Lymphocyte-independent pathways underlie the pathogenesis of murine cytomegalovirus-associated secondary haemophagocytic lymphohistiocytosis

Clin Exp Immunol. 2018 Apr;192(1):104-119. doi: 10.1111/cei.13084. Epub 2018 Jan 18.

Abstract

Haemophagocytic lymphohistiocytosis (HLH) constitutes a spectrum of immunological disorders characterized by uncontrolled immune activation and key symptoms such as fever, splenomegaly, pancytopenia, haemophagocytosis, hyperferritinaemia and hepatitis. In genetic or primary HLH, hyperactivated CD8+ T cells are the main drivers of pathology. However, in acquired secondary HLH, the role of lymphocytes remains vague. In the present study the involvement of lymphocytes in the pathogenesis of a cytomegalovirus-induced model of secondary HLH was explored. We have previously reported CD8+ T cells to be redundant in this model, and therefore focused on CD4+ helper and regulatory T cells. CD4+ T cells were activated markedly and skewed towards a proinflammatory T helper type 1 transcription profile in mice displaying a severe and complete HLH phenotype. Counter to expectations, regulatory T cells were not reduced in numbers and were, in fact, more activated. Therapeutic strategies targeting CD25high hyperactivated T cells were ineffective to alleviate disease, indicating that T cell hyperactivation is not a pathogenic factor in cytomegalovirus-induced murine HLH. Moreover, even though T cells were essential in controlling viral proliferation, CD4+ T cells, in addition to CD8+ T cells, were dispensable in the development of the HLH-like syndrome. In fact, no T or B cells were required for induction and propagation of HLH disease, as evidenced by the occurrence of cytomegalovirus-associated HLH in severe combined immunodeficient (SCID) mice. These data suggest that lymphocyte-independent mechanisms can underlie virus-associated secondary HLH, accentuating a clear distinction with primary HLH.

Keywords: T cells; haemophagocytic lymphohistiocytosis; macrophage activation syndrome; mouse cytomegalovirus; mouse model.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • CD4-Positive T-Lymphocytes / immunology*
  • Herpesviridae Infections / complications
  • Herpesviridae Infections / immunology*
  • Interferon-gamma / genetics
  • Lymphocyte Activation
  • Lymphocyte Depletion
  • Lymphohistiocytosis, Hemophagocytic / immunology*
  • Lymphohistiocytosis, Hemophagocytic / pathology*
  • Lymphohistiocytosis, Hemophagocytic / virology
  • Mice
  • Mice, Inbred BALB C
  • Mice, Knockout
  • Muromegalovirus
  • T-Lymphocytes, Regulatory / immunology*
  • Th1 Cells / immunology

Substances

  • Interferon-gamma