Information transfer in mammalian glycan-based communication
Glycan-binding proteins, so-called lectins, are exposed on mammalian cell surfaces and decipher the information encoded within glycans translating it into biochemical signal transduction pathways in the cell. These glycan-lectin communication pathways are complex and difficult to analyze. However, q...
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2023-02-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/69415 |
| _version_ | 1797854753543159808 |
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| author | Felix F Fuchsberger Dongyoon Kim Natalia Baranova Hanka Vrban Marten Kagelmacher Robert Wawrzinek Christoph Rademacher |
| author_facet | Felix F Fuchsberger Dongyoon Kim Natalia Baranova Hanka Vrban Marten Kagelmacher Robert Wawrzinek Christoph Rademacher |
| author_sort | Felix F Fuchsberger |
| collection | DOAJ |
| description | Glycan-binding proteins, so-called lectins, are exposed on mammalian cell surfaces and decipher the information encoded within glycans translating it into biochemical signal transduction pathways in the cell. These glycan-lectin communication pathways are complex and difficult to analyze. However, quantitative data with single-cell resolution provide means to disentangle the associated signaling cascades. We chose C-type lectin receptors (CTLs) expressed on immune cells as a model system to study their capacity to transmit information encoded in glycans of incoming particles. In particular, we used nuclear factor kappa-B-reporter cell lines expressing DC-specific ICAM-3–grabbing nonintegrin (DC-SIGN), macrophage C-type lectin (MCL), dectin-1, dectin-2, and macrophage-inducible C-type lectin (MINCLE), as well as TNFαR and TLR-1&2 in monocytic cell lines and compared their transmission of glycan-encoded information. All receptors transmit information with similar signaling capacity, except dectin-2. This lectin was identified to be less efficient in information transmission compared to the other CTLs, and even when the sensitivity of the dectin-2 pathway was enhanced by overexpression of its co-receptor FcRγ, its transmitted information was not. Next, we expanded our investigation toward the integration of multiple signal transduction pathways including synergistic lectins, which is crucial during pathogen recognition. We show how the signaling capacity of lectin receptors using a similar signal transduction pathway (dectin-1 and dectin-2) is being integrated by compromising between the lectins. In contrast, co-expression of MCL synergistically enhanced the dectin-2 signaling capacity, particularly at low-glycan stimulant concentration. By using dectin-2 and other lectins as examples, we demonstrate how signaling capacity of dectin-2 is modulated in the presence of other lectins, and therefore, the findings provide insight into how immune cells translate glycan information using multivalent interactions. |
| first_indexed | 2024-04-09T20:12:22Z |
| format | Article |
| id | doaj.art-b2548e092c7a40d9a756bb40a483d25b |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-09T20:12:22Z |
| publishDate | 2023-02-01 |
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| series | eLife |
| spelling | doaj.art-b2548e092c7a40d9a756bb40a483d25b2023-03-31T16:41:33ZengeLife Sciences Publications LtdeLife2050-084X2023-02-011210.7554/eLife.69415Information transfer in mammalian glycan-based communicationFelix F Fuchsberger0https://orcid.org/0000-0002-9379-9792Dongyoon Kim1https://orcid.org/0000-0001-9162-8730Natalia Baranova2https://orcid.org/0000-0002-3086-9124Hanka Vrban3Marten Kagelmacher4Robert Wawrzinek5Christoph Rademacher6https://orcid.org/0000-0001-7082-7239Department of Pharmaceutical Sciences, University of Vienna, Vienna, Austria; Department of Biomolecular Systems, Max Planck Institute of Colloids and Interfaces, Potsdam, Germany; Department of Microbiology, Immunology and Genetics University of Vienna, Max F. Perutz Labs, Vienna, AustriaDepartment of Pharmaceutical Sciences, University of Vienna, Vienna, Austria; Department of Biomolecular Systems, Max Planck Institute of Colloids and Interfaces, Potsdam, Germany; Department of Microbiology, Immunology and Genetics University of Vienna, Max F. Perutz Labs, Vienna, AustriaDepartment of Pharmaceutical Sciences, University of Vienna, Vienna, Austria; Department of Microbiology, Immunology and Genetics University of Vienna, Max F. Perutz Labs, Vienna, AustriaDepartment of Pharmaceutical Sciences, University of Vienna, Vienna, Austria; Department of Microbiology, Immunology and Genetics University of Vienna, Max F. Perutz Labs, Vienna, AustriaDepartment of Biomolecular Systems, Max Planck Institute of Colloids and Interfaces, Potsdam, GermanyDepartment of Pharmaceutical Sciences, University of Vienna, Vienna, Austria; Department of Biomolecular Systems, Max Planck Institute of Colloids and Interfaces, Potsdam, Germany; Department of Microbiology, Immunology and Genetics University of Vienna, Max F. Perutz Labs, Vienna, AustriaDepartment of Pharmaceutical Sciences, University of Vienna, Vienna, Austria; Department of Biomolecular Systems, Max Planck Institute of Colloids and Interfaces, Potsdam, Germany; Department of Microbiology, Immunology and Genetics University of Vienna, Max F. Perutz Labs, Vienna, AustriaGlycan-binding proteins, so-called lectins, are exposed on mammalian cell surfaces and decipher the information encoded within glycans translating it into biochemical signal transduction pathways in the cell. These glycan-lectin communication pathways are complex and difficult to analyze. However, quantitative data with single-cell resolution provide means to disentangle the associated signaling cascades. We chose C-type lectin receptors (CTLs) expressed on immune cells as a model system to study their capacity to transmit information encoded in glycans of incoming particles. In particular, we used nuclear factor kappa-B-reporter cell lines expressing DC-specific ICAM-3–grabbing nonintegrin (DC-SIGN), macrophage C-type lectin (MCL), dectin-1, dectin-2, and macrophage-inducible C-type lectin (MINCLE), as well as TNFαR and TLR-1&2 in monocytic cell lines and compared their transmission of glycan-encoded information. All receptors transmit information with similar signaling capacity, except dectin-2. This lectin was identified to be less efficient in information transmission compared to the other CTLs, and even when the sensitivity of the dectin-2 pathway was enhanced by overexpression of its co-receptor FcRγ, its transmitted information was not. Next, we expanded our investigation toward the integration of multiple signal transduction pathways including synergistic lectins, which is crucial during pathogen recognition. We show how the signaling capacity of lectin receptors using a similar signal transduction pathway (dectin-1 and dectin-2) is being integrated by compromising between the lectins. In contrast, co-expression of MCL synergistically enhanced the dectin-2 signaling capacity, particularly at low-glycan stimulant concentration. By using dectin-2 and other lectins as examples, we demonstrate how signaling capacity of dectin-2 is modulated in the presence of other lectins, and therefore, the findings provide insight into how immune cells translate glycan information using multivalent interactions.https://elifesciences.org/articles/69415cell signalinginformation theoryglycobiology |
| spellingShingle | Felix F Fuchsberger Dongyoon Kim Natalia Baranova Hanka Vrban Marten Kagelmacher Robert Wawrzinek Christoph Rademacher Information transfer in mammalian glycan-based communication eLife cell signaling information theory glycobiology |
| title | Information transfer in mammalian glycan-based communication |
| title_full | Information transfer in mammalian glycan-based communication |
| title_fullStr | Information transfer in mammalian glycan-based communication |
| title_full_unstemmed | Information transfer in mammalian glycan-based communication |
| title_short | Information transfer in mammalian glycan-based communication |
| title_sort | information transfer in mammalian glycan based communication |
| topic | cell signaling information theory glycobiology |
| url | https://elifesciences.org/articles/69415 |
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