Regulation of DJ-1 by Glutaredoxin 1 in Vivo: Implications for Parkinson's Disease

Biochemistry

Volumn 55, Issue 32, 2016, Pages 4519-4532

  Johnson, William M ^a   Golczak, Marcin ^a   Choe, Kyonghwan ^a   Curran, Pierce L ^a   Miller, Olga Gorelenkova ^a   Yao, Chen ^a   Wang, Wenzhang ^a   Lin, Jiusheng ^b   Milkovic, Nicole M ^b   Ray, Ajit ^d   Ravindranath, Vijayalakshmi ^d   Zhu, Xiongwei ^a   Wilson, Mark A ^b   Wilson Delfosse, Amy L ^a   Chen, Shu G ^a   Mieyal, John J ^a,c  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^c LOUIS STOKES CLEVELAND VA MEDICAL CENTER   (United States)

^d INDIAN INSTITUTE OF SCIENCE   (India)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CELL CULTURE; CELLS; CYTOLOGY; ENZYMES; NEURODEGENERATIVE DISEASES; PROTEINS;

CAENORHABDITIS ELEGANS; DOPAMINERGIC NEURONS; DOWNSTREAM TARGET; GLUTATHIONYLATION; OXIDATIVE MODIFICATION; PARKINSON'S DISEASE; REACTIVE CYSTEINE; REGULATORY MECHANISM;

NEURONS;

CYSTEINE; DJ 1 PROTEIN; GLUTAREDOXIN; GLUTATHIONE; PROTEIN DEGLYCASE DJ-1;

ANIMAL TISSUE; ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; MOUSE; NONHUMAN; OXIDATION REDUCTION REACTION; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN ISOLATION; PROTEIN MODIFICATION; PROTEIN PROCESSING; REGULATORY MECHANISM; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; DEFICIENCY; HUMAN; METABOLISM; TUMOR CELL LINE;

AMINO ACID SEQUENCE; ANIMALS; CAENORHABDITIS ELEGANS; CELL LINE, TUMOR; CYSTEINE; GLUTAREDOXINS; GLUTATHIONE; HUMANS; MICE; PARKINSON DISEASE; PROTEIN DEGLYCASE DJ-1; PROTEIN PROCESSING, POST-TRANSLATIONAL;

EID: 84982315589     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/acs.biochem.5b01132     Document Type: Article

References (48)

1. Lees, A. J., Hardy, J., and Revesz, T. (2009) Parkinson's disease Lancet 373, 2055-2066 10.1016/S0140-6736(09)60492-X
2. Johnson, W. M., Wilson-Delfosse, A. L., Chen, S. G., and Mieyal, J. J. (2015) The roles of redox enzymes in Parkinson's disease: Focus on glutaredoxin Ther. Targets Neurol. Dis. 2 e790
3. Li, J. Q., Tan, L., and Yu, J. T. (2014) The role of the LRRK2 gene in Parkinsonism Mol. Neurodegener. 9, 47 10.1186/1750-1326-9-47
4. Ariga, H., Takahashi-Niki, K., Kato, I., Maita, H., Niki, T., and Iguchi-Ariga, S. M. (2013) Neuroprotective function of DJ-1 in Parkinson's disease Oxid. Med. Cell. Longevity 2013, 683920 10.1155/2013/683920
5. Angeles, D. C., Ho, P., Chua, L. L., Wang, C., Yap, Y. W., Ng, C., Zhou, Z., Lim, K. L., Wszolek, Z. K., Wang, H. Y., and Tan, E. K. (2014) Thiol peroxidases ameliorate LRRK2 mutant-induced mitochondrial and dopaminergic neuronal degeneration in Drosophila Hum. Mol. Genet. 23, 3157-3165 10.1093/hmg/ddu026
6. Yao, C., El Khoury, R., Wang, W., Byrd, T. A., Pehek, E. A., Thacker, C., Zhu, X., Smith, M. A., Wilson-Delfosse, A. L., and Chen, S. G. (2010) LRRK2-mediated neurodegeneration and dysfunction of dopaminergic neurons in a Caenorhabditis elegans model of Parkinson's disease Neurobiol. Dis. 40, 73-81 10.1016/j.nbd.2010.04.002
7. Li, Y., Liu, W., Oo, T. F., Wang, L., Tang, Y., Jackson-Lewis, V., Zhou, C., Geghman, K., Bogdanov, M., Przedborski, S., Beal, M. F., Burke, R. E., and Li, C. (2009) Mutant LRRK2(R1441G) BAC transgenic mice recapitulate cardinal features of Parkinson's disease Nat. Neurosci. 12, 826-828 10.1038/nn.2349
8. Ramonet, D., Daher, J. P., Lin, B. M., Stafa, K., Kim, J., Banerjee, R., Westerlund, M., Pletnikova, O., Glauser, L., Yang, L., Liu, Y., Swing, D. A., Beal, M. F., Troncoso, J. C., McCaffery, J. M., Jenkins, N. A., Copeland, N. G., Galter, D., Thomas, B., Lee, M. K., Dawson, T. M., Dawson, V. L., and Moore, D. J. (2011) Dopaminergic neuronal loss, reduced neurite complexity and autophagic abnormalities in transgenic mice expressing G2019S mutant LRRK2 PLoS One 6, e18568 10.1371/journal.pone.0018568
9. Yue, M., Hinkle, K. M., Davies, P., Trushina, E., Fiesel, F. C., Christenson, T. A., Schroeder, A. S., Zhang, L., Bowles, E., Behrouz, B., Lincoln, S. J., Beevers, J. E., Milnerwood, A. J., Kurti, A., McLean, P. J., Fryer, J. D., Springer, W., Dickson, D. W., Farrer, M. J., and Melrose, H. L. (2015) Progressive dopaminergic alterations and mitochondrial abnormalities in LRRK2 G2019S knock-in mice Neurobiol. Dis. 78, 172-195 10.1016/j.nbd.2015.02.031
10. Alvarez-Castelao, B., Munoz, C., Sanchez, I., Goethals, M., Vandekerckhove, J., and Castano, J. G. (2012) Reduced protein stability of human DJ-1/PARK7 L166P, linked to autosomal recessive Parkinson disease, is due to direct endoproteolytic cleavage by the proteasome Biochim. Biophys. Acta, Mol. Cell Res. 1823, 524-533 10.1016/j.bbamcr.2011.11.010
11. Kumaran, R., Vandrovcova, J., Luk, C., Sharma, S., Renton, A., Wood, N. W., Hardy, J. A., Lees, A. J., and Bandopadhyay, R. (2009) Differential DJ-1 gene expression in Parkinson's disease Neurobiol. Dis. 36, 393-400 10.1016/j.nbd.2009.08.011
12. Taira, T., Saito, Y., Niki, T., Iguchi-Ariga, S. M., Takahashi, K., and Ariga, H. (2004) DJ-1 has a role in antioxidative stress to prevent cell death EMBO Rep. 5, 213-218 10.1038/sj.embor.7400074
13. Im, J. Y., Lee, K. W., Woo, J. M., Junn, E., and Mouradian, M. M. (2012) DJ-1 induces thioredoxin 1 expression through the Nrf2 pathway Hum. Mol. Genet. 21, 3013-3024 10.1093/hmg/dds131
14. Wilson, M. A. (2011) The role of cysteine oxidation in DJ-1 function and dysfunction Antioxid. Redox Signaling 15, 111-122 10.1089/ars.2010.3481
15. 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 10.1074/jbc.M806902200
16. 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 10.1073/pnas.0402959101
17. Anathy, V., Aesif, S. W., Guala, A. S., Havermans, M., Reynaert, N. L., Ho, Y. S., Budd, R. C., and Janssen-Heininger, Y. M. (2009) Redox amplification of apoptosis by caspase-dependent cleavage of glutaredoxin 1 and S-glutathionylation of Fas J. Cell Biol. 184, 241-252 10.1083/jcb.200807019
18. Qanungo, S., Starke, D. W., Pai, H. V., Mieyal, J. J., and Nieminen, A. L. (2007) Glutathione supplementation potentiates hypoxic apoptosis by S-glutathionylation of p65-NFkappaB J. Biol. Chem. 282, 18427-18436 10.1074/jbc.M610934200
19. Rodriguez-Rocha, H., Garcia Garcia, A., Zavala-Flores, L., Li, S., Madayiputhiya, N., and Franco, R. (2012) Glutaredoxin 1 protects dopaminergic cells by increased protein glutathionylation in experimental Parkinson's disease Antioxid. Redox Signaling 17, 1676-1693 10.1089/ars.2011.4474
20. Johnson, W. M., Yao, C., Siedlak, S. L., Wang, W., Zhu, X., Caldwell, G. A., Wilson-Delfosse, A. L., Mieyal, J. J., and Chen, S. G. (2015) Glutaredoxin deficiency exacerbates neurodegeneration in C. elegans models of Parkinson's disease Hum. Mol. Genet. 24, 1322-1335 10.1093/hmg/ddu542
21. Sabens, E. A., Distler, A. M., and Mieyal, J. J. (2010) Levodopa deactivates enzymes that regulate thiol-disulfide homeostasis and promotes neuronal cell death: implications for therapy of Parkinson's disease Biochemistry 49, 2715-2724 10.1021/bi9018658
22. Saeed, U., Ray, A., Valli, R. K., Kumar, A. M., and Ravindranath, V. (2010) DJ-1 loss by glutaredoxin but not glutathione depletion triggers Daxx translocation and cell death Antioxid. Redox Signaling 13, 127-144 10.1089/ars.2009.2832
23. Prahlad, J., Hauser, D. N., Milkovic, N. M., Cookson, M. R., and Wilson, M. A. (2014) Use of cysteine-reactive cross-linkers to probe conformational flexibility of human DJ-1 demonstrates that Glu18 mutations are dimers J. Neurochem. 130, 839-853 10.1111/jnc.12763
24. Murdoch, C. E., Shuler, M., Haeussler, D. J., Kikuchi, R., Bearelly, P., Han, J., Watanabe, Y., Fuster, J. J., Walsh, K., Ho, Y. S., Bachschmid, M. M., Cohen, R. A., and Matsui, R. (2014) Glutaredoxin-1 up-regulation induces soluble vascular endothelial growth factor receptor 1, attenuating post-ischemia limb revascularization J. Biol. Chem. 289, 8633-8644 10.1074/jbc.M113.517219
25. Yang, Y., Shi, W., Cui, N., Wu, Z., and Jiang, C. (2010) Oxidative stress inhibits vascular K(ATP) channels by S-glutathionylation J. Biol. Chem. 285, 38641-38648 10.1074/jbc.M110.162578
26. Zmijewski, J. W., Banerjee, S., and Abraham, E. (2009) S-glutathionylation of the Rpn2 regulatory subunit inhibits 26 S proteasomal function J. Biol. Chem. 284, 22213-22221 10.1074/jbc.M109.028902
27. Takata, T., Tsuchiya, Y., and Watanabe, Y. (2013) 90-kDa ribosomal S6 kinase 1 is inhibited by S-glutathionylation of its active-site cysteine residue during oxidative stress FEBS Lett. 587, 1681-1686 10.1016/j.febslet.2013.04.017
28. Butturini, E., Darra, E., Chiavegato, G., Cellini, B., Cozzolino, F., Monti, M., Pucci, P., Dell'Orco, D., and Mariotto, S. (2014) S-Glutathionylation at Cys328 and Cys542 impairs STAT3 phosphorylation ACS Chem. Biol. 9, 1885-1893 10.1021/cb500407d
29. Barrett, W. C., DeGnore, J. P., Konig, S., Fales, H. M., Keng, Y. F., Zhang, Z. Y., Yim, M. B., and Chock, P. B. (1999) Regulation of PTP1B via glutathionylation of the active site cysteine 215 Biochemistry 38, 6699-6705 10.1021/bi990240v
30. Girotto, S., Sturlese, M., Bellanda, M., Tessari, I., Cappellini, R., Bisaglia, M., Bubacco, L., and Mammi, S. (2012) Dopamine-derived quinones affect the structure of the redox sensor DJ-1 through modifications at Cys-106 and Cys-53 J. Biol. Chem. 287, 18738-18749 10.1074/jbc.M111.311589
31. Wang, J., Tekle, E., Oubrahim, H., Mieyal, J. J., Stadtman, E. R., and Chock, P. B. (2003) Stable and controllable RNA interference: Investigating the physiological function of glutathionylated actin Proc. Natl. Acad. Sci. U. S. A. 100, 5103-5106 10.1073/pnas.0931345100
32. Wilson, M. A., Collins, J. L., Hod, Y., Ringe, D., and Petsko, G. A. (2003) The 1.1-A 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 10.1073/pnas.1133288100
33. Heo, H. Y., Park, J. M., Kim, C. H., Han, B. S., Kim, K. S., and Seol, W. (2010) LRRK2 enhances oxidative stress-induced neurotoxicity via its kinase activity Exp. Cell Res. 316, 649-656 10.1016/j.yexcr.2009.09.014
34. Lee, J. Y., Song, J., Kwon, K., Jang, S., Kim, C., Baek, K., Kim, J., and Park, C. (2012) Human DJ-1 and its homologs are novel glyoxalases Hum. Mol. Genet. 21, 3215-3225 10.1093/hmg/dds155
35. Chen, P., DeWitt, M. R., Bornhorst, J., Soares, F. A., Mukhopadhyay, S., Bowman, A. B., and Aschner, M. (2015) Age- and manganese-dependent modulation of dopaminergic phenotypes in a C. elegans DJ-1 genetic model of Parkinson's disease Metallomics 7, 289-298 10.1039/C4MT00292J
36. Sawin, E. R., Ranganathan, R., and Horvitz, H. R. (2000) C. elegans locomotory rate is modulated by the environment through a dopaminergic pathway and by experience through a serotonergic pathway Neuron 26, 619-631 10.1016/S0896-6273(00)81199-X
37. Kim, R. H., Smith, P. D., Aleyasin, H., Hayley, S., Mount, M. P., Pownall, S., Wakeham, A., You-Ten, A. J., Kalia, S. K., Horne, P., Westaway, D., Lozano, A. M., Anisman, H., Park, D. S., and Mak, T. W. (2005) Hypersensitivity of DJ-1-deficient mice to 1-methyl-4-phenyl-1,2,3,6-tetrahydropyrindine (MPTP) and oxidative stress Proc. Natl. Acad. Sci. U. S. A. 102, 5215-5220 10.1073/pnas.0501282102
38. Xiong, R., Wang, Z., Zhao, Z., Li, H., Chen, W., Zhang, B., Wang, L., Wu, L., Li, W., Ding, J., and Chen, S. (2014) MicroRNA-494 reduces DJ-1 expression and exacerbates neurodegeneration Neurobiol. Aging 35, 705-714 10.1016/j.neurobiolaging.2013.09.027
39. Sabens Liedhegner, E. A., Gao, X. H., and Mieyal, J. J. (2012) Mechanisms of altered redox regulation in neurodegenerative diseases - focus on S - glutathionylation Antioxid. Redox Signaling 16, 543-566 10.1089/ars.2011.4119
40. Liu, X., Jann, J., Xavier, C., and Wu, H. (2015) Glutaredoxin 1 (Grx1) Protects Human Retinal Pigment Epithelial Cells From Oxidative Damage by Preventing AKT Glutathionylation Invest. Ophthalmol. Visual Sci. 56, 2821-2832 10.1167/iovs.14-15876
41. Wang, X., Yan, M. H., Fujioka, H., Liu, J., Wilson-Delfosse, A., Chen, S. G., Perry, G., Casadesus, G., and Zhu, X. (2012) LRRK2 regulates mitochondrial dynamics and function through direct interaction with DLP1 Hum. Mol. Genet. 21, 1931-1944 10.1093/hmg/dds003
42. Kinumi, T., Kimata, J., Taira, T., Ariga, H., and Niki, E. (2004) Cysteine-106 of DJ-1 is the most sensitive cysteine residue to hydrogen peroxide-mediated oxidation in vivo in human umbilical vein endothelial cells Biochem. Biophys. Res. Commun. 317, 722-728 10.1016/j.bbrc.2004.03.110
43. Chen, Y. J., Lu, C.-T., Lee, T.-Y., and Chen, Y.-J. (2014) dbGSH: a database of S-glutathionylation Bioinformatics 30, 2386-2388 10.1093/bioinformatics/btu301
44. Aleyasin, H., Rousseaux, M. W., Marcogliese, P. C., Hewitt, S. J., Irrcher, I., Joselin, A. P., Parsanejad, M., Kim, R. H., Rizzu, P., Callaghan, S. M., Slack, R. S., Mak, T. W., and Park, D. S. (2010) DJ-1 protects the nigrostriatal axis from the neurotoxin MPTP by modulation of the AKT pathway Proc. Natl. Acad. Sci. U. S. A. 107, 3186-3191 10.1073/pnas.0914876107
45. Ohta, E., Kawakami, F., Kubo, M., and Obata, F. (2011) LRRK2 directly phosphorylates Akt1 as a possible physiological substrate: impairment of the kinase activity by Parkinson's disease-associated mutations FEBS Lett. 585, 2165-2170 10.1016/j.febslet.2011.05.044
46. Ward, N. E., Stewart, J. R., Ioannides, C. G., and O'Brian, C. A. (2000) Oxidant-induced S-glutathiolation inactivates protein kinase C-alpha (PKC-alpha): a potential mechanism of PKC isozyme regulation Biochemistry 39, 10319-10329 10.1021/bi000781g
47. Antico Arciuch, V. G., Alippe, Y., Carreras, M. C., and Poderoso, J. J. (2009) Mitochondrial kinases in cell signaling: Facts and perspectives Adv. Drug Delivery Rev. 61, 1234-1249 10.1016/j.addr.2009.04.025
48. Moore, D. J., Zhang, L., Dawson, T. M., and Dawson, V. L. (2003) A missense mutation (L166P) in DJ-1, linked to familial Parkinson's disease, confers reduced protein stability and impairs homo-oligomerization J. Neurochem. 87, 1558-1567 10.1111/j.1471-4159.2003.02265.x