Cortical spreading depression increases protein synthesis and upregulates basic fibroblast growth factor

Experimental Neurology

Volumn 158, Issue 1, 1999, Pages 27-36

  Kawahara, Nobutaka ^a   Ruetzler, Christl A ^a   Mies, Günter ^b   Klatzo, Igor ^a  

^a NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^b MAX PLANCK INSTITUTE FOR NEUROLOGICAL RESEARCH   (Germany)

Author keywords

Basic FGF; Cerebral glucose utilization; Cerebral protein synthesis; Cortical spreading depression; Ischemic tolerance

Indexed keywords

BASIC FIBROBLAST GROWTH FACTOR; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUCOSE; POTASSIUM CHLORIDE; SODIUM CHLORIDE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN ISCHEMIA; BRAIN METABOLISM; BRAIN PROTECTION; BRAIN REGION; CELL ACTIVATION; CONTROLLED STUDY; GLIA CELL; GLUCOSE UTILIZATION; HISTOPATHOLOGY; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN INDUCTION; RAT; SPREADING CORTICAL DEPRESSION;

EID: 0032818774     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1006/exnr.1999.7091     Document Type: Article

References (57)

1. Barbe M. F., Tytell M., Gower D. J., Welch W. J. Hyperthermia protects against light damage in the rat retina. Science. 241:1988;1817-1820.
2. Barone F. C., White R. F., Spera P. A., Ellison J., Currie R. W., Wang X., 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.
3. Bonthius D. J., Steward O. Induction of cortical spreading depression with potassium chloride upregulates levels of messenger RNA for glial fibrillary acidic protein in cortex and hippocampus: Inhibition by MK-801. Brain Res. 618:1993;83-94.
4. Bonthius D. J., Stringer J. L., Lothman E. W., Steward O. Spreading depression and reverberatory seizures induce the upregulation of mRNA for glial fibrillary acidic protein. Brain Res. 645:1994;215-224.
5. Chernausek S. D. Insulin-like growth factor-I (IGF-I) production by astroglial cells: Regulation and importance for epidermal growth factor-induced cell replication. J. Neurosci. Res. 34:1993;189-197.
6. Cuevas P., Carceller F., Munoz-Willery I., Gimenez-Gallego G. Intravenous fibroblast growth factor penetrates the blood-brain barrier and protects hippocampal neurons against ischemia-reperfusion injury. Surg. Neurol. 49:1998;77-83.
7. Dietrich W. D., Alonso O., Busto R., Finklestein S. P. Posttreatment with intravenous basic fibroblast growth factor reduces histopathological damage following fluid-percussion brain injury in rats. J. Neurotrauma. 13:1996;309-316.
8. Fernandez-Sanchez M. T., Novelli A. Basic fibroblast growth factor protects cerebellar neurons in primary culture from NMDA and non-NMDA receptor mediated neurotoxicity. FEBS Lett. 335:1993;124-131.
9. Fisher M., Meadows M. E., Do T., Weise J., Trubetskoy V., Charette M., Finklestein S. P. Delayed treatment with intravenous basic fibroblast growth factor reduces infarct size following permanent focal cerebral ischemia in rats. J. Cereb. Blood Flow Metab. 15:1995;953-959.
10. Gehrmann J., Mies G., Bonnekoh P., Banati R., Iijima T., Kreutzberg G. W., Hossmann K. A. Microglial reaction in the rat cerebral cortex induced by cortical spreading depression. Brain Pathol. 3:1993;11-17.
11. Gjedde A., Hansen A. J., Quistorff B. Blood-brain glucose transfer in spreading depression. J. Neurochem. 37:1981;807-812.
12. Glazier S. S., O'Rourke D. M., Graham D. I., Welsh F. A. Induction of ischemic tolerance following brief focal ischemia in rat brain. J. Cereb. Blood Flow Metab. 14:1994;545-553.
13. Gomez-Pinilla F., Lee J. W., Cotman C. W. Basic FGF in adult rat brain: Cellular distribution and response to entorhinal lesion and fimbria-fornix transection. J. Neurosci. 12:1992;345-355.
14. Herdegen T., Sandkühler J., Gass P., Kiessling M., Bravo R., Zimmermann M. JUN, FOS, KROX, and CREB transcription factor proteins in the rat cortex: Basal expression and induction by spreading depression and epileptic seizures. J. Comp. Neurol. 333:1993;271-288.
15. Herrera D. G., Robertson H. A. Application of potassium chloride to the brain surface induces the c-fos proto-oncogene: Reversal by MK-801. Brain Res. 510:1990;166-170.
16. Herrera D. G., Maysinger D., Gadient R., Boeckh C., Otten U., Cuello A. C. Spreading depression induces c-fos like immunoreactivity and NGF mRNA in the rat cerebral cortex. Brain Res. 602:1993;99-103.
17. Kato H., Kogure K. Neuronal damage following non-lethal but repeated cerebral ischemia in the gerbil. Acta Neuropathol. 79:1990;494-500.
18. Kawahara N., Ruetzler C. A., Klatzo I. Protective effect of spreading depression against neuronal damage following cardiac arrest ischemia. Neurol. Res. 17:1995;9-16.
19. Kawahara N., Croll S. D., Wiegand S. J., Klatzo I. Cortical spreading depression induces long-term alterations of BDNF levels in cortex and hippocampus distinct from lesion effects: Implications for ischemic tolerance. Neurosci. Res. 29:1997;37-47.
20. Kirino T., Tsujita Y., Tamura A. Induced tolerance to ischemia in gerbil hippocampal neurons. J. Cereb. Blood Flow Metab. 11:1991;299-307.
21. Kitagawa K., Matsumoto M., Tagaya M., Hata R., Ueda H., Niinobe N., Handa N., Fukunaga R., Kimura K., Mikoshiba K., Kamada T. 'Ischemic tolerance' phenomenon found in the brain. Brain Res. 528:1990;21-24.
22. Kobayashi S., Harris V. A., Welsh F. A. Spreading depression induces tolerance of cortical neurons to ischemia in rat brain. J. Cereb. Blood Flow Metab. 15:1995;721-727.
23. Kocher M. Metabolic and hemodynamic activation of postischemic rat brain by cortical spreading depression. J. Cereb. Blood Flow Metab. 10:1990;564-571.
24. Koketsu N., Berlove D. J., Moskowitz M. A., Kowall N. W., Caday C. G., Finklestein S. P. Pretreatment with intraventricular basic fibroblast growth factor decreases infarct size following focal cerebral ischemia in rats. Ann. Neurol. 35:1994;451-457.
25. Kraig R. P., Dong L., Thisted R., Jaeger C. B. Spreading depression increases immunohistochemical staining of glial fibrillary acidic protein. J. Neurosci. 11:1991;2187-2198.
26. Langeveld C. H., Jongenelen C. A., Schepens E., Stoof J. C., Bast A., Drukarch B. Cultured rat striatal and cortical astrocytes protect mesencephalic dopaminergic neurons against hydrogen peroxide toxicity independent of their effect on neuronal development. Neurosci. Lett. 192:1995;13-16.
27. Leão A. A. P. Spreading depression of activity in the cerebral cortex. J. Neurophysiol. 7:1944;359-390.
28. Lippoldt A., Andbjer B., Rosen L., Richter E., Ganten D., Cao Y., Pettersson R. F., Fuxe K. Photochemically induced focal cerebral ischemia in rat: time dependent and global increase in expression of basic fibroblast growth factor mRNA. Brain Res. 625:1993;45-56.
29. Liu H. M., Chen H. H. Correlation between fibroblast growth factor expression and cell proliferation in experimental brain infarct: Studied with proliferating cell nuclear antigen immunohistochemistry. J. Neuropathol. Exp. Neurol. 53:1994;118-126.
30. Liu Y., Kato H., Nakata N., Kogure K. Protection of rat hippocampus against ischemic neuronal damage by pretreatment with sublethal ischemia. Brain Res. 586:1992;121-124.
31. Logan A., Frautschy S. A., Gonzalez A. M., Baird A. A time course for the focal elevation of synthesis of basic fibroblast growth factor and one of its high-affinity receptors (flg) following a localized cortical brain injury. J. Neurosci. 12:1992;3828-3837.
32. Louis J. C., Magal E., Gerdes W., Seifert W. Survival-promoting and protein kinase C-regulating roles of basic FGF for hippocampal neurons exposed to phorbol ester, glutamate and ischaemia-like conditions. Eur. J. Neurosci. 5:1993;1610-1621.
33. Lowenstein D. H., Chan P. H., Miles M. F. The stress protein response in cultured neurons: Characterization and evidence for a protective role in excitotoxicity. Neuron. 7:1991;1053-1060.
34. Maiese K., Boniece I., DeMeo D., Wagner W. A. Peptide growth factors protect against ischemia in culture by preventing nitric oxide toxicity. J. Neurosci. 13:1993;3034-3040.
35. Matsushima K., Hogan M. J., Hakim A. M. Cortical spreading depression protects against subsequent focal cerebral ischemia in rats. J. Cereb. Blood Flow Metab. 16:1996;221-226.
36. Mies G., Paschen W. Regional changes of blood flow, glucose, and ATP content determined on brain sections during a single passage of spreading depression in rat brain cortex. Exp. Neurol. 84:1984;249-258.
37. Mies G., Bodsch W., Paschen W., Hossmann K. A. Triple-tracer autoradiography of cerebral blood flow, glucose utilization, and protein synthesis in rat brain. J. Cereb. Blood Flow Metab. 6:1986;59-70.
38. Mies G. Inhibition of protein synthesis during repetitive cortical spreading depression. J. Neurochem. 60:1993;360-363.
39. Moskowitz M. A., Nozaki K., Kraig R. P. Neocortical spreading depression provokes the expression of c-fos protein-like immunoreactivity within trigeminal nucleus caudalis via trigeminovascular mechanisms. J. Neurosci. 13:1993;1167-1177.
40. Mraovitch S., Calando Y., Goadsby P. J., Seylaz J. Subcortical cerebral blood flow and metabolic changes elicited by cortical spreading depression in rat. Cephalalgia. 12:1992;137-141.
41. Nakano S., Kato H., Kogure K. Neuronal damage in the rat hippocampus in a new model of repeated reversible transient cerebral ischemia. Brain Res. 490:1989;178-180.
42. Nedergaard M., Hansen A. J. Spreading depression is not associated with neuronal injury in the normal brain. Brain Res. 449:1988;395-398.
43. Nowak T. S. Jr., Osborne O. C., Mies G. Cortical spreading depression induces the proto-oncogene, c-fos, but not the stress protein, HSP 70. J. Cereb. Blood Flow Metab. (Suppl.). 11:1991;S215.
44. Nozaki K., Finklestein S. P., Beal M. F. Basic fibroblast growth factor protects against hypoxia-ischemia and NMDA neurotoxicity in neonatal rats. J. Cereb. Blood Flow Metab. 13:1993;221-228.
45. Pappius H. M. Local cerebral glucose utilization in thermally traumatized rat brain. Ann. Neurol. 9:1981;484-491.
46. Pellegrino L. J., Pellegrino A., Cushman A. J. A Stereotaxic Atlas of the Rat Brain. 1979;Plenum Press, New York/London.
47. Rudge J. S., Morrissey D., Lindsay R. M., Pasnikowski E. M. Regulation of ciliary neurotrophic factor in cultured rat hippocampal astrocytes. Eur. J. Neurosci. 6:1994;218-229.
48. Sermet E., Gregoire M. C., Galy G., Lavenne F., Pierre C., Veyre L., Lebars D., Cinotti L., Comar D., Dalery J., Bobillier P. Paradoxical metabolic response of the human brain to a single electroconvulsive shock. Neurosci. Lett. 254:1998;41-44.
49. Shimojo M., Nakajima K., Takei N., Hamanoue M., Kohsaka S. Production of basic fibroblast growth factor in cultured rat brain microglia. Neurosci. Lett. 123:1991;229-231.
50. Shinohara M., Dollinger B., Brown G., Rapaport S., Sokoloff L. Cerebral glucose utilization: Local changes during and after recovery from spreading cortical depression. Science. 203:1979;188-190.
51. Smith C. B., Crane A. M., Kadekaro M., Agranoff B. W., Sokoloff L. Stimulation of protein synthesis and glucose utilization in the hypoglossal nucleus induced by axotomy. J. Neurosci. 4:1984;2489-2496.
52. Smith C. B., Deibler G. E., Eng N., Schmidt K., Sokoloff L. Measurement of local cerebral protein synthesis in vivo: Influence of recycling of amino acids derived from protein degradation. Proc. Natl. Acad. Sci. USA. 85:1988;9341-9345.
53. 14C]deoxyglucose method for the measurement of local cerebral glucose utilization: Theory, procedure, and normal values in the conscious and anesthetized albino rat. J. Neurochem. 28:1977;897-916.
54. Tanaka R., Miyasaka Y., Yada K., Ohwada T., Kameya T. Basic fibroblast growth factor increases regional cerebral blood flow and reduces infarct size after experimental ischemia in a rat model. Stroke. 26:1995;2154-2158.
55. Van Der Wal E. A., Gomez-Pinilla F., Cotman C. W. Seizure-associated induction of basic fibroblast growth factor and its receptor in the rat brain. Neuroscience. 60:1994;311-323.
56. Vibulsreth S., Hefti F., Ginsberg M. D., Dietrich W. D., Busto R. Astrocytes protect cultured neurons from degeneration induced by anoxia. Brain Res. 422:1987;303-311.
57. Xie Y., Mies G., Hossmann K. A. Ischemic threshold of brain protein synthesis after unilateral carotid artery occlusion in gerbils. Stroke. 20:1989;620-626.