دورية أكاديمية

Neuroligin-2 shapes individual slow waves during slow-wave sleep and the response to sleep deprivation in mice.

التفاصيل البيبلوغرافية
العنوان: Neuroligin-2 shapes individual slow waves during slow-wave sleep and the response to sleep deprivation in mice.
المؤلفون: Leduc T; Department of Neuroscience, Université de Montréal, Montreal, QC, Canada.; Centre d'études avancées en médecine du sommeil (CÉAMS), Recherche - Centre intégré universitaire de santé et services sociaux du Nord-de-l'Île-de-Montréal, Montreal, QC, Canada.; Centre de recherche du Centre hospitalier de l'Université de Montréal, 900, St-Denis street, Tour Viger Montréal, Montreal, QC, H2X 0A9, Canada., El Alami H; Department of Neuroscience, Université de Montréal, Montreal, QC, Canada.; Centre d'études avancées en médecine du sommeil (CÉAMS), Recherche - Centre intégré universitaire de santé et services sociaux du Nord-de-l'Île-de-Montréal, Montreal, QC, Canada., Bougadir K; Department of Neuroscience, Université de Montréal, Montreal, QC, Canada.; Centre d'études avancées en médecine du sommeil (CÉAMS), Recherche - Centre intégré universitaire de santé et services sociaux du Nord-de-l'Île-de-Montréal, Montreal, QC, Canada., Bélanger-Nelson E; Centre d'études avancées en médecine du sommeil (CÉAMS), Recherche - Centre intégré universitaire de santé et services sociaux du Nord-de-l'Île-de-Montréal, Montreal, QC, Canada.; Pfizer Canada ULC, Montreal, QC, Canada., Mongrain V; Department of Neuroscience, Université de Montréal, Montreal, QC, Canada. valerie.mongrain@umontreal.ca.; Centre d'études avancées en médecine du sommeil (CÉAMS), Recherche - Centre intégré universitaire de santé et services sociaux du Nord-de-l'Île-de-Montréal, Montreal, QC, Canada. valerie.mongrain@umontreal.ca.; Centre de recherche du Centre hospitalier de l'Université de Montréal, 900, St-Denis street, Tour Viger Montréal, Montreal, QC, H2X 0A9, Canada. valerie.mongrain@umontreal.ca.
المصدر: Molecular autism [Mol Autism] 2024 Apr 03; Vol. 15 (1), pp. 13. Date of Electronic Publication: 2024 Apr 03.
نوع المنشور: Journal Article; Research Support, Non-U.S. Gov't
اللغة: English
بيانات الدورية: Publisher: BioMed Central Country of Publication: England NLM ID: 101534222 Publication Model: Electronic Cited Medium: Internet ISSN: 2040-2392 (Electronic) NLM ISO Abbreviation: Mol Autism Subsets: MEDLINE
أسماء مطبوعة: Original Publication: [London] : BioMed Central
مواضيع طبية MeSH: Sleep Deprivation*/metabolism , Sleep, Slow-Wave*, Animals ; Humans ; Mice ; Electroencephalography ; Neuroligins ; Quality of Life ; Sleep/physiology
مستخلص: Background: Sleep disturbances are a common comorbidity to most neurodevelopmental disorders and tend to worsen disease symptomatology. It is thus crucial to understand mechanisms underlying sleep disturbances to improve patients' quality of life. Neuroligin-2 (NLGN2) is a synaptic adhesion protein regulating GABAergic transmission. It has been linked to autism spectrum disorders and schizophrenia in humans, and deregulations of its expression were shown to cause epileptic-like hypersynchronized cerebral activity in rodents. Importantly, the absence of Nlgn2 (knockout: KO) was previously shown to alter sleep-wake duration and quality in mice, notably increasing slow-wave sleep (SWS) delta activity (1-4 Hz) and altering its 24-h dynamics. This type of brain oscillation is involved in memory consolidation, and is also a marker of homeostatic sleep pressure. Sleep deprivation (SD) is notably known to impair cognition and the physiological response to sleep loss involves GABAergic transmission.
Methods: Using electrocorticographic (ECoG) recordings, we here first aimed to verify how individual slow wave (SW; 0.5-4 Hz) density and properties (e.g., amplitude, slope, frequency) contribute to the higher SWS delta activity and altered 24-h dynamics observed in Nlgn2 KO mice. We further investigated the response of these animals to SD. Finally, we tested whether sleep loss affects the gene expression of Nlgn2 and related GABAergic transcripts in the cerebral cortex of wild-type mice using RNA sequencing.
Results: Our results show that Nlgn2 KO mice have both greater SW amplitude and density, and that SW density is the main property contributing to the altered 24-h dynamics. We also found the absence of Nlgn2 to accelerate paradoxical sleep recovery following SD, together with profound alterations in ECoG activity across vigilance states. Sleep loss, however, did not modify the 24-h distribution of the hypersynchronized ECoG events observed in these mice. Finally, RNA sequencing confirmed an overall decrease in cortical expression of Nlgn2 and related GABAergic transcripts following SD in wild-type mice.
Conclusions: This work brings further insight into potential mechanisms of sleep duration and quality deregulation in neurodevelopmental disorders, notably involving NLGN2 and GABAergic neurotransmission.
(© 2024. The Author(s).)
References: Transl Psychiatry. 2016 Feb 16;6:e736. (PMID: 26882036)
Int Rev Psychiatry. 2010;22(5):417-28. (PMID: 21047156)
Nat Commun. 2020 Jul 27;11(1):3744. (PMID: 32719346)
J Sleep Res. 2016 Apr;25(2):131-43. (PMID: 26762182)
Eur J Cell Biol. 2004 Sep;83(9):449-56. (PMID: 15540461)
J Neurosci. 2009 Sep 23;29(38):11828-40. (PMID: 19776269)
Nat Commun. 2020 Jun 19;11(1):3130. (PMID: 32561733)
Schizophr Res. 2020 Sep;223:327-336. (PMID: 32980206)
Bioinformatics. 2015 Jan 15;31(2):166-9. (PMID: 25260700)
Neuron. 2017 Jun 21;94(6):1132-1141.e4. (PMID: 28641112)
Curr Psychiatry Rep. 2018 Mar 5;20(2):9. (PMID: 29504047)
Acta Neurobiol Exp (Wars). 2000;60(2):229-45. (PMID: 10909181)
Clin EEG Neurosci. 2017 May;48(3):200-208. (PMID: 27287223)
Clin Neurophysiol. 2011 Sep;122(9):1779-87. (PMID: 21441067)
Hum Neurobiol. 1982;1(3):195-204. (PMID: 7185792)
Autism Res. 2018 Apr;11(4):613-623. (PMID: 29381247)
Arch Neurol. 2000 Mar;57(3):363-8. (PMID: 10714662)
Neuron. 2001 Dec 6;32(5):883-98. (PMID: 11738033)
Sleep. 2013 Mar 01;36(3):311-23. (PMID: 23450268)
Physiol Genomics. 2010 Aug;42(3):427-36. (PMID: 20501693)
J Neurosci. 2008 Jun 11;28(24):6055-67. (PMID: 18550748)
Epilepsy Res. 2016 May;122:91-6. (PMID: 26994361)
Psychiatry Res. 2020 Dec;294:113489. (PMID: 33038793)
Neuron. 2006 Jul 20;51(2):171-8. (PMID: 16846852)
Sleep. 2016 Mar 01;39(3):613-24. (PMID: 26612390)
J Sleep Res. 2017 Oct;26(5):539-546. (PMID: 28488395)
J Cell Biol. 2013 Jun 10;201(6):929-44. (PMID: 23751499)
Neuron. 2007 Jun 21;54(6):919-31. (PMID: 17582332)
Bioinformatics. 2014 Aug 1;30(15):2114-20. (PMID: 24695404)
Epilepsia. 2005 Jan;46(1):104-9. (PMID: 15660775)
Neuropsychopharmacology. 2020 Jan;45(1):6-20. (PMID: 31216564)
Genome Biol. 2014;15(12):550. (PMID: 25516281)
Biomed Res Int. 2015;2015:498957. (PMID: 25839034)
Front Syst Neurosci. 2017 Mar 31;11:17. (PMID: 28408870)
BMC Neurosci. 2007 Feb 22;8:15. (PMID: 17316437)
PLoS One. 2011;6(8):e22679. (PMID: 21829643)
Neurobiol Sleep Circadian Rhythms. 2021 Jun 13;11:100068. (PMID: 34195482)
J Neurosci Res. 2021 Jan;99(1):37-56. (PMID: 31872500)
Am J Psychiatry. 2010 Nov;167(11):1339-48. (PMID: 20843876)
J Neurosci. 2005 Apr 27;25(17):4365-9. (PMID: 15858062)
Neuron. 2009 Sep 24;63(6):865-78. (PMID: 19778514)
Neuron. 2009 Sep 10;63(5):628-42. (PMID: 19755106)
Neurosci Lett. 2021 Apr 17;750:135753. (PMID: 33610673)
J Neurosci. 1991 Oct;11(10):3200-17. (PMID: 1941080)
Seizure. 2019 Jul;69:298-303. (PMID: 31152984)
J Neurosci. 1993 Aug;13(8):3266-83. (PMID: 8340807)
Proc Natl Acad Sci U S A. 2013 Jun 11;110(24):9974-9. (PMID: 23716671)
Sleep. 2007 Dec;30(12):1643-57. (PMID: 18246974)
Cell. 2019 Oct 3;179(2):514-526.e13. (PMID: 31585085)
Sci Rep. 2017 Mar 03;7:43656. (PMID: 28255162)
Proc Natl Acad Sci U S A. 2017 Jul 3;114(27):E5464-E5473. (PMID: 28630298)
J Sleep Res. 2019 Aug;28(4):e12775. (PMID: 30311707)
Chin J Integr Med. 2015 Nov 23;:. (PMID: 26597287)
Cell. 2019 Oct 3;179(2):289-291. (PMID: 31585076)
Eur J Neurosci. 2011 Feb;33(4):758-66. (PMID: 21226772)
Proc Natl Acad Sci U S A. 2013 Jan 2;110(1):336-41. (PMID: 23248271)
Mol Brain. 2018 Jun 1;11(1):31. (PMID: 29859117)
PLoS One. 2013 Sep 05;8(9):e72450. (PMID: 24039767)
Brain. 2005 May;128(Pt 5):1049-61. (PMID: 15705609)
J Neurosci. 2009 Nov 4;29(44):13883-97. (PMID: 19889999)
Sleep Med Rev. 2020 Jun;51:101276. (PMID: 32109833)
Neuron. 2017 Nov 15;96(4):808-826.e8. (PMID: 29107521)
Neuron. 2006 Sep 21;51(6):741-54. (PMID: 16982420)
Am J Med Genet A. 2017 Jan;173(1):213-216. (PMID: 27865048)
Epilepsy Behav. 2020 Jan;102:106661. (PMID: 31766003)
Nat Commun. 2017 Sep 1;8(1):408. (PMID: 28864826)
Sleep. 1999 Mar 15;22(2):155-69. (PMID: 10201060)
Proc Natl Acad Sci U S A. 2019 Dec 17;116(51):25773-25783. (PMID: 31776259)
Neuroscience. 2000;101(3):523-9. (PMID: 11113301)
eNeuro. 2018 Jan 3;4(6):. (PMID: 29302615)
J Vis Exp. 2021 Feb 21;(168):. (PMID: 33682857)
Proc Natl Acad Sci U S A. 2016 Apr 12;113(15):4206-11. (PMID: 27035941)
Genes Brain Behav. 2009 Feb;8(1):114-26. (PMID: 19016888)
Neuron. 2021 Jan 6;109(1):189-190. (PMID: 33412094)
Neuropediatrics. 2017 Feb;48(1):30-35. (PMID: 27780283)
Mol Brain. 2018 Sep 19;11(1):52. (PMID: 30231918)
Schizophr Bull. 2004;30(4):957-67. (PMID: 15954201)
Neuroscience. 2015 Jan 22;284:217-224. (PMID: 25286384)
Epilepsy Behav. 2012 Oct;25(2):289-94. (PMID: 23069696)
Hum Mol Genet. 2011 Aug 1;20(15):3042-51. (PMID: 21551456)
Genome Biol. 2013 Apr 25;14(4):R36. (PMID: 23618408)
Nat Neurosci. 2023 Jan;26(1):64-78. (PMID: 36510112)
Brain. 2017 Apr 1;140(4):1026-1040. (PMID: 28334879)
J Neurophysiol. 2004 Aug;92(2):1182-98. (PMID: 15028746)
J Sleep Res. 2010 Mar;19(1 Pt 2):228-37. (PMID: 19845847)
Sleep Sci. 2022 Apr-Jun;15(2):245-249. (PMID: 35755914)
Curr Opin Neurobiol. 2012 Jun;22(3):412-22. (PMID: 22424845)
Mol Brain. 2013 May 12;6:23. (PMID: 23663753)
Transl Psychiatry. 2014 Jan 21;4:e347. (PMID: 24448209)
Physiol Genomics. 2007 Nov 14;31(3):441-57. (PMID: 17698924)
Dev Med Child Neurol. 2020 Apr;62(4):426-433. (PMID: 31879946)
معلومات مُعتمدة: PJT-178117 Canada CIHR
فهرسة مساهمة: Keywords: Cerebral cortex; GABAergic neurotransmission; Gene expression; Mice; Sleep deprivation; Sleep-wake regulation; Slow waves; Synaptic adhesion molecules
المشرفين على المادة: 0 (Neuroligins)
0 (neuroligin 2)
تواريخ الأحداث: Date Created: 20240403 Date Completed: 20240405 Latest Revision: 20240729
رمز التحديث: 20240729
مُعرف محوري في PubMed: PMC10993465
DOI: 10.1186/s13229-024-00594-5
PMID: 38570872
قاعدة البيانات: MEDLINE
الوصف
تدمد:2040-2392
DOI:10.1186/s13229-024-00594-5