Conservation of oxidative protein stabilization in an insect homologue of parkinsonism-associated protein DJ-1

Biochemistry

Volumn 51, Issue 18, 2012, Pages 3799-3807

  Lin, Jiusheng ^a   Prahlad, Janani ^a   Wilson, Mark A ^a  

^a UNIVERSITY OF NEBRASKA LINCOLN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE RESIDUES; DISEASE-ASSOCIATED PROTEINS; DROSOPHILA MELANOGASTER; HUMAN PROTEINS; IN-VIVO; MITOCHONDRIAL DAMAGE; MODEL SYSTEM; OXIDATIVE MODIFICATION; POTENTIAL MECHANISM; PROTEIN FUNCTIONS; PROTEIN STABILIZATION; REACTIVE CYSTEINE; THERMAL STABILIZATION;

CHEMICAL COMPOUNDS; OXIDATION; PROTEINS; STABILIZATION; SULFUR DIOXIDE;

AMINO ACIDS;

CYSTEINE; DJ 1 PROTEIN; TYROSINE;

AMINO ACID SUBSTITUTION; ARTICLE; CATALYSIS; CELL PROTECTION; CRYSTAL STRUCTURE; CRYSTALLIZATION; DROSOPHILA MELANOGASTER; HUMAN; IN VIVO STUDY; MASS SPECTROMETRY; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN STABILITY; PROTEIN STRUCTURE; STRUCTURE ANALYSIS; THERMOSTABILITY;

ANIMALS; CRYSTALLOGRAPHY, X-RAY; CYSTEINE; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MODELS, MOLECULAR; NERVE TISSUE PROTEINS; ONCOGENE PROTEINS; OXIDATION-REDUCTION; PROTEIN STABILITY;

DROSOPHILA MELANOGASTER; HEXAPODA;

EID: 84860774386     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi3003296     Document Type: Article

References (75)

1. Nagakubo, D., Taira, T., Kitaura, H., Ikeda, M., Tamai, K., IguchiAriga, S. M. M., and Ariga, H. (1997) DJ-1, a novel oncogene which transforms mouse NIH3T3 cells in cooperation with ras Biochem. Biophys. Res. Commun. 231, 509-513 (Pubitemid 27214343)
2. Bonifati, V., Rizzu, P., van Baren, M. J., Schaap, O., Breedveld, G. J., Krieger, E., Dekker, M. C. J., Squitieri, F., Ibanez, P., Joosse, M., van Dongen, J. W., Vanacore, N., van Swieten, J. C., Brice, A., Meco, G., van Duijn, C. M., Oostra, B. A., and Heutink, P. (2003) Mutations in the DJ-1 gene associated with autosomal recessive early-onset parkinsonism Science 299, 256-259 (Pubitemid 36131051)
3. Canet-Aviles, R. M., Wilson, M. A., Miller, D. W., Ahmad, R., McLendon, C., Bandyopadhyay, S., Baptista, M. J., Ringe, D., Petsko, G. A., and Cookson, M. R. (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 (Pubitemid 38781618)
4. Takahashi-Niki, K., Niki, T., Taira, T., Iguchi-Ariga, S. M. M., and Ariga, H. (2004) Reduced anti-oxidative stress activities of DJ-1 mutants found in Parkinson's disease patients Biochem. Biophys. Res. Commun. 320, 389-397 (Pubitemid 38798879)
5. Meulener, M., Whitworth, A. J., Armstrong-Gold, C. E., Rizzu, P., Heutink, P., Wes, P. D., Pallanck, L. J., and Bonini, N. M. (2005) Drosophila DJ-1 mutants are selectively sensitive to environmental toxins associated with Parkinson's disease Curr. Biol. 15, 1572-1577 (Pubitemid 41219597)
6. Larsen, N. J., Ambrosi, G., Mullett, S. J., Berman, S. B., and Hinkle, D. A. (2011) DJ-1 knock-down impairs astrocyte mitochondrial function Neuroscience 196, 251-264
7. Guzman, J. N., Sanchez-Padilla, J., Wokosin, D., Kondapalli, J., Ilijic, E., Schumacker, P. T., and Surmeier, D. J. (2010) Oxidant stress evoked by pacemaking in dopaminergic neurons is attenuated by DJ-1 Nature 468, 696-700
8. Im, J. Y., Lee, K. W., Junn, E., and Mouradian, M. M. (2010) DJ-1 protects against oxidative damage by regulating the thioredoxin/ASK1 complex Neurosci. Res. 67, 203-208
9. Waak, J., Weber, S. S., Gorner, K., Schall, C., Ichijo, H., Stehle, T., and Kahle, P. J. (2009) Oxidizable residues mediating protein stability and cytoprotective interaction of DJ-1 with apoptosis signal-regulating kinase 1 J. Biol. Chem. 284, 14245-14257
10. Kim, R. H., Peters, M., Jang, Y., Shi, W., Pintilie, M., Fletcher, G. C., DeLuca, C., Liepa, J., Zhou, L., Snow, B., Binari, R. C., Manoukian, A. S., Bray, M. R., Liu, F. F., Tsao, M. S., and Mak, T. W. (2005) DJ-1, a novel regulator of the tumor suppressor PTEN Cancer Cell 7, 263-273 (Pubitemid 40568685)
11. Das, F., Dey, N., Venkatesan, B., Kasinath, B. S., Ghosh-Choudhury, N., and Choudhury, G. G. (2011) High glucose upregulation of early-onset Parkinson's disease protein DJ-1 integrates the PRAS40/TORC1 axis to mesangial cell hypertrophy Cell. Signalling 23, 1311-1319
12. Karunakaran, S., Diwakar, L., Saeed, U., Agarwal, V., Ramakrishnan, S., Iyengar, S., and Ravindranath, V. (2007) Activation of apoptosis signal regulating kinase 1 (ASK1) and translocation of death-associated protein, Daxx, in substantia nigra pars compacta in a mouse model of Parkinson's disease: Protection by α-lipoic acid FASEB J. 21, 2226-2236 (Pubitemid 47026457)
13. Ren, H., Fu, K., Mu, C., Li, B., Wang, D., and Wang, G. (2010) DJ-1, a cancer and Parkinson's disease associated protein, regulates autophagy through JNK pathway in cancer cells Cancer Lett. 297, 101-108
14. Aron, L., Klein, P., Pham, T. T., Kramer, E. R., Wurst, W., and Klein, R. (2010) Pro-survival role for Parkinson's associated gene DJ-1 revealed in trophically impaired dopaminergic neurons PLoS Biol. 8, e1000349
15. Wang, Z., Liu, J., Chen, S., Wang, Y., Cao, L., Zhang, Y., Kang, W., Li, H., Gui, Y., and Ding, J. (2011) DJ-1 modulates the expression of Cu/Zn-superoxide dismutase-1 through the Erk1/2-Elk1 pathway in neuroprotection Ann. Neurol. 70, 591-599
16. Fan, J., Ren, H., Jia, N., Fei, E., Zhou, T., Jiang, P., Wu, M., and Wang, G. (2008) DJ-1 decreases Bax expression through repressing p53 transcriptional activity J. Biol. Chem. 283, 4022-4030
17. Vasseur, S., Afzal, S., Tomasini, R., Guillaumond, F., Tardivel-Lacombe, J., Mak, T. W., and Iovanna, J. L. (2012) Consequences of DJ-1 upregulation following p53 loss and cell transformation Oncogene 31, 664-670
18. Bretaud, S., Allen, C., Ingham, P. W., and Bandmann, O. (2007) p53-dependent neuronal cell death in a DJ-1-deficient zebrafish model of Parkinson's disease J. Neurochem. 100, 1626-1635 (Pubitemid 46376201)
19. Shinbo, Y., Taira, T., Niki, T., Iguchi-Ariga, S. M., and Ariga, H. (2005) DJ-1 restores p53 transcription activity inhibited by Topors/p53BP3 Int. J. Oncol. 26, 641-648
20. McNally, R. S., Davis, B. K., Clements, C. M., Accavitti-Loper, M. A., Mak, T. W., and Ting, J. P. (2011) DJ-1 enhances cell survival through the binding of Cezanne, a negative regulator of NF-κB J. Biol. Chem. 286, 4098-4106
21. Clements, C. M., McNally, R. S., Conti, B. J., Mak, T. W., and Ting, J. P. (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 (Pubitemid 44583169)
22. Shendelman, S., Jonason, A., Martinat, C., Leete, T., and Abeliovich, A. (2004) DJ-1 is a redox-dependent molecular chaperone that inhibits α-synuclein aggregate formation PLoS Biol. 2, e362
23. Zhou, W., Zhu, M., Wilson, M. A., Petsko, G. A., and Fink, A. L. (2006) The oxidation state of DJ-1 regulates its chaperone activity toward α-synuclein J. Mol. Biol. 356, 1036-1048 (Pubitemid 43145955)
24. van der Brug, M. P., Blackinton, J., Chandran, J., Hao, L. Y., Lal, A., Mazan-Mamczarz, K., Martindale, J., Xie, C., Ahmad, R., Thomas, K. J., Beilina, A., Gibbs, J. R., Ding, J., Myers, A. J., Zhan, M., Cai, H., Bonini, N. M., Gorospe, M., and Cookson, M. R. (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
25. Liu, F., Nguyen, J. L., Hulleman, J. D., Li, L., and Rochet, J. C. (2008) Mechanisms of DJ-1 neuroprotection in a cellular model of Parkinson's disease J. Neurochem. 105, 2435-2453 (Pubitemid 351782273)
26. Zhou, W. and Freed, C. R. (2005) DJ-1 up-regulates glutathione synthesis during oxidative stress and inhibits A53T α-synuclein toxicity J. Biol. Chem. 280, 43150-43158 (Pubitemid 43049281)
27. Xu, J., Zhong, N., Wang, H., Elias, J. E., Kim, C. Y., Woldman, I., Pifl, C., Gygi, S. P., Geula, C., and Yankner, B. A. (2005) The Parkinson's disease-associated DJ-1 protein is a transcriptional co-activator that protects against neuronal apoptosis Hum. Mol. Genet. 14, 1231-1241 (Pubitemid 40613911)
28. Auluck, P. K., Chan, H. Y., Trojanowski, J. Q., Lee, V. M., and Bonini, N. M. (2002) Chaperone suppression of α-synuclein toxicity in a Drosophila model for Parkinson's disease Science 295, 865-868 (Pubitemid 34118369)
29. Menzies, F. M., Yenisetti, S. C., and Min, K. T. (2005) Roles of Drosophila DJ-1 in survival of dopaminergic neurons and oxidative stress Curr. Biol. 15, 1578-1582 (Pubitemid 41219598)
30. Park, J., Kim, S. Y., Cha, G. H., Lee, S. B., Kim, S., and Chung, J. (2005) Drosophila DJ-1 mutants show oxidative stress-sensitive locomotive dysfunction Gene 361, 133-139 (Pubitemid 41506941)
31. Lavara-Culebras, E., Munoz-Soriano, V., Gomez-Pastor, R., Matallana, E., and Paricio, N. (2010) Effects of pharmacological agents on the lifespan phenotype of Drosophila DJ-1β mutants Gene 462, 26-33
32. Hao, L. Y., Giasson, B. I., and Bonini, N. M. (2010) DJ-1 is critical for mitochondrial function and rescues PINK1 loss of function Proc. Natl. Acad. Sci. U.S.A. 107, 9747-9752
33. Meulener, M. C., Xu, K. X., Thomson, L., Ischiropoulos, H., and Bonini, N. M. (2006) Mutational analysis of DJ-1 in Drosophila implicates functional inactivation by oxidative damage and aging (vol 103, pg 12517, 2006) Proc. Natl. Acad. Sci. U.S.A. 103, 14978-14978
34. Blackinton, J., Lakshminarasimhan, M., Thomas, K. J., Ahmad, R., Greggio, E., Raza, A. S., Cookson, M. R., and Wilson, M. A. (2009) Formation of a stabilized cysteine sulfinic acid is critical for the mitochondrial function of the parkinsonism protein DJ-1 J. Biol. Chem. 284, 6476-6485
35. Madian, A. G., Hindupur, J., Hulleman, J. D., Diaz-Maldonado, N., Mishra, V. R., Guigard, E., Kay, C. M., Rochet, J. C., and Regnier, F. E. (2012) Effect of Single Amino Acid Substitution on Oxidative Modifications of the Parkinson's Disease-Related Protein, DJ-1 Mol. Cell. Proteomics 11, M111 010892
36. Mitsumoto, A., Nakagawa, Y., Takeuchi, A., Okawa, K., Iwamatsu, A., and Takanezawa, Y. (2001) Oxidized forms of peroxiredoxins and DJ-1 on two-dimensional gels increased in response to sublethal levels of paraquat Free Radical Res. 35, 301-310 (Pubitemid 32734231)
37. Wilson, M. A. (2011) The role of cysteine oxidation in DJ-1 function and dysfunction Antioxid. Redox Signaling 15, 111-122
38. Lin, J., Nazarenus, T. J., Frey, J. L., Liang, X., Wilson, M. A., and Stone, J. M. (2011) A plant DJ-1 homolog is essential for Arabidopsis thaliana chloroplast development PLoS One 6, e23731
39. Hulleman, J. D., Mirzaei, H., Guigard, E., Taylor, K. L., Ray, S. S., Kay, C. M., Regnier, F. E., and Rochet, J. C. (2007) Destabilization of DJ-1 by familial substitution and oxidative modifications: Implications for Parkinson's disease Biochemistry 46, 5776-5789 (Pubitemid 46764126)
40. Choi, J., Sullards, M. C., Olzmann, J. A., Rees, H. D., Weintraub, S. T., Bostwick, D. E., Gearing, M., Levey, A. I., Chin, L. S., and Li, L. (2006) Oxidative damage of DJ-1 is linked to sporadic Parkinson and Alzheimer diseases J. Biol. Chem. 281, 10816-10824 (Pubitemid 43855504)
41. a depression by a protonated glutamic acid in human DJ-1 Biochemistry 47, 7430-7440 (Pubitemid 351991022)
42. Chen, J., Li, L., and 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
43. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol. 276, 307-326 (Pubitemid 27085611)
44. Collaborative Computational Project, Number 4 (1994) The CCP4 suite: Programs for protein crystallography Acta Crystallogr. D50, 760-763
45. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software J. Appl. Crystallogr. 40, 658-674 (Pubitemid 47080256)
46. Terwilliger, T. C., Grosse-Kunstleve, R. W., Afonine, P. V., Moriarty, N. W., Zwart, P. H., Hung, L. W., Read, R. J., and Adams, P. D. (2008) Iterative model building, structure refinement and density modification with the PHENIX AutoBuild wizard Acta Crystallogr. D64, 61-69 (Pubitemid 350308678)
47. Emsley, P. and Cowtan, K. (2004) Coot: Model-building tools for molecular graphics Acta Crystallogr. D60, 2126-2132 (Pubitemid 41742764)
48. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallogr. D53, 240-255 (Pubitemid 27235885)
49. Winn, M. D., Isupov, M. N., and Murshudov, G. N. (2001) Use of TLS parameters to model anisotropic displacements in macromolecular refinement Acta Crystallogr. D57, 122-133 (Pubitemid 32062682)
50. Davis, I. W., Leaver-Fay, A., Chen, V. B., Block, J. N., Kapral, G. J., Wang, X., Murray, L. W., Arendall, W. B., III, Snoeyink, J., Richardson, J. S., and Richardson, D. C. (2007) MolProbity: All-atom contacts and structure validation for proteins and nucleic acids Nucleic Acids Res. 35, W375-W383
51. Pantoliano, M. W., Petrella, E. C., Kwasnoski, J. D., Lobanov, V. S., Myslik, J., Graf, E., Carver, T., Asel, E., Springer, B. A., Lane, P., and Salemme, F. R. (2001) High-density miniaturized thermal shift assays as a general strategy for drug discovery J. Biomol. Screening 6, 429-440 (Pubitemid 34052847)
52. Krissinel, E. and Henrick, K. (2007) Inference of macromolecular assemblies from crystalline state J. Mol. Biol. 372, 774-797 (Pubitemid 47321791)
53. Abou-Sleiman, P. M., Healy, D. G., Quinn, N., Lees, A. J., and Wood, N. W. (2003) The role of pathogenic DJ-1 mutations in Parkinson's disease Ann. Neurol. 54, 283-286 (Pubitemid 37072030)
54. Blackinton, J., Ahmad, R., Miller, D. W., van der Brug, M. P., Canet-Aviles, R. M., Hague, S. M., Kaleem, M., and Cookson, M. R. (2005) Effects of DJ-1 mutations and polymorphisms on protein stability and subcellular localization Brain Res. Mol. Brain Res. 134, 76-83 (Pubitemid 40403640)
55. Lakshminarasimhan, M., Maldonado, M. T., Zhou, W., Fink, A. L., and Wilson, M. A. (2008) Structural impact of three Parkinsonism-associated missense mutations on human DJ-1 Biochemistry 47, 1381-1392 (Pubitemid 351198714)
56. Malki, A., Caldas, T., Abdallah, J., Kern, R., Eckey, V., Kim, S. J., Cha, S. S., Mori, H., and Richarme, G. (2005) Peptidase activity of the Escherichia coli Hsp31 chaperone J. Biol. Chem. 280, 14420-14426 (Pubitemid 40562781)
57. Subedi, K. P., Choi, D., Kim, I., Min, B., and Park, C. (2011) Hsp31 of Escherichia coli K-12 is glyoxalase III Mol. Microbiol. 81, 926-936
58. Goda, M., Hashimoto, Y., Takase, M., Herai, S., Iwahara, Y., Higashibata, H., and Kobayashi, M. (2002) Isonitrile hydratase from Pseudomonas putida N19-2. Cloning, sequencing, gene expression, and identification of its active acid residue J. Biol. Chem. 277, 45860-45865 (Pubitemid 35417565)
59. Halio, S. B., Blumentals, I. I., Short, S. A., Merrill, B. M., and Kelly, R. M. (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 (Pubitemid 26134486)
60. Du, X. L., Choi, I. G., Kim, R., Wang, W. R., Jancarik, J., Yokota, H., and Kim, S. H. (2000) Crystal structure of an intracellular protease from Pyrococcus horikoshii at 2-angstrom resolution Proc. Natl. Acad. Sci. U.S.A. 97, 14079-14084 (Pubitemid 32016533)
61. Quigley, P. M., Korotkov, K., Baneyx, F., and Hol, W. G. (2003) The 1.6-Å 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 (Pubitemid 36356552)
62. Lee, S. J., Kim, S. J., Kim, I. K., Ko, J., Jeong, C. S., Kim, G. H., Park, C., Kang, S. O., Suh, P. G., Lee, H. S., and Cha, S. S. (2003) Crystal structures of human DJ-1 and Escherichia coli Hsp31, which share an evolutionarily conserved domain J. Biol. Chem. 278, 44552-44559 (Pubitemid 37377208)
63. Fioravanti, E., Dura, M. A., Lascoux, D., Micossi, E., Franzetti, B., and McSweeney, S. (2008) Structure of the Stress Response Protein DR1199 from Deinococcus radiodurans: A Member of the DJ-1 Superfamily Biochemistry 47, 11581-11589
64. Abdallah, J., Kern, R., Malki, A., Eckey, V., and Richarme, G. (2006) Cloning, expression, and purification of the general stress protein YhbO from Escherichia coli Protein Expression Purif. 47, 455-460 (Pubitemid 43729003)
65. Huai, Q., Sun, Y., Wang, H., Chin, L. S., Li, L., Robinson, H., and Ke, H. (2003) Crystal structure of DJ-1/RS and implication on familial Parkinson's disease FEBS Lett. 549, 171-175 (Pubitemid 36959865)
66. Knobbe, C. B., Revett, T. J., Bai, Y., Chow, V., Jeon, A. H., Bohm, C., Ehsani, S., Kislinger, T., Mount, H. T., Mak, T. W., St George-Hyslop, P., and Schmitt-Ulms, G. (2011) Choice of biological source material supersedes oxidative stress in its influence on DJ-1 in vivo interactions with Hsp90 J. Proteome Res. 10, 4388-4404
67. Emanuelsson, O., Brunak, S., von Heijne, G., and Nielsen, H. (2007) Locating proteins in the cell using TargetP, SignalP and related tools Nat. Protoc. 2, 953-971 (Pubitemid 46745592)
68. Wilson, M. A., Collins, J. L., Hod, Y., Ringe, D., and Petsko, G. A. (2003) The 1.1-Å 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 (Pubitemid 37033916)
69. Ren, H., Fu, K., Wang, D., Mu, C., and Wang, G. (2011) Oxidized DJ-1 interacts with the mitochondrial protein BCL-XL J. Biol. Chem. 286, 35308-35317
70. Premkumar, L., Dobaczewska, M. K., and Riedl, S. J. (2011) Identification of an artificial peptide motif that binds and stabilizes reduced human DJ-1 J. Struct. Biol. 176, 414-418
71. Mueller, M., Kratzer, R., Schiller, M., Slavica, A., Rechberger, G., Kollroser, M., and Nidetzky, B. (2010) The role of Cys108 in Trigonopsis variabilis d -amino acid oxidase examined through chemical oxidation studies and point mutations C108S and C108D Biochim. Biophys. Acta 1804, 1483-1491
72. Fox, J. H., Connor, T., Stiles, M., Kama, J., Lu, Z., Dorsey, K., Lieberman, G., Sapp, E., Cherny, R. A., Banks, M., Volitakis, I., DiFiglia, M., Berezovska, O., Bush, A. I., and Hersch, S. M. (2011) Cysteine oxidation within N-terminal mutant Huntingtin promotes oligomerization and delays clearance of soluble protein J. Biol. Chem. 286, 18320-18330
73. Willis, M. N., Liu, Y., Biterova, E. I., Simpson, M. A., Kim, H., Lee, J., and Barycki, J. J. (2011) Enzymatic defects underlying hereditary glutamate cysteine ligase deficiency are mitigated by association of the catalytic and regulatory subunits Biochemistry 50, 6508-6517
74. Logan, T., Clark, L., and Ray, S. S. (2010) Engineered disulfide bonds restore chaperone-like function of DJ-1 mutants linked to familial Parkinson's disease Biochemistry 49, 5624-5633
75. Malgieri, G. and Eliezer, D. (2008) Structural effects of Parkinson's disease linked DJ-1 mutations Protein Sci. 17, 855-868 (Pubitemid 351629580)