Binding and functional comparisons of two types of tumor necrosis factor antagonists.

Two tumor necrosis factor (TNF) antagonists infliximab (a chimeric monoclonal antibody) and etanercept (a p75 TNF receptor/Fc fusion protein) have been approved for treatment of rheumatoid arthritis. However, these agents have shown different degrees of clinical benefit in controlled clinical trials in other TNF-mediated diseases such as Crohn's disease (CD) and psoriasis. We investigated whether structural differences between these two antagonists translate into different binding and functional characteristics. To study the binding of infliximab and etanercept to both the soluble and cell-surface transmembrane forms of TNF, a variety of in vitro binding and cell-based assays were performed. Binding assays using (125)I-labeled TNF showed that infliximab binds to both monomer and trimer forms of soluble TNF (sTNF), whereas etanercept binding is restricted to the trimer form. Infliximab formed stable complexes with sTNF, whereas etanercept formed relatively unstable complexes, resulting in release of dissociated TNF. KYM-1D4 cell killing assays and human umbilical vein endothelial cell activation assays demonstrated that TNF that had dissociated from etanercept was bioactive. Infliximab also formed more stable complexes with the transmembrane form of TNF expressed on transfected cells relative to analogous complexes formed with etanercept. Additionally, more infliximab molecules bound to the transmembrane TNF with higher avidity than etanercept. Although both infliximab and etanercept inhibited transmembrane TNF-mediated activation of human endothelial cells, infliximab was significantly more effective. The differences between infliximab and etanercept in their TNF binding characteristics may help explain their differential efficacy in CD and psoriasis clinical trials.

[1]  P. Mease,et al.  Etanercept in the treatment of psoriatic arthritis and psoriasis: a randomised trial , 2000, The Lancet.

[2]  U. Chaudhari,et al.  Efficacy and safety of infliximab monotherapy for plaque-type psoriasis: a randomised trial , 2001, The Lancet.

[3]  R N Maini,et al.  Infliximab and methotrexate in the treatment of rheumatoid arthritis. Anti-Tumor Necrosis Factor Trial in Rheumatoid Arthritis with Concomitant Therapy Study Group. , 2000, The New England journal of medicine.

[4]  R. Gentz,et al.  Evolution of collagen arthritis in mice is arrested by treatment with anti-tumour necrosis factor (TNF) antibody or a recombinant soluble TNF receptor. , 1992, Immunology.

[5]  L. Gooding,et al.  A nonsecretable cell surface mutant of tumor necrosis factor (TNF) kills by cell-to-cell contact , 1990, Cell.

[6]  J. Kremer,et al.  A trial of etanercept, a recombinant tumor necrosis factor receptor:Fc fusion protein, in patients with rheumatoid arthritis receiving methotrexate. , 1999, The New England journal of medicine.

[7]  R. Cotran,et al.  Identification of an inducible endothelial-leukocyte adhesion molecule. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[8]  S. Opal,et al.  Treatment of septic shock with the tumor necrosis factor receptor:Fc fusion protein. The Soluble TNF Receptor Sepsis Study Group. , 1996, The New England journal of medicine.

[9]  D. Kioussis,et al.  Transgenic mice expressing human tumour necrosis factor: a predictive genetic model of arthritis. , 1991, The EMBO journal.

[10]  P. Lipsky,et al.  Infliximab (chimeric anti-tumour necrosis factor α monoclonal antibody) versus placebo in rheumatoid arthritis patients receiving concomitant methotrexate: a randomised phase III trial , 1999, The Lancet.

[11]  C A Smith,et al.  Soluble tumor necrosis factor (TNF) receptors are effective therapeutic agents in lethal endotoxemia and function simultaneously as both TNF carriers and TNF antagonists. , 1993, Journal of immunology.

[12]  B. Beutler,et al.  The tumor necrosis factor ligand and receptor families. , 1996, The New England journal of medicine.

[13]  B. Echtenacher,et al.  Requirement of endogenous tumor necrosis factor/cachectin for recovery from experimental peritonitis. , 1990, Journal of immunology.

[14]  A. Meager A cytotoxicity assay for tumour necrosis using a human rhabdomyosarcoma cell line , 1991 .

[15]  Joseph Keane,et al.  Tuberculosis associated with infliximab, a tumor necrosis factor alpha-neutralizing agent , 2001 .

[16]  J. Naismith,et al.  TNFα and the TNF receptor superfamily: Structure‐function relationship(s) , 2000, Microscopy research and technique.

[17]  H. Loetscher,et al.  Protective effect of 55- but not 75-kD soluble tumor necrosis factor receptor-immunoglobulin G fusion proteins in an animal model of gram- negative sepsis , 1994, The Journal of experimental medicine.

[18]  B. Scallon,et al.  TNF receptor fusion proteins are effective inhibitors of TNF-mediated cytotoxicity on human KYM-1D4 rhabdomyosarcoma cells. , 1994, Cytokine.

[19]  D. Banner,et al.  Crystal structure of the soluble human 55 kd TNF receptor-human TNFβ complex: Implications for TNF receptor activation , 1993, Cell.

[20]  S. Targan,et al.  An engineered human antibody to TNF (CDP571) for active Crohn's disease: a randomized double-blind placebo-controlled trial. , 2001, Gastroenterology.

[21]  C. Smith,et al.  A receptor for tumor necrosis factor defines an unusual family of cellular and viral proteins. , 1990, Science.

[22]  J. Richert,et al.  Demyelination occurring during anti-tumor necrosis factor alpha therapy for inflammatory arthritides. , 2001, Arthritis and rheumatism.

[23]  G. Wong,et al.  Molecular cloning and expression of a receptor for human tumor necrosis factor , 1990, Cell.

[24]  G. Kollias,et al.  Impaired on/off regulation of TNF biosynthesis in mice lacking TNF AU-rich elements: implications for joint and gut-associated immunopathologies. , 1999, Immunity.

[25]  Alcocer‐Varela,et al.  Interleukin‐8, Interleukin‐10, Intercellular Adhesion Molecule‐1 and Vascular Cell Adhesion Molecule‐1 Expression Levels are Higher in Synovial Tissue from Patients with Rheumatoid Arthritis than in Osteoarthritis , 1999, Scandinavian journal of immunology.

[26]  E. Tindall,et al.  Treatment of rheumatoid arthritis with a recombinant human tumor necrosis factor receptor (p75)-Fc fusion protein. , 1997, The New England journal of medicine.

[27]  Richard W. Martin,et al.  A comparison of etanercept and methotrexate in patients with early rheumatoid arthritis. , 2000, The New England journal of medicine.

[28]  G. Kollias,et al.  Transmembrane TNF is sufficient to induce localized tissue toxicity and chronic inflammatory arthritis in transgenic mice. , 1996, Journal of inflammation.

[29]  Samir A. Shah,et al.  Both the lymphotoxin and tumor necrosis factor pathways are involved in experimental murine models of colitis. , 1998, Gastroenterology.

[30]  M. Feldmann,et al.  INHIBITORY EFFECT OF TNFα ANTIBODIES ON SYNOVIAL CELL INTERLEUKIN-1 PRODUCTION IN RHEUMATOID ARTHRITIS , 1989, The Lancet.

[31]  G. Kollias,et al.  The mouse/human chimeric monoclonal antibody cA2 neutralizes TNF in vitro and protects transgenic mice from cachexia and TNF lethality in vivo. , 1995, Cytokine.

[32]  B. Scallon,et al.  Chimeric anti-TNF-α monoclonal antibody cA2 binds recombinant transmembrane TNF-α and activates immune effector functions , 1995 .

[33]  M. Feldmann,et al.  Anti-tumor necrosis factor ameliorates joint disease in murine collagen-induced arthritis. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[34]  S. Targan,et al.  A Short-Term Study of Chimeric Monoclonal Antibody cA2 to Tumor Necrosis Factor α for Crohn's Disease , 1997 .

[35]  R. Jordan,et al.  Effects of 2 different anti-tumor necrosis factor-alpha agents in a primate model of subcutaneous abscess formation. , 2002, The Journal of infectious diseases.

[36]  A. Corti,et al.  Oligomeric tumour necrosis factor α slowly converts into inactive forms at bioactive levels , 1992 .

[37]  B. Scallon,et al.  Construction and initial characterization of a mouse-human chimeric anti-TNF antibody. , 1993, Molecular immunology.

[38]  A. Zinsmeister,et al.  Etanercept for active Crohn's disease: a randomized, double-blind, placebo-controlled trial. , 2001, Gastroenterology.

[39]  A. Meager,et al.  Cytokines in synovial fluid: II. The presence of tumour necrosis factor and interferon. , 1988, Clinical and experimental immunology.