A Combinatorial Semaphorin Code Instructs the Initial Steps of Sensory Circuit Assembly in the Drosophila CNS

Neuron. 2011 Apr 28;70(2):281-98. doi: 10.1016/j.neuron.2011.02.050.

Abstract

Longitudinal axon fascicles within the Drosophila embryonic CNS provide connections between body segments and are required for coordinated neural signaling along the anterior-posterior axis. We show here that establishment of select CNS longitudinal tracts and formation of precise mechanosensory afferent innervation to the same CNS region are coordinately regulated by the secreted semaphorins Sema-2a and Sema-2b. Both Sema-2a and Sema-2b utilize the same neuronal receptor, plexin B (PlexB), but serve distinct guidance functions. Localized Sema-2b attraction promotes the initial assembly of a subset of CNS longitudinal projections and subsequent targeting of chordotonal sensory afferent axons to these same longitudinal connectives, whereas broader Sema-2a repulsion serves to prevent aberrant innervation. In the absence of Sema-2b or PlexB, chordotonal afferent connectivity within the CNS is severely disrupted, resulting in specific larval behavioral deficits. These results reveal that distinct semaphorin-mediated guidance functions converge at PlexB and are critical for functional neural circuit assembly.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Afferent Pathways / embryology
  • Afferent Pathways / physiology*
  • Alkaline Phosphatase / metabolism
  • Animals
  • Animals, Genetically Modified
  • Axons / physiology
  • Behavior, Animal
  • Body Patterning / genetics
  • Body Patterning / physiology*
  • Central Nervous System / cytology
  • Central Nervous System / embryology
  • Central Nervous System / physiology*
  • Drosophila
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism*
  • Embryo, Nonmammalian
  • Gene Expression Regulation, Developmental
  • Green Fluorescent Proteins / genetics
  • Membrane Glycoproteins / metabolism
  • Movement / physiology
  • Mutation / genetics
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / metabolism*
  • Neurons / cytology
  • Neurons / physiology*
  • Physical Stimulation
  • Receptors, Cell Surface / genetics
  • Receptors, Cell Surface / metabolism*
  • Semaphorins / classification
  • Semaphorins / genetics
  • Semaphorins / physiology*
  • Signal Transduction / genetics
  • Signal Transduction / physiology
  • Vibration

Substances

  • Drosophila Proteins
  • Membrane Glycoproteins
  • Nerve Tissue Proteins
  • Receptors, Cell Surface
  • Semaphorins
  • plexB protein, Drosophila
  • Green Fluorescent Proteins
  • Alkaline Phosphatase