C. elegans midbodies are released, phagocytosed and undergo LC3-dependent degradation independent of macroautophagy

J Cell Sci. 2016 Oct 15;129(20):3721-3731. doi: 10.1242/jcs.190223. Epub 2016 Aug 25.

Abstract

In animals, the midbody coordinates the end of cytokinesis when daughter cells separate through abscission. The midbody was thought to be sequestered by macroautophagy, but recent evidence suggests that midbodies are primarily released and phagocytosed. It was unknown, however, whether autophagy proteins play a role in midbody phagosome degradation. Using a protein degradation assay, we show that midbodies are released in Caenorhabditis elegans Released midbodies are known to be internalized by actin-driven phagocytosis, which we show requires the RAB-5 GTPase to localize the class III phosphoinositide 3-kinase (PI3K) complex at the cortex. Autophagy-associated proteins, including the Beclin 1 homolog BEC-1 and the Atg8/LC3-family members LGG-1 and LGG-2, localize around the midbody phagosome and are required for midbody degradation. In contrast, proteins required specifically for macroautophagy, such as UNC-51 and EPG-8 (homologous to ULK1/Atg1 and Atg14, respectively) are not required for midbody degradation. These data suggest that the C. elegans midbody is degraded by LC3-associated phagocytosis (LAP), not macroautophagy. Our findings reconcile the two prevailing models on the role of phagocytic and autophagy proteins, establishing a new non-canonical role for autophagy proteins in midbody degradation.

Keywords: Abscission; Cell division; Macroautophagy; Midbody; Phagocytosis.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Autophagy*
  • Caenorhabditis elegans / cytology*
  • Caenorhabditis elegans / embryology
  • Caenorhabditis elegans / genetics
  • Caenorhabditis elegans / metabolism*
  • Caenorhabditis elegans Proteins / metabolism*
  • Cell Membrane / metabolism
  • Embryo, Nonmammalian / cytology
  • Endocytosis
  • Genes, Helminth
  • Microtubule-Associated Proteins / metabolism*
  • Models, Biological
  • Phagocytosis*
  • Phosphatidylinositol 3-Kinases / metabolism

Substances

  • Caenorhabditis elegans Proteins
  • LGG-2 protein, C elegans
  • Microtubule-Associated Proteins
  • Phosphatidylinositol 3-Kinases