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Vascular development in endometriosis

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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.

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References

  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):585–96

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  3. Sampson JA. (1940). The development of the implantation theory for the origin of peitoneal endometriosis. Am J Obstet Gynecol 40:549–557

    Google Scholar 

  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):151–4

    PubMed  CAS  Google Scholar 

  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):560–4

    Article  PubMed  CAS  Google Scholar 

  6. Sanfilippo JS, Wakim NG, Schikler KN, Yussman MA. (1986). Endometriosis in association with uterine anomaly. Am J Obstet Gynecol 154(1):39–43

    PubMed  CAS  Google Scholar 

  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):635–8

    PubMed  CAS  Google Scholar 

  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):135–42

    PubMed  CAS  Google Scholar 

  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):264–8

    Article  PubMed  CAS  Google Scholar 

  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):681–4

    PubMed  CAS  Google Scholar 

  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):712–6

    Article  PubMed  CAS  Google Scholar 

  12. Conway EM, Collen D, Carmeliet P. (2001). Molecular mechanisms of blood vessel growth. Cardiovasc Res 49(3):507–21

    Article  PubMed  CAS  Google Scholar 

  13. Folkman J. (1971). Tumor angiogenesis: Therapeutic implications. N Engl J Med 285(21):1182–6

    PubMed  CAS  Google Scholar 

  14. Giordano FJ, Johnson RS. (2001). Angiogenesis: The role of the microenvironment in flipping the switch. Curr Opin Genet Dev 11(1):35–40

    Article  PubMed  CAS  Google Scholar 

  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):1119–24

    Article  PubMed  CAS  Google Scholar 

  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):30–4

    Article  PubMed  CAS  Google Scholar 

  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):1089–95

    Article  PubMed  CAS  Google Scholar 

  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):2889–99

    Article  PubMed  CAS  Google Scholar 

  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):909–18

    PubMed  CAS  Google Scholar 

  20. Haney AF. (1993). Endometriosis, macrophages, and adhesions. Prog Clin Biol Res 381:19–44

    PubMed  CAS  Google Scholar 

  21. Haney AF, Muscato JJ, Weinberg JB. (1981). Peritoneal fluid cell populations in infertility patients. Fertil Steril 35(6):696–8

    PubMed  CAS  Google Scholar 

  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):216–22

    PubMed  CAS  Google Scholar 

  23. Ho HN, Wu MY, Yang YS. (1997). Peritoneal cellular immunity and endometriosis. Am J Reprod Immunol 38(6):400–12

    PubMed  CAS  Google Scholar 

  24. Koninckx PR. (1994). Is mild endometriosis a condition occurring intermittently in all women?. Hum Reprod 9(12):2202–5

    PubMed  CAS  Google Scholar 

  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):402–9

    Article  PubMed  CAS  Google Scholar 

  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):271–8

    PubMed  CAS  Google Scholar 

  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):4140–5

    PubMed  CAS  Google Scholar 

  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):798–801

    PubMed  CAS  Google Scholar 

  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):360–8

    PubMed  CAS  Google Scholar 

  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):180–5

    Article  PubMed  CAS  Google Scholar 

  31. Dunselman GA, Bouckaert PX, Evers JL. (1988). The acute-phase response in endometriosis of women. J Reprod Fertil 83(2):803–8

    PubMed  CAS  Google Scholar 

  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):1039–46

    Article  PubMed  CAS  Google Scholar 

  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):309–14

    Article  PubMed  CAS  Google Scholar 

  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):2851–7

    PubMed  CAS  Google Scholar 

  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):1736–43

    Article  PubMed  CAS  Google Scholar 

  36. Papetti M, Herman IM. (2002). Mechanisms of normal and tumor-derived angiogenesis. Am J Physiol Cell Physiol 282(5):C947–70

    PubMed  CAS  Google Scholar 

  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):159–63

    Article  PubMed  CAS  Google Scholar 

  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):663–9

    Article  PubMed  CAS  Google Scholar 

  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):773–80

    PubMed  CAS  Google Scholar 

  40. Markee JE. (1940). Menstruation in intraocular endometrial transplants in the rhesus monkey. Contrib Emb 177:219–308

    Google Scholar 

  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. 65–79

    Google Scholar 

  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):265–74

    Article  PubMed  CAS  Google Scholar 

  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):2346–51

    Article  PubMed  CAS  Google Scholar 

  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):604–12

    Article  PubMed  CAS  Google Scholar 

  45. Finn CA. (1986). Implantation, menstruation and inflammation. Biol Rev Camb Philos Soc 61(4):313–28

    PubMed  CAS  Google Scholar 

  46. Salamonsen LA, Lathbury LJ. (2000). Endometrial leukocytes and menstruation. Hum Reprod Update 6(1):16–27

    Article  PubMed  CAS  Google Scholar 

  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, 396–406

    PubMed  Google Scholar 

  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):3442–52

    Article  PubMed  CAS  Google Scholar 

  49. Kunkel SL, Strieter RM, Lindley IJ, Westwick J. (1995). Chemokines: new ligands, receptors and activities. Immunol Today 16(12):559–61

    Article  PubMed  CAS  Google Scholar 

  50. Rogers PA, Abberton KM, Susil B. (1992). Endothelial cell migratory signal produced by human endometrium during the menstrual cycle. Hum Reprod 7(8):1061–6

    PubMed  CAS  Google Scholar 

  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):2356–66

    Article  PubMed  CAS  Google Scholar 

  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):652–61

    Article  PubMed  Google Scholar 

  53. Weston GC, Haviv I, Rogers PA. (2002). Microarray analysis of VEGF-responsive genes in myometrial endothelial cells. Mol Hum Reprod 8(9):855–63

    Article  PubMed  CAS  Google Scholar 

  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):1797–803

    Article  PubMed  CAS  Google Scholar 

  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):1557–61

    Article  PubMed  CAS  Google Scholar 

  56. Casslen B, Astedt B. (1983). Occurrence of both urokinase and tissue plasminogen activator in the human endometrium. Contraception 28(6):553–64

    Article  PubMed  CAS  Google Scholar 

  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):133–8

    PubMed  CAS  Google Scholar 

  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):1724–30

    Article  PubMed  CAS  Google Scholar 

  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):3359–67

    Article  PubMed  CAS  Google Scholar 

  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):768–71

    PubMed  CAS  Google Scholar 

  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):178–83

    PubMed  CAS  Google Scholar 

  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):759–67

    PubMed  CAS  Google Scholar 

  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):781–7

    Article  PubMed  CAS  Google Scholar 

  64. O’Reilly MS. (1997). Angiostatin: an endogenous inhibitor of angiogenesis and of tumor growth. Exs 79:273–94

    PubMed  CAS  Google Scholar 

  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):760–7

    Article  PubMed  CAS  Google Scholar 

  66. Mazar AP, Henkin J, Goldfarb RH. (1999). The urokinase plasminogen activator system in cancer: implications for tumor angiogenesis and metastasis. Angiogenesis 3(1):15–32

    Article  PubMed  CAS  Google Scholar 

  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):6986–90

    Article  PubMed  CAS  Google Scholar 

  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):923–8

    Article  PubMed  CAS  Google Scholar 

  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):67–71

    Article  PubMed  CAS  Google Scholar 

  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):1063–72

    Article  PubMed  CAS  Google Scholar 

  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):896–903

    PubMed  CAS  Google Scholar 

  72. Reddy KV, Mangale SS. (2003). Integrin receptors: the dynamic modulators of endometrial function. Tissue Cell 35(4):260–73

    Article  PubMed  CAS  Google Scholar 

  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):51–67

    PubMed  CAS  Google Scholar 

  74. Zeitoun KM, Bulun SE. (1999). Aromatase: a key molecule in the pathophysiology of endometriosis and a therapeutic target. Fertil Steril 72(6):961–9

    Article  PubMed  CAS  Google Scholar 

  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):2897–902

    Article  PubMed  CAS  Google Scholar 

  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):5212–6

    PubMed  CAS  Google Scholar 

  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):17–25

    PubMed  CAS  Google Scholar 

  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):755–63

    PubMed  CAS  Google Scholar 

  79. Jones RK, Bulmer JN, Searle RF. (1998). Phenotypic and functional studies of leukocytes in human endometrium and endometriosis. Hum Reprod Update 4(5):702–9

    Article  PubMed  CAS  Google Scholar 

  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):291–4

    PubMed  CAS  Google Scholar 

  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):341–4

    Article  PubMed  Google Scholar 

  82. Spuijbroek MD, Dunselman GA, Menheere PP, Evers JL. (1992). Early endometriosis invades the extracellular matrix. Fertil Steril 58(5):929–33

    PubMed  CAS  Google Scholar 

  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):197–9

    Article  PubMed  CAS  Google Scholar 

  84. Anaf V, Simon P, Fayt I, Noel J. (2000). Smooth muscles are frequent components of endometriotic lesions. Hum Reprod 15(4):767–71

    Article  PubMed  CAS  Google Scholar 

  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):371–5

    Article  PubMed  Google Scholar 

  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):57–62

    PubMed  CAS  Google Scholar 

  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):50–6

    Article  PubMed  Google Scholar 

  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):239–53

    Article  PubMed  CAS  Google Scholar 

  89. Williams CS, Tsujii M, Reese J, Dey SK, DuBois RN. (2000). Host cyclooxygenase-2 modulates carcinoma growth. J Clin Invest 105(11):1589–94

    PubMed  CAS  Google Scholar 

  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):399–407

    Article  PubMed  CAS  Google Scholar 

  91. Brigstock DR. (1999). The connective tissue growth factor/cysteine-rich 61/nephroblastoma overexpressed (CCN) family. Endocr Rev 20(2):189–206

    Article  PubMed  CAS  Google Scholar 

  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):645–9

    PubMed  CAS  Google Scholar 

  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):153–65

    Article  PubMed  CAS  Google Scholar 

  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):3090–6

    Article  PubMed  CAS  Google Scholar 

  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):24953–61

    Article  PubMed  CAS  Google Scholar 

  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):21943–50

    Article  PubMed  CAS  Google Scholar 

  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): 44177–87

    Google Scholar 

  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): 44166–76

    Google Scholar 

  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):13–24

    Article  PubMed  CAS  Google Scholar 

  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):964–73

    Article  PubMed  CAS  Google Scholar 

  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):21–6

    PubMed  CAS  Google Scholar 

  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):2373–85

    Article  PubMed  CAS  Google Scholar 

  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):380–6

    PubMed  CAS  Google Scholar 

  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):407–11

    Article  PubMed  CAS  Google Scholar 

  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):857–62

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Research Institute GROW, Department of Obstetrics and Gynaecology, University Hospital Maastricht, Maastricht, The Netherlands

    P.G. Groothuis & A.W. Nap

  2. Institute of Anatomy, University Hospital Duisburg-Essen, Essen, Germany

    E. Winterhager & R. Grümmer

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  1. P.G. Groothuis
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  2. A.W. Nap
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  3. E. Winterhager
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  4. R. Grümmer
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Correspondence to: Patrick G. Groothuis, Research Institute GROW, Department of Obstetrics and Gynecology, Academisch Ziekenhuis Maastricht, Peter Debyelaan 25, 6229 HX Maastricht, The Netherlands. Tel:␣+31-43-3876625; Fax: +31-43-3876613; E-mail: patrick.groothuis@ path.unimaas.nl

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Groothuis, P., Nap, A., Winterhager, E. et al. Vascular development in endometriosis. Angiogenesis 8, 147–156 (2005). https://doi.org/10.1007/s10456-005-9005-x

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