Endometriosis: Hormone regulation and clinical consequences of chemotaxis and apoptosis

Human Reproduction Update

Volumn 19, Issue 4, 2013, Pages 406-418

  Reis, Fernando M ^a   Petraglia, Felice ^b   Taylor, Robert N ^c  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^b UNIVERSITY OF SIENA   (Italy)

^c WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptosis; Chemokines; Endometriosis; Endometrium; Hormones

Indexed keywords

AROMATASE; BETA CHEMOKINE; CHEMOKINE; CHEMOKINE RECEPTOR CXCR4; CXCL13 CHEMOKINE; ESTROGEN; ESTROGEN RECEPTOR; FRACTALKINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 8; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; MONOCYTE CHEMOTACTIC PROTEIN 2; PROGESTERONE; PROTEIN BCL 2; PROTEIN KINASE B; RANTES; STROMAL CELL DERIVED FACTOR 1;

APOPTOSIS; ARTICLE; CELL PROLIFERATION; CELL VIABILITY; CHEMOTAXIS; CYTOKINE RELEASE; DOWN REGULATION; ENDOCRINE FUNCTION; ENDOMETRIOSIS; ENDOMETRIUM; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; EPITHELIUM CELL; GENETIC POLYMORPHISM; GENETIC VARIABILITY; HORMONAL REGULATION; HUMAN; PARACRINE SIGNALING; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; STROMA CELL; SYSTEMATIC REVIEW; UPREGULATION;

APOPTOSIS; CHEMOKINES; ENDOMETRIOSIS; ENDOMETRIUM; HORMONES;

APOPTOSIS; CHEMOTAXIS; ENDOMETRIOSIS; ENDOMETRIUM; ESTROGENS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; HUMANS; INTERLEUKIN-8; NF-KAPPA B; PROGESTINS; STROMAL CELLS;

EID: 84879424640     PISSN: 13554786     EISSN: 14602369     Source Type: Journal    
DOI: 10.1093/humupd/dmt010     Document Type: Article

References (137)

1. Adamson GD, Kennedy SH, Hummelshoj L. Creating solutions in endometriosis: global collaboration through the World Endometriosis Research Foundation. J Endometriosis 2010;2:3-6.
2. Akoum A, Lemay A, Brunet C, Hebert J. Secretion of monocyte chemotactic protein-1 by cytokine-stimulated endometrial cells of women with endometriosis. Le groupe d'investigation en gynecologie. Fertil Steril 1995; 63:322-328.
3. Akoum A, Lemay A, McColl S, Turcot-Lemay L, Maheux R. Elevated concentration and biologic activity of monocyte chemotactic protein-1 in the peritoneal fluid of patients with endometriosis. Fertil Steril 1996;66:17-23.
4. 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 2000;85:896-904.
5. Akoum A, Lemay A, Maheux R. Estradiol and interleukin-1beta 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 2002;87:5785-5792.
6. Al-Sabbagh M, Lam EW, Brosens JJ. Mechanisms of endometrial progesterone resistance. Mol Cell Endocrinol 2012;358:208-215.
7. Amaral JD, Sola S, Steer CJ, Rodrigues CM. Role of nuclear steroid receptors in apoptosis. Curr Med Chem 2009;16:3886-3902.
8. Arici A, Tazuke SI, Attar E, Kliman HJ, Olive DL. Interleukin-8 concentration in peritoneal fluid of patients with endometriosis and modulation of interleukin-8 expression in human mesothelial cells. Mol Hum Reprod 1996;2:40-45.
9. 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 1997;67:1065-1072.
10. 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 2000; 85:2897-2902.
11. Baggiolini M, Walz A, Kunkel SL. Neutrophil-activating peptide-1/interleukin 8, a novel cytokine that activates neutrophils. J Clin Invest 1989;84:1045-1049.
12. Batt RE. A History of Endometriosis. London: Springer, 2011.
13. Beliard A, Noel A, Foidart JM. Reduction of apoptosis and proliferation in endometriosis. Fertil Steril 2004;82:80-85.
14. Bersinger NA, Gunthert AR, McKinnon B, Johann S, Mueller MD. Dose-response effect of interleukin (IL)-1beta, tumour necrosis factor (TNF)-alpha, and interferon-gamma on the in vitro production of epithelial neutrophil activating peptide-78 (ENA-78), IL-8, and IL-6 by human endometrial stromal cells. Arch Gynecol Obstet 2011;283:1291-1296.
15. Bhavsar PK, Sukkar MB, Khorasani N, Lee KY, Chung KF. Glucocorticoid suppression of CX3CL1 (fractalkine) by reduced gene promoter recruitment of NF-kappaB. FASEB J 2008;22:1807-1816.
16. Boomsma CM, Kavelaars A, Eijkemans MJ, Fauser BC, Heijnen CJ, Macklon NS. Ovarian stimulation for in vitro fertilization alters the intrauterine cytokine, chemokine, and growth factor milieu encountered by the embryo. Fertil Steril 2010;94:1764-1768.
17. Boucher A, Lemay A, Akoum A. Effect of hormonal agents on monocyte chemotactic protein-1 expression by endometrial epithelial cells of women with endometriosis. Fertil Steril 2000a;74:969-975.
18. Boucher A, Mourad W, Mailloux J, Lemay A, Akoum A. Ovarian hormones modulate monocyte chemotactic protein-1 expression in endometrial cells of women with endometriosis. Mol Hum Reprod 2000b;6:618-626.
19. Brandenberger AW, Lebovic DI, Tee MK, Ryan IP, Tseng JF, Jaffe RB, Taylor RN. Oestrogen receptor (ER)-alpha and ER-beta isoforms in normal endometrial and endometriosis-derived stromal cells. Mol Hum Reprod 1999;5:651-655.
20. Braun DP, Ding J, Shaheen F, Willey JC, Rana N, Dmowski WP. Quantitative expression of apoptosis-regulating genes in endometrium from women with and without endometriosis. Fertil Steril 2007;87:263-268.
21. Bulmer JN, Pace D, Ritson A. Immunoregulatory cells in human decidua: morphology, immunohistochemistry and function. Reprod Nutr Dev 1988; 28:1599-1613.
22. Bulun SE, Monsavais D, Pavone ME, Dyson M, Xue Q, Attar E, Tokunaga H, Su EJ. Role of estrogen receptor-beta in endometriosis. Semin Reprod Med 2012; 30:39-45.
23. Caballero-Campo P, Dominguez F, Coloma J, Meseguer M, Remohi J, Pellicer A, Simon C. Hormonal and embryonic regulation of chemokines IL-8, MCP-1 and RANTES in the human endometrium during the window of implantation. Mol Hum Reprod 2002;8:375-384.
24. Cavallini A, Resta L, Caringella AM, Dinaro E, Lippolis C, Loverro G. Involvement of estrogen receptor-related receptors in human ovarian endometriosis. Fertil Steril 2011;96:102-106.
25. Chegini N, Luo X, Pan Q, Rhoton-Vlasak A, Archer DF. Endometrial expression of epithelial neutrophil-activating peptide-78 during the menstrual cycle or in progestin-only contraceptive users with breakthrough bleeding and the influence of doxycycline therapy. Hum Reprod 2007;22:427-433.
26. Choksuchat C, Zhao S, Deutch TD, Kimble TD, Archer DF. Effects of progesterone, levonorgestrel and medroxyprogesterone acetate on apoptosis in human endometrial endothelial cells. Contraception 2009;79:139-145.
27. Cinar O, Seval Y, Uz YH, Cakmak H, Ulukus M, Kayisli UA, Arici A. Differential regulation of Akt phosphorylation in endometriosis. Reprod Biomed Online 2009; 19:864-871.
28. Critchley HO, Tong S, Cameron ST, Drudy TA, Kelly RW, Baird DT. Regulation of bcl-2 gene family members in human endometrium by antiprogestin administration in vivo. J Reprod Fertil 1999;115:389-395.
29. Critchley HO, Kelly RW, Brenner RM, Baird DT. Antiprogestins as a model for progesterone withdrawal. Steroids 2003;68:1061-1068.
30. D'amora P, Maciel TT, Tambellini R, Mori MA, Pesquero JB, Sato H, Girao MJ, Guerreiro da Silva ID, Schor E. Disrupted cell cycle control in cultured endometrial cells from patients with endometriosis harboring the progesterone receptor polymorphism PROGINS. Am J Pathol 2009;175:215-224.
31. De Carvalho CV, Nogueira-De-Souza NC, Costa AM, Baracat EC, Girao MJ, D'Amora P, Schor E, da Silva ID. Genetic polymorphisms of cytochrome P450cl7alpha (CYP17) and progesterone receptor genes (PROGINS) in the assessment of endometriosis risk. Gynecol Endocrinol 2007;23:29-33.
32. DeLoia JA, Stewart-Akers AM, Brekosky J, Kubik C. Stimulation of uterine cell cytokine production by ovarian hormones. Am J Reprod Immunol 2000;44:16-21.
33. Dmowski WP, Gebel HM, Braun DP. The role of cell-mediated immunity in pathogenesis of endometriosis. Acta Obstet Gynecol Scand Suppl 1994;159:7-14.
34. Dominguez F, Galan A, Martin JJ, Remohi J, Pellicer A, Simon C. Hormonal and embryonic regulation of chemokine receptors CXCR1, CXCR4, CCR5 and CCR2B in the human endometrium and the human blastocyst. Mol Hum Reprod 2003;9:189-198.
35. Dufournet C, Uzan C, Fauvet R, Cortez A, Siffroi JP, Darai E. Expression of apoptosis-related proteins in peritoneal, ovarian and colorectal endometriosis. J Reprod Immunol 2006;70:151-162.
36. Dyson MT, Bulun SE. Cutting SRC-1 down to size in endometriosis. Nat Med 2012; 18:1016-1018.
37. Fazleabas AT. Progesterone resistance in a baboon model of endometriosis. Semin Reprod Med 2010;28:75-80.
38. Fujishita A, Nakane PK, Koji T, Masuzaki H, Chavez RO, Yamabe T, Ishimaru T. Expression of estrogen and progesterone receptors in endometrium and peritoneal endometriosis: an immunohistochemical and in situ hybridization study. Fertil Steril 1997;67:856-864.
39. Gebel HM, Braun DP, Tambur A, Frame D, Rana N, Dmowski WP. Spontaneous apoptosis of endometrial tissue is impaired in women with endometriosis. Fertil Steril 1998;69:1042-1047.
40. Gomes MK, Rosa-e-Silva JC, Garcia SB, de Sa Rosa-e-Silva AC, Turatti A, Vieira CS, Ferriani RA. Effects of the levonorgestrel-releasing intrauterine system on cell proliferation, Fas expression and steroid receptors in endometriosis lesions and normal endometrium. Hum Reprod 2009;24: 2736-2745.
41. Gonzalez-Ramos R, Van Langendonckt A, Defrere S, Lousse JC, Mettlen M, Guillet A, Donnez J. Agents blocking the nuclear factor-kappaB pathway are effective inhibitors of endometriosis in an in vivo experimental model. Gynecol Obstet Invest 2008;65:174-186.
42. GoumenouAG,Matalliotakis IM,Tzardi M, Fragouli YG,MahutteNG,AriciA. Apoptosis and differential expression of apoptosis-related proteins in endometriotic glandular and stromal cells. J Soc Gynecol Investig 2004;11:318-322.
43. Halban J. Hysteroadenosis metastatica. Zentralb Gynäkol 1925;7:387-391.
44. Halme J, Becker S, Hammond MG, Raj MH, Raj S. Increased activation of pelvic macrophages in infertile women with mild endometriosis. Am J Obstet Gynecol 1983;145:333-337.
45. Hampton AL, Rogers PA, Affandi B, Salamonsen LA. Expression of the chemokines, monocyte chemotactic protein (MCP)-1 and MCP-2 in endometrium of normal women and Norplant users, does not support a central role in macrophage infiltration into endometrium. J Reprod Immunol 2001;49:115-132.
46. Han SJ, Hawkins SM, Begum K, Jung SY, Kovanci E, Qin J, Lydon JP, Demayo FJ, O'Malley BW. A new isoform of steroid receptor coactivator-1 is crucial for pathogenic progression of endometriosis. Nat Med 2012;18:1102-1111.
47. Haney AF, Muscato JJ, Weinberg JB. Peritoneal fluid cell populations in infertility patients. Fertil Steril 1981;35:696-698.
48. Hannan NJ, Jones RL, Critchley HO, Kovacs GJ, Rogers PA, Affandi B, Salamonsen LA. Coexpression of fractalkine and its receptor in normal human endometrium and in endometrium from users of progestin-only contraception supports a role for fractalkine in leukocyte recruitment and endometrial remodeling. J Clin Endocrinol Metab 2004;89:6119-6129.
49. Harada T, Kaponis A, Iwabe T, Taniguchi F, Makrydimas G, Sofikitis N, Paschopoulos M, Paraskevaidis E, Terakawa N. Apoptosis in human endometrium and endometriosis. Hum Reprod Update 2004;10:29-38.
50. Hassa H, Tanir HM, Tekin B, Artan S, Dundar E, Kirilmaz SD, Sahin Mutlu F. Apoptosis patterns in eutopic and ectopic endometrium, adhesions and normal-looking peritoneum from women with or without endometriosis. Arch Gynecol Obstet 2009;280:195-199.
51. Horie S, Harada T, Mitsunari M, Taniguchi F, Iwabe T, Terakawa N. Progesterone and progestational compounds attenuate tumor necrosis factor alpha-induced interleukin-8 production via nuclear factor kappa B inactivation in endometriotic stromal cells. Fertil Steril 2005;83:1530-1535.
52. Hornung D, Ryan IP, Chao VA, Vigne JL, Schriock ED, Taylor RN. Immunolocalization and regulation of the chemokine RANTES in human endometrial and endometriosis tissues and cells. J Clin Endocrinol Metab 1997;82:1621-1628.
53. Hornung D, Dohrn K, Sotlar K, Greb RR, Wallwiener D, Kiesel L, Taylor RN. Localization in tissues and secretion of eotaxin by cells from normal endometrium and endometriosis. J Clin Endocrinol Metab 2000;85:2604-2608.
54. Hornung D, Bentzien F, Wallwiener D, Kiesel L, Taylor RN. Chemokine bioactivity of RANTES in endometriotic and normal endometrial stromal cells and peritoneal fluid. Mol Hum Reprod 2001a;7:163-168.
55. Hornung D, Klingel K, Dohrn K, Kandolf R, Wallwiener D, Taylor RN. Regulated on activation, normal T-cell-expressed and -secreted mRNA expression in normal endometrium and endometriotic implants: assessment of autocrine/paracrine regulation by in situ hybridization. Am J Pathol 2001b;158:1949-1954.
56. Imai A, Takagi A, Tamaya T. Gonadotropin-releasing hormone analog repairs reduced endometrial cell apoptosis in endometriosis in vitro. Am J Obstet Gynecol 2000;182:1142-1146.
57. Isozaki T, Otsuka K, Sato M, Takahashi R, Wakabayashi K, Yajima N, Miwa Y, Kasama T. Synergistic induction of CX3CL1 by interleukin-1beta and interferon-gamma in human lung fibroblasts: involvement of signal transducer and activator of transcription 1 signaling pathways. Transl Res 2011;157:64-70.
58. Izawa M, Harada T, Deura I, Taniguchi F, Iwabe T, Terakawa N. Drug-induced apoptosis was markedly attenuated in endometriotic stromal cells. Hum Reprod 2006;21:600-604.
59. Jain JK, Li A, Yang W, Minoo P, Felix JC. Effects of mifepristone on proliferation and apoptosis of human endometrium in new users of medroxyprogesterone acetate. Hum Reprod 2006;21:798-809.
60. Jolicoeur C, Boutouil M, Drouin R, Paradis I, Lemay A, Akoum A. Increased expression of monocyte chemotactic protein-1 in the endometrium of women with endometriosis. Am J Pathol 1998;152:125-133.
61. Jolicoeur C, Lemay A, Akoum A. Comparative effect of danazol and a GnRH agonist on monocyte chemotactic protein-1 expression by endometriotic cells. Am J Reprod Immunol 2001;45:86-93.
62. Jones RK, Bulmer JN, Searle RF. Phenotypic and functional studies of leukocytes in human endometrium and endometriosis. Hum Reprod Update 1998;4:702-709.
63. Jones RL, Morison NB, Hannan NJ, Critchley HO, Salamonsen LA. Chemokine expression is dysregulated in the endometrium of women using progestin-only contraceptives and correlates to elevated recruitment of distinct leukocyte populations. Hum Reprod 2005;20:2724-2735.
64. Kao LC, Germeyer A, Tulac S, Lobo S, Yang JP, Taylor RN, Osteen K, Lessey BA, Giudice LC. Expression profiling of endometrium from women with endometriosis reveals candidate genes for disease-based implantation failure and infertility. Endocrinology 2003;144:2870-2881.
65. Kelly RW, Illingworth P, Baldie G, Leask R, Brouwer S, Calder AA. Progesterone control of interleukin-8 production in endometrium and chorio-decidual cells underlines the role of the neutrophil in menstruation and parturition. Hum Reprod 1994;9:253-258.
66. Kerr JF, Wyllie AH, Currie AR. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 1972;26:239-257.
67. 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 1993;169:1545-1549.
68. Kitaya K, Nakayama T, Okubo T, Kuroboshi H, Fushiki S, Honjo H. Expression of macrophage inflammatory protein-1beta in human endometrium: its role in endometrial recruitment of natural killer cells. J Clin Endocrinol Metab 2003; 88:1809-1814.
69. Kizilay G, Cakmak H, Yen CF, Atabekoglu C, Arici A, Kayisli UA. Expression and regulation of c-Jun N-terminal kinase (JNK) in endometrial cells in vivo and in vitro. Histochem Cell Biol 2008;130:761-771.
70. Klemmt PA, Carver JG, Kennedy SH, Koninckx PR, Mardon HJ. Stromal cells from endometriotic lesions and endometrium from women with endometriosis have reduced decidualization capacity. Fertil Steril 2006;85:564-572.
71. Lattuada D, Somigliana E, Vigano P, Candiani M, Pardi G, Di Blasio AM. Genetics of endometriosis: a role for the progesterone receptor gene polymorphism PROGINS? Clin Endocrinol (Oxf) 2004;61:190-194.
72. Lebovic DI, Chao VA, Martini JF, Taylor RN. IL-1beta induction of RANTES (regulated upon activation, normal T cell expressed and secreted) chemokine gene expression in endometriotic stromal cells depends on a nuclear factor-kappaB site in the proximal promoter. J Clin Endocrinol Metab 2001a;86:4759-4764.
73. Lebovic DI, Mueller MD, Taylor RN. Immunobiology of endometriosis. Fertil Steril 2001b;75:1-10.
74. Leiva MC, Hasty LA, Pfeifer S, Mastroianni L Jr, Lyttle CR. Increased chemotactic activity of peritoneal fluid in patients with endometriosis. Am J Obstet Gynecol 1993;168:592-598.
75. Li HY, Chang SP, Yuan CC, Chao HT, Ng HT, Sung YJ. Nitric oxide induces extensive apoptosis in endometrial epithelial cells in the presence of progesterone: involvement of mitogen-activated protein kinase pathways. Mol Hum Reprod 2001;7:755-763.
76. Li A, Felix JC, Hao J, Minoo P, Jain JK. Menstrual-like breakdown and apoptosis in human endometrial explants. Hum Reprod 2005;20:1709-1719.
77. Lockwood CJ, Kumar P, Krikun G, Kadner S, Dubon P, Critchley H, Schatz F. Effects of thrombin, hypoxia, and steroids on interleukin-8 expression in decidualized human endometrial stromal cells: implications for long-term progestin-only contraceptive-induced bleeding. J Clin Endocrinol Metab 2004; 89:1467-1475.
78. Lovely LP, Fazleabas AT, Fritz MA, McAdams DG, Lessey BA. Prevention of endometrial apoptosis: randomized prospective comparison of human chorionic gonadotropin versus progesterone treatment in the luteal phase. J Clin Endocrinol Metab 2005;90:2351-2356.
79. Luk J, Seval Y, Kayisli UA, Ulukus M, Ulukus CE, Arici A. Regulation of interleukin-8 expression in human endometrial endothelial cells: a potential mechanism for the pathogenesis of endometriosis. J Clin Endocrinol Metab 2005;90:1805-1811.
80. Luk J, Seval Y, Ulukus M, Ulukus EC, Arici A, Kayisli UA. Regulation of monocyte chemotactic protein-1 expression in human endometrial endothelial cells by sex steroids: a potential mechanism for leukocyte recruitment in endometriosis. Reprod Sci 2010;17:278-287.
81. Macklon NS, van der Gaast MH, Hamilton A, Fauser BC, Giudice LC. The impact of ovarian stimulation with recombinant FSH in combination with GnRH antagonist on the endometrial transcriptome in the window of implantation. Reprod Sci 2008; 15:357-365.
82. Matta P, Lockwood CJ, Schatz F, Krikun G, Rahman M, Buchwalder L, Norwitz ER. Thrombin regulates monocyte chemoattractant protein-1 expression in human first trimester and term decidual cells. Am J Obstet Gynecol 2007;196:268e261- 268.
83. 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.
84. Meigs JV. Endometrial hematomas of the ovary. Boston Med Surg J 1922;187:1-13. Meresman GF, Auge L, Baranao RI, Lombardi E, Tesone M, Sueldo C. Oral contraceptives suppress cell proliferation and enhance apoptosis of eutopic endometrial tissue from patients with endometriosis. Fertil Steril 2002;77:1141-1147.
85. Meresman GF, Auge L, Baranao RI, Lombardi E, Tesone M, Sueldo C. Oral contraceptives suppress cell proliferation and enhance apoptosis of eutopic endometrial tissue from patients with endometriosis. Fertil Steril 2002;77:1141-1147.
86. Meresman GF, Bilotas M, Buquet RA, Baranao RI, Sueldo C, Tesone M. Gonadotropin-releasing hormone agonist induces apoptosis and reduces cell proliferation in eutopic endometrial cultures from women with endometriosis. Fertil Steril 2003;80(Suppl 2):702-707.
87. Meyer R. Zur Frage der heterotopen Epithelwucherung, insbesondere des Peritonealepithels und in die Ovarien. Virch Arch Path Anat Phys 1924;250:595-610.
88. Mizutani T, Sugihara A, Nakamuro K, Suehara N, Terada N. The gonadotropin-releasing hormone agonist leuprolide acetate induces apoptosis and suppresses cell proliferative activity in rectovaginal endometriosis. Am J Obstet Gynecol 1999;181:750-751.
89. Morsch DM, Carneiro MM, Lecke SB, Araujo FC, Camargos AF, Reis FM, Spritzer PM. c-fos gene and protein expression in pelvic endometriosis: a local marker of estrogen action. J Mol Histol 2009;40:53-58.
90. Mueller MD, Lebovic DI, Garrett E, Taylor RN. Neutrophils infiltrating the endometrium express vascular endothelial growth factor: potential role in endometrial angiogenesis. Fertil Steril 2000;74:107-112.
91. 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 2003;79(Suppl 1):815-820.
92. Murk W, Atabekoglu CS, Cakmak H, Heper A, Ensari A, Kayisli UA, Arici A. Extracellularly signal-regulated kinase activity in the human endometrium: possible roles in the pathogenesis of endometriosis. J Clin Endocrinol Metab 2008;93:3532-3540.
93. Na YJ, LeeDH, Kim SC, Joo JK,Wang JW, Jin JO, Kwak JY, Lee KS. Effects of peritoneal fluid from endometriosis patients on the release of monocyte-specific chemokines by leukocytes. Arch Gynecol Obstet 2011;283:1333-1341.
94. Nasu K, Arima K, Kai K, Fujisawa K, Nishida M, Miyakawa I. Expression of epithelial neutrophil-activating peptide 78 in cultured human endometrial stromal cells. Mol Hum Reprod 2001;7:453-458.
95. Nasu K, NishidaM, Kawano Y, Tsuno A,AbeW, YugeA, TakaiN, NaraharaH.Aberrant expression of apoptosis-related molecules in endometriosis: a possible mechanism underlying the pathogenesis of endometriosis. Reprod Sci 2011;18:206-218.
96. Near AM, Wu AH, Templeman C, Van Den Berg DJ, Doherty JA, Rossing MA, Goode EL, Cunningham JM, Vierkant RA, Fridley BL et al. Progesterone receptor gene polymorphisms and risk of endometriosis: results from an international collaborative effort. Fertil Steril 2011;95:40-45.
97. Nezhat FR, Kalir T. Comparative immunohistochemical studies of endometriosis lesions and endometriotic cysts. Fertil Steril 2002;78:820-824.
98. Nishida M, Nasu K, Ueda T, Fukuda J, Takai N, Miyakawa I. Endometriotic cells are resistant to interferon-gamma-induced cell growth inhibition and apoptosis: a possible mechanism involved in the pathogenesis of endometriosis. Mol Hum Reprod 2005;11:29-34.
99. Okada H, Okamoto R, Tsuzuki T, Tsuji S, Yasuda K, Kanzaki H. Progestins inhibit estradiol-induced vascular endothelial growth factor and stromal cell-derived factor 1 in human endometrial stromal cells. Fertil Steril 2011;96:786-791.
100. Oral E, Seli E, Bahtiyar MO, Olive DL, Arici A. Growth-regulated alpha expression in the peritoneal environment with endometriosis. Obstet Gynecol 1996;88:1050-1056.
101. Otsuki Y, Misaki O, Sugimoto O, Ito Y, Tsujimoto Y, Akao Y. Cyclic bcl-2 gene expression in human uterine endometrium during menstrual cycle. Lancet 1994; 344:28-29.
102. Pavone ME, Reierstad S, Sun H, Milad M, Bulun SE, Cheng YH. Altered retinoid uptake and action contributes to cell survival in endometriosis. J Clin Endocrinol Metab 2010;95:E300-E309.
103. Peloggia A, Petta CA, Bahamondes L, Oliveira-Ribeiro M, Zhang J, Salamonsen L. Endometrial chemokines, uterine natural killer cells and mast cells in long-term users of the levonorgestrel-releasing intrauterine system.HumReprod 2006;21:1129-1134.
104. Ramhorst R, Patel R, Corigliano A, Etchepareborda JJ, Fainboim L, Schust D. Induction of maternal tolerance to fetal alloantigens by RANTES production. Am J Reprod Immunol 2006;56:302-311.
105. Ruiz A, Salvo VA, Ruiz LA, Baez P, Garcia M, Flores I. Basal and steroid hormone-regulated expression of CXCR4 in human endometrium and endometriosis. Reprod Sci 2010;17:894-903.
106. Ryan IP, Tseng JF, Schriock ED, Khorram O, Landers DV, Taylor RN. Interleukin-8 concentrations are elevated in peritoneal fluid of women with endometriosis. Fertil Steril 1995;63:929-932.
107. Sampson JA. Peritoneal endometriosis due to menstrual dissemination of endometrial tissue into the peritoneal cavity. Am J Obstet Gynecol 1927;14:422-429.
108. Schall TJ, Jongstra J, Dyer BJ, Jorgensen J, Clayberger C, Davis MM, Krensky AM. A human T cell-specific molecule is a member of a new gene family. J Immunol 1988; 141:1018-1025.
109. Selam B, Kayisli UA, Akbas GE, Basar M, Arici A. Regulation of FAS ligand expression by chemokine ligand 2 in human endometrial cells. Biol Reprod 2006;75:203-209.
110. Seli E, Senturk LM, Bahtiyar OM, Kayisli UA, Arici A. Expression of aminopeptidase N in human endometrium and regulation of its activity by estrogen. Fertil Steril 2001;75:1172-1176.
111. Shi YL, Luo XZ, Zhu XY, Hua KQ, Zhu Y, Li DJ. Effects of combined 17beta-estradiol with TCDD on secretion of chemokine IL-8 and expression of its receptor CXCR1 in endometriotic focus-associated cells in co-culture. Hum Reprod 2006;21:870-879.
112. Shimoya K, Zhang Q, Temma-Asano K, Hayashi S, Kimura T, Murata Y. Fractalkine in the peritoneal fluid of women with endometriosis. Int J Gynaecol Obstet 2005; 91:36-41.
113. Song J, Rutherford T, Naftolin F, Brown S, Mor G. Hormonal regulation of apoptosis and the Fas and Fas ligand system in human endometrial cells. Mol Hum Reprod 2002;8:447-455.
114. Sozzani S, Agwu DE, Ellenburg MD, Locati M, Rieppi M, Rojas A, Mantovani A, McPhail LC. Activation of phospholipase D by interleukin-8 in human neutrophils. Blood 1994;84:3895-3901.
115. Strieter RM, Belperio JA, Burdick MD, Sharma S, Dubinett SM, Keane MP. CXC chemokines: angiogenesis, immunoangiostasis, and metastases in lung cancer. Ann N Y Acad Sci 2004;1028:351-360.
116. Suzumori N, Katano K, Suzumori K. Peritoneal fluid concentrations of epithelial neutrophil-activating peptide-78 correlate with the severity of endometriosis. Fertil Steril 2004;81:305-308.
117. Szymanowski K. Apoptosis pattern in human endometrium in women with pelvic endometriosis. Eur J Obstet Gynecol Reprod Biol 2007;132:107-110.
118. Tabibzadeh S. The signals and molecular pathways involved in human menstruation, a unique process of tissue destruction and remodelling. Mol Hum Reprod 1996; 2:77-92.
119. Tang L, Zhang Y, Pan H, Luo Q, Zhu XM, Dong MY, Leung PC, Sheng JZ, Huang HF. Involvement of cyclin B1 in progesterone-mediated cell growth inhibition, G2/M cell cycle arrest, and apoptosis in human endometrial cell. Reprod Biol Endocrinol 2009;7:144.
120. Tao XJ, Sayegh RA, Tilly JL, Isaacson KB. Elevated expression of the proapoptotic BCL-2 family member, BAK, in the human endometrium coincident with apoptosis during the secretory phase of the cycle. Fertil Steril 1998;70:338-343.
121. Taylor RN. Classical and neo-classical concepts in the etiology of endometriosis. In: Hédon B, Mettler L, Tinneberg H-R (eds) 20th World Congress on Fertility and Sterility. Germany: Lukon-Verlagsgesellschaft, 2010, 70-73.
122. Taylor RN, Yu J, Torres PB, Schickedanz AC, Park JK, Mueller MD, Sidell N. Mechanistic and therapeutic implications of angiogenesis in endometriosis. Reprod Sci 2009;16:140-146.
123. Tsutsumi A, Okada H, Nakamoto T, Okamoto R, Yasuda K, Kanzaki H. Estrogen induces stromal cell-derived factor 1 (SDF-1/CXCL12) production in human endometrial stromal cells: a possible role of endometrial epithelial cell growth. Fertil Steril 2011;95:444-447.
124. Vaskivuo TE, Stenback F, Karhumaa P, Risteli J, Dunkel L, Tapanainen JS. Apoptosis and apoptosis-related proteins in human endometrium. Mol Cell Endocrinol 2000; 165:75-83.
125. Vinatier D, Dufour P, Oosterlynck D. Immunological aspects of endometriosis. Hum Reprod Update 1996;2:371-384.
126. von Rango U, Classen-Linke I, Krusche CA, Beier HM. The receptive endometrium is characterized by apoptosis in the glands. Hum Reprod 1998;13:3177-3189.
127. von Rokitansky C. Lehrbuch der pathologischen anatomie. Wien: Braunmüller, 1861. Wang XQ, Yu J, Luo XZ, Shi YL, Wang Y,Wang L, Li DJ. The high level of RANTES in the ectopic milieu recruits macrophages and induces their tolerance in progression of endometriosis. J Mol Endocrinol 2010;45:291-299.
128. Wang XQ, Yu J, Luo XZ, Shi YL, Wang Y,Wang L, Li DJ. The high level of RANTES in the ectopic milieu recruits macrophages and induces their tolerance in progression of endometriosis. J Mol Endocrinol 2010;45:291-299.
129. Weed JC, Arquembourg PC. Endometriosis: can it produce an autoimmune response resulting in infertility? Clin Obstet Gynecol 1980;23:885-893.
130. Weil SJ, Wang S, Perez MC, Lyttle CR. Chemotaxis of macrophages by a peritoneal fluid protein in women with endometriosis. Fertil Steril 1997;67:865-869.
131. Wieser F, Schneeberger C, Tong D, Tempfer C, Huber JC, Wenzl R. PROGINS receptor gene polymorphism is associated with endometriosis. Fertil Steril 2002; 77:309-312.
132. Wieser F, Vigne JL, Ryan I, Hornung D, Djalali S, Taylor RN. Sulindac suppresses nuclear factor-kappaB activation and RANTES gene and protein expression in endometrial stromal cells from women with endometriosis. J Clin Endocrinol Metab 2005;90:6441-6447.
133. Wu HM, Wang HS, Huang HY, Soong YK, MacCalman CD, Leung PC. GnRH signaling in intrauterine tissues. Reproduction 2009;137:769-777.
134. Yeaman GR, Guyre PM, FangerMW, Collins JE, White HD, RathbunW, Orndorff KA, Gonzalez J, Stern JE, Wira CR. Unique CD8+ T cell-rich lymphoid aggregates in human uterine endometrium. J Leukoc Biol 1997;61:427-435.
135. 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 2008;23:1614-1626.
136. Zhao D, Lebovic DI, Taylor RN. Long-term progestin treatment inhibits RANTES (regulated on activation, normal T cell expressed and secreted) gene expression in human endometrial stromal cells. J Clin Endocrinol Metab 2002;87: 2514-2519.
137. Zubor P, Hatok J, Galo S, Dokus K, Klobusiakova D, Danko J, Racay P. Anti-apoptotic and pro-apoptotic gene expression evaluated from eutopic endometrium in the proliferative phase of the menstrual cycle among women with endometriosis and healthy controls. Eur J Obstet Gynecol Reprod Biol 2009; 145:172-176.