Gamma-secretase activity of presenilin 1 regulates acetylcholine muscarinic receptor-mediated signal transduction

J Biol Chem. 2004 Feb 20;279(8):6455-64. doi: 10.1074/jbc.M306041200. Epub 2003 Nov 18.

Abstract

Familial Alzheimer's disease (FAD) presenilin 1 (PS1) mutations give enhanced calcium responses upon different stimuli, attenuated capacitative calcium entry, an increased sensitivity of cells to undergo apoptosis, and increased gamma-secretase activity. We previously showed that the FAD mutation causing an exon 9 deletion in PS1 results in enhanced basal phospholipase C (PLC) activity (Cedazo-Minguez, A., Popescu, B. O., Ankarcrona, M., Nishimura, T., and Cowburn, R. F. (2002) J. Biol. Chem. 277, 36646-36655). To further elucidate the mechanisms by which PS1 interferes with PLC-calcium signaling, we studied the effect of two other FAD PS1 mutants (M146V and L250S) and two dominant negative PS1 mutants (D257A and D385N) on basal and carbachol-stimulated phosphoinositide (PI) hydrolysis and intracellular calcium concentrations ([Ca2+]i) in SH-SY5Y neuroblastoma cells. We found a significant increase in basal PI hydrolysis in PS1 M146V cells but not in PS1 L250S cells. Both PS1 M146V and PS1 L250S cells showed a significant increase in carbachol-induced [Ca2+]i as compared with nontransfected or wild type PS1 transfected cells. The elevated carbachol-induced [Ca2+]i signals were reversed by the PLC inhibitor neomycin, the ryanodine receptor antagonist dantrolene, the general aspartyl protease inhibitor pepstatin A, and the specific gamma-secretase inhibitor N-[N-(3,5-difluorophenacetyl)-L-alanyl]-S-phenylglycine t-butyl ester. The cells expressing either PS1 D257A or PS1 D385N had attenuated carbachol-stimulated PI hydrolysis and [Ca2+]i responses. In nontransfected or PS1 wild type transfected cells, N-[N-(3,5-difluorophenacetyl)-L-alanyl]-S-phenylglycine t-butyl ester and pepstatin A also attenuated both carbachol-stimulated PI hydrolysis and [Ca2+]i responses to levels found in PS1 D257A or PS1 D385N dominant negative cells. Our findings suggest that PS1 can regulate PLC activity and that this function is gamma-secretase activity-dependent.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amyloid Precursor Protein Secretases
  • Aspartic Acid Endopeptidases
  • Calcium / metabolism
  • Carbachol / chemistry
  • Carbachol / metabolism
  • Cell Line
  • Cell Line, Tumor
  • DNA, Complementary / metabolism
  • Dantrolene / pharmacology
  • Endopeptidases / metabolism*
  • Exons
  • Gene Deletion
  • Gene Expression Regulation*
  • Humans
  • Hydrolysis
  • Immunoblotting
  • Membrane Proteins / metabolism
  • Membrane Proteins / physiology*
  • Muscle Relaxants, Central / pharmacology
  • Mutation
  • Neomycin / pharmacology
  • Presenilin-1
  • Receptors, Muscarinic / metabolism*
  • Signal Transduction*
  • Time Factors
  • Transfection
  • Type C Phospholipases / metabolism

Substances

  • DNA, Complementary
  • Membrane Proteins
  • Muscle Relaxants, Central
  • PSEN1 protein, human
  • Presenilin-1
  • Receptors, Muscarinic
  • Carbachol
  • Type C Phospholipases
  • Amyloid Precursor Protein Secretases
  • Endopeptidases
  • Aspartic Acid Endopeptidases
  • BACE1 protein, human
  • Dantrolene
  • Neomycin
  • Calcium