Skip to main content
Log in

Reserpine- and tetrabenazine-sensitive transport of3H-histamine by the neuronal isoform of the vesicular monoamine transporter

  • Published:
Journal of Molecular Neuroscience Aims and scope Submit manuscript

Abstract

The transport of3H-histamine by the endocrine-specific (VMAT1) and neuronal (VMAT2) isoforms of the vesicular monoamine transporter has been evaluated in digitonin-permeabilized fibroblasts transfected with either VMAT1 or VMAT2. Transport of3H-histamine by both VMAT1 and VMAT2 was reserpine-sensitive but only transport by VMAT2 was inhibited by tetrabenazine. Maximal equilibrated levels of3H-histamine accumulation by VMAT2 (K m∼300 µM) were approximately three times greater than that mediated by VMAT1 when using a subsaturating concentration of exogenous3H-histamine (50 µM). The expression of VMAT2 in histaminergic neurons in the rat brain was examined with polyclonal antipeptide antibodies specific for VMAT1 or VMAT2. VMAT2-positive and tyrosine hydroxylase-negative immunoreactive cell bodies were localized to the ventral part of the posterior hypothalamus in the region of the mamillary nuclei. The transport properties of VMAT2 and the distribution of VMAT2 in cell bodies in the tuberomammillary nucleus of the posterior hypothalamus reported here and the apparent absence of VMAT1 and VMAT2 in tissue mast cells support previous findings of reserpine-sensitive and reserpine-resistant pools of histamine in brain and peripheral tissues.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Atack C. (1971) Reduction of histamine in mouse brain by N1-(D. L-seryl)-N2-(2,3,4-trihydroxybenzyl) hydrazine and reserpine.J. Pharm. Pharmacol. 23, 992,993.

    PubMed  CAS  Google Scholar 

  • Atack C. and Carlsson A. (1972) In vitro release of endogenous histamine, together with noradrenaline and 5-hydroxytryptamine, from slices of mouse cerebral hemispheres.J. Pharm. Pharmacol. 24, 990–992.

    PubMed  CAS  Google Scholar 

  • Buu N. T. (1989) Modification of vesicular dopamine and norepinephrine by monoamine oxidase inhibitors.Biochem. Pharmacol. 38, 1685–1692.

    Article  PubMed  CAS  Google Scholar 

  • Dismukes H. and Snyder S. H. (1974) Histamine turnover in rat brain.Brain Res. 78, 467–481.

    Article  PubMed  CAS  Google Scholar 

  • Erickson J. D., Eiden L. E., and Hoffman B. (1992) Expression cloning of a reserpine-sensitive vesicular monoamine transporter.Proc. Natl. Acad. Sci. USA 89, 10,993–10,997.

    Article  CAS  Google Scholar 

  • Erickson J. D. and Eiden L. E. (1993) Functional identification and molecular cloning of a human brain vesicle monoamine transporter.J. Neurochem. 61, 2314–2317.

    Article  PubMed  CAS  Google Scholar 

  • Erickson J. D., Schafer M. K.-H., Bonner T. I., Eiden L. E., and Weihe E. (1996) Distributions in neuronal and endocrine cells and distinct pharmacological properties of two isoforms of the human vesicular monoamine transporter.Proc. Natl. Acad. Sci. USA, in press.

  • Fuerst T. R., Niles E. G., Studier F. W., and Moss B. (1986) Eukaryotic transient-expression system based on recombinant vaccinia virus that synthesizes bacteriophage T7 RNA polymerase.Proc. Natl. Acad. Sci. USA 83, 8122–8126.

    Article  PubMed  CAS  Google Scholar 

  • Garbarg M., Barbin G., Bischoff S., Pollard H., and Schwartz J. C. (1976) Dual localization of histamine in an ascending neuronal pathway and in non-neuronal cells evidenced by lesions in the lateral hypothalamic area.Brain Res. 106, 333–348.

    Article  PubMed  CAS  Google Scholar 

  • Garbarg M., Barbin G., Rodergas E., and Schwartz J. C. (1980) Inhibition of histamine synthesis in brain by α-fluoromethylhistidine, a new irreversible inhibitor: in vitro and in vivo studies.J. Neurochem. 35, 1045–1052.

    Article  PubMed  CAS  Google Scholar 

  • Gonzalez A. M., Walther D., Pazos A., and Uhl G. A. (1994) Synaptic vesicular monamine transporter expression: distribution and pharmacologic profile.Mol. Brain Res. 22, 219–226.

    Article  PubMed  CAS  Google Scholar 

  • Green H. and Erickson R. W. (1964) Effect of some drugs upon rat brain histamine content.Int. J. Neuropharmacol. 3, 315–320.

    Article  PubMed  CAS  Google Scholar 

  • Hakanson R., Bottcher G., Ekblad E., Panula P., Simonsson M., Dohlsten M., Hallberg T., and Sundler F. (1986) Histamine in endocrine cells in the stomach: a survey of several species using a panel of histamine antibodies.Histochemistry 86, 5–17.

    Article  PubMed  CAS  Google Scholar 

  • Hough L. and Domino E. (1979) Tele-methylhistamine oxidation by type B monoamine oxidase.J. Pharmacol. Exp. Ther. 208, 422–428.

    PubMed  CAS  Google Scholar 

  • Kanner B. I. and Bendahan A. (1985) Transport of 5-hydroxytryptamine in membrane vesicles from rat basophilic leukemia cells.Biochim. Biophys. Acta 816, 403–410.

    Article  PubMed  CAS  Google Scholar 

  • Liu Y., Peter D., Roghani A., Schuldiner S., Prive G. G., Eisenberg D., Brecha N., and Edwards R. H. (1992) A cDNA that suppresses MPP+ toxicity encodes a vesicular amine transporter.Cell 70, 539–551.

    Article  PubMed  CAS  Google Scholar 

  • Maeyama K., Watanabe T., Yamatodani A., and Wada H. (1983) Effect of α-fluoromethylhistidine on the histamine content of the brain of W/W mice devoid of mast cells: turnover of brain histamine.J. Neurochem. 41, 128–134.

    Article  PubMed  CAS  Google Scholar 

  • Martres M. P., Baudry M., and Schwartz J. C. (1975) Histamine synthesis in the developing rat brain: evidence for multiple compartmentation.Brain Res. 83, 261–275.

    Article  PubMed  CAS  Google Scholar 

  • Menckel A. and Edwards, R. H. (1995) Transport of histamine by vesicular monoamine transporter-2.Neuropharmacology 34, 1543–1547.

    Article  Google Scholar 

  • Metcalfe D. D., Costa J. J., and Burd P. R. (1992) Mast cells and basophils, inInflammation: Basic Principles and Clinical Correlates, 2nd ed. (Gallin J. I., Goldstein I. M., and Snyderman R., eds.), Raven, New York, pp. 709–725.

    Google Scholar 

  • Moran N. C. and Westerholm B. (1963) The influence of reserpine on hydroxytryptamine and histamine content of rat mast cells and of some rat tissues.Acta Physiol. Scand. 58, 20–29.

    Article  CAS  Google Scholar 

  • Muroi N., Oishi R., and Saeki K. (1991) Effect of reserpine on histamine metabolism in the mouse brain.J. Pharmacol. Exp. Ther. 256, 967–972.

    PubMed  CAS  Google Scholar 

  • Oishi R., Nishibori M., and Saeke K. (1984) Regional differences in the turnover of neuronal histamine in the rat brain.Life Sci. 34, 691–699.

    Article  PubMed  CAS  Google Scholar 

  • Parratt J. R. and West G. B. (1957) Release of 5-hydroxytryptamine and histamine from tissues of the rat.J. Physiol. (Lond.) 137, 179–192.

    CAS  Google Scholar 

  • Peter D., Jimenez J., Liu Y., Kim J., and Edwards R. H. (1994) The chromaffin granule and synaptic vesicle amine transporters differ in substrate recognition and sensitivity to inhibitors.J. Biol. Chem. 269, 7231–7237.

    PubMed  CAS  Google Scholar 

  • Peter D., Liu Y., Sternini C., de Giorgio R., Brecha N., and Edwards R. H. (1995) Differential expression of two vesicular monoamine transporters.J. Neurosci. 15, 6179–6188.

    PubMed  CAS  Google Scholar 

  • Pollard H., Bischoff S., and Schwartz J. C. (1973) Increased synthesis and release of3H-histamine in rat brain by reserpine.J. Pharm. Pharmacol. 25, 920–922.

    PubMed  CAS  Google Scholar 

  • Romeo H. E., Fink T., Yanaihara N., and Weihe E. (1994) Distribution and relative proportions of neuropeptide Y- and proenkephalin-containing noradrenergic neurones in rat superior cervical ganglion: separate projections to submaxilliary lymph nodes.Peptides 15, 1479–1487.

    Article  PubMed  CAS  Google Scholar 

  • Russell W. L., Henry D. P., Phebus L. A., and Clemens J. A. (1990) Release of histamine in rat hypothalamus and corpus striatum in vivo.Brain Res. 512, 95–101.

    Article  PubMed  CAS  Google Scholar 

  • Schafer M. K.-H., Nohr D., Romeo H., Eiden L. E., and Weihe E. (1994) Pan-neuronal expression of chromogranin A in rat nervous system.Peptides 15, 263–279.

    Article  PubMed  CAS  Google Scholar 

  • Schayer R. W. and Reilly M. A. (1973) Formation and fate of histamine in rat and mouse brain.J. Pharmacol. Exp. Ther. 184, 33–40.

    PubMed  CAS  Google Scholar 

  • Schwartz J. C., Pollard H., Bischoff S., Rehault M. C., and Verdiere M. (1971) Catabolism of3H-histamine in the rat brain after intracisternal administration.Eur. J. Pharmacol. 16, 326–335.

    Article  PubMed  CAS  Google Scholar 

  • Schwartz J. C., Lampart C., and Rose C. (1972) Histamine formation in rat brain in vivo: effects of histidine loads.J. Neurochem. 19, 801–810.

    Article  PubMed  CAS  Google Scholar 

  • Schwartz J.-C., Arrang J.-M., Garbarg M., Pollard H., and Ruat M. (1991) Histaminergic transmission in the mammalian brain.Physiol. Rev. 71, 1–51.

    PubMed  CAS  Google Scholar 

  • Schuldiner S., Shirvan A., and Linial M. (1995) Vesicular neurotransmitter transporters: from bacteria to humans.Physiol. Rev. 75, 369–392.

    PubMed  CAS  Google Scholar 

  • Stitzel R. E. (1977) The biological fate of reserpine.Pharmacol. Rev. 28, 179–205.

    Google Scholar 

  • Steinbusch H. W. M. (1991) Distribution of histaminergic neurons and fibers in rat brain.Acta Otalaryngol. 479, 12–23.

    CAS  Google Scholar 

  • Sugimoto K., Maeyama K., Alam M. K., Sakurai E., Onoue H., Kasugai T., Kitamura Y., and Watanabe T. (1995) Brain histaminergic system in mast cell-deficient (Ws/Ws) rats: histamine content, histidine decarboxylase activity, and effects of (S) α-fluromethylhistidine.J. Neurochem. 65, 791–797.

    Article  PubMed  CAS  Google Scholar 

  • Taylor K. M. and Snyder S. H. (1971) Histamine in rat brain: sensitive assay of endogenous levels, formation in vivo and lowering by inhibitors of histidine decarboxylase.J. Pharmacol. Exp. Ther. 179, 619–633.

    PubMed  CAS  Google Scholar 

  • Taylor K. M. and Snyder S. H. (1972) Dynamics of the regulation of histamine levels in mouse brain.J. Neurochem. 19, 341–354.

    Article  PubMed  CAS  Google Scholar 

  • Taylor K. M. and Snyder S. H. (1973) The release of histamine from tissue slices of rat hypothalamus.J. Neurochem. 21, 1215–1223.

    Article  PubMed  CAS  Google Scholar 

  • Verdiere M., Rose C., and Schwartz J. C. (1975) Synthesis and release of histamine studied on slices from rat hypothalamus.Eur. J. Pharmacol. 34, 157–168.

    Article  PubMed  CAS  Google Scholar 

  • Wada H., Inagaki N., Yamatodani A., and Watanabe T. (1991) Is the histaminergic neuron system a regulatory center for whole-brain activity?Trends Neurosci. 14, 415–418.

    Article  PubMed  CAS  Google Scholar 

  • Weihe E., Schafer M. K.-H., Erickson J. D., and Eiden L. E. (1994) Localization of vesicular monoamine transporter isoforms (VMAT1 and VMAT2) to endocrine cells and neurons in rat.J. Mol. Neurosci. 5, 149–164.

    PubMed  CAS  Google Scholar 

  • Weiner N. (1970) Regulation of norepinephrine biosynthesis.Ann. Rev. Pharmacol. 10, 273–290.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Erickson, J.D., Eiden, L.E., Schäfer, M.K.H. et al. Reserpine- and tetrabenazine-sensitive transport of3H-histamine by the neuronal isoform of the vesicular monoamine transporter. J Mol Neurosci 6, 277–287 (1995). https://doi.org/10.1007/BF02736786

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02736786

Index Entries

Navigation