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      ADAMTS-1: a novel target gene of an estrogen-induced transcription factor, EGR1, critical for embryo implantation in the mouse uterus

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          Abstract

          Background

          Recently, we demonstrated that estrogen (E 2) induces early growth response 1 (Egr1) to mediate its actions on the uterine epithelium by controlling progesterone receptor signaling for successful embryo implantation. EGR1 is a transcription factor that regulates the spectrum of target genes in many different tissues, including the uterus. E 2-induced EGR1 regulates a set of genes involved in epithelial cell remodeling during embryo implantation in the uterus. However, only few target genes of EGR1 in the uterus have been identified.

          Result

          The expression of ADAM metallopeptidase with thrombospondin type 1 motif 1 ( Adamts-1) was significantly downregulated in the uteri of E 2-treated ovariectomized (OVX) Egr1(−/−) mice. Immunostaining of ADAMTS-1 revealed its exclusive expression in the uterine epithelium of OVX wild-type but not Egr1(−/−) mice treated with E 2. The expression profiles of Adamts-1 and Egr1 were similar in the uteri of E 2-treated OVX mice at various time points tested. Pre-treatment with ICI 182, 780, a nuclear estrogen receptor (ER) antagonist, effectively inhibited the E 2-dependent induction of Egr1 and Adamts-1. Pharmacologic inhibition of E 2-induced ERK1/2 or p38 phosphorylation interfered with the induction of EGR1 and ADAMTS-1. Furthermore, ADAMTS-1, as well as EGR1, was induced in stroma cells surrounding the implanting blastocyst during embryo implantation. Transient transfection with EGR1 expression vectors significantly induced the expression of ADAMTS-1. Luciferase activity of the Adamts-1 promoter containing EGR1 binding sites (EBSs) was increased by EGR1 in a dose-dependent manner, suggesting functional regulation of Adamts-1 transcription by EGR1. Site-directed mutagenesis of EBS on the Adamts-1 promoter demonstrated that EGR1 directly binds to the EBS at -1151/-1134 among four putative EBSs.

          Conclusions

          Collectively, we have demonstrated that Adamts-1 is a novel target gene of E 2-ER-MAPK-EGR1, which is critical for embryo implantation in the mouse uterus during early pregnancy.

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          Mechanisms of implantation: strategies for successful pregnancy.

          Jeeyeon Cha, Xiaofei Sun, Sudhansu Dey (2012)
          Physiological and molecular processes initiated during implantation for pregnancy success are complex but highly organized. This review primarily highlights adverse ripple effects arising from defects during the peri-implantation period that perpetuate throughout pregnancy. These defects are reflected in aberrations in embryo spacing, decidualization, placentation and intrauterine embryonic growth, manifesting in preeclampsia, miscarriages and/or preterm birth. Understanding molecular signaling networks that coordinate strategies for successful implantation and decidualization may lead to approaches to improve the outcome of natural pregnancy and pregnancy conceived from in vitro fertilization.
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            Mathematics of quantitative kinetic PCR and the application of standard curves.

            Hélène C. F. Côté, R. G. Rutledge (2003)
            Fluorescent monitoring of DNA amplification is the basis of real-time PCR, from which target DNA concentration can be determined from the fractional cycle at which a threshold amount of amplicon DNA is produced. Absolute quantification can be achieved using a standard curve constructed by amplifying known amounts of target DNA. In this study, the mathematics of quantitative PCR are examined in detail, from which several fundamental aspects of the threshold method and the application of standard curves are illustrated. The construction of five replicate standard curves for two pairs of nested primers was used to examine the reproducibility and degree of quantitative variation using SYBER Green I fluorescence. Based upon this analysis the application of a single, well- constructed standard curve could provide an estimated precision of +/-6-21%, depending on the number of cycles required to reach threshold. A simplified method for absolute quantification is also proposed, in which quantitative scale is determined by DNA mass at threshold.
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              Progesterone-regulated genes in the ovulation process: ADAMTS-1 and cathepsin L proteases.

              Stuart D. Russell, Nigel G. J. Richards, B. O’Malley … (2000)
              Ovulation is a precisely timed process by which a mature oocyte is released from an ovarian follicle. This process is initiated by the pituitary surge of luteinizing hormone (LH), is temporally associated with transcriptional regulation of numerous genes, and is presumed to involve the synthesis and/or activation of specific proteases that degrade the follicle wall. The progesterone receptor (PR), a nuclear receptor transcription factor, is induced in granulosa cells of preovulatory follicles in response to the LH surge and has been shown to be essential for ovulation, because mice lacking PR fail to ovulate and are infertile. Using these mice as a model in which to elucidate PR-regulated genes in the ovulation process, we show that the matrix metalloproteinases MMP-2 and MMP-9 are not targets of PR during ovulation. In contrast, two other proteases, ADAMTS-1 (A disintegrin and metalloproteinase with thrombospondin-like motifs) and cathepsin L (a lysosomal cysteine protease), are transcriptional targets of PR action. ADAMTS-1 is induced after LH stimulation in granulosa cells of preovulatory follicles and depends on PR. Cathepsin L is induced in granulosa cells of growing follicles by follicle-stimulating hormone, but the highest levels of cathepsin L mRNA occur in preovulatory follicles in response to LH in a PR-dependent manner. The identification of two regulated proteases in the ovary, together with their abnormal expression in anovulatory PR knockout mice, suggests that each plays a critical role in follicular rupture and represents a major advance in our understanding of the proteolytic events that control ovulation.
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                Author and article information

                Contributors
                Hyunjung J. Lim: hlim@konkuk.ac.kr
                Haengseok Song:
                ORCID: http://orcid.org/0000-0002-5027-7310
                hssong@cha.ac.kr
                Journal
                Journal ID (nlm-ta): Cell Biosci
                Journal ID (iso-abbrev): Cell Biosci
                Title: Cell & Bioscience
                Publisher: BioMed Central (London )
                ISSN (Electronic): 2045-3701
                Publication date (Electronic): 4 August 2021
                Publication date PMC-release: 4 August 2021
                Publication date Collection: 2021
                Volume: 11
                Electronic Location Identifier: 155
                Affiliations
                [1 ]GRID grid.410886.3, ISNI 0000 0004 0647 3511, Department of Biomedical Science, , CHA University, ; Seongnam, Gyeonggi-do 13488 Republic of Korea
                [2 ]GRID grid.258676.8, ISNI 0000 0004 0532 8339, Department of Veterinary Medicine, School of Veterinary Medicine, , Konkuk University, ; 120 Neungdong-ro, Gwangjin-gu, Seoul, 05029 South Korea
                Author information
                http://orcid.org/0000-0002-5027-7310
                Article
                Publisher ID: 672
                DOI: 10.1186/s13578-021-00672-8
                PMC ID: 8336340
                PubMed ID: 34348778
                SO-VID: 4b8442ba-a30f-41d3-ace3-3c058c0f4d7d
                Copyright © © The Author(s) 2021
                License:

                Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

                History
                Date received : 5 April 2021
                Date accepted : 28 July 2021
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100003725, National Research Foundation of Korea;
                Award ID: 2019R1A6A1A03032888
                Award ID: 2020R1A2C1004122
                Award ID: 2020R1A2C2005012
                Award Recipient :
                Categories
                Subject: Research
                Custom metadata
                issue-copyright-statement © The Author(s) 2021

                ScienceOpen disciplines: Cell biology
                Keywords: estrogen,egr1,adamts-1,transcription,uterus
                Data availability:
                ScienceOpen disciplines: Cell biology
                Keywords: estrogen, egr1, adamts-1, transcription, uterus

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