Estrogen receptors regulate an inflammatory pathway of dendritic cell differentiation: Mechanisms and implications for immunity

Hormones and Behavior

Volumn 62, Issue 3, 2012, Pages 254-262

  Kovats, Susan ^a  

^a OKLAHOMA MEDICAL RESEARCH FOUNDATION   (United States)

Author keywords

Antigen presenting cells; Cellular differentiation; Dendritic cells; Estrogen; Estrogen receptor; Hematopoiesis; Immunoendocrinology; Inflammation; SERM; Sex hormone

Indexed keywords

CD11B ANTIGEN; ESTRADIOL; ESTROGEN RECEPTOR; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; FLT3 LIGAND; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERFERON REGULATORY FACTOR 4; SELECTIVE ESTROGEN RECEPTOR MODULATOR;

ADAPTIVE IMMUNITY; ANTIGEN PRESENTING CELL; B LYMPHOCYTE ACTIVATION; CELL DIFFERENTIATION; CELL INTERACTION; CELL PROLIFERATION; CELL STIMULATION; CYTOKINE PRODUCTION; DENDRITIC CELL; HOMEOSTASIS; HUMAN; IMMUNE RESPONSE; IMMUNOREGULATION; IN VIVO STUDY; INNATE IMMUNITY; MOLECULAR DYNAMICS; MYELOID PROGENITOR CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION;

ANIMALS; CELL DIFFERENTIATION; DENDRITIC CELLS; IMMUNE SYSTEM; INFLAMMATION; RECEPTORS, ESTROGEN; SIGNAL TRANSDUCTION;

EID: 84866744758     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2012.04.011     Document Type: Review

References (87)

1. Askanase A.D., Buyon J.P. Reproductive health in SLE. Best Pract. Res. Clin. Rheumatol. 2002, 16:265-280.
2. Ballesteros-Tato A., Leon B., Lund F.E., Randall T.D. Temporal changes in dendritic cell subsets, cross-priming and costimulation via CD70 control CD8(+) T cell responses to influenza. Nat. Immunol. 2010, 11:216-224.
3. Behjati S., Frank M.H. The effects of tamoxifen on immunity. Curr. Med. Chem. 2009, 16:3076-3080.
4. Berghofer B., Frommer T., Haley G., Fink L., Bein G., Hackstein H. TLR7 ligands induce higher IFN-alpha production in females. J. Immunol. 2006, 177:2088-2096.
5. Berthois Y., Katzenellenbogen J.A., Katzenellenbogen B.S. Phenol red in tissue culture media is a weak estrogen: implications concerning the study of estrogen-responsive cells in culture. Proc. Natl. Acad. Sci. U. S. A. 1986, 83:2496-2500.
6. Bosschaerts T., Guilliams M., Stijlemans B., Morias Y., Engel D., Tacke F., Herin M., De Baetselier P., Beschin A. Tip-DC development during parasitic infection is regulated by IL-10 and requires CCL2/CCR2, IFN-gamma and MyD88 signaling. PLoS Pathog. 2010, 6:e1001045.
7. Carreras E., Turner S., Paharkova-Vatchkova V., Mao A., Dascher C., Kovats S. Estradiol acts directly on bone marrow myeloid progenitors to differentially regulate GM-CSF or Flt3 ligand-mediated dendritic cell differentiation. J. Immunol. 2008, 180:727-738.
8. Carreras E., Turner S., Frank M.B., Knowlton N., Osban J., Centola M., Park C.G., Simmons A., Alberola-Ila J., Kovats S. Estrogen receptor signaling promotes dendritic cell differentiation by increasing expression of the transcription factor IRF4. Blood 2010, 115:238-246.
9. Cunningham M., Gilkeson G. Estrogen receptors in immunity and autoimmunity. Clin. Rev. Allergy Immunol. 2011, 40:66-73.
10. Dakic A., Wu L., Nutt S.L. Is PU.1 a dosage-sensitive regulator of haemopoietic lineage commitment and leukaemogenesis?. Trends Immunol. 2007, 28:108-114.
11. Douin-Echinard V., Laffont S., Seillet C., Delpy L., Krust A., Chambon P., Gourdy P., Arnal J.F., Guery J.C. Estrogen receptor alpha, but not beta, is required for optimal dendritic cell differentiation and [corrected] CD40-induced cytokine production. J. Immunol. 2008, 180:3661-3669.
12. Du S., Sandoval F., Trinh P., Umeda E., Voskuhl R. Estrogen receptor-beta ligand treatment modulates dendritic cells in the target organ during autoimmune demyelinating disease. Eur. J. Immunol. 2011, 41:140-150.
13. Dutertre M., Smith C.L. Molecular mechanisms of selective estrogen receptor modulator (SERM) action. J. Pharmacol. Exp. Ther. 2000, 295:431-447.
14. Escribese M.M., Kraus T., Rhee E., Fernandez-Sesma A., Lopez C.B., Moran T.M. Estrogen inhibits dendritic cell maturation to RNA viruses. Blood 2008, 112:4574-4584.
15. Fish E.N. The X-files in immunity: sex-based differences predispose immune responses. Nat. Rev. Immunol. 2008, 8:737-744.
16. Fogg D.K., Sibon C., Miled C., Jung S., Aucouturier P., Littman D.R., Cumano A., Geissmann F. A clonogenic bone marrow progenitor specific for macrophages and dendritic cells. Science 2006, 311:83-87.
17. Foster H.L., Small J.D., Fox J.G. Normative Biology, Immunology and Husbandry 1983, Academic Press Inc., Orlando, FL.
18. Franchi L., Eigenbrod T., Munoz-Planillo R., Nunez G. The inflammasome: a caspase-1-activation platform that regulates immune responses and disease pathogenesis. Nat. Immunol. 2009, 10:241-247.
19. Frasor J., Danes J.M., Komm B., Chang K.C., Lyttle C.R., Katzenellenbogen B.S. Profiling of estrogen up- and down-regulated gene expression in human breast cancer cells: insights into gene networks and pathways underlying estrogenic control of proliferation and cell phenotype. Endocrinology 2003, 144:4562-4574.
20. Geissmann F., Manz M.G., Jung S., Sieweke M.H., Merad M., Ley K. Development of monocytes, macrophages, and dendritic cells. Science 2010, 327:656-661.
21. Grumont R.J., Gerondakis S. Rel induces interferon regulatory factor 4 (IRF-4) expression in lymphocytes: modulation of interferon-regulated gene expression by rel/nuclear factor kappaB. J. Exp. Med. 2000, 191:1281-1292.
22. Hamilton J.A. GM-CSF in inflammation and autoimmunity. Trends Immunol. 2002, 23:403-408.
23. Hamilton J.A. Colony-stimulating factors in inflammation and autoimmunity. Nat. Rev. Immunol. 2008, 8:533-544.
24. Harman B.C., Miller J.P., Nikbakht N., Gerstein R., Allman D. Mouse plasmacytoid dendritic cells derive exclusively from estrogen-resistant myeloid progenitors. Blood 2006, 108:878-885.
25. Hashimoto D., Miller J., Merad M. Dendritic cell and macrophage heterogeneity in vivo. Immunity 2011, 35:323-335.
26. Heldring N., Pike A., Andersson S., Matthews J., Cheng G., Hartman J., Tujague M., Strom A., Treuter E., Warner M., Gustafsson J.A. Estrogen receptors: how do they signal and what are their targets. Physiol. Rev. 2007, 87:905-931.
27. Helft J., Ginhoux F., Bogunovic M., Merad M. Origin and functional heterogeneity of non-lymphoid tissue dendritic cells in mice. Immunol. Rev. 2010, 234:55-75.
28. Hesske L., Vincenzetti C., Heikenwalder M., Prinz M., Reith W., Fontana A., Suter T. Induction of inhibitory central nervous system-derived and stimulatory blood-derived dendritic cells suggests a dual role for granulocyte-macrophage colony-stimulating factor in central nervous system inflammation. Brain 2010, 133:1637-1654.
29. Hughes G.C., Clark E.A. Regulation of dendritic cells by female sex steroids: relevance to immunity and autoimmunity. Autoimmunity 2007, 40:470-481.
30. Igarashi H., Kouro T., Yokota T., Comp P.C., Kincade P.W. Age and stage dependency of estrogen receptor expression by lymphocyte precursors. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:15131-15136.
31. Inaba K., Inaba M., Romani N., Aya H., Deguchi M., Ikehara S., Muramatsu S., Steinman R.M. Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor. J. Exp. Med. 1992, 176:1693-1702.
32. Jakubzick C., Bogunovic M., Bonito A.J., Kuan E.L., Merad M., Randolph G.J. Lymph-migrating, tissue-derived dendritic cells are minor constituents within steady-state lymph nodes. J. Exp. Med. 2008, 205:2839-2850.
33. Kalaitzidis D., Gilmore T.D. Transcription factor cross-talk: the estrogen receptor and NF-kappaB. Trends Endocrinol. Metab. 2005, 16:46-52.
34. Kawai T., Akira S. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat. Immunol. 2010, 11:373-384.
35. Kincade P.W., Medina K.L., Payne K.J., Rossi M.I., Tudor K.S., Yamashita Y., Kouro T. Early B-lymphocyte precursors and their regulation by sex steroids. Immunol. Rev. 2000, 175:128-137.
36. King I.L., Dickendesher T.L., Segal B.M. Circulating Ly-6C+ myeloid precursors migrate to the CNS and play a pathogenic role during autoimmune demyelinating disease. Blood 2009, 113:3190-3197.
37. Klein S.L., Hodgson A., Robinson D.P. Mechanisms of sex disparities in influenza pathogenesis 2011, J Leukoc Biol, (published online Nov. 30, 2011; [Electronic publication ahead of print]).
38. Komi J., Lassila O. Nonsteroidal anti-estrogens inhibit the functional differentiation of human monocyte-derived dendritic cells. Blood 2000, 95:2875-2882.
39. Komi J., Mottonen M., Luukkainen R., Lassila O. Non-steroidal anti-oestrogens inhibit the differentiation of synovial macrophages into dendritic cells. Rheumatology 2001, 185-191.
40. Kovats S., Carreras E. Regulation of dendritic cell differentiation and function by estrogen receptor ligands. Cell. Immunol. 2008, 252:81-90.
41. Kovats S., Carreras E., Agrawal H. Sex steroid receptors in immune cells. Sex Hormones and Immunity to Infection 2010, 53-91. Springer. S.L. Klein, C.W. Roberts (Eds.).
42. Laouar Y., Welte T., Fu X.Y., Flavell R.A. STAT3 is required for Flt3L-dependent dendritic cell differentiation. Immunity 2003, 19:903-912.
43. Laslo P., Spooner C.J., Warmflash A., Lancki D.W., Lee H.J., Sciammas R., Gantner B.N., Dinner A.R., Singh H. Multilineage transcriptional priming and determination of alternate hematopoietic cell fates. Cell 2006, 126:755-766.
44. Lehtonen A., Veckman V., Nikula T., Lahesmaa R., Kinnunen L., Matikainen S., Julkunen I. Differential expression of IFN regulatory factor 4 gene in human monocyte-derived dendritic cells and macrophages. J. Immunol. 2005, 175:6570-6579.
45. Leitman D.C., Paruthiyil S., Vivar O.I., Saunier E.F., Herber C.B., Cohen I., Tagliaferri M., Speed T.P. Regulation of specific target genes and biological responses by estrogen receptor subtype agonists. Curr. Opin. Pharmacol. 2010, 10:629-636.
46. Liu K., Victora G.D., Schwickert T.A., Guermonprez P., Meredith M.M., Yao K., Chu F.F., Randolph G.J., Rudensky A.Y., Nussenzweig M. In vivo analysis of dendritic cell development and homeostasis. Science 2009, 324:392-397.
47. Lyman S.D., Jacobsen S.E. c-kit ligand and Flt3 ligand: stem/progenitor cell factors with overlapping yet distinct activities. Blood 1998, 91:1101-1134.
48. Mann M., Cortez V., Vadlamudi R.K. Epigenetics of estrogen receptor signaling: role in hormonal cancer progression and therapy. Cancers (Basel) 2011, 3:1691-1707.
49. Mao A., Paharkova-Vatchkova V., Hardy J., Miller M.M., Kovats S. Estrogen selectively promotes the differentiation of dendritic cells with characteristics of Langerhans cells. J. Immunol. 2005, 175:5146-5151.
50. Marecki S., Fenton M.J. The role of IRF-4 in transcriptional regulation. J. Interferon Cytokine Res. 2002, 22:121-133.
51. Medina K.L., Garrett K.P., Thompson L.F., Rossi M.I., Payne K.J., Kincade P.W. Identification of very early lymphoid precursors in bone marrow and their regulation by estrogen. Nat. Immunol. 2001, 2:718-724.
52. Meier A., Chang J.J., Chan E.S., Pollard R.B., Sidhu H.K., Kulkarni S., Wen T.F., Lindsay R.J., Orellana L., Mildvan D., Bazner S., Streeck H., Alter G., Lifson J.D., Carrington M., Bosch R.J., Robbins G.K., Altfeld M. Sex differences in the Toll-like receptor-mediated response of plasmacytoid dendritic cells to HIV-1. Nat. Med. 2009, 15:955-959.
53. Mellman I., Steinman R.M. Dendritic cells: specialized and regulated antigen processing machines. Cell 2001, 106:255-258.
54. Merad M., Manz M.G. Dendritic cell homeostasis. Blood 2009, 113:3418-3427.
55. Mor G., Sapi E., Abrahams V.M., Rutherford T., Song J., Hao X.Y., Muzaffar S., Kohen F. Interaction of the estrogen receptors with the Fas ligand promoter in human monocytes. J. Immunol. 2003, 170:114-122.
56. Moro J.R., Iwata M., von Andriano U.H. Vitamin effects on the immune system: vitamins A and D take centre stage. Nat. Rev. Immunol. 2008, 8:685-698.
57. Mouchemore K.A., Pixley F.J. CSF-1 signaling in macrophages: pleiotrophy through phosphotyrosine-based signaling pathways. Crit. Rev. Clin. Lab. Sci. 2012, 49:49-61.
58. Naik S.H., Proietto A.I., Wilson N.S., Dakic A., Schnorrer P., Fuchsberger M., Lahoud M.H., O'Keeffe M., Shao Q.X., Chen W.F., Villadangos J.A., Shortman K., Wu L. Cutting edge: generation of splenic CD8+ and CD8- dendritic cell equivalents in Fms-like tyrosine kinase 3 ligand bone marrow cultures. J. Immunol. 2005, 174:6592-6597.
59. Nakano H., Lin K.L., Yanagita M., Charbonneau C., Cook D.N., Kakiuchi T., Gunn M.D. Blood-derived inflammatory dendritic cells in lymph nodes stimulate acute T helper type 1 immune responses. Nat. Immunol. 2009, 10:394-402.
60. Nalbandian G., Paharkova-Vatchkova V., Mao A., Nale S., Kovats S. The selective estrogen receptor modulators, tamoxifen and raloxifene, impair dendritic cell differentiation and activation. J. Immunol. 2005, 175:2666-2675.
61. O'Lone R., Frith M.C., Karlsson E.K., Hansen U. Genomic targets of nuclear estrogen receptors. Mol. Endocrinol. 2004, 18:1859-1875.
62. Olsen N.J., Kovacs W.J. Gonadal steroids and immunity. Endocr. Rev. 1996, 17:369-384.
63. Paharkova-Vatchkova V., Maldonado R., Kovats S. Estrogen preferentially promotes the differentiation of CD11c+ CD11b(intermediate) dendritic cells from bone marrow precursors. J. Immunol. 2004, 172:1426-1436.
64. Papenfuss T.L., Powell N.D., McClain M.A., Bedarf A., Singh A., Gienapp I.E., Shawler T., Whitacre C.C. Estriol generates tolerogenic dendritic cells in vivo that protect against autoimmunity. J. Immunol. 2011, 186:3346-3355.
65. Phiel K.L., Henderson R.A., Adelman S.J., Elloso M.M. Differential estrogen receptor gene expression in human peripheral blood mononuclear cell populations. Immunol. Lett. 2005, 97:107-113.
66. Rathinam V.A., Fitzgerald K.A. Cytosolic surveillance and antiviral immunity. Curr. Opin. Virol. 2011, 1:455-462.
67. Relloso M., Aragoneses-Fenoll L., Lasarte S., Bourgeois C., Romera G., Kuchler K., Corbi A.L., Munoz-Fernandez M.A., Nombela C., Rodriguez-Fernandez J.L., Diez-Orejas R. Estradiol impairs the Th17 immune response against Candida albicans. J. Leukoc. Biol. 2012, 91:159-165.
68. Sathe P., Wu L. The network of cytokines, receptors and transcription factors governing the development of dendritic cell subsets. Protein Cell 2011, 2:620-630.
69. Schmid M.A., Kingston D., Boddupalli S., Manz M.G. Instructive cytokine signals in dendritic cell lineage commitment. Immunol. Rev. 2010, 234:32-44.
70. Schmid M.A., Takizawa H., Baumjohann D.R., Saito Y., Manz M.G. Bone marrow dendritic cell progenitors sense pathogens via Toll-like receptors and subsequently migrate to inflamed lymph nodes. Blood 2011, 118:4829-4840.
71. Sciammas R., Shaffer A.L., Schatz J.H., Zhao H., Staudt L.M., Singh H. Graded expression of interferon regulatory factor-4 coordinates isotype switching with plasma cell differentiation. Immunity 2006, 25:225-236.
72. Segura E., Valladeau-Guilemond J., Donnadieu M.H., Sastre-Garau X., Soumelis V., Amigorena S. Characterization of resident and migratory dendritic cells in human lymph nodes. J. Exp. Med. 2012, 209:653-660.
73. Seillet C., Laffont S., Tremollieres F., Rouquie N., Ribot C., Arnal J.F., Douin-Echinard V., Gourdy P., Guery J.C. The TLR-mediated response of plasmacytoid dendritic cells is positively regulated by estradiol in vivo through cell-intrinsic estrogen receptor alpha signaling. Blood 2012, 119:454-464.
74. Serbina N.V., Salazar-Mather T.P., Biron C.A., Kuziel W.A., Pamer E.G. TNF/iNOS-producing dendritic cells mediate innate immune defense against bacterial infection. Immunity 2003, 19:59-70.
75. Serbina N.V., Jia T., Hohl T.M., Pamer E.G. Monocyte-mediated defense against microbial pathogens. Annu. Rev. Immunol. 2008, 26:421-452.
76. Shi C., Pamer E.G. Monocyte recruitment during infection and inflammation. Nat. Rev. Immunol. 2011, 11:762-774.
77. Shortman K., Naik S.H. Steady-state and inflammatory dendritic-cell development. Nat. Rev. Immunol. 2007, 7:19-30.
78. Siracusa M.C., Overstreet M.G., Housseau F., Scott A.L., Klein S.L. 17{beta}-Estradiol alters the activity of conventional and IFN-producing killer dendritic cells. J. Immunol. 2008, 180:1423-1431.
79. Straub R.H. The complex role of estrogens in inflammation. Endocr. Rev. 2007, 28:521-574.
80. Suzuki S., Honma K., Matsuyama T., Suzuki K., Toriyama K., Akitoyo I., Yamamoto K., Suematsu T., Nakamura M., Yui K., Kumatori A. Critical roles of interferon regulatory factor 4 in CD11bhighCD8alpha-dendritic cell development. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:8981-8986.
81. Tamura T., Tailor P., Yamaoka K., Kong H.J., Tsujimura H., O'Shea J.J., Singh H., Ozato K. IFN regulatory factor-4 and -8 govern dendritic cell subset development and their functional diversity. J. Immunol. 2005, 174:2573-2581.
82. van de Laar L., Coffer P.J., Woltman A.M. Regulation of dendritic cell development by GM-CSF: molecular control and implications for immune homeostasis and therapy. Blood 2012, 119:3383-3393.
83. Varol C., Yona S., Jung S. Origins and tissue-context-dependent fates of blood monocytes. Immunol. Cell Biol. 2009, 87:30-38.
84. Welner R.S., Pelayo R., Garrett K.P., Chen X., Perry S.S., Sun X.H., Kee B.L., Kincade P.W. Interferon-producing killer dendritic cells (IKDCs) arise via a unique differentiation pathway from primitive c-kitHiCD62L+ lymphoid progenitors. Blood 2007, 109:4825-4931.
85. Whitacre C.C. Sex differences in autoimmune disease. Nat. Immunol. 2001, 2:777-780.
86. Zhan Y., Lieschke G.J., Grail D., Dunn A.R., Cheers C. Essential roles for granulocyte-macrophage colony-stimulating factor (GM-CSF) and G-CSF in the sustained hematopoietic response of Listeria monocytogenes-infected mice. Blood 1998, 91:863-869.
87. Zhang Q.H., Hu Y.Z., Cao J., Zhong Y.Q., Zhao Y.F., Mei Q.B. Estrogen influences the differentiation, maturation and function of dendritic cells in rats with experimental autoimmune encephalomyelitis. Acta Pharmacol. Sin. 2004, 25:508-513.