Skip to main content

Advertisement

SpringerLink
Log in

Depletion of Brain Histamine Produces Regionally Selective Protection against Thiamine Deficiency-Induced Lesions in the Rat

  • Published:
Metabolic Brain Disease Aims and scope Submit manuscript

Abstract

Breakdown of the blood brain barrier and the subsequent accumulation of free radicals, lactate, and glutamate appear to be the immediate causes of thiamine deficiency (TD)-induced damage to thalamus. The mechanisms triggering these events are unknown but recent evidence suggests an important role of histamine. We therefore studied the effects of histamine depletion on thalamic lesions in the pyrithiamine-induced thiamine deficient (PTD) rat. Chronic intracerebroventricular (i.c.v., 7 days) infusion of α-fluoromethylhistidine (FMH), combined with bilateral ibotenate destruction of the histamine-containing neurons in the tuberomammillary (TM) nucleus and bolus i.c.v. infusion of 48/80, a potent mast cell degranulating agent, was used to deplete brain histamine levels. PTD rats receiving combined FMH + 48/80 + TM lesions developed acute neurological symptoms, including spontaneous seizures, approximately 1 day earlier than PTD rats treated with i.c.v. infusion of vehicle and sham lesions of the TM. When examined 1 week after restoration of thiamine, the PTD vehicle + sham lesion animals contained severe neuronal loss and gliosis in midline, intralaminar, ventral, lateral, and posterior nuclei. PTD animals treated with FMH + 48/80 + TM lesions had little evidence of neuronal loss or microglial proliferation in thalamus except in the gelatinosus and anteroventral nuclei, in which there was complete neuronal loss. These data demonstrate a significant and regionally selective role of histamine in the development of thalamic lesions in a rat model of Wernicke's encephalopathy. Furthermore, these data suggest either a dissociation between seizures and thalamic lesions or a significant role of histamine in seizure-related damage to the thalamus.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

REFERENCES

  • Abbott, N.J. (2000). Inflammatory mediators and modulation of blood-brain barrier permeability. Cell. Mol. Neurobiol. 20:131-147.

    Google Scholar 

  • Blass, J.P. (1979). Disorders of pyruvate metabolism. Neurology 29:280-286.

    Google Scholar 

  • Bugajski, A.J., Chlap, Z., Gadek-Michalska, A., Borycz, J., and Bugajski, J. (1997). Effect of compound 48/80 on mast cells and histamine levels in rat brain and on corticosterone secretion. Inflamm. Res. 46(Suppl. 1): S47-S48.

    Google Scholar 

  • Calingasan, N.Y., Baker, H., Sheu, K.-F.R., and Gibson, G.E. (1995). Blood-brain barrier abnormalities in vulnerable brain regions during thiamine deficiency. Exp. Neurol. 134:64-72.

    Google Scholar 

  • Calingasan, N.Y., Park, L.C.H., Callo, L.L., Trifiletti, R.R., Gandy, S.E., and Gibson, G.E. (1998). Induction of nitric oxide synthase and microglial responses precede selective cell death induced by impairment of oxidative metabolism. Am. J. Pathol. 153:599-610.

    Google Scholar 

  • Colwell, C.S., and Levine, M.S. (1997). Histamine modulates NMDA-mediated swelling in the neostriatum. Brain Res. 766:205-212.

    Google Scholar 

  • De Reuck, J.L., Sieben, G.J., Sieben-Praet, M.R., Ngendahayo, P., De Coster, W.J.P., and Vander Eecken, H.M. (1980). Wernicke's encephalopathy in patients with tumors of the lymphoid-hemopoietic systems. Arch. Neurol. 37:338-341.

    Google Scholar 

  • Ferguson, M., Dalve-Endres, A.M., McRee, R.C., and Langlais, P.J. (1999). Increased mast cell degranulation within thalamus in early pre-lesion stages of an experimental model of Wernicke's encephalopathy. J. Neuropathol. Exp. Neurol. 58:773-783.

    Google Scholar 

  • Foresti, V., Parisio, E., Scolari, N., Sparacio, F., and Confalonieri, F. (1986). Sindrome da immunodefizienza acquisita associata a tuberculosi disseminata ed a encefalopatia cronica di Wernicke. Recenti Prog. Med. 77:350-352.

    Google Scholar 

  • Galli, S.J. (1993). New concepts about the mast cell. N. Engl. J. Med. 328:257-265.

    Google Scholar 

  • Glowinski, J., and Iversen, L.L. (1966). Regional studies of catecholamines in the rat brain. I. The disposition of tritiated norepinephrine, dopamine and dopa in various regions of the brain. J. Neurochem. 13:655-669.

    Google Scholar 

  • Goldschmidt, R.C., Hough, L.B., Glick, S.D., and Padawer, J. (1984). Mast cells in rat thalamus: Nuclear localization, sex differences, and left-right asymmetry. Brain Res. 323:209-217.

    Google Scholar 

  • Hakim, A.M. (1984). The induction and reversibility of cerebral acidosis in thiamine deficiency. Ann. Neurol. 16:673-679.

    Google Scholar 

  • Hakim, A.M. (1986). Effect of thiamine deficiency and its reversal on cerebral blood flow in the rat. Observations on the phenomena of hyperperfusion, “no reflow” and delayed hypoperfusion. J. Cereb. Blood Flow Metab. 6:79-85.

    Google Scholar 

  • Harata, N., and Iwasaki, Y. (1995). Evidence for early blood-brain barrier breakdown in experimental thiamine deficiency in the mouse. Metab. Brain Dis. 10:159-174.

    Google Scholar 

  • Harper, C.G., Giles, M., and Finaly-Jones, R. (1986). Clinical signs in the Wernicke-Korsakoff complex-a retrospective analysis of 131 cases diagnosed at autopsy. J. Neurol. Neurosurg. Psychiatry 49:341-345.

    Google Scholar 

  • Hough, L.B. (1999). Histamine. In (G. Siegel, B. Agranoff, R. Albers, S. Fisher, and M. Uhler, eds.), Basic Neurochemistry, Lippincott-Raven, New York, pp. 293-313.

    Google Scholar 

  • Jellinger, K., and Seitelberger, F. (1970). Subacute necrotizing encephalomyelopathy. In (I. Mehilmeyer, A.F. Muller, A. Prader, and R. Schoen, eds.), Ergebuisse Der Innerren Medizin und Kinderkeikunde, Springer, Berlin-Heidelberg, pp. 155-219.

    Google Scholar 

  • Langlais, P.J., Anderson, G., Guo, S.-X., and Bondy, S.C. (1997). Increased cerebral free radical production during thiamine deficiency. Metab. Brain Dis. 12:137-143.

    Google Scholar 

  • Langlais, P.J., Anderson, G., Powell, H., and Dimlich, R. (1999). Mast cell degranulation and edematous changes in pre-necrotic stages of a rat model of Wernicke's encephalopathy. Brain Pathol. 7:1020.

    Google Scholar 

  • Langlais, P.J., and Mair, R.G. (1990). Protective effects of the glutamate antagonist MK-801 on pyrithiamine induced lesions and amino acid changes in rat brain. J. Neurosci. 10:1664-1674.

    Google Scholar 

  • Langlais, P.J., and Zhang, S.-X. (1993). Extracellular glutamate is increased in thalamus during thiamine deficiencyinduced lesions and is blocked by MK-801. J. Neurochem. 61:1155-1158.

    Google Scholar 

  • Langlais, P.J., Zhang, S.X., Weilersbacher, G., Hough, L.B., and Barke, K.E. (1994). Histamine-mediated neuronal death in a rat model of Wernicke's encephalopathy. J. Neurosci. Res. 38:564-565.

    Google Scholar 

  • Lindboe, C.F., and Loberg, E.M. (1988). The frequency of brain lesions in alcoholics. J. Neurol. Sci. 88:107-113.

    Google Scholar 

  • Lopez, R.I., and Collins, G.H. (1968).Wernicke's encephalopathy: A complication of chronic hemodialysis. Arch. Neurol. 18:248-259.

    Google Scholar 

  • McRee, R.C., Terry-Ferguson, M., Langlais, P.J., Chen, Y., Nalwalk, J.W., Blumenstock, F.A., and Hough, L.B. (2000). Increased histamine release and granulocytes within the thalamus of a rat model of Wernicke's encephalopathy. Brain Res. 858:227-236.

    Google Scholar 

  • Nightingale, S., Bates, D., Heath, P.D., and Barron, F. (1982). Wernicke's encephalopathy in hyperemesis gravidarum. Postgrad. Med. J. 58:558-559.

    Google Scholar 

  • Okayama, Y., Bradding, P., Tunon-de-Lara, J.M., Holgate, S.T., and Church, M.K. (1993). Cytokine production by human mast cells. In (G. Marone, ed.), Human Basophils and Mast cells: Biological Aspects, Vol. 61, Karger, New York, pp. 114-134.

    Google Scholar 

  • Omer, S.M., Kawi, M.Z., Watban, J., Bohlega, S., McLean, D.R., and Miller, G. (1995). Acute Wernicke's encephalopathy associated with hyperemesis gravidarum: Magnetic resonance findings. J. Neuroimaging 5:251-253.

    Google Scholar 

  • Onodera, K., Maeyama, K., and Watanabe, T. (1988). Regional changes in brain histamine levels following dietary-induced thiamine deficiency in rats. Jpn. J. Pharmacol. 47:323-326.

    Google Scholar 

  • Onodera, K., Shinoda, H., and Watanabe, T. (1990). Effects of thiamine on hypothermia and hypothalamic histamine levels in dietary-induced thiamine deficient rats. Jpn. J. Pharmacol. 54:339-343.

    Google Scholar 

  • O'Rourke, N.P., Bunker, V.W., Thomas, A.J., Finglas, P.M., Bailey, A.L., and Clayton, B.E. (1990). Thiamine status of healthy and institutionalized elderly subjects: Analysis of dietary intake and biochemical indices. Age Ageing 19:325-329.

    Google Scholar 

  • Palacios, J.M., Wamsley, J.K., and Kuhar, M.J. (1981). The distribution of H,-receptors in the rat brain: An autographic study. Neuroscience 6:15-37.

    Google Scholar 

  • Panula, P., Airaksinen, M.S., Pirvola, U., and Kotilainen, E. (1990). A histamine-containing neuronal system in human brain. Science 34:127-132.

    Google Scholar 

  • Pitella, J.E.H., and de Castro, L.P.F. (1990). Wernicke's encephalopathy manifested as Korsakoff syndrome in a patient with promyelocytic leukemia. South. Med. J. 83:570-573.

    Google Scholar 

  • Purcell, W.M., and Atterwill, C.K. (1995). Mast cells in neuroimmune function: Neurotoxicological and neuropharmacological perspectives. Neurochem. Res. 20:521-532.

    Google Scholar 

  • Schwenk, J., Gosztonyi, G., Thierauf, P., Iglesias, J., and Langer, E. (1990). Wernicke's encephalopathy in two patients with acquired immunodeficiency syndrome. J. Neurol. 237:445-447.

    Google Scholar 

  • Shelton, M.K., and McCarthy, K.D. (2000). Hippocampal astrocytes exhibit Ca++-elevating muscarinic, cholinergic and histaminergic receptors in situ. J. Neurochem. 74:555-563.

    Google Scholar 

  • Skratt, J.J., Hough, L.B., Nalwalk, J.W., and Barke, K.E. (1994). alpha-Fluoromethylhistidine-induced inhibition of brain histidine decarboxylase. Implications for the CO2-trapping enzymatic method. Biochem. Pharmacol. 47:397-402.

    Google Scholar 

  • Steinbusch, H.M., and Verhofstad, A.J. (1986). Immunocytochemical demonstration of noradrenaline, serotonin and histamine and some observations of the innervations of the intracerebral blood vessels. In (C. Owman and J.E. Hardebo, eds.), Neural Regulation of Brain Circulation, Elsevier, Amsterdam, Holland, pp. 181-194.

    Google Scholar 

  • Tagaki, H. Moroshima, T., Matsuyama, T., Hayashi, H., Watanabe, T., and Wada, H. (1986). Histaminergic axons in the neostriatum and cerebral cortex of the ratio correlated light and electron microscopic immunocytochemical study using histidine decarboxylase as a Marker. Brain Research 364:114-123.

    Google Scholar 

  • Todd, K.G., and Butterworth, R.F. (1998). Evaluation of the role ofNMDA-mediated excitotoxicity in the selective neuronal loss in experimental Wernicke encephalopathy. Exp. Neurol. 149:130-138.

    Google Scholar 

  • Verburg, K.M., Bowsher, R.R., and Henry, D.P. (1983). A new radioenzymatic assay for histamine using purified histamine-N-methyltransferase. Life Sci. 32:2855-2867.

    Google Scholar 

  • Victor, M., Adams, R.D., and Collins, G.H. (1989). The Wernicke-Korsakoff Syndrome and Related Neurologic Disorders Due to Alcoholism and Malnutrition, Davis, Philadelphia, Pennsylvania.

    Google Scholar 

  • Watanabe, I., and Kanabe, S. (1978). Early edematous lesion of pyrithiamine-induced acute thiamine-deficient encephalopathy in the mouse. J. Neuropathol. Exp. Neurol. 37:401-413.

    Google Scholar 

  • Watanabe, T., Yamatodani, A., Maeyama, K., and Wada, H. (1990). Pharmacology of ?-fluoromethylhistidine, a specific inhibitor of histidine decarboxylase. TIPS 11:363-367. Yokohama, H., Onodera, K.,Maeyama, K.,Yanai, K., Iinuma, K.,Tuomisto, L., andWatanabe,T. (1992). Histamine levels and clonic convulsions of electrically-induced seizure in mice: The effects of ?-fluoromethylhistidine and metoprine. N.-S. Arch. Pharmacol. 346:4-45.

    Google Scholar 

  • Zhang, S.-X., Weilersbacher, G.S., Henderson, S.W., Corso, T., Olney, J.W., and Langlais, P.J. (1995). Excitotoxic cytopathology, progression, and reversibility of thiamine deficiency-induced diencephalic lesions. J. Neuropathol. Exp. Neurol. 54:255-267.

    Google Scholar 

Download references

Authors
  1. Philip J. Langlais
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Robert Carter McRee
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Julia A. Nalwalk
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lindsay B. Hough
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Langlais, P.J., McRee, R.C., Nalwalk, J.A. et al. Depletion of Brain Histamine Produces Regionally Selective Protection against Thiamine Deficiency-Induced Lesions in the Rat. Metab Brain Dis 17, 199–210 (2002). https://doi.org/10.1023/A:1019930206196

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1019930206196

Search

Navigation