Histamine Function in Nervous Systems

Chapter
Part of the The Receptors book series (REC, volume 28)

Abstract

Histamine is evolutionarily highly conserved as a signaling molecule, a neuromodulator, and a neurotransmitter from bacteria to mammals that fulfills basic demands of living like the organization of behavioral state. From mussels to mammals, it gates ion channels like classical ionotropic transmitters. These relatively neglected functions are treated for arthropods and mollusks. In vertebrate brains, histamine actions are mostly mediated by three of the four known G-protein-coupled receptors: H1R, H2R, and H3R. Histamine also modifies other receptor proteins through allosteric interactions. We describe and discuss the anatomical, biophysical, and physiological properties of histaminergic neurons as well as their projections and actions on target neurons.

Keywords

Histaminergic neurons Electrophysiology Invertebrates Mammals Hypothalamus Sleep and waking Histamine receptors Neural plasticity 

References

  1. 1.
    McCaman RE, Weinreich D. On the nature of histamine-mediated slow hyperpolarizing synaptic potentials in identified molluscan neurones. J Physiol. 1982;328:485–506.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Carpenter DO, Gaubatz GL. H1 and H2 histamine receptors on Aplysia neurones. Nature. 1975;254(5498):343–4.CrossRefPubMedGoogle Scholar
  3. 3.
    Panula P, Yang HY, Costa E. Histamine-containing neurons in the rat hypothalamus. Proc Natl Acad Sci U S A. 1984;81(8):2572–6.CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Watanabe T, Maeyama K, Wada H. Histamine. Tanpakushitsu Kakusan Koso. 1984;29(12 Suppl):1443–58.PubMedGoogle Scholar
  5. 5.
    Ercan-Sencicek AG, Stillman AA, Ghosh AK, Bilguvar K, O’Roak BJ, Mason CE, et al. L-histidine decarboxylase and Tourette’s syndrome. N Engl J Med. 2010;362(20):1901–8.CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Ericson H, Watanabe T, Kohler C. Morphological analysis of the tuberomammillary nucleus in the rat brain: delineation of subgroups with antibody against L-histidine decarboxylase as a marker. J Comp Neurol. 1987;263(1):1–24.CrossRefPubMedGoogle Scholar
  7. 7.
    Yu X, Ye Z, Houston CM, Zecharia AY, Ma Y, Zhang Z, et al. Wakefulness is governed by GABA and histamine cotransmission. Neuron. 2015;87(1):164–78.CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Airaksinen MS, Paetau A, Paljarvi L, Reinikainen K, Riekkinen P, Suomalainen R, et al. Histamine neurons in human hypothalamus: anatomy in normal and Alzheimer diseased brains. Neuroscience. 1991;44(2):465–81.CrossRefPubMedGoogle Scholar
  9. 9.
    Giannoni P, Medhurst AD, Passani MB, Giovannini MG, Ballini C, Corte LD, et al. Regional differential effects of the novel histamine H3 receptor antagonist 6-[(3-cyclobutyl-2,3,4,5-tetrahydro-1H-3-benzazepin-7-yl)oxy]-N-methyl-3-pyridine carboxamide hydrochloride (GSK189254) on histamine release in the central nervous system of freely moving rats. J Pharmacol Exp Ther. 2010;332(1):164–72.CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Airaksinen MS, Reinikainen K, Riekkinen P, Panula P. Neurofibrillary tangles and histamine-containing neurons in Alzheimer hypothalamus. Agents Actions. 1991;33(1–2):104–7.CrossRefPubMedGoogle Scholar
  11. 11.
    Lin JS. Brain structures and mechanisms involved in the control of cortical activation and wakefulness, with emphasis on the posterior hypothalamus and histaminergic neurons. Sleep Med Rev. 2000;4(5):471–503.CrossRefPubMedGoogle Scholar
  12. 12.
    Taddese A, Bean BP. Subthreshold sodium current from rapidly inactivating sodium channels drives spontaneous firing of tuberomammillary neurons. Neuron. 2002;33(4):587–600.CrossRefPubMedGoogle Scholar
  13. 13.
    Greene RW, Haas HL, Reiner PB. Two transient outward currents in histamine neurones of the rat hypothalamus in vitro. J Physiol. 1990;420:149–63.CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Stevens DR, Eriksson KS, Brown RE, Haas HL. The mechanism of spontaneous firing in histamine neurons. Behav Brain Res. 2001;124(2):105–12.CrossRefPubMedGoogle Scholar
  15. 15.
    Takeshita Y, Watanabe T, Sakata T, Munakata M, Ishibashi H, Akaike N. Histamine modulates high-voltage-activated calcium channels in neurons dissociated from the rat tuberomammillary nucleus. Neuroscience. 1998;87(4):797–805.CrossRefPubMedGoogle Scholar
  16. 16.
    Sergeeva OA, Eriksson KS, Sharonova IN, Vorobjev VS, Haas HL. GABA(A) receptor heterogeneity in histaminergic neurons. Eur J Neurosci. 2002;16(8):1472–82.CrossRefPubMedGoogle Scholar
  17. 17.
    Sergeeva OA, Eriksson KS, Haas HL. Glycine receptor mediated responses in rat histaminergic neurons. Neurosci Lett. 2001;300(1):5–8.CrossRefPubMedGoogle Scholar
  18. 18.
    Prast H, Prast M, Philippu A. H3 autoreceptors and muscarinic acetylcholine receptors modulate histamine release in the anterior hypothalamus of freely moving rats. Agents Actions. 1994;41(Spec No):C64–5.CrossRefPubMedGoogle Scholar
  19. 19.
    Yanovsky Y, Li S, Klyuch BP, Yao Q, Blandina P, Passani MB, et al. L-Dopa activates histaminergic neurons. J Physiol. 2011;589(Pt 6):1349–66.CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Sergeeva OA, Amberger BT, Haas HL. Editing of AMPA and serotonin 2C receptors in individual central neurons, controlling wakefulness. Cell Mol Neurobiol. 2007;27(5):669–80.CrossRefPubMedGoogle Scholar
  21. 21.
    Siegel JM, Boehmer LN. Narcolepsy and the hypocretin system—where motion meets emotion. Nat Clin Pract Neurol. 2006;2(10):548–56.CrossRefPubMedGoogle Scholar
  22. 22.
    Zeitzer JM, Nishino S, Mignot E. The neurobiology of hypocretins (orexins), narcolepsy and related therapeutic interventions. Trends Pharmacol Sci. 2006;27(7):368–74.CrossRefPubMedGoogle Scholar
  23. 23.
    Parmentier R, Kolbaev S, Klyuch BP, Vandael D, Lin JS, Selbach O, et al. Excitation of histaminergic tuberomamillary neurons by thyrotropin-releasing hormone. J Neurosci. 2009;29(14):4471–83.CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Tasneem A, Iyer LM, Jakobsson E, Aravind L. Identification of the prokaryotic ligand-gated ion channels and their implications for the mechanisms and origins of animal Cys-loop ion channels. Genome Biol. 2005;6(1):R4.CrossRefPubMedGoogle Scholar
  25. 25.
    McClintock TS, Ache BW. Histamine directly gates a chloride channel in lobster olfactory receptor neurons. Proc Natl Acad Sci U S A. 1989;86(20):8137–41.CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Hardie RC. A histamine-activated chloride channel involved in neurotransmission at a photoreceptor synapse. Nature. 1989;339(6227):704–6.CrossRefPubMedGoogle Scholar
  27. 27.
    Pantazis A, Segaran A, Liu CH, Nikolaev A, Rister J, Thum AS, et al. Distinct roles for two histamine receptors (hclA and hclB) at the Drosophila photoreceptor synapse. J Neurosci. 2008;28(29):7250–9.CrossRefPubMedGoogle Scholar
  28. 28.
    Haas HL, Sergeeva OA, Selbach O. Histamine in the nervous system. Physiol Rev. 2008;88(3):1183–241.CrossRefPubMedGoogle Scholar
  29. 29.
    Chiel HJ, Weiss KR, Kupfermann I. Multiple roles of a histaminergic afferent neuron in the feeding behavior of Aplysia. Trends Neurosci. 1990;13(6):223–7.CrossRefPubMedGoogle Scholar
  30. 30.
    Chiel HJ, Kupfermann I, Weiss KR. An identified histaminergic neuron can modulate the outputs of buccal-cerebral interneurons in Aplysia via presynaptic inhibition. J Neurosci. 1988;8(1):49–63.PubMedGoogle Scholar
  31. 31.
    Saras A, Gisselmann G, Vogt-Eisele AK, Erlkamp KS, Kletke O, Pusch H, et al. Histamine action on vertebrate GABAA receptors: direct channel gating and potentiation of GABA responses. J Biol Chem. 2008;283(16):10470–5.CrossRefPubMedGoogle Scholar
  32. 32.
    Kletke O, Gisselmann G, May A, Hatt H, A Sergeeva O. Partial agonism of taurine at gamma-containing native and recombinant GABAA receptors. PLoS One. 2013;8(4), e61733.CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Kletke O, Sergeeva OA, Lorenz P, Oberland S, Meier JC, Hatt H, et al. New insights in endogenous modulation of ligand-gated ion channels: histamine is an inverse agonist at strychnine sensitive glycine receptors. Eur J Pharmacol. 2013;710(1–3):59–66.CrossRefPubMedGoogle Scholar
  34. 34.
    Yanovsky Y, Schubring SR, Yao Q, Zhao Y, Li S, May A, et al. Waking action of ursodeoxycholic acid (UDCA) involves histamine and GABAA receptor block. PLoS One. 2012;7(8), e42512.CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Diewald L, Heimrich B, Busselberg D, Watanabe T, Haas HL. Histaminergic system in co-cultures of hippocampus and posterior hypothalamus: a morphological and electrophysiological study in the rat. Eur J Neurosci. 1997;9(11):2406–13.CrossRefPubMedGoogle Scholar
  36. 36.
    Hatton GI, Yang QZ. Ionotropic histamine receptors and H2 receptors modulate supraoptic oxytocin neuronal excitability and dye coupling. J Neurosci. 2001;21(9):2974–82.PubMedGoogle Scholar
  37. 37.
    Lee KH, Broberger C, Kim U, McCormick DA. Histamine modulates thalamocortical activity by activating a chloride conductance in ferret perigeniculate neurons. Proc Natl Acad Sci U S A. 2004;101(17):6716–21.CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Haas HL, Anderson EG, Hosli L. Histamine and metabolites: their effects and interactions with convulsants on brain stem neurons. Brain Res. 1973;51:269–78.CrossRefPubMedGoogle Scholar
  39. 39.
    Lakoski JM, Aghajanian GK, Gallager DW. Interaction of histamine H2-receptor antagonists with GABA and benzodiazepine binding sites in the CNS. Eur J Pharmacol. 1983;88(2–3):241–5.CrossRefPubMedGoogle Scholar
  40. 40.
    Payne GW, Neuman RS. Effects of hypomagnesemia on histamine H1 receptor-mediated facilitation of NMDA responses. Br J Pharmacol. 1997;121(2):199–204.CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Bekkers JM, Stevens CF. NMDA receptors at excitatory synapses in the hippocampus: test of a theory of magnesium block. Neurosci Lett. 1993;156(1–2):73–7.CrossRefPubMedGoogle Scholar
  42. 42.
    Vorobjev VS, Sharonova IN, Walsh IB, Haas HL. Histamine potentiates N-methyl-D-aspartate responses in acutely isolated hippocampal neurons. Neuron. 1993;11(5):837–44.CrossRefPubMedGoogle Scholar
  43. 43.
    Green JP. Histamine and the nervous system. Fed Proc. 1964;23:1095–102.PubMedGoogle Scholar
  44. 44.
    Saybasili H, Stevens DR, Haas HL. pH-dependent modulation of N-methyl-D-aspartate receptor-mediated synaptic currents by histamine in rat hippocampus in vitro. Neurosci Lett. 1995;199(3):225–7.CrossRefPubMedGoogle Scholar
  45. 45.
    Yanovsky Y, Reymann K, Haas HL. pH-dependent facilitation of synaptic transmission by histamine in the CA1 region of mouse hippocampus. Eur J Neurosci. 1995;7(10):2017–20.CrossRefPubMedGoogle Scholar
  46. 46.
    Williams K. Subunit-specific potentiation of recombinant N-methyl-D-aspartate receptors by histamine. Mol Pharmacol. 1994;46(3):531–41.PubMedGoogle Scholar
  47. 47.
    Hansen KB, Mullasseril P, Dawit S, Kurtkaya NL, Yuan H, Vance KM, et al. Implementation of a fluorescence-based screening assay identifies histamine H3 receptor antagonists clobenpropit and iodophenpropit as subunit-selective N-methyl-D-aspartate receptor antagonists. J Pharmacol Exp Ther. 2010;333(3):650–62.CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Faucard R, Armand V, Heron A, Cochois V, Schwartz JC, Arrang JM. N-methyl-D-aspartate receptor antagonists enhance histamine neuron activity in rodent brain. J Neurochem. 2006;98(5):1487–96.CrossRefPubMedGoogle Scholar
  49. 49.
    Ikoma A, Steinhoff M, Stander S, Yosipovitch G, Schmelz M. The neurobiology of itch. Nat Rev Neurosci. 2006;7(7):535–47.CrossRefPubMedGoogle Scholar
  50. 50.
    Koerner P, Hesslinger C, Schaefermeyer A, Prinz C, Gratzl M. Evidence for histamine as a transmitter in rat carotid body sensor cells. J Neurochem. 2004;91(2):493–500.CrossRefPubMedGoogle Scholar
  51. 51.
    Whyment AD, Blanks AM, Lee K, Renaud LP, Spanswick D. Histamine excites neonatal rat sympathetic preganglionic neurons in vitro via activation of H1 receptors. J Neurophysiol. 2006;95(4):2492–500.CrossRefPubMedGoogle Scholar
  52. 52.
    Gorelova N, Reiner PB. Histamine depolarizes cholinergic septal neurons. J Neurophysiol. 1996;75(2):707–14.PubMedGoogle Scholar
  53. 53.
    Uteshev VV, Knot HJ. Somatic Ca(2+) dynamics in response to choline-mediated excitation in histaminergic tuberomammillary neurons. Neuroscience. 2005;134(1):133–43.CrossRefPubMedGoogle Scholar
  54. 54.
    Uteshev VV, Stevens DR, Haas HL. Alpha-bungarotoxin-sensitive nicotinic responses in rat tuberomammillary neurons. Pflugers Arch. 1996;432(4):607–13.CrossRefPubMedGoogle Scholar
  55. 55.
    Smith CC, Greene RW. CNS dopamine transmission mediated by noradrenergic innervation. J Neurosci. 2012;32(18):6072–80.CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Korotkova TM, Haas HL, Brown RE. Histamine excites GABAergic cells in the rat substantia nigra and ventral tegmental area in vitro. Neurosci Lett. 2002;320(3):133–6.CrossRefPubMedGoogle Scholar
  57. 57.
    Zhou FW, Xu JJ, Zhao Y, LeDoux MS, Zhou FM. Opposite functions of histamine H1 and H2 receptors and H3 receptor in substantia nigra pars reticulata. J Neurophysiol. 2006;96(3):1581–91.CrossRefPubMedGoogle Scholar
  58. 58.
    Tabarean IV. Histamine receptor signaling in energy homeostasis. Neuropharmacology. 2015.Google Scholar
  59. 59.
    Liou SY, Shibata S, Yamakawa K, Ueki S. Inhibitory and excitatory effects of histamine on suprachiasmatic neurons in rat hypothalamic slice preparation. Neurosci Lett. 1983;41(1–2):109–13.CrossRefPubMedGoogle Scholar
  60. 60.
    Stehle J. Effects of histamine on spontaneous electrical activity of neurons in rat suprachiasmatic nucleus. Neurosci Lett. 1991;130(2):217–20.CrossRefPubMedGoogle Scholar
  61. 61.
    Scott G, Piggins HD, Semba K, Rusak B. Actions of histamine in the suprachiasmatic nucleus of the Syrian hamster. Brain Res. 1998;783(1):1–9.CrossRefPubMedGoogle Scholar
  62. 62.
    Li Z, Hatton GI. Histamine suppresses non-NMDA excitatory synaptic currents in rat supraoptic nucleus neurons. J Neurophysiol. 2000;83(5):2616–25.PubMedGoogle Scholar
  63. 63.
    Bealer SL, Crowley WR. Histaminergic control of oxytocin release in the paraventricular nucleus during lactation in rats. Exp Neurol. 2001;171(2):317–22.CrossRefPubMedGoogle Scholar
  64. 64.
    Hatton GI, Li ZH. Neurophysiology of magnocellular neuroendocrine cells: recent advances. Prog Brain Res. 1998;119:77–99.CrossRefPubMedGoogle Scholar
  65. 65.
    Haas HL. Histamine: action on single hypothalamic neurones. Brain Res. 1974;76(2):363–6.CrossRefPubMedGoogle Scholar
  66. 66.
    Renaud LP. Histamine microiontophoresis on identified hypothalamic neurons: 3 patterns of response in the ventromedial nucleus of the rat. Brain Res. 1976;115(2):339–44.CrossRefPubMedGoogle Scholar
  67. 67.
    McCormick DA, Williamson A. Modulation of neuronal firing mode in cat and guinea pig LGNd by histamine: possible cellular mechanisms of histaminergic control of arousal. J Neurosci. 1991;11(10):3188–99.PubMedGoogle Scholar
  68. 68.
    Weiler HT, Hasenohrl RU, van Landeghem AA, van Landeghem M, Brankack J, Huston JP, et al. Differential modulation of hippocampal signal transfer by tuberomammillary nucleus stimulation in freely moving rats dependent on behavioral state. Synapse. 1998;28(4):294–301.CrossRefPubMedGoogle Scholar
  69. 69.
    Brown RE, Haas HL. On the mechanism of histaminergic inhibition of glutamate release in the rat dentate gyrus. J Physiol. 1999;515(Pt 3):777–86.CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Brown RE, Reymann KG. Histamine H3 receptor-mediated depression of synaptic transmission in the dentate gyrus of the rat in vitro. J Physiol. 1996;496(Pt 1):175–84.CrossRefPubMedPubMedCentralGoogle Scholar
  71. 71.
    Manahan-Vaughan D, Reymann KG, Brown RE. In vivo electrophysiological investigations into the role of histamine in the dentate gyrus of the rat. Neuroscience. 1998;84(3):783–90.CrossRefPubMedGoogle Scholar
  72. 72.
    Haas H, Panula P. The role of histamine and the tuberomamillary nucleus in the nervous system. Nat Rev Neurosci. 2003;4(2):121–30.CrossRefPubMedGoogle Scholar
  73. 73.
    Bliss TV, Lomo T. Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol. 1973;232(2):331–56.CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Yanovsky Y, Haas HL. Histamine increases the bursting activity of pyramidal cells in the CA3 region of mouse hippocampus. Neurosci Lett. 1998;240(2):110–2.CrossRefPubMedGoogle Scholar
  75. 75.
    Buzsaki G, Draguhn A. Neuronal oscillations in cortical networks. Science. 2004;304(5679):1926–9.CrossRefPubMedGoogle Scholar
  76. 76.
    Selbach O, Brown RE, Haas HL. Long-term increase of hippocampal excitability by histamine and cyclic AMP. Neuropharmacology. 1997;36(11–12):1539–48.CrossRefPubMedGoogle Scholar
  77. 77.
    Haas HL, Konnerth A. Histamine and noradrenaline decrease calcium-activated potassium conductance in hippocampal pyramidal cells. Nature. 1983;302(5907):432–4.CrossRefPubMedGoogle Scholar
  78. 78.
    Chepkova AN, Sergeeva OA, Haas HL. Carbenoxolone impairs LTP and blocks NMDA receptors in murine hippocampus. Neuropharmacology. 2008;55(2):139–47.CrossRefPubMedGoogle Scholar
  79. 79.
    Knoche A, Yokoyama H, Ponomarenko A, Frisch C, Huston J, Haas HL. High-frequency oscillation in the hippocampus of the behaving rat and its modulation by the histaminergic system. Hippocampus. 2003;13(2):273–80.CrossRefPubMedGoogle Scholar
  80. 80.
    Lin JS, Anaclet C, Sergeeva OA, Haas HL. The waking brain: an update. Cell Mol Life Sci. 2011;68(15):2499–512.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Faculty of Medicine, Department of Neuro- and Sensory PhysiologyHeinrich-Heine-University DüsseldorfDüsseldorfGermany
  2. 2.Department of Clinical Neuroscience and Medical PsychologyHeinrich-Heine-University DüsseldorfDüsseldorfGermany

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