Peroxisome proliferator-activated receptors α and γ down-regulate allergic inflammation and eosinophil activation

Journal of Experimental Medicine

Volumn 198, Issue 3, 2003, Pages 411-421

  Woerly, Gaetane ^a   Honda, Kohei ^a   Loyens, Marc ^a   Papin, Jean Paul ^a   Auwerx, Johan ^c   Staels, Bart ^b   Capron, Monique ^a   Dombrowicz, David ^a  

^a INSTITUT PASTEUR DE LILLE   (France)

^b INSERM   (France)

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

Author keywords

ADCC; Asthma; Eosinophils; IgE; Nuclear receptors

Indexed keywords

IMMUNOGLOBULIN E; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; TRANSCRIPTION FACTOR GATA 3;

AGONIST; ALLERGIC ASTHMA; ALLERGIC REACTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTIGEN EXPRESSION; ANTIGEN SPECIFICITY; ARTICLE; CELL TYPE; CHEMOTAXIS; CONTROLLED STUDY; CYTOKINE RELEASE; EFFECTOR CELL; EXPERIMENTAL MODEL; FEMALE; HUMAN; HUMAN CELL; HYPEREOSINOPHILIA; IMMUNE SYSTEM; IMMUNOGLOBULIN BLOOD LEVEL; LYMPHOCYTE ACTIVATION; LYMPHOCYTIC INFILTRATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; TARGET CELL DESTRUCTION;

ANILIDES; ANIMALS; ASTHMA; CHEMOTAXIS; DISEASE MODELS, ANIMAL; DNA-BINDING PROTEINS; DOWN-REGULATION; EOSINOPHILS; GATA3 TRANSCRIPTION FACTOR; HUMANS; INFLAMMATION; LUNG; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; RATS; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RESPIRATORY HYPERSENSITIVITY; THIAZOLES; THIAZOLIDINEDIONES; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS;

EID: 0042624848     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.20021384     Document Type: Article

References (68)

1. Wills-Karp, M. 1999. Immunologic basis of antigen-induced airway hyperresponsiveness. Annu. Rev. Immunol. 17:255-281.
2. Maddox, L., and D.A. Schwartz. 2002. The pathophysiology of asthma. Annu. Rev. Med. 53:477-498.
3. Dombrowicz, D., and M. Capron. 2001. Eosinophils, allergy and parasites. Curr. Opin. Immunol. 13:716-720.
4. Desvergne, B., and W. Wahli. 1999. Peroxisome proliferator-activated receptors: nuclear control of metabolism. Endocr. Rev. 20:649-688.
5. Devchand, P.R., H. Keller, J.M. Peters, M. Vazquez, F.J. Gonzalez, and W. Wahli. 1996. The PPAralpha-leukotriene B4 pathway to inflammation control. Nature. 384:39-43.
6. Hatae, T., M. Wada, C. Yokoyama, M. Shimonishi, and T. Tanabe. 2001. Prostacyclin-dependent apoptosis mediated by PPARdelta. J. Biol. Chem. 276:46260-46267.
7. Nagy, L., P. Tontonoz, J.G. Alvarez, H. Chen, and R.M. Evans. 1998. Oxidized LDL regulates macrophage gene expression through ligand activation of PPARgamma. Cell. 93: 229-240.
8. Forman, B.M., P. Tontonoz, J. Chen, R.P. Brun, B.M. Spiegelman, and R.M. Evans. 1995. 15-Deoxy-delta 12, 14-prostaglandin J2 is a ligand for the adipocyte determination factor PPAR gamma. Cell. 83:803-812.
9. Delerive, P., J.C. Fruchart, and B. Staels. 2001. Peroxisome proliferator-activated receptors in inflammation control. J. Endocrinol. 169:453-459.
10. Clark, R.B. 2002. The role of PPARs in inflammation and immunity. J. Leukoc. Biol. 71:388-400.
11. Daynes, R.A., and D.C. Jones. 2002. Emerging roles of PPARs in inflammation and immunity. Nat. Rev. Immunol. 2:748-759.
12. Clark, R.B., D. Bishop-Bailey, T. Estrada-Hernandez, T. Hla, L. Puddington, and S.J. Padula. 2000. The nuclear receptor PPAR gamma and immunoregulation: PPAR gamma mediates inhibition of helper T cell responses. J. Immunol. 164:1364-1371.
13. Jones, D.C., X. Ding, and R.A. Daynes. 2001. Nuclear receptor peroxisome proliferator-activated receptor alpha (PPARalpha) is expressed in resting murine lymphocytes: the PPARalpha in T and B lymphocytes is both transactivation and transrepression competent. J. Biol. Chem. 277:6838-6845.
14. Chinetti, G., S. Griglio, M. Antonucci, I.P. Torra, P. Delerive, Z. Majd, J.C. Fruchart, J. Chapman, J. Najib, and B. Staels. 1998. Activation of proliferator-activated receptors alpha and gamma induces apoptosis of human monocyte-derived macrophages. J. Biol. Chem. 273:25573-25580.
15. Ricote, M., A.C. Li, T.M. Willson, C.J. Kelly, and C.K. Glass. 1998. The peroxisome proliferator-activated receptor-gamma is a negative regulator of macrophage activation. Nature. 391:79-82.
16. Tontonoz, P., L. Nagy, J.G. Alvarez, V.A. Thomazy, and R.M. Evans. 1998. PPARgamma promotes monocyte/macrophage differentiation and uptake of oxidized LDL. Cell. 93: 241-252.
17. Huang, J.T., J.S. Welch, M. Ricote, C.J. Binder, T.M. Willson, C. Kelly, J.L. Witztum, C.D. Funk, D. Conrad, and C.K. Glass. 1999. Interleukin-4-dependent production of PPAR-gamma ligands in macrophages by 12/15-lipoxygenase. Nature. 400:378-382.
18. Moore, K.J., E.D. Rosen, M.L. Fitzgerald, F. Randow, L.P. Andersson, D. Altshuler, D.S. Milstone, R.M. Mortensen, B.M. Spiegelman, and M.W. Freeman. 2001. The role of PPAR-gamma in macrophage differentiation and cholesterol uptake. Nat. Med. 7:41-47.
19. Faveeuw, C., S. Fougeray, V. Angeli, J. Fontaine, G. Chinetti, P. Gosset, P. Delerive, C. Maliszewski, M. Capron, B. Staels, et al. 2000. Peroxisome proliferator-activated receptor gamma activators inhibit interleukin-12 production in murine dendritic cells. FEBS Lett. 486:261-266.
20. Sugiyama, H., T. Nonaka, T. Kishimoto, K. Komoriya, K. Tsuji, and T. Nakahata. 2000. Peroxisome proliferator-activated receptors are expressed in human cultured mast cells: a possible role of these receptors in negative regulation of mast cell activation. Eur. J. Immunol. 30:3363-3370.
21. Tan, N.S., L. Michalik, N. Noy, R. Yasmin, C. Pacot, M. Heim, B. Fluhmann, B. Desvergne, and W. Wahli. 2001. Critical roles of PPAR beta/delta in keratinocyte response to inflammation. Genes Dev. 15:3263-3277.
22. Su, C.G., X. Wen, S.T. Bailey, W. Jiang, S.M. Rangwala, S.A. Keilbaugh, A. Flanigan, S. Murthy, M.A. Lazar, and G.D. Wu. 1999. A novel therapy for colitis utilizing PPAR-gamma ligands to inhibit the epithelial inflammatory response. J. Clin. Invest. 104:383-389.
23. Desreumaux, P., L. Dubuquoy, S. Nutten, M. Peuchmaur, W. Englaro, K. Schoonjans, B. Derijard, B. Desvergne, W. Wahli, P. Chambon, et al. 2001. Attenuation of colon inflammation through activators of the retinoid X receptor (RXR)/peroxisome proliferator-activated receptor γ (PPARγ) heterodimer. A basis for new therapeutic strategies. J. Exp. Med. 193:827-838.
24. Setoguchi, K., Y. Misaki, Y. Terauchi, T. Yamauchi, K. Kawahata, T. Kadowaki, and K. Yamamoto. 2001. Peroxisome proliferator-activated receptor-gamma haploinsufficiency enhances B cell proliferative responses and exacerbates experimentally induced arthritis. J. Clin. Invest. 108:1667-1675.
25. Lewis, J.D., G.R. Lichtenstein, R.B. Stein, J.J. Deren, T.A. Judge, F. Fogt, E.E. Furth, E.J. Demissie, L.B. Hurd, C.G. Su, et al. 2001. An open-label trial of the PPAR-gamma ligand rosiglitazone for active ulcerative colitis. Am. J. Gastroenterol. 96:3323-3328.
26. Benayoun, L., S. Letuve, A. Druilhe, J. Boczkowski, M.C. Dombret, P. Mechighel, J. Megret, G. Leseche, M. Aubier, and M. Pretolani. 2001. Regulation of peroxisome proliferator-activated receptor gamma expression in human asthmatic airways: relationship with proliferation, apoptosis, and airway remodeling. Am. J. Respir. Crit. Care Med. 164:1487-1494.
27. Poynter, M.E., and R.A. Daynes. 1998. Peroxisome proliferator-activated receptor alpha activation modulates cellular redox status, represses nuclear factor-kappaB signaling, and reduces inflammatory cytokine production in aging. J. Biol. Chem. 273:32833-32841.
28. 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 alpha negatively regulates the vascular inflammatory gene response by negative cross-talk with transcription factors NF-kappaB and AP-1. J. Biol. Chem. 274: 32048-32054.
29. Lee, S.S., T. Pineau, J. Drago, E.J. Lee, J.W. Owens, D.L. Kroetz, P.M. Fernandez-Salguero, H. Westphal, and F.J. Gonzalez. 1995. Targeted disruption of the alpha isoform of the peroxisorne proliferator-activated receptor gene in mice results in abolishment of the pleiotropic effects of peroxisome proliferators. Mol. Cell. Biol. 15:3012-3022.
30. Kayaba, H., D. Dombrowicz, G. Woerly, J.P. Papin, S. Loiseau, and M. Capron. 2001. Human eosinophils and human high affinity IgE receptor transgenic mouse eosinophils express low levels of high affinity IgE receptor, but release IL-10 upon receptor activation. J. Immunol. 167:995-1003.
31. Hamelmann, E., J. Schwarze, K. Takeda, A. Oshiba, G.L. Larsen, C.G. Irvin, and E.W. Gelfand. 1997. Noninvasive measurement of airway responsiveness in allergic mice using barometric plethysmography. Am. J. Respir. Crit. Care Med. 156:766-775.
32. Standiford, T.J., S.L. Kunkel, N.W. Lukacs, M.J. Greenberger, J.M. Danforth, R.G. Kunkel, and R.M. Strieter. 1995. Macrophage inflammatory protein-1 alpha mediates lung leukocyte recruitment, lung capillary leak, and early mortality in murine endotoxemia. J. Immunol. 155:1515-1524.
33. Angeli, V., C. Faveeuw, P. Delerive, J. Fontaine, Y. Barriera, N. Franchimont, B. Staels, M. Capron, and F. Trottein. 2001. Schistosoma mansoni induces the synthesis of IL-6 in pulmonary microvascular endothelial cells: role of IL-6 in the control of lung eosinophilia during infection. Eur. J. Immunol. 31:2751-2761.
34. Woerly, G., N. Roger, S. Loiseau, D. Dombrowicz, A. Capron, and M. Capron. 1999. Expression of CD28 and CD86 by human eosinophils and role in the secretion of type 1 cytokines (interleukin 2 and interferon γ): inhibition by immunoglobulin A complexes. J. Exp. Med. 190:487-495.
35. Huang, W.W., E.A. Garcia-Zepeda, A. Sauty, H.C. Oettgen, M.E. Rothenberg, and A.D. Luster. 1998. Molecular and biological characterization of the murine leukotriene B4 receptor expressed on eosinophils. J. Exp. Med. 188:1063-1074.
36. Capron, M., S. Loiseau, J.P. Papin, S. Robertson, and A. Capron. 1998. Inhibitory effects of lodoxamide on eosinophil activation. Int. Arch. Allergy Immunol. 116:140-146.
37. Dombrowicz, D., B. Quatannens, J.P. Papin, A. Capron, and M. Capron. 2000. Expression of a functional Fc epsilon RI on rat eosinophils and macrophages. J. Immunol. 165:1266-1271.
38. Malm-Erjefalt, M., C.G. Persson, and J.S. Erjefalt. 2001. Degranulation status of airway tissue eosinophils in mouse models of allergic airway inflammation. Am. J. Respir. Cell Mol. Biol. 24:352-359.
39. Zheng, W., and R.A. Flavell. 1997. The transcription factor GATA-3 is necessary and sufficient for Th2 cytokine gene expression in CD4 T cells. Cell. 89:587-596.
40. Justice, J.P., M.T. Borchers, J.J. Lee, W.H. Rowan, Y. Shibata, and M.R. Van Scott. 2002. Ragweed-induced expression of GATA-3, IL-4, and IL-5 by eosinophils in the lungs of allergic C57BL/6J mice. Am. J. Physiol. Lung Cell. Mol. Physiol. 282:L302-L309.
41. Capron, M., and A. Capron. 1994. Immunoglobulin E and effector cells in schistosomiasis. Science. 264:1876-1877.
42. Grezel, D., M. Capron, J.M. Grzych, J. Fontaine, J.P. Lecocq, and A. Capron. 1993. Protective immunity induced in rat schistosomiasis by a single dose of the Sm28GST recombinant antigen: effector mechanisms involving IgE and IgA antibodies. Eur. J. Immunol. 23:454-460.
43. Gavett, S.H., X. Chen, F. Finkelman, and M. Wills-Karp. 1994. Depletion of murine CD4+ T lymphocytes prevents antigen-induced airway hyperreactivity and pulmonary eosinophilia. Am. J. Respir. Cell Mol. Biol. 10:587-593.
44. + T cells in the development of airway hyperresponsiveness in a marine model of airway sensitization. J. Exp. Med. 183:1719-1729.
45. Foster, P.S., A.W. Mould, M. Yang, J. Mackenzie, J. Mattes, S.P. Hogan, S. Mahalingam, A.N. McKenzie, M.E. Rothenberg, I.G. Young, et al. 2001. Elemental signals regulating eosinophil accumulation in the lung. Immunol. Rev. 179:173-181.
46. Hart, P.H. 2001. Regulation of the inflammatory response in asthma by mast cell products. Immunol. Cell Biol. 79:149-153.
47. Jones, D.C., B.M. Manning, and R.A. Daynes. 2002. A role for the peroxisome proliferator-activated receptor alpha in T-cell physiology and ageing immunobiology. Proc. Nutr. Soc. 61:363-369.
48. Woerly, G., P. Lacy, A.B. Younes, N. Roger, S. Loiseau, R. Moqbel, and M. Capron. 2002. Human eosinophils express and release IL-13 following CD28-dependent activation. J. Leukoc. Biol. 72:769-779.
49. Mattes, J., M. Yang, S. Mahalingam, J. Kuehr, D.C. Webb, L. Simson, S.P. Hogan, A. Koskinen, A.N. McKenzie, L.A. Dent, et al. 2002. Intrinsic defect in T cell production of interleukin (IL)-13 in the absence of both IL-5 and eotaxin precludes the development of eosinophilia and airways hyperreactivity in experimental asthma. J. Exp. Med. 195:1433-1444.
50. Zhu, Z., R.J. Homer, Z. Wang, Q. Chen, G.P. Geba, J. Wang, Y. Zhang, and J.A. Elias. 1999. Pulmonary expression of interleukin-13 causes inflammation, mucus hypersecretion, subepithelial fibrosis, physiologic abnormalities, and eotaxin production. J. Clin. Invest. 103:779-788.
51. Kuperman, D.A., X. Huang, L.L. Koth, G.H. Chang, G.M. Dolganov, Z. Zhu, J.A. Elias, D. Sheppard, and D.J. Erle. 2002. Direct effects of interleukin-13 on epithelial cells cause airway hyperreactivity and mucus overproduction in asthma. Nat. Med. 8:885-889.
52. Lee, J.H., N. Kaminski, G. Dolganov, G. Grunig, L. Koth, C. Solomon, D.J. Erle, and D. Sheppard. 2001. Interleukin-13 induces dramatically different transcriptional programs in three human airway cell types. Am. J. Respir. Cell Mol. Biol. 25:474-485.
53. Rothenberg, M.E., A.D. Luster, and P. Leder. 1995. Murine eotaxin: an eosinophil chemoattractant inducible in endothelial cells and in interleukin 4-induced tumor suppression. Proc. Natl. Acad. Sci. USA. 92:8960-8964.
54. Lee, H., W. Shi, P. Tontonoz, S. Wang, G. Subbanagounder, C.C. Hedrick, S. Hama, C. Borromeo, R.M. Evans, J.A. Berliner, and L. Nagy. 2000. Role for peroxisome proliferator-activated receptor alpha in oxidized phospholipid-induced synthesis of monocyte chemotactic protein-1 and interleukin-8 by endothelial cells. Circ. Res. 87: 516-521.
55. Wang, A.C., X. Dai, B. Luu, and D.J. Conrad. 2001. Peroxisome proliferator-activated receptor-gamma regulates airway epithelial cell activation. Am. J. Respir. Cell Mol. Biol. 24: 688-693.
56. Patel, H.J., M.G. Belvisi, D. Bishop-Bailey, M.H. Yacoub, and J.A. Mitchell. 2003. Activation of peroxisome proliferator-activated receptors in human airway smooth muscle cells has a superior anti-inflammatory profile to corticosteroids: relevance for chronic obstructive pulmonary disease therapy. J. Immunol. 170:2663-2669.
57. Gosset, P., A.S. Charbonnier, P. Delerive, J. Fontaine, B. Staels, J. Pestel, A.B. Tonnel, and F. Trottein. 2001. Peroxisome proliferator-activated receptor gamma activators affect the maturation of human monocyte-derived dendritic cells. Eur. J. Immunol. 31:2857-2865.
58. Lambrecht, B.N., M. De Veerman, A.J Coyle, J.C. Gutierrez-Ramos, K. Thielemans, and R.A. Pauwels. 2000. Myeloid dendritic cells induce Th2 responses to inhaled antigen, leading to eosinophilic airway inflammation. J. Clin. Invest. 106:551-559.
59. Angeli, V., C. Faveeuw, O. Roye, J. Fontaine, E. Teissier, A. Capron, I. Wolowczuk, M. Capron, and F. Trottein. 2001. Role of the parasite-derived prostaglandin D2 in the inhibition of epidermal Langerhans' cell migration during schistosomiasis infection. J. Exp. Med. 193:1135-1147.
60. Yang, X.Y., L.H. Wang, T. Chen, D.R. Hodge, J.H. Resau, L. DaSilva, and W.L. Farrar. 2000. Activation of human T lymphocytes is inhibited by peroxisome proliferator-activated receptor gamma (PPARgamma) agonists. PPARgamma co-association with transcription factor NFAT. J. Biol. Chem. 275:4541-4544.
61. Miyazaki, Y., H. Tachibana, and K. Yamada. 2002. Inhibitory effect of peroxisome proliferator-activated receptor-gamma ligands on the expression of IgE heavy chain germline transcripts in the human B cell line DND39. Biochem. Biophys. Res. Commun. 295:547-552.
62. Adachi, T., and R. Alam. 1998. The mechanism of IL-5 signal transduction. Am. J. Physiol. 275:C623-C633.
63. Kampen, G.T., S. Stafford, T. Adachi, T. Jinquan, S. Quan, J.A. Grant, P.S. Skov, L.K. Poulsen, and R. Alam. 2000. Eotaxin induces degranulation and chemotaxis of eosinophils through the activation of ERK2 and p38 mitogen-activated protein kinases. Blood. 95:1911-1917.
64. Tsai, M., S.Y. Tam, and S.J. Galli. 1993. Distinct patterns of early response gene expression and proliferation in mouse mast cells stimulated by stem cell factor, interleukin-3, or IgE and antigen. Eur. J. Immunol. 23:867-872.
65. Razin, E., Z. Szallasi, M.G. Kazanietz, P.M. Blumberg, and J. Rivera. 1994. Protein kinases C-beta and C-epsilon link the mast cell high-affinity receptor for IgE to the expression of c-fos and c-jun. Proc. Natl. Acad. Sci. USA. 91:7722-7726.
66. Ishizuka, T., K. Chayama, K. Takeda, E. Hamelmann, N. Terada, G.M. Keller, G.L. Johnson, and E.W. Gelfand. 1999. Mitogen-activated protein kinase activation through Fc epsilon receptor I and stem cell factor receptor is differentially regulated by phosphatidylinositol 3-kinase and calcineurin in mouse bone marrow-derived mast cells. J. Immunol. 162: 2087-2094.
67. Pelletier, C., N. Varin-Blank, J. Rivera, B. Iannascoli, F. Marchand, B. David, A. Weyer, and U. Blank. 1998. Fc epsilonRI-mediated induction of TNF-alpha gene expression in the RBL-2H3 mast cell line: regulation by a novel NF-kappaB-like nuclear binding complex. J. Immunol. 161:4768-4776.
68. Leckie, M.J., A. ten Brinke, J. Khan, Z. Diamant, B.J. O'Connor, C.M. Walls, A.K. Mathur, H.C. Cowley, K.F. Chung, R. Djukanovic, et al. 2000. Effects of an interleukin-5 blocking monoclonal antibody on eosinophils, airway hyperresponsiveness, and the late asthmatic response. Lancet. 356: 2144-2148.