Nucleolar delocalization of human topoisomerase I in response to topotecan correlates with sumoylation of the protein

J Biol Chem. 2002 Jan 25;277(4):2958-64. doi: 10.1074/jbc.M108263200. Epub 2001 Nov 14.

Abstract

DNA topoisomerase (topo) I is an essential nuclear protein and a target for anticancer drug camptothecin derivatives. As a nuclear protein, topo I is concentrated in the nucleolus. However, this nucleolar distribution of topo I is dynamic. It has been shown recently that topo I rapidly moves out of the nucleolus (nucleolar delocalization) in response to topo I inhibitors. In the present study, we demonstrated that nucleolar delocalization of topo I is associated with its conjugation by SUMOs (small ubiquitin-like modifiers) in response to the topo I inhibitor topotecan. Time-course experiments revealed that SUMO-topo I conjugation occurred at as early as 5 min after drug treatment, which was earlier than its observed nucleolar delocalization. Furthermore, heat shock blocked sumoylation of topo I; it also blocked the nucleolar delocalization of topo I fusion proteins. UBC9 is an E2 (ubiquitin carrier protein)-conjugating enzyme essential for sumoylation. Although overexpression of wild-type UBC9 enhanced both sumoylation and nuclear delocalization of topo I, overexpression of a UBC9 dominant negative mutant attenuated topo I sumoylation and its nucleolar delocalization. Taken together, our results suggest that sumoylation of topo I might serve as an addressing tag for its nucleolar delocalization in response to topo I inhibitors.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Active Transport, Cell Nucleus
  • Antineoplastic Agents / pharmacology
  • Blotting, Western
  • Cell Nucleolus / enzymology*
  • DNA Repair
  • DNA Topoisomerases, Type I / biosynthesis*
  • Dose-Response Relationship, Drug
  • Enzyme Inhibitors / pharmacology
  • Genes, Dominant
  • HeLa Cells
  • Hot Temperature
  • Humans
  • Microscopy, Confocal
  • Microscopy, Fluorescence
  • Mutation
  • Plasmids / metabolism
  • Recombinant Fusion Proteins / metabolism
  • Small Ubiquitin-Related Modifier Proteins / metabolism*
  • Temperature
  • Time Factors
  • Topotecan / pharmacology*
  • Transfection

Substances

  • Antineoplastic Agents
  • Enzyme Inhibitors
  • Recombinant Fusion Proteins
  • Small Ubiquitin-Related Modifier Proteins
  • Topotecan
  • DNA Topoisomerases, Type I