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5 - Molecular Chaperones: The Unorthodox View

Published online by Cambridge University Press:  10 August 2009

By
Brian Henderson  and
Alireza Shamaei-Tousi
Edited by
Brian Henderson  and
A. Graham Pockley
Brian Henderson
Affiliation:
Division of Microbial Diseases, Eastman Dental Institute, University College London, London, United Kingdom
Alireza Shamaei-Tousi
Affiliation:
Division of Microbial Diseases, Eastman Dental Institute, University College London, London, United Kingdom
Brian Henderson
Affiliation:
University College London
A. Graham Pockley
Affiliation:
University of Sheffield
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Summary

Introduction

Like a Brian Rix farce, in which the characters' identities are continuously changing, the functions of the class of protein known as molecular chaperones has been unfolding continuously over the past decade resulting in substantial confusion. However, like such farces, we are confident that the dénouement will be a complete surprise and will provide a new world picture of the processes with which molecular chaperones are involved. This short chapter aims to introduce the reader to the rapidly changing world of molecular chaperones as an aid to the reading of the rest of the chapters in this volume.

Molecular chaperones are protein folders

Our story starts with a huff and a puff with the study of the response of the polytene chromosomes of Drosophila to various stressors. This revealed novel patterns of specific chromosomal puffs, in response to heat, and a variety of other environmental stresses, representing the transcription of selected genes [1, 2]. The behaviour of cells exposed to various stresses became known as the heat shock response or the cell stress response and we now appreciate the very large number of environmental factors to which cells will respond in this stereotypical manner. The ‘molecularisation’ of the cell stress response occurred in the late 1980s with the pioneering work of Ellis and colleagues [3], who introduced both the concept of protein chaperoning and the term molecular chaperone.

Type
Chapter
Information
Molecular Chaperones and Cell Signalling , pp. 78 - 96
Publisher: Cambridge University Press
Print publication year: 2005

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References

Ritossa, F A.A new puffing pattern induced by temperature shock and DNP in Drosophila. Experientia 1962, 18: 571–573Google Scholar
Ashburner, M. Pattern of puffing activity in the salivary gland chromosomes of Drosophila. V. Response to environmental treatments. Chromosoma 1970, 31: 356–376Google Scholar
Hemmingsen, S M, Woolford, C, Vies, S M, Tilly, K, Dennis, D T, Georgopoulos, G C, Hendrix, R W and Ellis, R J. Homologous plant and bacterial proteins chaperone oligomeric protein assembly. Nature 1988, 333: 330–334Google Scholar
Young, D B, Ivanyi, J, Cox, J H and Lamb, J R. The 65 kDa antigen of mycobacteria – a common bacterial protein?Immunol Today 1987, 8: 215–219Google Scholar
Cohen, I R and Young, D B. Autoimmunity, microbial immunity and the immunological homunculus. Immunol Today 1991, 12: 105–109Google Scholar
Horner, D S, Hirt, R P, Kilvington, S, Lloyd, D and Embley, T M. Molecular data suggest an early acquisition of the mitochondrion endosymbiont. Proc Royal Soc London B Biol Sci 1996, 263: 1053–1059Google Scholar
Hartl, F U and Hayer-Hartl, M. Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 2002, 295: 1852–1858Google Scholar
Fisch, P, Malkovsky, M, Kovats, S, Sturm, E, Braakman, E, Klein, B S, Voss, S D, Morrissey, L W, DeMars, R, Welch, W J, Bolhuis, R L H and Sondel, P M. Recognition by human Vγ9/Vδ2 T cells of a GroEL homolog on Daudi Burkitt's lymphoma cells. Science 1990, 250: 1269–1273Google Scholar
Torok, Z, Horvath, I, Goloubinoff, P, Kovacs, E, Glatz, A, Balogh, G and Vigh, L. Evidence for a lipochaperonin: association of active protein-folding GroESL oligomers with lipids can stabilize membranes under heat shock conditions. Proc Natl Acad Sci USA 1997, 94: 2192–2197Google Scholar
Trent, J D, Kagawa, H K, Paavola, C D, McMillan, R A, Howard, J, Jahnke, L, Lavin, C, Embaye, T and Henze, C E. Intracellular localization of a group II chaperonin indicates a membrane-related function. Proc Natl Acad Sci USA 2003, 100: 15589–15594Google Scholar
Alder, G M, Austen, B M, Bashford, C L, Mehkert, A and Pasternak, C A. Heat shock proteins induce pores in membranes. Biosci Reports 1990, 10: 509–518Google Scholar
Triantafilou, K, Triantafilou, M and Dedrick, R L. A CD14-independent LPS receptor cluster. Nat Immunol 2001, 2: 338–344Google Scholar
Triantafilou, K, Triantafilou, M, Ladha, S, Mackie, A, Dedrick, R L, Fernandez, N and Cherry, R. Fluorescence recovery after photobleaching reveals that LPS rapidly transfers from CD14 to Hsp70 and Hsp90 on the cell membrane. J Cell Sci 2001, 114: 2535–2545Google Scholar
Bausinger, H, Lipsker, D, Ziylan, U, Manie, S, Briand, J P, Cazenave, J P, Muller, S, Haeuw, J F, Ravanat, C, Salle, H and Hanau, D. Endotoxin-free heat-shock protein 70 fails to induce APC activation. Eur J Immunol 2002, 32: 3708–3713Google Scholar
Gao, B and Tsan, M F. Induction of cytokines by heat shock proteins and endotoxin in murine macrophages. Biochem Biophys Res Commun 2004, 317: 1149–1154Google Scholar
Gao, B and Tsan, M F. Endotoxin contamination in recombinant human Hsp70 preparation is responsible for the induction of TNFα release by murine macrophages. J Biol Chem 2003, 278: 174–179Google Scholar
Gao, B and Tsan, M F. Recombinant human heat shock protein 60 does not induce the release of tumor necrosis factor α from murine macrophages. J Biol Chem 2003, 278: 22523–22529Google Scholar
Gobert, A P, Bambou, J C, Werts, C, Balloy, V, Chignard, M, Moran, A P and Ferrero, R L. Helicobacter pylori heat shock protein 60 mediates interleukin-6 production by macrophages via a Toll-like receptor (TLR)-2-, TLR-4-, and myeloid differentiation factor 88-independent mechanism. J Biol Chem 2004, 279: 245–250Google Scholar
Metz-Boutigue, M H, Kieffer, A E, Goumon, Y and Aunis, D. Innate immunity: involvement of new neuropeptides. Trends Microbiol 2003, 11: 585–592Google Scholar
Tagaya, Y, Maeda, Y, Mitsui, A, Kondo, N, Matsui, H, Hamuro, J, Brown, N, Arai, K, Yokota, T and Wakasugi, H. ATL-derived factor (ADF), an IL-2 receptor/Tac inducer homologous to thioredoxin; possible involvement of dithiol-reduction in the IL-2 receptor induction. EMBO J 1989, 8: 757–764Google Scholar
Bertini, R, Howard, O M, Dong, H F, Oppenheim, J J, Bizzarri, C, Sergi, R, Caselli, G, Pagliei, S, Romines, B, Wilshire, J A, Mengozzi, M, Nakamura, H, Yodoi, J, Pekkari, K, Gurunath, R, Holmgren, A, Herzenberg, L A, Herzenberg, L A and Ghezzi, P. Thioredoxin, a redox enzyme released in infection and inflammation, is a unique chemoattractant for neutrophils, monocytes, and T cells. J Exp Med 1999, 189: 1783–1789Google Scholar
Nakamura, H, Herzenberg, L A, Bai, J, Araya, S, Kondo, N, Nishinaka, Y, Herzenberg, L A and Yodoi, J. Circulating thioredoxin suppresses lipopolysaccharide-induced neutrophil chemotaxis. Proc Natl Acad Sci USA 2001, 98: 15143–15148Google Scholar
Makino, Y, Okamoto, K, Yoshikawa, N, Aoshima, M, Hirota, K, Yodoi, J, Umesono, K, Makino, I and Tanaka, H. Thioredoxin: a redox-regulating cellular cofactor for glucocorticoid hormone action. Cross talk between endocrine control of stress response and cellular antioxidant defense system. J Clin Invest 1996, 98: 2469–2477Google Scholar
Morton, H. Early pregnancy factor: an extracellular chaperonin 10 homologue. Immunol Cell Biol 1998, 76: 483–496Google Scholar
Meghji, S, White, P, Nair, S P, Reddi, K, Heron, K, Henderson, B, Zaliani, A, Fossati, G, Mascagni, P, Hunt, J F, Roberts, M M and Coates, A R. Mycobacterium tuberculosis chaperonin 10 stimulates bone resorption: a potential contributory factor in Pott's disease. J Exp Med 1997, 186: 1241–1246Google Scholar
Bhat, N R and Sharma, K K. Microglial activation by the small heat shock protein, α-crystallin. Neuroreport 1999, 10: 2869–2873Google Scholar
Sherry, N, Yarlett, A, Strupp, A and Cerami, A. Identification of cyclophilin as a proinflammatory secretory product of lipopolysaccharide-activated macrophages. Proc Natl Acad Sci USA 1992, 89: 3511–3515Google Scholar
Xu, Q, Lefeva, M C, Fischkoff, S A, Handschumacher, R E and Lyttle, C R. Leukocyte chemotactic activity of cyclophilin. J Biol Chem 1992, 267: 11968–11971Google Scholar
Aliberti, J, Valenzuela, J G, Carruthers, V B, Hieny, S, Andersen, J, Charest, H, Reis e Sousa, C, Fairlamb, A, Ribeiro, J M and Sher, A. Molecular mimicry of a CCR5 binding-domain in the microbial activation of dendritic cells. Nat Immunol 2003, 4: 485–490Google Scholar
De, A K, Kodys, K M, Yeh, B S and Miller-Graziano, C. Exaggerated human monocyte IL-10 concomitant to minimal TNF-α induction by heat-shock protein 27 (Hsp27) suggests Hsp27 is primarily an anti-inflammatory stimulus. J Immunol 2000, 165: 3951–3958Google Scholar
Detanico, T, Rodrigues, L, Sabritto, A C, Keisermann, M, Bauer, M E, Zwickey, H and Bonorino, C. Mycobacterial heat shock protein 70 induces interleukin-10 production: immunomodulation of synovial cell cytokine profile and dendritic cell maturation. Clin Exp Immunol 2004, 135: 336–342Google Scholar
Corrigall, V M, Bodman-Smith, M D, Fife, M S, Canas, B, Myers, L K, Wooley, P, Soh, C, Staines, N A, Pappin, D J, Berlo, S E, Eden, W, Zee, R, Lanchbury, J S and Panayi, G S. The human endoplasmic reticulum molecular chaperone BiP is an autoantigen for rheumatoid arthritis and prevents the induction of experimental arthritis. J Immunol 2001, 166: 1492–1498Google Scholar
Corrigall, V M, Bodman-Smith, M D, Brunst, M, Cornell, H and Panayi, G S. Inhibition of antigen-presenting cell function and stimulation of human peripheral blood mononuclear cells to express an anti-inflammatory cytokine profile by the stress protein BiP: Relevance to the treatment of inflammatory arthritis. Arthritis Rheum 2004, 50: 1164–1171Google Scholar
Prasadarao, N V, Srivastava, P K, Rudrabhatla, R S, Kim, K S, Huang, S H and Sukumaran, S K. Cloning and expression of the Escherichia coli K1 outer membrane protein A receptor, a gp96 homologue. Infect Immun 2003, 71: 1680–1688Google Scholar
Khan, N A, Shin, S, Chung, J W, Kim, K J, Elliott, S, Wang, Y and Kim, K S. Outer membrane protein A and cytotoxic necrotizing factor-1 use diverse signaling mechanisms for Escherichia coli K1 invasion of human brain microvascular endothelial cells. Microb Pathogenesis 2003, 35: 35–42Google Scholar
Randow, F and Seed, B. Endoplasmic reticulum chaperone gp96 is required for innate immunity but not cell viability. Nat Cell Biol 2001, 3: 891–896Google Scholar
Panjwani, N N, Popova, L and Srivastava, P K. Heat shock proteins gp96 and hsp70 activate the release of nitric oxide by APCs. J Immunol 2002, 168: 2997–3003Google Scholar
Vabulas, R M, Braedel, S, Hilf, N, Singh-Jasuja, H, Herter, S, Ahmad-Nejad, P, Kirschning, C J, Da Costa, C, Rammensee, H G, Wagner, H and Schild, H. The endoplasmic reticulum-resident heat shock protein Gp96 activates dendritic cells via the Toll-like receptor 2/4 pathway. J Biol Chem 2002, 277: 20847–20853Google Scholar
Radsak, M P, Hilf, N, Singh-Jasuja, H, Braedel, S, Brossart, P, Rammensee, H G and Schild, H. The heat shock protein Gp96 binds to human neutrophils and monocytes and stimulates effector functions. Blood 2003, 101: 2810–2815Google Scholar
Banerjee, P P, Vinay, D S, Mathew, A, Raje, M, Parekh, V, Prasad, D V, Kumar, A, Mitra, D and Mishra, G C. Evidence that glycoprotein 96 (B2), a stress protein, functions as a Th2-specific costimulatory molecule. J Immunol 2002, 169: 3507–3518Google Scholar
Chaput, M, Claes, V, Portetelle, D, Cludts, I, Cravador, A, Burny, A, Gras, H and Tartar, A. The neurotrophic factor neuroleukin is 90% homologous with phosphohexose isomerase. Nature 1988, 332: 454–455Google Scholar
Watanabe, H, Takehana, K, Date, M, Shinozaki, T and Raz, A. Tumor cell autocrine motility factor is the neuroleukin/phosphohexose isomerase polypeptide. Cancer Res 1996, 56: 2960–2963Google Scholar
Xu, W, Seiter, K, Feldman, E, Ahmed, T and Chiao, J W. The differentiation and maturation mediator for human myeloid leukemia cells shares homology with neuroleukin or phosphoglucose isomerase. Blood 1996, 87: 4502–4506Google Scholar
Schulz, L C and Bahr, J M. Glucose-6-phosphate isomerase is necessary for embryo implantation in the domestic ferret. Proc Natl Acad Sci USA 2003, 100: 8561–8566Google Scholar
Kogaki, H, Fujiwara, Y, Yoshiki, A, Kitajima, S, Tanimoto, T, Mitsui, A, Shimamura, T, Hamuro, J and Ashihara, Y. Sensitive enzyme-linked immunosorbent assay for adult T-cell leukemia-derived factor and normal value measurement. J Clin Lab Anal 1996, 10: 257–261Google Scholar
Nakamura, H, Rosa, S C, Yodoi, J, Holmgren, A, Ghezzi, P, Herzenberg, L A and Herzenberg, L A. Chronic elevation of plasma thioredoxin: inhibition of chemotaxis and curtailment of life expectancy in AIDS. Proc Natl Acad Sci USA 2001, 98: 2688–2693Google Scholar
Hoshino, T, Nakamura, H, Okamoto, M, Kato, S, Araya, S, Nomiyama, K, Oizumi, K, Young, H A, Aizawa, H and Yodoi, J. Redox-active protein thioredoxin prevents proinflammatory cytokine- or bleomycin-induced lung injury. Am J Respir Crit Care Med 2003, 168: 1075–1083Google Scholar
Morton, H, Rolfe, B and Clunie, G J. An early pregnancy factor detected in human serum by the rosette inhibition test. Lancet 1977, 1(8008): 394–397Google Scholar
Clarke, F M, Orozco, C, Perkins, A V, Cock, I, Tonissen, K F, Robins, A J and Wells, J R. Identification of molecules involved in the ‘early pregnancy factor’ phenomenon. J Reprod Fertil 1991, 93: 525–539Google Scholar
Cavanagh, A C and Morton, H. The purification of early-pregnancy factor to homogeneity from human platelets and identification as chaperonin 10. Eur J Biochem 1994, 222: 551–560Google Scholar
Lash, G E and Legge, M. Early pregnancy factor: an unresolved molecule. J Assist Reprod Genet 1997, 14: 495–496Google Scholar
Somodevilla-Torres, M J, Morton, H, Zhang, B, Reid, S and Cavanagh, A C. Purification and characterisation of functional early pregnancy factor expressed in Sf9 insect cells and in Escherichia coli. Protein Expr Purif 2003, 32: 276–287Google Scholar
Atkins, D, al Ghusein, H, Prehaud, C and Coates, A R M. Overproduction and purification of Mycobacterium tuberculosis chaperonin 10. Gene 1994, 150: 145–148Google Scholar
Ragno, S, Winrow, V R, Mascagni, P, Lucietto, P, Di Pierro, F, Morris, C J and Blake, D R. A synthetic 10-kD heat shock protein (hsp10) from Mycobacterium tuberculosis modulates adjuvant arthritis. Clin Exp Immunol 1996, 103: 384–390Google Scholar
Riffo-Vasquez, Y, Spina, D, Page, C, Tormay, P, Singh, M, Henderson, B and Coates, A R M. Effect of Mycobacterium tuberculosis chaperonins on bronchial eosinophilia and hyperresponsiveness in a murine model of allergic inflammation. Clin Exp Allergy 2004, 34: 712–719Google Scholar
Zhang, B, Walsh, M D, Nguyen, K B, Hillyard, N C, Cavanagh, A C, McCombe, P A and Morton, H. Early pregnancy factor treatment suppresses the inflammatory response and adhesion molecule expression in the spinal cord of SJL/J mice with experimental autoimmune encephalomyelitis and the delayed-type hypersensitivity reaction to trinitrochlorobenzene in normal BALB/c mice. J Neurol Sci 2003, 212: 37–46Google Scholar
Athanasas-Platsis, S, Zhang, B, Hillyard, N C, Cavanagh, A C, Csurhes, P A, Morton, H and McCombe, P A. Early pregnancy factor suppresses the infiltration of lymphocytes and macrophages in the spinal cord of rats during experimental autoimmune encephalomyelitis but has no effect on apoptosis. J Neurol Sci 2003, 214: 27–36Google Scholar
Spik, G, Haendler, B, Delmas, O, Mariller, C, Chamoux, M, Maes, P, Tartar, A, Montreuil, J, Stedman, K, Kocher, H P, Roland Kellers, R, Hiestand, P C and Movva, N R. A novel secreted cyclophilin-like protein (SCYLP). J Biol Chem 1991, 266: 10735–10738Google Scholar
Allain, F, Boutillon, C, Mariller, C and Spik, G. Selective assay for CypA and CypB in human blood using highly specific anti-peptide antibodies. J Immunol Methods 1995, 178: 113–120Google Scholar
Billich, A, Winkler, G, Aschauer, H, Rot, A and Peichl, P. Presence of cyclophilin A in synovial fluids of patients with rheumatoid arthritis. J Exp Med 1997, 185: 975–980Google Scholar
Tegeder, I, Schumacher, A, John, S, Geiger, H, Geisslinger, G, Bang, H and Brune, K. Elevated serum cyclophilin levels in patients with severe sepsis. J Clin Immunol 1997, 17: 380–386Google Scholar
Kol, A, Lichtman, A H, Finberg, R W, Libby, P and Kurt-Jones, E A. Heat shock protein (HSP) 60 activates the innate immune response: CD14 is an essential receptor for HSP60 activation of mononuclear cells. J Immunol 2000, 164: 13–17Google Scholar
Vabulas, R M, Ahmad-Nejad, P, da Costa, C, Miethke, T, Kirschning, C J, Hacker, H and Wagner, H. Endocytosed HSP60s use toll-like receptor 2 (TLR2) and TLR4 to activate the toll/interleukin-1 receptor signaling pathway in innate immune cells. J Biol Chem 2001, 276: 31332–31339Google Scholar
Yoshida, N, Oeda, K, Watanabe, E, Mikami, T, Fukita, Y, Nishimura, K, Komai, K and Matsuda, K. Protein function. Chaperonin turned insect toxin. Nature 2001, 411: 44Google Scholar
Gupta, S and Knowlton, A A. Cytosolic heat shock protein 60, hypoxia, and apoptosis. Circulation 2002, 106: 2727–2733Google Scholar
Kirchhoff, S R, Gupta, S and Knowlton, A A. Cytosolic heat shock protein 60, apoptosis, and myocardial injury. Circulation 2002, 105: 2899–2904Google Scholar
Knowlton, A A and Sun, L. Heat-shock factor-1, steroid hormones, and regulation of heat-shock protein expression in the heart. Am J Physiol Heart Circ Physiol 2001, 280: H455–464Google Scholar
Pratt, W B. The hsp90-based chaperone system: involvement in signal transduction from a variety of hormone and growth factor receptors. Proc Soc Exp Biol Med 1998, 217: 420–434Google Scholar
Xu, Q, Luef, G, Weimann, S, Gupta, R S, Wolf, H and Wick, G. Staining of endothelial cells and macrophages in atherosclerotic lesions with human heat shock protein-reactive antisera. Arteriosclerosis Thrombosis 1993, 13: 1763–1769Google Scholar
Shamaei-Tousi, A, Steptoe, A, Coates, A and Henderson, B. Circulating chaperonin 60 in the plasma of British civil servants. Biochem Soc Trans 2004, ‘abstr 13’Google Scholar
Libby, P. Current concepts of the pathogenesis of the acute coronary syndromes. Circulation 2001, 104: 365–372Google Scholar
Hemingway, H and Marmot, M. Evidence based cardiology: psychosocial factors in the aetiology and prognosis of coronary heart disease. Systematic review of prospective cohort studies. Brit Med J 1999, 318: 1460–1467Google Scholar
Olson, N C, Hellyer, P W and Dodam, J R. Mediators and vascular effects in response to endotoxin. Brit Vet J 1995, 151: 489–522Google Scholar
Sangster, T A, Lindquist, S and Queitsch, C. Under cover: causes, effects and implications of Hsp90-mediated genetic capacitance. Bioessays 2004, 26: 348–362Google Scholar
Srivastava, P. Roles of heat-shock proteins in innate and adaptive immunity. Nat Rev Immunol 2002, 2: 185–194Google Scholar
Morales, H, Muharemagic, A, Gantress, J, Cohen, N and Robert, J. Bacterial stimulation upregulates the surface expression of the stress protein gp96 on B cells in the frog Xenopus. Cell Stress Chaperones 2003, 8: 265–271Google Scholar
Singh-Jasuja, H, Scherer, H U, Hilf, N, Arnold-Schild, D, Rammensee, H-G, Toes, R E M and Schild, H. The heat shock protein gp96 induces maturation of dendritic cells and down-regulation of its receptor. Eur J Immunol 2000, 30: 2211–2215Google Scholar
Binder, R J and Srivastava, P K. Essential role of CD91 in re-presentation of gp96-chaperoned peptides. Proc Natl Acad Sci USA 2004, 101: 6128–6133Google Scholar
Liu, B, Dai, J, Zheng, H, Stoilova, D, Sun, S and Li, Z. Cell surface expression of an endoplasmic reticulum resident heat shock protein gp96 triggers MyD88-dependent systemic autoimmune diseases. Proc Nat Acad Sci USA 2003, 100: 15824–15829Google Scholar
Karunakaran, K P, Noguchi, Y, Read, T D, Cherkasov, A, Kwee, J, Shen, C, Nelson, C C and Brunham, R C. Molecular analysis of the multiple GroEL proteins of Chlamydiae. J Bacteriol 2003, 185: 1958–1966Google Scholar
Gerard, H C, Whittum-Hudson, J A, Schumacher, H R and Hudson, A P. Differential expression of three Chlamydia trachomatis hsp60-encoding genes in active vs persistent infections. Microb Pathogenesis 2004, 36: 35–39Google Scholar
Fabian, T K, Gaspar, J, Fejerdy, L, Kaan, B, Balint, M, Csermely, P and Fejerdy, P. Hsp70 is present in human saliva. Med Sci Monit 2003, 9: 62–65Google Scholar
Utleg, A G, Yi, E C, Xie, T, Shannon, P, White, J T, Goodlett, D R, Hood, L and Lin, B. Proteomic analysis of human prostasomes. Prostate 2003, 56: 150–161Google Scholar
Trougakos, I P and Gonos, E S. Clusterin/apolipoprotein J in human aging and cancer. Int J Biochem Cell Biol 2002, 34: 1430–1448Google Scholar
Rammes, A, Roth, J, Goebeler, M, Klempt, M, Hartmann, M and Sorg, C. Myeloid-related protein (MRP) 8 and MRP14, calcium-binding proteins of the S100 family, are secreted by activated monocytes via a novel, tubulin-dependent pathway. J Biol Chem 1997, 272: 9496–9502Google Scholar
Matzinger, P. The Danger Model: A renewed sense of self. Science 2002, 296: 301–305Google Scholar
Maguire, M, Coates, A R M and Henderson, B. Chaperonin 60 unfolds its secrets of cellular communication. Cell Stress Chaperones 2002, 7: 317–329Google Scholar
Wilson, M, McNab, R and Henderson, B.Bacterial Disease Mechanisms: An Introduction to Cellular Microbiology. Cambridge University Press: 2002
Asquith, K L, Baleato, R M, McLaughlin, E A, Nixon, B and Aitken, R J. Tyrosine phosphorylation activates surface chaperones facilitating sperm-zona recognition. J Cell Sci 2004, 117: 3645–3657Google Scholar
Ellis, R J. Proteins as molecular chaperones. Nature 1987, 328: 378–379Google Scholar

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