Phylotranscriptomics suggests the jawed vertebrate ancestor could generate diverse helper and regulatory T cell subsets

Redmond, Anthony K.; Macqueen, Daniel J.; Dooley, Helen

doi:10.1186/s12862-018-1290-2

Cited by 27 publications

(36 citation statements)

References 110 publications

(168 reference statements)

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“…1) incorporating a relaxed molecular clock model, which allows estimation of the most plausible root location in the tree (Drummond et al 2006; e.g. Macqueen and Wilcox 2014; Redmond et al 2018). Four distinct MTR clades (Fig.…”

Section: Resultsmentioning

confidence: 99%

Phylogenetic reclassification of vertebrate melatonin receptors to include Mel1d

Macqueen

Ebbesson

Hazlerigg

et al. 2019

Preprint

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30The circadian and seasonal actions of melatonin are mediated by high affinity G-31 protein coupled receptors (melatonin receptors, MTRs), classified into 32 phylogenetically distinct subtypes based on sequence divergence and 33 pharmacological characteristics. Three vertebrate MTR subtypes are currently 34 described: MT1 (MTNR1A), MT2 (MTNR1B), and Mel1c (MTNR1C / GPR50), which 35 exhibit distinct affinities, tissue distributions and signaling properties. We present 36 phylogenetic and comparative genomic analyses supporting a revised classification 37 of the vertebrate MTR family. We demonstrate four ancestral vertebrate MTRs, 38including a novel molecule hereafter named Mel1d. We reconstructed the evolution 39 of each vertebrate MTR, detailing genetic losses in addition to gains resulting from 40 whole genome duplication events in teleost fishes. We show that Mel1d was lost 41 separately in mammals and birds and has been previously mistaken for an MT1 42 paralogue. The genetic and functional diversity of vertebrate MTRs is more complex 43 than appreciated, with implications for our understanding of melatonin actions in 44 different taxa. The significance of our findings, including the existence of Mel1d, are 45 discussed in an evolutionary and functional context accommodating a robust 46 phylogenetic assignment of MTR gene family structure. 47 50 51Melatonin is an ancient eukaryotic signalling molecule that regulates diverse 52 biological functions. While best known as a regulator of biological rhythms in 53 humans, this hormone also regulates energy balance, temperature, behavior, blood 54 pressure, and seasonal reproduction. Melatonin is secreted by the pineal gland and 55 targets the brain as well as peripheral tissues (Hardeland et al. 2011, Slominski et 56 al. 2012), but is also produced by several tissues, eliciting paracrine effects (Weaver 57 and Reppert 1990). The actions of melatonin depend on the spatiotemporal 58 expression of high-affinity melatonin receptors (MTR), representing a specific class of 59 G protein-coupled receptor (GPCR). 60 61

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Section: Resultsmentioning

confidence: 99%

Phylogenetic reclassification of vertebrate melatonin receptors to include Mel1d

Macqueen

Ebbesson

Hazlerigg

et al. 2019

Preprint

Self Cite

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“…While type 3 immune responses (i.e., IL-17) appeared in invertebrates (Huang et al, 2015) and Drosophilia have an IL-6-related cytokine termed DOME, the evolution of g c family cytokines and their receptors is not evident in these species. Most g c cytokines, including IL-2, IL-4, IL-7, IL-15 and IL-21, are found in mammals, birds, and teleost and cartilaginous fish, with IL-2, IL-4, IL-7, and IL-21 present in the elephant shark genome (Redmond et al, 2018;Secombes, 2016). It is notable that the IL2/IL21 and IL4/IL13 gene clusters are conserved in mammals, birds, teleost fish, and the elephant shark, as is the gene encoding g c .…”

Section: Evolutionary Considerationsmentioning

confidence: 99%

The γc Family of Cytokines: Basic Biology to Therapeutic Ramifications

2019

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The common cytokine receptor g chain, g c , is a component of the receptors for interleukin-2 (IL-2), IL-4, IL-7, IL-9, IL-15, and IL-21. Mutation of the gene encoding g c results in X-linked severe combined immunodeficiency in humans, and g c family cytokines collectively regulate development, proliferation, survival, and differentiation of immune cells. Here, we review the basic biology of these cytokines, highlighting mechanisms of signaling and gene regulation that have provided insights for immunodeficiency, autoimmunity, allergic diseases, and cancer. Moreover, we discuss how studies of this family stimulated the development of JAK3 inhibitors and present an overview of current strategies targeting these pathways in the clinic, including novel antibodies, antagonists, and partial agonists. The diverse roles of these cytokines on a range of immune cells have important therapeutic implications.

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“…The primary amino acid sequence of interferons are short and rapidly evolving, both characteristics expected to promote phylogenetic error (41). Short alignments may have insufficient phylogenetic information to infer relationships between sequences and are more prone to stochastic errors.…”

Section: Introductionmentioning

confidence: 99%

Discovery of All Three Types in Cartilaginous Fishes Enables Phylogenetic Resolution of the Origins and Evolution of Interferons

et al. 2019

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Interferons orchestrate host antiviral responses in jawed vertebrates. They are categorized into three classes; IFN1 and IFN3 are the primary antiviral cytokine lineages, while IFN2 responds to a broader variety of pathogens. The evolutionary relationships within and between these three classes have proven difficult to resolve. Here, we reassess interferon evolution, considering key phylogenetic pitfalls including taxon sampling, alignment quality, model adequacy, and outgroup choice. We reveal that cartilaginous fishes, and hence the jawed vertebrate ancestor, possess(ed) orthologs of all three interferon classes. We show that IFN3 groups sister to IFN1, resolve the origins of the human IFN3 lineages, and find that intronless IFN3s emerged at least three times. IFN2 genes are highly conserved, except for IFN-γ-rel, which we confirm resulted from a teleost-specific duplication. Our analyses show that IFN1 phylogeny is highly sensitive to phylogenetic error. By accounting for this, we describe a new backbone IFN1 phylogeny that implies several IFN1 genes existed in the jawed vertebrate ancestor. One of these is represented by the intronless IFN1s of tetrapods, including mammalian-like repertoires of reptile IFN1s and a subset of amphibian IFN1s, in addition to newly-identified intron-containing shark IFN1 genes. IFN-f, previously only found in teleosts, likely represents another ancestral jawed vertebrate IFN1 family member, suggesting the current classification of fish IFN1s into two groups based on the number of cysteines may need revision. The providence of the remaining fish IFN1s and the coelacanth IFN1s proved difficult to resolve, but they may also be ancestral jawed vertebrate IFN1 lineages. Finally, a large group of amphibian-specific IFN1s falls sister to all other IFN1s and was likely also present in the jawed vertebrate ancestor. Our results verify that intronless IFN1s have evolved multiple times in amphibians and indicate that no one-to-one orthology exists between mammal and reptile IFN1s. Our data also imply that diversification of the multiple IFN1s present in the jawed vertebrate ancestor has occurred through a rapid birth-death process, consistent with functional maintenance over a 450-million-year host-pathogen arms race. In summary, this study reveals a new model of interferon evolution important to our understanding of jawed vertebrate antiviral immunity.

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Phylotranscriptomics suggests the jawed vertebrate ancestor could generate diverse helper and regulatory T cell subsets

Cited by 27 publications

References 110 publications

Phylogenetic reclassification of vertebrate melatonin receptors to include Mel1d

Phylogenetic reclassification of vertebrate melatonin receptors to include Mel1d

The γc Family of Cytokines: Basic Biology to Therapeutic Ramifications

Discovery of All Three Types in Cartilaginous Fishes Enables Phylogenetic Resolution of the Origins and Evolution of Interferons

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