Cell death: Protein misfolding and neurodegenerative diseases

Apoptosis

Volumn 14, Issue 4, 2009, Pages 455-468

  Nakamura, Tomohiro ^a   Lipton, Stuart A ^a,b  

^a BURNHAM INSTITUTE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Molecular chaperone; Neurodegeneration; Protein misfolding; S Nitrosylation; Ubiquitin proteasome system

Indexed keywords

CALCIUM ION; FREE RADICAL; MEMANTINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NITRIC OXIDE; PARKIN; PROTEIN DISULFIDE ISOMERASE; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; UBIQUITIN PROTEIN LIGASE; UBIQUITIN PROTEIN LIGASE E3;

ALZHEIMER DISEASE; AMYOTROPHIC LATERAL SCLEROSIS; BRAIN DAMAGE; CALCIUM TRANSPORT; CELL DEATH; DEMENTIA; DEPRESSION; DISEASE MODEL; DRUG MECHANISM; ENZYME SYNTHESIS; HUMAN; HUNTINGTON CHOREA; MOLECULAR MODEL; NERVE CELL NECROSIS; NERVE DEGENERATION; NEUROTOXICITY; NITROSATIVE STRESS; NITROSYLATION; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN FOLDING; RECEPTOR BLOCKING; REVIEW; SIGNAL TRANSDUCTION;

CELL DEATH; HUMANS; MODELS, BIOLOGICAL; NEURODEGENERATIVE DISEASES; NITRIC OXIDE; NITROSATION; PROTEIN DISULFIDE-ISOMERASES; PROTEIN FOLDING; REACTIVE OXYGEN SPECIES; UBIQUITIN-PROTEIN LIGASES;

EID: 62449244004     PISSN: 13608185     EISSN: 1573675X     Source Type: Journal    
DOI: 10.1007/s10495-008-0301-y     Document Type: Review

References (174)

1. NF Bence RM Sampat RR Kopito 2001 Impairment of the ubiquitin-proteasome system by protein aggregation Science 292 1552 1555 10.1126/science.292.5521. 1552
2. PJ Muchowski JL Wacker 2005 Modulation of neurodegeneration by molecular chaperones Nat Rev Neurosci 6 11 22 10.1038/nrn1587
3. A Ciechanover P Brundin 2003 The ubiquitin proteasome system in neurodegenerative diseases: sometimes the chicken, sometimes the egg Neuron 40 427 446 10.1016/S0896-6273(03)00606-8
4. RR Kopito D Ron 2000 Conformational disease Nat Cell Biol 2 E207 E209 10.1038/35041139
5. MT Lin MF Beal 2006 Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases Nature 443 787 795 10.1038/nature05292
6. KJ Barnham CL Masters AI Bush 2004 Neurodegenerative diseases and oxidative stress Nat Rev Drug Discov 3 205 214 10.1038/nrd1330
7. PJ Muchowski 2002 Protein misfolding, amyloid formation, and neurodegeneration: a critical role for molecular chaperones? Neuron 35 9 12 10.1016/S0896-6273(02)00761-4
8. J Emerit M Edeas F Bricaire 2004 Neurodegenerative diseases and oxidative stress Biomed Pharmacother 58 39 46 10.1016/j.biopha.2003.11.004
9. MF Beal 2001 Experimental models of Parkinson's disease Nat Rev Neurosci 2 325 334 10.1038/35072550
10. SA Lipton PA Rosenberg 1994 Excitatory amino acids as a final common pathway for neurologic disorders N Engl J Med 330 613 622 10.1056/ NEJM199403033300907
11. SA Lipton 2006 Paradigm shift in neuroprotection by NMDA receptor blockade: memantine and beyond Nat Rev Drug Discov 5 160 170 10.1038/nrd1958
12. DS Bredt PM Hwang CE Glatt 1991 Cloned and expressed nitric oxide synthase structurally resembles cytochrome P-450 reductase Nature 351 714 718 10.1038/351714a0
13. J Garthwaite SL Charles R Chess-Williams 1988 Endothelium-derived relaxing factor release on activation of NMDA receptors suggests role as intercellular messenger in the brain Nature 336 385 388 10.1038/336385a0
14. JS Beckman TW Beckman J Chen 1990 Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide Proc Natl Acad Sci USA 87 1620 1624 10.1073/pnas.87.4.1620
15. SA Lipton YB Choi ZH Pan 1993 A redox-based mechanism for the neuroprotective and neurodestructive effects of nitric oxide and related nitroso-compounds Nature 364 626 632 10.1038/364626a0
16. K Zhang RJ Kaufman 2006 The unfolded protein response: a stress signaling pathway critical for health and disease Neurology 66 S102 S109 10.1212/01.wnl.0000192306.98198.ec
17. KK Chung B Thomas X Li 2004 S-nitrosylation of parkin regulates ubiquitination and compromises parkin's protective function Science 304 1328 1331 10.1126/science.1093891
18. D Yao Z Gu T Nakamura 2004 Nitrosative stress linked to sporadic Parkinson's disease: S-nitrosylation of parkin regulates its E3 ubiquitin ligase activity Proc Natl Acad Sci USA 101 10810 10814 10.1073/pnas.0404161101
19. SA Lipton T Nakamura D Yao 2005 Comment on "S-nitrosylation of parkin regulates ubiquitination and compromises parkin's protective function" Science 308 1870 10.1126/science.1110135
20. T Uehara T Nakamura D Yao 2006 S-nitrosylated protein-disulphide isomerase links protein misfolding to neurodegeneration Nature 441 513 517 10.1038/nature04782
21. SA Lipton 2007 Pathologically activated therapeutics for neuroprotection Nat Rev Neurosci 8 803 808 10.1038/nrn2229
22. MR Cookson 2005 The biochemistry of Parkinson's disease Annu Rev Biochem 74 29 52 10.1146/annurev.biochem.74.082803.133400
23. L Zhao C Longo-Guess BS Harris 2005 Protein accumulation and neurodegeneration in the woozy mutant mouse is caused by disruption of SIL1, a cochaperone of BiP Nat Genet 37 974 979 10.1038/ng1620
24. KS McNaught DP Perl AL Brownell CW Olanow 2004 Systemic exposure to proteasome inhibitors causes a progressive model of Parkinson's disease Ann Neurol 56 149 162 10.1002/ana.20186
25. PK Auluck HY Chan JQ Trojanowski 2002 Chaperone suppression of alpha-synuclein toxicity in a Drosophila model for Parkinson's disease Science 295 865 868 10.1126/science.1067389
26. M Arrasate S Mitra ES Schweitzer 2004 Inclusion body formation reduces levels of mutant huntingtin and the risk of neuronal death Nature 431 805 810 10.1038/nature02998
27. D Kaganovich R Kopito J Frydman 2008 Misfolded proteins partition between two distinct quality control compartments Nature 454 1088 1095 10.1038/nature07195
28. GE Hardingham Y Fukunaga H Bading 2002 Extrasynaptic NMDARs oppose synaptic NMDARs by triggering CREB shut-off and cell death pathways Nat Neurosci 5 405 414
29. 2+ and the cAMP response element-binding protein family mediate a late phase of activity-dependent neuroprotection J Neurosci 25 4279 4287 10.1523/JNEUROSCI. 5019-04.2005
30. S Papadia FX Soriano F Leveille 2008 Synaptic NMDA receptor activity boosts intrinsic antioxidant defenses Nat Neurosci 11 476 487 10.1038/nn2071
31. M Ankarcrona JM Dypbukt E Bonfoco 1995 Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function Neuron 15 961 973 10.1016/0896-6273(95)90186-8
32. E Bonfoco D Krainc M Ankarcrona 1995 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 Proc Natl Acad Sci USA 92 7162 7166 10.1073/pnas.92.16.7162
33. SL Budd L Tenneti T Lishnak SA Lipton 2000 Mitochondrial and extramitochondrial apoptotic signaling pathways in cerebrocortical neurons Proc Natl Acad Sci USA 97 6161 6166 10.1073/pnas.100121097
34. L Nowak P Bregestovski P Ascher 1984 Magnesium gates glutamate-activated channels in mouse central neurones Nature 307 462 465 10.1038/307462a0
35. 2+ of NMDA responses in spinal cord neurones Nature 309 261 263 10.1038/309261a0
36. VL Dawson TM Dawson ED London 1991 Nitric oxide mediates glutamate neurotoxicity in primary cortical cultures Proc Natl Acad Sci USA 88 6368 6371 10.1073/pnas.88.14.6368
37. M Lafon-Cazal S Pietri M Culcasi J Bockaert 1993 NMDA-dependent superoxide production and neurotoxicity Nature 364 535 537 10.1038/364535a0
38. JW Olney 1969 Brain lesions, obesity, and other disturbances in mice treated with monosodium glutamate Science 164 719 721 10.1126/science.164.3880. 719
39. JW Olney DF Wozniak NB Farber 1997 Excitotoxic neurodegeneration in Alzheimer disease. New hypothesis and new therapeutic strategies Arch Neurol 54 1234 1240
40. HS Chen SA Lipton 2006 The chemical biology of clinically tolerated NMDA receptor antagonists J Neurochem 97 1611 1626 10.1111/j.1471-4159.2006.03991.x
41. HM Abu-Soud DJ Stuehr 1993 Nitric oxide synthases reveal a role for calmodulin in controlling electron transfer Proc Natl Acad Sci USA 90 10769 10772 10.1073/pnas.90.22.10769
42. U Forstermann JP Boissel H Kleinert 1998 Expressional control of the 'constitutive' isoforms of nitric oxide synthase (NOS I and NOS III) FASEB J 12 773 790
43. JL Boucher C Moali JP Tenu 1999 Nitric oxide biosynthesis, nitric oxide synthase inhibitors and arginase competition for L-arginine utilization Cell Mol Life Sci 55 1015 1028 10.1007/s000180050352
44. JT Groves CC Wang 2000 Nitric oxide synthase: models and mechanisms Curr Opin Chem Biol 4 687 695 10.1016/S1367-5931(00)00146-0
45. KE Kolodziejska AR Burns RH Moore 2005 Regulation of inducible nitric oxide synthase by aggresome formation Proc Natl Acad Sci USA 102 4854 4859 10.1073/pnas.0500485102
46. R Betarbet TB Sherer G MacKenzie 2000 Chronic systemic pesticide exposure reproduces features of Parkinson's disease Nat Neurosci 3 1301 1306 10.1038/81834
47. Y He SZ Imam Z Dong 2003 Role of nitric oxide in rotenone-induced nigro-striatal injury J Neurochem 86 1338 1345 10.1046/j.1471-4159.2003.01938.x
48. PM Abou-Sleiman MM Muqit NW Wood 2006 Expanding insights of mitochondrial dysfunction in Parkinson's disease Nat Rev Neurosci 7 207 219 10.1038/nrn1868
49. PR Castello PS David T McClure 2006 Mitochondrial cytochrome oxidase produces nitric oxide under hypoxic conditions: implications for oxygen sensing and hypoxic signaling in eukaryotes Cell Metab 3 277 287 10.1016/j.cmet.2006.02. 011
50. AM Isaacs DB Senn M Yuan 2006 Acceleration of amyloid beta-peptide aggregation by physiological concentrations of calcium J Biol Chem 281 27916 27923 10.1074/jbc.M602061200
51. TJ O'Dell RD Hawkins ER Kandel O Arancio 1991 Tests of the roles of two diffusible substances in long-term potentiation: evidence for nitric oxide as a possible early retrograde messenger Proc Natl Acad Sci USA 88 11285 11289 10.1073/pnas.88.24.11285
52. DS Bredt SH Snyder 1994 Nitric oxide: a physiologic messenger molecule Annu Rev Biochem 63 175 195 10.1146/annurev.bi.63.070194.001135
53. EM Schuman DV Madison 1994 Locally distributed synaptic potentiation in the hippocampus Science 263 532 536 10.1126/science.8290963
54. JS Stamler DI Simon JA Osborne 1992 S-nitrosylation of proteins with nitric oxide: synthesis and characterization of biologically active compounds Proc Natl Acad Sci USA 89 444 448 10.1073/pnas.89.1.444
55. SZ Lei ZH Pan SK Aggarwal 1992 Effect of nitric oxide production on the redox modulatory site of the NMDA receptor-channel complex Neuron 8 1087 1099 10.1016/0896-6273(92)90130-6
56. ER Kandel TJ O'Dell 1992 Are adult learning mechanisms also used for development? Science 258 243 245 10.1126/science.1411522
57. JS Stamler EJ Toone SA Lipton NJ Sucher 1997 (S)NO signals: translocation, regulation, and a consensus motif Neuron 18 691 696 10.1016/S0896-6273(00)80310-4
58. DT Hess A Matsumoto SO Kim 2005 Protein S-nitrosylation: purview and parameters Nat Rev Mol Cell Biol 6 150 166 10.1038/nrm1569
59. M Benhar MT Forrester DT Hess JS Stamler 2008 Regulated protein denitrosylation by cytosolic and mitochondrial thioredoxins Science 320 1050 1054 10.1126/science.1158265
60. D Nikitovic A Holmgren 1996 S-nitrosoglutathione is cleaved by the thioredoxin system with liberation of glutathione and redox regulating nitric oxide J Biol Chem 271 19180 19185 10.1074/jbc.271.32.19180
61. Romero, JM, Bizzozero, OA (2008) Intracellular glutathione mediates the denitrosylation of protein nitrosothiols in the rat spinal cord. J Neurosci Res [Epub ahead of print]
62. G Melino F Bernassola RA Knight 1997 S-nitrosylation regulates apoptosis Nature 388 432 433 10.1038/41237
63. L Tenneti DM D'Emilia SA Lipton 1997 Suppression of neuronal apoptosis by S-nitrosylation of caspases Neurosci Lett 236 139 142 10.1016/S0304-3940(97) 00780-5
64. S Dimmeler J Haendeler M Nehls AM Zeiher 1997 Suppression of apoptosis by nitric oxide via inhibition of interleukin-1 beta-converting enzyme (ICE)-like and cysteine protease protein (CPP)-32-like proteases J Exp Med 185 601 607 10.1084/jem.185.4.601
65. JB Mannick A Hausladen L Liu 1999 Fas-induced caspase denitrosylation Science 284 651 654 10.1126/science.284.5414.651
66. WK Kim YB Choi PV Rayudu 1999 Attenuation of NMDA receptor activity and neurotoxicity by nitroxyl anion, NO Neuron 24 461 469 10.1016/S0896-6273(00) 80859-4
67. YB Choi L Tenneti DA Le 2000 Molecular basis of NMDA receptor-coupled ion channel modulation by S-nitrosylation Nat Neurosci 3 15 21 10.1038/71090
68. Z Gu M Kaul B Yan 2002 S-nitrosylation of matrix metalloproteinases: signaling pathway to neuronal cell death Science 297 1186 1190 10.1126/science.1073634
69. MR Hara N Agrawal SF Kim 2005 S-nitrosylated GAPDH initiates apoptotic cell death by nuclear translocation following Siah1 binding Nat Cell Biol 7 665 674 10.1038/ncb1268
70. SR Jaffrey H Erdjument-Bromage CD Ferris 2001 Protein S-nitrosylation: a physiological signal for neuronal nitric oxide Nat Cell Biol 3 193 197 10.1038/35055104
71. J Haendeler J Hoffmann V Tischler 2002 Redox regulatory and anti-apoptotic functions of thioredoxin depend on S-nitrosylation at cysteine 69 Nat Cell Biol 4 743 749 10.1038/ncb851
72. I Sliskovic A Raturi B Mutus 2005 Characterization of the S-denitrosation activity of protein disulfide isomerase J Biol Chem 280 8733 8741 10.1074/jbc.M408080200
73. JS Stamler DJ Singel J Loscalzo 1992 Biochemistry of nitric oxide and its redox-activated forms Science 258 1898 1902 10.1126/science.1281928
74. JS Stamler 1994 Redox signaling: nitrosylation and related target interactions of nitric oxide Cell 78 931 936 10.1016/0092-8674(94)90269-0
75. JS Stamler S Lamas FC Fang 2001 Nitrosylation. The prototypic redox-based signaling mechanism Cell 106 675 683 10.1016/S0092-8674(01)00495-0
76. SA Lipton YB Choi H Takahashi 2002 Cysteine regulation of protein function-as exemplified by NMDA-receptor modulation Trends Neurosci 25 474 480 10.1016/S0166-2236(02)02245-2
77. JS Stamler A Hausladen 1998 Oxidative modifications in nitrosative stress Nat Struct Biol 5 247 249 10.1038/nsb0498-247
78. KN Houk BN Hietbrink MD Bartberger 2003 Nitroxyl disulfides, novel intermediates in transnitrosation reactions J Am Chem Soc 125 6972 6976 10.1021/ja029655l
79. Z Huang PL Huang N Panahian 1994 Effects of cerebral ischemia in mice deficient in neuronal nitric oxide synthase Science 265 1883 1885 10.1126/science.7522345
80. C Iadecola F Zhang R Casey 1997 Delayed reduction of ischemic brain injury and neurological deficits in mice lacking the inducible nitric oxide synthase gene J Neurosci 17 9157 9164
81. P Hantraye E Brouillet R Ferrante 1996 Inhibition of neuronal nitric oxide synthase prevents MPTP-induced parkinsonism in baboons Nat Med 2 1017 1021 10.1038/nm0996-1017
82. S Przedborski V Jackson-Lewis R Yokoyama 1996 Role of neuronal nitric oxide in 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine (MPTP)-induced dopaminergic neurotoxicity Proc Natl Acad Sci USA 93 4565 4571 10.1073/pnas.93.10.4565
83. GT Liberatore V Jackson-Lewis S Vukosavic 1999 Inducible nitric oxide synthase stimulates dopaminergic neurodegeneration in the MPTP model of Parkinson disease Nat Med 5 1403 1409 10.1038/70978
84. PE Chabrier C Demerle-Pallardy M Auguet 1999 Nitric oxide synthases: targets for therapeutic strategies in neurological diseases Cell Mol Life Sci 55 1029 1035 10.1007/s000180050353
85. TS Chen JP Richie Jr CA Lang 1989 The effect of aging on glutathione and cysteine levels in different regions of the mouse brain Proc Soc Exp Biol Med 190 399 402
86. BI Giasson JE Duda IV Murray 2000 Oxidative damage linked to neurodegeneration by selective alpha-synuclein nitration in synucleinopathy lesions Science 290 985 989 10.1126/science.290.5493.985
87. MR Reynolds RW Berry LI Binder 2007 Nitration in neurodegeneration: deciphering the "Hows" "nYs Biochemistry 46 7325 7336 10.1021/bi700430y
88. MR Reynolds JF Reyes Y Fu 2006 Tau nitration occurs at tyrosine 29 in the fibrillar lesions of Alzheimer's disease and other tauopathies J Neurosci 26 10636 10645 10.1523/JNEUROSCI.2143-06.2006
89. VN Uversky G Yamin LA Munishkina 2005 Effects of nitration on the structure and aggregation of alpha-synuclein Brain Res Mol Brain Res 134 84 102 10.1016/j.molbrainres.2004.11.014
90. T Kitada S Asakawa N Hattori 1998 Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism Nature 392 605 608 10.1038/33416
91. EM Valente PM Abou-Sleiman V Caputo 2004 Hereditary early-onset Parkinson's disease caused by mutations in PINK1 Science 304 1158 1160 10.1126/science.1096284
92. MH Polymeropoulos C Lavedan E Leroy 1997 Mutation in the alpha-synuclein gene identified in families with Parkinson's disease Science 276 2045 2047 10.1126/science.276.5321.2045
93. V Bonifati P Rizzu MJ van Baren 2003 Mutations in the DJ-1 gene associated with autosomal recessive early-onset parkinsonism Science 299 256 259 10.1126/science.1077209
94. E Leroy R Boyer G Auburger 1998 The ubiquitin pathway in Parkinson's disease Nature 395 451 452 10.1038/26652
95. C Paisan-Ruiz S Jain EW Evans 2004 Cloning of the gene containing mutations that cause PARK8-linked Parkinson's disease Neuron 44 595 600 10.1016/j.neuron.2004.10.023
96. A Zimprich S Biskup P Leitner 2004 Mutations in LRRK2 cause autosomal-dominant parkinsonism with pleomorphic pathology Neuron 44 601 607 10.1016/j.neuron.2004.11.005
97. A Ramirez A Heimbach J Grundemann 2006 Hereditary parkinsonism with dementia is caused by mutations in ATP13A2, encoding a lysosomal type 5 P-type ATPase Nat Genet 38 1184 1191 10.1038/ng1884
98. CA Ross CM Pickart 2004 The ubiquitin-proteasome pathway in Parkinson's disease and other neurodegenerative diseases Trends Cell Biol 14 703 711 10.1016/j.tcb.2004.10.006
99. H Shimura N Hattori S Kubo 2000 Familial Parkinson disease gene product, parkin, is a ubiquitin-protein ligase Nat Genet 25 302 305 10.1038/77060
100. I Marin A Ferrus 2002 Comparative genomics of the RBR family, including the Parkinson's disease-related gene parkin and the genes of the ariadne subfamily Mol Biol Evol 19 2039 2050
101. M Farrer P Chan R Chen 2001 Lewy bodies and parkinsonism in families with parkin mutations Ann Neurol 50 293 300 10.1002/ana.1132
102. SR Sriram X Li HS Ko 2005 Familial-associated mutations differentially disrupt the solubility, localization, binding and ubiquitination properties of parkin Hum Mol Genet 14 2571 2586 10.1093/hmg/ddi292
103. C Hampe H Ardila-Osorio M Fournier 2006 Biochemical analysis of Parkinson's disease-causing variants of Parkin, an E3 ubiquitin-protein ligase with monoubiquitylation capacity Hum Mol Genet 15 2059 2075 10.1093/hmg/ddl131
104. N Matsuda T Kitami T Suzuki 2006 Diverse effects of pathogenic mutations of Parkin that catalyze multiple monoubiquitylation in vitro J Biol Chem 281 3204 3209 10.1074/jbc.M510393200
105. KL Lim KC Chew JM Tan 2005 Parkin mediates nonclassical, proteasomal-independent ubiquitination of synphilin-1: implications for Lewy body formation J Neurosci 25 2002 2009 10.1523/JNEUROSCI.4474-04.2005
106. KL Lim VL Dawson TM Dawson 2006 Parkin-mediated lysine 63-linked polyubiquitination: a link to protein inclusions formation in Parkinson's and other conformational diseases? Neurobiol Aging 27 524 529 10.1016/j. neurobiolaging.2005.07.023
107. H Shimura MG Schlossmacher N Hattori 2001 Ubiquitination of a new form of alpha-synuclein by parkin from human brain: implications for Parkinson's disease Science 293 263 269 10.1126/science.1060627
108. KK Chung Y Zhang KL Lim 2001 Parkin ubiquitinates the alpha-synuclein-interacting protein, synphilin-1: implications for Lewy-body formation in Parkinson disease Nat Med 7 1144 1150 10.1038/nm1001-1144
109. Y Imai M Soda H Inoue 2001 An unfolded putative transmembrane polypeptide, which can lead to endoplasmic reticulum stress, is a substrate of Parkin Cell 105 891 902 10.1016/S0092-8674(01)00407-X
110. Y Zhang J Gao KK Chung 2000 Parkin functions as an E2-dependent ubiquitin-protein ligase and promotes the degradation of the synaptic vesicle-associated protein, CDCrel-1 Proc Natl Acad Sci USA 97 13354 13359 10.1073/pnas.240347797
111. JF Staropoli C McDermott C Martinat 2003 Parkin is a component of an SCF-like ubiquitin ligase complex and protects postmitotic neurons from kainate excitotoxicity Neuron 37 735 749 10.1016/S0896-6273(03)00084-9
112. O Corti C Hampe H Koutnikova 2003 The p38 subunit of the aminoacyl-tRNA synthetase complex is a Parkin substrate: linking protein biosynthesis and neurodegeneration Hum Mol Genet 12 1427 1437 10.1093/hmg/ddg159
113. DP Huynh DR Scoles D Nguyen SM Pulst 2003 The autosomal recessive juvenile Parkinson disease gene product, parkin, interacts with and ubiquitinates synaptotagmin XI Hum Mol Genet 12 2587 2597 10.1093/hmg/ddg269
114. Y Ren J Zhao J Feng 2003 Parkin binds to alpha/beta tubulin and increases their ubiquitination and degradation J Neurosci 23 3316 3324
115. A Yamamoto A Friedlein Y Imai 2005 Parkin phosphorylation and modulation of its E3 ubiquitin ligase activity J Biol Chem 280 3390 3399 10.1074/jbc.M407724200
116. Y Imai M Soda S Hatakeyama 2002 CHIP is associated with Parkin, a gene responsible for familial Parkinson's disease, and enhances its ubiquitin ligase activity Mol Cell 10 55 67 10.1016/S1097-2765(02)00583-X
117. SK Kalia S Lee PD Smith 2004 BAG5 inhibits parkin and enhances dopaminergic neuron degeneration Neuron 44 931 945 10.1016/j.neuron.2004.11.026
118. L Fallon CM Belanger AT Corera 2006 A regulated interaction with the UIM protein Eps15 implicates parkin in EGF receptor trafficking and PI(3)K-Akt signalling Nat Cell Biol 8 834 842 10.1038/ncb1441
119. DJ Moore AB West DA Dikeman 2008 Parkin mediates the degradation- independent ubiquitination of Hsp70 J Neurochem 105 1806 1819 10.1111/j.1471-4159.2008.05261.x
120. Y Liu L Fallon HA Lashuel 2002 The UCH-L1 gene encodes two opposing enzymatic activities that affect alpha-synuclein degradation and Parkinson's disease susceptibility Cell 111 209 218 10.1016/S0092-8674(02)01012-7
121. K Nishikawa H Li R Kawamura 2003 Alterations of structure and hydrolase activity of parkinsonism-associated human ubiquitin carboxyl-terminal hydrolase L1 variants Biochem Biophys Res Commun 304 176 183 10.1016/S0006-291X(03)00555-2
122. J Choi AI Levey ST Weintraub 2004 Oxidative modifications and down-regulation of ubiquitin carboxyl-terminal hydrolase L1 associated with idiopathic Parkinson's and Alzheimer's diseases J Biol Chem 279 13256 13264 10.1074/jbc.M314124200
123. KK Chung TM Dawson VL Dawson 2005 Nitric oxide, S-nitrosylation and neurodegeneration Cell Mol Biol Noisy-le-grand 51 247 254
124. Z Gu T Nakamura D Yao 2005 Nitrosative and oxidative stress links dysfunctional ubiquitination to Parkinson's disease Cell Death Differ 12 1202 1204 10.1038/sj.cdd.4401705
125. C Wang HS Ko B Thomas 2005 Stress-induced alterations in parkin solubility promote parkin aggregation and compromise parkin's protective function Hum Mol Genet 14 3885 3897 10.1093/hmg/ddi413
126. ES Wong JM Tan C Wang 2007 Relative sensitivity of parkin and other cysteine-containing enzymes to stress-induced solubility alterations J Biol Chem 282 12310 12318
127. MJ LaVoie GP Cortese BL Ostaszewski MG Schlossmacher 2007 The effects of oxidative stress on parkin and other E3 ligases J Neurochem 103 2354 2368 10.1111/j.1471-4159.2007.04911.x
128. MJ LaVoie BL Ostaszewski A Weihofen 2005 Dopamine covalently modifies and functionally inactivates parkin Nat Med 11 1214 1221 10.1038/nm1314
129. MJ LaVoie TG Hastings 1999 Peroxynitrite- and nitrite-induced oxidation of dopamine: implications for nitric oxide in dopaminergic cell loss J Neurochem 73 2546 2554 10.1046/j.1471-4159.1999.0732546.x
130. DW Andrews AE Johnson 1996 The translocon: more than a hole in the ER membrane? Trends Biochem Sci 21 365 369
131. C Sidrauski R Chapman P Walter 1998 The unfolded protein response: an intracellular signalling pathway with many surprising features Trends Cell Biol 8 245 249 10.1016/S0962-8924(98)01267-7
132. E Szegezdi SE Logue AM Gorman A Samali 2006 Mediators of endoplasmic reticulum stress-induced apoptosis EMBO Rep 7 880 885 10.1038/sj.embor.7400779
133. L Ellgaard M Molinari A Helenius 1999 Setting the standards: quality control in the secretory pathway Science 286 1882 1888 10.1126/science.286.5446. 1882
134. RJ Kaufman 1999 Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls Genes Dev 13 1211 1233 10.1101/gad.13.10.1211
135. K Mori 2000 Tripartite management of unfolded proteins in the endoplasmic reticulum Cell 101 451 454 10.1016/S0092-8674(00)80855-7
136. C Patil P Walter 2001 Intracellular signaling from the endoplasmic reticulum to the nucleus: the unfolded protein response in yeast and mammals Curr Opin Cell Biol 13 349 355 10.1016/S0955-0674(00)00219-2
137. H Yoshida T Matsui A Yamamoto 2001 XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor Cell 107 881 891 10.1016/S0092-8674(01)00611-0
138. MM Lyles HF Gilbert 1991 Catalysis of the oxidative folding of ribonuclease A by protein disulfide isomerase: dependence of the rate on the composition of the redox buffer Biochemistry 30 613 619 10.1021/bi00217a004
139. JC Edman L Ellis RW Blacher 1985 Sequence of protein disulphide isomerase and implications of its relationship to thioredoxin Nature 317 267 270 10.1038/317267a0
140. K Vuori T Pihlajaniemi R Myllyla KI Kivirikko 1992 Site-directed mutagenesis of human protein disulphide isomerase: effect on the assembly, activity and endoplasmic reticulum retention of human prolyl 4-hydroxylase in Spodoptera frugiperda insect cells EMBO J 11 4213 4217
141. L Ellgaard LW Ruddock 2005 The human protein disulphide isomerase family: substrate interactions and functional properties EMBO Rep 6 28 32 10.1038/sj.embor.7400311
142. CW Gruber M Cemazar B Heras 2006 Protein disulfide isomerase: the structure of oxidative folding Trends Biochem Sci 31 455 464 10.1016/j.tibs.2006.06.001
143. G Tian S Xiang R Noiva 2006 The crystal structure of yeast protein disulfide isomerase suggests cooperativity between its active sites Cell 124 61 73 10.1016/j.cell.2005.10.044
144. P Klappa LW Ruddock NJ Darby RB Freedman 1998 The b' domain provides the principal peptide-binding site of protein disulfide isomerase but all domains contribute to binding of misfolded proteins EMBO J 17 927 935 10.1093/emboj/17.4.927
145. KJ Conn W Gao A McKee 2004 Identification of the protein disulfide isomerase family member PDIp in experimental Parkinson's disease and Lewy body pathology Brain Res 1022 164 172 10.1016/j.brainres.2004.07.026
146. C Hetz M Russelakis-Carneiro S Walchli 2005 The disulfide isomerase Grp58 is a protective factor against prion neurotoxicity J Neurosci 25 2793 2802 10.1523/JNEUROSCI.4090-04.2005
147. R Ushioda J Hoseki K Araki 2008 ERdj5 is required as a disulfide reductase for degradation of misfolded proteins in the ER Science 321 569 572 10.1126/science.1159293
148. BR Hu ME Martone YZ Jones CL Liu 2000 Protein aggregation after transient cerebral ischemia J Neurosci 20 3191 3199
149. RV Rao DE Bredesen 2004 Misfolded proteins, endoplasmic reticulum stress and neurodegeneration Curr Opin Cell Biol 16 653 662 10.1016/j.ceb.2004.09.012
150. JD Atkin MA Farg BJ Turner 2006 Induction of the unfolded protein response in familial amyotrophic lateral sclerosis and association of protein-disulfide isomerase with superoxide dismutase 1 J Biol Chem 281 30152 30165 10.1074/jbc.M603393200
151. S Tanaka T Uehara Y Nomura 2000 Up-regulation of protein-disulfide isomerase in response to hypoxia/brain ischemia and its protective effect against apoptotic cell death J Biol Chem 275 10388 10393 10.1074/jbc.275.14. 10388
152. HS Ko T Uehara Y Nomura 2002 Role of ubiquitin associated with protein-disulfide isomerase in the endoplasmic reticulum in stress-induced apoptotic cell death J Biol Chem 277 35386 35392 10.1074/jbc.M203412200
153. T Gotoh S Oyadomari K Mori M Mori 2002 Nitric oxide-induced apoptosis in RAW 264.7 macrophages is mediated by endoplasmic reticulum stress pathway involving ATF6 and CHOP J Biol Chem 277 12343 12350 10.1074/jbc.M107988200
154. S Oyadomari K Takeda M Takiguchi 2001 Nitric oxide-induced apoptosis in pancreatic beta cells is mediated by the endoplasmic reticulum stress pathway Proc Natl Acad Sci USA 98 10845 10850 10.1073/pnas.191207498
155. MT Forrester M Benhar JS Stamler 2006 Nitrosative stress in the ER: a new role for S-nitrosylation in neurodegenerative diseases ACS Chem Biol 1 355 358 10.1021/cb600244c
156. L Xu JP Eu G Meissner JS Stamler 1998 Activation of the cardiac calcium release channel (ryanodine receptor) by poly-S-nitrosylation Science 279 234 237 10.1126/science.279.5348.234
157. L Tao X Jiao E Gao 2006 Nitrative inactivation of thioredoxin-1 and its role in postischemic myocardial apoptosis Circulation 114 1395 1402 10.1161/CIRCULATIONAHA.106.625061
158. P Aracena-Parks SA Goonasekera CP Gilman 2006 Identification of cysteines involved in s-nitrosylation, s-glutathionylation, and oxidation to disulfides in ryanodine receptor type 1 J Biol Chem 281 40354 40368 10.1074/jbc.M600876200
159. A Martinez-Ruiz L Villanueva C Gonzalez de Orduna 2005 S-nitrosylation of Hsp90 promotes the inhibition of its ATPase and endothelial nitric oxide synthase regulatory activities Proc Natl Acad Sci USA 102 8525 8530 10.1073/pnas.0407294102
160. J Kakimura Y Kitamura K Takata 2002 Microglial activation and amyloid-beta clearance induced by exogenous heat-shock proteins FASEB J 16 601 603
161. F Dou WJ Netzer K Tanemura 2003 Chaperones increase association of tau protein with microtubules Proc Natl Acad Sci USA 100 721 726 10.1073/pnas.242720499
162. DA Gray M Tsirigotis J Woulfe 2003 Ubiquitin, proteasomes, and the aging brain Sci Aging Knowl Environ 2003 RE6
163. M Paz Gavilan J Vela A Castano 2006 Cellular environment facilitates protein accumulation in aged rat hippocampus Neurobiol Aging 27 973 982 10.1016/j.neurobiolaging.2005.05.010
164. K Ditzler 1991 Efficacy and tolerability of memantine in patients with dementia syndrome. A double-blind, placebo controlled trial Arzneimittelforschung 41 773 780
165. WW Fleischhacker A Buchgeher H Schubert 1986 Memantine in the treatment of senile dementia of the Alzheimer type Prog Neuropsychopharmacol Biol Psychiatry 10 87 93 10.1016/0278-5846(86)90047-3
166. CG Parsons W Danysz G Quack 1999 Memantine is a clinically well tolerated N-methyl-D-aspartate (NMDA) receptor antagonist-a review of preclinical data Neuropharmacology 38 735 767 10.1016/S0028-3908(99)00019-2
167. HS Chen JW Pellegrini SK Aggarwal 1992 Open-channel block of N-methyl-D-aspartate (NMDA) responses by memantine: therapeutic advantage against NMDA receptor-mediated neurotoxicity J Neurosci 12 4427 4436
168. HS Chen YF Wang PV Rayudu 1998 Neuroprotective concentrations of the N-methyl-D-aspartate open-channel blocker memantine are effective without cytoplasmic vacuolation following post-ischemic administration and do not block maze learning or long-term potentiation Neuroscience 86 1121 1132 10.1016/S0306-4522(98)00163-8
169. SA Lipton 1992 Memantine prevents HIV coat protein-induced neuronal injury in vitro Neurology 42 1403 1405
170. NN Osborne 1999 Memantine reduces alterations to the mammalian retina, in situ, induced by ischemia Vis Neurosci 16 45 52 10.1017/S0952523899161017
171. Lipton SA, Wang YF (1996) NO-related species can protect from focal cerebral ischemia/reperfusion. In: Krieglstein J, Oberpichler-Schwenk H (eds) Pharmacology of cerebral ischemia. Wissenschaftliche Verlagsgesellschaft, Stuttgart, pp 183-191
172. D Zurakowski CK Vorwerk M Gorla 1998 Nitrate therapy may retard glaucomatous optic neuropathy, perhaps through modulation of glutamate receptors Vis Res 38 1489 1494 10.1016/S0042-6989(98)00003-0
173. H Takahashi Y Shin SJ Cho 2007 Hypoxia enhances S-nitrosylation-mediated NMDA receptor inhibition via a thiol oxygen sensor motif Neuron 53 53 64 10.1016/j.neuron.2006.11.023
174. DC Rubinsztein 2006 The roles of intracellular protein-degradation pathways in neurodegeneration Nature 443 780 786 10.1038/nature05291