Organotypic hippocampal slice cultures: A model system to study basic cellular and molecular mechanisms of neuronal cell death, neuroprotection, and synaptic plasticity

Neurochemical Research

Volumn 30, Issue 12, 2005, Pages 1521-1528

  Holopainen, Irma E ^a  

^a UNIVERSITY OF TURKU   (Finland)

Author keywords

Excitotoxicity; Hippocampal slice cultures; Nerve cell death; Neuroprotection; Plasticity

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR STIMULATING AGENT; [1 [(1 FORMYL 2 PHENYLETHYL)CARBAMOYL] 2 METHYLPROPYL]CARBAMIC ACID BENZYL ESTER; AMPA RECEPTOR ANTAGONIST; ANTICONVULSIVE AGENT; CALPASTATIN; CARBAMAZEPINE; DIAZEPAM; GABOXADOL; I KAPPA B; K 252A; KAINIC ACID RECEPTOR ANTAGONIST; LAMOTRIGINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; OXCARBAZEPINE; PROTEIN TYROSINE KINASE INHIBITOR; TIABABINE; UNCLASSIFIED DRUG;

BRAIN DAMAGE; BRAIN DISEASE; BRAIN FUNCTION; BRAIN HYPOXIA; BRAIN ISCHEMIA; BRAIN REGION; BRAIN SLICE; CELL CULTURE; CELL MATURATION; CELL PROLIFERATION; CELL TYPE; EPILEPSY; EXCITOTOXICITY; HIPPOCAMPUS; HUMAN; INFORMATION PROCESSING; LEARNING; MEMORY; MOLECULAR DYNAMICS; NERVE CELL; NERVE CELL CULTURE; NERVE CELL NECROSIS; NERVE CELL PLASTICITY; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; REVIEW;

ANIMALS; CELL DEATH; CYTOPROTECTION; HIPPOCAMPUS; MODELS, BIOLOGICAL; NEURONAL PLASTICITY; NEURONS; ORGAN CULTURE TECHNIQUES;

MAMMALIA;

EID: 29144533824     PISSN: 03643190     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11064-005-8829-5     Document Type: Review

References (72)

1. D. G. Amaral 1978 A Golgi study of cell types in the hilar region of the hippocampus in the rat J. Comp. Neurol. 182 851 914
2. D. G. Amaral N. Ishizuka B. Claiborne 1990 Neurons, numbers and the hippocampal network Prog. Brain Res. 83 1 11
3. E. W. Lothman E. H. Bertram 3rd J. L. Stringer 1991 Functional anatomy of hippocampal seizures Prog. Neurobiol. 37 1 82
4. T. F. Freund G. Buzsaki 1996 Interneurons of the hippocampus Hippocampus 6 347 470
5. L. Stoppini P. A. Buchs D. Muller 1991 A simple method for organotypic cultures of nervous tissue J. Neurosci. Methods 37 173 182
6. M. Gatherer L. E. Sundström 1998 Mossy fibre innervation is not required for the development of kainic acid toxicity in organotypic hippocampal slice cultures Neurosci. Lett. 253 119 122
7. M. J. Routbort S. B. Bausch J. O. [tmp] McNamara 1999 Seizures, cell death, and mossy fiber sprouting in kainic acid-treated organotypic hippocampal cultures Neuroscience 94 755 765
8. S. B. Bausch J. O. [tmp] McNamara 2000 Synaptic connections from multiple subfields contribute to granule cell hyperexcitability in hippocampal slice cultures J. Neurophysiol. 84 2918 2932
9. I. E. Holopainen H. B. Lauren A. Romppanen F. R. Lopez-Picon 2001 Changes in neurofilament protein-immunoreactivity after kainic acid treatment of organotypic hippocampal slice cultures J. Neurosci. Res. 66 620 629
10. Z. Xiang M. Yuan G. W. Hassen M. Gampel P. J. Bergold 2004 Lactate induced excitotoxicity in hippocampal slice cultures Exp. Neurol. 186 70 77
11. A. R. Schlessinger W. M. Cowan D. I. Gottlieb 1975 An autoradiographic study of the time of origin and the pattern of granule cell migration in the dentate gyrus of the rat J. Comp. Neurol. 159 149 175
12. S. A. Bayer 1985 Neuron production in the hippocampus and olfactory bulb of the adult rat brain: addition or replacement? Ann. NY Acad. Sci. 457 163 172
13. M. E. Dailey J. Buchanan D. E. Bergles S. J. Smith 1994 Mossy fiber growth and synaptogenesis in rat hippocampal slices in vitro J. Neurosci. 14 1060 1078
14. M. Frotscher S. Zafirov B. Heimrich 1995 Development of identified neuronal types and of specific synaptic connections in slice cultures of rat hippocampus Prog. Neurobiol. 45 143 164
15. B. H. Gähwiler M. Capogna D. Debanne R. A. [tmp] McKinney S.M. Thompson 1997 Organotypic slice cultures: A technique has come of age Trends Neurosci. 20 471 477
16. A receptor subunit expression in organotypic hippocampal slice cultures Neuroscience 118 967 974
17. B. W. Coltman E. M. Earley A. Shahar F. E. Dudek C. F. Ide 1995 Factors influencing mossy fiber collateral sprouting in organotypic slice cultures of neonatal mouse hippocampus J. Comp. Neurol. 362 209 222
18. R. Gutierrez U. Heinemann 1999 Synaptic reorganization in explanted cultures of rat hippocampus Brain Res. 815 304 316
19. M. M. Lindroos S. L. Soini T. K. Kukko-Lukjanov E. R. Korpi D. Lovinger I. E. Holopainen 2005 Maturation of cultured hippocampal slices results in increased excitability in granule cells Int. J. Dev. Neurosci. 23 65 73
20. J. Yuan M. Lipinski A. Degterev 2003 Diversity in the mechanisms of neuronal cell death Neuron 40 401 413
21. R. Schmidt-Kastner T. F. Freund 1991 Selective vulnerability of the hippocampus in brain ischemia Neuroscience 40 599 636
22. J. M. Lee G. J. Zipfel D. W. Choi 1999 The changing landscape of ischaemic brain injury mechanisms Nature 399 A7 A14
23. M. P. Mattson C. Culmsee Z. F. Yu 2000 Apoptotic and antiapoptotic mechanisms in stroke Cell Tissue Res. 301 173 187
24. J. Bengzon P. Mohapel C. T. Ekdahl O. Lindvall 2002 Neuronal apoptosis after brief and prolonged seizures Prog. Brain Res. 135 111 119
25. A. Rami 2003 Ischemic neuronal death in the rat hippocampus: The calpain-calpastatin-caspase hypothesis Neurobiol. Dis. 13 75 88
26. B. W. Kristensen J. Noraberg J. Zimmer 2001 Comparison of excitotoxic profiles of ATPA, AMPA, KA and NMDA in organotypic hippocampal slice cultures Brain Res. 917 21 44
27. J. J. Vornov R. C. Tasker J. T. Coyle 1991 Direct observation of the agonist-specific regional vulnerability to glutamate NMDA, and kainate neurotoxicity in organotypic hippocampal cultures Exp. Neurol. 114 11 22
28. A. J. Bruce S. Sakhi S. S. Schreiber M. Baudry 1995 Development of kainic acid and N-methyl-d-aspartic acid toxicity in organotypic hippocampal cultures Exp. Neurol. 132 209 219
29. I. E. Holopainen J. Järvelä F. R. Lopez-Picon L. J. Pelliniemi T. K. Kukko-Lukjanov 2004 Mechanisms of kainate-induced region-specific neuronal death in immature organotypic hippocampal slice cultures Neurochem. Int. 45 1 10
30. H. E. Scharfman 1994 EPSPs of dentate gyrus granule cells during epileptiform bursts of dentate hilar "mossy" cells and area CA3 pyramidal cells in disinhibited rat hippocampal slices J. Neurosci. 14 6041 6057
31. M. M. Okazaki D. A. Evenson J. V. Nadler 1995 Hippocampal mossy fiber sprouting and synapse formation after status epilepticus in rats: Visualization after retrograde transport of biocytin J. Comp. Neurol. 352 515 534
32. M. M. Okazaki P. Molnar J. V. Nadler 1999 Recurrent mossy fiber pathway in rat dentate gyrus: Synaptic currents evoked in presence and absence of seizure-induced growth J. Neurophysiol. 81 1645 1660
33. M. Kobayashi P. S. Buckmaster 2003 Reduced inhibition of dentate granule cells in a model of temporal lobe epilepsy J. Neurosci. 23 2440 2452
34. S. B. Bausch J. O. [tmp] McNamara 2004 Contributions of mossy fiber and CA1 pyramidal cell sprouting to dentate granule cell hyperexcitability in kainic acid-treated hippocampal slice cultures J. Neurophysiol. 92 3582 3595
35. W. C. Earnshaw L. M. Martins S. H. Kaufmann 1999 Mammalian caspases: Structure, activation, substrates, and functions during apoptosis Annu. Rev. Biochem. 68 383 424
36. G. Kroemer J. C. Reed 2000 Mitochondrial control of cell death Nat. Med. 6 513 519
37. P. S. Sastry K. S. Rao 2000 Apoptosis and the nervous system J. Neurochem. 74 1 20
38. B. M. Polster G. Fiskum 2004 Mitochondrial mechanisms of neural cell apoptosis J. Neurochem. 90 1281 1289
39. W. Liu R. Liu J. T. Chun R. Bi W. Hoe S. S. Schreiber M. Baudry 2001 Kainate excitotoxicity in organotypic hippocampal slice cultures: Evidence for multiple apoptotic pathways Brain Res. 916 239 248
40. P. Bittigau M. Sifringer D. Pohl D. Stadthaus M. Ishimaru H. Shimizu M. Ikeda D. Lang A. Speer J. W. Olney C. Ikonomidou 1999 Apoptotic neurodegeneration following trauma is markedly enhanced in the immature brain Ann. Neurol. 45 724 735
41. B. R. Hu C. L. Liu Y. Ouyang K. Blomgren B. K. Siesjo 2000 Involvement of caspase-3 in cell death after hypoxia-ischemia declines during brain maturation J. Cereb. Blood Flow Metab. 20 1294 1300
42. Z. Z. Khaing C. S. Weickert D. R. Weinberger B. K. Lipska 2000 Differential DNA damage in response to the neonatal and adult excitotoxic hippocampal lesion in rats Eur. J. Neurosci. 12 4424 4433
43. A. G. Yakovlev K. Ota G. Wang V. Movsesyan W. L. Bao K. Yoshihara A. I. Faden 2001 Differential expression of apoptotic protease-activating factor-1 and caspase-3 genes and susceptibility to apoptosis during brain development and after traumatic brain injury J. Neurosci. 21 7439 7446
44. T. Borsello K. Croquelois J. P. Hornung P. G. Clarke 2003 N-methyl-d-aspartate-triggered neuronal death in organotypic hippocampal cultures is endocytic, autophagic and mediated by the c-Jun N-terminal kinase pathway Eur. J. Neurosci. 18 473 485
45. J. Chen T. Nagayama K. Jin R. A. Stetler R. L. Zhu S. H. Graham R. P. Simon 1998 Induction of caspase-3-like protease may mediate delayed neuronal death in the hippocampus after transient cerebral ischemia J. Neurosci. 18 4914 4928
46. K. Hewitt D. Corbett 1992 Combined treatment with MK-801 and nicardipine reduces global ischemic damage in the gerbil Stroke 23 82 86
47. B. A. Eldadah A. I. Faden 2000 Caspase pathways, neuronal apoptosis, and CNS injury J. Neurotrauma 17 811 829
48. S. H. Graham J. Chen 2001 Programmed cell death in cerebral ischemia J. Cereb. Blood Flow Metab. 21 99 109
49. S. Cho D. Liu D. Fairman P. Li L. Jenkins P. [tmp] McGonigle A. Wood 2004 Spatiotemporal evidence of apoptosis-mediated ischemic injury in organotypic hippocampal slice cultures Neurochem. Int. 45 117 127
50. S. M. Allan N. J. Rothwell 2001 Cytokines and acute neurodegeneration Nat. Rev. Neurosci. 2 734 744
51. J. Y. Zou F. T. Crews 2005 TNF alpha potentiates glutamate neurotoxicity by inhibiting glutamate uptake in organotypic brain slice cultures: Neuroprotection by NF kappa B inhibition Brain Res. 1034 11 24
52. M. K. Lee D. W. Cleveland 1996 Neuronal intermediate filaments Annu. Rev. Neurosci. 19 187 217
53. Y. H. Chou O. Skalli R. D. Goldman 1997 Intermediate filaments and cytoplasmic networking: New connections and more functions Curr. Opin. Cell Biol. 9 49 53
54. K. S. Lee S. Frank P. Vanderklish A. Arai G. Lynch 1991 Inhibition of proteolysis protects hippocampal neurons from ischemia Proc. Natl. Acad. Sci. USA 88 7233 7237
55. C. Brana C. D. Benham L. E. Sundstrom 1999 Calpain activation and inhibition in organotypic rat hippocampal slice cultures deprived of oxygen and glucose Eur. J. Neurosci. 11 2375 2384
56. 2+ homeostasis pathways, cell death and protection after oxygen-glucose-deprivation in organotypic hippocampal slice cultures Neuroscience 128 729 740
57. H. Jourdi T. Yanagihara U. Martinez X. Bi G. Lynch M. Baudry 2005 Effects of positive AMPA receptor modulators on calpain-mediated spectrin degradation in cultured hippocampal slices Neurochem. Int. 46 31 40
58. F. Galeffi R. Sah B. B. Bond A. Geaorge R. D. Schwarz-Bloom 2004 Changes in intracellular chloride after oxygen-glucose deprivation of the adult hippocampal slice: Effect of diazepam J. Neurosci. 24 4478 4488
59. D. M. Gellerman X. Bi M. Baudry 1997 NMDA receptor-mediated regulation of AMPA receptor properties in organotypic hippocampal slice cultures J. Neurochem. 69 131 136
60. Y. Adamchik A. Baskys 2000 Glutamate-mediated neuroprotection against N-methyl-d-aspartate toxicity: A role for metabotropic glutamate receptors Neuroscience 99 731 736
61. Y. Sagara D. Schubert 1998 The activation of metabotropic glutamate receptors protects nerve cells from oxidative stress J. Neurosci. 18 6662 6671
62. A. Kalda A. Kaasik V. Vassiljev P. Pokk A. Zharkovsky 2000 Neuroprotective action of group I metabotropic glutamate receptor agonists against oxygen-glucose deprivation-induced neuronal death Brain Res. 853 370 373
63. M. Blaabjerg L. Fang J. Zimmer A. Baskys 2003 Neuroprotection against NMDA excitotoxicity by group I metabotropic glutamate receptors is associated with reduction of NMDA stimulated currents Exp. Neurol. 183 573 580
64. J. C. Rekling 2003 Neuroprotective effects of anticonvulsants in rat hippocampal slice cultures exposed to oxygen/glucose deprivation Neurosci. Lett. 335 167 170
65. A receptor agonist THIP is neuroprotective in organotypic hippocampal slice cultures Brain Res. 973 303 306
66. C. M. Gall P. J. Isackson 1989 Limbic seizures increase neuronal production of messenger RNA for nerve growth factor Science 245 758 761
67. R. Koyama M. K. Yamada S. Fujisawa R. Katoh-Semba N. Matsuki Y. Ikegaya 2004 Brain-derived neurotrophic factor induces hyperexcitabile reentrant circuits in the dentate gyrus J. Neurosci. 24 7215 7224
68. S. C. Danzer K. R. Crooks D. C. Lo J. O. [tmp] McNamara 2002 Increased expression of brain-derived neurotrophic factor induces formation of basal dendrites and axonal branching in dentate granule cells in hippocampal explant cultures J. Neurosci. 22 9754 9763
69. O. Raineteau L. Rietschin G. Gradwohl F. Guillemot B. H. Gähwiler 2004 Neurogenesis in hippocampal slice cultures Mol. Cell Neurosci. 26 241 250
70. P. S. Eriksson E. Perfilieva T. Bjork-Eriksson A. M. Alborn C. Nordborg D. A. Peterson F. H. Gage 1998 Neurogenesis in the adult human hippocampus Nat. Med. 4 1313 1317
71. H. van Praag A. F. Schinder B. R. Christie N. Toni T. D. Palmer F. H. Gage 2002 Functional neurogenesis in the adult hippocampus Nature 415 1030 1034
72. M. Kamada R. Y. Li M. Hashimoto M. Kakuda H. Okada Y. Koyanagi T. Ishizuka H Yawo 2004 Intrinsic and spontaneous neurogenesis in the postnatal slice culture of rat hippocampus Eur. J. Neurosci. 20 2499 2508