Suppression of reactive oxygen species production enhances neuronal survival in vitro and in vivo in the anoxia-tolerant turtle Trachemys scripta

Journal of Neurochemistry

Volumn 101, Issue 4, 2007, Pages 993-1001

  Milton, Sarah L ^a   Nayak, Gauri ^b   Kesaraju, Shailaja ^a   Kara, Laurie ^a   Prentice, Howard M ^b  

^a FLORIDA ATLANTIC UNIVERSITY   (United States)

^b FLORIDA ATLANTIC UNIVERSITY   (United States)

Author keywords

Adenosine; Anoxia; Reactive oxygen species; Reoxygenation; Trachemys scripta

Indexed keywords

2 CHLORO 6 N CYCLOPENTYLADENOSINE; 2,3 DIHYDROXYBENZOIC ACID; 8 CYCLOPENTYL 1,3 DIPROPYLXANTHINE; ADENOSINE; ADENOSINE RECEPTOR; ADENOSINE RECEPTOR STIMULATING AGENT; ANTIOXIDANT; FRESH WATER; HYDROGEN PEROXIDE; HYDROXYL GROUP; REACTIVE OXYGEN METABOLITE; SALICYLIC ACID;

ADAPTATION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANOXIA; ARTICLE; CELL DEATH; CELL SURVIVAL; CONTROLLED STUDY; CORPUS STRIATUM; FEMALE; IN VITRO STUDY; IN VIVO STUDY; MEASUREMENT; MICRODIALYSIS; NERVE CELL; NERVE CELL CULTURE; NONHUMAN; PHYSIOLOGY; PRIORITY JOURNAL; REOXYGENATION; TURTLE;

ADENOSINE DIPHOSPHATE; ANIMALS; ANOXEMIA; BRAIN; CELL SURVIVAL; CELLS, CULTURED; HYDROGEN PEROXIDE; MICRODIALYSIS; NEURONS; OXYGEN; PHOSPHOPYRUVATE HYDRATASE; REACTIVE OXYGEN SPECIES; TIME FACTORS; TURTLES; XANTHINES;

MAMMALIA; TESTUDINES; TRACHEMYS SCRIPTA;

EID: 34247566150     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2007.04466.x     Document Type: Article

References (61)

1. Atkuri K. R., Herzenberg L. A. Herzenberg L. A. (2005) Culturing at atmospheric oxygen levels impacts lymphocyte function. Proc. Natl Acad. Sci. 102, 3756 3759.
2. Belkin D. A. (1963) Anoxia: tolerance in reptiles. Science 139, 492 93.
3. Bickler P. E. Gallego S. M. (1993) Inhibition of brain calcium channels by plasma proteins from anoxic turtles. Am. J. Physiol. 265, R277 R281.
4. Bickler P. E., Donohoe P. H. Buck L. T. (2000) Hypoxia-induced silencing of NMDA receptors in turtle neurons. J. Neurosci. 20, 3522 3528.
5. Brewer G. J. (1997) Isolation and culture of adult rat hippocampal neurons. J. Neurosci. Meth. 71, 143 155.
6. Carney J. M. Floyd R. A. (1991) Protection against oxidative damage to CNS by alpha-phenyl-tert-butyl nitrone (PBN) and other spin-trapping agents: a novel series of nonlipid free radical scavengers. J. Mol. Neurosci. 3, 47 57.
7. Chi C. W., Wang C. N., Lin Y. L., Chen C. F. Shiao Y. J. (2005) Tournefolic acid B methyl ester attenuates glutamate-induced toxicity by blockade of ROS accumulation and abrogating the activation of caspases and JNK in rat cortical neurons. J. Neurochem. 92, 692 700.
8. Chiueh C. C., Krishna G., Tulsi P., Obata T., Lang K., Huang S. J. Murphy D. L. (1992) Intracerebral microdialysis of salicylic acid to detect hydroxyl radical generation trough dopamine auto-oxidation in the caudate nucleus: effect of MPP+. Free Rad. Biol. Med. 13, 581 583.
9. Coudray C. Favier A. (2000) Determination of salicylate hydroxylation products as an in vivo oxidative stress marker. Free Rad. Biol. Med. 29, 1064 1070.
10. Ferger B., Eberhardt O., Teismann P., de Groote C. Schulz J. B. (1999) Malonate-induced generation of reactive oxygen species in rat striatum depends on dopamine release but not NMDA receptor activation. J. Neurochem. 73, 1329 1332.
11. Fernandes J. A., Lutz P. L., Tannenbaum A., Todorov A. T., Liebovitch L. Vertes R. (1997) Electroencephalogram activity in the anoxic turtle brain. Am. J. Physiol. 273, R911 R919.
12. Floyd R. A. Carney J. M. (1992) Free radical damage to protein and DNA: mechanisms involved and relevant observations on brain undergoing oxidative stress. Lab. Invest. 47, 412 426.
13. Gabai V. L., Meriin A. B., Yaglom J. A., Wei J. Y., Mosser D. P. Sherman M. Y. (2000) Suppression of stress kinase JNK is involved in HSP72-mediated protection of myogenic cells from transient energy deprivation HSP72 alleviates the stress-induced inhibition of JNK dephosphorylation. J. Biol. Chem. 275, 38088 38094.
14. Globus M. Y., Alonso O., Dietrich W. D., Busto R. Ginsberg M. D. (1995a) Glutamate release and free radical production following brain injury: effects of posttraumatic hypothermia. J. Neurochem. 65, 1704 1711.
15. Globus M. Y., Busto R., Lin B., Shnippering H. Ginsberg M. D. (1995b) Detection of free radical activity during transient global ischemia and recirculation: effects of intraischemic brain temperature modulation. J. Neurochem. 65, 1250 1256.
16. Gum E. T., Swanson R. A., Alano C., Liu J., Hong S., Weinstein P. R. Panter S. S. (2004) Human serum albumin and its N-terminal tetrapeptide (DAHK) block oxidant-induced neuronal death. Stroke. 35, 590 595.
17. Gupta Y, Sinha K, Chaudhary G Jagannathan N. (2002) Protective effect of adenosine against neuronal injury induced by middle cerebral artery occlusion in rats as evidenced by diffusion-weighted imaging. Pharmacol. Biochem. Behav. 72, 569 576.
18. Hara S., Mukai T., Kurosaki K., Kuriiwa F. Endo T. (2004) Characterization of hydroxyl radical generation in the striatum of free-moving rats due to carbon monoxide poisoning, as determined by in vivo microdialysis. Brain Res. 1016, 281 284.
19. Hashimoto T., Yonetani M. Nakamura H. (2003) Selective brain hypothermia protects against hypoxic-ischemic injury in newborn rats by reducing hydroxyl radical production. Kobe J. Med. Sci. 49 (4 83 91.
20. Higashi H., Meno J. R., Marwaha A. S. Winn H. R. (2002) Hippocampal injury and neurobehavioral deficits following hyperglycemic cerebral ischemia: effect of theophylline and ZM 241385. J. Neurosurg. 96 (1 117 126.
21. Huang C. C., Lajevardi N. S., Tammela O., Pastuszko A., Delivoria-Papadopoulos M. Wilson D. F. (1994) Relationship of extracellular dopamine in striatum of newborn piglets to cortical oxygen pressure. Neurochem. Res. 19, 649 655.
22. Jackson D. C. (2000) Living without oxygen: lessons from the freshwater turtle. Comp. Biochem. Physiol. A. 125, 299 315.
23. Jiang A., Zhang Y., Chen X., Lam P. Y., Yang H., Xu Q. Yu A. C. (2002) Activation of Erk1/2 and Akt in astrocytes under ischemia. Biochem. Biophys. Res. Commun. 294, 726 733.
24. Kahlert S., Zundorf G. Reiser G. (2005) Glutamate-mediated influx of extracellular Ca2 + is coupled with reactive oxygen species generation in cultured hippocampal neurons but not in astrocytes. J. Neurosci. Res. 79, 262 271.
25. Kulinsky V. I., Minakina L. N. Usov L. A. (2001) Role of adenosine receptors in neuroprotective effect during global cerebral ischemia. Bull. Exp. Biol. Med. 131, 454 456.
26. Lancelot E., Revaud M. L., Boulu R. G., Plotkine M., Callebert J. (1998) A microdialysis study investigating the mechanisms of hydroxyl radical formation in rat striatum exposed to glutamate. Brain Res. 809, 294 296.
27. Laplanche L., Kamenka J. M. Barbanel G. (2000) The novel-non-competetive NMDA antagonist gacycline blocks the glutamate-induced hydroxyl radicals release in the striatum when dizocilpine don't. A microdialysis study in rats. Neurosci. Lett. 289, 49 52.
28. Lutz P. L. Manuel L. (1999) Maintenance of adenosine A1 receptor function during long term anoxia in the turtle brain. Am. J. Physiol. 276, R633 R636.
29. Lutz P. L. Milton S. L. (2004) Negotiating brain anoxia survival in the turtle. J. Exp. Biol. 207, 3141 3147.
30. Lutz P. L., Nilsson G. E. Prentice H. (2003) The Brain without Oxygen: Causes of Failure Molecular and Physiological Mechanisms for Survival Third edition. Kluwers Press, Dordrecht.
31. Milton S. L Lutz P. L. (1998) Low extracellular dopamine levels are maintained in the anoxic turtle brain. J. Cereb. Blood Flow Metab. 18, 803 807.
32. Milton S. L. Lutz P. L. (2005) Adenosine and ATP sensitive potassium channels modulate dopamine release in the anoxic turtle (Trachemys scripta) striatum. Am. J. Physiol. 289, R77 R83.
33. Milton S. L., Thompson J. W. Lutz P. L. (2002) Mechanisms for maintaining extracellular glutamate in the anoxic turtle striatum. Am. J. Physiol. 282, R1317 R1323.
34. Morimoto T., Globus M. Y., Busto R., Martinez E. Ginsberg M. D. (1996) Simultaneous measurement of salicylate hydroxylation and glutamate release in the penumbral cortex following transient middle cerebral artery occlusion in rats. J. Cereb. Blood Flow Metab. 16, 92 99.
35. Nagy K., Kis B., Rajapake N. C., Bari F. Busija D. W. (2004) Diazoxide preconditioning protects against neuronal cell death by attenuation of oxidative stress upon glutamate stimulation. J. Neurosci. Res. 76, 697 704.
36. Nilsson G. E. Lutz P. L. (1991) Release of inhibitory neurotransmitters in response to anoxia in turtle brain. Am. J. Physiol. 261, R32 R37.
37. Nilsson G. E. Lutz P. L. (1992) Adenosine release in the anoxic turtle brain: a possible mechanism for anoxic survival. J. Exp. Biol. 162, 345 351.
38. Nilsson G. N., Lutz P. L. Jackson T. L. (1991) Neurotransmitters and anoxic survival in the brain: A comparison of anoxia-tolerant and anoxia-intolerant vertebrates. Physiol. Zool. 64, 638 652.
39. Obata T. (2002) Dopamine efflux by MPTP and hydroxyl radical generation. J. Neural Transm, 109, 1159 1180.
40. Pek M. Lutz P. L. (1997) Role for adenosine in "channel arrest" in the anoxic turtle brain. J. Exp. Biol. 200, 1913 1917.
41. Pek-Scott M. Lutz P. L. (1998) K + ATP channel activation provides transient protection in anoxic turtle brain. Am. J. Physiol. 44, R2023 R2027.
42. Perez-Pinzon M., Rosenthal M., Sick T., Lutz P. L. Marsh D. (1992) Down-regulation of sodium channels during anoxia: a putative survival strategy of turtle brain. Am. J. Physiol. 31, R712 R715.
43. Prentice H. M., Milton S. L., Scheurle D. Lutz P. L. (2004) The upregulation of cognate and inducible heat shock proteins in the anoxic turtle brain. J. Cereb. Blood Flow Metab. 24, 826 828.
44. Rah D. K., Han D. W., Baek H. S., Hyon S. H. Park J. C. (2005) Prevention of reactive oxygen species-induced oxidative stress in human microvascular endothelial cells by green tea polyphenol. Toxicol. Lett. 155, 269 275.
45. Rice M. E., Lee E. J. Choy Y. (1995) High levels of ascorbic acid, not glutathione, in the CNS of anoxia-tolerant reptiles contrasted with levels in anoxia-intolerant species. J. Neurochem. 64, 1790 1799.
46. Rosseland C. M., Wierod L., Oksvold M. P., Werner H., Ostcold A. C., Thoresen G. H., Paulsen R. E., Huitfeldt H. S. Skarpen E. (2005) Cytoplasmic retention of peroxide-activated ERK provides survival in primary cultures of rat hepatocytes. Hepatol. 42, 200 207.
47. Roy S., Khanna S., Bickerstaff A. et al. (2003) Oxygen sensing by primary cardiac fibroblasts: a key role of p21(Waf1/Cip1/Sdi1). Circ. Res., 92, 264 271.
48. Sharikabad M. N., Ostbye K. M. Brors O. (2004) Effect of hydrogen peroxide on reoxygenation-induced Ca2 + accumulation in rat cardiomyocytes. Free Rad. Biol. Med., 37, 531 538.
49. Sharp C. D., Houghton J., Elrod J. W., Warren A., Jackson T.H. 4th, Jawahar A., Nanda A., Minager A. Alexander J. S. (2005) N-methyl-D-aspartate receptor activation in human cerebral endothelium promotes intracellular oxidant stress. Am. J. Physiol. Heart Circ. Physiol. 288, H1893 H1899.
50. Sheng H., Enghild J. J., Bowler R., Patel M., Batinic-Haberle I., Calvi C. L., Day B. J., Pearlstein R. D., Crapo J. D. Warner D. S. (2002) Effects of metalloporphyrin catalytic antioxidants in experimental brain ischemia. Free Rad. Biol. Med. 33, 947 961.
51. Sick T. J., Lutz P. L., LaManna J. C. Rosenthal M. (1982a) Comparative brain oxygenation and mitochondrial redox activity in turtles and rats. J. Appl. Physiol. 53, 1354 1359.
52. Sick T. J., Rosenthal M., LaManna J. C. Lutz P. L. (1982b) Brain potassium homeostasis, anoxia, and metabolic inhibition in turtles and rats. Am. J. Physiol. 243, R281 R288.
53. Sloot W. N. Gramsbergen J. B. P. (1995) Detection of salicylate and its hydroxylated adducts 2,3- and 2,5-dihydroxybenzoic acids as possible indices for in vivo hydroxyl radical formation in combination with catechol- and indoleamines and their metabolites in cerebrospinal fluid and brain tissue. J. Neurosci. Methods, 60, 141 149.
54. Snoeckx L. H., Cornelussen R. N., Van Nieuwenhoven F. A., Reneman R. S. van Der Vusse G. J. (2001) Heat shock proteins and cardiovascular pathohysiology. Physiol. Rev. 81, 1461 1497.
55. Sun H. Y., Wang N. P., Kerendi F., Halkos M., Kin H., Guyton R. A., Vinten-Johansen J. Zhao Z. Q. (2005) Hypoxic postconditioning reduces cardiomyocyte loss by inhibiting ROS generation and intracellular Ca2 + overload. Am. J. Physiol. Heart Circ. Physiol. 288, H1900 H1908.
56. Votyakova T. V. Reynolds I. J. (2004) detection of hydrogen peroxide with Amplex Red: interference by NADH and reduced glutathione auto-oxidation. Arch. Biochem. Biophys. 431, 138 144.
57. Wang H., Cheng E., Brooke S., Chang P. Sapolsky R. (2003) Over-expression of antioxidant enzymes protects cultured hippocampal and cortical neurons from necrotic insults. J. Neurochem. 87, 1527 1534.
58. Wang J. L., Ke D. S. Lin M. T. (2005) Heat shock pretreatment may protect against heatstroke-induced circulatory shock and cerebral ischemia by reducing oxidative stress and energy depletion. Shock, 23, 161 167.
59. Willmore W. G. Storey K. B. (1997a) Antioxidant systems and anoxia tolerance in a freshwater turtle Trachemys scripta elegans. Mol. Cell. Biochem. 170, 177 185.
60. Willmore W. G. Storey K. B. (1997b) Glutathione systems and anoxia tolerance in turtles. Am. J. Physiol. 273, R219 R225.
61. Xia X. G., Schmidt G. N., Teismann P., Ferger B. Schulz J. B. (2001) Dopamine mediates striatal malonate toxicity via dopamine transporter-dependent generation of reactive oxygen species and D2 but not D1 receptor activation. J. Neurochem. 79, 63 70.