Microinterfaces in biopolymer-based bicontinuous hydrogels guide rapid 3D cell migration

Karen L. Xu, Nikolas Caprio, Hooman Fallahi, Mohammad Dehghany, Matthew D. Davidson, Lorielle Laforest, Brian C. H. Cheung, Yuqi Zhang, Mingming Wu, Vivek Shenoy, Lin Han, Robert L. Mauck () and Jason A. Burdick ()
Additional contact information
Karen L. Xu: University of Pennsylvania
Nikolas Caprio: University of Pennsylvania
Hooman Fallahi: Drexel University
Mohammad Dehghany: University of Pennsylvania
Matthew D. Davidson: University of Pennsylvania
Lorielle Laforest: University of Pennsylvania
Brian C. H. Cheung: Cornell University
Yuqi Zhang: University of Pennsylvania
Mingming Wu: Cornell University
Vivek Shenoy: University of Pennsylvania
Lin Han: Drexel University
Robert L. Mauck: University of Pennsylvania
Jason A. Burdick: University of Pennsylvania

Nature Communications, 2024, vol. 15, issue 1, 1-17

Abstract: Abstract Cell migration is critical for tissue development and regeneration but requires extracellular environments that are conducive to motion. Cells may actively generate migratory routes in vivo by degrading or remodeling their environments or instead utilize existing extracellular matrix microstructures or microtracks as innate pathways for migration. While hydrogels in general are valuable tools for probing the extracellular regulators of 3-dimensional migration, few recapitulate these natural migration paths. Here, we develop a biopolymer-based bicontinuous hydrogel system that comprises a covalent hydrogel of enzymatically crosslinked gelatin and a physical hydrogel of guest and host moieties bonded to hyaluronic acid. Bicontinuous hydrogels form through controlled solution immiscibility, and their continuous subdomains and high micro-interfacial surface area enable rapid 3D migration, particularly when compared to homogeneous hydrogels. Migratory behavior is mesenchymal in nature and regulated by biochemical and biophysical signals from the hydrogel, which is shown across various cell types and physiologically relevant contexts (e.g., cell spheroids, ex vivo tissues, in vivo tissues). Our findings introduce a design that leverages important local interfaces to guide rapid cell migration.

Date: 2024
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DOI: 10.1038/s41467-024-46774-y

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