Epigenetic inactivation of laminin-5-encoding genes in lung cancers

Clin Cancer Res. 2003 Jul;9(7):2665-72.

Abstract

Purpose: We investigated the loss of expression of three laminin-5 (LN5)-encoding genes in lung cancer cell lines and elucidated the mechanism of inactivation of the genes in lung cancer cell lines and tumors.

Experimental design: We examined the expression of LN5-encoding genes by reverse transcription-PCR in 49 lung cancer cell lines. To elucidate the mechanism of gene silencing, we treated expression-negative cell lines (two for each gene) with a demethylating agent and examined the restoration of expression by reverse transcription-PCR. We dissected out the methylation patterns of CpG sites unique to the promoter regions of LN5-encoding genes by bisulfite genomic sequencing of expression-negative cell lines. We designed methylation-specific primers and validated the methylation status of the promoter regions in lung cancer cell lines using methylation-specific PCR. We further studied the methylation patterns of primary non-small cell lung cancer [NSCLC (n = 36)], small cell lung cancer [SCLC (n = 26)], and carcinoids (n = 24) tumors.

Results: We observed frequent losses of expression in NSCLC (20-60%) and SCLC (65-86%) cell lines. Expression of one or more genes was lost in 90% of SCLC cell lines and 65% of NSCLC cell lines. Treatment of expression-negative cell lines with demethylating agent restored expression in all of the cases. Methylation of LN5-encoding genes was present more frequently in SCLC cell lines (60-80%) than in NSCLC cell lines (15-60%), and at least one gene was methylated in 95% of SCLC and 60% of NSCLC cell lines. The concordances between loss of expression and methylation in 40 lung cancer cell lines for the three genes (90-95%) were statistically significant. Methylation was more frequent in SCLC tumors (58-77%) than in NSCLC tumors (22-42%) and carcinoids (13-33%), and at least one gene was methylated in 92% of SCLC tumors, 47% of NSCLC tumors, and 33% of carcinoids.

Conclusions: Our results demonstrate frequent epigenetic inactivation of LN5-encoding genes in lung cancers, and these findings are of biological interest and are potentially of clinical importance.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Azacitidine / analogs & derivatives*
  • Azacitidine / pharmacology
  • Carcinoid Tumor / genetics
  • Carcinoma, Non-Small-Cell Lung / genetics
  • Carcinoma, Small Cell / genetics
  • Cell Adhesion Molecules / biosynthesis
  • Cell Adhesion Molecules / metabolism*
  • Cell Line, Tumor
  • CpG Islands
  • DNA / metabolism
  • DNA Methylation
  • Decitabine
  • Humans
  • Kalinin
  • Laminin / biosynthesis
  • Lung Neoplasms / genetics*
  • Lung Neoplasms / metabolism
  • Lymphocytes / metabolism
  • Methylation
  • Models, Genetic
  • Mouth Mucosa / metabolism
  • Promoter Regions, Genetic
  • Reverse Transcriptase Polymerase Chain Reaction
  • Sequence Analysis, DNA
  • Sulfites / metabolism
  • Transcription, Genetic
  • Tumor Cells, Cultured

Substances

  • Cell Adhesion Molecules
  • LAMC2 protein, human
  • Laminin
  • Sulfites
  • laminin alpha 3
  • Decitabine
  • DNA
  • Azacitidine