The Occurrence of Sequences Identical with Epitopes from the Allergen Pen a 1.0102 Among Food and Non-Food Proteins

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Abstract

The presence of common epitopes among tropomyosins of invertebrates, including arthropods, e.g. edible ones, may help to explain the molecular basis of cross-reactivity between allergens. The work presented is the first survey concerning global distribution of epitopes from Pen a 1.0102 in universal proteome. In the group of known tropomyosin epitopes, the fragment with the sequence ESKIVELEEEL was found in the sequence of channel catfish (Ictalurus punctatus) tropomyosin. To date, this is the first result suggesting the presence of a complete sequential epitope interacting with gE in vertebrate tropomyosin. Another fragment with the sequence VAALNRRIQL, a major part of the epitope, was found in 11 fish, 8 amphibians, 3 birds, 19 mammalians and 4 human tropomyosin sequences. Identical epitopes are common in sequences of invertebrate tropomyosins, including food and non-food allergens annotated in the Allergome database. The rare pentapeptide with the DEERM sequence occurs in proteins not sharing homology with tropomyosins. Pathogenic microorganisms are the most abundant category of organisms synthesizing such proteins.

1. Abramovitch J.B., Kamath S., Varese N., Zubrinich C., Lopata A.L., O'Hehir R.E., Rolland J.M., IgE reactivity of blue swimmer crab (Portunus pelagicus) tropomyosin, Por p 1, and other allergens; cross-reactivity with black tiger prawn and effects of heating. PLoS ONE, 2013, 8, Article No e67487.

2. Albrecht M., KÜhne Y., Ballmer-Weber B.K., Becker W.-M., Holzhauser T., Lauer I., Reuter A., Randow S., Falk S., Wangorsch A., Lidholm J., Reese G., Vieths S., Relevance of IgE binding to short peptides for the allergenic activity of food allergens. J. Allergy Clin. Immunol., 2009, 124, 328-336.

3. Altschul S.F., Madden T.L., Schäffer A.A., Zhang J., Zhang Z., Miller W., Lipman D.J., Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res., 1997, 25, 3389-3402.

4. Ayuso R., Lehrer S.B., Reese G., Identification of continuous, allergenic regions of the major shrimp allergen Pen a 1 (tropomyosin). Int. Arch. Allergy Immunol., 2002, 127, 27-37.

5. Ayuso R., Sánchez-Garcia S., Pascal M., Lin J., Grishina G., Fu Z., IbáÑez M.D., Sastre J., Sampson H.A., Is epitope recognition of shrimp allergens useful to predict clinical reactivity? Clin. Exp. Allergy, 2012, 42, 293-304.

7. Berin M.C., Sampson H.A., Mucosal immunology of food allergy. Current Biol., 2013, 23, R389-R400.

8. Bessot J.C., Metz-Favre C., Rame J.M., De Blay F., Pauli G., Tropomyosin or not tropomyosin, what is the relevant allergen in house dust mite and snail cross allergies? Eur. Ann. Allergy Clin. Immunol., 2010, 42, 3-10.

9. Cabrera-Chávez F., Calderán de la Barca A.M., Bovine milk intolerance in celiac disease is related to IgA reactivity to ±- and ²- caseins. Nutrition, 2009, 25, 715-V716.

10. Cabrera-Chávez F., Iametti S., Miriani M., Calderón de la Barca A.M., Mamone G., Bonomi F., Maize prolamins resistant to peptic- tryptic digestion maintain immune-recognition by IgA from some celiac disease patients. Plant Foods Human Nutr., 2012, 67, 24-30.

11. Caraballo L., Acevedo N., Allergy in the tropics: the impact of cross-reactivity between mites and ascaris. Front. Biosci., 2011, E3, 51-64.

12. da Costa Santiago H., Bennuru S., Ribeiro J.M.C., Nutman T.B., Structural differences between human proteins and aero - and microbial allergens define allergenicity. PLoS ONE, 2012, 7, Article No e40552.

13. Dall'Antonia F., Pavkov-Keller T., Zangger K., Keller W., Structure of allergens and structure based epitope predictions. Methods, 2014, 66, 3-21.

14. Darewicz M., Dziuba J., Minkiewicz P., Computational characterisation and identification of peptides for in silico detection of potentially celiac-toxic proteins. Food Sci. Technol. Int., 2007, 13, 125-133.

15. Dziuba M., Minkiewicz P., Dąbek M., Peptides, specific proteolysis products as molecular markers of allergenic proteins - in silico studies. Acta Sci. Polon. Technol. Aliment., 2013, 12 (1), 101-112.

16. Glocker E., Grimbacher B., Inflammatory bowel disease: is it a primary immunodeficiency? Cell. Mol. Life Sci., 2012, 69, 41-48.

17. Goodman R.E., Practical and predictive bioinformatic methods for the identification of potentially cross-reactive protein matches. Mol. Nutr. Food Res., 2006, 50, 655-660.

18. Hajeb P., Selamat J., A contemporary review of seafood allergy. Clin. Rev. Allergy Immunol., 2012, 42, 365-385.

19. Hattori M., Taylor T.D., The human intestinal microbiome: a new frontier of human biology. DNA Res., 2009, 16, 1-12.

20. Hunter S., Jones P., Mitchell A., Apweiler R., Attwood T.K., Bateman A., Bernard T., Binns D., Bork P., Burge S., de Castro E., Coggill P., Corbett M., Das U., Daugherty L., Duquenne L., Finn R.D., Fraser M., Gough J., Haft D., Hulo N., Kahn D., Kelly E., Letunic I., Lonsdale D., Lopez R., Madera M., Maslen J., McAnulla C., McDowall J., McMenamin C., Mi H., Mutowo- Muellenet P., Mulder N., Natale D., Orengo C., Pesseat S., Punta M., Quinn A.F., Rivoire C., Sangrador-Vegas A., Selengut J.D., Sigrist C.J.A., Scheremetjew M., Tate J., Thimmajanarthanan M., Thomas P.D., Wu C.H., Yeats C., Yong S.-Y., InterPro in 2011: new developments in the family and domain prediction database. Nucleic Acids Res., 2012, 40, D306-D312.

21. Jêdrychowski L., Wróblewska B., Szymkiewicz A., State of the art on food allergens - a review. Pol. J. Food Nutr. Sci., 2008, 58, 165-175.

22. Kamath S.D., Abdel Rahman A.M., Komoda T., Lopata A.T., Impact of heat processing on the detection of the major shellfish allergen tropomyosin in crustaceans and molluscs using specific monoclonal antibodies. Food Chem., 2013, 141, 4031-4039

23. Kanduc D., Correlating low-similarity peptide sequences and allergenic epitopes. Curr. Pharm. Des., 2008, 14, 289-295.

24. Kanduc D., Homology, similarity, and identity in peptide epitope immunodefinition. J. Peptide Sci., 2012, 18, 487-494.

25. Kinjo A.R., Suzuki H., Yamashita R., Ikegawa Y., Kudou T., Igarashi R., Kengaku Y., Cho H., Standley D.M., Nakagawa A., Nakamura H., Protein Data Bank Japan (PDBj): Maintaining a structural data archive and resource description framework format. Nucleic Acids Res., 2012, 40, D453-D460.

26. Kleter G.A., Peijnenburg A.A.C.M., Screening of transgenic proteins expressed in transgenic food crops for the presence of short amino acid sequences identical to potential, IgE-binding linear epitopes of allergens. BMC Struct. Biol., 2002, 2, Article No 8.

27. Kumar S., Verma A.K., Das M., Dwivedi P.D., Allergenic diversity among plant and animal food proteins. Food Rev. Int., 2012, 28, 277-298.

28. Liu R., Holck A.L., Yang E., Liu C., Xue W., Tropomyosin from tilapia (Oreochromis mossambicus) as an allergen. Clin. Exp. Allergy, 2013, 43, 365-377.

29. Mari A., Rasi C., Palazzo P., Scala E., Allergen databases: current status and perspectives. Curr. Allergy Asthma Rep., 2009, 9, 376-383.

30. Marti P., Truffer R., Stadler M.B., Keller-Gautschi E., Crameri R., Mari A., Schmid-Grendelmeier P., Miescher S.M., Stadler B.M., Vogel M., Allergen motifs and the prediction of allergenicity. Immunol. Lett., 2007, 109, 47-55.

31. Minkiewicz P., Dziuba J., Gladkowska-Balewicz I., Update of the list of allergenic proteins from milk based on local amino acid sequence identity with known epitopes from bovine milk proteins - a short report. Pol. J. Food Nutr. Sci., 2011, 61, 153-158.

32. Minkiewicz P., Bucholska J., Darewicz M., Borawska J., Epitopic hexapeptide sequences from Baltic cod parvalbumin beta (allergen Gad c 1) are common in the universal proteome. Peptides, 2012, 38, 105-109.

33. Mirza Z.K., Sastri B., Lin J.J.C., Amenta P.S., Das K.M., Autoimmunity against human tropomyosin isoforms in ulcerative colitis - Localization of specific human tropomyosin isoforms in the intestine and extraintestinal organs. Inflamm. Bowel Dis., 2006, 12, 1036-1043.

34. Nagy A., Hegyi H., Farkas K., Tordai H., Kozma E., Bányai L., Patthy L., Identification and correction of abnormal, incomplete and mispredicted proteins in public databases. BMC Bioinform., 2008, 9, Article No 353

35. Rawlings N.D., Waller M., Barrett A.J., Bateman A., MEROPS: the database of proteolytic enzymes, their substrates and inhibitors. Nucleic Acids Res., 2014, 42, D503-D509.

36. Reese G., Ayuso R., Carle T., Lehrer S.B., IgE-binding epitopes of shrimp tropomyosin, the major allergen Pen a 1. Int. Arch. Allergy Immunol., 1999, 118, 300-301.

37. Reese G., Viebranz J., Leong-Kee S.M., Plante M., Lauer I., Randow S., Moncin M.S., Ayuso R., Lehrer S.B., Vieths S., Reduced allergenic potency of VR9-1, a mutant of the major shrimp allergen Pen a 1 (tropomyosin). J. Immunol., 2005, 175, 8354-8364.

38. Rose P.W., Beran B., Bi C., Bluhm W.F., Dimitropoulos D., Goodsell D.S., Prlić A.; Quesada M., Quinn G.B., Westbrook J.D., Young Y., Yukich B., Zardecki C., Berman H.M., Bourne P.E., The RCSB Protein Data Bank: Redesigned web site and web services. Nucleic Acids Res., 2011, 39, Suppl. 1, D392-D401.

39. Schnell S., Herman R.A., Should digestion assays be used to estimate persistence of potential allergens in tests for safety of novel food proteins? Clin. Mol. Allergy, 2009, 7, Article No 1.

40. Sen T.Z., Jernigan R.L., Garnier J., Kloczkowski A., GOR V server for protein secondary structure prediction. Bioinformatics, 2005, 21, 2787-2788

41. Sereda M.J., Hartûmann S., Bttner D.W., Volkmer R., Hovestädt M., Brattig N., Lucius R., Characterization of the allergen filarial tropomyosin with an invertebrate specific monoclonal antibody. Acta Tropica, 2010, 116, 61-67.

42. Shanti K.N., Martin B.M., Nagpal S., Metcalfe D.D., Rao P.V., Identification of tropomyosin as the major shrimp allergen and characterization of its IgE-binding epitopes. J. Immunol., 1993, 151, 5354-5363.

43. Snyder E.E., Kampanya N., Lu J., Nordberg E.K., Karur H.R., Shukla M., Soneja J., Tian Y., Xue T., Yoo H., Zhang F., Dharmanolla C., Dongre N.V., Gillespie J.J., Hamelius J., Hance M., Huntington K.I., Jukneliene D., Koziski J., Mackasmiel L., Mane S.P., Nguyen V., Purkayastha A., Shallom J., Yu G., Guo Y., Gabbard J., Hix D., Azad A.F., Baker S.C., Boyle S.M., Khudyakov Y., Meng X.J., Ru precht C., Vinje J., Crasta O.R., Czar M.J., Dickerman A., Eckart J.D., Kenyon R., Will R., Setubal J.C., Sobral B.W., PATRIC: the VBI PathoSystems Resource Integration Center. Nucleic Acids Res., 2007, 35, SI, D401-D406.

44. Tan J., Kuchibhatla D., Sirota F.L., Sherman W.A., Gattermayer T., Kwoh C.Y., Eisenhaber F., Schneider G., Maurer-Stroh S., Tachyon search speeds up retrieval of similar sequences by several orders of magnitude. Bioinformatics, 2012, 28, 1645-1646.

45. The UniProt Consortium, Activities at the Universal Protein Resource (UniProt). Nucleic Acids Res., 2014, 42, D191-D198.

46. Velankar S., Alhroub, Y., Best C., Caboche S., Conroy M.J., Dana J.M., Fernandez Montecelo M.A., van Ginkel G., Golovin A., Gore S.P., Gutmanas, A., Haslam P., Hendrickx P.M.S., Heuson E., Hirshberg M., John M., Lagerstedt I., Mir S., Newman L.E., Oldfield T.J., Patwardhan A., Rinaldi L., Sahni G., Sanz-García E., Sen S., Slowley R., Suarez-Uruena A., Swaminathan G.J., Symmons M.F., Vranken W.F., Wainwright M., Kleywegt G.J., PDBe: Protein Data Bank in Europe. Nucleic Acids Res., 2012, 40, D445-D452.

47. Vita R., Zarebski L., Greenbaum J.A., Emami H., Hoof I., Salimi N., Damle R., Sette A., Peters B., The immune epitope database 2.0. Nucleic Acids Res., 2010, 38, D854-D862.

48. Vojdani A., Tarash I., Cross-reaction between gliadin and different food and tissue antigens. Food Nutr. Sci., 203, 4, Suppl. 1, 20-32.

49. Wilkins M.R., Lindskog I., Gasteiger E., Bairoch A., Sanchez J-C., Hochstrasser D.F., Appel R.D., Detailed peptide characterisation using PeptideMass - a World-Wide Web accessible tool. Electrophoresis, 1997, 18, 403-408

50. Zheng L.N., Lin H., Pawar R., Li Z.X., Li M.H., Mapping IgE binding epitopes of major shrimp (Penaeus monodon) allergen with immunoinformatics tools. Food Chem. Toxicol., 2011, 49, 2954-2960.

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