TRP-ML1 regulates lysosomal pH and acidic lysosomal lipid hydrolytic activity

J Biol Chem. 2006 Mar 17;281(11):7294-301. doi: 10.1074/jbc.M508211200. Epub 2005 Dec 16.

Abstract

Mucolipidosis type IV (MLIV) is caused by mutations in the ion channel mucolipin 1 (TRP-ML1). MLIV is typified by accumulation of lipids and membranous materials in intracellular organelles, which was hypothesized to be caused by the altered membrane fusion and fission events. How mutations in TRP-ML1 lead to aberrant lipolysis is not known. Here we present evidence that MLIV is a metabolic disorder that is not associated with aberrant membrane fusion/fission events. Thus, measurement of lysosomal pH revealed that the lysosomes in TRP-ML1(-/-) cells obtained from the patients with MLIV are over-acidified. TRP-ML1 can function as a H(+) channel, and the increased lysosomal acidification in TRP-ML1(-/-) cells is likely caused by the loss of TRP-ML1-mediated H(+) leak. Measurement of lipase activity using several substrates revealed a marked reduction in lipid hydrolysis in TRP-ML1(-/-) cells, which was rescued by the expression of TRP-ML1. Cell fractionation indicated specific loss of acidic lipase activity in TRP-ML1(-/-) cells. Furthermore, dissipation of the acidic lysosomal pH of TRP-ML1(-/-) cells by nigericin or chloroquine reversed the lysosomal storage disease phenotype. These findings provide a new mechanism to account for the pathogenesis of MLIV.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acridine Orange / pharmacology
  • Calcium / chemistry
  • Calcium / metabolism
  • Calcium Signaling
  • Carboxylic Acids / pharmacology
  • Cell Line
  • Cell Membrane / metabolism
  • Chloroquine / chemistry
  • Chromatography, Thin Layer
  • Humans
  • Hydrogen-Ion Concentration
  • Hydrolases / chemistry
  • Hydrolysis
  • Ionophores / chemistry
  • Lipase / chemistry
  • Lipids / chemistry
  • Lysosomal Storage Diseases / metabolism
  • Lysosomes / chemistry
  • Lysosomes / metabolism*
  • Magnesium / chemistry
  • Membrane Fusion
  • Microscopy, Electron
  • Microscopy, Fluorescence
  • Models, Biological
  • Mutation
  • Phenotype
  • Protons
  • Sterol Esterase / chemistry*
  • Subcellular Fractions / metabolism
  • TRPM Cation Channels / chemistry*
  • TRPM Cation Channels / metabolism
  • Transient Receptor Potential Channels

Substances

  • Carboxylic Acids
  • Ionophores
  • Lipids
  • MCOLN1 protein, human
  • Oregon Green 488 carboxylic acid
  • Protons
  • TRPM Cation Channels
  • Transient Receptor Potential Channels
  • Chloroquine
  • Hydrolases
  • LIPA protein, human
  • Sterol Esterase
  • Lipase
  • Acridine Orange
  • Magnesium
  • Calcium