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Heat Shock Responses for Understanding Diseases of Protein Denaturation  

Kim, Hee-Jung (The Center for Cell Signaling and Drug Discovery Research, College of Pharmacy and Division of Life and Pharmaceutical Sciences, Ewha Womans University)
Hwang, Na Rae (The Center for Cell Signaling and Drug Discovery Research, College of Pharmacy and Division of Life and Pharmaceutical Sciences, Ewha Womans University)
Lee, Kong-Joo (The Center for Cell Signaling and Drug Discovery Research, College of Pharmacy and Division of Life and Pharmaceutical Sciences, Ewha Womans University)
Abstract
Extracellular stresses induce heat shock response and render cells resistant to lethal stresses. Heat shock response involves induction of heat shock proteins (Hsps). Recently the roles of Hsps in neurodegenerative diseases and cancer are attracting increasing attention and have accelerated the study of heat shock response mechanism. This review focuses on the stress sensing steps, molecules involved in Hsps production, diseases related to Hsp malfunctions, and the potential of proteomics as a tool for understanding the complex signaling pathways relevant to these events.
Keywords
Heat Shock Factor; Heat Shock Protein; Heat Shock Response; MAPK; Misfolding of Protein; ROS; Ubiquitin-Proteasome System;
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1 Aghdassi, A., Phillips, P., Dudeja, V., Dhaulakhandi, D., Sharif, R., et al. (2007) Heat shock protein 70 increases tumorigenicity and inhibits apoptosis in pancreatic adenocarcinoma. Cancer Res. 67, 616−625
2 Calderwood, S. K., Khaleque, M. A., Sawyer, D. B., and Ciocca, D. R. (2006) Heat shock proteins in cancer: chaperones of tumorigenesis. Trends Biochem. Sci. 31, 164−172
3 Dou, F., Netzer, W. J., Tanemura, K., Li, F., Hartl, F. U., et al. (2003) Chaperones increase association of tau protein with microtubules. Proc. Natl. Acad. Sci. USA 100, 721−726
4 Horwitz, J. (1992) Alpha-crystallin can function as a molecular chaperone. Proc. Natl. Acad. Sci. USA 89, 10449−10453
5 Huot, J., Lambert, H., Lavoie, J. N., Guimond, A., Houle, F., et al. (1995) Characterization of 45-kDa/54-kDa HSP27 kinase, a stress-sensitive kinase which may activate the phosphorylation- dependent protective function of mammalian 27-kDa heat-shock protein HSP27. Eur. J. Biochem. 227, 416−427
6 Kondo, T., Matsuda, T., Kitano, T., Takahashi, A., Tashima, M., et al. (2000) Role of c-jun expression increased by heat shock- and ceramide-activated caspase-3 in HL-60 cell apoptosis. Possible involvement of ceramide in heat shockinduced apoptosis. J. Biol. Chem. 275, 7668−7676
7 Lavoie, J. N., Lambert, H., Hickey, E., Weber, L. A., and Landry, J. (1995) Modulation of cellular thermoresistance and actin filament stability accompanies phosphorylation-induced changes in the oligomeric structure of heat shock protein 27. Mol. Cell. Biol. 15, 505−516
8 Lee, S. Y., Song, E. J., Kim, H. J., Kang, H. J., Kim, J. H., et al. (2001) Rac1 regulates heat shock responses by reorganization of vimentin filaments: identification using MALDI-TOF MS. Cell Death Differ. 8, 1093−1102
9 Lindquist, S. and Craig, E. A. (1988) The heat-shock proteins. Annu. Rev. Genet. 22, 631−677
10 Muchowski, P. J., Schaffar, G., Sittler, A., Wanker, E. E., Hayer- Hartl, M. K., et al. (2000) Hsp70 and hsp40 chaperones can inhibit self-assembly of polyglutamine proteins into amyloidlike fibrils. Proc. Natl. Acad. Sci. USA 97, 7841−7846
11 Nakai, A., Tanabe, M., Kawazoe, Y., Inazawa, J., Morimoto, R. I., et al. (1997) HSF4, a new member of the human heat shock factor family which lacks properties of a transcriptional activator. Mol. Cell. Biol. 17, 469−481
12 Rubinsztein, D. C. (2006) The roles of intracellular proteindegradation pathways in neurodegeneration. Nature 443, 780−786
13 Song, E. J., Yim, S. H., Kim, E., Kim, N. S., and Lee, K. J. (2005) Human Fas-associated factor 1, interacting with ubiquitinated proteins and valosin-containing protein, is involved in the ubiquitin-proteasome pathway. Mol. Cell. Biol. 25, 2511−2524
14 Hong, Y., Rogers, R., Matunis, M. J., Mayhew, C. N., Goodson, M. L., et al. (2001) Regulation of heat shock transcription factor 1 by stress-induced SUMO-1 modification. J. Biol. Chem. 276, 40263−40267
15 Wyttenbach, A., Sauvageot, O., Carmichael, J., Diaz-Latoud, C., Arrigo, A. P., et al. (2002) Heat shock protein 27 prevents cellular polyglutamine toxicity and suppresses the increase of reactive oxygen species caused by huntingtin. Hum. Mol. Genet. 11, 1137−1151
16 Young, J. C. and Hartl, F. U. (2002) Chaperones and transcriptional regulation by nuclear receptors. Nat. Struct. Biol. 9, 640−642
17 Meriin, A. B., Yaglom, J. A., Gabai, V. L., Zon, L., Ganiatsas, S., et al. (1999) Protein-damaging stresses activate c-Jun Nterminal kinase via inhibition of its dephosphorylation: a novel pathway controlled by HSP72. Mol. Cell. Biol. 19, 2547−2555
18 Warrick, J. M., Chan, H. Y., Gray-Board, G. L., Chai, Y., Paulson, H. L., et al. (1999) Suppression of polyglutaminemediated neurodegeneration in Drosophila by the molecular chaperone HSP70. Nat. Genet. 23, 425−428
19 Todd, J. L., Rigas, J. D., Rafty, L. A., and Denu, J. M. (2002) Dual-specificity protein tyrosine phosphatase VHR downregulates c-Jun N-terminal kinase (JNK). Oncogene 21, 2573−2583
20 Bush, K. T., Goldberg, A. L., and Nigam, S. K. (1997) Proteasome inhibition leads to a heat-shock response, induction of endoplasmic reticulum chaperones, and thermotolerance. J. Biol. Chem. 272, 9086−9092
21 Ahn, S. G. and Thiele, D. J. (2003) Redox regulation of mammalian heat shock factor 1 is essential for Hsp gene activation and protection from stress. Genes Dev. 17, 516−528
22 Park, J. and Liu, A. Y. (2001) JNK phosphorylates the HSF1 transcriptional activation domain: role of JNK in the regulation of the heat shock response. J. Cell. Biochem. 82, 326− 338
23 Manalo, D. J., Lin, Z., and Liu, A. Y. (2002) Redox-dependent regulation of the conformation and function of human heat shock factor 1. Biochemistry 41, 2580−2588
24 Mayer, M. P. and Bukau, B. (2005) Hsp70 chaperones: cellular functions and molecular mechanism. Cell Mol. Life Sci. 62, 670−684
25 Morimoto, R. I. (1998) Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones, and negative regulators. Genes Dev. 12, 3788−3796
26 Bost, F., McKay, R., Bost, M., Potapova, O., Dean, N. M., et al. (1999) The Jun kinase 2 isoform is preferentially required for epidermal growth factor-induced transformation of human A549 lung carcinoma cells. Mol. Cell. Biol. 19, 1938−1949
27 Clark, J. I. and Muchowski, P. J. (2000) Small heat-shock proteins and their potential role in human disease. Curr. Opin. Struct. Biol. 10, 52−59
28 Han, M. J., Kim, B. Y., Yoon, S. S., and Chung, A. S. (2003) Cell proliferation induced by reactive oxygen species is mediated via mitogen-activated protein kinase in Chinese hamster lung fibroblast (V79) cells. Mol. Cells 15, 94−101
29 Landry, J., Chretien, P., Laszlo, A., and Lambert, H. (1991) Phosphorylation of HSP27 during development and decay of thermotolerance in Chinese hamster cells. J. Cell. Physiol. 147, 93−101
30 Potapova, O., Anisimov, S. V., Gorospe, M., Dougherty, R. H., Gaarde, W. A., et al. (2002) Targets of c-Jun NH(2)-terminal kinase 2-mediated tumor growth regulation revealed by serial analysis of gene expression. Cancer Res. 62, 3257−3263
31 Minami, Y., Hohfeld, J., Ohtsuka, K., and Hartl, F. U. (1996) Regulation of the heat-shock protein 70 reaction cycle by the mammalian DnaJ homolog, Hsp40. J. Biol. Chem. 271, 19617−19624
32 Kakimura, J.-I., Kitamura, Y., Takata, K., Umeki, M., Suzuki, S., et al. (2002) Microglial activation and amyloid-{beta} clearance induced by exogenous heat-shock proteins. FASEB J. 16, 601−603
33 Kim, Y. M., Kim, K. E., Koh, G. Y., Ho, Y. S., and Lee, K. J. (2006) Hydrogen peroxide produced by angiopoietin-1 mediates angiogenesis. Cancer Res. 66, 6167−6174
34 Dorion, S., Lambert, H., and Landry, J. (2002) Activation of the p38 signaling pathway by heat shock involves the dissociation of glutathione S-transferase Mu from Ask1. J. Biol. Chem. 277, 30792−30797
35 Xiao, L., Lu, X., and Ruden, D. M. (2006) Effectiveness of hsp90 inhibitors as anti-cancer drugs. Mini Rev. Med. Chem. 6, 1137−1143
36 Chen, N., Nomura, M., She, Q. B., Ma, W. Y., Bode, A. M., et al. (2001a) Suppression of skin tumorigenesis in c-Jun NH(2)- terminal kinase-2-deficient mice. Cancer Res. 61, 3908−3912
37 Davis, R. J. (2000) Signal transduction by the JNK group of MAP kinases. Cell 103, 239−252
38 Mathew, A., Mathur, S. K., and Morimoto, R. I. (1998) Heat shock response and protein degradation: regulation of HSF2 by the ubiquitin-proteasome pathway. Mol. Cell. Biol. 18, 5091−5098
39 Yaglom, J., O'Callaghan-Sunol, C., Gabai, V., and Sherman, M. Y. (2003) Inactivation of dual-specificity phosphatases is involved in the regulation of extracellular signal-regulated kinases by heat shock and hsp72. Mol. Cell. Biol. 23, 3813− 3824
40 McLean, P. J., Kawamata, H., Shariff, S., Hewett, J., Sharma, N., et al. (2002) TorsinA and heat shock proteins act as molecular chaperones: suppression of alpha-synuclein aggregation. J. Neurochem. 83, 846−854
41 Muchowski, P. J. and Wacker, J. L. (2005) Modulation of neurodegeneration by molecular chaperones. Nat. Rev. Neurosci. 6, 11−22
42 Holmberg, C. I., Tran, S. E., Eriksson, J. E., and Sistonen, L. (2002) Multisite phosphorylation provides sophisticated regulation of transcription factors. Trends Biochem. Sci. 27, 619−627   DOI
43 Bae, Y. S., Kang, S. W., Seo, M. S., Baines, I. C., Tekle, E., et al. (1997) Epidermal growth factor (EGF)-induced generation of hydrogen peroxide. Role in EGF receptor-mediated tyrosine phosphorylation. J. Biol. Chem. 272, 217−221
44 Broquet, A. H., Thomas, G., Masliah, J., Trugnan, G., and Bachelet, M. (2003) Expression of the molecular chaperone Hsp70 in detergent-resistant microdomains correlates with its membrane delivery and release. J. Biol. Chem. 278, 21601− 21606
45 Bogoyevitch, M. A. (2006) The isoform-specific functions of the c-Jun N-terminal kinases (JNKs): differences revealed by gene targeting. Bioessays 28, 923−934
46 Klucken, J., Shin, Y., Masliah, E., Hyman, B. T., and McLean, P. J. (2004) Hsp70 reduces alpha-synuclein aggregation and toxicity. J. Biol. Chem. 279, 25497−25502
47 Kuan, C. Y., Yang, D. D., Samanta Roy, D. R., Davis, R. J., Rakic, P., et al. (1999) The Jnk1 and Jnk2 protein kinases are required for regional specific apoptosis during early brain development. Neuron 22, 667−676
48 Muda, M., Theodosiou, A., Rodrigues, N., Boschert, U., Camps, M., et al. (1996) The dual specificity phosphatases M3/6 and MKP-3 are highly selective for inactivation of distinct mitogen- activated protein kinases. J. Biol. Chem. 271, 27205− 27208
49 Chang, T. S., Jeong, W., Choi, S. Y., Yu, S., Kang, S. W., et al. (2002) Regulation of peroxiredoxin I activity by Cdc2- mediated phosphorylation. J. Biol. Chem. 277, 25370−25376
50 Giannoni, E., Buricchi, F., Raugei, G., Ramponi, G., and Chiarugi, P. (2005) Intracellular reactive oxygen species activate Src tyrosine kinase during cell adhesion and anchoragedependent cell growth. Mol. Cell. Biol. 25, 6391−6403
51 Chu, B., Zhong, R., Soncin, F., Stevenson, M. A., and Calderwood, S. K. (1998) Transcriptional activity of heat shock factor 1 at 37 degrees C is repressed through phosphorylation on two distinct serine residues by glycogen synthase kinase 3 and protein kinases Calpha and Czeta. J. Biol. Chem. 273, 18640−18646   DOI   ScienceOn
52 Rhee, S. G., Bae, Y. S., Lee, S. R., and Kwon, J. (2000) Hydrogen peroxide: a key messenger that modulates protein phosphorylation through cysteine oxidation. Sci. STKE 2000, PE1   DOI
53 Sabapathy, K., Jochum, W., Hochedlinger, K., Chang, L., Karin, M., et al. (1999) Defective neural tube morphogenesis and altered apoptosis in the absence of both JNK1 and JNK2. Mech. Dev. 89, 115−124
54 Rhee, S. G. (2006) Cell signaling. H2O2, a necessary evil for cell signaling. Science 312, 1882−1883   DOI
55 Richly, H., Rape, M., Braun, S., Rumpf, S., Hoege, C., et al. (2005) A series of ubiquitin binding factors connects CDC48/ p97 to substrate multiubiquitylation and proteasomal targeting. Cell 120, 73−84
56 Hu, Y. and Mivechi, N. F. (2006) Association and regulation of heat shock transcription factor 4b with both extracellular signal- regulated kinase mitogen-activated protein kinase and dual-specificity tyrosine phosphatase DUSP26. Mol. Cell. Biol. 26, 3282−3294
57 Westerheide, S. D. and Morimoto, R. I. (2005) Heat shock response modulators as therapeutic tools for diseases of protein conformation. J. Biol. Chem. 280, 33097−33100
58 Kyriakis, J. M. and Avruch, J. (2001) Mammalian mitogenactivated protein kinase signal transduction pathways activated by stress and inflammation. Physiol. Rev. 81, 807−869
59 Pagliari, L. J., Kuwana, T., Bonzon, C., Newmeyer, D. D., Tu, S., et al. (2005) The multidomain proapoptotic molecules Bax and Bak are directly activated by heat. Proc. Natl. Acad. Sci. USA 102, 17975−17980
60 Shinka, T., Sato, Y., Chen, G., Naroda, T., Kinoshita, K., et al. (2004) Molecular characterization of heat shock-like factor encoded on the human Y chromosome, and implications for male infertility. Biol. Reprod. 71, 297−306
61 Kim, D., Kim, S. H., and Li, G. C. (1999) Proteasome inhibitors MG132 and lactacystin hyperphosphorylate HSF1 and induce hsp70 and hsp27 expression. Biochem. Biophys. Res. Commun. 254, 264−268
62 Kim, S. A., Yoon, J. H., Lee, S. H., and Ahn, S. G. (2005) Pololike kinase 1 phosphorylates heat shock transcription factor 1 and mediates its nuclear translocation during heat stress. J. Biol. Chem. 280, 12653−12657
63 Chen, Y. R., Shrivastava, A., and Tan, T. H. (2001b) Downregulation of the c-Jun N-terminal kinase (JNK) phosphatase M3/6 and activation of JNK by hydrogen peroxide and pyrrolidine dithiocarbamate. Oncogene 20, 367−374
64 Chu, B., Soncin, F., Price, B. D., Stevenson, M. A., and Calderwood, S. K. (1996) Sequential phosphorylation by mitogenactivated protein kinase and glycogen synthase kinase 3 represses transcriptional activation by heat shock factor-1. J. Biol. Chem. 271, 30847−30857
65 Guettouche, T., Boellmann, F., Lane, W. S., and Voellmy, R. (2005) Analysis of phosphorylation of human heat shock factor 1 in cells experiencing a stress. BMC Biochem. 6, 4
66 Kim, Y. M., Song, E. J., Seo, J., Kim, H. J., and Lee, K. J. (2007) Proteomic analysis of tyrosine phosphorylations in vascular endothelial growth factor- and reactive oxygen species- mediated signaling pathway. J. Proteome Res. 6, 593− 601
67 Jacquier-Sarlin, M. R. and Polla, B. S. (1996) Dual regulation of heat-shock transcription factor (HSF) activation and DNAbinding activity by $H_2O_2$: role of thioredoxin. Biochem. J. 318 (Pt 1), 187−93
68 Kallio, M., Chang, Y., Manuel, M., Alastalo, T. P., Rallu, M., et al. (2002) Brain abnormalities, defective meiotic chromosome synapsis and female subfertility in HSF2 null mice. EMBO J. 21, 2591−2601
69 Lindquist, S. (1986) The heat-shock response. Annu. Rev. Biochem. 55, 1151−1191
70 Yang, Y., Turner, R. S., and Gaut, J. R. (1998) The chaperone BiP/GRP78 binds to amyloid precursor protein and decreases Abeta40 and Abeta42 secretion. J. Biol. Chem. 273, 25552− 25555
71 Sherman, M. Y. and Gabai, V. L. (2006) Multiple thermometers in mammalian cells: why do cells from homeothermic organisms need to measure temperature? Sci. STKE 2006, pe16
72 Hietakangas, V., Ahlskog, J. K., Jakobsson, A. M., Hellesuo, M., Sahlberg, N. M., et al. (2003) Phosphorylation of serine 303 is a prerequisite for the stress-inducible SUMO modification of heat shock factor 1. Mol. Cell. Biol. 23, 2953−2968
73 Lin, R. Z., Hu, Z. W., Chin, J. H., and Hoffman, B. B. (1997) Heat shock activates c-Src tyrosine kinases and phosphatidylinositol 3-kinase in NIH3T3 fibroblasts. J. Biol. Chem. 272, 31196−31202
74 Philip, B. and Levin, D. E. (2001) Wsc1 and Mid2 are cell surface sensors for cell wall integrity signaling that act through Rom2, a guanine nucleotide exchange factor for Rho1. Mol. Cell. Biol. 21, 271−280
75 Kim, H. J., Song, E. J., and Lee, K. J. (2002) Proteomic analysis of protein phosphorylations in heat shock response and thermotolerance. J. Biol. Chem. 277, 23193−23207
76 Auluck, P. K., Chan, H. Y., Trojanowski, J. Q., Lee, V. M., and Bonini, N. M. (2002) Chaperone suppression of alphasynuclein toxicity in a Drosophila model for Parkinson's disease. Science 295, 865−868   DOI
77 Cummings, C. J., Sun, Y., Opal, P., Antalffy, B., Mestril, R., et al. (2001) Over-expression of inducible HSP70 chaperone suppresses neuropathology and improves motor function in SCA1 mice. Hum. Mol. Genet. 10, 1511−1518
78 Garrido, C., Brunet, M., Didelot, C., Zermati, Y., Schmitt, E., et al. (2006) Heat shock proteins 27 and 70: anti-apoptotic proteins with tumorigenic properties. Cell Cycle 5, 2592−2601
79 Jana, N. R., Tanaka, M., Wang, G., and Nukina, N. (2000) Polyglutamine length-dependent interaction of Hsp40 and Hsp70 family chaperones with truncated N-terminal huntingtin: their role in suppression of aggregation and cellular toxicity. Hum. Mol. Genet. 9, 2009−2018
80 Shorter, J. and Lindquist, S. (2004) Hsp104 catalyzes formation and elimination of self-replicating Sup35 prion conformers. Science 304, 1793−1797
81 Kim, H. J. and Lee, K. J. (2002) Heat shock and ceramide have different apoptotic pathways in radiation induced fibrosarcoma (RIF) cells. Mol. Cell Biochem. 229, 139−151
82 Kline, M. P. and Morimoto, R. I. (1997) Repression of the heat shock factor 1 transcriptional activation domain is modulated by constitutive phosphorylation. Mol. Cell. Biol. 17, 2107− 2115
83 Palacios, C., Collins, M. K., and Perkins, G. R. (2001) The JNK phosphatase M3/6 is inhibited by protein-damaging stress. Curr. Biol. 11, 1439−1443
84 Pirkkala, L., Nykanen, P., and Sistonen, L. (2001) Roles of the heat shock transcription factors in regulation of the heat shock response and beyond. FASEB J. 15, 1118−1131
85 Rhee, S. G., Kang, S. W., Jeong, W., Chang, T. S., Yang, K. S., et al. (2005) Intracellular messenger function of hydrogen peroxide and its regulation by peroxiredoxins. Curr. Opin. Cell Biol. 17, 183−189
86 Shimura, H., Miura-Shimura, Y., and Kosik, K. S. (2004) Binding of tau to heat shock protein 27 leads to decreased concentration of hyperphosphorylated tau and enhanced cell survival. J. Biol. Chem. 279, 17957−17962
87 Urano, F., Wang, X., Bertolotti, A., Zhang, Y., Chung, P., et al. (2000) Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 287, 664−666
88 Holmberg, C. I., Hietakangas, V., Mikhailov, A., Rantanen, J. O., Kallio, M., et al. (2001) Phosphorylation of serine 230 promotes inducible transcriptional activity of heat shock factor 1. EMBO J. 20, 3800−3810