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Matrix metalloproteinases and their tissue inhibitors in endometrial remodelling and menstruation

  • Lois A Salamonsen (a1) and David E Woolley (a2)

Extract

The architecture of the human endometrium is extensively remodelled during the course of each normal menstrual cycle, unlike most other tissues and organs which undergo very little change during adult life. During menstruation, when loss of most of the functionalis layer occurs, there is concomitant epithelial regrowth; repair of the luminal surface is complete almost as bleeding ceases. During the proliferative phase of the cycle and under the influence of rising oestrogen levels, the stromal cells, glands and blood vessels undergo rapid proliferation which results in tissue thickening. Following ovulation (around day 14 of the idealized 28-day cycle), the secretory phase of the cycle is characterized by increasing tortuosity of the spiral arterioles and glands and increased glandular secretory activity. After about day 22, decidualization of many of the stromal fibroblasts also occurs, the resultant decidual cells having many characteristics typical of epithelial cells. Periods of tissue oedema are apparent both in mid-proliferative (days 8–11) and mid-secretory (days 20–23) endometrium. Late in the cycle, there is regression of the tissue as menstruation is initiated.

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Corresponding author

Prince Henry's Institute of Medical Research, PO Box 5152, Clayton, Victoria 3186, Australia.

References

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1Ludwig, H, Spornitz, UM. Microarchitecture of the endometrium by scanning electron microscopy: menstrual desquamation and remodelling. Ann N Y Acad Sci 1991; 622: 2846.
2Markee, JE. Menstruation in intraocular endometrial transplants in the rhesus monkey. Contrib Embryol 1940; 177: 220320.
3Roberts, DK, Parmley, TH, Walker, NJ, Horbelt, DV. Ultrastructure of the microvasculature in the human endometrium throughout the normal menstrual cycle. Am J Obstet Gynecol 1992; 166: 1393–406.
4Aplin, JD, Charlton, AK, Ayad, S. An immunohistochemical study of human endometrial extracellular matrix during the menstrual cycle and the first trimester of pregnancy. Cell Tissue Res 1988; 253: 231–40.
5Aplin, JD. Cellular biochemistry of the endometrium. In Wynn, RM, Jollie, WP eds. Biology of the uterus. New York, NY: Plenum Medical Book Co, 1989: 89129.
6Karkavelas, G, Kefalides, NA, Amenta, PS, Martinez-Hernandez, A. Comparative ultrastructural localization of collagen types III, IV, VI and laminin in rat uterus and kidney. J Ultrastruct Mol Struct Res 1988; 100: 137–55.
7Fleischmajer, R, Jacobs, L, Perlish, JS, Katchen, B, Schwartz, E, Timpl, R. Immunochemical analysis of human kidney reticulin. Am J Pathol 1992; 140: 1225–35.
8Woessner, JF Jr. Uterus, cervix and ovary. In: Weiss, JB, Jayson, MIV eds. Collagen in health and disease. Edinburgh: Churchill Livingstone, 1982: 506–27.
9Gross, J, Nagai, Y. Specific degradation of the collagen molecule by tadpole collagenolytic enzyme. Proc Natl Acad Sci USA 1965; 54: 1197–204.
10Birkedal-Hansen, H, Moore, WGI, Bodden, MK et al. Matrix metalloproteinases: a review. Crit Rev Oral Biol Med 1993; 4: 199250.
11Nagase, H. Matrix metalloproteinases 1, 2, and 3: substrate specificities and activation mechanisms. In: Leppert, PC, Woessner, JF Jr eds. The extracellular matrix of the uterus, cervix and fetal membranes: synthesis, degradation and hormonal regulation. Ithaca: Perinatology Press, 1991: 2844.
12Denhardt, DT, Feng, B, Edwards, DR, Cocuzzi, ET, Malyankar, UM. Tissue inhibitor of metalloproteinases (TIMP, aka EPA): structure, control of expression and biological functions. Pharmacol Ther 1993; 59: 329–41.
13Hampton, AL, Salamonsen, LA. Endometrial expression of messenger ribonucleic acid encoding matrix metalloproteinases and their tissue inhibitors coincides with menstruation. J Endocrinol 1994; 141: R1R3.
14Rodgers, WH, Osteen, KG, Matrisian, LM, Navre, M, Guidice, LC, Gorstein, F. Expression and localisation of matrilysin, a matrix metalloproteinase, in human endometrium during the reproductive cycle. Am J Obstet Gynecol 1993; 168: 253–60.
15Irwin, JC, Kirk, D, Gwatkin, RBL, Navre, M, Cannon, P, Guidice, LC. Human endometrial matrix metalloproteinase-2, a putative menstrual proteinase. Hormonal regulation in cultured stromal cells and messenger RNA expression during the menstrual cycle. J Clin Invest 1966; 97: 438–47.
16McLennan, CE, Rydell, AH. Extent of endometrial shedding during normal menstruation. Obstet Gynecol 1965; 26: 605–21.
17Higuchi, T, Kanzaki, H, Nakayama, H. Induction of tissue inhibitor of metalloproteinase 3 gene expression during in vitro decidualization of human endometrial stromal cells. Endocrinology 1995; 136: 4973–81.
18Rodgers, WH, Matrisian, LM, Guidice, LC et al. Patterns of matrix metalloproteinase expression in cycling endometrium imply differential functions and regulation by steroid hormones. J Clin Invest 1994; 94: 946–53.
19Saarialho-Kere, UK, Crouch, EC, Parks, WC. The matrix metalloproteinase matrilysin is constitutively expressed in adult human exocrine epithelium. J Invest Dermatol 1995; 105: 190–96.
20Wilson, CL, Heppner, KJ, Rudolph, LA, Matrisian, LM. The metalloproteinase matrilysin is preferentially expressed in epithelial cells in a tissue-restricted pattern in the mouse. Mol Biol Cell 1995; 6: 851–69.
21Sato, H, Takino, T, Okada, Y et al. A matrix metalloproteinase expressed on the surface of invasive tumour cells. Nature 1994; 370: 6165.
22Takino, T, Sato, H, Shinagawa, A, Seiki, M. Identification of the second membrane-type matrb metalloproteinase (MT-MMP-2) gene from a human placenta cDNA library. MT-MMPs form a unique membrane-type subclass in the MMP family. J Biol Chem 1995; 270: 23013–20.
23Sato, H, Takino, T, Kinoshita, T, Imai, K, Stetler, Stevenson WG, Seiki, M. Cell surface binding and activation of gelatinase A induced by expression of membrane-type-1-matrix metalloproteinase (MTI-MMP). FEBS Lett 1996; 385: 238–40.
24Will, H, Atkinson, SJ, Butler, GS, Smith, B, Murphy, G. The soluble catalytic domain of membrane type 1 matrix metalloproteinase cleaves the propeptide of progelatinase A and initiates autoproteolytic activation. J Biol Chem 1996; 271: 17119–23.
25Brenner, RM, Rudolph, L, Matrisian, L, Slayden, OD. Non human primate models: artificial menstrual cycles, endometrial matrix metalloproteinases and subcutaneous endometrial grafts. Human Reprod 1996; 11 [Suppl 2]: 150–64.
26Jeziorska, M, Nagase, H, Salamonsen, LA, Woolley, DE. Immunolocalization of the matrix metalloproteinases, gelatinase B and stromelysin-1 in human endometrium throughout the menstrual cycle. J Reprod Fertil 1996; 107: 4351.
27Salamonsen, LA, Woolley, DE. Matrix metalloproteinases in normal menstruation. Human Reprod 1996; 11 [Suppl 2]: 124–33.
28Marbaix, E, Kokorine, I, Moulin, P, Donnez, J, Eeckhout, Y, Courtoy, PJ. 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 1996; 93: 9120–25.
29Marbaix, E, Donnez, J, Courtoy, PJ, Eeckhout, Y. Progesterone regulates the activity of collagenase and related gelatinases A and B in human endometrial explants. Proc Natl Acad Sci USA 1992; 89: 11789–93.
30Rawdanowicz, TJ, Hampton, AL, Nagase, H, Woolley, DE, Salamonsen, LA. Matrix metalloproteinase secretion by cultured human endometrial stromal cells: identification of interstitial collagenase, gelatinase A, gelatinase B and stromelysin 1. Differential regulation by interleukin-1α and tumor necrosis factor β. J Clin Endocrinol Metab 1994; 79: 530–36.
31Salamonsen, LA, Butt, AR, Hammond, FR, Garcia, S, Zhang, J. Production of endometrial matrix metalloproteinases but not their tissue inhibitors is modulated by progesterone withdrawal in an in vitro model for menstruation. J Clin Endo Metab 1997; in press.
32Findlay, JK. Future directions for research on endometrial bleeding. Human Reprod 1996; 11 [Suppl 2]: 179–83.
33Ludwig, H. The morphologic response of the human endometrium to long-term treatment with progestational agents. Am J Obstet Gynecol 1982; 142: 796808.
34Jeffrey, JJ, Coffey, RJ, Eisen, AZ. Studies on uterine collagenase in tissue culture. II. Effect of steroid hormones on enzyme production. Biochim Biophys Acta 1971; 252: 143–50.
35Jeffrey, JJ, Koob, TJ. Hormonal regulation of collagen catabolism in the uterus. In: Endocrinology; Excerpta Medica Int Congr Ser 1973; 273: 1115–23.
36Wilcox, BD, Rydelek-Fitzgerald, L, Jeffrey, JJ. Regulation of collagenase gene expression by serotonin and progesterone in rat uterine smooth muscle cells. J Biol Chem 1992; 267: 20752–57.
37Sato, T, Ito, A, Mori, Y, Yamashita, K, Hayakawa, T, Nagase, H. Hormonal regulation of collagenolysis in uterine cervical fibroblasts. Biochem J 1991; 275: 645–50.
38Salamonsen, LA. matrix metalloproteinases and their tissue inhibitors in endocrinology. Trends Endocrinol 1996; 7: 2834.
39Lessey, BA, Killam, AP, Metzger, DA, Haney, AF, Greene, GI, McCarty, KS Jr. Immunohistochemical analysis of human uterine estrogen and progesterone receptors throughout the menstrual cycle. J Clin Endocrinol Metab 1988; 67: 334–40.
40Lydon, JP, DeMayo, FJ, Funk, CR et al. Mice lacking progesterone receptor exhibit pleiotropic reproductive abnormalities. Genes Dev 1995; 9: 2266–78.
41Marbaix, E, Kokorine, I, Henriet, P, Donnez, J, Courtoy, PJ, Eeckhout, Y. The expression of interstitial collagenase in human endometrium is controlled by progesterone and by oestradiol and is related to menstruation. Biochem J 1995; 305: 1027–30.
42Schatz, F, Papp, C, Toth-Pal, E, Lockwood, CJ. Ovarian steroid-modulated stromelysin-l expression in human endometrial stromal and decidual cells. J Clin Endocrinol Metab 1994; 78: 1467–72.
43Finn, CA. Implantation, menstruation and inflammation. Biol Rev 1986; 61: 313–28.
44Finn, CA. The adaptive significance of menstruation: the meaning of menstruation. Hum Reprod 1994; 9: 1202–207.
45Brenner, RM, Slayden, OD. Cyclic changes in the primate oviduct and endometrium. In: Knobil, E ed. The physiology of reproduction, 2nd edn. New York, NY: Raven Press, 1994: 541–70.
46Salamonsen, LA, Nagase, H, Woolley, DE. Production of matrix metalloproteinase 3 (stromelysin) by cultured ovine endometrial cells. J Cell Sci 1991; 100: 381–85.
47Salamonsen, LA, Nagase, H, Suzuki, R, Woolley, DE. Production for matrix metalloproteinase 1 (interstitial collagenase) and matrix metalloproteinase 2 (gelatinase A; 72kDa gelatinase) by ovine endometrial cells in vitro. Different regulation and preferential expression by stromal fibroblasts. J Reprod Fertil 1993; 98: 583–89.
48Hunt, JS, Chen, H-L, Hu, X-L, Tabibzadeh, S. Tumor necrosis factor-α messenger ribonucleic acid and protein in human endometrium. Biol Reprod 1992; 47: 141–47.
49Tabibzadeh, S, Sun, XZ. Cytokine expression in human endometrium throughout the menstrual cycle. Hum Reprod 1992; 7: 1214–21.
50Vogiagis, D, Marsh, MM, Fry, RC, Salamonsen, LA. Leukemia inhibitory factor in human endometrium throughout the menstrual cycle. J Endocrinol 1996; 148: 95102.
51Harvey, MB, Leco, KJ, Arcellana-Panlilo, MY, Zhang, X, Edwards, DR, Schultz, GA. Proteinase expression in early mouse embryos is regulated by leukaemia inhibitory factor and epidermal growth factor. Development 1995; 122: 1005–14.
52Bryant-Greenwood, GD, Rutanen, E-M, Partanen, S, Coelho, TK, Yamamoto, SY. Sequential appearance of relaxin, prolactin and IGFBP-1 during growth and differentiation of the human endometrium. Mol Cell Endocrinol 1993; 95: 2329.
53Bryant-Greenwood, GD, Yamamoto, SY. Control of peripartal collagenolysis in the human chorion-decidua. Am J Obstet Gynecol 1995; 172: 6370.
54Mushayandebvu, TI, Rajabi, MR. Relaxin stimulates interstitial collagenase activity in cultured uterine cervical cells from nonpregnant and pregnant but not immature guinea pigs; estradiol-17β restores relaxin's effect in immature cervical cells. Biol. Reprod 1995; 53: 1030–37.
55Salamonsen, LA, Butt, AR, Macpherson, AM, Rogers, PAW, Findlay, JK. Immunolocalization of the vasoconstrictor endothelin in human endometrium during the menstrual cycle and in umbilical cord at birth. Am J Obstet Gynecol 1992; 167: 163–67.
56Marsh, MM, Findlay, JK, Salamonsen, LA. Endothelin and menstruation. Hum Reprod 1996; 11 [Suppl 2]: 8389.
57Salamonsen, LA, Young, RJ, Garcia, S, Findlay, JK. Mitotic actions of endothelin and other growth factors in ovine endometrium. J Endocrinol 1997; 152: 283–90.
58Simonson, MS, Jones, JM, Dunn, MJ. Differential regulation of fos and jun gene expression and AP-1 cis-element activity by endothelin isopeptides. J Biol Chem 1992; 267: 8643–49.
59Hahn, AWA, Resnik, TJ, Kern, F, Buhler, FR. Peptide vasoconstrictors, vessel structure and vascular smooth muscle proliferation. J Cardiovasc Pharmacol 1993; 22 [Suppl 5]: S37S43.
60Salamonsen, LA, Findlay, JK. Regulation of endometrial prostaglandins during the menstrual cycle and in early pregnancy. Reprod Fertil Dev 1990; 2: 443–58.
61Dayer, J-M, Roelki, MS, Krane, SM. Effects of prostaglandin E2, indomethacin, trifluoperazine and drugs affecting the cytoskeleton on collagenase production by cultured adherent rheumatoid synovial cells. Biochem Pharmacol 1984; 33: 2893–900.
62Krane, SM, Dayer, J-M, Simon, LS, Bryne, MS. Mononuclear cell conditioned medium containing mononuclear cell factor (MCF) homologous with interleukin-1 stimulated collagen and fibronectin synthesis by adherent rheumatoid synovial cells: effect of prostaglandin E2 and indomethacin. Collagen Related Res 1985; 5: 99117.
62Goshowaki, H, Ito, A, Mori, Y. Effects of prostaglandins on the production of collagenase by rabbit uterine cervical fibroblasts. Prostaglandins 1988; 36: 107–14.
63Goshowaki, H, Ito, A, Mori, Y. Effects of prostaglandins on the production of collagenase by rabbit uterine cervical fibroblasts. Prostaglandins 1988; 36: 107–14.
64Osteen, KG, Rodgers, WH, Gaire, M, Hargrove, JT, Gorstein, F, Matrisian, LM. Stromal-epithelial interaction mediates steroidal regulation of metalloproteinase expression in human endometrium. Proc Natl Acad Sci USA 1994; 91: 10129–33.
65Bruner, KL, Rodgers, WH, Gold, LI et al. Transforming growth factor β mediates the progesterone suppression of an epithelial metalloproteinase by adjacent stroma in the human endometrium. Proc Natl Acad Sci USA 1995; 92: 7362–66.
66Kauma, S, Matt, D, Strom, S, Eierman, D, Turner, T. Interleukin-1β, human leukocyte antigen HLADRa, and transforming growth factor-β expression in endometrium, placenta and placental membranes. Am J Obstet Gynecol 1990; 163: 130–37.
67Chegini, N, Zhao, Y, Williams, RS, Flanders, KC. Human uterine tissue throughout the menstrual cycle expresses transforming growth factor beta-1 (TGF beta 1), TGF beta-2, TGR beta-3 and TGF beta type I receptor messenger ribonucleic acid and protein and contains [125I]TGF beta 1 binding sites. Endocrinology 1994; 135: 439–49.
68Marshburn, PB, Arici, AM, Casey, ML. Expression of transforming growth factor-beta 1 messenger ribonucleic acid and the modulation of deoxyribonucleic acid synthesis by transforming growth factor beta 1 in human endometrial cells. Am J Obstet Gynec 1994; 170: 1152–58.
69Wakefield, LM, Sporn, MB. Suppression of carcinogenesis: a role for TGF-β and related molecules in prevention of cancer. In: Klein, G ed. Tumor suppression genes. New York, NY: Dekker, 1990: 217–43.
70Osten, K, Bruner, K, Keller, N, Hargrove, J, Melner, M. Suppression of a stromal metalloproteinase (MMP) by TGF-β requires the presence of epithelial cells [Abstract]. Biol Reprod 1995; 52 [Suppl 1]: 161.
71Clark, DA. Cytokines and uterine bleeding. In: Alexander, NJ, d'Arcangues, C eds. Steroid hormones and uterine bleeding. Washington: American Association for the Advancement of Science, 1992: 263–75.
72King, A, Balendran, N, Wooding, P, Carter, NP, Loke, YW. CD3 leukocytes present in the human uterus during early placentation: phenotypic and morphologic characterisation of the CD56+ population. Dev Immunol 1991; 1: 169–90.
73King, A, Wellings, V, Gardner, L, Loke, YW. Immunocytochemical characterisation of the unusual large granular lymphocytes in human endometrium throughout the menstrual cycle. Hum Immunol 1989; 24: 195205.
74Bulmer, JN, Morrison, L, Longfellow, M, Ritson, A, Pace, D. Granulated lymphocytes in human endometrium: histochemical and immunohistochemical studies. Hum Reprod 1991; 6: 791–98.
75Pace, D, Morrison, L, Bulmer, JN. Proliferative activity in endometrial stromal granulocytes throughout the menstrual cycle and early pregnancy. J Clin Pathol 1989; 42: 3539.
76Bulmer, JN, Hollings, D, Ritson, A. Immunocytochemical evidence that endometrial stromal granulocytes are granulated lymphocytes. Pathol 1987; 153: 281–88.
77Kamat, BR, Isaacson, PG. The immunocytochemical distribution of leukocyte subpopulations in human endometrium. Am J Pathol 1987; 127: 6673.
78Marshall, RJ, Jones, D. An immunohistochemical study of lymphoid tissue in human endometrium. Int J Gynecol Pathol 1988; 7: 2535.
79Starkey, PM, Clover, LM, Rees, MCP. Variation during the menstrual cycle of immune cell populations in human endometrium. Eur J Obstet Gynecol 1991; 39: 203207.
80Bonatz, G, Hansmann, ML, Bucholz, F, Mettler, L, Radzun, HJ, Semm, K. Macrophage- and lymphocyte-subsets in the endometrium during different phases of the ovarian cycle. Int J Gynaecol Obstet 1992; 37: 2936.
81Klentzeris, LD, bulmer, JN, Warren, A et al. Endometrial lymphoid tissue in the timed endometrial biopsy: morphometric and immunohistochemical aspects. Am J Obstet Gynecol 1992; 167: 667–74.
82Poropatich, C, Rojas, M, Silverberg, SG. Polymorphonuclear leukocytes in the endometrium during the normal menstrual cycle. Int J Gynaecol Pathol 1987; 6: 230–34.
83Clark, DA, Wang, S, Rogers, P, Vince, G, Affandi, B. Endometrial lymphomyeloid cells in abnormal uterine bleeding due to levonorgestrel (Norplant). Hum Reprod 1996; 11: 1438–44.
84Jeziorska, M, Salamonsen, LA, Woolley, DE. Mast cell and eosinophil distribution and activation in human endometrium throughout the menstrual cycle. Biol Reprod 1995; 53: 312–20.
85Galli, SJ. New concepts about the mast cell. New Eng J Med 1993; 328: 257–65.
86Bartholomew, JS, Woolley, DE. Plasminogen activator release from cultured murine mast cells. Biochem Biophys Res Commun 1988; 153: 540–44.
87Kroegel, C, Virchow, J-C, Luttmann, W, Walker, C, Warner, JA. Pulmonary immune cells in health and disease: the eosinophil leukocyte (Part 1). Eur Respir J 1994; 7: 519–43.
88King, A, Wooding, P, Gardner, L, Loke, YW. Expression of perforin, granzyme A and TIA-1 by human uterine CD56+ NK cells implies they are activated and capable of effector functions. Hum Reprod 1993; 8: 2061–67.
89Shi, W, Mognetti, B, Campana, A, Bischof, P. Metalloproteinase secretion by endometrial leukocyte subsets. Am J Reprod Immunol 1995; 34: 299310.
90Gottshall, SL, Hansen, PJ. Regulation of leukocyte subpopulations in the sheep endometrium by progesterone. Immunology 1992; 76: 636–41.
91King, A, Gardner, L, Loke, YW. Evaluation of oestrogen and progesterone receptor expression in uterine mucosal lymphocytes. Hum Reprod 1996; 11: 1079–82.
92Kunkel, SL, Strieter, RM, Lindley, IJD, Westwick, J. Chemokines: new ligands, receptors and activities. Immunol Today 1995; 16: 559–61.
93Arici, A, MacDonald, PC, Casey, ML. Regulation of monocyte chemotactic protein-1 gene expression in human endometrial cells in culture. Mol Cell Endocrinol 1995; 107: 189–97.
94Critchley, HO, Kelly, RW, Kooy, J. Perivascular location of a chemokine interleukin-8 in human endometrium: a preliminary report. Hum Reprod 1994; 9: 1406–409.
95Wang, JM, Colella, S, Allavena, P, Mantovani, A. Chemotactic activity of human recombinant granulocyte-macrophage colony-stimulating factor. Immunology 1987; 60: 439–44.
96Robertson, SA, Seamark, AC, Seamark, RF. Uterine epithelial GM-CSF and its interlocutory role during early pregnancy in the mouse. In: Hunt, JS ed. Immunobiology of reproduction. New York, NY: Springer-Verlag, 1994; 9297.
97Giacomini, G, Tabibzadeh, SS, Satyaswaroop, PG et al. Epithelial cells are the major source of biologically active granulocyte macrophage colony-stimulating factor in human endometrium. Hum Reprod 1995; 10: 3259–63.
98Woessner, JF Jr. Matrix metalloproteinases and their inhibitors in connective tissue remodeling. FASEB J 1991; 5: 2145–54.
99Okada, Y, Morodomi, T, Enghild, JJ. Matrix metalloproteinase 2 from human rheumatoid synovial fibroblasts. Purification and activation of the precursor and enzymic properties. Eur J Biochem 1990; 194: 721–30.
100Crabbe, T, O'Connell, JP, Smith, BJ, Docherty, AJP. Reciprocated matrix metalloproteinase activation: a process performed by interstitial collagenase and progelatinase A. Biochemistry 1994; 33: 14419–25.
101Crabbe, T, Smith, B, O'Connell, J, Docherty, A. Human progelatinase A can be activated by matrilysin. FEBS Lett 1994; 345: 1416.
102Overall, CM, Sodek, J. Concanavalin-A produces a matrix-degradative phenotype in human fibroblasts. Induction/endogenous activation of collagenase, 72kDa gelatinase, & Pump-1 is accompanied by suppression of tissue inhibitor of matrix metalloproteinases. J Biol Chem 1990; 265: 21141–51.
103Ward, RV, Atkinson, SJ, Reynolds, JJ, Murphy, G. Cell surface-mediated activation of progelatinase A: demonstration of the involvement of the C-terminal domain of progelatinase A in cell surface binding and activation of progelatinase A by primary fibroblasts. Biochem J 1994; 304: 263–69.
104Lees, M, Taylor, DJ, Woolley, DE. Mast cells proteinases activate precursor forms of collagenase and stromelysin 1, but not of gelatinases A and B. Eur J Biochem 1994; 223: 171–77.
105Saarinen, J, Kalkkinen, N, Welgus, HG, Kovanen, PT. Activation of human interstitial procollagenase through direct cleavage of the leu83-thr84 bond by mast cell chymase. J Biol Chem 1994; 269: 18134–40.
106Koh, SC, Wong, PC, Yuen, R, Chua, S, Ng, B, Ratnam, SS. Concentration of plasminogen activators and inhibitor in the human endometrium at different phases of the menstrual cycle. J Reprod Fertil 1992; 96: 407–13.
107Casslen, B, Urano, S, Ny, T. Progesterone regulation of plasminogen activator inhibitor 1 (PAI-1) antigen and mRNA levels in human endometrial stromal cells. Thromb Res 1992; 66: 7587.
108 Casslén, B, Nordengren, J, Gustavsson, B, Nilbert, M, Lund, LR. Progesterone stimulates degradation of urokinase plasminogen activator (uPA) in endometrial stromal cells by increasing its inhibitor and surface expression of the u-PA receptor. J Clin Endocrinol Metab 1995; 80: 2776–84.
109Schatz, F, Aigner, S, Papp, C, Toth-Pal, E, Hausknecht, V, Lockwood, CJ. Plasminogen activator activity during decidualization of human endometrial stromal cells is regulated by plasminogen activator inhibitor 1. J Clin Endocrinol Metab 1995; 80: 2504–10.
110Carmellet, P, Schoonjans, L, Kleckens, L et al. Physiological consequences of loss of plasminogen activator gene function in mice. Nature 1994; 368: 419–24.
111Eeckhout, Y, Vaes, G. Further studies on the activation of procollagenase, the latent precursor of bone collagenase. Effects of lysosomal cathepsin B, plasmin and kallikrein and spontaneous activation. Biochem J 1977; 166: 2131.
112Nagase, H, Cawston, TE, De Silva, M, Barrett, AJ. Identification of plasma kallikrein as an activator of latent collagenase in rheumatoid synovial fluid. Biochim Biophys Acta 1982; 702: 133–42.
113Stancikova, M, Rybak, M, Trnavsky, K, Simonianova, E. Kallikrein in rheumatoid synovial-fluid and its relation to the activation of latent leukocyte collagenase. Biologia 1985; 40: 769–74.
114Tschesche, H, Michaelis, J, Kohnert, U, Fedrowitz, J, Oberhoff, R. Tissue kallikrein effectively activates latent matrix degrading metalloenzymes. In: Abe, K, Moriya, H, Fujii, S eds. Kinins 5, Part A - Advances in experimental biology and medicine. New York, NY: Plenum, 1989; 247: 545–48.
115Desrivieres, S, He, L, Peyri, N, Soria, C, Legrand, Y, Menashi, S. Activation of the 92-kDa type-IV collagenase by tissue kallikrein. J Cell Physiol 1993; 157: 587–93.
116Yap, B, Mukhtar, A, Hampton, AL, Marsh, MM, Salamonsen, LA, Clements, J. Glandular kallikreins and prostate-specific antigen are differentially expressed in the human endometrium across the menstrual cycle. Proc Endocrine Soc Aust 1994; 37: 85.
117Hayakawa, T, Yamashita, K, Ohuchi, E, Shinagawa, A. Cell growth promoting activity of tissue inhibitor of metalloproteinases-2 (TIMP-2). J Cell Sci 1994; 107: 2372–79.
118Boujrad, N, Ogwuegbu, SO, Garnier, M, Lee, C-H, Martin, BM, Papadopoulos, V. Identification of a stimulator of steroid hormone synthesis isolated from testis. Science 1995; 268: 1609–12.
119Barrett, AJ, Starkey, PM. The interaction of α2-macroglobulin with proteinase. Biochem J 1973; 133: 709–24.
120Casslén, B, Ohlsson, K. Cyclic variation of proteinase inhibitors in human uterine fluid and influence of an IUD. Contraception 1981; 23: 425–34.
121Sayegh, R, Awad, JT, Maxwell, C, Lessey, B, Isaacson, K. α2-Macroglobulin production by the human endometrium. J Clin Endocrinol Metab 1995; 80: 1021–26.
122LaMarre, J, Wollenberg, GK, Gonias, SL, Hayes, MA. Cytokine binding and clearance properties of proteinase-activated α2-macroglobulins. Lab Invest 1991; 65: 314.
123Brown, PD. Matrix metalloproteinase inhibitors: a new class of anticancer agent. Curr Opin Invest Drugs 1993; 2: 617–26.
124Hodgson, J. Remodeling MMPIs. Biotechnology 1995; 13: 554–57.
125Golub, LM, Ramamurthy, NS, McNamara, TF, Greenwald, RA, Rifkin, BR. Tetracyclines inhibit connective tissue breakdown: new therapeutic implications for an old family of drugs. Crit Rev Oral Biol Med 1991; 2: 297322.
126Campion, GV. The prospect for cytokine based therapeutic strategies in rheumatoid arthritis. Ann Rheum Dis 1994; 54: 485–87.
127Woolley, DE. Mast cells in the rheumatoid lesion - ringleaders or innocent bystanders. Ann Rheum Dis 1995; 54: 533–34.

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Matrix metalloproteinases and their tissue inhibitors in endometrial remodelling and menstruation

  • Lois A Salamonsen (a1) and David E Woolley (a2)

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