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Cell Stress and Chaperones

, Volume 20, Issue 1, pp 121–137 | Cite as

A role for the Parkinson’s disease protein DJ-1 as a chaperone and antioxidant in the anhydrobiotic nematode Panagrolaimus superbus

  • Bridget A. Culleton
  • Patrick Lall
  • Gemma K. Kinsella
  • Sean Doyle
  • John McCaffrey
  • David A. Fitzpatrick
  • Ann M. BurnellEmail author
Original Paper

Abstract

Mutations in the human DJ-1/PARK7 gene are associated with familial Parkinson’s disease. DJ-1 belongs to a large, functionally diverse family with homologues in all biological kingdoms. Several activities have been demonstrated for DJ-1: an antioxidant protein, a redox-regulated molecular chaperone and a modulator of multiple cellular signalling pathways. The majority of functional studies have focussed on human DJ-1 (hDJ-1), but studies on DJ-1 homologues in Drosophila melanogaster, Caenorhabditis elegans, Dugesia japonica and Escherichia coli also provide evidence of a role for DJ-1 as an antioxidant. Here, we show that dehydration is a potent inducer of a dj-1 gene in the anhydrobiotic nematode Panagrolaimus superbus. Our secondary structure and homology modelling analyses shows that recombinant DJ-1 protein from P. superbus (PsuDJ-1.1) is a well-folded protein, which is similar in structure to the hDJ-1. PsuDJ-1.1 is a heat stable protein; with T1/2 unfolding transition values of 76 and 70 °C obtained from both circular dichroism (CD) and Fourier transform infrared spectroscopy (FTIR) measurements respectively. We found that PsuDJ-1.1 is an efficient antioxidant that also functions as a ‘holdase’ molecular chaperone that can maintain its chaperone function in a reducing environment. In addition to its chaperone activity, PsuDJ-1.1 may also be an important non-enzymatic antioxidant, capable of providing protection to P. superbus from oxidative damage when the nematodes are in a desiccated, anhydrobiotic state.

Keywords

DJ-1 Chaperone Antioxidant Anhydrobiosis Homology modelling Molecular dynamics 

Abbreviations

BSA

Bovine serum albumin

CD

Circular dichroism

CRYAB

αB-crystallin

CS

Citrate synthase

DTT

Dithiothreitol

EST

Expressed sequence tag

FTIR

Fourier transform infrared spectroscopy

hDJ-1

Human DJ-1

HM

Homology model

MD

Molecular dynamics

MALDI-ToF MS

Matrix-assisted laser desorption/ionization time of flight mass spectrometry

MWCO

Molecular weight cut-off

Ni-NTA

Nickel nitrilotriacetic acid

PD

Parkinson’s disease

PsuDJ-1

P. superbus DJ-1

RMSD

Root mean square deviation

ROS

Reactive oxygen species.

Notes

Acknowledgments

This project was funded by Science Foundation Ireland (Projects 08/RFP/EOB1660 and 09/RFP/EOB2506). BAC was funded by an Irish Research Council EMBARK post-graduate fellowship. qPCR facilities were funded by Science Foundation Ireland (SFI/07/RFP/GEN/F571/EC07). The AKTA Purifier and MALDI-ToF MS were funded by the Irish Higher Education Authority and the Irish Health Research Board, respectively. The authors wish to acknowledge the DJEI/DES/SFI/HEA Irish Centre for High-End Computing (ICHEC) for the provision of computational facilities and support. The NAMD 2.10 simulation package was developed with NIH support by the Theoretical and Computational Biophysics Group in the Beckman Institute for Advanced Science and Technology at the University of Illinois at Urbana-Champaign.

Supplementary material

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Supplementary Fig. 1 (DOC 124 kb)
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Supplementary Fig. 4 (DOC 7342 kb)
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Supplementary Table 1 (DOC 51 kb)
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Supplementary Table 2 (XLS 47 kb)
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Supplementary Table 5 (DOC 35 kb)
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ESM 1 (DOC 1279 kb)

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Copyright information

© Cell Stress Society International 2014

Authors and Affiliations

  • Bridget A. Culleton
    • 1
    • 3
  • Patrick Lall
    • 2
  • Gemma K. Kinsella
    • 1
  • Sean Doyle
    • 1
  • John McCaffrey
    • 2
  • David A. Fitzpatrick
    • 1
  • Ann M. Burnell
    • 1
    Email author
  1. 1.Department of BiologyNational University of Ireland MaynoothMaynoothIreland
  2. 2.Department of ChemistryNational University of Ireland MaynoothMaynoothIreland
  3. 3.Megazyme International IrelandBrayIreland

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