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. Buelow

Research output: Contribution to journalArticle

13 Citations (Scopus)

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

Fingerprint

Neural Cell Adhesion Molecule L1
dendrites
Dendrites
skin (animal)
Cues
Muscle
Skin
chemoattractants
Chemotactic Factors
Physical vapor deposition
Dynamic mechanical analysis
Muscles
muscles
cell adhesion
Semaphorins
leukocytes
Leukocytes
Cell adhesion
Cell Adhesion
Neurons

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., ... Buelow, 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

Muscle- and Skin-Derived Cues Jointly Orchestrate Patterning of Somatosensory Dendrites. / Díaz-Balzac, Carlos A.; Rahman, Maisha; Lázaro-Peña, María I.; Martin Hernandez, Lourdes A.; Salzberg, Yehuda; Aguirre-Chen, Cristina; Kaprielian, Zaven; Buelow, Hannes E.

In: Current Biology, Vol. 26, No. 17, 12.09.2016, p. 2379-2387.

Research output: Contribution to journalArticle

Díaz-Balzac, CA, Rahman, M, Lázaro-Peña, MI, Martin Hernandez, LA, Salzberg, Y, Aguirre-Chen, C, Kaprielian, Z & Buelow, HE 2016, 'Muscle- and Skin-Derived Cues Jointly Orchestrate Patterning of Somatosensory Dendrites', Current Biology, vol. 26, no. 17, pp. 2379-2387. https://doi.org/10.1016/j.cub.2016.07.008
Díaz-Balzac CA, Rahman M, Lázaro-Peña MI, Martin Hernandez LA, Salzberg Y, Aguirre-Chen C et al. Muscle- and Skin-Derived Cues Jointly Orchestrate Patterning of Somatosensory Dendrites. Current Biology. 2016 Sep 12;26(17):2379-2387. https://doi.org/10.1016/j.cub.2016.07.008
Díaz-Balzac, Carlos A. ; Rahman, Maisha ; Lázaro-Peña, María I. ; Martin Hernandez, Lourdes A. ; Salzberg, Yehuda ; Aguirre-Chen, Cristina ; Kaprielian, Zaven ; Buelow, Hannes E. / Muscle- and Skin-Derived Cues Jointly Orchestrate Patterning of Somatosensory Dendrites. In: Current Biology. 2016 ; Vol. 26, No. 17. pp. 2379-2387.
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