Redox regulation of protein function via cysteine S-nitrosylation and its relevance to neurodegenerative diseases

International Journal of Cell Biology

Volumn , Issue , 2012, Pages

  Akhtar, Mohd Waseem ^a   Sunico, Carmen R ^a   Nakamura, Tomohiro ^a   Lipton, Stuart A ^a  

^a BURNHAM INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN E; CYCLIN DEPENDENT KINASE 5; CYSTEINE; DJ 1 PROTEIN; DYNAMIN RELATED PROTEIN 1; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; MEMBRANE PROTEIN; NITRIC OXIDE; PARKIN; PEROXIREDOXIN; PROTEIN DISULFIDE ISOMERASE; UNCLASSIFIED DRUG; X LINKED INHIBITOR OF APOPTOSIS;

ALZHEIMER DISEASE; CELL DEATH; CELL FUNCTION; CHEMICAL MODIFICATION; DEGENERATIVE DISEASE; ENDOPLASMIC RETICULUM; HUMAN; MITOCHONDRION; NITROSYLATION; NONHUMAN; OXIDATION REDUCTION REACTION; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; SYNAPSE; TRANSNITROSYLATION;

EID: 84866253155     PISSN: 16878876     EISSN: 16878884     Source Type: Journal    
DOI: 10.1155/2012/463756     Document Type: Review

References (99)

1. Finkel T., Signal transduction by reactive oxygen species. Journal of Cell Biology 2011 194 1 7 15 2-s2.0-79960286223 10.1083/jcb.201102095
2. Imlay J. A., Pathways of oxidative damage. Annual Review of Microbiology 2003 57 395 418 2-s2.0-0242608621 10.1146/annurev.micro.57.030502.090938 (Pubitemid 37392949)
3. 2 involves KEAP1 disulfide formation. Journal of Biological Chemistry 2010 285 11 8463 8471 2-s2.0-77950887186 10.1074/jbc.M109.051714
4. Groeger A. L., Freeman B. A., Signaling actions of electrophiles: anti-inflammatory therapeutic candidates. Molecular Interventions 2010 10 1 39 50 2-s2.0-76349087133 10.1124/mi.10.1.7
5. Akaike T., Fujii S., Sawa T., Ihara H., Cell signaling mediated by nitrated cyclic guanine nucleotide. Nitric Oxide 2010 23 3 166 174 2-s2.0-77956009695 10.1016/j.niox.2010.06.006
6. Satoh T., Lipton S. A., Redox regulation of neuronal survival mediated by electrophilic compounds. Trends in Neurosciences 2007 30 1 37 45 2-s2.0-33845648094 10.1016/j.tins.2006.11.004 (Pubitemid 44960491)
7. Satoh T., Okamoto S. I., Cui J., Watanabe Y., Furuta K., Suzuki M., Tohyama K., Lipton S. A., Activation of the Keap1/Nrf2 pathway for neuroprotection by electrophillic phase II inducers. Proceedings of the National Academy of Sciences of the United States of America 2006 103 3 768 773 2-s2.0-31444447800 10.1073/pnas.0505723102 (Pubitemid 43153100)
8. Satoh T., Kosaka K., Itoh K., Kobayashi A., Yamamoto M., Shimojo Y., Kitajima C., Cui J., Kamins J., Okamoto S. I., Izumi M., Shirasawa T., Lipton S. A., Carnosic acid, a catechol-type electrophilic compound, protects neurons both in vitro and in vivo through activation of the Keap1/Nrf2 pathway via S-alkylation of targeted cysteines on Keap1. Journal of Neurochemistry 2008 104 4 1116 1131 2-s2.0-38449111059 10.1111/j.1471-4159.2007.05039.x (Pubitemid 351143643)
9. Kraft A. D., Johnson D. A., Johnson J. A., Nuclear factor E2-related factor 2-dependent antioxidant response element activation by tert-butylhydroquinone and sulforaphane occurring preferentially in astrocytes conditions neurons against oxidative insult. Journal of Neuroscience 2004 24 5 1101 1112 2-s2.0-0842304134 10.1523/JNEUROSCI.3817-03.2004 (Pubitemid 38177017)
10. Morimoto R. I., Proteotoxic stress and inducible chaperone networks in neurodegenerative disease and aging. Genes and Development 2008 22 11 1427 1438 2-s2.0-44849094781 10.1101/gad.1657108 (Pubitemid 351793077)
11. Bukau B., Weissman J., Horwich A., Molecular chaperones and protein quality control. Cell 2006 125 3 443 451 2-s2.0-33646127577 10.1016/j.cell.2006. 04.014
12. Martínez-Ruiz A., Cadenas S., Lamas S., Nitric oxide signaling: classical, less classical, and nonclassical mechanisms. Free Radical Biology and Medicine 2011 51 1 17 29 2-s2.0-79957933470 10.1016/j.freeradbiomed.2011.04.010
13. Forstermann U., Schmidt H. H. H. W., Pollock J. S., Sheng H., Mitchell J. A., Warner T. D., Nakane M., Murad F., Isoforms of nitric oxide synthase. Characterization and purification from different cell types. Biochemical Pharmacology 1991 42 10 1849 1857 2-s2.0-0025989159 10.1016/0006-2952(91)90581-O
14. Steinert J. R., Chernova T., Forsythe I. D., Nitric oxide signaling in brain function, dysfunction, and dementia. Neuroscientist 2010 16 4 435 452 2-s2.0-77956318603 10.1177/1073858410366481
15. Sattler R., Xiong Z., Lu W. Y., Hafner M., MacDonald J. F., Tymianski M., Specific coupling of NMDA receptor activation to nitric oxide neurotoxicity by PSD-95 protein. Science 1999 284 5421 1845 1848 2-s2.0-0033546347 10.1126/science.284.5421.1845 (Pubitemid 29291436)
16. Russwurm M., Koesling D., NO activation of guanylyl cyclase. EMBO Journal 2004 23 22 4443 4450 2-s2.0-10044276844 10.1038/sj.emboj.7600422 (Pubitemid 39601969)
17. Hofmann F., The biology of cyclic GMP-dependent protein kinases. Journal of Biological Chemistry 2005 280 1 1 4 2-s2.0-12844256402 10.1074/jbc.R400035200 (Pubitemid 40164957)
18. Francis S. H., Busch J. L., Corbin J. D., cGMP-dependent protein kinases and cGMP phosphodiesterases in nitric oxide and cGMP action. Pharmacological Reviews 2010 62 3 525 563 2-s2.0-77956283047 10.1124/pr.110.002907
19. Lipton S. A., Choi Y. B., Pan Z. H., Lei S. Z., Chen H. S. V., Sucher N. J., Loscalzo J., Singel D. J., Stamler J. S., A redox-based mechanism for the neuroprotective and neurodestructive effects of nitric oxide and related nitroso-compounds. Nature 1993 364 6438 626 632 2-s2.0-0027194540 10.1038/364626a0 (Pubitemid 23274719)
20. Dawson V. L., Dawson T. M., London E. D., Bredt D. S., Snyder S. H., Nitric oxide mediates glutamate neurotoxicity in primary cortical cultures. Proceedings of the National Academy of Sciences of the United States of America 1991 88 14 6368 6371 2-s2.0-0025773785 (Pubitemid 21914947)
21. Bonfoco E., Krainc D., Ankarcrona M., Nicotera P., Lipton S. A., Apoptosis and necrosis: two distinct events induced, respectively, by mild and intense insults with N-methyl-D-aspartate or nitric oxide/superoxide in cortical cell cultures. Proceedings of the National Academy of Sciences of the United States of America 1995 92 16 7162 7166 2-s2.0-0029153913 10.1073/pnas.92.16.7162
22. Sen N., Hara M. R., Ahmad A. S., Cascio M. B., Kamiya A., Ehmsen J. T., Aggrawal N., Hester L., Doré S., Snyder S. H., Sawa A., GOSPEL: a neuroprotective protein that binds to GAPDH upon S-nitrosylation. Neuron 2009 63 1 81 91 2-s2.0-68349098976
23. Choi Y. B., Tenneti L., Le D. A., Ortiz J., Bai G., Chen H. S. V., Lipton S. A., Molecular basis of NMDA receptor-coupled ion channel modulation by S- nitrosylation. Nature Neuroscience 2000 3 1 15 21 2-s2.0-0033995950 10.1038/71090 (Pubitemid 30126343)
24. Hess D. T., Matsumoto A., Kim S. O., Marshall H. E., Stamler J. S., Protein S-nitrosylation: purview and parameters. Nature Reviews Molecular Cell Biology 2005 6 2 150 166 2-s2.0-13444282230 10.1038/nrm1569 (Pubitemid 40215810)
25. Qu J., Nakamura T., Cao G., S-Nitrosylation activates Cdk5 and contributes to synaptic spine loss induced by beta-amyloid peptide. Proceedings of the National Academy of Sciences of the United States of America 2011 108 34 14330 14335 10.1073/pnas.1105172108
26. Uehara T., Nakamura T., Yao D., Shi Z. Q., Gu Z., Ma Y., Masliah E., Nomura Y., Lipton S. A., S-Nitrosylated protein-disulphide isomerase links protein misfolding to neurodegeneration. Nature 2006 441 7092 513 517 2-s2.0-33745315287 10.1038/nature04782 (Pubitemid 44050153)
27. Benhar M., Forrester M. T., Stamler J. S., Protein denitrosylation: enzymatic mechanisms and cellular functions. Nature Reviews Molecular Cell Biology 2009 10 10 721 732 2-s2.0-70349466515 10.1038/nrm2764
28. LaFerla F. M., Green K. N., Oddo S., Intracellular amyloid- β in Alzheimer's disease. Nature Reviews Neuroscience 2007 8 7 499 509 2-s2.0-34250819839 10.1038/nrn2168 (Pubitemid 46985362)
29. Selkoe D. J., Alzheimer's disease is a synaptic failure. Science 2002 298 5594 789 791 2-s2.0-0037174618 10.1126/science.1074069 (Pubitemid 35231524)
30. Terry R. D., Masliah E., Salmon D. P., Butters N., DeTeresa R., Hill R., Hansen L. A., Katzman R., Physical basis of cognitive alterations in Alzheimer's disease: synapse loss is the major correlate of cognitive impairment. Annals of Neurology 1991 30 4 572 580 2-s2.0-0025987048 10.1002/ana.410300410
31. Harman D., Aging: a theory based on free radical and radiation chemistry. Journal of Gerontology 1956 11 3 298 300 2-s2.0-77049308856
32. Beckman K. B., Ames B. N., The free radical theory of aging matures. Physiological Reviews 1998 78 2 547 581 2-s2.0-0031916984 (Pubitemid 28182903)
33. Sayre L. M., Perry G., Smith M. A., Oxidative stress and neurotoxicity. Chemical Research in Toxicology 2008 21 1 172 188 2-s2.0-38949167692 10.1021/tx700210j (Pubitemid 351219718)
34. Lyles M. M., Gilbert H. F., Catalysis of the oxidative folding of ribonuclease A by protein disulfide isomerase: pre-steady-state kinetics and the utilization of the oxidizing equivalents of the isomerase. Biochemistry 1991 30 3 619 625 2-s2.0-0025972887
35. Lyles M. M., Gilbert H. F., Catalysis of the oxidative folding of ribonuclease A by protein disulfide isomerase: dependence of the rate on the composition of the redox buffer. Biochemistry 1991 30 3 613 619 2-s2.0-0026062381
36. Kaufman R. J., Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes and Development 1999 13 10 1211 1233 2-s2.0-0033562966 (Pubitemid 29250189)
37. Scheper W., Hoozemans J. J. M., Endoplasmic reticulum protein quality control in neurodegenerative disease: the good, the bad and the therapy. Current Medicinal Chemistry 2009 16 5 615 626 2-s2.0-63149175877 10.2174/ 092986709787458506
38. Doyle K. M., Kennedy D., Gorman A. M., Unfolded proteins and endoplasmic reticulum stress in neurodegenerative disorders. Journal of Cellular and Molecular Medicine 2011 15 10 2025 2039 10.1111/j.1582-4934.2011.01374.x
39. Chen H., Chan D. C., Mitochondrial dynamicsfusion, fission, movement, and mitophagyin neurodegenerative diseases. Human Molecular Genetics 2009 18 2 R169 R176 2-s2.0-77951096150
40. Detmer S. A., Chan D. C., Functions and dysfunctions of mitochondrial dynamics. Nature Reviews Molecular Cell Biology 2007 8 11 870 879 2-s2.0-35448960851 10.1038/nrm2275 (Pubitemid 47622562)
41. Okamoto K., Shaw J. M., Mitochondrial morphology and dynamics in yeast and multicellular eukaryotes. Annual Review of Genetics 2005 39 503 536 2-s2.0-27544466847 10.1146/annurev.genet.38.072902.093019 (Pubitemid 43011125)
42. Cho D. H., Nakamura T., Fang J., Cieplak P., Godzik A., Gu Z., Lipton S. A., β -Amyloid-related mitochondrial fission and neuronal injury. Science 2009 324 5923 102 105 2-s2.0-64249133725 10.1126/science.1171091
43. Frautschy S. A., Cole G. M., Why pleiotropic interventions are needed for alzheimer's disease. Molecular Neurobiology 2010 41 2-3 392 409 2-s2.0-77955084717 10.1007/s12035-010-8137-1
44. Patrick G. N., Zukerberg L., Nikolic M., De La Monte S., Dikkes P., Tsai L. H., Conversion of p35 to p25 deregulates Cdk5 activity and promotes neurodegeneration. Nature 1999 402 6762 615 622 2-s2.0-0033540060 10.1038/45159 (Pubitemid 129516324)
45. Ohshima T., Ward J. M., Huh C. G., Longenecker G., Veeranna, Pant H. C., Brady R. O., Martin L. J., Kulkarni A. B., Targeted disruption of the cyclin-dependent kinase 5 gene results in abnormal corticogenesis, neuronal pathology and perinatal death. Proceedings of the National Academy of Sciences of the United States of America 1996 93 20 11173 11178 2-s2.0-0029768093 10.1073/pnas.93.20.11173 (Pubitemid 26333137)
46. Xie Z., Sanada K., Samuels B. A., Shih H., Tsai L. H., Serine 732 phosphorylation of FAK by Cdk5 is important for microtubule organization, nuclear movement, and neuronal migration. Cell 2003 114 4 469 482 2-s2.0-0042329506 10.1016/S0092-8674(03)00605-6 (Pubitemid 37100995)
47. Kim Y., Sung J. Y., Ceglia I., Lee K. W., Ahn J. H., Halford J. M., Kim A. M., Kwak S. P., Park J. B., Ho Ryu S., Schenck A., Bardoni B., Scott J. D., Nairn A. C., Greengard P., Phosphorylation of WAVE1 regulates actin polymerization and dendritic spine morphology. Nature 2006 442 7104 814 817 2-s2.0-33747482904 10.1038/nature04976 (Pubitemid 44258911)
48. Bertram L., Lill C. M., Tanzi R. E., The genetics of alzheimer disease: back to the future. Neuron 2010 68 2 270 281 2-s2.0-77957927865 10.1016/j.neuron.2010.10.013
49. Abrams A. J., Farooq A., Wang G., S-nitrosylation of ApoE in Alzheimer's disease. Biochemistry 2011 50 17 3405 3407 2-s2.0-79955370372 10.1021/bi200266v
50. Mayeux R., Marder K., Cote L. J., The frequency of idiopathic Parkinson's disease by age, ethnic group, and sex in northern Manhattan. American Journal of Epidemiology 1988-1993 142 8 820 827 2-s2.0-0029976137
51. Giasson B. I., Lee V. M. Y., Are ubiquitination pathways central to Parkinson's disease? Cell 2003 114 1 1 8 2-s2.0-0038784529 10.1016/S0092- 8674(03)00509-9 (Pubitemid 36859837)
52. Jenner P., Oxidative stress in Parkinson's disease. Annals of Neurology 2003 53 supplement 3 S26 S36 10.1002/ana.10483 (Pubitemid 36368560)
53. Betarbet R., Sherer T. B., MacKenzie G., Garcia-Osuna M., Panov A. V., Greenamyre J. T., Chronic systemic pesticide exposure reproduces features of Parkinson's disease. Nature Neuroscience 2000 3 12 1301 1306 2-s2.0-0033681149 10.1038/81834
54. Langston J. W., Parkinson's disease: current and future challenges. NeuroToxicology 2002 23 4-5 443 450 2-s2.0-0036776975 10.1016/S0161-813X(02) 00098-0 (Pubitemid 36527664)
55. Miller R. L., James-Kracke M., Sun G. Y., Sun A. Y., Oxidative and inflammatory pathways in parkinson's disease. Neurochemical Research 2009 34 1 55 65 2-s2.0-58149466868 10.1007/s11064-008-9656-2
56. Kitada T., Asakawa S., Hattori N., Matsumine H., Yamamura Y., Minoshima S., Yokochi M., Mizuno Y., Shimizu N., Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature 1998 392 6676 605 608 2-s2.0-0032499264 10.1038/33416 (Pubitemid 28207717)
57. Lucking C. B., Durr A., Bonifati V., Association between early-onset Parkinson's disease and mutations in the parkin gene. The New England Journal of Medicine 2000 342 21 1560 1567 10.1056/NEJM200005253422103 (Pubitemid 30340501)
58. Oliveira S. A., Scott W. K., Martin E. R., Parkin mutations and susceptibility alleles in late-onset Parkinson's disease. Annals of Neurology 2003 53 5 624 629 10.1002/ana.10524 (Pubitemid 36529436)
59. Shimura H., Hattori N., Kubo S. I., Mizuno Y., Asakawa S., Minoshima S., Shimizu N., Iwai K., Chiba T., Tanaka K., Suzuki T., Familial Parkinson disease gene product, parkin, is a ubiquitin-protein ligase. Nature Genetics 2000 25 3 302 305 2-s2.0-0033933048 10.1038/77060 (Pubitemid 30437317)
60. Jiang H., Ren Y., Zhao J., Feng J., Parkin protects human dopaminergic neuroblastoma cells against dopamine-induced apoptosis. Human Molecular Genetics 2004 13 16 1745 1754 2-s2.0-4444327827 10.1093/hmg/ddh180 (Pubitemid 39173443)
61. Dawson T. M., Dawson V. L., Molecular pathways of neurodegeneration in Parkinson's disease. Science 2003 302 5646 819 822 2-s2.0-0242363670 10.1126/science.1087753 (Pubitemid 37339614)
62. Feany M. B., Pallanck L. J., Parkin: a multipurpose neuroprotective agent? Neuron 2003 38 1 13 16 2-s2.0-0037431172 10.1016/S0896-6273(03)00201-0 (Pubitemid 36423349)
63. Von Coelln R., Dawson V. L., Dawson T. M., Parkin-associated Parkinson's disease. Cell and Tissue Research 2004 318 1 175 184 2-s2.0-5444236802 10.1007/s00441-004-0924-4 (Pubitemid 39362637)
64. Bence N. F., Sampat R. M., Kopito R. R., Impairment of the ubiquitin-proteasome system by protein aggregation. Science 2001 292 5521 1552 1555 2-s2.0-0035947372 10.1126/science.292.5521.1552 (Pubitemid 32493425)
65. Masliah E., Rockenstein E., Veinbergs I., Mallory M., Hashimoto M., Takeda A., Sagara Y., Sisk A., Mucke L., Dopaminergic loss and inclusion body formation in α -synuclein mice: implications for neurodegenerative disorders. Science 2000 287 5456 1265 1269 2-s2.0-0034681471 10.1126/science.287.5456.1265 (Pubitemid 30112148)
66. da Costa C. A., Sunyach C., Giaime E., West A., Corti O., Brice A., Safe S., Abou-Sleiman P. M., Wood N. W., Takahashi H., Goldberg M. S., Shen J., Checler F., Transcriptional repression of p53 by parkin and impairment by mutations associated with autosomal recessive juvenile Parkinson's disease. Nature Cell Biology 2009 11 11 1370 1375 2-s2.0-70449519412 10.1038/ncb1981
67. Alves da Costa C., Checler F., Apoptosis in Parkinson's disease: is p53 the missing link between genetic and sporadic Parkinsonism? Cellular Signalling 2011 23 6 963 968 2-s2.0-79952701436 10.1016/j.cellsig.2010.10.020
68. Yao D., Gu Z., Nakamura T., Shi Z. Q., Ma Y., Gaston B., Palmer L. A., Rockenstein E. M., Zhang Z., Masliah E., Uehara T., Lipton S. A., Nitrosative stress linked to sporadic Parkinson's disease: S-nitrosylation of parkin regulates its E3 ubiquitin ligase activity. Proceedings of the National Academy of Sciences of the United States of America 2004 101 29 10810 10814 2-s2.0-3242733689 10.1073/pnas.0404161101 (Pubitemid 38955824)
69. Chung K. K. K., Thomas B., Li X., Pletnikova O., Troncoso J. C., Marsh L., Dawson V. L., Dawson T. M., S-nitrosylation of parkin regulates ubiquitination and compromises parkin's protective function. Science 2004 304 5675 1328 1331 2-s2.0-2542534741 10.1126/science.1093891 (Pubitemid 38697430)
70. Sue G. R., Ho Z. C., Kim K., Peroxiredoxins: a historical overview and speculative preview of novel mechanisms and emerging concepts in cell signaling. Free Radical Biology and Medicine 2005 38 12 1543 1552 2-s2.0-19444375216 10.1016/j.freeradbiomed.2005.02.026 (Pubitemid 40726061)
71. Rhee S. G., Kang S. W., Jeong W., Chang T. S., Yang K. S., Woo H. A., Intracellular messenger function of hydrogen peroxide and its regulation by peroxiredoxins. Current Opinion in Cell Biology 2005 17 2 183 189 2-s2.0-15044362438 10.1016/j.ceb.2005.02.004 (Pubitemid 40380942)
72. Wood Z. A., Schröder E., Harris J. R., Poole L. B., Structure, mechanism and regulation of peroxiredoxins. Trends in Biochemical Sciences 2003 28 1 32 40 2-s2.0-0037222255 10.1016/S0968-0004(02)00003-8 (Pubitemid 36051004)
73. Kim S. H., Fountoulakis M., Cairns N., Lubec G., Protein levels of human peroxiredoxin subtypes in brains of patients with Alzheimer's disease and Down Syndrome. Journal of Neural Transmission, Supplement 2001 61 223 235 2-s2.0-0035233637 (Pubitemid 38085085)
74. Krapfenbauer K., Engidawork E., Cairns N., Fountoulakis M., Lubec G., Aberrant expression of peroxiredoxin subtypes in neurodegenerative disorders. Brain Research 2003 967 1-2 152 160 2-s2.0-0344406145 10.1016/S0006-8993(02) 04243-9 (Pubitemid 36324297)
75. Fang J., Nakamura T., Cho D. H., Gu Z., Lipton S. A., S-nitrosylation of peroxiredoxin 2 promotes oxidative stress-induced neuronal cell death in Parkinson's disease. Proceedings of the National Academy of Sciences of the United States of America 2007 104 47 18742 18747 2-s2.0-36749094065 10.1073/pnas.0705904104 (Pubitemid 350210767)
76. Romero-Puertas M. C., Laxa M., Mattè A., Zaninotto F., Finkemeier I., Jones A. M. E., Perazzolli M., Vandelle E., Dietz K. J., Delledonne M., S-nitrosylation of peroxiredoxin II E promotes peroxynitrite-mediated tyrosine nitration. Plant Cell 2007 19 12 4120 4130 2-s2.0-39149133106 10.1105/tpc.107.055061 (Pubitemid 351253123)
77. Eckelman B. P., Salvesen G. S., Scott F. L., Human inhibitor of apoptosis proteins: why XIAP is the black sheep of the family. EMBO Reports 2006 7 10 988 994 2-s2.0-33749252583 10.1038/sj.embor.7400795 (Pubitemid 44480512)
78. Salvesen G. S., Duckett C. S., IAP proteins: blocking the road to death's door. Nature Reviews Molecular Cell Biology 2002 3 6 401 410 2-s2.0-0036088471 10.1038/nrm830 (Pubitemid 34685698)
79. Fuentes-Prior P., Salvesen G. S., The protein structures that shape caspase activity, specificity, activation and inhibition. Biochemical Journal 2004 384 2 201 232 2-s2.0-10644282148 10.1042/BJ20041142 (Pubitemid 39656233)
80. MacFarlane M., Merrison W., Bratton S. B., Cohen G. M., Proteasome-mediated degradation of Smac during apoptosis: XIAP promotes Smac ubiquitination in vitro. Journal of Biological Chemistry 2002 277 39 36611 36616 2-s2.0-0037184113 10.1074/jbc.M200317200
81. Schile A. J., García-Fernández M., Steller H., Regulation of apoptosis by XIAP ubiquitin-ligase activity. Genes and Development 2008 22 16 2256 2266 2-s2.0-50049110244 10.1101/gad.1663108
82. Suzuki Y., Nakabayashi Y., Takahashi R., Ubiquitin-protein ligase activity of X-linked inhibitor of apoptosis protein promotes proteasomal degradation of caspase-3 and enhances its anti-apoptotic effect in Fas-induced cell death. Proceedings of the National Academy of Sciences of the United States of America 2001 98 15 8662 8667 2-s2.0-0035902601 10.1073/pnas.161506698 (Pubitemid 32678084)
83. Vaux D. L., Silke J., IAPs, RINGs and ubiquitylation. Nature Reviews Molecular Cell Biology 2005 6 4 287 297 2-s2.0-17144377113 10.1038/nrm1621 (Pubitemid 40516895)
84. Yang Y., Fang S., Jensen J. P., Weissman A. M., Ashwell J. D., Ubiquitin protein ligase activity of IAPs and their degradation in proteasomes in response to apoptotic stimuli. Science 2000 288 5467 874 877 2-s2.0-0034607655 10.1126/science.288.5467.874 (Pubitemid 30257739)
85. Nakamura T., Wang L., Wong C. C. L., Scott F. L., Eckelman B. P., Han X., Tzitzilonis C., Meng F., Gu Z., Holland E. A., Clemente A. T., Okamoto S. I., Salvesen G. S., Riek R., Yates J. R., Lipton S. A., Transnitrosylation of XIAP regulates caspase-dependent neuronal cell death. Molecular Cell 2010 39 2 184 195 2-s2.0-77955480840 10.1016/j.molcel.2010.07.002
86. Tsang A. H. K., Lee Y. I. L., Ko H. S., Savitt J. M., Pletnikova O., Troncoso J. C., Dawson V. L., Dawson T. M., Chung K. K. K., S-nitrosylation of XIAP compromises neuronal survival in Parkinson's disease. Proceedings of the National Academy of Sciences of the United States of America 2009 106 12 4900 4905 2-s2.0-63849330999 10.1073/pnas.0810595106
87. Hara M. R., Agrawal N., Kim S. F., Cascio M. B., Fujimuro M., Ozeki Y., Takahashi M., Cheah J. H., Tankou S. K., Hester L. D., Ferris C. D., Hayward S. D., Snyder S. H., Sawa A., S-nitrosylated GAPDH initiates apoptotic cell death by nuclear translocation following Siah1 binding. Nature Cell Biology 2005 7 7 665 674 2-s2.0-22144477159 10.1038/ncb1268 (Pubitemid 40975747)
88. Wang H. Q., Takahashi R., Expanding insights on the involvement of endoplasmic reticulum stress in Parkinson's disease. Antioxidants and Redox Signaling 2007 9 5 553 561 2-s2.0-34247172998 10.1089/ars.2006.1524 (Pubitemid 46598253)
89. 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., Heutink P., Mutations in the DJ-1 gene associated with autosomal recessive early-onset parkinsonism. Science 2003 299 5604 256 259 2-s2.0-0037428241 10.1126/science.1077209 (Pubitemid 36131051)
90. Mitsumoto A., Nakagawa Y., Takeuchi A., Okawa K., Iwamatsu A., Takanezawa Y., Oxidized forms of peroxiredoxins and DJ-1 on two-dimensional gels increased in response to sublethal levels of paraquat. Free Radical Research 2001 35 3 301 310 2-s2.0-0034906096 (Pubitemid 32734231)
91. Taira T., Saito Y., Niki T., Iguchi-Ariga S. M. M., Takahashi K., Ariga H., DJ-1 has a role in antioxidative stress to prevent cell death. EMBO Reports 2004 5 2 213 218 2-s2.0-1642527499 10.1038/sj.embor.7400074 (Pubitemid 38401204)
92. Yokota T., Sugawara K., Ito K., Takahashi R., Ariga H., Mizusawa H., Down regulation of DJ-1 enhances cell death by oxidative stress, ER stress, and proteasome inhibition. Biochemical and Biophysical Research Communications 2003 312 4 1342 1348 2-s2.0-0345357664 10.1016/j.bbrc.2003.11.056 (Pubitemid 37490964)
93. Meulener M., Whitworth A. J., Armstrong-Gold C. E., Rizzu P., Heutink P., Wes P. D., Pallanck L. J., Bonini N. M., Drosophila DJ-1 mutants are selectively sensitive to environmental toxins associated with Parkinson's disease. Current Biology 2005 15 17 1572 1577 2-s2.0-24044472010 10.1016/j.cub.2005.07.064 (Pubitemid 41219597)
94. Menzies F. M., Yenisetti S. C., Min K. T., Roles of Drosophila DJ-1 in survival of dopaminergic neurons and oxidative stress. Current Biology 2005 15 17 1578 1582 2-s2.0-24044506249 10.1016/j.cub.2005.07.036 (Pubitemid 41219598)
95. Yang Y., Gehrke S., Haque M. E., Imai Y., Kosek J., Yang L., Beal M. F., Nishimura I., Wakamatsu K., Ito S., Takahashi R., Lu B., Inactivation of Drosophila DJ-1 leads to impairments of oxidative stress response and phosphatidylinositol 3-kinase/Akt signaling. Proceedings of the National Academy of Sciences of the United States of America 2005 102 38 13670 13675 2-s2.0-26444489693 10.1073/pnas.0504610102 (Pubitemid 41420906)
96. Park J., Sung Y. K., Cha G. H., Sung B. L., Kim S., Chung J., Drosophila DJ-1 mutants show oxidative stress-sensitive locomotive dysfunction. Gene 2005 361 1-2 133 139 2-s2.0-27144519984 10.1016/j.gene.2005.06.040 (Pubitemid 41506941)
97. 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., Mak T. W., Hypersensitivity of DJ-1-deficient mice to 1-methyl-4-phenyl-1,2,3,6- tetrahydropyrindine (MPTP) and oxidative stress. Proceedings of the National Academy of Sciences of the United States of America 2005 102 14 5215 5220 2-s2.0-20144389422 10.1073/pnas.0501282102
98. Ito G., Ariga H., Nakagawa Y., Iwatsubo T., Roles of distinct cysteine residues in S-nitrosylation and dimerization of DJ-1. Biochemical and Biophysical Research Communications 2006 339 2 667 672 2-s2.0-28444433110 10.1016/j.bbrc.2005.11.058 (Pubitemid 41739719)
99. Seth D., Stamler J. S., The SNO-proteome: causation and classifications. Current Opinion in Chemical Biology 2011 15 1 129 136 2-s2.0-79851512689 10.1016/j.cbpa.2010.10.012