Abstract
We have found a regional distribution of IL 1 beta mRNA and IL 1 activity in the normal adult rat brain, which reveals at least partially a colocalization with nerve growth factor (NGF). The predominantly neuronal signal patterns were found over the granule cells of the dentate gyrus, the pyramidal cells of the hippocampus, the granule cells of the cerebellum, the granule and periglomerular cells of the olfactory bulb, and over dispersed cells of the ventromedial hypothalamus and of the frontal cortex. In these areas also the highest levels of IL 1 activity were observed. In the striatum and septum much lower levels of IL 1 beta mRNA and IL 1 activity (shown for the striatum), most likely synthesized by glial cells, could be determined. IL 1 beta-expressing cells were mainly found in brain regions that also synthesize NGF mRNA as shown by in situ hybridization. NGF mRNA could be demonstrated over pyramidal cells of the hippocampus, granule cells of the dentate gyrus, periglomerular cells of the olfactory bulb and over prefrontal cortex neurons. These data indicate that IL 1 beta, among other factors, might also play a regulatory role in the synthesis of NGF in the CNS, as has been demonstrated in the peripheral nervous system (Lindholm, D., R. Heumann, M. Meyer, and H. Thoenen. 1987. Nature (Lond.). 330:658-659).
Full Text
The Full Text of this article is available as a PDF (4.8 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Ayer-LeLievre C., Olson L., Ebendal T., Seiger A., Persson H. Expression of the beta-nerve growth factor gene in hippocampal neurons. Science. 1988 Jun 3;240(4857):1339–1341. doi: 10.1126/science.2897715. [DOI] [PubMed] [Google Scholar]
- Balázs R., Jørgensen O. S., Hack N. N-methyl-D-aspartate promotes the survival of cerebellar granule cells in culture. Neuroscience. 1988 Nov;27(2):437–451. doi: 10.1016/0306-4522(88)90279-5. [DOI] [PubMed] [Google Scholar]
- Bandtlow C. E., Heumann R., Schwab M. E., Thoenen H. Cellular localization of nerve growth factor synthesis by in situ hybridization. EMBO J. 1987 Apr;6(4):891–899. doi: 10.1002/j.1460-2075.1987.tb04835.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bottenstein J. E., Sato G. H. Growth of a rat neuroblastoma cell line in serum-free supplemented medium. Proc Natl Acad Sci U S A. 1979 Jan;76(1):514–517. doi: 10.1073/pnas.76.1.514. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Breder C. D., Dinarello C. A., Saper C. B. Interleukin-1 immunoreactive innervation of the human hypothalamus. Science. 1988 Apr 15;240(4850):321–324. doi: 10.1126/science.3258444. [DOI] [PubMed] [Google Scholar]
- Flanders K. C., Roberts A. B., Ling N., Fleurdelys B. E., Sporn M. B. Antibodies to peptide determinants in transforming growth factor beta and their applications. Biochemistry. 1988 Jan 26;27(2):739–746. doi: 10.1021/bi00402a037. [DOI] [PubMed] [Google Scholar]
- Fontana A., Kristensen F., Dubs R., Gemsa D., Weber E. Production of prostaglandin E and an interleukin-1 like factor by cultured astrocytes and C6 glioma cells. J Immunol. 1982 Dec;129(6):2413–2419. [PubMed] [Google Scholar]
- Giulian D., Baker T. J., Shih L. C., Lachman L. B. Interleukin 1 of the central nervous system is produced by ameboid microglia. J Exp Med. 1986 Aug 1;164(2):594–604. doi: 10.1084/jem.164.2.594. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gray P. W., Glaister D., Chen E., Goeddel D. V., Pennica D. Two interleukin 1 genes in the mouse: cloning and expression of the cDNA for murine interleukin 1 beta. J Immunol. 1986 Dec 1;137(11):3644–3648. [PubMed] [Google Scholar]
- Greene L. A., Shooter E. M. The nerve growth factor: biochemistry, synthesis, and mechanism of action. Annu Rev Neurosci. 1980;3:353–402. doi: 10.1146/annurev.ne.03.030180.002033. [DOI] [PubMed] [Google Scholar]
- Hatten M. E., Lynch M., Rydel R. E., Sanchez J., Joseph-Silverstein J., Moscatelli D., Rifkin D. B. In vitro neurite extension by granule neurons is dependent upon astroglial-derived fibroblast growth factor. Dev Biol. 1988 Feb;125(2):280–289. doi: 10.1016/0012-1606(88)90211-4. [DOI] [PubMed] [Google Scholar]
- Hayashi S., Gillam I. C., Delaney A. D., Tener G. M. Acetylation of chromosome squashes of Drosophila melanogaster decreases the background in autoradiographs from hybridization with [125I]-labeled RNA. J Histochem Cytochem. 1978 Aug;26(8):677–679. doi: 10.1177/26.8.99471. [DOI] [PubMed] [Google Scholar]
- Hazuda D. J., Lee J. C., Young P. R. The kinetics of interleukin 1 secretion from activated monocytes. Differences between interleukin 1 alpha and interleukin 1 beta. J Biol Chem. 1988 Jun 15;263(17):8473–8479. [PubMed] [Google Scholar]
- Heumann R., Korsching S., Bandtlow C., Thoenen H. Changes of nerve growth factor synthesis in nonneuronal cells in response to sciatic nerve transection. J Cell Biol. 1987 Jun;104(6):1623–1631. doi: 10.1083/jcb.104.6.1623. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Heumann R., Lindholm D., Bandtlow C., Meyer M., Radeke M. J., Misko T. P., Shooter E., Thoenen H. Differential regulation of mRNA encoding nerve growth factor and its receptor in rat sciatic nerve during development, degeneration, and regeneration: role of macrophages. Proc Natl Acad Sci U S A. 1987 Dec;84(23):8735–8739. doi: 10.1073/pnas.84.23.8735. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Korsching S., Auburger G., Heumann R., Scott J., Thoenen H. Levels of nerve growth factor and its mRNA in the central nervous system of the rat correlate with cholinergic innervation. EMBO J. 1985 Jun;4(6):1389–1393. doi: 10.1002/j.1460-2075.1985.tb03791.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Le Moal M. A., Stoeck M., Cavaillon J. M., MacDonald H. O., Truffa-Bachi P. A sensitive, IL-2-independent, assay for IL-1. J Immunol Methods. 1988 Feb 24;107(1):23–30. doi: 10.1016/0022-1759(88)90004-x. [DOI] [PubMed] [Google Scholar]
- Levi-Montalcini R., Angeletti P. U. Nerve growth factor. Physiol Rev. 1968 Jul;48(3):534–569. doi: 10.1152/physrev.1968.48.3.534. [DOI] [PubMed] [Google Scholar]
- Lindholm D., Heumann R., Hengerer B., Thoenen H. Interleukin 1 increases stability and transcription of mRNA encoding nerve growth factor in cultured rat fibroblasts. J Biol Chem. 1988 Nov 5;263(31):16348–16351. [PubMed] [Google Scholar]
- Lindholm D., Heumann R., Meyer M., Thoenen H. Interleukin-1 regulates synthesis of nerve growth factor in non-neuronal cells of rat sciatic nerve. Nature. 1987 Dec 17;330(6149):658–659. doi: 10.1038/330658a0. [DOI] [PubMed] [Google Scholar]
- Lomedico P. T., Gubler U., Hellmann C. P., Dukovich M., Giri J. G., Pan Y. C., Collier K., Semionow R., Chua A. O., Mizel S. B. Cloning and expression of murine interleukin-1 cDNA in Escherichia coli. 1984 Nov 29-Dec 5Nature. 312(5993):458–462. doi: 10.1038/312458a0. [DOI] [PubMed] [Google Scholar]
- McCarthy K. D., de Vellis J. Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J Cell Biol. 1980 Jun;85(3):890–902. doi: 10.1083/jcb.85.3.890. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nieto-Sampedro M., Berman M. A. Interleukin-1-like activity in rat brain: sources, targets, and effect of injury. J Neurosci Res. 1987;17(3):214–219. doi: 10.1002/jnr.490170303. [DOI] [PubMed] [Google Scholar]
- Rennert P. D., Heinrich G. Nerve growth factor mRNA in brain: localization by in situ hybridization. Biochem Biophys Res Commun. 1986 Jul 31;138(2):813–818. doi: 10.1016/s0006-291x(86)80569-1. [DOI] [PubMed] [Google Scholar]
- Scott J., Selby M., Urdea M., Quiroga M., Bell G. I., Rutter W. J. Isolation and nucleotide sequence of a cDNA encoding the precursor of mouse nerve growth factor. Nature. 1983 Apr 7;302(5908):538–540. doi: 10.1038/302538a0. [DOI] [PubMed] [Google Scholar]
- Shelton D. L., Reichardt L. F. Studies on the expression of the beta nerve growth factor (NGF) gene in the central nervous system: level and regional distribution of NGF mRNA suggest that NGF functions as a trophic factor for several distinct populations of neurons. Proc Natl Acad Sci U S A. 1986 Apr;83(8):2714–2718. doi: 10.1073/pnas.83.8.2714. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Spranger Matthias, Lindholm Dan, Bandtlow Christine, Heumann Rolf, Gnahn Hannes, Näher-Noé Martina, Thoenen Hans. Regulation of Nerve Growth Factor (NGF) Synthesis in the Rat Central Nervous System: Comparison between the Effects of Interleukin-1 and Various Growth Factors in Astrocyte Cultures and in vivo. Eur J Neurosci. 1990 Jan;2(1):69–76. doi: 10.1111/j.1460-9568.1990.tb00382.x. [DOI] [PubMed] [Google Scholar]
- Tagaya Y., Okada M., Sugie K., Kasahara T., Kondo N., Hamuro J., Matsushima K., Dinarello C. A., Yodoi J. IL-2 receptor(p55)/Tac-inducing factor. Purification and characterization of adult T cell leukemia-derived factor. J Immunol. 1988 Apr 15;140(8):2614–2620. [PubMed] [Google Scholar]
- Thoenen H., Bandtlow C., Heumann R. The physiological function of nerve growth factor in the central nervous system: comparison with the periphery. Rev Physiol Biochem Pharmacol. 1987;109:145–178. doi: 10.1007/BFb0031026. [DOI] [PubMed] [Google Scholar]
- Thoenen H., Barde Y. A. Physiology of nerve growth factor. Physiol Rev. 1980 Oct;60(4):1284–1335. doi: 10.1152/physrev.1980.60.4.1284. [DOI] [PubMed] [Google Scholar]
- Whittemore S. R., Ebendal T., Lärkfors L., Olson L., Seiger A., Strömberg I., Persson H. Development and regional expression of beta nerve growth factor messenger RNA and protein in the rat central nervous system. Proc Natl Acad Sci U S A. 1986 Feb;83(3):817–821. doi: 10.1073/pnas.83.3.817. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Whittemore S. R., Friedman P. L., Larhammar D., Persson H., Gonzalez-Carvajal M., Holets V. R. Rat beta-nerve growth factor sequence and site of synthesis in the adult hippocampus. J Neurosci Res. 1988 Aug;20(4):403–410. doi: 10.1002/jnr.490200402. [DOI] [PubMed] [Google Scholar]
- Whittemore S. R., Seiger A. The expression, localization and functional significance of beta-nerve growth factor in the central nervous system. Brain Res. 1987 Nov;434(4):439–464. doi: 10.1016/0165-0173(87)90008-7. [DOI] [PubMed] [Google Scholar]
- Young P. R., Hazuda D. J., Simon P. L. Human interleukin 1 beta is not secreted from hamster fibroblasts when expressed constitutively from a transfected cDNA. J Cell Biol. 1988 Aug;107(2):447–456. doi: 10.1083/jcb.107.2.447. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Young P. R., Sylvester D. Cloning of rabbit interleukin-1 beta: differential evolution of IL-1 alpha and IL-1 beta proteins. Protein Eng. 1989 May;2(7):545–551. doi: 10.1093/protein/2.7.545. [DOI] [PubMed] [Google Scholar]
