cindr, the Drosophila Homolog of the CD2AP Alzheimer's Disease Risk Gene, Is Required for Synaptic Transmission and Proteostasis

Cell Rep. 2019 Aug 13;28(7):1799-1813.e5. doi: 10.1016/j.celrep.2019.07.041.

Abstract

The Alzheimer's disease (AD) susceptibility gene, CD2-associated protein (CD2AP), encodes an actin binding adaptor protein, but its function in the nervous system is largely unknown. Loss of the Drosophila ortholog cindr enhances neurotoxicity of human Tau, which forms neurofibrillary tangle pathology in AD. We show that Cindr is expressed in neurons and present at synaptic terminals. cindr mutants show impairments in synapse maturation and both synaptic vesicle recycling and release. Cindr associates and genetically interacts with 14-3-3ζ, regulates the ubiquitin-proteasome system, and affects turnover of Synapsin and the plasma membrane calcium ATPase (PMCA). Loss of cindr elevates PMCA levels and reduces cytosolic calcium. Studies of Cd2ap null mice support a conserved role in synaptic proteostasis, and CD2AP protein levels are inversely related to Synapsin abundance in human postmortem brains. Our results reveal CD2AP neuronal requirements with relevance to AD susceptibility, including for proteostasis, calcium handling, and synaptic structure and function.

Keywords: 14-3-3; GWAS; PMCA; Tau; endocytosis; exocytosis; neurofibrillary tangles; neuromascular junction; synapsin; ubiquitin-proteasome system.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 14-3-3 Proteins / genetics
  • 14-3-3 Proteins / metabolism*
  • Adaptor Proteins, Signal Transducing / genetics
  • Adaptor Proteins, Signal Transducing / metabolism*
  • Alzheimer Disease*
  • Animals
  • Cytoskeletal Proteins / genetics
  • Cytoskeletal Proteins / metabolism*
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism*
  • Drosophila melanogaster / genetics
  • Drosophila melanogaster / growth & development
  • Drosophila melanogaster / metabolism*
  • Female
  • Humans
  • Male
  • Mice
  • Microfilament Proteins / genetics
  • Microfilament Proteins / metabolism*
  • Neurons / cytology
  • Neurons / metabolism*
  • Proteome / analysis
  • Proteome / metabolism
  • Proteostasis*
  • Synaptic Transmission

Substances

  • 14-3-3 Proteins
  • Adaptor Proteins, Signal Transducing
  • CD2-associated protein
  • Cindr protein, Drosophila
  • Cytoskeletal Proteins
  • Drosophila Proteins
  • Microfilament Proteins
  • Proteome