A noninvasive fluorescence imaging-based platform measures 3D anisotropic extracellular diffusion

Peng Chen, Xun Chen, R. Glenn Hepfer, Brooke J. Damon, Changcheng Shi, Jenny J. Yao, Matthew C. Coombs, Michael J. Kern, Tong Ye () and Hai Yao ()
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Peng Chen: Clemson University
Xun Chen: Clemson University
R. Glenn Hepfer: Clemson University
Brooke J. Damon: Clemson University
Changcheng Shi: Clemson University
Jenny J. Yao: Harvard University
Matthew C. Coombs: Clemson University
Michael J. Kern: Medical University of South Carolina
Tong Ye: Clemson University
Hai Yao: Clemson University

Nature Communications, 2021, vol. 12, issue 1, 1-17

Abstract: Abstract Diffusion is a major molecular transport mechanism in biological systems. Quantifying direction-dependent (i.e., anisotropic) diffusion is vitally important to depicting how the three-dimensional (3D) tissue structure and composition affect the biochemical environment, and thus define tissue functions. However, a tool for noninvasively measuring the 3D anisotropic extracellular diffusion of biorelevant molecules is not yet available. Here, we present light-sheet imaging-based Fourier transform fluorescence recovery after photobleaching (LiFT-FRAP), which noninvasively determines 3D diffusion tensors of various biomolecules with diffusivities up to 51 µm2 s−1, reaching the physiological diffusivity range in most biological systems. Using cornea as an example, LiFT-FRAP reveals fundamental limitations of current invasive two-dimensional diffusion measurements, which have drawn controversial conclusions on extracellular diffusion in healthy and clinically treated tissues. Moreover, LiFT-FRAP demonstrates that tissue structural or compositional changes caused by diseases or scaffold fabrication yield direction-dependent diffusion changes. These results demonstrate LiFT-FRAP as a powerful platform technology for studying disease mechanisms, advancing clinical outcomes, and improving tissue engineering.

Date: 2021
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DOI: 10.1038/s41467-021-22221-0

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