Identification and Characterization of a FcR Homolog in an Ectothermic Vertebrate, the Channel Catfish (Ictalurus punctatus)

Abstract

An FcR homolog (IpFcRI), representing the first such receptor from an ectothermic vertebrate, has been identified in the channel catfish (Ictalurus punctatus). Mining of the catfish expressed sequence tag databases using mammalian FcR sequences for CD16, CD32, and CD64 resulted in the identification of a teleost Ig-binding receptor. IpFcRI is encoded by a single-copy gene containing three Ig C2-like domains, but lacking a transmembrane segment and cytoplasmic tail. The encoded Ig domains of IpFcRI are phylogenetically and structurally related to mammalian FcR and the presence of a putative Fc-binding region appears to be conserved. IpFcRI-related genomic sequences are also present in both pufferfish and rainbow trout, indicating the likely presence of a soluble FcR in other fish species. Northern blot and qualitative PCR analyses demonstrated that IpFcRI is primarily expressed in IgM-negative leukocytes derived from the lymphoid kidney tissues and PBL. Significantly lower levels of IpFcRI expression were detected in catfish clonal leukocyte cell lines. Using the native leader, IpFcRI was secreted when transfected into insect cells and importantly the native IpFcRI glycoprotein was detected in catfish plasma using a polyclonal Ab. Recombinant IpFcRI binds catfish IgM as assessed by both coimmunoprecipation and cell transfection studies and it is presumed that it functions as a secreted FcR akin to the soluble FcR found in mammals. The identification of an FcR homolog in an ectothermic vertebrate is an important first step toward understanding the evolutionary history and functional importance of vertebrate Ig-binding receptors.

Fc Receptors for Immunoglobulins and Their Appearance during Vertebrate Evolution

“…This molecule has three Ig domains and, in the phylogenetic analysis, is most closely related to the FcRL molecules. This latter finding further supports the notion that the classical FcRs in mammals originate from FcRL molecules [67]. Related molecules to this IgM receptor have also been found in other fish species, where non-membrane anchored soluble molecule forms also exist [67].…”

“…Finally, there are similarities in domain structure between the IgG and IgE receptors and FcRL3, 4, 5 and A and B, indicating that the three first domains of FcγRI and the two domains of FcγRII, III and IV came from a FcRL3, 4, 5, A or B gene (Figure 5). Interestingly, an IgM receptor has been identified in the channel catfish ( Ictalurus punctatus ), which is most likely a soluble receptor as it lacks both a transmembrane region and a classical GPI anchor [67]. This molecule has three Ig domains and, in the phylogenetic analysis, is most closely related to the FcRL molecules.…”

Histamine is stored in mast cells of most evolutionarily advanced fish and regulates the fish inflammatory response

“…More recently, heterotypic aggregation with activated T cells (39) and the direct recognition of soluble mediators derived from infectious agents, such us lipopolysaccharide, have also been found to induce MC activation and mediator release (40). All these ''alternative'' mechanisms may operate in the activation of fish MCs, because the presence of receptors for IgM (41), anaphylatoxins (42) and soluble mediators derived from infectious agents (43) are all functional in these animals.…”

The chicken leukocyte receptor complex encodes a primordial, activating, high-affinity IgY Fc receptor

“…However, there is only scarce information regarding nonmammalian Fc receptors. A soluble Fc receptor homolog that binds to IgM has recently been described in the catfish (7). In an attempt to identify a chicken equivalent of the mammalian MHCrelated neonatal Fc receptor, a homologue of the secretory phospholipase A2 receptor that is expressed in the yolk sac has been identified.…”