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Discovery of the Extracellular Agonist Actions of Molecular Chaperones and Protein-Folding Catalysts

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Cellular Trafficking of Cell Stress Proteins in Health and Disease

Part of the book series: Heat Shock Proteins ((HESP,volume 6))

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Abstract

Surprisingly, the history of the agonist actions of extracellular molecular chaperones can be traced back to the 1970s, with the cytokine macrophage migration inhibitory factor (MIF) and chaperonin (Hsp)10. The next cell stress protein to be identified as a molecular chaperone was the peptidylprolyl isomerase, cyclophilin A, in 1992. It is only later in the 1990s that the major signalling cell stress proteins—chaperonin (Hsp)60 and Hsp70 are found to have agonist activities. There are still ongoing discoveries of stress proteins with agonist actions and the latest such proteins are a new group of molecular chaperones—the extracellular/circulating molecular chaperones which include clusterin and α-acid1-glycoprotein.

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References

  • Al-Abed Y, Van Patten S (2011) MIF as a disease target: ISO-1 as a proof-of-concept therapeutic. Future Med Chem 3:45–63

    Article  PubMed  CAS  Google Scholar 

  • Asea A, Kraeft SK, Kurt-Jones EA, Stevenson MA, Chen LB, Finberg RW, Koo GC, Calderwood SK (2000) HSP70 stimulates cytokine production through a CD14-dependant pathway, demonstrating its dual role as a chaperone and cytokine. Nat Med 6:435–442

    Article  PubMed  CAS  Google Scholar 

  • 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 277:15028–1534

    Article  PubMed  CAS  Google Scholar 

  • Atanassov C, Pezennec L, d’Alayer J, Grollier G, Picard B, Fauchère JL (2002) Novel antigens of Helicobacter pylori correspond to ulcer-related antibody pattern of sera from infected patients. J Clin Microbiol 40:547–552

    Article  PubMed  CAS  Google Scholar 

  • Banerjee S, Lin CF, Skinner KA, Schiffhauer LM, Peacock J, Hicks DG, Redmond EM, Morrow D, Huston A, Shayne M, Langstein HN, Miller-Graziano CL, Strickland J, O’Donoghue L, De AK (2011) Heat shock protein 27 differentiates tolerogenic macrophages that may support human breast cancer progression. Cancer Res 71:318–327

    Article  PubMed  CAS  Google Scholar 

  • Bartfeld H, Atoynatan T (1971) Activity and properties of macrophage migration inhibitory factor produced by mixed lymphocyte cultures. Nat New Biol 230:246–247

    Article  PubMed  CAS  Google Scholar 

  • Basak C, Pathak SK, Bhattacharyya A, Pathak S, Basu J, Kundu M (2005) The secreted peptidyl prolyl cis, trans-isomerase HP0175 of Helicobacter pylori induces apoptosis of gastric epithelial cells in a TLR4- and apoptosis signal-regulating kinase 1-dependent manner. J Immunol 174:5672–5680

    PubMed  CAS  Google Scholar 

  • Becker T, Hartl FU, Wieland F (2002) CD40, an extracellular receptor for binding and uptake of Hsp70-peptide complexes. J Cell Biol 158:1277–1285

    Article  PubMed  CAS  Google Scholar 

  • Billich A, Winkler G, Aschauer H, Rot A, Peichl P (1997) Presence of cyclophilin A in synovial fluids of patients with rheumatoid arthritis. J Exp Med 185:975–980

    Article  PubMed  CAS  Google Scholar 

  • Broadley SA, Vanags D, Williams B, Johnson B, Feeney D, Griffiths L, Shakib S, Brown G, Coulthard A, Mullins P, Kneebone C (2009) Results of a phase IIa clinical trial of an anti-inflammatory molecule, chaperonin 10, in multiple sclerosis. Mult Scler 15:329–336

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Chang JW, Lee SH, Lu Y, Yoo YJ (2006) Transforming growth factor-beta1 induces the non-classical secretion of peroxiredoxin-I in A549 cells. Biochem Biophys Res Commun 345:118–123

    Article  PubMed  CAS  Google Scholar 

  • Chen B, Guan D, Cui ZJ, Wang X, Shen X (2010) Thioredoxin 1 downregulates MCP-1 secretion and expression in human endothelial cells by suppressing nuclear translocation of activator protein 1 and redox factor-1. Am J Physiol Cell Physiol 298:C1170–C1179

    Article  PubMed  CAS  Google Scholar 

  • Cheng CF, Fan J, Fedesco M, Guan S, Li Y, Bandyopadhyay B, Bright AM, Yerushalmi D, Liang M, Chen M, Han YP, Woodley DT, Li W (2008) Transforming growth factor alpha (TGFalpha)-stimulated secretion of HSP90 alpha: using the receptor LRP-1/CD91 to promote human skin cell migration against a TGFbeta-rich environment during wound healing. Mol Cell Biol 28:3344–3358

    Article  PubMed  CAS  Google Scholar 

  • Chen W, Syldath U, Bellmann K, Burkart V, Kolb H (1999) Human 60-kDa heat-shock protein: a danger signal to the innate immune system. J Immunol 162:3212–3219

    PubMed  CAS  Google Scholar 

  • Cherepkova OA, Lyutova EM, Eronina TB, Gurvits BY (2006) Accelerated protein aggregation induced by macrophage migration inhibitory factor under heat stress conditions. Biochemistry (Mosc) 71:140–145

    Article  CAS  Google Scholar 

  • Clarke FM, Morton H, Clunie GJ (1978) Detection and separation of two serum factors responsible for depression of lymphocyte activity in pregnancy. Clin Exp Immunol 32:318–323

    PubMed  CAS  Google Scholar 

  • 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 165:3951–3958

    PubMed  CAS  Google Scholar 

  • Dear JW, Simpson K, Nicolai MP, Catterson JH, Street J, Huizinga T, Craig D, Dhaliwal K, Webb S, Bateman DN, Webb DJ (2011) Cyclophilin A Is a damage-associated molecular pattern molecule that mediates acetaminophen-induced liver injury. J Immunol 187:3347–3352

    Article  PubMed  CAS  Google Scholar 

  • Dobocan MC, Sadvakassova G, Congote LF (2009) Chaperonin 10 as an endothelial-derived differentiation factor: role of glycogen synthase kinase-3. J Cell Physiol 219:470–476

    Article  PubMed  CAS  Google Scholar 

  • Engleberg NC, Carter C, Weber DR, Cianciotto NP, Eisenstein BI (1989) DNA sequence of mip, a Legionella pneumophila gene associated with macrophage infectivity. Infect Immun 57:1263–1270

    PubMed  CAS  Google Scholar 

  • Evdonin A, Kinev A, Tsupkina N, Guerriero V, Raynes DA, Medvedeva N (2009) Extracellular HspBP1 and Hsp72 synergistically activate epidermal growth factor receptor. Biol Cell 101:351–360

    Article  PubMed  CAS  Google Scholar 

  • Fischer G, Bang H, Ludwig B, Mann K, Hacker J (1992) Mip protein of Legionella pneumophila exhibits peptidyl-prolyl-cis/trans isomerase (PPlase) activity. Mol Microbiol 6:1375–1383

    Article  PubMed  CAS  Google Scholar 

  • Floto RA, MacAry PA, Boname JM, Mien TS, Kampmann B, Hair JR, Huey OS, Houben EN, Pieters J, Day C, Oehlmann W, Singh M, Smith KG, Lehner PJ (2006) Dendritic cell stimulation by mycobacterial Hsp70 is mediated through CCR5. Science 314:454–458

    Article  PubMed  CAS  Google Scholar 

  • Friedland JS, Shattock R, Remick DG, Griffin GE (1993) Mycobacterial 65-kD heat shock protein induces release of proinflammatory cytokines from human monocytic cells. Clin Exp Immunol 91:58–62

    Article  PubMed  CAS  Google Scholar 

  • Gangalum RK, Atanasov IC, Zhou ZH, Bhat SP (2010) AlphaB-crystallin is found in detergent-resistant membrane microdomains and is secreted via exosomes from human retinal pigment epithelial cells. J Biol Chem 286:3261–32699

    Article  PubMed  Google Scholar 

  • Gordon S, Martinez FO (2010) Alternative activation of macrophages: mechanism and functions. Immunity 32:593–604

    Article  PubMed  CAS  Google Scholar 

  • Göthel SF, Marahiel MA (1999) Peptidyl-prolyl cis-trans isomerases, a superfamily of ubiquitous folding catalysts. Cell Mol Life Sci 55:423–436

    Article  PubMed  Google Scholar 

  • Gupta S, Knowlton AA (2007) HSP60 trafficking in adult cardiac myocytes: role of the exosomal pathway. Am J Physiol Heart Circ Physiol 292:H3052–3056

    Article  PubMed  CAS  Google Scholar 

  • Hageman J, van Waarde MA, Zylicz A, Walerych D, Kampinga HH (2011) The diverse members of the mammalian HSP70 machine show distinct chaperone-like activities. Biochem J 435:127–142

    Article  PubMed  CAS  Google Scholar 

  • Heine SJ, Olive D, Gao JL, Murphy PM, Bukrinsky MI, Constant SL (2011) Cyclophilin A cooperates with MIP-2 to augment neutrophil migration. J Inflamm Res 4:93–104

    PubMed  CAS  Google Scholar 

  • Henderson B, Pockley AG (2010) Molecular chaperones and protein-folding catalysts as intercellular signaling regulators in immunity and inflammation. J Leukoc Biol 88:445–462

    Article  PubMed  CAS  Google Scholar 

  • Henderson B, Martin A (2011) Bacterial virulence in the moonlight: multitasking bacterial moonlighting proteins are virulence determinants in infectious disease. Infect Immun 79:3476–3491

    Article  PubMed  CAS  Google Scholar 

  • Henderson B, Calderwood SK, Coates AR, Cohen I, van Eden W, Lehner T, Pockley AG (2010) Caught with their PAMPs down? The extracellular signalling actions of molecular chaperones are not due to microbial contaminants. Cell Stress Chaperones 15:123–141

    Article  PubMed  CAS  Google Scholar 

  • Hickey TB, Thorson LM, Speert DP, Daffé M, Stokes RW (2009) Mycobacterium tuberculosis Cpn60.2 and DnaK are located on the bacterial surface, where Cpn60.2 facilitates efficient bacterial association with macrophages. Infect Immun 77:3389–3401

    Article  PubMed  CAS  Google Scholar 

  • Hickey TB, Ziltener HJ, Speert DP, Stokes RW (2010) Mycobacterium tuberculosis employs Cpn60.2 as an adhesin that binds CD43 on the macrophage surface. Cell Microbiol 12:1634–1647

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Holland IB (2010) The extraordinary diversity of bacterial protein secretion mechanisms. Methods Mol Biol 619:1–20

    Article  PubMed  CAS  Google Scholar 

  • Holmgren A, Lu J (2010) Thioredoxin and thioredoxin reductase: current research with special reference to human disease. Biochem Biophys Res Commun 396:120–124

    Article  PubMed  CAS  Google Scholar 

  • Jeffery CJ (1999) Moonlighting proteins. Trends Biochem Sci 24:8–11

    Article  PubMed  CAS  Google Scholar 

  • Jha R, Vardhan H, Bas S, Salhan S, Mittal A (2011) Chlamydia trachomatis heat shock proteins 60 and 10 induce apoptosis in endocervical epithelial cells. Inflamm Res 60:69–78

    Article  PubMed  CAS  Google Scholar 

  • Kleemann R, Kapurniotu A, Frank RW, Gessner A, Mischke R, Flieger O, Jüttner S, Brunner H, Bernhagen J (1998) Disulfide analysis reveals a role for macrophage migration inhibitory factor (MIF) as thiol-protein oxidoreductase. J Mol Biol 280:85–102

    Article  PubMed  CAS  Google Scholar 

  • Lancaster GI, Febbraio MA (2005) Exosome-dependent trafficking of HSP70: a novel secretory pathway for cellular stress proteins. J Biol Chem 280:23349–2355

    Article  PubMed  CAS  Google Scholar 

  • Laskey RA, Honda BM, Mills AD, Finch JT (1978) Nucleosomes are assembled by an acidic protein which binds histones and transfers them to DNA. Nature 275:416–420

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Lundemose AG, Kay JE, Pearce JH (1993) Chlamydia trachomatis Mip-like protein has peptidyl-prolyl cis/trans isomerase activity that is inhibited by FK506 and rapamycin and is implicated in initiation of chlamydial infection. Mol Microbiol 7:777–783

    Article  PubMed  CAS  Google Scholar 

  • Mambula SS, Calderwood SK (2006) Heat shock protein 70 is secreted from tumor cells by a nonclassical pathway involving lysosomal endosomes. J Immunol 177:7849–7857

    PubMed  CAS  Google Scholar 

  • Morton H, Rolfe B, Clunie GJ (1977) An early pregnancy factor detected in human serum by the rosette inhibition test. Lancet 1:394–397

    Article  PubMed  CAS  Google Scholar 

  • Mougiakakos D, Johansson CC, Jitschin R, Böttcher M, Kiessling R (2011) Increased thioredoxin-1 production in human naturally occurring regulatory T cells confers enhanced tolerance to oxidative stress. Blood 117:857–861

    Article  PubMed  CAS  Google Scholar 

  • Mukhtar RA, Nseyo O, Campbell MJ, Esserman LJ (2011) Tumor-associated macrophages in breast cancer as potential biomarkers for new treatments and diagnostics. Expert Rev Mol Diagn 11:91–100

    Article  PubMed  CAS  Google Scholar 

  • Nakamura H (2008) Extracellular functions of thioredoxin. Novartis Found Symp 291:184–192

    Article  PubMed  CAS  Google Scholar 

  • Nakamura H, De Rosa SC, Yodoi J, Holmgren A, Ghezzi P, Herzenberg LA, Herzenberg LA (2001) Chronic elevation of plasma thioredoxin: inhibition of chemotaxis and curtailment of life expectancy in AIDS. Proc Natl Acad Sci U S A 98:2688–26893

    Article  PubMed  CAS  Google Scholar 

  • Nickel W, Rabouille C (2009) Mechanisms of regulated unconventional protein secretion. Nat Rev Mol Cell Biol 10:148–155

    Article  PubMed  CAS  Google Scholar 

  • Noelle RJ, Lawrence DA (1981) Modulation of T-cell function. II. Chemical basis for the involvement of cell surface thiol-reactive sites in control of T-cell proliferation. Cell Immunol 60:453–469

    Article  PubMed  CAS  Google Scholar 

  • Noonan FP, Halliday WJ, Morton H, Clunie GJ (1979) Early pregnancy factor is immunosuppressive. Nature 278:649–651

    Article  PubMed  CAS  Google Scholar 

  • Norville IH, Harmer NJ, Harding SV, Fischer G, Keith KE, Brown KA, Sarkar-Tyson M, Titball RW (2011) A Burkholderia pseudomallei Mip-like protein has rapamycin inhibitable peptidyl-prolyl isomerase activity and has pleiotropic effects on virulence. Infect Immun 79:4299–4307

    Article  PubMed  CAS  Google Scholar 

  • Pathak SK, Basu S, Bhattacharyya A, Pathak S, Banerjee A, Basu J, Kundu M (2006) TLR4-dependent NF-kappaB activation and mitogen- and stress-activated protein kinase 1-triggered phosphorylation events are central to Helicobacter pylori peptidyl prolyl cis-, trans-isomerase (HP0175)-mediated induction of IL-6 release from macrophages. J Immunol 177:7950–7958

    PubMed  CAS  Google Scholar 

  • Peetermans WE, Raats CJ, Langermans JA, van Furth R (1994) Mycobacterial heat-shock protein 65 induces proinflammatory cytokines but does not activate human mononuclear phagocytes. Scand J Immunol 39:613–617

    Article  PubMed  CAS  Google Scholar 

  • Potolicchio I, Santambrogio L, Strominger JL (2003) Molecular interaction and enzymatic activity of macrophage migration inhibitory factor with immunorelevant peptides. J Biol Chem 278:30889–30895

    Article  PubMed  CAS  Google Scholar 

  • Ragno S, Winrow VR, Mascagni P, Lucietto P, Di Pierro F, Morris CJ, Blake DR (1996) A synthetic 10-kD heat shock protein (hsp10) from Mycobacterium tuberculosis modulates adjuvant arthritis. Clin Exp Immunol 103:384–390

    Article  PubMed  CAS  Google Scholar 

  • Randhawa AK, Ziltener HJ, Stokes RW (2008) CD43 controls the intracellular growth of Mycobacterium tuberculosis through the induction of TNF-alpha-mediated apoptosis. Cell Microbiol 10:2105–2117

    Article  PubMed  CAS  Google Scholar 

  • Ritossa F (1962) A new puffing pattern induced by temperature shock and DNP in drosophila. Cell Mol Life Sci 18:571–573

    Article  CAS  Google Scholar 

  • Rohde K, Yates RM, Purdy GE, Russell DG (2007) Mycobacterium tuberculosis and the environment within the phagosome. Immunol Rev 219:37–54

    Article  PubMed  CAS  Google Scholar 

  • Rubartelli A, Cozzolino F, Talio M, Sitia R (1990) A novel secretory pathway for interleukin-1 beta, a protein lacking a signal sequence. EMBO J 9:1503–1510

    PubMed  CAS  Google Scholar 

  • Rubartelli A, Bajetto A, Allavena G, Wollman E, Sitia R (1992) Secretion of thioredoxin by normal and neoplastic cells through a leaderless secretory pathway. J Biol Chem 267:24161–24164

    PubMed  CAS  Google Scholar 

  • Shachar I, Haran M (2011) The secret second life of an innocent chaperone: the story of CD74 and B cell/chronic lymphocytic leukemia cell survival. Leuk Lymphoma 52:1446–1454

    Article  PubMed  CAS  Google Scholar 

  • Schiene-Fischer C, Aumüller T, Fischer G (2011) Peptide bond cis/trans Isomerases: a biocatalysis perspective of conformational dynamics in proteins. Top Curr Chem [Epub ahead of print]

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Song F, Zhang X, Ren XB, Zhu P, Xu J, Wang L, Li YF, Zhong N, Ru Q, Zhang DW, Jiang JL, Xia B, Chen ZN (2011) Cyclophilin A (CyPA) induces chemotaxis independent of its peptidylprolyl cis-trans isomerase activity: direct binding between CyPA and the ectodomain of CD147. J Biol Chem 286:8197–8203

    Article  PubMed  CAS  Google Scholar 

  • Suzuki J, Jin Z-G, Meoli DF, Matoba T, Berk BC (2006) Cyclophilin A is secreted by a vesicular pathway in vascular smooth muscle cells. Circ Res 98:811–817

    Article  PubMed  CAS  Google Scholar 

  • Tagaya Y, Maeda Y, Mitsui A, Kondo N, Matsui H, Hamuro J, Brown N, Arai K, Yokota T, Wakasugi H et al (1989) 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 8:757–764

    PubMed  CAS  Google Scholar 

  • Tassi S, Carta S, Vené R, Delfino L, Ciriolo MR, Rubartelli A (2009) Pathogen-induced interleukin-1beta processing and secretion is regulated by a biphasic redox response. J Immunol 183:1456–1462

    Article  PubMed  CAS  Google Scholar 

  • Tegeder I, Schumacher A, John S, Geiger H, Geisslinger G, Bang H, Brune K (1997) Elevated serum cyclophilin levels in patients with severe sepsis. J Clin Immunol 17:380–386

    Article  PubMed  CAS  Google Scholar 

  • Thériault JR, Mambula SS, Sawamura T, Stevenson MA, Calderwood SK (2005) Extracellular HSP70 binding to surface receptors present on antigen presenting cells and endothelial/epithelial cells. FEBS Lett 579:1951–1960

    Article  PubMed  Google Scholar 

  • Thériault JR, Adachi H, Calderwood SK (2006) Role of scavenger receptors in the binding and internalization of heat shock protein 70. J Immunol 177:8604–8611

    PubMed  Google Scholar 

  • Tsan MF, Gao B (2009) Heat shock proteins and immune system. J Leukoc Biol 85:905–910

    Article  PubMed  CAS  Google Scholar 

  • Tytell M, Greenberg SG, Lasek RJ (1986) Heat shock-like protein is transferred from glia to axon. Brain Res 363:61–64

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Verdegaal EME, Zegveld ST, van Furth R (1996) Heat shock protein 65 induces CD62e, CD106 and CD54 on cultured human endothelial cells and increases their adhesiveness for monocytes and granulocytes. J Immunol 157:369–376

    PubMed  CAS  Google Scholar 

  • Wakasugi N, Tagaya Y, Wakasugi H, Mitsui A, Maeda M, Yodoi J, Tursz T (1990) Adult T-cell leukemia-derived factor/thioredoxin, produced by both human T-lymphotropic virus type I- and Epstein-Barr virus-transformed lymphocytes, acts as an autocrine growth factor and synergizes with interleukin 1 and interleukin 2. Proc Natl Acad Sci U S A 87:8282–8286

    Article  PubMed  CAS  Google Scholar 

  • Wang Y, Kelly CG, Karttunen JT, Whittall T, Lehner PJ, Duncan L, MacAry P, Younson JS, Singh M, Oehlmann W, Cheng G, Bergmeier L, Lehner T (2001) CD40 is a cellular receptor mediating mycobacterial heat shock protein 70 stimulation of CC-chemokines. Immunity 15:971–983

    Article  PubMed  CAS  Google Scholar 

  • Wang Y, Kelly CG, Singh M, McGowan EG, Carrara AS, 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 169:2422–2429

    PubMed  CAS  Google Scholar 

  • Xiao G, Chung TF, Pyun HY, Fine RE, Johnson RJ (1999) KDEL proteins are found on the surface of NG108-15 cells. Brain Res Mol Brain Res 72:121–128

    Article  PubMed  CAS  Google Scholar 

  • Yurchenko V, O’Connor M, Dai WW, Guo H, Toole B, Sherry B, Bukrinsky M (2001) CD147 is a signaling receptor for cyclophilin B. Biochem Biophys Res Commun 288:786–788

    Article  PubMed  CAS  Google Scholar 

  • Yurchenko V, Constant S, Eisenmesser E, Bukrinsky M (2010) Cyclophilin-CD147 interactions: a new target for anti-inflammatory therapeutics. Clin Exp Immunol 160:305–317

    Article  PubMed  CAS  Google Scholar 

  • Zhan R, Leng X, Liu X, Wang X, Gong J, Yan L, Wang L, Wang Y, Wang X, Qian LJ (2009) Heat shock protein 70 is secreted from endothelial cells by a non-classical pathway involving exosomes. Biochem Biophys Res Commun 387:229–233

    Article  PubMed  CAS  Google Scholar 

  • Zhang B, Walsh MD, Nguyen KB, Hillyard NC, Cavanagh AC, McCombe PA, Morton H (2003) 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 212:37–46

    Article  PubMed  CAS  Google Scholar 

  • Zhou Z, Wu Y, Chen L, Liu L, Chen H, Li Z, Chen C (2011) Heat shock protein 10 of Chlamydophila pneumoniae induces proinflammatory cytokines through Toll-like receptor (TLR) 2 and TLR4 in human monocytes THP-1. In Vitro Cell Dev Biol Anim 47:541–549

    Google Scholar 

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  1. Department of Microbial Diseases, UCL-Eastman Dental Institute, University College London, 256 Gray’s Inn Road, WC1X 8LD, London, UK

    Prof. Brian Henderson

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  1. Eastman Dental Institute, Div. Microbial Diseases, University College, London, Gray's Inn Road 256, London, WC1X 8LD, United Kingdom

    Brian Henderson

  2. School of Medicine & Biomedical Science, University of Sheffield, Beech Hill Road, Sheffield, S10 2RX, United Kingdom

    A. Graham Pockley

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Henderson, B. (2012). Discovery of the Extracellular Agonist Actions of Molecular Chaperones and Protein-Folding Catalysts. In: Henderson, B., Pockley, A. (eds) Cellular Trafficking of Cell Stress Proteins in Health and Disease. Heat Shock Proteins, vol 6. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-4740-1_2

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