scribble mutants cooperate with oncogenic Ras or Notch to cause neoplastic overgrowth in Drosophila

EMBO J. 2003 Nov 3;22(21):5769-79. doi: 10.1093/emboj/cdg548.

Abstract

Cancer is a multistep process involving cooperation between oncogenic or tumor suppressor mutations and interactions between the tumor and surrounding normal tissue. Here we present the first description of cooperative tumorigenesis in Drosophila, by using a system that mimics the development of tumors in mammals. We have used the MARCM system to generate mutant clones of the apical-basal cell polarity tumor suppressor gene, scribble, in the context of normal tissue. We show that scribble mutant clones in the eye disc exhibit ectopic expression of cyclin E and ectopic cell cycles, but do not overgrow due to increased cell death mediated by the JNK pathway and the surrounding wild-type tissue. In contrast, when oncogenic Ras or Notch is expressed within the scribble mutant clones, cell death is prevented and neoplastic tumors develop. This demonstrates, for the first time in Drosophila, that activated alleles of Ras and Notch can act as cooperating oncogenes in the development of epithelial tumors, and highlights the importance of epithelial polarity regulators in restraining oncogenes and preventing tumor formation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis
  • Cyclin E / genetics
  • Drosophila / genetics*
  • Drosophila / growth & development
  • Drosophila / physiology
  • Drosophila Proteins / genetics*
  • Drosophila Proteins / physiology
  • Eye / growth & development
  • Gene Expression Regulation, Neoplastic
  • Genes, Insect*
  • Genes, ras
  • JNK Mitogen-Activated Protein Kinases
  • Membrane Proteins / genetics*
  • Membrane Proteins / physiology
  • Mitogen-Activated Protein Kinases / physiology
  • Models, Biological
  • Mutation*
  • Neoplasms, Experimental / etiology
  • Neoplasms, Experimental / genetics
  • Receptors, Notch
  • Up-Regulation

Substances

  • Cyclin E
  • Drosophila Proteins
  • Membrane Proteins
  • N protein, Drosophila
  • Receptors, Notch
  • Scrib protein, Drosophila
  • JNK Mitogen-Activated Protein Kinases
  • Mitogen-Activated Protein Kinases