Origin and evolution of microvilli

IF 2.4 4区生物学 Q4 CELL BIOLOGY

Biology of the Cell Pub Date : 2024-09-05 DOI:10.1111/boc.202400054

Mylan Ansel, Kaustubh Ramachandran, Gautam Dey, Thibaut Brunet

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引用次数: 0

Abstract

Background Information

Microvilli are finger-like, straight, and stable cellular protrusions that are filled with F-actin and present a stereotypical length. They are present in a broad range of cell types across the animal tree of life and mediate several fundamental functions, including nutrient absorption, photosensation, and mechanosensation. Therefore, understanding the origin and evolution of microvilli is key to reconstructing the evolution of animal cellular form and function. Here, we review the current state of knowledge on microvilli evolution and perform a bioinformatic survey of the conservation of genes encoding microvillar proteins in animals and their unicellular relatives.

Results

We first present a detailed description of mammalian microvilli based on two well-studied examples, the brush border microvilli of enterocytes and the stereocilia of hair cells. We also survey the broader diversity of microvilli and discuss similarities and differences between microvilli and filopodia. Based on our bioinformatic survey coupled with carefully reconstructed molecular phylogenies, we reconstitute the order of evolutionary appearance of microvillar proteins. We document the stepwise evolutionary assembly of the “molecular microvillar toolkit” with notable bursts of innovation at two key nodes: the last common filozoan ancestor (correlated with the evolution of microvilli distinct from filopodia) and the last common choanozoan ancestor (correlated with the emergence of inter-microvillar adhesions).

Conclusion and Significance

We conclude with a scenario for the evolution of microvilli from filopodia-like ancestral structures in unicellular precursors of animals.

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微绒毛的起源和演变

背景信息微绒毛是指状、笔直和稳定的细胞突起，充满 F-肌动蛋白并呈现出定型的长度。它们存在于整个动物生命树中的多种细胞类型中，并介导着几种基本功能，包括营养吸收、光感受和机械感觉。因此，了解微绒毛的起源和进化是重建动物细胞形态和功能进化的关键。在此，我们回顾了有关微绒毛进化的知识现状，并对动物及其单细胞近亲中编码微绒毛蛋白的基因的保存情况进行了生物信息学调查：我们首先根据两个研究得比较清楚的例子--肠细胞的刷状缘微绒毛和毛细胞的立体纤毛--详细描述了哺乳动物的微绒毛。我们还调查了微绒毛更广泛的多样性，并讨论了微绒毛与丝状体之间的异同。基于我们的生物信息学调查和精心重建的分子系统进化，我们重建了微绒毛蛋白的进化出现顺序。我们记录了 "分子微绒毛工具包 "的逐步进化组装过程，其中在两个关键节点出现了显著的创新：最后一个共同的丝虫祖先（与微绒毛不同于丝状体的进化相关）和最后一个共同的choanozoan祖先（与微绒毛间粘附的出现相关）：最后，我们提出了动物单细胞前体中微绒毛从类似丝状体的祖先结构演化而来的设想。

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

Biology of the Cell 生物-细胞生物学

CiteScore

5.30

自引率

0.00%

发文量

审稿时长

>12 weeks

期刊介绍： The journal publishes original research articles and reviews on all aspects of cellular, molecular and structural biology, developmental biology, cell physiology and evolution. It will publish articles or reviews contributing to the understanding of the elementary biochemical and biophysical principles of live matter organization from the molecular, cellular and tissues scales and organisms. This includes contributions directed towards understanding biochemical and biophysical mechanisms, structure-function relationships with respect to basic cell and tissue functions, development, development/evolution relationship, morphogenesis, stem cell biology, cell biology of disease, plant cell biology, as well as contributions directed toward understanding integrated processes at the organelles, cell and tissue levels. Contributions using approaches such as high resolution imaging, live imaging, quantitative cell biology and integrated biology; as well as those using innovative genetic and epigenetic technologies, ex-vivo tissue engineering, cellular, tissue and integrated functional analysis, and quantitative biology and modeling to demonstrate original biological principles are encouraged.