Two widely used RSK inhibitors, BI-D1870 and SL0101, alter mTORC1 signaling in a RSK-independent manner

Cell Signal. 2015 Aug;27(8):1630-42. doi: 10.1016/j.cellsig.2015.04.004. Epub 2015 Apr 16.

Abstract

The 90 kDa ribosomal S6 kinases (RSK) are effectors of the Ras-ERK1/2 signaling pathway. RSK signaling controls proliferation and protein synthesis, and is altered in several types of tumors. BI-D1870 and SL0101 are two widely used inhibitors of RSK. After revision of the literature, discrepancies in the effects of the inhibitors were identified. Herein we report that while SL0101 inhibited mTORC1-p70S6K signaling, BI-D1870 increased p70S6K activation. Both effects were independent of ERK1/2 and RSK, and thus nonspecific. We also demonstrated how these opposite nonspecific effects mislead the identification of the RSK-dependent phosphorylation of rpS6 (S235/236), a known RSK and p70S6K substrate. Phosphorylation of tuberin at S1798 by RSK was proposed to mediate ERK1/2-dependent activation of mTORC1-p70S6K signaling. In glioblastoma-derived cells, phosphorylation of tuberin was abolished after RSK depletion or ERK1/2 inhibition, suggesting that RSK is its main kinase. However, RSK depletion did not reduce PMA-dependent p70S6K phosphorylation, which suggests that tuberin phosphorylation at S1798 is not the main mediator of ERK1/2-dependent activation of mTORC1. Remarkably, tuberin phosphorylation (S1798) followed the activation status of RSK in different cells and experimental conditions, suggesting that phosphorylation of that residue could be used as readout for RSK activation in cells. We confirmed the difference in the effects of SL0101 and BI-D1870 in cellular proliferation assays. Rapamycin potentiated the inhibition of proliferation induced by BI-D1870, but not by SL0101. We thus conclude that SL0101 and BI-D1870 induce distinct off-target effects in mTORC1-p70S6K signaling, and thus, the functions previously ascribed to RSK based on these inhibitors should be reassessed.

Keywords: BI-D1870; Ribosomal protein S6 (rpS6); SL0101; Tuberin (TSC2); p70 ribosomal S6 kinase (p70S6K); p90 kDa ribosomal S6 kinase (RSK).

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Benzopyrans / pharmacology*
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Data Mining
  • Dose-Response Relationship, Drug
  • Glioblastoma / enzymology
  • Glioblastoma / genetics
  • Glioblastoma / pathology
  • HEK293 Cells
  • Humans
  • Mechanistic Target of Rapamycin Complex 1
  • Monosaccharides / pharmacology*
  • Multiprotein Complexes / antagonists & inhibitors*
  • Multiprotein Complexes / metabolism
  • Phosphorylation
  • Protein Kinase Inhibitors / pharmacology*
  • Pteridines / pharmacology*
  • RNA Interference
  • Ribosomal Protein S6 Kinases, 70-kDa / metabolism
  • Ribosomal Protein S6 Kinases, 90-kDa / antagonists & inhibitors*
  • Ribosomal Protein S6 Kinases, 90-kDa / genetics
  • Ribosomal Protein S6 Kinases, 90-kDa / metabolism
  • Signal Transduction / drug effects*
  • Substrate Specificity
  • TOR Serine-Threonine Kinases / antagonists & inhibitors*
  • TOR Serine-Threonine Kinases / metabolism
  • Time Factors
  • Transfection
  • Tuberous Sclerosis Complex 2 Protein
  • Tumor Suppressor Proteins

Substances

  • BI D1870
  • Benzopyrans
  • Monosaccharides
  • Multiprotein Complexes
  • Protein Kinase Inhibitors
  • Pteridines
  • SL0101
  • TSC2 protein, human
  • Tuberous Sclerosis Complex 2 Protein
  • Tumor Suppressor Proteins
  • Mechanistic Target of Rapamycin Complex 1
  • RPS6KA1 protein, human
  • Ribosomal Protein S6 Kinases, 70-kDa
  • Ribosomal Protein S6 Kinases, 90-kDa
  • TOR Serine-Threonine Kinases
  • ribosomal protein S6 kinase, 90kDa, polypeptide 3