Interaction of the microtubule cytoskeleton with endocytic vesicles and cytoplasmic dynein in cultured rat hepatocytes

J Biol Chem. 1995 Jun 23;270(25):15242-9. doi: 10.1074/jbc.270.25.15242.

Abstract

In a recent study (Goltz, J.S., Wolkoff, A.W., Novikoff, P.M., Stockert, R.J., and Satir, P. (1992) Proc. Natl. Acad. Sci. U.S.A. 89, 7026-7030), we found that ligand- and receptor-containing endocytic vesicles bind to endogenous microtubules in vitro after 60 min of receptor-mediated endocytosis of asialo-orosomucoid. In the presence of ATP, ligand-containing endocytic vesicles are released from microtubules, while those containing receptor are not. We hypothesized that cytoplasmic dynein may associate with ligand-containing, but not receptor-containing, domains of endocytic vesicles and might be involved in the movement of ligand-containing vesicles along microtubules during sorting of ligand from receptor. Direct evidence in support of this hypothesis has been obtained in the present study. Binding of ligand-containing vesicles to microtubules correlates highly (p < 0.001) with binding of dynein, but not kinesin, under a variety of conditions. Binding of receptor-containing vesicles to microtubules is independent of both cytoplasmic dynein and kinesin binding. Tight association of cytoplasmic dynein with a population of ligand-containing vesicles is seen directly by immunoprecipitation. These results support the view that in receptor-mediated endocytosis, ligand-containing vesicles become bound to microtubules by cytoplasmic dynein. While receptor domains of endosomes remain attached to microtubules in an ATP-independent manner, ligand-containing domains might be moved away toward pericentrosomal lysosomes by this motor molecule.

Publication types

  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Adenosine Triphosphate / metabolism
  • Animals
  • Asialoglycoprotein Receptor
  • Asialoglycoproteins / metabolism
  • Cells, Cultured
  • Cytoplasm / metabolism
  • Cytoskeleton / metabolism
  • Cytoskeleton / ultrastructure*
  • Dyneins / metabolism*
  • Endocytosis*
  • Humans
  • Kinesins / metabolism
  • Kinetics
  • Ligands
  • Liver / metabolism*
  • Liver / ultrastructure*
  • Male
  • Microscopy, Confocal
  • Microtubules / metabolism
  • Microtubules / ultrastructure*
  • Orosomucoid / analogs & derivatives
  • Orosomucoid / metabolism
  • Rats
  • Rats, Sprague-Dawley
  • Receptors, Cell Surface / metabolism*
  • Ribonucleotides / pharmacology
  • Tubulin / metabolism

Substances

  • Asialoglycoprotein Receptor
  • Asialoglycoproteins
  • Ligands
  • Orosomucoid
  • Receptors, Cell Surface
  • Ribonucleotides
  • Tubulin
  • asialoorosomucoid
  • Adenosine Triphosphate
  • Dyneins
  • Kinesins