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Igh locus structure and evolution in Platyrrhines: new insights from a genomic perspective

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Abstract

Non-human primates have been used as animal models because of their phylogenetic closeness to humans. However, the genetic differences between humans and non-human primates must be considered to select the appropriate animal models. Recently, New World monkeys (Platyrrhines) have generated a higher interest in biomedical research, especially in assessing vaccine safety and immunogenicity. Given the continued and renewed interest in Platyrrhines as biomedical models, it is a necessary to have a better and more complete understanding of their immune system and its implications for research. Immunoglobulins (Ig) are the main proteins that mediate humoral immunity. These proteins have evolved as part of an adaptive immune response system derived from ancient vertebrates. There are at least four Ig classes in Prosimians, whereas five have been reported in Catarrhines. Information on the structure and evolution of the loci containing immunoglobulin heavy chain constant genes (Igh) in Platyrrhines, however, is limited. Here, Igh loci were characterized in 10 Platyrrhines using the available whole genome sequences. Human and Macaca Igh loci were also assessed to compare them with their Platyrrhines counterparts. Differences in Igh locus structure were observed between Platyrrhines and Catarrhines. Noteworthy changes occur in the γ gene, which encodes a key Ig involved in organism defense that would favor protection after vaccination. The remarkable differences between the immunoglobulin proteins of Platyrrhines and Catarrhines warrant a cautionary message to biomedical researchers.

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Acknowledgments

The authors wish to thank Heidy Catalina Bautista Rodríguez, Gisselle Rivera Cardenas, Marcela Castaño Rodriguez, and Gypsy Bonny Español for reviewing the manuscript.

Funding

This work was supported by the Fundación Scient. 

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  1. Pgame - Population Genetics And Molecular Evolution, Fundación Scient, Carrera 16-3 # 35-41, Tunja, Boyacá, Colombia

    Diego Garzón-Ospina & Sindy P. Buitrago

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  1. Diego Garzón-Ospina
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Correspondence to Diego Garzón-Ospina or Sindy P. Buitrago.

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Electronic supplementary material

Supplementary Material 1

Igh gene sequences identified within primates contigs used in this study. (TXT 184 kb)

Supplementary Material 2

Phylogenetic tree forIghγexons. The tree was inferred using the Bayesian method based on the GTR + G evolutionary model to assess the phylogenetic closeness of the exons. The Platyrrhines sequences were collapsed. Branches corresponding to each exon are depicted in colors: Exon 1: purple, Exon 2: blue, Exon 3: fuchsia, and Exon 4: green. Numbers on branches represent posterior probability values. Only posterior probability values higher than 0.85 are shown. Posterior probability values for Catarrhine exon 2 were higher than 0.70 but lower than 0.85. (PNG 432 kb)

High resolution image (TIF 1365 kb)

Supplementary Material 3

Sliding window for omega (ω = KN/KS) rate throughout primatesIghgenes. A color line represents the divergence rates (KN/KS) for each of the Igh genes, μ: orange, δ: purple, γ: green, ε: fuchsia and α: blue. Stars represent the gene regions with sites evolving under episodic positive selection. The discontinuity of some lines is due to InDels within the sequence alignment. (PNG 348 kb)

High resolution image (TIF 1200 kb)

Supplementary Material 4

Phylogenies analyzed for episodic selection. Each Igh gene cluster was analyzed using the adaptive Branch-Site Random Effects Likelihood (aBSREL) method. The red box size on branches represents the percentage of codons involved in episodic positive selection found by aBSREL. Branches have been classified as undergoing episodic diversifying selection by its p value and corrected for multiple testing using the Holm-Bonferroni method (p < 0.01). (a) μ gene; (b) δ gene; (c) γ gene; (d) ε gene; (e) α gene. (PDF 695 kb)

Supplementary Material 5

Hosa γupstream and downstream DNA fragments alignments. Upstream and downstream DNA fragments from γ genes were aligned to identify their closeness. Identity values were also estimated. Identity values obtained from the comparisons between γ upstream and downstream DNA fragments showed that the values obtained between γ4 and the other genes were the highest. (a) Hosa γ2 and γ4 duplicated fragment alignment (b) Hosa γ2, γ4, and γ3 duplicated fragment alignment (c) Hosa γ2, γ3, γ4, and Ψγ duplicated fragment alignment (d) upstream and downstream DNA fragment alignment for Hosa Ψγ and γ genes. (PDF 1802 kb)

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Garzón-Ospina, D., Buitrago, S.P. Igh locus structure and evolution in Platyrrhines: new insights from a genomic perspective. Immunogenetics 72, 165–179 (2020). https://doi.org/10.1007/s00251-019-01151-8

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  • DOI: https://doi.org/10.1007/s00251-019-01151-8

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