Comprehensive structural characterization of the human AAA+ disaggregase CLPB in the apo- and substrate-bound states reveals a unique mode of action driven by oligomerization

PLoS Biol. 2023 Feb 6;21(2):e3001987. doi: 10.1371/journal.pbio.3001987. eCollection 2023 Feb.

Abstract

The human AAA+ ATPase CLPB (SKD3) is a protein disaggregase in the mitochondrial intermembrane space (IMS) and functions to promote the solubilization of various mitochondrial proteins. Loss-of-function CLPB mutations are associated with a few human diseases with neutropenia and neurological disorders. Unlike canonical AAA+ proteins, CLPB contains a unique ankyrin repeat domain (ANK) at its N-terminus. How CLPB functions as a disaggregase and the role of its ANK domain are currently unclear. Herein, we report a comprehensive structural characterization of human CLPB in both the apo- and substrate-bound states. CLPB assembles into homo-tetradecamers in apo-state and is remodeled into homo-dodecamers upon substrate binding. Conserved pore-loops (PLs) on the ATPase domains form a spiral staircase to grip and translocate the substrate in a step-size of 2 amino acid residues. The ANK domain is not only responsible for maintaining the higher-order assembly but also essential for the disaggregase activity. Interactome analysis suggests that the ANK domain may directly interact with a variety of mitochondrial substrates. These results reveal unique properties of CLPB as a general disaggregase in mitochondria and highlight its potential as a target for the treatment of various mitochondria-related diseases.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Endopeptidase Clp / chemistry
  • Endopeptidase Clp / genetics
  • Endopeptidase Clp / metabolism
  • Escherichia coli Proteins* / metabolism
  • Heat-Shock Proteins* / genetics
  • Humans
  • Mutation
  • Protein Domains
  • Substrate Specificity

Substances

  • Endopeptidase Clp
  • Escherichia coli Proteins
  • Heat-Shock Proteins
  • CLPB protein, human

Grants and funding

The work was supported by the National Natural Science Foundation of China (https://www.nsfc.gov.cn/) (32230051 to N.G., 31922036 to N.L.), the National Key Research and Development Program of China (https://service.most.gov.cn/) (2019YFA0508904 to N.G.), and the Qidong-SLS Innovation Fund to N.G. This work is also partially supported by Changping Laboratory. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.