Global Transcriptome Abnormalities of the Eutopic Endometrium From Women With Adenomyosis

Christopher N. Herndon1, Lusine Aghajanova1, Shaina Balayan1, David W. Erikson2, Fatima Barragan1, Gabriel Goldfien1, Kim Chi Vo3, Shannon M. Hawkins4, Linda C. Giudice3
1Department of Obstetrics, Gynecology and Reproductive Sciences, University of California, San Francisco, USA
2Endocrine Technologies Support Core, Oregon National Primate Research Center, Beaverton, USA
3Department of Obstetrics, Gynecology, and Reproductive Sciences, University of California, San Francisco, USA
4Department of Obstetrics and Gynecology, Indiana University School of Medicine, Indianapolis, USA

Tóm tắt

Từ khóa


Tài liệu tham khảo

Tomassetti, C, Meuleman, C, Timmerman, D, D’Hooghe, T Ade-nomyosis and subfertility: evidence of association and causation. Semin Reprod Med. 2013;31(2):101–108.

Benagiano, G, Habiba, M, Brosens, I The pathophysiology of uter-ine adenomyosis: an update. Fertil Steril. 2012;98(3):572–579.

Bird, CC, McElin, TW, Manalo- Estrella, P The elusive adenomyo-sis of the uterus–revisited. Am J Obstet Gynecol. 1972;112(5): 583–593.

Fischer, CP, Kayisili, U, Taylor, HS HOXA10 expression is decreased in endometrium of women with adenomyosis. Fertil Steril. 2011;95(3):1133–1136.

Burney, RO, Talbi, S, Hamilton, AE, et al. Gene expression analysis of endometrium reveals progesterone resistance and candidate susceptibility genes in women with endometriosis. Endocrinol. 2007;148(8):3814–3826.

Kao, LC, Germeyer, A, Tulac, S, et al. Expression profiling of endometrium from women with endometriosis reveals candidate genes for disease-based implantation failure and infertility. Endo-crinol. 2003;144(7):2870–2881.

Matsumoto, Y, Iwasaka, T, Yamasaki, F, Sugimori, H Apoptosis and Ki-67 expression in adenomyotic lesions and in the corre-sponding eutopic endometrium. Obstet Gynecol. 1999;94(1):71.

Yang, JH, Wu, MY, Chen, CD, Chen, MJ, Yang, YS, Ho, HN Altered apoptosis and proliferation in endometrial stromal cells of women with adenomyosis. Hum Reprod. 2007;22(4):945–952.

Goteri, G, Lucarini, G, Montik, N, et al. Expression of vascular endothelial growth factor (VEGF), hypoxia inducible factor-1a (HIF-1a), and microvessel density in endometrial tissue in women with adenomyosis. Int J Gynecol Path. 2009;28(2):157–163.

Nie, J, Lu, Y, Liu, X, Guo S-W. Immunoreactivity of progesterone receptor isoform, B, nuclear factor kB, and IkBa in adenomyosis. Fertil Steril. 2009;92(3):886–889.

Ota, H, Igarashi, S, Kato, N, Tanaka, T Aberrant expression of glutathione peroxidase in eutopic and ectopic endometrium in endometriosis and adenomyosis. Fertil Steril. 2000;74(2): 313–318.

Ota, H Xanthine oxidase in eutopic and ectopic endometrium in endometriosis and adenomyosis. Fertil Steril. 2001;75(4): 785–790.

Xiaoyu, L, Weiyuan, Z, Ping, J, Anxia, W, Liane, Z Serum differ-ential proteomic analysis of endometriosis and adenomyosis by iTRAQ technique. Eur J Obstet Gynecol Reprod Biol. 2014;182: 62–65.

Hever, A, Roth, RB, Hevezi, PA, et al. Molecular characterization of human adenomyosis. Mol Hum Reprod. 2006;12(12):737–748.

Benagiano, G, Brosens, I The endometrium in adenomyosis. Women’s Health 2012;8(3):301–312.

Rackow, BW, Taylor, HS Submucosal uterine leiomyomas have a global effect on molecular determinants of endometrial receptivity. Fertil Steril. 2010;93(6):2027–2034.

Noyes, RW, Hertig, AT, Rock, J Dating the endometrial biopsy. Fertil Steril. 1950;1(0):3–25.

Talbi, S, Hamilton, AE, Vo, KC, et al. Molecular phenotyping of human endometrium distinguishes menstrual cycle phases and underlying biological processes in normo-ovulatory women. Endocrinol. 2006;147(3):1097–1121.

Kiss-László Z, Henry, Y, Kiss, T Sequence and structural ele-ments of methylation guide snoRNAs essential for site-specific ribose methylation of pre-rRNA. EMBO, J 1998;17(3): 797–807.

Nisolle, M, Donnez, J Peritoneal endometriosis, ovarian endome-triosis, and adenomyotic nodules of the rectovaginal septum are three different entities. Fertil Steril. 1997;68(4):585–596

Mehasseb, MK, Panchal, R, Taylor, AH, Brown, L, Bell, SC, Habiba, M Estrogen and progesterone receptor isoform distribution through the menstrual cycle in uteri with and without adenomyo-sis. Fertil Steril. 2011;95(7):2228–2235.e1.

Mohammed, H, D’Santos, C, Serandour, AA, et al. Endogenous purification reveals GREB1 as a key estrogen receptor regulatory factor. Cell Reports. 2013;3(2):342–349.

Chand, AL, Wijayakumara, DD, Knower, KC, et al. The orphan nuclear receptor LRH-1 and ERa activate GREB1 expression to induce breast cancer cell proliferation. PLoS ONE. 2012;7(2): e31593.

Pellegrini, C, Gori, I, Achtari, C, et al. The expression of estrogen receptors as well as GREB1, c-MYC, and cyclin D1, estrogen-regulated genes implicated in proliferation, is increased in peritoneal endometriosis. Fertil Steril. 2012;98(5):1200–1208.

Leyendecker, G, Wildt, L, Mall, G The pathophysiology of endo-metriosis and adenomyosis: tissue injury and repair. Arch Gynecol Obstet. 2009;280(4):529–538.

Yamamoto, T, Noguchi, T, Tamura, T, Kitawaki, J, Okada, H Evi-dence for estrogen synthesis in adenomyotic tissues. Am J Obstet Gynecol. 1993;169(3):734–738.

Chen Y-J, Li H-Y, Huang, CH, et al. Oestrogen-induced epithe-lial–mesenchymal transition of endometrial epithelial cells contributes to the development of adenomyosis. J Pathol. 2010; 222(3):261–270.

Huang T-S, Chen Y-J, Chou T-Y, et al. Oestrogen-induced angio-genesis promotes adenomyosis by activating the Slug-VEGF axis in endometrial epithelial cells. J Cell Mol Med. 2014;18(7): 1358–1371.

Gonzalez, G, Behringer, RR Dicer is required for female repro-ductive tract development and fertility in the mouse. Mol Reprod Dev. 2009;76(7):678–688.

Marsh, EE, Lin, Z, Yin, P, Milad, M, Chakravarti, D, Bulun, SE Differential expression of microRNA species in human uterine leiomyoma versus normal myometrium. Fertil Steril. 2008;89(6): 1771–1776.

Pan, Q, Luo, X, Chegini, N Differential expression of microRNAs in myometrium and leiomyomas and regulation by ovarian ster-oids. J Cell Mol Med. 2008;12(1):227–240.

Santamaria, X, Taylor, H MicroRNA and gynecological reproduc-tive diseases. Fertil Steril. 2014;101(6):1545–1551.

Burney, RO, Hamilton, AE, Aghajanova, L, et al. MicroRNA expression profiling of eutopic secretory endometrium in women with versus without endometriosis. Mol Hum Reprod. 2009;15(10):625–631.

Yuva-Aydemir, Y, Simkin, A, Gascon, E, Gao F-B. MicroRNA-9. RNA Biol. 2014;8(4):557–564.

Sa, R, Song, J Relationship between ultrastructural features with the expression of connexin 43 in the uterine junction zone and pathogenesis of adenomyosis. Zhonghua Fu Chan Ke Za Zhi. 2010;45(10):762–766.

Jones, RK, Searle, RF, Bulmer, JN Apoptosis and bcl-2 expression in normal human endometrium, endometriosis and adenomyosis. Hum Reprod. 1998;13(12):3496–3502.

Makker, A, Goel, MM, Das, V, Agarwal, A PI3K-Akt-mTOR and MAPK signaling pathways in polycystic ovarian syndrome, uter-ine leiomyomas and endometriosis: an update. Gynecol Endocri-nol. 2012;28(3):175–181.

Erikson, D, Chen, JC, Piltonen, TT, Conti, M, Irwin, JC, Giudice, LC Inhibition of epidermal growth factor receptor restores deciduali-zation markers in stromal fibroblasts from women with endome-triosis. JEPPD. 2014;6(4):196–211.

Sabatini, DM mTOR and cancer: insights into a complex relation-ship. Nat Rev Cancer. 2006;6(9):729–734.

Fasolo, A, Sessa, C mTOR inhibitors in the treatment of cancer. Expert Opin Investig Drugs. 2008;17(11):1717–1734.

deGraffenried, LA, Friedrichs, WE, Russell, DH, et al. Inhibition of mTOR activity restores tamoxifen response in breast cancer cells with aberrant Akt activity. Clin Cancer Res. 2004;10(23): 8059–8067.

Meric-Bernstam, F, Gonzalez-Angulo, AM Targeting the mTOR signaling network for cancer therapy. J Clin Oncol. 2009;27(13): 2278–2287.

Khan, KN, Kitajima, M, Hiraki, K, et al. Cell proliferation effect of GnRH agonist on pathological lesions of women with endome-triosis, adenomyosis and uterine myoma. Hum Reprod. 2010;25(11):2878–2890.

Mehasseb, MK, Taylor, AH, Pringle, JH, Bell, SC, Habiba, M 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. 2010;94(7):2547–2551.

Li, T, Li, YG, Pu, DM Matrix metalloproteinase-2 and -9 expres-sion correlated with angiogenesis in human adenomyosis. Gyne-col Obstet Invest. 2006;62(4):229–235.

Yang J-H, Wu M-Y, Chen M-J, Chen S-U, Yang Y-S, Ho H-N. Increased matrix metalloproteinase-2 and tissue inhibitor of metalloproteinase-1 secretion but unaffected invasiveness of endometrial stromal cells in adenomyosis. Fertil Steril. 2009; 91(5):2193–2198.

Symington, BE, Takada, Y, Carter, WG Interaction of integrins alpha 3 beta 1 and alpha 2 beta 1: potential role in keratinocyte intercellular adhesion. J Cell Biol. 1993;120(2):523–535.

Prifti, S, Zourab, Y, Koumouridis, A, Bohlmann, M, Strowitzki, T, Rabe, T Role of integrins in invasion of endometrial cancer cell lines. Gynecol Oncol. 2002;84(1):12–20.

Qiu, F, XM, G, GL, L, et al. Expression of matrix metalloproteinase and tissue inhibitor of metalloproteinase in adenomyosis. Sichuan Da Xue Xue Bao Yi Xue Ban. 2006;37(1):118–122.

Tokyol, C, Aktepe, F, Dilek, FH, Sahin, O, Arioz, DT Expression of cyclooxygenase-2 and matrix metalloproteinase-2 in adenomyo-sis and endometrial polyps and its correlation with angiogenesis. Int J Gynecol Path. 2009;28(2):148–156.

Aghajanova, L, Shen, S, Rojas, AM, Fisher, SJ, Irwin, JC, Giudice, LC Comparative transcriptome analysis of human trophectoderm and embryonic stem cell-derived trophoblasts reveal key partici-pants in early implantation. Biol Reprod. 2011;86(1):1–21.

Yu, J, Boicea, A, Barrett, KL, et al. Reduced connexin 43 in eutopic endometrium and cultured endometrial stromal cells from subjects with endometriosis. Mol Hum Reprod. 2014;20(3):260–270.

Regidor, PA, Regidor, M, Schindler, AE, Winterhager, E Aberrant expression pattern of gap junction connexins in endometriotic tissues. Mol Hum Reprod. 1997;3(5):375–381.

Aghajanova, L, Giudice, LC Molecular evidence for differences in endometrium in severe versus mild endometriosis. Reprod Sci. 2010;18(3):229–251.

McElin, TW, Bird, CC Adenomyosis of the uterus. Obstet Gynecol Annu. 1974;3(0):425–441.

Gonzales, M, de Matos, LA, da Costa Gonçalves, MO, et al. Patients with adenomyosis are more likely to have deep endome-triosis. Gynecol Surg. 2012;9(3):259–264.

Kunz, G, Beil, D, Huppert, P, Noe, M, Kissler, S, Leyendecker, G Adenomyosis in endometriosis–prevalence and impact on ferti-lity. Evidence from magnetic resonance imaging. Hum Reprod. 2005;20(8):2309–2316.

Larsen, SB, Lundorf, E, Forman, A, Dueholm, M Adenomyosis and junctional zone changes in patients with endometriosis. Eur J Obstet Gynecol Reprod Biol. 2011;157(2):206–211.

Sheldon, E, Vo, KC, McIntire, RA, et al. Biobanking human endometrial tissue and blood specimens: standard operating procedure and importance to reproductive biology research and diagnostic development. Fertil Steril. 2011;95(6): 2120–2122. e12.