Tolerogenic Dendritic Cells That Inhibit Autoimmune Arthritis Can Be Induced by a Combination of Carvacrol and Thermal Stress

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  Spiering, Rachel ^a   van der Zee, Ruurd ^a   Wagenaar, Josée ^a   Kapetis, Dimos ^b   Zolezzi, Francesca ^b,c   van Eden, Willem ^a   Broere, Femke ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

^b UNIVERSITY OF MILANO BICOCCA   (Italy)

^c AGENCY FOR SCIENCE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CHEMOKINE; CARVACROL; GAMMA INTERFERON; HEAT SHOCK PROTEIN 70; INTERLEUKIN 10; INTERLEUKIN 1BETA; LEUKEMIA INHIBITORY FACTOR; MESSENGER RNA; METALLOTHIONEIN I; MONOCYTE CHEMOTACTIC PROTEIN 1; MONOCYTE CHEMOTACTIC PROTEIN 3; MONOCYTE CHEMOTACTIC PROTEIN 5; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA;

AMPHIREGULIN GENE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN PRESENTING CELL; ARTHRITIS; ARTICLE; AUTOIMMUNE DISEASE; CD4+ T LYMPHOCYTE; CHEMOKINE LIGAND 12 GENE; CHEMOKINE LIGAND 2 GENE; CHEMOKINE LIGAND 7 GENE; CONTROLLED STUDY; DENDRITE; DRUG EFFICACY; DRUG MECHANISM; FEMALE; GENE; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; IFN GAMMA GENE; IMMUNOPATHOGENESIS; IN VIVO STUDY; INTERLEUKIN 10 GENE; INTERLEUKIN 1BETA GENE; LEUKEMIA INHIBITOR FACTOR GENE; LYMPHOCYTE ACTIVATION; LYMPHOCYTE PROLIFERATION; METALLOTHIONEIN 1 GENE; MOUSE; NONHUMAN; PROTEIN BINDING; QUANTITATIVE ANALYSIS; REGULATORY T LYMPHOCYTE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; T LYMPHOCYTE SUBPOPULATION; TEMPERATURE STRESS; TGF BETA GENE;

ANIMALS; ARTHRITIS, EXPERIMENTAL; AUTOIMMUNE DISEASES; DENDRITIC CELLS; FEMALE; FLOW CYTOMETRY; MICE; MICE, INBRED BALB C; MONOTERPENES; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REAL-TIME POLYMERASE CHAIN REACTION; TEMPERATURE;

EID: 84866684724     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0046336     Document Type: Article

References (41)

1. Thomson AW, Robbins PD, (2008) Tolerogenic dendritic cells for autoimmune disease and transplantation. Ann Rheum Dis 67 (Suppl 3) () 10.1136/ard.2008.099176.
2. Charbonnier LM, van Duivenvoorde LM, Apparailly F, Cantos C, Han WG, et al. (2006) Immature dendritic cells suppress collagen-induced arthritis by in vivo expansion of CD49b+ regulatory T cells. J Immunol 177(6): 3806-3813.
3. van Duivenvoorde LM, Han WG, Bakker AM, Louis-Plence P, Charbonnier LM, et al. (2007) Immunomodulatory dendritic cells inhibit Th1 responses and arthritis via different mechanisms. J Immunol 179(3): 1506-1515.
4. Salazar L, Aravena O, Abello P, Escobar A, Contreras-Levicoy J, et al. (2008) Modulation of established murine collagen-induced arthritis by a single inoculation of short-term lipopolysaccharide-stimulated dendritic cells. Ann Rheum Dis 67(9): 1235-1241 10.1136/ard.2007.072199.
5. Healy LJ, Collins HL, Thompson SJ, (2008) Systemic administration of tolerogenic dendritic cells ameliorates murine inflammatory arthritis. Open Rheumatol J2: 71-80 10.2174/1874312900802010071.
6. Morita Y, Yang J, Gupta R, Shimizu K, Shelden EA, et al. (2001) Dendritic cells genetically engineered to express IL-4 inhibit murine collagen-induced arthritis. J Clin Invest 107(10): 1275-1284 10.1172/JCI11490.
7. Stoop JN, Harry RA, von Delwig A, Isaacs JD, Robinson JH, et al. (2010) Therapeutic effect of tolerogenic dendritic cells in established collagen-induced arthritis is associated with a reduction in Th17 responses. Arthritis Rheum 62(12): 3656-3665. 10.1002/art.27756; 10.1002/art.27756.
8. Wieten L, van der Zee R, Spiering R, Wagenaar-Hilbers J, van Kooten P, et al. (2010) A novel heat-shock protein coinducer boosts stress protein Hsp70 to activate T cell regulation of inflammation in autoimmune arthritis. Arthritis Rheum 62(4): 1026-1035 10.1002/art.27344.
9. Singh IS, He JR, Calderwood S, Hasday JD, (2002) A high affinity HSF-1 binding site in the 5′-untranslated region of the murine tumor necrosis factor-alpha gene is a transcriptional repressor. J Biol Chem 277(7): 4981-4988 10.1074/jbc.M108154200.
10. Singh IS, Viscardi RM, Kalvakolanu I, Calderwood S, Hasday JD, (2000) Inhibition of tumor necrosis factor-alpha transcription in macrophages exposed to febrile range temperature. A possible role for heat shock factor-1 as a negative transcriptional regulator. J Biol Chem 275(13): 9841-9848.
11. Yoo CG, Lee S, Lee CT, Kim YW, Han SK, et al. (2000) Anti-inflammatory effect of heat shock protein induction is related to stabilization of I kappa B alpha through preventing I kappa B kinase activation in respiratory epithelial cells. J Immunol 164(10): 5416-5423.
12. Ostberg JR, Repasky EA, (2006) Emerging evidence indicates that physiologically relevant thermal stress regulates dendritic cell function. Cancer Immunol Immunother 55(3): 292-298 10.1007/s00262-005-0689-y.
13. Xu J, Zhou F, Ji BP, Pei RS, Xu N, (2008) The antibacterial mechanism of carvacrol and thymol against escherichia coli. Lett Appl Microbiol. 47(3): 174-179 10.1111/j.1472-765X.2008.02407.x.
14. Yanishlieva NV, Marinova EM, Gordon MH, Raneva VG, (1999) Antioxidant activity and mechanism of action of thymol and carvacrol in two lipid systems. Food Chem 64(1): 59-66 DOI: 10.1016/S0308-8146(98)00086-7.
15. Hotta M, Nakata R, Katsukawa M, Hori K, Takahashi S, et al. (2010) Carvacrol, a component of thyme oil, activates PPARalpha and gamma and suppresses COX-2 expression. J Lipid Res 51(1): 132-139 10.1194/jlr.M900255-JLR200.
16. Landa P, Kokoska L, Pribylova M, Vanek T, Marsik P, (2009) In vitro anti-inflammatory activity of carvacrol: Inhibitory effect on COX-2 catalyzed prostaglandin E(2) biosynthesis. Arch Pharm Res 32(1): 75-78 10.1007/s12272-009-1120-6.
17. Lutz MB, Kukutsch N, Ogilvie AL, Rossner S, Koch F, et al. (1999) An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow. J Immunol Methods 223(1): 77-92.
18. Wieten L, van der Zee R, Goedemans R, Sijtsma J, Serafini M, et al. (2010) Hsp70 expression and induction as a readout for detection of immune modulatory components in food. Cell Stress Chaperones 15(1): 25-37 10.1007/s12192-009-0119-8.
19. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, et al. (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4(2): 249-264 10.1093/biostatistics/4.2.249.
20. Wu ZJ, Irizarry RA, Gentleman R, Martinez-Murillo F, Spencer F, (2004) A model-based background adjustment for oligonucleotide expression arrays. Journal of the American Statistical Association 99(468): 909-917 10.1198/016214504000000683.
21. Smyth GK, (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: Article310.2202/1544-6115.1027.
22. Benjamini Y, Hochberg Y, (1995) Controlling the false discovery rate- a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B-Methodological 57(1): 289-300.
23. Broere F, Wieten L, Klein Koerkamp EI, van Roon JA, Guichelaar T, et al. (2008) Oral or nasal antigen induces regulatory T cells that suppress arthritis and proliferation of arthritogenic T cells in joint draining lymph nodes. J Immunol 181(2): 899-906.
24. Hanyecz A, Berlo SE, Szanto S, Broeren CP, Mikecz K, et al. (2004) Achievement of a synergistic adjuvant effect on arthritis induction by activation of innate immunity and forcing the immune response toward the Th1 phenotype. Arthritis Rheum 50(5): 1665-1676 10.1002/art.20180.
25. Brennan FM, McInnes IB, (2008) Evidence that cytokines play a role in rheumatoid arthritis. J Clin Invest 118(11): 3537-3545 10.1172/JCI36389.
26. Yamane S, Ishida S, Hanamoto Y, Kumagai K, Masuda R, et al. (2008) Proinflammatory role of amphiregulin, an epidermal growth factor family member whose expression is augmented in rheumatoid arthritis patients. J Inflamm (Lond) 5: 510.1186/1476-9255-5-5.
27. Reus IS, Bando I, Andres D, Cascales M, (2003) Relationship between expression of HSP70 and metallothionein and oxidative stress during mercury chloride induced acute liver injury in rats. J Biochem Mol Toxicol 17(3): 161-168 10.1002/jbt.10074.
28. Motta A, Schmitz C, Rodrigues L, Ribeiro F, Teixeira C, et al. (2007) 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 121(4): 462-472. 10.1111/j.1365-2567.2007.02564.x.
29. Youn J, Hwang SH, Ryoo ZY, Lynes MA, Paik DJ, et al. (2002) Metallothionein suppresses collagen-induced arthritis via induction of TGF-beta and down-regulation of proinflammatory mediators. Clin Exp Immunol 129(2): 232-239.
30. Driesen J, Popov A, Schultze JL, (2008) CD25 as an immune regulatory molecule expressed on myeloid dendritic cells. Immunobiology 213(9-10): 849-858 10.1016/j.imbio.2008.07.026.
31. Torres-Aguilar H, Blank M, Jara LJ, Shoenfeld Y, (2010) Tolerogenic dendritic cells in autoimmune diseases: Crucial players in induction and prevention of autoimmunity. Autoimmun Rev 10(1): 8-17 10.1016/j.autrev.2010.07.015.
32. Stoop JN, Robinson JH, Hilkens CM, (2011) Developing tolerogenic dendritic cell therapy for rheumatoid arthritis: What can we learn from mouse models? Ann Rheum Dis 70(9): 1526-1533 10.1136/ard.2011.151654.
33. Bruhl H, Cihak J, Schneider MA, Plachy J, Rupp T, et al. (2004) Dual role of CCR2 during initiation and progression of collagen-induced arthritis: Evidence for regulatory activity of CCR2+ T cells. J Immunol 172(2): 890-898.
34. Luther SA, Cyster JG, (2001) Chemokines as regulators of T cell differentiation. Nat Immunol 2(2): 102-107 10.1038/84205.
35. deSchoolmeester ML, Little MC, Rollins BJ, Else KJ, (2003) Absence of CC chemokine ligand 2 results in an altered Th1/Th2 cytokine balance and failure to expel trichuris muris infection. J Immunol 170(9): 4693-4700.
36. Bles N, Di Pietrantonio L, Boeynaems JM, Communi D, (2010) ATP confers tumorigenic properties to dendritic cells by inducing amphiregulin secretion. Blood 116(17): 3219-3226 10.1182/blood-2010-01-265611.
37. Detanico T, Rodrigues L, Sabritto AC, Keisermann M, Bauer ME, et al. (2004) Mycobacterial heat shock protein 70 induces interleukin-10 production: Immunomodulation of synovial cell cytokine profile and dendritic cell maturation. Clin Exp Immunol 135(2): 336-342.
38. Lynes MA, Borghesi LA, Youn J, Olson EA, (1993) Immunomodulatory activities of extracellular metallothionein. I. metallothionein effects on antibody production. Toxicology 85(2-3): 161-177.
39. Youn J, Borghesi LA, Olson EA, Lynes MA, (1995) Immunomodulatory activities of extracellular metallothionein. II. effects on macrophage functions. J Toxicol Environ Health 45(4): 397-413 10.1080/15287399509532004.
40. Youn J, Lynes MA, (1999) Metallothionein-induced suppression of cytotoxic T lymphocyte function: An important immunoregulatory control. Toxicol Sci 52(2): 199-208.
41. Huh S, Lee K, Yun HS, Paik DJ, Kim JM, et al. (2007) Functions of metallothionein generating interleukin-10-producing regulatory CD4+ T cells potentiate suppression of collagen-induced arthritis. J Microbiol Biotechnol 17(2): 348-358.