Estrogen modulation of endosome-associated toll-like receptor 8: An IFNα-independent mechanism of sex-bias in systemic lupus erythematosus

Clinical Immunology

Volumn 151, Issue 1, 2014, Pages 66-77

  Young, Nicholas A ^a,b   Wu, Lai Chu ^a,b   Burd, Craig J ^a,b   Friedman, Alexandra K ^a,b   Kaffenberger, Benjamin H ^a,b   Rajaram, Murugesan V S ^a,b   Schlesinger, Larry S ^a,b   James, Hayley ^c   Shupnik, Margaret A ^c   Jarjour, Wael N ^a,b  

^a OHIO STATE UNIVERSITY   (United States)

^b THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

^c UNIVERSITY OF VIRGINIA HEALTH SYSTEM   (United States)

Author keywords

Autoimmunity; Estrogen; Sex bias; Systemic lupus erythematosus; Toll like receptor

Indexed keywords

AUTOIMMUNITY; ESTROGEN; SEX-BIAS; SYSTEMIC LUPUS ERYTHEMATOSUS; TOLL-LIKE RECEPTOR;

ANIMALS; BINDING SITES; CELL LINE, TUMOR; CELLS, CULTURED; ENDOSOMES; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; FEMALE; GENE EXPRESSION REGULATION; HUMANS; IMIDAZOLES; IMMUNOLOGIC FACTORS; INTERFERON-ALPHA; LEUKOCYTES, MONONUCLEAR; LUPUS ERYTHEMATOSUS, SYSTEMIC; MALE; MICE; MICE, INBRED C57BL; PROTEIN BINDING; SEX FACTORS; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 8;

EID: 84893808760     PISSN: 15216616     EISSN: 15217035     Source Type: Journal    
DOI: 10.1016/j.clim.2014.01.006     Document Type: Article

References (57)

1. Hoyert D.L., Kochanek K.D., Murphy S.L. Deaths: final data for 1997. Natl. Vital Stat. Rep. 1999, 47:1-104.
2. Holmes C.B., Hausler H., Nunn P. A review of sex differences in the epidemiology of tuberculosis. Int. J. Tuberc. Lung Dis. 1998, 2:96-104.
3. Moller A.P., Sorci G., Erritzoe J. Sexual dimorphism in immune defense. Am. Nat. 1998, 152:605-619.
4. Zuk M., McKean K.A. Sex differences in parasite infections: patterns and processes. Int. J. Parasitol. 1996, 26:1009-1023.
5. Butterworth M., McClellan B., Allansmith M. Influence of sex in immunoglobulin levels. Nature 1967, 214:1224-1225.
6. Kotzin B.L. Systemic lupus erythematosus. Cell 1996, 85:303-306.
7. Zandman-Goddard G., Peeva E., Shoenfeld Y. Gender and autoimmunity. Autoimmun. Rev. 2007, 6:366-372.
8. Lockshin M.D. Sex differences in autoimmune disease. Lupus 2006, 15:753-756.
9. Tincani A. Cyclophosphamide therapy induces ovarian failure in premenopausal women affected by systemic lupus erythematosus. Clin. Exp. Rheumatol. 2001, 19:490-491.
10. Lahita R.G., Bradlow H.L., Kunkel H.G., Fishman J. Increased 16 alpha-hydroxylation of estradiol in systemic lupus erythematosus. J. Clin. Endocrinol. Metab. 1981, 53:174-178.
11. Folomeev M., Dougados M., Beaune J., Kouyoumdjian J.C., Nahoul K., Amor B., et al. Plasma sex hormones and aromatase activity in tissues of patients with systemic lupus erythematosus. Lupus 1992, 1:191-195.
12. Whitacre C.C., Reingold S.C., O'Looney P.A. A gender gap in autoimmunity. Science 1999, 283:1277-1278.
13. Rider V., Li X., Peterson G., Dawson J., Kimler B.F., Abdou N.I. Differential expression of estrogen receptors in women with systemic lupus erythematosus. J. Rheumatol. 2006, 33:1093-1101.
14. Hochberg M.C. Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum. 1997, 40:1725.
15. Young N.A., Friedman A.K., Kaffenberger B., Rajaram M.V., Birmingham D.J., Rovin B.H., et al. Novel estrogen target gene ZAS3 is overexpressed in systemic lupus erythematosus. Mol. Immunol. 2012, 54:23-31.
16. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25:402-408.
17. Schlesinger L.S. Macrophage phagocytosis of virulent but not attenuated strains of Mycobacterium tuberculosis is mediated by mannose receptors in addition to complement receptors. J. Immunol. 1993, 150:2920-2930.
18. Rajaram M.V., Ni B., Morris J.D., Brooks M.N., Carlson T.K., Bakthavachalu B., et al. Mycobacterium tuberculosis lipomannan blocks TNF biosynthesis by regulating macrophage MAPK-activated protein kinase 2 (MK2) and microRNA miR-125b. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:17408-17413.
19. Rajaram M.V., Brooks M.N., Morris J.D., Torrelles J.B., Azad A.K., Schlesinger L.S. Mycobacterium tuberculosis activates human macrophage peroxisome proliferator-activated receptor gamma linking mannose receptor recognition to regulation of immune responses. J. Immunol. 2010, 185:929-942.
20. Burd C.J., Ward J.M., Crusselle-Davis V.J., Kissling G.E., Phadke D., Shah R.R., et al. Analysis of chromatin dynamics during glucocorticoid receptor activation. Mol. Cell. Biol. 2012, 32:1805-1817.
21. Heinz S., Benner C., Spann N., Bertolino E., Lin Y.C., Laslo P., et al. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell 2010, 38:576-589.
22. Robinson J.T., Thorvaldsdottir H., Winckler W., Guttman M., Lander E.S., Getz G., et al. Integrative genomics viewer. Nat. Biotechnol. 2011, 29:24-26.
23. Komatsuda A., Wakui H., Iwamoto K., Ozawa M., Togashi M., Masai R., et al. Up-regulated expression of Toll-like receptors mRNAs in peripheral blood mononuclear cells from patients with systemic lupus erythematosus. Clin. Exp. Immunol. 2008, 152:482-487.
24. Krieg A.M., Vollmer J. Toll-like receptors 7, 8, and 9: linking innate immunity to autoimmunity. Immunol. Rev. 2007, 220:251-269.
25. Schlaepfer E., Speck R.F. TLR8 activates HIV from latently infected cells of myeloid-monocytic origin directly via the MAPK pathway and from latently infected CD4+ T cells indirectly via TNF-{alpha}. J. Immunol. 2011, 186:4314-4324.
26. Chang Z.L. Important aspects of Toll-like receptors, ligands and their signaling pathways. Inflamm. Res. 2010, 59:791-808.
27. Hewagama A., Patel D., Yarlagadda S., Strickland F.M., Richardson B.C. Stronger inflammatory/cytotoxic T-cell response in women identified by microarray analysis. Genes Immun. 2009, 10:509-516.
28. Zarember K.A., Godowski P.J. Tissue expression of human Toll-like receptors and differential regulation of Toll-like receptor mRNAs in leukocytes in response to microbes, their products, and cytokines. J. Immunol. 2002, 168:554-561.
29. Couse J.F., Korach K.S. Estrogen receptor null mice: what have we learned and where will they lead us?. Endocr. Rev. 1999, 20:358-417.
30. Panchanathan R., Shen H., Zhang X., Ho S.M., Choubey D. Mutually positive regulatory feedback loop between interferons and estrogen receptor-alpha in mice: implications for sex bias in autoimmunity. PLoS One 2010, 5:e10868.
31. Borras C., Sastre J., Garcia-Sala D., Lloret A., Pallardo F.V., Vina J. Mitochondria from females exhibit higher antioxidant gene expression and lower oxidative damage than males. Free Radic. Biol. Med. 2003, 34:546-552.
32. Whitacre C.C. Sex differences in autoimmune disease. Nat. Immunol. 2001, 2:777-780.
33. Sabry A., Sheashaa H., El-Husseini A., Mahmoud K., Eldahshan K.F., George S.K., et al. Proinflammatory cytokines (TNF-alpha and IL-6) in Egyptian patients with SLE: its correlation with disease activity. Cytokine 2006, 35:148-153.
34. Vila L.M., Molina M.J., Mayor A.M., Cruz J.J., Rios-Olivares E., Rios Z. Association of serum MIP-1alpha, MIP-1beta, and RANTES with clinical manifestations, disease activity, and damage accrual in systemic lupus erythematosus. Clin. Rheumatol. 2007, 26:718-722.
35. Scofield R.H. Genetics of systemic lupus erythematosus and Sjogren's syndrome. Curr. Opin. Rheumatol. 2009, 21:448-453.
36. Suarez-Gestal M., Calaza M., Endreffy E., Pullmann R., Ordi-Ros J., Domenico Sebastiani G., et al. Replication of recently identified systemic lupus erythematosus genetic associations: a case-control study. Arthritis Res. Ther. 2009, 11:R69.
37. Vollmer J., Tluk S., Schmitz C., Hamm S., Jurk M., Forsbach A., et al. Immune stimulation mediated by autoantigen binding sites within small nuclear RNAs involves Toll-like receptors 7 and 8. J. Exp. Med. 2005, 202:1575-1585.
38. Li J., McMurray R.W. Effects of estrogen receptor subtype-selective agonists on autoimmune disease in lupus-prone NZB/NZW F1 mouse model. Clin. Immunol. 2007, 123:219-226.
39. Lichtman E.I., Helfgott S.M., Kriegel M.A. Emerging therapies for systemic lupus erythematosus - focus on targeting interferon-alpha. Clin. Immunol. 2012, 143:210-221.
40. Chauhan S.K., Singh V.V., Rai R., Rai M., Rai G. Distinct autoantibody profiles in systemic lupus erythematosus patients are selectively associated with TLR7 and TLR9 upregulation. J. Clin. Immunol. 2013, 33:954-964.
41. Wong C.K., Wong P.T., Tam L.S., Li E.K., Chen D.P., Lam C.W. Activation profile of Toll-like receptors of peripheral blood lymphocytes in patients with systemic lupus erythematosus. Clin. Exp. Immunol. 2010, 159:11-22.
42. Li M., Zhou Y., Feng G., Su S.B. The critical role of Toll-like receptor signaling pathways in the induction and progression of autoimmune diseases. Curr. Mol. Med. 2009, 9:365-374.
43. Kono D.H., Haraldsson M.K., Lawson B.R., Pollard K.M., Koh Y.T., Du X., et al. Endosomal TLR signaling is required for anti-nucleic acid and rheumatoid factor autoantibodies in lupus. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:12061-12066.
44. Subramanian S., Tus K., Li Q.Z., Wang A., Tian X.H., Zhou J., et al. A Tlr7 translocation accelerates systemic autoimmunity in murine lupus. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:9970-9975.
45. Pisitkun P., Deane J.A., Difilippantonio M.J., Tarasenko T., Satterthwaite A.B., Bolland S. Autoreactive B cell responses to RNA-related antigens due to TLR7 gene duplication. Science 2006, 312:1669-1672.
46. Macfarlane D.E., Manzel L. Antagonism of immunostimulatory CpG-oligodeoxynucleotides by quinacrine, chloroquine, and structurally related compounds. J. Immunol. 1998, 160:1122-1131.
47. Rynes R.I. Antimalarial drugs in the treatment of rheumatological diseases. Br. J. Rheumatol. 1997, 36:799-805.
48. Doyle S.E., O'Connell R., Vaidya S.A., Chow E.K., Yee K., Cheng G. Toll-like receptor 3 mediates a more potent antiviral response than Toll-like receptor 4. J. Immunol. 2003, 170:3565-3571.
49. Duluc D., Tan F., Scotet M., Blanchard S., Fremaux I., Garo E., et al. PolyI:C plus IL-2 or IL-12 induce IFN-gamma production by human NK cells via autocrine IFN-beta. Eur. J. Immunol. 2009, 39:2877-2884.
50. Nakamura K., Deyama Y., Yoshimura Y., Suzuki K., Morita M. Toll-like receptor 3 ligand-induced antiviral response in mouse osteoblastic cells. Int. J. Mol. Med. 2007, 19:771-775.
51. Schroder K., Spille M., Pilz A., Lattin J., Bode K.A., Irvine K.M., et al. Differential effects of CpG DNA on IFN-beta induction and STAT1 activation in murine macrophages versus dendritic cells: alternatively activated STAT1 negatively regulates TLR signaling in macrophages. J. Immunol. 2007, 179:3495-3503.
52. Wagner H. Endogenous TLR, ligands and autoimmunity. Adv. Immunol. 2006, 91:159-173.
53. Ahlin E., Mathsson L., Eloranta M.L., Jonsdottir T., Gunnarsson I., Ronnblom L., et al. Autoantibodies associated with RNA are more enriched than anti-dsDNA antibodies in circulating immune complexes in SLE. Lupus 2012, 21:586-595.
54. Zandman-Goddard G., Shoenfeld Y. Infections and SLE. Autoimmunity 2005, 38:473-485.
55. Boks M.P., Derks E.M., Weisenberger D.J., Strengman E., Janson E., Sommer I.E., et al. The relationship of DNA methylation with age, gender and genotype in twins and healthy controls. PLoS One 2009, 4:e6767.
56. Hewagama A., Gorelik G., Patel D., Liyanarachchi P., McCune W.J., Somers E., et al. Overexpression of X-linked genes in T cells from women with lupus. J. Autoimmun. 2013, 41:60-71.
57. Carroll M. Innate immunity in the etiopathology of autoimmunity. Nat. Immunol. 2001, 2:1089-1090.