Inducers of G-protein coupled estrogen receptor (GPER) in endometriosis: Potential implications for macrophages and follicle maturation

Journal of Reproductive Immunology

Volumn 97, Issue 1, 2013, Pages 95-103

  Heublein, Sabine ^a   Vrekoussis, Thomas ^a   Kuhn, Christina ^a   Friese, Klaus ^a,b   Makrigiannakis, Antonis ^c   Mayr, Doris ^a   Lenhard, Miriam ^b   Jeschke, Udo ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^c UNIVERSITY OF CRETE   (Greece)

Author keywords

Endometriosis; GPER; Inflammation; Macrophages

Indexed keywords

CORTICOTROPIN; G PROTEIN COUPLED RECEPTOR 30; INTERLEUKIN 1BETA; PREDNISOLONE; PROSTAGLANDIN E2; TUMOR NECROSIS FACTOR ALPHA;

ADULT; ARTICLE; CONTROLLED STUDY; ENDOMETRIOSIS; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; MACROPHAGE; MAJOR CLINICAL STUDY; MICROENVIRONMENT; OVARY; OVARY FOLLICLE DEVELOPMENT; OVARY FOLLICLE MATURATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; STRESS; UPREGULATION; WESTERN BLOTTING;

ADRENOCORTICOTROPIC HORMONE; ADULT; CELL LINE, TUMOR; DINOPROSTONE; ENDOMETRIOSIS; ENDOMETRIUM; FEMALE; GENE EXPRESSION REGULATION; HUMANS; INFLAMMATION; INTERLEUKIN-1BETA; MIDDLE AGED; MOLECULAR TARGETED THERAPY; PREDNISOLONE; RECEPTORS, ESTROGEN; RECEPTORS, G-PROTEIN-COUPLED; STRESS, PSYCHOLOGICAL; TUMOR NECROSIS FACTOR-ALPHA; YOUNG ADULT;

EID: 84874513161     PISSN: 01650378     EISSN: 18727603     Source Type: Journal    
DOI: 10.1016/j.jri.2012.10.013     Document Type: Article

References (44)

1. Bacci M., Capobianco A., Monno A., Cottone L., Di puppo F., Camisa B., Mariani M., Brignole C., Ponzoni M., Ferrari S., Panina-Bordignon P., Manfredi A.A., Rovere-Querini P. Macrophages are alternatively activated in patients with endometriosis and required for growth and vascularization of lesions in a mouse model of disease. Am. J. Pathol. 2009, 175:547-556.
2. Capellino S., Montagna P., Villaggio B., Sulli A., Soldano S., Ferrero S., Remorgida V., Cutolo M. Role of estrogens in inflammatory response: expression of estrogen receptors in peritoneal fluid macrophages from endometriosis. Ann. N.Y. Acad. Sci. 2006, 1069:263-267.
3. Capobianco A., Monno A., Cottone L., Venneri M.A., Biziato D., Di Puppo F., Ferrari S., De Palma M., Manfredi A.A., Rovere-Querini P. Proangiogenic Tie2(+) macrophages infiltrate human and murine endometriotic lesions and dictate their growth in a mouse model of the disease. Am. J. Pathol. 2011, 179:2651-2659.
4. Cavallini A., Resta L., Caringella A.M., Dinaro E., Lippolis C., Loverro G. Involvement of estrogen receptor-related receptors in human ovarian endometriosis. Fertil. Steril. 2011, 96:102-106.
5. Chrousos G.P. Stress and disorders of the stress system. Nat. Rev. Endocrinol. 2009, 5:374-381.
6. Creus M., Fabregues F., Carmona F., Del Pino M., Manau D., Balasch J. Combined laparoscopic surgery and pentoxifylline therapy for treatment of endometriosis-associated infertility: a preliminary trial. Hum. Reprod. 2008, 23:1910-1916.
7. Cuevas M., Flores I., Thompson K.J., Ramos-Ortolaza D.L., Torres-Reveron A., Appleyard C.B. Stress exacerbates endometriosis manifestations and inflammatory parameters in an animal model. Reprod. Sci. 2012, 19:851-862.
8. Doody M.C., Gibbons W.E., Buttram V.C.J.R. Linear regression analysis of ultrasound follicular growth series: evidence for an abnormality of follicular growth in endometriosis patients. Fertil. Steril. 1988, 49:47-51.
9. Du G.Q., Zhou L., Chen X.Y., Wan X.P., He Y.Y. The G protein-coupled receptor GPR30 mediates the proliferative and invasive effects induced by hydroxytamoxifen in endometrial cancer cells. Biochem. Biophys. Res. Commun. 2012, 420:343-349.
10. Fagervold B., Jenssen M., Hummelshoj L., Moen M.H. Life after a diagnosis with endometriosis - a 15 years follow-up study. Acta Obstet. Gynecol. Scand. 2009, 88:914-919.
11. Filardo E.J., Graeber C.T., Quinn J.A., Resnick M.B., Giri D., Delellis R.A., Steinhoff M.M., Sabo E. Distribution of GPR30, a seven membrane-spanning estrogen receptor, in primary breast cancer and its association with clinicopathologic determinants of tumor progression. Clin. Cancer Res. 2006, 12:6359-6366.
12. Haber E., Danenberg H.D., Koroukhov N., Ron-el R., Golomb G., Schachter M. Peritoneal macrophage depletion by liposomal bisphosphonate attenuates endometriosis in the rat model. Hum. Reprod. 2009, 24:398-407.
13. Haller K., Salumets A., Uibo R. Anti-FSH antibodies associate with poor outcome of ovarian stimulation in IVF. Reprod. Biomed. Online 2008, 16:350-355.
14. Herington J.L., Crispens M.A., Carvalho-Macedo A.C., Camargos A.F., Lebovic D.I., Bruner-Tran K.L., Osteen K.G. Development and prevention of postsurgical adhesions in a chimeric mouse model of experimental endometriosis. Fertil. Steril. 2011, 95:1295-1301. e1.
15. Heublein S., Kazi S., Ogmundsdottir M.H., Attwood E.V., Kala S., Boyd C.A., Wilson C., Goberdhan D.C. Proton-assisted amino-acid transporters are conserved regulators of proliferation and amino-acid-dependent mTORC1 activation. Oncogene 2010, 29:4068-4079.
16. Heublein S., Lenhard M., Vrekoussis T., Schoepfer J., Kuhn C., Friese K., Makrigiannakis A., Mayr D., Jeschke U. The G-protein coupled estrogen receptor (GPER) is Expressed in normal human ovaries and is upregulated in ovarian endometriosis and pelvic inflammatory disease involving the ovary. Reprod. Sci. 2012, 19:1197-1204.
17. Kim D.J., Seok S.H., Baek M.W., Lee H.Y., Juhn J.H., Lee S., Yun M., Park J.H. Highly expressed recombinant human follicle-stimulating hormone from Chinese hamster ovary cells grown in serum-free medium and its effect on induction of folliculogenesis and ovulation. Fertil. Steril. 2010, 93:2652-2660.
18. Kim S.H., Lee H.W., Kim Y.H., Koo Y.H., Chae H.D., Kim C.H., Lee P.R., Kang B.M. Down-regulation of p21-activated kinase 1 by progestin and its increased expression in the eutopic endometrium of women with endometriosis. Hum. Reprod. 2009, 24:1133-1141.
19. Kitawaki J., Kado N., Ishihara H., Koshiba H., Kitaoka Y., Honjo H. Endometriosis: the pathophysiology as an estrogen-dependent disease. J. Steroid Biochem. Mol. Biol. 2002, 83:149-155.
20. Kitawaki J., Noguchi T., Amatsu T., Maeda K., Tsukamoto K., Yamamoto T., Fushiki S., Osawa Y., Honjo H. Expression of aromatase cytochrome P450 protein and messenger ribonucleic acid in human endometriotic and adenomyotic tissues but not in normal endometrium. Biol. Reprod. 1997, 57:514-519.
21. Kuroda M., Kuroda K., Arakawa A., Fukumura Y., Kitade M., Kikuchi I., Kumakiri J., Matsuoka S., Brosens I.A., Brosens J.J., Takeda S., Yao T. Histological assessment of impact of ovarian endometrioma and laparoscopic cystectomy on ovarian reserve. J. Obstet. Gynaecol. Res. 2012, 38:1187-1193.
22. Lachapelle M.H., Hemmings R., Roy D.C., Falcone T., Miron P. Flow cytometric evaluation of leukocyte subpopulations in the follicular fluids of infertile patients. Fertil. Steril. 1996, 65:1135-1140.
23. Lessey B.A., Palomino W.A., Apparao K.B., Young S.L., Lininger R.A. Estrogen receptor-alpha (ER-alpha) and defects in uterine receptivity in women. Reprod. Biol. Endocrinol. 2006, 4(Suppl. 1):S9.
24. Lima A.P., Moura M.D., Rosa e Silva A.A. Prolactin and cortisol levels in women with endometriosis. Braz. J. Med. Biol. Res. 2006, 39:1121-1127.
25. Melo M.L., Brito G.A., Soares R.C., Carvalho S.B., Silva J.V., Soares P.M., Vale M.L., Souza M.H., Cunha F.Q., Ribeiro R.A. Role of cytokines (TNF-alpha IL-1beta and KC) in the pathogenesis of CPT-11-induced intestinal mucositis in mice: effect of pentoxifylline and thalidomide. Cancer Chemother. Pharmacol. 2008, 61:775-784.
26. Moon C.E., Bertero M.C., Curry T.E., London S.N., Muse K.N., Sharpe K.L., Vernon M.W. The presence of luteinized unruptured follicle syndrome and altered folliculogenesis in rats with surgically induced endometriosis. Am. J. Obstet. Gynecol. 1993, 169:676-682.
27. Pavlik R., Wypior G., Hecht S., Papadopoulos P., Kupka M., Thaler C., Wiest I., Pestka A., Friese K., Jeschke U. Induction of G protein-coupled estrogen receptor (GPER) and nuclear steroid hormone receptors by gonadotropins in human granulosa cells. Histochem. Cell Biol. 2011, 136:289-299.
28. Plante B.J., Lessey B.A., Taylor R.N., Wang W., Bagchi M.K., Yuan L., Scotchie J., Fritz M.A., Young S.L. G protein-coupled estrogen receptor (GPER) expression in normal and abnormal endometrium. Reprod. Sci. 2012, 19:684-693.
29. Remmele W., Stegner H.E. Recommendation for uniform definition of an immunoreactive score (IRS) for immunohistochemical estrogen receptor detection (ER-ICA) in breast cancer tissue. Pathologe 1987, 8:138-140.
30. Revankar C.M., Cimino D.F., Sklar L.A., Arterburn J.B., Prossnitz E.R. A transmembrane intracellular estrogen receptor mediates rapid cell signaling. Science 2005, 307:1625-1630.
31. Samartzis N., Samartzis E.P., Noske A., Fedier A., Dedes K.J., Caduff R., Fink D., Imesch P. Expression of the G protein-coupled estrogen receptor (GPER) in endometriosis: a tissue microarray study. Reprod. Biol. Endocrinol. 2012, 10:30.
32. Siedentopf F., Tariverdian N., Rucke M., Kentenich H., Arck P.C. Immune status, psychosocial distress and reduced quality of life in infertile patients with endometriosis. Am. J. Reprod. Immunol. 2008, 60:449-461.
33. Smuc T., Hevir N., Ribic-Pucelj M., Husen B., Thole H., Rizner T.L. Disturbed estrogen and progesterone action in ovarian endometriosis. Mol. Cell. Endocrinol. 2009, 301:59-64.
34. Sokalska A., Wong D.H., Cress A., Piotrowski P.C., Rzepczynska I., Villanueva J., Duleba A.J. Simvastatin induces apoptosis and alters cytoskeleton in endometrial stromal cells. J. Clin. Endocrinol. Metab. 2010, 95:3453-3459.
35. Straub R.H. The complex role of estrogens in inflammation. Endocr. Rev. 2007, 28:521-574.
36. Struthers R.S., Nicholls A.J., Grundy J., Chen T., Jimenez R., Yen S.S., Bozigian H.P. Suppression of gonadotropins and estradiol in premenopausal women by oral administration of the nonpeptide gonadotropin-releasing hormone antagonist elagolix. J. Clin. Endocrinol. Metab. 2009, 94:545-551.
37. Tariverdian N., Theoharides T.C., Siedentopf F., Gutierrez G., Jeschke U., Rabinovich G.A., Blois S.M., Arck P.C. Neuroendocrine-immune disequilibrium and endometriosis: an interdisciplinary approach. Semin. Immunopathol. 2007, 29:193-210.
38. Tingen C.M., Kiesewetter S.E., Jozefik J., Thomas C., Tagler D., Shea L., Woodruff T.K. A macrophage and theca cell-enriched stromal cell population influences growth and survival of immature murine follicles in vitro. Reproduction 2011, 141:809-820.
39. Tsudo T., Harada T., Iwabe T., Tanikawa M., Nagano Y., Ito M., Taniguchi F., Terakawa N. Altered gene expression and secretion of interleukin-6 in stromal cells derived from endometriotic tissues. Fertil. Steril. 2000, 73:205-211.
40. Visser J., Van Boxel-Dezaire A., Methorst D., Brunt T., De Kloet E.R., Nagelkerken L. Differential regulation of interleukin-10 (IL-10) and IL-12 by glucocorticoids in vitro. Blood 1998, 91:4255-4264.
41. Wu R., Van der hoek K.H., Ryan N.K., Norman R.J., Robker R.L. Macrophage contributions to ovarian function. Hum. Reprod. Update 2004, 10:119-133.
42. Yamanaka K., Xu B., Suganuma I., Kusuki I., Mita S., Shimizu Y., Mizuguchi K., Kitawaki J. Dienogest inhibits aromatase and cyclooxygenase-2 expression and prostaglandin E(2) production in human endometriotic stromal cells in spheroid culture. Fertil. Steril. 2012, 97:477-482.
43. Yoshino O., Izumi G., Shi J., Osuga Y., Hirota Y., Hirata T., Harada M., Nishii O., Koga K., Taketani Y. Activin-A is induced by interleukin-1beta and tumor necrosis factor-alpha and enhances the mRNA expression of interleukin-6 and protease-activated receptor-2 and proliferation of stromal cells from endometrioma. Fertil. Steril. 2011, 96:118-121.
44. Zeitoun K., Takayama K., Michael M.D., Bulun S.E. Stimulation of aromatase P450 promoter (II) activity in endometriosis and its inhibition in endometrium are regulated by competitive binding of steroidogenic factor-1 and chicken ovalbumin upstream promoter transcription factor to the same cis-acting element. Mol. Endocrinol. 1999, 13:239-253.