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Suprachiasmatic Nucleus Neuropeptide Expression in Patients with Huntington’S Disease Daniel J

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Suprachiasmatic Nucleus Neuropeptide Expression in Patients with Huntington’S Disease Daniel J SUPRACHIASMATIC NUCLEUS IN HUNTINGTON’S DISEASE http://dx.doi.org/10.5665/sleep.2314 Suprachiasmatic Nucleus Neuropeptide Expression in Patients with Huntington’s Disease Daniel J. van Wamelen, MD1,2; N. Ahmad Aziz, MD, PhD2; Jasper J. Anink, BSc1; Robin van Steenhoven, BSc1; Debora Angeloni, PhD3; Franco Fraschini, PhD4; Ralf Jockers, PhD5-7; Raymund A. C. Roos, MD, PhD2; Dick F. Swaab, MD, PhD1 1Netherlands Institute for Neuroscience, an Institute of the Royal Netherlands Academy of Arts and Sciences, Amsterdam, the Netherlands; 2Department of Neurology, Leiden University Medical Center, Leiden, the Netherlands; 3Scuola Superiore Sant’Anna and Institute of Clinical Physiology, Pisa, Italy; 4Department of Medical Biotechnology and Translational Medicine, University of Milano, Milan, Italy; 5Inserm, U1016, Institut Cochin, Paris, France; 6CNRS, UMR 8104, Paris, France; 7Université Paris Descartes, Sorbonne Paris Cite, Paris, France Study Objective: To study whether sleep and circadian rhythm disturbances in patients with Huntington’s disease (HD) arise from dysfunction of the body’s master clock, the hypothalamic suprachiasmatic nucleus. Design: Postmortem cohort study. Patients: Eight patients with HD and eight control subjects matched for sex, age, clock time and month of death, postmortem delay, and fixation time of paraffin-embedded hypothalamic tissue. Measurements and Results: Using postmortem paraffin-embedded tissue, we assessed the functional integrity of the suprachiasmatic nucleus in patients with HD and control subjects by determining the expression of two major regulatory neuropeptides, vasoactive intestinal polypeptide and arginine vasopressin. Additionally, we studied melatonin 1 and 2 receptor expression. Compared with control subjects, the suprachiasmatic nucleus contained 85% fewer neurons immunoreactive for vasoactive intestinal polypeptide and 33% fewer neurons for arginine vasopressin in patients with HD (P = 0.002 and P = 0.027). The total amount of vasoactive intestinal polypeptide and arginine vasopressin messenger RNA was unchanged. No change was observed in the number of melatonin 1 or 2 receptor immunoreactive neurons. Conclusions: These findings indicate posttranscriptional neuropeptide changes in the suprachiasmatic nucleus of patients with HD, and suggest that sleep and circadian rhythm disorders in these patients may at least partly arise from suprachiasmatic nucleus dysfunction. Keywords: Arginine vasopressin, Huntington’s disease, hypothalamus, melatonin receptor, suprachiasmatic nucleus Citation: van Wamelen DJ; Aziz NA; Anink JJ; van Steenhoven R; Angeloni D; Fraschini F; Jockers R; Roos RAC; Swaab DF. Suprachiasmatic nucleus neuropeptide expression in patients with Huntington’s disease. SLEEP 2013;36(1):117-125. INTRODUCTION improve quality of life, but might also ameliorate cognitive and Huntington’s disease (HD) is an autosomal dominant neuro- motor dysfunction.10,11 To test the hypothesis that the biologi- degenerative disorder caused by a CAG repeat expansion in the cal clock is affected in patients with HD, we directly assessed gene encoding the protein huntingtin. Patients characteristical- the functional integrity of the SCN in HD and control brains ly develop motor, cognitive, and behavioral deficits during the by determining the expression of two major regulatory neuro- course of the disease.1 Other features include sleep and circa- peptides, vasoactive intestinal polypeptide (VIP) and arginine 2-4 5,6 dian rhythm disorders and symptoms of cognitive decline, vasopressin (AVP), as well as MT1 and MT2, which are crucial as well as disturbances in peripheral circadian pathways such as for SCN entrainment. the liver’s metabolic cycle.7 These disturbances in intrinsic cir- cadian rhythmicity and a delayed phase position of hormones METHODS such as melatonin and cortisol3,8 suggest a disorder of the en- dogenous biological masterclock, the suprachiasmatic nucleus Postmortem Material (SCN), in patients with HD similar to SCN pathology in the All brain material for patients with HD and control subjects R6/2 transgenic mouse model of HD.8-11 One of the principal was obtained through the Netherlands Brain Bank (NBB) and circadian hormones released under the influence of the SCN is consisted of formalin-fixed, paraffin-embedded hypothalamic melatonin, which in turn has a feedback mechanism on the SCN material (patients with HD n = 8, control subjects n = 8). Control during which its actions are mediated by the melatonin 1 and 2 subjects were matched to patients with HD for sex, age, clock 12,13 receptors (MT1 and MT2). time and month of death, postmortem delay, and fixation time Elucidation of the mechanisms underlying sleep and circa- (Table 1). Different control subjects were used for VIP/AVP dian rhythm disturbances in patients with HD is of great im- and MT1/MT2 analysis when insufficient hypothalamic sections portance because restoration of sleep-wake cycles may not only were available from the same control subject while maintaining adequate matching for the putative confounding factors men- tioned previously. Written informed consent for brain autopsy Submitted for publication November, 2011 as well as for the use of brain material and medical records for Submitted in final revised form July, 2012 research purposes was acquired by the NBB from patients or Accepted for publication August, 2012 their next of kin. This study was approved by the institutional Address correspondence to: DJ van Wamelen, MD, Leiden Univer- review board of the NBB. sity Medical Center, Department of Neurology, Albinusdreef 2, 2333ZA The diagnosis of HD was clinically and neuropathologically Leiden, the Netherlands; Tel: +31715263310; Fax: +31715266971; confirmed in all patients. Additionally, the diagnosis was geneti- E-mail: [email protected] cally confirmed (CAG repeat ≥ 39) in all but one patient (NBB SLEEP, Vol. 36, No. 1, 2013 117 Suprachiasmatic Nucleus in Huntington’s Disease—van Wamelen et al Table 1—Clinicopathologic characteristics of patients with Huntington’s disease and control subjects NBB Sex Age Onset CTD MD PMD Fix CAG Cause of death HD patients 99–108 M 49 40 9:15 8 5:45 49 51 Cachexia 03–047 F 50 35 18:25 6 5:40 55 47 Pneumonia 92–105 M 54 41 9:55 12 3:50 80 ND Sudden death 95–060 M 57 42 3:30 6 7:30 53 46 Cachexia 08–044 M 59 50 18:10 5 5:05 52 44 Legal euthanasia 01–128 M 61 39 10:55 11 10:25 48 43 Pneumonia 98–047 F 67 56 10:10 4 6:05 41 45 Legal euthanasia 99–120 M 79 54 19:00 10 6:15 34 44 Pneumonia Mean 60 45 12:25 8 6:19 52 46 SEM 3 3 1:57 1 0:41 5 1 Control subjects 98–006 (VIP, AVP) M 50 – 11:00 1 8:30 41 – Septic shock 00–090 (MT1, MT2) M 70 – 8:00 7 7:45 34 – Bladder carcinoma 97–127 F 49 – 3:30 4 13:30 165 – Cervix carcinoma 98–027 M 54 – 9:00 12 8:00 59 – Hepatocellular carcinoma 99–141 M 44 – 10:00 7 7:00 149 – Cardiac infarction 98–127 M 56 – 15:45 8 5:25 35 – Cardiac infarction 92–042 (VIP, AVP) M 61 – 21:00 4 13:50 52 – Esophageal carcinoma 97–143 (MT1, MT2) M 79 – 6:10 10 6:00 31 – Prostate carcinoma 98–036 F 69 – 6:15 3 9:25 31 – Cardiogenic shock 93–060 M 79 – 14:00 2 3:00 53 – Leaking aorta prosthesis Mean (VIP, AVP) 58 – 11:18 5 8:35 73 – Mean (MT1, MT2) 63 – 8:30 7 7:22 44 – SEM (VIP, AVP) 4 – 1:57 1 1:18 19 – SEM (MT1, MT2) 5 – 1:27 1 1:05 19 – P value (VIP, AVP) 0.631 – 0.912 0.182 0.201 0.721 – 0.423 0.093 0.673 1 2 2 1 1 P value (MT1, MT2) 0.75 – 0.52 0.89 0.37 0.83 – 0.603 0.403 0.783 a For the respective analyses different control patients had to be used (see (VIP, AVP), (MT1, MT2)) because of a lack of hypothalamic material. Unmarked control patients were used in all analyses. AVP, arginine vasopressin; CAG, mutant Huntingtin CAG repeat length; CTD, clock time of death; F, female; FIX, fixation time (in days); HD, Huntington’s disease; M, male; MD, month of death; MT, melatonin receptor; NA, not assessed; NBB, Netherlands Brain Bank number; PMD, postmortem delay (in hr); SEM, standard error of the mean; VIP, vasoactive intestinal polypeptide; Vonsattel, HD grading according to Vonsattel et al.14; 1Mann-Whitney-U test; 2Mardia–Watson test; 3Wilcoxon signed rank test. 92-105). This patient, however, had a positive family history and mounted on Superfrost Plus slides (Menzel, Braunschweig, the clinical features of HD, as well as a confirmed Vonsattel grade Germany) in four series, one for each neuropeptide or receptor, II HD neuropathology. In Vonsattel grade II and higher grades of and dried for 2 days at 37oC. After deparaffinization and rehy- HD neuropathology, the changes in the caudate nucleus are char- dration, sections for AVP and MT2 were heated by microwave acterized by atrophy, neuronal loss, and fibrillary astrocytosis, oven in citrate buffer pH 4.0 or Tris buffered saline (0.05M Tris whereas the globus pallidus in stage II is still relatively spared.14 and 0.15 M NaCl; pH 7.6), respectively, at 700 W. Sections were Exclusion criteria for control subjects were primary neurologic incubated in either rabbit antihuman-VIP (Netherlands Institute and/or psychiatric disorders and glucocorticoid therapy during for Neuroscience, Amsterdam, the Netherlands) 1:1500, poly- the 2 months before death because glucocorticoids can influence clonal rabbit antihuman-AVP (Netherlands Institute for Neu- 15 the activity of the SCN. Neuroleptic drugs were not considered roscience) 1:800, polyclonal rabbit antihuman-MT1 (provided an exclusion criterion for patients with HD because depletion of by R. Jockers) 1:200 or polyclonal rabbit anti-human-MT2- dopamine has no effect on clock gene expression in the SCN.16 antibody (provided by D.
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