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Chelicerata sDscam isoforms combine homophilic specificities to define unique cell recognition

Zhou, Fengyan ; Cao, Guozheng ; Dai, Songjun ; Li, Guo ; Li, Hao ; Ding, Zhu ; Hou, Shouqing ; Xu, Bingbing ; You, Wendong ; Wiseglass, Gil ; Shi, Feng ; Yang, Xiaofeng ; Rubinstein, Rotem ; Jin, Yongfeng

Proceedings of the National Academy of Sciences - PNAS, 2020-10, Vol.117 (40), p.24813-24824 [Periódico revisado por pares]

United States: National Academy of Sciences

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Título:
Chelicerata sDscam isoforms combine homophilic specificities to define unique cell recognition
Autor: Zhou, Fengyan ; Cao, Guozheng ; Dai, Songjun ; Li, Guo ; Li, Hao ; Ding, Zhu ; Hou, Shouqing ; Xu, Bingbing ; You, Wendong ; Wiseglass, Gil ; Shi, Feng ; Yang, Xiaofeng ; Rubinstein, Rotem ; Jin, Yongfeng
Assuntos: Animals ; Arthropod Proteins - genetics ; Arthropod Proteins - metabolism ; Arthropods - classification ; Arthropods - genetics ; Arthropods - metabolism ; Avoidance ; Biological Sciences ; Cell adhesion ; Cell adhesion & migration ; Cell adhesion molecules ; Cell Adhesion Molecules - chemistry ; Cell Adhesion Molecules - genetics ; Cell Adhesion Molecules - metabolism ; Cell Communication ; Cell interactions ; Cell recognition ; Chelicerata ; Combinatorial analysis ; Discrimination ; Domains ; Down's syndrome ; Drosophila - genetics ; Drosophila - metabolism ; Drosophila Proteins - chemistry ; Drosophila Proteins - genetics ; Drosophila Proteins - metabolism ; DSCAM protein ; Evolution ; Fibronectin ; Immunoglobulins ; Insects ; Isoforms ; Neural cell adhesion molecule ; Neural networks ; Neurons - metabolism ; Protein Isoforms - genetics ; Protein Isoforms - metabolism ; Proteins ; Recognition ; Vertebrates
É parte de: Proceedings of the National Academy of Sciences - PNAS, 2020-10, Vol.117 (40), p.24813-24824
Notas: ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 23
Edited by Barry Honig, Howard Hughes Medical Institute, Columbia University, New York, NY, and approved August 20, 2020 (received for review December 15, 2019)
Author contributions: Y.J. conceived this project; F.Z., G.C., S.D., G.L., H.L., B.X., and Y.J. designed research; F.Z., G.C., S.D., G.L., and H.L. performed research; F.Z., Z.D., and S.H. performed homology modeling and protein–protein docking; F.Z., Z.D., S.H., B.X., W.Y., G.W., F.S., X.Y., R.R., and Y.J. analyzed data; and F.Z., R.R., and Y.J. wrote the paper.
Descrição: Thousands of Down syndrome cell adhesion molecule (Dscam1) isoforms and ∼60 clustered protocadhrein (cPcdh) proteins are required for establishing neural circuits in insects and vertebrates, respectively. The strict homophilic specificity exhibited by these proteins has been extensively studied and is thought to be critical for their function in neuronal self-avoidance. In contrast, significantly less is known about the Dscam1-related family of ∼100 shortened Dscam (sDscam) proteins in Chelicerata. We report that Chelicerata sDscamα and some sDscamβ protein trans interactions are strictly homophilic, and that the trans interaction is meditated via the first Ig domain through an antiparallel interface. Additionally, different sDscam isoforms interact promiscuously in cis via membrane proximate fibronectin-type III domains. We report that cell–cell interactions depend on the combined identity of all sDscam isoforms expressed. A single mismatched sDscam isoform can interfere with the interactions of cells that otherwise express an identical set of isoforms. Thus, our data support a model by which sDscam association in cis and trans generates a vast repertoire of combinatorial homophilic recognition specificities. We propose that in Chelicerata, sDscam combinatorial specificity is sufficient to provide each neuron with a unique identity for self–nonself discrimination. Surprisingly, while sDscams are related to Drosophila Dscam1, our results mirror the findings reported for the structurally unrelated vertebrate cPcdh. Thus, our findings suggest a remarkable example of convergent evolution for the process of neuronal self-avoidance and provide insight into the basic principles and evolution of metazoan self-avoidance and self–nonself discrimination.
Editor: United States: National Academy of Sciences
Idioma: Inglês

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Chelicerata sDscam isoforms combine homophilic specificities to define unique cell recognition

Zhou, Fengyan ; Cao, Guozheng ; Dai, Songjun ; Li, Guo ; Li, Hao ; Ding, Zhu ; Hou, Shouqing ; Xu, Bingbing ; You, Wendong ; Wiseglass, Gil ; Shi, Feng ; Yang, Xiaofeng ; Rubinstein, Rotem ; Jin, Yongfeng

United States: National Academy of Sciences

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