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Melatonin Rhythmicity: Effect of Age and Alzheimer's

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Melatonin Rhythmicity: Effect of Age and Alzheimer's Age-related changes in circadian factors and light interventions in healthy and pathological human ageing Debra J. SKENE Chronobiology University of Surrey, Guildford, UK [email protected] Metabolomics • better understanding of circadian and sleep/wake regulation of metabolism • Powerful tool to elucidate mechanisms linking sleep restriction, circadian misalignment and metabolic disturbances - peripheral clock phase/function during circadian misalignment - biomarkers to track sleep and circadian disruption; and monitor recovery Age-related changes in circadian factors and light interventions in healthy and pathological human ageing Debra J. SKENE Chronobiology University of Surrey, Guildford, UK [email protected] 2 process model Borbély, A. A.Hum.Neurobiol., 1982 Daan, S., Beersma, D. G. M. and Borbély, A.A. Am. J.Physiol., 1984 Human circadian timing system Human circadian timing system Circadian rhythms Effect of ageing Treatment strategies - melatonin, light - in ageing Challenges Circadian rhythms and ageing research? Only measure clock outputs (eg melatonin, rest/activity) Confounded – field studies Cross-sectional, rarely longitudinal Older people - medication/mobility issues Participant numbers 7 care homes in south-east England Total number of residents = 256 Suitable = 131 Not suitable = 125 (51%) (49%) No = 51 Yes = 80 (39%) (61%) Wearing AWL = 73 In analysis = 48 (91%) (66%) Hopkins, S. et al. Current Alz. Res 2017 Not a homogenous group n = 80 Mobility Fully mobile 20% Walking stick 11% Walking frame 16% Wheelchair 53% MMSE score 27 – 30, no impairment 13% 21 – 26, mild 26% 11 – 20, moderate 53% 0 – 10, severe 8% 8 registered blind (2NLP; 6 LP) Hopkins, S. et al. Current Alz. Res 2017 24h activity profiles (7 days) (A) (B) (C) (D) (E) Hourly activity counts mean ± SEM A + C = fully mobile B + D = wheelchair E = walking frame Hopkins, S. et al. Current Alz. Res 2017 Challenges Circadian rhythms and ageing research? Only measure clock outputs (eg melatonin, rest/activity) Confounded – field studies The suprachiasmatic nuclei (SCN) of the hypothalamus Site of circadian oscillator Courtesy of Dr Michael Hastings The Clock in the Brain Hz A5 2 0 B7b 4 0 D1 3 0 G3b 4 0 24 48 72 Time (hours) Welsh, Logothetis, Meister & Reppert, Nature 1995 Courtesy of Till Roenneberg Retina-SCN-PVN-SCG-pineal pathway Stehle, J.H., et al. 2011 SCN rhythmicity drives melatonin rhythm Entrained to 24 h by light/dark via the retina-RHT pathway (Retina)-SCN-PVN-HPA axis Courtesy of Andries Kalsbeek (Retina)-SCN-PVN-ANS Courtesy of Andries Kalsbeek SCN-driven melatonin and cortisol rhythms in constant routine conditions males n = 14 Gunn et al., 2016 Confounders • Light/dark cycle • Sleep/wake cycle • Activity/exercise • Drugs • Food • Posture • Stress • Menstrual cycle? Challenges in measurement Diurnal versus circadian rhythms Diurnal – exogenous and endogenous Rhythms may be influenced, or even driven, by environmental cycles Circadian – endogenous Rhythms driven by endogenous timing mechanisms (“clocks”) persist in constant conditions Early “Clock” Experiments DAYTIME NIGHT TIME Leaves are open Leaves are closed Mimosa pudica de Marian, 1729 Diurnal versus circadian rhythms the constant routine protocol • Designed to remove/minimise effects of external environment and behaviour (e.g. sleep) • No knowledge of clock time • Constant dim light • Semi-recumbent posture • Minimal social interaction • Regular (e.g. hourly) small isocaloric snacks Human circadian rhythms - endogenously generated persist in constant conditions • Melatonin • Cortisol • Rectal temperature • Activity • Sleep • Mood • Performance Circadian rhythms melatonin core body temp subjective alertness task performance triacylglycerol Rajaratnam &Arendt 2001 Constant routine protocol versus entrained diurnal sleep/wake Czeisler & Klerman 1999 Recent Prog Horm Res 54:97-132 Melatonin as a reliable marker of circadian phase • unaffected by: meals, stress, bathing, sleep • dim light conditions (< 8 lux) • exclude drugs • control posture, exercise Markers of the melatonin rhythm used to characterise the timing of the circadian clock 80 duration 70 ) l m / 60 g p acrophase (calculated peak time) ( * 50 n i n o t 40 a l e m 30 mid-range crossing a * * m 20 s a 25% rise/fall l p 10 * * onset/offset * * 0 1500 1700 1900 2100 2300 100 300 500 700 900 1100 1300 1500 1700 clock time (h) ‘biological night’ Arendt & Skene, Sleep Medicine Reviews (2005) 9:25-39 Benloucif et al., 2007 SCN extra-SCN brain oscillators peripheral clocks • synchrony between different internal rhythms • synchrony between internal rhythms and external cycles e.g. for diurnal animals: sleep at night, visual function and metabolic responses optimal in the day Diagnosis Measures used to assess - human circadian timing system - SCN-driven rhythms (melatonin, cortisol) - Markers of peripheral clocks? Human peripheral clocks • Buccal tissue (Cajochen et al., 2006) • Blood cells (Archer et al., 2008; O’Neill and Reddy, 2011; Ackermann et al., 2013) • Skin fibroblasts (Brown et al., 2005; 2008) • Hair follicles (Akashi et al., 2010) • Adipose tissue (Otway et al., 2011) • Skeletal muscle (van Moorsel et al., 2016) SCN extra-SCN brain oscillators peripheral clocks Markers of human peripheral clocks? Plasma metabolome Blood cells, buccal tissue, skin fibroblasts, hair follicles, adipose tissue, muscle Skene et al., PNAS, 2018 Effects of Prior Simulated Shift Work on Metabolite Rhythms (Examples) Sphingolipid SM C20:2 24/27 (89%) had significantly shifted (reversed) rhythms Skene et al., PNAS, 2018 Conclusions • Rhythms in most metabolites dissociated from the SCN pacemaker rhythm • Vast majority aligning with the preceding sleep/wake and feeding/fasting cycles • Metabolic profiling (metabolomics) in plasma may provide a window onto peripheral clocks and the biobehavioral factors orchestrating them Skene et al., PNAS, 2018 Pathways of peripheral clock entrainment From Mohawk et al. Annu. Rev. Neurosci. 2012 Human circadian timing system Human circadian timing system Circadian rhythms Effect of ageing Possible causes of age-related changes in circadian system Possible causes of age-related changes in circadian system Output pathway RHT Pineal SCN PVN SCG Gland Input pathway cortisol temperature sleep/wake melatonin ? ? ? ? Output pathway RHT Pineal SCN PVN SCG Gland Input pathway cortisol temperature sleep/wake melatonin Possible causes of age-related changes in circadian system 1. Clock disturbance 2. Entrainment abnormalities 3. Insufficient zeitgebers (time cues) Biological rhythms t Period Phase f f Amplitude Salivary Melatonin Levels (pg/ml) 18 21 12 15 0 3 6 9 12 12 16 20 24 4 8 12 16 20 24 4 8 12 Circadian Terminology Clock Hour T Courtesy Ken Wright Courtesy Ken phase angle phase bedtime Amplitude Mesor Mean Age-related changes 1. Amplitude 2. Period 3. Phase 4. Phase angle of entrainment 5. Response to light Phase angle of entrainment = phase relationship between a circadian rhythm and the environmental signal entraining the rhythm (e.g. light-dark cycle; sleep onset) Duffy et al., Sleep Med. Clin. , 2016 Possible causes of age-related changes in circadian system 1. Clock disturbance Output pathway RHT Pineal SCN PVN SCG Gland Input pathway cortisol temperature sleep/wake melatonin Reduced amplitude 1. Clock disturbance Human SCN - reduced number of vasopressin neurons - reduced amplitude of rhythm - alterations in the neural and temporal organization of the SCN Hofman and Swaab, 1988; review 2006 Hofman and Swaab, 1988; review 2006 Age-related changes in melatonin - reduced melatonin amplitude Plasma melatonin Waldhauser et al., 1988 Urinary 6-sulphatoxymelatonin (aMT6s) Bojkowski and Arendt, 1990 Pre- and postmenopausal women (n=160) Skene et al., 1990 Pineal melatonin - human postmortem tissue Skene et al., 1990 Melatonin in CSF Liu et al., 1999 Possible causes of age-related changes in circadian system Output pathway RHT Pineal SCN PVN SCG Gland Input pathway cortisol temperature sleep/wake melatonin Concretions, reduced sympathetic innervation, b-receptor changes, reduced NAT Age-related changes in melatonin - reduced melatonin production/amplitude most studies (diurnal, entrained) Constant routine study 65+ Elderly- disease and drug free Dim light, semi-recumbent, sleep deprived, isocaloric meals Zeitzer et al., 1999 Possible causes of age-related changes in circadian system 1. Clock disturbance 2. Entrainment abnormalities Output pathway RHT Pineal SCN PVN SCG Gland Input pathway cortisol temperature sleep/wake melatonin Reduced amplitude Phase advance of circadian rhythms Age-related change in circadian period? Explain phase advance of circadian rhythms i.e shorter period as age? Human circadian period (t) Forced desynchrony n = 11 young Sighted n = 13 old t = 24.18 ± 0.02 h Czeisler et al., Science, 1999 aMT6s Period and Age Totally blind 25 24.9 Real life 24.8 24.7 24.6 aMT6s 24.5 tau (h) 24.4 24.3 24.2 24.1 r = -0.02 24 n = 23 23.9 0 10 20 30 40 50 60 70 80 Age (yrs) Skene et al., unpublished Age-related changes in melatonin 1. decreased melatonin production - decline in amplitude 2. phase advance of melatonin rhythm aMT6s acrophase mean ± SD 6 7 0 1 2 3 4 5 16-20 Earlier aMT6s peak time ageing Earlier with aMT6s 18 83 18 13 4 136 n 136 4 13 18 83 18 21-30 31-40 41-50 51-60 61-70 Englishunpublishedal.,et 71-81 16-81 years Older compared to young adults Earlier wrt clock time Later wrt to biological time i.e. sleep/darkness solid line - older group Duffy et al., Sleep Med.
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