An overview of the role of molecular chaperones in protein homeostasis

Protein and Peptide Letters

Volumn 18, Issue 2, 2011, Pages 101-109

  Tiroli Cepeda, Ana O ^b   Ramos, Carlos H I ^a  

^a UNIVERSITY OF CAMPINAS   (Brazil)

^b Instituto Nacional de Ciencia e Tecnologia   (Brazil)

Author keywords

Heat shock protein; Molecular chaperones; Protein folding; Protein homeostasis; Protein quality control

Indexed keywords

CHAPERONE;

ANIMAL; CHEMISTRY; HOMEOSTASIS; HUMAN; METABOLISM; PHYSIOLOGY; PROTEIN FOLDING; PROTEOSTASIS DEFICIENCY; REVIEW;

ANIMALS; HOMEOSTASIS; HUMANS; MOLECULAR CHAPERONES; PROTEIN FOLDING; PROTEOSTASIS DEFICIENCIES;

EID: 79952179088     PISSN: 09298665     EISSN: None     Source Type: Journal    
DOI: 10.2174/092986611794475093     Document Type: Review

References (77)

1. Ramos, C.H.I.; Ferreira, S.T. Protein folding, misfolding and aggregation: evolving concepts and conf (Pubitemid 40428409)
2. Tompa, P. Intrinsically unstructured proteins. Trends Biochem. Sci., 2002, 27(10), 527-533. (Pubitemid 35279598)
3. Luheshi, L.M.; Crowther, D.C.; Dobson, C.M. Protein misfolding and disease: from the test tube to the organism. Curr. Opin. Chem. Biol., 2008, 12, 25-31.
4. Sunde, M.; Blake, C. C. F. The structure of amyloid fibrils by electron microscopy and X-ray diffraction. Adv. Protein Chem., 1997, 50, 123-159. (Pubitemid 27449487)
5. Dobson, C.M. Experimental investigation of protein folding and misfolding. Methods, 2004, 34, 4-14. (Pubitemid 38993205)
6. Chiti, F.; Donson, C. M. Protein misfolding, functional amyloid and human disease. Annu. Rev. Biochem., 2006, 75, 333-366. (Pubitemid 44118036)
7. Zettlmeissl, G.; Rudolph, R.; Jaenicke, R. Reconstitution of lactic dehydrogenase. Noncovalent aggregation vs. reactivation. 1. Physical properties and kinetics of aggregation. Biochemistry, 1979, 18(25), 5567-5571.
8. Radford S. E. Protein folding: progress made and promises ahead. Trends Biochem. Sci., 2000, 25, 611-618.
9. Kelly, J.W. The alternative conformations of amyloidogenic proteins and their multi-step assembly pathways. Curr Opin Struct Biol., 1998, 8, 101-106. (Pubitemid 28107921)
10. Fändrich, M.; Fletcher, M. A.; Dobson, C. M. Amyloid fibrils from muscle myoglobin. Nature, 2001, 410, 165-166.
11. Ellis, R. J. Macromolecular crowding: an important but neglected aspect of the intracellular environment. Curr. Opin. Struct. Biol., 2001, 11, 114-119. (Pubitemid 32155560)
12. Csermely, P. Chaperone overload is a possible contributor to 'civilization diseases'. Trends Genet., 2001, 17, 701-704. (Pubitemid 33097519)
13. Cajigas, I. J.; Will, T.; Schuman, E. M. Protein homeostasis and synaptic plasticity. EMBO J., 2010, 29, 2746-2752.
14. Douglas, P. M.; Cyr, D. M. Interplay between protein homeostasis networks in protein aggregation and proteotoxicity. Biopolymers, 2010, 93(3), 229-236.
15. Taipale, M.; Jarosz, D. F.; Lindquist, S. HSP90 at the hub of protein homeostasis: emerging mechanistic insights. Nat. Rev. Mol. Cell Biol., 2010, 11(7), 515-528.
16. Lindquist, S.; Craig, E. A. The heat-shock proteins. Annu. Rev. Genet., 1988, 22, 631-677. (Pubitemid 19156675)
17. Borges, J. C.; Ramos, C. H. Protein folding assisted by chaperones. Protein Pept. Lett., 2005, 12, 257-261. (Pubitemid 40428416)
18. Mayer, M. P. Gymnastics of molecular chaperones. Mol. Cell, 2010, 39(3), 321-331.
19. Slepenkov, S.V.; Witt, S.N. The unfolding story of the Escherichia coli Hsp70 DnaK: is DnaK a holdase or an unfoldase? Mol. Microbiol, 2002, 45, 1197-1206. (Pubitemid 35015345)
20. Bosl, B.; Grimminger, V.; Walter, S. The molecular chaperone Hsp104 - A molecular machine for protein disaggregation. J. Struct. Biol., 2006, 156(1), 139-148. (Pubitemid 44486053)
21. Jakob, U.; Gaestel, M.; Engel, K; Buchner, J. Small heat shock proteins are molecular chaperones. J. Biol. Chem., 1993, 265, 1517-1520. (Pubitemid 23033534)
22. Boston, S.; Viitanen, P. V.; Vierling, E. Molecular chaperones and protein folding in plants. Plant. Mol. Biol, 1996, 32, 191-222. (Pubitemid 27015358)
23. Haslbeck, M, Franzmann, T, Weinfurtner, D, Buchner, J. Some like it hot: the structure and function of small heat-shock proteins. Nat. Struct. Mol. Biol, 2005, 12(10), 842-846. (Pubitemid 41486706)
24. Li, C.; Wang, L.; Ning, X.; Chen, A.; Zhang, L.; Qin, S.; Wu, H.; Zhao, J. Identification of two small heat shock proteins with different response profile to cadmium and pathogen stresses in Venerupis philippinarum. Cell Stress Chaperones, 2010, 15, 897-904.
25. Clark, J.I.; Muchowski, P.J. Small heat-shock proteins and their potential role in human disease. Curr. Opin. Struct. Biol., 2000, 10(1), 52-59. (Pubitemid 30099327)
26. Sun, Y.; MacRae, T.H. The small heat shock proteins and their role in human disease. FEBS J., 2005, 272(11), 2613-2627. (Pubitemid 40825410)
27. Caspers, G. J.; Leunissen, J. A. M.; de Jong, W. W. The expanding small heat shock protein family and structure predictions of the conserved 'a-crystallin-domain'. J. Mol. Evol., 1995, 40, 238-248.
28. van Montfort, R. L.; Basha, E.; Friedrich, K. L.; Slingsby, C.; Vierling, E. Crystal structure and assembly of a eukaryotic small heat shock protein. Nat. Struct. Biol., 2001, 8, 1025-1030. (Pubitemid 33101621)
29. Haslbeck, M.; Ignatiou, A.; Saibil, H.; Helmich, S.; Frenzl, E.; Stromer, T.; Buchner, J. A domain in the N-terminal part of Hsp26 is essential for chaperone function and oligomerization, J. Mol. Biol., 2004, 343, 445-455. (Pubitemid 39296877)
30. Tiroli, A.O.; Ramos, C.H. Biochemical and biophysical characterization of small heat shock proteins from sugarcane. Involvement of a specific region located at the N-terminus with substrate specificity. Int. J. Biochem. Cell Biol., 2007, 39(4), 818-831. (Pubitemid 46366807)
31. Jaya, N.; Garcia, V.; Vierling, E. Substrate binding site flexibility of the small heat shock protein molecular chaperones. Proc. Natl. Acad. Sci. USA, 2009, 106(37),15604-15609 .
32. Basha, E.; Lee, G.J.; Demeler, B.; Vierling, E. Chaperone activity of cytosolic small heat shock proteins from wheat. Eur. J. Bio-chem., 2004, 271, 1426-1436. (Pubitemid 38553549)
33. Sugino, C.; Hirose, M.; Tohda, H.; Yoshinari, Y.; Abe, T.; Giga-Hama, Y.; Iizuka, R.; Shimizu, M.; Kidokoro, S.; Ishii, N.; Yohda, M. Characterization of a sHsp of Schizosaccharomyces pombe, SpHsp15.8, and the implication of its functional mechanism by comparison with another sHsp, SpHsp16.0. Proteins, 2009, 74(1), 6-17.
34. Basha, E.; Jones, C.; Wysocki, V.; Vierling, E. Mechanistic differences between two conserved classes of small heat shock proteins found in the plant cytosol. J. Biol. Chem., 2010, 285(15), 11489-11497.
35. Stengel, F.; Baldwin, A. J.; Painter, A. J.; Jaya, N.; Basha, E.; Kay, L. E.; Vierling, E.; Robinson, C. V.; Benesch, J. L. Quaternary dynamics and plasticity underlie small heat-shock protein chaperone function. Proc. Natl. Acad. Sci. USA, 2010, 107, 2007-2012.
36. Tiroli-Cepeda, A. O.; Ramos, C. H. Heat causes oligomeric disassembly and increases the chaperone activity of small heat shock proteins from sugarcane. Plant Physiol. Biochem., 2010, 48(2-3), 108-116.
37. Mayer, M. P.; Brehmer, D.; Gässler C. S.; Bukau, B. Hsp70 Chaperone Machines. Adv. Protein Chem., 2001, 50, 1-45.
38. Hartl, F. U.; Hayer-Hartl, M. Molecular chaperones in the cytosol, from nascent chain to folded protein. Science, 2002, 295, 1852-1858. (Pubitemid 34214115)
39. Wegele, H.; Müller, L.; Buchner, J. Hsp70 and Hsp90 - a relay team for protein folding. Rev. Physiol. Biochem. Pharmacol., 2004, 151, 1-44.
40. Koo, E. H.; Lansbury, P. T. Jr.; Kelly, J. W. Amyloid diseases: abnormal protein aggregation in neurodegeneration. Proc. Natl. Acad. Sci. USA, 1999, 96(18), 9989-9990. (Pubitemid 29422496)
41. Caughey, B.; Lansbury, P. T. Protofibrils, pores, fibrils, and neu-rodegeneration: separating the responsible protein aggregates from the innocent bystanders. Annu. Rev. Neurosci., 2003, 26, 267-298. (Pubitemid 37064935)
42. Cohen, F. E.; Kelly, J. W. Therapeutic approaches to protein-misfolding diseases. Nature, 2003, 426(6968), 905-909. (Pubitemid 38056884)
43. Wadhwa, R.; Takano, S.; Kaur, K.; Deocaris, C. C.; Pereira-Smith, O. M.; Reddel, R. R.; Kaul, S. C. Upregulation of mortalin/mthsp70/Grp75 contributes to human carcinogenesis. Int. J. Cancer, 2006, 118(12), 2973-2980.
44. Lu, Z. ; Cyr, D.M. Protein folding activity of Hsp70 is modified differentially by the hsp40 co-chaperones Sis1 and Ydj1. J. Biol. Chem, 1998, 273, 27824-27830. (Pubitemid 28496069)
45. Cheetham, M.E.; Caplan, A.J. Structure, function and evolutionof DnaJ: Conservation and adaption of chaperone function. Cell Stress, 1998, 3, 28-36. (Pubitemid 28159676)
46. Summers, D. W.; Douglas, P. M.; Ramos, C. H. I.; Cyr, D. M. Polypeptide transfer from Hsp40 to Hsp70 molecular chaperones. Trends Biochem. Sci., 2009, 34, 230-233.
47. Borges, J. C.; Fischer, H.; Craievich, A. F.; Ramos, C. H. I. Lowresolution structural study of two human Hsp40 chaperones in solution. DjA1 from subfamily A and DjB4 from subfamily B, have different quaternary structures. J. Biol. Chem., 2005, 280, 13671-13681. (Pubitemid 40517262)
48. Ramos, C. H. I.; Oliveira, C. L. P.; Fan, C.; Torriani, I. C.; Cyr, D. M. Conserved Central Domains Control the Quaternary Structure of Type I and Type II Hsp40 Molecular Chaperones. J. Mol. Biol., 2008, 383, 155-166.
49. Wandinger, S. K.; Richter, K.; Buchner, J. The Hsp90 chaperone machinery. J. Biol. Chem., 2008, 283, 18473-18477.
50. Russell, L. C.; Whitt, S. R.; Chen, M. S.; Chinkers, M. Identification of conserved residues required for the binding of a tetratrico-peptide repeat domain to heat shock protein 90. J Biol Chem., 1999, 274(29), 20060-20063.
51. Scheufler, C.; Brinker, A.; Bourenkov, G.; Pegoraro, S.; Moroder, L.; Bartunik, H.; Hartl, F.U.; Moarefi, I. Structure of TPR domain-peptide complexes: critical elements in the assembly of the Hsp70-Hsp90 multichaperone machine. Cell, 2000, 101, 199-210. (Pubitemid 32004747)
52. Picard, D. Heat-shock protein 90, a chaperone for folding and regulation. CMLS Cell. Mol. Life Sci., 2002, 59, 1640-1648. (Pubitemid 35346967)
53. Prodromou, C.; Pearl, L.H. Structure and functional relationships of Hsp90. Curr. Cancer Drug Targets, 2003, 3, 301-323. (Pubitemid 37128317)
54. Chiosis, G.; Vilenchik, M.; Kim, J.; Solit, D. Hsp90: the vulnerable chaperone. Drug Discov. Today, 2004, 9(20), 881-888. (Pubitemid 39314553)
55. Pearl, L. H.; Prodromou, C.; Workman, P. The Hsp90 molecular chaperone: an open and shut case for treatment. Biochem. J., 2008, 410, 439-453. (Pubitemid 351429015)
56. Gava, L.; Ramos, C. H. I. Human 90 kDa heat shock protein Hsp90 as a target for cancer therapeutics. Curr. Chem. Biol., 2009, 3, 330-341.
57. Mollapour, M.; Tsutsumi, S.; Donnelly, A. C.; Beebe, K.; Tokita, M. J.; Lee, M. J.; Lee, S.; Morra, G.; Bourboulia, D.; Scroggins, B. T.; Colombo, G.; Blagg, B. S.; Panaretou, B.; Stetler-Stevenson, W. G.; Trepel, J. B.; Piper, P. W.; Prodromou, C.; Pearl, L. H.; Neckers, L. Swe1Wee1-dependent tyrosine phosphorylation of Hsp90 regulates distinct facets of chaperone function. Mol. Cell, 2010, 37, 333-343.
58. Zolkiewski, M. A camel passes through the eye of a needle: protein unfolding activity of Clp ATPases. Mol. Microbiol,, 2006, 61, 1094-1100. (Pubitemid 44215414)
59. 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(8), 289-296. (Pubitemid 26281031)
60. Dougan, D. A.; Mogk, A.; Bukau, B. Protein folding and degradation in bacteria: to degrade or not to degrade? That is the question. Cell. Mol. Life Sci., 2002, 59, 1607-1616. (Pubitemid 35346963)
61. Glover, J. R; Lindquist, S. Hsp104, Hsp70, and Hsp40: a novel chaperone system that rescues previously aggregated proteins. Cell, 1998, 94, 73-82. (Pubitemid 28347471)
62. Goloubinoff, P.; Mogk, A.; Zvi, A.P.; Tomoyasu, T.; Bukau, B. Sequential mechanism of solubilization and refolding of stable protein aggregates by a bichaperone network. Proc. Natl. Acad. Sci. USA, 1999, 96, 13732-13737.
63. Netzer, W. J,; Hartl, F. U. Protein folding in the cytosol: chaperonin-dependent and-independent mechanisms. Trends Biochem. Sci., 1998, 23, 68-73. (Pubitemid 28085230)
64. Horwich, A. L.; Fenton, W. A. Chaperonin-mediated protein folding: using a central cavity to kinetically assist polypeptide chain folding. Q. Rev. Biophys., 2009, 42(2), 83-116.
65. Borges, J. C.; Peroto, M. C.; Ramos, C. H. I. Molecular Chaperone Genes in the SugarCane Expressed Sequence Database (SUCEST). Gen. Mol. Biol., 2001, 24, 85-92. (Pubitemid 34567311)
66. Ramos, C. H. I. Prevention of protein misfolding and aggregation by the machinery of molecular chaperones. In: Protein Misfolding. Edit. Cian B. O'Doherty e Adam C. Byrne. 2008; Nova Science Publishers ISBN: 978-1-60456-881-3.
67. Goldschmidt, L.; Teng, P. K.; Riek, R.; Eisenberg, D. Identifying the amylome, proteins capable of forming amyloid-like fibrils. Proc. Natl. Acad. Sci. USA, 2010, 107, 3487-3492.
68. Akerfelt, M.; Morimoto, R. I.; Sistonen, L. Heat shock factors: integrators of cell stress, development and lifespan. Nat. Rev. Mol. Cell Biol., 2010, 11, 545-555.
69. Lindner, A. B.; Demarez, A. Protein aggregation as a paradigm of aging. Biochim. Biophys. Acta., 2009, 1790(10), 980-996.
70. Macario, A. J. L.; de Macario, E. C. Chaperonophaties and chaper-onotherapy. FEBS Lett., 2007, 581, 3681-3688.
71. Powers, M. V.; Workman, P. Inhibitors of the heat shock response: biology and pharmacology. FEBS Lett., 2007, 581(19), 3758-3769. (Pubitemid 47081010)
72. Bonini, N. M. Chaperoning brain degeneration. Proc. Natl. Acad. Sci. USA, 2002, 99, 16407-16411. (Pubitemid 35470986)
73. Morrow, G.; Kim, H. J.; Le Pécheur, M.; Kaul, S. C.; Wadhwa, R.; Tanguay, R. M. Protection from aging by small chaperones: A trade-off with cancer? Ann. NY Acad. Sci., 2010, 1197, 67-75.
74. Bukau, B.; Weissman, J.; Horwich, A. Molecular chaperones and protein quality control. Cell, 2006, 125, 443-451.
75. Kon, M.; Cuervo, A. M. Chaperone-mediated autophagy in health and disease. FEBS Lett., 2010, 584(7), 1399-1404.
76. Cagliari, T. C.; Tiroli, A. O.; Borges, J. C.; Ramos, C. H. I. Identification and in silico expression analysis of eucalyptus expressed sequencing tags (ESTs) encoding molecular chaperones. Gen. Mol. Biol., 2005, 28, 520-528. (Pubitemid 43102915)
77. Borges, J. C.; Cagliari, T. C.; Ramos, C. H. I. Expression and variability of molecular chaperones in the sugarcane expressome. J. Plant Physiol., 2007, 164, 505-513. (Pubitemid 46400899)