A positive COX-2/IL-1β loop promotes decidualization by upregulating CD82

in Reproduction
View More View Less
  • 1 Affiliated Maternity and Child Health Care Hospital of Nantong University, Nantong, People’s Republic of China
  • | 2 Laboratory for Reproductive Immunology, NHC Key Lab of Reproduction Regulation (Shanghai Institute of Planned Parenthood Research), Hospital of Obstetrics and Gynecology, Fudan University, Shanghai, People’s Republic of China
  • | 3 Clinical Epidemiology, Hospital of Obstetrics and Gynecology, Fudan University, Shanghai, People’s Republic of China
  • | 4 Department of Gynecology, Changzhou No. 2 People’s Hospital, affiliated with Nanjing Medical University, Changzhou, Jiangsu Province, People’s Republic of China
  • | 5 Shanghai Key Laboratory of Female Reproductive Endocrine Related Diseases, Hospital of Obstetrics and Gynecology, Fudan University, Shanghai, People’s Republic of China

Correspondence should be addressed to X-F Tan or L-B Liu or M-Q Li; Email: txf15@163.com or llb0704@yahoo.com or mqli@fudan.edu.cn

*(Q-C Qu and H-H Shen contributed equally to this work)

Restricted access

A successful pregnancy requires sufficient decidualization of endometrial stromal cells (ESCs). CD82, a metastasis suppressor, is a critical regulator for trophoblast invasion but the effect in decidualization was largely unknown. Here we reported that there was a high level of CD82 in DSC by the immunohistochemistry staining and flow cytometer analysis. Stimulation with prostaglandin E2 (PGE2) elevated the expression of CD82 in ESCs. In contrast, celecoxib, a selective COX-2 inhibitor, significantly downregulated the expression of CD82 in decidual stromal cells (DSCs). Bioinformatics analysis and further research showed that recombinant human interleukin (IL)-1β protein (rhIL-1β) upregulated CD82 in ESCs. Of note, blocking IL-1β signaling with anti-human IL-1β neutralizing antibody could reverse the stimulatory effect of PGE2 on CD82 in ESCs. Silencing CD82 resulted in the decease of the decidualization markers PRL and IGFBP1 mRNA levels in DSCs. More importantly, we observed rhIL-1β also upregulated the expression of COX-2, and the upregulation of PRL and IGFBP1 induced by rhIL-1β could be abolished by celecoxib in ESCs or CD82 deficiency in DSCs. This study suggests that CD82 should be a novel promotor for decidualization under a positive regulation of the COX-2/PGE2/IL-1β positive feedback loop.

 

     An official journal of

    Society for Reproduction and Fertility

 

Sept 2018 onwards Past Year Past 30 Days
Abstract Views 853 853 242
Full Text Views 38 39 2
PDF Downloads 48 48 3
  • Baek SH, Ohgi KA, Rose DW, Koo EH, Glass CK & Rosenfeld MG 2002 Exchange of N-CoR corepressor and Tip60 coactivator complexes links gene expression by NF-kappaB and beta-amyloid precursor protein. Cell 110 5567. (https://doi.org/10.1016/s0092-8674(0200809-7)

    • Search Google Scholar
    • Export Citation
  • Brosens JJ, Hayashi N & White JO 1999 Progesterone receptor regulates decidual prolactin expression in differentiating human endometrial stromal cells. Endocrinology 140 480948 20. (https://doi.org/10.1210/endo.140.10.7070)

    • Search Google Scholar
    • Export Citation
  • Brosens I, Puttemans P & Benagiano G 2019 Placental bed research: I. The placental bed: from spiral arteries remodeling to the great obstetrical syndromes. American Journal of Obstetrics and Gynecology 221 437456. (https://doi.org/10.1016/j.ajog.2019.05.044)

    • Search Google Scholar
    • Export Citation
  • Cha J, Sun X & Dey SK 2012 Mechanisms of implantation: strategies for successful pregnancy. Nature Medicine 18 175417 67. (https://doi.org/10.1038/nm.3012)

    • Search Google Scholar
    • Export Citation
  • Cho W & Choe J 2020 Prostaglandin E2 stimulates COX-2 expression via mitogen-activated protein kinase p38 but not ERK in human follicular dendritic cell-like cells. BMC Immunology 21 20. (https://doi.org/10.1186/s12865-020-00347-y)

    • Search Google Scholar
    • Export Citation
  • Erkenbrack EM, Maziarz JD, Griffith OW, Liang C, Chavan AR, Nnamani MC & Wagner GP 2018 The mammalian decidual cell evolved from a cellular stress response. PLoS Biology 16 e2005594. (https://doi.org/10.1371/journal.pbio.2005594)

    • Search Google Scholar
    • Export Citation
  • Fiebich BL, Mueksch B, Boehringer M & Hull M 2000 Interleukin-1beta induces cyclooxygenase-2 and prostaglandin E(2) synthesis in human neuroblastoma cells: involvement of p38 mitogen-activated protein kinase and nuclear factor-kappaB. Journal of Neurochemistry 75 2020202 8. (https://doi.org/10.1046/j.1471-4159.2000.0752020.x)

    • Search Google Scholar
    • Export Citation
  • Fitzgerald JS, Poehlmann TG, Schleussner E & Markert UR 2008 Trophoblast invasion: the role of intracellular cytokine signalling via signal transducer and activator of transcription 3 (STAT3). Human Reproduction Update 14 3353 44. (https://doi.org/10.1093/humupd/dmn010)

    • Search Google Scholar
    • Export Citation
  • Frank GR, Brar AK, Cedars MI & Handwerger S 1994 Prostaglandin E2 enhances human endometrial stromal cell differentiation. Endocrinology 134 2582 63. (https://doi.org/10.1210/endo.134.1.7506205)

    • Search Google Scholar
    • Export Citation
  • Frank GR, Brar AK, Jikihara H, Cedars MI & Handwerger S 1995 Interleukin-1 beta and the endometrium: an inhibitor of stromal cell differentiation and possible autoregulator of decidualization in humans. Biology of Reproduction 52 1841 91. (https://doi.org/10.1095/biolreprod52.1.184)

    • Search Google Scholar
    • Export Citation
  • Garrido-Gomez T, Dominguez F, Quinonero A, Diaz-Gimeno P, Kapidzic M, Gormley M, Ona K, Padilla-Iserte P, McMaster M & Genbacev O et al.2017 Defective decidualization during and after severe preeclampsia reveals a possible maternal contribution to the etiology. PNAS 114 E8468E8477. (https://doi.org/10.1073/pnas.1706546114)

    • Search Google Scholar
    • Export Citation
  • Gellersen B & Brosens JJ 2014 Cyclic decidualization of the human endometrium in reproductive health and failure. Endocrine Reviews 35 851905. (https://doi.org/10.1210/er.2014-1045)

    • Search Google Scholar
    • Export Citation
  • Gellersen B, Briese J, Oberndorfer M, Redlin K, Samalecos A, Richter DU, Loning T, Schulte HM & Bamberger AM 2007 Expression of the metastasis suppressor KAI1 in decidual cells at the human maternal-fetal interface: regulation and functional implications. American Journal of Pathology 170 1261 39. (https://doi.org/10.2353/ajpath.2007.060175)

    • Search Google Scholar
    • Export Citation
  • Gellersen B, Wolf A, Kruse M, Schwenke M & Bamberger AM 2013 Human endometrial stromal cell-trophoblast interactions: mutual stimulation of chemotactic migration and promigratory roles of cell surface molecules CD82 and CEACAM1. Biology of Reproduction 88 80. (https://doi.org/10.1095/biolreprod.112.106724)

    • Search Google Scholar
    • Export Citation
  • Gonzalez M, Neufeld J, Reimann K, Wittmann S, Samalecos A, Wolf A, Bamberger AM & Gellersen B 2011 Expansion of human trophoblastic spheroids is promoted by decidualized endometrial stromal cells and enhanced by heparin-binding epidermal growth factor-like growth factor and interleukin-1 beta. Molecular Human Reproduction 17 4214 33. (https://doi.org/10.1093/molehr/gar015)

    • Search Google Scholar
    • Export Citation
  • Han SW, Lei ZM & Rao CV 1996 Up-regulation of cyclooxygenase-2 gene expression by chorionic gonadotropin in mucosal cells from human fallopian tubes. Endocrinology 137 292929 37. (https://doi.org/10.1210/endo.137.7.8770916)

    • Search Google Scholar
    • Export Citation
  • Huang JC, Liu DY, Yadollahi S, Wu KK & Dawood MY 1998 Interleukin-1 beta induces cyclooxygenase-2 gene expression in cultured endometrial stromal cells. Journal of Clinical Endocrinology and Metabolism 83 5385 41. (https://doi.org/10.1210/jcem.83.2.4533)

    • Search Google Scholar
    • Export Citation
  • Ishihara O, Matsuoka K, Kinoshita K, Sullivan MH & Elder MG 1995 Interleukin-1 beta-stimulated PGE2 production from early first trimester human decidual cells is inhibited by dexamethasone and progesterone. Prostaglandins 49 1526. (https://doi.org/10.1016/0090-6980(9400009-l)

    • Search Google Scholar
    • Export Citation
  • Kang J, Chapdelaine P, Laberge PY & Fortier MA 2006 Functional characterization of prostaglandin transporter and terminal prostaglandin synthases during decidualization of human endometrial stromal cells. Human Reproduction 21 59259 9. (https://doi.org/10.1093/humrep/dei400)

    • Search Google Scholar
    • Export Citation
  • Kaufmann P, Black S & Huppertz B 2003 Endovascular trophoblast invasion: implications for the pathogenesis of intrauterine growth retardation and preeclampsia. Biology of Reproduction 69 17. (https://doi.org/10.1095/biolreprod.102.014977)

    • Search Google Scholar
    • Export Citation
  • Kaya Okur HS, Das A, Taylor RN, Bagchi IC & Bagchi MK 2016 Roles of estrogen receptor-alpha and the coactivator MED1 during human endometrial decidualization. Molecular Endocrinology 30 3023 13. (https://doi.org/10.1210/me.2015-1274)

    • Search Google Scholar
    • Export Citation
  • Kelleher AM, Milano-Foster J, Behura SK & Spencer TE 2018 Uterine glands coordinate on-time embryo implantation and impact endometrial decidualization for pregnancy success. Nature Communications 9 2435. (https://doi.org/10.1038/s41467-018-04848-8)

    • Search Google Scholar
    • Export Citation
  • Kniss DA, Zimmerman PD, Garver CL & Fertel RH 1997 Interleukin-1 receptor antagonist blocks interleukin-1-induced expression of cyclooxygenase-2 in endometrium. American Journal of Obstetrics and Gynecology 177 5595 67. (https://doi.org/10.1016/s0002-9378(9770146-7)

    • Search Google Scholar
    • Export Citation
  • Li MQ, Hou XF, Shao J, Tang CL & Li DJ 2010 The DSCs-expressed CD82 controls the invasiveness of trophoblast cells via integrinbeta1/MAPK/MAPK3/1 signaling pathway in human first-trimester pregnancy. Biology of Reproduction 82 9689 79. (https://doi.org/10.1095/biolreprod.109.080739)

    • Search Google Scholar
    • Export Citation
  • Librach CL, Feigenbaum SL, Bass KE, Cui TY, Verastas N, Sadovsky Y, Quigley JP, French DL & Fisher SJ 1994 Interleukin-1 beta regulates human cytotrophoblast metalloproteinase activity and invasion in vitro. Journal of Biological Chemistry 269 17125171 31. (https://doi.org/10.1016/S0021-9258(1732529-2)

    • Search Google Scholar
    • Export Citation
  • Lim H, Paria BC, Das SK, Dinchuk JE, Langenbach R, Trzaskos JM & Dey SK 1997 Multiple female reproductive failures in cyclooxygenase 2-deficient mice. Cell 91 197208. (https://doi.org/10.1016/s0092-8674(0080402-x)

    • Search Google Scholar
    • Export Citation
  • Liu XT, Sun HT, Zhang ZF, Shi RX, Liu LB, Yu JJ, Zhou WJ, Gu CJ, Yang SL & Liu YK et al.2018 Indoleamine 2,3-dioxygenase suppresses the cytotoxicity of 1 NK cells in response to ectopic endometrial stromal cells in endometriosis. Reproduction 156 397404. (https://doi.org/10.1530/REP-18-0112)

    • Search Google Scholar
    • Export Citation
  • Liu X, Guo X, Li H, Chen J & Han H 2021 Effects of KAI gene expression on ferroptosis in pancreatic cancer cells. Molecular Medicine Reports 23 163. (https://doi.org/10.3892/mmr.2020.11802)

    • Search Google Scholar
    • Export Citation
  • Long Y, Jiang Y, Zeng J, Dang Y, Chen Y, Lin J, Wei H, Xia H, Long J & Luo C et al.2020 The expression and biological function of chemokine CXCL12 and receptor CXCR4/CXCR7 in placenta accreta spectrum disorders. Journal of Cellular and Molecular Medicine 24 31673182. (https://doi.org/10.1111/jcmm.14990)

    • Search Google Scholar
    • Export Citation
  • Lu H, Jin LP, Huang HL, Ha SY, Yang HL, Chang RQ, Li DJ & Li MQ 2020 Trophoblast-derived CXCL12 promotes CD56(bright) CD82(-) CD29(+) NK cell enrichment in the decidua. American Journal of Reproductive Immunology 83 e13203. (https://doi.org/10.1111/aji.13203)

    • Search Google Scholar
    • Export Citation
  • Ma X, He X, Wang C, Huang X, Li Y & Ma K 2021 Small extracellular ring domain is necessary for CD82/KAI1’anti-metastasis function. Biochemical and Biophysical Research Communications 557 110116. (https://doi.org/10.1016/j.bbrc.2021.04.001)

    • Search Google Scholar
    • Export Citation
  • Mak VC, Wong OG, Siu MK, Wong ES, Ng WY, Wong RW, Chan KK, Ngan HY & Cheung AN 2015 FBI-1 is overexpressed in gestational trophoblastic disease and promotes tumor growth and cell aggressiveness of choriocarcinoma via PI3K/Akt signaling. American Journal of Pathology 185 203820 48. (https://doi.org/10.1016/j.ajpath.2015.03.011)

    • Search Google Scholar
    • Export Citation
  • Massimiani M, Lacconi V, La Civita F, Ticconi C, Rago R & Campagnolo L 2019 Molecular signaling regulating endometrium-blastocyst crosstalk. International Journal of Molecular Sciences 21 2 3. (https://doi.org/10.3390/ijms21010023)

    • Search Google Scholar
    • Export Citation
  • Milne SA, Perchick GB, Boddy SC & Jabbour HN 2001 Expression, localization, and signaling of PGE(2) and EP2/EP4 receptors in human nonpregnant endometrium across the menstrual cycle. Journal of Clinical Endocrinology and Metabolism 86 4453445 9. (https://doi.org/10.1210/jcem.86.9.7856)

    • Search Google Scholar
    • Export Citation
  • Mo HQ, Tian FJ, Ma XL, Zhang YC, Zhang CX, Zeng WH, Zhang Y & Lin Y 2020 PDIA3 regulates trophoblast apoptosis and proliferation in preeclampsia via the MDM2/p53 pathway. Reproduction 160 293305. (https://doi.org/10.1530/REP-20-0156)

    • Search Google Scholar
    • Export Citation
  • Neeb L, Hellen P, Boehnke C, Hoffmann J, Schuh-Hofer S, Dirnagl U & Reuter U 2011 IL-1beta stimulates COX-2 dependent PGE(2) synthesis and CGRP release in rat trigeminal ganglia cells. PLoS ONE 6 e17360. (https://doi.org/10.1371/journal.pone.0017360)

    • Search Google Scholar
    • Export Citation
  • Ochoa-Bernal MA & Fazleabas AT 2020 Physiologic events of embryo implantation and decidualization in human and non-human primates. International Journal of Molecular Sciences 21 1973. (https://doi.org/10.3390/ijms21061973)

    • Search Google Scholar
    • Export Citation
  • Palomba S, Russo T, Falbo A, Di Cello A, Amendola G, Mazza R, Tolino A, Zullo F, Tucci L & La Sala GB 2012 Decidual endovascular trophoblast invasion in women with polycystic ovary syndrome: an experimental case-control study. Journal of Clinical Endocrinology and Metabolism 97 2441244 9. (https://doi.org/10.1210/jc.2012-1100)

    • Search Google Scholar
    • Export Citation
  • Piltonen TT, Chen JC, Khatun M, Kangasniemi M, Liakka A, Spitzer T, Tran N, Huddleston H, Irwin JC & Giudice LC 2015 Endometrial stromal fibroblasts from women with polycystic ovary syndrome have impaired progesterone-mediated decidualization, aberrant cytokine profiles and promote enhanced immune cell migration in vitro. Human Reproduction 30 12031 21 5. (https://doi.org/10.1093/humrep/dev055)

    • Search Google Scholar
    • Export Citation
  • Poyser NL 1995 The control of prostaglandin production by the endometrium in relation to luteolysis and menstruation. Prostaglandins, Leukotrienes, and Essential Fatty Acids 53 1471 95. (https://doi.org/10.1016/0952-3278(9590115-9)

    • Search Google Scholar
    • Export Citation
  • Qin S, Zhang Y, Zhang J, Tian F, Sun L, He X, Ma X, Zhang J, Liu XR & Zeng W et al.2020 SPRY4 regulates trophoblast proliferation and apoptosis via regulating IFN-gamma-induced STAT1 expression and activation in recurrent miscarriage. American Journal of Reproductive Immunology 83 e13234. (https://doi.org/10.1111/aji.13234)

    • Search Google Scholar
    • Export Citation
  • Richards RG, Brar AK, Frank GR, Hartman SM & Jikihara H 1995 Fibroblast cells from term human decidua closely resemble endometrial stromal cells: induction of prolactin and insulin-like growth factor binding protein-1 expression. Biology of Reproduction 52 6096 15. (https://doi.org/10.1095/biolreprod52.3.609)

    • Search Google Scholar
    • Export Citation
  • Salamonsen LA, Evans J, Nguyen HP & Edgell TA 2016 The microenvironment of human implantation: determinant of reproductive success. American Journal of Reproductive Immunology 75 2182 2 5. (https://doi.org/10.1111/aji.12450)

    • Search Google Scholar
    • Export Citation
  • Silva JF & Serakides R 2016 Intrauterine trophoblast migration: a comparative view of humans and rodents. Cell Adhesion and Migration 10 88110. (https://doi.org/10.1080/19336918.2015.1120397)

    • Search Google Scholar
    • Export Citation
  • Simon C, Frances A, Piquette G, Hendrickson M, Milki A & Polan ML 1994 Interleukin-1 system in the materno-trophoblast unit in human implantation: immunohistochemical evidence for autocrine/paracrine function. Journal of Clinical Endocrinology and Metabolism 78 8478 54. (https://doi.org/10.1210/jcem.78.4.8157710)

    • Search Google Scholar
    • Export Citation
  • Strakova Z, Srisuparp S & Fazleabas AT 2000 Interleukin-1beta induces the expression of insulin-like growth factor binding protein-1 during decidualization in the primate. Endocrinology 141 466446 70. (https://doi.org/10.1210/endo.141.12.7810)

    • Search Google Scholar
    • Export Citation
  • Strakova Z, Srisuparp S & Fazleabas AT 2002 IL-1beta during in vitro decidualization in primate. Journal of Reproductive Immunology 55 3547. (https://doi.org/10.1016/s0165-0378(0100141-3)

    • Search Google Scholar
    • Export Citation
  • Su RW, Strug MR, Joshi NR, Jeong JW, Miele L, Lessey BA, Young SL & Fazleabas AT 2015 Decreased notch pathway signaling in the endometrium of women with endometriosis impairs decidualization. Journal of Clinical Endocrinology and Metabolism 100 E433E442. (https://doi.org/10.1210/jc.2014-3720)

    • Search Google Scholar
    • Export Citation
  • Tamura M, Sebastian S, Yang S, Gurates B, Fang Z & Bulun SE 2002 Interleukin-1beta elevates cyclooxygenase-2 protein level and enzyme activity via increasing its mRNA stability in human endometrial stromal cells: an effect mediated by extracellularly regulated kinases 1 and 2. Journal of Clinical Endocrinology and Metabolism 87 326332 73. (https://doi.org/10.1210/jcem.87.7.8594)

    • Search Google Scholar
    • Export Citation
  • Wang G, Liang R, Liu T, Wang L, Zou J, Liu N, Liu Y, Cai X, Liu Y & Ding X et al.2019 Opposing effects of IL-1beta/COX-2/PGE2 pathway loop on islets in type 2 diabetes mellitus. Endocrine Journal 66 691699. (https://doi.org/10.1507/endocrj.EJ19-0015)

    • Search Google Scholar
    • Export Citation
  • Yu J, Berga SL, Zou W, Yook DG, Pan JC, Andrade AA, Zhao L, Sidell N, Bagchi IC & Bagchi MK et al.2017 IL-1beta inhibits connexin 43 and disrupts decidualization of human endometrial stromal cells through ERK1/2 and p38 MAP kinase. Endocrinology 158 42704285. (https://doi.org/10.1210/en.2017-00495)

    • Search Google Scholar
    • Export Citation
  • Yu J, Berga SL, Zou W & Taylor RN 2019 Interleukin-1beta inhibits estrogen receptor-alpha, progesterone receptors A and B and biomarkers of human endometrial stromal cell differentiation: implications for endometriosis. Molecular Human Reproduction 25 625637. (https://doi.org/10.1093/molehr/gaz045)

    • Search Google Scholar
    • Export Citation
  • Zhou XL, Lei ZM & Rao CV 1999 Treatment of human endometrial gland epithelial cells with chorionic gonadotropin/luteinizing hormone increases the expression of the cyclooxygenase-2 gene. Journal of Clinical Endocrinology and Metabolism 84 33643377. (https://doi.org/10.1210/jcem.84.9.5943)

    • Search Google Scholar
    • Export Citation