Nuclear IGF-1R predicts chemotherapy and targeted therapy resistance in metastatic colorectal cancer

Br J Cancer. 2017 Dec 5;117(12):1777-1786. doi: 10.1038/bjc.2017.279. Epub 2017 Nov 9.

Abstract

Background: Although chemotherapy is the cornerstone treatment for patients with metastatic colorectal cancer (mCRC), acquired chemoresistance is common and constitutes the main reason for treatment failure. Monoclonal antibodies against insulin-like growth factor-1 receptor (IGF-1R) have been tested in pre-treated mCRC patients, but results have been largely deceiving.

Methods: We analysed time to progression, overall survival, and the mutational status of RAS, BRAF and nuclear p-IGF-1R expression by immunohistochemistry, in 470 metastatic CRC patients. The effect of IGF-1R activation and distribution was also assessed using cellular models of CRC and RNAi for functional validation.

Results: Nuclear IGF-1R increased in metastatic tumours compared to paired untreated primary tumours, and significantly correlated with poor overall survival in mCRC patients. In vitro, chemo-resistant cell lines presented significantly higher levels of IGF-1R expression within the nuclear compartment, and PIAS3, a protein implicated also in the sumoylation process of intranuclear proteins, contributed to IGF-1R nuclear sequestration, highlighting the essential role of PIAS3 in this process. Intriguingly, we observed that ganitumab, an IGF-1R blocking-antibody used in several clinical trials, and dasatinib, an SRC inhibitor, increased the nuclear localisation of IGF-1R.

Conclusions: Our study demonstrates that IGF-1R nuclear location might lead to chemotherapy and targeted agent resistance.

MeSH terms

  • Aged
  • Antibodies, Monoclonal / administration & dosage
  • Antibodies, Monoclonal / pharmacology
  • Antibodies, Monoclonal, Humanized
  • Antineoplastic Agents / pharmacology*
  • Antineoplastic Combined Chemotherapy Protocols / administration & dosage
  • Antineoplastic Combined Chemotherapy Protocols / therapeutic use*
  • Bevacizumab / administration & dosage
  • Camptothecin / administration & dosage
  • Camptothecin / analogs & derivatives
  • Cell Nucleus / metabolism*
  • Cell Survival / drug effects
  • Cetuximab / administration & dosage
  • Colorectal Neoplasms / drug therapy*
  • Colorectal Neoplasms / genetics
  • Colorectal Neoplasms / pathology
  • Curcumin / pharmacology
  • Dasatinib / pharmacology
  • Drug Resistance, Neoplasm*
  • Fatty Acids, Unsaturated / pharmacology
  • Female
  • Fluorouracil / administration & dosage
  • Fluorouracil / pharmacology
  • Gene Silencing
  • HCT116 Cells
  • HT29 Cells
  • Humans
  • Leucovorin / administration & dosage
  • Male
  • Middle Aged
  • Molecular Chaperones / genetics
  • Molecular Chaperones / metabolism
  • Molecular Targeted Therapy
  • Niacinamide / analogs & derivatives
  • Niacinamide / pharmacology
  • Organoplatinum Compounds / administration & dosage
  • Organoplatinum Compounds / pharmacology
  • Oxaliplatin
  • Panitumumab
  • Phenylurea Compounds / pharmacology
  • Protein Inhibitors of Activated STAT / genetics
  • Protein Inhibitors of Activated STAT / metabolism
  • Protein Transport / drug effects*
  • Proto-Oncogene Proteins B-raf / genetics
  • Proto-Oncogene Proteins p21(ras) / genetics
  • Pyrimidines / pharmacology
  • Pyrroles / pharmacology
  • Receptor, IGF Type 1 / metabolism*
  • Signal Transduction / drug effects
  • Sorafenib

Substances

  • Antibodies, Monoclonal
  • Antibodies, Monoclonal, Humanized
  • Antineoplastic Agents
  • Fatty Acids, Unsaturated
  • KRAS protein, human
  • Molecular Chaperones
  • NVP-AEW541
  • Organoplatinum Compounds
  • PIAS3 protein, human
  • Phenylurea Compounds
  • Protein Inhibitors of Activated STAT
  • Pyrimidines
  • Pyrroles
  • Oxaliplatin
  • Niacinamide
  • Bevacizumab
  • Panitumumab
  • Sorafenib
  • ganitumab
  • Receptor, IGF Type 1
  • BRAF protein, human
  • Proto-Oncogene Proteins B-raf
  • Proto-Oncogene Proteins p21(ras)
  • Curcumin
  • Cetuximab
  • Leucovorin
  • Dasatinib
  • Fluorouracil
  • Camptothecin
  • leptomycin B

Supplementary concepts

  • Folfox protocol
  • IFL protocol