Skip to main content
Top
Published in: Reproductive Biology and Endocrinology 1/2019

Open Access 01-12-2019 | Research

Endometrial TGF-β, IL-10, IL-17 and autophagy are dysregulated in women with recurrent implantation failure with chronic endometritis

Authors: Wen-juan Wang, Hong Zhang, Zhong-quan Chen, Wei Zhang, Xue-mei Liu, Jiang-ye Fang, Fu-jun Liu, Joanne Kwak-Kim

Published in: Reproductive Biology and Endocrinology | Issue 1/2019

Login to get access

Abstract

Background

Chronic endometritis (CE) is a condition which results in reduced receptivity of embryos by dysregulated lymphocyte subsets, abnormal expression of cytokines, chemokines and other regulatory molecules in the endometrium (EM). Macroautophagy (autophagy), the highly conserved cellular homeostasis pathway, plays an essential role in the development and function of T lymphocytes, and supports T cell lineage stability and survival fitness. The possible relationships between autophagy and local cytokine milieus in repeated implantation failure (RIF) with CE have not been elucidated yet.

Methods

This case-control study was performed at a large reproductive medicine center between February 2015 and July 2016. Seventy-five recurrent implantation falliure women with CE who had “strawberry aspect” and 75 women with male factor infertility were included. In this study, endometrial expressions of IL-17, IL-10, TGF-β and autophagy related molecules, including LC3-II and mTORC1 were investigated by qRT-PCR, Western blot, immunofluorescence and immunohistochemistry assays.

Results

The expression of IL-17 was significantly higher in patients with CE compared to women with male factor infertility, while the expressions of IL-10 and TGF-β were significantly lower. Moreover, the expression of autophagy (LC3-II) is increased, while the expression of mTORC1 was impaired.

Conclusions

CE is associated with shifted cytokine milieu towards Th17 over Treg immunity in endometrium through impaired autophagy by decreased mTORC1.
Literature
1.
go back to reference Coughlan C, Ledger W, Wang Q, Liu F, Demirol A, Gurgan T, Cutting R, Ong K, Sallam H, Li TC. Recurrent implantation failure: definition and management. Reprod BioMed Online. 2014;28:14–38.CrossRef Coughlan C, Ledger W, Wang Q, Liu F, Demirol A, Gurgan T, Cutting R, Ong K, Sallam H, Li TC. Recurrent implantation failure: definition and management. Reprod BioMed Online. 2014;28:14–38.CrossRef
2.
go back to reference Liu S, Diao L, Huang C, Li Y, Zeng Y, Kwak-Kim JYH. The role of decidual immune cells on human pregnancy. Reprod Immunol. 2017;124:44–53.CrossRef Liu S, Diao L, Huang C, Li Y, Zeng Y, Kwak-Kim JYH. The role of decidual immune cells on human pregnancy. Reprod Immunol. 2017;124:44–53.CrossRef
3.
go back to reference Dunk C, Smith S, Hazan A, Whittle W, Jones RL. Promotion of angiogenesis by human endometrial lymphocytes. Immunol Investig. 2008;37:583–610.CrossRef Dunk C, Smith S, Hazan A, Whittle W, Jones RL. Promotion of angiogenesis by human endometrial lymphocytes. Immunol Investig. 2008;37:583–610.CrossRef
4.
go back to reference Schatz F, Guzeloglu-Kayisli O, Arlier S, Kayisli UA, Lockwood CJ. The role of decidual cells in uterine hemostasis, menstruation, inflammation, adverse pregnancy outcomes and abnormal uterine bleeding. Hum Reprod Update. 2016;22:497–515.CrossRef Schatz F, Guzeloglu-Kayisli O, Arlier S, Kayisli UA, Lockwood CJ. The role of decidual cells in uterine hemostasis, menstruation, inflammation, adverse pregnancy outcomes and abnormal uterine bleeding. Hum Reprod Update. 2016;22:497–515.CrossRef
5.
go back to reference Maybin JA, Critchley HO, Jabbour HN. Inflammatory pathways in endometrial disorders. Mol Cell Endocrinol. 2011;335:42–51.CrossRef Maybin JA, Critchley HO, Jabbour HN. Inflammatory pathways in endometrial disorders. Mol Cell Endocrinol. 2011;335:42–51.CrossRef
6.
go back to reference Matteo M, Cicinelli E, Greco P, Massenzio F, Baldini D, Falagario T, Rosenberg P, Castellana L, Specchia G, Liso A. Abnormal pattern of lymphocyte subpopulations in the endometrium of infertile women with chronic endometritis. Am J Reprod Immunol. 2009;61:322–9.CrossRef Matteo M, Cicinelli E, Greco P, Massenzio F, Baldini D, Falagario T, Rosenberg P, Castellana L, Specchia G, Liso A. Abnormal pattern of lymphocyte subpopulations in the endometrium of infertile women with chronic endometritis. Am J Reprod Immunol. 2009;61:322–9.CrossRef
7.
go back to reference Di Pietro C, Cicinelli E, Guglielmino MR, Ragusa M, Farina M, Palumbo MA, Cianci A. Altered transcriptional regulation of cytokines, growth factors, and apoptotic proteins in the endometrium of infertile women with chronic endometritis. Am J Reprod Immunol. 2013;69:509–17.CrossRef Di Pietro C, Cicinelli E, Guglielmino MR, Ragusa M, Farina M, Palumbo MA, Cianci A. Altered transcriptional regulation of cytokines, growth factors, and apoptotic proteins in the endometrium of infertile women with chronic endometritis. Am J Reprod Immunol. 2013;69:509–17.CrossRef
8.
go back to reference Bouet PE, El Hachem H, Monceau E, Gariepy G, Kadoch IJ, Sylvestre C. Chronic endometritis in women with recurrent pregnancy loss and recurrent implantation failure: prevalence and role of office hysteroscopy and immunohistochemistry in diagnosis. Fertil Steril. 2016;105:106–10.CrossRef Bouet PE, El Hachem H, Monceau E, Gariepy G, Kadoch IJ, Sylvestre C. Chronic endometritis in women with recurrent pregnancy loss and recurrent implantation failure: prevalence and role of office hysteroscopy and immunohistochemistry in diagnosis. Fertil Steril. 2016;105:106–10.CrossRef
9.
go back to reference Park HJ, Kim YS, Yoon TK, Lee WS. Chronic endometritis and infertility. Clin Exp Reprod Med. 2016;43:185–92.CrossRef Park HJ, Kim YS, Yoon TK, Lee WS. Chronic endometritis and infertility. Clin Exp Reprod Med. 2016;43:185–92.CrossRef
10.
go back to reference Fontenot JD, Gavin MA, Rudensky AY. Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat Immunol. 2003;4:330–6.CrossRef Fontenot JD, Gavin MA, Rudensky AY. Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat Immunol. 2003;4:330–6.CrossRef
11.
go back to reference Khattri R, Cox T, Yasayko SA, Ramsdell F. An essential role for Scurfin in CD4+CD25+ T regulatory cells. Nat Immunol. 2003;4:337–42.CrossRef Khattri R, Cox T, Yasayko SA, Ramsdell F. An essential role for Scurfin in CD4+CD25+ T regulatory cells. Nat Immunol. 2003;4:337–42.CrossRef
12.
go back to reference Hori S, Nomura T, Sakaguchi S. Pillars. Control of regulatory T cell development by the transcription factor Foxp3. Science. 2003;299:1057–61.CrossRef Hori S, Nomura T, Sakaguchi S. Pillars. Control of regulatory T cell development by the transcription factor Foxp3. Science. 2003;299:1057–61.CrossRef
13.
go back to reference Thellin O, Coumans B, Zorzi W, Igout A, Heinen E. Tolerance to the foeto-placental ‘graft’: ten ways to support a child for nine months. Curr Opin Immunol. 2000;12:731–7.CrossRef Thellin O, Coumans B, Zorzi W, Igout A, Heinen E. Tolerance to the foeto-placental ‘graft’: ten ways to support a child for nine months. Curr Opin Immunol. 2000;12:731–7.CrossRef
14.
go back to reference Wang WJ, Hao CF, Qu QL, Wang X, Qiu LH, Lin QD. The deregulation of regulatory T cells on interleukin-17-producing T helper cells in patients with unexplained early recurrent miscarriage. Hum Reprod. 2010;25:2591–6.CrossRef Wang WJ, Hao CF, Qu QL, Wang X, Qiu LH, Lin QD. The deregulation of regulatory T cells on interleukin-17-producing T helper cells in patients with unexplained early recurrent miscarriage. Hum Reprod. 2010;25:2591–6.CrossRef
15.
go back to reference Wang WJ, Hao CF, Yi-Lin YGJ, Bao SH, Qiu LH, Lin QD. Increased prevalence of T helper 17 (Th17) cells in peripheral blood and decidua in unexplained recurrent spontaneous abortion patients. J Reprod Immunol. 2010;84:164–70.CrossRef Wang WJ, Hao CF, Yi-Lin YGJ, Bao SH, Qiu LH, Lin QD. Increased prevalence of T helper 17 (Th17) cells in peripheral blood and decidua in unexplained recurrent spontaneous abortion patients. J Reprod Immunol. 2010;84:164–70.CrossRef
16.
go back to reference Yang Z, Klionsky DJ. Eaten alive: a history of macroautophagy. Nat Cell Biol. 2010;12:814–22.CrossRef Yang Z, Klionsky DJ. Eaten alive: a history of macroautophagy. Nat Cell Biol. 2010;12:814–22.CrossRef
17.
go back to reference Mizushima N, Komatsu M. Autophagy: renovation of cells and tissues. Cell. 2011;147:728–41.CrossRef Mizushima N, Komatsu M. Autophagy: renovation of cells and tissues. Cell. 2011;147:728–41.CrossRef
18.
go back to reference Deretic V, Saitoh T, Akira S. Autophagy in infection, inflammation and immunity. Nat Rev Immunol. 2013;13:722–37.CrossRef Deretic V, Saitoh T, Akira S. Autophagy in infection, inflammation and immunity. Nat Rev Immunol. 2013;13:722–37.CrossRef
19.
go back to reference Wei J, Long L, Yang K, et al. Autophagy enforces functional integrity of regulatory T cells by coupling environmental cues and metabolic homeostasis. Nat Immunol. 2016;17:277–85.CrossRef Wei J, Long L, Yang K, et al. Autophagy enforces functional integrity of regulatory T cells by coupling environmental cues and metabolic homeostasis. Nat Immunol. 2016;17:277–85.CrossRef
20.
go back to reference Tsukamoto S, Kuma A, Murakami M, Kishi C, Yamamoto A, Mizushima N. Autophagy is essential for preimplantation development of mouse embryos. Science. 2008;321:117–20.CrossRef Tsukamoto S, Kuma A, Murakami M, Kishi C, Yamamoto A, Mizushima N. Autophagy is essential for preimplantation development of mouse embryos. Science. 2008;321:117–20.CrossRef
21.
go back to reference Avagliano L, Terraneo L, Virgili E, Martinelli C, Doi P, Samaja M, Bulfamante GP, Marconi AM. Autophagy in normal and abnormal early human pregnancies. Reprod Sci. 2015;22:838–44.CrossRef Avagliano L, Terraneo L, Virgili E, Martinelli C, Doi P, Samaja M, Bulfamante GP, Marconi AM. Autophagy in normal and abnormal early human pregnancies. Reprod Sci. 2015;22:838–44.CrossRef
22.
go back to reference Tanida I, Ueno T, Kominami E. LC3 and autophagy. Methods Mol Biol. 2008;445:77–88.CrossRef Tanida I, Ueno T, Kominami E. LC3 and autophagy. Methods Mol Biol. 2008;445:77–88.CrossRef
23.
go back to reference Noda T, Fujita N, Yoshimori T. The late stages of autophagy: how does the end begin? Cell Death Differ. 2009;16:984–90.CrossRef Noda T, Fujita N, Yoshimori T. The late stages of autophagy: how does the end begin? Cell Death Differ. 2009;16:984–90.CrossRef
24.
go back to reference Kim J, Kundu M, Viollet B, Guan KL. AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat Cell Biol. 2011;13:132–41.CrossRef Kim J, Kundu M, Viollet B, Guan KL. AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat Cell Biol. 2011;13:132–41.CrossRef
25.
go back to reference Jung CH, Ro SH, Cao J, Otto NM, Kim DH. mTOR regulation of autophagy. FEBS Lett. 2010;584:1287–95.CrossRef Jung CH, Ro SH, Cao J, Otto NM, Kim DH. mTOR regulation of autophagy. FEBS Lett. 2010;584:1287–95.CrossRef
26.
go back to reference Sengupta S, Peterson TR, Sabatini DM. Regulation of the mTOR complex 1 pathway by nutrients, growth factors, and stress. Mol Cell. 2010;40:310–22.CrossRef Sengupta S, Peterson TR, Sabatini DM. Regulation of the mTOR complex 1 pathway by nutrients, growth factors, and stress. Mol Cell. 2010;40:310–22.CrossRef
27.
go back to reference Wood SC, Seeley RJ, Cota D. Regulation of food intake through hypothalamic signaling networks involving mTOR. Annu Rev Nutr. 2008;28:295–331.CrossRef Wood SC, Seeley RJ, Cota D. Regulation of food intake through hypothalamic signaling networks involving mTOR. Annu Rev Nutr. 2008;28:295–331.CrossRef
28.
go back to reference Jansson N, Rosario FJ, Gaccioli F, Lager S, Jones HN, Roos S, Jansson T, Powell TL. Activation of placental mTOR signaling and amino acid transporters in obese women giving birth to large babies. J Clin Endocrinol Metab. 2013;98:105–13.CrossRef Jansson N, Rosario FJ, Gaccioli F, Lager S, Jones HN, Roos S, Jansson T, Powell TL. Activation of placental mTOR signaling and amino acid transporters in obese women giving birth to large babies. J Clin Endocrinol Metab. 2013;98:105–13.CrossRef
29.
go back to reference Resta L, Palumbo M, Rossi R, Piscitelli D, Grazia Fiore M, Cicinelli E. Histology of micro polyps in chronic endometritis. Histopathology. 2012;60:670–4.CrossRef Resta L, Palumbo M, Rossi R, Piscitelli D, Grazia Fiore M, Cicinelli E. Histology of micro polyps in chronic endometritis. Histopathology. 2012;60:670–4.CrossRef
30.
go back to reference Cicinelli E, Resta L, Nicoletti R, Zappimbulso V, Tartagni M, Saliani N. Endometrial micropolyps at fluid hysteroscopy suggest the existence of chronic endometritis. Hum Reprod. 2005;20:1386–9.CrossRef Cicinelli E, Resta L, Nicoletti R, Zappimbulso V, Tartagni M, Saliani N. Endometrial micropolyps at fluid hysteroscopy suggest the existence of chronic endometritis. Hum Reprod. 2005;20:1386–9.CrossRef
31.
go back to reference Cicinelli E, Resta L, Nicoletti R, Tartagni M, Marinaccio M, Bulletti C, Colafiglio G. Detection of chronic endometritis at fluid hysteroscopy. J Minim Invasive Gynecol. 2005;12:514–8.CrossRef Cicinelli E, Resta L, Nicoletti R, Tartagni M, Marinaccio M, Bulletti C, Colafiglio G. Detection of chronic endometritis at fluid hysteroscopy. J Minim Invasive Gynecol. 2005;12:514–8.CrossRef
32.
go back to reference Cicinelli E, De Ziegler D, Nicoletti R, Colafiglio G, Saliani N, Resta L, Rizzi D, De Vito D. Chronic endometritis: correlation among hysteroscopic, histologic, and bacteriologic findings in a prospective trial with 2190 consecutive office hysteroscopies. Fertil Steril. 2008;89:677–84.CrossRef Cicinelli E, De Ziegler D, Nicoletti R, Colafiglio G, Saliani N, Resta L, Rizzi D, De Vito D. Chronic endometritis: correlation among hysteroscopic, histologic, and bacteriologic findings in a prospective trial with 2190 consecutive office hysteroscopies. Fertil Steril. 2008;89:677–84.CrossRef
33.
go back to reference Kwak-Kim JY, Chung-Bang HS, Ng SC, Ntrivalas EI, Mangubat CP, Beaman KD, Beer AE, Gilman-Sachs A. Increased T helper 1 cytokine responses by circulating T cells are present in women with recurrent pregnancy losses and in infertile women with multiple implantation failures after IVF. Hum Reprod. 2003;18:767–73.CrossRef Kwak-Kim JY, Chung-Bang HS, Ng SC, Ntrivalas EI, Mangubat CP, Beaman KD, Beer AE, Gilman-Sachs A. Increased T helper 1 cytokine responses by circulating T cells are present in women with recurrent pregnancy losses and in infertile women with multiple implantation failures after IVF. Hum Reprod. 2003;18:767–73.CrossRef
34.
go back to reference Haggerty CL, Peipert JF, Weitzen S, Hendrix SL, Holley RL, Nelson DB, Randall H, Soper DE, Wiesenfeld HC, Ness RB. PID Evaluation and Clinical Health (PEACH) Study Investigators. Predictors of chronic pelvic pain in an urban population of women with symptoms and signs of pelvic inflammatory disease. Sex Transm Dis. 2005;32:293–9.CrossRef Haggerty CL, Peipert JF, Weitzen S, Hendrix SL, Holley RL, Nelson DB, Randall H, Soper DE, Wiesenfeld HC, Ness RB. PID Evaluation and Clinical Health (PEACH) Study Investigators. Predictors of chronic pelvic pain in an urban population of women with symptoms and signs of pelvic inflammatory disease. Sex Transm Dis. 2005;32:293–9.CrossRef
35.
go back to reference McQueen DB, Bernardi LA, Stephenson MD. Chronic endometritis in women with recurrent early pregnancy loss and/or fetal demise. Fertil Steril. 2014;101:1026–30.CrossRef McQueen DB, Bernardi LA, Stephenson MD. Chronic endometritis in women with recurrent early pregnancy loss and/or fetal demise. Fertil Steril. 2014;101:1026–30.CrossRef
36.
go back to reference Moser M, Murphy KM. Dendritic cell regulation of TH1-TH2 development. Nat Immunol. 2000;1:199–205.CrossRef Moser M, Murphy KM. Dendritic cell regulation of TH1-TH2 development. Nat Immunol. 2000;1:199–205.CrossRef
37.
go back to reference Reiner SL. Helper T cell differentiation, inside and out. Curr Opin Immunol. 2001;13:351–5.CrossRef Reiner SL. Helper T cell differentiation, inside and out. Curr Opin Immunol. 2001;13:351–5.CrossRef
38.
go back to reference Polese B, Gridelet V, Araklioti E, Martens H, Perrier d'Hauterive S, Geenen V. The Endocrine Milieu and CD4 T-Lymphocyte Polarization during Pregnancy. Front Endocrinol (Lausanne). 2014;5:106.CrossRef Polese B, Gridelet V, Araklioti E, Martens H, Perrier d'Hauterive S, Geenen V. The Endocrine Milieu and CD4 T-Lymphocyte Polarization during Pregnancy. Front Endocrinol (Lausanne). 2014;5:106.CrossRef
39.
go back to reference Zenclussen AC, Hämmerling GJ. Cellular Regulation of the Uterine Microenviroment That Enables Embryo Implantation. Front Immunol. 2015;6:321.CrossRef Zenclussen AC, Hämmerling GJ. Cellular Regulation of the Uterine Microenviroment That Enables Embryo Implantation. Front Immunol. 2015;6:321.CrossRef
40.
go back to reference Saxena D, Misra MK, Parveen F, Phadke SR, Agrawal S. The transcription factor Forkhead box P3 gene variants affect idiopathic recurrent pregnancy loss. Placenta. 2015;36:226–31.CrossRef Saxena D, Misra MK, Parveen F, Phadke SR, Agrawal S. The transcription factor Forkhead box P3 gene variants affect idiopathic recurrent pregnancy loss. Placenta. 2015;36:226–31.CrossRef
41.
go back to reference Wang WJ, Liu FJ, Xin-Liu HCF, 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/J x BALB/c mouse model. Hum Reprod. 2014;29:946–52.CrossRef Wang WJ, Liu FJ, Xin-Liu HCF, 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/J x BALB/c mouse model. Hum Reprod. 2014;29:946–52.CrossRef
42.
go back to reference Wang WJ, Liu FJ, Zhang X, Liu XM, Qu QL, Li FH, Zhuang LL, Li XX, Hao CF. Periodic elevation of regulatory T cells on the day of embryo transfer is associated with better in vitro fertilization outcome. J Reprod Immunol. 2017;119:49–53.CrossRef Wang WJ, Liu FJ, Zhang X, Liu XM, Qu QL, Li FH, Zhuang LL, Li XX, Hao CF. Periodic elevation of regulatory T cells on the day of embryo transfer is associated with better in vitro fertilization outcome. J Reprod Immunol. 2017;119:49–53.CrossRef
43.
go back to reference Kleinewietfeld M, Hafler DA. The plasticity of human Treg and Th17 cells and its role in autoimmunity. Semin Immunol. 2013;25:305–12.CrossRef Kleinewietfeld M, Hafler DA. The plasticity of human Treg and Th17 cells and its role in autoimmunity. Semin Immunol. 2013;25:305–12.CrossRef
44.
go back to reference Hirota K, Duarte JH, Veldhoen M, Hornsby E, Li Y, Cua DJ, Ahlfors H, Wilhelm C, Tolaini M, Menzel U, Garefalaki A, Potocnik AJ, Stockinger B. Fate mapping of IL-17-producing T cells in inflammatory responses. Nat Immunol. 2011;12:255–63.CrossRef Hirota K, Duarte JH, Veldhoen M, Hornsby E, Li Y, Cua DJ, Ahlfors H, Wilhelm C, Tolaini M, Menzel U, Garefalaki A, Potocnik AJ, Stockinger B. Fate mapping of IL-17-producing T cells in inflammatory responses. Nat Immunol. 2011;12:255–63.CrossRef
45.
go back to reference Wan YY, Flavell RA. Regulatory T-cell functions are subverted and converted owing to attenuated Foxp3 expression. Nature. 2007;445:766–70.CrossRef Wan YY, Flavell RA. Regulatory T-cell functions are subverted and converted owing to attenuated Foxp3 expression. Nature. 2007;445:766–70.CrossRef
46.
go back to reference Muranski P, Borman ZA, Kerkar SP, Klebanoff CA, Ji Y, Sanchez-Perez L, Sukumar M, Reger RN, Yu Z, Kern SJ, Roychoudhuri R, Ferreyra GA, Shen W, Durum SK, Feigenbaum L, Palmer DC, Antony PA, Chan CC, Laurence A, Danner RL, Gattinoni L, Restifo NP. Th17 cells are long lived and retain a stem cell-like molecular signature. Immunity. 2011;35:972–85.CrossRef Muranski P, Borman ZA, Kerkar SP, Klebanoff CA, Ji Y, Sanchez-Perez L, Sukumar M, Reger RN, Yu Z, Kern SJ, Roychoudhuri R, Ferreyra GA, Shen W, Durum SK, Feigenbaum L, Palmer DC, Antony PA, Chan CC, Laurence A, Danner RL, Gattinoni L, Restifo NP. Th17 cells are long lived and retain a stem cell-like molecular signature. Immunity. 2011;35:972–85.CrossRef
47.
go back to reference Komatsu N, Okamoto K, Sawa S, Nakashima T, Oh-hora M, Kodama T, Tanaka S, Bluestone JA, Takayanagi H. Pathogenic conversion of Foxp3+ T cells into TH17 cells in autoimmune arthritis. Nat Med. 2014;20:62–8.CrossRef Komatsu N, Okamoto K, Sawa S, Nakashima T, Oh-hora M, Kodama T, Tanaka S, Bluestone JA, Takayanagi H. Pathogenic conversion of Foxp3+ T cells into TH17 cells in autoimmune arthritis. Nat Med. 2014;20:62–8.CrossRef
48.
go back to reference Netea-Maier RT, Plantinga TS, van de Veerdonk FL, Smit JW, Netea MG. Modulation of inflammation by autophagy: consequences for human disease. Autophagy. 2016;12(2):245–60.CrossRef Netea-Maier RT, Plantinga TS, van de Veerdonk FL, Smit JW, Netea MG. Modulation of inflammation by autophagy: consequences for human disease. Autophagy. 2016;12(2):245–60.CrossRef
49.
go back to reference He C, Klionsky DJ. Regulation mechanisms and signaling pathways of autophagy. Annu Rev Genet. 2009;43:67–93.CrossRef He C, Klionsky DJ. Regulation mechanisms and signaling pathways of autophagy. Annu Rev Genet. 2009;43:67–93.CrossRef
50.
go back to reference Martinet W, De Meyer GR. Autophagy in atherosclerosis: a cell survival and death phenomenon with therapeutic potential. Circ Res. 2009;104:304–17.CrossRef Martinet W, De Meyer GR. Autophagy in atherosclerosis: a cell survival and death phenomenon with therapeutic potential. Circ Res. 2009;104:304–17.CrossRef
51.
go back to reference Nakashima A, Yamanaka-Tatematsu M, Fujita N, Koizumi K, Shima T, Yoshida T, Nikaido T, Okamoto A, Yoshimori T, Saito S. Impaired autophagy by soluble endoglin, under physiological hypoxia in early pregnant period, is involved in poor placentation in preeclampsia. Autophagy. 2013;9:303–16.CrossRef Nakashima A, Yamanaka-Tatematsu M, Fujita N, Koizumi K, Shima T, Yoshida T, Nikaido T, Okamoto A, Yoshimori T, Saito S. Impaired autophagy by soluble endoglin, under physiological hypoxia in early pregnant period, is involved in poor placentation in preeclampsia. Autophagy. 2013;9:303–16.CrossRef
52.
go back to reference Delgoffe GM, Pollizzi KN, Waickman AT, Heikamp E, Meyers DJ, Horton MR, Xiao B, Worley PF, Powell JD. The kinase mTOR regulates the differentiation of helper T cells through the selective activation of signaling by mTORC1 and mTORC2. Nat Immunol. 2011;12:295–303.CrossRef Delgoffe GM, Pollizzi KN, Waickman AT, Heikamp E, Meyers DJ, Horton MR, Xiao B, Worley PF, Powell JD. The kinase mTOR regulates the differentiation of helper T cells through the selective activation of signaling by mTORC1 and mTORC2. Nat Immunol. 2011;12:295–303.CrossRef
53.
go back to reference Zhang B, Fang L, Wu HM, Ding PS, Xu K, Liu R. Mer receptor tyrosine kinase negatively regulates lipoteichoic acid-induced inflammatory response via PI3K/Akt and SOCS3. Mol Immunol. 2016;76:98–107.CrossRef Zhang B, Fang L, Wu HM, Ding PS, Xu K, Liu R. Mer receptor tyrosine kinase negatively regulates lipoteichoic acid-induced inflammatory response via PI3K/Akt and SOCS3. Mol Immunol. 2016;76:98–107.CrossRef
54.
go back to reference Xu L, Brink M. mTOR, cardiomyocytes and inflammation in cardiac hypertrophy. Biochim Biophys Acta. 2016;1863(7 Pt B):1894–903.CrossRef Xu L, Brink M. mTOR, cardiomyocytes and inflammation in cardiac hypertrophy. Biochim Biophys Acta. 2016;1863(7 Pt B):1894–903.CrossRef
Metadata
Title
Endometrial TGF-β, IL-10, IL-17 and autophagy are dysregulated in women with recurrent implantation failure with chronic endometritis
Authors
Wen-juan Wang
Hong Zhang
Zhong-quan Chen
Wei Zhang
Xue-mei Liu
Jiang-ye Fang
Fu-jun Liu
Joanne Kwak-Kim
Publication date
01-12-2019
Publisher
BioMed Central
Published in
Reproductive Biology and Endocrinology / Issue 1/2019
Electronic ISSN: 1477-7827
DOI
https://doi.org/10.1186/s12958-018-0444-9

Other articles of this Issue 1/2019

Reproductive Biology and Endocrinology 1/2019 Go to the issue