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组蛋白及变体在染色质重塑中的功能:以水生动物精子发生为例
徐文腾,孙雪雪
1.广东海洋大学水产学院 广东省水产动物病害防控与健康养殖重点实验室 广东 湛江 524088;2.中国水产科学研究院黄海水产研究所 海水养殖生物育种与可持续产出全国重点实验室 青岛海洋科技中心海洋渔业科学与食物产出过程功能实验室 山东 青岛 266071
摘要:
两性生殖中,精子作为携带父本信息的载体,是物种延续的关键因素。精子发生经历精原细胞、初级和次级精母细胞、圆形精子、成熟精子阶段。在圆形精子形成成熟精子过程中,染色质进行重塑,细胞形态发生剧烈变化,其中,组蛋白修饰和组蛋白变体在这些过程中发挥了重要作用:如甲基化主要与基因表达的激活或抑制有关;乙酰化激活转录活性并参与组蛋白沉积和DNA修复;磷酸化促进转录后修饰或参与DNA双链断裂修复;泛素化调节不同细胞途径中各式各样的蛋白质底物。组蛋白变体在调节染色体结构中发挥重要功能:如组蛋白H1变体在分化过程中具有抑制转录的作用;组蛋白H2A和H2B变体在精子染色质包装过程中发挥特有功能;H3.3是H3最重要的变体,在细胞周期的各时期都有表达;组蛋白H4则是进化最慢的组蛋白之一,目前还没有发现其组蛋白变体。本文围绕组蛋白翻译后修饰,梳理了甲基化、乙酰化、磷酸化、泛素化等方面的最新进展和组蛋白变体在染色质重塑过程中的功能研究进展,随后针对各类组蛋白变体及其功能进行了总结,最后以半滑舌鳎(Cynoglossus semilaevis)为例简要介绍这些研究对水生动物精子发生的启示。
关键词:  组蛋白  翻译后修饰  染色质重塑  精子发生
DOI:
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基金项目:国家重点研发计划(2022YFD2400405)和国家自然科学基金(32072955)共同资助
Function of histones and variants in chromatin remodeling: A case study of spermatogenesis in aquatic animals
XU Wenteng1,2,3,4,5, SUN Xuexue1,2,3,4,5
1.College of Fisheries, Guangdong Ocean University;2.Guangdong Provincial Key Laboratory of Aquatic Animal Disease Control and Healthy Culture, Zhanjiang 524088, China;3.Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences;4.State Key Laboratory of Mariculture Biobreeding and Sustainable Goods;5.Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao Marine Science and Technology Center, Qingdao 266071, China
Abstract:
Epigenetics refers to heritable changes that do not affect DNA sequences. Compared to genetic changes, epigenetic changes affect gene expression and protein products in cells, and these changes are reversible and dependent on the environment. There are three major types of epigenetic changes: DNA methylation, histone post-translational modifications (PTMs) increase the functional diversity of the proteome through the covalent addition of functional groups or proteins, proteolytic cleavage of regulatory subunits, or degradation of whole proteins), and non-coding Ribonucleic Acid.. This study focused on post-translational histone modifications. There are five main histone types: H1/H5, H2A, H2B, H3, and H4. Genes encoding histones do not contain introns and are among the most conserved proteins in eukaryotes. Histones are basic structural proteins comprising eukaryotic chromosomes. Generally, two molecules, H2A, H2B, H3, and H4 form a histone octamer that combines with DNA to form a structural unit called a nucleosome. This nucleosome appears every 200 bp and is connected by H1 histones to form chromatin. Histone modification refers to the addition of functional groups to histone tails, most commonly lysines. This process regulates gene expression by altering chromatin structure through condensation and depolymerization. Additionally, histone modification creates binding sites for various proteins. Histone modifications reported in animals include methylation, acetylation, phosphorylation, ubiquitination, SUMOylation (which is a small ubiquitin-related modifier involved in post-translational modification of proteins), ADP-ribosylation (which is a small ubiquitin-related modifier involved in post-translational modification of proteins), and short-chain lysine acylation. Many studies have shown that chromatin remodeling is a key step in spermatogenesis, involving the transformation of histones to protamines. Briefly, protamine replacement requires (Ⅰ) histone PTMs to promote the opening of histone-based chromatin structures, especially histone hyperacetylation and incorporation into histone variants; (Ⅱ) binding of bromine domain proteins to acetyl residues and remodeling of chromatin; (Ⅲ) formation and repair of DNA strand breaks in chromatin remodeling; and (Ⅳ) incorporation of protamine. Herein, we focused on Process (Ⅰ). In bisexual reproduction, sperm, as a paternal information carrier, is a key factor in a species continuation. Spermatogenesis includes various stages, including spermatogonia, primary and secondary spermatocytes, round sperms, and mature sperms. During round sperm transformation into mature sperm, chromatin remodeling occurs and cell morphology undergoes dramatic changes, in which histone PTMs and variants are essential. Histone PTMs patterns affect gene expression over a wide range, such as methylation, which is mainly related to gene expression activation or inhibition; acetylation, which activates transcriptional activity and participates in histone deposition and DNA repair; phosphorylation, which promotes post-transcriptional modification or participates in DNA double-strand break repair; and ubiquitin, which regulates various protein substrates in different cellular pathways. Histone variants have special functions in regulating chromosome structure. For example, histone H1 variants inhibit transcription during differentiation, histone H2A and H2B variants play a unique role in sperm chromatin packaging, H3.3 is the most important variant of H3, which is expressed in all stages of the cell cycle and participates in chromosome formation outside the S phase, Histone H4 is one of the slowest evolving proteins, and no histone variant has ever been found. Focusing on post-translational histone modifications, this study reviews the latest progress in methylation, acetylation, phosphorylation, and ubiquitination. Subsequently, the histone variants and their functions in chromatin remodeling are summarized. Finally, using Cynoglossus semilaevis as an example, this study briefly introduces the implications of these studies on spermatogenesis in aquatic animals. Elucidating the effect of PTMs on spermatogenesis will aid in exploring the regulatory mechanism of specific sperm (W-type) absence, which expands the fundamental theory of reproductive biology and provides novel solutions to monosex fry cultivation in aquaculture.
Key words:  Histone  Post-translational modification  Chromatin remodeling  Spermatogenesis