Regulators of alternative polyadenylation operate at the transition from mitosis to meiosis

Lingjuan Shan; Chan Wu; Di Chen; Lei Hou; Xin Li; Lixia Wang; Xiao Chu; Yifeng Hou; Zhaohui Wang

doi:10.1016/j.jgg.2016.12.007

Volume 44 Issue 2

Feb. 2017

Turn off MathJax

Article Contents

Article Navigation > Journal of Genetics and Genomics > 2017 > 44(2): 95-106

PDF( 5077 KB)

Regulators of alternative polyadenylation operate at the transition from mitosis to meiosis

doi: 10.1016/j.jgg.2016.12.007

Lingjuan Shan^{a, b, #},
Chan Wu^{a, b, #},
Di Chen^b,
Lei Hou^c,
Xin Li^a,
Lixia Wang^a,
Xiao Chu^{b, e},
Yifeng Hou^d,
Zhaohui Wang^a

a
State Key Laboratory of Molecular Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China
b
The University of Chinese Academy of Sciences, Beijing 100049, China
c
Key Laboratory of Computational Biology, Chinese Academy of Sciences-Max Planck Partner Institute for Computational Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200031, China
d
State Key Laboratory of Plant Genomics and National Center for Plant Gene Research, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China
e
Key Laboratory of Genetic Network Biology, Collaborative Innovation Center of Genetics and Development, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China

More Information

Corresponding author: E-mail address: zhwang@genetics.ac.cn (Zhaohui Wang)
Received Date: 2016-11-08
Accepted Date: 2016-12-28
Rev Recd Date: 2016-12-14

Available Online: 2017-01-27

Publish Date: 2017-02-20

Abstract

Abstract

In the sexually reproductive organisms, gametes are produced by meiosis following a limited mitotic amplification. However, the intrinsic program switching cells from mitotic to meiotic cycle is unclear. Alternative polyadenylation (APA) is a highly conserved means of gene regulation and is achieved by the RNA 3′-processing machinery to generate diverse 3′UTR profiles. In Drosophila spermatogenesis, we observed distinct profiles of transcriptome-wide 3′UTR between mitotic and meiotic cells. In mutant germ cells stuck in mitosis, 3′UTRs of hundreds of genes were consistently shifted. Remarkably, altering the levels of multiple 3′-processing factors disrupted germline's progression to meiosis, indicative of APA's active role in this transition. An RNA-binding protein (RBP) Tut could directly bind 3′UTRs of 3′-processing factors whose expressions were repressed in the presence of Tut-containing complex. Further, we demonstrated that this RBP complex could execute the repression post-transcriptionally by recruiting CCR4/Twin of deadenylation complex. Thus, we propose that an RBP complex regulates the dynamic APA profile to promote the mitosis-to-meiosis transition.
- Germ cell,
- Mitosis to meiosis,
- Alternative polyadenylation,
- RNA-binding protein,
- 3′UTR

These authors contributed equally to this study.

FullText(HTML)

References(61)

References

[1]	An, J.J., Gharami, K., Liao, G.-Y. et al. Distinct role of long 3′UTR BDNF mRNA in spine morphology and synaptic plasticity in hippocampal neurons Cell, 134 (2008),pp. 175-187
[2]	Anderson, E.L., Baltus, A.E., Roepers-Gajadien, H.L. et al. Stra8 and its inducer, retinoic acid, regulate meiotic initiation in both spermatogenesis and oogenesis in mice Proc. Natl. Acad. Sci. U. S. A., 105 (2008),pp. 14976-14980
[3]	Andreassi, C., Riccio, A. To localize or not to localize: mRNA fate is in 3′UTR ends Trends Cell Biol., 19 (2009),pp. 465-474
[4]	Baltus, A.E., Menke, D.B., Hu, Y.C. et al. In germ cells of mouse embryonic ovaries, the decision to enter meiosis precedes premeiotic DNA replication Nat. Genet., 38 (2006),pp. 1430-1434
[5]	Baltz, A.G., Munschauer, M., Schwanhausser, B. et al. The mRNA-bound proteome and its global occupancy profile on protein-coding transcripts Mol. Cell, 46 (2012),pp. 674-690
[6]	Batra, R., Charizanis, K., Manchanda, M. et al. Loss of MBNL leads to disruption of developmentally regulated alternative polyadenylation in RNA-mediated disease Mol. Cell, 56 (2014),pp. 311-322
[7]	Berkovits, B.D., Mayr, C. Alternative 3′UTRs act as scaffolds to regulate membrane protein localization Nature, 522 (2015),pp. 363-367
[8]	Bernstein, D.S., Buter, N., Stumpf, C. et al. Analyzing mRNA-protein complexes using a yeast three-hybrid system Methods, 26 (2002),pp. 123-141
[9]	Bischof, J., Maeda, R.K., Hediger, M. et al. Proc. Natl. Acad. Sci. U. S. A., 104 (2007),pp. 3312-3317
[10]	Bowles, J., Knight, D., Smith, C. et al. Retinoid signaling determines germ cell fate in mice Science, 312 (2006),pp. 596-600
[11]	Chen, D., DM, M. Development, 130 (2003),pp. 1159-1170
[12]	Chen, D., McKearin, D. Gene circuitry controlling a stem cell niche Curr. Biol., 15 (2005),pp. 179-184
[13]	Chen, D., Wu, C., Zhao, S. et al. PLoS Genet., 10 (2014),p. e1004797
[14]	de Klerk, E., Venema, A., Anvar, S.Y. et al. Poly(A) binding protein nuclear 1 levels affect alternative polyadenylation Nucleic Acids Res., 40 (2012),pp. 9089-9101
[15]	Derti, A., Garrett-Engele, P., Macisaac, K.D. et al. A quantitative atlas of polyadenylation in five mammals Genome Res., 22 (2012),pp. 1173-1183
[16]	Di Giammartino, D.C., Nishida, K., Manley, J.L. Mechanisms and consequences of alternative polyadenylation Mol. Cell, 43 (2011),pp. 853-866
[17]	Eberhart, C.G., Maines, J.Z., Wasserman, S.A. Nature, 381 (1996),pp. 783-785
[18]	Fu, Z., Geng, C., Wang, H. et al. Twin promotes the maintenance and differentiation of germline stem cell lineage through modulation of multiple pathways Cell Rep., 13 (2015),pp. 1366-1379
[19]	Honigberg, S.M., Purnapatre, K. Signal pathway integration in the switch from the mitotic cell cycle to meiosis in yeast J. Cell Sci., 116 (2003),pp. 2137-2147
[20]	Hoque, M., Ji, Z., Zheng, D. et al. Analysis of alternative cleavage and polyadenylation by 3′ region extraction and deep sequencing Nat. Methods, 10 (2013),pp. 133-139
[21]	Insco, M.L., Bailey, A.S., Kim, J. et al. A self-limiting switch based on translational control regulates the transition from proliferation to differentiation in an adult stem cell lineage Cell Stem Cell, 11 (2012),pp. 689-700
[22]	Insco, M.L., Leon, A., Tam, C.H. et al. Accumulation of a differentiation regulator specifies transit amplifying division number in an adult stem cell lineage Proc. Natl. Acad. Sci. U. S. A., 106 (2009),pp. 22311-22316
[23]	Jenal, M., Elkon, R., Loayza-Puch, F. et al. The poly(A)-binding protein nuclear 1 suppresses alternative cleavage and polyadenylation sites Cell, 149 (2012),pp. 538-553
[24]	Ji, Z., Lee, J.Y., Pan, Z. et al. Progressive lengthening of 3′ untranslated regions of mRNAs by alternative polyadenylation during mouse embryonic development Proc. Natl. Acad. Sci. U. S. A., 106 (2009),pp. 7028-7033
[25]	Ji, Z., Tian, B. Reprogramming of 3′ untranslated regions of mRNAs by alternative polyadenylation in generation of pluripotent stem cells from different cell types PLoS One, 4 (2009),p. e8419
[26]	Jin, Z., Kirilly, D., Weng, C. et al. Cell Stem Cell, 2 (2008),pp. 39-49
[27]	Kim, D., Pertea, G., Trapnell, C. et al. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions Genome Biol., 14 (2013),p. R36
[28]	Kim, S., Yamamoto, J., Chen, Y. et al. Evidence that cleavage factor Im is a heterotetrameric protein complex controlling alternative polyadenylation Genes Cells, 15 (2010),pp. 1003-1013
[29]	Koubova, J., Menke, D.B., Zhou, Q. et al. Retinoic acid regulates sex-specific timing of meiotic initiation in mice Proc. Natl. Acad. Sci. U. S. A., 103 (2006),pp. 2474-2479
[30]	Kubo, T., Wada, T., Yamaguchi, Y. et al. Knock-down of 25 kDa subunit of cleavage factor Im in Hela cells alters alternative polyadenylation within 3′-UTRs Nucleic Acids Res., 34 (2006),pp. 6264-6271
[31]	Lackford, B., Yao, C., Charles, G.M. et al. Fip1 regulates mRNA alternative polyadenylation to promote stem cell self-renewal EMBO J., 33 (2014),pp. 878-889
[32]	Li, C.Y., Guo, Z., Wang, Z. Dev. Biol., 309 (2007),pp. 70-77
[33]	Li, W., Park, J.Y., Zheng, D. et al. Alternative cleavage and polyadenylation in spermatogenesis connects chromatin regulation with post-transcriptional control BMC Biol., 14 (2016),p. 6
[34]	Lin, Y., Gill, M.E., Koubova, J. et al. Germ cell-intrinsic and -extrinsic factors govern meiotic initiation in mouse embryos Science, 322 (2008),pp. 1685-1687
[35]	Mangone, M., Manoharan, A.P., Thierry-Mieg, D. et al. Science, 329 (2010),pp. 432-435
[36]	Martin, G., Gruber, A.R., Keller, W. et al. Genome-wide analysis of pre-mRNA 3′ end processing reveals a decisive role of human cleavage factor I in the regulation of 3′UTR length Cell Rep., 1 (2012),pp. 753-763
[37]	Masamha, C.P., Xia, Z., Yang, J. et al. CFIm25 links alternative polyadenylation to glioblastoma tumour suppression Nature, 510 (2014),pp. 412-416
[38]	Mayr, C. Evolution and biological roles of alternative 3′UTRs Trends Cell Biol., 26 (2016),pp. 227-237
[39]	Mayr, C., Bartel, D.P. Widespread shortening of 3′UTRs by alternative cleavage and polyadenylation activates oncogenes in cancer cells Cell, 138 (2009),pp. 673-684
[40]	McKearin, D., Ohlstein, B. Development, 121 (1995),pp. 2937-2947
[41]	Norbury, C.J. Cytoplasmic RNA: a case of the tail wagging the dog Nat. Rev. Mol. Cell Biol., 14 (2013),pp. 643-653
[42]	Ohlstein, B., Lavoie, C.A., Vef, O. et al. Genetics, 155 (2000),pp. 1809-1819
[43]	Ozsolak, F., Kapranov, P., Foissac, S. et al. Comprehensive polyadenylation site maps in yeast and human reveal pervasive alternative polyadenylation Cell, 143 (2010),pp. 1018-1029
[44]	Parker, R., Song, H. The enzymes and control of eukaryotic mRNA turnover Nat. Struct. Mol. Biol., 11 (2004),pp. 121-127
[45]	Pinto, P.A.B., Henriques, T., Freitas, M.O. et al. EMBO J., 30 (2011),pp. 2431-2444
[46]	Sandberg, R., Neilson, J.R., Sarma, A. et al. Proliferating cells express mRNAs with shortened 3′ untranslated regions and fewer microRNA target sites Science, 320 (2008),pp. 1643-1647
[47]	Shepard, P.J., Choi, E.A., Lu, J. et al. Complex and dynamic landscape of RNA polyadenylation revealed by PAS-Seq RNA, 17 (2011),pp. 761-772
[48]	Shi, Y. Alternative polyadenylation: new insights from global analyses RNA, 18 (2012),pp. 2105-2117
[49]	Smibert, P., Miura, P., Westholm, J.O. et al. Cell Rep., 1 (2012),pp. 277-289
[50]	Sun, Y.C., Cheng, S.F., Sun, R. et al. J. Genet. Genomics, 41 (2014),pp. 87-95
[51]	Suzuki, A., Hirasaki, M., Hishida, T. et al. Loss of MAX results in meiotic entry in mouse embryonic and germline stem cells Nat. Commun., 7 (2016),p. 11056
[52]	Takagaki, Y., Manley, J.L. Levels of polyadenylation factor CstF-64 control IgM heavy chain mRNA accumulation and other events associated with B cell differentiation Mol. Cell, 2 (1998),pp. 761-771
[53]	Takagaki, Y., Seipelt, R.L., Peterson, M.L. et al. The polyadenylation factor CstF-64 regulates alternative processing of IgM heavy chain pre-mRNA during B cell differentiation Cell, 87 (1996),pp. 941-952
[54]	Trapnell, C., Hendrickson, D.G., Sauvageau, M. et al. Differential analysis of gene regulation at transcript resolution with RNA-seq Nat. Biotechnol., 31 (2013),pp. 46-53
[55]	Ulitsky, I., Shkumatava, A., Jan, C.H. et al. Extensive alternative polyadenylation during zebrafish development Genome Res., 22 (2012),pp. 2054-2066
[56]	Wahle, E., Winkler, G.S. RNA decay machines: deadenylation by the Ccr4-not and Pan2-Pan3 complexes Biochim. Biophys. Acta, 1829 (2013),pp. 561-570
[57]	Wolf, J., Passmore, L.A. mRNA deadenylation by Pan2-Pan3 Biochem. Soc. Trans., 42 (2014),pp. 184-187
[58]	Wu, X., Liu, M., Downie, B. et al. Proc. Natl. Acad. Sci. U. S. A., 108 (2011),pp. 12533-12538
[59]	Xu, E.Y., Lee, D.F., Klebes, A. et al. Hum. Mol. Genet., 12 (2003),pp. 169-175
[60]	Zhao, S., Chen, D., Geng, Q. et al. Dev. Biol., 376 (2013),pp. 163-170
[61]	Zheng, D., Tian, B. RNA-binding proteins in regulation of alternative cleavage and polyadenylation Adv. Exp. Med. Biol., 825 (2014),pp. 97-127