Bidirectional signaling between TM4SF5 and IGF1R promotes resistance to EGFR kinase inhibitors

Lung Cancer. 2015 Oct;90(1):22-31. doi: 10.1016/j.lungcan.2015.06.023. Epub 2015 Jul 2.

Abstract

Objectives: The membrane glycoprotein TM4SF5 (transmembrane 4 L6 family member 5), which is similar to the tetraspanins, is highly expressed in different cancers and causes epithelial-mesenchymal transition (EMT). TM4SF5 interacts with other membrane proteins during its pro-tumorigenic roles, presumably at tetraspanin-enriched microdomains (TEMs/TERMs). Here, we explored TM4SF5-mediated resistance against the clinically important EGFR kinase inhibitors, with regards to cooperation with other membrane proteins, particularly the insulin-like growth factor 1 receptor (IGF1R).

Materials and methods: Using cancer cells including NSCLC with TM4SF5 overexpression or IGF1R suppression in either normal 2 dimensional (2D), 3D aqueous spheroids, or 3D collagen I gels systems, the sensitivity to tyrosine kinase inhibitors (TKIs) were evaluated.

Results and conclusion: We found that TM4SF5 and IGF1R transcriptionally modulated one another, with each protein promoting the expressions of the other. Expression of TM4SF5 in gefitinib-sensitive HCC827 cells caused resistance to erlotinib and gefitinib, but not to sorafenib [a platelet derived growth factor receptor (PDGFR) inhibitor]; whereas suppression of IGF1R from gefitinib-resistant NCI-H1299 cells caused enhanced sensitization to the inhibitors. Expression of TM4SF5 and IGF1R in the drug-sensitive cells promoted signaling activities of extracellular signal-regulated kinases (ERKs), protein kinase B (Akt), and S6 kinase (S6K), and resulted in a higher residual EGFR activity, even after EGFR kinase inhibitor treatment. Complex formation between TM4SF5 and IGF1R was observed, and also included EGFR, dependent on TM4SF5 expression. The TM4SF5-mediated drug resistance was further confirmed in an aqueous 3D spheroid system or upon being embedded in 3D extracellular matrix (ECM)-surrounded gel systems. Collectively, these data suggest that anti-TM4SF5 reagents may be combined with the EGFR kinase inhibitors to enhance the efficacy of chemotherapies against NSCLC.

Keywords: Epithelial–mesenchymal transition; Gefitinib resistance; IGF1R; Non-small-cell lung carcinoma; TM4SF5.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Antineoplastic Agents / pharmacology
  • Carcinoma, Non-Small-Cell Lung / drug therapy*
  • Carcinoma, Non-Small-Cell Lung / metabolism
  • Cell Line, Tumor
  • Drug Resistance, Neoplasm
  • Epithelial-Mesenchymal Transition / drug effects
  • ErbB Receptors / antagonists & inhibitors
  • ErbB Receptors / metabolism
  • Erlotinib Hydrochloride / pharmacology*
  • Gefitinib
  • Humans
  • Lung Neoplasms / drug therapy*
  • Lung Neoplasms / metabolism
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism*
  • Protein Kinase Inhibitors / pharmacology*
  • Quinazolines / pharmacology*
  • Receptor, IGF Type 1
  • Receptors, Somatomedin / biosynthesis
  • Receptors, Somatomedin / genetics
  • Receptors, Somatomedin / metabolism*
  • Signal Transduction
  • Spheroids, Cellular

Substances

  • Antineoplastic Agents
  • IGF1R protein, human
  • Membrane Proteins
  • Protein Kinase Inhibitors
  • Quinazolines
  • Receptors, Somatomedin
  • TM4SF5 protein, human
  • Erlotinib Hydrochloride
  • EGFR protein, human
  • ErbB Receptors
  • Receptor, IGF Type 1
  • Gefitinib