Estradiol promotes the development of a fibrotic phenotype and is increased in the serum of patients with systemic sclerosis

Arthritis Research and Therapy

Volumn 15, Issue 1, 2013, Pages

  Aida Yasuoka, Keiko ^a   Peoples, Christine ^a   Yasuoka, Hidekata ^a   Hershberger, Pamela ^b   Thiel, Katelynn ^a   Cauley, Jane A ^c   Medsger, Thomas A ^a   Feghali Bostwick, Carol A ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b ROSWELL PARK CANCER INSTITUTE   (United States)

^c UNIVERSITY OF PITTSBURGH GRADUATE SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1,3,5 TRIS(4 HYDROXYPHENYL) 4 PROPYLPYRAZOLE; 1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; 2 MORPHOLINO 8 PHENYLCHROMONE; 4 (4 FLUOROPHENYL) 2 (4 HYDROXYPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; ESTRADIOL; ESTROGEN; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; ESTRONE; FIBRONECTIN; FULVESTRANT; GENISTEIN; INOSITOL 1,4,5 TRIPHOSPHATE INHIBITOR; INOSITOL 1,4,5 TRISPHOSPHATE DERIVATIVE; MITOGEN ACTIVATED PROTEIN KINASE P38 INHIBITOR; UNCLASSIFIED DRUG; ESTROGEN RECEPTOR ANTAGONIST;

ADULT; AGED; ARTICLE; BLOOD SAMPLING; CLINICAL ARTICLE; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; ESTROGEN BLOOD LEVEL; ESTRONE BLOOD LEVEL; EX VIVO STUDY; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; MASS SPECTROMETRY; MEDIATOR; ORGAN CULTURE; PHENOTYPE; PROTEIN EXPRESSION; SERUM; SIGNAL TRANSDUCTION; SKIN; SKIN FIBROBLAST; SKIN FIBROSIS; SYSTEMIC SCLEROSIS; BIOSYNTHESIS; BLOOD; CELL CULTURE; DRUG EFFECTS; FEMALE; FIBROBLAST; FIBROSIS; IMMUNOHISTOCHEMISTRY; LIQUID CHROMATOGRAPHY; METABOLISM; MIDDLE AGED; PATHOLOGY; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TANDEM MASS SPECTROMETRY; WESTERN BLOTTING;

AGED; BLOTTING, WESTERN; CELLS, CULTURED; CHROMATOGRAPHY, LIQUID; ESTRADIOL; ESTROGEN RECEPTOR ANTAGONISTS; FEMALE; FIBROBLASTS; FIBRONECTINS; FIBROSIS; HUMANS; IMMUNOHISTOCHEMISTRY; MIDDLE AGED; PHENOTYPE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SCLERODERMA, SYSTEMIC; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY;

EID: 84872102610     PISSN: 14786354     EISSN: 14786362     Source Type: Journal    
DOI: 10.1186/ar4140     Document Type: Article

References (55)

1. Silver RM, Medsger TA, Bolster MB. Systemic sclerosis and scleroderma variants: clinical aspects. Arthritis and Allied Conditions 2005, 1633-1680. Philadelphia, PA: Lippincott, Williams & Wilkins, Koopman WJ, Moreland LW.
2. Highland KB, Silver RM. New developments in scleroderma interstitial lung disease. Curr Opin Rheumatol 2005, 17:734-745.
3. Deroo BJ, Korach KS. Estrogen receptors and human disease. J Clin Invest 2006, 116:561-570. 10.1172/JCI27987, 2373424, 16511588.
4. Henderson BE, Feigelson HS. Hormonal carcinogenesis. Carcinogenesis 2000, 21:427-433. 10.1093/carcin/21.3.427, 10688862.
5. Harris HA, Albert LM, Leathurby Y, Malamas MS, Mewshaw RE, Miller CP, Kharode YP, Marzolf J, Komm BS, Winneker RC, Frail DE, Henderson RA, Zhu Y, Keith JC. Evaluation of an estrogen receptor-beta agonist in animal models of human disease. Endocrinology 2003, 144:4241-4249. 10.1210/en.2003-0550, 14500559.
6. Wise PM, Dubal DB, Wilson ME, Rau SW, Bottner M. Minireview. Neuroprotective effects of estrogen: new insights into mechanisms of action. Endocrinology 2001, 142:969-973. 10.1210/en.142.3.969, 11181507.
7. Hurn PD, Sacco RL. Sex, steroids and stroke: introduction. Stroke 2004, 35:2642-2643.
8. Ohlsson C, Hellberg N, Parini P, Vidal O, Bohlooly-Y M, Rudling M, Lindberg MK, Warner M, Angelin B, Gustafsson JA. Obesity and disturbed lipoprotein profile in estrogen receptor-alpha-deficient male mice. Biochem Biophys Res Commun 2006, 278:640-645.
9. Beretta L, Caronni M, Origgi L, Ponti A, Santaniello A, Scorza R. Hormone replacement therapy may prevent the development of isolated pulmonary hypertension in patients with systemic sclerosis. Scand J Rheumatol 2006, 35:468-471. 10.1080/03009740600844498, 17343256.
10. Thomas-Golbanov CK, Wilke WS, Fessler BJ, Hoffman GS. Open label trial of tamoxifen in scleroderma. Clin Exp Rheumatol 2003, 21:99-102.
11. Feghali-Bostwick C, Medsger TA, Wright TM. Analysis of systemic sclerosis in twins reveals low concordance for disease and high concordance for the presence of antinuclear antibodies. Arthritis Rheum 2003, 48:1956-1963. 10.1002/art.11173, 12847690.
12. Zhou X, Tan FK, Xiong M, Arnett FC, Feghali-Bostwick CA. Monozygotic twins clinically discordant for scleroderma show concordance for fibroblast gene expression profiles. Arthritis Rheum 2005, 52:3305-3314. 10.1002/art.21355, 16200604.
13. Sun J, Meyers MJ, Fink BE, Rajendran R, Katzenellenbogen JA, Katzenellenbogen BS. Novel ligands that function as selective estrogens or antiestrogens for estrogen receptor-alpha or estrogen receptor-beta. Endocrinology 1999, 140:800-804. 10.1210/en.140.2.800, 9927308.
14. Pilewski JM, Liu L, Henry AC, Knauer AV, Feghali-Bostwick CA. Insulin-like growth factor binding protein 3 and 5 are overexpressed in idiopathic pulmonary fibrosis and contribute to extracellular matrix deposition. Am J Pathol 2005, 166:399-407. 10.1016/S0002-9440(10)62263-8, 1602317, 15681824.
15. Yasuoka H, Larregina AT, Yamaguchi Y, Feghali-Bostwick CA. Human skin culture as an ex vivo model for assessing the fibrotic effects of insulin-like growth factor binding proteins. Open Rheumatol J 2008, 2:17-22. 10.2174/1874312900802010017, 2577950, 19088866.
16. Ashcroft GS, Dodsworth J, van Boxtel E, Tarnuzzer RW, Horan MA, Schultz GS, Ferguson MW. Estrogen accelerates cutaneous wound healing associated with an increase in TGF-β1 levels. Nat Med 1997, 3:1209-1215. 10.1038/nm1197-1209, 9359694.
17. Ashcroft GS, Greenwell-wild T, Horan MA, Wahl SM, Ferguson MW. Topical estrogen accelerates cutaneous wound healing in aged humans associated with an altered inflammation response. Am J Pathol 1999, 155:1137-1146. 10.1016/S0002-9440(10)65217-0, 1867002, 10514397.
18. Feghali CA, Wright TM. Identification of multiple, deferentially expressed messenger RNAs in dermal fibroblasts from patients with systemic sclerosis. Arthritis Rheum 1999, 42:1451-1457. 10.1002/1529-0131(199907)42:7<1451::AID-ANR19>3.0.CO;2-6, 10403273.
19. Meyringer R, Neumann E, Judex M, Landthaler M, Kullmann F, Scholmerich J, Gay S, Tarner IH, Distler O, Müller-Ladner U. Analysis of gene expression patterns in systemic sclerosis fibroblasts using RNA arbitrarily primed-polymerase chain reaction for different display. J Rheumatol 2007, 34:747-753.
20. Mercier I, Colombo F, Mader S, Calderone A. Ovarian hormones induce TGF-beta (3) and fibronectin mRNAs but exhibit a disparate action on cardiac fibroblast proliferation. Cardiovasc Res 2002, 53:728-739. 10.1016/S0008-6363(01)00525-9, 11861043.
21. Ziegler WF, Bernstein I, Badger G, Leavitt T, Cerrero ML. Regional hemodinamic adaptation during the menstrual cycle. Obstet Gynecol 1999, 94:695-699. 10.1016/S0029-7844(99)00397-X, 10546712.
22. Bakos O, Lundkvist O, Wide L, Bergh T. Ultrasonographical and hormonal description of normal ovulatory menstrual cycle. Acta Obstet Gynecol Scand 1994, 73:790-796. 10.3109/00016349409072507, 7817731.
23. Notelovitz M, Funk S, Nanavati N, Mazzeo M. Estradiol absorption from vaginal tablets in postmenoposal women. Obstet Gynecol 2002, 99:556-562. 10.1016/S0029-7844(01)01385-0, 12039110.
24. Haczynski J, Tarkowski R, Jarzabek K, Slomczynska M, Wolczynski S, Magoffin DA, Jakowicki JA, Jakimiuk AJ. Human cultured skin fibroblasts express estrogen receptor alpha and beta. Int J Mol Med 2002, 10:149-153.
25. Foley EF, Jazaeri AA, Shupnik MA, Jazaeri O, Rice LW. Selective loss of estrogen receptor beta in malignant human colon. Cancer Res 2000, 60:245-248.
26. Jassam N, Bell SM, Speirs V, Quirke P. Loss of expression of oestrogen receptor beta in col on cancer and its association with Duke's staging. Oncol Rep 2005, 14:17-21.
27. Konstantinopoulos PA, Kominea A, Vandoros G, Sykiotis GP, Andricopoulos P, Varakis I, Sotiropoulou-Bonikou G, Papavassiliou AG. Oestrogen receptor beta (ERβ) is abundantly expressed in normal colonic mucosa, but declines in colon adenocarcinoma paralleling the tumor's dedifferentiation. Eur J Cancer 2003, 39:1251-1258. 10.1016/S0959-8049(03)00239-9, 12763213.
28. Campbell-Thompson M, Lynch IJ, Bhardwaj B. Expression of estrogen receptor (ER) subtypes and ERβ isoforms in colon cancer. Cancer Res 2001, 61:632-640.
29. Leav I, Lau KM, Adams JY, McNeal JE, Taplin ME, Wang J, Singh H, Ho SM. Comparative studies of the estrogen receptors beta and alpha and the androgen receptor in normal human prostate glands, dysplasia, and in primary and metastatic carcinoma. Am J Pathol 2001, 159:79-92. 10.1016/S0002-9440(10)61676-8, 1850428, 11438457.
30. Horvath LG, Henshall SM, Lee CS, Head DR, Quinn DI, Makela S, Delprado W, Golovsky D, Brenner PC, O'Neill G, Kooner R, Stricker PD, Grygiel JJ, Gustafsson JA, Sutherland RL. Frequent loss of estrogen receptor-beta expression in prostate cancer. Cancer Res 2001, 61:5331-5335.
31. Weihua Z, Makela S, Andersson LC, Salmi S, Saji S, Webster JI, Jensen EV, Nilsson S, Warner M, Gustafsson JA. A role for estrogen receptor β in the regulation of growth of the ventral prostate. Proc Natl Acad Sci USA 2001, 98:6330-6335. 10.1073/pnas.111150898, 33468, 11371645.
32. Soldano S, Montagna P, Brizzolara R, Sulli A, Parodi A, Seriolo B, Paolino S, Villaggio B, Cutolo M. Effects of estrogens on extracellular matrix synthesis in cultures of human and normal scleroderma skin fibroblasts. Ann N Y Acad Sci 2010, 1193:25-29. 10.1111/j.1749-6632.2009.05296.x, 20398004.
33. Mankhey RW, Wells CC, Bhatti F, Maric C. 17β-estradiol supplementation reduces tubulointerstitial fibrosis by increasing MMP activity in the diabetic kidney. Am J Physiol Regul Integr Comp Physiol 2007, 292:R769-R777.
34. Pedram A, Razandi M, O'Mahony F, Lubahn D, Levin ER. Estrogen receptor-beta prevents cardiac fibrosis. Mol Endocrinol 2010, 24:2152-2165. 10.1210/me.2010-0154, 2958752, 20810711.
35. Nilsson S, Mäkelä S, Treuter E, Tujague M, Thomsen J, Andersson G, Enmark E, Pettersson K, Warner M, Gustafsson JA. Mechanisms of estrogen action. Physiol Rev 2001, 81:1535-1565.
36. O'Lone R, Frith MC, Karlsson EK, Hansen U. Genomic targets of nuclear estrogen receptors. Mol Endocrinol 2004, 18:1859-1875. 10.1210/me.2003-0044, 15031323.
37. Gottlicher M, Heck S, Herrlich P. Transcriptional cross-talk, the second mode of steroid hormone receptor action. J Mol Med 1998, 76:480-489. 10.1007/s001090050242, 9660166.
38. Razandi M, Pedram A, Merchenthaler I, Greene GL, Levin ER. Plasma membrane estrogen receptors exist and functions as dimers. Mol Endocrinol 2004, 18:2854-2865. 10.1210/me.2004-0115, 15231873.
39. Levin ER. Cellular functions of plasma membrane estrogen receptors. Steroid 2002, 67:471-475.
40. Olson JM, Hallahan AR. P38 MAP kinase: a convergence point in cancer therapy. Trends Mol Med 2004, 10:125-129. 10.1016/j.molmed.2004.01.007, 15102355.
41. Kim JK, Levin ER. Estrogen signaling in the cardiovascular system. Nucl Res Signaling 2006, 4:1-5.
42. Chang L, Karin M. Mammalian MAP kinase signaling cascades. Nature 2001, 410:37-40. 10.1038/35065000, 11242034.
43. Xia Z, Dickens M, Raingeaud J, Davis RJ. Opposing effects of ERK and JNK-p38 kinases in apoptosis. Science 1995, 270:1326-1331. 10.1126/science.270.5240.1326, 7481820.
44. Redaelli C, Granucci F, De Gioia L, Cipolla L. Synthesis and biological activity of Akt/PI3K inhibitors. Mini Rev Med Chem 2006, 6:1127-1136. 10.2174/138955706778560139, 17073713.
45. Brincat M, Moniz CJ, Studd JW, Darby A, Magos A, Emburey G, Versi E. Long-term effects of the menopause and sex hormones on skin thickness. Br J Obstet Gynaecol 1985, 92:256-259. 10.1111/j.1471-0528.1985.tb01091.x, 3978054.
46. Meschia M, Bruschi F, Amicarelli F, Barbacini P, Monza GC, Crosignani PG. Transdermal hormone replacement therapy and skin in postmenopausal women, a placebo controlled study. Menopause 1994, 1:79-82.
47. Maheux R, Naud F, Rioux M, Grenier R, Lemay A, Guy J, Langevin M. A randomized, double-blind, placebo-controlled study on the effect of conjugated estrogens on skin thickness. Am J Obstet Gynecol 1994, 170:642-649.
48. Castelo-Branco C, Duran M, Gonzalez-Merlo J. Skin collagen changes related to age and hormone replacement therapy. Maturitas 1992, 15:113-119. 10.1016/0378-5122(92)90245-Y, 1345134.
49. Kalogirou D, Aroni K, Kalogirou O, Antoniou G, Botsis D, Kontoravdis A. Histological changes induced by tibolone and estrogen/glucocorticoid on aging skin. Int J Fertil Womens Med 2000, 45:273-278.
50. Hall G, Phillips TJ. Estrogen and skin: the effects of estrogen, menopause, and hormone replacement therapy on the skin. J Am Acad Dermatol 2005, 53:555-568. 10.1016/j.jaad.2004.08.039, 16198774.
51. Charaee-Kermani M, Hatano K, Nozaki Y, Phan SH. Gender-based differences in bleomycin-induced pulmonary fibrosis. Am J Pathol 2005, 166:1593-1606. 10.1016/S0002-9440(10)62470-4, 1602429, 15920145.
52. Markiewicz M, Asano Y, Znoyko S, Gong Y, Watson DK, Trojanowska M. Distinct effects of gonadectomy in male and female mice on collagen fibrillogenesis in the skin. J Dermatol Sci 2007, 47:217-226. 10.1016/j.jdermsci.2007.05.008, 2717737, 17601707.
53. Inoue T, Miki Y, Abe K, Hatori M, Hosaka M, Kariya Y, Kakuo S, Fujimura T, Hachiya A, Honma S, Aiba S, Sasano H. Sex steroid synthesis in human skin in situ: the role of aromatase and steroidogenic acute regulatory protein in the homeostasis of human skin. Mol Cell Endocrinol 2012, 362:19-28. 10.1016/j.mce.2012.05.005, 22634420.
54. Cutolo M, Sulli A, Straub RH. Estrogen metabolism and autoimmunity. Autoimmun Rev 2012, 11:A460-A464. 10.1016/j.autrev.2011.11.014, 22155198.
55. Feghali CA, Bost KL, Boulware DW, Levy LS. Mechanisms of pathogenesis in scleroderma. I. Overproduction of interleukin 6 by fibroblasts cultured from affected skin sites of patients with scleroderma. J Rheumatol 1992, 19:1207-1211.