An innexin-dependent cell network establishes left-right neuronal asymmetry in C. elegans.
Gap junctions are widespread in immature neuronal circuits, but their functional significance is poorly understood. We show here that a transient network formed by the innexin gap-junction protein NSY-5 coordinates left-right asymmetry in the developing nervous system of Caenorhabditis elegans. nsy-5 is required for the left and right AWC olfactory neurons to establish stochastic, asymmetric patterns of gene expression during embryogenesis. nsy-5-dependent gap junctions in the embryo transiently connect the AWC cell bodies with those of numerous other neurons. Both AWCs and several other classes of nsy-5-expressing neurons participate in signaling that coordinates left-right AWC asymmetry. The right AWC can respond to nsy-5 directly, but the left AWC requires nsy-5 function in multiple cells of the network. NSY-5 forms hemichannels and intercellular gap-junction channels in Xenopus oocytes, consistent with a combination of cell-intrinsic and network functions. These results provide insight into gap-junction activity in developing circuits.
Chuang
Chiou-Fen
CF
Howard Hughes Medical Institute, The Rockefeller University, 1230 York Avenue, New York, NY 10021, USA.
Vanhoven
Miri K
MK
Fetter
Richard D
RD
Verselis
Vytas K
VK
Bargmann
Cornelia I
CI
D000595:Amino Acid Sequence; D000818:Animals; D001483:Base Sequence; D019521:Body Patterning / Q000502:physiology*; D017173:Caenorhabditis elegans / Q000196:embryology* / Q000378:metabolism / Q000648:ultrastructure; D029742:Caenorhabditis elegans Proteins / Q000235:genetics / Q000302:isolation & purification / Q000378:metabolism*; D020013:Calcium Signaling / Q000502:physiology; D002450:Cell Communication / Q000502:physiology; D002454:Cell Differentiation / Q000502:physiology; D017630:Connexins / Q000235:genetics / Q000302:isolation & purification / Q000378:metabolism*; D007839:Functional Laterality / Q000502:physiology; D017629:Gap Junctions / Q000378:metabolism; D008565:Membrane Proteins / Q000378:metabolism; D008969:Molecular Sequence Data; D009415:Nerve Net / Q000196:embryology* / Q000378:metabolism / Q000648:ultrastructure; D009420:Nervous System / Q000196:embryology* / Q000378:metabolism / Q000648:ultrastructure; D009474:Neurons / Q000378:metabolism* / Q000648:ultrastructure; D009833:Olfactory Pathways / Q000196:embryology / Q000378:metabolism / Q000648:ultrastructure
D029742:Caenorhabditis elegans Proteins; D017630:Connexins; D008565:Membrane Proteins; C521128:inx-19 protein, C elegans; C093204:unc-2 protein, C elegans