ENDOMETRIAL MOLECULAR BIOLOGICAL CHANGES IN WOMEN WITH EXTERNAL GENITAL ENDOMETRIOSIS


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Abstract

Objective. To carry out a systematic analysis of the data available in modern literature on molecular changes in the eutopic endometrium of women with external genital endometriosis. Materials and methods. The review included the data of foreign and Russian papers published in 2011-2016 and found in Pubmed on this topic. These papers were the basis for this review; however, for a better understanding of the topic, we expanded searches and included older, but widely quoted articles. Results. This review describes the basic theories of the pathogenesis of endometriosis, which are known at the moment. There is an update on differences in the eutopic endometrium of healthy women and in that of women with endometriosis and endometrioid heterotopias, which include changes in the expression of the factors of adhesion, invasion, angiogenesis, morphogenesis, receptivity, and oncogenesis, as well as hormonal and immune factors. Conclusion. The established differences in the endometrium of healthy women and in that of women with endometriosis and endometrioid heterotopias can not only expand knowledge of the pathogenesis of endometriosis, but also prove to be important therapeutic targets for its treatment. The findings may be also useful in the early diagnosis and prediction of genital endometriosis.

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About the authors

Ekaterina Yuryevna Tikhonchuk

Email: best-kauty@mail.ru
PhD student, Department of Surgical Gynecology, Research Center of Obstetrics, Gynecology and Perinatology, Ministry of Health of Russia. 119997, Russia, Moscow, Ac. Oparina str. 4

Alexandra Vyacheslavovna Asaturova

Email: a_asaturova@oparina4.ru
PhD, senior scientific researcher of pathology department, Research Center of Obstetrics, Gynecology and Perinatology, Ministry of Health of Russia 119997, Russia, Moscow, Ac. Oparina str. 4

Leila Vladimirovna Adamyan

Email: l_adamyan@oparina4.ru
MD, professor, academician of RAS; deputy director on science, head of department of operative gynecology, Research Center of Obstetrics, Gynecology and Perinatology; head of department of reproductive medicine and surgery, faculty of postgraduate education, Moscow State University of Medicine and Dentistry 119997, Russia, Moscow, Ac. Oparina str. 4

References

  1. Адамян Л.В., Спицын В.А., Андреева Е.Н. Генетические аспекты гинекологических заболеваний. М.: ГЭОТАР-Медиа; 2008. 215с. [Adamyan L.V., Spitsyn V.A. Andreeva E.N. Genetic aspects of gynecological diseases. Moscow: GEOTAR-Media; 2008. 215p. (in Russian)]
  2. Адамян Л.В., Азнаурова Я.Б. Молекулярные аспекты патогенеза эндо-метриоза. Проблемы репродукции. 2015; 21(2): 67-77. [Adamyan L.V., Aznaurova Ya.B. Molecular aspects of the pathogenesis of endometriosis. Problemy reproduktsii. 2015; 21(2): 67-77. (in Russian)]
  3. Коган Е.А., Калинина Е.А., Колотовкина А.В., Файзуллина Н.М., Адамян Л.В. Морфологический и молекулярный субстрат нарушения рецептивности эндометрия у бесплодных пациенток с наружно-генитальным эндометриозом. Акушерство и гинекология. 2014; 8: 71-5. [Kondratovich L.M., Kozachenko A.V., Kogan E.A., Faizullina N.M., Adamyan L.V. The clinical and morphological features of an adhesive process in patients with uterine myoma. Akusherstvo i Ginekologiya/Obstetrics and Gynecology. 2014; (8): 71-5. (in Russian)]
  4. Бурлев В.А., Павлович С.В., Ильясова Н.А. Апоптоз и пролиферативная активность в эндометрии при перитонеальном эндометриозе. Бюллетень экспериментальной биологии и медицины. 2006; 141(2): 165-8. [Burlev V.A., Pavlovich S.V., Ilyasova N.A. Apoptosis and proliferative activity in the endometrium in peritoneal endometriosis. Byulleten eksperimentalnoy biologii i meditsiny. 2006; 141(2): 165-8. (in Russian)]
  5. Зайратьянц О.В., Адамян Л.В., Андреева Е.Н., Максимова Ю.В., Мурдалова З.Х., Опаленов К.В., Мовтаева Х.Р., Сонова М.М. Молекулярно-биологические особенности эктопического и эутопического эндометрия при генитальном эндометриозе. Архив патологии. 2010; 72(5): 6-12. [Zayratyants O.V., Adamyan L.V., Andreeva E.N., Maksimova Yu.V., Murdalova Z.H., Opalenov K.V., Movtaeva H.R., Sonova M.M. Molecular-biological features of ectopic and eutopic endometrium in genital endometriosis. Arkhiv patologii. 2010; 72(5): 6-12. (in Russian)]
  6. Зайратьянц О.В., Адамян Л.В., Сомова М.М., Борзенкова И.П., Опаленов К.В., Барсанова Т.Г., Мовтаева Х.Р. Экспрессия ароматазы цитохрома Р-450 в эктопическом и эутопическом эндометрии при эндометриозе. Архив патологии. 2008; 70(5): 16-20. [Zayratyants O.V., Adamyan L.V., Somova M.M., Borzenkova I.P., Opalenov K.V., Barsanova T.G., Movtaeva X.R. The expression of aromatase cytochrome P-450 in ectopic and eutopic endometrium of endometriosis. Arkhiv patologii. 2008; 70(5): 16-20. (in Russian)]
  7. Sourial S., Tempest N., Hapangama D.K. Theories on the pathogenesis of endometriosis. Int. J. Reprod. Med. 2014; 2014: 179515. doi: 10.1155/2014/179515.
  8. Burney R.O., Giudice L.C. Pathogenesis and pathophysiology of endometriosis. Fertil. Steril. 2012; 98(3): 511-9. doi: 10.1016/j.fertnstert.2012.06.029.
  9. Augoulea A., Alexandrou A., Creatsa M., Vrachnis N., Lambrinoudaki I. Pathogenesis of endometriosis: the role of genetics, inflammation and oxidative stress. Arch. Gynecol. Obstet. 2012; 286(1): 99-103. doi: 10.1007/s00404-012-2357-8.
  10. Osuga Y., Koga K., Hirota Y., Hirata T., Yoshino O., Taketani Y. Lymphocytes in endometriosis. Am. J. Reprod. Immunol. 2011; 65(1): 1-10. doi: 10.1111/j.1600-0897.2010.00887.x.
  11. Laschke M. W., Giebels C., Menger M.D. Vasculogenesis: a new piece of the endometriosis puzzle. Hum. Reprod. Update. 2011; 17(5): 628-36. doi: 10.1093/ humupd/dmr023.
  12. Taniguchi F., Kaponis A., Izawa M., Kiyama T., Deura I., Ito M. et al. Apoptosis and endometriosis. Front. Biosci. (Elite Ed). 2011; 3: 648-62.
  13. Albertsen H.M., Chettier R., Farrington P., Ward K. Genome-wide association study link novel loci to endometriosis. PLoS One. 2013; 8(3): e58257. doi: 10.1371/journal.pone.0058257.
  14. Khan M.A., Sengupta J., Mittal S., Ghosh D. Genome-wide expressions in autologous eutopic and ectopic endometrium of fertile women with endometriosis. Reprod. Biol. Endocrinol. 2012; 10: 84. doi: 10.1186/1477-7827-10-84.
  15. Maruyama T., Yoshimura Y. Stem cell theory for the pathogenesis of endometriosis. Front. Biosci. (Elite Ed). 2012; 4: 2854-63.
  16. Nasu K., Yuge A., Tsuno A., Nishida M., Narahara H. Involvement of resistance to apoptosis in the pathogenesis of endometriosis. Histol. Histopathol. 2009; 24(9): 1181-92.
  17. Takebayashi A., Kimura F., Kishi Y., Ishida M., Takahashi A., Yamanaka A. et al. The association between endometriosis and chronic endometritis. PLoS One. 2014; 9(2): e88354. doi: 10.1371/journal.pone.0088354. eCollection 2014.
  18. Johnston-MacAnanny E.B., Hartnett J., Engmann L.L., Nulsen J.C., Sanders M.M., Benadiva C.A. Chronic endometritis is a frequent finding in women with recurrent implantation failure after in vitro fertilization. Fertil. Steril. 2010; 93(2): 437-41. doi: 10.1016/j.fertnstert.2008.12.131.
  19. Tong J.L., Lang J.H., Zhu L., Feng R.E., Cui Q.C. Study on pathological characteristics of eutopic endometrium in endometriosis. Zhonghua Fu Chan Ke Za Zhi. 2012; 47(11): 829-32.
  20. Locci R., Nisolle M., Angioni S., Foidart J.M., Munaut C. Expression of the gamma 2 chain of laminin-332 in eutopic and ectopic endometrium of patients with endometriosis. Reprod. Biol. Endocrinol. 2013; 11: 94. doi: 10.1186/1477-7827-11-94.
  21. Sundqvist J., Andersson K.L., Scarselli G., Gemzell-Danielsson K., Lalitkumar P.G. Expression of adhesion, attachment and invasion markers in eutopic and ectopic endometrium: a link to the aetiology of endometriosis. Hum. Reprod. 2012; 27(9): 2737-46. doi: 10.1093/humrep/des220.
  22. Li X., Zhang Y., Zhao L., Wang L., Wu Z., Mei Q. et al. Whole-exome sequencing of endometriosis identifies frequent alterations in genes involved in cell adhesion and chromatin-remodeling complexes. Hum. Mol. Genet. 2014; 23(22): 6008-21. doi: 10.1093/hmg/ddu330.
  23. Huang Y., Shen L., Cai A., Xiao J. Effect of warming Yang and removing blood stasis method on matrix metalloproteinases / tissue inhibitor metalloproteinases levels secreted by cultured endometrial cells from patients with endometriosis. J. Tradit. Chin. Med. 2015; 35(5): 571-6.
  24. Jana S.K., Banerjee P., Mukherjee R., Chakravarty B., Chaudhury K. HOXA-11 mediated dysregulation of matrix remodeling during implantation window in women with endometriosis. J. Assist. Reprod. Genet. 2013; 30(11): 1505-12. doi: 10.1007/s10815-013-0088-9.
  25. Trovo de Marqui A.B. Genetic polymorphisms and endometriosis: contribution of genes that regulate vascular function and tissue remodeling. Rev. Assoc. Med. Bras. 2012; 58(5): 620-32.
  26. Xu H., Zhang T., Man G.C., May K.E., Becker C.M., Davis T.N. et al. Vascular endothelial growth factor C is increased in endometrium and promotes endothelial functions, vascular permeability and angiogenesis and growth of endometriosis. Angiogenesis. 2013; 16(3): 541-51. doi: 10.1007/s10456-013-9333-1.
  27. Hey-Cunningham A.J., Markham R., Fraser I.S., Berbic M. Dysregulation of vascular endothelial growth factors and their neuropilin receptors in the eutopic endometrium of women with endometriosis. Reprod. Sci. 2013; 20(11): 1382-9. doi: 10.1177/1933719113485299.
  28. Cho S., Choi Y.S., Jeon Y.E., Im K.J., Choi Y.M., Yim S.Y. et al. Expression of vascular endothelial growth factor (VEGF) and its soluble receptor-1 in endometriosis. Microvasc. Res. 2012; 83(2): 237-42. doi: 10.1016/ j.mvr.2011.12.004.
  29. Saliminejad K., Memariani T., Ardekani A.M., Kamali K., Edalatkhah H., Pahlevanzadeh Z., KhorramKhorshid H.R. Association study of the TNF-α -1031T/C and VEGF +450G/C polymorphisms with susceptibility to endometriosis. Gynecol. Endocrinol. 2013; 29(11): 974-7. doi: 10.3109/09513590.2013.824956.
  30. Laudanski P., Charkiewicz R., Kuzmicki M., Szamatowicz J., Swiqtecka J., Mroczko B., Niklinski J. Profiling of selected angiogenesis-related genes in proliferative eutopic endometrium of women with endometriosis. Eur. J. Obstet. Gynecol. Reprod. Biol. 2014; 172: 85-92. doi: 10.1016/ j.ejogrb.2013.10.007.
  31. Deng K.X., Liu X.C., Zheng Y.H., Hu L.Q., Luo R.H., Qiang R. Expression and significance of HOXA10 gene in the eutopic and ectopic endometrium of endometriosis. Zhonghua Fu Chan Ke Za Zhi. 2011; 46(11): 813-6.
  32. Forte A., Cipollaro M., Galderisi U. Genetic, epigenetic and stem cell alterations in endometriosis: new insights and potential therapeutic perspectives. Clin. Sci. (London). 2014; 126(2): 123-38. doi: 10.1042/CS20130099.
  33. Meola J., Dentillo D.B., Rosa e Silva J.C., Hidalgo Gdos S., Paz C.C., Ferriani R.A. RHOC: a key gene for endometriosis. Reprod. Sci. 2013; 20(8): 998-1002. doi: 10.1177/1933719112472743.
  34. Mafra F/A., Christofolini D.M., Cavalcanti V., Vilarino F.L., André G.M., Kato P. et al. Aberrant telomerase expression in the endometrium of infertile women with deep endometriosis. Arch. Med. Res. 2014; 45(1): 31-5. doi: 10.1016/j. arcmed.2013.12.002.
  35. Timologou A., Zafrakas M., Grimbizis G., Miliaras D., Kotronis K., Stamatopoulos P., Tarlatzis B.C. Immunohistochemical expression pattern of metastasis suppressors KAI1 and KISS1 in endometriosis and normal endometrium. Eur. J. Obstet. Gynecol. Reprod. Biol. 2016; 199: 110-5. doi: 10.1016/j. ejogrb.2016.02.004.
  36. Harada T., Taniguchi F., Izawa M., Ohama Y., Takenaka Y., Tagashira Y. et al. Apoptosis and endometriosis. Front. Biosci. 2007; 12: 3140-51.
  37. Xue Q., Zhou Y.F., Zhu S.N., Bulun S.E. Hypermethylation of the CpG island spanning from exon II to intron III is associated with steroidogenic factor 1 expression in stromal cells of endometriosis. Reprod. Sci. 2011; 18(11): 1080-4. doi: 10.1177/1933719111404614.
  38. Xue Q., Xu Y., Yang H., Zhang L., Shang J., Zeng C. et al. Methylation of a novel CpG island of intron 1 is associated with steroidogenic factor 1 expression in endometriotic stromal cells. Reprod. Sci. 2014; 21(3): 395-400. doi: 10.1177/1933719113497283.
  39. Xue Q., Bai L., Li T., Dong Y., Zhang Y., Zhou Y.F. Expression of steroidogenic factor 1 in ovarian endometriosis and adenomyosis. Zhonghua Fu Chan Ke Za Zhi. 2011; 46(11): 831-3.
  40. Noël J.C., Borghese B., Vaiman D., Fayt I., Anaf V., Chapron C. Steroidogenic factor-1 expression in ovarian endometriosis. Appl. Immunohistochem. Mol. Morphol. 2010; 18(3): 258-61. doi: 10.1097/ PAI.0b013e3181c06948.
  41. Kitawaki J., Kado N., Ishihara H., Koshiba H., Kitaoka Y., Honjo H. Endometriosis: the pathophysiology as an estrogen dependent disease. J. Steroid Biochem. Mol. Biol. 2002; 83: 149-55.
  42. Dassen H., Punyadeera C., Kamps R., Delvoux B., Van Langendonckt A., Donnez J. et al. Estrogen metabolizing enzymes in endometrium and endometriosis. Hum. Reprod. 2007; 22(12): 3148-58.
  43. Margarit L., Taylor A., Roberts M.H., Hopkins L., Davies C., Brenton A.G. et al. MUC1 as a discriminator between endometrium from fertile and infertile patients with PCOS and endometriosis. J. Clin. Endocrinol. Metab. 2010; 95(12): 5320-9. doi: 10.1210/jc.2010-0603.
  44. Jones C.J., Nardo L.G., Litta P., Fazleabas A.T. Peritoneal ectopic lesions from women with endometriosis show abnormalities in progesterone-dependent glycan expression. Fertil. Steril. 2009; 91(4, Suppl.): 1608-10. doi: 10.1016/j. fertnstert.2008.11.032.
  45. Colette S., Defrère S., Van Kerk O., Van Langendonckt A., Dolmans M.M., Donnez J. Differential expression of steroidogenic enzymes accord ing to endometriosis type. Fertil. Steril. 2013; 100(6): 1642-9. doi: 10.1016/ j.fertnstert.2013.08.003.
  46. Yu X., Ren H., Liu T., Yong M., Zhong H. Expression and significance of ERß and TrkB in endometriosis. Clin. Exp. Obstet. Gynecol. 2016; 43(1): 75-81.
  47. Chishima F., Hayakawa S., Yamamoto T., Sugitani M., Karasaki-Suzuki M., Sugita K., Nemoto N. Expression of inducible microsomal prostaglandin E synthase in local lesions of endometriosis patients. Am. J. Reprod. Immunol. 2007; 57(3): 218-26.
  48. Santulli P., Borghese B., Noël J.C., Fayt I., Anaf V., de Ziegler D. et al. Hormonal therapy deregulates prostaglandin-endoperoxidase synthase 2 (PTGS2) expression in endometriotic tissues. J. Clin. Endocrinol. Metab. 2014; 99(3): 881-90. doi: 10.1210/jc.2013-2950.
  49. Wölfler M.M., Küppers M., Rath W., Buck V.U., Meinhold-Heerlein I., Classen-Linke I. Altered expression of progesterone receptor isoforms A and B in human eutopic endometrium in endometriosis patients. Ann. Anat. 2016; 206: 1-6. doi: 10.1016/j.aanat.2016.03.004.
  50. Carrarelli P., Rocha A.L., Belmonte G., Zupi E., Abrno M.S., Arcuri F. et al. Increased expression of antimüllerian hormone and its receptor in endometriosis. Fertil Steril. 2014; 101(5): 1353-8. doi: 10.1016/j.fertnstert.2014.01.052.

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