Chronic estradiol administration in vivo promotes the proinflammatory response of macrophages to TLR4 activation: Involvement of the phosphatidylinositol 3-kinase pathway

Journal of Immunology

Volumn 180, Issue 12, 2008, Pages 7980-7988

  Calippe, Bertrand ^a   Douin Echinard, Victorine ^a   Laffargue, Muriel ^b   Laurell, Henrik ^a   Rana Poussine, Vanessa ^a   Pipy, Bernard ^c   Guéry, Jean Charles ^b   Bayard, Francis ^a   Arnal, Jean François ^a   Gourdy, Pierre ^a,d,e  

^a INSERM   (France)

^b France   (France)

^c TOULOUSE UNIVERSITY HOSPITAL   (France)

^d Unité'Propre à I'Enscignement Supérieur Associée Toulouse Rangueil   (France)

^e Institut National de la Santé et de la Recherche Médicate U858   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ESTRADIOL; ESTROGEN RECEPTOR ALPHA; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 12P40; INTERLEUKIN 1BETA; INTERLEUKIN 6; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; TOLL LIKE RECEPTOR 4; TRANSCRIPTION FACTOR RELA; WORTMANNIN; AUTACOID; CYTOKINE; LIPOPOLYSACCHARIDE; TLR4 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME ACTIVITY; FEMALE; GENE ACTIVATION; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CELL CULTURE; DELAYED RELEASE FORMULATION; DRUG ANTAGONISM; DRUG EFFECT; DRUG IMPLANT; ENZYMOLOGY; GENETICS; IMMUNOLOGY; INTRADERMAL DRUG ADMINISTRATION; MACROPHAGE ACTIVATION; METABOLISM; MOUSE MUTANT; PERITONEUM MACROPHAGE; PHYSIOLOGY; SIGNAL TRANSDUCTION; TIME;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ADMINISTRATION, CUTANEOUS; ANIMALS; CELLS, CULTURED; CYTOKINES; DELAYED-ACTION PREPARATIONS; DRUG IMPLANTS; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; FEMALE; INFLAMMATION MEDIATORS; LIPOPOLYSACCHARIDES; MACROPHAGE ACTIVATION; MACROPHAGES, PERITONEAL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; SIGNAL TRANSDUCTION; TIME FACTORS; TOLL-LIKE RECEPTOR 4;

EID: 50949111554     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.180.12.7980     Document Type: Article

References (33)

1. Klein, S. L. 2000. Hormones and mating system affect sex and species differences in immune function among vertebrates. Behav. Processes 51: 149-166.
2. Waters, D. D., D. Gordon, J. E. Rossouw, R. O. Cannon, III, P. Collins, D. M. Herrington, J. Hsia, R. Longer, L. Mosca, P. Ouyang, et al. 2004. Women's Ischemic Syndrome Evaluation: current status and future research directions: report of the National Heart, Lung and Blood Institute workshop: October 2-4, 2002: Section 4: lessons from hormone replacement trials. Circulation 109: e53-e55.
3. Whitacre, C. C, S. C. Reingold, and P. A. O'Looney. 1999. A gender gap in autoimmunity. Science 283: 1277-1278.
4. Delpy, L., V. Douin-Echinard, L. Garidou, C. Bruand, A. Saoudi, and J. C. Guery. 2005. Estrogen enhances susceptibility to experimental autoimmune myasthenia gravis by promoting type 1-polarized immune responses. J. Immunol. 175: 5050-5057.
5. Gourdy, P., L. M. Araujo, R. Zhu, B. Garmy-Susini, S. Diem, H. Laurell, M. Leite-de-Moraes, M. Dy, J. F. Arnal, F. Bayard, and A. Herbelin. 2005. Relevance of sexual dimorphism to regulatory T cells: estradiol-promotes IFN-γ production by invariant natural killer T cells. Blood 105: 2415-2420.
6. Maret, A., J. D. Coudert, L. Garidou, G. Foucras, P. Gourdy, A. Krust, S. Dupont, P. Chambon, P. Druet, F. Bayard, and J. C. Guery. 2003. Estradiol enhances primary antigen-specific CD4 T cell responses and Th1 development in vivo: essential role of estrogen receptor α expression in hematopoietic cells. Eur. J. Immunol. 33: 512-521.
7. Taylor, P. R., L. Martinez-Pomares, M. Stacey, H. H. Lin, G. D. Brown, and S. Gordon. 2005. Macrophage receptors and immune recognition. Annu. Rev. Immunol. 23: 901-944.
8. Akira, S., and K. Takeda. 2004. Toll-like receptor signaling. Nat. Rev. Immunol. 4:499-511.
9. Takeda, K., T. Kaisho, and S. Akira. 2003. Toll-like receptors. Annu. Rev. Immunol. 21: 335-376.
10. Liew, F. Y., D. Xu, E. K. Brint, and L. A. O'Neill. 2005. Negative regulation of toll-like receptor-mediated immune responses. Nat. Rev. Immunol. 5: 446-458.
11. Fukao, T., and S. Koyasu. 2003. PI3K and negative regulation of TLR signaling. Trends Immunol. 24: 358-363.
12. Fukao, T., M. Tanabe, Y. Terauchi, T. Ota, S. Matsuda, T. Asano, T. Kadowaki, T. Takeuchi, and S. Koyasu. 2002. PI3K-mediated negative feedback regulation of IL-12 production in DCs. Nat. Immunol. 3: 875-881.
13. Guha, M., and N. Mackman. 2002. The phosphatidylinositol 3-kinase-Akt pathway limits lipopolysaccharide activation of signaling pathways and expression of inflammatory mediators in human monocytic cells. J. Biol. Chem. 277: 32124-32132.
14. Hawlisch, H., Y. Belkaid, R. Baelder, D. Hildeman, C. Gerard, and J. Kohl. 2005. C5a negatively regulates toll-like receptor 4-induced immune responses. Immunity 22: 415-426.
15. Molnarfi, N., L. Gruaz, J. M. Dayer, and D. Burger. 2007. Opposite regulation of IL-1β and secreted IL-1 receptor antagonist production by phosphatidylinosit-ide-3 kinases in human monocytes activated by lipopolysaccharides or contact with T cells. J. Immunol. 178: 446-454.
16. Ghisletti, S., C. Meda, A. Maggi, and E. Vegeto. 2005. 17β-estradiol inhibits inflammatory gene expression by controlling NF-κB intracellular localization. Mol. Celt. Biol. 25: 2957-2968.
17. Vegeto, E., S. Belcredito, S. Etteri, S. Ghisletti, A. Brusadelli, C. Meda, A. Krust, S. Dupont, P. Ciana, P. Chambon, and A. Maggi. 2003. Estrogen receptor-α mediates the brain antiinflammatory activity of estradiol. Proc. Natl. Acad. Sci. USA 100: 9614-9619.
18. Vegeto, E., C. Bonincontro, G. Pollio, A. Sala, S. Viappiani, F. Nardi, A. Brusadelli, B. Viviani, P. Ciana, and A. Maggi. 2001. Estrogen prevents the lipopolysaccharide-induced inflammatory response in microglia. J. Neurosci. 21-1809-1818.
19. Vegeto, E., S. Ghisletti, C. Meda, S. Etteri, S. Belcredito, and A. Maggi. 2004. Regulation of the lipopolysaccharide signal transduction pathway by 17β-estradiol in macrophage cells. J. Steroid Biochem. Mol. Biol. 91: 59-66.
20. Soucy, G., G. Boivin, F. Labrie, and S. Rivest. 2005. Estradiol is required for a proper immune response to bacterial and viral pathogens in the female brain J. Immunol. 174: 6391-6398.
21. Dupont, S., A. Krust, A. Gansmuller, A. Dierich, P. Chambon, and M. Mark. 2000. Effect of single and compound knockouts of estrogen receptors α (ERα) and β (ERβ) on mouse reproductive phenotypes. Development 127: 4277-4291.
22. Giulietti, A., L. Overbergh, D. Valckx, B. Decallonne, R. Bouillon, and C. Mathieu. 2001. An overview of real-time quantitative PCR: applications to quantify cytokine gene expression. Methods 25: 386-401.
23. Burns, K., F. Martinon, and J. Tschopp. 2003. New insights into the mechanism of IL-1β maturation. Curr. Opin. Immunol. 15: 26-30.
24. Li, P., H. Allen, S. Banerjee, S. Franklin, L. Herzog, C. Johnston, J. McDowell, M. Paskind, L. Rodman, J. Salfeld, et al. 1995. Mice deficient in IL-1 β-converting enzyme are defective in production of mature IL-1 β and resistant to endotoxic shock. Cell 80: 401-411.
25. Deshpande, R., H. Khalili, R. G. Pergolizzi, S. D. Michael, and M. D. Chang. 1997. Estradiol down-regulates LPS-induced cytokine production and NFκB activation in murine macrophages. Am. J. Reprod. Immunol. 38: 46-54.
26. Yu, Y., S. Nagai, H. Wu, A. S. Neish, S. Koyasu, and A. T. Gewirtz. 2006. TLR5-mediated phosphoinositide 3-kinase activation negatively regulates flagel-lin-induced proinflammatory gene expression. J. Immunol. 176: 6194-6201.
27. Mannella, P., arid R. D. Brinton. 2006. Estrogen receptor protein interaction with phosphatidylinositol 3-kinase leads to activation of phosphorylated Akt and extracellular signal-regulated kinase 1/2 in the same population of cortical neurons: a unified mechanism of estrogen action. J. Neurosci. 26: 9439-9447.
28. Mendelsohn, M. E. 2002. Nomic and nongenomic effects of estrogen in the vas-culature. Am. J. Cardiol. 90: 3F-6F.
29. Simoncini, T., E. Rabkin, and J. K. Liao. 2003. Molecular basis of cell membrane estrogen receptor interaction with phosphatidylinositol 3-kinase in endothelial cells. Arterioscler Thromb. Vasc. Biol. 23: 198-203.
30. Lu, Q., D. C. Pallas, H. K. Surks, W. E. Baur, M. E. Mendelsohn, and R. H. Karas. 2004. Striatin assembles a membrane signaling complex necessary for rapid, nongenomic activation of endothelial NO synthase by estrogen receptor α. Proc. Natl. Acad. Sci. USA 101: 17126-17131.
31. Douin-Echinard, V., S. Laffont, C. Seillet, L. Delpy, A. Krust, P. Chambon, P. Gourdy, J. F. Amal, and J. C. Guery. 2008. Estrogen receptor a, but not β, is required for optimal dendritic cell differentiation and CD40-induced cytokine production. J. Immunol. 180: 3661-3669.
32. Bebo, B. F., Jr., A. Fyfe-Johnson, K. Adlard, A. G. Beam, A. A. Vandenbark, and H. Offner. 2001. Low-dose estrogen therapy ameliorates experimental autoimmune encephalomyelitis in two different inbred mouse strains. J. Immunol. 166: 2080-2089.
33. Garidou, L., S. Laffont, V. Douin-Echinard, C. Coureau, A. Krust, P. Chambon, and J. C. Guery. 2004. Estrogen receptor α signaling in inflammatory leukocytes is dispensable for 17β-estradiol-mediated inhibition of experimental autoimmune encephalomyelitis. J. Immunol. 173: 2435-2442.