The signals and molecular pathways involved in human menstruation, a unique process of tissue destruction and remodelling

Molecular Human Reproduction

Volumn 2, Issue 2, 1996, Pages 77-92

  Tabibzadeh, S ^a  

^a H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

Author keywords

Apoptosis; Epithelial cells; Proliferation; Steroid hormones; TNF

Indexed keywords

ACTIN; CADHERIN; ESTROGEN; METALLOPROTEINASE; PROGESTERONE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL; APOPTOSIS; CYTOLOGY; ENDOMETRIUM; EPITHELIUM; EPITHELIUM CELL; FEMALE; GENE EXPRESSION; GENETICS; HUMAN; MENSTRUATION; MICROCIRCULATION; PHYSIOLOGY; REVIEW; SIGNAL TRANSDUCTION; VASCULARIZATION;

ACTINS; ANIMALS; APOPTOSIS; CADHERINS; ENDOMETRIUM; EPITHELIAL CELLS; EPITHELIUM; ESTROGENS; FEMALE; GENE EXPRESSION; HUMANS; MENSTRUATION; METALLOENDOPEPTIDASES; MICROCIRCULATION; PROGESTERONE; SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTOR-ALPHA;

EID: 0030072584     PISSN: 13609947     EISSN: None     Source Type: Journal    
DOI: 10.1093/molehr/2.2.77     Document Type: Review

References (176)

1. Armitage, R.J. (1994) Tumour necrosis factor receptor superfamily members and their ligands. Curr. Opinions Immunol., 6, 407-413.
2. Armitage, R.J., Maliszweski, C.R., Alderson, M.R. et al. (1993) CD40L: a multi-functional ligand. Semin. Immunol., 5, 401-412.
3. Banchereau, J., Bazan, F., Blanchard, D. et al. (1994) The CD40 antigen and its ligand. Annu. Rev. Immunol., 12, 881-992.
4. Bartelmez, G.W. (1933) The histological studies of the menstruating mucous membrane of the human uterus. Carnegie Inst. Contrib. Embryol., 24, 141-186.
5. Bartelmez, G.W. (1957a) The form and the function of the uterine blood vessels in the Rhesus monkeys. Carnegie Inst. Contrib. Embryol., 36, 153-182.
6. Bartelmez, G.W. (1957b) The phases of the menstrual cycle and their interpretation in terms of the pregnancy cycle. Am. J. Obstet. Gynecol., 74, 931-955.
7. Beutler, B. (1992) Tumor necrosis factors. In The Molecules and their Emerging Role in Medicine. Raven Press, New York.
8. Beutler, B. and Van Huffel, C. (1994) Unraveling function in the TNF ligand and receptor families. Science, 264, 667-668.
9. Billing, H., Furuta, I. and Hsueh, A.J.W. (1993) Estrogens inhibit and androgens enhance ovarian granulosa cell apoptosis. Endocrinology, 133, 2204-2212.
10. Birkedal-Hansen, H., Moore, W.G., Bodden, M.K. et al. (1993) Matrix metalloproteinases: a review. Crit. Rev. Oral Biol. Med., 4, 197-250.
11. Blaschuk, O.W., Munro, S.B. and Farookhi, R. (1995) Cadherins, steroids and cancer. Endocrine, 3, 83-89.
12. Brett, J., Gerlack, B.H., Nawroth, P. et al. (1989) Tumor necrosis factor/cachectin increases permeability of endothelial cell monolayers by a mechanism involving regulatory G proteins. J. Exp. Med., 169, 1977-1991.
13. Browning, J.L., Ngam-ek, A., Lawton, P. et al. (1993) Lymphotoxin β, a novel member of the TNF family that forms a heteromeric complex with lymphotoxin on the cell surface. Cell, 72, 847-856.
14. Brunner, N., Bronzert, D., Vindelov, L.L. et al. (1989) Effect on growth and cell cycle kinetics of estradiol and tamoxifen on MCF-7 human breast cancer cells grown in vitro and in nude mice. Cancer Res., 49, 1515-1520.
15. Bulmer, J.N. (1994) Human endometrial lymphocytes in normal pregnancy and pregnancy loss. Ann. N.Y. Acad. Sci., 734, 185-192.
16. Bursch, W., Liehr, J.G., Sirbasku, D.A. et al. (1991) Control of cell death (apoptosis) by diethylstilbestrol in an estrogen-dependent kidney tumor. Carcinogenesis, 12, 855-860.
17. Camerini, D., Walz, G., Loenen, W.A.M. et al. (1991) The T cell activation antigen CD27 is a member of the nerve growth factor/tumor necrosis factor receptor gene family. J. Immunol., 147, 3165-3169.
18. Camussi, G., Albano, E., Tetta, C. and Bussolino, F. (1991) The molecular action of tumor necrosis factor-α. Eur. J. Biochem., 202, 3-14.
19. Carswell, E.A., Old, L.J., Kassel, R.L. et al. (1987) An endotoxin-induced serum factor that causes necrosis of tumors. Proc. Natl. Acad. Sci. USA, 72, 3665-3670.
20. Casslen, B., Andersson, A., Nilsson, I.M. and Astedt, B. (1986) Hormonal regulation of the release of plasminogen activators and of a specific activator inhibitor from endometrial tissue in culture. Proc. Soc. Exp. Biol. Med., 182, 419-424.
21. Christiaens, G.C., Sixma, J.J. and Haspels, A.A. (1980) Morphology of haemostasis in menstrual endometrium. Br. J. Obstet. Gynaecol., 87, 425-439.
22. Claudio, L., Martiney, J.A. and Brosnan, C.F. (1994) Ultrastructural studies of the blood-retina barrier after exposure to interleukin-1β or tumor necrosis factor-α. Lab. Invest., 70, 850-861.
23. Cohen, J.J. and Duke, R.C. (1984) Glucocorticoid activation of a calcium-dependent endonuclease in thymocyte nuclei leads to cell death. J. Immunol., 132, 38-42.
24. Dano, K., Andreasen, J., Grondahl-Hansen. et al. (1985) Plasminogen activators, tissue degradation and cancer. Adv. Cancer Res., 44, 139-266.
25. De, M., Sanford, T.R. and Wood, G.W. (1992) Interleukin-1, interleukin-6, and tumor necrosis factor alpha are produced in the mouse uterus during the estrous cycle and are induced by oestrogen and progesterone. Dev. Biol., 151, 297-305.
26. Denhardt, D.T., Feng, B., Edwards, D.R. et al. (1993) Tissue inhibitor of metalloproteinases (TIMPS, aka EPA): structure, control of expression and biological functions. Pharm. Ther., 59, 329-341.
27. Dubinett, S.M., Huang, M., Lichtenstein, A. et al. (1994) Tumor necrosis factor-α plays a central role in interleukin- 2-induced pulmonary vascular leak and lymphocyte accumulation. Cell. Immunol., 157, 170-180.
28. Duke, R.C. and Cohen, J.J. (1986) IL-2 addiction: withdrawal of growth factor activates a suicide program in dependent cells. Lymphokine Res., 5, 289-299.
29. Durkop, H., Latz, U., Hummel, M. et al. (1992) Molecular cloning and expression of a new member of the nerve growth factor family that is characteristic for Hodgkin's disease. Cell, 68, 421-427.
30. Englemann, H., Holtman, H., Brakebusch, C. et al. (1990) Antibodies to a soluble form of a tumor necrosis factor (TNF) receptor have TNF-like activity. J. Biol. Chem., 265, 14497-14504.
31. Ferenczy, A. (1976) Studies on the cytodynamics of human endometrial regeneration. I. Scanning electron microscopy. Am. J. Obstet. Gynecol., 124, 64-74.
32. Ferenczy, A. (1979) Regeneration of the human endometrium. In Fengolio, C.M. and Wolff, M. (eds). Progress in Surgical Pathology. Masson Publishing, New York, pp. 157-172.
33. Ferenczy, A., Bertrand, G. and Gelfand, M.M. (1979) Proliferation kinetics of human endometrium during the normal menstrual cycle. Am. J. Obstet. Gynecol., 133, 859-867.
34. Frisch, S. and Ruley, H. (1987) Transcription from the stromelysin promoter is induced by interleukin-1 and repressed by dexamethasone. J. Biol. Chem., 262, 16300-16304.
35. Geiger, B. and Ayalon, O. (1992) Cadherins. Ann. Rev. Cell Biol., 8, 307-332.
36. Goldberg, G.I., Marmer, B.L., Grant, G.A. et al. (1989) Human 72-kilodalton type IV collagenase forms a complex with tissue inhibitor of metalloproteases designated TIMP-2. Proc. Natl. Acad. Sci. USA, 86, 8207-8211.
37. Goldblum, S.E., Ding, X. and Campbell-Washington, J. (1993) TNF-α induces endothelial F-actin depolymerization, new actin synthesis and barrier dysfunction. Am. J. Cell. Physiol., 264, C894-C905.
38. Goodwin, R.G., Alderson, M.R., Smith, C.A. et al. (1993a) Molecular and biological characterization of a ligand for CD27 defines a new family of cytokines with homology to tumor necrosis factor. Cell, 73, 447-456.
39. Goodwin, R.G., Din, W.S., Davis-Smith, T. et al. (1993b) Molecular cloning of a ligand for the inducible T-cell gene 4-1BB: a member of an emerging family of cytokines with homology to tumor necrosis factor. Eur. J. Immunol., 23, 2631-2641.
40. Gordon, J.L., Drummond, A.H. and Galloway, W.A. (1993) Metalloproteinases inhibitors as therapeutics. Clin. Exp. Rheumatol., 11, S91-S94.
41. Grell, M., Zimmermann, G., Husler, D. et al. (1994) TNF receptors TR60 and TR80 can mediate apoptosis via induction of distinct signal pathways. J. Immunol., 153, 1963-1972.
42. Hampton, A.L. and Salamonsen, L.A. (1994) Expression of messenger ribonucleic acid encoding matrix metalloproteinases and their tissue inhibitors is related to menstruation. J. Endocrinol., 141, R1-3.
43. Hanemaaijer, R., Koolwijk, P., Le Clercq, L. et al. (1993) Regulation of matrix metalloproteinase expression in human vein and microvascular endothelial cells. Biochem. J., 296, 803-809.
44. Heller, R.A., Song, K., Fan, N. and Chang, D.J. (1992) The p70 tumor necrosis factor receptor mediates cytotoxicity. Cell, 70, 47-56.
45. Herbert, J.M., Savi, P., Laplcae, M.C. et al. (1993) IL-4 and IL-13 exhibit comparable abilities to reduce pyrogen-induced expression of procoagulant activity in endothelial cells and monocytes. FEBS Lett., 328, 268-270.
46. Herrenknecht, K., Ozawa, M., Eckerskom, C. et al. (1991) The uvomorulin-anchorage protein α catenin is a vinculin homologue. Proc. Natl. Acad. Sci. USA, 88, 609-614.
47. Higuchi, M. and Aggarwal, B.B. (1993) P80 form of the human tumor necrosis factor receptor is involved in DNA fragmentation. Fed. Eur. Biochem. Soc., 331, 252-255.
48. Hopwood, D. and Levison, D.A. (1975) Atrophy and apoptosis in the cyclical human endometrium. J. Pathol., 119, 159-166.
49. Hunt, J.S., Chen, H.-L., Hu, X.-L. and Tabibzadeh, S. (1992) Tumor necrosis factor-α mRNA and protein in human endometrium. Biol. Reprod., 47, 141-147.
50. Imada, K., Ito, A., Itoh, Y. et al. (1994) Progesterone increases the production of tissue inhbitor of metalloproteinases-2 in rabbit uterine cervical fibroblasts. FEBS Lett., 341, 109-112.
51. Ininns, E.K., Gatanaga, M., Cappuccini, F. et al. (1992) Growth of the endometrial adenocarcinoma cell line AN3 is modulated by tumor necrosis factor and its receptor is up-regulated by oestrogen in vitro. Endocrinology, 130, 1852-1856.
52. Ishii, H., Horie, S., Kizaki, K. and Kazama, M. (1992) Retinoic acid counteracts both the downregulation of thrombomodulin and the induction of tissue factor in cultured human endothelial cells exposed to tumor necrosis factor. Blood, 80, 2556-2562.
53. Ito, A., Sato, T., Iga, T. and Mori, Y. (1990) Tumor necrosis factor bifunctionally regulates matrix metalloproteinases and tissue inhibitor of metalloproteinase (TIMP) production by human fibroblasts. FEBS Lett., 269, 93-95.
54. Itoh, N., Yonehara, A., Ishi, A., et al. (1991) The polypeptide encoded by the cDNA for human cell surface antigen Fas can mediate apoptosis. Cell, 66, 233-243.
55. Jasser, M.Z., Mitchell, P.G. and Cheung, H.S. (1994) Induction of stromelysin-I and collagenase synthesis in fibrochondrocytes by tumor necrosis factor-α. Matrix Biol., 14, 241-249.
56. Jeffrey, J.J., Coffey, R.J. and Eisen, A.Z. (1971) Studies on uterine collagenase in tissue culture. II. Effect of steroid hormones on enzyme production. Biochim. Biophys. Acta, 252, 143-149.
57. Jiang, W. and Bond, J.S. (1992) Families of metalloendopeptidases and their relationships. FEBS Lett., 312, 110-114.
58. Johnson, D., Lanahan, A., Buck, C.R. et al. (1986) Expression and structure of the human NGF receptor. Cell, 47, 454-554.
59. Jonat, C., Rahmsdorf, H., Park, K.-K. (1990) Anti-tumor promotion and anti-inflammation down-modulation of AP-1 (Fos/Jun) activity by glucocorticoid hormone. Cell, 62, 1189-1204.
60. Jue, D.M., Sherry, B., Leudke, C. and Cerami, A. (1990) Processing of newly synthesized cachectin/tumor necrosis factor in endotoxin-stimulated macrophages. Biochemistry, 29, 8371-8377.
61. Kamat, B. and Isaacson, D.M. (1987) The immunocytochemical distribution of leukocytic subpopulations in human endometrium. Am. J. Pathol., 127, 66-73.
62. Kapprell, H.P., Owaribe, K. and Franke, W.W. (1988) Identification of a basic protein of Mr 75,000 as an accessory desmosomal plaque protein in stratified and complex epithelia. J. Cell. Biol., 106, 1679-1691.
63. Kerr, J.F.R., Wyllie, A.H. and Currie, A.R. (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer, 26, 239-257.
64. Kleiner, D.E. Jr. and Stetler Stevenson, W.G. (1993) Structural biochemistry and activation of matrix metalloproteases. Curr. Opinions Cell. Biol., 5, 891-897.
65. Kohno, K., Hamanaka, R., Abe, T. et al. (1993) Morphological change and destabilization of β-actin mRNA by tumor necrosis factor in human microvascular endothelial cells. Exp. Cell. Res., 208, 498-503.
66. Kohno, T., Brewer, M.T., Baker, S.L. et al. (1990) A second tumor necrosis factor receptor gene product can shed a naturally occurring tumor necrosis factor inhibitor. Proc. Natl. Acad. Sci. USA, 87, 8331-8335.
67. Kown, B.S. and Weissman, S.M. (1989) cDNA sequences of two inducible T-cell genes. Proc. Natl. Acad. Sci. USA, 86, 1963-1967.
68. Kyprianou, N., English, H.F., Davidson, N.E. and Issacs, J.T. (1991) Programmed cells death during regression of the MCF-7 human breast cancer following estrogen ablation. Cancer Res., 51, 162-166.
69. Lindeman, H.J. (1979) Hysteroscopic data during menstruation. In Beller, L.R.K. and Schaumacher, G.F.B. (eds), The Biology of the Fluids of the Female Genital Tract. Elsevier, North-Holland, NY, Amsterdam, pp. 225-229.
70. Lockwood, C.J., Nemerson, Y., Guller, S. et al. (1993a) Progestational regulation of human endometrial stromal cell tissue factor expression during decidualization. J. Clin. Endocrinol. Metab., 76, 231-236.
71. Lockwood, C.J., Nemerson, Y., Krikun, G. et al. (1993b) Steroid-modulated stromal cell tissue factor expression: a model for the regulation of endometrial hemostasis and menstruation. J. Clin. Endocrinol. Metab., 77, 1725-1726.
72. Lockwood, C.J., Krikun, G., Papp, C. et al. (1994a) Biological mechanisms underlying RU 486 clinical effects: inhibition of endometrial stromal cell tissue factor content. J. Clin. Endocrinol. Metab., 79, 786-790.
73. Lockwood, C.J., Krikun, G., Papp, C. et al. (1994b) The role of progestionally regulated stromal cell tissue factor and type-1 plasminogen activator inhibitor (PAI-1) in endometrial hemostasis and menstruation. Ann. N.Y. Acad. Sci., 734, 57-79.
74. Loskutoff, D.J., Sawdey, M. and Mimuro, J. (1989) Type 1 plasminogen activator. Prog. Hemostasis Thromb., 9, 87-115.
75. Lotz, M. and Guerne, P.-A. (1991) Interleukin-6 induces the synthesis of tissue inhibitor of metalloproteinase-1/erythroid potentiating activity (TIMP-1/EPA). J. Biol. Chem., 5, 2017-2020.
76. Loughney, A.D., Kumarendran, M.K., Thomas, E.J. and Redfern, C.P.F. (1995) Variation in the expression of cellular retinoid binding proteins in human endometrium throughout the menstrual cycle. Mol. Hum. Reprod., 1,
77. see Hum. Reprod., 10, 1297-1304.
78. Loy, R.A., Loukides, J.A. and Polan, M.L. (1992) Ovarian steroids modulate human monocyte tumor necrosis factor alpha messenger ribonucleic acid levels in cultured human peripheral monocytes. Fertil. Steril., 58, 733-739.
79. Luna, E.J. and Hitt, A.L. (1992) Cytoskeleton-plasma membrane interactions. Science, 258, 955-963.
80. Mallett, S., Fossum, S. and Barclay, A.N. (1990) Characterization of the MRC OX-40 antigen of activated CD4 positive T lymphocytes - a molecule related to nerve growth factor receptor. EMBO J., 9, 1063-1068.
81. Mangan, D.F. and Wahl, S.M. (1991) Differential regulation of human monocyte programmed cell death (apoptosis) by chemotactic factors and pro-inflammatory cytokines. J. Immunol., 147, 3408-3412.
82. Marbaix, E., Donnez, J., Courtoy, P.J. and Eeckhout, Y. (1992) Progesterone regulates the activity of collagenase and related gelatinases A and B in human endometrial explants. Proc. Natl. Acad. Sci, USA, 89, 11789-11793.
83. Mareel, M., Bracke, M., Van Roy, R. and Vakaet, L. (1993) Expression of E-cadherin in embryogenetic ingression and cancer invasion. Int. J. Dev. Biol., 37, 227-235.
84. Markee, J.E. (1940) The morphological and endocrine basis for menstrual bleeding. Prog. Gynecol., 2, 63-74.
85. Markee, J.E. (1946) Menstruation in intraocular endometrial transplants in the rhesus monkeys. J. Am. Med. Assoc., 250, 2167-2171.
86. Markee, J.E. (1948) Morphological basis for menstrual bleeding: relation of regression to the initiation of bleeding. Bull. N.Y. Acad. Med., 24, 253-270.
87. Marshal, R.J. and Jones, D.B. (1988) An immunohistochemical study of lymphoid tissue in human endometrium. Int. J. Gynecol. Pathol., 7, 225-235.
88. Martin, L. (1980) Effect of anti-estrogens on cell proliferation in the rodent reproductive tract. In McLacklan, J.A. (ed.), Estrogens in the Environment. Elsevier, NY, New York, pp. 103-130.
89. Martin, L. and Finn, C.A. (1968) Hormonal regulation of cell division in epithelial and connective tissues of the mouse uterus. J. Endocrinol., 41, 363-371.
90. Martin, L. and Finn, C.A. (1970) Interactions of estradiol and progestins in the mouse uterus. J. Endocrinol., 48, 109-115.
91. Martin, L., Finn, C.A. and Trinder, G. (1973) Hypertrophy and hyperplasia in the mouse uterus after estrogen treatment: an autoradiographic study. J. Endocrinol., 56, 133-144.
92. Martin, L., Pollard, J.W. and Fagg, B. (1976) Oestriol, estradiol-17β and the proliferation and death of uterine cells. J. Endocrinol., 69, 103-115.
93. Matrisian, L.M., Gaire, M., Rodgers, W.H. and Osteen, K.G. (1994) Metalloproteinase expression and hormonal regulation during tissue remodeling in the cycling human endometrium. Contrib. Nephrol., 107, 94-100.
94. McDonnell, S., Wright, J.H., Gaire, M. and Matrisian, L.M. (1994) Expression and regulation of stromelysin and matrilysin by growth factors and oncogenes. Biochem. Soc. Trans., 22, 55-57.
95. Milatovich, A., Song, K., Heller, R.A. and Francke, U. (1991) Tumor necrosis factor receptor genes, TNFR1 and TNFR2, on human chromosomes 12 and 1. Somatic Cell. Mol. Genet., 17, 519-523.
96. Miller, K., Mattey, D., Measures, H., Hopkins, C. and Garrod, D. (1987) Localization of the protein and glycoprotein components of bovine nasal epithelial desmosomes by immunoelectron microscopy. EMBO J., 6, 885-889.
97. Morris, H., Edwards, J., Tiltman, A. and Malcolm, E. (1985) Endometrial lymphoid tissue: an immunohistological study. J. Clin. Pathol., 38, 644-652.
98. Mueller, H. and Franke, W.W. (1983) Biochemical and immunological characteristics of desmoplakin I and II, the major polypeptides of the desmosomal plaque. J. Mol. Biol., 163, 647-671.
99. Murphy, G. and Docherty, J.P. (1992) The matrix metalloproteinases and their inhibitors. Am. J. Resp. Cell. Mol. Biol, 7, 120-125.
100. Murphy, G., Atkinson, S., Ward, R., Gavrilovic, J. and Reynolds, J.J. (1992) The role of plasminogen activators in the regulation of connective tissue metalloproteinases. Ann. N.Y. Acad. Sci., 667, 1-12.
101. Nagafuchi, A. and Takeichi, M. (1989) Transmembrane control of cadherin-mediated cell adhesion. A 94 kDa protein functionally associated with a specific region of the cytoplasmic domain of E-cadherin. Cell Regulation, 1, 37-44.
102. Nagase, H., Okata, Y., Suzuki, K. et al. (1991) Substrate specificities and activation mechanisms of matrix metalloproteinases. Biochem. Soc. Trans., 19, 715-718.
103. Nemerson, Y. (1988) Tissue factor and hemostasis. Blood, 71, 1-8.
104. Nicholson, R., Mader, S., Nagpal, S. et al. (1990) Negative regulation of the rat stromelysin gene promoter by retinoic acid is mediated by an AP-1 binding site. EMBO J., 9, 4443-4454.
105. Ogata, Y., Enghild, J.J. and Nagase, H. (1992) Matrix metalloproteinase 3 (stromelysin) activates the precursor for the human matrix metalloproteinase 9. J. Biol. Chem., 267, 3581-3584.
106. Old, L.J. (1985) Tumor necrosis factor. Science, 230, 631-632.
107. Osteen, K.G., Rodgers, W.H., Gaire, M. et al. (1994) Stromal-epithelial interactions mediate steroidal regulation of metalloproteinase expression in human endometrium. Proc. Natl. Acad. Sci. USA, 91, 10129-10133.
108. Otani, H., Erdos, M. and Leonard, W.J. (1993) Tyrosine kinase(s) regulate apoptosis and bcl-2 expression in a growth factor-dependent cell line. J. Biol. Chem., 268, 22733-22736.
109. Otto, J.J. (1990) Vinculin. Cell Motil. Cytoskeleton, 12, 1-6.
110. Ozawa, M., Baribault, H. and Kemler, R. (1989) The cytoplasmic domain of the cell adhesion molecule uvomorulin associates with three independent proteins structurally related in different species. EMBO J., 8, 1711-1717.
111. Partridge, C.A., Jeffrey, J.J. and Malik, A.B. (1993) A 96-kDa gelatinase induced by TNF-α contributes to increased microvascular endothelial permeability. Lung Cell. Mol. Physiol., 9,
112. see Am. J. Phsyiol., 265, L438-L447.
113. Philippaeaux, M.-M. and Piguet, P.F. (1993) Expression of tumor necrosis factor-α and its mRNA in the endometrial mucosa during the menstrual cycle. Am. J. Pathol., 143, 480-486.
114. Pollard, J.W., Pacey, J., Cheng, S.V.Y. and Jordan, E.G. (1987) Estrogens and cell death in murine luminal epithelium. Cell Tissue Res., 249, 533-540.
115. Rajabi, M., Solomon, S. and Poole, A.R. (1991) Hormonal regulation of interstitial collagenase in the uterine cervix of the pregnant guinea pig. Endocrinology, 128, 863-871.
116. Ralston, S.H., Russell, R.G.R. and Gowen, M. (1990) Estrogen inhibits release of tumor necrosis factor from peripheral blood mononuclear cells in postmenopausal women. J. Bone Min. Res., 5, 983-988.
117. Rawdanowicz, T.J., Hampton, A.L., Nagase, H. et al. (1994) 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-1α and tumor necrosis factor-α J. Clin. Endocrinol. Metab., 79, 530-536.
118. Remick, D.G. and Kunkel, S.L. (1994) Pathophysiologic alteration induced by tumor necrosis factor. Int. Rev. Exp. Pathol., 34B, 7-25.
119. Rhodin, J.A.G. (1974) Rhodin Histology. Library of Congress, New York, pp. 65-76.
120. Robaye, B., Mosselmans, R., Fiers, W. et al. (1991) Tumor necrosis factor induces apoptosis (programmed cell death) in normal endothelial cells in vitro. Am. J. Pathol., 138, 447-453.
121. Roberts, D.K., Parmley, T.H., Walker, N.J. et al. (1992) Ultrastructure of the microvasculature in the human endometrium throughout the normal menstrual cycle. Am. J. Obstet. Gynecol, 166, 1393-1406.
122. Roby, K. and Hunt, J.S. (1994) Mouse endometrial tumor necrosis factor-α messenger ribonucleic acid and protein: localization and regulation by estradiol and progesterone. Endocrinology, 135, 2780-2789.
123. Rodgers, W.H., Osteen, K.G., Matrisian, L.M. et al. (1993) Expression and localization of matrilysin, a matrix metalloproteinase, in human endometrium during the reproductive cycle. J. Obstet. Gynecol., 168, 9413-9417.
124. Rodgers, W.H., Matrisian, L.M., Giudice, L.C. et al. (1994) Patterns of matrix metalloproteinase expression in cycling endometrium imply differential functions and regulation by steroid hormones. J. Clin. Invest., 94, 946-953.
125. Rotello, R.J., Lieberman, R.C., Lepoff, R.B. and Gerschenson, L.E. (1992) Characterization of uterine epithelium apoptotic cell death kinetics and regulation by progesterone and RU 486. Am. J. Pathol., 140, 449-456.
126. Sandow, B.A., West, N.B., Norman, R.L. and Brenner, R.M. (1979) Hormonal control of apoptosis in hamster uterine luminal epithelium. Am. J. Anat., 156, 15-36.
127. Sato, T., Ito, A., Mori, Y. et al. (1991) Hormonal regulation of collagenolysis in uterine cervical fibroblasts. Modulation of synthesis of procollagenase, prostromelysin and tissue inhibitor of metalloproteinase (TIMP) by progesterone and estradiol-17β. Biochem. J., 275, 645-650.
128. Schall, J.S., Lewis, M., Koller, K.J. et al. (1990) Molecular cloning and expression of a receptor for human tumor necrosis factor. Cell, 61, 361-370.
129. Schatz, F., Papp, C., Toth-Pal, E. and Lockwood, C.J. (1994) Ovarian steroid-modulated stromelysin-1 expression in human endometrial stromal and decidual cells. J. Clin. Endocrinol. Metab., 78, 1467-1472.
130. Sen, D.K. and Fox, H. (1967) The lymphoid tissue of the endometrium. Gynaecologia, 163, 371-378.
131. Shalaby, M.R., Laegried, W.W., Ammann, A.J. and Liggitt, H.D. (1989) Tumor necrosis factor-α associated uterine endothelial injury in vivo. Influence of dietary fat. Lab Invest., 61, 564-570.
132. Shalaby, M.R., Sundan, A., Loetscher, H. et al. (1990) Binding and regulation of cellular functions by monoclonal antibodies against human tumor necrosis factor receptors. J. Exp. Med., 172, 1517-1520.
133. Skerrow, C.J. and Matoltsy, A.G. (1974) Isolation of epidermal desmosomes. J. Cell. Biol., 63, 515-523.
134. Slayden, O.D., Hirst, J.J. and Brenner, R.M. (1993) Estrogen action in the reproductive tract of rhesus monkeys during antiprogestin treatment. J. Endocrinol. Metab., 132, 1845-1856.
135. Smith, C.A., Davis, T., Anderson, D. et al. (1990) A receptor of tumor necrosis factor defines an unusual family of cellular and viral proteins. Science, 248, 1019-1023.
136. Smith, C.A., Gruss, H.-J., Davis, T. et al. (1993) CD30 antigen, a marker for Hodgkin's lymphoma, is a receptor whose ligand defines an emerging family of cytokines with homology to TNF. Cell, 73, 1349-1360.
137. So, T., Ito, A., Sato, T. et al. (1992) Tumor necrosis factor-α stimulates the biosynthesis of matrix metalloproteinases and plasminogen activator in cultured human chorionic cells. Biol. Reprod., 46, 772-778.
138. Srivista, K.C. (1978) Prostaglandins and platelet function. South Afr. J. Sci., 74, 290-294.
139. Stamenkovic, I., Clark, E.A. and Seed, B. (1989) A B-lymphocyte activation molecule related to the nerve growth factor receptor and induced in carcinomas. EMBO J., 8, 1403-1410.
140. Steinberg, M.S., Shida, H., Giudice, G.J. et al. (1987) On the molecular organization, diversity and functions of desmosomal proteins. In Bock, G. and Clark, C. (eds), Junctional Complexes of Epithelial Cells. John Wiley and Sons, Chichester, UK, pp. 3-25.
141. Stetler-Stevenson, W.G., Krutzch, H.S. and Liotta, L.A. (1989) Tissue inhibitor of metalloproteinase (TIMP-2). A new member of the metalloproteinase inhibitor family. J. Biol. Chem., 264, 17374-17378.
142. Suda, T., Takahashi, T., Golstein, P. and Nagata, S. (1993) Molecular cloning and expression of the Fas ligand, a novel member of the tumor necrosis factor family. Cell, 75, 1169-1178.
143. Suzuki, S., Sano, K. and Tahihara, H. (1991) Diversity of the cadherin family: evidence for eight new cadherins in nervous tissue. Cell Reg., 2, 261-270.
144. Tabibzadeh, S.S. (1990a) Evidence of T cell activation and potential cytokine action in human endometrium. J. Clin. Endocrinol. Metab., 71, 645-649.
145. Tabibzadeh, S.S. (1990b) Proliferative activity of lymphoid cells in human endometrium throughout the menstrual cycle. J. Clin. Endocrinol. Metab., 70, 437-443.
146. Tabibzadeh, S. (1991a) Induction of HLA-DR expression in endometrial epithelial cells by endometrial T cells: potential regulatory role of endometrial T cells in vivo. J. Clin. Endocrinol. Metab., 73, 1352-1359.
147. Tabibzadeh, S. (1991b) Human endometrium; an active site of cytokine production and action. Endocrine Rev., 12, 272-290.
148. Tabibzadeh, S. (1991c) Ubiquitous expression of TNF-α/cachectin in human endometrium. Am. J. Rep. Immunol., 26, 1-5.
149. Tabibzadeh, S. (1994a) Regulatory roles of IFN-gamma in human endometrium. Ann. N.Y. Acad. Sci., 734, 1-6.
150. Tabibzadeh, S. (1994b) Cytokines and hypothalamic-pituitary-ovarian-endometrial axis. Hum. Reprod., 9, 947-967.
151. Tabibzadeh, S.S. and Poubouridis, D. (1990) Expression of leukocyte adhesion molecules in human endometrium. Am. J. Clin. Pathol., 93, 183-189.
152. Tabibzadeh, S., Kong, Q.F. and Sun, X.Z. (1993) Regulatory roles of TNF-α on transepithelial migration of leukocytes and epithelial dyscohesion. Endocrine, 1, 417-425.
153. Tabibzadeh, S., Kong, Q.F., Satyaswaroop, P.G. et al. (1994) Distinct regional and menstrual cycle dependent distribution of apoptosis in human endometrium. Potential regulatory role of T cells and TNF-α. Endocrine, 2, 87-95.
154. Tabibzadeh, S., Babaknia, A., Kong, Q.F. et al. (1995a) Menstruation is associated with disordered expression of Desmoplakin I/II, cadherin/catenins and conversion of F to G actin in endometrial epithelium. Hum. Reprod., 10, 776-784.
155. Tabibzadeh, S., Babaknia, A., Liu, R. et al. (1995b) Site and menstrual cycle-dependent expression of proteins of the TNF receptor family, and BCL-2 oncoprotein and phase specific productipn of TNF-α in human endometrium. Hum. Reprod., 10, 277-286.
156. Tabibzadeh, S., Kong, Q.F., Kapur, S. et al. (1995c) TNF-α mediated dyscohesion of epithelial cells is associated with disordered expression of cadherin/β-catenin and disassembly of actin filaments. Mol. Hum. Reprod., 1,
157. see Hum. Reprod., 10, 994-1004.
158. Takeichi, M. (1991) Cadherin cell adhesion receptors as a morphogenetic regulator. Science, 251, 1451-1455.
159. Tartaglia, L.A., Ayers, T.M., Wong, G.H.W. and Goeddel, D.V. (1993a) A novel domain within the 55 kDa TNF receptor signals cell death. Cell, 74, 845-853.
160. Tartaglia, L.A., Rothe, M., Hu, Y.-F. and Goeddel, D.V. (1993b) Tumor necrosis factor's cytotoxic activity is signaled by the p55 TNF receptor. Cell, 73, 213-216.
161. Totpal, K., Chaturvedi, M.M., LaPushin, R. and Aggarwal, B.B. (1995) Retinoids downregulate both p60 and p80 forms of tumor necrosis factor receptors in human histiocytic lymphoma U937 cells. Blood, 85, 3547-3555.
162. Tracey, K.J., Beutler, B., Lowry, S.F. et al. (1986) Shock and tissue injury induced by recombinant human cachectin. Science, 234, 470-474.
163. Treisman, J., Hwu, P., Yannelli, J.R. et al. (1994) Upregulation of tumor necrosis factor-α production by retrovirally transduced human tumor-infiltrating lymphocytes using trans-retinoic acid. Cell. Immunol., 156, 448-457.
164. Turpin, J., Mehta, K., Blick, M. et al. (1990) Effect of tumor necrosis factor on the release and gene expression of tumor necrosis factor-α in human peripheral blood monocytes. J. Leuk. Biol., 48, 444-450.
165. Uria, J.A., Fermando, A.A., Velasco, G. et al. (1994) Structure and expression in breast tumors of human TIMP-3, a new member of the metalloproteinase inhibitor family. Cancer Res., 54, 2091-2094.
166. Vassalli, J.-D., Sappino, A.-P. and Belin, D. (1991) The plasminogen activator/plasmin system. J. Clin. Invest., 88, 1067-1072.
167. Waage, A. and Espevik, T. (1988) Interleukin 1 potentiates the lethal effect of tumor necrosis factor α/cachectin in mice. J. Exp. Med., 167, 1987-1992.
168. Wahl, L.M. (1977) Hormonal regulation of macrophage collagenase activity. Biochem. Biophys. Res. Commun., 74, 838-845.
169. Ward, R.V., Atkinson, S.J., Slocombe, P.M. et al. (1991a) Tissue inhibitor of metalloproteinases-2 inhibits the activation of 72 kDa progelatinase by fibroblast membranes. Biochim. Biophys. Acta, 1079, 242-246.
170. Ward, R.V., Hembry, R.M., Reynolds, J.J. and Murphy, G. (1991b) The purification of tissue inhibitor of metalloproteinases-2 from its 72 kDa progelatinase complex. Demonstration of the biochemical similarities of tissue inhibitor of metalloproteinases-2 and tissue inhibitor of metalloproteinases-1. Biochem J., 278, 179-187.
171. West, N.B., Norman, R.L., Sandow, B.A. and Brenner, R.M. (1978) Hormonal control of nuclear estradiol receptor content and the luminal epithelium in the uterus of the golden hamster. Endocrinology, 103, 1732-1741.
172. Williams, G.T., Smith, C.A., Spooner, E. et al. (1990) Haemopoietic colony stimulating factors promote cell survival by suppressing apoptosis. Nature, 343, 76-79.
173. Woessner, J.F. (1991) Matrix metalloproteinases and their inhibitors in connective tissue remodeling. FASEB J., 5, 2145-2154.
174. Woessner, J.F. and Taplin, C.J. (1988) Purification and properties of a small latent matrix metalloproteinase of the rat uterus. J. Biol. Chem., 263, 16918-16925.
175. Wyllie, A.H. (1993) Apoptosis. Br. J. Cancer, 67, 205-208.
176. Wyllie, A.H. and Morris, R.G. (1982) Hormone-induced cell death. Purification and properties of thymocytes undergoing apoptosis after glucocorticoid treatment. Am. J. Pathol., 109, 78-87.