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Chronic treatment of newborn rats with naltrexone alters astrocyte production of nerve growth factor

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Abstract

Newborn rats were treated with the opiate antagonist naltrexone daily for 1–2 wk in order to examine the effects of endogenous opioid peptides on astrocytes during CNS development. Nerve growth factor (NGF) and cyclic AMP were measured in astrocytes cultured from cerebellum, striatum, and hippocampus of 1 d, 1 wk, and 2 wk postnatal rats. Cerebellar and striatal, but not hippocampal, astrocytes prepared from naltrexone-treated animals produced higher levels of NGF than those from controls. The turnover rate of cyclic AMP, measured following treatment of the cells with forskolin in the presence of the phosphodiesterase inhibitor IBMX, was increased in naltrexone-derived cerebellar and striatal astrocytes. Opiate receptors could not be detected on the cultured astrocytes, either by direct binding of3H-etorphine or by modulation of cyclic AMP content. These results suggest that endogenous opioid peptides may function indirectly to alter trophic factor synthesis in astrocytes.

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References

  • Brenneman D. E., Nicol T., Warren D., and Bowers L. M. (1990) Vasoactive intestinal peptide: a neuro-trophic releasing agent and an astroglial mitogen.J. Neurosci. Res. 25, 386–394.

    Article  PubMed  CAS  Google Scholar 

  • Carman-Krzan M., Vige X., and Wise B. C. (1991) Regulation by interleukin-1 of nerve growth factor secretion and nerve growth factor mRNA expression in rat primary astroglial cultures.J. Neurochem. 56, 636–643.

    Article  PubMed  CAS  Google Scholar 

  • Cholewinski A. J. and Wilkin G. P. (1988) Astrocytes from forebrain, cerebellum, and spinal cord differ in their responses to vasoactive intestinal peptide.J. Neurochem. 51, 1626–1633.

    Article  PubMed  CAS  Google Scholar 

  • Delitala G., Motta M., and Serio M., eds. (1984)The Opioid Modulation of Endocrine Function, Raven, New York.

    Google Scholar 

  • Eriksson P. S., Hansson E., and Rönnbäck L. (1990) δ and K opiate receptors in primary astroglial cultures from rat cerebral cortex.Neurochem. Res. 15, 1123–1126.

    Article  PubMed  CAS  Google Scholar 

  • Gadient R. A., Cron K. C., and Otten U. (1990) Interleukin-1 beta and tumor necrosis factor-alpha synergistically stimulate nerve growth factor (NGF) release from cultured rat astrocytes.Neurosci. Lett. 117, 335–340.

    Article  PubMed  CAS  Google Scholar 

  • Hendrickson C. M. and Lin S. (1980) Opiate receptors in highly purified neuronal cell populations isolated in bulk from embryonic chick brain.Neuropharmacology 19, 731–739.

    Article  PubMed  CAS  Google Scholar 

  • Kimmelberg H. K. (1988)Glial Cell Receptors, Raven, New York.

    Google Scholar 

  • Large T. H., Bodary S. C., Clegg D. O., Weskamp G., Otten U., and Reichardt L. F. (1986) Nerve growth factor gene expression in the developing rat brain.Science 234, 352–355.

    Article  PubMed  CAS  Google Scholar 

  • Lowry O. H., Rosebrough N. J., Farr A. L., and Randall R. J. (1951) Protein measurement with the Folin phenol reagent.J. Biol. Chem. 193, 265–275.

    PubMed  CAS  Google Scholar 

  • Maderspach K. and Solomonia R. (1988) Glial and neuronal opioid receptors: apparent positive cooperativity observed in intact cultured cells.Brain Res. 441, 41–47.

    Article  PubMed  CAS  Google Scholar 

  • McCarthy K. D. and DeVellis J. (1980) Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue.J. Cell Biol. 85, 890–902.

    Article  PubMed  CAS  Google Scholar 

  • Mobley W. C., Woo J. E., Edwards R. H., Riopelle R. J., Longo F. M., Weskamp G., Otten U., Valletta J. S., and Johnston M. V. (1989) Developmental regulation of nerve growth factor and its receptor in the rat caudate-putamen.Neuron 3, 655–664.

    Article  PubMed  CAS  Google Scholar 

  • Pearce B., Cambray-Deakin M., and Murphy S. (1985) Astrocyte opioid receptors: activation modifies the noradrenaline-evoked increase in 2-[14C]deoxyglucose incorporation into glycogen.Neurosci. Lett. 55, 157–160.

    Article  PubMed  CAS  Google Scholar 

  • Rougon G., Noble M., and Mudge A. W. (1983) Neuro-peptides modulate the β-adrenergic response of purified astrocytes in vitro.Nature 305, 715–717.

    Article  PubMed  CAS  Google Scholar 

  • Schwartz J. P. (1992) Neurotransmitters as neurotrophic factors: a new set of functions.Int. Rev. Neurobiol. 34, 1–23.

    Article  PubMed  CAS  Google Scholar 

  • Schwartz J. P. and Mishler K. (1990) β-Adrenergic receptor regulation, through cyclic AMP, of nerve growth factor expression in rat cortical and cerebellar astrocytes.Cell. Mol. Neurobiol. 10, 447–457.

    Article  PubMed  CAS  Google Scholar 

  • Schwartz J. P. and Passonneau J. V. (1974) Cyclic AMP-mediated induction of the cyclic AMP phosphodiesterase of C6 glioma cells.Proc. Natl. Acad. Sci. USA 71, 3844–3848.

    Article  PubMed  CAS  Google Scholar 

  • Schwartz J. P. and Wilson D. J. (1992) Preparation and characterization of type 1 astrocytes cultured from adult rat cortex, cerebellum, and striatum.Glia 5, 75–80.

    Article  PubMed  CAS  Google Scholar 

  • Slotkin T. A., Seidler F. J., and Whitmore W. L. (1980) Effects of maternal methadone administration on ornithine decarboxylase in brain and heart of the offspring: relationships of enzyme activity to dose and to growth impairment in the rat.Life Sci. 26, 861–867.

    Article  PubMed  CAS  Google Scholar 

  • Smith A. A., Hui F. W., and Crofford M. J. (1977) Inhibition of growth in young mice treated with d,1-methadone.Eur. J. Pharmacol. 43, 307–314.

    Article  PubMed  CAS  Google Scholar 

  • Stiene-Martin A. and Hauser K. F. (1990) Opioid-dependent growth of glial cultures: suppression of astrocyte DNA synthesis by met-enkephalin.Life Sci. 46, 91–98.

    Article  PubMed  CAS  Google Scholar 

  • Vaysse P. J-J., Zukin R. S., Fields K. L., and Kessler J. A. (1990) Characterization of opioid receptors in cultured neurons.J. Neurochem. 55, 624–631.

    Article  PubMed  CAS  Google Scholar 

  • Whitaker-Azmitia P. M., Murphy R., and Azmitia E. C. (1990) Stimulation of astroglial 5-HT1A receptors releases the serotonergic growth factor, protein S-100, and alters astroglial morphology.Brain Res. 528, 155–158.

    Article  PubMed  CAS  Google Scholar 

  • Whittemore S. R., Ebendal T., Lärkfors L., Olson L., Seiger A., Strömberg I., and Persson H. (1986) Developmental and regional expression of β-nerve growth factor messenger RNA and protein in the rat central nervous system.Proc. Natl. Acad. Sci. USA 83, 817–821.

    Article  PubMed  CAS  Google Scholar 

  • Wilson G. S., McCreary R., Kean J., and Baxter J. C. (1979) The development of preschool children of heroin-addicted mothers: a controlled study.Pediatrics 63, 135–141.

    PubMed  CAS  Google Scholar 

  • Zagon I. S. and McLaughlin P. J. (1983) Increased brain size and cellular content in infant rats treated with an opiate antagonist.Science 221, 1179–1180.

    Article  PubMed  CAS  Google Scholar 

  • Zagon I. S. and McLaughlin P. J. (1985) Naltrexone’s influence on neurobehavioral development.Pharmacol. Biochem. Behav. 22, 441–448.

    Article  PubMed  CAS  Google Scholar 

  • Zagon I. S. and McLaughlin P. J. (1986a) Opioid antagonist-induced modulation of cerebral and hippocampal development: histological and morphometric studies.Dev. Brain Res. 28, 233–246.

    Article  CAS  Google Scholar 

  • Zagon I. S. and McLaughlin P. J. (1986b) Opioid antagonist (naltrexone) modulation of cerebellar development: histological and morphometric studies.J. Neurosci. 6, 1424–1432.

    PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Clinical Neuroscience Branch, National Institute of Neurological Disorders and Stroke, National Institutes of Health, 20892, Bethesda, MD

    Kunihiko Mitsuo & Joan P. Schwartz

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  1. Kunihiko Mitsuo
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  2. Joan P. Schwartz
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Mitsuo, K., Schwartz, J.P. Chronic treatment of newborn rats with naltrexone alters astrocyte production of nerve growth factor. J Mol Neurosci 4, 21–28 (1993). https://doi.org/10.1007/BF02736687

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  • DOI: https://doi.org/10.1007/BF02736687

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