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Role of cytokines in endometrium and at the fetomaternal interface

Published online by Cambridge University Press:  02 March 2009

S Tabibzadeh
S Tabibzadeh*
Affiliation:
University of South Florida Health Sciences Center and Moffitt Cancer Center, Tampa, Florida, USA
*
S Tabibzadeh, Department of Pathology, Moffitt Cancer Center, 12902 Magnolia Drive, Tampa, FL 33612, USA.
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Extract

Cytokines were first recognized as factors involved in the immune responses. However, emerging evidence suggests that cytokines serve as the unanimous language through which cells in organ systems as diverse as hypothalamus to endometrium communicate. Evidence for the participation of these factors in the normal function of the endometrium and uteroplacental unit and development of the embryo is being recognized. This review will highlight the significant insight gained over the past several years for the role of cytokines in the field of reproductive biology. Major emphasis will be placed on interleukins, tumour necrosis factor-α, transforming growth factors, colony stimulating factors and interferon-gamma.

Type
Articles
Information
Reproductive Medicine Review , Volume 3 , Issue 1 , March 1994 , pp. 11 - 28
Copyright
Copyright © Cambridge University Press 1994

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References

1Arai, K-I, Lee, F, Miyajiima, A, Miatake, S, Arai, N, Yokota, T. Cytokines: Coordination of immune and inflammatory responses. Ann Rev Biochem 1990; 59: 783–836.CrossRefGoogle ScholarPubMed
2Ijzermans, JNM, Marquet, RL. Interferon gamma: a review. Immunobiol 1989; 179: 456–73.Google Scholar
3Le, J, Vilcek, J. Biology of disease. Tumor necrosis factor and interleukin 1: Cytokines with multiple overlapping biological activities. Lab Invest 1987; 56: 234–48.Google Scholar
4Dinarello, CA. Multiple biological properties of recombinant human interleukin 1 (beta). Immunobiol 1986; 172: 301–15.Google Scholar
5March, CJ, Mosley, B, Larsen, A et al. Cloning, sequence and expression of two distinct human interleukin-1 complementary DNAs. Nature 1985; 315: 641–47.Google Scholar
6Oppenheim, JJ, Kovacs, EJ, Matsushima, K, Durum, SK. There is more than one interleukin 1. Immunol Today 1986; 7: 45–56.Google Scholar
7Dower, SK, Urdal, DL. The interleukin-1 receptor. Immunol Today 1987; 8: 46–51.CrossRefGoogle ScholarPubMed
8Kilian, PL, Kaffka, KL, Stern, AS et al. Interleukin a and interleukin β bind to the same receptor on T cells. J Immunol 1986; 136: 4509–14.Google Scholar
9Dower, SK, Kronheim, SR, Hopp, TP et al. The cell surface receptors for interleukin-1α and interleukin-1β are identical. Nature 1986; 324: 266–68.Google Scholar
10Lomedico, PT, Kilian, PL, Gubler, U, Stern, AS, Chizzonite, R. Molecular biology of interleukins. Cold Spring Harb Symp Quant Biol 1986; 51: 631–39.Google Scholar
11Mizel, SB, Kilian, PL, Lewis, JC, Paganelli, KA, Chizzonite, RA. The interleukin 1 receptor. Dynamics of interleukin 1 binding and internalization in T cells and fibroblasts. J Immunol 1987; 138: 2906–12.Google Scholar
12Bomsztyk, K, Sims, JE, Stanton, TH. Evidence for different IL-1 receptors in murine B- and T-cell lines. Proc Natl Acad Sci USA 1989; 86: 8034–38.Google Scholar
13Tackacs, L, Kavacs, EJ, Smith, MR, Young, HA, Durum, SK. Detection of IL-1α and IL-1α gene expression by in situ hybridization. Tissue localization of IL-1 mRNA in the normal C57BL/6 mouse. J Immunol 1988; 141: 3081–95.Google Scholar
14Tabibzadeh, S, Sun, XZ. Cytokine expression in human endometrium throughout the menstrual cycle. Hum Reprod 1992; 7: 1214–21.Google Scholar
15Tabibzadeh, SS, Kaffka, KL, Satyaswaroop, PG, Kilian, PL. IL-1 regulation of human endometrial function: Presence of IL-1 receptor correlates with IL-1 stimulated PGE2 production. J Endocrinol Metab 1990; 70: 1000–1006.Google Scholar
16Tabibzadeh, SS. Cytokine regulation of human endometrial functions. Ann N Y Acad Sci 1991; 622: 89–98.CrossRefGoogle Scholar
17Kauma, S, Matt, D, Strom, S, Eierman, D, Turner, T. Interleukin-1β, human leukocyte antigen HLA-DRα, and transforming growth factor-β expression in endometrium, placenta, and placental membranes. Am J Obstet Gynecol 1990; 163: 1430–37.Google Scholar
18Cannon, JG, Dinarello, CA. Increased plasma interleukin-1 activity in women after ovulation. Science 1985; 227: 1247–49.Google Scholar
19Hu, X-L, Yange, Y, Hunt, JS. Differential distribution of interleukin-1α and interleukin-1β proteins in human placentas. J Reprod Immunol 1992; 22: 257–58.CrossRefGoogle Scholar
20Van Damme, J, Opdenakker, G, Simpson, RJ et al. Identification of the human 26K protein (IFN-β2) as a B-cell hybridoma/plasmacytoma growth factor induced by interleukin-1 and tumor necrosis factor. J Exp Med 1987; 165: 914–19.Google Scholar
21Kruttgen, A, Rose-John, S, Moller, C et al. Structure-function of human interleukin-6. Evidence for the involvement of the carboxy-terminus in function. FEBS Lett 1990; 262: 323–26.Google Scholar
22Murakami, M, Hibi, M, Nakagawa, N et al. IL-6-induced homodimerization of gp-130 and associated activation of a tyrosine kinase. Science 1993; 260: 1808–10.CrossRefGoogle Scholar
23Tabibzadeh, SS, Poubouridis, D, May, LT, Sehgal, PB. Interleukin-6 immunoreactivity in human tumors. Am J Pathol 1989; 135: 427–33.Google Scholar
24Tabibzadeh, SS, Santhanam, U, Sehgal, PB, May, L. Cytokine-induced production of interferonβ2/interleukin-6 by freshly explanted human endometrial stromal cells. Modulation by estradiol-17β. J Immunol 1989; 142: 3134–39.CrossRefGoogle Scholar
25Jacobs, AL, Sehgal, PB, Julian, J, Carson, DD. Secretion and hormonal regulation of interleukin-6 production by mouse uterine stromal and polarized epithelial cells cultured in vitro. Endocrinol 1992; 131: 1037–46.CrossRefGoogle ScholarPubMed
26Robertson, SA, Maryhofer, G, Seamark, RF. Uterine epithelial cells synthesize granulocyte-macrophage colony-stimulating factor (GM-CSF) and interleukin-6 (IL-6) in pregnant and non-pregnant mice. Biol Reprod 1992; 46: 1069–79.CrossRefGoogle Scholar
27Dudley, DJ, Trautman, MS, Araneo, BA, Edwin, SS, Mitchell, MD. Decidual cell biosynthesis of interleukin-6: Regulation by inflammatory cytokines. J Clin Endocrinol Metab 1992; 74: 884–89.Google Scholar
28Nishino, E, Matsuzaki, N, Masuhiro, K et al. Trophoblast-derived interleukin-6 (IL-6) regulates human chorionic gonadotropin release through IL-6 receptor on human trophoblasts. J Endocrinol Metab 1990; 71: 436–41.Google Scholar
29Dudley, DJ, Trautman, MS, Edwin, SS, Lundlin-Schiller, S, Mitchell, MD. Biosynthesis of interleukin-6 by cultured human chorion laeve cells: Regulation by cytokines. J Endocrinol Metab 1992; 75: 1081–86.Google ScholarPubMed
30Jue, D-M, Sherry, B, Leudke, C, Cerami, A. Processing of newly synthesized cachectin/tumor necrosis factor in endotoxin-stimulated macrophages. Biochem 1990; 29: 8371–77.Google Scholar
31Camussi, G, Albano, E, Tetta, C, Bussolino, F. The molecular action of tumor necrosis factor-α. Eur J Biochem 1991; 202: 3–14.Google Scholar
32Hunt, JS, Chen, H-L, Hu, X-L, Tabibzadeh, S. Tumor necrosis factor-α mRNA and protein in human endometrium. Hum Reprod 1992; 47:141–47.Google Scholar
33Tabibzadeh, S. Ubiquitous expression of TNF-α/Cachectin in human endometrium. Am J Rep Immunol 1991; 26: 1–5.CrossRefGoogle ScholarPubMed
34Yelavarthi, KK, Chen, HL, Yang, Y, Cowley, BD, Fishback, JL, Hunt, JS. Tumor necrosis factor-α mRNA and protein in rat uterine and placental cells. J Immunol 1991; 146: 3840–48.CrossRefGoogle ScholarPubMed
35Casey, ML, Cox, SM, Beutler, B, Milewich, L, MacDonald, PC. Cachectin/tumor necrosis factor-α in human decidua. Potential role of cytokines in infection-induced preterm labor. J Clin Invest 1989; 83: 430–36.Google Scholar
36Jaattela, M, Kuusela, P, Saksela, E. Demonstration of tumor necrosis factor in human amniotic fluids and supernatants of placental and decidual tissues. Lab Invest 1988; 58: 48–52.Google ScholarPubMed
37Eades, DK, Corneium, P, Pekala, PH. Characterization of tumor necrosis factor receptor in human placenta. Placenta 1988; 9: 247–51.CrossRefGoogle ScholarPubMed
38Scherr, CJ. Regulation of mononuclear phagocyte proliferation by colony-stimulating factor-1. Int J Cell Cloning 1990; 8: 46–62.Google Scholar
39Scherr, CJ. The colony stimulating factor 1 receptor: Pleiotropy of signal-response coupling. Lymphokine Res 1990; 9: 543–48.Google Scholar
40Pampfer, S, Arceci, RJ, Pollard, JW. Role of colony stimulating factor-1 (CSF-1) and other lympho-hematopoietic growth factors in mouse pre-implantation development. Bioassays 1991; 13: 535–40.CrossRefGoogle ScholarPubMed
41Pollard, JW. Regulation of polypeptide growth factor synthesis and growth factor-related gene expression in the rat and mouse uterus before and after implantation. J Reprod Fertil 1990; 88: 721–31.Google Scholar
42Pampfer, S, Tabibzadeh, S, Chuan, F-C, Pollard, JW. Molecular cloning of a novel transcript for colony stimulating factor-1 from human endometrial glands. Production of a transmembrane form of the protein. J Mol Endocrinol 1991; 5: 1931–38.Google Scholar
43Croy, BA, Guilbert, LJ, Browne, MA et al. Characterization of cytokine production by the metrial gland and granulated metrial gland cells. J Reprod Immunol 1991; 19:149–66.Google Scholar
44Jokhi, PP, Chumbley, G, King, A, Gardner, L, Loke, YW. Expression of the colony stimulating factor-1 receptor (c-fms product) by cells at the human uteroplacental interface. Lab Invest 1993; 68: 308–20.Google Scholar
45Pampfer, S, Diater, E, Barad, D, Pollard, JW. Expression of the colony-stimulating factor-1 receptor (c-fms proto-Oncogene product) in the human uterus and placenta. Biol Reprod 1992; 46: 48–57.CrossRefGoogle Scholar
46Wong, GG, Witek, JS, Temple, PA et al. GM-CSF: Molecular cloning of the complementary DNA and purification of the natural and recombinant proteins. Science 1985; 228: 810–15.CrossRefGoogle ScholarPubMed
47Chiba, S, Shibuya, K, Piao, Y-F et al. Identification and cellular distribution of distinct proteins forming human GM-CSF receptor. Cell Reg 1990; 1: 327–35.CrossRefGoogle ScholarPubMed
48Robertson, SA, Seamark, RF. Uterine granulocyte-macrophage colony stimulating factor in early pregnancy: cellular origin and potential regulators. In: Chaout, G, Mowbray, J eds. Molecular and cellular biology of the feto-maternal relationship. InSERM 212, John Libbey Eurotext, Paris Edition 1991, 113–21.Google Scholar
49Carpenter, G, Zendegui, JG. Epidermal growth factor, its receptor and related proteins. Exp Cell Res 1986; 164: 1–10.Google Scholar
50Downward, J, Yarden, Y, Mayes, E et al. Close similarity of epidermal growth factor receptor and v-er-B oncogene protein sequences. Nature 1984; 307: 521–27.Google Scholar
51Lee, DC, Rose, TM, Webb, NR, Todaro, GJ. Cloning and sequence analysis of cDNA of rat transforming growth factor-alpha. Nature 1985; 313: 489–91.CrossRefGoogle ScholarPubMed
52Derynck, R, Roberts, AB, Winkler, ME, Chen, EY, Goeddel, DV. Human transforming growth factor-α: precursor structure and expression in E. coli. Cell 1984; 38: 287–97.Google Scholar
53Ignotz, RA, Kelly, B, Davis, RJ, Massague, J. Biological active precursor for transforming growth factor type a, released by retrovirally transformed cells. Proc Natl Acad Sci USA 1986; 83: 6307–11.Google Scholar
54Nelson, KG, Takahashi, T, Lee, DC et al. Transforming growth factor-α is a potential mediator of estrogen action in the mouse uterus. Endocrinol 1992; 131: 1657–64.CrossRefGoogle ScholarPubMed
55Teng, CT, McLachlan, JA, Bell, GI, Di Augustine, RP. Estrogens stimulated epidermal growth factor (EGF) mRNA in immature mouse uterus (Abstract). Proceedings of the 10th International Congress of the International Society of Developmental Biologists, Los Angeles, California, 1985.Google Scholar
56Haining, REB, Schofield, JP, Jones, DS, Rajput-Williams, J, Smith, SK. Identification of mRNA for epidermal growth factor and transforming growth factor-alpha in low copy number in human endometrium and decidua using reverse transcriptase-polymerase chain reaction. J Mol Endocrinol 1991; 6: 207–14.CrossRefGoogle ScholarPubMed
57Horowitz, GM, Scott, RT, Drews, MR, Navot, D, Hofmann, GE. Immunohistochemical localization of transforming growth factor-α in human endometrium, decidua, and trophoblast. J Endocrinol Metab 1993; 76: 786–92.Google Scholar
58Bissonnette, F, Cook, C, Geoghegan, T et al. Transforming growth factor-α and epidermal growth factor messenger ribonucleic acid and protein levels in human placentas from early, mid, and late gestation. Am J Obstet Gynecol 1992; 166: 192–99.Google Scholar
59Berchuck, A, Soisson, AP, Olt, GJ et al. Epidermal growth factor receptor expression in normal and malignant endometrium. Am J Obstet Gynecol 1989; 161: 1247–52.Google Scholar
60Sheets, EE, Tibris, JCM, Cook, NI, Virgin, SD, DeMay, RM, Spellacy, WN. In vitro binding of insulin and epidermal growth factor to human endometrium and endocervix. Am J Obstet Gynecol 1985; 153: 60–65.Google Scholar
61Chengini, N, Rao, CV, Wakin, N, Sanfilippo, J. Binding of 125I-epidermal growth factor in human uterus. Cell Tissue Res 1986; 246: 543–48.Google Scholar
62Hofmann, GE, Rao, CV, Barrows, GH, Schultz, GS, Sanfilippo, J. Binding sites for epidermal growth factor in human uterine tissues and leiomyomas. J Endocrinol Metab 1984; 58: 880–84.Google Scholar
63Sorrentino, JM, Hendrix, JC. EGF receptor binding studies in endometrial cell culture. Life Sci 1984; 34: 1769–74.Google Scholar
64Damahanov, I, Mildner, B, Knowles, BB. Immunohistochemical localization of the epidermal growth factor receptor in normal human tissues. Lab Invest 1986; 55: 588–92.Google Scholar
65Reynolds, RK, Talavera, F, Roberts, JA, Hopkins, MP, Menon, KMJ. Characterization of epidermal growth factor receptor in normal and neoplastic human endometrium. Cancer 1990; 66: 1967–74.Google Scholar
66Mukku, VR, Stancel, GM. Receptors for epidermal growth factor in the rat uterus. Endocrinol 1985; 117:149–54.CrossRefGoogle ScholarPubMed
67Massague, J, Cheifetz, S, Boyd, FT, Andres, JL. TGF-β receptors and TGF-β binding proteoglycans: Recent progress in identifying their functional properties. Ann N Y Acad Sci 1990; 593: 59–72.Google Scholar
68Tamada, H, McMaster, MT, Flanders, KC, Andrews, GK, Sudhansu, KD. Cell type-specific expression of transforming growth factor-β1 in the mouse uterus during the periimplantation period. Mol Endocrinol 1990; 4: 965–72.Google Scholar
69Graham, CH, Lysiak, JJ, McCrae, KR, Lala, PK. Localization of transforming growth factor-β at the human fetal-maternal interface: Role in trophoblast growth and differentiation. Biol Reprod 1992; 46: 561–72.Google Scholar
70Altman, DJ, Schneider, SL, Thompson, DA, Chneg, H-L, Tomasi, TB. A transforming growth factor β2 (TGF-β2)-like immunosuppresive factor in amniotic fluid and localization of TGF-β2 in the pregnant uterus. J Exp Med 1990; 172:1391–401.Google Scholar
71Clark, DA, Flanders, KC, Banwatt, D et al. Murine pregnancy decidua produces a unique immunosuppressive molecule related to transforming growth factor β-2. J Immunol 1990; 144: 3008–14.Google Scholar
72Halloran, PF. Interferon-γ, prototype of the proinflammatory cytokines-importance in activation, suppression and maintenance of the immune response. Transplant Proc 1993; 25: 10–15.Google ScholarPubMed
73Grasso, G, Muscettola, M, Bocci, V. The physiologic interferon response. I: cells attached to intrauterine devices release interferon in vitro. Proc Soc Exp Biol Med 1983; 173: 276–80.Google Scholar
74Tabibzadeh, SS. Evidence of T cell activation and potential cytokine action in human endometrium. J Endocrinol Metab 1990; 71: 645–49.Google Scholar
75Tabibzadeh, S. Induction of HLA-DR expression in endometrial epithelial cells by endometrial T cells: Potential regulatory role of endometrial T cells in vivo. J Endocrinol Metab 1991; 73: 1352–59.Google Scholar
76Tabibzadeh, S, Sun, XZ, Kong, QG, Kasnic, G, Miller, J, Satyaswaroop, PG. In vitro induction of a polarized microenvironment by T cells and IFN-gamma in three dimensional spheroid cultures of endometrial epithelial cells. Hum Reprod 1993; 8: 182–92.Google Scholar
77Blaustein, A. Pathology of the female genital tract, second edition. New York, NY: Springer-Verlag, 1982.Google Scholar
78Tabibzadeh, SS, Bellica, A, Gerber, MA. Variable expression of Ia anligens in human endomelrium and in chronic endometrilis. Am J Clin Pathol 1986; 86: 153–60.Google Scholar
79Tabibzadeh, SS, Salyaswaroop, PG. Sex sleroid receptors in lymphoid cells of human endometrium. Am J Clin Pathol 1989; 91: 656–63.Google Scholar
80Tabibzadeh, SS, Satyaswaroop, PG. Differential expression of HLA-DR, HLA-DP and HLA-DQ antigenic determinants of the major histocompalibilily complex in human endometrium. Am J Reprod Immunol Microbiol 1989; 18: 124–30.Google Scholar
81Tabibzadeh, SS. Proliferative activity of lymphoid cells in human endometrium ihroughout the menstrual cycle. J Endocrinol Metab 1990; 70: 437–43.Google Scholar
82Klenlzeris, LD, Bulmer, JN, Warren, A, Morrison, L, Li, T-C, Cooke, ID. Endometrial lymphoid tissue in ihe timed endometrial biopsy: Morphometric and immunohistochemical aspects. Am J Obstet Gynecol 1992; 167: 667–74.Google Scholar
83Sen, DK, Fox, H. The lymphoid tissue of the endometrium. Gynaecologia 1967; 163: 371–78.Google Scholar
84Marshal, RJ, Jones, DB. An immunohistochemical study of lymphoid lissue in human endometrium. Int J Gynecol Pathol 1988; 7: 225–35.Google Scholar
85Kamat, BR, Isaacson, DM. The immunocytochemical distribulion of leukocytic subpopulations in human endometrium. Am J Pathol 1987; 127: 66–73.Google ScholarPubMed
86Morris, H, Edwards, J, Tiltman, A, Malcolm, E. Endometrial lymphoid tissue: An immuno-histological study. J Clin Pathol 1985; 38: 644–52.Google Scholar
87Tabibzadeh, SS, Gerber, MA. Immunohistologic analysis of lymphoid cells by a rapid double immunoenzymatic labeling. J Immunol Methods 1986; 91: 169–74.CrossRefGoogle Scholar
88Stewart, CJR, Maura, A, Farquharson, A, Foulis, AK. The distribution and possible function of gamma-interferon-immunoreactive cells in normal endometrium and myometrium. Virchows Archi A Pathol Anat 1992; 420: 419–24.CrossRefGoogle ScholarPubMed
89Vlaente, G, Ozmen, L, Novelli, F et al. Distribution of interferon-γ receptor in human tissues. Eur J Immunol 1992; 22: 2403–12.Google Scholar
90Calderon, J, Sheehan, KCF, Chance, C, Thomas, ML, Schrieber, RD. Purification and characterization of the human interferon-γ receptor from placenta. Proc Nati Acad Sci USA 1988; 85: 4837–41.Google Scholar
91Berkowitz, RS, Heidi, MPF, Hill, JA, Anderson, DJ. Localization of leukocytes and cytokines in chorionic villi of normal placentas and complete hydatidiform moles. Gynecol Oncol 1990; 37: 396–400.Google Scholar
92Palladino, MA, Morris, RE, Starnes, HF, Levinson, AD. The transforming growth factor-betas. A new family of immunoregulatory molecules. Ann N Y Acad Sci 1990; 593: 181–87.Google Scholar
93Ming, WJ, Bersani, L, Montovani, A. Tumor necrosis factor is chemotactic for monocytes and polymorphonuclear leukocytes. J Immunol 1987; 138: 1469–74.CrossRefGoogle ScholarPubMed
94Pohlman, TH, Stanness, KA, Beatty, PG, Ochs, HD, Harlan, JM. An endothelial cell surface factor(s) induced in vitro by lipopolsysaccharide, interleukin 1, tumor necrosis factor-alpha increases neutrophil adherence by a CDw18-dependent mechanism. J Immunol 1986; 136: 4548–53.CrossRefGoogle ScholarPubMed
95Wahl, SM, Hunt, DA, Wakefield, LM et al. Transforming growth factor type β induces monocyte chemotaxis and growth factor production. Proc Natl Acad Sci USA 1987; 84: 5788–92.Google Scholar
96Wiseman, DM, Polverini, PJ, Kamp, DW, Leibovich, SJ. Transforming growth factor-beta (TGF-β) is chemotactic for human monocytes and induces their expression of angiogenic activity. Biochem Biophys Res Commun 1988; 1572: 793–800.Google Scholar
97Postlewaite, AE, Keski-Oja, J, Moses, HL, Kang, AH. Stimulation of the chemotactic migration of human fibroblasts by transforming growth factor beta. J Exp Med 1987; 165: 251–56.Google Scholar
98Hendricks, HR, Korn, C, Mebius, RE, Kraal, G. Interferon-gamma-increased adherence of lymphocytes to high endothelial venules. Immunology 1989; 68: 221–26.Google Scholar
99Bergh, A, Soder, O. Interleukin-1β but not interleukin-1α induces acute inflammation-like changes in the testicular microcirculation of adult rats. J Reprod Immunol 1990; 17: 155–65.Google Scholar
100Barker, JNWN, Hallen, MH, Macdonald, DM. Alterations induced in normal human skin by in vivo interferon-gamma. Br J Dermatol 1990; 122: 451–58.Google Scholar
101Kawakami, Y, Kuzuya, N, Watanabe, T, Uchiyama, Y, Yamashita, K. Induction of experimental thyroditis in mice by recombinant interferon-gamma administration. Acta Endocrinologica (Copenh) 1990; 122: 41–48.Google Scholar
102Fierlbeck, G, Rassner, G, Muller, C. Psoriasis induced at the injection site of recombinant interferon gamma. Arch Dermatol 1990; 126: 351–55.CrossRefGoogle ScholarPubMed
103Lynch, J, Twardzik, DR, Todaro, GJ. Epithelial wound healing enhanced by transforming factor-α and vaccinia growth factor. Science 1987; 235: 350–52.Google Scholar
104Schreiber, AB, Wrinkler, ME, Derynck, R. Transforming growth factor-α: A more potent angiogenic mediator than epidermal growth factor. Science 1986; 232: 1250–53.Google Scholar
105Tomooka, Y, DiAugustine, RP, McLachlan, JA. Proliferation of mouse uterine epithelial cells in vitro. Endocrinology 1986; 118: 1011–18.Google Scholar
106Ghahary, A, Murphy, LJ. Regulation of uterine insulin-like growth factor receptors by estrogen and variation throughout the estrous cycle. Endocrinology 1989; 125: 597–604.Google Scholar
107Ghahary, A, Murphy, LJ. In situ localization of the sites of synthesis and action of insulin-like growth factor-1 in the rat uterus. Mol Endocrinol 1990; 4: 191–95.Google Scholar
108Tabibzadeh, AA, Satyaswaroop, PG, Rao, PN. Antiproliferative effect of interferon gamma in human endometrial epithelial cells in vitro: potential local growth modulatory role in endometrium. J Endocrinol Metab 1988; 67: 131–38.CrossRefGoogle ScholarPubMed
109Le, LV, Oh, S-T, Anners, JA, Rinhart, CA, Halme, J. Interleukin-1 inhibits growth of normal human endometrial stromal cells. Obstet Gynecol 1992; 80: 405–409.Google ScholarPubMed
110Padykula, HA, Coles, LG, McCracken, JA, King, NW Jr, Longcope, C, Kaiserman-Abramof, IR. A zonal pattern of cell proliferation and differentiation in the Rhesus endometrium during the estrogen surge. Biol Reprod 1984; 31: 1103–18.Google Scholar
111Tabibzadeh, S. Distinct subsets of stromal cells confined to unique microenvironments in human endometrium throughout the menstrual cycle. Am J Rep Immunol 1991; 26: 5–10.CrossRefGoogle ScholarPubMed
112Tabibzadeh, SS, Mordilo, S, Gerber, MA. Immunoultrastructural localization of la antigens in human endometrium. Arch Pathol Lab Med 1987; 111: 32–37.Google Scholar
113Tabibzadeh, S. Patterns of expression of integrin molecules in human endometrium throughout the menstrual cycle. Human Reprod 1992; 7: 876–82.CrossRefGoogle ScholarPubMed
114Ferenczy, A, Bertrand, G, Gelfand, MM. Proliferation kinetics of human endometrium during the normal menstrual cycle. Am J Obstet Gynecol 1979; 133 859–67.Google Scholar
115Silberstein, GB, Daniel, CW. Reversible inhibition of mammary gland growth by transforming growth factor-β. Science 1987; 237: 291–92.Google Scholar
116Tabibzadeh, S. Human endometrium; an active site of cytokine production and action. End Rev 1991; 12: 272–90.CrossRefGoogle ScholarPubMed
117Tsujimoto, M, Yokota, S, Vilcek, J, Weismann, G. Tumor necrosis factor provokes Superoxide anion generation from neutrophils. Biochem Biophys Res Commun 1986; 137: 1094–100.Google Scholar
118Wahl, SM, Wahl, LM. Modulation of fibroblast growth and function by monokines and lymphokines. In: Pick, E ed. Lymphokines, Volume 2. New York: Academic Press, 1981: 179–201.Google Scholar
119Philippaeaux, M-M, Piguet, PF. Expression of tumor necrosis factor-α and its mRNA in the endometrial mucosa during the menstrual cycle. Am J Pathol 1993; 143: 480–86.Google Scholar
120Brett, J, Gerlach, H, Naworth, P, Steinberg, S, Godman, G, Stern, D. Tumor necrosis factor/cachectin increases permeability of endothelial cell monolayers by a mechanism involving regulatory G proteins. J Exp Med 1989; 169: 1977–91.Google Scholar
121Camussi, G, Turello, E, Bussolino, F, Bagliolni, C. Tumor necrosis factor alters cytoskeletal organization and barrier function of endothelial cells. Intl Arch Allergy Appl Immunol 1991; 96: 84–91.Google Scholar
122Mullin, JM, Snock, KV. Effect of tumor necrosis on epithelial tight junctions and transepithelial permeability. Cancer Res 1990; 50: 2172–76.Google Scholar
123Shalaby, MR, Laegried, WW, Ammann, AJ, Liggitt, HD. Tumor necrosis factor-α-associated uterine endothelial injury in vivo. Influence of dietary fat. Lab Invest 1989; 61: 564–70.Google Scholar
124Ferenczy, A. Regeneration of the human endometrium. In: Fengolio, CM, Wolff, M eds. Progress in surgical pathology. New York: Masson Publishing, 1979: 157–72.Google Scholar
125Tabibzadeh, S, Kong, QF, Sun, XZ. Regulatory roles of TNF-α on transepithelial migration of leukocytes and epithelial dyscohesion. Endocr J 1993; 1: 417–25.Google Scholar
126Levitt, MJ, Tobon, H, Josimovish, JB. Prostaglandin content of human endometrium. Fertil Steril 1976; 26: 296–300.Google Scholar
127Simon, C, Piquette, GN, Frances, A, Polan ML: Localization of interleukin-1 type receptor and interleukin-1β in human endometrium throughout the menstrual cycle. J Clin Endocrinol Metab 1993; 77: 549–55.Google Scholar
128Quaglino, D Jr, Nanney, LB, Kennedy, R, Davidson, JM. Transforming growth factor-β stimulates wound healing and modulates extracellular matrix gene expression in pig skin. I: excisional wound model. Lab Invest 1990; 63: 307–19.Google Scholar
129Casscells, W, Bazoberry, F, Speir, E et al. Transforming growth factor-β in normal heart and in myocardial infarction. Ann N Y Acad Sci 1990; 593: 148–60.Google Scholar
130Sporn, MB, Roberts, AB. The transforming growth factor-betas: past, present and future. Ann N Y Acad Sci 1990; 593: 1–6.Google Scholar
131Daiter, E, Pollard, JW. Colony stimulating factor-1 (CSF-1) in pregnancy. Reprod Med Rev 1992; 1: 83–97.Google Scholar
132Pollard, JW, Pampfer, S, Daiter, E, Barad, D, Arceci, RJ. Colony stimulating factor-1 in the mouse and human uteroplacental unit. In: Schomberg DW ed. Growth factors in reproduction 1994 (in press).Google Scholar
133Arceci, RJ, Shanhan, F, Stanley, ER, Pollard, JW. Temporal expression and location of colony stimulating-factor 1 (CSF-1) and its receptor in the female reproductive tract are consistent with CSF-1 regulated placental development. Proc Natl Acad Sci USA 1989; 86: 8818–22.Google Scholar
134Kariya, M, Kanzaki, H, Takakura, K et al. Interleukin-1 inhibit. in vitro decidualization of human endometrial stromal cells. J Clin Endocrinol Metab 1991; 73: 1170–74.Google Scholar
135Kauma, SW. Interleukin-1β stimulates colony stimulating factor-1 production in human term placenta. J Clin Endocrinol Metab 1991; 76: 701–703.Google Scholar
136Harty, JR, Kauma, SW. Interleukin-1β stimulates colony stimulating factor-1 production in placental villous core mesenchymal cells. J Endocrinol Metab 1992; 75: 947–50.Google Scholar
137Masuhiro, K, Matsuzaki, N, Nishino, E et al. Trophoblast-derived interleukin-1 (IL-1) stimulates the release of human chorionic gonadotropin by activating IL-6 and IL-6 receptor system in first trimester human trophoblasts. J Clin Endocrinol Metab 1991; 72: 594–601.Google Scholar
138Pollard, JW, Hunt, JS, Wiktor-Jedrejczak, W, Stanley, ER. A pregnancy defect in the osteoporotic (op/op) mouse demonstrates the requirement for CSF-1 in female fertility. Dev Biol 1991; 148: 273–83.Google Scholar
139Tartakovsy, B. CSF-1 induces resorption of embryos in mice. Immunol Lett 1989; 23: 65–70.CrossRefGoogle Scholar
140Tartakovsky, B, Goldstein, O. The effect of cytokines on pregnancy and embryonic development in mice. In: Dinarello, CA, Kluger, MJ, Powanda, MC, Oppenheim, J eds. The physiological and pathological effects of cytokines. Progress in leukocyte biology, 10B. New York: Wiley-USS, 1990: 243–48.Google Scholar
141Tartakovsky, B, Goldstein, O, Broshi, N. Colony stimulating factor-1 blocks early pregnancy in mice. Biol Reprod 1991; 44: 906–12.Google Scholar
142Tartakovsky, B, Ben-Yair, E. Cytokines modulate preimplantation development and pregnancy. Dev Biol 1991; 146: 345–52.Google Scholar
143Hill, JA, Haimovici, F, Anderson, DJ. Products of activated lymphocytes and macrophages inhibit mouse embryo development in vitro. J Immunol 1987; 139: 2250–59.Google Scholar
144Haimovici, F, Hill, JA, Anderson, D. The effects of soluble products of activated lymphocytes and macrophages on blastocyst implantation events in vitro. Biol Reprod 1991; 44: 69–75.Google Scholar
145Chaouat, G, Menu, E, Clark, DA, Minkowski, M, Wegman, TG. Control of fetal survival in CBAxDBA/2 mice by lymphokine therapy. J Reprod Dert 1990; 89: 447–58.Google Scholar
146Kossodo, S, Grau, GE, Daneva, T et al. Tumor necrosis factor α is involved in mouse growth and lymphoid tissue development. J Exp Med 1992; 176: 1259–64.Google Scholar
147Tartakovsky, B, Ben-Yair, E. Cytokines modulate preimplantation development and pregnancy. Dev Biol 1991; 146: 345–52.Google Scholar
148Romero, R, Wu, YK, Brody, DT, Oyarzun, E, Gordon, WD, Durum, SK. Human decidua: A source of interleukin-1. Obstet Gynecol 1989; 73: 31–34.Google Scholar
149Romero, R, Durum, S, Dinarello, CA, Oyarzun, E, Hobbins, JC, Mitchell, MD. Interleukin-1 stimulates prostaglandin biosynthesis by human amnion. Prostaglandins 1989; 37: 13–27.Google Scholar
150Tamatani, T, Tsunoda, H, Iwasaki, H, Kanedo, M, Hashimoto, T, Onozaki, K. Existence of both IL-1α and β in normal human aminiotic fluid: unique high molecular weight form of IL-1α. Immunology 1988; 65: 337–42.Google Scholar
151Romero, R, Brody, DT, Oyarzun, E et al. Infection and labor. III. Interleukin-1: A signal for the onset of parturition. Am J Obstet Gynecol 1989; 160: 1117–23.CrossRefGoogle ScholarPubMed
152Taniguchi, T, Matsuzaki, N, Kameda, T et al. The enhanced production of placental interleukin-1 during labor and intrauterine infection. Am J Obstet Gynecol 1991; 165: 131–37.Google Scholar
153Romero, R, Sepulveda, W, Mazor, M et al. The natural interleukin-1 receptor antagonist in term and preterm parturition. Am J Obstet Gynecol 1992; 167: 863–72.CrossRefGoogle ScholarPubMed
154Romero, R, Mazor, M, Tartakovsky, B. Systemic administration of interleukin-1 induces preterm parturition in mice. Am J Obstet Gynecol 1991; 165: 969–71.Google Scholar
155Romero, R, Tartakovsky, B. The natural interleukin-1 receptor antagonist prevents interleukin-1 induced preterm delivery in mice. Am J Obstet Gynecol 1992; 167:1041–45.Google Scholar
156Romero, R, Mnogue, KR, Mitchell, MD et al. Infection and labor. IV: cachectin-tumor necrosis factor in the amniotic fluid of women with intraamniotic infection and preterm labor. Am J Obstet Gynecol 1989; 161: 336–41.Google Scholar
157Zahl, PA, Bjerknes, C. Induction of decidua-placental hemorrhage in mice by the endotoxins in certain gram-negative bacteria. Proc Soc Exp Biol Med 1943; 54: 329–35.Google Scholar
158Kass, EH. Effect of corticosteroids and of hormones of pregnancy on the lethal action of bacterial endotoxins. Ann N Y Acad Sci 1960; 88: 107–15.Google Scholar
159Bry, K, Hallman, M. Transforming growth factor-β2 prevents delivery induced by interleukin-1α and tumor necrosis factor-α in the rabbit. Am J Obstet Gynecol 1993; 168: 1318–22.Google Scholar
160Romero, R, Wu, YK, Oyarzun, E, Hobbins, JC, Mitchell, MD. A potential role for epidermal growth factor/α-transforming growth factor in human parturition. Eur J Obstet Gynecol Reprod Biol 1989; 33: 55–60.Google Scholar
161Saito, S, Kasahara, T, Kato, Y, Ishihara, Y, Ichijo, M. Elevation of amniotic fluid interleukin 6 (IL-6), IL-8 and granulocyte colony stimulating factor (G-CSF) in term and preterm parturition. Cylokine 1993; 5: 81–88.Google Scholar
162Wolvekamp, MCJ, Marquet, RL. Interleukin-6: Historical background, genetics and biological significance. Immunol Lett 1990; 24: 1–10.Google Scholar
163Le, J, Vilcek, J. Interleukin 6: A multifunctional cytokine regulating immune reactions and the acute phase protein response. Lab Invest 1989; 61: 588–602.Google Scholar
164Old, LJ. Tumor necrosis factor. Science 1985; 230: 631–32.Google Scholar
165Blackwill, FR, Burke, F. The cytokine network. Immunol Today 1989; 10: 299–304.Google Scholar
166Cohen, S. The epidermal growth factor (EGF). Cancer 1983; 51: 1787–91.Google Scholar
167Nathan, C, Sporn, M. Cytokines in context. J Cell Biol 1991; 113: 981–86.Google Scholar
168Dinarello, CA, Mier, JA. Lymphokines. N Engl J Med 1987; 317: 940–45.Google Scholar
169Miyajiima, A, Hara, T, Kitamura, T. Common subunits of cytokine receptors and the functional redundancy of cytokines. Trends Biochem Sci 1992; 17: 378–82.Google Scholar
170Brigstock, DR. Growth factors in the uterus: Steroidal regulation and biological actions. Baillieres Clin Endocrinol Metab 1991; 5: 791–808.Google Scholar
171Ininns, EK, Gatanaga, M, Cappuccini, F et al. Growth of the endometrial adenocarcinoma cell line AN3 CA is modulated by tumor necrosis factor and its receptor is up-regulated by estrogen in vitro. Endocrinology 1992; 130: 1852–56.Google Scholar
172Loy, RA, Loukides, JA, Polan, ML. Ovarian steroids modulate human monocyte tumor necrosis factor alpha messenger ribonucleic acid levels in cultured human peripheral monocytes. Fertil Steril 1992; 58: 733–39.Google Scholar
173Gonzalez, F, Lakshamann, J, Hoath, S, Fisher, DA. Effect of oestradiol-17β on uterine epidermal growth factor concentration in immature mice. Acta Endocrinol 1984; 105: 425–28.Google Scholar
174Fox, H, Bond, BL, Parslow, TG. Estrogen regulates the IFN-γ promoter. J Immunol 1991; 146: 4362–67.Google Scholar
175Mori, H, Nakagawa, M, Itoh, N, Wada, K, Tamaya, T. Danazol suppresses the production of interleukin-1β and tumor necrosis factor by human monocytes. Am J Reprod Immunol 1990; 24: 45–50.Google Scholar
176Polan, ML, Daniele, A, Kuo, A. Gonadal steroids modulate human monocyte interleukin-1 (IL-1) activity. Fertil Steril 1988; 49: 964–68.Google Scholar
177Pacifici, R, Brown, C, Puscheck, E et al. Effect of surgical menopause and estrogen replacement on cytokine release from human blood mononuclear cells. Proc Natl Acad Sci USA 1991; 88: 5134–38.Google Scholar
178Danforth, DN Jr, Sgagias, MK. Interleukin 1α blocks estradiol-stimulated growth and down-regulates the estrogen receptor in MCF-7 breast cancer cells in vitro. Cancer Res 1991; 51: 1488–93.Google Scholar
179Wang, Y, Campbell, HD, Young, IG. Sex hormones and dexamethasone modulate interleukin-5 gene expression in T lymphocytes. J Steroid Biochem Mol Biol 1993; 44: 203–10.Google Scholar