Validation of organotypical hippocampal slice cultures as an ex vivo model of brain ischemia: Different roles of NMDA receptors in cell death signalling after exposure to NMDA or oxygen and glucose deprivation

Cell and Tissue Research

Volumn 345, Issue 3, 2011, Pages 329-341

  Ahlgren, Hanna ^a,b   Henjum, Kristi ^a   Ottersen, Ole Petter ^a   Rundén Pran, Elise ^a,c  

^a UNIVERSITY OF OSLO   (Norway)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c NORWEGIAN INSTITUTE FOR AIR RESEARCH   (Norway)

Author keywords

Excitotoxicity; Ischemia; NMDA receptors; Organotypical hippocampal slice cultures; Oxygen and glucose deprivation (OGD)

Indexed keywords

DIZOCILPINE; GLUCOSE; MESSENGER RNA; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2A; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; OXYGEN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN ISCHEMIA; BRAIN SLICE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; EX VIVO STUDY; EXCITOTOXICITY; GENE EXPRESSION REGULATION; HIPPOCAMPUS; INTRACELLULAR SIGNALING; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1 GENE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2A GENE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B GENE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR GENE; NERVE CELL CULTURE; NERVE CELL NECROSIS; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; RECEPTOR GENE; VALIDATION PROCESS; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; BRAIN ISCHEMIA; CATTLE; CELL DEATH; CHICKENS; DIZOCILPINE MALEATE; GENE EXPRESSION REGULATION; GLUCOSE; HYDROGEN-ION CONCENTRATION; MODELS, BIOLOGICAL; N-METHYLASPARTATE; NEUROTOXINS; ORGAN CULTURE TECHNIQUES; OXYGEN; PROTEIN SUBUNITS; RATS; RATS, WISTAR; RECEPTORS, N-METHYL-D-ASPARTATE; REPRODUCIBILITY OF RESULTS; RNA, MESSENGER; SIGNAL TRANSDUCTION;

EID: 80052779624     PISSN: 0302766X     EISSN: 14320878     Source Type: Journal    
DOI: 10.1007/s00441-011-1218-2     Document Type: Article

References (58)

1. Aamodt SM, Constantine-Paton M (1999) The role of neural activity in synaptic development and its implications for adult brain function. Adv Neurol 79:133-144
2. Aarts M, Iihara K, Wei WL, Xiong ZG, Arundine M, Cerwinski W, MacDonald JF, Tymianski M (2003) A key role for TRPM7 channels in anoxic neuronal death. Cell 115:863-877 (Pubitemid 38058498)
3. Arundine M, Tymianski M (2003) Molecular mechanisms of calcium-dependent neurodegeneration in excitotoxicity. Cell Calcium 34:325-337 (Pubitemid 37021228)
4. Benveniste H, Drejer J, Schousboe A, Diemer NH (1984) Elevation of the extracellular concentrations of glutamate and aspartate in rat hippocampus during transient cerebral ischemia monitored by intracerebral microdialysis. J Neurochem 43:1369-1374 (Pubitemid 15205893)
5. Bliss TV, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31-39 (Pubitemid 23020772)
6. C Bonde J Noraberg H Noer J Zimmer 2005 Ionotropic glutamate receptors and glutamate transporters are involved in necrotic neuronal cell death induced by oxygen-glucose deprivation of hippocampal slice cultures Neuroscience 136 779 794 16344151 10.1016/j.neuroscience.2005.07.020 1:CAS:528:DC%2BD2MXhtlaiurvF (Pubitemid 41774724)
7. Brewer LD, Thibault O, Staton J, Thibault V, Rogers JT, Garcia-Ramos G, Kraner S, Landfield PW, Porter NM (2007) Increased vulnerability of hippocampal neurons with age in culture: temporal association with increases in NMDA receptor current, NR2A subunit expression and recruitment of L-type calcium channels. Brain Res 1151:20-31 (Pubitemid 46709872)
8. Camacho A, Massieu L (2006) Role of glutamate transporters in the clearance and release of glutamate during ischemia and its relation to neuronal death. Arch Med Res 37:11-18 (Pubitemid 41727885)
9. Choi DW (1992) Excitotoxic cell death. J Neurobiol 23:1261-1276
10. Clark AJ, Bissinger P, Bullock DW, Damak S, Wallace R, Whitelaw CB, Yull F (1994) Chromosomal position effects and the modulation of transgene expression. Reprod Fertil Dev 6:589-598
11. DJ Cook M Tymianski 2011 Translating promising preclinical neuroprotective therapies to human stroke trials Expert Rev Cardiovasc Ther 9 433 449 21517728 10.1586/erc.11.34
12. S Dos-Anjos B Martinez-Villayandre S Montori CC Perez-Garcia A Fernandez-Lopez 2009 Early modifications in N-methyl-D-aspartate receptor subunit mRNA levels in an oxygen and glucose deprivation model using rat hippocampal brain slices Neuroscience 164 1119 1126 19761817 10.1016/j.neuroscience.2009.09.019 1:CAS:528:DC%2BD1MXhtlymurjJ
13. Dravid SM, Erreger K, Yuan H, Nicholson K, Le P, Lyuboslavsky P, Almonte A, Murray E, Mosely C, Barber J, et al. (2007) Subunit-specific mechanisms and proton sensitivity of NMDA receptor channel block. J Physiol 581:107-128 (Pubitemid 46712031)
14. Gähwiler BH, Capogna M, Debanne D, McKinney RA, Thompson SM (1997) Organotypic slice cultures: a technique has come of age. Trends Neurosci 20:471-477
15. AC Gambrill A Barria 2011 NMDA receptor subunit composition controls synaptogenesis and synapse stabilization Proc Natl Acad Sci USA 108 5855 5860 21427228 10.1073/pnas.1012676108 1:CAS:528:DC%2BC3MXkvVCmsLc%3D
16. Gao J, Duan B, Wang DG, Deng XH, Zhang GY, Xu L, Xu TL (2005) Coupling between NMDA receptor and acid-sensing ion channel contributes to ischemic neuronal death. Neuron 48:635-646 (Pubitemid 41654684)
17. Hardingham GE, Fukunaga Y, Bading H (2002) Extrasynaptic NMDARs oppose synaptic NMDARs by triggering CREB shut-off and cell death pathways. Nat Neurosci 5:405-414 (Pubitemid 34454245)
18. GE Hardingham H Bading 2010 Synaptic versus extrasynaptic NMDA receptor signalling: implications for neurodegenerative disorders Nat Rev Neurosci 11 682 696 20842175 10.1038/nrn2911 1:CAS:528:DC%2BC3cXhtFGntL7P
19. Kohr G (2006) NMDA receptor function: subunit composition versus spatial distribution. Cell Tissue Res 326:439-446 (Pubitemid 44435819)
20. Kristensen BW, Noraberg J, Zimmer J (2001) Comparison of excitotoxic profiles of ATPA, AMPA, KA and NMDA in organotypic hippocampal slice cultures. Brain Res 917:21-44 (Pubitemid 32973195)
21. JH Laake FM Haug T Wieloch OP Ottersen 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 10446412 10.1016/S1385-299X(99)00021-5 1:STN:280:DyaK1Mznslaqsw%3D%3D (Pubitemid 29396417)
22. Lipton SA, Rosenberg PA (1994) Excitatory amino acids as a final common pathway for neurologic disorders. N Engl J Med 330:613-622
23. Liu Y, Wong TP, Aarts M, Rooyakkers A, Liu L, Lai TW, Wu DC, Lu J, Tymianski M, Craig AM, et al. (2007) NMDA receptor subunits have differential roles in mediating excitotoxic neuronal death both in vitro and in vivo. J Neurosci 27:2846-2857 (Pubitemid 46438991)
24. Malenka RC, Nicoll RA (1999) Long-term potentiation - a decade of progress? Science 285:1870-1874
25. Martel MA, Wyllie DJ, Hardingham GE (2009) In developing hippocampal neurons, NR2B-containing N-methyl-D-aspartate receptors (NMDARs) can mediate signaling to neuronal survival and synaptic potentiation, as well as neuronal death. Neuroscience 158:334-343
26. Martinez-Sanchez M, Striggow F, Schroder UH, Kahlert S, Reymann KG, Reiser G (2004) Na(+) and Ca(2+) homeostasis pathways, cell death and protection after oxygen-glucose-deprivation in organotypic hippocampal slice cultures. Neuroscience 128:729-740 (Pubitemid 39298426)
27. AJ Milnerwood CM Gladding MA Pouladi AM Kaufman RM Hines JD Boyd RW Ko OC Vasuta RK Graham MR Hayden TH Murphy LA Raymond 2010 Early increase in extrasynaptic NMDA receptor signaling and expression contributes to phenotype onset in Huntington's disease mice Neuron 65 178 190 20152125 10.1016/j.neuron.2010.01.008 1:CAS:528:DC%2BC3cXlt1Kmsbo%3D
28. Montero M, Poulsen FR, Noraberg J, Kirkeby A, van Beek J, Leist M, Zimmer J (2007) Comparison of neuroprotective effects of erythropoietin (EPO) and carbamylerythropoietin (CEPO) against ischemia-like oxygen-glucose deprivation (OGD) and NMDA excitotoxicity in mouse hippocampal slice cultures. Exp Neurol 204:106-117 (Pubitemid 46330263)
29. H Monyer R Sprengel R Schoepfer A Herb M Higuchi H Lomeli N Burnashev B Sakmann PH Seeburg 1992 Heteromeric NMDA receptors: molecular and functional distinction of subtypes Science 256 1217 1221 1350383 10.1126/science.256.5060. 1217 1:CAS:528:DyaK3sXisVOrs7o%3D
30. Monyer H, Burnashev N, Laurie DJ, Sakmann B, Seeburg PH (1994) Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12:529-540 (Pubitemid 24100885)
31. K Moriyoshi M Masu T Ishii R Shigemoto N Mizuno S Nakanishi 1991 Molecular cloning and characterization of the rat NMDA receptor Nature 354 31 37 1834949 10.1038/354031a0 1:CAS:528:DyaK3sXhs1Cjuw%3D%3D (Pubitemid 21896774)
32. Nedergaard M, Kraig RP, Tanabe J, Pulsinelli WA (1991) Dynamics of interstitial and intracellular pH in evolving brain infarct. Am J Physiol 260:R581-588
33. Newell DW, Barth A, Papermaster V, Malouf AT (1995) Glutamate and non-glutamate receptor mediated toxicity caused by oxygen and glucose deprivation in organotypic hippocampal cultures. J Neurosci 15:7702-7711
34. J Noraberg CV Jensen C Bonde M Montero JV Nielsen NA Jensen J Zimmer 2007 The developmental expression of fluorescent proteins in organotypic hippocampal slice cultures from transgenic mice and its use in the determination of excitotoxic neurodegeneration Altern Lab Anim 35 61 70 17411353 1:CAS:528:DC%2BD2sXksVKrsLk%3D (Pubitemid 46596006)
35. Noraberg J, Kristensen BW, Zimmer J (1999) Markers for neuronal degeneration in organotypic slice cultures. Brain Res Brain Res Protoc 3:278-290 (Pubitemid 29023528)
36. JW Olney 1969 Brain lesions, obesity, and other disturbances in mice treated with monosodium glutamate Science 164 719 721 5778021 10.1126/science.164.3880.719 1:CAS:528:DyaF1MXktFWhurw%3D
37. A Ring R Tanso J Noraberg 2010 The use of organotypic hippocampal slice cultures to evaluate protection by non-competitive NMDA receptor antagonists against excitotoxicity Altern Lab Anim 38 71 82 20377305 1:CAS:528: DC%2BC3cXlvVahsLc%3D
38. V Rolseth E Runden-Pran CG Neurauter A Yndestad L Luna P Aukrust OP Ottersen M Bjoras 2008 Base excision repair activities in organotypic hippocampal slice cultures exposed to oxygen and glucose deprivation DNA Repair (Amst) 7 869 878 10.1016/j.dnarep.2008.02.009 1:CAS:528:DC%2BD1cXmt1OktLc%3D
39. Rossi DJ, Oshima T, Attwell D (2000) Glutamate release in severe brain ischaemia is mainly by reversed uptake. Nature 403:316-321 (Pubitemid 30062388)
40. E Runden-Pran FM Haug JF Storm OP Ottersen 2002 BK channel activity determines the extent of cell degeneration after oxygen and glucose deprivation: a study in organotypical hippocampal slice cultures Neuroscience 112 277 288 12044446 10.1016/S0306-4522(02)00092-1 1:CAS:528:DC%2BD38XktVartbc%3D (Pubitemid 34607012)
41. E Runden-Pran R Tanso FM Haug OP Ottersen A Ring 2005 Neuroprotective effects of inhibiting N-methyl-D-aspartate receptors, P2X receptors and the mitogen-activated protein kinase cascade: a quantitative analysis in organotypical hippocampal slice cultures subjected to oxygen and glucose deprivation Neuroscience 136 795 810 16344152 10.1016/j.neuroscience.2005.08.069 1:CAS:528:DC%2BD2MXhtlaiurjM (Pubitemid 41774725)
42. Runden E, Seglen PO, Haug FM, Ottersen OP, Wieloch T, Shamloo M, Laake JH (1998) Regional selective neuronal degeneration after protein phosphatase inhibition in hippocampal slice cultures: evidence for a MAP kinase-dependent mechanism. J Neurosci 18:7296-7305 (Pubitemid 28425814)
43. A Rytter T Cronberg F Asztely S Nemali T Wieloch 2003 Mouse hippocampal organotypic tissue cultures exposed to in vitro "ischemia" show selective and delayed CA1 damage that is aggravated by glucose J Cereb Blood Flow Metab 23 23 33 12500088 10.1097/00004647-200301000-00003 1:CAS:528:DC%2BD38Xpslakt70%3D (Pubitemid 36015091)
44. K Sakimura T Kutsuwada I Ito T Manabe C Takayama E Kushiya T Yagi S Aizawa Y Inoue H Sugiyama 1995 Reduced hippocampal LTP and spatial learning in mice lacking NMDA receptor epsilon 1 subunit Nature 373 151 155 7816096 10.1038/373151a0 1:CAS:528:DyaK2MXjtFSrtLo%3D
45. R Sattler Z Xiong WY Lu JF MacDonald M Tymianski 2000 Distinct roles of synaptic and extrasynaptic NMDA receptors in excitotoxicity J Neurosci 20 22 33 10627577 1:CAS:528:DC%2BD3cXhtF2itbw%3D (Pubitemid 30220487)
46. Sheng M, Cummings J, Roldan LA, Jan YN, Jan LY (1994) Changing subunit composition of heteromeric NMDA receptors during development of rat cortex. Nature 368:144-147 (Pubitemid 24101524)
47. +] in the hippocampus during recovery from short-term, transient ischemia. J Cereb Blood Flow Metab 12:759-772
48. Stanika RI, Pivovarova NB, Brantner CA, Watts CA, Winters CA, Andrews SB (2009) Coupling diverse routes of calcium entry to mitochondrial dysfunction and glutamate excitotoxicity. Proc Natl Acad Sci U S A 106:9854-9859
49. L Stoppini PA Buchs D Muller 1991 A simple method for organotypic cultures of nervous tissue J Neurosci Methods 37 173 182 1715499 10.1016/0165-0270(91)90128-M 1:STN:280:DyaK3MzltVymtA%3D%3D
50. Sun HS, Jackson MF, Martin LJ, Jansen K, Teves L, Cui H, Kiyonaka S, Mori Y, Jones M, Forder JP, et al. (2009) Suppression of hippocampal TRPM7 protein prevents delayed neuronal death in brain ischemia. Nat Neurosci 12:1300-1307
51. K Szydlowska M Tymianski 2010 Calcium, ischemia and excitotoxicity Cell Calcium 47 122 129 20167368 10.1016/j.ceca.2010.01.003 1:CAS:528: DC%2BC3cXjtVSmsrw%3D
52. Tang CM, Dichter M, Morad M (1990) Modulation of the N-methyl-D-aspartate channel by extracellular H+. Proc Natl Acad Sci U S A 87:6445-6449
53. J von Engelhardt B Doganci V Jensen O Hvalby C Gongrich A Taylor C Barkus DJ Sanderson JN Rawlins PH Seeburg DM Bannerman H Monyer 2008 Contribution of hippocampal and extra-hippocampal NR2B-containing NMDA receptors to performance on spatial learning tasks Neuron 60 846 860 10.1016/j.neuron.2008.09.039
54. L Wise-Faberowski PN Robinson S Rich DS Warner 2009 Oxygen and glucose deprivation in an organotypic hippocampal slice model of the developing rat brain: the effect on N-methyl-D-aspartate subunit composition Anesth Analg 109 205 210 19535712 10.1213/ane.0b013e3181a27e37 1:CAS:528:DC%2BD1MXnsFOqs7k%3D
55. Zhang SJ, Steijaert MN, Lau D, Schutz G, Delucinge-Vivier C, Descombes P, Bading H (2007) Decoding NMDA receptor signaling: identification of genomic programs specifying neuronal survival and death. Neuron 53:549-562 (Pubitemid 46216756)
56. SJ Zhang B Buchthal D Lau S Hayer O Dick M Schwaninger R Veltkamp M Zou U Weiss H Bading 2011 A signaling cascade of nuclear calcium-CREB-ATF3 activated by synaptic NMDA receptors defines a gene repression module that protects against extrasynaptic NMDA receptor-induced neuronal cell death and ischemic brain damage J Neurosci 31 4978 4990 21451036 10.1523/JNEUROSCI.2672-10.2011 1:CAS:528:DC%2BC3MXkslSltbo%3D
57. Zhang SJ, Steijaert MN, Lau D, Schutz G, Delucinge-Vivier C, Descombes P, Bading H (2007) Decoding NMDA receptor signaling: identification of genomic programs specifying neuronal survival and death. Neuron 53:549-562 (Pubitemid 46216756)
58. Zhou M, Baudry M (2006) Developmental changes in NMDA neurotoxicity reflect developmental changes in subunit composition of NMDA receptors. J Neurosci 26:2956-2963