The PI3K/Akt and mTOR/P70S6K signaling pathways in human uveal melanoma cells: interaction with B-Raf/ERK

Invest Ophthalmol Vis Sci. 2010 Jan;51(1):421-9. doi: 10.1167/iovs.09-3974. Epub 2009 Aug 6.

Abstract

Purpose: Activated B-Raf alone cannot induce melanoma but must cooperate with other signaling pathways. The phosphatidylinositol 3-kinase (PI3K)/Akt and mammalian target of rapamycin (mTOR)/p70S6K pathways are critical for tumorigenesis. The authors investigated the role of these pathways in uveal melanoma cells.

Methods: The effects of PI3K and mTOR activation and inhibition on the proliferation of human uveal melanoma cell lines expressing either activated (WT)B-Raf or (V600E)B-Raf were investigated. Interactions among PI3K, mTOR, and B-Raf/ERK were studied.

Results: Inhibition of PI3K deactivated P70S6 kinase, reduced cell proliferation by 71% to 84%, and increased apoptosis by a factor of 5.0 to 8.4 without reducing ERK1/2 activation, indicating that ERK plays no role in mediating PI3K in these processes. In contrast, rapamycin-induced inhibition of mTOR did not significantly affect cell proliferation because it simultaneously stimulated PI3K/Akt activation and cyclin D1 expression. Regardless of B-Raf mutation status, cotreatment with the PI3K inhibitor effectively sensitized all melanoma cell lines to the B-Raf or ERK1/2 inhibition-induced reduction of cell proliferation. B-Raf/ERK and PI3K signaling, but not mTOR signaling, converged to control cyclin D1 expression. Moreover, p70S6K required the activation of ERK1/2. These data demonstrate that PI3K/Akt and mTOR/P70S6K interact with B-Raf/ERK.

Conclusions: Activated PI3K/Akt attenuates the inhibitory effects of rapamycin on cell proliferation and thus serves as a negative feedback mechanism. This finding suggests that rapamycin is unlikely to inhibit uveal melanoma growth. In contrast, targeting PI3K while inhibiting B-Raf/ERK may be a promising approach to reduce the proliferation of uveal melanoma cells.

MeSH terms

  • Apoptosis
  • Blotting, Western
  • Cell Cycle / physiology
  • Cell Proliferation
  • Dose-Response Relationship, Drug
  • Enzyme Activation / drug effects
  • Enzyme Inhibitors / pharmacology
  • Extracellular Signal-Regulated MAP Kinases / metabolism*
  • Feedback, Physiological
  • Humans
  • Intracellular Signaling Peptides and Proteins / physiology*
  • Melanoma / metabolism*
  • Melanoma / pathology
  • Phosphatidylinositol 3-Kinases / physiology*
  • Phosphoinositide-3 Kinase Inhibitors
  • Phosphorylation
  • Protein Serine-Threonine Kinases / physiology*
  • Proto-Oncogene Proteins B-raf / metabolism*
  • Proto-Oncogene Proteins c-akt / metabolism*
  • Ribosomal Protein S6 Kinases, 70-kDa / metabolism*
  • Signal Transduction / physiology*
  • Sirolimus / pharmacology
  • TOR Serine-Threonine Kinases
  • Tumor Cells, Cultured
  • Uveal Neoplasms / metabolism*
  • Uveal Neoplasms / pathology

Substances

  • Enzyme Inhibitors
  • Intracellular Signaling Peptides and Proteins
  • Phosphoinositide-3 Kinase Inhibitors
  • MTOR protein, human
  • Protein Serine-Threonine Kinases
  • Proto-Oncogene Proteins B-raf
  • Proto-Oncogene Proteins c-akt
  • Ribosomal Protein S6 Kinases, 70-kDa
  • TOR Serine-Threonine Kinases
  • Extracellular Signal-Regulated MAP Kinases
  • Sirolimus