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Published in: Journal of Neuroinflammation 1/2020

Open Access 01-12-2020 | Endometriosis | Review

Autonomic nervous system and inflammation interaction in endometriosis-associated pain

Authors: Yajing Wei, Yanchun Liang, Haishan Lin, Yujing Dai, Shuzhong Yao

Published in: Journal of Neuroinflammation | Issue 1/2020

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Abstract

Endometriosis is a chronic inflammatory disease. Pain is the most common symptom in endometriosis. Endometriosis-associated pain is caused by inflammation, and is related to aberrant innervation. Although the specific mechanism between endometriosis-associated pain and the interaction of aberrant innervation and inflammation remains unclear, many studies have confirmed certain correlations between them. In addition, we found that some chronic inflammatory autoimmune diseases (AIDs) such as inflammatory bowel disease (IBD) and rheumatoid arthritis (RA) share similar characteristics: the changes in dysregulation of inflammatory factors as well as the function and innervation of the autonomic nervous system (ANS). The mechanisms underlying the interaction between the ANS and inflammation have provided new advances among these disorders. Therefore, the purpose of this review is to compare the changes in inflammation and ANS in endometriosis, IBD, and RA; and to explore the role and possible mechanism of sympathetic and parasympathetic nerves in endometriosis-associated inflammation by referring to IBD and RA studies to provide some reference for further endometriosis research and treatment.
Literature
1.
go back to reference Symons LK, Miller JE, Kay VR, Marks RM, Liblik K, Koti M, Tayade C. The Immunopathophysiology of endometriosis. Trends Mol Med. 2018;24:748–62.PubMedCrossRef Symons LK, Miller JE, Kay VR, Marks RM, Liblik K, Koti M, Tayade C. The Immunopathophysiology of endometriosis. Trends Mol Med. 2018;24:748–62.PubMedCrossRef
2.
go back to reference Morotti M, Vincent K, Brawn J, Zondervan KT, Becker CM. Peripheral changes in endometriosis-associated pain. Hum Reprod Update. 2014;20:717–36.PubMedCrossRef Morotti M, Vincent K, Brawn J, Zondervan KT, Becker CM. Peripheral changes in endometriosis-associated pain. Hum Reprod Update. 2014;20:717–36.PubMedCrossRef
3.
go back to reference McKinnon BD, Bertschi D, Bersinger NA, Mueller MD. Inflammation and nerve fiber interaction in endometriotic pain. Trends Endocrinol Metab. 2015;26:1–10.PubMedCrossRef McKinnon BD, Bertschi D, Bersinger NA, Mueller MD. Inflammation and nerve fiber interaction in endometriotic pain. Trends Endocrinol Metab. 2015;26:1–10.PubMedCrossRef
4.
go back to reference Zhang T, De Carolis C, Man G, Wang CC. The link between immunity, autoimmunity and endometriosis: a literature update. Autoimmun Rev. 2018;17:945–55.PubMedCrossRef Zhang T, De Carolis C, Man G, Wang CC. The link between immunity, autoimmunity and endometriosis: a literature update. Autoimmun Rev. 2018;17:945–55.PubMedCrossRef
5.
go back to reference Yu J, Francisco A, Patel BG, Cline JM, Zou E, Berga SL, Taylor RN. IL-1beta stimulates brain-derived neurotrophic factor production in eutopic endometriosis stromal cell cultures: a model for cytokine regulation of neuroangiogenesis. Am J Pathol. 2018;188:2281–92.PubMedPubMedCentralCrossRef Yu J, Francisco A, Patel BG, Cline JM, Zou E, Berga SL, Taylor RN. IL-1beta stimulates brain-derived neurotrophic factor production in eutopic endometriosis stromal cell cultures: a model for cytokine regulation of neuroangiogenesis. Am J Pathol. 2018;188:2281–92.PubMedPubMedCentralCrossRef
6.
go back to reference Arnold J, Barcena DAM, Ruster C, Vercellino GF, Chiantera V, Schneider A, Mechsner S. Imbalance between sympathetic and sensory innervation in peritoneal endometriosis. Brain Behav Immun. 2012;26:132–41.PubMedCrossRef Arnold J, Barcena DAM, Ruster C, Vercellino GF, Chiantera V, Schneider A, Mechsner S. Imbalance between sympathetic and sensory innervation in peritoneal endometriosis. Brain Behav Immun. 2012;26:132–41.PubMedCrossRef
7.
go back to reference Tai FW, Chang CY, Chiang JH, Lin WC, Wan L. Association of pelvic inflammatory disease with risk of endometriosis: a nationwide cohort study involving 141,460 individuals. J Clin Med. 2018;7(11):379.PubMedCentralCrossRef Tai FW, Chang CY, Chiang JH, Lin WC, Wan L. Association of pelvic inflammatory disease with risk of endometriosis: a nationwide cohort study involving 141,460 individuals. J Clin Med. 2018;7(11):379.PubMedCentralCrossRef
8.
go back to reference Wang G, Tokushige N, Markham R, Fraser IS. Rich innervation of deep infiltrating endometriosis. Hum Reprod. 2009;24:827–34.PubMedCrossRef Wang G, Tokushige N, Markham R, Fraser IS. Rich innervation of deep infiltrating endometriosis. Hum Reprod. 2009;24:827–34.PubMedCrossRef
9.
go back to reference Mechsner S, Kaiser A, Kopf A, Gericke C, Ebert A, Bartley J. A pilot study to evaluate the clinical relevance of endometriosis-associated nerve fibers in peritoneal endometriotic lesions. Fertil Steril. 2009;92:1856–61.PubMedCrossRef Mechsner S, Kaiser A, Kopf A, Gericke C, Ebert A, Bartley J. A pilot study to evaluate the clinical relevance of endometriosis-associated nerve fibers in peritoneal endometriotic lesions. Fertil Steril. 2009;92:1856–61.PubMedCrossRef
10.
go back to reference Coxon L, Horne AW, Vincent K. Pathophysiology of endometriosis-associated pain: a review of pelvic and central nervous system mechanisms. Best Pract Res Clin Obstet Gynaecol. 2018;51:53–67.PubMedCrossRef Coxon L, Horne AW, Vincent K. Pathophysiology of endometriosis-associated pain: a review of pelvic and central nervous system mechanisms. Best Pract Res Clin Obstet Gynaecol. 2018;51:53–67.PubMedCrossRef
11.
go back to reference Ferrero S, Haas S, Remorgida V, Camerini G, Fulcheri E, Ragni N, Straub RH, Capellino S. Loss of sympathetic nerve fibers in intestinal endometriosis. Fertil Steril. 2010;94:2817–9.PubMedCrossRef Ferrero S, Haas S, Remorgida V, Camerini G, Fulcheri E, Ragni N, Straub RH, Capellino S. Loss of sympathetic nerve fibers in intestinal endometriosis. Fertil Steril. 2010;94:2817–9.PubMedCrossRef
12.
go back to reference Greaves E, Cousins FL, Murray A, Esnal-Zufiaurre A, Fassbender A, Horne AW, Saunders PT. A novel mouse model of endometriosis mimics human phenotype and reveals insights into the inflammatory contribution of shed endometrium. Am J Pathol. 2014;184:1930–9.PubMedPubMedCentralCrossRef Greaves E, Cousins FL, Murray A, Esnal-Zufiaurre A, Fassbender A, Horne AW, Saunders PT. A novel mouse model of endometriosis mimics human phenotype and reveals insights into the inflammatory contribution of shed endometrium. Am J Pathol. 2014;184:1930–9.PubMedPubMedCentralCrossRef
13.
go back to reference Halme J, Hammond MG, Hulka JF, Raj SG, Talbert LM. Retrograde menstruation in healthy women and in patients with endometriosis. Obstet Gynecol. 1984;64:151–4.PubMed Halme J, Hammond MG, Hulka JF, Raj SG, Talbert LM. Retrograde menstruation in healthy women and in patients with endometriosis. Obstet Gynecol. 1984;64:151–4.PubMed
14.
go back to reference Tran LV, Tokushige N, Berbic M, Markham R, Fraser IS. Macrophages and nerve fibres in peritoneal endometriosis. Hum Reprod. 2009;24:835–41.PubMedCrossRef Tran LV, Tokushige N, Berbic M, Markham R, Fraser IS. Macrophages and nerve fibres in peritoneal endometriosis. Hum Reprod. 2009;24:835–41.PubMedCrossRef
15.
go back to reference Bacci M, Capobianco A, Monno A, Cottone L, Di Puppo F, Camisa B, Mariani M, Brignole C, Ponzoni M, Ferrari S, et al. Macrophages are alternatively activated in patients with endometriosis and required for growth and vascularization of lesions in a mouse model of disease. Am J Pathol. 2009;175:547–56.PubMedPubMedCentralCrossRef Bacci M, Capobianco A, Monno A, Cottone L, Di Puppo F, Camisa B, Mariani M, Brignole C, Ponzoni M, Ferrari S, et al. Macrophages are alternatively activated in patients with endometriosis and required for growth and vascularization of lesions in a mouse model of disease. Am J Pathol. 2009;175:547–56.PubMedPubMedCentralCrossRef
16.
go back to reference Takamura M, Osuga Y, Izumi G, Yoshino O, Koga K, Saito A, Hirata T, Hirota Y, Harada M, Hasegawa A, Taketani Y. Interleukin-17A is present in neutrophils in endometrioma and stimulates the secretion of growth-regulated oncogene-alpha (Gro-alpha) from endometrioma stromal cells. Fertil Steril. 2012;98:1218–24.PubMedCrossRef Takamura M, Osuga Y, Izumi G, Yoshino O, Koga K, Saito A, Hirata T, Hirota Y, Harada M, Hasegawa A, Taketani Y. Interleukin-17A is present in neutrophils in endometrioma and stimulates the secretion of growth-regulated oncogene-alpha (Gro-alpha) from endometrioma stromal cells. Fertil Steril. 2012;98:1218–24.PubMedCrossRef
18.
go back to reference Chang KK, Liu LB, Jin LP, Zhang B, Mei J, Li H, Wei CY, Zhou WJ, Zhu XY, Shao J, et al. IL-27 triggers IL-10 production in Th17 cells via a c-Maf/RORgammat/Blimp-1 signal to promote the progression of endometriosis. Cell Death Dis. 2017;8:e2666.PubMedPubMedCentralCrossRef Chang KK, Liu LB, Jin LP, Zhang B, Mei J, Li H, Wei CY, Zhou WJ, Zhu XY, Shao J, et al. IL-27 triggers IL-10 production in Th17 cells via a c-Maf/RORgammat/Blimp-1 signal to promote the progression of endometriosis. Cell Death Dis. 2017;8:e2666.PubMedPubMedCentralCrossRef
19.
go back to reference Wang F, Wang H, Jin D, Zhang Y. Serum miR-17, IL-4, and IL-6 levels for diagnosis of endometriosis. Medicine (Baltimore). 2018;97:e10853.CrossRef Wang F, Wang H, Jin D, Zhang Y. Serum miR-17, IL-4, and IL-6 levels for diagnosis of endometriosis. Medicine (Baltimore). 2018;97:e10853.CrossRef
20.
go back to reference Yao C, Narumiya S. Prostaglandin-cytokine crosstalk in chronic inflammation. Br J Pharmacol. 2019;176:337–54.PubMedCrossRef Yao C, Narumiya S. Prostaglandin-cytokine crosstalk in chronic inflammation. Br J Pharmacol. 2019;176:337–54.PubMedCrossRef
21.
go back to reference McAllister SL, Giourgas BK, Faircloth EK, Leishman E, Bradshaw HB, Gross ER. Prostaglandin levels, vaginal innervation, and cyst innervation as peripheral contributors to endometriosis-associated vaginal hyperalgesia in rodents. Mol Cell Endocrinol. 2016;437:120–9.PubMedPubMedCentralCrossRef McAllister SL, Giourgas BK, Faircloth EK, Leishman E, Bradshaw HB, Gross ER. Prostaglandin levels, vaginal innervation, and cyst innervation as peripheral contributors to endometriosis-associated vaginal hyperalgesia in rodents. Mol Cell Endocrinol. 2016;437:120–9.PubMedPubMedCentralCrossRef
22.
go back to reference Orellana R, Garcia-Solares J, Donnez J, van Kerk O, Dolmans MM, Donnez O. Important role of collective cell migration and nerve fiber density in the development of deep nodular endometriosis. Fertil Steril. 2017;107:987–95.PubMedCrossRef Orellana R, Garcia-Solares J, Donnez J, van Kerk O, Dolmans MM, Donnez O. Important role of collective cell migration and nerve fiber density in the development of deep nodular endometriosis. Fertil Steril. 2017;107:987–95.PubMedCrossRef
23.
go back to reference Burns KA, Thomas SY, Hamilton KJ, Young SL, Cook DN, Korach KS. Early endometriosis in females is directed by immune-mediated estrogen receptor alpha and IL-6 cross-talk. Endocrinology. 2018;159:103–18.PubMedCrossRef Burns KA, Thomas SY, Hamilton KJ, Young SL, Cook DN, Korach KS. Early endometriosis in females is directed by immune-mediated estrogen receptor alpha and IL-6 cross-talk. Endocrinology. 2018;159:103–18.PubMedCrossRef
25.
go back to reference Pepe G, Locati M, Della TS, Mornata F, Cignarella A, Maggi A, Vegeto E. The estrogen-macrophage interplay in the homeostasis of the female reproductive tract. Hum Reprod Update. 2018;24:652–72.PubMedCrossRef Pepe G, Locati M, Della TS, Mornata F, Cignarella A, Maggi A, Vegeto E. The estrogen-macrophage interplay in the homeostasis of the female reproductive tract. Hum Reprod Update. 2018;24:652–72.PubMedCrossRef
28.
go back to reference Yuan M, Li D, An M, Li Q, Zhang L, Wang G. Rediscovering peritoneal macrophages in a murine endometriosis model. Hum Reprod. 2017;32:94–102.PubMedCrossRef Yuan M, Li D, An M, Li Q, Zhang L, Wang G. Rediscovering peritoneal macrophages in a murine endometriosis model. Hum Reprod. 2017;32:94–102.PubMedCrossRef
29.
go back to reference Shao J, Zhang B, Yu JJ, Wei CY, Zhou WJ, Chang KK, Yang HL, Jin LP, Zhu XY, Li MQ. Macrophages promote the growth and invasion of endometrial stromal cells by downregulating IL-24 in endometriosis. Reproduction. 2016;152:673–82.PubMedCrossRef Shao J, Zhang B, Yu JJ, Wei CY, Zhou WJ, Chang KK, Yang HL, Jin LP, Zhu XY, Li MQ. Macrophages promote the growth and invasion of endometrial stromal cells by downregulating IL-24 in endometriosis. Reproduction. 2016;152:673–82.PubMedCrossRef
30.
go back to reference Nie MF, Xie Q, Wu YH, He H, Zou LJ, She XL, Wu XQ. Serum and ectopic endometrium from women with endometriosis modulate macrophage M1/M2 polarization via the Smad2/Smad3 pathway. J Immunol Res. 2018;2018:6285813.PubMedPubMedCentralCrossRef Nie MF, Xie Q, Wu YH, He H, Zou LJ, She XL, Wu XQ. Serum and ectopic endometrium from women with endometriosis modulate macrophage M1/M2 polarization via the Smad2/Smad3 pathway. J Immunol Res. 2018;2018:6285813.PubMedPubMedCentralCrossRef
31.
go back to reference Sekulovski N, Whorton AE, Shi M, MacLean JI, Hayashi K. Endometriotic inflammatory microenvironment induced by macrophages can be targeted by niclosamidedagger. Biol Reprod. 2019;100:398–408.PubMedCrossRef Sekulovski N, Whorton AE, Shi M, MacLean JI, Hayashi K. Endometriotic inflammatory microenvironment induced by macrophages can be targeted by niclosamidedagger. Biol Reprod. 2019;100:398–408.PubMedCrossRef
32.
go back to reference Ponce C, Torres M, Galleguillos C, Sovino H, Boric MA, Fuentes A, Johnson MC. Nuclear factor kappaB pathway and interleukin-6 are affected in eutopic endometrium of women with endometriosis. Reproduction. 2009;137:727–37.PubMedCrossRef Ponce C, Torres M, Galleguillos C, Sovino H, Boric MA, Fuentes A, Johnson MC. Nuclear factor kappaB pathway and interleukin-6 are affected in eutopic endometrium of women with endometriosis. Reproduction. 2009;137:727–37.PubMedCrossRef
33.
go back to reference Binda MM, Donnez J, Dolmans MM. Targeting mast cells: a new way to treat endometriosis. Expert Opin Ther Targets. 2017;21:67–75.PubMedCrossRef Binda MM, Donnez J, Dolmans MM. Targeting mast cells: a new way to treat endometriosis. Expert Opin Ther Targets. 2017;21:67–75.PubMedCrossRef
34.
go back to reference Menzies FM, Shepherd MC, Nibbs RJ, Nelson SM. The role of mast cells and their mediators in reproduction, pregnancy and labour. Hum Reprod Update. 2011;17:383–96.PubMedCrossRef Menzies FM, Shepherd MC, Nibbs RJ, Nelson SM. The role of mast cells and their mediators in reproduction, pregnancy and labour. Hum Reprod Update. 2011;17:383–96.PubMedCrossRef
35.
go back to reference Olivera A, Beaven MA, Metcalfe DD. Mast cells signal their importance in health and disease. J Allergy Clin Immunol. 2018;142:381–93.PubMedCrossRef Olivera A, Beaven MA, Metcalfe DD. Mast cells signal their importance in health and disease. J Allergy Clin Immunol. 2018;142:381–93.PubMedCrossRef
36.
go back to reference Bungum HF, Nygaard U, Vestergaard C, Martensen PM, Knudsen UB. Increased IL-25 levels in the peritoneal fluid of patients with endometriosis. J Reprod Immunol. 2016;114:6–9.PubMedCrossRef Bungum HF, Nygaard U, Vestergaard C, Martensen PM, Knudsen UB. Increased IL-25 levels in the peritoneal fluid of patients with endometriosis. J Reprod Immunol. 2016;114:6–9.PubMedCrossRef
37.
go back to reference Gonzalez-de-Olano D, Alvarez-Twose I. Mast cells as key players in allergy and inflammation. J Investig Allergol Clin Immunol. 2018;28:365–78.PubMedCrossRef Gonzalez-de-Olano D, Alvarez-Twose I. Mast cells as key players in allergy and inflammation. J Investig Allergol Clin Immunol. 2018;28:365–78.PubMedCrossRef
38.
go back to reference Mortaz E, Amani S, Mumby S, Adcock IM, Movassaghi M, Folkerts J, Garssen J, Folkerts G. Role of mast cells and type 2 innate lymphoid (ILC2) cells in lung transplantation. J Immunol Res. 2018;2018:2785971.PubMedPubMedCentralCrossRef Mortaz E, Amani S, Mumby S, Adcock IM, Movassaghi M, Folkerts J, Garssen J, Folkerts G. Role of mast cells and type 2 innate lymphoid (ILC2) cells in lung transplantation. J Immunol Res. 2018;2018:2785971.PubMedPubMedCentralCrossRef
39.
go back to reference Wilcock A, Bahri R, Bulfone-Paus S, Arkwright PD. Mast cell disorders: from infancy to maturity. Allergy. 2019;74:53–63.PubMedCrossRef Wilcock A, Bahri R, Bulfone-Paus S, Arkwright PD. Mast cell disorders: from infancy to maturity. Allergy. 2019;74:53–63.PubMedCrossRef
40.
go back to reference Zhu TH, Ding SJ, Li TT, Zhu LB, Huang XF, Zhang XM. Estrogen is an important mediator of mast cell activation in ovarian endometriomas. Reproduction. 2018;155:73–83.PubMedCrossRef Zhu TH, Ding SJ, Li TT, Zhu LB, Huang XF, Zhang XM. Estrogen is an important mediator of mast cell activation in ovarian endometriomas. Reproduction. 2018;155:73–83.PubMedCrossRef
41.
go back to reference Takamura M, Koga K, Izumi G, Urata Y, Nagai M, Hasegawa A, Harada M, Hirata T, Hirota Y, Wada-Hiraike O, et al. Neutrophil depletion reduces endometriotic lesion formation in mice. Am J Reprod Immunol. 2016;76:193–8.PubMedCrossRef Takamura M, Koga K, Izumi G, Urata Y, Nagai M, Hasegawa A, Harada M, Hirata T, Hirota Y, Wada-Hiraike O, et al. Neutrophil depletion reduces endometriotic lesion formation in mice. Am J Reprod Immunol. 2016;76:193–8.PubMedCrossRef
42.
go back to reference Wang XM, Ma ZY, Song N. Inflammatory cytokines IL-6, IL-10, IL-13, TNF-alpha and peritoneal fluid flora were associated with infertility in patients with endometriosis. Eur Rev Med Pharmacol Sci. 2018;22:2513–8.PubMed Wang XM, Ma ZY, Song N. Inflammatory cytokines IL-6, IL-10, IL-13, TNF-alpha and peritoneal fluid flora were associated with infertility in patients with endometriosis. Eur Rev Med Pharmacol Sci. 2018;22:2513–8.PubMed
43.
go back to reference Kolaczkowska E, Kubes P. Neutrophil recruitment and function in health and inflammation. Nat Rev Immunol. 2013;13:159–75.PubMedCrossRef Kolaczkowska E, Kubes P. Neutrophil recruitment and function in health and inflammation. Nat Rev Immunol. 2013;13:159–75.PubMedCrossRef
44.
go back to reference Na YJ, Yang SH, Baek DW, Lee DH, Kim KH, Choi YM, Oh ST, Hong YS, Kwak JY, Lee KS. Effects of peritoneal fluid from endometriosis patients on the release of vascular endothelial growth factor by neutrophils and monocytes. Hum Reprod. 2006;21:1846–55.PubMedCrossRef Na YJ, Yang SH, Baek DW, Lee DH, Kim KH, Choi YM, Oh ST, Hong YS, Kwak JY, Lee KS. Effects of peritoneal fluid from endometriosis patients on the release of vascular endothelial growth factor by neutrophils and monocytes. Hum Reprod. 2006;21:1846–55.PubMedCrossRef
45.
go back to reference Saito S, Nakashima A, Ito M, Shima T. Clinical implication of recent advances in our understanding of IL-17 and reproductive immunology. Expert Rev Clin Immunol. 2011;7:649–57.PubMedCrossRef Saito S, Nakashima A, Ito M, Shima T. Clinical implication of recent advances in our understanding of IL-17 and reproductive immunology. Expert Rev Clin Immunol. 2011;7:649–57.PubMedCrossRef
46.
go back to reference Gogacz M, Winkler I, Bojarska-Junak A, Tabarkiewicz J, Semczuk A, Rechberger T, Adamiak A. Increased percentage of Th17 cells in peritoneal fluid is associated with severity of endometriosis. J Reprod Immunol. 2016;117:39–44.PubMedCrossRef Gogacz M, Winkler I, Bojarska-Junak A, Tabarkiewicz J, Semczuk A, Rechberger T, Adamiak A. Increased percentage of Th17 cells in peritoneal fluid is associated with severity of endometriosis. J Reprod Immunol. 2016;117:39–44.PubMedCrossRef
47.
go back to reference Hirata T, Osuga Y, Takamura M, Saito A, Hasegawa A, Koga K, Yoshino O, Hirota Y, Harada M, Taketani Y. Interleukin-17F increases the secretion of interleukin-8 and the expression of cyclooxygenase 2 in endometriosis. Fertil Steril. 2011;96:113–7.PubMedCrossRef Hirata T, Osuga Y, Takamura M, Saito A, Hasegawa A, Koga K, Yoshino O, Hirota Y, Harada M, Taketani Y. Interleukin-17F increases the secretion of interleukin-8 and the expression of cyclooxygenase 2 in endometriosis. Fertil Steril. 2011;96:113–7.PubMedCrossRef
49.
go back to reference Sikora J, Ferrero S, Mielczarek-Palacz A, Kondera-Anasz Z. The delicate balance between the good and the bad IL-1 proinflammatory effects in endometriosis. Curr Med Chem. 2018;25:2105–21.PubMedCrossRef Sikora J, Ferrero S, Mielczarek-Palacz A, Kondera-Anasz Z. The delicate balance between the good and the bad IL-1 proinflammatory effects in endometriosis. Curr Med Chem. 2018;25:2105–21.PubMedCrossRef
50.
go back to reference Jiang JF, Deng Y, Xue W, Zheng TP, Sun AJ. Increased expression of interleukin 37 in the eutopic and ectopic endometrium of patients with ovarian endometriosis. Reprod Sci. 2016;23:244–8.PubMedCrossRef Jiang JF, Deng Y, Xue W, Zheng TP, Sun AJ. Increased expression of interleukin 37 in the eutopic and ectopic endometrium of patients with ovarian endometriosis. Reprod Sci. 2016;23:244–8.PubMedCrossRef
51.
go back to reference Fan YY, Chen HY, Chen W, Liu YN, Fu Y, Wang LN. Expression of inflammatory cytokines in serum and peritoneal fluid from patients with different stages of endometriosis. Gynecol Endocrinol. 2018;34:507–12.PubMedCrossRef Fan YY, Chen HY, Chen W, Liu YN, Fu Y, Wang LN. Expression of inflammatory cytokines in serum and peritoneal fluid from patients with different stages of endometriosis. Gynecol Endocrinol. 2018;34:507–12.PubMedCrossRef
52.
go back to reference Jiang J, Yu K, Jiang Z, Xue M. IL-37 affects the occurrence and development of endometriosis by regulating the biological behavior of endometrial stromal cells through multiple signaling pathways. Biol Chem. 2018;399:1325–37.PubMedCrossRef Jiang J, Yu K, Jiang Z, Xue M. IL-37 affects the occurrence and development of endometriosis by regulating the biological behavior of endometrial stromal cells through multiple signaling pathways. Biol Chem. 2018;399:1325–37.PubMedCrossRef
53.
go back to reference Conti P, Caraffa A, Mastrangelo F, Tettamanti L, Ronconi G, Frydas I, Kritas SK, Theoharides TC. Critical role of inflammatory mast cell in fibrosis: potential therapeutic effect of IL-37. Cell Prolif. 2018;51:e12475.PubMedCrossRefPubMedCentral Conti P, Caraffa A, Mastrangelo F, Tettamanti L, Ronconi G, Frydas I, Kritas SK, Theoharides TC. Critical role of inflammatory mast cell in fibrosis: potential therapeutic effect of IL-37. Cell Prolif. 2018;51:e12475.PubMedCrossRefPubMedCentral
54.
go back to reference Xu WD, Zhao Y, Liu Y. Insights into IL-37, the role in autoimmune diseases. Autoimmun Rev. 2015;14:1170–5.PubMedCrossRef Xu WD, Zhao Y, Liu Y. Insights into IL-37, the role in autoimmune diseases. Autoimmun Rev. 2015;14:1170–5.PubMedCrossRef
55.
go back to reference Kaabachi W, Kacem O, Belhaj R, Hamzaoui A, Hamzaoui K. Interleukin-37 in endometriosis. Immunol Lett. 2017;185:52–5.PubMedCrossRef Kaabachi W, Kacem O, Belhaj R, Hamzaoui A, Hamzaoui K. Interleukin-37 in endometriosis. Immunol Lett. 2017;185:52–5.PubMedCrossRef
56.
go back to reference Mari-Alexandre J, Barcelo-Molina M, Belmonte-Lopez E, Garcia-Oms J, Estelles A, Braza-Boils A, Gilabert-Estelles J. Micro-RNA profile and proteins in peritoneal fluid from women with endometriosis: their relationship with sterility. Fertil Steril. 2018;109:675–84.PubMedCrossRef Mari-Alexandre J, Barcelo-Molina M, Belmonte-Lopez E, Garcia-Oms J, Estelles A, Braza-Boils A, Gilabert-Estelles J. Micro-RNA profile and proteins in peritoneal fluid from women with endometriosis: their relationship with sterility. Fertil Steril. 2018;109:675–84.PubMedCrossRef
57.
go back to reference Nematian SE, Mamillapalli R, Kadakia TS, Majidi ZM, Moustafa S, Taylor HS. Systemic inflammation induced by microRNAs: endometriosis-derived alterations in circulating microRNA 125b-5p and let-7b-5p regulate macrophage cytokine production. J Clin Endocrinol Metab. 2018;103:64–74.PubMedCrossRef Nematian SE, Mamillapalli R, Kadakia TS, Majidi ZM, Moustafa S, Taylor HS. Systemic inflammation induced by microRNAs: endometriosis-derived alterations in circulating microRNA 125b-5p and let-7b-5p regulate macrophage cytokine production. J Clin Endocrinol Metab. 2018;103:64–74.PubMedCrossRef
58.
go back to reference Wang XQ, Zhou WJ, Luo XZ, Tao Y, Li DJ. Synergistic effect of regulatory T cells and proinflammatory cytokines in angiogenesis in the endometriotic milieu. Hum Reprod. 2017;32:1304–17.PubMedCrossRef Wang XQ, Zhou WJ, Luo XZ, Tao Y, Li DJ. Synergistic effect of regulatory T cells and proinflammatory cytokines in angiogenesis in the endometriotic milieu. Hum Reprod. 2017;32:1304–17.PubMedCrossRef
59.
go back to reference Wang WJ, Liu FJ, Xin-Liu, Hao CF, Bao HC, Qu QL, Liu XM. Adoptive transfer of pregnancy-induced CD4+CD25+ regulatory T cells reverses the increase in abortion rate caused by interleukin 17 in the CBA/JxBALB/c mouse model. Hum Reprod. 2014;29:946–52.PubMedCrossRef Wang WJ, Liu FJ, Xin-Liu, Hao CF, Bao HC, Qu QL, Liu XM. Adoptive transfer of pregnancy-induced CD4+CD25+ regulatory T cells reverses the increase in abortion rate caused by interleukin 17 in the CBA/JxBALB/c mouse model. Hum Reprod. 2014;29:946–52.PubMedCrossRef
60.
go back to reference Ahn SH, Edwards AK, Singh SS, Young SL, Lessey BA, Tayade C. IL-17A contributes to the pathogenesis of endometriosis by triggering Proinflammatory cytokines and angiogenic growth factors. J Immunol. 2015;195:2591–600.PubMedCrossRef Ahn SH, Edwards AK, Singh SS, Young SL, Lessey BA, Tayade C. IL-17A contributes to the pathogenesis of endometriosis by triggering Proinflammatory cytokines and angiogenic growth factors. J Immunol. 2015;195:2591–600.PubMedCrossRef
61.
go back to reference Matson BC, Quinn KE, Lessey BA, Young SL, Caron KM. Elevated levels of adrenomedullin in eutopic endometrium and plasma from women with endometriosis. Fertil Steril. 2018;109:1072–8.PubMedPubMedCentralCrossRef Matson BC, Quinn KE, Lessey BA, Young SL, Caron KM. Elevated levels of adrenomedullin in eutopic endometrium and plasma from women with endometriosis. Fertil Steril. 2018;109:1072–8.PubMedPubMedCentralCrossRef
62.
go back to reference Volpato LK, Horewicz VV, Bobinski F, Martins DF, Piovezan AP. Annexin A1, FPR2/ALX, and inflammatory cytokine expression in peritoneal endometriosis. J Reprod Immunol. 2018;129:30–5.PubMedCrossRef Volpato LK, Horewicz VV, Bobinski F, Martins DF, Piovezan AP. Annexin A1, FPR2/ALX, and inflammatory cytokine expression in peritoneal endometriosis. J Reprod Immunol. 2018;129:30–5.PubMedCrossRef
63.
go back to reference Soni UK, Chadchan SB, Kumar V, Ubba V, Khan M, Vinod B, Konwar R, Bora HK, Rath SK, Sharma S, Jha RK. A high level of TGF-B1 promotes endometriosis development via cell migration, adhesiveness, colonization, and invasivenessdagger. Biol Reprod. 2019;100:917–38.PubMedCrossRef Soni UK, Chadchan SB, Kumar V, Ubba V, Khan M, Vinod B, Konwar R, Bora HK, Rath SK, Sharma S, Jha RK. A high level of TGF-B1 promotes endometriosis development via cell migration, adhesiveness, colonization, and invasivenessdagger. Biol Reprod. 2019;100:917–38.PubMedCrossRef
64.
go back to reference Choi HJ, Chung TW, Choi HJ, Han JH, Choi JH, Kim CH, Ha KT. Increased alpha2-6 sialylation of endometrial cells contributes to the development of endometriosis. Exp Mol Med. 2018;50:164.PubMedCentral Choi HJ, Chung TW, Choi HJ, Han JH, Choi JH, Kim CH, Ha KT. Increased alpha2-6 sialylation of endometrial cells contributes to the development of endometriosis. Exp Mol Med. 2018;50:164.PubMedCentral
65.
go back to reference Howard FM. Endometriosis and mechanisms of pelvic pain. J Minim Invasive Gynecol. 2009;16:540–50.PubMedCrossRef Howard FM. Endometriosis and mechanisms of pelvic pain. J Minim Invasive Gynecol. 2009;16:540–50.PubMedCrossRef
66.
go back to reference Peng Y, Ma J, Lin J. Activation of the CXCL16/CXCR6 Axis by TNF-alpha contributes to ectopic endometrial stromal cells migration and invasion. Reprod Sci. 2019;26:420–7.PubMedCrossRef Peng Y, Ma J, Lin J. Activation of the CXCL16/CXCR6 Axis by TNF-alpha contributes to ectopic endometrial stromal cells migration and invasion. Reprod Sci. 2019;26:420–7.PubMedCrossRef
67.
go back to reference Arosh JA, Lee J, Balasubbramanian D, Stanley JA, Long CR, Meagher MW, Osteen KG, Bruner-Tran KL, Burghardt RC, Starzinski-Powitz A, Banu SK. Molecular and preclinical basis to inhibit PGE2 receptors EP2 and EP4 as a novel nonsteroidal therapy for endometriosis. Proc Natl Acad Sci U S A. 2015;112:9716–21.PubMedPubMedCentralCrossRef Arosh JA, Lee J, Balasubbramanian D, Stanley JA, Long CR, Meagher MW, Osteen KG, Bruner-Tran KL, Burghardt RC, Starzinski-Powitz A, Banu SK. Molecular and preclinical basis to inhibit PGE2 receptors EP2 and EP4 as a novel nonsteroidal therapy for endometriosis. Proc Natl Acad Sci U S A. 2015;112:9716–21.PubMedPubMedCentralCrossRef
68.
go back to reference Chang HM, Wu HC, Sun ZG, Lian F, Leung P. Neurotrophins and glial cell line-derived neurotrophic factor in the ovary: physiological and pathophysiological implications. Hum Reprod Update. 2019;25:224–42.PubMedPubMedCentralCrossRef Chang HM, Wu HC, Sun ZG, Lian F, Leung P. Neurotrophins and glial cell line-derived neurotrophic factor in the ovary: physiological and pathophysiological implications. Hum Reprod Update. 2019;25:224–42.PubMedPubMedCentralCrossRef
69.
go back to reference Odagiri K, Konno R, Fujiwara H, Netsu S, Yang C, Suzuki M. Smooth muscle metaplasia and innervation in interstitium of endometriotic lesions related to pain. Fertil Steril. 2009;92:1525–31.PubMedCrossRef Odagiri K, Konno R, Fujiwara H, Netsu S, Yang C, Suzuki M. Smooth muscle metaplasia and innervation in interstitium of endometriotic lesions related to pain. Fertil Steril. 2009;92:1525–31.PubMedCrossRef
70.
go back to reference Mita S, Shimizu Y, Sato A, Notsu T, Imada K, Kyo S. Dienogest inhibits nerve growth factor expression induced by tumor necrosis factor-alpha or interleukin-1beta. Fertil Steril. 2014;101:595–601.PubMedCrossRef Mita S, Shimizu Y, Sato A, Notsu T, Imada K, Kyo S. Dienogest inhibits nerve growth factor expression induced by tumor necrosis factor-alpha or interleukin-1beta. Fertil Steril. 2014;101:595–601.PubMedCrossRef
71.
go back to reference Novella-Maestre E, Herraiz S, Vila-Vives JM, Carda C, Ruiz-Sauri A, Pellicer A. Effect of antiangiogenic treatment on peritoneal endometriosis-associated nerve fibers. Fertil Steril. 2012;98:1209–17.PubMedCrossRef Novella-Maestre E, Herraiz S, Vila-Vives JM, Carda C, Ruiz-Sauri A, Pellicer A. Effect of antiangiogenic treatment on peritoneal endometriosis-associated nerve fibers. Fertil Steril. 2012;98:1209–17.PubMedCrossRef
72.
go back to reference McKinnon B, Bersinger NA, Wotzkow C, Mueller MD. Endometriosis-associated nerve fibers, peritoneal fluid cytokine concentrations, and pain in endometriotic lesions from different locations. Fertil Steril. 2012;97:373–80.PubMedCrossRef McKinnon B, Bersinger NA, Wotzkow C, Mueller MD. Endometriosis-associated nerve fibers, peritoneal fluid cytokine concentrations, and pain in endometriotic lesions from different locations. Fertil Steril. 2012;97:373–80.PubMedCrossRef
73.
go back to reference Wang G, Tokushige N, Fraser IS. Nerve fibers and menstrual cycle in peritoneal endometriosis. Fertil Steril. 2011;95:2772–4.PubMedCrossRef Wang G, Tokushige N, Fraser IS. Nerve fibers and menstrual cycle in peritoneal endometriosis. Fertil Steril. 2011;95:2772–4.PubMedCrossRef
74.
go back to reference Kamimura K, Inoue R, Nagoya T, Sakai N, Goto R, Ko M, Niwa Y, Terai S. Autonomic nervous system network and liver regeneration. World J Gastroenterol. 2018;24:1616–21.PubMedPubMedCentralCrossRef Kamimura K, Inoue R, Nagoya T, Sakai N, Goto R, Ko M, Niwa Y, Terai S. Autonomic nervous system network and liver regeneration. World J Gastroenterol. 2018;24:1616–21.PubMedPubMedCentralCrossRef
75.
go back to reference Monica BM, Smith PG. Estrogen and female reproductive tract innervation: cellular and molecular mechanisms of autonomic neuroplasticity. Auton Neurosci. 2015;187:1–17.CrossRef Monica BM, Smith PG. Estrogen and female reproductive tract innervation: cellular and molecular mechanisms of autonomic neuroplasticity. Auton Neurosci. 2015;187:1–17.CrossRef
76.
go back to reference Kaelberer MM, Buchanan KL, Klein ME, Barth BB, Montoya MM, Shen X, Bohorquez DV. A gut-brain neural circuit for nutrient sensory transduction. Science. 2018;361(6408):eaat5236.PubMedPubMedCentralCrossRef Kaelberer MM, Buchanan KL, Klein ME, Barth BB, Montoya MM, Shen X, Bohorquez DV. A gut-brain neural circuit for nutrient sensory transduction. Science. 2018;361(6408):eaat5236.PubMedPubMedCentralCrossRef
77.
go back to reference Richeri A, Bianchimano P, Crutcher KA, Brauer MM. Reduced sympathetic neurite outgrowth on uterine tissue sections from rats treated with estrogen. Cell Tissue Res. 2010;340:287–301.PubMedCrossRef Richeri A, Bianchimano P, Crutcher KA, Brauer MM. Reduced sympathetic neurite outgrowth on uterine tissue sections from rats treated with estrogen. Cell Tissue Res. 2010;340:287–301.PubMedCrossRef
78.
go back to reference Liang Y, Yao S. Potential role of estrogen in maintaining the imbalanced sympathetic and sensory innervation in endometriosis. Mol Cell Endocrinol. 2016;424:42–9.PubMedCrossRef Liang Y, Yao S. Potential role of estrogen in maintaining the imbalanced sympathetic and sensory innervation in endometriosis. Mol Cell Endocrinol. 2016;424:42–9.PubMedCrossRef
79.
go back to reference Possover M, Tersiev P, Angelov DN. Comparative study of the neuropeptide-Y sympathetic nerves in endometriotic involved and noninvolved sacrouterine ligaments in women with pelvic endometriosis. J Minim Invasive Gynecol. 2009;16:340–3.PubMedCrossRef Possover M, Tersiev P, Angelov DN. Comparative study of the neuropeptide-Y sympathetic nerves in endometriotic involved and noninvolved sacrouterine ligaments in women with pelvic endometriosis. J Minim Invasive Gynecol. 2009;16:340–3.PubMedCrossRef
80.
go back to reference Rob L, Halaska M, Robova H. Nerve-sparing and individually tailored surgery for cervical cancer. Lancet Oncol. 2010;11:292–301.PubMedCrossRef Rob L, Halaska M, Robova H. Nerve-sparing and individually tailored surgery for cervical cancer. Lancet Oncol. 2010;11:292–301.PubMedCrossRef
81.
go back to reference Hollabaugh RJ, Steiner MS, Sellers KD, Samm BJ, Dmochowski RR. Neuroanatomy of the pelvis: implications for colonic and rectal resection. Dis Colon Rectum. 2000;43:1390–7.PubMedCrossRef Hollabaugh RJ, Steiner MS, Sellers KD, Samm BJ, Dmochowski RR. Neuroanatomy of the pelvis: implications for colonic and rectal resection. Dis Colon Rectum. 2000;43:1390–7.PubMedCrossRef
82.
go back to reference Shoja MM, Sharma A, Mirzayan N, Groat C, Watanabe K, Loukas M, Tubbs RS. Neuroanatomy of the female abdominopelvic region: a review with application to pelvic pain syndromes. Clin Anat. 2013;26:66–76.PubMedCrossRef Shoja MM, Sharma A, Mirzayan N, Groat C, Watanabe K, Loukas M, Tubbs RS. Neuroanatomy of the female abdominopelvic region: a review with application to pelvic pain syndromes. Clin Anat. 2013;26:66–76.PubMedCrossRef
83.
go back to reference Ricu M, Paredes A, Greiner M, Ojeda SR, Lara HE. Functional development of the ovarian noradrenergic innervation. Endocrinology. 2008;149:50–6.PubMedCrossRef Ricu M, Paredes A, Greiner M, Ojeda SR, Lara HE. Functional development of the ovarian noradrenergic innervation. Endocrinology. 2008;149:50–6.PubMedCrossRef
84.
go back to reference Zhu L, Huang Q, Huang X, Zhang J, Xu H, Zhang X. Decreased nerve fibers in the oviduct isthmus of women with endometriosis. Acta Histochem. 2014;116:871–7.PubMedCrossRef Zhu L, Huang Q, Huang X, Zhang J, Xu H, Zhang X. Decreased nerve fibers in the oviduct isthmus of women with endometriosis. Acta Histochem. 2014;116:871–7.PubMedCrossRef
85.
go back to reference Tokushige N, Russell P, Black K, Barrera H, Dubinovsky S, Markham R, Fraser IS. Nerve fibers in ovarian endometriomas. Fertil Steril. 2010;94:1944–7.PubMedCrossRef Tokushige N, Russell P, Black K, Barrera H, Dubinovsky S, Markham R, Fraser IS. Nerve fibers in ovarian endometriomas. Fertil Steril. 2010;94:1944–7.PubMedCrossRef
86.
go back to reference Liang Y, Liu D, Yang F, Pan W, Zeng F, Wu J, Xie H, Li J, Yao S. Perineural invasion in endometriotic lesions contributes to endometriosis-associated pain. J Pain Res. 2018;11:1999–2009.PubMedPubMedCentralCrossRef Liang Y, Liu D, Yang F, Pan W, Zeng F, Wu J, Xie H, Li J, Yao S. Perineural invasion in endometriotic lesions contributes to endometriosis-associated pain. J Pain Res. 2018;11:1999–2009.PubMedPubMedCentralCrossRef
87.
go back to reference Ianieri MM, Mautone D, Ceccaroni M. Recurrence in deep infiltrating endometriosis: a systematic review of the literature. J Minim Invasive Gynecol. 2018;25:786–93.PubMedCrossRef Ianieri MM, Mautone D, Ceccaroni M. Recurrence in deep infiltrating endometriosis: a systematic review of the literature. J Minim Invasive Gynecol. 2018;25:786–93.PubMedCrossRef
88.
go back to reference Kelm JA, Lancellotti CL, Donadio N, Auge AP, Lima SM, Aoki T, Ribeiro PA. Nerve fibers in uterosacral ligaments of women with deep infiltrating endometriosis. J Reprod Immunol. 2008;79:93–9.CrossRef Kelm JA, Lancellotti CL, Donadio N, Auge AP, Lima SM, Aoki T, Ribeiro PA. Nerve fibers in uterosacral ligaments of women with deep infiltrating endometriosis. J Reprod Immunol. 2008;79:93–9.CrossRef
89.
go back to reference A randomised controlled trial to assess the efficacy of laparoscopic uterosacral nerve ablation (LUNA) in the treatment of chronic pelvic pain: the trial protocol [ISRCTN41196151]. BMC Womens Health. 2003;3:6. A randomised controlled trial to assess the efficacy of laparoscopic uterosacral nerve ablation (LUNA) in the treatment of chronic pelvic pain: the trial protocol [ISRCTN41196151]. BMC Womens Health. 2003;3:6.
90.
go back to reference De Vadder F, Grasset E, Manneras HL, Karsenty G, Macpherson AJ, Olofsson LE, Backhed F. Gut microbiota regulates maturation of the adult enteric nervous system via enteric serotonin networks. Proc Natl Acad Sci U S A. 2018;115:6458–63.PubMedPubMedCentralCrossRef De Vadder F, Grasset E, Manneras HL, Karsenty G, Macpherson AJ, Olofsson LE, Backhed F. Gut microbiota regulates maturation of the adult enteric nervous system via enteric serotonin networks. Proc Natl Acad Sci U S A. 2018;115:6458–63.PubMedPubMedCentralCrossRef
91.
go back to reference Avetisyan M, Rood JE, Huerta LS, Sengupta R, Wright-Jin E, Dougherty JD, Behrens EM, Heuckeroth RO. Muscularis macrophage development in the absence of an enteric nervous system. Proc Natl Acad Sci U S A. 2018;115:4696–701.PubMedPubMedCentralCrossRef Avetisyan M, Rood JE, Huerta LS, Sengupta R, Wright-Jin E, Dougherty JD, Behrens EM, Heuckeroth RO. Muscularis macrophage development in the absence of an enteric nervous system. Proc Natl Acad Sci U S A. 2018;115:4696–701.PubMedPubMedCentralCrossRef
92.
93.
go back to reference Peng B, Zhan H, Alotaibi F, Alkusayer GM, Bedaiwy MA, Yong PJ. Nerve growth factor is associated with sexual pain in women with endometriosis. Reprod Sci. 2018;25:540–9.PubMedCrossRef Peng B, Zhan H, Alotaibi F, Alkusayer GM, Bedaiwy MA, Yong PJ. Nerve growth factor is associated with sexual pain in women with endometriosis. Reprod Sci. 2018;25:540–9.PubMedCrossRef
94.
go back to reference Merighi A, Salio C, Ghirri A, Lossi L, Ferrini F, Betelli C, Bardoni R. BDNF as a pain modulator. Prog Neurobiol. 2008;85:297–317.PubMedCrossRef Merighi A, Salio C, Ghirri A, Lossi L, Ferrini F, Betelli C, Bardoni R. BDNF as a pain modulator. Prog Neurobiol. 2008;85:297–317.PubMedCrossRef
95.
go back to reference Sikandar S, Minett MS, Millet Q, Santana-Varela S, Lau J, Wood JN, Zhao J. Brain-derived neurotrophic factor derived from sensory neurons plays a critical role in chronic pain. Brain. 2018;141:1028–39.PubMedPubMedCentralCrossRef Sikandar S, Minett MS, Millet Q, Santana-Varela S, Lau J, Wood JN, Zhao J. Brain-derived neurotrophic factor derived from sensory neurons plays a critical role in chronic pain. Brain. 2018;141:1028–39.PubMedPubMedCentralCrossRef
96.
go back to reference Ding S, Zhu T, Tian Y, Xu P, Chen Z, Huang X, Zhang X. Role of brain-derived neurotrophic factor in endometriosis pain. Reprod Sci. 2018;25:1045–57.PubMedCrossRef Ding S, Zhu T, Tian Y, Xu P, Chen Z, Huang X, Zhang X. Role of brain-derived neurotrophic factor in endometriosis pain. Reprod Sci. 2018;25:1045–57.PubMedCrossRef
97.
go back to reference Wessels JM, Kay VR, Leyland NA, Agarwal SK, Foster WG. Assessing brain-derived neurotrophic factor as a novel clinical marker of endometriosis. Fertil Steril. 2016;105:119–28.PubMedCrossRef Wessels JM, Kay VR, Leyland NA, Agarwal SK, Foster WG. Assessing brain-derived neurotrophic factor as a novel clinical marker of endometriosis. Fertil Steril. 2016;105:119–28.PubMedCrossRef
98.
go back to reference Bonaz B, Sinniger V, Pellissier S. The vagus nerve in the neuro-immune axis: implications in the pathology of the gastrointestinal tract. Front Immunol. 2017;8:1452.PubMedPubMedCentralCrossRef Bonaz B, Sinniger V, Pellissier S. The vagus nerve in the neuro-immune axis: implications in the pathology of the gastrointestinal tract. Front Immunol. 2017;8:1452.PubMedPubMedCentralCrossRef
99.
go back to reference Liang Y, Wang W, Huang J, Tan H, Liu T, Shang C, Liu D, Guo L, Yao S. Potential role of Semaphorin 3A and its receptors in regulating aberrant sympathetic innervation in peritoneal and deep infiltrating endometriosis. PLoS One. 2015;10:e146027. Liang Y, Wang W, Huang J, Tan H, Liu T, Shang C, Liu D, Guo L, Yao S. Potential role of Semaphorin 3A and its receptors in regulating aberrant sympathetic innervation in peritoneal and deep infiltrating endometriosis. PLoS One. 2015;10:e146027.
100.
go back to reference Bonaz B, Sinniger V, Pellissier S. Vagus nerve stimulation: a new promising therapeutic tool in inflammatory bowel disease. J Intern Med. 2017;282:46–63.PubMedCrossRef Bonaz B, Sinniger V, Pellissier S. Vagus nerve stimulation: a new promising therapeutic tool in inflammatory bowel disease. J Intern Med. 2017;282:46–63.PubMedCrossRef
101.
go back to reference Willemze RA, Welting O, van Hamersveld P, Verseijden C, Nijhuis LE, Hilbers FW, Meijer SL, Heesters BA, Folgering J, Darwinkel H, et al. Loss of intestinal sympathetic innervation elicits an innate immune driven colitis. Mol Med. 2019;25:1.PubMedPubMedCentralCrossRef Willemze RA, Welting O, van Hamersveld P, Verseijden C, Nijhuis LE, Hilbers FW, Meijer SL, Heesters BA, Folgering J, Darwinkel H, et al. Loss of intestinal sympathetic innervation elicits an innate immune driven colitis. Mol Med. 2019;25:1.PubMedPubMedCentralCrossRef
102.
go back to reference Straub RH, Grum F, Strauch U, Capellino S, Bataille F, Bleich A, Falk W, Scholmerich J, Obermeier F. Anti-inflammatory role of sympathetic nerves in chronic intestinal inflammation. Gut. 2008;57:911–21.PubMedCrossRef Straub RH, Grum F, Strauch U, Capellino S, Bataille F, Bleich A, Falk W, Scholmerich J, Obermeier F. Anti-inflammatory role of sympathetic nerves in chronic intestinal inflammation. Gut. 2008;57:911–21.PubMedCrossRef
103.
go back to reference Kunath J, Delaroque N, Szardenings M, Neundorf I, Straub RH. Sympathetic nerve repulsion inhibited by designer molecules in vitro and role in experimental arthritis. Life Sci. 2017;168:47–53.PubMedCrossRef Kunath J, Delaroque N, Szardenings M, Neundorf I, Straub RH. Sympathetic nerve repulsion inhibited by designer molecules in vitro and role in experimental arthritis. Life Sci. 2017;168:47–53.PubMedCrossRef
104.
go back to reference Taborsky GJ, Mei Q, Hackney DJ, Figlewicz DP, LeBoeuf R, Mundinger TO. Loss of islet sympathetic nerves and impairment of glucagon secretion in the NOD mouse: relationship to invasive insulitis. Diabetologia. 2009;52:2602–11.PubMedCrossRef Taborsky GJ, Mei Q, Hackney DJ, Figlewicz DP, LeBoeuf R, Mundinger TO. Loss of islet sympathetic nerves and impairment of glucagon secretion in the NOD mouse: relationship to invasive insulitis. Diabetologia. 2009;52:2602–11.PubMedCrossRef
107.
go back to reference Lee KK, Jharap B, Maser EA, Colombel JF. Impact of concomitant endometriosis on phenotype and natural history of inflammatory bowel disease. Inflamm Bowel Dis. 2016;22:159–63.PubMedCrossRef Lee KK, Jharap B, Maser EA, Colombel JF. Impact of concomitant endometriosis on phenotype and natural history of inflammatory bowel disease. Inflamm Bowel Dis. 2016;22:159–63.PubMedCrossRef
108.
go back to reference Ganesh T, Banik A, Dingledine R, Wang W, Amaradhi R. Peripherally restricted, highly potent, selective, aqueous-soluble EP2 antagonist with anti-inflammatory properties. Mol Pharm. 2018;15:5809–17.PubMedPubMedCentralCrossRef Ganesh T, Banik A, Dingledine R, Wang W, Amaradhi R. Peripherally restricted, highly potent, selective, aqueous-soluble EP2 antagonist with anti-inflammatory properties. Mol Pharm. 2018;15:5809–17.PubMedPubMedCentralCrossRef
109.
go back to reference Ribeiro-da-Silva M, Vasconcelos DM, Alencastre IS, Oliveira MJ, Linhares D, Neves N, Costa G, Henrique R, Lamghari M, Alves CJ. Interplay between sympathetic nervous system and inflammation in aseptic loosening of hip joint replacement. Sci Rep. 2018;8:16044.PubMedPubMedCentralCrossRef Ribeiro-da-Silva M, Vasconcelos DM, Alencastre IS, Oliveira MJ, Linhares D, Neves N, Costa G, Henrique R, Lamghari M, Alves CJ. Interplay between sympathetic nervous system and inflammation in aseptic loosening of hip joint replacement. Sci Rep. 2018;8:16044.PubMedPubMedCentralCrossRef
110.
go back to reference Weidler C, Holzer C, Harbuz M, Hofbauer R, Angele P, Scholmerich J, Straub RH. Low density of sympathetic nerve fibres and increased density of brain derived neurotrophic factor positive cells in RA synovium. Ann Rheum Dis. 2005;64:13–20.PubMedPubMedCentralCrossRef Weidler C, Holzer C, Harbuz M, Hofbauer R, Angele P, Scholmerich J, Straub RH. Low density of sympathetic nerve fibres and increased density of brain derived neurotrophic factor positive cells in RA synovium. Ann Rheum Dis. 2005;64:13–20.PubMedPubMedCentralCrossRef
111.
go back to reference Imdad A, Nicholson MR, Tanner-Smith EE, Zackular JP, Gomez-Duarte OG, Beaulieu DB, Acra S. Fecal transplantation for treatment of inflammatory bowel disease. Cochrane Database Syst Rev. 2018;11:D12774. Imdad A, Nicholson MR, Tanner-Smith EE, Zackular JP, Gomez-Duarte OG, Beaulieu DB, Acra S. Fecal transplantation for treatment of inflammatory bowel disease. Cochrane Database Syst Rev. 2018;11:D12774.
112.
go back to reference Bai A, Lu N, Guo Y, Chen J, Liu Z. Modulation of inflammatory response via alpha2-adrenoceptor blockade in acute murine colitis. Clin Exp Immunol. 2009;156:353–62.PubMedPubMedCentralCrossRef Bai A, Lu N, Guo Y, Chen J, Liu Z. Modulation of inflammatory response via alpha2-adrenoceptor blockade in acute murine colitis. Clin Exp Immunol. 2009;156:353–62.PubMedPubMedCentralCrossRef
113.
go back to reference Di Giovangiulio M, Verheijden S, Bosmans G, Stakenborg N, Boeckxstaens GE, Matteoli G. The neuromodulation of the intestinal immune system and its relevance in inflammatory bowel disease. Front Immunol. 2015;6:590.PubMedPubMedCentralCrossRef Di Giovangiulio M, Verheijden S, Bosmans G, Stakenborg N, Boeckxstaens GE, Matteoli G. The neuromodulation of the intestinal immune system and its relevance in inflammatory bowel disease. Front Immunol. 2015;6:590.PubMedPubMedCentralCrossRef
114.
go back to reference Moynes DM, Lucas GH, Beyak MJ, Lomax AE. Effects of inflammation on the innervation of the colon. Toxicol Pathol. 2014;42:111–7.PubMedCrossRef Moynes DM, Lucas GH, Beyak MJ, Lomax AE. Effects of inflammation on the innervation of the colon. Toxicol Pathol. 2014;42:111–7.PubMedCrossRef
115.
go back to reference Rubio A, Pellissier S, Picot A, Dantzer C, Bonaz B. The link between negative affect, vagal tone, and visceral sensitivity in quiescent Crohn's disease. Neurogastroenterol Motil. 2014;26:1200–3.PubMedCrossRef Rubio A, Pellissier S, Picot A, Dantzer C, Bonaz B. The link between negative affect, vagal tone, and visceral sensitivity in quiescent Crohn's disease. Neurogastroenterol Motil. 2014;26:1200–3.PubMedCrossRef
116.
go back to reference Pellissier S, Dantzer C, Canini F, Mathieu N, Bonaz B. Psychological adjustment and autonomic disturbances in inflammatory bowel diseases and irritable bowel syndrome. Psychoneuroendocrino. 2010;35:653–62.CrossRef Pellissier S, Dantzer C, Canini F, Mathieu N, Bonaz B. Psychological adjustment and autonomic disturbances in inflammatory bowel diseases and irritable bowel syndrome. Psychoneuroendocrino. 2010;35:653–62.CrossRef
117.
go back to reference Brzozowski B, Mazur-Bialy A, Pajdo R, Kwiecien S, Bilski J, Zwolinska-Wcislo M, Mach T, Brzozowski T. Mechanisms by which stress affects the experimental and clinical inflammatory bowel disease (IBD): role of brain-gut Axis. Curr Neuropharmacol. 2016;14:892–900.PubMedPubMedCentralCrossRef Brzozowski B, Mazur-Bialy A, Pajdo R, Kwiecien S, Bilski J, Zwolinska-Wcislo M, Mach T, Brzozowski T. Mechanisms by which stress affects the experimental and clinical inflammatory bowel disease (IBD): role of brain-gut Axis. Curr Neuropharmacol. 2016;14:892–900.PubMedPubMedCentralCrossRef
118.
go back to reference Pellissier S, Bonaz B. The place of stress and emotions in the irritable bowel syndrome. Vitam Horm. 2017;103:327–54.PubMedCrossRef Pellissier S, Bonaz B. The place of stress and emotions in the irritable bowel syndrome. Vitam Horm. 2017;103:327–54.PubMedCrossRef
119.
go back to reference Engel T, Ben-Horin S, Beer-Gabel M. Autonomic dysfunction correlates with clinical and inflammatory activity in patients with Crohn's disease. Inflamm Bowel Dis. 2015;21:2320–6.PubMed Engel T, Ben-Horin S, Beer-Gabel M. Autonomic dysfunction correlates with clinical and inflammatory activity in patients with Crohn's disease. Inflamm Bowel Dis. 2015;21:2320–6.PubMed
121.
go back to reference Boisse L, Chisholm SP, Lukewich MK, Lomax AE. Clinical and experimental evidence of sympathetic neural dysfunction during inflammatory bowel disease. Clin Exp Pharmacol Physiol. 2009;36:1026–33.PubMedCrossRef Boisse L, Chisholm SP, Lukewich MK, Lomax AE. Clinical and experimental evidence of sympathetic neural dysfunction during inflammatory bowel disease. Clin Exp Pharmacol Physiol. 2009;36:1026–33.PubMedCrossRef
122.
123.
go back to reference Weatherby KE, Zwilling BS, Lafuse WP. Resistance of macrophages to Mycobacterium avium is induced by alpha2-adrenergic stimulation. Infect Immun. 2003;71:22–9.PubMedPubMedCentralCrossRef Weatherby KE, Zwilling BS, Lafuse WP. Resistance of macrophages to Mycobacterium avium is induced by alpha2-adrenergic stimulation. Infect Immun. 2003;71:22–9.PubMedPubMedCentralCrossRef
124.
go back to reference Willemze RA, Luyer MD, Buurman WA, de Jonge WJ. Neural reflex pathways in intestinal inflammation: hypotheses to viable therapy. Nat Rev Gastroenterol Hepatol. 2015;12:353–62.PubMedCrossRef Willemze RA, Luyer MD, Buurman WA, de Jonge WJ. Neural reflex pathways in intestinal inflammation: hypotheses to viable therapy. Nat Rev Gastroenterol Hepatol. 2015;12:353–62.PubMedCrossRef
125.
go back to reference Noble BT, Brennan FH, Popovich PG. The spleen as a neuroimmune interface after spinal cord injury. J Neuroimmunol. 2018;321:1–11.PubMedCrossRef Noble BT, Brennan FH, Popovich PG. The spleen as a neuroimmune interface after spinal cord injury. J Neuroimmunol. 2018;321:1–11.PubMedCrossRef
126.
go back to reference Murray K, Godinez DR, Brust-Mascher I, Miller EN, Gareau MG, Reardon C. Neuroanatomy of the spleen: mapping the relationship between sympathetic neurons and lymphocytes. PLoS One. 2017;12:e182416. Murray K, Godinez DR, Brust-Mascher I, Miller EN, Gareau MG, Reardon C. Neuroanatomy of the spleen: mapping the relationship between sympathetic neurons and lymphocytes. PLoS One. 2017;12:e182416.
127.
go back to reference Jess T, Frisch M, Jorgensen KT, Pedersen BV, Nielsen NM. Increased risk of inflammatory bowel disease in women with endometriosis: a nationwide Danish cohort study. Gut. 2012;61:1279–83.PubMedCrossRef Jess T, Frisch M, Jorgensen KT, Pedersen BV, Nielsen NM. Increased risk of inflammatory bowel disease in women with endometriosis: a nationwide Danish cohort study. Gut. 2012;61:1279–83.PubMedCrossRef
128.
go back to reference Bonaz B, Sinniger V, Pellissier S. Anti-inflammatory properties of the vagus nerve: potential therapeutic implications of vagus nerve stimulation. J Physiol. 2016;594:5781–90.PubMedPubMedCentralCrossRef Bonaz B, Sinniger V, Pellissier S. Anti-inflammatory properties of the vagus nerve: potential therapeutic implications of vagus nerve stimulation. J Physiol. 2016;594:5781–90.PubMedPubMedCentralCrossRef
129.
go back to reference Spiller R, Major G. IBS and IBD—separate entities or on a spectrum? Nat Rev Gastroenterol Hepatol. 2016;13:613–21.PubMedCrossRef Spiller R, Major G. IBS and IBD—separate entities or on a spectrum? Nat Rev Gastroenterol Hepatol. 2016;13:613–21.PubMedCrossRef
130.
go back to reference Guerrero-Alba R, Valdez-Morales EE, Jimenez-Vargas NN, Lopez-Lopez C, Jaramillo-Polanco J, Okamoto T, Nasser Y, Bunnett NW, Lomax AE, Vanner SJ. Stress activates pronociceptive endogenous opioid signalling in DRG neurons during chronic colitis. Gut. 2017;66:2121–31.PubMedCrossRef Guerrero-Alba R, Valdez-Morales EE, Jimenez-Vargas NN, Lopez-Lopez C, Jaramillo-Polanco J, Okamoto T, Nasser Y, Bunnett NW, Lomax AE, Vanner SJ. Stress activates pronociceptive endogenous opioid signalling in DRG neurons during chronic colitis. Gut. 2017;66:2121–31.PubMedCrossRef
131.
go back to reference Herrmann M, Anders S, Straub RH, Jenei-Lanzl Z. TNF inhibits catecholamine production from induced sympathetic neuron-like cells in rheumatoid arthritis and osteoarthritis in vitro. Sci Rep. 2018;8:9645.PubMedPubMedCentralCrossRef Herrmann M, Anders S, Straub RH, Jenei-Lanzl Z. TNF inhibits catecholamine production from induced sympathetic neuron-like cells in rheumatoid arthritis and osteoarthritis in vitro. Sci Rep. 2018;8:9645.PubMedPubMedCentralCrossRef
132.
go back to reference Koopman FA, Tang MW, Vermeij J, de Hair MJ, Choi IY, Vervoordeldonk MJ, Gerlag DM, Karemaker JM, Tak PP. Autonomic dysfunction precedes development of rheumatoid arthritis: a prospective cohort study. Ebiomedicine. 2016;6:231–7.PubMedPubMedCentralCrossRef Koopman FA, Tang MW, Vermeij J, de Hair MJ, Choi IY, Vervoordeldonk MJ, Gerlag DM, Karemaker JM, Tak PP. Autonomic dysfunction precedes development of rheumatoid arthritis: a prospective cohort study. Ebiomedicine. 2016;6:231–7.PubMedPubMedCentralCrossRef
133.
go back to reference Jenei-Lanzl Z, Capellino S, Kees F, Fleck M, Lowin T, Straub RH. Anti-inflammatory effects of cell-based therapy with tyrosine hydroxylase-positive catecholaminergic cells in experimental arthritis. Ann Rheum Dis. 2015;74:444–51.PubMedCrossRef Jenei-Lanzl Z, Capellino S, Kees F, Fleck M, Lowin T, Straub RH. Anti-inflammatory effects of cell-based therapy with tyrosine hydroxylase-positive catecholaminergic cells in experimental arthritis. Ann Rheum Dis. 2015;74:444–51.PubMedCrossRef
134.
go back to reference Bellinger DL, Lorton D. Sympathetic nerve hyperactivity in the spleen: causal for nonpathogenic-driven chronic immune-mediated inflammatory diseases (IMIDs)? Int J Mol Sci. 2018;19(4):1188.PubMedCentralCrossRef Bellinger DL, Lorton D. Sympathetic nerve hyperactivity in the spleen: causal for nonpathogenic-driven chronic immune-mediated inflammatory diseases (IMIDs)? Int J Mol Sci. 2018;19(4):1188.PubMedCentralCrossRef
135.
go back to reference Liu Y, Rui XX, Shi H, Qiu YH, Peng YP. Norepinephrine inhibits Th17 cells via beta2-adrenergic receptor (beta2-AR) signaling in a mouse model of rheumatoid arthritis. Med Sci Monit. 2018;24:1196–204.PubMedPubMedCentralCrossRef Liu Y, Rui XX, Shi H, Qiu YH, Peng YP. Norepinephrine inhibits Th17 cells via beta2-adrenergic receptor (beta2-AR) signaling in a mouse model of rheumatoid arthritis. Med Sci Monit. 2018;24:1196–204.PubMedPubMedCentralCrossRef
136.
go back to reference Nackley AG, Tan KS, Fecho K, Flood P, Diatchenko L, Maixner W. Catechol-O-methyltransferase inhibition increases pain sensitivity through activation of both beta2- and beta3-adrenergic receptors. Pain. 2007;128:199–208.PubMedCrossRef Nackley AG, Tan KS, Fecho K, Flood P, Diatchenko L, Maixner W. Catechol-O-methyltransferase inhibition increases pain sensitivity through activation of both beta2- and beta3-adrenergic receptors. Pain. 2007;128:199–208.PubMedCrossRef
137.
go back to reference Harle P, Mobius D, Carr DJ, Scholmerich J, Straub RH. An opposing time-dependent immune-modulating effect of the sympathetic nervous system conferred by altering the cytokine profile in the local lymph nodes and spleen of mice with type II collagen-induced arthritis. Arthritis Rheum. 2005;52:1305–13.PubMedCrossRef Harle P, Mobius D, Carr DJ, Scholmerich J, Straub RH. An opposing time-dependent immune-modulating effect of the sympathetic nervous system conferred by altering the cytokine profile in the local lymph nodes and spleen of mice with type II collagen-induced arthritis. Arthritis Rheum. 2005;52:1305–13.PubMedCrossRef
138.
go back to reference Chen P, Wang DB, Liang YM. Evaluation of estrogen in endometriosis patients: regulation of GATA-3 in endometrial cells and effects on Th2 cytokines. J Obstet Gynaecol Res. 2016;42:669–77.PubMedCrossRef Chen P, Wang DB, Liang YM. Evaluation of estrogen in endometriosis patients: regulation of GATA-3 in endometrial cells and effects on Th2 cytokines. J Obstet Gynaecol Res. 2016;42:669–77.PubMedCrossRef
139.
go back to reference Greaves E, Temp J, Esnal-Zufiurre A, Mechsner S, Horne AW, Saunders PT. Estradiol is a critical mediator of macrophage-nerve cross talk in peritoneal endometriosis. Am J Pathol. 2015;185:2286–97.PubMedPubMedCentralCrossRef Greaves E, Temp J, Esnal-Zufiurre A, Mechsner S, Horne AW, Saunders PT. Estradiol is a critical mediator of macrophage-nerve cross talk in peritoneal endometriosis. Am J Pathol. 2015;185:2286–97.PubMedPubMedCentralCrossRef
140.
go back to reference Gou Y, Li X, Li P, Zhang H, Xu T, Wang H, Wang B, Ma X, Jiang X, Zhang Z. Estrogen receptor beta upregulates CCL2 via NF-kappaB signaling in endometriotic stromal cells and recruits macrophages to promote the pathogenesis of endometriosis. Hum Reprod. 2019;34:646–58.PubMedCrossRef Gou Y, Li X, Li P, Zhang H, Xu T, Wang H, Wang B, Ma X, Jiang X, Zhang Z. Estrogen receptor beta upregulates CCL2 via NF-kappaB signaling in endometriotic stromal cells and recruits macrophages to promote the pathogenesis of endometriosis. Hum Reprod. 2019;34:646–58.PubMedCrossRef
141.
go back to reference Krizsan-Agbas D, Pedchenko T, Hasan W, Smith PG. Oestrogen regulates sympathetic neurite outgrowth by modulating brain derived neurotrophic factor synthesis and release by the rodent uterus. Eur J Neurosci. 2003;18:2760–8.PubMedCrossRef Krizsan-Agbas D, Pedchenko T, Hasan W, Smith PG. Oestrogen regulates sympathetic neurite outgrowth by modulating brain derived neurotrophic factor synthesis and release by the rodent uterus. Eur J Neurosci. 2003;18:2760–8.PubMedCrossRef
142.
go back to reference Barcena DAM, Oldeweme J, Arnold J, Schneider A, Mechsner S. Remodeling of estrogen-dependent sympathetic nerve fibers seems to be disturbed in adenomyosis. Fertil Steril. 2013;100:801–9.CrossRef Barcena DAM, Oldeweme J, Arnold J, Schneider A, Mechsner S. Remodeling of estrogen-dependent sympathetic nerve fibers seems to be disturbed in adenomyosis. Fertil Steril. 2013;100:801–9.CrossRef
143.
go back to reference Martinez GF, Bianchimano P, Brauer MM. Estrogen-induced collagen reorientation correlates with sympathetic denervation of the rat myometrium. Auton Neurosci. 2016;201:32–9.PubMedCrossRef Martinez GF, Bianchimano P, Brauer MM. Estrogen-induced collagen reorientation correlates with sympathetic denervation of the rat myometrium. Auton Neurosci. 2016;201:32–9.PubMedCrossRef
144.
go back to reference Jana B, Meller KA, Czajkowska M, Calka J. Long-term estradiol-17beta exposure decreases the cholinergic innervation pattern of the pig ovary. Ann Anat. 2018;216:135–41.PubMedCrossRef Jana B, Meller KA, Czajkowska M, Calka J. Long-term estradiol-17beta exposure decreases the cholinergic innervation pattern of the pig ovary. Ann Anat. 2018;216:135–41.PubMedCrossRef
145.
147.
go back to reference Brown J, Crawford TJ, Allen C, Hopewell S, Prentice A. Nonsteroidal anti-inflammatory drugs for pain in women with endometriosis. Cochrane Database Syst Rev. 2017;1:D4753. Brown J, Crawford TJ, Allen C, Hopewell S, Prentice A. Nonsteroidal anti-inflammatory drugs for pain in women with endometriosis. Cochrane Database Syst Rev. 2017;1:D4753.
148.
go back to reference Baurle S, Nagel J, Peters O, Brauer N, Ter Laak A, Preusse C, Rottmann A, Heldmann D, Bothe U, Blume T, et al. Identification of a Benzimidazolecarboxylic acid derivative (BAY 1316957) as a potent and selective human prostaglandin E2 receptor subtype 4 (hEP4-R) antagonist for the treatment of endometriosis. J Med Chem. 2019;62:2541–63.PubMedCrossRef Baurle S, Nagel J, Peters O, Brauer N, Ter Laak A, Preusse C, Rottmann A, Heldmann D, Bothe U, Blume T, et al. Identification of a Benzimidazolecarboxylic acid derivative (BAY 1316957) as a potent and selective human prostaglandin E2 receptor subtype 4 (hEP4-R) antagonist for the treatment of endometriosis. J Med Chem. 2019;62:2541–63.PubMedCrossRef
149.
go back to reference Vercellini P, Vigano P, Somigliana E, Fedele L. Endometriosis: pathogenesis and treatment. Nat Rev Endocrinol. 2014;10:261–75.PubMedCrossRef Vercellini P, Vigano P, Somigliana E, Fedele L. Endometriosis: pathogenesis and treatment. Nat Rev Endocrinol. 2014;10:261–75.PubMedCrossRef
150.
go back to reference Vercellini P, Buggio L, Berlanda N, Barbara G, Somigliana E, Bosari S. Estrogen-progestins and progestins for the management of endometriosis. Fertil Steril. 2016;106:1552–71.PubMedCrossRef Vercellini P, Buggio L, Berlanda N, Barbara G, Somigliana E, Bosari S. Estrogen-progestins and progestins for the management of endometriosis. Fertil Steril. 2016;106:1552–71.PubMedCrossRef
151.
go back to reference Berlanda N, Somigliana E, Frattaruolo MP, Buggio L, Dridi D, Vercellini P. Surgery versus hormonal therapy for deep endometriosis: is it a choice of the physician? Eur J Obstet Gynecol Reprod Biol. 2017;209:67–71.PubMedCrossRef Berlanda N, Somigliana E, Frattaruolo MP, Buggio L, Dridi D, Vercellini P. Surgery versus hormonal therapy for deep endometriosis: is it a choice of the physician? Eur J Obstet Gynecol Reprod Biol. 2017;209:67–71.PubMedCrossRef
152.
go back to reference Lang J, Yu Q, Zhang S, Li H, Gude K, von Ludwig C, Ren X, Dong L. Dienogest for treatment of endometriosis in Chinese women: a placebo-controlled, randomized, double-blind phase 3 study. J Women's Health (Larchmt). 2018;27:148–55.CrossRef Lang J, Yu Q, Zhang S, Li H, Gude K, von Ludwig C, Ren X, Dong L. Dienogest for treatment of endometriosis in Chinese women: a placebo-controlled, randomized, double-blind phase 3 study. J Women's Health (Larchmt). 2018;27:148–55.CrossRef
153.
go back to reference Andres MP, Lopes LA, Baracat EC, Podgaec S. Dienogest in the treatment of endometriosis: systematic review. Arch Gynecol Obstet. 2015;292:523–9.CrossRef Andres MP, Lopes LA, Baracat EC, Podgaec S. Dienogest in the treatment of endometriosis: systematic review. Arch Gynecol Obstet. 2015;292:523–9.CrossRef
154.
go back to reference Tarjanne S, Ng C, Manconi F, Arola J, Mentula M, Maneck B, Fraser IS, Heikinheimo O. Use of hormonal therapy is associated with reduced nerve fiber density in deep infiltrating, rectovaginal endometriosis. Acta Obstet Gynecol Scand. 2015;94:693–700.PubMedCrossRef Tarjanne S, Ng C, Manconi F, Arola J, Mentula M, Maneck B, Fraser IS, Heikinheimo O. Use of hormonal therapy is associated with reduced nerve fiber density in deep infiltrating, rectovaginal endometriosis. Acta Obstet Gynecol Scand. 2015;94:693–700.PubMedCrossRef
155.
go back to reference Liao Z, Smith PG. Persistent genital hyperinnervation following progesterone administration to adolescent female rats. Biol Reprod. 2014;91:144.PubMedPubMedCentral Liao Z, Smith PG. Persistent genital hyperinnervation following progesterone administration to adolescent female rats. Biol Reprod. 2014;91:144.PubMedPubMedCentral
156.
go back to reference Dull AM, Moga MA, Dimienescu OG, Sechel G, Burtea V, Anastasiu CV. Therapeutic approaches of resveratrol on endometriosis via anti-inflammatory and anti-Angiogenic pathways. Molecules. 2019;24(4):667.PubMedCentralCrossRef Dull AM, Moga MA, Dimienescu OG, Sechel G, Burtea V, Anastasiu CV. Therapeutic approaches of resveratrol on endometriosis via anti-inflammatory and anti-Angiogenic pathways. Molecules. 2019;24(4):667.PubMedCentralCrossRef
157.
go back to reference Vercellini P, Frattaruolo MP, Rosati R, Dridi D, Roberto A, Mosconi P, De Giorgi O, Cribiu FM, Somigliana E. Medical treatment or surgery for colorectal endometriosis? Results of a shared decision-making approach. Hum Reprod. 2018;33:202–11.PubMedCrossRef Vercellini P, Frattaruolo MP, Rosati R, Dridi D, Roberto A, Mosconi P, De Giorgi O, Cribiu FM, Somigliana E. Medical treatment or surgery for colorectal endometriosis? Results of a shared decision-making approach. Hum Reprod. 2018;33:202–11.PubMedCrossRef
158.
go back to reference Wang Q, Sun X. Recent advances in nanomedicines for the treatment of rheumatoid arthritis. Biomater Sci. 2017;5:1407–20.PubMedCrossRef Wang Q, Sun X. Recent advances in nanomedicines for the treatment of rheumatoid arthritis. Biomater Sci. 2017;5:1407–20.PubMedCrossRef
159.
go back to reference Goenka L, George M, Sen M. A peek into the drug development scenario of endometriosis—a systematic review. Biomed Pharmacother. 2017;90:575–85.PubMedCrossRef Goenka L, George M, Sen M. A peek into the drug development scenario of endometriosis—a systematic review. Biomed Pharmacother. 2017;90:575–85.PubMedCrossRef
160.
go back to reference Pazhohan A, Amidi F, Akbari-Asbagh F, Seyedrezazadeh E, Aftabi Y, Abdolalizadeh J, Khodarahmian M, Khanlarkhani N, Sobhani A. Expression and shedding of CD44 in the endometrium of women with endometriosis and modulating effects of vitamin D: a randomized exploratory trial. J Steroid Biochem Mol Biol. 2018;178:150–8.PubMedCrossRef Pazhohan A, Amidi F, Akbari-Asbagh F, Seyedrezazadeh E, Aftabi Y, Abdolalizadeh J, Khodarahmian M, Khanlarkhani N, Sobhani A. Expression and shedding of CD44 in the endometrium of women with endometriosis and modulating effects of vitamin D: a randomized exploratory trial. J Steroid Biochem Mol Biol. 2018;178:150–8.PubMedCrossRef
161.
go back to reference Hasegawa A, Yoshino O, Osuga Y, Hirata T, Yano T, Taketani Y. High soluble CD44 concentration in peritoneal fluid in endometriosis. Fertil Steril. 2008;89:1267–8.PubMedCrossRef Hasegawa A, Yoshino O, Osuga Y, Hirata T, Yano T, Taketani Y. High soluble CD44 concentration in peritoneal fluid in endometriosis. Fertil Steril. 2008;89:1267–8.PubMedCrossRef
162.
go back to reference Koushik S, Joshi N, Nagaraju S, Mahmood S, Mudeenahally K, Padmavathy R, Jegatheesan SK, Mullangi R, Rajagopal S. PAD4: pathophysiology, current therapeutics and future perspective in rheumatoid arthritis. Expert Opin Ther Targets. 2017;21:433–47.PubMedCrossRef Koushik S, Joshi N, Nagaraju S, Mahmood S, Mudeenahally K, Padmavathy R, Jegatheesan SK, Mullangi R, Rajagopal S. PAD4: pathophysiology, current therapeutics and future perspective in rheumatoid arthritis. Expert Opin Ther Targets. 2017;21:433–47.PubMedCrossRef
164.
go back to reference Liang Y, Wu J, Wang W, Xie H, Yao S. Pro-endometriotic niche in endometriosis. Reprod BioMed Online. 2019;38:549–59.PubMedCrossRef Liang Y, Wu J, Wang W, Xie H, Yao S. Pro-endometriotic niche in endometriosis. Reprod BioMed Online. 2019;38:549–59.PubMedCrossRef
Metadata
Title
Autonomic nervous system and inflammation interaction in endometriosis-associated pain
Authors
Yajing Wei
Yanchun Liang
Haishan Lin
Yujing Dai
Shuzhong Yao
Publication date
01-12-2020
Publisher
BioMed Central
Published in
Journal of Neuroinflammation / Issue 1/2020
Electronic ISSN: 1742-2094
DOI
https://doi.org/10.1186/s12974-020-01752-1

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