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Published in: Seminars in Immunopathology 2/2007

Open Access 01-06-2007 | Review

Neuroendocrine–immune disequilibrium and endometriosis: an interdisciplinary approach

Authors: Nadja Tariverdian, Theoharis C. Theoharides, Friederike Siedentopf, Gabriela Gutiérrez, Udo Jeschke, Gabriel A. Rabinovich, Sandra M. Blois, Petra C. Arck

Published in: Seminars in Immunopathology | Issue 2/2007

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Abstract

Endometriosis, a chronic disease characterized by endometrial tissue located outside the uterine cavity, affects one fourth of young women and is associated with chronic pelvic pain and infertility. However, an in-depth understanding of the pathophysiology and effective treatment strategies of endometriosis is still largely elusive. Inadequate immune and neuroendocrine responses are significantly involved in the pathophysiology of endometriosis, and key findings are summarized in the present review. We discuss here the role of different immune mechanisms particularly adhesion molecules, protein–glycan interactions, and pro-angiogenic mediators in the development and progression of the disease. Finally, we introduce the concept of endometrial dissemination as result of a neuroendocrine-immune disequilibrium in response to high levels of perceived stress caused by cardinal clinical symptoms of endometriosis.
Literature
1.
go back to reference Rokitansky K (1860) Über Uterusdrüsen-Neubildung. Z Gesellschaft Aerzte (Wien) 16:577–581 Rokitansky K (1860) Über Uterusdrüsen-Neubildung. Z Gesellschaft Aerzte (Wien) 16:577–581
2.
go back to reference Moen MH, Muus KM (1991) Endometriosis in pregnant and non-pregnant women at tubal sterilization. Hum Reprod 6:699–702PubMed Moen MH, Muus KM (1991) Endometriosis in pregnant and non-pregnant women at tubal sterilization. Hum Reprod 6:699–702PubMed
3.
go back to reference Koninckx PR, Meuleman C, Demeyere S, Lesaffre E, Cornillie FJ (1991) Suggestive evidence that pelvic endometriosis is a progressive disease, whereas deeply infiltrating endometriosis is associated with pelvic pain. Fertil Steril 55:759–765PubMed Koninckx PR, Meuleman C, Demeyere S, Lesaffre E, Cornillie FJ (1991) Suggestive evidence that pelvic endometriosis is a progressive disease, whereas deeply infiltrating endometriosis is associated with pelvic pain. Fertil Steril 55:759–765PubMed
4.
go back to reference Bruckner C (2004) Symptoms and diagnosis. In: Steck T, Felberbaum R, Küpker W, Bruckner C, Finas D (eds) Endometriosis. Development, diagnosis, progression, therapy. Springer, New York, pp 81–101 Bruckner C (2004) Symptoms and diagnosis. In: Steck T, Felberbaum R, Küpker W, Bruckner C, Finas D (eds) Endometriosis. Development, diagnosis, progression, therapy. Springer, New York, pp 81–101
5.
go back to reference Steck T (2004) Manifestations and progression. In: Steck T, Felberbaum R, Küpker W, Bruckner C, Finas D (eds) Endometriosis. Development, diagnosis, progression, therapy. Springer, Berlin Heidelberg New York, pp 37–79 Steck T (2004) Manifestations and progression. In: Steck T, Felberbaum R, Küpker W, Bruckner C, Finas D (eds) Endometriosis. Development, diagnosis, progression, therapy. Springer, Berlin Heidelberg New York, pp 37–79
6.
go back to reference Redwine DB (1999) Ovarian endometriosis: a marker for more extensive pelvic and intestinal disease. Fertil Steril 72:310–315PubMed Redwine DB (1999) Ovarian endometriosis: a marker for more extensive pelvic and intestinal disease. Fertil Steril 72:310–315PubMed
7.
go back to reference ASRM (1997) Revised American Society for Reproductive Medicine classification of endometriosis: 1996. Fertil Steril 67:817–821 ASRM (1997) Revised American Society for Reproductive Medicine classification of endometriosis: 1996. Fertil Steril 67:817–821
8.
go back to reference Tummon IS, Maclin VM, Radwanska E, Binor Z, Dmowski WP (1988) Occult ovulatory dysfunction in women with minimal endometriosis or unexplained infertility. Fertil Steril 50:716–720PubMed Tummon IS, Maclin VM, Radwanska E, Binor Z, Dmowski WP (1988) Occult ovulatory dysfunction in women with minimal endometriosis or unexplained infertility. Fertil Steril 50:716–720PubMed
9.
go back to reference Harlow CR, Cahill DJ, Maile LA, Talbot WM, Mears J, Wardle PG, Hull MG (1996) Reduced preovulatory granulosa cell steroidogenesis in women with endometriosis. J Clin Endocrinol Metab 81:426–429PubMed Harlow CR, Cahill DJ, Maile LA, Talbot WM, Mears J, Wardle PG, Hull MG (1996) Reduced preovulatory granulosa cell steroidogenesis in women with endometriosis. J Clin Endocrinol Metab 81:426–429PubMed
10.
go back to reference Suginami H, Yano K, Watanabe K, Matsuura S (1986) A factor inhibiting ovum capture by the oviductal fimbriae present in endometriosis peritoneal fluid. Fertil Steril 46:1140–1146PubMed Suginami H, Yano K, Watanabe K, Matsuura S (1986) A factor inhibiting ovum capture by the oviductal fimbriae present in endometriosis peritoneal fluid. Fertil Steril 46:1140–1146PubMed
11.
go back to reference Jha P, Farooq A, Agarwal N, Buckshee K (1996) In vitro sperm phagocytosis by human peritoneal macrophages in endometriosis-associated infertility. Am J Reprod Immunol 36:235–237PubMed Jha P, Farooq A, Agarwal N, Buckshee K (1996) In vitro sperm phagocytosis by human peritoneal macrophages in endometriosis-associated infertility. Am J Reprod Immunol 36:235–237PubMed
12.
go back to reference Haney AF, Misukonis MA, Weinberg JB (1983) Macrophages and infertility: oviductal macrophages as potential mediators of infertility. Fertil Steril 39:310–315PubMed Haney AF, Misukonis MA, Weinberg JB (1983) Macrophages and infertility: oviductal macrophages as potential mediators of infertility. Fertil Steril 39:310–315PubMed
13.
go back to reference Nip MM, Taylor PV, Rutherford AJ, Hancock KW (1995) Autoantibodies and antisperm antibodies in sera and follicular fluids of infertile patients; relation to reproductive outcome after in-vitro fertilization. Hum Reprod 10:2564–2569PubMed Nip MM, Taylor PV, Rutherford AJ, Hancock KW (1995) Autoantibodies and antisperm antibodies in sera and follicular fluids of infertile patients; relation to reproductive outcome after in-vitro fertilization. Hum Reprod 10:2564–2569PubMed
14.
go back to reference Aeby TC, Huang T, Nakayama RT (1996) The effect of peritoneal fluid from patients with endometriosis on human sperm function in vitro. Am J Obstet Gynecol 174:1779–1783 (discussion 1783–1785)PubMed Aeby TC, Huang T, Nakayama RT (1996) The effect of peritoneal fluid from patients with endometriosis on human sperm function in vitro. Am J Obstet Gynecol 174:1779–1783 (discussion 1783–1785)PubMed
15.
go back to reference Qiao J, Yeung WS, Yao YQ, Ho PC (1998) The effects of follicular fluid from patients with different indications for IVF treatment on the binding of human spermatozoa to the zona pellucida. Hum Reprod 13:128–131PubMed Qiao J, Yeung WS, Yao YQ, Ho PC (1998) The effects of follicular fluid from patients with different indications for IVF treatment on the binding of human spermatozoa to the zona pellucida. Hum Reprod 13:128–131PubMed
16.
go back to reference Damewood MD, Hesla JS, Schlaff WD, Hubbard M, Gearhart JD, Rock JA (1990) Effect of serum from patients with minimal to mild endometriosis on mouse embryo development in vitro. Fertil Steril 54:917–920PubMed Damewood MD, Hesla JS, Schlaff WD, Hubbard M, Gearhart JD, Rock JA (1990) Effect of serum from patients with minimal to mild endometriosis on mouse embryo development in vitro. Fertil Steril 54:917–920PubMed
17.
go back to reference Matson PL, Yovich JL (1986) The treatment of infertility associated with endometriosis by in vitro fertilization. Fertil Steril 46:432–434PubMed Matson PL, Yovich JL (1986) The treatment of infertility associated with endometriosis by in vitro fertilization. Fertil Steril 46:432–434PubMed
18.
go back to reference Sampson J (1927) Peritoneal endometriosis due to the menstrual dissemination of endometrial tissue into the peritoneal cavity. Am J Obstet Gynecol 14:422 Sampson J (1927) Peritoneal endometriosis due to the menstrual dissemination of endometrial tissue into the peritoneal cavity. Am J Obstet Gynecol 14:422
19.
go back to reference Meyer R (1919) Über den Stand der Frage der Adenomyositis und Adenomyome im allgemeinen und insbesondere über Adenomyositis seroepithelialis und Adenomyometritis sarcomatosa. Zentralbl Gynäkol 43:745–750 Meyer R (1919) Über den Stand der Frage der Adenomyositis und Adenomyome im allgemeinen und insbesondere über Adenomyositis seroepithelialis und Adenomyometritis sarcomatosa. Zentralbl Gynäkol 43:745–750
20.
go back to reference Quinn M (2004) Endometriosis: the consequence of neurological dysfunction? Med Hypotheses 63:602–608PubMed Quinn M (2004) Endometriosis: the consequence of neurological dysfunction? Med Hypotheses 63:602–608PubMed
21.
go back to reference Chatman DL (1981) Pelvic peritoneal defects and endometriosis: Allen-Masters syndrome revisited. Fertil Steril 36:751–756PubMed Chatman DL (1981) Pelvic peritoneal defects and endometriosis: Allen-Masters syndrome revisited. Fertil Steril 36:751–756PubMed
22.
go back to reference Rier SE, Martin DC, Bowman RE, Dmowski WP, Becker JL (1993) Endometriosis in rhesus monkeys (Macaca mulatta) following chronic exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Fundam Appl Toxicol 21:433–441PubMed Rier SE, Martin DC, Bowman RE, Dmowski WP, Becker JL (1993) Endometriosis in rhesus monkeys (Macaca mulatta) following chronic exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Fundam Appl Toxicol 21:433–441PubMed
23.
go back to reference Moen MH, Magnus P (1993) The familial risk of endometriosis. Acta Obstet Gynecol Scand 72:560–564PubMed Moen MH, Magnus P (1993) The familial risk of endometriosis. Acta Obstet Gynecol Scand 72:560–564PubMed
24.
25.
go back to reference Kao LC, Germeyer A, Tulac S, Lobo S, Yang JP, Taylor RN, Osteen K, Lessey BA, Giudice LC (2003) Expression profiling of endometrium from women with endometriosis reveals candidate genes for disease-based implantation failure and infertility. Endocrinology 144:2870–2881PubMed Kao LC, Germeyer A, Tulac S, Lobo S, Yang JP, Taylor RN, Osteen K, Lessey BA, Giudice LC (2003) Expression profiling of endometrium from women with endometriosis reveals candidate genes for disease-based implantation failure and infertility. Endocrinology 144:2870–2881PubMed
26.
go back to reference Hu WP, Tay SK, Zhao Y (2006) Endometriosis-specific genes identified by real-time reverse transcription-polymerase chain reaction expression profiling of endometriosis versus autologous uterine endometrium. J Clin Endocrinol Metab 91:228–238PubMed Hu WP, Tay SK, Zhao Y (2006) Endometriosis-specific genes identified by real-time reverse transcription-polymerase chain reaction expression profiling of endometriosis versus autologous uterine endometrium. J Clin Endocrinol Metab 91:228–238PubMed
27.
go back to reference Haney AF, Muscato JJ, Weinberg JB (1981) Peritoneal fluid cell populations in infertility patients. Fertil Steril 35:696–698PubMed Haney AF, Muscato JJ, Weinberg JB (1981) Peritoneal fluid cell populations in infertility patients. Fertil Steril 35:696–698PubMed
28.
go back to reference D’Hooghe TM, Hill JA, Oosterlynck DJ, Koninckx PR, Bambra CS (1996) Effect of endometriosis on white blood cell subpopulations in peripheral blood and peritoneal fluid of baboons. Hum Reprod 11:1736–1740PubMed D’Hooghe TM, Hill JA, Oosterlynck DJ, Koninckx PR, Bambra CS (1996) Effect of endometriosis on white blood cell subpopulations in peripheral blood and peritoneal fluid of baboons. Hum Reprod 11:1736–1740PubMed
29.
go back to reference Sukhikh GT, Sotnikova NY, Antsiferova YS, Posiseeva LV, Veryasov VN, Van’ko LV (2004) Cytokine production by immunocompetent cells of peritoneal fluid in women with external genital endometriosis. Bull Exp Biol Med 137:568–571PubMed Sukhikh GT, Sotnikova NY, Antsiferova YS, Posiseeva LV, Veryasov VN, Van’ko LV (2004) Cytokine production by immunocompetent cells of peritoneal fluid in women with external genital endometriosis. Bull Exp Biol Med 137:568–571PubMed
30.
go back to reference Halme J, Becker S, Hammond MG, Raj MH, Raj S (1983) Increased activation of pelvic macrophages in infertile women with mild endometriosis. Am J Obstet Gynecol 145:333–337PubMed Halme J, Becker S, Hammond MG, Raj MH, Raj S (1983) Increased activation of pelvic macrophages in infertile women with mild endometriosis. Am J Obstet Gynecol 145:333–337PubMed
31.
go back to reference Fukaya T, Sugawara J, Yoshida H, Yajima A (1994) The role of macrophage colony stimulating factor in the peritoneal fluid in infertile patients with endometriosis. Tohoku J Exp Med 172:221–226PubMed Fukaya T, Sugawara J, Yoshida H, Yajima A (1994) The role of macrophage colony stimulating factor in the peritoneal fluid in infertile patients with endometriosis. Tohoku J Exp Med 172:221–226PubMed
32.
go back to reference Akoum A, Lemay A, McColl S, Turcot-Lemay L, Maheux R (1996) Elevated concentration and biologic activity of monocyte chemotactic protein-1 in the peritoneal fluid of patients with endometriosis. Fertil Steril 66:17–23PubMed Akoum A, Lemay A, McColl S, Turcot-Lemay L, Maheux R (1996) Elevated concentration and biologic activity of monocyte chemotactic protein-1 in the peritoneal fluid of patients with endometriosis. Fertil Steril 66:17–23PubMed
33.
go back to reference Keenan JA, Chen TT, Chadwell NL, Torry DS, Caudle MR (1994) Interferon-gamma (IFN-gamma) and interleukin-6 (IL-6) in peritoneal fluid and macrophage-conditioned media of women with endometriosis. Am J Reprod Immunol 32:180–183PubMed Keenan JA, Chen TT, Chadwell NL, Torry DS, Caudle MR (1994) Interferon-gamma (IFN-gamma) and interleukin-6 (IL-6) in peritoneal fluid and macrophage-conditioned media of women with endometriosis. Am J Reprod Immunol 32:180–183PubMed
34.
go back to reference Keenan JA, Chen TT, Chadwell NL, Torry DS, Caudle MR (1995) IL-1 beta, TNF-alpha, and IL-2 in peritoneal fluid and macrophage-conditioned media of women with endometriosis. Am J Reprod Immunol 34:381–385PubMed Keenan JA, Chen TT, Chadwell NL, Torry DS, Caudle MR (1995) IL-1 beta, TNF-alpha, and IL-2 in peritoneal fluid and macrophage-conditioned media of women with endometriosis. Am J Reprod Immunol 34:381–385PubMed
35.
go back to reference Beliard A, Noel A, Goffin F, Frankenne F, Foidart JM (2003) Adhesion of endometrial cells labeled with 111Indium-tropolonate to peritoneum: a novel in vitro model to study endometriosis. Fertil Steril 79(Suppl 1):724–729PubMed Beliard A, Noel A, Goffin F, Frankenne F, Foidart JM (2003) Adhesion of endometrial cells labeled with 111Indium-tropolonate to peritoneum: a novel in vitro model to study endometriosis. Fertil Steril 79(Suppl 1):724–729PubMed
36.
go back to reference Taketani Y, Kuo TM, Mizuno M (1992) Comparison of cytokine levels and embryo toxicity in peritoneal fluid in infertile women with untreated or treated endometriosis. Am J Obstet Gynecol 167:265–270PubMed Taketani Y, Kuo TM, Mizuno M (1992) Comparison of cytokine levels and embryo toxicity in peritoneal fluid in infertile women with untreated or treated endometriosis. Am J Obstet Gynecol 167:265–270PubMed
37.
go back to reference Gomez-Torres MJ, Acien P, Campos A, Velasco I (2002) Embryotoxicity of peritoneal fluid in women with endometriosis. Its relation with cytokines and lymphocyte populations. Hum Reprod 17:777–781PubMed Gomez-Torres MJ, Acien P, Campos A, Velasco I (2002) Embryotoxicity of peritoneal fluid in women with endometriosis. Its relation with cytokines and lymphocyte populations. Hum Reprod 17:777–781PubMed
38.
go back to reference Iwabe T, Harada T, Tsudo T, Nagano Y, Yoshida S, Tanikawa M, Terakawa N (2000) Tumor necrosis factor-alpha promotes proliferation of endometriotic stromal cells by inducing interleukin-8 gene and protein expression. J Clin Endocrinol Metab 85:824–829PubMed Iwabe T, Harada T, Tsudo T, Nagano Y, Yoshida S, Tanikawa M, Terakawa N (2000) Tumor necrosis factor-alpha promotes proliferation of endometriotic stromal cells by inducing interleukin-8 gene and protein expression. J Clin Endocrinol Metab 85:824–829PubMed
39.
go back to reference Rojas-Cartagena C, Appleyard CB, Santiago OI, Flores I (2005) Experimental intestinal endometriosis is characterized by increased levels of soluble TNFRSF1B and downregulation of Tnfrsf1a and Tnfrsf1b gene expression. Biol Reprod 73:1211–1218PubMed Rojas-Cartagena C, Appleyard CB, Santiago OI, Flores I (2005) Experimental intestinal endometriosis is characterized by increased levels of soluble TNFRSF1B and downregulation of Tnfrsf1a and Tnfrsf1b gene expression. Biol Reprod 73:1211–1218PubMed
40.
go back to reference Morita M, Yano Y, Otaka K, Kojima E, Momose K (1990) Minimal and mild endometriosis. Nd:YAG laser treatment and changes in prostaglandin concentrations in peritoneal fluid. J Reprod Med 35:621–624PubMed Morita M, Yano Y, Otaka K, Kojima E, Momose K (1990) Minimal and mild endometriosis. Nd:YAG laser treatment and changes in prostaglandin concentrations in peritoneal fluid. J Reprod Med 35:621–624PubMed
41.
go back to reference Golan A, Dargenio R, Winston RM (1986) The effect of treatment on experimentally produced endometrial peritoneal implants. Fertil Steril 46:954–958PubMed Golan A, Dargenio R, Winston RM (1986) The effect of treatment on experimentally produced endometrial peritoneal implants. Fertil Steril 46:954–958PubMed
42.
go back to reference Kusume T, Maeda N, Izumiya C, Yamamoto Y, Hayashi K, Oguri H, Nishimori Y, Fukaya T (2005) Human leukocyte antigen expression by peritoneal macrophages from women with pelvic endometriosis is depressed but coordinated with costimulatory molecule expression. Fertil Steril 83(Suppl 1):1232–1240PubMed Kusume T, Maeda N, Izumiya C, Yamamoto Y, Hayashi K, Oguri H, Nishimori Y, Fukaya T (2005) Human leukocyte antigen expression by peritoneal macrophages from women with pelvic endometriosis is depressed but coordinated with costimulatory molecule expression. Fertil Steril 83(Suppl 1):1232–1240PubMed
43.
go back to reference Braun DP, Gebel H, Rotman C, Rana N, Dmowski WP (1992) The development of cytotoxicity in peritoneal macrophages from women with endometriosis. Fertil Steril 57:1203–1210PubMed Braun DP, Gebel H, Rotman C, Rana N, Dmowski WP (1992) The development of cytotoxicity in peritoneal macrophages from women with endometriosis. Fertil Steril 57:1203–1210PubMed
44.
go back to reference Kempuraj D, Papadopoulou N, Stanford EJ, Christodoulou S, Madhappan B, Sant GR, Solage K, Adams T, Theoharides TC (2004) Increased numbers of activated mast cells in endometriosis lesions positive for corticotropin-releasing hormone and urocortin. Am J Reprod Immunol 52:267–275PubMed Kempuraj D, Papadopoulou N, Stanford EJ, Christodoulou S, Madhappan B, Sant GR, Solage K, Adams T, Theoharides TC (2004) Increased numbers of activated mast cells in endometriosis lesions positive for corticotropin-releasing hormone and urocortin. Am J Reprod Immunol 52:267–275PubMed
45.
go back to reference Osuga Y, Koga K, Tsutsumi O, Igarashi T, Okagaki R, Takai Y, Matsumi H, Hiroi H, Fujiwara T, Momoeda M, Yano T, Taketani Y (2000) Stem cell factor (SCF) concentrations in peritoneal fluid of women with or without endometriosis. Am J Reprod Immunol 44:231–235PubMed Osuga Y, Koga K, Tsutsumi O, Igarashi T, Okagaki R, Takai Y, Matsumi H, Hiroi H, Fujiwara T, Momoeda M, Yano T, Taketani Y (2000) Stem cell factor (SCF) concentrations in peritoneal fluid of women with or without endometriosis. Am J Reprod Immunol 44:231–235PubMed
46.
go back to reference Vliagoftis H, Worobec AS, Metcalfe DD (1997) The protooncogene c-kit and c-kit ligand in human disease. J Allergy Clin Immunol 100:435–440PubMed Vliagoftis H, Worobec AS, Metcalfe DD (1997) The protooncogene c-kit and c-kit ligand in human disease. J Allergy Clin Immunol 100:435–440PubMed
47.
go back to reference Hirota Y, Osuga Y, Hirata T, Harada M, Morimoto C, Yoshino O, Koga K, Yano T, Tsutsumi O, Taketani Y (2005) Activation of protease-activated receptor 2 stimulates proliferation and interleukin (IL)-6 and IL-8 secretion of endometriotic stromal cells. Hum Reprod 20:3547–3553PubMed Hirota Y, Osuga Y, Hirata T, Harada M, Morimoto C, Yoshino O, Koga K, Yano T, Tsutsumi O, Taketani Y (2005) Activation of protease-activated receptor 2 stimulates proliferation and interleukin (IL)-6 and IL-8 secretion of endometriotic stromal cells. Hum Reprod 20:3547–3553PubMed
48.
go back to reference Anaf V, Chapron C, El Nakadi I, De Moor V, Simonart T, Noel JC (2006) Pain, mast cells, and nerves in peritoneal, ovarian, and deep infiltrating endometriosis. Fertil Steril 86:1336–1343PubMed Anaf V, Chapron C, El Nakadi I, De Moor V, Simonart T, Noel JC (2006) Pain, mast cells, and nerves in peritoneal, ovarian, and deep infiltrating endometriosis. Fertil Steril 86:1336–1343PubMed
49.
go back to reference Oosterlynck DJ, Cornillie FJ, Waer M, Vandeputte M, Koninckx PR (1991) Women with endometriosis show a defect in natural killer activity resulting in a decreased cytotoxicity to autologous endometrium. Fertil Steril 56:45–51PubMed Oosterlynck DJ, Cornillie FJ, Waer M, Vandeputte M, Koninckx PR (1991) Women with endometriosis show a defect in natural killer activity resulting in a decreased cytotoxicity to autologous endometrium. Fertil Steril 56:45–51PubMed
50.
go back to reference Oosterlynck DJ, Meuleman C, Waer M, Vandeputte M, Koninckx PR (1992) The natural killer activity of peritoneal fluid lymphocytes is decreased in women with endometriosis. Fertil Steril 58:290–295PubMed Oosterlynck DJ, Meuleman C, Waer M, Vandeputte M, Koninckx PR (1992) The natural killer activity of peritoneal fluid lymphocytes is decreased in women with endometriosis. Fertil Steril 58:290–295PubMed
51.
go back to reference Iwasaki K, Makino T, Maruyama T, Matsubayashi H, Nozawa S, Yokokura T (1993) Leukocyte subpopulations and natural killer activity in endometriosis. Int J Fertil Menopausal Stud 38:229–234PubMed Iwasaki K, Makino T, Maruyama T, Matsubayashi H, Nozawa S, Yokokura T (1993) Leukocyte subpopulations and natural killer activity in endometriosis. Int J Fertil Menopausal Stud 38:229–234PubMed
52.
go back to reference Oosterlynck DJ, Meuleman C, Waer M, Koninckx PR (1994) Transforming growth factor-beta activity is increased in peritoneal fluid from women with endometriosis. Obstet Gynecol 83:287–292PubMed Oosterlynck DJ, Meuleman C, Waer M, Koninckx PR (1994) Transforming growth factor-beta activity is increased in peritoneal fluid from women with endometriosis. Obstet Gynecol 83:287–292PubMed
53.
go back to reference Wu MY, Yang JH, Chao KH, Hwang JL, Yang YS, Ho HN (2000) Increase in the expression of killer cell inhibitory receptors on peritoneal natural killer cells in women with endometriosis. Fertil Steril 74:1187–1191PubMed Wu MY, Yang JH, Chao KH, Hwang JL, Yang YS, Ho HN (2000) Increase in the expression of killer cell inhibitory receptors on peritoneal natural killer cells in women with endometriosis. Fertil Steril 74:1187–1191PubMed
54.
go back to reference Arimoto T, Katagiri T, Oda K, Tsunoda T, Yasugi T, Osuga Y, Yoshikawa H, Nishii O, Yano T, Taketani Y, Nakamura Y (2003) Genome-wide cDNA microarray analysis of gene-expression profiles involved in ovarian endometriosis. Int J Oncol 22:551–560PubMed Arimoto T, Katagiri T, Oda K, Tsunoda T, Yasugi T, Osuga Y, Yoshikawa H, Nishii O, Yano T, Taketani Y, Nakamura Y (2003) Genome-wide cDNA microarray analysis of gene-expression profiles involved in ovarian endometriosis. Int J Oncol 22:551–560PubMed
55.
go back to reference Witz CA, Montoya IA, Dey TD, Schenken RS (1994) Characterization of lymphocyte subpopulations and T cell activation in endometriosis. Am J Reprod Immunol 32:173–179PubMed Witz CA, Montoya IA, Dey TD, Schenken RS (1994) Characterization of lymphocyte subpopulations and T cell activation in endometriosis. Am J Reprod Immunol 32:173–179PubMed
56.
go back to reference Jones RK, Bulmer JN, Searle RF (1996) Immunohistochemical characterization of stromal leukocytes in ovarian endometriosis: comparison of eutopic and ectopic endometrium with normal endometrium. Fertil Steril 66:81–89PubMed Jones RK, Bulmer JN, Searle RF (1996) Immunohistochemical characterization of stromal leukocytes in ovarian endometriosis: comparison of eutopic and ectopic endometrium with normal endometrium. Fertil Steril 66:81–89PubMed
57.
go back to reference Akoum A, Lemay A, Maheux R (2002) 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 87:5785–5792PubMed Akoum A, Lemay A, Maheux R (2002) 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 87:5785–5792PubMed
58.
go back to reference Khorram O, Taylor RN, Ryan IP, Schall TJ, Landers DV (1993) Peritoneal fluid concentrations of the cytokine RANTES correlate with the severity of endometriosis. Am J Obstet Gynecol 169:1545–1549PubMed Khorram O, Taylor RN, Ryan IP, Schall TJ, Landers DV (1993) Peritoneal fluid concentrations of the cytokine RANTES correlate with the severity of endometriosis. Am J Obstet Gynecol 169:1545–1549PubMed
59.
go back to reference Sakaguchi S, Sakaguchi N, Asano M, Itoh M, Toda M (1995) Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor alpha-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J Immunol 155:1151–1164PubMed Sakaguchi S, Sakaguchi N, Asano M, Itoh M, Toda M (1995) Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor alpha-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J Immunol 155:1151–1164PubMed
60.
go back to reference Szyllo K, Tchorzewski H, Banasik M, Glowacka E, Lewkowicz P, Kamer-Bartosinska A (2003) The involvement of T lymphocytes in the pathogenesis of endometriotic tissues overgrowth in women with endometriosis. Mediators Inflamm 12:131–138PubMed Szyllo K, Tchorzewski H, Banasik M, Glowacka E, Lewkowicz P, Kamer-Bartosinska A (2003) The involvement of T lymphocytes in the pathogenesis of endometriotic tissues overgrowth in women with endometriosis. Mediators Inflamm 12:131–138PubMed
61.
go back to reference Podgaec S, Abrao MS, Dias JA Jr, Rizzo LV, de Oliveira RM, Baracat EC (2007) Endometriosis: an inflammatory disease with a Th2 immune response component. Hum Reprod 22(5):1373–1379PubMed Podgaec S, Abrao MS, Dias JA Jr, Rizzo LV, de Oliveira RM, Baracat EC (2007) Endometriosis: an inflammatory disease with a Th2 immune response component. Hum Reprod 22(5):1373–1379PubMed
62.
go back to reference Zenclussen AC, Joachim R, Hagen E, Peiser C, Klapp BF, Arck PC (2002) Heme oxygenase is downregulated in stress-triggered and interleukin-12-mediated murine abortion. Scand J Immunol 55:560–569PubMed Zenclussen AC, Joachim R, Hagen E, Peiser C, Klapp BF, Arck PC (2002) Heme oxygenase is downregulated in stress-triggered and interleukin-12-mediated murine abortion. Scand J Immunol 55:560–569PubMed
63.
go back to reference Van Langendonckt A, Casanas-Roux F, Dolmans MM, Donnez J (2002) Potential involvement of hemoglobin and heme in the pathogenesis of peritoneal endometriosis. Fertil Steril 77:561–570PubMed Van Langendonckt A, Casanas-Roux F, Dolmans MM, Donnez J (2002) Potential involvement of hemoglobin and heme in the pathogenesis of peritoneal endometriosis. Fertil Steril 77:561–570PubMed
64.
go back to reference Szczepanska M, Kozlik J, Skrzypczak J, Mikolajczyk M (2003) Oxidative stress may be a piece in the endometriosis puzzle. Fertil Steril 79:1288–1293PubMed Szczepanska M, Kozlik J, Skrzypczak J, Mikolajczyk M (2003) Oxidative stress may be a piece in the endometriosis puzzle. Fertil Steril 79:1288–1293PubMed
65.
go back to reference D’Antonio M, Martelli F, Peano S, Papoian R, Borrelli F (2000) Ability of recombinant human TNF binding protein-1 (r-hTBP-1) to inhibit the development of experimentally-induced endometriosis in rats. J Reprod Immunol 48:81–98PubMed D’Antonio M, Martelli F, Peano S, Papoian R, Borrelli F (2000) Ability of recombinant human TNF binding protein-1 (r-hTBP-1) to inhibit the development of experimentally-induced endometriosis in rats. J Reprod Immunol 48:81–98PubMed
66.
go back to reference Somigliana E, Vigano P, Rossi G, Carinelli S, Vignali M, Panina-Bordignon P (1999) Endometrial ability to implant in ectopic sites can be prevented by interleukin-12 in a murine model of endometriosis. Hum Reprod 14:2944–2950PubMed Somigliana E, Vigano P, Rossi G, Carinelli S, Vignali M, Panina-Bordignon P (1999) Endometrial ability to implant in ectopic sites can be prevented by interleukin-12 in a murine model of endometriosis. Hum Reprod 14:2944–2950PubMed
67.
go back to reference Antsiferova YS, Sotnikova NY, Posiseeva LV, Shor AL (2005) Changes in the T-helper cytokine profile and in lymphocyte activation at the systemic and local levels in women with endometriosis. Fertil Steril 84:1705–1711PubMed Antsiferova YS, Sotnikova NY, Posiseeva LV, Shor AL (2005) Changes in the T-helper cytokine profile and in lymphocyte activation at the systemic and local levels in women with endometriosis. Fertil Steril 84:1705–1711PubMed
68.
go back to reference Odukoya OA, Bansal A, Wilson P, Lim K, Weetman AP, Cooke ID (1996) Soluble CD23 protein in the peritoneal fluid of patients with endometriosis. Hum Reprod 11:2018–2021PubMed Odukoya OA, Bansal A, Wilson P, Lim K, Weetman AP, Cooke ID (1996) Soluble CD23 protein in the peritoneal fluid of patients with endometriosis. Hum Reprod 11:2018–2021PubMed
69.
go back to reference Confino E, Harlow L, Gleicher N (1990) Peritoneal fluid and serum autoantibody levels in patients with endometriosis. Fertil Steril 53:242–245PubMed Confino E, Harlow L, Gleicher N (1990) Peritoneal fluid and serum autoantibody levels in patients with endometriosis. Fertil Steril 53:242–245PubMed
70.
go back to reference Mathur S, Peress MR, Williamson HO, Youmans CD, Maney SA, Garvin AJ, Rust PF, Fudenberg HH (1982) Autoimmunity to endometrium and ovary in endometriosis. Clin Exp Immunol 50:259–266PubMed Mathur S, Peress MR, Williamson HO, Youmans CD, Maney SA, Garvin AJ, Rust PF, Fudenberg HH (1982) Autoimmunity to endometrium and ovary in endometriosis. Clin Exp Immunol 50:259–266PubMed
71.
go back to reference Moncayo H, Moncayo R, Benz R, Wolf A, Lauritzen C (1989) Ovarian failure and autoimmunity. Detection of autoantibodies directed against both the unoccupied luteinizing hormone/human chorionic gonadotropin receptor and the hormone–receptor complex of bovine corpus luteum. J Clin Invest 84:1857–1865PubMed Moncayo H, Moncayo R, Benz R, Wolf A, Lauritzen C (1989) Ovarian failure and autoimmunity. Detection of autoantibodies directed against both the unoccupied luteinizing hormone/human chorionic gonadotropin receptor and the hormone–receptor complex of bovine corpus luteum. J Clin Invest 84:1857–1865PubMed
72.
go back to reference D’Cruz OJ, Wild RA, Haas GG Jr, Reichlin M (1996) Antibodies to carbonic anhydrase in endometriosis: prevalence, specificity, and relationship to clinical and laboratory parameters. Fertil Steril 66:547–556PubMed D’Cruz OJ, Wild RA, Haas GG Jr, Reichlin M (1996) Antibodies to carbonic anhydrase in endometriosis: prevalence, specificity, and relationship to clinical and laboratory parameters. Fertil Steril 66:547–556PubMed
73.
go back to reference Lang GA, Yeaman GR (2001) Autoantibodies in endometriosis sera recognize a Thomsen–Friedenreich-like carbohydrate antigen. J Autoimmun 16:151–161PubMed Lang GA, Yeaman GR (2001) Autoantibodies in endometriosis sera recognize a Thomsen–Friedenreich-like carbohydrate antigen. J Autoimmun 16:151–161PubMed
74.
go back to reference Mathur SP, Holt VL, Lee JH, Jiang H, Rust PF (1998) Levels of antibodies to transferrin and alpha 2-HS glycoprotein in women with and without endometriosis. Am J Reprod Immunol 40:69–73PubMed Mathur SP, Holt VL, Lee JH, Jiang H, Rust PF (1998) Levels of antibodies to transferrin and alpha 2-HS glycoprotein in women with and without endometriosis. Am J Reprod Immunol 40:69–73PubMed
75.
go back to reference Liu FT, Rabinovich GA (2005) Galectins as modulators of tumour progression. Nat Rev Cancer 5:29–41PubMed Liu FT, Rabinovich GA (2005) Galectins as modulators of tumour progression. Nat Rev Cancer 5:29–41PubMed
76.
go back to reference Rubinstein N, Alvarez M, Zwirner NW, Toscano MA, Ilarregui JM, Bravo A, Mordoh J, Fainboim L, Podhajcer OL, Rabinovich GA (2004) Targeted inhibition of galectin-1 gene expression in tumor cells results in heightened T cell-mediated rejection; a potential mechanism of tumor-immune privilege. Cancer Cell 5:241–251PubMed Rubinstein N, Alvarez M, Zwirner NW, Toscano MA, Ilarregui JM, Bravo A, Mordoh J, Fainboim L, Podhajcer OL, Rabinovich GA (2004) Targeted inhibition of galectin-1 gene expression in tumor cells results in heightened T cell-mediated rejection; a potential mechanism of tumor-immune privilege. Cancer Cell 5:241–251PubMed
77.
go back to reference Vigano P, Gaffuri B, Somigliana E, Busacca M, Di Blasio AM, Vignali M (1998) Expression of intercellular adhesion molecule (ICAM)-1 mRNA and protein is enhanced in endometriosis versus endometrial stromal cells in culture. Mol Hum Reprod 4:1150–1156PubMed Vigano P, Gaffuri B, Somigliana E, Busacca M, Di Blasio AM, Vignali M (1998) Expression of intercellular adhesion molecule (ICAM)-1 mRNA and protein is enhanced in endometriosis versus endometrial stromal cells in culture. Mol Hum Reprod 4:1150–1156PubMed
78.
go back to reference Fukaya T, Sugawara J, Yoshida H, Murakami T, Yajima A (1999) Intercellular adhesion molecule-1 and hepatocyte growth factor in human endometriosis: original investigation and a review of literature. Gynecol Obstet Invest 47(Suppl 1):11–16 (discussion 16–17)PubMed Fukaya T, Sugawara J, Yoshida H, Murakami T, Yajima A (1999) Intercellular adhesion molecule-1 and hepatocyte growth factor in human endometriosis: original investigation and a review of literature. Gynecol Obstet Invest 47(Suppl 1):11–16 (discussion 16–17)PubMed
79.
go back to reference Piva M, Sharpe-Timms KL (1999) Peritoneal endometriotic lesions differentially express a haptoglobin-like gene. Mol Hum Reprod 5:71–78PubMed Piva M, Sharpe-Timms KL (1999) Peritoneal endometriotic lesions differentially express a haptoglobin-like gene. Mol Hum Reprod 5:71–78PubMed
80.
go back to reference Piva M, Moreno JI, Sharpe-Timms KL (2002) Glycosylation and over-expression of endometriosis-associated peritoneal haptoglobin. Glycoconj J 19:33–41PubMed Piva M, Moreno JI, Sharpe-Timms KL (2002) Glycosylation and over-expression of endometriosis-associated peritoneal haptoglobin. Glycoconj J 19:33–41PubMed
81.
go back to reference Daniel Y, Geva E, Amit A, Eshed-Englender T, Baram A, Fait G, Lessing JB (2000) Do soluble cell adhesion molecules play a role in endometriosis? Am J Reprod Immunol 43:160–166PubMed Daniel Y, Geva E, Amit A, Eshed-Englender T, Baram A, Fait G, Lessing JB (2000) Do soluble cell adhesion molecules play a role in endometriosis? Am J Reprod Immunol 43:160–166PubMed
82.
go back to reference Schmidt M, Regidor PA, Engel K, Regidor M, Winterhager E, Scotti S, Schindler AE (2000) E- and P-selectin expression in endometriotic tissues and the corresponding endometria. Gynecol Endocrinol 14:111–117PubMedCrossRef Schmidt M, Regidor PA, Engel K, Regidor M, Winterhager E, Scotti S, Schindler AE (2000) E- and P-selectin expression in endometriotic tissues and the corresponding endometria. Gynecol Endocrinol 14:111–117PubMedCrossRef
83.
go back to reference Sharpe-Timms KL, Zimmer RL, Ricke EA, Piva M, Horowitz GM (2002) Endometriotic haptoglobin binds to peritoneal macrophages and alters their function in women with endometriosis. Fertil Steril 78:810–819PubMed Sharpe-Timms KL, Zimmer RL, Ricke EA, Piva M, Horowitz GM (2002) Endometriotic haptoglobin binds to peritoneal macrophages and alters their function in women with endometriosis. Fertil Steril 78:810–819PubMed
84.
go back to reference Stahn R, Goletz S, Stahn R, Wilmanowski R, Wang X, Briese V, Friese K, Jeschke U (2005) Human chorionic gonadotropin (hCG) as inhibitior of E-selectin-mediated cell adhesion. Anticancer Res 25:1811–1816PubMed Stahn R, Goletz S, Stahn R, Wilmanowski R, Wang X, Briese V, Friese K, Jeschke U (2005) Human chorionic gonadotropin (hCG) as inhibitior of E-selectin-mediated cell adhesion. Anticancer Res 25:1811–1816PubMed
85.
go back to reference Jeschke U, Wang X, Briese V, Friese K, Stahn R (2003) Glycodelin and amniotic fluid transferrin as inhibitors of E-selectin-mediated cell adhesion. Histochem Cell Biol 119:345–354PubMed Jeschke U, Wang X, Briese V, Friese K, Stahn R (2003) Glycodelin and amniotic fluid transferrin as inhibitors of E-selectin-mediated cell adhesion. Histochem Cell Biol 119:345–354PubMed
86.
go back to reference Jones CJ, Denton J, Fazleabas AT (2006) Morphological and glycosylation changes associated with the endometrium and ectopic lesions in a baboon model of endometriosis. Hum Reprod 21:3068–3080PubMed Jones CJ, Denton J, Fazleabas AT (2006) Morphological and glycosylation changes associated with the endometrium and ectopic lesions in a baboon model of endometriosis. Hum Reprod 21:3068–3080PubMed
87.
go back to reference Aplin JD, Meseguer M, Simon C, Ortiz ME, Croxatto H, Jones CJ (2001) MUC1, glycans and the cell-surface barrier to embryo implantation. Biochem Soc Trans 29:153–156PubMed Aplin JD, Meseguer M, Simon C, Ortiz ME, Croxatto H, Jones CJ (2001) MUC1, glycans and the cell-surface barrier to embryo implantation. Biochem Soc Trans 29:153–156PubMed
88.
go back to reference Aplin JD (1997) Adhesion molecules in implantation. Rev Reprod 2:84–93PubMed Aplin JD (1997) Adhesion molecules in implantation. Rev Reprod 2:84–93PubMed
89.
go back to reference Bourlev V, Volkov N, Pavlovitch S, Lets N, Larsson A, Olovsson M (2006) The relationship between microvessel density, proliferative activity and expression of vascular endothelial growth factor-A and its receptors in eutopic endometrium and endometriotic lesions. Reproduction 132:501–509PubMed Bourlev V, Volkov N, Pavlovitch S, Lets N, Larsson A, Olovsson M (2006) The relationship between microvessel density, proliferative activity and expression of vascular endothelial growth factor-A and its receptors in eutopic endometrium and endometriotic lesions. Reproduction 132:501–509PubMed
90.
go back to reference Laschke MW, Elitzsch A, Scheuer C, Holstein JH, Vollmar B, Menger MD (2006) Rapamycin induces regression of endometriotic lesions by inhibiting neovascularization and cell proliferation. Br J Pharmacol 149:137–144PubMed Laschke MW, Elitzsch A, Scheuer C, Holstein JH, Vollmar B, Menger MD (2006) Rapamycin induces regression of endometriotic lesions by inhibiting neovascularization and cell proliferation. Br J Pharmacol 149:137–144PubMed
91.
go back to reference Lin YJ, Lai MD, Lei HY, Wing LY (2006) Neutrophils and macrophages promote angiogenesis in the early stage of endometriosis in a mouse model. Endocrinology 147:1278–1286PubMed Lin YJ, Lai MD, Lei HY, Wing LY (2006) Neutrophils and macrophages promote angiogenesis in the early stage of endometriosis in a mouse model. Endocrinology 147:1278–1286PubMed
92.
go back to reference Jeon SH, Chae BC, Kim HA, Seo GY, Seo DW, Chun GT, Kim NS, Yie SW, Byeon WH, Eom SH, Ha KS, Kim YM, Kim PH (2007) Mechanisms underlying TGF-{beta}1-induced expression of VEGF and Flk-1 in mouse macrophages and their implications for angiogenesis. J Leukoc Biol 81:557–566PubMed Jeon SH, Chae BC, Kim HA, Seo GY, Seo DW, Chun GT, Kim NS, Yie SW, Byeon WH, Eom SH, Ha KS, Kim YM, Kim PH (2007) Mechanisms underlying TGF-{beta}1-induced expression of VEGF and Flk-1 in mouse macrophages and their implications for angiogenesis. J Leukoc Biol 81:557–566PubMed
93.
go back to reference Sokolov DI, Solodovnikova NG, Pavlov OV, Niauri DA, Volkov NN, Sel’kov SA (2005) Study of cytokine profile and angiogenic potential of peritoneal fluid in patients with external genital endometriosis. Bull Exp Biol Med 140:541–544PubMed Sokolov DI, Solodovnikova NG, Pavlov OV, Niauri DA, Volkov NN, Sel’kov SA (2005) Study of cytokine profile and angiogenic potential of peritoneal fluid in patients with external genital endometriosis. Bull Exp Biol Med 140:541–544PubMed
94.
go back to reference Ryan IP, Tseng JF, Schriock ED, Khorram O, Landers DV, Taylor RN (1995) Interleukin-8 concentrations are elevated in peritoneal fluid of women with endometriosis. Fertil Steril 63:929–932PubMed Ryan IP, Tseng JF, Schriock ED, Khorram O, Landers DV, Taylor RN (1995) Interleukin-8 concentrations are elevated in peritoneal fluid of women with endometriosis. Fertil Steril 63:929–932PubMed
95.
go back to reference Li A, Dubey S, Varney ML, Dave BJ, Singh RK (2003) IL-8 directly enhanced endothelial cell survival, proliferation, and matrix metalloproteinases production and regulated angiogenesis. J Immunol 170:3369–3376PubMed Li A, Dubey S, Varney ML, Dave BJ, Singh RK (2003) IL-8 directly enhanced endothelial cell survival, proliferation, and matrix metalloproteinases production and regulated angiogenesis. J Immunol 170:3369–3376PubMed
96.
go back to reference Hudelist G, Lass H, Keckstein J, Walter I, Wieser F, Wenzl R, Mueller R, Czerwenka K, Kubista E, Singer CF (2005) Interleukin 1alpha and tissue-lytic matrix metalloproteinase-1 are elevated in ectopic endometrium of patients with endometriosis. Hum Reprod 20:1695–1701PubMed Hudelist G, Lass H, Keckstein J, Walter I, Wieser F, Wenzl R, Mueller R, Czerwenka K, Kubista E, Singer CF (2005) Interleukin 1alpha and tissue-lytic matrix metalloproteinase-1 are elevated in ectopic endometrium of patients with endometriosis. Hum Reprod 20:1695–1701PubMed
97.
go back to reference Huang HF, Hong LH, Tan Y, Sheng JZ (2004) Matrix metalloproteinase 2 is associated with changes in steroid hormones in the sera and peritoneal fluid of patients with endometriosis. Fertil Steril 81:1235–1239PubMed Huang HF, Hong LH, Tan Y, Sheng JZ (2004) Matrix metalloproteinase 2 is associated with changes in steroid hormones in the sera and peritoneal fluid of patients with endometriosis. Fertil Steril 81:1235–1239PubMed
98.
go back to reference Chung HW, Lee JY, Moon HS, Hur SE, Park MH, Wen Y, Polan ML (2002) Matrix metalloproteinase-2, membranous type 1 matrix metalloproteinase, and tissue inhibitor of metalloproteinase-2 expression in ectopic and eutopic endometrium. Fertil Steril 78:787–795PubMed Chung HW, Lee JY, Moon HS, Hur SE, Park MH, Wen Y, Polan ML (2002) Matrix metalloproteinase-2, membranous type 1 matrix metalloproteinase, and tissue inhibitor of metalloproteinase-2 expression in ectopic and eutopic endometrium. Fertil Steril 78:787–795PubMed
99.
go back to reference Cramer DW, Wilson E, Stillman RJ, Berger MJ, Belisle S, Schiff I, Albrecht B, Gibson M, Stadel BV, Schoenbaum SC (1986) The relation of endometriosis to menstrual characteristics, smoking, and exercise. JAMA 255:1904–1908PubMed Cramer DW, Wilson E, Stillman RJ, Berger MJ, Belisle S, Schiff I, Albrecht B, Gibson M, Stadel BV, Schoenbaum SC (1986) The relation of endometriosis to menstrual characteristics, smoking, and exercise. JAMA 255:1904–1908PubMed
100.
go back to reference Fujishita A, Nakane PK, Koji T, Masuzaki H, Chavez RO, Yamabe T, Ishimaru T (1997) Expression of estrogen and progesterone receptors in endometrium and peritoneal endometriosis: an immunohistochemical and in situ hybridization study. Fertil Steril 67:856–864PubMed Fujishita A, Nakane PK, Koji T, Masuzaki H, Chavez RO, Yamabe T, Ishimaru T (1997) Expression of estrogen and progesterone receptors in endometrium and peritoneal endometriosis: an immunohistochemical and in situ hybridization study. Fertil Steril 67:856–864PubMed
101.
go back to reference Wieser F, Schneeberger C, Tong D, Tempfer C, Huber JC, Wenzl R (2002) PROGINS receptor gene polymorphism is associated with endometriosis. Fertil Steril 77:309–312PubMed Wieser F, Schneeberger C, Tong D, Tempfer C, Huber JC, Wenzl R (2002) PROGINS receptor gene polymorphism is associated with endometriosis. Fertil Steril 77:309–312PubMed
102.
go back to reference Attia GR, Zeitoun K, Edwards D, Johns A, Carr BR, Bulun SE (2000) Progesterone receptor isoform A but not B is expressed in endometriosis. J Clin Endocrinol Metab 85:2897–2902PubMed Attia GR, Zeitoun K, Edwards D, Johns A, Carr BR, Bulun SE (2000) Progesterone receptor isoform A but not B is expressed in endometriosis. J Clin Endocrinol Metab 85:2897–2902PubMed
103.
go back to reference Casey ML, MacDonald PC, Andersson S (1994) 17 beta-hydroxysteroid dehydrogenase type 2: chromosomal assignment and progestin regulation of gene expression in human endometrium. J Clin Invest 94:2135–2141PubMedCrossRef Casey ML, MacDonald PC, Andersson S (1994) 17 beta-hydroxysteroid dehydrogenase type 2: chromosomal assignment and progestin regulation of gene expression in human endometrium. J Clin Invest 94:2135–2141PubMedCrossRef
104.
go back to reference Zeitoun K, Takayama K, Sasano H, Suzuki T, Moghrabi N, Andersson S, Johns A, Meng L, Putman M, Carr B, Bulun SE (1998) Deficient 17beta-hydroxysteroid dehydrogenase type 2 expression in endometriosis: failure to metabolize 17beta-estradiol. J Clin Endocrinol Metab 83:4474–4480PubMed Zeitoun K, Takayama K, Sasano H, Suzuki T, Moghrabi N, Andersson S, Johns A, Meng L, Putman M, Carr B, Bulun SE (1998) Deficient 17beta-hydroxysteroid dehydrogenase type 2 expression in endometriosis: failure to metabolize 17beta-estradiol. J Clin Endocrinol Metab 83:4474–4480PubMed
105.
go back to reference Fazleabas AT, Brudney A, Chai D, Langoi D, Bulun SE (2003) Steroid receptor and aromatase expression in baboon endometriotic lesions. Fertil Steril 80(Suppl 2):820–827PubMed Fazleabas AT, Brudney A, Chai D, Langoi D, Bulun SE (2003) Steroid receptor and aromatase expression in baboon endometriotic lesions. Fertil Steril 80(Suppl 2):820–827PubMed
106.
go back to reference Fang Z, Yang S, Gurates B, Tamura M, Simpson E, Evans D, Bulun SE (2002) Genetic or enzymatic disruption of aromatase inhibits the growth of ectopic uterine tissue. J Clin Endocrinol Metab 87:3460–3466PubMed Fang Z, Yang S, Gurates B, Tamura M, Simpson E, Evans D, Bulun SE (2002) Genetic or enzymatic disruption of aromatase inhibits the growth of ectopic uterine tissue. J Clin Endocrinol Metab 87:3460–3466PubMed
107.
go back to reference Sakamoto Y, Harada T, Horie S, Iba Y, Taniguchi F, Yoshida S, Iwabe T, Terakawa N (2003) Tumor necrosis factor-alpha-induced interleukin-8 (IL-8) expression in endometriotic stromal cells, probably through nuclear factor-kappa B activation: gonadotropin-releasing hormone agonist treatment reduced IL-8 expression. J Clin Endocrinol Metab 88:730–735PubMed Sakamoto Y, Harada T, Horie S, Iba Y, Taniguchi F, Yoshida S, Iwabe T, Terakawa N (2003) Tumor necrosis factor-alpha-induced interleukin-8 (IL-8) expression in endometriotic stromal cells, probably through nuclear factor-kappa B activation: gonadotropin-releasing hormone agonist treatment reduced IL-8 expression. J Clin Endocrinol Metab 88:730–735PubMed
108.
go back to reference Vliagoftis H, Dimitriadou V, Boucher W, Rozniecki JJ, Correia I, Raam S, Theoharides TC (1992) Estradiol augments while tamoxifen inhibits rat mast cell secretion. Int Arch Allergy Immunol 98:398–409PubMedCrossRef Vliagoftis H, Dimitriadou V, Boucher W, Rozniecki JJ, Correia I, Raam S, Theoharides TC (1992) Estradiol augments while tamoxifen inhibits rat mast cell secretion. Int Arch Allergy Immunol 98:398–409PubMedCrossRef
109.
go back to reference McLaren J, Prentice A, Charnock-Jones DS, Millican SA, Muller KH, Sharkey AM, Smith SK (1996) Vascular endothelial growth factor is produced by peritoneal fluid macrophages in endometriosis and is regulated by ovarian steroids. J Clin Invest 98:482–489PubMed McLaren J, Prentice A, Charnock-Jones DS, Millican SA, Muller KH, Sharkey AM, Smith SK (1996) Vascular endothelial growth factor is produced by peritoneal fluid macrophages in endometriosis and is regulated by ovarian steroids. J Clin Invest 98:482–489PubMed
110.
go back to reference Joachim R, Zenclussen AC, Polgar B, Douglas AJ, Fest S, Knackstedt M, Klapp BF, Arck PC (2003) The progesterone derivative dydrogesterone abrogates murine stress-triggered abortion by inducing a Th2 biased local immune response. Steroids 68:931–940PubMed Joachim R, Zenclussen AC, Polgar B, Douglas AJ, Fest S, Knackstedt M, Klapp BF, Arck PC (2003) The progesterone derivative dydrogesterone abrogates murine stress-triggered abortion by inducing a Th2 biased local immune response. Steroids 68:931–940PubMed
111.
go back to reference Blois SM, Joachim R, Kandil J, Margni R, Tometten M, Klapp BF, Arck PC (2004) Depletion of CD8+ cells abolishes the pregnancy protective effect of progesterone substitution with dydrogesterone in mice by altering the Th1/Th2 cytokine profile. J Immunol 172:5893–5899PubMed Blois SM, Joachim R, Kandil J, Margni R, Tometten M, Klapp BF, Arck PC (2004) Depletion of CD8+ cells abolishes the pregnancy protective effect of progesterone substitution with dydrogesterone in mice by altering the Th1/Th2 cytokine profile. J Immunol 172:5893–5899PubMed
112.
go back to reference Orsal AS, Blois S, Labuz D, Peters EM, Schaefer M, Arck PC (2006) The progesterone derivative dydrogesterone down-regulates neurokinin 1 receptor expression on lymphocytes, induces a Th2 skew and exerts hypoalgesic effects in mice. J Mol Med 84:159–167PubMed Orsal AS, Blois S, Labuz D, Peters EM, Schaefer M, Arck PC (2006) The progesterone derivative dydrogesterone down-regulates neurokinin 1 receptor expression on lymphocytes, induces a Th2 skew and exerts hypoalgesic effects in mice. J Mol Med 84:159–167PubMed
113.
go back to reference Schor E, Baracat EC, Simoes MJ, de Freitas V, Giannotti Filho O, de Lima GR (1999) Effects of conjugated estrogens and progestogen in surgically induced endometriosis in oophorectomized rats. Clin Exp Obstet Gynecol 26:158–161PubMed Schor E, Baracat EC, Simoes MJ, de Freitas V, Giannotti Filho O, de Lima GR (1999) Effects of conjugated estrogens and progestogen in surgically induced endometriosis in oophorectomized rats. Clin Exp Obstet Gynecol 26:158–161PubMed
114.
go back to reference Quereda F, Barroso J, Acien P (1996) Individual and combined effects of triptoreline and gestrinone on experimental endometriosis in rats. Eur J Obstet Gynecol Reprod Biol 67:35–40PubMed Quereda F, Barroso J, Acien P (1996) Individual and combined effects of triptoreline and gestrinone on experimental endometriosis in rats. Eur J Obstet Gynecol Reprod Biol 67:35–40PubMed
115.
go back to reference Katsuki Y, Takano Y, Futamura Y, Shibutani Y, Aoki D, Udagawa Y, Nozawa S (1998) Effects of dienogest, a synthetic steroid, on experimental endometriosis in rats. Eur J Endocrinol 138:216–226PubMed Katsuki Y, Takano Y, Futamura Y, Shibutani Y, Aoki D, Udagawa Y, Nozawa S (1998) Effects of dienogest, a synthetic steroid, on experimental endometriosis in rats. Eur J Endocrinol 138:216–226PubMed
116.
go back to reference Vercellini P, Fedele L, Pietropaolo G, Frontino G, Somigliana E, Crosignani PG (2003) Progestogens for endometriosis: forward to the past. Hum Reprod Update 9:387–396PubMed Vercellini P, Fedele L, Pietropaolo G, Frontino G, Somigliana E, Crosignani PG (2003) Progestogens for endometriosis: forward to the past. Hum Reprod Update 9:387–396PubMed
117.
go back to reference Crosignani P, Olive D, Bergqvist A, Luciano A (2006) Advances in the management of endometriosis: an update for clinicians. Hum Reprod Update 12:179–189PubMed Crosignani P, Olive D, Bergqvist A, Luciano A (2006) Advances in the management of endometriosis: an update for clinicians. Hum Reprod Update 12:179–189PubMed
118.
go back to reference Winkel CA, Scialli AR (2001) Medical and surgical therapies for pain associated with endometriosis. J Womens Health Gend Based Med 10:137–162PubMed Winkel CA, Scialli AR (2001) Medical and surgical therapies for pain associated with endometriosis. J Womens Health Gend Based Med 10:137–162PubMed
119.
go back to reference Atwal G, du Plessis D, Armstrong G, Slade R, Quinn M (2005) Uterine innervation after hysterectomy for chronic pelvic pain with, and without, endometriosis. Am J Obstet Gynecol 193:1650–1655PubMed Atwal G, du Plessis D, Armstrong G, Slade R, Quinn M (2005) Uterine innervation after hysterectomy for chronic pelvic pain with, and without, endometriosis. Am J Obstet Gynecol 193:1650–1655PubMed
120.
go back to reference Tokushige N, Markham R, Russell P, Fraser IS (2006) High density of small nerve fibres in the functional layer of the endometrium in women with endometriosis. Hum Reprod 21:782–787PubMed Tokushige N, Markham R, Russell P, Fraser IS (2006) High density of small nerve fibres in the functional layer of the endometrium in women with endometriosis. Hum Reprod 21:782–787PubMed
121.
go back to reference Tokushige N, Markham R, Russell P, Fraser IS (2006) Nerve fibres in peritoneal endometriosis. Hum Reprod 21:3001–3007PubMed Tokushige N, Markham R, Russell P, Fraser IS (2006) Nerve fibres in peritoneal endometriosis. Hum Reprod 21:3001–3007PubMed
122.
go back to reference Berkley KJ, Dmitrieva N, Curtis KS, Papka RE (2004) Innervation of ectopic endometrium in a rat model of endometriosis. Proc Natl Acad Sci USA 101:11094–11098PubMed Berkley KJ, Dmitrieva N, Curtis KS, Papka RE (2004) Innervation of ectopic endometrium in a rat model of endometriosis. Proc Natl Acad Sci USA 101:11094–11098PubMed
123.
go back to reference Luts L, Sundler F (1998) Autotransplantation of rat parathyroid glands: a study on morphological changes. Transplantation 66:446–453PubMed Luts L, Sundler F (1998) Autotransplantation of rat parathyroid glands: a study on morphological changes. Transplantation 66:446–453PubMed
124.
go back to reference Ferretti A, Boschi E, Stefani A, Spiga S, Romanelli M, Lemmi M, Giovannetti A, Longoni B, Mosca F (2003) Angiogenesis and nerve regeneration in a model of human skin equivalent transplant. Life Sci 73:1985–1994PubMed Ferretti A, Boschi E, Stefani A, Spiga S, Romanelli M, Lemmi M, Giovannetti A, Longoni B, Mosca F (2003) Angiogenesis and nerve regeneration in a model of human skin equivalent transplant. Life Sci 73:1985–1994PubMed
125.
go back to reference Skoff AM, Adler JE (2006) Nerve growth factor regulates substance P in adult sensory neurons through both TrkA and p75 receptors. Exp Neurol 197:430–436PubMed Skoff AM, Adler JE (2006) Nerve growth factor regulates substance P in adult sensory neurons through both TrkA and p75 receptors. Exp Neurol 197:430–436PubMed
126.
go back to reference Bracci-Laudiero L, Aloe L, Caroleo MC, Buanne P, Costa N, Starace G, Lundeberg T (2005) Endogenous NGF regulates CGRP expression in human monocytes, and affects HLA-DR and CD86 expression and IL-10 production. Blood 106:3507–3514PubMed Bracci-Laudiero L, Aloe L, Caroleo MC, Buanne P, Costa N, Starace G, Lundeberg T (2005) Endogenous NGF regulates CGRP expression in human monocytes, and affects HLA-DR and CD86 expression and IL-10 production. Blood 106:3507–3514PubMed
127.
go back to reference Dmitrieva N, McMahon SB (1996) Sensitisation of visceral afferents by nerve growth factor in the adult rat. Pain 66:87–97PubMed Dmitrieva N, McMahon SB (1996) Sensitisation of visceral afferents by nerve growth factor in the adult rat. Pain 66:87–97PubMed
128.
go back to reference Qiu BS, Vallance BA, Blennerhassett PA, Collins SM (1999) The role of CD4+ lymphocytes in the susceptibility of mice to stress-induced reactivation of experimental colitis. Nat Med 5:1178–1182PubMed Qiu BS, Vallance BA, Blennerhassett PA, Collins SM (1999) The role of CD4+ lymphocytes in the susceptibility of mice to stress-induced reactivation of experimental colitis. Nat Med 5:1178–1182PubMed
129.
go back to reference Levenstein S (2003) Stress and ulcerative colitis: convincing the doubting Thomases. Am J Gastroenterol 98:2112–2115PubMed Levenstein S (2003) Stress and ulcerative colitis: convincing the doubting Thomases. Am J Gastroenterol 98:2112–2115PubMed
130.
go back to reference Gil KM, Keefe FJ, Sampson HA, McCaskill CC, Rodin J, Crisson JE (1987) The relation of stress and family environment to atopic dermatitis symptoms in children. J Psychosom Res 31:673–684PubMed Gil KM, Keefe FJ, Sampson HA, McCaskill CC, Rodin J, Crisson JE (1987) The relation of stress and family environment to atopic dermatitis symptoms in children. J Psychosom Res 31:673–684PubMed
131.
go back to reference Paus R, Theoharides TC, Arck PC (2006) Neuroimmunoendocrine circuitry of the ‘brain–skin connection’. Trends Immunol 27:32–39PubMed Paus R, Theoharides TC, Arck PC (2006) Neuroimmunoendocrine circuitry of the ‘brain–skin connection’. Trends Immunol 27:32–39PubMed
132.
go back to reference Arck P, Knackstedt MK, Blois SM (2006) Current insights and future perspectives on neuro-endocrine–immune circuitry challenging pregnancy maintenance and fetal health. J Reprod Med Endo 3:98–102 Arck P, Knackstedt MK, Blois SM (2006) Current insights and future perspectives on neuro-endocrine–immune circuitry challenging pregnancy maintenance and fetal health. J Reprod Med Endo 3:98–102
133.
go back to reference Lima AP, Moura MD, Rosa e Silva AA (2006) Prolactin and cortisol levels in women with endometriosis. Braz J Med Biol Res 39:1121–1127PubMed Lima AP, Moura MD, Rosa e Silva AA (2006) Prolactin and cortisol levels in women with endometriosis. Braz J Med Biol Res 39:1121–1127PubMed
134.
go back to reference Cacioppo JT, Berntson GG, Malarkey WB, Kiecolt-Glaser JK, Sheridan JF, Poehlmann KM, Burleson MH, Ernst JM, Hawkley LC, Glaser R (1998) Autonomic, neuroendocrine, and immune responses to psychological stress: the reactivity hypothesis. Ann N Y Acad Sci 840:664–673PubMed Cacioppo JT, Berntson GG, Malarkey WB, Kiecolt-Glaser JK, Sheridan JF, Poehlmann KM, Burleson MH, Ernst JM, Hawkley LC, Glaser R (1998) Autonomic, neuroendocrine, and immune responses to psychological stress: the reactivity hypothesis. Ann N Y Acad Sci 840:664–673PubMed
135.
go back to reference Blalock JE (1994) The syntax of immune–neuroendocrine communication. Immunol Today 15:504–511PubMed Blalock JE (1994) The syntax of immune–neuroendocrine communication. Immunol Today 15:504–511PubMed
136.
go back to reference Glaser R, Kiecolt-Glaser JK (2005) Stress-induced immune dysfunction: implications for health. Nat Rev Immunol 5:243–251PubMed Glaser R, Kiecolt-Glaser JK (2005) Stress-induced immune dysfunction: implications for health. Nat Rev Immunol 5:243–251PubMed
137.
go back to reference Benschop RJ, Rodriguez-Feuerhahn M, Schedlowski M (1996) Catecholamine-induced leukocytosis: early observations, current research, and future directions. Brain Behav Immun 10:77–91PubMed Benschop RJ, Rodriguez-Feuerhahn M, Schedlowski M (1996) Catecholamine-induced leukocytosis: early observations, current research, and future directions. Brain Behav Immun 10:77–91PubMed
138.
go back to reference Webster JI, Tonelli L, Sternberg EM (2002) Neuroendocrine regulation of immunity. Annu Rev Immunol 20:125–163PubMed Webster JI, Tonelli L, Sternberg EM (2002) Neuroendocrine regulation of immunity. Annu Rev Immunol 20:125–163PubMed
139.
go back to reference Dhabhar FS (2000) Acute stress enhances while chronic stress suppresses skin immunity. The role of stress hormones and leukocyte trafficking. Ann N Y Acad Sci 917:876–893PubMedCrossRef Dhabhar FS (2000) Acute stress enhances while chronic stress suppresses skin immunity. The role of stress hormones and leukocyte trafficking. Ann N Y Acad Sci 917:876–893PubMedCrossRef
140.
go back to reference Wonnacott KM, Bonneau RH (2002) The effects of stress on memory cytotoxic T lymphocyte-mediated protection against herpes simplex virus infection at mucosal sites. Brain Behav Immun 16:104–117PubMed Wonnacott KM, Bonneau RH (2002) The effects of stress on memory cytotoxic T lymphocyte-mediated protection against herpes simplex virus infection at mucosal sites. Brain Behav Immun 16:104–117PubMed
141.
go back to reference Elenkov IJ, Webster EL, Torpy DJ, Chrousos GP (1999) Stress, corticotropin-releasing hormone, glucocorticoids, and the immune/inflammatory response: acute and chronic effects. Ann N Y Acad Sci 876:1–11 (discussion 11–13)PubMed Elenkov IJ, Webster EL, Torpy DJ, Chrousos GP (1999) Stress, corticotropin-releasing hormone, glucocorticoids, and the immune/inflammatory response: acute and chronic effects. Ann N Y Acad Sci 876:1–11 (discussion 11–13)PubMed
142.
go back to reference Crofford LJ, Sano H, Karalis K, Friedman TC, Epps HR, Remmers EF, Mathern P, Chrousos GP, Wilder RL (1993) Corticotropin-releasing hormone in synovial fluids and tissues of patients with rheumatoid arthritis and osteoarthritis. J Immunol 151:1587–1596PubMed Crofford LJ, Sano H, Karalis K, Friedman TC, Epps HR, Remmers EF, Mathern P, Chrousos GP, Wilder RL (1993) Corticotropin-releasing hormone in synovial fluids and tissues of patients with rheumatoid arthritis and osteoarthritis. J Immunol 151:1587–1596PubMed
143.
go back to reference van Tol EA, Petrusz P, Lund PK, Yamauchi M, Sartor RB (1996) Local production of corticotropin releasing hormone is increased in experimental intestinal inflammation in rats. Gut 39:385–392PubMed van Tol EA, Petrusz P, Lund PK, Yamauchi M, Sartor RB (1996) Local production of corticotropin releasing hormone is increased in experimental intestinal inflammation in rats. Gut 39:385–392PubMed
144.
go back to reference Singh VK (1989) Stimulatory effect of corticotropin-releasing neurohormone on human lymphocyte proliferation and interleukin-2 receptor expression. J Neuroimmunol 23:257–262PubMed Singh VK (1989) Stimulatory effect of corticotropin-releasing neurohormone on human lymphocyte proliferation and interleukin-2 receptor expression. J Neuroimmunol 23:257–262PubMed
145.
go back to reference Singh VK, Leu SJ (1990) Enhancing effect of corticotropin-releasing neurohormone on the production of interleukin-1 and interleukin-2. Neurosci Lett 120:151–154PubMed Singh VK, Leu SJ (1990) Enhancing effect of corticotropin-releasing neurohormone on the production of interleukin-1 and interleukin-2. Neurosci Lett 120:151–154PubMed
146.
go back to reference Angioni S, Petraglia F, Gallinelli A, Cossarizza A, Franceschi C, Muscettola M, Genazzani AD, Surico N, Genazzani AR (1993) Corticotropin-releasing hormone modulates cytokines release in cultured human peripheral blood mononuclear cells. Life Sci 53:1735–1742PubMed Angioni S, Petraglia F, Gallinelli A, Cossarizza A, Franceschi C, Muscettola M, Genazzani AD, Surico N, Genazzani AR (1993) Corticotropin-releasing hormone modulates cytokines release in cultured human peripheral blood mononuclear cells. Life Sci 53:1735–1742PubMed
147.
go back to reference Maes M, Kenis G, Kubera M (2003) In humans, corticotropin releasing hormone antagonizes some of the negative immunoregulatory effects of serotonin. Neuro Endocrinol Lett 24:420–424PubMed Maes M, Kenis G, Kubera M (2003) In humans, corticotropin releasing hormone antagonizes some of the negative immunoregulatory effects of serotonin. Neuro Endocrinol Lett 24:420–424PubMed
148.
go back to reference Karalis K, Sano H, Redwine J, Listwak S, Wilder RL, Chrousos GP (1991) Autocrine or paracrine inflammatory actions of corticotropin-releasing hormone in vivo. Science 254:421–423PubMed Karalis K, Sano H, Redwine J, Listwak S, Wilder RL, Chrousos GP (1991) Autocrine or paracrine inflammatory actions of corticotropin-releasing hormone in vivo. Science 254:421–423PubMed
149.
go back to reference Singh VK, Fudenberg HH (1988) Binding of [125I]corticotropin releasing factor to blood immunocytes and its reduction in Alzheimer’s disease. Immunol Lett 18:5–8PubMed Singh VK, Fudenberg HH (1988) Binding of [125I]corticotropin releasing factor to blood immunocytes and its reduction in Alzheimer’s disease. Immunol Lett 18:5–8PubMed
150.
go back to reference Cao J, Papadopoulou N, Kempuraj D, Boucher WS, Sugimoto K, Cetrulo CL, Theoharides TC (2005) Human mast cells express corticotropin-releasing hormone (CRH) receptors and CRH leads to selective secretion of vascular endothelial growth factor. J Immunol 174:7665–7675PubMed Cao J, Papadopoulou N, Kempuraj D, Boucher WS, Sugimoto K, Cetrulo CL, Theoharides TC (2005) Human mast cells express corticotropin-releasing hormone (CRH) receptors and CRH leads to selective secretion of vascular endothelial growth factor. J Immunol 174:7665–7675PubMed
151.
go back to reference Stephanou A, Jessop DS, Knight RA, Lightman SL (1990) Corticotrophin-releasing factor-like immunoreactivity and mRNA in human leukocytes. Brain Behav Immun 4:67–73PubMed Stephanou A, Jessop DS, Knight RA, Lightman SL (1990) Corticotrophin-releasing factor-like immunoreactivity and mRNA in human leukocytes. Brain Behav Immun 4:67–73PubMed
152.
go back to reference Kempuraj D, Papadopoulou NG, Lytinas M, Huang M, Kandere-Grzybowska K, Madhappan B, Boucher W, Christodoulou S, Athanassiou A, Theoharides TC (2004) Corticotropin-releasing hormone and its structurally related urocortin are synthesized and secreted by human mast cells. Endocrinology 145:43–48PubMed Kempuraj D, Papadopoulou NG, Lytinas M, Huang M, Kandere-Grzybowska K, Madhappan B, Boucher W, Christodoulou S, Athanassiou A, Theoharides TC (2004) Corticotropin-releasing hormone and its structurally related urocortin are synthesized and secreted by human mast cells. Endocrinology 145:43–48PubMed
153.
go back to reference Bileviciute I, Ahmed M, Bergstrom J, Ericsson-Dahlstrand A, Kreicbergs A, Lundeberg T (1997) Expression of corticotropin-releasing factor in the peripheral nervous system of the rat. Neuroreport 8:3127–3130PubMed Bileviciute I, Ahmed M, Bergstrom J, Ericsson-Dahlstrand A, Kreicbergs A, Lundeberg T (1997) Expression of corticotropin-releasing factor in the peripheral nervous system of the rat. Neuroreport 8:3127–3130PubMed
154.
go back to reference Merchenthaler I, Hynes MA, Vigh S, Shally AV, Petrusz P (1983) Immunocytochemical localization of corticotropin releasing factor (CRF) in the rat spinal cord. Brain Res 275:373–377PubMed Merchenthaler I, Hynes MA, Vigh S, Shally AV, Petrusz P (1983) Immunocytochemical localization of corticotropin releasing factor (CRF) in the rat spinal cord. Brain Res 275:373–377PubMed
155.
go back to reference Saunders PR, Santos J, Hanssen NP, Yates D, Groot JA, Perdue MH (2002) Physical and psychological stress in rats enhances colonic epithelial permeability via peripheral CRH. Dig Dis Sci 47:208–215PubMed Saunders PR, Santos J, Hanssen NP, Yates D, Groot JA, Perdue MH (2002) Physical and psychological stress in rats enhances colonic epithelial permeability via peripheral CRH. Dig Dis Sci 47:208–215PubMed
156.
go back to reference Florio P, Busacca M, Vignali M, Vigano P, Woods RJ, Lowry PJ, Genazzani AR, Luisi S, Santuz M, Petraglia F (1998) Peritoneal fluid levels of immunoreactive corticotropin-releasing factor (CRF) and CRF-binding protein (CRF-BP) in healthy and endometriosic women. J Endocrinol Invest 21:37–42PubMed Florio P, Busacca M, Vignali M, Vigano P, Woods RJ, Lowry PJ, Genazzani AR, Luisi S, Santuz M, Petraglia F (1998) Peritoneal fluid levels of immunoreactive corticotropin-releasing factor (CRF) and CRF-binding protein (CRF-BP) in healthy and endometriosic women. J Endocrinol Invest 21:37–42PubMed
157.
go back to reference Benschop RJ, Nieuwenhuis EE, Tromp EA, Godaert GL, Ballieux RE, van Doornen LJ (1994) Effects of beta-adrenergic blockade on immunologic and cardiovascular changes induced by mental stress. Circulation 89:762–769PubMed Benschop RJ, Nieuwenhuis EE, Tromp EA, Godaert GL, Ballieux RE, van Doornen LJ (1994) Effects of beta-adrenergic blockade on immunologic and cardiovascular changes induced by mental stress. Circulation 89:762–769PubMed
158.
go back to reference Sanders VM, Baker RA, Ramer-Quinn DS, Kasprowicz DJ, Fuchs BA, Street NE (1997) Differential expression of the beta2-adrenergic receptor by Th1 and Th2 clones: implications for cytokine production and B cell help. J Immunol 158:4200–4210PubMed Sanders VM, Baker RA, Ramer-Quinn DS, Kasprowicz DJ, Fuchs BA, Street NE (1997) Differential expression of the beta2-adrenergic receptor by Th1 and Th2 clones: implications for cytokine production and B cell help. J Immunol 158:4200–4210PubMed
159.
go back to reference Arck PC, Merali FS, Stanisz AM, Stead RH, Chaouat G, Manuel J, Clark DA (1995) Stress-induced murine abortion associated with substance P-dependent alteration in cytokines in maternal uterine decidua. Biol Reprod 53:814–819PubMed Arck PC, Merali FS, Stanisz AM, Stead RH, Chaouat G, Manuel J, Clark DA (1995) Stress-induced murine abortion associated with substance P-dependent alteration in cytokines in maternal uterine decidua. Biol Reprod 53:814–819PubMed
160.
go back to reference Aloe L, Alleva E, Fiore M (2002) Stress and nerve growth factor: findings in animal models and humans. Pharmacol Biochem Behav 73:159–166PubMed Aloe L, Alleva E, Fiore M (2002) Stress and nerve growth factor: findings in animal models and humans. Pharmacol Biochem Behav 73:159–166PubMed
161.
go back to reference Peters EM, Handjiski B, Kuhlmei A, Hagen E, Bielas H, Braun A, Klapp BF, Paus R, Arck PC (2004) Neurogenic inflammation in stress-induced termination of murine hair growth is promoted by nerve growth factor. Am J Pathol 165:259–271PubMed Peters EM, Handjiski B, Kuhlmei A, Hagen E, Bielas H, Braun A, Klapp BF, Paus R, Arck PC (2004) Neurogenic inflammation in stress-induced termination of murine hair growth is promoted by nerve growth factor. Am J Pathol 165:259–271PubMed
162.
go back to reference Massaad CA, Safieh-Garabedian B, Poole S, Atweh SF, Jabbur SJ, Saade NE (2004) Involvement of substance P, CGRP and histamine in the hyperalgesia and cytokine upregulation induced by intraplantar injection of capsaicin in rats. J Neuroimmunol 153:171–182PubMed Massaad CA, Safieh-Garabedian B, Poole S, Atweh SF, Jabbur SJ, Saade NE (2004) Involvement of substance P, CGRP and histamine in the hyperalgesia and cytokine upregulation induced by intraplantar injection of capsaicin in rats. J Neuroimmunol 153:171–182PubMed
163.
go back to reference Dallos A, Kiss M, Polyanka H, Dobozy A, Kemeny L, Husz S (2006) Effects of the neuropeptides substance P, calcitonin gene-related peptide, vasoactive intestinal polypeptide and galanin on the production of nerve growth factor and inflammatory cytokines in cultured human keratinocytes. Neuropeptides 40:251–263PubMed Dallos A, Kiss M, Polyanka H, Dobozy A, Kemeny L, Husz S (2006) Effects of the neuropeptides substance P, calcitonin gene-related peptide, vasoactive intestinal polypeptide and galanin on the production of nerve growth factor and inflammatory cytokines in cultured human keratinocytes. Neuropeptides 40:251–263PubMed
164.
go back to reference Seegers HC, Hood VC, Kidd BL, Cruwys SC, Walsh DA (2003) Enhancement of angiogenesis by endogenous substance P release and neurokinin-1 receptors during neurogenic inflammation. J Pharmacol Exp Ther 306:8–12PubMed Seegers HC, Hood VC, Kidd BL, Cruwys SC, Walsh DA (2003) Enhancement of angiogenesis by endogenous substance P release and neurokinin-1 receptors during neurogenic inflammation. J Pharmacol Exp Ther 306:8–12PubMed
165.
go back to reference Barouch R, Kazimirsky G, Appel E, Brodie C (2001) Nerve growth factor regulates TNF-alpha production in mouse macrophages via MAP kinase activation. J Leukoc Biol 69:1019–1026PubMed Barouch R, Kazimirsky G, Appel E, Brodie C (2001) Nerve growth factor regulates TNF-alpha production in mouse macrophages via MAP kinase activation. J Leukoc Biol 69:1019–1026PubMed
166.
go back to reference Tometten M, Blois S, Kuhlmei A, Stretz A, Klapp BF, Arck PC (2006) Nerve growth factor translates stress response and subsequent murine abortion via adhesion molecule-dependent pathways. Biol Reprod 74:674–683PubMed Tometten M, Blois S, Kuhlmei A, Stretz A, Klapp BF, Arck PC (2006) Nerve growth factor translates stress response and subsequent murine abortion via adhesion molecule-dependent pathways. Biol Reprod 74:674–683PubMed
167.
go back to reference Blasing H, Hendrix S, Paus R (2005) Pro-inflammatory cytokines upregulate the skin immunoreactivity for NGF, NT-3, NT-4 and their receptor, p75NTR in vivo: a preliminary report. Arch Dermatol Res 296:580–584PubMed Blasing H, Hendrix S, Paus R (2005) Pro-inflammatory cytokines upregulate the skin immunoreactivity for NGF, NT-3, NT-4 and their receptor, p75NTR in vivo: a preliminary report. Arch Dermatol Res 296:580–584PubMed
168.
go back to reference Hattori A, Iwasaki S, Murase K, Tsujimoto M, Sato M, Hayashi K, Kohno M (1994) Tumor necrosis factor is markedly synergistic with interleukin 1 and interferon-gamma in stimulating the production of nerve growth factor in fibroblasts. FEBS Lett 340:177–180PubMed Hattori A, Iwasaki S, Murase K, Tsujimoto M, Sato M, Hayashi K, Kohno M (1994) Tumor necrosis factor is markedly synergistic with interleukin 1 and interferon-gamma in stimulating the production of nerve growth factor in fibroblasts. FEBS Lett 340:177–180PubMed
169.
go back to reference Steinhoff M, Vergnolle N, Young SH, Tognetto M, Amadesi S, Ennes HS, Trevisani M, Hollenberg MD, Wallace JL, Caughey GH, Mitchell SE, Williams LM, Geppetti P, Mayer EA, Bunnett NW (2000) Agonists of proteinase-activated receptor 2 induce inflammation by a neurogenic mechanism. Nat Med 6:151–158PubMed Steinhoff M, Vergnolle N, Young SH, Tognetto M, Amadesi S, Ennes HS, Trevisani M, Hollenberg MD, Wallace JL, Caughey GH, Mitchell SE, Williams LM, Geppetti P, Mayer EA, Bunnett NW (2000) Agonists of proteinase-activated receptor 2 induce inflammation by a neurogenic mechanism. Nat Med 6:151–158PubMed
170.
go back to reference Sanfilippo JS, Williams RS, Yussman MA, Cook CL, Bissonnette F (1992) Substance P in peritoneal fluid. Am J Obstet Gynecol 166:155–159PubMed Sanfilippo JS, Williams RS, Yussman MA, Cook CL, Bissonnette F (1992) Substance P in peritoneal fluid. Am J Obstet Gynecol 166:155–159PubMed
171.
go back to reference Watkins LR, Maier SF (2000) The pain of being sick: implications of immune-to-brain communication for understanding pain. Annu Rev Psychol 51:29–57PubMed Watkins LR, Maier SF (2000) The pain of being sick: implications of immune-to-brain communication for understanding pain. Annu Rev Psychol 51:29–57PubMed
172.
go back to reference Yirmiya R, Weidenfeld J, Barak O, Avitsur R, Pollak Y, Gallily R, Wohlman A, Ovadia H, Ben-Hur T (1999) The role of brain cytokines in mediating the behavioral and neuroendocrine effects of intracerebral mycoplasma fermentans. Brain Res 829:28–38PubMed Yirmiya R, Weidenfeld J, Barak O, Avitsur R, Pollak Y, Gallily R, Wohlman A, Ovadia H, Ben-Hur T (1999) The role of brain cytokines in mediating the behavioral and neuroendocrine effects of intracerebral mycoplasma fermentans. Brain Res 829:28–38PubMed
173.
go back to reference Avitsur R, Cohen E, Yirmiya R (1997) Effects of interleukin-1 on sexual attractivity in a model of sickness behavior. Physiol Behav 63:25–30PubMed Avitsur R, Cohen E, Yirmiya R (1997) Effects of interleukin-1 on sexual attractivity in a model of sickness behavior. Physiol Behav 63:25–30PubMed
174.
go back to reference Reichenberg A, Yirmiya R, Schuld A, Kraus T, Haack M, Morag A, Pollmacher T (2001) Cytokine-associated emotional and cognitive disturbances in humans. Arch Gen Psychiatry 58:445–452PubMed Reichenberg A, Yirmiya R, Schuld A, Kraus T, Haack M, Morag A, Pollmacher T (2001) Cytokine-associated emotional and cognitive disturbances in humans. Arch Gen Psychiatry 58:445–452PubMed
175.
go back to reference Charmandari E, Tsigos C, Chrousos G (2005) Endocrinology of the stress response. Annu Rev Physiol 67:259–284PubMed Charmandari E, Tsigos C, Chrousos G (2005) Endocrinology of the stress response. Annu Rev Physiol 67:259–284PubMed
176.
go back to reference Sapolsky R, Rivier C, Yamamoto G, Plotsky P, Vale W (1987) Interleukin-1 stimulates the secretion of hypothalamic corticotropin-releasing factor. Science 238:522–524PubMed Sapolsky R, Rivier C, Yamamoto G, Plotsky P, Vale W (1987) Interleukin-1 stimulates the secretion of hypothalamic corticotropin-releasing factor. Science 238:522–524PubMed
177.
go back to reference Harbuz MS, Stephanou A, Sarlis N, Lightman SL (1992) The effects of recombinant human interleukin (IL)-1 alpha, IL-1 beta or IL-6 on hypothalamo–pituitary–adrenal axis activation. J Endocrinol 133:349–355PubMedCrossRef Harbuz MS, Stephanou A, Sarlis N, Lightman SL (1992) The effects of recombinant human interleukin (IL)-1 alpha, IL-1 beta or IL-6 on hypothalamo–pituitary–adrenal axis activation. J Endocrinol 133:349–355PubMedCrossRef
178.
go back to reference Schobitz B, Reul JM, Holsboer F (1994) The role of the hypothalamic–pituitary–adrenocortical system during inflammatory conditions. Crit Rev Neurobiol 8:263–291PubMed Schobitz B, Reul JM, Holsboer F (1994) The role of the hypothalamic–pituitary–adrenocortical system during inflammatory conditions. Crit Rev Neurobiol 8:263–291PubMed
179.
go back to reference Braun DP, Gebel H, House R, Rana N, Dmowski NP (1996) Spontaneous and induced synthesis of cytokines by peripheral blood monocytes in patients with endometriosis. Fertil Steril 65:1125–1129PubMed Braun DP, Gebel H, House R, Rana N, Dmowski NP (1996) Spontaneous and induced synthesis of cytokines by peripheral blood monocytes in patients with endometriosis. Fertil Steril 65:1125–1129PubMed
180.
go back to reference Banks WA (2005) Blood–brain barrier transport of cytokines: a mechanism for neuropathology. Curr Pharm Des 11:973–984PubMed Banks WA (2005) Blood–brain barrier transport of cytokines: a mechanism for neuropathology. Curr Pharm Des 11:973–984PubMed
181.
go back to reference Esposito P, Gheorghe D, Kandere K, Pang X, Connolly R, Jacobson S, Theoharides TC (2001) Acute stress increases permeability of the blood–brain-barrier through activation of brain mast cells. Brain Res 888:117–127PubMed Esposito P, Gheorghe D, Kandere K, Pang X, Connolly R, Jacobson S, Theoharides TC (2001) Acute stress increases permeability of the blood–brain-barrier through activation of brain mast cells. Brain Res 888:117–127PubMed
182.
go back to reference Luheshi GN, Bluthe RM, Rushforth D, Mulcahy N, Konsman JP, Goldbach M, Dantzer R (2000) Vagotomy attenuates the behavioural but not the pyrogenic effects of interleukin-1 in rats. Auton Neurosci 85:127–132PubMed Luheshi GN, Bluthe RM, Rushforth D, Mulcahy N, Konsman JP, Goldbach M, Dantzer R (2000) Vagotomy attenuates the behavioural but not the pyrogenic effects of interleukin-1 in rats. Auton Neurosci 85:127–132PubMed
183.
go back to reference Fazleabas AT (2006) A baboon model for inducing endometriosis. Methods Mol Med 121:95–99PubMed Fazleabas AT (2006) A baboon model for inducing endometriosis. Methods Mol Med 121:95–99PubMed
184.
go back to reference Sharpe-Timms KL (2002) Using rats as a research model for the study of endometriosis. Ann N Y Acad Sci 955:318–327 (discussion 340–312, 396–406)PubMedCrossRef Sharpe-Timms KL (2002) Using rats as a research model for the study of endometriosis. Ann N Y Acad Sci 955:318–327 (discussion 340–312, 396–406)PubMedCrossRef
185.
go back to reference Vernon MW, Wilson EA (1985) Studies on the surgical induction of endometriosis in the rat. Fertil Steril 44:684–694PubMed Vernon MW, Wilson EA (1985) Studies on the surgical induction of endometriosis in the rat. Fertil Steril 44:684–694PubMed
186.
go back to reference Harris HA, Bruner-Tran KL, Zhang X, Osteen KG, Lyttle CR (2005) A selective estrogen receptor-beta agonist causes lesion regression in an experimentally induced model of endometriosis. Hum Reprod 20:936–941PubMed Harris HA, Bruner-Tran KL, Zhang X, Osteen KG, Lyttle CR (2005) A selective estrogen receptor-beta agonist causes lesion regression in an experimentally induced model of endometriosis. Hum Reprod 20:936–941PubMed
187.
go back to reference Hirata T, Osuga Y, Yoshino O, Hirota Y, Harada M, Takemura Y, Morimoto C, Koga K, Yano T, Tsutsumi O, Taketani Y (2005) Development of an experimental model of endometriosis using mice that ubiquitously express green fluorescent protein. Hum Reprod 20:2092–2096PubMed Hirata T, Osuga Y, Yoshino O, Hirota Y, Harada M, Takemura Y, Morimoto C, Koga K, Yano T, Tsutsumi O, Taketani Y (2005) Development of an experimental model of endometriosis using mice that ubiquitously express green fluorescent protein. Hum Reprod 20:2092–2096PubMed
188.
go back to reference Fang Z, Yang S, Lydon JP, DeMayo F, Tamura M, Gurates B, Bulun SE (2004) Intact progesterone receptors are essential to counteract the proliferative effect of estradiol in a genetically engineered mouse model of endometriosis. Fertil Steril 82:673–678PubMed Fang Z, Yang S, Lydon JP, DeMayo F, Tamura M, Gurates B, Bulun SE (2004) Intact progesterone receptors are essential to counteract the proliferative effect of estradiol in a genetically engineered mouse model of endometriosis. Fertil Steril 82:673–678PubMed
189.
go back to reference Efstathiou JA, Sampson DA, Levine Z, Rohan RM, Zurakowski D, Folkman J, D’Amato RJ, Rupnick MA (2005) Nonsteroidal antiinflammatory drugs differentially suppress endometriosis in a murine model. Fertil Steril 83:171–181PubMed Efstathiou JA, Sampson DA, Levine Z, Rohan RM, Zurakowski D, Folkman J, D’Amato RJ, Rupnick MA (2005) Nonsteroidal antiinflammatory drugs differentially suppress endometriosis in a murine model. Fertil Steril 83:171–181PubMed
190.
go back to reference Bruner-Tran KL, Eisenberg E, Yeaman GR, Anderson TA, McBean J, Osteen KG (2002) Steroid and cytokine regulation of matrix metalloproteinase expression in endometriosis and the establishment of experimental endometriosis in nude mice. J Clin Endocrinol Metab 87:4782–4791PubMed Bruner-Tran KL, Eisenberg E, Yeaman GR, Anderson TA, McBean J, Osteen KG (2002) Steroid and cytokine regulation of matrix metalloproteinase expression in endometriosis and the establishment of experimental endometriosis in nude mice. J Clin Endocrinol Metab 87:4782–4791PubMed
191.
go back to reference Fortin M, Lepine M, Page M, Osteen K, Massie B, Hugo P, Steff AM (2003) An improved mouse model for endometriosis allows noninvasive assessment of lesion implantation and development. Fertil Steril 80(Suppl 2):832–838PubMed Fortin M, Lepine M, Page M, Osteen K, Massie B, Hugo P, Steff AM (2003) An improved mouse model for endometriosis allows noninvasive assessment of lesion implantation and development. Fertil Steril 80(Suppl 2):832–838PubMed
192.
go back to reference Waller KG, Shaw RW (1993) Gonadotropin-releasing hormone analogues for the treatment of endometriosis: long-term follow-up. Fertil Steril 59:511–515PubMed Waller KG, Shaw RW (1993) Gonadotropin-releasing hormone analogues for the treatment of endometriosis: long-term follow-up. Fertil Steril 59:511–515PubMed
193.
go back to reference Prentice A, Deary AJ, Bland E (2000) Progestagens and anti-progestagens for pain associated with endometriosis. Cochrane Database Syst Rev 2:CD002122PubMed Prentice A, Deary AJ, Bland E (2000) Progestagens and anti-progestagens for pain associated with endometriosis. Cochrane Database Syst Rev 2:CD002122PubMed
194.
go back to reference Overton CE, Lindsay PC, Johal B, Collins SA, Siddle NC, Shaw RW, Barlow DH (1994) A randomized, double-blind, placebo-controlled study of luteal phase dydrogesterone (Duphaston) in women with minimal to mild endometriosis. Fertil Steril 62:701–707PubMed Overton CE, Lindsay PC, Johal B, Collins SA, Siddle NC, Shaw RW, Barlow DH (1994) A randomized, double-blind, placebo-controlled study of luteal phase dydrogesterone (Duphaston) in women with minimal to mild endometriosis. Fertil Steril 62:701–707PubMed
195.
go back to reference Kempuraj D, Madhappan B, Christodoulou S, Boucher W, Cao J, Papadopoulou N, Cetrulo CL, Theoharides TC (2005) Flavonols inhibit proinflammatory mediator release, intracellular calcium ion levels and protein kinase C theta phosphorylation in human mast cells. Br J Pharmacol 145:934–944PubMed Kempuraj D, Madhappan B, Christodoulou S, Boucher W, Cao J, Papadopoulou N, Cetrulo CL, Theoharides TC (2005) Flavonols inhibit proinflammatory mediator release, intracellular calcium ion levels and protein kinase C theta phosphorylation in human mast cells. Br J Pharmacol 145:934–944PubMed
196.
go back to reference Osteen KG, Bruner-Tran KL, Eisenberg E (2005) Reduced progesterone action during endometrial maturation: a potential risk factor for the development of endometriosis. Fertil Steril 83:529–537PubMed Osteen KG, Bruner-Tran KL, Eisenberg E (2005) Reduced progesterone action during endometrial maturation: a potential risk factor for the development of endometriosis. Fertil Steril 83:529–537PubMed
Metadata
Title
Neuroendocrine–immune disequilibrium and endometriosis: an interdisciplinary approach
Authors
Nadja Tariverdian
Theoharis C. Theoharides
Friederike Siedentopf
Gabriela Gutiérrez
Udo Jeschke
Gabriel A. Rabinovich
Sandra M. Blois
Petra C. Arck
Publication date
01-06-2007
Publisher
Springer-Verlag
Published in
Seminars in Immunopathology / Issue 2/2007
Print ISSN: 1863-2297
Electronic ISSN: 1863-2300
DOI
https://doi.org/10.1007/s00281-007-0077-0

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