Angiogenesis

, Volume 8, Issue 2, pp 147–156 | Cite as

Vascular development in endometriosis

  • P.G. Groothuis
  • A.W. Nap
  • E. Winterhager
  • R. Grümmer
Review

Abstract

Endometriosis, defined as the presence of endometrial tissue outside the uterus, is an estrogen-dependent disease which causes pelvic pain and subfertility in women of reproductive age. The condition has a dramatic impact on the professional, social and marital life of sufferers. Direct and indirect evidence suggests that angiogenesis is required for the development and persistence of endometriosis. In this review the state-of-the-art with regard to our understanding of the role of angiogenesis in the ectopic implantation and survival of menstrual endometrial tissue will be discussed.

Key words

angiogenesis chronic inflammation endometriosis endometrium invasion migration peritoneum vasculogenesis 

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References

  1. 1.
    Nisolle M, Donnez J. (1997). Peritoneal endometriosis, ovarian endometriosis, and adenomyotic nodules of the rectovaginal septum are three different entities. Fertil Steril 68(4):585–96CrossRefPubMedGoogle Scholar
  2. 2.
    Sampson JA. (1927). Peritoneal endometriosis due to menstrual dissemination of endometrial tissue into the peritoneal cavity. Am J Obstet Gynecol 14:422–469Google Scholar
  3. 3.
    Sampson JA. (1940). The development of the implantation theory for the origin of peitoneal endometriosis. Am J Obstet Gynecol 40:549–557Google Scholar
  4. 4.
    Halme J, Hammond MG, Hulka JF, Raj SG, Talbert LM. (1984). Retrograde menstruation in healthy women and in patients with endometriosis. Obstet Gynecol 64(2):151–4PubMedGoogle Scholar
  5. 5.
    Koks CA, Dunselman GA, de Goeij AF, Arends JW, Evers JL. (1997). Evaluation of a menstrual cup to collect shed endometrium for in vitro studies. Fertil Steril 68(3):560–4CrossRefPubMedGoogle Scholar
  6. 6.
    Sanfilippo JS, Wakim NG, Schikler KN, Yussman MA. (1986). Endometriosis in association with uterine anomaly. Am J Obstet Gynecol 154(1):39–43PubMedGoogle Scholar
  7. 7.
    D’Hooghe TM, Bambra CS, Suleman MA, Dunselman GA, Evers HL, Koninckx PR. (1994). Development of a model of retrograde menstruation in baboons (Papio anubis). Fertil Steril 62(3):635–8PubMedGoogle Scholar
  8. 8.
    Darrow SL, Vena JE, Batt RE, Zielezny MA, Michalek AM, Selman S. (1993). Menstrual cycle characteristics and the risk of endometriosis. Epidemiology 4(2):135–42PubMedGoogle Scholar
  9. 9.
    Vercellini P, De Giorgi O, Aimi G, Panazza S, Uglietti A, Crosignani PG. (1997). Menstrual characteristics in women with and without endometriosis. Obstet Gynecol 90(2):264–8CrossRefPubMedGoogle Scholar
  10. 10.
    Nisolle M, Casanas-Roux F, Anaf V, Mine JM, Donnez J. (1993). Morphometric study of the stromal vascularization in peritoneal endometriosis. Fertil Steril 59(3):681–4PubMedGoogle Scholar
  11. 11.
    Matsuzaki S, Canis M, Murakami T, Dechelotte P, Bruhat MA, Okamura K. (2001). Immunohistochemical analysis of the role of angiogenic status in the vasculature of peritoneal endometriosis. Fertil Steril 76(4):712–6CrossRefPubMedGoogle Scholar
  12. 12.
    Conway EM, Collen D, Carmeliet P. (2001). Molecular mechanisms of blood vessel growth. Cardiovasc Res 49(3):507–21CrossRefPubMedGoogle Scholar
  13. 13.
    Folkman J. (1971). Tumor angiogenesis: Therapeutic implications. N Engl J Med 285(21):1182–6PubMedGoogle Scholar
  14. 14.
    Giordano FJ, Johnson RS. (2001). Angiogenesis: The role of the microenvironment in flipping the switch. Curr Opin Genet Dev 11(1):35–40CrossRefPubMedGoogle Scholar
  15. 15.
    Groothuis PG, Koks CA, de Goeij AF, Dunselman GA, Arends JW, Evers JL. (1999). Adhesion of human endometrial fragments to peritoneum in vitro. Fertil Steril 71(6):1119–24CrossRefPubMedGoogle Scholar
  16. 16.
    Nap AW, Groothuis PG, Demir AY, Maas JW, Dunselman GA, de Goeij AF, et al. (2003). Tissue integrity is essential for ectopic implantation of human endometrium in the chicken chorioallantoic membrane. Hum Reprod 18(1):30–4CrossRefPubMedGoogle Scholar
  17. 17.
    Nap AW, Griffioen AW, Dunselman GA, Bouma-Ter Steege JC, Thijssen VL, Evers JL, et al. (2004). Antiangiogenesis therapy for endometriosis. J Clin Endocrinol Metab 89(3):1089–95CrossRefPubMedGoogle Scholar
  18. 18.
    Hull ML, Charnock-Jones DS, Chan CL, Bruner-Tran KL, Osteen KG, Tom BD, et al. (2003). Antiangiogenic agents are effective inhibitors of endometriosis. J Clin Endocrinol Metab 88(6):2889–99CrossRefPubMedGoogle Scholar
  19. 19.
    Dabrosin C, Gyorffy S, Margetts P, Ross C, Gauldie J. (2002). Therapeutic effect of angiostatin gene transfer in a murine model of endometriosis. Am J Pathol 161(3):909–18PubMedGoogle Scholar
  20. 20.
    Haney AF. (1993). Endometriosis, macrophages, and adhesions. Prog Clin Biol Res 381:19–44PubMedGoogle Scholar
  21. 21.
    Haney AF, Muscato JJ, Weinberg JB. (1981). Peritoneal fluid cell populations in infertility patients. Fertil Steril 35(6):696–8PubMedGoogle Scholar
  22. 22.
    Hill JA, Faris HM, Schiff I, Anderson DJ. (1988). Characterization of leukocyte subpopulations in the peritoneal fluid of women with endometriosis. Fertil Steril 50(2):216–22PubMedGoogle Scholar
  23. 23.
    Ho HN, Wu MY, Yang YS. (1997). Peritoneal cellular immunity and endometriosis. Am J Reprod Immunol 38(6):400–12PubMedGoogle Scholar
  24. 24.
    Koninckx PR. (1994). Is mild endometriosis a condition occurring intermittently in all women?. Hum Reprod 9(12):2202–5PubMedGoogle Scholar
  25. 25.
    Sharkey AM, Day K, McPherson A, Malik S, Licence D, Smith SK, et al. (2000). Vascular endothelial growth factor expression in human endometrium is regulated by hypoxia. J Clin Endocrinol Metab 85(1):402–9CrossRefPubMedGoogle Scholar
  26. 26.
    Harmey JH, Dimitriadis E, Kay E, Redmond HP, Bouchier-Hayes D. (1998). Regulation of macrophage production of vascular endothelial growth factor (VEGF) by hypoxia and transforming growth factor beta-1. Ann Surg Oncol 5(3):271–8PubMedGoogle Scholar
  27. 27.
    Freeman MR, Schneck FX, Gagnon ML, Corless C, Soker S, Niknejad K, et al. (1995). Peripheral blood T lymphocytes and lymphocytes infiltrating human cancers express vascular endothelial growth factor: a potential role for T cells in angiogenesis. Cancer Res 55(18):4140–5PubMedGoogle Scholar
  28. 28.
    Selgas R, del Peso G, Bajo MA, Castro MA, Molina S, Cirugeda A, et al. (2000). Spontaneous VEGF production by cultured peritoneal mesothelial cells from patients on peritoneal dialysis. Perit Dial Int 20(6):798–801PubMedGoogle Scholar
  29. 29.
    Nagy JA, Masse EM, Herzberg KT, Meyers MS, Yeo KT, Yeo TK, et al. (1995). Pathogenesis of ascites tumor growth: vascular permeability factor, vascular hyperpermeability, and ascites fluid accumulation. Cancer Res 55(2):360–8PubMedGoogle Scholar
  30. 30.
    Maas JW, Calhaz-Jorge C, ter Riet G, Dunselman GA, de Goeij AF, Struijker-Boudier HA. (2001). Tumor necrosis factor-alpha but not interleukin-1 beta or interleukin-8 concentrations correlate with angiogenic activity of peritoneal fluid from patients with minimal to mild endometriosis. Fertil Steril 75(1):180–5CrossRefPubMedGoogle Scholar
  31. 31.
    Dunselman GA, Bouckaert PX, Evers JL. (1988). The acute-phase response in endometriosis of women. J Reprod Fertil 83(2):803–8PubMedGoogle Scholar
  32. 32.
    Volpert OV, Fong T, Koch AE, Peterson JD, Waltenbaugh C, Tepper RI, et al. (1998). Inhibition of angiogenesis by interleukin 4. J Exp Med 188(6):1039–46CrossRefPubMedGoogle Scholar
  33. 33.
    Ogawa H, Nishihira J, Sato Y, Kondo M, Takahashi N, Oshima T, et al. (2000). An antibody for macrophage migration inhibitory factor suppresses tumour growth and inhibits tumour-associated angiogenesis. Cytokine 12(4):309–14CrossRefPubMedGoogle Scholar
  34. 34.
    Bruner KL, Matrisian LM, Rodgers WH, Gorstein F, Osteen KG. (1997). Suppression of matrix metalloproteinases inhibits establishment of ectopic lesions by human endometrium in nude mice. J Clin Invest 99(12):2851–7PubMedGoogle Scholar
  35. 35.
    Grummer R, Schwarzer F, Bainczyk K, Hess-Stumpp H, Regidor PA, Schindler AE, et al. (2001). Peritoneal endometriosis: validation of an in-vivo model. Hum Reprod 16(8):1736–43CrossRefPubMedGoogle Scholar
  36. 36.
    Papetti M, Herman IM. (2002). Mechanisms of normal and tumor-derived angiogenesis. Am J Physiol Cell Physiol 282(5):C947–70PubMedGoogle Scholar
  37. 37.
    Krikun G, Schatz F, Finlay T, Kadner S, Mesia A, Gerrets R, et al. (2000). Expression of angiopoietin-2 by human endometrial endothelial cells: regulation by hypoxia and inflammation. Biochem Biophys Res Commun 275(1):159–63CrossRefPubMedGoogle Scholar
  38. 38.
    Hirchenhain J, Huse I, Hess A, Bielfeld P, De Bruyne F, Krussel JS. (2003). Differential expression of angiopoietins 1 and 2 and their receptor Tie-2 in human endometrium. Mol Hum Reprod 9(11):663–9CrossRefPubMedGoogle Scholar
  39. 39.
    Hewett P, Nijjar S, Shams M, Morgan S, Gupta J, Ahmed A. (2002). Down-regulation of angiopoietin-1 expression in menorrhagia. Am J Pathol 160(3):773–80PubMedGoogle Scholar
  40. 40.
    Markee JE. (1940). Menstruation in intraocular endometrial transplants in the rhesus monkey. Contrib Emb 177:219–308Google Scholar
  41. 41.
    Fraser IS, Peek M.J. (1992). Effects of exogenous hormones on endometrial capillaries. In: Alexander NJ, d’Arcangues C., (eds) Steroid Hormones and Uterine Bleeding. Washington, AAAS Publications, pp. 65–79Google Scholar
  42. 42.
    Zhang J, Salamonsen LA. (2002). Expression of hypoxia-inducible factors in human endometrium and suppression of matrix metalloproteinases under hypoxic conditions do not support a major role for hypoxia in regulating tissue breakdown at menstruation. Hum Reprod 17(2):265–74CrossRefPubMedGoogle Scholar
  43. 43.
    Zhang J, Salamonsen LA. (2002). In vivo evidence for active matrix metalloproteinases in human endometrium supports their role in tissue breakdown at menstruation. J Clin Endocrinol Metab 87(5):2346–51CrossRefPubMedGoogle Scholar
  44. 44.
    Koks CA, Groothuis PG, Slaats P, Dunselman GA, de Goeij AF, Evers JL. (2000). Matrix metalloproteinases and their tissue inhibitors in antegradely shed menstruum and peritoneal fluid. Fertil Steril 73(3):604–12CrossRefPubMedGoogle Scholar
  45. 45.
    Finn CA. (1986). Implantation, menstruation and inflammation. Biol Rev Camb Philos Soc 61(4):313–28PubMedGoogle Scholar
  46. 46.
    Salamonsen LA, Lathbury LJ. (2000). Endometrial leukocytes and menstruation. Hum Reprod Update 6(1):16–27CrossRefPubMedGoogle Scholar
  47. 47.
    Brenner RM, Nayak NR, Slayden OD, et al. (2002). Premenstrual and menstrual changes in the macaque and human endometrium: relevance to endometriosis. Ann N Y Acad Sci 955:60–74; discussion 86–8, 396–406PubMedGoogle Scholar
  48. 48.
    Nayak NR, Critchley HO, Slayden OD, Menrad A, Chwalisz K, Baird DT, et al. (2000). Progesterone withdrawal up-regulates vascular endothelial growth factor receptor type 2 in the superficial zone stroma of the human and macaque endometrium: potential relevance to menstruation. J Clin Endocrinol Metab 85(9):3442–52CrossRefPubMedGoogle Scholar
  49. 49.
    Kunkel SL, Strieter RM, Lindley IJ, Westwick J. (1995). Chemokines: new ligands, receptors and activities. Immunol Today 16(12):559–61CrossRefPubMedGoogle Scholar
  50. 50.
    Rogers PA, Abberton KM, Susil B. (1992). Endothelial cell migratory signal produced by human endometrium during the menstrual cycle. Hum Reprod 7(8):1061–6PubMedGoogle Scholar
  51. 51.
    Print C, Valtola R, Evans A, Lessan K, Malik S, Smith S. (2004). Soluble factors from human endometrium promote angiogenesis and regulate the endothelial cell transcriptome. Hum Reprod 19(10):2356–66CrossRefPubMedGoogle Scholar
  52. 52.
    Khan KN, Masuzaki H, Fujishita A, Kitajima M, Sekine I, Ishimaru T. (2004). Differential macrophage infiltration in early and advanced endometriosis and adjacent peritoneum. Fertil Steril 81(3):652–61CrossRefPubMedGoogle Scholar
  53. 53.
    Weston GC, Haviv I, Rogers PA. (2002). Microarray analysis of VEGF-responsive genes in myometrial endothelial cells. Mol Hum Reprod 8(9):855–63CrossRefPubMedGoogle Scholar
  54. 54.
    Yang S, Toy K, Ingle G, Zlot C, Williams PM, Fuh G, et al. (2002). Vascular endothelial growth factor-induced genes in human umbilical vein endothelial cells: relative roles of KDR and Flt-1 receptors. Arterioscler Thromb Vasc Biol 22(11):1797–803CrossRefPubMedGoogle Scholar
  55. 55.
    Maas JW, Groothuis PG, Dunselman GA, de Goeij AF, Struyker Boudier HA, Evers JL. (2001). Endometrial angiogenesis throughout the human menstrual cycle. Hum Reprod 16(8):1557–61CrossRefPubMedGoogle Scholar
  56. 56.
    Casslen B, Astedt B. (1983). Occurrence of both urokinase and tissue plasminogen activator in the human endometrium. Contraception 28(6):553–64CrossRefPubMedGoogle Scholar
  57. 57.
    Casslen B, Urano S, Lecander I, Ny T. (1992). Plasminogen activators in the human endometrium, cellular origin and hormonal regulation. Blood Coagul Fibrinolysis 3(2):133–8PubMedGoogle Scholar
  58. 58.
    Sandberg T, Ehinger A, Casslen B. (2001). Paracrine stimulation of capillary endothelial cell migration by endometrial tissue involves epidermal growth factor and is mediated via up-regulation of the urokinase plasminogen activator receptor. J Clin Endocrinol Metab 86(4):1724–30CrossRefPubMedGoogle Scholar
  59. 59.
    Koolwijk P, Kapiteijn K, Molenaar B, van Spronsen E, van der Vecht B, Helmerhorst FM, et al. (2001). Enhanced angiogenic capacity and urokinase-type plasminogen activator expression by endothelial cells isolated from human endometrium. J Clin Endocrinol Metab 86(7):3359–67CrossRefPubMedGoogle Scholar
  60. 60.
    Gleeson N, Devitt M, Sheppard BL, Bonnar J. (1993). Endometrial fibrinolytic enzymes in women with normal menstruation and dysfunctional uterine bleeding. Br J Obstet Gynaecol 100(8):768–71PubMedGoogle Scholar
  61. 61.
    Gleeson NC. (1994). Cyclic changes in endometrial tissue plasminogen activator and plasminogen activator inhibitor type 1 in women with normal menstruation and essential menorrhagia. Am J Obstet Gynecol 171(1):178–83PubMedGoogle Scholar
  62. 62.
    Sandberg T, Casslen B, Gustavsson B, Benraad TJ. (1998). Human endothelial cell migration is stimulated by urokinase plasminogen activator:plasminogen activator inhibitor 1 complex released from endometrial stromal cells stimulated with transforming growth factor beta1; possible mechanism for paracrine stimulation of endometrial angiogenesis. Biol Reprod 59(4):759–67PubMedGoogle Scholar
  63. 63.
    Sandberg T, Eriksson P, Gustavsson B, Casslen B. (1997). Differential regulation of the plasminogen activator inhibitor-1 (PAI-1) gene expression by growth factors and progesterone in human endometrial stromal cells. Mol Hum Reprod 3(9):781–7CrossRefPubMedGoogle Scholar
  64. 64.
    O’Reilly MS. (1997). Angiostatin: an endogenous inhibitor of angiogenesis and of tumor growth. Exs 79:273–94PubMedGoogle Scholar
  65. 65.
    Westphal JR, Van’t Hullenaar R, Geurts-Moespot A, Sweep FC, Verheijen JH, Bussemakers MM, et al. (2000). Angiostatin generation by human tumor cell lines: involvement of plasminogen activators. Int J Cancer 86(6):760–7CrossRefPubMedGoogle Scholar
  66. 66.
    Mazar AP, Henkin J, Goldfarb RH. (1999). The urokinase plasminogen activator system in cancer: implications for tumor angiogenesis and metastasis. Angiogenesis 3(1):15–32CrossRefPubMedGoogle Scholar
  67. 67.
    Bajou K, Maillard C, Jost M, Lijnen RH, Gils A, Declerck P, et al. (2004). Host-derived plasminogen activator inhibitor-1 (PAI-1) concentration is critical for in vivo tumoral angiogenesis and growth. Oncogene 23(41):6986–90CrossRefPubMedGoogle Scholar
  68. 68.
    Bajou K, Noel A, Gerard RD, Masson V, Brunner N, Holst-Hansen C, et al. (1998). Absence of host plasminogen activator inhibitor 1 prevents cancer invasion and vascularization. Nat Med 4(8):923–8CrossRefPubMedGoogle Scholar
  69. 69.
    Whawell SA, Wang Y, Fleming KA, Thompson EM, Thompson JN. (1993). Localization of plasminogen activator inhibitor-1 production in inflamed appendix by in situ mRNA hybridization. J Pathol 169(1):67–71CrossRefPubMedGoogle Scholar
  70. 70.
    Anderson CR, Ponce AM, Price RJ. (2004). Immunohistochemical identification of an extracellular matrix scaffold that microguides capillary sprouting in vivo. J Histochem Cytochem 52(8):1063–72CrossRefPubMedGoogle Scholar
  71. 71.
    Demarchez M, Hartmann DJ, Prunieras M. (1987). An immunohistological study of the revascularization process in human skin transplanted onto the nude mouse. Transplantation 43(6):896–903PubMedGoogle Scholar
  72. 72.
    Reddy KV, Mangale SS. (2003). Integrin receptors: the dynamic modulators of endometrial function. Tissue Cell 35(4):260–73CrossRefPubMedGoogle Scholar
  73. 73.
    Ruegg C, Dormond O, Mariotti A. (2004). Endothelial cell integrins and COX-2: mediators and therapeutic targets of tumor angiogenesis. Biochim Biophys Acta 1654(1):51–67PubMedGoogle Scholar
  74. 74.
    Zeitoun KM, Bulun SE. (1999). Aromatase: a key molecule in the pathophysiology of endometriosis and a therapeutic target. Fertil Steril 72(6):961–9CrossRefPubMedGoogle Scholar
  75. 75.
    Attia GR, Zeitoun K, Edwards D, Johns A, Carr BR, Bulun SE. (2000). Progesterone receptor isoform A but not B is expressed in endometriosis. J Clin Endocrinol Metab 85(8):2897–902CrossRefPubMedGoogle Scholar
  76. 76.
    Weiner CP, Lizasoain I, Baylis SA, Knowles RG, Charles IG, Moncada S. (1994). Induction of calcium-dependent nitric oxide synthases by sex hormones. Proc Natl Acad Sci USA 91(11):5212–6PubMedGoogle Scholar
  77. 77.
    Cid MC, Kleinman HK, Grant DS, Schnaper HW, Fauci AS, Hoffman GS. (1994). Estradiol enhances leukocyte binding to tumor necrosis factor (TNF)-stimulated endothelial cells via an increase in TNF-induced adhesion molecules E-selectin, intercellular adhesion molecule type 1, and vascular cell adhesion molecule type 1. J Clin Invest 93(1):17–25PubMedGoogle Scholar
  78. 78.
    Morales DE, McGowan KA, Grant DS, Maheshwari S, Bhartiya D, Cid MC, et al. (1995). Estrogen promotes angiogenic activity in human umbilical vein endothelial cells in vitro and in a murine model. Circulation 91(3):755–63PubMedGoogle Scholar
  79. 79.
    Jones RK, Bulmer JN, Searle RF. (1998). Phenotypic and functional studies of leukocytes in human endometrium and endometriosis. Hum Reprod Update 4(5):702–9CrossRefPubMedGoogle Scholar
  80. 80.
    Matsuzaki S, Canis M, Darcha C, Fukaya T, Yajima A, Bruhat MA. (1998). Increased mast cell density in peritoneal endometriosis compared with eutopic endometrium with endometriosis. Am J Reprod Immunol 40(4):291–4PubMedGoogle Scholar
  81. 81.
    Fujiwara H, Konno R, Netsu S, Sugamata M, Shibahara H, Ohwada M, et al. (2004). Localization of mast cells in endometrial cysts. Am J Reprod Immunol 51(5):341–4CrossRefPubMedGoogle Scholar
  82. 82.
    Spuijbroek MD, Dunselman GA, Menheere PP, Evers JL. (1992). Early endometriosis invades the extracellular matrix. Fertil Steril 58(5):929–33PubMedGoogle Scholar
  83. 83.
    Matsuzaki S, Canis M, Darcha C, Dechelotte P, Pouly JL, Bruhat MA. (1999). Fibrogenesis in peritoneal endometriosis. A semi-quantitative analysis of type-I collagen. Gynecol Obstet Invest 47(3):197–9CrossRefPubMedGoogle Scholar
  84. 84.
    Anaf V, Simon P, Fayt I, Noel J. (2000). Smooth muscles are frequent components of endometriotic lesions. Hum Reprod 15(4):767–71CrossRefPubMedGoogle Scholar
  85. 85.
    Itoga T, Matsumoto T, Takeuchi H, Yamasaki S, Sasahara N, Hoshi T, et al. (2003). Fibrosis and smooth muscle metaplasia in rectovaginal endometriosis. Pathol Int 53(6):371–5CrossRefPubMedGoogle Scholar
  86. 86.
    Van Voorhis BJ, Huettner PC, Clark MR, Hill JA. (1990). Immunohistochemical localization of prostaglandin H synthase in the female reproductive tract and endometriosis. Am J Obstet Gynecol 163(1 Pt 1):57–62PubMedGoogle Scholar
  87. 87.
    Chishima F, Hayakawa S, Sugita K, Kinukawa N, Aleemuzzaman S, Nemoto N, et al. (2002). Increased expression of cyclooxygenase-2 in local lesions of endometriosis patients. Am J Reprod Immunol 48(1):50–6CrossRefPubMedGoogle Scholar
  88. 88.
    Zeitoun K, Takayama K, Michael MD, Bulun SE. (1999). Stimulation of aromatase P450 promoter (II) activity in endometriosis and its inhibition in endometrium are regulated by competitive binding of steroidogenic factor-1 and chicken ovalbumin upstream promoter transcription factor to the same cis-acting element. Mol Endocrinol 13(2):239–53CrossRefPubMedGoogle Scholar
  89. 89.
    Williams CS, Tsujii M, Reese J, Dey SK, DuBois RN. (2000). Host cyclooxygenase-2 modulates carcinoma growth. J Clin Invest 105(11):1589–94PubMedGoogle Scholar
  90. 90.
    Absenger Y, Hess-Stumpp H, Kreft B, Kratzschmar J, Haendler B, Schutze N, et al. (2004). Cyr61, a deregulated gene in endometriosis. Mol Hum Reprod 10(6):399–407CrossRefPubMedGoogle Scholar
  91. 91.
    Brigstock DR. (1999). The connective tissue growth factor/cysteine-rich 61/nephroblastoma overexpressed (CCN) family. Endocr Rev 20(2):189–206CrossRefPubMedGoogle Scholar
  92. 92.
    Perbal B. (2001). The CCN family of cell growth regulators: a new family of normal and pathologic cell growth and differentiation regulators: lessons from the first international workshop on CCN gene family. Bull Cancer 88(7):645–9PubMedGoogle Scholar
  93. 93.
    Brigstock DR. (2002). Regulation of angiogenesis and endothelial cell function by connective tissue growth factor (CTGF) and cysteine-rich 61 (CYR61). Angiogenesis 5(3):153–65CrossRefPubMedGoogle Scholar
  94. 94.
    Kireeva ML, Lam SC, Lau LF. (1998). Adhesion of human umbilical vein endothelial cells to the immediate-early gene product Cyr61 is mediated through integrin alphavbeta3. J Biol Chem 273(5):3090–6CrossRefPubMedGoogle Scholar
  95. 95.
    Chen N, Chen CC, Lau LF. (2000). Adhesion of human skin fibroblasts to Cyr61 is mediated through integrin alpha 6beta 1 and cell surface heparan sulfate proteoglycans. J Biol Chem 275(32):24953–61CrossRefPubMedGoogle Scholar
  96. 96.
    Grzeszkiewicz TM, Kirschling DJ, Chen N, Lau LF. (2001). CYR61 stimulates human skin fibroblast migration through Integrin alpha vbeta 5 and enhances mitogenesis through integrin alpha vbeta 3, independent of its carboxyl-terminal domain. J Biol Chem 276(24):21943–50CrossRefPubMedGoogle Scholar
  97. 97.
    Leu SJ, Chen N, Chen CC et al. Targeted mutagenesis of the angiogenic protein CCN1 (CYR61): Selective inactivation of integrin alpha 6beta 1-heparan sulfate proteoglycan coreceptor-mediated cellular functions. J Biol Chem 2004; 279(42): 44177–87Google Scholar
  98. 98.
    Chen N, Leu SJ, Todorovic V et al. Identification of a novel integrin alpha vbeta 3 binding site in CCN1 (CYR61) critical for pro-angiogenic activities in vascular endothelial cells. J Biol Chem 2004; 279(42): 44166–76Google Scholar
  99. 99.
    Rivera-Gonzalez R, Petersen DN, Tkalcevic G, Thompson DD, Brown TA. (1998). Estrogen-induced genes in the uterus of ovariectomized rats and their regulation by droloxifene and tamoxifen. J Steroid Biochem Mol Biol 64(1–2):13–24CrossRefPubMedGoogle Scholar
  100. 100.
    Tsai MS, Bogart DF, Li P, Mehmi I, Lupu R. (2002). Expression and regulation of Cyr61 in human breast cancer cell lines. Oncogene 21(6):964–73CrossRefPubMedGoogle Scholar
  101. 101.
    Lindahl P, Betsholtz C. (1998). Not all myofibroblasts are alike: revisiting the role of PDGF-A and PDGF-B using PDGF-targeted mice. Curr Opin Nephrol Hypertens 7(1):21–6PubMedGoogle Scholar
  102. 102.
    Chegini N, Rossi MJ, Masterson BJ. (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. Endocrinology 130(4):2373–85CrossRefPubMedGoogle Scholar
  103. 103.
    Overton C, Fernandez-Shaw S, Hicks B, Barlow D, Starkey P. (1996). Peritoneal fluid cytokines and the relationship with endometriosis and pain. Hum Reprod 11(2):380–6PubMedGoogle Scholar
  104. 104.
    Lindahl P, Hellstrom M, Kalen M, Betsholtz C. (1998). Endothelial-perivascular cell signaling in vascular development: lessons from knockout mice. Curr Opin Lipidol 9(5):407–11CrossRefPubMedGoogle Scholar
  105. 105.
    Gescher DM, Berndorff U, Meyhoefer-Malik A, Moubayed P, Malik E. (2004). Immunolocalization of angiopoietin 1 in human peritoneal endometriotic lesions. Fertil Steril 81(Suppl 1):857–62CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2005

Authors and Affiliations

  • P.G. Groothuis
    • 1
  • A.W. Nap
    • 1
  • E. Winterhager
    • 2
  • R. Grümmer
    • 2
  1. 1.Research Institute GROW, Department of Obstetrics and GynaecologyUniversity Hospital MaastrichtMaastrichtThe Netherlands
  2. 2.Institute of AnatomyUniversity Hospital Duisburg-EssenEssenGermany

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