Actin Waves and Dynamic Patterning of the Plasma Membrane

Yale J Biol Med. 2019 Sep 20;92(3):397-411. eCollection 2019 Sep.

Abstract

Plasma membrane and underlying actin network are connected to a functional unit that by non-linear interactions is capable of forming patterns. For instance, in cell motility and chemotaxis, cells polarize to form a protruding front and a retracting tail. Here we address dynamic patterns that are formed on a planar substrate surface and are therefore easily accessible to optical recording. In these patterns two distinct areas of the membrane and actin cortex are interconverted at the site of circular actin waves. The inner territory circumscribed by a wave is distinguished from the external area by a high PIP3 content and high Ras activity. In contrast, the external area is occupied with the PIP3-degrading phosphatase PTEN. In the underlying cortex, these areas differ in the proteins associated with the actin network. Actin waves can be formed at zones of increasing as well as decreasing Ras activity. Both types of waves are headed by myosin IB. When waves collide, they usually extinguish each other, and their decay is accompanied by the accumulation of coronin. No membrane patterns have been observed after efficient depolymerization of actin, suggesting that residual actin filaments are necessary for the pattern generating system to work. Where appropriate, we relate the experimental data obtained with Dictyostelium to human normal and malignant cell behavior, in particular to the role of Ras-GAP as an enhancer of macropinocytosis, to mutations in the tumor suppressor PTEN, to frustrated phagocytosis, and to the role of coronin in immune cells and neurons.

Keywords: Dictyostelium; PIP3; PTEN; Ras; coronin; myosin; phagocytosis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actins / metabolism*
  • Cell Membrane / metabolism*
  • Dictyostelium / metabolism*
  • Microfilament Proteins / metabolism
  • PTEN Phosphohydrolase / metabolism
  • Phosphatidylinositol Phosphates / metabolism
  • Protein Binding
  • ras Proteins / metabolism

Substances

  • Actins
  • Microfilament Proteins
  • Phosphatidylinositol Phosphates
  • phosphatidylinositol 3-phosphate
  • coronin proteins
  • PTEN Phosphohydrolase
  • ras Proteins