Comparative systems genetics view of endometriosis and uterine leiomyoma: Two sides of the same coin?

References

• Aznaurova, Y.B., Zhumataev, M.B., Roberts, T.K., Aliper, A.M. and Zhavoronkov, A.A. (2014) Molecular aspects of development and regulation of endometriosis. Reprod Biol Endocrinol 12: 50.
   PubMed Web of Science ®Google Scholar
• Baranov, V.S., Ivaschenko, T.E., Liehr, T. and Yarmolinskaya M.I. (2015) System genetics view of endometriosis: a common complex disorder. Eur J Obstet Gynecol Reprod Biol 185: 59–65.
   PubMed Web of Science ®Google Scholar
• Beliard, A., Noel, A. and Foidart, J.M. (2004) Reduction of apoptosis and proliferation in endometriosis. Fertil Steril 82: 80–85.
   PubMed Web of Science ®Google Scholar
• Bertsch, E., Qiang, W., Zhang, Q., Espona-Fiedler, M., Druschitz, S., Liu, Y., et al. (2014) MED12 and HMGA2 mutations: Two independent genetic events in uterine leiomyoma and leiomyosarcoma. Mod Pathol 27: 1144–1153.
   PubMed Web of Science ®Google Scholar
• Benassayag, C., Leroy, M. J., Rigourd, V., Robert, B., Honore, J. C., Mignot, T. M., et al. (1999) Estrogen receptors (ERα/ERβ) in normal and pathological growth of the human myometrium: pregnancy and leiomyoma. Am J Physiol Endocrinol Metab 276: E1112–E1118.
   PubMed Web of Science ®Google Scholar
• Bischoff, F.Z., Heard, M. and Simpson, J. L. (2002) Somatic DNA alterations in endometriosis: high frequency of chromosome 17 and p53 loss in late-stage endometriosis. J Reprod Immunol 55: 49–64.
   PubMed Web of Science ®Google Scholar
• Borahay, M.A., All-Hendy, A.A., Killic, G.S. and Boehning D. (2015) Signalling pathways in leiomyoma: understanding and implication for therapy. Mol Med 21: 242–256.
   PubMed Web of Science ®Google Scholar
• Bulun, C. (2013) Uterine Leiomyoma. N Engl J Med 369: 1344–1355.
   PubMed Web of Science ®Google Scholar
• Burney, R.O.and Giudice, L.C. (2012) Pathogenesis and pathophysiology of endometriosis. Fertil Steril 98(3): 511–519.
   PubMed Web of Science ®Google Scholar
• Canis, M., Donnez, J. G., Guzick, D. S., Halme, J. K., Rock, J. A., Schenken, R. S., et al. (1997) Revised American Society for Reproductive Medicine classification of endometriosis: 1996. Fertil Steril 67(5): 817–821.
   PubMed Web of Science ®Google Scholar
• Chan, R.W., Schwab, K.E. and Gargett, C.E. (2004) Clonogenicity of human endometrial epithelial and stromal cells. Biol Reprod 70:1738-1750.
   PubMed Web of Science ®Google Scholar
• Chang, J.H., Au, H-K., Lee, W.C., Chi, C.C., Ling, T.Y, Wang, L.M., et al. (2013) Expression of the pluripotent transcription factor OCT4 promotes cell migration in endometriosis. Fertil Steril 99: 1332–1339.
   PubMed Web of Science ®Google Scholar
• Ciavattini, A., Giuseppe, J.D., Storton, P., Montik, N., Giannubilo, S. R., Litta, P., et al. (2013) Uterine fibroids: pathogenesis and interactions with endometrium and endomyometrial junction. Obstet Gynecol Int 2013: 173184.
   PubMedGoogle Scholar
• Dyson, M.T., Roqueiro, D. and Monsivais, D. (2014) Genome-wide DNA methylation analysis predicts an epigenetic switch for GATA factor expression in endometriosis. PLoS Genet 10: e1004158.
   PubMed Web of Science ®Google Scholar
• Forte, A., Cipollaro, M. and Galderisi, U. (2014) Genetic, epigenetic and stem cell alterations in endometriosis: new insights and potential therapeutic perspectives. Clin Sci (Lond) 126: 123–138.
   Google Scholar
• Fujimota, J., Hirose, R., Ichigo, S., Sakaguchi, H., Li, Y. and Tamaya, T. (1998) Expression of progesterone receptor form A and B mRNAs in uterine leiomyoma. Tumor Biol 19: 126–131.
   PubMed Web of Science ®Google Scholar
• Fung, J.N., Holdsworth-Carson, S.J., Sapkota, Y., Zhao, Z.Z., Jones, L., Girling, J.E., et al. (2015) Functional evaluation of genetic variants associated with endometriosis near GREB1. Hum Reprod 30(5): 1263–1275.
   PubMed Web of Science ®Google Scholar
• Gargett, C.E., Schwab, K.E., Zillwood, R.M., Nguyen, H.P. and Wu, D. (2009) Isolation and culture of epithelial progenitors and mesenchymal stem cells from human endometrium. Biol Reprod 80: 1136–1145.
   PubMed Web of Science ®Google Scholar
• Gotte, M., Wolf, M., Staebler, A., Buchweitz, O., Kelsch, R., Schuring A.N., et al. (2008) Increased expression of the adult stem cell marker Musashi-1 in endometriosis and endometrial carcinoma. J Pathol 215: 317–329.
   PubMed Web of Science ®Google Scholar
• Grings, A.O., Lora, V., Ferreira, G.D., Brum, I.S., Corleta, H. and Capp, E. (2012) Protein expression of estrogen receptors α and β and aromatase in myometrium and uterine leiomyoma. Gynecol Obstet Invest 73: 113–117.
   PubMed Web of Science ®Google Scholar
• Holzmann, C., Markowski, D.N., Koczan, D., Küpker, W., Helmkeand, B.M. and Bullerdiek, J. (2014) Cytogenetically normal uterine leiomyomas without MED12-mutations – a source to identify unknown mechanisms of the development of uterine smooth muscle tumors. Mol Cytogenet 7: 88–96.
   PubMed Web of Science ®Google Scholar
• Houshdaran, S., Zelenko, Z., Irwin, J.C. and Giudice, L.C. (2014) Human endometrial DNA methylome is cycle- dependent and is associated with gene expression regulation. Mol Endocrinol 28: 1118–1135.
   PubMed Web of Science ®Google Scholar
• Huang, H.P., Chen, P.H., Yu, C.Y., Chuang, C.Y., Stone, L., Hsiao, W.C., et al. (2011) Epithelial cell adhesion molecule (EpCAM) complex proteins promote transcription factor-mediated pluripotency reprogramming. J Biol Chem 286: 33520–33532.
   PubMed Web of Science ®Google Scholar
• Jolinière, J.B., Ayoubi, J.M.B., Gianaroli, L., Dubuisson, J.B., Gogusev, J. and Feki, A. (2014) Endometriosis: A new cellular and molecular genetic approach for understanding the pathogenesis and evolutivity. Front Surg 1: 16.
   Google Scholar
• Kalluri, R. (2009) EMT: when epithelial cells decide to become mesenchymal-like cells. J Clin Invest 119: 1417–1419.
   PubMed Web of Science ®Google Scholar
• Kim, J.J. and Sefton, E.C. (2012) The role of progesterone signaling in the pathogenesis of uterine leiomyoma. Mol Cell Endocrinol 358: 223–231.
   PubMed Web of Science ®Google Scholar
• Kim, S., Xu, X., Hecht, A. and Boyer, T.G. (2006) Mediator is a transducer of Wnt/beta-catenin signaling J Biol Chem 281: 14066–14075.
   PubMed Web of Science ®Google Scholar
• Kobayashi, H. (2014) Imprinting genes associated with endometriosis. EXCLI J 13:252-264.
   PubMed Web of Science ®Google Scholar
• Kobayashi, H, Iwai, K., Niiro, E., Morioka, S. and Yamada, Y. (2014) Fetal programming theory: implication for the understanding of endometriosis. Hum Immunol 75: 208–217.
   PubMed Web of Science ®Google Scholar
• Kocbek, V., Vouk, K., Bersinger, N.A., Mueller, M.D. and Rizner, L.T. (2015) Panels of cytokines and other secretory proteins as potential biomarkers of ovarian endometriosis. J Mol Diagn 17: 325–334.
   PubMed Web of Science ®Google Scholar
• Kunz, G., Beil, D., Huppert, P. Noe, M., Kissler, S. and Leyendecker, G. (2005) Adenomyosis in endometriosis – prevalence and impact on fertility. Evidence from magnetic resonance imaging. Human Reprod 20:2309- 2316.
   Google Scholar
• Larsen, S.B., Lundorf, E., Forman, A. and Dueholm, M. (2011) Adenomyosis and junctional zone changes in patients with endometriosis. Eur J Obstet Gynecol Reprod Biol 157: 206–211.
   PubMed Web of Science ®Google Scholar
• Laughlin, S.K., Herring, A.H., Savitz, D.A., Olshan, A.F., Fielding, J.R., Hartmann, K.E., et al. (2010) Pregnancy-related fibroid reduction. Fertil Steril 94: 2421–2423.
   PubMed Web of Science ®Google Scholar
• Leppert, P.C., Catherino, W.H. and Segars, J.H. (2006) A new hypothesis about the origin of uterine fibroids based on gene expression profiling with microarrays. Am J Obstet Gynecol 195: 415–420.
   PubMed Web of Science ®Google Scholar
• Mäkinen, N., Vahteristo, P., Bützow, R., Sjöberg, J. and Aaltonen, L.A. (2013) Exomic landscape of MED12 mutation-negative and –positive uterine leiomyomas. Intern J Cancer 134: 1008–1012.
   PubMed Web of Science ®Google Scholar
• Malik, M. and Catherino, W.H. (2012) Development and validation of a three-dimensional in vitro model for uterine leiomyoma and patient-matched myometrium. Fertil Steril 97:1287–1293.
   PubMed Web of Science ®Google Scholar
• Malik, M., Norian, J., McCarthy-Keith, D., Britten, J. and Catherino, W.H. (2010) Why leiomyomas are called fibroids: the central role of extracellular matrix in symptomatic women. Semin Reprod Med 28: 169–179.
   PubMed Web of Science ®Google Scholar
• Marsh, E.E., Lin, Z., Yin, P., Milad, M., Chakravarti, D. and Bulun, S.E. (2008) Differential expression of microRNA species in human uterine leiomyoma versus normal myometrium. Fertil Steril 89: 1771–1776.
   PubMed Web of Science ®Google Scholar
• Markowski, D.N., Helmke, B.M., Belge, G., Nimzyk, R., Bartnitzke, S., Deichert, U., et al. (2011) HMGA2 and p14Arf: major roles in cellular senescence of fibroids and therapeutic implications. Anticancer Res 31: 753–761.
   PubMed Web of Science ®Google Scholar
• Markowski, D.N., Helmke, B.M., Bernitzke, S., Loning, T. and Bullerdierk J. (2014) Uterine fibroids – do we deal with more than one disease? Int J Gynecol Pathol 33(6): 568–572.
   Google Scholar
• Maruyama, T. (2014) Endometrial stem/progenitor cells. J Obstet Gynec Res 40: 2015–2022.
   PubMed Web of Science ®Google Scholar
• Mas A., Cervello I., Gill-Sanchis, C. and Sim, C. (2014) Current understanding of somatic stem cells in leiomyoma formation. Fertil Steril 102(3):613–620.
   PubMed Web of Science ®Google Scholar
• Matsuzaki, S. and Darcha, C. (2012) Epithelial to mesenchymal transition-like and mesenchymal to epithelial transition-like processes might be involved in the pathogenesis of pelvic endometriosis. Hum Reprod 27: 712–721.
   PubMed Web of Science ®Google Scholar
• Miller, N.A., Farrow, E.G., Gibson, M., Willig, L.K., Twist, G., Yoo, B., et al. (2015) A 26-hour system of highly sensitive whole genome sequencing for emergency management of genetic disease. Genome Med 7: 100.
   Google Scholar
• Montgomery, G.W., Zondervan, K.T. and Nyholt, D.R. (2014) The future for genetic studies in reproduction. Mol Hum Reprod 20: 1–14.
   PubMed Web of Science ®Google Scholar
• Moroni, R.M., Vieira, C.S., Ferriani, R.A., Reis, R.M., Nogueira, A.A. and Brito, L.G. (2015) Presentation and treatment of uterine leiomyoma in adolescence: a systematic review. BMC Womens Health 15: 4.
   PubMed Web of Science ®Google Scholar
• Norian, J.M., Malik, M., Parker, C.Y., Joseph, D., Leppert, P.C. and Segars, J.H. (2009) Transforming growth factor beta3 regulates the versican variants in the extracellular matrix-rich uterine leiomyomas. Reprod Sci 16: 1153–1164.
   PubMed Web of Science ®Google Scholar
• Norian, J.M., Owen, C.M. and Taboas, J. (2012) Characterization of tissue biomechanics and mechanical signaling in uterine leiomyoma. Matrix Biol 31: 57–65.
   PubMed Web of Science ®Google Scholar
• Nothnick, W.B., Al-Hendy, A. and Lue, J.R. (2015) Circulating microRNAs as diagnostic biomarkers for endometriosis: privation and promise. J Minim Invasive Gynecol 22(5): 719–726.
   PubMed Web of Science ®Google Scholar
• Okamoto, M., Nasu1, K., Abe, W., Aoyagi, Y., Kawano, Y., Kai, K., et al. (2014) Enhanced miR-210 expression promotes the pathogenesis of endometriosis through activation of signal transducer and activator of transcription 3. Hum Reprod 30(3):632–641.
   PubMed Web of Science ®Google Scholar
• Okolo, S. (2008) Incidence, aetiology and epidemiology of uterine fibroids. Best Pract Res Clin Obstet Gynaecol 22(4): 571–588.
   PubMed Web of Science ®Google Scholar
• Ono, M., Qiang, W., Serna, V.A., Yin, P., Coon, J.S., Navarro, V.A., et al. (2012) Role of stem cells in human uterine leiomyoma growth. PLoS ONE 7(5): e36935.
   Web of Science ®Google Scholar
• Osinovskaya, N.S., Malysheva, O.V., Shved, N.Yu., Ivashchenko, T.E., Sultanov, I.Yu., Efimova, O.A., et al. (2015) Frequency and spectrum of MED12 exon 2 mutations in multiple versus solitary uterine leiomyomas from Russian patients. Int J Gynecol Pathol ( in press).
   PubMed Web of Science ®Google Scholar
• Padykula, H.A. (1991) Regeneration in the primate uterus: the role of stem cells. Ann N Y Acad Sci 622: 47–56.
   PubMedGoogle Scholar
• Pellegrini, C., Gori, I., Achtari, C., Hornung, D., Chardonnens, E., Wunder, D., et al. (2012) The expression of estrogen receptors as well as GREB1, c-MYC, and cyclin D1, estrogenregulated genes implicated in proliferation, is increased in peritoneal endometriosis. Fertil Steril 98: 1200–1208.
   Google Scholar
• Pfaundler, M. and von Sehr, L. (1922) Weiteres uber Syntropie kindlicher Krankheitzzustande. Z Kinderheilkd 30: 298–313.
   Google Scholar
• Pittatore, G., Moggio, A., Benedetto, C., Bussolati, B. and Revelli, A. (2013) Endometrial Adult/Progenitor Stem Cells: Pathogenetic Theory and New Antiangiogenic Approach for Endometriosis Therapy. Reprod Sci 21(3):296–304.
   PubMed Web of Science ®Google Scholar
• Proestling, K., Birner, P., Gamperl, S., Nirtl, N, Marton, E., Yerlikaya, G., et al. (2015) Enhanced epithelial to mesenchymal transition (EMT) and upregulated MYC in ectopic lesions contribute independently to endometriosis. Reprod Biol Endocrinol 13: 75.
   PubMed Web of Science ®Google Scholar
• Puzyrev, V.P., Makeeva, O.A. and Freidin, M.B. (2010) Syntropy, genetic testing and personalized medicine. Personalized Med 7: 399–405.
   PubMed Web of Science ®Google Scholar
• Rahmioglu, N., Nyholt, D.R., Morris, A.P., Missmer, S.A., Montgomery, G.W. and Zodervan, K.T. (2014) Genetic variants underlying risk of endometriosis: insight from meta-analysis of eight genome-wide association and replication datasets. Hum Reprod Update 20: 702–716.
   PubMed Web of Science ®Google Scholar
• Sasson, I.E. and Taylor, H.S. (2008) Stem cells and the pathogenesis of endometriosis. Ann NY Acad Sci 1127: 106–115.
   PubMed Web of Science ®Google Scholar
• Schwab, K.E., Hutchinson, P. and Gargett, C.E. (2008) Identification of surface markers for prospective isolation of human endometrial stromal colony-forming cells. Hum Reprod 23: 934–943.
   PubMed Web of Science ®Google Scholar
• Signorilea, P.G. and Baldia, A. (2015) New evidence in endometriosis. Int J Biochem Cell Biol 60: 19–22.
   PubMed Web of Science ®Google Scholar
• Sotomayor, P., Godoy, A., Smith, G.J. and Huss, W.J. (2009) Oct4A is expressed by a subpopulation of prostate neuroendocrine cells. Prostate 69:401–410.
   PubMed Web of Science ®Google Scholar
• Su, J., You, P., Li, W.L., Tao, X.R., Zhu, H.Y., Yao, Y.C., et al. (2010) The existence of multipotent stem cells with epithelial-mesenchymal transition features in the human liver bud. Int J Biochem Cell Biol 42: 2047–2055.
   PubMed Web of Science ®Google Scholar
• Sun, F.Q., Duan, H., Wang, S. and Li, J.J. (2015) 17β-Estradiol Induces Overproliferation in Adenomyotic Human Uterine Smooth Muscle Cells of the Junctional Zone Through Hyperactivation of the Estrogen Receptor-Enhanced RhoA/ROCK Signaling Pathway. Reprod Sci 22(11): 1436–1444.
   PubMed Web of Science ®Google Scholar
• Suryawanshi, S., Vlad, A.M., Lin, H.M. and Mantia-Smaldone, G. (2013) Plasma microRNAs as novel biomarkers for endometriosis and endometriosis-associated ovarian cancer. Clin Cancer Res 19: 1213–1224.
   PubMed Web of Science ®Google Scholar
• Tal, R. and Segars, J.H. (2014) The role of angiogenic factors in fibroid pathogenesis: potential implications for future therapy. Hum Reprod Update 20: 194–216.
   PubMed Web of Science ®Google Scholar
• Thiery, J.P., Acloque, H., Huang, R.Y. and Nieto, M.A. (2009) Epithelial-mesenchymal transitions in development and disease. Cell 139: 871–890.
   PubMed Web of Science ®Google Scholar
• Tocci, A., Greco, E. and Ubaldi, F.M. (2008) Adenomyosis and endometrial-ubendometrial myometrium unit disruption disease are two different entities. Reprod Biomed Online 17: 285–291.
   Web of Science ®Google Scholar
• Tulac, S., Nayak, N.R., Kao, L.C., VanWaes, M., Huang, J., Lobo, S., et al. (2003) Identification, characterization, and regulation of the canonical Wnt signaling pathway in human endometrium. J Clin Endocrinol Metab 88: 3860–3866.
   Google Scholar
• Waddington, C.H. (1966) Principles of development and differentiation. New York, Macmillan Pub Co Inc.
   Google Scholar
• Wang, T., Zhang, X., Obijuru, L., Laser, J., Aris, V., Lee, P., et al. (2007) A micro-RNA signature associated with race, tumor size, and target gene activity in human uterine leiomyomas. Genes Chromosomes Cancer 46: 336–347.
   PubMed Web of Science ®Google Scholar
• Wei, J., Chiriboga, L. and Mittal K. (2005) Expression profile of the tumorigenic factors associated with tumor size and sex steroid hormone status in uterine leiomyomata. Fertil Steril 84: 474–484.
   PubMed Web of Science ®Google Scholar
• Yamagata, Y., Maekawa, R. and Asada, H. (2009) Aberrant DNA methylation status in human uterine leiomyoma. Mol Hum Reprod 15: 259–267.
   PubMed Web of Science ®Google Scholar
• Yang, J., Mani, S.A., Donaher, J.L., Ramaswamy, S., Itzykson, R.A. and Come, C. (2004) Twist, a master regulator 380 of morphogenesis, plays an essential role in tumor metastasis. Cell 117: 927–939.
   Google Scholar
• Yang, W., Zhang, Y., Fu, F. and Li, R. (2013) High-resolution array-comparative genomic hybridization profiling reveals 20q13.33 alterations associated with ovarian endometriosis. Gynecol Endocrinol 29: 603–607.
   PubMed Web of Science ®Google Scholar
• Ying, Z. and Weiyuan, Z. (2009) Dual actions of progesterone on uterine leiomyoma correlate with the ratio of progesterone receptor A:B. Gynec Endocrinol 25: 520–523.
   PubMed Web of Science ®Google Scholar
• Zhang, Y., Yu, P., Sun, F., Li, T.C., Cheng, Jm. and Duan H. (2015) Expression of oxytocin receptors in the uterine junctional zone in women with adenomyosis. Acta Obstet Gynecol Scand 94(4): 412–418.
   PubMed Web of Science ®Google Scholar
• Zondervan, K.T., Cardon, L.R. and Kennedy, S.H. (2001) The genetic basis of endometriosis. Curr Opin Obstet Gynecol 13: 309–314.
   PubMed Web of Science ®Google Scholar
• Zondervan, K.T, Cardon, L.R. and Kennedy, S.H. (2002) What makes a good case-control study? Design issues for complex traits such as endometriosis. Hum Reprod 17: 1415–1423.
   PubMed Web of Science ®Google Scholar