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Family of neural wiring receptors in bilaterians defined by phylogenetic, biochemical, and structural evidence.

ABSTRACT: The evolution of complex nervous systems was accompanied by the expansion of numerous protein families, including cell-adhesion molecules, surface receptors, and their ligands. These proteins mediate axonal guidance, synapse targeting, and other neuronal wiring-related functions. Recently, 32 interacting cell surface proteins belonging to two newly defined families of the Ig superfamily (IgSF) in fruit flies were discovered to label different subsets of neurons in the brain and ventral nerve cord. They have been shown to be involved in synaptic targeting and morphogenesis, retrograde signaling, and neuronal survival. Here, we show that these proteins, Dprs and DIPs, are members of a widely distributed family of two- and three-Ig domain molecules with neuronal wiring functions, which we refer to as Wirins. Beginning from a single ancestral Wirin gene in the last common ancestor of Bilateria, numerous gene duplications produced the heterophilic Dprs and DIPs in protostomes, along with two other subfamilies that diversified independently across protostome phyla. In deuterostomes, the ancestral Wirin evolved into the IgLON subfamily of neuronal receptors. We show that IgLONs interact with each other and that their complexes can be broken by mutations designed using homology models based on Dpr and DIP structures. The nematode orthologs ZIG-8 and RIG-5 also form heterophilic and homophilic complexes, and crystal structures reveal numerous apparently ancestral features shared with Dpr-DIP complexes. The evolutionary, biochemical, and structural relationships we demonstrate here provide insights into neural development and the rise of the metazoan nervous system.

SUBMITTER: Cheng S

PROVIDER: S-EPMC6525511 | biostudies-literature | 2019 May

REPOSITORIES: biostudies-literature

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Family of neural wiring receptors in bilaterians defined by phylogenetic, biochemical, and structural evidence.

Cheng Shouqiang S Park Yeonwoo Y Kurleto Justyna D JD Jeon Mili M Zinn Kai K Thornton Joseph W JW Özkan Engin E

Proceedings of the National Academy of Sciences of the United States of America 20190501 20

The evolution of complex nervous systems was accompanied by the expansion of numerous protein families, including cell-adhesion molecules, surface receptors, and their ligands. These proteins mediate axonal guidance, synapse targeting, and other neuronal wiring-related functions. Recently, 32 interacting cell surface proteins belonging to two newly defined families of the Ig superfamily (IgSF) in fruit flies were discovered to label different subsets of neurons in the brain and ventral nerve cor ...[more]

PMID: 31043568

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Project description:BackgroundSall (Spalt-like) proteins are zinc-finger transcription factors involved in a number of biological processes. They have only been studied in a few model organisms, such as Drosophila melanogaster, Caenorhabditis elegans, Schmidtea mediterranea and some vertebrates. Further taxon sampling is critical to understand the evolution and diversification of this protein and its functional roles in animals.ResultsUsing genome and transcriptome mining, we confirmed the presence of sall genes in a range of additional animal taxa, for which their presence had not yet been described. We show that sall genes are broadly conserved across the Bilateria, and likely appeared in the bilaterian stem lineage. Our analysis of the protein domains shows that the characteristic arrangement of the multiple zinc-finger domains is conserved in bilaterians and may represent the ancient arrangement of this family of transcription factors. We also show the existence of a previously unknown zinc-finger domain. In situ hybridization was used to describe the gene expression patterns in embryonic and larval stages in two species of snails: Crepidula fornicata and Lottia gigantea. In L. gigantea, sall presents maternal expression, although later on the expression is restricted to the A and B quadrants during gastrulation and larval stage. In C. fornicata, sall has no maternal expression and it is expressed mainly in the A, C and D quadrants during blastula stages and in an asymmetric fashion during the larval stage.DiscussionOur results suggest that the bilaterian common ancestor had a Sall protein with at least six zinc-finger domains. The evolution of Sall proteins in bilaterians might have occurred mostly as a result of the loss of protein domains and gene duplications leading to diversification. The new evidence complements previous studies in highlighting an important role of Sall proteins in bilaterian development. Our results show maternal expression of sall in the snail L. gigantea, but not C. fornicata. The asymmetric expression shown in the ectoderm of the trochophore larva of snails is probably related to shell/mantle development. The observed sall expression in cephalic tissue in snails and some other bilaterians suggests a possible ancestral role of sall in neural development in bilaterians.

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Family of neural wiring receptors in bilaterians defined by phylogenetic, biochemical, and structural evidence.

Publications

Family of neural wiring receptors in bilaterians defined by phylogenetic, biochemical, and structural evidence.

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