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Title: Pollen Lipidomics: Lipid Profiling Exposes a Notable Diversity in 22 Allergenic Pollen and Potential Biomarkers of the Allergic Immune Response

Abstract

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. 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, andmore » 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. 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.« less

Authors:
 [1];  [1];  [2];  [1];  [3]
+ Show Author Affiliations
  1. University of Chicago, IL (United States)
  2. University of Chicago, IL (United States); University of Arizona, Tucson, AZ (United States)
  3. University of Chicago, IL (United States); Chromatin, Inc., Chicago, IL (United States)
Publication Date:
Research Org.:
University of Chicago, IL (United States)
Sponsoring Org.:
USDOE Office of Science (SC); Strategic Program for Asthma Research; National Science Foundation (NSF); McHugh Otolaryngology Research Fund
OSTI Identifier:
1904580
Grant/Contract Number:  
FG02-96ER20240; MCB-0520283
Resource Type:
Accepted Manuscript
Journal Name:
PLoS ONE
Additional Journal Information:
Journal Volume: 8; Journal Issue: 2; Journal ID: ISSN 1932-6203
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; pollen; lipids; allergies; immune response; cytokines; gas chromatography-mass spectrometry; lipid analysis; inflammation

Citation Formats

Bashir, Mohamed H., Lui, Jan Hsi, Palnivelu, Ravishankar, Naclerio, Robert M., and Preuss, Daphne. Pollen Lipidomics: Lipid Profiling Exposes a Notable Diversity in 22 Allergenic Pollen and Potential Biomarkers of the Allergic Immune Response. United States: N. p., 2013. Web. doi:10.1371/journal.pone.0057566.
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Bashir, Mohamed H., Lui, Jan Hsi, Palnivelu, Ravishankar, Naclerio, Robert M., & Preuss, Daphne. Pollen Lipidomics: Lipid Profiling Exposes a Notable Diversity in 22 Allergenic Pollen and Potential Biomarkers of the Allergic Immune Response. United States. https://doi.org/10.1371/journal.pone.0057566
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Bashir, Mohamed H., Lui, Jan Hsi, Palnivelu, Ravishankar, Naclerio, Robert M., and Preuss, Daphne. Thu . "Pollen Lipidomics: Lipid Profiling Exposes a Notable Diversity in 22 Allergenic Pollen and Potential Biomarkers of the Allergic Immune Response". United States. https://doi.org/10.1371/journal.pone.0057566. https://www.osti.gov/servlets/purl/1904580.
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@article{osti_1904580,
title = {Pollen Lipidomics: Lipid Profiling Exposes a Notable Diversity in 22 Allergenic Pollen and Potential Biomarkers of the Allergic Immune Response},
author = {Bashir, Mohamed H. and Lui, Jan Hsi and Palnivelu, Ravishankar and Naclerio, Robert M. and Preuss, Daphne},
abstractNote = {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. 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. 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.},
doi = {10.1371/journal.pone.0057566},
journal = {PLoS ONE},
number = 2,
volume = 8,
place = {United States},
year = {Thu Feb 28 00:00:00 EST 2013},
month = {Thu Feb 28 00:00:00 EST 2013}
}
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https://doi.org/10.1371/journal.pone.0057566
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The Effects of Temperature and Oleic Acid on Murine Memory and Virgin T Cell Activation: Interleukin-2 Secretion and Interleukin-2 Receptor Expression
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  • DOI: 10.1006/cimm.1993.1265

Behavior of storage lipids during development and germination of olive (Olea europaea L.) pollen
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Palmitic acid induces IP-10 expression in human macrophages via NF-κB activation
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  • DOI: 10.1016/j.bbrc.2007.04.092

Autoimmunity induced by adjuvant hydrocarbon oil components of vaccine
journal, June 2004

Gas-particle concentration and distribution of n-alkanes and polycyclic aromatic hydrocarbons in the atmosphere of Prato (Italy)
journal, June 2007

Activation of PPARγ Specifies a Dendritic Cell Subtype Capable of Enhanced Induction of iNKT Cell Expansion
journal, July 2004

Recognition of pollen-derived phosphatidyl-ethanolamine by human CD1d-restricted γδ T cells
journal, May 2006

  • Russano, Anna M.; Agea, Elisabetta; Corazzi, Lanfranco
  • Journal of Allergy and Clinical Immunology, Vol. 117, Issue 5
  • DOI: 10.1016/j.jaci.2006.01.001

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Lipids are required for directional pollen-tube growth
journal, April 1998

  • Wolters-Arts, Mieke; Lush, W. Mary; Mariani, Celestina
  • Nature, Vol. 392, Issue 6678
  • DOI: 10.1038/33929

Rapid initiation of Arabidopsis pollination requires the oleosin-domain protein GRP17
journal, January 2000

  • Mayfield, Jacob A.; Preuss, Daphne
  • Nature Cell Biology, Vol. 2, Issue 2
  • DOI: 10.1038/35000084

Regulation of immunity by self-reactive T cells
journal, June 2005

  • Kronenberg, Mitchell; Rudensky, Alexander
  • Nature, Vol. 435, Issue 7042
  • DOI: 10.1038/nature03725

PPARG Locus Haplotype Variation and Exacerbations in Asthma
journal, February 2007

  • Palmer, C. N. A.; Doney, A. S. F.; Ismail, T.
  • Clinical Pharmacology & Therapeutics, Vol. 81, Issue 5
  • DOI: 10.1038/sj.clpt.6100119

Intra- and extracellular lipid composition and associated gene expression patterns during pollen development in Brassica napus
journal, March 1997

Constituents of the tapetosomes and elaioplasts inBrassica campestristapetum and their degradation and retention during microsporogenesis
journal, December 1998

Biological And Health Effects Of Exposure To Kerosene-Based Jet Fuels And Performance Additives
journal, January 2003

  • Ritchie, Glenn; Still, Kenneth; Rossi III, John
  • Journal of Toxicology and Environmental Health, Part B, Vol. 6, Issue 4
  • DOI: 10.1080/10937400306473

Positive selection of mouse NK1+ T cells by CD1-expressing cortical thymocytes.
journal, December 1995

Palmitate Activates the NF-κB Transcription Factor and Induces IL-6 and TNFα Expression in 3T3-L1 Adipocytes
journal, August 2005

  • Ajuwon, Kolapo M.; Spurlock, Michel E.
  • The Journal of Nutrition, Vol. 135, Issue 8
  • DOI: 10.1093/jn/135.8.1841

Nutrients, Nuclear Receptors, Inflammation, Immunity Lipids, PPAR, and Allergic Asthma
journal, March 2006

  • August, Avery; Mueller, Cynthia; Weaver, Veronika
  • The Journal of Nutrition, Vol. 136, Issue 3
  • DOI: 10.1093/jn/136.3.695

Human maximization test of falcarinol, the principal contact allergen of English ivy and Algerian ivy (Hedera helix, H. canariensis)
journal, August 1988

Gene Families from the Arabidopsis thaliana Pollen Coat Proteome
journal, June 2001

  • Mayfield, Jacob A.; Fiebig, Aretha; Johnstone, Sarah E.
  • Science, Vol. 292, Issue 5526
  • DOI: 10.1126/science.1060972

Links between Pollen, Atopy and the Asthma Epidemic
journal, January 2007

  • Taylor, Philip E.; Jacobson, Kraig W.; House, James M.
  • International Archives of Allergy and Immunology, Vol. 144, Issue 2
  • DOI: 10.1159/000103230

Adjuvanticity and Inflammatory Response Following Administration of Water-in-Oil Emulsions Prepared with Saturated Hydrocarbons in Chickens.
journal, January 2000

  • Fukanoki, Shin-ichi; Matsumoto, Kohei; Mori, Hajime
  • Journal of Veterinary Medical Science, Vol. 62, Issue 8
  • DOI: 10.1292/jvms.62.917

Treating Moderate-to-Severe Allergic Asthma with a Recombinant Humanized Anti-IgE Monoclonal Antibody (Omalizumab)
journal, January 2006

Transcription Factors in Asthma: Are Transcription Factors a New Target for Asthma Therapy?
journal, May 2006

Genetic Evidence for a Long-Range Activity That Directs Pollen Tube Guidance in Arabidopsis
journal, January 1995

  • Hulskamp, Martin; Schneitz, Kay; Pruitt, Robert E.
  • The Plant Cell, Vol. 7, Issue 1
  • DOI: 10.2307/3869837

The burden of allergic rhinitis
journal, January 2007

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