εPKC is required for the induction of tolerance by ischemic and NMDA-mediated preconditioning in the organotypic hippocampal slice

Journal of Neuroscience

Volumn 23, Issue 2, 2003, Pages 384-391

  Raval, Ami P ^a   Dave, Kunjan R ^a   Mochly Rosen, Daria ^b   Sick, Thomas J ^a   Pérez Pinzón, Miguel A ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Anoxia; Glutamate receptors; In vitro cultures; Metabolism; Signal transduction; Tolerance

Indexed keywords

GLUTAMATE RECEPTOR; N METHYL DEXTRO ASPARTIC ACID; PROTEIN KINASE C EPSILON; 1-OLEOYL-2-ACETYLGLYCEROL; CALCIUM; DIACYLGLYCEROL; ENZYME ACTIVATOR; ENZYME INHIBITOR; GLUCOSE; GLYCEROL 2 ACETATE 1 OLEATE; ISOENZYME; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYLASPARTIC ACID; PHORBOL 13 ACETATE 12 MYRISTATE; PRKCE PROTEIN, RAT; PROPIDIUM IODIDE; PROTEIN KINASE C;

ADAPTATION; ANIMAL CELL; ANOXIA; ARTICLE; BRAIN ISCHEMIA; BRAIN SLICE; CALCIUM TRANSPORT; ENZYME ACTIVATION; ENZYME INDUCTION; HIPPOCAMPUS; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; RECEPTOR BLOCKING; SIGNAL TRANSDUCTION; STIMULUS RESPONSE; ANIMAL; CELL CULTURE; CELL HYPOXIA; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; FLUORESCENCE MICROSCOPY; IMMUNOBLOTTING; IN VITRO STUDY; ISCHEMIC PRECONDITIONING; METABOLISM; NERVE CELL; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; CALCIUM; CELL HYPOXIA; CELLS, CULTURED; DIGLYCERIDES; ENZYME ACTIVATORS; ENZYME INHIBITORS; GLUCOSE; HIPPOCAMPUS; IMMUNOBLOTTING; ISCHEMIC PRECONDITIONING; ISOENZYMES; MICROSCOPY, FLUORESCENCE; N-METHYLASPARTATE; NEURONS; PROPIDIUM; PROTEIN KINASE C; PROTEIN KINASE C-EPSILON; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; SIGNAL TRANSDUCTION; TETRADECANOYLPHORBOL ACETATE;

EID: 0037437356     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-02-00384.2003     Document Type: Article

References (71)

1. Albers GW, Goldberg MP, Choi DW (1992) Do NMDA antagonists prevent neuronal injury? Yes. Arch Neurol 49:418-420.
2. Anantharam V, Kitazawa M, Wagner J, Kaul S, Kanthasamy AG (2002) Caspase-3-dependent proteolytic cleavage of protein kinase C delta is essential for oxidative stress-mediated dopaminergic cell death after exposure to methylcyclopentadienyl manganese tricarbonyl. J Neurosci 22:1738-1751.
3. Bergold PJ, Casaccia-Bonnefil P (1997) Preparation of organotypic hippocampal slice cultures using the membrane filter method. Methods Mol Biol 72:15-22.
4. Best N, Sunsstrom LE, Mitchell J, Wheal HV (1996) Pre-exposure to subtoxic levels prevents kainic acid lesions in organotypic hippocampal slice cultures: effects of kainic acid on parvalbumin-immunoreactive neurons and expression of heat shock protein-72 following induction of tolerance. Eur J Neurosci 8:1209-1219.
5. Bharti A, Kraeft SK, Gounder M, Pandey P, Jin S, Yuan ZM, Lees-Miller SP, Weichselbaum R, Weaver D, Chen LB, Kufe D, Kharbanda S (1998) Inactivation of DNA-dependent protein kinase by protein kinase C delta: implications for apoptosis. Mol Cell Biol 18:6719-6728.
6. Blondeau N, Plamondon H, Richelme C, Heurteaux C, Lazdunski M (2000) K(ATP) channel openers, adenosine agonists and epileptic preconditioning are stress signals inducing hippocampal neuroprotection. Neuroscience 100:465-474.
7. Bond A, Lodge D, Hicks CA, Ward MA, O'Neill MJ (1999) NMDA receptor antagonism, but not AMPA receptor antagonism attenuates induced ischaemic tolerance in the gerbil hippocampus. Eur J Pharmacol 380:91-99.
8. Brooks G, Hearse DJ (1996) Role of protein kinase C in ischemic preconditioning: player or spectator? Circ Res 79:627-630.
9. Bruno V, Battaglia G, Copani A, D'Onofrio M, Di Iorio P, De Blasi A, Melchiorri D, Flor PJ, Nicoletti F (2001) Metabotropic glutamate receptor subtypes as targets for neuroprotective drugs. J Cereb Blood Flow Metab 21:1013-1033.
10. Caggiano AO, Kraig RP (1998) Neuronal nitric oxide synthase expression is induced in neocortical astrocytes after spreading depression. J Cereb Blood Flow Metab 18:75-87.
11. Centeno JM, Orti M, Salom JB, Sick TJ, Perez-Pinzon MA (1999) Nitric oxide is involved in anoxic preconditioning neuroprotection in rat hippocampal slices. Brain Res 836:62-69.
12. Chen L, Hahn H, Wu G, Chen CH, Liron T, Schechtman D, Cavallaro G, Banci L, Guo Y, Bolli R, Dorn GW II, Mochly-Rosen D (2001) Opposing cardioprotective actions and parallel hypertrophic effects of delta PKC and epsilon PKC. Proc Natl Acad Sci USA 98:11114-11119.
13. Choi DW (1995) Calcium: still center-stage in hypoxic-ischemic neuronal death. Trends Neurosci 18:58-60.
14. Chopp M, Chen H, Ho KL, Dereski MO, Brown E, Hetzel FW, Welch KM (1989) Transient hyperthermia protects against subsequent forebrain ischemic cell damage in the rat. Neurology 39:1396-1398.
15. Cimarosti H, Rodnight R, Tavares A, Paiva R, Valentim L, Rocha E, Salbego C (2001) An investigation of the neuroprotective effect of lithium in organotypic slice cultures of rat hippocampus exposed to oxygen and glucose deprivation. Neurosci Lett 315:33-36.
16. Dorn II GW, Souroujon MC, Liron T, Chen CH, Gray MO, Zhou HZ, Csukai M, Wu G, Lorenz JN, Mochly-Rosen D (1999) Sustained in vivo cardiac protection by a rationally designed peptide that causes epsilon protein kinase C translocation. Proc Natl Acad Sci USA 96:12798-12803.
17. Downey JM, Cohen MV, Ytrehus K, Liu Y (1994) Cellular mechanisms in ischemic preconditioning: the role of adenosine and protein kinase C. Ann NY Acad Sci 723:82-98.
18. Goldberg MP, Pham PC, Choi DW (1987) Dextrorphan and dextromethorphan attenuate hypoxic injury in neuronal culture. Neurosci Lett 80:11-15.
19. Gonzalez-Zulueta M, Feldman AB, Klesse LJ, Kalb RG, Dillman JF, Parada LF, Dawson TM, Dawson VL (2000) Requirement for nitric oxide activation of p21 (ras)/extracellular regulated kinase in neuronal ischemic preconditioning. Proc Natl Acad Sci USA 97:436-441.
20. Grabb MC, Choi DW (1999) Ischemic tolerance in murine cortical cell culture: critical role for NMDA receptors. J Neurosci 19:1657-1662.
21. Gray MO, Karliner JS, Mochly-Rosen D (1997) A selective epsilon-protein kinase C antagonist inhibits protection of cardiac myocytes from hypoxia-induced cell death. J Biol Chem 272:30945-30951.
22. Guang SL, Cohen MV, Mochly-Rosen D, Downey JM (1999) Protein kinase C-ε is responsible for the protection of preconditioning in rabbit cardiomyocytes. J Mol Cell Cardiol 31:1937-1948.
23. + channels in cerebral ischemic preconditioning. Proc Natl Acad Sci USA 92:4666-4670.
24. Huang HM, Weng CH, Ou SC, Hwang T (1999) Selective subcellular redistributions of protein kinase C isoforms by chemical hypoxia. J Neurosci Res 56:668-678.
25. Kato H, Araki T, Murase K, Kogure K (1992a) Induction of tolerance to ischemia: alterations in second-messenger systems in the gerbil hippocampus. Brain Res Bull 29:559-565.
26. Kato H, Liu Y, Araki T, Kogure K (1992b) MK-801, but not anisomycin, inhibits the induction of tolerance to ischemia in the gerbil hippocampus. Neurosci Lett 139:118-121.
27. 2+/calmodulin-dependent protein kinase II to cell membranes during complete cerebral ischemia. Brain Res 849:119-127.
28. Katsura KI, Kurihara J, Kato H, Katayama Y (2001) Ischemic preconditioning affects the subcellular distribution of protein kinase C and calcium/calmodulin-dependent protein kinase II in the gerbil hippocampal CA-neurons. Neurol Res 23:751-754.
29. Kawahara N, Croll SD, Wiegand SJ, Klatzo I (1997) Cortical spreading depression induces long-term alterations of BDNF levels in cortex and hippocampus distinct from lesion effects: implications for ischemic tolerance. Neurosci Res 29:37-47.
30. Kobayashi S, Harris VA, Welsh FA (1995) Spreading depression induces tolerance of cortical neurons to ischemia in rat brain. J Cereb Blood Flow Metab 15:721-727.
31. Koponen S, Goldsteins G, Keinanen R, Koistinaho J (2000) Induction of protein kinase Cdelta subspecies in neurons and microglia after transient global brain ischemia. J Cereb Blood Flow Metab 20:93-102.
32. 2+, phospholipid-dependent protein kinase associated with plasma membrane. Nature 301:621-623.
33. Laake JH, Haug FM, Wieloch T, Ottersen OP (1999) A simple in vitro model of ischemia based on hippocampal slice cultures and propidium iodide fluorescence. Brain Res Brain Res Protoc 4:173-184.
34. Liniger R, Popovic R, Sullivan B, Gregory G, Bickler PE (2001) Effects of neuroprotective cocktails on hippocampal neuron death in an in vitro model of cerebral ischemia. J Neurosurg Anesthesiol 13:19-25.
35. Mackay K, Mochly-Rosen D (2001) Arachidonic acid protects neonatal rat cardiac myocytes from ischaemic injury through epsilon protein kinase C. Cardiovasc Res 50:65-74.
36. Matsushima K, Hogan MJ, Hakim AM (1996) Cortical spreading depression protects against subsequent focal cerebral ischemia in rats. J Cereb Blood Flow Metab 16:221-226.
37. Nandagopal K, Dawson TM, Dawson VL (2001) Critical role for nitric oxide signaling in cardiac and neuronal ischemic preconditioning and tolerance. J Pharmacol Exp Ther 297:474-478.
38. Nawashiro H, Tasaki K, Ruetzler CA, Hallenbeck JM (1996) TNF-alpha pretreatment induces protective effects against focal cerebral ischemia in mice. J Cereb Blood Flow Metab 17:483-490.
39. Nishio S, Yunoki M, Chen ZF, Anzivino MJ, Lee KS (2000) Ischemic tolerance in the rat neocortex following hypothermic preconditioning. J Neurosurg 93:845-851.
40. Nishizawa Y (2001) Glutamate release and neuronal damage in ischemia. Life Sci 69:369-381.
41. Nishizuka Y (1992) Intracellular signaling by hydrolysis of phospholipids and activation of protein kinase C. Science 258:607-614.
42. Ohtsuki T, Matsumoto M, Kuwabara K, Kitagawa K, Suzuki K, Taniguchi N, Kamada T (1992) Influence of oxidative stress on induced tolerance to ischemia in gerbil hippocampal neurons. Brain Res 599:246-252.
43. Ohtsuki T, Ruetzler CA, Tasaki K, Hallenbeck JM (1996) Interleukin-1 mediates induction of tolerance to global ischemia in gerbil hippocampal CA1 neurons. J Cereb Blood Flow Metab 16:1137-1142.
44. Ozyurt E, Graham DI, WoodruffGN, McCulloch J (1988) Protective effect of the glutamate antagonist, MK-801 in focal cerebral ischemia in the cat. J Cereb Blood Flow Metab 8:138-143.
45. Pellegrini-Giampietro DE, Peruginelli F, Meli E, Cozzi A, Albani-Torregrossa S, Pellicciari R, Moroni F (1999) Protection with metabotropic glutamate 1 receptor antagonists in models ofischemic neuronal death: time-course and mechanisms. Neuropharmacology 38:1607-1619.
46. ATP channel and protein kinase C. Neuroscience 89:453-459.
47. Perez-Pinzon MA, Mumford PL, Rosenthal M, Sick TJ (1996) Anoxic preconditioning in hippocampal slices: role of adenosine. Neuroscience 75:687-694.
48. Perez-Pinzon MA, Born JG, Centeno JM (1999) Calcium and increase excitability promote tolerance against anoxia in hippocampal slices. Brain Res 833:20-26.
49. Plumier JC, Krueger AM, Currie RW, Kontoyiannis D, Kollias G, Pagoulatos GN (1997) Transgenic mice expressing the human inducible Hsp70 have hippocampal neurons resistant to ischemic injury. Cell Stress Chaperones 2:162-167.
50. Pringle AK, Benham CD, Sim L, Kennedy J, Iannotti F, Sundstrom LE (1996) Selective N-type calcium channel antagonist omega conotoxin MVIIA is neuroprotective against hypoxic neurodegeneration in organotypic hippocampal-slice cultures. Stroke 27:2124-2130.
51. Pringle AK, Angunawela R, Wilde GJ, Mepham JA, Sundstrom LE, Iannotti F (1997a) Induction of 72 kDa heat-shock protein following sub-lethal oxygen deprivation in organotypic hippocampal slice cultures. Neuropathol Appl Neurobiol 23:289-298.
52. Pringle AK, Iannotti F, Wilde GJ, Chad JE, Seeley PJ, Sundstrom LE (1997b) Neuroprotection by both NMDA and non-NMDA receptor antagonists in in vitro ischemia. Brain Res 755:36-46.
53. Rao AM, Hatcher JF, Dempsey RJ (2000) Neuroprotection by group I metabotropic glutamate receptor antagonists in forebrain ischemia of gerbil. Neurosci Lett 293:1-4.
54. Reshef A, Sperling O, Zoref-Shani E (2000) Role of K(ATP) channels in the induction ofischemic tolerance by the "adenosine mechanism" in neuronal cultures. Adv Exp Med Biol 486:217-221.
55. Riepe MW, Esclaire F, Kasischke K, Schreiber S, Nakase H, Kempski O, Ludolph AC, Dirnagl U, Hugon J (1997) Increased hypoxic tolerance by chemical inhibition of oxidative phosphorylation: "chemical preconditioning." J Cereb Blood Flow Metab 17:257-264.
56. Rordorff G, Koroshetz WJ, Bonventre JV (1991) Heat shock protects cultured neurons from glutamate toxicity. Neuron 7:1043-1051.
57. Rothman SM, Olney JW (1986) Glutamate and the pathophysiology of hypoxic-ischemic brain damage. Ann Neurol 19:105-111.
58. Sakaguchi T, Okada M, Kuno M, Kawasaki K (1997) Dual mode of N-methyl-D-aspartate-induced neuronal death in hippocampal slice cultures in relation to N-methyl-D-aspartate receptor properties. Neuroscience 76:411-423.
59. Savolainen KM, Loikkanen J, Naarala J (1995) Amplification of glutamateinduced oxidative stress. Toxicol Lett 82-83:399-405.
60. Schwarze SR, Ho A, Vocero-Akbani A, Dowdy SF (1999) In vivo protein transduction: delivery of a biologically active protein into the mouse. Science 285:1569-1572.
61. Shamloo M, Wieloch T (1999) Rapid decline in protein kinase C gamma levels in the synaptosomal fraction of rat hippocampus after ischemic preconditioning. NeuroReport 10:931-935.
62. Sieber FE, Traystman RJ, Brown PR, Martin LJ (1998) Protein kinase C expression and activity after cerebral incomplete cerebral ischemia in dogs. Stroke 29:1445-1453.
63. Simon RP, Swan JH, Griffiths T, Meldrum BS (1984) Blockade of N-methyl-D-aspartate receptors may protect against ischemic damage in the brain. Science 226:850-852.
64. Souroujon MC, Mochly-Rosen D (1998) Peptide modulators of proteinprotein interactions in intracellular signaling. Nat Biotechnol 16:919-924.
65. Steinberg GK, George CP, DeLaPaz R, Shibata DK, Gross T (1988) Dextromethorphan protects against cerebral injury following transient focal ischemia in rabbits. Stroke 19:1112-1118.
66. Swan JH, Meldrum BS (1990) Protection by NMDA antagonists against selective cell loss following transient ischaemia. J Cereb Blood Flow Metab 10:343-351.
67. Tan S, Wood M, Maher P (1998) Oxidative stress induces a form of programmed cell death with characteristics of both apoptosis and necrosis in neuronal cells. J Neurochem 71:95-105.
68. Tauskela JS, Chakravarthy BR, Murray CL, Wang Y, Comas T, Hogan M, Hakim A, Morley P (1999) Evidence from cultured rat cortical neurons of differences in the mechanism ofischemic preconditioning of brain and heart. Brain Res 827:143-151.
69. Vaccarino FM, Liljequist S, Tallman JF (1991) Modulation of protein kinase C translocation by excitatory and inhibitory amino acids in primary cultures of neurons. J Neurochem 57:391-396.
70. + overload injury in rat myocardium. Circ Res 84:1156-1165.
71. Xu G-P, Dave KR, Vivero R, Schmidt-Kastner R, Sick TJ, Perez-Pinzon MA (2002) Improvement in neuronal survival after ischemic preconditioning in hippocampal slice cultures. Brain Res 952:153-158.