The Role of Protein Glycosylation in Allergy
Abstract
The asparagine-linked carbohydrate moieties of plant and insect glycoproteins are the most abundant environmental immune determinants. They are the structural basis of what is known as cross-reactive carbohydrate determinants (CCDs). Despite some structural variation, the two main motifs are the xylose and the core-3-linked fucose, which form the essential part of two independent epitopes. Plants contain both epitopes, insect glycoproteins only fucose. These epitopes and other fucosylated determinants are also found in helminth parasites where they exert remarkable immunomodulatory effects. About 20% or more of allergic patients generate specific anti-glycan IgE, which is often accompanied by IgG. Even though antibody-binding glycoproteins are widespread in pollens, foods and insect venoms, CCDs do not appear to cause clinical symptoms in most, if not all patients. When IgE binding is solely due to CCDs, a glycoprotein allergen thus can be rated as clinical irrelevant allergen. Low binding affinity between IgE and plant N-glycans now drops out as a plausible explanation for the benign nature of CCDs. This rather may result from blocking antibodies induced by an incidental ‘immune therapy’ (‘glyco-specific immune therapy’) exerted by everyday contact with plant materials, e.g. fruits or vegetables. The need to detect and suppress anti-CCD IgE without interference from peptide epitopes can be best met by artificial glycoprotein allergens. Hydroxyproline-linked arabinose (single β-arabinofuranosyl residues) has been identified as a new IgE-binding carbohydrate epitope in the major mugwort allergen. However, currently the occurrence of this O-glycan determinant appears to be rather restricted.
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Antibodies specific to carbohydrate determinants are frequently found in many food allergies, particularly to plant proteins, although they appear not to have clinical relevance.
“In the case of many food allergies, particularly to plant proteins, antibodies specific to carbohydrate determinants are frequently found, although they appear not to have clinical relevance [9].”
From Influence of the Carbohydrate Moieties on the Immunoreactivity and Digestibility of the Egg Allergen Ovomucoid (2013) · cites this paper as [9]
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EAACI Molecular Allergology User's Guide
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“Gluc, recently designated as Mus a 5 by the IUIS Allergen Nomenclature Sub-Committee, harbored cross-reactive carbohydrate determinants (CCDs) (35).”
BackgroundRadauer, C., Adhami, F., Fürtler, I., Wagner, S., Allwardt, D., Scala, E., Ebner, C., Hafner, C., Hemmer, W., Mari, A., et al. (2011) · Molecular Immunology · doi:10.1016/j.molimm.2010.10.019 · Cited by 56 · see citing works
“Most patients with CCD sensitization display allergic symptoms towards a limited range of sources despite the ubiquitous reactivity of their IgE (Altmann, 2007).”
BackgroundGlycoproteomic profile in wine: a 'sweet' molecular renaissance.
Palmisano, G., Antonacci, D., & Larsen, M. (2010) · Journal of Proteome Research · doi:10.1021/pr100298j · Cited by 56 · see citing works
Mapping the interactions between a major pollen allergen and human IgE antibodies.
Razzera, G., Gadermaier, G., de Paula, V. S., Almeida, M., Egger, M., Jahn-Schmid, B., Almeida, F. C., Ferreira, F., & Valente, A. (2010) · Structure · doi:10.1016/j.str.2010.05.012 · Cited by 55 · see citing works
“Moreover, their involvement in IgE cross-reactivity (Altmann, 2007) seems to be very limited due to restricted distribution of hydroxyproline-linked b-arabinoses within plant proteins.”
BackgroundBecker, S., Schlederer, T., Kramer, M., Haack, M., Vrtala, S., Resch, Y., Lupinek, C., Valenta, R., & Gröger, M. (2016) · International Archives of Allergy and Immunology · doi:10.1159/000447694 · Cited by 54 · see citing works
Curin, M., Garib, V., & Valenta, R. (2017) · Annals of Allergy, Asthma & Immunology · doi:10.1016/j.anai.2016.11.022 · Cited by 52 · see citing works
Meevissen, M. H. J., Balog, C., Koeleman, C., Doenhoff, M., Schramm, G., Haas, H., Deelder, A., Wuhrer, M., & Hokke, C. (2011) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m110.005710 · Cited by 52 · see citing works
“Notably, asparagine-linked glycans belong to the most abundant environmental immune determinants and form the basis of the so-called cross-reactive carbohydrate determinants (46).”
BackgroundSelgrade, M., Bowman, C., Ladics, G., Privalle, L., & Laessig, S. A. (2009) · Toxicological Sciences · doi:10.1093/toxsci/kfp075 · Cited by 52
“Generally, IgE binding to carbohydrate domains is irrelevant to clinical allergy, unless there are multiple carbohydrates on the potentially allergenic protein (Altmann, 2007).”
BackgroundShin, Y., Chong, Y.-J., Yang, M., & Kwon, T. (2011) · Plant Biotechnology Journal · doi:10.1111/j.1467-7652.2011.00636.x · Cited by 52 · see citing works
“…proteins requires modification of their N-glycosylation patterns because the plant-specific core a-1,3-fucose, b-1,2-xylose and Lewis a epitope of their complex-type N-glycans are potentially immunogenic or allergenic to humans (Chargelegue et al., 2000; Bardor et al., 2003b; Altmann, 2007).”
InfluentialStříž, I., Golebski, K., Strizova, Z., Loukides, S., Bakakos, P., Hanania, N., Jeseňák, M., & Diamant, Z. (2023) · Clinical science · doi:10.1042/cs20190281 · Cited by 50 · see citing works
Glesner, J., Wünschmann, S., Li, M., Gustchina, A., Wlodawer, A., Himly, M., Chapman, M., & Pomés, A. (2011) · PLoS ONE · doi:10.1371/journal.pone.0022223 · Cited by 50 · see citing works
“Cross-reactive carbohydrate determinants (CCD) from plants and insects are N-glycans recognized by IgE, with minimal or no clinical significance [35–37].”
BackgroundRup, B., Alon, S., Amit-Cohen, B.-C., Almon, E. B., Chertkoff, R., Tekoah, Y., & Rudd, P. (2017) · PLoS ONE · doi:10.1371/journal.pone.0186211 · Cited by 48
“However, further studies have indicated that anti-cross-reactive carbohydrate determinant antibodies do not bind equally to all glycans with α (1,3) fucose and/or β (1,2) xylose, indicating that other features of the glycan structure or protein play a critical role in the binding [7].”
Innate immunostimulatory properties of allergens and their relevance to food allergy
Ruiter, B., & Shreffler, W. G. (2012) · Seminars in Immunopathology · doi:10.1007/s00281-012-0334-8 · Cited by 47 · see citing works
“The finding that glycan-specific antibodies are common from human clinical contexts as well as in murine models suggests that glycans enhance immunogenicity [13, 14].”
Mertens, M., Amler, S., Moerschbacher, B., & Brehler, R. (2010) · Clinical and Experimental Allergy · doi:10.1111/j.1365-2222.2010.03535.x · Cited by 47 · see citing works
Amann, T., Schmieder, V., Faustrup Kildegaard, H., Borth, N., & Andersen, M. R. (2019) · Biotechnology and Bioengineering · doi:10.1002/bit.27101 · Cited by 46 · see citing works
“Plants contain β-hexosaminidases, which give rise to N-glycan structures with terminal mannoses (Altmann, 2006; Choi, et al., 2012) and thus are far from their human counterparts.”
Wilson, A., Heesom, K., Mawby, W., Mellor, P., & Russell, C. L. (2008) · Veterinary Immunology and Immunopathology · doi:10.1016/j.vetimm.2007.10.011 · Cited by 46
Sensitization to cross‐reactive carbohydrate determinants in relation to alcohol consumption
González-Quintela, A., Garrido, M., Gude, F., Campos, J., Linneberg, A., Lojo, S., & Vidal, C. (2007) · Clinical and Experimental Allergy · doi:10.1111/j.1365-2222.2007.02863.x · Cited by 46 · see citing works
Rosenberg, Y., Saxena, A., Sun, W., Jiang, X., Chilukuri, N., Luo, C., Doctor, B. P., & Lee, K. D. (2010) · Chemico-Biological Interactions · doi:10.1016/j.cbi.2010.02.042 · Cited by 45
Component-resolved allergy diagnosis by microarray: potential, pitfalls, and prospects.
Knop, K. J. D., Bridts, C., Verweij, M., Hagendorens, M., Clerck, L. D. D., Stevens, W., & Ebo, D. (2010) · Advances in Clinical Chemistry · doi:10.1016/s0065-2423(10)50005-2 · Cited by 45 · see citing works
“Sera containing antiprofilin and anti-CCD sIgE antibodies display a very broad spectrum of cross-reactivity involving pollen, latex, fruit, vegetables, and venoms extending beyond clinical relevance, as these antibodies rarely give rise to clinically relevant allergy [6–12].”
BackgroundThe red meat allergy syndrome in Sweden
Apostolović, D., Tran, T. A. T., Starkhammar, M., Sánchez-Vidaurre, S., Hamsten, C., & van Hage, M. (2016) · Allergo Journal International · doi:10.1007/s40629-016-0098-0 · Cited by 44 · see citing works
“e current estimate is that 15–30 % of allergic patients generate speci c anti-carbohydrate IgE antibodies [34], but this IgE response has very little clinical relevance [35].”
BackgroundThe production of human glucocerebrosidase in glyco‐engineered N icotiana benthamiana plants
Limkul, J., Iizuka, S., Sato, Y., Misaki, R., Ohashi, T., Ohashi, T., & Fujiyama, K. (2016) · Plant Biotechnology Journal · doi:10.1111/pbi.12529 · Cited by 45 · see citing works
“N-glycosylation processes in the endoplasmic reticulum (ER) of plants are similar to those in humans, but the modification processes in the Golgi complex differ between plants and humans, with the former leading to the formation of plantspecific sugars that may induce immune responses in humans (Altmann, 2007; Bosch e…”
BackgroundCabauatan, C., Lupinek, C., Scheiblhofer, S., Weiss, R., Focke-Tejkl, M., Bhalla, P., Singh, M. B., Knight, P., van Hage, M., Ramos, J. D., et al. (2013) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2013.10.004 · Cited by 44 · see citing works
Multiple grass mixes as opposed to single grasses for allergen immunotherapy in allergic rhinitis
Gangl, K., Niederberger, V., & Valenta, R. (2013) · Clinical and Experimental Allergy · doi:10.1111/cea.12128 · Cited by 44 · see citing works
Ascaris lumbricoides: an overview of therapeutic targets.
Hagel, I., & Giusti, T. (2010) · Infectious Diseases - Drug Targets · doi:10.2174/187152610793180876 · Cited by 44 · see citing works
“Immunological cross reactivity between different carbohydrate epitopes of different species of plants and invertebrates have been also reported [201] suggesting that these IgE stimulating glycans may represent a fundamental class of ligands widely distributed in nature.”
BackgroundThe Changing Fate of a Secretory Glycoprotein in Developing Maize Endosperm1[C][W]
Arcalís, E., Stadlmann, J., Marcel, S., Drakakaki, G., Winter, V., Rodríguez, J., Fischer, R., Altmann, F., & Stoger, E. (2010) · Plant Physiology · doi:10.1104/pp.109.152363 · Cited by 44
“This localization is in agreement with the main N-glycan structure attached to phytase at this stage (MMXF), which is typically found on vacuolar glycoproteins (Lerouge et al., 1998).”
BackgroundInfluentialSelf-citationEffect of Food Thermal Processing on Allergenicity Proteins in Bombay Locust (Patanga Succincta)
Phiriyangkul, P., Srinroch, C., Srisomsap, C., Chokchaichamnankit, D., & Punyarit, P. (2015) · doi:10.18178/ijfe.1.1.23-28 · Cited by 44
“Moreover, Altmann (2006) [27] has review about structural of insect glycoprotein that discovery of core 1, 3 fucose in insect glycoproteins, it became apparent that this widely distributed residue is involved in cross-reactions between plant and insect glycoproteins.”
BackgroundMauff, F. L., Mercier, G., Chan, P., Burel, C., Vaudry, D., Bardor, M., Vézina, L., Couture, M., Lerouge, P., & Landry, N. (2015) · Plant Biotechnology Journal · doi:10.1111/pbi.12301 · Cited by 43 · see citing works
“, 2003) and could be involved in allergic reactions (Altmann, 2007).”
Background
- Authors
- Altmann, F.
- Affiliations
- BOKU University (AT)
- Corresponding author
- Altmann, Friedrich
- ORCID
- Altmann, Friedrich
- Venue
- International Archives of Allergy and Immunology
- Publisher
- S. Karger AG
- Published
- 2006-10-09
- Volume
- 142
- Issue
- 2
- Pages
- 99-115
- ISSN
- 1018-2438 (ISSN-L)
- 1423-0097
- OpenAlex
- W1976454430
- Cited by
- 393
- References
- 0
- Citations by year
- 2026: 11 · 2025: 10 · 2024: 10 · 2023: 10 · 2022: 5 · 2021: 17 · 2020: 20 · 2019: 17 · 2018: 16 · 2017: 23 · 2016: 21 · 2015: 31 · 2014: 25 · 2013: 33 · 2012: 25
- FWCI
- 1.27
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- International Archives of Allergy and Immunology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Glycosylation and Glycoproteins Research
- Health Sciences › Medicine › Immunology and Allergy › Allergic Rhinitis and Sensitization
- Health Sciences › Medicine › Immunology and Allergy › Food Allergy and Anaphylaxis Research
- Keywords
- protein glycosylation, allergy, cross-reactive carbohydrate determinants, N-glycans, helminth immunomodulation, pollen allergens, insect venom, food allergens
- MeSH terms
- Allergens, Animals, Carbohydrate Conformation, Carbohydrates, Glycoproteins, Glycosylation, Humans, Hypersensitivity
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