Drosophila models of pathogenic copy-number variant genes show global and non-neuronal defects during development

PLoS Genet. 2020 Jun 24;16(6):e1008792. doi: 10.1371/journal.pgen.1008792. eCollection 2020 Jun.

Abstract

While rare pathogenic copy-number variants (CNVs) are associated with both neuronal and non-neuronal phenotypes, functional studies evaluating these regions have focused on the molecular basis of neuronal defects. We report a systematic functional analysis of non-neuronal defects for homologs of 59 genes within ten pathogenic CNVs and 20 neurodevelopmental genes in Drosophila melanogaster. Using wing-specific knockdown of 136 RNA interference lines, we identified qualitative and quantitative phenotypes in 72/79 homologs, including 21 lines with severe wing defects and six lines with lethality. In fact, we found that 10/31 homologs of CNV genes also showed complete or partial lethality at larval or pupal stages with ubiquitous knockdown. Comparisons between eye and wing-specific knockdown of 37/45 homologs showed both neuronal and non-neuronal defects, but with no correlation in the severity of defects. We further observed disruptions in cell proliferation and apoptosis in larval wing discs for 23/27 homologs, and altered Wnt, Hedgehog and Notch signaling for 9/14 homologs, including AATF/Aatf, PPP4C/Pp4-19C, and KIF11/Klp61F. These findings were further supported by tissue-specific differences in expression patterns of human CNV genes, as well as connectivity of CNV genes to signaling pathway genes in brain, heart and kidney-specific networks. Our findings suggest that multiple genes within each CNV differentially affect both global and tissue-specific developmental processes within conserved pathways, and that their roles are not restricted to neuronal functions.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Compound Eye, Arthropod / embryology
  • Compound Eye, Arthropod / metabolism
  • DNA Copy Number Variations*
  • Drosophila Proteins / genetics*
  • Drosophila Proteins / metabolism
  • Drosophila melanogaster
  • Gene Expression Regulation, Developmental*
  • Hedgehog Proteins / genetics
  • Hedgehog Proteins / metabolism
  • Neurodevelopmental Disorders / genetics*
  • Neurons / cytology
  • Neurons / metabolism
  • Organ Specificity
  • Receptors, Notch / genetics
  • Receptors, Notch / metabolism
  • Signal Transduction
  • Wings, Animal / embryology
  • Wings, Animal / metabolism
  • Wnt Proteins / genetics
  • Wnt Proteins / metabolism

Substances

  • Drosophila Proteins
  • Hedgehog Proteins
  • Receptors, Notch
  • Wnt Proteins