Cadherin-catenin complex dissociation in lobular neoplasia of the breast

Breast Cancer Res Treat. 2012 Apr;132(2):641-52. doi: 10.1007/s10549-011-1860-0. Epub 2011 Nov 13.

Abstract

E-cadherin (E-CD) inactivation with loss of E-CD-mediated cell adhesion is the hallmark of lesions of the lobular phenotype. E-CD is typically absent by immunohistochemistry in both lobular carcinoma in situ (LCIS) and invasive lobular lesions, suggesting it occurs early in the neoplastic process. In laboratory models, downstream post-transcriptional modifiers such as TWIST and SNAIL contribute to the dissociation of the intracellular component of the cadherin-catenin complex (CCC), resulting in tumor progression and invasion. We hypothesized that complete CCC dissociation may play a role in lobular neoplasia progression. Here we explore the relationship between loss of E-CD and dissociation of the CCC in pure LCIS and LCIS associated with invasive cancer. Fresh-frozen tissues were obtained from 36 patients undergoing mastectomy for pure LCIS (n = 11), LCIS with ILC (n = 18) or LCIS with IDC (n = 7). Individual lesions were subject to laser-capture microdissection and gene-expression analysis (Affymetrix HG-U133A 2.0). Immunohistochemistry for ER,PR,HER2, E-CD,N-CD,α-,β-, and phosphoβ-catenin, TWIST, and SNAIL were evaluated in normal, in situ, and invasive components from matched formalin-fixed paraffin-embedded samples (n = 36). CCC-dissociation was defined as negative membranous E-CD, α- and β-catenin expression. E-CD was negative in all LCIS and ILC lesions, and positive in all normal and IDC lesions. Membranous α and β-catenin expressions decreased with the transition from LCIS to ILC (pure LCIS 82%; LCIS w/ILC 28%; ILC 0%), while TWIST expression increased (pure LCIS low; LCIS w/ILC moderate; ILC high). Gene expression paralleled IHC-staining patterns with a stepwise downregulation of E-CD, α and β-catenins from normal to LCIS to invasive lesions, and increasing expression of TWIST from normal to LCIS to ILC. Loss of E-CD expression is an early event in lobular neoplasia. Decreasing membranous catenin expression in tandem with increasing levels of TWIST across the spectrum of lobular lesions suggests that CCC dissociation is a progressive process.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Antigens, CD
  • Biomarkers, Tumor / analysis*
  • Biomarkers, Tumor / genetics
  • Breast Neoplasms / chemistry*
  • Breast Neoplasms / genetics
  • Breast Neoplasms / pathology
  • Cadherins / analysis*
  • Cadherins / genetics
  • Carcinoma, Ductal, Breast / chemistry*
  • Carcinoma, Ductal, Breast / genetics
  • Carcinoma, Ductal, Breast / pathology
  • Carcinoma, Intraductal, Noninfiltrating / chemistry*
  • Carcinoma, Intraductal, Noninfiltrating / genetics
  • Carcinoma, Intraductal, Noninfiltrating / pathology
  • Carcinoma, Lobular / chemistry*
  • Carcinoma, Lobular / genetics
  • Carcinoma, Lobular / pathology
  • Female
  • Gene Expression Regulation, Neoplastic
  • Humans
  • Immunohistochemistry
  • Microdissection
  • Middle Aged
  • Neoplasm Invasiveness
  • Neoplasms, Complex and Mixed / chemistry*
  • Neoplasms, Complex and Mixed / genetics
  • Neoplasms, Complex and Mixed / pathology
  • New York City
  • Nuclear Proteins / analysis
  • Phosphorylation
  • Prognosis
  • Prospective Studies
  • Protein Binding
  • Snail Family Transcription Factors
  • Transcription Factors / analysis
  • Twist-Related Protein 1 / analysis
  • alpha Catenin / analysis*
  • alpha Catenin / genetics
  • beta Catenin / analysis*
  • beta Catenin / genetics

Substances

  • Antigens, CD
  • Biomarkers, Tumor
  • CDH1 protein, human
  • CTNNA1 protein, human
  • CTNNB1 protein, human
  • Cadherins
  • Nuclear Proteins
  • Snail Family Transcription Factors
  • TWIST1 protein, human
  • Transcription Factors
  • Twist-Related Protein 1
  • alpha Catenin
  • beta Catenin