Astrocytes are the major source of nerve growth factor upregulation following traumatic brain injury in the rat

Experimental Neurology

Volumn 149, Issue 2, 1998, Pages 301-309

  Goss, James R ^a   O'Malley, Mark E ^a   Zou, Lanling ^a   Styren, Scot D ^a   Kochanek, Patrick M ^a   Dekosky, Steven T ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

Astrocyte; Hippocampus; Hypothermia; In situ hybridization; Nerve growth factor; Traumatic brain injury

Indexed keywords

GLIAL FIBRILLARY ACIDIC PROTEIN; NERVE GROWTH FACTOR; RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; ASTROCYTE; BRAIN INJURY; HEAD INJURY; HIPPOCAMPUS; HYPOTHERMIA; HYPOTHESIS; IMMUNOCYTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; NONHUMAN; NORTHERN BLOTTING; PRIORITY JOURNAL; PROTEIN ANALYSIS; RAT; RECEPTOR UPREGULATION;

EID: 0032005523     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1006/exnr.1997.6712     Document Type: Article

References (56)

1. Arendt T., Bruckner M. K., Krell T., Pagliusi S., Kruska L., Heumann R. Degeneration of rat cholinergic basal forebrain neurons and reactive changes in nerve growth factor expression after chronic neurotoxic injury. II. Reactive expression of the nerve growth factor gene in astrocytes. Neuroscience. 65:1995;647-659.
2. Awatsuji H., Furukawa Y., Hirota M., Murakami Y., Nii S., Furukawa S., Hayashi K. Interleukin-4 and interleukin-5 as modulators of nerve growth factor synthesis/secretion in astrocytes. J. Neurosci. Res. 34:1993;539-545.
3. Bakhit C., Armanini M., Bennett G. L., Wong W. L. T., Hansen S. E., Taylor R. Increase in glia-derived nerve growth factor following destruction of hippocampal neurons. Brain Res. 560:1991;76-83.
4. Ballarin M., Ernfors P., Linderfors N., Persson H. Hippocampal damage and kainic acid injection induce a rapid increase in mRNA for BDNF and NGF in the rat brain. Exp. Neurol. 114:1991;35-43.
5. Brodie C. Platelet activating factor induces nerve growth factor production by rat astrocytes. Neurosci. Lett. 186:1995;5-8.
6. Carman-Krzan M., Wise B. C. Arachidonic acid lipoxygenation may mediate interleukin-1 stimulation of nerve growth factor secretion in astroglial cultures. J. Neurosci. Res. 34:1993;225-232.
7. Dekosky S. T., Goss J. R., Miller P. D., Styren S. D., Kochanek P. M., Marion D. Upregulation of nerve growth factor following cortical trauma. Exp. Neurol. 130:1994;173-177.
8. Dekosky S. T., Styren S. D., O'Malley M. E., Goss J. R., Kochanek P. M., Evans C. H., Robbins P. D., Marion D. W. Interleukin-1 receptor antagonist suppresses neurotrophin response in injured rat brain. Ann. Neurol. 39:1996;123-127.
9. Dreyfus C. F. Effects of nerve growth factor on cholinergic brain neurons. Trends Pharmacol. Sci. 10:1989;145-149.
10. Eng L. F. Glial fibrillary acidic protein (GFAP): The major protein of glial intermediate filaments in differentiated astrocytes. J. Neuroimmunol. 8:1985;203-214.
11. Frederickson R. C. A., Silver J. Glial cells, the unsung heroes of the brain. Biotechnology. 9:1991;1-4.
12. Gage F. H., Olejniczak P., Armstrong D. M. Astrocytes are important for sprouting in the septohippocampal circuit. Exp. Neurol. 102:1988;2-13.
13. Gall C., Murray K., Isackson P. J. Kainic acid-induced seizures stimulate increased expression of nerve growth factor mRNA in rat hippocampus. Mol. Brain Res. 9:1991;113-123.
14. Gall C. M., Isackson J. P. Limbic seizures increase neuronal production of messenger RNA for nerve growth factor. Science. 245:1989;758-761.
15. Gomez-Pinilla F., Lee J. W.-K., 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.
16. Goss J. R., Morgan D. G. Enhanced glial fibrillary acidic protein RNA response to fornix transection in aged mice. J. Neurochem. 64:1995;1351-1360.
17. Goss J. R., Styren S. D., Miller P. D., Kochanek P. M., Palmer A. M., Marion D. W., Dekosky S. T. Hypothermia attenuates the normal increase in interleukin-1B RNA and nerve growth factor following traumatic brain injury in the rat. J. Neurotrauma. 12:1995;159-167.
18. Goss J. R., Taffe K. M., Kochanek M. D., Dekosky S. T. The antioxidant enzymes glutathione peroxidase and catalase increase following traumatic brain injury in the rat. Exp. Neurol. 146:1997;291-294.
19. Guthrie K. M., Nguyen T., Gall C. M. Insulin-like growth factor-1 mRNA increased in deafferented hippocampus: Spatiotemporal correspondence of a trophic event with axon sprouting. J. Comp. Neurol. 352:1995;147-160.
20. Hahn M., Lorez H., Fisher G. The immortalized astroglial cell line RC7 is a new model system for the study of nerve growth factor (NGF) regulation: Stimulation of interleukin-1 beta and transforming growth factor-beta 1 is additive and affected differently by dibutryryl cyclic AMP. Glia. 10:1994;286-295.
21. Hengerer B., Lindholm D., Heumann R., Ruther U., Wagner E. F., Thoenen H. Lesion-induced increase in nerve growth factor mRNA is mediated by c-fos. Proc. Natl. Acad. Sci. USA. 87:1990;3899-3903.
22. 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.
23. Hoff S. F., Scheff S. W., Benardo L. S., Cotman C. W. Lesion-induced synaptogenesis in the dentate gyrus of aged rats. I. Loss and reacquisition of normal synaptic density. J. Comp. Neurol. 205:1982;246-252.
24. Isackson J. P., Huntsman M., Marray K. D., Gall C. M. BDNF mRNA expression is increased in adult forebrain after limbic seizures: Temporal patterns of induction distinct from NGF. Neuron. 6:1991;937-948.
25. Kesslak J. P., Nieto-Sampedro M., Globus J., Cotman C. W. Transplants of purified astrocytes promote behavioral recovery after frontal cortex ablation. Exp. Neurol. 93:1986;377-390.
26. Landfield P. W., Rose G., Sandles L., Wohlstadter T. C., Lynch G. Patterns of astroglial hypertrophy and neuronal degeneration in the hippocampus of aged, memory-deficient rats. J. Gerontol. 32:1977;3-12.
27. Levi-Montalcini R. The nerve growth factor 35 years later. Science. 237:1987;1154-1161.
28. Lighthall J. W. Controlled cortical impact: A new experimental brain injury model. J. Neurotrauma. 5:1988;1-15.
29. Lindsay R. M., Barber P. C., Sherwood M. R. C., Zimmer J., Raisman G. Astrocyte cultures from adult rat brain: Derivation, characterization, and neurotrophic properties of pure astroglial cells from corpus collosum. Brain Res. 243:1982;329-343.
30. Lindvall O., Ernfors P., Bengzon J., Kokaia Z., Smith M. L., Siesjo B. K., Persson H. Differential regulation of messenger RNAs for nerve growth factor, brain-derived neurotrophic factor, and neurotrophin-3 in the adult rat brain following cerebral ischemia and hypoglycemic coma. Proc. Natl. Acad. Sci. USA. 89:1992;648-652.
31. Liuzzi F., Lasek R. J. Astrocytes block axonal regeneration in mammals by activating the physiological stop pathway. Science. 237:1987;642-645.
32. Liuzzi F. J. Proteolysis is a critical step in the physiological stop pathway: Mechanisms involved in the blockade of axonal regeneration by mammalian astrocytes. Brain Res. 512:1990;277-283.
33. Mattson M. P., Scheff S. W. Endogenous neuroprotection factors and traumatic brain injury: Mechanisms of action and implications for therapy. J. Neurotrauma. 11:1994;3-33.
34. McKeon R. J., Schreiber R. C., Rudge J. S., Silver J. Reduction of neurite outgrowth in a model of glial scarring following CNS injury is correlated with the expression of inhibitory molecules on reactive astrocytes. J. Neurosci. 11:1991;3398-3411.
35. Mocchetti I., Bernardi M. A., Szekely A. M., Alho H., Brooker G., Costa E. Regulation of nerve growth factor biosynthesis by b-adrenergic receptor activation in astrocytoma cells: A potential role of c-Fos protein. Proc. Natl. Acad. Sci. USA. 86:1989;3891-3895.
36. Nieto-Sampedro M., Berman M. A. Interleukin 1-like activity in rat brain: Sources, targets, and effect of injury. J. Neurosci. Res. 17:1987;214-219.
37. Nisho T., Furukawa S., Akiguchi I., Oka N., Ohnishi K., Tomimoto H., Nakamura S., Kimura J. Cellular localization of nerve growth factor-like immunoreactivity in adult rat brain: Quantitative and immunohistochemical study. Neuroscience. 1:1994;67-84.
38. Oderfeld-Nowak B., Bacia A., Gradkowska M., Fusco M., Vantini G., Leon A., Aloe L. In vivo activated brain astrocytes may produce and secrete nerve growth factor-like molecules. Neurochem. Int. 21:1992;455-461.
39. Pan Z., Perez-Polo R. Role of nerve growth factor in oxidant homeostasis: Glutathione metabolism. J. Neurochem. 61:1993;1713-1721.
40. Politis M. J., Miller J. E. The roles of reactive gliosis and mitosis on tropic factor production in traumatized nervous system tissue. Brain Res. 346:1985;186-189.
41. Pshenichkin S. P., Szekely A. M., Wise B. C. Transcriptional and postranscriptional mechanisms involved in the interleukin-1, steroid, and protein kinase C regulation of nerve growth factor in cortical astrocytes. J. Neurochem. 63:1994;419-428.
42. Pshenichkin S. P., Wise B. C. Okadaic acid increases nerve growth factor secretion, mRNA stability, and gene transcription in primary cultures of cortical astrocytes. J. Biol. Chem. 270:1995;5994-5999.
43. Rocamora N., Palacios J. M., Mengod G. Limbic seizures induce a differential regulation of the expression of nerve growth factor, brain-derived neurotrophic factor and neurotrophin-3, in the rat hippocampus. Mol. Brain Res. 13:1992;27-33.
44. Rudge J. S., Smith G. M., Silver J. An in vitro model of wound healing in the CNS: Analysis of cell reaction and interaction at different ages. Exp. Neurol. 103:1989;1-16.
45. Schwartz J. P., Nishiyama N. Neurotrophic factor gene expression in astrocytes during development and following injury. Brain Res. Bull. 35:1994;403-407.
46. Strauss S., Otten U., Joggerst B., Pluss K., Volk B. Increased levels of nerve growth factor (NGF) protein and mRNA and reactive gliosis following kainic acid injection into the rat striatum. Neurosci. Lett. 168:1994;193-196.
47. Timmusk T., Palm K., Metsis M., Saarma M., Persson H. Multiple promoters direct tissue-specific and seizure-induced expression of the rat BDNF gene. Soc. Neurosci. Abstr. 18:1992;387.2.
48. Vige X., Costa E., Wise B. C. Mechanism of nerve growth factor mRNA regulation by interleukin-1 and basic fibroblast growth factor in primary cultures of rat astrocytes. Mol. Pharmacol. 40:1991;186-192.
49. Vige X., Tang B., Wise B. C. Cortical neurons inhibit basal and interleukin-1-stimulated astroglial cell secretion of nerve growth factor. Brain Res. 591:1992;345-350.
50. Whittemore S. R., Friedman P. L., Larhammar D., Persson H., Gonzalez-Garvajal M., Holets V. R. Rat B-nerve growth factor sequence and site of synthesis in the adult hippocampus. J. Neurosci. Res. 20:1988;403-410.
51. Whittemore S. R., Larkfors L., Ebendal T., Holets V. R., Ericsson A., Persson H. Increased B-nerve growth factor messenger RNA and protein levels in neonatal rat hippocampus following specific cholinergic lesions. J. Neurosci. 7:1987;247-251.
52. Whittemore S. R., Seiger A. The expression, localization and functional significance of B-nerve growth factor in the central nervous system. Brain Res. Rev. 12:1987;429-464.
53. Yang K., Mu X. S., Xue J. J., Perez-Polo J. R., Hayes R. L. Regional and temporal profiles of c-fos and nerve growth factor mRNA expression in rat brain after lateral cortical impact injury. J. Neurosci. Res. 42:1995;571-578.
54. Zheng M., Heinrich G. Structural and functional analysis of the promoter region of the nerve growth factor gene. Mol. Brain Res. 3:1988;133-140.
55. Bruce A. J., Baudry M. Oxygen free radicals in rat limbic structures after kainate-induced seizures. Free Rad. Biol. & Med. 18:1995;993-1002.
56. DeKosky S. T., Miller P. O., Styren S. D., O'Malley M., Marion D. Interleukin-1β elevation in CSF following head injury in humans is attenuated by hypothermia. J. Neurotrauma. 11:1994;106.