The elusive middle domain of Hsp104 and ClpB: Location and function

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1823, Issue 1, 2012, Pages 29-39

  DeSantis, Morgan E ^a   Shorter, James ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Aggregate; ClpB; Hexamer; Hsp104; Prion

Indexed keywords

ADENOSINE TRIPHOSPHATE; CHAPERONE; HEAT SHOCK PROTEIN 104; HEAT SHOCK PROTEIN 40; HEAT SHOCK PROTEIN 70; PROTEIN CLPB;

CRYOELECTRON MICROSCOPY; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN QUATERNARY STRUCTURE; REVIEW; THERMUS THERMOPHILUS;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ESCHERICHIA COLI PROTEINS; HEAT-SHOCK PROTEINS; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STRUCTURE, QUATERNARY; SACCHAROMYCES CEREVISIAE PROTEINS; STRUCTURAL HOMOLOGY, PROTEIN;

EID: 84855207518     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2011.07.014     Document Type: Review

References (136)

1. Schirmer E.C., Glover J.R., Singer M.A., Lindquist S. HSP100/Clp proteins: a common mechanism explains diverse functions. Trends Biochem. Sci. 1996, 21:289-296.
2. Doyle S.M., Wickner S. Hsp104 and ClpB: protein disaggregating machines. Trends Biochem. Sci. 2009, 34:40-48.
3. Glover J.R., Lum R. Remodeling of protein aggregates by Hsp104. Protein Pept. Lett. 2009, 16:587-597.
4. Barends T.R., Werbeck N.D., Reinstein J. Disaggregases in 4 dimensions. Curr. Opin. Struct. Biol. 2010, 20:46-53.
5. Haslberger T., Bukau B., Mogk A. Towards a unifying mechanism for ClpB/Hsp104-mediated protein disaggregation and prion propagation. Biochem. Cell Biol. 2010, 88:63-75.
6. Vashist S., Cushman M., Shorter J. Applying Hsp104 to protein-misfolding disorders. Biochem. Cell Biol. 2010, 88:1-13.
7. Grimminger-Marquardt V., Lashuel H.A. Structure and function of the molecular chaperone Hsp104 from yeast. Biopolymers 2010, 93:252-276.
8. Bosl B., Grimminger V., Walter S. The molecular chaperone Hsp104-a molecular machine for protein disaggregation. J. Struct. Biol. 2006, 156:139-148.
9. Lindquist S., Patino M.M., Chernoff Y.O., Kowal A.S., Singer M.A., Liebman S.W., Lee K.H., Blake T. The role of Hsp104 in stress tolerance and [PSI+] propagation in Saccharomyces cerevisiae. Cold Spring Harb. Symp. Quant. Biol. 1995, 60:451-460.
10. Hanson P.I., Whiteheart S.W. AAA+ proteins: have engine, will work. Nat. Rev. Mol. Cell Biol. 2005, 6:519-529.
11. Erzberger J.P., Berger J.M. Evolutionary relationships and structural mechanisms of AAA+ proteins. Annu. Rev. Biophys. Biomol. Struct. 2006, 35:93-114.
12. Neuwald A.F., Aravind L., Spouge J.L., Koonin E.V. AAA+: a class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes. Genome. Res. 1999, 9:27-43.
13. Parsell D.A., Kowal A.S., Singer M.A., Lindquist S. Protein disaggregation mediated by heat-shock protein Hspl04. Nature 1994, 372:475-478.
14. Sanchez Y., Taulin J., Borkovich K.A., Lindquist S. Hsp104 is required for tolerance to many forms of stress. EMBO J. 1992, 11:2357-2364.
15. Sanchez Y., Lindquist S.L. HSP104 required for induced thermotolerance. Science 1990, 248:1112-1115.
16. Glover J.R., Lindquist S. Hsp104, Hsp70, and Hsp40: a novel chaperone system that rescues previously aggregated proteins. Cell 1998, 94:73-82.
17. Lindquist S., Kim G. Heat-shock protein 104 expression is sufficient for thermotolerance in yeast. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:5301-5306.
18. Parsell D.A., Taulien J., Lindquist S. The role of heat-shock proteins in thermotolerance. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 1993, 339:279-285. discussion 285-276.
19. Fink A.L. Protein aggregation: folding aggregates, inclusion bodies and amyloid. Fold. Des. 1998, 3:R9-R23.
20. Wang L., Schubert D., Sawaya M.R., Eisenberg D., Riek R. Multidimensional structure-activity relationship of a protein in its aggregated states. Angew. Chem. Int. Ed. 2010, 49:3904-3908.
21. Shorter J., Lindquist S. Hsp104 catalyzes formation and elimination of self-replicating Sup35 prion conformers. Science 2004, 304:1793-1797.
22. Shorter J., Lindquist S. Prions as adaptive conduits of memory and inheritance. Nat. Rev. Genet. 2005, 6:435-450.
23. Shorter J., Lindquist S. Destruction or potentiation of different prions catalyzed by similar Hsp104. Remodeling Act. 2006, 23:425-438.
24. Shorter J., Lindquist S. Hsp104, Hsp70 and Hsp40 interplay regulates formation, growth and elimination of Sup35 prions. EMBO J. 2008, 27:2712-2724.
25. +]. Science 1995, 268:880-884.
26. Moriyama H., Edskes H.K., Wickner R.B. [URE3] Prion propagation in Saccharomyces cerevisiae: requirement for chaperone Hsp104 and curing by overexpressed chaperone Ydj1p. Mol. Cell. Biol. 2000, 20:8916-8922.
27. Alberti S., Halfmann R., King O., Kapila A., Lindquist S. A systematic survey identifies prions and illuminates sequence features of prionogenic proteins. Cell 2009, 137:146-158.
28. Sweeny E.A., Shorter J. Prion proteostasis: Hsp104 meets its supporting cast. Prion 2008, 2:135-140.
29. Sondheimer N., Lindquist S. Rnq1: an epigenetic modifier of protein function in yeast. Mol. Cell. 2000, 5:163-172.
30. Du Z., Park K.W., Yu H., Fan Q., Li L. Newly identified prion linked to the chromatin-remodeling factor Swi1 in Saccharomyces cerevisiae. Nat. Genet. 2008, 40:460-465.
31. Patel B.K., Gavin-Smyth J., Liebman S.W. The yeast global transcriptional co-repressor protein Cyc8 can propagate as a prion. Nat. cell biol. 2009, 11:344-349.
32. DiSalvo S., Derdowski A., Pezza J.A., Serio T.R. Dominant prion mutants induce curing through pathways that promote chaperone-mediated disaggregation. Nat. Struct. Mol. Biol. 2011, 18:486-492.
33. Satpute-Krishnan P., Langseth S.X., Serio T.R. Hsp104-dependent remodeling of prion complexes mediates protein-only inheritance. PLoS Biol. 2007, 5:e24.
34. Sunde M., Serpell L.C., Bartlam M., Fraser P.E., Pepys M.B., Blake C.C.F. Common core structure of amyloid fibrils by synchrotron X-ray diffraction. J. Mol. Biol. 1997, 273:729-739.
35. Nelson R., Sawaya M.R., Balbirnie M., Madsen A.O., Riekel C., Grothe R., Eisenberg D. Structure of the cross-beta spine of amyloid-like fibrils. Nature 2005, 435:773-778.
36. +]. Nat. Struct. Mol. Biol. 2009, 16:598-605.
37. Aguzzi A., O'Connor T. Protein aggregation diseases: pathogenicity and therapeutic perspectives. Nat. Rev. Drug Discov. 2010, 9:237-248.
38. Aguzzi A., Rajendran L. The transcellular spread of cytosolic amyloids, prions, and prionoids. Neuron 2009, 64:783-790.
39. Cushman M., Johnson B.S., King O.D., Gitler A.D., Shorter J. Prion-like disorders: blurring the divide between transmissibility and infectivity. J. Cell Sci. 2010, 123:1191-1201.
40. Halfmann R., Lindquist S. Epigenetics in the extreme: prions and the inheritance of environmentally acquired traits. Science 2010, 330:629-632.
41. Shorter J. Emergence and natural selection of drug-resistant prions. Mol. Biosyst. 2010, 6:1115-1130.
42. True H.L., Lindquist S.L. A yeast prion provides a mechanism for genetic variation and phenotypic diversity. Nature 2000, 407:477-483.
43. Shorter J. Hsp104: a weapon to combat diverse neurodegenerative disorders. Neurosignals 2008, 16:63-74.
44. Lo Bianco C., Shorter J., Ragulier E., Lashuel H., Iwatsubo T., Lindquist S., Aebischer P. Hsp104 antagonizes alpha-synuclein aggregation and reduces dopaminergic degeneration in a rat model of Parkinson disease. J. Clin. Investig. 2008, 118:3087-3097.
45. Vacher C., Garcia-Oroz L., Rubinsztein D.C. Overexpression of yeast hsp104 reduces polyglutamine aggregation and prolongs survival of a transgenic mouse model of Huntington's disease. Hum. Mol. Genet. 2005, 14:3425-3433.
46. Motohashi K., Watanabe Y., Yohda M., Yoshida M. Heat-inactivated proteins are rescued by the DnaK.J-GrpE set and ClpB chaperones. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:7184-7189.
47. Mogk A., Tomoyasu T., Goloubinoff P., Rudiger S., Roder D., Langen H., Bukau B. Identification of thermolabile E. coli proteins: prevention and reversion of aggregation by DnaK and ClpB. EMBO J. 1999, 18:6934-6949.
48. Zolkiewski M. ClpB cooperates with DnaK, DnaJ, and GrpE in suppressing protein aggregation. A novel multi-chaperone system from Escherichia coli. J. Biol. Chem. 1999, 274:28083-28086.
49. Goloubinoff P., Mogk A., Zvi A.P.B., Tomoyasu T., Bukau B. Sequential mechanism of solubilization and refolding of stable protein aggregates by a bichaperone network. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:13732-13737.
50. Squires C.L., Pedersen S., Ross B.M., Squires C. ClpB is the Escherichia coli heat shock protein F84.1. J. Bacteriol. 1991, 173:4254-4262.
51. Tipton K.A., Verges K.J., Weissman J.S. In vivo monitoring of the prion replication cycle reveals a critical role for sis1 in delivering substrates to Hsp104. Cell 2008, 32:584-591.
52. Hinault M.P., Cuendet A.F., Mattoo R.U., Mensi M., Dietler G., Lashuel H.A., Goloubinoff P. Stable alpha-synuclein oligomers strongly inhibit chaperone activity of the Hsp70 system by weak interactions with J-domain co-chaperones. J. Biol. Chem. 2010, 285:38173-38182.
53. Parsell D.A., Kowal A.S., Lindquist S. Saccharomyces cerevisiae Hsp104 protein. Purification and characterization of ATP-induced structural changes. J. Biol. Chem. 1994, 269:4480-4487.
54. Zolkiewski M., Kessel M., Ginsburg A., Maurizi M.R. Nucleotide-dependent oligomerization of C1pB from Escherichia coli. Protein Sci. 1999, 8:1899-1903.
55. Lum R., Niggemann M., Glover J.R. Peptide and protein binding in the axial channel of Hsp104: insights into the mechanism of protein unfolding. J. Biol. Chem. 2008, 283:30139-30150.
56. Lum R., Tkach J.M., Vierling E., Glover J.R. Evidence for an unfolding/threading mechanism for protein disaggregation by Saccharomyces cerevisiae Hsp104. J. Biol. Chem. 2004, 279:29139-29146.
57. Schlieker C., Weibezahn J., Patzelt H., Tessarz P., Strub C., Zeth K., Erbse A., Schneider-Mergener J., Chin J.W., Schultz P.G., Bukau B., Mogk A. Substrate recognition by the AAA+ chaperone ClpB. Nat. Struct. Mol. Biol. 2004, 11:607-615.
58. Weibezahn J., Tessarz P., Schlieker C., Zahn R., Maglica Z., Lee S., Zentgraf H., Weber-Ban E.U., Dougan D.A., Tsai F.T.F., Mogk A., Bukau B. Thermotolerance requires refolding of aggregated proteins by substrate translocation through the central pore of ClpB. Cell 2004, 119:653-665.
59. Shorter J., Lindquist S. Navigating the ClpB channel to solution. Nat. Struct. Mol. Biol. 2005, 12:4-6.
60. Horwich A.L. Chaperoned protein disaggregation-the ClpB ring uses its central channel. Cell 2004, 119:579-581.
61. Lee S., Choi J.-M., Tsai F.T.F. Visualizing the ATPase cycle in a protein disaggregating machine: structural basis for substrate binding by ClpB. Mol. Cell 2007, 25:261-271.
62. Lee S., Sielaff B., Lee J., Tsai F.T.F. CryoEM structure of Hsp104 and its mechanistic implication for protein disaggregation. Proc. Natl. Acad. Sci. 2010, 107:8135-8140.
63. Lee S., Sowa M.E., Watanabe Y.-h., Sigler P.B., Chiu W., Yoshida M., Tsai F.T.F. The structure of ClpB: a molecular chaperone that rescues proteins from an aggregated state. Cell 2003, 115:229-240.
64. Wendler P., Shorter J., Plisson C., Cashikar A.G., Lindquist S., Saibil H.R. Atypical AAA+ subunit packing creates an expanded cavity for disaggregation by the protein-remodeling factor Hsp104. Cell 2007, 131:1366-1377.
65. Wendler P., Shorter J., Snead D., Plisson C., Clare D.K., Lindquist S., Saibil H.R. Motor mechanism for protein threading through Hsp104. Mol. Cell 2009, 34:81-92.
66. Wendler P., Saibil H.R. Cryo electron microscopy structures of Hsp100 proteins: crowbars in or out?. Biochem. Cell Biol. 2010, 88:89-96.
67. Haslberger T., Weibezahn J., Zahn R., Lee S., Tsai F.T.F., Bukau B., Mogk A. M domains couple the ClpB threading motor with the DnaK chaperone activity. Mol. Cell 2007, 25:247-260.
68. Miot M., Reidy M., Doyle S.M., Hoskins J.R., Johnston D.M., Genest O., Vitery M.-C., Masison D.C., Wickner S. Species-specific collaboration of heat shock proteins (Hsp) 70 and 100 in thermotolerance and protein disaggregation. Proc. Natl. Acad. Sci. 2011, 108:6915-6920.
69. Sielaff B., Tsai F.T.F. The M-domain controls Hsp104 protein remodeling activity in an Hsp70/Hsp40-dependent manner. J. Mol. Biol. 2010, 402:30-37.
70. Parsell D.A., Lindquist S. The function of heat-shock proteins in stress tolerance: degradation and reactivation of damaged proteins. Annu. Rev. Genet. 1993, 27:437-496.
71. Parsell D.A., Sanchez Y., Stitzel J.D., Lindquist S. Hspl04 is a highly conserved protein with two essential nucleotide-binding sites. Nature 1991, 353:270-273.
72. Barnett M.E., Zolkiewska A., Zolkiewski M. Structure and activity of ClpB from Escherichia coli. J. Biol. Chem. 2000, 275:37565-37571.
73. Cashikar A.G., Schirmer E.C., Hattendorf D.A., Glover J.R., Ramakrishnan M.S., Ware D.M., Lindquist S.L. Defining a pathway of communication from the C-terminal peptide binding domain to the N-terminal ATPase domain in a AAA protein. Mol. Cell 2002, 9:751-760.
74. Mackay R.G., Helsen C.W., Tkach J.M., Glover J.R. The C-terminal extension of saccharomyces cerevisiae Hsp104 plays a role in oligomer assembly. Biochemistry 2008, 47:1918-1927.
75. Li J., Sha B. Crystal structure of E. coli Hsp100 ClpB nucleotide-binding domain 1 (NBD1) and mechanistic studies on ClpB ATPase activity. J. Mol. Biol. 2002, 318:1127-1137.
76. Li J., Sha B. Crystal structure of the E. coli Hsp100 ClpB N-terminal domain. Structure (Camb) 2003, 11:323-328.
77. Hattendorf D.A., Lindquist S.L. Cooperative kinetics of both Hsp104 ATPase domains and interdomain communication revealed by AAA sensor-1 mutants. EMBO J. 2002, 21:12-21.
78. Schirmer E.C., Queitsch C., Kowal A.S., Parsell D.A., Lindquist S. The ATPase activity of Hsp104, effects of environmental conditions and mutations. J. Biol. Chem. 1998, 273:15546-15552.
79. Schirmer E.C., Ware D.M., Queitsch C., Kowal A.S., Lindquist S.L. Subunit interactions influence the biochemical and biological properties of Hsp104. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:914-919.
80. Mogk A., Schlieker C., Strub C., Rist W., Weibezahn J., Bukau B. Roles of individual domains and conserved motifs of the AAA+ protein ClpB in oligomerization, ATP-hydrolysis and chaperone activity. J. Biol. Chem. 2003, M209686200.
81. Tkach J.M., Glover J.R. Amino acid substitutions in the C-terminal AAA+ module of Hsp104 prevent substrate recognition by disrupting oligomerization and cause high temperature inactivation. J. Biol. Chem. 2004, 279:35692-35701.
82. Doyle S.M., Shorter J., Zolkiewski M., Hoskins J.R., Lindquist S., Wickner S. Asymmetric deceleration of ClpB or Hsp104 ATPase activity unleashes protein-remodeling activity. Nat. Struct. Mol. Biol. 2007, 14:114-122.
83. Franzmann T.M., Czekalla A., Walter S.G. Regulatory circuits of the AAA+ disaggregase Hsp104. J. Biol. Chem. 2011, 286:17992-18001.
84. Schaupp A., Marcinowski M., Grimminger V., Bosl B., Walter S. Processing of proteins by the molecular chaperone Hsp104. J. Mol. Biol. 2007, 370:674-686.
85. Schirmer E.C., Homann O.R., Kowal A.S., Lindquist S. Dominant gain-of-function mutations in Hsp104p reveal crucial roles for the middle region. Mol. Biol. Cell 2004, 15:2061-2072.
86. Weibezahn J., Schlieker C., Bukau B., Mogk A. Characterization of a trap mutant of the AAA+ chaperone ClpB. J. Biol. Chem. 2003, 278:32608-32617.
87. Watanabe Y.-h., Takano M., Yoshida M. ATP binding to nucleotide binding domain (NBD)1 of the ClpB chaperone induces motion of the long coiled-coil, stabilizes the hexamer, and activates NBD2. J. Biol. Chem. 2005, 280:24562-24567.
88. Ogura T., Whiteheart S.W., Wilkinson A.J. Conserved arginine residues implicated in ATP hydrolysis, nucleotide-sensing, and inter-subunit interactions in AAA and AAA+ ATPases. J. Struct. Biol. 2004, 146:106-112.
89. Lupas A.N., Martin J. AAA proteins. Curr. Opin. Struct. Biol. 2002, 12:746-753.
90. Bochtler M., Hartmann C., Song H.K., Bourenkov G.P., Bartunik H.D., Huber R. The structures of HsIU and the ATP-dependent protease HsIU-HsIV. Nature 2000, 403:800-805.
91. Wang F., Mei Z., Qi Y., Yan C., Hu Q., Wang J., Shi Y. Structure and mechanism of the hexameric MecA-ClpC molecular machine. Nature 2011, 471:331-335.
92. Kirstein J., Zuhlke D., Gerth U., Turgay K., Hecker M. A tyrosine kinase and its activator control the activity of the CtsR heat shock repressor in B. subtilis. EMBO J. 2005, 24:3435-3445.
93. Kruger E., Witt E., Ohlmeier S., Hanschke R., Hecker M. The clp proteases of Bacillus subtilis are directly involved in degradation of misfolded proteins. J. Bacteriol. 2000, 182:3259-3265.
94. Kirstein J., Moliere N., Dougan D.A., Turgay K. Adapting the machine: adaptor proteins for Hsp100/Clp and AAA+ proteases. Nat. Rev. Microbiol. 2009, 7:589-599.
95. Schlothauer T., Mogk A., Dougan D.A., Bukau B., Turgay K. MecA, an adaptor protein necessary for ClpC chaperone activity. Proc. Natl. Acad. Sci. 2003, 100:2306-2311.
96. Kirstein J., Schlothauer T., Dougan D.A., Lilie H., Tischendorf G., Mogk A., Bukau B., Turgay K. Adaptor protein controlled oligomerization activates the AAA+ protein ClpC. EMBO J. 2006, 25:1481-1491.
97. Werbeck N.D., Schlee S., Reinstein J. Coupling and dynamics of subunits in the hexameric AAA+ chaperone ClpB. J. Mol. Biol. 2008, 378:178-190.
98. Haslberger T., Zdanowicz A., Brand I., Kirstein J., Turgay K., Mogk A., Bukau B. Protein disaggregation by the AAA+ chaperone ClpB involves partial threading of looped polypeptide segments. Nat. Struct. Mol. Biol. 2008, 15:641-650.
99. Kedzierska S., Akoev V., Barnett M.E., Zolkiewski M. Structure and function of the middle domain of ClpB from Escherichia coli. Biochemistry 2003, 42:14242-14248.
100. Watanabe Y.h., Nakazaki Y., Suno R., Yoshida M. Stability of the two wings of the coiled-coil domain of ClpB chaperone is critical for its disaggregation activity. Biochem. J. 2009, 421:71-77.
101. Kruger E., Volker U., Hecker M. Stress induction of clpC in Bacillus subtilis and its involvement in stress tolerance. J. Bacteriol. 1994, 176:3360-3367.
102. Turgay K., Hamoen L.W., Venema G., Dubnau D. Biochemical characterization of a molecular switch involving the heat shock protein ClpC, which controls the activity of ComK, the competence transcription factor of Bacillus subtilis. Genes Dev. 1997, 11:119-128.
103. Leidhold C., Janowsky B.v., Becker D., Bender T., Voos W. Structure and function of Hsp78, the mitochondrial ClpB homolog. J. Struct. Biol. 2006, 156:149-164.
104. Lewandowska A., Gierszewska M., Marszalek J., Liberek K. Hsp78 chaperone functions in restoration of mitochondrial network following heat stress. Biochim. et Biophy. Acta (BBA) - Mol. Cell Res. 2006, 1763:141-151.
105. Röttgers K., Zufall N., Guiard B., Voos W. The ClpB homolog Hsp78 is required for the efficient degradation of proteins in the mitochondrial matrix. J. Biol. Chem. 2002, 277:45829-45837.
106. Krzewska J., Langer T., Liberek K. Mitochondrial Hsp78, a member of the Clp/Hsp100 family in Saccharomyces cerevisiae, cooperates with Hsp70 in protein refolding. FEBS Lett. 2001, 489:92-96.
107. Nieto-Sotelo J., Kannan K.B., Martínez L.M., Segal C. Characterization of a maize heat-shock protein 101 gene, HSP101, encoding a ClpB/Hsp100 protein homologue. Gene 1999, 230:187-195.
108. Queitsch C., Hong S.-W., Vierling E., Lindquist S. Heat shock protein 101 plays a crucial role in thermotolerance in Arabidopsis. Plant Cell 2000, 12:479-492.
109. Lee Y., Nagao R.T., Key J.L. A soybean 101-kD heat shock protein complements a yeast HSP104 deletion mutant in acquiring thermotolerance. Plant Cell Online 1994, 6:1889-1897.
110. Gallie D.R., Fortner D., Peng J., Puthoff D. ATP-dependent hexameric assembly of the heat shock protein Hsp101 involves multiple interaction domains and a functional C-proximal nucleotide-binding domain. J. Biol. Chem. 2002, 277:39617-39626.
111. Derré I., Rapoport G., Devine K., Rose M., Msadek T. ClpE, a novel type of HSP100 ATPase, is part of the CtsR heat shock regulon of Bacillus subtilis. Mol. Microbiol. 1999, 32:581-593.
112. Ingmer H., Vogensen F.K., Hammer K., Kilstrup M. Disruption and analysis of the clpB, clpC, and clpE genes in Lactococcus lactis: ClpE, a new Clp family in gram-positive bacteria. J. Bacteriol. 1999, 181:2075-2083.
113. Miethke M., Hecker M., Gerth U. Involvement of Bacillus subtilis ClpE in CtsR degradation and protein quality control. J. Bacteriol. 2006, 188:4610-4619.
114. Doyle S.M., Hoskins J.R., Wickner S. Collaboration between the ClpB AAA+ remodeling protein and the DnaK chaperone system. Proc. Natl. Acad. Sci. 2007, 104:11138-11144.
115. Schlieker C., Zentgraf H., Dersch P., Mogk A. ClpV, a unique Hsp100/Clp member of pathogenic proteobacteria. Biol. Chem. 2005, 386:1115-1127.
116. Dougan D.A., Reid B.G., Horwich A.L., Bukau B. ClpS, a substrate modulator of the ClpAP machine. Mol. Cell 2002, 9:673-683.
117. Sanchez Y., Parsell D.A., Taulien J., Vogel J.L., Craig E.A., Lindquist S. Genetic evidence for a functional relationship between Hsp104 and Hsp70. J. Bacteriol. 1993, 175:6484-6491.
118. Vogel J.L., Parsell D.A., Lindquist S. Heat-shock proteins Hsp104 and Hsp70 reactivate mRNA splicing after heat inactivation. Curr. Biol. 1995, 5:306-317.
119. Higurashi T., Hines J.K., Sahi C., Aron R., Craig E.A. Specificity of the J-protein Sis1 in the propagation of 3 yeast prions. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:16596-16601.
120. Tessarz P., Mogk A., Bukau B. Substrate threading through the central pore of the Hsp104 chaperone as a common mechanism for protein disaggregation and prion propagation. Mol. Microbiol. 2008, 68:87-97.
121. Zietkiewicz S., Krzewska J., Liberek K. Successive and synergistic action of the Hsp70 and Hsp100 chaperones in protein disaggregation. J. Biol. Chem. 2004, 279:44376-44383.
122. Zietkiewicz S., Lewandowska A., Stocki P., Liberek K. Hsp70 chaperone machine remodels protein aggregates at the initial step of Hsp70-Hsp100-dependent disaggregation. J. Biol. Chem. 2006, 281:7022-7029.
123. Hoskins J.R., Doyle S.M., Wickner S. Coupling ATP utilization to protein remodeling by ClpB, a hexameric AAA+ protein. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:22233-22238.
124. Mosser D.D., Ho S., Glover J.R. Saccharomyces cerevisiae Hsp104 enhances the chaperone capacity of human cells and inhibits heat stress-induced proapoptotic signaling. Biochemistry 2004, 43:8107-8115.
125. +] prion of Saccharomyces cerevisiae can be propagated by an Hsp104 orthologue from Candida albicans. Eukaryot Cell 2006, 5:217-225.
126. Schirmer E.C., Lindquist S., Vierling E. An Arabidopsis heat shock protein complements a thermotolerance defect in yeast. Plant Cell 1994, 6:1899-1909.
127. +] prion. PLoS One 2009, 4:e6939.
128. Lee Y.R., Nagao R.T., Key J.L. A soybean 101-kD heat shock protein complements a yeast HSP104 deletion mutant in acquiring thermotolerance. Plant Cell 1994, 6:1889-1897.
129. Schlee S., Beinker P., Akhrymuk A., Reinstein J. A chaperone network for the resolubilization of protein aggregates: direct interaction of ClpB and DnaK. J. Mol. Biol. 2004, 336:275-285.
130. Kedzierska S., Chesnokova L.S., Witt S.N., Zolkiewski M. Interactions within the ClpB/DnaK bi-chaperone system from Escherichia coli. Arch. Biochem. Biophys. 2005, 444:61-65.
131. Liu Y.H., Han Y.L., Song J., Wang Y., Jing Y.Y., Shi Q., Tian C., Wang Z.Y., Li C.P., Han J., Dong X.P. Heat shock protein 104 inhibited the fibrillization of prion peptide 106-126 and disassembled prion peptide 106-126 fibrils in vitro. Int. J. Biochem. Cell Biol. 2011, 43:768-774.
132. Narayanan S., Walter S., Reif B. Yeast prion-protein, sup35, fibril formation proceeds by addition and substraction of oligomers. Chembiochem 2006, 7:757-765.
133. Savistchenko J., Krzewska J., Fay N., Melki R. Molecular chaperones and the assembly of the prion Ure2p in vitro. J. Biol. Chem. 2008, 283:15732-15739.
134. +] prion propagation in S. cerevisiae by comprehensive chromosomal mutations. Prion 2007, 1:69-77.
135. Gokhale K.C., Newnam G.P., Sherman M.Y., Chernoff Y.O. Modulation of prion-dependent polyglutamine aggregation and toxicity by chaperone proteins in the yeast model. J. Biol. Chem. 2005, 280:22809-22818.
136. Kurahashi H., Nakamura Y. Channel mutations in Hsp104 hexamer distinctively affect thermotolerance and prion-specific propagation. Mol. Microbiol. 2007, 63:1669-1683.