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Angiogenesis in Endometriosis

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Part of the book series: Cardiovascular Molecular Morphogenesis ((CARDMM))

Abstract

Endometriosis is a common gynecologic disorder defined by the presence, growth, and progression of endometrial tissue outside the uterine cavity. Endometriosis can be asymptomatic, but it typically is associated with a multitude of clinical symptoms, the most common being pelvic pain and impaired fertility. The disease affects about 10% of all reproductive-age women and the prevalence rises to 20% to 50% in infertile women. Genes seem to influence liability to endometriosis (Treloar et al, 1999); however, the mode of hereditary transmission appears to be multifactorial (Malinak et al, 1980). Retrograde menstruation and increased exposure to menstrual flow (reduced parity, longer duration of menstrual periods, or shorter cycle length) have been identified as risk factors for endometriosis. Recently, environmental factors, in particular dioxin (Rier et al, 1993) and other presumed endocrine disrupters have been implicated in its development.

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References

  • Adams, J. 1997. Thrombospondin-1.Int. J. Biochem. Cell. Biol.29:861–865.

    Article  PubMed  CAS  Google Scholar 

  • Ahmed, A., Acevedo, C., Nijjar, S., Aplin, J., Yancopoulos, G., and Shams, M. 2000. Angiopoietin-1 and Tie-2 are downregulated in dysfunctional uterine bleeding.J. Soc. Gynecol. Invest.7(suppl 1):57A.

    Google Scholar 

  • Arici, A., Head, J., MacDonald, P., and Casey, M. 1993. Regulation of interleukin-8 gene expression in human endometrial cells in culture.Mol. Cell. Endocrinol.94:195–204.

    Article  PubMed  CAS  Google Scholar 

  • Arici, A., MacDonald, P., and Casey, M. 1996a. Progestin regulation of interleukin-8 mRNA levels and protein synthesis in human endometrial stromal cells.J. Steroid. Biochem. Mol. Biol.58:71–76.

    Article  CAS  Google Scholar 

  • Arici, A., MacDonald, P. C., and Casey, M. L. 1996b. Modulation of the levels of transforming growth factor beta messenger ribonucleic acids in human endometrial stromal cells.Biol. Reprod.54:463–469.

    Article  CAS  Google Scholar 

  • Arici, A., Tazuke, S. I., Attar, E., Kliman, H. J., and Olive, D. L. 1996c. Interleukin-8 concentration in peritoneal fluid of patients with endometriosis and modulation of interleukin-8 expression in human mesothelial cells.Mol. Hum. Reprod.2:40–45.

    Article  CAS  Google Scholar 

  • Baker, J., Liu, J., Robertson, E., and Efstratiadis, A. 1993. Role of insulin-like growth factors in embryonic and postnatal growth.Cell75:73–82.

    PubMed  CAS  Google Scholar 

  • Ben-Av, P., Crofford, L. J., Wilder, R. L., and Hla, T. 1995. Induction of vascular endothelial growth factor expression in synovial fibroblasts by prostaglandin E and interleukin1: a potential mechanism for inflammatory angiogenesis.FEBS Lett.372:83–87.

    CAS  Google Scholar 

  • Bentzien, F., Vigne, J.-L., Weiner, R., and Taylor, R. 1997. Potential role of cathepsin D in the formation of antiangiogenic fragment of prolactin in the human endometrium.Endocrine Society AbstractsP1–33.

    Google Scholar 

  • Brogi, E., Wu, T., Namiki, A., and Isner, J. 1994. Indirect angiogenic cytokines upregulate VEGF and bFGF gene expression in vascular smooth muscle cells, whereas hypoxia upregulates VEGF expression only.Circulation90:649–652.

    Article  PubMed  CAS  Google Scholar 

  • Bulmer, J., Longfellow, M., and Ritson, A. 1991. Leukocytes and resident blood cells in endometrium.Ann. NY Acad. Sci.622:57–68.

    Article  PubMed  CAS  Google Scholar 

  • Charnock-Jones, D., Sharkey, A., Rajput-Williams, J., Burch, D., Schofield, J., and Fountain, S. 1993. Identification and localization of alternately spliced mRNAs for vascular endothelial growth factor in human uterus and estrogen regulation in endometrial carcinoma cell lines.Biol. Reprod.48:1120–1128.

    Article  PubMed  CAS  Google Scholar 

  • Chegini, N., Rossi, M., and Masterson, B. 1992. Platelet-derived growth factor (PDGF), epidermal growth factor (EGF), and EGF and PDGF beta-receptors in human endometrial tissue: localization and in vitro action.Endocrinology130:2373–2385.

    Article  PubMed  CAS  Google Scholar 

  • Chew, P., Peh, K., Loganath, A., Gunasegaram, R., and Ratnam, S. 1990. Elevated peritoneal fluid luteinizing hormone and prolactin concentrations in infertile women with endometriosis.Int. J. Gynaecol. Obstet.33:35–39.

    Article  PubMed  CAS  Google Scholar 

  • Cohen, T., Nahari, D., Cerem, L. W., Neufeld, G., and Levi, B. Z. 1996. Interleukin 6 induces the expression of vascular endothelial growth factor.J. Biol. Chem.271:736–741.

    Article  PubMed  CAS  Google Scholar 

  • Cordon-Cardo, C., Vlodaysky, I., Haimovitz-Friedman, A., Hicklin, D., and Fuks, Z. 1990. Expression of basic fibroblast growth factor in normal human tissues.Lab. Invest.63:832–840.

    PubMed  CAS  Google Scholar 

  • Crum, R., Szabo, S., and Folkman, J. 1985. A new class of steroids inhibits angiogenesis in the presence of heparin or a heparin fragment.Science230:1375–1378.

    Article  PubMed  CAS  Google Scholar 

  • Cullinan-Bove, K., and Koos, R. 1993. Vascular endothelial growth factor/vascular permeability factor expression in the rat uterus: rapid stimulation by estrogen correlates with estrogen-induced increases in uterine capillary permeability and growth.Endocrinology133:829–837.

    Article  PubMed  CAS  Google Scholar 

  • Curtis, S., Washburn, T., Sewall, C., DiAugustine, R., Lindzey, J., and Couse, J. 1996. Physiological coupling of growth factor and steroid receptor signaling pathways: estrogen receptor knockout mice lack estrogen-like response to epidermal growth factor.Proc. Natl. Acad. Sci. USA93:12626–12630.

    Article  PubMed  CAS  Google Scholar 

  • D’Angelo, G., Martini, J. F., Iiri, T., Fand, W. J., Martial, J., and Weiner, R. I. 1999. 16K human prolactin inhibits vascular endothelial growth factor-induced activation of Ras in capillary endothelial cells.Mol. Endocrinol.13:692–704.

    Article  PubMed  Google Scholar 

  • D’Angelo, G., Struman, I., Martial, J., and Weiner, R. 1995. Activation of mitogen-activated protein kinases by vascular endothelial growth factor and basic fibroblast growth factor in capillary endothelial cells is inhibited by the antiangiogenic factor 16-kDa-terminal fragment of prolactin.Proc. Natl. Acad. Sci. USA92:6374–6378.

    Article  PubMed  Google Scholar 

  • Daniel, T., Liu, H., Morrow, J., Crews, B., and Marnett, L. 1999. Thromboxane A2 is a mediator of cyclooxygenase-2-dependent endothelial migration and angiogenesis.Cancer Res.59:4574–4577.

    PubMed  CAS  Google Scholar 

  • Davis, S., Aldrich, T., Jones, P., Acheson, A., Compton, L., and Jain, V. 1996. Isolation of angiopoietin-1, a ligand for the TIE2 receptor, by secretion-trap expression cloning.Cell87:1161–1169.

    Article  PubMed  CAS  Google Scholar 

  • D’Hooghe, T. M. 1997. Clinical relevance of the baboon as a model for the study of endometriosis.Fertil. Steril.68:613–625.

    Article  PubMed  Google Scholar 

  • Di Lieto, A., De Rosa, G., Albano, G., Staibano, S., Campanile, M., and Pontillo, M. 1997. Influence of goserelin depot therapy on epidermal growth factor receptor expression in pelvic endometriosis.Gynecol. Endocrinol.11:17–20.

    Article  PubMed  CAS  Google Scholar 

  • DiZerega, G., Barber, D., and Hodgen, G. 1980. Endometriosis: role of ovarian steroids in intiation, maintenance and suppression.Fertil. Steril.33:649–653.

    PubMed  CAS  Google Scholar 

  • Donnez, J., Smoes, P., Gillerot, S., Casanas-Roux, F., and Nisolle, M. 1998. Vascular endothelial growth factor (VEGF) in endometriosis.Hum. Reprod.13:1686–1690.

    Article  PubMed  CAS  Google Scholar 

  • Dumont, N., O’Connor-McCourt, M., and Philip, A. 1995. Transforming growth factor-beta receptors on human endometrial cells: identification of the type I, II, and III receptors and glycosyl-phosphatidylinositol anchored TGF-beta binding proteins.Mol. Cell. Endocrinol.111:57–66.

    Article  PubMed  CAS  Google Scholar 

  • Fakih, H., Baggett, B., Holtz, G., Tsang, K., Lee, J., and Williamson, H. 1987. Interleukin 1: a possible role in the infertility associated with endometriosis.Fertil. Steril.47:213–217.

    PubMed  CAS  Google Scholar 

  • Fernandez-Shaw, S., Marshall, J., Hicks, B., Barlow, D., and Starkey, P. 1995. Plasminogen activators in ectopic and uterine endometrium.Fertil. Steril.63:45–51.

    PubMed  CAS  Google Scholar 

  • Ferrara, N. 1999a. Role of vascular endothelial growth factor in the regulation of angiogenesis.Kidney Int.56:794–814.

    Article  CAS  Google Scholar 

  • Ferrara, N. 1999b. Vascular endothelial growth factor: molecular and biological aspects.Curr. Top. Microbiol. Immunol.237:1–30.

    Article  CAS  Google Scholar 

  • Ferrara, N., Clapp, C., and Weiner, R. 1991. The 16K fragment of prolactin specifically inhibits basal or fibroblast growth factor stimulated growth of capillary endothelial cells.Endocrinology129:896–900.

    Article  PubMed  CAS  Google Scholar 

  • Ferriani, R. A., Charnock-Jones, D. S., Prentice, A., Thomas, E. J., and Smith, S. K. 1993. Immunohistochemical localization of acidic and basic fibroblast growth factors in normal human endometrium and endometriosis and the detection of their mRNA by polymerase chain reaction.Hum. Reprod.8:11–16.

    PubMed  CAS  Google Scholar 

  • Folkman, J. 1995. Clinical applications of research on angiogenesis.N. Engl. J. Med.333:1757–1764.

    Article  PubMed  CAS  Google Scholar 

  • Folkman, J. 1997. Addressing tumor blood vessels.Nat. Biotechnol.15:510.

    Article  PubMed  CAS  Google Scholar 

  • Fujimoto, J., Sakaguchi, H., Hirose, R., and Tamaya, T. 1999. Expression of platelet-derived endothelial cell growth factor (PD-ECGF) related to angiogenesis in ovarian endometriosis.J. Clin. Endocrinol. Metab.84:359–362.

    Article  PubMed  CAS  Google Scholar 

  • Giudice, L., Dsupin, B., Gargosky, S., Rosenfeld, R., and Irwin, J. 1994. The insulin-like growth factor system in human peritoneal fluid: its effects on endometrial stromal cells and its potential relevance to endometriosis.J. Clin. Endocrinol. Metab.79:1284–1293.

    Article  PubMed  CAS  Google Scholar 

  • Giudice, L., Dsupin, B., Jin, I., Vu, T., and Hoffman, A. 1993. Differential expression of messenger ribonucleic acids encoding insulin-like growth factors and their receptors in human uterine endometrium and decidua.J. Clin. Endocrinol. Metab.76:1115–1122.

    Article  PubMed  CAS  Google Scholar 

  • Goldman, C., Kim, J., Wong, W., King, V., Brock, T., and Gillespie, G. Y. 1993. Epidermal growth factor stimulates vascular endothelial growth factor production by human malignant glioma cells: a model of glioblastoma multiforme pathophysiology.Mol. Biol. Cell4:121–133.

    PubMed  CAS  Google Scholar 

  • Gospodarowicz, D., Brown, K., Birdwell, C., and Zetter, B. 1978. Control of proliferation of human vascular endothelial cells. Characterization of the response of human umbilical vein endothelial cells to fibroblast growth factor, epidermal growth factor, and thrombin.J. Cell Biol.77:774–788.

    Article  PubMed  CAS  Google Scholar 

  • Greb, R., Heikinheimo, O., Williams, R., Hodgen, G., and Goodman, A. 1997. Vascular endothelial growth factor in primate endometrium is regulated by oestrogen-receptor and progesterone-receptor ligands in vivo.Hum. Reprod.12:1280–1292.

    Article  PubMed  CAS  Google Scholar 

  • Grimwood, J., Bicknell, R., and Rees, M. 1995. The isolation, characterization and culture of human decidual endothelium.Hum. Reprod.10:2142–2148.

    PubMed  CAS  Google Scholar 

  • Groothuis, P., Koks, C., de Goeij, A., Dunselman, G., Arends, J., and Evers, J. 1999. Adhesion of human endometrial fragments to peritoneum in vitro.Fertil. Steril.71:1119–1124.

    Article  PubMed  CAS  Google Scholar 

  • Gurgan, T., Bukulmez, O., Yarali, H., Tanir, M., and Akyildiz, S. 1999. Serum and peritoneal fluid levels of IGF I and II and insulinlike growth binding protein-3 in endometriosis. J.Reprod. Med.44:450–454.

    PubMed  CAS  Google Scholar 

  • Halme, J., Hammond, M., Hulka, J., Raj, S., and Talbert, L. 1984. Retrograde menstruation in healthy women and in patients with endometriosis.Obstet. Gynecol.64:151–154.

    PubMed  CAS  Google Scholar 

  • Halme, J., White, C., Kauma, S., Estes, J., and Haskill, S. 1988. Peritoneal macrophages from patients with endometriosis release growth factor activity in vitro.J. Clin. Endocrinol. Metab.66:1044–1049.

    Article  PubMed  CAS  Google Scholar 

  • Hanahan, D., and Folkman, J. 1996. Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis.Cell86:353–364.

    Article  PubMed  CAS  Google Scholar 

  • Harrington, D., Lessey, B., Rai, V., Bergqvist, A., Kennedy, S., and Manek, S. 1999. Tenascin is differentially expressed in endometrium and endometriosis.J. Pathol.187:242–248.

    Article  PubMed  CAS  Google Scholar 

  • Heldin, C., Backstrom, G., Ostman, A., Hammacher, A., Ronnstrand, L., and Rubin, K. 1988. Binding of different dimeric forms of PDGF to human fibroblasts: evidence for two separate receptor types.EMBOJ. 7:1387–1393.

    PubMed  CAS  Google Scholar 

  • Hill, J. 1992. Immunological factors in endometriosis and endometriosis-associated reproductive failure.Med. Clin. NorthAm. 3:583–596.

    Google Scholar 

  • Hooper, W. 1991. The role of transforming growth factor-beta in hematopoiesis. A review.Leuk. Res.15:179–184.

    Article  PubMed  CAS  Google Scholar 

  • Hornung, D., Lebovic, D., Shifren, J., Vigne, J., and Taylor, R. 1998. Vectorial secretion of vascular endothelial growth factor by polarized human endometrial epithelial cells.Fertil. Steril.69:909–915.

    Article  PubMed  CAS  Google Scholar 

  • Huang, J. C., Papasakelariou, C., Dawood, M. Y. 1996. Epidermal growth factor and basic fibroblast growth factor in peritoneal fluid of women with endometriosis.Fertil. Steril.65:931–944.

    PubMed  CAS  Google Scholar 

  • Huang, J., and Yeh, J. 1994. Quantitative analysis of epidermal growth factor receptor gene expression in endometriosis.J. Clin. Endocrinol. Metab.79:1097–1101.

    Article  PubMed  CAS  Google Scholar 

  • Imai, T., Kurachi, H., Adachi, K., Adachi, H., Yoshimoto, Y., and Homma, H. 1995. Changes in epidermal growth factor receptor and the levels of its ligands during menstrual cycle in human endometrium.Biol. Reprod.52:928–938.

    Article  PubMed  CAS  Google Scholar 

  • Iruela-Arispe, M., Porter, P., Bornstein, P., and Sage, E. 1996. Thrombospondin-1, an inhibitor of angiogenesis, is regulated by progesterone in the human endometrium.J. Clin. Invest.97:403–412.

    Article  PubMed  CAS  Google Scholar 

  • Iruela-Arispe, M. L., Rodriguez-Manzaneque, J. C., and Abu-Jawdeh, G. 1999. Endometrial endothelial cells express estrogen and progesterone receptors and exhibit a tissue specific response to angiogenic growth factors.Microcirculation6:127–140.

    PubMed  CAS  Google Scholar 

  • John, H., Preissner, K. T., Forssmann, W. G., and Ständker, L. 1999. Novel glycosylated forms of human plasma endostatin and circulating endostatin-related fragments of collagen XV.Biochemistry38:10217–10224.

    Article  PubMed  CAS  Google Scholar 

  • Karuri, A., Kumar, A., and Mukhopadhyay, D. 1998. Differential expression and selective localization of vascular permeability factor/vascular endothelial growth factor in the rat uterus during the estrous cycle.J. Endocrinol.159:488–499.

    Article  Google Scholar 

  • Keenan, J., Chen, T. T., Chadwell, N. L., Torry, D. S., and Caudle, M. R. 1994. Interferon-gamma (IFN-gamma) and interleukin-6 (IL-6) in peritoneal fluid and macrophage-conditioned media of women with endometriosis. Am.J. Reprod. Immunol.32:180–183.

    PubMed  CAS  Google Scholar 

  • Keenan, J. A., Chen, T. T., Chadwell, N. L., Torry, D. S., and Caudle, M. R. 1995. IL-1 beta, TNF-alpha, and IL-2 in peritoneal fluid and macrophage-conditioned media of women with endometriosis.Am. J. Reprod. Immunol.34:381–385.

    PubMed  CAS  Google Scholar 

  • Kennedy, S. 1999. The genetics of endometriosis.Eur. J. Obstet. Gynecol. Reprod. Biol.82:129–133.

    Article  PubMed  CAS  Google Scholar 

  • Khorram, O., Taylor, R., Ryan, I., Schall, T., and Landers, D. 1993. Peritoneal fluid concentrations of the cytokine RANTES correlate with the severity of endometriosis. Am.J. Obstet. Gynecol.169:1545–1549.

    PubMed  CAS  Google Scholar 

  • Kitamura, K., Kangawa, K., Matsuo, H., and Eto, T. 1995. Adrenomedullin. Implications for hypertension research.Drugs49:485–495.

    Article  PubMed  CAS  Google Scholar 

  • Klein, N., Pergola, G., Tekmal, R., Montoya, I., Dey, T., and Schenken, R. 1994. Cytokine regulation of cellular proliferation in endometriosis.Ann. NY Acad. Sci.734:322–332. Knudson, A. G. Jr. 1977. Genetics and etiology of human cancer.Adv. Hum. Genet.8:1–66.

    Google Scholar 

  • Koblizek, T. I., Weiss, C., Yancopoulos, G. D., Deutsch, U., and Risau, W. 1998. Angiopoietin-1 induces sprouting angiogenesis in vitro.Curr. Biol.8:529–532.

    Article  PubMed  CAS  Google Scholar 

  • Koch, A., Polverini, P., Kunkel, S., Harlow, L., Di Pietro, L., and Elner, V. 1992. Interleukin-8 as a macrophage-derived mediator of angiogenesis.Science258:1798–1801.

    Article  PubMed  CAS  Google Scholar 

  • Kruitwagen, R., Poels, L., Willemsen, W., de Ronde, I. J., Jap, P. H., and Rolland, R. 1991. Endometrial epithelial cells in peritoneal fluid during the early follicular phase.Fertil. Steril.55:297–303.

    PubMed  CAS  Google Scholar 

  • LaRosa, G., Thomas, K., Kaufmann, M., Mark, R., White, M., and Taylor, L. 1992. Amino terminus of the interleukin-8 receptor is a major determinant of receptor subtype specificity.J. Biol. Chem.267:25402–25406.

    PubMed  CAS  Google Scholar 

  • Le Roith, D. 1996. Insulin-like growth factor receptors and binding proteins.Baillieres Clin. Endocrinol. Metab.10:49–73.

    Google Scholar 

  • Lebovic, D., Bentzien, F., Chao, V., Garrett, E., Meng, Y., and Taylor, R. 2000. Induction of an angiogenic phenotype in endometriosis stromal cell cultures by interleukin-1ß.Mol. Hum. Reprod.6:269–275.

    Article  PubMed  CAS  Google Scholar 

  • Lebovic, D. I., Mueller, M. D., and Taylor, R. N. 1999. Vascular endothelial growth factor in reproductive biology. Curr.Opin. Obstet. Gynecol.11:255–260.

    Article  PubMed  CAS  Google Scholar 

  • Leek, R., Landers, R., Fox, S., Ng, F., Harris, A., and Lewis, C. 1998. Association of tumour necrosis factor alpha and its receptors with thymidine phosphorylase expression in invasive breast carcinoma.Br. J. Cancer77:2246–2251.

    Article  PubMed  CAS  Google Scholar 

  • Liu, Y., Cox, S., Morita, T., and Kourembanas, S. 1995. Hypoxia regulates vascular endothelial growth factor gene expression in endothelial cells. Identification of a 5’ enhancer.Circ. Res.77:638–643.

    Article  PubMed  CAS  Google Scholar 

  • Lundell, D., and Narula, S. 1994. Structural elements required for receptor recognition of human interferon-gamma.Pharm. Ther.64:1–21.

    Article  CAS  Google Scholar 

  • Maisonpierre, P., Suri, C., Jones, P., Bartunkova, S., Wiegand, S., and Radziejewski, C. 1997. Angiopoietin-2, a natural antagonist for Tie2 that disrupts in vivo angiogenesis.Science277:55–60.

    Article  PubMed  CAS  Google Scholar 

  • Malinak, L. R., Buttram, V. C., Jr., Elias, S., and Simpson, J. L. 1980. Heritage aspects of endometriosis. II. Clinical characteristics of familial endometriosis.Am. J. Obstet. Gynecol.137:332–337.

    PubMed  CAS  Google Scholar 

  • Markee, J. 1940. Menstruation in intraocular endometrial transplants in the rhesus monkey.Contrib. Embryol.177:220–230.

    Google Scholar 

  • Massagué, J., Cheifetz, S., Boyd, F., Boyd, F., and Andres, J. 1990. TGF-beta receptors and TGF-beta binding proteoglycans: recent progress in identifying their functional properties.Ann. NY Acad. Sci.593:59–72.

    Article  PubMed  Google Scholar 

  • Mateo, R. B., Reichner, J. S., and Albina, J. E. 1994. Interleukin-6 activity in wounds. Am.J. Physiol.266(6 pt 2): R1840–1844.

    PubMed  CAS  Google Scholar 

  • McLaren, J., Prentice, A., Charnock-Jones, D., and Smith, S. 1996a. Vascular endothelial growth factor (VEGF) concentrations are elevated in peritoneal fluid of women with endometriosis.Hum. Reprod.11:220–223.

    Article  CAS  Google Scholar 

  • McLaren, J., Prentice, A., Charnock-Jones, D., Millican, S., Muller, K., and Sharkey, A. 1996b. Vascular endothelial growth factor is produced by peritoneal fluid macrophages in endometriosis and is regulated by ovarian steroids.J. Clin. Invest.98:482–489.

    Article  CAS  Google Scholar 

  • Michishita, M., Minegishi, T., Abe, K., Kangawa, K., Kojima, M., and Ibuki, Y. 1999. Expression of adrenomedullin in the endometrium of the human uterus.Obstet. Gynecol.93:66–70.

    Article  PubMed  CAS  Google Scholar 

  • Miller, T. A., Bulman, A. L., Thompson, C. D., Garst, M. E., and Macdonald, T. L. 1997. Synthesis and structure-activity profiles of A-homoestranes, the estratropones.J. Med. Chem.40:3836–3841.

    Article  PubMed  CAS  Google Scholar 

  • Milne, S., Critchley, H., Drudy, T., Kelly, R., and Baird, D. 1999. Perivascular interleukin8 messenger ribonucleic acid expression in human endometrium varies across the menstrual cycle and in early pregnancy decidua.J. Clin. Endocrinol. Metab.84:2563–2567.

    Article  PubMed  CAS  Google Scholar 

  • Miyauchi, A., Momoeda, M., Nakabayashi, M., Osuga, Y., Yano, T., and Tsutsumi, O., et al. 1995. Regulation of the plasminogen activator/plasmin system by epidermal growth factor in cultured human endometrial cells.Hum. Reprod.10:3284–3288.

    PubMed  CAS  Google Scholar 

  • Moghaddam, A., Zhang, H. T., Fan, T. P., Hu, D. E., Lees, V. C., and Turley, H. 1995. Thymidine phosphorylase is angiogenic and promotes tumor growth.Proc. Natl. Acad. Sci. USA92:998–1002.

    Article  PubMed  CAS  Google Scholar 

  • Mori, H., Sawairi, M., Nakagawa, M., Itoh, N., Wada, K., and Tamaya, T. 1992. Expression of interleukin-1 (IL-1) beta messenger ribonucleic acid (mRNA) and IL-1 receptor antagonist mRNA in peritoneal macrophages from patients with endometriosis.Fertil. Steril.57:535–542.

    PubMed  CAS  Google Scholar 

  • Motro, B., Itin, A., Sachs, L., and Keshet, E. 1990. Pattern of interleukin 6 gene expression in vivo suggests a role for this cytokine in angiogenesis.Proc. Natl. Acad. Sci. USA87:3092–3096.

    Article  PubMed  CAS  Google Scholar 

  • Mueller, M. D., Lebovic, D. I., Garrett, E., and Taylor, R. N. 2000. Neutrophils infiltrating the endometrium express vascular endothelial growth factor (VEGF): potential role in endometrial angiogenesis.Fertil. Steril.74:107–112.

    Article  PubMed  CAS  Google Scholar 

  • Munson, L., Upadhyaya, N., and Van Meter, S. 1995. Platelet-derived growth factor promotes endometrial epithelial cell proliferation.Am. J. Obstet. Gynecol.173:1820–1825.

    Article  PubMed  CAS  Google Scholar 

  • Nelson, K., Takahashi, T., Bossert, N., Walmer, D., and McLachlan, J. 1991. Epidermal growth factor replaces estrogen in the stimulation of female genital-tract growth and differentiation.Proc. Natl. Acad. Sci. USA88:21–25.

    Article  PubMed  CAS  Google Scholar 

  • Nicosia, R., Nicosia, S., and Smith, M. 1994. Vascular endothelial growth factor, platelet-derived growth factor, and insulin-like growth factor-1 promote rat aortic angiogenesis in vitro. Am.J. Pathol.145:1023–1029.

    PubMed  CAS  Google Scholar 

  • Nisolle, M., Casanas Roux, B., Anaf, V., Mine, J., and Donnez, J. 1993. Morphometric study of the stromal vascularization in peritoneal endometriosis.Fertil. Steril.59:681–684.

    PubMed  CAS  Google Scholar 

  • Noyes, R., Hertig, A., and Rock, J. 1950. Dating the endometrial biopsy.Fertil. Steril.1:3–25.

    Google Scholar 

  • Odukoya, O. A., Ajjan, R., Lim, K., Watson, P. F., Weetman, A. P., and Cooke, I. D. 1997. The pattern of cytokine mRNA expression in ovarian endometriomata.Mol. Hum. Reprod.3:393–397.

    Article  PubMed  CAS  Google Scholar 

  • Olive, D., Montoya, I., Riehl, R., and Schenken, R. 1991. Macrophage-conditioned media enhance endometrial stromal cell proliferation in vitro. Am.J. Obstet. Gynecol.164:953–958.

    PubMed  CAS  Google Scholar 

  • Oosterlynck, D. J., Meuleman, C., Sobis, H., Vandeputte, M., and Koninckx, P. R. 1993. Angiogenic activity of peritoneal fluid from women with endometriosis.Fertil. Steril.59:778–782.

    PubMed  CAS  Google Scholar 

  • Oosterlynck, D., Meuleman, C., Waer, M., and Koninckx, P. 1994. Transforming growth factor-beta activity is increased in peritoneal fluid from women with endometriosis.Obstet. Gynecol.83:287–292.

    PubMed  CAS  Google Scholar 

  • O’Reilly, M. S., Boehm, T., Shing, Y., Fukai, N., Vasios, G., and Lane, W. S. 1997. Endo-statin: an endogenous inhibitor of angiogenesis and tumor growth.Cell88:277–285.

    Article  PubMed  Google Scholar 

  • O’Reilly, M. S., Homgren, L., Shing, Y., Chen, C., Rosenthal, R, and Moses, M. 1994. Angiostatin: a novel angiogenesis inhibitor that mediates the suppression of metastases by a Lewis lung carcinoma.Cell88:1–20.

    Google Scholar 

  • Osteen, K., Bruner, K., and Sharpe-Timms, K. 1996. Steroid and growth factor regulation of matrix metalloproteinase expression and endometriosis.Semin. Reprod. Endocrinol.14:247–255.

    Article  PubMed  CAS  Google Scholar 

  • Osuga, Y., Toyoshima, H., Mitsuhashi, N., and Taketani, Y. 1995. The presence of platelet-derived endothelial cell growth factor in human endometrium and its characteristic expression during the menstrual cycle and early gestational period.Hum. Reprod.10:989–993.

    PubMed  CAS  Google Scholar 

  • Patterson, C., Perrella, M., Endege, W., Yoshizumi, M., Lee, M., and Haber, E. 1996. Down-regulation of vascular endothelial growth factor receptors by tumor necrosis factor-alpha in cultured human vascular endothelial cells.J. Clin. Invest.98:490–496.

    Article  PubMed  CAS  Google Scholar 

  • Perrot-Applanat, M., Deng, M., Fernandez, H., Lelaidier, C., Meduri, G., and Bouchard, P. 1994. Immunohistochemical localization of estradiol and progesterone receptors in human uterus throughout pregnancy: expression in endometrial blood vessels.J. Clin. Endocrinol. Metab.78:216–224.

    Article  PubMed  CAS  Google Scholar 

  • Peters, K. G. 1998. Vascular endothelial growth factor and the angiopoietins: working together to build a better blood vessel. Circ.Res.83:342–343.

    CAS  Google Scholar 

  • Peters, K., Coogan, A., Berry, D., Marks, J., Iglehart, J., and Kontos, C. 1998. Expression of Tie2/Tek in breast tumour vasculature provides a new marker for evaluation of tumour angiogenesis.Br. J. Cancer77:51–56.

    Article  PubMed  CAS  Google Scholar 

  • Piva, M., and Sharpe-Timms, K. L. 1999. Peritoneal endometriotic lesions differentially express a haptoglobin-like gene.Mol. Hum. Reprod.5:71–78.

    Article  PubMed  CAS  Google Scholar 

  • Presta, M. 1988. Sex hormones modulate the synthesis of basic fibroblast growth factor in human endometrial adenocarcinoma cells: implications for the neovascularization of normal and neoplastic endometrium.J. Cell Physiol.137:593–597.

    Article  PubMed  CAS  Google Scholar 

  • Rana, N., Braun, D. P., House, R., Gebel, H., Rotman, C., and Dmowski, W. P. 1996. Basal and stimulated secretion of cytokines by peritoneal macrophages in women with endometriosis.Fertil. Steril.65:925–930.

    PubMed  CAS  Google Scholar 

  • Redwine, D. 1988. Mülleriosis: the single best-fit model of the origin of endometriosis.J. Reprod. Med.33:915–920.

    Google Scholar 

  • Rier, S. E., Martin, D. C., Bowman, R. E., Dmowski, W. P., and Becker, J. L. 1993. Endometriosis in rhesus monkeys(Macaca mulatta)following chronic exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin.Fundam. Appl. Toxicol.21:433–441.

    Article  PubMed  CAS  Google Scholar 

  • Ryan, I. P., Schriock, E. D., and Taylor, R. N. 1994. Isolation, characterization, and comparison of human endometrial and endometriosis cells in vitro.J. Clin. Endocrinol. Metab.78:642–649.

    Article  PubMed  CAS  Google Scholar 

  • Ryan, I., and Taylor, R. 1997. Endometriosis and infertility: new concepts.Obstet. Gynecol. Surv.52:365–371.

    Article  PubMed  CAS  Google Scholar 

  • Ryan, I., Tseng, J., Schriock, E., Khorram, O., Landers, D., and Taylor, R. 1995. Interleukin8 concentrations are elevated in peritoneal fluid of women with endometriosis.Fertil. Steril.63:929–932.

    PubMed  CAS  Google Scholar 

  • Salat-Baroux, J., Romain, S., Alvarez, S., Antoine, J., Kopp, K., and Raulais, D. 1994. Biochemical and immunohistochemical multiparametric analysis of steroid receptors and growth factor receptors in human normal endometrium in spontaneous cycles and after the induction of ovulation.Hum. Reprod.9:200–208.

    PubMed  CAS  Google Scholar 

  • Sampson, J. 1927. Peritoneal endometriosis due to the menstrual dissemination of endometrial tissue into the peritoneal cavity.Am. J. Obstet. Gynecol.14:422–469.

    Google Scholar 

  • Sangha, R., Li, X., Shams, M., and Ahmed, A. 1997. Fibroblast growth factor receptor-1 is a critical component for endometrial remodeling: localization and expression of basic fibroblast growth factor and FGF-R1 in human endometrium during the menstrual cycle and decreased FGF-R1 expression in menorrhagia.Lab. Invest.77:389–402.

    PubMed  CAS  Google Scholar 

  • Schriock, E., Monroe, S., Henzl, M., and Jaffe, R. 1985. Treatment of endometriosis with a potent agonist of gonadotropin-releasing hormone (nafarelin).Fertil. Steril.44:583588.

    Google Scholar 

  • Seli, E., Zeyneloglu, H. B., Senturk, L. M., Bahtiyar, O. M., Olive, D. L., and Arici, A. 1998. Basic fibroblast growth factor: peritoneal and follicular fluid levels and its effect on early embryonic development.Fertil. Steril.69:1145–1148.

    Article  PubMed  CAS  Google Scholar 

  • Sharpe, K. L., and Vernon, M. W. 1993. Polypeptides synthesized and released by rat ectopic uterine implants differ from those of the uterus in culture.Biol. Reprod.48:1334–1340.

    Article  PubMed  CAS  Google Scholar 

  • Sharpe, K., Zimmer, R., Griffin, W., and Penney, L. 1993. Polypeptides synthesized and released by human endometriosis differ from those of the uterine endometrium in cell and tissue explant culture.Fertil. Steril.60:839–851.

    PubMed  CAS  Google Scholar 

  • Sharpe-Timms, K. L. 1997. Basic research in endometriosis.Obstet. Gynecol. Clin. North Am.24:269–290.

    Article  PubMed  CAS  Google Scholar 

  • Sharpe-Timms, K. L., Penney, L. L., Zimmer, R. L., Wright, J. A., Zhang, Y., and Surewicz, K. 1995. Partial purification and amino acid sequence analysis of endometriosis protein-II (ENDO-II) reveals homology with tissue inhibitor of metalloproteinases-1 (TIMP-1).J. Clin. Endocrinol. Metab.80:3784–3787.

    Article  PubMed  CAS  Google Scholar 

  • Shifren, J., Tseng, J., Zaloudek, C., Ryan, I., Meng, Y., and Ferrara, N. 1996. Ovarian steroid regulation of vascular endothelial growth factor in the human endometrium: implications for angiogenesis during the menstrual cycle and in the pathogenesis of endometriosis.J. Clin. Endocrinol. Metab.81:3112–3118.

    Article  PubMed  CAS  Google Scholar 

  • Shimazawa, R., Miyachi, H., Takayama, H., Kuroda, K., Kato, F., and Kato, M. 1993. Antiangiogenic activity of tumor necrosis factor-alpha production regulators derived from thalidomide.Biol. Pharmaceut. Bull.22:224–226.

    Article  Google Scholar 

  • Shimekake, Y., Nagata, K., Ohta, S., Kambayashi, Y., Teraoka, H., and Kitamura, K. 1995. Adrenomedullin stimulates two signal transduction pathways, cAMP accumulation and Ca’ mobilization, in bovine aortic endothelial cells.J. Biol. Chem.270:4412–4417.

    Article  PubMed  CAS  Google Scholar 

  • Sillem, M., Prifti, S., Neher, M., and Runnebaum, B. 1998. Extracellular matrix remodelling in the endometrium and its possible relevance to the pathogenesis of endometriosis.Hum. Reprod. Update4:730–735.

    Article  PubMed  CAS  Google Scholar 

  • Simón, C., Frances, A., and Piquette, G. 1994. The immune mediator interleukin-1 receptor antagonist (IL-lra) preevents embryo implantation.Endocrinology134:521–528.

    Article  PubMed  Google Scholar 

  • Simón, C., Piquette, G., Frances, A., Westphal, L., Heinrichs, W., and Polan, M. 1993. Interleukin-1 type I receptor messenger ribonucleic acid expression in human endometrium throughout the menstrual cycle.Fertil. Steril.59:791–796.

    PubMed  Google Scholar 

  • Singer, G. A., Strowitzki, T., Rettig, I., and Kimmig, R. 1998. Flow cytometric detection and binding studies of human endometrial stromal cell epidermal growth factor receptor in monolayer culture: influence of progesterone.Mol. Hum. Reprod.4:577–583.

    Article  PubMed  CAS  Google Scholar 

  • Surrey, E., and Halme, J. 1991. Effect of platelet-derived growth factor on endometrial stromal cell proliferation in vitro: a model for endometriosis?Fertil. Steril.56:672–679.

    PubMed  CAS  Google Scholar 

  • Tabibzadeh, S. 1990. Evidence of T cell activation and potential cytokine action in human endometrium.J. Clin. Endocrinol. Metab.71:645–653.

    Article  PubMed  CAS  Google Scholar 

  • Tabibzadeh, S. 1991. Human endometrium: an active site of cytokine production and action.Endocr. Rev.1991:272–290.

    Article  Google Scholar 

  • Tabibzadeh, S., Gerber, M., and Satyaswaroop, P. 1986. Induction of HLA-DR antigen expression in human endometrial epithelial cells in vitro by recombinant gamma-interferon.Am. J. Pathol.125:90–96.

    PubMed  CAS  Google Scholar 

  • Tabibzadeh, S., Kong, Q. F., Babaknia, A., and May, L. T. 1995. Progressive rise in the expression of interleukin-6 in human endometrium during menstrual cycle is initiated during the implantation window.Hum. Reprod.10:2793–2799.

    PubMed  CAS  Google Scholar 

  • Tabibzadeh, S., Satyaswaroop, P., and Rao, P. 1988. Antiproliferative effect of interferon-g in human endometrial epithelial cell in vitro: potential local growth modulatory role in endometrium.J. Clin. Endocrinol. Metab.67:131–138.

    Article  PubMed  CAS  Google Scholar 

  • Taketani, Y., Kuo, T. M., and Mizuno, M. 1992. Comparison of cytokine levels and embryo toxicity in peritoneal fluid in infertile women with untreated or treated endometriosis.Am. J. Obstet. Gynecol.167:265–270.

    PubMed  CAS  Google Scholar 

  • Tang, X., Rossi, M., Masterson, B., and Chegini, N. 1994a. Insulin-like growth factor I (IGF-I), IGF-I receptors, and IGF binding proteins 1–4 in human uterine tissue: tissue localization and IGF-I action in endometrial stromal and myometrial smooth muscle cells in vitro.Biol. Reprod.50:1113–1125.

    Article  CAS  Google Scholar 

  • Tang, X., Zhao, Y., Rossi, M., Abu-Rustum, R., Ksander, G., and Chegini, N. 1994b. Expression of transforming growth factor-beta (TGF beta) isoforms and TGF beta type II receptor messenger ribonucleic acid and protein, and the effect of TGF betas on endometrial stromal cell growth and protein degradation in vitro.Endocrinology135:4450–4459.

    Google Scholar 

  • Tao, X. J., Sayegh, R. A., and Isaacson, K. B. 1997. Increased expression of complement component 3 in human ectopic endometrium compared with the matched eutopic endometrium.Fertil. Steril.68:460–467.

    Article  PubMed  CAS  Google Scholar 

  • Taylor, R., Ryan, I., Moore, E., Hornung, D., Shifren, J., and Tseng, J. 1997. Angiogenesis and macrophage activation in endometriosis.Ann. NY Acad. Sri.828:194–207.

    Article  CAS  Google Scholar 

  • Taylor, R., Ryan, I., Tseng, J., Shifren, J., Hornung, D., and Lebovic, D. 1999. Ovarian steroids and angiogenesis. In: Lemay, A., and Maheux, R., eds.Understanding Endometriosis: Advances in Research and Practice.Parthenon, Carnforth., UK pp. 131–137.

    Google Scholar 

  • Telgmann, R., and Gellersen, B. 1998. Marker genes of decidualization: activation of the decidual prolactin gene.Hum. Reprod. Update4:472–479.

    Article  PubMed  CAS  Google Scholar 

  • Treloar, S., O’Connor, D., O’Connor, V., and Martin, N. 1999. Genetic influences on endometriosis in an Australian twin sample.Fenil. Steril.71:701–710.

    Article  CAS  Google Scholar 

  • Tseng, J., Ryan, I., Milam, T., Murai, J., Schriock, E., and Landers, D. 1996. Interleukin-6 secretion in vitro is up-regulated in ectopic and eutopic endometrial stromal cells from women with endometriosis.J. Clin. Endocrinol. Metab.81:1118–1122.

    Article  PubMed  CAS  Google Scholar 

  • Tsuruoka, N., Sugiyama, M., Tawaragi, Y., Tsujimoto, M., Nishihara, T., and Goto, T. 1988. Inhibition of in vitro angiogenesis by lymphotoxin and interferon-gamma.Biochem. Biophys. Res. Commun.155:429–435.

    Article  PubMed  CAS  Google Scholar 

  • Upton, P., Austin, C., Taylor, G., Nandha, K., Clark, A., and Ghatei, M. 1997. Expression of adrenomedullin (ADM) and its binding sites in the rat uterus: Increased number of binding sites and ADM messenger ribonucleic acid in 20-day pregnant rats compared with nonpregnant rats.Endocrinology138:2508–2514.

    Article  PubMed  CAS  Google Scholar 

  • Vandermolen, D. T., and Gu, Y. 1996. Human endometrial interleukin-6 (IL-6): in vivo messenger ribonucleic acid expression, in vitro protein production, and stimulation thereof by IL-1 beta.Fertil. Steril.66:741–747.

    PubMed  CAS  Google Scholar 

  • Vazquez, F., Rodraiguez-Manzaneque, J. C., Lydon, J. P., Edwards, D. P., O’Malley, B. W., and Iruela-Arispe, M. L. 1999. Progesterone regulates proliferation of endothelial cells.J. Biol. Chem.274:2185–2192.

    Article  PubMed  CAS  Google Scholar 

  • Watson, H., Franks, S., and Bonney, R. C. 1996. Regulation of epidermal growth factor receptor synthesis by ovarian steroids in human endometrial cells in culture.J. Reprod. Fertil.107:199–205.

    Article  PubMed  CAS  Google Scholar 

  • Williams, L. 1989. Signal transduction by the platelet-derived growth factor receptor.Science243:1564–1570.

    Article  PubMed  CAS  Google Scholar 

  • Witz, C. A., Monotoya-Rodriguez, I. A., and Schenken, R. S. 1999. Whole explants of peritoneum and endometrium: a novel model of the early endometriosis lesion.Fertil. Steril.71:56–60.

    Article  PubMed  CAS  Google Scholar 

  • Wu, M. H., Yang, B. C., Hsu, C. C., Lee, Y. C., and Huang, K. E. 1998. The expression of soluble intercellular adhesion molecule-1 in endometriosis.Fertil. Steril.70:1139–1142.

    Article  PubMed  CAS  Google Scholar 

  • Zetter, B. R. 1998. Angiogenesis and tumor metastasis.Annu. Rev. Med.49:407–424.

    Article  PubMed  CAS  Google Scholar 

  • Zhang, L., Mackenzie, I., Rees, M., and Bicknell, R. 1997. Regulation of the expression of the angiogenic enzyme platelet-derived endothelial cell growth factor/thymidine phosphorylase in endometrial isolates by ovarian steroids and cytokines.Endocrinology138:4921–4930.

    Article  PubMed  CAS  Google Scholar 

  • Zhang, L., Scott, P., Turley, H., Leek, R., Lewis, C., and Gatter,K. 1998.Validation of anti-vascular endothelial growth factor (anti-VEGF) antibodies for immunohistochemical localization of VEGF in tissue sections: expression of VEGF in the human endometrium.J. Pathol. 185:402–408.

    Article  PubMed  CAS  Google Scholar 

  • Zhou, J., Dsupin, B., Giudice, L., and Bondy, C.1994.Insulin-like growth factor system gene expression in human endometrium during the menstrual cycle.J. Clin. Endocrinol. Metab. 79:1723–1734.

    Article  PubMed  CAS  Google Scholar 

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Mueller, M.D., Taylor, R.N. (2001). Angiogenesis in Endometriosis. In: Augustin, H.G., Rogers, P.A.W., Iruela-Arispe, M.L., Smith, S.K. (eds) Vascular Morphogenesis in the Female Reproductive System. Cardiovascular Molecular Morphogenesis. Birkhäuser, Boston, MA. https://doi.org/10.1007/978-1-4612-0213-4_13

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