Neural immunoglobulin superfamily interaction networks

Zinn, Kai; Özkan, Engin

doi:10.1016/j.conb.2017.05.010

Cited by 59 publications

(57 citation statements)

References 46 publications

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“…Many of the DEGs have been implicated in neuronal wiring specificity ( Figure 4). Approximately half of the DEGs encoded CSPs with cell adhesion domains (Ig/LRR), including multiple members of the dpr/DIP and beat/side families of interacting proteins (Zinn and Özkan, 2017); specific members of these families have been shown to regulate axon guidance and synaptic specificity in the developing fly nervous system. Taken together, these results reveal that the transcriptional organization of T4/T5 neurons mirrored their wiring patterns.…”

Section: Transcriptional Program Of a Single T4/t5 Subtypementioning

confidence: 99%

Modular transcriptional programs separately define axon and dendrite connectivity

Kurmangaliyev

Yoo

LoCascio

et al. 2019

Preprint

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Patterns of synaptic connectivity are remarkably precise and complex. Single-cell RNA sequencing has revealed a vast transcriptional diversity of neurons. Nevertheless, a clear logic underlying the transcriptional control of neuronal connectivity has yet to emerge. Here, we focused on Drosophila T4/T5 neurons, a class of closely related neuronal subtypes with different wiring patterns. Eight subtypes of T4/T5 neurons are defined by combinations of two patterns of dendritic inputs and four patterns of axonal outputs. Single-cell profiling during development revealed distinct transcriptional programs defining each dendrite and axon wiring pattern. These programs were defined by the expression of a few transcription factors and different combinations of cell surface proteins. Gain and loss of function studies provide evidence for independent control of different wiring features. We propose that modular transcriptional programs for distinct wiring features are assembled in different combinations to generate diverse patterns of neuronal connectivity.

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Section: Transcriptional Program Of a Single T4/t5 Subtypementioning

confidence: 99%

Modular transcriptional programs separately define axon and dendrite connectivity

Kurmangaliyev

Yoo

LoCascio

et al. 2019

Preprint

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“…Like DIPs and IgLONs, Nectins and Necls have three Ig domains (13). They are known to interact homo-and heterophilically, mediate cell-tocell interactions in the nervous and immune systems (13,14), and form complexes structurally similar to Dpr-DIP complexes (8). When the ECIA was performed with all five mouse IgLONs and eight out of nine Nectins and Necls, we saw that Nectins and Necls interact with each other but do not produce complexes with IgLONs ( Fig.…”

Section: Iglons Interact With Each Other As Predicted By Homology To mentioning

confidence: 94%

A new family of neural wiring receptors across bilaterians defined by phylogenetic, biochemical and structural evidence

Cheng¹,

Park

Kurleto

et al. 2018

Preprint

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The evolution of complex nervous systems was accompanied by the expansion of groups of protein families, most notably cell adhesion molecules, surface receptors and their ligands. These proteins mediate axonal guidance, synapse targeting, and other neuronal wiring-related functions. Recently, members of a set of thirty interacting cell surface proteins belonging to two newly defined families of the immunoglobulin 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, denoted as Dprs and DIPs, belong to a family of two and three-Ig domain molecules in bilaterians generally known for neuronal wiring functions. In protostomes, the ancestral Dpr/DIP gene has duplicated to form heterophilic partners, such as Dprs and DIPs, while in deuterostomes, they have evolved to create the IgLON family of neuronal receptors. In support of this phylogeny, 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. Similarly, the nematode orthologs ZIG-8 and RIG-5 can form heterophilic and homophilic complexes structurally matching Dpr-DIP and DIP-DIP complexes. The evolutionary, biochemical and structural relationships we demonstrate here provides insights into neural development and the rise of complexity in metazoans. Significance StatementCell surface receptors assign and display unique identities to neurons, and direct proper and robust wiring of neurons to create functional neural circuits. Recent work has identified two new classes of receptors in fruit flies, called the Dpr and DIP families with 30 members, which interact in 38 pairwise combinations. These proteins are implicated in neural identity, wiring and survival in many parts of the fly nervous system. Here, using evolutionary, biochemical and structural evidence, we show that Dprs and DIPs are members of an ancient bilaterian family of receptors. Members of this family share functional roles relevant to wiring across species, and are likely crucial in the emergence of the bilaterian nervous systems common to vertebrate and invertebrate animals.

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“…Our results suggest that mechanisms used to target axons and dendrites to specific cell types or layers may be further implicated to orchestrate the formation of axonal compartment. Pairwise IgSF molecular interactions are conserved in vertebrates and 35 invertebrates (32,33) implying similar mechanisms for the formation subcellular compartments in other organisms.…”

Section: Main Textmentioning

confidence: 99%

Transneuronal Dpr12/DIP-δ interactions facilitate compartmentalized dopaminergic innervation ofDrosophilamushroom body axons

Bornstein

Alyagor

Berkun

et al. 2019

Preprint

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15Precise connectivity of neurites to subcellular domains is a conserved feature of complex circuits, but the mechanisms defining precise wiring are largely unknown. The Drosophila mushroom-body is uniquely poised to study subcellular wiring as the adult γ-lobe harbors five distinct compartments, defined by localized innervations of other neuronal populations. Here we identify mechanisms required for precise wiring of γ-axons: Dpr12 and its interacting protein 20 DIP-δ are both enriched at the γ4/5 compartments. However, while Dpr12 is cell-autonomously required in γ-neurons, DIP-δ acts in dopaminergic neurons for the formation of the γ4/5 compartments and the correct network architecture. Furthermore, γ-axons grow into regions preoccupied by DIP-δ+ neurons suggesting that they innervate a prepatterned lobe. Thus, transneuronal interactions that mediate precise wiring are required for axon 25 compartmentalization. One Sentence Summary:Transneuronal interactions instruct precise wiring that enables localized innervation by specific neurons to distinct axonal compartments.

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Neural immunoglobulin superfamily interaction networks

Cited by 59 publications

References 46 publications

Modular transcriptional programs separately define axon and dendrite connectivity

Modular transcriptional programs separately define axon and dendrite connectivity

A new family of neural wiring receptors across bilaterians defined by phylogenetic, biochemical and structural evidence

Transneuronal Dpr12/DIP-δ interactions facilitate compartmentalized dopaminergic innervation ofDrosophilamushroom body axons

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