Insulin-like growth factor I modulates sleep through hypothalamic orexin neurons.
IGF-I
orexin neurons
sleep
Journal
FASEB journal : official publication of the Federation of American Societies for Experimental Biology
ISSN: 1530-6860
Titre abrégé: FASEB J
Pays: United States
ID NLM: 8804484
Informations de publication
Date de publication:
12 2020
12 2020
Historique:
received:
21
05
2020
revised:
30
08
2020
accepted:
21
09
2020
pubmed:
19
10
2020
medline:
24
4
2021
entrez:
18
10
2020
Statut:
ppublish
Résumé
Although sleep disturbances are common co-morbidities of metabolic diseases, the underlying processes linking both are not yet fully defined. Changes in the duration of sleep are paralleled by changes in the levels of insulin-like growth factor-I (IGF-I), an anabolic hormone that shows a circadian pattern in the circulation and activity-dependent entrance in the brain. However, the specific role, if any, of IGF-I in this universal homeostatic process remains poorly understood. We now report that the activity of orexin neurons, a discrete cell population in the lateral hypothalamus that is involved in the circadian sleep/wake cycle and arousal, is modulated by IGF-I. Furthermore, mice with blunted IGF-I receptor activity in orexin neurons have lower levels of orexin in the hypothalamus, show altered electro-corticographic patterns with predominant slow wave activity, and reduced onset-sleep latency. Collectively, these results extend the role in the brain of this pleiotropic growth factor to shaping sleep architecture through the regulation of orexin neurons. We speculate that poor sleep quality associated to diverse conditions may be related to disturbed brain IGF-I input to orexin neurons.
Identifiants
pubmed: 33070417
doi: 10.1096/fj.202001281RR
doi:
Substances chimiques
Orexins
0
Insulin-Like Growth Factor I
67763-96-6
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
15975-15990Informations de copyright
© 2020 Federation of American Societies for Experimental Biology.
Références
Arrigoni E, Chee MJS, Fuller PM. To eat or to sleep: that is a lateral hypothalamic question. Neuropharmacology. 2019;154:34-49.
Rutter J, Reick M, McKnight SL. Metabolism and the control of circadian rhythms. Annu Rev Biochem. 2002;71:307-331.
Van CE, Plat L, Copinschi G. Interrelations between sleep and the somatotropic axis. Sleep. 1998;21:553-566.
Kern W, Halder R, al-Reda S, Spath-Schwalbe E, Fehm HL, Born J. Systemic growth hormone does not affect human sleep. J Clin Endocrinol Metab. 1993;76:1428-1432.
Steiger A, Guldner J, Hemmeter U, Rothe B, Wiedemann K, Holsboer F. Effects of growth hormone-releasing hormone and somatostatin on sleep EEG and nocturnal hormone secretion in male controls. Neuroendocrinology. 1992;56:566-573.
Ziegenbein M, Held K, Kuenzel HE, Murck H, Antonijevic IA, Steiger A. The somatostatin analogue octreotide impairs sleep and decreases EEG sigma power in young male subjects. Neuropsychopharmacology. 2004;29:146-151.
Obal F Jr, Kapas L, Gardi J, Taishi P, Bodosi B, Krueger JM. Insulin-like growth factor-1 (IGF-1)-induced inhibition of growth hormone secretion is associated with sleep suppression. Brain Res. 1999;818:267-274.
Prinz PN, Moe KE, Dulberg EM, et al. Higher plasma IGF-1 levels are associated with increased delta sleep in healthy older men. J Gerontol A Biol Sci Med Sci. 1995;50:M222-M226.
Ashlin TG, Blunsom NJ, Ghosh M, Cockcroft S, Rihel J. Pitpnc1a regulates zebrafish sleep and wake behavior through modulation of insulin-like growth factor signaling. Cell Rep. 2018;24:1389-1396.
Skora S, Mende F, Zimmer M. Energy scarcity promotes a brain-wide sleep state modulated by insulin signaling in C. elegans. Cell Rep. 2018;22:953-966.
Monyak RE, Emerson D, Schoenfeld BP, et al. Insulin signaling misregulation underlies circadian and cognitive deficits in a Drosophila fragile X model. Mol Psychiatry. 2017;22:1140-1148.
Chennaoui M, Arnal PJ, Dorey R, et al. Changes of cerebral and/or peripheral adenosine A(1) receptor and IGF-I concentrations under extended sleep duration in rats. Int J Mol Sci. 2017;18.
Chennaoui M, Arnal PJ, Drogou C, Sauvet F, Gomez-Merino D. Sleep extension increases IGF-I concentrations before and during sleep deprivation in healthy young men. Appl Physiol Nutr Metab. 2016;41:963-970.
Monico-Neto M, Dattilo M, Ribeiro DA, et al. REM sleep deprivation impairs muscle regeneration in rats. Growth Factors. 2017;35:12-18.
de Lecea L, Kilduff TS, Peyron C, et al. The hypocretins: hypothalamus-specific peptides with neuroexcitatory activity. Proc Natl Acad Sci U S A. 1998;95:322-327.
Sakurai T, Amemiya A, Ishii M, et al. Orexins and orexin receptors: a family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior. Cell. 1998;92:573-585.
Sakurai T. The neural circuit of orexin (hypocretin): maintaining sleep and wakefulness. Nat Rev Neurosci. 2007;8:171-181.
Kotz CM. Integration of feeding and spontaneous physical activity: role for orexin. Physiol Behav. 2006;88:294-301.
Sakurai T. The role of orexin in motivated behaviours. Nat Rev Neurosci. 2014;15:719-731.
Honda M, Eriksson KS, Zhang S, et al. IGFBP3 colocalizes with and regulates hypocretin (orexin). PLoS One. 2009;4:e4254.
Alam MN, Gong H, Alam T, Jaganath R, McGinty D, Szymusiak R. Sleep-waking discharge patterns of neurons recorded in the rat perifornical lateral hypothalamic area. J Physiol. 2002;538:619-631.
Koyama Y, Takahashi K, Kodama T, Kayama Y. State-dependent activity of neurons in the perifornical hypothalamic area during sleep and waking. Neuroscience. 2003;119:1209-1219.
Sakurai T, Nagata R, Yamanaka A, et al. Input of orexin/hypocretin neurons revealed by a genetically encoded tracer in mice. Neuron. 2005;46:297-308.
Carro E, Nunez A, Busiguina S, Torres-Aleman I. Circulating insulin-like growth factor I mediates effects of exercise on the brain. J Neurosci. 2000;20:2926-2933.
Nishijima T, Piriz J, Duflot S, et al. Neuronal activity drives localized blood-brain-barrier transport of serum insulin-like growth factor-I into the CNS. Neuron. 2010;67:834-846.
Chaudhari A, Gupta R, Patel S, Velingkaar N, Kondratov R. Cryptochromes regulate IGF-1 production and signaling through control JAK2 dependent STAT5B phosphorylation. Mol Biol Cell. 2017;28:834-842.
Crosby P, Hamnett R, Putker M, et al. Insulin/IGF-1 drives PERIOD synthesis to entrain circadian rhythms with feeding time. Cell. 2019;177:896-909.e20.
Breit A, Miek L, Schredelseker J, Geibel M, Merrow M, Gudermann T. Insulin-like growth factor-1 acts as a zeitgeber on hypothalamic circadian clock gene expression via glycogen synthase kinase-3beta signalling. J Biol Chem. 2018;293:17278-17290.
Matsuki T, Nomiyama M, Takahira H, et al. Selective loss of GABA(B) receptors in orexin-producing neurons results in disrupted sleep/wakefulness architecture. Proc Natl Acad Sci U S A. 2009;106:4459-4464.
Zink AN, Bunney PE, Holm AA, Billington CJ, Kotz CM. Neuromodulation of orexin neurons reduces diet-induced adiposity. Int J Obes (Lond). 2018;42:737-745.
Stanojlovic M, Pallais Yllescas JP Jr., Mavanji V, Kotz C. Chemogenetic activation of orexin/hypocretin neurons ameliorates aging-induced changes in behavior and energy expenditure. Am J Physiol Regul Integr Comp Physiol. 2019;316:R571-R583.
Xuan S, Kitamura T, Nakae J, et al. Defective insulin secretion in pancreatic beta cells lacking type 1 IGF receptor. J Clin Invest. 2002;110:1011-1019.
Kappeler L, De Magalhaes Filho CM, Dupont J, et al. Brain IGF-1 receptors control mammalian growth and lifespan through a neuroendocrine mechanism. PLoS Biol. 2008;6:e254.
Cardin JA, Carlen M, Meletis K, et al. Targeted optogenetic stimulation and recording of neurons in vivo using cell-type-specific expression of Channelrhodopsin-2. Nat Protoc. 2010;5:247-254.
Aravanis AM, Wang LP, Zhang F, et al. An optical neural interface: in vivo control of rodent motor cortex with integrated fiberoptic and optogenetic technology. J Neural Eng. 2007;4:S143-156.
Martinez-Rachadell L, Aguilera A, Perez-Domper P, Pignatelli J, Fernandez AM, Torres-Aleman I. Cell-specific expression of insulin/insulin-like growth factor-I receptor hybrids in the mouse brain. Growth Horm IGF Res. 2019;45:25-30.
Guez-Barber D, Fanous S, Harvey BK, et al. FACS purification of immunolabeled cell types from adult rat brain. J Neurosci Methods. 2012;203:10-18.
Franco C, Genis L, Navarro JA, et al. A role for astrocytes in cerebellar deficits in frataxin deficiency: protection by insulin-like growth factor I. Mol Cell Neurosci. 2017;80:100-110.
Blair LA, Bence-Hanulec KK, Mehta S, Franke T, Kaplan D, Marshall J. Akt-dependent potentiation of L channels by insulin-like growth factor- 1 is required for neuronal survival. J Neurosci. 1999;19:1940-1951.
Carter ME, Brill J, Bonnavion P, Huguenard JR, Huerta R, de Lecea L. Mechanism for Hypocretin-mediated sleep-to-wake transitions. Proc Natl Acad Sci U S A. 2012;109:E2635-E2644.
Tortorella S, Rodrigo-Angulo ML, Nunez A, Garzon M. Synaptic interactions between perifornical lateral hypothalamic area, locus coeruleus nucleus and the oral pontine reticular nucleus are implicated in the stage succession during sleep-wakefulness cycle. Front Neurosci. 2013;7:216.
Trueba-Sáiz, A., Cavada, C., Fernandez, A. et al. Loss of serum IGF-I input to the brain as an early biomarker of disease onset in Alzheimer mice. Transl Psychiatry. 2013;3:e330. https://doi.org/10.1038/tp.2013.102.
Adamantidis AR, Zhang F, Aravanis AM, Deisseroth K, de Lecea L. Neural substrates of awakening probed with optogenetic control of hypocretin neurons. Nature. 2007;450:420-424.
Karnani MM, Schöne C, Bracey EF, et al. Role of spontaneous and sensory orexin network dynamics in rapid locomotion initiation. Prog Neurobiol. 2020;187:101771.
Grubbs JJ, Lopes LE, van der Linden AM, Raizen DM. A salt-induced kinase is required for the metabolic regulation of sleep. PLoS Biol. 2020;18:e3000220.
Herrera CG, Ponomarenko A, Korotkova T, Burdakov D, Adamantidis A. Sleep & metabolism: the multitasking ability of lateral hypothalamic inhibitory circuitries. Front Neuroendocrinol. 2017;44:27-34.
Burdakov D, Gerasimenko O, Verkhratsky A. Physiological changes in glucose differentially modulate the excitability of hypothalamic melanin-concentrating hormone and orexin neurons in situ. J Neurosci. 2005;25:2429-2433.
Karnani MM, Apergis-Schoute J, Adamantidis A, et al. Activation of central orexin/hypocretin neurons by dietary amino acids. Neuron. 2011;72:616-629.
Zegarra-Valdivia JA, Santi A, Fernandez de Sevilla ME, Nunez A, Torres Aleman I. Serum insulin-like growth factor I deficiency associates to Alzheimer's disease co-morbidities. J Alzheimers Dis. 2019;69:979-987.
Metaxakis A, Tain LS, Gronke S, et al. Lowered insulin signalling ameliorates age-related sleep fragmentation in Drosophila. PLoS Biol. 2014;12:e1001824.
Tsuneki H, Wada T, Sasaoka T. Chronopathophysiological implications of orexin in sleep disturbances and lifestyle-related disorders. Pharmacol Ther. 2018;186:25-44.
Chemelli RM, Willie JT, Sinton CM, et al. Narcolepsy in orexin knockout mice: molecular genetics of sleep regulation. Cell. 1999;98:437-451.
Nishino S, Ripley B, Overeem S, Lammers GJ, Mignot E. Hypocretin (orexin) deficiency in human narcolepsy. Lancet. 2000;355:39-40.
Hara J, Beuckmann CT, Nambu T, et al. Genetic ablation of orexin neurons in mice results in narcolepsy, hypophagia, and obesity. Neuron. 2001;30:345-354.
Bastianini S, Silvani A, Berteotti C, Lo Martire V, Zoccoli G. High-amplitude theta wave bursts during REM sleep and cataplexy in hypocretin-deficient narcoleptic mice. J Sleep Res. 2012;21:185-188.
Lee MG, Hassani OK, Jones BE. Discharge of identified orexin/hypocretin neurons across the sleep-waking cycle. J Neurosci. 2005;25:6716-6720.
Mileykovskiy BY, Kiyashchenko LI, Siegel JM. Behavioral correlates of activity in identified hypocretin/orexin neurons. Neuron. 2005;46:787-798.
Peyron C, Tighe DK, van den Pol AN, et al. Neurons containing hypocretin (orexin) project to multiple neuronal systems. J Neurosci. 1998;18:9996-10015.
Thannickal TC, Moore RY, Nienhuis R, et al. Reduced number of hypocretin neurons in human narcolepsy. Neuron. 2000;27:469-474.
Sakurai T, Mieda M. Connectomics of orexin-producing neurons: interface of systems of emotion, energy homeostasis and arousal. Trends Pharmacol Sci. 2011;32:451-462.
Mander BA, Winer JR, Walker MP. Sleep and human aging. Neuron. 2017;94:19-36.
Cipriani G, Lucetti C, Danti S, Nuti A. Sleep disturbances and dementia. Psychogeriatrics. 2015;15:65-74.
Ju YE, Lucey BP, Holtzman DM. Sleep and Alzheimer disease pathology-a bidirectional relationship. Nat Rev Neurol. 2014;10:115-119.
Wennberg A, Lorusso R, Dassie F, et al. Sleep disorders and cognitive dysfunction in acromegaly. Endocrine. 2019;66:634-641.
Breese CR, Ingram RL, Sonntag WE. Influence of age and long-term dietary restriction on plasma insulin- like growth factor-1 (IGF-1), IGF-1 gene expression, and IGF-1 binding proteins. J Gerontol. 1991;46:B180-B187.
Muller AP, Fernandez AM, Haas C, Zimmer E, Portela LV, Torres-Aleman I. Reduced brain insulin-like growth factor I function during aging. Mol Cell Neurosci. 2012;49:9-12.
Kessler BA, Stanley EM, Frederick-Duus D, Fadel J. Age-related loss of orexin/hypocretin neurons. Neuroscience. 2011;178:82-88.
Swaab DF, Fliers E, Partiman TS. The suprachiasmatic nucleus of the human brain in relation to sex, age and senile dementia. Brain Res. 1985;342:37-44.
van Oostrom SH, Nooyens ACJ, van Boxtel MPJ, Verschuren WMM. Long sleep duration is associated with lower cognitive function among middle-age adults - the Doetinchem Cohort Study. Sleep Med. 2018;41:78-85.
Sindi S, Kareholt I, Johansson L, et al. Sleep disturbances and dementia risk: a multicenter study. Alzheimers Dement. 2018;14:1235-1242.
Hung CM, Li YC, Chen HJ, et al. Risk of dementia in patients with primary insomnia: a nationwide population-based case-control study. BMC Psychiatry. 2018;18:38.
Larsson SC, Wolk A. The role of lifestyle factors and sleep duration for late-onset dementia: a cohort study. J Alzheimers Dis. 2018;66:579-586.
Chen JC, Espeland MA, Brunner RL, et al. Sleep duration, cognitive decline, and dementia risk in older women. Alzheimers Dement. 2016;12:21-33.
Carro E, Torres-Aleman I. The role of insulin and insulin-like growth factor I in the molecular and cellular mechanisms underlying the pathology of Alzheimer's disease. Eur J Pharmacol. 2004;490:127-133.
Talbot K, Wang HY, Kazi H, et al. Demonstrated brain insulin resistance in Alzheimer's disease patients is associated with IGF-1 resistance, IRS-1 dysregulation, and cognitive decline. J Clin Invest. 2012;122:1316-1338.
Venner A, Anaclet C, Broadhurst RY, Saper CB, Fuller PM. A Novel population of wake-promoting GABAergic neurons in the ventral lateral hypothalamus. Curr Biol. 2016;26:2137-2143.
McGregor R, Shan L, Wu MF, Siegel JM. Diurnal fluctuation in the number of hypocretin/orexin and histamine producing: Implication for understanding and treating neuronal loss. PLoS ONE. 2017;12:e0178573.
Date Y, Mondal MS, Matsukura S, et al. Distribution of orexin/hypocretin in the rat median eminence and pituitary. Mol Brain Res. 2000;76:1-6.