Embryonic implantation in mice is blocked by interleukin-1 receptor antagonist.

Simón, Carlos; Frances, Ana; Piquette, Gary N.; Danasouri, Imam El; Zurawski, Gérard; Dang, W; Polan, Mary Lake

doi:10.1210/endo.134.2.8299552

Cited by 203 publications

(43 citation statements)

References 20 publications

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“…Deletion of IL-1RT1 in knockout mice results in only a slightly reduced litter size [27]. However, repeated injections of IL1Rant into pregnant mice prior to implantation caused implantation failure [28]. Regardless of the receptor pathway, these studies indicate the importance of IL-1␤ signaling during implantation in the mouse.…”

Section: Discussionmentioning

confidence: 83%

Characterization of the Interleukin-1 System During Porcine Trophoblastic Elongation and Early Placental Attachment

Ross

Malayer

Ritchey

et al. 2003

Biology of Reproduction

135

153

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Conceptus-uterine communication is established during trophoblastic elongation when the conceptus synthesizes and releases estrogen, the maternal recognition signal in the pig. Interleukin-1beta (IL-1beta) is a differentially expressed gene during rapid trophoblastic elongation in the pig. The current investigation determined conceptus and endometrial changes in gene expression for IL-1beta, IL-1 receptor antagonist (IL-1Rant), IL-1 receptor type 1 (IL-1RT1), and IL-1 receptor accessory protein (IL-1RAP) in developing peri- and postimplantation conceptuses as well as uterine endometrium collected from cyclic and pregnant gilts. Conceptus IL-1beta gene expression was enhanced during the period of rapid trophoblastic elongation compared with earlier spherical conceptuses, followed by a dramatic decrease in elongated Day 15 conceptuses. IL-1RT1 and IL-1RAP gene expression was greater in Day 12 and 15 filamentous conceptuses compared with earlier morphologies while IL-1Rant gene expression was unchanged by conceptus development. The uterine lumenal content of IL-1beta increased during the process of trophoblastic elongation on Day 12. Uterine IL-1beta content declined on Day 15, reaching a nadir by Day 18 of pregnancy. IL-1beta gene expression in porcine conceptuses was temporally associated with an increase in endometrial IL-1RT1 and IL-1RAP gene expression in pregnant gilts. Endometrial IL-1beta and IL-1Rant gene expression were lowest during Days 10-15 of the estrous cycle and pregnancy. The temporal expression of IL-1beta during conceptus development and the initiation of conceptus-uterine communication suggests conceptus IL-1beta synthesis plays an important role in porcine conceptus elongation and the establishment of pregnancy in the pig.

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Section: Discussionmentioning

confidence: 83%

Characterization of the Interleukin-1 System During Porcine Trophoblastic Elongation and Early Placental Attachment

Ross

Malayer

Ritchey

et al. 2003

Biology of Reproduction

135

153

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show abstract

“…Current data suggest that IL-1␤ can activate multiple signaling pathways regulating insulin-like growth factor binding protein-1 gene expression and decidualization in vitro and may be involved in the events leading to decidualization in baboons [50]. During human embryonic implantation, the interactions between embryo and endometrium are mediated through the embryonic IL-1␣ and IL-1␤ [51], and blockade of the endometrial IL-1 receptor prevents implantation in the mouse by interfering with embryonic attachment [52]. Furthermore, the embryo is able to synthesize PGs [53].…”

Section: Discussionmentioning

confidence: 99%

Different Regulatory Pathways of Endometrial Connexin Expression: Preimplantation Hormonal-Mediated Pathway Versus Embryo Implantation-Initiated Pathway1

Grümmer

Hewitt

Traub

et al. 2004

Biology of Reproduction

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Transformation of the endometrium into the receptive phase is under the control of ovarian steroid hormones and is modulated by embryonic signals during implantation. We have previously shown that this differentiation process is accompanied by a suppression of gap junction connexins (Cx) 26 and 43 before implantation followed by a local induction of both connexins in the implantation chamber. In the present study, we demonstrate that connexin gene expression in the rodent endometrium is regulated via two distinct signaling pathways during these different stages of early pregnancy. During preimplantation, transcription of connexins can be induced by estrogen via an estrogen receptor (ER)-dependent pathway. Additionally, Cx26 and Cx43 are induced by embryonic signals during implantation and delayed implantation as well as during artificially induced decidualization. In contrast to the estrogen-induced expression, this embryonic/decidual-associated induction of Cx26 and Cx43 could not be blocked by antiestrogen, thus pointing to another regulatory pathway independent of the ER. Studies in ERalpha and ERbeta knockout mice confirmed these different pathways, demonstrating that in the endometrium, estrogen-mediated Cx26 gene induction, but not induction during decidualization, is dependent on functional ERalpha. To evaluate potential embryonic signals regulating Cx26 expression, uteri of pseudopregnant animals were incubated with different mediators in an organ-culture model, showing that catechol estrogen and mediators of the inflammatory cascade such as prostaglandin F(2alpha) and interleukin-1beta are able to induce Cx26 expression through the ER-independent pathway. Thus, the present study demonstrates that endometrial expression of Cx26 and Cx43 is induced via estrogen and ERalpha during preimplantation but then utilizes an ER-independent signaling pathway during embryo implantation and decidualization.

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“…Thus, IL-1i may have a dual role of increasing cytotrophoblast and maternal MMP-9 expression, while simultaneously decreasing maternal TIMPs-1 and -3, enhancing the invasive capacity for early gestational cytotrophoblasts. The potential importance of these observations is underscored by the fact that embryonic implantation in mice can be blocked by the administration of an IL-1i receptor antagonist [139]. On the other hand, progesterone has the ability to downregulate MMP-9 expression by trophoblasts, possibly acting to reduce trophoblast invasion later in gestation [140].…”

Section: Placentationmentioning

confidence: 99%

Cellular turnover and extracellular matrix remodeling in female reproductive tissues: functions of metalloproteinases and their inhibitors

Fata¹,

Ho²,

Leco³

et al. 2000

Cellular and Molecular Life Sciences (CMLS)

131

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Female reproductive tissues possess a unique ability to accommodate a remarkable amount of cell turnover and extracellular matrix (ECM) remodeling following puberty. Cellular structures within ovary, uterus, and mammary tissue not only change cyclically in response to ovarian hormones but also undergo differentiation during pregnancy, and eventually revert to that resembling the pre-pregnant stage. Cell proliferation, apoptosis, invasion, and differentiation are integral cellular processes that are precisely regulated in reproductive tissues, but become dysregulated in pathologies such as cancer. Explicit reorganization of ECM and basement membranes is also critical to preserve the form and function of these tissues. Here we review the evidence that coordinated spatiotemporal expression patterns of matrix metalloproteinase (MMP) genes and their tissue inhibitors (TIMPs) are important in cell and ECM turnover of the ovary, uterus, and mammary tissues. We discuss how perturbation in these gene families may impact the biology of these reproductive tissues and the factors implicated in the control of MMP and TIMP gene expression. The observed trends in MMP and TIMP expression involved in ovarian and mammary carcinomas are also presented.

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Embryonic implantation in mice is blocked by interleukin-1 receptor antagonist.

Cited by 203 publications

References 20 publications

Characterization of the Interleukin-1 System During Porcine Trophoblastic Elongation and Early Placental Attachment

Characterization of the Interleukin-1 System During Porcine Trophoblastic Elongation and Early Placental Attachment

Different Regulatory Pathways of Endometrial Connexin Expression: Preimplantation Hormonal-Mediated Pathway Versus Embryo Implantation-Initiated Pathway1

Cellular turnover and extracellular matrix remodeling in female reproductive tissues: functions of metalloproteinases and their inhibitors

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