17β-estradiol inhibits inflammatory gene expression by controlling NF-κB intracellular localization

Molecular and Cellular Biology

Volumn 25, Issue 8, 2005, Pages 2957-2968

  Ghisletti, Serena ^a   Meda, Clara ^a   Maggi, Adriana ^a   Vegeto, Elisabetta ^a  

^a UNIVERSITY OF MILAN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLSALICYLIC ACID; ANTIINFLAMMATORY AGENT; DACTINOMYCIN; DEXAMETHASONE; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; I KAPPA B; IBUPROFEN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDOMETACIN; LIPOPOLYSACCHARIDE; MITOGEN ACTIVATED PROTEIN KINASE; NOCODAZOLE; NONSTEROID ANTIINFLAMMATORY AGENT; PHOSPHATIDYLINOSITOL 3 KINASE; PIRINIXIC ACID; PIROXICAM; PROTEIN P50; SYNAPTOTAGMIN; TRANSCRIPTION FACTOR REL; AUTACOID; DNA BINDING PROTEIN; NFKB1 PROTEIN, MOUSE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL NUCLEUS; CELL TRANSPORT; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DNA BINDING; DRUG MECHANISM; ENZYME ACTIVATION; GENE EXPRESSION; HUMAN; HUMAN CELL; INFLAMMATION; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FAMILY; PROTEIN SYNTHESIS; TRANSCRIPTION INITIATION; ACTIVE TRANSPORT; ANIMAL; CELL LINE; CHEMISTRY; CYTOPLASM; DOWN REGULATION; DRUG ANTAGONISM; DRUG EFFECT; GENE EXPRESSION REGULATION; METABOLISM; MICROGLIA; PHYSIOLOGY;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; CELL LINE; CELL NUCLEUS; CYTOPLASM; DNA-BINDING PROTEINS; DOWN-REGULATION; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; GENE EXPRESSION REGULATION; HUMANS; INFLAMMATION MEDIATORS; LIPOPOLYSACCHARIDES; MACROPHAGES; MICE; MICROGLIA; NF-KAPPA B; NF-KAPPA B P50 SUBUNIT; NOCODAZOLE; PROTO-ONCOGENE PROTEINS C-REL; TRANSCRIPTION FACTOR RELA; TRANSCRIPTION FACTORS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 16244373963     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.25.8.2957-2968.2005     Document Type: Article

References (47)

1. Ashcroft, G. S., S. J. Mills, K. Lei, L. Gibbons, M. J. Jeong, M. Taniguchi, M. Burow, M. A. Horan, S. M. Wahl, and T. Nakayama. 2003. Estrogen modulates cutaneous wound healing by downregulating macrophage migration inhibitory factor. J. Clin. Investig. 111:1309-1318.
2. Auphan, N., J. DiDonato, C. Rosette, A. Hemberg, and M. Karin. 1995. Immunosuppression by glucocorticoids: inhibition of NFκB activity through induction of IκB synthesis. Science 270:286-290.
3. 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.
4. Beg, A. A., W. C. Sha, R. T. Bronson, and D. Baltimore. 1995. Constitutive NF-kappa B activation, enhanced granulopoiesis, and neonatal lethality in I kappa B alpha-deficient mice. Genes Dev. 9:2736-2746.
5. Bourgarel-Rey, V., S. Vallee, O. Rimet, S. Champion, D. Braguer, A. Desobry, C. Briand, and Y. Barra. 2001. Involvement of nuclear factor kappaB in c-Myc induction by tubulin polymerization inhibitors. Mol. Pharmacol. 59:1165-1170.
6. Bruce-Keller, A., S. W. Barger, N. I. Moss, J. T. Pham, J. N. Keller, and A. Nath. 2001. Pro-inflammatory and pro-oxidant properties of the HIV protein Tat in a microglial cell line: attenuation by 17β-estradiol. J. Neurochem. 78:1515-1524.
7. Crepieux, P., H. Kwon, N. Leclerc, W. Spencer, S. Richard, R. Lin, and J. Hiscott. 1997. IκBα physically interacts with a cytoskeleton-associated protein through its signal response domain. Mol. Cell. Biol. 17:7375-7385.
8. De Bosscher, K., M. L. Schmitz, W. Vanden Berghe, S. Plaisance, W. Fiers, and G. Haegeman. 1997. Glucocorticoid-mediated repression of nuclear factor-kappaB-dependent transcription involves direct interference with transactivation. Proc. Natl. Acad. Sci. USA 94:13504-13509.
9. Diaz-Guerra, M. J., A. Castrillo, P. Martin-Sanz, and L. Bosca. 1999. Negative regulation by phosphatidylinositol 3-kinase of inducible nitric oxide synthase expression in macrophages. J. Immunol. 162:6184-6190.
10. Dubal, D. B., H. Zhu, J. Yu, S. W. Rau, P. J. Shughrue, I. Merchenthaler, M. S. Kindy, and P. M. Wise. 2001. Estrogen receptor alpha, not beta, is a critical link in estradiol-mediated protection against brain injury. Proc. Natl. Acad. Sci. USA 98:1952-1957.
11. 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.
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. Galien, R., and T. Garcia. 1997. Estrogen receptor impairs interleukin-6 expression by preventing protein binding on the NF-κB site. Nucleic Acids Res. 25:342-346.
14. Garidou, L., S. Laffont, V. Douin-Echinard, C. Coureau, A. Krust, P. Chambon, and J. C. Guery. 2004. Estrogen receptor alpha signaling in inflammatory leukocytes is dispensable for 17beta-estradiol-mediated inhibition of experimental autoimmune encephalomyelitis. J. Immunol. 173:2435-2442.
15. 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.
16. Gundersen, G. G., and T. A. Cook. 1999. Microtubules and signal transduction. Curr. Opin. Cell Biol. 11:81-94.
17. Hayashi, T., K. Yamada, T. Esaki, E. Muto, G. Chaudhuri, and A. Iguchi. 1998. Physiological concentrations of 17beta-estradiol inhibit the synthesis of nitric oxide synthase in macrophages via a receptor-mediated system. J. Cardiovasc. Pharmacol. 31:292-298.
18. Hodgin, J. B., and N. Maeda. 2002. Minireview: estrogen and mouse models of atherosclerosis. Endocrinology 143:4495-4501.
19. Holmes-McNary, M., and A. S. Baldwin, Jr. 2000. Chemopreventive properties of trans-resveratrol are associated with inhibition of activation of the IkappaB kinase. Cancer Res. 60:3477-3483.
20. Huang, T. T., N. Kudo, M. Yoshida, and S. Miyamoto. 2000. A nuclear export signal in the N-terminal regulatory domain of IκBα controls cytoplasmic localization of inactive NF-κB/IκBα complexes. Proc. Natl. Acad. Sci. USA 97:1014-1019.
21. Insall, R. H., and O. D. Weiner. 2001. PIP3, PIP2, and cell movement - similar messages, different meanings? Dev. Cell 1:743-747.
22. Ito, A., B. F. J. Bebo, A. Matejuk, A. Zamora, M. Silverman, A. Fyfe-Johnson, and H. Offner. 2001. Estrogen treatment down-regulates TNF-α production and reduces the severity of experimental autoimmune encephalomyelitis in cytokine knockout mice. J. Immunol. 167:529-542.
23. Jansson, L., T. Olsson, and R. Holmdahl. 1994. Estrogen induces a potent suppression of experimental autoimmune encephalomyelitis and collagen-induced arthritis in mice. J. Neuroimmunol. 53:203-207.
24. Jung, Y. J., J. S. Isaacs, S. Lee, J. Trepel, and L. Neckers. 2003. Microtubule disruption utilizes an NFkappa B-dependent pathway to stabilize HIF-1alpha protein. J. Biol. Chem. 278:7445-7452.
25. Klement, J. F., N. R. Rice, B. D. Car, S. J. Abbondanzo, G. D. Powers, P. H. Bhatt, C. H. Chen, C. A. Rosen, and C. L. Stewart. 1996. IκBα deficiency results in a sustained NF-κB response and severe widespread dermatitis in mice. Mol. Cell. Biol. 16:2341-2349.
26. Ma, Z. Q., E. Spreafico, G. Pollio, S. Santagati, E. Conti, E. Cattaneo, and A. Maggi. 1993. Activated estrogen receptor mediates growth arrest and differentiation of a neuroblastoma cell line. Proc. Natl. Acad. Sci. USA 90:3740-3744.
27. Matsuda, J., M. T. Vanier, Y. Saito, K. Suzuki, and S. Kunihiko. 2001. Dramatic phenotypic improvement during pregnancy in a genetic leukodystrophy: estrogen appears to be a critical factor. Hum. Mol. Genet. 10:2709-2715.
28. Miyamoto, N., M. Mandai, I. Suzuma, K. Suzuma, K. Kobayashi, and Y. Honda. 1999. Estrogen protects against cellular infiltration by reducing the expressions of E-selectin and IL-6 in endotoxin-induced uveitis. J. Immunol. 163:374-379.
29. Moggs, J. G., and G. Orphanides. 2001. Estrogen receptors: orchestrators of pleiotropic cellular responses. EMBO Rep. 2:775-781.
30. Nissen, R. M., and K. R. Yamamoto. 2000. The glucocorticoid receptor inhibits NFkappaB by interfering with serine-2 phosphorylation of the RNA polymerase II carboxy-terminal domain. Genes Dev. 14:2314-2329.
31. Polanczyk, M., A. Zamora, S. Subramanian, A. Matejuk, D. L. Hess, E. P. Blankenhorn, C. Teuscher, A. A. Vandenbark, and H. Offner. 2003. The protective effect of 17beta-estradiol on experimental autoimmune encephalomyelitis is mediated through estrogen receptor-alpha. Am. J. Pathol. 163:1599-1605.
32. 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.
33. Rosette, C., and M. Karin. 1995. Cytoskeletal control of gene expression: depolymerization of microtubules activates NF-kappa B. J. Cell Biol. 128:1111-1119.
34. Rossi, A., P. Kapahi, G. Natoli, T. Takahashi, Y. Chen, M. Karin, and M. G. Santoro. 2000. Anti-inflammatory cyclopentenone prostaglandins are direct inhibitors of IkappaB kinase. Nature 403:103-108.
35. Saccani, S., S. Pantano, and G. Natoli. 2001. Two waves of nuclear factor kappaB recruitment to target promoters. J. Exp. Med. 193:1351-1359.
36. Scheinman, R. I., P. C. Cogswell, A. K. Lofquist, and A. S. Baldwin, Jr. 1995. Role of transcriptional activation of I kappa B alpha in mediation of immunosuppression by glucocorticoids. Science 270:283-286.
37. Scheinman, R. I., A. Guadalberto, C. M. Jewell, J. A. Cidlowski, and A. S. Baldwin. 1995. Characterization of mechanisms involved in transrepression of NF-κB by activated glucocorticoid receptors. Mol. Cell. Biol. 15:943-953.
38. Simoncini, T., A. H. Moghadam, D. P. Brazil, K. Ley, W. W. Chin, and J. K. Liao. 2000. Interaction of estrogen receptor with the regulatory subunit of phosphatidylinositol-3-OH kinase. Nature 407:538-541.
39. Tam, W. F., L. H. Lee, L. Davis, and R. Sen. 2000. Cytoplasmic sequestration of Rel proteins by IκBα requires CRM1-dependent nuclear export. Mol. Cell. Biol. 20:2269-2284.
40. Valentine, J. E., E. Kalkhoven, R. White, S. Hoare, and M. G. Parker. 2000. Mutations in the estrogen receptor ligand binding domain discriminate between hormone-dependent transactivation and transrepression. J. Biol. Chem. 275:25322-25329.
41. Vegeto, E., S. Ghisletti, C. Meda, S. Etteri, S. Belcredito, and A. Maggi. 2004. Regulation of the lipopolysaccharide signal transduction pathway by 17beta-estradiol in macrophage cells. J. Steroid Biochem. Mol. Biol. 91:59-66.
42. 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-alpha mediates the brain antiinflammatory activity of estradiol. Proc. Natl. Acad. Sci. USA 100:9614-9619.
43. 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.
44. Vegeto, E., G. Pollio, C. Pellicciari, and A. Maggi. 1999. Estrogen and progesterone induction of survival of monoblastoid cells undergoing TNF-alpha-induced apoptosis. FASEB J. 13:793-803.
45. Wahl, C., S. Liptay, G. Adler, and R. M. Schmid. 1998. Sulfasalazine: a potent and specific inhibitor of nuclear factor kappa B. J. Clin. Investig. 101:1163-1174.
46. Yamamoto, Y., M. J. Yin, K. M. Lin, and R. B. Gaynor. 1999. Sulindac inhibits activation of the NF-kappaB pathway. J. Biol. Chem. 274:27307-27314.
47. Yin, M. J., Y. Yamamoto, and R. B. Gaynor. 1998. The anti-inflammatory agents aspirin and salicylate inhibit the activity of I(kappa)B kinase-beta. Nature 396:77-80.