Replacement of protamines by nucleosomes in the male pronucleus

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R-HSA-9821993
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Homo sapiens
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5/5
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Replacement of protamines by nucleosomes in the male pronucleus
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In human sperm, about 85 to 90% of the genome is associated with protamines rather than histones (reviewed in Torres-Flores and Hernández-Hernández 2020, Ribas-Maynou et al. 2022). Protamines provide a much higher packing density of DNA in the nucleus but there are few reports of epigenetic marks on protamines (Brunner et al. 2014). After fertilization, protamines in the male pronucleus are replaced with histones provided by the oocyte cytoplasm (reviewed in Yang et al. 2015, Okada and Yamaguchi 2017). The result is a decondensation of sperm chromatin that produces a chromatin state that is permissive for transcription.
Dissociation of protamines from DNA appears to be controlled by phosphorylation of the protamines PRM1 and PRM2 (inferred from mouse homologs in Gou et al. 2020). The kinase SRPK1 phosphorylates both PRM1 and PRM2, which recruit the histone chaperones Nucleoplasmin 2 (NPM2) and HIRA (inferred from mouse homologs in Gou et al. 2020). NPM2 then dissociates the phosphorylated PRM1 from DNA. By inference NPM1 and NPM3, which are also present in the zygote, may also dissociate PRM1 and PRM2 from DNA (Okuwaki et al. 2012).
Nucleosomes in the zygote are characterized by H3.3 and H2AX (H2A.X) (reviewed in Martire and Banaszynski 2020). HIRA chaperones histone H3.3 and acts together with NPM proteins to assemble nucleosomes from individual histone proteins. Asymmetric dimethylation of H3.3 arginine-17 catalyzed by METTL23 is required for assembly of H3.3 into chromatin in the male pronucleus (inferred from mouse homologs in Hatanaka et al. 2017) . The oocyte-specific histone H1, H1FOO (H1.8, H1-8), is also deposited on the newly formed chromatin at this time and persists until the 8-cell stage (McGraw et al. 2006). In mouse embryos, H1foo is not required for development (Sánchez-Sáez et al. 2022).
Literature References
PubMed ID Title Journal Year
24443974 Epigenetic marking of sperm by post-translational modification of histones and protamines

Nanni, P, Mansuy, IM, Brunner, AM

Epigenetics Chromatin 2014
32765595 The Interplay Between Replacement and Retention of Histones in the Sperm Genome

Torres-Flores, U, Hernandez-Hernandez, A

Front Genet 2020
28930672 Histone H3 Methylated at Arginine 17 Is Essential for Reprogramming the Paternal Genome in Zygotes

Hatanaka, Y, Ogonuki, N, Shinkai, Y, Hirose, M, Shimizu, N, Hosoi, Y, Kurumizaka, H, Ogura, A, Inoue, K, Nakano, T, Tsusaka, T, Honda, A, Machida, S, Kamimura, S, Suzuki, T, Dohmae, N, Satoh, M, Morita, K, Matsumoto, K, Nakamura, T

Cell Rep 2017
32665685 The roles of histone variants in fine-tuning chromatin organization and function

Martire, S, Banaszynski, LA

Nat Rev Mol Cell Biol 2020
36348112 Functional Aspects of Sperm Chromatin Organization

Ward, WS, Ribas-Maynou, J, Nguyen, H, Wu, H

Results Probl Cell Differ 2022
28050628 Epigenetic modifications and reprogramming in paternal pronucleus: sperm, preimplantation embryo, and beyond

Yamaguchi, K, Okada, Y

Cell Mol Life Sci 2017
36429134 The Oocyte-Specific Linker Histone H1FOO Is Not Essential for Mouse Oogenesis and Fertility

Sánchez-Martín, M, Sánchez-Sáez, F, Pendás, AM, Llano, E, Condezo, YB, Felipe-Medina, N, Sainz-Urruela, R

Cells 2022
22362753 Function of homo- and hetero-oligomers of human nucleoplasmin/nucleophosmin family proteins NPM1, NPM2 and NPM3 during sperm chromatin remodeling

Saotome-Nakamura, A, Okuwaki, M, Nishimura, Y, Akashi, S, Nagata, K, Hisaoka, M, Sumi, A

Nucleic Acids Res 2012
32169215 Initiation of Parental Genome Reprogramming in Fertilized Oocyte by Splicing Kinase SRPK1-Catalyzed Protamine Phosphorylation

Gou, LT, Adams, JA, Zhao, J, Lim, DH, Li, H, Meng, F, Hao, Y, Rosenfeld, MG, Li, D, Ma, W, Liang, Z, Fu, XD, Liu, MF, Shao, C, Zhang, X, Wang, X, Aubol, BE, Mellon, PL, Xu, R, Zhang, X

Cell 2020
25328107 Maternal histone variants and their chaperones promote paternal genome activation and boost somatic cell reprogramming

Wu, W, Macfarlan, TS, Yang, P

Bioessays 2015
16470586 Characterization of linker histone H1FOO during bovine in vitro embryo development

Sirard, MA, McGraw, S, Tremblay, K, Vigneault, C

Mol Reprod Dev 2006
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epigenetic programming in the zygotic pronuclei (0044725)
Authored
May, B  (2022-12-12)
Reviewed
Xie, W  (2023-08-08)
Created
May, B  (2022-12-16)
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