Systemic steroid exposure is associated with differential methylation in chronic obstructive pulmonary disease

American Journal of Respiratory and Critical Care Medicine

Volumn 186, Issue 12, 2012, Pages 1248-1255

  Wan, Emily S ^a,b   Qiu, Weiliang ^a   Baccarelli, Andrea ^c   Carey, Vincent J ^a   Bacherman, Helene ^a   Rennard, Stephen I ^d   Agustí, Alvar ^e   Anderson, Wayne H ^f   Lomas, David A ^g   DeMeo, Dawn L ^a,b  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^d UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^e UNIVERSITY OF BARCELONA   (Spain)

^f UNIVERSITY OF NORTH CAROLINA   (United States)

^g UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Chronic obstructive pulmonary disease; DNA methylation; Glucocorticoids

Indexed keywords

CORTICOSTEROID; STEROID;

ABHD16B GENE; ADULT; ARTICLE; AZU1 GENE; CHEMOTAXIS; CHRONIC OBSTRUCTIVE LUNG DISEASE; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; DRUG USE; FEMALE; FXYD1 GENE; GENE; GENE CLUSTER; GENE SEQUENCE; GRP97 GENE; HEMOSTASIS; HIPK3 GENE; HUMAN; INTERFERON REGULATORY FACTOR 7 GENE; LEUKOCYTE ACTIVATION; LPR3 GENE; LYMPHOCYTE ACTIVATION; MALE; PRIORITY JOURNAL; PROTEIN TRANSPORT; RABGEF1 GENE; SCNN1A GENE; SIT1 GENE; SLC22A18 GENE; SYSTEMIC THERAPY;

EID: 84871763019     PISSN: 1073449X     EISSN: 15354970     Source Type: Journal    
DOI: 10.1164/rccm.201207-1280OC     Document Type: Article

References (66)

1. Barnes PJ. Glucocorticosteroids: current and future directions. Br J Pharmacol 2011;163:29-43.
2. Barnes PJ, Adcock IM. Glucocorticoid resistance in inflammatory diseases. Lancet 2009;373:1905-1917.
3. Turner JD, Pelascini LP, Macedo JA, Muller CP. Highly individual methylation patterns of alternative glucocorticoid receptor promoters suggest individualized epigenetic regulatory mechanisms. Nucleic Acids Res 2008;36:7207-7218.
4. Wiench M, John S, Baek S, Johnson TA, Sung MH, Escobar T, Simmons CA, Pearce KH, Biddie SC, Sabo PJ, et al . DNA methylation status predicts cell type-specific enhancer activity. EMBO J 2011;30:3028-3039.
5. Oberlander TF, Weinberg J, Papsdorf M, Grunau R, Misri S, Devlin AM. Prenatal exposure to maternal depression, neonatal methylation of human glucocorticoid receptor gene (NR3C1) and infant cortisol stress responses. Epigenetics 2008;3:97-106.
6. Tyrka AR, Price LH, Marsit C, Walters OC, Carpenter LL. Childhood adversity and epigenetic modulation of the leukocyte glucocorticoid receptor: preliminary findings in healthy adults. PLoS ONE 2012;7:e30148.
7. Yang X, Ewald ER, Huo Y, Tamashiro KL, Salvatori R, Sawa A, Wand GS, Lee RS. Glucocorticoid-induced loss of DNA methylation in non-neuronal cells and potential involvement of DNMT1 in epigenetic regulation of Fkbp5. Biochem Biophys Res Commun 2012;420:570-575.
8. Menke A, Arloth J, Putz B, Weber P, Klengel T, Mehta D, Gonik M, Rex-Haffner M, Rubel J, Uhr M, et al. Dexamethasone stimulated gene expression in peripheral blood is a sensitive marker for glucocorticoid receptor resistance in depressed patients. Neuropsychopharmacology 2012;37:1455-1464.
9. Maranville JC, Luca F, Richards AL, Wen X, Witonsky DB, Baxter S, Stephens M, Di Rienzo A. Interactions between glucocorticoid treatment and cis-regulatory polymorphisms contribute to cellular response phenotypes. PLoS Genet 2011;7:e1002162.
10. Lee RS, Tamashiro KL, Yang X, Purcell RH, Huo Y, Rongione M, Potash JB, Wand GS. A measure of glucocorticoid load provided by DNA methylation of Fkbp5 in mice. Psychopharmacology (Berl) 2011;218:303-312.
11. Lu R, Au WC, Yeow WS, Hageman N, Pitha PM. Regulation of the promoter activity of interferon regulatory factor-7 gene: activation by interferon snd silencing by hypermethylation. J Biol Chem 2000;275:31805-31812.
12. Martinez-Arguelles DB, Papadopoulos V. Epigenetic regulation of the expression of genes involved in steroid hormone biosynthesis and action. Steroids 2010;75:467-476.
13. Turner JD, Alt SR, Cao L, Vernocchi S, Trifonova S, Battello N, Muller CP. Transcriptional control of the glucocorticoid receptor: CpG islands, epigenetics and more. Biochem Pharmacol 2010;80:1860-1868.
14. Wan ES, Qiu W, Bacherman H, Carey V, Baccarelli A, Rennard S, Agusti A, Lomas DA, DeMeo DL. Epigenome-wide impact of chronic systemic steroids in COPD. Am J Respir Crit Care Med 2012;185:A3482.
15. Patel BD, Coxson HO, Pillai SG, Agusti AG, Calverley PM, Donner CF, Make BJ, Muller NL, Rennard SI, Vestbo J, et al. Airway wall thickening and emphysema show independent familial aggregation in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2008;178:500-505.
16. Zhu G, Warren L, Aponte J, Gulsvik A, Bakke P, Anderson WH, Lomas DA, Silverman EK, Pillai SG. The SERPINE2 gene is associated with chronic obstructive pulmonary disease in two large populations. Am J Respir Crit Care Med 2007;176:167-173. (Pubitemid 47057853)
17. Silverman EK, Chapman HA, Drazen JM, Weiss ST, Rosner B, Campbell EJ, O'Donnell WJ, Reilly JJ, Ginns L, Mentzer S, et al. Genetic epidemiology of severe, early-onset chronic obstructive pulmonary disease: risk to relatives for airflow obstruction and chronic bronchitis. Am J Respir Crit Care Med 1998;157:1770-1778.
18. Wan ES, Qiu W, Baccarelli A, Carey VJ, Bacherman H, Rennard SI, Agusti A, Anderson W, Lomas DA, Demeo DL. Cigarette smoking behaviors and time since quitting are associated with differential DNA methylation across the human genome. Hum Mol Genet 2012;21:3073-3082.
19. Johnson WE, Li C, Rabinovic A. Adjusting batch effects in microarray expression data using empirical Bayes methods. Biostatistics 2007;8:118-127. (Pubitemid 44906106)
20. Leek JT, Storey JD. Capturing heterogeneity in gene expression studies by surrogate variable analysis. PLoS Genet 2007;3:1724-1735. (Pubitemid 47510264)
21. Leek JT, Storey JD. A general framework for multiple testing dependence. Proc Natl Acad Sci USA 2008;105:18718-18723.
22. Breslow NE, Clayton DG. Approximate inference in generalized linear mixed models. J Am Stat Assoc 1993;88:9-25.
23. Silverman EK, Weiss ST, Drazen JM, Chapman HA, Carey V, Campbell EJ, Denish P, Silverman RA, Celedon JC, Reilly JJ, et al. Gender-related differences in severe, early-onset chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2000;162:2152-2158. (Pubitemid 32051679)
24. Liptak T. On the combination of independent tests. Magyar Tud Akad Mat Kutato Int 1958;3:171-197.
25. Won S, Morris N, Lu Q, Elston RC. Choosing an optimal method to combine p-values. Stat Med 2009;28:1537-1553.
26. Huang DW, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009;4:44-57.
27. Huang DW, Sherman BT, Lempicki RA. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 2009;37:1-13.
28. Du P, Zhang X, Huang CC, Jafari N, Kibbe WA, Hou L, Lin SM. Comparison of beta-value and m-value methods for quantifying methylation levels by microarray analysis. BMC Bioinformatics 2010;11:587.
29. Swift I, Satti A, Kim V, Make BJ, Newell J, Steiner RM, Wilson C, Murphy JR, Silverman EK, Criner GJ. Demographic, physiologic and radiographic characteristics of COPD patients taking chronic systemic corticosteroids. COPD 2012;9:29-35.
30. Agarwal R, Aggarwal AN, Gupta D, Jindal SK. Inhaled corticosteroids vs placebo for preventing COPD exacerbations: a systematic review and metaregression of randomized controlled trials. Chest 2010;137:318-325.
31. Anttila S, Hakkola J, Tuominen P, Elovaara E, Husgafvel-Pursiainen K, Karjalainen A, Hirvonen A, Nurminen T. Methylation of cytochrome P4501A1 promoter in the lung is associated with tobacco smoking. Cancer Res 2003;63:8623-8628. (Pubitemid 38064036)
32. Ghotbi R, Gomez A, Milani L, Tybring G, Syvanen AC, Bertilsson L, Ingelman-Sundberg M, Aklillu E. Allele-specific expression and gene methylation in the control of CYP1A2 mRNA level in human livers. Pharmacogenomics J 2009;9:208-217.
33. Johnson CS, Chung I, Trump DL. Epigenetic silencing of cyp24 in the tumor microenvironment. J Steroid Biochem Mol Biol 2010;121:338-342.
34. Nakajima M, Iwanari M, Yokoi T. Effects of histone deacetylation and DNA methylation on the constitutive and TCDD-inducible expressions of the human CYP1 family in MCF-7 and HeLa cells. Toxicol Lett 2003;144:247-256. (Pubitemid 36966733)
35. Tokizane T, Shiina H, Igawa M, Enokida H, Urakami S, Kawakami T, Ogishima T, Okino ST, Li LC, Tanaka Y, et al. Cytochrome P450 1B1 is overexpressed and regulated by hypomethylation in prostate cancer. Clin Cancer Res 2005;11:5793-5801. (Pubitemid 41170305)
36. Kastrup IB, Worm J, Ralfkiaer E, Hokland P, Guldberg P, Gronbaek K. Genetic and epigenetic alterations of the reduced folate carrier in untreated diffuse large B-cell lymphoma. Eur J Haematol 2008;80:61-66. (Pubitemid 350265231)
37. Park JY, Helm JF, Zheng W, Ly QP, Hodul PJ, Centeno BA, Malafa MP. Silencing of the candidate tumor suppressor gene solute carrier family 5 member 8 (SLC5A8) in human pancreatic cancer. Pancreas 2008;36:e32-e39. (Pubitemid 351591592)
38. Sharma G, Mirza S, Parshad R, Srivastava A, Datta Gupta S, Pandya P, Ralhan R. CpG hypomethylation of MDR1 gene in tumor and serum of invasive ductal breast carcinoma patients. Clin Biochem 2010;43:373-379.
39. Cao-Lei L, Leija SC, Kumsta R, Wust S, Meyer J, Turner JD, Muller CP. Transcriptional control of the human glucocorticoid receptor: Identification and analysis of alternative promoter regions. Hum Genet 2011;129:533-543.
40. Iversen LF, Kastrup JS, Bjorn SE, Rasmussen PB, Wiberg FC, Flodgaard HJ, Larsen IK. Structure of HBP, a multifunctional protein with a serine proteinase fold. Nat Struct Biol 1997;4:265-268. (Pubitemid 27157197)
41. McCabe D, Cukierman T, Gabay JE. Basic residues in azurocidin/HBP contribute to both heparin binding and antimicrobial activity. J Biol Chem 2002;277:27477-27488. (Pubitemid 34951768)
42. Zimmer M, Medcalf RL, Fink TM, Mattmann C, Lichter P, Jenne DE. Three human elastase-like genes coordinately expressed in the myelomonocyte lineage are organized as a single genetic locus on 19pter. Proc Natl Acad Sci USA 1992;89:8215-8219.
43. Arndt B, Krieger T, Kalinski T, Thielitz A, Reinhold D, Roessner A, Schraven B, Simeoni L. The transmembrane adaptor protein SIT inhibits TCR-mediated signaling. PLoS ONE 2011;6:e23761.
44. Hubener C, Mincheva A, Lichter P, Schraven B, Bruyns E. Complete sequence, genomic organization, and chromosomal localization of the human gene encoding the SHP2-interacting transmembrane adaptor protein (SIT). Immunogenetics 2001;53:337-341. (Pubitemid 32678768)
45. Au WC, Moore PA, LaFleur DW, Tombal B, Pitha PM. Characterization of the interferon regulatory factor-7 and its potential role in the transcription activation of interferon a genes. J Biol Chem 1998;273:29210-29217. (Pubitemid 28507622)
46. Zhang L, Pagano JS. Irf-7, a new interferon regulatory factor associated with epstein-barr virus latency. Mol Cell Biol 1997;17:5748-5757. (Pubitemid 27411082)
47. Jaspers I, Horvath KM, Zhang W, Brighton LE, Carson JL, Noah TL. Reduced expression of IRF7 in nasal epithelial cells from smokers after infection with influenza. Am J Respir Cell Mol Biol 2010;43:368-375.
48. Takeyama K, Kitanaka S, Sato T, Kobori M, Yanagisawa J, Kato S. 25-Hydroxyvitamin D3 1alpha-hydroxylase and vitamin D synthesis. Science 1997;277:1827-1830.
49. Lan HC, Li HJ, Lin G, Lai PY, Chung BC. Cyclic amp stimulates SF-1-dependent CYP11A1 expression through homeodomain-interacting protein kinase 3-mediated Jun N-terminal kinase and c-Jun phosphorylation. Mol Cell Biol 2007;27:2027-2036. (Pubitemid 46418461)
50. Fredriksson R, Lagerstrom MC, Hoglund PJ, Schioth HB. Novel human G protein-coupled receptors with long N-terminals containing GPS domains and ser/thr-rich regions. FEBS Lett 2002;531:407-414. (Pubitemid 35336060)
51. Ishii H, Kim DH, Fujita T, Endo Y, Saeki S, Yamamoto TT. cDNA cloning of a new low-density lipoprotein receptor-related protein and mapping of its gene (LRP3) to chromosome bands 19q12-q13. 2. Genomics 1998;51:132-135. (Pubitemid 28373382)
52. Cooper PR, Smilinich NJ, Day CD, Nowak NJ, Reid LH, Pearsall RS, Reece M, Prawitt D, Landers J, Housman DE, et al. Divergently transcribed overlapping genes expressed in liver and kidney and located in the 11p15.5 imprinted domain. Genomics 1998;49:38-51. (Pubitemid 28194435)
53. Dao D, Frank D, Qian N, O'Keefe D, Vosatka RJ, Walsh CP, Tycko B. IMPT1, an imprinted gene similar to polyspecific transporter and multi-drug resistance genes. Hum Mol Genet 1998;7:597-608. (Pubitemid 28152258)
54. Sakatani T, Wei M, Katoh M, Okita C, Wada D, Mitsuya K, Meguro M, Ikeguchi M, Ito H, Tycko B, et al. Epigenetic heterogeneity at imprinted loci in normal populations. Biochem Biophys Res Commun 2001;283:1124-1130. (Pubitemid 32912884)
55. Ali AM, Bajaj V, Gopinath KS, Kumar A. Characterization of the human SLC22A18 gene promoter and its regulation by the transcription factor sp1. Gene 2009;429:37-43.
56. Chu SH, Feng DF, Ma YB, Zhang H, Zhu ZA, Li ZQ, Jiang PC. Promoter methylation and downregulation of SLC22A18 are associated with the development and progression of human glioma. J Transl Med 2011;9:156.
57. Gallagher E, Mc Goldrick A, Chung WY, Mc Cormack O, Harrison M, Kerin M, Dervan PA, Mc Cann A. Gain of imprinting of SLC22A18 sense and antisense transcripts in human breast cancer. Genomics 2006;88:12-17. (Pubitemid 43851174)
58. + channel. Am J Physiol 1994;266:L728-L734.
59. + channel: biophysical properties, pharmacology, ontogenesis, and molecular cloning. Proc Natl Acad Sci USA 1994;91:247-251.
60. Chow YH, Wang Y, Plumb J, O'Brodovich H, Hu J. Hormonal regulation and genomic organization of the human amiloride-sensitive epithelial sodium channel alpha subunit gene. Pediatr Res 1999;46:208-214. (Pubitemid 29362736)
61. Janer C, Pitkanen OM, Helve O, Andersson S. Airway expression of the epithelial sodium channel alpha-subunit correlates with cortisol in term newborns. Pediatrics 2011;128:e414-e421.
62. McTavish N, Getty J, Burchell A, Wilson SM. Glucocorticoids can activate the alpha-ENAC gene promoter independently of SGK1. Biochem J 2009;423:189-197.
63. Reddy TE, Pauli F, Sprouse RO, Neff NF, Newberry KM, Garabedian MJ, Myers RM. Genomic determination of the glucocorticoid response reveals unexpected mechanisms of gene regulation. Genome Res 2009;19:2163-2171.
64. Lit L, Sharp FR, Apperson M, Liu DZ, Walker WL, Liao I, Xu H, Ander BP, Wong B. Corticosteroid effects on blood gene expression in Duchenne muscular dystrophy. Pharmacogenomics J 2009;9:411-418.
65. Tantisira KG, Lasky-Su J, Harada M, Murphy A, Litonjua AA, Himes BE, Lange C, Lazarus R, Sylvia J, Klanderman B, et al. Genomewide association between GLCCI1 and response to glucocorticoid therapy in asthma. N Engl J Med 2011;365:1173-1183.
66. Qiu W, Baccarelli A, Carey VJ, Boutaoui N, Bacherman H, Klanderman B, Rennard S, Agusti A, Anderson W, Lomas DA, et al. Variable DNA methylation is associated with chronic obstructive pulmonary disease and lung function. Am J Respir Crit Care Med 2012;185:373-381.