Developmentally Regulated Post-translational Modification of Nucleoplasmin Controls Histone Sequestration and Deposition

Cell Reports
Takashi OnikuboDavid Shechter

Abstract

Nucleoplasmin (Npm) is an abundant histone chaperone in vertebrate oocytes and embryos. During embryogenesis, regulation of Npm histone binding is critical for its function in storing and releasing maternal histones to establish and maintain the zygotic epigenome. Here, we demonstrate that Xenopus laevis Npm post-translational modifications (PTMs) specific to the oocyte and egg promote either histone deposition or sequestration, respectively. Mass spectrometry and Npm phosphomimetic mutations used in chromatin assembly assays identified hyperphosphorylation on the N-terminal tail as a critical regulator for sequestration. C-terminal tail phosphorylation and PRMT5-catalyzed arginine methylation enhance nucleosome assembly by promoting histone interaction with the second acidic tract of Npm. Electron microscopy reconstructions of Npm and TTLL4 activity toward the C-terminal tail demonstrate that oocyte- and egg-specific PTMs cause Npm conformational changes. Our results reveal that PTMs regulate Npm chaperoning activity by modulating Npm conformation and Npm-histone interaction, leading to histone sequestration in the egg.

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Citations

Dec 16, 2016·Molecular Biology of the Cell·Faryal IjazMitsutoshi Setou
Aug 26, 2016·Scientific Reports·Noelia Fernández-RiveroAdelina Prado
Apr 14, 2017·Molecular Biology of the Cell·Mariah L HanleyTimothy J Mitchison
Feb 25, 2018·Cold Spring Harbor Protocols·Wei-Lin WangDavid Shechter
Oct 23, 2019·The Journal of Cell Biology·Pan ChenDaniel L Levy
Sep 6, 2020·Arthritis Research & Therapy·Yonghui DongJia Zheng
Sep 28, 2016·Biochemistry and Cell Biology = Biochimie Et Biologie Cellulaire·Daniel D Scott, Marlene Oeffinger
Nov 11, 2019·Cell Stress & Chaperones·Ashish Kumar, Dileep Vasudevan
Nov 28, 2019·Biological Reviews of the Cambridge Philosophical Society·Danton H O'DayRobert J Huber
Aug 5, 2020·Nature Structural & Molecular Biology·Kishore K MahalinganAntonina Roll-Mecak
Sep 3, 2020·Nutrients·Mirela IbrahimovicLaura A Kresty

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