Immunopathogenesis of pelvic endometriosis: Role of hepatocyte growth factor, macrophages and ovarian steroids

American Journal of Reproductive Immunology

Volumn 60, Issue 5, 2008, Pages 383-404

  Khan, Khaleque Newaz ^a   Kitajima, Michio ^a   Hiraki, Koichi ^a   Fujishita, Akira ^b   Sekine, Ichiro ^a   Ishimaru, Tadayuki ^c   Masuzaki, Hideaki ^a  

^a NAGASAKI UNIVERSITY   (Japan)

^b Nagasaki Municipal Hospital   (Japan)

^c SASEBO CHUO HOSPITAL   (Japan)

Author keywords

Hepatocyte growth factor; Inflammation; Macrophages; Ovarian steroids; Pelvic endometriosis; Toll like receptor 4

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; BILIRUBIN; BILIVERDIN; CARBON MONOXIDE; CHEMOATTRACTANT; ESTRADIOL; ESTROGEN; ESTROGEN RECEPTOR; HEME; HEME OXYGENASE; INTEGRIN; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 1; INTERLEUKIN 10; INTERLEUKIN 6; IRON; MATRIX METALLOPROTEINASE; PROGESTERONE; PROGESTERONE RECEPTOR; SCATTER FACTOR; SCATTER FACTOR RECEPTOR; TESTOSTERONE 17BETA DEHYDROGENASE; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA; UVOMORULIN;

ANGIOGENESIS; CELL ADHESION; CELL COMPOSITION; CELL INTERACTION; CYTOKINE PRODUCTION; DISEASE ASSOCIATION; ENDOMETRIOSIS; ENDOMETRIUM CELL; ESCHERICHIA COLI; FEMALE; FEMALE INFERTILITY; HUMAN; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IMMUNOPATHOGENESIS; INNATE IMMUNITY; MACROPHAGE; MENSTRUATION; NONHUMAN; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PELVIS PAIN SYNDROME; PLEIOTROPY; PRIORITY JOURNAL; PROTEIN SYNTHESIS; REVIEW; VAGINA FLORA;

CADHERINS; ENDOMETRIOSIS; ESTROGENS; FEMALE; HEPATOCYTE GROWTH FACTOR; HUMANS; INTEGRINS; MACROPHAGES, PERITONEAL; OVARY; PELVIS; PROGESTERONE; PROTO-ONCOGENE PROTEINS C-MET; TOLL-LIKE RECEPTOR 4;

EID: 54049121098     PISSN: 10467408     EISSN: 16000897     Source Type: Journal    
DOI: 10.1111/j.1600-0897.2008.00643.x     Document Type: Review

References (133)

1. Strathy JH, Molgaard CA, Aoulman CB: Endometriosis and infertility: a laparoscopic study of endometriosis among fertile and infertile women. Fertil Steril 1982; 38: 667-672.
2. Sugawara J, Fukaya T, Murakami T, Yoshida H, Yajima A: Hepatocyte growth factor stimulates proliferation, migration, and lumen formation of human endometrial epithelial cells in vitro. Biol Reprod 1997; 57: 936-942.
3. Ishimaru T, Khan KN, Fujishita A, Kitajima M, Masuzaki H: Hepatocyte growth factor may be involved in cellular changes to the peritoneal mesothelium adjacent to pelvic endometriosis. Fertil Steril, 2004; 81 (Suppl. 1): 810-818.
4. Sampson J: Peritoneal endometriosis due to menstrual dissemination of endometrial tissue into the peritoneal cavity. Am J Obstet Gynecol 1927; 14: 422-429.
5. Thomas EJ, Prentice A: The etiology and pathogenesis of endometriosis. Reprod Med Rev 1992; 1: 21-36.
6. Fujishita A, Nakane PK, Koji T, Masuzaki H, Chavez RO, Yamabe T, Ishimaru T: Expression of estrogen and progesterone in endometrium and peritoneal endometriosis: An immunohistochemical and in situ hybridization study. Fertil Steril 1997; 67: 856-864.
7. Nisolle M, Casanas-Rouz F, Donnez J: Immunohistochemical analysis of proliferative activity and steroid receptor expression in peritoneal and ovarian endometriosis. Fertil Steril 1997; 68: 912-919.
8. Folkman J, Klagsbrun M: Angiogenic factors. Science 1987; 235: 442-446.
9. Halme J, Becker S, Haskill S: Altered maturation and function of peritoneal macrophages: Possible role in pathogenesis endometriosis. Am J Obstet Gynecol 1987; 156: 783-789.
10. Khan KN, Fujishita A, Kitajima M, Masuzaki H, Sekine I, Ishimaru T: Infiltrated macrophage activity in intact tissue of endometriosis. Proc Endometriosis 2002; 23: 137-142 (in Japanese).
11. Khan KN, Masuzaki H, Fujishita A, Kitajima M, Sekine I, Ishimaru T: Differential macrophage infiltration in early and advanced endometriosis and adjacent peritoneum. Fertil Steril 2004; 81: 652-661.
12. 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.
13. Halme J: Release of tumor necrosis factor-alpha by human peritoneal macrophages in vivo and in vitro. Am J Obstet Gynecol 1989; 161: 1718-1725.
14. Khan KN, Masuzaki H, Fujishita A, Hamasaki T, Kitajima M, Hasuo A, Ishimaru T: Association of interleukin-6 and estradiol with hepatocyte growth factor in peritoneal fluid of women with endometriosis. Acta Obstet Gynecol Scand 2002; 81: 764-771.
15. Kitajima M, Khan KN, Fujishita A, Masuzaki H, Ishimaru T: Histomorphometric alteration and cell-type specific modulation of arylhydrocarbon receptor and estrogen receptor expression by 2,3,7,8-tetrachlorodibemzo-p-dioxin and 17b-estradiol in mouse experimental model of endometriosis. Reprod Toxicol 2004; 18: 793-801.
16. Tabibzadeh SS, Santhanan V, Sehgal PB, May LT: Cytokine induced production of IFN-β2/IL-6 by freshly implanted human endometrial stromal cells: Modulation by estradiol 17β. J Immunol 1989; 42: 3134-3139.
17. Meyer R: Ueber den Stand der Frage der Adenomyositis und Adenomyom im Allgemeinen und insbesonderes ueber Adenomyositis seroepithelialis und Adeno-myometritis sarcomatosa. Zbl Gynaekol 1919; 36: 745-750.
18. Oosterlynck DJ, Cornillie FJ, Waer M, Vandeputte M, Koninckx PR: Women with endometriosis show a defect in natural killer activity resulting in a decreased cytotoxicity to autologous endometrium. Fertil Steril 1991; 56: 45-51.
19. Lebovic DI, Mueller MD, Taylor RN: Immunobiology of endometriosis. Fertil Steril 2001; 75: 1-10.
20. Giudice LC, Kao L: Endometriosis. Lancet 2004; 364: 1789-1799.
21. Witz CA, Montoya-RodrAguez AI, Schenken RS: Whole peritoneal explants: a novel model of the early endometriosis lesion. Fertil Steril 1999; 71: 56-60.
22. Debrock S, Vander P, Meuleman C, Moerman PH, Hill JA, D'Hooghe TM: In vitro adhesion of endometrium to autologous peritoneal membranes: Effect of the cycle phase and the stage of endometriosis. Hum Reprod 2002; 17: 2523-2528.
23. Groothuis PG, Koks CA, de Goeij AF, Dunselman GA, Arends JW, Evers JL: Adhesion of human endometrial fragments to peritoneum in vitro. Fertil Steril 1999; 71: 1119-1124.
24. Lessey BA, Damjanovich L, Coutifaris C: Integrin adhesion molecules in the human endometrium. Correlation with the normal and abnormal menstrual cycle. J Clin Invest 1992; 90: 188-195.
25. Lessey BA, Castel baum AJ, Sawin SW, Buck CA, Schinnar R, Bilker W, Strom BL: Aberrant integrin expression in the endometrium of women with endometriosis. J Clin Endocrinol Metab 1994; 79: 643-649.
26. Regidor PA, Vogel C, Regidor M, Schindler AE, Winterhager E: Expression pattern of integrin and adhesion molecules in endometriosis and human endometrium. Hum Reprod 1998; 4: 710-718.
27. Chung HW, Wen Y, Chun SH, Nezhat C, Woo BH, Polan ML: Matrix metalloproteinase-9 and tissue inhibitors of metalloproteinase-3 mRNA expression in ectopic and eutopic endometrium in women with endometriosis: A rationale for endometriotic invasiveness. Fertil Steril 2001; 75: 152-159.
28. Sillem M, Prifti S, Koch A, Neher M, Jauckus J, Runnebaum B: Regulation of matrix metalloproteinases and their inhibitors in uterine endometrial cells of patients with and without endometriosis. Eur J Obstet Gynecol Reprod Biol 2001; 95: 167-174.
29. Osteen KG, Keller NR, Feltus FA, Melner MH: Paracrine regulation of matrix metalloproteinase expression in the normal human endometrium. Gynecol Obstet Invest 1999; 48: 2-13.
30. van der Linden PJQ, van der Linden EPM, de Goeij AFPM, Ramaekers FC, Dunselman GAJ: Expression of integrins and E-cadherin in cells from menstrual effluent, endometrium, peritoneal fluid, peritoneum, and endometriosis. Fertil Steril 1994; 61: 85-90.
31. Witz CA, Takahashi A, Montoya-Rodriguez IA, Cho S, Schenken RS: Expression of the α2β1 and α3β1 integrins at the surface of mesothelial cells: A potential attachment site of endometrial cells. Fertil Steril 2000; 74: 579-584.
32. Sillem M, Prifti S, Monga B, Arslic T, Runnebaum B: Integrin-mediated adhesion of uterine endometrial cells from endometriosis patients to extracellular matrix proteins is enhanced by tumor necrosis factor alpha (TNF alpha) and interleukin-1 (IL-1). Eur J Obstet Gynecol Reprod Biol 1999; 87: 123-127.
33. 1 and laminin interaction. Mol Hum Reprod 2000; 6: 170-177.
34. Dechaud H, Witz CA, Montoya-Rodriguez IA, Degraffenreid LA, Schenken RS: Mesothelial cell-associated hyaluronic acid promotes adhesion of endometrial cells to mesothelium. Fertil Steril 2001; 76: 1012-1018.
35. Mulayim N, Savlu A, Guzeloglu-Kayisli O, Kayisli UA, Arici A: Regulation of endometrial stromal cell matrix metalloproteinase activity and invasiveness by interleukin-8. Fertil Steril 2004; 81: 904-911.
36. Gaetje R, Kotzian S, Herrmann G, Baumann R, Starzinski-Powitz A: Nonmalignant epithelial cells, potentially invasive in human endometriosis, lack the tumor suppressor molecule E-cadherin. Am J Pathol 1997; 150: 461-467.
37. Langendonckt AV, Casanas-Roux F, Dolmans M-M, Donnez J: Potential involvement of hemoglobin and heme in the pathogenesis of peritoneal endometriosis. Fertil Steril 2002; 77: 561-570.
38. Khan KN, Masuzaki H, Fujishita A, Kitajima M, Sekine I, Ishimaru T: Higher activity by opaque endometriotic lesions than non-opaque lesions in women with endometriosis. Acta Obstet Gynecol Scand 2004; 83: 375-382.
39. Miyazawa K, Tsubouchi H, Naka D, Takahashi K, Okigaki M, Arakaki N: Molecular cloning and sequence analysis of cDNA for human hepatocyte growth factor. Biochem Biophys Res Commun 1998; 163: 967-973.
40. Nakamura T, Nishizawa T, Hagiya M, Seki T, Shimonishi M, Sugimura A: Molecular cloning and expression of human hepatocyte growth factor. Nature 1989; 342: 440-443.
41. Wiedner KM, Arakaki N, Vandekereckhove J, Weingart S, Hartmann G, Rieder H: Evidence for the identity of human scatter factor and human hepatocyte growth factor. Proc Natl Acad Sci USA 1991; 88: 7001-7005.
42. Gherardi E, Gray J, Stocker M, Perryman M, Furlong R: Purification of scatter factor, a fibroblast-derived basic protein which modulates epithelial interactions and movement. Proc Natl Acad Sci USA 1989; 86: 5844-5848.
43. Nakamura T, Teramoto H, Ichihara A: Purification and characterization of a growth factor from rat platelets from mature parenchymal hepatocytes in primary culture. Proc Natl Acad Sci USA 1986; 83: 6489-6493.
44. Tajima H, Matsumoto K, Nakamura T: Regulation of cell growth and motility by hepatocyte growth factor and receptor expression in various cell species. Exp Cell Res 1992; 202: 423-431.
45. Bottaro DP, Rubin JS, Falleto DL, Chan AML, Kmeicik TE, Vande Woude GF: Identification of the hepatocyte growth factor receptor as the c-met proto-oncogene product. Science 1991; 251: 802-804.
46. Wagatsuma S, Konno R, Sato S, Yajima A: Tumor angiogenesis, hepatocyte growth factor, and c-Met expression in endometrial carcinoma. Cancer 1998; 82: 520-530.
47. Sonnenberg E, Meyer D, Weidner KM, Birchmeier C: Scatter factor/ hepatocyte growth factor and its receptor, c-met tyrosine kinase, can mediate a signal exchange between mesenchyme and epithelia during mouse development. J Cell Biol 1993; 123: 223-235.
48. Grant SD, Kleinman HK, Goldberg ID, Bhargava MM, Nickoloff BJ, Kinsella JL: Scatter factor induces blood vessel formation in vivo. Proc Natl Acad Sci USA 1993; 90: 1937-1941.
49. Rosen EM, Nigam SK, Goldberg ID: Scatter factor and the c-Met receptor: a paradigm for mesenchymal/epithelial interaction. J Cell Biol 1994; 127: 1783-1787.
50. Skrtic S, Wallenius V, Ekberg S, Brenzel A, Gressner AM, Jansson JO: Hepatocyte-stimulated expression of hepatocyte growth factor (HGF) in cultured rat hepatic stellate cells. J Hepatol, 1999; 30: 115-124.
51. Morimoto K, Amano H, Sonoda F, Baba M, Senba M, Yoshimine H, Yamamoto H, Ii T, Oishi K, Nagatake T: Alveolar macrophages that phagocytose apoptotic neutrophils produce hepatocyte growth factor during bacterial pneumonia in mice. Am J Respir Cell Mol Biol, 2001; 24: 608-615.
52. Crestani B, Dehoux M, Hayem G, Lecon V, Hochedez F, Marchal J, Jaffre S, Stern JB, Durand G, Valeyre D, Fournier M, Aubier M: Differential role of neutrophils and alveolar macrophages in hepatocyte growth factor production in pulmonary fibrosis. Lab Invest 2002; 82: 1015-1022.
53. Osuga Y, Tsutsumi O, Okagaki R, Takai Y, Fujimoto A, Suenaga A, Maruyama M, Momoeda M, Yano T, Taketani Y: Hepatocyte growth factor concentrations are elevated in peritoneal fluid of women with endometriosis. Hum Reprod 1999; 14: 1611-1613.
54. Mahnke JL, Dawood Y, Huang JH: Vascular endothelial growth factor and interleukin-6 in peritoneal fluid of women with endometriosis. Fertil Steril 2000; 73: 166-170.
55. Sugawara J, Fukaya T, Murakami T, Yoshida H, Yajima A: Increased secretion of hepatocyte growth factor by eutopic endometrial stromal cells in women with endometriosis. Fertil Steril 1997; 68: 468-472.
56. The American Society for Reproductive Medicine: Revised American Society for Reproductive Medicine classification of endometriosis: 1996. Fertil Steril 1997; 67: 817-821.
57. Khan KN, Masuzaki H, Fujishita A, Kitajima M, Hiraki K, Miura S, Sekine I, Ishimaru T: Peritoneal fluid and serum levels of hepatocyte growth factor may predict the activity of endometriosis. Acta Obstet Gynecol Scand 2006; 85: 458-466.
58. Kitamura M, Matsumiya K, Yamanaka M, Matsumoto K, Okuyama A: Effect of hepatocyte growth factor on sperm motility. Am J Reprod Immunol 2000; 44: 193-196.
59. Wiltshire EJ, Flaherty SP, Couper RT: Hepatocyte growth factor in human semen and its association with semen parameters. Hum Reprod 2000; 15: 1525-1528.
60. Khan KN, Masuzaki H, Fujishita A, Kitajima M, Sekine I, Ishimaru T: Immunoexpression of hepatocyte growth factor and c-Met receptor in eutopic endometrium predicts the activity of ectopic endometrium. Fertil Steril, 2003; 79: 173-181.
61. Yoshida S, Harada T, Mitsunari M, Iwabe T, Sakamoto Y, Tsukihara S, Iba Y, Horie S, Terakawa N: Hepatocyte growth factor/Met system promotes endometrial and endometriotic stromal cell invasion via autocrine and paracrine pathways. J Clin Endocrinol Metab 2004; 89: 823-832.
62. Yashiro M, Chung YS, Inoue T, Nishimura S, Matsuoka T, Fujihara T: Hepatocyte growth factor (HGF) produced by peritoneal fibroblasts may effect mesothelial cell morphology and promote peritoneal dissemination. Int J Cancer 1996; 67: 289-293.
63. Bae-Jump V, Segreti EM, Vandermolen D, Kauma S: Hepatocyte growth factor (HGF) induced invasion of endometrial carcinoma cell line in vitro. Gynecol Oncol 1999; 7: 265-272.
64. Kataoka H, Hamasuna R, Itoh H, Kitamura N, Koono M: Activation of hepatocyte growth factor/scatter factor in colorectal carcinoma. Cancer Res 2000; 60: 6148-6159.
65. Becker IL, Widen RH, Mahan CS, Yeko TR, Parsons AK, Spellacy WN: Human peritoneal macrophage and T lymphocyte populations in mild and severe endometriosis. Am J Reprod Immunol 1995; 34: 179-187.
66. Khan KN, Fujishita A, Kitajima M, Hasuo A, Miyamura Y, Masuzaki H, Ishimaru T: Immunoexpression of hepatocyte growth factor and c-met receptor in eutopic endometrium predicts the activity of ectopic endometrium. In Recent Research in Gynecological Endocrinology, AR Genazzani, PG Artini, F Petraglia (eds). New York, Parthenon, 2000, pp 111-114.
67. Khan KN, Fujishita A, Kitajima M, Masuzaki H, Sekine I, Ishimaru T: Infiltrated macrophage activity in intact tissue of endometriosis. Proc Endometriosis 2002; 23: 137-142 (in Japanese).
68. Ishimaru T, Fujishita A, Khan KN, Kitajima M, Masuzaki H, Matsuyama T: Morphological appearance and growth of pelvic endometriosis. Acta Obstet Gynaecol Jpn 2002; 54: 1158-1163 (in Japanese).
69. Donnez J, Nisolle M, Smoes P, Gillet N, Beguin S, Casanas-Roux F: Peritoneal endometriosis and 'endometriotic' nodule of rectovaginal septum are two different entities. Fertil Steril 1996; 66: 362-368.
70. Donnez J, Smoes P, Gillerot S, Casanas-Roux F, Nisolle M: Vascular endothelial growth factor in endometriosis. Hum Reprod 1998; 13: 1686-1690.
71. Khan KN, Masuzaki H, Fujishita A, Kitajima M, Sekine I, Matsuyama T, Ishimaru T: Estrogen and progesterone receptor expression in macrophages and regulation of hepatocyte growth factor by ovarian steroids in women with endometriosis. Hum Reprod 2005; 20: 2004-2013.
72. Khan KN, Fujishita A, Kitajima M, Masuzaki H, Matsuyama T, Sekine I, Ishimaru T: Detection of Escherichia coli in menstrual blood and its possible involvement in the growth of endometriosis. Endo2003, The 85th Annual Meeting of American Endocrine Society, 2003; Philadelphia, June 19-22, Vol. 383: 564.
73. Khan KN, Masuzaki H, Fujishita A, Kitajima M, Kohno T, Sekine I, Matsuyama T, Ishimaru T: Regulation of hepatocyte growth factor by basal and stimulated macrophages in women with endometriosis. Hum Reprod, 2005; 20: 49-60.
74. Akira S, Takeda K: Toll-like receptor signaling. Nat Rev Immunol 2004; 4: 499-511.
75. Check W: Innate immunity depends on Toll-like receptors. ASM News 2004; 70: 317-322.
76. Takeda K, Akira S: Toll-like receptors in innate immunity. Int Immunol 2005; 7: 1-14.
77. Wira CR, Fahey JV, Sentman CL, Pioli PA, Shen L: Innate and adaptive immunity in female genital tract: Cellular responses and interactions. Immunol Rev 2005; 206: 306-335.
78. Aflatoonian R, Tuckerman E, Elliot SL, Bruce C, Aflatoonian A, Li TC, Fazeli A: Menstrual cycle-dependent changes of toll-like receptors in endometrium. Hum Reprod 2007; 22: 586-593.
79. Fazeli A, Bruce C, Anumba DO: Characterization of Toll-like receptors in the female reproductive tract in humans. Hum Reprod 2005; 20: 1372-1378.
80. Khan KN, Fujishita A, Kitajima M, Hiraki K, Masuzaki H, Sekine I, Matsuyama T, Ishimaru T: Detection of Escherichia coli in menstrual blood and endotoxin in peritoneal fluid: An implication in pelvic inflammation and toll-like receptor 4 (TLR4)-mediated growth of endometriosis. Eur J Obstet Gynecol Reprod Biol 2005; 123: S15-S16.
81. Khan KN, Kitajima M, Imamura T, Hiraki K, Fujishita A, Matsuyama T, Sekine I, Ishimaru T, Masuzaki H: Toll-like receptor 4 (TLR4)-mediated growth of endometriosis by endogenous heat shock protein 70. Proceedings of the Endocrine Society's 88th Annual Meeting 2006; Boston, MA, June 24-27, 256-257.
82. Hirata T, Osuga Y, Hirota Y, Koga K, Yoshino O, Harada M, Morimoto C, Yano T, Nishii O, Tsutsumi O, Taketani Y: Evidence for the presence of Toll-like receptor 4 system in the human endometrium. J Clin Endocrinol Metab 2005; 90: 548-556.
83. Kiechl S, Lorenz E, Reindl M, Wiedermann CJ, Oberhollenzer F, Bonora E, Willeit J, Schwartz DA: Toll-like receptor 4 polymorphisms and atherogenesis. N Engl J Med 2002; 347: 185-192.
84. Kitawaki J, Kado N, Ishihara H, Koshiba H, Kitaoka Y, Honjo H: Endometriosis: The pathophysiology as an estrogen-dependent disease. J Steroid Biochem Mol Biol 2003; 83: 149-155.
85. Tamaya T, Motoyama T, Ohono Y, Ide N, Tsurusaki T, Okada H: Steroid receptor levels and histology of endometriosis and adenomyosis. Fertil Steril 1979; 31: 396-400.
86. Jane O, Kauppila A, Kokko E, Lantto T, Ronberg L, Vihko R: Estrogen and progesterone receptors in endometriosis lesions: Comparison with endometrial tissue. Am J Obstet Gynecol 1981; 141: 562-566.
87. Gould SF, Shannon JM, Cunha GR: Nuclear receptor binding sites in human endometriosis. Fertil Steril 1983; 39: 520-524.
88. McClellan MC, West NB, Tacha DF, Green GL, Brenner RM: Immunocytochemical localization of estrogen receptors in the macaque reproductive tract with monoclonal antiestrophilins. Endocrinology 1984; 114: 2002-2014.
89. Okulicz WC, Savasta AM, Hoberg LM, Longcope C: Biochemical and immunohistochemical analysis of estrogen and progesterone receptors in the rhesus monkey uterus during the proliferative and secretory phases of artificial menstrual cycles. Fertil Steril 1990; 53: 913-920.
90. Nisolle M, Menten Y, Casanas-Roux F, Mathieu PE, Wyns C, Donnez J: Immunohistochemical analysis of estrogen and progesterone receptors in endometrium and peritoneal endometriosis: A new quantitative method. Fertil Steril 1994; 62: 751-759.
91. Lessey BA, Metzgeer DA, Haney AF, McCarty KS: Immunohistochemical analysis of estrogen and progesterone receptors in endometriosis: comparison with normal endometrium during the menstrual cycle and the effect of medical therapy. Fertil Steril 1989; 51: 409-415.
92. Bergqvist A, Ljunberg O, Skoog L: Immunohistochemical analysis of estrogen and progesterone receptors in endometriotic tissue and endometrium. Hum Reprod 1993; 8: 1915-1922.
93. Prentice A, Randall BJ, Weddell A, McGill A, Herny L, Horne CHW: Ovarian steroid receptor expression in endometriosis and in two potential parent epithelia: Endometrium and peritoneal mesothelium. Hum Reprod 1992; 9: 1318-1325.
94. Howell RJ, Dowsett M, Edmonds DK: Oestrogen and progesterone receptors in endometriosis: Heterogeneity of different sites. Hum Reprod 1994; 9: 1752-1758.
95. Attar E, Bulun SE: Aromatase and other steroidogenic genes in endometriosis: Translational aspects. Hum Reprod Update 2006; 12: 49-56.
96. Bulun SE, Imir G, Utsunomiya H, Thung S, Gurates B, Tamura M, Lin Z: Aromatase in endometriosis and uterine leiomyomata. J Steroid Biochem Mol Biol 2005; 95: 57-62.
97. Lewis GS: Steroidal regulation of uterine immune defenses. Anim Reprod Sci 2004; 82-83: 281-294.
98. Beagley KW, Gockel CM: Regulation of innate and adaptive immunity by the female sex hormones estradiol and progesterone. FEMS Immunol Med Microbiol 2003; 38: 13-22.
99. Larsen S, Galask RPP Vaginal microbial flora: practical and theoretic relevance. Obstet Gynecol 1980; 55: 100S-113S.
100. Herath S, Fischer FD, Werling D, Williams EJ, Lilly ST, Dobson H, Bryant CE, Sheldon IM: Expression and Function of Toll-like receptor 4 in the endometrial cells of the uterus. Endocrinology 2006; 147: 562-570.
101. Mori T, Kobayashi H, Nishimoto H, Suzuki A, Nishimura T, Mori T: Inhibitory effect of progesterone and 20 alpha-hydroxypregn-4-en-3-one on the phytohemagglutinin-induced transformation of human lymphocytes. Am J Obstet Gynecol 1977; 127: 151-157.
102. Grossman CJ: Regulation of the immune system by sex steroids. Endocrinol Rev 1984; 5: 435-455.
103. Lahita RG: The role of sex hormones in systemic lupus erythematosus. Curr Opin Rheumatol 1999; 11: 352-356.
104. Tanriverdi F, Silveira IFG, MacColl GS, Bouloux PMG: The hypothalamic-pituitary-gonadal axis: Immune function and anutoimmunity. J Endocrinol 2003; 176: 293-304.
105. Giglio T, Imro MA, Filaci G, Scudeletti M, Puppo F, Cecco D, Indiveri F, Costantini S: Immune cell circulating subsets are affected by gonadal function. Life Sci 1994; 54: 1305-1312.
106. Yang JH, Chen CD, Wu MY, Chao KH, Yang YS, Ho HN: Hormone replacement therapy reverses the decrease in natural killer cytotoxicity but does not reverse the decreases in the T-cell subpopulation or interferon-gamma production in postmenopausal women. Fertil Steril 2000; 74: 261-266.
107. Kamada M, Irahara M, Maegawa M, Ohmoto Y, Takeji T, Yasui T, Aono T: Postmenopausal changes in serum cytokine levels and hormone replacement therapy. Am J Obstet Gynecol 2001; 184: 309-313.
108. Deguchi K, Kamada M, Irahara M, Maegawa M, Yamamoto S, Ohmoto Y, Murata K, Yasui T, Yamano S, Aono T: Postmenopausal changes in production of type 1 and type 2 cytokines and the effects of hormone replacement therapy. Menopause 2001; 8: 266-272.
109. Seaman WE, Blackman MA, Ginhart TD, Roubinian JR, Loeb JM, Talal N: β-estradiol reduces natural killer cells in mice. J Immunol 1978; 121: 2193-2198.
110. Hanna N: Role of natural killer cells in control of cancer metastasis. Cancer Metastasis Rev 1882; 1: 45-64.
111. Hanna N, Schneider M: Enhancement of tumor metastasis and suppression of natural killer cell activity by β-estradiol treatment. J Immunol 1883; 130: 974-980.
112. Shakhar K, Shakhar G, Rosenne E, Ben-Eliyahu S: Timing within the menstrual cycle, sex and the use of oral contraceptives determine adrenergic suppression of NK cell activity. Br J Cancer 2002; 83: 1630-1636.
113. Yovel G, Shakhar K, Ben-Eliyahu S: The effect of sex, menstrual cycle, and oral contraceptives in the number and activity of natural killer cells. Gynecol Oncol 2001; 81: 254-262.
114. Albrecht AE, Hartmann BW, Scholten CH, Huber JC, Kalinowska W, Zielinski CC: Effects of estrogen replacement therapy on natural killer cell activity in postmenopausal women. Maturitas 1996; 25: 217-222.
115. Stopinska-Gluszak U, Waligora J, Grzela T, Gluszak M, Jozwiak J, Radomski R, Roszkowski PI, Malejczyk J: Effect of estrogen/progesterone hormone replacement therapy on natural killer cell cytotoxicity and immunoregulatory cytokine release by peripheral blood mononuclear cells of postmenopausal women. J Reprod Immunol 2006; 69: 65-75.
116. Cutolo M, Villaggio B, Craviotto C, Pizzzorni C, Seriolo B, Sulli A: Sex hormones and rheumatoid arthritis. Autoimmun Rev 2002; 1: 284-289.
117. Cutolo M, Sulli A, Capellino S, Villaggio B, Montagna P, Seriolo B, Straub RH: Sex hormones influence on thB immune system: basic and clinic aspects in autoimmunity. Lupus 2004; 13: 635-638.
118. Canellada A, Blios S, Gentile T, Margni Idehu RA: In vitro modulation of protective antibody responses by estrogen, progesterone and interleukin-6. Am J Reprod Immunol 2002; 48: 334-343.
119. Whitacre CA, Reingold SC, O'Looney PA: A gender gap in autoimmunity. Science 1999; 283: 1277-1278.
120. Tariverdian N, Theoharides TC, Sindentopf F, Gutierrez G, Jeschke U, Rabinovich GA, Blois SM, Arck PC: Neuro-endocrine-immune disequilibrium and endometriosis: An interdisciplinary approach. Semin Immunopathol 2007; 29: 193-210.
121. Khan KN, Kitajima M, Imamura T, Hiraki K, Fujishita A, Sekine I, Ishimaru T, Masuzaki H: Toll-like receptor 4 (TLR4)-mediated growth of endometriosis by human heat shock protein 70 (Hsp70). Hum Reprod 2008; 23: 2210-2219.
122. Babson AL: The DPC Cirrus IMMULITE automated immunoassay system. J Clin Immunol 1991; 14: 817-821.
123. Jansen RPS, Russell P: Con-pigmented endometriosis: clinical, laparoscopic, and pathological definition. Am J Obstet Gynecol 1986; 155: 1154-1159.
124. Martin DC, Hubert GD, Vander-Zwaag R, EL-Zeky F: Laparoscopic appearances of peritoneal endometriosis. Fertil Steril 1989; 51: 63-67.
125. Ishimaru T, MasuzakiEH: Peritoneal endometriosis: endometrial tissue implantation as its primary etiologic mechanism. Am J Obstet Gynecol 1991; 165: 210-214.
126. Murphy AA, Green WR, Bobbie D, dela Cruz ZC, Rock JA: Unsuspected endometriosis documented by scanning electron microscopy. Fertil Steril 1986; 46: 522-524.
127. Nakamura M, Katabuchi H, Tohya T, Fukumatsu Y, Matsuura K, Okamura H: Scanning electron microscopic and immunohistochemical studies of pelvic endometriosis. Hum Reprod 1993; 8: 2218-2226.
128. McLaren J, Prentice A, Charnock-Jones DS, Millican SA, Muller KH, Sharkey AM, Smith SK: 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.
129. Bergqvist A: Steroid receptors in endometriosis. In Modern Approaches to Endometriosis, E Thomas, J Rock (eds). Dordrecht, The Netherlands, Kluwer, 1992, pp 257-274.
130. Eischen A, Duclos B, Schmitt-Gognel M, Rouyer N, Bergerat JP, Hummel M, Oskam R, Oberling F: Human residePt peritoneal macrophages: phenotype and histology. Br J Haematol 1994; 88: 712-722.
131. Khan KN, Masuzaki H, Fujishita A, Kitajima M, Hiraki K, Sekine I, Matsuyama T, Ishimaru T: Interleukin-6- and tumor necrosis factor α-mediated expression of hepatocyte growth factor by stromal cells and its involvement in the growth of endometriosis. Hum Reprod 2005; 20: 2715-2723.
132. Lauchlan SC: The secondary Mullerian system. Obstet Gynecol Surv 1992; 27: 133-146.
133. Witz CA, Schenken RS: Pathogenesis. Semin Reprod Endocrinol 1997; 15: 199-208.