., Shifrin V. I. and Sherman M. Y. (1998) Proteasome inhibitors activate stress kinases and induce Hsp72. Diverse effects on apoptosis. J. Biol. Chem. 273, 6373-6379.
45. Morocz M., Kalman J., Juhasz A., Sinko I. I., McGlynn A. P., Downes C. S., Janka Z. and Rasko I. I. (2002) Elevated levels of oxidative DNA damage in lymphocytes from patients with Alzheimer's disease (1). Neurobiol. Aging 23, 47-53.
46. Murata S., Minami Y., Minami M., Chiba T. and Tanaka K. (2001) CHIP is a chaperone-dependent E3 ligase that ubiquitylates unfolded protein. EMBO Rep. 2, 1133-1138.
47. Papasozomenos S. C. (1996) Heat shock induces rapid dephosphorylation of tau in both female and male rats followed by hyperphosphorylation only in female rats: implications for Alzheimer's disease. J. Neurochem. 66, 1140-1149.
48. Petrucelli L., O'Farrell C., Lockhart P. J., Baptista M., Kehoe K., Vink L., Choi P., Wolozin B., Farrer M., Hardy J. and Cookson M. R. (2002) Parkin protects against the toxicity associated with mutant α-synuclein: proteasome dysfunction selectively affects catecholaminergic neurons. Neuron 36, 1007-1019.
49. Pickart C. M. (1997) Targeting of substrates to the 26S proteasome. FasebJ 11, 1055-1066.
50. Riley N. E., Li J., Worrall S., Rothnagel J. A., Swagell C., van Leeuwen F. W. and French S. W. (2002) The mallory body as an aggresome: in vitro studies. Exp. Mol. Pathol. 72, 17-23.
51. Rockwell P., Yuan H., Magnusson R. and Figueiredo-Pereira M. E. (2000) Proteasome inhibition in neuronal cells induces a proinflammatory response manifested by upregulation of cyclo-oxygenase-2, its accumulation as ubiquitin conjugates, and production of the prostaglandin PGE(2). Arch. Biochem. Biophys. 374, 325-333.
52. Ryan M. C., Shooter E. M. and Notterpek L. (2002) Aggresome formation in neuropathy models based on peripheral myelin protein 22 mutations. Neurobiol. Dis. 10, 109-118.
53. Savel'ev A. S., Novikova L. A., Kovaleva I. E., Luzikov V. N., Neupert W. and Langer T (1998) ATP-dependent proteolysis in mitochondria. m-AAA protease and PIM1 protease exert overlapping substrate specificities and cooperate with the mtHsp70 system. J. Biol. Chem. 273, 20596-20602.
54. Sayre L. M., Perry G., Harris P. L., Liu Y., Schubert K. A. and Smith M. A. (2000) In situ oxidative catalysis by neurofibrillary tangles and senile plaques in Alzheimer's disease: a central role for bound transition metals. J. Neurochem. 74, 270-279.
55. Shanavas A. and Papasozomenos S. C. (2000) tau kinases in the rat heat shock model: possible implications for Alzheimer disease. Proc. Natl Acad. Sci. USA 97, 14139-14144.
56. Shringarpure R., Grune T., Mehlhase J. and Davies K. J. (2003) Ubiquitin conjugation is not required for the degradation of oxidized proteins by proteasome. J. Biol. Chem. 278, 311-318.
57. Smith C. D., Carney J. M., Starke-Reed P. E., Oliver C. N., Stadtman E. R., Floyd R. A. and Markesbery W. R. (1991) Excess brain protein oxidation and enzyme dysfunction in normal aging and in Alzheimer's disease. Proc. Natl Acad. Sci. USA 88, 10540-10543.
58. Stangl K., Gunther C., Frank T., Lorenz M., Meiners S., Ropke T., Stelter L., Moobed M., Baumann G., Kloetzel P. M. and Stangl V. (2002) Inhibition of the ubiquitin-proteasome pathway induces differential heat-shock protein response in cardiomyocytes and renders early cardiac protection. Biochem. Biophys. Res. Commun. 291, 542-549.
59. Straus D. B., Walter W. A. and Gross C. A. (1988) Escherichia coli heat shock gene mutants are defective in proteolysis. Genes Dev. 2, 1851-1858.
60. Tsirigotis M., Zhang M., Chiu R. K., Wouters B. G. and Gray D. A. (2001) Sensitivity of mammalian cells expressing mutant ubiquitin to protein-damaging agents. J. Biol. Chem. 276, 46073-46078.
61. Wagner I., Arlt H., van Dyck L., Langer T and Neupert W. (1994) Molecular chaperones cooperate with PIM1 protease in the degradation of misfolded proteins in mitochondria. EMBO J. 13, 5135-5145.
62. Warrick J. M., Chan H. Y., Gray-Board G. L., Chai Y., Paulson H. L. and Bonini N. M. (1999) Suppression of polyglutamine-mediated neurodegeneration in Drosophila by the molecular chaperone HSP70. Nat. Genet. 23, 425-428.
63. Wu S. S., De Chadarevian J. P., McPhaul L., Riley N. E., Van Leeuwen F. W. and French S. W. (2002) Coexpression and accumulation of ubiquitin + 1 and ZZ proteins in livers of children with α(1)-antitrypsin deficiency. Pediatr. Dev. Pathol. 5, 293-298.
64. Yoo B. C., Kim S. H., Cairns N., Fountoulakis M. and Lubec G. (2001) Deranged expression of molecular chaperones in brains of patients with Alzheimer's disease. Biochem. Biophys. Res. Commun. 280, 249-258.
65. Zhou M., Wu X. and Ginsberg H. N. (1996) Evidence that a rapidly turning over protein, normally degraded by proteasomes, regulates hsp72 gene transcription in HepG2 cells. J. Biol. Chem. 271, 24769-24775.