Endometriosis in Experimental Models

To investigate the factors involved in the initiation and progression of endometriosis, an animal model of this disease has been employed. Animal models are often used to investigate factors affecting the initiation and progression of endometriosis. This chapter describes these models and focuses on the murine model of endometriosis as a potential tool to evaluate therapies. The traditional explanation for the existence of endometrium in ectopic locations is based on the common occurrence of retrograde menstruation. This implantation hypothesis is widely accepted as the etiology of endometriosis. Animal models are crucial for elucidating the mechanisms underlying endometriosis. Several animal models of endometriosis have been used in the past, most of which consist of transplanting endometrium into the peritoneal cavity. Because primates spontaneously develop endometriosis, primate models most closely resemble the disease in women; however, rodent models are more cost effective and readily available. Nevertheless, since rodents do not menstruate, rodent models used for the research in endometriosis have certain limitations. We addressed the question whether a murine endometriosis model is suitable for evaluating drugs employed in human endometriosis. We concluded that the murine endometriosis model may be a valuable and reliable tool for evaluating new therapeutic approaches in human endometriosis. The authors have no conflicts to disclose relative to this work. Access this chapter Tax calculation will be finalised at checkout Purchases are for personal use only Similar content being viewed by others

Sampson JA. Metastatic or embolic endometriosis, due to the menstrual dissemination of endometrial tissue into the venous circulation. Am J Pathol. 1927;3:93–110.43. Giudice LC, Kao LC. Endometriosis. Lancet. 2004;364:1789–99. MacKenzie WF, Casey HW. Animal model of human disease. Endometriosis. Animal model: endometriosis in rhesus monkeys. Am J Pathol. 1975;80:341–4. Scott RB, Te Linde RW, Wharton Jr LR. Further studies on experimental endometriosis. Am J Obstet Gynecol. 1953;66:1082–103. Donnez O, Soares M, Defrere S, Dehoux JP, van Langendonckt A, et al. Nerve fiber density in deep nodular endometriotic lesions induced in a baboon experimental model. Fertil Steril. 2013;100(4):1144–50. Langoi D, Pavone ME, Gurates B, Chai D, Fazleabas A, et al. Aromatase inhibitor treatment limits progression of peritoneal endometriosis in baboons. Fertil Steril. 2013;99(656–662):e653. Lebovic DI, Mwenda JM, Chai DC, Santi A, Xu X, et al. Peroxisome proliferator-activated receptor-(gamma) receptor ligand partially prevents the development of endometrial explants in baboons: a prospective, randomized, placebo-controlled study. Endocrinology. 2010;151:1846–52. Golan A, Dargenio R, Winston RM. The effect of treatment on experimentally produced endometrial peritoneal implants. Fertil Steril. 1986;46:954–8. Vernon MW, Wilson EA. Studies on the surgical induction of endometriosis in the rat. Fertil Steril. 1985;44:684–94. Abbas MA, Taha MO, Disi AM, Shomaf M. Regression of endometrial implants treated with vitamin D in a rat model of endometriosis. Eur J Pharmacol. 2013;715:72–5. Stilley JA, Sharpe-Timms KL. TIMP1 contributes to ovarian anomalies in both an MMP-dependent and -independent manner in a rat model. Biol Reprod. 2012;86:47. Yuan P, Chen B, Huang Y, Xin X. Long-term regression of experimental endometriosis in a rat model treated with local application of levonorgestrel-loaded biodegradable microspheres. Hum Reprod. 2012;27:2089–95. Rock JA, Prendergast RA, Bobbie D, Green WR, Parmley TH, et al. Intraocular endometrium in the rabbit as a model for endometriosis. Fertil Steril. 1993;59:232–5. Yuan P, Huang Y, Wu H, Teng Z, Zhang J, et al. Induction of a local pseudo-pregnancy via levonorgestrel-loaded microspheres for the treatment of endometriosis in a rabbit model. Hum Reprod. 2010;25:462–9. Zamah NM, Dodson MG, Stephens LC, Buttram Jr VC, Besch PK, et al. Transplantation of normal and ectopic human endometrial tissue into athymic nude mice. Am J Obstet Gynecol. 1984;149:591–7. Fortin M, Lepine M, Merlen Y, Thibeault I, Rancourt C, et al. Quantitative assessment of human endometriotic tissue maintenance and regression in a noninvasive mouse model of endometriosis. Mol Ther. 2004;9:540–7. Aoki D, Katsuki Y, Shimizu A, Kakinuma C, Nozawa S. Successful heterotransplantation of human endometrium in SCID mice. Obstet Gynecol. 1994;83:220–8. Cummings AM, Metcalf JL. Induction of endometriosis in mice: a new model sensitive to estrogen. Reprod Toxicol. 1995;9:233–8. Grummer R, Schwarzer F, Bainczyk K, Hess-Stumpp H, Regidor PA, et al. Peritoneal endometriosis: validation of an in-vivo model. Hum Reprod. 2001;16:1736–43. Rossi G, Somigliana E, Moschetta M, Santorsola R, Cozzolino S, et al. Dynamic aspects of endometriosis in a mouse model through analysis of implantation and progression. Arch Gynecol Obstet. 2000;263:102–7. Hirata T, Osuga Y, Yoshino O, Hirota Y, Harada M, et al. Development of an experimental model of endometriosis using mice that ubiquitously express green fluorescent protein. Hum Reprod. 2005;20:2092–6. Story L, Kennedy S. Animal studies in endometriosis: a review. ILAR J. 2004;45:132–8. Tirado-Gonzalez I, Barrientos G, Tariverdian N, Arck PC, Garcia MG, et al. Endometriosis research: animal models for the study of a complex disease. J Reprod Immunol. 2010;86:141–7. Lee B, Du H, Taylor HS. Experimental murine endometriosis induces DNA methylation and altered gene expression in eutopic endometrium. Biol Reprod. 2009;80:79–85. Bruner-Tran KL, Eisenberg E, Yeaman GR, Anderson TA, McBean J, et al. Steroid and cytokine regulation of matrix metalloproteinase expression in endometriosis and the establishment of experimental endometriosis in nude mice. J Clin Endocrinol Metab. 2002;87:4782–91. Styer AK, Sullivan BT, Puder M, Arsenault D, Petrozza JC, et al. Ablation of leptin signaling disrupts the establishment, development, and maintenance of endometriosis-like lesions in a murine model. Endocrinology. 2008;149:506–14. Burns KA, Rodriguez KF, Hewitt SC, Janardhan KS, Young SL, et al. Role of estrogen receptor signaling required for endometriosis-like lesion establishment in a mouse model. Endocrinology. 2012;153:3960–71. Takai E, Taniguchi F, Nakamura K, Uegaki T, Iwabe T, et al. Parthenolide reduces cell proliferation and prostaglandin E synthesis in human endometriotic stromal cells and inhibits development of endometriosis in the murine model. Fertil Steril. 2013;100(4):1170–8. Sokalska A, Anderson M, Villanueva J, Ortega I, Bruner-Tran KL, et al. Effects of simvastatin on retinoic acid system in primary human endometrial stromal cells and in a chimeric model of human endometriosis. J Clin Endocrinol Metab. 2013;98:E463–71. Daftary GS, Zheng Y, Tabbaa ZM, Schoolmeester JK, Gada RP, et al. A novel role of the Sp/KLF transcription factor KLF11 in arresting progression of endometriosis. PLoS One. 2013;8:e60165. Rudzitis-Auth J, Menger MD, Laschke MW. Resveratrol is a potent inhibitor of vascularization and cell proliferation in experimental endometriosis. Hum Reprod. 2013;28:1339–47. Novella-Maestre E, Herraiz S, Vila-Vives JM, Carda C, Ruiz-Sauri A, et al. Effect of antiangiogenic treatment on peritoneal endometriosis-associated nerve fibers. Fertil Steril. 2012;98:1209–17. Han SJ, Hawkins SM, Begum K, Jung SY, Kovanci E, et al. A new isoform of steroid receptor coactivator-1 is crucial for pathogenic progression of endometriosis. Nat Med. 2012;18:1102–11. Mariani M, Vigano P, Gentilini D, Camisa B, Caporizzo E, et al. The selective vitamin D receptor agonist, elocalcitol, reduces endometriosis development in a mouse model by inhibiting peritoneal inflammation. Hum Reprod. 2012;27:2010–9. Wieser F, Wu J, Shen Z, Taylor RN, Sidell N. Retinoic acid suppresses growth of lesions, inhibits peritoneal cytokine secretion, and promotes macrophage differentiation in an immunocompetent mouse model of endometriosis. Fertil Steril. 2012;97:1430–7. Cakmak H, Basar M, Seval-Celik Y, Osteen KG, Duleba AJ, et al. Statins inhibit monocyte chemotactic protein 1 expression in endometriosis. Reprod Sci. 2012;19:572–9. Leconte M, Nicco C, Ngo C, Chereau C, Chouzenoux S, et al. The mTOR/AKT inhibitor temsirolimus prevents deep infiltrating endometriosis in mice. Am J Pathol. 2011;179:880–9. Olivares C, Ricci A, Bilotas M, Baranao RI, Meresman G. The inhibitory effect of celecoxib and rosiglitazone on experimental endometriosis. Fertil Steril. 2011;96:428–33. Kulak Jr J, Fischer C, Komm B, Taylor HS. Treatment with bazedoxifene, a selective estrogen receptor modulator, causes regression of endometriosis in a mouse model. Endocrinology. 2011;152:3226–32. Lu Y, Nie J, Liu X, Zheng Y, Guo SW. Trichostatin A, a histone deacetylase inhibitor, reduces lesion growth and hyperalgesia in experimentally induced endometriosis in mice. Hum Reprod. 2010;25:1014–25. Jain NK, Kulkarni SK. Antinociceptive and anti-inflammatory effects of Tanacetum parthenium L. extract in mice and rats. J Ethnopharmacol. 1999;68:251–9. Guzman ML, Rossi RM, Karnischky L, Li X, Peterson DR, et al. The sesquiterpene lactone parthenolide induces apoptosis of human acute myelogenous leukemia stem and progenitor cells. Blood. 2005;105:4163–9. Liu JW, Cai MX, Xin Y, Wu QS, Ma J, et al. Parthenolide induces proliferation inhibition and apoptosis of pancreatic cancer cells in vitro. J Exp Clin Cancer Res. 2010;29:108. Sweeney CJ, Mehrotra S, Sadaria MR, Kumar S, Shortle NH, et al. The sesquiterpene lactone parthenolide in combination with docetaxel reduces metastasis and improves survival in a xenograft model of breast cancer. Mol Cancer Ther. 2005;4:1004–12. Pelch KE, Sharpe-Timms KL, Nagel SC. Mouse model of surgically-induced endometriosis by auto-transplantation of uterine tissue. J Vis Exp. 2012;59:e3396 doi 10.3791/3396. Cummings AM, Hedge JM, Birnbaum LS. Effect of prenatal exposure to TCDD on the promotion of endometriotic lesion growth by TCDD in adult female rats and mice. Toxicol Sci. 1999;52:45–9. Sharpe-Timms KL, Piva M, Ricke EA, Surewicz K, Zhang YL, et al. Endometriotic lesions synthesize and secrete a haptoglobin-like protein. Biol Reprod. 1998;58:988–94. Yavuz E, Oktem M, Esinler I, Toru SA, Zeyneloglu HB. Genistein causes regression of endometriotic implants in the rat model. Fertil Steril. 2007;88:1129–34. Dmitrieva N, Nagabukuro H, Resuehr D, Zhang G, McAllister SL, et al. Endocannabinoid involvement in endometriosis. Pain. 2010;151:703–10. Efstathiou JA, Sampson DA, Levine Z, Rohan RM, Zurakowski D, et al. Nonsteroidal antiinflammatory drugs differentially suppress endometriosis in a murine model. Fertil Steril. 2005;83:171–81. Becker CM, Sampson DA, Short SM, Javaherian K, Folkman J, et al. Short synthetic endostatin peptides inhibit endothelial migration in vitro and endometriosis in a mouse model. Fertil Steril. 2006;85:71–7. Author information Authors and Affiliations Corresponding author Editor information Editors and Affiliations Rights and permissions Copyright information © 2014 Springer Japan About this chapter Cite this chapter Taniguchi, F., Harada, T. (2014). Endometriosis in Experimental Models. In: Harada, T. (eds) Endometriosis. Springer, Tokyo. https://doi.org/10.1007/978-4-431-54421-0_14 Download citation DOI: https://doi.org/10.1007/978-4-431-54421-0_14 Published: Publisher Name: Springer, Tokyo Print ISBN: 978-4-431-54420-3 Online ISBN: 978-4-431-54421-0 eBook Packages: MedicineMedicine (R0)