IQGAP1 and NWASP promote human cancer cell dissemination and metastasis by regulating β1-integrin via FAK and MRTF/SRF

Cell Rep. 2024 Apr 23;43(4):113989. doi: 10.1016/j.celrep.2024.113989. Epub 2024 Mar 26.

Abstract

Attachment of circulating tumor cells to the endothelial cells (ECs) lining blood vessels is a critical step in cancer metastatic colonization, which leads to metastatic outgrowth. Breast and prostate cancers are common malignancies in women and men, respectively. Here, we observe that β1-integrin is required for human prostate and breast cancer cell adhesion to ECs under shear-stress conditions in vitro and to lung blood vessel ECs in vivo. We identify IQGAP1 and neural Wiskott-Aldrich syndrome protein (NWASP) as regulators of β1-integrin transcription and protein expression in prostate and breast cancer cells. IQGAP1 and NWASP depletion in cancer cells decreases adhesion to ECs in vitro and retention in the lung vasculature and metastatic lung nodule formation in vivo. Mechanistically, NWASP and IQGAP1 act downstream of Cdc42 to increase β1-integrin expression both via extracellular signal-regulated kinase (ERK)/focal adhesion kinase signaling at the protein level and by myocardin-related transcription factor/serum response factor (SRF) transcriptionally. Our results identify IQGAP1 and NWASP as potential therapeutic targets to reduce early metastatic dissemination.

Keywords: CP: Cancer; IQGAP1; NWASP; Rho GTPases; cancer metastasis; cell-cell adhesion; endothelial adhesion; shear stress; signaling; β-integrin.

Publication types

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

MeSH terms

  • Animals
  • Breast Neoplasms / genetics
  • Breast Neoplasms / metabolism
  • Breast Neoplasms / pathology
  • Cell Adhesion
  • Cell Line, Tumor
  • Female
  • Focal Adhesion Kinase 1 / genetics
  • Focal Adhesion Kinase 1 / metabolism
  • Gene Expression Regulation, Neoplastic
  • Humans
  • Integrin beta1* / genetics
  • Integrin beta1* / metabolism
  • Male
  • Mice
  • Neoplasm Metastasis*
  • Prostatic Neoplasms / genetics
  • Prostatic Neoplasms / metabolism
  • Prostatic Neoplasms / pathology
  • Serum Response Factor* / metabolism
  • Trans-Activators / metabolism
  • Wiskott-Aldrich Syndrome Protein, Neuronal / genetics
  • Wiskott-Aldrich Syndrome Protein, Neuronal / metabolism
  • cdc42 GTP-Binding Protein / metabolism
  • ras GTPase-Activating Proteins* / genetics
  • ras GTPase-Activating Proteins* / metabolism

Substances

  • IQ motif containing GTPase activating protein 1
  • Integrin beta1
  • ras GTPase-Activating Proteins
  • Serum Response Factor
  • Trans-Activators
  • Wiskott-Aldrich Syndrome Protein, Neuronal
  • Focal Adhesion Kinase 1
  • SRF protein, human
  • PTK2 protein, human
  • WASL protein, human
  • MRTFA protein, human
  • cdc42 GTP-Binding Protein