Phenotypic complementation of genetic immunodeficiency by chronic herpesvirus infection

Elife. 2015 Jan 20:4:e04494. doi: 10.7554/eLife.04494.

Abstract

Variation in the presentation of hereditary immunodeficiencies may be explained by genetic or environmental factors. Patients with mutations in HOIL1 (RBCK1) present with amylopectinosis-associated myopathy with or without hyper-inflammation and immunodeficiency. We report that barrier-raised HOIL-1-deficient mice exhibit amylopectin-like deposits in the myocardium but show minimal signs of hyper-inflammation. However, they show immunodeficiency upon acute infection with Listeria monocytogenes, Toxoplasma gondii or Citrobacter rodentium. Increased susceptibility to Listeria was due to HOIL-1 function in hematopoietic cells and macrophages in production of protective cytokines. In contrast, HOIL-1-deficient mice showed enhanced control of chronic Mycobacterium tuberculosis or murine γ-herpesvirus 68 (MHV68), and these infections conferred a hyper-inflammatory phenotype. Surprisingly, chronic infection with MHV68 complemented the immunodeficiency of HOIL-1, IL-6, Caspase-1 and Caspase-1;Caspase-11-deficient mice following Listeria infection. Thus chronic herpesvirus infection generates signs of auto-inflammation and complements genetic immunodeficiency in mutant mice, highlighting the importance of accounting for the virome in genotype-phenotype studies.

Keywords: Listeria monocytogenes; NF-kappaB; immunodeficiency; immunology; infectious disease; linear ubiquitination; microbiology; mouse; murine gamma-herpesvirus 68.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Acute Disease
  • Animals
  • Bone Marrow Cells / cytology
  • Caspase 1 / metabolism
  • Cell Compartmentation
  • Chronic Disease
  • Citrobacter / physiology
  • Cytokines / biosynthesis
  • Genetic Complementation Test
  • Herpesviridae / physiology*
  • Herpesviridae Infections / immunology*
  • Herpesviridae Infections / pathology*
  • Herpesviridae Infections / virology
  • Humans
  • Immunity, Innate
  • Immunologic Deficiency Syndromes / genetics*
  • Immunologic Deficiency Syndromes / virology*
  • Inflammation / pathology
  • Inflammation Mediators / metabolism
  • Interleukin-6 / metabolism
  • Listeria monocytogenes / physiology
  • Listeriosis / immunology
  • Listeriosis / microbiology
  • Listeriosis / pathology
  • Macrophages / metabolism
  • Mice
  • Mice, Knockout
  • Mycobacterium tuberculosis / physiology
  • Phenotype
  • Rhadinovirus / physiology
  • Toxoplasma
  • Ubiquitin-Protein Ligases / genetics
  • Ubiquitin-Protein Ligases / metabolism

Substances

  • Cytokines
  • Inflammation Mediators
  • Interleukin-6
  • Ubiquitin-Protein Ligases
  • Caspase 1