Regulation of Uterine Matrix Metalloproteinase-9 and the Role of MicroRNAs

ABSTRACT

Controlled expression of matrix metalloproteinase-9 (MMP9) is vital for normal uterine physiology, whereas abnormal expression of MMP9 is associated with uterine disease. Despite the importance of MMP9 within the uterus, its regulation is poorly understood. In this review, the complex regulation of MMP9 within the uterus is highlighted, and the potential novel role of microRNAs in the regulation of this protease is discussed. Emphasis is placed on the necessity to enhance our understanding of the regulation of MMP9 expression, which may lead to the establishment of novel approaches to counteract misexpression of this protease and the diseases associated with it.

MMP9 - uterus - estrogen - miRNA

REFERENCES

• 1 Nagase H, Woessner Jr J F. Matrix metalloproteinases.  J Biol Chem. 1999;  274 21491-21494
• 2 Sternlicht M D, Werb Z. How matrix metalloproteinases regulate cell behavior.  Annu Rev Cell Dev Biol. 2001;  17 463-516
• 3 Birkedal-Hansen H, Moore W G, Bodden M K et al.. Matrix metalloproteinases: a review.  Crit Rev Oral Biol Med. 1993;  4 197-250
• 4 Gomez D E, Alonso D F, Yoshiji H, Thorgeirsson U P. Tissue inhibitors of metalloproteinases: structure, regulation and biological functions.  Eur J Cell Biol. 1997;  74 111-122
• 5 Brew K, Dinakarpandian D, Nagase H. Tissue inhibitors of metalloproteinases: evolution, structure and function.  Biochim Biophys Acta. 2000;  1477 267-283
• 6 Yoshida S, Matsumoto K, Tomioka D et al.. Recombinant hepatocyte growth factor accelerates cutaneous wound healing in a diabetic mouse model.  Growth Factors. 2004;  22 111-119
• 7 Curry Jr T E, Osteen K G. The matrix metalloproteinase system: changes, regulation, and impact throughout the ovarian and uterine reproductive cycle.  Endocr Rev. 2003;  24 428-465
• 8 Zhang X, Nothnick W B. The role and regulation of the uterine matrix metalloproteinase system in menstruating and non-menstruating species.  Front Biosci. 2005;  10 353-366
• 9 Bany B M, Harvey M B, Schultz G A. Expression of matrix metalloproteinases 2 and 9 in the mouse uterus during implantation and oil-induced decidualization.  J Reprod Fertil. 2000;  120 125-134
• 10 Freitas S, Meduri G, Le Nestour E, Bausero P, Perrot-Applanat M. Expression of metalloproteinases and their inhibitors in blood vessels in human endometrium.  Biol Reprod. 1999;  61 1070-1082
• 11 Vincent A J, Malakooti N, Zhang J, Rogers P A, Affandi B, Salamonsen L A. Endometrial breakdown in women using Norplant is associated with migratory cells expressing matrix metalloproteinases-9 (gelatinase-B).  Hum Reprod. 1999;  14 807-815
• 12 Jeziorska M, Nagase H, Salamonsen L A, Woolley D E. Immunolocalization of the matrix metalloproteinases gelatinase B and stromelysin 1 in human endometrium throughout the menstrual cycle.  J Reprod Fertil. 1996;  107 43-51
• 13 Rawdanowicz T J, Hampton A L, Nagase H, Woolley D E, Salamonsen L A. Matrix metalloproteinase production by cultured human endometrial stromal cells: identification of interstitial collagenase, gelatinase-A, gelatinase-B, and stromelysin-1 and their differential regulation by interleukin-1 alpha and tumor necrosis factor-alpha.  J Clin Endocrinol Metab. 1994;  79 530-536
• 14 Salamonsen L A, Woolley D E. Matrix metalloproteinases in normal menstruation.  Hum Reprod. 1996;  11(Suppl 2) 124-133
• 15 Stygar D, Wang H, Vladic Y S, Ekman G, Eriksson H, Sahlin L. Increased level of matrix metalloproteinases 2 and 9 in the ripening process of the human cervix.  Biol Reprod. 2002;  67 889-894
• 16 Skinner J L, Riley S C, Gebbie A E, Glasier A F, Critchley H O. Regulation of matrix metalloproteinase-9 in endometrium during the menstrual cycle and following administration of intrauterine levonorgestrel.  Hum Reprod. 1999;  14 793-799
• 17 Hickey M, Higham J, Sullivan M, Miles L, Fraser I S. Endometrial bleeding in hormone replacement therapy users: preliminary findings regarding the role of matrix metalloproteinase 9 (MMP9) and tissue inhibitors of MMPs.  Fertil Steril. 2001;  75 288-296
• 18 Vincent A J, Zhang J, Ostor A et al.. Decreased tissue inhibitor of metalloproteinase in the endometrium of women using depot medroxyprogesterone acetate: a role for altered endometrial matrix metalloproteinase/tissue inhibitor of metalloproteinase balance in the pathogenesis of abnormal uterine bleeding?.  Hum Reprod. 2002;  17 1189-1198
• 19 Galant C, Berliere M, Dubois D et al.. Focal expression and final activity of matrix metalloproteinases may explain irregular dysfunctional endometrial bleeding.  Am J Pathol. 2004;  165 83-94
• 20 Chung H W, Wen Y, Chun S H, Nezhat C, Woo B H, Lake Polan 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. 2001;  75 152-159
• 21 Szamatowicz J, Laudanski P, Tomaszewska I. Matrix metalloproteinase-9 and tissue inhibitor of matrix metalloproteinase-1: a possible role in the pathogenesis of endometriosis.  Hum Reprod. 2002;  17 284-288
• 22 Collette T, Bellehumeur C, Kats R et al.. 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. 2004;  19 1257-1264
• 23 Collette T, Maheux R, Mailloux J, Akoum A. Increased expression of matrix metalloproteinase-9 in the eutopic endometrial tissue of women with endometriosis.  Hum Reprod. 2006;  21 3059-3067
• 24 Inagaki N, Stern C, McBain J, Lopata A, Kornman L, Wilkinson D. Analysis of intra-uterine cytokine concentration and matrix metalloproteinase activity in women with recurrent failed embryo transfer.  Hum Reprod. 2003;  18 608-615
• 25 Inagaki N, Ung L, Otani T, Wilkinson D, Lopata A. Uterine cavity matrix metalloproteinases and cytokines in patients with leiomyoma, adenomyosis or endometrial polyp.  Eur J Obstet Gynecol Reprod Biol. 2003;  111 197-203
• 26 Soini Y, Alarakkola E, Autio-Harmainen H. Expression of messenger RNAs for metalloproteinases 2 and 9, type IV collagen, and laminin in non-neoplastic and neoplastic endometrium.  Hum Pathol. 1997;  28 220-226
• 27 Di Nezza L A, Misajon A, Zhang J et al.. Presence of active gelatinases in endometrial carcinoma and correlation of matrix metalloproteinase expression with increasing tumor grade and invasion.  Cancer. 2002;  94 1466-1475
• 28 Lopata A, Agresta F, Quinn M A, Smith C, Ostor A G, Salamonsen L A. Detection of endometrial cancer by determination of matrix metalloproteinases in the uterine cavity.  Gynecol Oncol. 2003;  90 318-324
• 29 Aglund K, Rauvala M, Puistola U et al.. Gelatinases A and B (MMP-2 and MMP9) in endometrial cancer – MMP9 correlates to the grade and the stage.  Gynecol Oncol. 2004;  94 699-704
• 30 Kamat A A, Feng S, Agoulnik I U et al.. The role of relaxin in endometrial cancer.  Cancer Biol Ther. 2006;  5 71-77
• 31 Chantrain C F, Shimada H, Jodele S et al.. Stromal matrix metalloproteinase-9 regulates the vascular architecture in neuroblastoma by promoting pericyte recruitment.  Cancer Res. 2004;  64 1675-1686
• 32 Ueno H, Yamashita K, Azumano I, Inoue M, Okada Y. Enhanced production and activation of matrix metalloproteinase-7 (matrilysin) in human endometrial carcinomas.  Int J Cancer. 1999;  84 470-477
• 33 Marbaix E, Donnez J, Courtoy P J, Eeckhout Y. Progesterone regulates the activity of collagenase and related gelatinases A and B in human endometrial explants.  Proc Natl Acad Sci U S A. 1992;  89 11789-11793
• 34 Cornet P B, Galant C, Eeckhout Y, Courtoy P J, Marbaix E, Henriet P. Regulation of matrix metalloproteinase-9/gelatinase B expression and activation by ovarian steroids and LEFTY-A/endometrial bleeding-associated factor in the human endometrium.  J Clin Endocrinol Metab. 2005;  90 1001-1011
• 35 Van den Steen P E, Dubois B, Nelissen I, Rudd P M, Dwek R A, Opdenakker G. Biochemistry and molecular biology of gelatinase B or matrix metalloproteinase-9 (MMP9).  Crit Rev Biochem Mol Biol. 2002;  37 375-536
• 36 Zhang X, Christenson L K, Nothnick W B. Regulation of MMP9 expression and activity in the mouse uterus by estrogen.  Mol Reprod Dev. 2007;  74 321-331
• 37 Ambros V. The function of animal microRNAs.  Nature. 2004;  431 350-355
• 38 Bartel D P. MicroRNAs: genomics, biogenesis, mechanism and function.  Cell. 2004;  116 281-297
• 39 He L, Hannon G J. MicroRNAs: small RNAs with a big role in gene regulation.  Nat Rev Genet. 2004;  5 522-531
• 40 Valencia-Sanchez M A, Liu J, Hannon G J, Parker R. Control of translation and mRNA degradation by miRNAs and siRNAs.  Genes Dev. 2006;  20 515-524
• 41 Iorio M V, Ferracin M, Liu C G et al.. MicroRNA gene expression deregulation in human breast cancer.  Cancer Res. 2005;  65 7065-7070
• 42 Calin G A, Croce C M. MicroRNA-cancer connection: the beginning of a new tale.  Cancer Res. 2006;  66 7390-7394
• 43 Thomson J M, Newman M, Parker J S, Morin-Kensicki E M, Wright T, Hammond S M. Extensive post-transcriptional regulation of microRNAs and its implications for cancer.  Genes Dev. 2006;  20 2202-2207
• 44 Saito Y, Liang G, Egger G et al.. Specific activation of microRNA-127 with down regulation of the proto-oncogne BCL6 by chromatin-modifying drugs in human cancer cells.  Cancer Cell. 2006;  9 435-443