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Expression of lncRNA TINCR in the placenta of patients with pre-eclampsia and its effect on the biological behaviours of trophoblasts

Published online by Cambridge University Press:  28 June 2021

Li Qin ,
Qin Yang ,
Zhiyi Fei  and
Dandan Zhang Open the ORCID record for Dandan Zhang [Opens in a new window]
Li Qin
Affiliation:
Obstetrics Department, Puren Hospital affiliated to Wuhan University of Science and Technology, Wuhan City, Hubei Province 430081, China
Qin Yang
Affiliation:
Reproductive Medicine Section, Puren Hospital affiliated to Wuhan University of Science and Technology, Wuhan City, Hubei Province 430081, China
Zhiyi Fei
Affiliation:
Obstetrics Department, Puren Hospital affiliated to Wuhan University of Science and Technology, Wuhan City, Hubei Province 430081, China
Dandan Zhang*
Affiliation:
Reproductive Medicine Section, Puren Hospital affiliated to Wuhan University of Science and Technology, Wuhan City, Hubei Province 430081, China
*
Author for correspondence: Dandan Zhang. Reproductive Medicine Section, Puren Hospital, affiliated to Wuhan University of Science and Technology, No. 1 Benxi Street, Qingshan District, Wuhan, 430081, Hubei Province, China. Tel: +86 27 86857375. E-mail: Zdandan0902@163.com
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Summary

To explore the effect of lncRNA TINCR on the biological behaviours of trophoblasts, we detected and analyzed the expression of terminal differentiation-induced non-protein coding RNA (TINCR) in the placenta tissues of pre-eclamptic and non-pre-eclamptic pregnant women. The gain- and loss-of-function of TINCR was performed to examine the proliferation, migration and invasion abilities of Htr-8/Svneo cells. The levels of epithelial–mesenchymal transition (EMT)-related proteins, cyclin and Wnt/β-catenin pathway were detected. High expression of lncRNA TINCR appeared in placental tissues of patients with pre-eclampsia. The proliferation, invasion and migration of Htr-8/Svneo cells were promoted by TINCR downregulation; the cells were transited from G0/G1 to S phase; and EMT was promoted and the Wnt/β-catenin pathway was activated. In summary, the downregulation of lncRNA TINCR activated the Wnt/β-catenin pathway and promoted the proliferation, invasion and migration of Htr-8/Svneo cells. This study may provide a theoretical basis for treatment of patients with pre-eclampsia.

Keywords

Cell cycleEpithelial–mesenchymal transitionHtr-8/SvneoInvasion and migrationlncRNA TINCRPre-eclampsiaProliferationWnt/β-catenin
Type
Research Article
Information
Zygote , Volume 30 , Issue 1 , February 2022 , pp. 111 - 119
Copyright
© The Author(s), 2021. Published by Cambridge University Press

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References

Adon, AM, Zeng, X, Harrison, MK, Sannem, S, Kiyokawa, H, Kaldis, P and Saavedra, HI (2010). Cdk2 and Cdk4 regulate the centrosome cycle and are critical mediators of centrosome amplification in p53-null cells. Mol Cell Biol 30, 694–710.CrossRefGoogle ScholarPubMed
Alasztics, B, Kukor, Z, Panczel, Z and Valent, S (2012). [The pathophysiology of pre-eclampsia in view of the two-stage model]. Orv Hetil 153, 1167–76.CrossRefGoogle ScholarPubMed
Brown, LM, Lacey, HA, Baker, PN and Crocker, IP (2005). E-cadherin in the assessment of aberrant placental cytotrophoblast turnover in pregnancies complicated by pre-eclampsia. Histochem Cell Biol 124, 499–506.CrossRefGoogle ScholarPubMed
Burris, HH, Just, AC, Haviland, MJ, Neo, DT, Baccarelli, AA, Dereix, AE, Brennan, KJ, Rodosthenous, RS, Ralston, SJ, Hecht, JL and Hacker, MR (2018). Long noncoding RNA expression in the cervix mid-pregnancy is associated with the length of gestation at delivery. Epigenetics 13, 742–50.CrossRefGoogle ScholarPubMed
Chen, L, Wang, J, Fan, X, Zhang, Y, Zhoua, M, Li, X and Wang, L (2020). LASP2 inhibits trophoblast cell migration and invasion in pre-eclampsia through inactivation of the Wnt/beta-catenin signaling pathway. J Recept Signal Transduct Res 41, 67–73.CrossRefGoogle ScholarPubMed
Cheng, D, Jiang, S, Chen, J, Li, J, Ao, L and Zhang, Y (2019). The increased lncRNA MIR503HG in pre-eclampsia modulated trophoblast cell proliferation, invasion, and migration via regulating matrix metalloproteinases and NF-kappaB signaling. Dis Markers 2019, 4976845.CrossRefGoogle ScholarPubMed
DaSilva-Arnold, SC, Zamudio, S, Al-Khan, A, Alvarez-Perez, J, Mannion, C, Koenig, C, Luke, D, Perez, AM, Petroff, M, Alvarez, M and Illsley, NP (2018). Human trophoblast epithelial–mesenchymal transition in abnormally invasive placenta. Biol Reprod 99, 409–21.CrossRefGoogle ScholarPubMed
Fu, G, Ye, G, Nadeem, L, Ji, L, Manchanda, T, Wang, Y, Zhao, Y, Qiao, J, Wang, YL, Lye, S, Yang, BB and Peng, C (2013). MicroRNA-376c impairs transforming growth factor-beta and nodal signaling to promote trophoblast cell proliferation and invasion. Hypertension 61, 864–72.CrossRefGoogle ScholarPubMed
Garovic, VD (2000). Hypertension in pregnancy: diagnosis and treatment. Mayo Clin Proc 75, 1071–6.CrossRefGoogle ScholarPubMed
Ghafouri-Fard, S, Dashti, S, Taheri, M and Omrani, MD (2020). TINCR: An lncRNA with dual functions in the carcinogenesis process. Noncoding RNA Res 5, 109–115.CrossRefGoogle ScholarPubMed
Guo, F, Zhu, X, Zhao, Q and Huang, Q (2020). miR5893p sponged by the lncRNA TINCR inhibits the proliferation, migration and invasion and promotes the apoptosis of breast cancer cells by suppressing the Akt pathway via IGF1R. Int J Mol Med 46, 989–1002.CrossRefGoogle ScholarPubMed
Han, Y and Sun, G (2020). Overexpression of lncRNA TINCR is associated with high-grade, invasive, and recurring tumors, and facilitates proliferation in vitro and in vivo of urothelial carcinoma of the bladder. Urol Oncol 38, 738.e1–e8.CrossRefGoogle ScholarPubMed
He, X, He, Y, Xi, B, Zheng, J, Zeng, X, Cai, Q, Ouyang, Y, Wang, C, Zhou, X, Huang, H, Deng, W, Xin, S, Huang, Q and Liu, H (2013). LncRNAs expression in pre-eclampsia placenta reveals the potential role of LncRNAs contributing to pre-eclampsia pathogenesis. PLoS One 8, e81437.CrossRefGoogle Scholar
Hou, A, Zhang, Y, Zheng, Y, Fan, Y, Liu, H and Zhou, X (2019). LncRNA terminal differentiation-induced ncRNA (TINCR) sponges miR-302 to upregulate cyclin D1 in cervical squamous cell carcinoma (CSCC). Hum Cell 32, 515–21.CrossRefGoogle Scholar
Huppertz, B (2018). The critical role of abnormal trophoblast development in the etiology of pre-eclampsia. Curr Pharm Biotechnol 19, 771–80.CrossRefGoogle Scholar
Ji, L, Brkic, J, Liu, M, Fu, G, Peng, C and Wang, YL (2013). Placental trophoblast cell differentiation: physiological regulation and pathological relevance to pre-eclampsia. Mol Aspects Med 34, 981–1023.CrossRefGoogle Scholar
Jordan, NV, Johnson, GL and Abell, AN (2011). Tracking the intermediate stages of epithelial–mesenchymal transition in epithelial stem cells and cancer. Cell Cycle 10, 2865–73.CrossRefGoogle ScholarPubMed
Karimian, A, Ahmadi, Y and Yousefi, B (2016). Multiple functions of p21 in cell cycle, apoptosis and transcriptional regulation after DNA damage. DNA Repair (Amst) 42, 63–71.CrossRefGoogle ScholarPubMed
Kretz, M, Siprashvili, Z, Chu, C, Webster, DE, Zehnder, A, Qu, K, Lee, CS, Flockhart, RJ, Groff, AF, Chow, J, Johnston, D, Kim, GE, Spitale, RC, Flynn, RA, Zheng, GX, Aiyer, S, Raj, A, Rinn, JL, Chang, HY and Khavari, PA (2013). Control of somatic tissue differentiation by the long non-coding RNA TINCR. Nature 493, 231–5.CrossRefGoogle Scholar
Li, N, Huang, L, Li, Y, Chen, X, Yang, Y, Hou, Y and Qiao, C (2020). Lin28B/miR-92b promote the proliferation, migration, and invasion in the pathogenesis of pre-eclampsia via the DKK1/Wnt/beta-catenin pathway. Reprod Sci 27, 815–22.CrossRefGoogle ScholarPubMed
Li, Z, Zhou, X, Gao, W, Sun, M, Chen, H and Meng, T (2021). Circular RNA VRK1 facilitates pre-eclampsia progression via sponging miR-221–3P to regulate PTEN/Akt. J Cell Mol Med, doi: 10.1111/jcmm.16454. Epub ahead of print.CrossRefGoogle Scholar
Liu, B, Zhou, Z, Zhou, W, Liu, J, Zhang, Q, Xia, J, Liu, J, Chen, N, Li, M and Zhu, R (2014). Resveratrol inhibits proliferation in human colorectal carcinoma cells by inducing G1/S phase cell cycle arrest and apoptosis through caspase/cyclin CDK pathways. Mol Med Rep 10, 1697–702.CrossRefGoogle Scholar
Liu, N, Guo, YN, Gong, LK and Wang, BS (2021). Advances in biomarker development and potential application for pre-eclampsia based on pathogenesis. Eur J Obstet Gynecol Reprod Biol X 9, 100119.CrossRefGoogle Scholar
Livak, KJ and Schmittgen, TD (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25, 402–8.CrossRefGoogle Scholar
Long, W, Rui, C, Song, X, Dai, X, Xue, X, Lu, Y, Shen, R, Li, J, Li, J and Ding, H (2016). Distinct expression profiles of lncRNAs between early-onset pre-eclampsia and preterm controls. Clin Chim Acta 463, 193–9.CrossRefGoogle ScholarPubMed
Ma, X, Long, C, Wang, F, Lou, B, Yuan, M, Duan, F, Yang, Y, Li, J, Qian, X, Zeng, J, Lin, S, Shen, H and Lin, X (2021). METTL3 attenuates proliferative vitreoretinopathy and epithelial–mesenchymal transition of retinal pigment epithelial cells via Wnt/beta-catenin pathway. J Cell Mol Med 25, 4220–34.CrossRefGoogle ScholarPubMed
Ou, Y, Zhu, L, Wei, X, Bai, S, Chen, M, Chen, H and Zhang, J (2020). Circular RNA circ_0111277 attenuates human trophoblast cell invasion and migration by regulating miR-494/HTRA1/Notch-1 signal pathway in pre-eclampsia. Cell Death Dis 11, 479.CrossRefGoogle ScholarPubMed
Qi, H, Yao, C, Xing, J and Qin, Y (2021). Hypoxia-induced GPR4 suppresses trophoblast cell migration and proliferation through the MAPK signaling pathway. Reprod Toxicol 99, 1–8.CrossRefGoogle ScholarPubMed
Rana, S, Lemoine, E, Granger, JP and Karumanchi, SA (2019). Pre-eclampsia: pathophysiology, challenges, and perspectives. Circ Res 124, 1094–112.CrossRefGoogle ScholarPubMed
Rana, S, Burke, SD and Karumanchi, SA (2020). Imbalances in circulating angiogenic factors in the pathophysiology of pre-eclampsia and related disorders. Am J Obstet Gynecol S0002-9378(20)31196-0. doi: 10.1016/j.ajog.2020.10.022. Epub ahead of print.CrossRefGoogle Scholar
Safa, A, Gholipour, M, Dinger, ME, Taheri, M and Ghafouri-Fard, S (2020). The critical roles of lncRNAs in the pathogenesis of melanoma. Exp Mol Pathol 117, 104558.CrossRefGoogle ScholarPubMed
Sakowicz, A, Pietrucha, T, Rybak-Krzyszkowska, M, Huras, H, Gach, A, Sakowicz, B, Banaszczyk, M, Grzesiak, M and Biesiada, L (2017). Double hit of NEMO gene in pre-eclampsia. PLoS One 12, e0180065.CrossRefGoogle Scholar
Sakowicz, A, Bralewska, M, Pietrucha, T, Habrowska-Gorczynska, DE, Piastowska-Ciesielska, AW, Gach, A, Rybak-Krzyszkowska, M, Witas, PJ, Huras, H, Grzesiak, M and Biesiada, L (2020). Canonical, non-canonical and atypical pathways of nuclear factor kb activation in pre-eclampsia. Int J Mol Sci 21, 5574.CrossRefGoogle Scholar
Sze, SC, Wong, KL, Liu, WK, Ng, TB, Wong, JH, Cheung, HP, Yow, CM, Chu, ES, Qing, L, Hu, YM Tsang, KW, Lee, WS and Yao, T (2011). Regulation of p21, MMP-1, and MDR-1 expression in human colon carcinoma HT29 cells by Tian Xian liquid, a chinese medicinal formula, in vitro and in vivo. Integr Cancer Ther 10, 58–69.CrossRefGoogle ScholarPubMed
Wang, M, Liu, S, Wang, H, Tang, R and Chen, Z (2020). Morphine post-conditioning-induced up-regulation of lncRNA TINCR protects cardiomyocytes from ischemia-reperfusion injury via inhibiting degradation and ubiquitination of FGF1. QJM 113, 859–69.CrossRefGoogle ScholarPubMed
Wang, X, Li, S, Xiao, H and Deng, X (2020). Serum lncRNA TINCR serve as a novel biomarker for predicting the prognosis in triple-negative breast cancer. Technol Cancer Res Treat 19, 1533033820965574.CrossRefGoogle ScholarPubMed
Xie, D, Zhu, J, Liu, Q, Li, J, Song, M, Wang, K, Zhou, Q, Jia, Y and Li, T (2019). Dysregulation of HDAC9 represses trophoblast cell migration and invasion through TIMP3 activation in pre-eclampsia. Am J Hypertens 32, 515–23.CrossRefGoogle Scholar
Xue, P, Fan, W, Diao, Z, Li, Y, Kong, C, Dai, X, Peng, Y, Chen, L, Wang, H, Hu, Y and Hu, Z (2020). Up-regulation of PTEN via LPS/AP-1/NF-kappaB pathway inhibits trophoblast invasion contributing to pre-eclampsia. Mol Immunol 118, 182–90.CrossRefGoogle Scholar
Yang, X and Meng, T (2019). Long noncoding RNA in pre-eclampsia: transcriptional noise or innovative indicators? Biomed Res Int 2019, 5437621.Google ScholarPubMed
Zhang, Y, Cao, L, Jia, J, Ye, L, Wang, Y, Zhou, B and Zhou, R (2019). CircHIPK3 is decreased in pre-eclampsia and affects migration, invasion, proliferation, and tube formation of human trophoblast cells. Placenta 85, 1–8.CrossRefGoogle ScholarPubMed
Zhang, Z, Li, H, Zhang, L, Jia, L and Wang, P (2013). Differential expression of beta-catenin and Dickkopf-1 in the third trimester placentas from normal and preeclamptic pregnancies: a comparative study. Reprod Biol Endocrinol 11, 17.CrossRefGoogle ScholarPubMed
Zhang, Z, Wang, X, Zhang, L, Shi, Y, Wang, J and Yan, H (2017). Wnt/beta-catenin signaling pathway in trophoblasts and abnormal activation in pre-eclampsia. Mol Med Rep 16, 1007–13.CrossRefGoogle Scholar
Zheng, J, Huang, Y, Li, Y, Lai, J, Chen, C, Yi, C, Pang, F, Lan, Y, Xu, L and Fang, B (2020). lncRNA-TINCR functions as a competitive endogenous RNA to regulate the migration of mesenchymal stem cells by sponging miR-761. Biomed Res Int 2020, 9578730.Google ScholarPubMed
Zheng, W, Chen, A, Yang, H and Hong, L (2020). MicroRNA-27a inhibits trophoblast cell migration and invasion by targeting SMAD2: potential role in pre-eclampsia. Exp Ther Med 20, 2262–9.Google Scholar
Zhou, F, Sun, Y, Chi, Z, Gao, Q and Wang, H (2020). Long noncoding RNA SNHG12 promotes the proliferation, migration, and invasion of trophoblast cells by regulating the epithelial–mesenchymal transition and cell cycle. J Int Med Res 48, 300060520922339.CrossRefGoogle ScholarPubMed