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The evolution of IgE‐mediated type I hypersensitivity and its immunological value

Pritchard, David I., Falcone, Franco H., Mitchell, Piers D.·2021·Allergy
DOI 10.1111/all.14570
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Abstract

The allergic phenotype manifests itself in a spectrum of troublesome to life‐threatening diseases, from seasonal hay fever, through the food allergies, atopic eczema, asthma, to anaphylaxis. Allergy, that is an overreaction to allergen in hypersensitive individuals, results from the production of IgE, mast cell and basophil sensitisation and degranulation, requiring a range of medications to manage the conditions. Yet it is highly likely that allergy evolved for a purpose and that allergic diseases are accidental consequences of an insufficiently regulated immune response. This article presents a viewpoint from which to restore the immunological reputation of the allergic phenotype. We consider the evolutionary origins of potential allergens, toxins and parasites, and how they might have influenced early‐mammal species in existence when IgE first developed. We conclude that the allergic phenotype has likely saved the lives of many more mammals than have ever died from allergy, so justifying the positive role of IgE in our evolution.

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FIGURE 1 Approximate timeline of key events related to allergenic sources (normal font) or evolution of mammals (bold font) described in this paper. The timeline highlights how potential sources of archetypal allergens (insects and plants) preceded the evolution of IgE and its receptor in mammals, while other sources of allergens (such as venom from bees and human parasites) arose well after the evolution of IgE, putatively increasing its evolutionary value, thus leading to its preservation and consolidation across all mammals
FIGURE 1 Approximate timeline of key events related to allergenic sources (normal font) or evolution of mammals (bold font) described in this paper. The timeline highlights how potential sources of archetypal allergens (insects and plants) preceded the evolution of IgE and its receptor in mammals, while other sources of allergens (such as venom from bees and human parasites) arose well after the evolution of IgE, putatively increasing its evolutionary value, thus leading to its preservation and consolidation across all mammalsCC-BY-NC · From the PDF
Image 2
CC-BY-NC · From the PDF
FIGURE 2 Schematic illustration attempting to reconstruct the putative 'allergenic environment' which may have been present during the early Jurassic, at the time when the first mammal ancestors are thought to have arisen. The centre of the picture shows early mammal Morganucodon in an environment which consists of early plants (dominated by cycads, ferns, giant horsetailtrees and conifers), but would also have included early angiosperms (indicated by the pollen), as well as fungal spores, which would also have been omnipresent. Many exo- and ectoparasites would also have been present, such as ticks, fleas, lice and haematophagous dipterans (mosquitoes) as well as an array of intestinal and other worm parasites. Other sources of allergens might have been found in food, such as insects, nuts and seeds. Finally, allergens would also have been present in venomous animals, some of which originated in the Paleozoic era (scorpions, spiders), well before the first mammals existed, while others (bees) arose later. Some of these may also have played a role as a source of food, suggesting the interplay between early mammalian protection against the venoms of their prey (as a source of food) as a possible driving force underlying the evolution and preservation of the IgE response. The increased incidence of sensitization to insect-derived proteins in the context of the rising popularity of entomoculture and entomophagy also illustrates the potential link between insects and food as a source of ancestral allergens
FIGURE 2 Schematic illustration attempting to reconstruct the putative 'allergenic environment' which may have been present during the early Jurassic, at the time when the first mammal ancestors are thought to have arisen. The centre of the picture shows early mammal Morganucodon in an environment which consists of early plants (dominated by cycads, ferns, giant horsetailtrees and conifers), but would also have included early angiosperms (indicated by the pollen), as well as fungal spores, which would also have been omnipresent. Many exo- and ectoparasites would also have been present, such as ticks, fleas, lice and haematophagous dipterans (mosquitoes) as well as an array of intestinal and other worm parasites. Other sources of allergens might have been found in food, such as insects, nuts and seeds. Finally, allergens would also have been present in venomous animals, some of which originated in the Paleozoic era (scorpions, spiders), well before the first mammals existed, while others (bees) arose later. Some of these may also have played a role as a source of food, suggesting the interplay between early mammalian protection against the venoms of their prey (as a source of food) as a possible driving force underlying the evolution and preservation of the IgE response. The increased incidence of sensitization to insect-derived proteins in the context of the rising popularity of entomoculture and entomophagy also illustrates the potential link between insects and food as a source of ancestral allergensCC-BY-NC · From the PDF
FIGURE 3 Infographic illustrating the three approaches that can be used for identification of parasites affecting ancestral hominids
FIGURE 3 Infographic illustrating the three approaches that can be used for identification of parasites affecting ancestral hominidsCC-BY-NC · From the PDF
FIGURE 4 Chosen examples of tissues and immunological contexts where an IgE-dependent immune response provides advantages to the host. (A) Shows a muscular Trichinella spiralis cyst. In the rat, the presence of parasite-specific IgE around T spiralis larvae in muscle cysts has been demonstrated, together with an increased destruction of cysts. 106 (B) shows several examples of IgE-dependent host-protective immune responses against parasites or animal venoms. On the left, a tick lodged in the skin is shown. Elegant work by the Karasuyama group has shown how upon repeated exposure, mice develop acquired resistance characterized by strong infiltrations of IgE-bearing basophils, which can be detected in proximity of the tick mouth parts. 76 Mast cells, which are also shown in the picture, appear less essential in terms of acquired immunity to ticks. The importance of basophils had also been shown earlier by Brown et al 77 This immunity does not result in sterilising immunity but results in shorter feeding times and reduced engorgement weight of ticks, which is thought to reduce transmission of pathogens. 107 Further examples are venoms of bees (eg PLA2) 43 and other animal-derived venoms (Russell viper, Gila monster, scorpion), where an IgE-dependent degranulation of mast cells with the release of powerful proteases such as chymase, tryptase and carboxypeptidase A has been shown to provide protection by the Galli group. 40,48,108 Some toxins can activate mast cell directly by binding to receptors (eg helodermin to VIP-R), without the need for IgE. However, the presence of specific IgE may enhance this response 44 (C) Shows examples of intestinal parasites which have been shown to be expelled, reduced or killed IgE dependently in secondary immune responses, in a reaction which also involves Th2-driven mechanisms such as cell hyperplasia, increased mucin production and epithelial cell turnover. Such examples include Strongyloides venezuelensis , 109 T spiralis and 80,109-111 Heligmosomoides polygyrus . 81 Anisakis simplex is also listed as an interesting example of a parasite driving a strong IgE response, in its unique dual role as a zoonotic parasite but also as a common foodborne allergen. 112-114 To this day, anisakis is the best characterized nematode in terms of its allergenicity, 113,115 with 22 allergens listed on the Allergome database. 30 Also shown is the beneficial effect of elevated IgE in response to infection with the human hookworm Necator americanus , correlating with smaller size, number and reduced fecundity of adult hookworms, and the inability of new incoming parasites to establish in the gut
FIGURE 4 Chosen examples of tissues and immunological contexts where an IgE-dependent immune response provides advantages to the host. (A) Shows a muscular Trichinella spiralis cyst. In the rat, the presence of parasite-specific IgE around T spiralis larvae in muscle cysts has been demonstrated, together with an increased destruction of cysts. 106 (B) shows several examples of IgE-dependent host-protective immune responses against parasites or animal venoms. On the left, a tick lodged in the skin is shown. Elegant work by the Karasuyama group has shown how upon repeated exposure, mice develop acquired resistance characterized by strong infiltrations of IgE-bearing basophils, which can be detected in proximity of the tick mouth parts. 76 Mast cells, which are also shown in the picture, appear less essential in terms of acquired immunity to ticks. The importance of basophils had also been shown earlier by Brown et al 77 This immunity does not result in sterilising immunity but results in shorter feeding times and reduced engorgement weight of ticks, which is thought to reduce transmission of pathogens. 107 Further examples are venoms of bees (eg PLA2) 43 and other animal-derived venoms (Russell viper, Gila monster, scorpion), where an IgE-dependent degranulation of mast cells with the release of powerful proteases such as chymase, tryptase and carboxypeptidase A has been shown to provide protection by the Galli group. 40,48,108 Some toxins can activate mast cell directly by binding to receptors (eg helodermin to VIP-R), without the need for IgE. However, the presence of specific IgE may enhance this response 44 (C) Shows examples of intestinal parasites which have been shown to be expelled, reduced or killed IgE dependently in secondary immune responses, in a reaction which also involves Th2-driven mechanisms such as cell hyperplasia, increased mucin production and epithelial cell turnover. Such examples include Strongyloides venezuelensis , 109 T spiralis and 80,109-111 Heligmosomoides polygyrus . 81 Anisakis simplex is also listed as an interesting example of a parasite driving a strong IgE response, in its unique dual role as a zoonotic parasite but also as a common foodborne allergen. 112-114 To this day, anisakis is the best characterized nematode in terms of its allergenicity, 113,115 with 22 allergens listed on the Allergome database. 30 Also shown is the beneficial effect of elevated IgE in response to infection with the human hookworm Necator americanus , correlating with smaller size, number and reduced fecundity of adult hookworms, and the inability of new incoming parasites to establish in the gutCC-BY-NC · From the PDF
Image 6
CC-BY-NC · From the PDF
FIGURE 5 Three-dimensional structures of nine known parasite-derived allergens (UniProt accession number in brackets) together with the corresponding Allergen Family (AF) number and known representatives in plants (green), fungi (violet) or nonparasitic animals (blue). All structures were computed using Phyre 2, 116 except where a pdb accession number is given next to the UniProt accession number
FIGURE 5 Three-dimensional structures of nine known parasite-derived allergens (UniProt accession number in brackets) together with the corresponding Allergen Family (AF) number and known representatives in plants (green), fungi (violet) or nonparasitic animals (blue). All structures were computed using Phyre 2, 116 except where a pdb accession number is given next to the UniProt accession numberCC-BY-NC · From the PDF
FIGURE 6 Infographic summarizing the key arguments and counter arguments underlying the two main hypotheses explaining the evolutionary benefits of the IgE response in mammals
FIGURE 6 Infographic summarizing the key arguments and counter arguments underlying the two main hypotheses explaining the evolutionary benefits of the IgE response in mammalsCC-BY-NC · From the PDF
Image 9
CC-BY-NC · From the PDF
Image 10
CC-BY-NC · From the PDF

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Metadata

Authors
Pritchard, D. I., Falcone, F. H., & Mitchell, P. D.
Venue
Allergy
Publisher
Wiley
Published
2020-09-22
Volume
76
Issue
4
Pages
1024-1040
ISSN
  • 0105-4538
  • 1398-9995
DOI
10.1111/all.14570
Cited by
48
References
3
Language
en
Licence
creativecommons.org/licenses/by-nc/4.0/ (vor)

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