Staying connected under tension

doi:10.1126/science.abf2782

GSTDTAP > 气候变化

DOI	10.1126/science.abf2782
	Staying connected under tension
	Srikala Raghavan; Valeri Vasioukhin
	2020-11-27
发表期刊	Science
出版年	2020
英文摘要	The primary function of cells in all epithelial tissues is to form a physical barrier separating different compartments. Cell-cell adhesion structures seal neighboring membranes to form a barrier. Depending on the number of cells that are clumped together, these are called bicellular or tricellular junctions ([ 1 ][1]). During development and normal tissue homeostasis, cells in epithelia move and change their respective positions without complete loss of membrane connections and disruption of junctions. The mechanisms responsible for this junctional remodeling are not well understood. On page 1060 of this issue, Yu and Zallen ([ 2 ][2]) identify a signaling pathway that connects changes in mechanical forces at tricellular junctions with biochemical signals that either reinforce or weaken these adhesion structures. These results provide a molecular basis for understanding how cells sense and react to the mechanical changes in their environment. Yu and Zallen studied early embryonic development in vivo using the fruit fly Drosophila melanogaster . During a process called convergent extension, cells in the surface epithelial sheet migrate and change their respective positions in a highly organized manner and without disrupting the tissue architecture ([ 3 ][3]). Epithelial cells are held together by adherens junctions that are connected through transmembrane cadherins, proteins that also link to the actomyosin cytoskeleton. Adherens junctions are used by cells to sense mechanical signals from their neighbors ([ 4 ][4], [ 5 ][5]). Cells use various mechanisms for mechanotransduction, to convert mechanical stimuli into biochemical signals. The mechanisms underpinning mechanotransduction at bicellular junctions in cultured cells have been identified. However, less is known about how these signals govern collective cell rearrangements in vivo and whether distinct mechanisms are involved at tricellular junctions ([ 5 ][5]). Tricellular adherens junctions are special: They need to withstand tremendous forces, and besides cadherins, they also contain the cell-cell adhesion protein Sidekick ([ 6 ][6]). In addition, actin-binding proteins Canoe and Polychaetoid are enriched at tricellular junctions. They interact with each other and act in parallel in junctional remodeling and maintenance of epithelial integrity during morphogenesis ([ 7 ][7]). Sidekick physically interacts with Polychaetoid and is necessary to organize Polychaetoid and Canoe at tricellular junctions and link these structur es to the actin cytoskeleton ([ 8 ][8]). Canoe membrane localization is also regulated by the small guanosine triphosphatase (GTPase) Rap1 and its effector protein Dizzy ([ 9 ][9]). Tricellular junctions nucleate actomyosin fibers, which help to limit elongation of larger cells and regulate the Hippo signaling pathway to favor the divisions of larger cells to control the final number and size of cells within a tissue ([ 10 ][10]). The mechanisms connecting mechanical forces with biochemical pathways that regulate tricellular junction assembly and function were not known. Yu and Zallen found that an increase in mechanical tension at the tricellular junction results in the Abelson tyrosine kinase (Abl)–mediated phosphorylation of Canoe, which directs it to tricellular junctions to promote connection to the actin cytoskeleton, thus increasing its mechanical strength during convergent extension movement ([ 3 ][3]). ![Figure][11] Regulating junction strength The strengths of tricellular junctions are dynamically regulated in response to changes in mechanical tension during Drosophila melanogaster morphogenesis. Increased tension results in Abelson tyrosine kinase (Abl)–mediated phosphorylation of Canoe, which then accumulates at tricellular junctions and reinforces them by promoting connection with the actin cytoskeleton. GRAPHIC: C. BICKEL/ SCIENCE Abl was first discovered as a primary driver of leukemia and later was implicated in regulation of diverse cellular functions involving cytoskeletal changes, cellular motility, polarity, and adhesion ([ 11 ][12]). Imatinib, a prototypical example of targeted cancer therapy, inhibits abnormally activated ABL in the BRC-ABL fusion protein that causes chronic myeloid leukemia. Additionally, Abl was previously identified as a kinase that phosphorylates the cell adhesion protein β-catenin and directs bicellular junction remodeling during D. melanogaster convergent extension ([ 12 ][13]). If Abl-mediated phosphorylation of Canoe is necessary for its function, what regulates this phosphorylation? This is the most exciting discovery of the study. Yu and Zallen found that Canoe phosphorylation and its localization at tricellular junctions are mechanosensitive. The dynamic and tension-regulated localization of Canoe to tricellular junctions was necessary for their remodeling and proper cellular movements during convergent extension. Yu and Zallen observed that Canoe recruitment was strongly correlated with bursts of myosin accumulation at tricellular junctions and that its localization was uncoupled from myosin in the absence of Abl activity. This finding prompted the authors to ask if the localization of Canoe was regulated by force and if this was part of a force-regulated mechanism that strengthens adhesion at tricellular junctions under tension. They found that Canoe localization at tricellular junctions requires mechanical forces generated by actomyosin contractility (see the figure). Moreover, constitutive and mechanically uncoupled localization of Canoe to tricellular junctions resulted in their overstabilization and delayed or reduced cell rearrangements. Therefore, mechanosensitive coupling of Canoe localization to tricellular junctions was necessary for proper junction remodeling during morphogenesis. The loss of this localization caused disruption of tricellular junctions, whereas constitutive localization resulted in tricellular junction overstabilization and prevented normal morphogenesis. Substantial knowledge has been accumulated concerning the mechanotransduction mechanisms at bicellular junctions ([ 5 ][5]). α-Catenin and vinculin, two actin-binding proteins that link junctional cadherins with the cytoskeleton, play a central role in this process. Increased actomyosin tension stretches α-catenin, which in turn increases the strength of its F-actin binding domain and, in addition, opens up the binding site for vinculin, which then accumulates at the junctions and reinforces their connection to the actin cytoskeleton ([ 13 ][14], [ 14 ][15]). Vinculin can also be phosphorylated by Abl at Tyr822, and this stabilizes its active open conformation, promotes association with F-actin, and strengthens cell-cell junctions ([ 15 ][16]). The connections between cytoskeletal tension, Abl-mediated Canoe phosphorylation, and its targeting to tricellular junctions found by Yu and Zallen provide important insights about the distinct mechanisms governing mechanotransduction. As with all exciting discoveries, the study of Yu and Zallen raises new questions. What is the primary tension-dependent mechanosensor at tricellular junctions? How exactly is phosphorylated Canoe targeted to tricellular junctions? It is also unknown if additional scaffolding or signaling molecules are recruited to tricellular junctions in a tension-dependent manner. The availability of powerful in vivo model systems and tools will help to answer these questions and uncover additional mechanisms connecting mechanical forces to changes in cellular functions enabling adaptive control of morphogenesis. 1. [↵][17]1. F. Bosveld et al ., Curr. Opin. Cell Biol. 54, 80 (2018). [OpenUrl][18] 2. [↵][19]1. H. H. Yu, 2. J. A. Zallen , Science 370, eaba5528 (2020). [OpenUrl][20][Abstract/FREE Full Text][21] 3. [↵][22]1. K. Z. Perez-Vale, 2. M. Peifer , Development 147, dev191049 (2020). [OpenUrl][23][Abstract/FREE Full Text][24] 4. [↵][25]1. O. Klezovitch, 2. V. Vasioukhin , F1000 Res. 4, 550 (2015). [OpenUrl][26] 5. [↵][27]1. A. Angulo-Urarte, 2. T. van der Wal, 3. S. Huveneers , Biochim. Biophys. Acta Biomembr. 1862, 183316 (2020). [OpenUrl][28][CrossRef][29] 6. [↵][30]1. T. Higashi, 2. H. Chiba , Biochim. Biophys. 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{openurl}?query=rft.jtitle%253DJ.%2BCell%2BBiol.%26rft_id%253Dinfo%253Adoi%252F10.1083%252Fjcb.201309092%26rft_id%253Dinfo%253Apmid%252F24751539%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx [67]: /lookup/ijlink/YTozOntzOjQ6InBhdGgiO3M6MTQ6Ii9sb29rdXAvaWpsaW5rIjtzOjU6InF1ZXJ5IjthOjQ6e3M6ODoibGlua1R5cGUiO3M6NDoiQUJTVCI7czoxMToiam91cm5hbENvZGUiO3M6MzoiamNiIjtzOjU6InJlc2lkIjtzOjk6IjIwNS8yLzI1MSI7czo0OiJhdG9tIjtzOjIzOiIvc2NpLzM3MC82NTIwLzEwMzYuYXRvbSI7fXM6ODoiZnJhZ21lbnQiO3M6MDoiIjt9
领域	气候变化 ; 资源环境
URL	查看原文
引用统计
文献类型	期刊论文
条目标识符	http://119.78.100.173/C666/handle/2XK7JSWQ/304870
专题	气候变化资源环境科学
推荐引用方式 GB/T 7714	Srikala Raghavan,Valeri Vasioukhin. Staying connected under tension[J]. Science,2020.
APA	Srikala Raghavan,&Valeri Vasioukhin.(2020).Staying connected under tension.Science.
MLA	Srikala Raghavan,et al."Staying connected under tension".Science (2020).