A tetrapod‐like repertoire of innate immune receptors and effectors for coelacanths

Abstract

The recent availability of both robust transcriptome and genome resources for coelacanth (Latimeria chalumnae) has led to unique discoveries for coelacanth immunity such as the lack of IgM, a central component of adaptive immunity. This study was designed to more precisely address the origins and evolution of gene families involved in the initial recognition and response to microbial pathogens, which effect innate immunity. Several multigene families involved in innate immunity are addressed, including: Toll-like receptors (TLRs), retinoic acid inducible gene 1 (RIG1)-like receptors (RLRs), the nucleotide-binding domain and leucine-rich repeat containing proteins (NLRs), diverse immunoglobulin domain-containing proteins (DICP) and modular domain immune-type receptors (MDIRs). Our analyses also include the tripartite motif-containing proteins (TRIM), which are involved in pathogen recognition as well as the positive regulation of antiviral immunity. Finally, this study addressed some of the downstream effectors of the antimicrobial response including IL-1 family members, type I and II interferons (IFN) and IFN-stimulated effectors (ISGs). Collectively, the genes and gene families in coelacanth that effect innate immune functions share characteristics both in content, structure and arrangement with those found in tetrapods but not in teleosts. The findings support the sister group relationship of coelacanth fish with tetrapods.

Identification and characterisation of TLR18-21 genes in Atlantic salmon (Salmo salar)

“…To date, in addition to homologues of the mammalian TLR genes, many so-called non-mammalian TLRs have been found in several vertebrates by comprehensive genome survey and gene cloning [14], but the types and numbers may differ between species due to genome/ gene duplication events and environmental adaptation [14]. For example, only one copy of TLR22 was found in lamprey [13], coelacanth [14] and frog [27], while two TLR22 genes are found in several teleost species such as rainbow trout, Atlantic salmon [19] and channel catfish [16], and Atlantic cod possess an expanded number (12) of TLR22 genes [18]. Among non-mammalian TLRs, TLR18, TLR19, TLR20, TLR25 and TLR26 are considered teleost specific with the last two types of TLR found only in channel catfish [16].…”

“…These can be divided into six major families, namely TLR1, TLR3, TLR4, TLR5, TLR7 and TLR11 [10]. The so called "fish-specific" TLRs [11] or "non-mammalian" TLRs (as TLR21 is also found in birds and amphibians [12]) include TLR18-TLR27, with TLR24 only present in jawless fish [13] and TLR27 in coelacanth (Latimeria chalumnae) [14]. Many of these non-mammalian TLRs have been reported in teleost species, such as zebrafish (TLR18-22) [15], channel catfish (TLR18-22 and TLR25-26) [16], fugu (TLR21-23) [10], common carp (TLR20) [17] and Atlantic cod (TLR21, TLR22a-l and TLR23a-b) [18].…”

A formalin-inactivated immunogen against viral encephalopathy and retinopathy (VER) disease in European sea bass (Dicentrarchus labrax): immunological and protection effects

“…administration in sea bass, we examined the effects on the transcription of genes coding for antiviral responses. Interferon exerts its biological functions mainly through the downstream activation of Mx and ISG genes [39–42], which are both interferon-inducible and known to play an active-role in antiviral immune responses [43, 44]. Mx proteins are key players of antiviral responses, triggered by interferon type I (IFN-I) in response to viral infections and have been considered the main factor in determining the resistance of fish species to nodavirus infections.…”

Evolution of Innate Immunity: Clues from Invertebrates via Fish to Mammals

“…Following receptor–ligand binding, signal transduction initiates a complex cascade of reactions, which leads to production of one or more of a wide array of effector molecules eventually resulting in elimination or inactivation of the intruder. A large number of TLRs are known with individual affinities to various PAMPs (28). TLRs have been traced to the most ancient multicellular invertebrates such as sponges, cnidarians (29), oligochaetes (earthworms) (30), mollusks (snails and mussels) (31), crustaceans (e.g., shrimps), and insects (32).…”

“…The echinoderms, representing the most developed invertebrates, exhibit a complex and rich array of innate recognition molecules where among TLRs are present in numerous copies (33). The most primitive fish, the agnathans, have at least 7 identified TLRs, bony fish at least 18, amphibians 14, birds 10, and mammals 13 (28). One major receptor group comprises the scavenger receptors binding bacteria and a range of antigens including lipoproteins, which are polyanionic (34).…”