Please wait a minute...
Journal of Integrative Agriculture  2020, Vol. 19 Issue (12): 3054-3064    DOI: 10.1016/S2095-3119(20)63441-4
Special Issue: 动物科学合辑Animal Science
Animal Science · Veterinary Medicine Advanced Online Publication | Current Issue | Archive | Adv Search |
The expression of Lin28B was co-regulated by H3K4me2 and Wnt5a/β-catenin/TCF7L2
ZHANG Ya-ni1, 2, HU Cai1, 2, WANG Ying-jie1, 2, ZUO Qi-sheng1, 2, LI Bi-chun1, 2 
1 Key Laboratory of Animal Breeding Reproduction and Molecular Design for Jiangsu Province, College of Animal Science and Technology, Yangzhou University, Yangzhou 225009, P.R.China
2 Joint International Research Laboratory of Agriculture and Agri-Product Safety of Ministry of Education, Yangzhou University, Yangzhou 225009, P.R.China
Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
Abstract  
Lin28A and Lin28B are homologous RNA-binding proteins that participate in the development of primordial germ cells.  The mechanisms underlying expression and regulation of Lin28A have been well documented, but such information for Lin28B is limited.  In this study, a fragment of the Lin28B promoter was cloned, the pEGFP-pLin28B vector was constructed.  DF-1 chicken fibroblasts were transfected and the expression of green fluorescent protein (GFP) was measured.  Furtherly, Lin28B promoter of different lengths fragments was cloned using the chromosome-walking method and the fragments were ligated into the PGL3-Basic vector, and transfected into DF-1 cells.  Results of dual-luciferase reporter assay showed that the core of the Lin28B promoter was included in the sequence from –1 431 to –1 034 bp.  The binding sites of the transcription factor TCF7L2 was showed within this sequence by bioinformatics analysis.  The promoter activity of Lin28B was downregulated (P<0.05) when the TCF7L2 binding site was mutated.  Further experiments suggested that Lin28B promoter activity responded to the activation or inhibition of Wnt signaling.  Results of chromatin immunoprecipitation and quantitative PCR showed that β-catenin-TCF7L2 may be enriched in the Lin28B promoter core area.  In vivo and in vitro activation or inhibition of Wnt signaling significantly up- or down-regulated (P<0.05) Lin28B expression.  H3K4me2 enriched in the promoter of Lin28B, which affected the regulation of Wnt signaling to Lin28B.  In conclusion, our results showed that H3K4me2 and Wnt5a/β-catenin/TCF7L2 were the positive regulators of Lin28B expression.  Findings of this study may lay a theoretical foundation for illuminating the mechanism underlying Lin28B expression.
Keywords:  primordial germ cells        Lin28B        promoter        H3K4me2        Wnt5a/β-catenin/TCF7L2  
Received: 15 May 2020   Accepted:
Fund: We thank the Experimental Poultry Farm of the Poultry Institute, Chinese Academy of Agricultural Sciences, for providing experimental materials. This work was supported by the Key Research and Development Program of China (2017YFE0108000), the National Natural Science Foundation of China (31872341, 31572390), and the High-Level Talent Support Program of Yangzhou University, China.
Corresponding Authors:  Correspondence ZUO Qi-sheng, Tel: +86-514-87997206, Fax: +86-514-87997206, E-mail: 006664@yzu.edu.cn; LI Bi-chun, Tel: +86-514-87977207, Fax: +86-514-87350440, E-mail: yubcli@yzu.edu.cn   
About author:  ZHANG Ya-ni, E-mail: ynzhang@yzu.edu.cn;

Cite this article: 

ZHANG Ya-ni, HU Cai, WANG Ying-jie, ZUO Qi-sheng, LI Bi-chun. 2020. The expression of Lin28B was co-regulated by H3K4me2 and Wnt5a/β-catenin/TCF7L2. Journal of Integrative Agriculture, 19(12): 3054-3064.

Aramak S, Hayashi K, Kurimoto K, Ohta H, Yabuta Y, Iwanari H, Mochizuki Y, Hamakubo T, Kato Y, Shirahige K, Saitou M. 2013. A mesodermal factor, T, specifies mouse germ cell fate by directly activating germline determinants. Develop Cell, 27, 516–529.
Beshir A, Ren G, Magpusao A, Barone L, Yeung K, Fenteany G. 2010. Raf kinase inhibitor protein suppresses nuclear factor-κB-dependent cancer cell invasion through negative regulation of matrix metalloproteinase expression. Cancer Letters, 299, 137–149.
Bialecka M, Young T, Chuva S, Berge D, Sanders A, Beck F, Deschamps J. 2012. Cdx2 contributes to the expansion of the early primordial germ cell population in the mouse. Developmental Biology, 371, 227–234.
Billin A, Thirlwell H, Ayer D. 2000. Beta-catenin-histone deacetylase interactions regulate the transition of LEF1 from a transcriptional repressor to an activator. Molecular and Cellular Biology, 20, 6882–6890.
Cantú A, Altshuler-Keylin S, Laird D. 2016. Discrete somatic niches coordinate proliferation and migration of primordial germ cells via Wnt signaling. Journal of Cell Biology, 214, 215–229.
Cervantes S, Yamaguchi T, Hebrok M. 2009. Wnt5a is essential for intestinal elongation in mice. Developmental Biology, 326, 285–294.
Childs A, Kinnell H, He J, Anderson R. 2012. LIN28 is selectively expressed by primordial and pre-meiotic germ cells in the human fetal ovary. Stem Cells and Development, 21, 2343–2349.
Dahl J, Jung I, Aanes H, Greggains G, Manaf A, Lerdrup M, Li G, Kuan S, Li B, Lee A, Preissl S, Jermstad I, Haugen M, Suganthan R, Bjørås M, Hansen K, Dalen K, Fedorcsak P, Ren B, Klungland A. 2016. Broad histone H3K4me3 domains in mouse oocytes modulate maternal-to-zygotic transition. Nucleic Acids Research, 537, 548–552.
Desjardins A, Bouvette J, Legault P. 2014. Stepwise assembly of multiple Lin28 proteins on the terminal loop of let-7 miRNA precursors. Nucleic Acids Research, 42, 4615–4628.
El-Khairi R, Parnaik R, Duncan A, Lin L, Gerrelli D, Dattani M, Conway G, Achermann J. 2012. Analysis of Lin28A in early human ovary development and as a candidate gene for primary ovarian insufficiency. Molecular and Cellular Endocrinology, 351, 264–268.
Graf R, Munschauer M, Mastrobuoni G, Mayr F, Heinemann U, Kempa S, Rajewsky N, Landthale M. 2013. Identification of LIN28B-bound mRNAs reveals features of target recognition and regulation. RNA Biology, 10, 1146–1159.
Hayashi K, Yoshida K, Matsui Y. 2005. A histone H3 methyltransferase controls epigenetic events required for meiotic prophase. Nature, 438, 374–378.
Hecht A, Vleminckx K, Stemmler M, Roy F, Kemler R. 2000. The p300/CBP acetyltransferases function as transcriptional coactivators of beta-catenin in vertebrates. Embo Journal, 19, 1839–1850.
Iliopoulos D, Hirsch H, Struhl K. 2009. An epigenetic switch involving NF-kappaB, Lin28, Let-7 microRNA, and IL6 links inflammation to cell transformation. Cell, 139, 693–706.
Jaenisch R, Bird A. 2003. Epigenetic regulation of gene expression: How the genome integrates intrinsic and environmental signals. Nature Genetic, 33, 245–254.
Jiang J, Lan C, Li L, Yang D, Xia X, Liao Q, Fu W, Chen X, An S, Wang W E, Zeng C. 2018. A novel porcupine inhibitor blocks WNT pathways and attenuates cardiac hypertrophy. Biochim Biochimica et Biophysica Acta (Molecular Basis of Disease), 1864, 3459–3467.
Margueron R, Trojer P, Reinberg D. 2005. The key to development: Interpreting the histone code? Current Opinion in Genetics & Development, 15, 163–176.
Maruyama R, Shimizu M, Li J, Inoue J, Sato R. 2016. Fibroblast growth factor 21 induction by activating transcription factor 4 is regulated through three amino acid response elements in its promoter region. Bioscience, Biotechnology, and Biochemistry, 80, 929–934.
Moss E G, Lee R C, Ambros V. 1997. The cold shock domain protein LIN-28 controls developmental timing in C. elegans and is regulated by the lin-4 RNA. Cell, 88, 637–646.
Murray M J, Saini H K, Siegler C A, Hanning J E, Barker E M, van Dongen S, Ward D M, Raby K L, Groves I J, Scarpini C G, Pett M R, Thornton C M, Enright A J, Nicholson J C, Coleman N. 2013. LIN28 expression in malignant germ cell tumors downregulates let-7 and increases oncogene levels. Cancer Research, 73, 4872–4884.
Noh K M, Wang H, Kim H, Wenderski W, Fang F, Li C, Dewell S, Hughes S, Melnick A, Patel D, Li H, Allis C. 2018. Engineering of a histone-recognition domain in Dnmt3a alters the epigenetic landscape and phenotypic features of mouse ESCs. Molecular Cell, 69, 533–540.
Pedersen A, Baldi P, Chauvin Y, Brunak S. 1999. The biology of eukaryotic promoter prediction - a review. Computers & chemistry, 23, 191–207.
Tsukamoto K, Saito S, Saeki S, Sato T, Tanimura N, Isobe T, Mase M, Imada T, Yuasa N, Yamaguchi S. 2002. Complete, long-lasting protection against lethal infectious bursal disease virus challenge by a single vaccination with an avian herpesvirus vector expressing VP2 antigens. Journal of Virology, 76, 5637–5645.
Urbach A, Yermalovich A, Zhang J, Spina C S, Zhu H, Perez-Atayde A, Shukrun R, Charlton J, Sebire N, Mifsud W, Dekel B, Pritchard-Jones K, Daley G. 2014. Lin28 sustains early renal progenitors and induces Wilms tumor. Genes & Development, 28, 971–982.
Wang X, Wang Q, Wang J, Bai P, Shi L, Shen W, Zhou M, Zhou X, Zhang Y, Cai M. 2016. Mit1 transcription factor mediates methanol signaling and regulates the alcohol oxidase 1 (AOX1) promoter in Pichia pastoris. Journal of Biological Chemistry, 291, 6245–6261.
West J, Viswanathan S, Yabuuchi A, Cunniff K, Takeuchi A, Park I, Sero J, Zhu H, Perez-Atayde A, Frazier A, Surani M, Daley G. 2009. A role for Lin28 in primordial germ-cell development and germ-cell malignancy. Nature, 460, 909–913.
Yang M, Yang S, Herrlinger S, Liang C, Dzieciatkowska M, Hansen K, Desai R, Nagy A, Niswander L, Moss E, Chen J. 2015. Lin28 promotes the proliferative capacity of neural progenitor cells in brain development. Development, 142, 1616–1627.
Yoshimoto N, Takahashi H, Smith FW, Yamaya T, Saito K. 2002. Two distinct high-affinity sulfate transporters with different inducibilities mediate uptake of sulfate in Arabidopsis roots. The Plant Journal, 29, 465–473.
Zhang B, Zheng H, Huang B, Li W, Xiang Y, Peng X, Ming J, Wu X, Zhang Y, Xu Q, Liu W, Kou X, Zhao Y, He W, Li C, Chen B, Li Y, Wang Q, Ma J, Yin Q, et al. 2016. Allelic reprogramming of the histone modification H3K4me3 in early mammalian development. Nature, 537, 553–557.
Zhang E, Han L, Yin D, He X, Hong L, Si X, Qiu M, Xu T, De W, Xu L, Shu Y, Chen J. 2017. H3K27 acetylation activated-long non-coding RNA CCAT1 affects cell proliferation and migration by regulating SPRY4 and HOXB13 expression in esophageal squamous cell carcinoma. Nucleic Acids Research, 45, 3086–3101.
[1] WU Yan-qing, ZHU Meng-yuan, JIANG Yu, ZHAO Da-qiu, TAO Jun. Molecular characterization of chalcone isomerase (CHI) regulating flower color in herbaceous peony (Paeonia lactiflora Pall.)[J]. >Journal of Integrative Agriculture, 2018, 17(01): 122-129.
[2] WANG Hao-jie, JIANG Yong-hua, QI Ying-wei, DAI Jie-yu, LIU Yan-li, ZHU Xian-bo, LIU Cui-hua, Lü Yan-rong, REN Xiao-lin . Identification and functional characterization of the MdHB-1 gene promoter sequence from Malus×domestica[J]. >Journal of Integrative Agriculture, 2017, 16(08): 1730-1741.
[3] XU Yuan, ZHANG Ai-ling, XIAO Guang, ZHANG Zhe, CHEN Zan-mou, ZHANG Hao, LI Jia-qi. p53 and NFκB regulate microRNA-34c expression in porcine ovarian granulosa cells[J]. >Journal of Integrative Agriculture, 2016, 15(8): 1816-1824.
[4] XU Yuan-yuan, WANG Jing, NIE Shan-shan, HUANG Dan-qiong, WANG Yan, XU Liang, WANG Rong-hua, LUO Xiao-bo, LIU Li-wang. Isolation and molecular characterization of the FLOWERING LOCUS C gene promoter sequence in radish (Raphanus sativus L.)[J]. >Journal of Integrative Agriculture, 2016, 15(4): 763-774.
No Suggested Reading articles found!