The bimodal role of matrix metalloproteinases and their inhibitors in etiology and pathogenesis of endometriosis (Review)
- Authors:
- Magdalenia Bałkowiec
- Radosław B. Maksym
- Paweł K. Włodarski
-
Affiliations: Department of Histology and Embryology, Medical University of Warsaw, 02-004 Warsaw, Poland, Center for Preclinical Research, Department of Methodology, Medical University of Warsaw, 02-097 Warsaw, Poland - Published online on: July 23, 2018 https://doi.org/10.3892/mmr.2018.9303
- Pages: 3123-3136
-
Copyright: © Bałkowiec et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
|
Burney RO and Giudice LC: Pathogenesis and pathophysiology of endometriosis. Fertil Steril. 98:511–519. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Sampson JA: Metastatic or embolic endometriosis, due to the menstrual dissemination of endometrial tissue into the venous circulation. Am J Pathol. 3(93–110): 1431927.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 | |
|
BRENDA: The Comprehensive Enzyme Information System. https://www.brenda-enzymes.org | |
|
Verma RP and Hansch C: Matrix metalloproteinases (MMPs): Chemical-biological functions and (Q)SARs. Bioorg Med Chem. 15:2223–2268. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Rodgers WH, Osteen KG, Matrisian LM, Navre M, Giudice LC and Gorstein F: Expression and localization of matrilysin, a matrix metalloproteinase, in human endometrium during the reproductive cycle. Am J Obstet Gynecol. 168:253–260. 1993. View Article : Google Scholar : PubMed/NCBI | |
|
Rodgers WH, Matrisian LM, Giudice LC, Dsupin B, Cannon P, Svitek C, Gorstein F and Osteen KG: Patterns of matrix metalloproteinase expression in cycling endometrium imply differential functions and regulation by steroid hormones. J Clin Invest. 94:946–953. 1994. View Article : Google Scholar : PubMed/NCBI | |
|
Chevronnay Gaide HP, Selvais C, Emonard H, Galant C, Marbaix E and Henriet P: Regulation of matrix metalloproteinases activity studied in human endometrium as a paradigm of cyclic tissue breakdown and regeneration. Biochim Biophys Acta. 1824:146–156. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Amălinei C, Căruntu ID, Giuşcă SE and Bălan RA: Matrix metalloproteinases involvement in pathologic conditions. Rom J Morphol Embryol. 51:215–228. 2010.PubMed/NCBI | |
|
Di Nezza LA, Misajon A, Zhang J, Jobling T, Quinn MA, Ostör AG, Nie G, Lopata A and Salamonsen LA: Presence of active gelatinases in endometrial carcinoma and correlation of matrix metalloproteinase expression with increasing tumor grade and invasion. Cancer. 94:1466–1475. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Takahashi C, Sheng Z, Horan TP, Kitayama H, Maki M, Hitomi K, Kitaura Y, Takai S, Sasahara RM, Horimoto A, et al: Regulation of matrix metalloproteinase-9 and inhibition of tumor invasion by the membrane-anchored glycoprotein RECK. Proc Natl Acad Sci USA. 95:13221–13226. 1998. View Article : Google Scholar : PubMed/NCBI | |
|
Matrisian LM: The matrix-degrading metalloproteinases. Bioessays. 14:455–463. 1992. View Article : Google Scholar : PubMed/NCBI | |
|
Murphy G: Tissue inhibitors of metalloproteinases. Genome Biol. 12:2332011. View Article : Google Scholar : PubMed/NCBI | |
|
Wang WM, Ge G, Lim NH, Nagase H and Greenspan DS: TIMP-3 inhibits the procollagen N-proteinase ADAMTS-2. Biochem J. 398:515–519. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Kashiwagi M, Tortorella M, Nagase H and Brew K: TIMP-3 is a potent inhibitor of aggrecanase 1 (ADAM-TS4) and aggrecanase 2 (ADAM-TS5). J Biol Chem. 276:12501–12504. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
Amour A, Slocombe PM, Webster A, Butler M, Knight CG, Smith BJ, Stephens PE, Shelley C, Hutton M, Knäuper V, et al: TNF-alpha converting enzyme (TACE) is inhibited by TIMP-3. FEBS Lett. 435:39–44. 1998. View Article : Google Scholar : PubMed/NCBI | |
|
Amour A, Knight CG, Webster A, Slocombe PM, Stephens PE, Knäuper V, Docherty AJ and Murphy G: The in vitro activity of ADAM-10 is inhibited by TIMP-1 and TIMP-3. FEBS Lett. 473:275–279. 2000. View Article : Google Scholar : PubMed/NCBI | |
|
Seals DF and Courtneidge SA: The ADAMs family of metalloproteases: Multidomain proteins with multiple functions. Genes Dev. 17:7–30. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Alexius-Lindgren M, Andersson E, Lindstedt I and Engström W: The RECK gene and biological malignancy-its significance in angiogenesis and inhibition of matrix metalloproteinases. Anticancer Res. 34:3867–3873. 2014.PubMed/NCBI | |
|
Clark JC, Thomas DM, Choong PF and Dass CR: RECK-a newly discovered inhibitor of metastasis with prognostic significance in multiple forms of cancer. Cancer Metastasis Rev. 26:675–683. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Bruner-Tran KL, Eisenberg E, Yeaman GR, Anderson TA, McBean J and Osteen KG: Steroid and cytokine regulation of matrix metalloproteinase expression in endometriosis and the establishment of experimental endometriosis in nude mice. J Clin Endocrinol Metab. 87:4782–4791. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Osteen KG, Bruner KL and Sharpe-Timms KL: Steroid and growth factor regulation of matrix metalloproteinase expression and endometriosis. Semin Reprod Endocrinol. 14:247–255. 1996. View Article : Google Scholar : PubMed/NCBI | |
|
Sharpe-Timms KL and Cox KE: Paracrine regulation of matrix metalloproteinase expression in endometriosis. Ann N Y Acad Sci. 955(147–158): 396–406. 2002. | |
|
Gezer A and Oral E: Progestin therapy in endometriosis. Womens Health (Lond). 11:643–652. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Osteen KG, Rodgers WH, Gaire M, Hargrove JT, Gorstein F and Matrisian LM: Stromal-epithelial interaction mediates steroidal regulation of metalloproteinase expression in human endometrium. Proc Natl Acad Sci USA. 91:10129–10133. 1994. View Article : Google Scholar : PubMed/NCBI | |
|
Marbaix E, Donnez J, Courtoy PJ and Eeckhout Y: Progesterone regulates the activity of collagenase and related gelatinases A and B in human endometrial explants. Proc Natl Acad Sci USA. 89:11789–11793. 1992. View Article : Google Scholar : PubMed/NCBI | |
|
Sillem M, Prifti S, Koch A, Neher M, Jauckus J and Runnebaum B: Regulation of matrix metalloproteinases and their inhibitors in uterine endometrial cells of patients with and without endometriosis. Eur J Obstet Gynecol Reprod Biol. 95:167–174. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
Mönckedieck V, Sannecke C, Husen B, Kumbartski M, Kimmig R, Tötsch M, Winterhager E and Grümmer R: Progestins inhibit expression of MMPs and of angiogenic factors in human ectopic endometrial lesions in a mouse model. Mol Hum Reprod. 15:633–643. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Sillem M, Prifti S, Neher M and Runnebaum B: Extracellular matrix remodelling in the endometrium and its possible relevance to the pathogenesis of endometriosis. Hum Reprod Update. 4:730–735. 1998. View Article : Google Scholar : PubMed/NCBI | |
|
Bruner-Tran KL, Zhang Z, Eisenberg E, Winneker RC and Osteen KG: Down-regulation of endometrial matrix metalloproteinase-3 and −7 expression in vitro and therapeutic regression of experimental endometriosis in vivo by a novel nonsteroidal progesterone receptor agonist, tanaproget. J Clin Endocrinol Metab. 91:1554–1560. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Shan B, Li W, Yang SY and Li ZR: Estrogen up-regulates MMP2/9 expression in endometrial epithelial cell via VEGF-ERK1/2 pathway. Asian Pac J Trop Med. 6:826–830. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Huang HF, Hong LH, Tan Y and Sheng JZ: Matrix metalloproteinase 2 is associated with changes in steroid hormones in the sera and peritoneal fluid of patients with endometriosis. Fertil Steril. 81:1235–1239. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Ahn JH, Choi YS and Choi JH: Leptin promotes human endometriotic cell migration and invasion by up-regulating MMP-2 through the JAK2/STAT3 signaling pathway. Mol Hum Reprod. 21:792–802. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Sevket O, Sevket A, Molla T, Buyukpınarbasılı N, Uysal O, Yılmaz B, Dane B and Kelekcı S: Somatostatin analogs regress endometriotic implants in rats by decreasing implant levels of vascular endothelial growth factor and matrix metaloproteinase 9. Reprod Sci. 20:639–645. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Yilmaz B, Kilic S, Aksakal O, Ertas IE, Tanrisever GG, Aksoy Y, Lortlar N, Kelekci S and Gungor T: Melatonin causes regression of endometriotic implants in rats by modulating angiogenesis, tissue levels of antioxidants and matrix metalloproteinases. Arch Gynecol Obstet. 292:209–216. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Parkin KL and Fazleabas AT: Uterine leukocyte function and dysfunction: A hypothesis on the impact of endometriosis. Am J Reprod Immunol. 75:411–417. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Braundmeier AG and Nowak RA: Cytokines regulate matrix metalloproteinases in human uterine endometrial fibroblast cells through a mechanism that does not involve increases in extracellular matrix metalloproteinase inducer. Am J Reprod Immunol. 56:201–214. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Chegini N: TGF-beta system: The principal profibrotic mediator of peritoneal adhesion formation. Semin Reprod Med. 26:298–312. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Singer CF, Marbaix E, Lemoine P, Courtoy PJ and Eeckhout Y: Local cytokines induce differential expression of matrix metalloproteinases but not their tissue inhibitors in human endometrial fibroblasts. Eur J Biochem. 259:40–45. 1999. View Article : Google Scholar : PubMed/NCBI | |
|
Mulayim N, Savlu A, Guzeloglu-Kayisli O, Kayisli UA and Arici A: Regulation of endometrial stromal cell matrix metalloproteinase activity and invasiveness by interleukin-8. Fertil Steril. 81 Suppl 1:S904–S911. 2004. View Article : Google Scholar | |
|
Singer CF, Marbaix E, Kokorine I, Lemoine P, Donnez J, Eeckhout Y and Courtoy PJ: Paracrine stimulation of interstitial collagenase (MMP-1) in the human endometrium by interleukin 1alpha and its dual block by ovarian steroids. Proc Natl Acad Sci USA. 94:10341–10345. 1997. View Article : Google Scholar : PubMed/NCBI | |
|
Khoufache K, Bondza PK, Harir N, Daris M, Leboeuf M, Mailloux J, Lemyre M, Foster W and Akoum A: Soluble human IL-1 receptor type 2 inhibits ectopic endometrial tissue implantation and growth: Identification of a novel potential target for endometriosis treatment. Am J Pathol. 181:1197–1205. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Quattrone F, Sanchez AM, Pannese M, Hemmerle T, Viganò P, Candiani M, Petraglia F, Neri D and Panina-Bordignon P: The targeted delivery of interleukin 4 inhibits development of endometriotic lesions in a mouse model. Reprod Sci. 22:1143–1152. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Kumar R, Clerc AC, Gori I, Russell R, Pellegrini C, Govender L, Wyss JC, Golshayan D and Canny GO: Lipoxin A4 prevents the progression of de novo and established endometriosis in a mouse model by attenuating prostaglandin E2 production and estrogen signaling. PLoS One. 9:e897422014. View Article : Google Scholar : PubMed/NCBI | |
|
Lee J, Banu SK, Subbarao T, Starzinski-Powitz A and Arosh JA: Selective inhibition of prostaglandin E2 receptors EP2 and EP4 inhibits invasion of human immortalized endometriotic epithelial and stromal cells through suppression of metalloproteinases. Mol Cell Endocrinol. 332:306–313. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Edwards DR, Murphy G, Reynolds JJ, Whitham SE, Docherty AJ, Angel P and Heath JK: Transforming growth factor beta modulates the expression of collagenase and metalloproteinase inhibitor. EMBO J. 6:1899–1904. 1987.PubMed/NCBI | |
|
Osteen KG, Keller NR, Feltus FA and Melner MH: Paracrine regulation of matrix metalloproteinase expression in the normal human endometrium. Gynecol Obstet Invest. 48 Suppl 1:S2–S13. 1999. View Article : Google Scholar | |
|
Braundmeier AG, Fazleabas AT, Lessey BA, Guo H, Toole BP and Nowak RA: Extracellular matrix metalloproteinase inducer regulates metalloproteinases in human uterine endometrium. J Clin Endocrinol Metab. 91:2358–2365. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Bruner KL, Eisenberg E, Gorstein F and Osteen KG: Progesterone and transforming growth factor-beta coordinately regulate suppression of endometrial matrix metalloproteinases in a model of experimental endometriosis. Steroids. 64:648–653. 1999. 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): discussion 340–342. 396–406. 2002. | |
|
Koks CA, Weusten Demir AY, Groothuis PG, Dunselman GA, de Goeij AF and Evers JL: Menstruum induces changes in mesothelial cell morphology. Gynecol Obstet Invest. 50:13–18. 2000. View Article : Google Scholar : PubMed/NCBI | |
|
Zhang J and Salamonsen LA: In vivo evidence for active matrix metalloproteinases in human endometrium supports their role in tissue breakdown at menstruation. J Clin Endocrinol Metab. 87:2346–2351. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Bruner KL, Matrisian LM, Rodgers WH, Gorstein F and Osteen KG: Suppression of matrix metalloproteinases inhibits establishment of ectopic lesions by human endometrium in nude mice. J Clin Invest. 99:2851–2857. 1997. View Article : Google Scholar : PubMed/NCBI | |
|
Malik S, Day K, Perrault I, Charnock-Jones DS and Smith SK: Menstrual effluent in endometriosis shows no difference in volume, VEGF-A, MMP2 and MMP9 or sFLT. Reprod Biomed Online. 12:174–181. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Eisermann J, Gast MJ, Pineda J, Odem RR and Collins JL: Tumor necrosis factor in peritoneal fluid of women undergoing laparoscopic surgery. Fertil Steril. 50:573–579. 1988. View Article : Google Scholar : PubMed/NCBI | |
|
Taketani Y, Kuo TM and Mizuno M: Comparison of cytokine levels and embryo toxicity in peritoneal fluid in infertile women with untreated or treated endometriosis. Am J Obstet Gynecol. 167:265–270. 1992. View Article : Google Scholar : PubMed/NCBI | |
|
Oosterlynck DJ, Meuleman C, Waer M and Koninckx PR: Transforming growth factor-beta activity is increased in peritoneal fluid from women with endometriosis. Obstet Gynecol. 83:287–292. 1994.PubMed/NCBI | |
|
Sotnikova NY, Antsiferova YS, Posiseeva LV, Shishkov DN, Posiseev DV and Filippova ES: Mechanisms regulating invasiveness and growth of endometriosis lesions in rat experimental model and in humans. Fertil Steril. 93:2701–2705. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Gilabert-Estellés J, Ramón LA, España F, Gilabert J, Vila V, Réganon E, Castelló R, Chirivella M and Estellés A: Expression of angiogenic factors in endometriosis: Relationship to fibrinolytic and metalloproteinase systems. Hum Reprod. 22:2120–2127. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Liu H, Wang J, Wang H, Tang N, Li Y, Zhang Y and Hao T: Correlation between matrix metalloproteinase-9 and endometriosis. Int J Clin Exp Pathol. 8:13399–13404. 2015.PubMed/NCBI | |
|
Szamatowicz J, Laudański P and Tomaszewska I: Matrix metalloproteinase-9 and tissue inhibitor of matrix metalloproteinase-1: A possible role in the pathogenesis of endometriosis. Hum Reprod. 17:284–288. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Laudanski P, Szamatowicz J and Ramel P: Matrix metalloproteinase-13 and membrane type-1 matrix metalloproteinase in peritoneal fluid of women with endometriosis. Gynecol Endocrinol. 21:106–110. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Sharpe-Timms KL, Keisler LW, McIntush EW and Keisler DH: Tissue inhibitor of metalloproteinase-1 concentrations are attenuated in peritoneal fluid and sera of women with endometriosis and restored in sera by gonadotropin-releasing hormone agonist therapy. Fertil Steril. 69:1128–1134. 1998. View Article : Google Scholar : PubMed/NCBI | |
|
Sharpe-Timms KL, Zimmer RL, Jolliff WJ, Wright JA, Nothnick WB and Curry TE: Gonadotropin-releasing hormone agonist (GnRH-a) therapy alters activity of plasminogen activators, matrix metalloproteinases, and their inhibitors in rat models for adhesion formation and endometriosis: Potential GnRH-a-regulated mechanisms reducing adhesion formation. Fertil Steril. 69:916–923. 1998. View Article : Google Scholar : PubMed/NCBI | |
|
Ulukus M, Cakmak H and Arici A: The role of endometrium in endometriosis. J Soc Gynecol Investig. 13:467–476. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Collette T, Bellehumeur C, Kats R, Maheux R, Mailloux J, Villeneuve M and Akoum A: Evidence for an increased release of proteolytic activity by the eutopic endometrial tissue in women with endometriosis and for involvement of matrix metalloproteinase-9. Hum Reprod. 19:1257–1264. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Collette T, Maheux R, Mailloux J and Akoum A: Increased expression of matrix metalloproteinase-9 in the eutopic endometrial tissue of women with endometriosis. Hum Reprod. 21:3059–3067. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Di Carlo C, Bonifacio M, Tommaselli GA, Bifulco G, Guerra G and Nappi C: Metalloproteinases, vascular endothelial growth factor, and angiopoietin 1 and 2 in eutopic and ectopic endometrium. Fertil Steril. 91:2315–2323. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Szymanowski K, Mikolajczyk M, Wirstlein P and Dera-Szymanowska A: Matrix metalloproteinase-2 (MMP-2), MMP-9, tissue inhibitor of matrix metalloproteinases (TIMP-1) and transforming growth factor-β2 (TGF-U2) expression in eutopic endometrium of women with peritoneal endometriosis. Ann Agric Environ Med. 23:649–653. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Wenzl RJ and Heinzl H: Localization of matrix metalloproteinase-2 in uterine endometrium and ectopic implants. Gynecol Obstet Invest. 45:253–257. 1998. View Article : Google Scholar : PubMed/NCBI | |
|
Uzan C, Cortez A, Dufournet C, Fauvet R, Siffroi JP and Daraï E: Eutopic endometrium and peritoneal, ovarian and bowel endometriotic tissues express a different profile of matrix metalloproteinases-2, −3 and −11, and of tissue inhibitor metalloproteinases-1 and −2. Virchows Archiv. 445:603–609. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Chung HW, Lee JY, Moon HS, Hur SE, Park MH, Wen Y and Polan ML: Matrix metalloproteinase-2, membranous type 1 matrix metalloproteinase, and tissue inhibitor of metalloproteinase-2 expression in ectopic and eutopic endometrium. Fertil Steril. 78:787–795. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Gilabert-Estellés J, Estellés A, Gilabert J, Castelló R, España F, Falcó C, Romeu A, Chirivella M, Zorio E and Aznar J: Expression of several components of the plasminogen activator and matrix metalloproteinase systems in endometriosis. Hum Reprod. 18:1516–1522. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Ramón L, Gilabert-Estellés J, Castelló R, Gilabert J, España F, Romeu A, Chirivella M, Aznar J and Estellés A: mRNA analysis of several components of the plasminogen activator and matrix metalloproteinase systems in endometriosis using a real-time quantitative RT-PCR assay. Hum Reprod. 20:272–278. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Chung HW, Wen Y, Chun SH, Nezhat C, Woo BH and Polan Lake M: Matrix metalloproteinase-9 and tissue inhibitor of metalloproteinase-3 mRNA expression in ectopic and eutopic endometrium in women with endometriosis: A rationale for endometriotic invasiveness. Fertil Steril. 75:152–159. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
Pan H, Sheng JZ, Tang L, Zhu R, Zhou TH and Huang HF: Increased expression of c-fos protein associated with increased matrix metalloproteinase-9 protein expression in the endometrium of endometriotic patients. Fertil Steril. 90:1000–1007. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Gaetje R, Holtrich U, Engels K, Kourtis K, Cikrit E, Kissler S, Rody A, Karn T and Kaufmann M: Expression of membrane-type 5 matrix metalloproteinase in human endometrium and endometriosis. Gynecol Endocrinol. 23:567–573. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Laudanski P, Charkiewicz R, Kuzmicki M, Szamatowicz J, Świątecka J, Mroczko B and Niklinski J: Profiling of selected angiogenesis-related genes in proliferative eutopic endometrium of women with endometriosis. Eur J Obstet Gynecol Reprod Biol. 172:85–92. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Lu XE, Ning WX, Dong MY, Liu AX, Jin F and Huang HF: Vascular endothelial growth factor and matrix metalloproteinase-2 expedite formation of endometriosis in the early stage ICR mouse model. Fertil Steril. 86 4 Suppl:S1175–S1181. 2006. View Article : Google Scholar | |
|
Cox KE, Piva M and Sharpe-Timms KL: Differential regulation of matrix metalloproteinase-3 gene expression in endometriotic lesions compared with endometrium. Biol Reprod. 65:1297–1303. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
Ueda M, Yamashita Y, Takehara M, Terai Y, Kumagai K, Ueki K, Kanda K, Hung YC and Ueki M: Gene expression of adhesion molecules and matrix metalloproteinases in endometriosis. Gynecol Endocrinol. 16:391–402. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Kokorine I, Nisolle M, Donnez J, Eeckhout Y, Courtoy PJ and Marbaix E: Expression of interstitial collagenase (matrix metalloproteinase-1) is related to the activity of human endometriotic lesions. Fertil Steril. 68:246–251. 1997. View Article : Google Scholar : PubMed/NCBI | |
|
Cominelli A, Chevronnay Gaide HP, Lemoine P, Courtoy PJ, Marbaix E and Henriet P: Matrix metalloproteinase-27 is expressed in CD163+/CD206+ M2 macrophages in the cycling human endometrium and in superficial endometriotic lesions. Mol Hum Reprod. 20:767–775. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Mizumoto H, Saito T, Ashihara K, Nishimura M, Takehara M, Tanaka R, Ito E and Kudo R: Expression of matrix metalloproteinases in ovarian endometriomas: Immunohistochemical study and enzyme immunoassay. Life Sci. 71:259–273. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Shaco-Levy R, Sharabi S, Benharroch D, Piura B and Sion-Vardy N: Matrix metalloproteinases 2 and 9, E-cadherin, and beta-catenin expression in endometriosis, low-grade endometrial carcinoma and non-neoplastic eutopic endometrium. Eur J Obstet Gynecol Reprod Biol. 139:226–232. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Londero AP, Calcagno A, Grassi T, Marzinotto S, Orsaria M, Beltrami CA, Marchesoni D and Mariuzzi L: Survivin, MMP-2, MT1-MMP, and TIMP-2: Their impact on survival, implantation, and proliferation of endometriotic tissues. Virchows Arch. 461:589–599. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Meola J, Rosa e Silva JC, Dentillo DB, da Silva WA Jr, Veiga-Castelli LC, Bernardes LA, Ferriani RA, de Paz CC, Giuliatti S and Martelli L: Differentially expressed genes in eutopic and ectopic endometrium of women with endometriosis. Fertil Steril. 93:1750–1773. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Liu XJ, He YL and Peng DX: Expression of metalloproteinase-9 in ectopic endometrium in women with endometriosis. Di Yi Jun Yi Da Xue Xue Bao. 22:467–469. 2002.PubMed/NCBI | |
|
Gottschalk C, Malberg K, Arndt M, Schmitt J, Roessner A, Schultze D, Kleinstein J and Ansorge S: Matrix metalloproteinases and TACE play a role in the pathogenesis of endometriosis. Adv Exp Med Biol. 477:483–486. 2000. View Article : Google Scholar : PubMed/NCBI | |
|
Ria R, Loverro G, Vacca A, Ribatti D, Cormio G, Roccaro AM and Selvaggi L: Angiogenesis extent and expression of matrix metalloproteinase-2 and −9 agree with progression of ovarian endometriomas. Eur J Clin Invest. 32:199–206. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Nisenblat V, Bossuyt PM, Shaikh R, Farquhar C, Jordan V, Scheffers CS, Mol BW, Johnson N and Hull ML: Blood biomarkers for the non-invasive diagnosis of endometriosis. Cochrane Database Syst Rev: Cd012179. 2016. View Article : Google Scholar | |
|
Salata IM, Stojanovic N, Cajdler-Łuba A, Lewandowski KC and Lewiński A: Gelatinase A (MM-2), gelatinase B (MMP-9) and their inhibitors (TIMP 1, TIMP-2) in serum of women with endometriosis: Significant correlation between MMP-2, MMP-9 and their inhibitors without difference in levels of matrix metalloproteinases and tissue inhibitors of metalloproteinases in relation to the severity of endometriosis. Gynecol Endocrinol. 24:326–330. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Malvezzi H, Aguiar VG, Paz CC, Tanus-Santos JE, Penna IA and Navarro PA: Increased circulating MMP-2 levels in infertile patients with moderate and severe pelvic endometriosis. Reprod Sci. 20:557–562. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Kennedy S: Is there a genetic basis to endometriosis? Semin Reprod Endocrinol. 15:309–318. 1997. View Article : Google Scholar : PubMed/NCBI | |
|
Georgiou I, Syrrou M, Bouba I, Dalkalitsis N, Paschopoulos M, Navrozoglou I and Lolis D: Association of estrogen receptor gene polymorphisms with endometriosis. Fertil Steril. 72:164–166. 1999. View Article : Google Scholar : PubMed/NCBI | |
|
Chang CC, Hsieh YY, Tsai FJ, Tsai CH, Tsai HD and Lin CC: The proline form of p53 codon 72 polymorphism is associated with endometriosis. Fertil Steril. 77:43–45. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Baranova H, Bothorishvilli R, Canis M, Albuisson E, Perriot S, Glowaczower E, Bruhat MA, Baranov V and Malet P: Glutathione S-transferase M1 gene polymorphism and susceptibility to endometriosis in a French population. Mol Hum Reprod. 3:775–780. 1997. View Article : Google Scholar : PubMed/NCBI | |
|
Han YJ, Kim HN, Yoon JK, Yi SY, Moon HS, Ahn JJ, Kim HL and Chung HW: Haplotype analysis of the matrix metalloproteinase-9 gene associated with advanced-stage endometriosis. Fertil Steril. 91:2324–2330. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Saare M, Lamp M, Kaart T, Karro H, Kadastik U, Metspalu A, Peters M and Salumets A: Polymorphisms in MMP-2 and MMP-9 promoter regions are associated with endometriosis. Fertil Steril. 94:1560–1563. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Shan K, Ying W, Jian-Hui Z, Wei G, Na W and Yan L: The function of the SNP in the MMP1 and MMP3 promoter in susceptibility to endometriosis in China. Mol Hum Reprod. 11:423–427. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Shan K, Lian-Fu Z, Hui D, Wei G, Na W, Xia J and Yan L: Polymorphisms in the promoter regions of the matrix metalloproteinases-7, −9 and the risk of endometriosis and adenomyosis in China. Mol Hum Reprod. 12:35–39. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Borghese B, Chiche JD, Vernerey D, Chenot C, Mir O, Bijaoui G, Bonaiti-Pellié C and Chapron C: Genetic polymorphisms of matrix metalloproteinase 12 and 13 genes are implicated in endometriosis progression. Hum Reprod. 23:1207–1213. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Cho YJ, Kim NH, Jeong KA, Lee JY, Moon HS, Kim HL and Chung HW: Association between MMP-2 and TIMP-2 gene polymorphisms and advanced-stage endometriosis in Korean women. Am J Reprod Immunol. 69:73–84. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Kang S, Zhao XW, Wang N, Chen SC, Zhou RM and Li Y: Association of polymorphisms of the MMP-2 and TIMP-2 genes with the risk of endometriosis in North Chinese women. Fertil Steril. 90:2023–2029. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Ye H, He Y, Wang J, Song T, Lan Z, Zhao Y and Xi M: Effect of matrix metalloproteinase promoter polymorphisms on endometriosis and adenomyosis risk: Evidence from a meta-analysis. J Genet. 95:611–619. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Yang H, Liu J, Fan Y, Guo Q, Ge L, Yu N, Zheng X, Dou Y and Zheng S: Associations between various possible promoter polymorphisms of MMPs genes and endometriosis risk: A meta-analysis. Eur J Obstet Gynecol Reprod Biol. 205:174–188. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Xin L, Hou Q, Xiong QI and Ding X: Association between matrix metalloproteinase-2 and matrix metalloproteinase-9 polymorphisms and endometriosis: A systematic review and meta-analysis. Biomed Rep. 3:559–565. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Protopapas A, Markaki S, Mitsis T, Milingos D, Athanasiou S, Haidopoulos D, Loutradis D and Antsaklis A: IImmunohistochemical expression of matrix metalloproteinases, their tissue inhibitors, and cathepsin-D in ovarian endometriosis: Correlation with severity of disease. Fertil Steril. 94:2470–2472. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Stilley JA, Birt JA, Nagel SC, Sutovsky M, Sutovsky P and Sharpe-Timms KL: Neutralizing TIMP1 restores fecundity in a rat model of endometriosis and treating control rats with TIMP1 causes anomalies in ovarian function and embryo development. Biol Reprod. 83:185–194. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Kaya H and Oral B: Effect of ovarian involvement on the frequency of luteinized unruptured follicle in endometriosis. Gynecol Obstet Invest. 48:123–126. 1999. View Article : Google Scholar : PubMed/NCBI | |
|
Shibata T, Makinoda S, Waseda T, Tomizawa H, Fujii R and Utsunomiya T: Granulocyte colony-stimulating factor as a potential inducer of ovulation in infertile women with luteinized unruptured follicle syndrome. Transl Res. 171:63–70. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Fassbender A, Rahmioglu N, Vitonis AF, Viganò P, Giudice LC, D'Hooghe TM, Hummelshoj L, Adamson GD, Becker CM, Missmer SA, et al: World endometriosis research foundation endometriosis phenome and biobanking harmonisation project: IV. Tissue collection, processing, and storage in endometriosis research. Fertil Steril. 102:1244–1253. 2014. View Article : Google Scholar : PubMed/NCBI |
