Targeting a ribonucleoprotein complex containing the caprin-1 protein and the c-Myc mRNA suppresses tumor growth in mice: an identification of a novel oncotarget

Oncotarget. 2015 Feb 10;6(4):2148-63. doi: 10.18632/oncotarget.3236.

Abstract

Tylophorine compounds have been the focus of drug development for decades. Tylophorine derivatives exhibit anti-cancer activities but their cellular targets remain unknown. We used a biotinylated tylophorine derivative to probe for the interacting cellular target(s) of tylophorine. Tylophorine directly binds to caprin-1 and consequently enhances the recruitment of G3BP1, c-Myc mRNA, and cyclin D2 mRNA to form a ribonucleoprotein complex. Subsequently, this tylophorine targeted ribonucleoprotein complex is sequestered to the polysomal fractions and the protein expressions of the associated mRNA-transcripts are repressed. Caprin-1 depleted carcinoma cells become more resistant to tylophorine, associated with decreased formation of the ribonucleoprotein complex targeted by tylophorine. Consequently, tylophorine downregulates c-Myc and cyclins D1/D2, causing hypophosphorylation of Rb and suppression of both processing-body formation and the Warburg effect. Gene expression profiling and gain-of-c-Myc-function experiments also revealed that the downregulated c-Myc contributes to the anti-oncogenic effects of tylophorine compounds. Furthermore, the potent tylophorine derivative dibenzoquinoline-33b elicited a similar effect, as c-Myc protein levels were also decreased in xenograft tumors treated with dibenzoquinoline-33b. Thus, tylophorine compounds exert anti-cancer activity predominantly by targeting and sequestering the caprin-1 protein and c-Myc mRNA associated ribonucleoprotein complex.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alkaloids / chemistry
  • Alkaloids / metabolism
  • Alkaloids / pharmacology
  • Animals
  • Blotting, Western
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism
  • Cell Cycle Proteins / genetics
  • Cell Cycle Proteins / metabolism*
  • Cell Line
  • Cell Line, Tumor
  • Cyclin D2 / genetics
  • Cyclin D2 / metabolism
  • DNA Helicases
  • HEK293 Cells
  • HeLa Cells
  • Hep G2 Cells
  • Humans
  • Indolizines / chemistry
  • Indolizines / metabolism
  • Indolizines / pharmacology
  • MCF-7 Cells
  • Mice
  • Multiprotein Complexes / genetics
  • Multiprotein Complexes / metabolism
  • Neoplasms / drug therapy
  • Neoplasms / genetics
  • Neoplasms / metabolism*
  • Phenanthrenes / chemistry
  • Phenanthrenes / metabolism
  • Phenanthrenes / pharmacology
  • Poly-ADP-Ribose Binding Proteins
  • Protein Binding
  • Proto-Oncogene Proteins c-myb / genetics
  • Proto-Oncogene Proteins c-myb / metabolism*
  • RNA Helicases
  • RNA Interference
  • RNA Recognition Motif Proteins
  • RNA, Messenger / genetics*
  • RNA, Messenger / metabolism*
  • Reverse Transcriptase Polymerase Chain Reaction
  • Ribonucleoproteins / genetics
  • Ribonucleoproteins / metabolism
  • Tumor Burden / drug effects
  • Tumor Burden / genetics
  • U937 Cells
  • Xenograft Model Antitumor Assays

Substances

  • Alkaloids
  • CAPRIN1 protein, human
  • Carrier Proteins
  • Cell Cycle Proteins
  • Cyclin D2
  • Indolizines
  • Multiprotein Complexes
  • Phenanthrenes
  • Poly-ADP-Ribose Binding Proteins
  • Proto-Oncogene Proteins c-myb
  • RNA Recognition Motif Proteins
  • RNA, Messenger
  • Ribonucleoproteins
  • DNA Helicases
  • G3BP1 protein, human
  • RNA Helicases
  • tylophorine