Pollen lipidomics: lipid profiling exposes a notable diversity in 22 allergenic pollen and potential biomarkers of the allergic immune response

PLoS One. 2013;8(2):e57566. doi: 10.1371/journal.pone.0057566. Epub 2013 Feb 28.

Abstract

Background/aim: Pollen grains are the male gametophytes that deliver sperm cells to female gametophytes during sexual reproduction of higher plants. Pollen is a major source of aeroallergens and environmental antigens. The pollen coat harbors a plethora of lipids that are required for pollen hydration, germination, and penetration of the stigma by pollen tubes. In addition to proteins, pollen displays a wide array of lipids that interact with the human immune system. Prior searches for pollen allergens have focused on the identification of intracellular allergenic proteins, but have largely overlooked much of the extracellular pollen matrix, a region where the majority of lipid molecules reside. Lipid antigens have attracted attention for their potent immunoregulatory effects. By being in close proximity to allergenic proteins on the pollen surface when they interact with host cells, lipids could modify the antigenic properties of proteins.

Methodology/principal findings: We performed a comparative pollen lipid profiling of 22 commonly allergenic plant species by the use of gas chromatography-mass spectroscopy, followed by detailed data mining and statistical analysis. Three experiments compared pollen lipid profiles. We built a database library of the pollen lipids by matching acquired pollen-lipid mass spectra and retention times with the NIST/EPA/NIH mass-spectral library. We detected, identified, and relatively quantified more than 106 lipid molecular species including fatty acids, n-alkanes, fatty alcohols, and sterols. Pollen-derived lipids stimulation up-regulate cytokines expression of dendritic and natural killer T cells co-culture.

Conclusions/significance: Here we report on a lipidomic analysis of pollen lipids that can serve as a database for identifying potential lipid antigens and/or novel candidate molecules involved in allergy. The database provides a resource that facilitates studies on the role of lipids in the immunopathogenesis of allergy. Pollen lipids vary greatly among allergenic species and contain many molecules that have stimulatory or regulatory effects on immune responses.

Publication types

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

MeSH terms

  • Allergens / immunology
  • Allergens / metabolism*
  • Biomarkers*
  • Flow Cytometry
  • Gas Chromatography-Mass Spectrometry
  • Humans
  • Hypersensitivity / immunology*
  • Killer Cells, Natural / immunology
  • Lipid Metabolism*
  • Lymphocyte Activation
  • Pollen / metabolism*
  • Principal Component Analysis

Substances

  • Allergens
  • Biomarkers

Grant support

This study was supported by the Strategic Program for Asthma Research (www.spar-aaf.org); National Science Foundation (http://www.nsf.gov/) “Arabidopsis 2010: Functional analysis of pollen exine assembly,” MCB-0520283; Department of Energy (http://energy.gov/) “Cell-Cell Interaction during Pollen Tube Guidance in Arabidopsis,” DE-FG02-96ER20240; The McHugh Otolaryngology Research Fund. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.