Temperature sensitivity of bat antibodies links metabolic state of bats with antigen-recognition diversity

Nia Toshkova, Violeta Zhelyzkova, Alejandra Reyes-Ruiz, Eline Haerens, Marina Castro Deus, Robin V. Lacombe, Maxime Lecerf, Gaelle Gonzalez, Nolwenn Jouvenet, Cyril Planchais and Jordan D. Dimitrov ()
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Nia Toshkova: Bulgarian Academy of Sciences
Violeta Zhelyzkova: Bulgarian Academy of Sciences
Alejandra Reyes-Ruiz: Centre de Recherche des Cordeliers, INSERM, CNRS, Sorbonne Université, Université Paris Cité
Eline Haerens: Centre de Recherche des Cordeliers, INSERM, CNRS, Sorbonne Université, Université Paris Cité
Marina Castro Deus: Centre de Recherche des Cordeliers, INSERM, CNRS, Sorbonne Université, Université Paris Cité
Robin V. Lacombe: Centre de Recherche des Cordeliers, INSERM, CNRS, Sorbonne Université, Université Paris Cité
Maxime Lecerf: Centre de Recherche des Cordeliers, INSERM, CNRS, Sorbonne Université, Université Paris Cité
Gaelle Gonzalez: Laboratoire de Santé Animale
Nolwenn Jouvenet: Virus Sensing and Signaling Unit
Cyril Planchais: Institut Pasteur, INSERM U1222, Université Paris Cité
Jordan D. Dimitrov: Centre de Recherche des Cordeliers, INSERM, CNRS, Sorbonne Université, Université Paris Cité

Nature Communications, 2024, vol. 15, issue 1, 1-19

Abstract: Abstract The bat immune system features multiple unique properties such as dampened inflammatory responses and increased tissue protection, explaining their long lifespan and tolerance to viral infections. Here, we demonstrated that body temperature fluctuations corresponding to different physiological states in bats exert a large impact on their antibody repertoires. At elevated temperatures typical for flight, IgG from the bat species Myotis myotis and Nyctalus noctula show elevated antigen binding strength and diversity, recognizing both pathogen-derived antigens and autoantigens. The opposite is observed at temperatures reflecting inactive physiological states. IgG antibodies of human and other mammals, or antibodies of birds do not appear to behave in a similar way. Importantly, diversification of bat antibody specificities results in preferential recognition of damaged endothelial and epithelial cells, indicating an anti-inflammatory function. The temperature-sensitivity of bat antibodies is mediated by the variable regions of immunoglobulin molecules. Additionally, we uncover specific molecular features of bat IgG, such as low thermodynamic stability and implication of hydrophobic interactions in antigen binding as well as high prevalence of polyreactivity. Overall, our results extend the understanding of bat tolerance to disease and inflammation and highlight the link between metabolism and immunity.

Date: 2024
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DOI: 10.1038/s41467-024-50316-x

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