Schwannomin-interacting Protein 1 Isoform IQCJ-SCHIP1 Is a Multipartner Ankyrin- and Spectrin-binding Protein Involved in the Organization of Nodes of Ranvier

J Biol Chem. 2017 Feb 10;292(6):2441-2456. doi: 10.1074/jbc.M116.758029. Epub 2016 Dec 15.

Abstract

The nodes of Ranvier are essential regions for action potential conduction in myelinated fibers. They are enriched in multimolecular complexes composed of voltage-gated Nav and Kv7 channels associated with cell adhesion molecules. Cytoskeletal proteins ankyrin-G (AnkG) and βIV-spectrin control the organization of these complexes and provide mechanical support to the plasma membrane. IQCJ-SCHIP1 is a cytoplasmic protein present in axon initial segments and nodes of Ranvier. It interacts with AnkG and is absent from nodes and axon initial segments of βIV-spectrin and AnkG mutant mice. Here, we show that IQCJ-SCHIP1 also interacts with βIV-spectrin and Kv7.2/3 channels and self-associates, suggesting a scaffolding role in organizing nodal proteins. IQCJ-SCHIP1 binding requires a βIV-spectrin-specific domain and Kv7 channel 1-5-10 calmodulin-binding motifs. We then investigate the role of IQCJ-SCHIP1 in vivo by studying peripheral myelinated fibers in Schip1 knock-out mutant mice. The major nodal proteins are normally enriched at nodes in these mice, indicating that IQCJ-SCHIP1 is not required for their nodal accumulation. However, morphometric and ultrastructural analyses show an altered shape of nodes similar to that observed in βIV-spectrin mutant mice, revealing that IQCJ-SCHIP1 contributes to nodal membrane-associated cytoskeleton organization, likely through its interactions with the AnkG/βIV-spectrin network. Our work reveals that IQCJ-SCHIP1 interacts with several major nodal proteins, and we suggest that it contributes to a higher organizational level of the AnkG/βIV-spectrin network critical for node integrity.

Keywords: SCHIP1; animal model; axon; electron microscopy (EM); immunohistochemistry; nodal shape architecture; peripheral myelinated fibers; potassium channel; protein-protein interaction; spectrin.

MeSH terms

  • Animals
  • Ankyrins / metabolism*
  • Biopolymers / metabolism
  • COS Cells
  • Carrier Proteins / chemistry
  • Carrier Proteins / metabolism*
  • Chlorocebus aethiops
  • Mice
  • Mice, Mutant Strains
  • Motor Activity
  • Peripheral Nervous System / physiology
  • Peripheral Nervous System / ultrastructure
  • Ranvier's Nodes / metabolism*

Substances

  • Ankyrins
  • Biopolymers
  • Carrier Proteins
  • SCHIP1 protein, mouse
  • spectrin-binding proteins