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      Shining Light in Mechanobiology: Optical Tweezers, Scissors, and Beyond

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          Abstract

          Mechanobiology helps us to decipher cell and tissue functions by looking at changes in their mechanical properties that contribute to development, cell differentiation, physiology, and disease. Mechanobiology sits at the interface of biology, physics and engineering. One of the key technologies that enables characterization of properties of cells and tissue is microscopy. Combining microscopy with other quantitative measurement techniques such as optical tweezers and scissors, gives a very powerful tool for unraveling the intricacies of mechanobiology enabling measurement of forces, torques and displacements at play. We review the field of some light based studies of mechanobiology and optical detection of signal transduction ranging from optical micromanipulation—optical tweezers and scissors, advanced fluorescence techniques and optogenentics. In the current perspective paper, we concentrate our efforts on elucidating interesting measurements of forces, torques, positions, viscoelastic properties, and optogenetics inside and outside a cell attained when using structured light in combination with optical tweezers and scissors. We give perspective on the field concentrating on the use of structured light in imaging in combination with tweezers and scissors pointing out how novel developments in quantum imaging in combination with tweezers and scissors can bring to this fast growing field.

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          Most cited references254

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          Observation of a single-beam gradient force optical trap for dielectric particles

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            Effects of extracellular matrix viscoelasticity on cellular behaviour

            Significant research over the past two decades has established that extracellular matrix (ECM) elasticity, or stiffness, impacts fundamental cell processes including spreading, growth, proliferation, migration, differentiation, and organoid formation. Linearly elastic polyacrylamide hydrogels and polydimethylsiloxane (PDMS) elastomers coated with ECM proteins have become widely-used tools for assessing the role of stiffness, and results from these experiments are often assumed to reproduce the effect of the mechanical environment experienced by cells in vivo . However, tissues and ECMs are not linearly elastic materials – they in fact exhibit far more complex mechanical behaviors, including viscoelasticity, or a time-dependent response to loading or deformation, as well as mechanical plasticity and nonlinear elasticity. Recent work has revealed that matrix viscoelasticity regulates these same fundamental cell processes, and importantly can promote behaviors not observed with elastic hydrogels in both 2D and 3D culture microenvironments. These important findings have provided new insights into cell-matrix interactions and have given context as to how these interactions differentially modulate mechano-sensitive molecular pathways in cells. Moreover, these results indicate new design guidelines for the next generation of biomaterials that better match tissue and ECM mechanics for in vitro tissue models and applications in regenerative medicine.
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              Nuclear lamin-A scales with tissue stiffness and enhances matrix-directed differentiation.

              Tissues can be soft like fat, which bears little stress, or stiff like bone, which sustains high stress, but whether there is a systematic relationship between tissue mechanics and differentiation is unknown. Here, proteomics analyses revealed that levels of the nucleoskeletal protein lamin-A scaled with tissue elasticity, E, as did levels of collagens in the extracellular matrix that determine E. Stem cell differentiation into fat on soft matrix was enhanced by low lamin-A levels, whereas differentiation into bone on stiff matrix was enhanced by high lamin-A levels. Matrix stiffness directly influenced lamin-A protein levels, and, although lamin-A transcription was regulated by the vitamin A/retinoic acid (RA) pathway with broad roles in development, nuclear entry of RA receptors was modulated by lamin-A protein. Tissue stiffness and stress thus increase lamin-A levels, which stabilize the nucleus while also contributing to lineage determination.
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                Author and article information

                Journal
                ACS Photonics
                ACS Photonics
                ph
                apchd5
                ACS Photonics
                American Chemical Society
                2330-4022
                11 March 2024
                20 March 2024
                : 11
                : 3
                : 917-940
                Affiliations
                [# ]School of Mathematics and Physics, The University of Queensland , Brisbane, 4074, Australia
                []ARC CoE for Engineered Quantum Systems, The University of Queensland , Brisbane, 4074, Australia
                []ARC CoE in Quantum Biotechnology, The University of Queensland , 4074, Brisbane, Australia
                [§ ]Queensland Brain Institute, The University of Queensland , Brisbane, 4074, Australia
                []Institute of Engineering and Medicine, University of California San Diego , San Diego, California 92093, United States
                []Beckman Laser Institute, University of California Irvine , Irvine, California 92612, United States
                Author notes
                Author information
                https://orcid.org/0000-0002-9299-5695
                https://orcid.org/0000-0003-4259-724X
                https://orcid.org/0000-0002-8332-2309
                Article
                10.1021/acsphotonics.4c00064
                10958612
                38523746
                04372610-0584-4981-8f4a-844602a1282b
                © 2024 The Authors. Published by American Chemical Society

                Permits non-commercial access and re-use, provided that author attribution and integrity are maintained; but does not permit creation of adaptations or other derivative works ( https://creativecommons.org/licenses/by-nc-nd/4.0/).

                History
                : 11 January 2024
                : 23 February 2024
                : 22 February 2024
                Funding
                Funded by: Air Force Office of Scientific Research, doi 10.13039/100000181;
                Award ID: FA9550-17-1- 0193
                Funded by: National Health and Medical Research Council, doi 10.13039/501100000925;
                Award ID: 2012140
                Funded by: Australian Research Council, doi 10.13039/501100000923;
                Award ID: DP220103812
                Funded by: Australian Research Council, doi 10.13039/501100000923;
                Award ID: DP180101002
                Funded by: Australian Research Council, doi 10.13039/501100000923;
                Award ID: DE230100972
                Funded by: Australian Research Council, doi 10.13039/501100000923;
                Award ID: CE230100021
                Funded by: Australian Research Council, doi 10.13039/501100000923;
                Award ID: CE170100009
                Funded by: Australian Government, doi 10.13039/100015539;
                Award ID: NA
                Funded by: Beckman Laser Institute and Medical Clinic, doi 10.13039/100001490;
                Award ID: NA
                Categories
                Perspective
                Custom metadata
                ph4c00064
                ph4c00064

                mechanobiology,optical tweezers,laser scissors,quantum light,cell biology

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