Primary vascularization of allografts governs their immunogenicity and susceptibility to tolerogenesis

J Immunol. 2013 Aug 15;191(4):1948-56. doi: 10.4049/jimmunol.1202092. Epub 2013 Jul 5.

Abstract

We investigated the influence of allograft primary vascularization on alloimmunity, rejection, and tolerance in mice. First, we showed that fully allogeneic primarily vascularized and conventional skin transplants were rejected at the same pace. Remarkably, however, short-term treatment of mice with anti-CD40L Abs achieved long-term survival of vascularized skin and cardiac transplants but not conventional skin grafts. Nonvascularized skin transplants triggered vigorous direct and indirect proinflammatory type 1 T cell responses (IL-2 and IFN-γ), whereas primarily vascularized skin allografts failed to trigger a significant indirect alloresponse. A similar lack of indirect alloreactivity was also observed after placement of different vascularized organ transplants, including hearts and kidneys, whereas hearts placed under the skin (nonvascularized) triggered potent indirect alloresponses. Altogether, these results suggest that primary vascularization of allografts is associated with a lack of indirect T cell alloreactivity. Finally, we show that long-term survival of vascularized skin allografts induced by anti-CD40L Abs was associated with a combined lack of indirect alloresponse and a shift of the direct alloresponse toward a type 2 cytokine (IL-4, IL-10)-secretion pattern but no activation/expansion of Foxp3(+) regulatory T cells. Therefore, primary vascularization of allografts governs their immunogenicity and tolerogenicity.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Allografts
  • Anastomosis, Surgical
  • Animals
  • Antibodies, Monoclonal / therapeutic use
  • CD4-Positive T-Lymphocytes / immunology
  • CD40 Ligand / antagonists & inhibitors
  • CD40 Ligand / immunology
  • Graft Enhancement, Immunologic
  • Graft Survival
  • Heart Transplantation
  • Interferon-gamma / metabolism
  • Lymphocyte Activation
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C3H
  • Mice, Inbred C57BL
  • Organ Specificity
  • Skin / blood supply*
  • Skin Transplantation*
  • Specific Pathogen-Free Organisms
  • T-Lymphocyte Subsets / immunology
  • T-Lymphocytes, Regulatory / immunology
  • Transplantation Tolerance / immunology*
  • Transplants / blood supply*

Substances

  • Antibodies, Monoclonal
  • CD40 Ligand
  • Interferon-gamma