In‑vitro models of human endometriosis (Review)
- Authors:
- Hongjie Fan
-
Affiliations: The Obstetrics and Gynecology Hospital of Fudan University, Shanghai 200011, P.R. China - Published online on: December 20, 2019 https://doi.org/10.3892/etm.2019.8363
- Pages: 1617-1625
-
Copyright: © Fan . This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
Kuznetsov L, Dworzynski K, Davies M and Overton C; Guideline Committee, : Diagnosis and management of endometriosis: Summary of NICE guidance. BMJ. 358:j39352017. View Article : Google Scholar : PubMed/NCBI | |
Dunselman GA, Vermeulen N, Becker C, Calhaz-Jorge C, D'Hooghe T, De Bie B, Heikinheimo O, Horne AW, Kiesel L, Nap A, et al: ESHRE guideline: Management of women with endometriosis. Hum Reprod. 29:400–412. 2014. View Article : Google Scholar : PubMed/NCBI | |
Guo SW: Recurrence of endometriosis and its control. Hum Reprod Update. 15:441–461. 2009. View Article : Google Scholar : PubMed/NCBI | |
Halme J, Hammond MG, Hulka JF, Raj SG and Talbert LM: Retrograde menstruation in healthy women and in patients with endometriosis. Obstet Gynecol. 64:151–154. 1984.PubMed/NCBI | |
Bruner-Tran KL, Mokshagundam S, Herington JL, Ding T and Osteen KG: Rodent models of experimental endometriosis: Identifying mechanisms of disease and therapeutic targets. Curr Womens Health Rev. 14:173–188. 2018. View Article : Google Scholar : PubMed/NCBI | |
King CM, Barbara C, Prentice A, Brenton JD and Charnock-Jones DS: Models of endometriosis and their utility in studying progression to ovarian clear cell carcinoma. J Pathol. 238:185–196. 2016. View Article : Google Scholar : PubMed/NCBI | |
Banu SK, Lee J, Starzinski-Powitz A and Arosh JA: Gene expression profiles and functional characterization of human immortalized endometriotic epithelial and stromal cells. Fertil Steril. 90:972–987. 2008. View Article : Google Scholar : PubMed/NCBI | |
Lee J, Banu SK, Rodriguez R, Starzinski-Powitz A and Arosh JA: Selective blockade of prostaglandin E2 receptors EP2 and EP4 signaling inhibits proliferation of human endometriotic epithelial cells and stromal cells through distinct cell cycle arrest. Fertil Steril. 93:2498–2506. 2010. View Article : Google Scholar : PubMed/NCBI | |
Köster F, Jin L, Shen Y, Schally AV, Cai RZ, Block NL, Hornung D, Marschner G, Rody A, Engel JB and Finas D: Effects of an antagonistic analog of growth hormone-releasing hormone on endometriosis in a mouse model and in vitro. Reprod Sci. 24:1503–1511. 2017. View Article : Google Scholar : PubMed/NCBI | |
Adammek M, Greve B, Kassens N, Schneider C, Brüggemann K, Schüring AN, Starzinski-Powitz A, Kiesel L and Götte M: MicroRNA miR-145 inhibits proliferation, invasiveness, and stem cell phenotype of an in vitro endometriosis model by targeting multiple cytoskeletal elements and pluripotency factors. Fertil Steril. 99:1346–1355.e5. 2013. View Article : Google Scholar : PubMed/NCBI | |
Králíčková M, Fiala L, Losan P, Tomes P and Vetvicka V: Altered immunity in endometriosis: What came first? Immunol Invest. 47:569–582. 2018. View Article : Google Scholar : PubMed/NCBI | |
Miller JE, Monsanto SP, Ahn SH, Khalaj K, Fazleabas AT, Young SL, Lessey BA, Koti M and Tayade C: Interleukin-33 modulates inflammation in endometriosis. Sci Rep. 7:179032017. View Article : Google Scholar : PubMed/NCBI | |
Ruiz A, Ruiz L, Colòn-Caraballo M, Torres-Collazo BJ, Monteiro JB, Bayona M, Fazleabas AT and Flores I: Pharmacological blockage of the CXCR4-CXCL12 axis in endometriosis leads to contrasting effects in proliferation, migration, and invasion. Biol Reprod. 98:4–14. 2018. View Article : Google Scholar : PubMed/NCBI | |
Brueggmann D, Templeman C, Starzinski-Powitz A, Rao NP, Gayther SA and Lawrenson K: Novel three-dimensional in vitro models of ovarian endometriosis. J Ovarian Res. 7:172014. View Article : Google Scholar : PubMed/NCBI | |
Ryan IP, Schriock ED and Taylor RN: Isolation, characterization, and comparison of human endometrial and endometriosis cells in vitro. J Clin Endocrinol Metab. 78:642–649. 1994. View Article : Google Scholar : PubMed/NCBI | |
Boccellino M, Quagliuolo L, Verde A, La Porta R, Crispi S, Piccolo MT, Vitiello A, Baldi A and Signorile PG: In vitro model of stromal and epithelial immortalized endometriotic cells. J Cell Biochem. 113:1292–1301. 2012. View Article : Google Scholar : PubMed/NCBI | |
Liu J, Zhang Z, Liu J and Wang D: LIM Kinase 1 mediates estradiol effects on the phosphorylation of Cofilin1 in eutopic endometrial stromal cells during the invasion and proliferation of endometriosis. Reprod Sci. 26:1499–1505. 2019. View Article : Google Scholar : PubMed/NCBI | |
Olivares C, Bilotas M, Buquet R, Borghi M, Sueldo C, Tesone M and Meresman G: Effects of a selective cyclooxygenase-2 inhibitor on endometrial epithelial cells from patients with endometriosis. Hum Reprod. 23:2701–2708. 2008. View Article : Google Scholar : PubMed/NCBI | |
Matsuzaki S, Canis M, Pouly JL and Darcha C: Soft matrices inhibit cell proliferation and inactivate the fibrotic phenotype of deep endometriotic stromal cells in vitro. Hum Reprod. 31:541–553. 2016. View Article : Google Scholar : PubMed/NCBI | |
Matsuzaki S and Darcha C: Co-operation between the AKT and ERK signaling pathways may support growth of deep endometriosis in a fibrotic microenvironment in vitro. Hum Reprod. 30:1606–1616. 2015. View Article : Google Scholar : PubMed/NCBI | |
Overton CE, Fernandez-Shaw S, Hicks B, Barlow DH and Starkey P: In vitro culture of endometrial stromal and gland cells as a model for endometriosis: The effect of peritoneal fluid on proliferation. Fertil Steril. 67:51–56. 1997. View Article : Google Scholar : PubMed/NCBI | |
Braza-Boïls A, Salloum-Asfar S, Marí-Alexandre J, Arroyo AB, González-Conejero R, Barcelo-Mólina M, García-Oms J, Vicente V, Estelles A, Gilabert-Estelles J and Martínez C: Peritoneal fluid modifies the microRNA expression profile in endometrial and endometriotic cells from women with endometriosis. Hum Reprod. 30:2292–2302. 2015. View Article : Google Scholar : PubMed/NCBI | |
Braza-Boïls A, Gilabert-Estélles J, Ramon LA, Gilabert J, Marí-Alexandre J, Chirivella M, Espana F and Estelles A: Peritoneal fluid reduces angiogenesis-related microRNA expression in cell cultures of endometrial and endometriotic tissues from women with endometriosis. PLoS One. 8:e623702013. View Article : Google Scholar : PubMed/NCBI | |
Surrey ES and Halme J: Effect of platelet-derived growth factor on endometrial stromal cell proliferation in vitro: A model for endometriosis? Fertil Steril. 56:672–679. 1991. View Article : Google Scholar : PubMed/NCBI | |
Liang Z, Chen Y, Zhao Y, Xu C, Zhang A, Zhang Q, Wang D, He J, Hua W and Duan P: miR-200c suppresses endometriosis by targeting MALAT1 in vitro and in vivo. Stem Cell Res Ther. 8:2512017. View Article : Google Scholar : PubMed/NCBI | |
Matsuzaki S and Darcha C: Antifibrotic properties of epigallocatechin-3-gallate in endometriosis. Hum Reprod. 29:1677–1687. 2014. View Article : Google Scholar : PubMed/NCBI | |
Kim SH, Cho S, Ihm HJ, Oh YS, Heo SH, Chun S, Im H, Chae HD, Kim CH and Kang BM: Possible role of phthalate in the pathogenesis of endometriosis: In vitro, animal, and human data. J Clin Endocrinol Metab. 100:E1502–E1511. 2015. View Article : Google Scholar : PubMed/NCBI | |
Matsuzaki S and Darcha C: Involvement of the Wnt/β-catenin signaling pathway in the cellular and molecular mechanisms of fibrosis in endometriosis. PLoS One. 8:e768082013. View Article : Google Scholar : PubMed/NCBI | |
Laschke MW and Menger MD: In vitro and in vivo approaches to study angiogenesis in the pathophysiology and therapy of endometriosis. Hum Reprod Update. 13:331–342. 2007. View Article : Google Scholar : PubMed/NCBI | |
Fujimoto J, Sakaguchi H, Hirose R and Tamaya T: Expression of platelet-derived endothelial cell growth factor (PD-ECGF) related to angiogenesis in ovarian endometriosis. J Clin Endocrinol Metab. 84:359–362. 1999. View Article : Google Scholar : PubMed/NCBI | |
Gazvani R, Smith L and Fowler PA: Effect of interleukin-8 (IL-8), anti-IL-8, and IL-12 on endometrial cell survival in combined endometrial gland and stromal cell cultures derived from women with and without endometriosis. Fertil Steril. 77:62–67. 2002. View Article : Google Scholar : PubMed/NCBI | |
Lv J, Zhu Q, Jia X, Yu N and Li Q: In vitro and in vivo effects of tumor suppressor gene PTEN on endometriosis: An experimental study. Med Sci Monit. 22:3727–3736. 2016. View Article : Google Scholar : PubMed/NCBI | |
Wang Y, Nicholes K and Shih IM: The origin and pathogenesis of endometriosis. Annu Rev Pathol. Sep 3–2019.(Epub ahead of print). PubMed/NCBI | |
Savilova AM, Yushina MN, Rudimova YV, Khabas GN, Chuprynin VD and Sukhikh GT: Characteristics of multipotent mesenchymal stromal cells isolated from human endometrium and endometriosis lesions. Bull Exp Biol Med. 161:610–615. 2016. View Article : Google Scholar : PubMed/NCBI | |
Savilova AM, Farkhat KN, Yushina MN, Rudimova YV, Makiyan ZN and Adamyan LV: Characteristics of multipotent mesenchymal stromal cells isolated from the endometrium and endometriosis lesions of women with malformations of the internal reproductive organs. Bull Exp Biol Med. 162:539–544. 2017. View Article : Google Scholar : PubMed/NCBI | |
Kao AP, Wang KH, Long CY, Chai CY, Tsai CF, Hsieh TH, Hsu CY, Chang CC, Lee JN and Tsai EM: Interleukin-1β induces cyclooxygenase-2 expression and promotes the invasive ability of human mesenchymal stem cells derived from ovarian endometrioma. Fertil Steril. 96:678–684 e671. 2011. View Article : Google Scholar : PubMed/NCBI | |
Canosa S, Moggio A, Brossa A, Pittatore G, Marchino GL, Leoncini S, Benedetto C, Revelli A and Bussolati B: Angiogenic properties of endometrial mesenchymal stromal cells in endothelial co-culture: An in vitro model of endometriosis. Mol Hum Reprod. 23:187–198. 2017.PubMed/NCBI | |
Hapangama DK, Drury J, Da Silva L, Al-Lamee H, Earp A, Valentijn AJ, Edirisinghe DP, Murray PA, Fazleabas AT and Gargett CE: Abnormally located SSEA1+/SOX9+ endometrial epithelial cells with a basalis-like phenotype in the eutopic functionalis layer may play a role in the pathogenesis of endometriosis. Hum Reprod. 34:56–68. 2019. View Article : Google Scholar : PubMed/NCBI | |
Esfandiari N, Nazemian Z and Casper RF: Three-dimensional culture of endometrial cells: An in vitro model of endometriosis. Am J Reprod Immunol. 60:283–289. 2008. View Article : Google Scholar : PubMed/NCBI | |
Fasciani A, Bocci G, Xu J, Bielecki R, Greenblatt E, Leyland N and Casper RF: Three-dimensional in vitro culture of endometrial explants mimics the early stages of endometriosis. Fertil Steril. 80:1137–1143. 2003. View Article : Google Scholar : PubMed/NCBI | |
Prechapanich J, Kajihara T, Fujita K, Sato K, Uchino S, Tanaka K, Matsumoto S, Akita M, Nagashima M, Brosens JJ and Ishihara O: Effect of a dienogest for an experimental three-dimensional endometrial culture model for endometriosis. Med Mol Morphol. 47:189–195. 2014. View Article : Google Scholar : PubMed/NCBI | |
Esfandiari N, Ai J, Nazemian Z, Javed MH, Gotlieb L and Casper RF: Expression of glycodelin and cyclooxygenase-2 in human endometrial tissue following three-dimensional culture. Am J Reprod Immunol. 57:49–54. 2007. View Article : Google Scholar : PubMed/NCBI | |
Esfandiari N, Khazaei M, Ai J, Bielecki R, Gotlieb L, Ryan E and Casper RF: Effect of a statin on an in vitro model of endometriosis. Fertil Steril. 87:257–262. 2007. View Article : Google Scholar : PubMed/NCBI | |
Maas JW, Le Noble FA, Dunselman GA, de Goeij AF, Struyker Boudier HA and Evers JL: The chick embryo chorioallantoic membrane as a model to investigate the angiogenic properties of human endometrium. Gynecol Obstet Invest. 48:108–112. 1999. View Article : Google Scholar : PubMed/NCBI | |
Nap AW, Groothuis PG, Demir AY, Maas JW, Dunselman GA, de Goeij AF and Evers JL: Tissue integrity is essential for ectopic implantation of human endometrium in the chicken chorioallantoic membrane. Hum Reprod. 18:30–34. 2003. View Article : Google Scholar : PubMed/NCBI | |
Nap AW, Groothuis PG, Punyadeera C, Klein-Hitpass L, Kamps R, Delvoux B and Dunselman GA: Oral contraceptives prevent the development of endometriosis in the chicken chorioallantoic membrane model. Contraception. 78:257–265. 2008. View Article : Google Scholar : PubMed/NCBI | |
Nap AW, Dunselman GA, Griffioen AW, Mayo KH, Evers JL and Groothuis PG: Angiostatic agents prevent the development of endometriosis-like lesions in the chicken chorioallantoic membrane. Fertil Steril. 83:793–795. 2005. View Article : Google Scholar : PubMed/NCBI | |
Koks CA, Groothuis PG, Dunselman GA, de Goeij AF and Evers JL: Adhesion of shed menstrual tissue in an in-vitro model using amnion and peritoneum: A light and electron microscopic study. Hum Reprod. 14:816–1822. 1999. View Article : Google Scholar : PubMed/NCBI | |
van der Linden PJ, de Goeij AF, Dunselman GA, Erkens HW and Evers JL: Amniotic membrane as an in vitro model for endometrium-extracellular matrix interactions. Gynecol Obstet Invest. 45:7–11. 1998. View Article : Google Scholar : PubMed/NCBI | |
Groothuis PG, Koks CA, de Goeij AF, Dunselman GA, Arends JW and Evers JL: Adhesion of human endometrium to the epithelial lining and extracellular matrix of amnion in vitro: An electron microscopic study. Hum Reprod. 13:2275–2281. 1998. View Article : Google Scholar : PubMed/NCBI | |
van der Linden PJ, de Goeij AF, Dunselman GA, Erkens HW and Evers JL: Endometrial cell adhesion in an in vitro model using intact amniotic membranes. Fertil Steril. 65:76–80. 1996. View Article : Google Scholar : PubMed/NCBI | |
Witz CA, Dechaud H, Montoya-Rodriguez IA, Thomas MR, Nair AS, Centonze VE and Schenken RS: An in vitro model to study the pathogenesis of the early endometriosis lesion. Ann N Y Acad Sci. 955:296–307, 340–342, 396–406. 2002. View Article : Google Scholar : PubMed/NCBI | |
Witz CA, Monotoya-Rodriguez IA and Schenken RS: Whole explants of peritoneum and endometrium: A novel model of the early endometriosis lesion. Fertil Steril. 71:56–60. 1999. View Article : Google Scholar : PubMed/NCBI | |
Groothuis PG, Koks CA, de Goeij AF, Dunselman GA, Arends JW and Evers JL: Adhesion of human endometrial fragments to peritoneum in vitro. Fertil Steril. 71:1119–1124. 1999. View Article : Google Scholar : PubMed/NCBI | |
Wild RA, Zhang RJ and Medders D: Whole endometrial fragments form characteristics of in vivo endometriosis in a mesothelial cell co-culture system: An in vitro model for the study of the histogenesis of endometriosis. J Soc Gynecol Investig. 1:65–68. 1994. View Article : Google Scholar : PubMed/NCBI | |
Lucidi RS, Witz CA, Chrisco M, Binkley PA, Shain SA and Schenken RS: A novel in vitro model of the early endometriotic lesion demonstrates that attachment of endometrial cells to mesothelial cells is dependent on the source of endometrial cells. Fertil Steril. 84:16–21. 2005. View Article : Google Scholar : PubMed/NCBI | |
Debrock S, De Strooper B, Vander Perre S, Hill JA and D'Hooghe TM: Tumour necrosis factor-alpha, interleukin-6 and interleukin-8 do not promote adhesion of human endometrial epithelial cells to mesothelial cells in a quantitative in vitro model. Hum Reprod. 21:605–609. 2006. View Article : Google Scholar : PubMed/NCBI | |
Griffith JS, Binkley PA, Kirma NB, Schenken RS, Witz CA and Tekmal RR: Imatinib decreases endometrial stromal cell transmesothial migration and proliferation in the extracellular matrix of modeled peritoneum. Fertil Steril. 94:2531–2535. 2010. View Article : Google Scholar : PubMed/NCBI | |
Nair AS, Nair HB, Lucidi RS, Kirchner AJ, Schenken RS, Tekmal RR and Witz CA: Modeling the early endometriotic lesion: Mesothelium-endometrial cell co-culture increases endometrial invasion and alters mesothelial and endometrial gene transcription. Fertil Steril. 90:1487–1495. 2008. View Article : Google Scholar : PubMed/NCBI | |
Chen Z, Dai Y, Dong Z, Li M, Mu X, Zhang R, Wang Z, Zhang W, Lang J, Leng J and Jiang X: Co-cultured endometrial stromal cells and peritoneal mesothelial cells for an in vitro model of endometriosis. Integr Biol (Camb). 4:1090–1095. 2012. View Article : Google Scholar : PubMed/NCBI | |
Yu J, Wang Y, Zhou WH, Wang L, He YY and Li DJ: Combination of estrogen and dioxin is involved in the pathogenesis of endometriosis by promoting chemokine secretion and invasion of endometrial stromal cells. Hum Reprod. 23:1614–1626. 2008. View Article : Google Scholar : PubMed/NCBI | |
Loh FH, Bongso A, Fong CY, Koh DR, Lee SH and Zhao HQ: Effects of peritoneal macrophages from women with endometriosis on endometrial cellular proliferation in an in vitro coculture model. Fertil Steril. 72:533–538. 1999. View Article : Google Scholar : PubMed/NCBI | |
Takaoka O, Mori T, Ito F, Okimura H, Kataoka H, Tanaka Y, Koshiba A, Kusuki I, Shigehiro S, Amami T and Kitawaki J: Daidzein-rich isoflavone aglycones inhibit cell growth and inflammation in endometriosis. J Steroid Biochem Mol Biol. 181:125–132. 2018. View Article : Google Scholar : PubMed/NCBI | |
Wu D, Lu P, Mi X and Miao J: Exosomal miR-214 from endometrial stromal cells inhibits endometriosis fibrosis. Mol Hum Reprod. 24:357–365. 2018.PubMed/NCBI | |
Lawrenson K, Lee N, Torres HA, Lee JM, Brueggmann D, Rao PN, Noushmehr H and Gayther SA: Src as a novel therapeutic target for endometriosis. Gynecol Oncol. 135:100–107. 2014. View Article : Google Scholar : PubMed/NCBI | |
Ohtake H, Katabuchi H, Matsuura K and Okamura H: A novel in vitro experimental model for ovarian endometriosis: The three-dimensional culture of human ovarian surface epithelial cells in collagen gels. Fertil Steril. 71:50–55. 1999. View Article : Google Scholar : PubMed/NCBI | |
Vigano P, Candiani M, Monno A, Giacomini E, Vercellini P and Somigliana E: Time to redefine endometriosis including its pro-fibrotic nature. Hum Reprod. 33:347–352. 2018. View Article : Google Scholar : PubMed/NCBI | |
Zhang Q, Duan J, Liu X and Guo SW: Platelets drive smooth muscle metaplasia and fibrogenesis in endometriosis through epithelial-mesenchymal transition and fibroblast-to-myofibroblast transdifferentiation. Mol Cell Endocrinol. 428:1–16. 2016. View Article : Google Scholar : PubMed/NCBI |