Production of recombinant human trimeric CD137L (4-1BBL). Cross-linking is essential to its T cell co-stimulation activity

J Biol Chem. 2005 Dec 16;280(50):41472-81. doi: 10.1074/jbc.M506881200. Epub 2005 Oct 4.

Abstract

The interaction between 4-1BB ligand (CD137L), a member of the tumor necrosis factor superfamily, and its receptor 4-1BB provides a co-stimulatory signal for T lymphocyte proliferation and survival. However, the structure of 4-1BBL has not been thoroughly investigated, and none of the human recombinant 4-1BBL molecules available have been described as capable of co-stimulating T cells. The present work provides a model of the three-dimensional structure of the tumor necrosis factor homology domain of 4-1BBL and describes the production of a recombinant human soluble 4-1BBL whose originality lies in that it contains the whole extracellular tail preceding the tumor necrosis factor homology domain and an AviTag peptide (AviTag-4-1BBL) allowing enzymatic biotinylation and multimerization via streptavidin. We provide evidence that this chimeric protein exists as a homotrimer, whereas commercial FLAG-tagged 4-1BBL does not. This resulted in a much higher affinity for 4-1BB (1.2 nM) as compared with FLAG-4-1BBL (55.2 nM). We demonstrate that the single extracellular cysteine residue in the tail (Cys-51) could form a disulfide bond, both in our recombinant protein and in physiologically expressed 4-1BBL. The mutation of this cysteine residue exerted no effect on trimerization but increased the dissociation rate of AviTag-4-1BBL from 4-1BB. In its soluble form, AviTag-4-1BBL did not stimulate purified T cells but dramatically inhibited proliferation of peripheral blood mononuclear cells stimulated with anti-CD3 mAb. In contrast, a very significant co-stimulatory effect was observed on purified T cells once AviTag-4-1BBL was immobilized onto streptavidin beads. In addition, we show that the cross-linking of two trimeric AviTag-4-1BBL molecules was the minimum step required to elicit significant costimulatory activity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 4-1BB Ligand
  • Amino Acid Sequence
  • Animals
  • Antigens, CD / chemistry*
  • Biotinylation
  • Blotting, Western
  • Cell Proliferation
  • Chromatography, Gel
  • Cross-Linking Reagents / pharmacology
  • Cysteine / chemistry
  • DNA, Complementary / metabolism
  • Dimerization
  • Disulfides / chemistry
  • Dose-Response Relationship, Drug
  • Drosophila
  • Electrophoresis, Polyacrylamide Gel
  • Humans
  • Insecta
  • Leukocytes, Mononuclear / cytology
  • Models, Molecular
  • Models, Statistical
  • Molecular Sequence Data
  • Peptides / chemistry
  • Protein Binding
  • Protein Conformation
  • Protein Structure, Tertiary
  • Receptors, Nerve Growth Factor / chemistry*
  • Receptors, Tumor Necrosis Factor / chemistry*
  • Receptors, Tumor Necrosis Factor / metabolism
  • Recombinant Fusion Proteins / chemistry*
  • Recombinant Proteins / chemistry
  • Sequence Homology, Amino Acid
  • Signal Transduction
  • Streptavidin / chemistry
  • Surface Plasmon Resonance
  • T-Lymphocytes / cytology
  • T-Lymphocytes / metabolism*
  • Time Factors
  • Tumor Necrosis Factor Receptor Superfamily, Member 9
  • Tumor Necrosis Factors / chemistry*
  • Tumor Necrosis Factors / metabolism

Substances

  • 4-1BB Ligand
  • Antigens, CD
  • Cross-Linking Reagents
  • DNA, Complementary
  • Disulfides
  • Peptides
  • Receptors, Nerve Growth Factor
  • Receptors, Tumor Necrosis Factor
  • Recombinant Fusion Proteins
  • Recombinant Proteins
  • TNFRSF9 protein, human
  • TNFSF9 protein, human
  • Tumor Necrosis Factor Receptor Superfamily, Member 9
  • Tumor Necrosis Factors
  • Streptavidin
  • Cysteine