Disrupted nocturnal melatonin in autism: Association with tumor necrosis factor and sleep disturbances.

Tytuł:: Disrupted nocturnal melatonin in autism: Association with tumor necrosis factor and sleep disturbances.
Autorzy:: da Silveira Cruz-Machado S; Laboratory of Chronopharmacology, Department of Physiology, Institute of Biosciences, University of São Paulo (USP), São Paulo, Brazil.
Guissoni Campos LM; Department of Anatomy, School of Medicine, University of Marilia (UNIMAR), Marília, Brazil.
Fadini CC; Department of Speech, Language and Hearing Sciences, São Paulo State University (UNESP), Marilia, Brazil.
Anderson G; CRC Scotland & London, London, UK.
Markus RP; Laboratory of Chronopharmacology, Department of Physiology, Institute of Biosciences, University of São Paulo (USP), São Paulo, Brazil.
Pinato L; Department of Speech, Language and Hearing Sciences, São Paulo State University (UNESP), Marilia, Brazil.
Źródło:: Journal of pineal research [J Pineal Res] 2021 Apr; Vol. 70 (3), pp. e12715. Date of Electronic Publication: 2021 Jan 26.
Typ publikacji:: Journal Article
Język:: English
Imprint Name(s):: Publication: : Oxford : Wiley
Original Publication: New York : Liss, c1984-
MeSH Terms:: Circadian Rhythm*
Sleep*
Autistic Disorder/*metabolism
Melatonin/*analogs & derivatives
Pineal Gland/*metabolism
Sleep Disorders, Circadian Rhythm/*metabolism
Tumor Necrosis Factor-alpha/*metabolism
Adolescent ; Autistic Disorder/complications ; Autistic Disorder/physiopathology ; Biomarkers/metabolism ; Biomarkers/urine ; Case-Control Studies ; Child ; Child, Preschool ; Female ; Humans ; Interleukin-6/metabolism ; Male ; Melatonin/metabolism ; Melatonin/urine ; Pineal Gland/physiopathology ; Saliva/metabolism ; Sleep Disorders, Circadian Rhythm/etiology ; Sleep Disorders, Circadian Rhythm/physiopathology ; Time Factors
References:: American Psychiatric Association. Diagnostic and statistical manual of mental disorders, 5th edn. Arlington, VA: American Psychiatric Association Publishing; 2013.
Ning M, Daniels J, Schwartz J, et al. Identification and Quantification of Gaps in Access to Autism Resources in the United States: an infodemiological study. J Med Internet Res. 2019;21(7):e13094.
Gevezova M, Sarafian V, Anderson G, Maes M. Inflammation and mitochondrial dysfunction in autism spectrum disorder. CNS Neurol Disord Drug Targets. 2020;19(5):320-333.
Maes M, Anderson G, Betancort Medina SR, et al. Integrating autism spectrum disorder pathophysiology: mitochondria, vitamin A, CD38, oxytocin, serotonin and melatonergic alterations in the placenta and gut. Curr Pharm Des. 2019;25(41):4405-4420.
Modabbernia A, Velthorst E, Reichenberg A. Environmental risk factors for autism: an evidence-based review of systematic reviews and meta-analyses. Molecular Autism. 2017;8:13.
Prata J, Machado AS, von Doellinger O, et al. The contribution of inflammation to autism spectrum disorders: recent clinical evidence. Methods Mol Biol. 2019;2011:493-510.
Smolensky MH, Hermida RC, Reinberg A, et al. Circadian disruption: New clinical perspective of disease pathology and basis for chronotherapeutic intervention. Chronobiol Int. 2016;16:1-19.
Tordjman S, Davlantis KS, Georgieff N, et al. Autism as a disorder of biological and behavioral rhythms: toward new therapeutic perspectives. Front Pediatr. 2015;23(3):1.
Claustrat B, Brun J, Chazot G. The basic physiology and pathophysiology of melatonin. Sleep Med Rev. 2005;9:11-24.
Zisapel N. New perspectives on the role of melatonin in human sleep, circadian rhythms and their regulation. Br J Pharmacol. 2018;175(16):3190-3199.
Shochat T, Haimov I, Lavie P. Melatonin - the key to the gate of sleep. Ann Med. 1998;30:109-114.
Richdale AL, Schreck KA. Sleep problems in autism spectrum disorders: prevalence, nature, and possible biopsychosocial aetiologies. Sleep Med Rev. 2009;13:403-411.
Parvataneni T, Srinivas S, Shah K, et al. Perspective on melatonin use for sleep problems in autism and attention-deficit hyperactivity disorder: a systematic review of randomized clinical trials. Cureus. 2020;12(5):e8335.
Ritvo ER, Ritvo R, Yuwiler A, et al. Elevated daytime melatonin concentrations in autism: a pilot study. Eur Child Adolesc Psychiatry. 1993;2:75-78.
Nir I, Meir D, Zilber N, et al. Brief report: circadian melatonin, thyroid-stimulating hormone, prolactin, and cortisol levels in serum of young adults with autism. J Autism Dev Disord. 1995;25:641-654.
Kulman G, Lissoni P, Rovelli F, et al. Evidence of pineal endocrine hypofunction in autistic children. Neuroendocrinol Lett. 2000;21:31-34.
Tordjman S, Anderson GM, Bellissant E, et al. Day and nighttime excretion of 6-sulphatoxymelatonin in adolescents and young adults with autistic disorder. Psychoneuroendocrinology. 2012;37:1990-1997.
Pagan C, Goubran-Botros H, Delorme R, et al. Disruption of melatonin synthesis is associated with impaired 14-3-3 and miR-451 levels in patients with autism spectrum disorders. Sci Rep. 2017;7:1-10.
Seo M, Anderson G. Gut-amygdala interactions in autism spectrum disorders: developmental roles via regulating mitochondria, exosomes, immunity and microRNAs. Curr Pharm Des. 2019;25(41):4344-4356.
Takano T. Role of microglia in autism: recent advances. Dev Neurosci. 2015;37:195-202.
Ashwood P, Krakowiak P, Hertz-Picciotto I, et al. Elevated plasma cytokines in autism spectrum disorders provide evidence of immune dysfunction and are associated with impaired behavioral outcome. Brain Behav Immun. 2011;25:40-45.
Molloy CA, Morrow AL, Meinzen-Derr J, et al. Elevated cytokine levels in children with autism spectrum disorder. J Neuroimmunol. 2006;172:198-205.
Heuer L, Ashwood P, Schauer J, et al. Reduced levels of immunoglobulin in children with autism correlates with behavioral symptoms. Autism Res. 2008;1:275-283.
Markus RP, Fernandes PA, Kinker GS, et al. Immune-pineal axis - acute inflammatory responses coordinate melatonin synthesis by pinealocytes and phagocytes. Br J Pharmacol. 2018;175:3185-3432.
Simonneaux V, Ribelayga C. Generation of the melatonin endocrine message in mammals: a review of the complex regulation of melatonin synthesis by norepinephrine, peptides, and other pineal transmitters. Pharmacol Rev. 2003;55(2):325-395.
Carvalho-Sousa CE, da Silveira C-M, Tamura EK, et al. Molecular basis for defining the pineal gland and pinealocytes as targets for tumor necrosis factor. Front Endocrinol (Lausanne). 2011;2:10.
Da Silveira C-M, Carvalho-Sousa CE, Tamura EK, et al. TLR4 and CD14 receptors expressed in rat pineal gland trigger NFKB pathway. J Pineal Res. 2010;49:183-192.
Da Silveira C-M, Pinato L, Tamura EK, et al. Glia-pinealocyte network: the paracrine modulation of melatonin synthesis by tumor necrosis factor (TNF). PLoS One. 2012;7(7):e40142.
Da Silveira C-M, Tamura EK, Carvalho-Sousa CE, et al. Daily corticosterone rhythm modulates pineal function through NFκB-related gene transcriptional program. Sci Rep. 2017;7(1):2091.
Pinato L, da Silveira C-M, Franco DG, et al. Selective protection of the cerebellum against intracerebroventricular LPS is mediated by local melatonin synthesis. Brain Struct Funct. 2015;220:827-840.
De Oliveira T-D, Levandovski RM, Custódio de Souza IC, et al. The concept of the immune-pineal axis tested in patients undergoing an abdominal hysterectomy. NeuroImmunoModulation. 2013;20:205-212.
Pontes GN, Cardoso EC, Carneiro-Sampaio MM, et al. Pineal melatonin and the innate immune response: the TNF-alpha increase after cesarean section suppresses nocturnal melatonin production. J Pineal Res. 2007;43:365-371.
Lucas K, Maes M. Role of the Toll Like receptor (TLR) radical cycle in chronic inflammation: possible treatments targeting the TLR4 pathway. Mol Neurobiol. 2013;1:190-204.
Lord C, Rutter M, Le Couteur A. Autism Diagnostic Interview-Revised: a revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. J Autism Dev Disord. 1994;24(5):659-685.
Pereira A, Riesgo RS, Wagner MB. Childhood autism: translation and validation of the Childhood Autism Rating Scale for use in Brazil. J Pediatr (Rio J). 2008;84:487-494.
Brazilian Market Research Association. www.abep.org - ABEP. Brazilian Economic Classification Criteria. São Paulo, Brazil: Brazilian Market Research Association; 2016.
Ferreira VR, Carvalho LB, Ruotolo F, et al. Sleep disturbance scale for children: translation, cultural adaptation, and validation. Sleep Med. 2009;10:457-463.
Carvalho LA, Gorenstein C, Moreno RA, et al. Melatonin levels in drug-free patients with major depression from the southern hemisphere. Psychoneuroendocrinology. 2006;31(6):761-768.
Hidalgo MP, Caumo W, Dantas G, et al. 6-Sulfatoxymelatonin as a predictor of clinical outcome in depressive patients. Hum Psychopharmacol. 2011;26(3):252-257.
Carazo I, Norambuena F, Oliveira C, et al. The effect of night illumination, red and infrared light, on locomotor activity, behavior, and melatonin of Senegalese sole (Solea senegalensis) broodstock. Physiol Behav. 2013;118:201-207.
Grof E, Grof P, Brown GM, et al. Investigations of melatonin secretion in man. Prog Neuropsychopharmacol Biol Psychiatry. 1985;9(5-6):609-612.
Song J. Pineal gland dysfunction in Alzheimer's disease: relationship with the immune-pineal axis, sleep disturbance, and neurogenesis. Mol Neurodegener. 2019;14(1):28.
Beriwal N, Namgyal T, Sangay P, et al. Role of immune-pineal axis in neurodegenerative diseases, unraveling novel hybrid dark hormone therapies. Heliyon. 2019;5(1):e01190.
Harry GJ, Lefebvre d'Hellencourt C, McPherson CA, et al. Tumor necrosis factor p55 and p75 receptors are involved in chemical-induced apoptosis of dentate granule neurons. J Neurochemical. 2008;106:281-298.
Belarbi K, Jopson T, Tweedie D, et al. TNF-α protein synthesis inhibitor restores neuronal function and reverses cognitive deficits induced by chronic neuroinflammation. J Neuroinflammation. 2012;9:23.
Ricci S, Businaro R, Ippoliti F, et al. Altered cytokine and BDNF levels in autism spectrum disorder. Neurotox Res. 2013;24:491-501.
Ziats MN, Rennert OM. Expression profiling of autism candidate genes during human brain development implicates central immune signaling pathways. PLoS One. 2011;6:24691.
Ferguson BJ, Marler S, Altstein LL, et al. Associations between cytokines, endocrine stress response, and gastrointestinal symptoms in autism spectrum disorder. Brain Behav Immun. 2016;58:57-62.
Vanuytsel T, van Wanrooy S, Vanheel H, et al. Psychological stress and corticotropin-releasing hormone increase intestinal permeability in humans by a mast cell-dependent mechanism. Gut. 2014;63(8):1293-1299.
Raskind MA, Burke BL, Crites NJ, et al. Olanzapine-induced weight gain and increased visceral adiposity is blocked by melatonin replacement therapy in rats. Neuropsychopharmacology. 2007;32:284-288.
Agez L, Laurent V, Guerrero HY, et al. Endogenous melatonin provides an effective circadian message to both the suprachiasmatic nuclei and the pars tuberalis of the rat. J Pineal Res. 2009;46:95-105.
Anderson G, Carbone A, Mazzoccoli G. Aryl Hydrocarbon receptor role in co-ordinating SARS-CoV-2 entry and symptomatology: linking cytotoxicity changes in COVID-19 and cancers; modulation by racial discrimination stress. Biology. 2020;9(9):249.
Bian J, Wang Z, Dong Y, et al. Role of BMAL1 and CLOCK in regulating the secretion of melatonin in chick retina under monochromatic green light. Chronobiol Int. 2020;37(12):1677-1692.
Roomruangwong C, Noto C, Kanchanatawan B, et al. The role of aberrations in the immune-inflammatory response system (IRS) and the compensatory immune-regulatory reflex system (CIRS) in different phenotypes of schizophrenia: the IRS-CIRS theory of schizophrenia. Mol Neurobiol. 2020;57(2):778-797.
Yang Z, Matsumoto A, Nakayama K, et al. Circadian-relevant genes are highly polymorphic in autism spectrum disorder patients. Brain Dev. 2016;38:91-99.
Singh VK. Plasma increase of interleukin-12 and interferon-gamma. Pathological significance in autism. J Neuroimmunol. 1996;66:143-145.
Yang CJ, Liu CL, Sang B, et al. The combined role of serotonin and interleukin-6 as biomarker for autism. Neuroscience. 2015;284:290-296.
Maes M, Anderson G, Kubera M, et al. Targeting classical IL-6 signalling or IL-6 trans-signalling in depression? Expert Opin Ther Targets. 2014;18(5):495-512.
Carmassi C, Palagini L, Caruso D, et al. Systematic review of sleep disturbances and circadian sleep desynchronization in autism spectrum disorder: toward an integrative model of a self-reinforcing loop. Front Psychiatry. 2019;10:366.
Díaz-Román A, Zhang J, Delorme R, et al. Sleep in youth with autism spectrum disorders: systematic review and meta-analysis of subjective and objective studies. Evid Based Ment Health. 2018;21(4):146-154.
Yavuz-Kodat E, Reynaud E, Geoffray MM, et al. Disturbances of continuous sleep and circadian rhythms account for behavioral difficulties in children with autism spectrum disorder. J Clin Med. 2020;9(6):1978.
Huang Y, Zou Y, Mai F, et al. Sleep-disordered breathing children: Measurement of nasal nitric oxide and fractional exhaled nitric oxide. HNO. 2016;64:169-174.
Kritikou I, Basta M, Vgontzas NA, et al. Sleep apnoea, sleepiness, inflammation and insulin resistance in middle-aged males and females. Eur Respir J. 2014;43:145-155.
Ulfberg J, Micic S, Strøm J. Afternoon serum-melatonin in sleep disordered breathing. J Intern Med. 1998;244:163-168.
Olsen I, Hicks SD. Oral microbiota and autism spectrum disorder (ASD). J Oral Microbiol. 2019;12(1):1702806.
Anderson G, Rodriguez M, Reiter RJ. Multiple sclerosis: melatonin, orexin, and ceramide interact with platelet activation coagulation factors and gut-microbiome-derived butyrate in the circadian dysregulation of mitochondria in glia and immune cells. Int J Mol Sci. 2019;20(21):5500.
Sommansson A, Nylander O, Sjöblom M. Melatonin decreases duodenal epithelial paracellular permeability via a nicotinic receptor-dependent pathway in rats in vivo. J Pineal Res. 2013;54(3):282-291.
Goldman SE, Alder ML, Burgess HJ, et al. Characterizing sleep in adolescents and adults with autism spectrum disorders. J Autism Dev Disord. 2017;47(6):1682-1695.
Bilgiç A, Abuşoğlu S, Sadıç Çelikkol Ç, et al. Altered kynurenine pathway metabolite levels in toddlers and preschool children with autism spectrum disorder. Int J Neurosci. 2020;29:1-9.
Fujisawa TX, Nishitani S, Iwanaga R, et al. Association of aryl hydrocarbon receptor-related gene variants with the severity of autism spectrum disorders. Front Psychiatry. 2016;7:184.
Grant Information:: 2011/15713-7 Fundação de Amparo à Pesquisa do Estado de São Paulo; 2011/51495-4 Fundação de Amparo à Pesquisa do Estado de São Paulo; 2015/04557-5 Fundação de Amparo à Pesquisa do Estado de São Paulo; Coordenação de Aperfeiçoamento de Pessoal de Nível Superior; Conselho Nacional de Desenvolvimento Científico e Tecnológico
Contributed Indexing:: Keywords: 6-sulfatoxymelatonin; autism spectrum disorder; behavior; cytokines; immune-pineal axis; melatonin; neuroinflammation
Substance Nomenclature:: 0 (Biomarkers)
0 (IL6 protein, human)
0 (Interleukin-6)
0 (TNF protein, human)
0 (Tumor Necrosis Factor-alpha)
2208-40-4 (6-sulfatoxymelatonin)
JL5DK93RCL (Melatonin)
Entry Date(s):: Date Created: 20210109 Date Completed: 20211110 Latest Revision: 20211110
Update Code:: 20240105
DOI:: 10.1111/jpi.12715
PMID:: 33421193
: Czasopismo naukowe

Pełny tekst

Sleep disturbances, abnormal melatonin secretion, and increased inflammation are aspects of autism spectrum disorder (ASD) pathophysiology. The present study evaluated the daily urinary 6-sulfatoxymelatonin (aMT6s) excretion profile and the salivary levels of tumor necrosis factor (TNF) and interleukin-6 (IL-6) in 20 controls and 20 ASD participants, as well as correlating these measures with sleep disturbances. Although 60% of ASD participants showed a significant night-time rise in aMT6s excretion, this rise was significantly attenuated, compared to controls (P < .05). The remaining 40% of ASD individuals showed no significant increase in nocturnal aMT6s. ASD individuals showed higher nocturnal levels of saliva TNF, but not IL-6. Dysfunction in the initiation and maintenance of sleep, as indicated by the Sleep Disturbance Scale for Children, correlated with night-time aMT6s excretion (r = -.28, P < .05). Dysfunction in sleep breathing was inversely correlated with aMT6s (r = -.31, P < .05) and positively associated with TNF level (r = .42, P < .01). Overall such data indicate immune-pineal axis activation, with elevated TNF but not IL-6 levels associated with disrupted pineal melatonin release and sleep dysfunction in ASD. It is proposed that circadian dysregulation in ASD is intimately linked to heightened immune-inflammatory activity. Such two-way interactions of the immune-pineal axis may underpin many aspects of ASD pathophysiology, including sleep disturbances, as well as cognitive and behavioral alterations.
(© 2021 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd.)

Zaloguj się, aby uzyskać dostęp do pełnego tekstu.

Informacja