The evolution of the Th2 immune responses and its relationships with parasitic diseases and allergy
Abstract
A variety of links occur between parasites, particularly helminths, and allergic diseases--both common conditions of epidemiological importance in tropical regions. Although speculations are often made about the effects of parasitic diseases on the evolution of the immune system, the selective forces that have shaped the allergic response are unknown and probably include evolutionary mechanisms different to those traditionally reported. Helminths, infectious and antigenic sources that induce allergiclike responses, established themselves as parasites in organisms that already had cell groups related to the type 2 immunity. An essential component in the relationship between helminths and their hosts is that the former induce immunosuppression, creating a kind of balance that allows the survival of both. The development of this equilibrium undoubtedly includes adaptations in both organisms, and the survival of the parasite is the result of (a) acquiring immune suppressor mechanisms and (b) finding hosts with lower intensity of the type 2 response. This in turn suggests that although helminth infections have influenced the formation of type 2 immunity, they have not been an important selective force in the
particular case of allergic response. The latter is more related to an exaggerated Th2/IgE response.
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References
Allen JE, Maizels RM. Diversity and dialogue in immunity to helminths. Nat Rev Immunol. 2011;11:375-88.
Moro K, Yamada T, Tanabe M, Takeuchi T, Ikawa T, Kawamoto H, et al. Innate production of T(H)2 cytokines by adipose tissue-associated c-Kit(+)Sca-1(+) lymphoid cells. Nature. 2010;463:540-4.
Neill DR, Wong SH, Bellosi A, Flynn RJ, Daly M, Langford TK, et al. Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity. Nature. 2010;464:1367-70.
Sáenz SA, Siracusa MC, Perrigoue JG, Spencer SP, Urban JF Jr, Tocker JE, et al. IL25 elicits a multipotent progenitor cell population that promotes T(H)2 cytokine responses. Nature. 2010;464:1362-6.
Jenkins SJ, Ruckerl D, Cook PC, Jones LH, Finkelman FD, van Rooijen N, et al. Local macrophage proliferation, rather than recruitment from the blood, is a signature of TH2 inflammation. Science. 2011;332:1284-8.
McCoy KD, Harris NL, Diener P, Hatak S, Odermatt B, Hangartner L, et al. Natural IgE production in the absence of MHC Class II cognate help. Immunity. 2006;24:329-39.
Mattes J, Collison A, Plank M, Phipps S, Foster PS. Antagonism of microRNA-126 suppresses the effector function of TH2 cells and the development of allergic airways disease. Proc Natl Acad Sci U S A. 2009;106:18704-9.
Mousavi M, Rabbani H, Hammarstrom L. Characterization of the bovine epsilon gene. Immunology. 1997;92:369-73.
Sakoyama Y, Hong KJ, Byun SM, Hisajima H, Ueda S, Yaoita Y, et al. Nucleotide sequences of immunoglobulin epsilon genes of chimpanzee and orangutan: DNA molecular clock and hominoid evolution. Proc Natl Acad Sci U S A. 1987 84:1080-4.
Vernersson M, Pejler G, Kristersson T, Alving K, Hellman L. Cloning, structural analysis, and expression of the pig IgE epsilon chain. Immunogenetics. 1997;46:461-8.
Faith RE, Clem LW. Passive cutaneous anaphylaxis in the chicken. Biological fractionation of the mediating antibody
population. Immunology. 1973;25:151-64.
Jurd RD. Hypersensitivity in fishes: A review. J Fish Biol. 1987;31:1-7.
Miller NW. In vitro culture approaches for studying immune cell functions in ectothermic vertebrates. Dev Comp lmmunol. 1994;18(Suppl.1):S132.
Jackson JA, Friberg IM, Little S, Bradley JE. Review series on helminths, immune modulation and the hygiene hypothesis. Immunity against helminths and immunological phenomena in modern human populations: Coevolutionary legacies? Immunology. 2009;126:18-27.
Hu YL, Xiang LX, Shao JZ. Identification and characterization of a novel immunoglobulin Z isotype in zebrafish: Implications for a distinct B cell receptor in lower vertebrates. Mol Immunol. 2010;47:738-46.
Paul W. Fundamental Immunology. 6th edition. Philadelphia: Lippincott Williams and Wilkins; 2008.
Sung SC, Cheng CH, Chou CM, Chu CY, Chen GD, Hwang PP, et al. Expression and characterization of a constitutively active STAT6 from Tetraodon. Fish Shellfish Immunol. 2010;28:819-28.
Hirasawa R, Shimizu R, Takahashi S, Osawa M, Takayanagi S, Kato Y, et al. Essential and instructive roles of GATA factors in eosinophil development. J Exp Med. 2002;195:1379-86.
Gould HJ, Sutton BJ. IgE in allergy and asthma today. Nat Rev Immunol. 2008;8:205-17.
Oettgen HC, Martin TR, Wynshaw-Boris A, Deng C, Drazen JM, Leder P. Active anaphylaxis in IgE-deficient mice. Nature. 1994;370:367-70.
Altin J, Shen C, Liston A. Understanding the genetic regulation of IgE production. Blood Rev. 2010;24:163-9.
McSharry C, Xia Y, Holland CV, Kennedy MW. Natural immunity to Ascaris lumbricoides associated with immunoglobulin E antibody to ABA-1 allergen and inflammation indicators in children. Infect Immun. 1999;67:484-9.
Karagiannis SN, Wang Q, East N, Burke F, Riffard S, Bracher MG, et al. Activity of human monocytes in IgE antibody-dependent surveillance and killing of ovarian tumor cells. Eur J Immunol. 2003;33:1030-40.
Melbye M, Smedby KE, Lehtinen T, Rostgaard K, Glimelius B, Munksgaard L, et al. Atopy and risk of non-Hodgkin lymphoma. J Natl Cancer Inst. 2007;99:158-66.
Wiemels JL, Wiencke JK, Patoka J, Moghadassi M, Chew T, McMillan A, et al. Reduced immunoglobulin E and allergy among adults with glioma compared with controls. Cancer Res. 2004;64:8468-73.
Riemer AB, Untersmayr E, Knittelfelder R, Duschl A, Pehamberger H, Zielinski CC, et al. Active induction of tumor-specific IgE antibodies by oral mimotope vaccination. Cancer Res. 2007;67:3406-11.
Gambon-Deza F, Sánchez-Espinel C, Magadan-Mompo S. The immunoglobulin heavy chain locus in the platypus (Ornithorhynchus anatinus). Mol Immunol. 2009;46:2515-23.
Fellah JS, Kerfourn F, Wiles MV, Schwager J, Charlemagne J. Phylogeny of immunoglobulin heavy chain isotypes: Structure of the constant region of Ambystoma mexicanum upsilon chain deduced from cDNA sequence. Immunogenetics. 1993;38:311-7.
Mussmann R, Wilson M, Marcuz A, Courtet M, Du Pasquier L. Membrane exon sequences of the three Xenopus Ig classes explain the evolutionary origin of mammalian isotypes. Eur J Immunol. 1996;26:409-14.
Taylor AI, Gould HJ, Sutton BJ, Calvert RA. Avian IgY binds to a monocyte receptor with IgG-like kinetics despite an IgE-like structure. J Biol Chem. 2008;283:16384-90.
Huising MO, Kruiswijk CP, Flik G. Phylogeny and evolution of class-I helical cytokines. J Endocrinol. 2006;189:1-25.
Avery S, Rothwell L, Degen WD, Schijns VE, Young J, Kaufman J, et al. Characterization of the first nonmammalian T2 cytokine gene cluster: The cluster contains functional single-copy genes for IL-3, IL-4, IL-13, and GM-CSF, a gene for IL-5 that appears to be a pseudogene, and a gene encoding another cytokinelike transcript, KK34. J Interferon Cytokine Res. 2004;24:600-10.
Li JH, Shao JZ, Xiang LX, Wen Y. Cloning, characterization and expression analysis of pufferfish interleukin-4 cDNA: The first evidence of Th2-type cytokine in fish. Mol Immunol. 2007;44:2078-86.
Liongue C, Ward AC. Evolution of class I cytokine receptors. BMC Evol Biol. 2007;7:120.
Giulianini PG, Bierti M, Lorenzon S, Battistella S, Ferrero EA. Ultrastructural and functional characterization of circulating hemocytes from the freshwater crayfish Astacus leptodactylus: Cell types and their role after in vivo artificial
non-self challenge. Micron. 2007;38:49-57.
Balla KM, Lugo-Villarino G, Spitsbergen JM, Stachura DL, Hu Y, Banuelos K, et al. Eosinophils in the zebrafish: Prospective isolation, characterization, and eosinophilia induction by helminth determinants. Blood. 2010;116:3944-54.
Klion AD, Nutman TB. The role of eosinophils in host defense against helminth parasites. J Allergy Clin Immunol. 2004;113:30-7.
Zhang J, Rosenberg HF, Nei M. Positive Darwinian selection after gene duplication in primate ribonuclease genes. Proc Natl Acad Sci USA. 1998;95:3708-13.
Lee JJ, Lee NA. Eosinophil degranulation: An evolutionary vestige or a universally destructive effector function? Clin Exp Allergy. 2005;35:986-94.
de Barros CM, Andrade LR, Allodi S, Viskov C, Mourier PA, Cavalcante MC, et al. The hemolymph of the ascidian Styela plicata (Chordata-Tunicata) contains heparin inside basophil-like cells and a unique sulfated galactoglucan in the plasma. J Biol Chem. 2007;282:1615-26.
Crivellato E, Ribatti D. The mast cell: An evolutionary perspective. Biol Rev Camb Philos Soc. 2010;85:347-60.
Reite OB, Evensen O. Inflammatory cells of teleostean fish: A review focusing on mast cells/eosinophilic granule cells and rodlet cells. Fish Shellfish Immunol. 2006;20:192-208.
Matsuyama T, Lida T. Degranulation of eosinophilic granular cells with possible involvement in neutrophil migration to site of inflammation in tilapia. Dev Comp Immunol. 1999;23:451-7.
Fey F. Vergleichende hamozytologie niederer Vertebraten. III. Granulozyten. Folia Haematol. 1966;86:1-20.
Rowley A, Hunt T, Page M. Fish. In: Rowley AF, Ratcliffe NA, editors. Vertebrate blood cells. Cambridge: Cambridge University Press; 1988.
Arinobu Y, Iwasaki H, Akashi K. Origin of basophils and mast cells. Allergol Int. 2009;58:21-8.
Chang YJ, Kim HY, Albacker LA, Baumgarth N, McKenzie AN, Smith DE, et al. Innate lymphoid cells mediate influenza-induced airway hyper-reactivity independently of adaptive immunity. Nat Immunol. 2011;12:631-8.
Schmid-Hempel P. Parasite immune evasion: A momentous molecular war. Trends Ecol Evol. 2008;23:318-26.
Anderson RM, May RM. Coevolution of hosts and parasites. Parasitology. 1982;85:411-26.
LoVerde PT, DeWald J, Minchella DJ, Bosshardt SC, Damian RT. Evidence for host-induced selection in Schistosoma mansoni. J Parasitol. 1985;71:297-301.
Littlewood DT, Curini-Galletti M, Herniou EA. The interrelationships of proseriata (Platyhelminthes: seriata) tested with molecules and morphology. Mol Phylogenet Evol. 2000;16:449-66.
Varki A, Altheide TK. Comparing the human and chimpanzee genomes: Searching for needles in a haystack. Genome Res. 2005;15:1746-58.
Caporale LH. Natural selection and the emergence of a mutation phenotype: An update of the evolutionary synthesis considering mechanisms that affect genome variation. Annu Rev Microbiol. 2003;57:467-85.
Bethony J, Loukas A, Smout M, Brooker S, Mendez S, Plieskatt J, et al. Antibodies against a secreted protein from hookworm larvae reduce the intensity of hookworm infection in humans and vaccinated laboratory animals. FASEB J. 2005;19:1743-5.
Turner JD, Faulkner H, Kamgno J, Kennedy MW, Behnke J, Boussinesq M, et al. Allergen-specific IgE and IgG4 are markers of resistance and susceptibility in a human intestinal nematode infection. Microbes Infect. 2005;7:990-6.
Dunne DW, Butterworth AE, Fulford AJ, Kariuki HC, Langley JG, Ouma JH, et al. Immunity after treatment of human schistosomiasis: Association between IgE antibodies to adult worm antigens and resistance to reinfection. Eur J Immunol. 1992;22:1483-94.
Pinot de Moira A, Fulford AJ, Kabatereine NB, Ouma JH, Booth M, Dunne DW. Analysis of complex patterns of human exposure and immunity to Schistosomiasis mansoni: The influence of age, sex, ethnicity and IgE. PLoS Negl Trop Dis. 2010;4:e820.
Lee JJ, Jacobsen EA, McGarry MP, Schleimer RP, Lee NA. Eosinophils in health and disease: The LIAR hypothesis. Clin Exp Allergy. 2010;40:563-75.
Maizels RM, Kurniawan-Atmadja A. Variation and polymorphism in helminth parasites. Parasitology. 2002;125(Suppl.):S25-37.
Dunne DW, Cooke A. A worm’s eye view of the immune system: Consequences for evolution of human autoimmune disease. Nat Rev Immunol. 2005;5:420-6.
Fernández-Caldas E, Puerta L, Caraballo L, Lockey RF. Mite allergens. Clin Allergy Immunol. 2008;21:161-82.
Grant AV, Araujo MI, Ponte EV, Oliveira RR, Cruz AA, Barnes KC, et al. Polymorphisms in IL10 are associated with total immunoglobulin E levels and Schistosoma mansoni infection intensity in a Brazilian population. Genes Immun. 2011;12:46-50.
Moller M, Gravenor MB, Roberts SE, Sun D, Gao P, Hopkin JM. Genetic haplotypes of Th-2 immune signalling link allergy to enhanced protection to parasitic worms. Hum Mol Genet. 2007;16:1828-36.
Fumagalli M, Pozzoli U, Cagliani R, Comi GP, Bresolin N, Clerici M, et al. The landscape of human genes involved in the immune response to parasitic worms. BMC Evol Biol. 2010;10:264.
Acevedo N, Mercado D, Vergara C, Sánchez J, Kennedy MW, Jiménez S, et al. Association between total immunoglobulin E and antibody responses to naturally acquired Ascaris lumbricoides infection and polymorphisms of immune system-related LIG4, TNFSF13B and IRS2 genes. Clin Exp Immunol. 2009;157:282-90.
Acevedo N, Caraballo L. IgE cross-reactivity between Ascaris lumbricoides and mite allergens: Possible influences on allergic sensitization and asthma. Parasite Immunol. 2011;33:309-21.
Coyne J. Why evolution is true. New York: Penguin Group; 2009.
Caraballo L, Acevedo N. New allergens of relevance in tropical regions: The impact of Ascaris lumbricoides infections. World Allergy Organization Journal. 2011;4:77-84.
Hoffmann KF, Cheever AW, Wynn TA. IL-10 and the dangers of immune polarization: excessive type 1 and type 2 cytokine responses induce distinct forms of lethal immunopathology in murine schistosomiasis. J Immunol. 2000;164:6406-16.
Pearce EJ, MacDonald AS. The immunobiology of schistosomiasis. Nat Rev Immunol. 2002;2:499-511.
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