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

Cell Stress and Chaperones

Volumn 20, Issue 1, 2015, Pages 121-137

  Culleton, Bridget A ^a,b   Lall, Patrick ^a   Kinsella, Gemma K ^a   Doyle, Sean ^a   McCaffrey, John ^a   Fitzpatrick, David A ^a   Burnell, Ann M ^a  

^a NATIONAL UNIVERSITY OF IRELAND   (Ireland)

^b Megazyme International Ireland Ltd   (Ireland)

Author keywords

Anhydrobiosis; Antioxidant; Chaperone; DJ 1; Homology modelling; Molecular dynamics

Indexed keywords

PANAGROLAIMUS SUPERBUS;

ANTIOXIDANT; HELMINTH PROTEIN; RECOMBINANT PROTEIN; SIGNAL PEPTIDE;

AMINO ACID SEQUENCE; ANIMAL; BIOSYNTHESIS; CHEMISTRY; CIRCULAR DICHROISM; CLASSIFICATION; GENE EXPRESSION; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MOLECULAR DYNAMICS; MOLECULAR GENETICS; OXIDATIVE STRESS; PHYLOGENY; PHYSIOLOGY; PROTEIN DENATURATION; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; RHABDITIDA; SEQUENCE ALIGNMENT; TRANSITION TEMPERATURE;

AMINO ACID SEQUENCE; ANIMALS; ANTIOXIDANTS; CIRCULAR DICHROISM; GENE EXPRESSION; HELMINTH PROTEINS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; OXIDATIVE STRESS; PHYLOGENY; PROTEIN DENATURATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; RHABDITIDA; SEQUENCE ALIGNMENT; TRANSITION TEMPERATURE;

EID: 84914684649     PISSN: 13558145     EISSN: 14661268     Source Type: Journal    
DOI: 10.1007/s12192-014-0531-6     Document Type: Article

References (98)

1. Alpert P (2006) Constraints of tolerance: why are desiccation-tolerant organisms so small or rare? J Exp Biol 209:1575–1584
2. Andres-Mateos E et al (2007) DJ-1 gene deletion reveals that DJ-1 is an atypical peroxiredoxin-like peroxidase. Proc Natl Acad Sci U S A 104:14807–14812
3. Aroian R, Carta L, Kaloshian I, Sternberg P (1993) A free-living Panagrolaimus sp. from Armenia can survive anhydrobiosis for 8.7 years. J Nematol 25:500–502
4. Bandyopadhyay S, Cookson MR (2004) Evolutionary and functional relationships within the DJ1 superfamily. BMC Evol Biol 4:9
5. Barrett J (1991) Anhydrobiotic nematodes. In: Evans K (ed) Agricultural zoology reviews Intercept Ltd. Andover, England, pp 161–176
6. Betts MJ, Russell RR (2003) Amino acid properties and consequeces of substitutions. In: Barnes MR, Gray, I.C. (ed) Bioinformatics for Geneticists, John Wiley and Sons, pp 289–316
7. Bladursson S, Ingadóttir Á (eds) (2007) Nomination of Surtsey for the UNESCO world heritage list. Icelandic Institute of Natural History, Reykjavík
8. Bonifati V et al (2003) Mutations in the DJ-1 gene associated with autosomal recessive early-onset parkinsonism. Science 299:256–259
9. Boström S (1988) Descriptions and morphological variability of three populations of Panagrolaimus Fuchs, 1930 (Nematoda, Panagrolaimidae). Nematologica 34:144–155
10. Bowie JU, Lüthy R, Eisenberg D (1991) A method to identify protein sequences that fold into a known three-dimensional structure. Science 253:164–170
11. Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77:71–94
12. Burnell AM, Tunnacliffe A (2011) Gene induction and desiccation stress in nematodes. In: Perry RN, Wharton DA (eds) Molecular and physiological basis of nematode survival. CAB International, Wallingford, Oxfordshire, pp 125–156
13. Canet-Aviles RM et al (2004) The Parkinson’s disease protein DJ-1 is neuroprotective due to cysteine-sulfinic acid-driven mitochondrial localization. Proc Natl Acad Sci U S A 101:9103–9108
14. Chen T, Villeneuve TS, Garant KA, Amons R, MacRae TH (2007) Functional characterization of artemin, a ferritin homolog synthesized in Artemia embryos during encystment and diapause. FEBS J 274:1093–1101
15. Chen J, Li L, Chin L-S (2010) Parkinson disease protein DJ-1 converts from a zymogen to a protease by carboxyl-terminal cleavage. Hum Mol Genet 19:2395–2408
16. Clark MS et al (2012) Long-term survival of hydrated resting eggs from Brachionus plicatilis. PLoS One 7:e29365
17. Clegg JS (1967) Metabolic studies of cryptobiosis in encysted embryos of Artemia salina. Comp Biochem Physiol 20(20):801–809
18. Clegg JS (2001) Cryptobiosis—a peculiar state of biological organization. Comp Biochem Physiol B Biochem Mol Biol 128:613–624
19. Clements CM, McNally RS, Conti BJ, Mak TW, Ting JP (2006) DJ-1, a cancer- and Parkinson’s disease-associated protein, stabilizes the antioxidant transcriptional master regulator Nrf2. Proc Natl Acad Sci U S A 103:15091–15096
20. Colovos C, Yeates T (1993) Verification of protein structures: patterns of nonbonded atomic interactions. Protein Sci 2:1511–1519
21. Cornette R, Kikawada T (2011) The induction of anhydrobiosis in the sleeping chironomid: current status of our knowledge. IUBMB Life 63:419–429
22. Crowe JH, Hoekstra FA, Crowe LM (1992) Anhydrobiosis. Annu Rev Physiol 54:579–599
23. Darden T, York D, Pedersen L (1993) Particle mesh Ewald: An N log(N) method for Ewald sums in large systems. J Chem Phys 98:10089–10092
24. Davies MJ, Gilbert BC, Haywood RM (1993) Radical-induced damage to bovine serum albumin: role of the cysteine residue. Free Radic Res Commun 18:353–367
25. Darden T, York D and Pedersen L (1993) Particle mesh Ewald: An Nlog(N) method for Ewald sums in large systems. J Chem Phys 98:10089–10092
26. DeLano WL (2002) The PyMOL Molecular Graphics System. In. DeLano Scientific LLC, San Carlos, CA, USA. http://www.pymol.org
27. Du XL et al (2000) Crystal structure of an intracellular protease from Pyrococcus horikoshii at 2-angstrom resolution. Proc Natl Acad Sci U S A 97:14079–14084
28. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucl Acids Res 32:1792–1797
29. Edgecombe GD et al (2011) Higher-level metazoan relationships: recent progress and remaining questions. Org Divers Evol 11:151–172
30. Erkut C, Vasilj A, Boland S, Habermann B, Shevchenko A, Kurzchalia TV (2013) Molecular strategies of the Caenorhabditis elegans dauer larva to survive extreme desiccation. PLoS One 8:e82473
31. Farrant JM, Moore JP (2011) Programming desiccation-tolerance: from plants to seeds to resurrection plants. Curr Opin Plant Biol 14:340–345
32. Franca MB, Panek AD, Eleutherio ECA (2007) Oxidative stress and its effects during dehydration. Comp Biochem Physiol A Mol Integr Physiol 146:621–631
33. Feller S. E, Zhang Y. H, Pastor R. W, Brooks B. R (1995) Constant pressure molecular dynamics simulation: The Langevin piston method. J Chem Phys 103:4613–4621
34. Go Y-M, Jones DP (2008) Redox compartmentalization in eukaryotic cells. Biochim Biophy Acta 1780:1273–1290
35. Goyal K, Walton LJ, Tunnacliffe A (2005) LEA proteins prevent protein aggregation due to water stress. Biochem J 388:151–157
36. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704
37. Halio S, Blumentals I, Short S, Merrill B, Kelly R (1996) Sequence, expression in Escherichia coli, and analysis of the gene encoding a novel intracellular protease (PfpI) from the hyperthermophilic archaeon Pyrococcus furiosus. J Bacteriol 178:2605–2612
38. Hand SC, Menze MA, Toner M, Boswell L, Moore D (2011) LEA proteins during water stress: not just for plants anymore. Annu Rev Physiol 73:115–134
39. Honbou K et al (2003) The crystal structure of DJ-1, a protein related to male fertility and Parkinson’s disease. J Biol Chem 278:31380–31384
40. Huai Q et al (2003) Crystal structure of DJ-1/RS and implication on familial Parkinson’s disease. FEBS Lett 549:171–175
41. Humphrey W, Dalke A, Schulten K (1996) VMD: visual molecular dynamics. J Mol Graph 14(33–38):27–38
42. Jorgensen WL, Chandrasekhar J, Buckner JK, Madura JD (1986) Computer simulations of organic reactions in solution. Ann N Y Acad Sci 482:198–209
43. Keane TM, Creevey CJ, Pentony MM, Naughton TJ, McLnerney JO (2006) Assessment of methods for amino acid matrix selection and their use on empirical data shows that ad hoc assumptions for choice of matrix are not justified. BMC Evol Biol 6:29
44. Kiefhaber T, Rudolph R, Kohler HH, Buchner J (1991) Protein aggregation in vitro and in vivo—a quantitative model of the kinetic competition between folding and aggregation. Nat Biotechnol 9:825–829
45. Kim S-J, Park Y-J, Hwang I-Y, Youdim MBH, Park K-S, Oh YJ (2012) Nuclear translocation of DJ-1 during oxidative stress-induced neuronal cell death. Free Radic Biol Med 53:936–950
46. Kranner I, Birtic S (2005) A modulating role for antioxidants in desiccation tolerance. Integr Comp Biol 45:734–740
47. Kranner I, Beckett RP, Wornik S, Zorn M, Pfeifhofer HW (2002) Revival of a resurrection plant correlates with its antioxidant status. Plant J 31:13–24
48. Kthiri F et al (2010) Protein aggregation in a mutant deficient in YajL, the bacterial homolog of the parkinsonism-associated protein DJ-1. J Biol Chem 285:10328–10336
49. Kulig M, Ecroyd H (2012) The small heat-shock protein alpha B-crystallin uses different mechanisms of chaperone action to prevent the amorphous versus fibrillar aggregation of alpha-lactalbumin. Biochem J 448:343–352
50. Kwon S, Jung Y, Lim D (2008) Proteomic analysis of heat-stable proteins in Escherichia coli. BMB Rep 41:108–111
51. Lakshminarasimhan M, Madzelan P, Nan R, Milkovic NM, Wilson MA (2010) Evolution of new enzymatic function by structural modulation of cysteine reactivity in Pseudomonas fluorescens isocyanide hydratase. J Biol Chem 285:29651–29661
52. Lartillot N, Philippe H (2008) Improvement of molecular phylogenetic inference and the phylogeny of Bilateria. Phil Trans R Soc B 363:1463–1472
53. Laskowski R, Rullmannn J, MacArthur M, Kaptein R, Thornton J (1996) AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J Biomol NMR 8:477–486
54. Le H-T et al (2012) YajL, prokaryotic homolog of parkinsonism-associated protein DJ-1, functions as a covalent chaperone for thiol proteome. J Biol Chem 287:5861–5870
55. Leber TM, Balkwill FR (1997) Zymography: a single-step staining method for quantitation of proteolytic activity on substrate gels. Anal Biochem 249:24–28
56. Lee SJ et al (2003) Crystal structures of human DJ-1 and Escherichia coli Hsp31, which share an evolutionarily conserved domain. J Biol Chem 278:44552–44559
57. Lin J, Prahlad J, Wilson MA (2012) Conservation of oxidative protein stabilization in an insect homologue of parkinsonism-associated protein DJ-1. Biochemistry 51:3799–3807
58. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-[Delta] [Delta] CT method. Methods 25:402–408
59. Lucas JI, Marin I (2007) A new evolutionary paradigm for the Parkinson disease gene DJ-1. Mol Biol Evol 24:551–561
60. Mackerell AD (2004) Empirical force fields for biological macromolecules: overview and issues. J Comput Chem 25:1584–1604
61. MacKerell AD et al (1998) All-atom empirical potential for molecular modeling and dynamics studies of proteins. J Phys Chem B 102:3586–3616
62. Malgieri G, Eliezer D (2008) Structural effects of Parkinson’s disease linked DJ-1 mutations. Protein Sci 17:855–868
63. Moore DJ, West AB, Dawson VL, Dawson TM (2005) Molecular pathophysiology of Parkinson’s disease. Annu Rev Neurosci 28:57–87
64. Nagakubo D et al (1997) DJ-1, a novel oncogene which transforms mouse NIH3T3 cells in cooperation with ras. Biochem Biophys Res Commun 231:509–513
65. Nosé S. A, (1984) unified formulation of the constant temperature molecular-dynamics methods. J Chem Phys 81:511–519
66. Pace CN, Scholtz JM (1998) A helix propensity scale based on experimental studies of peptides and proteins. Biophys J 75:422–427
67. Pereira EJ, Panek AD, Eleutherio ECA (2003) Protection against oxidation during dehydration of yeast. Cell Stress Chaperon 8:120–124
68. Pfaffl MW (2006) Relative quantification. In: Dorak T (ed) Real-time PCR. Taylor and Francis Group, New York, pp 63–82
69. Phillips JC et al (2005) Scalable molecular dynamics with NAMD. J Comput Chem 26:1781–1802
70. Prestrelski SJ, Tedeschi N, Arakawa T, Carpenter JF (1993) Dehydration-induced conformational transitions in proteins and their inhibition by stabilizers. Biophys J 65:661–671
71. Quigley PM, Korotkov K, Baneyx F, Hol WGJ (2003) The 1.6-angstrom crystal structure of the class of chaperones represented by Escherichia coli Hsp31 reveals a putative catalytic triad. Proc Natl Acad Sci U S A 100:3137–3142
72. Reardon W et al (2010) Expression profiling and cross-species RNA interference (RNAi) of desiccation-induced transcripts in the anhydrobiotic nematode Aphelenchus avenae. BMC Mol Biol 11:6
73. Reddy GB, Kumar PA, Kumar MS (2006) Chaperone-like activity and hydrophobicity of alpha-crystallin. IUBMB Life 58:632–641
74. Rizzo AM et al (2010) Antioxidant defences in hydrated and desiccated states of the tardigrade Paramacrobiotus richtersi. Comp Biochem Physiol B Biochem Mol Biol 156:115–121
75. 2 release from human granulocytes during phagocytosis. J Clin Invest 60:1266–1279
76. Sali A, Blundell T (1993) Comparative protein modelling by satisfaction of spatial restraints. J Mol Biol 234:779–815
77. Sali A, Overington J (1994) Derivation of rules for comparative protein modeling from a database of protein structure alignments. Protein Sci 3:1582–1596
78. Sastry MSR, Korotkov K, Brodsky Y, Baneyx F (2002) Hsp31, the Escherichia coli yedU gene product, is a molecular chaperone whose activity is inhibited by ATP at high temperatures. J Biol Chem 277:46026–46034
79. Sevinc M, Switala J, Bravo J, Fita I, Loewen P (1998) Truncation and heme pocket mutations reduce production of functional catalase HPII in Escherichia coli. Protein Eng 11:549–555
80. Sharma SK, Christen P, Goloubinoff P (2009) Disaggregating chaperones: an unfolding story. Curr Protein Pept Sci 10:432–446
81. Shendelman S, Jonason A, Martinat C, Leete T, Abeliovich A (2004) DJ-1 is a redox-dependent molecular chaperone that inhibits alpha-synuclein aggregate formation. PLoS Biol 2:1764–1773
82. Shevchenko A, Tomas H, Havlis J, Olsen JV, Mann M (2007) In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat Protoc 1:2856–2860
83. Shimodaira H (2002) An approximately unbiased test of phylogenetic tree selection. Syst Biol 51:492–508
84. Stefanatos R et al (2012) dj-1β regulates oxidative stress, insulin-like signaling and development in Drosophila melanogaster. Cell Cycle 11:3876–3886
85. Taira T, Saito Y, Niki T, Iguchi-Ariga SMM, Takahashi K, Ariga H (2004) DJ-1 has a role in antioxidative stress to prevent cell death. EMBO Rep 5:213–218
86. Tao X, Tong L (2003) Crystal structure of human DJ-1, a protein associated with early onset Parkinson’s disease. J Biol Chem 278:31372–31379
87. Thomas KJ et al (2011) DJ-1 acts in parallel to the PINK1/parkin pathway to control mitochondrial function and autophagy. Hum Mol Genet 20:40–50
88. Tsushima J et al (2012) Protective effect of planarian DJ-1 against 6-hydroxydopamine-induced neurotoxicity. Neurosci Res 74:277–283
89. Tyson T et al (2012) A molecular analysis of desiccation tolerance mechanisms in the anhydrobiotic nematode Panagrolaimus superbus using expressed sequenced tags. BMC Res Notes 5:68
90. van der Brug MP et al (2008) RNA binding activity of the recessive parkinsonism protein DJ-1 supports involvement in multiple cellular pathways. Proc Natl Acad Sci U S A 105:10244–10249
91. Waak J et al (2009) Oxidizable residues mediating protein stability and cytoprotective interaction of DJ-1 with apoptosis signal-regulating kinase 1. J Biol Chem 284:14245–14257
92. Warner AH, Brunet RT, MacRae TH, Clegg JS (2004) Artemin is an RNA-binding protein with high thermal stability and potential RNA chaperone activity. Arch Biochem Biophys 424:189–200
93. Whitmore L, Wallace BA (2004) DICHROWEB, an online server for protein secondary structure analyses from circular dichroism spectroscopic data. Nucl Acids Res 32:W668–673
94. Wilson MA (2011) The role of cysteine oxidation in DJ-1 function and dysfunction. Antioxid Redox Signal 15:111–122
95. Wilson MA, Collins JL, Hod Y, Ringe D, Petsko GA (2003) The 1.1-angstrom resolution crystal structure of DJ-1, the protein mutated in autosomal recessive early onset Parkinson’s disease. Proc Natl Acad Sci U S A 100:9256–9261
96. Wilson MA, Ringe D, Petsko GA (2005) The atomic resolution crystal structure of the YajL (ThiJ) protein from Escherichia coli: a close prokaryotic homologue of the Parkinsonism-associated protein DJ-1. J Mol Biol 353:678–691
97. Winston PW, Bates PS (1960) Saturated salt solutions for the control of humidity in biological research. Ecology 41:232–237
98. Zhou WB, Zhu M, Wilson MA, Petsko GA, Fink AL (2006) The oxidation state of DJ-1 regulates its chaperone activity toward α-synuclein. J Mol Biol 356:1036–1048