Synthesis, biological, and biophysical studies of DAG-indololactones designed as selective activators of RasGRP

Bioorg Med Chem. 2014 Jun 15;22(12):3123-40. doi: 10.1016/j.bmc.2014.04.024. Epub 2014 Apr 20.

Abstract

The development of selective agents capable of discriminating between protein kinase C (PKC) isoforms and other diacylglycerol (DAG)-responsive C1 domain-containing proteins represents an important challenge. Recent studies have highlighted the role that Ras guanine nucleotide-releasing protein (RasGRP) isoforms play both in immune responses as well as in the development of prostate cancer and melanoma, suggesting that the discovery of selective ligands could have potential therapeutic value. Thus far, the N-methyl-substituted indololactone 1 is the agonist with the highest reported potency and selectivity for RasGRP relative to PKC. Here we present the synthesis, binding studies, cellular assays and biophysical analysis of interactions with model membranes of a family of regioisomers of 1 (compounds 2-5) that differ in the position of the linkage between the indole ring and the lactone moiety. These structural variations were studied to explore the interaction of the active complex (C1 domain-ligand) with cellular membranes, which is believed to be an important factor for selectivity in the activation of DAG-responsive C1 domain containing signaling proteins. All compounds were potent and selective activators of RasGRP when compared to PKCα with selectivities ranging from 6 to 65 fold. However, the parent compound 1 was appreciably more selective than any of the other isomers. In intact cells, modest differences in the patterns of translocation of the C1 domain targets were observed. Biophysical studies using giant vesicles as model membranes did show substantial differences in terms of molecular interactions impacting lipid organization, dynamics and membrane insertion. However, these differences did not yield correspondingly large changes in patterns of biological response, at least for the parameters examined.

Keywords: C1 domain; Cancer; Indolo-lactones; RasGRP.

Publication types

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

MeSH terms

  • Animals
  • CHO Cells
  • Cell Membrane / metabolism
  • Cells, Cultured
  • Cricetulus
  • DNA-Binding Proteins / metabolism*
  • Diglycerides / chemistry
  • Diglycerides / pharmacology*
  • Fluorescence Polarization
  • Fluorescence Resonance Energy Transfer
  • Guanine Nucleotide Exchange Factors / metabolism*
  • HEK293 Cells
  • Humans
  • Indoles / chemistry
  • Indoles / pharmacology*
  • Lactones / chemistry
  • Lactones / pharmacology*
  • Male
  • Models, Molecular
  • Prostatic Neoplasms / drug therapy
  • Prostatic Neoplasms / metabolism
  • Prostatic Neoplasms / pathology*
  • Protein Isoforms
  • Protein Kinase C / metabolism*

Substances

  • 1,2-diacylglycerol
  • DNA-Binding Proteins
  • Diglycerides
  • Guanine Nucleotide Exchange Factors
  • Indoles
  • Lactones
  • Protein Isoforms
  • RASGRP1 protein, human
  • Protein Kinase C