Induction of TGF-beta 1, not regulatory T cells, impairs antiviral immunity in the lung following bone marrow transplant

J Immunol. 2010 May 1;184(9):5130-40. doi: 10.4049/jimmunol.0901871. Epub 2010 Mar 26.

Abstract

Patients receiving hematopoietic stem cell transplantation or bone marrow transplantation (BMT) as therapy for various malignancies or autoimmune diseases have an increased risk for infectious complications posttransplant, especially in the lung. We have used BMT in mice and murine gammaherpesvirus, gammaHV-68, to study the efficacy of adaptive immune responses post-BMT. Five weeks posttransplant, mice have fully reconstituted their hematopoietic lineages in both the lung and periphery. When challenged with virus, however, BMT mice have a reduced ability to clear lytic virus from the lung. Defective viral control in BMT mice is not related to impaired leukocyte recruitment or defective APC function. Rather, BMT mice are characterized by defective CD4 cell proliferation, skewing of effector CD4 T cells from a Th1 to a Th17 phenotype, and an immunosuppressive lung environment at the time of infection that includes overexpression of TGF-beta1 and PGE(2) and increased numbers of regulatory T cells. Neither indomethacin treatment to block PG synthesis nor anti-CD25 depletion of regulatory T cells improved antiviral host defense post-BMT. Transplanting mice with transgenic bone marrow expressing a dominant-negative TGF-betaRII under the permissive CD4 promoter created mice in which effector CD4 and CD8 cells were unresponsive to TGF-beta1. Mice with TGF-beta1-nonresponsive effector T cells had restored antiviral immunity and improved Th1 responses post-BMT. Thus, our results indicate that overexpression of TGF-beta1 following myeloablative conditioning post-BMT results in impaired effector T cell responses to viral infection.

Publication types

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

MeSH terms

  • Animals
  • Bone Marrow Transplantation / adverse effects
  • Bone Marrow Transplantation / immunology*
  • Cell Differentiation / immunology
  • Cell Proliferation
  • Growth Inhibitors / adverse effects
  • Growth Inhibitors / biosynthesis
  • Growth Inhibitors / genetics
  • Herpesviridae Infections / immunology*
  • Herpesviridae Infections / therapy
  • Herpesviridae Infections / virology
  • Interleukin-17 / biosynthesis
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C3H
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Pneumonia, Viral / immunology*
  • Pneumonia, Viral / therapy
  • Pneumonia, Viral / virology
  • Protein Serine-Threonine Kinases / administration & dosage
  • Protein Serine-Threonine Kinases / therapeutic use
  • Receptor, Transforming Growth Factor-beta Type II
  • Receptors, Transforming Growth Factor beta / administration & dosage
  • Receptors, Transforming Growth Factor beta / therapeutic use
  • Rhadinovirus / immunology*
  • T-Lymphocytes, Regulatory / immunology*
  • T-Lymphocytes, Regulatory / pathology
  • T-Lymphocytes, Regulatory / virology
  • Th1 Cells / immunology
  • Th1 Cells / pathology
  • Th1 Cells / virology
  • Transforming Growth Factor beta1 / adverse effects*
  • Transforming Growth Factor beta1 / biosynthesis*
  • Transforming Growth Factor beta1 / genetics
  • Transplantation Conditioning / methods
  • Tumor Virus Infections / immunology*
  • Tumor Virus Infections / therapy
  • Tumor Virus Infections / virology

Substances

  • Growth Inhibitors
  • Interleukin-17
  • Receptors, Transforming Growth Factor beta
  • Transforming Growth Factor beta1
  • Protein Serine-Threonine Kinases
  • Receptor, Transforming Growth Factor-beta Type II