Modified High-Molecular-Weight Hyaluronan Promotes Allergen-Specific Immune Tolerance

Am J Respir Cell Mol Biol. 2017 Jan;56(1):109-120. doi: 10.1165/rcmb.2016-0111OC.

Abstract

The extracellular matrix in asthmatic lungs contains abundant low-molecular-weight hyaluronan, and this is known to promote antigen presentation and allergic responses. Conversely, high-molecular-weight hyaluronan (HMW-HA), typical of uninflamed tissues, is known to suppress inflammation. We investigated whether HMW-HA can be adapted to promote tolerance to airway allergens. HMW-HA was thiolated to prevent its catabolism and was tethered to allergens via thiol linkages. This platform, which we call "XHA," delivers antigenic payloads in the context of antiinflammatory costimulation. Allergen/XHA was administered intranasally to mice that had been sensitized previously to these allergens. XHA prevents allergic airway inflammation in mice sensitized previously to either ovalbumin or cockroach proteins. Allergen/XHA treatment reduced inflammatory cell counts, airway hyperresponsiveness, allergen-specific IgE, and T helper type 2 cell cytokine production in comparison with allergen alone. These effects were allergen specific and IL-10 dependent. They were durable for weeks after the last challenge, providing a substantial advantage over the current desensitization protocols. Mechanistically, XHA promoted CD44-dependent inhibition of nuclear factor-κB signaling, diminished dendritic cell maturation, and reduced the induction of allergen-specific CD4 T-helper responses. XHA and other potential strategies that target CD44 are promising alternatives for the treatment of asthma and allergic sinusitis.

Keywords: T cell; allergy; dendritic cell; hyaluronan; tolerance.

Publication types

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

MeSH terms

  • Allergens / immunology*
  • Animals
  • Anti-Inflammatory Agents / pharmacology
  • Bone Marrow Cells / cytology
  • Cell Differentiation / drug effects
  • Cell Nucleus / drug effects
  • Cell Nucleus / metabolism
  • Cell Proliferation / drug effects
  • Cross-Linking Reagents / metabolism
  • Dendritic Cells / drug effects
  • Hyaluronan Receptors / metabolism
  • Hyaluronic Acid / chemistry*
  • Hyaluronic Acid / pharmacology*
  • Immune Tolerance / drug effects*
  • Immunization
  • Interleukin-10
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Molecular Weight
  • NF-kappa B / metabolism
  • Pneumonia / immunology
  • Pneumonia / pathology
  • Pneumonia / physiopathology
  • Protein Transport / drug effects
  • Sulfhydryl Compounds / metabolism

Substances

  • Allergens
  • Anti-Inflammatory Agents
  • Cross-Linking Reagents
  • Hyaluronan Receptors
  • NF-kappa B
  • Sulfhydryl Compounds
  • Interleukin-10
  • Hyaluronic Acid