Dysregulated expression of stem cell factor Bmi1 in precancerous lesions of the gastrointestinal tract

Clin Cancer Res. 2006 Dec 1;12(23):6960-6. doi: 10.1158/1078-0432.CCR-06-0449.

Abstract

Purpose: It is important to identify the definitive molecular switches involved in the malignant transformation of premalignant tissues. Cellular senescence is a specific characteristic of precancerous tissues, but not of cancers, which might reflect tumorigenesis-protecting mechanisms in premalignant lesions. Polycomb protein Bmi1, which is a potent negative regulator of the p16INK4 gene, suppresses senescence in primary cells and is overexpressed in various cancers. We hypothesized that Bmi1 expression would also be dysregulated in precancerous lesions in human digestive precancerous tissues.

Experimental design: Bmi1 expression was investigated in cancerous and precancerous tissues of the digestive tract. The expression of p16, beta-catenin, and Gli1 and the in vivo methylation status of the p16 gene were also analyzed in serial sections of colonic precancerous lesions.

Results: Bmi1 was clearly overexpressed across a broad spectrum of gastrointestinal cancers, and the expression of Bmi1 increased in a manner that reflected the pathologic malignant features of precancerous colonic tissues (low-grade dysplasia, 12.9 +/- 2.0%; high-grade dysplasia, 82.9 +/- 1.6%; cancer, 87.5 +/- 2.4%). p16 was also strongly expressed in high-grade dysplasia, but not in cancers. p16 promoter methylation was detected only in some Bmi1-positive neoplastic cells.

Conclusions: Bmi1 overexpression was correlated with the malignant grades of human digestive precancerous tissues, which suggests that advanced Bmi1 dysregulation might predict malignant progression. The abnormal Bmi1 expression might link to malignant transformation via the disturbance of orderly histone modification.

MeSH terms

  • Cell Line, Tumor
  • Colon / metabolism
  • Colon / pathology
  • Colonic Neoplasms / genetics*
  • Colonic Neoplasms / metabolism
  • Colonic Neoplasms / pathology
  • Cyclin-Dependent Kinase Inhibitor p16 / genetics
  • Cyclin-Dependent Kinase Inhibitor p16 / metabolism
  • DNA Methylation
  • Gastrointestinal Neoplasms / genetics*
  • Gastrointestinal Neoplasms / metabolism
  • Gastrointestinal Neoplasms / pathology
  • Gastrointestinal Tract / metabolism
  • Gastrointestinal Tract / pathology*
  • Gene Expression Profiling
  • Gene Expression Regulation, Neoplastic / genetics*
  • Hedgehog Proteins / metabolism
  • Humans
  • Nuclear Proteins / genetics*
  • Nuclear Proteins / metabolism
  • Polycomb Repressive Complex 1
  • Polymerase Chain Reaction / methods
  • Precancerous Conditions / genetics*
  • Precancerous Conditions / pathology
  • Promoter Regions, Genetic / genetics
  • Proto-Oncogene Proteins / genetics*
  • Proto-Oncogene Proteins / metabolism
  • RNA, Messenger / biosynthesis
  • RNA, Messenger / genetics
  • Repressor Proteins / genetics*
  • Repressor Proteins / metabolism
  • Signal Transduction / genetics
  • Wnt Proteins / metabolism

Substances

  • BMI1 protein, human
  • Cyclin-Dependent Kinase Inhibitor p16
  • Hedgehog Proteins
  • Nuclear Proteins
  • Proto-Oncogene Proteins
  • RNA, Messenger
  • Repressor Proteins
  • Wnt Proteins
  • Polycomb Repressive Complex 1