Oxidative stress is related to the deleterious effects of heme oxygenase-1 in an in vivo neuroinflammatory rat model

Oxidative Medicine and Cellular Longevity

Volumn , Issue , 2013, Pages

  Tronel, Claire ^a   Rochefort, Gaël Y ^b   Arlicot, Nicolas ^a   Bodard, Sylvie ^a   Chalon, Sylvie ^a   Antier, Daniel ^a,c  

^a UNIVERSITÉ DE TOURS   (France)

^b CENTRE HOSPITALIER RÉGIONAL D ORLÉANS   (France)

^c UNIVERSITY HOSPITAL OF TOURS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CEREBRAL TISSUES; DELETERIOUS EFFECTS; EXPERIMENTAL CONDITIONS; HEME OXYGENASE-1; MICROGLIAL ACTIVATIONS; NEURODEGENERATIVE; NEUROINFLAMMATION; REACTIVE OXYGEN SPECIES;

IRON; PORPHYRINS; RATS; SUBSTRATES; TISSUE;

BRAIN;

DEFEROXAMINE; HEME OXYGENASE 1; HEMIN; IRON; QUINOLINIC ACID; REACTIVE OXYGEN METABOLITE; FERROUS ION; IRON CHELATING AGENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN TISSUE; CATABOLISM; CELL ACTIVATION; CELL SURVIVAL; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME SUBSTRATE; IN VIVO STUDY; MALE; MICROGLIA; NERVE CELL NECROSIS; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; RAT; ANIMAL; APOPTOSIS; BRAIN; DEGENERATIVE DISEASE; DISEASE MODEL; DRUG EFFECT; ENZYMOLOGY; METABOLISM; NERVE CELL; PATHOLOGY; WISTAR RAT;

ANIMALIA; RATTUS; RODENTIA;

ANIMALS; APOPTOSIS; BRAIN; DISEASE MODELS, ANIMAL; FERROUS COMPOUNDS; HEME OXYGENASE-1; HEMIN; IRON CHELATING AGENTS; MALE; MICROGLIA; NEURODEGENERATIVE DISEASES; NEURONS; OXIDATIVE STRESS; QUINOLINIC ACID; RATS; RATS, WISTAR; REACTIVE OXYGEN SPECIES;

EID: 84875497898     PISSN: 19420900     EISSN: 19420994     Source Type: Journal    
DOI: 10.1155/2013/264935     Document Type: Article

References (48)

1. Glass C. K., Saijo K., Winner B., Marchetto M. C., Gage F. H., Mechanisms underlying inflammation in neurodegeneration. Cell 2010 140 6 918 934 2-s2.0-77950363010 10.1016/j.cell.2010.02.016
2. Ulvestad E., Williams K., Bjerkvig R., Tiekotter K., Antel J., Matre R., Human microglial cells have phenotypic and functional characteristics in common with both macrophages and dendritic antigen-presenting cells. Journal of Leukocyte Biology 1994 56 6 732 740 2-s2.0-0028558519
3. Kreutzberg G. W., Microglia: a sensor for pathological events in the CNS. Trends in Neurosciences 1996 19 8 312 318 2-s2.0-0030222037 10.1016/0166-2236(96)10049-7 (Pubitemid 26349059)
4. Ransohoff R. M., Perry V. H., Microglial physiology: unique stimuli, specialized responses. Annual Review of Immunology 2009 27 119 145
5. Block M. L., Hong J. S., Microglia and inflammation-mediated neurodegeneration: multiple triggers with a common mechanism. Progress in Neurobiology 2005 76 2 77 98 (Pubitemid 41242883)
6. McGeer P. L., McGeer E. G., NSAIDs and Alzheimer disease: epidemiological, animal model and clinical studies. Neurobiology of Aging 2007 28 5 639 647 2-s2.0-33847339301 10.1016/j.neurobiolaging.2006.03.013 (Pubitemid 46349357)
7. Gupta A., Kumar A., Kulkarni S. K., 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 2011 35 4 974 981 2-s2.0-79955999259 10.1016/j.pnpbp.2011.01.017
8. Mirshafiey A., Matsuo H., Nakane S., Rehm B. H. A., Koh C. S., Miyoshi S., Novel immunosuppressive therapy by M2000 in experimental multiple sclerosis. Immunopharmacology and Immunotoxicology 2005 27 2 255 265 2-s2.0-23244440434 10.1081/IPH-200067751 (Pubitemid 41098456)
9. Jantzen P. T., Connor K. E., DiCarlo G., Wenk G. L., Wallace J. L., Rojiani A. M., Coppola D., Morgan D., Gordon M. N., 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 2002 22 6 2246 2254 2-s2.0-0037088914 (Pubitemid 35386524)
10. Imbimbo B. P., An update on the efficacy of non-steroidal anti-inflammatory drugs in Alzheimer's disease. Expert Opinion on Investigational Drugs 2009 18 8 1147 1168 2-s2.0-68049118952 10.1517/13543780903066780
11. Tenhunen R., Marver H. S., Schmid R., The enzymatic conversion of heme to bilirubin by microsomal heme oxygenase. Proceedings of the National Academy of Sciences of the United States of America 1968 61 2 748 755 2-s2.0-0014348401
12. Immenschuh S., Ramadori G., Gene regulation of heme oxygenase-1 as a therapeutic target. Biochemical Pharmacology 2000 60 8 1121 1128 2-s2.0-0034668216 10.1016/S0006-2952(00)00443-3
13. Stocker R., Antioxidant activities of bile pigments. Antioxidants and Redox Signaling 2004 6 5 841 849 2-s2.0-4544386856 10.1089/ars.2004.6.841 (Pubitemid 39237937)
14. Jeong G. S., Lee D. S., Kim D. C., Jahng Y., Son J. K., Lee S. H., Kim Y. C., Neuroprotective and anti-inflammatory effects of mollugin via up-regulation of heme oxygenase-1 in mouse hippocampal and microglial cells. European Journal of Pharmacology 2011 654 3 226 234 2-s2.0-79951674708 10.1016/j.ejphar.2010.12. 027
15. Chora A., Fontoura P., Cunha A., Pais T. F., Cardoso S., Ho P. P., Lee L. Y., Sobel R. A., Steinman L., Soares M. P., Heme oxygenase-1 and carbon monoxide suppress autoimmune neuroinflammation. Journal of Clinical Investigation 2007 117 2 438 447 2-s2.0-33846819008 10.1172/JCI28844 (Pubitemid 46203972)
16. Schipper H. M., Heme oxygenase-1: role in brain aging and neurodegeneration. Experimental Gerontology 2000 35 6-7 821 830 10.1016/S0531-5565(00)00148-0
17. Justicia C., Ramos-Cabrer P., Hoehn M., MRI detection of secondary damage after stroke: chronic iron accumulation in the thalamus of the rat brain. Stroke 2008 39 5 1541 1547 2-s2.0-44449097256 10.1161/STROKEAHA.107.503565
18. Schwarcz R., Köhler C., Differential vulnerability of central neurons of the rat to quinolinic acid. Neuroscience Letters 1983 38 1 85 90 10.1016/0304-3940(83)90115-5 (Pubitemid 13029108)
19. Arlicot N., Katsifis A., Garreau L., Mattner F., Vergote J., Duval S., Kousignian I., Bodard S., Guilloteau D., Chalon S., 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 2008 35 12 2203 2211 2-s2.0-58149299495 10.1007/s00259-008-0882-2
20. Estrada Sánchez A. M., Mejía-Toiber J., Massieu L., Excitotoxic neuronal death and the pathogenesis of Huntington's disease. Archives of Medical Research 2008 39 3 265 276 10.1016/j.arcmed.2007.11.011 (Pubitemid 351221151)
21. Desbuards N., Rochefort G. Y., Schlecht D., Machet M. C., Halimi J. M., Eder V., Hyvelin J. M., Antier D., Heme oxygenase-1 inducer hemin prevents vascular thrombosis. Thrombosis and Haemostasis 2007 98 3 614 620 2-s2.0-34548687462 10.1160/TH06-12-0717 (Pubitemid 47412887)
22. Bektaşoǧlu B., Esin Celik S., Ozyürek M., Güçlü K., Apak R., Novel hydroxyl radical scavenging antioxidant activity assay for water-soluble antioxidants using a modified CUPRAC method. Biochemical and Biophysical Research Communications 2006 345 3 1194 1200 10.1016/j.bbrc.2006.05.038 (Pubitemid 44218793)
23. Chang C. K., Albarillo M. V., Schumer W., Therapeutic effect of dimethyl sulfoxide on ICAM-1 gene expression and activation of NF- B and AP-1 in septic rats. Journal of Surgical Research 2001 95 2 181 187 2-s2.0-0035746977 10.1006/jsre.2000.6033 (Pubitemid 34953553)
24. Paxinos G., Watson C., The Rat Brain in Stereotaxic Coordonates 1986 6th New York, NY, USA Academic Press
25. Desbuards N., Hyvelin J. M., Machet M. C., Eder V., Garrigue M. A., Halimi J. M., Antier D., Heme oxygenase-1 inducer hemin attenuates the progression of remnant kidney model. Nephron-Experimental Nephrology 2009 113 1 e35 e44 2-s2.0-67649847848 10.1159/000228081
26. Borgmann S., Electrochemical quantification of reactive oxygen and nitrogen: challenges and opportunities. Analytical and Bioanalytical Chemistry 2009 394 1 95 105 10.1007/s00216-009-2692-1
27. Kalyanaraman B., Oxidative chemistry of fluorescent dyes: implications in the detection of reactive oxygen and nitrogen species. Biochemical Society Transactions 2011 39 5 1221 1225 10.1042/BST0391221
28. Khandelwal S., Saxena R. K., Age-dependent increase in green autofluorescence of blood erythrocytes. Journal of Biosciences 2007 32 2 1139 1145 10.1007/s12038-007-0115-z (Pubitemid 47583874)
29. Poulet R., Gentile M. T., Vecchione C., Distaso M., Aretini A., Fratta L., Russo G., Echart C., Maffei A., De Simoni M. G., Lembo G., Acute hypertension induces oxidative stress in brain tissues. Journal of Cerebral Blood Flow and Metabolism 2006 26 2 253 262 2-s2.0-31444453709 10.1038/sj.jcbfm.9600188 (Pubitemid 43151580)
30. Shichinohe H., Kuroda S., Yasuda H., Ishikawa T., Iwai M., Horiuchi M., Iwasaki Y., Neuroprotective effects of the free radical scavenger Edaravone (MCI-186) in mice permanent focal brain ischemia. Brain Research 2004 1029 2 200 206 2-s2.0-7944234144 10.1016/j.brainres.2004.09.055 (Pubitemid 39470176)
31. Yamamoto E., Tamamaki N., Nakamura T., Kataoka K., Tokutomi Y., Dong Y. F., Fukuda M., Matsuba S., Ogawa H., Kim-Mitsuyama S., Excess salt causes cerebral neuronal apoptosis and inflammation in stroke-prone hypertensive rats through angiotensin II-induced NADPH oxidase activation. Stroke 2008 39 11 3049 3056 2-s2.0-55749113002 10.1161/STROKEAHA.108.517284
32. Lu D. Y., Tsao Y. Y., Leung Y. M., Su K. P., 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 2010 35 11 2238 2248 2-s2.0-78651292670 10.1038/npp.2010.98
33. Laird M. D., Wakade C., Alleyne C. H. Jr., Dhandapani K. M., Hemin-induced necroptosis involves glutathione depletion in mouse astrocytes. Free Radical Biology and Medicine 2008 45 8 1103 1114 2-s2.0-53049083456 10.1016/j.freeradbiomed.2008.07.003
34. Park J. S., Shin J. A., Jung J. S., Hyun J. W., Le T. K., Kim D. H., Park E. M., Kim H. S., Anti-inflammatory mechanism of compound K in activated microglia and its neuroprotective effect on experimental stroke in mice. Journal of Pharmacology and Experimental Therapeutics 2012 341 1 59 67 10.1124/jpet.111.189035
35. Kettenmann H., Hanisch U. K., Noda M., Verkhratsky A., Physiology of microglia. Physiological Reviews 2011 91 461 553 10.1152/physrev.00011.2010
36. Zhao H., Joseph J., Fales H. M., Sokoloski E. A., Levine R. L., Vasquez-Vivar J., Kalyanaraman B., 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 2005 102 16 5727 5732 2-s2.0-17644394600 10.1073/pnas. 0501719102 (Pubitemid 40559627)
37. Morita T., Heme oxygenase and atherosclerosis. Arteriosclerosis, Thrombosis, and Vascular Biology 2005 25 9 1786 1795 (Pubitemid 41243444)
38. Syapin P. J., Regulation of haeme oxygenase-1 for treatment of neuroinflammation and brain disorders. British Journal of Pharmacology 2008 155 5 623 640 2-s2.0-54949143147 10.1038/bjp.2008.342
39. Schipper H. M., Gupta A., Szarek W. A., Suppression of glial HO-1 activitiy as a potential neurotherapeutic intervention in AD. Current Alzheimer Research 2009 6 5 424 430 2-s2.0-67649617842 10.2174/156720509789207985
40. Ryu J. K., Choi H. B., McLarnon J. G., Peripheral benzodiazepine receptor ligand PK11195 reduces microglial activation and neuronal death in quinolinic acid-injected rat striatum. Neurobiology of Disease 2005 20 2 550 561 2-s2.0-26944485506 10.1016/j.nbd.2005.04.010 (Pubitemid 41476281)
41. Soltys Z., Orzylowska-Sliwinska O., Zaremba M., Orlowski D., Piechota M., Fiedorowicz A., Janeczko K., Oderfeld-Nowak B., Quantitative morphological study of microglial cells in the ischemic rat brain using principal component analysis. Journal of Neuroscience Methods 2005 146 1 50 60 10.1016/j.jneumeth. 2005.01.009 (Pubitemid 40776123)
42. Wong R. J., Vreman H. J., Schulz S., Kalish F. S., Pierce N. W., Stevenson D. K., In vitro inhibition of heme oxygenase isoenzymes by metalloporphyrins. Journal of Perinatology 2011 1 S35 S41
43. Kim Y. M., Pae H. O., Park J. E., Lee Y. C., Woo J. M., Kim N. H., Choi Y. K., Lee B. S., Kim S. R., Chung H. T., Heme oxygenase in the regulation of vascular biology: from molecular mechanisms to therapeutic opportunities. Antioxidants & Redox Signaling 2011 14 1 137 167 10.1089/ars.2010.3153
44. Sodhi K., Inoue K., Gotlinger K. H., Canestraro M., Vanella L., Kim D. H., Manthati V. L., Koduru S. R., Falck J. R., Schwartzman M. L., Abraham N. G., Epoxyeicosatrienoic acid agonist rescues the metabolic syndrome phenotype of HO-2-null mice. Journal of Pharmacology and Experimental Therapeutics 2009 331 3 906 916 2-s2.0-73349106519 10.1124/jpet.109.157545
45. Lin S., Zhong Q., Lv F. L., Zhou Y., Li J. Q., Wang J. Z., Yang Q. W., Yin Q., Heme activates TLR4-mediated inflammatory injury via MyD88/TRIF signaling pathway in intracerebral hemorrhage. Journal of Neuroinflammation 2012 9 46
46. Miyake K., 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 2004 3 3 291 297 2-s2.0-4444291514 10.2174/1568010043343633 (Pubitemid 39206657)
47. Takeda K., Akira S., TLR signaling pathways. Seminars in Immunology 2004 16 3 9 10.1016/j.smim.2003.10.003 (Pubitemid 38147427)
48. Schipper H. M., Heme oxygenase-1 in Alzheimer disease: a tribute to Moussa Youdim. Journal of Neural Transmission 2011 118 3 381 387