Cell-Cell Signalling Properties of Chaperonins

Anthony Coates; Peter Tormay

doi:10.1017/CBO9780511546310.007

6 - Cell-Cell Signalling Properties of Chaperonins

Published online by Cambridge University Press: 10 August 2009

Anthony Coates and

Peter Tormay

Edited by

Brian Henderson and

A. Graham Pockley

Show author details

Anthony Coates: Affiliation:
Department of Medical Microbiology, St. George's Hospital Medical School, London, United Kingdom
Peter Tormay: Affiliation:
Department of Medical Microbiology, St. George's Hospital Medical School, London, United Kingdom
Brian Henderson: Affiliation:
University College London
A. Graham Pockley: Affiliation:
University of Sheffield

Book contents

Get access

Summary

Introduction

In the beginning, bacteria evolved chaperonins (Cpns) to help in the folding of other proteins. Then, about one and a half billion years ago, bacteria began to live with eukaryotic cells. The career of the chaperonin began to expand beyond the protein folding area, and they developed new functions in order to adapt to the eukaryotic evolutionary niche. As the eukaryotes became ever more complex, the chaperonins evolved into cell-cell signalling molecules. The sophistication of this new role has only recently begun to emerge.

The chaperonins that are the subject of this chapter belong to the 60- and 10-kDa classes and are called Cpn60 and Cpn10, respectively. The folding actions of these proteins have been described in detail in Chapter 1. If there is more than one Cpn60 or Cpn10 in any one species, they are called Cpn60.1, Cpn60.2 and so on [1]. Cpn60 proteins are also called heat shock protein (Hsp) 60 or 65, and Cpn10s are also named Hsp10. For example, the Mycobacterium tuberculosis genome contains two cpn60 genes. One of these, termed cpn60.1 [2], appears to form an operon with the cpn10 gene. This is the usual relationship in most bacteria. The second cpn60 gene encodes Cpn60.2, the well-known Hsp65 protein of M. tuberculosis, and is found elsewhere in the genome.

What is a cell-cell signalling molecule?

A cell-cell signalling molecule is one that directly communicates a message from one cell to another.

Type: Chapter
Information: Molecular Chaperones and Cell Signalling , pp. 99 - 112

DOI: https://doi.org/10.1017/CBO9780511546310.007 [Opens in a new window]

Publisher: Cambridge University Press

Print publication year: 2005

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Coates, A R M, Shinnick, T M and Ellis, J R.Chaperonin nomenclature. Mol Microb 1993, 8: 787Google Scholar

Kong, T H, Coates, A R M, Butcher, P D, Hickman, C J and Shinnick, T M. Mycobacterium tuberculosis expresses two chaperonin-60 homologs. Proc Natl Acad Sci USA 1993, 90: 2608–2612Google 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

Soltys, B J and Gupta, R S. Mitochondrial-matrix proteins at unexpected locations: are they exported?Trends Biochem Sci 1999, 24: 174–177Google Scholar

Morton, H. Early pregnancy factor: an extracellular chaperonin 10 homologue. Immunol Cell Biol 1998, 76: 483–496Google Scholar

Goulhen, F, Hafezi, A, Uitto, V J, Hinode, D, Nakamura, R, Grenier, D and Mayrand, D. Subcellular localization and cytotoxic activity of the GroEL-like protein isolated from Actinobacillus actinomycetemcomitans. Infect Immun 1998, 66: 5307–5313Google Scholar

Kol, A, Sukhova, G K, Lichtman, A H and Libby, P. Chlamydial heat shock protein 60 localizes in human atheroma and regulates macrophage tumour necrosis factor-α and matrix metalloproteinase expression. Circulation 1998, 98: 300–307Google Scholar

Bassan, M, Zamostiano, R, Giladi, E, Davidson, A, Wollman, Y, Pitman, J, Hauser, J, Brenneman, D E and Gozes, I. The identification of secreted heat shock 60-like protein from rat glial cells and a human neuroblastoma cell line. Neurosci Lett 1998, 250: 37–40Google Scholar

Coates, A R M and Henderson, B. Chaperonins in health and disease. Ann NY Acad Sci 1998, 851: 48–53Google Scholar

Frisk, A, Ison, C A and Lagergard, T. GroEL heat shock protein of Haemophilus ducreyi: association with cell surface and capacity to bind to eukaryotic cells. Infect Immun 1998, 66: 1252–1257Google Scholar

Cavanagh, A C. Identification of early pregnancy factor as chaperonin 10: implications for understanding its role. Rev Reprod 1996, 1: 28–32Google Scholar

Esaguy, N and Aguas, A P. Subcellular localization of the 65-kDa heat shock protein in mycobacteria by immunoblotting and immunogold ultracytochemistry. J Submicrosc Cytol Pathol 1997, 29: 85–90Google Scholar

Brenneman, D E and Gozes, I. A femtomolar-acting neuroprotective peptide. J Clin Invest 1996, 97: 2299–2307Google Scholar

Sethna, K B, Mistry, N F, Dholakia, Y, Antia, N H and Harboe, M. Longitudinal trends in serum levels of mycobacterial secretory (30 kD) and cytoplasmic (65 kD) antigens during chemotherapy of pulmonary tuberculosis patients. Scand J Infect Dis 1998, 30: 363–369Google Scholar

Soltys, B J and Gupta, R S. Cell surface localization of the 60 kDa heat shock chaperonin protein (hsp60) in mammalian cells. Cell Biol Int 1997, 21: 315–320Google Scholar

Lewthwaite, J, Owen, N, Coates, A, Henderson, B and Steptoe, A. Circulating human heat shock protein 60 in the plasma of British civil servants. Circulation 2002, 106: 196–201Google Scholar

Fossati, G, Izzo, G, Rizzi, E, Gancia, E, Niccolai, N, Giannozzi, E, Spiga, O, Bono, L, Marone, P, Leone, E, Mangili, F, Harding, S, Errington, N, Walter, C, Henderson, B, Roberts, M M, Coates, A R M, Casetta, B and Mascagni, P. Mycobacterium tuberculosis chaperonin 10 is secreted in the macrophage phagolysosome: is secretion due to dissociation and the adoption of partially helical structure at the membrane?J Bact 2003, 185: 4256–4267Google 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

Winrow V R, Meghji S, Mesher J, Coates A R M, Morris C J, Tormay P and Henderson B. Mycobacterium tuberculosis chaperonin 60.1, but not chaperonin 60.2, inhibits osteoclastic bone resorption by blocking RANKL activity

Lewthwaite, J, George, R, Lund, P A, Poole, S, Tormay, P, Sharp, L, Coates, A R M and Henderson, B. Rhizobium leguminosarum chaperonin 60.3, but not chaperonin 60.1, induces cytokine production by human monocytes: activity is dependent on interaction with cell surface CD14. Cell Stress Chaperon 2002, 7: 130–136Google Scholar

Lewthwaite, J C, Coates, A R M, Tormay, P, Singh, M, Mascagni, P, Poole, S, Roberts, M, Sharp, L and Henderson, B. Mycobacterium tuberculosis chaperonin 60.1 is a more potent cytokine stimulator than chaperonin 60.2 (hsp 65) and contains a CD14-binding domain. Infect Immun 2001, 69: 7349–7355Google Scholar

Friedland, J S, Shattock, R, Remick, D G and Griffin, G E. Mycobacterial 65-kD heat shock protein induces release of proinflammatory cytokines from human monocytic cells. Clin Exp Immunol 1993, 91: 58–62Google Scholar

Tabona, P, Reddi, K, Khan, S, Nair, S P, Crean, S J, Meghji, S, Wilson, M, Preuss, M, Miller, A D, Poole, S, Carne, S and Henderson, B. Homogeneous Escherichia coli chaperonin 60 induces IL-1 and IL-6 gene expression in human monocytes by a mechanism independent of protein conformation. J Immunol 1998, 161: 1414–1421Google Scholar

Bethke, K, Staib, F, Distler, M, Schmitt, U, Jonuleit, H, Enk, A H, Galle, P R and Heike, M. Different efficiency of heat shock proteins to activate human monocytes and dendritic cells: superiority of HSP60. J Immunol 2002, 169: 6141–6148Google Scholar

Maguire, M, Coates, A R M and Henderson, B. Cloning expression and purification of three chaperonin 60 homologues. J Chromatography 2003, 786: 117–125Google Scholar

Kol, A, Bourcier, T, Lichtman, A and Libby, P. Chlamydial and human heat shock protein 60s activate human vascular endothelium, smooth muscle cells, and macrophages. J Clin Invest 1999, 103: 571–577Google Scholar

Billack, B, Heck, D E, Mariano, T M, Gardner, C R, Sur, R, Laskin, D L and Laskin, J D. Induction of cyclooxygenase-2 by heat shock protein 60 in macrophages and endothelial cells. Am J Physiol (Cell Physiol) 2002, 283: C1267–1277Google Scholar

Zhang, L, Pelech, S L, Mayrand, D, Grenier, D, Heino, J and Uitto, V J. Bacterial heat shock protein-60 increases epithelial cell proliferation through the ERK1/2 MAP kinases. Exp Cell Res 2001, 266: 11–20Google Scholar

Sasu, S, LaVerda, D, Qureshi, N, Golenbock, D T and Beasley, D. Chlamydia pneumoniae and chlamydial heat shock protein 60 stimulate proliferation of human vascular smooth muscle cells via toll-like receptor 4 and p44/p42 mitogen-activated protein kinase activation. Circ Res 2001, 89: 244–250Google Scholar

Flohé, S B, Bruggemann, J, Lendemans, S, Nikulina, M, Meierhoff, G, Flohé, S and Kolb, H. Human heat shock protein 60 induces maturation of dendritic cells versus a Th1-promoting phenotype. J Immunol 2003, 170: 2340–2348Google Scholar

Kirby, A C, Meghji, S, Nair, S P, White, P, Reddi, K, Nishihara, T, Nakashima, K, Willis, A C, Sim, R, Wilson, M and Henderson, B. The potent bone-resorbing mediator of Actinobacillus actinomycetemcomitans is homologous to the molecular chaperone GroEL. J Clin Invest 1995, 96: 1185–1194Google Scholar

Reddi, K, Meghji, S, Nair, S P, Arnett, T R, Miller, A D, Preuss, M, Wilson, M, Henderson, B and Hill, P. The Escherichia coli chaperonin 60 (groEL) is a potent stimulator of osteoclast formation. J Bone Miner Res 1998, 13: 1260–1266Google Scholar

Gozes, I, Divinsky, I, Pilzer, I, Fridkin, M, Brenneman, D E and Spier, A D. From vasoactive intestinal peptide (VIP) through activity-dependent neuroprotective protein (ADNP) to NAP: a view of neuroprotection and cell division. J Mol Neurosci 2003, 20: 315–322Google Scholar

Habich, C, Kempe, K, Zee, R, Burkart, V and Kolb, H. Different heat shock protein 60 species share pro-inflammatory activity but not binding sites on macrophages. FEBS Lett 2003, 533: 105–109Google 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

Rolfe, B, Cavanagh, A, Forde, C, Bastin, F, Chen, C and Morton, H. Modified rosette inhibition test with mouse lymphocytes for detection of early pregnancy factor in human pregnancy serum. J Immunol Methods 1984, 70: 1–11Google Scholar

Sadacharan, S K, Cavanagh, A C and Gupta, R S. Immunoelectron microscopy provides evidence for the presence of mitochondrial heat shock 10-kDa protein (chaperonin 10) in red blood cells and a variety of secretory granules. Histochem Cell Biol 2001, 116: 507–517Google Scholar

Zhang, L, Pelech, S and Uitto, V J. Long-term effect of heat shock protein 60 from Actinobacillus actinomycetemcomitans on epithelial cell viability and mitogen-activated protein kinases. Infect Immun 2004, 72: 38–45Google Scholar

Shan, Y X, Yang, T L, Mestril, R and Wang, P H. Hsp10 and Hsp60 suppress ubiquitination of insulin-like growth factor-1 receptor and augment insulin-like growth factor-1 receptor signaling in cardiac muscle: implications on decreased myocardial protection in diabetic cardiomyopathy. J Biol Chem 2003, 278: 45492–45498Google Scholar

Coates, A R M, Hewitt, J, Allen, B W, Ivanyi, J and Mitchison, D A. Antigenic diversity of Mycobacterium tuberculosis and Mycobacterium bovis detected by means of monoclonal antibodies. Lancet 1981, 2: 167–169Google Scholar

Coates A R M. Immunological aspects of chaperonins. In Ellis, R. J. (Ed.) The Chaperonins. Academic Press, London 1996, pp 267–296

Eden, W, Thole, J E R, Zee, R, Noordzij, A, Embden, J D A, Hensen, E J and Cohen, I R. Cloning of the mycobacterial epitope recognized by T lymphocytes in adjuvant arthritis. Nature 1988, 331: 171–173Google Scholar

Elias, D, Markovits, D, Reshef, T, Zee, R and Cohen, I R. Induction and therapy of autoimmune diabetes in the non-obese diabetic mouse by a 65-kDa heat shock protein. Proc Natl Acad Sci USA 1990, 87: 1576–1580Google Scholar

Srivastava, P K. Immunotherapy of human cancer: lessons from mice. Nat Immunol 2000, 1: 363–366Google Scholar

Raz, I, Elias, D, Avron, A, Tamir, M, Metzger, M and Cohen, I R. Beta-cell function in new-onset type 1 diabetes and immunomodulation with a heat-shock protein peptide (DiaPep277): a randomised, double-blind, phase II trial. Lancet 2001, 358: 1749–1753Google Scholar

Billingham M E J. Adjuvant arthritis: The first model. In Henderson, B., Edwards, J. C. W. and Pettipher, E. R. (Eds.) Mechanisms and Models in Rheumatoid Arthritis. Academic Press, London 1995, pp 389–409

Winrow, V R, Coates, A R M, Tormay, P, Henderson, B, Singh, M, Blake, D R and Morris, C J. Chaperonin 60.1 prevents bone destruction in Wistar rats with adjuvant-induced arthritis. Rheumatology 2002, 41 (abstr suppl 1): 47Google Scholar

Gozes, I and Brenneman, D E. Activity-dependent neurotrophic factor (ADNF). An extracellular neuroprotective chaperonin?J Mol Neurosci 1996, 7: 235–244Google 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

Cohen, I R. Peptide therapy for Type I diabetes: the immunological homunculus and the rationale for vaccination. Diabetologia 2002, 45: 1468–1474Google Scholar

Cohen, I R. The Th1/Th2 dichotomy, hsp60 autoimmunity, and type I diabetes. Clin Immunol Immunopathol 1997, 84: 103–106Google 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

Rha, Y-H, Taube, C, Haczku, A, Joeham, A, Takeda, K, Duez, C, Siegel, M, Ayditung, M K, Born, W K, Dakhama, A and Gelfand, E W. Effect of microbial heat shock proteins on airway inflammation and hyperresponsiveness. J Immunol 2002, 169: 5300–5307Google Scholar

Matzinger, P. An innate sense of danger. Semin Immunol 1998, 10: 399–415Google Scholar

Asea, A, Kraeft, S-K, Kurt-Jones, E A, Stevenson, M A, Chen, L B, Finberg, R W, Koo, G C and Calderwood, S K. Hsp70 stimulates cytokine production through a CD14-dependent pathway, demonstrating its dual role as a chaperone and cytokine. Nat Med 2000, 6: 435–442Google 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

Medzhitov, R and Janeway, C A J. Innate immunity: the virtues of a nonclonal system of recognition. Cell Stress Chaperon 1997, 91: 295–298Google Scholar

Takeda, K and Akira, S. Toll receptors and pathogen resistance. Cell Microbiol 2003, 5: 143–153Google Scholar

Girardin, S E, Sansonetti, P J and Philpott, D J. Intracellular vs extracellular recognition of pathogens – common concepts in mammals and flies. Trends Microbiol 2002, 10: 193–199Google Scholar

Colonna, M. TREMS in the immune system and beyond. Nat Rev Immunol 2003, 3: 1–9Google Scholar

Gao, B and Tsan, M F. Recombinant human heat shock protein 60 does not induce the release of tumor necrosis factor alpha from murine macrophages. J Biol Chem 2003, 278: 22523–22529Google Scholar

Book contents

6 - Cell-Cell Signalling Properties of Chaperonins

Summary

Access options

References

Save book to Kindle

Save book to Dropbox

Save book to Google Drive