Abstract
NITRIC oxide, a free-radical gas produced endogenously by several mammalian cell types1–6, has been implicated as a diffusible inter-cellular messenger subserving use-dependent modification of synaptic efficacy in the mature central nervous system7–10. It has been suggested on theoretical grounds that nitric oxide might play an analogous role during the establishment of ordered connections by developing neurons11. We report here that nitric oxide rapidly and reversibly inhibits growth of neurites of rat dorsal root ganglion neurons in vitro. In addition, we show that exposure to nitric oxide inhibits thioester-linked long-chain fatty acylation of neuronal proteins, possibly through a direct modification of substrate cysteine thiols. Our results demonstrate a potential role for nitric oxide in the regulation of process outgrowth and remodelling during neuronal development, which may be effected at least in part through modulation of dynamic protein fatty acylation in neuronal growth cones.
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References
Ignarro, L. J. A. Rev. Pharmac. Toxicol. 30, 535–560 (1990).
Garthwaite, J. Trends Neurosci. 14, 60–67 (1991).
Garthwaite, J., Charles, S. L. & Chess-Williams, R. Nature 336, 385–388 (1988).
Knowles, R. G., Palacios, M., Palmer, R. M. J. & Moncada, S. Proc. natn. Acad. Sci. U.S.A. 86, 5159–5162 (1989).
Bredt, D. S. et al. Neuron 7, 615–624 (1991).
Bredt, D. S. & Snyder, S. H. Proc. natn. Acad. Sci. U.S.A. 87, 682–685 (1990).
Böhme, G. A., Bon, C., Stutzmann, J.-M., Doble, A. & Blanchard, J. C. Eur. J. Pharmac. 199, 379–381 (1991).
O'Dell, T. J., Hawkins, R. D., Kandel, E. R. & Arancio, O. Proc. natn. Acad. Sci. U.S.A. 88, 11285–11289 (1991).
Schuman, E. M. & Madison, D. V. Science 254, 1503–1506 (1991).
Shibuki, K. & Okada, D. Nature 349, 326–328 (1991).
Gally, J. A., Montague, P. R., Reeke, G. N. Jr & Edelman, G. M. Proc. natn. Acad. Sci. U.S.A. 87, 3574–3551 (1990).
Böhme, E. et al. Adv. Cyclic Nucleotide Prot. Phosphorylation Res. 17, 259–266 (1984).
Manzoni, O. et al. Neuron 8, 653–662 (1992).
Stamler, J. S. et al. Proc. natn. Acad. Sci. U.S.A. 89, 444–448 (1992).
Lipton, S. A. et al. Nature 364, 626–632 (1993).
Skene, J. H. P. & Virag, I. J. Cell Biol. 108, 613–624 (1989).
Kaufman, J. F., Krangel, M. S. & Strominger, J. L. J. biol. Chem. 259, 7230–7238 (1984).
Hess, D. T., Slater, T. M., Wilson, M. C. & Skene, J. H. P. J. Neurosci. 12, 4634–4641 (1992).
Skene, J. H. P. et al. Science 233, 783–786 (1986).
Oyler, G. A. et al. J. Cell Biol. 109, 3039–3052 (1989).
Osen-Sand, A. et al. Nature 364, 445–448 (1993).
Patterson, P. H. Neuron 1, 263–267 (1988).
Walter, J., Allsopp, T. E. & Bonhoffer, F. Trends Neurosci. 13, 447–452 (1990).
Bredt, D. S. & Snyder, S. H. Proc. natn. Acad. Sci. U.S.A. 86, 9030–9033 (1989).
Constantine-Paton, M., Cline, H. T. & Debski, E. A. Rev. Neurosci. 13, 129–154 (1990).
Smith, D. S. & Skene, J. H. P. Soc. Neurosci. Abstr. 16, 1163 (1990).
Lindsay, R. M. J. Neurosci. 8, 2394–2405 (1988).
Bottenstein, J. E. Adv. cell. Neurobiol. 4, 333–379 (1983).
Lei, S. Z. et al. Neuron 8, 1087–1099 (1992).
Juguelin, H. & Cassagne, C. Analyt. Biochem. 142, 329–335 (1984)
Patterson, S. I. & Skene, J. H. P. J. Cell Biol. (in the press).
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Hess, D., Patterson, S., Smith, D. et al. Neuronal growth cone collapse and inhibition of protein fatty acylation by nitric oxide. Nature 366, 562–565 (1993). https://doi.org/10.1038/366562a0
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DOI: https://doi.org/10.1038/366562a0
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