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Allorecognition Proteins in an Invertebrate Exhibit Homophilic Interactions

2015; Elsevier BV; Volume: 25; Issue: 21 Linguagem: Inglês

10.1016/j.cub.2015.09.030

1879-0445

Uma Karadge, Minja Gosto, Matthew L. Nicotra,

Myxozoan Parasites in Aquatic Species

Sessile colonial invertebrates—animals such as sponges, corals, bryozoans, and ascidians—can distinguish between their own tissues and those of conspecifics upon contact [1Rosengarten R.D. Nicotra M.L. Model systems of invertebrate allorecognition.Curr. Biol. 2011; 21: R82-R92Abstract Full Text Full Text PDF PubMed Scopus (65) Google Scholar]. This ability, called allorecognition, mediates spatial competition and can prevent stem cell parasitism by ensuring that colonies only fuse with self or close kin. In every taxon studied to date, allorecognition is controlled by one or more highly polymorphic genes [2Scofield V.L. Schlumpberger J.M. West L.A. Weissman I.L. Protochordate allorecognition is controlled by a MHC-like gene system.Nature. 1982; 295: 499-502Crossref PubMed Scopus (320) Google Scholar, 3Mokady O. Buss L.W. Transmission genetics of allorecognition in Hydractinia symbiolongicarpus (Cnidaria:Hydrozoa).Genetics. 1996; 143: 823-827PubMed Google Scholar, 4Hughes R.N. Manríquez P.H. Morley S. Craig S.F. Bishop J.D. Kin or self-recognition? Colonial fusibility of the bryozoan Celleporella hyalina.Evol. Dev. 2004; 6: 431-437Crossref PubMed Scopus (37) Google Scholar, 5Cadavid L.F. Powell A.E. Nicotra M.L. Moreno M. Buss L.W. An invertebrate histocompatibility complex.Genetics. 2004; 167: 357-365Crossref PubMed Scopus (73) Google Scholar, 6De Tomaso A.W. Nyholm S.V. Palmeri K.J. Ishizuka K.J. Ludington W.B. Mitchel K. Weissman I.L. Isolation and characterization of a protochordate histocompatibility locus.Nature. 2005; 438: 454-459Crossref PubMed Scopus (171) Google Scholar, 7Nyholm S.V. Passegue E. Ludington W.B. Voskoboynik A. Mitchel K. Weissman I.L. De Tomaso A.W. fester, A candidate allorecognition receptor from a primitive chordate.Immunity. 2006; 25: 163-173Abstract Full Text Full Text PDF PubMed Scopus (79) Google Scholar, 8Voskoboynik A. Newman A.M. Corey D.M. Sahoo D. Pushkarev D. Neff N.F. Passarelli B. Koh W. Ishizuka K.J. Palmeri K.J. et al.Identification of a colonial chordate histocompatibility gene.Science. 2013; 341: 384-387Crossref PubMed Scopus (64) Google Scholar]. However, in no case is it understood how the proteins encoded by these genes discriminate self from non-self. In the cnidarian Hydractinia symbiolongicarpus, allorecognition is controlled by at least two highly polymorphic allorecognition genes, Alr1 and Alr2 [3Mokady O. Buss L.W. Transmission genetics of allorecognition in Hydractinia symbiolongicarpus (Cnidaria:Hydrozoa).Genetics. 1996; 143: 823-827PubMed Google Scholar, 5Cadavid L.F. Powell A.E. Nicotra M.L. Moreno M. Buss L.W. An invertebrate histocompatibility complex.Genetics. 2004; 167: 357-365Crossref PubMed Scopus (73) Google Scholar, 9Powell A.E. Nicotra M.L. Moreno M.A. Lakkis F.G. Dellaporta S.L. Buss L.W. Differential effect of allorecognition loci on phenotype in Hydractinia symbiolongicarpus (Cnidaria: Hydrozoa).Genetics. 2007; 177: 2101-2107Crossref PubMed Scopus (27) Google Scholar, 10Powell A.E. Moreno M. Gloria-Soria A. Lakkis F.G. Dellaporta S.L. Buss L.W. Genetic background and allorecognition phenotype in Hydractinia symbiolongicarpus.G3 (Bethesda). 2011; 1: 499-504Crossref PubMed Scopus (11) Google Scholar, 11Nicotra M.L. Powell A.E. Rosengarten R.D. Moreno M. Grimwood J. Lakkis F.G. Dellaporta S.L. Buss L.W. A hypervariable invertebrate allodeterminant.Curr. Biol. 2009; 19: 583-589Abstract Full Text Full Text PDF PubMed Scopus (81) Google Scholar, 12Rosa S.F. Powell A.E. Rosengarten R.D. Nicotra M.L. Moreno M.A. Grimwood J. Lakkis F.G. Dellaporta S.L. Buss L.W. Hydractinia allodeterminant alr1 resides in an immunoglobulin superfamily-like gene complex.Curr. Biol. 2010; 20: 1122-1127Abstract Full Text Full Text PDF PubMed Scopus (49) Google Scholar]. Sequence variation at each gene predicts allorecognition in laboratory strains such that colonies reject if they do not share a common allele at either locus, fuse temporarily if they share an allele at only one locus, or fuse permanently if they share an allele at both genes [5Cadavid L.F. Powell A.E. Nicotra M.L. Moreno M. Buss L.W. An invertebrate histocompatibility complex.Genetics. 2004; 167: 357-365Crossref PubMed Scopus (73) Google Scholar, 9Powell A.E. Nicotra M.L. Moreno M.A. Lakkis F.G. Dellaporta S.L. Buss L.W. Differential effect of allorecognition loci on phenotype in Hydractinia symbiolongicarpus (Cnidaria: Hydrozoa).Genetics. 2007; 177: 2101-2107Crossref PubMed Scopus (27) Google Scholar]. Here, we show that the gene products of Alr1 and Alr2 (Alr1 and Alr2) are self-ligands with extraordinary specificity. Using an in vitro cell aggregation assay, we found that Alr1 and Alr2 bind to themselves homophilically across opposing cell membranes. For both proteins, each isoform bound only to itself or to an isoform of nearly identical sequence. These results provide a mechanistic explanation for the exquisite specificity of Hydractinia allorecognition. Our results also indicate that hydroids have evolved a molecular strategy of self-recognition that is unique among characterized allorecognition systems within and outside invertebrates.