Superoxide (•O2-) production in CA1 neurons of rat hippocampal slices exposed to graded levels of oxygen

Journal of Neurophysiology

Volumn 98, Issue 2, 2007, Pages 1030-1041

  D'Agostino, Dominic P ^a   Putnam, Robert W ^b   Dean, Jay B ^a  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

^b WRIGHT STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

OXYGEN; SUPEROXIDE; ANTIOXIDANT; CARBONYL CYANIDE 4 (TRIFLUOROMETHOXY)PHENYLHYDRAZONE; DRUG DERIVATIVE; ETHIDIUM; HYDROETHIDINE; UNCOUPLING PROTEIN;

ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CONTROLLED STUDY; EVOKED RESPONSE; HIPPOCAMPUS; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; RAT; TISSUE OXYGENATION; ANIMAL; CELL MEMBRANE POTENTIAL; CYTOLOGY; DOSE RESPONSE; DRUG EFFECT; DRUG INTERACTION; IN VITRO STUDY; METABOLISM; NERVE CELL; NEWBORN; PHYSIOLOGY; RADIATION EXPOSURE; SPRAGUE DAWLEY RAT; TIME;

ANIMALS; ANIMALS, NEWBORN; ANTIOXIDANTS; CARBONYL CYANIDE P-TRIFLUOROMETHOXYPHENYLHYDRAZONE; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; ETHIDIUM; HIPPOCAMPUS; MEMBRANE POTENTIALS; NEURONS; OXYGEN; RATS; RATS, SPRAGUE-DAWLEY; SUPEROXIDES; TIME FACTORS; UNCOUPLING AGENTS;

EID: 34547802699     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.01003.2006     Document Type: Article

References (71)

1. Baydas G, Reiter RJ, Akbulut M, Tuzcu M, Tamer S. Melatonin inhibits neural apoptosis induced by homocysteine in hippocampus of rats via inhibition of cytochrome c translocation and caspase-3 activation and by regulating pro- and anti-apoptotic protein levels. Neuroscience 135: 879-886, 2005.
2. Benov L, Sztejnberg L, Fridovich I. Critical evaluation of the use of hydroethidine as a measure of superoxide anion radical. Free Rad Biol Med 25: 826-831, 1998.
3. Bickler PE, Hansen BM. Hypoxia-tolerant neonatal CA1 neurons: relationship of survival to evoked glutamate release and glutamate receptor-mediated calcium changes in hippocampal slices. Brain Res Dev Brain Res 106: 57-69, 1998.
4. Bindokas VP, Jordan J, Lee CC, Miller RJ. Superoxide production in rat hippocampal neurons: selective imaging with hydroethidine. J Neurosci 16: 1324-1336, 1996.
5. Bingmann D, Kolde G. Burst activity elicited in hippocampal slices by a rise of PO2. Pfluegers Arch 382: R38, 1979.
6. Bingmann D, Kolde G, Speckmann EJ. Effects of elevated pO2 values in the superfusate on the neural activity in hippocampal slices. In: Physiology and Pharmacology of Epileptogenic Phenomenon, edited by Klee MR, Lux HD, Speckmann EJ. New York: Raven, 1982, p. 97-104.
7. Brahma B, Forman RE, Stewart EE, Nicholson C, Rice ME. Ascorbate inhibits edema in brain slices. J Neurochem 74: 1263-1270, 2000.
8. Brewer GJ, Cotman CW. Survival and growth of hippocampal neurons in defined medium at low density: advantages of a sandwich culture technique or low oxygen. Brain Res 494: 65-74, 1989.
9. Budd SL, Castilho RF, Nicholls DG. Mitochondrial membrane potential and hydroethidine-monitored superoxide generation in cultured cerebellar granule cells. FEBS Lett 415: 21-24, 1997.
10. Castilho RF, Ward MW, Nicholls DG. Oxidative stress, mitochondrial function, and acute glutamate excitotoxicity in cultured cerebellar granule cells. J Neurochem 72: 1394-1401, 1999.
11. Chan PH, Kawase M, Murakami K, Chen SF, Li Y, Calagui B, Reola L, Carlson E, Epstein CJ. Overexpression of SOD1 in transgenic rats protects vulnerable neurons against ischemic damage after global cerebral ischemia and reperfusion. J Neurosci 18: 8292-8299, 1998.
12. Dantas APV, Tostes RCA, Fortes ZB, Costa SG, Nigro D, Carvalho MHC. In vivo evidence for antioxidant potential of estrogen in microvessels of female spontaneously hypertensive rats. Hypertension 39: 405-411, 2002.
13. Dean JB, Mulkey DK, Garcia III AJ, Putnam RW, Henderson III RA. Neuronal sensitivity to hyperoxia, hypercapnia and inert gases at hyperbaric pressures. J Appl Physiol 95: 883-909, 2003.
14. Dean JB, Mulkey DK, Henderson III RA, Potter SJ, Putnam RW. Hyperoxia, reactive oxygen species, and hyperventilation: oxygen sensitivity of brain stem neurons. J Appl Physiol 96: 784-791, 2004.
15. Dean JB, Potter SJ, Garcia III, AJ, Henderson III RA, Putnam RW. Oxygen tension profiles differ in rat brain slices superfused on one side versus two sides. FASEB J 19: A645, 2005.
16. Dong H, Xiong L, Zhu Z, Chen S, Hou L, Sakabe T. Preconditioning with hyperbaric oxygen and hyperoxia induces tolerance against spinal cord ischemia in rabbits. Anesthesiology 96: 907-912, 2002.
17. Droge W. Free radicals in the physiological control of cell function. Physiol Rev 82: 47-95, 2002.
18. Emerit J, Edeas M, Bricaire F. Neurodegenerative diseases and oxidative stress. Biomed Pharmacother 58: 39-46, 2004.
19. Fessel J, Arbeson WC, Winder D, Roberts LJ. Standard brain slice protocols result in neuronal oxidative injury in hippocampal brain slices. Free Rad Biol Med 33: S433, 2002.
20. Freiberger JJ, Suliman HB, Sheng H, McAdoo J, Piantadosi CA, Warner DS. A comparison of hyperbaric oxygen versus hypoxic cerebral preconditioning in neonatal rats. Brain Res 1075: 213-222, 2006.
21. Fukui K, Onodera K, Shinkai T, Suzuki S, Urano S. Impairment of learning and memory in rats caused by oxidative stress and aging, and changes in antioxidative defense systems. Ann NY Acad Sci 928: 168-175, 2001.
22. Furuichi T, Liu W, Shi H, Miyake M, Liu KJ. Generation of hydrogen peroxide during brief oxygen-glucose deprivation induces preconditioning neuronal protection in primary cultured neurons. J Neurosci Res 79: 816-824, 2005.
23. Gahtan E, Auerbach JM, Segal M. Reversible impairment of long-term potentiation in transgenic Cu/Zn-SOD mice. Eur J Neurosci 10: 538-544, 1998.
24. Garcia III AJ, Henderson III RA, Putnam RW, Dean JB. Oxidative stress induced by hyperbaric oxygen increases the synaptic response of CA1 neurons in the rat hippocampus. FASEB J 17: A71, 2003.
25. Garcia III, AJ, Henderson III, RA, Putnam RW, Dean JB. Hyperoxia increases neuronal excitability by affecting membrane properties and excitatory input within the CA1 hippocampus. FASEB J 18: A1058, 2004.
26. Garcia III AJ, Henderson III RA, Putnam RW, Pearson JC, Dean JB. Neuronal excitability at 0.95 atmosphere absolute (ATAo2) is elevated relative to a lesser degree of oxygenation in the rat CA1 hippocampus. Soc Neurosci Abstr 729.18, 2005.
27. Gomes A, Fernandes E, Lima JLFC. Fluorescence probes used for detection of reactive oxygen species. J Biochem Biophys Methods 65: 45-80, 2005.
28. Gonenc S, Uysal N, Acikgoz O, Kayatekin BM, Sonmez A, Kiray M, Aksu I, Gulecer B, Topcu A, Semin I. Effects of melatonin on oxidative stress and spatial memory impairment induced by acute ethanol treatment in rats. Physiol Res Acad Scie Bohemoslovaca 54: 341-348, 2005.
29. Graulich J, Hoffmann U, Maier RF, Ruscher K, Pomper JK, Ko HK, Gabriel S, Obladen M, Heinemann U. Acute neuronal injury after hypoxia is influenced by the reoxygenation mode in juvenile hippocampal slice cultures. Brain Res Dev Brain Res 137: 35-42, 2002.
30. Kaplan FS, Brighton CT, Boytim MJ, Selzer ME, Lee V, Spindler K, Silberberg D, Black J. Enhanced survival of rat neonatal cerebral cortical neurons at subatmospheric oxygen tensions in vitro. Brain Res 384: 199-203, 1986.
31. Katoh S, Mitsui Y, Kitani K, Suzuki T. Hyperoxia induces the differentiated neuronal phenotype of PC12 cells by producing reactive oxygen species. Biochem Biophysic Res Commun 241: 347-351, 1997.
32. Kawase M, Murakami K, Fujimura M, Morita-Fujimura Y, Gasche Y, Kondo T, Scott RW, Chan PH. Exacerbation of delayed cell injury after transient global ischemia in mutant mice with CuZn superoxide dismutase deficiency. Stroke 30: 1962-1968, 1999.
33. Kishida KT, Pao M, Holland SM, Klann E. NADPH oxidase is required for NMDA receptor-dependent activation of ERK in hippocampal area CA1. J Neurochem 94: 299-306, 2005.
34. Klann E. Cell-permeable scavengers of superoxide prevent long-term potentiation in hippocampal area CA1. J Neurophysiol 80: 452-457, 1998.
35. Klann E, Roberson E, Knapp L, Sweatt J. A role for superoxide in protein kinase C activation and induction of long-term potentiation. J Bioll Chem 273: 4516-4522, 1998.
36. Klann E, Thiels E. Modulation of protein kinases and protein phosphatases by reactive oxygen species: implications for hippocampal synaptic plasticity. Prog Neuropsychopharmocol Biol Psychiatry 23: 359-376, 1999.
37. Knapp LT, Klann E. Potentiation of hippocampal synaptic transmission by superoxide requires the oxidative activation of protein kinase C. J Neurosci 22: 674-683, 2002.
38. 2+ signalling and changes of mitochondrial function during low-Mg2-induced epileptiform activity in organotypic hippocampal slice cultures. Eur J Neurosci 13: 1311-1319, 2001.
39. Li J, Gao X, Qian M, Eaton JW. Mitochondrial metabolism underlies hyperoxic cell damage. Free Rad Biol Med 36: 1460-1470, 2004.
40. Lynn S, Huang EJ, Elchuri S, Naeemuddin M, Nishinaka Y, Yodoi J, Ferriero DM, Epstein CJ, Huang T-T. Selective neuronal vulnerability and inadequate stress response in superoxide dismutase mutant mice. Free Rad Biol Med 38: 817-828, 2005.
41. Maharaj DS, Maharaj H, Antunes EM, Maree DM, Nyokong T, Glass BD, Daya S. 6-Hydroxymelatonin protects against quinolinic-acid-induced oxidative neurotoxicity in the rat hippocampus. J Pharmacy Pharmacol 57: 877-881, 2005.
42. McCord JM. Superoxide radical: controversies, contradictions, and paradoxes. Proc Soc Exp Biol Med 209: 112-117, 1995.
43. Moncada S, Bolanos JP. Nitric oxide, cell bioenergetics and neurodegeneration. J Neurochem 97: 1676-1689, 2006.
44. Morgan AR, Evans DH, Lee JS, Pulleyblank DE. Review: ethidium fluorescence assay. II. Enzymatic studies and DNA-protein interactions. Nucl Acids Res 7: 571-594, 1979.
45. Mulkey DK, Henderson III RA, Olson JE, Putnam RW, Dean JB. Oxygen measurement in brainstem slices exposed to normobaric hyperoxia and hyperbaric oxygen. J Appl Physiol 90: 1887-1899, 2001.
46. Murakami K, Kondo T, Kawase M, Li Y, Sato S, Chen SF, Chan PH. Mitochondrial susceptibility to oxidative stress exacerbates cerebral infarction that follows permanent focal cerebral ischemia in mutant mice with manganese superoxide dismutase deficiency. J Neurosci 18: 205-213, 1998.
47. Muranyi M, Li P-A. Hyperglycemia increases superoxide production in the CA1 pyramidal neurons after global cerebral ischemia. Neurosci Lett 393: 119-121, 2006.
48. Nakamura K, Bindokas VP, Kowlessur D, Elas M, Milstien S, Marks JD, Halpern HJ, Kang UJ. Tetrahydrobiopterin scavenges superoxide in dopaminergic neurons. J Biol Chem 276: 34402-34407, 2001.
49. Nicholls DG. Mitochondrial dysfunction and glutamate excitotoxicity studied in primary neuronal cultures. Curr Mol Med 4: 149-177, 2004.
50. Nie H, Xiong L, Lao N, Chen S, Xu N, Zhu Z. Hyperbaric oxygen preconditioning induces tolerance against spinal cord ischemia by upregulation of antioxidant enzymes in rabbits. J Cereb Blood Flow Metab 26: 666-674, 2006.
51. Onodera K, Omoi N-O, Fukui K, Hayasaka T, Shinkai T, Suzuki S, Abe K, Urano S. Oxidative damage of rat cerebral cortex and hippocampus, and changes in antioxidative defense systems caused by hyperoxia. Free Rad Res 37: 367-372, 2003.
52. Peterson SL, Morrow D, Liu S, Liu KJ. Hydroethidine detection of superoxide production during the lithium-pilocarpine model of status epilepticus. Epilepsy Res 49: 226-238, 2002.
53. Pinheiro AC, Gomez RS, Massensini AR, Cordeiro MN, Richardson M, Romano-Silva MA, Prado MA, De Marco L, Gomez MV. Neuroprotective effect on brain injury by neurotoxins from the spider Phoneutria nigriventer. Neurochem Int 49: 543-547, 2006.
54. Pomper JK, Graulich J, Kovacs R, Hoffmann U, Gabriel S, Heinemann U. High oxygen tension leads to acute cell death in organotypic hippocampal slice cultures. Brain Res Dev Brain Res 126: 109-116, 2001.
55. Prehn JH. Mitochondrial transmembrane potential and free radical production in excitotoxic neurodegeneration. Naunyn-Schmiedebergs Arch Pharmacol 357: 316-322, 1998.
56. Ravati A, Ahlemeyer B, Becker A, Krieglstein J. Preconditioning-induced neuroprotection is mediated by reactive oxygen species. Brain Res 866: 23-32, 2000.
57. Rice ME. Use of ascorbate in the preparation and maintenance of brain slices. Methods Enzymol 18: 144-149, 1999.
58. Rice ME, Forman RE, Chen BT, Avshalumov MV, Cragg SJ, Drew KL. Brain antioxidant regulation in mammals and anoxia-tolerant reptiles: balanced for neuroprotection and neuromodulation. Comp Biochem Physiol Toxicol Pharmacol 133: 515-525, 2002.
59. Rice ME, Perez-Pinzon MA, Lee EJK. Ascorbic acid, but not glutathione, is taken up by brain slices and preserves cell morphology. J Neurophysiol 71: 1591-1596, 1994.
60. Scanlon JM, Reynolds IJ. Effects of oxidants and glutamate receptor activation on mitochondrial membrane potential in rat forebrain neurons. J Neurochem 71: 2392-2400, 1998.
61. Sengpiel B, Preis E, Krieglstein J, Prehn JH. NMDA-induced superoxide production and neurotoxicity in cultured rat hippocampal neurons: role of mitochondria. Eur J Neurosci 10: 1903-1910, 1998.
62. Serrano F, Klann E. Reactive oxygen species and synaptic plasticity in the aging hippocampus. Ageing Res Rev 3: 431-443, 2004.
63. Shibata M, Blatteis CM. High perfusate PO2 impairs thermosensitivity of hypothalamic thermosensitive neurons in slice preparations. Brain Res Bull 26: 467-471, 1991.
64. Shimabuku R, Ota A, Pereyra S, Veliz B, Paz E, Nakachi G, More M, Oliveros M. Hyperoxia with 100% oxygen following hypoxia-ischemia increases brain damage in newborn rats. Biol Neonate 88: 168-171, 2005.
65. Sugawara T, Chan PH. Reactive oxygen radicals and pathogenesis of neuronal death after cerebral ischemia. Antioxidants Redox Signal 5: 597-607, 2003.
66. Uchida K, Samejima M, Okabe A, Fukuda A. Neuroprotective effects of melatonin against anoxia/aglycemia stress, as assessed by synaptic potentials and superoxide production in rat hippocampal slices. J Pineal Res 37: 215-222, 2004.
67. Wang T, Liu B, Qin L, Wilson B, Hong JS. Protective effect of the SOD/catalase mimetic MnTMPyP on inflammation-mediated dopaminergic neurodegeneration in mesencephalic neuronal-glial cultures. J Neuroimmunol 147: 68-72, 2004.
68. Weinstock M, Shoham S. Rat models of dementia based on reductions in regional glucose metabolism, cerebral blood flow and cytochrome oxidase activity. J Neural Transmission 111: 347-366, 2004.
69. Wilde GJ, Pringle AK, Wright P, Iannotti F. Differential vulnerability of the CA1 and CA3 subfields of the hippocampus to superoxide and hydroxyl radicals in vitro. J Neurochem 69: 883-886, 1997.
70. Zhao H, Kalivendi S, Zhang H, Joseph J, Nithipatikom K, Vasquez-Vivar J, Kalyanaraman B. Superoxide reacts with hydroethidine but forms a fluorescent product that is distinctly different from ethidium: potential implications in intracellular fluorescence detection of superoxide. Free Rad Biol Med 34: 1359-1368, 2003.
71. Zuo L, Clanton TL. Detection of reactive oxygen species and nitrogen species in tissues using redox-sensitive fluorescent probes. Methods Enzymol 352: 307-325, 2002.