- About this Journal ·
- Abstracting and Indexing ·
- Advance Access ·
- Aims and Scope ·
- Annual Issues ·
- Article Processing Charges ·
- Articles in Press ·
- Author Guidelines ·
- Bibliographic Information ·
- Citations to this Journal ·
- Contact Information ·
- Editorial Board ·
- Editorial Workflow ·
- Free eTOC Alerts ·
- Publication Ethics ·
- Reviewers Acknowledgment ·
- Submit a Manuscript ·
- Subscription Information ·
- Table of Contents
Oxidative Medicine and Cellular Longevity
Volume 2013 (2013), Article ID 264935, 10 pages
Oxidative Stress Is Related to the Deleterious Effects of Heme Oxygenase-1 in an In Vivo Neuroinflammatory Rat Model
1UMR INSERM U930, Université François Rabelais de Tours, PRES Centre Val de Loire Université, 37000 Tours, France
2EA 4708, IPROS, CHR Orléans, BP 2439, 1 rue Porte Madeleine, 45032 Orléans, France
3Département Pharmacie, CHRU de Tours, Tours, France
Received 5 November 2012; Revised 21 January 2013; Accepted 22 January 2013
Academic Editor: Sumitra Miriyala
Copyright © 2013 Claire Tronel et al. 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.
- C. K. Glass, K. Saijo, B. Winner, M. C. Marchetto, and F. H. Gage, “Mechanisms underlying inflammation in neurodegeneration,” Cell, vol. 140, no. 6, pp. 918–934, 2010.
- E. Ulvestad, K. Williams, R. Bjerkvig, K. Tiekotter, J. Antel, and R. Matre, “Human microglial cells have phenotypic and functional characteristics in common with both macrophages and dendritic antigen-presenting cells,” Journal of Leukocyte Biology, vol. 56, no. 6, pp. 732–740, 1994.
- G. W. Kreutzberg, “Microglia: a sensor for pathological events in the CNS,” Trends in Neurosciences, vol. 19, no. 8, pp. 312–318, 1996.
- R. M. Ransohoff and V. H. Perry, “Microglial physiology: unique stimuli, specialized responses,” Annual Review of Immunology, vol. 27, pp. 119–145, 2009.
- M. L. Block and J. S. Hong, “Microglia and inflammation-mediated neurodegeneration: multiple triggers with a common mechanism,” Progress in Neurobiology, vol. 76, no. 2, pp. 77–98, 2005.
- P. L. McGeer and E. G. McGeer, “NSAIDs and Alzheimer disease: epidemiological, animal model and clinical studies,” Neurobiology of Aging, vol. 28, no. 5, pp. 639–647, 2007.
- A. Gupta, A. Kumar, and S. K. Kulkarni, “Targeting oxidative stress, mitochondrial dysfunction and neuroinflammatory signaling by selective cyclooxygenase (COX)-2 inhibitors mitigates MPTP-induced neurotoxicity in mice,” Progress in Neuro-Psychopharmacology and Biological Psychiatry, vol. 35, no. 4, pp. 974–981, 2011.
- A. Mirshafiey, H. Matsuo, S. Nakane, B. H. A. Rehm, C. S. Koh, and S. Miyoshi, “Novel immunosuppressive therapy by M2000 in experimental multiple sclerosis,” Immunopharmacology and Immunotoxicology, vol. 27, no. 2, pp. 255–265, 2005.
- P. T. Jantzen, K. E. Connor, G. DiCarlo et al., “Microglial activation and β-amyloid deposit reduction caused by a nitric oxide-releasing nonsteroidal anti-inflammatory drug in amyloid precursor protein plus presenilin-1 transgenic mice,” Journal of Neuroscience, vol. 22, no. 6, pp. 2246–2254, 2002.
- B. P. Imbimbo, “An update on the efficacy of non-steroidal anti-inflammatory drugs in Alzheimer's disease,” Expert Opinion on Investigational Drugs, vol. 18, no. 8, pp. 1147–1168, 2009.
- R. Tenhunen, H. S. Marver, and R. Schmid, “The enzymatic conversion of heme to bilirubin by microsomal heme oxygenase,” Proceedings of the National Academy of Sciences of the United States of America, vol. 61, no. 2, pp. 748–755, 1968.
- S. Immenschuh and G. Ramadori, “Gene regulation of heme oxygenase-1 as a therapeutic target,” Biochemical Pharmacology, vol. 60, no. 8, pp. 1121–1128, 2000.
- R. Stocker, “Antioxidant activities of bile pigments,” Antioxidants and Redox Signaling, vol. 6, no. 5, pp. 841–849, 2004.
- G. S. Jeong, D. S. Lee, D. C. Kim et al., “Neuroprotective and anti-inflammatory effects of mollugin via up-regulation of heme oxygenase-1 in mouse hippocampal and microglial cells,” European Journal of Pharmacology, vol. 654, no. 3, pp. 226–234, 2011.
- A. Chora, P. Fontoura, A. Cunha et al., “Heme oxygenase-1 and carbon monoxide suppress autoimmune neuroinflammation,” Journal of Clinical Investigation, vol. 117, no. 2, pp. 438–447, 2007.
- H. M. Schipper, “Heme oxygenase-1: role in brain aging and neurodegeneration,” Experimental Gerontology, vol. 35, no. 6-7, pp. 821–830, 2000.
- C. Justicia, P. Ramos-Cabrer, and M. Hoehn, “MRI detection of secondary damage after stroke: chronic iron accumulation in the thalamus of the rat brain,” Stroke, vol. 39, no. 5, pp. 1541–1547, 2008.
- R. Schwarcz and C. Köhler, “Differential vulnerability of central neurons of the rat to quinolinic acid,” Neuroscience Letters, vol. 38, no. 1, pp. 85–90, 1983.
- N. Arlicot, A. Katsifis, L. Garreau et al., “Evaluation of CLINDE as potent translocator protein (18 kDa) SPECT radiotracer reflecting the degree of neuroinflammation in a rat model of microglial activation,” European Journal of Nuclear Medicine and Molecular Imaging, vol. 35, no. 12, pp. 2203–2211, 2008.
- A. M. Estrada Sánchez, J. Mejía-Toiber, and L. Massieu, “Excitotoxic neuronal death and the pathogenesis of Huntington's disease,” Archives of Medical Research, vol. 39, no. 3, pp. 265–276, 2008.
- N. Desbuards, G. Y. Rochefort, D. Schlecht et al., “Heme oxygenase-1 inducer hemin prevents vascular thrombosis,” Thrombosis and Haemostasis, vol. 98, no. 3, pp. 614–620, 2007.
- B. Bektaşoğlu, S. Esin Celik, M. Ozyürek, K. Güçlü, and R. Apak, “Novel hydroxyl radical scavenging antioxidant activity assay for water-soluble antioxidants using a modified CUPRAC method,” Biochemical and Biophysical Research Communications, vol. 345, no. 3, pp. 1194–1200, 2006.
- C. K. Chang, M. V. Albarillo, and W. Schumer, “Therapeutic effect of dimethyl sulfoxide on ICAM-1 gene expression and activation of NF-κB and AP-1 in septic rats,” Journal of Surgical Research, vol. 95, no. 2, pp. 181–187, 2001.
- G. Paxinos and C. Watson, The Rat Brain in Stereotaxic Coordonates, Academic Press, New York, NY, USA, 6th edition, 1986.
- N. Desbuards, J. M. Hyvelin, M. C. Machet et al., “Heme oxygenase-1 inducer hemin attenuates the progression of remnant kidney model,” Nephron—Experimental Nephrology, vol. 113, no. 1, pp. e35–e44, 2009.
- S. Borgmann, “Electrochemical quantification of reactive oxygen and nitrogen: challenges and opportunities,” Analytical and Bioanalytical Chemistry, vol. 394, no. 1, pp. 95–105, 2009.
- B. Kalyanaraman, “Oxidative chemistry of fluorescent dyes: implications in the detection of reactive oxygen and nitrogen species,” Biochemical Society Transactions, vol. 39, no. 5, pp. 1221–1225, 2011.
- S. Khandelwal and R. K. Saxena, “Age-dependent increase in green autofluorescence of blood erythrocytes,” Journal of Biosciences, vol. 32, no. 2, pp. 1139–1145, 2007.
- R. Poulet, M. T. Gentile, C. Vecchione et al., “Acute hypertension induces oxidative stress in brain tissues,” Journal of Cerebral Blood Flow and Metabolism, vol. 26, no. 2, pp. 253–262, 2006.
- H. Shichinohe, S. Kuroda, H. Yasuda et al., “Neuroprotective effects of the free radical scavenger Edaravone (MCI-186) in mice permanent focal brain ischemia,” Brain Research, vol. 1029, no. 2, pp. 200–206, 2004.
- E. Yamamoto, N. Tamamaki, T. Nakamura et al., “Excess salt causes cerebral neuronal apoptosis and inflammation in stroke-prone hypertensive rats through angiotensin II-induced NADPH oxidase activation,” Stroke, vol. 39, no. 11, pp. 3049–3056, 2008.
- D. Y. Lu, Y. Y. Tsao, Y. M. Leung, and K. P. Su, “Docosahexaenoic acid suppresses neuroinflammatory responses and induces heme oxygenase-1 expression in BV-2 microglia: implications of antidepressant effects for omega-3 fatty acids,” Neuropsychopharmacology, vol. 35, no. 11, pp. 2238–2248, 2010.
- M. D. Laird, C. Wakade, C. H. Alleyne Jr., and K. M. Dhandapani, “Hemin-induced necroptosis involves glutathione depletion in mouse astrocytes,” Free Radical Biology and Medicine, vol. 45, no. 8, pp. 1103–1114, 2008.
- J. S. Park, J. A. Shin, J. S. Jung et al., “Anti-inflammatory mechanism of compound K in activated microglia and its neuroprotective effect on experimental stroke in mice,” Journal of Pharmacology and Experimental Therapeutics, vol. 341, no. 1, pp. 59–67, 2012.
- H. Kettenmann, U. K. Hanisch, M. Noda, and A. Verkhratsky, “Physiology of microglia,” Physiological Reviews, vol. 91, pp. 461–553, 2011.
- H. Zhao, J. Joseph, H. M. Fales et al., “Detection and characterization of the product of hydroethidine and intracellular superoxide by HPLC and limitations of fluorescence,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 16, pp. 5727–5732, 2005.
- T. Morita, “Heme oxygenase and atherosclerosis,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 25, no. 9, pp. 1786–1795, 2005.
- P. J. Syapin, “Regulation of haeme oxygenase-1 for treatment of neuroinflammation and brain disorders,” British Journal of Pharmacology, vol. 155, no. 5, pp. 623–640, 2008.
- H. M. Schipper, A. Gupta, and W. A. Szarek, “Suppression of glial HO-1 activitiy as a potential neurotherapeutic intervention in AD,” Current Alzheimer Research, vol. 6, no. 5, pp. 424–430, 2009.
- J. K. Ryu, H. B. Choi, and J. G. McLarnon, “Peripheral benzodiazepine receptor ligand PK11195 reduces microglial activation and neuronal death in quinolinic acid-injected rat striatum,” Neurobiology of Disease, vol. 20, no. 2, pp. 550–561, 2005.
- Z. Soltys, O. Orzylowska-Sliwinska, M. Zaremba et al., “Quantitative morphological study of microglial cells in the ischemic rat brain using principal component analysis,” Journal of Neuroscience Methods, vol. 146, no. 1, pp. 50–60, 2005.
- R. J. Wong, H. J. Vreman, S. Schulz, F. S. Kalish, N. W. Pierce, and D. K. Stevenson, “In vitro inhibition of heme oxygenase isoenzymes by metalloporphyrins,” Journal of Perinatology, vol. 1, pp. S35–S41, 2011.
- Y. M. Kim, H. O. Pae, J. E. Park et al., “Heme oxygenase in the regulation of vascular biology: from molecular mechanisms to therapeutic opportunities,” Antioxidants & Redox Signaling, vol. 14, no. 1, pp. 137–167, 2011.
- K. Sodhi, K. Inoue, K. H. Gotlinger et al., “Epoxyeicosatrienoic acid agonist rescues the metabolic syndrome phenotype of HO-2-null mice,” Journal of Pharmacology and Experimental Therapeutics, vol. 331, no. 3, pp. 906–916, 2009.
- S. Lin, Q. Zhong, F. L. Lv et al., “Heme activates TLR4-mediated inflammatory injury via MyD88/TRIF signaling pathway in intracerebral hemorrhage,” Journal of Neuroinflammation, vol. 9, no. 46, 2012.
- K. Miyake, “Endotoxin recognition molecules MD-2 and toll-like receptor 4 as potential targets for therapeutic intervention of endotoxin shock,” Current Drug Targets: Inflammation and Allergy, vol. 3, no. 3, pp. 291–297, 2004.
- K. Takeda and S. Akira, “TLR signaling pathways,” Seminars in Immunology, vol. 16, pp. 3–9, 2004.
- H. M. Schipper, “Heme oxygenase-1 in Alzheimer disease: a tribute to Moussa Youdim,” Journal of Neural Transmission, vol. 118, no. 3, pp. 381–387, 2011.