Integrated quantitative analysis of the phosphoproteome and transcriptome in tamoxifen-resistant breast cancer

J Biol Chem. 2011 Jan 7;286(1):818-29. doi: 10.1074/jbc.M110.156877. Epub 2010 Nov 2.

Abstract

Quantitative phosphoproteome and transcriptome analysis of ligand-stimulated MCF-7 human breast cancer cells was performed to understand the mechanisms of tamoxifen resistance at a system level. Phosphoproteome data revealed that WT cells were more enriched with phospho-proteins than tamoxifen-resistant cells after stimulation with ligands. Surprisingly, decreased phosphorylation after ligand perturbation was more common than increased phosphorylation. In particular, 17β-estradiol induced down-regulation in WT cells at a very high rate. 17β-Estradiol and the ErbB ligand heregulin induced almost equal numbers of up-regulated phospho-proteins in WT cells. Pathway and motif activity analyses using transcriptome data additionally suggested that deregulated activation of GSK3β (glycogen-synthase kinase 3β) and MAPK1/3 signaling might be associated with altered activation of cAMP-responsive element-binding protein and AP-1 transcription factors in tamoxifen-resistant cells, and this hypothesis was validated by reporter assays. An examination of clinical samples revealed that inhibitory phosphorylation of GSK3β at serine 9 was significantly lower in tamoxifen-treated breast cancer patients that eventually had relapses, implying that activation of GSK3β may be associated with the tamoxifen-resistant phenotype. Thus, the combined phosphoproteome and transcriptome data set analyses revealed distinct signal transcription programs in tumor cells and provided a novel molecular target to understand tamoxifen resistance.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Breast Neoplasms / genetics*
  • Breast Neoplasms / immunology
  • Breast Neoplasms / metabolism*
  • Breast Neoplasms / pathology
  • Cell Line, Tumor
  • Cyclic AMP Response Element-Binding Protein / metabolism
  • Drug Resistance, Neoplasm / drug effects
  • Drug Resistance, Neoplasm / genetics*
  • Gene Expression Profiling / methods*
  • Glycogen Synthase Kinase 3 / metabolism
  • Glycogen Synthase Kinase 3 beta
  • Humans
  • Ligands
  • Mitogen-Activated Protein Kinases / metabolism
  • Phosphoproteins / genetics
  • Phosphoproteins / metabolism*
  • Proteome / genetics
  • Proteome / metabolism*
  • Signal Transduction / drug effects
  • Tamoxifen / pharmacology*
  • Transcription Factor AP-1 / metabolism
  • Transcription, Genetic
  • Treatment Outcome

Substances

  • Cyclic AMP Response Element-Binding Protein
  • Ligands
  • Phosphoproteins
  • Proteome
  • Transcription Factor AP-1
  • Tamoxifen
  • GSK3B protein, human
  • Glycogen Synthase Kinase 3 beta
  • Mitogen-Activated Protein Kinases
  • Glycogen Synthase Kinase 3