Complete sequencing of a cynomolgus macaque major histocompatibility complex haplotype

Author:

Karl Julie A.ORCID,Prall Trent M.ORCID,Bussan Hailey E.ORCID,Varghese Joshua M.ORCID,Pal Aparna,Wiseman Roger W.ORCID,O'Connor David H.ORCID

Abstract

Macaques provide the most widely used nonhuman primate models for studying the immunology and pathogenesis of human diseases. Although the macaque major histocompatibility complex (MHC) region shares most features with the human leukocyte antigen (HLA) region, macaques have an expanded repertoire of MHC class I genes. Although a chimera of two rhesus macaque MHC haplotypes was first published in 2004, the structural diversity of MHC genomic organization in macaques remains poorly understood owing to a lack of adequate genomic reference sequences. We used ultralong Oxford Nanopore and high-accuracy Pacific Biosciences (PacBio) HiFi sequences to fully assemble the ∼5.2-Mb M3 haplotype of an MHC-homozygous, Mauritian-origin cynomolgus macaque (Macaca fascicularis). The MHC homozygosity allowed us to assemble a single MHC haplotype unambiguously and avoid chimeric assemblies that hampered previous efforts to characterize this exceptionally complex genomic region in macaques. The high quality of this new assembly is exemplified by the identification of an extended cluster of sixMafa-AGgenes that contains a recent duplication with a highly similar ∼48.5-kb block of sequence. The MHC class II region of this M3 haplotype is similar to the previously sequenced rhesus macaque haplotype and HLA class II haplotypes. The MHC class I region, in contrast, contains 13MHC-Bgenes, fourMHC-Agenes, and threeMHC-Egenes (vs. 19MHC-B, twoMHC-A, and oneMHC-Ein the previously sequenced haplotype). These results provide an unambiguously assembled single contiguous cynomolgus macaque MHC haplotype with fully curated gene annotations that will inform infectious disease and transplantation research.

Funder

National Institute of Allergy and Infectious Diseases

National Institutes of Health

Office of Research Infrastructure Programs

Research Facilities Improvement Program

Publisher

Cold Spring Harbor Laboratory

Subject

Genetics (clinical),Genetics

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