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Metalloproteinase-Dependent Shedding of Low-Density Lipoprotein Receptor-Related Protein-1 Ectodomain Decreases Endocytic Clearance of Endometrial Matrix Metalloproteinase-2 and -9 at Menstruation

Selvais, Charlotte, Gaide Chevronnay, Héloïse P., Lemoine, Pascale, Dedieu, Stéphane, Henriet, Patrick, Courtoy, Pierre J., Marbaix, Etienne, Emonard, Hervé·2009·Endocrinology

Abstract

Cyclic elimination of the endometrium functional layer through menstrual bleeding results from intense tissue breakdown by proteolytic enzymes, mainly members of the matrix metalloproteinase (MMP) family. In contrast to menstrual-restricted MMPs, e.g. interstitial collagenase (MMP-1), gelatinases A (MMP-2) and B (MMP-9) mRNAs are abundant throughout the cycle without detectable tissue degradation at proliferative and secretory phases, implying a tight posttranslational control of both gelatinases. This paper addresses the role of low-density lipoprotein receptor-related protein (LRP)-1 in the endocytic clearance of endometrial gelatinases. LRP-1 mRNA and protein were studied using RT-PCR, Western blotting, and immunolabeling. Posttranslational control of LRP-1 was analyzed in explant culture. The receptor-associated protein (RAP), used as LRP antagonist, strongly increased (pro)gelatinase accumulation in medium conditioned by endometrial explants, suggesting a role for LRP-1 in their clearance. Although LRP-1 mRNA remained constant throughout the cycle, the protein ectodomain vanished at menses. LRP-1 immunolabeling selectively disappeared in areas of extracellular matrix breakdown in menstrual samples. It also disappeared from explants cultured without estrogen and progesterone (EP) due to ectodomain shedding in the medium. The shedding was inhibited by metalloproteinase inhibitors, including a disintegrin and metalloproteinase (ADAM) inhibitor, and by tissue inhibitors of MMPs (TIMP)-3 and -2, but barely by TIMP-1, pointing to ADAM-12 as the putative sheddase. In good agreement, ADAM-12 mRNA expression was repressed by EP. In conclusion, the efficient LRP-1-mediated clearance of gelatinase activity in nonbleeding endometrium is abrogated upon EP withdrawal, due to shedding of LRP-1 ectodomain by a metalloproteinase, presumably ADAM-12, itself regulated by EP.

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Research works printed but not linked: 37

  1. Marastoni, 2008, Extracellular matrix: a matter of life and death., Connect Tissue Res, 49, 203, 10.1080/03008200802143190 · DOI
  2. Marbaix, 1995, The expression of interstitial collagenase in human endometrium is controlled by progesterone and by oestradiol and is related to menstruation., Biochem J, 305, 1027, 10.1042/bj3051027 · DOI
  3. Vassilev, 2005, Response of matrix metalloproteinases and tissue inhibitors of metalloproteinases messenger ribonucleic acids to ovarian steroids in human endometrial explants mimics their gene- and phase-specific differential control in vivo., J Clin Endocrinol Metab, 90, 5848, 10.1210/jc.2005-0762 · DOI
  4. Singer, 1997, Paracrine stimulation of interstitial collagenase (MMP-1) in the human endometrium by interleukin 1α and its dual block by ovarian steroids., Proc Natl Acad Sci USA, 94, 10341, 10.1073/pnas.94.19.10341 · DOI
  5. Pretto, 2008, Production of interleukin-1α by human endometrial stromal cells is triggered during menses and dysfunctional bleeding and is induced in culture by epithelial interleukin-1α released upon ovarian steroids withdrawal., J Clin Endocrinol Metab, 93, 4126, 10.1210/jc.2007-2636 · DOI
  6. Cornet, 2002, Regulation and function of LEFTY-A/EBAF in the human endometrium. mRNA expression during the menstrual cycle, control by progesterone, and effect on matrix metalloproteinases., J Biol Chem, 277, 42496, 10.1074/jbc.M201793200 · DOI
  7. Bruner, 1995, Transforming growth factor β mediates the progesterone suppression of an epithelial metalloproteinase by adjacent stroma in the human endometrium., Proc Natl Acad Sci USA, 92, 7362, 10.1073/pnas.92.16.7362 · DOI
  8. Nagase, 1997, Activation mechanisms of matrix metalloproteinases., Biol Chem, 378, 151
  9. Berton, 2007, Binding of matrilysin-1 to human epithelial cells promotes its activity., Cell Mol Life Sci, 64, 610, 10.1007/s00018-007-6415-5 · DOI
  10. Brew, 2000, Tissue inhibitors of metalloproteinases: evolution, structure and function., Biochim Biophys Acta, 1477, 267, 10.1016/S0167-4838(99)00279-4 · DOI
  11. Emonard, 2005, Regulation of matrix metalloproteinase (MMP) activity by the low-density lipoprotein receptor-related protein (LRP). A new function for an “old friend.”, Biochimie (Paris), 87, 369, 10.1016/j.biochi.2004.11.013 · DOI
  12. Willnow, 1996, The low-density lipoprotein receptor-related protein (LRP) is processed by furin in vivo and in vitro., Biochem J, 313, 71, 10.1042/bj3130071 · DOI
  13. Lillis, 2008, LDL receptor-related protein 1: unique tissue-specific functions revealed by selective gene knockout studies., Physiol Rev, 88, 887, 10.1152/physrev.00033.2007 · DOI · Paper page
  14. Emonard, 2004, Low density lipoprotein receptor-related protein mediates endocytic clearance of pro-MMP-2.TIMP-2 complex through a thrombospondin-independent mechanism., J Biol Chem, 279, 54944, 10.1074/jbc.M406792200 · DOI
  15. Bu, 1998, RAP, a novel type of ER chaperone., Trends Cell Biol, 8, 272, 10.1016/S0962-8924(98)01283-5 · DOI · Paper page
  16. Rozanov, 2004, The low density lipoprotein receptor-related protein LRP is regulated by membrane type-1 matrix metalloproteinase (MT1-MMP) proteolysis in malignant cells., J Biol Chem, 279, 4260, 10.1074/jbc.M311569200 · DOI · Paper page
  17. Quinn, 1997, Soluble low density lipoprotein receptor-related protein (LRP) circulates in human plasma., J Biol Chem, 272, 23946, 10.1074/jbc.272.38.23946 · DOI
  18. Quinn, 1999, Characterization of the soluble form of the low density lipoprotein receptor-related protein (LRP)., Exp Cell Res, 251, 433, 10.1006/excr.1999.4590 · DOI · Paper page
  19. Polavarapu, 2007, Tissue-type plasminogen activator-mediated shedding of astrocytic low-density lipoprotein receptor-related protein increases the permeability of the neurovascular unit., Blood, 109, 3270, 10.1182/blood-2006-08-043125 · DOI
  20. Raucci, 2008, A soluble form of the receptor for advanced glycation endproducts (RAGE) is produced by proteolytic cleavage of the membrane-bound form by the sheddase a disintegrin and metalloprotease 10 (ADAM10)., FASEB J, 22, 3716, 10.1096/fj.08-109033 · DOI
  21. Kodama, 2004, ADAM12 is selectively overexpressed in human glioblastomas and is associated with glioblastoma cell proliferation and shedding of heparin-binding epidermal growth factor., Am J Pathol, 165, 1743, 10.1016/S0002-9440(10)63429-3 · DOI
  22. Okada, 2008, ADAM-12 (meltrin α) is involved in chondrocyte proliferation via cleavage of insulin-like growth factor binding protein 5 in osteoarthritic cartilage., Arthritis Rheum, 58, 778, 10.1002/art.23262 · DOI
  23. Zatovicova, 2005, Ectodomain shedding of the hypoxia-induced carbonic anhydrase IX is a metalloprotease-dependent process regulated by TACE/ADAM17., Br J Cancer, 93, 1267, 10.1038/sj.bjc.6602861 · DOI
  24. Goffin, 2003, Expression pattern of metalloproteinases and tissue inhibitors of matrix-metalloproteinases in cycling human endometrium., Biol Reprod, 69, 976, 10.1095/biolreprod.103.015933 · DOI
  25. Cornet, 2005, 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, 90, 1001, 10.1210/jc.2004-1277 · DOI
  26. Rigot, 2001, In vivo perimenstrual activation of progelatinase B (proMMP-9) in the human endometrium and its dependence on stromelysin 1 (MMP-3) ex vivo., Biochem J, 358, 275, 10.1042/bj3580275 · DOI
  27. Foca, 2000, Differential expression of the α2-macroglobulin receptor and the receptor associated protein in normal human endometrium and endometrial carcinoma., Mol Hum Reprod, 6, 921, 10.1093/molehr/6.10.921 · DOI
  28. Sayegh, 1995, Immunohistochemical localization of α-2 macroglobulin receptor/low-density lipoprotein receptor-related protein, receptor-associated protein, and Gp330 in the human endometrium., J Soc Gynecol Invest, 2, 748
  29. Troeberg, 2002, E. coli expression of TIMP-4 and comparative kinetic studies with TIMP-1 and TIMP-2: insights into the interactions of TIMPs and matrix metalloproteinase 2 (gelatinase A)., Biochemistry, 41, 15025, 10.1021/bi026454l · DOI
  30. Kashiwagi, 2001, TIMP-3 is a potent inhibitor of aggrecanase 1 (ADAM-TS4) and aggrecanase 2 (ADAM-TS5)., J Biol Chem, 276, 12501, 10.1074/jbc.C000848200 · DOI
  31. Marbaix, 1996, Menstrual breakdown of human endometrium can be mimicked in vitro and is selectively and reversibly blocked by inhibitors of matrix metalloproteinases., Proc Natl Acad Sci USA, 93, 9120, 10.1073/pnas.93.17.9120 · DOI
  32. Cornillie, 1991, Lysosomal enzymes in the human endometrium: a biochemical study in untreated and levonorgestrel-treated women., Contraception, 43, 387, 10.1016/0010-7824(91)90076-R · DOI
  33. Fröhlich, 2006, Molecular profiling of ADAM12 in human bladder cancer., Clin Cancer Res, 12, 7359, 10.1158/1078-0432.CCR-06-1066 · DOI
  34. Gaide Chevronnay, 2008, Opposite regulation of transforming growth factors-β2 and -β3 expression in the human endometrium., Endocrinology, 149, 1015, 10.1210/en.2007-0849 · DOI
  35. Marzolo, 2003, Differential distribution of low-density lipoprotein-receptor-related protein (LRP) and megalin in polarized epithelial cells is determined by their cytoplasmic domains., Traffic, 4, 273, 10.1034/j.1600-0854.2003.00081.x · DOI · Paper page
  36. Rocks, 2008, Emerging roles of ADAM and ADAMTS metalloproteinases in cancer., Biochimie (Paris), 90, 369, 10.1016/j.biochi.2007.08.008 · DOI
  37. Jacobsen, 2008, Catalytic properties of ADAM12 and its domain deletion mutants., Biochemistry, 47, 537, 10.1021/bi701629c · DOI

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Metadata

Authors
Selvais, C., Gaide Chevronnay, H. P., Lemoine, P., Dedieu, S., Henriet, P., Courtoy, P. J., Marbaix, E., & Emonard, H.
Affiliations
  • Cell Biology Unit (C.S., H.P.G.C., P.L., P.H., P.J.C., E.M.), Université catholique de Louvain, B-1200 Brussels, Belgium
  • Centre National de la Recherche Scientifique, Unité Mixte de Recherche 6237, Matrice Extracellulaire et Dynamique Cellulaire (MEDyC) (S.D., H.E.), University of Reims Champagne-Ardenne, F-51100 Reims, France
Venue
Endocrinology
Published
2009-04-30
Volume
150
Issue
8
Pages
3792-3799
ISSN
  • 0013-7227
  • 1945-7170
Cited by
54
References
1
Language
en

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