A feedforward circuit shaped by ECT2 and USP7 contributes to breast carcinogenesis

Theranostics. 2020 Aug 29;10(23):10769-10790. doi: 10.7150/thno.46878. eCollection 2020.

Abstract

Rationale: A number of guanine nucleotide exchange factors (GEFs) including epithelial cell transforming factor ECT2 are believed to drive carcinogenesis through activating distinct oncogenic GTPases. Yet, whether GEF-independent activity of ECT2 also plays a role in tumorigenesis remains unclear. Methods: Immunohistochemical (IHC) staining, colony formation and xenograft assays were used to examine the role of ECT2 in breast carcinogenesis. Co-immunoprecipitation, immunofluorescent stainings, in vivo deubiquitination and in vitro deubiquitination experiments were performed to examine the physical and functional interaction between ECT2 and ubiquitin-specific protease USP7. High-throughput RNA sequencing, quantitative reverse transcription-PCR and Western blotting were employed to investigate the biological significance of the interplay between ECT2 and USP7. Results: We report that ECT2 plays a tumor-promoting role in breast cancer, and GEF activity-deficient ECT2 is able to alleviate ECT2 depletion associated growth defects in breast cancer cells. Mechanistically, we demonstrated that ECT2 physically interacts with ubiquitin-specific protease USP7 and functionally facilitates USP7 intermolecular self-association, -deubiquitination and -stabilization in a GEF activity-independent manner. USP7 in turn, deubiquitinates and stabilizes ECT2, resulting in a feedforward regulatory circuit that ultimately sustains the expression of oncogenic protein MDM2. Conclusion: Our study uncovers a GEF-independent role of ECT2 in promoting survival of breast cancer cells, provides a molecular insight for the reciprocal regulation of ECT2 and USP7, and supports the pursuit of ECT2/USP7 as potential targets for breast cancer intervention.

Keywords: Breast cancer; Deubiquitinase; Deubiquitination; Guanine nucleotide exchange factors; Protein stability.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Breast Neoplasms / genetics*
  • Breast Neoplasms / pathology
  • Carcinogenesis / genetics*
  • Cell Line, Tumor
  • Cell Survival / genetics
  • Enzyme Assays
  • Feedback, Physiological
  • Female
  • Gene Expression Regulation, Neoplastic
  • Gene Knockdown Techniques
  • Gene Knockout Techniques
  • HEK293 Cells
  • Humans
  • Mice
  • Protein Binding / genetics
  • Protein Stability
  • Proto-Oncogene Proteins / genetics
  • Proto-Oncogene Proteins / isolation & purification
  • Proto-Oncogene Proteins / metabolism*
  • Proto-Oncogene Proteins c-mdm2 / genetics*
  • RNA-Seq
  • Recombinant Proteins / isolation & purification
  • Recombinant Proteins / metabolism
  • Ubiquitin-Specific Peptidase 7 / genetics
  • Ubiquitin-Specific Peptidase 7 / isolation & purification
  • Ubiquitin-Specific Peptidase 7 / metabolism*
  • Ubiquitination
  • Xenograft Model Antitumor Assays

Substances

  • ECT2 protein, human
  • Proto-Oncogene Proteins
  • Recombinant Proteins
  • MDM2 protein, human
  • Proto-Oncogene Proteins c-mdm2
  • USP7 protein, human
  • Ubiquitin-Specific Peptidase 7