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Clinical and Experimental Obstetrics & Gynecology  2020, Vol. 47 Issue (2): 147-153    DOI: 10.31083/j.ceog.2020.02.5140
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Extracellular matrix metalloproteinases in the etiopathogenesis of endometriosis: a systematic review and critical appraisal
M. Ζafrakas1, 2, *(), Κ. Κοtronis1, P. Papasozomenou2, P. Eskitzis2, G. Grimbizis1
11st Department of Obstetrics and Gynecology, Medical School, Aristotle University of Thessaloniki, Thessaloniki, Greece
2School of Health Science, International Hellenic University, Thessaloniki, Greece
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Despite extensive research in the field, the etiopathogenesis of endometriosis remains an unresolved enigma. The possible role of different enzymes of the extracellular matrix, in particular the role of the matrix metalloproteases or metalloproteinases (MMPs) in the etiopathogenesis and the mechanisms involved in the processes of benign dissemination of endometriosis have been widely investigated in recent years. Various members of the enzymatic system of the MMPs, as well as their inhibitors, termed tissue inhibitors of metalloproteinases (TIMPs) and their inducer, termed extracellular matrix metalloproteinase inducer (EMMPRIN), have been implicated in the mechanisms involved in endometriosis formation, progression, and maintenance. The aim of the present paper was to provide an overview and critical evaluation of existing experimental evidence on this issue. For this purpose the authors have conducted a systematic review of the literature and evaluated relevant papers regarding experimental animal models, in vitro experiments, and analyses in human samples and studies regarding genetic polymorphisms in humans. In conclusion, members of the system of matrix MMPs, their inhibitors and inducers could be useful as novel diagnostic and prognostic biomarkers in determining the severity of endometriosis and response to therapy. Furthermore, in depth knowledge in this field could possibly lead to the development of more efficient treatment modalities. Future research should focus on the systematic investigation of the entire MMPs system in endometriosis, as well as on the interaction between its members.

Key words:  Endometriosis      Etiopathogenesis      Extracellular matrix metalloproteases      Metalloproteinases      Tissue Inhibitors of metalloproteases      Extracellular matrix metalloproteinase inducer     
Published:  15 April 2020     
*Corresponding Author(s):  M. Ζafrakas     E-mail:

Cite this article: 

M. Ζafrakas, Κ. Κοtronis, P. Papasozomenou, P. Eskitzis, G. Grimbizis. Extracellular matrix metalloproteinases in the etiopathogenesis of endometriosis: a systematic review and critical appraisal. Clinical and Experimental Obstetrics & Gynecology, 2020, 47(2): 147-153.

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Table 1  — Overview of studies in experimental animal models regarding the matrix metalloproteinase (MMP) system.
Publication Animal model MMP-system member(s) Other factors Correlation of MMP
member with endometriosis
Paul et al. [8] Mouse proMMP-9, TIMP-1 Effect of Melatonin Yes / Yes
Paul et al. [9] Mouse MMP-3, MMP-9, TIMP-3 uPA; effect of Melatonin Yes / Yes / Yes
Machado et al. [10] Rat MMP-9 VEGF, Flk-1 Yes
Swarmakar and Paul [11] Mouse MMP-9 Effect of curcumin Yes
Chen et al. [12] Mouse MMP-2 and MMP-9 None Yes / Yes
Lu et al. [13] Mouse MMP-2 VEGF Yes
Wang and Ma [14] Nude mouse MMP-2, TIMP-2 Effects of E2 and progestin Yes / Yes
Bruner-Tran et al. [15] Nude mouse MMP-3, MMP-7 Effects of progesterone Yes / Yes
Bruner-Tran et al. [16] Mouse MMP-3, MMP-7 Effect of tanaproget Yes / Yes
Nothnick and Soloway [17] Mouse TIMP-1 Activated macrophages Yes
Stilley et al. [18] Rat TIMP-1 None Yes
Braundmeier et al. [19] Baboon EMMPRIN, MMPs None Yes / Yes
Table 2  — Overview of in vitro studies and studies in human samples regarding MMP-9.
Publication Type of sample MMP-system member(s) Other factors Correlation with
Chung et al. [20] ET MMP-9, TIMP-3 None Yes / Yes
Collete et al. [21] Cell culture MMP-9, MMP-2, TIMP-1 None Yes / No / Yes
Szymanowski et al. [22] ET, serum MMP-9, MMP-2, TIMP-1 TGF-β2 No / No / No
Collette et al. [23] ET MMP-9, TIMP-1 None Yes / Yes
Liu et al. [24] Serum, PF, ET MMP-9 None Yes
Liu et al. [25] Plasma, PF MMP-9 None Yes
Szamatowitcz et al. [26] PF MMP-9, TIMP-1 None Yes / Yes
Wu et al. [27] PF MMP-9, TIMP-1, TIMP-2 Effects of PGE2 Yes / Yes / Yes
De Sanctis et al. [28] Peripheral blood MMP-9, MMP-3 VEGF-A No / Yes
Salata et al. [29] Serum MMP-9, MMP-2, TIMP-1, TIMP-2 None No /No / No/ No
Yang et al. [30] Cell culture MMP-9 Osteopontin, E2 Yes
Zhang et al. [31] Cell culture MMP-9 Wnt signaling, E2 Yes
Table 3  — Overview of in vitro studies and studies in human samples regarding various members of the matrix metalloproteinase MMP-system other than MMP-9.
Publication Type of Sample MMP-system member(s) Other factors Correlation with
Hudelist et al. [32] ET MMP-1 Interleukin-1 Yes
Hudelist et al. [33] ET MMP-1 ER-alpha, ER-beta Yes
Juhasz-B?ss et al. [34] CAM MMP-1, MMP-2 None Yes / Yes
Huang et al. [35] PF and serum MMP-2 E2 and progesterone Yes
Kim et al. [36] ET MMP-2 VEGF, CD44, Ki-67 Yes
Jana et al. [37] ET MMP-2 VEGF, VEGFR-2, COX-2, vW Yes
Ramón et al. [38] ET MMP-3 uPA Yes
Gilabert-Estellés et al. [39] ET MMP-3, TIMP-1 uPA, PAI-1 Yes / Yes
Gilabert-Estellés et al. [40] PF MMP-3 VEGF, uPA Yes
Matsuzaki et al. [41] ET MMP-7 None Yes
Laudanski et al. [42] PF MMP-13, MMP-14, TIMP-2 None Yes / Yes / No
Gaetje et al. [43] ET MMP-24/25 None Yes
Sharpe-Timms et al. [44] PF, serum TIMP-1 Effect of GnRH-agonists Yes
Smedts et al. [45] ET EMMPRIN None Yes
Table 4  — Overview of studies regarding genetic polymorphisms of the MMP-system in humans.
Publication MMP-system member(s) Correlation with endometriosis
Ferrari et al. [46] MMP-1 and MMP-3 promoters No / No
Borghese et al. [47] MMP-12 and MMP-13 genes Yes, in combination, in superficial lesions
Han et al. [48] MMP-9 haplotypes and SNPs Yes for two haplotypes / No for 4 SNPs
Kang et al. [49] MMP-2, TIMP-2 No / Yes, protective role of TIMP-2
Cho et al. [50] MMP-2, TIMP-2 (10 SNPs) Yes, with advanced endometriosis
Ye et al. [51] MMP-1, MMP-2, MMP-3, MMP-9 Yes, for one MMP-1 polymorphism
Figure 1.  — Diagrammatic representation of the role of different members of the matrix metalloproteases (MMP) enzymatic system in endometriosis formation, maintenance, and progression.

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