Haploidy-linked cell proliferation defects limit larval growth in zebrafish.

IF 4.5 3区 生物学 Q1 BIOCHEMISTRY & MOLECULAR BIOLOGY
Open Biology Pub Date : 2024-10-01 Epub Date: 2024-10-09 DOI:10.1098/rsob.240126
Kan Yaguchi, Daiki Saito, Triveni Menon, Akira Matsura, Miyu Hosono, Takeomi Mizutani, Tomoya Kotani, Sreelaja Nair, Ryota Uehara
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引用次数: 0

Abstract

Haploid larvae in non-mammalian vertebrates are lethal, with characteristic organ growth retardation collectively called 'haploid syndrome'. In contrast to mammals, whose haploid intolerance is attributed to imprinting misregulation, the cellular principle of haploidy-linked defects in non-mammalian vertebrates remains unknown. Here, we investigated cellular defects that disrupt the ontogeny of gynogenetic haploid zebrafish larvae. Unlike diploid control larvae, haploid larvae manifested unscheduled cell death at the organogenesis stage, attributed to haploidy-linked p53 upregulation. Moreover, we found that haploid larvae specifically suffered the gradual aggravation of mitotic spindle monopolarization during 1-3 days post-fertilization, causing spindle assembly checkpoint-mediated mitotic arrest throughout the entire body. High-resolution imaging revealed that this mitotic defect accompanied the haploidy-linked centrosome loss occurring concomitantly with the gradual decrease in larval cell size. Either resolution of mitotic arrest or depletion of p53 partially improved organ growth in haploid larvae. Based on these results, we propose that haploidy-linked mitotic defects and cell death are parts of critical cellular causes shared among vertebrates that limit the larval growth in the haploid state, contributing to an evolutionary constraint on allowable ploidy status in the vertebrate life cycle.

与单倍体相关的细胞增殖缺陷限制了斑马鱼幼体的生长。
非哺乳类脊椎动物的单倍体幼虫是致命的,其特征性器官生长迟缓统称为 "单倍体综合征"。与哺乳动物的单倍体不耐受归因于印记失调不同,非哺乳脊椎动物单倍体相关缺陷的细胞原理仍不清楚。在这里,我们研究了破坏雌核发育单倍体斑马鱼幼体本体发育的细胞缺陷。与二倍体对照幼体不同,单倍体幼体在器官形成阶段表现出计划外的细胞死亡,这归因于与单倍体相关的 p53 上调。此外,我们还发现单倍体幼虫在受精后的1-3天内,有丝分裂纺锤体单极化逐渐加剧,导致整个身体的纺锤体组装检查点介导的有丝分裂停滞。高分辨率成像显示,这种有丝分裂缺陷伴随着与单倍体相关的中心体缺失,与此同时,幼虫细胞体积逐渐缩小。有丝分裂停滞的解决或 p53 的消耗都部分改善了单倍体幼虫的器官生长。基于这些结果,我们提出单倍体相关的有丝分裂缺陷和细胞死亡是脊椎动物共有的关键细胞原因的一部分,它们限制了单倍体状态下的幼虫生长,从而对脊椎动物生命周期中允许的倍数状态产生了进化限制。
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来源期刊
Open Biology
Open Biology BIOCHEMISTRY & MOLECULAR BIOLOGY-
CiteScore
10.00
自引率
1.70%
发文量
136
审稿时长
6-12 weeks
期刊介绍: Open Biology is an online journal that welcomes original, high impact research in cell and developmental biology, molecular and structural biology, biochemistry, neuroscience, immunology, microbiology and genetics.
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