title: The specification and global reprogramming of histone epigenetic marks during gamete formation and early embryo development in C. elegans.
abstract: In addition to the DNA contributed by sperm and oocytes, embryos receive parent-specific epigenetic information that can include histone variants, histone post-translational modifications (PTMs), and DNA methylation. However, a global view of how such marks are erased or retained during gamete formation and reprogrammed after fertilization is lacking. To focus on features conveyed by histones, we conducted a large-scale proteomic identification of histone variants and PTMs in sperm and mixed-stage embryo chromatin from C. elegans, a species that lacks conserved DNA methylation pathways. The fate of these histone marks was then tracked using immunostaining. Proteomic analysis found that sperm harbor ∼2.4 fold lower levels of histone PTMs than embryos and revealed differences in classes of PTMs between sperm and embryos. Sperm chromatin repackaging involves the incorporation of the sperm-specific histone H2A variant HTAS-1, a widespread erasure of histone acetylation, and the retention of histone methylation at sites that mark the transcriptional history of chromatin domains during spermatogenesis. After fertilization, we show HTAS-1 and 6 histone PTM marks distinguish sperm and oocyte chromatin in the new embryo and characterize distinct paternal and maternal histone remodeling events during the oocyte-to-embryo transition. These include the exchange of histone H2A that is marked by ubiquitination, retention of HTAS-1, removal of the H2A variant HTZ-1, and differential reprogramming of histone PTMs. This work identifies novel and conserved features of paternal chromatin that are specified during spermatogenesis and processed in the embryo. Furthermore, our results show that different species, even those with diverged DNA packaging and imprinting strategies, use conserved histone modification and removal mechanisms to reprogram epigenetic information.
authors.affiliation: Department of Biology, San Francisco State University, San Francisco, California, United States of America.
authors.forename: Mark
authors.initials: M
authors.lastname: Samson
authors.affiliation: Department of Biology, San Francisco State University, San Francisco, California, United States of America.
authors.forename: Margaret M
authors.initials: MM
authors.lastname: Jow
authors.affiliation: Department of Chemical Physiology, The Scripps Research Institute, La Jolla, California, United States of America; Mass Spectrometry Division, National Center for Protein Science Shanghai, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Science, Shanghai, China.
authors.forename: Catherine C L
authors.initials: CC
authors.lastname: Wong
authors.affiliation: Department of Biology, San Francisco State University, San Francisco, California, United States of America.
authors.forename: Colin
authors.initials: C
authors.lastname: Fitzpatrick
authors.affiliation: Department of Chemical Physiology, The Scripps Research Institute, La Jolla, California, United States of America.
authors.forename: Aaron
authors.initials: A
authors.lastname: Aslanian
authors.affiliation: Department of Biology, San Francisco State University, San Francisco, California, United States of America.
authors.forename: Israel
authors.initials: I
authors.lastname: Saucedo
authors.affiliation: Department of Biology, San Francisco State University, San Francisco, California, United States of America.
authors.forename: Rodrigo
authors.initials: R
authors.lastname: Estrada
authors.affiliation: Department of Biochemistry, Nagasaki University School of Medicine, Nagasaki, Japan.
authors.forename: Takashi
authors.initials: T
authors.lastname: Ito
authors.affiliation: Department of Chemical Physiology, The Scripps Research Institute, La Jolla, California, United States of America.
authors.forename: Sung-kyu Robin
authors.initials: SK
authors.lastname: Park
authors.affiliation: Department of Chemical Physiology, The Scripps Research Institute, La Jolla, California, United States of America.
authors.forename: John R
authors.initials: JR
authors.lastname: Yates
authors.affiliation: Department of Biology, San Francisco State University, San Francisco, California, United States of America.
authors.forename: Diana S
authors.initials: DS
authors.lastname: Chu
mesh_terms: D000107:Acetylation; D000595:Amino Acid Sequence; D000818:Animals; D017173:Caenorhabditis elegans / Q000196:embryology* / Q000235:genetics*; D029742:Caenorhabditis elegans Proteins / Q000235:genetics / Q000378:metabolism; D002843:Chromatin / Q000378:metabolism; D004625:Embryo, Nonmammalian; D044127:Epigenesis, Genetic; D005260:Female; D018507:Gene Expression Regulation, Developmental; D006657:Histones / Q000378:metabolism*; D008297:Male; D008745:Methylation; D008969:Molecular Sequence Data; D009865:Oocytes / Q000378:metabolism; D011499:Protein Processing, Post-Translational; D013094:Spermatozoa / Q000378:metabolism / Q000502:physiology*; D054875:Ubiquitination
chemical_list: D029742:Caenorhabditis elegans Proteins; D002843:Chromatin; D006657:Histones