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Особенности эпителиально-мезенхимального перехода в эктопическом эндометрии у пациенток с экстрагенитальным эндометриозом различной локализации
Особенности эпителиально-мезенхимального перехода в эктопическом эндометрии у пациенток с экстрагенитальным эндометриозом различной локализации
Казаку Е., Зота Е., Варданян М.А., Нигуляну Р., Претула Р., Асатурова А.В., Ежова Л.С., Бадлаева А.С. Особенности эпителиально-мезенхимального перехода в эктопическом эндометрии у пациенток с экстрагенитальным эндометриозом различной локализации. Гинекология. 2024;26(2):159–164.
DOI: 10.26442/20795696.2024.2.202799
© ООО «КОНСИЛИУМ МЕДИКУМ», 2024 г.
DOI: 10.26442/20795696.2024.2.202799
© ООО «КОНСИЛИУМ МЕДИКУМ», 2024 г.
________________________________________________
Материалы доступны только для специалистов сферы здравоохранения. Авторизуйтесь или зарегистрируйтесь.
Аннотация
Обоснование. Эпителиально-мезенхимальный переход (ЭМП) является консервативным механизмом в процессе морфогенеза и органогенеза. ЭМП обеспечивает клетки миграционными и инвазивными свойствами, что является необходимым условием для формирования эндометриоидных гетеротопий.
Цель. Подтвердить наличие признаков ЭМП при разных типах эндометриоза.
Материалы и методы. За период 2012–2017 гг. нами проанализировано 43 случая экстрагенитального эндометриоза различной локализации: аппендикс (n=3), ободочная кишка (n=5), тонкая кишка (n=1), передняя брюшная стенка после кесарева сечения (n=24) и паховая грыжа (n=10). Выполнено гистологическое и иммуногистохимическое исследование на парафиновых срезах с использованием моноклональных антител к E-кадгерину и поликлональных антител к виментину.
Результаты. В результате проведенного исследования получены средние значения отношения экспрессии E-кадгерина к виментину в железистых и стромальных клетках эндометриоидных имплантов: брюшины малого таза – 10,3 балла, в колоректальном инфильтрате – 9,1 балла, в червеобразном отростке – 8,6 балла, в подвздошной кишке – 5,5 балла, в грыжевом мешке – 4,2 балла. Выявлена низкая экспрессия Е-кадгерина одновременно по отношению к экспрессии виментина (p<0,05).
Заключение. Результаты нашего исследования подтвердили участие ЭМП в патогенезе экстрагенитального эндометриоза, с одной стороны, и с другой – подтверждают его инвазивный потенциал в изученных локализациях.
Ключевые слова: эндометриоз, эпителиально-мезенхимальный переход, экстрагенитальный эндометриоз
Aim. To confirm the presence of EMT features in different types of endometriosis.
Materials and methods. During a period of five years (2012–2017) we analyzed 43 cases of extragenital endometriosis: appendix (3 case), colon (5 cases), ileum (1 case), abdominal scar endometriosis after caesarean section (24 cases), and inguinal hernia (10 cases). The material was processed according to histological and immunohistochemical technique using monoclonal E-cadherin and polyclonal Vimentin antibodies to assess local invasiveness.
Results. In peritoneal endometriosis, the ratio of E-cadherin to Vimentin expression was 10.3, in the colon = 9.1, in the appendix 8.6, in the ileum 5.5, in the hernial sac 4.2. Thus, in diffuse infiltrative forms of endometriosis, the lesion phenotype is characterized by low expression of E-cadherin, while expression of Vimentin is at a high level (p<0.05).
Conclusion. The results of our study confirmed involvement of the epithelial-mesenchymal transition process in the pathogenesis of extragenital endometriosis lesions, on the one hand, and they certify its invasive potential in these localizations, on the other hand.
Keywords: endometriosis, epithelial to mesenchymal transition process, extragenital endometriosis
Цель. Подтвердить наличие признаков ЭМП при разных типах эндометриоза.
Материалы и методы. За период 2012–2017 гг. нами проанализировано 43 случая экстрагенитального эндометриоза различной локализации: аппендикс (n=3), ободочная кишка (n=5), тонкая кишка (n=1), передняя брюшная стенка после кесарева сечения (n=24) и паховая грыжа (n=10). Выполнено гистологическое и иммуногистохимическое исследование на парафиновых срезах с использованием моноклональных антител к E-кадгерину и поликлональных антител к виментину.
Результаты. В результате проведенного исследования получены средние значения отношения экспрессии E-кадгерина к виментину в железистых и стромальных клетках эндометриоидных имплантов: брюшины малого таза – 10,3 балла, в колоректальном инфильтрате – 9,1 балла, в червеобразном отростке – 8,6 балла, в подвздошной кишке – 5,5 балла, в грыжевом мешке – 4,2 балла. Выявлена низкая экспрессия Е-кадгерина одновременно по отношению к экспрессии виментина (p<0,05).
Заключение. Результаты нашего исследования подтвердили участие ЭМП в патогенезе экстрагенитального эндометриоза, с одной стороны, и с другой – подтверждают его инвазивный потенциал в изученных локализациях.
Ключевые слова: эндометриоз, эпителиально-мезенхимальный переход, экстрагенитальный эндометриоз
________________________________________________
Aim. To confirm the presence of EMT features in different types of endometriosis.
Materials and methods. During a period of five years (2012–2017) we analyzed 43 cases of extragenital endometriosis: appendix (3 case), colon (5 cases), ileum (1 case), abdominal scar endometriosis after caesarean section (24 cases), and inguinal hernia (10 cases). The material was processed according to histological and immunohistochemical technique using monoclonal E-cadherin and polyclonal Vimentin antibodies to assess local invasiveness.
Results. In peritoneal endometriosis, the ratio of E-cadherin to Vimentin expression was 10.3, in the colon = 9.1, in the appendix 8.6, in the ileum 5.5, in the hernial sac 4.2. Thus, in diffuse infiltrative forms of endometriosis, the lesion phenotype is characterized by low expression of E-cadherin, while expression of Vimentin is at a high level (p<0.05).
Conclusion. The results of our study confirmed involvement of the epithelial-mesenchymal transition process in the pathogenesis of extragenital endometriosis lesions, on the one hand, and they certify its invasive potential in these localizations, on the other hand.
Keywords: endometriosis, epithelial to mesenchymal transition process, extragenital endometriosis
Полный текст
Список литературы
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8. Forster C. Tight junctions and the modulation of barrier function in disease. Histochem. Cell Biol. 2008;130(1):55-70.
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13. Micalizzi DS, Farabaugh SM, Ford HL. Epithelial-mesenchymal transition in cancer: parallels between normal development and tumor progression. J Mammary Gland Biol Noplasia. 2010;15(2):117-34.
14. Zeisberg M, Neilson EG. Biomarkers for epithelial-mesenchymal transition. J Clin Invest. 2009;119(6):1429-37.
15. Mendez MG, Kojima SI, Goldman RD. Vimentin induces changes in cell, motility, and adhesion, during the epithelial to mesenchymal transition. FASEB J. 2010;24(6):1838-51.
16. Turley EA, Veiseh M, Radisky DC, Bissell MJ. Mecanisms of disease: epithelial-mesenchymal transition-does cellular plasticity fuel neoplastic progression? Nat Clin Pract Oncol. 2008;5(5):280-90.
17. Lee J, Dedhar S, Kalluri R, Thompson EW. The epithelial-mesenchymal transition: new insights signaling, development and diseas. J Cell Biol. 2006;172(7):973-81.
18. Xiong Y, Liu Y, Xiong W, et al. Hypoxia-inducible factor 1α-induced epithelial-mesenchymal transition of endometrial epithelial cells may contribute to the development of endometriosis. Hum Reprod. 2016;31(6):1327-38.
19. Pawson T. Signal transduction – a conserved pathway from the membrane to the nucleus. Developmental Genet. 1993;14(5):333-8.
20. Osborne CK, Scchiff R, Fuqua SA, Shou J. Estrogen receptor: current understanding of its activation and modulation. Clin Cancer Res. 2001;7(Suppl. 12):43388-421.
21. Bartley J, Jülicher A, Hotz B, et al. Epithelial to mesenchymal transition (EMT) seems to be regulated differently in endometriosis and the endometrium. Arch Gynecol Obstet. 2014;289(4):871-81.
22. Carver EA, Jiang R, Lan Y, et al. The mouse snail gene in codes a key regulator of epithelial-mesenchymal transition. Mol Cell Biol. 2001;26(13):8148-8.
23. Olmeda D, Jorda M, Peinado H, et al. Snail silencine effectively suppresses tumor growth and invasiveness. Oncogene. 2007;26(13):1862-74.
24. Moreno-Bueno G, Cubillo E, Sarrio D, et al. Genetic profiling of epithelial cells expressing E-cadherin repressors reveals a distinct role for Snail and E47 factors in epithelila-mesenchimal transition. Cancer Res. 2006;66(19):9543-56.
25. De Wever O, Pauwels P, De Craene B, et al. Molecular and pathological signatures of epithelial-mesenchymal transition at the cancer invasion front. Histochem Cell Biol. 2008;130(3):481-94.
26. Huang Y, Fernandez SV, Goodwin S, et al. Epithelial to mesenchymal transition in human breast epithelial cells transformed by 17beta-estradiol. Cancer Res. 2007;67(23):11147-57.
27. Vicovac L, Aplin JD. Epithelial-mesenchymal transition during trophoblast differentiation. Acta Anat (Basel). 1996;156(3):202-16.
28. Hugo H, Ackland ML, Blick T, et al. Epithelial-mesenchymal and mesenchymal-epithelial transitions in carcinoma progression. J Cell Physiol. 2007;213:374-83.
29. Thiery JP, Sleeman JP. Complex networks orchestrate epithelial-mesenchymal transition. Nat Rev Mol Cell Biol. 2006;7(2):131-42.
30. Cano A, Perez-Moreno MA, Rodrigo I, et al. The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat Cell Biol.
2000;2:76-83. DOI:10.1038/35000025
31. Proestling K, Birner P, Gamperl S, et al. Enhanced epithelial to mesenchymal transition (EMT) and upregulated MYC in ectopic lesions contribute independently to endometriosis. Reprod Biol Endocrinol. 2015;13:75.
32. Sachiko M, Darcha Cl. Epithelial to mesenchymal transition like and mesenchymal to epithelial transition-like processes might be involved in the pathogenesis of pelvic endometriosis. Human Reproduction. 2012;27(3):712-21.
33. Gaetje R, Kotzian S, Herrmann G, et al. Nonmalignant epithelial cells, potentially invasive in human endometriosis, lack the tumor suppressor molecule E-cadherin. Am J Pathol. 1997;150(2):461-7.
34. Zeitvogel A, Baumann R, Starzinski-Powitz A. Identification of an invasive, N-cadherin-expressing epithelial cell type in endometriosis using a new cell culture model. Am J Pathol. 2001;159(5):1839-52. DOI:10.1016/S0002-9440(10)63030-1
35. Kalluri R, Weinberg RA. The basics of epithelial-mesenchymal transition. J Clin Invest. 2009;119(6):1420-8.
36. Radisky ES, Radisky GC. Matrix metallo-proteinase-induced epithelial-mesenchymal transition in breast. J Mammary Gland Biol Neoplasia. 2010;15(2):201-12.
2. Zondervan KT, Becker CM, Missmer SA. Endometriosis. N Engl J Med. 2020;382:1244-56.
3. Falcone T, Flyckt R. Clinical Management of Endometriosis. Obstet Gynecol. 2018;131(3):557-71. DOI:10.1097/AOG.0000000000002469
4. Hay EB. Organization and fine structure of epithelium and mesenchyme in the developing chick embrio. In: Epithelial-mesenchymal interactions. R Fleischmajer and RE Billinghram, editors. Williams and Wilkins. Baltimore, Maryland, USA, 1968; p. 31-55.
5. Kalluri R, Neilson EG. Epithelial-mesenchymal transition and its implications in fibrosis. J Clin Invest. 2003;112(12):1776-84.
6. Acloque H, Adams M, Fishwick K, et al. Epithelial-mesenchymal interaction: the importance of changing cell state in development and disease. J Clin Invest. 2009;119(6):1438-49.
7. Yang YM, Yang WX. Epithelial-to-mesenchymal transition in the development of endometriosis. Oncotarget. 2017;8(25):41679-89. DOI:10.18632/oncotarget.16472
8. Forster C. Tight junctions and the modulation of barrier function in disease. Histochem. Cell Biol. 2008;130(1):55-70.
9. Hulpiau P, van Roy F. Molecular evolution of the cadtherin superfamily. Int J Biochem Cell Biol. 2009;41(2):349-69.
10. Walker JL, Menko A, Khalil S, et al. Diverse roles of E-cadherin in the morphogenesis of submandibular gland. Dev Dyn. 2008;237(11):3126-41.
11. Al-Amoudi A, Castano-Diez D, Devos DP, et al. The three-dimensional molecular structure of the desmosomal plaque. Proc Natl Acad Sci USA. 2011;108(16):6480-5. DOI:10.1073/pnas.1019469108
12. Acepan D, Petzold C, Gumper I, et al. Plakoglobin is required for effective intermediate filament anchorage to desmosomes. J Invest Dermatol. 2008;128(11):2665-75.
13. Micalizzi DS, Farabaugh SM, Ford HL. Epithelial-mesenchymal transition in cancer: parallels between normal development and tumor progression. J Mammary Gland Biol Noplasia. 2010;15(2):117-34.
14. Zeisberg M, Neilson EG. Biomarkers for epithelial-mesenchymal transition. J Clin Invest. 2009;119(6):1429-37.
15. Mendez MG, Kojima SI, Goldman RD. Vimentin induces changes in cell, motility, and adhesion, during the epithelial to mesenchymal transition. FASEB J. 2010;24(6):1838-51.
16. Turley EA, Veiseh M, Radisky DC, Bissell MJ. Mecanisms of disease: epithelial-mesenchymal transition-does cellular plasticity fuel neoplastic progression? Nat Clin Pract Oncol. 2008;5(5):280-90.
17. Lee J, Dedhar S, Kalluri R, Thompson EW. The epithelial-mesenchymal transition: new insights signaling, development and diseas. J Cell Biol. 2006;172(7):973-81.
18. Xiong Y, Liu Y, Xiong W, et al. Hypoxia-inducible factor 1α-induced epithelial-mesenchymal transition of endometrial epithelial cells may contribute to the development of endometriosis. Hum Reprod. 2016;31(6):1327-38.
19. Pawson T. Signal transduction – a conserved pathway from the membrane to the nucleus. Developmental Genet. 1993;14(5):333-8.
20. Osborne CK, Scchiff R, Fuqua SA, Shou J. Estrogen receptor: current understanding of its activation and modulation. Clin Cancer Res. 2001;7(Suppl. 12):43388-421.
21. Bartley J, Jülicher A, Hotz B, et al. Epithelial to mesenchymal transition (EMT) seems to be regulated differently in endometriosis and the endometrium. Arch Gynecol Obstet. 2014;289(4):871-81.
22. Carver EA, Jiang R, Lan Y, et al. The mouse snail gene in codes a key regulator of epithelial-mesenchymal transition. Mol Cell Biol. 2001;26(13):8148-8.
23. Olmeda D, Jorda M, Peinado H, et al. Snail silencine effectively suppresses tumor growth and invasiveness. Oncogene. 2007;26(13):1862-74.
24. Moreno-Bueno G, Cubillo E, Sarrio D, et al. Genetic profiling of epithelial cells expressing E-cadherin repressors reveals a distinct role for Snail and E47 factors in epithelila-mesenchimal transition. Cancer Res. 2006;66(19):9543-56.
25. De Wever O, Pauwels P, De Craene B, et al. Molecular and pathological signatures of epithelial-mesenchymal transition at the cancer invasion front. Histochem Cell Biol. 2008;130(3):481-94.
26. Huang Y, Fernandez SV, Goodwin S, et al. Epithelial to mesenchymal transition in human breast epithelial cells transformed by 17beta-estradiol. Cancer Res. 2007;67(23):11147-57.
27. Vicovac L, Aplin JD. Epithelial-mesenchymal transition during trophoblast differentiation. Acta Anat (Basel). 1996;156(3):202-16.
28. Hugo H, Ackland ML, Blick T, et al. Epithelial-mesenchymal and mesenchymal-epithelial transitions in carcinoma progression. J Cell Physiol. 2007;213:374-83.
29. Thiery JP, Sleeman JP. Complex networks orchestrate epithelial-mesenchymal transition. Nat Rev Mol Cell Biol. 2006;7(2):131-42.
30. Cano A, Perez-Moreno MA, Rodrigo I, et al. The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat Cell Biol.
2000;2:76-83. DOI:10.1038/35000025
31. Proestling K, Birner P, Gamperl S, et al. Enhanced epithelial to mesenchymal transition (EMT) and upregulated MYC in ectopic lesions contribute independently to endometriosis. Reprod Biol Endocrinol. 2015;13:75.
32. Sachiko M, Darcha Cl. Epithelial to mesenchymal transition like and mesenchymal to epithelial transition-like processes might be involved in the pathogenesis of pelvic endometriosis. Human Reproduction. 2012;27(3):712-21.
33. Gaetje R, Kotzian S, Herrmann G, et al. Nonmalignant epithelial cells, potentially invasive in human endometriosis, lack the tumor suppressor molecule E-cadherin. Am J Pathol. 1997;150(2):461-7.
34. Zeitvogel A, Baumann R, Starzinski-Powitz A. Identification of an invasive, N-cadherin-expressing epithelial cell type in endometriosis using a new cell culture model. Am J Pathol. 2001;159(5):1839-52. DOI:10.1016/S0002-9440(10)63030-1
35. Kalluri R, Weinberg RA. The basics of epithelial-mesenchymal transition. J Clin Invest. 2009;119(6):1420-8.
36. Radisky ES, Radisky GC. Matrix metallo-proteinase-induced epithelial-mesenchymal transition in breast. J Mammary Gland Biol Neoplasia. 2010;15(2):201-12.
2. Zondervan KT, Becker CM, Missmer SA. Endometriosis. N Engl J Med. 2020;382:1244-56.
3. Falcone T, Flyckt R. Clinical Management of Endometriosis. Obstet Gynecol. 2018;131(3):557-71. DOI:10.1097/AOG.0000000000002469
4. Hay EB. Organization and fine structure of epithelium and mesenchyme in the developing chick embrio. In: Epithelial-mesenchymal interactions. R Fleischmajer and RE Billinghram, editors. Williams and Wilkins. Baltimore, Maryland, USA, 1968; p. 31-55.
5. Kalluri R, Neilson EG. Epithelial-mesenchymal transition and its implications in fibrosis. J Clin Invest. 2003;112(12):1776-84.
6. Acloque H, Adams M, Fishwick K, et al. Epithelial-mesenchymal interaction: the importance of changing cell state in development and disease. J Clin Invest. 2009;119(6):1438-49.
7. Yang YM, Yang WX. Epithelial-to-mesenchymal transition in the development of endometriosis. Oncotarget. 2017;8(25):41679-89. DOI:10.18632/oncotarget.16472
8. Forster C. Tight junctions and the modulation of barrier function in disease. Histochem. Cell Biol. 2008;130(1):55-70.
9. Hulpiau P, van Roy F. Molecular evolution of the cadtherin superfamily. Int J Biochem Cell Biol. 2009;41(2):349-69.
10. Walker JL, Menko A, Khalil S, et al. Diverse roles of E-cadherin in the morphogenesis of submandibular gland. Dev Dyn. 2008;237(11):3126-41.
11. Al-Amoudi A, Castano-Diez D, Devos DP, et al. The three-dimensional molecular structure of the desmosomal plaque. Proc Natl Acad Sci USA. 2011;108(16):6480-5. DOI:10.1073/pnas.1019469108
12. Acepan D, Petzold C, Gumper I, et al. Plakoglobin is required for effective intermediate filament anchorage to desmosomes. J Invest Dermatol. 2008;128(11):2665-75.
13. Micalizzi DS, Farabaugh SM, Ford HL. Epithelial-mesenchymal transition in cancer: parallels between normal development and tumor progression. J Mammary Gland Biol Noplasia. 2010;15(2):117-34.
14. Zeisberg M, Neilson EG. Biomarkers for epithelial-mesenchymal transition. J Clin Invest. 2009;119(6):1429-37.
15. Mendez MG, Kojima SI, Goldman RD. Vimentin induces changes in cell, motility, and adhesion, during the epithelial to mesenchymal transition. FASEB J. 2010;24(6):1838-51.
16. Turley EA, Veiseh M, Radisky DC, Bissell MJ. Mecanisms of disease: epithelial-mesenchymal transition-does cellular plasticity fuel neoplastic progression? Nat Clin Pract Oncol. 2008;5(5):280-90.
17. Lee J, Dedhar S, Kalluri R, Thompson EW. The epithelial-mesenchymal transition: new insights signaling, development and diseas. J Cell Biol. 2006;172(7):973-81.
18. Xiong Y, Liu Y, Xiong W, et al. Hypoxia-inducible factor 1α-induced epithelial-mesenchymal transition of endometrial epithelial cells may contribute to the development of endometriosis. Hum Reprod. 2016;31(6):1327-38.
19. Pawson T. Signal transduction – a conserved pathway from the membrane to the nucleus. Developmental Genet. 1993;14(5):333-8.
20. Osborne CK, Scchiff R, Fuqua SA, Shou J. Estrogen receptor: current understanding of its activation and modulation. Clin Cancer Res. 2001;7(Suppl. 12):43388-421.
21. Bartley J, Jülicher A, Hotz B, et al. Epithelial to mesenchymal transition (EMT) seems to be regulated differently in endometriosis and the endometrium. Arch Gynecol Obstet. 2014;289(4):871-81.
22. Carver EA, Jiang R, Lan Y, et al. The mouse snail gene in codes a key regulator of epithelial-mesenchymal transition. Mol Cell Biol. 2001;26(13):8148-8.
23. Olmeda D, Jorda M, Peinado H, et al. Snail silencine effectively suppresses tumor growth and invasiveness. Oncogene. 2007;26(13):1862-74.
24. Moreno-Bueno G, Cubillo E, Sarrio D, et al. Genetic profiling of epithelial cells expressing E-cadherin repressors reveals a distinct role for Snail and E47 factors in epithelila-mesenchimal transition. Cancer Res. 2006;66(19):9543-56.
25. De Wever O, Pauwels P, De Craene B, et al. Molecular and pathological signatures of epithelial-mesenchymal transition at the cancer invasion front. Histochem Cell Biol. 2008;130(3):481-94.
26. Huang Y, Fernandez SV, Goodwin S, et al. Epithelial to mesenchymal transition in human breast epithelial cells transformed by 17beta-estradiol. Cancer Res. 2007;67(23):11147-57.
27. Vicovac L, Aplin JD. Epithelial-mesenchymal transition during trophoblast differentiation. Acta Anat (Basel). 1996;156(3):202-16.
28. Hugo H, Ackland ML, Blick T, et al. Epithelial-mesenchymal and mesenchymal-epithelial transitions in carcinoma progression. J Cell Physiol. 2007;213:374-83.
29. Thiery JP, Sleeman JP. Complex networks orchestrate epithelial-mesenchymal transition. Nat Rev Mol Cell Biol. 2006;7(2):131-42.
30. Cano A, Perez-Moreno MA, Rodrigo I, et al. The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat Cell Biol.
2000;2:76-83. DOI:10.1038/35000025
31. Proestling K, Birner P, Gamperl S, et al. Enhanced epithelial to mesenchymal transition (EMT) and upregulated MYC in ectopic lesions contribute independently to endometriosis. Reprod Biol Endocrinol. 2015;13:75.
32. Sachiko M, Darcha Cl. Epithelial to mesenchymal transition like and mesenchymal to epithelial transition-like processes might be involved in the pathogenesis of pelvic endometriosis. Human Reproduction. 2012;27(3):712-21.
33. Gaetje R, Kotzian S, Herrmann G, et al. Nonmalignant epithelial cells, potentially invasive in human endometriosis, lack the tumor suppressor molecule E-cadherin. Am J Pathol. 1997;150(2):461-7.
34. Zeitvogel A, Baumann R, Starzinski-Powitz A. Identification of an invasive, N-cadherin-expressing epithelial cell type in endometriosis using a new cell culture model. Am J Pathol. 2001;159(5):1839-52. DOI:10.1016/S0002-9440(10)63030-1
35. Kalluri R, Weinberg RA. The basics of epithelial-mesenchymal transition. J Clin Invest. 2009;119(6):1420-8.
36. Radisky ES, Radisky GC. Matrix metallo-proteinase-induced epithelial-mesenchymal transition in breast. J Mammary Gland Biol Neoplasia. 2010;15(2):201-12.
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Авторы
Е. Казаку1, Е. Зота1, М.А. Варданян*2, Р. Нигуляну1, Р. Претула1, А.В. Асатурова2, Л.С. Ежова2, А.С. Бадлаева2
1Государственный университет медицины и фармакологии им. Николая Тестемицану, Кишинев, Молдавия;
2ФГБУ «Национальный медицинский исследовательский центр акушерства, гинекологии и перинатологии им. акад. В.И. Кулакова» Минздрава России, Москва, Россия
*mv132013@mail.ru
1Nicolae Testemitanu State University of Medicine and Pharmacology, Chisinau, Moldova;
2Kulakov National Medical Research Center for Obstetrics, Gynecology and Perinatology, Moscow, Russia
*mv132013@mail.ru
1Государственный университет медицины и фармакологии им. Николая Тестемицану, Кишинев, Молдавия;
2ФГБУ «Национальный медицинский исследовательский центр акушерства, гинекологии и перинатологии им. акад. В.И. Кулакова» Минздрава России, Москва, Россия
*mv132013@mail.ru
________________________________________________
1Nicolae Testemitanu State University of Medicine and Pharmacology, Chisinau, Moldova;
2Kulakov National Medical Research Center for Obstetrics, Gynecology and Perinatology, Moscow, Russia
*mv132013@mail.ru
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