The Thr300Ala variant of ATG16L1 is associated with decreased risk of brain metastasis in patients with non-small cell lung cancer

Autophagy. 2017 Jun 3;13(6):1053-1063. doi: 10.1080/15548627.2017.1308997. Epub 2017 Apr 25.

Abstract

Non-small cell lung cancer (NSCLC) often metastasizes to the brain, but identifying which patients will develop brain metastases (BM) is difficult. Macroautophagy/autophagy is critical for cancer initiation and progression. We hypothesized that genetic variants of autophagy-related genes may affect brain metastases (BM) in NSCLC patients. We genotyped 16 single nucleotide polymorphisms (SNPs) in 7 autophagy-related (ATG) genes (ATG3, ATG5, ATG7, ATG10, ATG12, ATG16L1, and MAP1LC3/LC3) by using DNA from blood samples of 323 NSCLC patients. Further, we evaluated the potential associations of these genes with subsequent BM development. Lung cancer cell lines stably transfected with ATG16L1: rs2241880 (T300A) were established. Mouse models of brain metastasis were developed using cells transfected with ATG16L1-300T or ATG16L1-300A. ATG10: rs10036653 and ATG16L1: rs2241880 were significantly associated with a decreased risk of BM (respective hazard ratios [HRs]=0.596, 95% confidence interval [CI] 0.398-0.894, P = 0.012; and HR = 0. 655, 95% CI 0.438-0.978, P = 0.039, respectively). ATG12: rs26532 was significantly associated with an increased risk of BM (HR=1.644, 95% CI 1.049-2.576, P = 0.030). Invasion and migration assays indicated that transfection with ATG16L1-300T (vs. 300A) stimulated the migration of A549 cells. An in vivo metastasis assay revealed that transfection with ATG16L1-300T (vs. 300A) significantly increased brain metastasis. Our results indicate that genetic variations in autophagy-related genes can predict BM and that genome analysis would facilitate stratification of patients for BM prevention trials.

Keywords: ATG16L1; SNPs; autophagy; brain metastasis; non-small cell lung cancer; prevention.

MeSH terms

  • A549 Cells
  • Adult
  • Aged
  • Aged, 80 and over
  • Animals
  • Autophagy-Related Proteins / genetics*
  • Brain Neoplasms / secondary*
  • Carcinoma, Non-Small-Cell Lung / pathology*
  • Cell Movement / genetics
  • Female
  • Genetic Predisposition to Disease*
  • Humans
  • Kaplan-Meier Estimate
  • Lung Neoplasms / pathology*
  • Male
  • Mice, Nude
  • Middle Aged
  • Neoplasm Invasiveness
  • Polymorphism, Single Nucleotide / genetics*
  • Risk Factors

Substances

  • ATG16L1 protein, human
  • Autophagy-Related Proteins