Abstract
We have previously reported the purification and preliminary X-ray characterization of a hemagglutinin from the seeds of Jatropha curcas and, with the detailed sequencing information available now, we find that it is similar to a 2S albumin allergen isolated from the same source. Through a search of Jatropha genome database (http://www.kazusa.or.jp/jatropha/), we map it to the sequence id JcCA0234191 (now referred to as Jcr4S00619.70 in the new version, release 4.5) which has a conserved alpha amylase inhibitor/seed storage protein domain found in the 2S albumin allergens. The putative sequence of the small and large chains of the protein is assigned and the total mass of the two subunits matches with the intact mass 10 kDa determined through MALDI. The protein retains hemagglutination activity between pH 6–9 and up to 60 °C on heat treatment and its hemagglutination activity is inhibited by sialic acid and fetuin. Bioinformatics studies show that the isolated protein sequence clusters in close association with a 2S albumin from Ricinus communis in phylogeny analysis and has a conservation of the characteristic four disulfide linkage pattern. Hemagglutinins and lectins are known to have allergenic effects through their interaction with immunoglobulin E and histamine release and earlier studies have shown that this interaction can be inhibited by lectin-specific sugars. We hope this report bridges the plant allergens and hemagglutinins further for exploring possible mediation of allergenic activity through sialic acid and complex sugar interactions and generates further interest in the area.
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Abbreviations
- nsLTP:
-
Non-specific lipid transfer protein
- AAI:
-
Alpha amylase inhibitor
- NeuNAc:
-
N-acetylneuraminic acid
- MIC:
-
Minimum inhibitory concentration
- DTT:
-
Dithiothreitol
- BME:
-
Beta mercaptoethanol
- RIP:
-
Ribosomal inactivating protein
- JHg:
-
Jatropha hemagglutinin
- SS:
-
Seed storage protein
- RBC:
-
Red blood cells
References
Breiteneder H, Clare Mills EN (2005) Plant food allergens—structural and functional aspects of allergenicity. Biotechnol Adv 23:395–399
Breiteneder H, Ebner C (2000) Molecular and biochemical classification of plant-derived food allergens. J Allergy Clin Immunol 106:27–36
Crouch ML, Tenbarge KM, Simon AE, Ferl R (1983) cDNA clones of Brassica napus seed storage proteins: evidence from nucleotide sequence analysis that both subunits of napin are cleaved from a precursor polypeptide. J Mol Appl Genet 2:273–283
Ericson ML, Rodln J, Lenman M, Glimellus K, Josefsson LG, Rask L (1986) Structure of the 1.7 S storage protein, napin and its precursor. J Biol Chem 261:14576–14581
Imberty A, Gautier C, Lescar J, Pérez S, Wyns L, Loris R (2000) An unusual carbohydrate binding site revealed by the structures of two Maackia amurensis lectins complexed with sialic acid-containing oligosaccharides. J Biol Chem 275:17541–17548
Jeanmougin F, Thompson JD, Gouy M, Higgins DG, Gibson TJ (1998) Multiple sequence alignment with Clustal X. Trends Biochem Sci 23:403–405
Kaku H, Kaneko H, Minamihara N, Iwata K, Jordan ET, Rojo MA, Minami-Ishii N, Minami E, Hisajima S, Shibuya N (2007) Elderberry bark lectins evolved to recognize Neu5Ac alpha2,6Gal/GalNAc sequence from a Gal/GalNAc binding lectin through the substitution of amino-acid residues critical for the binding to sialic acid. J Biochem 142:393–401
Lehman F, Tiralongo E, Tiralongo J (2006) Sialic acid specific lectins: occurence, specificity and function. Cell Mol Life Sci 63:1331–1354
Li CY, Devappa RK, Liu JX, Lv JM, Makkar HPS, Becker K (2010) Toxicity of Jatropha curcas phorbol esters in mice. Food Chem Toxicol 48:620–625
Maciel FM, Laberty MA, Oliveira ND, Felix SP, Soares AM, Verícimo MA, Machado OL (2009) A new 2S albumin from Jatropha curcas L. seeds and assessment of its allergenic properties. Peptides 30:2103–2107
Martin DC, Anna P, Heimo B, Fatima F (2007) Nomenclature and structural biology of allergens. J Allergy Clin Immunol 119:414–420
Moreno FJ, Clemente A (2008) 2S albumin storage proteins: what makes them food allergens? Open Biochem J 2:16–28
Müthing J, Meisen I, Bulau P, Langer M, Witthohn K, Lentzen H, Neumann U, Peter-Katalinić J (2004) Mistletoe lectin I is a sialic acid-specific lectin with strict preference to gangliosides and glycoproteins with terminal Neu5Ac alpha 2–6Gal beta 1–4GlcNAc residues. Biochemistry 43:2996–3007
Nair DN, Suresh CG, Singh DD (2011) Purification, crystallization and preliminary X-ray characterization of a hemagglutinin from the seeds of Jatropha curcas. Acta Crystallogr, Sect F: Struct Biol Cryst Commun 67:1534–1536
Oda Y, Matsunga T, Fukuyama K, Miyazaki T, Morimoto T (1997) Tertiary and quaternary structures of 0.19 alpha-amylase inhibitor from wheat kernel determined by X-ray analysis at 2.06 A resolution. Biochemistry 36:13503–13511
Pantoja-Uceda D, Bruix M, Gimenez-Gallego G, Rico M, Santoro J (2003) Solution structure of Ric C3, a 2S albumin storage protein from Ricinus communis. Biochemistry 42:13839–13847
Peters BP, Ebisu S, Goldstein IJ, Flashner M (1979) Interaction of wheat germ agglutinin with sialic acid. Biochemistry 18:5505–5511
Ratanapo S, Ngamjunyaporn W, Chulavatnatol M (1998) Sialic acid binding lectins from leaf of mulberry (Morus alba). Plant Sci 139:141–148
Sato S, Hirakawa H, Isobe S, Fukai E, Watanabe A et al (2011) Sequence analysis of the genome of an oil bearing tree Jatropha curcas L. DNA Res 18:65–76
Schägger H (2006) Tricine-SDS-PAGE. Nat Protoc 1:16–22
Shibasaki M, Sumazaki R, Isoyama S, Takita H (1992) Interaction of lectins with human IgE: IgE-binding property and histamine-releasing activity of twelve plant lectins. Int Arch Allergy Appl Immunol 61:32–39
Shibuya N, Tazaki K, Song ZW, Tarr GE, Goldstein IJ, Peumans WJ (1989) A comparative study of bark lectins from three elderberry (Sambucus) species. J Biochem 106:1098–1103
Stirpe F, Pession-Brizzi A, Lorenzoni E, Strocchi P, Montanaro L, Sperti S (1976) Studies on the proteins from the seeds of Croton tiglium and of Jatropha curcas. Biochem J 156:1–6
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599
Wright CS (1990) 2.2 A resolution structure analysis of two refined N-acetylneuraminyl-lactose—wheat germ agglutinin isolectin complexes. J Mol Biol 215:635–651
Yamamoto K, Konami Y, Irimura T (1997) Sialic acid-binding motif of Maackia amurensis lectins. J Biochem 121:756–761
Acknowledgments
The authors thank DST, Govt. of India and Puri Foundation for Education in India for financial support. We thank Professors M. Vijayan and A. Surolia for useful discussions and encouragement and Dr. Suguna and Dr. Alok Sharma from MBU, IISc, for conducting some experiments. The kind support of Dr. C.G. Suresh from NCL Pune in giving critical inputs is very gratefully acknowledged.
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Nair, D.N., Singh, V., Yamaguchi, Y. et al. Jatropha curcas hemagglutinin is similar to a 2S albumin allergen from the same source and has unique sugar affinities. Planta 236, 1499–1505 (2012). https://doi.org/10.1007/s00425-012-1702-2
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DOI: https://doi.org/10.1007/s00425-012-1702-2