A multi-protein receptor-ligand complex underlies combinatorial dendrite guidance choices in C. elegans

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Abstract

Ligand receptor interactions instruct axon guidance during development. How dendrites are guided to specific targets is less understood. The C. elegans PVD sensory neuron innervates muscle-skin interface with its elaborate dendritic branches. Here, we found that LECT-2, the ortholog of leukocyte cell-derived chemotaxin-2 (LECT2), is secreted from the muscles and required for muscle innervation by PVD. Mosaic analyses showed that LECT-2 acted locally to guide the growth of terminal branches. Ectopic expression of LECT-2 from seam cells is sufficient to redirect the PVD dendrites onto seam cells. LECT-2 functions in a multi-protein receptor-ligand complex that also contains two transmembrane ligands on the skin, SAX-7/L1CAM and MNR-1, and the neuronal transmembrane receptor DMA-1. LECT-2 greatly enhances the binding between SAX-7, MNR-1 and DMA-1. The activation of DMA-1 strictly requires all three ligands, which establishes a combinatorial code to precisely target and pattern dendritic arbors.

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Wei Zou

Department of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United States

Competing interests
No competing interests declared.
Ao Shen

Department of Pharmacology, University of California, Davis, Davis, United States

Competing interests
No competing interests declared.
Xintong Dong

Department of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United States

Competing interests
No competing interests declared.
Madina Tugizova

Department of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United States

Competing interests
No competing interests declared.
Yang K Xiang

Department of Pharmacology, University of California, Davis, Davis, United States

Competing interests
No competing interests declared.
Kang Shen

Department of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United States

For correspondence
kangshen@stanford.edu

Competing interests
Kang Shen, Reviewing editor, eLife.

"This ORCID iD identifies the author of this article:" 0000-0003-4059-8249

Funding

Howard Hughes Medical Institute

Wei Zou
Xintong Dong
Madina Tugizova
Kang Shen

National Institute of Neurological Disorders and Stroke (1R01NS082208)

Wei Zou
Xintong Dong
Madina Tugizova
Kang Shen

National Heart, Lung, and Blood Institute (R01HL127764-01)

Ao Shen
Yang K Xiang

American Heart Association

Ao Shen

NIH Office of Research Infrastructure Programs (P40 OD010440)

Kang Shen

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

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This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.