Molecular chaperones as regulatory elements of cellular networks

Current Opinion in Cell Biology

Volumn 17, Issue 2, 2005, Pages 210-215

  Soti, Csaba ^a   Pál, Csaba ^b,c   Papp, Balázs ^b,d   Csermely, Péter ^a  

^a SEMMELWEIS UNIVERSITY   (Hungary)

^b EÖTVÖS LORÁND UNIVERSITY   (Hungary)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^d UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLSALICYLIC ACID; CHAPERONE; GELDANAMYCIN; HEAT SHOCK COGNATE PROTEIN 70; HEAT SHOCK PROTEIN 90; IMATINIB; METFORMIN; PROTEIN INHIBITOR;

BINDING AFFINITY; CELL MEMBRANE; CELL ORGANELLE; CELL PROTECTION; CLINICAL TRIAL; CYTOLOGY; HUMAN; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION;

EID: 15044351289     PISSN: 09550674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ceb.2005.02.012     Document Type: Review

References (53)

1. J. Frydman Folding of newly translated proteins in vivo: the role of molecular chaperones Annu Rev Biochem 70 2001 603 647
2. B. Kleizen, and I. Braakman Protein folding and quality control in the endoplasmic reticulum Curr Opin Cell Biol 16 2004 343 349
3. J.C. Young, V.R. Agashe, K. Siegers, and F.U. Hartl Pathways of chaperone-mediated protein folding in the cytosol Nat Rev Mol Cell Biol 5 2004 781 791
4. A.L. Barabasi, and Z.N. Oltvai Network biology: understanding the cell's functional organization Nat Rev Genet 5 2004 101 113 A very clear summary of and introduction to the network model of our cells. This review is a good starting point for those who are not familiar with the network approach.
5. I.F. Tsigelny, and S.K. Nigam Complex dynamics of chaperone-protein interactions under cellular stress Cell Biochem Biophys 40 2004 263 276 A network model of cellular protein folding is presented and its stability is examined under stress (represented by a drop in ATP concentration as occurs, for example, in ischemia or heat shock). A drop in ATP level (stress) is shown to induce a massive instability of protein folding dynamism, which is enhanced by a defect in the proteolytic apparatus (proteasome) and buffered by increased chaperone activity.
6. P. Csermely Strongs links are important - but weak links stabilize them Trends Biochem Sci 29 2004 331 334 Chaperones are shown here as parts of the protein network of the cell and the idea is raised that the genetic buffering of molecular chaperones may be a special form of the general stabilizing role of weak links (i.e. low-affinity interactions) in many types of networks, including social nets and ecosystems.
7. J.C. Young, N.J. Hoogenraad, and F.U. Hartl Molecular chaperones Hsp90 and Hsp70 deliver preproteins to the mitochondrial import receptor Tom70 Cell 112 2003 41 50
8. J. Imai, M. Maruya, H. Yashiroda, I. Yahara, and K. Tanaka The molecular chaperone Hsp90 plays a role in the assembly and maintenance of the 26S proteasome EMBO J 22 2003 3557 3567
9. J.E. Whittier, Y. Xiong, M.C. Rechsteiner, and T.C. Squier Hsp90 enhances degradation of oxidized calmodulin by the 20 S proteasome J Biol Chem 279 2004 46135 46142 Proteasomes are preferentially inactivated by oxidized proteins and show decreased activity during aging. The in vitro studies described in this paper introduce a novel role for chaperone-mediated protection of the proteasomal system, raising the idea that Hsp90 helps proteasomes to degrade oxidized proteins.
10. K. Sachs, D. Gifford, T. Jaakkola, P. Sorger, and D.A. Lauffenburger Bayesian network approach to cell signaling pathway modelling Sci STKE 2002 2002 PE38
11. J. Song, M. Takeda, and R.I. Morimoto Bag1-Hsp70 mediates a physiological stress signalling pathway that regulates Raf-1/ERK and cell growth Nat Cell Biol 3 2001 276 282
12. A. Brouet, P. Sonveaux, C. Dessy, S. Moniotte, J.L. Balligand, and O. Feron Hsp90 and caveolin are key targets for the proangiogenic nitric oxide-mediated effects of statins Circ Res 89 2001 866 873
13. J. Jiang, D. Cyr, R.W. Babbitt, W.C. Sessa, and C. Patterson Chaperone-dependent regulation of endothelial nitric-oxide synthase intracellular trafficking by the co-chaperone/ubiquitin ligase CHIP J Biol Chem 278 2003 49332 49341
14. L.J. Foster, C.L. De Hoog, and M. Mann Unbiased quantitative proteomics of lipid rafts reveals high specificity for signaling factors Proc Natl Acad Sci USA 100 2003 5813 5818
15. α13 to lipid rafts J Biol Chem 277 2002 32409 32412
16. M. Shah, K. Patel, V.A. Fried, and P.B. Sehgal Interactions of STAT3 with caveolin-1 and heat shock protein 90 in plasma membrane raft and cytosolic complexes. Preservation of cytokine signaling during fever J Biol Chem 277 2002 45662 45669
17. T. Sakisaka, T. Meerlo, J. Matteson, H. Plutner, and W.E. Balch Rab-αGDI activity is regulated by a Hsp90 chaperone complex EMBO J 21 2002 6125 6135
18. Z. Torok, P. Goloubinoff, I. Horvath, N.M. Tsvetkova, A. Glatz, G. Balogh, V. Varvasovszki, D.A. Los, E. Vierling, and J.H. Crowe Synechocystis HSP17 is an amphitropic protein that stabilizes heat-stressed membranes and binds denatured proteins for subsequent chaperone-mediated refolding Proc Natl Acad Sci USA 98 2001 3098 3103
19. L. Filippin, P.J. Magalhaes, G. Di Benedetto, M. Colella, and T. Pozzan Stable interactions between mitochondria and endoplasmic reticulum allow rapid accumulation of calcium in a subpopulation of mitochondria J Biol Chem 278 2003 39224 39234
20. M.A. Aon, S. Cortassa, and B. O'Rourke Percolation and criticality in a mitochondrial network Proc Natl Acad Sci USA 101 2004 4447 4452
21. 2+-mediated apoptosis Mol Cell 16 2004 59 68
22. A.S. Verkman Solute and macromolecule diffusion in cellular aqueous compartments Trends Biochem Sci 27 2002 27 33
23. J.M. Harrell, P.J. Murphy, Y. Morishima, H. Chen, J.F. Mansfield, M.D. Galigniana, and W.B. Pratt Evidence for glucocorticoid receptor transport on microtubules by dynein J Biol Chem 279 2004 54647 54654
24. P. Csermely A nonconventional role of molecular chaperones: involvement in the cytoarchitecture News Physiol Sci 16 2001 123 126
25. A.S. Sreedhar, K. Mihaly, B. Pato, T. Schnaider, A. Stetak, K. Kis-Petik, J. Fidy, T. Simonics, A. Maraz, and P. Csermely Hsp90 inhibition accelerates cell lysis. Anti-Hsp90 ribozyme reveals a complex mechanism of Hsp90 inhibitors involving both superoxide- and Hsp90-dependent events J Biol Chem 278 2003 35231 35240
26. J.K. VanSlyke, and L.S. Musil Dislocation and degradation from the ER are regulated by cytosolic stress J Cell Biol 157 2002 381 394
27. T. Yoneda, C. Benedetti, F. Urano, S.G. Clark, H.P. Harding, and D. Ron Compartment-specific perturbation of protein handling activates genes encoding mitochondrial chaperones J Cell Sci 117 2004 4055 4066
28. W. Xu, L. Liu, I.G. Charles, and S. Moncada Nitric oxide induces coupling of mitochondrial signalling with the endoplasmic reticulum stress response Nat Cell Biol 6 2004 1129 1134
29. E.A. Nollen, F.A. Salomons, J.F. Brunsting, J.J. Want, O.C. Sibon, and H.H. Kampinga Dynamic changes in the localization of thermally unfolded nuclear proteins associated with chaperone-dependent protection Proc Natl Acad Sci USA 98 2001 12038 12043
30. H. Schlatter, T. Langer, S. Rosmus, M.L. Onneken, and H. Fasold A novel function for the 90 kDa heat-shock protein (Hsp90): facilitating nuclear export of 60 S ribosomal subunits Biochem J 362 2002 675 684
31. C. Elbi, D.A. Walker, G. Romero, W.P. Sullivan, D.O. Toft, G.L. Hager, and D.B. DeFranco Molecular chaperones function as steroid receptor nuclear mobility factors Proc Natl Acad Sci USA 101 2004 2876 2881
32. H. Zheng, H. You, X.Z. Zhou, S.A. Murray, T. Uchida, G. Wulf, L. Gu, X. Tang, K.P. Lu, and Z.X. Xiao The prolyl isomerase Pin1 is a regulator of p53 in genotoxic response Nature 419 2002 849 853
33. P. Zacchi, M. Gostissa, T. Uchida, C. Salvagno, F. Avolio, S. Volinia, Z. Ronai, G. Blandino, C. Schneider, and G. Del Sal The prolyl isomerase Pin1 reveals a mechanism to control p53 functions after genotoxic insults Nature 419 2002 853 857
34. R. Hamamoto, Y. Furukawa, M. Morita, Y. Iimura, F.P. Silva, M. Li, R. Yagyu, and Y. Nakamura SMYD3 encodes a histone methyltransferase involved in the proliferation of cancer cells Nat Cell Biol 6 2004 731 740
35. Y. Guo, T. Guettouche, M. Fenna, F. Boellmann, W.B. Pratt, D.O. Toft, D.F. Smith, and R. Voellmy Evidence for a mechanism of repression of heat shock factor 1 transcriptional activity by a multichaperone complex J Biol Chem 276 2001 45791 45799
36. B.C. Freeman, and Yamamoto KR Disassembly of transcriptional regulatory complexes by molecular chaperones Science 296 2002 2232 2235
37. T.I. Lee, N.J. Rinaldi, F. Robert, D.T. Odom, Z. Bar-Joseph, G.K. Gerber, N.M. Hannett, C.T. Harbison, C.M. Thompson, and I. Simon Transcriptional regulatory networks in Saccharomyces cerevisiae Science 298 2002 799 804
38. S.L. Rutherford, and S. Lindquist Hsp90 as a capacitor for morphological evolution Nature 396 1998 336 342
39. C. Queitsch, T.A. Sangster, and S. Lindquist Hsp90 as a capacitor of phenotypic variation Nature 417 2002 618 624
40. V. Sollars, X. Lu, L. Xiao, X. Wang, M.D. Garfinkel, and D.M. Ruden Evidence for an epigenetic mechanism by which Hsp90 acts as a capacitor for morphological evolution Nat Genet 33 2003 70 74 The paper describes a mechanism for how the inhibition of the 90 kDa molecular chaperone Hsp90 induces developmental alterations in Drosophila melanogaster and Arabidopsis thaliana [ 38,39 ]. Reduced activity of Hsp90 induces a heritably altered chromatin state in D. melanogaster, which shows that an inheritable epigenetic mechanism contributes to the genetic buffering effect of Hsp90.
41. P. Csermely Chaperone-overload as a possible contributor to 'civilization diseases': atherosclerosis, cancer, diabetes Trends Genet 17 2001 701 704
42. G. Nardai, P. Csermely, and C.S. Soto Chaperone function and chaperone overload in the aged Exp Gerontol 37 2002 1257 1262
43. Cs. Sõti, and P. Csermely Ageing and molecular chaperones Exp Gerontol 38 2003 1037 1040
44. A. Bergman, and M.L. Siegal Evolutionary capacitance as a general feature of complex gene networks Nature 424 2003 549 552 This paper describes numerical simulations of complex gene networks as well as providing a meta-analysis of genome-wide expression data from yeast single-gene deletion strains. The authors argue that many genes besides molecular chaperones reveal phenotypic variation when functionally compromised.
45. H.L. True, I. Berlin, and S.L. Lindquist Epigenetic regulation of translation reveals hidden genetic variation to produce complex traits Nature 431 2004 184 187 The paper extends the earlier findings of the Lindquist laboratory [ 38,39 ], which showed that the yeast prion, [PSI(+)], which is formed by a change in the conformation and function of the translation termination factor Sup35p, produces a spectrum of phenotypes in different genetic backgrounds. This paper shows that the cause of this effect is the [PSI(+)]-mediated read-through of nonsense codons. It has been also demonstrated that genetic re-assortment converts some appearing phenotypes to stable traits that persist in the absence of the yeast prion.
46. T.A. Sangster, S. Lindquist, and C. Queitsch Under cover: causes, effects and implications of Hsp90-mediated genetic capacitance Bioessays 26 2004 348 362
47. Agoston V, Csermely P, Pongor S: Multiple weak hits confuse complex systems. URL: www.arxiv.org/q-bio.MN/0410026.
48. A.R. Sawkar, W.C. Cheng, E. Beutler, C.H. Wong, W.E. Balch, and J.W. Kelly Chemical chaperones increase the cellular activity of N370S β-glucosidase: a therapeutic strategy for Gaucher disease Proc Natl Acad Sci USA 99 2002 15428 15433
49. D. Kieran, B. Kalmar, J.R. Dick, J. Riddoch-Contreras, G. Burnstock, and L. Greensmith Treatment with arimoclomol, a coinducer of heat shock proteins, delays disease progression in ALS mice Nat Med 10 2004 402 405 The paper reports an efficient treatment for the fatal disease amyotrophic lateral sclerosis (Lou Gehrig's disease). The disease, which is caused by a mutation in the Cu/Zn superoxide dismutase-1, is slowed down by arimoclomol, a compound that promotes the induction of Hsp70 and Hsp70 by extending the binding of their major transcriptional factor, the heat shock factor 1, to the DNA. Arimoclomol is a typical multi-target drug, since it also stabilizes membranes and has additional effects.
50. A. Kamal, L. Thao, J. Sensintaffar, L. Zhang, M.F. Boehm, L.C. Fritz, and F.J. Burrows A high-affinity conformation of Hsp90 confers tumour selectivity on Hsp90 inhibitors Nature 425 2003 407 410 Hsp90 inhibitors provide an efficient therapeutic approach against various types of cancer. However, the inhibition of this major chaperone should affect normal cells and cause toxic side-effects. The paper explains the high selectivity of Hsp90 inhibitors towards tumor cells by showing that Hsp90 recruits numerous co-chaperones in tumor cells and that the inhibitor binds to this holo-chaperone with a hundred-fold higher affinity. The selective inhibition of Hsp90, which is a chaperone for many oncogenic proteins including mutant p53, Akt, Raf-1, HER-Erb and Bcr-Abl, attacks the malignant signaling network at multiple points.
51. Rieger TR, Morimoto RI, Hatzimanikatis V: Mathematical modeling of the eukaryotic heat shock response: dynamics of the hsp70 promoter. Biophys J, in press.
52. A. Citri, J. Gan, Y. Mosesson, G. Vereb, J. Szollosi, and Y. Yarden Hsp90 restrains ErbB-2/HER2 signalling by limiting heterodimer formation EMBO Rep 5 2004 1165 1170
53. Csermely P, Ágoston V, Pongor S: The efficiency of multi-target drugs: the network approach might help drug design. Trends Pharmacol Sci 2005, in press.