A SnoRNA-derived piRNA interacts with human interleukin-4 pre-mRNA and induces its decay in nuclear exosomes

被引:114
作者
Zhong, Fudi [1 ,2 ,3 ]
Zhou, Nan [1 ,2 ,3 ]
Wu, Kang [1 ,2 ,3 ]
Guo, Yubiao [4 ,5 ]
Tan, Weiping [6 ]
Zhang, Hong [1 ,2 ,3 ]
Zhang, Xue [1 ,2 ,3 ]
Geng, Guannan [1 ,2 ,3 ]
Pan, Ting [1 ,2 ,3 ]
Luo, Haihua [1 ,2 ,3 ]
Zhang, Yijun [1 ,2 ,3 ]
Xu, Zhibin [1 ,2 ,3 ]
Liu, Jun [1 ,2 ,3 ]
Liu, Bingfeng [1 ,2 ,3 ]
Gao, Wenchao [1 ,2 ,3 ]
Liu, Chao [1 ,2 ,3 ]
Ren, Liangliang [1 ,2 ,3 ]
Li, Jun [1 ,2 ,3 ]
Zhou, Jie [1 ,2 ,3 ]
Zhang, Hui [1 ,2 ,3 ]
机构
[1] Sun Yat Sen Univ, Zhongshan Sch Med, Inst Human Virol, Guangzhou 510080, Guangdong, Peoples R China
[2] Sun Yat Sen Univ, Zhongshan Sch Med, Key Lab Trop Dis Control, Minist Educ China, Guangzhou 510080, Guangdong, Peoples R China
[3] Sun Yat Sen Univ, Zhongshan Sch Med, Guangdong Engn Res Ctr Antimicrobial Agent & Immu, Guangzhou 510080, Guangdong, Peoples R China
[4] Sun Yat Sen Univ, Affiliated Hosp 1, Div Resp, Guangzhou 510080, Guangdong, Peoples R China
[5] Sun Yat Sen Univ, Affiliated Hosp 1, Med Intens Care Unit, Guangzhou 510080, Guangdong, Peoples R China
[6] Sun Yat Sen Univ, Sun Yat Sen Mem Hosp, Dept Pediat, Guangzhou 510080, Guangdong, Peoples R China
关键词
NOVO DNA METHYLATION; PIWI PROTEINS; DROSOPHILA-MELANOGASTER; CHROMATIN STATE; GENE-EXPRESSION; MOUSE GERMLINE; NONCODING RNA; CANCER-CELLS; 3' TERMINI; IDENTIFICATION;
D O I
10.1093/nar/gkv954
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
PIWI interacting RNAs (piRNAs) are highly expressed in germline cells and are involved in maintaining genome integrity by silencing transposons. These are also involved in DNA/histone methylation and gene expression regulation in somatic cells of invertebrates. The functions of piRNAs in somatic cells of vertebrates, however, remain elusive. We found that snoRNA-derived and C (C')/D' (D)-box conserved piRNAs are abundant in human CD4 primary T-lymphocytes. piRNA (piR30840) significantly downregulated interleukin-4 (IL-4) via sequence complementarity binding to pre-mRNA intron, which subsequently inhibited the development of Th2 T-lymphocytes. Piwil4 and Ago4 are associated with this piRNA, and this complex further interacts with Trf4-Air2-Mtr4 Polyadenylation (TRAMP) complex, which leads to the decay of targeted pre-mRNA through nuclear exosomes. Taken together, we demonstrate a novel piRNA mechanism in regulating gene expression in highly differentiated somatic cells and a possible novel target for allergy therapeutics.
引用
收藏
页码:10474 / 10491
页数:18
相关论文
共 79 条
[1]   Maternally deposited germline piRNAs silence the tirant retrotransposon in somatic cells [J].
Akkouche, Abdou ;
Grentzinger, Thomas ;
Fablet, Marie ;
Armenise, Claudia ;
Burlet, Nelly ;
Braman, Virginie ;
Chambeyron, Severine ;
Vieira, Cristina .
EMBO REPORTS, 2013, 14 (05) :458-464
[2]   The small RNA profile during Drosophila melanogaster development [J].
Aravin, AA ;
Lagos-Quintana, M ;
Yalcin, A ;
Zavolan, M ;
Marks, D ;
Snyder, B ;
Gaasterland, T ;
Meyer, J ;
Tuschl, T .
DEVELOPMENTAL CELL, 2003, 5 (02) :337-350
[3]   A novel class of small RNAs bind to MILI protein in mouse testes [J].
Aravin, Alexei ;
Gaidatzis, Dimos ;
Pfeffer, Sebastien ;
Lagos-Quintana, Mariana ;
Landgraf, Pablo ;
Iovino, Nicola ;
Morris, Patricia ;
Brownstein, Michael J. ;
Kuramochi-Miyagawa, Satomi ;
Nakano, Toru ;
Chien, Minchen ;
Russo, James J. ;
Ju, Jingyue ;
Sheridan, Robert ;
Sander, Chris ;
Zavolan, Mihaela ;
Tuschl, Thomas .
NATURE, 2006, 442 (7099) :203-207
[4]   A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice [J].
Aravin, Alexei A. ;
Sachidanandam, Ravi ;
Bourc'his, Deborah ;
Schaefer, Christopher ;
Pezic, Dubravka ;
Toth, Katalin Fejes ;
Bestor, Timothy ;
Hannon, Gregory J. .
MOLECULAR CELL, 2008, 31 (06) :785-799
[5]   piRNAs Can Trigger a Multigenerational Epigenetic Memory in the Germline of C. elegans [J].
Ashe, Alyson ;
Sapetschnig, Alexandra ;
Weick, Eva-Maria ;
Mitchell, Jacinth ;
Bagijn, Marloes P. ;
Cording, Amy C. ;
Doebley, Anna-Lisa ;
Goldstein, Leonard D. ;
Lehrbach, Nicolas J. ;
Le Pen, Jeremie ;
Pintacuda, Greta ;
Sakaguchi, Aisa ;
Sarkies, Peter ;
Ahmed, Shawn ;
Miska, Eric A. .
CELL, 2012, 150 (01) :88-99
[6]   MicroRNA-mediated regulation of T helper cell differentiation and plasticity [J].
Baumjohann, Dirk ;
Ansel, K. Mark .
NATURE REVIEWS IMMUNOLOGY, 2013, 13 (09) :666-678
[7]   An Epigenetic Role for Maternally Inherited piRNAs in Transposon Silencing [J].
Brennecke, Julius ;
Malone, Colin D. ;
Aravin, Alexei A. ;
Sachidanandam, Ravi ;
Stark, Alexander ;
Hannon, Gregory J. .
SCIENCE, 2008, 322 (5906) :1387-1392
[8]  
Brennecke J, 2007, CELL, V128, P1089, DOI 10.1016/j.cell.2007.01.043
[9]   Drosophila PIWI associates with chromatin and interacts directly with HP1a [J].
Brower-Toland, Brent ;
Findley, Seth D. ;
Jiang, Ling ;
Liu, Li ;
Yin, Hang ;
Dus, Monica ;
Zhou, Pei ;
Elgin, Sarah C. R. ;
Lin, Haifan .
GENES & DEVELOPMENT, 2007, 21 (18) :2300-2311
[10]   The evolution of gene regulation by transcription factors and microRNAs [J].
Chen, Kevin ;
Rajewsky, Nikolaus .
NATURE REVIEWS GENETICS, 2007, 8 (02) :93-103