SLX4IP Antagonizes Promiscuous BLM Activity during ALT Maintenance

Mol Cell. 2019 Oct 3;76(1):27-43.e11. doi: 10.1016/j.molcel.2019.07.010. Epub 2019 Aug 22.

Abstract

Cancer cells acquire unlimited proliferative capacity by either re-expressing telomerase or inducing alternative lengthening of telomeres (ALT), which relies on telomere recombination. Here, we show that ALT recombination requires coordinate regulation of the SMX and BTR complexes to ensure the appropriate balance of resolution and dissolution activities at recombining telomeres. Critical to this control is SLX4IP, which accumulates at ALT telomeres and interacts with SLX4, XPF, and BLM. Loss of SLX4IP increases ALT-related phenotypes, which is incompatible with cell growth following concomitant loss of SLX4. Inactivation of BLM is sufficient to rescue telomere aggregation and the synthetic growth defect in this context, suggesting that SLX4IP favors SMX-dependent resolution by antagonizing promiscuous BLM activity during ALT recombination. Finally, we show that SLX4IP is inactivated in a subset of ALT-positive osteosarcomas. Collectively, our findings uncover an SLX4IP-dependent regulatory mechanism critical for telomere maintenance in ALT cancer cells.

Keywords: ALT; BLM; SLX4; SLX4IP; XPF; cancer; genome stability; homologous recombination; telomere.

Publication types

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

MeSH terms

  • Animals
  • Bone Neoplasms / enzymology*
  • Bone Neoplasms / genetics
  • Bone Neoplasms / pathology
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism*
  • Cell Proliferation
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • Female
  • Gene Expression Regulation, Enzymologic
  • Gene Expression Regulation, Neoplastic
  • HEK293 Cells
  • HeLa Cells
  • Humans
  • Mice, Knockout
  • Mice, SCID
  • Osteosarcoma / enzymology*
  • Osteosarcoma / genetics
  • Osteosarcoma / pathology
  • Protein Binding
  • Protein Interaction Domains and Motifs
  • RecQ Helicases / genetics
  • RecQ Helicases / metabolism*
  • Recombinases / genetics
  • Recombinases / metabolism
  • Signal Transduction
  • Telomere / genetics
  • Telomere / metabolism*
  • Telomere / pathology
  • Telomere Homeostasis*

Substances

  • Carrier Proteins
  • DNA-Binding Proteins
  • Recombinases
  • SLX4IP protein, human
  • xeroderma pigmentosum group F protein
  • SLX4 protein, human
  • Bloom syndrome protein
  • RecQ Helicases