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Evaluating the Pathogenic Potential of IgE Targeting Cross-Reactive Carbohydrate Determinants in Dogs

Olivry, Thierry, Mas Fontao, Ana, Widorn, Laura, Mueller, Ralf S.·2024·Animals

Abstract

Cross-reactive carbohydrate determinants (CCDs) are complex N-glycans shared among allergens of plant, insect venom, and nematode origin. In allergic humans, IgE anti-CCD often develop and cause discrepancies between serological and skin tests. Overall, CCD-IgE are believed to be of low pathogenic relevance. IgE-targeting CCDs are also detected in companion animals, but their pathogenic potential and biological relevance are unknown. Herein, we first establish that, in 34 dogs with atopic dermatitis, the presence of serum anti-CCD IgE was detected in 14 pets (41.2%). In dogs, as in humans, IgE-targeting CCDs are heterogeneous, as they differentially recognized four distinct CCD-expressing proteins. The presence of CCD-IgE was associated with a higher and more frequent recognition of plant extracts in serological but not intradermal tests. Two different CCD-expressing proteins did not elicit immediate reactions when injected intradermally in dogs with detectable serum anti-CCD IgE. Similarly, two different CCD-expressing proteins did not induce the activation of mast cells passively transferred with canine anti-CCD IgE. Altogether, these results suggest that in dogs, as in humans, anti-CCD IgE are likely to have little pathogenic potential and blocking them in allergen-specific IgE serological tests is warranted to avoid false-positive results to plant extracts.

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Crossref · 10.3390/ani14223275

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Figures

Figure 1 Major plant CCDs. Blue squares: N-acetyl glucosamines; green circles: mannoses; orange star: xylose; red triangle: fucose; N: asparagine.
Figure 1 Major plant CCDs. Blue squares: N-acetyl glucosamines; green circles: mannoses; orange star: xylose; red triangle: fucose; N: asparagine.CC BY · PubMed Central
Figure 2 Number of CCD-expressing proteins recognized in 14 dogs with AD (dogs CCD1-CCD14). The x-axis represents the number of CCD proteins targeted by serum IgE, while the y-axis indicates the number of dogs recognizing that number.
Figure 2 Number of CCD-expressing proteins recognized in 14 dogs with AD (dogs CCD1-CCD14). The x-axis represents the number of CCD proteins targeted by serum IgE, while the y-axis indicates the number of dogs recognizing that number.CC BY · PubMed Central
Figure 3 Detection of serum IgE to plant extracts by ELISA. Significantly more plant extracts were recognized in dogs with detectable CCD-IgE (CCD) than in dogs without such IgE (NCCD).
Figure 3 Detection of serum IgE to plant extracts by ELISA. Significantly more plant extracts were recognized in dogs with detectable CCD-IgE (CCD) than in dogs without such IgE (NCCD).CC BY · PubMed Central
Figure 4 Detection of reactions to plant extracts by IDT. The number of positive responses to plant pollen was not significantly different between dogs with detectable serum CCD-specific IgE (CCD) and those without (NCCD).
Figure 4 Detection of reactions to plant extracts by IDT. The number of positive responses to plant pollen was not significantly different between dogs with detectable serum CCD-specific IgE (CCD) and those without (NCCD).CC BY · PubMed Central
Figure 5 Mast cell activation test with CCD-expressing proteins. Five dogs with detectable serum CCD-IgE (refer to Supplementary Table S3 for their profiles) were passively transferred onto Hoxb8 mast cells transfected with the human high-affinity IgE receptors. There was no specific activation of mast cells after activation with either CCD-HSA, rhLF-CCD, or their non-CCD-expressing respective controls (HSA and rhLF). In contrast, there was a high percentage of activation when mast cells were incubated with each serum and stimulated with an antibody against the high-affinity IgE receptor FcεRI (bottom right).
Figure 5 Mast cell activation test with CCD-expressing proteins. Five dogs with detectable serum CCD-IgE (refer to Supplementary Table S3 for their profiles) were passively transferred onto Hoxb8 mast cells transfected with the human high-affinity IgE receptors. There was no specific activation of mast cells after activation with either CCD-HSA, rhLF-CCD, or their non-CCD-expressing respective controls (HSA and rhLF). In contrast, there was a high percentage of activation when mast cells were incubated with each serum and stimulated with an antibody against the high-affinity IgE receptor FcεRI (bottom right).CC BY · PubMed Central

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Metadata

Authors
Olivry, T., Mas Fontao, A., Widorn, L., & Mueller, R. S.
Venue
Animals
Publisher
MDPI AG
Published
2024-11-14
Volume
14
Issue
22
Pages
3275
ISSN
2076-2615
Cited by
6
References
2
Language
en
Funders
Nextmune AB

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