Vitamin D receptor ChIP-seq in primary CD4+ cells: Relationship to serum 25-hydroxyvitamin D levels and autoimmune disease

BMC Medicine

Volumn 11, Issue 1, 2013, Pages

  Handel, Adam E ^a,b   Sandve, Geir K ^c   Disanto, Giulio ^a   Berlanga Taylor, Antonio J ^a   Gallone, Giuseppe ^a   Hanwell, Heather ^a   Drabløs, Finn ^d   Giovannoni, Gavin ^b   Ebers, George C ^a   Ramagopalan, Sreeram V ^a,b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^c UNIVERSITY OF OSLO   (Norway)

^d NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

Author keywords

Autoimmune disease; ChIP seq; Functional genomics; Vitamin D

Indexed keywords

25 HYDROXYVITAMIN D; CD4 ANTIGEN; DEOXYRIBONUCLEASE I; VITAMIN D RECEPTOR;

ARTICLE; ARTIFACT; ATOPIC DERMATITIS; AUTOIMMUNE DISEASE; BINDING SITE; BONE DENSITY; CD4+ T LYMPHOCYTE; CHRONIC LYMPHATIC LEUKEMIA; CONTROLLED STUDY; DNA PROTEIN COMPLEX; EXON; FEMALE; GENE EXPRESSION; GENE LINKAGE DISEQUILIBRIUM; GENETIC ASSOCIATION; GENOTYPE ENVIRONMENT INTERACTION; HELPER CELL; HISTONE MODIFICATION; HUMAN; HUMAN CELL; IN VIVO STUDY; ISCHEMIC HEART DISEASE; LYMPHOCYTE DIFFERENTIATION; MALE; NON INSULIN DEPENDENT DIABETES MELLITUS; NORMAL HUMAN; PRACTICE GUIDELINE; PROTEIN FOLDING; REGULATORY T LYMPHOCYTE; RNA PROCESSING; RNA SPLICING; T LYMPHOCYTE ACTIVATION; VITAMIN BLOOD LEVEL;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; AUTOIMMUNE DISEASES; BINDING SITES; CD4-POSITIVE T-LYMPHOCYTES; GENOMICS; HUMANS; PRIMARY CELL CULTURE; PROTEIN ARRAY ANALYSIS; RECEPTORS, CALCITRIOL; VITAMIN D;

EID: 84880008405     PISSN: None     EISSN: 17417015     Source Type: Journal    
DOI: 10.1186/1741-7015-11-163     Document Type: Article

References (49)

1. Lehmann B, Meurer M. Vitamin D metabolism. Dermatol Ther 2010, 23:2-12. 10.1111/j.1529-8019.2009.01286.x, 20136904.
2. Handel AE, Handunnetthi L, Ebers GC, Ramagopalan SV. Type 1 diabetes mellitus and multiple sclerosis: common etiological features. Nat Rev Endocrinol 2009, 5:655-664. 10.1038/nrendo.2009.216, 19884899.
3. Kriegel MA, Manson JE, Costenbader KH. Does vitamin D affect risk of developing autoimmune disease?: a systematic review. Semin Arthritis Rheum 2011, 40:512-531. 10.1016/j.semarthrit.2010.07.009, 3098920, 21047669.
4. Munger KL, Levin LI, Hollis BW, Howard NS, Ascherio A. Serum 25-hydroxyvitamin D levels and risk of multiple sclerosis. JAMA 2006, 296:2832-2838. 10.1001/jama.296.23.2832, 17179460.
5. Orgaz-Molina J, Buendía-Eisman A, Arrabal-Polo MA, Ruiz JC, Arias-Santiago S. Deficiency of serum concentration of 25-hydroxyvitamin D in psoriatic patients: a case-control study. J Am Acad Dermatol 2012, 67:931-938. 10.1016/j.jaad.2012.01.040, 22387034.
6. Li K, Shi Q, Yang L, Li X, Liu L, Wang L, Li Q, Wang G, Li C-Y, Gao T-W. The association of vitamin D receptor gene polymorphisms and serum 25-hydroxyvitamin D levels with generalized vitiligo. Br J Dermatol 2012, 167:815-821. 10.1111/j.1365-2133.2012.11132.x, 22762534.
7. McCullough ML, Bostick RM, Daniel CR, Flanders WD, Shaukat A, Davison J, Rangaswamy U, Hollis BW. Vitamin D status and impact of vitamin D3 and/or calcium supplementation in a randomized pilot study in the Southeastern United States. J Am Coll Nutr 2009, 28:678-686. 10.1080/07315724.2009.10719801, 20516268.
8. Issa LL, Leong GM, Eisman JA. Molecular mechanism of vitamin D receptor action. Inflamm Res 1998, 47:451-475. 10.1007/s000110050360, 9892040.
9. Ramagopalan SV, Heger A, Berlanga AJ, Maugeri NJ, Lincoln MR, Burrell A, Handunnetthi L, Handel AE, Disanto G, Orton S-M, Watson CT, Morahan JM, Giovannoni G, Ponting CP, Ebers GC, Knight JC. A ChIP-seq defined genome-wide map of vitamin D receptor binding: associations with disease and evolution. Genome Res 2010, 20:1352-1360. 10.1101/gr.107920.110, 2945184, 20736230.
10. Heikkinen S, Väisänen S, Pehkonen P, Seuter S, Benes V, Carlberg C. Nuclear hormone 1α,25-dihydroxyvitamin D3 elicits a genome-wide shift in the locations of VDR chromatin occupancy. Nucleic Acids Res 2011, 39:9181-9193. 10.1093/nar/gkr654, 3241659, 21846776.
11. Carlberg C, Seuter S, Heikkinen S. The first genome-wide view of vitamin D receptor locations and their mechanistic implications. Anticancer Res 2012, 32:271-282.
12. Shirley MD, Baugher JD, Stevens EL, Tang Z, Gerry N, Beiswanger CM, Berlin DS, Pevsner J. Chromosomal variation in lymphoblastoid cell lines. Hum Mutat 2012, 33:1075-1086. 10.1002/humu.22062, 3370055, 22374857.
13. Caliskan M, Cusanovich DA, Ober C, Gilad Y. The effects of EBV transformation on gene expression levels and methylation profiles. Hum Mol Genet 2011, 20:1643-1652. 10.1093/hmg/ddr041, 3063990, 21289059.
14. Owen TA, Aronow MS, Barone LM, Bettencourt B, Stein GS, Lian JB. Pleiotropic effects of vitamin D on osteoblast gene expression are related to the proliferative and differentiated state of the bone cell phenotype: dependency upon basal levels of gene expression, duration of exposure, and bone matrix competency in normal rat osteoblast cultures. Endocrinology 1991, 128:1496-1504. 10.1210/endo-128-3-1496, 1999168.
15. Berglund D, Korsgren O, Lorant T, Schneider K, Tufveson G, Carlsson B. Isolation, expansion and functional assessment of CD4 + CD25 + FoxP3+ regulatory T cells and Tr1 cells from uremic patients awaiting kidney transplantation. Transpl Immunol 2012, 26:27-33. 10.1016/j.trim.2011.09.003, 21958749.
16. Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 2009, 10:R25. 10.1186/gb-2009-10-3-r25, 2690996, 19261174.
17. Rashid NU, Giresi PG, Ibrahim JG, Sun W, Lieb JD. ZINBA integrates local covariates with DNA-seq data to identify broad and narrow regions of enrichment, even within amplified genomic regions. Genome Biol 2011, 12:R67. 10.1186/gb-2011-12-7-r67, 3218829, 21787385.
18. Kundaje A. A comprehensive collection of signal artifact blacklist regions in the human genome ENCODE. [hg19-blacklist-README.doc - EBI]. https://sites.google.com/site/anshulkundaje/projects/blacklists (last accessed 30/06/2013).
19. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, Nusbaum C, Myers RM, Brown M, Li W, Liu XS. Model-based analysis of ChIP-Seq (MACS). Genome Biol 2008, 9:R137. 10.1186/gb-2008-9-9-r137, 2592715, 18798982.
20. Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 2009, 37:W202-W208. 10.1093/nar/gkp335, 2703892, 19458158.
21. Pavesi G, Mereghetti P, Mauri G, Pesole G. Weeder Web: discovery of transcription factor binding sites in a set of sequences from co-regulated genes. Nucleic Acids Res 2004, 32:W199-W203. 10.1093/nar/gkh465, 441603, 15215380.
22. Kulakovskiy IV, Boeva VA, Favorov AV, Makeev VJ. Deep and wide digging for binding motifs in ChIP-Seq data. Bioinformatics 2010, 26:2622-2623. 10.1093/bioinformatics/btq488, 20736340.
23. Martens JHA, Brinkman AB, Simmer F, Francoijs K-J, Nebbioso A, Ferrara F, Altucci L, Stunnenberg HG. PML-RARalpha/RXR alters the epigenetic landscape in acute promyelocytic leukemia. Cancer Cell 2010, 17:173-185. 10.1016/j.ccr.2009.12.042, 20159609.
24. Thomas-Chollier M, Herrmann C, Defrance M, Sand O, Thieffry D, van Helden J. RSAT peak-motifs: motif analysis in full-size ChIP-seq datasets. Nucleic Acids Res 2012, 40:e31. 10.1093/nar/gkr1104, 3287167, 22156162.
25. Grant CE, Bailey TL, Noble WS. FIMO: scanning for occurrences of a given motif. Bioinformatics 2011, 27:1017-1018. 10.1093/bioinformatics/btr064, 3065696, 21330290.
26. McLean CY, Bristor D, Hiller M, Clarke SL, Schaar BT, Lowe CB, Wenger AM, Bejerano G. GREAT improves functional interpretation of cis-regulatory regions. Nat Biotechnol 2010, 28:495-501. 10.1038/nbt.1630, 20436461.
27. Sandve GK, Gundersen S, Rydbeck H, Glad IK, Holden L, Holden M, Liestøl K, Clancy T, Ferkingstad E, Johansen M, Nygaard V, Tøstesen E, Frigessi A, Hovig E. The Genomic HyperBrowser: inferential genomics at the sequence level. Genome Biol 2010, 11:R121. 10.1186/gb-2010-11-12-r121, 3046481, 21182759.
28. Gundersen S, Kalaš M, Abul O, Frigessi A, Hovig E, Sandve GK. Identifying elemental genomic track types and representing them uniformly. BMC Bioinformatics 2011, 12:494. 10.1186/1471-2105-12-494, 3315820, 22208806.
29. Hindorff LA, Sethupathy P, Junkins HA, Ramos EM, Mehta JP, Collins FS, Manolio TA. Potential etiologic and functional implications of genome-wide association loci for human diseases and traits. Proc Natl Acad Sci USA 2009, 106:9362-9367. 10.1073/pnas.0903103106, 2687147, 19474294.
30. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G. Gene ontology: tool for the unification of biology, The Gene Ontology Consortium. Nat Genet 2000, 25:25-29. 10.1038/75556, 3037419, 10802651.
31. Fujita PA, Rhead B, Zweig AS, Hinrichs AS, Karolchik D, Cline MS, Goldman M, Barber GP, Clawson H, Coelho A, Diekhans M, Dreszer TR, Giardine BM, Harte RA, Hillman-Jackson J, Hsu F, Kirkup V, Kuhn RM, Learned K, Li CH, Meyer LR, Pohl A, Raney BJ, Rosenbloom KR, Smith KE, Haussler D, Kent WJ. The UCSC Genome Browser database: update 2011. Nucleic Acids Res 2011, 39:D876-D882. 10.1093/nar/gkq963, 3242726, 20959295.
32. Liu T, Ortiz JA, Taing L, Meyer CA, Lee B, Zhang Y, Shin H, Wong SS, Ma J, Lei Y, Pape UJ, Poidinger M, Chen Y, Yeung K, Brown M, Turpaz Y, Liu XS. Cistrome: an integrative platform for transcriptional regulation studies. Genome Biol 2011, 12:R83. 10.1186/gb-2011-12-8-r83, 3245621, 21859476.
33. The ENCODE (ENCyclopedia Of DNA Elements) Project. Science 2004, 306:636-640.
34. Sanyal A, Lajoie BR, Jain G, Dekker J. The long-range interaction landscape of gene promoters. Nature 2012, 489:109-113. 10.1038/nature11279, 3555147, 22955621.
35. Bernstein BE, Birney E, Dunham I, Green ED, Gunter C, Snyder M. An integrated encyclopedia of DNA elements in the human genome. Nature 2012, 489:57-74. 10.1038/nature11247, 3439153, 22955616.
36. Birzele F, Fauti T, Stahl H, Lenter MC, Simon E, Knebel D, Weith A, Hildebrandt T, Mennerich D. Next-generation insights into regulatory T cells: expression profiling and FoxP3 occupancy in Human. Nucleic Acids Res 2011, 39:7946-7960. 10.1093/nar/gkr444, 3185410, 21729870.
37. Souberbielle J-C, Body J-J, Lappe JM, Plebani M, Shoenfeld Y, Wang TJ, Bischoff-Ferrari HA, Cavalier E, Ebeling PR, Fardellone P, Gandini S, Gruson D, Guérin AP, Heickendorff L, Hollis BW, Ish-Shalom S, Jean G, von Landenberg P, Largura A, Olsson T, Pierrot-Deseilligny C, Pilz S, Tincani A, Valcour A, Zittermann A. Vitamin D and musculoskeletal health, cardiovascular disease, autoimmunity and cancer: recommendations for clinical practice. Autoimmun Rev 2010, 9:709-715. 10.1016/j.autrev.2010.06.009, 20601202.
38. Bailey TL, Machanick P. Inferring direct DNA binding from ChIP-seq. Nucleic Acids Res 2012, 40:e128. 10.1093/nar/gks433, 3458523, 22610855.
39. Sandelin A, Wasserman WW. Constrained binding site diversity within families of transcription factors enhances pattern discovery bioinformatics. J Mol Biol 2004, 338:207-215. 10.1016/j.jmb.2004.02.048, 15066426.
40. Wingender E, Dietze P, Karas H, Knüppel R. TRANSFAC: a database on transcription factors and their DNA binding sites. Nucleic Acids Res 1996, 24:238-241. 10.1093/nar/24.1.238, 145586, 8594589.
41. Bailey TL, Gribskov M. Methods and statistics for combining motif match scores. J Comput Biol 1998, 5:211-221. 10.1089/cmb.1998.5.211, 9672829.
42. Boyle AP, Hong EL, Hariharan M, Cheng Y, Schaub MA, Kasowski M, Karczewski KJ, Park J, Hitz BC, Weng S, Cherry JM, Snyder M. Annotation of functional variation in personal genomes using RegulomeDB. Genome Res 2012, 22:1790-1797. 10.1101/gr.137323.112, 3431494, 22955989.
43. Huang Y-C, Chen J-Y, Hung W-C. Vitamin D3 receptor/Sp1 complex is required for the induction of p27Kip1 expression by vitamin D3. Oncogene 2004, 23:4856-4861. 10.1038/sj.onc.1207621, 15064717.
44. Tolón RM, Castillo AI, Jiménez-Lara AM, Aranda A. Association with Ets-1 causes ligand- and AF2-independent activation of nuclear receptors. Mol Cell Biol 2000, 20:8793-8802. 10.1128/MCB.20.23.8793-8802.2000, 86515, 11073980.
45. Marshall PA, Hernandez Z, Kaneko I, Widener T, Tabacaru C, Aguayo I, Jurutka PW. Discovery of novel vitamin D receptor interacting proteins that modulate 1,25-dihydroxyvitamin D3 signaling. J Steroid Biochem Mol Biol 2012, 132:147-159. 10.1016/j.jsbmb.2012.05.001, 22626544.
46. Salehi-Tabar R, Nguyen-Yamamoto L, Tavera-Mendoza LE, Quail T, Dimitrov V, An B-S, Glass L, Goltzman D, White JH. Vitamin D receptor as a master regulator of the c-MYC/MXD1 network. Proc Natl Acad Sci U S A 2012, 109:18827-18832. 10.1073/pnas.1210037109, 3503153, 23112173.
47. Weth O, Weth C, Bartkuhn M, Leers J, Uhle F, Renkawitz R. Modular insulators: genome wide search for composite CTCF/thyroid hormone receptor binding sites. PLoS One 2010, 5:e10119. 10.1371/journal.pone.0010119, 2852416, 20404925.
48. Ross-Innes CS, Brown GD, Carroll JS. A co-ordinated interaction between CTCF and ER in breast cancer cells. BMC Genomics 2011, 12:593. 10.1186/1471-2164-12-593, 3248577, 22142239.
49. Lutz M, Burke LJ, LeFevre P, Myers FA, Thorne AW, Crane-Robinson C, Bonifer C, Filippova GN, Lobanenkov V, Renkawitz R. Thyroid hormone-regulated enhancer blocking: cooperation of CTCF and thyroid hormone receptor. EMBO J 2003, 22:1579-g1587. 10.1093/emboj/cdg147, 152892, 12660164.