Extracellular Hsp70 inhibits pro-inflammatory cytokine production by IL-10 driven down-regulation of C/EBPβ and C/EBPδ

References

• Fleshner M, Johnson JD. Endogenous extra-cellular heat shock protein 72: Releasing signal(s) and function. Int J Hyperthermia 2005;21:457–71
   PubMed Web of Science ®Google Scholar
• Borges TJ, Wieten L, van Herwijnen MJ, Broere F, van der Zee R, Bonorino C, et al. The anti-inflammatory mechanisms of Hsp70. Front Immunol 2012;3:95
   PubMed Web of Science ®Google Scholar
• Tanaka S, Kimura Y, Mitani A, Yamamoto G, Nishimura H, Spallek R, et al. Activation of T cells recognizing an epitope of heat-shock protein 70 can protect against rat adjuvant arthritis. J Immunol 1999;163:5560–5
   PubMed Web of Science ®Google Scholar
• Wendling U, Paul L, van der Zee R, Prakken B, Singh M, van Eden W. A conserved mycobacterial heat shock protein (HSP) 70 sequence prevents adjuvant arthritis upon nasal administration and induces IL-10-producing T cells that cross-react with the mammalian self-Hsp70 homologue. J Immunol 2000;164:2711–17
   PubMed Web of Science ®Google Scholar
• van Eden W, van der Zee R, Prakken B. Heat-shock proteins induce T-cell regulation of chronic inflammation. Nat Rev Immunol 2005;5:318–30
   PubMed Web of Science ®Google Scholar
• Broere F, Wieten L, Klein Koerkamp EI, van Roon JA, Guichelaar T, Lafeber FP, et al. Oral or nasal antigen induces regulatory T cells that suppress arthritis and proliferation of arthritogenic T cells in joint draining lymph nodes. J Immunol 2008;181:899–906
   PubMed Web of Science ®Google Scholar
• Wieten L, Berlo SE, Ten Brink CB, van Kooten PJ, Singh M, van der Zee R, et al. IL-10 is critically involved in mycobacterial Hsp70 induced suppression of proteoglycan-induced arthritis. PLoS One 2009;4:e4186
   PubMed Web of Science ®Google Scholar
• Borges TJ, Porto BN, Teixeira CA, Rodrigues M, Machado FD, Ornaghi AP, et al. Prolonged survival of allografts induced by mycobacterial Hsp70 is dependent on CD4+CD25+ regulatory T cells. PLoS One 2010;5:e14264
   PubMed Web of Science ®Google Scholar
• Tanaka K, Namba T, Arai Y, Fujimoto M, Adachi H, Sobue G, et al. Genetic evidence for a protective role for heat shock factor 1 and heat shock protein 70 against colitis. J Biol Chem 2007;282:23240–52
   PubMed Web of Science ®Google Scholar
• Detanico T, Rodrigues L, Sabritto AC, Keisermann M, Bauer ME, Zwickey H, et al. Mycobacterial heat shock protein 70 induces interleukin-10 production: Immunomodulation of synovial cell cytokine profile and dendritic cell maturation. Clin Exp Immunol 2004;135:336–42
   PubMed Web of Science ®Google Scholar
• Watowich SS, Liu YJ. Mechanisms regulating dendritic cell specification and development. Immunol Rev 2010;238:76–92
   PubMed Web of Science ®Google Scholar
• Heath WR, Carbone FR. Dendritic cell subsets in primary and secondary T cell responses at body surfaces. Nat Immunol 2009;10:1237–44
   PubMed Web of Science ®Google Scholar
• Shortman K, Liu YJ. Mouse and human dendritic cell subtypes. Nat Rev Immunol 2002;2:151–61
   PubMed Web of Science ®Google Scholar
• Liu K, Nussenzweig MC. Origin and development of dendritic cells. Immunol Rev 2010;234:45–54
   PubMed Web of Science ®Google Scholar
• Sarkar S, Fox DA. Dendritic cells in rheumatoid arthritis. Front Biosci 2005;10:656–65
   PubMed Web of Science ®Google Scholar
• Khan S, Greenberg JD, Bhardwaj N. Dendritic cells as targets for therapy in rheumatoid arthritis. Nat Rev Rheumatol 2009;5:566–71
   PubMed Web of Science ®Google Scholar
• Motta A, Schmitz C, Rodrigues L, Ribeiro F, Teixeira C, Detanico T, et al. Mycobacterium tuberculosis heat-shock protein 70 impairs maturation of dendritic cells from bone marrow precursors, induces interleukin-10 production and inhibits T-cell proliferation in vitro. Immunology 2007;121:462–72
   PubMed Web of Science ®Google Scholar
• Kawai T, Akira S. Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity 2011;34:637–50
   PubMed Web of Science ®Google Scholar
• Baldwin AS Jr.. The NF-kappa B and I kappa B proteins: New discoveries and insights. Annu Rev Immunol 1996;14:649–83
   PubMed Web of Science ®Google Scholar
• Ruland J. Return to homeostasis: Downregulation of NF-kappaB responses. Nat Immunol 2011;12:709–14
   PubMed Web of Science ®Google Scholar
• Shi Y, Tu Z, Tang D, Zhang H, Liu M, Wang K, et al. The inhibition of LPS-induced production of inflammatory cytokines by Hsp70 involves inactivation of the NF-kappaB pathway but not the MAPK pathways. Shock 2006;26:277–84
   PubMed Web of Science ®Google Scholar
• Dokladny K, Lobb R, Wharton W, Ma TY, Moseley PL. LPS-induced cytokine levels are repressed by elevated expression of HSP70 in rats: Possible role of NF-kappaB. Cell Stress Chaperones 2010;15:153–63
   PubMed Web of Science ®Google Scholar
• Malhotra V, Wong HR. Interactions between the heat shock response and the nuclear factor-kappaB signaling pathway. Crit Care Med 2002;30:S89–95
   PubMed Web of Science ®Google Scholar
• Lekstrom-Himes J, Xanthopoulos KG. Biological role of the CCAAT/enhancer-binding protein family of transcription factors. J Biol Chem 1998;273:28545–8
   PubMed Web of Science ®Google Scholar
• Lu YC, Kim I, Lye E, Shen F, Suzuki N, Suzuki S, et al. Differential role for c-Rel and C/EBPbeta/delta in TLR-mediated induction of proinflammatory cytokines. J Immunol 2009;182:7212–21
   PubMed Web of Science ®Google Scholar
• Poli V. The role of C/EBP isoforms in the control of inflammatory and native immunity functions. J Biol Chem 1998;273:29279–82
   PubMed Web of Science ®Google Scholar
• Hu HM, Baer M, Williams SC, Johnson PF, Schwartz RC. Redundancy of C/EBP-alpha, -beta, and -delta in supporting the lipopolysaccharide-induced transcription of IL-6 and monocyte chemoattractant protein-1. J Immunol 1998;160:2334–42
   PubMed Web of Science ®Google Scholar
• Mehlert A, Young DB. Biochemical and antigenic characterization of the Mycobacterium tuberculosis 71-kD antigen, a member of the 70-kD heat-shock protein family. Mol Microbiol 1989;3:125–30
   PubMed Web of Science ®Google Scholar
• Aida Y, Pabst MJ. Removal of endotoxin from protein solutions by phase-separation using triton X-114. J Immunol Methods 1990;132:191–5
   PubMed Web of Science ®Google Scholar
• Inaba K, Inaba M, Romani N, Aya H, Deguchi M, Ikehara S, et al. Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor. J Exp Med 1992;176:1693–1702
   PubMed Web of Science ®Google Scholar
• Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 2008;3:1101–8
   PubMed Web of Science ®Google Scholar
• Chalmin F, Ladoire S, Mignot G, Vincent J, Bruchard M, Remy-Martin JP, et al. Membrane-associated Hsp72 from tumor-derived exosomes mediates STAT3-dependent immunosuppressive function of mouse and human myeloid-derived suppressor cells. J Clin Invest 2010;120:457–71
   PubMed Web of Science ®Google Scholar
• Dillon S, Agrawal S, Banerjee K, Letterio J, Denning TL, Oswald-Richter K, et al. Yeast zymosan, a stimulus for TLR2 and dectin-1, induces regulatory antigen-presenting cells and immunological tolerance. J Clin Invest 2006;116:916–28
   PubMed Web of Science ®Google Scholar
• Manicassamy S, Ravindran R, Deng J, Oluoch H, Denning TL, Kasturi SP, et al. Toll-like receptor 2-dependent induction of vitamin A-metabolizing enzymes in dendritic cells promotes T regulatory responses and inhibits autoimmunity. Nat Med 2009;15:401–9
   PubMed Web of Science ®Google Scholar
• Filippi CM, Ehrhardt K, Estes EA, Larsson P, Oldham JE, von Herrath MG. TLR2 signaling improves immunoregulation to prevent type 1 diabetes. Eur J Immunol 2011;41:1399–409
   PubMed Web of Science ®Google Scholar
• Saraiva M, O’Garra A. The regulation of IL-10 production by immune cells. Nat Rev Immunol 2010;10:170–81
   PubMed Web of Science ®Google Scholar
• Cheng F, Wang HW, Cuenca A, Huang M, Ghansah T, Brayer J, et al. A critical role for STAT3 signaling in immune tolerance. Immunity 2003;19:425–36
   PubMed Web of Science ®Google Scholar
• Barton BE. STAT3: A potential therapeutic target in dendritic cells for the induction of transplant tolerance. Expert Opin Ther Targets 2006;10:459–70
   PubMed Web of Science ®Google Scholar
• Dhingra S, Bagchi AK, Ludke AL, Sharma AK, Singal PK. Akt regulates IL-10 mediated suppression of TNFalpha-induced cardiomyocyte apoptosis by upregulating STAT3 phosphorylation. PLoS One 2011;6:e25009
   PubMed Web of Science ®Google Scholar
• Kubo M, Motomura Y. Transcriptional regulation of the anti-inflammatory cytokine IL-10 in acquired immune cells. Front Immunol 2012;3:275
   PubMed Web of Science ®Google Scholar
• Banchereau J, Steinman RM. Dendritic cells and the control of immunity. Nature 1998;392:245–52
   PubMed Web of Science ®Google Scholar
• Granucci F, Girolomoni G, Lutz MB, Foti M, Marconi G, Gnocchi P, et al. Modulation of cytokine expression in mouse dendritic cell clones. Eur J Immunol 1994;24:2522–6
   PubMed Web of Science ®Google Scholar
• Amodio G, Gregori S. Dendritic cells a double-edge sword in autoimmune responses. Front Immunol 2012;3:233
   PubMed Web of Science ®Google Scholar
• Hackstein H, Thomson AW. Dendritic cells: Emerging pharmacological targets of immunosuppressive drugs. Nat Rev Immunol 2004;4:24–34
   PubMed Web of Science ®Google Scholar
• Baldwin HM, Ito-Ihara T, Isaacs JD, Hilkens CM. Tumour necrosis factor alpha blockade impairs dendritic cell survival and function in rheumatoid arthritis. Ann Rheum Dis 2010;69:1200–7
   PubMed Web of Science ®Google Scholar
• Spiering R, van der Zee R, Wagenaar J, van Eden W, Broere F. Mycobacterial and mouse Hsp70 have immuno-modulatory effects on dendritic cells. Cell Stress Chaperones 2012
   Google Scholar
• Rossi D, Zlotnik A. The biology of chemokines and their receptors. Annu Rev Immunol 2000;18:217–42
   PubMed Web of Science ®Google Scholar
• Frodermann V, Chau TA, Sayedyahossein S, Toth JM, Heinrichs DE, Madrenas J. A modulatory interleukin-10 response to staphylococcal peptidoglycan prevents Th1/Th17 adaptive immunity to Staphylococcus aureus. J Infect Dis 2011;204:253–62
   PubMed Web of Science ®Google Scholar
• Dearman RJ, Cumberbatch M, Maxwell G, Basketter DA, Kimber I. Toll-like receptor ligand activation of murine bone marrow-derived dendritic cells. Immunology 2009;126:475–84
   PubMed Web of Science ®Google Scholar
• Harding CV, Boom WH. Regulation of antigen presentation by Mycobacterium tuberculosis: A role for toll-like receptors. Nat Rev Microbiol 2010;8:296–307
   PubMed Web of Science ®Google Scholar
• Aderem A, Ulevitch RJ. Toll-like receptors in the induction of the innate immune response. Nature 2000;406:782–7
   PubMed Web of Science ®Google Scholar
• Raymond L, Eck S, Mollmark J, Hays E, Tomek I, Kantor S, et al. Interleukin-1 beta induction of matrix metalloproteinase-1 transcription in chondrocytes requires ERK-dependent activation of CCAAT enhancer-binding protein-beta. J Cell Physiol 2006;207:683–8
   PubMed Web of Science ®Google Scholar
• Zhang T, He YM, Wang JS, Shen J, Xing YY, Xi T. Ursolic acid induces HL60 monocytic differentiation and upregulates C/EBPbeta expression by ERK pathway activation. Anticancer Drugs 2011;22:158–65
   PubMed Web of Science ®Google Scholar
• Niehof M, Streetz K, Rakemann T, Bischoff SC, Manns MP, Horn F, et al. Interleukin-6-induced tethering of STAT3 to the LAP/C/EBPbeta promoter suggests a new mechanism of transcriptional regulation by STAT3. J Biol Chem 2001;276:9016–27
   PubMed Web of Science ®Google Scholar
• Nakahara T, Moroi Y, Uchi H, Furue M. Differential role of MAPK signaling in human dendritic cell maturation and Th1/Th2 engagement. J Dermatol Sci 2006;42:1–11
   PubMed Web of Science ®Google Scholar
• Puig-Kroger A, Relloso M, Fernandez-Capetillo O, Zubiaga A, Silva A, Bernabeu C, et al. Extracellular signal-regulated protein kinase signaling pathway negatively regulates the phenotypic and functional maturation of monocyte-derived human dendritic cells. Blood 2001;98:2175–82
   PubMed Web of Science ®Google Scholar
• Yamada T, Tobita K, Osada S, Nishihara T, Imagawa M. CCAAT/enhancer-binding protein delta gene expression is mediated by APRF/STAT3. J Biochem 1997;121:731–8
   PubMed Web of Science ®Google Scholar
• Tanaka N, Hoshino Y, Gold J, Hoshino S, Martiniuk F, Kurata T, et al. Interleukin-10 induces inhibitory C/EBPbeta through STAT-3 and represses HIV-1 transcription in macrophages. Am J Respir Cell Mol Biol 2005;33:406–11
   PubMed Web of Science ®Google Scholar
• Zhang K, Guo W, Yang Y, Wu J. JAK2/STAT3 pathway is involved in the early stage of adipogenesis through regulating C/EBPbeta transcription. J Cell Biochem 2011;112:488–97
   PubMed Web of Science ®Google Scholar
• Stocki P, Dickinson AM. The immunosuppressive activity of heat shock protein 70. Autoimmune dis 2012;2012:617213
   PubMedGoogle Scholar
• Csoka B, Nemeth ZH, Virag L, Gergely P, Leibovich SJ, Pacher P, et al. A2A adenosine receptors and C/EBPbeta are crucially required for IL-10 production by macrophages exposed to Escherichia coli. Blood 2007;110:2685–95
   PubMed Web of Science ®Google Scholar
• Ruffell D, Mourkioti F, Gambardella A, Kirstetter P, Lopez RG, Rosenthal N, et al. A CREB-C/EBPbeta cascade induces M2 macrophage-specific gene expression and promotes muscle injury repair. Proc Natl Acad Sci USA 2009;106:17475–80
   PubMed Web of Science ®Google Scholar
• Spiering R, van der Zee R, Wagenaar J, Kapetis D, Zolezzi F, van Eden W, et al. Tolerogenic dendritic cells that inhibit autoimmune arthritis can be induced by a combination of carvacrol and thermal stress. PLoS One 2012;7:e46336
   PubMed Web of Science ®Google Scholar
• Ahmed K, Furusawa Y, Tabuchi Y, Emam HF, Piao JL, Hassan MA, et al. Chemical inducers of heat shock proteins derived from medicinal plants and cytoprotective genes response. Int J Hyperthermia 2012;28:1–8
   PubMed Web of Science ®Google Scholar