Abstract
The aim of this study was to investigate the differential expression and regulation of Runt-related transcription factor 3 (Runx3) in mouse uterus during early pregnancy and its regulation by steroid hormones using in situ hybridization. There was a low level of the Runx3 mRNA expression in the mouse uterus on days 1–4 of pregnancy. On day 5 when embryo implanted, Runx3 mRNA signal was obviously observed in the stromal cells surrounding the implanting blastocyst. From day 6 to 8 of pregnancy, Runx3 mRNA was highly expressed in the decidual cells and mesometrial decidual beds. Similarly, Runx3 mRNA was strongly expressed in decidualized cells under artificial decidualization. Compared with the delayed uterus, a high level of Runx3 mRNA signal was detected in the uterus with activated implantation. In the ovariectomized mouse uterus, estrogen could induce the expression of Runx3, while progesterone had no effects. These results suggest that Runx3 may play an important role during mouse implantation and decidualization. Estrogen can induce the expression of Runx3 in the ovariectomized mouse uterus.
Similar content being viewed by others
References
Cakmak H, Taylor HS (2011) Implantation failure: molecular mechanisms and clinical treatment. Hum Reprod Update 17:242–253
Chakraborty I, Das SK, Dey SK (1995) Differential expression of vascular endothelial growth factor and its receptor mRNAs in the mouse uterus around the time of implantation. J Endocrinol 147:339–352
Chuang LS, Ito K, Ito Y (2013) RUNX family: regulation and diversification of roles through interacting proteins. Int J Cancer 132:1260–1271
Dey SK, Lim H, Das SK, Reese J, Paria BC, Daikoku T, Wang H (2004) Molecular cues to implantation. Endocr Rev 25:341–373
Guo ZL, Chen K, Wang XQ, Hu W (2011) Expression and relationship of Ezh2, Runx3 and caspase-3 in endometrial adenocarcinoma. Zhonghua Bing Li Xue Za Zhi 40:387–391
Guo B, Wang W, Li SJ, Han YS, Zhang L, Zhang XM, Liu JX, Yue ZP (2012) Differential expression and regulation of angiopoietin-2 in mouse uterus during preimplantation period. Anat Rec (Hoboken) 295:338–346
Huang B, Qu Z, Ong CW, Tsang YH, Xiao G, Shapiro D, Salto-Tellez M, Ito K, Ito Y, Chen LF (2012) RUNX3 acts as a tumor suppressor in breast cancer by targeting estrogen receptor alpha. Oncogene 31:527–534
Huehn J, Polansky JK, Hamann A (2009) Epigenetic control of FOXP3 expression: the key to a stable regulatory T-cell lineage? Nat Rev Immunol 9:83–89
Klunker S, Chong MM, Mantel PY, Palomares O, Bassin C, Ziegler M, Rückert B, Meiler F, Akdis M, Littman DR, Akdis CA (2009) Transcription factors RUNX1 and RUNX3 in the induction and suppressive function of Foxp3+ inducible regulatory T cells. J Exp Med 206:2701–2715
Nevadunsky NS, Barbieri JS, Kwong J, Merritt MA, Welch WR, Berkowitz RS, Mok SC (2009) RUNX3 protein is overexpressed in human epithelial ovarian cancer. Gynecol Oncol 112:325–330
Nimmo R, Woollard A (2008) Worming out the biology of Runx. Dev Biol 313:492–500
Peng Z, Wei D, Wang L, Tang H, Zhang J, Le X, Jia Z, Li Q, Xie K (2006) RUNX3 inhibits the expression of vascular endothelial growth factor and reduces the angiogenesis, growth, and metastasis of human gastric cancer. Clin Cancer Res 12:6386–6394
Piva M, Flieger O, Rider V (1996) Growth factor control of cultured rat uterine stromal cell proliferation is progesterone dependent. Biol Reprod 55:1333–1342
Rockwell LC, Pillai S, Olson CE, Koos RD (2002) Inhibition of vascular endothelial growth factor/vascular permeability factor action blocks estrogen-induced uterine edema and implantation in rodents. Biol Reprod 67:1804–1810
Sakuma A, Fukamachi H, Ito K, Ito Y, Takeuchi S, Takahashi S (2008) Loss of Runx3 affects ovulation and estrogen‐induced endometrial cell proliferation in female mice. Mol Reprod Dev 75:1653–1661
Salgado RM, Covarrubias AC, Favaro RR, Serrano-Nascimento C, Nunes MT, Zorn TM (2013) Estradiol induces transcriptional and posttranscriptional modifications in versican expression in the mouse uterus. J Mol Histol 44:221–229
Shima T, Sasaki Y, Itoh M, Nakashima A, Ishii N, Sugamura K, Saito S (2010) Regulatory T cells are necessary for implantation and maintenance of early pregnancy but not late pregnancy in allogeneic mice. J Reprod Immunol 85:121–129
Singh M, Chaudhry P, Asselin E (2011) Bridging endometrial receptivity and implantation: network of hormones, cytokines, and growth factors. J Endocrinol 210:5–14
Tsuchiya Y, Saito Y, Taniuchi S, Sakuma A, Maekawa T, Fukamachi H, Takeuchi S, Takahashi S (2012) Runx3 expression and its roles in mouse endometrial cells. J Reprod Dev 58:592–598
Wang H, Dey SK (2006) Roadmap to embryo implantation: clues from mouse models. Nat Rev Genet 7:185–199
Yaba A, Kayisli UA, Johnson J, Demir R, Demir N (2011) The Abelson tyrosine kinase (c-Abl) expression on the mouse uterus and placenta during gestational period. J Mol Histol 42:91–96
Acknowledgments
This work was financially supported by National Natural Science Foundation of China (31072099 and 31101778), Research Fund for the Doctoral Program of Higher Education of China (20100061110078) and “985” Platform Construction Foundation of Jilin University.
Author information
Authors and Affiliations
Corresponding authors
Additional information
Zhi-Kun Bai and Bin Guo contributed equally to this work.
Rights and permissions
About this article
Cite this article
Bai, ZK., Guo, B., Tian, XC. et al. Expression and regulation of Runx3 in mouse uterus during the peri-implantation period. J Mol Hist 44, 519–526 (2013). https://doi.org/10.1007/s10735-013-9501-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10735-013-9501-z