Genomic analysis of ischemic preconditioning in adult rat hippocampal slice cultures

Brain Research

Volumn 1292, Issue , 2009, Pages 107-122

  Benardete, Ethan A ^a   Bergold, Peter J ^a  

^a SUNY DOWNSTATE MEDICAL CENTER   (United States)

Author keywords

Apoptosis; Hippocampus; Ischemic preconditioning; Microarray; Receptor signaling pathway; Slice culture

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; JANUS KINASE; MITOGEN ACTIVATED PROTEIN KINASE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; RNA; STAT PROTEIN; TOLL LIKE RECEPTOR; TRANSFORMING GROWTH FACTOR BETA; VASCULOTROPIN; WNT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CONTROLLED STUDY; GENE EXPRESSION; GENE IDENTIFICATION; GENETIC TRANSCRIPTION; GENOMICS; ISCHEMIC PRECONDITIONING; MICROARRAY ANALYSIS; NERVE CELL NECROSIS; NEUROPROTECTION; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; SIGNAL TRANSDUCTION;

ANIMALS; CELL COUNT; CELL DEATH; CELL HYPOXIA; FEMALE; GLUCOSE; HIPPOCAMPUS; ISCHEMIC PRECONDITIONING; LINEAR MODELS; MALE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROTEIN BIOSYNTHESIS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TIME FACTORS;

RATTUS;

EID: 69449088403     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2009.07.027     Document Type: Article

References (56)

1. Aketa S., Nakase H., Kamada Y., Hiramatsu K., and Sakaki T. Chemical preconditioning with 3-nitropropionic acid in gerbil hippocampal slices: therapeutic window and the participation of adenosine receptor. Exp. Neurol. 166 (2000) 385-391
2. Andreasson K.I., Savonenko A., Vidensky S., Goellner J.J., Zhang Y., Shaffer A., Kaufmann W.E., Worley P.F., Isakson P., and Markowska A.L. Age-dependent cognitive deficits and neuronal apoptosis in cyclooxygenase-2 transgenic mice. J. Neurosci. 21 (2001) 8198-8209
3. Barone F.C., White R.F., Spera P.A., Ellison J., Currie R.W., Wang X., and Feuerstein G.Z. Ischemic preconditioning and brain tolerance: temporal histological and functional outcomes, protein synthesis requirement, and interleukin-1 receptor antagonist and early gene expression. Stroke 29 (1998) 1937-1950 discussion 1950-1
4. Bates S., Read S.J., Harrison D.C., Topp S., Morrow R., Gale D., Murdock P., Barone F.C., Parsons A.A., and Gloger I.S. Characterisation of gene expression changes following permanent MCAO in the rat using subtractive hybridisation. Brain Res. Mol. Brain Res. 93 (2001) 70-80
5. Bernaudin M., Tang Y., Reilly M., Petit E., and Sharp F.R. Brain genomic response following hypoxia and re-oxygenation in the neonatal rat. Identification of genes that might contribute to hypoxia-induced ischemic tolerance. J. Biol. Chem. 277 (2002) 39728-39738
6. Bond A., Lodge D., Hicks C.A., Ward M.A., and O'Neill M.J. NMDA receptor antagonism, but not AMPA receptor antagonism attenuates induced ischaemic tolerance in the gerbil hippocampus. Eur. J. Pharmacol. 380 (1999) 91-99
7. Bossenmeyer-Pourie C., Koziel V., and Daval J.L. Effects of hypothermia on hypoxia-induced apoptosis in cultured neurons from developing rat forebrain: comparison with preconditioning. Pediatr. Res. 47 (2000) 385-391
8. Burda J., Hrehorovska M., Bonilla L.G., Danielisova V., Cizkova D., Burda R., Nemethova M., Fando J.L., and Salinas M. Role of protein synthesis in the ischemic tolerance acquisition induced by transient forebrain ischemia in the rat. Neurochem. Res. 28 (2003) 1213-1219
9. Burda J., Danielisova V., Nemethova M., Gottlieb M., Matiasova M., Domorakova I., Mechirova E., Ferikova M., Salinas M., and Burda R. Delayed postconditioning initiates additive mechanism necessary for survival of selectively vulnerable neurons after transient ischemia in rat brain. Cell Mol Neurobiol. 26 (2006) 1141-1151
10. Chen M., Lu T.J., Chen X.J., Zhou Y., Chen Q., Feng X.Y., Xu L., Duan W.H., and Xiong Z.Q. Differential roles of NMDA receptor subtypes in ischemic neuronal cell death and ischemic tolerance. Stroke 39 (2008) 3042-3048
11. Choi J.S., Kim H.Y., Chun M.H., Chung J.W., and Lee M.Y. Differential regulation of cyclooxygenase-2 in the rat hippocampus after cerebral ischemia and ischemic tolerance. Neurosci. Lett. 393 (2006) 231-236
12. Currie R.W., Ellison J.A., White R.F., Feuerstein G.Z., Wang X., and Barone F.C. Benign focal ischemic preconditioning induces neuronal Hsp70 and prolonged astrogliosis with expression of Hsp27. Brain Res. 863 (2000) 169-181
13. Davies J., Evans R.H., Herrling P.L., Jones A.W., Olverman H.J., Pook P., and Watkins J.C. CPP, a new potent and selective NMDA antagonist. Depression of central neuron responses, affinity for [3H]D-AP5 binding sites on brain membranes and anticonvulsant activity. Brain Res. 382 (1986) 169-173
14. Dhodda V.K., Sailor K.A., Bowen K.K., and Vemuganti R. Putative endogenous mediators of preconditioning-induced ischemic tolerance in rat brain identified by genomic and proteomic analysis. J. Neurochem. 89 (2004) 73-89
15. Dirnagl U., Simon R.P., and Hallenbeck J.M. Ischemic tolerance and endogenous neuroprotection. Trends Neurosci. 26 (2003) 248-254
16. Duszczyk M., Gadamski R., Ziembowicz A., Danysz W., and Lazarewicz J.W. NMDA receptor antagonism does not inhibit induction of ischemic tolerance in gerbil brain in vivo. Neurotox. Res. 7 (2005) 283-292
17. Emerson M.R., Nelson S.R., Samson F.E., and Pazdernik T.L. Hypoxia preconditioning attenuates brain edema associated with kainic acid-induced status epilepticus in rats. Brain Res. 825 (1999) 189-193
18. In: Federoff S., and Richardson A. (Eds). Protocols for Neural Cell Culture (2001), Humana Press, Inc., Totowa, NJ
19. Feng Z., Davis D.P., Sasik R., Patel H.H., Drummond J.C., and Patel P.M. Pathway and gene ontology based analysis of gene expression in a rat model of cerebral ischemic tolerance. Brain Res. 1177 (2007) 103-123
20. Gage A.T., and Stanton P.K. Hypoxia triggers neuroprotective alterations in hippocampal gene expression via a heme-containing sensor. Brain Res. 719 (1996) 172-178
21. Gidday J.M., Fitzgibbons J.C., Shah A.R., and Park T.S. Neuroprotection from ischemic brain injury by hypoxic preconditioning in the neonatal rat. Neurosci. Lett. 168 (1994) 221-224
22. Gidday J.M. Cerebral preconditioning and ischaemic tolerance. Nat. Rev. Neurosci. 7 (2006) 437-448
23. Hassen G.W., Tian D., Ding D., and Bergold P.J. A new model of ischemic preconditioning using young adult hippocampal slice cultures. Brain Res. Brain Res. Protoc. 13 (2004) 135-143
24. Hua Y., Keep R.F., Hoff J.T., and Xi G. Thrombin preconditioning attenuates brain edema induced by erythrocytes and iron. J. Cereb. Blood Flow Metab. 23 (2003) 1448-1454
25. Irizarry R.A., Bolstad B.M., Collin F., Cope L.M., Hobbs B., and Speed T.P. Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res. 31 (2003) e15
26. Kariko K., Weissman D., and Welsh F.A. Inhibition of toll-like receptor and cytokine signaling-a unifying theme in ischemic tolerance. J. Cereb. Blood Flow Metab. 24 (2004) 1288-1304
27. Kawahara N., Wang Y., Mukasa A., Furuya K., Shimizu T., Hamakubo T., Aburatani H., Kodama T., and Kirino T. Genome-wide gene expression analysis for induced ischemic tolerance and delayed neuronal death following transient global ischemia in rats. J. Cereb. Blood Flow Metab. 24 (2004) 212-223
28. Khaspekov L., Shamloo M., Victorov I., and Wieloch T. Sublethal in vitro glucose-oxygen deprivation protects cultured hippocampal neurons against a subsequent severe insult. NeuroReport 9 (1998) 1273-1276
29. Lahousse S.A., Wallace D.G., Liu D., Gaido K.W., and Johnson K.J. Testicular gene expression profiling following prepubertal rat mono-(2-ethylhexyl) phthalate exposure suggests a common initial genetic response at fetal and prepubertal ages. Toxicol. Sci. 93 (2006) 369-381
30. Larsen M.H., Olesen M., Woldbye D.P., Hay-Schmidt A., Hansen H.H., Ronn L.C., and Mikkelsen J.D. Regulation of activity-regulated cytoskeleton protein (Arc) mRNA after acute and chronic electroconvulsive stimulation in the rat. Brain Res. 1064 (2005) 161-165
31. Lehmann J., Schneider J., McPherson S., Murphy D.E., Bernard P., Tsai C., Bennett D.A., Pastor G., Steel D.J., Boehm C., et al. CPP, a selective N-methyl-d-aspartate (NMDA)-type receptor antagonist: characterization in vitro and in vivo. J. Pharmacol. Exp. Ther. 240 (1987) 737-746
32. Livak K.J., and Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods 25 (2001) 402-408
33. Ma D., Hossain M., Pettet G.K., Luo Y., Lim T., Akimov S., Sanders R.D., Franks N.P., and Maze M. Xenon preconditioning reduces brain damage from neonatal asphyxia in rats. J. Cereb. Blood Flow Metab. 26 (2006) 199-208
34. Marsh B.J., Williams-Karnesky R.L., and Stenzel-Poore M.P. Toll-like receptor signaling in endogenous neuroprotection and stroke. Neuroscience 158 (2009) 1007-1020
35. Murphy D.E., Hutchison A.J., Hurt S.D., Williams M., and Sills M.A. Characterization of the binding of [3H]-CGS 19755: a novel N-methyl-d-aspartate antagonist with nanomolar affinity in rat brain. Br. J. Pharmacol. 95 (1988) 932-938
36. Nakagawa I., Ogawa Y., Noriyama Y., Nakase H., Yamashita M., and Sakaki T. Chemical preconditioning prevents paradoxical increase in glutamate release during ischemia by activating ATP-dependent potassium channels in gerbil hippocampus. Exp. Neurol. 183 (2003) 180-187
37. Nishio S., Yunoki M., Chen Z.F., Anzivino M.J., and Lee K.S. Ischemic tolerance in the rat neocortex following hypothermic preconditioning. J. Neurosurg. 93 (2000) 845-851
38. Noraberg J., Kristensen B.W., and Zimmer J. Markers for neuronal degeneration in organotypic slice cultures. Brain Res. Brain Res. Protoc. 3 (1999) 278-290
39. Park C., Cho I.H., Kim D., Jo E.K., Choi S.Y., Oh S.B., Park K., Kim J.S., and Lee S.J. Toll-like receptor 2 contributes to glial cell activation and heme oxygenase-1 expression in traumatic brain injury. Neurosci. Lett. 431 (2008) 123-128
40. Pellegrini-Giampietro D.E., Peruginelli F., Meli E., Cozzi A., Albani-Torregrossa S., Pellicciari R., and Moroni F. Protection with metabotropic glutamate 1 receptor antagonists in models of ischemic neuronal death: time-course and mechanisms. Neuropharmacology 38 (1999) 1607-1619
41. Perez-Pinzon M.A. Excitatory and inhibitory pathways for anoxic preconditioning neuroprotection in hippocampal slices. Adv. Exp. Med. Biol. 471 (1999) 165-173
42. Perez-Pinzon M.A., Mumford P.L., Rosenthal M., and Sick T.J. Anoxic preconditioning in hippocampal slices: role of adenosine. Neuroscience 75 (1996) 687-694
43. Perez-Pinzon M.A., and Born J.G. Rapid preconditioning neuroprotection following anoxia in hippocampal slices: role of the K+ ATP channel and protein kinase C. Neuroscience 89 (1999) 453-459
44. Satoh T., Okamoto S.I., Cui J., Watanabe Y., Furuta K., Suzuki M., Tohyama K., and Lipton S.A. Activation of the Keap1/Nrf2 pathway for neuroprotection by electrophilic [correction of electrophillic] phase II inducers. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 768-773
45. Semenza G.L. Hypoxia-inducible factor 1 (HIF-1) pathway. Sci. STKE 2007 cm8 (2007)
46. Shen H., Chan J., Kass I.S., and Bergold P.J. Transient acidosis induces delayed neurotoxicity in cultured hippocampal slices. Neurosci. Lett. 185 (1995) 115-118
47. Steiger H.J., and Hanggi D. Ischaemic preconditioning of the brain, mechanisms and applications. Acta Neurochir. (Wien) 149 (2007) 1-10
48. Stenzel-Poore M.P., Stevens S.L., Xiong Z., Lessov N.S., Harrington C.A., Mori M., Meller R., Rosenzweig H.L., Tobar E., Shaw T.E., Chu X., and Simon R.P. Effect of ischaemic preconditioning on genomic response to cerebral ischaemia: similarity to neuroprotective strategies in hibernation and hypoxia-tolerant states. Lancet 362 (2003) 1028-1037
49. Stenzel-Poore M.P., Stevens S.L., and Simon R.P. Genomics of preconditioning. Stroke 35 (2004) 2683-2686
50. Stevens S.L., and Stenzel-Poore M.P. Toll-like receptors and tolerance to ischaemic injury in the brain. Biochem. Soc. Trans. 34 (2006) 1352-1355
51. Tang Y., Pacary E., Freret T., Divoux D., Petit E., Schumann-Bard P., and Bernaudin M. Effect of hypoxic preconditioning on brain genomic response before and following ischemia in the adult mouse: identification of potential neuroprotective candidates for stroke. Neurobiol. Dis. 21 (2006) 18-28
52. Tremblay R., Chakravarthy B., Hewitt K., Tauskela J., Morley P., Atkinson T., and Durkin J.P. Transient NMDA receptor inactivation provides long-term protection to cultured cortical neurons from a variety of death signals. J. Neurosci. 20 (2000) 7183-7192
53. Vieira H.L., Queiroga C.S., and Alves P.M. Pre-conditioning induced by carbon monoxide provides neuronal protection against apoptosis. J. Neurochem. 107 (2008) 375-384
54. Wang R.M., Yang F., and Zhang Y.X. Preconditioning-induced activation of ERK5 is dependent on moderate Ca2+ influx via NMDA receptors and contributes to ischemic tolerance in the hippocampal CA1 region of rats. Life Sci. 79 (2006) 1839-1846
55. Werner C.G., Scartabelli T., Pancani T., Landucci E., Moroni F., and Pellegrini-Giampietro D.E. Differential role of mGlu1 and mGlu5 receptors in rat hippocampal slice models of ischemic tolerance. Eur. J. Neurosci. 25 (2007) 3597-3604
56. Zhang F., Signore A.P., Zhou Z., Wang S., Cao G., and Chen J. Erythropoietin protects CA1 neurons against global cerebral ischemia in rat: potential signaling mechanisms. J. Neurosci. Res. 83 (2006) 1241-1251