The TLR-mediated response of plasmacytoid dendritic cells is positively regulated by estradiol in vivo through cell-intrinsic estrogen receptor α signaling

Blood

Volumn 119, Issue 2, 2012, Pages 454-464

  Seillet, Cyril ^a,b,c   Laffont, Sophie ^a,b,c   Trémollières, Florence ^d,e,f   Rouquié, Nelly ^a,b,c   Ribot, Claude ^d,e,f   Arnal, Jean François ^d,e   Douin Echinard, Victorine ^d,e   Gourdy, Pierre ^d,e   Guéry, Jean Charles ^a,b,c,e  

^a CHU PURPAN   (France)

^b CNRS   (France)

^c France   (France)

^d University Hospital of Toulouse   (France)

^e TOULOUSE UNIVERSITY HOSPITAL   (France)

^f Paul Sabatier University   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; INTERLEUKIN 12P40; RESIQUIMOD; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 9; TUMOR NECROSIS FACTOR ALPHA;

ADULT; AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTOIMMUNE DISEASE; CELL FUNCTION; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; FEMALE; HEMATOPOIETIC SYSTEM; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VIVO CULTURE; INFECTION; MALE; MOUSE; NONHUMAN; PLASMACYTOID DENDRITIC CELL; POSTMENOPAUSE; PRIORITY JOURNAL; SEX DIFFERENCE; SIGNAL TRANSDUCTION;

EID: 84855857588     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2011-08-371831     Document Type: Article

References (50)

1. Gilliet M, Cao W, Liu YJ. Plasmacytoid dendritic cells: sensing nucleic acids in viral infection and autoimmune diseases. Nat Rev Immunol. 2008; 8(8):594-606.
2. Marshak-Rothstein A. Toll-like receptors in systemic autoimmune disease. Nat Rev Immunol. 2006;6(11):823-835. (Pubitemid 44631651)
3. Blanco P, Palucka AK, Gill M, Pascual V, Banchereau J. Induction of dendritic cell differentiation by IFN-alpha in systemic lupus erythematosus. Science. 2001;294(5546):1540-1543. (Pubitemid 33063928)
4. Barrat FJ, Coffman RL. Development of TLR inhibitors for the treatment of autoimmune diseases. Immunol Rev. 2008;223:271-283. (Pubitemid 351986175)
5. Hooks JJ, Moutsopoulos HM, Geis SA, Stahl NI, Decker JL, Notkins AL. Immune interferon in the circulation of patients with autoimmune disease. N Engl J Med. 1979;301(1):5-8. (Pubitemid 9226519)
6. Ytterberg SR, Schnitzer TJ. Serum interferon levels in patients with systemic lupus erythematosus. Arthritis Rheum. 1982;25(4):401-406. (Pubitemid 12158948)
7. Baechler EC, Batliwalla FM, Karypis G, et al. Interferon-inducible gene expression signature in peripheral blood cells of patients with severe lupus. Proc Natl Acad Sci U S A. 2003;100(5): 2610-2615. (Pubitemid 36297546)
8. Bennett L, Palucka AK, Arce E, et al. Interferon and granulopoiesis signatures in systemic lupus erythematosus blood. J Exp Med. 2003;197(6): 711-723. (Pubitemid 36350866)
9. Ioannou Y, Isenberg DA. Current evidence for the induction of autoimmune rheumatic manifestations by cytokine therapy. Arthritis Rheum. 2000; 43(7):1431-1442. (Pubitemid 30452458)
10. Mathian A, Weinberg A, Gallegos M, Banchereau J, Koutouzov S. IFN-alpha induces early lethal lupus in preautoimmune (New Zealand Black x New Zealand White) F1 but not in BALB/c mice. J Immunol. 2005;174(5):2499-2506. (Pubitemid 40279662)
11. Fairhurst AM, Mathian A, Connolly JE, et al. Systemic IFN-alpha drives kidney nephritis in B6.Sle123 mice. Eur J Immunol. 2008;38(7): 1948-1960.
12. Lopez P, Gomez J, Prado C, Gutierrez C, Suarez A. Influence of functional interleukin 10/tumor necrosis factor-alpha polymorphisms on interferon-alpha, IL-10, and regulatory T cell population in patients with systemic lupus erythematosus receiving antimalarial treatment. J Rheumatol. 2008;35(8):1559-1566.
13. Studnicka-Benke A, Steiner G, Petera P, Smolen JS. Tumour necrosis factor alpha and its soluble receptors parallel clinical disease and autoimmune activity in systemic lupus erythematosus. Br J Rheumatol. 1996;35(11): 1067-1074.
14. Aringer M, Smolen JS. The role of tumor necrosis factor-alpha in systemic lupus erythematosus. Arthritis Res Ther. 2008;10(1):202.
15. Whitacre CC. Sex differences in autoimmune disease. Nat Immunol. 2001;2(9):777-780.
16. Fish EN. The X-files in immunity: sex-based differences predispose immune responses. Nat Rev Immunol. 2008;8(9):737-744.
17. Costenbader KH, Feskanich D, Stampfer MJ, Karlson EW. Reproductive and menopausal factors and risk of systemic lupus erythematosus in women. Arthritis Rheum. 2007;56(4):1251-1262. (Pubitemid 46608650)
18. Roubinian JR, Talal N, Greenspan JS, Goodman JR, Siiteri PK. Effect of castration and sex hormone treatment on survival, anti-nucleic acid antibodies, and glomerulonephritis in NZB/NZW F1 mice. J Exp Med. 1978;147(6):1568-1583. (Pubitemid 8372952)
19. Carlsten H, Nilsson N, Jonsson R, Backman K, Holmdahl R, Tarkowski A. Estrogen accelerates immune complex glomerulonephritis but ameliorates T cell-mediated vasculitis and sialadenitis in autoimmune MRL lpr/lpr mice. Cell Immunol. 1992;144(1):190-202.
20. Farzadegan H, Hoover DR, Astemborski J, et al. Sex differences in HIV-1 viral load and progression to AIDS. Lancet. 1998;352(9139):1510-1514. (Pubitemid 28512927)
21. Gandhi M, Bacchetti P, Miotti P, Quinn TC, Veronese F, Greenblatt RM. Does patient sex affect human immunodeficiency virus levels? Clin Infect Dis. 2002;35(3):313-322. (Pubitemid 34800281)
22. Berghofer B, Frommer T, Haley G, Fink L, Bein G, Hackstein H. TLR-7 ligands induce higher IFN-alpha production in females. J Immunol. 2006; 177(4):2088-2096. (Pubitemid 44200966)
23. Meier A, Chang JJ, Chan ES, et al. Sex differences in the Toll-like receptor-mediated response of plasmacytoid dendritic cells to HIV-1. Nat Med. 2009;15(8):955-959.
24. + hematopoietic progenitors. Blood. 2003;102(9):3302-3310.
25. Dupont S, Krust A, Gansmuller A, Dierich A, Chambon P, Mark M. Effect of single and compound knockouts of estrogen receptors alpha (ERalpha) and beta (ERbeta) on mouse reproductive phenotypes. Development. 2000;127(19): 4277-4291.
26. Lelu K, Laffont S, Delpy L, et al. Estrogen receptor alpha signaling in T lymphocytes is required for estradiol-mediated inhibition of Th1 and Th17 cell differentiation and protection against experimental autoimmune encephalomyelitis. J Immunol. 2011;187(5):2386-2393.
27. Elhage R, Arnal JF, Pieraggi MT, et al. 17 betaestradiol prevents fatty streak formation in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol. 1997;17(11):2679-2684. (Pubitemid 28016008)
28. Lovgren T, Eloranta ML, Bave U, Alm GV, Ronnblom L. Induction of interferon-alpha production in plasmacytoid dendritic cells by immune complexes containing nucleic acid released by necrotic or late apoptotic cells and lupus IgG. Arthritis Rheum. 2004;50(6):1861-1872. (Pubitemid 38725099)
29. Asselin-Paturel C, Brizard G, Chemin K, et al. Type I interferon dependence of plasmacytoid dendritic cell activation and migration. J Exp Med. 2005;201(7):1157-1167. (Pubitemid 40528442)
30. Cros J, Cagnard N, Woollard K, et al. Human CD14dim monocytes patrol and sense nucleic acids and viruses via TLR-7 and TLR-8 receptors. Immunity. 2010;33(3):375-386.
31. Decalf J, Fernandes S, Longman R, et al. Plasmacytoid dendritic cells initiate a complex chemokine and cytokine network and are a viable drug target in chronic HCV patients. J Exp Med. 2007; 204(10):2423-2437. (Pubitemid 47529327)
32. Vallin H, Blomberg S, Alm GV, Cederblad B, Ronnblom L. Patients with systemic lupus erythematosus (SLE) have a circulating inducer of interferon-α (IFN-α) production acting on leucocytes resembling immature dendritic cells. Clin Exp Immunol. 1999;115(1):196-202. (Pubitemid 29030385)
33. Vallin H, Perers A, Alm GV, Ronnblom L. Anti-double-stranded DNA antibodies and immunostimulatory plasmid DNA in combination mimic the endogenous IFN-alpha inducer in systemic lupus erythematosus. J Immunol. 1999;163(11):6306-6313.
34. 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(2):727-738.
35. Caton ML, Smith-Raska MR, Reizis B. Notch-RBP-J signaling controls the homeostasis of CD8- dendritic cells in the spleen. J Exp Med. 2007;204(7):1653-1664. (Pubitemid 47048031)
36. Fogg K, Sibon C, Miled C, et al. A clonogenic bone marrow progenitor specific for macrophages and dendritic cells. Science. 2006; 311(5757):83-87. (Pubitemid 43063063)
37. 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(3):1426-1436. (Pubitemid 38116784)
38. Carreras E, Turner S, Frank MB, et al. Estrogen receptor signaling promotes dendritic cell differentiation by increasing expression of the transcription factor IRF4. Blood. 2009;115(2):238-246.
39. Douin-Echinard V, Laffont S, Seillet C, et al. Estrogen receptorα, but not β, is required for optimal dendritic cell differentiation and CD40-induced cytokine production. J Immunol. 2008;180(6): 3661-3669.
40. Liu K, Victora GD, Schwickert TA, et al. In vivo analysis of dendritic cell development and homeostasis. Science. 2009;324(5925):392-397.
41. Reizis B, Bunin A, Ghosh HS, Lewis KL, Sisirak V. Plasmacytoid dendritic cells: recent progress and open questions. Annu Rev Immunol. 2011;29:163-183.
42. Calippe B, Douin-Echinard V, Laffargue M, et al. Chronic estradiol administration in vivo promotes the proinflammatory response of macrophages to TLR4 activation: involvement of the phosphatidylinositol 3-kinase pathway. J Immunol. 2008; 180(12):7980-7988.
43. Soucy G, Boivin G, Labrie F, Rivest S. Estradiol is required for a proper immune response to bacterial and viral pathogens in the female brain. J Immunol. 2005;174(10):6391-6398. (Pubitemid 40663832)
44. Calippe B, Douin-Echinard V, Delpy L, et al. 17Beta-estradiol promotes TLR4-triggered proinflammatory mediator production through direct estrogen receptor alpha signaling in macrophages in vivo. J Immunol. 2010;185(2):1169- 1176.
45. Bynote KK, Hackenberg JM, Korach KS, Lubahn DB, Lane PH, Gould KA. Estrogen receptor-alpha deficiency attenuates autoimmune disease in (NZB x NZW)F1 mice. Genes Immun. 2008;9(2):137-152. (Pubitemid 351351656)
46. Guiducci C, Gong M, Xu Z, et al. TLR recognition of self nucleic acids hampers glucocorticoid activity in lupus. Nature. 2010;465(7300):937-941.
47. Takahashi K, Asabe S, Wieland S, et al. Plasmacytoid dendritic cells sense hepatitis C virus-infected cells, produce interferon, and inhibit infection. Proc Natl Acad Sci U S A. 2010;107(16): 7431-7436.
48. Davis GL, Alter MJ, El-Serag H, Poynard T, Jennings LW. Aging of hepatitis C virus (HCV)- infected persons in the United States: a multiple cohort model of HCV prevalence and disease progression. Gastroenterology. 2010;138(2):513-521.
49. Di Martino V, Lebray P, Myers RP, et al. Progression of liver fibrosis in women infected with hepatitis C: long-term benefit of estrogen exposure. Hepatology. 2004;40(6):1426-1433. (Pubitemid 39657018)
50. Codes L, Asselah T, Cazals-Hatem D, et al. Liver fibrosis in women with chronic hepatitis C: evidence for the negative role of the menopause and steatosis and the potential benefit of hormone replacement therapy. Gut. 2007;56(3): 390-395. (Pubitemid 46579771)