CXCR4 and CXCR7 Mediate TFF3-Induced Cell Migration Independently From the ERK1/2 Signaling Pathway

Invest Ophthalmol Vis Sci. 2016 Jan 1;57(1):56-65. doi: 10.1167/iovs.15-18129.

Abstract

Purpose: Trefoil factor family (TFF) peptides, and in particular TFF3, are characteristic secretory products of mucous epithelia that promote antiapoptosis, epithelial migration, restitution, and wound healing. For a long time, a receptor for TFF3 had not yet been identified. However, the chemokine receptor CXCR4 has been described as a low affinity receptor for TFF2. Additionally, CXCR7, which is able to heterodimerize with CXCR4, has also been discussed as a potential TFF2 receptor. Since there are distinct structural similarities between the three known TFF peptides, this study evaluated whether CXCR4 and CXCR7 may also act as putative TFF3 receptors.

Methods: We evaluated the expression of both CXCR4 and CXCR7 in samples of human ocular surface tissues and cell lines, using RT-PCR, immunohistochemistry, and Western blot analysis. Furthermore, we studied possible binding interactions between TFF3 and the receptor proteins in an x-ray structure-based modeling system. Functional studies of TFF3-CXCR4/CXCR7 interaction were accomplished by cell culture-based migration assays, flow cytometry, and evaluation of activation of the mitogen-activated protein (MAP) kinase signaling cascade.

Results: We detected both receptors at mRNA and protein level in all analyzed ocular surface tissues, and in lesser amount in ocular surface cell lines. X-ray structure-based modeling revealed CXCR4 and CXCR7 dimers as possible binding partners to TFF3. Cell culture-based assays revealed enhanced cell migration under TFF3 stimulation in a conjunctival epithelial cell line, which was completely suppressed by blocking CXCR4 and/or CXCR7. Flow cytometry showed increased proliferation rates after TFF3 treatment, while blocking both receptors had no effect on this increase. Trefoil factor family 3 also activated the MAP kinase signaling cascade independently from receptor activity.

Conclusions: Dimers CXCR4 and CXCR7 are involved in TFF3-dependent activation of cell migration, but not cell proliferation. The ERK1/2 pathway is activated in the process, but not influenced by CXCR4 or CXCR7. These results implicate a dependence of TFF3 activity as to cell migration on the chemokine receptors CXCR4 and CXCR7 at the ocular surface.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aged
  • Aged, 80 and over
  • Apoptosis
  • Blotting, Western
  • Cadaver
  • Cell Line
  • Cell Movement
  • Cell Proliferation
  • Epithelium, Corneal / cytology
  • Epithelium, Corneal / metabolism*
  • Female
  • Gene Expression Regulation*
  • Humans
  • Immunohistochemistry
  • MAP Kinase Signaling System / physiology*
  • Male
  • Peptides / genetics*
  • Peptides / metabolism
  • RNA / genetics*
  • Receptors, CXCR / biosynthesis
  • Receptors, CXCR / genetics*
  • Receptors, CXCR4 / biosynthesis
  • Receptors, CXCR4 / genetics*
  • Reverse Transcriptase Polymerase Chain Reaction
  • Signal Transduction
  • Trefoil Factor-2
  • Trefoil Factor-3

Substances

  • ACKR3 protein, human
  • CXCR4 protein, human
  • Peptides
  • Receptors, CXCR
  • Receptors, CXCR4
  • TFF2 protein, human
  • TFF3 protein, human
  • Trefoil Factor-2
  • Trefoil Factor-3
  • RNA