Stinging Insect Allergens

Le       Cui; Ying-Yang       Xu; Xiu-Jie       Wang; Kai       Guan
Abstract

Hymenoptera venom allergy is one of the common causes of anaphylaxis. However, when physicians make the diagnosis of Hymenoptera venom allergy, the history of being stung is not always consistent with the results of venom-specific IgE. With the development of component-resolved diagnosis, it is possible to accurately localize an allergic reaction to certain sensitized proteins. This paper reviewed the studies that have addressed the identified allergenicity and cross-reactivity of Hymenoptera venom allergens accepted by the WHO/IUIS Nomenclature Sub-committee, the componentresolved diagnosis of Hymenoptera venom allergy and its predictive values for the efficacy and safety of venom immunotherapy. Also special attention was paid to the spread of Hymenoptera venom allergy in Asian countries.
Keywords: Allergens, cross-reactions, Hymenoptera, hypersensitivity, immunoglobulin E, immunotherapy, venoms.
Graphical Abstract

[1] 
OSTEN. T. Hymenoptera: bees, wasps and ants; Cambridge University Press: Cambridge, 2007. 
[2] 
O’Neill, K.M. Solitary wasps: behaviour and natural history; Cornell: U.S.A, 2000. 
[3] 
Michener, C.D. The bees of the World; The Johns Hopkins University Press: Baltimore, and London, 2000. 
[4] 
Bilò, M.B. Anaphylaxis caused by Hymenoptera stings: from epidemiology to treatment. Allergy,  2011, 66(Suppl. 95), 35-37.
[http://dx.doi.org/10.1111/j.1398-9995.2011.02630.x] [PMID:  21668850] 
[5] 
Fernandez, J.; Blanca, M.; Soriano, V.; Sanchez, J.; Juarez, C. Epidemiological study of the prevalence of allergic reactions to Hymenoptera in a rural population in the Mediterranean area. Clin. Exp. Allergy,  1999, 29(8), 1069-1074.
[http://dx.doi.org/10.1046/j.1365-2222.1999.00614.x] [PMID:  10457110] 
[6] 
Xie, C.; Xu, S.; Ding, F.; Xie, M.; Lv, J.; Yao, J.; Pan, D.; Sun, Q.; Liu, C.; Chen, T.; Li, S.; Wang, W. Clinical features of severe wasp sting patients with dominantly toxic reaction: analysis of 1091 cases. PLoS One,  2013, 8(12) e83164
[http://dx.doi.org/10.1371/journal.pone.0083164] [PMID:  24391743] 
[7] 
Graif, Y.; Romano-Zelekha, O.; Livne, I.; Green, M.S.; Shohat, T. Allergic reactions to insect stings: results from a national survey of 10,000 junior high school children in Israel. J. Allergy Clin. Immunol.,  2006, 117(6), 1435-1439.
[http://dx.doi.org/10.1016/j.jaci.2006.03.004] [PMID:  16751010] 
[8] 
Ertoy Karagol, H.I.; Bakirtas, A.; Yilmaz, O.; Topal, E.; Arga, M.; Demirsoy, M.S.; Turktas, I. Long-term follow-up of re-sting reactions in children with moderate to severe venom hypersensitivity. Eur. J. Pediatr.,  2015, 174(7), 891-896.
[http://dx.doi.org/10.1007/s00431-014-2478-0] [PMID:  25563216] 
[9] 
Kalyoncu, A.F.; Demir, A.U.; Ozcan, U.; Ozkuyumcu, C.; Sahin, A.A.; Bariş, Y.I. Bee and wasp venom allergy in Turkey. Ann. Allergy Asthma Immunol.,  1997, 78(4), 408-412.
[http://dx.doi.org/10.1016/S1081-1206(10)63203-6] [PMID:  9109709] 
[10] 
Hayashih, Y.; Hirata, H.; Watanabe, M.; Yoshida, N.; Yokoyama, T.; Murayama, Y.; Sugiyama, K.; Arima, M.; Fukushima, Y.; Fukuda, T.; Ishii, Y. Epidemiologic Investigation of Hornet and Paper Wasp Stings in Forest Workers and Electrical Facility Field Workers in Japan. Allergol. Int.,  2014, 63(1), 21-26.
[http://dx.doi.org/10.2332/allergolint.13-OA-0556] [PMID:  28942981] 
[11] 
Kochuyt, A.M.; Van Hoeyveld, E.; Stevens, E.A. Occupational allergy to bumble bee venom. Clin. Exp. Allergy,  1993, 23(3), 190-195.
[http://dx.doi.org/10.1111/j.1365-2222.1993.tb00881.x] [PMID:  8472189] 
[12] 
Przybilla, B.; Ruëff, F. Hymenoptera venom allergy. J. Dtsch. Dermatol. Ges.,  2010, 8(2), 114-127.
[http://dx.doi.org/10.1111/j.1610-0387.2009.07125_supp.x] [PMID:  19751222] 
[13] 
Ollert, M.; Blank, S. Anaphylaxis to insect venom allergens: role of molecular diagnostics. Curr. Allergy Asthma Rep.,  2015, 15(5), 26.
[http://dx.doi.org/10.1007/s11882-015-0527-z] [PMID:  26139335] 
[14] 
Greene, A.; Breisch, N.L. Avoidance of bee and wasp stings: an entomological perspective. Curr. Opin. Allergy Clin. Immunol.,  2005, 5(4), 337-341.
[http://dx.doi.org/10.1097/01.all.0000173781.58154.53] [PMID:  15985816] 
[15] 
Bonifazi, F.; Jutel, M.; Biló, B.M.; Birnbaum, J.; Muller, U. Prevention and treatment of hymenoptera venom allergy: guidelines for clinical practice. Allergy,  2005, 60(12), 1459-1470.
[http://dx.doi.org/10.1111/j.1398-9995.2005.00960.x] [PMID:  16266376] 
[16] 
Schiener, M.; Graessel, A.; Ollert, M.; Schmidt-Weber, C.B.; Blank, S. Allergen-specific immunotherapy of Hymenoptera venom allergy - also a matter of diagnosis. Hum. Vaccin. Immunother.,  2017, 13(10), 2467-2481.
[http://dx.doi.org/10.1080/21645515.2017.1334745] [PMID:  28604163] 
[17] 
Jakob, T.; Müller, U.; Helbling, A.; Spillner, E. Component resolved diagnostics for hymenoptera venom allergy. Curr. Opin. Allergy Clin. Immunol.,  2017, 17(5), 363-372.
[http://dx.doi.org/10.1097/ACI.0000000000000390] [PMID:  28759475] 
[18] 
Choi, M.B.; Kim, T.G.; Kwon, O. Recent Trends in Wasp Nest Removal and Hymenoptera Stings in South Korea. J. Med. Entomol.,  2019, 56(1), 254-260.
[http://dx.doi.org/10.1093/jme/tjy144] [PMID:  30137561] 
[19] 
Tan, K.; Meixner, M.D.; Fuchs, S.; Zhang, X.; He, S.; Kandemir, I.; Sheppard, W.S.; Koeniger, N. Geographic distribution of the eastern honeybee, Apis cerana (Hymenoptera: Apidae), across ecological zones in China: Morphological and molecular analyses. Syst. Biodivers.,  2006, 4, 473-482.
[http://dx.doi.org/10.1017/S1477200006002015] [PMID: ] 
[20] 
Yu-suo, J.; Hui-ting, Z.; Jun-bing, J.; Guo-qing, C.; Gui-xian, Z. Wen-jin, Z.; Chuan-jia, G. Studies on mtDNA tRNA~(leu)~COII Gene Polymorphisms of Apis cerana Distributed in Different Geo-graphic Areas in China. Zhongguo Nong Ye Ke Xue,  2007, 07, 1535-1542.
[21] 
Yang, G.H. Harm of introducing the western honeybee Apis mellifera L. to the Chinese honeybee Apis cerana F. and its ecological impact. Acta Entomologica Sinica,  2005, 48(3), 401-406.
[22] 
Sakagami, F. Some Interspecific Relations Between Japanese and
European Honeybees. J. Ecol,  1959, 12(3), 1962-06-01.
[23] 
Celikel, S.; Karakaya, G.; Yurtsever, N.; Sorkun, K.; Kalyoncu, A.F. Bee and bee products allergy in Turkish beekeepers: determination of risk factors for systemic reactions. Allergol. Immunopathol. (Madr.),  2006, 34(5), 180-184.
[http://dx.doi.org/10.1157/13094024] [PMID:  17064646] 
[24] 
Le, C.; Kai, G.; Lisha, L.; Junda, L.; Zixi, W.; Yingyang, X.; Lianglu, W.; Jia, Y. Analysis of prevalence and related risk factors of bee venom in bee research population. Shandong Daxue Er-Bi-Hou-Yan Xuebao,  2019, 33, 63-66.
[25] 
Lee, J.A.; Son, M.J.; Choi, J.; Jun, J.H.; Kim, J.I.; Lee, M.S. Bee venom acupuncture for rheumatoid arthritis: a systematic review of randomised clinical trials. BMJ Open,  2014, 4(11) e006140
[http://dx.doi.org/10.1136/bmjopen-2014-006140] [PMID:  25380812] 
[26] 
Guan, K.; Li, L.; Wang, R.; Yin, J. Clinical Characteristics of Anaphylaxis Induced by Honeybee Venom. Chin. J. Allergy Clin. Immunol.,  2016, 197-201.
[27] 
Vazquez-Revuelta, P.; Madrigal-Burgaleta, R. Death due to Live
Bee Acupuncture Apitherapy. Journal of investigational allergology
and clinical immunology: official organ of the International
Association of Asthmology (INTERASMA) and Sociedad Latinoamericana
de Alergia e Inmunología,  2018, 28, 45-46.
[28] 
Jung, J.W.; Jeon, E.J.; Kim, J.W.; Choi, J.C.; Shin, J.W.; Kim, J.Y.; Park, I.W.; Choi, B.W. A fatal case of intravascular coagulation after bee sting acupuncture. Allergy Asthma Immunol. Res.,  2012, 4(2), 107-109.
[http://dx.doi.org/10.4168/aair.2012.4.2.107] [PMID:  22379607] 
[29] 
Le, C.; Zi-xi, W.; Kai, G.; Lanier, B.Q.; Li-sha, L.; Ying-yang, X.; Jia, Y.; Tao, X. Clinical manifestations and risk factors of honeybee venom allergy induced by apitherapy. Chin. J. Allergy Clin. Immunol.,  2018, 12, 277-282.
[30] 
Li, L.S.; Guan, K. Occupational Asthma Caused by Inhalable Royal Jelly and Its Cross-reactivity with Honeybee Venom. Chin. Med. J. (Engl.),  2016, 129(23), 2888-2889.
[http://dx.doi.org/10.4103/0366-6999.194650] [PMID:  27901009] 
[31] 
Choi, M.B.; Martin, S.J.; Lee, J.W. Distribution, spread, and impact of the invasive hornet Vespa velutina in South Korea. J. Asia Pac. Entomol.,  2012, 15, 473-477.
[http://dx.doi.org/10.1016/j.aspen.2011.11.004] 
[32] 
Takahashi, J.; Okuyama, H.; Kiyoshi, T.; Takeuchi, T.; Martin, S.J. Origins of Vespa velutina hornets that recently invaded Iki Island, Japan and Jersey Island, UK. Mitochondrial DNA A. DNA Mapp. Seq. Anal.,  2019, 30(3), 434-439.
[http://dx.doi.org/10.1080/24701394.2018.1538366] [PMID:  30489182] 
[33] 
Yamasaki, K.; Takahashi, R.; Harada, R.; Matsuo, Y.; Nakamura, M.; Takahashi, J. Reproductive interference by alien hornet Vespa velutina threatens the native populations of Vespa simillima in Japan; SpringerLink: Berlin, 2019. 
[34] 
Habermann, E. Bee and wasp venoms. Science,  1972, 177(4046), 314-322.
[http://dx.doi.org/10.1126/science.177.4046.314] [PMID:  4113805] 
[35] 
Müller, U.R.; Johansen, N.; Petersen, A.B.; Fromberg-Nielsen, J.; Haeberli, G. Hymenoptera venom allergy: analysis of double positivity to honey bee and Vespula venom by estimation of IgE antibodies to species-specific major allergens Api m1 and Ves v5. Allergy,  2009, 64(4), 543-548.
[http://dx.doi.org/10.1111/j.1398-9995.2008.01794.x] [PMID:  19120073] 
[36] 
Hofmann, S.C.; Pfender, N.; Weckesser, S.; Huss-Marp, J.; Jakob, T. Added value of IgE detection to rApi m 1 and rVes v 5 in patients with Hymenoptera venom allergy. J. Allergy Clin. Immunol.,  2011, 127(1), 265-267.
[http://dx.doi.org/10.1016/j.jaci.2010.06.042] [PMID:  20719373] 
[37] 
Kohler, J.; Blank, S.; Muller, S.; Bantleon, F.; Frick, M. Component resolution reveals additional major allergens in patients with honeybee venom allergy. J. Allergy Clin. Immunol.,  2014, 133, 1383-1389.
[38] 
Marković-Housley, Z.; Miglierini, G.; Soldatova, L.; Rizkallah, P.J.; Müller, U.; Schirmer, T. Crystal structure of hyaluronidase, a major allergen of bee venom. Structure,  2000, 8(10), 1025-1035.
[http://dx.doi.org/10.1016/S0969-2126(00)00511-6] [PMID:  11080624 ] 
[39] 
Binder, M.; Fierlbeck, G.; King, Ti.; Valent, P.; Bühring, H.J. Individual hymenoptera venom compounds induce upregulation of the basophil activation marker ectonucleotide pyrophosphatase/phosphodiesterase 3 (CD203c) in sensitized patients. Int. Arch. Allergy Immunol.,  2002, 129(2), 160-168.
[http://dx.doi.org/10.1159/000065875] [PMID:  12403934] 
[40] 
Grunwald, T.; Bockisch, B.; Spillner, E.; Ring, J.; Bredehorst, R.; Ollert, M.W. Molecular cloning and expression in insect cells of honeybee venom allergen acid phosphatase (Api m 3). J. Allergy Clin. Immunol.,  2006, 117(4), 848-854.
[http://dx.doi.org/10.1016/j.jaci.2005.12.1331] [PMID:  16630944] 
[41] 
Paull, B.R.; Yunginger, J.W.; Gleich, G.J. Melittin: an allergen of honeybee venom. J. Allergy Clin. Immunol.,  1977, 59(4), 334-338.
[http://dx.doi.org/10.1016/0091-6749(77)90056-2] [PMID:  850023] 
[42] 
Schröder, E.; Lübke, K.; Lehmann, M.; Beetz, I. Haemolytic activity and action on the surface tension of aqueous solutions of synthetic melittins and their derivatives. Experientia,  1971, 27(7), 764-765.
[http://dx.doi.org/10.1007/BF02136851] [PMID:  5139482] 
[43] 
Sessa, G.; Freer, J.H.; Colacicco, G.; Weissmann, G. Interaction of alytic polypeptide, melittin, with lipid membrane systems. J. Biol. Chem.,  1969, 244(13), 3575-3582.
[PMID:  5794226] 
[44] 
Tosteson, M.T.; Holmes, S.J.; Razin, M.; Tosteson, D.C. Melittin lysis of red cells. J. Membr. Biol.,  1985, 87(1), 35-44.
[http://dx.doi.org/10.1007/BF01870697] [PMID:  4057243] 
[45] 
Park, D.; Jung, J.W.; Lee, M.O.; Lee, S.Y.; Kim, B.; Jin, H.J.; Kim, J.; Ahn, Y.J.; Lee, K.W.; Song, Y.S.; Hong, S.; Womack, J.E.; Kwon, H.W. Functional characterization of naturally occurring melittin peptide isoforms in two honey bee species, Apis mellifera and Apis cerana. Peptides,  2014, 53, 185-193.
[http://dx.doi.org/10.1016/j.peptides.2014.01.026] [PMID:  24512991] 
[46] 
Mollay, C.; Kreil, G. Enhancement of bee venom phospholipase A2 activity by melittin, direct lytic factor from cobra venom and polymyxin B. FEBS Lett.,  1974, 46(1), 141-144.
[http://dx.doi.org/10.1016/0014-5793(74)80354-6] [PMID:  4371280] 
[47] 
Steffen, P.; Hofbauer, H.; Noll-Hussong, M. Bee Stings and Chronic Pain Disorder. Cureus,  2018, 10(1) e2060
[PMID:  29545983] 
[48] 
Chen, J.; Guan, S.M.; Sun, W.; Fu, H. Melittin, the Major Pain-Producing Substance of Bee Venom. Neurosci. Bull.,  2016, 32(3), 265-272.
[http://dx.doi.org/10.1007/s12264-016-0024-y] [PMID:  26983715] 
[49] 
Blank, S.; Seismann, H.; Bockisch, B.; Braren, I.; Cifuentes, L.; McIntyre, M.; Rühl, D.; Ring, J.; Bredehorst, R.; Ollert, M.W.; Grunwald, T.; Spillner, E. Identification, recombinant expression, and characterization of the 100 kDa high molecular weight Hymenoptera venom allergens Api m 5 and Ves v 3. J. Immunol.,  2010, 184(9), 5403-5413.
[http://dx.doi.org/10.4049/jimmunol.0803709] [PMID:  20348419] 
[50] 
Peiren, N.; de Graaf, D.C.; Brunain, M.; Bridts, C.H.; Ebo, D.G.; Stevens, W.J.; Jacobs, F.J. Molecular cloning and expression of icarapin, a novel IgE-binding bee venom protein. FEBS Lett.,  2006, 580(20), 4895-4899.
[http://dx.doi.org/10.1016/j.febslet.2006.08.005] [PMID:  16914147] 
[51] 
Blank, S.; Seismann, H.; Michel, Y.; McIntyre, M.; Cifuentes, L.; Braren, I.; Grunwald, T.; Darsow, U.; Ring, J.; Bredehorst, R.; Ollert, M.; Spillner, E. Api m 10, a genuine A. mellifera venom allergen, is clinically relevant but underrepresented in therapeutic extracts. Allergy,  2011, 66(10), 1322-1329.
[http://dx.doi.org/10.1111/j.1398-9995.2011.02667.x] [PMID:  21658068] 
[52] 
Piulachs, M.D.; Guidugli, K.R.; Barchuk, A.R.; Cruz, J.; Simões, Z.L.; Bellés, X. The vitellogenin of the honey bee, Apis mellifera: structural analysis of the cDNA and expression studies. Insect Biochem. Mol. Biol.,  2003, 33(4), 459-465.
[http://dx.doi.org/10.1016/S0965-1748(03)00021-3] [PMID:  12650694] 
[53] 
Kamakura, M. Royalactin induces queen differentiation in honeybees. Nature,  2011, 473(7348), 478-483.
[http://dx.doi.org/10.1038/nature10093] [PMID:  21516106] 
[54] 
Havukainen, H.; Underhaug, J.; Wolschin, F.; Amdam, G.; Halskau, Ø. A vitellogenin polyserine cleavage site: highly disordered conformation protected from proteolysis by phosphorylation. J. Exp. Biol.,  2012, 215(Pt 11), 1837-1846.
[http://dx.doi.org/10.1242/jeb.065623] [PMID:  22573762] 
[55] 
Blank, S.; Seismann, H.; McIntyre, M.; Ollert, M.; Wolf, S.; Bantleon, F.I.; Spillner, E. Vitellogenins are new high molecular weight components and allergens (Api m 12 and Ves v 6) of Apis mellifera and Vespula vulgaris venom. PLoS One,  2013, 8(4) e62009
[http://dx.doi.org/10.1371/journal.pone.0062009] [PMID:  23626765] 
[56] 
King, T.P.; Kochoumian, L.; Joslyn, A. Wasp venom proteins: phospholipase A1 and B. Arch. Biochem. Biophys.,  1984, 230(1), 1-12.
[http://dx.doi.org/10.1016/0003-9861(84)90080-8] [PMID:  6712224] 
[57] 
Henriksen, A.; King, T.P.; Mirza, O.; Monsalve, R.I.; Meno, K.; Ipsen, H.; Larsen, J.N.; Gajhede, M.; Spangfort, M.D. Major venom allergen of yellow jackets, Ves v 5: structural characterization of a pathogenesis-related protein superfamily. Proteins,  2001, 45(4), 438-448.
[http://dx.doi.org/10.1002/prot.1160] [PMID:  11746691] 
[58] 
Hoffman, D.R. Allergens in Hymenoptera venom XIV: IgE binding activities of venom proteins from three species of vespids. J. Allergy Clin. Immunol.,  1985, 75(5), 606-610.
[http://dx.doi.org/10.1016/0091-6749(85)90037-5] [PMID:  3989146] 
[59] 
King, T.P.; Spangfort, M.D. Structure and biology of stinging insect venom allergens. Int. Arch. Allergy Immunol.,  2000, 123(2), 99-106.
[http://dx.doi.org/10.1159/000024440] [PMID:  11060481] 
[60] 
Hoffman, D.R.; Wood, C.L. Allergens in Hymenoptera venom XI. Isolation of protein allergens from Vespula maculifrons (yellow jacket) venom. J. Allergy Clin. Immunol.,  1984, 74(1), 93-103.
[http://dx.doi.org/10.1016/0091-6749(84)90094-0] [PMID:  6736487] 
[61] 
Schiener, M.; Eberlein, B.; Moreno-Aguilar, C.; Pietsch, G.; Serrano, P.; McIntyre, M.; Schwarze, L.; Russkamp, D.; Biedermann, T.; Spillner, E.; Darsow, U.; Ollert, M.; Schmidt-Weber, C.B.; Blank, S. Application of recombinant antigen 5 allergens from seven allergy-relevant Hymenoptera species in diagnostics. Allergy,  2017, 72(1), 98-108.
[http://dx.doi.org/10.1111/all.13000] [PMID:  27496543] 
[62] 
King, T.P.; Lu, G.; Gonzalez, M.; Qian, N.; Soldatova, L. Yellow jacket venom allergens, hyaluronidase and phospholipase: sequence similarity and antigenic cross-reactivity with their hornet and wasp homologs and possible implications for clinical allergy. J. Allergy Clin. Immunol.,  1996, 98(3), 588-600.
[http://dx.doi.org/10.1016/S0091-6749(96)70093-3] [PMID:  8828537] 
[63] 
Lu, G.; Villalba, M.; Coscia, M.R.; Hoffman, D.R.; King, T.P. Sequence analysis and antigenic cross-reactivity of a venom allergen, antigen 5, from hornets, wasps, and yellow jackets. J. Immunol.,  1993, 150(7), 2823-2830.
[PMID:  8454859] 
[64] 
Kolarich, D.; Léonard, R.; Hemmer, W.; Altmann, F. The N-glycans of yellow jacket venom hyaluronidases and the protein sequence of its major isoform in Vespula vulgaris. FEBS J.,  2005, 272(20), 5182-5190.
[http://dx.doi.org/10.1111/j.1742-4658.2005.04841.x] [PMID:  16218950] 
[65] 
Skov, L.K.; Seppälä, U.; Coen, J.J.; Crickmore, N.; King, T.P.; Monsalve, R.; Kastrup, J.S.; Spangfort, M.D.; Gajhede, M. Structure of recombinant Ves v 2 at 2.0 Angstrom resolution: structural analysis of an allergenic hyaluronidase from wasp venom. Acta Crystallogr. D Biol. Crystallogr.,  2006, 62(Pt 6), 595-604.
[http://dx.doi.org/10.1107/S0907444906010687] [PMID:  16699186] 
[66] 
De Amici, M.; Barocci, F.; Caimmi, S.; Nespoli, L.; Licari, A.; Giuliani, G.; Marseglia, G. Clinical use of basophil activation test in drug, food and hymenoptera venom allergies. Minerva Pediatr.,  2019, 71(2), 209-217.
[http://dx.doi.org/10.23736/S0026-4946.18.05144-7] [PMID:  30299021] 
[67] 
Peternelj, A.; Silar, M.; Bajrovic, N.; Adamic, K.; Music, E.; Kosnik, M.; Korosec, P. Diagnostic value of the basophil activation test in evaluating Hymenoptera venom sensitization. Wien. Klin. Wochenschr.,  2009, 121(9-10), 344-348.
[http://dx.doi.org/10.1007/s00508-009-1174-y] [PMID:  19562299] 
[68] 
Mertens, M.; Amler, S.; Moerschbacher, B.M.; Brehler, R. Cross-reactive carbohydrate determinants strongly affect the results of the basophil activation test in hymenoptera-venom allergy. Clin. Exp. Allergy,  2010, 40(9), 1333-1345.
[http://dx.doi.org/10.1111/j.1365-2222.2010.03535.x] [PMID:  20545702] 
[69] 
Vos, B.; Kohler, J.; Muller, S.; Stretz, E.; Rueff, F.; Jakob, T. Spiking venom with rVes v 5 improves sensitivity of IgE detection in patients with allergy to Vespula venom. J. Allergy Clin. Immunol.,  2013, 131, 1225-1227.
[70] 
Sturm, G.J.; Böhm, E.; Trummer, M.; Weiglhofer, I.; Heinemann, A.; Aberer, W. The CD63 basophil activation test in Hymenoptera venom allergy: a prospective study. Allergy,  2004, 59(10), 1110-1117.
[http://dx.doi.org/10.1111/j.1398-9995.2004.00400.x] [PMID:  15355471] 
[71] 
Sturm, G.J.; Hemmer, W.; Hawranek, T.; Lang, R.; Ollert, M.; Spillner, E.; Blank, S.; Bokanovic, D.; Aberer, W. Detection of IgE to recombinant Api m 1 and rVes v 5 is valuable but not sufficient to distinguish bee from wasp venom allergy. J. Allergy Clin. Immunol.,  2011, 128, 247-248.
[72] 
Sturm, G.J.; Biló, M.B.; Bonadonna, P.; Hemmer, W.; Caruso, B.; Bokanovic, D.; Aberer, W. Ves v 5 can establish the diagnosis in patients without detectable specific IgE to wasp venom and a possible north-south difference in Api m 1 sensitization in Europe. J. Allergy Clin. Immunol.,  2012, 130(3), 817.
[http://dx.doi.org/10.1016/j.jaci.2012.05.047] [PMID:  22795371] 
[73] 
Jin, C.; Focke, M.; Léonard, R.; Jarisch, R.; Altmann, F.; Hemmer, W. Reassessing the role of hyaluronidase in yellow jacket venom allergy. J. Allergy Clin. Immunol.,  2010, 125(1), 184-90.e1.
[http://dx.doi.org/10.1016/j.jaci.2009.08.037] [PMID:  19910026] 
[74] 
Wypych, J.I.; Abeyounis, C.J.; Reisman, R.E. Analysis of differing patterns of cross-reactivity of honeybee and yellow jacket venom-specific IgE: use of purified venom fractions. Int. Arch. Allergy Appl. Immunol.,  1989, 89(1), 60-66.
[http://dx.doi.org/10.1159/000234924] [PMID:  2499550] 
[75] 
Hemmer, W.; Focke, M.; Kolarich, D.; Wilson, I.B.; Altmann, F.; Wöhrl, S.; Götz, M.; Jarisch, R. Antibody binding to venom carbohydrates is a frequent cause for double positivity to honeybee and yellow jacket venom in patients with stinging-insect allergy. J. Allergy Clin. Immunol.,  2001, 108(6), 1045-1052.
[http://dx.doi.org/10.1067/mai.2001.120013] [PMID:  11742287] 
[76] 
Hemmer, W.; Focke, M.; Kolarich, D.; Dalik, I.; Götz, M.; Jarisch, R. Identification by immunoblot of venom glycoproteins displaying immunoglobulin E-binding N-glycans as cross-reactive allergens in honeybee and yellow jacket venom. Clin. Exp. Allergy,  2004, 34(3), 460-469.
[http://dx.doi.org/10.1111/j.1365-2222.2004.01897.x] [PMID:  15005742] 
[77] 
Eberlein, B.; Krischan, L.; Darsow, U.; Ollert, M.; Ring, J. Double positivity to bee and wasp venom: improved diagnostic procedure by recombinant allergen-based IgE testing and basophil activation test including data about cross-reactive carbohydrate determinants. J. Allergy Clin. Immunol.,  2012, 130(1), 155-161.
[http://dx.doi.org/10.1016/j.jaci.2012.02.008] [PMID:  22421265] 
[78] 
Korošec, P.; Valenta, R.; Mittermann, I.; Celesnik, N.; Eržen, R.; Zidarn, M.; Košnik, M. Low sensitivity of commercially available rApi m 1 for diagnosis of honeybee venom allergy. J. Allergy Clin. Immunol.,  2011, 128(3), 671-673.
[http://dx.doi.org/10.1016/j.jaci.2011.03.012] [PMID:   21481443] 
[79] 
Jakob, T.; Kohler, J.; Blank, S.; Magnusson, U.; Huss-Marp, J.; Spillner, E.; Lidholm, J. Comparable IgE reactivity to natural and recombinant Api m 1 in cross-reactive carbohydrate determinant-negative patients with bee venom allergy. J. Allergy Clin. Immunol.,  2012, 130, 276-278.
[80] 
Biló, B.M.; Rueff, F.; Mosbech, H.; Bonifazi, F.; Oude-Elberink, J.N. Diagnosis of Hymenoptera venom allergy. Allergy,  2005, 60(11), 1339-1349.
[http://dx.doi.org/10.1111/j.1398-9995.2005.00963.x] [PMID:  16197464] 
[81] 
Korošec, P.; Valenta, R.; Mittermann, I.; Celesnik, N.; Silar, M.; Zidarn, M.; Košnik, M. High sensitivity of CAP-FEIA rVes v 5 and rVes v 1 for diagnosis of Vespula venom allergy. J. Allergy Clin. Immunol.,  2012, 129(5), 1406-1408.
[http://dx.doi.org/10.1016/j.jaci.2011.12.975] [PMID:  22277201] 
[82] 
Mittermann, I.; Zidarn, M.; Silar, M.; Markovic-Housley, Z.; Aberer, W.; Korosec, P.; Kosnik, M.; Valenta, R. Recombinant allergen-based IgE testing to distinguish bee and wasp allergy. J. Allergy Clin. Immunol.,  2010, 125(6), 1300-1307.e3.
[http://dx.doi.org/10.1016/j.jaci.2010.03.017] [PMID:  20466415] 
[83] 
Seismann, H.; Blank, S.; Cifuentes, L.; Braren, I.; Bredehorst, R.; Grunwald, T.; Ollert, M.; Spillner, E. Recombinant phospholipase A1 (Ves v 1) from yellow jacket venom for improved diagnosis of hymenoptera venom hypersensitivity. Clin. Mol. Allergy,  2010, 8, 7.
[http://dx.doi.org/10.1186/1476-7961-8-7] [PMID:  20359368] 
[84] 
King, T.P.; Alagon, A.C.; Kuan, J.; Sobotka, A.K.; Lichtenstein, L.M. Immunochemical studies of yellowjacket venom proteins. Mol. Immunol.,  1983, 20(3), 297-308.
[http://dx.doi.org/10.1016/0161-5890(83)90069-X] [PMID:  6865952] 
[85] 
Seismann, H.; Blank, S.; Braren, I.; Greunke, K.; Cifuentes, L.; Grunwald, T.; Bredehorst, R.; Ollert, M.; Spillner, E. Dissecting cross-reactivity in hymenoptera venom allergy by circumvention of alpha-1,3-core fucosylation. Mol. Immunol.,  2010, 47(4), 799-808.
[http://dx.doi.org/10.1016/j.molimm.2009.10.005] [PMID:  19896717] 
[86] 
Kucharewicz, I.; Bodzenta-Lukaszyk, A.; Szymanski, W.; Mroczko, B.; Szmitkowski, M. Basal serum tryptase level correlates with severity of hymenoptera sting and age. J. Investig. Allergol. Clin. Immunol.,  2007, 17(2), 65-69.
[PMID:  17460943] 
[87] 
Stoevesandt, J.; Sturm, G.; Bonadonna, P.; Oude, E.J.; Trautmann, A. Risk factors and indicators of severe systemic insect sting reactions. Allergy, 2019.
[http://dx.doi.org/10.1111/011.13945] 
[88] 
Soyyigit, S.; Arslan, S.; Caliskaner, A.Z. Investigation of the factors that determine the severity of allergic reactions to Hymenoptera venoms. Allergy Asthma Proc.,  2019, 40(2), 116-122.
[http://dx.doi.org/10.2500/aap.2019.40.4191] [PMID:  30819281] 
[89] 
Michel, J.; Brockow, K.; Darsow, U.; Ring, J.; Schmidt-Weber, C.B.; Grunwald, T.; Blank, S.; Ollert, M. Added sensitivity of component-resolved diagnosis in hymenoptera venom-allergic patients with elevated serum tryptase and/or mastocytosis. Allergy,  2016, 71(5), 651-660.
[http://dx.doi.org/10.1111/all.12850] [PMID:  26836051] 
[90] 
Golden, D.B.K.; Carter, M.C. Insect Sting Anaphylaxis-Or Mastocytosis-Or Something Else? J. Allergy Clin. Immunol. Pract.,  2019, 7(4), 1117-1123.
[http://dx.doi.org/10.1016/j.jaip.2019.01.014] [PMID:  30961837] 
[91] 
Pasaoglu, G.; Sin, B.A.; Misirligil, Z. Rush hymenoptera venom immunotherapy is efficacious and safe. J. Investig. Allergol. Clin. Immunol.,  2006, 16(4), 232-238.
[PMID:  16889280] 
[92] 
Hirata, H.; Asakura, T.; Arima, M.; Cheng, G.; Honda, K.; Fukushima, F.; Yamaguchi, B.; Yoshida, N.; Fukuda, T. Efficacy and safety of rush immunotherapy in patients with Hymenoptera allergy in Japan. Asian Pac. J. Allergy Immunol.,  2003, 21(2), 89-94.
[PMID:  14629126] 
[93] 
Van Vaerenbergh, M.; De Smet, L.; Rafei-Shamsabadi, D.; Blank, S.; Spillner, E.; Ebo, D.G.; Devreese, B.; Jakob, T.; de Graaf, D.C. IgE recognition of chimeric isoforms of the honeybee (Apis mellifera) venom allergen Api m 10 evaluated by protein array technology. Mol. Immunol.,  2015, 63(2), 449-455.
[http://dx.doi.org/10.1016/j.molimm.2014.09.018] [PMID:  25451974] 
[94] 
Frick, M.; Fischer, J.; Helbling, A.; Ruëff, F.; Wieczorek, D.; Ollert, M.; Pfützner, W.; Müller, S.; Huss-Marp, J.; Dorn, B.; Biedermann, T.; Lidholm, J.; Ruecker, G.; Bantleon, F.; Miehe, M.; Spillner, E.; Jakob, T. Predominant Api m 10 sensitization as risk factor for treatment failure in honey bee venom immunotherapy. J. Allergy Clin. Immunol.,  2016, 138(6), 1663-1671.e9.
[http://dx.doi.org/10.1016/j.jaci.2016.04.024] [PMID:  27372568] 
[95] 
Ruiz, B.; Serrano, P.; Verdú, M.; Moreno, C. Sensitization to Api m 1, Api m 2, and Api m 4: association with safety of bee venom immunotherapy. Ann. Allergy Asthma Immunol.,  2015, 114(4), 350-352.
[http://dx.doi.org/10.1016/j.anai.2015.01.010] [PMID:  25736542] 
[96] 
Vinson, S.B. Invasion of the red imported fire ant (hymenoptera: Formicidae) spread, biology, and impact. Am. Entomol. (Lanham Md.),  1997, 1997(Spring), 23-39.
[http://dx.doi.org/10.1093/ae/43.1.23] 
[97] 
Potiwat, R.; Sitcharungsi, R. Ant allergens and hypersensitivity reactions in response to ant stings. Asian Pac. J. Allergy Immunol.,  2015, 33(4), 267-275.
[PMID:  26708389] 
[98] 
Srisong, H.; Daduang, S.; Lopata, A.L. Current advances in ant venom proteins causing hypersensitivity reactions in the Asia-Pacific region. Mol. Immunol.,  2016, 69, 24-32.
[http://dx.doi.org/10.1016/j.molimm.2015.11.003] [PMID:  26641698] 
[99] 
Hoffman, D.R.; Smith, A.M.; Schmidt, M.; Moffitt, J.E.; Guralnick, M. Allergens in Hymenoptera venom. XXII. Comparison of venoms from two species of imported fire ants, Solenopsis invicta and richteri. J. Allergy Clin. Immunol.,  1990, 85(6), 988-996.
[http://dx.doi.org/10.1016/0091-6749(90)90042-3] [PMID:  2355158] 
[100] 
Wu, N.; Lu, W.; Luo, H.; He, Z.; He, J.; Liang, K.; Yang, C.; Ke, J.; Xiao, K. A survey on human bitten by red imported fire ants in mainland for the first time. Zhongguo Meijie Shengwuxue Ji Kongzhi Zazhi,  2005, 16(5), 342-344.
[101] 
Yun, Y.Y.; Ko, S.H.; Park, J.W.; Hong, C.S. Anaphylaxis to venom of the Pachycondyla species ant. J. Allergy Clin. Immunol.,  1999, 104(4 Pt 1), 879-882.
[http://dx.doi.org/10.1016/S0091-6749(99)70302-7] [PMID:  10518836] 
[102] 
Cho, Y.S.; Lee, Y.M.; Lee, C.K.; Yoo, B.; Park, H.S.; Moon, H.B. Prevalence of Pachycondyla chinensis venom allergy in an ant-infested area in Korea. J. Allergy Clin. Immunol.,  2002, 110(1), 54-57.
[http://dx.doi.org/10.1067/mai.2002.124890] [PMID:  12110820] 
[103] 
Kim, S.S.; Park, H.S.; Kim, H.Y.; Lee, S.K.; Nahm, D.H. Anaphylaxis caused by the new ant, Pachycondyla chinensis: demonstration of specific IgE and IgE-binding components. J. Allergy Clin. Immunol.,  2001, 107(6), 1095-1099.
[http://dx.doi.org/10.1067/mai.2001.114341] [PMID:  11398091] 
[104] 
Fukuzawa, M.; Arakura, F.; Yamazaki, Y.; Uhara, H.; Saida, T. Urticaria and anaphylaxis due to sting by an ant (Brachyponera chinensis). Acta Derm. Venereol.,  2002, 82(1), 59.
[http://dx.doi.org/10.1080/000155502753600939] [PMID:  12013203] 
[105] 
Dib, G.; Guerin, B.; Banks, W.A.; Leynadier, F. Systemic reactions to the Samsum ant: an IgE-mediated hypersensitivity. J. Allergy Clin. Immunol.,  1995, 96(4), 465-472.
[http://dx.doi.org/10.1016/S0091-6749(95)70288-1] [PMID:  7560656] 
[106] 
Shek, L.P.; Ngiam, N.S.; Lee, B.W. Ant allergy in Asia and Australia. Curr. Opin. Allergy Clin. Immunol.,  2004, 4(4), 325-328.
[http://dx.doi.org/10.1097/01.all.0000136761.51195.01] [PMID:  15238800] 
[107] 
Nelder, M.P.; Paysen, E.S.; Zungoli, P.A.; Benson, E.P. Emergence of the introduced ant Pachycondyla chinensis (Formicidae: Ponerinae) as a public health threat in the southeastern United States. J. Med. Entomol.,  2006, 43(5), 1094-1098.
[http://dx.doi.org/10.1093/jmedent/43.5.1094] [PMID:  17017251] 
[108] 
Kim, S.C.; Hong, C.S. A case of anaphylaxis by ant (Ectomomyrmex spp.) venom and measurements of specific IgE and IgG subclasses. Yonsei Med. J.,  1992, 33(3), 281-287.
[http://dx.doi.org/10.3349/ymj.1992.33.3.281] [PMID:  1292253] 
[109] 
Hoffman, D.R. Fire ant venom allergy. Allergy,  1995, 50(7), 535-544.
[http://dx.doi.org/10.1111/j.1398-9995.1995.tb01196.x] [PMID:  8588684] 
[110] 
Hoffman, D.R. Allergens in hymenoptera venom. XXVI: The complete amino acid sequences of two vespid venom phospholipases. Int. Arch. Allergy Immunol.,  1994, 104(2), 184-190.
[http://dx.doi.org/10.1159/000236728] [PMID:  8199462 ] 
[111] 
Hoffman, D.R.; Sakell, R.H.; Schmidt, M. Sol i 1, the phospholipase allergen of imported fire ant venom. J. Allergy Clin. Immunol.,  2005, 115(3), 611-616.
[http://dx.doi.org/10.1016/j.jaci.2004.11.020] [PMID:  15753912] 
[112] 
Hoffman, D.R. Allergens in Hymenoptera venom XXIV: the amino acid sequences of imported fire ant venom allergens Sol i II, Sol i III, and Sol i IV. J. Allergy Clin. Immunol.,  1993, 91(1 Pt 1), 71-78.
[http://dx.doi.org/10.1016/0091-6749(93)90298-T] [PMID:  8423273] 
[113] 
Schmidt, M.; Walker, R.B.; Hoffman, D.R.; McConnell, T.J. Nucleotide sequence of cDNA encoding the fire ant venom protein Sol i II. FEBS Lett.,  1993, 319(1-2), 138-140.
[http://dx.doi.org/10.1016/0014-5793(93)80053-W] [PMID:  8454046] 
[114] 
Hoffman, D.R.; Dove, D.E.; Moffitt, J.E.; Stafford, C.T. Allergens in Hymenoptera venom. XXI. Cross-reactivity and multiple reactivity between fire ant venom and bee and wasp venoms. J. Allergy Clin. Immunol.,  1988, 82(5 Pt 1), 828-834.
[http://dx.doi.org/10.1016/0091-6749(88)90085-1] [PMID:  3192866] 
[115] 
Lee, E.K.; Jeong, K.Y.; Lyu, D.P.; Lee, Y.W.; Sohn, J.H.; Lim, K.J.; Hong, C.S.; Park, J.W. Characterization of the major allergens of Pachycondyla chinensis in ant sting anaphylaxis patients. Clin. Exp. Allergy,  2009, 39(4), 602-607.
[http://dx.doi.org/10.1111/j.1365-2222.2008.03181.x] [PMID:  19178543] 
[116] 
Jeong, K.Y.; Yi, M.H.; Son, M.; Lyu, D.; Lee, J.H.; Yong, T.S.; Park, J.W. IgE Reactivity of Recombinant Pac c 3 from the Asian Needle Ant (Pachycondyla chinensis). Int. Arch. Allergy Immunol.,  2016, 169(2), 93-100.
[http://dx.doi.org/10.1159/000444364] [PMID:  27043037] 
Cite As
Current Protein & Peptide Science

Stinging Insect Allergens

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