Abstract
Oligodendrocytes (OL) are the only myelinating cells of the central nervous system thus interferences, either environmental or genetic, with their maturation or function have devastating consequences. Albeit so far neglected, one of the less appreciated, nevertheless possible, regulators of OL maturation and function is the circadian cycle. Yet, disruptions in these rhythms are unfortunately becoming a common “disorder” in the today’s world. The temporal patterning of behaviour and physiology is controlled by a circadian timing system based in the anterior hypothalamus. At the molecular level, circadian rhythms are generated by a transcriptional/translational feedback system that regulates transcription and has a major impact on cellular function(s). Fundamental cellular properties/functions in most cell types vary with the daily circadian cycle: OL are unlikely an exception! To be clear, the presence of circadian oscillators or the cell-specific function(s) of the circadian clock in OL has yet to be defined. Furthermore, we wish to entertain the idea of links between the “thin” evidence on OL intrinsic circadian rhythms and their interjection(s) at different stages of lineage progression as well as in supporting/regulating OL crucial function: myelination. Individuals with intellectual and developmental syndromes as well as neurodegenerative diseases present with a disrupted sleep/wake cycle; hence, we raise the possibility that these disturbances in timing can contribute to the loss of white matter observed in these disorders. Preclinical and clinical work in this area is needed for a better understanding of how circadian rhythms influence OL maturation and function(s), to aid the development of new therapeutic strategies and standards of care for these patients.
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References
Bercury KK, Macklin WB (2015) Dynamics and mechanisms of CNS myelination. Dev Cell 32(4):447–458. https://doi.org/10.1016/j.devcel.2015.01.016
Hughes EG, Appel B (2016) The cell biology of CNS myelination. Curr Opin Neurobiol 39:93–100. https://doi.org/10.1016/j.conb.2016.04.013
Mount CW, Monje M (2017) Wrapped to adapt: experience-dependent myelination. Neuron 95(4):743–756. https://doi.org/10.1016/j.neuron.2017.07.009
Forbes TA, Gallo V (2017) All wrapped up: environmental effects on myelination. Trends Neurosci 40(9):572–587. https://doi.org/10.1016/j.tins.2017.06.009
Filley CM, Fields RD (2016) White matter and cognition: making the connection. J Neurophysiol 116(5):2093–2104. https://doi.org/10.1152/jn.00221.2016
Porter A, Leckie R, Verstynen T (2018) White matter pathways as both a target and mediator of health behaviors. Ann N Y Acad Sci 1428(1):71–88. https://doi.org/10.1111/nyas.13708
Wang Y, Olson IR (2018) The original social network: white matter and social cognition. Trends Cogn Sci 22(6):504–516. https://doi.org/10.1016/j.tics.2018.03.005
Saab AS, Nave KA (2017) Myelin dynamics: protecting and shaping neuronal functions. Curr Opin Neurobiol 47:104–112. https://doi.org/10.1016/j.conb.2017.09.013
Bergles DE, Richardson WD (2015) Oligodendrocyte development and plasticity cold spring. Harb Perspect Biol 8(2):a020453. http://cshperspectives.cshlp.org/
van Tilborg E, de Theije CGM, van Hal M, Wagenaar N, de Vries LS, Benders MJ, Rowitch DH, Nijboer CH (2018) Origin and dynamics of oligodendrocytes in the developing brain: Implications for perinatal white matter injury. Glia 66(2):221–238. https://doi.org/10.1002/glia.23256
Sauvageot CM, Stiles CD (2002) Molecular mechanisms controlling cortical gliogenesis. Curr Opin Neurobiol 12(3):244–9. https://doi.org/10.1016/S0959-4388(02)00322-7
Zuchero JB, Barres BA (2013) Intrinsic and extrinsic control of oligodendrocyte development. Curr Opin Neurobiol 23: 914–20. https://doi.org/10.1016/j.conb.2013.06.005
Mayoral SR, Chan JR (2016) The environment rules: spatiotemporal regulation of oligodendrocyte differentiation. Curr Opin Neurobiol 39:47–52. https://doi.org/10.1016/j.conb.2016.04.002
Mitew S, Hay CM, Peckham H, Xiao J, Koenning M, Emery B (2014) Mechanisms regulating the development of oligodendrocytes and central nervous system myelin. Neuroscience 276:29–47. https://doi.org/10.1016/j.neuroscience.2013.11.029
Almeida RG, Lyons DA (2017) On myelinated axon plasticity and neuronal circuit formation and function. J Neurosci 37(42):10023–10034. https://doi.org/10.1523/JNEUROSCI.3185-16.2017
Verkhratsky A, Steinhäuser C (2000) Ion channels in glial cells. Brain Res Brain Res Rev 32(2–3):380–412. https://doi.org/10.1016/S0165-0173(99)00093-4
Butt AM, Fern RF, Matute C (2014) Neurotransmitter signaling in white matter. Glia 62(11):1762–1779. https://doi.org/10.1002/glia.22674
Ragheb F, Molina-Holgado E, Cui QL, Khorchid A, Liu HN, Larocca JN, Almazan G (2001) Pharmacological and functional characterization of muscarinic receptor subtypes in developing oligodendrocytes. J Neurochem 77(5):1396–1406. https://doi.org/10.1046/j.1471-4159.2001.00356.x
De Angelis F, Bernardo A, Magnaghi V, Minghetti L, Tata AM (2012) Muscarinic receptor subtypes as potential targets to modulate oligodendrocyte progenitor survival, proliferation, and differentiation. Dev Neurobiol 72(5):713–728. https://doi.org/10.1002/dneu.20976
Ghiani CA, Eisen AM, Yuan X, DePinho RA, McBain CJ, Gallo V (1999) Neurotransmitter receptor activation triggers p27(Kip1)and p21(CIP1) accumulation and G1 cell cycle arrest in oligodendrocyte progenitors. Development 126(5):1077–1090
Ghiani CA, Gallo V (2001) Inhibition of cyclin E-cyclin-dependent kinase 2 complex formation and activity is associated with cell cycle arrest and withdrawal in oligodendrocyte progenitor cells. J Neurosci 21(4):1274–1282. https://doi.org/10.1523/JNEUROSCI.21-04-01274.2001
Weger M, Diotel N, Dorsemans AC, Dickmeis T, Weger BD (2017) Stem cells and the circadian clock. Dev Biol 431(2):111–123. https://doi.org/10.1016/j.ydbio.2017.09.012
Traiffort E, Zakaria M, Laouarem Y, Ferent J (2016) Hedgehog: a key signaling in the development of the oligodendrocyte lineage. J Develop Biol 4(3):E28. https://doi.org/10.3390/jdb4030028
Barres B, Raff M (1994) Control of oligodendrocyte number in the developing rat optic nerve. Neuron 12:935–942
Gao F-B, Durand B, Raff M (1997) Oligodendrocyte precursor cells count time but not cell divisions before differentiation. Curr Biol 7:152–155
Casaccia-Bonnefil P, Hardy RJ, Teng KK, Levine JM, Koff A, Chao MV (1999) Loss of p27Kip1 function results in increased proliferative capacity of oligodendrocyte progenitors but unaltered timing of differentiation. Development 126(18):4027–4037
Draijer S, Chaves I, Hoekman MFM (2018) The circadian clock in adult neural stem cell maintenance. Prog Neurobiol. https://doi.org/10.1016/j.pneurobio.2018.05.007
Gaucher J, Montellier E, Sassone-Corsi P (2018) Molecular cogs: interplay between circadian clock and cell cycle. Trends Cell Biol 28(5):368–379. https://doi.org/10.1016/j.tcb.2018.01.006
Bellesi M, Pfister-Genskow M, Maret S, Keles S, Tononi G, Cirelli C (2013) Effects of sleep and wake on oligodendrocytes and their precursors. J Neurosci 33:14288–14300. https://doi.org/10.1523/JNEUROSCI.5102-12.2013
Gallo V, Zhou JM, McBain CJ, Wright P, Knutson PL, Armstrong RC (1996) Oligodendrocyte progenitor cell proliferation and lineage progression are regulated by glutamate receptor-mediated K+ channel block. J Neurosci 16(8):2659–2670. https://doi.org/10.1523/JNEUROSCI.16-08-02659.1996
Gallo V, Ghiani CA (2000) Glutamate receptors in glia: new cells, new inputs and new functions. Trends Pharmacol Sci 21(7):252–258. https://doi.org/10.1016/S0165-6147(00)01494-2
Fannon J, Tarmier W, Fulton D (2015) Neuronal activity and AMPA-type glutamate receptor activation regulates the morphological development of oligodendrocyte precursor cells. Glia 63(6):1021–1035. https://doi.org/10.1002/glia.22799
Gudz TI, Komuro H, Macklin WB (2006) Glutamate stimulates oligodendrocyte progenitor migration mediated via an alphav integrin/myelin proteolipid protein complex. J Neurosci 26(9):2458–2466. https://doi.org/10.1523/JNEUROSCI.4054-05.2006
Harlow DE, Saul KE, Komuro H, Macklin WB (2015) Myelin proteolipid protein complexes with αv integrin and ampa receptors in vivo and regulates AMPA-dependent oligodendrocyte progenitor cell migration through the modulation of cell-surface glur2 expression. J Neurosci 35(34):12018–12032. https://doi.org/10.1523/JNEUROSCI.5151-14.2015
Yuan X, Eisen AM, McBain CJ, Gallo V (1998) A role for glutamate and its receptors in the regulation of oligodendrocyte development in cerebellar tissue slices. Development 125(15):2901–2914
Luyt K, Slade TP, Dorward JJ, Durant CF, Wu Y, Shigemoto R, Mundell SJ, Váradi A, Molnár E (2007) Developing oligodendrocytes express functional GABA(B) receptors that stimulate cell proliferation and migration. J Neurochem 100(3):822–840. https://doi.org/10.1111/j.1471-4159.2006.04255.x
Hamilton NB, Clarke LE, Arancibia-Carcamo IL, Kougioumtzidou E, Matthey M, Káradóttir R, Whiteley L, Bergersen LH, Richardson WD, Attwell D (2017) Endogenous GABA controls oligodendrocyte lineage cell number, myelination, and CNS internode length. Glia 65(2):309–321. https://doi.org/10.1002/glia.23093
Cirelli C, Tononi G (2000) Gene expression in the brain across the sleep-waking cycle. Brain Res 885:303–321. https://doi.org/10.1016/S0006-8993(00)03008-0
Cirelli C, Gutierrez CM, Tononi G (2004) Extensive and divergent effects of sleep and wakefulness on brain gene expression. Neuron 41:35–43. https://doi.org/10.1016/S0896-6273(03)00814-6
Cirelli C, Faraguna U, Tononi G (2006) Changes in brain gene expression after long-term sleep deprivation. J Neurochem 98:1632–1645. https://doi.org/10.1111/j.1471-4159.2006.04058.x
Terao A, Wisor JP, Peyron C, Apte-Deshpande A, Wurts SW, Edgar DM, Kilduff TS (2006) Gene expression in the rat brain during sleep deprivation and recovery sleep: an Affymetrix GeneChip® study. Neuroscience 137:593–605. https://doi.org/10.1016/j.neuroscience.2005.08.059
Vecsey CG, Peixoto L, Choi JHK, Wimmer M, Jaganath D, Hernandez PJ, Blackwell J, Meda K, Park AJ, Hannenhalli S, Abel T (2012) Genomic analysis of sleep deprivation reveals translational regulation in the hippocampus. Physiol Genomics 44:981–991. https://doi.org/10.1152/physiolgenomics.00084.2012
Bellesi M, Haswell JD, de Vivo L, Marshall W, Roseboom PH, Tononi G, Cirelli C (2018) Myelin modifications after chronic sleep loss in adolescent mice. Sleep 41: 5. https://doi.org/10.1093/sleep/zsy034
Blum ID, Bell B, Wu MN (2018) Time for bed: genetic mechanisms mediating the circadian regulation of sleep. Trends Genet 34(5):379–388. https://doi.org/10.1016/j.tig.2018.01.001
Takahashi JS (2017) Transcriptional architecture of the mammalian circadian clock. Nat Rev Genet 2017 Mar 18(3):164–179. https://doi.org/10.1038/nrg.2016.150
Zhang R, Lahens NF, Ballance HI, Hughes ME, Hogenesch JB (2014) A circadian gene expression atlas in mammals: implications for biology and medicine. Proc Natl Acad Sci USA 111:16219–16224. https://doi.org/10.1073/pnas.1408886111
Hernandez M, Casaccia P (2015) Interplay between transcriptional control and chromatin regulation in the oligodendrocyte lineage. Glia 63(8):1357–1375. https://doi.org/10.1002/glia.22818
Gregath A, Lu QR (2018) Epigenetic modifications-insight into oligodendrocyte lineage progression, regeneration, and disease. FEBS Lett 592(7):1063–1078. https://doi.org/10.1002/1873-3468.12999
Cahoy JD, Emery B, Kaushal A, Foo LC, Zamanian JL, Christopherson KS, Xing Y, Lubischer JL, Krieg PA, Krupenko SA, Thompson WJ, Barres BA (2008) A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. J Neurosci 28:264–278. https://doi.org/10.1523/JNEUROSCI.4178-07.2008
Nobuta H, Ghiani CA, Paez PM, Spreuer V, Dong H, Korsak RA, Manukyan A, Li J, Vinters HV, Huang EJ, Rowitch DH, Sofroniew MV, Campagnoni AT, de Vellis J, Waschek JA (2012) STAT3-mediated astrogliosis protects myelin development in neonatal brain injury. Ann Neurol 72(5):750–765. https://doi.org/10.1002/ana.23670
Lee FY, Wang HB, Hitchcock ON, Loh DH, Whittaker DS, Kim YS, Aiken A, Kokikian C, Dell’Angelica EC, Colwell CS, Ghiani CA (2018) Sleep/wake disruption in a mouse model of bloc-1 deficiency. Front Neurosci 12:759. https://doi.org/10.3389/fnins.2018.00759
Sommer I, Schachner M (1981) Monoclonal antibodies (O1 to O4) to oligodendrocyte cell surfaces: an immunocytological study in the central nervous system. Dev Biol 83:311–327. https://doi.org/10.1016/0012-1606(81)90477-2
Bansal R, Warrington AE, Gard AL, Ranscht B, Pfeiffer SE (1989) Multiple and novel specificities of monoclonal antibodies O1, O4, and R-mAb used in the analysis of oligodendrocyte development. J Neurosci Res 24:548–557. https://doi.org/10.1002/jnr.490240413
Pembroke WG, Babbs A, Davies KE, Ponting CP, Oliver PL (2015) Temporal transcriptomics suggest that twin-peaking genes reset the clock. Elife 4: e10518. https://doi.org/10.7554/eLife.10518
Hinds LR, Chun LE, Woodruff ER, Christensen JA, Hartsock MJ, Spencer RL (2017) Dynamic glucocorticoid-dependent regulation of Sgk1 expression in oligodendrocytes of adult male rat brain by acute stress and time of day. PLoS ONE 12(4):e0175075. https://doi.org/10.1371/journal.pone.0175075
Matsumoto Y, Tsunekawa Y, Nomura T, Suto F, Matsumata M, Tsuchiya S, Osumi N (2011) Differential proliferation rhythm of neural progenitor and oligodendrocyte precursor cells in the young adult hippocampus. PLoS ONE 6(11):e27628. https://doi.org/10.1371/journal.pone.0027628
Chrast R, Saher G, Nave KA, Verheijen MH (2011) Lipid metabolism in myelinating glial cells: lessons from human inherited disorders and mouse models. J Lipid Res 52(3):419–434. http://www.jlr.org/content/early/2010/11/09/jlr.R009761
Björkhem I, Meaney S, Fogelman AM (2004) Brain cholesterol: long secret life behind a barrier. Arterioscler Thromb Vasc Biol 24:806–815. https://doi.org/10.1161/01.ATV.0000120374.59826.1b
Hatori M, Vollmers C, Zarrinpar A, DiTacchio L, Bushong EA, Gill S, Leblanc M, Chaix A, Joens M, Fitzpatrick JA, Ellisman MH, Panda S (2012) Time-restricted feeding without reducing caloric intake prevents metabolic diseases in mice fed a high-fat diet. Cell Metab 15(6):848–860. https://doi.org/10.1016/j.cmet.2012.04.019
Panda S (2016) Circadian physiology of metabolism. Science 354(6315):1008–1015. https://doi.org/10.1126/science.aah4967
Morrison BM, Lee Y, Rothstein JD (2013) Oligodendroglia: metabolic supporters of axons. Trends Cell Biol 23(12):644–651. https://doi.org/10.1016/j.tcb.2013.07.007
Yin X, Kidd GJ, Ohno N, Perkins GA, Ellisman MH, Bastian C, Brunet S, Baltan S, Trapp BD (2016) Proteolipid protein-deficient myelin promotes axonal mitochondrial dysfunction via altered metabolic coupling. J Cell Biol 215(4):531–542. https://doi.org/10.1083/jcb.201607099
Saab AS, Tzvetavona ID, Trevisiol A, Baltan S, Dibaj P, Kusch K, Möbius W, Goetze B, Jahn HM, Huang W, Steffens H, Schomburg ED, Pérez-Samartín A, Pérez-Cerdá F, Bakhtiari D, Matute C, Löwel S, Griesinger C, Hirrlinger J, Kirchhoff F, Nave KA (2016) Oligodendroglial NMDA receptors regulate glucose import and axonal energy metabolism. Neuron 91(1):119–132. https://doi.org/10.1016/j.neuron.2016.05.016
Neufeld-Cohen A, Robles MS, Aviram R, Manella G, Adamovich Y, Ladeuix B, Nir D, Rousso-Noori L, Kuperman Y, Golik M, Mann M, Asher G (2016) Circadian control of oscillations in mitochondrial rate-limiting enzymes and nutrient utilization by PERIOD proteins. Proc Natl Acad Sci USA 113:E1673–E1682. https://doi.org/10.1073/pnas.1519650113
Taylor CM, Marta CB, Claycomb RJ, Han DK, Rasband MN, Coetzee T, Pfeiffer SE (2004) Proteomic mapping provides powerful insights into functional myelin biology. Proc Natl Acad Sci USA 101:4643–4648. https://doi.org/10.1073/pnas.0400922101
Mugnaini E, Osen KK, Schnapp B, Friedrich VL Jr (1977) Distribution of Schwann cell cytoplasm and plasmalemmal vesicles (caveolae) in peripheral myelin sheaths. An electron microscopic study with thin sections and freeze-fracturing. J Neurocytol 6:647–668
Bhat S, Pfeiffer SE (1985) Subcellular distribution and developmental expression of cholesterol ester hydrolases in fetal rat brain cultures. J Neurochem 45:1356–1362. https://doi.org/10.1111/j.1471-4159.1985.tb07200.x
Rinholm JE, Vervaeke K, Tadross MR, Tkachuk AN, Kopek BG, Brown TA, Bergersen LH, Clayton DA (2016) Movement and structure of mitochondria in oligodendrocytes and their myelin sheaths. Glia 64(5):810–825. https://doi.org/10.1002/glia.22965
Ravera S, Bartolucci M, Calzia D, Aluigi MG, Ramoino P, Morelli A, Panfoli I (2013) Tricarboxylic acid cycle-sustained oxidative phosphorylation in isolated myelin vesicles. Biochimie 95:1991–1998. https://doi.org/10.1016/j.biochi.2013.07.003
Fünfschilling U, Supplie LM, Mahad D, Boretius S, Saab AS, Edgar J, Brinkmann BG, Kassmann CM, Tzvetanova ID, Möbius W, Diaz F, Meijer D, Suter U, Hamprecht B, Sereda MW, Moraes CT, Frahm J, Goebbels S, Nave KA (2012) Glycolytic oligodendrocytes maintain myelin and long-term axonal integrity. Nature 485:517–521. https://doi.org/10.1038/nature11007
Lee Y, Morrison BM, Li Y, Lengacher S, Farah MH, Hoffman PN, Liu Y, Tsingalia A, Jin L, Zhang PW, Pellerin L, Magistretti PJ, Rothstein JD (2012) Oligodendroglia metabolically support axons and contribute to neurodegeneration. Nature 487(7408):443–448. https://doi.org/10.1038/nature11314
Bass J, Takahashi JS (2010) Circadian integration of metabolism and energetics. Science 330(6009):1349–1354. https://doi.org/10.1126/science.1195027
de Goede P, Wefers J, Brombacher EC, Schrauwen P, Kalsbeek A (2018) Circadian rhythms in mitochondrial respiration. J Mol Endocrinol 60(3):R115–R130. https://doi.org/10.1530/JME-17-0196
Ramsey KM, Yoshino J, Brace CS, Abrassart D, Kobayashi Y, Marcheva B, Hong HK, Chong JL, Buhr ED, Lee C, Takahashi JS, Imai S, Bass J (2009) Circadian clock feedback cycle through NAMPT-mediated NAD + biosynthesis. Science 324(5927):651–654. https://doi.org/10.1126/science.1171641
Musiek ES, Lim MM, Yang G, Bauer AQ, Qi L, Lee Y, Roh JH, Ortiz-Gonzalez X, Dearborn JT, Culver JP, Herzog ED, Hogenesch JB, Wozniak DF, Dikranian K, Giasson BI, Weaver DR, Holtzman DM, Fitzgerald GA (2013) Circadian clock proteins regulate neuronal redox homeostasis and neurodegeneration. J Clin Invest 123(12):5389–5400. https://doi.org/10.1172/JCI70317
Ravera S, Panfoli I (2015) Role of myelin sheath energy metabolism in neurodegenerative diseases. Neural Regen Res 10(10):1570–1571. http://www.nrronline.org/text.asp?2015/10/10/1570/167749
Valanne L, Ketonen L, Majander A, Suomalainen A, Pihko H (1998) Neuroradiologic findings in children with mitochondrial disorders. AJNR Am J Neuroradiol 19(2):369–377
Prolo LM, Takahashi JS, Herzog ED (2005) Circadian rhythm generation and entrainment in astrocytes. J Neurosci 2005; 25:404–408. https://doi.org/10.1523/JNEUROSCI.4133-04.2005
Beaulé C, Swanstrom A, Leone MJ, Herzog ED (2009) Circadian modulation of gene expression, but not glutamate uptake, in mouse and rat cortical astrocytes. PLoS ONE 2009; 4:e7476. https://doi.org/10.1371/journal.pone.0007476
Womac AD1, Burkeen JF, Neuendorff N, Earnest DJ, Zoran MJ (2009) Circadian rhythms of extracellular ATP accumulation in suprachiasmatic nucleus cells and cultured astrocytes. Eur J Neurosci 30(5):869–876. https://doi.org/10.1111/j.1460-9568.2009.06874.x
Marpegan L, Swanstrom AE, Chung K, Simon T, Haydon PG, Khan SK, Liu AC, Herzog ED, Beaulé C (2011) Circadian regulation of ATP release in astrocytes. J Neurosci 31(23):8342–8350. https://doi.org/10.1523/JNEUROSCI.6537-10.2011
van den Pol AN, Finkbeiner SM, Cornell-Bell AH (1992) Calcium excitability and oscillations in suprachiasmatic nucleus neurons and glia in vitro. J Neurosci 12(7):2648–2664. https://doi.org/10.1523/JNEUROSCI.12-07-02648.1992
Burkeen JF, Womac AD, Earnest DJ, Zoran MJ (2011) Mitochondrial calcium signaling mediates rhythmic extracellular ATP accumulation in suprachiasmatic nucleus astrocytes. J Neurosci 31(23):8432–8440. https://doi.org/10.1523/JNEUROSCI.6576-10.2011
Brancaccio M, Patton AP, Chesham JE, Maywood ES, Hastings MH (2017) Astrocytes control circadian timekeeping in the suprachiasmatic nucleus via glutamatergic signaling. Neuron 2017 Mar 22 93(6):1420–1435.e5. https://doi.org/10.1016/j.neuron.2017.02.030
Barca-Mayo O, Pons-Espinal M, Follert P, Armirotti A, Berdondini L, De Pietri Tonelli D (2017) Astrocyte dletion of Bmal1 alters daily locomotor activity and cognitive functions via GABA signalling. Nat Commun 8:14336. https://doi.org/10.1038/ncomms14336
Tso CF, Simon T, Greenlaw AC, Puri T, Mieda M, Herzog ED. Astrocytes regulate daily rhythms in the suprachiasmatic nucleus and behavior. Curr Biol. 2017 Apr 3;27(7):1055–1061. https://doi.org/10.1016/j.cub.2017.02.037
Nakazato R, Kawabe K, Yamada D, Ikeno S, Mieda M, Shimba S, Hinoi E, Yoneda Y, Takarada T (2017) Disruption of Bmal1 impairs blood-brain barrier integrity via pericyte dysfunction. J Neurosci 37:10052–10062. https://doi.org/10.1523/JNEUROSCI.3639-16.2017
Lananna BV, Nadarajah CJ, Izumo M, Cedeño MR, Xiong DD, Dimitry J, Tso CF, McKee CA, Griffin P, Sheehan PW, Haspel JA, Barres BA, Liddelow SA, Takahashi JS, Karatsoreos IN, Musiek ES (2018) Cell-autonomous regulation of astrocyte activation by the circadian clock protein BMAL1. Cell Rep 2018 25(1):1–9.e5. https://doi.org/10.1016/j.celrep.2018.09.015
Lucassen EA, Coomans CP, van Putten M, de Kreij SR, van Genugten JH, Sutorius RP, de Rooij KE, van der Velde M, Verhoeve SL, Smit JW, Löwik CW, Smits HH, Guigas B, Aartsma-Rus AM, Meijer JH (2016) Environmental 24-hr cycles are essential for health. Curr Biol 26(14):1843–1853. https://doi.org/10.1016/j.cub.2016.05.038
Ohta H, Mitchell AC, McMahon DG (2006) Constant light disrupts the developing mouse biological clock. Pediatr Res 60(3):304–308. https://doi.org/10.1203/01.pdr.0000233114.18403.66 (Epub 2006 Jul 20)
Rivkees SA, Mayes L, Jacobs H, Gross I (2004) Rest-activity patterns of premature infants are regulated by cycled lighting. Pediatrics 113:833–839. https://doi.org/10.1542/peds.113.4.833
Guyer C, Huber R, Fontijn J, Bucher HU, Nicolai H, Werner H, Molinari L, Latal B, Jenni OG (2012) Cycled light exposure reduces fussing and crying in very preterm infants. Pediatrics 130:e145–e151. https://doi.org/10.1542/peds.2011-2671
Vásquez-Ruiz S, Maya-Barrios JA, Torres-Narváez P, Vega-Martínez BR, Rojas-Granados A, Escobar C, Angeles-Castellanos M (2014) A light/dark cycle in the NICU accelerates body weight gain and shortens time to discharge in preterm infants. Early Hum Dev 90:535–540. https://doi.org/10.1016/j.earlhumdev.2014.04.015
Morag I, Ohlsson A (2016) Cycled light in the intensive care unit for preterm and low birth weight infants. Cochrane Database Syst Rev 8:CD006982. https://doi.org/10.1002/14651858.CD006982.pub4
Brandon DH, Silva SG, Park J, Malcolm W, Kamhawy H, Holditch-Davis D (2017) Timing for the introduction of cycled Light for extremely preterm infants: a randomized controlled trial. Res Nurs Health 40(4):294–310. https://doi.org/10.1002/nur.21797.10.1002%2Fnur.21797
Rea MS, Figueiro MG (2016) The NICU lighted environment. Newborn Infant Nurs Rev 16(4):195–202. https://doi.org/10.1053/j.nainr.2016.09.009
Back SA (2017) White matter injury in the preterm infant: pathology and mechanisms. Acta Neuropathol 134:331–349. https://doi.org/10.1007/s00401-017-1718-6
Paus T, Keshavan M, Giedd JN (2008) Why do many psychiatric disorders emerge during adolescence? Nat Rev Neurosci 9(12):947–957. https://doi.org/10.1038/nrn2513
Galván A (2017) Adolescence, brain maturation and mental health. Nat Neurosci 20(4):503–504
Mazurek MO, Sohl K (2016) Sleep and behavioral problems in children with autism spectrum disorder. J Autism Dev Disord 46:1906–1915. https://doi.org/10.1007/s10803-016-2723-7
Robinson-Shelton A, Malow BA (2016) Sleep disturbances in neurodevelopmental disorders. Curr Psychiatry Rep 18:6. https://doi.org/10.1007/s11920-015-0638-1
Engelhardt CR, Mazurek MO, Sohl K (2013) Media use and sleep among boys with autism spectrum disorder, ADHD, or typical development. Pediatrics 132:1081–1089. https://doi.org/10.1542/peds.2013-2066
Mazurek MO, Engelhardt CR, Hilgard J, Sohl K (2016) Bedtime electronic media use and sleep in children with autism spectrum disorder. J Dev Behav Pediatr 37(7):525–531. https://doi.org/10.1097/DBP.0000000000000314
Wood B, Rea MS, Plitnick B, Figueiro MG (2013) Light level and duration of exposure determine the impact of self-luminous tablets on melatonin suppression. Appl Ergon 44:237–240. https://doi.org/10.1016/j.apergo.2012.07.008
Chang AM, Aeschbach D, Duffy JF, Czeisler CA (2015) Evening use of light-emitting eReaders negatively affects sleep, circadian timing, and next-morning alertness. Proc Natl Acad Sci USA 112:1232–1237. https://doi.org/10.1073/pnas.1418490112
Gronli J, Byrkjedal IK, Bjorvatn B, Nodtvedt O, Hamre B, Pallesen S (2016) Reading from an iPad or from a book in bed: the impact on human sleep. A randomized controlled crossover trial. Sleep Med 21:86–92. https://doi.org/10.1016/j.sleep.2016.02.006
Kleinhans NM, Pauley G, Richards T, Neuhaus E, Martin N, Corrigan NM, Shaw DW, Estes A, Dager SR (2012) Age-related abnormalities in white matter microstructure in autism spectrum disorders. Brain Res 1479:1–16. https://doi.org/10.1016/j.brainres.2012.07.056
Ameis SH, Catani M (2015) Altered white matter connectivity as a neural substrate for social impairment in Autism. Spectrum Disorder Cortex 62:158–181. https://doi.org/10.1016/j.cortex.2014.10.014
Maricich SM, Azizi P, Jones JY, Morriss MC, Hunter JV, Smith EO, Miller G (2007) Myelination as assessed by conventional MR imaging is normal in young children with idiopathic developmental delay. AJNR Am J Neuroradiol 28(8):1602. https://doi.org/10.3174/ajnr.A0602
Samara A, Feng K, Pivik RT, Jarratt KP, Badger TM, Ou X (2018) White matter microstructure correlates with memory performance in healthy children: a diffusion tensor imaging study. J Neuroimaging Nov https://doi.org/10.1111/jon.12580
Telzer EH, Fuligni AJ, Lieberman MD, Galván A (2013) The effects of poor quality sleep on brain function and risk taking in adolescence. Neuroimage 71:275–283. https://doi.org/10.1016/j.neuroimage.2013.01.025
Telzer EH, Goldenberg D, Fuligni AJ, Lieberman MD, Gálvan A (2015) Sleep variability in adolescence is associated with altered brain development. Dev Cogn Neurosci 14:16–22. https://doi.org/10.1016/j.dcn.2015.05.007
Tashjian SM, Goldenberg D, Galván A (2017) Neural connectivity moderates the association between sleep and impulsivity in adolescents. Dev Cogn Neurosci 27:35–44. https://doi.org/10.1016/j.dcn.2017.07.006
Wittmann M, Dinich J, Merrow M, Roenneberg T (2006) Social jetlag: misalignment of biological and social time. Chronobiol Int 23(1–2):497–509. https://doi.org/10.1080/07420520500545979
Touitou Y, Touitou D, Reinberg A (2016) Disruption of adolescents’ circadian clock: the vicious circle of media use, exposure to light at night, sleep loss and risk behaviors. J Physiol Paris 110(4 Pt B):467–479. https://doi.org/10.1016/j.jphysparis.2017.05.001
Roenneberg T, Merrow M (2016) The circadian clock and human health. Curr Biol 26:R432–R443. https://doi.org/10.1016/j.cub.2016.04.011
Dunster GP, de la Iglesia L, Ben-Hamo M, Nave C, Fleischer JG, Panda S, de la Iglesia HO (2018) Sleepmore in Seattle: later school start times are associated with more sleep and better performance in high school students. Sci Adv 2018 Dec 12;4(12):eaau6200. https://doi.org/10.1126/sciadv.aau6200
Scalfari A, Lederer C, Daumer M, Nicholas R, Ebers GC, Muraro PA (2016) The relationship of age with the clinical phenotype in multiple sclerosis. Mult Scler 22(13):1750–1758. https://doi.org/10.1177/1352458516630396
Caminero A, Bartolomé M (2011) Sleep disturbances in multiple sclerosis. J Neurol Sci 309(1–2):86–91. https://doi.org/10.1016/j.jns.2011.07.015
Lunde HM, Bjorvatn B, Myhr KM, Bø L (2013) Clinical assessment and management of sleep disorders in multiple sclerosis: a literature review. Acta Neurol Scand Suppl (196):24–30. https://doi.org/10.1111/ane.12046
Chinnadurai SA, Gandhirajan D, Pamidimukala V, Kesavamurthy B, Venkatesan SA (2018) Analysing the relationship between polysomnographic measures of sleep with measures of physical and cognitive fatigue in people with multiple sclerosis. Mult Scler Relat Disord 24:32–37. https://doi.org/10.1016/j.msard.2018.05.016
Nociti V, Losavio FA, Gnoni V, Losurdo A, Testani E, Vollono C, Frisullo G, Brunetti V, Mirabella M, Della Marca G (2017) Sleep and fatigue in multiple sclerosis: A questionnaire-based, cross-sectional, cohort study. J Neurol Sci 372:387–392. https://doi.org/10.1016/j.jns.2016.10.040
Braley TJ, Kratz AL, Kaplish N, Chervin RD (2016) Sleep and cognitive function in multiple sclerosis. Sleep 39(8):1525–1533. https://doi.org/10.5665/sleep.6012
Vitkova M, Gdovinova Z, Rosenberger J, Szilasiova J, Mikula P, Stewart RE, Groothoff JW, van Dijk JP (2018) Is poor sleep quality associated with greater disability in patients with multiple sclerosis? Behav Sleep Med 16(2):106–116. https://doi.org/10.1080/15402002.2016.1173555
Kern S, Krause I, Horntrich A, Thomas K, Aderhold J, Ziemssen T (2013) Cortisol awakening response is linked to disease course and progression in multiple sclerosis. PLoS ONE 8(4):e60647. https://doi.org/10.1371/journal.pone.0060647
Akpinar Z, Tokgöz S, Gökbel H, Okudan N, Uğuz F, Yilmaz G (2008) The association of nocturnal serum melatonin levels with major depression in patients with acute multiple sclerosis. Psychiatry Res 161(2):253–257. https://doi.org/10.1016/j.psychres.2007.11.022
Damasceno A, Moraes AS, Farias A, Damasceno BP, dos Santos LM, Cendes F (2015) Disruption of melatonin circadian rhythm production is related to multiple sclerosis severity: a preliminary study. J Neurol Sci 353(1–2):166–168. https://doi.org/10.1016/j.jns.2015.03.040
Melamud L, Golan D, Luboshitzky R, Lavi I, Miller A (2012) Melatonin dysregulation, sleep disturbances and fatigue in multiple sclerosis. J Neurol Sci 314(1–2):37–40. https://doi.org/10.1016/j.jns.2011.11.003
Streckis V, Skurvydas A, Mamkus G (2014) Effect of the time of day on central and peripheral fatigue during 2-min maximal voluntary contractions in persons with multiple sclerosis: gender differences. J Electromyogr Kinesiol 24(5):601–606. https://doi.org/10.1016/j.jelekin.2014.06.001
Kratz AL, Murphy SL, Braley TJ (2017) Ecological momentary assessment of pain, fatigue, depressive, and cognitive symptoms reveals significant daily variability in multiple sclerosis. Arch Phys Med Rehabil 98(11):2142–2150. https://doi.org/10.1016/j.apmr.2017.07.002
Wens I, Hansen D (2017) Muscle strength, but not muscle oxidative capacity, varies between the morning and the afternoon in patients with multiple sclerosis: a pilot study. Am J Phys Med Rehabil 96(11):828–830. https://doi.org/10.1097/PHM.0000000000000703
Golalipour M, Maleki Z, Farazmandfar T, Shahbazi M (2017) PER3 VNTR polymorphism in multiple sclerosis: a new insight to impact of sleep disturbances in MS. Mult Scler Relat Disord 17:84–86. https://doi.org/10.1016/j.msard.2017.07.005
Lavtar P, Rudolf G, Maver A, Hodžić A, Starčević Čizmarević N, Živković M, Šega Jazbec S, Klemenc Ketiš Z, Kapović M, Dinčić E, Raičević R, Sepčić J, Lovrečić L, Stanković A, Ristić S, Peterlin B (2018) Association of circadian rhythm genes ARNTL/BMAL1 and CLOCK with multiple sclerosis. PLoS ONE 13(1):e0190601. https://doi.org/10.1371/journal.pone.0190601
Wipfler P, Heikkinen A, Harrer A, Pilz G, Kunz A, Golaszewski SM, Reuss R, Oschmann P, Kraus J (2013) Circadian rhythmicity of inflammatory serum parameters: a neglected issue in the search of biomarkers in multiple sclerosis. J Neurol 260(1):221–227. https://doi.org/10.1007/s00415-012-6622-3
Procaccini C, De Rosa V, Pucino V, Formisano L, Matarese G (2015) Animal models of Multiple Sclerosis. Eur J Pharmacol 759:182–191. https://doi.org/10.1016/j.ejphar.2015.03.042
Buenafe AC (2012) Diurnal rhythms are altered in a mouse model of multiple sclerosis. J Neuroimmunol 243(1–2):12–17. https://doi.org/10.1016/j.jneuroim.2011.12.002
Sutton CE, Finlay CM, Raverdeau M, Early JO, DeCourcey J, Zaslona Z, O’Neill LAJ, Mills KHG, Curtis AM (2017) Loss of the molecular clock in myeloid cells exacerbates T cell-mediated CNS autoimmune disease. Nat Commun 8(1):1923. https://doi.org/10.1038/s41467-017-02111-0
Vallée A, Lecarpentier Y, Guillevin R, Vallée JN (2018) Demyelination in multiple sclerosis: reprogramming energy metabolism and potential PPARγ agonist treatment approaches. Int J Mol Sci 19(4): E1212. https://doi.org/10.3390/ijms19041212
Eckel-Mahan KL, Patel VR, de Mateo S, Orozco-Solis R, Ceglia NJ, Sahar S, Dilag-Penilla SA, Dyar KA, Baldi P, Sassone-Corsi P. Reprogramming of the circadian clock by nutritional challenge. Cell 155(7):1464–1478. https://doi.org/10.1016/j.cell.2013.11.034
Narasimamurthy R, Hatori M, Nayak SK, Liu F, Panda S, Verma IM (2012) Circadian clock protein cryptochrome regulates the expression of proinflammatory cytokines. Proc Natl Acad Sci USA 109(31):12662–12667. https://doi.org/10.1073/pnas.1209965109
Spengler ML, Kuropatwinski KK, Comas M, Gasparian AV, Fedtsova N, Gleiberman AS, Gitlin II, Artemicheva NM, Deluca KA, Gudkov AV, Antoch MP (2012) Core circadian protein CLOCK is a positive regulator of NF-κB–mediated transcription. Proc Natl Acad Sci USA 109(37):E2457–E2465. https://doi.org/10.1073/pnas.1206274109
Bates GP, Dorsey R, Gusella JF, Hayden MR, Kay C, Leavitt BR, Nance M, Ross CA, Scahill RI, Wetzel R, Wild EJ, Tabrizi SJ (2015) Huntington disease. Nat Rev Dis Primers 1:15005. https://doi.org/10.1038/nrdp.2015.5
Bartzokis G, Lu PH, Tishler TA, Fong SM, Oluwadara B, Finn JP, Huang D, Bordelon Y, Mintz J, Perlman S (2007) Myelin breakdown and iron changes in Huntington’s disease: pathogenesis and treatment implications. Neurochem Res 32(10):1655–1664. https://doi.org/10.1007/s11064-007-9352-7
Poudel GR, Stout JC, Domínguez DJF, Churchyard A, Chua P, Egan GF, Georgiou-Karistianis N (2015) Longitudinal change in white matter microstructure in Huntington’s disease: The IMAGE-HD study. Neurobiol Dis 74:406–412. https://doi.org/10.1016/j.nbd.2014.12.009
Faria AV, Ratnanather JT, Tward DJ, Lee DS, van den Noort F, Wu D, Brown T, Johnson H, Paulsen JS, Ross CA, Younes L, Miller MI, PREDICT-HD Investigators and Coordinators of the Huntington Study Group (2016) Linking white matter and deep gray matter alterations in premanifest Huntington disease. Neuroimage Clin 11:450–460. https://doi.org/10.1016/j.nicl.2016.02.014
Bourbon-Teles J, Bells S, Jones DK, Coulthard E, Rosser A, Metzler-Baddeley C (2017) Myelin breakdown in human Huntington’s disease: multi-modal evidence from diffusion MRI and quantitative magnetization transfer. Neuroscience pii: S 0306-4522(17):30376–30377. https://doi.org/10.1016/j.neuroscience.2017.05.042
Xiang Z, Valenza M, Cui L, Leoni V, Jeong HK, Brilli E, Zhang J, Peng Q, Duan W, Reeves SA, Cattaneo E, Krainc D (2011) Peroxisome-proliferator-activated receptor gamma coactivator 1 α contributes to dysmyelination in experimental models of Huntington’s disease. J Neurosci 31(26):9544–9553. https://doi.org/10.1523/JNEUROSCI.1291-11.2011
Jin J, Peng Q, Hou Z, Jiang M, Wang X, Langseth AJ, Tao M, Barker PB, Mori S, Bergles DE, Ross CA, Detloff PJ, Zhang J, Duan W (2015) Early white matter abnormalities, progressive brain pathology and motor deficits in a novel knock-in mouse model of Huntington’s disease. Hum Mol Genet 24(9):2508–2527. https://doi.org/10.1093/hmg/ddv016
Teo RT, Hong X, Yu-Taeger L, Huang Y, Tan LJ, Xie Y, To XV, Guo L, Rajendran R, Novati A, Calaminus C, Riess O, Hayden MR, Nguyen HP, Chuang KH, Pouladi MA (2016) Structural and molecular myelination deficits occur prior to neuronal loss in the YAC128 and BACHD models of Huntington disease. Hum Mol Genet 25(13):2621–2632. https://doi.org/10.1093/hmg/ddw122
Shankaran M, Di Paolo E, Leoni V, Caccia C, Ferrari Bardile C, Mohammed H, Di Donato S, Kwak S, Marchionini D, Turner S, Cattaneo E, Valenza M (2017) Early and brain region-specific decrease of de novo cholesterol biosynthesis in Huntington’s disease: a cross-validation study in Q175 knock-in mice. Neurobiol Dis 98:66–76. https://doi.org/10.1016/j.nbd.2016.11.013
Di Pardo A, Amico E, Maglione V (2016) Impaired levels of gangliosides in the corpus callosum of huntington disease animal models. Front Neurosci 10:457. https://doi.org/10.3389/fnins.2016.00457
Huang B, Wei W, Wang G, Gaertig MA, Feng Y, Wang W, Li XJ, Li S (2015) Mutant huntingtin downregulates myelin regulatory factor-mediated myelin gene expression and affects mature oligodendrocytes. Neuron 85(6):1212–1226. https://doi.org/10.1016/j.neuron.2015.02.026
Morton AJ, Wood NI, Hastings MH, Hurelbrink C, Barker RA, Maywood ES (2005) Disintegration of the sleep-wake cycle and circadian timing in Huntington’s disease. J Neurosci 25(1):157–163. https://doi.org/10.1523/JNEUROSCI.3842-04.2005
Goodman AO, Rogers L, Pilsworth S, McAllister CJ, Shneerson JM, Morton AJ, Barker RA (2011) Asymptomatic sleep abnormalities are a common early feature in patients with Huntington’s disease. Curr Neurol Neurosci Rep 11(2):211–217. https://doi.org/10.1007/s11910-010-0163-x
Kalliolia E, Silajdžić E, Nambron R, Hill NR, Doshi A, Frost C, Watt H, Hindmarsh P, Björkqvist M, Warner TT (2014) Plasma melatonin is reduced in Huntington’s disease. Mov Disord 29(12):1511–1515. https://doi.org/10.1002/mds.26003
van Wamelen DJ, Aziz NA, Roos RA, Swaab DF (2014) Hypothalamic alterations in Huntington’s disease patients: comparison with genetic rodent models. J Neuroendocrinol 26(11):761–775. https://doi.org/10.1111/jne.12190
Kudo T, Schroeder A, Loh DH, Kuljis D, Jordan MC, Roos KP, Colwell CS (2011) Dysfunctions in circadian behavior and physiology in mouse models of Huntington’s disease. Exp Neurol 228(1):80–90. https://doi.org/10.1016/j.expneurol.2010.12.011
Loh DH, Kudo T, Truong D, Wu Y, Colwell CS (2013) The Q175 mouse model of Huntington’s disease shows gene dosage- and age-related decline in circadian rhythms of activity and sleep. PLoS ONE 8(7):e69993. https://doi.org/10.1371/journal.pone.006999330
Kuljis DA, Gad L, Loh DH, MacDowell Kaswan Z, Hitchcock ON, Ghiani CA, Colwell CS (2016) Sex Differences in Circadian Dysfunction in the BACHD Mouse Model of Huntington’s Disease. PLoS ONE 11(2):e0147583. https://doi.org/10.1371/journal.pone.0147583
Wang HB, Loh DH, Whittaker DS, Cutler T, Howland D, Colwell CS (2018) Time-restricted feeding improves circadian dysfunction as well as motor symptoms in the Q175 Mouse Model of Huntington’s Disease. eNeuro 5: 1. https://doi.org/10.1523/ENEURO.0431-17.2017
Whittaker DS, Loh DH, Wang HB, Tahara Y, Kuljis D, Cutler T, Ghiani CA, Shibata S, Block GD, Colwell CS (2018) Circadian-based treatment strategy effective in the BACHD mouse model of Huntington’s Disease. J Biol Rhythms 33(5):535–554. https://doi.org/10.1177/0748730418790401
Acknowledgements
Cristina A. Ghiani is supported by a grant from the National Institute of General Medical Sciences (RO1GM112942). Images were acquired using equipment in core facilities supported by the National Institute of Child Health Development under award number: 5U54HD087101.
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Colwell, C.S., Ghiani, C.A. Potential Circadian Rhythms in Oligodendrocytes? Working Together Through Time. Neurochem Res 45, 591–605 (2020). https://doi.org/10.1007/s11064-019-02778-5
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DOI: https://doi.org/10.1007/s11064-019-02778-5