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[1]Giudice LC, Kao LC: Endometriosis. Lancet 364:1789-99 (2004)
[2]Flores JM, Rodríguez A, Sánchez J, Gómez-Cuétara C, Ramiro F: Endometrosis in mares: incidence of histopathological alterations. Reprod Domest Anim 30:61-65 (1995)
[3]Sampson JA: Peritoneal endometriosis due to menstrual dissemination of endometrial tissues into the peritoneal cavity. Am J Obstet Gynecol 14:422-69 (1927)
[4]Chand AL, Murray AS, Jones RL, Hannan NJ, Salamonsen LA, Rombauts L: Laser capture microdissection and cDNA array analysis of endometrium identify CCL16 and CCL21 as epithelial-derived inflammatory mediators associated with endometriosis. Reprod Biol Endocrinol 5:18 (2007)
[5]Sharpe-Timms KL, Nabli H, Zimmer RL, Birt JA, Davis JW: Inflammatory cytokines differentially up-regulate human endometrial haptoglobin production in women with endometriosis. Hum Reprod 25(5):1241-50 (2010)
[6]Kinugasa S, Shinohara K, Wakatsuki A: Increased asymmetric dimethylarginine and enhanced inflammation are associated with impaired vascular reactivity in women with endometriosis. Atherosclerosis 219(2):784-8 (2011)
[7]Fuseya C, Horiuchi A, Hayashi A, Suzuki A, Miyamoto T, Hayashi T, Shiozawa T: Involvement of pelvic inflammation-related mismatch repair abnormalities and microsatellite instability in the malignant transformation of ovarian endometriosis. Hum Pathol 43(11):1964-72 (2012)
[8]Haney AF, Jenkins S, Weinberg JB: The stimulus responsible for the peritoneal fluid inflammation observed in infertile women with endometriosis. Fertil Steril 56(3):408-13 (1991)
[9]Haney AF, Weinberg JB: Reduction of the intraperitoneal inflammation associated with endometriosis by treatment with medroxyprogesterone acetate. Am J Obstet Gynecol 159(2):450-4 (1988)
[10]Cao X, Yang D, Song M, Murphy A, Parthasarathy S: The presence of endometrial cells in the peritoneal cavity enhances monocyte recruitment and induces inflammatory cytokines in mice: implications for endometriosis. Fertil Steril 82 Suppl 3:999-1007 (2004)
[11]Scholl B, Bersinger NA, Kuhn A, Mueller MD: Correlation between symptoms of pain and peritoneal fluid inflammatory cytokine concentrations in endometriosis. Gynecol Endocrinol 25(11):701-6 (2009)
[12]Kuteken FS, Lancellotti CL, Ribeiro HS, Aldrighi JM, Ribeiro PA: Expression of neurotrophic and inflammatory mediators in rectosigmoid endometriosis. Rev Bras Ginecol Obstet 34(12):568-74 (2012)
[13]Novembri R, Carrarelli P, Toti P, Rocha AL, Borges LE, Reis FM, Piomboni P, Florio P, Petraglia F: Urocortin 2 and urocortin 3 in endometriosis: evidence for a possible role in inflammatory response. Mol Hum Reprod 17(9):587-93 (2011)
[14]Koga K, Osuga Y, Yoshino O, Hirota Y, Yano T, Tsutsumi O, Taketani Y: Elevated interleukin-16 levels in the peritoneal fluid of women with endometriosis may be a mechanism for inflammatory reactions associated with endometriosis. Fertil Steril 83(4):878-82 (2005)
[15]Leiva MC, Hasty LA, Lyttle CR: Inflammatory changes of the endometrium in patients with minimal-to-moderate endometriosis. Fertil Steril 62(5):967-72 (1994)
[16]Riley CF, Moen MH, Videm V: Inflammatory markers in endometriosis: reduced peritoneal neutrophil response in minimal endometriosis. Acta Obstet Gynecol Scand 86(7):877-81 (2007)
[17]Capellino S, Montagna P, Villaggio B, Sulli A, Soldano S, Ferrero S, Remorgida V, Cutolo M: Role of estrogens in inflammatory response: expression of estrogen receptors in peritoneal fluid macrophages from endometriosis. Ann N Y Acad Sci 1069:263-7 (2006)
[18]Montagna P, Capellino S, Villaggio B, Remorgida V, Ragni N, Cutolo M, Ferrero S: Peritoneal fluid macrophages in endometriosis: correlation between the expression of estrogen receptors and inflammation. Fertil Steril 90(1):156-64 (2008)
[19]Heublein S, Lenhard M, Vrekoussis T, Schoepfer J, Kuhn C, Friese K, Makrigiannakis A, Mayr D, Jeschke U: The G-protein-coupled estrogen receptor (GPER) is expressed in normal human ovaries and is upregulated in ovarian endometriosis and pelvic inflammatory disease involving the ovary. Reprod Sci 19(11):1197-204 (2012)
[20]Ferrero S, Gillott DJ, Remorgida V, Anserini P, Ragni N, Grudzinskas JG: GnRH analogue remarkably down-regulates inflammatory proteins in peritoneal fluid proteome of women with endometriosis. J Reprod Med 54(4):223-31 (2009)
[21]Khan KN, Kitajima M, Hiraki K, Fujishita A, Sekine I, Ishimaru T, Masuzaki H: Changes in tissue inflammation, angiogenesis and apoptosis in endometriosis, adenomyosis and uterine myoma after GnRH agonist therapy. Hum Reprod 25(3):642-53 (2010)
[22]Nirgianakis K, Bersinger NA, McKinnon B, Kostov P, Imboden S, Mueller MD: Regression of the inflammatory microenvironment of the peritoneal cavity in women with endometriosis by GnRHa treatment. Eur J Obstet Gynecol Reprod Biol 170(2):550-4 (2013)
[23]Bukulmez O, Hardy DB, Carr BR, Word RA, Mendelson CR: Inflammatory status influences aromatase and steroid receptor expression in endometriosis. Endocrinology 149(3):1190-204 (2008)
[24]Tariverdian N, Rücke M, Szekeres-Bartho J, Blois SM, Karpf EF, Sedlmayr P, Klapp BF, Kentenich H, Siedentopf F, Arck PC: Neuroendocrine circuitry and endometriosis: progesterone derivative dampens corticotropin-releasing hormone-induced inflammation by peritoneal cells in vitro. J Mol Med (Berl) 88(3):267-78 (2010)
[25]Cuevas M, Flores I, Thompson KJ, Ramos-Ortolaza DL, Torres-Reveron A, Appleyard CB: Stress exacerbates endometriosis manifestations and inflammatory parameters in an animal model. Reprod Sci 19(8):851-62 (2012)
[26]Mariani M, Viganò P, Gentilini D, Camisa B, Caporizzo E, Di Lucia P, Monno A, Candiani M, Somigliana E, Panina-Bordignon P: The selective vitamin D receptor agonist, elocalcitol, reduces endometriosis development in a mouse model by inhibiting peritoneal inflammation. Hum Reprod 27(7):2010-9 (2012)
[27]Xu Z, Zhao F, Lin F, Chen J, Huang Y: Lipoxin A4 inhibits the development of endometriosis in mice: the role of anti-inflammation and anti-angiogenesis. Am J Reprod Immunol 67(6):491-7 (2012)
[28]Taguchi A, Wada-Hiraike O, Kawana K, Koga K, Yamashita A, Shirane A, Urata Y, Kozuma S, Osuga Y, Fujii T: Resveratrol suppresses inflammatory responses in endometrial stromal cells derived from endometriosis: A possible role of the sirtuin 1 pathway. J Obstet Gynaecol Res 40(3):770-8 (2014)
[29]Nowak NM, Fischer OM, Gust TC, Fuhrmann U, Habenicht UF, Schmidt A: Intraperitoneal inflammation decreases endometriosis in a mouse model. Hum Reprod 23(11):2466-74 (2008)
[30]Aresu L, Benali S, Giannuzzi D, Mantovani R, Castagnaro M, Falomo ME: The role of inflammation and matrix metalloproteinases in equine endometriosis. J Vet Sci 13(2):171-7 (2012)
[31]Cocchi F1, DeVico AL, Garzino-Demo A, Arya SK, Gallo RC, Lusso P: Identification of RANTES, MIP-1 alpha, and MIP-1 beta as the major HIV-suppressive factors produced by CD8+ T cells. Science 270 (5243):1811-5 (1995)
[32]Hornung D, Ryan IP, Chao VA, Vigne JL, Schriock ED, Taylor RN: Immunolocalization and regulation of the chemokine RANTES in human endometrial and endometriosis tissues and cells. J Clin Endocrinol Metab 82(5):1621-8 (1997)
[33]Bersinger NA, von Roten S, Wunder DM, Raio L, Dreher E, Mueller MD: PAPP-A and osteoprotegerin, together with interleukin-8 and RANTES, are elevated in the peritoneal fluid of women with endometriosis. Am J Obstet Gynecol 195(1):103-8 (2006)
[34]Kyama CM, Overbergh L, Mihalyi A, Meuleman C, Mwenda JM, Mathieu C, D’Hooghe TM: Endometrial and peritoneal expression of aromatase, cytokines, and adhesion factors in women with endometriosis. Fertil Steril 89(2):301-10 (2008)
[35]Xu H, Schultze-Mosgau A, Agic A, Diedrich K, Taylor RN, Hornung D: Regulated upon activation, normal T cell expressed and secreted (RANTES) and monocyte chemotactic protein 1 in follicular fluid accumulate differentially in patients with and without endometriosis undergoing in vitro fertilization. Fertil Steril 86(6):1616-20 (2006)
[36]Umezawa M, Sakata C, Tanaka N, Kudo S, Tabata M, Takeda K, Ihara T, Sugamata M: Cytokine and chemokine expression in a rat endometriosis is similar to that in human endometriosis. Cytokine 43(2):105-9 (2008)
[37]Yuan DP, Gu L, Long J, Chen J, Ni J, Qian N, Shi YL: Shikonin reduces endometriosis by inhibiting RANTES secretion and mononuclear macrophage chemotaxis. Exp Ther Med 7(3):685-690 (2014)
[38]Antiñolo G, Fernández RM, Noval JA, Moliní JL, Borrego S: Analysis of the involvement of CCR5-Delta32 and CCR2-V64I variants in the development of endometriosis. Mol Hum Reprod 10(3):155-7 (2004)
[39]Yu J, Wang Y, Zhou WH, Wang L, He YY, Li DJ: Combination of estrogen and dioxin is involved in the pathogenesis of endometriosis by promoting chemokine secretion and invasion of endometrial stromal cells. Hum Reprod 23(7):1614-26 (2008)
[40]Yu J, Wang Y, Zhou WH, Wang L, Li DJ: Roles of regulated upon activation normal T cell expressed and secreted in pathogenesis of endometriosis. Zhonghua Fu Chan Ke Za Zhi 43(5):336-40 (2008)
[41]Wang XQ, Yu J, Luo XZ, Shi YL, Wang Y, Wang L, Li DJ: The high level of RANTES in the ectopic milieu recruits macrophages and induces their tolerance in progression of endometriosis. J Mol Endocrinol 45(5):291-9 (2010)
[42]Gentilini D, Perino A, Viganò P, Chiodo I, Cucinella G, Vignali M, Di Blasio AM, Busacca M: Gene expression profiling of peripheral blood mononuclear cells in endometriosis identifies genes altered in non-gynaecologic chronic inflammatory diseases. Hum Reprod 26(11):3109-17 (2011)
[43]Elizur SE, Lebovitz O, Weintraub AY, Eisenberg VH, Seidman DS, Goldenberg M, Soriano D: Pelvic inflammatory disease in women with endometriosis is more severe than in those without. Aust N Z J Obstet Gynaecol (2014) (Epub ahead of print)
[44]Kreiner D, Fromowitz FB, Richardson DA, Kenigsberg D: Endometrial immunofluorescence associated with endometriosis and pelvic inflammatory disease. Fertil Steril 46(2):243-6 (1986)
[45]Klein NA, Pérgola GM, Rao-Tekmal R, Dey TD, Schenken RS: Enhanced expression of resident leukocyte interferon gamma mRNA in endometriosis. Am J Reprod Immunol 30(2-3):74-81 (1993)
[46]Cunningham DS, Hansen KA, Coddington CC: Changes in T-cell regulation of responses to self antigens in women with pelvic endometriosis. Fertil Steril 58(1):114-9 (1992)
[47]Witz CA, Montoya IA, Dey TD, Schenken RS: Characterization of lymphocyte subpopulations and T cell activation in endometriosis. Am J Reprod Immunol 32(3):173-9 (1994)
[48]Na YJ, Lee DH, Kim SC, Joo JK, Wang JW, Jin JO, Kwak JY, Lee KS: Effects of peritoneal fluid from endometriosis patients on the release of monocyte-specific chemokines by leukocytes. Arch Gynecol Obstet 283(6):1333-41 (2011)
[49]Jerzak M, Baranowski W, Rechberger T, Gorski A: Enhanced T cells interactions with extracellular matrix proteins in infertile women with endometriosis. Immunol Lett 81(1):65-70 (2002)
[50]Chrobak A, Gmyrek GB, Sozański R, Sieradzka U, Paprocka M, Gabryś M, Jerzak M: The influence of extracellular matrix proteins on T-cell proliferation and apoptosis in women with endometriosis or uterine leiomyoma. Am J Reprod Immunol 51(2):123-9 (2004)
[51]Stanic AK, Kim M, Styer AK, Rueda BR: Dendritic Cells Attenuate the Early Establishment of Endometriosis-Like Lesions in a Murine Model. Reprod Sci (2014) (Epub ahead of print)
[52]Badawy SZ, Cuenca V, Stitzel A, Tice D: Immune rosettes of T and B lymphocytes in infertile women with endometriosis. J Reprod Med 32(3):194-7 (1987)
[53]Szyllo K, Tchorzewski H, Banasik M, Glowacka E, Lewkowicz P, Kamer-Bartosinska A: The involvement of T lymphocytes in the pathogenesis of endometriotic tissues overgrowth in women with endometriosis. Mediators Inflamm 12(3):131-8 (2003)
[54]Tripputi P, Bignotto M, Cigognini D, Bianchi S, Fedele L: T-cell receptor beta polymorphism is not associated with endometriosis. J Obstet Gynaecol Res 37(10):1405-8 (2011)
[55]Furuya K, Murakami M, Makimura N, Matsuda H, Ikou K, Saito K, Kawakami Y, Shibazaki T, Fukui U, Mizumoto Y, Tokuoka S, Nagata I, Kikuchi Y: Immunological and endocrinological studies on lymphocyte subpopulation and medical treatment for infertility in patients with endometriosis. Mol Cell Endocrinol 202(1-2):195-9 (2003)
[56]Mier-Cabrera J, Jiménez-Zamudio L, García-Latorre E, Cruz-Orozco O, Hernández-Guerrero C: Quantitative and qualitative peritoneal immune profiles, T-cell apoptosis and oxidative stress-associated characteristics in women with minimal and mild endometriosis. BJOG 118(1):6-16 (2011)
[57]Ho HN, Wu MY, Chao KH, Chen CD, Chen SU, Yang YS: Peritoneal interleukin-10 increases with decrease in activated CD4+ T lymphocytes in women with endometriosis. Hum Reprod 12(11):2528-33 (1997)
[58]Milewski Ł, Barcz E, Dziunycz P, Radomski D, Kamiński P, Roszkowski PI, Korczak-Kowalska G, Malejczyk J: Association of leptin with inflammatory cytokines and lymphocyte subpopulations in peritoneal fluid of patients with endometriosis. J Reprod Immunol 79(1):111-7 (2008)
[59]Podgaec S, Abrao MS, Dias JA Jr, Rizzo LV, de Oliveira RM, Baracat EC: Endometriosis: an inflammatory disease with a Th2 immune response component. Hum Reprod 22(5):1373-9 (2007)
[60]Braundmeier A, Jackson K, Hastings J, Koehler J, Nowak R, Fazleabas A: Induction of endometriosis alters the peripheral and endometrial regulatory T cell population in the non-human primate. Hum Reprod 27(6):1712-22 (2012)
[61]Olkowska-Truchanowicz J, Bocian K, Maksym RB, Białoszewska A, Włodarczyk D, Baranowski W, Ząbek J, Korczak-Kowalska G, Malejczyk J: CD4+ CD25+ FOXP3+ regulatory T cells in peripheral blood and peritoneal fluid of patients with endometriosis. Hum Reprod 28(1):119-24 (2013)
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Frontiers in Bioscience-Landmark (FBL) is published by IMR Press from Volume 26 Issue 5 (2021). Previous articles were published by another publisher on a subscription basis, and they are hosted by IMR Press on imrpress.com as a courtesy and upon agreement with Frontiers in Bioscience.
1 Department of Obstetrics and Gynecology, Zhou Pu Hospital, Shanghai, China
2 Department of Obstetrics and Gynecology, Shanghai First Maternity and Infant Hospital, Shanghai 200040, China
Abstract
Endometriosis is defined by presence of endometrial glands and stroma outside the uterine cavity and it affects approximately 5%–10% of women of reproductive age. Although endometriosis is usually considered to be due to retrograde menstruation, the true pathogenesis of this disease remains poorly understood. Endometriosis is associated with an inflammatory response and this inflammation leads to endothelial dysfunction and might even lead to carcinogenesis. Here, we review our current understanding of the role of inflammatory processes in the pathogenesis of endometriosis.
Keywords
- Endometrium
- Endometriosis
- Inflammation
- RANTES
- Review
References
- [1] Giudice LC, Kao LC: Endometriosis. Lancet 364:1789-99 (2004)
- [2] Flores JM, Rodríguez A, Sánchez J, Gómez-Cuétara C, Ramiro F: Endometrosis in mares: incidence of histopathological alterations. Reprod Domest Anim 30:61-65 (1995)
- [3] Sampson JA: Peritoneal endometriosis due to menstrual dissemination of endometrial tissues into the peritoneal cavity. Am J Obstet Gynecol 14:422-69 (1927)
- [4] Chand AL, Murray AS, Jones RL, Hannan NJ, Salamonsen LA, Rombauts L: Laser capture microdissection and cDNA array analysis of endometrium identify CCL16 and CCL21 as epithelial-derived inflammatory mediators associated with endometriosis. Reprod Biol Endocrinol 5:18 (2007)
- [5] Sharpe-Timms KL, Nabli H, Zimmer RL, Birt JA, Davis JW: Inflammatory cytokines differentially up-regulate human endometrial haptoglobin production in women with endometriosis. Hum Reprod 25(5):1241-50 (2010)
- [6] Kinugasa S, Shinohara K, Wakatsuki A: Increased asymmetric dimethylarginine and enhanced inflammation are associated with impaired vascular reactivity in women with endometriosis. Atherosclerosis 219(2):784-8 (2011)
- [7] Fuseya C, Horiuchi A, Hayashi A, Suzuki A, Miyamoto T, Hayashi T, Shiozawa T: Involvement of pelvic inflammation-related mismatch repair abnormalities and microsatellite instability in the malignant transformation of ovarian endometriosis. Hum Pathol 43(11):1964-72 (2012)
- [8] Haney AF, Jenkins S, Weinberg JB: The stimulus responsible for the peritoneal fluid inflammation observed in infertile women with endometriosis. Fertil Steril 56(3):408-13 (1991)
- [9] Haney AF, Weinberg JB: Reduction of the intraperitoneal inflammation associated with endometriosis by treatment with medroxyprogesterone acetate. Am J Obstet Gynecol 159(2):450-4 (1988)
- [10] Cao X, Yang D, Song M, Murphy A, Parthasarathy S: The presence of endometrial cells in the peritoneal cavity enhances monocyte recruitment and induces inflammatory cytokines in mice: implications for endometriosis. Fertil Steril 82 Suppl 3:999-1007 (2004)
- [11] Scholl B, Bersinger NA, Kuhn A, Mueller MD: Correlation between symptoms of pain and peritoneal fluid inflammatory cytokine concentrations in endometriosis. Gynecol Endocrinol 25(11):701-6 (2009)
- [12] Kuteken FS, Lancellotti CL, Ribeiro HS, Aldrighi JM, Ribeiro PA: Expression of neurotrophic and inflammatory mediators in rectosigmoid endometriosis. Rev Bras Ginecol Obstet 34(12):568-74 (2012)
- [13] Novembri R, Carrarelli P, Toti P, Rocha AL, Borges LE, Reis FM, Piomboni P, Florio P, Petraglia F: Urocortin 2 and urocortin 3 in endometriosis: evidence for a possible role in inflammatory response. Mol Hum Reprod 17(9):587-93 (2011)
- [14] Koga K, Osuga Y, Yoshino O, Hirota Y, Yano T, Tsutsumi O, Taketani Y: Elevated interleukin-16 levels in the peritoneal fluid of women with endometriosis may be a mechanism for inflammatory reactions associated with endometriosis. Fertil Steril 83(4):878-82 (2005)
- [15] Leiva MC, Hasty LA, Lyttle CR: Inflammatory changes of the endometrium in patients with minimal-to-moderate endometriosis. Fertil Steril 62(5):967-72 (1994)
- [16] Riley CF, Moen MH, Videm V: Inflammatory markers in endometriosis: reduced peritoneal neutrophil response in minimal endometriosis. Acta Obstet Gynecol Scand 86(7):877-81 (2007)
- [17] Capellino S, Montagna P, Villaggio B, Sulli A, Soldano S, Ferrero S, Remorgida V, Cutolo M: Role of estrogens in inflammatory response: expression of estrogen receptors in peritoneal fluid macrophages from endometriosis. Ann N Y Acad Sci 1069:263-7 (2006)
- [18] Montagna P, Capellino S, Villaggio B, Remorgida V, Ragni N, Cutolo M, Ferrero S: Peritoneal fluid macrophages in endometriosis: correlation between the expression of estrogen receptors and inflammation. Fertil Steril 90(1):156-64 (2008)
- [19] Heublein S, Lenhard M, Vrekoussis T, Schoepfer J, Kuhn C, Friese K, Makrigiannakis A, Mayr D, Jeschke U: The G-protein-coupled estrogen receptor (GPER) is expressed in normal human ovaries and is upregulated in ovarian endometriosis and pelvic inflammatory disease involving the ovary. Reprod Sci 19(11):1197-204 (2012)
- [20] Ferrero S, Gillott DJ, Remorgida V, Anserini P, Ragni N, Grudzinskas JG: GnRH analogue remarkably down-regulates inflammatory proteins in peritoneal fluid proteome of women with endometriosis. J Reprod Med 54(4):223-31 (2009)
- [21] Khan KN, Kitajima M, Hiraki K, Fujishita A, Sekine I, Ishimaru T, Masuzaki H: Changes in tissue inflammation, angiogenesis and apoptosis in endometriosis, adenomyosis and uterine myoma after GnRH agonist therapy. Hum Reprod 25(3):642-53 (2010)
- [22] Nirgianakis K, Bersinger NA, McKinnon B, Kostov P, Imboden S, Mueller MD: Regression of the inflammatory microenvironment of the peritoneal cavity in women with endometriosis by GnRHa treatment. Eur J Obstet Gynecol Reprod Biol 170(2):550-4 (2013)
- [23] Bukulmez O, Hardy DB, Carr BR, Word RA, Mendelson CR: Inflammatory status influences aromatase and steroid receptor expression in endometriosis. Endocrinology 149(3):1190-204 (2008)
- [24] Tariverdian N, Rücke M, Szekeres-Bartho J, Blois SM, Karpf EF, Sedlmayr P, Klapp BF, Kentenich H, Siedentopf F, Arck PC: Neuroendocrine circuitry and endometriosis: progesterone derivative dampens corticotropin-releasing hormone-induced inflammation by peritoneal cells in vitro. J Mol Med (Berl) 88(3):267-78 (2010)
- [25] Cuevas M, Flores I, Thompson KJ, Ramos-Ortolaza DL, Torres-Reveron A, Appleyard CB: Stress exacerbates endometriosis manifestations and inflammatory parameters in an animal model. Reprod Sci 19(8):851-62 (2012)
- [26] Mariani M, Viganò P, Gentilini D, Camisa B, Caporizzo E, Di Lucia P, Monno A, Candiani M, Somigliana E, Panina-Bordignon P: The selective vitamin D receptor agonist, elocalcitol, reduces endometriosis development in a mouse model by inhibiting peritoneal inflammation. Hum Reprod 27(7):2010-9 (2012)
- [27] Xu Z, Zhao F, Lin F, Chen J, Huang Y: Lipoxin A4 inhibits the development of endometriosis in mice: the role of anti-inflammation and anti-angiogenesis. Am J Reprod Immunol 67(6):491-7 (2012)
- [28] Taguchi A, Wada-Hiraike O, Kawana K, Koga K, Yamashita A, Shirane A, Urata Y, Kozuma S, Osuga Y, Fujii T: Resveratrol suppresses inflammatory responses in endometrial stromal cells derived from endometriosis: A possible role of the sirtuin 1 pathway. J Obstet Gynaecol Res 40(3):770-8 (2014)
- [29] Nowak NM, Fischer OM, Gust TC, Fuhrmann U, Habenicht UF, Schmidt A: Intraperitoneal inflammation decreases endometriosis in a mouse model. Hum Reprod 23(11):2466-74 (2008)
- [30] Aresu L, Benali S, Giannuzzi D, Mantovani R, Castagnaro M, Falomo ME: The role of inflammation and matrix metalloproteinases in equine endometriosis. J Vet Sci 13(2):171-7 (2012)
- [31] Cocchi F1, DeVico AL, Garzino-Demo A, Arya SK, Gallo RC, Lusso P: Identification of RANTES, MIP-1 alpha, and MIP-1 beta as the major HIV-suppressive factors produced by CD8+ T cells. Science 270 (5243):1811-5 (1995)
- [32] Hornung D, Ryan IP, Chao VA, Vigne JL, Schriock ED, Taylor RN: Immunolocalization and regulation of the chemokine RANTES in human endometrial and endometriosis tissues and cells. J Clin Endocrinol Metab 82(5):1621-8 (1997)
- [33] Bersinger NA, von Roten S, Wunder DM, Raio L, Dreher E, Mueller MD: PAPP-A and osteoprotegerin, together with interleukin-8 and RANTES, are elevated in the peritoneal fluid of women with endometriosis. Am J Obstet Gynecol 195(1):103-8 (2006)
- [34] Kyama CM, Overbergh L, Mihalyi A, Meuleman C, Mwenda JM, Mathieu C, D’Hooghe TM: Endometrial and peritoneal expression of aromatase, cytokines, and adhesion factors in women with endometriosis. Fertil Steril 89(2):301-10 (2008)
- [35] Xu H, Schultze-Mosgau A, Agic A, Diedrich K, Taylor RN, Hornung D: Regulated upon activation, normal T cell expressed and secreted (RANTES) and monocyte chemotactic protein 1 in follicular fluid accumulate differentially in patients with and without endometriosis undergoing in vitro fertilization. Fertil Steril 86(6):1616-20 (2006)
- [36] Umezawa M, Sakata C, Tanaka N, Kudo S, Tabata M, Takeda K, Ihara T, Sugamata M: Cytokine and chemokine expression in a rat endometriosis is similar to that in human endometriosis. Cytokine 43(2):105-9 (2008)
- [37] Yuan DP, Gu L, Long J, Chen J, Ni J, Qian N, Shi YL: Shikonin reduces endometriosis by inhibiting RANTES secretion and mononuclear macrophage chemotaxis. Exp Ther Med 7(3):685-690 (2014)
- [38] Antiñolo G, Fernández RM, Noval JA, Moliní JL, Borrego S: Analysis of the involvement of CCR5-Delta32 and CCR2-V64I variants in the development of endometriosis. Mol Hum Reprod 10(3):155-7 (2004)
- [39] Yu J, Wang Y, Zhou WH, Wang L, He YY, Li DJ: Combination of estrogen and dioxin is involved in the pathogenesis of endometriosis by promoting chemokine secretion and invasion of endometrial stromal cells. Hum Reprod 23(7):1614-26 (2008)
- [40] Yu J, Wang Y, Zhou WH, Wang L, Li DJ: Roles of regulated upon activation normal T cell expressed and secreted in pathogenesis of endometriosis. Zhonghua Fu Chan Ke Za Zhi 43(5):336-40 (2008)
- [41] Wang XQ, Yu J, Luo XZ, Shi YL, Wang Y, Wang L, Li DJ: The high level of RANTES in the ectopic milieu recruits macrophages and induces their tolerance in progression of endometriosis. J Mol Endocrinol 45(5):291-9 (2010)
- [42] Gentilini D, Perino A, Viganò P, Chiodo I, Cucinella G, Vignali M, Di Blasio AM, Busacca M: Gene expression profiling of peripheral blood mononuclear cells in endometriosis identifies genes altered in non-gynaecologic chronic inflammatory diseases. Hum Reprod 26(11):3109-17 (2011)
- [43] Elizur SE, Lebovitz O, Weintraub AY, Eisenberg VH, Seidman DS, Goldenberg M, Soriano D: Pelvic inflammatory disease in women with endometriosis is more severe than in those without. Aust N Z J Obstet Gynaecol (2014) (Epub ahead of print)
- [44] Kreiner D, Fromowitz FB, Richardson DA, Kenigsberg D: Endometrial immunofluorescence associated with endometriosis and pelvic inflammatory disease. Fertil Steril 46(2):243-6 (1986)
- [45] Klein NA, Pérgola GM, Rao-Tekmal R, Dey TD, Schenken RS: Enhanced expression of resident leukocyte interferon gamma mRNA in endometriosis. Am J Reprod Immunol 30(2-3):74-81 (1993)
- [46] Cunningham DS, Hansen KA, Coddington CC: Changes in T-cell regulation of responses to self antigens in women with pelvic endometriosis. Fertil Steril 58(1):114-9 (1992)
- [47] Witz CA, Montoya IA, Dey TD, Schenken RS: Characterization of lymphocyte subpopulations and T cell activation in endometriosis. Am J Reprod Immunol 32(3):173-9 (1994)
- [48] Na YJ, Lee DH, Kim SC, Joo JK, Wang JW, Jin JO, Kwak JY, Lee KS: Effects of peritoneal fluid from endometriosis patients on the release of monocyte-specific chemokines by leukocytes. Arch Gynecol Obstet 283(6):1333-41 (2011)
- [49] Jerzak M, Baranowski W, Rechberger T, Gorski A: Enhanced T cells interactions with extracellular matrix proteins in infertile women with endometriosis. Immunol Lett 81(1):65-70 (2002)
- [50] Chrobak A, Gmyrek GB, Sozański R, Sieradzka U, Paprocka M, Gabryś M, Jerzak M: The influence of extracellular matrix proteins on T-cell proliferation and apoptosis in women with endometriosis or uterine leiomyoma. Am J Reprod Immunol 51(2):123-9 (2004)
- [51] Stanic AK, Kim M, Styer AK, Rueda BR: Dendritic Cells Attenuate the Early Establishment of Endometriosis-Like Lesions in a Murine Model. Reprod Sci (2014) (Epub ahead of print)
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