Microtubule-Mediated Inositol Lipid Signaling Plays Critical Roles in Regulation of Blebbing

PLoS One. 2015 Aug 28;10(8):e0137032. doi: 10.1371/journal.pone.0137032. eCollection 2015.

Abstract

Cells migrate by extending pseudopods such as lamellipodia and blebs. Although the signals leading to lamellipodia extension have been extensively investigated, those for bleb extension remain unclear. Here, we investigated signals for blebbing in Dictyostelium cells using a newly developed assay to induce blebbing. When cells were cut into two pieces with a microneedle, the anucleate fragments vigorously extended blebs. This assay enabled us to induce blebbing reproducibly, and analyses of knockout mutants and specific inhibitors identified candidate molecules that regulate blebbing. Blebs were also induced in anucleate fragments of leukocytes, indicating that this assay is generally applicable to animal cells. After cutting, microtubules in the anucleate fragments promptly depolymerized, followed by the extension of blebs. Furthermore, when intact cells were treated with a microtubule inhibitor, they frequently extended blebs. The depolymerization of microtubules induced the delocalization of inositol lipid phosphatidylinositol 3,4,5-trisphosphate from the cell membrane. PI3 kinase-null cells frequently extended blebs, whereas PTEN-null cells extended fewer blebs. From these observations, we propose a model in which microtubules play a critical role in bleb regulation via inositol lipid metabolism.

MeSH terms

  • Animals
  • Cell Membrane / chemistry
  • Cell Movement
  • Cell Polarity
  • Dictyostelium / genetics
  • Dictyostelium / physiology*
  • Leukocytes / physiology
  • Microtubules / physiology*
  • Models, Biological
  • PTEN Phosphohydrolase / genetics
  • PTEN Phosphohydrolase / metabolism
  • Phosphatidylinositol 3-Kinases / genetics
  • Phosphatidylinositol 3-Kinases / metabolism
  • Phosphatidylinositol Phosphates / metabolism*
  • Protozoan Proteins / genetics
  • Protozoan Proteins / metabolism
  • Pseudopodia / genetics
  • Pseudopodia / physiology*
  • Signal Transduction

Substances

  • Phosphatidylinositol Phosphates
  • Protozoan Proteins
  • phosphatidylinositol 3,4,5-triphosphate
  • Phosphatidylinositol 3-Kinases
  • PTEN Phosphohydrolase

Grants and funding

The authors have no support or funding to report.