Table of Contents Author Guidelines Submit a Manuscript
Mediators of Inflammation
Volume 2012, Article ID 401264, 12 pages
http://dx.doi.org/10.1155/2012/401264
Review Article

Oxidative Stress and Microglial Cells in Parkinson's Disease

North Carolina Oral Health Institute, The University of North Carolina at Chapel Hill, CB#7454, Chapel Hill, NC 27599-7454, USA

Received 4 November 2011; Revised 3 January 2012; Accepted 9 January 2012

Academic Editor: Luc Vallières

Copyright © 2012 Lynda J. Peterson and Patrick M. Flood. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. K. A. Jellinger, “The pathology of Parkinson's disease,” Advances in Neurology, vol. 86, pp. 55–72, 2001. View at Google Scholar · View at Scopus
  2. M. H. Polymeropoulos, C. Lavedan, E. Leroy et al., “Mutation in the α-synuclein gene identified in families with Parkinson's disease,” Science, vol. 276, no. 5321, pp. 2045–2047, 1997. View at Publisher · View at Google Scholar · View at Scopus
  3. M. Sun, J. C. Latourelle, G. F. Wooten et al., “Influence of heterozygosity for Parkin mutation on onset age in familial parkinson disease: the genePD study,” Archives of Neurology, vol. 63, no. 6, pp. 826–832, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  4. V. Bonifati, Y. H. Wu-Chou, D. Schweiger, A. Di Fonzo, C. S. Lu, and B. Oostra, “LRRK2 mutation analysis in parkinson disease families with evidence of linkage to PARK8,” Neurology, vol. 70, no. 24, pp. 2348–2349, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  5. Y. H. Weng, Y. H. W. Chou, W. S. Wu et al., “PINK1 mutation in Taiwanese early-onset parkinsonism: clinical, genetic, and dopamine transporter studies,” Journal of Neurology, vol. 254, no. 10, pp. 1347–1355, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  6. P. M. Abou-Sleiman, D. G. Healy, N. Quinn, A. J. Lees, and N. W. Wood, “The role of pathogenic DJ-1 mutations in Parkinson's disease,” Annals of Neurology, vol. 54, no. 3, pp. 283–286, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  7. M. S. Goldberg, A. Pisani, M. Haburcak et al., “Nigrostriatal dopaminergic deficits and hypokinesia caused by inactivation of the familial parkinsonism-linked gene DJ-1,” Neuron, vol. 45, no. 4, pp. 489–496, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  8. M. Alam and W. J. Schmidt, “Rotenone destroys dopaminergic neurons and induces parkinsonian symptoms in rats,” Behavioural Brain Research, vol. 136, no. 1, pp. 317–324, 2002. View at Publisher · View at Google Scholar · View at Scopus
  9. A. D. Ebert, J. H. Hoo, and M. C. Bohn, “Progressive degeneration of dopamine neurons in 6-hydroxydopamine rat model of Parkinson's disease does not involve activation of caspase-9 and caspase-3,” Journal of Neuroscience Research, vol. 86, no. 2, pp. 317–325, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  10. W. Meissner, C. Prunier, D. Guilloteau, S. Chalon, C. E. Gross, and E. Bezard, “Time-course of nigrostriatal degeneration in a progressive MPTP-lesioned macaque model of Parkinson's disease,” Molecular Neurobiology, vol. 28, no. 3, pp. 209–218, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  11. E. C. Hirsch, S. Hunot, and A. Hartmann, “Neuroinflammatory processes in Parkinson's disease,” Parkinsonism and Related Disorders, vol. 11, supplement 1, pp. S9–S15, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  12. R. L. Mosley, E. J. Benner, I. Kadiu et al., “Neuroinflammation, oxidative stres and the pathogenesis of Parkinson's disease,” Clinical Neurosicence Research, vol. 6, no. 5, pp. 261–281, 2006. View at Publisher · View at Google Scholar · View at PubMed
  13. A. L. Bartels and K. L. Leenders, “Neuroinflammation in the pathophysiology of Parkinson's disease: evidence from animal models to human in vivo studies with [11C]-PK11195 PET,” Movement Disorders, vol. 22, no. 13, pp. 1852–1856, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  14. S. K. Van Den Eeden, C. M. Tanner, A. L. Bernstein et al., “Incidence of Parkinson's disease: variation by age, gender, and race/ethnicity,” American Journal of Epidemiology, vol. 157, no. 11, pp. 1015–1022, 2003. View at Google Scholar · View at Scopus
  15. J. H. Baik, R. Picetti, A. Saiardi et al., “Parkinsonian-like locomotor impairment in mice lacking dopamine D2 receptors,” Nature, vol. 377, no. 6548, pp. 424–428, 1995. View at Google Scholar · View at Scopus
  16. Y. Wang, R. Xu, T. Sasaoka, S. Tonegawa, M. P. Kung, and E. B. Sankoorikal, “Dopamine D2 long receptor-deficient mice display alterations in striatum-dependent functions,” Journal of Neuroscience, vol. 20, no. 22, pp. 8305–8314, 2000. View at Google Scholar · View at Scopus
  17. S. C. Fowler, T. J. Zarcone, E. Vorontsova, and R. Chen, “Motor and associative deficits in D2 dopamine receptor knockout mice,” International Journal of Developmental Neuroscience, vol. 20, no. 3–5, pp. 309–321, 2002. View at Publisher · View at Google Scholar · View at Scopus
  18. P. Jenner, “Dopamine agonists, receptor selectivity and dyskinesia induction in Parkinson's disease,” Current Opinion in Neurology, vol. 16, supplement 1, pp. S3–S7, 2003. View at Google Scholar · View at Scopus
  19. B. Liu and J. S. Hong, “Role of microglia in inflammation-mediated neurodegenerative diseases: mechanisms and strategies for therapeutic intervention,” Journal of Pharmacology and Experimental Therapeutics, vol. 304, no. 1, pp. 1–7, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  20. P. T. Nelson, L. A. Soma, and E. Lavi, “Microglia in diseases of the central nervous system,” Annals of Medicine, vol. 34, no. 7-8, pp. 491–500, 2002. View at Google Scholar · View at Scopus
  21. G. J. Guillemin and B. J. Brew, “Microglia, macrophages, perivascular macrophages, and pericytes: a review of function and identification,” Journal of Leukocyte Biology, vol. 75, no. 3, pp. 388–397, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  22. W. Dauer and S. Przedborski, “Parkinson's disease: mechanisms and models,” Neuron, vol. 39, no. 6, pp. 889–909, 2003. View at Publisher · View at Google Scholar · View at Scopus
  23. H. M. Gao, P. T. Kotzbauer, K. Uryu, S. Leight, J. Q. Trojanowski, and V. M. Y. Lee, “Neuroinflammation and oxidation/nitration of α-synuclein linked to dopaminergic neurodegeneration,” Journal of Neuroscience, vol. 28, no. 30, pp. 7687–7698, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  24. M. L. Block and J. S. Hong, “Chronic microglial activation and progressive dopaminergic neurotoxicity,” Biochemical Society Transactions, vol. 35, no. 5, pp. 1127–1132, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  25. A. Członkowska, M. Kohutnicka, I. Kurkowska-Jastrzȩbska, and A. Członkowski, “Microglial reaction in MPTP (1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine) induced Parkinson's disease mice model,” Neurodegeneration, vol. 5, no. 2, pp. 137–143, 1996. View at Publisher · View at Google Scholar · View at Scopus
  26. W. G. Kim, R. P. Mohney, B. Wilson, G. H. Jeohn, B. Liu, and J. S. Hong, “Regional difference in susceptibility to lipopolysaccharide-induced neurotoxicity in the rat brain: role of microglia,” Journal of Neuroscience, vol. 20, no. 16, pp. 6309–6316, 2000. View at Google Scholar · View at Scopus
  27. A. Ghosh, A. Roy, X. Liu et al., “Selective inhibition of NF-κB activation prevents dopaminergic neuronal loss in a mouse model of Parkinson's disease,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 47, pp. 18754–18759, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  28. F. Cicchetti, A. L. Brownell, K. Williams, Y. I. Chen, E. Livni, and O. Isacson, “Neuroinflammation of the nigrostriatal pathway during progressive 6-OHDA dopamine degeneration in rats monitored by immunohistochemistry and PET imaging,” European Journal of Neuroscience, vol. 15, no. 6, pp. 991–998, 2002. View at Publisher · View at Google Scholar · View at Scopus
  29. P. L. McGeer, S. Itagaki, B. E. Boyes, and E. G. McGeer, “Reactive microglia are positive for HLA-DR in the substantia nigra of Parkinson's and Alzheimer's disease brains,” Neurology, vol. 38, no. 8, pp. 1285–1291, 1988. View at Google Scholar · View at Scopus
  30. T. Nagatsu, M. Mogi, H. Ichinose, and A. Togari, “Changes in cytokines and neurotrophins in Parkinson's disease,” Journal of Neural Transmission, Supplement, no. 60, pp. 277–290, 2000. View at Google Scholar · View at Scopus
  31. M. Mogi, M. Harada, T. Kondob et al., “Interleukin-1β, interleukin-6, epidermal growth factor and transforming growth factor-α are elevated in the brain from parkinsonian patients,” Neuroscience Letters, vol. 180, no. 2, pp. 147–150, 1994. View at Publisher · View at Google Scholar · View at Scopus
  32. H. Bessler, R. Djaldetti, H. Salman, M. Bergman, and M. Djaldetti, “IL-1β, IL-2, IL-6 and TNF-α production by peripheral blood mononuclear cells from patients with Parkinson's disease,” Biomedicine and Pharmacotherapy, vol. 53, no. 3, pp. 141–145, 1999. View at Publisher · View at Google Scholar · View at Scopus
  33. G. A. Qureshi, S. Baig, I. Bednar, P. Sodersten, G. Forsberg, and A. Siden, “Increased cerebrospinal fluid concentration of nitrite ire Parkinson's disease,” NeuroReport, vol. 6, no. 12, pp. 1642–1644, 1995. View at Google Scholar · View at Scopus
  34. S. Hunot, F. Boissière, B. Faucheux et al., “Nitric oxide synthase and neuronal vulnerability in Parkinson's disease,” Neuroscience, vol. 72, no. 2, pp. 355–363, 1996. View at Publisher · View at Google Scholar · View at Scopus
  35. T. Nagatsu, M. Mogi, H. Ichinose, and A. Togari, “Cytokines in Parkinson's disease,” Journal of Neural Transmission, Supplement, no. 58, pp. 143–151, 2000. View at Google Scholar · View at Scopus
  36. M. E. Lull and M. L. Block, “Microglial activation and chronic neurodegeneration,” Neurotherapeutics, vol. 7, no. 4, pp. 354–365, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  37. B. Liu, H. M. Gao, J. Y. Wang, G. H. Jeohn, C. L. Cooper, and J. S. Hong, “Role of nitric oxide in inflammation-mediated neurodegeneration,” Annals of the New York Academy of Sciences, vol. 962, pp. 318–331, 2002. View at Google Scholar · View at Scopus
  38. V. Shukla, S. K. Mishra, and H. C. Pant, “Oxidative stress in neurodegeneration,” Advances in Pharmacological Sciences, vol. 2011, Article ID 572634, 13 pages, 2011. View at Publisher · View at Google Scholar · View at PubMed
  39. A. D. Kraft and G. Jean Harry, “Features of microglia and neuroinflammation relevant to environmental exposure and neurotoxicity,” International Journal of Environmental Research and Public Health, vol. 8, no. 7, pp. 2980–3018, 2011. View at Publisher · View at Google Scholar · View at PubMed
  40. U. K. Hanisch, “Microglia as a source and target of cytokines,” GLIA, vol. 40, no. 2, pp. 140–155, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  41. K. Heese, C. Hock, and U. Otten, “Inflammatory signals induce neurotrophin expression in human microglial cells,” Journal of Neurochemistry, vol. 70, no. 2, pp. 699–707, 1998. View at Google Scholar · View at Scopus
  42. N. P. Whitney, T. M. Eidem, H. Peng, Y. Huang, and J. C. Zheng, “Inflammation mediates varying effects in neurogenesis: relevance to the pathogenesis of brain injury and neurodegenerative disorders,” Journal of Neurochemistry, vol. 108, no. 6, pp. 1343–1359, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  43. K. Heese, B. L. Fiebich, J. Bauer, and U. Otten, “NF-κB modulates lipopolysaccharide-induced microglial nerve growth factor expression,” GLIA, vol. 22, no. 4, pp. 401–407, 1998. View at Publisher · View at Google Scholar · View at Scopus
  44. M. Yoneyama, T. Shiba, S. Hasebe, and K. Ogita, “Adult neurogenesis is regulated by endogenous factors produced during neurodegeneration,” Journal of Pharmacological Sciences, vol. 115, no. 4, pp. 425–432, 2011. View at Publisher · View at Google Scholar
  45. D. M. Bronstein, I. Perez-Otano, V. Sun et al., “Glia-dependent neurotoxicity and neuroprotection in mesencephalic cultures,” Brain Research, vol. 704, no. 1, pp. 112–116, 1995. View at Publisher · View at Google Scholar · View at Scopus
  46. E. Araki, C. Forster, J. M. Dubinsky, M. E. Ross, and C. Iadecola, “Cyclooxygenase-2 inhibitor NS-398 protects neuronal cultures from lipopolysaccharide-induced neurotoxicity,” Stroke, vol. 32, no. 10, pp. 2370–2375, 2001. View at Google Scholar · View at Scopus
  47. W. Zhang, T. Wang, Z. Pei et al., “Aggregated α-synuclein activates microglia: a process leading to disease progression in Parkinson's disease,” The FASEB Journal, vol. 19, no. 6, pp. 533–542, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  48. Y. Itzhak, J. L. Martin, and S. F. Ali, “Methamphetamine- and 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine- induced dopaminergic neurotoxicity in inducible nitric oxide synthase-deficient mice,” Synapse, vol. 34, no. 4, pp. 305–312, 1999. View at Publisher · View at Google Scholar · View at Scopus
  49. G. T. Liberatore, V. Jackson-Lewis, S. Vukosavic et al., “Inducible nitric oxide synthase stimulates dopaminergic neurodegeneration in the MPTP model of Parkinson disease,” Nature Medicine, vol. 5, no. 12, pp. 1403–1409, 1999. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  50. T. Dehmer, J. Lindenau, S. Haid, J. Dichgans, and J. B. Schulz, “Deficiency of inducible nitric oxide synthase protects against MPTP toxicity in vivo,” Journal of Neurochemistry, vol. 74, no. 5, pp. 2213–2216, 2000. View at Google Scholar · View at Scopus
  51. Y. Du, Z. Ma, S. Lin et al., “Minocycline prevents nigrostriatal dopaminergic neurodegeneration in the MPTP model of Parkinson's disease,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 25, pp. 14669–14674, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  52. S. A. Factor, J. Sanchez-Ramos, and W. J. Weiner, “Trauma as an etiology of parkinsonism: a historical review of the concept,” Movement Disorders, vol. 3, no. 1, pp. 30–36, 1988. View at Google Scholar · View at Scopus
  53. Z. Ling, D. A. Gayle, S. Y. Ma et al., “In utero bacterial endotoxin exposure causes loss of tyrosine hydroxylase neurons in the postnatal rat midbrain,” Movement Disorders, vol. 17, no. 1, pp. 116–124, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  54. A. S. Baldwin Jr., “The NF-κB and IκB proteins: new discoveries and insights,” Annual Review of Immunology, vol. 14, pp. 649–681, 1996. View at Google Scholar · View at Scopus
  55. A. S. Baldwin Jr., “Series introduction: the transcription factor NF-kappaB and human disease,” The Journal of Clinical Investigation, vol. 107, no. 1, pp. 3–6, 2001. View at Google Scholar
  56. E. M. Boyle Jr., J. C. Kovacich, C. A. Hebert et al., “Inhibition of interleukin-8 blocks myocardial ischemia-reperfusion injury,” Journal of Thoracic and Cardiovascular Surgery, vol. 116, no. 1, pp. 114–121, 1998. View at Publisher · View at Google Scholar · View at Scopus
  57. B. Chandrasekar and G. L. Freeman, “Induction of nuclear factor κB and activation protein 1 in postischemic myocardium,” FEBS Letters, vol. 401, no. 1, pp. 30–34, 1997. View at Publisher · View at Google Scholar · View at Scopus
  58. V. Jackson-Lewis and R. J. Smeyne, “MPTP and SNpc DA neuronal vulnerability: role of dopamine, superoxide and nitric oxide in neurotoxicity. Minireview,” Neurotoxicity Research, vol. 7, no. 3, pp. 193–201, 2005. View at Publisher · View at Google Scholar · View at Scopus
  59. Y. Liu, L. Qin, G. Li et al., “Dextromethorphan protects dopaminergic neurons against inflammation-mediated degeneration through inhibition of microglial activation,” Journal of Pharmacology and Experimental Therapeutics, vol. 305, no. 1, pp. 212–218, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  60. L. Qian, M. L. Block, S. J. Wei et al., “Interleukin-10 protects lipopolysaccharide-induced neurotoxicity in primary midbrain cultures by inhibiting the function of NADPH oxidase,” Journal of Pharmacology and Experimental Therapeutics, vol. 319, no. 1, pp. 44–52, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  61. L. Qian, S. T. Kai, S. J. Wei et al., “Microglia-mediated neurotoxicity is inhibited by morphine through an opioid receptor-independent reduction of NADPH oxidase activity,” Journal of Immunology, vol. 179, no. 2, pp. 1198–1209, 2007. View at Google Scholar · View at Scopus
  62. D. A. Loeffler, A. J. DeMaggio, P. L. Juneau, M. K. Havaich, and P. A. LeWitt, “Effects of enhanced striatal dopamine turnover in vivo on glutathione oxidation,” Clinical Neuropharmacology, vol. 17, no. 4, pp. 370–379, 1994. View at Google Scholar · View at Scopus
  63. S. Sanlioglu, C. M. Williams, L. Samavati et al., “Lipopolysaccharide induces rac1-dependent reactive oxygen species formation and coordinates tumor necrosis factor-α secretion through IKK regulation of NF-κB,” Journal of Biological Chemistry, vol. 276, no. 32, pp. 30188–30198, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  64. H. Neumann, “Control of glial immune function by neurons,” GLIA, vol. 36, no. 2, pp. 191–199, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  65. K. Biber, H. Neumann, K. Inoue, and H. W. G. M. Boddeke, “Neuronal “On” and “Off” signals control microglia,” Trends in Neurosciences, vol. 30, no. 11, pp. 596–602, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  66. J. M. Pocock and H. Kettenmann, “Neurotransmitter receptors on microglia,” Trends in Neurosciences, vol. 30, no. 10, pp. 527–535, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  67. A. N. Barclay, G. J. Wright, G. Brooke, and M. H. Brown, “CD200 and membrane protein interactions in the control of myeloid cells,” Trends in Immunology, vol. 23, no. 6, pp. 285–290, 2002. View at Publisher · View at Google Scholar · View at Scopus
  68. A. Lyons, E. J. Downer, S. Crotty, Y. M. Nolan, K. H. G. Mills, and M. A. Lynch, “CD200 ligand-receptor interaction modulates microglial activation in vivo and in vitro: a role for IL-4,” Journal of Neuroscience, vol. 27, no. 31, pp. 8309–8313, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  69. R. H. Hoek, S. R. Ruuls, C. A. Murphy et al., “Down-regulation of the macrophage lineage through interaction with OX2 (CD200),” Science, vol. 290, no. 5497, pp. 1768–1771, 2000. View at Publisher · View at Google Scholar · View at Scopus
  70. G. J. Wright, M. J. Puklavec, A. C. Willis et al., “Lymphoid/neuronal cell surface OX2 glycoprotein recognizes a novel receptor on macrophages implicated in the control of their function,” Immunity, vol. 13, no. 2, pp. 233–242, 2000. View at Google Scholar · View at Scopus
  71. X. J. Wang, S. Zhang, Z. Q. Yan et al., “Impaired CD200-CD200R-mediated microglia silencing enhances midbrain dopaminergic neurodegeneration: roles of aging, superoxide, NADPH oxidase, and p38 MAPK,” Free Radical Biology and Medicine, vol. 50, no. 9, pp. 1094–1106, 2011. View at Publisher · View at Google Scholar · View at PubMed
  72. L. Qin, Y. Liu, T. Wang et al., “NADPH oxidase mediates lipopolysaccharide-induced neurotoxicity and proinflammatory gene expression in activated microglia,” Journal of Biological Chemistry, vol. 279, no. 2, pp. 1415–1421, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  73. L. Qian, X. Gao, Z. Pei et al., “NADPH oxidase inhibitor DPI is neuroprotective at femtomolar concentrations through inhibition of microglia over-activation,” Parkinsonism and Related Disorders, vol. 13, supplement 3, pp. S316–S320, 2007. View at Publisher · View at Google Scholar · View at Scopus
  74. H. Kono, I. Rusyn, T. Uesugi et al., “Diphenyleneiodonium sulfate, an NADPH oxidase inhibitor, prevents early alcohol-induced liver injury in the rat,” American Journal of Physiology, vol. 280, no. 5, pp. G1005–G1012, 2001. View at Google Scholar · View at Scopus
  75. J. S. Gujral, J. A. Hinson, A. Farhood, and H. Jaeschke, “NADPH oxidase-derived oxidant stress is critical for neutrophil cytotoxicity during endotoxemia,” American Journal of Physiology, vol. 287, no. 1, pp. G243–G252, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  76. S. Pawate, Q. Shen, F. Fan, and N. R. Bhat, “Redox regulation of glial inflammatory response to lipopolysaccharide and interferonγ,” Journal of Neuroscience Research, vol. 77, no. 4, pp. 540–551, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  77. J. E. Le Belle, N. M. Orozco, A. A. Paucar et al., “Proliferative neural stem cells have high endogenous ROS levels that regulate self-renewal and neurogenesis in a PI3K/Akt-dependant manner,” Cell Stem Cell, vol. 8, no. 1, pp. 59–71, 2011. View at Publisher · View at Google Scholar · View at PubMed
  78. Q. Li and J. F. Engelhardt, “Interleukin-1β induction of NFκB is partially regulated by H2O2-mediated activation of NFκB-inducing kinase,” Journal of Biological Chemistry, vol. 281, no. 3, pp. 1495–1505, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  79. B. Halliwell and P. Jenner, “Impaired clearance of oxidised proteins in neurodegenerative diseases,” Lancet, vol. 351, no. 9114, p. 1510, 1998. View at Google Scholar · View at Scopus
  80. P. Jenner, “Oxidative mechanisms in nigral cell death in Parkinson's disease,” Movement Disorders, vol. 13, supplement 1, pp. 24–34, 1998. View at Google Scholar · View at Scopus
  81. P. Jenner and C. W. Olanow, “Understanding cell death in Parkinson's disease,” Annals of Neurology, vol. 44, no. 3, supplement 1, pp. S72–S84, 1998. View at Google Scholar · View at Scopus
  82. K. Jomova, D. Vondrakova, M. Lawson, and M. Valko, “Metals, oxidative stress and neurodegenerative disorders,” Molecular and Cellular Biochemistry, vol. 345, no. 1-2, pp. 91–104, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  83. M. J. Morgan and Z. G. Liu, “Crosstalk of reactive oxygen species and NF-κB signaling,” Cell Research, vol. 21, no. 1, pp. 103–115, 2011. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  84. P. M. Flood, L. Qian, L. J. Peterson et al., “Transcriptional factor NF-kappaB as a target for therapy in Parkinson's disease,” Parkinson's Disease, vol. 2011, Article ID 216298, 8 pages, 2011. View at Publisher · View at Google Scholar · View at PubMed
  85. H. Zhong, M. J. May, E. Jimi, and S. Ghosh, “The phosphorylation status of nuclear NF-κB determines its association with CBP/p300 or HDAC-1,” Molecular Cell, vol. 9, no. 3, pp. 625–636, 2002. View at Publisher · View at Google Scholar · View at Scopus
  86. I. Jaspers, W. Zhang, A. Fraser, J. M. Samet, and W. Reed, “Hydrogen peroxide has opposing effects on IKK activity and IκBα breakdown in airway epithelial cells,” American Journal of Respiratory Cell and Molecular Biology, vol. 24, no. 6, pp. 769–777, 2001. View at Google Scholar · View at Scopus
  87. Y. Jing, J. Yang, Y. Wang et al., “Alteration of subcellular redox equilibrium and the consequent oxidative modification of nuclear factor κB are critical for anticancer cytotoxicity by emodin, a reactive oxygen species-producing agent,” Free Radical Biology and Medicine, vol. 40, no. 12, pp. 2183–2197, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  88. Y. Wang, X. Huang, H. Cang et al., “The endogenous reactive oxygen species promote NF-κB activation by targeting on activation of NF-κB-inducing kinase in oral squamous carcinoma cells,” Free Radical Research, vol. 41, no. 9, pp. 963–971, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  89. Y. Wang, J. Yang, J. Yi et al., “Redox sensing by proteins: oxidative modifications on cysteines and the consequent events,” Antioxid Redox Signal, vol. 16, no. 7, pp. 649–657, 2012. View at Google Scholar
  90. F. Zhang, L. Qian, P. M. Flood, J. S. Shi, J. S. Hong, and H. M. Gao, “Inhibition of IκB kinase-β protects dopamine neurons against lipopolysaccharide-induced neurotoxicity,” Journal of Pharmacology and Experimental Therapeutics, vol. 333, no. 3, pp. 822–833, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  91. S. J. Chinta and J. K. Andersen, “Nitrosylation and nitration of mitochondrial complex i in Parkinson's disease,” Free Radical Research, vol. 45, no. 1, pp. 53–58, 2011. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  92. E. Clementi, G. C. Brown, M. Feelisch, and S. Moncada, “Persistent inhibition of cell respiration by nitric oxide: crucial role of S-nitrosylation of mitochondrial complex I and protective action of glutathione,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 13, pp. 7631–7636, 1998. View at Publisher · View at Google Scholar · View at Scopus
  93. C. Isobe, T. Abe, and Y. Terayama, “Levels of reduced and oxidized coenzymeQ-10 and 8-hydroxy-2′-deoxyguanosine in the cerebrospinal fluid of patients with living Parkinson's disease demonstrate that mitochondrial oxidative damage and/or oxidative DNA damage contributes to the neurodegenerative process,” Neuroscience Letters, vol. 469, no. 1, pp. 159–163, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  94. C. Isobe, T. Abe, T. Kikuchi, T. Murata, C. Sato, and Y. Terayama, “Cabergoline scavenges peroxynitrite enhanced by L-DOPA therapy in patients with Parkinson's disease,” European Journal of Neurology, vol. 13, no. 4, pp. 346–350, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  95. M. Tomás-Camardiel, I. Rite, A. J. Herrera et al., “Minocycline reduces the lipopolysaccharide-induced inflammatory reaction, peroxynitrite-mediated nitration of proteins, disruption of the blood-brain barrier, and damage in the nigral dopaminergic system,” Neurobiology of Disease, vol. 16, no. 1, pp. 190–201, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  96. M. F. Beal, “Oxidatively modified proteins in aging and disease,” Free Radical Biology and Medicine, vol. 32, no. 9, pp. 797–803, 2002. View at Publisher · View at Google Scholar · View at Scopus
  97. I. Kurkowska-Jastrzebska, A. Wrońska, M. S. Kohutnicka, A. Czlonkowski, and A. Czlonkowska, “The inflammatory reaction following 1-methyl-4-phenyl-1,2,3,6- tetrahydropyridine intoxication in mouse,” Experimental Neurology, vol. 156, no. 1, pp. 50–61, 1999. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  98. A. Castaño, A. J. Herrera, J. Cano, and A. Machado, “The degenerative effect of a single intranigral injection of LPS on the dopaminergic system is prevented by dexamethasone, and not mimicked by rh-TNF-α IL-1β IFN-γ,” Journal of Neurochemistry, vol. 81, no. 1, pp. 150–157, 2002. View at Publisher · View at Google Scholar · View at Scopus
  99. K. Sairam, K. S. Saravanan, R. Banerjee, and K. P. Mohanakumar, “Non-steroidal anti-inflammatory drug sodium salicylate, but not diclofenac or celecoxib, protects against 1-methyl-4-phenyl pyridinium-induced dopaminergic neurotoxicity in rats,” Brain Research, vol. 966, no. 2, pp. 245–252, 2003. View at Publisher · View at Google Scholar · View at Scopus
  100. F. Zhang, L. Qian, P. M. Flood et al., “Inhibition of IkappaB kinase-beta protects dopamine neurons against lipopolysaccharide-induced neurotoxicity,” Journal of Pharmacology and Experimental Therapeutics, vol. 333, no. 3, pp. 822–833, 2010. View at Google Scholar
  101. A. Bernardo, L. Gasparini, E. Ongini, and L. Minghetti, “Dynamic regulation of microglial functions by the non-steroidal anti-inflammatory drug NCX 2216: implications for chronic treatments of neurodegenerative diseases,” Neurobiology of Disease, vol. 22, no. 1, pp. 25–32, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  102. A. Bernardo, M. A. Ajmone-Cat, L. Gasparini, E. Ongini, and L. Minghetti, “Nuclear receptor peroxisome proliferator-activated receptor-γ is activated in rat microglial cells by the anti-inflammatory drug HCT1026, a derivative of flurbiprofen,” Journal of Neurochemistry, vol. 92, no. 4, pp. 895–903, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  103. K. Strle, J. H. Zhou, W. H. Shen et al., “Interleukin-10 in the brain,” Critical Reviews in Immunology, vol. 21, no. 5, pp. 427–449, 2001. View at Google Scholar
  104. K. W. Moore, R. De Waal Malefyt, R. L. Coffman, and A. O'Garra, “Interleukin-10 and the interleukin-10 receptor,” Annual Review of Immunology, vol. 19, pp. 683–765, 2001. View at Publisher · View at Google Scholar · View at PubMed
  105. L. C. Johnston, X. Su, K. Maguire-Zeiss et al., “Human interleukin-10 gene transfer is protective in a rat model of parkinson's disease,” Molecular Therapy, vol. 16, no. 8, pp. 1392–1399, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  106. Y. Zhu, G. Y. Yang, B. Ahlemeyer et al., “Transforming growth factor-β1 increases bad phosphorylation and protects neurons against damage,” Journal of Neuroscience, vol. 22, no. 10, pp. 3898–3909, 2002. View at Google Scholar · View at Scopus
  107. J. H. Prehn and J. Krieglstein, “Opposing effects of transforming growth factor-β1 on glutamate neurotoxicity,” Neuroscience, vol. 60, no. 1, pp. 7–10, 1994. View at Publisher · View at Google Scholar · View at Scopus
  108. L. Qian, S. J. Wei, D. Zhang et al., “Potent anti-inflammatory and neuroprotective effects of tgf-β1 are mediated through the inhibition of erk and p47phox-Ser345 phosphorylation and translocation in microglia,” Journal of Immunology, vol. 181, no. 1, pp. 660–668, 2008. View at Google Scholar · View at Scopus
  109. W. Zhang, T. Wang, L. Qin et al., “Neuroprotective effect of dextromethorphan in the MPTP Parkinson's disease model: role of NADPH oxidase,” The FASEB Journal Biology, vol. 18, no. 3, pp. 589–591, 2004. View at Google Scholar · View at Scopus
  110. W. Zhang, L. Qin, T. Wang et al., “3-Hydroxymorphinan is neurotrophic to dopaminergic neurons and is also neuroprotective against LPS-induced neurotoxicity,” The FASEB Journal, vol. 19, no. 3, pp. 395–397, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  111. W. Zhang, E. J. Shin, T. Wang et al., “3-Hydroxymorphinan, a metabolite of dextromethorphan, protects nigrostriatal pathway against MPTP-elicited damage both in vivo and in vitro,” The FASEB Journal, vol. 20, no. 14, pp. 2496–2511, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  112. L. Liu, K. Resch, and V. Kaever, “Inhibition of lymphocyte proliferation by the anti-arthritic drug sinomenine,” International Journal of Immunopharmacology, vol. 16, no. 8, pp. 685–691, 1994. View at Publisher · View at Google Scholar · View at Scopus
  113. L. Liu, E. Buchner, D. Beitze et al., “Amelioration of rat experimental arthritides by treatment with the alkaloid sinomenine,” International Journal of Immunopharmacology, vol. 18, no. 10, pp. 529–543, 1996. View at Publisher · View at Google Scholar · View at Scopus
  114. W. C. Koff, A. V. Fann, M. A. Dunegan, and L. B. Lachman, “Catecholamine-induced suppression of interleukin-1 production,” Lymphokine Research, vol. 5, no. 4, pp. 239–247, 1986. View at Google Scholar · View at Scopus
  115. T. van der Poll, J. Jansen, E. Endert, H. P. Sauerwein, and S. J. H. Van Deventer, “Noradrenaline inhibits lipopolysaccharide-induced tumor necrosis factor and interleukin 6 production in human whole blood,” Infection and Immunity, vol. 62, no. 5, pp. 2046–2050, 1994. View at Google Scholar · View at Scopus
  116. L. Sekut, B. R. Champion, K. Page, J. A. Menius, and K. M. Connolly, “Anti-inflammatory activity of salmeterol: down-regulation of cytokine production,” Clinical and Experimental Immunology, vol. 99, no. 3, pp. 461–466, 1995. View at Google Scholar · View at Scopus
  117. A. Severn, N. T. Rapson, C. A. Hunter, and F. Y. Liew, “Regulation of tumor necrosis factor production by adrenaline and β-adrenergic agonists,” Journal of Immunology, vol. 148, no. 11, pp. 3441–3445, 1992. View at Google Scholar
  118. P. Farmer and J. Pugin, “beta-adrenergic agonists exert their “anti-inflammatory” effects in monocytic cells through the IkappaB/NF-kappaB pathway,” American Journal of Physiology, vol. 279, no. 4, pp. L675–L682, 2000. View at Google Scholar
  119. N. W. Kin and V. M. Sanders, “It takes nerve to tell T and B cells what to do,” Journal of Leukocyte Biology, vol. 79, no. 6, pp. 1093–1104, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  120. P. Panina-Bordignon, D. Mazzeo, P. D. Lucia et al., “Beta2-agonists prevent Th1 development by selective inhibition of interleukin 12,” The Journal of Clinical Investigation, vol. 100, no. 6, pp. 1513–1519, 1997. View at Google Scholar
  121. L. Qian, H. M. Wu, S. H. Chen et al., “{beta}2-adrenergic receptor activation prevents rodent dopaminergic neurotoxicity by inhibiting microglia via a novel signaling pathway,” The Journal of Immunology, vol. 186, no. 7, pp. 4443–4454, 2011. View at Google Scholar
  122. K. S. Tan, A. G. Nackley, K. Satterfield, W. Maixner, L. Diatchenko, and P. M. Flood, “Beta2 adrenergic receptor activation stimulates pro-inflammatory cytokine production in macrophages via PKA- and NF-kappaB-independent mechanisms,” Cellular Signalling, vol. 19, no. 2, pp. 251–260, 2007. View at Google Scholar
  123. K. A. Maguire-Zeiss, D. W. Short, and H. J. Federoff, “Synuclein, dopamine and oxidative stress: co-conspirators in Parkinson's disease?” Molecular Brain Research, vol. 134, no. 1, pp. 18–23, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  124. S. Gandhi and N. W. Wood, “Molecular pathogenesis of Parkinson's disease,” Human Molecular Genetics, vol. 14, no. 18, pp. 2749–2755, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  125. D. G. Graham, “Oxidative pathways for catecholamines in the genesis of neuromelanin and cytotoxic quinones,” Molecular Pharmacology, vol. 14, no. 4, pp. 633–643, 1978. View at Google Scholar · View at Scopus
  126. A. N. Basma, E. J. Morris, W. J. Nicklas, and H. M. Geller, “L-DOPA cytotoxicity to PC12 cells in culture is via its autoxidation,” Journal of Neurochemistry, vol. 64, no. 2, pp. 825–832, 1995. View at Google Scholar · View at Scopus
  127. C. M. Jin, Y. J. Yang, H. S. Huang, M. Kai, and M. K. Lee, “Mechanisms of L-DOPA-induced cytotoxicity in rat adrenal pheochromocytoma cells: implication of oxidative stress-related kinases and cyclic AMP,” Neuroscience, vol. 170, no. 2, pp. 390–398, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  128. E. A. Sabens Liedhegner, K. M. Steller, and J. J. Mieyal, “Levodopa activates apoptosis signaling kinase 1 (ASK1) and promotes apoptosis in a neuronal model: implications for the treatment of Parkinson's disease,” Chemical Research in Toxicology, vol. 24, no. 10, pp. 1644–1652, 2011. View at Publisher · View at Google Scholar · View at PubMed
  129. C. Buhmann, S. Arlt, A. Kontush et al., “Plasma and CSF markers of oxidative stress are increased in Parkinson's disease and influenced by antiparkinsonian medication,” Neurobiology of Disease, vol. 15, no. 1, pp. 160–170, 2004. View at Publisher · View at Google Scholar · View at Scopus
  130. A. Prigione, B. Begni, A. Galbussera et al., “Oxidative stress in peripheral blood mononuclear cells from patients with Parkinson's disease: negative correlation with levodopa dosage,” Neurobiology of Disease, vol. 23, no. 1, pp. 36–43, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus