FHIT loss confers cisplatin resistance in lung cancer via the AKT/NF-κB/Slug-mediated PUMA reduction

Oncogene. 2015 May 7;34(19):2505-15. doi: 10.1038/onc.2014.184. Epub 2014 Jul 7.

Abstract

Fragile histidine triad (FHIT) loss by the two-hit mechanism of loss of heterozygosity and promoter hypermethylation commonly occurrs in non-small cell lung cancer (NSCLC) and may confer cisplatin resistance in NSCLC cells. However, the underlying mechanisms of FHIT loss in cisplatin resistance and the response to cisplatin-based chemotherapy in NSCLC patients have not yet been reported. In the present study, inhibition concentration of 50% cell viability induced by cisplatin (IC50) and soft agar growth and invasion capability were increased and decreased in FHIT-knockdown and -overexpressing cells, respectively. Mechanistically, Slug transcription is upregulated by AKT/NF-κB activation due to FHIT loss and, in turn, Slug suppresses PUMA expression; this decrease of PUMA by FHIT loss is responsible for cisplatin resistance. In addition, cisplatin resistance due to FHIT loss can be conquered by AKT inhibitor-perifosine in xenograft tumors. Among NSCLC patients, low FHIT, high p-AKT, high Slug and low PUMA were correlated with shorter overall survival, relapse-free survival and poorer response to cisplatin-based chemotherapy. Therefore, the AKT inhibitor perifosine might potentially overcome the resistance to cisplatin-based chemotherapy in NSCLC patients with low-FHIT tumors, and consequently improve the outcome.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acid Anhydride Hydrolases / genetics*
  • Adult
  • Aged
  • Aged, 80 and over
  • Animals
  • Antineoplastic Agents / therapeutic use
  • Apoptosis / genetics
  • Apoptosis Regulatory Proteins / genetics
  • Apoptosis Regulatory Proteins / metabolism
  • Carcinoma, Non-Small-Cell Lung / drug therapy
  • Carcinoma, Non-Small-Cell Lung / genetics
  • Carcinoma, Non-Small-Cell Lung / mortality
  • Cisplatin / therapeutic use
  • Drug Resistance, Neoplasm / genetics*
  • Female
  • Humans
  • Lung Neoplasms / drug therapy
  • Lung Neoplasms / genetics
  • Lung Neoplasms / mortality
  • Male
  • Mice
  • Mice, Inbred BALB C
  • Mice, Nude
  • Middle Aged
  • Neoplasm Proteins / genetics*
  • Neoplasm Transplantation
  • Nitriles / pharmacology
  • Phosphorylcholine / analogs & derivatives
  • Phosphorylcholine / pharmacology
  • Proto-Oncogene Proteins / genetics
  • Proto-Oncogene Proteins / metabolism
  • Proto-Oncogene Proteins c-akt / antagonists & inhibitors
  • Proto-Oncogene Proteins c-akt / metabolism*
  • RNA Interference
  • RNA, Small Interfering
  • Snail Family Transcription Factors
  • Sulfones / pharmacology
  • Transcription Factor RelA / antagonists & inhibitors
  • Transcription Factor RelA / metabolism*
  • Transcription Factors / genetics
  • Transcription Factors / metabolism*
  • Transplantation, Heterologous
  • Treatment Outcome

Substances

  • 3-(4-methylphenylsulfonyl)-2-propenenitrile
  • Antineoplastic Agents
  • Apoptosis Regulatory Proteins
  • BBC3 protein, human
  • Neoplasm Proteins
  • Nitriles
  • Proto-Oncogene Proteins
  • RNA, Small Interfering
  • SNAI1 protein, human
  • Snai2 protein, mouse
  • Snail Family Transcription Factors
  • Sulfones
  • Transcription Factor RelA
  • Transcription Factors
  • fragile histidine triad protein
  • Phosphorylcholine
  • perifosine
  • Proto-Oncogene Proteins c-akt
  • Acid Anhydride Hydrolases
  • Cisplatin