Chromosome instability induced by Mps1 and p53 mutation generates aggressive lymphomas exhibiting aneuploidy-induced stress

Proc Natl Acad Sci U S A. 2014 Sep 16;111(37):13427-32. doi: 10.1073/pnas.1400892111. Epub 2014 Sep 2.

Abstract

Aneuploidy is a hallmark of human solid cancers that arises from errors in mitosis and results in gain and loss of oncogenes and tumor suppressors. Aneuploidy poses a growth disadvantage for cells grown in vitro, suggesting that cancer cells adapt to this burden. To understand better the consequences of aneuploidy in a rapidly proliferating adult tissue, we engineered a mouse in which chromosome instability was selectively induced in T cells. A flanked by Lox mutation was introduced into the monopolar spindle 1 (Mps1) spindle-assembly checkpoint gene so that Cre-mediated recombination would create a truncated protein (Mps1(DK)) that retained the kinase domain but lacked the kinetochore-binding domain and thereby weakened the checkpoint. In a sensitized p53(+/-) background we observed that Mps1(DK/DK) mice suffered from rapid-onset acute lymphoblastic lymphoma. The tumors were highly aneuploid and exhibited a metabolic burden similar to that previously characterized in aneuploid yeast and cultured cells. The tumors nonetheless grew rapidly and were lethal within 3-4 mo after birth.

Keywords: CIN; T-cell acute lymphoblastic lymphoma; chromosomal instability; mouse models; tumor metabolism.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aneuploidy*
  • Animals
  • Chromosomal Instability / genetics*
  • Chromosome Aberrations
  • Clone Cells
  • Gene Dosage
  • Gene Expression Regulation, Leukemic
  • Heterozygote
  • Humans
  • Karyotyping
  • M Phase Cell Cycle Checkpoints / genetics
  • Mice
  • Mutation / genetics*
  • Precursor T-Cell Lymphoblastic Leukemia-Lymphoma / genetics*
  • Precursor T-Cell Lymphoblastic Leukemia-Lymphoma / pathology*
  • Protein Serine-Threonine Kinases / chemistry
  • Protein Serine-Threonine Kinases / genetics*
  • Protein Structure, Tertiary
  • Stress, Physiological / genetics*
  • Transcription, Genetic
  • Tumor Suppressor Protein p53 / genetics*

Substances

  • Tumor Suppressor Protein p53
  • Ttk protein, mouse
  • Protein Serine-Threonine Kinases

Associated data

  • GEO/GSE57334