Endometriosis: Interaction of immune and endocrine systems

Seminars in Reproductive Medicine

Volumn 21, Issue 2, 2003, Pages 135-144

  Seli, Emre ^a   Arici, Aydin ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cytokines; Endometriosis; Immune response; Treatment of endometriosis

Indexed keywords

CYTOKINE; DANAZOL; GONADORELIN AGONIST; GROWTH FACTOR;

CELL ACTIVITY; CELL PROLIFERATION; CELLULAR IMMUNITY; DISEASE ASSOCIATION; DISEASE PREDISPOSITION; DOWN REGULATION; ENDOCRINE SYSTEM; ENDOMETRIOSIS; ENDOMETRIUM CELL; GYNECOLOGIC DISEASE; HUMAN; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNE SYSTEM; IMMUNOCOMPETENT CELL; IMMUNOLOGY; IMPLANT; INFERTILITY; MACROPHAGE; MENSTRUATION DISORDER; NATURAL KILLER CELL; PATHOGENESIS; PELVIS PAIN SYNDROME; PERITONEAL FLUID; PROTEIN SECRETION; REVIEW; RISK FACTOR; UTERUS CAVITY;

ANTIBODY FORMATION; CYTOKINES; ENDOCRINE GLANDS; ENDOMETRIOSIS; FEMALE; HUMANS; IMMUNE SYSTEM; IMMUNITY, CELLULAR; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 0038042823     PISSN: 15268004     EISSN: None     Source Type: Journal    
DOI: 10.1055/s-2003-41320     Document Type: Review

References (111)

1. Sampson JA. Peritoneal endometriosis due to the menstrual dissemination of endometrial tissue into the peritoneal cavity. Am J Obstet Gynecol 1927;14:422-469
2. Beyth Y, Yaffe H, Levij S, et al. Retrograde seeding of endometrium: a sequela of tubal flushing. Fertil Steril 1975;26:1094-1097
3. Bartosik D, Jacobs SL, Kelly LJ. Endometrial tissue in peritoneal fluid. Fertil Steril 1986;46:796-800
4. TeLinde RW, Scott RB. Experimental endometriosis. Am J Obstet Gynecol 1950;60:1147-1173
5. Ridley JH, Edwards IK. Experimental endometriosis in the human. Am J Obstet Gynecol 1958;76:783-790
6. Jenkins S, Olive DL, Haney AF. Endometriosis: pathogenic implications of the anatomic distribution. Obstet Gynecol 1986;67:335-338
7. Blumenkrantz JM, Gallagher N, Bashore RA, et al. Retrograde menstruation in women undergoing chronic peritoneal dialysis. Obstet Gynecol 1981;57:667-670
8. Halme J, Hammond MG, Hulka JF, et al. Retrograde menstruation in healthy women and in patients with endometriosis. Obstet Gynecol 1984;64:151-154
9. Houston DE, Noller KL, Melton LJ 3rd, et al. Incidence of pelvic endometriosis in Rochester, Minnesota, 1970-1979. Am J Epidemiol 1987;125:959-969
10. Kjerulff KH, Erickson BA, Langenberg PW. Chronic gynecological conditions reported by US women: findings from the National Health Interview Survey, 1984 to 1992. Am J Public Health 1996;86:195-199
11. vanFurth R, Raeburn JA, vanZwet TI. Characteristics of human mononuclear phagocytes. Blood 1979;54:485-500
12. Haney AF, Muscato JJ, Weinberg JB. Peritoneal fluid cell populations in infertility patients. Fertil Steril 1981;35:696-698
13. Olive DL, Weinberg JB, Haney AF. Peritoneal macrophages and infertility: the association between cell number and pelvic pathology. Fertil Steril 1985;44:772-777
14. Halme J, Becher S, Hammond MG, et al. Increased activation of pelvic macrophages in infertile women with mild endometriosis. Am J Obstet Gynecol 1983;145:333-337
15. Zeller JM, Henig I, Radwanska E, et al. Enhancement of human monocyte and peritoneal macrophage chemiluminescence activities in women with endometriosis. Am J Reprod Immunol 1987;13:78-82
16. Dunselman GA, Hendrix MG, Bouckaert PX, et al. Functional aspects of peritoneal macrophages in endometriosis of women. J Reprod Fertil 1988;1988:707-710
17. Hill JA, Faris HMP, Schiff I, et al. Characterization of leukocyte subpopulations in the peritoneal fluid of women with endometriosis. Fertil Steril 1988;50:216-222
18. Lebovic DI, Mueller MD, Taylor RN. Immunobiology of endometriosis. Fertil Steril 2001;75:1-10
19. Ramprasad MP, Fischer W, Witztum JL, et al. The 94- to 97-kDa mouse macrophage membrane protein that recognizes oxidized low density lipoprotein and phosphatidylserine-rich liposomes is identical to macrosialin, the mouse homologue of human CD68. Proc Natl Acad Sci U S A 1995;92:9580-9584
20. Ottnad E, Parthasarathy S, Sambrano GR, et al. A macrophage receptor for oxidized low density lipoprotein distinct from the receptor for acetyl low density lipoprotein: partial purification and role in recognitioh of oxidatively damaged cells. Proc Natl Acad Sci USA 1995;92:1391-1395
21. Stanton LW, White RT, Bryant CM, et al. A macrophage Fc receptor for IgG is also a receptor for oxidized low density lipoprotein. J Biol Chem 1992;267:22446-22451
22. Endemann G, Stanton LW, Madden KS, et al. CD36 is a receptor for oxidized low density lipoprotein. J Biol Chem 1993;268:11811-11816
23. Moulton KS, Wu H, Barnett J, et al. Regulated expression of the human acetylated low density lipoprotein receptor gene and isolation of promoter sequences. Proc Natl Acad Sci USA 1992;89:8102-8106
24. Wu H, Moulton K, Horvai A, et al. Combinatorial interactions between AP-1 and ets domain proteins contribute to the developmental regulation of the macrophage scavenger receptor gene. Mol Cell Biol 1994;14:2129-2139
25. de Villiers WJ, Fraser IP, Gordon S. Cytokine and growth factor regulation of macrophage scavenger receptor expression and function. Immunol Lett 1994;43:73-79
26. Sidell N, Han SW, Parthasarathy S. Regulation and modulation of abnormal immune responses in endometriosis. Ann NY Acad Sci 2002;955:159-173; discussion 199-200, 396-406
27. Kim JG, Keshava C, Murphy AA, et al. Fresh mouse peritoneal macrophages have low scavenger receptor activity. J Lipid Res 1997;38:2207-2215
28. Surrey ES, Halme J. Effect of peritoneal fluid from endometriosis patients on endometrial stromal cell proliferation in vitro. Obstet Gynecol 1990;76:792-797
29. Braun DP, Muriana A, Gebel H, et al. Monocyte-mediated enhancement of endometrial cell proliferation in women with endometriosis. Fertil Steril 1994;61:78-84
30. Holmberg LA, Ault KA. Characterization of natural killer cells induced in the peritoneal exudates of mice infected with Listeria monocytogenes: a study of their tumor target specificity and their expression of murine differentiation antigens and human NK-associated antigens. Cell Immunol 1984;89:151-168
31. Voogt PJ, Falkenburg JH, Fibbe WE, et al. Normal hematopoietic progenitor cells and malignant lymphohematopoietic cells show different susceptibility to direct cell-mediated MHC-non-restricted lysis by T cell receptor-/ CD3-, T cell receptor gamma delta+/CD3+ and T cell receptor-alpha beta+/CD3+ lymphocytes. J Immunol 1989;142:1774-1780
32. Moretta A, Sivori S, Vitale M, et al. Existence of both inhibitory (p58) and activatory (p50) receptors for HLA-C molecules in human natural killer cells. J Exp Med 1995;182:875-884
33. Kikuchi Y, Ishikawa N, Hirata J, et al. Changes of peripheral blood lymphocyte subsets before and after operation of patients with endometriosis. Acta Obstet Gynecol Scand 1993;72:157-161
34. Oosterlynck DJ, Cornillie FJ, Waer M, et al. Women with endometriosis show a defect in natural killer activity resulting in a decreased cytotoxicity to autologous endometrium. Fertil Steril 1991;56:45-51
35. Wilson TJ, Hertzog PJ, Angus D, et al. Decreased natural killer cell activity in endometriosis patients: relationship to disease pathogenesis. Fertil Steril 1994;62:1086-1088
36. Ho HN, Chao KH, Chen HF, et al. Peritoneal natural killer cytotoxicity and CD25+ CD3+ lymphocyte subpopulation are decreased in women with stage III-IV endometriosis. Hum Reprod 1995;10:2671-2675
37. Kanzaki H, Wang H-S, Kariya M, et al. Suppression of natural killer cell activity by sera from patients with endometriosis. Am J Obstet Gynecol 1992;167:257-261
38. Oosterlynck DJ, Meuleman C, Waer M, et al. Immunosuppressive activity of peritoneal fluid in women with endometriosis. Obstet Gynecol 1993;82:206-212
39. Ho HN, Wu MY, Yang YS. Peritoneal cellular immunity and endometriosis. Am J Reprod Immunol 1997;38:400-412
40. Wu MY, Yang JH, Chao KH, et al. Increase in the expression of killer cell inhibitory receptors on peritoneal natural killer cells in women with endometriosis. Fertil Steril 2000;74:1187-1191
41. Maeda N, Izumiya C, Yamamoto Y, et al. Increased killer inhibitory receptor KIR2DL1 expression among natural killer cells in women with pelvic endometriosis. Fertil Steril 2002;77:297-302
42. Garzetti GG, Ciavattini A, Provinciali M, et al. Natural cytotoxicity and GnRH agonist administration in advanced endometriosis: positive modulation on natural killer activity. Obstet Gynecol 1996;88:234-240
43. Hsu CC, Lin YS, Wang ST, et al. Immunomodulation in women with endometriosis receiving GnRH agonist. Obstet Gynecol 1997;89:993-998
44. Vigano P, Di Blasio AM, Busacca M, et al. Danazol suppresses both spontaneous and activated human lymphocyte-mediated cytotoxicity. Am J Reprod Immunol 1992;28:38-42
45. Dmowski WP, Steele RW, Baker GF. Deficient cellular immunity in endometriosis. Am J Obstet Gynecol 1981;141:377-383
46. Steele RW, Dmowski WP, Marmer DJ. Immunologic aspects of human endometriosis. Am J Reprod Immunol 1984;6:33-36
47. Dmowski WP, Gebel HM, Braun DP. The role of cell-mediated immunity in pathogenesis of endometriosis. Acta Obstet Gynecol Scand 1994;159:7-14
48. Gleicher N, Dmowski WP, Siegel I, et al. Lymphocyte subsets in endometriosis. Obstet Gynecol 1984;63:463-466
49. Badawy SZA, Cuenca V, Stitzel A, et al. Immune rosettes of T and B lymphocytes in infertile women with endometriosis. J Reprod Med 1987;32:194-197
50. Mettler L, Volkov NI, Kulakov VI, et al. Lymphocyte subsets in the endometrium of patients with endometriosis throughout the menstrual cycle. Am J Reprod Immunol 1996;36:342-348
51. Witz CA, Montoya IA, Dey TD, et al. Characterization of lymphocyte subpopulations and T cell activation in endometriosis. Am J Reprod Immunol 1994;32:173-179
52. Hill JA, Barbieri RL, Anderson DJ. Immunosuppressive effects of danazol in vitro. Fertil Steril 1987;48:414-418
53. Braun DP, Gebel H, Dmowski WP. Effect of danazol in vitro and in vivo on monocyte-mediated enhancement of endometrial cell proliferation in women with endometriosis. Fertil Steril 1994;62:89-95
54. Weed JC, Arquembourg PC. Endometriosis: can it produce an autoimmune response resulting in infertility? Clin Obstet Gynecol 1980;23:885-893
55. Mathur S, Peress MR, Williamson HO, et al. Autoimmunity to endometrium and ovary in endometriosis. Clin Exp Immunol 1982;50:259-266
56. Gleicher N, el-Roeiy A, Confino E, et al. Is endometriosis an autoimmune disease? Obstet Gynecol 1987;70:115-122
57. Pillai S, Zhou GX, Arnaud P, et al. Antibodies to endometrial transferrin and alpha 2-Heremans Schmidt (HS) glycoprotein in patients with endometriosis. Am J Reprod Immunol 1996;35:483-494
58. Lang GA, Yeaman GR. Autoantibodies in endometriosis sera recognize a Thomsen-Friedenreich-like carbohydrate antigen. J Autoimmun 2001;16:151-161
59. Yeaman GR, Collins JE, Lang GA. Autoantibody responses to carbohydrate epitopes in endometriosis. Ann NY Acad Sci 2002;955:174-182; discussion 199-200, 396-406
60. Gleicher N, el-Roeiy A, Confino E, et al. Reproductive failure because of autoantibodies: unexplained infertility and pregnancy wastage. Am J Obstet Gynecol 1989;160:1376-1380; discussion 1380-1375
61. Glinoer D, Soto MF, Bourdoux P, et al. Pregnancy in patients with mild thyroid abnormalities: maternal and neonatal repercussions. J Clin Endocrinol Metab 1991;73:421-427
62. el-Roeiy A, Dmowski WP, Gleicher N, et al. Danazol but not gonadotropin-releasing hormone agonists suppresses autoantibodies in endometriosis. Fertil Steril 1988;50:864-871
63. Kennedy SH, Starkey PM, Sargent IL, et al. Antiendometrial antibodies in endometriosis measured by an enzyme-linked immunosorbent assay before and after treatment with danazol and nafarelin. Obstet Gynecol 1990;75:914-918
64. Ota H, Igarashi S, Hayakawa M, et al. Effect of danazol on the immunocompetent cells in the eutopic endometrium in patients with endometriosis: a multicenter cooperative study. Fertil Steril 1996;65:545-551
65. Dmowski WP, Rana N, Michalowska J, et al. The effect of endometriosis, its stage and activity, and of autoantibodies on in vitro fertilization and embryo transfer success rates. Fertil Steril 1995;63:555-562
66. Nothnick WB. Treating endometriosis as an autoimmune disease. Fertil Steril 2001;76:223-231
67. Hang L, Slack JH, Amundson C, et al. Induction of murine autoimmune disease by chronic polyclonal B cell activation. J Exp Med 1983;157:874-883
68. Prud'homme GJ, Balderas RS, Dixon FJ, et al. B cell dependence on and response to accessory signals in murine lupus strains. J Exp Med 1983;157:1815-1827
69. Rose NR, Bona C. Defining criteria for autoimmune diseases (Witebsky's postulates revised). Immunol Today 1993;14:426-430
70. 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 1989;161:861-864
71. Fakih H, Bagget B, Holtz G, et al, Interleukin-1: possible role in the infertility associated with endometriosis. Fertil Steril 1987;47:213-217
72. Mori H, Sawairi M, Nakagawa M, et al. Peritoneal fluid interleukin-1 beta and tumor necrosis factor in patients with benign gynecologic disease. Am J Reprod Immunol 1991;26:62-67
73. Keenan JA, Chen TT, Chadwell NL, et al. IL-1β, TNF-α, and IL-2 in peritoneal fluid and macrophage conditioned media of women with endometriosis. Am J Reprod Immunol 1995;34:381-385
74. Lebovic DI, Bentzien F, Chao VA, et al. Induction of an angiogenic phenotype in endometriotic stromal cell cultures by interleukin-1beta. Mol Hum Reprod 2000;6:269-275
75. Vigano P, Gaffuri B, Somigliana E, et al. Expression of intercellular adhesion molecule (ICAM)-1 mRNA and protein is enhanced in endometriosis versus endometrial stromal cells in culture. Mol Hum Reprod 1998;4:1150-1156
76. Hill JA, Haimovici F, Politch J, et al. Effect of soluble products of activated lymphocytes and macrophages (lymphokines and monokines) on human sperm motion parameters. Fertil Steril 1987;47:460-465
77. Hill JA, Haimovici F, Anderson DJ. Products of activated lymphocytes and macrophages inhibit mouse embryo development in vitro. J Immunol 1987;139:2250-2254
78. Sueldo CE, Kelly E, Montoro L, et al. Effect of interleukin-1 on gamete interaction and mouse embryo development. J Reprod Med 1990;35:868-872
79. Koumantakis E, Matalliotakis I, Neonaki M, et al. Soluble serum interleukin-2 receptor, interleukin-6 and interleukin-1a in patients with endometriosis and in controls. Arch Gynecol Obstet 1994;255:107-112
80. Mori H, Nakagawa M, Itoh N, et al. Danazol suppresses the production of interleukin-1 beta and tumor necrosis factor by human monocytes. Am J Reprod Immunol 1990;24:45-50
81. Taketani Y, Kuo TM, Mizuno M. Comparison of cytokine levels and embryo toxicity in peritoneal fluid in infertile women with untreated or treated endometriosis. Am J Obstet Gynecol 1992;167:265-270
82. Arici A, Head JR, MacDonald PC, et al. Regulation of interleukin-8 gene expression in human endometrial cells in culture. Mol Cell Endocrinol 1993;94:195-204
83. Arici A, Tazuke SI, Attar E, et al. 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
84. Arici A, Seli E, Senturk LM, et al. Interleukin-8 in the human endometrium. J Clin Endocrinol Metab 1998;83:1783-1787
85. Ryan IP, Tseng JF, Schriock ED, et al. Interleukin-8 concentrations are elevated in peritoneal fluid of women with endometriosis. Fertil Steril 1995;63:929-932
86. Akoum A, Lawson C, McColl S, et al. 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 2001;7:859-866
87. Garcia-Velasco JA, Arici A. Interleukin-8 stimulates the adhesion of endometrial stromal cells to fibronectin. Fertil Steril 1999;72:336-340
88. Garcia-Velasco JA, Arici A. Interleukin-8 expression in endometrial stromal cells is regulated by integrin-dependent cell adhesion. Mol Hum Reprod 1999;5:1135-1140
89. Spuijbroek MDEH, Dunselman GAJ, Menheere PPJA, et al. Early endometriosis invades the extracellular matrix. Fertil Steril 1992;58:929-933
90. Arici A. Local cytokines in endometrial tissue: the role of interleukin-8 in the pathogenesis of endometriosis. Ann NY Acad Sci 2002;955:101-109; discussion 118, 396-406
91. Arici A, Seli E, Zeyneloglu HB, et al. Interleukin-8 induces proliferation of endometrial stromal cells: a potential autocrine growth factor. J Clin Endocrinol Metab 1998;83:1201-1205
92. Arici A, Oral E, Attar E, et al. 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
93. Jolicoeur C, Boutouil M, Drouin R, et al. Increased expression of monocyte chemotactic protein-1 in the endometrium of women with endometriosis. Am J Pathol 1998;152:125-133
94. 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
95. Akoum A, Lemay A, Brunet C, et al. 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
96. Akoum A, Lemay A, Brunet C, et al. Cytokine-induced secretion of monocyte chemotactic protein-1 by human endometriotic cells in culture. Am J Obstet Gynecol 1995;172:594-600
97. Boucher A, Mourad W, Mailloux J, et al. Ovarian hormones modulate monocyte chemotactic protein-1 expression in endometrial cells of women with endometriosis. Mol Hum Reprod 2000;6:618-626
98. 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 2000;74:969-975
99. 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
100. Khorram O, Taylor RN, Ryan IP, et al. Peritoneal fluid concentrations of the cytokine RANTES correlate with the severity of endometriosis. Am J Obstet Gynecol 1993;169:1545-1549
101. Hornung D, Ryan IP, Chao VA, et al. Immunolocalization and regulation of the chemokine RANTES in human endometrial and endometriosis tissues and cells. J Clin Endocrinol Metab 1997;82:1621-1628
102. Philippeaux MM, Piguet PF. Expression of tumor necrosis factor-alpha and its mRNA in the endometrial mucosa during the menstrual cycle. Am J Pathol 1993;143:480-486
103. Laird SM, Tuckerman EM, Saravelos H, et al. The production of tumour necrosis factor alpha (TNF-alpha) by human endometrial cells in culture. Hum Reprod 1996;11:1318-1323
104. Eisermann J, Gast MJ, Pineda J, et al. Tumor necrosis factor in peritoneal fluid of women undergoing laparoscopic surgery. Fertil Steril 1988;50:573-579
105. Zhang R, Wild R, Ojago J. Effect of tumor necrosis factorα on adhesion of human endometrial stromal cells to peritoneal mesothelial cells: an in vitro system. Fertil Steril 1993;59:1196-1201
106. 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 1996;81:3112-3118
107. Li XF, Gregory J, Ahmed A. Immunolocalisation of vascular endothelial growth factor in human endometrium. Growth Factors 1994;11:277-282
108. 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 1996;98:482-489
109. Brogi E, Wu T, Namiki A, et al. Indirect angiogenic cytokines upregulate VEGF and bFGF gene expression in vascular smooth muscle cells, whereas hypoxia upregulates VEGF expression only. Circulation 1994;90:649-652
110. Ben-Av P, Crofford LJ, Wilder RL, et al. Induction of vascular endothelial growth factor expression in synovial fibroblasts by prostaglandin E and interleukin-1: a potential mechanism for inflammatory angiogenesis. FEBS Lett 1995;372:83-87
111. Donnez J, Smoes P, Gillerot S, et al. Vascular endothelial growth factor (VEGF) in endometriosis. Hum Reprod 1998;13:1686-1690