TY - JOUR
T1 - Muscle- and Skin-Derived Cues Jointly Orchestrate Patterning of Somatosensory Dendrites
AU - Díaz-Balzac, Carlos A.
AU - Rahman, Maisha
AU - Lázaro-Peña, María I.
AU - Martin Hernandez, Lourdes A.
AU - Salzberg, Yehuda
AU - Aguirre-Chen, Cristina
AU - Kaprielian, Zaven
AU - Bülow, Hannes E.
N1 - Funding Information:
We thank S. Cook, K. Gritsman, O. Hobert, A. Meléndez, R. Townley, and members of the H.E.B. laboratory for comments on the manuscript and for discussion during the course of this work. We thank S. Chen and S. Rodriguez for help with initial experiments; the Caenorhabditis Genome Center for strains (funded by the NIH Office of Research Infrastructure Programs, P40OD010440); O. Hobert, N. Ramirez-Suarez, and K. Shen for reagents and discussions; and Yuji Kohara for the yk2005k01 cDNA clone. This work was funded in part through the NIH (R21NS081505 to H.E.B; T32GM007288 and F31HD066967 to C.A.D.-B.; T32GM07491 to M.I.L.-P. and C.A.-C.; and P30HD071593 and P30CA013330 to Albert Einstein College of Medicine) and a Human Genome Pilot Project from Albert Einstein College of Medicine. H.E.B. is an Irma T. Hirschl/Monique Weill-Caulier Research Fellow.
Publisher Copyright:
© 2016 Elsevier Ltd
PY - 2016/9/12
Y1 - 2016/9/12
N2 - 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.
AB - 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.
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U2 - 10.1016/j.cub.2016.07.008
DO - 10.1016/j.cub.2016.07.008
M3 - Article
C2 - 27451901
AN - SCOPUS:84995933530
SN - 0960-9822
VL - 26
SP - 2379
EP - 2387
JO - Current Biology
JF - Current Biology
IS - 17
ER -