Both combinatorial K4me0-K36me3 marks on sister histone H3s of a nucleosome are required for Dnmt3a-Dnmt3L mediated de novo DNA methylation

Ting Gong; Xin Gu; Yu-Ting Liu; Zhen Zhou; Ling-Li Zhang; Yang Wen; Wei-Li Zhong; Guo-Liang Xu; Jin-Qiu Zhou

doi:10.1016/j.jgg.2019.12.006

Volume 47 Issue 2

Feb. 2020

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Article Navigation > Journal of Genetics and Genomics > 2020 > 47(2): 105-114

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Both combinatorial K4me0-K36me3 marks on sister histone H3s of a nucleosome are required for Dnmt3a-Dnmt3L mediated de novo DNA methylation

doi: 10.1016/j.jgg.2019.12.006

a
State Key Laboratory of Molecular Biology, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, University of Chinese Academy of Sciences, Shanghai, 200031, China
b
School of Life Science and Technology, ShanghaiTech University, Shanghai, 201210, China

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Corresponding author: E-mail address: jqzhou@sibcb.ac.cn (Jin-Qiu Zhou)
Publish Date: 2020-02-25

Abstract

Abstract

A nucleosome contains two copies of each histone H2A, H2B, H3 and H4. Histone H3 K4me0 and K36me3 are two key chromatin marks forde novo DNA methylation catalyzed by DNA methyltransferases in mammals. However, it remains unclear whether K4me0 and K36me3 marks on both sister histone H3s regulate de novo DNA methylation independently or cooperatively. Here, taking advantage of the bivalent histone H3 system in yeast, we examined the contributions of K4 and K36 on sister histone H3s to genomic DNA methylation catalyzed by ectopically co-expressed murine Dnmt3a and Dnmt3L. The results show that lack of both K4me0 and K36me3 on one sister H3 tail, or lack of K4me0 and K36me3 on respective sister H3s results in a dramatic reduction of 5mC, revealing a synergy of two sister H3s in DNA methylation regulation. Accordingly, the Dnmt3a or Dnmt3L mutation that disrupts the interaction of ^Dnmt3aADD domain-H3K4me0, ^Dnmt3LADD domain-H3K4me0, or ^Dnmt3aPWWP domain-H3K36me3 causes a significant reduction of DNA methylation. These results support the model that each heterodimeric Dnmt3a-Dnmt3L reads both K4me0 and K36me3 marks on one tail of sister H3s, and the dimer of heterodimeric Dnmt3a-Dnmt3L recognizes two tails of sister histone H3s to efficiently execute de novo DNA methylation.
- Asymmetrical nucleosome,
- Histone H3K4 methylation,
- Histone H3K36 methylation,
- Yeast

These authors contribute equally to this work.

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References(40)

References

[1]	Baubec, T., Colombo, D.F., Wirbelauer, C., Schmidt, J., Burger, L., Krebs, A.R., Akalin, A., Schubeler, D., 2015. Genomic profiling of DNA methyltransferases reveals a role for DNMT3B in genic methylation. Nature 520, 243-247.
[2]	Bauer, I., Graessle, S., Loidl, P., Hohenstein, K., Brosch, G., 2010. Novel insights into the functional role of three protein arginine methyltransferases in Aspergillus nidulans. Fungal Genet. Biol. 47, 551-561.
[3]	Bestor, T.H., 2000. The DNA methyltransferases of mammals. Hum. Mol. Genet. 9, 2395-2402.
[4]	Capuano, F., Mulleder, M., Kok, R., Blom, H.J., Ralser, M., 2014. Cytosine DNA methylation is found in Drosophila melanogaster but absent in Saccharomyces cerevisiae, Schizosaccharomyces pombe, and other yeast species. Anal. Chem. 86, 3697-3702.
[5]	Chedin, F., Lieber, M.R., Hsieh, C.L., 2002. The DNA methyltransferase-like protein DNMT3L stimulates de novo methylation by Dnmt3a. Proc. Natl. Acad. Sci. U. S. A. 99, 16916-16921.
[6]	Chen, T., Tsujimoto, N., Li, E., 2004. The PWWP domain of Dnmt3a and Dnmt3b is required for directing DNA methylation to the major satellite repeats at pericentric heterochromatin. Mol. Cell. Biol. 24, 9048-9058.
[7]	Dhayalan, A., Rajavelu, A., Rathert, P., Tamas, R., Jurkowska, R.Z., Ragozin, S., Jeltsch, A., 2010. The Dnmt3a PWWP domain reads histone 3 lysine 36 trimethylation and guides DNA methylation. J. Biol. Chem. 285, 26114-26120.
[8]	Edwards, J.R., Yarychkivska, O., Boulard, M., Bestor, T.H., 2017. DNA methylation and DNA methyltransferases. Epigenet. Chromatin 10, 23.
[9]	Ge, Y.Z., Pu, M.T., Gowher, H., Wu, H.P., Ding, J.P., Jeltsch, A., Xu, G.L., 2004. Chromatin targeting of de novo DNA methyltransferases by the PWWP domain. J. Biol. Chem. 279, 25447-25454.
[10]	Gietz, R.D., Schiestl, R.H., 2007. High-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method. Nat. Protoc. 2, 31-34.
[11]	Gowher, H., Stockdale, C.J., Goyal, R., Ferreira, H., Owen-Hughes, T., Jeltsch, A., 2005. De novo methylation of nucleosomal DNA by the mammalian Dnmt1 and Dnmt3A DNA methyltransferases. Biochemistry 44, 9899-9904.
[12]	Guo, X., Wang, L., Li, J., Ding, Z., Xiao, J., Yin, X., He, S., Shi, P., Dong, L., Li, G., Tian, C., Wang, J., Cong, Y., Xu, Y., 2015. Structural insight into autoinhibition and histone H3-induced activation of DNMT3A. Nature 517, 640-644.
[13]	Holz-Schietinger, C., Matje, D.M., Harrison, M.F., Reich, N.O., 2011. Oligomerization of DNMT3A controls the mechanism of de novo DNA methylation. J. Biol. Chem. 286, 41479-41488.
[14]	Hu, J.L., Zhou, B.O., Zhang, R.R., Zhang, K.L., Zhou, J.Q., Xu, G.L., 2009. The N-terminus of histone H3 is required for de novo DNA methylation in chromatin. Proc. Natl. Acad. Sci. U. S. A. 106, 22187-22192.
[15]	Huang, H., Lin, S., Garcia, B.A., Zhao, Y., 2015. Quantitative proteomic analysis of histone modifications. Chem. Rev. 115, 2376-2418.
[16]	Infante, J.J., Law, G.L., Young, E.T., 2012. Analysis of nucleosome positioning using a nucleosome-scanning assay. Methods Mol. Biol. 833, 63-87.
[17]	Jaenisch, R., Bird, A., 2003. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat. Genet. 33 Suppl, 245-254.
[18]	Jia, D., Jurkowska, R.Z., Zhang, X., Jeltsch, A., Cheng, X., 2007. Structure of Dnmt3a bound to Dnmt3L suggests a model for de novo DNA methylation. Nature 449, 248-251.
[19]	Jurkowska, R.Z., Jurkowski, T.P., Jeltsch, A., 2011. Structure and function of mammalian DNA methyltransferases. Chembiochem 12, 206-222.
[20]	Kirmizis, A., Santos-Rosa, H., Penkett, C.J., Singer, M.A., Vermeulen, M., Mann, M., Bahler, J., Green, R.D., Kouzarides, T., 2007. Arginine methylation at histone H3R2 controls deposition of H3K4 trimethylation. Nature 449, 928-932.
[21]	Law, J.A., Jacobsen, S.E., 2010. Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat. Rev. Genet .11, 204-220.
[22]	Luger, K., Mader, A.W., Richmond, R.K., Sargent, D.F., Richmond, T.J., 1997. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389, 251-260.
[23]	Lund, G., Andersson, L., Lauria, M., Lindholm, M., Fraga, M.F., Villar-Garea, A., Ballestar, E., Esteller, M., Zaina, S., 2004. DNA methylation polymorphisms precede any histological sign of atherosclerosis in mice lacking apolipoprotein E. J. Biol. Chem. 279, 29147-29154.
[24]	Morselli, M., Pastor, W.A., Montanini, B., Nee, K., Ferrari, R., Fu, K., Bonora, G., Rubbi, L., Clark, A.T., Ottonello, S., Jacobsen, S.E., Pellegrini, M., 2015. In vivo targeting of de novo DNA methylation by histone modifications in yeast and mouse. eLife 4, e06205.
[25]	Okano, M., Bell, D.W., Haber, D.A., Li, E., 1999. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99, 247-257.
[26]	Ooi, S.K., Qiu, C., Bernstein, E., Li, K., Jia, D., Yang, Z., Erdjument-Bromage, H., Tempst, P., Lin, S.P., Allis, C.D., Cheng, X., Bestor, T.H., 2007. DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA. Nature 448, 714-717.
[27]	Otani, J., Nankumo, T., Arita, K., Inamoto, S., Ariyoshi, M., Shirakawa, M., 2009. Structural basis for recognition of H3K4 methylation status by the DNA methyltransferase 3A ATRX-DNMT3-DNMT3L domain. EMBO Rep. 10, 1235-1241.
[28]	Peng, J., Zhou, J.Q., 2012. The tail-module of yeast Mediator complex is required for telomere heterochromatin maintenance. Nucleic Acids Res. 40, 581-593.
[29]	Rando, O.J., 2010. Genome-wide mapping of nucleosomes in yeast. Methods Enzymol. 470, 105-118.
[30]	Robertson, A.K., Geiman, T.M., Sankpal, U.T., Hager, G.L., Robertson, K.D., 2004. Effects of chromatin structure on the enzymatic and DNA binding functions of DNA methyltransferases DNMT1 and Dnmt3a in vitro. Biochem. Biophys. Res. Commun. 322, 110-118.
[31]	Rondelet, G., Dal Maso, T., Willems, L., Wouters, J., 2016. Structural basis for recognition of histone H3K36me3 nucleosome by human de novo DNA methyltransferases 3A and 3B. J. Struct. Biol. 194, 357-367.
[32]	Shirohzu, H., Kubota, T., Kumazawa, A., Sado, T., Chijiwa, T., Inagaki, K., Suetake, I., Tajima, S., Wakui, K., Miki, Y., Hayashi, M., Fukushima, Y., Sasaki, H., 2002. Three novel DNMT3B mutations in Japanese patients with ICF syndrome. Am. J. Med. Genet. 112, 31-37.
[33]	Smith, Z.D., Meissner, A., 2013. DNA methylation: roles in mammalian development. Nat. Rev. Genet. 14, 204-220.
[34]	Suetake, I., Shinozaki, F., Miyagawa, J., Takeshima, H., Tajima, S., 2004. DNMT3L stimulates the DNA methylation activity of Dnmt3a and Dnmt3b through a direct interaction. J. Biol. Chem. 279, 27816-27823.
[35]	Suganuma, T., Workman, J.L., 2008. Crosstalk among histone modifications. Cell 135, 604-607.
[36]	Takeshima, H., Suetake, I., Shimahara, H., Ura, K., Tate, S., Tajima, S., 2006. Distinct DNA methylation activity of Dnmt3a and Dnmt3b towards naked and nucleosomal DNA. J. Biochem. 139, 503-515.
[37]	Takeshima, H., Suetake, I., Tajima, S., 2008. Mouse Dnmt3a preferentially methylates linker DNA and is inhibited by histone H1. J. Mol. Biol. 383, 810-821.
[38]	Zhang, Y., Jurkowska, R., Soeroes, S., Rajavelu, A., Dhayalan, A., Bock, I., Rathert, P., Brandt, O., Reinhardt, R., Fischle, W., Jeltsch, A., 2010. Chromatin methylation activity of Dnmt3a and Dnmt3a/3L is guided by interaction of the ADD domain with the histone H3 tail. Nucleic Acids Res. 38, 4246-4253.
[39]	Zhang, Z.M., Lu, R., Wang, P., Yu, Y., Chen, D., Gao, L., Liu, S., Ji, D., Rothbart, S.B., Wang, Y., Wang, G.G., Song, J., 2018. Structural basis for DNMT3A-mediated de novo DNA methylation. Nature 554, 387-391.
[40]	Zhou, Z., Liu, Y.T., Ma, L., Gong, T., Hu, Y.N., Li, H.T., Cai, C., Zhang, L.L., Wei, G., Zhou, J.Q., 2017. Independent manipulation of histone H3 modifications in individual nucleosomes reveals the contributions of sister histones to transcription. eLife 6, e30178.