Estrogen receptor α regulates tripartite motif-containing protein 21 expression, contributing to dysregulated cytokine production in systemic lupus erythematosus

Arthritis and Rheumatology

Volumn 66, Issue 1, 2014, Pages 163-172

  Smith, Siobhán ^a   Nígabhann, Joan ^a   McCarthy, Eoghan ^a   Coffey, Barbara ^a   Mahony, Rebecca ^a   Byrne, Jennifer C ^a   Stacey, Kevin ^a   Ball, Elizabeth ^b   Bell, Aubrey ^b   Cunnane, Gaye ^c   Doran, Michele F ^c   Molloy, Eamonn S ^d   Lee, Ruth Z ^e   Harvey, Brian ^e   Kearns, Grainne ^e   Jefferies, Caroline A ^a  

^a ROYAL COLLEGE OF SURGEONS IN IRELAND   (Ireland)

^b BELFAST CITY HOSPITAL   (United Kingdom)

^c ST JAMES S HOSPITAL   (Ireland)

^d ST VINCENT S UNIVERSITY HOSPITAL   (Ireland)

^e BEAUMONT HOSPITAL   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIESTROGEN; AUTOANTIGEN; BETA INTERFERON; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; CYCLIC AMP RESPONSIVE ELEMENT MODULATOR; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON REGULATORY FACTOR 3; INTERLEUKIN 23; METHYL PIPERIDINO PYRAZOLE DIHYDROCHLORIDE; TRIPARTITE MOTIF CONTAINING PROTEIN 21; UNCLASSIFIED DRUG; CREM PROTEIN, HUMAN; CYTOKINE; RIBONUCLEOPROTEIN; SS A ANTIGEN; SS-A ANTIGEN;

ADULT; ARTICLE; BINDING SITE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; ESTROGEN RESPONSIVE ELEMENT; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IMMUNE DYSREGULATION; KERATINOCYTE; MOLECULAR PATHOLOGY; MONOCYTE; PATHOGENESIS; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; RECEPTOR BINDING; REGULATORY MECHANISM; SYSTEMIC LUPUS ERYTHEMATOSUS; WESTERN BLOTTING; BIOSYNTHESIS; CASE CONTROL STUDY; CELL CULTURE; DNA RESPONSIVE ELEMENT; DRUG ANTAGONISM; GENE EXPRESSION REGULATION; GENETICS; MALE; METABOLISM; MIDDLE AGED; PHYSIOLOGY; YOUNG ADULT;

ADULT; AUTOANTIGENS; CASE-CONTROL STUDIES; CELLS, CULTURED; CHROMATIN IMMUNOPRECIPITATION; CYCLIC AMP RESPONSE ELEMENT MODULATOR; CYTOKINES; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; FEMALE; GENE EXPRESSION REGULATION; HUMANS; LUPUS ERYTHEMATOSUS, SYSTEMIC; MALE; MIDDLE AGED; MONOCYTES; PROMOTER REGIONS, GENETIC; REAL-TIME POLYMERASE CHAIN REACTION; RESPONSE ELEMENTS; RIBONUCLEOPROTEINS; YOUNG ADULT;

EID: 84897019249     PISSN: 23265191     EISSN: 23265205     Source Type: Journal    
DOI: 10.1002/art.38187     Document Type: Article

References (48)

1. Tenbrock K, Juang YT, Kyttaris VC, Tsokos GC. Altered signal transduction in SLE T cells. Rheumatology (Oxford) 2007;46:1525-30. (Pubitemid 47500564)
2. Zhang J, Jacobi AM, Wang T, Berlin R, Volpe BT, Diamond B. Polyreactive autoantibodies in systemic lupus erythematosus have pathogenic potential. J Autoimmun 2009;33:270-4.
3. Salmon JE, Kimberly RP, Gibofsky A, Fotino M. Defective mononuclear phagocyte function in systemic lupus erythematosus: dissociation of Fcreceptor-ligand binding and internalization. J Immunol 1984;133:2525-31. (Pubitemid 15204779)
4. Cervera R, Khamashta MA, Font J, Sebastiani GD, Gil A, Lavilla P, et al, the European Working Party on Systemic Lupus Erythematosus. Systemic lupus erythematosus: clinical and immunologic patterns of disease expression in a cohort of 1, 000 patients. Medicine (Baltimore) 1993;72:113-24. (Pubitemid 23097765)
5. Jungers P, Dougados M, Pelissier C, Kuttenn F, Tron F, Lesavre P, et al. Influence of oral contraceptive therapy on the activity of systemic lupus erythematosus. Arthritis Rheum 1982;25:618-23. (Pubitemid 12078974)
6. Doria A, Iaccarino L, Sarzi-Puttini P, Ghirardello A, Zampieri S, Arienti S, et al. Estrogens in pregnancy and systemic lupus erythematosus. Ann N Y Acad Sci 2006;1069:247-56. (Pubitemid 43989867)
7. Carlsten H, Tarkowski A, Holmdahl R, Nilsson LA. Oestrogen is a potent disease accelerator in SLE-prone MRL lpr/lpr mice. Clin Exp Immun 1990;80:467-73. (Pubitemid 20180346)
8. Petri M, Kim MY, Kalunian KC, Grossman J, Hahn BH, Sammaritano LR, et al. Combined oral contraceptives in women with systemic lupus erythematosus. N Engl J Med 2005;353:2550-8. (Pubitemid 41785892)
9. Sanchez-Guerrero J, Uribe AG, Jimenez-Santana L, Mestanza-Peralta M, Lara-Reyes P, Seuc AH, et al. A trial of contraceptive methods in women with systemic lupus erythematosus. N Engl J Med 2005;353:2539-49. (Pubitemid 41785891)
10. Costenbader KH, Feskanich D, Stampfer MJ, Karlson EW. Reproductive and menopausal factors and risk of systemic lupus erythematosus in women. Arthritis Rheum 2007;56:1251-62. (Pubitemid 46608650)
11. Svenson JL, EuDaly J, Ruiz P, Korach KS, Gilkeson GS. Impact of estrogen receptor deficiency on disease expression in the NZM2410 lupus prone mouse. Clin Immunol 2008;128:259-68.
12. Paech K, Webb P, Kuiper GG, Nilsson S, Gustafsson JA, Kushner PJ, et al. Differential ligand activation of estrogen receptors ERα and ERβ at AP1 sites. Science 1997;277:1508-10. (Pubitemid 27449239)
13. McKay LI, Cidlowski JA. Cross-talk between nuclear factor-κB and the steroid hormone receptors: mechanisms of mutual antagonism. Mol Endocrinol 1998;12:45-56. (Pubitemid 28124778)
14. Colasanti T, Maselli A, Conti F, Sanchez M, Alessandri C, Barbati C, et al. Autoantibodies to estrogen receptor α interfere with T lymphocyte homeostasis and are associated with disease activity in systemic lupus erythematosus. Arthritis Rheum 2012;64:778-87.
15. Inui A, Ogasawara H, Naito T, Sekigawa I, Takasaki Y, Hayashida Y, et al. Estrogen receptor expression by peripheral blood mononuclear cells of patients with systemic lupus erythematosus. Clin Rheumatol 2007;26:1675-8.
16. Shen H, Panchanathan R, Rajavelu P, Duan X, Gould KA, Choubey D. Gender-dependent expression of murine IRF5 gene: implications for sex bias in autoimmunity. J Mol Cell Biol 2010;2:284-90.
17. Panchanathan R, Choubey D. Murine BAFF expression is upregulated by estrogen and interferons: implications for sex bias in the development of autoimmunity. Mol Immunol 2013;53:15-23.
18. Panchanathan R, Shen H, Bupp MG, Gould KA, Choubey D. Female and male sex hormones differentially regulate expression of Ifi202, an interferon-inducible lupus susceptibility gene within the Nba2 interval. J Immunol 2009;183:7031-8.
19. Ward J, Rider V, Abdou N, Kimler B. Estradiol differentially regulates calreticulin: a potential link with abnormal T cell function in systemic lupus erythematosus? Lupus 2013;22:583-96.
20. Moulton VR, Holcomb DR, Zajdel MC, Tsokos GC. Estrogen upregulates cyclic AMP response element modulator α expression and downregulates interleukin-2 production by human T lymphocytes. Mol Med 2012;18:370-8.
21. Li X, Xu Y, Ma L, Sun L, Fu G, Hou Y. 17β-estradiol enhances the response of plasmacytoid dendritic cell to CpG. PLoS One 2009;4:e8412.
22. Siracusa MC, Overstreet MG, Housseau F, Scott AL, Klein SL. 17β-estradiol alters the activity of conventional and IFN-producing killer dendritic cells. J Immunol 2008;180:1423-31.
23. Higgs R, NíGabhann J, Larbi NB, Breen EP, Fitzgerald KA, Jefferies CA. The E3 ubiquitin ligase Ro52 negatively regulates IFNβ production post-pathogen recognition by polyubiquitinmediated degradation of IRF3. J Immunol 2008;181:1780-6.
24. Espinosa A, Dardalhon V, Brauner S, Ambrosi A, Higgs R, Quintana FJ, et al. Loss of the lupus autoantigen Ro52/Trim21 induces tissue inflammation and systemic autoimmunity by disregulating the IL-23-Th17 pathway. J Exp Med 2009;206:1661-71.
25. Smith S, NíGabhann J, Higgs R, Stacey K, Wahren-Herlenius M, Espinosa A, et al. Enhanced interferon regulatory factor 3 binding to the interleukin-23p19 promoter correlates with enhanced interleukin-23 expression in systemic lupus erythematosus. Arthritis Rheum 2012;64:1601-9.
26. Kim JY, Ozato K. The sequestosome 1/p62 attenuates cytokine gene expression in activated macrophages by inhibiting IFN regulatory factor 8 and TNF receptor-associated factor 6/NF-κB activity. J Immunol 2009;182:2131-40.
27. Espinosa A, Zhou W, Ek M, Hedlund M, Brauner S, Popovic K, et al. The Sjögren's syndrome-associated autoantigen Ro52 is an E3 ligase that regulates proliferation and cell death. J Immunol 2006;176:6277-85.
28. Tan EM, Cohen AS, Fries JF, Masi AT, McShane DJ, Rothfield NF, et al. The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 1982;25:1271-7. (Pubitemid 13221242)
29. Hochberg MC, for the Diagnostic and Therapeutic Criteria Committee of the American College of Rheumatology. Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus [letter]. Arthritis Rheum 1997;40:1725.
30. Heinlen LD, McClain MT, Merrill J, Akbarali YW, Edgerton CC, Harley JB, et al. Clinical criteria for systemic lupus erythematosus precede diagnosis, and associated autoantibodies are present before clinical symptoms. Arthritis Rheum 2007;56:2344-51. (Pubitemid 47173582)
31. ΔΔCT method. Methods 2001;25:402-8. (Pubitemid 34164012)
32. Furukawa F, Lyons MB, Lee LA, Coulter SN, Norris DA. Estradiol enhances binding to cultured human keratinocytes of antibodies specific for SS-A/Ro and SS-B/La: another possible mechanism for estradiol influence of lupus erythematosus. J Immunol 1988;141:1480-8.
33. Lahita RG. The role of sex hormones in systemic lupus erythematosus. Curr Opin Rheumatol 1999;11:352-6.
34. Ahlmann M, Varga G, Sturm K, Lippe R, Benedyk K, Viemann D, et al. The cyclic AMP response element modulator α suppresses CD86 expression and APC function. J Immunol 2009;182:4167-74.
35. Bolland S, Garcia-Sastre A. Vicious circle: systemic autoreactivity in Ro52/TRIM21-deficient mice. J Exp Med 2009;206:1647-51.
36. Jefferies C, Wynne C, Higgs R. Antiviral TRIMs: friend or foe in autoimmune and autoinflammatory disease? Nat Rev Immunol 2011;11:617-25.
37. Weckerle C, Niewold T. The unexplained female predominance of systemic lupus erythematosus: clues from genetic and cytokine studies. Clin Rev Allergy Immunol 2011;40:42-9.
38. Mok CC, Lau CS, Ho CT, Wong RW. Do flares of systemic lupus erythematosus decline after menopause? Scand J Rheumatol 1999;28:357-62. (Pubitemid 30033049)
39. Hwang SH, Lee H, Yamamoto M, Jones LA, Dayalan J, Hopkins R, et al. B cell TLR7 expression drives anti-RNA autoantibody production and exacerbates disease in systemic lupus erythematosus-prone mice. J Immunol 2012;189:5786-96.
40. Christensen SR, Kashgarian M, Alexopoulou L, Flavell RA, Akira S, Shlomchik MJ. Toll-like receptor 9 controls anti-DNA autoantibody production in murine lupus. J Exp Med 2005;202:321-31. (Pubitemid 41043827)
41. Zhang Z, Bao M, Lu N, Weng L, Yuan B, Liu YJ. The E3 ubiquitin ligase TRIM21 negatively regulates the innate immune response to intracellular double-stranded DNA. Nat Immunol 2013;14:172-8.
42. Keeble AH, Khan Z, Forster A, James LC. TRIM21 is an IgG receptor that is structurally, thermodynamically, and kinetically conserved. Proc Natl Acad Sci U S A 2008;105:6045-50. (Pubitemid 351758396)
43. McEwan WA, Tam JC, Watkinson RE, Bidgood SR, Mallery DL, James LC. Intracellular antibody-bound pathogens stimulate immune signaling via the Fc receptor TRIM21. Nat Immunol 2013;14:327-36.
44. Higgs R, Lazzari E, Wynne C, NíGabhann J, Espinosa A, Wahren-Herlenius M, et al. Self protection from anti-viral responses-Ro52 promotes degradation of the transcription factor IRF7 downstream of the viral Toll-like receptors. PLoS One; 5:e11776.
45. Wu WM, Suen JL, Lin BF, Chiang BL. Tamoxifen alleviates disease severity and decreases double negative T cells in autoimmune MRL-lpr/lpr mice. Immunology 2000;100:110-8.
46. Sturgess AD, Evans DT, Mackay IR, Riglar A. Effects of the oestrogen antagonist tamoxifen on disease indices in systemic lupus erythematosus. J Clin Lab Immunol 1984;13:11-4. (Pubitemid 14177541)
47. Abdou NI, Rider V, Greenwell C, Li X, Kimler BF. Fulvestrant (Faslodex), an estrogen selective receptor downregulator, in therapy of women with systemic lupus erythematosus. Clinical, serologic, bone density, and T cell activation marker studies: a double-blind placebo-controlled trial. J Rheumatol 2008;35:797-803. (Pubitemid 351747119)
48. Lahita RG, Bradlow HL, Kunkel HG, Fishman J. Alterations of estrogen metabolism in systemic lupus erythematosus. Arthritis Rheum 1979;22:1195-8. (Pubitemid 10163784)