Histone variants — ancient wrap artists of the epigenome

Key Points Canonical histones H2A, H2B, H3 and H4 wrap DNA to form nucleosome particles that compact the genome. Histone variants have diverse additional roles in chromosome metabolism and can differ from canonical histones in stability, DNA wrapping and specialized domains. The 'universal'...

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Published in:	Nature reviews. Molecular cell biology Vol. 11; no. 4; pp. 264 - 275
Main Authors:	Talbert, Paul B., Henikoff, Steven
Format:	Journal Article
Language:	English
Published:	London Nature Publishing Group UK 01.04.2010 Nature Publishing Group
Subjects:	631/337/100/102 631/337/100/1701 631/337/100/2286 631/535 Animals Biochemistry Biomedical and Life Sciences Cancer Research Cell Biology Chromosomes Deoxyribonucleic acid Developmental Biology DNA DNA binding proteins DNA Repair DNA replication Epigenesis, Genetic Evolution Genes Genetic Variation Genomes Histones Histones - genetics Humans Life Sciences Packaging Physiological aspects Protein Processing, Post-Translational Proteins review-article Sperm Stem Cells
ISSN:	1471-0072, 1471-0080, 1471-0080
Online Access:	Get full text
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Abstract	Key Points Canonical histones H2A, H2B, H3 and H4 wrap DNA to form nucleosome particles that compact the genome. Histone variants have diverse additional roles in chromosome metabolism and can differ from canonical histones in stability, DNA wrapping and specialized domains. The 'universal' variants, centromeric histone variant H3 (CenH3), H3.3, H2A.Z and H2A.X, appeared before the divergence of modern eukaryotes and function in common eukaryotic cellular processes such as histone replacement, chromosome segregation, DNA repair, and transcriptional regulation. Specialized histones have arisen in some lineages to perform additional tasks. Centromeric nucleosomes contain CenH3 and form the essential foundation of the kinetochore. The subunit composition of the CenH3 histone core has been the subject of lively debate and it has been found to wrap DNA in a right-handed direction, opposite to that of ordinary nucleosomes. H2A.Z has a conserved role in transcription initiation that might be descended from a hypothetical ancient mode of gene regulation by histone variants found in modern trypanosomes. Dynamic cellular processes might dramatically alter the stability of H2A.Z nucleosomes and thereby facilitate transcription initiation. Chromatin must be remodelled in processes such as DNA repair and sex chromosome silencing. Variants H2A.X and H3.3 have prominent roles in remodelling, with specialized sperm histones and protamines mediating sperm packaging and decondensation. Lineage-specific H2A variants have diverse carboxy-terminal tails that can wrap more DNA with additional oligopeptide motifs, or less DNA with a shorter docking domain. They sometimes have non-histone domains, which in macroH2As inhibit polyADP-ribosylation and contribute to conditional gene silencing. Histone core particles are spools for wrapping DNA, whereas histone variants have evolved diverse additional roles in chromosome metabolism. Some variants mediate universal functions, such as chromosome segregation and DNA repair, and others specialize in organism-specific tasks. Histones wrap DNA to form nucleosome particles that compact eukaryotic genomes. Variant histones have evolved crucial roles in chromosome segregation, transcriptional regulation, DNA repair, sperm packaging and other processes. 'Universal' histone variants emerged early in eukaryotic evolution and were later displaced for bulk packaging roles by the canonical histones (H2A, H2B, H3 and H4), the synthesis of which is coupled to DNA replication. Further specializations of histone variants have evolved in some lineages to perform additional tasks. Differences among histone variants in their stability, DNA wrapping, specialized domains that regulate access to DNA, and post-translational modifications, underlie the diverse functions that histones have acquired in evolution.
AbstractList	Histones wrap DNA to form nucleosome particles that compact eukaryotic genomes. Variant histones have evolved crucial roles in chromosome segregation, transcriptional regulation, DNA repair, sperm packaging and other processes. 'Universal' histone variants emerged early in eukaryotic evolution and were later displaced for bulk packaging roles by the canonical histones (H2A, H2B, H3 and H4), the synthesis of which is coupled to DNA replication. Further specializations of histone variants have evolved in some lineages to perform additional tasks. Differences among histone variants in their stability, DNA wrapping, specialized domains that regulate access to DNA, and post-translational modifications, underlie the diverse functions that histones have acquired in evolution. Histones wrap DNA to form nucleosome particles that compact eukaryotic genomes. Variant histones have evolved crucial roles in chromosome segregation, transcriptional regulation, DNA repair, sperm packaging and other processes. 'Universal' histone variants emerged early in eukaryotic evolution and were later displaced for bulk packaging roles by the canonical histones (H2A, H2B, H3 and H4), the synthesis of which is coupled to DNA replication. Further specializations of histone variants have evolved in some lineages to perform additional tasks. Differences among histone variants in their stability, DNA wrapping, specialized domains that regulate access to DNA, and post-translational modifications, underlie the diverse functions that histones have acquired in evolution.Histones wrap DNA to form nucleosome particles that compact eukaryotic genomes. Variant histones have evolved crucial roles in chromosome segregation, transcriptional regulation, DNA repair, sperm packaging and other processes. 'Universal' histone variants emerged early in eukaryotic evolution and were later displaced for bulk packaging roles by the canonical histones (H2A, H2B, H3 and H4), the synthesis of which is coupled to DNA replication. Further specializations of histone variants have evolved in some lineages to perform additional tasks. Differences among histone variants in their stability, DNA wrapping, specialized domains that regulate access to DNA, and post-translational modifications, underlie the diverse functions that histones have acquired in evolution. Key Points Canonical histones H2A, H2B, H3 and H4 wrap DNA to form nucleosome particles that compact the genome. Histone variants have diverse additional roles in chromosome metabolism and can differ from canonical histones in stability, DNA wrapping and specialized domains. The 'universal' variants, centromeric histone variant H3 (CenH3), H3.3, H2A.Z and H2A.X, appeared before the divergence of modern eukaryotes and function in common eukaryotic cellular processes such as histone replacement, chromosome segregation, DNA repair, and transcriptional regulation. Specialized histones have arisen in some lineages to perform additional tasks. Centromeric nucleosomes contain CenH3 and form the essential foundation of the kinetochore. The subunit composition of the CenH3 histone core has been the subject of lively debate and it has been found to wrap DNA in a right-handed direction, opposite to that of ordinary nucleosomes. H2A.Z has a conserved role in transcription initiation that might be descended from a hypothetical ancient mode of gene regulation by histone variants found in modern trypanosomes. Dynamic cellular processes might dramatically alter the stability of H2A.Z nucleosomes and thereby facilitate transcription initiation. Chromatin must be remodelled in processes such as DNA repair and sex chromosome silencing. Variants H2A.X and H3.3 have prominent roles in remodelling, with specialized sperm histones and protamines mediating sperm packaging and decondensation. Lineage-specific H2A variants have diverse carboxy-terminal tails that can wrap more DNA with additional oligopeptide motifs, or less DNA with a shorter docking domain. They sometimes have non-histone domains, which in macroH2As inhibit polyADP-ribosylation and contribute to conditional gene silencing. Histone core particles are spools for wrapping DNA, whereas histone variants have evolved diverse additional roles in chromosome metabolism. Some variants mediate universal functions, such as chromosome segregation and DNA repair, and others specialize in organism-specific tasks. Histones wrap DNA to form nucleosome particles that compact eukaryotic genomes. Variant histones have evolved crucial roles in chromosome segregation, transcriptional regulation, DNA repair, sperm packaging and other processes. 'Universal' histone variants emerged early in eukaryotic evolution and were later displaced for bulk packaging roles by the canonical histones (H2A, H2B, H3 and H4), the synthesis of which is coupled to DNA replication. Further specializations of histone variants have evolved in some lineages to perform additional tasks. Differences among histone variants in their stability, DNA wrapping, specialized domains that regulate access to DNA, and post-translational modifications, underlie the diverse functions that histones have acquired in evolution.
Audience	Academic
Author	Henikoff, Steven Talbert, Paul B.
Author_xml	– sequence: 1 givenname: Paul B. surname: Talbert fullname: Talbert, Paul B. organization: Howard Hughes Medical Institute, Fred Hutchinson Cancer Research Center – sequence: 2 givenname: Steven surname: Henikoff fullname: Henikoff, Steven organization: Howard Hughes Medical Institute, Fred Hutchinson Cancer Research Center
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/20197778$$D View this record in MEDLINE/PubMed
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Snippet	Key Points Canonical histones H2A, H2B, H3 and H4 wrap DNA to form nucleosome particles that compact the genome. Histone variants have diverse additional roles... Histones wrap DNA to form nucleosome particles that compact eukaryotic genomes. Variant histones have evolved crucial roles in chromosome segregation,...
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SubjectTerms	631/337/100/102 631/337/100/1701 631/337/100/2286 631/535 Animals Biochemistry Biomedical and Life Sciences Cancer Research Cell Biology Chromosomes Deoxyribonucleic acid Developmental Biology DNA DNA binding proteins DNA Repair DNA replication Epigenesis, Genetic Evolution Genes Genetic Variation Genomes Histones Histones - genetics Humans Life Sciences Packaging Physiological aspects Protein Processing, Post-Translational Proteins review-article Sperm Stem Cells
Title	Histone variants — ancient wrap artists of the epigenome
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