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Geburtshilfe Frauenheilkd 2000; 60(12): 585-593
DOI: 10.1055/s-2000-9542
Übersicht

Georg Thieme Verlag Stuttgart · New York

Auf der Spur eines Rätsels: Angiogenese und Endometriose

Endometriosis and Angiogenesis: On the Tail of a RiddleM. D. Mueller1 , E. Dreher1 , R. N. Taylor2
  • 1 Endometriose-Zentrum, Universitäts-Frauenklinik, Inselspital Bern
  • 2 Center for Reproductive Sciences, University of California San Francisco
Further Information

Publication History

Publication Date:
31 December 2000 (online)

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Zusammenfassung

Endometriose ist ein komplexes Krankheitsbild, dessen Pathogenese rätselhaft ist. Praktisch mit jedem Zyklus gelangen Endometriosezellen durch retrograde Menstruation in die Abdominalhöhle. Ein Ansiedeln dieser Zellen in ektopem Gewebe kommt wahrscheinlich nur bei Frauen vor, bei welchen eine Dysregulation der umgebenden intraperitonealen Abwehrmechanismen vorliegt. Die erhöhten Konzentrationen an aktivierten Makrophagen, Lymphozyten, Zytokinen und Wachstumsfaktoren, welche in der peritonealen Flüssigkeit von Endometriose-Patientinnen nachgewiesen werden, sprechen zugunsten dieser Hypothese. In der vorliegenden Übersicht schlagen wir ein Modell vor, welches das komplexe Zusammenspiel der lokal produzierten Zytokine, Wachstumsfaktoren, Sexualhormone und Eikosanoide im Wachstumsprozess und in der damit verbundenen Gefäßneubildung dieser ektopischen Endometrium-Herde zusammenfasst. Die erhöhte lokale Sekretion von angiostimulatorischen Proteinen durch Endometrioseherde und deren begleitenden Immunzellen fördern die Rekrutierung von Kapillaren zum Ort des Wachstums der anwachsenden Läsionen. Zukünftige Therapien, welche diese angiostimulatorischen Faktoren bekämpfen und somit das Potenzial haben, die vaskuläre Pathogenese der Endometriose zu blockieren, werden ebenfalls erwähnt.

Summary

Endometriosis is a complex condition with an enigmatic pathogenesis. While retrograde passage of endometrial cells into the abdominal cavity during menstruation occurs in most women, implantation of these cells at ectopic sites appears to occur only in those with altered intraperitoneal defense mechanisms. The peritoneal fluid of women with endometriosis contains increased levels of activated macrophages, lymphocytes, cytokines and growth factors. We describe a model which integrates the complex interactions among locally produced cytokines, growth factors, sex steroid hormones, and eicosanoids in the growth and angiogenesis of endometriotic foci. Increased local secretion of angiostimulatory proteins by endometriotic deposits and accompanying immunologic cells promote the local growth of capillaries. Future therapeutic strategies may aim to counter these angiostimulatory factors.

Literatur

  • 1 Adams J. Thrombospondin-1.  Int J Biochem Cell Biol. 1997;  29 861-865
    CrossrefPubMedGoogle Scholar
  • 2 Ahmed A, Acevedo C, Nijjar S, Alpin J, Yancopoulos G, Shams M. Angiopoietin-1 and Tie-2 are downregulated in dysfunctional uterine bleeding.  J Soc Gynecol Investig. 2000;  7 (Suppl 1) 57
    PubMedGoogle Scholar
  • 3 Arici A, Tazuke S I, Attar E, Kliman H J, Olive D L. Interleukin-8 concentration in peritoneal fluid of patients with endometriosis and modulation of interleukin-8 expression in human mesothelial cells.  Mol Hum Reprod. 1996;  2 (1) 40-45
    CrossrefPubMedGoogle Scholar
  • 4 Augustin H, Kuhn W S. Zyklische Angiogenese-Prozesse im Ovar.  Gynaekologe. 1999;  32 582-589
    PubMedGoogle Scholar
  • 5 Ben-Av P, Crofford L J, Wilder R L, Hla T. Induction of vascular endothelial growth factor expression in synovial fibroblasts by prostaglandin E and interleukin-1: a potential mechanism for inflammatory angiogenesis.  FEBS Lett. 1995;  372 (1) 83-87
    CrossrefPubMedGoogle Scholar
  • 6 Brogi E, Wu T, Namiki A, Isner J. Indirect angiogenic cytokines upregulate VEGF and bFGF gene expression in vascular smooth muscle cells, whereas hypoxia upregulates VEGF expression only.  Circulation. 1994;  90 649-652
    CrossrefPubMedGoogle Scholar
  • 7 Brosens I, Donnez J. Current status of endometriosis. Carnforth; Parthenon Publishing 1993
    Google Scholar
  • 8 Bulmer J, Longfellow M, Ritson A. Leukocytes and resident blood cells in endometrium.  Ann NY Acad Sci. 1991;  622 57-68
    PubMedGoogle Scholar
  • 9 Charnock-Jones D, Sharkey A, Rajput-Williams J, Burch D, Schofield J, Fountain S. et al . 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. 1993;  48 (5) 1120-1128
    CrossrefPubMedGoogle Scholar
  • 10 Cordon-Cardo C, Vlodavsky I, Haimovitz-Friedman A, Hicklin D, Fuks Z. Expression of basic fibroblast growth factor in normal human tissues.  Lab Invest. 1990;  63 832-840
    PubMedGoogle Scholar
  • 11 Crum R, Szabo S, Folkman J. A new class of steroids inhibits angiogenesis in the presence of heparin or a heparin fragment.  Science. 1985;  230 (4732) 1375-1378
    PubMedGoogle Scholar
  • 12 Cullinan-Bove K, Koos R. 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.  Endocrinology. 1993;  133 (2) 829-837
    CrossrefPubMedGoogle Scholar
  • 13 Curtis S, Washburn T, Sewall C, DiAugustine R, Lindzey J, Couse J. et al . 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 USA. 1996;  93 12626-12630
    CrossrefPubMedGoogle Scholar
  • 14 Daniel T, Liu H, Morrow J, Crews B, Marnett L. Thromboxane A2 is a mediator of cyclooxygenase-2-dependent endothelial migration and angiogenesis.  Cancer Res. 1999;  59 (18) 4574-4577
    PubMedGoogle Scholar
  • 15 Davis S, Aldrich T, Jones P, Acheson A, Compton L, Jain V. et al . Isolation of angiopoietin-1, a ligand for the TIE2 receptor, by secretion-trap expression cloning.  Cell. 1996;  87 1161-1169
    CrossrefPubMedGoogle Scholar
  • 16 D'Hooghe T M. Clinical relevance of the baboon as a model for the study of endometriosis.  Fertil Steril. 1997;  68 (4) 613-625
    CrossrefPubMedGoogle Scholar
  • 17 Di Lieto A, De Rosa G, Albano G, Staibano S, Campanile M, Pontillo M. et al . Influence of goserelin depot therapy on epidermal growth factor receptor expression in pelvic endometriosis.  Gynecol Endocrinol. 1997;  11 (1) 17-20
    PubMedGoogle Scholar
  • 18 DiZerega G, Barber D, Hodgen G. Endometriosis: role of ovarian steroids in intiation, maintenance and suppression.  Fertil Steril. 1980;  33 649-653
    PubMedGoogle Scholar
  • 19 Donnez J, Smoes P, Gillerot S, Casanas-Roux F, Nisolle M. Vascular endothelial growth factor (VEGF) in endometriosis.  Hum Reprod. 1998;  13 (6) 1686-1690
    CrossrefPubMedGoogle Scholar
  • 20 Drake T, Grunert G. The unsuspected pelvic factor in the infertility investigation.  Fertil Steril. 1980;  34 27-31
    PubMedGoogle Scholar
  • 21 Fernandez-Shaw S, Marshall J, Hicks B, Barlow D, Starkey P. Plasminogen activators in ectopic and uterine endometrium.  Fertil Steril. 1995;  63 (1) 45-51
    PubMedGoogle Scholar
  • 22 Ferrara N, Clapp C, Weiner R. The 16 K fragment of prolactin specifically inhibits basal or fibroblast growth factor stimulated growth of capillary endothelial cells.  Endocrinology. 1991;  129 (2) 896-900
    PubMedGoogle Scholar
  • 23 Ferrara N, Houck K, Jakeman L, Winer J, Leung D. The vascular endothelial growth factor family of polypeptides.  J Cell Biochem. 1991;  47 211-218
    CrossrefPubMedGoogle Scholar
  • 24 Ferriani R A, Charnock-Jones D S, Prentice A, Thomas E J, Smith S K. 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. 1993;  8 (1) 11-16
    PubMedGoogle Scholar
  • 25 Folkman J. The role of angiogenesis in tumor growth.  Semin Cancer Biol. 1992;  3 (2) 65-71
    PubMedGoogle Scholar
  • 26 Folkman J. Clinical applications of research on angiogenesis.  N Engl J Med. 1995;  333 1757-1764
    CrossrefPubMedGoogle Scholar
  • 27 Folkman J. Addressing tumor blood vessels.  Nature Biotechnol. 1997;  15 510
    CrossrefPubMedGoogle Scholar
  • 28 Fujimoto J, Sakaguchi H, Hirose R, Tamaya T. Expression of platelet-derived endothelial cell growth factor (PD-ECGF) related to angiogenesis in ovarian endometriosis.  J Clin Endocrinol Metab. 1999;  84 (1) 359-362
    CrossrefPubMedGoogle Scholar
  • 29 Giudice L, Dsupin B, Gargosky S, Rosenfeld R, Irwin J. The insulin-like growth factor system in human peritoneal fluid: its effects on endometrial stroma cells and its potential relevance to endometriosis.  J Clin Endocrinol Metab. 1994;  79 (5) 1284-1293
    CrossrefPubMedGoogle Scholar
  • 30 Giudice L, Dsupin B, Jin I, Vu T, Hoffman A. Differential expression of messenger ribonucleic acids encoding insulin-like growth factors and their receptors in human uterine endometrium and decidua.  J Clin Endocrinol Metab. 1993;  76 1115-1122
    CrossrefPubMedGoogle Scholar
  • 31 Goldman C, Kim J, Wong W, King V, Brock T, Gy G. Epidermal human factor stimulates vascular endothelial growth factor production by human malignant gliom cells: a model of glioblastoma multiforme pathophysiology.  Mol Biol Cell. 1993;  4 121-133
    PubMedGoogle Scholar
  • 32 Gospodarowicz D, Brown K, Birdwell C, Zetter B. 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. 1978;  77 (3) 774-788
    CrossrefPubMedGoogle Scholar
  • 33 Groothuis P, Koks C, de Goeij A, Dunselman G, Arends J, Evers J. Adhesion of human endometrial fragments to peritoneum in vitro.  Fertil Steril. 1999;  71 (6) 1119-1124
    CrossrefPubMedGoogle Scholar
  • 34 Gurgan T, Bukulmez O, Yarali H, Tanir M, Akyildiz S. Serum and peritoneal fluid levels of IGF I and II and insulinlike growth binding protein-3 in endometriosis.  J Reprod Med. 1999;  44 (5) 450-454
    PubMedGoogle Scholar
  • 35 Halme J, Hammond M, Hulka J, Raj S, Talbert L. Retrograde menstruation in healthy women and in patients with endometriosis.  Obstet Gynecol. 1984;  64 (2) 151-154
    PubMedGoogle Scholar
  • 36 Halme J, White C, Kauma S, Estes J, Haskill S. Peritoneal macrophages from patients with endometriosis release growth factor activity in vitro.  J Clin Endocrinol Metab. 1988;  66 1044-1049
    CrossrefPubMedGoogle Scholar
  • 37 Hanahan D, Folkman J. Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis.  Cell. 1996;  86 353-364
    CrossrefPubMedGoogle Scholar
  • 38 Harrington D, Lessey B, Rai V, Bergqvist A, Kennedy S, Manek S. et al . Tenascin is differentially expressed in endometrium and endometriosis.  J Pathol. 1999;  187 (2) 242-248
    PubMedGoogle Scholar
  • 39 Hill J. Immunological factors in endometriosis and endometriosis-associated reproductive failure.  Med Clin North Am. 1992;  3 583-596
    PubMedGoogle Scholar
  • 40 Huang J C, Papasakelariou C, Dawood M Y. Epidermal growth factor and basic fibroblast growth factor in peritoneal fluid of women with endometriosis.  Fertil Steril. 1996;  65 (5) 931-934
    PubMedGoogle Scholar
  • 41 Imai T, Kurachi H, Adachi K, Adachi H, Yoshimoto Y, Homma H. et al . Changes in epidermal growth factor receptor and the levels of its ligands during menstrual cycle in human endometrium.  Biol Reprod. 1995;  52 (4) 928-938
    PubMedGoogle Scholar
  • 42 Iruela-Arispe M, Porter P, Bornstein P, Sage E. Thrombospondin-1, an inhibitor of angiogenesis, is regulated by progesterone in the human endometrium.  J Clin Invest. 1996;  97 (2) 403-412
    PubMedGoogle Scholar
  • 43 Iruela-Arispe M L, Rodriguez-Manzaneque J C, Abu-Jawdeh G. Endometrial endothelial cells express estrogen and progesterone receptors and exhibit a tissue specific response to angiogenic growth factors.  Microcirculation. 1999;  6 (2) 127-140
    CrossrefPubMedGoogle Scholar
  • 44 Keenan J, Chen T T, Chadwell N L, Torry D S, Caudle M R. Interferon-gamma (IFN-gamma) and interleukin-6 (IL-6) in peritoneal fluid and macrophage-conditioned media of women with endometriosis.  Am J Reprod Immunol. 1994;  32 (3) 180-183
    PubMedGoogle Scholar
  • 45 Keenan J A, Chen T T, Chadwell N L, Torry D S, Caudle M R. IL-1 beta, TNF-alpha, and IL-2 in peritoneal fluid and macrophage-conditioned media of women with endometriosis.  Am J Reprod Immunol. 1995;  34 (6) 381-385
    PubMedGoogle Scholar
  • 46 Kennedy S. The genetics of endometriosis.  Eur J Obstet Gynecol Reprod Biol. 1999;  82 (2) 129-133
    CrossrefPubMedGoogle Scholar
  • 47 Khorram O, Taylor R, Ryan I, Schall T, Landers D. Peritoneal fluid concentrations of the cytokine RANTES correlate with the severity of endometriosis.  Am J Obstet Gynecol. 1993;  169 (6) 1545-1549
    CrossrefPubMedGoogle Scholar
  • 48 Koch A, Polverini P, Kunkel S, Harlow L, DiPietro L, Elner V. et al . Interleukin-8 as a macrophage-derived mediator of angiogenesis.  Science. 1992;  258 1798-1801
    PubMedGoogle Scholar
  • 49 Koninckx P R, Braet P, Kennedy S H, Barlow D H. Dioxin pollution and endometriosis in Belgium.  Hum Reprod. 1994;  9 (6) 1001-1002
    PubMedGoogle Scholar
  • 50 Kruitwagen R, Poels L. Willemsen W, et al. Endometrial epithelial cells in peritoneal fluid during the early follicular phase.  Fertil Steril. 1991;  55 297-303
    PubMedGoogle Scholar
  • 51 Lebovic D, Bentzien F, Chao V, Garrett E, Meng Y, Taylor R. Induction of an angiogenic phenotype in endometriosis stromal cell cultures by Interleukin-1β.  Mol Hum Reprod. 2000;  6 (3) 269-275
    CrossrefPubMedGoogle Scholar
  • 52 Lebovic D I, Mueller M D, Taylor R N. Vascular endothelial growth factor in reproductive biology.  Curr Opin Obstet Gynecol. 1999;  11 (3) 255-260
    CrossrefPubMedGoogle Scholar
  • 53 Leek R, Landers R, Fox S, Ng F, Harris A, Lewis C. Association of tumor necrosis factor alpha and its receptors with thymidine phosphorylase expression in invasive breast carcinoma.  Br J Cancer. 1998;  77 (12) 2246-2251
    PubMedGoogle Scholar
  • 54 Liu Y, Cox S, Morita T, Kourembanas S. Hypoxia regulates vascular endothelial growth factor gene expression in endothelial cells. Identification of a 5′ enhancer.  Circ Res. 1995;  77 638-643
    CrossrefPubMedGoogle Scholar
  • 55 Maisonpierre P, Suri C, Jones P, Bartunkova S, Wiegand S, Radziejewski C. et al . Angiopoietin-2, a natural antagonist for Tie2 that disrupts in vivo angiogenesis.  Science. 1997;  277 (5322) 55-60
    CrossrefPubMedGoogle Scholar
  • 56 McLaren J, Prentice A, Charnock-Jones D, Millican S, Muller K, Sharkey A. et al . Vascular endothelial growth factor is produced by peritoneal fluid macrophages in endometriosis and is regulated by ovarian steroids.  J Clin Invest. 1996;  98 482-489
    CrossrefPubMedGoogle Scholar
  • 57 McLaren J, Prentice A, Charnock-Jones D, Smith S. Vascular endothelial growth factor (VEGF) concentrations are elevated in peritoneal fluid of women with endometriosis.  Hum Reprod. 1996;  11 220-223
    PubMedGoogle Scholar
  • 58 Michishita M, Minegishi T, Abe K, Kangawa K, Kojima M, Ibuki Y. Expression of adrenomedullin in the endometrium of the human uterus.  Obstet Gynecol. 1999;  93 (1) 66-70
    CrossrefPubMedGoogle Scholar
  • 59 Miller T A, Bulman A L, Thompson C D, Garst M E, Macdonald T L. Synthesis and structure-activity profiles of A-homoestranes, the estratropones.  J Med Chem. 1997;  40 (23) 3836-3841
    CrossrefPubMedGoogle Scholar
  • 60 Milne S, Critchley H, Drudy T, Kelly R, Baird D. Perivascular interleukin-8 messenger ribonucleic acid expression in human endometrium varies across the menstrual cycle and in early pregnancy decidua.  J Clin Endocrinol Metab. 1999;  84 (7) 2563-2567
    CrossrefPubMedGoogle Scholar
  • 61 Moghaddam A, Zhang H T, Fan T P, Hu D E, Lees V C, Turley H. et al . Thymidine phosphorylase is angiogenic and promotes tumor growth.  Proc Natl Acad Sci USA. 1995;  92 (4) 998-1002
    PubMedGoogle Scholar
  • 62 Mori H, Sawairi M, Nakagawa M, Itoh N, Wada K, Tamaya T. Expression of interleukin-1 (IL-1) beta messenger rebonucleic acid (mRNA) and IL-1 receptor antagonist mRNA in peritoneal macrophages from patients with endometriosis.  Fertil Steril. 1992;  57 (3) 535-542
    PubMedGoogle Scholar
  • 63 Motro B, Itin A, Sachs L, Keshet E. Pattern of interleukin 6 gene expression in vivo suggests a role for this cytokine in angiogenesis.  Proc Natl Acad Sci USA. 1990;  87 (8) 3092-3096
    PubMedGoogle Scholar
  • 64 Mueller M, Lebovic D, Minchenko A, Vigne J, Leitman D, Taylor R. Vascular Endothelial Growth Factor (VEGF) gene transcription is regulated by estrogen receptor in human endometrial cells.  J Soc Gynecol Investig. 2000;  7 (Suppl 1) 48
    PubMedGoogle Scholar
  • 65 Mueller M D, Lebovic D I, Garrett E, Taylor R N. Neutrophils infiltrating the endometrium express Vascular Endothelial Growth Factor (VEGF): potential role in endometrial angiogenesis.  Fertil Steril. 2000;  74 (1) 107-112
    CrossrefPubMedGoogle Scholar
  • 66 Munson L, Upadhyaya N, Van Meter S. Platelet-derived growth factor promotes endometrial epithelial cell proliferation.  Am J Obstet Gynecol. 1995;  173 1820-1825
    CrossrefPubMedGoogle Scholar
  • 67 Nelson K, Takahashi T, Bossert N, Walmer D, McLachlan J. Epidermal growth factor replaces estrogen in the stimulation of female genital-tract growth and differentiation.  Proc Natl Acad Sci USA. 1991;  88 21-25
    PubMedGoogle Scholar
  • 68 Nicosia R, Nicosia S, Smith M. Vascular endothelial growth factor, platelet-derived growth factor, and insulin-like growth factor-1 promote rat aortic angiogenesis in vitro.  Am J Pathol. 1994;  145 1023-1029
    PubMedGoogle Scholar
  • 69 Nisolle M, Casanas Roux B, Anaf V, Mine J, Donnez J. Morphometric study of the stromal vascularization in peritoneal endometriosis.  Fertil Steril. 1993;  59 (3) 681-684
    PubMedGoogle Scholar
  • 70 Odukoya O A, Ajjan R, Lim K, Watson P F, Weetman A P, Cooke I D. The pattern of cytokine mRNA expression in ovarian endometriomata.  Mol Hum Reprod. 1997;  3 (5) 393-397
    CrossrefPubMedGoogle Scholar
  • 71 Olive D, Montoya I, Riehl R, Schenken R. Macrophage-conditioned media enhance endometrial stromal cell proliferation in vitro.  Am J Obstet Gynecol. 1991;  164 953-958
    PubMedGoogle Scholar
  • 72 Oosterlynck D, Meuleman C, Waer M, Koninckx P. Tansforming growth factor-beta activity is increased in peritoneal fluid from women with endometriosis.  Obstet Gynecol. 1994;  83 287-292
    PubMedGoogle Scholar
  • 73 O'Reilly M S, Homgren L, Shing Y, Chen C, Rosenthal R, Moses M. et al . Angiostatin: a novel angiogenesis inhibitor that mediates the suppression of metastases by a Lewis lung carcinoma.  Cell. 1994;  88 1-20
    PubMedGoogle Scholar
  • 74 Osteen K, Bruner K, Sharpe-Timms K. Steroid and growth factor regulation of matrix metalloproteinase expression and endometriosis.  Sem Reprod Endocrinol. 1996;  14 (3) 247-255
    PubMedGoogle Scholar
  • 75 Patterson C, Perrella M, Endege W, Yoshizumi M, Lee M, Haber E. Downregulation of vascular endothelial growth factor receptors by tumor necrosis factor-alpha in cultured human vascular endothelial cells.  J Clin Invest. 1996;  98 (2) 490-496
    PubMedGoogle Scholar
  • 76 Peters K, Coogan A, Berry D, Marks J, Iglehart J, Kontos C. et al . Expression of Tie2/Tek in breast tumour vasculature provides a new marker for evaluation of tumour angiogenesis.  Br J Cancer. 1998;  77 51-56
    PubMedGoogle Scholar
  • 77 Peters K G. Vascular endothelial growth factor and the angiopoietins: working together to build a better blood vessel.  Circ Res. 1998;  83 (3) 342-343
    PubMedGoogle Scholar
  • 78 Piva M, Sharpe-Timms K L. Peritoneal endometriotic lesions differentially express a haptoglobin-like gene.  Mol Hum Reprod. 1999;  5 (1) 71-78
    CrossrefPubMedGoogle Scholar
  • 79 Rana N, Braun D P, House R, Gebel H, Rotman C, Dmowski W P. Basal and stimulated secretion of cytokines by peritoneal macrophages in women with endometriosis.  Fertil Steril. 1996;  65 (5) 925-930
    PubMedGoogle Scholar
  • 80 Rier S, Parsons A, Becker J. Altered interleukin-6 production by peritoneal leukocytes from patients with endometriosis.  Fertil Steril. 1994;  61 (2) 294-299
    PubMedGoogle Scholar
  • 81 Rier S E, Martin D C, Bowman R E, Dmowski W P, Becker J L. Endometriosis in rhesus monkeys (Macaca mulatta) following chronic exposure to 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin.  Fund Appl Toxicol. 1993;  21 (4) 433-441
    CrossrefPubMedGoogle Scholar
  • 82 Rier S E, Zarmakoupis P N, Hu X, Becker J L. Dysregulation of interleukin-6 responses in ectopic endometrial stromal cells: correlation with decreased soluble receptor levels in peritoneal fluid of women with endometriosis.  J Clin Endocrinol Metab. 1995;  80 (4) 1431-1437
    CrossrefPubMedGoogle Scholar
  • 83 Rippy M K, Lee D R, Pearson S L, Bernal J C, Kuehl T J. Identification of rhesus macaques with spontaneous endometriosis.  J Med Primatol. 1996;  25 (5) 346-355
    PubMedGoogle Scholar
  • 84 Ryan I, Tseng J, Schriock E, Khorram O, Landers D, Taylor R. Interleukin-8 concentrations are elevated in peritoneal fluid of women with endometriosis.  Fertil Steril. 1995;  63 (4) 929-932
    PubMedGoogle Scholar
  • 85 Ryan I P, Schriock E D, Taylor R N. Isolation, characterization, and comparison of human endometrial and endometriosis cells in vitro.  J Clin Endocrinol Metab. 1994;  78 (3) 642-649
    CrossrefPubMedGoogle Scholar
  • 86 Sampson J. Peritoneal Endometriosis due to to the menstrual dissemination of endometrial tissue into the peritoneal cavity.  Am J Obstet Gynecol. 1927;  14 422-469
    CrossrefPubMedGoogle Scholar
  • 87 Sangha R, Li X, Shams M, Ahmed A. 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. 1997;  77 (4) 389-402
    PubMedGoogle Scholar
  • 88 Schriock E, Monroe S, Henzl M, Jaffe R. Treatment of endometriosis with a potent agonist of gonadotropin-releasing hormone (nafarelin).  Fertil Steril. 1985;  44 583-588
    PubMedGoogle Scholar
  • 89 Seli E, Zeyneloglu H B, Senturk L M, Bahtiyar O M, Olive D L, Arici A. Basic fibroblast growth factor: peritoneal and follicular fluid levels and its effect on early embryonic development.  Fertil Steril. 1998;  69 (6) 1145-1148
    CrossrefPubMedGoogle Scholar
  • 90 Sharpe K, Zimmer R, Griffin W, Penney L. Polypeptides synthesized and released by human endometriosis differ from those of the uterine endometrium in cell and tissue explant culture.  Fertil Steril. 1993;  60 (5) 839-851
    PubMedGoogle Scholar
  • 91 Sharpe K L, Vernon M W. Polypeptides synthesized and released by rat ectopic uterine implants differ from those of the uterus in culture.  Biol Reprod. 1993;  48 (6) 1334-1340
    PubMedGoogle Scholar
  • 92 Sharpe-Timms K L. Basic research in endometriosis.  Obstet Gynecol Clin North Am. 1997;  24 (2) 269-290
    CrossrefPubMedGoogle Scholar
  • 93 Shifren J, Tseng J, Zaloudek C, Ryan I, Meng Y, Ferrara N. et al . 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. 1996;  81 (8) 3112-3118
    CrossrefPubMedGoogle Scholar
  • 94 Shimazawa R, Miyachi H, Takayama H, Kuroda K, Kato F, Kato M. et al . Antiangiogenic activity of tumor necrosis factor-alpha production regulators derived from thalidomide.  Biol Pharmaceut Bulletin. 1993;  22 (2) 224-226
    PubMedGoogle Scholar
  • 95 Sillem M, Prifti S, Neher M, Runnebaum B. Extracellular matrix remodelling in the endometrium and its possible relevance to the pathogenesis of endometriosis.  Hum Reprod Update. 1998;  4 (5) 730-735
    CrossrefPubMedGoogle Scholar
  • 96 Surrey E, Halme J. Effect of platelet-derived growth factor on endometrial stromal cell proliferation in vitro: a model for endometriosis?.  Fertil Steril. 1991;  56 672-679
    PubMedGoogle Scholar
  • 97 Tabibzadeh S. Evidence of T cell activation and potential cytokine action in human endometrium.  J Clin Endocrinol Metab. 1990;  71 645-653
    PubMedGoogle Scholar
  • 98 Tabibzadeh S, Kong Q F, Babaknia A, May L T. Progressive rise in the expression of interleukin-6 in human endometrium during menstrual cycle is initiated during the implantation window.  Hum Reprod. 1995;  10 (10) 2793-2799
    PubMedGoogle Scholar
  • 99 Tabibzadeh S, Satyaswaroop P, Rao P. Antiproliferative effect of interferon-g in human endometrial epithelial cell in vitro: potential local growth modulatory role in endometrium.  J Clin Endocrinol Metab. 1988;  67 131-138
    PubMedGoogle Scholar
  • 100 Tao X J, Sayegh R A, Isaacson K B. Increased expression of complement component 3 in human ectopic endometrium compared with the matched eutopic endometrium.  Fertil Steril. 1997;  68 (3) 460-467
    CrossrefPubMedGoogle Scholar
  • 101 Taylor R, Ryan I, Moore E, Hornung D, Shifren J, Tseng J. Angiogenesis and macrophage activation in endometriosis.  Ann NY Acad Sci. 1997;  828 194-207
    PubMedGoogle Scholar
  • 102 Taylor R, Ryan I, Tseng J, Shifren J, Hornung D, Lebovic D. Ovarian Steroids and Angiogenesis. Understanding Endometriosis. Advances in Research and Practice. Carnforth; Parthenon 2000: in press
    Google Scholar
  • 103 Treloar S, O'Connor D, O'Connor V, Martin N. Genetic influences on endometriosis in an Australian twin sample.  Fertil Steril. 1999;  71 (4) 701-710
    CrossrefPubMedGoogle Scholar
  • 104 Tseng J, Ryan I, Milam T, Murai J, Schriock E, Landers D. et al . Interleukin-6 secretion in vitro is up-regulated in ectopic and eutopic endometrial stromal cells from women with endometriosis.  J Clin Endocrinol Metab. 1996;  81 (3) 1118-1122
    CrossrefPubMedGoogle Scholar
  • 105 Tsudo T, Harada T, Iwabe T, Tanikawa M, Nagano Y, Ito M. et al . Altered gene expression and secretion of interleukin-6 in stromal cells derived from endometriotic tissues.  Fertil Steril. 2000;  73 (2) 205-211
    CrossrefPubMedGoogle Scholar
  • 106 Tsuruoka N, Sugiyama M, Tawaragi Y, Tsujimoto M, Nishihara T, Goto T. et al . Inhibition of in vitro angiogenesis by lymphotoxin and interferon gamma.  Biochem Biophys Res Commun. 1988;  155 (1) 429-435
    CrossrefPubMedGoogle Scholar
  • 107 Van der Linden P, de Goeif A, Dunselman G, Erkens H W, Evers J. Endometrial cell adhesion in an in vitro model using intact amniotic membranes.  Fertil Steril. 1996;  65 76-80
    PubMedGoogle Scholar
  • 108 Vandermolen D T, Gu Y. 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. 1996;  66 (5) 741-747
    PubMedGoogle Scholar
  • 109 Witz C A, Monotoya-Rodriguez I A, Schenken R S. Whole explants of peritoneum and endometrium: a novel model of the early endometriosis lesion.  Fertil Steril. 1999;  71 (1) 56-60
    CrossrefPubMedGoogle Scholar
  • 110 Wu M H, Yang B C, Hsu C C, Lee Y C, Huang K E. The expression of soluble intercellular adhesion molecule-1 in endometriosis.  Fertil Steril. 1998;  70 (6) 1139-1142
    CrossrefPubMedGoogle Scholar
  • 111 Zetter B R. Angiogenesis and tumor metastasis.  Annu Rev Med. 1998;  49 407-424
    CrossrefPubMedGoogle Scholar
  • 112 Zhang L, Mackenzie I, Rees M, Bicknell R. Regulation of the expression of the angiogenic enzyme platelet-derived endothelial cell growth factor/thymidine phosphorylase in endometrial isolates by ovarian steroids and cytokines.  Endocrinology. 1997;  138 (11) 4921-4930
    CrossrefPubMedGoogle Scholar
  • 113 Zhou J, Dsupin B, Giudice L, Bondy C. Insulin-like growth factor system gene expression in human endometrium during the menstrual cycle.  J Clin Endocrinol Metab. 1994;  79 1723-1734
    CrossrefPubMedGoogle Scholar

Dr. med. M. D. Mueller

Oberarzt Frauenklinik des Inselspitals

Schanzeneckstrasse 1

3012 Bern

Schweiz

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