Transient neuroprotection by SRY upregulation in dopamine cells following injury in males

Endocrinology. 2014 Jul;155(7):2602-12. doi: 10.1210/en.2013-2158. Epub 2014 Apr 7.

Abstract

Emerging evidence suggest sex-specific regulation of dopamine neurons may underlie susceptibility of males to disorders such as Parkinson's disease (PD). In healthy male dopamine neurons, the Y-chromosome gene product, the sex-determining region on the Y chromosome (SRY) modulates dopamine biosynthesis and motor function. We investigated the regulation and function of SRY in a model of dopamine cell injury. Treatment with the dopaminergic toxin, 6-hydroxydopamine (6-OHDA), significantly elevated SRY mRNA expression (9-fold) in human male dopamine M17 cells. SRY up-regulation occurred via the p-quinone pathway, associated with a 3.5-fold increase in expression of GADD45γ, a DNA damage inducible factor gene and known SRY regulator. In turn, a signaling cascade involving GADD45γ/p38-MAPK/GATA activated the SRY promoter. Knockdown of SRY mRNA in 6-OHDA-treated M17 cells was deleterious, increasing levels of reactive oxygen species (ROS), pro-apoptotic marker PUMA mRNA, and cell injury (+25%, +32% and +34%, respectively). Conversely, ectopic over-expression of SRY in 6-OHDA-treated female SH-SY5Y cells was protective, decreasing ROS, PUMA, and cell injury (-40%, -46%, and -30%, respectively). However, the 6-OHDA-induced increase in SRY expression was diminished with higher concentrations of toxins or with chronic exposure to 6-OHDA. We conclude that SRY upregulation after dopamine cell injury is initially a protective response in males, but diminishes with gradual loss in dopamine cells. We speculate that dysregulation of SRY may contribute the susceptibility of males to PD.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis Regulatory Proteins / genetics
  • Apoptosis Regulatory Proteins / metabolism
  • Benzoquinones / metabolism
  • Blotting, Western
  • Cell Line, Tumor
  • Cell Survival / drug effects
  • Dopamine / metabolism*
  • Dopaminergic Neurons / drug effects
  • Dopaminergic Neurons / metabolism*
  • GADD45 Proteins
  • GATA Transcription Factors / metabolism
  • Gene Expression Regulation, Neoplastic / drug effects
  • Humans
  • Hydrogen Peroxide / pharmacology
  • Intracellular Signaling Peptides and Proteins / genetics
  • Intracellular Signaling Peptides and Proteins / metabolism
  • Male
  • Oxidopamine / pharmacology
  • PC12 Cells
  • Promoter Regions, Genetic / genetics
  • Proto-Oncogene Proteins / genetics
  • Proto-Oncogene Proteins / metabolism
  • RNA Interference
  • Rats
  • Reactive Oxygen Species / metabolism
  • Reverse Transcriptase Polymerase Chain Reaction
  • Sex-Determining Region Y Protein / genetics*
  • Sex-Determining Region Y Protein / metabolism
  • Signal Transduction / drug effects
  • Up-Regulation / drug effects
  • Up-Regulation / genetics*
  • p38 Mitogen-Activated Protein Kinases / metabolism

Substances

  • Apoptosis Regulatory Proteins
  • BBC3 protein, human
  • Benzoquinones
  • GATA Transcription Factors
  • Intracellular Signaling Peptides and Proteins
  • Proto-Oncogene Proteins
  • Reactive Oxygen Species
  • Sex-Determining Region Y Protein
  • quinone
  • Oxidopamine
  • Hydrogen Peroxide
  • p38 Mitogen-Activated Protein Kinases
  • Dopamine