Evidence for Epigenetic Regulation of Pro-Inflammatory Cytokines, Interleukin-12 and Interferon Gamma, in Peripheral Blood Mononuclear Cells from PTSD Patients

Journal of Neuroimmune Pharmacology

Volumn 11, Issue 1, 2016, Pages 168-181

  Bam, Marpe ^a   Yang, Xiaoming ^a   Zhou, Juhua ^a,c   Ginsberg, Jay P ^b   Leyden, Quinne ^b   Nagarkatti, Prakash S ^a   Nagarkatti, Mitzi ^a,b  

^a UNIVERSITY OF SOUTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b Dorn Research Institute   (United States)

^c LUDONG UNIVERSITY   (China)

Author keywords

DNA methylation; Histone modification; IL 12; Inflammation; miRNA; Post traumatic stress disorder

Indexed keywords

AZACITIDINE; COMPLEMENTARY DNA; CYTOKINE; DNA (CYTOSINE 5) METHYLTRANSFERASE; DOUBLE STRANDED DNA; GAMMA INTERFERON; GENOMIC DNA; HISTONE H3; INTERLEUKIN 12; LYSINE SPECIFIC DEMETHYLASE 5B; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; ACETYLCYSTEINE;

ARTICLE; BLOOD ANALYSIS; CONTROLLED STUDY; CORRELATION ANALYSIS; DNA METHYLATION; ENZYME ACTIVITY; EPIGENETICS; GENE INTERACTION; GENETIC ASSOCIATION; GENETIC TRANSFECTION; HISTONE METHYLATION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; INFORMATION PROCESSING; MICROARRAY ANALYSIS; PERIPHERAL BLOOD MONONUCLEAR CELL; POSTTRAUMATIC STRESS DISORDER; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; ADULT; BIOSYNTHESIS; CHROMATIN IMMUNOPRECIPITATION; FEMALE; GENE EXPRESSION REGULATION; GENE SILENCING; GENETIC EPIGENESIS; GENETICS; IMMUNOLOGY; MALE; METABOLISM; MONONUCLEAR CELL; PROMOTER REGION;

ACETYLCYSTEINE; ADULT; CHROMATIN IMMUNOPRECIPITATION; CYTOKINES; DNA METHYLATION; EPIGENESIS, GENETIC; FEMALE; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; HUMANS; INTERFERON-GAMMA; INTERLEUKIN-12; LEUKOCYTES, MONONUCLEAR; MALE; PROMOTER REGIONS, GENETIC; REAL-TIME POLYMERASE CHAIN REACTION; STRESS DISORDERS, POST-TRAUMATIC; TRANSFECTION;

EID: 84957431527     PISSN: 15571890     EISSN: 15571904     Source Type: Journal    
DOI: 10.1007/s11481-015-9643-8     Document Type: Article

References (44)

1. Ambros V (2004) The functions of animal microRNAs. Nature 431(7006):350–355. doi:10.1038/nature02871
2. Bannister AJ, Schneider R, Myers FA, Thorne AW, Crane-Robinson C, Kouzarides T (2005) Spatial distribution of di- and tri-methyl lysine 36 of histone H3 at active genes. J Biol Chem 280:17732–17736. doi:10.1074/jbc.M500796200
3. Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116(2):281–297. doi:10.1016/S0092-8674(04)00045-5
4. Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J, Fry B, Meissner A, Wernig M, Plath K, Jaenisch R, Wagschal A, Feil R, Schreiber SL, Lander ES (2006) A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125:315–326. doi:10.1016/j.cell.2006.02.041
5. Blankenberg D, Von Kuster G, Coraor N, Ananda G, Lazarus R, Mangan M, Nekrutenko A, Taylor J (2010) Galaxy: a web-based genome analysis tool for experimentalists. Curr Protoc Mol Biol Chapter 19: Unit 19 10 11–21
6. Christman JK (2002) 5-Azacytidine and 5-aza-2′-deoxycytidine as inhibitors of DNA methylation: mechanistic studies and their implications for cancer therapy. Oncogene 21(35):5483–5495. doi:10.1038/sj.onc.1205699
7. Collier SP, Henderson MA, Tossberg JT, Aune TM (2014) Regulation of the Th1 genomic locus from Ifng through Tmevpg1 by T-bet. J Immunol 193(8):3959–3965. doi:10.4049/jimmunol.1401099
8. Djuretic IM, Levanon D, Negreanu V, Groner Y, Rao A, Ansel KM (2007) Transcription factors T-bet and Runx3 cooperate to activate Ifng and silence Il4 in T helper type 1 cells. Nat Immunol 8(2):145–153. doi:10.1038/ni1424
9. Flintoft L (2013) Non-coding RNA: structure and function for lncRNAs. Nat Rev Genet 14:598. doi:10.1038/nrg3561
10. Frayne SM, Chiu VY, Iqbal S, Berg EA, Laungani KJ, Cronkite RC, Pavao J, Kimerling R (2011) Medical care needs of returning veterans with PTSD: their other burden. J Gen Intern Med 26(1):33–39. doi:10.1007/s11606-010-1497-4
11. Gill JM, Saligan L, Woods S, Page G (2009) PTSD is associated with an excess of inflammatory immune activities. Perspect Psychiatr Care 45:262–277. doi:10.1111/j.1744-6163.2009.00229.x
12. Greer EL, Shi Y (2012) Histone methylation: a dynamic mark in health, disease and inheritance. Nat Rev Genet 13:343–357. doi:10.1038/nrg3173
13. He L, Hannon GJ (2004) MicroRNAs: small RNAs with a big role in gene regulation. Nat Rev Genet 5:522–531. doi:10.1038/nrg1379
14. Hoge EA, Brandstetter K, Moshier S, Pollack MH, Wong KK, Simon NM (2009) Broad spectrum of cytokine abnormalities in panic disorder and posttraumatic stress disorder. Depress Anxiet 26:447–455. doi:10.1002/da.20564
15. Hunter RG, McCarthy KJ, Milne TA, Pfaff DW, McEwen BS (2009) Regulation of hippocampal H3 histone methylation by acute and chronic stress. Proc Natl Acad Sci U S A 106:20912–20917. doi:10.1073/pnas.0911143106
16. Kessler RC, Chiu WT, Demler O, Merikangas KR, Walters EE (2005) Prevalence, severity, and comorbidity of 12-month DSM-IV disorders in the National Comorbidity Survey Replication. Arch Gen Psychiatry 62:617–627. doi:10.1001/archpsyc.62.6.617
17. Klein BJ, Piao L, Xi Y, Rincon-Arano H, Rothbart SB, Peng D, Wen H, Larson C, Zhang X, Zheng X, Cortazar MA, Peña PV, Mangan A, Bentley DL, Strahl BD, Groudine M, Li W, Shi X, Kutateladze TG (2014) The histone-H3K4-specific demethylase KDM5B binds to its substrate and product through distinct PHD fingers. Cell Rep 6(2):325–335. doi:10.1016/j.celrep.2013.12.021
18. Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10(3):R25. doi:10.1186/gb-2009-10-3-r25
19. Lehnertz B, Ueda Y, Derijck AA, Braunschweig U, Perez-Burgos L, Kubicek S, Chen T, Li E, Jenuwein T, Peters AH (2003) Suv39h-mediated histone H3 lysine 9 methylation directs DNA methylation to major satellite repeats at pericentric heterochromatin. Curr Biol 13:1192–1200. doi:10.1016/S0960-9822(03)00432-9
20. Li LC, Dahiya R (2002) MethPrimer: designing primers for methylation PCRs. Bioinformatics 18(11):1427–1431. doi:10.1093/bioinformatics/18.11.1427
21. Lienhard M, Grimm C, Morkel M, Herwig R, Chavez L (2014) MEDIPS: genome-wide differential coverage analysis of sequencing data derived from DNA enrichment experiments. Bioinformatics 30:284–286. doi:10.1093/bioinformatics/btt650
22. Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, Giannoukos G, Alvarez P, Brockman W, Kim TK, Koche RP, Lee W, Mendenhall E, O’Donovan A, Presser A, Russ C, Xie X, Meissner A, Wernig M, Jaenisch R, Nusbaum C, Lander ES, Bernstein BE (2007) Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448:553–560. doi:10.1038/nature06008
23. Muers M (2013) Gene expression: disentangling DNA methylation. Nat Rev Genet 14:519. doi:10.1038/nrg3535
24. Puddu P, Fantuzzi L, Borghi P, Varano B, Rainaldi G, Guillemard E, Malorni W, Nicaise P, Wolf SF, Belardelli F, Gessani S (1997) IL-12 induces IFN-gamma expression and secretion in mouse peritoneal macrophages. J Immunol 159:3490–3497
25. Roh TY, Cuddapah S, Cui K, Zhao K (2006) The genomic landscape of histone modifications in human T cells. Proc Natl Acad Sci U S A 103:15782–15787. doi:10.1073/pnas.0607617103
26. Roh TY, Wei G, Farrell CM, Zhao K (2007) Genome-wide prediction of conserved and nonconserved enhancers by histone acetylation patterns. Genome Res 17:74–81. doi:10.1101/gr.5767907
27. Rohleder N, Karl A (2006) Role of endocrine and inflammatory alterations in comorbid somatic diseases of post-traumatic stress disorder. Minerva Endocrinol 31:273–288
28. Ross-Innes CS, Stark R, Teschendorff AE, Holmes KA, Ali HR, Dunning MJ, Brown GD, Gojis O, Ellis IO, Green AR, Ali S, Chin SF, Palmieri C, Caldas C, Carroll JS (2012) Differential oestrogen receptor binding is associated with clinical outcome in breast cancer. Nature 481:389–393. doi:10.1038/nature10730
29. Rothbart SB, Strahl BD (2014) Interpreting the language of histone and DNA modifications. Biochim Biophys Acta 1839(8):627–643. doi:10.1016/j.bbagrm.2014.03.001
30. Rusiecki JA, Byrne C, Galdzicki Z, Srikantan V, Chen L, Poulin M, Yan L, Baccarelli A (2013) PTSD and DNA methylation in select immune function gene promoter regions: a repeated measures case–control study of U.S. Military Service Members. Front Psychiatr 4:56. doi:10.3389/fpsyt.2013.00056
31. Schroder K, Hertzog PJ, Ravasi T, Hume DA (2004) Interferon-gamma: an overview of signals, mechanisms and functions. J Leukoc Biol 75(2):163–189. doi:10.1189/jlb.0603252
32. Shin H, Liu T, Manrai AK, Liu XS (2009) CEAS: cis-regulatory element annotation system. Bioinformatics 25:2605–2606. doi:10.1093/bioinformatics/btp479
33. Smith AK, Conneely KN, Kilaru V, Mercer KB, Weiss TE, Bradley B, Tang Y, Gillespie CF, Cubells JF, Ressler KJ (2011) Differential immune system DNA methylation and cytokine regulation in post-traumatic stress disorder. Am J Med Genet B Neuropsychiatr Genet 156B:700–708. doi:10.1002/ajmg.b.31212
34. Sun H, Kennedy PJ, Nestler EJ (2013) Epigenetics of the depressed brain: role of histone acetylation and methylation. Neuropsychopharmacology 38:124–137. doi:10.1038/npp.2012.73
35. Sutherland AG, Alexander DA, Hutchison JD (2003) Disturbance of pro-inflammatory cytokines in post-traumatic psychopathology. Cytokine 24:219–225. doi:10.1016/j.cyto.2003.09.004
36. Thomas JL, Wilk JE, Riviere LA, McGurk D, Castro CA, Hoge CW (2010) Prevalence of mental health problems and functional impairment among active component and National Guard soldiers 3 and 12 months following combat in Iraq. Arch Gen Psychiatry 67:614–623. doi:10.1001/archgenpsychiatry.2010.54
37. Uddin M, Aiello AE, Wildman DE, Koenen KC, Pawelec G, de Los Santos R, Goldmann E, Galea S (2010) Epigenetic and immune function profiles associated with posttraumatic stress disorder. Proc Natl Acad Sci U S A 107:9470–9475. doi:10.1073/pnas.0910794107
38. Vakoc CR, Mandat SA, Olenchock BA, Blobel GA (2005) Histone H3 lysine 9 methylation and HP1gamma are associated with transcription elongation through mammalian chromatin. Mol Cell 19:381–391. doi:10.1016/j.molcel.2005.06.011
39. Vire E, Brenner C, Deplus R, Blanchon L, Fraga M, Didelot C, Morey L, Van Eynde A, Bernard D, Vanderwinden JM, Bollen M, Esteller M, Di Croce L, de Launoit Y, Fuks F (2006) The Polycomb group protein EZH2 directly controls DNA methylation. Nature 439:871–874. doi:10.1038/nature04431
40. von Kanel R, Hepp U, Kraemer B, Traber R, Keel M, Mica L, Schnyder U (2007) Evidence for low-grade systemic proinflammatory activity in patients with posttraumatic stress disorder. J Psychiatr Res 41:744–752. doi:10.1016/j.jpsychires.2006.06.009
41. Wei G, Wei L, Zhu J, Zang C, Hu-Li J, Yao Z, Cui K, Kanno Y, Roh TY, Watford WT, Schones DE, Peng W, Sun HW, Paul WE, O’Shea JJ, Zhao K (2009) Global mapping of H3K4me3 and H3K27me3 reveals specificity and plasticity in lineage fate determination of differentiating CD4+ T cells. Immunity 30:155–167. doi:10.1016/j.immuni.2008.12.009
42. Zang C, Schones DE, Zeng C, Cui K, Zhao K, Peng W (2009) A clustering approach for identification of enriched domains from histone modification ChIP-Seq data. Bioinformatics 25:1952–1958. doi:10.1093/bioinformatics/btp340
43. Zhou VW, Goren A, Bernstein BE (2011) Charting histone modifications and the functional organization of mammalian genomes. Nat Rev Genet 12:7–18. doi:10.1038/nrg2905
44. Zhou J, Nagarkatti P, Zhong Y, Ginsberg JP, Singh NP, Zhang J, Nagarkatti M (2014) Dysregulation in microRNA expression is associated with alterations in immune functions in combat veterans with post-traumatic stress disorder. PLoS One 9:e94075. doi:10.1371/journal.pone.0094075. eCollection 2014