Skip to main content
SpringerLink
Log in

Rhythmic Epigenetics in Neuroendocrine and Immune Systems

  • Chapter
  • First Online:
Developmental Neuroendocrinology

Part of the book series: Masterclass in Neuroendocrinology ((MANEURO,volume 9))

Abstract

Biological rhythms in neuroendocrine and immune systems are pervasive. Daily and seasonal changes in day lengths regulate multiple physiological and immunological parameters in a diverse range of animals. A series of studies have shown that epigenetic modifications exhibit naturally occurring rhythms across short- and long-term timescales. In this chapter, we describe daily, estrous and seasonal oscillations in epigenetic enzymes in neuroendocrine substrates, peripheral reproductive tissues and immune cells (e.g. leukocytes). The predominant focus of the chapter includes enzymes involved in DNA methylation and histone modifications, such as DNA methyltransferase and histone deacetylases. The findings presented herein highlight that epigenetic modifications can be permanent as well as transient with long-term consequences on the timing of physiological and behavioural processes. Moreover, the bidirectional interaction between the immune system and the neuroendocrine nucleus that controls biological rhythmicity, the suprachiasmatic nucleus, emphasizes the need to understand rhythmic changes in epigenetic enzymes and the consequences of disrupted daily and seasonal rhythms.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Agarwal S, Rao A (1998) Modulation of chromatin structure regulates cytokine gene expression during T cell differentiation. Immunity 9:765–775

    Article  CAS  PubMed  Google Scholar 

  • Ahluwalia A, Hurteau JA, Bigsby RM, Nephew KP (2001) DNA methylation in ovarian cancer. II. Expression of DNA methyltransferases in ovarian cancer cell lines and normal ovarian epithelial cells. Gynecol Oncol 82:299–304

    Article  CAS  PubMed  Google Scholar 

  • Alvarado S, Mak T, Liu S, Storey KB, Szyf M (2015) Dynamic changes in global and gene-specific DNA methylation during hibernation in adult thirteen-lined ground squirrels, Ictidomys tridecemlineatus. J Exp Biol 218:1787–1795

    Article  PubMed  Google Scholar 

  • Asher G, Sassone-Corsi P (2015) Time for food: the intimate interplay between nutrition, metabolism and the circadian clock. Cell 161:84–92

    Article  CAS  PubMed  Google Scholar 

  • Azzi A, Dallmann R, Casserly A, Rehrauer RH, Patrignani A, Maier B, Kramer A, Brown SA (2014) Circadian behavior is light-programmed by plastic DNA methylation. Nat Neurosci 17:377–382

    Article  CAS  PubMed  Google Scholar 

  • Banks R, Delibegovic M, Stevenson TJ (2016) Photoperiod- and triiodothyronine-dependent regulation of reproductive neuropeptides, proinflammatory cytokines, and peripheral physiology in Siberian hamsters (Phodopus sungorus). J Biol Rhythm 31:299–307

    Article  CAS  Google Scholar 

  • Bilbo SD, Dhabhar FS, Viswanathan K, Saul A, Yellon SM, Nelson RJ (2002) Short day lengths augment stress-induced leukocyte trafficking and stress-induced enhancement of skin immune function. Proc Natl Acad Sci U S A 99:4067–4072

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bots M, Verbrugge I, Martin B, Salmon J, Ghisi M, Baker A, Stanley K, Shortt J, Ossenkoppele G, Zuber J, Rappaport A, Atadja P, Lowe S, Johnstone R (2014) Differentiation therapy for the treatment of t(8;21) acute myeloid leukemia using histone deacetylase inhibitors. Blood 123:1341–1352

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brehm A, Miska EA, McCance DJ, Reid JL, Bannister AJ, Kouzarides T (1998) Retinoblastoma protein recruits histone deacetylase to repress transcription. Nature 391:597–601

    Article  CAS  PubMed  Google Scholar 

  • Brenner C, Deplus R, Didelot C, Loriot A, Viré E, De Smet C, Gutierrez A, Danovi D, Bernard D, Boon T, Pelicci PG (2005) Myc represses transcription through recruitment of DNA methyltransferase corepressor. EMBO J 24:336–346

    Article  CAS  PubMed  Google Scholar 

  • Bronson FH (1990) Mammalian reproductive biology. University of Chicago Press, Chicago

    Google Scholar 

  • Coffee B, Zhang F, Warren ST, Reines D (1999) Acetylated histones are associated with FMR1 in normal but not fragile X-syndrome cells. Nat Genet 22:98–101

    Article  CAS  PubMed  Google Scholar 

  • Colón-Díaz M, Báez-Vega P, García M, Ruiz A, Monteiro JB, Fourquet J, Bayona M, Alvarez-Garriga C, Achille A, Seto E, Flores I (2012) HDAC1 and HDAC2 are differentially expressed in endometriosis. Reprod Sci 19:483–492

    Article  PubMed  PubMed Central  Google Scholar 

  • Cora MC, Looistra L, Travlos G (2015) Vaginal cytology of the laboratory rat and mouse: review and criteria for the staging of the estrous cycle using stained vaginal smears. Toxicol Pathol 43:776–793

    Article  CAS  PubMed  Google Scholar 

  • Cornacchia E, Golbus J, Maybaum J, Strahler J, Hanash S, Richardson B (1988) Hydralazine and procainamide inhibit T cell DNA methylation and induce autoreactivity. J Immunol 140:2197–2200

    CAS  PubMed  Google Scholar 

  • Cress WD, Seto E (2000) Histone deacetylases, transcriptional control, and cancer. J Cell Physiol 184:1–16

    Article  CAS  PubMed  Google Scholar 

  • Dopico XC, Evangelou M, Ferreira RC, Guo H, Pekalski M, Smyth DJ, Cooper N, Burren OS, Fulford AJ, Hennig BJ, Am P, Ziegler AG, Bonifacio E, Wallace C, Todd JA (2015) Widespread seasonal gene expression reveals annual differences in human immunity and physiology. Nat Commun 6:7000

    Article  CAS  PubMed  Google Scholar 

  • Druzd D, Matveeva O, Ince L, Harrison U, Wenyan H, Schmal C, Herzel H, Tsang AH, Kawakami N, Leliavske A, Uhl O, Yao L, Sander LE, Chen CS, Kraus K, de Juan A, Hergenhan SM, Ehlers M, Koletzko B, Haas R, Solbach W, Oster H, Scheiermann C (2017) Lymphocyte circadian clocks control lymph node trafficking and adaptive immune responses. Immunity 46:120–132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Durrin LK, Weber JL, Gorksi J (1984) Chromatin structure, transcription, and methylation of the prolactin gene domain in pituitary tumors of Fischer 344 rats. J Biol Chem 259:7086–7093

    CAS  PubMed  Google Scholar 

  • Esteller M (2008) Epigenetics in cancer. N Engl J Med 358:1148–1159

    Article  CAS  PubMed  Google Scholar 

  • Evans GS, Gibson DF, Roberts SA, Hind TM, Potten CS (1990) Proliferative change in the genital tissues of female ice during the oestrous cycle. Cell Tissue Kinet 23:619–635

    CAS  PubMed  Google Scholar 

  • Fagerberg L, Hallstrom BM, Oksvold P, Kampf C, Djureinovic D, Odeberg J, Habuka M, Tahmasebpoor S, Danielsson A, Edlund K, Asplund A, Sjostedt E, Lundberg E, Szigyarto CA, Skogs M, Takanen JO, Berling H, Tegel H, Mulder J, Nilsson P, Schwenk JM, Lindskog C, Danielsson F, Mardinoglu A, Sivertsson A, von Feilitzen K, Forsberg M, Zwahlen M, Olsson I, Navani S, Huss M, Nielsen J, Ponten F, Uhlen M (2014) Analysis of the human tissue specific expression by genome-wide integration of transcriptomics and antibody-based proteomics. Mol Cell Proteomics 13:397–406

    Article  CAS  PubMed  Google Scholar 

  • Fitzpatrick DR, Wilson CB (2003) Methylation and demethylation in the regulation of genes, cells, and responses in the immune system. Clin Immunol 109:37–45

    Article  CAS  PubMed  Google Scholar 

  • Fontenot JD, Gavin MA, Rudensky AY (2003) Foxp3 programs the development and function of CD4+ CD25+ regulatory T cells. Nat Immunol 4:330

    Article  CAS  PubMed  Google Scholar 

  • Fournel M, Sapieha P, Beaulieu N, Besterman JM, MacLeod AR (1999) Down-regulation of human DNA-(Cytosine-5) methyltransferase induces cell cycle regulators p16 ink4A and p21WAF/Cip1 by distinct mechanisms. J Biol Chem 274:24250–24256

    Article  CAS  PubMed  Google Scholar 

  • Francis YI, Fà M, Ashraf H, Zhang H, Staniszewski A, Latchman DS, Arancio O (2009) Dysregulation of histone acetylation in the APP/PS1 mouse model of Alzheimer’s disease. J Alzheimers Dis 18:131–139

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fu L, Pelicano H, Liu J, Huang P, Lee CC (2002) The circadian gene Period2 plays an important role in tumor suppression and DNA damage response in vivo. Cell 111:41–50

    Article  CAS  PubMed  Google Scholar 

  • Gaudet F, Hodgson JG, Eden A, Jackson-Grusby L, Dausman J, Gray JW, Leonhardt J, Jaenisch R (2003) Induction of tumors in mice by genomic hypomethylation. Science 300:489–492

    Article  CAS  PubMed  Google Scholar 

  • Greives TJ, Kriegsfeld LJ, Bentley GE, Tsutsui K, Demas GE (2008) Recent advances in reproductive neuroendocrinology: a role for RFamide peptides in seasonal reproduction? Proc Biol Sci 275:1943–1951

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guil S, Esteller M (2009) DNA methylomes, histone codes and miRNAs: tying it all together. Int J Biochem Cell Biol 41:87–95

    Article  CAS  PubMed  Google Scholar 

  • Hanahan D, Weinberg R (2011) Hallmarks of cancer: the next generation. Cell 144:646–674

    Article  CAS  PubMed  Google Scholar 

  • Hastings MH, Brancaccio M, Maywood ES (2014) Circadian pacemaking in cells and circuits of the suprachiasmatic nucleus. J Neuroendocrinol 26:2–10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heard E, Martienssen RA (2014) Transgenerational epigenetic inheritance: myths and mechanisms. Cell 157:95–109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Helm B, Stevenson TJ (2015) Circannual rhythms: history, present challenges, future directions. In: Numata H, Helm B (eds) Annual, lunar and tidal clocks: patterns and mechanisms of nature’s enigmatic rhythms. Springer Japan, Tokyo, pp 213–225

    Google Scholar 

  • Herman JG, Baylin SB (2003) Gene silencing in cancer in association with promoter hypermethylation. N Engl J Med 349:2042–2054

    Article  CAS  PubMed  Google Scholar 

  • Hughes ME, DiTacchio L, Hayes KR, Vollmers C, Pulivarthy S, Baggs JE, Panda S, Hogenesch JB (2009) Harmonics of circadian gene transcription in mammas. PLoS Genet 5:e1000442

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jackson-Grusby L, Beard C, Possemato R, Tudor M, Fambrough D, Csankovszki G, Jaenisch R (2001) Loss of genomic methylation causes p53-dependent apoptosis and epigenetic deregulation. Nat Genet 27:31–39

    Article  CAS  PubMed  Google Scholar 

  • Jang HS, Shin WJ, Lee JE, Tae Do J (2017) CpG and non-CpG methylation in epigenetic gene regulation and brain function. Genes (Basel) 8:148

    Article  CAS  Google Scholar 

  • Jefferson WN, Chevalier DM, Phelps JY, Cantor AM, Padilla-Banks E, Newbold RR, Archer TK, Kinyamu HK, Williams CJ (2013) Persistently altered epigenetic marks in the mouse uterus after neonatal estrogen exposure. Mol Endocrinol 27:1666–1677

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones P, Baylin S (2007) The epigenomics of cancer. Cell 128:683–692

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Josefowicz SZ, Wilson CB, Rudensky AY (2009) Cutting edge: TCR stimulation is sufficient for induction of Foxp3 expression in the absence of DNA methyltransferase 1. J Immunol 182:6648–6652

    Article  CAS  PubMed  Google Scholar 

  • Kaplan MJ, Beretta L, Yung RL, Richardson BC (2000) LFA-1 overexpression and T cell autoreactivity: mechanisms. Immunol Investig 29:427–442

    CAS  Google Scholar 

  • Kautiainen TL, Jones PA (1986) DNA methyltransferase levels in tumorigenic and nontumorigenic cells in culture. J Biol Chem 261:1594–1598

    CAS  PubMed  Google Scholar 

  • Klose RJ, Bird AP (2006) Genomic DNA methylation: the mark and its mediators. Trends Biochem Sci 31:89–97

    Article  CAS  PubMed  Google Scholar 

  • Knox JD, Araujo FD, Bigey P, Slack AD, Price GB, Zannis-Hadjopoulos M, Szyf M (2000) Inhibition of DNA methyltransferase inhibits DNA replication. J Biol Chem 275:17986–17990

    Article  CAS  PubMed  Google Scholar 

  • Kohli RM, Zhang Y (2013) TET enzymes, TDG and the dynamics of DNA demethylation. Nature 502:472–479

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koike N, Yoo SH, Huang HC, Kumar V, Lee C, Kim TK, Takahashi JS (2012) Transcriptional architecture and chromatin landscape of the core circadian clock in mammals. Science 338:349–354

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kurian JR, Terasawa E (2013) Epigenetic control of gonadotropin releasing hormone neurons. Front Endocrinol 4:61

    Article  Google Scholar 

  • Lee PP, Fitzpatrick DR, Beard C, Jessup HK, Lehar S, Makar KW, Cherry SR (2001) A critical role for Dnmt1 and DNA methylation in T cell development, function, and survival. Immunity 15:763–774

    Article  CAS  PubMed  Google Scholar 

  • Lei H, Oh SP, Okano M, Juttermann R, Goss KA, Jaenisch R, Li E (1996) De novo DNA cytosine methyltransferase activities in mouse embryonic stem cells. Development 122:3195–3205

    CAS  PubMed  Google Scholar 

  • Li E (2002) Chromatin modification and epigenetic reprogramming in mammalian development. Nat Rev Genet 3:662–673

    Article  CAS  PubMed  Google Scholar 

  • Li E, Bestor TH, Jaenisch R (1992) Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 69:915–926

    Article  CAS  PubMed  Google Scholar 

  • Logan PC, Ponnampalam AP, Steiner M, Mitchell MD (2013) Effect of cyclic AMP and estrogen/progesterone on the transcription of DNA methyltransferase during the decidualization of human endometrial stromal cells. Mol Hum Reprod 19:302–312

    Article  CAS  PubMed  Google Scholar 

  • Lynch EWJ, Coyle CS, Lorgen M, Campbell E, Bowman A, Stevenson TJ (2016) Cyclical DNA methyltransferase 3a expression is a seasonal and oestrus timer in reproductive tissues. Endocrinology 157:2469–2478

    Article  CAS  PubMed  Google Scholar 

  • Lynch EWJ, Coyle CS, Stevenson TJ (2017) Light and hormonal regulation of histone deacetylase 1, 2, 3 in reproductive tissues. Gen Comp Endocrinol 246:194–199

    Article  CAS  PubMed  Google Scholar 

  • Ma P, Pan H, Montgomery RL, Olson EN, Schultz RM (2012) Compensatory functions of histone deacetylase 1 (HDAC1) and HDAC2 regulate transcription and apoptosis during mouse oocyte development. Proc Natl Acad Sci U S A 109:E481–E489

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miki T, Matsumoto T, Zhao Z, Lee CC (2013) p53 regulates Period2 expression and the circadian clock. Nat Commun 4:2444

    Article  PubMed  CAS  Google Scholar 

  • Nakahata Y, Kaluzova M, Grimaldi B, Sahar S, Hirayama J, Chen D, Guarente LP, Sassone-Corsi P (2008) The NAD+-dependent deacetylase SIRT1 modulates CLOCK-mediated chromatin remodelling and circadian control. Cell 134:329–340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nelson RJ (2004) Seasonal immune function and sickness responses. Trends Immunol 25:187–192

    Article  CAS  PubMed  Google Scholar 

  • Nugent BM, Wright CL, Shetty AC, Hodes GE, Lenz KM, Mahurkar A, Russo SJ, Devine SE, McCarthy MM (2015) Brain feminization requires active repression of masculinization via DNA methylation. Nat Neurosci 18:690–697

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Okano M, Bell DW, Haber DA, Li E (1999) DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99:247–257

    Article  CAS  PubMed  Google Scholar 

  • Olsen EA, Kim YH, Kuzel TM, Pacheco TR, Foss FM, Parker S, Frankel SR, Chen C, Ricker JL, Arduino JM, Duvic M (2007) Phase IIb multicenter trial of vorinostat in patients with persistent, progressive, or treatment refractory cutaneous T-cell lymphoma. J Clin Oncol 25:3109–3115

    Article  CAS  PubMed  Google Scholar 

  • Orozco-Solis R, Ramadori G, Coppari R, Sassone-Corsi P (2015) SIRT1 relays nutritional inputs to the circadian clock through the Sf1 neurons of the ventromedial hypothalamus. Endocrinol 156:2174–2184

    Article  CAS  Google Scholar 

  • Pelengaris S, Khan M, Evan G (2002) c-MYC: more than just a matter of life and death. Nat Rev Cancer 10:764

    Article  CAS  Google Scholar 

  • Pfaff DW, Phillips MI, Rubin RT (2004) Hormonal secretions and responses are affected by biological clocks. In: Principles of hormone/behavior relations. Elsevier Academic Press, San Diego, pp 181–196

    Chapter  Google Scholar 

  • Pizarro A, Hayer K, Lahens NF, Hogenesch JB (2013) CircaDB: a database of mammalian circadian gene expression profiles. Nucleic Acids Res 41:D1009–D1013

    Article  CAS  PubMed  Google Scholar 

  • Prendergast BJ, Cable EJ, Patel PN, Pyter LM, Onishi KG, Stevenson TJ, Ruby NF, Bradley SP (2013) Impaired leukocyte trafficking and skin inflammatory responses in hamsters lacking a functional circadian system. Brain Behav Immun 32:94–104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Quddus J, Johnson KJ, Gavalchin J, Amento EP, Chrisp CE, Yung RL, Richardson BC (1993) Treating activated CD4+ T cells with either of two distinct DNA methyltransferase inhibitors, 5-azacytidine or procainamide, is sufficient to cause a lupus-like disease in syngeneic mice. J Clin Invest 92:38–53

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rasool M, Malik A, Naseer MI, Manan A, Ansari SA, Begum I, Qazi MH, Pushparaji PN, Abuzenadah AM, Al-Qahtani MH, Kamal MA, Pushparaji PN, Gan SH (2015) The role of epigenetics in personalized medicine: challenges and opportunities. BMC Med Genet 8:S5

    Google Scholar 

  • Rhee I, Jair KW, Yen RWC, Lengauer C, Herman JG, Kinzler KW, Vogelstein B, Baylin SB, Schuebel KE (2000) CpG methylation is maintained in human cancer cells lacking DNMT1. Nature 404:1003–1007

    Article  CAS  PubMed  Google Scholar 

  • Ricceri F, Trevisan M, Fiano V, Grasso C, Fasanelli F, Scoccianti C, De Marco L, Tox AG, Vineis P, Sacerdote C (2014) Seasonality modifies methylation profiles in healthy people. PLoS One 9:e106846

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Richardson B, Scheinbart L, Strahler J, Gross L, Hanash S, Johnson M (1990) Evidence for impaired T cell DNA methylation in systemic lupus erythematosus and rheumatoid arthritis. Arthritis Rheum 33:1665–1673

    Article  CAS  PubMed  Google Scholar 

  • Richter A, Löhning M, Radbruch A (1999) Instruction for cytokine expression in T helper lymphocytes in relation to proliferation and cell cycle progression. J Exp Med 190:1439–1450

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Riggs AD, Porter TN (1996) Overview of epigenetic mechanisms. In: Russo VEA, Martienssen R, Riggs AD (eds) Epigenetic mechanisms of gene regulation. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp 29–45

    Google Scholar 

  • Roy A, Matzuk MM (2006) Deconstructing mammalian reproduction: using knockouts to define fertility pathways. Reproduction 131:207–219

    Article  CAS  PubMed  Google Scholar 

  • Savvidis C, Koutsilieris M (2013) Circadian rhythm disruption in cancer biology. Mol Med 18:1249–1260

    Article  CAS  Google Scholar 

  • Stevenson TJ (2017a) Environmental and hormonal regulation of neuroendocrine epigenetic enzymes. J Neuroendocrinol 29(5)

    Google Scholar 

  • Stevenson TJ (2017b) Circannual and circadian rhythms in hypothalamic DNA methyltransferase and histone deacetylase in Siberian hamsters (Phodopus sungorus). Gen Comp Endocrinol 243:130–137

    Article  CAS  PubMed  Google Scholar 

  • Stevenson TJ (2018) Epigenetic regulation of biological rhythms: an evolutionary ancient molecular timer. Trends Genet 43:90–100

    Article  CAS  Google Scholar 

  • Stevenson TJ, Lincoln GA (2017) Epigenetic mechanisms regulating circannual rhythms, Chap 29. In: Kumar V (ed) Biological timekeeping: clocks, rhythms and behaviour. Springer, India

    Google Scholar 

  • Stevenson TJ, Prendergast BJ (2013) Reversible DNA methylation regulates seasonal photoperiodic time measurement. Proc Natl Acad Sci USA 110:16651–16656

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stevenson TJ, Prendergast BJ (2015) Photoperiodic time measurement and seasonal immunological plasticity. Front Neuroendocrinol 37:76–88

    Article  PubMed  Google Scholar 

  • Stevenson TJ, Hahn TP, MacDougall-Shackleton SA, Ball GF (2012) Gonadotropin-releasing hormone plasticity: a comparative perspective. Front Neuroendocrinol 33:287–300

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stevenson TJ, Bernard DJ, McCarthy MM, Ball GF (2013) Photoperiod-dependent regulation of gonadotropin-releasing hormone 1 messenger ribonucleic acid levels in the songbird brain. Gen Comp Endocrinol 190:81–87

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stevenson TJ, Onishi KG, Bradley SP, Prendergast BJ (2014) Cell-autonomous iodothyronine deiodinase expression mediates seasonal plasticity in immune function. Brain Behav Immun 36:61–70

    Article  CAS  PubMed  Google Scholar 

  • Stevenson TJ, Visser ME, Arnold W, Barrett P, Biello S, Dawson A, Denlinger DL, Dominoni D, Ebling FJ, Elton S, Evans N, Ferguson HM, Foster RG, Hau M, Haydon DT, Hazlerigg DG, Heideman P, Hopcraft JGC, Jonsson NN, Kronfeld-Schor N, Kumar V, Lincoln GA, MacLeod R, Martin SAM, Martinez-Bakker M, Nelson RJ, Reed T, Robinson JE, Rock D, Schwartz WJ, Steffan-Dewenter I, Tauber E, Thackeray SJ, Umstatter C, Yoshimura T, Helm B (2015) Disrupted seasonal biology impacts health food security and ecosystems. Proc R Soc B 282:1–10

    Article  CAS  Google Scholar 

  • Symonds H, Krall L, Remington L, Saenz-Robles M, Lowe S, Jacks T, Van Dyke T (1994) p53-dependent apoptosis suppresses tumor growth and progression in vivo. Cell 78:703–711

    Article  CAS  PubMed  Google Scholar 

  • Taunton J, Hassig CA, Schreiber SL (1996) A mammalian histone deacetylase related to the yeast transcriptional regulator Rpd3p. Science 272:408–411

    Article  CAS  PubMed  Google Scholar 

  • Van Kaam KJ, Delvoux B, Romano A, D’Hooghe T, Dunselman GA, Groothuis PG (2011) Deoxyribonucleic acid methyltransferase and methyl-CpG binding domain proteins in human endometrium and endometriosis. Fertil Steril 95:1421–1427

    Article  PubMed  CAS  Google Scholar 

  • Waddington CH (1953) Epigenetics and evolution. Symp Soc Exp Biol 7:186–199

    Google Scholar 

  • Weaver ICG, Cervoni N, Champagne FA, D’Alessio AC, Sharma S, Seckl JR, Dymov S, Szyf M, Meaney MJ (2004) Epigenetic programming by maternal behavior. Nat Neurosci 7:847–854

    Article  CAS  PubMed  Google Scholar 

  • Westwood FR (2008) The female rat reproductive cycle: a practical histological guide to staging. Toxicol Pathol 36:375–384

    Article  PubMed  Google Scholar 

  • Widschwendter M, Jones A, Evans I, Reisel D, Dillner J, Sundstrom K, Steyerberg EW, Vergouwe Y, Wegwarth O, Rebitschek FG, Siebert U, Sroczynski G, de Beaufort ID, Bolt I, Cibula D, Zikan M, Bjorge L, Colombo N, Harbeck N, Dudbridge F, Am T, Knoppers BM, Joly Y, Teschendorff AE, Pashayan N, FORECEE 4C Consortium (2018) Epigenome-based cancer risk prediction: rationale, opportunities and challenges. Nat Rev Clin Oncol 15:292–309

    Article  PubMed  Google Scholar 

  • Wood GA, Fata JE, Watson KLM, Khokha R (2007) Circulating hormones and estrous stage predict cellular and stromal remodelling in murine uterus. Reproduction 133:1035–1044

    Article  CAS  PubMed  Google Scholar 

  • Xu HJ, Cairns P, Hu SX, Knowles MA, Benedict WF (1993) Loss of RB protein expression in primary bladder cancer correlates with loss of heterozygosity at the RB locus and tumor progression. Int J Cancer 53:781–784

    Article  CAS  PubMed  Google Scholar 

  • Yeo GS, Heisler LK (2012) Unraveling the brain regulation of appetite: lessons from genetics. Nat Neurosci 15:1343–1349

    Article  CAS  PubMed  Google Scholar 

  • Yoder JA, Soman NS, Verdine GL, Bestor TH (1997) DNA (cytosine-T)-methyltransferase in mouse cells and tissues. Studies with a mechanism-based probe. J Mol Biol 270:385–395

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Biodiversity, Animal Health and Comparative Medicine, University of Glasgow, Glasgow, UK

    Christopher S. Coyle, Elisabetta Tolla & Tyler J. Stevenson

Authors
  1. Christopher S. Coyle
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Elisabetta Tolla
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tyler J. Stevenson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tyler J. Stevenson .

Editor information

Editors and Affiliations

  1. Cellular and Developmental Neurobiology, NINDS, NIH, Bethesda, USA

    Susan Wray

  2. Department of Neuroscience, School of Medicine, Johns Hopkins University, Baltimore, MD, USA

    Seth Blackshaw

Key References

Key References

  • Azzi et al. (2014). This study shows that daily oscillations in SCN DNA methylation regulates circadian clock function.

  • Bilbo et al. (2002). This is an exciting report on the seasonal regulation of immune function.

  • Dopico et al. (2015). This study reveals large annual changes in leukocyte transcriptomes in humans.

  • Koike et al. (2012). One key finding identified in this paper were daily rhythms in BMAL1 binding on the dnmt3a promoter.

  • Lynch et al. (2016). This report illustrated increased dnmt3a expression was negatively associated with oscillations in fertility.

  • Nugent et al. (2015). This study discovered sex-differences in neuroendocrine DNMT3a and a lack of expression facilitated masculinization.

  • Stevenson and Prendergast. (2013). This study established that rhythmic neuroendocrine DNA methylation underlies seasonal timing of reproduction.

Rights and permissions

Reprints and permissions

Copyright information

© 2020 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Coyle, C.S., Tolla, E., Stevenson, T.J. (2020). Rhythmic Epigenetics in Neuroendocrine and Immune Systems. In: Wray, S., Blackshaw, S. (eds) Developmental Neuroendocrinology. Masterclass in Neuroendocrinology, vol 9. Springer, Cham. https://doi.org/10.1007/978-3-030-40002-6_11

Download citation

Publish with us

Policies and ethics

Search

Navigation