Autoantibodies to estrogen receptors and their involvement in autoimmune diseases and cancer

Journal of Steroid Biochemistry and Molecular Biology

Volumn 144, Issue PART B, 2014, Pages 260-267

  Ortona, Elena ^a,b   Pierdominici, Marina ^a   Berstein, Lev ^c  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^b Istituto San Raffaele   (Italy)

^c N N PETROV RESEARCH INSTITUTE OF ONCOLOGY   (Russian Federation)

Author keywords

Autoantibodies; Autoimmunity; Cancer; Estrogen; Estrogen receptors

Indexed keywords

AUTOANTIBODY; ESTROGEN; ESTROGEN RECEPTOR; TRANSCRIPTION FACTOR; TUMOR MARKER;

AUTOIMMUNE DISEASE; AUTOIMMUNITY; CELL MEMBRANE; ESTROGEN ACTIVITY; HUMAN; IMMUNOCOMPETENT CELL; LIGAND BINDING; NEOPLASM; NONHUMAN; PROTEIN LOCALIZATION; REVIEW; SIGNAL TRANSDUCTION; SYSTEMIC LUPUS ERYTHEMATOSUS; ANIMAL; BREAST TUMOR; FEMALE; IMMUNOLOGY;

ANIMALS; AUTOANTIBODIES; AUTOIMMUNE DISEASES; BREAST NEOPLASMS; FEMALE; HUMANS; RECEPTORS, ESTROGEN; TUMOR MARKERS, BIOLOGICAL;

EID: 84906840685     PISSN: 09600760     EISSN: 18791220     Source Type: Journal    
DOI: 10.1016/j.jsbmb.2014.07.004     Document Type: Review

References (149)

1. L.M. Berstein Extragonadal Estrogen Production (Role in Physiology and Pathology) 1998 Nauka Publishers St. Petersburg
2. S. Nilsson, S. Makela, E. Treuter, M. Tujague, J. Thomsen, G. Andersson, E. Enmark, K. Pettersson, M. Warner, and J.A. Gustafsson Mechanisms of estrogen action Physiol. Rev. 81 2001 1535 1565 (Pubitemid 32951806)
3. A. Borkowski, M. Gyling, C. Muquardt, J.J. Body, and G. Leclercq Estrogen-like activity of a subpopulation of natural antiestrogen receptor autoantibodies in man Endocrinology 128 1991 3283 3292
4. M. Pierdominici, and E. Ortona Estrogen impact on autoimmunity onset and progression: the paradigm of systemic lupus erythematosus Int. Trends Immun. 1 2013 24 34
5. J. Tassignon, F. Haeseleer, and A. Borkowski Natural antiestrogen receptor autoantibodies in man with estrogenic activity in mammary carcinoma cell culture: study of their mechanism of action; evidence for involvement of estrogen-like epitopes J. Clin. Endocrinol. Metab. 82 1997 3464 3470 (Pubitemid 27419106)
6. E. Enmark, and J.A. Gustafsson Oestrogen receptors - an overview J. Intern. Med. 246 1999 133 138 (Pubitemid 29378917)
7. E.V. Jensen The contribution of alternative approaches to understanding steroid hormone action Mol. Endocrinol. 19 2005 1439 1442 (Pubitemid 41002975)
8. E.V. Jensen, E.R. Desombre, T. Kawashima, T. Suzuki, K. Kyser, and P.W. Jungblut Estrogen-binding substances of target tissues Science 158 1967 529 530
9. G.G. Kuiper, E. Enmark, M. Pelto-Huikko, S. Nilsson, and J.A. Gustafsson Cloning of a novel receptor expressed in rat prostate and ovary Proc. Natl. Acad. Sci. U. S. A. 93 1996 5925 5930 (Pubitemid 26190778)
10. P. Walter, S. Green, G. Greene, A. Krust, J.M. Bornert, J.M. Jeltsch, A. Staub, E. Jensen, G. Scrace, and M. Waterfield et al. Cloning of the human estrogen receptor cDNA Proc. Natl. Acad. Sci. U. S. A. 82 1985 7889 7893 (Pubitemid 16179869)
11. P. Ascenzi, A. Bocedi, and M. Marino Structure-function relationship of estrogen receptor alpha and beta: impact on human health Mol. Aspects Med. 27 2006 299 402 (Pubitemid 44255847)
12. M. Bottner, P. Thelen, and H. Jarry Estrogen receptor beta: tissue distribution and the still largely enigmatic physiological function J. Steroid Biochem. Mol. Biol. 139 2014 245 251
13. D.J. Mangelsdorf, C. Thummel, M. Beato, P. Herrlich, G. Schutz, K. Umesono, B. Blumberg, P. Kastner, M. Mark, P. Chambon, and R.M. Evans The nuclear receptor superfamily: the second decade Cell 83 1995 835 839
14. C. Zhao, K. Dahlman-Wright, and J.A. Gustafsson Estrogen receptor beta: an overview and update Nucl. Recept. Signal. 6 2008 e003
15. H. Gronemeyer, J.A. Gustafsson, and V. Laudet Principles for modulation of the nuclear receptor superfamily Nat. Rev. Drug Discov. 3 2004 950 964 (Pubitemid 39534319)
16. N. Heldring, A. Pike, S. Andersson, J. Matthews, G. Cheng, J. Hartman, M. Tujague, A. Strom, E. Treuter, M. Warner, and J.A. Gustafsson Estrogen receptors: how do they signal and what are their targets Physiol. Rev. 87 2007 905 931 (Pubitemid 47084672)
17. E.R. Levin Extra-nuclear estrogen receptors roles in physiology: lessons from mouse models Am. J. Physiol. Endocrinol. Metab. 307 2014 E133 E140
18. E.R. Levin Plasma membrane estrogen receptors Trends Endocrinol. Metab. 20 2009 477 482
19. M.E. Mendelsohn, and R.H. Karas Rapid progress for non-nuclear estrogen receptor signaling J. Clin. Invest. 120 2010 2277 2279
20. T.C. Pappas, B. Gametchu, and C.S. Watson Membrane estrogen receptor-enriched GH(3)/B6 cells have an enhanced non-genomic response to estrogen Endocrine 3 1995 743 749
21. R.J. Pietras, and C.M. Szego Specific binding sites for oestrogen at the outer surfaces of isolated endometrial cells Nature 265 1977 69 72 (Pubitemid 8004314)
22. X. Guo, M. Razandi, A. Pedram, G. Kassab, and E.R. Levin Estrogen induces vascular wall dilation: mediation through kinase signaling to nitric oxide and estrogen receptors alpha and beta J. Biol. Chem. 280 2005 19704 19710 (Pubitemid 41379495)
23. P.G. Mermelstein Membrane-localised oestrogen receptor alpha and beta influence neuronal activity through activation of metabotropic glutamate receptors J. Neuroendocrinol. 21 2009 257 262
24. M. Pierdominici, A. Maselli, T. Colasanti, A.M. Giammarioli, F. Delunardo, D. Vacirca, M. Sanchez, A. Giovannetti, W. Malorni, and E. Ortona Estrogen receptor profiles in human peripheral blood lymphocytes Immunol. Lett. 132 2010 79 85
25. A. Pedram, M. Razandi, and E.R. Levin Nature of functional estrogen receptors at the plasma membrane Mol. Endocrinol. 20 2006 1996 2009 (Pubitemid 44286700)
26. F. Acconcia, P. Ascenzi, A. Bocedi, E. Spisni, V. Tomasi, A. Trentalance, P. Visca, and M. Marino Palmitoylation-dependent estrogen receptor alpha membrane localization: regulation by 17beta-estradiol Mol. Biol. Cell 16 2005 231 237 (Pubitemid 40028339)
27. A. Pedram, M. Razandi, R.C. Sainson, J.K. Kim, C.C. Hughes, and E.R. Levin A conserved mechanism for steroid receptor translocation to the plasma membrane J. Biol. Chem. 282 2007 22278 22288 (Pubitemid 47267344)
28. M. Razandi, G. Alton, A. Pedram, S. Ghonshani, P. Webb, and E.R. Levin Identification of a structural determinant necessary for the localization and function of estrogen receptor alpha at the plasma membrane Mol. Cell Biol. 23 2003 1633 1646 (Pubitemid 36246045)
29. D. Zhang, and V.L. Trudeau Integration of membrane and nuclear estrogen receptor signaling Comp. Biochem. Physiol. A Mol. Integr. Physiol. 144 2006 306 315 (Pubitemid 43956565)
30. N. Tubiana, Z. Mishal, F. le Caer, J.M. Seigneurin, Y. Berthoix, P.M. Martin, and Y. Carcassonne Quantification of oestradiol binding at the surface of human lymphocytes by flow cytofluorimetry Br. J. Cancer 54 1986 501 504 (Pubitemid 16031554)
31. W.P. Benten, M. Lieberherr, G. Giese, and F. Wunderlich Estradiol binding to cell surface raises cytosolic free calcium in T cells FEBS Lett. 422 1998 349 353 (Pubitemid 28075493)
32. K.S. Russell, M.P. Haynes, D. Sinha, E. Clerisme, and J.R. Bender Human vascular endothelial cells contain membrane binding sites for estradiol, which mediate rapid intracellular signaling Proc. Natl. Acad. Sci. U. S. A. 97 2000 5930 5935 (Pubitemid 30367501)
33. C.S. Watson, and B. Gametchu Membrane estrogen and glucocorticoid receptors - implications for hormonal control of immune function and autoimmunity Int. Immunopharmacol. 1 2001 1049 1063 (Pubitemid 32451742)
34. W.R. Harrington, S.H. Kim, C.C. Funk, Z. Madak-Erdogan, R. Schiff, J.A. Katzenellenbogen, and B.S. Katzenellenbogen Estrogen dendrimer conjugates that preferentially activate extranuclear, nongenomic versus genomic pathways of estrogen action Mol. Endocrinol. 20 2006 491 502 (Pubitemid 43291204)
35. K.L. Chambliss, Q. Wu, S. Oltmann, E.S. Konaniah, M. Umetani, K.S. Korach, G.D. Thomas, C. Mineo, I.S. Yuhanna, S.H. Kim, Z. Madak-Erdogan, A. Maggi, S.P. Dineen, C.L. Roland, D.Y. Hui, R.A. Brekken, J.A. Katzenellenbogen, B.S. Katzenellenbogen, and P.W. Shaul Non-nuclear estrogen receptor alpha signaling promotes cardiovascular protection but not uterine or breast cancer growth in mice J. Clin. Invest. 120 2010 2319 2330
36. T.W. Wu, S. Chen, and R.D. Brinton Membrane estrogen receptors mediate calcium signaling and MAP kinase activation in individual hippocampal neurons Brain Res. 1379 2011 34 43
37. M. Barbati, L. Pierdominici, F. Malchiodi Albedi, G. Karas, W. Rosano, and E. Ortona Cell surface estrogen receptor alpha is upregulated during subchronic metabolic stress and inhibits neuronal cell degeneration PLoS One 7 2012 e42339
38. E.R. Prossnitz, J.B. Arterburn, and L.A. Sklar GPR30: a G protein-coupled receptor for estrogen Mol. Cell Endocrinol. 265-266 2007 138 142 (Pubitemid 46273957)
39. C. Otto, B. Rohde-Schulz, G. Schwarz, I. Fuchs, M. Klewer, D. Brittain, G. Langer, B. Bader, K. Prelle, R. Nubbemeyer, and K.H. Fritzemeier G protein-coupled receptor 30 localizes to the endoplasmic reticulum and is not activated by estradiol Endocrinology 149 2008 4846 4856
40. M. Barton Position paper: the membrane estrogen receptor GPER - clues and questions Steroids 77 2012 935 942
41. M. Maggiolini, and D. Picard The unfolding stories of GPR30, a new membrane-bound estrogen receptor J. Endocrinol. 204 2010 105 114
42. E.J. Filardo, and P. Thomas Minireview: G protein-coupled estrogen receptor-1 GPER-1: its mechanism of action and role in female reproductive cancer, renal and vascular physiology Endocrinology 153 2012 2953 2962
43. A. Bouman, M.J. Heineman, and M.M. Faas Sex hormones and the immune response in humans Hum. Reprod. Update 11 2005 411 423 (Pubitemid 40895468)
44. M. Cunningham, and G. Gilkeson Estrogen receptors in immunity and autoimmunity Clin. Rev. Allergy Immunol. 40 2011 66 73
45. E. Karpuzoglu, and M. Zouali The multi-faceted influences of estrogen on lymphocytes: toward novel immuno-interventions strategies for autoimmunity management Clin. Rev. Allergy Immunol. 40 2011 16 26
46. + T cells Curr. Opin. Rheumatol. 19 2007 414 420
47. A. Giovannetti, M. Pierdominici, A. Di Iorio, R. Cianci, G. Murdaca, F. Puppo, F. Pandolfi, and R. Paganelli Apoptosis in the homeostasis of the immune system and in human immune mediated diseases Curr. Pharm. Des. 14 2008 253 268 (Pubitemid 351516870)
48. K.L. Phiel, R.A. Henderson, S.J. Adelman, and M.M. Elloso Differential estrogen receptor gene expression in human peripheral blood mononuclear cell populations Immunol. Lett. 97 2005 107 113 (Pubitemid 40038861)
49. G.J. Shim, D. Gherman, H.J. Kim, Y. Omoto, H. Iwase, D. Bouton, L.L. Kis, C.T. Andersson, M. Warner, and J.A. Gustafsson Differential expression of oestrogen receptors in human secondary lymphoid tissues J. Pathol. 208 2006 408 414 (Pubitemid 43210528)
50. V. Rider, X. Li, G. Peterson, J. Dawson, B.F. Kimler, and N.I. Abdou Differential expression of estrogen receptors in women with systemic lupus erythematosus J. Rheumatol. 33 2006 1093 1101 (Pubitemid 43825458)
51. R.H. Straub The complex role of estrogens in inflammation Endocr. Rev. 28 2007 521 574 (Pubitemid 47236336)
52. C.M. Grimaldi, J. Cleary, A.S. Dagtas, D. Moussai, and B. Diamond Estrogen alters thresholds for B cell apoptosis and activation J. Clin. Invest. 109 2002 1625 1633 (Pubitemid 34663525)
53. C.M. Grimaldi, V. Jeganathan, and B. Diamond Hormonal regulation of B cell development: 17beta-estradiol impairs negative selection of high-affinity DNA-reactive B cells at more than one developmental checkpoint J. Immunol. 176 2006 2703 2710
54. M.C. Erlandsson, C. Ohlsson, J.A. Gustafsson, and H. Carlsten Role of oestrogen receptors alpha and beta in immune organ development and in oestrogen-mediated effects on thymus Immunology 103 2001 17 25 (Pubitemid 32453095)
55. M.R. Ryan, R. Shepherd, J.K. Leavey, Y. Gao, F. Grassi, F.J. Schnell, W.P. Qian, G.J. Kersh, M.N. Weitzmann, and R. Pacifici An IL-7-dependent rebound in thymic T cell output contributes to the bone loss induced by estrogen deficiency Proc. Natl. Acad. Sci. U. S. A. 102 2005 16735 16740 (Pubitemid 41688846)
56. A.L. Zoller, and G.J. Kersh Estrogen induces thymic atrophy by eliminating early thymic progenitors and inhibiting proliferation of beta-selected thymocytes J. Immunol. 176 2006 7371 7378 (Pubitemid 43849038)
57. J.D. Neill Knobil and Neill's Physiology of Reproduction third ed. 2005 Academic Press New York
58. C. Aristimuno, R. Teijeiro, L. Valor, B. Alonso, M. Tejera-Alhambra, C. de Andres, D.O. Minarro, N. Lopez-Lazareno, F. Faure, and S. Sanchez-Ramon Sex-hormone receptors pattern on regulatory T-cells: clinical implications for multiple sclerosis Clin. Exp. Med. 12 2012 247 255
59. + regulatory T cell compartment J. Immunol. 173 2004 2227 2230 (Pubitemid 39063075)
60. L. Moroni, I. Bianchi, and A. Lleo Geoepidemiology, gender and autoimmune disease Autoimmun. Rev. 11 2012 A386 392
61. C. Selmi, E. Brunetta, M.G. Raimondo, and P.L. Meroni The X chromosome and the sex ratio of autoimmunity Autoimmun. Rev. 11 2012 A531 537
62. O.L. Quintero, M.J. Amador-Patarroyo, G. Montoya-Ortiz, A. Rojas-Villarraga, and J.M. Anaya Autoimmune disease and gender: plausible mechanisms for the female predominance of autoimmunity J. Autoimmun. 38 2012 J109 J119
63. C.P. Mavragani, and H.M. Moutsopoulos The geoepidemiology of Sjogren's syndrome Autoimmun. Rev. 9 2010 A305 310
64. T. Grodzicky, R. Lahita, R. Comtois, and J.L. Senecal Severe mixed connective tissue disease in a woman with pure gonadal dysgenesis: estrogens do not influence disease expression J. Rheumatol. 26 1999 923 926 (Pubitemid 29195684)
65. A.T. Borchers, S.M. Naguwa, C.L. Keen, and M.E. Gershwin The implications of autoimmunity and pregnancy J. Autoimmun. 34 2010 J287 299
66. A.T. Borchers, S.M. Naguwa, Y. Shoenfeld, and M.E. Gershwin The geoepidemiology of systemic lupus erythematosus Autoimmun. Rev. 9 2010 A277 287
67. R. Cervera, M.A. Khamashta, and G.R. Hughes The Euro-lupus project: epidemiology of systemic lupus erythematosus in Europe Lupus 18 2009 869 874
68. J.C. Crispin, S.N. Liossis, K. Kis-Toth, L.A. Lieberman, V.C. Kyttaris, Y.T. Juang, and G.C. Tsokos Pathogenesis of human systemic lupus erythematosus: recent advances Trends Mol. Med. 16 2010 47 57
69. R. Gualtierotti, M. Biggioggero, A.E. Penatti, and P.L. Meroni Updating on the pathogenesis of systemic lupus erythematosus Autoimmun. Rev. 10 2010 3 7
70. J. Roubinian, N. Talal, P.K. Siiteri, and J.A. Sadakian Sex hormone modulation of autoimmunity in NZB/NZW mice Arthritis Rheum. 22 1979 1162 1169 (Pubitemid 10163780)
71. J.R. Roubinian, N. Talal, J.S. Greenspan, J.R. Goodman, and P.K. Siiteri Effect of castration and sex hormone treatment on survival anti-nucleic acid antibodies, and glomerulonephritis in NZB/NZW F1 mice J. Exp. Med. 147 1978 1568 1583 (Pubitemid 8372952)
72. J. Li, and R.W. McMurray Effects of estrogen receptor subtype-selective agonists on autoimmune disease in lupus-prone NZB/NZW F1 mouse model Clin. Immunol. 123 2007 219 226 (Pubitemid 46591958)
73. J.L. Svenson, J. EuDaly, P. Ruiz, K.S. Korach, and G.S. Gilkeson Impact of estrogen receptor deficiency on disease expression in the NZM2410 lupus prone mouse Clin. Immunol. 128 2008 259 268
74. M. Cutolo, A. Sulli, and R.H. Straub Estrogen metabolism and autoimmunity Autoimmun. Rev. 11 2012 A460 464
75. E. Ortona, P. Margutti, P. Matarrese, F. Franconi, and W. Malorni Redox state, cell death and autoimmune diseases: a gender perspective Autoimmun. Rev. 7 2008 579 584
76. G. Zandman-Goddard, E. Peeva, and Y. Shoenfeld Gender and autoimmunity Autoimmun. Rev. 6 2007 366 372 (Pubitemid 46810396)
77. M. Cutolo, S. Capellino, A. Sulli, B. Serioli, M.E. Secchi, B. Villaggio, and R.H. Straub Estrogens and autoimmune diseases Ann. N. Y. Acad. Sci. 1089 2006 538 547 (Pubitemid 47092097)
78. M. Folomeev, M. Dougados, J. Beaune, J.C. Kouyoumdjian, K. Nahoul, B. Amor, and Z. Alekberova Plasma sex hormones and aromatase activity in tissues of patients with systemic lupus erythematosus Lupus 1 1992 191 195
79. A. Lateef, and M. Petri Hormone replacement and contraceptive therapy in autoimmune diseases J. Autoimmun. 38 2012 J170 176
80. N.I. Abdou, V. Rider, C. Greenwell, X. Li, and B.F. Kimler 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. 35 2008 797
81. N. Kanda, T. Tsuchida, and K. Tamaki Estrogen enhancement of anti-double-stranded DNA antibody and immunoglobulin G production in peripheral blood mononuclear cells from patients with systemic lupus erythematosus Arthritis Rheum. 42 1999 328 337 (Pubitemid 29072851)
82. V. Rider, S. Keltner, and N.I. Abdou Increased estrogen-dependent expression of calcineurin in female SLE T cells is regulated by multiple mechanisms J. Gend. Specif. Med. 6 2003 14 21 (Pubitemid 36790208)
83. E. Walters, V. Rider, N.I. Abdou, C. Greenwell, S. Svojanovsky, P. Smith, and B.F. Kimler Estradiol targets T cell signaling pathways in human systemic lupus Clin. Immunol. 133 2009 428 436
84. E.N. Kassi, P.G. Vlachoyiannopoulos, H.M. Moutsopoulos, C.E. Sekeris, and P. Moutsatsou Molecular analysis of estrogen receptor alpha and beta in lupus patients Eur. J. Clin. Invest. 31 2001 86 93 (Pubitemid 32151126)
85. R. Suenaga, M.J. Evans, K. Mitamura, V. Rider, and N.I. Abdou Peripheral blood T cells and monocytes and B cell lines derived from patients with lupus express estrogen receptor transcripts similar to those of normal cells J. Rheumatol. 25 1998 1305 1312 (Pubitemid 28312347)
86. Z.H. Liu, Z.H. Cheng, R.J. Gong, H. Liu, D. Liu, and L.S. Li Sex differences in estrogen receptor gene polymorphism and its association with lupus nephritis in Chinese Nephron 90 2002 174 180 (Pubitemid 34701993)
87. B.M. Kisiel, J. Kosinska, M. Wierzbowska, L. Rutkowska-Sak, E. Musiej-Nowakowska, M. Wudarski, M. Olesinska, P. Krajewski, J. Lacki, M. Rell-Bakalarska, P.P. Jagodzinski, W. Tlustochowicz, and R. Ploski Differential association of juvenile and adult systemic lupus erythematosus with genetic variants of oestrogen receptors alpha and beta Lupus 20 2011 85 89
88. Y.J. Lee, K.S. Shin, S.W. Kang, C.K. Lee, B. Yoo, H.S. Cha, E.M. Koh, S.J. Yoon, and J. Lee Association of the oestrogen receptor alpha gene polymorphisms with disease onset in systemic lupus erythematosus Ann. Rheum. Dis. 63 2004 1244 1249 (Pubitemid 39273502)
89. J.B. Harley, M.E. Alarcon-Riquelme, L.A. Criswell, C.O. Jacob, R.P. Kimberly, K.L. Moser, B.P. Tsao, T.J. Vyse, C.D. Langefeld, S.K. Nath, J.M. Guthridge, B.L. Cobb, D.B. Mirel, M.C. Marion, A.H. Williams, J. Divers, W. Wang, S.G. Frank, B. Namjou, S.B. Gabriel, A.T. Lee, P.K. Gregersen, T.W. Behrens, K.E. Taylor, M. Fernando, R. Zidovetzki, P.M. Gaffney, J.C. Edberg, J.D. Rioux, J.O. Ojwang, J.A. James, J.T. Merrill, G.S. Gilkeson, M.F. Seldin, H. Yin, E.C. Baechler, Q.Z. Li, E.K. Wakeland, G.R. Bruner, K.M. Kaufman, and J.A. Kelly Genome-wide association scan in women with systemic lupus erythematosus identifies susceptibility variants in ITGAM, PXK, KIAA1542 and other loci Nat. Genet. 40 2008 204 210 (Pubitemid 351171405)
90. G. Hom, R.R. Graham, B. Modrek, K.E. Taylor, W. Ortmann, S. Garnier, A.T. Lee, S.A. Chung, R.C. Ferreira, P.V. Pant, D.G. Ballinger, R. Kosoy, F.Y. Demirci, M.I. Kamboh, A.H. Kao, C. Tian, I. Gunnarsson, A.A. Bengtsson, S. Rantapaa-Dahlqvist, M. Petri, S. Manzi, M.F. Seldin, L. Ronnblom, A.C. Syvanen, L.A. Criswell, P.K. Gregersen, and T.W. Behrens Association of systemic lupus erythematosus with C8orf13-BLK and ITGAM-ITGAX N. Engl. J. Med. 358 2008 900 909 (Pubitemid 351397089)
91. J.D. Yager, and N.E. Davidson Estrogen carcinogenesis in breast cancer N. Engl. J. Med. 354 2006 270 282
92. L.M. Berstein, and R.J. Santen Innovative Endocrinology of Cancer 2008 Landes Bioscience and Springer Science + Business Media New York
93. E. Cavalieri, and E. Rogan The molecular etiology and prevention of estrogen-initiated cancers: Ockham's razor: pluralitas non est ponenda sine necessitate. Plurality should not be posited without necessity Mol. Aspects Med. 36 2013 1 55
94. W. Yue, J.D. Yager, J.P. Wang, E.R. Jupe, and R.J. Santen Estrogen receptor-dependent and independent mechanisms of breast cancer carcinogenesis Steroids 78 2013 161 170
95. C.R. Jefcoate, J.G. Liehr, R.J. Santen, T.R. Sutter, J.D. Yager, W. Yue, S.J. Santner, R. Tekmal, L. Demers, R. Pauley, F. Naftolin, G. Mor, and L. Berstein Tissue-specific synthesis and oxidative metabolism of estrogens J. Natl. Cancer Inst. Monogr. 27 2000 95 112
96. V.C. Jordan, J.S. Lewis, C. Osipo, and D. Cheng The apoptotic action of estrogen following exhaustive antihormonal therapy: a new clinical treatment strategy Breast 14 2005 624 630 (Pubitemid 41683589)
97. R.X. Song, and R.J. Santen Apoptotic action of estrogen Apoptosis 8 2003 55 60 (Pubitemid 36133138)
98. A.Z. LaCroix, R.T. Chlebowski, J.E. Manson, A.K. Aragaki, K.C. Johnson, L. Martin, K.L. Margolis, M.L. Stefanick, R. Brzyski, J.D. Curb, B.V. Howard, C.E. Lewis, and J. Wactawski-Wende Health outcomes after stopping conjugated equine estrogens among postmenopausal women with prior hysterectomy: a randomized controlled trial JAMA 305 2011 1305 1314
99. L.L. Schierbeck, L. Rejnmark, C.L. Tofteng, L. Stilgren, P. Eiken, L. Mosekilde, L. Kober, and J.E. Jensen Effect of hormone replacement therapy on cardiovascular events in recently postmenopausal women: randomised trial BMJ 345 2012 e6409
100. R.J. Santen, Y. Song, W. Yue, J.P. Wang, and D.F. Heitjan Effects of menopausal hormonal therapy on occult breast tumors J. Steroid Biochem. Mol. Biol. 137 2013 150 156
101. T.J. Key Endogenous oestrogens and breast cancer risk in premenopausal and postmenopausal women Steroids 76 2011 812 815
102. Collaborative Group on Hormonal Factors in Breast Cancer Menarche, menopause, and breast cancer risk: individual participant meta-analysis including 118 964 women with breast cancer from 117 epidemiological studies Lancet Oncol. 13 2012 1141 1151
103. K. Nichols, P.A. Newcomb, J.M. Hampton, K.M. Egan, L. Titus-Ernstoff, and A. Trentham-Dietz Bilateral oophorectomy in relation to risk of postmenopausal breast cancer: confounding by nonmalignant indications for surgery? Am. J. Epidemiol. 173 2011 1111 1120
104. V. Beral Breast cancer and hormone-replacement therapy in the Million Women Study Lancet 362 2003 419 427 (Pubitemid 36999703)
105. H.S. Taylor, and J.E. Manson Update in hormone therapy use in menopause J. Clin. Endocrinol. Metab. 96 2011 255 264
106. E.R. Levin, and R.J. Pietras Estrogen receptors outside the nucleus in breast cancer Breast Cancer Res. Treat. 108 2008 351 361 (Pubitemid 351431076)
107. Y. Berthois, N. Pourreau-Schneider, P. Gandilhon, H. Mittre, N. Tubiana, and P.M. Martin Estradiol membrane binding sites on human breast cancer cell lines. Use of a fluorescent estradiol conjugate to demonstrate plasma membrane binding systems J. Steroid Biochem. 25 1986 963 972 (Pubitemid 17206014)
108. D. Zivadinovic, B. Gametchu, and C.S. Watson Membrane estrogen receptor-alpha levels in MCF-7 breast cancer cells predict cAMP and proliferation responses Breast Cancer Res. 7 2005 R101 112
109. D. Zivadinovic, and C.S. Watson Membrane estrogen receptor-alpha levels predict estrogen-induced ERK1/2 activation in MCF-7 cells Breast Cancer Res. 7 2005 R130 144
110. T. Sorlie, C.M. Perou, R. Tibshirani, T. Aas, S. Geisler, H. Johnsen, T. Hastie, M.B. Eisen, M. van de Rijn, S.S. Jeffrey, T. Thorsen, H. Quist, J.C. Matese, P.O. Brown, D. Botstein, P.E. Lonning, and A.L. Borresen-Dale Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications Proc. Natl. Acad. Sci. U. S. A. 98 2001 10869 10874 (Pubitemid 32878711)
111. A. Jemal, R. Siegel, E. Ward, Y. Hao, J. Xu, and M.J. Thun Cancer statistics, 2009 CA Cancer J. Clin. 59 2009 225 249
112. L.C. Murphy, S.V. Seekallu, and P.H. Watson Clinical significance of estrogen receptor phosphorylation Endocr. Relat. Cancer 18 2011 R1 14
113. A.H. Partridge, O. Pagani, O. Abulkhair, S. Aebi, F. Amant, H.A. Azim Jr., A. Costa, S. Delaloge, G. Freilich, O.D. Gentilini, N. Harbeck, C.M. Kelly, S. Loibl, D. Meirow, F. Peccatori, B. Kaufmann, and F. Cardoso First international consensus guidelines for breast cancer in young women (BCY1) Breast 23 2014 209 220
114. F. Senkus Time for more optimism in metastatic breast cancer? Cancer Treat. Rev. 40 2014 220 228
115. Q. Li, H. Sun, J. Zou, C. Ge, K. Yu, Y. Cao, and Q. Hong Increased expression of estrogen receptor alpha-36 by breast cancer oncogene IKKepsilon promotes growth of ER-negative breast cancer cells Cell Physiol. Biochem. 31 2013 833 841
116. K.A. Burns, and K.S. Korach Estrogen receptors and human disease: an update Arch. Toxicol. 86 2012 1491 1504
117. E. Leygue, and L.C. Murphy A bi-faceted role of estrogen receptor beta in breast cancer Endocr. Relat. Cancer 20 2013 R127 139
118. A.M. Shaaban, A.R. Green, S. Karthik, Y. Alizadeh, T.A. Hughes, L. Harkins, I.O. Ellis, J.F. Robertson, E.C. Paish, P.T. Saunders, N.P. Groome, and V. Speirs Nuclear and cytoplasmic expression of ERbeta1 ERbeta2, and ERbeta5 identifies distinct prognostic outcome for breast cancer patients Clin. Cancer Res. 14 2008 5228 5235
119. M. Yan, M. Rayoo, E.A. Takano, and S.B. Fox Nuclear and cytoplasmic expressions of ERbeta1 and ERbeta2 are predictive of response to therapy and alters prognosis in familial breast cancers Breast Cancer Res. Treat. 126 2011 395 405
120. P. Dey, R.P. Barros, M. Warner, A. Strom, and J.A. Gustafsson Insight into the mechanisms of action of estrogen receptor beta in the breast prostate, colon, and CNS J. Mol. Endocrinol. 51 2013 T61 74
121. J. Haring, S. Schuler, C. Lattrich, O. Ortmann, and O. Treeck Role of estrogen receptor beta in gynecological cancer Gynecol. Oncol. 127 2012 673 676
122. Y.S. Jung, S.J. Lee, M.H. Yoon, N.C. Ha, and B.J. Park Estrogen receptor alpha is a novel target of the Von Hippel-Lindau protein and is responsible for the proliferation of VHL-deficient cells under hypoxic conditions Cell Cycle 11 2012 4462 4473
123. A. Rudolph, C. Toth, M. Hoffmeister, W. Roth, E. Herpel, P. Schirmacher, H. Brenner, and J. Chang-Claude Colorectal cancer risk associated with hormone use varies by expression of estrogen receptor-beta Cancer Res. 73 2013 3306 3315
124. W. Sieh, M. Kobel, T.A. Longacre, D.D. Bowtell, A. deFazio, M.T. Goodman, E. Hogdall, S. Deen, N. Wentzensen, K.B. Moysich, J.D. Brenton, B.A. Clarke, U. Menon, C.B. Gilks, A. Kim, J. Madore, S. Fereday, J. George, L. Galletta, G. Lurie, L.R. Wilkens, M.E. Carney, P.J. Thompson, R.K. Matsuno, S.K. Kjaer, A. Jensen, C. Hogdall, K.R. Kalli, B.L. Fridley, G.L. Keeney, R.A. Vierkant, J.M. Cunningham, L.A. Brinton, H.P. Yang, M.E. Sherman, M. Garcia-Closas, J. Lissowska, K. Odunsi, C. Morrison, S. Lele, W. Bshara, L. Sucheston, M. Jimenez-Linan, K. Driver, J. Alsop, M. Mack, V. McGuire, J.H. Rothstein, B.P. Rosen, M.Q. Bernardini, H. Mackay, A. Oza, E.L. Wozniak, E. Benjamin, A. Gentry-Maharaj, S.A. Gayther, A.V. Tinker, L.M. Prentice, C. Chow, M.S. Anglesio, S.E. Johnatty, G. Chenevix-Trench, A.S. Whittemore, P.D. Pharoah, E.L. Goode, D.G. Huntsman, and S.J. Ramus Hormone-receptor expression and ovarian cancer survival: an Ovarian Tumor Tissue Analysis consortium study Lancet Oncol. 14 2013 853 862
125. T. Zellweger, S. Sturm, S. Rey, I. Zlobec, J.R. Gsponer, C.A. Rentsch, L.M. Terracciano, A. Bachmann, L. Bubendorf, and C. Ruiz Estrogen receptor beta expression and androgen receptor phosphorylation correlate with a poor clinical outcome in hormone-naive prostate cancer and are elevated in castration-resistant disease Endocr. Relat. Cancer 20 2013 403 413
126. C.Z. Altuntas, R. Jaini, P. Kesaraju, D. Jane-wit, J.M. Johnson, K. Covey, C.A. Flask, M. Dutertre, J.Y. Picard, and V.K. Tuohy Autoimmune mediated regulation of ovarian tumor growth Gynecol. Oncol. 124 2012 98 104
127. G. Curigliano Immunity and autoimmunity: revising the concepts of response to breast cancer Breast 3 Suppl. 20 2011 S71 74
128. R. Einefors, U. Kogler, C. Ellberg, and H. Olsson Autoimmune diseases and hypersensitivities improve the prognosis in ER-negative breast cancer SpringerPlus 2 2013 357
129. M.F. Neurath, and S. Finotto IL-6 signaling in autoimmunity, chronic inflammation and inflammation-associated cancer Cytokine Growth Factor Rev. 22 2011 83 89
130. E.V. Vykhovanets, G.T. Maclennan, O.V. Vykhovanets, and S. Gupta IL-17 Expression by macrophages is associated with proliferative inflammatory atrophy lesions in prostate cancer patients Int. J. Clin. Exp. Pathol. 4 2011 552 565
131. S. Kobold, T. Lutkens, Y. Cao, C. Bokemeyer, and D. Atanackovic Autoantibodies against tumor-related antigens: incidence and biologic significance Hum. Immunol. 71 2010 643 651
132. P. Zaenker, and M.R. Ziman Serologic autoantibodies as diagnostic cancer biomarkers - a review Cancer Epidemiol. Biomarkers Prev. 22 2013 2161 2181
133. M. Abu-Shakra, D. Buskila, M. Ehrenfeld, K. Conrad, and Y. Shoenfeld Cancer and autoimmunity: autoimmune and rheumatic features in patients with malignancies Ann. Rheum. Dis. 60 2001 433 441
134. C. Chapman, A. Murray, J. Chakrabarti, A. Thorpe, C. Woolston, U. Sahin, A. Barnes, and J. Robertson Autoantibodies in breast cancer: their use as an aid to early diagnosis Ann. Oncol. 18 2007 868 873 (Pubitemid 47054083)
135. R. Kiyamova, O. Garifulin, V. Gryshkova, O. Kostianets, M. Shyian, I. Gout, and V. Filonenko Preliminary study of thyroid and colon cancers-associated antigens and their cognate autoantibodies as potential cancer biomarkers Biomarkers 17 2012 362 371
136. E. Giustarini, A. Pinchera, P. Fierabracci, M. Roncella, L. Fustaino, C. Mammoli, and C. Giani Thyroid autoimmunity in patients with malignant and benign breast diseases before surgery Eur. J. Endocrinol. 154 2006 645 649 (Pubitemid 43810849)
137. P.J. Hardefeldt, G.D. Eslick, and S. Edirimanne Benign thyroid disease is associated with breast cancer: a meta-analysis Breast Cancer Res. Treat. 133 2012 1169 1177
138. E. Fiore, E. Giustarini, C. Mammoli, F. Fragomeni, D. Campani, I. Muller, A. Pinchera, and C. Giani Favorable predictive value of thyroid autoimmunity in high aggressive breast cancer J. Endocrinol. Invest. 30 2007 734 738 (Pubitemid 350238198)
139. A. Mudarris, and E.J. Peck Jr. Human anti-estrogen receptor antibodies: assay, characterization, and age- and sex-related differences J. Clin. Endocrinol. Metab. 64 1987 246 254 (Pubitemid 17007928)
140. K.A. Counihan, F.T. Vertosick, and R.H. Kelly Anti-estrogen antibodies in systemic lupus erythematosus: a quantitative evaluation of serum levels Immunol. Invest. 20 1991 317 331
141. M. Feldman Steroid receptor antibodies in autoimmune disorders Biochem. Biophys. Res. Commun. 145 1987 1342 1348
142. R.H. Kelly, and F.T. Vertosick Jr. Systemic lupus erythematosus: a role for anti-receptor antibodies? Med. Hypotheses 20 1986 95 101 (Pubitemid 16022725)
143. T. Colasanti, A. Maselli, F. Conti, M. Sanchez, C. Alessandri, C. Barbati, D. Vacirca, A. Tinari, F. Chiarotti, A. Giovannetti, F. Franconi, G. Valesini, W. Malorni, M. Pierdominici, and E. Ortona Autoantibodies to estrogen receptor alpha interfere with T lymphocyte homeostasis and are associated with disease activity in systemic lupus erythematosus Arthritis Rheum. 64 2012 778 787
144. U.S. Gaipl, A. Kuhn, A. Sheriff, L.E. Munoz, S. Franz, R.E. Voll, J.R. Kalden, and M. Herrmann Clearance of apoptotic cells in human SLE Curr. Dir. Autoimmun. 9 2006 173 187
145. G.E. Grossmayer, L.E. Munoz, U.S. Gaipl, S. Franz, A. Sheriff, R.E. Voll, J.R. Kalden, and M. Herrmann Removal of dying cells and systemic lupus erythematosus Mod. Rheumatol. 15 2005 383 390 (Pubitemid 43135299)
146. A. Giovannetti, A. Maselli, T. Colasanti, E. Rosato, F. Salsano, S. Pisarri, I. Mezzaroma, W. Malorni, E. Ortona, and M. Pierdominici Autoantibodies to estrogen receptor alpha in systemic sclerosis (SSc) as pathogenetic determinants and markers of progression PLoS One 8 2013 e74332
147. A. Gabrielli, E.V. Avvedimento, T. Krieg, and N. Scleroderma N. Engl. J. Med. 360 2009 1989 2003
148. B. Ranque, and L. Mouthon Geoepidemiology of systemic sclerosis Autoimmun. Rev. 9 2010 A311 318
149. V. Racanelli, M. Prete, G. Musaraj, F. Dammacco, and F. Perosa Autoantibodies to intracellular antigens: generation and pathogenetic role Autoimmun. Rev. 10 2011 503 508