リケラボ論文検索は、全国の大学リポジトリにある学位論文・教授論文を一括検索できる論文検索サービスです。

リケラボ 全国の大学リポジトリにある学位論文・教授論文を一括検索するならリケラボ論文検索大学・研究所にある論文を検索できる

リケラボ 全国の大学リポジトリにある学位論文・教授論文を一括検索するならリケラボ論文検索大学・研究所にある論文を検索できる

大学・研究所にある論文を検索できる 「PHF7 Modulates BRDT Stability and Histone-to-Protamine Exchange during Spermiogenesis」の論文概要。リケラボ論文検索は、全国の大学リポジトリにある学位論文・教授論文を一括検索できる論文検索サービスです。

コピーが完了しました

URLをコピーしました

論文の公開元へ論文の公開元へ
書き出し

PHF7 Modulates BRDT Stability and Histone-to-Protamine Exchange during Spermiogenesis

Kim, Chang Rok 大阪大学

2020.07.28

概要

Spermatogenesis is a complex process of sperm generation, including mitosis, meiosis, and spermiogenesis. During spermiogenesis, histones in post-meiotic spermatids are removed from chromatin and replaced by protamines. Although histone-to-protamine exchange is important for sperm nuclear condensation, the underlying regulatory mechanism is still poorly understood. Here, we identify PHD finger protein 7 (PHF7) as an E3 ubiquitin ligase for histone H3K14 in post-meiotic spermatids. Generation of Phf7-deficient mice and Phf7 C160A knockin mice with impaired E3 ubiquitin ligase activity reveals defects in histone-to-protamine exchange caused by dysregulation of histone removal factor Bromodomain, testis-specific (BRDT) in early condensing spermatids. Surprisingly, E3 ubiquitin ligase activity of PHF7 on histone ubiquitination leads to stabilization of BRDT by attenuating ubiquitination of BRDT. Collectively, our findings identify PHF7 as a critical factor for sperm chromatin condensation and contribute to mechanistic understanding of fundamental phenomenon of histone-to-protamine exchange and potential for drug development for the male reproduction system. Histone-to-protamine exchange is essential for functional sperm. Kim et al. demonstrate that PHF7 is an E3 ubiquitin ligase for histone H3, and that PHF7-mediated histone ubiquitination regulates BRDT stability during histone removal. Mice with impaired Phf7 show dysfunctional sperm caused by defects in histone ubiquitination and histone-to-protamine exchange.

この論文で使われている画像

参考文献

Baba, A., Ohtake, F., Okuno, Y., Yokota, K., Okada, M., Imai, Y., Ni, M., Meyer, C.A., Igarashi, K., Kanno, J., et al. (2011). PKA-dependent regulation of the his- tone lysine demethylase complex PHF2-ARID5B. Nat. Cell Biol. 13, 668–675.

Barral, S., Morozumi, Y., Tanaka, H., Montellier, E., Govin, J., de Dieuleveult, M., Charbonnier, G., Coute´ , Y., Puthier, D., Buchou, T., et al. (2017). Histone Variant H2A.L.2 Guides Transition Protein-Dependent Protamine Assembly in Male Germ Cells. Mol. Cell 66, 89–101.e8.

Berkovits, B.D., and Wolgemuth, D.J. (2013). The role of the double bromodo- main-containing BET genes during mammalian spermatogenesis. Curr. Top. Dev. Biol. 102, 293–326.

Bryant, J.M., Meyer-Ficca, M.L., Dang, V.M., Berger, S.L., and Meyer, R.G. (2013). Separation of spermatogenic cell types using STA-PUT velocity sedi- mentation. J. Vis. Exp. 80, 50648.

Butler, A., Hoffman, P., Smibert, P., Papalexi, E., and Satija, R. (2018). Inte- grating single-cell transcriptomic data across different conditions, technolo- gies, and species. Nat. Biotechnol. 36, 411–420.

Cai, L., Rothbart, S.B., Lu, R., Xu, B., Chen, W.Y., Tripathy, A., Rockowitz, S., Zheng, D., Patel, D.J., Allis, C.D., et al. (2013). An H3K36 methylation-engaging Tudor motif of polycomb-like proteins mediates PRC2 complex targeting. Mol. Cell 49, 571–582.

Chitalia, V.C., Foy, R.L., Bachschmid, M.M., Zeng, L., Panchenko, M.V., Zhou, M.I., Bharti, A., Seldin, D.C., Lecker, S.H., Dominguez, I., and Cohen, H.T. (2008). Jade-1 inhibits Wnt signalling by ubiquitylating beta-catenin and medi- ates Wnt pathway inhibition by pVHL. Nat. Cell Biol. 10, 1208–1216.

Cho, C., Willis, W.D., Goulding, E.H., Jung-Ha, H., Choi, Y.C., Hecht, N.B., and Eddy, E.M. (2001). Haploinsufficiency of protamine-1 or -2 causes infertility in mice. Nat. Genet. 28, 82–86.

Dai, X., Gan, W., Li, X., Wang, S., Zhang, W., Huang, L., Liu, S., Zhong, Q., Guo, J., Zhang, J., et al. (2017). Prostate cancer-associated SPOP mutations confer resistance to BET inhibitors through stabilization of BRD4. Nat. Med. 23, 1063– 1071.

Dhar, S., Thota, A., and Rao, M.R. (2012). Insights into role of bromodomain, testis-specific (Brdt) in acetylated histone H4-dependent chromatin remodel- ing in mammalian spermiogenesis. J. Biol. Chem. 287, 6387–6405.

Fujihara, Y., Kaseda, K., Inoue, N., Ikawa, M., and Okabe, M. (2013). Produc- tion of mouse pups from germline transmission-failed knockout chimeras. Transgenic Res. 22, 195–200.

Gaucher, J., Boussouar, F., Montellier, E., Curtet, S., Buchou, T., Bertrand, S., Hery, P., Jounier, S., Depaux, A., Vitte, A.L., et al. (2012). Bromodomain- dependent stage-specific male genome programming by Brdt. EMBO J. 31, 3809–3820.

Gou, L.T., Kang, J.Y., Dai, P., Wang, X., Li, F., Zhao, S., Zhang, M., Hua, M.M., Lu, Y., Zhu, Y., et al. (2017). Ubiquitination-Deficient Mutations in Human Piwi Cause Male Infertility by Impairing Histone-to-Protamine Exchange during Spermiogenesis. Cell 169, 1090–1104.e13.

Goudarzi, A., Shiota, H., Rousseaux, S., and Khochbin, S. (2014). Genome- scale acetylation-dependent histone eviction during spermatogenesis. J. Mol. Biol. 426, 3342–3349.

Goudarzi, A., Zhang, D., Huang, H., Barral, S., Kwon, O.K., Qi, S., Tang, Z., Bu- chou, T., Vitte, A.L., He, T., et al. (2016). Dynamic Competing Histone H4 K5K8 Acetylation and Butyrylation Are Hallmarks of Highly Active Gene Promoters. Mol. Cell 62, 169–180.

Green, C.D., Ma, Q., Manske, G.L., Shami, A.N., Zheng, X., Marini, S., Moritz, L., Sultan, C., Gurczynski, S.J., Moore, B.B., et al. (2018). A Comprehensive Roadmap of Murine Spermatogenesis Defined by Single-Cell RNA-Seq. Dev. Cell 46, 651–667.e10.

Griswold, M.D. (2016). Spermatogenesis: The Commitment to Meiosis. Phys- iol. Rev. 96, 1–17.

Han, X., Gui, B., Xiong, C., Zhao, L., Liang, J., Sun, L., Yang, X., Yu, W., Si, W., Yan, R., et al. (2014). Destabilizing LSD1 by Jade-2 promotes neurogenesis: an antibraking system in neural development. Mol. Cell 55, 482–494.

Hermann, B.P., Cheng, K., Singh, A., Roa-De La Cruz, L., Mutoji, K.N., Chen, I.C., Gildersleeve, H., Lehle, J.D., Mayo, M., Westernstro¨ er, B., et al. (2018). The mammalian spermatogenesis single-cell transcriptome, from spermato- gonial stem cells to spermatids. Cell Rep. 25, 1650–1667.e8.

Janouskova, H., El Tekle, G., Bellini, E., Udeshi, N.D., Rinaldi, A., Ulbricht, A., Bernasocchi, T., Civenni, G., Losa, M., Svinkina, T., et al. (2017). Opposing ef- fects of cancer-type-specific SPOP mutants on BET protein degradation and sensitivity to BET inhibitors. Nat. Med. 23, 1046–1054.

Kim, S., and Pevzner, P.A. (2014). MS-GF+ makes progress towards a univer- sal database search tool for proteomics. Nat. Commun. 5, 5277.

Lee, M., Kim, I.S., Park, K.C., Kim, J.S., Baek, S.H., and Kim, K.I. (2017). Mitosis-specific phosphorylation of Mis18a by Aurora B kinase enhances kinetochore recruitment of polo-like kinase 1. Oncotarget 9, 1563–1576

Li, G., Ci, W., Karmakar, S., Chen, K., Dhar, R., Fan, Z., Guo, Z., Zhang, J., Ke, Y., Wang, L., et al. (2014a). SPOP promotes tumorigenesis by acting as a key regulatory hub in kidney cancer. Cancer Cell 25, 455–468.

Li, W., Wu, J., Kim, S.Y., Zhao, M., Hearn, S.A., Zhang, M.Q., Meistrich, M.L., and Mills, A.A. (2014b). Chd5 orchestrates chromatin remodelling during sperm development. Nat. Commun. 5, 3812.

Liu, W., Tanasa, B., Tyurina, O.V., Zhou, T.Y., Gassmann, R., Liu, W.T., Ohgi, K.A., Benner, C., Garcia-Bassets, I., Aggarwal, A.K., et al. (2010). PHF8 medi- ates histone H4 lysine 20 demethylation events involved in cell cycle progres- sion. Nature 466, 508–512.

Lu, L.Y., Wu, J., Ye, L., Gavrilina, G.B., Saunders, T.L., and Yu, X. (2010). RNF8-dependent histone modifications regulate nucleosome removal during spermatogenesis. Dev. Cell 18, 371–384.

Matsumura, T., Noda, T., Muratani, M., Okada, R., Yamane, M., Isotani, A., Kudo, T., Takahashi, S., and Ikawa, M. (2019). Male mice, caged in the Inter- national Space Station for 35 days, sire healthy offspring. Sci. Rep. 9, 13733.

Matzuk, M.M., McKeown, M.R., Filippakopoulos, P., Li, Q., Ma, L., Agno, J.E., Lemieux, M.E., Picaud, S., Yu, R.N., Qi, J., et al. (2012). Small-molecule inhibi- tion of BRDT for male contraception. Cell 150, 673–684.

Miller, T.C., Simon, B., Rybin, V., Gro¨ tsch, H., Curtet, S., Khochbin, S., Carlo- magno, T., and Mu€ller, C.W. (2016). A bromodomain-DNA interaction facili- tates acetylation-dependent bivalent nucleosome recognition by the BET pro- tein BRDT. Nat. Commun. 7, 13855.

Morinie` re, J., Rousseaux, S., Steuerwald, U., Soler-Lo´ pez, M., Curtet, S., Vitte, A.L., Govin, J., Gaucher, J., Sadoul, K., Hart, D.J., et al. (2009). Cooperative binding of two acetylation marks on a histone tail by a single bromodomain. Nature 461, 664–668.

Noda, T., Oji, A., and Ikawa, M. (2017). Genome Editing in Mouse Zygotes and Embryonic Stem Cells by Introducing SgRNA/Cas9 Expressing Plasmids. Methods Mol. Biol. 1630, 67–80.

Noda, T., Sakurai, N., Nozawa, K., Kobayashi, S., Devlin, D.J., Matzuk, M.M., and Ikawa, M. (2019). Nine genes abundantly expressed in the epididymis are not essential for male fecundity in mice. Andrology 7, 644–653.

Oji, A., Noda, T., Fujihara, Y., Miyata, H., Kim, Y.J., Muto, M., Nozawa, K., Mat- sumura, T., Isotani, A., and Ikawa, M. (2016). CRISPR/Cas9 mediated genome editing in ES cells and its application for chimeric analysis in mice. Sci. Rep. 6, 31666.

Okada, Y., Scott, G., Ray, M.K., Mishina, Y., and Zhang, Y. (2007). Histone de- methylase JHDM2A is critical for Tnp1 and Prm1 transcription and spermato- genesis. Nature 450, 119–123.

Pivot-Pajot, C., Caron, C., Govin, J., Vion, A., Rousseaux, S., and Khochbin, S. (2003). Acetylation-dependent chromatin reorganization by BRDT, a testis- specific bromodomain-containing protein. Mol. Cell. Biol. 23, 5354–5365.

Qi, H.H., Sarkissian, M., Hu, G.Q., Wang, Z., Bhattacharjee, A., Gordon, D.B., Gonzales, M., Lan, F., Ongusaha, P.P., Huarte, M., et al. (2010). Histone H4K20/H3K9 demethylase PHF8 regulates zebrafish brain and craniofacial development. Nature 466, 503–507.

Qian, M.X., Pang, Y., Liu, C.H., Haratake, K., Du, B.Y., Ji, D.Y., Wang, G.F., Zhu, Q.Q., Song, W., Yu, Y., et al. (2013). Acetylation-mediated proteasomal degradation of core histones during DNA repair and spermatogenesis. Cell 153, 1012–1024.

Sasaki, K., Ito, T., Nishino, N., Khochbin, S., and Yoshida, M. (2009). Real-time imaging of histone H4 hyperacetylation in living cells. Proc. Natl. Acad. Sci. USA 106, 16257–16262.

Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., et al. (2012). Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682.

Shang, E., Nickerson, H.D., Wen, D., Wang, X., and Wolgemuth, D.J. (2007). The first bromodomain of Brdt, a testis-specific member of the BET sub-family of double-bromodomain-containing proteins, is essential for male germ cell differentiation. Development 134, 3507–3515.

Shapiro-Kulnane, L., Smolko, A.E., and Salz, H.K. (2015). Maintenance of Drosophila germline stem cell sexual identity in oogenesis and tumorigenesis. Development 142, 1073–1082.

Shiota, H., Barral, S., Buchou, T., Tan, M., Coute´ , Y., Charbonnier, G., Rey- noird, N., Boussouar, F., Ge´ rard, M., Zhu, M., et al. (2018). Nut Directs p300-Dependent, Genome-Wide H4 Hyperacetylation in Male Germ Cells. Cell Rep. 24, 3477–3487.e6.

Shirakata, Y., Hiradate, Y., Inoue, H., Sato, E., and Tanemura, K. (2014). His- tone h4 modification during mouse spermatogenesis. J. Reprod. Dev. 60, 383–387.

Sin, H.S., Barski, A., Zhang, F., Kartashov, A.V., Nussenzweig, A., Chen, J., Andreassen, P.R., and Namekawa, S.H. (2012). RNF8 regulates active epige- netic modifications and escape gene activation from inactive sex chromo- somes in post-meiotic spermatids. Genes Dev. 26, 2737–2748.

Toyoda, Y., Yokoyama, M., and Hosi, T. (1971). Studies on the fertilization of mouse eggs in vitro. II. Effects of in vitro pre-incubation of spermatozoa on time of sperm penetration of mouse eggs in vitro. Jpn. J. Anim. Reprod. 16, 152–157.

Tyanova, S., Temu, T., and Cox, J. (2016). The MaxQuant computational plat- form for mass spectrometry-based shotgun proteomics. Nat. Protoc. 11, 2301–2319.

Udeshi, N.D., Mertins, P., Svinkina, T., and Carr, S.A. (2013). Large-scale iden- tification of ubiquitination sites by mass spectrometry. Nat. Protoc. 8, 1950– 1960.

Wang, L., and Wolgemuth, D.J. (2016). BET Protein BRDT Complexes With HDAC1, PRMT5, and TRIM28 and Functions in Transcriptional Repression During Spermatogenesis. J. Cell. Biochem. 117, 1429–1438.

Wang, H., Zhao, R., Guo, C., Jiang, S., Yang, J., Xu, Y., Liu, Y., Fan, L., Xiong, W., Ma, J., et al. (2016). Knockout of BRD7 results in impaired spermatogen- esis and male infertility. Sci. Rep. 6, 21776.

Wang, T., Gao, H., Li, W., and Liu, C. (2019a). Essential Role of Histone Replacement and Modifications in Male Fertility. Front. Genet. 10, 962.

Wang, X., Kang, J.Y., Wei, L., Yang, X., Sun, H., Yang, S., Lu, L., Yan, M., Bai, M., Chen, Y., et al. (2019b). PHF7 is a novel histone H2A E3 ligase prior to his- tone-to-protamine exchange during spermiogenesis. Development 146, dev175547.

Wen, H., Li, J., Song, T., Lu, M., Kan, P.Y., Lee, M.G., Sha, B., and Shi, X. (2010). Recognition of histone H3K4 trimethylation by the plant homeodomain of PHF2 modulates histone demethylation. J. Biol. Chem. 285, 9322–9326.

Xia, X., Cai, H., Qin, S., and Xu, C. (2012). Histone acetylase inhibitor curcumin impairs mouse spermiogenesis-an in vitro study. PLoS ONE 7, e48673.

Yang, S.Y., Baxter, E.M., and Van Doren, M. (2012). Phf7 controls male sex determination in the Drosophila germline. Dev. Cell 22, 1041–1051.

Yang, S.Y., Chang, Y.C., Wan, Y.H., Whitworth, C., Baxter, E.M., Primus, S., Pi, H., and Van Doren, M. (2017). Control of a Novel Spermatocyte-Promoting Factor by the Male Germline Sex Determination Factor PHF7 of Drosophila melanogaster. Genetics 206, 1939–1949.

Zhang, P., Wang, D., Zhao, Y., Ren, S., Gao, K., Ye, Z., Wang, S., Pan, C.W., Zhu, Y., Yan, Y., et al. (2017). Intrinsic BET inhibitor resistance in SPOP- mutated prostate cancer is mediated by BET protein stabilization and AKT- mTORC1 activation. Nat. Med. 23, 1055–1062.

Zhuang, T., Hess, R.A., Kolla, V., Higashi, M., Raabe, T.D., and Brodeur, G.M. (2014). CHD5 is required for spermiogenesis and chromatin condensation. Mech. Dev. 131, 35–46.

参考文献をもっと見る

全国の大学の
卒論・修論・学位論文

一発検索!

この論文の関連論文を見る