Histamine s Role in Vestibular Function and Recovery
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1 Histamine s Role in Vestibular Function and Recovery Brahim Tighilet Laboratoire de Neurosciences Intégratives et Adaptatives UMR 7260-Fed 3C Physiologie et thérapie des désordres vestibulaires Aix-Marseille Université CNRS, Marseille, France AAO-HNSF Annual Meeting Auris Medical Satellite Symposium Chicago, September, 11 th 2017
2 The vestibular system 3a PIVC Vestibulo-cortical system Cortex Body perception Perception of subjective verticality Spatial and memory navigation Vestibulo-ocular system Thalamus Oculomoteurs nuclei III IV Gaze stabilisation Vestibulo-spinal system Vestibular nuclei Lateral, superior, medial and inferior Scarpa s ganglion Body stabilisation Body orientation Locomotor control Postural Control Spinal cord
3 Vestibular syndrome Perceptivo-cognitive symptoms Spatial disorientation Vertigo 6 3 CVPI Oculomotor symptoms Nystagmus Cyclotorsion Impaired vestibulo-ocular reflex Thalamus Vegetative symptoms Nausea Vomiting Anxiety Vestibular nuclei projections: o Nucleus of the solitary tract o Area postrema o Dorsal nucleus of the vagus o Parabrachial nucleus VN III IV VN Oculomotor nuclei Brainstem Vestibular nerve (VIII) Posturo-locomotor symptoms Ataxia, falls Impaired vestibulo-spinal reflex Increased support surface Spinal cord Unilateral vestibular damage Vestibular receptors (inner ear) From Dutheil et al. 2011
4 Vestibular syndrome Over time, the expression of these vestibular symptoms progressively decreases Vestibular compensation Very good model of adaptive plasticity of the central nervous system but also of vestibular pathology
5 Vestibular loss and electrophysiology of the vestibular nuclei (VN) Cellular level Spontaneous electrical activity - + Deafferented VN Intact VN Deafferented VN Intact VN First week after unilateral lesion Imbalance Compensated stage ( > Day 30) Equilibrium Behavioral level Precht et al. 1966, Zennou-Azogui et al. 1993, Ris et al. 1995, Beraneck 2012
6 Vestibular nuclei reactive plasticity mechanisms in vestibular compensation Immediate early genes and transcription factors Fos et ZiF 268 Tighilet and Lacour 2010 Neurotransmitter system plasticity, changes in neuronal phenotypes Neurones GABAergiques Tighilet and Lacour 1998; Dutheil et al., 2009,2011;2013 Changes in the number of membrane receptors H3, GABAA, NMDA Tighilet et al., 2002,2006,2016 Reactive cell proliferation and neurogenesis Tighilet et al Astrocytic and microglial reactions (Inflammation) IBA1-GFAP-OX42 Dutheil et al., 2009; 2011; 2013; 2016 Modulation of neurotrophic factors BDNF, NGF, NT3 Tighilet et al., 2004; Dutheil et al., 2016 Positive regulation of stress hormones CRF, AVP Tighilet et al., 2009 Synaptic reorganizations Synaptophysine, GAP43 Raymond et al., 1991 Paterson 2006, Gustave dit Duflo 1999, Janssen 1992, Smith 1998, Bolger 1999, Yamanaka 1995, Gliddon 2003, Campos-Torres 2005
7 Neurochemical pathways controlling vestibular functions Neurochemistry of the peripheral vestibular system Soto & Vega 2010 Current Neuropharmacology 8: 26-40
8 Neurochemical pathways controlling vestibular functions Neurochemistry of the central vestibular system Soto & Vega 2010 Current Neuropharmacology 8: 26-40
9 Key role of histaminergic system in vestibular function and recovery The TM nuclei send direct projections to the VN complex The presence of mast cells in the subepithelial connective tissue of the human endolymphatic sac The peripheral, the central vestibular system and the endolymphatic sac contain all types of Histamine receptors H 1, H 2, H 3 and H 4 Vestibular stimulations (rotatory, caloric or galvanic) enhance Histamine release in the hypothalamus and brainstem Histamine induces depolarization of vestibular neurons via H 1 and H 2 receptors
10 Histamine sources Damijana et al 2016 Neuronal histaminergic system: The tuberomamillary nuclei of the posterior hypothalamus Vestibular Nuclei Haas and Panula, Nature reviews neuroscience; 2003
11 Histamine transport and metabolism in neurons Haas and Panula, Nature reviews neuroscience; 2003
12 Histamine receptors Presence of H 1, H 2, H 3 and H 4 receptors in both the central and peripheral vestibular system From Lin,1993
13 Effects of H3 receptor antagonists in vestibular pathology model Behavioural data VN Unilateral vestibular neurectomy (UVN) Oral treatment with Betahistine 50mg/kg (H3R antagonist and partial H1R agonist) or Thioperamide 3,5 mg/kg i.p (pure H3 antagonist) 0 30 Time (days) Pre-operative time Post-operative time Nystagmus Static balance Dynamic balance Immunohistochemistry Histamine antibody (Histaminergic neurons in the TM, HA fibers in the Vestibular nuclei)
14 Effects of H3 receptor antagonists in vestibular pathology model Behavioural data Administration of betahistine and thioperamide after unilateral vestibular neurectomy accelerates the recovery of vestibular functions (posture, dynamic balance and gaze stabilisation) Weak but significant differences were found between betahistine and thioperamide Tighilet et al., 1995; 2007
15 H3 receptor antagonists interaction with the histaminergic system Immunohistochemical data Quantification of histamine immunoreactivity in Hypothalamus TM Vestibular nuclei VN the TM and VN after H3R antagonist treatment Thioperamide 30 µm 300 µm Betahistine and thioperamide treatment significantly reduce histamine immunoreactivity in the vestibular and the TM nuclei probably due to increase in histamine turnover (depletion). Tighilet and Lacour, Eur J Pharmacol, 1997
16 Betahistine interaction with the histaminergic system Molecular data VN Unilateral vestibular neurectomy (UVN) Pre-operative time 0 Oral treatment with Betahistine (50 mg/kg) Post-operative time 1 3 Time (weeks) In situ hybridization and Autoradiography Quantification of the mrna coding for histidine decarboxylase in the TM nuclei Quantification of the H3R binding sites in the TMN and the VN using an H3R agonist Namethyl histamine
17 Betahistine interaction with the histaminergic system Molecular data Nα methylhistamine to H3 receptors HDC m RNA in the TM nuclei TMN VN Betahistine up-regulates HDCm RNA in the TM nuclei Betahistine down regulates the binding density of the agonist Nα methylhistamine to H3 receptors in both the TM and the VN nuclei Tighilet et al, Eur J Pharm, 2002; 2005
18 Betahistine interaction with the histaminergic system Molecular data Betahistine treatment up-regulates HDC m RNA in the TM nuclei Betahistine down regulates the binding density of the agonist Nαmethylhistamine to H3 receptors in both the TM and the VN nuclei Taken together the results demonstrate that betahistine increases histamine turnover (synthesis and release) through blockade of the presynaptic H3 histamine receptors
19 Summary of the cascade of events underlying changes in the histaminergic system after unilateral vestibular lesion HA binding to H1 and H2 receptors induces depolarization of deafferented vestibular neurons Key mechanism of functional vestibular recovery VN H1 VN H2 UVN Electrophysiological asymmetry between homologous VN H3 HA binding to H3 receptors leads to their desensitization, internalization and degradation in the deafferented VN Increased histamine release TM TM Increased histamine synthesis
20 Summary of the cascade of events underlying changes in the histaminergic system after unilateral vestibular lesion and betahistine treatment Bet HA binding to H1 and H2 receptors induces depolarization of deafferented vestibular neurons Key mechanism of functional vestibular recovery H1 VN H2 H1 VN H2 UVN Negative feed back H3 Bet Electrophysiological asymmetry between homologous VN HA binding to H3 receptors leads to their desensitization, internalization and degradation in the deafferented VN Increase histamine release TM TM Increase histamine synthesis
21 Mechanisms of action of betahistine Central Nervous System Increase histamine turnover by blocking the H3R autoreceptor Increase other neurotransmitters turnover by blocking the H3R heteroreceptor Histamine H3R antagonist/inverse agonist Histamine H1R agonist Rebalancing VN activity Brain arousal Synaptic plasticity Long term potentiation Cognitive effects Faster functional recovery Arrang 1985,Tighilet, 2002, Wang and Dutia 1995, Zhang 2013, Li 2017; Brown 2001, Haas and Panula 2003, Brioni 2011, Lin, Haas 2011
22 Mechanisms of action of betahistine Inner ear vascular tree Histamine H3R antagonist Histamine H1R agonist Vascular effects Peripheral level Increased cochlear and vestibular blood flow Central effects Increases the metabolism in the vestibular neurons on the lesioned side Faster vestibular functional recovery Martinez 1972; Laurikainen, 1993, 1998; Dziadziola, 1999; Ihler 2012; Bertlich 2014, 2015
23 Mechanisms of action of betahistine Peripheral Labyrinth Histamine H3R antagonist Histamine H1R agonist Reduces vestibular receptor resting firing rate leading to a decrease in the sensory input from the vestibular endorgans Demonstrated in amphibians but not in mammals Anti-vertigo action Bota 1998, 2001; Chavez 2001; Soto 2001
24 Mechanisms of action of betahistine Endolymphatic sac? Localization of H1, H2, H3 and H4 receptors (mouse, rabbit and humans) Homeostasis of the inner ear Reduce increased endolymphatic pressure and hydrops Dagli, 2008; Møller 2016; Takumida 2016
25 Acknowledgements Thanks for your attention Collaborations Dr. Michel Lacour Jacques Leonard Dr. Suzanne Trottier Dr. Christiane Mourre
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