Proteomic analysis of the sponge Aggregation Factor implicates an ancient toolkit for allorecognition and adhesion in animals

IF 9.4 1区 综合性期刊 Q1 MULTIDISCIPLINARY SCIENCES
Fabian Ruperti, Monika Dzieciatkowska, M. Sabrina Pankey, Cedric S. Asensio, Dario Anselmetti, Xavier Fernàndez-Busquets, Scott A. Nichols
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Abstract

The discovery that sponges (Porifera) can fully regenerate from aggregates of dissociated cells launched them as one of the earliest experimental models to study the evolution of cell adhesion and allorecognition in animals. This process depends on an extracellular glycoprotein complex called the Aggregation Factor (AF), which is composed of proteins thought to be unique to sponges. We used quantitative proteomics to identify additional AF components and interacting proteins in the classical model, Clathria prolifera , and compared them to proteins involved in cell interactions in Bilateria. Our results confirm MAFp3/p4 proteins as the primary components of the AF but implicate related proteins with calx-beta and wreath domains as additional components. Using AlphaFold, we unveiled close structural similarities of AF components to protein domains in other animals, previously masked by the mutational decay of sequence similarity. The wreath domain, believed to be unique to the AF, was predicted to contain a central beta-sandwich of the same organization as the vWFD domain (also found in extracellular, gel-forming glycoproteins in other animals). Additionally, many copurified proteins share a conserved C-terminus, containing divergent immunoglobulin (Ig) and Fn3 domains predicted to serve as an AF–interaction interface. One of these proteins, MAF-associated protein 1, resembles Ig superfamily cell adhesion molecules and we hypothesize that it may function to link the AF to the surface of cells. Our results highlight the existence of an ancient toolkit of conserved protein domains regulating cell–cell and cell–extracellular matrix protein interactions in all animals, and likely reflect a common origin of cell adhesion and allorecognition.
海绵聚集因子的蛋白质组分析揭示了动物异体识别和粘附的古老工具包
海绵(Porifera)可以从游离细胞的聚集体中完全再生,这一发现使其成为最早研究动物细胞粘附和异体识别进化的实验模型之一。这一过程依赖于一种叫做聚集因子(AF)的细胞外糖蛋白复合物,它由被认为是海绵特有的蛋白质组成。我们使用定量蛋白质组学方法鉴定了经典模型Clathria prolifera中额外的AF成分和相互作用蛋白,并将它们与Bilateria中参与细胞相互作用的蛋白进行了比较。我们的研究结果证实了MAFp3/p4蛋白是AF的主要成分,但与calx- β和环结构域相关的蛋白是附加成分。使用AlphaFold,我们揭示了AF成分与其他动物蛋白质结构域的密切结构相似性,以前被序列相似性的突变衰减所掩盖。花环结构域,被认为是AF独有的,预计包含与vWFD结构域(也存在于其他动物的细胞外凝胶形成糖蛋白中)相同组织的中央β -三明治。此外,许多共化蛋白共享一个保守的c端,包含不同的免疫球蛋白(Ig)和Fn3结构域,被预测为af相互作用的界面。其中一种蛋白,maf相关蛋白1,类似于Ig超家族细胞粘附分子,我们假设它可能起连接AF与细胞表面的作用。我们的研究结果强调了在所有动物中都存在一种古老的保守蛋白结构域工具箱,用于调节细胞-细胞和细胞-细胞外基质蛋白相互作用,并可能反映了细胞粘附和异体识别的共同起源。
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来源期刊
CiteScore
19.00
自引率
0.90%
发文量
3575
审稿时长
2.5 months
期刊介绍: The Proceedings of the National Academy of Sciences (PNAS), a peer-reviewed journal of the National Academy of Sciences (NAS), serves as an authoritative source for high-impact, original research across the biological, physical, and social sciences. With a global scope, the journal welcomes submissions from researchers worldwide, making it an inclusive platform for advancing scientific knowledge.
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