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From Mice to Primates: Assessing Hormone-Based Endometriosis Models for Preclinical and Therapeutic Insights

Articles InPress

Document Type : Review Article

Authors

1 Department of Natural Sciences, West Kazakhstan Marat Ospanov Medical University, Aktobe, Kazakhstan

2 Stem Cells Technology Research Center, Shiraz University of Medical Sciences, Shiraz, Iran;

3 PerciaVista R&D Co., Shiraz, Iran

4 Stem Cell Research Center, Tabriz University of Medical Sciences, Tabriz, Iran

5 Department of Applied Cell Sciences, Faculty of Advanced Medical Sciences, Tabriz University of Medical Sciences, Tabriz, Iran

6 Department of General Surgery, West Kazakhstan Medical University, Aktobe, Kazakhstan

7 Department of Family Medicine No 1, Astana Medical University, Astana, Kazakhstan

8 Department of Internal Medicine No. 1, West Kazakhstan Marat Ospanov Medical University, Aktobe, Kazakhstan

9 Department of Psychology, West Kazakhstan Marat Ospanov Medical University, Aktobe, Republic of Kazakhstan

10 Department of Languages, West Kazakhstan Marat Ospanov Medical University, Aktobe, Kazakhstan

11 Department of Therapeutic and Prosthetic Dentistry, West Kazakhstan Marat Ospanov Medical University, Aktobe, Kazakhstan

12 Health Management Center, The Fifth People's Hospital of Chongqing,Chongqing,400060, China

10.30476/ijms.2025.105805.3975

Abstract

Endometriosis, a complex gynecological disorder characterized by ectopic endometrial-like tissue, affects over 10% of women, causing chronic pain and infertility. Despite extensive research, its pathophysiology remains incompletely understood, with proposed mechanisms including inflammation, hormonal dysregulation, and retrograde menstruation. Given ethical and practical challenges in human studies, animal models are essential for investigating endometriosis pathogenesis and evaluating therapeutic interventions. This review examines hormone-related animal models of endometriosis, comparing induction methods (autotransplantation, xenotransplantation, and spontaneous models) and their applications in studying sex steroid hormones (SSH) and the hypothalamic-pituitary-gonadal (HPG) axis. We analyzed 158 studies (2010–2024) from PubMed Central/Medline, focusing on SSH and HPG axis involvement. A novel scoring system was developed to assess the model’s suitability based on species, induction method, pharmacological effects, hormonal/genetic evaluations, histological confirmation, feasibility, ethics, and cost. Non-human primate models, particularly spontaneous and hormone-induced baboon models, scored highest due to their physiological resemblance to humans. However, rodent models remain widely used due to practicality. Our findings highlight the need for improved preclinical models to enhance translational research, ultimately aiding in the development of targeted therapies for endometriosis. This comprehensive analysis provides a framework for selecting optimal animal models in future endometriosis research.

Highlights

Amin Tamadon (Google Scholar)

Chong Fu (Google Scholar)

Keywords

References
  1. Moradi Y, Shams-Beyranvand M, Khateri S, Gharahjeh S, Tehrani S, Varse F, et al. A systematic review on the prevalence of endometriosis in women. Indian J Med Res. 2021;154:446-54. doi: 10.4103/ijmr.IJMR_817_18. PubMed PMID: 35345070; PubMed Central PMCID: PMCPMC9131783.
  2. Sarria-Santamera A, Orazumbekova B, Terzic M, Issanov A, Chaowen C, Asunsolo-Del-Barco A. Systematic Review and Meta-Analysis of Incidence and Prevalence of Endometriosis. Healthcare (Basel). 2020;9. doi: 10.3390/healthcare9010029. PubMed PMID: 33396813; PubMed Central PMCID: PMCPMC7824417.
  3. Malvezzi H, Marengo EB, Podgaec S, Piccinato CA. Endometriosis: current challenges in modeling a multifactorial disease of unknown etiology. J Transl Med. 2020;18:311. doi: 10.1186/s12967-020-02471-0. PubMed PMID: 32787880; PubMed Central PMCID: PMCPMC7425005.
  4. Malutan AM, Drugan T, Costin N, Ciortea R, Bucuri C, Rada MP, et al. Pro-inflammatory cytokines for evaluation of inflammatory status in endometriosis. Cent Eur J Immunol. 2015;40:96-102. doi: 10.5114/ceji.2015.50840. PubMed PMID: 26155190; PubMed Central PMCID: PMCPMC4472546.
  5. Riccio L, Santulli P, Marcellin L, Abrao MS, Batteux F, Chapron C. Immunology of endometriosis. Best Pract Res Clin Obstet Gynaecol. 2018;50:39-49. doi: 10.1016/j.bpobgyn.2018.01.010. PubMed PMID: 29506962.
  6. Bellelis P, Podgaec S, Abrao MS. Environmental factors and endometriosis. Rev Assoc Med Bras (1992). 2011;57:448-52. doi: 10.1590/s0104-42302011000400022. PubMed PMID: 21876930.
  7. Sapkota Y, Steinthorsdottir V, Morris AP, Fassbender A, Rahmioglu N, De Vivo I, et al. Meta-analysis identifies five novel loci associated with endometriosis highlighting key genes involved in hormone metabolism. Nat Commun. 2017;8:15539. doi: 10.1038/ncomms15539. PubMed PMID: 28537267; PubMed Central PMCID: PMCPMC5458088.
  8. Maddern J, Grundy L, Castro J, Brierley SM. Pain in Endometriosis. Front Cell Neurosci. 2020;14:590823. doi: 10.3389/fncel.2020.590823. PubMed PMID: 33132854; PubMed Central PMCID: PMCPMC7573391.
  9. Practice Committee of the American Society for Reproductive M. Endometriosis and infertility: a committee opinion. Fertil Steril. 2012;98:591-8. doi: 10.1016/j.fertnstert.2012.05.031. PubMed PMID: 22704630.
  10. Sampson JA. The development of the implantation theory for the origin of peritoneal endometriosis. American Journal of Obstetrics and Gynecology. 1940;40:549-57. doi: 10.1016/s0002-9378(40)91238-8.
  11. Sampson JA. Heterotopic or misplaced endometrial tissue. American Journal of Obstetrics and Gynecology. 1925;10:649-64. doi: 10.1016/S0002-9378(25)90629-1.
  12. Maruyama T. A Revised Stem Cell Theory for the Pathogenesis of Endometriosis. J Pers Med. 2022;12. doi: 10.3390/jpm12020216. PubMed PMID: 35207704; PubMed Central PMCID: PMCPMC8875896.
  13. Lamceva J, Uljanovs R, Strumfa I. The Main Theories on the Pathogenesis of Endometriosis. Int J Mol Sci. 2023;24. doi: 10.3390/ijms24054254. PubMed PMID: 36901685; PubMed Central PMCID: PMCPMC10001466.
  14. Bulun SE, Monsivais D, Kakinuma T, Furukawa Y, Bernardi L, Pavone ME, et al. Molecular biology of endometriosis: from aromatase to genomic abnormalities. Semin Reprod Med. 2015;33:220-4. doi: 10.1055/s-0035-1554053. PubMed PMID: 26036904.
  15. Giudice LC. Clinical practice. Endometriosis. N Engl J Med. 2010;362:2389-98. doi: 10.1056/NEJMcp1000274. PubMed PMID: 20573927; PubMed Central PMCID: PMCPMC3108065.
  16. Stratton P, Berkley KJ. Chronic pelvic pain and endometriosis: translational evidence of the relationship and implications. Hum Reprod Update. 2011;17:327-46. doi: 10.1093/humupd/dmq050. PubMed PMID: 21106492; PubMed Central PMCID: PMCPMC3072022.
  17. Bulun SE, Monsavais D, Pavone ME, Dyson M, Xue Q, Attar E, et al. Role of estrogen receptor-beta in endometriosis. Semin Reprod Med. 2012;30:39-45. doi: 10.1055/s-0031-1299596. PubMed PMID: 22271293; PubMed Central PMCID: PMCPMC4034571.
  18. Prossnitz ER, Barton M. The G-protein-coupled estrogen receptor GPER in health and disease. Nat Rev Endocrinol. 2011;7:715-26. doi: 10.1038/nrendo.2011.122. PubMed PMID: 21844907; PubMed Central PMCID: PMCPMC3474542.
  19. Erol A, Ho AM, Winham SJ, Karpyak VM. Sex hormones in alcohol consumption: a systematic review of evidence. Addict Biol. 2019;24:157-69. doi: 10.1111/adb.12589. PubMed PMID: 29280252; PubMed Central PMCID: PMCPMC6585852.
  20. Chen Y, Chen C, Shi S, Han J, Wang J, Hu J, et al. Endometriotic implants regress in rat models treated with puerarin by decreasing estradiol level. Reprod Sci. 2011;18:886-91. doi: 10.1177/1933719111398500. PubMed PMID: 21673282.
  21. Berkley KJ, Dmitrieva N, Curtis KS, Papka RE. Innervation of ectopic endometrium in a rat model of endometriosis. Proc Natl Acad Sci U S A. 2004;101:11094-8. doi: 10.1073/pnas.0403663101. PubMed PMID: 15256593; PubMed Central PMCID: PMCPMC491992.
  22. Li Z, Liu H, He Z, Zhang G, Lang J. Effects of cisplatin and letrozole on surgically induced endometriosis and comparison of the two medications in a rat model. Eur J Pharm Sci. 2016;93:132-40. doi: 10.1016/j.ejps.2016.07.018. PubMed PMID: 27481456.
  23. Korbel C, Menger MD, Laschke MW. Size and spatial orientation of uterine tissue transplants on the peritoneum crucially determine the growth and cyst formation of endometriosis-like lesions in mice. Hum Reprod. 2010;25:2551-8. doi: 10.1093/humrep/deq201. PubMed PMID: 20693239.
  24. Yang XJ, Yang J, Liu Z, Yang G, Shen ZJ. Telocytes damage in endometriosis-affected rat oviduct and potential impact on fertility. J Cell Mol Med. 2015;19:452-62. doi: 10.1111/jcmm.12427. PubMed PMID: 25388530; PubMed Central PMCID: PMCPMC4407595.
  25. Appleyard CB, Cruz ML, Rivera E, Hernandez GA, Flores I. Experimental endometriosis in the rat is correlated with colonic motor function alterations but not with bacterial load. Reprod Sci. 2007;14:815-24. doi: 10.1177/1933719107309722. PubMed PMID: 18089600.
  26. Vernon MW, Wilson EA. Studies on the surgical induction of endometriosis in the rat. Fertil Steril. 1985;44:684-94. PubMed PMID: 4054348.
  27. Prather GR, MacLean JA, 2nd, Shi M, Boadu DK, Paquet M, Hayashi K. Niclosamide As a Potential Nonsteroidal Therapy for Endometriosis That Preserves Reproductive Function in an Experimental Mouse Model. Biol Reprod. 2016;95:76. doi: 10.1095/biolreprod.116.140236. PubMed PMID: 27535961; PubMed Central PMCID: PMCPMC5333938.
  28. Zhao Y, Li Q, Katzenellenbogen BS, Lau LF, Taylor RN, Bagchi IC, et al. Estrogen-induced CCN1 is critical for establishment of endometriosis-like lesions in mice. Mol Endocrinol. 2014;28:1934-47. doi: 10.1210/me.2014-1080. PubMed PMID: 25321413; PubMed Central PMCID: PMCPMC4250364.
  29. Greaves E, Cousins FL, Murray A, Esnal-Zufiaurre A, Fassbender A, Horne AW, et al. A novel mouse model of endometriosis mimics human phenotype and reveals insights into the inflammatory contribution of shed endometrium. Am J Pathol. 2014;184:1930-9. doi: 10.1016/j.ajpath.2014.03.011. PubMed PMID: 24910298; PubMed Central PMCID: PMCPMC4076466.
  30. Greaves E, Temp J, Esnal-Zufiurre A, Mechsner S, Horne AW, Saunders PT. Estradiol is a critical mediator of macrophage-nerve cross talk in peritoneal endometriosis. Am J Pathol. 2015;185:2286-97. doi: 10.1016/j.ajpath.2015.04.012. PubMed PMID: 26073038; PubMed Central PMCID: PMCPMC4530129.
  31. Taylor HS, Alderman Iii M, D’Hooghe TM, Fazleabas AT, Duleba AJ. Effect of simvastatin on baboon endometriosis. Biol Reprod. 2017;97:32-8. doi: 10.1093/biolre/iox058. PubMed PMID: 28637327; PubMed Central PMCID: PMCPMC6248548.
  32. D’Hooghe TM, Bambra CS, Raeymaekers BM, De Jonge I, Lauweryns JM, Koninckx PR. Intrapelvic injection of menstrual endometrium causes endometriosis in baboons (Papio cynocephalus and Papio anubis). Am J Obstet Gynecol. 1995;173:125-34. doi: 10.1016/0002-9378(95)90180-9. PubMed PMID: 7631669.
  33. Zhao Y, Gong P, Chen Y, Nwachukwu JC, Srinivasan S, Ko C, et al. Dual suppression of estrogenic and inflammatory activities for targeting of endometriosis. Sci Transl Med. 2015;7:271. doi: 10.1126/scitranslmed.3010626. PubMed PMID: 25609169; PubMed Central PMCID: PMCPMC4790140.
  34. Becker CM, Wright RD, Satchi-Fainaro R, Funakoshi T, Folkman J, Kung AL, et al. A novel noninvasive model of endometriosis for monitoring the efficacy of antiangiogenic therapy. Am J Pathol. 2006;168:2074-84. doi: 10.2353/ajpath.2006.051133. PubMed PMID: 16723720; PubMed Central PMCID: PMCPMC1606629.
  35. Kulak J, Jr., 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. doi: 10.1210/en.2010-1010. PubMed PMID: 21586552; PubMed Central PMCID: PMCPMC3138238.
  36. 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. doi: 10.1093/humrep/des142. PubMed PMID: 22563024.
  37. Zhang J, Zhu Y, Zhou X, Hao S, Xie S, Zhou J, et al. Evaluation of biodegradable microspheres containing nomegestrol acetate in a rat model of endometriosis. Eur J Pharm Sci. 2014;65:15-20. doi: 10.1016/j.ejps.2014.08.011. PubMed PMID: 25201168.
  38. Mishra A, Galvankar M, Singh N, Modi D. Spatial and temporal changes in the expression of steroid hormone receptors in mouse model of endometriosis. J Assist Reprod Genet. 2020;37:1069-81. doi: 10.1007/s10815-020-01725-6. PubMed PMID: 32152908; PubMed Central PMCID: PMCPMC7300172.
  39. Pelch KE, Sharpe-Timms KL, Nagel SC. Mouse model of surgically-induced endometriosis by auto-transplantation of uterine tissue. J Vis Exp. 2012:e3396. doi: 10.3791/3396. PubMed PMID: 22257948; PubMed Central PMCID: PMCPMC3339870.
  40. Vasquez YM, Wu SP, Anderson ML, Hawkins SM, Creighton CJ, Ray M, et al. Endometrial Expression of Steroidogenic Factor 1 Promotes Cystic Glandular Morphogenesis. Mol Endocrinol. 2016;30:518-32. doi: 10.1210/me.2015-1215. PubMed PMID: 27018534; PubMed Central PMCID: PMCPMC4853565.
  41. Han SJ, Hawkins SM, Begum K, Jung SY, Kovanci E, Qin J, et al. A new isoform of steroid receptor coactivator-1 is crucial for pathogenic progression of endometriosis. Nat Med. 2012;18:1102-11. doi: 10.1038/nm.2826. PubMed PMID: 22660634; PubMed Central PMCID: PMCPMC3541027.
  42. Palmer SS, Altan M, Denis D, Tos EG, Gotteland JP, Osteen KG, et al. Bentamapimod (JNK Inhibitor AS602801) Induces Regression of Endometriotic Lesions in Animal Models. Reprod Sci. 2016;23:11-23. doi: 10.1177/1933719115600553. PubMed PMID: 26335175; PubMed Central PMCID: PMCPMC5933194.
  43. Bruner KL, Eisenberg E, Gorstein F, Osteen KG. Progesterone and transforming growth factor-beta coordinately regulate suppression of endometrial matrix metalloproteinases in a model of experimental endometriosis. Steroids. 1999;64:648-53. doi: 10.1016/s0039-128x(99)00048-3. PubMed PMID: 10503723.
  44. Heard ME, Melnyk SB, Simmen FA, Yang Y, Pabona JM, Simmen RC. High-Fat Diet Promotion of Endometriosis in an Immunocompetent Mouse Model is Associated With Altered Peripheral and Ectopic Lesion Redox and Inflammatory Status. Endocrinology. 2016;157:2870-82. doi: 10.1210/en.2016-1092. PubMed PMID: 27175969; PubMed Central PMCID: PMCPMC4929556.
  45. Hirata T, Osuga Y, Yoshino O, Hirota Y, Harada M, Takemura Y, et al. Development of an experimental model of endometriosis using mice that ubiquitously express green fluorescent protein. Hum Reprod. 2005;20:2092-6. doi: 10.1093/humrep/dei012. PubMed PMID: 15831509.
  46. Braundmeier AG, Fazleabas AT, Nowak RA. Extracellular matrix metalloproteinase inducer expression in the baboon endometrium: menstrual cycle and endometriosis. Reproduction. 2010;140:911-20. doi: 10.1530/REP-09-0481. PubMed PMID: 20841363; PubMed Central PMCID: PMCPMC5069969.
  47. Fazleabas AT, Brudney A, Gurates B, Chai D, Bulun S. A modified baboon model for endometriosis. Ann N Y Acad Sci. 2002;955:308-17; discussion 40-2, 96-406. doi: 10.1111/j.1749-6632.2002.tb02791.x. PubMed PMID: 11949957.
  48. Cummings AM, Metcalf JL. Induction of endometriosis in mice: a new model sensitive to estrogen. Reprod Toxicol. 1995;9:233-8. doi: 10.1016/0890-6238(95)00004-t. PubMed PMID: 7579907.
  49. Heard ME, Velarde MC, Giudice LC, Simmen FA, Simmen RC. Kruppel-Like Factor 13 Deficiency in Uterine Endometrial Cells Contributes to Defective Steroid Hormone Receptor Signaling but Not Lesion Establishment in a Mouse Model of Endometriosis. Biol Reprod. 2015;92:140. doi: 10.1095/biolreprod.115.130260. PubMed PMID: 25904015; PubMed Central PMCID: PMCPMC4652611.
  50. Colette S, Defrere S, Lousse JC, Van Langendonckt A, Gotteland JP, Loumaye E, et al. Inhibition of steroid sulfatase decreases endometriosis in an in vivo murine model. Hum Reprod. 2011;26:1362-70. doi: 10.1093/humrep/der079. PubMed PMID: 21441545.
  51. Defrere S, Van Langendonckt A, Gonzalez Ramos R, Jouret M, Mettlen M, Donnez J. Quantification of endometriotic lesions in a murine model by fluorimetric and morphometric analyses. Hum Reprod. 2006;21:810-7. doi: 10.1093/humrep/dei387. PubMed PMID: 16293650.
  52. Tang Q, Shang F, Wang X, Yang Y, Chen G, Chen Y, et al. Combination use of ferulic acid, ligustrazine and tetrahydropalmatine inhibits the growth of ectopic endometrial tissue: a multi-target therapy for endometriosis rats. J Ethnopharmacol. 2014;151:1218-25. doi: 10.1016/j.jep.2013.12.047. PubMed PMID: 24389027.
  53. Kumar R, Clerc AC, Gori I, Russell R, Pellegrini C, Govender L, et al. Lipoxin A(4) prevents the progression of de novo and established endometriosis in a mouse model by attenuating prostaglandin E(2) production and estrogen signaling. PLoS One. 2014;9:e89742. doi: 10.1371/journal.pone.0089742. PubMed PMID: 24587003; PubMed Central PMCID: PMCPMC3933674.
  54. Kim SM, Yoo T, Lee SY, Kim EJ, Lee SM, Lee MH, et al. Effect of SKI2670, a novel, orally active, non-peptide GnRH antagonist, on hypothalamic-pituitary-gonadal axis. Life Sci. 2015;139:166-74. doi: 10.1016/j.lfs.2015.08.016. PubMed PMID: 26321528.
  55. Cetinkaya N, Attar R, Yildirim G, Ficicioglu C, Ozkan F, Yilmaz B, et al. The effects of different doses of melatonin treatment on endometrial implants in an oophorectomized rat endometriosis model. Arch Gynecol Obstet. 2015;291:591-8. doi: 10.1007/s00404-014-3466-3. PubMed PMID: 25223860.
  56. Koc O, Gunduz B, Topcuoglu A, Bugdayci G, Yilmaz F, Duran B. Effects of pinealectomy and melatonin supplementation on endometrial explants in a rat model. Eur J Obstet Gynecol Reprod Biol. 2010;153:72-6. doi: 10.1016/j.ejogrb.2010.06.012. PubMed PMID: 20667645.
  57. Yildirim G, Attar R, Ozkan F, Kumbak B, Ficicioglu C, Yesildaglar N. The effects of letrozole and melatonin on surgically induced endometriosis in a rat model: a preliminary study. Fertil Steril. 2010;93:1787-92. doi: 10.1016/j.fertnstert.2009.09.021. PubMed PMID: 19878935.
  58. Guney M, Oral B, Karahan N, Mungan T. Regression of endometrial explants in a rat model of endometriosis treated with melatonin. Fertil Steril. 2008;89:934-42. doi: 10.1016/j.fertnstert.2007.04.023. PubMed PMID: 17582405.
  59. Lebovic DI, Kir M, Casey CL. Peroxisome proliferator-activated receptor-gamma induces regression of endometrial explants in a rat model of endometriosis. Fertil Steril. 2004;82:1008-13. doi: 10.1016/j.fertnstert.2004.02.148. PubMed PMID: 15474065.
  60. Uygur D, Aytan H, Zergeroglu S, Batioglu S. Leflunomide--an immunomodulator--induces regression of endometrial explants in a rat model of endometriosis. J Soc Gynecol Investig. 2006;13:378-83. doi: 10.1016/j.jsgi.2006.03.006. PubMed PMID: 16713311.
  61. Wu LL, Pang RP, Yin YZ, Shen KF, Zhang PZ. Human chorionic gonadotropin improves endometriosis through downregulation of leptin expression in rats. Gynecol Obstet Invest. 2015;79:189-94. doi: 10.1159/000367655. PubMed PMID: 25722014.
  62. Cotroneo MS, Lamartiniere CA. Pharmacologic, but not dietary, genistein supports endometriosis in a rat model. Toxicol Sci. 2001;61:68-75. doi: 10.1093/toxsci/61.1.68. PubMed PMID: 11294976.
  63. Dabrosin C, Gyorffy S, Margetts P, Ross C, Gauldie J. Therapeutic effect of angiostatin gene transfer in a murine model of endometriosis. Am J Pathol. 2002;161:909-18. doi: 10.1016/S0002-9440(10)64251-4. PubMed PMID: 12213719; PubMed Central PMCID: PMCPMC1867254.
  64. Burns KA, Rodriguez KF, Hewitt SC, Janardhan KS, Young SL, Korach KS. Role of estrogen receptor signaling required for endometriosis-like lesion establishment in a mouse model. Endocrinology. 2012;153:3960-71. doi: 10.1210/en.2012-1294. PubMed PMID: 22700766; PubMed Central PMCID: PMCPMC3404357.
  65. Boztosun A, Ozer H, Atilgan R, Acmaz G, Yalta T, Muderris, II, et al. Effect of fibrin glue and comparison with suture on experimental induction of endometriosis in a rat endometrial autograft model. Clin Exp Obstet Gynecol. 2012;39:107-11. PubMed PMID: 22675967.
  66. Han SJ, Jung SY, Wu SP, Hawkins SM, Park MJ, Kyo S, et al. Estrogen Receptor beta Modulates Apoptosis Complexes and the Inflammasome to Drive the Pathogenesis of Endometriosis. Cell. 2015;163:960-74. doi: 10.1016/j.cell.2015.10.034. PubMed PMID: 26544941; PubMed Central PMCID: PMCPMC4640214.
  67. Kim TH, Yu Y, Luo L, Lydon JP, Jeong JW, Kim JJ. Activated AKT pathway promotes establishment of endometriosis. Endocrinology. 2014;155:1921-30. doi: 10.1210/en.2013-1951. PubMed PMID: 24605828; PubMed Central PMCID: PMCPMC3990849.
  68. Huang ZX, Mao XM, Lin DC, Hong YH, Liang GS, Chen QX, et al. Establishment and characterization of immortalized human eutopic endometrial stromal cells. Am J Reprod Immunol. 2020;83:e13213. doi: 10.1111/aji.13213. PubMed PMID: 31802565.
  69. Burns KA, Thomas SY, Hamilton KJ, Young SL, Cook DN, Korach KS. Early Endometriosis in Females Is Directed by Immune-Mediated Estrogen Receptor alpha and IL-6 Cross-Talk. Endocrinology. 2018;159:103-18. doi: 10.1210/en.2017-00562. PubMed PMID: 28927243; PubMed Central PMCID: PMCPMC5761597.
  70. Hayashi S, Nakamura T, Motooka Y, Ito F, Jiang L, Akatsuka S, et al. Novel ovarian endometriosis model causes infertility via iron-mediated oxidative stress in mice. Redox Biol. 2020;37:101726. doi: 10.1016/j.redox.2020.101726. PubMed PMID: 32961443; PubMed Central PMCID: PMCPMC7509075.
  71. Naqvi H, Sakr S, Presti T, Krikun G, Komm B, Taylor HS. Treatment with bazedoxifene and conjugated estrogens results in regression of endometriosis in a murine model. Biol Reprod. 2014;90:121. doi: 10.1095/biolreprod.113.114165. PubMed PMID: 24740602; PubMed Central PMCID: PMCPMC4093999.
  72. Nakamura S, Ochiai K, Ochi A, Ito M, Kamiya T, Yamamoto H. Spontaneous endometriosis in a mandrill (Mandrillus sphinx). J Comp Pathol. 2012;147:386-90. doi: 10.1016/j.jcpa.2012.01.004. PubMed PMID: 22520805.
  73. Assaf BT, Miller AD. Pleural endometriosis in an aged rhesus macaque (Macaca mulatta): a histopathologic and immunohistochemical study. Vet Pathol. 2012;49:636-41. doi: 10.1177/0300985811406890. PubMed PMID: 21521902; PubMed Central PMCID: PMCPMC3597994.
  74. Nair HB, Baker R, Owston MA, Escalona R, Dick EJ, VandeBerg JL, et al. An efficient model of human endometriosis by induced unopposed estrogenicity in baboons. Oncotarget. 2016;7:10857-69. doi: 10.18632/oncotarget.7516. PubMed PMID: 26908459; PubMed Central PMCID: PMCPMC4905444.
  75. D’Hooghe TM, Kyama CM, Chai D, Fassbender A, Vodolazkaia A, Bokor A, et al. Nonhuman primate models for translational research in endometriosis. Reprod Sci. 2009;16:152-61. doi: 10.1177/1933719108322430. PubMed PMID: 19208783.
  76. Ferreira GS, Veening-Griffioen DH, Boon WPC, Moors EHM, van Meer PJK. Levelling the Translational Gap for Animal to Human Efficacy Data. Animals (Basel). 2020;10. doi: 10.3390/ani10071199. PubMed PMID: 32679706; PubMed Central PMCID: PMCPMC7401509.
  77. Denayer T, Stöhr T, Van Roy M. Animal models in translational medicine: Validation and prediction. New Horizons in Translational Medicine. 2014;2:5-11. doi: 10.1016/j.nhtm.2014.08.001.
  78. Sams-Dodd F. Strategies to optimize the validity of disease models in the drug discovery process. Drug Discov Today. 2006;11:355-63. doi: 10.1016/j.drudis.2006.02.005. PubMed PMID: 16580978.
  79. Vargas E, Aghajanova L, Gemzell-Danielsson K, Altmae S, Esteban FJ. Cross-disorder analysis of endometriosis and its comorbid diseases reveals shared genes and molecular pathways and proposes putative biomarkers of endometriosis. Reprod Biomed Online. 2020;40:305-18. doi: 10.1016/j.rbmo.2019.11.003. PubMed PMID: 31926826.
  80. Jones RC. The effect of a luteinizing hormone-releasing hormone antagonist on experimental endometriosis in the rat. Acta Endocrinol (Copenh). 1987;114:379-82. doi: 10.1530/acta.0.1140379. PubMed PMID: 3551430.
  81. Mishra A, Galvankar M, Vaidya S, Chaudhari U, Modi D. Mouse model for endometriosis is characterized by proliferation and inflammation but not epithelial-to-mesenchymal transition and fibrosis. J Biosci. 2020;45. PubMed PMID: 32975232.
  82. Nishimoto-Kakiuchi A, Netsu S, Okabayashi S, Taniguchi K, Tanimura H, Kato A, et al. Spontaneous endometriosis in cynomolgus monkeys as a clinically relevant experimental model. Hum Reprod. 2018;33:1228-36. doi: 10.1093/humrep/dey095. PubMed PMID: 29684118; PubMed Central PMCID: PMCPMC6012197.
  83. Persoons E, De Clercq K, Van den Eynde C, Pinto S, Luyten K, Van Bree R, et al. Mimicking Sampson’s Retrograde Menstrual Theory in Rats: A New Rat Model for Ongoing Endometriosis-Associated Pain. Int J Mol Sci. 2020;21. doi: 10.3390/ijms21072326. PubMed PMID: 32230898; PubMed Central PMCID: PMCPMC7177935.
  84. Konno R, Fujiwara H, Netsu S, Odagiri K, Shimane M, Nomura H, et al. Gene expression profiling of the rat endometriosis model. Am J Reprod Immunol. 2007;58:330-43. doi: 10.1111/j.1600-0897.2007.00507.x. PubMed PMID: 17845203.
  85. Cosar E, Mamillapalli R, Moridi I, Duleba A, Taylor HS. Serum MicroRNA Biomarkers Regulated by Simvastatin in a Primate Model of Endometriosis. Reprod Sci. 2019;26:1343-50. doi: 10.1177/1933719118765971. PubMed PMID: 29587611; PubMed Central PMCID: PMCPMC6949973.
  86. Kim YS, Kim YJ, Kim MJ, Lee SJ, Kwon H, Lee JH. Novel Medicine for Endometriosis and Its Therapeutic Effect in a Mouse Model. Biomedicines. 2020;8. doi: 10.3390/biomedicines8120619. PubMed PMID: 33339236; PubMed Central PMCID: PMCPMC7766695.
  87. Ma Y, He YL. Study of an antiangiogenesis gene therapy with endostatin on endometriosis in the nude mouse model. Clin Exp Obstet Gynecol. 2014;41:328-34. PubMed PMID: 24992787.
  88. Gupta D, Hull ML, Fraser I, Miller L, Bossuyt PM, Johnson N, et al. Endometrial biomarkers for the non-invasive diagnosis of endometriosis. Cochrane Database Syst Rev. 2016;4:CD012165. doi: 10.1002/14651858.CD012165. PubMed PMID: 27094925; PubMed Central PMCID: PMCPMC6953323
  89. Nisenblat V, Bossuyt PM, Shaikh R, Farquhar C, Jordan V, Scheffers CS, et al. Blood biomarkers for the non-invasive diagnosis of endometriosis. Cochrane Database Syst Rev. 2016;2016:CD012179. doi: 10.1002/14651858.CD012179. PubMed PMID: 27132058; PubMed Central PMCID: PMCPMC7076288.
Iranian Journal of Medical Sciences

Articles InPress, Corrected Proof
Available Online from 14 September 2025
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  • Received: 05 February 2025
  • Revised: 29 March 2025
  • Accepted: 18 April 2025
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