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Published in: Reproductive Biology and Endocrinology 1/2010

Open Access 01-12-2010 | Research

Evidence of inhibin/activin subunit betaC and betaE synthesis in normal human endometrial tissue

Authors: Ioannis Mylonas, Ansgar Brüning, Naim Shabani, Susanne Kunze, Markus S Kupka

Published in: Reproductive Biology and Endocrinology | Issue 1/2010

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Abstract

Background

Inhibins are important regulators of the female reproductive system. Recently, two new inhibin subunits betaC and betaE have been described, although it is unclear if they are synthesized in normal human endometrium.

Methods

Samples of human endometrium were obtained from 82 premenopausal, non-pregnant patients undergoing gynecological surgery for benign diseases. Endometrium samples were classified according to anamnestic and histological dating into proliferative (day 1-14, n = 46), early secretory (day 15-22, n = 18) and late secretory phase (day 23-28, n = 18). Immunohistochemical analyses were performed with specific antibodies against inhibin alpha (n = 81) as well as inhibin betaA (n = 82), betaB (n = 82), betaC (n = 74) and betaE (n = 76) subunits. RT-PCR was performed for all inhibin subunits. Correlation was assessed with the Spearman factor to assess the relationship of inhibin-subunits expression within the different endometrial samples.

Results

The novel inhibin betaC and betaE subunits were found in normal human endometrium by immunohistochemical and molecular techniques. Inhibin alpha, betaA, betaB and betaE subunits showed a circadian expression pattern, being more abundant during the late secretory phase than during the proliferative phase. Additionally, a significant correlation between inhibin alpha and all inhibin beta subunits was observed.

Conclusions

The differential expression pattern of the betaC- and betaE-subunits in normal human endometrial tissue suggests that they function in endometrial maturation and blastocyst implantation. However, the precise role of these novel inhibin/activin subunits in human endometrium is unclear and warrants further investigation.
Appendix
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Literature
1.
go back to reference Chang H, Brown CW, Matzuk MM: Genetic analysis of the mammalian transforming growth factor-beta superfamily. Endocr Rev. 2002, 23 (6): 787-823. 10.1210/er.2002-0003.CrossRefPubMed Chang H, Brown CW, Matzuk MM: Genetic analysis of the mammalian transforming growth factor-beta superfamily. Endocr Rev. 2002, 23 (6): 787-823. 10.1210/er.2002-0003.CrossRefPubMed
2.
go back to reference Vale W, Wiater E, Gray P, Harrison C, Bilezikjian L, Choe S: Activins and inhibins and their signaling. Ann N Y Acad Sci. 2004, 1038: 142-147. 10.1196/annals.1315.023.CrossRefPubMed Vale W, Wiater E, Gray P, Harrison C, Bilezikjian L, Choe S: Activins and inhibins and their signaling. Ann N Y Acad Sci. 2004, 1038: 142-147. 10.1196/annals.1315.023.CrossRefPubMed
3.
go back to reference Xia Y, Schneyer AL: The biology of activin: recent advances in structure, regulation and function. J Endocrinol. 2009, 202 (1): 1-12. 10.1677/JOE-08-0549.PubMedCentralCrossRefPubMed Xia Y, Schneyer AL: The biology of activin: recent advances in structure, regulation and function. J Endocrinol. 2009, 202 (1): 1-12. 10.1677/JOE-08-0549.PubMedCentralCrossRefPubMed
4.
go back to reference Hötten G, Neidhardt H, Schneider C, Pohl J: Cloning of a new member of the TGF-beta family: a putative new activin beta C chain. Biochem Biophys Res Commun. 1995, 206 (2): 608-613. 10.1006/bbrc.1995.1086.CrossRef Hötten G, Neidhardt H, Schneider C, Pohl J: Cloning of a new member of the TGF-beta family: a putative new activin beta C chain. Biochem Biophys Res Commun. 1995, 206 (2): 608-613. 10.1006/bbrc.1995.1086.CrossRef
5.
go back to reference Hashimoto O, Tsuchida K, Ushiro Y, Hosoi Y, Hoshi N, Sugino H, Hasegawa Y: cDNA cloning and expression of human activin betaE subunit. Mol Cell Endocrinol. 2002, 194 (1-2): 117-122. 10.1016/S0303-7207(02)00157-0.CrossRefPubMed Hashimoto O, Tsuchida K, Ushiro Y, Hosoi Y, Hoshi N, Sugino H, Hasegawa Y: cDNA cloning and expression of human activin betaE subunit. Mol Cell Endocrinol. 2002, 194 (1-2): 117-122. 10.1016/S0303-7207(02)00157-0.CrossRefPubMed
6.
go back to reference Fang J, Yin W, Smiley E, Wang SQ, Bonadio J: Molecular cloning of the mouse activin beta E subunit gene. Biochem Biophys Res Commun. 1996, 228 (3): 669-674. 10.1006/bbrc.1996.1715.CrossRefPubMed Fang J, Yin W, Smiley E, Wang SQ, Bonadio J: Molecular cloning of the mouse activin beta E subunit gene. Biochem Biophys Res Commun. 1996, 228 (3): 669-674. 10.1006/bbrc.1996.1715.CrossRefPubMed
7.
go back to reference Fang J, Wang SQ, Smiley E, Bonadio J: Genes coding for mouse activin beta C and beta E are closely linked and exhibit a liver-specific expression pattern in adult tissues. Biochem Biophys Res Commun. 1997, 231 (3): 655-661. 10.1006/bbrc.1997.6162.CrossRefPubMed Fang J, Wang SQ, Smiley E, Bonadio J: Genes coding for mouse activin beta C and beta E are closely linked and exhibit a liver-specific expression pattern in adult tissues. Biochem Biophys Res Commun. 1997, 231 (3): 655-661. 10.1006/bbrc.1997.6162.CrossRefPubMed
8.
go back to reference Vejda S, Cranfield M, Peter B, Mellor SL, Groome N, Schulte-Hermann R, Rossmanith W: Expression and dimerization of the rat activin subunits betaC and betaE: evidence for the ormation of novel activin dimers. J Mol Endocrinol. 2002, 28 (2): 137-148. 10.1677/jme.0.0280137.CrossRefPubMed Vejda S, Cranfield M, Peter B, Mellor SL, Groome N, Schulte-Hermann R, Rossmanith W: Expression and dimerization of the rat activin subunits betaC and betaE: evidence for the ormation of novel activin dimers. J Mol Endocrinol. 2002, 28 (2): 137-148. 10.1677/jme.0.0280137.CrossRefPubMed
9.
go back to reference Petraglia F, Florio P, Luisi S, Gallo R, Gadducci A, Vigano P, Di Blasio AM, Genazzani AR, Vale W: Expression and secretion of inhibin and activin in normal and neoplastic uterine tissues. High levels of serum activin A in women with endometrial and cervical carcinoma. J Clin Endocrinol Metab. 1998, 83 (4): 1194-1200. 10.1210/jc.83.4.1194.PubMed Petraglia F, Florio P, Luisi S, Gallo R, Gadducci A, Vigano P, Di Blasio AM, Genazzani AR, Vale W: Expression and secretion of inhibin and activin in normal and neoplastic uterine tissues. High levels of serum activin A in women with endometrial and cervical carcinoma. J Clin Endocrinol Metab. 1998, 83 (4): 1194-1200. 10.1210/jc.83.4.1194.PubMed
10.
go back to reference Leung PH, Salamonsen LA, Findlay JK: Immunolocalization of inhibin and activin subunits in human endometrium across the menstrual cycle. Hum Reprod. 1998, 13 (12): 3469-3477. 10.1093/humrep/13.12.3469.CrossRefPubMed Leung PH, Salamonsen LA, Findlay JK: Immunolocalization of inhibin and activin subunits in human endometrium across the menstrual cycle. Hum Reprod. 1998, 13 (12): 3469-3477. 10.1093/humrep/13.12.3469.CrossRefPubMed
11.
go back to reference Mylonas I, Jeschke U, Wiest I, Hoeing A, Vogl J, Shabani N, Kuhn C, Schulze S, Kupka MS, Friese K: Inhibin/activin subunits alpha, beta-A and beta-B are differentially expressed in normal human endometrium throughout the menstrual cycle. Histochem Cell Biol. 2004, 122 (5): 461-471. 10.1007/s00418-004-0709-6.CrossRefPubMed Mylonas I, Jeschke U, Wiest I, Hoeing A, Vogl J, Shabani N, Kuhn C, Schulze S, Kupka MS, Friese K: Inhibin/activin subunits alpha, beta-A and beta-B are differentially expressed in normal human endometrium throughout the menstrual cycle. Histochem Cell Biol. 2004, 122 (5): 461-471. 10.1007/s00418-004-0709-6.CrossRefPubMed
12.
go back to reference Worbs S, Shabani N, Mayr D, Gingelmaier A, Makrigiannakis A, Kuhn C, Jeschke U, Kupka MS, Friese K, Mylonas I: Expression of the inhibin/activin subunits (-alpha, -betaA and -betaB) in normal and carcinogenic endometrial tissue: possible immunohistochemical differentiation markers. Oncol Rep. 2007, 17 (1): 97-104.PubMed Worbs S, Shabani N, Mayr D, Gingelmaier A, Makrigiannakis A, Kuhn C, Jeschke U, Kupka MS, Friese K, Mylonas I: Expression of the inhibin/activin subunits (-alpha, -betaA and -betaB) in normal and carcinogenic endometrial tissue: possible immunohistochemical differentiation markers. Oncol Rep. 2007, 17 (1): 97-104.PubMed
13.
go back to reference Mylonas I, Worbs S, Shabani N, Kuhn C, Kunze S, Schulze S, Dian D, Gingelmaier A, Schindlbeck C, Bruning A: Inhibin-alpha subunit is an independent prognostic parameter in human endometrial carcinomas: analysis of inhibin/activin-alpha, -betaA and -betaB subunits in 302 cases. Eur J Cancer. 2009, 45 (7): 1304-1314. 10.1016/j.ejca.2009.01.008.CrossRefPubMed Mylonas I, Worbs S, Shabani N, Kuhn C, Kunze S, Schulze S, Dian D, Gingelmaier A, Schindlbeck C, Bruning A: Inhibin-alpha subunit is an independent prognostic parameter in human endometrial carcinomas: analysis of inhibin/activin-alpha, -betaA and -betaB subunits in 302 cases. Eur J Cancer. 2009, 45 (7): 1304-1314. 10.1016/j.ejca.2009.01.008.CrossRefPubMed
14.
go back to reference Mylonas I, Makovitzky J, Fernow A, Richter DU, Jeschke U, Briese V, Gerber B, Friese K: Expression of the inhibin/activin subunits alpha (alpha), beta-A (betaA) and beta-B (betaB) in benign human endometrial polyps and tamoxifen-associated polyps. Arch Gynecol Obstet. 2005, 272 (1): 59-66. 10.1007/s00404-004-0666-2.CrossRefPubMed Mylonas I, Makovitzky J, Fernow A, Richter DU, Jeschke U, Briese V, Gerber B, Friese K: Expression of the inhibin/activin subunits alpha (alpha), beta-A (betaA) and beta-B (betaB) in benign human endometrial polyps and tamoxifen-associated polyps. Arch Gynecol Obstet. 2005, 272 (1): 59-66. 10.1007/s00404-004-0666-2.CrossRefPubMed
15.
go back to reference Mylonas I, Makovitzky J, Hoeing A, Richter DU, Vogl J, Schulze S, Jeschke U, Briese V, Friese K: Inhibin/activin subunits beta-A (-betaA) and beta-B (-betaB) are differentially localised in normal, hyperplastic and malignant human endometrial tissue. Acta Histochem. 2006, 108 (1): 1-11. 10.1016/j.acthis.2005.11.002.CrossRefPubMed Mylonas I, Makovitzky J, Hoeing A, Richter DU, Vogl J, Schulze S, Jeschke U, Briese V, Friese K: Inhibin/activin subunits beta-A (-betaA) and beta-B (-betaB) are differentially localised in normal, hyperplastic and malignant human endometrial tissue. Acta Histochem. 2006, 108 (1): 1-11. 10.1016/j.acthis.2005.11.002.CrossRefPubMed
16.
go back to reference de Kretser DM, Hedger MP, Loveland KL, Phillips DJ: Inhibins, activins and follistatin in reproduction. Hum Reprod Update. 2002, 8 (6): 529-541. 10.1093/humupd/8.6.529.CrossRefPubMed de Kretser DM, Hedger MP, Loveland KL, Phillips DJ: Inhibins, activins and follistatin in reproduction. Hum Reprod Update. 2002, 8 (6): 529-541. 10.1093/humupd/8.6.529.CrossRefPubMed
17.
go back to reference Welt C, Sidis Y, Keutmann H, Schneyer A: Activins, inhibins, and follistatins: from endocrinology to signaling. A paradigm for the new millennium. Exp Biol Med (Maywood). 2002, 227 (9): 724-752. Welt C, Sidis Y, Keutmann H, Schneyer A: Activins, inhibins, and follistatins: from endocrinology to signaling. A paradigm for the new millennium. Exp Biol Med (Maywood). 2002, 227 (9): 724-752.
18.
go back to reference Risbridger GP, Schmitt JF, Robertson DM: Activins and inhibins in endocrine and other tumors. Endocr Rev. 2001, 22 (6): 836-858. 10.1210/er.22.6.836.CrossRefPubMed Risbridger GP, Schmitt JF, Robertson DM: Activins and inhibins in endocrine and other tumors. Endocr Rev. 2001, 22 (6): 836-858. 10.1210/er.22.6.836.CrossRefPubMed
19.
go back to reference Sugawara K, Kizaki K, Herath CB, Hasegawa Y, Hashizume K: Transforming growth factor beta family expression at the bovine feto-maternal interface. Reprod Biol Endocrinol. 2010, 8 (1): 120-10.1186/1477-7827-8-120.PubMedCentralCrossRefPubMed Sugawara K, Kizaki K, Herath CB, Hasegawa Y, Hashizume K: Transforming growth factor beta family expression at the bovine feto-maternal interface. Reprod Biol Endocrinol. 2010, 8 (1): 120-10.1186/1477-7827-8-120.PubMedCentralCrossRefPubMed
20.
go back to reference Stoikos CJ, Salamonsen LA, Hannan NJ, O'Connor AE, Rombauts L, Dimitriadis E: Activin A regulates trophoblast cell adhesive properties: implications for implantation failure in women with endometriosis-associated infertility. Hum Reprod. 2010, 25 (7): 1767-1774. 10.1093/humrep/deq097.CrossRefPubMed Stoikos CJ, Salamonsen LA, Hannan NJ, O'Connor AE, Rombauts L, Dimitriadis E: Activin A regulates trophoblast cell adhesive properties: implications for implantation failure in women with endometriosis-associated infertility. Hum Reprod. 2010, 25 (7): 1767-1774. 10.1093/humrep/deq097.CrossRefPubMed
21.
go back to reference Florio P, Gabbanini M, Borges LE, Bonaccorsi L, Pinzauti S, Reis FM, Boy Torres P, Rago G, Litta P, Petraglia F: Activins and related proteins in the establishment of pregnancy. Reprod Sci. 2010, 17 (4): 320-330. 10.1177/1933719109353205.CrossRefPubMed Florio P, Gabbanini M, Borges LE, Bonaccorsi L, Pinzauti S, Reis FM, Boy Torres P, Rago G, Litta P, Petraglia F: Activins and related proteins in the establishment of pregnancy. Reprod Sci. 2010, 17 (4): 320-330. 10.1177/1933719109353205.CrossRefPubMed
22.
go back to reference Jones RL, Findlay JK, Farnworth PG, Robertson DM, Wallace E, Salamonsen LA: Activin A and inhibin A differentially regulate human uterine matrix metalloproteinases: potential interactions during decidualization and trophoblast invasion. Endocrinology. 2006, 147 (2): 724-732. 10.1210/en.2005-1183.CrossRefPubMed Jones RL, Findlay JK, Farnworth PG, Robertson DM, Wallace E, Salamonsen LA: Activin A and inhibin A differentially regulate human uterine matrix metalloproteinases: potential interactions during decidualization and trophoblast invasion. Endocrinology. 2006, 147 (2): 724-732. 10.1210/en.2005-1183.CrossRefPubMed
23.
go back to reference Jones RL, Salamonsen LA, Findlay JK: Potential roles for endometrial inhibins, activins and follistatin during human embryo implantation and early pregnancy. Trends Endocrinol Metab. 2002, 13 (4): 144-150. 10.1016/S1043-2760(01)00559-8.CrossRefPubMed Jones RL, Salamonsen LA, Findlay JK: Potential roles for endometrial inhibins, activins and follistatin during human embryo implantation and early pregnancy. Trends Endocrinol Metab. 2002, 13 (4): 144-150. 10.1016/S1043-2760(01)00559-8.CrossRefPubMed
24.
go back to reference Dimitriadis E, White CA, Jones RL, Salamonsen LA: Cytokines, chemokines and growth factors in endometrium related to implantation. Hum Reprod Update. 2005, 11 (6): 613-30. 10.1093/humupd/dmi023.CrossRefPubMed Dimitriadis E, White CA, Jones RL, Salamonsen LA: Cytokines, chemokines and growth factors in endometrium related to implantation. Hum Reprod Update. 2005, 11 (6): 613-30. 10.1093/humupd/dmi023.CrossRefPubMed
25.
go back to reference Florio P, Bruni L, Galleri L, Reis FM, Borges LE, Bocchi C, Litta P, De Leo V, Petraglia F: Evaluation of endometrial activin A secretion for prediction of pregnancy after intrauterine insemination. Fertil Steril. 2009, 93 (7): 2316-2320. 10.1016/j.fertnstert.2008.12.125.CrossRefPubMed Florio P, Bruni L, Galleri L, Reis FM, Borges LE, Bocchi C, Litta P, De Leo V, Petraglia F: Evaluation of endometrial activin A secretion for prediction of pregnancy after intrauterine insemination. Fertil Steril. 2009, 93 (7): 2316-2320. 10.1016/j.fertnstert.2008.12.125.CrossRefPubMed
26.
go back to reference Chang HJ, Lee JH, Hwang KJ, Kim MR, Chang KH, Park DW, Min CK: Transforming growth factor (TGF)-beta1-induced human endometrial stromal cell decidualization through extracellular signal-regulated kinase and Smad activation in vitro: peroxisome proliferator-activated receptor gamma acts as a negative regulator of TGF-beta1. Fertil Steril. 2008, 90 (4 Suppl): 1357-1365. 10.1016/j.fertnstert.2007.09.010.CrossRefPubMed Chang HJ, Lee JH, Hwang KJ, Kim MR, Chang KH, Park DW, Min CK: Transforming growth factor (TGF)-beta1-induced human endometrial stromal cell decidualization through extracellular signal-regulated kinase and Smad activation in vitro: peroxisome proliferator-activated receptor gamma acts as a negative regulator of TGF-beta1. Fertil Steril. 2008, 90 (4 Suppl): 1357-1365. 10.1016/j.fertnstert.2007.09.010.CrossRefPubMed
27.
go back to reference Mellor SL, Cranfield M, Ries R, Pedersen J, Cancilla B, de Kretser D, Groome NP, Mason AJ, Risbridger GP: Localization of activin beta(A)-, beta(B)-, and beta(C)-subunits in humanprostate and evidence for formation of new activin heterodimers of beta(C)-subunit. J Clin Endocrinol Metab. 2000, 85 (12): 4851-4858. 10.1210/jc.85.12.4851.PubMed Mellor SL, Cranfield M, Ries R, Pedersen J, Cancilla B, de Kretser D, Groome NP, Mason AJ, Risbridger GP: Localization of activin beta(A)-, beta(B)-, and beta(C)-subunits in humanprostate and evidence for formation of new activin heterodimers of beta(C)-subunit. J Clin Endocrinol Metab. 2000, 85 (12): 4851-4858. 10.1210/jc.85.12.4851.PubMed
28.
go back to reference Mylonas I, Makovitzky J, Kunze S, Brüning A, Kainer F, Schiessl B: Inhibin-betaC subunit expression in normal and pathological human placental tissues. Syst Biol Reprod Med. 2010 Mylonas I, Makovitzky J, Kunze S, Brüning A, Kainer F, Schiessl B: Inhibin-betaC subunit expression in normal and pathological human placental tissues. Syst Biol Reprod Med. 2010
29.
go back to reference Weissenbacher T, Bruning A, Kimmich T, Makovitzky J, Gingelmaier A, Mylonas I: Immunohistochemical labeling of the inhibin/activin betaC subunit in normal human placental tissue and chorionic carcinoma cell lines. J Histochem Cytochem. 2010, 58 (8): 751-757. 10.1369/jhc.2010.956185.PubMedCentralCrossRefPubMed Weissenbacher T, Bruning A, Kimmich T, Makovitzky J, Gingelmaier A, Mylonas I: Immunohistochemical labeling of the inhibin/activin betaC subunit in normal human placental tissue and chorionic carcinoma cell lines. J Histochem Cytochem. 2010, 58 (8): 751-757. 10.1369/jhc.2010.956185.PubMedCentralCrossRefPubMed
30.
go back to reference Käufl SD, Makovitzky J, Kuhn C, Kunze S, Jeschke U, Mylonas I: Inhibin/activin-betaC subunit in human endometrial adenocarcinomas and HEC-1a adenocarcinoma cell line. In Vivo. 2010, 282: 185-191. Käufl SD, Makovitzky J, Kuhn C, Kunze S, Jeschke U, Mylonas I: Inhibin/activin-betaC subunit in human endometrial adenocarcinomas and HEC-1a adenocarcinoma cell line. In Vivo. 2010, 282: 185-191.
31.
go back to reference Kimmich T, Bruning A, Kaufl SD, Makovitzky J, Kuhn C, Jeschke U, Friese K, Mylonas I: Inhibin/activin-betaC and -betaE subunits in the Ishikawa human endometrial adenocarcinoma cell line. Arch Gynecol Obstet. 2010, 282 (2): 185-191. 10.1007/s00404-009-1310-y.CrossRefPubMed Kimmich T, Bruning A, Kaufl SD, Makovitzky J, Kuhn C, Jeschke U, Friese K, Mylonas I: Inhibin/activin-betaC and -betaE subunits in the Ishikawa human endometrial adenocarcinoma cell line. Arch Gynecol Obstet. 2010, 282 (2): 185-191. 10.1007/s00404-009-1310-y.CrossRefPubMed
32.
go back to reference Käufl SD, Kuhn C, Kunze S, Shabani N, Bruning A, Friese K, Mylonas I: Inhibin/activin-betaC subunit does not represent a prognostic parameter in human endometrial cancer. Arch Gynecol Obstet. 2010 Käufl SD, Kuhn C, Kunze S, Shabani N, Bruning A, Friese K, Mylonas I: Inhibin/activin-betaC subunit does not represent a prognostic parameter in human endometrial cancer. Arch Gynecol Obstet. 2010
33.
go back to reference Blankenstein TJF, Jückstock JK, Shabani N, Kunze S, Brüning A, Bergauer F, Mylonas I: Immunolabelling of the inhibin/activin-betaC subunit in normal and malignant human uterine cervical tissue and cervical cancer cell lines. Oncol Rep. 2010 Blankenstein TJF, Jückstock JK, Shabani N, Kunze S, Brüning A, Bergauer F, Mylonas I: Immunolabelling of the inhibin/activin-betaC subunit in normal and malignant human uterine cervical tissue and cervical cancer cell lines. Oncol Rep. 2010
34.
go back to reference Gingelmaier A, Bruning A, Kimmich T, Makovitzky J, Bergauer F, Schiessl B, Friese K, Mylonas I: Inhibin/activin-betaE subunit is expressed in normal and pathological human placental tissue including chorionic carcinoma cell lines. Arch Gynecol Obstet. 2010 Gingelmaier A, Bruning A, Kimmich T, Makovitzky J, Bergauer F, Schiessl B, Friese K, Mylonas I: Inhibin/activin-betaE subunit is expressed in normal and pathological human placental tissue including chorionic carcinoma cell lines. Arch Gynecol Obstet. 2010
35.
go back to reference Mylonas I, Shabani N, Vogl J, Makovitzky J, Kunze S, Kuhn C, Schulze S, Friese K, Jeschke U: Inhibin/activin subunits are immunohistochemically expressed in complete and partial hydatidiform moles. Anticancer Res. 2007, 27 (4A): 1995-2000.PubMed Mylonas I, Shabani N, Vogl J, Makovitzky J, Kunze S, Kuhn C, Schulze S, Friese K, Jeschke U: Inhibin/activin subunits are immunohistochemically expressed in complete and partial hydatidiform moles. Anticancer Res. 2007, 27 (4A): 1995-2000.PubMed
36.
go back to reference Bergauer F, Bruning A, Shabani N, Blankenstein T, Juckstock J, Dian D, Mylonas I: Inhibin/activin-betaE subunit in normal and malignant human cervical tissue and cervical cancer cell lines. J Mol Histol. 2009, 40 (5-6): 353-359. 10.1007/s10735-009-9246-x.CrossRefPubMed Bergauer F, Bruning A, Shabani N, Blankenstein T, Juckstock J, Dian D, Mylonas I: Inhibin/activin-betaE subunit in normal and malignant human cervical tissue and cervical cancer cell lines. J Mol Histol. 2009, 40 (5-6): 353-359. 10.1007/s10735-009-9246-x.CrossRefPubMed
37.
go back to reference Tsuchida K, Nakatani M, Hitachi K, Uezumi A, Sunada Y, Ageta H, Inokuchi K: Activin signaling as an emerging target for therapeutic interventions. Cell Commun Signal. 2009, 7: 15-PubMedCentralCrossRefPubMed Tsuchida K, Nakatani M, Hitachi K, Uezumi A, Sunada Y, Ageta H, Inokuchi K: Activin signaling as an emerging target for therapeutic interventions. Cell Commun Signal. 2009, 7: 15-PubMedCentralCrossRefPubMed
38.
go back to reference Mylonas I, Jeschke U, Kunert-Keil C, Shabani N, Dian D, Bauerfeind I, Kuhn C, Kupka MS, Friese K: Glycodelin A is expressed differentially in normal human endometrial tissue throughout the menstrual cycle as assessed by immunohistochemistry and in situ hybridization. Fertil Steril. 2006, 86 (5): 1488-1497. 10.1016/j.fertnstert.2006.03.062.CrossRefPubMed Mylonas I, Jeschke U, Kunert-Keil C, Shabani N, Dian D, Bauerfeind I, Kuhn C, Kupka MS, Friese K: Glycodelin A is expressed differentially in normal human endometrial tissue throughout the menstrual cycle as assessed by immunohistochemistry and in situ hybridization. Fertil Steril. 2006, 86 (5): 1488-1497. 10.1016/j.fertnstert.2006.03.062.CrossRefPubMed
39.
go back to reference Noyes RW, Hertig AT, Rock J: Dating the endometrial biopsy. Fertil Steril. 1950, 1: 3-15. Noyes RW, Hertig AT, Rock J: Dating the endometrial biopsy. Fertil Steril. 1950, 1: 3-15.
40.
go back to reference Mylonas I, Speer R, Makovitzky J, Richter DU, Briese V, Jeschke U, Friese K: Immunohistochemical analysis of steroid receptors and glycodelin A (PP14) in isolated glandular epithelial cells of normal human endometrium. Histochem Cell Biol. 2000, 114 (5): 405-411.PubMed Mylonas I, Speer R, Makovitzky J, Richter DU, Briese V, Jeschke U, Friese K: Immunohistochemical analysis of steroid receptors and glycodelin A (PP14) in isolated glandular epithelial cells of normal human endometrium. Histochem Cell Biol. 2000, 114 (5): 405-411.PubMed
41.
go back to reference Mylonas I, Makovitzky J, Shabani N, Gingelmaier A, Dian D, Kuhn C, Schulze S, Kunze S, Jeschke U, Friese K: Development and characterisation of an antibody for the immunohistochemical detection of inhibin/activin betaE (betaE) in normal human ovarian and placental tissue. Acta Histochem. 2009, 111 (4): 366-371.PubMed Mylonas I, Makovitzky J, Shabani N, Gingelmaier A, Dian D, Kuhn C, Schulze S, Kunze S, Jeschke U, Friese K: Development and characterisation of an antibody for the immunohistochemical detection of inhibin/activin betaE (betaE) in normal human ovarian and placental tissue. Acta Histochem. 2009, 111 (4): 366-371.PubMed
42.
go back to reference Mylonas I: Inhibin-alpha, -betaA and -betaB subunits in uterine non-endometrioid carcinomas: Prognostic significance and clinical implications. Eur J Cancer. 2010, 46 (13): 2485-2493. 10.1016/j.ejca.2010.06.001.CrossRefPubMed Mylonas I: Inhibin-alpha, -betaA and -betaB subunits in uterine non-endometrioid carcinomas: Prognostic significance and clinical implications. Eur J Cancer. 2010, 46 (13): 2485-2493. 10.1016/j.ejca.2010.06.001.CrossRefPubMed
43.
go back to reference Mylonas I: Inhibin-betaA subunit immunolabeling as a prognostic factor in endometrioid adenocarcinomas: a matter of evaluation?. Arch Gynecol Obstet. 2010 Mylonas I: Inhibin-betaA subunit immunolabeling as a prognostic factor in endometrioid adenocarcinomas: a matter of evaluation?. Arch Gynecol Obstet. 2010
44.
go back to reference Mylonas I, Jeschke U, Shabani N, Kuhn C, Friese K, Gerber B: Inhibin/activin subunits (inhibin-alpha, -betaA and -betaB) are differentially expressed in human breast cancer and their metastasis. Oncol Rep. 2005, 13 (1): 81-88.PubMed Mylonas I, Jeschke U, Shabani N, Kuhn C, Friese K, Gerber B: Inhibin/activin subunits (inhibin-alpha, -betaA and -betaB) are differentially expressed in human breast cancer and their metastasis. Oncol Rep. 2005, 13 (1): 81-88.PubMed
45.
go back to reference Jückstock K, Brüning A, Blankenstein T, Kunze S, Shaban N, Bergauer F, Mylonas I: Immunolabelling of the inhibin-betaA and -betaB subunit in normal and malignant human cervical tissue and cervical cancer cell line. Int J Gynecol Cancer. 2010, 20 (7): 1177-1125.CrossRef Jückstock K, Brüning A, Blankenstein T, Kunze S, Shaban N, Bergauer F, Mylonas I: Immunolabelling of the inhibin-betaA and -betaB subunit in normal and malignant human cervical tissue and cervical cancer cell line. Int J Gynecol Cancer. 2010, 20 (7): 1177-1125.CrossRef
46.
go back to reference Mylonas I, Schiessl B, Jeschke U, Vogl J, Makrigiannakis A, Kuhn C, Kunze S, Schulze S, Kainer F, Friese K: Expression of inhibin/activin subunits alpha (-alpha), beta A (-beta (A)) and beta B (-beta (B)) in placental tissue of normal and intrauterine growth restricted (IUGR) pregnancies. J Mol Histol. 2006, 37 (1-2): 43-52. 10.1007/s10735-006-9029-6.CrossRefPubMed Mylonas I, Schiessl B, Jeschke U, Vogl J, Makrigiannakis A, Kuhn C, Kunze S, Schulze S, Kainer F, Friese K: Expression of inhibin/activin subunits alpha (-alpha), beta A (-beta (A)) and beta B (-beta (B)) in placental tissue of normal and intrauterine growth restricted (IUGR) pregnancies. J Mol Histol. 2006, 37 (1-2): 43-52. 10.1007/s10735-006-9029-6.CrossRefPubMed
47.
go back to reference Mylonas I, Schiessl B, Jeschke U, Vogl J, Makrigiannakis A, Kuhn C, Schulze S, Kainer F, Friese K: Expression of inhibin/activin subunits alpha (-alpha), betaA (-betaA), and betaB (-betaB) in placental tissue of normal, preeclamptic, and HELLP pregnancies. Endocr Pathol. 2006, 17 (1): 19-33. 10.1385/EP:17:1:19.CrossRefPubMed Mylonas I, Schiessl B, Jeschke U, Vogl J, Makrigiannakis A, Kuhn C, Schulze S, Kainer F, Friese K: Expression of inhibin/activin subunits alpha (-alpha), betaA (-betaA), and betaB (-betaB) in placental tissue of normal, preeclamptic, and HELLP pregnancies. Endocr Pathol. 2006, 17 (1): 19-33. 10.1385/EP:17:1:19.CrossRefPubMed
48.
go back to reference Lau AL, Kumar TR, Nishimori K, Bonadio J, Matzuk MM: Activin betaC and betaE genes are not essential for mouse liver growth, differentiation, and regeneration. Mol Cell Biol. 2000, 20 (16): 6127-6137. 10.1128/MCB.20.16.6127-6137.2000.PubMedCentralCrossRefPubMed Lau AL, Kumar TR, Nishimori K, Bonadio J, Matzuk MM: Activin betaC and betaE genes are not essential for mouse liver growth, differentiation, and regeneration. Mol Cell Biol. 2000, 20 (16): 6127-6137. 10.1128/MCB.20.16.6127-6137.2000.PubMedCentralCrossRefPubMed
49.
go back to reference Ferreira MC, Cavallo IK, Florio P, Petraglia F, Reis FM: Activin betaA subunit, follistatin and follistatin-like 3 are expressed in the endometrium of ovariectomized rats and regulated by estrogen replacement. J Mol Histol. 2008, 39 (5): 535-541. 10.1007/s10735-008-9194-x.CrossRefPubMed Ferreira MC, Cavallo IK, Florio P, Petraglia F, Reis FM: Activin betaA subunit, follistatin and follistatin-like 3 are expressed in the endometrium of ovariectomized rats and regulated by estrogen replacement. J Mol Histol. 2008, 39 (5): 535-541. 10.1007/s10735-008-9194-x.CrossRefPubMed
50.
go back to reference Ni X, Luo S, Minegishi T, Peng C: Activin A in JEG-3 cells: potential role as an autocrine regulator of steroidogenesis in humans. Biol Reprod. 2000, 62 (5): 1224-1230. 10.1095/biolreprod62.5.1224.CrossRefPubMed Ni X, Luo S, Minegishi T, Peng C: Activin A in JEG-3 cells: potential role as an autocrine regulator of steroidogenesis in humans. Biol Reprod. 2000, 62 (5): 1224-1230. 10.1095/biolreprod62.5.1224.CrossRefPubMed
51.
go back to reference Menkhorst E, Salamonsen LA, Zhang J, Harrison CA, Gu J, Dimitriadis E: Interleukin 11 and activin A synergise to regulate progesterone-induced but not cAMP-induced decidualization. J Reprod Immunol. 2010, 84 (2): 124-132. 10.1016/j.jri.2009.12.001.CrossRefPubMed Menkhorst E, Salamonsen LA, Zhang J, Harrison CA, Gu J, Dimitriadis E: Interleukin 11 and activin A synergise to regulate progesterone-induced but not cAMP-induced decidualization. J Reprod Immunol. 2010, 84 (2): 124-132. 10.1016/j.jri.2009.12.001.CrossRefPubMed
52.
go back to reference Caniggia I, Lye SJ, Cross JC: Activin is a local regulator of human cytotrophoblast cell differentiation. Endocrinology. 1997, 138 (9): 3976-3986. 10.1210/en.138.9.3976.PubMed Caniggia I, Lye SJ, Cross JC: Activin is a local regulator of human cytotrophoblast cell differentiation. Endocrinology. 1997, 138 (9): 3976-3986. 10.1210/en.138.9.3976.PubMed
53.
go back to reference Keelan JA, Zhou RL, Mitchell MD: Activin A exerts both pro- and anti-inflammatory effects on human term gestational tissues. Placenta. 2000, 21 (1): 38-43. 10.1053/plac.1999.0451.CrossRefPubMed Keelan JA, Zhou RL, Mitchell MD: Activin A exerts both pro- and anti-inflammatory effects on human term gestational tissues. Placenta. 2000, 21 (1): 38-43. 10.1053/plac.1999.0451.CrossRefPubMed
54.
go back to reference Beattie GM, Lopez AD, Bucay N, Hinton A, Firpo MT, King CC, Hayek A: Activin A maintains pluripotency of human embryonic stem cells in the absence of feeder layers. Stem Cells. 2005, 23 (4): 489-495. 10.1634/stemcells.2004-0279.CrossRefPubMed Beattie GM, Lopez AD, Bucay N, Hinton A, Firpo MT, King CC, Hayek A: Activin A maintains pluripotency of human embryonic stem cells in the absence of feeder layers. Stem Cells. 2005, 23 (4): 489-495. 10.1634/stemcells.2004-0279.CrossRefPubMed
55.
go back to reference Sulzbacher S, Schroeder IS, Truong TT, Wobus AM: Activin A-Induced Differentiation of Embryonic Stem Cells into Endoderm and Pancreatic Progenitors-The Influence of Differentiation Factors and Culture Conditions. Stem Cell Rev. 2009, 5 (2): 159-173. 10.1007/s12015-009-9061-5.CrossRefPubMed Sulzbacher S, Schroeder IS, Truong TT, Wobus AM: Activin A-Induced Differentiation of Embryonic Stem Cells into Endoderm and Pancreatic Progenitors-The Influence of Differentiation Factors and Culture Conditions. Stem Cell Rev. 2009, 5 (2): 159-173. 10.1007/s12015-009-9061-5.CrossRefPubMed
56.
go back to reference Chen YG, Lui HM, Lin SL, Lee JM, Ying SY: Regulation of cell proliferation, apoptosis, and carcinogenesis by activin. Exp Biol Med (Maywood). 2002, 227 (2): 75-87. Chen YG, Lui HM, Lin SL, Lee JM, Ying SY: Regulation of cell proliferation, apoptosis, and carcinogenesis by activin. Exp Biol Med (Maywood). 2002, 227 (2): 75-87.
57.
go back to reference Esquela AF, Zimmers TA, Koniaris LG, Sitzmann JV, Lee SJ: Transient down-regulation of inhibin-betaC expression following partial hepatectomy. Biochem Biophys Res Commun. 1997, 235 (3): 553-556. 10.1006/bbrc.1997.6850.CrossRefPubMed Esquela AF, Zimmers TA, Koniaris LG, Sitzmann JV, Lee SJ: Transient down-regulation of inhibin-betaC expression following partial hepatectomy. Biochem Biophys Res Commun. 1997, 235 (3): 553-556. 10.1006/bbrc.1997.6850.CrossRefPubMed
58.
go back to reference Zhang YQ, Shibata H, Schrewe H, Kojima I: Reciprocal expression of mRNA for inhibin betaC and betaA subunits in hepatocytes. Endocr J. 1997, 44 (5): 759-764. 10.1507/endocrj.44.759.CrossRefPubMed Zhang YQ, Shibata H, Schrewe H, Kojima I: Reciprocal expression of mRNA for inhibin betaC and betaA subunits in hepatocytes. Endocr J. 1997, 44 (5): 759-764. 10.1507/endocrj.44.759.CrossRefPubMed
59.
go back to reference Ushiro Y, Hashimoto O, Seki M, Hachiya A, Shoji H, Hasegawa Y: Analysis of the Function of Activin beta(C) Subunit Using Recombinant Protein. J Reprod Dev. 2006, 52 (4): 487-495. 10.1262/jrd.17110.CrossRefPubMed Ushiro Y, Hashimoto O, Seki M, Hachiya A, Shoji H, Hasegawa Y: Analysis of the Function of Activin beta(C) Subunit Using Recombinant Protein. J Reprod Dev. 2006, 52 (4): 487-495. 10.1262/jrd.17110.CrossRefPubMed
60.
go back to reference Chabicovsky M, Herkner K, Rossmanith W: Overexpression of activin beta(C) or activin beta(E) in the mouse liver inhibits regenerative deoxyribonucleic acid synthesis of hepatic cells. Endocrinology. 2003, 144 (8): 3497-3504. 10.1210/en.2003-0388.CrossRefPubMed Chabicovsky M, Herkner K, Rossmanith W: Overexpression of activin beta(C) or activin beta(E) in the mouse liver inhibits regenerative deoxyribonucleic acid synthesis of hepatic cells. Endocrinology. 2003, 144 (8): 3497-3504. 10.1210/en.2003-0388.CrossRefPubMed
61.
go back to reference Vejda S, Erlach N, Peter B, Drucker C, Rossmanith W, Pohl J, Schulte-Hermann R, Grusch M: Expression of activins C and E induces apoptosis in human and rat hepatoma cells. Carcinogenesis. 2003, 24 (11): 1801-1809. 10.1093/carcin/bgg154.CrossRefPubMed Vejda S, Erlach N, Peter B, Drucker C, Rossmanith W, Pohl J, Schulte-Hermann R, Grusch M: Expression of activins C and E induces apoptosis in human and rat hepatoma cells. Carcinogenesis. 2003, 24 (11): 1801-1809. 10.1093/carcin/bgg154.CrossRefPubMed
62.
go back to reference Wada W, Medina JJ, Kuwano H, Kojima I: Comparison of the function of the beta(C) and beta(E) subunits of activin in AML12 hepatocytes. Endocr J. 2005, 52 (2): 169-175. 10.1507/endocrj.52.169.CrossRefPubMed Wada W, Medina JJ, Kuwano H, Kojima I: Comparison of the function of the beta(C) and beta(E) subunits of activin in AML12 hepatocytes. Endocr J. 2005, 52 (2): 169-175. 10.1507/endocrj.52.169.CrossRefPubMed
63.
go back to reference Gold EJ, Zhang X, Wheatley AM, Mellor SL, Cranfield M, Risbridger GP, Groome NP, Fleming JS: betaA- and betaC-activin, follistatin, activin receptor mRNA and betaC-activin peptide expression during rat liver regeneration. J Mol Endocrinol. 2005, 34 (2): 505-515. 10.1677/jme.1.01657.CrossRefPubMed Gold EJ, Zhang X, Wheatley AM, Mellor SL, Cranfield M, Risbridger GP, Groome NP, Fleming JS: betaA- and betaC-activin, follistatin, activin receptor mRNA and betaC-activin peptide expression during rat liver regeneration. J Mol Endocrinol. 2005, 34 (2): 505-515. 10.1677/jme.1.01657.CrossRefPubMed
64.
go back to reference Gold E, Jetly N, O'Bryan MK, Meachem S, Srinivasan D, Behuria S, Sanchez-Partida LG, Woodruff T, Hedwards S, Wang H: Activin C antagonizes activin A in vitro and overexpression leads to pathologies in vivo. Am J Pathol. 2009, 174 (1): 184-195. 10.2353/ajpath.2009.080296.PubMedCentralCrossRefPubMed Gold E, Jetly N, O'Bryan MK, Meachem S, Srinivasan D, Behuria S, Sanchez-Partida LG, Woodruff T, Hedwards S, Wang H: Activin C antagonizes activin A in vitro and overexpression leads to pathologies in vivo. Am J Pathol. 2009, 174 (1): 184-195. 10.2353/ajpath.2009.080296.PubMedCentralCrossRefPubMed
65.
go back to reference Mellor SL, Ball EM, O'Connor AE, Ethier JF, Cranfield M, Schmitt JF, Phillips DJ, Groome NP, Risbridger GP: Activin betaC-subunit heterodimers provide a new mechanism of regulating activin levels in the prostate. Endocrinology. 2003, 144 (10): 4410-4419. 10.1210/en.2003-0225.CrossRefPubMed Mellor SL, Ball EM, O'Connor AE, Ethier JF, Cranfield M, Schmitt JF, Phillips DJ, Groome NP, Risbridger GP: Activin betaC-subunit heterodimers provide a new mechanism of regulating activin levels in the prostate. Endocrinology. 2003, 144 (10): 4410-4419. 10.1210/en.2003-0225.CrossRefPubMed
66.
go back to reference Butler CM, Gold EJ, Risbridger GP: Should activin betaC be more than a fading snapshot in the activin/TGFbeta family album?. Cytokine Growth Factor Rev. 2005, 16 (4-5): 377-385. 10.1016/j.cytogfr.2005.04.005.CrossRefPubMed Butler CM, Gold EJ, Risbridger GP: Should activin betaC be more than a fading snapshot in the activin/TGFbeta family album?. Cytokine Growth Factor Rev. 2005, 16 (4-5): 377-385. 10.1016/j.cytogfr.2005.04.005.CrossRefPubMed
67.
go back to reference O'Bryan MK, Sebire KL, Gerdprasert O, Hedger MP, Hearn MT, de Kretser DM: Cloning and regulation of the rat activin betaE subunit. J Mol Endocrinol. 2000, 24 (3): 409-418. 10.1677/jme.0.0240409.CrossRefPubMed O'Bryan MK, Sebire KL, Gerdprasert O, Hedger MP, Hearn MT, de Kretser DM: Cloning and regulation of the rat activin betaE subunit. J Mol Endocrinol. 2000, 24 (3): 409-418. 10.1677/jme.0.0240409.CrossRefPubMed
68.
go back to reference Takamura K, Tsuchida K, Miyake H, Tashiro S, Sugino H: Activin and activin receptor expression changes in liver regeneration in rat. J Surg Res. 2005, 126 (1): 3-11. 10.1016/j.jss.2005.01.002.CrossRefPubMed Takamura K, Tsuchida K, Miyake H, Tashiro S, Sugino H: Activin and activin receptor expression changes in liver regeneration in rat. J Surg Res. 2005, 126 (1): 3-11. 10.1016/j.jss.2005.01.002.CrossRefPubMed
69.
go back to reference Rodgarkia-Dara C, Vejda S, Erlach N, Losert A, Bursch W, Berger W, Schulte-Hermann R, Grusch M: The activin axis in liver biology and disease. Mutat Res. 2006, 613 (2-3): 123-137. 10.1016/j.mrrev.2006.07.002.CrossRefPubMed Rodgarkia-Dara C, Vejda S, Erlach N, Losert A, Bursch W, Berger W, Schulte-Hermann R, Grusch M: The activin axis in liver biology and disease. Mutat Res. 2006, 613 (2-3): 123-137. 10.1016/j.mrrev.2006.07.002.CrossRefPubMed
Metadata
Title
Evidence of inhibin/activin subunit betaC and betaE synthesis in normal human endometrial tissue
Authors
Ioannis Mylonas
Ansgar Brüning
Naim Shabani
Susanne Kunze
Markus S Kupka
Publication date
01-12-2010
Publisher
BioMed Central
Published in
Reproductive Biology and Endocrinology / Issue 1/2010
Electronic ISSN: 1477-7827
DOI
https://doi.org/10.1186/1477-7827-8-143

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