An optochemical tool for light-induced dissociation of adherens junctions to control mechanical coupling between cells

Ollech, Dirk; Pflästerer, Tim; Shellard, Adam; Zambarda, Chiara; Spatz, Joachim P.; Marcq, Philippe; Mayor, Roberto; Wombacher, Richard; Cavalcanti‐Adam, Elisabetta Ada

doi:10.1038/s41467-020-14390-1

Cited by 33 publications

(22 citation statements)

References 45 publications

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“…[ 11 ] To overcome general concerns related to the chemical modification of the cell membrane (e.g., degradation over time, off‐target cell toxicity), it is possible to regulate the expression and the activity of genetically encoded native cell–cell adhesion molecules such as cadherins [ 12 ] or artificial surface receptors. [ 1 d, 9 b, 6,12,13 ] These adhesions allow cells to not only just be brought together but in some cases also to transduce intracellular signals. [ 1 e, 12,14 ]…”

Section: Figurementioning

confidence: 99%

“…[ 1 d, 9 b, 6,12,13 ] These adhesions allow cells to not only just be brought together but in some cases also to transduce intracellular signals. [ 1 e, 12,14 ]…”

Section: Figurementioning

confidence: 99%

“…In this study, we employed the green light-responsive protein CarH as an adhesion molecule to mediate cell-cell adhesions. The cobalamin binding domain of CarH derived from Thermus thermophilus is a monomer in the absence of its cofactor, AdoB 12 , but forms a tetramer (a dimer of dimers) upon binding to AdoB 12 . Exposure to blue or green light causes a ligand exchange at the AdoB 12 center in CarH, leading to a global conformational change in the protein and the disassembly of the CarH tetramer.…”

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Spatiotemporal Control Over Multicellular Migration Using Green Light Reversible Cell–Cell Interactions

et al. 2021

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cell-cell adhesions leads to the progression of cancer [1c] and subsequent metastasis. [4] Additionally, the control of cell-cell interactions is of interest in the field of bottomup tissue-engineering, which aims to assemble cells as the basic unit into functional tissues. [5] Precise control in time and space over cell-cell interactions is required to successfully assemble appropriate multicellular architectures that resemble the in vivo structures and to control how cells work together within a tissue.In recent years, many tools have been developed to control the formation and the disassembly of cell-cell interactions in a controlled manner and thereby have given insight into the role of cell-cell adhesions. [6] For instance, chemical modifications of the plasma membrane with bioorthogonal reactive functional groups [7] and specific noncovalent interaction partners [8] including complementary DNA strands, [9] biotin-streptavidin, [10] and supramolecular binding partners [11] result in the formation of chemical bonds between neighboring cells. However, in only a few examples, it is possible to reverse these cell-cell interactions once formed. [11] To overcome general concerns related to the chemical modification of the cell membrane (e.g., degradation over time, off-target cell toxicity), it is possible to regulate the expression and the activity of genetically encoded native cell-cell adhesion molecules such as cadherins [12] or artificial surface receptors. [1d,9b,6,12,13] These adhesions allow cells to not only just be brought together but in some cases also to transduce intracellular signals. [1e,12,14] Photoregulation of cell-cell adhesions provides high spatiotemporal control, since light, as a stimulus, can be focused on the desired area and delivered at any given time. Using photocleavable nitrobenzyl [15] and switchable azobenzyl [14] chemical linkers, it has been shown possible to control cell-cell interactions with UV light. [11b,15,16] More recently, optogenetic tools for the regulation of cell-cell interactions with visible light have improved the biocompatibility, [13b,e] while also making it possible to dynamically and reversibly control cell-cell interactions between multiple cell types. [13b,e,16b,17] In these reports, photoswitchable proteins were expressed on the cell's plasma membrane as artificial adhesion molecules, which induced cell-cell interactions through the light-dependent dimerization of these proteins. [6] Depending on the photoswitchable proteins employed cell-cell adhesions between the same or differentThe regulation of cell-cell adhesions in space and time plays a crucial role in cell biology, especially in the coordination of multicellular behavior. Therefore, tools that allow for the modulation of cell-cell interactions with high precision are of great interest to a better understanding of their roles and building tissuelike structures. Herein, the green light-responsive protein CarH is expressed at the plasma membrane of cells as an artificial cell adhesion rece...

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Section: Figurementioning

confidence: 99%

“…[ 1 d, 9 b, 6,12,13 ] These adhesions allow cells to not only just be brought together but in some cases also to transduce intracellular signals. [ 1 e, 12,14 ]…”

Section: Figurementioning

confidence: 99%

mentioning

confidence: 99%

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Spatiotemporal Control Over Multicellular Migration Using Green Light Reversible Cell–Cell Interactions

et al. 2021

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“…Genetic modification like gene knockout ( Elosegui-Artola et al, 2016 ; Strohmeyer et al, 2017 ), protein expression modulation by siRNA ( Plotnikov et al, 2012 ; Bazellières et al, 2015 ) and the use of externally added inhibitors ( Bashoura et al, 2014 ; Collins et al, 2017 ) are important methods to investigate the role of different proteins in the cell sensing mechanism. Cell behavior as a consequence of these modifications is often monitored by optical microscopy-based techniques like immunofluorescence ( Engler et al, 2006 ), in vivo observation of recombinant fluorescence proteins ( Reffay et al, 2014 ; Oria et al, 2017 ), genetically incorporated molecular probes ( Grashoff et al, 2010 ), and more recently optochemical probes ( Endo et al, 2019 ; Ollech et al, 2020 ). Even though these methods have revealed important aspects of the molecular mechanisms of cellular mechanotransduction, they could not provide a complete description of the interaction between cells and their environment.…”

Section: Relevance Of Biosensors In Cell Adhesion Studiesmentioning

confidence: 99%

Biosensors for Studies on Adhesion-Mediated Cellular Responses to Their Microenvironment

Saffioti

Cavalcanti‐Adam

Pallarola

2020

Front. Bioeng. Biotechnol.

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Cells interact with their microenvironment by constantly sensing mechanical and chemical cues converting them into biochemical signals. These processes allow cells to respond and adapt to changes in their environment, and are crucial for most cellular functions. Understanding the mechanism underlying this complex interplay at the cell-matrix interface is of fundamental value to decipher key biochemical and mechanical factors regulating cell fate. The combination of material science and surface chemistry aided in the creation of controllable environments to study cell mechanosensing and mechanotransduction. Biologically inspired materials tailored with specific bioactive molecules, desired physical properties and tunable topography have emerged as suitable tools to study cell behavior. Among these materials, synthetic cell interfaces with built-in sensing capabilities are highly advantageous to measure biophysical and biochemical interaction between cells and their environment. In this review, we discuss the design of micro and nanostructured biomaterials engineered not only to mimic the structure, properties, and function of the cellular microenvironment, but also to obtain quantitative information on how cells sense and probe specific adhesive cues from the extracellular domain. This type of responsive biointerfaces provides a readout of mechanics, biochemistry, and electrical activity in real time allowing observation of cellular processes with molecular specificity. Specifically designed sensors based on advanced optical and electrochemical readout are discussed. We further provide an insight into the emerging role of multifunctional micro and nanosensors to control and monitor cell functions by means of material design.

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“…[10] Recently,a ne DHFR-caged trimethoprim system was reported as asuitable non-covalent photo-CID tool, [11] and various chemical biology methods have been studied actively using this system. [12][13][14][15][16][17][18][19][20] However,the majority of these photo-CID systems utilize non-covalent protein-labeling technologies to induce protein dimerization. Since covalent CID systems can maintain stable protein dimers regardless of ligand and protein concentrations,t he development of ac ovalent photo-CID system that functions in living cells has been in high demand.…”

Section: Introductionmentioning

confidence: 99%

Optical Manipulation of Subcellular Protein Translocation Using a Photoactivatable Covalent Labeling System

et al. 2021

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The photoactivatable chemically induced dimerization (photo-CID) technique for tag-fused proteins is one of the most promising methods for regulating subcellular protein translocations and protein-protein interactions.H owever, light-induced covalent protein dimerization in living cells has yet to be established, despite its various advantages.Herein, we developed ap hotoactivatable covalent protein-labeling technology by applying ac aged ligand to the BL-tag system, ac ovalent protein labeling system that uses mutant b-lactamase.Wefurther developed CBHD,acaged protein dimerizer, using caged BL-tag and HaloTag ligands,a nd achieved lightinduced protein translocation from the cytoplasm to subcellular regions.I na ddition, this covalent photo-CID system enabled quickp rotein translocation to al aser-illuminated microregion. These results indicate that the covalent photo-CID system will expand the scope of CID applications in the optical manipulation of cellular functions.

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An optochemical tool for light-induced dissociation of adherens junctions to control mechanical coupling between cells

Cited by 33 publications

References 45 publications

Spatiotemporal Control Over Multicellular Migration Using Green Light Reversible Cell–Cell Interactions

Spatiotemporal Control Over Multicellular Migration Using Green Light Reversible Cell–Cell Interactions

Biosensors for Studies on Adhesion-Mediated Cellular Responses to Their Microenvironment

Optical Manipulation of Subcellular Protein Translocation Using a Photoactivatable Covalent Labeling System

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