The Proto-MHC of Placozoans, a Region Specialized in Cellular Stress and Ubiquitination/Proteasome Pathways

Suurväli, Jaanus; Jouneau, Luc; Thépot, Dominique; Grusea, Simona; Pontarotti, Pierre; Pasquier, Louis Du; Boudinot, Sirje Rüütel; Boudinot, Pierre

doi:10.4049/jimmunol.1401177

Cited by 23 publications

(17 citation statements)

References 76 publications

(101 reference statements)

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“…The intracellular domain (ID) of BTN3A1 and BTN3A3 belongs to the B30.2 family ( 85 , 86 ) and is often found in proteins involved in innate immunity. This includes even molecules encoded by genes found in the hypothetical “proto MHC” of placozoa, which form the most basal branch of Metazoa ( 87 ). The BTN3A2 molecule has a truncated intracellular B30.2-negative domain.…”

Section: Btn3 Is Mandatory For Pag-mediated Activation Of Vγ9vδ2 T Cementioning

confidence: 99%

The VÎ³9VÎ´2 T Cell Antigen Receptor and Butyrophilin-3 A1: Models of Interaction, the Possibility of Co-Evolution, and the Case of Dendritic Epidermal T Cells

Karunakaran

Herrmann

2014

Front. Immunol.

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Most circulating human gamma delta T cells are Vγ9Vδ2 T cells. Their hallmark is the expression of T cell antigen receptors (TCR) whose γ-chains show a Vγ9-JP (Vγ2-Jγ1.2) rearrangement and are paired with Vδ2-containing δ-chains, a dominant TCR configuration, which until recently seemed to occur in primates only. Vγ9Vδ2 T cells respond to phosphoantigens (PAg) such as (E)-4-Hydroxy-3-methyl-but-2-enyl pyrophosphate (HMBPP), which is produced by many pathogens and isopentenyl pyrophosphate (IPP), which accumulates in certain tumors or cells treated with aminobisphosphonates such as zoledronate. A prerequisite for PAg-induced activation is the contact of Vγ9Vδ2 T cells with cells expressing butyrophilin-3 A1 (BTN3A1). We will first critically review models of how BTN3 might act in PAg-mediated Vγ9Vδ2 T cell activation and then address putative co-evolution of Vγ9, Vδ2, and BTN3 genes. In those rodent and lagomorphs used as animal models, all three genes are lost but a data-base analysis showed that they emerged together with placental mammals. A strong concomitant conservation of functional Vγ9, Vδ2, and BTN3 genes in other species suggests co-evolution of these three genes. A detailed analysis was performed for the new world camelid alpaca (Vicugna pacos). It provides an excellent candidate for a non-primate species with presumably functional Vγ9Vδ2 T cells since TCR rearrangements share features characteristic for PAg-reactive primate Vγ9Vδ2 TCR and proposed PAg-binding sites of BTN3A1 have been conserved. Finally, we analyze the possible functional relationship between the butyrophilin-family member Skint1 and the γδ TCR-V genes used by murine dendritic epithelial T cells (DETC). Among placental mammals, we identify five rodents, the cow, a bat, and the cape golden mole as the only species concomitantly possessing potentially functional homologs of murine Vγ3, Vδ4 genes, and Skint1 gene and suggest to search for DETC like cells in these species.

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Section: Btn3 Is Mandatory For Pag-mediated Activation Of Vγ9vδ2 T Cementioning

confidence: 99%

The VÎ³9VÎ´2 T Cell Antigen Receptor and Butyrophilin-3 A1: Models of Interaction, the Possibility of Co-Evolution, and the Case of Dendritic Epidermal T Cells

Karunakaran

Herrmann

2014

Front. Immunol.

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“…The genes that were originally identified as being paralogous (Kasahara 1997) are located within a 3.2-Mb region in the MHC on human chromosome 6 but are spread over roughly 21 to 76 Mb in each of the paralogous regions, with these paralogous genes separated by many tens of other genes that are not obviously paralogous (as found by locating these genes in ENSEMBL). More recent analyses, taking into account other organisms (Kasahara 2000; Abi-Rached et al 2002; Azumi et al 2003; Danchin and Pontarotti 2004; Kasahara et al 2004; Suurväli et al 2014), improve but do not substantially change this view (with interesting details outside the scope of this review). The selective identification of genes considered to be paralogous in a sea of genes that are not obviously paralogous (particularly for genes that are part of a large multigene family with members throughout the genome) certainly led to skepticism for the early claims for two rounds of genome-wide duplication at the base of the vertebrates (for instance, Hughes 1998), which was largely dispelled once the amphioxus genome became available (Putnam et al 2008).…”

Section: The Genomic Location Of Cd1 Genes Varies In Different Speciesmentioning

confidence: 85%

“…This finding is most easily accommodated by the CD1 genes being part of the region before duplication, but it remains possible that the CD1 genes were inserted into the middle of an existing paralogous region. In contrast, the FcRn gene is located at one end of the 47-Mb region containing the paralogous genes on chromosome 19, relatively far away (and across the centromere) from the bulk of those paralogous genes (particularly as determined by later analyses, for instance Suurväli et al 2014). Thus, examination of the human genome does not rule out any of the proposed models but it would seem most parsimonious for CD1 genes to be present before the genome-wide duplications and consistent with FcRn gene appearing later in evolution.…”

Section: The Genomic Location Of Cd1 Genes Varies In Different Speciesmentioning

confidence: 99%

Location, location, location: the evolutionary history of CD1 genes and the NKR-P1/ligand systems

Rogers

Kaufman

2016

Immunogenetics

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CD1 genes encode cell surface molecules that present lipid antigens to various kinds of T lymphocytes of the immune system. The structures of CD1 genes and molecules are like the major histocompatibility complex (MHC) class I system, the loading of antigen and the tissue distribution for CD1 molecules are like those in the class II system, and phylogenetic analyses place CD1 between class I and class II sequences, altogether leading to the notion that CD1 is a third ancient system of antigen presentation molecules. However, thus far, CD1 genes have only been described in mammals, birds and reptiles, leaving major questions as to their origin and evolution. In this review, we recount a little history of the field so far and then consider what has been learned about the structure and functional attributes of CD1 genes and molecules in marsupials, birds and reptiles. We describe the central conundrum of CD1 evolution, the genomic location of CD1 genes in the MHC and/or MHC paralogous regions in different animals, considering the three models of evolutionary history that have been proposed. We describe the natural killer (NK) receptors NKR-P1 and ligands, also found in different genomic locations for different animals. We discuss the consequence of these three models, one of which includes the repudiation of a guiding principle for the last 20 years, that two rounds of genome-wide duplication at the base of the vertebrates provided the extra MHC genes necessary for the emergence of adaptive immune system of jawed vertebrates.

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“…While TRIM genes are present across metazoans, the implication in antiviral immunity of the few trim genes found in the genomes of basal branches of metazoans or in invertebrates (5, 23, 24, 48) remains unknown. Interestingly, these trim mostly belong to the class 1 (domain structure: RBCC-COS-Fn3-B302), which enhances the RIG I pathway in human (21).…”

Section: Discussionmentioning

confidence: 99%

“…(6, 22). TRIMs involved in basic cellular functions often belong to the most ancient subsets, e.g., RBCC-Cos-Fn3-B30.2 TRIM, which were already present in early metazoans (23) and are found both in vertebrates and invertebrates (24). Only a few trim genes are generally present in the genome of invertebrates, while the family greatly expanded in vertebrates.…”

Section: Introductionmentioning

confidence: 99%

FTR83, a Member of the Large Fish-Specific finTRIM Family, Triggers IFN Pathway and Counters Viral Infection

et al. 2017

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Tripartite motif (TRIM) proteins are involved in various cellular functions and constitute key factors of the antiviral innate immune response. TRIM proteins can bind viral particles directly, sending them to degradation by the proteasome, or ubiquitinate signaling molecules leading to upregulation of innate immunity. TRIM proteins are present in across metazoans but are particularly numerous in vertebrates where genes comprising a B30.2 domain have been often duplicated. In fish, a TRIM subset named finTRIM is highly diversified, with large gene numbers and clear signatures of positive selection in the B30.2 domain suggesting they may be involved in antiviral mechanisms. finTRIM provides a beautiful model to investigate the primordial implication of B30.2 TRIM subsets in the arsenal of vertebrate antiviral defenses. We show here that ftr83, a zebrafish fintrim gene mainly expressed in the gills, skin and pharynx, encodes a protein affording a potent antiviral activity. In vitro, overexpression of FTR83, but not of its close relative FTR82, induced IFN and IFN-stimulated gene expression and afforded protection against different enveloped and non-enveloped RNA viruses. The kinetics of IFN induction paralleled the development of the antiviral activity, which was abolished by a dominant negative IRF3 mutant. In the context of a viral infection, FTR83 potentiated the IFN response. Expression of chimeric proteins in which the B30.2 domain of FTR83 and the non-protective FTR82 had been exchanged, showed that IFN upregulation and antiviral activity requires both the Ring/BBox/Coiled coil domain (supporting E3 ubiquitin ligase) and the B30.2 domain of FTR83. Finally, loss of function experiments in zebrafish embryos confirms that ftr83 mediates antiviral activity in vivo. Our results show that a member of the largest TRIM subset observed in fish upregulates type I IFN response and afford protection against viral infections, supporting that TRIMs are key antiviral factors across vertebrates.

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The Proto-MHC of Placozoans, a Region Specialized in Cellular Stress and Ubiquitination/Proteasome Pathways

Abstract: International audienc

Cited by 23 publications

References 76 publications

The VÎ³9VÎ´2 T Cell Antigen Receptor and Butyrophilin-3 A1: Models of Interaction, the Possibility of Co-Evolution, and the Case of Dendritic Epidermal T Cells

The VÎ³9VÎ´2 T Cell Antigen Receptor and Butyrophilin-3 A1: Models of Interaction, the Possibility of Co-Evolution, and the Case of Dendritic Epidermal T Cells

Location, location, location: the evolutionary history of CD1 genes and the NKR-P1/ligand systems

FTR83, a Member of the Large Fish-Specific finTRIM Family, Triggers IFN Pathway and Counters Viral Infection

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