Preclinical development of a novel class of CXCR4 antagonist impairing solid tumors growth and metastases

PLoS One. 2013 Sep 13;8(9):e74548. doi: 10.1371/journal.pone.0074548. eCollection 2013.

Abstract

The CXCR4/CXCL12 axis plays a role in cancer metastases, stem cell mobilization and chemosensitization. Proof of concept for efficient CXCR4 inhibition has been demonstrated in stem cell mobilization prior to autologous transplantation in hematological malignancies. Nevertheless CXCR4 inhibitors suitable for prolonged use as required for anticancer therapy are not available. To develop new CXCR4 antagonists a rational, ligand-based approach was taken, distinct from the more commonly used development strategy. A three amino acid motif (Ar-Ar-X) in CXCL12, also found in the reverse orientation (X-Ar-Ar) in the vMIP-II inhibitory chemokine formed the core of nineteen cyclic peptides evaluated for inhibition of CXCR4-dependent migration, binding, P-ERK1/2-induction and calcium efflux. Peptides R, S and I were chosen for evaluation in in vivo models of lung metastases (B16-CXCR4 and KTM2 murine osteosarcoma cells) and growth of a renal cells xenograft. Peptides R, S, and T significantly reduced the association of the 12G5-CXCR4 antibody to the receptor and inhibited CXCL12-induced calcium efflux. The four peptides efficiently inhibited CXCL12-dependent migration at concentrations as low as 10 nM and delayed CXCL12-mediated wound healing in PES43 human melanoma cells. Intraperitoneal treatment with peptides R, I or S drastically reduced the number of B16-CXCR4-derived lung metastases in C57/BL mice. KTM2 osteosarcoma lung metastases were also reduced in Balb/C mice following CXCR4 inhibition. All three peptides significantly inhibited subcutaneous growth of SN12C-EGFP renal cancer cells. A novel class of CXCR4 inhibitory peptides was discovered. Three peptides, R, I and S inhibited lung metastases and primary tumor growth and will be evaluated as anticancer agents.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Calcium / metabolism
  • Cell Line, Tumor
  • Cell Movement / drug effects
  • Cell Proliferation / drug effects
  • Chemokine CXCL12 / pharmacology
  • Drug Design
  • Drug Screening Assays, Antitumor
  • Extracellular Signal-Regulated MAP Kinases / metabolism
  • Humans
  • Lung Neoplasms / drug therapy*
  • Lung Neoplasms / secondary*
  • Melanoma, Experimental / drug therapy*
  • Melanoma, Experimental / pathology*
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Molecular Sequence Data
  • Osteosarcoma / drug therapy
  • Osteosarcoma / pathology*
  • Peptides, Cyclic / chemistry
  • Peptides, Cyclic / pharmacology
  • Peptides, Cyclic / therapeutic use*
  • Phosphorylation / drug effects
  • Protein Binding / drug effects
  • Receptors, CXCR4 / antagonists & inhibitors*
  • Receptors, CXCR4 / metabolism
  • Wound Healing / drug effects

Substances

  • Chemokine CXCL12
  • Peptides, Cyclic
  • Receptors, CXCR4
  • Extracellular Signal-Regulated MAP Kinases
  • Calcium

Grants and funding

This work was supported by Alleanza Contro il Cancro (ACC9), Associazione Italiana per la Ricerca sul Cancro IG 13192, and FIRB RBAP11884M-008. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.