Involvement of Histone Acetylation in Ovarian Steroid-induced Decidualization of Human Endometrial Stromal Cells*

Histone acetyltransferases and histone deacetylases (HDACs) determine the acetylation status of histones, regulating gene transcription. Decidualization is the progestin-induced differentiation of estrogen-primed endometrial stromal cells (ESCs), which is crucial for implantation and maintenance of pregnancy. We here show that trichostatin A (TSA), a specific HDAC inhibitor, enhances the up-regulation of decidualization markers such as insulin-like growth factor binding protein-1 (IGFBP-1) and prolactin in a dose-dependent manner that is directed by 17β-estradiol (E2) plus progesterone (P4) in cultured ESCs, but not glandular cells, both isolated from human endometrium. Morphological changes resembling decidual transformation were also augmented by co-addition of TSA. Acid urea triton gel analysis and immunoblot using acetylated histone type-specific antibodies demonstrated that treatment with E2 plus P4 significantly increased the levels of acetylated H3 and H4 whose increment was augmented by co-treatment with TSA. Chromatin immunoprecipitation assay revealed that treatment with E2plus P4 increased the amount of proximal progesterone-responsive region of IGFBP-1 promoter associated with acetylated H4, which was dramatically enhanced by co-addition of TSA. Taken together, our results suggest that histone acetylation is deeply involved in differentiation of human ESCs and that TSA has a potential as an enhancer of decidualization through promotion of progesterone action.

• Publication year

  2003

• Venue

  Journal of Biological Chemistry

• Publication date

  2003-05-09

• Fields of study

  Biology, Medicine

• Identifiers
  DOI 10.1074/JBC.M211715200PMID 12609987
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• Steroid receptor coactivator expression throughout the menstrual cycle in normal and abnormal endometrium.

  2002cited by this paper
• Regulated expression of signal transducer and activator of transcription, Stat5, and its enhancement of PRL expression in human endometrial stromal cells in vitro.

  2002cited by this paper
• Endometrial nuclear receptor co-factors SRC-1 and N-CoR are increased in human endometrium during menstruation.

  2002cited by this paper
• Histone-deacetylase inhibitors: novel drugs for the treatment of cancer

  2002cited by this paper
• Expression and subcellular distribution of the active form of c-Src tyrosine kinase in differentiating human endometrial stromal cells.

  2002cited by this paper
• Histone acetyltransferases.

  2001cited by this paper
• Telomerase activation by histone deacetylase inhibitor in normal cells.

  2001cited by this paper
• CREB-binding Protein and p300 in Transcriptional Regulation*

  2001cited by this paper
• Gene induction and categorical reprogramming during in vitro human endometrial fibroblast decidualization.

  2001cited by this paper
• Nuclear hormone receptor coregulators in action: diversity for shared tasks.

  2000cited by this paper
• Discovery of new inducible genes in in vitro decidualized human endometrial stromal cells using microarray technology.

  2000cited by this paper
• Acetylation of Histones and Transcription-Related Factors

  2000cited by this paper
• Ligand-activated progesterone receptor isoform hPR-A is a stronger transactivator than hPR-B for the expression of IGFBP-1 (insulin-like growth factor binding protein-1) in human endometrial stromal cells.

  2000cited by this paper
• Tyrosine phosphorylation and subcellular localization of focal adhesion proteins during in vitro decidualization of human endometrial stromal cells.

  1999cited by this paper
• Activation of the insulin-like growth factor binding protein-1 promoter by progesterone receptor in decidualized human endometrial stromal cells.

  1999cited by this paper
• Activation of c-Src kinase is associated with in vitro decidualization of human endometrial stromal cells.

  1999cited by this paper
• Progesterone receptor regulates decidual prolactin expression in differentiating human endometrial stromal cells.

  1999cited by this paper
• Induction of thioredoxin, a redox-active protein, by ovarian steroid hormones during growth and differentiation of endometrial stromal cells in vitro.

  1999cited by this paper
• Partial hormone resistance in mice with disruption of the steroid receptor coactivator-1 (SRC-1) gene.

  1998cited by this paper
• Hypoxia stimulates insulin-like growth factor binding protein 1 (IGFBP-1) gene expression in HepG2 cells: a possible model for IGFBP-1 expression in fetal hypoxia.

  1998cited by this paper
• Expression of functional prolactin receptors in nonpregnant human endometrium: janus kinase-2, signal transducer and activator of transcription-1 (STAT1), and STAT5 proteins are phosphorylated after stimulation with prolactin.

  1998cited by this paper
• Roles of histone acetyltransferases and deacetylases in gene regulation

  1998cited by this paper
• Progesterone-dependent decidualization of the human endometrium is mediated by cAMP

  1997cited by this paper
• Activated protein kinase A is required for differentiation-dependent transcription of the decidual prolactin gene in human endometrial stromal cells.

  1997cited by this paper
• Thioredoxin expression in the human endometrium during the menstrual cycle.

  1997cited by this paper
• Distal Sp3 binding sites in the hIGBP-1 gene promoter suppress transcriptional repression in decidualized human endometrial stromal cells: identification of a novel Sp3 form in decidual cells.

  1996cited by this paper
• The expression of a small fraction of cellular genes is changed in response to histone hyperacetylation.

  1996cited by this paper
• Trichostatin A and trapoxin: Novel chemical probes for the role of histone acetylation in chromatin structure and function

  1995cited by this paper
• Identification of a Distal Regulatory Sequence of the Human IGFBP-1 Gene Promoter and Regulation by the Progesterone Receptor in a Human Endometrial Adenocarcinoma Cell Line

  1994cited by this paper
• Molecular cloning and functional analysis of the adenovirus E1A-associated 300-kD protein (p300) reveals a protein with properties of a transcriptional adaptor.

  1994cited by this paper
• Rapid construction of deleted DNA fragments for use as internal standards in competitive PCR.

  1994cited by this paper
• Growth factors and growth modulators in human uterine endometrium: their potential relevance to reproductive medicine.

  1994cited by this paper
• Cyclic adenosine 3',5'-monophosphate induces prolactin expression in stromal cells isolated from human proliferative endometrium.

  1993cited by this paper
• Phosphorylated CREB binds specifically to the nuclear protein CBP

  1993cited by this paper
• Human endometrium: an active site of cytokine production and action.

  1991cited by this paper
• Potent and specific inhibition of mammalian histone deacetylase both in vivo and in vitro by trichostatin A.

  1990cited by this paper
• Hormonal regulation of human endometrial stromal cells in culture: an in vitro model for decidualization.

  1989cited by this paper
• Regulation of prolactin production by progestin, estrogen, and relaxin in human endometrial stromal cells.

  1987cited by this paper
• Histone 2A, a heteromorphous family of eight protein species.

  1980cited by this paper
• Synthesis and modification of the histones during the decidual cell reaction in the mouse uterus.

  1979cited by this paper
• Dating the endometrial biopsy.

  1950cited by this paper

• Endometrial Receptivity–Lessons from “Omics”

  2025cites this paper
• Advances in post-translational modifications and recurrent spontaneous abortion.

  2024cites this paper
• Epithelial mesenchymal transition in human menstruation and implantation.

  2024cites this paper
• Deciphering the role of PGRMC2 in the human endometrium during the menstrual cycle and in vitro decidualization using an in vitro approach.

  2024cites this paper
• Histone H4 hyperacetylation but not DNA methylation regulates the expression of decidualization-associated genes during induced human endometrial stromal cells decidualization.

  2023cites this paper
• Non-coding RNAs in Recurrent implantation failure.

  2023cites this paper
• Gαq-PKD/PKCμ signal regulating the nuclear export of HDAC5 to induce the IκB expression and limit the NF-κB-mediated inflammatory response essential for early pregnancy

  2023cites this paper
• Genome-wide analysis of histone modifications that underlie the dynamic changes in gene expression during decidualization in human endometrial stromal cells.

  2023cites this paper
• Downregulated INHBB in endometrial tissue of recurrent implantation failure patients impeded decidualization through the ADCY1/cAMP signalling pathway

  2023cites this paper
• The regulation and function of acetylated high-mobility group box 1 during implantation and decidualization

  2023cites this paper
• Menstrual Blood-Derived Endometrial Stem Cells’ Impact for the Treatment Perspective of Female Infertility

  2021influential citation
• The role of epigenetic mechanisms in the regulation of gene expression in the cyclical endometrium

  2021cites this paper
• Genetic, Epigenetic, and Steroidogenic Modulation Mechanisms in Endometriosis

  2020cites this paper
• Novel nonclassic progesterone receptor PGRMC1 pulldown-precipitated proteins reveal a key role during human decidualization.

  2020cites this paper
• Nitration of protein phosphatase 2A increases via Epac1/PLCε/CaMKII/HDAC5/iNOS cascade in human endometrial stromal cell decidualization

  2020cites this paper
• Histone acetylation and the role of histone deacetylases in normal cyclic endometrium

  2020cites this paper
• The Pathogenesis of Endometriosis: Molecular and Cell Biology Insights

  2019cites this paper
• Epigenetic modifications working in the decidualization and endometrial receptivity

  2019cites this paper
• Regulatory mechanisms of endometrial decidualization and pregnancy-related diseases.

  2019cites this paper
• Genome-Wide Profiling of Long Noncoding RNA Expression Patterns in Women With Repeated Implantation Failure by RNA Sequencing

  2019cites this paper
• Trichostatin A inhibits uterine histomorphology alterations induced by cigarette smoke exposure in mice.

  2019cites this paper
• HDAC Inhibitors in Acute Myeloid Leukemia

  2019cites this paper
• Epigenetic control of embryo–uterine crosstalk at peri-implantation

  2019cites this paper
• Differential regulation of mTORC1 and mTORC2 is critical for 8-Br-cAMP-induced decidualization

  2018cites this paper
• Loss of high‐mobility group N5 contributes to the promotion of human endometrial stromal cell decidualization

  2018cites this paper
• Emerging role for dysregulated decidualization in the genesis of preeclampsia.

  2017cites this paper
• Effects of high progesterone level on the day of human chorionic gonadotrophin administration in in vitro fertilization cycles on epigenetic modification of endometrium in the peri-implantation period.

  2017cites this paper
• Epigenetics in endometrial carcinogenesis - part 2: histone modifications, chromatin remodeling and noncoding RNAs.

  2017cites this paper
• Serum estradiol levels in controlled ovarian stimulation directly affect the endometrium

  2017cites this paper
• SREBP1c-CRY1 signalling represses hepatic glucose production by promoting FOXO1 degradation during refeeding

  2016cites this paper
• Decidualization and Epigenetic Regulation

  2016cites this paper
• Rbbp7 Is Required for Uterine Stromal Decidualization in Mice1

  2015cites this paper
• Reproduction and nutriment–nurture crosstalk: epigenetic perspectives

  2015cites this paper
• Removal of REVERB inhibition contributes to the prostaglandin G / H synthase 2 1 expression in rat endometrial stromal cells 2

  2015cites this paper
• Removal of Rev-erbα inhibition contributes to the prostaglandin G/H synthase 2 expression in rat endometrial stromal cells.

  2015cites this paper
• Microarray Analysis on Gene Regulation by Estrogen, Progesterone and Tamoxifen in Human Endometrial Stromal Cells

  2015cites this paper
• Fetal programming theory: implication for the understanding of endometriosis.

  2014cites this paper
• Cyclic decidualization of the human endometrium in reproductive health and failure.

  2014cites this paper
• Genome-Wide Analysis of the Mouse Deciduoma

  2014cites this paper
• Genes Downregulated in Endometriosis Are Located Near the Known Imprinting Genes

  2014cites this paper
• Endometriosis Is Characterized by a Distinct Pattern of Histone 3 and Histone 4 Lysine Modifications

  2014cites this paper
• Two methods for establishing primary human endometrial stromal cells from hysterectomy specimens.

  2014cites this paper
• Derivation of human decidua-like cells from amnion and menstrual blood

  2014cites this paper
• Regulation of Matrix Metalloproteinases and Their Inhibitors by DNA Methylation in Human Gestational Tissues

  2013influential citation
• The motile and invasive capacity of human endometrial stromal cells: implications for normal and impaired reproductive function.

  2013cites this paper
• Effect of cyclic AMP and estrogen/progesterone on the transcription of DNA methyltransferases during the decidualization of human endometrial stromal cells.

  2013cites this paper
• The endometrial epigenome and its response to steroid hormones.

  2012cites this paper
• Inhibition of Histone Deacetylase Activity in Human Endometrial Stromal Cells Promotes Extracellular Matrix Remodelling and Limits Embryo Invasion

  2012influential citation
• Induction of IGFBP-1 expression by cAMP is associated with histone acetylation status of the promoter region in human endometrial stromal cells.

  2012cites this paper
• Expression of epigenetic effectors in decidualizing human endometrial stromal cells.

  2012cites this paper
• HDAC1 and HDAC2 are Differentially Expressed in Endometriosis

  2012cites this paper
• Cell Cycle Regulation of Human Endometrial Stromal Cells During Decidualization

  2012cites this paper
• Histone deacetylase inhibitors as therapeutics for endometriosis

  2012cites this paper
• DNA Methylation Regulates Human Endometrial Stromal Cell Decidualisation

  2012influential citation
• Individualized COS to optimize the quantity and quality of oocytes and embryos generated in ART cycles

  2011cites this paper
• Down-regulation of the histone methyltransferase EZH2 contributes to the epigenetic programming of decidualizing human endometrial stromal cells.

  2011cites this paper
• Role of estrogen on the maintenance and homing capacity of bone marrow derived rat mesenchymal stem cells

  2011cites this paper
• Epigenetic modification of suppressor of cytokine signaling-3 in asthmatic mouse lung: role of interleukin-6

  2011cites this paper
• Immunohistochemical detection of histone deacetylases in endometrial carcinoma: involvement of histone deacetylase 2 in the proliferation of endometrial carcinoma cells.

  2010cites this paper
• Epigenetic regulation of endometrium during the menstrual cycle.

  2010influential citation
• Constitutive and Tumor Necrosis Factor-Alpha-Stimulated Activation of Nuclear Factor-KappaB in Immortalized Endometriotic Cells and Their Suppression by Trichostatin A

  2010cites this paper
• The effect of DNA methylation inhibitor 5-Aza-2'-deoxycytidine on human endometrial stromal cells.

  2010influential citation
• Epigenetic Treatment in Assisted Human Embryo Implantation

  2009cites this paper
• Epigenetic regulation of the embryonic oncogene ERas in gastric cancer cells.

  2009cites this paper
• DNA methyltransferase expression in the human endometrium: down-regulation by progesterone and estrogen.

  2009cites this paper
• Molecular and cellular mechanisms for differentiation and regeneration of the uterine endometrium.

  2008cites this paper
• Activation of SRC kinase and phosphorylation of signal transducer and activator of transcription-5 are required for decidual transformation of human endometrial stromal cells.

  2008cites this paper
• Histone deacetylase inhibitors stimulate cell migration in human endometrial adenocarcinoma cells through up-regulation of glycodelin.

  2007cites this paper
• Noninvasive and real-time assessment of reconstructed functional human endometrium in NOD/SCID/γcnull immunodeficient mice

  2007cites this paper
• Histone deacetylase inhibitor-induced glycodelin enhances the initial step of implantation.

  2007cites this paper
• Class I histone deacetylase expression in the human cyclic endometrium and endometrial adenocarcinomas.

  2007cites this paper
• Decidualization Regulates the Expression of the Endometrial Chorionic Gonadotropin Receptor in the Primate1

  2006cites this paper
• Human endometrial cytodifferentiation by histone deacetylase inhibitors

  2006cites this paper
• Gender difference in estrogen receptor alpha promoter hypermethylation and its prognostic value in non‐small cell lung cancer

  2005cites this paper
• Progesterone-dependent release of transforming growth factor-beta1 from epithelial cells enhances the endometrial decidualization by turning on the Smad signalling in stromal cells.

  2005cites this paper
• Historie acetylation in reproductive organs: Significance of histone deacetylase inhibitors in gene transcription

  2005cites this paper
• Effects of histone deacetylase inhibitors on estradiol-induced proliferation and hyperplasia formation in the mouse uterus.

  2005cites this paper
• Histone deacetylase inhibitors induce differentiation of human endometrial adenocarcinoma cells through up-regulation of glycodelin.

  2005cites this paper
• Pyrazolo Pyrimidine-Type Inhibitors of Src Family Tyrosine Kinases Promote Ovarian Steroid-Induced Differentiation of Human Endometrial Stromal Cells In Vitro1

  2004cites this paper
• Reproductive Biology and Endocrinology Characterization of a Novel Telomerase-immortalized Human Endometrial Stromal Cell Line, St-t1b

  year unknowncites this paper