Structural determinants controlling 14-3-3 recruitment to the endocytic adaptor Numb and dissociation of the Numb·α-adaptin complex

J Biol Chem. 2018 Mar 16;293(11):4149-4158. doi: 10.1074/jbc.RA117.000897. Epub 2018 Jan 30.

Abstract

Traffic of cargo across membranes helps establish, maintain, and reorganize distinct cellular compartments and is fundamental to many metabolic processes. The cargo-selective endocytic adaptor Numb participates in clathrin-dependent endocytosis by attaching cargoes to the clathrin adaptor α-adaptin. The phosphorylation of Numb at Ser265 and Ser284 recruits the regulatory protein 14-3-3, accompanied by the dissociation of Numb from α-adaptin and Numb's translocation from the cortical membrane to the cytosol. However, the molecular mechanisms underlying the Numb-α-adaptin interaction and its regulation by Numb phosphorylation and 14-3-3 recruitment remain poorly understood. Here, biochemical and structural analyses of the Numb·14-3-3 complex revealed that Numb phosphorylation at both Ser265 and Ser284 is required for Numb's efficient interaction with 14-3-3. We also discovered that an RQFRF motif surrounding Ser265 in Numb functions together with the canonical C-terminal DPF motif, required for Numb's interaction with α-adaptin, to form a stable complex with α-adaptin. Of note, we provide evidence that the phosphorylation-induced binding of 14-3-3 to Numb directly competes with the binding of α-adaptin to Numb. Our findings suggest a potential mechanism governing the dynamic assembly of Numb with α-adaptin or 14-3-3. This dual-site recognition of Numb by α-adaptin may have implications for other α-adaptin targets. We propose that the newly identified α-adaptin-binding site surrounding Ser265 in Numb functions as a triggering mechanism for the dynamic dissociation of the Numb·α-adaptin complex.

Keywords: 14-3-3 protein; Numb; adaptor protein; dual-site binding mode; dynamic assembly; membrane transport; phosphorylation; protein complex; protein-protein interaction; α-adaptin.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 14-3-3 Proteins / chemistry
  • 14-3-3 Proteins / metabolism*
  • Adaptor Protein Complex alpha Subunits / chemistry
  • Adaptor Protein Complex alpha Subunits / metabolism*
  • Animals
  • Binding Sites
  • Catalysis
  • Catalytic Domain
  • Crystallography, X-Ray
  • Endocytosis / physiology*
  • Membrane Proteins / chemistry*
  • Membrane Proteins / metabolism*
  • Mice
  • Models, Molecular
  • Nerve Tissue Proteins / chemistry*
  • Nerve Tissue Proteins / metabolism*
  • Phosphorylation
  • Protein Binding
  • Protein Conformation
  • Structure-Activity Relationship

Substances

  • 14-3-3 Proteins
  • Adaptor Protein Complex alpha Subunits
  • Membrane Proteins
  • Nerve Tissue Proteins
  • Numb protein, mouse

Associated data

  • PDB/4HKC