Discovery of an ancient MHC category with both class I and class II features

Two classes of major histocompatibility complex (MHC) molecules, MHC class I and class II, play important roles in our immune system, presenting antigens to functionally distinct T lymphocyte populations. However, the origin of this essential MHC class divergence is poorly understood. Here, we disco...

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Bibliographic Details
Published in:Proceedings of the National Academy of Sciences - PNAS 2021-12, Vol.118 (51)
Main Authors: Okamura, Kazuhiko, Dijkstra, Johannes M, Tsukamoto, Kentaro, Grimholt, Unni, Wiegertjes, Geert F, Kondow, Akiko, Yamaguchi, Hisateru, Hashimoto, Keiichiro
Format: Article
Language:English
Subjects:
Amino Acid Sequence
Animals
Antigens
Biological Sciences
Cluster Analysis
Evolution, Molecular
Fish
Fishes - classification
Fishes - genetics
Fishes - immunology
Histocompatibility Antigens - chemistry
Histocompatibility Antigens - genetics
Histocompatibility Antigens Class I - chemistry
Histocompatibility Antigens Class I - genetics
Histocompatibility Antigens Class II - chemistry
Histocompatibility Antigens Class II - genetics
Humans
Immune system
Lymphocytes
Lymphocytes T
Major histocompatibility complex
Major Histocompatibility Complex - genetics
Multigene Family
Phylogeny
Protein Domains
Protein Multimerization
Vertebrates
Vertebrates - classification
Vertebrates - genetics
Vertebrates - immunology
β2 Microglobulin
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Summary:Two classes of major histocompatibility complex (MHC) molecules, MHC class I and class II, play important roles in our immune system, presenting antigens to functionally distinct T lymphocyte populations. However, the origin of this essential MHC class divergence is poorly understood. Here, we discovered a category of MHC molecules (W-category) in the most primitive jawed vertebrates, cartilaginous fish, and also in bony fish and tetrapods. W-category, surprisingly, possesses class II-type α- and β-chain organization together with class I-specific sequence motifs for interdomain binding, and the W-category α2 domain shows unprecedented, phylogenetic similarity with β -microglobulin of class I. Based on the results, we propose a model in which the ancestral MHC class I molecule evolved from class II-type W-category. The discovery of the ancient MHC group, W-category, sheds a light on the long-standing critical question of the MHC class divergence and suggests that class II type came first.
ISSN:0027-8424
1091-6490
DOI:10.1073/pnas.2108104118