Roles of molecular chaperones in protein misfolding diseases

Seminars in Cell and Developmental Biology

Volumn 15, Issue 1, 2004, Pages 17-29

  Barral, José M ^a   Broadley, Sarah A ^a   Schaffar, Gregor ^a   Hartl, F Ulrich ^a  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

Author keywords

Amyloid; Misfolding diseases; Molecular chaperones; Polyglutamine diseases; Ubiquitin proteasome system

Indexed keywords

ACYL COENZYME A; ALPHA SYNUCLEIN; AMYLOID; CHAPERONE; CHAPERONIN; COLLAGEN; CRYSTALLIN; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 60; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; HUNTINGTIN; KERATIN; LOW DENSITY LIPOPROTEIN RECEPTOR; OXIDOREDUCTASE; PHENYLALANINE 4 MONOOXYGENASE; POLYPEPTIDE; PREALBUMIN; PRION PROTEIN; PROTEASOME; PROTEIN; PROTEIN SUBUNIT; TRANSMEMBRANE CONDUCTANCE REGULATOR; UBIQUITIN;

ALZHEIMER DISEASE; AMINO ACID SEQUENCE; BARDET BIEDL SYNDROME; BIOACCUMULATION; CREUTZFELDT JAKOB DISEASE; CYSTIC FIBROSIS; CYTOSOL; DEGENERATIVE DISEASE; DISEASE COURSE; ENDOPLASMIC RETICULUM; EPIDERMOLYSIS BULLOSA SIMPLEX; EUBACTERIUM; EUKARYOTE; FAMILIAL AMYLOIDOSIS; FAMILIAL HYPERCHOLESTEROLEMIA; GENETIC CODE; HEREDITARY MOTOR SENSORY NEUROPATHY; HUMAN; HYPERTROPHIC CARDIOMYOPATHY; MCKUSICK KAUFMAN SYNDROME; MOLECULE; MUTATION; MYOPATHY; NEUROTOXICITY; NONHUMAN; OPEN READING FRAME; OSTEOGENESIS IMPERFECTA; PARKINSON DISEASE; PHENYLKETONURIA; PROTEIN AGGREGATION; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; REVIEW; SEQUENCE HOMOLOGY; SPASTIC PARAPLEGIA; SYNDROME; TOXICITY;

EID: 0842303213     PISSN: 10849521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.semcdb.2003.12.010     Document Type: Review

References (127)

1. Dobson C.M. Protein misfolding, evolution and disease. Trends Biochem. Sci. 24:1999;329-332.
2. Radford S.E. Protein folding: progress made and promises ahead. Trends Biochem. Sci. 25:2000;611-618.
3. Ellis R.J. Macromolecular crowding: an important but neglected aspect of the intracellular environment. Curr. Opin. Struct. Biol. 11:2001;114-119.
4. Netzer W.J., Hartl F.U. Protein folding in the cytosol: chaperonin-dependent and -independent mechanisms. Trends Biochem. Sci. 23:1998;68-73.
5. Frydman J., Hartl F.U. Principles of chaperone-assisted protein folding: differences between in vitro and in vivo mechanisms. Science. 272:1996;1497-1502.
6. Ellis R.J. Proteins as molecular chaperones. Nature. 328:1987;378-379.
7. Hartl F.U., Hayer-Hartl M. Molecular chaperones in the cytosol: from nascent chain to folded protein. Science. 295:2002;1852-1858.
8. Hartl F.U. Molecular chaperones in cellular protein folding. Nature. 381:1996;571-579.
9. Ellis R.J., Hart F.U. Folding and binding: problems with proteins. Curr. Opin. Struct. Biol. 10:2000;13-15.
10. Braig K. Chaperonins. Curr. Opin. Struct. Biol. 8:1998;159-165.
11. Klumpp M., Baumeister W., Essen L.O. Structure of the substrate binding domain of the thermosome, an archaeal group II chaperonin. Cell. 91:1997;263-270.
12. Ditzel L., Lowe J., Stock D., Stetter K.O., Huber H., Huber R.et al. Crystal structure of the thermosome, the archaeal chaperonin and homolog of CCT. Cell. 93:1998;125-138.
13. Gutsche I., Holzinger J., Rauh N., Baumeister W., May R.P. ATP-induced structural change of the thermosome is temperature-dependent. J. Struct. Biol. 135:2001;139-146.
14. Frydman J., Nimmesgern E., Ohtsuka K., Hartl F.U. Folding of nascent polypeptide chains in a high molecular mass assembly with molecular chaperones. Nature. 370:1994;111-117.
15. Siegers K., Bolter B., Schwarz J.P., Bottcher U.M., Guha S., Hartl F.U. TRiC/CCT cooperates with different upstream chaperones in the folding of distinct protein classes. Embo. J. 22:2003;5230-5240.
16. Thulasiraman V., Yang C.F., Frydman J. In vivo newly translated polypeptides are sequestered in a protected folding environment. Embo. J. 18:1999;85-95.
17. Feldman D.E., Thulasiraman V., Ferreyra R.G., Frydman J. Formation of the VHL-elongin BC tumor suppressor complex is mediated by the chaperonin TRiC. Mol. Cell. 4:1999;1051-1061.
18. Dougan D.A., Mogk A., Zeth K., Turgay K., Bukau B. AAA+ proteins and substrate recognition, it all depends on their partner in crime. FEBS Lett. 529:2002;6-10.
19. Saleh A., Srinivasula S.M., Balkir L., Robbins P.D., Alnemri E.S. Negative regulation of the Apaf-1 apoptosome by Hsp70. Nat. Cell Biol. 2:2000;476-483.
20. Pilon M., Schekman R. Protein translocation: how Hsp70 pulls it off. Cell. 97:1999;679-682.
21. Flaherty K.M., McKay D.B., Kabsch W., Holmes K.C. Similarity of the three-dimensional structures of actin and the ATPase fragment of a 70-kDa heat shock cognate protein. Proc. Natl. Acad. Sci. U.S.A. 88:1991;5041-5045.
22. Zhu X., Zhao X., Burkholder W.F., Gragerov A., Ogata C.M., Gottesman M.E.et al. Structural analysis of substrate binding by the molecular chaperone DnaK. Science. 272:1996;1606-1614.
23. Rudiger S., Germeroth L., Schneider-Mergener J., Bukau B. Substrate specificity of the DnaK chaperone determined by screening cellulose-bound peptide libraries. Embo. J. 16:1997;1501-1507.
24. Szabo A., Langer T., Schroder H., Flanagan J., Bukau B., Hartl F.U. The ATP hydrolysis-dependent reaction cycle of the Escherichia coli Hsp70 system DnaK, DnaJ, and GrpE. Proc. Natl. Acad. Sci. U.S.A. 91:1994;10345-10349.
25. Langer T., Lu C., Echols H., Flanagan J., Hayer M.K., Hartl F.U. Successive action of DnaK, DnaJ and GroEL along the pathway of chaperone-mediated protein folding. Nature. 356:1992;683-689.
26. Hohfeld J., Jentsch S. GrpE-like regulation of the hsc70 chaperone by the anti-apoptotic protein BAG-1. Embo. J. 16:1997;6209-6216.
27. Young J.C., Hoogenraad N.J., Hartl F.U. Molecular chaperones Hsp90 and Hsp70 deliver preproteins to the mitochondrial import receptor Tom70. Cell. 112:2003;41-50.
28. Takayama S., Reed J.C. Molecular chaperones targeting and regulation by BAG family proteins. Nat. Cell Biol. 3:2001;E237-E241.
29. Luders J., Demand J., Hohfeld J. The ubiquitin-related BAG-1 provides a link between the molecular chaperones Hsc70/Hsp70 and the proteasome. J. Biol. Chem. 275:2000;4613-4617.
30. Alberti S., Demand J., Esser C., Emmerich N., Schild H., Hohfeld J. Ubiquitylation of BAG-1 suggests a novel regulatory mechanism during the sorting of chaperone substrates to the proteasome. J. Biol. Chem. 277:2002;45920-45927.
31. Wiederkehr T., Bukau B., Buchberger A. Protein turnover: a CHIP programmed for proteolysis. Curr. Biol. 12:2002;R26-R28.
32. Picard D. Heat-shock protein 90, a chaperone for folding and regulation. Cell Mol. Life Sci. 59:2002;1640-1648.
33. Aligue R., Akhavan-Niak H., Russell P. A role for Hsp90 in cell cycle control: Wee1 tyrosine kinase activity requires interaction with Hsp90. Embo. J. 13:1994;6099-6106.
34. Young J.C., Moarefi I., Hartl F.U. Hsp90: a specialized but essential protein-folding tool. J. Cell Biol. 154:2001;267-273.
35. Hutchison K.A., Dittmar K.D., Pratt W.B. All of the factors required for assembly of the glucocorticoid receptor into a functional heterocomplex with heat shock protein 90 are preassociated in a self-sufficient protein folding structure, a "foldosome" J. Biol. Chem. 269:1994;27894-27899.
36. Scheufler C., Brinker A., Bourenkov G., Pegoraro S., Moroder L., Bartunik H.et al. Structure of TPR domain-peptide complexes: critical elements in the assembly of the Hsp70-Hsp90 multichaperone machine. Cell. 101:2000;199-210.
37. Prodromou C., Panaretou B., Chohan S., Siligardi G., O'Brien R., Ladbury J.E.et al. The ATPase cycle of Hsp90 drives a molecular 'clamp' via transient dimerization of the N-terminal domains. Embo. J. 19:2000;4383-4392.
38. Obermann W.M., Sondermann H., Russo A.A., Pavletich N.P., Hartl F.U. In vivo function of Hsp90 is dependent on ATP binding and ATP hydrolysis. J. Cell Biol. 143:1998;901-910.
39. Freeman B.C., Morimoto R.I. The human cytosolic molecular chaperones hsp90, hsp70 (hsc70) and hdj-1 have distinct roles in recognition of a non-native protein and protein refolding. Embo. J. 15:1996;2969-2979.
40. Pratt W.B. The hsp90-based chaperone system: involvement in signal transduction from a variety of hormone and growth factor receptors. Proc. Soc. Exp. Biol. Med. 217:1998;420-434.
41. Clark J.I., Muchowski P.J. Small heat-shock proteins and their potential role in human disease. Curr. Opin. Struct. Biol. 10:2000;52-59.
42. Haslbeck M. sHsps and their role in the chaperone network. Cell Mol. Life Sci. 59:2002;1649-1657.
43. Ellgaard L., Molinari M., Helenius A. Setting the standards: quality control in the secretory pathway. Science. 286:1999;1882-1888.
44. McCracken A.A., Brodsky J.L. Evolving questions and paradigm shifts in endoplasmic-reticulum-associated degradation (ERAD). Bioessays. 25:2003;868-877.
45. Gilbert H.F. Protein disulfide isomerase. Methods Enzymol. 290:1998;26-50.
46. Nagata K. Hsp47: a collagen-specific molecular chaperone. Trends Biochem. Sci. 21:1996;22-26.
47. Bu G., Schwartz A.L. RAP, a novel type of ER chaperone. Trends Cell Biol. 8:1998;272-276.
48. Cowan N.J., Lewis S.A. Type II chaperonins, prefoldin, and the tubulin-specific chaperones. Adv. Protein Chem. 59:2001;73-104.
49. Barral J.M., Hutagalung A.H., Brinker A., Hartl F.U., Epstein H.F. Role of the myosin assembly protein UNC-45 as a molecular chaperone for myosin. Science. 295:2002;669-671.
50. Kihm A.J., Kong Y., Hong W., Russell J.E., Rouda S., Adachi K.et al. An abundant erythroid protein that stabilizes free alpha-haemoglobin. Nature. 417:2002;758-763.
51. Hansen J.J., Durr A., Cournu-Rebeix I., Georgopoulos C., Ang D., Nielsen M.N.et al. Hereditary spastic paraplegia SPG13 is associated with a mutation in the gene encoding the mitochondrial chaperonin Hsp60. Am. J. Hum. Genet. 70:2002;1328-1332.
52. Fink J.K. Hereditary spastic paraplegia: the pace quickens. Ann. Neurol. 51:2002;669-672.
53. Ostermann J., Horwich A.L., Neupert W., Hartl F.U. Protein folding in mitochondria requires complex formation with hsp60 and ATP hydrolysis. Nature. 341:1989;125-130.
54. Richardson A., Schwager F., Landry S.J., Georgopoulos C. The importance of a mobile loop in regulating chaperonin/co-chaperonin interaction: humans versus Escherichia coli. J. Biol. Chem. 276:2001;4981-4987.
55. Stone D.L., Slavotinek A., Bouffard G.G., Banerjee-Basu S., Baxevanis A.D., Barr M.et al. Mutation of a gene encoding a putative chaperonin causes McKusick-Kaufman syndrome. Nat. Genet. 25:2000;79-82.
56. Slavotinek A.M., Stone E.M., Mykytyn K., Heckenlively J.R., Green J.S., Heon E.et al. Mutations in MKKS cause Bardet-Biedl syndrome. Nat. Genet. 26:2000;15-16.
57. Katsanis N., Beales P.L., Woods M.O., Lewis R.A., Green J.S., Parfrey P.S.et al. Mutations in MKKS cause obesity, retinal dystrophy and renal malformations associated with Bardet-Biedl syndrome. Nat. Genet. 26:2000;67-70.
58. Mykytyn K., Nishimura D.Y., Searby C.C., Shastri M., Yen H.J., Beck J.S.et al. Identification of the gene (BBS1) most commonly involved in Bardet-Biedl syndrome, a complex human obesity syndrome. Nat. Genet. 31:2002;435-438.
59. Nishimura D.Y., Searby C.C., Carmi R., Elbedour K., Van Maldergem L., Fulton A.B.et al. Positional cloning of a novel gene on chromosome 16q causing Bardet-Biedl syndrome (BBS2). Hum. Mol. Genet. 10:2001;865-874.
60. Mykytyn K., Braun T., Carmi R., Haider N.B., Searby C.C., Shastri M.et al. Identification of the gene that, when mutated, causes the human obesity syndrome BBS4. Nat. Genet. 28:2001;188-191.
61. Badano J.L., Ansley S.J., Leitch C.C., Lewis R.A., Lupski J.R., Katsanis N. Identification of a novel Bardet-Biedl syndrome protein, BBS7, that shares structural features with BBS1 and BBS2. Am. J. Hum. Genet. 72:2003;650-658.
62. Ansley S.J., Badano J.L., Blacque O.E., Hill J., Hoskins B.E., Leitch C.C.et al. Basal body dysfunction is a likely cause of pleiotropic Bardet-Biedl syndrome. Nature. 425:2003;628-633.
63. Engert J.C., Berube P., Mercier J., Dore C., Lepage P., Ge B.et al. ARSACS, a spastic ataxia common in northeastern Quebec, is caused by mutations in a new gene encoding an 11.5-kb ORF. Nat. Genet. 24:2000;120-125.
64. 2-terminal 108 amino acids of the Escherichia coli DnaJ protein stimulate the ATPase activity of DnaK and are sufficient for lambda replication. J. Biol. Chem. 269:1994;5446-5451.
65. Grynberg M., Erlandsen H., Godzik A. HEPN: a common domain in bacterial drug resistance and human neurodegenerative proteins. Trends Biochem. Sci. 28:2003;224-226.
66. Kimura Y., Yahara I., Lindquist S. Role of the protein chaperone YDJ1 in establishing Hsp90-mediated signal transduction pathways. Science. 268:1995;1362-1365.
67. Dittmar K.D., Banach M., Galigniana M.D., Pratt W.B. The role of DnaJ-like proteins in glucocorticoid receptor.hsp90 heterocomplex assembly by the reconstituted hsp90.p60.hsp70 foldosome complex. J. Biol. Chem. 273:1998;7358-7366.
68. Litt M., Kramer P., LaMorticella D.M., Murphey W., Lovrien E.W., Weleber R.G. Autosomal dominant congenital cataract associated with a missense mutation in the human alpha crystallin gene CRYAA. Hum. Mol. Genet. 7:1998;471-474.
69. Vicart P., Caron A., Guicheney P., Li Z., Prevost M.C., Faure A.et al. A missense mutation in the alphaB-crystallin chaperone gene causes a desmin-related myopathy. Nat. Genet. 20:1998;92-95.
70. Djabali K., de Nechaud B., Landon F., Portier M.M. AlphaB-crystallin interacts with intermediate filaments in response to stress. J. Cell Sci. 110(Pt 21):1997;2759-2769.
71. Goldfarb L.G., Park K.Y., Cervenakova L., Gorokhova S., Lee H.S., Vasconcelos O.et al. Missense mutations in desmin associated with familial cardiac and skeletal myopathy. Nat. Genet. 19:1998;402-403.
72. Parvari R., Hershkovitz E., Grossman N., Gorodischer R., Loeys B., Zecic A.et al. Mutation of TBCE causes hypoparathyroidism-retardation-dysmorphism and autosomal recessive Kenny-Caffey syndrome. Nat. Genet. 32:2002;448-452.
73. Martin N., Jaubert J., Gounon P., Salido E., Haase G., Szatanik M.et al. A missense mutation in Tbce causes progressive motor neuronopathy in mice. Nat. Genet. 32:2002;443-447.
74. Schwahn U., Lenzner S., Dong J., Feil S., Hinzmann B., van Duijnhoven G.et al. Positional cloning of the gene for X-linked retinitis pigmentosa 2. Nat. Genet. 19:1998;327-332.
75. Bartolini F., Bhamidipati A., Thomas S., Schwahn U., Lewis S.A., Cowan N.J. Functional overlap between retinitis pigmentosa 2 protein and the tubulin-specific chaperone cofactor C. J. Biol. Chem. 277:2002;14629-14634.
76. Muchowski P.J. Protein misfolding, amyloid formation, and neurodegeneration: a critical role for molecular chaperones? Neuron. 35:2002;9-12.
77. Shulman J.M., Shulman L.M., Weiner W.J., Feany M.B. From fruit fly to bedside: translating lessons from Drosophila models of neurodegenerative disease. Curr. Opin. Neurol. 16:2003;443-449.
78. Temussi P.A., Masino L., Pastore A. From Alzheimer to Huntington: why is a structural understanding so difficult? Embo. J. 22:2003;355-361.
79. Bates G. Huntingtin aggregation and toxicity in Huntington's disease. Lancet. 361:2003;1642-1644.
80. Stefani M, Dobson CM. Protein aggregation and aggregate toxicity: new insights into protein folding, misfolding diseases and biological evolution. J Mol Med 2003, in press.
81. Sakahira H., Breuer P., Hayer-Hartl M.K., Hartl F.U. Molecular chaperones as modulators of polyglutamine protein aggregation and toxicity. Proc. Natl. Acad. Sci. U.S.A. 99(Suppl. 4):2002;16412-16418.
82. Caughey B., Lansbury P.T. Protofibrils, pores, fibrils, and neurodegeneration: separating the responsible protein aggregates from the innocent bystanders. Annu. Rev. Neurosci. 26:2003;267-298.
83. Chiti F., Bucciantini M., Capanni C., Taddei N., Dobson C.M., Stefani M. Solution conditions can promote formation of either amyloid protofilaments or mature fibrils from the HypF N-terminal domain. Protein Sci. 10:2001;2541-2547.
84. Taylor J.P., Tanaka F., Robitschek J., Sandoval C.M., Taye A., Markovic-Plese S.et al. Aggresomes protect cells by enhancing the degradation of toxic polyglutamine-containing protein. Hum. Mol. Genet. 12:2003;749-757.
85. Mishra R.S., Bose S., Gu Y., Li R., Singh N. Aggresome formation by mutant prion proteins: the unfolding role of proteasomes in familial prion disorders. J. Alzheimers Dis. 5:2003;15-23.
86. McNaught K.S., Shashidharan P., Perl D.P., Jenner P., Olanow C.W. Aggresome-related biogenesis of Lewy bodies. Eur. J. Neurosci. 16:2002;2136-2148.
87. Kopito R.R., Sitia R. Aggresomes and Russell bodies. Symptoms of cellular indigestion? EMBO Rep. 1:2000;225-231.
88. Muchowski P.J., Ning K., D'Souza-Schorey C., Fields S. Requirement of an intact microtubule cytoskeleton for aggregation and inclusion body formation by a mutant huntingtin fragment. Proc. Natl. Acad. Sci. U.S.A. 99:2002;727-732.
89. Saudou F., Finkbeiner S., Devys D., Greenberg M.E. Huntingtin acts in the nucleus to induce apoptosis but death does not correlate with the formation of intranuclear inclusions. Cell. 95:1998;55-66.
90. Warrick J.M., Chan H.Y., Gray-Board G.L., Chai Y., Paulson H.L., Bonini N.M. Suppression of polyglutamine-mediated neurodegeneration in Drosophila by the molecular chaperone HSP70. Nat. Genet. 23:1999;425-428.
91. Klement I.A., Skinner P.J., Kaytor M.D., Yi H., Hersch S.M., Clark H.B. et al. Ataxin-1 nuclear localization and aggregation: role in polyglutamine-induced disease in SCA1 transgenic mice. Cell. 95:1998;41-53.
92. Walsh D.M., Klyubin I., Fadeeva J.V., Cullen W.K., Anwyl R., Wolfe M.S. et al. Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature. 416:2002;535-539.
93. Scherzinger E., Sittler A., Schweiger K., Heiser V., Lurz R., Hasenbank R.et al. Self-assembly of polyglutamine-containing huntingtin fragments into amyloid-like fibrils: implications for Huntington's disease pathology. Proc. Natl. Acad. Sci. U.S.A. 96:1999;4604-4609.
94. Yang W., Dunlap J.R., Andrews R.B., Wetzel R. Aggregated polyglutamine peptides delivered to nuclei are toxic to mammalian cells. Hum. Mol. Genet. 11:2002;2905-2917.
95. Sanchez I., Mahlke C., Yuan J. Pivotal role of oligomerization in expanded polyglutamine neurodegenerative disorders. Nature. 421:2003;373-379.
96. Schaffar G, Boteva R, Behrends C, Tzvetkoff N, Sakahira H, Siegers K, et al. Dissecting the mechanism of transcription factor deactivation by a polyglutamine disease protein. Embo J, submitted for publication.
97. Michalik A., Van Broeckhoven C. Pathogenesis of polyglutamine disorders: aggregation revisited. Hum. Mol. Genet. 12(Suppl. 2):2003;R173-R186.
98. Volles M.J., Lee S.J., Rochet J.C., Shtilerman M.D., Ding T.T., Kessler J.C.et al. Vesicle permeabilization by protofibrillar alpha-synuclein: implications for the pathogenesis and treatment of Parkinson's disease. Biochemistry. 40:2001;7812-7819.
99. Kagan B.L., Hirakura Y., Azimov R., Azimova R. The channel hypothesis of Huntington's disease. Brain Res. Bull. 56:2001;281-284.
100. Monoi H., Futaki S., Kugimiya S., Minakata H., Yoshihara K. Poly-L-glutamine forms cation channels: relevance to the pathogenesis of the polyglutamine diseases. Biophys. J. 78:2000;2892-2899.
101. Berke S.J., Paulson H.L. Protein aggregation and the ubiquitin proteasome pathway: gaining the upper hand on neurodegeneration. Curr. Opin. Genet. Dev. 13:2003;253-261.
102. Braun B.C., Glickman M., Kraft R., Dahlmann B., Kloetzel P.M., Finley D.et al. The base of the proteasome regulatory particle exhibits chaperone-like activity. Nat. Cell Biol. 1:1999;221-226.
103. Imai J., Yashiroda H., Maruya M., Yahara I., Tanaka K. Proteasomes and molecular chaperones: cellular machinery responsible for folding and destruction of unfolded proteins. Cell Cycle. 2:2003;585-590.
104. Muchowski P.J., Schaffar G., Sittler A., Wanker E.E., Hayer-Hartl M.K., Hartl F.U. Hsp70 and hsp40 chaperones can inhibit self-assembly of polyglutamine proteins into amyloid-like fibrils. Proc. Natl. Acad. Sci. U.S.A. 97:2000;7841-7846.
105. Jana N.R., Tanaka M., Wang G., Nukina N. Polyglutamine length-dependent interaction of Hsp40 and Hsp70 family chaperones with truncated N-terminal huntingtin: their role in suppression of aggregation and cellular toxicity. Hum. Mol. Genet. 9:2000;2009-2018.
106. Cummings C.J., Mancini M.A., Antalffy B., DeFranco D.B., Orr H.T., Zoghbi H.Y. Chaperone suppression of aggregation and altered subcellular proteasome localization imply protein misfolding in SCA1. Nat. Genet. 19:1998;148-154.
107. Fonte V., Kapulkin V., Taft A., Fluet A., Friedman D., Link C.D. Interaction of intracellular beta amyloid peptide with chaperone proteins. Proc. Natl. Acad. Sci. U.S.A. 99:2002;9439-9444.
108. Sherman M.Y., Goldberg A.L. Cellular defenses against unfolded proteins: a cell biologist thinks about neurodegenerative diseases. Neuron. 29:2001;15-32.
109. Krobitsch S., Lindquist S. Aggregation of huntingtin in yeast varies with the length of the polyglutamine expansion and the expression of chaperone proteins. Proc. Natl. Acad. Sci. U.S.A. 97:2000;1589-1594.
110. Chai Y., Koppenhafer S.L., Bonini N.M., Paulson H.L. Analysis of the role of heat shock protein (Hsp) molecular chaperones in polyglutamine disease. J. Neurosci. 19:1999;10338-10347.
111. Takata K., Kitamura Y., Tsuchiya D., Kawasaki T., Taniguchi T., Shimohama S. Heat shock protein-90-induced microglial clearance of exogenous amyloid-beta1-42 in rat hippocampus in vivo. Neurosci. Lett. 344:2003;87-90.
112. McLean P.J., Kawamata H., Shariff S., Hewett J., Sharma N., Ueda K.et al. TorsinA and heat shock proteins act as molecular chaperones: suppression of alpha-synuclein aggregation. J. Neurochem. 83:2002;846-854.
113. Stockel J., Hartl F.U. Chaperonin-mediated de novo generation of prion protein aggregates. J. Mol. Biol. 313:2001;861-872.
114. Cummings C.J., Sun Y., Opal P., Antalffy B., Mestril R., Orr H.T.et al. Over-expression of inducible HSP70 chaperone suppresses neuropathology and improves motor function in SCA1 mice. Hum. Mol. Genet. 10:2001;1511-1518.
115. Auluck P.K., Chan H.Y., Trojanowski J.Q., Lee V.M., Bonini N.M. Chaperone suppression of alpha-synuclein toxicity in a Drosophila model for Parkinson's disease. Science. 295:2002;865-868.
116. Bennett M.C., Bishop J.F., Leng Y., Chock P.B., Chase T.N., Mouradian M.M. Degradation of alpha-synuclein by proteasome. J. Biol. Chem. 274:1999;33855-33858.
117. Verhoef L.G., Lindsten K., Masucci M.G., Dantuma N.P. Aggregate formation inhibits proteasomal degradation of polyglutamine proteins. Hum. Mol. Genet. 11:2002;2689-2700.
118. Bence N.F., Sampat R.M., Kopito R.R. Impairment of the ubiquitin-proteasome system by protein aggregation. Science. 292:2001;1552-1555.
119. Keller J.N., Hanni K.B., Markesbery W.R. Impaired proteasome function in Alzheimer's disease. J. Neurochem. 75:2000;436-439.
120. McNaught K.S., Jenner P. Proteasomal function is impaired in substantia nigra in Parkinson's disease. Neurosci. Lett. 297:2001;191-194.
121. Saigoh K., Wang Y.L., Suh J.G., Yamanishi T., Sakai Y., Kiyosawa H.et al. Intragenic deletion in the gene encoding ubiquitin carboxy-terminal hydrolase in gad mice. Nat. Genet. 23:1999;47-51.
122. Kitada T., Asakawa S., Hattori N., Matsumine H., Yamamura Y., Minoshima S.et al. Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature. 392:1998;605-608.
123. Cummings C.J., Reinstein E., Sun Y., Antalffy B., Jiang Y., Ciechanover A.et al. Mutation of the E6-AP ubiquitin ligase reduces nuclear inclusion frequency while accelerating polyglutamine-induced pathology in SCA1 mice. Neuron. 24:1999;879-892.
124. Chai Y., Koppenhafer S.L., Shoesmith S.J., Perez M.K., Paulson H.L. Evidence for proteasome involvement in polyglutamine disease: localization to nuclear inclusions in SCA3/MJD and suppression of polyglutamine aggregation in vitro. Hum. Mol. Genet. 8:1999;673-682.
125. Waelter S., Boeddrich A., Lurz R., Scherzinger E., Lueder G., Lehrach H.et al. Accumulation of mutant huntingtin fragments in aggresome-like inclusion bodies as a result of insufficient protein degradation. Mol. Biol. Cell. 12:2001;1393-1407.
126. Sittler A., Lurz R., Lueder G., Priller J., Lehrach H., Hayer-Hartl M.K.et al. Geldanamycin activates a heat shock response and inhibits huntingtin aggregation in a cell culture model of Huntington's disease. Hum. Mol. Genet. 10:2001;1307-1315.
127. Auluck P.K., Bonini N.M. Pharmacological prevention of Parkinson disease in Drosophila. Nat. Med. 8:2002;1185-1186.