The Lego hypothesis of tissue morphogenesis: stereotypic organization of parallel orientational cell adhesions for epithelial self-assembly.

IF 11 1区生物学 Q1 BIOLOGY Biological Reviews Pub Date : 2024-09-23 DOI:10.1111/brv.13147

Lili Zhang, Xiangyun Wei

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Abstract

How tissues develop distinct structures remains poorly understood. We propose herein the Lego hypothesis of tissue morphogenesis, which states that during tissue morphogenesis, the topographical properties of cell surface adhesion molecules can be dynamically altered and polarised by regulating the spatiotemporal expression and localization of orientational cell adhesion (OCA) molecules cell-autonomously and non-cell-autonomously, thus modulating cells into unique Lego pieces for self-assembling into distinct cytoarchitectures. This concept can be exemplified by epithelial morphogenesis, in which cells are coalesced into a sheet by many types of adhesions. Among them, parallel OCAs (pOCAs) at the lateral cell membranes are essential for configuring cells in parallel. Major pOCAs include Na⁺/K⁺-ATPase-mediated adhesions, Crumbs-mediated adhesions, tight junctions, adherens junctions, and desmosomes. These pOCAs align in stereotypical orders along the apical-to-basal axis, and their absolute positioning is also regulated. Such spatial organization of pOCAs underlies proper epithelial morphogenesis. Thus, a key open question about tissue morphogenesis is how to regulate OCAs to make compatible adhesive cellular Lego pieces for tissue construction.

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组织形态发生的乐高假说：上皮自组装的平行定向细胞粘附立体组织。

人们对组织如何形成独特的结构仍然知之甚少。我们在此提出了组织形态发生的乐高假说，即在组织形态发生过程中，细胞表面粘附分子的地形特性可通过调节细胞自主和非细胞自主的定向细胞粘附（OCA）分子的时空表达和定位而发生动态改变和极化，从而将细胞调节成独特的乐高积木，自我组装成独特的细胞结构。上皮细胞的形态发生就是这一概念的例证，在上皮细胞的形态发生过程中，细胞通过多种类型的粘附凝聚成片。其中，侧细胞膜上的平行 OCA（pOCAs）对于平行配置细胞至关重要。主要的平行 OCA 包括 Na+/K+-ATP 酶介导的粘附、Crumbs 介导的粘附、紧密连接、粘连和脱膜小体。这些 pOCAs 沿顶端至基底轴按定型顺序排列，其绝对位置也受到调控。pOCAs 的这种空间组织是上皮正常形态发生的基础。因此，关于组织形态发生的一个关键性开放问题是如何调节 OCA，使细胞乐高积木具有相容性粘合力，从而构建组织。

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

Biological Reviews 生物-生物学

CiteScore

21.30

自引率

2.00%

发文量

审稿时长

6-12 weeks

期刊介绍： Biological Reviews is a scientific journal that covers a wide range of topics in the biological sciences. It publishes several review articles per issue, which are aimed at both non-specialist biologists and researchers in the field. The articles are scholarly and include extensive bibliographies. Authors are instructed to be aware of the diverse readership and write their articles accordingly. The reviews in Biological Reviews serve as comprehensive introductions to specific fields, presenting the current state of the art and highlighting gaps in knowledge. Each article can be up to 20,000 words long and includes an abstract, a thorough introduction, and a statement of conclusions. The journal focuses on publishing synthetic reviews, which are based on existing literature and address important biological questions. These reviews are interesting to a broad readership and are timely, often related to fast-moving fields or new discoveries. A key aspect of a synthetic review is that it goes beyond simply compiling information and instead analyzes the collected data to create a new theoretical or conceptual framework that can significantly impact the field. Biological Reviews is abstracted and indexed in various databases, including Abstracts on Hygiene & Communicable Diseases, Academic Search, AgBiotech News & Information, AgBiotechNet, AGRICOLA Database, GeoRef, Global Health, SCOPUS, Weed Abstracts, and Reaction Citation Index, among others.