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Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

CircRNA-9119 regulates the expression of prostaglandin-endoperoxide synthase 2 (PTGS2) by sponging miR-26a in the endometrial epithelial cells of dairy goat

Lei Zhang A , Xiaorui Liu A , Sicheng Che A , Jiuzeng Cui A , Yuexia Liu A , Xiaopeng An A , Binyun Cao A and Yuxuan Song A B
+ Author Affiliations
- Author Affiliations

A College of Animal Science and Technology, Northwest A&F University, No. 22 Xinong Road, Yangling, Shaanxi 712100, P.R. China.

B Corresponding author. Email: yuxuan_song2016@163.com

Reproduction, Fertility and Development 30(12) 1759-1769 https://doi.org/10.1071/RD18074
Submitted: 29 January 2018  Accepted: 7 June 2018   Published: 9 July 2018

Abstract

Circular RNAs (circRNAs) have been found to play important functional roles in epigenetic regulation under certain physiological and pathological conditions. However, knowledge of circRNAs during the development of receptive endometrium (RE) from pre-RE is limited. In the RE of dairy goats, higher circRNA-9119 levels, with lower miR-26a and higher prostaglandin-endoperoxide synthase 2 (PTGS2) levels, were detected. Further study showed that circRNA-9119 decreased levels of miR-26a by acting as a microRNA sponge, and that miR-26a downregulated the expression of PTGS2 via the predicted target site in endometrial epithelial cells (EECs) of dairy goats in vitro. In this way, circRNA-9119 functioned as a competing endogenous RNAs (ceRNA) that sequestered miR-26a, thereby protecting PTGS2 transcripts from miR-26a-mediated suppression in dairy goat EECs in vitro. Furthermore, PTGS2 participated in the regulation of some protein markers for endometrial receptivity in dairy goat EECs in vitro. Thus, a circRNA-9119–miR-26a–PTGS2 pathway in the endometrium was identified, and modulation of circRNA-9119–miR-26a–PTGS2 expression in EECs may emerge as a potential target to regulate the development of RE.

Additional keywords: competing endogenous RNAs (ceRNA), development, embryo implantation, epigenetic regulation, mechanism, non-coding RNAs (ncRNAs), receptive endometrium, reproduction.


References

Arai, M., Yoshioka, S., Nishimura, R., and Okuda, K. (2014). FAS/FASL-mediated cell death in the bovine endometrium. Anim. Reprod. Sci. 151, 97–104.
FAS/FASL-mediated cell death in the bovine endometrium.Crossref | GoogleScholarGoogle Scholar |

Aupperle, H., Özgen, S., Schoon, H. A., Schoon, D., Hoppen, H. O., Sieme, H., and Tannapfel, A. (2000). Cyclical endometrial steroid hormone receptor expression and proliferation intensity in the mare. Equine Vet. J. 32, 228–232.
Cyclical endometrial steroid hormone receptor expression and proliferation intensity in the mare.Crossref | GoogleScholarGoogle Scholar |

Bae, S. H., Jung, E. S., Park, Y. M,, Kim, B. S., Kim, B. K., Kim, D. G., and Ryu, W. S. (2001). Expression of cyclooxygenase-2 (COX-2) in hepatocellular carcinoma and growth inhibition of hepatoma cell lines by a COX-2 inhibitor, NS-398. Clin. Cancer Res. 7, 1410–1418.

Carson, D. D., Lagow, E., Thathiah, A., Alshami, R., Farachcarson, M. C., Vernon, M., Yuan, L., Fritz, M. A., and Lessey, B. (2002). Changes in gene expression during the early to mid-luteal (receptive phase) transition in human endometrium detected by high-density microarray screening. Mol. Hum. Reprod. 8, 871–879.
Changes in gene expression during the early to mid-luteal (receptive phase) transition in human endometrium detected by high-density microarray screening.Crossref | GoogleScholarGoogle Scholar |

Chakraborty, I., Das, S. K., and Dey, S. K. (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.
Differential expression of vascular endothelial growth factor and its receptor mRNAs in the mouse uterus around the time of implantation.Crossref | GoogleScholarGoogle Scholar |

Chen, L., Zhang, S., Wu, J., Cui, J., Zhong, L., Zeng, L., and Ge, S. (2017). circRNA_100290 plays a role in oral cancer by functioning as a sponge of the miR-29 family. Oncogene 36, 4551–4561.
circRNA_100290 plays a role in oral cancer by functioning as a sponge of the miR-29 family.Crossref | GoogleScholarGoogle Scholar |

Chu, P. Y., Wright, P. J., and Lee, C. S. (2002). Apoptosis of endometrial cells in the bitch. Reprod. Fertil. Dev. 14, 297–305.
Apoptosis of endometrial cells in the bitch.Crossref | GoogleScholarGoogle Scholar |

Chu, P. Y., Lee, C. S., and Wright, P. J. (2006). Degeneration and apoptosis of endometrial cells in the bitch. Theriogenology 66, 1545–1549.
Degeneration and apoptosis of endometrial cells in the bitch.Crossref | GoogleScholarGoogle Scholar |

Das, S. K., Chakraborty, I., Wang, J., Dey, S. K., and Hoffman, L. H. (1997). Expression of vascular endothelial growth factor (VEGF) and VEGF-receptor messenger ribonucleic acids in the peri-implantation rabbit uterus. Biol. Reprod. 56, 1390–1399.
Expression of vascular endothelial growth factor (VEGF) and VEGF-receptor messenger ribonucleic acids in the peri-implantation rabbit uterus.Crossref | GoogleScholarGoogle Scholar |

Demir, R., Yaba, A., and Huppertz, B. (2010). Vasculogenesis and angiogenesis in the endometrium during menstrual cycle and implantation. Acta Histochem. 112, 203–214.
Vasculogenesis and angiogenesis in the endometrium during menstrual cycle and implantation.Crossref | GoogleScholarGoogle Scholar |

Denkert, C., Fürstenberg, A., Daniel, P. T., Koch, I., Köbel, M., Weichert, W., Siegert, A., and Hauptmann, S. (2003). Induction of G0/G1 cell cycle arrest in ovarian carcinoma cells by the anti-inflammatory drug NS-398, but not by COX-2-specific RNA interference. Oncogene 22, 8653–8661.
Induction of G0/G1 cell cycle arrest in ovarian carcinoma cells by the anti-inflammatory drug NS-398, but not by COX-2-specific RNA interference.Crossref | GoogleScholarGoogle Scholar |

Etich, J., Holzer, T., Pitzler, L., Bluhm, B., and Brachvogel, B. (2015). MiR-26a modulates extracellular matrix homeostasis in cartilage. Matrix Biol. 43, 27–34.
MiR-26a modulates extracellular matrix homeostasis in cartilage.Crossref | GoogleScholarGoogle Scholar |

Gargett, C. E., Lederman, F., Heryanto, B., Gambino, L. S., and Rogers, P. A. W. (2001). Focal vascular endothelial growth factor correlates with angiogenesis in human endometrium. Role of intravascular neutrophils. Hum. Reprod. 16, 1065–1075.
Focal vascular endothelial growth factor correlates with angiogenesis in human endometrium. Role of intravascular neutrophils.Crossref | GoogleScholarGoogle Scholar |

Gerstenberg, C., Allen, W. R., and Stewart, F. (1999). Cell proliferation patterns in the equine endometrium throughout the non-pregnant reproductive cycle. J. Reprod. Fertil. 116, 167–175.
Cell proliferation patterns in the equine endometrium throughout the non-pregnant reproductive cycle.Crossref | GoogleScholarGoogle Scholar |

Hansen, T. B., Jensen, T. I., Clausen, B. H., Bramsen, J. B., Finsen, B., Damgaard, C. K., and Kjems, J. (2013). Natural RNA circles function as efficient microRNA sponges. Nature 495, 384–388.
Natural RNA circles function as efficient microRNA sponges.Crossref | GoogleScholarGoogle Scholar |

He, Q., Tian, L., Jiang, H., Zhang, J., Li, Q., Sun, Y., Zhao, J., Li, H., and Liu, M. (2017). Identification of laryngeal cancer prognostic biomarkers using an inflammatory gene-related, competitive endogenous RNA network. Oncotarget 8, 9525.
Identification of laryngeal cancer prognostic biomarkers using an inflammatory gene-related, competitive endogenous RNA network.Crossref | GoogleScholarGoogle Scholar |

Heryanto, B., and Rogers, P. A. (2002). Regulation of endometrial endothelial cell proliferation by oestrogen and progesterone in the ovariectomized mouse. Reproduction 123, 107–113.
Regulation of endometrial endothelial cell proliferation by oestrogen and progesterone in the ovariectomized mouse.Crossref | GoogleScholarGoogle Scholar |

Igwebuike, U. M, (2009). A review of uterine structural modifications that influence conceptus implantation and development in sheep and goats. Anim. Reprod. Sci. 112, 1–7.
A review of uterine structural modifications that influence conceptus implantation and development in sheep and goats.Crossref | GoogleScholarGoogle Scholar |

Isayama, K., Zhao, L., Chen, H., Yamauchi, N., Shigeyoshi, Y., Hashimoto, S., and Hattori, M. A. (2015). Removal of Rev-erbα inhibition contributes to the prostaglandin G/H synthase 2 expression in rat endometrial stromal cells. Am. J. Physiol. Endocrinol. Metab. 308, E2462–E2467.
Removal of Rev-erbα inhibition contributes to the prostaglandin G/H synthase 2 expression in rat endometrial stromal cells.Crossref | GoogleScholarGoogle Scholar |

Jiang, D. S., Wang, Y. W., Jiang, J., Li, S. M., Liang, S. Z., and Fang, H. Y. (2014). MicroRNA-26a involved in Toll-like receptor 9-mediated lung cancer growth and migration. Int. J. Mol. Med. 34, 307–312.
MicroRNA-26a involved in Toll-like receptor 9-mediated lung cancer growth and migration.Crossref | GoogleScholarGoogle Scholar |

Kaeoket, K., Persson, E., and Dalin, A. M. (2001). The sow endometrium at different stages of the oestrous cycle: studies on morphological changes and infiltration by cells of the immune system. Anim. Reprod. Sci. 65, 95–114.
The sow endometrium at different stages of the oestrous cycle: studies on morphological changes and infiltration by cells of the immune system.Crossref | GoogleScholarGoogle Scholar |

Kaufmann, P., Mayhew, T. M., and Charnock-Jones, D. S. (2004). Aspects of human fetoplacental vasculogenesis and angiogenesis. II. Changes during normal pregnancy. Placenta 25, 114–126.
Aspects of human fetoplacental vasculogenesis and angiogenesis. II. Changes during normal pregnancy.Crossref | GoogleScholarGoogle Scholar |

Lim, H., Paria, B. C., Das, S. K., Dinchuk, J. E., Langenbach, R., Trzaskos, J. M., and Dey, S. K. (1997). Multiple female reproductive failures in cyclooxygenase 2-deficient mice. Cell 91, 197–208.
Multiple female reproductive failures in cyclooxygenase 2-deficient mice.Crossref | GoogleScholarGoogle Scholar |

Liu, C. Q., Yuan, Y., and Wang, Z. X. (2001). Effects of leukaemia inhibitory factor on endometrial receptivity and its hormonal regulation in rabbits. Cell Biol. Int. 25, 1029–1032.
Effects of leukaemia inhibitory factor on endometrial receptivity and its hormonal regulation in rabbits.Crossref | GoogleScholarGoogle Scholar |

Liu, X., Zhang, L., Liu, Y., Cui, J., Che, S., An, X., Song, Y., and Cao, B. (2018). Circ-8073 regulates CEP55 by sponging miR-449a to promote caprine endometrial epithelial cells proliferation via the PI3K/AKT/mTOR pathway. BBA-MCR 1865, 1130–1147.
Circ-8073 regulates CEP55 by sponging miR-449a to promote caprine endometrial epithelial cells proliferation via the PI3K/AKT/mTOR pathway.Crossref | GoogleScholarGoogle Scholar |

Martín, H., Flández, M., Nombela, C., and Molina, M. (2005). Protein phosphatases in MAPK signalling: we keep learning from yeast. Mol. Microbiol. 58, 6–16.
Protein phosphatases in MAPK signalling: we keep learning from yeast.Crossref | GoogleScholarGoogle Scholar |

Miravet-Valenciano, J. A., Rinconbertolin, A., Vilella, F., and Simon, C. (2015). Understanding and improving endometrial receptivity. Curr. Opin. Obstet. Gynecol. 27, 187–192.
Understanding and improving endometrial receptivity.Crossref | GoogleScholarGoogle Scholar |

Nawaz, S., Lynch, M. P., Galand, P., and Gerschenson, L. E. (1987). Hormonal regulation of cell death in rabbit uterine epithelium. Am. J. Pathol. 127, 51–59.

Otsuki, Y. (2001). Apoptosis in human endometrium: apoptotic detection methods and signaling. Med. Electron Microsc. 34, 166–173.

Reuland, S. N., Smith, S. M., Bemis, L. T., Goldstein, N. B., Almeida, A. R., Partyka, K. A., Marquez, V. E., Zhang, Q., Norris, D. A., and Shellman, Y. G. (2013). MicroRNA-26a is strongly downregulated in melanoma and induces cell death through repression of silencer of death domains (SODD). J. Invest. Dermatol. 133, 1286–1293.
MicroRNA-26a is strongly downregulated in melanoma and induces cell death through repression of silencer of death domains (SODD).Crossref | GoogleScholarGoogle Scholar |

Revel, A., Achache, H., Stevens, J., Smith, Y., and Reich, R. (2011). MicroRNAs are associated with human embryo implantation defects. Hum. Reprod. 26, 2830–2840.
MicroRNAs are associated with human embryo implantation defects.Crossref | GoogleScholarGoogle Scholar |

Simmons, D. G., and Kennedy, T. G. (2002). Uterine sensitization-associated gene-1: a novel gene induced within the rat endometrium at the time of uterine receptivity/sensitization for the decidual cell reaction. Biol. Reprod. 67, 1638–1645.
Uterine sensitization-associated gene-1: a novel gene induced within the rat endometrium at the time of uterine receptivity/sensitization for the decidual cell reaction.Crossref | GoogleScholarGoogle Scholar |

Song, Y., An, X., Zhang, L., Fu, M., Peng, J., Han, P., Hou, J., Zhou, Z., and Cao, B. (2015). Identification and profiling of microRNAs in goat endometrium during embryo implantation. PLoS One 10, e0122202.
Identification and profiling of microRNAs in goat endometrium during embryo implantation.Crossref | GoogleScholarGoogle Scholar |

Subramaniam, K. S., Omar, I. S., Kwong, S. C., Mohamed, Z., Woo, Y. L., Mat Adenan, N. A., and Chung, I. (2016). Cancer-associated fibroblasts promote endometrial cancer growth via activation of interleukin-6/STAT-3/c-Myc pathway. Am. J. Cancer Res. 6, 200–213.

Suzuki, H. I., Yamagata, K., Sugimoto, K., Iwamoto, T., Kato, S., and Miyazono, K. (2009). Modulation of microRNA processing by p53. Nature 460, 529–533.
Modulation of microRNA processing by p53.Crossref | GoogleScholarGoogle Scholar |

Sukjumlong, S., Persson, E., Kaeoket, K., and Dalin, A-M. (2004). Immunohistochemical studies on oestrogen receptor alpha (ERalpha) and the proliferative marker Ki-67 in the sow uterus at oestrus and early pregnancy. Reprod. Domest. Anim. 39, 361–369.
Immunohistochemical studies on oestrogen receptor alpha (ERalpha) and the proliferative marker Ki-67 in the sow uterus at oestrus and early pregnancy.Crossref | GoogleScholarGoogle Scholar |

Sukjumlong, S., Dalin, A. M., Sahlin, L., and Persson, E. (2005). Immunohistochemical studies on the progesterone receptor (PR) in the sow uterus during the oestrous cycle and in inseminated sows at oestrus and early pregnancy. Reproduction 129, 349–359.
Immunohistochemical studies on the progesterone receptor (PR) in the sow uterus during the oestrous cycle and in inseminated sows at oestrus and early pregnancy.Crossref | GoogleScholarGoogle Scholar |

Talbi, S., Hamilton, A. E., Vo, K. C., Tulac, S., Overgaard, M. T., Dosiou, C., Le, S. N., Nezhat, C. N., Kempson, R., and Lessey, B. A. (2006). Molecular phenotyping of human endometrium distinguishes menstrual cycle phases and underlying biological processes in normo-ovulatory women. Endocrinology 147, 1097–1121.
Molecular phenotyping of human endometrium distinguishes menstrual cycle phases and underlying biological processes in normo-ovulatory women.Crossref | GoogleScholarGoogle Scholar |

Tamura, I., Sato, S., Okada, M., Tanabe, M., Lee, L., Maekawa, R., Asada, H., Yamagata, Y., Tamura, H., and Sugino, N. (2014). Importance of C/EBPβ binding and histone acetylation status in the promoter regions for induction of IGFBP-1, PRL, and Mn-SOD by cAMP in human endometrial stromal cells. Endocrinology 155, 275–286.
Importance of C/EBPβ binding and histone acetylation status in the promoter regions for induction of IGFBP-1, PRL, and Mn-SOD by cAMP in human endometrial stromal cells.Crossref | GoogleScholarGoogle Scholar |

Tang, C. M., Zhang, M., Huang, L., Hu, Z. Q., Zhu, J. N., Xiao, Z., Zhang, Z., Lin, Q. X., Zheng, X. L., and Yang, M. (2017). CircRNA_000203 enhances the expression of fibrosis-associated genes by derepressing targets of miR-26b-5p, Col1a2 and CTGF, in cardiac fibroblasts. Sci. Rep. 7, 40342.
CircRNA_000203 enhances the expression of fibrosis-associated genes by derepressing targets of miR-26b-5p, Col1a2 and CTGF, in cardiac fibroblasts.Crossref | GoogleScholarGoogle Scholar |

Van Cruchten, S., Van den Broeck, W., Duchateau, L., and Simoens, P. (2003). Apoptosis in the canine endometrium during the estrous cycle. Theriogenology 60, 1595–1608.
Apoptosis in the canine endometrium during the estrous cycle.Crossref | GoogleScholarGoogle Scholar |

Vilella, F., Ramirez, L., Berlanga, O., Martínez, S., Alamá, P., Meseguer, M., Pellicer, A., and Simón, C. (2013). PGE2 and PGF2α concentrations in human endometrial fluid as biomarkers for embryonic implantation. J. Clin. Endocrinol. Metab. 98, 4123–4132.
PGE2 and PGF2α concentrations in human endometrial fluid as biomarkers for embryonic implantation.Crossref | GoogleScholarGoogle Scholar |

Wang, Y., Xue, S., Liu, X., Liu, H., Hu, T., Qiu, X., Zhang, J., and Lei, M. (2016). Analyses of long non-coding RNA and mRNA profiling using RNA sequencing during the pre-implantation phases in pig endometrium. Sci. Rep. 6, 20238.
Analyses of long non-coding RNA and mRNA profiling using RNA sequencing during the pre-implantation phases in pig endometrium.Crossref | GoogleScholarGoogle Scholar |

Wang, Y., Tao, H., Wu, L., Liu, X., Xue, S., and Lei, M. (2017). Identification of non-coding and coding RNAs in porcine endometrium. Genomics 109, 43–50.
Identification of non-coding and coding RNAs in porcine endometrium.Crossref | GoogleScholarGoogle Scholar |

Wasowska, B., Ludkiewicz, B., Stefańczyk-Krzymowska, S., Grzegorzewski, W., and Skipor, J. (2001). Apoptotic cell death in the porcine endometrium during the oestrous cycle. Acta Vet. Hung. 49, 71–79.
Apoptotic cell death in the porcine endometrium during the oestrous cycle.Crossref | GoogleScholarGoogle Scholar |

Wu, Y., Zhang, Y., Zhang, Y., and Wang, J. J. (2017). CircRNA hsa_circ_0005105 up regulates NAMPT expression and promotes chondrocyte extracellular matrix degradation by sponging miR-26a. Cell Biology International 41, 1283–1289.
CircRNA hsa_circ_0005105 up regulates NAMPT expression and promotes chondrocyte extracellular matrix degradation by sponging miR-26a.Crossref | GoogleScholarGoogle Scholar |

Yoon, S., and Seger, R. (2006). The extracellular signal-regulated kinase: multiple substrates regulate diverse cellular functions. Growth Factors 24, 21–44.
The extracellular signal-regulated kinase: multiple substrates regulate diverse cellular functions.Crossref | GoogleScholarGoogle Scholar |

Zanatta, A., Rocha, A. M., Carvalho, F. M., Pereira, R. M. A., Taylor, H. S., Motta, E. L. A., Baracat, E. C., and Serafini, P. C. (2010). The role of the Hoxa10/HOXA10 gene in the etiology of endometriosis and its related infertility: a review. J. Assist. Reprod. Genet. 27, 701–710.
The role of the Hoxa10/HOXA10 gene in the etiology of endometriosis and its related infertility: a review.Crossref | GoogleScholarGoogle Scholar |

Zhang, L., Zhou, Z. Q., Li, G., and Fu, M. Z. (2013). The effect of deposition Se on the mRNA expression levels of GPxs in goats from a Se-enriched county of China. Biol. Trace Elem. Res. 156, 111–123.
The effect of deposition Se on the mRNA expression levels of GPxs in goats from a Se-enriched county of China.Crossref | GoogleScholarGoogle Scholar |

Zhang, L., Wang, Y., Fu, M., Li, G., An, N., Li, S., and Zhou, Z. (2014). The effects of ovariectomy on meat performance and expression of GH/IGF-I in young goats. Can. J. Anim. Sci. 94, 619–626.
The effects of ovariectomy on meat performance and expression of GH/IGF-I in young goats.Crossref | GoogleScholarGoogle Scholar |

Zhang, D., Dong, C., Tao, L., Zhang, Y., Chen, Z. J., and Cong, Z. (2015a). Dysfunction of liver receptor Homolog-1 in decidua: possible relevance to the pathogenesis of preeclampsia. PLoS One 10, e0145968.
Dysfunction of liver receptor Homolog-1 in decidua: possible relevance to the pathogenesis of preeclampsia.Crossref | GoogleScholarGoogle Scholar |

Zhang, L., An, X. P., Liu, X. R., Fu, M. Z., Han, P., Peng, J. Y., Hou, J. X., Zhou, Z. Q., Cao, B. Y., and Song, Y. X. (2015b). Characterization of the transcriptional complexity of the receptive and pre-receptive endometria of dairy goats. Sci. Rep. 5, 14244.
Characterization of the transcriptional complexity of the receptive and pre-receptive endometria of dairy goats.Crossref | GoogleScholarGoogle Scholar |

Zhang, L., Wang, Y., Zhou, Z., Fu, M., Li, G., Peng, F., and Wan, L. (2015c). Fatty acid composition and mRNA expression levels of lipid-metabolic genes in the muscles of ovariectomised young goats. Anim. Prod. Sci. 56, 1585–1592.

Zhang, Y., Qin, W., Zhang, L., Wu, X., Du, N., Hu, Y., Li, X., Shen, N., Xiao, D., and Zhang, H. (2015d). MicroRNA-26a prevents endothelial cell apoptosis by directly targeting TRPC6 in the setting of atherosclerosis. Sci. Rep. 5, 9401.

Zhang, L., Liu, X. R., Han, P., Zhou, Z. Q., Cao, B. Y., and Song, Y. X. (2017a). The study of endometrium at gestational days 5 and 15 in dairy goats (Capra hircus). Czech J. Anim. Sci. 62, 358–367.
The study of endometrium at gestational days 5 and 15 in dairy goats (Capra hircus).Crossref | GoogleScholarGoogle Scholar |

Zhang, L., Liu, X. R., Liu, J. Z., Song, Y. X., Zhou, Z. Q., and Cao, B. Y. (2017b). miR-182 selectively targets HOXA10 in goat endometrial epithelium cells in vitro. Reproduction in domestic animals 52, 1081–1092.
miR-182 selectively targets HOXA10 in goat endometrial epithelium cells in vitro.Crossref | GoogleScholarGoogle Scholar |

Zhang, L., Liu, X., Liu, J., Ma, X., Zhou, Z., Song, Y., and Cao, B. (2018). miR-26a promoted endometrial epithelium cells (EECs) proliferation and induced stromal cells (ESCs) apoptosis via the PTEN–PI3K/AKT pathway in dairy goats. J. Cell. Physiol. 233, 4688–4706.
miR-26a promoted endometrial epithelium cells (EECs) proliferation and induced stromal cells (ESCs) apoptosis via the PTEN–PI3K/AKT pathway in dairy goats.Crossref | GoogleScholarGoogle Scholar |

Zhou, J., Ju, W. Q., Yuan, X. P., Zhu, X. F., Wang, D. P., and He, X. S. (2016). miR-26a regulates mouse hepatocyte prolifera-tion via directly targeting the 3′ untranslated region of CCND2 and CCNE2. Hepatobiliary Pancreat. Dis. Int. 15, 65–72.
miR-26a regulates mouse hepatocyte prolifera-tion via directly targeting the 3′ untranslated region of CCND2 and CCNE2.Crossref | GoogleScholarGoogle Scholar |