2-Deoxy-D-glucose protects hippocampal neurons against excitotoxic and oxidative injury: Evidence for the involvement of stress proteins

Journal of Neuroscience Research

Volumn 57, Issue 1, 1999, Pages 48-61

  Lee, Jaewon ^a   Bruce Keller, Annadora J ^a   Kruman, Yuri ^a   Chan, Sic L ^a   Mattson, Mark P ^a,b  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

Author keywords

Apoptosis; Calcium; Dietary restriction; Epileptic seizures; Glutamate; Heat shock protein 70; Kainic acid; Mitochondrial transmembrane potential

Indexed keywords

CALCIUM ION; DEOXYGLUCOSE; GLUCOSE; GLUTAMIC ACID; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 70; IRON; PROTEIN BCL 2;

AMNESIA; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CALCIUM HOMEOSTASIS; DIET RESTRICTION; INTRAPERITONEAL DRUG ADMINISTRATION; MALE; NERVE CELL DEGENERATION; NERVE CELL EXCITABILITY; NERVE CELL NECROSIS; NERVE INJURY; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; RAT;

ANIMALS; BLOTTING, WESTERN; CALCIUM; CARRIER PROTEINS; CELLS, CULTURED; DEOXYGLUCOSE; EXCITATORY AMINO ACID AGONISTS; HEAT-SHOCK PROTEINS; HIPPOCAMPUS; HOMEOSTASIS; HSP70 HEAT-SHOCK PROTEINS; IMMUNOHISTOCHEMISTRY; KAINIC ACID; MALE; MEMBRANE POTENTIALS; MITOCHONDRIA; MOLECULAR CHAPERONES; NEURONS; NEUROPROTECTIVE AGENTS; OXIDATIVE STRESS; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES;

EID: 0033168080     PISSN: 03604012     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4547(19990701)57:1<48::AID-JNR6>3.0.CO;2-L     Document Type: Article

References (69)

1. Aly KB, Pipkin JL, Hinson WG, Feuers RJ, Duffy PH, Lyn-Cook L, Hart RW. 1994. Chronic caloric restriction induces stress proteins in the hypothalamus of rats. Mech Ageing Dev 76:11-23.
2. Ames BN. 1989. Endogenous oxidative DNA damage, aging and cancer. Free Rad Res Commun 7:121-128.
3. Beal MF. 1998. Mitochondrial dysfunction in neurodegenerative diseases. Biochim Biophys Acta 1366:211-223.
4. Ben-Ari Y. 1985. Limbic seizures and brain damage produced by kainic acid: mechanisms and relevance to human temporal lobe epilepsy. Neuroscience 14:375-403.
5. Bruce-Keller AJ, Umberger G, McFall R, Mattson MP. 1999. Food restriction reduces brain damage and improves behavioral outcome following excitotoxic and metabolic insults. Ann Neurol 45:8-15.
6. Callahan B, Yuan J, Stover G, Hatzidimitriou G, Ricaurte G. 1998. Effects of 2-deoxy-D-glucose on methamphetamine-induced dopamine and serotonin neurotoxicity. J Neurochem 70:190-197.
7. Cefalu WT, Wagner JD, Wang ZQ, Bell-Farrow AD, Collins J, Haskell D, Bechtold R, Morgan T. 1997. A study of caloric restriction and cardiovascular aging in cynomolgus monkeys (Macaca fascicularis): a potential model for aging research. J Gerontol A Biol Sci Med Sci 52:B10-B19.
8. Chan PH. 1996. Role of oxidants in ischemic brain damage. Stroke 27:1124-1129.
9. Crandall DL, Feirer RP, Griffith DR, Beitz DC. 1981. Relative role of caloric restriction and exercise training upon susceptibility to isoproterenol-induced myocardial infarction in male rats. Am J Clin Nutr 34:841-847.
10. Dubey A, Forster MJ, Lal H, Sohal RS. 1996. Effect of age and caloric intake on protein oxidation in different brain regions and on behavioral functions of mouse. Arch Biochem Biophys 333:189-197.
11. Dugan LL, Sensi SL, Canzoniero LMT, Handran SD, Rothman SM, Lin TS, Goldberg MP, Choi DW. 1995. Mitochondrial production of reactive oxygen species in cortical neurons following exposure to N-methyl-D-aspartate. J Neurosci 15:6377-6388.
12. Ehrenfried JA, Evers BM, Chu KU, Townsend CM, Thompson JC. 1996. Caloric restriction increases the expression of heat shock protein in the gut. Ann Surg 223:592-597.
13. Finch CE, Morgan TE. 1997. Food restriction and brain aging. In: Mattson MP, Geddes JW, editors. The aging brain. Greenwich, CT: JAI Press, Adv Cell Aging Gerontol 2:279-297.
14. Goodman Y, Bruce AJ, Cheng B, Mattson MP. 1996. Estrogens attenuate and corticosterone exacerbates excitotoxicity, oxidative injury and amyloid β-peptide toxicity in hippocampal neurons. J Neurochem 66:1836-1844.
15. He H, Lam M, McCormick TS, Distelhorst CW. 1997. Maintenance of calcium homeostasis in the endoplasmic reticulum by Bcl-2. J Cell Biol 138:1219-1228.
16. Heydari AR, You S, Takahashi R, Gutsmann A, Sarge KD, Richardson A. 1996. Effect of caloric restriction on the expression of heat shock protein 70 and the activation of heat shock transcription factor 1. Dev Genet 18:114-124.
17. Idrobo F, Nandy K, Mostofsky DI, Blatt L, Nandy L. 1987. Dietary restriction: effects on radial maze learning and lipofuscin pigment deposition in the hippocampus and frontal cortex. Arch Gerontol Geriatr 6:355-362.
18. Johnson LV, Walsh ML, Bokus BJ, Chen LB. 1981. Monitoring relative mitochondrial transmembrane potential in living cells by fluorescence microscopy. J Cell Biol 88:526-532.
19. Kanarck RB, Marks-Kaufman R, Ruthazer R, Gualtieri L. 1983. Increased carbohydrate consumption by rats as a function of 2-deoxy-D-glucose administration. Pharmacol Biochem Behav 18:47-50.
20. Keller JN, Kindy MS, Holtsberg FW, St Clair DK, Yen H-C, Germeyer A, Steiner SM, Bruce-Keller AJ, Hutchins JB, Mattson MP. 1998. Mitochondrial MnSOD prevents neural apoptosis and reduces ischemic brain injury: suppression of peroxynitrite production, lipid peroxidation and mitochondrial dysfunction. J Neurosci 18:687-697.
21. Kennedy AL, Lyons TJ. 1997. Glycation, oxidation, and lipoxidation in the development of diabetic complications. Metabolism 46: 14-21.
22. Kooy NW, Royall JA, Ischoropoulos H, Beckman JS. 1994. Peroxynitrite-mediated oxidation of dihydrorhodamine 123. Free Rad Biol Med 16:149-156.
23. Kraemer PJ, Brown RW, Baldwin SA, Scheff SW. 1996. Validation of a single-day Morris water maze procedure used to assess cognitive deficits associated with brain damage. Brain Res Bull 39:17-22.
24. Kruman I, Bruce AJ, Bredesen DE, Waeg G, Mattson MP. 1997. Evidence that 4-hydroxynonenal mediates oxidative stress-induced neuronal apoptosis. J Neurosci 17:5089-5100.
25. Lafon-Cazal M, Pietri S, Cuicasi M, Bockaert J. 1993. NMDA-dependent superoxide production and neurotoxicity. Nature 364:535-537.
26. Lane MA, Baer DJ, Rumpler WV, Weindruch R, Ingram DK, Tilmont EM, Cutler RG, Roth GS. 1996. Calorie restriction lowers body temperature in rhesus monkeys, consistent with a postulated anti-aging mechanism in rodents. Proc Natl Acad Sci USA 93:4159-4164.
27. Latchman DS. 1995. Cell stress genes and neuronal protection. Neuropathol Appl Neurobiol 21:475-477.
28. Lee AS. 1992. Mammalian stress response: induction of the glucose regulated protein family. Curr Opin Cell Biol 4:267-273.
29. Little E, Ramakrishnan M, Roy B, Gazit G, Lee AS. 1994. The glucose-regulated proteins (GRP78 and GRP94): functions, gene regulation, and applications. Crit Rev Euk Gene Expr 4:1-18.
30. Little E, Tocco G, Baudry M, Lee AS, Schreiber SS. 1996. Induction of glucose-regulated protein (glucose-regulated protein 78/BiP and glucose-regulated protein 94) and heat shock protein 70 transcripts in the immature rat brain following status epilepticus. Neuroscience 75:209-219.
31. 2+ disturbances, and cell death in renal epithelial cells. J Biol Chem 272:21751-21759.
32. Lowenstein DH, Chan P, Miles M. 1991. The stress protein response in cultured neurons: characterization and evidence for a protective role in excitotoxicity. Neuron 7:1053-1060.
33. Lowenstein DH, Gwinn RP, Seren MS, Simon RP, McIntosh TK. 1994. Increased expression of mRNA encoding calbindin-D28k, the glucose-regulated proteins, or the 72 heat-shock protein in three models of acute CNS injury. Mol Brain Res 22:299-308.
34. 2+ homeostasis and cell death. J Neurosci 15:6239-6249.
35. Mark RJ, Lovell MA, Markesbery WR, Uchida K, Mattson MP. 1997. A role for 4-hydroxynonenal in disruption of ion homeostasis and neuronal death induced by amyloid β-peptide. J Neurochem 68:255-264.
36. Mattson MP, Murrain M. Guthrie PB, Kater SB. 1989. Fibroblast growth factor and glutamate: opposing actions in the generation and degeneration of hippocampal neuroarchitecture. J Neurosci 9:3728-3740.
37. Mattson MP, Wang H, Michaelis EK. 1991. Developmental expression, compartmentalization, and possible role in excitotoxicity of a putative NMDA receptor protein in cultured hippocampal neurons. Brain Res 565:94-108.
38. Mattson MP, Zhang Y, Bose S. 1993. Growth factors prevent mitochondrial dysfunction, loss of calcium homeostasis and cell injury, but not ATP depletion in hippocampal neurons deprived of glucose. Exp Neurol 121:1-13.
39. Mattson MP, Barger SW, Begley JG, Mark RJ. 1995a. Calcium, free radicals, and excitotoxic neuronal death in primary cell culture. Methods Cell Biol 46:187-216.
40. i and neurotoxicity, and increase antioxidant enzyme activities in hippocampal neurons. J Neurochem 65:1740-1751.
41. Mattson MP, Furukawa K, Bruce AJ, Mark RJ, Blanc E. 1996. Calcium homeostasis and free radical metabolism as convergence points in the pathophysiology of dementia. In: Wasco W, Tanzi RE, editors. Molecular mechanisms of dementia. Totowa, NJ: Humana Press. p 103-143.
42. Mattson MP, Goodman Y, Luo H, Fu W, Furukawa K. 1997. Activation of NF-KB protects hippocampal neurons against oxidative stress-induced apoptosis: evidence for induction of Mn-SOD and suppression of peroxynitrite production and protein tyrosine nitration. J Neurosci Res 49:681-697.
43. McCormick TS, McColl KS, Distelhorst CW. 1997. Mouse lymphoma cells destined to undergo apoptosis in response to thapsigargin treatment fail to generate a calcium-mediated grp78/grp94 stress response. J Biol Chem 272:6087-6092.
44. Mizzen LA, Kabiling AN, Welch WJ. 1991. The two mammalian mitochondrial stress proteins, grp 75 and hsp 58, transiently interact with newly synthesized mitochondrial proteins. Cell Regul 2:165-179.
45. Morgan TE, Rozovsky I, Goldsmith SK, Stone DJ, Yoshida T, Finch CE. 1997. Increased transcription of the astrocyte gene GFAP during middle-age is attenuated by food restriction: implications for the role of oxidative stress. Free Rad Biol Med 23:524-528.
46. Morris RGM, Garrud P, Rawlins JNP, O'Keefe J. 1982. Place navigation is impaired in rats with hippocampal lesions. Nature 297:681-683.
47. Muscari C, Giaccari A, Giordano E, Clo C, Guarnieri C, Caldarera CM. 1996. Role of reactive oxygen species in cardiovascular aging. Mol Cell Biochem 160-161:159-166.
48. Nakao N, Grasbon-Frodl EM, Widner H, Brundin P. 1996. Antioxidant treatment protects striatal neurons against excitotoxic insults. Neuroscience 73:185-200.
49. Pahl HL, Baeuerle PA. 1995. A novel signal transduction pathway from the endoplasmic reticulum to the nucleus is mediated by transcription factor NF-KB. EMBO J 14:2580-2588.
50. Pitsikas N, Algeri S. 1992. Deterioration of spatial and nonspatial reference and working memory in aged rats: protective effect of life-long calorie restriction. Neurobiol Aging 13:369-373.
51. Reis DJ, Golanov EV, Galea E, Feinstein DL. 1997. Central neurogenic neuroprotection: central neural systems that protect the brain from hypoxia and ischemia. Ann NY Acad Sci 835:168-186.
52. Reynolds IJ, Hastings TG. 1995. Glutamate induces the production of reactive oxygen species in cultured forebrain neurons following NMDA receptor activation. J Neurosci 15:3318-3327.
53. Schinder AF, Olson EC, Spitzer NC, Montal M. 1996. Mitochondrial dysfunction is a primary event in glutamate neurotoxicity. J Neurosci 16:6125-6133.
54. Silver IA, Deas J, Erecinska M. 1997. Ion homeostasis in brain cells: differences in intracellular ion responses to energy limitation between cultured neurons and glial cells. Neuroscience 78:589-601.
55. Smith-Swintosky VL, Kraemer PJ, Bruce AJ, McCants N, Maki A, Brown RW, Alcala M, Goodman Y, Slevin JT, Mattson MP. 1996. Bacterial alkaloids mitigate seizure-induced hippocampal damage and memory deficits. Exp Neurol 141:287-296.
56. Sohal RS, Weindruch R. 1996. Oxidative stress, caloric restriction, and aging. Science 273:59-63.
57. Sohal RS, Ku HH, Agarwal S, Forster MJ, Lal H. 1994a. Oxidative damage, mitochondrial oxidant generation and antioxidant defenses during aging and in response to food restriction in the mouse. Mech Ageing Dev 74:121-33.
58. Sohal RS, Agarwal S, Candas M, Forster MJ, Lal H. 1994b. Effect of age and caloric restriction on DNA oxidative damage in different tissues of C57BL/6 mice. Mech Ageing Dev 76:215-224.
59. Stein-Behrens B, Mattson MP, Chang I, Yeh M, Sapolsky RM. 1994. Stress excacerbates neuron loss and cytoskeletal pathology in the hippocampus. J Neurosci 14:5373-5380.
60. Stewart J, Mitchell J, Kalant N. 1989. The effects of life-long food restriction on spatial memory in young and aged Fischer 344 rats measured in the eight-arm radial and the Morris water mazes. Neurobiol Aging 10:669-675.
61. Vass K, Berger ML, Nowak TS Jr, Welch WJ, Lassmann H. 1989. Induction of stress protein HSP70 in nerve cells after status epilepticus in the rat. Neurosci Lett 100:259-264.
62. Wachsman JT. 1996. The beneficial effects of dietary restriction: reduced oxidative damage and enhanced apoptosis. Mutat Res 350:25-34.
63. Weindruch RL, Walford S, Fligiel S, Guthrie D. 1986. The retardation of aging by dietary restriction: longevity, immunity and lifetime energy intake. J Nutr 116:641-654.
64. Weindruch R, Walford RL. 1988. The retardation of aging and disease by dietary restriction. Springfield IL: Thompson. 436 p.
65. Yellon DM, Baxter GF, Garcia-Dorado D, Heusch G, Sumeray MS. 1998. Ischaemic preconditioning: present position and future directions. Cardiovasc Res 37:21-33.
66. Yu ZF, Luo H, Fu W, Mattson MP. 1999. The endoplasmic reticulum stress-responsive protein GRP78 protects neurons against excitotoxicity and apoptosis: suppression of oxidative stress and stabilization of calcium homeostasis. Exp Neurol 155:302-314.
67. Yun J, Tomida A, Nagata K, Tsuruo T. 1995. Glucose-regulated stresses confer resistance to VP-16 in human cancer cells through a decreased expression of DNA topoisomerase II. Oncol Res 7:583-590.
68. Zamzami N, Marchetti P, Castedo M, Decaudin D, Macho A, Hirsch T, Susin S, Petit P, Mignotte B, Kroemer G. 1995. Sequential reduction of mitochondrial transmembrane potential and generation of reactive oxygen species in early programmed cell death. J Exp Med 182:367-377.
69. Zhang Y, Tatsuno T, Carney J, Mattson MP. 1993. Basic FGF, NGF, and IGFs protect hippocampal neurons against iron-induced degeneration. J Cerebral Blood Flow Metab 13:378-388.