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

Proc Natl Acad Sci U S A. 2021 Dec 21;118(51):e2108104118. doi: 10.1073/pnas.2108104118.

Abstract

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 β2-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.

Keywords: MHC class I; MHC class II; MHC class divergence; major histocompatibility complex; molecular evolution.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Cluster Analysis
  • Evolution, Molecular
  • 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
  • Major Histocompatibility Complex / genetics*
  • Multigene Family
  • Phylogeny
  • Protein Domains
  • Protein Multimerization
  • Vertebrates / classification
  • Vertebrates / genetics
  • Vertebrates / immunology

Substances

  • Histocompatibility Antigens
  • Histocompatibility Antigens Class I
  • Histocompatibility Antigens Class II