High cortisol in 5-year-old children causes loss of DNA methylation in SINE retrotransposons: a possible role for ZNF263 in stress-related diseases

Clinical Epigenetics

Volumn 7, Issue 1, 2015, Pages

  Nätt, Daniel ^a   Johansson, Ingela ^a   Faresjö, Tomas ^a   Ludvigsson, Johnny ^a   Thorsell, Annika ^a  

^a LINKÖPING UNIVERSITY   (Sweden)

Author keywords

Blood; Children; Cortisol; DNA methylation; EGR1; Hair; Retrotransposon; Stress; Transcription factor; ZNF263

Indexed keywords

HYDROCORTISONE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ZNF263; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN;

ADULT DISEASE; AGING; ARTICLE; BINDING SITE; CALCIUM TRANSPORT; CHILD; CHILDHOOD STRESS; CONTROLLED STUDY; DISEASE PREDISPOSITION; DNA METHYLATION; EPIGENETICS; FEMALE; HAIR LEVEL; HUMAN; MALE; PRESCHOOL CHILD; PRIORITY JOURNAL; RETROPOSON; SHORT INTERSPERSED REPEAT; STRESS;

EID: 84940835582     PISSN: 18687075     EISSN: 18687083     Source Type: Journal    
DOI: 10.1186/s13148-015-0123-z     Document Type: Article

References (68)

1. Wegman HL, Stetler C. A meta-analytic review of the effects of childhood abuse on medical outcomes in adulthood. Psychosom Med. 2009;71(8):805–12. doi:10.1097/PSY.0b013e3181bb2b46.
2. Rich-Edwards JW, Spiegelman D, Lividoti Hibert EN, Jun H-J, Todd TJ, Kawachi I, et al. Abuse in childhood and adolescence as a predictor of type 2 diabetes in adult women. Am J Prev Med. 2010;39(6):529–36. doi:http://dx.doi.org/10.1016/j.amepre.2010.09.007.
3. Dong M, Giles WH, Felitti VJ, Dube SR, Williams JE, Chapman DP, et al. Insights into causal pathways for ischemic heart disease: adverse childhood experiences study. Circulation. 2004;110(13):1761–6. doi:10.1161/01.cir.0000143074.54995.7f.
4. Shalev I, Entringer S, Wadhwa PD, Wolkowitz OM, Puterman E, Lin J, et al. Stress and telomere biology: a lifespan perspective. Psychoneuroendocrinology. 2013;38(9):1835–42. doi:http://dx.doi.org/10.1016/j.psyneuen.2013.03.010.
5. Anda R, Dong M, Brown D, Felitti V, Giles W, Perry G, et al. The relationship of adverse childhood experiences to a history of premature death of family members. BMC Public Health. 2009;9(1):106.
6. Heim C, Bradley B, Mletzko T, Deveau TC, Musselmann DL, Nemeroff CB et al. Effect of childhood trauma on adult depression and neuroendocrine function: sex-specific moderation by CRH receptor 1 gene. Front Behav Neurosci. 2009;3. doi:10.3389/neuro.08.041.2009.
7. Spijker AT, van Rossum EFC. Glucocorticoid sensitivity in mood disorders. Neuroendocrinology. 2012;95(3):179–86.
8. Walker BR. Glucocorticoids and cardiovascular disease. European J Endocrinol. 2007;157(5):545–59. doi:10.1530/eje-07-0455.
9. Pervanidou P, Chrousos GP. Metabolic consequences of stress during childhood and adolescence. Metabolism. 2012;61(5):611–9.
10. Wosu AC, Valdimarsdóttir U, Shields AE, Williams DR, Williams MA. Correlates of cortisol in human hair: implications for epidemiologic studies on health effects of chronic stress. Ann Epidemiol. 2013;23(12):797–811.e2. doi:http://dx.doi.org/10.1016/j.annepidem.2013.09.006.
11. Karlen J, Ludvigsson J, Frostell A, Theodorsson E, Faresjo T. Cortisol in hair measured in young adults—a biomarker of major life stressors? BMC Clin Pathol. 2011;11(1):12.
12. Karlén J, Frostell A, Theodorsson E, Faresjö T, Ludvigsson J. Maternal influence on child hpa axis: a prospective study of cortisol levels in hair. Pediatrics. 2013;132(5):e1333–e40. doi:10.1542/peds.2013-1178.
13. LaPlant Q, Vialou V, Covington III HE, Dumitriu D, Feng J, Warren BL, et al. Dnmt3a regulates emotional behavior and spine plasticity in the nucleus accumbens. Nature Neurosci. 2010;13(9):1137–43.
14. Sailaja BS, Cohen-Carmon D, Zimmerman G, Soreq H, Meshorer E. Stress-induced epigenetic transcriptional memory of acetylcholinesterase by HDAC4. Proc Natl Acad Sci. 2012;109(52):E3687–E95. doi:10.1073/pnas.1209990110.
15. Pena CJ, Bagot RC, Labonte B, Nestler EJ. Epigenetic signaling in psychiatric disorders. J Mol Biol. 2014;426(20):3389–412. doi:10.1016/j.jmb.2014.03.016.
16. Lam LL, Emberly E, Fraser HB, Neumann SM, Chen E, Miller GE, et al. Factors underlying variable DNA methylation in a human community cohort. Proceedings of the National. Academy of Sciences. 2012;109(Supplement 2):17253–60. doi:10.1073/pnas.1121249109.
17. Labonté B, Suderman M, Maussion G, et al. GEnome-wide epigenetic regulation by early-life trauma. Arch Gen Psychiatry. 2012;69(7):722–31. doi:10.1001/archgenpsychiatry.2011.2287.
18. McGowan PO, Sasaki A, D'Alessio AC, Dymov S, Labonte B, Szyf M, et al. Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nat Neurosci. 2009;12(3):342–8.
19. Goerlich VC, Nätt D, Elfwing M, Macdonald B, Jensen P. Transgenerational effects of early experience on behavioral, hormonal and gene expression responses to acute stress in the precocial chicken. Horm Behav. 2012;61(5):711–8. doi:10.1016/j.yhbeh.2012.03.006.
20. Knapska E, Kaczmarek L. A gene for neuronal plasticity in the mammalian brain: Zif268/Egr-1/NGFI-A/Krox-24/TIS8/ZENK? Prog Neurobiol. 2004;74(4):183–211.
21. Okashita N, Kumaki Y, Ebi K, Nishi M, Okamoto Y, Nakayama M, et al. PRDM14 promotes active DNA demethylation through the ten-eleven translocation (TET)-mediated base excision repair pathway in embryonic stem cells. Development. 2014;141(2):269–80. doi:10.1242/dev.099622.
22. Brennan K, Flanagan JM. Is there a link between genome-wide hypomethylation in blood and cancer risk? Cancer Prev Res. 2012;5(12):1345–57. doi:10.1158/1940-6207.capr-12-0316.
23. Portela A, Esteller M. Epigenetic modifications and human disease. Nat Biotech. 2010;28(10):1057–68. doi:10.1038/nbt.1685.
24. Ponomarev I. Epigenetic control of gene expression in the alcoholic brain. Alcohol research: current reviews. 2013;35(1):69.
25. Tremolizzo L, Conti E, Bomba M, Uccellini O, Rossi MS, Marfone M et al. Decreased whole-blood global DNA methylation is related to serum hormones in anorexia nervosa adolescents. World J Biol Psychiatry. 2014 15(4):327-33. doi:10.3109/15622975.2013.860467.
26. Kim GH, Ryan JJ, Archer SL. The role of redox signaling in epigenetics and cardiovascular disease. Antioxid Redox Signal. 2013;18(15):1920–36.
27. Johnson AA, Akman K, Calimport SR, Wuttke D, Stolzing A, de Magalhaes JP. The role of DNA methylation in aging, rejuvenation, and age-related disease. Rejuvenation Res. 2012;15(5):483–94.
28. Jaffe A, Irizarry R. Accounting for cellular heterogeneity is critical in epigenome-wide association studies. Genome Biol. 2014;15(2):R31.
29. Reinius LE, Acevedo N, Joerink M, Pershagen G, Dahlén S-E, Greco D, et al. Differential dna methylation in purified human blood cells: implications for cell lineage and studies on disease susceptibility. PLoS One. 2012;7(7), e41361. doi:10.1371/journal.pone.0041361.
30. Zilbauer M, Rayner TF, Clark C, Coffey AJ, Joyce CJ, Palta P et al. Genome-wide methylation analyses of primary human leukocyte subsets identifies functionally important cell-type–specific hypomethylated regions. Blood. 2013 122(25):e52-60. doi:10.1182/blood-2013-05-503201.
31. Koch CM, Reck K, Shao K, Lin Q, Joussen S, Ziegler P, et al. Pluripotent stem cells escape from senescence-associated DNA methylation changes. Genome Res. 2013;23(2):248–59.
32. Horvath S. DNA methylation age of human tissues and cell types. Genome Biol. 2013;14(10):R115.
33. Hannum G, Guinney J, Zhao L, Zhang L, Hughes G, Sadda S, et al. Genome-wide methylation profiles reveal quantitative views of human aging rates. Mol Cell. 2013;49(2):359–67.
34. Hanzelmann S, Beier F, Gusmao E, Koch C, Hummel S, Charapitsa I, et al. Replicative senescence is associated with nuclear reorganization and with DNA methylation at specific transcription factor binding sites. Clin Epigenetics. 2015;7(1):19.
35. Ferrari P. Cortisol and the renal handling of electrolytes: role in glucocorticoid-induced hypertension and bone disease. Best Pract Res Clin Endocrinol Metab. 2003;17(4):575–89. doi:http://dx.doi.org/10.1016/S1521-690X(03)00053-8.
36. Buehring B, Viswanathan R, Binkley N, Busse W. Glucocorticoid-induced osteoporosis: an update on effects and management. J Allergy Clin Immunol. 2013;132(5):1019–30. doi:http://dx.doi.org/10.1016/j.jaci.2013.08.040.
37. Tóth M, Grossman A. Glucocorticoid-induced osteoporosis: lessons from Cushing’s syndrome. Clin Endocrinol. 2013;79(1):1–11. doi:10.1111/cen.12189.
38. Camandola S, Mattson MP. Aberrant subcellular neuronal calcium regulation in aging and Alzheimer’s disease. BBA-Mol Cell Res. 2011;1813(5):965–73. doi:http://dx.doi.org/10.1016/j.bbamcr.2010.10.005.
39. Hurt, C., Montaigne, D., Ennezat, P. V., Hatem, S., & Vallet, B. (2014). Cardiovascular Disease: Calcium Channel Anomalies. In Uncommon Diseases in the ICU (pp. 29-35). Springer International Publishing.
40. Rorsman P, Braun M, Zhang Q. Regulation of calcium in pancreatic α-and β-cells in health and disease. Cell Calcium. 2012;51(3):300–8.
41. Bailey TL, Elkan C. Fitting a mixture model by expectation maximization to discover motifs in bipolymers. University of California, San Diego: Department of Computer Science and Engineering; 1994.
42. Gupta S, Stamatoyannopoulos JA, Bailey TL, Noble WS. Quantifying similarity between motifs. Genome Biol. 2007;8(2):R24.
43. Stolzenberg DS, Grant PA, Bekiranov S. Epigenetic methodologies for behavioral scientists. Horm Behav. 2011;59(3):407–16.
44. Frietze S, Lan X, Jin VX, Farnham PJ. Genomic targets of the KRAB and SCAN domain-containing zinc finger protein 263. J Biol Chem. 2010;285(2):1393–403.
45. Jacobs FMJ, Greenberg D, Nguyen N, Haeussler M, Ewing AD, Katzman S, et al. An evolutionary arms race between KRAB zinc-finger genes ZNF91/93 and SVA/L1 retrotransposons. Nature. 2014;516(7530):242–5. doi:10.1038/nature13760.
46. Versteeg R, van Schaik BDC, Roos M, Monajemi R, Caron H, et al. The human transcriptome map reveals extremes in gene density, intron length, gc content, and repeat pattern for domains of highly and weakly expressed genes. Genome Res. 2003;13(9):1998–2004. doi:10.1101/gr.1649303.
47. Brenet F, Moh M, Funk P, Feierstein E, Viale AJ, Socci ND, et al. DNA methylation of the first exon is tightly linked to transcriptional silencing. PLoS One. 2011;6(1):e14524.
48. Romens SE, McDonald J, Svaren J, Pollak SD. Associations between early life stress and gene methylation in children. Child Dev. 2015 86(1):303-9. doi:10.1111/cdev.12270. Epub 2014 Jul 24.
49. Loi M, Koricka S, Lucassen P, Joels M. Age- and sex-dependent effects of early life stress on hippocampal neurogenesis. Front Endocrinol. 2014;5 doi:10.3389/fendo.2014.00013.
50. Lagdon S, Armour C, Stringer M. Adult experience of mental health outcomes as a result of intimate partner violence victimisation: a systematic review. European Journal of Psychotraumatology. 2014;5:10.3402/ejpt.v5.24794. doi:10.3402/ejpt.v5.24794.
51. Bale TL. Epigenetic and transgenerational reprogramming of brain development. Nat Rev Neurosci. 2015;16(6):332–44. doi:10.1038/nrn3818.
52. Karlén J, Ludvigsson J, Hedmark M, Faresjö Å, Theodorsson E, Faresjö T. Early psychosocial exposures, hair cortisol levels, and disease risk. Pediatrics. 2015:peds. 2014–561.
53. Morelius E, Nelson N, Theodorsson E. Salivary cortisol and administration of concentrated oral glucose in newborn infants: improved detection limit and smaller sample volumes without glucose interference. Scand J Clin Lab Invest. 2004;64(2):113–8.
54. Taiwo O, Wilson GA, Morris T, Seisenberger S, Reik W, Pearce D, et al. Methylome analysis using MeDIP-seq with low DNA concentrations. Nat Protocols. 2012;7(4):617–36.
55. Li H, Durbin R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics. 2009;25(14):1754–60. doi:10.1093/bioinformatics/btp324.
56. Lienhard M, Grimm C, Morkel M, Herwig R, Chavez L. MEDIPS: genome-wide differential coverage analysis of sequencing data derived from DNA enrichment experiments. Bioinformatics. 2014;30(2):284–6.
57. Lawrence M, Huber W, Pag\`es H, Aboyoun P, Carlson M, et al. (2013) Software for Computing and Annotating Genomic Ranges. PLoS Comput Biol 9(8):e1003118. doi:10.1371/journal.pcbi.1003118.
58. Risso D, Schwartz K, Sherlock G, Dudoit S. GC-content normalization for RNA-Seq data. BMC Bioinformatics. 2011;12(1):480.
59. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010;26(1):139–40.
60. Bao Y, Vinciotti V, Wit E, 't Hoen P. Accounting for immunoprecipitation efficiencies in the statistical analysis of ChIP-seq data. BMC Bioinformatics. 2013;14(1):169.
61. Wang J, Duncan D, Shi Z, Zhang B. WEB-based GEne SeT AnaLysis Toolkit (WebGestalt): update 2013. Nucleic Acids Res. 2013;41(Web Server issue):W77–83. gkt439.
62. Becker KG, Barnes KC, Bright TJ, Wang SA. The Genetic Association Database. Nat Genet. 2004;36(5):431–2.
63. Warnes GR, Bolker B, Bonebakker L, Gentleman R, Huber W, Liaw A et al. gplots: Various R programming tools for plotting data. 2014. http://cran.r-project.org/web/packages/gplots/index.html.
64. Shimodaira H. Approximately unbiased tests of regions using multistep-multiscale bootstrap resampling. The Annals of Statistics. 2004;32(6):2616–41.
65. Favorov A, Mularoni L, Cope LM, Medvedeva Y, Mironov AA, Makeev VJ, et al. Exploring massive, genome scale datasets with the genometricorr package. PLoS Comput Biol. 2012;8(5), e1002529. doi:10.1371/journal.pcbi.1002529.
66. Grant CE, Bailey TL, Noble WS. FIMO: scanning for occurrences of a given motif. Bioinformatics. 2011;27(7):1017–8.
67. Consortium EP. An integrated encyclopedia of DNA elements in the human genome. Nature. 2012;489(7414):57–74.
68. DePristo MA, Banks E, Poplin R, Garimella KV, Maguire JR, Hartl C, et al. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet. 2011;43(5):491–8.