LMO4 controls the balance between excitatory and inhibitory spinal V2 interneurons

Neuron. 2009 Mar 26;61(6):839-51. doi: 10.1016/j.neuron.2009.02.011.

Abstract

Multiple excitatory and inhibitory interneurons form the motor circuit with motor neurons in the ventral spinal cord. Notch signaling initiates the diversification of immature V2-interneurons into excitatory V2a-interneurons and inhibitory V2b-interneurons. Here, we provide a transcriptional regulatory mechanism underlying their balanced production. LIM-only protein LMO4 controls this binary cell fate choice by regulating the activity of V2a- and V2b-specific LIM complexes inversely. In the spinal cord, LMO4 induces GABAergic V2b-interneurons in collaboration with SCL and inhibits Lhx3 from generating glutamatergic V2a-interneuons. In LMO4;SCL compound mutant embryos, V2a-interneurons increase markedly at the expense of V2b-interneurons. We further demonstrate that LMO4 nucleates the assembly of a novel LIM-complex containing SCL, Gata2, and NLI. This complex activates specific enhancers in V2b-genes consisting of binding sites for SCL and Gata2, thereby promoting V2b-interneuron fate. Thus, LMO4 plays essential roles in directing a balanced generation of inhibitory and excitatory neurons in the ventral spinal cord.

Publication types

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

MeSH terms

  • Adaptor Proteins, Signal Transducing
  • Animals
  • Basic Helix-Loop-Helix Transcription Factors / genetics
  • Cell Adhesion Molecules, Neuronal
  • Cell Differentiation / drug effects
  • Cells, Cultured
  • Chickens
  • Chromatin Immunoprecipitation / methods
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • Embryo, Mammalian
  • GATA3 Transcription Factor / genetics
  • GATA3 Transcription Factor / metabolism
  • Gene Expression Regulation, Developmental / genetics
  • Gene Expression Regulation, Developmental / physiology*
  • Homeodomain Proteins / genetics
  • Homeodomain Proteins / metabolism
  • Homeodomain Proteins / physiology*
  • Humans
  • Interneurons / physiology*
  • LIM Domain Proteins
  • Mice
  • Mice, Mutant Strains
  • Models, Biological
  • Multiprotein Complexes / genetics
  • Multiprotein Complexes / metabolism
  • Neural Cell Adhesion Molecules / genetics
  • Neural Cell Adhesion Molecules / metabolism
  • Neural Inhibition / physiology*
  • Protein Binding / genetics
  • Proto-Oncogene Proteins / genetics
  • RNA, Messenger / metabolism
  • Spinal Cord / cytology
  • T-Cell Acute Lymphocytic Leukemia Protein 1
  • Transcription Factors / genetics
  • Transcription Factors / metabolism
  • Transcription Factors / physiology*
  • Transfection / methods
  • Vesicular Glutamate Transport Protein 2 / genetics
  • gamma-Aminobutyric Acid / metabolism

Substances

  • Adaptor Proteins, Signal Transducing
  • Basic Helix-Loop-Helix Transcription Factors
  • Cell Adhesion Molecules, Neuronal
  • DNA-Binding Proteins
  • GATA3 Transcription Factor
  • Gata3 protein, mouse
  • Homeodomain Proteins
  • LIM Domain Proteins
  • Lmo4 protein, mouse
  • Multiprotein Complexes
  • Neural Cell Adhesion Molecules
  • Proto-Oncogene Proteins
  • RNA, Messenger
  • Slc17a6 protein, mouse
  • Ssbp3 protein, mouse
  • T-Cell Acute Lymphocytic Leukemia Protein 1
  • Tal1 protein, mouse
  • Transcription Factors
  • Vesicular Glutamate Transport Protein 2
  • Vsx2 protein, mouse
  • neuroligin 1
  • gamma-Aminobutyric Acid