Preventing Ca2+-mediated nitrosative stress in neurodegenerative diseases: Possible pharmacological strategies

Cell Calcium

Volumn 47, Issue 2, 2010, Pages 190-197

  Nakamura, Tomohiro ^a   Lipton, Stuart A ^a  

^a BURNHAM INSTITUTE   (United States)

Author keywords

Memantine; Mitochondrial fission; Molecular chaperone; Neurodegeneration; Protein misfolding; Reactive nitrogen species; S Nitrosylation; Ubiquitin proteasome system

Indexed keywords

ALPHA SYNUCLEIN; AMPA RECEPTOR; CALCIUM ION; CARNOSIC ACID; CATECHOL DERIVATIVE; CHAPERONE; CURCUMIN; CYTOCHROME C OXIDASE; DIZOCILPINE; GELATINASE B; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; GUANYLATE CYCLASE; HEAT SHOCK PROTEIN 70; HEME OXYGENASE 1; KAINIC ACID RECEPTOR; KELCH LIKE ECH ASSOCIATED PROTEIN 1; MEMANTINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; NEURITE PROMOTING FACTOR; NITRIC OXIDE; NITROMEMANTINE; PARKIN; PROTEIN DISULFIDE ISOMERASE; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); TRANSCRIPTION FACTOR NRF2; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; UNINDEXED DRUG; AMINO ACID RECEPTOR BLOCKING AGENT; CALCIUM;

ALZHEIMER DISEASE; ANTIOXIDANT ACTIVITY; AUTOSOMAL DOMINANT OPTIC ATROPHY; BRAIN ISCHEMIA; CALCIUM SIGNALING; CALCIUM TRANSPORT; CLINICAL TRIAL; DEGENERATIVE DISEASE; DEMENTIA; DRUG SELECTIVITY; DRUG TARGETING; DRUG TOLERABILITY; GENE MUTATION; HEREDITARY MOTOR SENSORY NEUROPATHY; HUMAN; HUNTINGTON CHOREA; NERVE CELL NECROSIS; NEUROPROTECTION; NITROSATIVE STRESS; NITROSYLATION; NONHUMAN; OXIDATIVE STRESS; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN FOLDING; PROTEIN GLYCOSYLATION; REVIEW; STROKE; ANIMAL; APOPTOSIS; METABOLISM; MITOCHONDRION; NERVE CELL; NITROSATION; PATHOLOGY;

ANIMALS; APOPTOSIS; CALCIUM; CALCIUM SIGNALING; EXCITATORY AMINO ACID ANTAGONISTS; HUMANS; MEMANTINE; MITOCHONDRIA; NEURODEGENERATIVE DISEASES; NEURONS; NITRIC OXIDE; NITROSATION; OXIDATIVE STRESS; PROTEIN FOLDING; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 77549085875     PISSN: 01434160     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ceca.2009.12.009     Document Type: Review

References (86)

1. Beal M.F. Experimental models of Parkinson's disease. Nat. Rev. Neurosci. 2 (2001) 325-334
2. Lipton S.A., and Rosenberg P.A. Excitatory amino acids as a final common pathway for neurologic disorders. N. Engl. J. Med. 330 (1994) 613-622
3. Lipton S.A. Paradigm shift in neuroprotection by NMDA receptor blockade: memantine and beyond. Nat. Rev. Drug Discov. 5 (2006) 160-170
4. Garthwaite J., Charles S.L., and Chess-Williams R. Endothelium-derived relaxing factor release on activation of NMDA receptors suggests role as intercellular messenger in the brain. Nature 336 (1988) 385-388
5. Lipton S.A., Choi Y.B., Pan Z.H., et al. A redox-based mechanism for the neuroprotective and neurodestructive effects of nitric oxide and related nitroso-compounds. Nature 364 (1993) 626-632
6. Muchowski P.J., and Wacker J.L. Modulation of neurodegeneration by molecular chaperones. Nat. Rev. Neurosci. 6 (2005) 11-22
7. Ciechanover A., and Brundin P. The ubiquitin proteasome system in neurodegenerative diseases: sometimes the chicken, sometimes the egg. Neuron 40 (2003) 427-446
8. Zhang K., and Kaufman R.J. The unfolded protein response: a stress signaling pathway critical for health and disease. Neurology 66 (2006) S102-S109
9. Chung K.K., Thomas B., Li X., et al. S-Nitrosylation of parkin regulates ubiquitination and compromises parkin's protective function. Science 304 (2004) 1328-1331
10. Yao D., Gu Z., Nakamura T., et al. Nitrosative stress linked to sporadic Parkinson's disease: S-nitrosylation of parkin regulates its E3 ubiquitin ligase activity. Proc Natl Acad Sci USA 101 (2004) 10810-10814
11. Uehara T., Nakamura T., Yao D., et al. S-Nitrosylated protein-disulphide isomerase links protein misfolding to neurodegeneration. Nature 441 (2006) 513-517
12. Lipton S.A. Pathologically activated therapeutics for neuroprotection. Nat. Rev. Neurosci. 8 (2007) 803-808
13. Papadia S., Soriano F.X., Leveille F., et al. Synaptic NMDA receptor activity boosts intrinsic antioxidant defenses. Nat. Neurosci. 11 (2008) 476-487
14. Okamoto S., Pouladi M.A., Talantova M., et al. Balance between synaptic versus extrasynaptic NMDA receptor activity influences inclusions and neurotoxicity of mutant Huntingin. Nat. Med. 15 (2009) 1407-1413
15. Ankarcrona M., Dypbukt J.M., Bonfoco E., et al. Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function. Neuron 15 (1995) 961-973
16. Bonfoco E., Krainc D., Ankarcrona M., Nicotera P., and 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. Proc. Natl. Acad. Sci. U.S.A. 92 (1995) 7162-7166
17. Budd S.L., Tenneti L., Lishnak T., and Lipton S.A. Mitochondrial, extramitochondrial apoptotic signaling pathways in cerebrocortical neurons. Proc. Natl. Acad. Sci. U.S.A. 97 (2000) 6161-6166
18. 2+ of NMDA responses in spinal cord neurones. Nature 309 (1984) 261-263
19. Dawson V.L., Dawson T.M., London E.D., Bredt D.S., and Snyder S.H. Nitric oxide mediates glutamate neurotoxicity in primary cortical cultures. Proc. Natl. Acad. Sci. U.S.A. 88 (1991) 6368-6371
20. Olney J.W. Brain lesions, obesity, and other disturbances in mice treated with monosodium glutamate. Science 164 (1969) 719-721
21. Chen H.S., and Lipton S.A. The chemical biology of clinically tolerated NMDA receptor antagonists. J. Neurochem. 97 (2006) 1611-1626
22. Abu-Soud H.M., and Stuehr D.J. Nitric oxide synthases reveal a role for calmodulin in controlling electron transfer. Proc. Natl. Acad. Sci. U.S.A. 90 (1993) 10769-10772
23. Bredt D.S., Hwang P.M., Glatt C.E., Lowenstein C., Reed R.R., and Snyder S.H. Cloned and expressed nitric oxide synthase structurally resembles cytochrome P-450 reductase. Nature 351 (1991) 714-718
24. Betarbet R., Sherer T.B., MacKenzie G., Garcia-Osuna M., Panov A.V., and Greenamyre J.T. Chronic systemic pesticide exposure reproduces features of Parkinson's disease. Nat. Neurosci. 3 (2000) 1301-1306
25. Isaacs A.M., Senn D.B., Yuan M., Shine J.P., and Yankner B.A. Acceleration of amyloid beta-peptide aggregation by physiological concentrations of calcium. J. Biol. Chem. 281 (2006) 27916-27923
26. Hess D.T., Matsumoto A., Kim S.O., Marshall H.E., and Stamler J.S. Protein S-nitrosylation: purview and parameters. Nat. Rev. Mol. Cell Biol. 6 (2005) 150-166
27. Gu Z., Kaul M., Yan B., et al. S-Nitrosylation of matrix metalloproteinases: signaling pathway to neuronal cell death. Science 297 (2002) 1186-1190
28. Hara M.R., Agrawal N., Kim S.F., et al. S-Nitrosylated GAPDH initiates apoptotic cell death by nuclear translocation following Siah1 binding. Nat. Cell. Biol. 7 (2005) 665-674
29. Stamler J.S., Lamas S., and Fang F.C. Nitrosylation the prototypic redox-based signaling mechanism. Cell 106 (2001) 675-683
30. Houk K.N., Hietbrink B.N., Bartberger M.D., et al. Nitroxyl disulfides, novel intermediates in transnitrosation reactions. J. Am. Chem. Soc. 125 (2003) 6972-6976
31. Lipton S.A., Nakamura T., Yao D., Shi Z.Q., Uehara T., and Gu Z. Comment on "S-nitrosylation of parkin regulates ubiquitination and compromises parkin's protective function". Science 308 (2005) 1870 (author reply 1870)
32. Cleeter M.W., Cooper J.M., Darley-Usmar V.M., Moncada S., and Schapira A.H. Reversible inhibition of cytochrome c oxidase, the terminal enzyme of the mitochondrial respiratory chain, by nitric oxide. Implications for neurodegenerative diseases. FEBS Lett. 345 (1994) 50-54
33. Clementi E., Brown G.C., Feelisch M., and Moncada S. Persistent inhibition of cell respiration by nitric oxide: crucial role of S-nitrosylation of mitochondrial complex I and protective action of glutathione. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 7631-7636
34. Barsoum M.J., Yuan H., Gerencser A.A., et al. Nitric oxide-induced mitochondrial fission is regulated by dynamin-related GTPases in neurons. EMBO J. 25 (2006) 3900-3911
35. Bossy-Wetzel E., and Lipton S.A. Nitric oxide signaling regulates mitochondrial number and function. Cell Death Differ. 10 (2003) 757-760
36. Yuan H., Gerencser A.A., Liot G., et al. Mitochondrial fission is an upstream and required event for bax foci formation in response to nitric oxide in cortical neurons. Cell Death Differ. 14 (2007) 462-471
37. Cho D.H., Nakamura T., Fang J., et al. S-Nitrosylation of Drp1 mediates beta-amyloid-related mitochondrial fission and neuronal injury. Science 324 (2009) 102-105
38. Cookson M.R. The biochemistry of Parkinson's disease. Annu. Rev. Biochem. 74 (2005) 29-52
39. McNaught K.S., Perl D.P., Brownell A.L., and Olanow C.W. Systemic exposure to proteasome inhibitors causes a progressive model of Parkinson's disease. Ann. Neurol. 56 (2004) 149-162
40. Auluck P.K., Chan H.Y., Trojanowski J.Q., Lee V.M., and Bonini N.M. Chaperone suppression of alpha-synuclein toxicity in a Drosophila model for Parkinson's disease. Science 295 (2002) 865-868
41. Ross C.A., and Pickart C.M. The ubiquitin-proteasome pathway in Parkinson's disease and other neurodegenerative diseases. Trends Cell Biol. 14 (2004) 703-711
42. Marin I., and Ferrus A. 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 (2002) 2039-2050
43. Lim K.L., Chew K.C., Tan J.M., et al. Parkin mediates nonclassical, proteasomal-independent ubiquitination of synphilin-1: implications for Lewy body formation. J. Neurosci. 25 (2005) 2002-2009
44. Lim K.L., Dawson V.L., and Dawson T.M. Parkin-mediated lysine 63-linked polyubiquitination: a link to protein inclusions formation in Parkinson's and other conformational diseases?. Neurobiol. Aging 27 (2006) 524-529
45. Lyles M.M., and 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 30 (1991) 613-619
46. Conn K.J., Gao W., McKee A., et al. Identification of the protein disulfide isomerase family member PDIp in experimental Parkinson's disease and Lewy body pathology. Brain Res. 1022 (2004) 164-172
47. Forrester M.T., Benhar M., and Stamler J.S. Nitrosative stress in the ER: a new role for S-nitrosylation in neurodegenerative diseases. ACS Chem. Biol. 1 (2006) 355-358
48. Xu L., Eu J.P., Meissner G., and Stamler J.S. Activation of the cardiac calcium release channel (ryanodine receptor) by poly-S-nitrosylation. Science 279 (1998) 234-237
49. Paz Gavilan M., Vela J., Castano A., et al. Cellular environment facilitates protein accumulation in aged rat hippocampus. Neurobiol. Aging 27 (2006) 973-982
50. Chen H., and Chan D.C. Critical dependence of neurons on mitochondrial dynamics. Curr. Opin. Cell Biol. 18 (2006) 453-459
51. Li H., Chen Y., Jones A.F., et al. Bcl-xL induces Drp1-dependent synapse formation in cultured hippocampal neurons. Proc. Natl. Acad. Sci. U.S.A. 105 (2008) 2169-2174
52. Li Z., Okamoto K., Hayashi Y., and Sheng M. The importance of dendritic mitochondria in the morphogenesis and plasticity of spines and synapses. Cell 119 (2004) 873-887
53. Youle R.J., and Karbowski M. Mitochondrial fission in apoptosis. Nat. Rev. Mol. Cell Biol. 6 (2005) 657-663
54. Kijima K., Numakura C., Izumino H., et al. Mitochondrial GTPase mitofusin 2 mutation in Charcot-Marie-Tooth neuropathy type 2A. Hum. Genet. 116 (2005) 23-27
55. Zuchner S., Mersiyanova I.V., Muglia M., et al. Mutations in the mitochondrial GTPase mitofusin 2 cause Charcot-Marie-Tooth neuropathy type 2A. Nat. Genet. 36 (2004) 449-451
56. Delettre C., Lenaers G., Griffoin J.M., et al. Nuclear gene OPA1, encoding a mitochondrial dynamin-related protein, is mutated in dominant optic atrophy. Nat. Genet. 26 (2000) 207-210
57. Waterham H.R., Koster J., van Roermund C.W., Mooyer P.A., Wanders R.J., and Leonard J.V. A lethal defect of mitochondrial and peroxisomal fission. N. Engl. J. Med. 356 (2007) 1736-1741
58. Wasiak S., Zunino R., and McBride H.M. Bax/Bak promote sumoylation of DRP1 and its stable association with mitochondria during apoptotic cell death. J. Cell Biol. 177 (2007) 439-450
59. Breckenridge D.G., Kang B.H., Kokel D., Mitani S., Staehelin L.A., and Xue D. Caenorhabditis elegans drp-1 and fis-2 regulate distinct cell-death execution pathways downstream of ced-3 and independent of ced-9. Mol. Cell 31 (2008) 586-597
60. Karbowski M., Neutzner A., and Youle R.J. The mitochondrial E3 ubiquitin ligase MARCH5 is required for Drp1 dependent mitochondrial division. J. Cell Biol. 178 (2007) 71-84
61. Nakamura N., Kimura Y., Tokuda M., Honda S., and Hirose S. MARCH-V is a novel mitofusin 2- and Drp1-binding protein able to change mitochondrial morphology. EMBO Rep. 7 (2006) 1019-1022
62. Yonashiro R., Ishido S., Kyo S., et al. A novel mitochondrial ubiquitin ligase plays a critical role in mitochondrial dynamics. EMBO J. 25 (2006) 3618-3626
63. Chang C.R., and Blackstone C. Cyclic AMP-dependent protein kinase phosphorylation of Drp1 regulates its GTPase activity and mitochondrial morphology. J. Biol. Chem. 282 (2007) 21583-21587
64. Cribbs J.T., and Strack S. Reversible phosphorylation of Drp1 by cyclic AMP-dependent protein kinase and calcineurin regulates mitochondrial fission and cell death. EMBO Rep. 8 (2007) 939-944
65. Taguchi N., Ishihara N., Jofuku A., Oka T., and Mihara K. Mitotic phosphorylation of dynamin-related GTPase Drp1 participates in mitochondrial fission. J. Biol. Chem. 282 (2007) 11521-11529
66. Low H.H., and Lowe J. A bacterial dynamin-like protein. Nature 444 (2006) 766-769
67. Zhu P.P., Patterson A., Stadler J., Seeburg D.P., Sheng M., and Blackstone C. Intra- and intermolecular domain interactions of the C-terminal GTPase effector domain of the multimeric dynamin-like GTPase Drp1. J. Biol. Chem. 279 (2004) 35967-35974
68. Ramachandran R., Surka M., Chappie J.S., et al. The dynamin middle domain is critical for tetramerization and higher-order self-assembly. EMBO J. 26 (2007) 559-566
69. Pitts K.R., McNiven M.A., and Yoon Y. Mitochondria-specific function of the dynamin family protein DLP1 is mediated by its C-terminal domains. J. Biol. Chem. 279 (2004) 50286-50294
70. Wang X., Su B., Lee H.G., et al. Impaired balance of mitochondrial fission and fusion in Alzheimer's disease. J. Neurosci. 29 (2009) 9090-9103
71. Murphy T.H., Schnaar R.L., and Coyle J.T. Immature cortical neurons are uniquely sensitive to glutamate toxicity by inhibition of cystine uptake. Faseb J. 4 (1990) 1624-1633
72. Chen H.S., Pellegrini J.W., Aggarwal S.K., et al. Open-channel block of N-methyl-d-aspartate (NMDA) responses by memantine: therapeutic advantage against NMDA receptor-mediated neurotoxicity. J. Neurosci. 12 (1992) 4427-4436
73. Satoh T., and Lipton S.A. Redox regulation of neuronal survival mediated by electrophilic compounds. Trends Neurosci. 30 (2007) 37-45
74. Kraft A.D., Johnson D.A., and 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. J. Neurosci. 24 (2004) 1101-1112
75. Satoh T., Okamoto S.I., Cui J., et al. Activation of the Keap1/Nrf2 pathway for neuroprotection by electrophilic [correction of electrophillic] phase II inducers. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 768-773
76. Itoh K., Tong K.I., and Yamamoto M. Molecular mechanism activating Nrf2-Keap1 pathway in regulation of adaptive response to electrophiles. Free Radic. Biol. Med. 36 (2004) 1208-1213
77. Padmanabhan B., Tong K.I., Ohta T., et al. Structural basis for defects of Keap1 activity provoked by its point mutations in lung cancer. Mol. Cell 21 (2006) 689-700
78. Li C.Q., Kim M.Y., Godoy L.C., Thiantanawat A., Trudel L.J., and Wogan G.N. Nitric oxide activation of Keap1/Nrf2 signaling in human colon carcinoma cells. Proc. Natl. Acad. Sci. U.S.A. 106 (2009) 14547-14551
79. Yazawa K., Kihara T., Shen H., Shimmyo Y., Niidome T., and Sugimoto H. Distinct mechanisms underlie distinct polyphenol-induced neuroprotection. FEBS Lett. 580 (2006) 6623-6628
80. Nakamura Y., Kumagai T., Yoshida C., et al. Pivotal role of electrophilicity in glutathione S-transferase induction by tert-butylhydroquinone. Biochemistry 42 (2003) 4300-4309
81. Lipton S.A. Turning down, but not off. Nature 428 (2004) 473
82. Ahlgren-Beckendorf J.A., Reising A.M., Schander M.A., Herdler J.W., and Johnson J.A. Coordinate regulation of NAD(P)H:quinone oxidoreductase and glutathione-S-transferases in primary cultures of rat neurons and glia: role of the antioxidant/electrophile responsive element. Glia 25 (1999) 131-142
83. Kosaka K., and Yokoi T. Carnosic acid, a component of rosemary (Rosmarinus officinalis L.), promotes synthesis of nerve growth factor in T98G human glioblastoma cells. Biol. Pharm. Bull. 26 (2003) 1620-1622
84. Aruoma O.I., Halliwell B., Aeschbach R., and Loligers J. Antioxidant and pro-oxidant properties of active rosemary constituents: carnosol and carnosic acid. Xenobiotica 22 (1992) 257-268
85. Satoh T., Kosaka K., Itoh K., et al. 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. J. Neurochem. 104 (2008) 1116-1131
86. Jenner P. Oxidative stress and Parkinson's disease. Handb. Clin. Neurol. 83 (2007) 507-520