Invading cancer cells are predominantly in G0/G1 resulting in chemoresistance demonstrated by real-time FUCCI imaging

Cell Cycle. 2014;13(6):953-60. doi: 10.4161/cc.27818. Epub 2014 Jan 20.

Abstract

Invasive cancer cells are a critical target in order to prevent metastasis. In the present report, we demonstrate real-time visualization of cell cycle kinetics of invading cancer cells in 3-dimensional (3D) Gelfoam® histoculture, which is in vivo-like. A fluorescence ubiquitination cell cycle indicator (FUCCI) whereby G0/G1 cells express a red fluorescent protein and S/G2/M cells express a green fluorescent protein was used to determine the cell cycle position of invading and non-invading cells. With FUCCI 3D confocal imaging, we observed that cancer cells in G0/G1 phase in Gelfoam® histoculture migrated more rapidly and further than cancer cells in S/G2/M phases. Cancer cells ceased migrating when they entered S/G2/M phases and restarted migrating after cell division when the cells re-entered G0/G1. Migrating cancer cells also were resistant to cytotoxic chemotherapy, since they were preponderantly in G0/G1, where cytotoxic chemotherapy is not effective. The results of the present report suggest that novel therapy targeting G0/G1 cancer cells should be developed to prevent metastasis.

Keywords: 3D; FUCCI; Gelfoam histoculture; cancer invasion; cell cycle kinetics; confocal laser microscopy; fluorescent proteins; real-time imaging.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Adenocarcinoma / drug therapy
  • Adenocarcinoma / pathology*
  • Antineoplastic Agents / therapeutic use
  • Cell Line, Tumor
  • Cell Movement
  • Cisplatin / therapeutic use
  • Drug Resistance, Neoplasm / physiology*
  • G1 Phase / physiology*
  • Gelatin Sponge, Absorbable
  • Green Fluorescent Proteins / genetics
  • Green Fluorescent Proteins / metabolism
  • Humans
  • Luminescent Proteins / genetics
  • Luminescent Proteins / metabolism
  • Microscopy, Confocal
  • Neoplasm Invasiveness
  • Red Fluorescent Protein
  • Resting Phase, Cell Cycle / physiology*
  • Stomach Neoplasms / drug therapy
  • Stomach Neoplasms / pathology*

Substances

  • Antineoplastic Agents
  • Luminescent Proteins
  • Green Fluorescent Proteins
  • Cisplatin