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Review Open Access

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
  • View Affiliations / Copyright

    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
    Copyright: © Bałkowiec et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
  • Pages: 3123-3136
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    Published online on: July 23, 2018
       https://doi.org/10.3892/mmr.2018.9303
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Abstract

Aberrant regulation of matrix metalloproteinases (MMPs) may be the primary cause of endometrial lesion formation in a group of predisposed women. Prospect for the genuine origin of endometriosis is ongoing, since retrograde menstruation leads to presence of endometrial debris in peritoneal cavity of many women, which do not experience endometriosis. Tissue remodeling is regulated precisely by a balance of MMPs and their inhibitors. Interplay between factors enhancing and suppressing matrix turnover is crucial for cyclic preparation of endometrium for embryo implantation, and endometrial shedding and renewal in physiology of primates. Disorders of the regulation of matrix remodeling leads to augmentation of implantation and invasive growth of ectopic endometrial tissue. Moreover, endometriosis‑induced changes in the matrix balance leads to adhesion formation, ovulatory dysfunction and fertility impairment. The review summarizes the current knowledge regarding the regulation of extracellular matrix turnover in the physiology of the endometrial cycle and in the development of endometriosis, as well as the pathophysiology of ovulatory dysfunction in endometriotic women. Therapeutic modalities utilizing modulation of tissue remodeling were discussed.
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1 

Burney RO and Giudice LC: Pathogenesis and pathophysiology of endometriosis. Fertil Steril. 98:511–519. 2012. View Article : Google Scholar : PubMed/NCBI

2 

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

3 

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

4 

BRENDA: The Comprehensive Enzyme Information System. https://www.brenda-enzymes.org

5 

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

6 

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

7 

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

8 

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

9 

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

10 

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

11 

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

12 

Matrisian LM: The matrix-degrading metalloproteinases. Bioessays. 14:455–463. 1992. View Article : Google Scholar : PubMed/NCBI

13 

Murphy G: Tissue inhibitors of metalloproteinases. Genome Biol. 12:2332011. View Article : Google Scholar : PubMed/NCBI

14 

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

15 

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

16 

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

17 

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

18 

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

19 

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

20 

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

21 

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

22 

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

23 

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.

24 

Gezer A and Oral E: Progestin therapy in endometriosis. Womens Health (Lond). 11:643–652. 2015. View Article : Google Scholar : PubMed/NCBI

25 

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

26 

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

27 

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

28 

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

29 

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

30 

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

31 

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

32 

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

33 

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

34 

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

35 

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

36 

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

37 

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

38 

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

39 

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

40 

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

41 

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

42 

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

43 

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

44 

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

45 

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

46 

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

47 

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

48 

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

49 

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

50 

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.

51 

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

52 

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

53 

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

54 

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

55 

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

56 

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

57 

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

58 

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

59 

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

60 

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

61 

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

62 

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

63 

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

64 

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

65 

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

66 

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

67 

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

68 

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

69 

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

70 

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

71 

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

72 

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

73 

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

74 

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

75 

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

76 

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

77 

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

78 

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

79 

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

80 

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

81 

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

82 

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

83 

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

84 

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

85 

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

86 

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

87 

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

88 

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

89 

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

90 

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

91 

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

92 

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

93 

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

94 

Kennedy S: Is there a genetic basis to endometriosis? Semin Reprod Endocrinol. 15:309–318. 1997. View Article : Google Scholar : PubMed/NCBI

95 

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

96 

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

97 

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

98 

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

99 

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

100 

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

101 

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

102 

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

103 

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

104 

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

105 

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

106 

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

107 

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

108 

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

109 

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

110 

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

111 

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

112 

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

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Copy and paste a formatted citation
Spandidos Publications style
Bałkowiec M, Maksym RB and Włodarski PK: The bimodal role of matrix metalloproteinases and their inhibitors in etiology and pathogenesis of endometriosis (Review). Mol Med Rep 18: 3123-3136, 2018.
APA
Bałkowiec, M., Maksym, R.B., & Włodarski, P.K. (2018). The bimodal role of matrix metalloproteinases and their inhibitors in etiology and pathogenesis of endometriosis (Review). Molecular Medicine Reports, 18, 3123-3136. https://doi.org/10.3892/mmr.2018.9303
MLA
Bałkowiec, M., Maksym, R. B., Włodarski, P. K."The bimodal role of matrix metalloproteinases and their inhibitors in etiology and pathogenesis of endometriosis (Review)". Molecular Medicine Reports 18.3 (2018): 3123-3136.
Chicago
Bałkowiec, M., Maksym, R. B., Włodarski, P. K."The bimodal role of matrix metalloproteinases and their inhibitors in etiology and pathogenesis of endometriosis (Review)". Molecular Medicine Reports 18, no. 3 (2018): 3123-3136. https://doi.org/10.3892/mmr.2018.9303
Copy and paste a formatted citation
x
Spandidos Publications style
Bałkowiec M, Maksym RB and Włodarski PK: The bimodal role of matrix metalloproteinases and their inhibitors in etiology and pathogenesis of endometriosis (Review). Mol Med Rep 18: 3123-3136, 2018.
APA
Bałkowiec, M., Maksym, R.B., & Włodarski, P.K. (2018). The bimodal role of matrix metalloproteinases and their inhibitors in etiology and pathogenesis of endometriosis (Review). Molecular Medicine Reports, 18, 3123-3136. https://doi.org/10.3892/mmr.2018.9303
MLA
Bałkowiec, M., Maksym, R. B., Włodarski, P. K."The bimodal role of matrix metalloproteinases and their inhibitors in etiology and pathogenesis of endometriosis (Review)". Molecular Medicine Reports 18.3 (2018): 3123-3136.
Chicago
Bałkowiec, M., Maksym, R. B., Włodarski, P. K."The bimodal role of matrix metalloproteinases and their inhibitors in etiology and pathogenesis of endometriosis (Review)". Molecular Medicine Reports 18, no. 3 (2018): 3123-3136. https://doi.org/10.3892/mmr.2018.9303
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