Sex differences in sleep deficits in mice with an autism-linked Shank3 mutation.
Autism spectrum disorder
Development
SHANK3
Sex differences
Sleep
Journal
Biology of sex differences
ISSN: 2042-6410
Titre abrégé: Biol Sex Differ
Pays: England
ID NLM: 101548963
Informations de publication
Date de publication:
28 Oct 2024
28 Oct 2024
Historique:
received:
16
08
2024
accepted:
18
10
2024
medline:
29
10
2024
pubmed:
29
10
2024
entrez:
29
10
2024
Statut:
epublish
Résumé
Insomnia is more prevalent in individuals with Autism Spectrum Disorder (ASD), can worsen core-symptoms and reduces quality of life of both individuals and caregivers. Although ASD is four times more prevalent in males than females, less is known about sex specific sleep differences in autistic individuals. Recent ASD studies suggest that sleep problems may be more severe in females, which aligns with the sex bias seen in insomnia for the general population. We have previously shown that male mice with a mutation in the high confidence ASD gene Shank3, Shank3 Adult male and female Shank3 Sex and genotype effects were found during baseline sleep and after SD. At baseline, male Shank3 Overall, our study demonstrates sex differences in sleep architecture and homeostatic response to SD in adult Shank3 Sleep problems are common in people with Autism Spectrum Disorder (ASD) and can make their condition worse, impacting both their lives and those of their caregivers. Historically ASD has been diagnosed more often in males and much less is known about the female phenotype. However, recent studies suggest that sleep problems may be more severe in autistic females. We previously shown that the ASD mouse model, Shank3
Sections du résumé
BACKGROUND
BACKGROUND
Insomnia is more prevalent in individuals with Autism Spectrum Disorder (ASD), can worsen core-symptoms and reduces quality of life of both individuals and caregivers. Although ASD is four times more prevalent in males than females, less is known about sex specific sleep differences in autistic individuals. Recent ASD studies suggest that sleep problems may be more severe in females, which aligns with the sex bias seen in insomnia for the general population. We have previously shown that male mice with a mutation in the high confidence ASD gene Shank3, Shank3
METHODS
METHODS
Adult male and female Shank3
RESULTS
RESULTS
Sex and genotype effects were found during baseline sleep and after SD. At baseline, male Shank3
CONCLUSIONS
CONCLUSIONS
Overall, our study demonstrates sex differences in sleep architecture and homeostatic response to SD in adult Shank3
Sleep problems are common in people with Autism Spectrum Disorder (ASD) and can make their condition worse, impacting both their lives and those of their caregivers. Historically ASD has been diagnosed more often in males and much less is known about the female phenotype. However, recent studies suggest that sleep problems may be more severe in autistic females. We previously shown that the ASD mouse model, Shank3
Autres résumés
Type: plain-language-summary
(eng)
Sleep problems are common in people with Autism Spectrum Disorder (ASD) and can make their condition worse, impacting both their lives and those of their caregivers. Historically ASD has been diagnosed more often in males and much less is known about the female phenotype. However, recent studies suggest that sleep problems may be more severe in autistic females. We previously shown that the ASD mouse model, Shank3
Identifiants
pubmed: 39468684
doi: 10.1186/s13293-024-00664-6
pii: 10.1186/s13293-024-00664-6
doi:
Substances chimiques
Shank3 protein, mouse
0
Nerve Tissue Proteins
0
Microfilament Proteins
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
85Subventions
Organisme : NIH HHS
ID : 1F99NS135815-01
Pays : United States
Organisme : NIH HHS
ID : R56NS124805
Pays : United States
Organisme : Simons Foundation Autism Research Initiative
ID : 878115
Informations de copyright
© 2024. The Author(s).
Références
Achermann P. EEG analysis applied to sleep. 2009
Achermann P, Borbély AA. Mathematical models of sleep regulation. Front Biosci. 2003;8:s683-693. https://doi.org/10.2741/1064 .
doi: 10.2741/1064
pubmed: 12700054
Achermann P, Borbely AA. Sleep homeostasis and models of sleep regulation. Principles and practice of sleep medicine, 6th ed. In: M. Kryger, T. Roth and W.C. Dement, eds. Elsevier. Vol. 6, 2017, pp. 377–387. https://doi.org/10.1016/B978-0-323-24288-2.00036-2
Angell AM, Deavenport-Saman A, Yin L, Zou B, Bai C, Varma D, Solomon O. Sex differences in co-occurring conditions among autistic children and youth in florida: a retrospective cohort study (2012–2019). J Autism Dev Disord. 2021;51(10):3759–65. https://doi.org/10.1007/s10803-020-04841-5 .
doi: 10.1007/s10803-020-04841-5
pubmed: 33394250
pmcid: 8254818
Bian W-J, González OC, de Lecea L. Adolescent sleep defects and dopaminergic hyperactivity in mice with a schizophrenia-linked Shank3 mutation. Sleep. 2023;46(7):zsad131. https://doi.org/10.1093/sleep/zsad131 .
doi: 10.1093/sleep/zsad131
pubmed: 37144901
pmcid: 10334736
Bonanni E, Maestri M, Tognoni G, Fabbrini M, Nucciarone B, Manca ML, Gori S, Iudice A, Murri L. Daytime sleepiness in mild and moderate Alzheimer’s disease and its relationship with cognitive impairment. J Sleep Res. 2005;14(3):311–7. https://doi.org/10.1111/j.1365-2869.2005.00462.x .
doi: 10.1111/j.1365-2869.2005.00462.x
pubmed: 16120107
Borbely AA, Achermann P. Sleep homeostasis and models of sleep regulation. J Biol Rhythms. 1999;14(6):559–70. https://doi.org/10.1177/074873099129000894 .
doi: 10.1177/074873099129000894
Bozdagi O, Sakurai T, Papapetrou D, Wang X, Dickstein DL, Takahashi N, Kajiwara Y, Yang M, Katz AM, Scattoni ML, Harris MJ, Saxena R, Silverman JL, Crawley JN, Zhou Q, Hof PR, Buxbaum JD. Haploinsufficiency of the autism-associated Shank3 gene leads to deficits in synaptic function, social interaction, and social communication. Molecular Autism. 2010;1:15. https://doi.org/10.1186/2040-2392-1-15 .
doi: 10.1186/2040-2392-1-15
pubmed: 21167025
pmcid: 3019144
Cohen S, Conduit R, Lockley SW, Rajaratnam SM, Cornish KM. The relationship between sleep and behavior in autism spectrum disorder (ASD): a review. J Neurodev Disord. 2014;6(1):44. https://doi.org/10.1186/1866-1955-6-44 .
doi: 10.1186/1866-1955-6-44
pubmed: 25530819
pmcid: 4271434
D’Agati E, Abate R, Gialloreti LE, Napolitano C, Postorino V, Curatolo P, Mazzone L. Sleep problems in attention-deficit/hyperactivity disorder and autism spectrum disorder: sex differences and parental stress. Psychiatry Res. 2020;291: 113099. https://doi.org/10.1016/j.psychres.2020.113099 .
doi: 10.1016/j.psychres.2020.113099
pubmed: 32540683
Dijk D-J, Duffy JF, Silva EJ, Shanahan TL, Boivin DB, Czeisler CA. Amplitude reduction and phase shifts of melatonin, cortisol and other circadian rhythms after a gradual advance of sleep and light exposure in humans. PLoS ONE. 2012;7(2): e30037. https://doi.org/10.1371/journal.pone.0030037 .
doi: 10.1371/journal.pone.0030037
pubmed: 22363414
pmcid: 3281823
Estes A, Munson J, St John T, Finlayson R, Pandey J, Gottlieb B, Herrington J, Schultz RT. Sleep problems in autism: Sex differences in the school-age population. Autism Res. 2023;16(1):164–73. https://doi.org/10.1002/aur.2848 .
doi: 10.1002/aur.2848
pubmed: 36341856
Franken P, Dijk DJ, Tobler I, Borbély AA. Sleep deprivation in rats: effects on EEG power spectra, vigilance states, and cortical temperature. Am J Physiol. 1991;261(1 Pt 2):R198-208. https://doi.org/10.1152/ajpregu.1991.261.1.R198 .
doi: 10.1152/ajpregu.1991.261.1.R198
pubmed: 1858947
Gandhi KD, Mansukhani MP, Silber MH, Kolla BP. Excessive daytime sleepiness: a clinical review. Mayo Clin Proc. 2021;96(5):1288–301. https://doi.org/10.1016/j.mayocp.2020.08.033 .
doi: 10.1016/j.mayocp.2020.08.033
pubmed: 33840518
Goldman SE, Surdyka K, Cuevas R, Adkins K, Wang L, Malow BA. Defining the sleep phenotype in children with autism. Dev Neuropsychol. 2009;34(5):560–73. https://doi.org/10.1080/87565640903133509 .
doi: 10.1080/87565640903133509
pubmed: 20183719
pmcid: 2946240
Hodge D, Carollo TM, Lewin M, Hoffman CD, Sweeney DP. Sleep patterns in children with and without autism spectrum disorders: developmental comparisons. Res Dev Disabil. 2014;35(7):1631–8. https://doi.org/10.1016/j.ridd.2014.03.037 .
doi: 10.1016/j.ridd.2014.03.037
pubmed: 24780146
Ingiosi AM, Schoch H, Wintler T, Singletary KG, Righelli D, Roser LG, Medina E, Risso D, Frank MG, Peixoto L. Shank3 modulates sleep and expression of circadian transcription factors. Elife. 2019;8:e42819. https://doi.org/10.7554/eLife.42819 .
doi: 10.7554/eLife.42819
pubmed: 30973326
pmcid: 6488297
Johnson EO, Roth T, Schultz L, Breslau N. Epidemiology of DSM-IV insomnia in adolescence: lifetime prevalence, chronicity, and an emergent gender difference. Pediatrics. 2006;117(2):e247-256. https://doi.org/10.1542/peds.2004-2629 .
doi: 10.1542/peds.2004-2629
pubmed: 16452333
Kouser M, Speed HE, Dewey CM, Reimers JM, Widman AJ, Gupta N, Liu S, Jaramillo TC, Bangash M, Xiao B, Worley PF, Powell CM. Loss of predominant Shank3 isoforms results in hippocampus-dependent impairments in behavior and synaptic transmission. J Neurosci. 2013;33(47):18448–68. https://doi.org/10.1523/JNEUROSCI.3017-13.2013 .
doi: 10.1523/JNEUROSCI.3017-13.2013
pubmed: 24259569
pmcid: 3834052
Long S, Ding R, Wang J, Yu Y, Lu J, Yao D. Sleep quality and electroencephalogram delta power. Front Neurosci. 2021;15: 803507. https://doi.org/10.3389/fnins.2021.803507 .
doi: 10.3389/fnins.2021.803507
pubmed: 34975393
pmcid: 8715081
Lord JS, Gay SM, Harper KM, Nikolova VD, Smith KM, Moy SS, Diering GH. Early life sleep disruption potentiates lasting sex-specific changes in behavior in genetically vulnerable Shank3 heterozygous autism model mice. Mol Autism. 2022;13:35. https://doi.org/10.1186/s13229-022-00514-5 .
doi: 10.1186/s13229-022-00514-5
pubmed: 36038911
pmcid: 9425965
Maenner MJ, Warren Z, Williams AR, Amoakohene E, Bakian AV, Bilder DA, Durkin MS, Fitzgerald RT, Furnier SM, Hughes MM, Ladd-Acosta CM, McArthur D, Pas ET, Salinas A, Vehorn A, Williams S, Esler A, Grzybowski A, Hall-Lande J, Shaw KA. Prevalence and characteristics of autism spectrum disorder among children aged 8 years—autism and developmental disabilities monitoring network, 11 Sites, United States, 2020. MMWR Surveill Summ. 2023;72(2):1–14. https://doi.org/10.15585/mmwr.ss7202a1 .
doi: 10.15585/mmwr.ss7202a1
pubmed: 36952289
pmcid: 10042615
Manconi M, Ferri R, Miano S, Maestri M, Bottasini V, Zucconi M, Ferini-Strambi L. Sleep architecture in insomniacs with severe benzodiazepine abuse. Clin Neurophysiol. 2017;128(6):875–81. https://doi.org/10.1016/j.clinph.2017.03.009 .
doi: 10.1016/j.clinph.2017.03.009
pubmed: 28399441
Medina E, Peterson S, Ford K, Singletary K, Peixoto L. Critical periods and autism spectrum disorders, a role for sleep. Neurobiol Sleep Circ Rhythms. 2023;14: 100088. https://doi.org/10.1016/j.nbscr.2022.100088 .
doi: 10.1016/j.nbscr.2022.100088
Medina E, Schoch H, Ford K, Wintler T, Singletary KG, Peixoto L. Shank3 influences mammalian sleep development. J Neurosci Res. 2022;100(12):2174–86. https://doi.org/10.1002/jnr.25119 .
doi: 10.1002/jnr.25119
pubmed: 36056598
pmcid: 9588578
Mong JA, Cusmano DM. Sex differences in sleep: impact of biological sex and sex steroids. Phil Trans R Soc B Biol Sci. 2016;371(1688):20150110. https://doi.org/10.1098/rstb.2015.0110 .
doi: 10.1098/rstb.2015.0110
Ohayon MM. Prevalence of DSM-IV diagnostic criteria of insomnia: Distinguishing insomnia related to mental disorders from sleep disorders. J Psychiatr Res. 1997;31(3):333–46. https://doi.org/10.1016/s0022-3956(97)00002-2 .
doi: 10.1016/s0022-3956(97)00002-2
pubmed: 9306291
Palchykova S, Winsky-Sommerer R, Shen H-Y, Boison D, Gerling A, Tobler I. Manipulation of adenosine kinase affects sleep regulation in mice. J Neurosci. 2010;30(39):13157–65. https://doi.org/10.1523/JNEUROSCI.1359-10.2010 .
doi: 10.1523/JNEUROSCI.1359-10.2010
pubmed: 20881134
pmcid: 2950004
Perrier J, Clochon P, Bertran F, Couque C, Bulla J, Denise P, Bocca M-L. Specific EEG sleep pattern in the prefrontal cortex in primary insomnia. PLoS ONE. 2015;10(1): e0116864. https://doi.org/10.1371/journal.pone.0116864 .
doi: 10.1371/journal.pone.0116864
pubmed: 25611059
pmcid: 4303266
Petruzzelli MG, Matera E, Giambersio D, Marzulli L, Gabellone A, Legrottaglie AR, Margari A, Margari L. Subjective and electroencephalographic sleep parameters in children and adolescents with autism spectrum disorder: a systematic review. J Clin Med. 2021;10(17):3893. https://doi.org/10.3390/jcm10173893 .
doi: 10.3390/jcm10173893
pubmed: 34501341
pmcid: 8432113
Pigeon WR, Perlis ML. Sleep homeostasis in primary insomnia. Sleep Med Rev. 2006;10(4):247–54. https://doi.org/10.1016/j.smrv.2005.09.002 .
doi: 10.1016/j.smrv.2005.09.002
pubmed: 16563817
Rothman SM, Mattson MP. Sleep disturbances in Alzheimer’s and Parkinson’s diseases. NeuroMol Med. 2012;14(3):194–204. https://doi.org/10.1007/s12017-012-8181-2 .
doi: 10.1007/s12017-012-8181-2
Singer EV, Niarchou M, Maxwell-Horn A, Hucks D, Johnston R, Sutcliffe JS, Davis LK, Malow BA. Characterizing sleep disorders in an autism-specific collection of electronic health records. Sleep Med. 2022;92:88–95. https://doi.org/10.1016/j.sleep.2022.03.009 .
doi: 10.1016/j.sleep.2022.03.009
pubmed: 35367909
pmcid: 9018608
Singletary KG, Naidoo N. Disease and degeneration of aging neural systems that integrate sleep drive and circadian oscillations. Front Neurol. 2011;2:66. https://doi.org/10.3389/fneur.2011.00066 .
doi: 10.3389/fneur.2011.00066
pubmed: 22028699
pmcid: 3199684
Speed HE, Kouser M, Xuan Z, Reimers JM, Ochoa CF, Gupta N, Liu S, Powell CM. Autism-associated insertion mutation (InsG) of Shank3 Exon 21 causes impaired synaptic transmission and behavioral deficits. J Neurosci. 2015;35(26):9648–65. https://doi.org/10.1523/JNEUROSCI.3125-14.2015 .
doi: 10.1523/JNEUROSCI.3125-14.2015
pubmed: 26134648
pmcid: 4571502
Van Someren EJW. Brain mechanisms of insomnia: new perspectives on causes and consequences. Physiol Rev. 2021;101(3):995–1046. https://doi.org/10.1152/physrev.00046.2019 .
doi: 10.1152/physrev.00046.2019
pubmed: 32790576
Veatch OJ, Maxwell-Horn AC, Malow BA. Sleep in autism spectrum disorders. Curr Sleep Med Rep. 2015;1(2):131–40. https://doi.org/10.1007/s40675-015-0012-1 .
doi: 10.1007/s40675-015-0012-1
pubmed: 26046012
pmcid: 4450800
Wang C, Ramakrishnan S, Laxminarayan S, Dovzhenok A, Cashmere JD, Germain A, Reifman J. An attempt to identify reproducible high-density EEG markers of PTSD during sleep. Sleep. 2020;43(1):zsz207. https://doi.org/10.1093/sleep/zsz207 .
doi: 10.1093/sleep/zsz207
pubmed: 31553047
Wintler T, Schoch H, Frank MG, Peixoto L. Sleep, brain development, and autism spectrum disorders: Insights from animal models. J Neurosci Res. 2020;98(6):1137–49. https://doi.org/10.1002/jnr.24619 .
doi: 10.1002/jnr.24619
pubmed: 32215963
pmcid: 7199437
Yang M, Zhang Z, Wang Y, Li J, Guo Q, Chen X, Wang E. Association of nap frequency with hypertension or ischemic stroke supported by prospective cohort data and mendelian randomization in predominantly middle-aged european subjects. Hypertension. 2022;79(9):1962–70. https://doi.org/10.1161/HYPERTENSIONAHA.122.19120 .
doi: 10.1161/HYPERTENSIONAHA.122.19120
pubmed: 35876003
Zhang B, Wing Y-K. Sex differences in insomnia: a meta-analysis. Sleep. 2006;29(1):85–93. https://doi.org/10.1093/sleep/29.1.85 .
doi: 10.1093/sleep/29.1.85
pubmed: 16453985
Zhong G, Wang Y, Tao T, Ying J, Zhao Y. Daytime napping and mortality from all causes, cardiovascular disease, and cancer: a meta-analysis of prospective cohort studies. Sleep Med. 2015;16(7):811–9. https://doi.org/10.1016/j.sleep.2015.01.025 .
doi: 10.1016/j.sleep.2015.01.025
pubmed: 26051864