Stretch-induced injury in organotypic hippocampal slice cultures reproduces in vivo post-traumatic neurodegeneration: Role of glutamate receptors and voltage-dependent calcium channels

Journal of Neurochemistry

Volumn 101, Issue 2, 2007, Pages 434-447

  Cater, Heather L ^a,d   Gitterman, Daniel ^b,e   Davis, Susan M ^a   Benham, Christopher D ^b,f   Morrison III, Barclay ^c   Sundstrom, Lars E ^a  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^b GLAXOSMITHKLINE   (United Kingdom)

^c Columbia University ^*  (United States)

^d Biomedical Sciences Building   (United Kingdom)

^e Vernalis PLC   (United Kingdom)

^f UNIVERSITY OF HERTFORDSHIRE   (United Kingdom)

Author keywords

Calcium; Electrophysiology; Glutamate; Immunohistochemistry; Trauma; Traumatic brain injury

Indexed keywords

1 (4 AMINOPHENYL) 3,4 DIHYDRO 4 METHYL 3 METHYLCARBAMOYL 7,8 METHYLENEDIOXY 5H 2,3 BENZODIAZEPINE; 4 (3 PHOSPHONOPROPYL) 2 PIPERAZINECARBOXYLIC ACID; DIZOCILPINE; NIFEDIPINE; OMEGA CONOTOXIN MVIIA; SILICONE;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DEGENERATION; BRAIN SLICE; CONTROLLED STUDY; DISEASE SEVERITY; HIPPOCAMPUS; IMMUNOREACTIVITY; IN VIVO CULTURE; NERVE CELL LESION; NONHUMAN; ORGAN CULTURE; PRIORITY JOURNAL; RAT; SYNAPSE; TRAUMATIC BRAIN INJURY;

ANIMALS; BRAIN INJURIES; CALCIUM CHANNEL BLOCKERS; CALCIUM CHANNELS; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; GLUTAMIC ACID; HIPPOCAMPUS; MEMBRANES, ARTIFICIAL; MICROTUBULE-ASSOCIATED PROTEINS; MODELS, NEUROLOGICAL; NERVE DEGENERATION; NEUROPROTECTIVE AGENTS; NEUROTOXINS; ORGAN CULTURE TECHNIQUES; PHYSICAL STIMULATION; RATS; RECEPTORS, GLUTAMATE; SILICONES; STRESS, MECHANICAL; SYNAPTIC TRANSMISSION;

ANIMALIA; RATTUS;

EID: 34047112884     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2006.04379.x     Document Type: Article

References (78)

1. Adembri C., Bechi A., Meli E., Gramigni E., Venturi L., Moroni F., De Gaudio A. R. and Pellegrini-Giampietro D. E. (2004) Erythropoietin attenuates post-traumatic injury in organotypic hippocampal slices. J. Neurotrauma 21, 1103-1112.
2. Agrawal S. K. and Fehlings M. G. (1997) Role of NMDA and non-NMDA ionotropic glutamate receptors in traumatic spinal cord axonal injury. J. Neurosci. 17, 1055-1063.
3. Agrawal S. K., Nashmi R. and Fehlings M. G. (2000) Role of L- and N-type calcium channels in the pathophysiology of traumatic spinal cord white matter injury. Neuroscience 99, 179-188.
4. Allen J. W., Knoblach S. M. and Faden A. I. (1999) Combined mechanical trauma and metabolic impairment in vitro induces NMDA receptor-dependent neuronal cell death and caspase-3-dependent apoptosis. FASEB J. 13, 1875-1882.
5. Bandak F. A. (1995) On the mechanics of impact neurotrauma: a review and critical synthesis. J. Neurotrauma 12, 635-649.
6. Berman R. F., Verweij B. H. and Muizelaar J. P. (2000) Neurobehavioral protection by the neuronal calcium channel blocker ziconotide in a model of traumatic diffuse brain injury in rats. J. Neurosurg. 93, 821-828.
7. Blaha G. R., Raghupathi R., Saatman K. E. and McIntosh T. K. (2000) Brain-derived neurotrophic factor administration after traumatic brain injury in the rat does not protect against behavioral or histological deficits. Neuroscience 99, 483-493.
8. Bradshaw D. R., Ivarsson J., Morfey C. L. and Viano D. C. (2001) Simulation of acute subdural hematoma and diffuse axonal injury in coronal head impact. J Biomech. 34, 85-94.
9. Bruns J. Jr and Hauser W. A. (2003) The epidemiology of traumatic brain injury: a review. Epilepsia 44(Suppl. 10), 2-10.
10. Cargill R. S. and Thibault L. E. (1996) Acute alterations in [Ca2 + ]i in NG108-15 cells subjected to high strain rate deformation and chemical hypoxia: an in vitro model for neural trauma. J. Neurotrauma 13, 395-407.
11. Cater H. L., Davis S. M., Morrison B. III and Sundstrom L. E. (2004) Immunohistological characterisation of neuronal process damage in a novel in vitro model of traumatic brain injury. J. Neurotrauma 21, 1275.
12. Cater H. L., Sundstrom L. E. and Morrison B. Jr (2006) Temporal development of hippocampal cell death is dependent on tissue strain but not strain rate. J Biomech. 39, 2810-2818.
13. Colak A., Soy O., Uzun H., Aslan O., Barut S., Belce A., Akyildiz A. and Tasyurekli M. (2003) Neuroprotective effects of GYKI 52466 on experimental spinal cord injury in rats. J. Neurosurg. Spine 98, 275-281.
14. D'Ambrosio R., Maris D. O., Grady M. S., Winn H. R. and Janigro D. (1999) Impaired K(+) homeostasis and altered electrophysiological properties of post-traumatic hippocampal glia. J. Neurosci. 19, 8152-8162.
15. Ellis E. F., McKinney J. S., Willoughby K. A., Liang S. and Povlishock J. T. (1995) A new model for rapid stretch-induced injury of cells in culture: characterization of the model using astrocytes. J. Neurotrauma 12, 325-339.
16. Faden A. I., Demediuk P., Panter S. S. and Vink R. (1989) The role of excitatory amino acids and NMDA receptors in traumatic brain injury. Science 244, 798-800.
17. Folkerts M. M., Berman R. F., Muizelaar J. P. and Rafols J. A. (1998) Disruption of MAP-2 immunostaining in rat hippocampus after traumatic brain injury. J. Neurotrauma 15, 349-363.
18. Gahwiler B. H., Capogna M., Debanne D., McKinney R. A. and Thompson S. M. (1997) Organotypic slice cultures: a technique has come of age. Trends Neurosci. 20, 471-477.
19. Geddes D. M. and Cargill R. S. (2001) An in vitro model of neural trauma: device characterization and calcium response to mechanical stretch. J. Biomech. Eng 123, 247-255.
20. Goda M., Isono M., Fujiki M. and Kobayashi H. (2002) Both MK801 and NBQX reduce the neuronal damage after impact-acceleration brain injury. J. Neurotrauma 19, 1445-1456.
21. Goforth P. B., Ellis E. F. and Satin L. S. (1999) Enhancement of AMPA-mediated current after traumatic injury in cortical neurons. J. Neurosci. 19, 7367-7374.
22. Goforth P. B., Ellis E. F. and Satin L. S. (2004) Mechanical injury modulates AMPA receptor kinetics via an NMDA receptor-dependent pathway. J. Neurotrauma 21, 719-732.
23. Golarai G., Greenwood A. C., Feeney D. M. and Connor J. A. (2001) Physiological and structural evidence for hippocampal involvement in persistent seizure susceptibility after traumatic brain injury. J. Neurosci. 21, 8523-8537.
24. Graham D. I., McIntosh T. K., Maxwell W. L. and Nicoll J. A. (2000) Recent advances in neurotrauma. J. Neuropathol. Exp. Neurol. 59, 641-651.
25. Hamm R. J., O'Dell D. M., Pike B. R. and Lyeth B. G. (1993) Cognitive impairment following traumatic brain injury: the effect of pre- and post-injury administration of scopolamine and MK-801. Brain Res. Cogn Brain Res. 1, 223-226.
26. Hicks R. R., Baldwin S. A. and Scheff S. W. (1997) Serum extravasation and cytoskeletal alterations following traumatic brain injury in rats. Comparison of lateral fluid percussion and cortical impact models. Mol. Chem. Neuropathol. 32, 1-16.
27. Huh J. W., Raghupathi R., Laurer H. L., Helfaer M. A. and Saatman K. E. (2003) Transient loss of microtubule-associated protein 2 immunoreactivity after moderate brain injury in mice. J. Neurotrauma 20, 975-984.
28. Ikonomidou C. and Turski L. (1996) Prevention of trauma-induced neurodegeneration in infant and adult rat brain: glutamate antagonists. Metab Brain Dis. 11, 125-141.
29. Jennett B. (1979) Posttraumatic epilepsy. Adv. Neurol. 22, 137-147.
30. King A. I. (2000) Fundamentals of impact biomechanics: part I - biomechanics of the head, neck, and thorax. Annu. Rev. Biomed. Eng. 2, 55-81.
31. Koura S. S., Doppenberg E. M., Marmarou A., Choi S., Young H. F. and Bullock R. (1998) Relationship between excitatory amino acid release and outcome after severe human head injury. Acta Neurochir. Suppl (Wien.) 71, 244-246.
32. Krassioukov A. V., Ackery A., Schwartz G., Adamchik Y., Liu Y. and Fehlings M. G. (2002) An in vitro model of neurotrauma in organotypic spinal cord cultures from adult mice. Brain Res. Brain Res. Protoc. 10, 60-68.
33. Lammie G. A., Piper I. R., Thomson D. and Brannan F. (1999) Neuropathologic characterization of a rodent model of closed head injury - addition of clinically relevant secondary insults does not significantly potentiate brain damage. J. Neurotrauma 16, 603-615.
34. Laurer H. L., Lenzlinger P. M. and McIntosh T. K. (2000) Models of traumatic brain injury. Eur. J. Trauma 26, 95-110.
35. Lee L. L., Galo E., Lyeth B. G., Muizelaar J. P. and Berman R. F. (2004) Neuroprotection in the rat lateral fluid percussion model of traumatic brain injury by SNX-185, an N-type voltage-gated calcium channel blocker. Exp. Neurol. 190, 70-78.
36. Lewen A., Li G. L., Olsson Y. and Hillered L. (1996) Changes in microtubule-associated protein 2 and amyloid precursor protein immunoreactivity following traumatic brain injury in rat: influence of MK-801 treatment. Brain Res. 719, 161-171.
37. Lewen A., Fredriksson A., Li G. L., Olsson Y. and Hillered L. (1999) Behavioural and morphological outcome of mild cortical contusion trauma of the rat brain: influence of NMDA-receptor blockade. Acta Neurochir. (Wien.) 141, 193-202.
38. Leybaert L. and de Hemptinne A. (1996) Changes of intracellular free calcium following mechanical injury in a spinal cord slice preparation. Exp. Brain Res. 112, 392-402.
39. Lowenstein D. H., Thomas M. J., Smith D. H. and McIntosh T. K. (1992) Selective vulnerability of dentate hilar neurons following traumatic brain injury: a potential mechanistic link between head trauma and disorders of the hippocampus. J. Neurosci. 12, 4846-4853.
40. Margulies S. S., Thibault L. E. and Gennarelli T. A. (1990) Physical model simulations of brain injury in the primate. J. Biomech. 23, 823-836.
41. Matsushita Y., Shima K., Nawashiro H. and Wada K. (2000) Real-time monitoring of glutamate following fluid percussion brain injury with hypoxia in the rat. J. Neurotrauma 17, 143-153.
42. Miyazaki S., Katayama Y., Lyeth B. G., Jenkins L. W., DeWitt D. S., Goldberg S. J., Newlon P. G. and Hayes R. L. (1992) Enduring suppression of hippocampal long-term potentiation following traumatic brain injury in rat. Brain Res. 585, 335-339.
43. Morrison B. III, Pringle A. K., McManus T., Ellard J., Bradley M., Signorelli F., Iannotti F. and Sundstrom L. E. (2002) L-arginyl-3,4-spermidine is neuroprotective in several in vitro models of neurodegeneration and in vivo ischaemia without suppressing synaptic transmission. Br. J. Pharmacol. 137, 1255-1268.
44. Morrison B. III, Cater H. L., Wang C. C.-B., Thomas F. C., Hung C. T., Ateshian G. A. and Sundstrom L. E. (2003) A tissue level tolerance criterion for living brain developed with an in vitro model of traumatic mechanical loading. Stapp Car Crash J. 47, 93-105.
45. Morrison B. III, Cater H. L., Benham C. D. and Sundstrom L. E. (2006) An in vitro model of traumatic brain injury utilising two-dimensional stretch of organotypic hippocampal slice cultures. J Neurosci. Methods 150, 192-201.
46. Olesen J. and Leonardi M. (2003) The burden of brain diseases in Europe. Eur. J. Neurol. 10, 471-477.
47. Ommaya A. K., Goldsmith W. and Thibault L. (2002) Biomechanics and neuropathology of adult and paediatric head injury. Br. J. Neurosurg. 16, 220-242.
48. Palmer A. M., Marion D. W., Botscheller M. L., Swedlow P. E., Styren S. D. and DeKosky S. T. (1993) Traumatic brain injury-induced excitotoxicity assessed in a controlled cortical impact model. J. Neurochem. 61, 2015-2024.
49. Panizzon K. L., Shin D., Frautschy S. and Wallis R. A. (1998) Neuroprotection with Bcl-2(20-34) peptide against trauma. Neuroreport 9, 4131-4136.
50. Pfister B. J., Weihs T. P., Betenbaugh M. and Bao G. (2003) An in vitro uniaxial stretch model for axonal injury. Ann. Biomed. Eng 31, 589-598.
51. Pierce J. E., Smith D. H., Trojanowski J. Q. and McIntosh T. K. (1998) Enduring cognitive, neurobehavioral and histopathological changes persist for up to one year following severe experimental brain injury in rats. Neuroscience 87, 359-369.
52. Prado G. R., Ross J. D., DeWeerth S. P. and LaPlaca M. C. (2005) Mechanical trauma induces immediate changes in neuronal network activity. J. Neural Eng. 2, 148-158.
53. Pringle A. K., Benham C. D., Sim L., Kennedy J., Iannotti F. and Sundstrom L. E. (1996) Selective N-type calcium channel antagonist omega conotoxin MVIIA is neuroprotective against hypoxic neurodegeneration in organotypic hippocampal-slice cultures. Stroke 27, 2124-2130.
54. Randall R. D. and Thayer S. A. (1992) Glutamate-induced calcium transient triggers delayed calcium overload and neurotoxicity in rat hippocampal neurons. J. Neurosci. 12, 1882-1895.
55. Reeves T. M., Kao C. Q., Phillips L. L., Bullock M. R. and Povlishock J. T. (2000) Presynaptic excitability changes following traumatic brain injury in the rat. J. Neurosci. Res. 60, 370-379.
56. Regan R. F. and Choi D. W. (1994) The effect of NMDA, AMPA/kainate, and calcium channel antagonists on traumatic cortical neuronal injury in culture. Brain Res. 633, 236-242.
57. Royo N. C., Schouten J. W., Fulp C. T., Shimizu S., Marklund N., Graham D. I. and McIntosh T. K. (2003) From cell death to neuronal regeneration: building a new brain after traumatic brain injury. J. Neuropathol. Exp. Neurol. 62, 801-811.
58. Samii A., Badie H., Fu K., Luther R. R. and Hovda D. A. (1999) Effects of an N-type calcium channel antagonist (SNX 111; Ziconotide) on calcium-45 accumulation following fluid-percussion injury. J. Neurotrauma 16, 879-892.
59. Santhakumar V., Ratzliff A. D., Jeng J., Toth Z. and Soltesz I. (2001) Long-term hyperexcitability in the hippocampus after experimental head trauma. Ann. Neurol. 50, 708-717.
60. Santhakumar V., Voipio J., Kaila K. and Soltesz I. (2003) Post-traumatic hyperexcitability is not caused by impaired buffering of extracellular potassium. J. Neurosci. 23, 5865-5876.
61. Sick T. J., Perez-Pinzon M. A. and Feng Z. Z. (1998) Impaired expression of long-term potentiation in hippocampal slices 4 and 48 h following mild fluid-percussion brain injury in vivo. Brain Res. 785, 287-292.
62. Singleton R. H. and Povlishock J. T. (2004) Identification and characterization of heterogeneous neuronal injury and death in regions of diffuse brain injury: evidence for multiple independent injury phenotypes. J. Neurosci. 24, 3543-3553.
63. Singleton R. H., Zhu J., Stone J. R. and Povlishock J. T. (2002) Traumatically induced axotomy adjacent to the soma does not result in acute neuronal death. J. Neurosci. 22, 791-802.
64. Smith D. H., Wolf J. A., Lusardi T. A., Lee V. M. and Meaney D. F. (1999) High tolerance and delayed elastic response of cultured axons to dynamic stretch injury. J. Neurosci. 19, 4263-4269.
65. Sosin D. M., Sniezek J. E. and Waxweiler R. J. (1995) Trends in death associated with traumatic brain injury, 1979 through 1992. Success and failure. JAMA 273, 1778-1780.
66. Sundstrom L., Morrison B. III, Bradley M. and Pringle A. (2005) Organotypic cultures as tools for functional screening in the CNS. Drug Discov. Today 10, 993-1000.
67. Tavalin S. J., Ellis E. F. and Satin L. S. (1995) Mechanical perturbation of cultured cortical neurons reveals a stretch- induced delayed depolarization. J. Neurophysiol. 74, 2767-2773.
68. Tavalin S. J., Ellis E. F. and Satin L. S. (1997) Inhibition of the electrogenic Na pump underlies delayed depolarization of cortical neurons after mechanical injury or glutamate. J. Neurophysiol. 77, 632-638.
69. Toth Z., Hollrigel G. S., Gorcs T. and Soltesz I. (1997) Instantaneous perturbation of dentate interneuronal networks by a pressure wave-transient delivered to the neocortex. J. Neurosci. 17, 8106-8117.
70. Trosseille X., Tarrire C., Lavaste F., Guillon F. and Domont A. (1992) Development of a F.E.M. of the human head according to a specific test protocol. Stapp Car Crash J. 36, 235-253.
71. Wallis R. A. and Panizzon K. L. (1995) Felbamate neuroprotection against CA1 traumatic neuronal injury. Eur. J. Pharmacol. 294, 475-482.
72. Westenbroek R. E., Bausch S. B., Lin R. C., Franck J. E., Noebels J. L. and Catterall W. A. (1998) Upregulation of L-type Ca2 + channels in reactive astrocytes after brain injury, hypomyelination, and ischemia. J. Neurosci. 18, 2321-2334.
73. Wilson S., Raghupathi R., Saatman K. E., MacKinnon M. A., McIntosh T. K. and Graham D. I. (2004) Continued in situ DNA fragmentation of microglia/macrophages in white matter weeks and months after traumatic brain injury J. Neurotrauma 21, 239-250.
74. Winkler T., Sharma H. S., Stalberg E., Badgaiyan R. D., Gordh T. and Westman J. (2003) An L-type calcium channel blocker, nimodipine influences trauma induced spinal cord conduction and axonal injury in the rat. Acta Neurochir. Suppl 86, 425-432.
75. Witgen B. M., Lifshitz J., Smith M. L., Schwarzbach E., Liang S. L., Grady M. S. and Cohen A. S. (2005) Regional hippocampal alteration associated with cognitive deficit following experimental brain injury: a systems, network and cellular evaluation. Neuroscience 133, 1-15.
76. Wolf J. A., Stys P. K., Lusardi T., Meaney D. and Smith D. H. (2001) Traumatic axonal injury induces calcium influx modulated by tetrodotoxin- sensitive sodium channels. J. Neurosci. 21, 1923-1930.
77. Zhang L., Rzigalinski B. A., Ellis E. F. and Satin L. S. (1996) Reduction of voltage-dependent Mg2 + blockade of NMDA current in mechanically injured neurons. Science 274, 1921-1923.
78. Zhang L., Yang K. H. and King A. I. (2001) Biomechanics of neurotrauma. Neurol. Res. 23, 144-156.