The search to understand the development of the chicken immune system: Differences in expression of MHC class I loci and waves of thymocytes as evolutionary relics?

Abstract

Chickens are renowned as a model for embryogenesis but have also been responsible for crucial advances in virology, cancer research and immunology. However, chickens are best known as a major source of animal protein for human nutrition, with roughly 80 billion chickens alive each year supplying meat and eggs, the vast majority part of a global poultry industry. As a result, avian immunology been studied intensively for over 60 years, and it has become clear that a major genetic locus in chickens determining resistance to infectious disease and response to vaccines is the major histocompatibility complex (MHC). Compared to typical mammals, the chicken MHC is compact and simple, with only two classical class I genes. A dominantly-expressed class I gene, BF2, is the major ligand for cytotoxic T lymphocytes (CTLs), while the other locus, BF1, is much less well-expressed, lacking in some MHC haplotypes, and is a ligand for natural killer (NK) cells. Cell surface class I expression in neonatal chicks is far less than in adults, and one possibility is that BF2 is not well-expressed early in ontogeny. A precedent is found for amphibians: the single classical class I molecule is not expressed in tadpoles of Xenopus frogs, although non-polymorphic (and thus non-classical) class I molecules from the XNC locus are expressed, which are recognised for immune defence by non-canonical NKT lymphocytes. Indeed, three waves of different T cells are produced by the Xenopus thymus: in tadpoles, during metamorphosis and finally as adults. Three waves of thymic emigrants are also found for chickens, and reasoning by analogy, it may be that the waves of thymocytes and the expression of class I molecules during ontogeny of chickens are evolutionary relics. As well as scientific interest in the ontogeny of MHC class I expression and appearance of peripheral T cells, there are potential practical implications, given the importance of vaccination in ovo and in day-old chicks for the poultry industry.