Crystal structure and immunologic characterization of the major grass pollen allergen Phl p 4

J Allergy Clin Immunol. 2013 Sep;132(3):696-703.e10. doi: 10.1016/j.jaci.2013.03.021. Epub 2013 May 14.

Abstract

Background: Phl p 4 is a major pollen allergen but exhibits lower allergenicity than other major allergens. The natural protein is glycosylated and shows cross-reactivity with related and structurally unrelated allergens.

Objective: We sought to determine the high-resolution crystal structure of Phl p 4 and to evaluate the immunologic properties of the recombinant allergen in comparison with natural Phl p 4.

Methods: Different isoallergens of Phl p 4 were expressed, and the nonglycosylated mutant was crystallized. The specific role of protein and carbohydrate epitopes for allergenicity was studied by using IgE inhibition and basophil release assays.

Results: The 3-dimensional structure was determined by using x-ray crystallography at a resolution of 1.9 Å. The allergen is a glucose dehydrogenase with a bicovalently attached flavin adenine dinucleotide. Glycosylated and nonglycosylated recombinant Phl p 4 showed identical inhibition of IgE binding, but compared with natural Phl p 4, all recombinant isoforms displayed a reduced IgE-binding inhibition. However, the recombinant protein exhibited an approximately 10-fold higher potency in basophil release assays than the natural protein.

Conclusion: The crystal structure reveals the compact globular nature of the protein, and the observed binding pocket implies the size of the natural substrate. Plant-derived cross-reactive carbohydrate determinants (CCDs) appear to reduce the allergenicity of the natural allergen, whereas the Pichia pastoris-derived glycosylation does not. Our results imply yet undescribed mechanism of how CCDs dampen the immune response, leading to a novel understanding of the role of CCDs.

Keywords: BBE; CCD; CD; Circular dichroism; Cross-reactive carbohydrate determinant; FAD; FSAS; Flavin adenine dinucleotide; Fractional solvent-accessible surfaces; GPA; Grass pollen allergen; Grass pollen allergy; Phl p 4; RMSD; Reticuline oxidase (informally known as the berberine bridge enzyme); Root-mean-square deviation; Sec c 4; basophil release assay; bicovalently attached flavin adenine dinucleotide; cross-reactive carbohydrate determinant; dehydrogenase; recombinant allergen.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 2,6-Dichloroindophenol / metabolism
  • Allergens / chemistry*
  • Allergens / immunology*
  • Allergens / metabolism
  • Amino Acid Sequence
  • Basophils / immunology
  • Glucose 1-Dehydrogenase / chemistry
  • Glucose 1-Dehydrogenase / immunology
  • Glucose 1-Dehydrogenase / metabolism
  • Immunoglobulin E / blood
  • Molecular Sequence Data
  • Phleum / immunology*
  • Plant Proteins / chemistry*
  • Plant Proteins / immunology*
  • Plant Proteins / metabolism
  • Pollen / chemistry
  • Pollen / immunology*
  • Protein Conformation
  • Recombinant Proteins / immunology

Substances

  • Allergens
  • Phl p 4 protein, Phleum pratense
  • Plant Proteins
  • Recombinant Proteins
  • Immunoglobulin E
  • 2,6-Dichloroindophenol
  • Glucose 1-Dehydrogenase