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Ig Superfamily Ligand and Receptor Pairs Expressed in Synaptic Partners in Drosophila

Tan, Liming and Zhang, Kelvin Xi and Pecot, Matthew Y. and Nagarkar-Jaiswal, Sonal and Lee, Pei-Tseng and Takemura, Shin-ya and McEwen, Jason M. and Nern, Aljoscha and Xu, Shuwa and Tadros, Wael and Chen, Zhenqing and Zinn, Kai and Bellen, Hugo J. and Morey, Marta and Zipursky, S. Lawrence (2015) Ig Superfamily Ligand and Receptor Pairs Expressed in Synaptic Partners in Drosophila. Cell, 163 (7). pp. 1756-1769. ISSN 0092-8674. PMCID PMC4804707. https://resolver.caltech.edu/CaltechAUTHORS:20151218-113427419

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Abstract

Information processing relies on precise patterns of synapses between neurons. The cellular recognition mechanisms regulating this specificity are poorly understood. In the medulla of the Drosophila visual system, different neurons form synaptic connections in different layers. Here, we sought to identify candidate cell recognition molecules underlying this specificity. Using RNA sequencing (RNA-seq), we show that neurons with different synaptic specificities express unique combinations of mRNAs encoding hundreds of cell surface and secreted proteins. Using RNA-seq and protein tagging, we demonstrate that 21 paralogs of the Dpr family, a subclass of immunoglobulin (Ig)-domain containing proteins, are expressed in unique combinations in homologous neurons with different layer-specific synaptic connections. Dpr interacting proteins (DIPs), comprising nine paralogs of another subclass of Ig-containing proteins, are expressed in a complementary layer-specific fashion in a subset of synaptic partners. We propose that pairs of Dpr/DIP paralogs contribute to layer-specific patterns of synaptic connectivity.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1016/j.cell.2015.11.021DOIArticle
http://www.cell.com/cell/abstract/S0092-8674%2815%2901501-9PublisherArticle
http://www.sciencedirect.com/science/article/pii/S0092867415015019#appd003PublisherSupplemental material
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4804707PubMed CentralArticle
ORCID:
AuthorORCID
Zinn, Kai0000-0002-6706-5605
Additional Information:© 2015 Elsevier Inc. Received: April 23, 2015; Received in revised form: September 27, 2015; Accepted: November 10, 2015. Published: December 17, 2015. We thank Orkun Akin, John Carlson, Claude Desplan, Yasushi Hiromi, Frank Laski, Cheng-yu Lee for sharing reagents; members of our laboratory for discussion; Louis K. Scheffer and Ian Meinertzhagen for discussions, sharing results from the EM studies at Janelia Research Campus (HHMI) and comments on the manuscript; Kaushiki Menon and Robert Carrillo (Zinn group) for communicating results prior to publication; Donghui Cheng, Tanya Stoyanova and Owen Witte for assistance in FACS purification of cells; Dorian Gunning for generating Bsh antibody; and Barret Pfeiffer and Gerald Rubin (JRC/HHMI) for reagents to construct the markers for R7 neurons. The work was supported by a Graduate Student Fellowship from the China Scholarship Council (CSC) and a Graduate Student Fellowship from the University of California, Los Angeles (UCLA) Philip Whitcome Training Program (L.T.); the Canadian Institute of Health Research Fellowship (K.X.Z.); Jane Coffin Childs Memorial Fund for Medical Research (M.P.); the Robert A. and Renee E. Belfer Family Foundation (S.N.-J.); Target A.L.S. (P.-T.L.); a Long-Term Fellowship from the Human Frontiers Science Program (W.T.); grants from National Institute of Health (R01GM067858 (H.J.B.), R01NS62821 (K.Z.), and R01NS28182 (K.Z.); a Ramon y Cajal contract (RYC-2011-09479) and a Ministerio de Economia y Competitividad grant (BFU2012-32282) (M.M.). H.J.B. and S.L.Z. are investigators of Howard Hughes Medical Institute.
Funders:
Funding AgencyGrant Number
China Scholarship CouncilUNSPECIFIED
University of California Los Angeles (UCLA)UNSPECIFIED
Canadian Institutes of Health Research (CIHR)UNSPECIFIED
Jane Coffin Childs Memorial Fund for Medical ResearchUNSPECIFIED
Robert A. and Renee E. Belfer Family FoundationUNSPECIFIED
Target ALSUNSPECIFIED
Human Frontiers Science ProgramUNSPECIFIED
NIHR01GM067858
NIHR01NS62821
NIHR01NS28182
Ramon y CajalRYC-2011-09479
Ministerio de Economía y Competitividad (MINECO)BFU2012-32282
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
Issue or Number:7
PubMed Central ID:PMC4804707
Record Number:CaltechAUTHORS:20151218-113427419
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20151218-113427419
Official Citation:Ig Superfamily Ligand and Receptor Pairs Expressed in Synaptic Partners in Drosophila Tan, Liming et al. Cell , Volume 163 , Issue 7 , 1756 - 1769
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:63073
Collection:CaltechAUTHORS
Deposited By: Ruth Sustaita
Deposited On:19 Dec 2015 00:07
Last Modified:03 Oct 2019 09:25

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