Immune interactions in endometriosis

Expert Review of Clinical Immunology

Volumn 7, Issue 5, 2011, Pages 611-626

  Herington, Jennifer L ^a   Bruner Tran, Kaylon L ^a   Lucas, John A ^a   Osteen, Kevin G ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

chemokines; cytokines; dioxin; endocrine disrupting chemicals; endometriosis; estrogen; immune endocrine interactions; inflammation; peritoneum; progesterone; TCDD

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; CD36 ANTIGEN; CYCLOOXYGENASE 2; ESTROGEN; FAS LIGAND; GAMMA INTERFERON; GELATINASE B; GONADORELIN DERIVATIVE; INTERLEUKIN 1; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; LYMPHOTOXIN; MONOCYTE CHEMOTACTIC PROTEIN 1; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PLATELET DERIVED GROWTH FACTOR; PROGESTERONE; RANTES; RECOMBINANT INTERLEUKIN 8; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN;

ANGIOGENESIS; ANTIGEN EXPRESSION; APOPTOSIS; ARTICLE; CELL COMMUNICATION; CELL DIFFERENTIATION; CELL FUNCTION; CELL PROLIFERATION; CYTOKINE PRODUCTION; CYTOKINE RELEASE; ENDOMETRIOSIS; ENDOMETRIUM CELL; HUMAN; IMMUNOPATHOGENESIS; IMMUNOSURVEILLANCE; INNATE IMMUNITY; LEUKOCYTE ACTIVATION; LYMPHOCYTOTOXICITY; MENSTRUAL CYCLE; MONOCYTE; NATURAL KILLER CELL; PERITONEAL CAVITY; PERITONEUM MACROPHAGE; PHENOTYPE; PROGESTERONE RELEASE; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; STEROID METABOLISM; TH17 CELL;

ANIMALS; ENDOMETRIOSIS; ENVIRONMENTAL EXPOSURE; FEMALE; HUMANS; IMMUNOLOGIC SURVEILLANCE; PROGESTERONE; TERATOGENS; TETRACHLORODIBENZODIOXIN;

EID: 80052644366     PISSN: 1744666X     EISSN: 17448409     Source Type: Journal    
DOI: 10.1586/eci.11.53     Document Type: Article

References (173)

1. Bulun SE. Endometriosis. N. Engl. J. Med. 360(3), 268-279 (2009).
2. Benagiano G, Brosens I. The history of endometriosis: identifying the disease. Hum. Reprod. 6(7), 963-968 (1991).
3. Diesterweg A. Ein Fall von Cystofibroma uteri verum. Z. Geburtshilfe 9, 191-195 (1883).
4. Sampson JA. Metastatic or embolic endometriosis, due to the menstrual dissemination of endometrial tissue into the venous circulation. Am. J. Pathol. 3(2), 93-110 143 (1927).
5. El-Mahgoub S, Yaseen S. A positive proof for the theory of coelomic metaplasia. Am. J. Obstet. Gynecol. 137(1), 137-140 (1980). (Pubitemid 10068299)
6. Meyer R. Ueber eine adenomatose Wucherung der Serosa in einer Banchuabe. Zeit. Gerburt. Gynak. 49, 32-38 (1903).
7. Meyer R. Ueber den stand der Frage der Adenomyositis und Adenomyome in algemeinen und insbesondere iiber Adenomyositis serosoeithelialis und Adenomyometritis sarcomatosa. Zentralbl. Gyndkol. 43, 745-750 (1919).
8. Nakamura M, Katabuchi H, Tohya T, Fukumatsu Y, Matsuura K, Okamura H. Scanning electron microscopic and immunohistochemical studies of pelvic endometriosis. Hum. Reprod. 8(12), 2218-2226 (1993). (Pubitemid 24012827)
9. Batt RE, Smith RA. Embryologic theory of histogenesis of endometriosis in peritoneal pockets. Obstet. Gynecol. Clin. North Am. 16(1), 15-28 (1989). (Pubitemid 19054701)
10. Batt RE, Smith RA, Buck GM, Severino MF, Naples JD. Mullerianosis. Prog. Clin. Biol. Res. 323, 413-426 (1990).
11. Halban J. Hysteroadenosis metastatica. Zentralbl. Gynakol. 7, 387-391 (1925).
12. Sasson IE, Taylor HS. Stem cells and the pathogenesis of endometriosis. Ann. NY Acad. Sci. 1127, 106-115 (2008). (Pubitemid 351565719)
13. Fujii S. Secondary mullerian system and endometriosis. Am. J. Obstet. Gynecol. 165(1), 219-225 (1991).
14. Sinaii N, Cleary SD, Ballweg ML, Nieman LK, Stratton P. High rates of autoimmune and endocrine disorders, fibromyalgia, chronic fatigue syndrome and atopic diseases among women with endometriosis: a survey analysis. Hum. Reprod. 17(10), 2715-2724 (2002). (Pubitemid 35174127)
15. Shepperson Mills D, Vernon M. Endometriosis: A Key to Healing Through Nutrition. Element Books Limited, Boston, MA, USA (1999).
16. Revised American Fertility Society classification of endometriosis: 1985. Fertil. Steril. 43(3), 351-352 (1985).
17. Gupta S, Goldberg JM, Aziz N, Goldberg E, Krajcir N, Agarwal A. Pathogenic mechanisms in endometriosis-associated infertility. Fertil. Steril. 90(2), 247-257 (2008). (Pubitemid 352040722)
18. Tomassetti C, Meuleman C, Pexsters A et al. Endometriosis, recurrent miscarriage and implantation failure: is there an immunological link? Reprod. Biomed. Online 13(1), 58-64 (2006). (Pubitemid 44054846)
19. Weiss G, Goldsmith LT, Taylor RN, Bellet D, Taylor HS. Inflammation in reproductive disorders. Reprod. Sci. 16(2), 216-229 (2009).
20. Agic A, Xu H, Finas D, Banz C, Diedrich K, Hornung D. Is endometriosis associated with systemic subclinical inflammation? Gynecol. Obstet. Invest. 62(3), 139-147 (2006). (Pubitemid 44474973)
21. Viatour P, Merville MP, Bours V, Chariot A. Phosphorylation of NF-kB and IkB proteins: implications in cancer and inflammation. Trends Biochem. Sci. 30(1), 43-52 (2005). (Pubitemid 40093740)
22. Cao WG, Morin M, Sengers V et al. Tumour necrosis factor-α up-regulates macrophage migration inhibitory factor expression in endometrial stromal cells via the nuclear transcription factor NF-kB. Hum. Reprod. 21(2), 421-428 (2006). (Pubitemid 43159917)
23. Sugino N, Karube-Harada A, Sakata A, Takiguchi S, Kato H. Nuclear factor-k B is required for tumor necrosis factor-α-induced manganese superoxide dismutase expression in human endometrial stromal cells. J. Clin. Endocrinol. Metab. 87(8), 3845-3850 (2002). (Pubitemid 34879537)
24. Gonzalez-Ramos R, Donnez J, Defrere S et al. Nuclear factor-k B is constitutively activated in peritoneal endometriosis. Mol. Hum. Reprod. 13(7), 503-509 (2007). (Pubitemid 47062889)
25. Okino ST, Whitlock JP Jr. The aromatic hydrocarbon receptor, transcription, and endocrine aspects of dioxin action. Vitam. Horm. 59, 241-264 (2000).
26. Kerkvliet NI. AHR-mediated immunomodulation: the role of altered gene transcription. Biochem. Pharmacol. 77(4), 746-760 (2009).
27. Rier SE, Martin DC, Bowman RE, Dmowski WP, Becker JL. Endometriosis in rhesus monkeys (Macaca mulatta) following chronic exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Fundam. Appl. Toxicol. 21(4), 433-441 (1993). (Pubitemid 23338558)
28. Birnbaum LS. Endocrine effects of prenatal exposure to PCBs, dioxins, and other xenobiotics: implications for policy and future research. Environ. Health Perspect. 102(8), 676-679 (1994). (Pubitemid 24276618)
29. Fierens S, Mairesse H, Heilier JF et al. Dioxin/polychlorinated biphenyl body burden, diabetes and endometriosis: findings in a population-based study in Belgium. Biomarkers 8(6), 529-534 (2003). (Pubitemid 38418283)
30. Heilier JF, Nackers F, Verougstraete V, Tonglet R, Lison D, Donnez J. Increased dioxin-like compounds in the serum of women with peritoneal endometriosis and deep endometriotic (adenomyotic) nodules. Fertil. Steril. 84(2), 305-312 (2005). (Pubitemid 41125249)
31. Pauwels A, Schepens PJ, D'Hooghe T et al. The risk of endometriosis and exposure to dioxins and polychlorinated biphenyls: a case-control study of infertile women. Hum. Reprod. 16(10), 2050-2055 (2001). (Pubitemid 32951893)
32. Porpora MG, Ingelido AM, Di Domenico A et al. Increased levels of polychlorobiphenyls in Italian women with endometriosis. Chemosphere 63(8), 1361-1367 (2006).
33. Koninckx PR. The physiopathology of endometriosis: pollution and dioxin. Gynecol. Obstet. Invest. 47(Suppl. 1), 47-49; discussion 50 (1999).
34. Bruner-Tran KL, Ding T, Osteen KG. Dioxin and endometrial progesterone resistance. Semin. Reprod. Med.28(1), 59-68 (2010).
35. Bruner-Tran KL, Osteen KG. Dioxin-like PCBs and endometriosis. Syst. Biol. Reprod. Med. 56(2), 132-146 (2010).
36. Heindel JJ. Role of exposure to environmental chemicals in the developmental basis of reproductive disease and dysfunction. Semin. Reprod. Med. 24(3), 168-177 (2006).
37. Nayyar T, Bruner-Tran KL, Piestrzeniewicz-Ulanska D, Osteen KG. Developmental exposure of mice to TCDD elicits a similar uterine phenotype in adult animals as observed in women with endometriosis. Reprod. Toxicol. 23(3), 326-336 (2007). (Pubitemid 46602923)
38. Dmowski WP, Ding J, Shen J, Rana N, Fernandez BB, Braun DP. Apoptosis in endometrial glandular and stromal cells in women with and without endometriosis. Hum. Reprod. 16(9), 1802-1808 (2001). (Pubitemid 32916203)
39. Christodoulakos G, Augoulea A, Lambrinoudaki I, Sioulas V, Creatsas G. Pathogenesis of endometriosis: the role of defective 'immunosurveillance'. Eur. J. Contracept. Reprod. Health Care 12(3), 194-202 (2007). (Pubitemid 47347172)
40. Paul Dmowski W, Braun DP. Immunology of endometriosis. Best Pract. Res. Clin. Obstet. Gynaecol. 18(2), 245-263 (2004). (Pubitemid 38786631)
41. Kaminski K, Kotarski J, Gogacz M. Characterization of cellular components in the peritoneal fluid and in the endometrial tissue of women with endometriosis. Arch. Immunol. Ther. Exp. (Warsz) 43(5-6), 247-252 (1995).
42. Oosterlynck DJ, Meuleman C, Waer M, Vandeputte M, Koninckx PR. The natural killer activity of peritoneal fluid lymphocytes is decreased in women with endometriosis. Fertil. Steril. 58(2), 290-295 (1992).
43. Braun DP, Gebel H, House R, Rana N, Dmowski NP. Spontaneous and induced synthesis of cytokines by peripheral blood monocytes in patients with endometriosis. Fertil. Steril. 65(6), 1125-1129 (1996). (Pubitemid 26158627)
44. Rana N, Braun DP, House R, Gebel H, Rotman C, Dmowski WP. Basal and stimulated secretion of cytokines by peritoneal macrophages in women with endometriosis. Fertil. Steril. 65(5), 925-930 (1996). (Pubitemid 26126822)
45. Zeller JM, Henig I, Radwanska E, Dmowski WP. Enhancement of human monocyte and peritoneal macrophage chemiluminescence activities in women with endometriosis. Am. J. Reprod. Immunol. Microbiol. 13(3), 78-82 (1987). (Pubitemid 17075991)
46. Cassatella MA. The production of cytokines by polymorphonuclear neutrophils. Immunol. Today. 16(1), 21-26 (1995).
47. Mantovani A, Allavena P, Sica A, Balkwill F. Cancer-related inflammation. Nature 454(7203), 436-444 (2008).
48. Lebovic DI, Mueller MD, Taylor RN. Immunobiology of endometriosis. Fertil. Steril. 75(1), 1-10 (2001). (Pubitemid 32041217)
49. Osteen KG, Yeaman GR, Bruner-Tran KL. Matrix metalloproteinases and endometriosis. Semin. Reprod. Med. 21(2), 155-164 (2003).
50. Febbraio M, Hajjar DP, Silverstein RL. CD36: a class B scavenger receptor involved in angiogenesis, atherosclerosis, inflammation, and lipid metabolism. J. Clin. Invest. 108(6), 785-791 (2001). (Pubitemid 32880285)
51. Linton MF, Fazio S. Class A scavenger receptors, macrophages, and atherosclerosis. Curr. Opin. Lipidol. 12(5), 489-495 (2001). (Pubitemid 32980296)
52. Critchley HO, Kelly RW, Brenner RM, Baird DT. The endocrinology of menstruation - a role for the immune system. Clin. Endocrinol. (Oxf) 55(6), 701-710 (2001). (Pubitemid 34008738)
53. Wu MH, Shoji Y, Wu MC et al. Suppression of matrix metalloproteinase-9 by prostaglandin E(2) in peritoneal macrophage is associated with severity of endometriosis. Am. J. Pathol. 167(4), 1061-1069 (2005). (Pubitemid 41416258)
54. De Villiers WJ, Fraser IP, Gordon S. Cytokine and growth factor regulation of macrophage scavenger receptor expression and function. Immunol. Lett. 43(1-2), 73-79 (1994).
55. Chuang PC, Wu MH, Shoji Y, Tsai SJ. Downregulation of CD36 results in reduced phagocytic ability of peritoneal macrophages of women with endometriosis. J. Pathol. 219(2), 232-241 (2009).
56. Dmowski WP, Braun D, Gebel H. Endometriosis: genetic and immunologic aspects. Prog. Clin. Biol. Res. 323, 99-122 (1990).
57. Halme J, Becker S, Wing R. Accentuated cyclic activation of peritoneal macrophages in patients with endometriosis. Am. J. Obstet. Gynecol. 148(1), 85-90 (1984). (Pubitemid 14218551)
58. Han J, Hajjar DP, Tauras JM, Feng J, Gotto AM Jr, Nicholson AC. Transforming growth factor-β1 (TGF-β1) and TGF-β2 decrease expression of CD36, the type B scavenger receptor, through mitogen-activated protein kinase phosphorylation of peroxisome proliferator-activated receptor-G. J. Biol. Chem. 275(2), 1241-1246 (2000). (Pubitemid 30051177)
59. Huang JT, Welch JS, Ricote M et al. Interleukin-4-dependent production of PPAR-γ ligands in macrophages by 12/15-lipoxygenase. Nature 400(6742), 378-382 (1999). (Pubitemid 29344205)
60. Herington JL, Crispens MA, Carvalho- Macedo AC et al. Development and prevention of postsurgical adhesions in a chimeric mouse model of experimental endometriosis. Fertil. Steril. 95(4), 1295-1301 e1 (2011).
61. Lebovic DI, Kir M, Casey CL. Peroxisome proliferator-activated receptor-γ induces regression of endometrial explants in a rat model of endometriosis. Fertil. Steril. 82(Suppl. 3), 1008-1013 (2004). (Pubitemid 39341177)
62. Lebovic DI, Mwenda JM, Chai DC, Santi A, Xu X, D'hooghe T. Peroxisome proliferator-activated receptor-(g) receptor ligand partially prevents the development of endometrial explants in baboons: a prospective, randomized, placebo-controlled study. Endocrinology 151(4), 1846-1852 (2010).
63. Chuang PC, Lin YJ, Wu MH, Wing LY, Shoji Y, Tsai SJ. Inhibition of CD36- dependent phagocytosis by prostaglandin E2 contributes to the development of endometriosis. Am. J. Pathol. 176(2), 850-860 (2010).
64. Somigliana E, Vigano P, Gaffuri B, Guarneri D, Busacca M, Vignali M. Human endometrial stromal cells as a source of soluble intercellular adhesion molecule (ICAM)-1 molecules. Hum. Reprod. 11(6), 1190-1194 (1996). (Pubitemid 26245312)
65. Vigano P, Gaffuri B, Somigliana E, Busacca M, Di Blasio AM, Vignali M. Expression of intercellular adhesion molecule (ICAM)-1 mRNA and protein is enhanced in endometriosis versus endometrial stromal cells in culture. Mol. Hum. Reprod. 4(12), 1150-1156 (1998). (Pubitemid 28552799)
66. Dmowski WP, Gebel HM, Braun DP. The role of cell-mediated immunity in pathogenesis of endometriosis. Acta. Obstet. Gynecol. Scand. Suppl. 159, 7-14 (1994). (Pubitemid 24174510)
67. Hill JA, Faris HM, Schiff I, Anderson DJ. Characterization of leukocyte subpopulations in the peritoneal fluid of women with endometriosis. Fertil. Steril. 50(2), 216-222 (1988).
68. Raiter-Tenenbaum A, Baranao RI, Etchepareborda JJ, Meresman GF, Rumi LS. Functional and phenotypic alterations in peritoneal macrophages from patients with early and advanced endometriosis. Arch. Gynecol. Obstet. 261(3), 147-157 (1998). (Pubitemid 28301651)
69. Hsu CC, Lin YS, Wang ST, Huang KE. Immunomodulation in women with endometriosis receiving GnRH agonist. Obstet. Gynecol. 89(6), 993-998 (1997).
70. 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. 56(1), 45-51 (1991).
71. Wilson TJ, Hertzog PJ, Angus D, Munnery L, Wood EC, Kola I. Decreased natural killer cell activity in endometriosis patients: relationship to disease pathogenesis. Fertil. Steril. 62(5), 1086-1088 (1994). (Pubitemid 24328246)
72. Wu MY, Yang JH, Chao KH, Hwang JL, Yang YS, Ho HN. Increase in the expression of killer cell inhibitory receptors on peritoneal natural killer cells in women with endometriosis. Fertil. Steril. 74(6), 1187-1191 (2000).
73. Ota H, Igarashi S. Expression of major histocompatibility complex class II antigen in endometriotic tissue in patients with endometriosis and adenomyosis. Fertil. Steril. 60(5), 834-838 (1993). (Pubitemid 23324772)
74. Semino C, Semino A, Pietra G et al. Role of major histocompatibility complex class I expression and natural killer-like T cells in the genetic control of endometriosis. Fertil. Steril. 64(5), 909-916 (1995).
75. Harada T, Kaponis A, Iwabe T et al. Apoptosis in human endometrium and endometriosis. Hum. Reprod. Update 10(1), 29-38 (2004). (Pubitemid 38263161)
76. Tariverdian N, Siedentopf F, Rucke M et al. Intraperitoneal immune cell status in infertile women with and without endometriosis. J. Reprod. Immunol. 80(1-2), 80-90 (2009).
77. Cassatella MA. Neutrophil-derived proteins: selling cytokines by the pound. Adv. Immunol. 73, 369-509 (1999). (Pubitemid 29300434)
78. Riley CF, Moen MH, Videm V. Inflammatory markers in endometriosis: reduced peritoneal neutrophil response in minimal endometriosis. Acta. Obstet. Gynecol. Scand. 86(7), 877-881 (2007). (Pubitemid 47035818)
79. Mueller MD, Mazzucchelli L, Buri C, Lebovic DI, Dreher E, Taylor RN. Epithelial neutrophil-activating peptide 78 concentrations are elevated in the peritoneal fluid of women with endometriosis. Fertil. Steril. 79(Suppl. 1), 815-820 (2003). (Pubitemid 36279689)
80. Hirata T, Osuga Y, Hamasaki K et al. Interleukin (IL)-17A stimulates IL-8 secretion, cyclooxygensase-2 expression, and cell proliferation of endometriotic stromal cells. Endocrinology 149(3), 1260-1267 (2008). (Pubitemid 351397970)
81. Hirata T, Osuga Y, Takamura M et al. Recruitment of CCR6-expressing Th17 cells by CCL 20 secreted from IL-1 β-, TNF-α-, and IL-17A-stimulated endometriotic stromal cells. Endocrinology 151(11), 5468-5476 (2010).
82. Steele RW, Dmowski WP, Marmer DJ. Immunologic aspects of human endometriosis. Am. J. Reprod. Immunol. 6(1), 33-36 (1984). (Pubitemid 14063047)
83. Osuga Y, Koga K, Hirota Y, Hirata T, Yoshino O, Taketani Y. Lymphocytes in endometriosis. Am. J. Reprod. Immunol. 65(1), 1-10 (2011).
84. Matarese G, De Placido G, Nikas Y, Alviggi C. Pathogenesis of endometriosis: natural immunity dysfunction or autoimmune disease? Trends Mol. Med. 9(5), 223-228 (2003). (Pubitemid 36713393)
85. Ouyang Z, Hirota Y, Osuga Y et al. Interleukin-4 stimulates proliferation of endometriotic stromal cells. Am. J. Pathol. 173(2), 463-469 (2008).
86. Podgaec S, Abrao MS, Dias JA Jr, Rizzo LV, De Oliveira RM, Baracat EC. Endometriosis: an inflammatory disease with a Th2 immune response component. Hum. Reprod. 22(5), 1373-1379 (2007). (Pubitemid 47062809)
87. Fakih H, Baggett B, Holtz G, Tsang KY, Lee JC, Williamson HO. Interleukin-1: a possible role in the infertility associated with endometriosis. Fertil. Steril. 47(2), 213-217 (1987). (Pubitemid 17024497)
88. Hill JA, Anderson DJ. Lymphocyte activity in the presence of peritoneal fluid from fertile women and infertile women with and without endometriosis. Am. J. Obstet. Gynecol. 161(4), 861-864 (1989). (Pubitemid 19266184)
89. Keenan JA, Chen TT, Chadwell NL, Torry DS, Caudle MR. IL-1 βb, TNF-α, and IL-2 in peritoneal fluid and macrophage-conditioned media of women with endometriosis. Am. J. Reprod. Immunol. 34(6), 381-385 (1995). (Pubitemid 3005647)
90. Mori H, Sawairi M, Nakagawa M, Itoh N, Wada K, Tamaya T. Peritoneal fluid interleukin-1 β and tumor necrosis factor in patients with benign gynecologic disease. Am. J. Reprod. Immunol. 26(2), 62-67 (1991).
91. Laird SM, Li TC, Bolton AE. The production of placental protein 14 and interleukin 6 by human endometrial cells in culture. Hum. Reprod. 8(6), 793-798 (1993). (Pubitemid 23193667)
92. Tabibzadeh SS, Santhanam U, Sehgal PB, May LT. Cytokine-induced production of IFN-b 2/IL-6 by freshly explanted human endometrial stromal cells. Modulation by estradiol-17 β. J. Immunol. 142(9), 3134-3139 (1989). (Pubitemid 19129933)
93. Bedaiwy MA, Falcone T, Sharma RK et al. Prediction of endometriosis with serum and peritoneal fluid markers: a prospective controlled trial. Hum. Reprod. 17(2), 426-431 (2002). (Pubitemid 34168452)
94. Darai E, Detchev R, Hugol D, Quang NT. Serum and cyst fluid levels of interleukin (IL) -6, IL-8 and tumour necrosis factor-α in women with endometriomas and benign and malignant cystic ovarian tumours. Hum. Reprod. 18(8), 1681-1685 (2003). (Pubitemid 36958050)
95. Iwabe T, Harada T, Sakamoto Y et al. Gonadotropin-releasing hormone agonist treatment reduced serum interleukin-6 concentrations in patients with ovarian endometriomas. Fertil. Steril. 80(2), 300-304 (2003). (Pubitemid 36959786)
96. Martinez S, Garrido N, Coperias J, et al. Serum interleukin-6 levels are elevated in women with minimal-mild endometriosis. Hum. Reprod. 22(3), 836-842 (2007).
97. Pellicer A, Albert C, Mercader A, Bonilla- Musoles F, Remohi J, Simon C. The follicular and endocrine environment in women with endometriosis: local and systemic cytokine production. Fertil. Steril. 70(3), 425-431 (1998). (Pubitemid 28435625)
98. Othman Eel-D Hd, Salem HT, Khalifa EA, El-Metwally TH, Al-Hendy A. Serum cytokines as biomarkers for nonsurgical prediction of endometriosis. Eur. J. Obstet. Gynecol. Reprod. Biol. 137(2), 240-246 (2008). (Pubitemid 351423457)
99. Jee BC, Suh CS, Kim SH, Moon SY. Serum soluble CD163 and interleukin-6 levels in women with ovarian endometriomas. Gynecol. Obstet. Invest. 66(1), 47-52 (2008). (Pubitemid 352009131)
100. Kalu E, Sumar N, Giannopoulos T et al. Cytokine profiles in serum and peritoneal fluid from infertile women with and without endometriosis. J. Obstet. Gynaecol. Res. 33(4), 490-495 (2007). (Pubitemid 47222738)
101. Seeber B, Sammel MD, Fan X et al. Panel of markers can accurately predict endometriosis in a subset of patients. Fertil. Steril. 89(5), 1073-1081 (2008). (Pubitemid 351671727)
102. Baggiolini M, Clark-Lewis I. Interleukin-8, a chemotactic and inflammatory cytokine. FEBS Lett. 307(1), 97-101 (1992).
103. Gazvani MR, Christmas S, Quenby S, Kirwan J, Johnson PM, Kingsland CR. Peritoneal fluid concentrations of interleukin-8 in women with endometriosis: relationship to stage of disease. Hum. Reprod. 13(7), 1957-1961 (1998).
104. Pizzo A, Salmeri FM, Ardita FV, Sofo V, Tripepi M, Marsico S. Behaviour of cytokine levels in serum and peritoneal fluid of women with endometriosis. Gynecol. Obstet. Invest. 54(2), 82-87 (2002). (Pubitemid 36164637)
105. + T cells. Am. J. Reprod. Immunol. 62(3), 128-138 (2009).
106. Oral E, Olive DL, Arici A. The peritoneal environment in endometriosis. Hum. Reprod. Update 2(5), 385-398 (1996). (Pubitemid 27087175)
107. Yoshimura T, Leonard EJ. Secretion by human fibroblasts of monocyte chemoattractant protein-1, the product of gene JE. J. Immunol. 144(6), 2377-2383 (1990). (Pubitemid 20106583)
108. Yoshimura T, Yuhki N, Moore SK, Appella E, Lerman MI, Leonard EJ. Human monocyte chemoattractant protein-1 (MCP-1).Full-length cDNA cloning, expression in mitogen-stimulated blood mononuclear leukocytes, and sequence similarity to mouse competence gene JE. FEBS Lett. 244(2), 487-493 (1989). (Pubitemid 19067175)
109. Arici A, Oral E, Attar E, Tazuke SI, Olive DL. Monocyte chemotactic protein-1 concentration in peritoneal fluid of women with endometriosis and its modulation of expression in mesothelial cells. Fertil. Steril. 67(6), 1065-1072 (1997). (Pubitemid 27241899)
110. Khorram O, Taylor RN, Ryan IP, Schall TJ, Landers DV. Peritoneal fluid concentrations of the cytokine RANTES correlate with the severity of endometriosis. Am. J. Obstet. Gynecol. 169(6), 1545-1549 (1993). (Pubitemid 24009193)
111. Wieser F, Dogan S, Klingel K, Diedrich K, Taylor RN, Hornung D. Expression and regulation of CCR1 in peritoneal macrophages from women with and without endometriosis. Fertil. Steril. 83(6), 1878-1881 (2005). (Pubitemid 40824835)
112. Debrock S, De Strooper B, Vander Perre S, Hill JA, D'hooghe TM. Tumour necrosis factor-α, interleukin-6 and interleukin-8 do not promote adhesion of human endometrial epithelial cells to mesothelial cells in a quantitative in vitro model. Hum. Reprod. 21(3), 605-609 (2006). (Pubitemid 43372962)
113. Cho SH, Oh YJ, Nam A et al. Evaluation of serum and urinary angiogenic factors in patients with endometriosis. Am. J. Reprod. Immunol. 58(6), 497-504 (2007). (Pubitemid 350091186)
114. sCD4 during danazol treatment in patients with endometriosis. Int. J. Fertil. Womens Med. 42(3), 211-214 (1997).
115. Xavier P, Belo L, Beires J et al. Serum levels of VEGF and TNF-α and their association with C-reactive protein in patients with endometriosis. Arch. Gynecol. Obstet. 273(4), 227-231 (2006). (Pubitemid 43004695)
116. Eisermann J, Gast MJ, Pineda J, Odem RR, Collins JL. Tumor necrosis factor in peritoneal fluid of women undergoing laparoscopic surgery. Fertil. Steril. 50(4), 573-579 (1988).
117. Mclaren J, Prentice A, Charnock-Jones DS et al. Vascular endothelial growth factor is produced by peritoneal fluid macrophages in endometriosis and is regulated by ovarian steroids. J. Clin. Invest. 98(2), 482-489 (1996). (Pubitemid 26255749)
118. Mueller MD, Lebovic DI, Garrett E, Taylor RN. Neutrophils infiltrating the endometrium express vascular endothelial growth factor: potential role in endometrial angiogenesis. Fertil. Steril. 74(1), 107-112 (2000). (Pubitemid 30427282)
119. Shifren JL, Tseng JF, Zaloudek CJ 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. 81(8), 3112-3118 (1996). (Pubitemid 26323917)
120. Becker CM, D'Amato RJ. Angiogenesis and antiangiogenic therapy in endometriosis. Microvasc. Res. 74(2-3), 121-130 (2007). (Pubitemid 350051024)
121. Taylor RN, Lebovic DI, Mueller MD. Angiogenic factors in endometriosis. Ann. NY Acad. Sci. 955, 89-100; discussion 118, 396-406 (2002). (Pubitemid 34271066)
122. Hull ML, Charnock-Jones DS, Chan Cl et al. Antiangiogenic agents are effective inhibitors of endometriosis. J. Clin. Endocrinol. Metab. 88(6), 2889-2899 (2003). (Pubitemid 36733546)
123. Novella-Maestre E, Carda C, Noguera I et al. Dopamine agonist administration causes a reduction in endometrial implants through modulation of angiogenesis in experimentally induced endometriosis. Hum. Reprod. 24(5), 1025-1035 (2009).
124. D'hooghe TM, Debrock S, Meuleman C, Hill JA, Mwenda JM. Future directions in endometriosis research. Obstet. Gynecol. Clin. North Am. 30(1), 221-244 (2003). (Pubitemid 36356723)
125. Osteen KG, Bruner-Tran KL, Eisenberg E. Reduced progesterone action during endometrial maturation: a potential risk factor for the development of endometriosis. Fertil. Steril. 83(3), 529-537 (2005). (Pubitemid 40348557)
126. + Tregs and immune control. J. Clin. Invest. 114(9), 1209-1217 (2004). (Pubitemid 40385288)
127. + lymphocytes correlates with intratumoral angiogenesis in endometrial cancer. Gynecol. Oncol. 110(2), 216-221 (2008).
128. + regulatory T cells during the follicular phase of the menstrual cycle: implications for human reproduction. J. Immunol. 178(4), 2572-2578 (2007). (Pubitemid 46233460)
129. + regulatory T-cells in endometriosis: a potential controlling mechanism for a complex, chronic immunological condition. Hum. Reprod. 25(4), 900-907 (2010).
130. Nandakumar S, Miller CW, Kumaraguru U. T regulatory cells: an overview and intervention techniques to modulate allergy outcome. Clin. Mol. Allergy 7, 5 (2009).
131. Sakaguchi S, Yamaguchi T, Nomura T, Ono M. Regulatory T cells and immune tolerance. Cell 133(5), 775-787 (2008). (Pubitemid 351707693)
132. Thornton AM. T regulatory cells. Curr. Biol. 15(15), R582 (2005).
133. + regulatory T-cell response? Dis. Model Mech. 4(2), 139-140 (2011).
134. + regulatory T cells in the human immune system. Nat. Rev. Immunol. 10(7), 490-500 (2010).
135. Wu MH, Lu CW, Chuang PC, Tsai SJ. Prostaglandin E2: the master of endometriosis? Exp. Biol. Med. (Maywood) 235(6), 668-677 (2010).
136. Dawood MY, Khan-Dawood FS, Wilson L Jr. Peritoneal fluid prostaglandins and prostanoids in women with endometriosis, chronic pelvic inflammatory disease, and pelvic pain. Am. J. Obstet. Gynecol. 148(4), 391-395 (1984). (Pubitemid 14190710)
137. Wu MH, Sun HS, Lin CC et al. Distinct mechanisms regulate cyclooxygenase-1 and -2 in peritoneal macrophages of women with and without endometriosis. Mol. Hum. Reprod. 8(12), 1103-1110 (2002). (Pubitemid 36032848)
138. Akoum A, Lemay A, Maheux R. Estradiol and interleukin-1b exert a synergistic stimulatory effect on the expression of the chemokine regulated upon activation, normal T cell expressed, and secreted in endometriotic cells. J. Clin. Endocrinol. Metab. 87(12), 5785-5792 (2002). (Pubitemid 36034390)
139. Sakamoto Y, Harada T, Horie S et al. Tumor necrosis factor-α- induced interleukin-8 (IL-8) expression in endometriotic stromal cells, probably through nuclear factor-k B activation: gonadotropin-releasing hormone agonist treatment reduced IL-8 expression. J. Clin. Endocrinol. Metab. 88(2), 730-735 (2003). (Pubitemid 36207815)
140. Akoum A, Jolicoeur C, Boucher A. Estradiol amplifies interleukin-1- induced monocyte chemotactic protein-1 expression by ectopic endometrial cells of women with endometriosis. J. Clin. Endocrinol. Metab. 85(2), 896-904 (2000). (Pubitemid 32273685)
141. Akoum A, Lawson C, Mccoll S, Villeneuve M. Ectopic endometrial cells express high concentrations of interleukin (IL)-8 in vivo regardless of the menstrual cycle phase and respond to oestradiol by up-regulating IL-1-induced IL-8 expression in vitro. Mol. Hum. Reprod. 7(9), 859-866 (2001). (Pubitemid 32842754)
142. Provinciali M, Di Stefano G, Muzzioli M, Garzetti GG, Ciavattini A, Fabris N. Relationship between 17-β-estradiol and prolactin in the regulation of natural killer cell activity during progression of endometriosis. J. Endocrinol. Invest. 18(8), 645-652 (1995).
143. Garzetti GG, Ciavattini A, Provinciali M, Muzzioli M, Di Stefano G, Fabris N. Natural cytotoxicity and GnRH agonist administration in advanced endometriosis: positive modulation on natural killer activity. Obstet. Gynecol. 88(2), 234-240 (1996). (Pubitemid 26250298)
144. Umesaki N, Tanaka T, Miyama M, Mizuno K, Kawamura N, Ogita S. Increased natural killer cell activities in patients treated with gonadotropin releasing hormone agonist. Gynecol. Obstet. Invest. 48(1), 66-68 (1999). (Pubitemid 29338843)
145. Wu MY, Chao KH, Chen Su et al. The suppression of peritoneal cellular immunity in women with endometriosis could be restored after gonadotropin releasing hormone agonist treatment. Am. J. Reprod. Immunol. 35(6), 510-516 (1996).
146. Beato M, Klug J. Steroid hormone receptors: an update. Hum. Reprod. Update 6(3), 225-236 (2000). (Pubitemid 30348891)
147. Attia GR, Zeitoun K, Edwards D, Johns A, Carr BR, Bulun SE. Progesterone receptor isoform A but not B is expressed in endometriosis. J. Clin. Endocrinol. Metab. 85(8), 2897-2902 (2000). (Pubitemid 32269170)
148. Igarashi TM, Bruner-Tran KL, Yeaman GR et al. Reduced expression of progesterone receptor-B in the endometrium of women with endometriosis and in cocultures of endometrial cells exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Fertil. Steril. 84(1), 67-74 (2005). (Pubitemid 40991462)
149. Wu Y, Strawn E, Basir Z, Halverson G, Guo SW. Promoter hypermethylation of progesterone receptor isoform B (PR-B) in endometriosis. Epigenetics 1(2), 106-111 (2006).
150. Arruvito L, Giulianelli S, Flores AC et al. NK cells expressing a progesterone receptor are susceptible to progesterone-induced apoptosis. J. Immunol. 180(8), 5746-5753 (2008).
151. Henderson TA, Saunders PT, Moffett-King A, Groome NP, Critchley HO. Steroid receptor expression in uterine natural killer cells. J. Clin. Endocrinol. Metab. 88(1), 440-449 (2003). (Pubitemid 36115200)
152. Khan KN, Masuzaki H, Fujishita A et al. Estrogen and progesterone receptor expression in macrophages and regulation of hepatocyte growth factor by ovarian steroids in women with endometriosis. Hum. Reprod. 20(7), 2004-2013 (2005). (Pubitemid 40932391)
153. Lydon JP, Demayo FJ, Funk CR et al. Mice lacking progesterone receptor exhibit pleiotropic reproductive abnormalities. Genes Dev. 9(18), 2266-2278 (1995).
154. Tibbetts TA, Conneely OM, O'Malley BW. Progesterone via its receptor
155. Bruner-Tran KL, Eisenberg E, Yeaman GR, Anderson TA, Mcbean J, Osteen KG. Steroid and cytokine regulation of matrix metalloproteinase expression in endometriosis and the establishment of experimental endometriosis in nude mice. J. Clin. Endocrinol. Metab. 87(10), 4782-4791 (2002). (Pubitemid 35247076)
156. Bruner-Tran KL, Zhang Z, Eisenberg E, Winneker RC, Osteen KG. Down-regulation of endometrial matrix metalloproteinase-3 and -7 expression in vitro and therapeutic regression of experimental endometriosis in vivo by a novel nonsteroidal progesterone receptor agonist, tanaproget. J. Clin. Endocrinol. Metab. 91(4), 1554-1560 (2006).
157. Parks WC, Wilson CL, Lopez-Boado YS. Matrix metalloproteinases as modulators of inflammation and innate immunity. Nat. Rev. Immunol. 4(8), 617-629 (2004). (Pubitemid 39025047)
158. Heimler I, Rawlins RG, Owen H, Hutz RJ. Dioxin perturbs, in a dose- and time-dependent fashion, steroid secretion, and induces apoptosis of human luteinized granulosa cells. Endocrinology 139(10), 4373-4379 (1998). (Pubitemid 28513727)
159. Moran FM, Vandevoort CA, Overstreet JW, Lasley BL, Conley AJ. Molecular target of endocrine disruption in human luteinizing granulosa cells by 2,3,7,8-tetrachlorodibenzo-p-dioxin: inhibition of estradiol secretion due to decreased 17a-hydroxylase/17,20-lyase cytochrome P450 expression. Endocrinology 144(2), 467-473 (2003). (Pubitemid 36205217)
160. Pocar P, Fischer B, Klonisch T, Hombach- Klonisch S. Molecular interactions of the aryl hydrocarbon receptor and its biological and toxicological relevance for reproduction. Reproduction 129(4), 379-389 (2005). (Pubitemid 40542164)
161. Porpora MG, Medda E, Abballe A et al. Endometriosis and organochlorinated environmental pollutants: a case-control study on Italian women of reproductive age. Environ. Health Perspect. 117(7), 1070-1075 (2009).
162. Bofinger DP, Feng L, Chi LH et al. Effect of TCDD exposure on CYP1A1 and CYP1B1 expression in explant cultures of human endometrium. Toxicol. Sci. 62(2), 299-314 (2001). (Pubitemid 32707745)
163. Bruner-Tran KL, Yeaman GR, Crispens MA, Igarashi TM, Osteen KG. Dioxin may promote inflammation-related development of endometriosis. Fertil. Steril. 89(Suppl. 5), 1287-1298 (2008).
164. Tian Y, Ke S, Denison MS, Rabson AB, Gallo MA. Ah receptor and NF-kB interactions, a potential mechanism for dioxin toxicity. J. Biol. Chem. 274(1), 510-515 (1999). (Pubitemid 29035090)
165. Baba T, Mimura J, Gradin K et al. Structure and expression of the Ah receptor repressor gene. J. Biol. Chem. 276(35), 33101-33110 (2001).
166. Puga A, Barnes SJ, Chang C et al. Activation of transcription factors activator protein-1 and nuclear factor-kB by 2,3,7,8-tetrachlorodibenzo-p- dioxin. Biochem. Pharmacol. 59(8), 997-1005 (2000). (Pubitemid 30110816)
167. Schlezinger JJ, Blickarz CE, Mann KK, Doerre S, Stegeman JJ. Identification of NF-kB in the marine fish Stenotomus chrysops and examination of its activation by aryl hydrocarbon receptor agonists. Chem. Biol. Interact. 126(2), 137-157 (2000). (Pubitemid 30336362)
168. Sulentic CE, Holsapple MP, Kaminski NE. Putative link between transcriptional regulation of IgM expression by 2,3,7,8-tetrachlorodibenzo-p- dioxin and the aryl hydrocarbon receptor/dioxin-responsive enhancer signaling pathway. J. Pharmacol. Exp. Ther. 295(2), 705-716 (2000).
169. yu j, wang y, zhou wh, wang l, he yy, li dj. combination of estrogen and dioxin is involved in the pathogenesis of endometriosis by promoting chemokine secretion and invasion of endometrial stromal cells. hum. reprod. 23(7), 1614-1626 (2008).
170. Quaranta MG, Porpora MG, Mattioli B et al. Impaired NK-cell-mediated cytotoxic activity and cytokine production in patients with endometriosis: a possible role for PCBs and DDE. Life Sci. 79(5), 491-498 (2006). (Pubitemid 43866128)
171. Singh NP, Nagarkatti M, Nagarkatti P. Primary peripheral T cells become susceptible to 2,3,7,8-tetrachlorodibenzo-p-dioxin-mediated apoptosis in vitro upon activation and in the presence of dendritic cells. Mol. Pharmacol. 73(6), 1722-1735 (2008). (Pubitemid 351724360)
172. Singh NP, Nagarkatti M, Nagarkatti PS. Role of dioxin response element and nuclear factor-kB motifs in 2,3,7,8-tetrachlorodibenzo-p-dioxin-mediated regulation of Fas and Fas ligand expression. Mol. Pharmacol. 71(1), 145-157 (2007). (Pubitemid 46020984)
173. Bruner-Tran KL, Osteen KG. Developmental exposure to TCDD reduces fertility and negatively affects pregnancy outcomes across multiple generations. Reprod. Toxicol. 31(3), 344-350 (2011).