MTA1-mediated transcriptional repression of Cox2 confers resistance against neutrophil infiltration in endometritis

MTA1-mediated transcriptional repression of Cox2 confers resistance against neutrophil infiltration in endometritis

  • Einenkel R, Zygmunt M, Muzzio DO. Microorganisms in the healthy upper reproductive tract: from denial to beneficial assignments for reproductive biology. Reprod Biol. 2019;19:113–8.

    Article 
    PubMed 

    Google Scholar
     

  • Gao H, Lu N, Chen Y, Li G, Li H, Chen I, et al. Endometrial microbiome during early pregnancy among women with and without chronic endometritis: a pilot study. Front Cell Infect Microbiol. 2025;15:1615182.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Li H, Liu L, Wang J, Zhao W. The emerging role of neutrophil extracellular traps in endometritis. Front Immunol. 2023;14:1153851.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kato T, Kitagawa S. Regulation of neutrophil functions by proinflammatory cytokines. Int J Hematol. 2006;84:205–9.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • McLoughlin RM, Witowski J, Robson RL, Wilkinson TS, Hurst SM, Williams AS, et al. Interplay between IFN-gamma and IL-6 signaling governs neutrophil trafficking and apoptosis during acute inflammation. J Clin Investig. 2003;112:598–607.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Liu K, Mao W, Liu B, Li T, Wang X, Pei L, et al. Prostaglandin E2 promotes staphylococcus aureus infection via EP4 receptor in bovine endometrium. Micro Pathog. 2021;158:105019.

    Article 
    CAS 

    Google Scholar
     

  • Li T, Liu B, Guan H, Mao W, Wang L, Zhang C, et al. PGE2 increases inflammatory damage in Escherichia coli-infected bovine endometrial tissue in vitro via the EP4-PKA signaling pathway. Biol Reprod. 2019;100:175–86.

    Article 
    PubMed 

    Google Scholar
     

  • Yang X, Zhang S, Liu B, Guo L, Gong P, Wu J, et al. Exogenous prostaglandin D(2) as a modulator in bovine endometritis: implications for reducing antibiotic use in dairy cattle. Front Vet Sci. 2025;12:1618203.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Johnson H, Torres CG, Carvallo F, Duchens M, Peralta OA. Endometrial expression of selected transcripts in postpartum of primiparous Holstein cows with clinical and subclinical endometritis. Anim Reprod Sci. 2015;156:34–9.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Herath S, Lilly ST, Santos NR, Gilbert RO, Goetze L, Bryant CE, et al. Expression of genes associated with immunity in the endometrium of cattle with disparate postpartum uterine disease and fertility. Reprod Biol Endocrinol. 2009;7:55.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Yi Y, Nie J, Liu X, Guo SW. Progressively diminished prostaglandin E2 signaling in concordance with increasing fibrosis in the Ectopic endometrium. Reprod Sci. 2025;32:1271–86.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Sakamoto R, Fujiwara T, Kawano Y, Aikawa S, Inazumi T, Nakayama O, et al. Uterine prostaglandin DP receptor, induced upon implantation, contributes to decidualization together with EP4 receptor. J Lipid Res. 2024;65:100636.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Sztachelska M, Ponikwicka-Tyszko D, Sokolowska G, Anisimowicz S, Czerniecki J, Lebiedzinska W, et al. Oxytocin antagonism reverses the effects of high oestrogen levels and oxytocin on decidualization and cyclooxygenase activity in endometrial tissues. Reprod Biomed Online. 2019;39:737–44.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Li W, Wu ZQ, Zhao J, Guo SJ, Li Z, Feng X, et al. Transient protection from heat-stress-induced apoptotic stimulation by metastasis-associated protein 1 in pachytene spermatocytes. PLoS ONE. 2011;6:e26013.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Sen N, Gui B, Kumar R. Physiological functions of MTA family of proteins. Cancer Metastasis Rev. 2014;33:869–77.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Pakala SB, Reddy SDN, Bui-Nguyen TM, Rangparia SS, Bommana A, Kumar R. MTA1 coregulator regulates LPS response via MyD88-dependent signaling. J Biol Chem. 2010;285:32787–92.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Chen JK, Wang WC, Zang L, Zhao J, Li W, Jiang T. Repression of a chromatin modifier aggravates lipopolysaccharide-induced acute lung injury in mouse. Biochem Biophys Res Commun. 2016;471:515–21.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Wang H, Dong BW, Zheng ZH, Wu ZB, Li W, Ding J. Metastasis-associated protein 1 (MTA1) signaling in rheumatoid synovium: regulation of inflammatory response and cytokine-mediated production of prostaglandin E2 (PGE2). Biochem Biophys Res Commun. 2016;473:442–8.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ghanta KS, Pakala SB, Reddy SD, Li DQ, Nair SS, Kumar R. MTA1 coregulation of transglutaminase 2 expression and function during inflammatory response. J Biol Chem. 2011;286:7132–8.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • D’Ippolito S, Tersigni C, Marana R, Di Nicuolo F, Gaglione R, Rossi ED, et al. Inflammosome in the human endometrium: further step in the evaluation of the “maternal side. Fertil Steril. 2016;105:111–8 e1-4.

    Article 
    PubMed 

    Google Scholar
     

  • Cicinelli E, De Ziegler D, Nicoletti R, Colafiglio G, Saliani N, Resta L, et al. Chronic endometritis: correlation among hysteroscopic, histologic, and bacteriologic findings in a prospective trial with 2190 consecutive office hysteroscopies. Fertil Steril. 2008;89:677–84.

    Article 
    PubMed 

    Google Scholar
     

  • Song D, Li TC, Zhang Y, Feng X, Xia E, Huang X, et al. Correlation between hysteroscopy findings and chronic endometritis. Fertil Steril. 2019;111:772–9.

    Article 
    PubMed 

    Google Scholar
     

  • Kobayashi R, Tajika Y, Kohmaru J, Morita S, Horii T, Mizukami Y, et al. The histone methyltransferase KMT2D is essential for embryo implantation via regulating the precise differentiation of endometrial cells. Cell Death Discov. 2024;10:357.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Yu Y, Mao N, Yu L, Lin F, Shi X, Lu X, et al. YiMu-QingGong san alleviates lipopolysaccharide-induced endometritis in mice via inhibiting inflammation and oxidative stress through regulating macrophage polarization. J Ethnopharmacol. 2025;337:118992.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Wu Y, Zhang J, Qin Y. S100A4 promotes the development of lipopolysaccharide-induced mouse endometritis. Biol Reprod. 2018;99:960–7.

    PubMed 

    Google Scholar
     

  • Na YR, Yoon YN, Son D, Jung D, Gu GJ, Seok SH. Consistent inhibition of cyclooxygenase drives macrophages towards the inflammatory phenotype. PLoS ONE. 2015;10:e0118203.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Shaukat A, Shaukat I, Rajput SA, Shukat R, Hanif S, Zhang X, et al. Ginsenoside Rb1 mitigates Escherichia coli lipopolysaccharide-induced endometritis through TLR4-mediated NF-kappaB pathway. Molecules 2021;26:7089.

  • OuYang Z, Hirota Y, Osuga Y, Hamasaki K, Hasegawa A, Tajima T, et al. Interleukin-4 stimulates the proliferation of endometriotic stromal cells. Am J Pathol. 2008;173:463–9.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Stadtmauer DJ, Wagner GP. Single-cell analysis of prostaglandin E2-induced human decidual cell in vitro differentiation: a minimal ancestral deciduogenic signal. Biol Reprod. 2022;106:155–72.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Doi-Tanaka Y, Tamura I, Shiroshita A, Fujimura T, Shirafuta Y, Maekawa R, et al. Differential gene expression in decidualized human endometrial stromal cells induced by different stimuli. Sci Rep. 2024;14:7726.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Xing X, Zhang G, Yi F, Xu X. Overexpression of USP22 ameliorates LPS-induced endometrial stromal cells inflammation and modulates cells decidualization by inhibiting ferroptosis. Reprod Biol. 2024;24:100913.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Makabe T, Koga K, Nagabukuro H, Asada M, Satake E, Taguchi A, et al. Use of selective PGE2 receptor antagonists on human endometriotic stromal cells and peritoneal macrophages. Mol Hum Reprod. 2021;27:gaaa077.

  • Shao Y, Luo Y, Sun Y, Jiang J, Li Z, Wang Z et al. Leonurine exerts anti-inflammatory effects in lipopolysaccharide (LPS)-induced endometritis by modulating mouse JAK-STAT/PI3K-Akt/PPAR signaling pathways. Genes. 2024;15:857.

  • Dong YS, Hou WG, Li Y, Liu DB, Hao GZ, Zhang HF, et al. Unexpected requirement for a binding partner of the syntaxin family in phagocytosis by murine testicular Sertoli cells. Cell Death Differ. 2016;23:787–800.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Jin X, Zhang S, Ding T, Zhao P, Zhang C, Zhang Y, et al. Testicular Lmcd1 regulates phagocytosis by Sertoli cells through modulation of NFAT1/Txlna signaling pathway. Aging Cell. 2020;19:e13217.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kitaya K, Yasuo T. Immunohistochemical and clinicopathological characterization of chronic endometritis. Am J Reprod Immunol. 2011;66:410–5.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Guo J, Chen L, Luo N, Li C, Chen R, Qu X, et al. LPS/TLR4-mediated stromal cells acquire an invasive phenotype and are implicated in the pathogenesis of adenomyosis. Sci Rep. 2016;6:21416.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zhang C, Lai JH, Hu B, Zhang S, Zhao J, Li W. A chromatin modifier regulates Sertoli cell response to mono-(2-ethylhexyl) phthalate (MEHP) via tissue inhibitor of metalloproteinase 2 (TIMP2) signaling. Biochim Biophys Acta. 2014;1839:1170–82.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Zhang S, Li W, Zhu C, Wang X, Li Z, Zhang J, et al. Sertoli cell-specific expression of metastasis-associated protein 2 (MTA2) is required for transcriptional regulation of the follicle-stimulating hormone receptor (FSHR) gene during spermatogenesis. J Biol Chem. 2012;287:40471–83.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Yu L, Su YS, Zhao J, Wang H, Li W. Repression of NR4A1 by a chromatin modifier promotes docetaxel resistance in PC-3 human prostate cancer cells. FEBS Lett. 2013;587:2542–51.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Wang J, Chitsaz F, Derbyshire MK, Gonzales NR, Gwadz M, Lu S, et al. The conserved domain database in 2023. Nucleic Acids Res. 2023;51:D384–D388.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Millard CJ, Fairall L, Schwabe JW. Towards an understanding of the structure and function of MTA1. Cancer Metastasis Rev. 2014;33:857–67.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Shang W, Xiao Z, Yu Z, Wei N, Zhao G, Zhang Q, et al. Chemical synthesis of the outer core oligosaccharide of Escherichia coli R3 and immunological evaluation. Org Biomol Chem. 2015;13:4321–30.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Li SY, Mi YH, Shen W, Hu XL, Zhang J, Nan F, et al. Two new xanthones from the twigs of Calophyllum membranaceum and their anti-inflammatory activities in HESC cells. Chem Biodivers. 2022;19:e202200355.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Shen W, Ma X, Shao D, Wu X, Wang S, Zheng J, et al. Neutrophil extracellular traps mediate bovine endometrial epithelial cell pyroptosis in dairy cows with endometritis. Int J Mol Sci. 2022;23:14013.

  • Zeindler J, Angehrn F, Droeser R, Daster S, Piscuoglio S, Ng CKY, et al. Infiltration by myeloperoxidase-positive neutrophils is an independent prognostic factor in breast cancer. Breast Cancer Res Treat. 2019;177:581–9.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Yang M, Liu S, Cai J, Sun X, Li C, Tan M, et al. Bile acids ameliorate lipopolysaccharide-induced endometritis in mice by inhibiting NLRP3 inflammasome activation. Life Sci. 2023;331:122062.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Li L, Qi J, Tao H, Wang L, Wang N, Huang Q. Protective effect of the total flavonoids from Clinopodium chinense against LPS-induced mice endometritis by inhibiting NLRP3 inflammasome-mediated pyroptosis. J Ethnopharmacol. 2023;312:116489.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Poloso NJ, Urquhart P, Nicolaou A, Wang J, Woodward DF. PGE2 differentially regulates monocyte-derived dendritic cell cytokine responses depending on receptor usage (EP2/EP4). Mol Immunol. 2013;54:284–95.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Jana B, Calka J, Bulc M, Witek K. Role of noradrenaline and adrenoreceptors in regulating prostaglandin E2 synthesis cascade in inflamed endometrium of pigs. Int J Mol Sci 2023;24:5856.

  • Frank GR, Brar AK, Cedars MI, Handwerger S. Prostaglandin E2 enhances human endometrial stromal cell differentiation. Endocrinology. 1994;134:258–63.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Peng-Fei H, Na AR, Hui C, Hong-Yu W, Jin-Shan C. Activation of alpha7 nicotinic acetylcholine receptor protects bovine endometrial tissue against LPS-induced inflammatory injury via JAK2/STAT3 pathway and COX-2 derived prostaglandin E(2). Eur J Pharmacol. 2021;900:174067.

    Article 
    PubMed 

    Google Scholar
     

  • Tsatsanis C, Androulidaki A, Venihaki M, Margioris AN. Signalling networks regulating cyclooxygenase-2. Int J Biochem Cell Biol. 2006;38:1654–61.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Liu J, Li C, Wang J, Xu D, Wang H, Wang T, et al. Chromatin modifier MTA1 regulates mitotic transition and tumorigenesis by orchestrating mitotic mRNA processing. Nat Commun. 2020;11:4455.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Li J, Wei J, Chen S, Wang X, Chen J, Zeng D, et al. Prevalence and risk factors for chronic endometritis in patients with adenomyosis and infertility: a retrospective cohort study. BMC Women’s Health. 2024;24:403.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Hirata T, Narumiya S. Prostanoids as regulators of innate and adaptive immunity. Adv Immunol. 2012;116:143–74.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Lara E, Rivera N, Cabezas J, Navarrete F, Saravia F, Rodríguez-Álvarez L et al. Endometrial stem cells in farm animals: potential role in uterine physiology and pathology. Bioengineering. 2018;5:75.

  • Mason KL, Rogers LM, Soares EM, Bani-Hashemi T, Erb Downward J, Agnew D, et al. Intrauterine group A streptococcal infections are exacerbated by prostaglandin E2. J Immunol. 2013;191:2457–65.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Banu SK, Lee J, Speights VO Jr., Starzinski-Powitz A, Arosh JA. Selective inhibition of prostaglandin E2 receptors EP2 and EP4 induces apoptosis of human endometriotic cells through suppression of ERK1/2, AKT, NFkappaB, and beta-catenin pathways and activation of intrinsic apoptotic mechanisms. Mol Endocrinol. 2009;23:1291–305.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Nishimura T, Zhao X, Gan H, Koyasu S, Remold HG. The prostaglandin E2 receptor EP4 is integral to a positive feedback loop for prostaglandin E2 production in human macrophages infected with Mycobacterium tuberculosis. FASEB J. 2013;27:3827–36.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Cheng H, Huang H, Guo Z, Chang Y, Li Z. Role of prostaglandin E2 in tissue repair and regeneration. Theranostics. 2021;11:8836–54.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Mitacek MCG, Praderio RG, Stornelli MC, de la Sota RL, Stornelli MA. Endometritis in the bitch: immunohistochemical localization of cyclooxygenase 2. Open Vet J. 2020;10:157–63.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Park YK, Hong H, Jang BC. Transcriptional and translational regulation of COX-2 expression by cadmium in C6 glioma cells. Int J Mol Med. 2012;30:960–6.

    Article 
    CAS 
    PubMed 

    Google Scholar