#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

24-Hour Rhythms of DNA Methylation and Their Relation with Rhythms of RNA Expression in the Human Dorsolateral Prefrontal Cortex


Circadian rhythms are intrinsic 24-hour biological rhythms that influence many aspects of human biology, including normal and abnormal human brain functions such as cognition and seizures. Circadian rhythms are maintained by a near 24-hour feedback loop mediated by a series of “clock” genes that are similar across species, including humans. However, the specific mechanisms underlying the circadian regulation of gene transcription are unknown. DNA methylation is an epigenetic mechanism that can influence gene expression without changes in DNA sequence. The 24-hour rhythms of DNA methylation are one mechanism contributing to 24-hour rhythms of clock gene expression in fungi. However, this has not been demonstrated in mammals including humans. In this study, we examined levels of DNA methylation at>400,000 sites across the genome in the brains of 738 human subjects and showed significant 24-hour rhythms of DNA methylation. Moreover, we showed that for specific locations of DNA methylation site, these rhythms of methylation were linked to rhythms of gene expression. This is important because it suggests that circadian rhythms of DNA methylation may be an important mechanism underlying circadian rhythms of gene expression in the human brain, and hence circadian rhythms of normal and abnormal brain function.


Vyšlo v časopise: 24-Hour Rhythms of DNA Methylation and Their Relation with Rhythms of RNA Expression in the Human Dorsolateral Prefrontal Cortex. PLoS Genet 10(11): e32767. doi:10.1371/journal.pgen.1004792
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004792

Souhrn

Circadian rhythms are intrinsic 24-hour biological rhythms that influence many aspects of human biology, including normal and abnormal human brain functions such as cognition and seizures. Circadian rhythms are maintained by a near 24-hour feedback loop mediated by a series of “clock” genes that are similar across species, including humans. However, the specific mechanisms underlying the circadian regulation of gene transcription are unknown. DNA methylation is an epigenetic mechanism that can influence gene expression without changes in DNA sequence. The 24-hour rhythms of DNA methylation are one mechanism contributing to 24-hour rhythms of clock gene expression in fungi. However, this has not been demonstrated in mammals including humans. In this study, we examined levels of DNA methylation at>400,000 sites across the genome in the brains of 738 human subjects and showed significant 24-hour rhythms of DNA methylation. Moreover, we showed that for specific locations of DNA methylation site, these rhythms of methylation were linked to rhythms of gene expression. This is important because it suggests that circadian rhythms of DNA methylation may be an important mechanism underlying circadian rhythms of gene expression in the human brain, and hence circadian rhythms of normal and abnormal brain function.


Zdroje

1. TakahashiJS, HongHK, KoCH, McDearmonEL (2008) The genetics of mammalian circadian order and disorder: implications for physiology and disease. Nat Rev Genet 9: 764–775.

2. HastingsMH, ReddyAB, MaywoodES (2003) A clockwork web: circadian timing in brain and periphery, in health and disease. Nat Rev Neurosci 4: 649–661.

3. KoikeN, YooSH, HuangHC, KumarV, LeeC, et al. (2012) Transcriptional Architecture and Chromatin Landscape of the Core Circadian Clock in Mammals. Science

4. MasriS, Sassone-CorsiP (2010) Plasticity and specificity of the circadian epigenome. Nat Neurosci 13: 1324–1329.

5. BeldenWJ, LewisZA, SelkerEU, LorosJJ, DunlapJC (2011) CHD1 remodels chromatin and influences transient DNA methylation at the clock gene frequency. PLoS Genet 7: e1002166.

6. AzziA, DallmannR, CasserlyA, RehrauerH, PatrignaniA, et al. (2014) Circadian behavior is light-reprogrammed by plastic DNA methylation. Nat Neurosci 17: 377–382.

7. StevensonTJ, PrendergastBJ (2013) Reversible DNA methylation regulates seasonal photoperiodic time measurement. Proc Natl Acad Sci U S A 110: 16651–16656.

8. VollmersC, SchmitzRJ, NathansonJ, YeoG, EckerJR, et al. (2012) Circadian oscillations of protein-coding and regulatory RNAs in a highly dynamic mammalian liver epigenome. Cell Metab 16: 833–845.

9. SmithEE, JonidesJ (1999) Storage and executive processes in the frontal lobes. Science 283: 1657–1661.

10. CallicottJH, BertolinoA, MattayVS, LangheimFJ, DuynJ, et al. (2000) Physiological Dysfunction of the Dorsolateral Prefrontal Cortex in Schizophrenia Revisited. Cerebral cortex Cerebral Corte 1078–1092.

11. LiJZ, BunneyBG, MengF, HagenauerMH, WalshDM, et al. (2013) Circadian patterns of gene expression in the human brain and disruption in major depressive disorder. Proc Natl Acad Sci U S A 110: 9950–9955.

12. CzeislerCA, DumontM, DuffyJF, SteinbergJD, RichardsonGS, et al. (1992) Association of sleep-wake habits in older people with changes in output of circadian pacemaker. Lancet 340: 933–936.

13. CainSW, DennisonCF, ZeitzerJM, GuzikAM, KhalsaSB, et al. (2010) Sex differences in phase angle of entrainment and melatonin amplitude in humans. J Biol Rhythms 25: 288–296.

14. DuffyJF, CainSW, ChangAM, PhillipsAJ, MunchMY, et al. (2011) Sex difference in the near-24-hour intrinsic period of the human circadian timing system. Proc Natl Acad Sci U S A 108 Suppl 3: 15602–15608.

15. HatfieldCF, HerbertJ, van SomerenEJ, HodgesJR, HastingsMH (2004) Disrupted daily activity/rest cycles in relation to daily cortisol rhythms of home-dwelling patients with early Alzheimer's dementia. Brain 127: 1061–1074.

16. EtchegarayJP, LeeC, WadePA, ReppertSM (2003) Rhythmic histone acetylation underlies transcription in the mammalian circadian clock. Nature 421: 177–182.

17. SaharS, Sassone-CorsiP (2013) The epigenetic language of circadian clocks. Handb Exp Pharmacol 217: 29–44.

18. BrownSE, FragaMF, WeaverIC, BerdascoM, SzyfM (2007) Variations in DNA methylation patterns during the cell cycle of HeLa cells. Epigenetics 2: 54–65.

19. KangaspeskaS, StrideB, MetivierR, Polycarpou-SchwarzM, IbbersonD, et al. (2008) Transient cyclical methylation of promoter DNA. Nature 452: 112–115.

20. BeldenWJ, LewisZA, SelkerEU, LorosJJ, DunlapJC (2011) CHD1 remodels chromatin and influences transient DNA methylation at the clock gene frequency. PLoS Genet 7: e1002166.

21. BonschD, HothornT, KrieglsteinC, KochM, NehmerC, et al. (2007) Daily variations of homocysteine concentration may influence methylation of DNA in normal healthy individuals. Chronobiol Int 24: 315–326.

22. JonesPA (2012) Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nature Reviews Genetics 13: 484–492.

23. MaekawaF, ShimbaS, TakumiS, SanoT, SuzukiT, et al. (2012) Diurnal expression of Dnmt3b mRNA in mouse liver is regulated by feeding and hepatic clockwork. Epigenetics 7: 1046–1056.

24. LimAS, MyersAJ, YuL, BuchmanAS, DuffyJF, et al. (2013) Sex difference in daily rhythms of clock gene expression in the aged human cerebral cortex. J Biol Rhythms 28: 117–129.

25. LimAS, ChangAM, ShulmanJM, RajT, ChibnikLB, et al. (2012) A common polymorphism near PER1 and the timing of human behavioral rhythms. Ann Neurol 72: 324–334.

26. WittingW, KwaIH, EikelenboomP, MirmiranM, SwaabDF (1990) Alterations in the circadian rest-activity rhythm in aging and Alzheimer's disease. Biol Psychiatry 27: 563–572.

27. BennettDA, SchneiderJA, BuchmanAS, BarnesLL, BoylePA, et al. (2012) Overview and findings from the rush Memory and Aging Project. Curr Alzheimer Res 9: 646–663.

28. BennettDA, SchneiderJA, ArvanitakisZ, WilsonRS (2012) Overview and findings from the religious orders study. Curr Alzheimer Res 9: 628–645.

29. BennettDA, YuL, YangJ, SrivastavaGP, AubinC, et al. (2014) Epigenomics of Alzheimer's disease. Transl Res doi:10.1016/j.trsl.2014.05.006

30. De JagerPL, SrivastavaG, LunnonK, BurgessJ, SchalkwykLC, et al. (2014) Alzheimer's disease: early alterations in brain DNA methylation at ANK1, BIN1, RHBDF2 and other loci. Nat Neurosci 17: 1156–1163.

31. ChenYA, LemireM, ChoufaniS, ButcherDT, GrafodatskayaD, et al. (2013) Discovery of cross-reactive probes and polymorphic CpGs in the Illumina Infinium HumanMethylation450 microarray. Epigenetics 8: 203–209.

32. LevinJZ, YassourM, AdiconisX, NusbaumC, ThompsonDA, et al. (2010) Comprehensive comparative analysis of strand-specific RNA sequencing methods. Nature Methods 7: 709–715.

33. AdiconisX, Borges-RiveraD, SatijaR, DeLucaDS, BusbyMA, et al. (2013) Comparative analysis of RNA sequencing methods for degraded or low-input samples. Nature Methods 10: 623–629.

34. LangmeadB, TrapnellC, PopM, SalzbergSL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25.

35. BennettDA, SchneiderJA, AggarwalNT, ArvanitakisZ, ShahRC, et al. (2006) Decision rules guiding the clinical diagnosis of Alzheimer's disease in two community-based cohort studies compared to standard practice in a clinic-based cohort study. Neuroepidemiology 27: 169–176.

36. WilsonRS, BarnesLL, KruegerKR, HogansonG, BieniasJL, et al. (2005) Early and late life cognitive activity and cognitive systems in old age. J Int Neuropsychol Soc 11: 400–407.

37. McKhannG, DrachmanD, FolsteinM, KatzmanR, PriceD, et al. (1984) Clinical diagnosis of Alzheimer's disease: report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer's Disease. Neurology 34: 939–944.

38. BennettDA, SchneiderJA, ArvanitakisZ, KellyJF, AggarwalNT, et al. (2006) Neuropathology of older persons without cognitive impairment from two community-based studies. Neurology 66: 1837–1844.

39. BraakH, BraakE (1991) Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 82: 239–259.

40. National Institute on Aging and Reagan Institute Working Group of Diagnostic Criteria for the Neuropathological Assessment of Alzheimer's Disease (1997) Consensus recommendations for the postmortem diagnosis of Alzheimer's disease. Neurobiol Aging 18: S1–2.

41. SokolovePG, BushellWN (1978) The chi square periodogram: its utility for analysis of circadian rhythms. J Theor Biol 72: 131–160.

42. Jammalamadaka SR, Sengupta A (2001) Topics in circular statistics. Singapore: World Scientific. 336 p.

43. HarrowJ, FrankishA, GonzalezJM, TapanariE, DiekhansM, et al. (2012) GENCODE: the reference human genome annotation for The ENCODE Project. Genome Res 22: 1760–1774.

44. Zar JH (1999) Biostatistical Analysis. 4th edition. Saddle River, NJ: Prentice Hall. 929 p.

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2014 Číslo 11
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#