Loss of DeltaNp63alpha promotes invasion of urothelial carcinomas via N-cadherin/Src homology and collagen/extracellular signal-regulated kinase pathway

Cancer Res. 2009 Dec 15;69(24):9263-70. doi: 10.1158/0008-5472.CAN-09-1188.

Abstract

p63 plays a critical role in normal development and maintenance of stratified epithelia, including the urothelium. In the normal urothelium, urothelial cells in the basal layers abundantly express the predominant p63 isoform DeltaNp63alpha. We previously showed that (a) DeltaNp63alpha expression at the similar level to the normal urothelium is retained in most low-grade papillary noninvasive (LPN) tumors, whereas frequently lost in high-grade invasive carcinomas, and that (b) loss of DeltaNp63alpha is associated with poor prognosis of invasive bladder urothelial carcinoma patients. However, a functional role of DeltaNp63alpha in progression of urothelial carcinomas remains to be elucidated. Here, we show that loss of DeltaNp63alpha expression promotes invasion of urothelial carcinoma cells. In 5637 cells substantially expressing only DeltaNp63alpha isoform at the protein level, knockdown of endogenous p63 upregulated N-cadherin, which recruited more Src homology and collagen to N-cadherin and activated extracellular signal-regulated kinase (ERK) signaling, and consequently potentiated cell motility, excretion of matrix metalloproteinase-9, and invasion. In T24 cells originally lacking endogenous DeltaNp63alpha expression, exogenous expression of DeltaNp63alpha attenuated invasion by downregulating N-cadherin expression and ERK activity, confirming an invasion-suppressive role of DeltaNp63alpha in urothelial carcinoma cells. We further documented loss of DeltaNp63 expression accompanied by N-cadherin upregulation during muscle-invasive recurrence in patients whose bladder cancer had progressed from LPN tumors to muscle-invasive disease. These results suggest that loss of DeltaNp63alpha and subsequent upregulation of N-cadherin is one of the mechanisms underlying progression of bladder cancer.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Antigens, CD / biosynthesis
  • Antigens, CD / genetics
  • Antigens, CD / metabolism*
  • Cadherins / biosynthesis
  • Cadherins / genetics
  • Cadherins / metabolism*
  • Cell Line, Tumor
  • Collagen / metabolism*
  • Disease Progression
  • Enzyme Activation
  • Extracellular Signal-Regulated MAP Kinases / metabolism*
  • Gene Expression Profiling
  • Humans
  • MAP Kinase Signaling System*
  • Neoplasm Invasiveness
  • Neoplasm Recurrence, Local / enzymology
  • Neoplasm Recurrence, Local / genetics
  • Neoplasm Recurrence, Local / metabolism
  • Neoplasm Recurrence, Local / pathology
  • Shc Signaling Adaptor Proteins / metabolism*
  • Trans-Activators / deficiency*
  • Trans-Activators / genetics
  • Trans-Activators / metabolism
  • Transcription Factors
  • Tumor Suppressor Proteins / deficiency*
  • Tumor Suppressor Proteins / genetics
  • Tumor Suppressor Proteins / metabolism
  • Up-Regulation
  • Urinary Bladder Neoplasms / enzymology
  • Urinary Bladder Neoplasms / genetics
  • Urinary Bladder Neoplasms / metabolism*
  • Urinary Bladder Neoplasms / pathology

Substances

  • Antigens, CD
  • CDH2 protein, human
  • Cadherins
  • Shc Signaling Adaptor Proteins
  • TP63 protein, human
  • Trans-Activators
  • Transcription Factors
  • Tumor Suppressor Proteins
  • Collagen
  • Extracellular Signal-Regulated MAP Kinases