Cholinergic stimulation of lacrimal acinar cells promotes redistribution of membrane-associated kinesin and the secretory protein, beta-hexosaminidase, and increases kinesin motor activity

Exp Eye Res. 1997 Feb;64(2):141-56. doi: 10.1006/exer.1996.0198.

Abstract

The role of the microtubule-based motor, kinesin, in membrane trafficking has been investigated in resting and stimulated acinar cells from rabbit lacrimal gland, a cholinergically controlled secretory tissue. Microtubule-dependent motors from extracts of control and carbachol-treated acini were isolated by microtubule-affinity purification and their activity was determined using a video-enhanced differential interference contrast microscopy assay for microtubule gliding. The observation that carbachol treatment resulted in a 2.2-fold stimulation of the frequency of GTP-dependent microtubule gliding in fractions isolated by microtubule-affinity purification and GTP release suggested that kinesin was a target of carbachol-induced stimulation. Resolution of membranes from resting cells by fractionation on a sorbitol density gradient followed by partitioning analysis in a dextran-polyethyleneglycol two-phase system revealed that membrane-associated kinesin codistributed with Golgi-derived membranes, a post-Golgi secretory compartment designated Hex1, membranes from a trans Golgi network-like compartment, endoplasmic reticulum and a group of putative lysosomal membranes containing cathepsin B. Comparable fractionation of carbachol-treated acini showed that stimulation caused redistributions of membrane-associated kinesin, the secretory enzyme beta-hexosaminidase, and galactosyltransferase that appeared to reflect both a reorganization within the Golgi complex and a return of material to the Golgi complex from the secretory pathway. Our findings that carbachol promotes activation of lacrimal acinar kinesin as well as major shifts in kinesin-membrane association within the secretory pathway suggests that kinesin plays a major role in secretory vesicle assembly, apical secretion, and/or secretory vesicle membrane recycling in the lacrimal gland.

Publication types

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

MeSH terms

  • Animals
  • Carbachol / pharmacology
  • Cells, Cultured / drug effects
  • Cells, Cultured / ultrastructure
  • Chick Embryo
  • Female
  • Galactosyltransferases / drug effects
  • Intracellular Membranes / chemistry
  • Intracellular Membranes / ultrastructure
  • Kinesins / drug effects*
  • Kinesins / isolation & purification
  • Kinesins / physiology
  • Lacrimal Apparatus / chemistry
  • Lacrimal Apparatus / cytology
  • Lacrimal Apparatus / drug effects*
  • Microtubules / physiology
  • Miotics / pharmacology
  • Rabbits
  • Subcellular Fractions / chemistry
  • Subcellular Fractions / drug effects
  • Subcellular Fractions / ultrastructure
  • beta-N-Acetylhexosaminidases / drug effects*
  • beta-N-Acetylhexosaminidases / isolation & purification

Substances

  • Miotics
  • Carbachol
  • Galactosyltransferases
  • beta-N-Acetylhexosaminidases
  • Kinesins