Development of a unique small molecule modulator of CXCR4

PLoS One. 2012;7(4):e34038. doi: 10.1371/journal.pone.0034038. Epub 2012 Apr 2.

Abstract

Background: Metastasis, the spread and growth of tumor cells to distant organ sites, represents the most devastating attribute and plays a major role in the morbidity and mortality of cancer. Inflammation is crucial for malignant tumor transformation and survival. Thus, blocking inflammation is expected to serve as an effective cancer treatment. Among anti-inflammation therapies, chemokine modulation is now beginning to emerge from the pipeline. CXC chemokine receptor-4 (CXCR4) and its ligand stromal cell-derived factor-1 (CXCL12) interaction and the resulting cell signaling cascade have emerged as highly relevant targets since they play pleiotropic roles in metastatic progression. The unique function of CXCR4 is to promote the homing of tumor cells to their microenvironment at the distant organ sites.

Methodology/principal findings: We describe the actions of N,N'-(1,4-phenylenebis(methylene))dipyrimidin-2-amine (designated MSX-122), a novel small molecule and partial CXCR4 antagonist with properties quite unlike that of any other reported CXCR4 antagonists, which was prepared in a single chemical step using a reductive amination reaction. Its specificity toward CXCR4 was tested in a binding affinity assay and a ligand competition assay using (18)F-labeled MSX-122. The potency of the compound was determined in two functional assays, Matrigel invasion assay and cAMP modulation. The therapeutic potential of MSX-122 was evaluated in three different murine models for inflammation including an experimental colitis, carrageenan induced paw edema, and bleomycin induced lung fibrosis and three different animal models for metastasis including breast cancer micrometastasis in lung, head and neck cancer metastasis in lung, and uveal melanoma micrometastasis in liver in which CXCR4 was reported to play crucial roles.

Conclusions/significance: We developed a novel small molecule, MSX-122, that is a partial CXCR4 antagonist without mobilizing stem cells, which can be safer for long-term blockade of metastasis than other reported CXCR4 antagonists.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Anti-Inflammatory Agents / pharmacology*
  • Anti-Inflammatory Agents / therapeutic use
  • Antineoplastic Agents / pharmacology*
  • Antineoplastic Agents / therapeutic use
  • Breast Neoplasms / pathology
  • Cell Line, Tumor
  • Colitis / chemically induced
  • Colitis / drug therapy
  • Colitis / pathology
  • Computer Simulation
  • Drug Design
  • Edema / chemically induced
  • Edema / drug therapy
  • Female
  • Fibrosis / chemically induced
  • Fibrosis / drug therapy
  • Head and Neck Neoplasms / pathology
  • Humans
  • Liver Neoplasms / prevention & control
  • Liver Neoplasms / secondary
  • Lung / drug effects
  • Lung / pathology
  • Lung Neoplasms / prevention & control
  • Lung Neoplasms / secondary
  • Male
  • Melanoma / pathology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Nude
  • Models, Molecular
  • Protein Binding
  • Pyrimidines / pharmacology*
  • Pyrimidines / therapeutic use
  • Receptors, CXCR4 / antagonists & inhibitors*
  • Receptors, CXCR4 / metabolism
  • Uveal Neoplasms / pathology
  • Xenograft Model Antitumor Assays

Substances

  • Anti-Inflammatory Agents
  • Antineoplastic Agents
  • CXCR4 protein, human
  • N,N'-(1,4-phenylenebis(methylene))dipyrimidin-2-amine
  • Pyrimidines
  • Receptors, CXCR4

Supplementary concepts

  • Uveal melanoma