N6 -methyladenosine sequencing highlights the involvement of mRNA methylation in oocyte meiotic maturation and embryo development by regulating translation in xenopus laevis

Journal of Biological Chemistry

Volumn 291, Issue 44, 2016, Pages 23020-23026

  Qi, Shu Tao ^a   Ma, Jun Yu ^b   Wang, Zhen Bo ^a   Guo, Lei ^a   Hou, Yi ^a   Sun, Qing Yuan ^a,b  

^a INSTITUTE OF ZOOLOGY   (China)

^b QINGDAO AGRICULTURAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ALKYLATION; CELL PROLIFERATION; METHYLATION; PROTEINS; RNA;

ACCURATELY REGULATED; CELL DIVISIONS; EMBRYO DEVELOPMENT; GERMINAL VESICLES; PROTEIN PHOSPHORYLATION; RNA TRANSLATION; TRANSCRIPTION ACTIVITY; TRANSCRIPTOMES;

NUCLEIC ACIDS;

6 N METHYLADENOSINE; MESSENGER RNA; ADENOSINE; N(6)-METHYLADENOSINE; XENOPUS PROTEIN;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; EMBRYO DEVELOPMENT; FEMALE; GENE EXPRESSION; GERMINAL VESICLE; METAPHASE; NONHUMAN; OOCYTE MATURATION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RNA METHYLATION; RNA SEQUENCE; TRANSLATION REGULATION; XENOPUS LAEVIS; ANALOGS AND DERIVATIVES; ANIMAL; EMBRYOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MALE; MEIOSIS; METABOLISM; OOCYTE; PROTEIN SYNTHESIS;

ADENOSINE; ANIMALS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MALE; MEIOSIS; OOCYTES; PROTEIN BIOSYNTHESIS; RNA, MESSENGER; XENOPUS LAEVIS; XENOPUS PROTEINS;

EID: 84994031793     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M116.748889     Document Type: Article

References (42)

1. Bellier, S., Dubois, M. F., Nishida, E., Almouzni, G., and Bensaude, O. (1997) Phosphorylation of the RNA polymerase II largest subunit during Xenopus laevis oocyte maturation. Mol. Cell. Biol. 17, 1434-1440
2. Miyara, F., Migne, C., Dumont-Hassan, M., Le Meur, A., Cohen-Bacrie, P., Aubriot, F. X., Glissant, A., Nathan, C., Douard, S., Stanovici, A., and Debey, P. (2003) Chromatin configuration and transcriptional control in human and mouse oocytes. Mol. Reprod. Dev. 64, 458-470
3. Lee, M. T., Bonneau, A. R., and Giraldez, A. J. (2014) Zygotic genome activation during the maternal-to-zygotic transition. Annu. Rev. Cell Dev. Biol. 30, 581-613
4. Prather, R. S. (2010) Whatever happened to the "cell-block" during mammalian embryogenesis? Mol. Reprod. Dev. 77, NA
5. Graf, A., Krebs, S., Heininen-Brown, M., Zakhartchenko, V., Blum, H., and Wolf, E. (2014) Genome activation in bovine embryos: review of the literature and new insights from RNA sequencing experiments. Animal Reprod. Sci. 149, 46-58
6. Yu, C., Ji, S. Y., Dang, Y. J., Sha, Q. Q., Yuan, Y. F., Zhou, J. J., Yan, L. Y., Qiao, J., Tang, F., and Fan, H. Y. (2016) Oocyte-expressed yes-associated protein is a key activator of the early zygotic genome in mouse. Cell Res. 26, 275-287
7. Yu, C., Ji, S. Y., Sha, Q. Q., Dang, Y., Zhou, J. J., Zhang, Y. L., Liu, Y., Wang, Z. W., Hu, B., Sun, Q. Y., Sun, S. C., Tang, F., and Fan, H. Y. (2016) BTG4 is a meiotic cell cycle-coupled maternal-zygotic-transition licensing factor in oocytes. Nat. Struct. Mol. Biol. 23, 387-394
8. Radford, H. E., Meijer, H. A., and de Moor, C. H. (2008) Translational control by cytoplasmic polyadenylation in Xenopus oocytes. Biochim. Biophys. Acta 1779, 217-229
9. Stebbins-Boaz, B., Hake, L. E., and Richter, J. D. (1996) CPEB controls the cytoplasmic polyadenylation of cyclin, Cdk2 and c-mos mRNAs and is necessary for oocyte maturation in Xenopus. EMBO J. 15, 2582-2592
10. Hake, L. E., and Richter, J. D. (1994) CPEB is a specificity factor that mediates cytoplasmic polyadenylation during Xenopus oocyte maturation. Cell 79, 617-627
11. Mendez, R., Murthy, K. G., Ryan, K., Manley, J. L., and Richter, J. D. (2000) Phosphorylation of CPEB by Eg2 mediates the recruitment of CPSF into an active cytoplasmic polyadenylation complex. Mol. Cell 6, 1253-1259
12. Zhou, J., Wan, J., Gao, X., Zhang, X., Jaffrey, S. R., and Qian, S. B. (2015) Dynamic m6 A mRNA methylation directs translational control of heat shock response. Nature 526, 591-594
13. Fu, Y., Dominissini, D., Rechavi, G., and He, C. (2014) Gene expression regulation mediated through reversible m6 A RNA methylation. Nat. Rev. Genet. 15, 293-306
14. Lee, M., Kim, B., and Kim, V. N. (2014) Emerging roles of RNA modification: m6 A and U-tail. Cell 158, 980-987
15. Ke, S., Alemu, E. A., Mertens, C., Gantman, E. C., Fak, J. J., Mele, A., Haripal, B., Zucker-Scharff, I., Moore, M. J., Park, C. Y., Vagbo, C. B., Kussnierczyk, A., Klungland, A., Darnell, J. E., Jr., and Darnell, R. B. (2015) A majority of m6 A residues are in the last exons, allowing the potential for 3' UTR regulation. Genes Dev. 29, 2037-2053
16. Meyer, K. D., Patil, D. P., Zhou, J., Zinoviev, A., Skabkin, M. A., Elemento, O., Pestova, T. V., Qian, S. B., and Jaffrey, S. R. (2015) 5ô UTR m6 A promotes cap-independent translation. Cell 163, 999-1010
17. Geula, S., Moshitch-Moshkovitz, S., Dominissini, D., Mansour, A. A., Kol, N., Salmon-Divon, M., Hershkovitz, V., Peer, E., Mor, N., Manor, Y. S., Ben-Haim, M. S., Eyal, E., Yunger, S., Pinto, Y., Jaitin, D. A., Viukov, S., et al. (2015) Stem cells. m6A mRNA methylation facilitates resolution of naive pluripotency toward differentiation. Science 347, 1002-1006
18. Dominissini, D., Moshitch-Moshkovitz, S., Salmon-Divon, M., Amariglio, N., and Rechavi, G. (2013) Transcriptome-wide mapping of N6 -methyladenosine by m6 A-seq based on immunocapturing and massively parallel sequencing. Nat. Protoc. 8, 176-189
19. Karpinka, J. B., Fortriede, J. D., Burns, K. A., James-Zorn, C., Ponferrada, V. G., Lee, J., Karimi, K., Zorn, A. M., and Vize, P. D. (2015) Xenbase, the Xenopus model organism database: new virtualized system, data types and genomes. Nucleic Acids Res. 43, D756-763
20. Charlier, C., Montfort, J., Chabrol, O., Brisard, D., Nguyen, T., Le Cam, A., Richard-Parpaillon, L., Moreews, F., Pontarotti, P., Uzbekova, S., Chesnel, F., and Bobe, J. (2012) Oocyte-somatic cells interactions, lessons from evolution. BMC Genomics 13, 560
21. Huang da, W, Sherman, B. T., and Lempicki, R. A. (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44-57
22. Smits, A. H., Lindeboom, R. G., Perino, M., van Heeringen, S. J., Veenstra, G. J., and Vermeulen, M. (2014) Global absolute quantification reveals tight regulation of protein expression in single Xenopus eggs. Nucleic Acids Res. 42, 9880-9891
23. Peshkin, L., Wühr, M., Pearl, E., Haas, W., Freeman, R. M., Jr., Gerhart, J. C., Klein, A. M., Horb, M., Gygi, S. P., and Kirschner, M. W. (2015) On the relationship of protein and mRNA dynamics in vertebrate embryonic development. Dev. Cell 35, 383-394
24. Heasman, J. (2006) Patterning the early Xenopus embryo. Development 133, 1205-1217
25. Lin, S., Choe, J., Du, P., Triboulet, R., and Gregory, R. I. (2016) The m(6)A methyltransferase METTL3 promotes translation in human cancer cells. Mol. Cell 62, 335-345
26. Liu, J., Yue, Y., Han, D., Wang, X., Fu, Y., Zhang, L., Jia, G., Yu, M., Lu, Z., Deng, X., Dai, Q., Chen, W., and He, C. (2014) A METTL3-METTL14 complex mediates mammalian nuclear RNA N6 -adenosine methylation. Nat. Chem. Biol. 10, 93-95
27. Ping, X. L., Sun, B. F., Wang, L., Xiao, W., Yang, X., Wang, W. J., Adhikari, S., Shi, Y., Lv, Y., Chen, Y. S., Zhao, X., Li, A., Yang, Y., Dahal, U., Lou, X. M., et al. (2014) Mammalian WTAP is a regulatory subunit of the RNA N6 -methyladenosine methyltransferase. Cell Res. 24, 177-189
28. Schwartz, S., Mumbach, M. R., Jovanovic, M., Wang, T., Maciag, K., Bushkin, G. G., Mertins, P., Ter-Ovanesyan, D., Habib, N., Cacchiarelli, D., Sanjana, N. E., Freinkman, E., Pacold, M. E., Satija, R., Mikkelsen, T. S., et al. (2014) Perturbation of m6 A writers reveals two distinct classes of mRNA methylation at internal and 5' sites. Cell Rep. 8, 284-296
29. Jia, G., Fu, Y., Zhao, X., Dai, Q., Zheng, G., Yang, Y., Yi, C., Lindahl, T., Pan, T., Yang, Y. G., and He, C. (2011) N6 -methyladenosine in nuclear RNA is a major substrate of the obesity-associated FTO. Nat. Chem. Biol. 7, 885-887
30. Zheng, G., Dahl, J. A., Niu, Y., Fedorcsak, P., Huang, C. M., Li, C. J., Vågbø, C. B., Shi, Y., Wang, W. L., Song, S. H., Lu, Z., Bosmans, R. P., Dai, Q., Hao, Y. J., Yang, X., et al. (2013) ALKBH5 is a mammalian RNA demethylase that impacts RNA metabolism and mouse fertility. Mol. Cell 49, 18-29
31. Cao, G., Li, H. B., Yin, Z., and Flavell, R. A. (2016) Recent advances in dynamic m6 A RNA modification. Open Biol. 6, 160003
32. Pan, H., O'Brien, M. J., Wigglesworth, K., Eppig, J. J., and Schultz, R. M. (2005) Transcript profiling during mouse oocyte development and the effect of gonadotropin priming and development in vitro. Dev. Biol. 286, 493-506
33. Yoshitome, S., Furuno, N., Prigent, C., and Hashimoto, E. (2012) The subcellular localization of cyclin B2 is required for bipolar spindle formation during Xenopus oocyte maturation. Biochem. Biophys. Res. Commun. 422, 770-775
34. Peter, M., Labbé, J. C., Doree, M., and Mandart, E. (2002) A new role for Mos in Xenopus oocyte maturation: targeting Myt1 independently of MAPK. Development 129, 2129-2139
35. Colledge, W. H., Carlton, M. B., Udy, G. B., and Evans, M. J. (1994) Disruption of c-mos causes parthenogenetic development of unfertilized mouse eggs. Nature 370, 65-68
36. Araki, K., Naito, K., Haraguchi, S., Suzuki, R., Yokoyama, M., Inoue, M., Aizawa, S., Toyoda, Y., and Sato, E. (1996) Meiotic abnormalities of c-mos knockout mouse oocytes: activation after first meiosis or entrance into third meiotic metaphase. Biol. Reprod. 55, 1315-1324
37. Narasimhachar, Y., and Coué, M. (2009) Geminin stabilizes Cdt1 during meiosis in Xenopus oocytes. J. Biol. Chem. 284, 27235-27242
38. Arentson, E., Faloon, P., Seo, J., Moon, E., Studts, J. M., Fremont, D. H., and Choi, K. (2002) Oncogenic potential of the DNA replication licensing protein CDT1. Oncogene 21, 1150-1158
39. Arias, E. E., and Walter, J. C. (2005) Replication-dependent destruction of Cdt1 limits DNA replication to a single round per cell cycle in Xenopus egg extracts. Genes Dev. 19, 114-126
40. Langmead, B., Trapnell, C., Pop, M., and Salzberg, S. L. (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25
41. Feng, J., Liu, T., and Zhang, Y. (2011) Using MACS to identify peaks from ChIP-seq data. Curr. Protoc. Bioinformatics Chapter 2, Unit 2 14
42. Machanick, P., and Bailey, T. L. (2011) MEME-ChIP: motif analysis of large DNA datasets. Bioinformatics 27, 1696-1697