Zhu J, Paul WE, 2008. CD4 T cells: fates, functions, and faults. Blood 112: 1557–1569.
Medzhitov R, Schneider DS, Soares MP, 2012. Disease tolerance as a defense strategy. Science 335: 936–941.
Strachan DP, 1989. Hay fever, hygiene, and household size. BMJ 299: 1259–1260.
Bach JF, 2002. The effect of infections on susceptibility to autoimmune and allergic diseases. N Engl J Med 347: 911–920.
Elliott DE, Weinstock JV, 2012. Where are we on worms? Curr Opin Gastroenterol 28: 551–556.
Aravindhan V, Mohan V, Surendar J, Rao MM, Ranjani H, Kumaraswami V, Nutman TB, Babu S, 2010. Decreased prevalence of lymphatic filariasis among subjects with type-1 diabetes. Am J Trop Med Hyg 83: 1336–1339.
Panda AK, Ravindran B, Das BK, 2013. Rheumatoid arthritis patients are free of filarial infection in an area where filariasis is endemic: comment on the article by Pineda et al. Arthritis Rheum 65: 1402–1403.
Pineda MA, McGrath MA, Smith PC, Al-Riyami L, Rzepecka J, Gracie JA, Harnett W, Harnett MM, 2012. The parasitic helminth product ES-62 suppresses pathogenesis in collagen-induced arthritis by targeting the interleukin-17-producing cellular network at multiple sites. Arthritis Rheum 64: 3168–3178.
Rocha FA, Leite AK, Pompeu MM, Cunha TM, Verri WA Jr, Soares FM, Castro RR, Cunha FQ, 2008. Protective effect of an extract from Ascaris suum in experimental arthritis models. Infect Immun 76: 2736–2745.
Hagel I, Lynch NR, Perez M, Di Prisco MC, Lopez R, Rojas E, 1993. Modulation of the allergic reactivity of slum children by helminthic infection. Parasite Immunol 15: 311–315.
van den Biggelaar AH, van Ree R, Rodrigues LC, Lell B, Deelder AM, Kremsner PG, Yazdanbakhsh M, 2000. Decreased atopy in children infected with Schistosoma haematobium: a role for parasite-induced interleukin-10. Lancet 356: 1723–1727.
Araujo MI, Lopes AA, Medeiros M, Cruz AA, Sousa-Atta L, Sole D, Carvalho EM, 2000. Inverse association between skin response to aeroallergens and Schistosoma mansoni infection. Int Arch Allergy Immunol 123: 145–148.
van den Biggelaar AH, Lopuhaa C, van Ree R, van der Zee JS, Jans J, Hoek A, Migombet B, Borrmann S, Luckner D, Kermsner PG, Yazdanbakhsh M, 2001. The prevalence of parasite infestation and house dust mite sensitization in Gabonese schoolchildren. Int Arch Allergy Immunol 126: 321–338.
Nyan OA, Walraven GE, Banya WA, Milligan P, Van Der Sande M, Ceesay SM, Del Prete G, McAdam KP, 2001. Atopy, intestinal helminth infection and total serum IgE in rural and urban adult Gambian communities. Clin Exp Allergy 31: 1672–1678.
Scrivener S, Yemaneberhan H, Zebenigus M, Tilahun D, Girma S, Ali S, McElroy P, Custovic A, Woodcock A, Pritchard D, Venn A, Britton J, 2001. Independent effects of intestinal parasite infection and domestic allergen exposure on risk of wheeze in Ethiopia: a nested case-control study. Lancet 358: 1493–1499.
Huang SL, Tsai PF, Yeh YF, 2002. Negative association of Enterobius infestation with asthma and rhinitis in primary school children in Taipei. Clin Exp Allergy 32: 1029–1032.
Cooper PJ, Chico ME, Bland M, Griffin GE, Nutman TB, 2003. Allergic symptoms, atopy, and geohelminth infections in a rural area of Ecuador. Am J Respir Crit Care Med 168: 313–317.
Cooper PJ, Chico ME, Rodrigues LC, Ordonez M, Strachan D, Griffin GE, Nutman TB, 2003. Reduced risk of atopy among school-age children infected with geohelminth parasites in a rural area of the tropics. J Allergy Clin Immunol 111: 995–1000.
Dagoye D, Bekele Z, Woldemichael K, Nida H, Yimam M, Hall A, Venn AJ, Britton JR, Hubbard R, Lewis SA, 2003. Wheezing, allergy, and parasite infection in children in urban and rural Ethiopia. Am J Respir Crit Care Med 167: 1369–1373.
Wahyuni S, Sartono E, Supali T, van der Zee JS, Mangali A, van Ree R, Houwing-Duistermaat JJ, Yazdanbakhsh M, 2005. Clustering of allergic outcomes within families and households in areas endemic for helminth infections. Int Arch Allergy Immunol 136: 356–364.
Flohr C, Tuyen LN, Lewis S, Quinnell R, Minh TT, Liem HT, Campbell J, Pritchard D, Hien TT, Farrar J, Williams H, Britton J, 2006. Poor sanitation and helminth infection protect against skin sensitization in Vietnamese children: a cross-sectional study. J Allergy Clin Immunol 118: 1305–1311.
Rodrigues LC, Newcombe PJ, Cunha SS, Alcantara-Neves NM, Genser B, Cruz AA, Simoes SM, Fiaccone R, Amorim L, Cooper PJ, Barreto ML, 2008. Early infection with Trichuris trichiura and allergen skin test reactivity in later childhood. Clin Exp Allergy 38: 1769–1777.
Endara P, Vaca M, Chico ME, Erazo S, Oviedo G, Quinzo I, Rodriguez A, Lovato R, Moncayo AL, Barreto ML, Rodrigues LC, Cooper PJ, 2010. Long-term periodic anthelmintic treatments are associated with increased allergen skin reactivity. Clin Exp Allergy 40: 1669–1677.
Supali T, Djuardi Y, Wibowo H, van Ree R, Yazdanbakhsh M, Sartono E, 2010. Relationship between different species of helminths and atopy: a study in a population living in helminth-endemic area in Sulawesi, Indonesia. Int Arch Allergy Immunol 153: 388–394.
Rujeni N, Nausch N, Bourke CD, Midzi N, Mduluza T, Taylor DW, Mutapi F, 2012. Atopy is inversely related to schistosome infection intensity: a comparative study in Zimbabwean villages with distinct levels of Schistosoma haematobium infection. Int Arch Allergy Immunol 158: 288–298.
Kanobana K, Vereecken K, Junco Diaz R, Sariego I, Rojas L, Bonet Gorbea M, Polman K, 2013. Toxocara seropositivity, atopy and asthma: a study in Cuban schoolchildren. Trop Med Int Health 18: 403–406.
Alcantara-Neves NM, Veiga RV, Dattoli VC, Fiaccone RL, Esquivel R, Cruz AA, Cooper PJ, Rodrigues LC, Barreto ML, 2012. The effect of single and multiple infections on atopy and wheezing in children. J Allergy Clin Immunol 129: 359–367.
Mendonca LR, Veiga RV, Dattoli VC, Figueiredo CA, Fiaccone R, Santos J, Cruz AA, Rodrigues LC, Cooper PJ, Pontes-de-Carvalho LC, Barreto ML, Alcantara-Neves NM, 2012. Toxocara seropositivity, atopy and wheezing in children living in poor neighbourhoods in urban Latin American. PLoS Negl Trop Dis 6: e1886.
Manuel AM, Kuljit S, Gopalakrishnan G, Suresh KG, Balraj P, 2012. The role of worm infestation in allergic rhinitis. Trop Biomed 29: 360–365.
Oliveira SM, Bezerra FS, Carneiro TR, Pinheiro MC, Queiroz JA, 2014. Association between allergic responses and Schistosoma mansoni infection in residents in a low-endemic setting in Brazil. Rev Soc Bras Med Trop 47: 770–774.
Davey G, Venn A, Belete H, Berhane Y, Britton J, 2005. Wheeze, allergic sensitization and geohelminth infection in Butajira, Ethiopia. Clin Exp Allergy 35: 301–307.
Ponte EV, Rasella D, Souza-Machado C, Stelmach R, Barreto ML, Cruz AA, 2014. Reduced asthma morbidity in endemic areas for helminth infections: a longitudinal ecological study in Brazil. J Asthma 51: 1022–1027.
Calvert J, Burney P, 2010. Ascaris, atopy, and exercise-induced bronchoconstriction in rural and urban South African children. J Allergy Clin Immunol 125: 100–105.
Vereecken K, Kanobana K, Wordemann M, Junco Diaz R, Menocal Heredia L, Ruiz Espinosa A, Nunez FA, Rojas Rivero L, Bonet Gorbea M, Polman K, 2012. Associations between atopic markers in asthma and intestinal helminth infections in Cuban schoolchildren. Pediatr Allergy Immunol 23: 332–338.
Souza V, Medeiros D, Sales I, Costa V, Silva A, Rizzo J, Sole D, Sarinho E, 2014. Ascaris lumbricoides infection in urban schoolchildren: specific IgE and IL-10 production. Allergol Immunopathol (Madr) 42: 206–211.
Alcantara-Neves NM, Britto GDSG, Veiga RV, Figueiredo CA, Fiaccone RL, da Conceicao JS, Cruz AA, Rodrigues LC, Cooper PJ, Pontes-de-Carvalho LC, Barreto ML, 2014. Effects of helminth co-infections on atopy, asthma and cytokine production in children living in a poor urban area in Latin America. BMC Res Notes 7: 817–827.
Hamid F, Wahyuni S, van Leeuwen A, van Ree R, Yazdanbakhsh M, Sartono E, 2015. Allergic disorders and socio-economic status: a study of schoolchildren in an urban area of Makassar, Indonesia. Clin Exp Allergy 45: 1226–1236.
Wordemann M, Diaz RJ, Heredia LM, Collado Madurga AM, Ruiz Espinosa A, Prado RC, Millan IA, Escobedo A, Rojas Rivero L, Gryseels B, Gorbea MB, Polman K, 2008. Association of atopy, asthma, allergic rhinoconjunctivitis, atopic dermatitis and intestinal helminth infections in Cuban children. Trop Med Int Health 13: 180–186.
Obeng BB, Amoah AS, Larbi IA, de Souza DK, Uh HW, Fernandez-Rivas M, van Ree R, Rodrigues LC, Boakye DA, Yazdanbakhsh M, Hartgers FC, 2014. Schistosome infection is negatively associated with mite atopy, but not wheeze and asthma in Ghanaian schoolchildren. Clin Exp Allergy 44: 965–975.
Kayhan B, Telatar H, Karacadag S, 1978. Bronchial asthma associated with intestinal parasites. Am J Gastroenterol 69: 605–606.
Joubert JR, van Schalkwyk DJ, Turner KJ, 1980. Ascaris lumbricoides and the human immunogenic response: enhanced IgE-mediated reactivity to common inhaled allergens. Bull World Health Organ 57: 409–412.
Alshishtawy MM, Abdella AM, Gelber LE, Chapman MD, 1991. Asthma in Tanta, Egypt: serologic analysis of total and specific IgE antibody levels and their relationship to parasite infection. Int Arch Allergy Appl Immunol 96: 348–354.
Buijs J, Borsboom G, Renting M, Hilgersom WJ, van Wieringen JC, Jansen G, Neijens J, 1997. Relationship between allergic manifestations and Toxocara seropositivity: a cross-sectional study among elementary school children. Eur Respir J 10: 1467–1475.
Lynch NR, Palenque M, Hagel I, DiPrisco MC, 1997. Clinical improvement of asthma after anthelminthic treatment in a tropical situation. Am J Respir Crit Care Med 156: 50–54.
Dold S, Heinrich J, Wichmann HE, Wjst M, 1998. Ascaris-specific IgE and allergic sensitization in a cohort of school children in the former East Germany. J Allergy Clin Immunol 102: 414–420.
Palmer LJ, Celedon JC, Weiss ST, Wang B, Fang Z, Xu X, 2002. Ascaris lumbricoides infection is associated with increased risk of childhood asthma and atopy in rural China. Am J Respir Crit Care Med 165: 1489–1493.
Benicio MH, Ferreira MU, Cardoso MR, Konno SC, Monteiro CA, 2004. Wheezing conditions in early childhood: prevalence and risk factors in the city of Sao Paulo, Brazil. Bull World Health Organ 82: 516–522.
Daschner A, Vega de la Osada F, Pascual CY, 2005. Allergy and parasites reevaluated: wide-scale induction of chronic urticaria by the ubiquitous fish-nematode Anisakis simplex in an endemic region. Allergol Immunopathol (Madr) 33: 31–37.
Obihara CC, Beyers N, Gie RP, Hoekstra MO, Fincham JE, Marais BJ, Lombard CJ, Dini LA, Kimpen JL, 2006. Respiratory atopic disease, Ascaris-immunoglobulin E and tuberculin testing in urban South African children. Clin Exp Allergy 36: 640–648.
Bahceciler NN, Ozdemir C, Kucukosmanoglu E, Arikan C, Over U, Karavelioglu S, Akkoc T, Yazi D, Yesil O, Soysal A, Bakir M, Barlan IB, 2007. Association between previous enterobiasis and current wheezing: evaluation of 1018 children. Allergy Asthma Proc 28: 174–182.
Pereira MU, Sly PD, Pitrez PM, Jones MH, Escouto D, Dias AC, Weiland SK, Stein RT, 2007. Nonatopic asthma is associated with helminth infections and bronchiolitis in poor children. Eur Respir J 29: 1154–1160.
Hagel I, Cabrera M, Hurtado MA, Sanchez P, Puccio F, Di Prisco MC, Palenque M, 2007. Infection by Ascaris lumbricoides and bronchial hyper reactivity: an outstanding association in Venezuelan school children from endemic areas. Acta Trop 103: 231–241.
Hunninghake GM, Soto-Quiros ME, Avila L, Ly NP, Liang C, Sylvia JS, Klanderman BJ, Silverman EK, Celedon JC, 2007. Sensitization to Ascaris lumbricoides and severity of childhood asthma in Costa Rica. J Allergy Clin Immunol 119: 654–661.
Alcantara-Neves NM, Badaro SJ, dos Santos MC, Pontes-de-Carvalho L, Barreto ML, 2010. The presence of serum anti-Ascaris lumbricoides IgE antibodies and of Trichuris trichiura infection are risk factors for wheezing and/or atopy in preschool-aged Brazilian children. Respir Res 11: 114.
Walsh MG, 2011. Toxocara infection and diminished lung function in a nationally representative sample from the United States population. Int J Parasitol 41: 243–247.
Choi MH, Chang YS, Lim MK, Bae YM, Hong ST, Oh JK, Yun EH, Bae MJ, Kwon HS, Lee SM, Park HW, Min KU, Kim YY, Cho SH, 2011. Clonorchis sinensis infection is positively associated with atopy in endemic area. Clin Exp Allergy 41: 697–705.
Moncayo AL, Vaca M, Oviedo G, Workman LJ, Chico ME, Platts-Mills TA, Rodrigues LC, Barreto ML, Cooper PJ, 2013. Effects of geohelminth infection and age on the associations between allergen-specific IgE, skin test reactivity and wheeze: a case-control study. Clin Exp Allergy 43: 60–72.
Buendia E, Zakzuk J, Mercado D, Alvarez A, Caraballo L, 2015. The IgE response to Ascaris molecular components is associated with clinical indicators of asthma severity. World Allergy Organ J 8: 8.
Webb EL, Nampijja M, Kaweesa J, Kizindo R, Namutebi M, Nakazibwe E, Oduru G, Kabubi P, Kabagenyi J, Nkurunungi G, Kizito D, Muhangi L, Akello M, Verweij JJ, Nerima B, Tukahebwa E, Elliott AM; LaVIISWA Trial Team, 2016. Helminths are positively associated with atopy and wheeze in Ugandan fishing communities: results from a cross-sectional survey. Allergy 71: 1156–1169.
Leonardi-Bee J, Pritchard D, Britton J, 2006. Asthma and current intestinal parasite infection: systematic review and meta-analysis. Am J Respir Crit Care Med 174: 514–523.
Feary J, Britton J, Leonardi-Bee J, 2011. Atopy and current intestinal parasite infection: a systematic review and meta-analysis. Allergy 66: 569–578.
Alcasid ML, Chiaramonte LT, Kim HJ, Zohn B, Bongiorno JR, Mullin W, 1973. Bronchial asthma and intestinal parasites. N Y State J Med 73: 1786–1788.
Turton JA, 1976. Letter: IgE, parasites, and allergy. Lancet 2: 686.
Turner KJ, Quinn EH, Anderson HR, 1978. Regulation of asthma by intestinal parasites. Investigation of possible mechanisms. Immunology 35: 281–288.
Tullis DC, 1970. Bronchial asthma associated with intestinal parasites. N Engl J Med 282: 370–372.
Van Dellen RG, Thompson JH Jr, 1971. Absence of intestinal parasites in asthma. N Engl J Med 285: 146–148.
Jarrett EE, Kerr JW, 1973. Threadworms and IgE in allergic asthma. Clin Allergy 3: 203–207.
Carswell F, Meakins RH, Harland PS, 1976. Parasites and asthma in Tanzanian children. Lancet 2: 706–707.
Macfarlane JT, Bachelor M, Ridyard JB, Ball PA, 1979. Asthma, IgE and environment in northern Nigeria. Clin Allergy 9: 333–337.
Mitre E, Norwood S, Nutman TB, 2005. Saturation of immunoglobulin E (IgE) binding sites by polyclonal IgE does not explain the protective effect of helminth infections against atopy. Infect Immun 73: 4106–4111.
Pritchard DI, Hooi DS, Brown A, Bockarie MJ, Caddick R, Quinnell RJ, 2007. Basophil competence during hookworm (Necator americanus) infection. Am J Trop Med Hyg 77: 860–865.
Ejrnaes AM, Bodtger U, Larsen JN, Svenson M, 2004. The blocking activity of birch pollen-specific immunotherapy-induced IgG4 is not qualitatively superior to that of other IgG subclasses. Mol Immunol 41: 471–478.
Strait RT, Morris SC, Finkelman FD, 2006. IgG-blocking antibodies inhibit IgE-mediated anaphylaxis in vivo through both antigen interception and Fc gamma RIIb cross-linking. J Clin Invest 116: 833–841.
Saxon A, Kepley C, Zhang K, 2008. “Accentuate the negative, eliminate the positive”: engineering allergy therapeutics to block allergic reactivity through negative signaling. J Allergy Clin Immunol 121: 320–325.
Zhu D, Kepley CL, Zhang M, Zhang K, Saxon A, 2002. A novel human immunoglobulin Fc gamma Fc epsilon bifunctional fusion protein inhibits Fc epsilon RI-mediated degranulation. Nat Med 8: 518–521.
Hussain R, Poindexter RW, Ottesen EA, 1992. Control of allergic reactivity in human filariasis. Predominant localization of blocking antibody to the IgG4 subclass. J Immunol 148: 2731–2737.
Kepley CL, Cambier JC, Morel PA, Lujan D, Ortega E, Wilson BS, Oliver JM, 2000. Negative regulation of FcepsilonRI signaling by FcgammaRII costimulation in human blood basophils. J Allergy Clin Immunol 106: 337–348.
Mertsching E, Bafetti L, Hess H, Perper S, Giza K, Allen LC, Negrou E, Hathaway K, Hopp J, Chung J, Perret D, Shields M, Saxon A, Kehry MR, 2008. A mouse Fcgamma-Fcepsilon protein that inhibits mast cells through activation of FcgammaRIIB, SH2 domain-containing inositol phosphatase 1, and SH2 domain-containing protein tyrosine phosphatases. J Allergy Clin Immunol 121: 441–447.
King CL, Medhat A, Malhotra I, Nafeh M, Helmy A, Khaudary J, Ibrahim S, ElSherbiny M, Zaky S, Stupi RJ, Brustoski K, Shehata M, Shata MT, 1996. Cytokine control of parasite-specific anergy in human urinary schistosomiasis: IL-10 modulates lymphocyte reactivity. J Immunol 156: 4715–4721.
Metenou S, Dembele B, Konate S, Dolo H, Coulibaly SY, Coulibaly YI, Diallo AA, Soumaoro L, Coulibaly ME, Sanogo D, Doumbia SS, Traore SF, Mahanty S, Klion A, Nutman TB, 2010. At homeostasis filarial infections have expanded adaptive T regulatory but not classical Th2 cells. J Immunol 184: 5375–5382.
Steel C, Guinea A, Ottesen EA, 1996. Evidence for protective immunity to bancroftian filariasis in the Cook Islands. J Infect Dis 174: 598–605.
Yazdanbakhsh M, Kremsner PG, van Ree R, 2002. Allergy, parasites, and the hygiene hypothesis. Science 296: 490–494.
Maizels RM, Yazdanbakhsh M, 2003. Immune regulation by helminth parasites: cellular and molecular mechanisms. Nat Rev Immunol 3: 733–744.
Taylor JJ, Mohrs M, Pearce EJ, 2006. Regulatory T cell responses develop in parallel to Th responses and control the magnitude and phenotype of the Th effector population. J Immunol 176: 5839–5847.
Metenou S, Coulibaly YI, Sturdevant D, Dolo H, Diallo AA, Soumaoro L, Coulibaly ME, Kanakabandi K, Porcella SF, Klion AD, Nutman TB, 2014. Highly heterogeneous, activated, and short-lived regulatory T cells during chronic filarial infection. Eur J Immunol 44: 2036–2047.
Wilson MS, Taylor MD, O'Gorman MT, Balic A, Barr TA, Filbey K, Anderton SM, Maizels RM, 2010. Helminth-induced CD19 + CD23hi B cells modulate experimental allergic and autoimmune inflammation. Eur J Immunol 40: 1682–1696.
Khan AR, Amu S, Saunders SP, Fallon PG, 2014. The generation of regulatory B cells by helminth parasites. Methods Mol Biol 1190: 143–162.
van der Vlugt LE, Zinsou JF, Ozir-Fazalalikhan A, Kremsner PG, Yazdanbakhsh M, Adegnika AA, Smits HH, 2014. Interleukin 10 (IL-10)-producing CD1dhi regulatory B cells from Schistosoma haematobium-infected individuals induce IL-10-positive T cells and suppress effector T-cell cytokines. J Infect Dis 210: 1207–1216.
Larson D, Hubner MP, Torrero MN, Morris CP, Brankin A, Swierczewski BE, Davies SJ, Vonakis BM, Mitre E, 2012. Chronic helminth infection reduces basophil responsiveness in an IL-10-dependent manner. J Immunol 188: 4188–4199.
Araujo MI, Hoppe B, Medeiros M Jr, Alcantara L, Almeida MC, Schriefer A, Oliveira RR, Kruschewsky R, Figueiredo JP, Cruz AA, Carvalho EM, 2004. Impaired T helper 2 response to aeroallergen in helminth-infected patients with asthma. J Infect Dis 190: 1797–1803.
Hartmann W, Haben I, Fleischer B, Breloer M, 2011. Pathogenic nematodes suppress humoral responses to third-party antigens in vivo by IL-10-mediated interference with Th cell function. J Immunol 187: 4088–4099.
Malisan F, Briere F, Bridon JM, Harindranath N, Mills FC, Max EE, Banchereau J, Martinez-Valdez H, 1996. Interleukin-10 induces immunoglobulin G isotype switch recombination in human CD40-activated naive B lymphocytes. J Exp Med 183: 937–947.
Jeannin P, Lecoanet S, Delneste Y, Gauchat JF, Bonnefoy JY, 1998. IgE versus IgG4 production can be differentially regulated by IL-10. J Immunol 160: 3555–3561.
Akdis CA, Blaser K, 1999. IL-10-induced anergy in peripheral T cell and reactivation by microenvironmental cytokines: two key steps in specific immunotherapy. FASEB J 13: 603–609.
van de Veen W, Stanic B, Yaman G, Wawrzyniak M, Sollner S, Akdis DG, Ruckert B, Akdis CA, Akdis M, 2013. IgG4 production is confined to human IL-10-producing regulatory B cells that suppress antigen-specific immune responses. J Allergy Clin Immunol 131: 1204–1212.
Wadee AA, Piessens WF, 1986. Microfilariae of Brugia malayi contain a T cell mitogen. Am J Trop Med Hyg 35: 141–147.
Urban JF Jr, Katona IM, Paul WE, Finkelman FD, 1991. Interleukin 4 is important in protective immunity to a gastrointestinal nematode infection in mice. Proc Natl Acad Sci USA 88: 5513–5517.
Liwski RS, Lee TD, 1999. Nematode infection enhances survival of activated T cells by modulating accessory cell function. J Immunol 163: 5005–5012.
Donnelly S, Dalton JP, Loukas A, 2006. Proteases in helminth- and allergen-induced inflammatory responses. Chem Immunol Allergy 90: 45–64.
Devlin MG, Gasser RB, Cocks TM, 2007. Initial support for the hypothesis that PAR2 is involved in the immune response to Nippostrongylus brasiliensis in mice. Parasitol Res 101: 105–109.
Liang G, Barker T, Xie Z, Charles N, Rivera J, Druey KM, 2012. Naive T cells sense the cysteine protease allergen papain through protease-activated receptor 2 and propel TH2 immunity. J Allergy Clin Immunol 129: 1377–1386.
Park MK, Cho MK, Kang SA, Park HK, Kim YS, Kim KU, Ahn SC, Kim DH, Yu HS, 2011. Protease-activated receptor 2 is involved in Th2 responses against Trichinella spiralis infection. Korean J Parasitol 49: 235–243.
Kouzaki H, O'Grady SM, Lawrence CB, Kita H, 2009. Proteases induce production of thymic stromal lymphopoietin by airway epithelial cells through protease-activated receptor-2. J Immunol 183: 1427–1434.
Snelgrove RJ, Gregory LG, Peiro T, Akthar S, Campbell GA, Walker SA, Lloyd CM, 2014. Alternaria-derived serine protease activity drives IL-33-mediated asthma exacerbations. J Allergy Clin Immunol 134: 583–592.
Yamaguchi R, Yamamoto T, Sakamoto A, Ishimaru Y, Narahara S, Sugiuchi H, Hirose E, Yamaguchi Y, 2015. Mechanism of interleukin-13 production by granulocyte-macrophage colony-stimulating factor-dependent macrophages via protease-activated receptor-2. Blood Cells Mol Dis 55: 21–26.
Bartemes KR, Kephart GM, Fox SJ, Kita H, 2014. Enhanced innate type 2 immune response in peripheral blood from patients with asthma. J Allergy Clin Immunol 134: 671–678.
Boyd A, Killoran K, Mitre E, Nutman TB, 2015. Pleural cavity type 2 innate lymphoid cells precede Th2 expansion in murine Litomosoides sigmodontis infection. Exp Parasitol 159: 118–126.
Klein Wolterink RG, Kleinjan A, van Nimwegen M, Bergen I, de Bruijn M, Levani Y, Hendriks RW, 2012. Pulmonary innate lymphoid cells are major producers of IL-5 and IL-13 in murine models of allergic asthma. Eur J Immunol 42: 1106–1116.
Oliphant CJ, Hwang YY, Walker JA, Salimi M, Wong SH, Brewer JM, Englezakis A, Barlow JL, Hams E, Scanlon ST, Ogg GS, Fallon PG, McKenzie AN, 2014. MHCII-mediated dialog between group 2 innate lymphoid cells and CD4+ T cells potentiates type 2 immunity and promotes parasitic helminth expulsion. Immunity 41: 283–295.
Halim TY, Hwang YY, Scanlon ST, Zaghouani H, Garbi N, Fallon PG, McKenzie AN, 2016. Group 2 innate lymphoid cells license dendritic cells to potentiate memory TH2 cell responses. Nat Immunol 17: 57–64.
Harris N, Gause WC, 2010. To B or not to B: B cells and the Th2-type immune response to helminths. Trends Immunol 32: 80–88.
Cooper PJ, Espinel I, Wieseman M, Paredes W, Espinel M, Guderian RH, Nutman TB, 1999. Human onchocerciasis and tetanus vaccination: impact on the postvaccination antitetanus antibody response. Infect Immun 67: 5951–5957.
Jarrett E, Bazin H, 1974. Elevation of total serum IgE in rats following helminth parasite infection. Nature 251: 613–614.
Orr TS, Blair AM, 1969. Potentiated reagin response to egg albumin and conalbumin in Nippostrongylus brasiliensis infected rats. Life Sci 8: 1073–1077.
Santiago HC, Ribeiro-Gomes FL, Bennuru S, Nutman TB, 2015. Helminth infection alters IgE responses to allergens structurally related to parasite proteins. J Immunol 194: 93–100.
Suzuki M, Hara M, Ichikawa S, Kamijo S, Nakazawa T, Hatanaka H, Akiyama K, Ogawa H, Okumura K, Takai T, 2016. Presensitization to Ascaris antigens promotes induction of mite-specific IgE upon mite antigen inhalation in mice. Allergol Int 65: 44–51.
Pascual CY, Crespo JF, San Martin S, Ornia N, Ortega N, Caballero T, Munoz-Pereira M, Martin-Esteban M, 1997. Cross-reactivity between IgE-binding proteins from Anisakis, German cockroach, and chironomids. Allergy 52: 514–520.
Huang CH, Liew LM, Mah KW, Kuo IC, Lee BW, Chua KY, 2006. Characterization of glutathione S-transferase from dust mite, Der p 8 and its immunoglobulin E cross-reactivity with cockroach glutathione S-transferase. Clin Exp Allergy 36: 369–376.
Acevedo N, Sanchez J, Erler A, Mercado D, Briza P, Kennedy M, Fernandez A, Gutierrez M, Chua KY, Cheong N, Jimenez S, Puerta L, Caraballo L, 2009. IgE cross-reactivity between Ascaris and domestic mite allergens: the role of tropomyosin and the nematode polyprotein ABA-1. Allergy 64: 1635–1643.
Caraballo L, Acevedo N, 2011. Allergy in the tropics: the impact of cross-reactivity between mites and Ascaris. Front Biosci 3: 51–64.
Santiago HC, Bennuru S, Boyd A, Eberhard M, Nutman TB, 2011. Structural and immunologic cross-reactivity among filarial and mite tropomyosin: implications for the hygiene hypothesis. J Allergy Clin Immunol 127: 479–486.
Santiago HC, LeeVan E, Bennuru S, Ribeiro-Gomes F, Mueller E, Wilson M, Wynn T, Garboczi D, Urban J, Mitre E, Nutman TB, 2012. Molecular mimicry between cockroach and helminth glutathione S-transferases promotes cross-reactivity and cross-sensitization. J Allergy Clin Immunol 130: 248–256.
Valmonte GR, Cauyan GA, Ramos JD, 2012. IgE cross-reactivity between house dust mite allergens and Ascaris lumbricoides antigens. Asia Pac Allergy 2: 35–44.
Nakazawa T, Khan AF, Yasueda H, Saito A, Fukutomi Y, Takai T, Zaman K, Yunus M, Takeuchi H, Iwata T, Akiyama K, 2013. Immunization of rabbits with nematode Ascaris lumbricoides antigens induces antibodies cross-reactive to house dust mite Dermatophagoides farinae antigens. Biosci Biotechnol Biochem 77: 145–150.
Fitzsimmons CM, Falcone FH, Dunne DW, 2014. Helminth allergens, parasite-specific IgE, and its protective role in human immunity. Front Immunol 5: 61.
Rodriguez-Perez R, Monsalve RI, Galan A, Perez-Pinar T, Umpierrez A, Lluch-Bernal M, Polo F, Caballero ML, 2014. Cross-reactivity between Anisakis spp. and wasp venom allergens. Int Arch Allergy Immunol 163: 179–184.
Mueller GA, Pedersen LC, Glesner J, Edwards LL, Zakzuk J, London RE, Arruda LK, Chapman MD, Caraballo L, Pomes A, 2015. Analysis of glutathione S-transferase allergen cross-reactivity in a North American population: relevance for molecular diagnosis. J Allergy Clin Immunol 136: 1369–1377.
Santos AB, Rocha GM, Oliver C, Ferriani VP, Lima RC, Palma MS, Sales VS, Aalberse RC, Chapman MD, Arruda LK, 2008. Cross-reactive IgE antibody responses to tropomyosins from Ascaris lumbricoides and cockroach. J Allergy Clin Immunol 121: 1040–1046.
Reese G, Ayuso R, Lehrer SB, 1999. Tropomyosin: an invertebrate pan-allergen. Int Arch Allergy Immunol 119: 247–258.
Acevedo N, Caraballo L, 2011. IgE cross-reactivity between Ascaris lumbricoides and mite allergens: possible influences on allergic sensitization and asthma. Parasite Immunol 33: 309–321.
Sereda MJ, Hartmann S, Lucius R, 2008. Helminths and allergy: the example of tropomyosin. Trends Parasitol 24: 272–278.
Santiago HC, Bennuru S, Ribeiro JM, Nutman TB, 2012. Structural differences between human proteins and aero- and microbial allergens define allergenicity. PLoS One 7: e40552.
Tyagi N, Farnell EJ, Fitzsimmons CM, Ryan S, Tukahebwa E, Maizels RM, Dunne DW, Thornton JM, Furnham N, 2015. Comparisons of allergenic and metazoan parasite proteins: allergy the price of immunity. PLOS Comput Biol 11: e1004546.
Jeong KY, Jeong KJ, Yi MH, Lee H, Hong CS, Yong TS, 2009. Allergenicity of sigma and delta class glutathione S-transferases from the German cockroach. Int Arch Allergy Immunol 148: 59–64.
Shankar J, Gupta PD, Sridhara S, Singh BP, Gaur SN, Arora N, 2005. Immunobiochemical analysis of cross-reactive glutathione-S-transferase allergen from different fungal sources. Immunol Invest 34: 37–51.
Shankar J, Singh BP, Gaur SN, Arora N, 2006. Recombinant glutathione-S-transferase a major allergen from Alternaria alternata for clinical use in allergy patients. Mol Immunol 43: 1927–1932.
Acevedo N, Mohr J, Zakzuk J, Samonig M, Briza P, Erler A, Pomes A, Huber CG, Ferreira F, Caraballo L, 2013. Proteomic and immunochemical characterization of glutathione transferase as a new allergen of the nematode Ascaris lumbricoides. PLoS One 8: e78353.
Hong SJ, Yun Kim T, Gan XX, Shen LY, Sukontason K, Kang SY, 2002. Clonorchis sinensis: glutathione S-transferase as a serodiagnostic antigen for detecting IgG and IgE antibodies. Exp Parasitol 101: 231–233.
Hayes JD, Flanagan JU, Jowsey IR, 2005. Glutathione transferases. Annu Rev Pharmacol Toxicol 45: 51–88.
Acevedo N, Erler A, Briza P, Puccio F, Ferreira F, Caraballo L, 2011. Allergenicity of Ascaris lumbricoides tropomyosin and IgE sensitization among asthmatic patients in a tropical environment. Int Arch Allergy Immunol 154: 195–206.
Fernandes J, Reshef A, Patton L, Ayuso R, Reese G, Lehrer SB, 2003. Immunoglobulin E antibody reactivity to the major shrimp allergen, tropomyosin, in unexposed Orthodox Jews. Clin Exp Allergy 33: 956–961.
Purohit A, Shao J, Degreef JM, van Leeuwen A, van Ree R, Pauli G, de Blay F, 2007. Role of tropomyosin as a cross-reacting allergen in sensitization to cockroach in patients from Martinique (French Caribbean island) with a respiratory allergy to mite and a food allergy to crab and shrimp. Eur Ann Allergy Clin Immunol 39: 85–88.
Wang J, Calatroni A, Visness CM, Sampson HA, 2011. Correlation of specific IgE to shrimp with cockroach and dust mite exposure and sensitization in an inner-city population. J Allergy Clin Immunol 128: 834–837.
Past two years | Past Year | Past 30 Days | |
---|---|---|---|
Abstract Views | 12 | 12 | 12 |
Full Text Views | 710 | 295 | 8 |
PDF Downloads | 368 | 140 | 8 |
There is much debate about the interaction between helminths and allergic disease. The “Hygiene Hypothesis,” a very popular concept among scientists and the lay public, states that infections, especially during childhood, can protect against allergic diseases. Indeed, helminth infections are known to induce regulatory responses in the host that can help the control of inflammation (including allergic inflammation). However, these infections also induce type-2-associated immune responses including helminth-specific IgE that can cross-react against environmental allergens and mediate IgE-driven effector responses. Thus, it is the delicate balance between the parasites' anti- and pro-allergenic effects that define the helminth/allergy interface.
Financial support: This work was supported, in part, by the Division of Intramural Research (DIR), National Institute of Allergy and Infectious Diseases (NIAID), the Conselho Nacional de Pesquisa (CNPq), and the Fundação de Amparo a Pesquisa de Minas Gerais (Fapemig).
Authors' addresses: Helton C. Santiago, Departamento de Bioquímica e Imunologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, Brazil, E-mail: heltonsantiago@icb.ufmg.br. Thomas B. Nutman, Laboratory of Parasitic Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, E-mail: tnutman@niaid.nih.gov.