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Idiopathic Hypersomnia Patients Revealed Longer Circadian Period Length in Peripheral Skin Fibroblasts

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Idiopathic Hypersomnia Patients Revealed Longer Circadian Period Length in Peripheral Skin Fibroblasts ORIGINAL RESEARCH published: 07 June 2018 doi: 10.3389/fneur.2018.00424 Idiopathic Hypersomnia Patients Revealed Longer Circadian Period Length in Peripheral Skin Fibroblasts Linus Materna 1, Hartmut Halfter 1, Anna Heidbreder 1, Matthias Boentert 1, Julian Lippert 2, Raphael Koch 3† and Peter Young 1*† 1 Division of Sleep Medicine and Neuromuscular Disorders, Department of Neurology, University Hospital Muenster, Muenster, Germany, 2 Department of Neurology, Inselspital, University Hospital Bern, University of Bern, Bern, Switzerland, 3 Institute of Biostatistics and Clinical Research, University of Muenster, Muenster, Germany The vast majority of living organisms have evolved a circadian rhythm of roughly 24 h in adaptation to ever-changing environmental conditions, such as the cycle of light and darkness. In some sleep disorders like idiopathic hypersomnia (IH) this adaptation is defective. As the etiology of this disease is largely unknown, we examined the in vitro circadian period length of patients suffering from IH. The patients were diagnosed Edited by: according to the ICSD3-criteria by clinical history, polysomnography (PSG), and multiple Michel Billiard, Hôpital Gui De Chauliac, France sleep latency testing (MSLT). In order to gain insight into the molecular mechanism of Reviewed by: this sleep disorder we collected fibroblasts from skin biopsies of IH patients and healthy Sona Nevsimalova, subjects. We determined the circadian period length of the primary fibroblast cells by Charles University, Czechia lentiviral infection with a construct expressing a luciferase gene under the control of a Liborio Parrino, Università degli Studi di Parma, Italy BMAL1 promoter. The group of IH patients revealed on average a prolonged circadian *Correspondence: period length. In comparison to the group of healthy controls (HC) the mean period length Peter Young was estimated to be 0.82 h (95%-CI 0.44–1.20 h) longer in the patient group. This finding [email protected] further stresses a disturbed regulation of the circadian rhythm in IH patients as part of †These authors have contributed the pathophysiology of this complex and poorly understood primary sleep disorder. equally to this work as senior authors. Keywords: idiopathic hypersomnia, circadian rhythm, circadian period length, clock genes, fibroblasts Specialty section: This article was submitted to Sleep and Chronobiology, INTRODUCTION a section of the journal Frontiers in Neurology According to the recent classification of sleep disorders, central disorders of hypersomnolence Received: 22 March 2018 are subdivided into different categories including narcolepsy with cataplexy (NT1), narcolepsy Accepted: 22 May 2018 without cataplexy (NT2), recurrent hypersomnia (Kleine-Levin-Syndrome, KLS), and idiopathic Published: 07 June 2018 hypersomnia (IH) (1). The key manifestation in all categories is excessive daytime sleepiness. Citation: IH is a primary sleep disorder of not yet finally resolved etiology characterized by a high and Materna L, Halfter H, Heidbreder A, disabling amount of sleep required during the day, despite normal or even prolonged sleep times Boentert M, Lippert J, Koch R and at night. It is a rare disease with an estimated prevalence of 0.5/100.000 people (2, 3). No current Young P (2018) Idiopathic reliable epidemiological data are available due to a lack of any clinical observational studies. The Hypersomnia Patients Revealed Longer Circadian Period Length in symptoms of the disease include extreme difficulties waking up, excessive daytime sleepiness (EDS) Peripheral Skin Fibroblasts. with extensive, mostly involuntary and unrefreshing daytime naps in addition to problems with Front. Neurol. 9:424. concentration and prominent mood disturbances. Sleep drunkenness, sleep inertia, and hypnagogic doi: 10.3389/fneur.2018.00424 hallucinations are also frequently reported (4). Frontiers in Neurology | www.frontiersin.org 1 June 2018 | Volume 9 | Article 424 Materna et al. Circadian Period Length in Idiopathic Hypersomnia Disease onset occurs most often during adolescence or young population the circadian period length is on average τ = 24.3h adulthood and is accompanied by severe social and economic (17), which is slightly longer than the duration of the actual day, impairments for the patients, resulting in a great loss in the making the process of entrainment necessary. patient’s quality of life. Currently there is no admitted medical The length of the circadian period of the cells can be treatment for IH. However, a recent double-blind, placebo- monitored using a lentiviral bioluminescence assay (18, 19).Ithas controlled study suggests Modafinil might be efficacious in been demonstrated that fibroblasts from subjects with different treating IH patients (5). chronotypes displayed different circadian period lengths (20, Sleep regulation seems to be disturbed in patients suffering 21), indicating a connection between the daytime preference or from IH (6, 7). This might be due to a pathologically high sleep diurnal pattern of activity and the endogenous circadian period pressure, a lack of an adequate homeostatic antagonist or the of the subject. malfunctioning of the underlying circadian process. Reports of We have recently shown that the mRNA expression of several distinctive HLA markers have been inconsistent (8). A series of clock genes was impaired in fibroblast cells from IH patients 138 patients with IH found that the prevalence of inflammatory compared to healthy controls (HC) (22). We hypothesized that disorders, allergies, and the incidence of family members with the excessive sleepiness seen in IH patients partly results from inflammatory disorders was increased in patients compared with an altered circadian rhythm. To answer this, we investigated the controls (9). circadian period length in isolated dermal fibroblast cells from Concerning the pathophysiology of IH, one study suggested patients suffering from IH and compared them to cells from that an un-specified endogenous substance in the cerebrospinal healthy volunteers to gain further insight into the sleep and wake fluid of some patients with primary hypersomnia, including regulation at the molecular level. IH, might enhance inhibitory signaling through gamma- aminobutyric acid type A (GABAA) receptors, thereby MATERIALS AND METHODS promoting sleepiness. The effects were reversed in vitro by flumazenil, which also normalized vigilance in seven patients Study Patients and Controls in vivo (10). A pilot study from the same group found that All procedures, consent forms and questionnaires were approved clarithromycin as a GABAA affecting drug improved subjective by the Medical Ethical Committee of the University Muenster sleepiness without improving objective signs of alertness in (ref.-no.: 2009-361-f-S, renewed 08/05/2017). All patients and patients with evidence of abnormal GABAA potentiation (11). controls gave signed written informed consent. In contrast, a separate study could not confirm in vitro GABAA Fifteen patients suffering from IH were consecutively potentiation with cerebrospinal fluid from 15 patients with IH recruited from the Department of Neurology, Division of Sleep (12). Hypocretin-1, the wake-promoting neurotransmitter that is Medicine and Neuromuscular Diseases at the University Hospital absent or deficient in patients with narcolepsy type 1, is normal Muenster. Diagnosis was made according to standard criteria in patients with IH (13, 14). Findings about the contribution of the ICSD-3 (1) as described recently (23). The Epworth of the monoaminergic transmitter system and central acting Sleepiness Score (ESS) to assess subjective daytime sleepiness substances are inconsistent. Therefore a malfunctioning of (24) had to be above 10 and the Horne-Ostberg (HO) score the underlying circadian system should be considered as an was evaluated by the self-assessment HO questionnaire (25). alternative cause of IH. All patients underwent polysomnography (PSG) for at least one Numerous autonomous circadian clocks can be found in night to prove high sleep efficiency, followed by a Multiple nearly all different tissues of the body, coordinated by a central Sleep Latency Test (MSLT). MSLT had to be below 8 min on master clock located in the hypothalamus–the suprachiasmatic average with less than 2 Sleep Onset REM Episodes (SOREM), nucleus (SCN). The SCN integrates the information about so no 24 h PSG had to be conducted. Sleep efficiency had to be exogenous factors such as light and then orchestrates the activity above 85%. Patients with comorbid psychiatric or neurological of the circadian oscillators in peripheral tissues via systemic and disorders, as well as other disorders explaining EDS including endocrine signals. Thereby the SCN adjusts the physiological obesity (BMI > 35 kg/m2) were excluded. Cerebrospinal fluid processes by which the organism responds to and anticipates the (CSF) investigation was performed in all patients to exclude other diurnal requirements and thus resets the internal clock every day. central causes for sleepiness (for example, chronic inflammatory This process is called “entrainment.” disorders) and to exclude hypocretin deficiency. Within the cell, the molecular mechanism underlying the Sixteen HC, unrelated to the patients, were included. course of the circadian rhythms has been identified as a feedback mechanism that involves transcriptional, translational and post- Cell Culture of Human Fibroblasts translational cycles of clock genes and their products (15). At Establishing of fibroblast
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