Myostatin, follistatin and activin type II receptors are highly expressed in adenomyosis

Fertility and Sterility

Volumn 104, Issue 3, 2015, Pages 744-752.e1

  Carrarelli, Patrizia ^a   Yen, Chih Fen ^b   Arcuri, Felice ^a   Funghi, Lucia ^a   Tosti, Claudia ^a   Wang, Tzu Hao ^b,c   Huang, Joseph S ^d   Petraglia, Felice ^a  

^a UNIVERSITY OF SIENA   (Italy)

^b CHANG GUNG UNIVERSITY COLLEGE OF MEDICINE   (Taiwan)

^c CHANG GUNG MEMORIAL HOSPITAL   (Taiwan)

^d THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

activin; activin receptors; Adenomyosis; crypto; eutopic endometrium; follistatin; infertility; inhibin; myostatin; nodular adenomyosis

Indexed keywords

ACTIVIN A; ACTIVIN RECEPTOR 2; COMPLEMENTARY DNA; FOLLISTATIN; INHIBIN A; MESSENGER RNA; MYELOPID; MYOSTATIN; ACTIVIN; ACTIVIN RECEPTOR TYPE II-A; ACVR2B PROTEIN, HUMAN; FST PROTEIN, HUMAN; MSTN PROTEIN, HUMAN;

ADENOMYOSIS; ADULT; APOPTOSIS; ARTICLE; CELL PROLIFERATION; CLINICAL ARTICLE; CONTROLLED STUDY; ENDOMETRIUM; FEMALE; FEMALE INFERTILITY; HUMAN; HUMAN TISSUE; HYSTERECTOMY; IMMUNOHISTOCHEMISTRY; PREMENOPAUSE; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; UTERUS; UTERUS DISEASE; CASE CONTROL STUDY; CHEMISTRY; GENETICS; METABOLISM; PROSPECTIVE STUDY;

ACTIVIN RECEPTORS, TYPE II; ACTIVINS; ADENOMYOSIS; ADULT; CASE-CONTROL STUDIES; ENDOMETRIUM; FEMALE; FOLLISTATIN; HUMANS; IMMUNOHISTOCHEMISTRY; MYOSTATIN; PROSPECTIVE STUDIES; REAL-TIME POLYMERASE CHAIN REACTION; RNA, MESSENGER;

EID: 84940720962     PISSN: 00150282     EISSN: 15565653     Source Type: Journal    
DOI: 10.1016/j.fertnstert.2015.05.032     Document Type: Article

References (50)

1. A. Ferenczy Pathophysiology of adenomyosis Hum Reprod Update 4 1998 312 322
2. L. Garcia, and K. Isaacson Adenomyosis: review of the literature J Minim Invasive Gynecol 18 2011 428 437
3. M. Levgur, M.A. Abadi, and A. Tucker Adenomyosis: symptoms, histology, and pregnancy terminations Obstet Gynecol 95 2000 688 691
4. N. Jichan, L. Xishi, and S.W. Guo Promoter hypermethylation of progesterone receptor isoform B (PR-B) in adenomyosis and its rectification by a histone deacetylase inhibitor and a demethylation agent Reprod Sci 17 2010 995 1005
5. J. Nie, Y. Lu, X. Liu, and S.W. Guo Immunoreactivity of progesterone receptor isoform B, nuclear factor kappaB, and IkappaBalpha in adenomyosis Fertil Steril 92 2009 886 889
6. S. Jaffer, O. Shynlova, and S. Lye Mammalian target of rapamycin is activated in association with myometrial proliferation during pregnancy Endocrinology 150 2009 4672 4680
7. Y.J. Chen, H.Y. Li, C.H. Huang, N.F. Twu, M.S. Yen, P.H. Wang, and et al. Oestrogen-induced epithelial-mesenchymal transition of endometrial epithelial cells contributes to the development of adenomyosis J Pathol 222 2010 261 270
8. T. Yamamoto, T. Noguchi, T. Tamura, J. Kitawaki, and H. Okada Evidence for estrogen synthesis in adenomyotic tissues Am J Obstet Gynecol 169 1993 734 738
9. I.A. Voutsadakis Epithelial to mesenchymal transition in the pathogenesis of uterine malignant mixed Mullerian tumours: the role of ubiquitin proteasome system and therapeutic opportunities Clin Transl Oncol 14 2012 243 253
10. S. Zhou, T. Yi, R. Liu, C. Bian, X. Qi, X. He, and et al. Proteomics identification of annexin A2 as a key mediator in the metastasis and proangiogenesis of endometrial cells in human adenomyosis Mol Cell Proteomics 11 2012 M112 017988
11. K.M. Curtis, S.D. Hillis, P.A. Marchbanks, and H.B. Peterson Disruption of the endometrial-myometrial border during pregnancy as a risk factor for adenomyosis Am J Obstet Gynecol 187 2002 543 544
12. E. Parrott, M. Butterworth, A. Green, I.N. White, and P. Greaves Adenomyosis - a result of disordered stromal differentiation Am J Pathol 159 2001 623 630
13. G. Leyendecker, L. Wildt, and G. Mall The pathophysiology of endometriosis and adenomyosis: tissue injury and repair Arch Gynecol Obstet 280 2009 529 538
14. G. Benagiano, and I. Brosens The endometrium in adenomyosis Womens Health (Lond Engl) 8 2012 301 312
15. G. Benagiano, I. Brosens, and M. Habiba Structural and molecular features of the endomyometrium in endometriosis and adenomyosis Hum Reprod Update 20 2014 386 402
16. M.K. Mehasseb, A.H. Taylor, J.H. Pringle, S.C. Bell, and M. Habiba Enhanced invasion of stromal cells from adenomyosis in a three-dimensional coculture model is augmented by the presence of myocytes from affected uteri Fertil Steril 94 2010 2547 2551
17. T. Li, Y.G. Li, and D.M. Pu Matrix metalloproteinase-2 and -9 expression correlated with angiogenesis in human adenomyosis Gynecol Obstet Invest 62 2006 229 235
18. C. Tokyol, F. Aktepe, F.H. Dilek, O. Sahin, and D.T. Arioz Expression of cyclooxygenase-2 and matrix metalloproteinase-2 in adenomyosis and endometrial polyps and its correlation with angiogenesis Int J Gynecol Pathol 28 2009 148 156
19. J.H. Yang, M.Y. Wu, D.Y. Chang, C.H. Chang, Y.S. Yang, and H.N. Ho Increased interleukin-6 messenger RNA expression in macrophage-cocultured endometrial stromal cells in adenomyosis Am J Reprod Immunol 55 2006 181 187
20. C. Bamberger, A. Scharer, M. Antsiferova, B. Tychsen, S. Pankow, M. Muller, and et al. Activin controls skin morphogenesis and wound repair predominantly via stromal cells and in a concentration-dependent manner via keratinocytes Am J Pathol 167 2005 733 747
21. J. Yu, and K.E. Dolter Production of activin A and its roles in inflammation and hematopoiesis Cytokines Cell Mol Ther 3 1997 169 177
22. C.A. Harrison, P.C. Gray, W.W. Vale, and D.M. Robertson Antagonists of activin signaling: mechanisms and potential biological applications Trends Endocrinol Metab 16 2005 73 78
23. R.L. Jones, L.A. Salamonsen, and J.K. Findlay Activin A promotes human endometrial stromal cell decidualization in vitro J Clin Endocrinol Metab 87 2002 4001 4004
24. P. Florio, F.M. Severi, S. Luisi, P. Ciarmela, G. Calonaci, L. Cobellis, and et al. Endometrial expression and secretion of activin A, but not follistatin, increase in the secretory phase of the menstrual cycle J Soc Gynecol Investig 10 2003 237 243
25. T. Otani, S. Minami, M. Yamoto, and N. Umesaki Production of activin A in hyperplasia and adenocarcinoma of the human endometrium Gynecol Oncol 83 2001 31 38
26. F. Petraglia, P. Florio, S. Luisi, R. Gallo, A. Gadducci, P. Vigano, and et al. 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 83 1998 1194 1200
27. A.L. Rocha, P. Carrarelli, R. Novembri, F. de Pascalis, S. Luisi, F.M. Reis, and et al. Activin A stimulates interleukin 8 and vascular endothelial growth factor release from cultured human endometrial stromal cells: possible implications for the pathogenesis of endometriosis Reprod Sci 19 2012 832 838
28. M.C. Ferreira, C.A. Witz, L.S. Hammes, N. Kirma, F. Petraglia, R.S. Schenken, and et al. Activin A increases invasiveness of endometrial cells in an in vitro model of human peritoneum Mol Hum Reprod 14 2008 301 307
29. S.J. Lee, and A.C. McPherron Regulation of myostatin activity and muscle growth Proc Natl Acad Sci U S A 98 2001 9306 9311
30. P. Ciarmela, E. Wiater, S.M. Smith, and W. Vale Presence, actions, and regulation of myostatin in rat uterus and myometrial cells Endocrinology 150 2009 906 914
31. P. Ciarmela, E. Wiater, and W. Vale Activin-A in myometrium: characterization of the actions on myometrial cells Endocrinology 149 2008 2506 2516
32. P. Ciarmela, E. Bloise, P.C. Gray, P. Carrarelli, M.S. Islam, F. de Pascalis, and et al. Activin-A and myostatin response and steroid regulation in human myometrium: disruption of their signalling in uterine fibroid J Clin Endocrinol Metab 96 2011 755 765
33. M.S. Islam, W.H. Catherino, O. Protic, M. Janjusevic, P.C. Gray, S.R. Giannubilo, and et al. Role of activin-A and myostatin and their signaling pathway in human myometrial and leiomyoma cell function J Clin Endocrinol Metab 99 2014 E775 E785
34. D.H. Kozian, M. Ziche, and H.G. Augustin The activin-binding protein follistatin regulates autocrine endothelial cell activity and induces angiogenesis Lab Invest 76 1997 267 276
35. P. Florio, F.M. Reis, P.B. Torres, F. Calonaci, M.S. Abrao, L.L. Nascimento, and et al. High serum follistatin levels in women with ovarian endometriosis Hum Reprod 24 2009 2600 2606
36. A.L. Rocha, P. Carrarelli, R. Novembri, L. Sabbioni, S. Luisi, F.M. Reis, and et al. Altered expression of activin, cripto, and follistatin in the endometrium of women with endometrioma Fertil Steril 95 2011 2241 2246
37. C. Exacoustos, L. Manganaro, and E. Zupi Imaging for the evaluation of endometriosis and adenomyosis Best Pract Res Clin Obstet Gynaecol 28 2014 655 681
38. F.M. Severi, C. Bocchi, P. Florio, L. Cobellis, E. Ignacchiti, and F. Petraglia Transvaginal ultrasonography in women receiving emergency contraception Fertil Steril 79 2003 1074 1077
39. B. Refaat, S. Amer, B. Ola, N. Chapman, and W. Ledger The expression of activin-betaA- and -betaB-subunits, follistatin, and activin type II receptors in fallopian tubes bearing an ectopic pregnancy J Clin Endocrinol Metab 93 2008 293 299
40. M.P. Hedger, W.R. Winnall, D.J. Phillips, and D.M. de Kretser The regulation and functions of activin and follistatin in inflammation and immunity Vitam Horm 85 2011 255 297
41. S. Werner, and C. Alzheimer Roles of activin in tissue repair, fibrosis, and inflammatory disease Cytokine Growth Factor Rev 17 2006 157 171
42. M. Antsiferova, and S. Werner The bright and the dark sides of activin in wound healing and cancer J Cell Sci 125 2012 3929 3937
43. D.M. De Kretser, R.E. O'Hehir, C.L. Hardy, and M.P. Hedger The roles of activin A and its binding protein, follistatin, in inflammation and tissue repair Mol Cell Endocrinol 359 2012 101 106
44. C.J. Stoikos, C.A. Harrison, L.A. Salamonsen, and E. Dimitriadis A distinct cohort of the TGFbeta superfamily members expressed in human endometrium regulate decidualization Hum Reprod 23 2008 1447 1456
45. R. Rios, I. Carneiro, V.M. Arce, and J. Devesa Myostatin is an inhibitor of myogenic differentiation Am J Physiol Cell Physiol 282 2002 C993 C999
46. D. Zhou, N. Luo, Q. Wu, Y. You, Z. Zhai, Z. Mou, and et al. Transcellular distribution heterogeneity of Annexin A5 represents a protective response to lupus-related thrombophilia: a pilot Proteomics-based study Biochem Biophys Res Commun 420 2012 357 363
47. R.L. Jones, J.K. Findlay, P.G. Farnworth, D.M. Robertson, E. Wallace, and L.A. Salamonsen Activin A and inhibin A differentially regulate human uterine matrix metalloproteinases: potential interactions during decidualization and trophoblast invasion Endocrinology 147 2006 724 732
48. G. Leyendecker, M. Herbertz, G. Kunz, and G. Mall Endometriosis results from the dislocation of basal endometrium Hum Reprod 17 2002 2725 2736
49. S. Campo, V. Campo, and G. Benagiano Adenomyosis and infertility Reprod Biomed Online 24 2012 35 46
50. L. Benaglia, L. Cardellicchio, M. Leonardi, S. Faulisi, P. Vercellini, A. Paffoni, an d et al. Asymptomatic adenomyosis and embryo implantation in IVF cycles Reprod Biomed Online 29 2014 606 611