Increased NADPH oxidase-derived superoxide is involved in the neuronal cell death induced by hypoxiaischemia in neonatal hippocampal slice cultures

Free Radical Biology and Medicine

Volumn 53, Issue 5, 2012, Pages 1139-1151

  Lu, Qing ^a   Wainwright, Mark S ^b   Harris, Valerie A ^a   Aggarwal, Saurabh ^a   Hou, Yali ^a   Rau, Thomas ^c   Poulsen, David J ^c   Black, Stephen M ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c University of Missoula   (United States)

Author keywords

Apoptosis; Free radicals; Hydrogen peroxide; Hypoxiaischemia; NADPH oxidase; Neonatal brain; Neuronal cell death; p38MAP kinase; p47phox; Superoxide

Indexed keywords

APOCYNIN; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN P47; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE;

ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN SLICE; CELL DEATH; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; HIPPOCAMPUS; HYPOXIC ISCHEMIC ENCEPHALOPATHY; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; RAT;

ACETOPHENONES; ANIMALS; ANIMALS, NEWBORN; CELL DEATH; GLUCOSE; HIPPOCAMPUS; HYPOXIA-ISCHEMIA, BRAIN; MICROTOMY; NADPH OXIDASE; NEURONS; ORGAN CULTURE TECHNIQUES; OXYGEN; RATS; RATS, SPRAGUE-DAWLEY; SUPEROXIDES;

ADENO-ASSOCIATED VIRUS; RATTUS;

EID: 84865464576     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2012.06.012     Document Type: Article

References (72)

1. K.E. Smith, S. Keeney, L. Zhang, J.R. Perez-Polo, and D.K. Rassin The association of early blood oxygenation with child development in preterm infants with acute respiratory disorders Int. J. Dev. Neurosci. 26 2008 125 131
2. H.C. Glass, and D.M. Ferriero Treatment of hypoxicischemic encephalopathy in newborns Curr. Treat. Options Neurol 9 2007 414 423
3. J.M. Perlman Intervention strategies for neonatal hypoxicischemic cerebral injury Clin. Ther. 28 2006 1353 1365
4. P. Lipton Ischemic cell death in brain neurons Physiol. Rev. 79 1999 1431 1568
5. L.J. Martin, A.M. Brambrink, A.C. Price, A. Kaiser, D.M. Agnew, R.N. Ichord, and R.J. Traystman Neuronal death in newborn striatum after hypoxiaischemia is necrosis and evolves with oxidative stress Neurobiol. Dis. 7 2000 169 191
6. A.N. Clarkson, B.A. Sutherland, and I. Appleton The biology and pathology of hypoxiaischemia: an update Arch. Immunol. Ther. Exp. (Warsaw) 53 2005 213 225
7. C. Cheret, A. Gervais, A. Lelli, C. Colin, L. Amar, P. Ravassard, J. Mallet, A. Cumano, K.H. Krause, and M. Mallat Neurotoxic activation of microglia is promoted by a nox1-dependent NADPH oxidase J. Neurosci. 28 2008 12039 12051
8. K. Al-Hathlol, S. Phillips, M.K. Seshia, O. Casiro, R.E. Alvaro, and H. Rigatto Alveolar capillary dysplasia: report of a case of prolonged life without extracorporeal membrane oxygenation (ECMO) and review of the literature Early Hum. Dev. 57 2000 85 94
9. P. Zhang, M. Hou, Y. Li, X. Xu, M. Barsoum, Y. Chen, and R.J. Bache NADPH oxidase contributes to coronary endothelial dysfunction in the failing heart Am. J. Physiol. Heart Circ. Physiol 296 2009 H840 846
10. S.W. Suh, B.S. Shin, H. Ma, M. Van Hoecke, A.M. Brennan, M.A. Yenari, and R.A. Swanson Glucose and NADPH oxidase drive neuronal superoxide formation in stroke Ann. Neurol. 64 2008 654 663
11. A.M. Brennan, S.W. Suh, S.J. Won, P. Narasimhan, T.M. Kauppinen, H. Lee, Y. Edling, P.H. Chan, and R.A. Swanson NADPH oxidase is the primary source of superoxide induced by NMDA receptor activation Nat. Neurosci. 12 2009 857 863
12. K. Bedard, and K.H. Krause The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology Physiol. Rev. 87 2007 245 313
13. J.L. Johnson, J.W. Park, J.E. Benna, L.P. Faust, O. Inanami, and B.M. Babior Activation of p47(PHOX), a cytosolic subunit of the leukocyte NADPH oxidase: phosphorylation of ser-359 or ser-370 precedes phosphorylation at other sites and is required for activity J. Biol. Chem. 273 1998 35147 35152
14. C.E. Walder, S.P. Green, W.C. Darbonne, J. Mathias, J. Rae, M.C. Dinauer, J.T. Curnutte, and G.R. Thomas Ischemic stroke injury is reduced in mice lacking a functional NADPH oxidase Stroke 28 1997 2252 2258
15. T. Cronberg, A. Rytter, F. Asztely, A. Soder, and T. Wieloch Glucose but not lactate in combination with acidosis aggravates ischemic neuronal death in vitro Stroke 35 2004 753 757
16. J.Y. Khan, and S.M. Black Developmental changes in murine brain antioxidant enzymes Pediatr. Res. 54 2003 77 82
17. Q. Lu, T.F. Rau, V. Harris, M. Johnson, D.J. Poulsen, and S.M. Black Increased p38 mitogen-activated protein kinase signaling is involved in the oxidative stress associated with oxygen and glucose deprivation in neonatal hippocampal slice cultures Eur. J. Neurosci. 34 2011 1093 1101
18. S. Zolotukhin, B.J. Byrne, E. Mason, I. Zolotukhin, M. Potter, K. Chesnut, C. Summerford, R.J. Samulski, and N. Muzyczka Recombinant adeno-associated virus purification using novel methods improves infectious titer and yield Gene Ther 6 1999 973 985
19. S. Levine Anoxicischemic encephalopathy in rats Am. J. Pathol. 36 1960 1 17
20. J.E. Rice 3rd, R.C. Vannucci, and J.B. Brierley The influence of immaturity on hypoxicischemic brain damage in the rat Ann. Neurol. 9 1981 131 141
21. - and systolic blood pressure in mice Circ. Res. 89 2001 408 414
22. J.B. Bederson, L.H. Pitts, S.M. Germano, M.C. Nishimura, R.L. Davis, and H.M. Bartkowski Evaluation of 2,3,5-triphenyltetrazolium chloride as a stain for detection and quantification of experimental cerebral infarction in rats Stroke 17 1986 1304 1308
23. R.A. Swanson, M.T. Morton, G. Tsao-Wu, R.A. Savalos, C. Davidson, and F.R. Sharp A semiautomated method for measuring brain infarct volume J. Cereb. Blood Flow Metab. 10 1990 290 293
24. T.N. Lin, Y.Y. He, G. Wu, M. Khan, and C.Y. Hsu Effect of brain edema on infarct volume in a focal cerebral ischemia model in rats Stroke 24 1993 117 121
25. K.L. Quick, and L.L. Dugan Superoxide stress identifies neurons at risk in a model of ataxia-telangiectasia Ann. Neurol. 49 2001 627 635
26. D. Hu, F. Serrano, T.D. Oury, and E. Klann Aging-dependent alterations in synaptic plasticity and memory in mice that overexpress extracellular superoxide dismutase J. Neurosci. 26 2006 3933 3941
27. F. Yu, T. Sugawara, and P.H. Chan Treatment with dihydroethidium reduces infarct size after transient focal cerebral ischemia in mice Brain Res. 978 2003 223 227
28. S.A. Saeed, K.F. Shad, T. Saleem, F. Javed, and M.U. Khan Some new prospects in the understanding of the molecular basis of the pathogenesis of stroke Exp. Brain Res. 182 2007 1 10
29. N. Opitz, G.R. Drummond, S. Selemidis, S. Meurer, and H.H. Schmidt The 'A's and 'O's of NADPH oxidase regulation: a commentary on "Subcellular localization and function of alternatively spliced Noxo1 isoforms" Free Radic. Biol. Med. 42 2007 175 179
30. C. Meischl, and D. Roos The molecular basis of chronic granulomatous disease Springer Semin. Immunopathol. 19 1998 417 434
31. S.H. Jackson, J.I. Gallin, and S.M. Holland The p47phox mouse knock-out model of chronic granulomatous disease J. Exp. Med. 182 1995 751 758
32. T. Aoki, M. Nishimura, H. Kataoka, R. Ishibashi, K. Nozaki, and N. Hashimoto Reactive oxygen species modulate growth of cerebral aneurysms: a study using the free radical scavenger edaravone and p47phox(-/-) mice Lab. Invest. 89 2009 730 741
33. G.S. Kim, J.E. Jung, K. Niizuma, and P.H. Chan CK2 is a novel negative regulator of NADPH oxidase and a neuroprotectant in mice after cerebral ischemia J. Neurosci. 29 2009 14779 14789
34. H. Chen, Y.S. Song, and P.H. Chan Inhibition of NADPH oxidase is neuroprotective after ischemiareperfusion J. Cereb. Blood Flow Metab. 29 2009 1262 1272
35. Q. Wang, K.D. Tompkins, A. Simonyi, R.J. Korthuis, A.Y. Sun, and G.Y. Sun Apocynin protects against global cerebral ischemiareperfusion-induced oxidative stress and injury in the gerbil hippocampus Brain Res. 1090 2006 182 189
36. L. He, X. Liu, J. Chen, B. Dinger, L. Stensaas, and S. Fidone Modulation of chronic hypoxia-induced chemoreceptor hypersensitivity by NADPH oxidase subunits in rat carotid body J. Appl. Physiol. 108 2010 1304 1310
37. W.M. Nauseef, B.D. Volpp, S. McCormick, K.G. Leidal, and R.A. Clark Assembly of the neutrophil respiratory burst oxidase. protein kinase C promotes cytoskeletal and membrane association of cytosolic oxidase components J. Biol. Chem. 266 1991 5911 5917
38. P.M. Dang, A. Fontayne, J. Hakim, J. El Benna, and A. Perianin Protein kinase C zeta phosphorylates a subset of selective sites of the NADPH oxidase component p47phox and participates in formyl peptide-mediated neutrophil respiratory burst J. Immunol 166 2001 1206 1213
39. E.P. Reeves, L.V. Dekker, L.V. Forbes, F.B. Wientjes, A. Grogan, D.J. Pappin, and A.W. Segal Direct interaction between p47phox and protein kinase C: evidence for targeting of protein kinase C by p47phox in neutrophils Biochem. J. 344 1999 859 866
40. T. Yamamori, O. Inanami, H. Nagahata, Y. Cui, and M. Kuwabara Roles of p38 MAPK, PKC and PI3-K in the signaling pathways of NADPH oxidase activation and phagocytosis in bovine polymorphonuclear leukocytes FEBS Lett 467 2000 253 258
41. G.E. Brown, M.Q. Stewart, S.A. Bissonnette, A.E. Elia, E. Wilker, and M.B. Yaffe Distinct ligand-dependent roles for p38 MAPK in priming and activation of the neutrophil NADPH oxidase J. Biol. Chem. 279 2004 27059 27068
42. C. Dewas, M. Fay, M.A. Gougerot-Pocidalo, and J. El-Benna The mitogen-activated protein kinase extracellular signal-regulated kinase 1/2 pathway is involved in formyl-methionyl-leucyl-phenylalanine-induced p47phox phosphorylation in human neutrophils J. Immunol 165 2000 5238 5244
43. H. Fujimoto, M. Ohno, S. Ayabe, H. Kobayashi, N. Ishizaka, H. Kimura, K. Yoshida, and R. Nagai Carbon monoxide protects against cardiac ischemiareperfusion injury in vivo via MAPK and AkteNOS pathways Arterioscler. Thromb. Vasc. Biol. 24 2004 1848 1853
44. F. Amersi, X.D. Shen, D. Anselmo, J. Melinek, S. Iyer, D.J. Southard, M. Katori, H.D. Volk, R.W. Busuttil, R. Buelow, and J.W. Kupiec-Weglinski Ex vivo exposure to carbon monoxide prevents hepatic ischemia/reperfusion injury through p38 MAP kinase pathway Hepatology 35 2002 815 823
45. F.C. Barone, E.A. Irving, A.M. Ray, J.C. Lee, S. Kassis, S. Kumar, A.M. Badger, J.J. Legos, J.A. Erhardt, E.H. Ohlstein, A.J. Hunter, D.C. Harrison, K. Philpott, B.R. Smith, J.L. Adams, and A.A. Parsons Inhibition of p38 mitogen-activated protein kinase provides neuroprotection in cerebral focal ischemia Med. Res. Rev. 21 2001 129 145
46. A.S. Borders, L. de Almeida, L.J. Van Eldik, and D.M. Watterson The p38alpha mitogen-activated protein kinase as a central nervous system drug discovery target BMC Neurosci. 9 Suppl. 2 2008 S12
47. A. Sun, M. Liu, X.V. Nguyen, and G. Bing p38 MAP kinase is activated at early stages in Alzheimer's disease brain Exp. Neurol. 183 2003 394 405
48. F.C. Barone, E.A. Irving, A.M. Ray, J.C. Lee, S. Kassis, S. Kumar, A.M. Badger, R.F. White, M.J. McVey, J.J. Legos, J.A. Erhardt, A.H. Nelson, E.H. Ohlstein, A.J. Hunter, K. Ward, B.R. Smith, J.L. Adams, and A.A. Parsons SB 239063, a second-generation p38 mitogen-activated protein kinase inhibitor, reduces brain injury and neurological deficits in cerebral focal ischemia J. Pharmacol. Exp. Ther. 296 2001 312 321
49. J.J. Legos, J.A. Erhardt, R.F. White, S.C. Lenhard, S. Chandra, A.A. Parsons, R.F. Tuma, and F.C. Barone SB 239063, a novel p38 inhibitor, attenuates early neuronal injury following ischemia Brain Res. 892 2001 70 77
50. J. El Benna, J. Han, J.W. Park, E. Schmid, R.J. Ulevitch, and B.M. Babior Activation of p38 in stimulated human neutrophils: phosphorylation of the oxidase component p47phox by p38 and ERK but not by JNK Arch. Biochem. Biophys. 334 1996 395 400
51. I.A. Manke, A. Nguyen, D. Lim, M.Q. Stewart, A.E. Elia, and M.B. Yaffe MAPKAP kinase-2 is a cell cycle checkpoint kinase that regulates the G2/M transition and S phase progression in response to UV irradiation Mol. Cell 17 2005 37 48
52. T. Yamamori, O. Inanami, H. Sumimoto, T. Akasaki, H. Nagahata, and M. Kuwabara Relationship between p38 mitogen-activated protein kinase and small GTPase Rac for the activation of NADPH oxidase in bovine neutrophils Biochem. Biophys. Res. Commun. 293 2002 1571 1578
53. P.M. Dang, A. Stensballe, T. Boussetta, H. Raad, C. Dewas, Y. Kroviarski, G. Hayem, O.N. Jensen, M.A. Gougerot-Pocidalo, and J. El-Benna A specific p47phox-serine phosphorylated by convergent MAPKs mediates neutrophil NADPH oxidase priming at inflammatory sites J. Clin. Invest. 116 2006 2033 2043
54. J. Raingeaud, A.J. Whitmarsh, T. Barrett, B. Derijard, and R.J. Davis MKK3- and MKK6-regulated gene expression is mediated by the p38 mitogen-activated protein kinase signal transduction pathway Mol. Cell. Biol. 16 1996 1247 1255
55. B. Derijard, J. Raingeaud, T. Barrett, I.H. Wu, J. Han, R.J. Ulevitch, and R.J. Davis Independent human MAP-kinase signal transduction pathways defined by MEK and MKK isoforms Science 267 1995 682 685
56. B. Ge, H. Gram, F. Di Padova, B. Huang, L. New, R.J. Ulevitch, Y. Luo, and J. Han MAPKK-independent activation of p38alpha mediated by Table1-dependent autophosphorylation of p38alpha Science 295 2002 1291 1294
57. B.F. Trump, and I.K. Berezesky Calcium-mediated cell injury and cell death FASEB J 9 1995 219 228
58. U. Wojda, E. Salinska, and J. Kuznicki Calcium ions in neuronal degeneration IUBMB Life 60 2008 575 590
59. T. Kristian, and B.K. Siesjo Calcium in ischemic cell death Stroke 29 1998 705 718
60. 2/calmodulin-dependent protein kinase II: potential role in neuronal damage J. Neurochem. 58 1992 1743 1753
61. E.K. Kelly, L. Wang, and L.B. Ivashkiv Calcium-activated pathways and oxidative burst mediate zymosan-induced signaling and IL-10 production in human macrophages J. Immunol 184 2010 5545 5552
62. D. Pandey, J.P. Gratton, R. Rafikov, S.M. Black, and D.J. Fulton Calcium/calmodulin-dependent kinase II mediates the phosphorylation and activation of NADPH oxidase 5 Mol. Pharmacol. 80 2011 407 415
63. R.S. Arnold, J. Shi, E. Murad, A.M. Whalen, C.Q. Sun, R. Polavarapu, S. Parthasarathy, and J.A. Petros Lambeth, J. D. Hydrogen peroxide mediates the cell growth and transformation caused by the mitogenic oxidase Nox1 Proc. Natl. Acad. Sci. USA 98 2001 5550 5555
64. F. Serrano, N.S. Kolluri, F.B. Wientjes, J.P. Card, and E. Klann NADPH oxidase immunoreactivity in the mouse brain Brain Res. 988 2003 193 198
65. M. Ibi, M. Katsuyama, C. Fan, K. Iwata, T. Nishinaka, T. Yokoyama, and C. Yabe-Nishimura NOX1/NADPH oxidase negatively regulates nerve growth factor-induced neurite outgrowth Free Radic. Biol. Med. 40 2006 1785 1795
66. P. Vallet, Y. Charnay, K. Steger, E. Ogier-Denis, E. Kovari, F. Herrmann, J.P. Michel, and I. Szanto Neuronal expression of the NADPH oxidase NOX4, and its regulation in mouse experimental brain ischemia Neuroscience 132 2005 233 238
67. I. Kusaka, G. Kusaka, C. Zhou, M. Ishikawa, A. Nanda, D.N. Granger, J.H. Zhang, and J. Tang Role of AT1 receptors and NAD(P)H oxidase in diabetes-aggravated ischemic brain injury Am. J. Physiol. Heart Circ. Physiol 286 2004 H2442 2451
68. Q.G. Zhang, L. Raz, R. Wang, D. Han, L. De Sevilla, F. Yang, R.K. Vadlamudi, and D.W. Brann Estrogen attenuates ischemic oxidative damage via an estrogen receptor alpha-mediated inhibition of NADPH oxidase activation J. Neurosci. 29 2009 13823 13836
69. K.A. Jackman, A.A. Miller, G.R. Drummond, and C.G. Sobey Importance of NOX1 for angiotensin II-induced cerebrovascular superoxide production and cortical infarct volume following ischemic stroke Brain Res. 1286 2009 215 220
70. L. Serrander, L. Cartier, K. Bedard, B. Banfi, B. Lardy, O. Plastre, A. Sienkiewicz, L. Forro, W. Schlegel, and K.H. Krause NOX4 activity is determined by mRNA levels and reveals a unique pattern of ROS generation Biochem. J. 406 2007 105 114
71. A. Shiino, M. Matsuda, J. Handa, and B. Chance Poor recovery of mitochondrial redox state in CA1 after transient forebrain ischemia in gerbils Stroke 29 1998 2421 2424 discussion 2425
72. D. Newrzella, P.S. Pahlavan, C. Kruger, C. Boehm, O. Sorgenfrei, H. Schrock, G. Eisenhardt, N. Bischoff, G. Vogt, O. Wafzig, M. Rossner, M.H. Maurer, H. Hiemisch, A. Bach, W. Kuschinsky, and A. Schneider The functional genome of CA1 and CA3 neurons under native conditions and in response to ischemia BMC Genomics 8 2007 370