Nanotopography modulates intracellular excitable systems through cytoskeleton actuation

Cellular sensing of most environmental cues involves receptors that affect a signal-transduction excitable network (STEN), which is coupled to a cytoskeletal excitable network (CEN). We show that the mechanism of sensing of nanoridges is fundamentally different. CEN activity occurs preferentially on...

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Bibliographic Details
Published in:Proceedings of the National Academy of Sciences - PNAS 2023-05, Vol.120 (19), p.e2218906120-e2218906120
Main Authors: Yang, Qixin, Miao, Yuchuan, Banerjee, Parijat, Hourwitz, Matt J, Hu, Minxi, Qing, Quan, Iglesias, Pablo A, Fourkas, John T, Losert, Wolfgang, Devreotes, Peter N
Format: Article
Language:English
Subjects:
Actin
Actin Cytoskeleton
Actins
Actuation
Biological Sciences
Cell Movement
Cytoskeleton
Feedback loops
Microenvironments
Microtubules
Signal transduction
Wave propagation
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Summary:Cellular sensing of most environmental cues involves receptors that affect a signal-transduction excitable network (STEN), which is coupled to a cytoskeletal excitable network (CEN). We show that the mechanism of sensing of nanoridges is fundamentally different. CEN activity occurs preferentially on nanoridges, whereas STEN activity is constrained between nanoridges. In the absence of STEN, waves disappear, but long-lasting F-actin puncta persist along the ridges. When CEN is suppressed, wave propagation is no longer constrained by nanoridges. A computational model reproduces these experimental observations. Our findings indicate that nanotopography is sensed directly by CEN, whereas STEN is only indirectly affected due to a CEN-STEN feedback loop. These results explain why texture sensing is robust and acts cooperatively with multiple other guidance cues in complex, in vivo microenvironments.
ISSN:0027-8424
1091-6490
DOI:10.1073/pnas.2218906120