Peroxisome proliferator-activated receptor-α activation inhibits langerhans cell function

Journal of Immunology

Volumn 178, Issue 7, 2007, Pages 4362-4372

  Dubrac, Sandrine ^a   Stoitzner, Patrizia ^a   Pirkebner, Daniela ^a   Elentner, Andreas ^a   Schoonjans, Kristina ^b   Auwerx, Johan ^b   Saeland, Sem ^c   Hengster, Paul ^a   Fritsch, Peter ^a   Romani, Nikolaus ^a   Schmuth, Matthias ^a  

^a INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^b INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^c DermImmune   (France)

Author keywords

[No Author keywords available]

Indexed keywords

4 PHENYLBUTYRIC ACID; CYTOKINE; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; MACROPHAGE INFLAMMATORY PROTEIN 2; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE P38; OLEIC ACID; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PICRYL CHLORIDE; PIRINIXIC ACID; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL MATURATION; CELL MIGRATION; CELL PROLIFERATION; CONFOCAL MICROSCOPY; CONTACT DERMATITIS; CONTROLLED STUDY; CYTOKINE PRODUCTION; EPIDERMIS CELL; FLOW CYTOMETRY; IMMUNE RESPONSE; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; INFLAMMATION; KERATINOCYTE; LANGERHANS CELL; MAJOR HISTOCOMPATIBILITY COMPLEX; MIXED LYMPHOCYTE REACTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SKIN; SKIN ALLERGY; T LYMPHOCYTE;

EID: 33947674880     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.178.7.4362     Document Type: Article

References (57)

1. Chawla, A., J. J. Repa, R. M. Evans, and D. J. Mangelsdorf. 2001. Nuclear receptors and lipid physiology: opening the X-files. Science 294: 1866-1870.
2. Shulman, A. I., and D. J. Mangelsdorf. 2005. Retinoid X receptor heterodimers in the metabolic syndrome. N. Engl. J. Med. 353: 604-615.
3. Desvergne, B., L. Michalik, and W. Wahli. 2004. Be fit or be sick: peroxisome proliferator-activated receptors are down the road. Mol. Endocrinol. 18: 1321-1332.
4. Glass, C. K., and S. Ogawa. 2006. Combinatorial roles of nuclear receptors in inflammation and immunity. Nature 6: 44-55.
5. Devchand, P. R., H. Keller, J. M. Peters, M. Vazquez, F. J. Gonzalez, and W. Wahli. 1996. The PPAR α-leukotriene B4 pathway to inflammation control. Nature 384: 39-43.
6. Szatmari, I., P. Gogolak, J. S. Im, B. Dezso, E. Rajnavolgyi, and L. Nagy. 2004. Activation of PPARγ specifies a dendritic cell subtype capable of enhanced induction of iNKT cell expansion. Immunity 21: 95-106.
7. Nencioni, A., F. Grünebach, A. Zobywlaski, C. Denzlinger, W. Brugger, and P. Brossart. 2002. Dendritic cell immunogenicity is regulated by peroxisome proliferator-activated receptor γ. J. Immunol. 169: 1228-1235.
8. Angeli, V., H. Hammad, B. Staels, M. Capron, B. N. Lambrecht, and F. Trottein. 2003. Peroxisome proliferator-activated receptor γ inhibits the migration of dendritic cells: consequences for the immune response. J. Immunol. 170: 5295-5301.
9. Appel, S., V. Mirakaj, A. Bringmann, M. M. Weck, F. Grünebach, and P. Brossart 2005. PPAR-γ agonists inhibit Toll-like receptor-mediated activation of dendritic cells via the MAP kinase and NF-κB pathways. Blood 106: 3888-3894.
10. Schachtrup, C., T. E. Scholzen, V. Grau, T. A. Luger, C. Sorg, F. Spener, and C. Kerkhoff. 2004. L-FABP is exclusively expressed in alveolar macrophages within the myeloid lineage: evidence for a PPAR α-independent expression. Int J. Biochem. Cell Biol. 36: 2042-2053.
11. Jakobsen, M. A., R. K. Petersen, K. Kristiansen, M. Lange, and S. T. Lillevang. 2006. Peroxisome proliferator-activated receptor α, δ1, γ1 and γ2 expressions are present in human monocyte-derived dendritic cells and modulate dendritic cell maturation by addition of subtype-specific ligands. Scand. J. Immunol. 63: 330-337.
12. Li, A. C., Binder, C. J. Gutierrez, A. Brown, K. K. Plotkin, C. R. Pattison, J. W. Valledor, A. F. Davis, R. A. Willson, T. M. Witztum, et al. 2004. Differential inhibition of macrophage foam-cell formation and atherosclerosis in mice by PPAR α, β/δ, and γ. J. Clin. Invest. 114: 1564-1576.
13. Barish, G. D., V. A. Narkar, and R. M. Evans. 2006. PPAR δ: a dagger in the heart of the metabolic syndrome. J. Clin. Invest. 116: 590-597.
14. Sheu, M. Y., A. J. Fowler, J. Kao, M. Schmuth, K. Schoonjans, J. Auwerx, J. W. Fluhr, M. Q. Man, P. M. Elias, and K. R. Feingold. 2002. Topical peroxisome proliferator activated receptor-α activators reduce inflammation in irritant and allergic contact dermatitis models. J. Invest. Dermatol. 118: 94-101.
15. Romani, N., S. Holzmann, C. H. Tripp, F. Koch, and P. Stoitzner. 2003. Langerhans cells-dendritic cells of the epidermis. APMIS 111: 725-740.
16. Matzinger, P. 2002. The danger model: a renewed sense of self. Science 296: 301-305.
17. Ruzicka, T., and J. Auböck. 1987. Arachidonic acid metabolism in guinea pig Langerhans cells: studies on cyclooxygenase and lipoxygenase pathways. J. Immunol. 138: 539-543.
18. 2-EP4 signaling initiates skin immune responses by promoting migration and maturation of Langerhans cells. Nat. Med. 9: 744-749.
19. Dreyer, C., H. Keller, A. Mahfoudi, V. Laudet, G. Krey, and W. Wahli. 1993. Positive regulation of the peroxisomal β-oxidation pathway by fatty acids through activation of peroxisome proliferator-activated receptors (PPAR). Biol. Cell 77: 67-76.
20. Schmuth, M., K. Schoonjans, Q. C. Yu, J. W. Fluhr, D. Crumrine, J. P. Hachem, P. Lau, J. Auwerx, P. M. Elias, and K. R. Feingold. 2002. Role of peroxisome proliferator-activated receptor α in epidermal development in utero. J. Invest. Dermatol. 119: 1298-1303.
21. Stoitzner, P., S. Holzmann, A. D. McLellan, L. Ivarsson, H. Stössel, M. Kapp, U. Kämmerer, P. Douillard, E. Kämpgen, F. Koch, et al. 2003. Visualization and characterization of migratory Langerhans cells in murine skin and lymph nodes by antibodies against Langerin/CD207. J. Invest. Dermatol. 120: 266-274.
22. McLellan, A. D., G. C. Starling, and D. N. Hart. 1995. Isolation of human blood dendritic cells by discontinuous Nycodenz gradient centrifugation. J. Immunol. Methods 184: 81-89.
23. Stoitzner, P., C. H. Tripp, P. Douillard, S. Saeland, and N. Romani. 2005. Migratory Langerhans cells in mouse lymph nodes in steady state and inflammation. J. Invest. Dermatol. 125: 116-125.
24. Ricote, M., A. C. Li, T. M. Willson, C. J. Kelly, and C. K. Glass. 1998. The peroxisome proliferator-activated receptor-γ is a negative regulator of macrophage activation. Nature 391: 79-82.
25. Keller, H., C. Dreyer, J. Medin, A. Mahfoudi, K. Ozato, and W. Wahli. 1993. Fatty acids and retinoids control lipid metabolism through activation of peroxisome proliferator-activated receptor-retinoid X receptor heterodimers. Proc. Natl. Acad. Sci. USA 90: 2160-2164.
26. Yu, K., W. Bayona, C. B. Kallen, H. P. Harding, C. P. Ravera, G. McMahon, M. Brown, and M. A. Lazar. 1995. Differential activation of peroxisome proliferator-activated receptors by eicosanoids. J. Biol. Chem. 270: 23975-23983.
27. Gondcaille, C., M. Depreter, S. Fourcade, M. R. Lecca, S. Leclercq, P. G. P. Martin, T. Pineau, F. Cadepond, M. ElEtr, N. Bertrand, et al. 2005. Phenylbutyrate up-regulates the adrenoleukodystrophy-related gene as a nonclassical peroxisome proliferator. J. Cell Biol. 169: 93-104.
28. Kehrer, J. P., S. S. Biswal, E. La, P. Thuillier, K. Datta, S. M. Fischer, and J. P. Vanden Heuvel. 2001. Inhibition of peroxisome-proliferator- activated receptor (PPAR)α by MK886. Biochem. J. 356: 899-906.
29. Rescigno, M., M. Martino, C. L. Sutherland, M. R. Gold, and P. Ricciardi-Castagnoli. 1998. Dendritic cell survival and maturation are regulated by different signaling pathways. J. Exp. Med. 188: 2175-2180.
30. Boisleve, F., S. Kerdine-Romer, and M. Pallardy. 2005. Implication of the MAPK pathways in the maturation of human dendritic cells induced by nickel and TNF-α. Toxicology 206: 233-244.
31. Nakagawa, S., T. Ohtani, M. Mizuashi, Z. U. Mellah, Y. Ito, H. Tagami, and S. Aiba. 2004. p38 Mitogen-activated protein kinase mediates dual role of ultraviolet B radiation in induction of maturation and apoptosis of monocyte-derived dendritic cells. J. Invest. Dermatol. 123: 361-370.
32. Chung, S., J. M. Brown, J. N. Provo, R. Hopkins, and M. K. McIntosh. 2005. Conjugated linoleic acid promotes human adipocyte insulin resistance through NFκB-dependent cytokine production. J. Biol. Chem. 280: 38445-38456.
33. Kippenberger, S., S. M. Loitsch, M. Grundmann-Kollmann, S. Simon, T. Dang, K. Hardt-Weinelt, R. Kaufmann, and A. Bernd. 2001. Activators of peroxisome proliferator-activated receptors protect human skin from ultraviolet-B-light-induced inflammation. J. Invest. Dermatol. 117: 1430-1436.
34. Sumanasekera, W. K., E. S. Tien, J. W. Davis, I. I. R. Turpey, G. H. Perdew, and J. P. Vanden Heuvel. 2003. Heat shock protein-90 (Hsp90) acts as a repressor of peroxisome proliferator-activated receptor-α (PPAR α) and PPAR β activity. Biochemistry 42: 10726-10735.
35. Sumanasekera, W. K., E. S. Tien, R. Turpey, J. P. Vanden Heuvel, and G. H. Perdew. 2003. Evidence that peroxisome proliferator-activated receptor α is complexed with the 90-kDa heat shock protein and the hepatitis virus B X-associated protein 2. J. Biol. Chem. 278: 4467-4473.
36. Blanquart, C., O. Barbier, J. C. Fruchart, B. Staels, and C. Glineur. 2003. Peroxisome proliferator-activated receptors: regulation of transcriptional activities and roles in inflammation. J. Steroid Biochem. Mol. Biol. 85: 267-273.
37. Kriehuber, E., W. Bauer, A. S. Charbonnier, D. Winter, S. Amatschek, D. Tamandl, N. Schweifer, G. Stingl, and D. Maurer. 2005. Balance between NF-κB and JNK/AP-1 activity controls dendritic cell life and death. Blood 106: 175-183.
38. Randolph, G. J., G. Sanchez-Schmitz, and V. Angeli. 2005. Factors and signals that govern the migration of dendritic cells via lymphatics: recent advances. Springer Semin. Immunopathol. 26: 273-287.
39. Delerive, P., K. De Bosscher, S. Besnard, W. Vanden Berghe, J. M. Peters, F. J. Gonzalez, J. C. Fruchart, A. Tedgui, G. Haegeman, and B. Staels. 1999. Peroxisome proliferator-activated receptor α negatively regulates the vascular inflammatory gene response by negative cross-talk with transcription factors NF-κB and AP-1. J. Biol. Chem. 274: 32048-32054.
40. Delerive, P., P. Gervois, J. C. Fruchart, and B. Staels. 2000. Induction of IκBα expression as a mechanism contributing to the anti-inflammatory activities of peroxisome proliferator-activated receptor-α activators. J. Biol. Chem. 275: 36703-36707.
41. Delerive, P., K. De Bosscher, W. Vanden Berghe, I. C. Fruchart, G. Haegeman, and B. Staels. 2002. DNA binding-independent induction of IκBα gene transcription by PPAR α. Mol. Endocrinol. 6: 1029-1039.
42. Heufler, C., G. Topar, F. Koch, B. Trockenbacher, E. Kämpgen, N. Romani, and G. Schuler. 1992. Cytokine gene expression in murine epidermal cell suspensions: interleukin 1β and macrophage inflammatory protein 1α are selectively expressed in Langerhans cells but are differentially regulated in culture. J. Exp. Med. 176: 1221-1226.
43. Enk, A. H., V. L. Angeloni, M. C. Udey, and S. I. Katz. 1993. An essential role for Langerhans cell-derived IL-1β in the initiation of primary immune responses in skin. J. Immunol. 150: 3698-3704.
44. Cumberbatch, M., R. J. Dearman, and I. Kimber. 1997. Langerhans cells require signals from both tumour necrosis factor-α and interleukin-1β for migration. Immunology 92: 388-395.
45. Cumberbatch, M., M. Bhushan, R. J. Dearman, I. Kimber, and C. E. Griffiths. 2003. IL-1β-induced Langerhans cell migration and TNF-α production in human skin: regulation by lactoferrin. Clin. Exp. Immunol. 132: 352-359.
46. Shornick, L. P., A. K. Bisarya, and D. D. Chaplin. 2001. IL-1β is essential for Langerhans cell activation and antigen delivery to the lymph nodes during contact sensitization: evidence for a dermal source of IL-1β. Cell Immunol. 211: 105-112.
47. Stoitzner, P., M. Zanella, U. Ortner, M. Lukas, A. Tagwerker, K. Janke, M. B. Lutz, G. Schuler, B. Echtenacher, B. Ryffel, et al. 1999. Migration of Langerhans cells and dermal dendritic cells in skin organ cultures: augmentation by TNF-α and IL-1β. J. Leukocyte Biol. 66: 462-470.
48. Schwarzenberger, K., and M. C. Udey. 1996. Contact allergens and proinflammatory cytokines modulate LC E-cadherin expression in situ. J. Invest. Dermatol. 106: 553-558.
49. Zhang, Y., K. McCluskey, K. Fujii, and L. M. Wahl. 1998. Differential regulation of monocyte matrix metalloproteinase and TIMP-1 production by TNF-α, granulocyte-macrophage CSF, and IL-1β through prostaglandin-dependent and -independent mechanisms. J. Immunol. 161: 3071-3076.
50. Kobayashi, Y., M. Matsumoto, M. Kotani, and T. Makino. 1999. Possible involvement of matrix metalloproteinase-9 in Langerhans cell migration and maturation. J. Immunol. 163: 5989-5993.
51. Ratzinger, G., P. Stoitzner, S. Ebner, M. B. Lutz, G. T. Layton, C. Rainer, R. M. Senior, J. M. Shipley, P. Fritsch, G. Schuler, and N. Romani. 2002. Matrix metalloproteinases 9 and 2 are necessary for the migration of Langerhans cells and dermal dendritic cells from human and murine skin. J. Immunol. 168: 4361-4371.
52. Enk, A. H., and S. I. Katz. 1992. Early molecular events in the induction phase of contact sensitivity. Proc. Natl. Acad. Sci. USA 89: 1398-1402.
53. Romani, N., S. Holzmann, C. H. Tripp, M. Sixt, and P. Stoitzner. 2005. Trafficking of dendritic cells. In Leukocyte Trafficking. A. Hamann and B. Engelhardt, eds. Wiley-VCH Publishers, Weinheim, Germany, pp. 184-215.
54. Randolph, G. J., G. Sanchez-Schmitz, and V. Angeli. 2005. Factors and signals that govern the migration of dendritic cells via lymphatics: recent advances. Springer Semin. Immunopathol. 26: 273-287.
55. Bonizzi, G., and M. Karin. 2004. The two NF-κB activation pathways and their role in innate and adaptive immunity. Trends Immunol. 25: 280-288.
56. Cunard, R., D. DiCampli, D. C. Archer, J. L. Stevenson, M. Ricote, C. K. Glass, and C. J. Kelly. 2002. WY14,643, a PPAR α ligand, has profound effects on immune responses in vivo. J. Immunol. 169: 6806-6812.
57. Xu, J., P. D. Storer, J. A. Chavis, M. K. Racke, and P. D. Drew. 2005. Agonists for the peroxisome proliferator-activated receptor-α and the retinoid X receptor inhibit inflammatory responses of microglia. J. Neurosci. Res. 81: 403-411.