457
Views
20
CrossRef citations to date
0
Altmetric
Review Article

The role of TGFβ superfamily members in the pathophysiology of endometriosis

&
Pages 511-515 | Received 09 Dec 2014, Accepted 26 Jan 2015, Published online: 19 May 2015

References

  • Luo X, Xu J, Chegini N. The expression of Smads in human endometrium and regulation and induction in endometrial epithelial and stromal cells by transforming growth factor-beta. J Clin Endocrinol Metab 2003;88:4967–76
  • Papageorgiou I, Nicholls PK, Wang F, et al. Expression of nodal signalling components in cycling human endometrium and in endometrial cancer. Reprod Biol Endocrinol 2009;7:122
  • Yan X, Liu Z, Chen Y. Regulation of TGF-beta signaling by Smad7. Acta Biochim Biophys Sinica 2009;41:263–72
  • Godkin JD, Dore JJ. Transforming growth factor beta and the endometrium. Rev Reprod 1998;3:1–6
  • Torres PB, Florio P, Galleri L, et al. Activin A, activin receptor type II, nodal, and cripto mRNA are expressed by eutopic and ectopic endometrium in women with ovarian endometriosis. Reprod Sci 2009;16:727–33
  • Rogers PA, D'Hooghe TM, Fazleabas A, et al. Priorities for endometriosis research: recommendations from an international consensus workshop. Reprod Sci 2009;16:335–46
  • Omwandho CO, Konrad L, Halis G, et al. Role of TGF-betas in normal human endometrium and endometriosis. Hum Reprod 2010;25:101–9
  • Houston DE. Evidence for the risk of pelvic endometriosis by age, race and socioeconomic status. Epidemiol Rev 1984;6:167–91
  • Husby GK, Haugen RS, Moen MH. Diagnostic delay in women with pain and endometriosis. Acta Obstet Gynecol Scand 2003;82:649–53
  • Practice Committee of American Society for Reproductive M. Treatment of pelvic pain associated with endometriosis. Fertil Steril 2008;90:S260–9
  • Kuohung W, Jones GL, Vitonis AF, et al. Characteristics of patients with endometriosis in the United States and the United Kingdom. Fertil Steril 2002;78:767–72
  • Ethier JF, Findlay JK. Roles of activin and its signal transduction mechanisms in reproductive tissues. Reproduction 2001;121:667–75
  • Miyazawa K, Shinozaki M, Hara T, Furuya T, Miyazono K. Two major Smad pathways in TGF-beta superfamily signalling. Genes Cells 2002;7:1191–204
  • Liu T, Feng XH. Regulation of TGF-beta signalling by protein phosphatases. Biochem J 2010;430:191–8
  • Massague J. TGFbeta signalling in context. Nat Rev Mol Cell Biol 2012;13:616–30
  • Wrana JL, Attisano L. The Smad pathway. Cytokine Growth Factor Rev 2000;11:5–13
  • Yoshimura A, Wakabayashi Y, Mori T. Cellular and molecular basis for the regulation of inflammation by TGF-beta. J Biochem 2010;147:781–92
  • Findlay JK, Drummond AE, Dyson M, et al. Production and actions of inhibin and activin during folliculogenesis in the rat. Mol Cell Endocrinol 2001;180:139–44
  • Jones RL, Findlay JK, Farnworth PG, et al. Activin A and inhibin A differentially regulate human uterine matrix metalloproteinases: potential interactions during decidualization and trophoblast invasion. Endocrinology 2006;147:724–32
  • Harrison CA, Gray PC, Vale WW, Robertson DM. Antagonists of activin signaling: mechanisms and potential biological applications. Trends Endocrinol Metab 2005;16:73–8
  • Zhu J, Lin SJ, Zou C, et al. Inhibin alpha-subunit N terminus interacts with activin type IB receptor to disrupt activin signaling. J Biol Chem 2012;287:8060–70
  • Postovit LM, Seftor EA, Seftor RE, Hendrix MJ. Targeting Nodal in malignant melanoma cells. Expert Opin Therap Targets 2007;11:497–505
  • Wagner N, Weyhersmuller A, Blauth A, et al. The Drosophila LEM-domain protein MAN1 antagonizes BMP signaling at the neuromuscular junction and the wing crossveins. Dev Biol 2010;339:1–13
  • Pangas SA. Regulation of the ovarian reserve by members of the transforming growth factor beta family. Molecular Reprod Dev 2012;79:666–79
  • Wakefield LM, Hill CS. Beyond TGFbeta: roles of other TGFbeta superfamily members in cancer. Nat Rev Cancer 2013;13:328–41
  • Shen MM. Nodal signaling: developmental roles and regulation. Development 2007;134:1023–34
  • Schier AF. Nodal morphogens. Cold Spring Harbor Persp Biol 2009;1:a003459
  • Zhang YE. Non-Smad pathways in TGF-beta signaling. Cell Res 2009;19:128–39
  • Gold LI, Saxena B, Mittal KR, et al. Increased expression of transforming growth factor beta isoforms and basic fibroblast growth factor in complex hyperplasia and adenocarcinoma of the endometrium: evidence for paracrine and autocrine action. Cancer Res 1994;54:2347–58
  • Chegini N, Gold LI, Williams RS. Localization of transforming growth factor beta isoforms TGF-beta 1, TGF-beta 2, and TGF-beta 3 in surgically induced endometriosis in the rat. Obstet Gynecol 1994;83:455–61
  • Bischof P, Meisser A, Campana A. Mechanisms of endometrial control of trophoblast invasion. J Reprod Fertil Suppl 2000;55:65–71
  • Johnson MC, Torres M, Alves A, et al. Augmented cell survival in eutopic endometrium from women with endometriosis: expression of c-myc, TGF-beta1 and bax genes. Reprod Biol Endocrinol 2005;3:45
  • Jones RL, Stoikos C, Findlay JK, Salamonsen LA. TGF-beta superfamily expression and actions in the endometrium and placenta. Reproduction 2006;132:217–32
  • Komiyama S, Aoki D, Komiyama M, Nozawa S. Local activation of TGF-beta1 at endometriosis sites. J Reprod Med 2007;52:306–12
  • Bruner KL, Rodgers WH, Gold LI, et al. Transforming growth factor beta mediates the progesterone suppression of an epithelial metalloproteinase by adjacent stroma in the human endometrium. Proc Natl Acad Sci USA 1995;92:7362–6
  • Gaide Chevronnay HP, Cornet PB, et al. Opposite regulation of transforming growth factors-beta2 and -beta3 expression in the human endometrium. Endocrinology 2008;149:1015–25
  • Reis FM, Ribeiro MF, Maia AL, Spritzer PM. Regulation of human endometrial transforming growth factor beta1 and beta3 isoforms through menstrual cycle and medroxyprogesterone acetate treatment. Histol Histopathol 2002;17:739–45
  • Singh M, Chaudhry P, Asselin E. Bridging endometrial receptivity and implantation: network of hormones, cytokines, and growth factors. J Endocrinol 2011;210:5–14
  • Salamonsen LA, Dimitriadis E, Jones RL, Nie G. Complex regulation of decidualization: a role for cytokines and proteases – a review. Placenta 2003;24:S76–85
  • Florio P, Severi FM, Luisi S, et al. Endometrial expression and secretion of activin A, but not follistatin, increase in the secretory phase of the menstrual cycle. J Soc Gynecol Invest 2003;10:237–43
  • Rocha AL, Carrarelli P, Novembri R, et al. Altered expression of activin, cripto, and follistatin in the endometrium of women with endometrioma. Fertil Steril 2011;95:2241–6
  • Mylonas I, Jeschke U, Winkler L, et al. Immunohistochemical expression of inhibin-alpha in human endometrium and the in vitro secretion of inhibin, estradiol and cortisol in cultured human endometrial glandular cells. Arch Gynecol Obstet 2003;268:142–50
  • Mylonas I, Jeschke U, Wiest I, et al. Inhibin/activin subunits alpha, beta-A and beta-B are differentially expressed in normal human endometrium throughout the menstrual cycle. Histochem Cell Biol 2004;122:461–71
  • Wang HQ, Takebayashi K, Tsuchida K, et al. Follistatin-related gene (FLRG) expression in human endometrium: sex steroid hormones regulate the expression of FLRG in cultured human endometrial stromal cells. J Clin Endocrinol Metab 2003;88:4432–9
  • Ferreira MC, Witz CA, Hammes LS, et al. Activin A increases invasiveness of endometrial cells in an in vitro model of human peritoneum. Mol Hum Reprod 2008;14:301–7
  • Jones RL, Salamonsen LA, Zhao YC, et al. Expression of activin receptors, follistatin and betaglycan by human endometrial stromal cells: consistent with a role for activins during decidualization. Mol Hum Reprod 2002;8:363–74
  • Maruyama T, Masuda H, Ono M, et al. Human uterine stem/progenitor cells: their possible role in uterine physiology and pathology. Reproduction 2010;140:11–22
  • Park CB, Dufort D. NODAL signaling components regulate essential events in the establishment of pregnancy. Reproduction 2013;145:R55–64
  • Oliveira FR, Dela Cruz C, Del Puerto HL, et al. Stem cells: are they the answer to the puzzling etiology of endometriosis? Histol Histopathol 2012;27:23–9
  • Nap AW, Groothuis PG, Demir AY, et al. Pathogenesis of endometriosis. Best Pract Res Clin Obstet Gynaecol 2004;18:233–44
  • Bulun SE. Endometriosis. N Eng J Med 2009;360:268–79
  • Sasson IE, Taylor HS. Stem cells and the pathogenesis of endometriosis. Ann NY Acad Sci 2008;1127:106–15
  • Fassbender A, Vodolazkaia A, Saunders P, et al. Biomarkers of endometriosis. Fertil Steril 2013;99:1135–45
  • Pizzo A, Salmeri FM, Ardita FV, et al. Behaviour of cytokine levels in serum and peritoneal fluid of women with endometriosis. Gynecol Obstet Invest 2002;54:82–7
  • Oosterlynck DJ, Meuleman C, Waer M, Koninckx PR. Transforming growth factor-beta activity is increased in peritoneal fluid from women with endometriosis. Obstet Gynecol 1994;83:287–92
  • Kupker W, Schultze-Mosgau A, Diedrich K. Paracrine changes in the peritoneal environment of women with endometriosis. Hum Reprod Update 1998;4:719–23
  • D'Hooghe TM, Xiao L, Hill JA. Cytokine profiles in autologous peritoneal fluid and peripheral blood of women with deep and superficial endometriosis. Arch Gynecol Obstet 2001;265:40–4
  • Hao M, Shi Y, Dong M. [Measurements of interleukin-6, interleukin-8 and transforming growth factor-beta 1 levels in peritoneal fluid of patients with endometriosis]. Zhonghua fu Chan ke za Zhi 2000;35:329–31
  • Tamura M, Fukaya T, Enomoto A, et al. Transforming growth factor-beta isoforms and receptors in endometriotic cysts of the human ovary. Am J Reprod Immunol 1999;42:160–7
  • Carrarelli P, Rocha AL, Belmonte G, et al. Increased expression of antimullerian hormone and its receptor in endometriosis. Fertil Steril 2014;101:1353–8
  • Namkung J, Song JY, Jo HH, et al. Mullerian inhibiting substance induces apoptosis of human endometrial stromal cells in endometriosis. J Clin Endocrinol Metab 2012;97:3224–30
  • Florio P, Luisi S, Vigano P, et al. Healthy women and patients with endometriosis show high concentrations of inhibin A, inhibin B, and activin A in peritoneal fluid throughout the menstrual cycle. Hum Reprod 1998;13:2606–11
  • Ferreira MC, Cavallo IK, Florio P, et al. 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;39:535–41
  • Reis FM, Di Blasio AM, Florio P, et al. Evidence for local production of inhibin A and activin A in patients with ovarian endometriosis. Fertil Steril 2001;75:367–73
  • Rombauts L, Donoghue J, Cann L, et al. Activin-A secretion is increased in the eutopic endometrium from women with endometriosis. Austral NZ J Obstet Gynaecol 2006;46:148–53
  • Mabuchi Y, Yamoto M, Minami S, Umesaki N. Immunohistochemical localization of inhibin and activin subunits, activin receptors and Smads in ovarian endometriosis. Int J Mol Med 2010;25:17–23
  • Dela Cruz C, Puerto HL, Rocha AL, et al. Expression of nodal, cripto, SMAD3, phosphorylated SMAD3, and SMAD4 in the proliferative endometrium of women with endometriosis. Reprod Sci 2014. PubMed PMID: 25228630
  • Reis FM, Luisi S, Abrao MS, et al. Diagnostic value of serum activin A and follistatin levels in women with peritoneal, ovarian and deep infiltrating endometriosis. Hum Reprod 2012;27:1445–50
  • Torres PB, Florio P, Ferreira MC, et al. Deranged expression of follistatin and follistatin-like protein in women with ovarian endometriosis. Fertil Steril 2007;88:200–5
  • Thompson TB, Woodruff TK, Jardetzky TS. Structures of an ActRIIB:activin A complex reveal a novel binding mode for TGF-beta ligand:receptor interactions. EMBO J 2003;22:1555–66

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.