Cooperation of Hsp70 and Hsp100 chaperone machines in protein disaggregation

Frontiers in Molecular Biosciences

Volumn 2, Issue MAY, 2015, Pages

  Mogk, Axel ^a   Kummer, Eva ^a,b   Bukau, Bernd ^a  

^a GERMAN CANCER RESEARCH CENTER   (Germany)

^b ETH ZURICH   (Switzerland)

Author keywords

AAA+ proteins; Chaperone; Hsp100; Hsp70; Protein disaggregation

Indexed keywords

EID: 84950160369     PISSN: None     EISSN: 2296889X     Source Type: Journal    
DOI: 10.3389/fmolb.2015.00022     Document Type: Review

References (85)

1. Acebron, S. P., Martin, I., del Castillo, U., Moro, F., and Muga, A. (2009). DnaK-mediated association of ClpB to protein aggregates. A bichaperone network at the aggregate surface. FEBS Lett. 583, 2991-2996. doi: 10.1016/j.febslet.2009.08.020
2. Aguado, A., Fernandez-Higuero, J. A., Cabrera, Y., Moro, F., and Muga, A. (2015). ClpB dynamics is driven by its ATPase cycle and regulated by the DnaK system and substrate proteins. Biochem. J. 466, 561-570. doi: 10.1042/BJ20141390
3. Aubin-Tam, M. E., Olivares, A. O., Sauer, R. T., Baker, T. A., and Lang, M. J. (2011). Single-molecule protein unfolding and translocation by an ATP-fueled proteolytic machine. Cell 145, 257-267. doi: 10.1016/j.cell.2011.03.036
4. Baker, T. A., and Sauer, R. T. (2012). ClpXP, an ATP-powered unfolding and protein-degradation machine. Biochim. Biophys. Acta 1823, 15-28. doi: 10.1016/j.bbamcr.2011.06.007
5. Beinker, P., Schlee, S., Groemping, Y., Seidel, R., and Reinstein, J. (2002). The N terminus of ClpB from Thermus thermophilus is not essential for the chaperone activity. J. Biol. Chem. 277, 47160-47166. doi: 10.1074/jbc. M207853200
6. Biter, A. B., Lee, J., Sung, N., Tsai, F. T., and Lee, S. (2012). Functional analysis of conserved cis-and trans-elements in the Hsp104 protein disaggregating machine. J. Struct. Biol. 179, 172-180. doi: 10.1016/j.jsb.2012.05.007
7. Burton, R. E., Siddiqui, S. M., Kim, Y. I., Baker, T. A., and Sauer, R. T. (2001). Effects of protein stability and structure on substrate processing by the ClpXP unfolding and degradation machine. EMBO J. 20, 3092-3100. doi: 10.1093/emboj/20.12.3092
8. Carroni, M., Kummer, E., Oguchi, Y., Wendler, P., Clare, D. K., Sinning, I., et al. (2014). Head-to-tail interactions of the coiled-coil domains regulate ClpB activity and cooperation with Hsp70 in protein disaggregation. Elife 3:e02481. doi: 10.7554/eLife.02481
9. del Castillo, U., Alfonso, C., Acebron, S. P., Martos, A., Moro, F., Rivas, G., et al. (2011). A quantitative analysis of the effect of nucleotides and the M domain on the association equilibrium of ClpB. Biochemistry 50, 1991-2003. doi: 10.1021/bi101670s
10. del Castillo, U., Fernandez-Higuero, J. A., Perez-Acebron, S., Moro, F., and Muga, A. (2010). Nucleotide utilization requirements that render ClpB active as a chaperone. FEBS Lett. 584, 929-934. doi: 10.1016/j.febslet.2010.01.029
11. Desantis, M. E., Leung, E. H., Sweeny, E. A., Jackrel, M. E., Cushman-Nick, M., Neuhaus-Follini, A., et al. (2012). Operational plasticity enables hsp104 to disaggregate diverse amyloid and nonamyloid clients. Cell 151, 778-793. doi: 10.1016/j.cell.2012.09.038
12. Doyle, S. M., Hoskins, J. R., and Wickner, S. (2007). Collaboration between the ClpB AAA+ remodeling protein and the DnaK chaperone system. Proc. Natl. Acad. Sci. U.S.A. 104, 11138-11144. doi: 10.1073/pnas.0703980104
13. Doyle, S. M., Hoskins, J. R., and Wickner, S. (2012). DnaK chaperone-dependent disaggregation by caseinolytic peptidase B (ClpB) mutants reveals functional overlap in the N-terminal domain and nucleotide-binding domain-1 pore tyrosine. J. Biol. Chem. 287, 28470-28479. doi: 10.1074/jbc. M112.383091
14. Fernandez-Higuero, J. A., Acebron, S. P., Taneva, S. G., del Castillo, U., Moro, F., and Muga, A. (2011). Allosteric communication between the nucleotide binding domains of caseinolytic peptidase B. J. Biol. Chem. 286, 25547-25555. doi: 10.1074/jbc. M111.231365
15. Franzmann, T. M., Czekalla, A., and Walter, S. G. (2011). Regulatory circuits of the AAA+ disaggregase Hsp104. J. Biol. Chem. 286, 17992-18001. doi: 10.1074/jbc. M110.216176
16. Glover, J. R., and Lindquist, S. (1998). Hsp104, Hsp70, and Hsp40: a novel chaperone system that rescues previously aggregated proteins. Cell 94, 73-82. doi: 10.1016/S0092-8674(00)81223-4
17. Glynn, S. E., Martin, A., Nager, A. R., Baker, T. A., and Sauer, R. T. (2009). Structures of asymmetric ClpX hexamers reveal nucleotide-dependent motions in a AAA+ protein-unfolding machine. Cell 139, 744-756. doi: 10.1016/j.cell.2009.09.034
18. Goloubinoff, P., Mogk, A., Peres Ben Zvi, A., Tomoyasu, T., and Bukau, B. (1999). Sequential mechanism of solubilization and refolding of stable protein aggregates by a bichaperone network. Proc. Natl. Acad. Sci. U.S.A. 96, 13732-13737. doi: 10.1073/pnas.96.24.13732
19. Grimminger, V., Richter, K., Imhof, A., Buchner, J., and Walter, S. (2004). The prion curing agent guanidinium chloride specifically inhibits ATP hydrolysis by Hsp104. J. Biol. Chem. 279, 7378-7383. doi: 10.1074/jbc. M312403200
20. Haslberger, T., Weibezahn, J., Zahn, R., Lee, S., Tsai, F. T., Bukau, B., et al. (2007). M domains couple the ClpB threading motor with the DnaK chaperone activity. Mol. Cell 25, 247-260. doi: 10.1016/j.molcel.2006.11.008
21. Haslberger, T., Zdanowicz, A., Brand, I., Kirstein, J., Turgay, K., Mogk, A., et al. (2008). Protein disaggregation by the AAA+ chaperone ClpB involves partial threading of looped polypeptide segments. Nat. Struct. Mol. Biol. 15, 641-650. doi: 10.1038/nsmb.1425
22. Hattendorf, D. A., and Lindquist, S. L. (2002). Cooperative kinetics of both Hsp104 ATPase domains and interdomain communication revealed by AAA sensor-1 mutants. EMBO J. 21, 12-21. doi: 10.1093/emboj/21.1.12
23. Hersch, G. L., Burton, R. E., Bolon, D. N., Baker, T. A., and Sauer, R. T. (2005). Asymmetric Interactions of ATP with the AAA+ ClpX(6) unfoldase: allosteric control of a protein machine. Cell 121, 1017-1027. doi: 10.1016/j.cell.2005.05.024
24. Higurashi, T., Hines, J. K., Sahi, C., Aron, R., and Craig, E. A. (2008). Specificity of the J-protein Sis1 in the propagation of 3 yeast prions. Proc. Natl. Acad. Sci. U.S.A. 105, 16596-16601. doi: 10.1073/pnas.0808934105
25. Hines, J. K., Li, X., Du, Z., Higurashi, T., Li, L., and Craig, E. A. (2011). [SWI], the prion formed by the chromatin remodeling factor Swi1, is highly sensitive to alterations in Hsp70 chaperone system activity. PLoS Genet. 7:e1001309. doi: 10.1371/annotation/65a80750-95f9-40a1-a509-64ee5febbaa3
26. Hong, S. W., and Vierling, E. (2000). Mutants of Arabidopsis thaliana defective in the acquisition of tolerance to high temperature stress. Proc. Natl. Acad. Sci. U.S.A. 97, 4392-4397. doi: 10.1073/pnas.97.8.4392
27. Inoue, Y., Taguchi, H., Kishimoto, A., and Yoshida, M. (2004). Hsp104 binds to yeast sup35 prion fiber but needs other factor(s) to sever it. J. Biol. Chem. 279, 52319-52323. doi: 10.1074/jbc. M408159200
28. Jackrel, M. E., Desantis, M. E., Martinez, B. A., Castellano, L. M., Stewart, R. M., Caldwell, K. A., et al. (2014). Potentiated Hsp104 variants antagonize diverse proteotoxic misfolding events. Cell 156, 170-182. doi: 10.1016/j.cell.2013.11.047
29. Kedzierska, S., Akoev, V., Barnett, M. E., and Zolkiewski, M. (2003). Structure and function of the middle domain of ClpB from Escherichia coli. Biochemistry 42, 14242-14248. doi: 10.1021/bi035573d
30. Konieczny, I., and Liberek, K. (2002). Cooperative action of Escherichia coli ClpB protein and DnaK chaperone in the activation of a replication initiation protein. J. Biol. Chem. 277, 18483-18488. doi: 10.1074/jbc. M107580200
31. Krzewska, J., Langer, T., and Liberek, K. (2001). Mitochondrial Hsp78, a member of the Clp/Hsp100 family in Saccharomyces cerevisiae, cooperates with Hsp70 in protein refolding. FEBS Lett. 489, 92-96. doi: 10.1016/S0014-5793(00)02423-6
32. Kummer, E., Oguchi, Y., Seyffer, F., Bukau, B., and Mogk, A. (2013). Mechanism of Hsp104/ClpB inhibition by prion curing Guanidinium hydrochloride. FEBS Lett. 587, 810-817. doi: 10.1016/j.febslet.2013.02.011
33. Lee, C., Schwartz, M. P., Prakash, S., Iwakura, M., and Matouschek, A. (2001). ATP-dependent proteases degrade their substrates by processively unraveling them from the degradation signal. Mol. Cell 7, 627-637. doi: 10.1016/S1097-2765(01)00209-X
34. Lee, J., Kim, J. H., Biter, A. B., Sielaff, B., Lee, S., and Tsai, F. T. (2013). Heat shock protein (Hsp) 70 is an activator of the Hsp104 motor. Proc. Natl. Acad. Sci. U.S.A. 110, 8513-8518. doi: 10.1073/pnas.1217988110
35. Lee, S., Choi, J. M., and Tsai, F. T. (2007). Visualizing the ATPase cycle in a protein disaggregating machine: structural basis for substrate binding by ClpB. Mol. Cell 25, 261-271. doi: 10.1016/j.molcel.2007.01.002
36. Lee, S., Sowa, M. E., Watanabe, Y., Sigler, P. B., Chiu, W., Yoshida, M., et al. (2003). The Structure of ClpB. A molecular chaperone that rescues proteins from an aggregated state. Cell 115, 229-240. doi: 10.1016/S0092-8674(03)00807-9
37. Lipinska, N., Zietkiewicz, S., Sobczak, A., Jurczyk, A., Potocki, W., Morawiec, E., et al. (2013). Disruption of ionic interactions between the nucleotide binding domain 1 (NBD1) and middle (M) domain in Hsp100 disaggregase unleashes toxic hyperactivity and partial independence from Hsp70. J. Biol. Chem. 288, 2857-2869. doi: 10.1074/jbc. M112.387589
38. Liu, Z., Tek, V., Akoev, V., and Zolkiewski, M. (2002). Conserved amino acid residues within the amino-terminal domain of ClpB are essential for the chaperone activity. J. Mol. Biol. 321, 111-120. doi: 10.1016/S0022-2836(02)00591-0
39. Lum, R., Tkach, J. M., Vierling, E., and Glover, J. R. (2004). Evidence for an unfolding/threading mechanism for protein disaggregation by Saccharomyces cerevisiae Hsp104. J. Biol. Chem. 279, 29139-29146. doi: 10.1074/jbc. M403777200
40. Maillard, R. A., Chistol, G., Sen, M., Righini, M., Tan, J., Kaiser, C. M., et al. (2011). ClpX(P) generates mechanical force to unfold and translocate its protein substrates. Cell 145, 459-469. doi: 10.1016/j.cell.2011.04.010
41. Martin, A., Baker, T. A., and Sauer, R. T. (2005). Rebuilt AAA+ motors reveal operating principles for ATP-fuelled machines. Nature 437, 1115-1120. doi: 10.1038/nature04031
42. Miot, M., Reidy, M., Doyle, S. M., Hoskins, J. R., Johnston, D. M., Genest, O., et al. (2011). Species-specific collaboration of heat shock proteins (Hsp) 70 and 100 in thermotolerance and protein disaggregation. Proc. Natl. Acad. Sci. U.S.A. 108, 6915-6920. doi: 10.1073/pnas.1102828108
43. Mizuno, S., Nakazaki, Y., Yoshida, M., and Watanabe, Y. H. (2012). Orientation of the amino-terminal domain of ClpB affects the disaggregation of the protein. FEBS J. 279, 1474-1484. doi: 10.1111/j.1742-4658.2012.08540.x
44. Mogk, A., Schlieker, C., Strub, C., Rist, W., Weibezahn, J., and Bukau, B. (2003). Roles of individual domains and conserved motifs of the AAA+ chaperone ClpB in oligomerization, ATP-hydrolysis and chaperone activity. J. Biol. Chem. 278, 15-24. doi: 10.1074/jbc. M209686200
45. Morimoto, R. I. (2011). The heat shock response: systems biology of proteotoxic stress in aging and disease. Cold Spring Harb. Symp. Quant. Biol. 76, 91-99. doi: 10.1101/sqb.2012.76.010637
46. Motohashi, K., Watanabe, Y., Yohda, M., and Yoshida, M. (1999). Heat-inactivated proteins are rescued by the DnaK.J-GrpE set and ClpB chaperones. Proc. Natl. Acad. Sci. U.S.A. 96, 7184-7189. doi: 10.1073/pnas.96.13.7184
47. Neuwald, A. F., Aravind, L., Spouge, J. L., and Koonin, E. V. (1999). AAA+: a class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes. Genome Res. 9, 27-43
48. Oguchi, Y., Kummer, E., Seyffer, F., Berynskyy, M., Anstett, B., Zahn, R., et al. (2012). A tightly regulated molecular toggle controls AAA+ disaggregase. Nat. Struct. Mol. Biol. 19, 1338-1346. doi: 10.1038/nsmb.2441
49. Queitsch, C., Hong, S. W., Vierling, E., and Lindquist, S. (2000). Heat shock protein 101 plays a crucial role in thermotolerance in Arabidopsis. Plant Cell 12, 479-492. doi: 10.1105/tpc.12.4.479
50. Reidy, M., Miot, M., and Masison, D. C. (2012). Prokaryotic chaperones support yeast prions and thermotolerance and define disaggregation machinery interactions. Genetics 192, 185-193. doi: 10.1534/genetics.112.142307
51. Reidy, M., Sharma, R., Shastry, S., Roberts, B. L., Albino-Flores, I., Wickner, S., et al. (2014). Hsp40s specify functions of hsp104 and hsp90 protein chaperone machines. PLoS Genet. 10:e1004720. doi: 10.1371/journal.pgen.1004720
52. Rosenzweig, R., Moradi, S., Zarrine-Afsar, A., Glover, J. R., and Kay, L. E. (2013). Unraveling the mechanism of protein disaggregation through a ClpB-DnaK interaction. Science 339, 1080-1083. doi: 10.1126/science.1233066
53. Sanchez, Y., and Lindquist, S. L. (1990). HSP104 required for induced thermotolerance. Science 248, 1112-1115. doi: 10.1126/science.2188365
54. Satpute-Krishnan, P., Langseth, S. X., and Serio, T. R. (2007). Hsp104-dependent remodeling of prion complexes mediates protein-only inheritance. PLoS Biol. 5:e24. doi: 10.1371/journal.pbio.0050024
55. Schirmer, E. C., Homann, O. R., Kowal, A. S., and Lindquist, S. (2004). Dominant gain-of-function mutations in Hsp104p reveal crucial roles for the middle region. Mol. Biol. Cell 15, 2061-2072. doi: 10.1091/mbc. E02-08-0502
56. Schirmer, E. C., Ware, D. M., Queitsch, C., Kowal, A. S., and Lindquist, S. L. (2001). Subunit interactions influence the biochemical and biological properties of Hsp104. Proc. Natl. Acad. Sci. U.S.A. 98, 914-919. doi: 10.1073/pnas.98.3.914
57. Schlee, S., Groemping, Y., Herde, P., Seidel, R., and Reinstein, J. (2001). The chaperone function of ClpB from Thermus thermophilus depends on allosteric interactions of its two ATP-binding sites. J. Mol. Biol. 306, 889-899. doi: 10.1006/jmbi.2001.4455
58. Schlieker, C., Weibezahn, J., Patzelt, H., Tessarz, P., Strub, C., Zeth, K., et al. (2004). Substrate recognition by the AAA+ chaperone ClpB. Nat. Struct. Mol. Biol. 11, 607-615. doi: 10.1038/nsmb787
59. Sen, M., Maillard, R. A., Nyquist, K., Rodriguez-Aliaga, P., Presse, S., Martin, A., et al. (2013). The ClpXP protease unfolds substrates using a constant rate of pulling but different gears. Cell 155, 636-646. doi: 10.1016/j.cell.2013.09.022
60. Seyffer, F., Kummer, E., Oguchi, Y., Winkler, J., Kumar, M., Zahn, R., et al. (2012). Hsp70 proteins bind Hsp100 regulatory M domains to activate AAA+ disaggregase at aggregate surfaces. Nat. Struct. Mol. Biol. 19, 1347-1355. doi: 10.1038/nsmb.2442
61. Shorter, J., and Lindquist, S. (2004). Hsp104 catalyzes formation and elimination of self-replicating Sup35 prion conformers. Science 304, 1793-1797. doi: 10.1126/science.1098007
62. Shorter, J., and Lindquist, S. (2005). Prions as adaptive conduits of memory and inheritance. Nat. Rev. Genet. 6, 435-450. doi: 10.1038/nrg1616
63. Shorter, J., and Lindquist, S. (2006). Destruction or potentiation of different prions catalyzed by similar Hsp104 remodeling activities. Mol. Cell 23, 425-438. doi: 10.1016/j.molcel.2006.05.042
64. Sielaff, B., and Tsai, F. T. (2010). The M-domain controls Hsp104 protein remodeling activity in an Hsp70/Hsp40-dependent manner. J. Mol. Biol. 402, 30-37. doi: 10.1016/j.jmb.2010.07.030
65. Smith, D. M., Fraga, H., Reis, C., Kafri, G., and Goldberg, A. L. (2011). ATP binds to proteasomal ATPases in pairs with distinct functional effects, implying an ordered reaction cycle. Cell 144, 526-538. doi: 10.1016/j.cell.2011.02.005
66. Squires, C. L., Pedersen, S., Ross, B. M., and Squires, C. (1991). ClpB is the Escherichia coli heat shock protein F84.1. J. Bacteriol. 173, 4254-4262
67. Stinson, B. M., Nager, A. R., Glynn, S. E., Schmitz, K. R., Baker, T. A., and Sauer, R. T. (2013). Nucleotide binding and conformational switching in the hexameric ring of a AAA+ Machine. Cell 153, 628-639. doi: 10.1016/j.cell.2013.03.029
68. Sweeny, E. A., Jackrel, M. E., Go, M. S., Sochor, M. A., Razzo, B. M., Desantis, M. E., et al. (2015). The hsp104 N-terminal domain enables disaggregase plasticity and potentiation. Mol. Cell 57, 836-849. doi: 10.1016/j.molcel.2014.12.021
69. Tessarz, P., Mogk, A., and Bukau, B. (2008). Substrate threading through the central pore of the Hsp104 chaperone as a common mechanism for protein disaggregation and prion propagation. Mol. Microbiol. 68, 87-97. doi: 10.1111/j.1365-2958.2008.06135.x
70. Tipton, K. A., Verges, K. J., and Weissman, J. S. (2008). In vivo monitoring of the prion replication cycle reveals a critical role for Sis1 in delivering substrates to Hsp104. Mol. Cell 32, 584-591. doi: 10.1016/j.molcel.2008.11.003
71. Watanabe, Y. H., Motohashi, K., and Yoshida, M. (2002). Roles of the two ATP binding sites of ClpB from Thermus thermophilus. J. Biol. Chem. 277, 5804-5809. doi: 10.1074/jbc. M109349200
72. Weibezahn, J., Tessarz, P., Schlieker, C., Zahn, R., Maglica, Z., Lee, S., et al. (2004). Thermotolerance requires refolding of aggregated proteins by substrate translocation through the central pore of ClpB. Cell 119, 653-665. doi: 10.1016/j.cell.2004.11.027
73. Wendler, P., Shorter, J., Plisson, C., Cashikar, A. G., Lindquist, S., and Saibil, H. R. (2007). Atypical AAA+ subunit packing creates an expanded cavity for disaggregation by the protein-remodeling factor Hsp104. Cell 131, 1366-1377. doi: 10.1016/j.cell.2007.10.047
74. Wendler, P., Shorter, J., Snead, D., Plisson, C., Clare, D. K., Lindquist, S., et al. (2009). Motor mechanism for protein threading through Hsp104. Mol. Cell 34, 81-92. doi: 10.1016/j.molcel.2009.02.026
75. Werbeck, N. D., Schlee, S., and Reinstein, J. (2008). Coupling and dynamics of subunits in the hexameric AAA+ chaperone ClpB. J. Mol. Biol. 378, 178-190. doi: 10.1016/j.jmb.2008.02.026
76. Winkler, J., Tyedmers, J., Bukau, B., and Mogk, A. (2012). Hsp70 targets Hsp100 chaperones to substrates for protein disaggregation and prion fragmentation. J. Cell Biol. 198, 387-404. doi: 10.1083/jcb.201201074
77. Woo, K. M., Kim, K. I., Goldberg, A. L., Ha, D. B., and Chung, C. H. (1992). The heat-shock protein ClpB in Escherichia coli is a protein-activated ATPase. J. Biol. Chem. 267, 20429-20434
78. Yakamavich, J. A., Baker, T. A., and Sauer, R. T. (2008). Asymmetric nucleotide transactions of the HslUV protease. J. Mol. Biol. 380, 946-957. doi: 10.1016/j.jmb.2008.05.070
79. Yamasaki, T., Nakazaki, Y., Yoshida, M., and Watanabe, Y. H. (2011). Roles of conserved arginines in ATP-binding domains of AAA+ chaperone ClpB from Thermus thermophilus. FEBS J. 278, 2395-2403. doi: 10.1111/j.1742-4658.2011.08167.x
80. Yamasaki, T., Oohata, Y., Nakamura, T., and Watanabe, Y. H. (2015). Analysis of the cooperative ATPase Cycle of the AAA+ Chaperone ClpB from Thermus thermophilus by using ordered heterohexamers with an alternating subunit arrangement. J. Biol. Chem. 290, 9789-9800. doi: 10.1074/jbc. M114.617696
81. Yuan, A. H., Garrity, S. J., Nako, E., and Hochschild, A. (2014). Prion propagation can occur in a prokaryote and requires the ClpB chaperone. Elife 3:e02949. doi: 10.7554/eLife.02949
82. Zeymer, C., Fischer, S., and Reinstein, J. (2014). trans-Acting arginine residues in the AAA+ chaperone ClpB allosterically regulate the activity through inter-and intradomain communication. J. Biol. Chem. 289, 32965-32976. doi: 10.1074/jbc. M114.608828
83. Zeymer, C., Werbeck, N. D., Schlichting, I., and Reinstein, J. (2013). The molecular mechanism of Hsp100 chaperone inhibition by the prion curing agent guanidinium chloride. J. Biol. Chem. 288, 7065-7076. doi: 10.1074/jbc. M112.432583
84. Zietkiewicz, S., Krzewska, J., and Liberek, K. (2004). Successive and synergistic action of the Hsp70 and Hsp100 chaperones in protein disaggregation. J. Biol. Chem. 279, 44376-44383. doi: 10.1074/jbc. M402405200
85. Zolkiewski, M. (1999). ClpB cooperates with DnaK, DnaJ, and GrpE in suppressing protein aggregation. A novel multi-chaperone system from Escherichia coli. J. Biol. Chem. 274, 28083-28086. doi: 10.1074/jbc.274.40.28083