Wave patterns organize cellular protrusions and control cortical dynamics

Yuchuan Miao, Sayak Bhattacharya, Tatsat Banerjee, Bedri Abubaker-Sharif, Yu Long, Takanari Inoue, Pablo A Iglesias, Peter N Devreotes

Research output: Contribution to journalArticle

Abstract

Cellular protrusions are typically considered as distinct structures associated with specific regulators. However, we found that these regulators coordinately localize as propagating cortical waves, suggesting a common underlying mechanism. These molecular events fell into two excitable networks, the signal transduction network STEN and the cytoskeletal network CEN with different wave substructures. Computational studies using a coupled-network model reproduced these features and showed that the morphology and kinetics of the waves depended on strengths of feedback loops. Chemically induced dimerization at multiple nodes produced distinct, coordinated alterations in patterns of other network components. Taken together, these studies indicate: STEN positive feedback is mediated by mutual inhibition between Ras/Rap and PIP2, while negative feedback depends on delayed PKB activation; PKBs link STEN to CEN; CEN includes positive feedback between Rac and F-actin, and exerts fast positive and slow negative feedbacks to STEN. The alterations produced protrusions resembling filopodia, ruffles, pseudopodia, or lamellipodia, suggesting that these structures arise from a common regulatory mechanism and that the overall state of the STEN-CEN system determines cellular morphology.

Original languageEnglish (US)
Article numbere8585
JournalMolecular systems biology
Volume15
Issue number3
DOIs
StatePublished - Mar 1 2019

Fingerprint

Cell Surface Extensions
pseudopodia
Dynamic Control
Pseudopodia
Feedback
Positive Feedback
Negative Feedback
Regulator
dimerization
Distinct
strength (mechanics)
actin
Signal Transduction
signal transduction
Actin
Coupled Model
Feedback Loop
Substructure
Network components
Signal transduction

Keywords

  • cell migration
  • cellular protrusion
  • complex network
  • excitable system
  • pattern formation

ASJC Scopus subject areas

  • Biochemistry, Genetics and Molecular Biology(all)
  • Immunology and Microbiology(all)
  • Agricultural and Biological Sciences(all)
  • Applied Mathematics

Cite this

Wave patterns organize cellular protrusions and control cortical dynamics. / Miao, Yuchuan; Bhattacharya, Sayak; Banerjee, Tatsat; Abubaker-Sharif, Bedri; Long, Yu; Inoue, Takanari; Iglesias, Pablo A; Devreotes, Peter N.

In: Molecular systems biology, Vol. 15, No. 3, e8585, 01.03.2019.

Research output: Contribution to journalArticle

Miao Y, Bhattacharya S, Banerjee T, Abubaker-Sharif B, Long Y, Inoue T et al. Wave patterns organize cellular protrusions and control cortical dynamics. Molecular systems biology. 2019 Mar 1;15(3). e8585. https://doi.org/10.15252/msb.20188585
Miao, Yuchuan ; Bhattacharya, Sayak ; Banerjee, Tatsat ; Abubaker-Sharif, Bedri ; Long, Yu ; Inoue, Takanari ; Iglesias, Pablo A ; Devreotes, Peter N. / Wave patterns organize cellular protrusions and control cortical dynamics. In: Molecular systems biology. 2019 ; Vol. 15, No. 3.
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