Proteomic profiling of the weed feverfew, a neglected pollen allergen source

Feverfew (Parthenium hysterophorus), an invasive weed from the Asteraceae family, has been reported as allergen source. Despite its relevance, knowledge of allergens is restricted to a partial sequence of a hydroxyproline-rich glycoprotein. We aimed to obtain the entire sequence for recombinant production and characterize feverfew pollen using proteomics and immunological assays. Par h 1, a defensin-proline fusion allergen was obtained by cDNA cloning and recombinantly produced in E. coli. Using two complementary proteomic strategies, a total of 258 proteins were identified in feverfew pollen among those 47 proteins belonging to allergenic families. Feverfew sensitized patients’ sera from India revealed IgE reactivity with a pectate lyase, PR-1 protein and thioredoxin in immonoblot. In ELISA, recombinant Par h 1 was recognized by 60 and 40% of Austrian and Indian sera, respectively. Inhibition assays demonstrated the presence of IgE cross-reactive Par h 1, pectate lyase, lipid-transfer protein, profilin and polcalcin in feverfew pollen. This study reveals significant data on the allergenic composition of feverfew pollen and makes recombinant Par h 1 available for cross-reactivity studies. Feverfew might become a global player in weed pollen allergy and inclusion of standardized extracts in routine allergy diagnosis is suggested in exposed populations.

[1]  Richard J. Lavallee,et al.  Optimized fast and sensitive acquisition methods for shotgun proteomics on a quadrupole orbitrap mass spectrometer. , 2012, Journal of proteome research.

[2]  C. Srinivas,et al.  Parthenium the terminator: An update , 2012, Indian dermatology online journal.

[3]  Franky R. G. Terras,et al.  Plant Defensins: Novel Antimicrobial Peptides as Components of the Host Defense System , 1995, Plant physiology.

[4]  O. Prakash,et al.  Immediate hypersensitivity to Parthenium hysterophorus. II. Clinical studies on the prevalence of parthenium rhinitis , 1991, Clinical and experimental allergy : journal of the British Society for Allergy and Clinical Immunology.

[5]  Klapper,et al.  Cloning and Expression of Ragweed Allergen Amb a 6 , 1998, Scandinavian journal of immunology.

[6]  D. Delmer,et al.  Annual review of plant physiology and plant molecular biology , 1988 .

[7]  F. Aberger,et al.  Array‐based profiling of ragweed and mugwort pollen allergens , 2008, Allergy.

[8]  B. Saha,et al.  Search for Allergens from the Pollen Proteome of Sunflower (Helianthus annuus L.): A Major Sensitizer for Respiratory Allergy Patients , 2015, PloS one.

[9]  J. Kader.  LIPID-TRANSFER PROTEINS IN PLANTS. , 1996, Annual review of plant physiology and plant molecular biology.

[10]  S. Adkins,et al.  What do we really know about alien plant invasion? A review of the invasion mechanism of one of the world’s worst weeds , 2016, Planta.

[11]  C. Radauer,et al.  A New Allergen from Ragweed (Ambrosia artemisiifolia) with Homology to Art v 1 from Mugwort* , 2010, The Journal of Biological Chemistry.

[12]  A J Carlson,et al.  Frederick R. Rickles, MD, FACP, Appointed Executive Director of the Federation of American Societies for Experimental Biology , 2004, Journal of Investigative Medicine.

[13]  P. Moingeon,et al.  Identification of Novel Short Ragweed Pollen Allergens Using Combined Transcriptomic and Immunoproteomic Approaches , 2015, PloS one.

[14]  McFadyen Re,et al.  Parthenium weed and human health in Queensland. , 1995 .

[15]  Hiller Km,et al.  Cloning and expression of ragweed allergen Amb a 6. , 1998 .

[16]  M. Wallner,et al.  Pollen Allergens for Molecular Diagnosis , 2016, Current Allergy and Asthma Reports.

[17]  J. Asturias,et al.  Cloning, expression and characterization of mugwort pollen allergen Art v 2, a pathogenesis-related protein from family group 1. , 2007, Molecular immunology.

[18]  M. Ungerer,et al.  Transcriptome resources for the perennial sunflower Helianthus maximiliani obtained from ecologically divergent populations , 2014, Molecular ecology resources.

[19]  Seema Patel,et al.  Harmful and beneficial aspects of Parthenium hysterophorus: an update , 2011, 3 Biotech.

[20]  P. Briza,et al.  Art v 1, the major allergen of mugwort pollen, is a modular glycoprotein with a defensin‐like and a hydroxyproline‐rich domain , 2003, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[21]  B. Martin,et al.  Identification of a novel hydroxyproline-rich glycoprotein as the major allergen in Parthenium pollen. , 1996, The Journal of allergy and clinical immunology.

[22]  Manpreet Kaur,et al.  Effects and Management of Parthenium hysterophorus: A Weed of Global Significance , 2014, International scholarly research notices.

[23]  Douglas J. H. Olson,et al.  Compatibility of plant protein extraction methods with mass spectrometry for proteome analysis , 2009 .

[24]  P. Briza,et al.  Targeting the cysteine-stabilized fold of Art v 1 for immunotherapy of Artemisia pollen allergy. , 2010, Molecular immunology.

[25]  P. Briza,et al.  Isoform identification and characterization of Art v 3, the lipid-transfer protein of mugwort pollen. , 2009, Molecular immunology.

[26]  P. Briza,et al.  Molecular and Immunological Characterization of Profilin from Mugwort Pollen , 2002, Biological chemistry.

[27]  P. V. Rao,et al.  Immunochemical characterization of rapid and slowly released allergens from the pollen of Parthenium hysterophorus. , 1995, International archives of allergy and immunology.

[28]  P. Briza,et al.  Molecular and immunological characterization of novel weed pollen pan‐allergens , 2008, Allergy.

[29]  N. Khanna,et al.  Immunological Response to Parthenium hysterophorus in Indian Patients with Parthenium Sensitive Atopic Dermatitis , 2012, Immunological investigations.

[30]  P. Moingeon,et al.  Identification of the cysteine protease Amb a 11 as a novel major allergen from short ragweed. , 2015, The Journal of allergy and clinical immunology.

[31]  M. Fernández-Rivas,et al.  Lipid‐transfer proteins as potential plant panallergens: cross‐reactivity among proteins of Artemisia pollen, Castanea nut and Rosaceae fruits, with different IgE‐binding capacities , 2000, Clinical and experimental allergy : journal of the British Society for Allergy and Clinical Immunology.

[32]  O. Prakash,et al.  Standardization of pollen allergens of Parthenium hysterophoms and selection of an in‐house reference extract , 1993, Clinical and experimental allergy : journal of the British Society for Allergy and Clinical Immunology.

[33]  M. Mann,et al.  In-gel digestion for mass spectrometric characterization of proteins and proteomes , 2006, Nature Protocols.

[34]  B. Thiede,et al.  High Resolution Quantitative Proteomics of HeLa Cells Protein Species Using Stable Isotope Labeling with Amino Acids in Cell Culture(SILAC), Two-Dimensional Gel Electrophoresis(2DE) and Nano-Liquid Chromatograpohy Coupled to an LTQ-OrbitrapMass Spectrometer* , 2012, Molecular & Cellular Proteomics.

[35]  P. Briza,et al.  Pectate Lyase Pollen Allergens: Sensitization Profiles and Cross-Reactivity Pattern , 2015, PloS one.

[36]  W. Vensel,et al.  Proteome mapping of mature pollen of Arabidopsis thaliana , 2005, Proteomics.

[37]  A. Mari,et al.  The Role of Lipid Transfer Proteins in Allergic Diseases , 2010, Current allergy and asthma reports.

[38]  P. Sriramarao,et al.  Allergenic cross-reactivity between Parthenium and ragweed pollen allergens. , 1993, International archives of allergy and immunology.

[39]  R. McFadyen.  Parthenium weed and human health in Queensland. , 1995, Australian family physician.

[40]  Douglas J. H. Olson,et al.  Proteome profile and functional classification of proteins in Arabidopsis thaliana (Landsberg erecta) mature pollen , 2006, Sexual Plant Reproduction.

[41]  P. Briza,et al.  Humoral and Cellular Cross-Reactivity between Amb a 1, the Major Ragweed Pollen Allergen, and Its Mugwort Homolog Art v 6 , 2012, The Journal of Immunology.