Muscle- and Skin-Derived Cues Jointly Orchestrate Patterning of Somatosensory Dendrites

Carlos A. Díaz-Balzac, Maisha Rahman, María I. Lázaro-Peña, Lourdes A. Martin Hernandez, Yehuda Salzberg, Cristina Aguirre-Chen, Zaven Kaprielian, Hannes E. Bülow

Research output: Contribution to journalArticle

13 Scopus citations

Abstract

Sensory dendrite arbors are patterned through cell-autonomously and non-cell-autonomously functioning factors [1–3]. Yet, only a few non-cell-autonomously acting proteins have been identified, including semaphorins [4, 5], brain-derived neurotrophic factors (BDNFs) [6], UNC-6/Netrin [7], and the conserved MNR-1/Menorin–SAX-7/L1CAM cell adhesion complex [8, 9]. This complex acts from the skin to pattern the stereotypic dendritic arbors of PVD and FLP somatosensory neurons in Caenorhabditis elegans through the leucine-rich transmembrane receptor DMA-1/LRR-TM expressed on PVD neurons [8, 9]. Here we describe a role for the diffusible C. elegans protein LECT-2, which is homologous to vertebrate leukocyte cell-derived chemotaxin 2 (LECT2)/Chondromodulin II. LECT2/Chondromodulin II has been implicated in a variety of pathological conditions [10–13], but the developmental functions of LECT2 have remained elusive. We find that LECT-2/Chondromodulin II is required for development of PVD and FLP dendritic arbors and can act as a diffusible cue from a distance to shape dendritic arbors. Expressed in body-wall muscles, LECT-2 decorates neuronal processes and hypodermal cells in a pattern similar to the cell adhesion molecule SAX-7/L1CAM. LECT-2 functions genetically downstream of the MNR-1/Menorin–SAX-7/L1CAM adhesion complex and upstream of the DMA-1 receptor. LECT-2 localization is dependent on SAX-7/L1CAM, but not on MNR-1/Menorin or DMA-1/LRR-TM, suggesting that LECT-2 functions as part of the skin-derived MNR-1/Menorin-SAX-7/L1CAM adhesion complex. Collectively, our findings suggest that LECT-2/Chondromodulin II acts as a muscle-derived, diffusible cofactor together with a skin-derived cell adhesion complex to orchestrate the molecular interactions of three tissues during patterning of somatosensory dendrites.

Original languageEnglish (US)
Pages (from-to)2379-2387
Number of pages9
JournalCurrent Biology
Volume26
Issue number17
DOIs
StatePublished - Sep 12 2016

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ASJC Scopus subject areas

  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)

Cite this

Díaz-Balzac, C. A., Rahman, M., Lázaro-Peña, M. I., Martin Hernandez, L. A., Salzberg, Y., Aguirre-Chen, C., Kaprielian, Z., & Bülow, H. E. (2016). Muscle- and Skin-Derived Cues Jointly Orchestrate Patterning of Somatosensory Dendrites. Current Biology, 26(17), 2379-2387. https://doi.org/10.1016/j.cub.2016.07.008