Genome-wide CRISPR screen for PARKIN regulators reveals transcriptional repression as a determinant of mitophagy

Proc Natl Acad Sci U S A. 2018 Jan 9;115(2):E180-E189. doi: 10.1073/pnas.1711023115. Epub 2017 Dec 21.

Abstract

PARKIN, an E3 ligase mutated in familial Parkinson's disease, promotes mitophagy by ubiquitinating mitochondrial proteins for efficient engagement of the autophagy machinery. Specifically, PARKIN-synthesized ubiquitin chains represent targets for the PINK1 kinase generating phosphoS65-ubiquitin (pUb), which constitutes the mitophagy signal. Physiological regulation of PARKIN abundance, however, and the impact on pUb accumulation are poorly understood. Using cells designed to discover physiological regulators of PARKIN abundance, we performed a pooled genome-wide CRISPR/Cas9 knockout screen. Testing identified genes individually resulted in a list of 53 positive and negative regulators. A transcriptional repressor network including THAP11 was identified and negatively regulates endogenous PARKIN abundance. RNAseq analysis revealed the PARKIN-encoding locus as a prime THAP11 target, and THAP11 CRISPR knockout in multiple cell types enhanced pUb accumulation. Thus, our work demonstrates the critical role of PARKIN abundance, identifies regulating genes, and reveals a link between transcriptional repression and mitophagy, which is also apparent in human induced pluripotent stem cell-derived neurons, a disease-relevant cell type.

Keywords: PARKIN; THAP11; genome-wide screen; mitophagy; phosphoubiquitin.

MeSH terms

  • CRISPR-Cas Systems*
  • Cell Line, Tumor
  • Cells, Cultured
  • Gene Expression Regulation*
  • Genome, Human / genetics*
  • HCT116 Cells
  • HEK293 Cells
  • Humans
  • Induced Pluripotent Stem Cells / metabolism
  • Infant, Newborn
  • Mitophagy / genetics*
  • Neurons / metabolism
  • Phosphorylation
  • Protein Kinases / genetics
  • Protein Kinases / metabolism
  • Repressor Proteins / genetics*
  • Repressor Proteins / metabolism
  • Ubiquitin / metabolism
  • Ubiquitin-Protein Ligases / genetics*
  • Ubiquitin-Protein Ligases / metabolism

Substances

  • Repressor Proteins
  • THAP11 protein, human
  • Ubiquitin
  • Ubiquitin-Protein Ligases
  • parkin protein
  • Protein Kinases
  • PTEN-induced putative kinase