Cell Stress and Chaperones

, Volume 14, Issue 4, pp 329–341 | Cite as

Unfolding the relationship between secreted molecular chaperones and macrophage activation states

Mini Review

Abstract

Over the last 20 years, it has emerged that many molecular chaperones and protein-folding catalysts are secreted from cells and function, somewhat in the manner of cytokines, as pleiotropic signals for a variety of cells, with much attention being focused on the macrophage. During the last decade, it has become clear that macrophages respond to bacterial, protozoal, parasitic and host signals to generate phenotypically distinct states of activation. These activation states have been termed ‘classical’ and ‘alternative’ and represent not a simple bifurcation in response to external signals but a range of cellular phenotypes. From an examination of the literature, the hypothesis is propounded that mammalian molecular chaperones are able to induce a wide variety of alternative macrophage activation states, and this may be a system for relating cellular or tissue stress to appropriate macrophage responses to restore homeostatic equilibrium.

Keywords

Molecular chaperones Macrophages Macrophage activation Inflammation 

Notes

Acknowledgments

BH acknowledges financial support from the Wellcome Trust. SH is grateful to Professor Salvador Moncada, The Wolfson Institute for Biomedical Research, University College London, for financial support. We would like to thank the referees for providing incisive comments and to one of the referees for his suggestion that non-folding stress proteins may also play a role in modulating cell behaviour.

References

  1. Adams DO, Hamilton TA (1984) The cell biology of macrophage activation. Annu Rev Immunol 2:283–318 doi: 10.1146/annurev.iy.02.040184.001435 PubMedGoogle Scholar
  2. Aliberti J, Valenzuela JG, Carruthers VB et al (2003) Molecular mimicry of a CCR5 binding-domain in the microbial activation of dendritic cells. Nat Immunol 4:485–490 doi: 10.1038/ni915 PubMedGoogle Scholar
  3. Arrigo AP (2007) The cellular “networking” of mammalian Hsp27 and its functions in the control of protein folding, redox state and apoptosis. Adv Exp Med Biol 594:14–26 doi: 10.1007/978-0-387-39975-1_2 PubMedGoogle Scholar
  4. Asea A, Kraeft S-K, Kurt-Jones EA, Stevenson MA, Chen LB, Finberg RW, Koo GC, Calderwood SK (2000) Hsp70 stimulates cytokine production through a CD14-dependent pathway, demonstrating its dual role as a chaperone and cytokine. Nature Med 6:435–442 doi: 10.1038/74697 PubMedGoogle Scholar
  5. Asea A, Rehli M, Kabingu E, Boch JA, Bare O, Auron PE, Stevenson MA, Calderwood SK (2002) Novel signal transduction pathway utilized by extracellular HSP70: role of toll-like receptor (TLR) 2 and TLR4. J Biol Chem 277:15028–15034 doi: 10.1074/jbc.M200497200 PubMedGoogle Scholar
  6. Asquith KL, Baleato RM, McLaughlin EA, Nixon B, Aitken RJ (2004) Tyrosine phosphorylation activates surface chaperones facilitating sperm-zona recognition. J Cell Sci 117:3645–3657 doi: 10.1242/jcs.01214 PubMedGoogle Scholar
  7. Babaahmady K, Oehlmann W, Singh M, Lehner T (2007) Inhibition of human immunodeficiency virus type 1 infection of human CD4+ T cells by microbial HSP70 and the peptide epitope 407–426. J Virol 81:3354–3360 doi: 10.1128/JVI.02320-06 PubMedGoogle Scholar
  8. Berndt C, Lillig CH, Holmgren A (2008) Thioredoxins and glutaredoxins as facilitators of protein folding. Biochim Biophys Acta 1783:641–650 doi: 10.1016/j.bbamcr.2008.02.003 PubMedGoogle Scholar
  9. Bernhagen J, Krohn R, Lue H et al (2007) MIF is a noncognate ligand of CXC chemokine receptors in inflammatory and atherogenic cell recruitment. Nat Med 13:587–596 doi: 10.1038/nm1567 PubMedGoogle Scholar
  10. Bertini R, Howard OMZ, Dong H-F et al (1999) Thioredoxin, a redox enzyme released in infection and inflammation, is a unique chemoattractant for neutrophils, monocytes and T cells. J Exp Med 189:1783–1789 doi: 10.1084/jem.189.11.1783 PubMedGoogle Scholar
  11. Billiet L, Furman C, Larigauderie G, Copin C, Brand K, Fruchart JC, Rouis M (2005) Extracellular human thioredoxin-1 inhibits lipopolysaccharide-induced interleukin-1beta expression in human monocyte-derived macrophages. J Biol Chem 280:40310–40318 doi: 10.1074/jbc.M503644200 PubMedGoogle Scholar
  12. Bomford R, Henderson B (1989) Interleukin-1, inflammation and disease. North Holland, ElsevierGoogle Scholar
  13. Cascales E (2008) The type VI secretion toolkit. EMBO Rep 9:735–741 doi: 10.1038/embor.2008.131 PubMedGoogle Scholar
  14. Cavanagh AC, Morton H (1994) The purification of early-pregnancy factor to homogeneity from human platelets and identification as chaperonin 10. Eur J Biochem 222:551–560 doi: 10.1111/j.1432-1033.1994.tb18897.x PubMedGoogle Scholar
  15. Cicala C, Arthos J, Martinelli E, Censoplano N, Cruz CC, Chung E et al (2005) R5 and X4 HIV envelopes induce distinct gene expression profiles in primary peripheral blood mononuclear cells. Proc Natl Acad Sci USA 103:3746–3751 doi: 10.1073/pnas.0511237103 Google Scholar
  16. Conway JP, KInter M (2006) Dual role of peroxiredoxin I in macrophage-derived foam cells. J Biol Chem 281:27991–28001 doi: 10.1074/jbc.M605026200 PubMedGoogle Scholar
  17. Corrigall VM, Bodman-Smith MD, Fife MS et al (2001) The human endoplasmic reticulum molecular chaperone BiP is an autoantigen for rheumatoid arthritis and prevents the induction of experimental arthritis. J Immunol 166:1492–1498PubMedGoogle Scholar
  18. Corrigall VM, Bodman-Smith M, Panayi GS (2005) BiP stimulation induces and anti-inflammatory gene activation profile in monocytes. Rheumatology 44(Suppl):48Google Scholar
  19. Czarnecka AM, Campanella C, Zummo G, Capello F (2006) Heat shock protein 10 and signal transduction: a ‘capsula eburnea’ of carcinogenesis? Cell Stress Chaperones 11:287–294 doi: 10.1379/CSC-200.1 PubMedGoogle Scholar
  20. Daugaard M, Rohde M, Jaattela M (2007) The heat shock protein 70 family: highly homologous proteins with overlapping and distinct functions. FEBS Letts 581:3702–3710 doi: 10.1016/j.febslet.2007.05.039 Google Scholar
  21. De AK, Kodys KM, Yeh BS, Miller-Graziano C (2000) Exaggerated human monocyte IL-10 concomitant to minimal TNF-alpha induction by heat-shock protein 27 (Hsp27) suggests Hsp27 is primarily an antiinflammatory stimulus. J Immunol 165:3951–3958PubMedGoogle Scholar
  22. Donnelly S, O’Neill SM, Sekiya M, Mulcahy G, Dalton JP (2005) Thioredoxin peroxidase secreted by Fasciola hepatica induces the alternative activation of macrophages. Infect Immun 73:166–173 doi: 10.1128/IAI.73.1.166-173.2005 PubMedGoogle Scholar
  23. Ettrich R, Brandt W Jr, Kopecký V, Baumruk V, Hofbauerová K, Pavlícek Z (2002) Study of chaperone-like activity of human haptoglobin: conformational changes under heat shock conditions and localization of interaction sites. Biol Chem 383:1667–1676 doi: 10.1515/BC.2002.187 PubMedGoogle Scholar
  24. Fanghänel J, Fischer G (2004) Insights into the catalytic mechanism of peptidyl prolyl cis/trans isomerases. Front Biosci 9:3453–3478 doi: 10.2741/1494 PubMedGoogle Scholar
  25. Fevrier B, Raposo G (2004) Exosomes: endosomal-derived vesicles shipping extracellular messages. Curr Opin Cell Biol 16:415–421 doi: 10.1016/j.ceb.2004.06.003 PubMedGoogle Scholar
  26. Friedland JS, Shattock R, Remick DG, Griffin GE (1993) Mycobacterial 65-kDa heat shock protein induces release of proinflammatory cytokines from human monocytic cells. Clin Exp Immunol 91:58–62PubMedCrossRefGoogle Scholar
  27. Gething M-J (1997) Guidebook to molecular chaperones and protein-folding catalysts. University Press, OxfordGoogle Scholar
  28. Glezer I, Simard AR, Rivest S (2007) Neuroprotective role of the innate immune system by microglia. Neuroscience 147:867–883 doi: 10.1016/j.neuroscience.2007.02.055 PubMedGoogle Scholar
  29. Gobert AP, Bambou JC, Werts C, Balloy V, Chignard M, Moran AP, Ferrero RL (2004) 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 279:245–250 doi: 10.1074/jbc.M307858200 PubMedGoogle Scholar
  30. Goerdt S, Politz O, Schledzewski K et al (1999) Alternative versus classical activation of macrophages. Pathobiology 67:222–226 doi: 10.1159/000028096 PubMedGoogle Scholar
  31. Golding H, Aliberti J, King LR, Manischewitz J, Andersen J, Valenzuela J, Landau NR, Sher A (2003) Inhibition of HIV-1 infection by a CCR5-binding cyclophilin from Toxoplasma gondii. Blood 102:3280–3286 doi: 10.1182/blood-2003-04-1096 PubMedGoogle Scholar
  32. Goldmann O, von Köckritz-Blickwede M, Höltje C, Chhatwal GS, Geffers R, Medina E (2007) Transcriptome analysis of murine macrophages in response to infection with Streptococcus pyogenes reveals an unusual activation program. Infect Immun 75:4148–4157 doi: 10.1128/IAI.00181-07 PubMedGoogle Scholar
  33. Gordon S (1999) Macrophages and the immune system. In: Paul WE (ed) Fundamental immunology. 4th edn. Lippincott-Raven, Philidelphia, pp 533–545Google Scholar
  34. Gordon S (2003) Alternative activation of macrophages. Nat Rev Immunol 3:23–35 doi: 10.1038/nri978 PubMedGoogle Scholar
  35. Gordon S (2007) Macrophage heterogeneity and tissue lipids. J Clin Invest 117:89–93 doi: 10.1172/JCI30992 PubMedGoogle Scholar
  36. Hahn H, Kaufmann SH (1982) T lymphocyte-macrophage interactions in cellular antibacterial immunity. Immunobiology 161:361–368PubMedGoogle Scholar
  37. Halcox JP, Shamaei-Tousi A, Steptoe A, Coates AR, Henderson B, Deanfield J (2005) Circulating human heat shock protein 60 in the blood of healthy teenagers: a novel determinant of endothelial dysfunction and early vascular injury? Arterioscler Thromb Vasc Biol 25:141–142 doi: 10.1161/01.ATV.0000185832.34992.ff Google Scholar
  38. Harness J, Cavanagh A, Morton H, McCombe P (2003) A protective effect of early pregnancy factor on experimental autoimmune encephalomyelitis induced in Lewis rats by inoculation with myelin basic protein. J Neurol Sci 216:33–41 doi: 10.1016/S0022-510X(03)00212-0 PubMedGoogle Scholar
  39. Helming L, Gordon S (2008) The molecular basis of macrophage fusion. Immunobiol 212:785–793 doi: 10.1016/j.imbio.2007.09.012 Google Scholar
  40. Henderson B, Poole S, Wilson M (1998) Bacteria-cytokine interactions in health and disease. Portland, LondonGoogle Scholar
  41. Hightower LE, Guidon PT (1989) Selective release from cultured mammalian cells of heat-shock (stress) proteins that resemble glia-axon transfer proteins. J Cell Physiol 138:257–266 doi: 10.1002/jcp.1041380206 PubMedGoogle Scholar
  42. Hill JE, Penny SL, Crowell KG, Goh SH, Hemmingsen SM (2004) cpnDB: a chaperonin sequence database. Genome Res 14:1669–1675 doi: 10.1101/gr.2649204 PubMedGoogle Scholar
  43. Holmgren A (1985) Thioredoxin. Annu Rev Biochem 54:237–271 doi: 10.1146/annurev.bi.54.070185.001321 PubMedGoogle Scholar
  44. Holt PG (1986) Down-regulation of immune responses in the lower respiratory tract: the role of alveolar macrophages. Clin Exp Immunol 63:261–270PubMedGoogle Scholar
  45. Hu Y, Henderson B, Lund PA, Tormay P, Liu HL, Gurcha SS, Besra GS, Coates ARM (2008) A Mycobacterium tuberculosis mutant lacking the groEL homologue cpn60.1 is viable, but fails to induce an inflammatory response in animal models of infection. Infect Immun 76:1535–1546 doi: 10.1128/IAI.01078-07 PubMedGoogle Scholar
  46. Johnson BJ, Le TT, Dobbin CA et al (2005) Heat shock protein 10 inhibits lipopolysaccharide-induced inflammatory mediator production. J Biol Chem 280:4037–4047 doi: 10.1074/jbc.M411569200 PubMedGoogle Scholar
  47. Kampinga HH, Hageman J, Vos MJ, Kubota H, Tanguay RM, Bruford EA, Cheetham ME, Chen B, Hightower LE (2008) Guideline for the nomenclature of the human heat shock proteins. Cell Stress Chaperones (in press)Google Scholar
  48. Khan N, Alam K, Mande SC, Valluri VL, Hasnain SE, Mukhopadhyay S (2008) Mycobacterium tuberculosis heat shock protein 60 modulates immune response to PPD by manipulating the surface expression of TLR2 on macrophages. Cell Microbiol 10:1711–1722PubMedGoogle Scholar
  49. Kim K-P, Jagadeesan B, Burkholder KM, Jaradat ZW, Wampler JL, Lathrop AA, Morgan MT, Bhunia AK (2006) Adhesion characteristics of Listeria adhesion protein (LAP)-expressing Escherichia coli to Caco-2 cells and of recombinant LAP to eukaryotic receptor Hsp60 as examined in a surface plasmon resonance sensor. FEMS Microbiol Lett 256:324–332 doi: 10.1111/j.1574-6968.2006.00140.x PubMedGoogle Scholar
  50. Kirby AC, Meghji S, Nair SP et al (1995) The potent bone resorbing mediator of Actinobacillus actinomycetemcomitans is homologous to the molecular chaperone GroEL. J Clin Invest 96:1185–1194 doi: 10.1172/JCI118150 PubMedGoogle Scholar
  51. Kleemann R, Kapurniotu A, Frank RW et al (1998) Disulfide analysis reveals a role for macrophage migration inhibitory factor (MIF) as thiol-protein oxidoreductase. J Mol Biol 280:85–102 doi: 10.1006/jmbi.1998.1864 PubMedGoogle Scholar
  52. Laudanski K, De A, Miller-Graziano C (2007) Exogenous heat shock protein 27 uniquely blocks differentiation of monocytes to dendritic cells. Eur J Immunol 37:2812–2824 doi: 10.1002/eji.200636993 PubMedGoogle Scholar
  53. Lehner T, Wang Y, Whittall T, Bergmeier LA (2005) Heat shock proteins, their cell surface receptors and effects on the immune system. In: Henderson B, Pockley AG (eds) Molecular chaperones and cell signalling. Cambridge University Press, Cambridge, pp 160–178Google Scholar
  54. Lewthwaite JC, Coates ARM, Tormay P, Singh M, Mascagni P, Poole S, Roberts M, Sharp L, Henderson B (2001) 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 69:7349–7355 doi: 10.1128/IAI.69.12.7349-7355.2001 PubMedGoogle Scholar
  55. Lewthwaite JC, George R, Lund PA, Poole S, Tormay P, Sharp L, Coates ARM, Henderson B (2002a) 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 Chaperones 7:130–136 doi: 10.1379/1466-1268(2002)007<0130:RLCBNC>2.0.CO;2 PubMedGoogle Scholar
  56. Lewthwaite J, Owen N, Coates ARM, Henderson B, Steptoe AD (2002b) Circulating heat shock protein (Hsp)60 in the plasma of British civil servants: relationship to physiological and psychosocial stress. Circulation 106:196–201 doi: 10.1161/01.CIR.0000021121.26290.2C PubMedGoogle Scholar
  57. Liu W, Nakamura H, Shioji K et al (2004) Thioredoxin-1 ameliorates myosin-induced autoimmune myocarditis by suppressing chemokine expressions and leukocyte chemotaxis in mice. Circulation 110:1276–1283 doi: 10.1161/01.CIR.0000141803.41217.B6 PubMedGoogle Scholar
  58. Lynes MA, Zaffuto K, Unfricht DW, Marusov G, Samson JS, Yin X (2006) The physiological roles of extracellular metallothionein. Exp Biol Med (Maywood) 231:1548–1554Google Scholar
  59. Mackaness GB (1962) Cellular resistance to infection. J Exp Med 116:381–406 doi: 10.1084/jem.116.3.381 PubMedGoogle Scholar
  60. Maguire M, Coates ARM, Henderson B (2002) Chaperonin 60 unfolds its secrets of cellular communication. Cell Stress Chaperones 7:317–329 doi: 10.1379/1466-1268(2002)007<0317:CUISOC>2.0.CO;2 PubMedGoogle Scholar
  61. Mambula SS, Stevenson MA, Ogawa K, Calderwood SK (2007) Mechanisms for Hsp70 secretion: crossing membranes without a leader. Methods 43:168–175 doi: 10.1016/j.ymeth.2007.06.009 PubMedGoogle Scholar
  62. Mantovani A, Sica A, Sozzani S, Allavena P, Vecchi A, Locati M (2004) The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol 25:677–686 doi: 10.1016/j.it.2004.09.015 PubMedGoogle Scholar
  63. Martinez FO, Sica A, Mantovani A, Locati M (2008) Macrophage activation and polarization. Front Biosci 13:453–461 doi: 10.2741/2692 PubMedGoogle Scholar
  64. Matzinger P (2002) The danger model: a renewed sense of self. Science 296:301–305 doi: 10.1126/science.1071059 PubMedGoogle Scholar
  65. Meghji S, White PA, Nair SP et al (1997) Mycobacterium tuberculosis chaperonin 10 stimulates bone resorption: a potential contributory factor in Pott’s disease. J Exp Med 186:1241–1246 doi: 10.1084/jem.186.8.1241 PubMedGoogle Scholar
  66. Meghji S, Lillicrap M, Maguire M, Tabona P, Gaston JSH, Poole S, Henderson B (2003) Human chaperonin 60 (Hsp60) stimulates bone resorption: structure/function relationships. Bone 33:419–425 doi: 10.1016/S8756-3282(03)00117-0 PubMedGoogle Scholar
  67. Metchnikoff E (1905) Immunity to infective diseases. Cambridge University Press, LondonGoogle Scholar
  68. Miller-Graziano CL, De A, Laudanski K, Herrmann T, Bandyopadhyay S (2008) HSP27: an anti-inflammatory and immunomodulatory stress protein acting to dampen immune function. Novartis Found Symp 291:196–208 doi: 10.1002/9780470754030.ch15 PubMedGoogle Scholar
  69. Moestrup SK, Møller HJ (2004) CD163: a regulated hemoglobin scavenger receptor with a role in the anti-inflammatory response. Ann Med 36:347–354 doi: 10.1080/07853890410033171 PubMedGoogle Scholar
  70. Morton H, Rolfe B, Clunie GJ (1977) An early pregnancy factor detected in human serum by the rosette inhibition test. Lancet 1:394–397 doi: 10.1016/S0140-6736(77)92605-8 PubMedGoogle Scholar
  71. Nakamura H (2008) Extracellular functions of thioredoxin. Novartis Found Symp 291:184–192 (discussion 192–5, 221–224)PubMedGoogle Scholar
  72. Nakamura H, Herzenberg LA, Bai J, Araya S, Kondo N, Nishinaka Y, Herzenberg LA, Yodoi J (2001a) Circulating thioredoxin suppresses lipopolysaccharide-induced neutrophil chemotaxis. Proc Natl Acad Sci U SA 98:15143–15148 doi: 10.1073/pnas.191498798 Google Scholar
  73. Nakamura H, De Rosa SC, Yodoi J, Holmgren A, Ghezzi P, Herzenberg LA, Herzenberg LA (2001b) Chronic elevation of plasma thioredoxin: inhibition of chemotaxis and curtailment of life expectancy in AIDS. Proc Natl Acad Sci U S A 98:2688–2693 doi: 10.1073/pnas.041624998 PubMedGoogle Scholar
  74. Nathan CF, Murray HW, Weibe ME, Rubin BY (1983) Identification of interferon-gamma as the lymphokine that activates human macrophage oxidative metabolism and antimicrobial activity. J Exp Med 158:670–689 doi: 10.1084/jem.158.3.670 PubMedGoogle Scholar
  75. Noonan FP, Halliday WJ, Morton H, Clunie GJ (1979) Early pregnancy factor is immunosuppressive. Nature 278:649–651 doi: 10.1038/278649a0 PubMedGoogle Scholar
  76. Panayi GS, Corrigall VM (2008) BiP, an anti-inflammatory ER protein, is a potential new therapy for the treatment of rheumatoid arthritis. Novartis Found Symp 291:212–220 doi: 10.1002/9780470754030.ch16 PubMedGoogle Scholar
  77. Pekkari K, Goodarzi MT, Scheynius A, Holmgen A, Avila-Carino J (2005) Truncated thioredoxin (Trx80) induces differentiation of human CD14+ monocytes into a novel cell type (TAMs) via activation of the MAP kinases p38, ERK and JNK. Blood 105:1598–1605 doi: 10.1182/blood-2004-04-1577 PubMedGoogle Scholar
  78. Porta C, Subhra Kumar B, Larghi P, Rubino L, Mancino A, Sica A (2007) Tumor promotion by tumor-associated macrophages. Adv Exp Med Biol 604:67–86 doi: 10.1007/978-0-387-69116-9_5 PubMedGoogle Scholar
  79. Puissegur MP, Botanch C, Duteyrat JL, Delsol G, Caratero C, Altare F (2004) An in vitro dual model of mycobacterial granulomas to investigate the molecular interactions between mycobacteria and human host cells. Cell Microbiol 6:423–433 doi: 10.1111/j.1462-5822.2004.00371.x PubMedGoogle Scholar
  80. Quaye IK (2008) Haptoglobin, inflammation and disease. Trans R Soc Trop Med Hyg 102:735–742PubMedGoogle Scholar
  81. Randow F, Seed B (2001) Endoplasmic reticulum chaperone gp96 is required for innate immunity but not cell viability. Nat Cell Biol 3:891–896 doi: 10.1038/ncb1001-891 PubMedGoogle Scholar
  82. Rayner K, Chen YX, McNulty M, Simard T, Zhao X, Wells DJ, de Belleroche J, O’Brien ER (2008) Extracellular release of the atheroprotective heat shock protein 27 is mediated by estrogen and competitively inhibits acLDL binding to scavenger receptor-A. Circ Res 103:133–141PubMedGoogle Scholar
  83. Reddi K, Meghji S, Nair SP, Arnett TR, Miller AD, Preuss M, Wilson M, Henderson B, Hill P (1998) The Escherichia coli chaperonin 60 (groEL) is a potent stimulator of osteoclast formation. J Bone Miner Res 13:1260–1266 doi: 10.1359/jbmr.1998.13.8.1260 PubMedGoogle Scholar
  84. Rha Y, Taube C, Haczku A et al (2002) Effect of microbial heat shock proteins on airway inflammation and hyperresponsiveness. J Immunol 169:5300–5307PubMedGoogle Scholar
  85. Rhee SG, Chae HZ, Kim K (2005) Peroxiredoxins: a historical overview and speculative preview of novel mechanisms and emerging concepts in cell signaling. Free Radic Biol Med 38:1543–1552 doi: 10.1016/j.freeradbiomed.2005.02.026 PubMedGoogle Scholar
  86. Riffo-Vasquez Y, Spina D, Page C, Desel C, Whelan M, Tormay P, Singh M, Henderson B, Coates ARM (2004) Differential effects of Mycobacterium tuberculosis chaperonins on bronchial eosinophilia and hyperresponsiveness in a murine model of allergic inflammation. Clin Exp Allergy 34:712–719 doi: 10.1111/j.1365–2222.2004.1931.x PubMedGoogle Scholar
  87. Rodriguez NE, Chang HK, Wilson ME (2004) Novel program of macrophage gene expression induced by phagocytosis of Leishmania chagasi. Infect Immun 72:2111–2122 doi: 10.1128/IAI.72.4.2111-2122.2004 PubMedGoogle Scholar
  88. Rook GA, Dheda K, Zumla A (2005) Immune responses to tuberculosis in developing countries: implications for new vaccines. Nat Rev Immunol 5:661–667 doi: 10.1038/nri1666 PubMedGoogle Scholar
  89. Rutkowski DT, Kaufman RJ (2004) A trip to the ER: coping with stress. Trends Cell Biol 14:20–27 doi: 10.1016/j.tcb.2003.11.001 PubMedGoogle Scholar
  90. Shamaei-Tousi A, D’Aiuto F, Nibali L, Steptoe A, Coates AR, Parkar M, Donos N, Henderson B (2007a) Differential regulation of circulating levels of molecular chaperones in patients undergoing treatment for periodontal disease. PLoS One 2:e1198 doi: 10.1371/journal.pone.0001198 PubMedGoogle Scholar
  91. Shamaei-Tousi A, Steptoe A, O’Donnell K et al (2007b) Plasma heat shock protein 60 and cardiovascular disease risks: the role of psychosocial, genetic and biological factors. Cell Stress Chaperones 12:284–392 doi: 10.1379/CSC-300.1 Google Scholar
  92. Sherry B, Yarlett N, Strupp A, Cerami A (1992) Identification of cyclophilin as a proinflammatory secretory product of lipopolysaccharide-activated macrophages. Proc Natl Acad Sci U S A 89:3511–3515 doi: 10.1073/pnas.89.8.3511 PubMedGoogle Scholar
  93. Sherry B, Zybarth G, Alfano M, Dubrovsky L, Mitchell R, Rich D, Ulrich P, Bucala R, Cerami A, Bukrinsky M (1998) Role of cyclophilin A in the uptake of HIV-1 by macrophages and T lymphocytes. Proc Natl Acad Sci U S A 95:1758–1763 doi: 10.1073/pnas.95.4.1758 PubMedGoogle Scholar
  94. Sica A, Allavena P, Mantovani A (2008) Cancer related inflammation: the macrophage connection. Cancer Lett 267:204–215PubMedGoogle Scholar
  95. Silberstein DS, Ali MH, Baker SL, David JR (1989) Human eosinophil cytotoxicity-enhancing factor. Purification, physical characteristics, and partial amino acid sequence of an active polypeptide. J Immunol 143:979–983PubMedGoogle Scholar
  96. Soderberg A, Sahaf B, Rosen A (2000) Thioredoxin reductase, a redox-active selenoprotein, is secreted by normal and neoplastic cells: presence in the human plasma. Cancer Res 60:2281–2289PubMedGoogle Scholar
  97. Splettstoesser WD, Schuff-Werner P (2002) Oxidative stress in macrophages—“the enemy within”. Micros Res Tech 57:441–445 doi: 10.1002/jemt.10098 Google Scholar
  98. Stein M, Keshav S, Harris N, Gordon S (1992) Interleukin 4 potently enhances murine macrophage mannose receptor activity: a marker of alternative immunologic macrophage activation. J Exp Med 176:287–292 doi: 10.1084/jem.176.1.287 PubMedGoogle Scholar
  99. Tagayi Y, Maeda Y, Mitsui A et al (1989) ATL-derived factor (ADF), and IL-2 receptor/Tac inducer homologous to thioredoxin; possible involvement in dithiol reduction in the IL-2 receptor induction. EMBO J 8:757–764Google Scholar
  100. Tamaki H, Nakamura H, Nishio A et al (2006) Human thioredoxin-1 ameliorates experimental murine colitis in association with suppressed macrophage inhibitory factor production. Gastroenterology 131:1110–1121 doi: 10.1053/j.gastro.2006.08.023 PubMedGoogle Scholar
  101. Thériault JR, Adachi H, Calderwood SK (2006) Role of scavenger receptors in the binding and internalization of heat shock protein 70. J Immunol 177:8604–8611PubMedGoogle Scholar
  102. Tiemessen MM, Jagger AL, Evans HG, van Herwijnen MJ, John S, Taams LS (2007) CD4+CD25+Foxp3+regulatory T cells induce alternative activation of human monocytes/macrophages. Proc Natl Acad Sci U S A 104:19446–19451 doi: 10.1073/pnas.0706832104 PubMedGoogle Scholar
  103. Vabulas RM et al (2002) HSP70 as endogenous stimulus of the Toll/interleukin-1 receptor signal pathway. J Biol Chem 277:15107–15112PubMedGoogle Scholar
  104. Vabulas RM, Ahmad-Nejad P, Ghose S, Kirschning CJ, Issels RD, Wagner H (2002a) Hsp70 as endogenous stimulus of the Toll/interleukin-1 receptor signal pathway. J Biol Chem 277:15107–15112 doi: 10.1074/jbc.M111204200 PubMedGoogle Scholar
  105. Vabulas RM, Braedel S, Hilf N et al (2002b) The endoplasmic reticulum-resident heat shock protein Gp96 activates dendritic cells via the Toll-like receptor 2/4 pathway. J Biol Chem 277:20847–20853 doi: 10.1074/jbc.M200425200 PubMedGoogle Scholar
  106. Vanags D, Williams B, Johnson B, Hall S, Nash P, Taylor A, Weiss J, Feeney D (2006) Therapeutic efficacy and safety of chaperonin 10 in patients with rheumatoid arthritis: a double-blind randomised trial. Lancet 368:855–863 doi: 10.1016/S0140-6736(06)69210-6 PubMedGoogle Scholar
  107. Walsh A, Whelan D, Bielanowicz A, Skinner B, Aitken RJ, O’Bryan MK, Nixon B (2008) Identification of the molecular chaperone, heat shock protein 1 (chaperonin 10), in the reproductive tract and in capacitating spermatozoa in the male mouse. Biol Reprod 78:983–993 doi: 10.1095/biolreprod.107.066860 PubMedGoogle Scholar
  108. Wang Y, Kelly CG, Karttunen JT et al (2001) CD40 is a cellular receptor mediating mycobacterial heat shock protein 70 stimulation of CC-chemokines. Immunity 15:971–983 doi: 10.1016/S1074-7613(01)00242-4 PubMedGoogle Scholar
  109. Wang Y, Kelly CG, Singh M, McGowan EG, Carrara A-S, Bergmeier LA, Lehner T (2002) Stimulation of Th1-polarizing cytokines, C-C chemokines, maturation of dendritic cells, and adjuvant function by the peptide binding fragment of heat shock protein 70. J Immunol 169:2422–2429PubMedGoogle Scholar
  110. Wang Y, Whittall T, McGowan E, Younson J, Kelly C, Bergmeier LA, Singh M, Lehner T (2005) Identification of stimulating and inhibitory epitopes within the heat shock protein 70 molecule that modulate cytokine production and maturation of dendritic cells. J Immunol 174:3306–3316PubMedGoogle Scholar
  111. Whittall T, Wang Y, Younson J, Kelly C, Bergmeier L, Peters B, Singh M, Lehner T (2006) Interaction between the CCR5 chemokine receptors and microbial HSP70. Eur J Immunol 36:2304–2314 doi: 10.1002/eji.200635953 PubMedGoogle Scholar
  112. Williams JH, Ireland HE (2008) Sensing danger—Hsp72 and HMGB1 as candidate signals. J Leukoc Biol 83:489–492 doi: 10.1189/jlb.0607356 PubMedGoogle Scholar
  113. Wilsher ML, Hagan C, Prestidge R, Wells AU, Murison G (1999) Human in vitro immune responses to Mycobacterium tuberculosis. Tuber Lung Dis 79:371–377 doi: 10.1054/tuld.1999.0223 PubMedGoogle Scholar
  114. Wilson MR, Easterbrook-Smith SB (2000) Clusterin is a secreted mammalian chaperone. TIBS 25:95–98 doi: 10.1016/S0968-0004(99)01534-0 PubMedGoogle Scholar
  115. Winrow VR, Mesher J, Meghji S, Morris CJ, Fox S, Coates ARM, Tormay P, Blake D, Henderson B (2008) The two homologous chaperonin 60 proteins of Mycobacterium tuberculosis have distinct effects on monocyte differentiation into osteoclasts. Cell Microbiol 10:2091–2104 doi: 10.1111/j.1462-5822.2008.01193.x PubMedGoogle Scholar
  116. Xie Z, Harris-White ME, Wals PA, Frautschy SA, Finch CE, Morgan TE (2005) Apolipoprotein J (clusterin) activates rodent microglia in vitro and in vivo. J Neurochem 93:1038–1046 doi: 10.1111/j.1471-4159.2005.03065.x PubMedGoogle Scholar
  117. Yagi M, Ninomiya K, Fujita N et al (2007) Induction of DC-STAMP by alternative activation and downstream signalling mechanisms. J Bone Miner Res 22:992–1001 doi: 10.1359/jbmr.070401 PubMedGoogle Scholar
  118. Yamawaki H, Berk BC (2005) Thioredoxin: a multifunctional antioxidant enzyme in kidney, heart and vessels. Curr Opin Nephrol Hypertens 14:149–153 doi: 10.1097/00041552-200503000-00010 PubMedCrossRefGoogle Scholar
  119. Yang CS, Lee DS, Song CH et al (2007a) Roles of peroxiredoxin II in the regulation of proinflammatory responses to LPS and protection against endotoxin-induced lethal shock. J Exp Med 204:583–594 doi: 10.1084/jem.20061849 PubMedGoogle Scholar
  120. Yang Y, Liu B, Dai J, Srivastava PK, Zammit DJ, Lefrançois L, Li Z (2007b) Heat shock protein gp96 is a master chaperone for toll-like receptors and is important in the innate function of macrophages. Immunity 26:215–226 doi: 10.1016/j.immuni.2006.12.005 PubMedGoogle Scholar
  121. Yerbury JJ, Rybchyn MS, Easterbrook-Smith SB, Henriques C, Wilson MR (2005) The acute phase protein haptoglobin is a mammalian extracellular chaperone with an action similar to clusterin. Biochemistry 44:10914–10925 doi: 10.1021/bi050764x PubMedGoogle Scholar
  122. Yoshida N, Oeda K, Watanabe E, Mikami T, Fukita Y, Nishimura K, Komai K, Matsuda K (2001) Chaperonin turned insect toxin. Nature 411:44 doi: 10.1038/35075148 PubMedGoogle Scholar
  123. Youn J, Borghesi LA, Olson EA, Lynes MA (1995) Immunomodulatory activities of extracellular metallothionein. II. Effects on macrophage functions. Toxicol Env Health 45:397–413CrossRefGoogle Scholar
  124. Young DB, Perkins MD, Duncan K, Barry CR (2008) Confronting the scientific obstacles to global control of tuberculosis. J Clin Invest 118:1255–1265 doi: 10.1172/JCI34614 PubMedGoogle Scholar
  125. Yurchenko V, Zybarth G, O’Connor M et al (2002) Active site residues of cyclophilin A are crucial for its signalling activity via CD147. J Biol Chem 277:2259–22965 doi: 10.1074/jbc.M201593200 Google Scholar

Copyright information

© Cell Stress Society International 2008

Authors and Affiliations

  1. 1.Division of Microbial Diseases, UCL Eastman Dental InstituteUniversity College LondonLondonUK
  2. 2.Department of BiochemistryUniversity of OxfordOxfordUK

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