Highly infiltrative brain tumours show reduced chemosensitivity associated with a stem cell-like phenotype

Neuropathol Appl Neurobiol. 2009 Aug;35(4):380-93. doi: 10.1111/j.1365-2990.2008.01008.x.

Abstract

Aims: Cancer stem-like cells might have important functions in chemoresistance. We have developed a model where highly infiltrative brain tumours with a stem-like phenotype were established by orthotopic transplantation of human glioblastomas to immunodeficient rats. Serial passaging gradually transformed the tumours into a less invasive and more angiogenic phenotype (high-generation tumours). The invasive phenotype (low-generation tumours) was characterized by an increase in stem cell markers and increased phosphorylation of kinases in the phosphatidylinositol 3-kinase (PI3K)/AKT pathway. These markers were reduced in the serially passaged vascular tumours. The present study was aimed at investigating how the two phenotypes responded in vitro to doxorubicin, a clinically potent cytotoxic drug for solid tumours.

Methods: Biopsy spheroids were implanted and passaged intracranially in nude rats. Gene expression and protein analyses were performed, and drug sensitivity was assessed.

Results: Microarray analysis revealed gene ontology categories connected to developmental aspects and negative regulators of differentiation, especially in the infiltrative stem cell-like tumours. The highly invasive stem-like phenotype was chemoresistant compared with the angiogenic phenotype. By interfering with the PI3K it was possible to sensitize tumour spheroids to chemotherapy. Real-time quantitative polymerase chain reaction showed downregulation of the stem cell markers Nestin and Musashi-1 in low-generation biopsy spheroids following PI3K inhibition.

Conclusions: Highly invasive tumours with a stem-like phenotype are more chemoresistant than angiogenic tumours derived from the same patients. We suggest that treatment resistance in glioblastomas can be related to PI3K/AKT activity in stem-like tumour cells, and that targeted interference with the PI3K/AKT pathway might differentiate and sensitize this subpopulation to chemotherapy.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antineoplastic Agents / pharmacology
  • Brain / drug effects
  • Brain / physiopathology
  • Brain Neoplasms / drug therapy*
  • Brain Neoplasms / physiopathology*
  • Chromones / pharmacology
  • Doxorubicin / pharmacology
  • Enzyme Inhibitors / pharmacology
  • Glioblastoma / drug therapy*
  • Glioblastoma / physiopathology*
  • Glycogen Synthase Kinase 3 / metabolism
  • Humans
  • Intermediate Filament Proteins / metabolism
  • Morpholines / pharmacology
  • Neoplasm Transplantation
  • Nerve Tissue Proteins / metabolism
  • Nestin
  • Phenotype
  • Phosphatidylinositol 3-Kinases / metabolism
  • Phosphoinositide-3 Kinase Inhibitors
  • Phosphorylation
  • RNA, Messenger / metabolism
  • RNA-Binding Proteins / metabolism
  • Rats
  • Rats, Nude
  • Stem Cells / physiology*

Substances

  • Antineoplastic Agents
  • Chromones
  • Enzyme Inhibitors
  • Intermediate Filament Proteins
  • Morpholines
  • Msi1 protein, rat
  • NES protein, human
  • Nerve Tissue Proteins
  • Nes protein, rat
  • Nestin
  • Phosphoinositide-3 Kinase Inhibitors
  • RNA, Messenger
  • RNA-Binding Proteins
  • 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one
  • Doxorubicin
  • Glycogen Synthase Kinase 3
  • glycogen synthase kinase 3 alpha