Comparisons of Allergenic and Metazoan Parasite Proteins: Allergy the Price of Immunity

PLoS Computational Biology

Volumn 11, Issue 10, 2015, Pages

  Tyagi, Nidhi ^a   Farnell, Edward J ^b   Fitzsimmons, Colin M ^b   Ryan, Stephanie ^c   Tukahebwa, Edridah ^d   Maizels, Rick M ^c   Dunne, David W ^b   Thornton, Janet M ^a   Furnham, Nicholas ^e  

^a EUROPEAN BIOINFORMATICS INSTITUTE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

^d MINISTRY OF HEALTH   (Uganda)

^e LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALLERGIES; AMINO ACIDS; IMMUNE SYSTEM; MAMMALS; MOLECULES; PLANTS (BOTANY); PROTEINS;

ALLERGENIC PROTEIN; ALLERGIC REACTIONS; COMPUTATIONAL APPROACH; HUMAN POPULATION; IMMUNE RESPONSE; MAMMALIAN HOSTS; MOLECULAR FEATURE; PARASITE-; PROPERTY; PROTEIN MOLECULES;

ALLERGENS;

ALLERGEN; ALLERGENIC PARASITE PROTEIN; BETV1 PROTEIN; EPITOPE; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G4; METAZOAN PARASITE PROTEIN; MICROORGANISM PROTEIN; UNCLASSIFIED DRUG; VEGETABLE PROTEIN; HELMINTH PROTEIN; PARASITE ANTIGEN;

ALLERGY; AMINO ACID SEQUENCE; ARTICLE; BINDING SITE; CONTROLLED STUDY; HUMAN; IMMUNE RESPONSE; NONHUMAN; PREDICTION; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN TARGETING; SCHISTOSOMIASIS; SEQUENCE ANALYSIS; STRUCTURE ANALYSIS; ANIMAL; CHEMISTRY; GENETICS; HELMINTH; HYPERSENSITIVITY; IMMUNOLOGY; INNATE IMMUNITY; MOLECULAR EVOLUTION; PARASITOLOGY;

ALLERGENS; ANIMALS; ANTIGENS, HELMINTH; EVOLUTION, MOLECULAR; HELMINTH PROTEINS; HELMINTHS; HUMANS; HYPERSENSITIVITY; IMMUNITY, INNATE; IMMUNOGLOBULIN E;

EID: 84946045490     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1004546     Document Type: Article

References (57)

1. Fallon PG, Mangan NE, (2007) Suppression of TH2-type allergic reactions by helminth infection. Nature reviews Immunology 7: 220–230. Available: http://www.ncbi.nlm.nih.gov/pubmed/17318233. Accessed 23 May 2014. 17318233
2. Maizels RM, Yazdanbakhsh M, (2003) Immune regulation by helminth parasites: cellular and molecular mechanisms. Nature reviews Immunology 3: 733–744. Available: http://www.ncbi.nlm.nih.gov/pubmed/12949497. Accessed 23 May 2014. 12949497
3. Pontes-de-Carvalho L, Mengel J, (2014) A Question of Nature: Some Antigens are Bound to be Allergens. Frontiers in immunology 5: 373. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=4122158&tool=pmcentrez&rendertype=abstract. Accessed 22 December 2014. doi: 10.3389/fimmu.2014.00373 25140169
4. Hagan P, Blumenthal UJ, Dunn D, Simpson AJ, Wilkins HA, (1991) Human IgE, IgG4 and resistance to reinfection with Schistosoma haematobium. Nature 349: 243–245. Available: http://www.ncbi.nlm.nih.gov/pubmed/1898985. Accessed 23 May 2014. 1898985
5. Rihet P, Demeure CE, Bourgois A, Prata A, Dessein AJ, (1991) Evidence for an association between human resistance to Schistosoma mansoni and high anti-larval IgE levels. European journal of immunology 21: 2679–2686. Available: http://www.ncbi.nlm.nih.gov/pubmed/1936116. Accessed 23 May 2014. 1936116
6. Dunne DW, Butterworth AE, Fulford AJ, Kariuki HC, Langley JG, et al. (1992) Immunity after treatment of human schistosomiasis: association between IgE antibodies to adult worm antigens and resistance to reinfection. European journal of immunology 22: 1483–1494. Available: http://www.ncbi.nlm.nih.gov/pubmed/1601036. Accessed 23 May 2014. 1601036
7. Zhang Z, Wu H, Chen S, Hu L, Xie Z, et al. (1997) Association between IgE antibody against soluble egg antigen and resistance to reinfection with Schistosoma japonicum. Transactions of the Royal Society of Tropical Medicine and Hygiene 91: 606–608. Available: http://www.ncbi.nlm.nih.gov/pubmed/9463682. Accessed 23 May 2014. 9463682
8. Moreno M, Benavidez U, Carol H, Rosenkranz C, Welle M, et al. (2004) Local and systemic immune responses to Echinococcus granulosus in experimentally infected dogs. Veterinary parasitology 119: 37–50. Available: http://www.ncbi.nlm.nih.gov/pubmed/15036575. Accessed 23 May 2014. 15036575
9. Bethony J, Loukas A, Smout M, Brooker S, Mendez S, et al. (2005) Antibodies against a secreted protein from hookworm larvae reduce the intensity of hookworm infection in humans and vaccinated laboratory animals. FASEB journal: official publication of the Federation of American Societies for Experimental Biology 19: 1743–1745. Available: http://www.ncbi.nlm.nih.gov/pubmed/16037096. Accessed 23 May 2014.
10. Faulkner H, Turner J, Kamgno J, Pion SD, Boussinesq M, et al. (2002) Age- and infection intensity-dependent cytokine and antibody production in human trichuriasis: the importance of IgE. The Journal of infectious diseases 185: 665–672. Available: http://www.ncbi.nlm.nih.gov/pubmed/11865424. Accessed 23 May 2014. 11865424
11. Turner JD, Faulkner H, Kamgno J, Kennedy MW, Behnke J, et al. (2005) Allergen-specific IgE and IgG4 are markers of resistance and susceptibility in a human intestinal nematode infection. Microbes and infection / Institut Pasteur 7: 990–996. Available: http://www.ncbi.nlm.nih.gov/pubmed/15961339. Accessed 23 May 2014. 15961339
12. Matsuda H, Watanabe N, Kiso Y, Hirota S, Ushio H, et al. (1990) Necessity of IgE antibodies and mast cells for manifestation of resistance against larval Haemaphysalis longicornis ticks in mice. Journal of immunology (Baltimore, Md: 1950) 144: 259–262. Available: http://www.ncbi.nlm.nih.gov/pubmed/2295794. Accessed 23 May 2014.
13. Tarigan S, Huntley JF, (2005) Failure to protect goats following vaccination with soluble proteins of Sarcoptes scabiei: evidence for a role for IgE antibody in protection. Veterinary parasitology 133: 101–109. Available: http://www.ncbi.nlm.nih.gov/pubmed/16118041. Accessed 23 May 2014. 16118041
14. Lello E, de Rosis AMB, (2003) Inflammatory reaction to the human bot-fly, Dermatobia hominis, in infested and reinfested mice. Medical and veterinary entomology 17: 55–60. Available: http://www.ncbi.nlm.nih.gov/pubmed/12680926. Accessed 23 May 2014. 12680926
15. Johansson E, Aponno M, Lundberg M, van Hage-Hamsten M, (2001) Allergenic cross-reactivity between the nematode Anisakis simplex and the dust mites Acarus siro, Lepidoglyphus destructor, Tyrophagus putrescentiae, and Dermatophagoides pteronyssinus. Allergy 56: 660–666. Available: http://www.ncbi.nlm.nih.gov/pubmed/11421925. Accessed 23 May 2014. 11421925
16. Bernardini R, Mistrello G, Novembre E, Roncarolo D, Zanotta S, et al. (n.d.) Cross-reactivity between IgE-binding proteins from Anisakis simplex and Dermatophagoides pteronyssinus. International journal of immunopathology and pharmacology 18: 671–675. Available: http://www.ncbi.nlm.nih.gov/pubmed/16388714. Accessed 23 May 2014. 16388714
17. Santos ABR, Rocha GM, Oliver C, Ferriani VPL, Lima RC, et al. (2008) Cross-reactive IgE antibody responses to tropomyosins from Ascaris lumbricoides and cockroach. The Journal of allergy and clinical immunology 121: 1040–6.e1. Available: http://www.ncbi.nlm.nih.gov/pubmed/18275995. Accessed 23 May 2014. doi: 10.1016/j.jaci.2007.12.1147 18275995
18. Santiago H da C, Ribeiro-Gomes FL, Bennuru S, Nutman TB, (2015) Helminth Infection Alters IgE Responses to Allergens Structurally Related to Parasite Proteins. Journal of immunology (Baltimore, Md: 1950) 194: 93–100. Available: http://www.ncbi.nlm.nih.gov/pubmed/25404363. Accessed 5 January 2015.
19. Mari A, Scala E, (2006) Allergome: a unifying platform. Arbeiten aus dem Paul-Ehrlich-Institut (Bundesamt für Sera und Impfstoffe) zu Frankfurt aM 95: 29–39; discussion 39–40. Available: http://www.ncbi.nlm.nih.gov/pubmed/7393720. Accessed 23 May 2014.
20. Radauer C, Bublin M, Wagner S, Mari A, Breiteneder H, (2008) Allergens are distributed into few protein families and possess a restricted number of biochemical functions. The Journal of allergy and clinical immunology 121: 847–52.e7. Available: http://www.ncbi.nlm.nih.gov/pubmed/18395549. Accessed 23 May 2014. doi: 10.1016/j.jaci.2008.01.025 18395549
21. Fitzsimmons CM, Dunne DW, (2009) Survival of the fittest: allergology or parasitology? Trends in parasitology 25: 447–451. Available: http://www.ncbi.nlm.nih.gov/pubmed/19744885. Accessed 23 May 2014. doi: 10.1016/j.pt.2009.07.004 19744885
22. Sokol CL, Barton GM, Farr AG, Medzhitov R, (2008) A mechanism for the initiation of allergen-induced T helper type 2 responses. Nature immunology 9: 310–318. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3888112&tool=pmcentrez&rendertype=abstract. Accessed 22 December 2014. doi: 10.1038/ni1558 18300366
23. Palm NW, Rosenstein RK, Medzhitov R, (2012) Allergic host defences. Nature 484: 465–472. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3596087&tool=pmcentrez&rendertype=abstract. Accessed 22 December 2014. doi: 10.1038/nature11047 22538607
24. Fitzsimmons CM, Jones FM, Stearn A, Chalmers IW, Hoffmann KF, et al. (2012) The Schistosoma mansoni tegumental-allergen-like (TAL) protein family: influence of developmental expression on human IgE responses. PLoS neglected tropical diseases 6: e1593. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3317908&tool=pmcentrez&rendertype=abstract. Accessed 14 July 2014. doi: 10.1371/journal.pntd.0001593 22509417
25. Farias LP, Rodrigues D, Cunna V, Rofatto HK, Faquim-Mauro EL, et al. (2012) Schistosoma mansoni venom allergen like proteins present differential allergic responses in a murine model of airway inflammation. PLoS neglected tropical diseases 6: e1510. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3274501&tool=pmcentrez&rendertype=abstract. Accessed 14 July 2014. doi: 10.1371/journal.pntd.0001510 22347513
26. Chalmers IW, McArdle AJ, Coulson RM, Wagner MA, Schmid R, et al. (2008) Developmentally regulated expression, alternative splicing and distinct sub-groupings in members of the Schistosoma mansoni venom allergen-like (SmVAL) gene family. BMC genomics 9: 89. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2270263&tool=pmcentrez&rendertype=abstract. Accessed 14 July 2014. doi: 10.1186/1471-2164-9-89 18294395
27. Silas S, Fitzsimmons CM, Jones FM, Pinot de Moira A, Wawrzyniak J, et al. (2014) Human IgE responses to different splice variants of Schistosoma mansoni tropomyosin: associations with immunity. International journal for parasitology 44: 381–390. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=4026961&tool=pmcentrez&rendertype=abstract. Accessed 14 July 2014. doi: 10.1016/j.ijpara.2014.02.004 24657550
28. Fitzsimmons CM, McBeath R, Joseph S, Jones FM, Walter K, et al. (2007) Factors affecting human IgE and IgG responses to allergen-like Schistosoma mansoni antigens: Molecular structure and patterns of in vivo exposure. International archives of allergy and immunology 142: 40–50. Available: http://www.ncbi.nlm.nih.gov/pubmed/17019080. Accessed 14 July 2014. 17019080
29. Akdis M, Akdis CA, (2007) Mechanisms of allergen-specific immunotherapy. The Journal of allergy and clinical immunology 119: 780–791. Available: http://www.ncbi.nlm.nih.gov/pubmed/17321578. Accessed 14 July 2014. 17321578
30. Platts-Mills TAE, Woodfolk JA, Erwin EA, Aalberse R, (2004) Mechanisms of tolerance to inhalant allergens: the relevance of a modified Th2 response to allergens from domestic animals. Springer seminars in immunopathology 25: 271–279. Available: http://www.ncbi.nlm.nih.gov/pubmed/15007631. Accessed 5 January 2015. 15007631
31. Fox JG, Beck P, Dangler CA, Whary MT, Wang TC, et al. (2000) Concurrent enteric helminth infection modulates inflammation and gastric immune responses and reduces helicobacter-induced gastric atrophy. Nature medicine 6: 536–542. Available: http://www.ncbi.nlm.nih.gov/pubmed/10802709. Accessed 23 May 2014. 10802709
32. Nacher M, Singhasivanon P, Silachamroon U, Treeprasertsuk S, Vannaphan S, et al. (2001) Helminth infections are associated with protection from malaria-related acute renal failure and jaundice in Thailand. The American journal of tropical medicine and hygiene 65: 834–836. Available: http://www.ncbi.nlm.nih.gov/pubmed/11791982. Accessed 23 May 2014. 11791982
33. Araujo MI, Lopes AA, Medeiros M, Cruz AA, Sousa-Atta L, et al. (2000) Inverse association between skin response to aeroallergens and Schistosoma mansoni infection. International archives of allergy and immunology 123: 145–148. Available: http://www.ncbi.nlm.nih.gov/pubmed/11060486. Accessed 23 May 2014. 11060486
34. van den Biggelaar AH, van Ree R, Rodrigues LC, Lell B, Deelder AM, et al. (2000) Decreased atopy in children infected with Schistosoma haematobium: a role for parasite-induced interleukin-10. Lancet 356: 1723–1727. Available: http://www.ncbi.nlm.nih.gov/pubmed/11095260. Accessed 23 May 2014. 11095260
35. Shani N, Shani Z, Shoseyov O, Mruwat R, Shoseyov D, (2011) Oxidized cellulose binding to allergens with a carbohydrate-binding module attenuates allergic reactions. Journal of immunology (Baltimore, Md: 1950) 186: 1240–1247. Available: http://www.ncbi.nlm.nih.gov/pubmed/21169552. Accessed 23 May 2014.
36. Vita R, Zarebski L, Greenbaum JA, Emami H, Hoof I, et al. (2010) The immune epitope database 2.0. Nucleic acids research 38: D854–62. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2808938&tool=pmcentrez&rendertype=abstract. Accessed 23 May 2014. doi: 10.1093/nar/gkp1004 19906713
37. Apweiler R, Bateman A, Martin MJ, O’Donovan C, Magrane M, Alam-Faruque Y AE, (2014) Activities at the Universal Protein Resource (UniProt). Nucleic acids research 42: D191–8. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3965022&tool=pmcentrez&rendertype=abstract. Accessed 23 May 2014. doi: 10.1093/nar/gkt1140 24253303
38. Eddy SR, (1998) Profile hidden Markov models. Bioinformatics (Oxford, England) 14: 755–763. Available: http://www.ncbi.nlm.nih.gov/pubmed/9918945. Accessed 23 May 2014.
39. Orengo CA, Bray JE, Buchan DWA, Harrison A, Lee D, et al. (2002) The CATH protein family database: a resource for structural and functional annotation of genomes. Proteomics 2: 11–21. Available: http://www.ncbi.nlm.nih.gov/pubmed/11788987. Accessed 23 May 2014. 11788987
40. Lees J, Yeats C, Perkins J, Sillitoe I, Rentzsch R, et al. (2012) Gene3D: a domain-based resource for comparative genomics, functional annotation and protein network analysis. Nucleic acids research 40: D465–71. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3245158&tool=pmcentrez&rendertype=abstract. Accessed 23 May 2014. doi: 10.1093/nar/gkr1181 22139938
41. Pieper U, Eswar N, Braberg H, Madhusudhan MS, Davis FP, et al. (2004) MODBASE, a database of annotated comparative protein structure models, and associated resources. Nucleic acids research 32: D217–22. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=308829&tool=pmcentrez&rendertype=abstract. Accessed 23 May 2014. 14681398
42. Zhang Y, Skolnick J, (2004) Scoring function for automated assessment of protein structure template quality. Proteins 57: 702–710. Available: http://www.ncbi.nlm.nih.gov/pubmed/15476259. Accessed 23 May 2014. 15476259
43. Lipman DJ, Pearson WR, (1985) Rapid and sensitive protein similarity searches. Science (New York, NY) 227: 1435–1441. Available: http://www.ncbi.nlm.nih.gov/pubmed/2983426. Accessed 23 May 2014.
44. Guyon F, Tufféry P, (2014) Fast protein fragment similarity scoring using a Binet-Cauchy kernel. Bioinformatics (Oxford, England) 30: 784–791. Available: http://www.ncbi.nlm.nih.gov/pubmed/24167157. Accessed 23 May 2014.
45. Fitzpatrick JM, Peak E, Perally S, Chalmers IW, Barrett J, et al. (2009) Anti-schistosomal intervention targets identified by lifecycle transcriptomic analyses. PLoS neglected tropical diseases 3: e543. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2764848&tool=pmcentrez&rendertype=abstract. Accessed 14 July 2014. doi: 10.1371/journal.pntd.0000543 19885392
46. Micallef L, Rodgers P, (2014) eulerAPE: drawing area-proportional 3-Venn diagrams using ellipses. PloS one 9: e101717. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=4102485&tool=pmcentrez&rendertype=abstract. Accessed 7 October 2014. doi: 10.1371/journal.pone.0101717 25032825
47. Emanuelsson C, Spangfort MD, (2007) Allergens as eukaryotic proteins lacking bacterial homologues. Molecular immunology 44: 3256–3260. Available: http://www.ncbi.nlm.nih.gov/pubmed/17382394. Accessed 22 December 2014. 17382394
48. Santiago H da C, Bennuru S, Ribeiro JMC, Nutman TB, (2012) Structural differences between human proteins and aero- and microbial allergens define allergenicity. PloS one 7: e40552. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3399830&tool=pmcentrez&rendertype=abstract. Accessed 15 July 2014. doi: 10.1371/journal.pone.0040552 22815762
49. Kringelum JV, Nielsen M, Padkjær SB, Lund O, (2013) Structural analysis of B-cell epitopes in antibody:protein complexes. Molecular immunology 53: 24–34. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3461403&tool=pmcentrez&rendertype=abstract. Accessed 23 May 2014. doi: 10.1016/j.molimm.2012.06.001 22784991
50. Perez-Gordo M, Lin J, Bardina L, Pastor-Vargas C, Cases B, et al. (2012) Epitope mapping of Atlantic salmon major allergen by peptide microarray immunoassay. International archives of allergy and immunology 157: 31–40. Available: http://www.ncbi.nlm.nih.gov/pubmed/21894026. Accessed 23 May 2014. doi: 10.1159/000324677 21894026
51. Fedorov AA, Ball T, Mahoney NM, Valenta R, Almo SC, (1997) The molecular basis for allergen cross-reactivity: crystal structure and IgE-epitope mapping of birch pollen profilin. Structure (London, England: 1993) 5: 33–45. Available: http://www.ncbi.nlm.nih.gov/pubmed/9016715. Accessed 23 May 2014.
52. Pruett JH, (1999) Identification and purification of a 16-kDa allergen from Psoroptes ovis (Acarina: Psoroptidae). Journal of medical entomology 36: 544–550. Available: http://www.ncbi.nlm.nih.gov/pubmed/10534947. Accessed 23 May 2014. 10534947
53. Ball T, Fuchs T, Sperr WR, Valent P, Vangelista L, et al. (1999) B cell epitopes of the major timothy grass pollen allergen, phl p 1, revealed by gene fragmentation as candidates for immunotherapy. FASEB journal: official publication of the Federation of American Societies for Experimental Biology 13: 1277–1290. Available: http://www.ncbi.nlm.nih.gov/pubmed/10428753. Accessed 23 May 2014.
54. Jenkins JA, Breiteneder H, Mills ENC, (2007) Evolutionary distance from human homologs reflects allergenicity of animal food proteins. The Journal of allergy and clinical immunology 120: 1399–1405. Available: http://www.ncbi.nlm.nih.gov/pubmed/17935767. Accessed 25 May 2014. 17935767
55. Curwen RS, Ashton PD, Johnston DA, Wilson RA, (2004) The Schistosoma mansoni soluble proteome: a comparison across four life-cycle stages. Molecular and biochemical parasitology 138: 57–66. Available: http://www.ncbi.nlm.nih.gov/pubmed/15500916. Accessed 15 July 2014. 15500916
56. Sinclair D, Peters SA, (2004) The predictive value of total serum IgE for a positive allergen specific IgE result. Journal of clinical pathology 57: 956–959. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1770430&tool=pmcentrez&rendertype=abstract. Accessed 14 July 2014. 15333657
57. Farnell EJ, Tyagi N, Ryan S, Chalmers IW, Pinot de Moira A, et al. (2015) Known Allergen Structures Predict Schistosoma mansoni IgE-Binding Antigens in Human Infection. Frontiers in immunology 6: 26. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=4315118&tool=pmcentrez&rendertype=abstract. Accessed 28 June 2015. doi: 10.3389/fimmu.2015.00026 25691884