Cloning and characterizing mutated human stromal cell-derived factor-1 (SDF-1): C-terminal alpha-helix of SDF-1alpha plays a critical role in CXCR4 activation and signaling, but not in CXCR4 binding affinity

Exp Hematol. 2006 Nov;34(11):1553-62. doi: 10.1016/j.exphem.2006.07.001.

Abstract

Objective: A novel C-terminal alpha-helix-defective mutant of human stromal cell-derived factor-1 (SDF-1), hSDF-154, was designed and produced in order to develop an optimal CXC chemokine receptor 4 (CXCR4) antagonist.

Materials and methods: Human native SDF-1 and alpha-helix defective SDF-1 (hSDF-154) were cloned from human bone marrow stromal cells by reverse transcription polymerase chain reaction, inserted into vector pET-30a(+), and transformed into Escherichia coli strain BL21(DE3). The recombinant hSDF-154 was purified and refolded under optimized conditions and its functional characteristics were compared with the native form of SDF-1. Functional evaluation includes migration of Jurkat and MOLT4 cells assessed by chemotaxis assay, intracellular calcium influx in these cells measured by flow cytometry, extracellular signal-regulated kinase (ERK) phosphorylation analyzed by Western blot assay, receptor binding affinity examined by sequential concentrations of unlabeled SDF-1alpha, hSDF-154 competition with (125)I- SDF-1alpha, and internalization of CXCR4 on the cell surface detected by flow cytometry.

Results: hSDF-154 had significantly decreased chemotaxic ability, such as cell migration, as compared to the native hSDF-1. hSDF-154 failed to trigger CXCR4 to induce transient calcium influx and ERK phosphorylation. However, both hSDF-154 and the native hSDF-1 have similar binding affinity to CXCR4 and a similar ability to induce CXCR4 internalization.

Conclusion: These results indicate that hSDF-154, which has a defective C-terminal alpha-helix, a normal N-terminus, and a normal central beta-strand scaffold structure, retains normal binding affinity to CXCR4 and normal induction of CXCR4 internalization, but fails to activate CXCR4-mediated cellular signaling and chemotaxis. Therefore, the C-terminal alpha-helix of hSDF-1 plays a critical role for CXCR4 stimulation. The hSDF-154, which efficiently binds to and induces internalization of CXCR4 without activating CXCR4-related intracellular signaling and cell migration, may serve as an optimal CXCR4 antagonist.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cell Line
  • Chemokine CXCL12 / genetics*
  • Chemokine CXCL12 / metabolism*
  • Chemokine CXCL12 / pharmacology
  • Cloning, Molecular
  • Humans
  • Mutation
  • Protein Binding / drug effects
  • Protein Structure, Secondary / physiology
  • Receptors, CXCR4 / antagonists & inhibitors
  • Receptors, CXCR4 / metabolism*
  • Recombinant Proteins / genetics
  • Recombinant Proteins / metabolism
  • Signal Transduction / drug effects
  • Stromal Cells / metabolism

Substances

  • CXCL12 protein, human
  • Chemokine CXCL12
  • Receptors, CXCR4
  • Recombinant Proteins