Differential hippocampal protection when blocking intracellular sodium and calcium entry during traumatic brain injury in rats

Journal of Neurotrauma

Volumn 25, Issue 10, 2008, Pages 1195-1205

  Zhao, Xueren ^a   Gorin, Fredric A ^b   Berman, Robert F ^a   Lyeth, Bruce G ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Astrocyte; Glia; Hippocampus; Ion exchangers; Lateral fluid percussion injury; Neuronal degeneration; Sodium; Traumatic brain injury

Indexed keywords

2 [2 [4 (4 NITROBENZYLOXY)PHENYL]ETHYL]ISOTHIOUREA METHANESULFONATE; 5 (N ETHYL N ISOPROPYL)AMILORIDE; A 3805; A 7410; ACID SENSING ION CHANNEL; ACID SENSING ION CHANNEL TYPE 1A; AMILORIDE; CALCIUM; CALCIUM CHANNEL; GLIAL FIBRILLARY ACIDIC PROTEIN; SODIUM; SODIUM CALCIUM EXCHANGE PROTEIN; SODIUM PROTON EXCHANGE PROTEIN 1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ASTROCYTE; CALCIUM CELL LEVEL; CELL PROTECTION; CEREBROSPINAL FLUID; CONFERENCE PAPER; CONTROLLED STUDY; DRUG DOSE REDUCTION; DRUG INHIBITION; GLIA CELL; HIPPOCAMPUS; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; IMMUNOLOCALIZATION; IMMUNOREACTIVITY; ION TRANSPORT; MALE; NERVE CELL; NERVE DEGENERATION; NEUROPATHOLOGY; NEUROPROTECTION; NONHUMAN; PATHOLOGY; PERCUSSION; PROTEIN ANALYSIS; RAT; SODIUM CALCIUM EXCHANGE; SODIUM CELL LEVEL; STEREOMETRY; TRAUMATIC BRAIN INJURY; TREATMENT DURATION; TREATMENT OUTCOME;

ANIMALS; ASTROCYTES; BIOLOGICAL MARKERS; BRAIN INJURIES; CALCIUM CHANNEL BLOCKERS; CALCIUM CHANNELS; DISEASE MODELS, ANIMAL; GLIAL FIBRILLARY ACIDIC PROTEIN; GLIOSIS; HIPPOCAMPUS; INJECTIONS, INTRAVENTRICULAR; MALE; NERVE TISSUE PROTEINS; NEURONS; NEUROPROTECTIVE AGENTS; RATS; RATS, SPRAGUE-DAWLEY; SODIUM CHANNEL BLOCKERS; SODIUM CHANNELS; SODIUM-HYDROGEN ANTIPORTER;

EID: 55549130488     PISSN: 08977151     EISSN: None     Source Type: Journal    
DOI: 10.1089/neu.2008.0635     Document Type: Conference Paper

References (63)

1. Alexander, S.P., Mathie, A., and Peters, J.A. (2008). Guide to Receptors and Channels (GRAC), 3rd edition. Br. J. Pharmacol. 153, Suppl 2, S1-S209.
2. Andreeva, N., Khodorov, B., Stelmashook, E., Sokolova, S., Cragoe, E., Jr., and Victorov, I. (1992). 5-(N-ethyl-N-isopropyl) amiloride and mild acidosis protect cultured cerebellar granule cells against glutamate-induced delayed neuronal death. Neuroscience 49, 175-181.
3. Bakay, L., Lee, J.C., Lee, G.C., and Peng, J.R. (1977). Experimental cerebral concussion. Part 1: An electron microscopic study. J. Neurosurg. 47, 525-531.
4. Bernardinelli, Y., Azarias, G., and Chatton, J.Y. (2006). In situ fluorescence imaging of glutamate-evoked mitochondrial Na responses in astrocytes. Glia 54, 460-470.
5. Bondarenko, A., and Chesler, M. (2001). Calcium dependence of rapid astrocyte death induced by transient hypoxia, acidosis, and extracellular ion shifts. Glia 34, 143-149.
6. Breder, J., Sabelhaus, C.F., Opitz, T., Reymann, K.G., and Schroder, U.H. (2000). Inhibition of different pathways influencing Na homeostasis protects organotypic hippocampal slice cultures from hypoxic/hypoglycemic injury. Neuropharmacology 39, 1779-1787.
7. + uniporters and exchangers. J. Bioenerg. Biomembr. 26, 519-526.
8. Bullock, R., Maxwell, W.L., Graham, D.I., Teasdale, G.M., and Adams, J.H. (1991). Glial swelling following human cerebral contusion: an ultrastructural study. J. Neurol. Neurosurg. Psychiatry 54, 427-434.
9. Castejon, O.J. (1998). Morphological astrocytic changes in complicated human brain trauma. A light and electron microscopic study. Brain Inj. 12, 409-427.
10. + exchange blockers. J. Mol. Cell Cardiol. 32, 1181-1192.
11. Cho, J.H., and Askwith, C.C. (2008). Presynaptic release probability is increased in hippocampal neurons from ASIC1 knockout mice. J. Neurophysiol. 99, 426-441.
12. Danbolt, N.C. (1994). The high affinity uptake system for excitatory amino acids in the brain. Prog. Neurobiol. 44, 377-396.
13. Danbolt, N.C. (2001). Glutamate uptake. Prog. Neurobiol. 65, 1-105.
14. Dixon, C.E., Lyeth, B.G., Povlishock, J.T., Findling, R.L., Hamm, R.J., Marmarou, A., Young, H.F., and Hayes, R.L. (1987). A fluid percussion model of experimental brain injury in the rat. J. Neurosurg. 67, 110-119.
15. 2+ in primary rat astrocytes. Glia 2, 397-402.
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. + exchange in cortical astrocytes. Glia 51, 35-46.
18. Floyd, C.L., and Lyeth, B.G. (2007). Astroglia: important mediators of traumatic brain injury, in: J.T. Weber, A.I. R. Maas, Eds., Neurotrauma: New Insights into Pathology and Treatment. Progress in Brain Research, Vol. 161. Elsevier: Amsterdam, pps. 61-79.
19. Globus, M.Y.T., Alonso, O., Dietrich, W.D., Busto, R., and Ginsberg, M.D. (1995). Glutamate release and free radical production following brain injury: effects of posttraumatic hypothermia. J. Neurochem. 65, 1704-1711.
20. + exchanger. J. Membr. Biol. 90, 1-12.
21. Gundersen, H.J. (1986). Stereology of arbitrary particles. A review of unbiased number and size estimators and the presentation of some new ones, in memory of William R. Thompson. J. Microsc. 143, 3-45.
22. Hallam, T.M., Floyd, C.L., Folkerts, M.M., Lee, L.L., Gong, Q.Z., Lyeth, B.G., Muizelaar, J.P., and Berman, R.F. (2004). Comparison of behavioral deficits and acute neuronal degeneration in rat lateral fluid percussion and weight-drop brain injury models. J. Neurotrauma 21, 521-539.
23. Jenkins, L.W., Becker, D.P., and Coburn, T.H. (1984). A quantitative analysis of glial swelling and ischemic neuronal injury following cerebral ischemia, in: T.G. Go, A. Baethmann, Eds., Recent Progress in the Study and Therapy of Brain Edema. Plenum Press: New York, pps. 523-537.
24. Katayama, Y., Becker, D.P., Tamura, T., and Hovda, D.A. (1990). Massive increases in extracellular potassium and the indiscriminate release of glutamate following concussive brain injury. J. Neurosurg. 73, 889-900.
25. Kempski, O., Staub, F., Jansen, M., and Baethmann, A. (1990). Molecular mechanisms of glial cell swelling in acidosis. Adv. Neurol. 52, 39-45.
26. Kimelberg, H.K. (1992). Astrocytic edema in CNS trauma. J. Neurotrauma 9, S71-S81.
27. Kimelberg, H.K., Jalonen, T., and Walz, W. (1992). Regulation of the brain microenvironment: transmitter and ions, in: S. Murphy, Ed., Astrocytes: Pharmacology and Function. Academic Press: Orlando, FL.
28. Kleyman, T.R., and Cragoe, E.J., Jr. (1988). Amiloride and its analogs as tools in the study of ion transport. J. Membr. Biol. 105, 1-21.
29. Liu, D., Smith, C.L., Barone, F.C., Ellison, J.A., Lysko, P.G., Li, K., and Simpson, I.A. (1999). Astrocytic demise precedes delayed neuronal death in focal ischemic rat brain. Brain Res. Mol. Brain Res. 68, 29-41.
30. MacGregor, D.G., Avshalumov, M.V., and Rice, M.E. (2003). Brain edema induced by in vitro ischemia: causal factors and neuroprotection. J. Neurochem. 85, 1402-1411.
31. Magistretti, P.J., and Pellerin, L. (1996). Cellular bases of brain energy metabolism and their relevance to functional brain imaging: evidence for a prominent role of astrocytes. Cereb. Cortex 6, 50-61.
32. Marmarou, A. (1992). Intracellular acidosis in human and experimental brain injury. J. Neurotrauma. 9, Suppl 2, S551-s562.
33. 31P nuclear magnetic resonance. J. Neurochem. 49, 1530-1540.
34. McIntosh, T.K., Vink, R., Noble, L., Yamakami, I., Fernyak, S., Soares, H., and Faden, A.I. (1989). Traumatic brain injury in the rat: characterization of a lateral fluid-percussion model. Neuroscience 28, 233-244.
35. Myer, D.J., Gurkoff, G.G., Lee, S.M., Hovda, D.A., and Sofroniew, M.V. (2006). Essential protective roles of reactive astrocytes in traumatic brain injury. Brain 129, 2761-2772.
36. Nelson, L.R., Auen, E.L., and Bourke, R.S. (1982). A comparison of animal head injury models developed for treatment modality evaluation, in: R. Grossman, G.P.L., Eds., Head Injury: Basic and Clinical Aspects. Raven Press: New York, pps. 117-127.
37. Noble, L.J., Hall, J.J., Chen, S., and Chan, P.H. (1992). Morphologic changes in cultured astrocytes after exposure to glutamate. J. Neurotrauma 9, 255-267.
38. Ouyang, Y.B., Voloboueva, L.A., Xu, L.J., and Giffard, R.G. (2007). Selective dysfunction of hippocampal CA1 astrocytes contributes to delayed neuronal damage after transient forebrain ischemia. J. Neurosci. 27, 4253-4260.
39. Pellerin, L., and Magistretti, P.J. (1994). Glutamate uptake into astrocytes stimulates aerobic glycolysis: a mechanism coupling neuronal activity to glucose utilization. Proc. Natl. Acad. Sci. USA 91, 10625-10629.
40. Petito, C.K., Olarte, J.P., Roberts, B., Nowak, T.S., Jr., and Pulsinelli, W.A. (1998). Selective glial vulnerability following transient global ischemia in rat brain. J. Neuropathol. Exp. Neurol. 57, 231-238.
41. + exchange inhibitor, protects gerbil hippocampal neurons from ischemic injury. Brain Res. 839, 199-202.
42. + exchange. Brain Res. 812, 297-300.
43. + exchange by 5-(N-ethyl-N-isopropyl)-amiloride reduces free fatty acid efflux from the ischemic reperfused rat cerebral cortex. Brain Res. 884, 155-162.
44. Pignataro, G., Simon, R.P., and Xiong, Z.G. (2007). Prolonged activation of ASIC1a and the time window for neuroprotection in cerebral ischaemia. Brain 130, 151-158.
45. + exchange by KB-R7943, a novel selective antagonist, attenuates phosphoethanolamine and free fatty acid efflux in rat cerebral cortex during ischemia-reperfusion injury. Brain Res. 916, 192-198.
46. + exchange by SM-20220 attenuates free fatty acid efflux in rat cerebral cortex during ischemia-reperfusion injury. Brain Res. 913, 156-158.
47. Rogister, F., Laeckmann, D., Plasman, P., Van Eylen, F., Ghyoot, M., Maggetto, C., Liegeois, J., Geczy, J., Herchuelz, A., Delarge, J., and Masereel, B. (2001). Novel inhibitors of the sodium-calcium exchanger: benzene ring analogues of N-guanidino substituted amiloride derivatives. Eur. J. Med. Chem. 36, 597-614.
48. Schmued, L.C., Albertson, C., and Slikker, W.J. (1997). Fluoro-Jade: a novel fluorochrome for the sensitive and reliable histochemical localization of neuronal degeneration. Brain Res. 751, 37-46.
49. Schmued, L.C., and Hopkins, K.J. (2000). Fluoro-Jade: novel fluorochromes for detecting toxicant-induced neuronal degeneration. Toxicol. Pathol. 28, 91-99.
50. + exchange inhibitor KB-R7943 protects CA1 neurons in rat hippocampal slices against hypoxic/ hypoglycemic injury. Neuropharmacology 38, 319-321.
51. 2+ exchange in membrane vesicle and papillary muscle preparations from guinea pig heart by analogs of amiloride. Proc. Natl. Acad. Sci. USA 81, 3238-3242.
52. Silver, I.A., Deas, J., and Erecinska, M. (1997). Ion homeostasis in brain cells: differences in intracellular ion responses to energy limitation between cultured neurons and glial cells. Neuroscience 78, 589-601.
53. + ATPase in mammalian astrocytes. Glia 21, 35-45.
54. Sterio, D.C. (1984). The unbiased estimation of number and sizes of arbitrary particles using the disector. J. Microsc. 134, 127-136.
55. Takahashi, M., Billups, B., Rossi, D., Sarantis, M., Hamann, M., and Attwell, D. (1997). The role of glutamate transporters in glutamate homeostasis in the brain. J. Exp. Biol. 200, 401-409.
56. + exchange system in various cell types. Biochem. Biophys. Res. Commun. 116, 86-90.
57. 31P magnetic resonance spectroscopy study. J. Cereb. Blood Flow Metab. 7, 563-571.
58. + exchanger NHE-1 in the basolateral membrane. Hearing Res. 94, 94-106.
59. Wemmie, J.A., Price, M.P., and Welsh, M.J. (2006). Acid-sensing ion channels: advances, questions and therapeutic opportunities. Trends Neurosci. 29, 578-586.
60. West, M.J., Slomianka, L., and Gundersen, H.J. (1991). Unbiased stereological estimation of the total number of neurons in the-subdivisions of the rat hippocampus using the optical fractionator. Anat. Rec. 231, 482-497.
61. Xiong, Z.G., Zhu, X.M., Chu, X.P., Minami, M., Hey, J., Wei, W.L., MacDonald, J.F., Wemmie, J.A., Price, M.P., Welsh, M.J., and Simon, R.P. (2004). Neuroprotection in ischemia: blocking calcium-permeable acid-sensing ion channels. Cell 118, 687-698.
62. Zhao, X., Ahram, A., Berman, R.F., Muizelaar, J.P., and Lyeth, B.G. (2003). Early loss of astrocytes after experimental traumatic brain injury. Glia 44, 140-152.
63. Zhong, C., Zhao, X., Van, K.C., Bzdega, T., Smyth, A., Zhou, J., Kozikowski, A.P., Jiang, J., O'Connor, W.T., Berman, R.F., Neale, J.H., and Lyeth, B.G. (2006). NAAG peptidase inhibitor increases dialysate NAAG and reduces glutamate, aspartate and GABA levels in the dorsal hippocampus following fluid percussion injury in the rat. J. Neurochem. 97, 1015-1025.