Proteomic Analysis of the Ubiquitin Landscape in the Drosophila Embryonic Nervous System and the Adult Photoreceptor Cells

PLoS One. 2015 Oct 13;10(10):e0139083. doi: 10.1371/journal.pone.0139083. eCollection 2015.

Abstract

Background: Ubiquitination is known to regulate physiological neuronal functions as well as to be involved in a number of neuronal diseases. Several ubiquitin proteomic approaches have been developed during the last decade but, as they have been mostly applied to non-neuronal cell culture, very little is yet known about neuronal ubiquitination pathways in vivo.

Methodology/principal findings: Using an in vivo biotinylation strategy we have isolated and identified the ubiquitinated proteome in neurons both for the developing embryonic brain and for the adult eye of Drosophila melanogaster. Bioinformatic comparison of both datasets indicates a significant difference on the ubiquitin substrates, which logically correlates with the processes that are most active at each of the developmental stages. Detection within the isolated material of two ubiquitin E3 ligases, Parkin and Ube3a, indicates their ubiquitinating activity on the studied tissues. Further identification of the proteins that do accumulate upon interference with the proteasomal degradative pathway provides an indication of the proteins that are targeted for clearance in neurons. Last, we report the proof-of-principle validation of two lysine residues required for nSyb ubiquitination.

Conclusions/significance: These data cast light on the differential and common ubiquitination pathways between the embryonic and adult neurons, and hence will contribute to the understanding of the mechanisms by which neuronal function is regulated. The in vivo biotinylation methodology described here complements other approaches for ubiquitome study and offers unique advantages, and is poised to provide further insight into disease mechanisms related to the ubiquitin proteasome system.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Biotinylation
  • Blotting, Western
  • Cell Line
  • Drosophila Proteins / chemistry
  • Drosophila Proteins / metabolism
  • Drosophila melanogaster / cytology
  • Drosophila melanogaster / embryology*
  • Drosophila melanogaster / metabolism*
  • Embryo, Nonmammalian / metabolism*
  • Green Fluorescent Proteins / metabolism
  • Mass Spectrometry
  • Molecular Sequence Data
  • Nervous System / embryology*
  • Nervous System / metabolism
  • Neurons / metabolism
  • Photoreceptor Cells, Invertebrate / cytology
  • Photoreceptor Cells, Invertebrate / metabolism*
  • Proteasome Endopeptidase Complex / metabolism
  • Proteomics / methods*
  • Reproducibility of Results
  • Ubiquitin / metabolism*
  • Ubiquitination

Substances

  • Drosophila Proteins
  • Ubiquitin
  • Green Fluorescent Proteins
  • Proteasome Endopeptidase Complex

Grants and funding

UM was supported by the Basque Government research grant (PI2011-24), the Asociación Síndrome de Angelman, and the March of Dimes Basil O´Connor Award (5-FY12-16). JR was supported by the CIC bioGUNE PhD fellowship. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.