Identification of Heat Shock Protein 60 as a Regulator of Neutral Sphingomyelinase 2 and Its Role in Dopamine Uptake

PLoS One. 2013 Jun 19;8(6):e67216. doi: 10.1371/journal.pone.0067216. Print 2013.

Abstract

Activation of sphingomyelinase (SMase) by extracellular stimuli is the major pathway for cellular production of ceramide, a bioactive lipid mediator acting through sphingomyelin (SM) hydrolysis. Previously, we reported the existence of six forms of neutral pH-optimum and Mg(2+)-dependent SMase (N-SMase) in the membrane fractions of bovine brain. Here, we focus on N-SMase ε from salt-extracted membranes. After extensive purification by 12,780-fold with a yield of 1.3%, this enzyme was eventually characterized as N-SMase2. The major single band of 60-kDa molecular mass in the active fractions of the final purification step was identified as heat shock protein 60 (Hsp60) by matrix-assisted laser desorption/ionization time-of-flight mass spectrometric analysis. Proximity ligation assay and immunoprecipitation study showed that Hsp60 interacted with N-SMase2, prompting us to examine the effect of Hsp60 on N-SMase2 and ceramide production. Interestingly, Hsp60 siRNA treatment significantly increased the protein level of N-SMase2 in N-SMase2-overexpressed HEK293 cells. Furthermore, transfection of Hsp60 siRNA into PC12 cells effectively increased both N-SMase activity and ceramide production and increased dopamine re-uptake with paralleled increase. Taken together, these results show that Hsp60 may serve as a negative regulator in N-SMase2-induced dopamine re-uptake by decreasing the protein level of N-SMase2.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cattle
  • Chaperonin 60 / physiology*
  • Dopamine / metabolism*
  • HEK293 Cells
  • Humans
  • PC12 Cells
  • Rats
  • Rats, Sprague-Dawley
  • Sphingomyelin Phosphodiesterase / metabolism*

Substances

  • Chaperonin 60
  • Sphingomyelin Phosphodiesterase
  • Dopamine

Grants and funding

This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korea government (MEST) (20120006542). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.