Fol. Biol. 2024, 70, 152-165
https://doi.org/10.14712/fb2024070030152
Heat Shock Protein Network: the Mode of Action, the Role in Protein Folding and Human Pathologies
References
1. , S.-G., Kim, S.-A., Yoon, J.-H. et al. (2005) Heat-shock cognate 70 is required for the activation of heat-shock factor 1 in mammalian cells. Biochem. J. 392, 145-152.
<https://doi.org/10.1042/BJ20050412>
2. , M. D., Hogan, D. J., Pechmann, S. et al. (2011) Defining the specificity of cotranslationally acting chaperones by systematic analysis of mRNAs associated with ribosome-nascent chain complexes. PLoS Biol. 9, e1001100.
<https://doi.org/10.1371/journal.pbio.1001100>
3. , V., Reissmann, S., Frydman, J. (2010) A ribosome-anchored chaperone network that facilitates eukaryotic ribosome biogenesis. J. Cell Biol. 189, 69-81.
<https://doi.org/10.1083/jcb.201001054>
4. , S., Sueksakit, K., Fong-Ngern, K. et al. (2017) Role of HSP60 (HSPD1) in diabetes-induced renal tubular dysfunction: regulation of intracellular protein aggregation, ATP production, and oxidative stress. FASEB J. 31, 2157-2167.
<https://doi.org/10.1096/fj.201600910RR>
5. , G. J., Morgan, J. R., Villalba-Galea, C. A. et al. (2006) Clathrin and synaptic vesicle endocytosis: studies at the squid giant synapse. Biochem. Soc. Trans. 34, 68-72.
<https://doi.org/10.1042/BST0340068>
6. , B., Stancovski, I., Mayer, A. et al. (1997) Ubiquitin-dependent degradation of certain protein substrates in vitro requires the molecular chaperone Hsc70. J. Biol. Chem. 272, 9002-9010.
<https://doi.org/10.1074/jbc.272.14.9002>
7. , A., Benomar, A., Bouslam, N. et al. (2005) Mutation in the epsilon subunit of the cytosolic chaperonin-containing t-complex peptide-1 (Cct5) gene causes autosomal recessive mutilating sensory neuropathy with spastic paraplegia. J. Med. Genet. 43, 441-443.
<https://doi.org/10.1136/jmg.2005.039230>
8. , M., Voisine, C., Rolland, T. et al. (2014) A chaperome subnetwork safeguards proteostasis in aging and neurodegenerative disease. Cell Rep. 9, 1135-1150.
<https://doi.org/10.1016/j.celrep.2014.09.042>
9. , J. D., Onuchic, J. N., Socci, N. D. et al. (1995) Funnels, pathways, and the energy landscape of protein folding: a synthesis. Proteins 21, 167-195.
<https://doi.org/10.1002/prot.340210302>
10. , B., Morimoto, R. I. (2012) Protein homeostasis as a therapeutic target for diseases of protein conformation. Curr. Top. Med. Chem. 12, 2623-2640.
<https://doi.org/10.2174/1568026611212220014>
11. , T. G., Welch, W. J., Schlossman, D. M. et al. (1986) Uncoating ATPase is a member of the 70 kilodalton family of stress proteins. Cell 45, 3-13.
<https://doi.org/10.1016/0092-8674(86)90532-5>
12. , B., Piel, W. H., Gui, L. et al. (2005) The HSP90 family of genes in the human genome: insights into their divergence and evolution. Genomics 86, 627-637.
<https://doi.org/10.1016/j.ygeno.2005.08.012>
13. , X., Glytsou, C., Zhou, H. et al. (2019) Targeting mitochondrial structure sensitizes acute myeloid leukemia to venetoclax treatment. Cancer Discov. 9, 890-909.
<https://doi.org/10.1158/2159-8290.CD-19-0117>
14. , D. R., Calderwood, S. K. (2005) Heat shock proteins in cancer: diagnostic, prognostic, predictive, and treatment implications. Cell Stress Chaperones 10, 86.
<https://doi.org/10.1379/CSC-99r.1>
15. , D., Ecroyd, H. (2017) The small heat shock proteins αB-crystallin (HSPB5) and Hsp27 (HSPB1) inhibit the intracellular aggregation of α-synuclein. Cell Stress Chaperones 22, 589-600.
<https://doi.org/10.1007/s12192-017-0785-x>
16. , E. A. (2018) Hsp70 at the membrane: driving protein translocation. BMC Biol. 16, 11.
<https://doi.org/10.1186/s12915-017-0474-3>
17. , J. M., Behringer, R. R. (1995) An insertional mutation in theBTF3 transcription factor gene leads to an early postimplantation lethality in mice. Transgenic Res. 4, 264-269.
<https://doi.org/10.1007/BF01969120>
18. , C., Carroni, M., Franke, K. B. et al. (2017) Structural pathway of regulated substrate transfer and threading through an Hsp100 disaggregase. Sci. Adv. 3, e1701726.
<https://doi.org/10.1126/sciadv.1701726>
19. , C., Eriksen, J., Kamal, A. et al. (2005) Development of a high throughput drug screening assay for the detection of changes in tau levels – proof of concept with HSP90 inhibitors. Curr. Alzheimer Res. 2, 231-238.
<https://doi.org/10.2174/1567205053585927>
20. , K. A., Bromberg, S., Yue, K. et al. (1995) Principles of protein folding – a perspective from simple exact models. Protein Sci. 4, 561-602.
<https://doi.org/10.1002/pro.5560040401>
21. , L., Löwe, J., Stock, D. et al. (1998) Crystal structure of the thermosome, the archaeal chaperonin and homolog of CCT. Cell 93, 125-138.
<https://doi.org/10.1016/S0092-8674(00)81152-6>
22. , C. M., Šali, A., Karplus, M. (1998) Protein folding: a perspective from theory and experiment. Angew. Chem. Int. Ed. Engl. 37, 868-893.
<https://doi.org/10.1002/(SICI)1521-3773(19980420)37:7<868::AID-ANIE868>3.0.CO;2-H>
23. , F., Netzer, W. J., Tanemura, K. et al. (2003) Chaperones increase association of tau protein with microtubules. Proc. Natl. Acad. Sci. U.S.A. 100, 721-726.
<https://doi.org/10.1073/pnas.242720499>
24. , J. (1987) Proteins as molecular chaperones. Nature 328, 378-379.
<https://doi.org/10.1038/328378a0>
25. , D. U., Hegler, J. A., Komives, E. A. et al. (2007) Localizing frustration in native proteins and protein assemblies. Proc. Natl. Acad. Sci. U.S.A. 104, 19819-19824.
<https://doi.org/10.1073/pnas.0709915104>
26. , G. C., Pohl, J., Flocco, M. T. et al. (1991) Peptide-binding specificity of the molecular chaperone BiP. Nature 353, 726-730.
<https://doi.org/10.1038/353726a0>
27. , V., Kapulkin, W. J., Taft, A. et al. (2002) Interaction of intracellular β amyloid peptide with chaperone proteins. Proc. Natl. Acad. Sci. U.S.A. 99, 9439-9444.
<https://doi.org/10.1073/pnas.152313999>
28. , J., Hartl, F. U. (1996) Principles of chaperone-assisted protein folding: differences between in vitro and in vivo mechanisms. Science 272, 1497-1502.
<https://doi.org/10.1126/science.272.5267.1497>
29. J., Nimmesgern E., Ohtsuka, K. et al. (1994) Folding of nascent polypeptide chains in a high molecular mass assembly with molecular chaperones. Nature 370, 111-117.
<https://doi.org/10.1038/370111a0>
30. , Y., Thomas, J. O., Chow, R. L. et al. (1992) A cytoplasmic chaperonin that catalyzes β-actin folding. Cell 69, 1043-1050.
<https://doi.org/10.1016/0092-8674(92)90622-J>
31. , M., Marienhagen, J., Eichholtz-Wirth, H. et al. (2005) Dual function of membrane-bound heat shock protein 70 (Hsp70), Bag-4, and Hsp40: protection against radiation-induced effects and target structure for natural killer cells. Cell Death Differ. 12, 38-51.
<https://doi.org/10.1038/sj.cdd.4401510>
32. , R., Taguwa, S., Frydman, J. (2012) Broad action of Hsp90 as a host chaperone required for viral replication. Biochim. Biophys. Acta 1823, 698-706.
<https://doi.org/10.1016/j.bbamcr.2011.11.007>
33. , P., Georgopoulos, C., Kelley, W. L. (2007) The Hsp70 chaperone machines of Escherichia coli: a paradigm for the repartition of chaperone functions. Mol. Microbiol. 66, 840-857.
<https://doi.org/10.1111/j.1365-2958.2007.05961.x>
34. , D., Roh, S. H., Ma, B. et al. (2019) The chaperonin TRiC/CCT associates with prefoldin through a conserved electrostatic interface essential for cellular proteostasis. Cell 177, 751-765.e15.
<https://doi.org/10.1016/j.cell.2019.03.012>
35. , M.-J., Sambrook, J. (1992) Protein folding in the cell. Nature 355, 33-45.
<https://doi.org/10.1038/355033a0>
36. , N., Perng, M. D., Quinlan, R. A. et al. (2000) Comparison of the small heat shock proteins αB-crystallin, MKBP, HSP25, HSP20, and cvHSP in heart and skeletal muscle. Histochem. Cell Biol. 122, 415-425.
<https://doi.org/10.1007/s00418-004-0711-z>
37. , S. F., Marahiel, M. A. (1999) Peptidyl-prolyl cis-trans isomerases, a superfamily of ubiquitous folding catalysts. Cell. Mol. Life Sci. 55, 423-436.
<https://doi.org/10.1007/s000180050299>
38. , E., Yokota, S., Yamamoto, S. et al. (2015) Geranylgeranylacetone selectively binds to the HSP70 of Helicobacter pylori and alters its coccoid morphology. Sci. Rep. 5, 13738.
<https://doi.org/10.1038/srep13738>
39. , S., Lumia, V., Creti, R. et al. (1999) Discontinuous occurrence of the hsp70 (dnaK) gene among Archaea and sequence features of HSP70 suggest a novel outlook on phylogenies inferred from this protein. J. Bacteriol. 181, 434-443.
<https://doi.org/10.1128/JB.181.2.434-443.1999>
40. , I. G., Wabl M. (1983) Immunoglobulin heavy chain binding protein. Nature 306, 387-389.
<https://doi.org/10.1038/306387a0>
41. , J. J., Dürr, A., Cournu-Rebeix, I. et al. (2002) Hereditary spastic paraplegia SPG13 is associated with a mutation in the gene encoding the mitochondrial chaperonin Hsp60. Am. J. Hum. Genet. 70, 1328-1332.
<https://doi.org/10.1086/339935>
42. , F. U., Bracher, A., Hayer-Hartl, M. (2011) Molecular chaperones in protein folding and proteostasis. Nature 475, 324-332.
<https://doi.org/10.1038/nature10317>
43. , M., Franzmann, T., Weinfurtner, D. et al. (2005) Some like it hot: the structure and function of small heat-shock proteins. Nat. Struct. Mol. Biol. 12, 842-846.
<https://doi.org/10.1038/nsmb993>
44. , S. M., Woolford, C., Van Der Vies, S. M. et al. (1988) Homologous plant and bacterial proteins chaperone oligomeric protein assembly. Nature 333, 330-334.
<https://doi.org/10.1038/333330a0>
45. , J. P., Hartl, F.-U. (1993) Molecular chaperone functions of heat-shock proteins. Annu. Rev. Biochem. 62, 349-384.
<https://doi.org/10.1146/annurev.bi.62.070193.002025>
46. , S. E., Aisner, D. L., Baur, J. et al. (1999) Functional requirement of p23 and Hsp90 in telomerase complexes. Genes Dev. 13, 817-826.
<https://doi.org/10.1101/gad.13.7.817>
47. , W. A., O’Malley, K. L. (2003) Parkinsonian mimetics induce aspects of unfolded protein response in death of dopaminergic neurons. J. Biol. Chem. 278, 19367-19377.
<https://doi.org/10.1074/jbc.M211821200>
48. , A. L., Fenton, W. A., Chapman E. et al. (2007) Two families of chaperonin: physiology and mechanism. Annu. Rev. Cell Dev. Biol. 23, 115-145.
<https://doi.org/10.1146/annurev.cellbio.23.090506.123555>
49. , G., Tang, J., Zhang, B. et al. (2006) A novel endothelial-specific heat shock protein HspA12B is required in both zebrafish development and endothelial functions in vitro. J. Cell Sci. 119, 4117-4126.
<https://doi.org/10.1242/jcs.03179>
50. , H. A., Walter, W., Bairstow S. et al. (2005) Human Mpp11 J protein: ribosome-tethered molecular chaperones are ubiquitous. Science 308, 1032-1034.
<https://doi.org/10.1126/science.1109247>
51. , T. S., Han, H. S., Choi, H. K. et al. (2003) Differential, stage‐dependent expression of Hsp70, Hsp110 and Bcl‐2 in colorectal cancer. J. Gastroenterol. Hepatol. 18, 690-700.
<https://doi.org/10.1046/j.1440-1746.2003.03011.x>
52. , T. R., Radford, S. E. (2005) The yin and yang of protein folding. FEBS J. 272, 5962-5970.
<https://doi.org/10.1111/j.1742-4658.2005.05021.x>
53. , U., Gaestel, M., Engel, K. et al. (1993) Small heat shock proteins are molecular chaperones. J. Biol. Chem. 268, 1517-1520.
<https://doi.org/10.1016/S0021-9258(18)53882-5>
54. , K., Taldone, T., Modi, S. et al. (2012) Advances in the clinical development of heat shock protein 90 (Hsp90) inhibitors in cancers. Biochim. Biophys. Acta 1823, 742-755.
<https://doi.org/10.1016/j.bbamcr.2011.10.008>
55. , Y., Rossi, P., Kalodimos, C. G. (2019) Structural basis for client recognition and activity of Hsp40 chaperones. Science 365, 1313-1319.
<https://doi.org/10.1126/science.aax1280>
56. , C. J. O., Peters, C., Schmid, P. W. N. et al. (2019) The structure and oxidation of the eye lens chaperone αA-crystallin. Nat. Struct. Mol. Biol. 26, 1141-1150.
<https://doi.org/10.1038/s41594-019-0332-9>
57. , H. H., Bergink, S. (2016) Heat shock proteins as potential targets for protective strategies in neurodegeneration. Lancet Neurol. 15, 748-759.
<https://doi.org/10.1016/S1474-4422(16)00099-5>
58. , R., Kopp, J., Mayer, M. P. (2018) Molecular mechanism of J-domain-triggered ATP hydrolysis by Hsp70 chaperones. Mol. Cell 69, 227-237.e4.
<https://doi.org/10.1016/j.molcel.2017.12.003>
59. , A., Preissler, S., Ilina, Y. et al. (2010) A dual function for chaperones SSB-RAC and the NAC nascent polypeptide-associated complex on ribosomes. J. Cell Biol. 189, 57-68.
<https://doi.org/10.1083/jcb.200910074>
60. , G., Hoffmann, R., Chattergoon, M. A. et al. (2002) Identification of crucial residues for the antibacterial activity of the proline‐rich peptide, pyrrhocoricin. Eur. J. Biochem. 269, 4226-4237.
<https://doi.org/10.1046/j.1432-1033.2002.03119.x>
61. , Y. C., Hiddinga, H. J., Butler, P. C. et al. (1997) Small heat shock proteins inhibit in vitro Aβ 1–42 amyloidogenesis. FEBS Lett. 416, 117-121.
<https://doi.org/10.1016/S0014-5793(97)01180-0>
62. , R. E., Maciejewski, A., Ostapchenko, V. G. et al. (2017) The Hsp70/Hsp90 chaperone machinery in neurodegenerative diseases. Front. Neurosci. 11, 254.
<https://doi.org/10.3389/fnins.2017.00254>
63. , G. J., Roseman, A. M., Saibil, H. R. et al. (1997) A small heat shock protein stably binds heat-denatured model substrates and can maintain a substrate in a folding-competent state. EMBO J. 16, 659-671.
<https://doi.org/10.1093/emboj/16.3.659>
64. , J. H., Won, S. M., Suh, J. et al. (2010) Induction of the unfolded protein response and cell death pathway in Alzheimer’s disease, but not in aged Tg2576 mice. Exp. Mol. Med. 42, 386.
<https://doi.org/10.3858/emm.2010.42.5.040>
65. , G. D., Alexiou, G. A., Mangano, A. et al. (2015) The role of heat shock proteins in cancer. Cancer Lett. 360, 114-118.
<https://doi.org/10.1016/j.canlet.2015.02.026>
66. , S., Craig, E. A. (1988) The heat-shock proteins. Annu. Rev. Genet. 22, 631-677.
<https://doi.org/10.1146/annurev.ge.22.120188.003215>
67. , T., Houry, W. A. (2012) The role of Hsp90 in protein complex assembly. Biochim. Biophys. Acta 1823, 674-682.
<https://doi.org/10.1016/j.bbamcr.2011.09.001>
68. , D. C., Gajewski, K. M., Nazimiec, M. E. et al. (2000) bicaudal encodes the Drosophila beta NAC homolog, a component of the ribosomal translational machinery*. Development 127, 559-572.
<https://doi.org/10.1242/dev.127.3.559>
69. , M. P. (2021) The Hsp70-chaperone machines in bacteria. Front. Mol. Biosci. 8, 694012.
<https://doi.org/10.3389/fmolb.2021.694012>
70. , M. P., Bukau, B. (2005) Hsp70 chaperones: cellular functions and molecular mechanism. Cell. Mol. Life Sci. 62, 670-684.
<https://doi.org/10.1007/s00018-004-4464-6>
71. , A. A., Kanon, B., Konings, A. W. T. et al. (1997) Hsp70 and Hsp40 chaperone activities in the cytoplasm and the nucleus of mammalian cells. J. Biol. Chem. 272, 33283-33289.
<https://doi.org/10.1074/jbc.272.52.33283>
72. , W., Angileri, F., Luo, H. et al. (2014) A human CCT5 gene mutation causing distal neuropathy impairs hexadecamer assembly in an archaeal model. Sci. Rep. 4, 6688.
<https://doi.org/10.1038/srep06688>
73. , R., Wu, K., Lee, C. et al. (2022) ATP-independent chaperones. Annu. Rev. Biophys. 51, 409-429.
<https://doi.org/10.1146/annurev-biophys-090121-082906>
74. , L. A., Chang, C., Garrels, J. I. et al. (1989) Identification, characterization, and purification of two mammalian stress proteins present in mitochondria, grp 75, a member of the hsp 70 family and hsp 58, a homolog of the bacterial groEL protein. J. Biol. Chem. 264, 20664-20675.
<https://doi.org/10.1016/S0021-9258(19)47115-9>
75. , A., Deuerling, E., Vorderwülbecke, S. et al. (2003) Small heat shock proteins, ClpB and the DnaK system form a functional triade in reversing protein aggregation. Mol. Microbiol. 50, 585-595.
<https://doi.org/10.1046/j.1365-2958.2003.03710.x>
76. , T., Kityk, R., Mayer, M. P. et al. (2018) Hsp90 breaks the deadlock of the Hsp70 chaperone system. Mol. Cell 70, 545-552.e9.
<https://doi.org/10.1016/j.molcel.2018.03.028>
77. , R. C., Wang, H., Flynn, G. C. et al. (1995) The peptide-binding domain of the chaperone protein Hsc70 has an unusual secondary structure topology. Biochemistry 34, 6261-6266.
<https://doi.org/10.1021/bi00019a001>
78. , S., Pelham, H. R. B. (1986) An Hsp70-like protein in the ER: identity with the 78 kDa glucose-regulated protein and immunoglobulin heavy chain binding protein. Cell 46, 291-300.
<https://doi.org/10.1016/0092-8674(86)90746-4>
79. , P. N., Marchion, D. C., Basso A. D. et al. (2002) Degradation of HER2 by ansamycins induces growth arrest and apoptosis in cells with HER2 overexpression via a HER3, phosphatidylinositol 3′-kinase-AKT-dependent pathway. Cancer Res. 62, 3132-3137.
80. , L., Scharf, K.-D. (1984) Synthesis, modification and structural binding of heat-shock proteins in tomato cell cultures. Eur. J. Biochem. 139, 303-313.
<https://doi.org/10.1111/j.1432-1033.1984.tb08008.x>
81. , M., Yamamoto, S., Ogasawara, K. et al. (2007) The induction mechanism of the molecular chaperone HSP70 in the gastric mucosa by Geranylgeranylacetone (HSP-inducer). Biochem. Biophys. Res. Commun. 353, 399-404.
<https://doi.org/10.1016/j.bbrc.2006.12.031>
82. , H., Conz, C., Maier, P. et al. (2005) The chaperones MPP11 and Hsp70L1 form the mammalian ribosome-associated complex. Proc. Natl. Acad. Sci. U.S.A. 102, 10064-10069.
<https://doi.org/10.1073/pnas.0504400102>
83. , B., Prodromou, C., Roe, S. M. et al. (1998) ATP binding and hydrolysis are essential to the function of the Hsp90 molecular chaperone in vivo. EMBO J. 17, 4829-4836.
<https://doi.org/10.1093/emboj/17.16.4829>
84. , G., Wilsher, J. A., Mark Roe, S. et al. (2002) Crystal structure of the CCTγ apical domain: implications for substrate binding to the eukaryotic cytosolic chaperonin. J. Mol. Biol. 318, 1367-1379.
<https://doi.org/10.1016/S0022-2836(02)00190-0>
85. , D. A., Kowal, A. S., Lindquist, S. (1994) Saccharomyces cerevisiae Hsp104 protein. Purification and characterization of ATP-induced structural changes. J. Biol. Chem. 269, 4480-4487.
<https://doi.org/10.1016/S0021-9258(17)41804-7>
86. , D. (2002) Heat-shock protein 90, a chaperone for folding and regulation. Cell. Mol. Life Sci. 59, 1640-1648.
<https://doi.org/10.1007/PL00012491>
87. , A. G., Shepherd, J., Corton, J. M. (1998) Detection of heat shock protein 70 (HSP70) and anti-HSP70 antibodies in the serum of normal individuals. Immunol. Invest. 27, 367-377.
<https://doi.org/10.3109/08820139809022710>
88. , S., Deuerling, E. (2012) Ribosome-associated chaperones as key players in proteostasis. Trends Biochem. Sci. 37, 274-283.
<https://doi.org/10.1016/j.tibs.2012.03.002>
89. , C., Hong, S.-W., Vierling, E. et al. (2000) Heat shock protein 101 plays a crucial role in thermotolerance in arabidopsis. Plant Cell 4, 479-492.
<https://doi.org/10.1105/tpc.12.4.479>
90. , J. (2016) The human HSP70 family of chaperones: where do we stand? Cell Stress Chaperones 21, 379-404.
<https://doi.org/10.1007/s12192-016-0676-6>
91. , S., Missiakas, D. (1997) Making and breaking disulfide bonds. Annu. Rev. Microbiol. 51, 179-202.
<https://doi.org/10.1146/annurev.micro.51.1.179>
92. Ramirez-Alvarado, M., Kelly, J. W., Dobson C. M., eds. (2010) Protein Misfolding Diseases: Current and Emerging Principles and Therapies. Wiley, Hoboken.
93. , R., Nillegoda, N. B., Mayer, M. P. et al. (2019) The Hsp70 chaperone network. Nat. Rev. Mol. Cell Biol. 20, 665-680.
<https://doi.org/10.1038/s41580-019-0133-3>
94. , H. S., Burston, S. G., Fenton, W. A. et al. (1997) Distinct actions of cis and trans ATP within the double ring of the chaperonin GroEL. Nature 388, 792-798.
<https://doi.org/10.1038/42047>
95. , Y., Taulien, J., Borkovich, K. A. et al. (1992) Hsp104 is required for tolerance to many forms of stress. EMBO J. 11, 2357-2364.
<https://doi.org/10.1002/j.1460-2075.1992.tb05295.x>
96. , M., Farrell, D. W., Dill, K. A. (2017) Bacterial proteostasis balances energy and chaperone utilization efficiently. Proc. Natl. Acad. Sci. U.S.A. 114, E2654-E2661.
<https://doi.org/10.1073/pnas.1620646114>
97. , E. C., Glover, J. R., Singer M. A. et al. (1996) HSP100/Clp proteins: a common mechanism explains diverse functions. Trends Biochem. Sci. 21, 289-296.
<https://doi.org/10.1016/S0968-0004(96)10038-4>
98. , T. W., Blagosklonny, M. V., Romanova, L. et al. (1996) Destabilization of Raf-1 by geldanamycin leads to disruption of the Raf-1-MEK-mitogen-activated protein kinase signalling pathway. Mol. Cell. Biol. 16, 5839-5845.
<https://doi.org/10.1128/MCB.16.10.5839>
99. , W. P., Shore, G. C., Randall S. K. (1990) Mitochondrial precursor protein. Effects of 70-kilodalton heat shock protein on polypeptide folding, aggregation, and import competence. J. Biol. Chem. 265, 11069-11076.
<https://doi.org/10.1016/S0021-9258(19)38558-8>
100. , J., Cegielska, A., Georgopoulos, C. (1990) Role of Escherichia coli heat shock proteins DnaK and HtpG (C62.5) in response to nutritional deprivation. J. Bacteriol. 172, 7157-7166.
<https://doi.org/10.1128/jb.172.12.7157-7166.1990>
101. , C. L., Ross, B. M., Squires, C. et al. (1991) C1pB is the Escherichia coli heat shock protein F84. J. Bacteriol. 173, 4254-4262.
<https://doi.org/10.1128/jb.173.14.4254-4262.1991>
102. , M., Dobson, C. M. (2003) Protein aggregation and aggregate toxicity: new insights into protein folding, misfolding diseases and biological evolution. J. Mol. Med. 81, 678-699.
<https://doi.org/10.1007/s00109-003-0464-5>
103. , G. J. J., Renkawek, K., Overkamp, P. S. G. et al. (1999) The molecular chaperone αB-crystallin enhances amyloid β neurotoxicity. Biochem. Biophys. Res. Commun. 262, 152-156.
<https://doi.org/10.1006/bbrc.1999.1167>
104. , S. A., Houry, W. A., Ang, D. et al. (1999) Polypeptide flux through bacterial Hsp70: DnaK cooperates with trigger factor in chaperoning nascent chains. Cell 75, 755-765.
<https://doi.org/10.1016/S0092-8674(00)80787-4>
105. , X., Campos, L., Mounier, C. et al. (2005) Expression of heat-shock proteins is associated with major adverse prognostic factors in acute myeloid leukemia. Leuk. Res. 29, 1049-1058.
<https://doi.org/10.1016/j.leukres.2005.02.010>
106. , V., Fang, C. F., Frydman, J. (1999) In vivo newly translated polypeptides are sequestered in a protected folding environment. EMBO J. 18, 85-95.
<https://doi.org/10.1093/emboj/18.1.85>
107. , M. J., Viitanen, P. V., Lorimer, G. H. (1994) Dynamics of the chaperonin ATPase cycle: implications for facilitated protein folding. Science 265, 659-666.
<https://doi.org/10.1126/science.7913555>
108. , I. E., Lewis, S. A., Rommelaere, H. et al. (1998) Prefoldin, a chaperone that delivers unfolded proteins to cytosolic chaperonin. Cell 93, 863-873.
<https://doi.org/10.1016/S0092-8674(00)81446-4>
109. , M., Mayer, M. P., Bukau, B. (2006) Allosteric regulation of Hsp70 chaperones involves a conserved interdomain linker. J. Biol. Chem. 281, 38705-38711.
<https://doi.org/10.1074/jbc.M609020200>
110. , S. K., Richter, K., Buchner, J. (2008) The Hsp90 chaperone machinery. J. Biol. Chem. 283, 18473-18477.
<https://doi.org/10.1074/jbc.R800007200>
111. , H., Wandinger, S. K., Schmid, A. B. et al. (2006) Substrate transfer from the chaperone Hsp70 to Hsp90. J. Mol. Biol. 356, 802-811.
<https://doi.org/10.1016/j.jmb.2005.12.008>
112. , L., Lindquist, S. L. (2005) HSP90 and the chaperoning of cancer. Nat. Rev. Cancer 5, 761-772.
<https://doi.org/10.1038/nrc1716>
113. , H., Buchner, J., Zimmermann, R. et al. (1992) Hsp90 chaperones protein folding in vitro. Nature 358, 169-170.
<https://doi.org/10.1038/358169a0>
114. , D. B. (2006) Beyond lectins: the calnexin/calreticulin chaperone system of the endoplasmic reticulum. J. Cell Sci. 119, 615-623.
<https://doi.org/10.1242/jcs.02856>
115. , S. B., Ziętkiewicz, S., Kousi, M. et al. (2015) CLPB mutations cause 3-methylglutaconic aciduria, progressive brain atrophy, intellectual disability, congenital neutropenia, cataracts, movement disorder. Am. J. Hum. Genet. 96, 245-257.
<https://doi.org/10.1016/j.ajhg.2014.12.013>
116. , D., Liu, Y., Dai, Y. et al. (2023) Comprehensive structural characterization of the human AAA+ disaggregase CLPB in the apo- and substrate-bound states reveals a unique mode of action driven by oligomerization. PLoS Biol. 21, e3001987.
<https://doi.org/10.1371/journal.pbio.3001987>
117. , N., He, L., Cui, P. et al. (2015) Ranking of persister genes in the same Escherichia coli genetic background demonstrates varying importance of individual persister genes in tolerance to different antibiotics. Front. Microbiol. 6, 1003.
118. , Z., Horwich, A. L., Sigler, P. B. (1997) The crystal structure of the asymmetric GroEL-GroES-(ADP)7 chaperonin complex. Nature 388, 741-750.
<https://doi.org/10.1038/41944>
119. , M. B., Farr, G. W., Miklos, D. et al. (1992) TCP1 complex is a molecular chaperone in tubulin biogenesis. Nature 358, 245-248.
<https://doi.org/10.1038/358245a0>
120. , Y., Sinning, I., Rospert, S. (2017) Two chaperones locked in an embrace: structure and function of the ribosome-associated complex RAC. Nat. Struct. Mol. Biol. 24, 611-619.
<https://doi.org/10.1038/nsmb.3435>
