Volume 16, Issue 5 (May 2018)                   IJRM 2018, 16(5): 305-314 | Back to browse issues page

XML Persian Abstract Print

Download citation:
BibTeX | RIS | EndNote | Medlars | ProCite | Reference Manager | RefWorks
Send citation to:
Kiani K, Movahedin M, Malekafzali H, Mirfasihi F, Sadati S N, Moini A, et al . Effect of the estrus cycle stage on the establishment of murine endometriosis lesions. IJRM 2018; 16 (5) :305-314
URL: http://ijrm.ir/article-1-1106-en.html
Effect of the estrus cycle stage on the establishment of murine endometriosis lesions
Kiandokht Kiani1 , Mansoureh Movahedin * 2, Hossein Malekafzali3 , Faramarz Mirfasihi4 , Seyedeh Nargess Sadati5 , Ashraf Moini6 , Seyed Nasser Ostad7 , Reza Aflatoonian8
1- Valiasr Reproductive Health Research Center, Tehran University of Medical Sciences, Tehran, Iran
2- Department of Anatomical Sciences, Faculty of Medical Sciences, Tarbiat Modares University, Tehran, Iran. , movahed.m@modares.ac.ir
3- Department of Epidemiology and Biostatistics, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran
4- Department of Pathology, Massoud Clinical Laboratory, Tehran, Iran
5- Department of Traditional Pharmacy, School of Traditional Medicine, Tehran University of Medical Sciences, Tehran, Iran
6- Department of Obstetrics and Gynecology, School of Medicine, Tehran University of Medical Sciences, Tehran, Iran
7- Department of Toxicology and Pharmacology, School of Pharmacy, Tehran University of Medical Sciences, Tehran, Iran
8- Department of Endocrinology and Female Infertility, Reproductive Biomedicine Research Center, Royan Institute for Reproductive Biomedicine, ACECR, Tehran, Iran
Abstract:   (3269 Views)
Background: Establishment of a standardized animal endometriosis model is necessary for evaluation of new drug effects and for explaining different ethological aspects of this disease. For this purpose, we need a model which has more similarity to human endometriosis.
Objective: Our objective was to establish an autologous endometriosis mouse model based on endogenous estrogen level and analyze the influence of estrus cycle on the maintenance of endometriotic lesions.
Materials and Methods: In this experimental study, endometriotic lesions were induced in 52 female NMRI mice by suturing uterine tissue samples to the abdominal wall. The transplantation was either performed at proestrus/estrus or at metestrus/diestrus cycles. Urine-soaked beddings from males and also male vasectomized mice were transferred to the cages to synchronize and maintenance of estrus cycle in female mice. The mice were sacrificed after different transplantation periods (2, 4, 6 or 8 wk). The lesions size, macroscopic growth, model success rate, histological and immune-histochemical analyses were assessed at the end.
Results: From a total of 200 tissue samples sutured into the peritoneal cavity, 83 endometriotic lesions were confirmed by histopathology (41.5%). Model success rate for proestrus/estrus mice was 60.7% vs. 79.2% for metestrus/diestrus mice. The endometriotic lesions had similar growth in both groups. Number of caspase-3, Ki67-positive cells and CD31-positive micro vessels were also similar in endometriotic lesions of two groups.
Conclusion: If we maintain the endogenous estrogen levels in mice, we can induce endometriosis mouse model in both proestrus/estrus and metestrus/diestrus cycle without any significant difference.
Keywords: Endometriosis, Animal models, Transplantation, Autologous, Estrus cycle.
Full-Text [PDF 664 kb]   (743 Downloads) |   |   Full-Text (HTML)  (1200 Views)  
Type of Study: Original Article |
References
1. 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.
2. Grummer R. Animal models in endometriosis research. Hum Reprod Update 2006; 12: 641-649. [DOI:10.1093/humupd/dml026]
3. Story L, Kennedy S. Animal studies in endometriosis: a review. ILAR J 2004; 45: 132-138. [DOI:10.1093/ilar.45.2.132]
4. do Amaral VF, Dal Lago EA, Kondo W, Souza LC, Francisco JC. Development of an experimental model of endometriosis in rats. Rev Col Bras Cir 2009; 36: 250-255. [DOI:10.1590/S0100-69912009000300012]
5. 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]
6. Vernon MW, Wilson EA. Studies on the surgical induction of endometriosis in the rat. Fertil Steril 1985; 44: 684-694. [DOI:10.1016/S0015-0282(16)48988-0]
7. Körbel 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: 2551-2558. [DOI:10.1093/humrep/deq201]
8. 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: 2092-2096. [DOI:10.1093/humrep/dei012]
9. The Academy of Medical Sciences. Animals containing human material. London, The Academy of Medical Sciences; 2011.
10. Mihalyi A, Simsa P, Mutinda KC, Meuleman C, Mwenda JM, D'Hooghe TM. Emerging drugs in endometriosis. Exp Opin Emerg Drugs 2006; 11: 503-524. [DOI:10.1517/14728214.11.3.503]
11. Rudzitis-Auth J, Körbel C, Scheuer C, Menger MD, Laschke MW. Xanthohumol inhibits growth and vascularization of developing endometriotic lesions. Hum Reprod 2012; 27: 1735-1744. [DOI:10.1093/humrep/des095]
12. Laschke MW, Schwender C, Scheuer C, Vollmar B, Menger MD. Epigallocatechin-3-gallate inhibits estrogen-induced activation of endometrial cells in vitro and causes regression of endometriotic lesions in vivo. Hum Reprod 2008; 23: 2308-2318. [DOI:10.1093/humrep/den245]
13. Santmyire BR, Venkat V, Beinder E, Baylis C. Impact of the estrus cycle and reduction in estrogen levels with aromatase inhibition, on renal function and nitric oxide activity in female rats. Steroids 2010; 75: 1011-1015. [DOI:10.1016/j.steroids.2010.06.016]
14. Uchida M, Kobayashi O. Sequential observation of implanted endometriosis by laparoscopy in rats: correlation between the prevalence rate and the estrous cycle. J Pharmacol Sci 2013; 121: 299-304. [DOI:10.1254/jphs.12180FP]
15. Laschke MW, Körbel C, Rudzitis-Auth J, Gashaw I, Reinhardt M, Hauff P, et al. High-resolution ultrasound imaging: a novel technique for the noninvasive in vivo analysis of endometriotic lesion and cyst formation in small animal models. Am J Pathol 2010; 176: 585-593. [DOI:10.2353/ajpath.2010.090617]
16. Ergenoğlu AM, Yeniel AÖ, Erbaş O, Aktuğ H, Yildirim N, Ulukuş M, et al. Regression of endometrial implants by resveratrol in an experimentally induced endometriosis model in rats. Reprod Sci 2013; 20: 1230-1236. [DOI:10.1177/1933719113483014]
17. Güney M, Nasir S, Oral B, Karahan N, Mungan T. Effect of caffeic acid phenethyl ester on the regression of endometrial explants in an experimental rat model. Reprod Sci 2007; 14: 270-279. [DOI:10.1177/1933719107300911]
18. Nogueira Neto J, Coelho TM, Aguiar GC, Carvalho LR, de Araújo AG, Girão MJ, et al. Experimental endometriosis reduction in rats treated with Uncaria tomentosa (cat's claw) extract. Eur J Obstet Gynecol Reprod Biol 2011; 154: 205-208. [DOI:10.1016/j.ejogrb.2010.10.002]
19. Peterse DP, Fassbender A, O DF, Vanhie A, Saunders P, Vriens J, et al. Laparoscopic surgery: a new technique to induce endometriosis in a mouse model. Reprod Sci 2016; 23: 1332-1339. [DOI:10.1177/1933719116638178]
20. McGrath JC, Drummond GB, McLachlan EM, Kilkenny C, Wainwright CL. Guidelines for reporting experiments involving animals: the ARRIVE guidelines. Br J Pharmacol 2010; 160: 1573-1576. [DOI:10.1111/j.1476-5381.2010.00873.x]
21. Whitten WK. Modification of the oestrous cycle of the mouse by external stimuli associated with the male;changes in the oestrous cycle determined by vaginal smears. J Endocrinol 1958; 17: 307-313. [DOI:10.1677/joe.0.0170307]
22. McLean AC, Valenzuela N, Fai S, Bennett SA. Performing vaginal lavage, crystal violet staining, and vaginal cytological evaluation for mouse estrous cycle staging identification. J Vis Exp 2012; 67: e4389. [DOI:10.3791/4389]
23. Ricci AG, Olivares CN, Bilotas MA, Bastón JI, Singla JJ, Meresman GF, et al. Natural therapies assessment for the treatment of endometriosis. Hum Reprod 2013; 28: 178-188. [DOI:10.1093/humrep/des369]
24. Quereda F, Barroso J, Acien P. Individual and combined effects of triptoreline and gestrinone on experimental endometriosis in rats. Eur J Obstet Gynecol Reprod Biol 1996; 67: 35-40. [DOI:10.1016/0301-2115(96)02435-9]
25. Keenan JA, Williams-Boyce PK, Massey PJ, Chen TT, Caudle MR, Bukovsky A. Regression of endometrial explants in a rat model of endometriosis treated with the immune modulators loxoribine and levamisole. Fertil Steril 1999; 72: 135-141. [DOI:10.1016/S0015-0282(99)00157-0]
26. Wood GA, Fata JE, Watson KL, Khokha R. Circulating hormones and estrous stage predict cellular and stromal remodeling in murine uterus. Reproduction 2007; 133: 1035-1044. [DOI:10.1530/REP-06-0302]
27. Hawkins SM, Matzuk MM. The menstrual cycle: basic biology. Ann N Y Acad Sci 2008; 1135: 10-18. [DOI:10.1196/annals.1429.018]
28. Mihm M, Gangooly S, Muttukrishna S. The normal menstrual cycle in women. Anim Reprod Sci 2011; 124: 229-236. [DOI:10.1016/j.anireprosci.2010.08.030]
29. Sander VA, Facorro GB, Piehl L, Rubín de Celis E, Motta AB. Effect of DHEA and metformin on corpus luteum in mice. Reproduction 2009; 138: 571-579. [DOI:10.1530/REP-08-0325]
30. Rudolph M, Döcke WD, Müller A, Menning A, Röse L, Zollner TM, et al. Induction of overt menstruation in intact mice. PLoS One 2012; 7: e32922. [DOI:10.1371/journal.pone.0032922]
31. Harirchian P, Gashaw I, Lipskind ST, Braundmeier AG, Hastings JM, Olson MR, et al. Lesion kinetics in a non-human primate model of endometriosis. Hum Reprod 2012; 27: 2341-2351. [DOI:10.1093/humrep/des196]
32. Cason AM, Samuelsen CL, Berkley KJ. Estrous changes in vaginal nociception in a rat model of endometriosis. Horm Behav 2003; 44: 123-131. [DOI:10.1016/S0018-506X(03)00121-1]
33. Bourlev V, Volkov N, Pavlovitch S, Lets N, Larsson A, Olovsson M. The relationship between microvessel density, proliferative activity and expression of vascular endothelial growth factor-A and its receptors in eutopic endometrium and endometriotic lesions. Reproduction 2006; 132: 501-509. [DOI:10.1530/rep.1.01110]
34. Pellegrini C, Gori I, Achtari C, Hornung D, Chardonnens E, Wunder D, 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: 1200-1208. [DOI:10.1016/j.fertnstert.2012.06.056]
35. Salmassi A, Acar-Perk B, Schmutzler AG, Koch K, Püngel F, Jonat W, et al. Apoptosis resistance in endometriosis. Bioimpacts 2011; 1: 129-134.
36. Rocha AL, Reis FM, Taylor RN. Angiogenesis and endometriosis. Obstet Gynecol Int 2013; 2013: 1-8. [DOI:10.1155/2013/859619]
37. Hsiao KY, Chang N, Lin SC, Li YH, Wu MH. Inhibition of dual specificity phosphatase-2 by hypoxia promotes interleukin-8-mediated angiogenesis in endometriosis. Hum Reprod 2014; 29: 2747-2755. [DOI:10.1093/humrep/deu255]
38. Nothnick WB, Graham A, Holbert J, Weiss MJ. miR-451 deficiency is associated with altered endometrial fibrinogen alpha chain expression and reduced endometriotic implant establishment in an experimental mouse model. PloS One 2014; 9: 1-11 [DOI:10.1371/journal.pone.0100336]
Send email to the article author

Rights and permissions
Creative Commons License This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

Designed & Developed by : Yektaweb