Mechanisms of cilia regeneration in Xenopus multiciliated epithelium in vivo.

IF 6.5 1区生物学 Q1 BIOCHEMISTRY & MOLECULAR BIOLOGY EMBO Reports Pub Date : 2025-03-14 DOI:10.1038/s44319-025-00414-8

Venkatramanan G Rao, Vignesh A Subramanianbalachandar, Magdalena M Magaj, Stefanie Redemann, Saurabh S Kulkarni

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Abstract

Cilia regeneration is a physiological event, and while studied extensively in unicellular organisms, it remains poorly understood in vertebrates. In this study, using Xenopus multiciliated cells (MCCs), we demonstrate that, unlike unicellular organisms, deciliation removes the transition zone (TZ) and the ciliary axoneme. While MCCs immediately begin regenerating the axoneme, surprisingly, the TZ assembly is delayed. However, ciliary tip proteins, Sentan and Clamp, localize to regenerating cilia without delay. Using cycloheximide (CHX) to block protein synthesis, we show that the TZ protein B9d1 is not present in the cilia precursor pool and requires new transcription/translation, providing insights into the delayed repair of TZ. Moreover, MCCs in CHX treatment assemble fewer but near wild-type length cilia by gradually concentrating ciliogenesis proteins like IFTs at a few basal bodies. Using mathematical modeling, we show that cilia length, compared to cilia number, has a larger influence on the force generated by MCCs. Our results question the requirement of TZ in motile cilia assembly and provide insights into the fundamental question of how cells determine organelle size and number.

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章鱼体内多纤毛上皮细胞的纤毛再生机制

纤毛再生是一种生理现象，虽然对单细胞生物进行了广泛研究，但对脊椎动物的纤毛再生仍然知之甚少。在这项研究中，我们利用章鱼多纤毛细胞（MCCs）证明，与单细胞生物不同，纤毛脱落会移除过渡区（TZ）和纤毛轴丝。虽然睫状细胞立即开始再生轴丝，但令人惊讶的是，TZ的组装却延迟了。然而，纤毛顶端蛋白（Sentan和Clamp）却毫不延迟地定位到再生纤毛上。利用环己亚胺（CHX）阻断蛋白质合成，我们发现 TZ 蛋白 B9d1 并不存在于纤毛前体池中，而是需要新的转录/翻译，这为 TZ 的延迟修复提供了启示。此外，CHX 处理的 MCC 通过逐渐将纤毛生成蛋白（如 IFTs）集中在少数基底体上，组装出数量较少但接近野生型长度的纤毛。通过数学建模，我们发现与纤毛数量相比，纤毛长度对 MCCs 产生的力有更大的影响。我们的研究结果质疑了TZ在纤毛运动组装中的必要性，并为细胞如何决定细胞器大小和数量这一基本问题提供了见解。

本文章由计算机程序翻译，如有差异，请以英文原文为准。

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来源期刊

EMBO Reports 生物-生化与分子生物学

CiteScore

11.20

自引率

1.30%

发文量

267

审稿时长

1 months

期刊介绍： EMBO Reports is a scientific journal that specializes in publishing research articles in the fields of molecular biology, cell biology, and developmental biology. The journal is known for its commitment to publishing high-quality, impactful research that provides novel physiological and functional insights. These insights are expected to be supported by robust evidence, with independent lines of inquiry validating the findings. The journal's scope includes both long and short-format papers, catering to different types of research contributions. It values studies that: Communicate major findings: Articles that report significant discoveries or advancements in the understanding of biological processes at the molecular, cellular, and developmental levels. Confirm important findings: Research that validates or supports existing knowledge in the field, reinforcing the reliability of previous studies. Refute prominent claims: Studies that challenge or disprove widely accepted ideas or hypotheses in the biosciences, contributing to the correction and evolution of scientific understanding. Present null data: Papers that report negative results or findings that do not support a particular hypothesis, which are crucial for the scientific process as they help to refine or redirect research efforts. EMBO Reports is dedicated to maintaining high standards of scientific rigor and integrity, ensuring that the research it publishes contributes meaningfully to the advancement of knowledge in the life sciences. By covering a broad spectrum of topics and encouraging the publication of both positive and negative results, the journal plays a vital role in promoting a comprehensive and balanced view of scientific inquiry.