Mechanisms of action of antithymocyte globulin: T-cell depletion and beyond

The success of allogeneic stem cell transplantation and solid-organ transplantation owes much to improvements in the immunosuppressive regimens that prevent graft-versus-host disease (GVHD) or suppress allograft rejection. A better understanding of the immune mechanisms underlying induction of immunological tolerance is the key to successful transplantation. Polyclonal antibodies such as antithymocyte globulins (ATG) have been used for decades. The common belief is that ATG efficacy relies on its capacity to deplete T lymphocytes. The aim of this review is to offer an overview of the recent findings that have been demonstrated in ATG's immunomodulatory activity. The polyclonal nature of ATG is reflected in its diverse effects on the immune system: (1) T-cell depletion in blood and peripheral lymphoid tissues through complement-dependent lysis and T-cell activation and apoptosis; (2) modulation of key cell surface molecules that mediate leukocyte/endothelium interactions; (3) induction of apoptosis in B-cell lineages; (4) interference with dendritic cell functional properties; and (5) induction of regulatory T and natural killer T cells. As a consequence, ATG provides multifaceted immunomodulation paving the way for future applications and suggesting that the use of ATG should be included in the immunosuppression therapeutic armamentarium to help reduce the incidence of organ rejection and GVHD.

[1]  M. Sayegh,et al.  A novel mechanism of action for anti-thymocyte globulin: induction of CD4+CD25+Foxp3+ regulatory T cells. , 2006, Journal of the American Society of Nephrology : JASN.

[2]  D. Brennan Functional Antibodies to Leukocyte Adhesion Molecules in Antithymocyte Globulins. , 2003 .

[3]  D. Blaise,et al.  Graft-versus-host disease following allogeneic transplantation from HLA-identical sibling with antithymocyte globulin-based reduced-intensity preparative regimen. , 2003, Blood.

[4]  Michel C Nussenzweig,et al.  Tolerogenic dendritic cells. , 2003, Annual review of immunology.

[5]  N. Kröger,et al.  Antithymocyte globulin induces ex vivo and in vivo depletion of myeloid and plasmacytoid dendritic cells. , 2005, Transplantation.

[6]  E. Bielek,et al.  CD32‐Mediated Platelet Aggregation In Vitro by Anti‐Thymocyte Globulin: Implication of Therapy‐Induced In Vivo Thrombocytopenia , 2003, American journal of transplantation : official journal of the American Society of Transplantation and the American Society of Transplant Surgeons.

[7]  N. Young,et al.  Biological and immunological characterization of ATG and ALG , 1986 .

[8]  R. Conte,et al.  Detection of a novel specificity (CTLA-4) in ATG/TMG globulins and sera from ATG-treated leukemic patients1 , 2002, Transplantation.

[9]  J. Revillard,et al.  Mechanisms of immunosuppression induced by antithymocyte globulins and OKT3. , 1996, The Journal of heart and lung transplantation : the official publication of the International Society for Heart Transplantation.

[10]  A. Beiras-Fernandez,et al.  In Vivo Visualization of the Effect of Polyclonal Antithymocyte Globulins on the Microcirculation after Ischemia/Reperfusion in a Primate Model , 2006, Transplantation.

[11]  H. Hirai,et al.  Human CD4+ CD25+ regulatory T cells suppress NKT cell functions. , 2003, Cancer research.

[12]  C. Figdor,et al.  Activation and increased expression of adhesion molecules on peripheral blood lymphocytes is a mechanism for the immediate lymphocytopenia after administration of OKT3. , 1996, Blood.

[13]  H. Lange,et al.  Detection of renal allograft rejection by complement components C5A and TCC in plasma and urine. , 1997, The Journal of laboratory and clinical medicine.

[14]  S. Lonial,et al.  Pharmacokinetics and pharmacodynamics of anti-thymocyte globulin in recipients of partially HLA-matched blood hematopoietic progenitor cell transplantation. , 2003, Biology of blood and marrow transplantation : journal of the American Society for Blood and Marrow Transplantation.

[15]  N. Kröger,et al.  Antithymocyte globulin induces complement-dependent cell lysis and caspase-dependent apoptosis in myeloma cells. , 2005, Experimental hematology.

[16]  T. Howard,et al.  Short course induction immunosuppression with thymoglobulin for renal transplant recipients. , 2002, Transplantation.

[17]  L. Genestier,et al.  TNFα and CD95-L contribute to apoptosis of activated lymphocytes triggered by ATGs , 1999 .

[18]  D. Rigal,et al.  Rabbit Antithymocyte Globulin Inhibits Monocyte-Derived Dendritic Cells Maturation In Vitro and Polarizes Monocyte-Derived Dendritic Cells Towards Tolerogenic Dendritic Cells Expressing Indoleamine 2,3-dioxygenase , 2006, Transplantation.

[19]  P. Huie,et al.  Predominance of NK1.1+TCRαβ+ or DX5+TCRαβ+ T Cells in Mice Conditioned with Fractionated Lymphoid Irradiation Protects Against Graft-Versus-Host Disease: “Natural Suppressor” Cells1 , 2001, The Journal of Immunology.

[20]  J. Thomas,et al.  A comprehensive definition of the major antibody specificities in polyclonal rabbit antithymocyte globulin. , 1994, Transplantation.

[21]  B. Hendry,et al.  The pharmacokinetics of anti-thymocyte globulin (ATG) following intravenous infusion in man. , 1996, Clinical nephrology.

[22]  F. Sallusto,et al.  Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/macrophage colony-stimulating factor plus interleukin 4 and downregulated by tumor necrosis factor alpha , 1994, The Journal of experimental medicine.

[23]  J. Revillard,et al.  MECHANISMS INVOLVED IN ANTITHYMOCYTE GLOBULIN IMMUNOSUPPRESSIVE ACTIVITY IN A NONHUMAN PRIMATE MODEL 1 , 2001, Transplantation.

[24]  M. Zand,et al.  Apoptosis and complement-mediated lysis of myeloma cells by polyclonal rabbit antithymocyte globulin. , 2006, Blood.

[25]  J. Revillard,et al.  A quantitative flow cytometry assay for the preclinical testing and pharmacological monitoring of rabbit antilymphocyte globulins (rATG). , 2000, Journal of immunological methods.

[26]  J. Myśliwska,et al.  CD4+CD25+ T regulatory cells inhibit cytotoxic activity of T CD8+ and NK lymphocytes in the direct cell-to-cell interaction. , 2004, Clinical immunology.

[27]  R. Merion,et al.  Partial T-cell activation and anergy induction by polyclonal antithymocyte globulin. , 1998, Transplantation.

[28]  L. Genestier,et al.  Functional antibodies to leukocyte adhesion molecules in antithymocyte globulins1 , 2003, Transplantation.

[29]  T. Laufer,et al.  Major Histocompatibility Complex Class II–Positive Cortical Epithelium Mediates the Selection of Cd4+25+ Immunoregulatory T Cells , 2001, The Journal of experimental medicine.

[30]  Yong‐jun Liu,et al.  IPC: professional type 1 interferon-producing cells and plasmacytoid dendritic cell precursors. , 2005, Annual review of immunology.

[31]  R. Steinman,et al.  Dendritic cells and the control of immunity , 1998, Nature.

[32]  E. Hauben,et al.  Regulatory T cells: prospective for clinical application in hematopoietic stem cell transplantation , 2005, Current opinion in hematology.

[33]  F. Powrie,et al.  IL-10 Is Required for Regulatory T Cells to Mediate Tolerance to Alloantigens In Vivo1 , 2001, The Journal of Immunology.

[34]  P. Huie,et al.  Predominance of NK1.1+TCR alpha beta+ or DX5+TCR alpha beta+ T cells in mice conditioned with fractionated lymphoid irradiation protects against graft-versus-host disease: "natural suppressor" cells. , 2001, Journal of immunology.

[35]  D. Brennan,et al.  Rabbit antithymocyte globulin versus basiliximab in renal transplantation. , 2006, The New England journal of medicine.

[36]  E. Holler,et al.  Isolation of CD4+CD25+ regulatory T cells for clinical trials. , 2006, Biology of blood and marrow transplantation : journal of the American Society for Blood and Marrow Transplantation.

[37]  G. May,et al.  Short and long-term results after pretransplant high-dose single ATG-fresenius bolus in cadaveric kidney transplantation. , 1998, Transplantation proceedings.

[38]  A. Banham,et al.  Cutting Edge: Direct Suppression of B Cells by CD4+CD25+ Regulatory T Cells1 , 2005, The Journal of Immunology.

[39]  S. Strober,et al.  Host conditioning with total lymphoid irradiation and antithymocyte globulin prevents graft-versus-host disease: the role of CD1-reactive natural killer T cells. , 2003, Biology of blood and marrow transplantation : journal of the American Society for Blood and Marrow Transplantation.

[40]  Wanjun Chen Dendritic cells and (CD4+)CD25+ T regulatory cells: crosstalk between two professionals in immunity versus tolerance. , 2006, Frontiers in bioscience : a journal and virtual library.

[41]  H. Rabb,et al.  The role of adhesion molecules and T cells in ischemic renal injury , 2003, Current opinion in nephrology and hypertension.

[42]  L. Genestier,et al.  Induction of Fas (Apo-1, CD95)-mediated apoptosis of activated lymphocytes by polyclonal antithymocyte globulins. , 1998, Blood.

[43]  Y. Kooyk,et al.  DC-SIGN: escape mechanism for pathogens , 2003, Nature Reviews Immunology.

[44]  E. Yvon,et al.  Antigen-induced regulatory T cells. , 2004, Blood.

[45]  P. Greipp,et al.  Thymoglobulin targets multiple plasma cell antigens and has in vitro and in vivo activity in multiple myeloma , 2006, Leukemia.

[46]  C. June,et al.  CD4+CD25+ regulatory T-cell lines from human cord blood have functional and molecular properties of T-cell anergy. , 2004, Blood.

[47]  L. Genestier,et al.  TNF alpha and CD95-L contribute to apoptosis of activated lymphocytes triggered by ATGs. , 1999, Transplantation proceedings.

[48]  Andreas Radbruch,et al.  Activation of human NK cells by plasmacytoid dendritic cells and its modulation by CD4+ T helper cells and CD4+ CD25hi T regulatory cells , 2005, European journal of immunology.

[49]  M. Garcia-Ojeda,et al.  Bone Marrow NK1.1− and NK1.1+ T Cells Reciprocally Regulate Acute Graft versus Host Disease , 1999, The Journal of experimental medicine.

[50]  M. Zand,et al.  Polyclonal Rabbit Antithymocyte Globulin Triggers B-Cell and Plasma Cell Apoptosis by Multiple Pathways , 2005, Transplantation.

[51]  A. Rudensky,et al.  Foxp3 programs the development and function of CD4+CD25+ regulatory T cells , 2003, Nature Immunology.

[52]  P. Hoffmann,et al.  Suppression of graft-versus-host disease by naturally occurring regulatory T cells. , 2004, Transplantation.

[53]  F. Delmonico,et al.  A prospective, randomized, clinical trial of intraoperative versus postoperative thymoglobulin in adult cadaveric renal transplant recipients1 , 2003, Transplantation.

[54]  C. Vincent,et al.  Antibodies against functional leukocyte surface molecules in polyclonal antilymphocyte and antithymocyte globulins. , 1991, Transplantation.

[55]  P. Allavena,et al.  Effects of anti-lymphocytes and anti-thymocytes globulin on human dendritic cells. , 2003, International immunopharmacology.

[56]  M. Zand,et al.  TREATMENT OF C4D-POSITIVE ACUTE HUMORAL REJECTION WITH PLASMAPHERESIS AND RABBIT POLYCLONAL ANTITHYMOCYTE GLOBULIN , 2004, Transplantation.

[57]  M. Remberger,et al.  Rabbit-immunoglobulin G levels in patients receiving thymoglobulin as part of conditioning before unrelated donor stem cell transplantation. , 2005, Haematologica.

[58]  S. Fuggle,et al.  Cell adhesion molecules in clinical renal transplantation. , 1998, Transplantation.

[59]  R. Gress,et al.  Cells of Th2 cytokine phenotype prevent LPS-induced lethality during murine graft-versus-host reaction. Regulation of cytokines and CD8+ lymphoid engraftment. , 1994, Journal of immunology.

[60]  S. Sakaguchi Naturally arising CD4+ regulatory t cells for immunologic self-tolerance and negative control of immune responses. , 2004, Annual review of immunology.

[61]  C. Mackay,et al.  T-cell function and migration. Two sides of the same coin. , 2000, The New England journal of medicine.

[62]  W. Strober,et al.  Cell Contact–Dependent Immunosuppression by Cd4+Cd25+Regulatory T Cells Is Mediated by Cell Surface–Bound Transforming Growth Factor β , 2001, The Journal of experimental medicine.

[63]  D. M. Hamlin,et al.  COMPARATIVE POLYCLONAL ANTITHYMOCYTE GLOBULIN AND ANTILYMPHOCYTE/ANTILYMPHOBLAST GLOBULIN ANTI‐CD ANTIGEN ANALYSIS BY FLOW CYTOMETRY , 1995, Transplantation.

[64]  Akemi Sakamoto,et al.  CD25+CD4+ T cells contribute to the control of memory CD8+ T cells , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[65]  S. Kojima,et al.  Comparison of antibody specificities of four anti-thymocyte/anti-lymphocyte globulin products , 1995 .

[66]  D. Bloch,et al.  Protective conditioning for acute graft-versus-host disease. , 2005, The New England journal of medicine.

[67]  J. Bluestone Regulatory T-cell therapy: is it ready for the clinic? , 2005, Nature Reviews Immunology.