Organ-specific profiles of genetic changes in cancers caused by activation-induced cytidine deaminase expression

Int J Cancer. 2008 Dec 15;123(12):2735-40. doi: 10.1002/ijc.23853.

Abstract

Various molecular changes characterizing organ-specific carcinogenesis have been identified in human tumors; however, the molecular mechanisms of the genomic changes specific for each cancer are not well defined. A transgenic (Tg) mouse model with constitutive expression of the nucleotide-editing enzyme, activation-induced cytidine deaminase (AID), develops tumors in various organs as a result of the mutagenic activities of AID. This phenotypic character of AID Tg mice allowed us to analyze the organ-specific genetic changes in tumor-related genes commonly triggered by AID-mediated mutagenesis. Among the 80 AID Tg mice analyzed, 11 mice developed hepatocellular carcinomas, and 7 developed lung cancers. In addition, 1 developed the gastric cancer and 3 developed gastric adenomas. Organ-specific preferences for nucleotide changes were observed in some of the tumor-related genes in each epithelial tissue of the AID Tg mice. Of note, the c-myc and K-ras genes were the preferential targets of the mutagenic activity of AID in lung and stomach cancers, respectively, whereas mutations in the p53 and beta-catenin genes were commonly observed in all 3 organs. Quantitative RT-PCR analyses revealed that alpha-fetoprotein, insulin-like growth factor-2 and cyclin D1 genes were specifically upregulated in HCC, whereas upregulation of the matrix metalloproteinase-7 gene was more marked in lung cancer. Our findings suggest that AID, a DNA mutator that plays a critical role linking inflammation to human cancers, might be involved in the generation of organ-specific genetic diversity in oncogenic pathways during cancer development.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cyclin D1 / genetics
  • Cyclin D1 / metabolism
  • Cytidine Deaminase / genetics*
  • Cytidine Deaminase / metabolism*
  • Enzyme Activation
  • Gene Expression Regulation, Enzymologic
  • Gene Expression Regulation, Neoplastic
  • Genes, myc
  • Genes, ras
  • Insulin-Like Growth Factor II / genetics
  • Insulin-Like Growth Factor II / metabolism
  • Liver Neoplasms, Experimental / enzymology
  • Liver Neoplasms, Experimental / genetics
  • Lung Neoplasms / enzymology
  • Lung Neoplasms / genetics
  • Matrix Metalloproteinase 7 / genetics
  • Matrix Metalloproteinase 7 / metabolism
  • Mice
  • Mice, Transgenic
  • Mutation*
  • Neoplasms, Experimental / enzymology*
  • Neoplasms, Experimental / genetics*
  • Organ Specificity*
  • Reverse Transcriptase Polymerase Chain Reaction
  • Signal Transduction
  • Stomach Neoplasms / enzymology
  • Stomach Neoplasms / genetics
  • Tumor Suppressor Protein p53 / genetics
  • Tumor Suppressor Protein p53 / metabolism
  • Up-Regulation
  • alpha-Fetoproteins / genetics
  • alpha-Fetoproteins / metabolism
  • beta Catenin / genetics
  • beta Catenin / metabolism

Substances

  • Tumor Suppressor Protein p53
  • alpha-Fetoproteins
  • beta Catenin
  • Cyclin D1
  • Insulin-Like Growth Factor II
  • Matrix Metalloproteinase 7
  • Cytidine Deaminase