DNA methylation dynamics during ex vivo differentiation and maturation of human dendritic cells

Epigenetics and Chromatin

Volumn 7, Issue 1, 2014, Pages

  Zhang, Xue ^a   Ulm, Ashley ^a   Somineni, Hari K ^a   Oh, Sunghee ^b   Weirauch, Matthew T ^a   Zhang, Hong Xuan ^c   Chen, Xiaoting ^d   Lehn, Maria A ^a   Janssen, Edith M ^a   Ji, Hong ^a  

^a CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^b Kim Sook Za Children's Hospital Medical Center Research Foundation   (South Korea)

^c PROCTER AND GAMBLE COMPANY   (United States)

^d 705 Engineering Research Center   (United States)

Author keywords

Differentiation; DNA methylation; DNMT; Human dendritic cells; Maturation; Monocytes; TET

Indexed keywords

5 METHYLCYTOSINE; DNA; RNA; TRANSCRIPTION FACTOR;

ARTICLE; CELL DIFFERENTIATION; CELL MATURATION; CELL SELECTION; CONTROLLED STUDY; DENDRITIC CELL; DNA ISOLATION; DNA METHYLATION; DNMT1 GENE; DNMT3A GENE; DNMT3B GENE; EX VIVO STUDY; FLOW CYTOMETRY; GENE EXPRESSION; GENE MAPPING; HUMAN; HUMAN CELL; IMMUNE RESPONSE; MICROARRAY ANALYSIS; MONOCYTE; PHENOTYPE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PYROSEQUENCING; RNA ISOLATION; TET2 GENE; UPREGULATION;

EID: 84988932995     PISSN: None     EISSN: 17568935     Source Type: Journal    
DOI: 10.1186/1756-8935-7-21     Document Type: Article

References (96)

1. Steinman RM: Decisions about dendritic cells: past, present, and future. Annu Rev Immunol 2012, 30:1-22.
2. Cao H, Verge V, Baron C, Martinache C, Leon A, Scholl S, Gorin NC, Salamero J, Assari S, Bernard J, Lopez M: In vitro generation of dendritic cells from human blood monocytes in experimental conditions compatible for in vivo cell therapy. J Hematother Stem Cell Res 2000, 9:183-194.
3. Randolph GJ, Inaba K, Robbiani DF, Steinman RM, Muller WA: Differentiation of phagocytic monocytes into lymph node dendritic cells in vivo. Immunity 1999, 11:753-761.
4. Lung TL, Saurwein-Teissl M, Parson W, Schonitzer D, Grubeck-Loebenstein B: Unimpaired dendritic cells can be derived from monocytes in old age and can mobilize residual function in senescent T cells. Vaccine 2000, 18:1606-1612.
5. Jonuleit H, Kuhn U, Muller G, Steinbrink K, Paragnik L, Schmitt E, Knop J, Enk AH: Pro-inflammatory cytokines and prostaglandins induce maturation of potent immunostimulatory dendritic cells under fetal calf serum-free conditions. Eur J Immunol 1997, 27:3135-3142.
6. MacDonald KP, Munster DJ, Clark GJ, Dzionek A, Schmitz J, Hart DN: Characterization of human blood dendritic cell subsets. Blood 2002, 100:4512-4520.
7. Jongbloed SL, Kassianos AJ, McDonald KJ, Clark GJ, Ju X, Angel CE, Chen CJ, Dunbar PR, Wadley RB, Jeet V, Vulink AJ, Hart DN, Radford KJ: Human CD141+ (BDCA-3) + dendritic cells (DCs) represent a unique myeloid DC subset that cross-presents necrotic cell antigens. J Exp Med 2010, 207:1247-1260.
8. Poulin LF, Salio M, Griessinger E, Anjos-Afonso F, Craciun L, Chen JL, Keller AM, Joffre O, Zelenay S, Nye E, Le Moine A, Faure F, Donckier V, Sancho D, Cerundolo V, Bonnet D, Reis E Sousa C: Characterization of human DNGR-1+ BDCA3+ leukocytes as putative equivalents of mouse CD8alpha + dendritic cells. J Exp Med 2010, 207:1261-1271.
9. Satpathy AT, Wu X, Albring JC, Murphy KM: Re(de)fining the dendritic cell lineage. Nat Immunol 2012, 13:1145-1154.
10. Ji H, Ehrlich LI, Seita J, Murakami P, Doi A, Lindau P, Lee H, Aryee MJ, Irizarry RA, Kim K, Rossi DJ, Inlay MA, Serwold T, Karsunky H, Ho L, Daley GQ, Weissman IL, Feinberg AP: Comprehensive methylome map of lineage commitment from haematopoietic progenitors. Nature 2010, 467:338-342.
11. Deaton AM, Webb S, Kerr AR, Illingworth RS, Guy J, Andrews R, Bird A: Cell type-specific DNA methylation at intragenic CpG islands in the immune system. Genome Res 2011, 21:1074-1086.
12. Bullwinkel J, Ludemann A, Debarry J, Singh PB: Epigenotype switching at the CD14 and CD209 genes during differentiation of human monocytes to dendritic cells. Epigenetics 2011, 6:45-51.
13. Bock C, Beerman I, Lien WH, Smith ZD, Gu H, Boyle P, Gnirke A, Fuchs E, Rossi DJ, Meissner A: DNA methylation dynamics during in vivo differentiation of blood and skin stem cells. Mol Cell 2012, 47:633-647.
14. Ooi SK, Bestor TH: The colorful history of active DNA demethylation. Cell 2008, 133:1145-1148.
15. Gao Y, Chen J, Li K, Wu T, Huang B, Liu W, Kou X, Zhang Y, Huang H, Jiang Y, Yao C, Liu X, Lu Z, Xu Z, Kang L, Chen J, Wang H, Cai T, Gao S: Replacement of Oct4 by Tet1 during iPSC induction reveals an important role of DNA methylation and hydroxymethylation in reprogramming. Cell Stem Cell 2013, 12:453-469.
16. Booth MJ, Ost TW, Beraldi D, Bell NM, Branco MR, Reik W, Balasubramanian S: Oxidative bisulfite sequencing of 5-methylcytosine and 5-hydroxymethylcytosine. Nat Protoc 2013, 8:1841-1851.
17. Ito S, Shen L, Dai Q, Wu SC, Collins LB, Swenberg JA, He C, Zhang Y: Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science 2011, 333:1300-1303.
18. Klug M, Heinz S, Gebhard C, Schwarzfischer L, Krause SW, Andreesen R, Rehli M: Active DNA demethylation in human postmitotic cells correlates with activating histone modifications, but not transcription levels. Genome Biol 2010, 11:R63.
19. Kalinski P, Muthuswamy R, Urban J: Dendritic cells in cancer immunotherapy: vaccines and combination immunotherapies. Expert Rev Vaccines 2013, 12:285-295.
20. Heintzman ND, Hon GC, Hawkins RD, Kheradpour P, Stark A, Harp LF, Ye Z, Lee LK, Stuart RK, Ching CW, Ching KA, Antosiewicz-Bourget JE, Liu H, Zhang X, Green RD, Lobanenkov VV, Stewart R, Thomson JA, Crawford GE, Kellis M, Ren B: Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 2009, 459:108-112.
21. Heintzman ND, Stuart RK, Hon G, Fu Y, Ching CW, Hawkins RD, Barrera LO, Van Calcar S, Qu C, Ching KA, Wang W, Weng Z, Green RD, Crawford GE, Ren B: Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat Genet 2007, 39:311-318.
22. Thurman RE, Rynes E, Humbert R, Vierstra J, Maurano MT, Haugen E, Sheffield NC, Stergachis AB, Wang H, Vernot B, Garg K, John S, Sandstrom R, Bates D, Boatman L, Canfield TK, Diegel M, Dunn D, Ebersol AK, Frum T, Giste E, Johnson AK, Johnson EM, Kutyavin T, Lajoie B, Lee BK, Lee K, London D, Lotakis D, Neph S, et al: The accessible chromatin landscape of the human genome. Nature 2012, 489:75-82.
23. Glasmacher E, Agrawal S, Chang AB, Murphy TL, Zeng W, Vander Lugt B, Khan AA, Ciofani M, Spooner CJ, Rutz S, Hackney J, Nurieva R, Escalante CR, Ouyang W, Littman DR, Murphy KM, Singh H: A genomic regulatory element that directs assembly and function of immune-specific AP-1-IRF complexes. Science 2012, 338:975-980.
24. Becker AM, Michael DG, Satpathy AT, Sciammas R, Singh H, Bhattacharya D: IRF-8 extinguishes neutrophil production and promotes dendritic cell lineage commitment in both myeloid and lymphoid mouse progenitors. Blood 2012, 119:2003-2012.
25. Ohtsuka H, Sakamoto A, Pan J, Inage S, Horigome S, Ichii H, Arima M, Hatano M, Okada S, Tokuhisa T: Bcl6 is required for the development of mouse CD4+ and CD8alpha + dendritic cells. J Immunol 2011, 186:255-263.
26. Hambleton S, Salem S, Bustamante J, Bigley V, Boisson-Dupuis S, Azevedo J, Fortin A, Haniffa M, Ceron-Gutierrez L, Bacon CM, Menon G, Trouillet C, McDonald D, Carey P, Ginhoux F, Alsina L, Zumwalt TJ, Kong XF, Kumararatne D, Butler K, HubeauM, Feinberg J, Al-Muhsen S, Cant A, Abel L, Chaussabel D, Doffinger R, Talesnik E, Grumach A, Duarte A, et al: IRF8 mutations and human dendritic-cell immunodeficiency. N Engl JMed 2011, 365:127-138.
27. Edelson BT, Kc W, Juang R, Kohyama M, Benoit LA, Klekotka PA, Moon C, Albring JC, Ise W, Michael DG, Bhattacharya D, Stappenbeck TS, Holtzman MJ, Sung SS, Murphy TL, Hildner K, Murphy KM: Peripheral CD103+ dendritic cells form a unified subset developmentally related to CD8alpha + conventional dendritic cells. J Exp Med 2010, 207:823-836.
28. Hildner K, Edelson BT, Purtha WE, Diamond M, Matsushita H, Kohyama M, Calderon B, Schraml BU, Unanue ER, Diamond MS, Schreiber RD, Murphy TL, Murphy KM: Batf3 deficiency reveals a critical role for CD8alpha + dendritic cells in cytotoxic T cell immunity. Science 2008, 322:1097-1100.
29. Poulin LF, Reyal Y, Uronen-Hansson H, Schraml BU, Sancho D, Murphy KM, Hakansson UK, Moita LF, Agace WW, Bonnet D, Reis e Sousa C: DNGR-1 is a specific and universal marker of mouse and human Batf3-dependent dendritic cells in lymphoid and nonlymphoid tissues. Blood 2012, 119:6052-6062.
30. Suzuki S, Honma K, Matsuyama T, Suzuki K, Toriyama K, Akitoyo I, Yamamoto K, Suematsu T, Nakamura M, Yui K, Kumatori A: Critical roles of interferon regulatory factor 4 in CD11bhighCD8alpha-dendritic cell development. Proc Natl Acad Sci U S A 2004, 101:8981-8986.
31. Ghosh HS, Cisse B, Bunin A, Lewis KL, Reizis B: Continuous expression of the transcription factor e2-2 maintains the cell fate of mature plasmacytoid dendritic cells. Immunity 2010, 33:905-916.
32. Schotte R, Nagasawa M, Weijer K, Spits H, Blom B: The ETS transcription factor Spi-B is required for human plasmacytoid dendritic cell development. J Exp Med 2004, 200:1503-1509.
33. Ouaaz F, Arron J, Zheng Y, Choi Y, Beg AA: Dendritic cell development and survival require distinct NF-kappaB subunits. Immunity 2002, 16:257-270.
34. Vakkila J, Demarco RA, Lotze MT: Coordinate NF-kappaB and STAT1 activation promotes development of myeloid type 1 dendritic cells. Scand J Immunol 2008, 67:260-269.
35. Vorderstrasse BA, Kerkvliet NI: 2,3,7,8-Tetrachlorodibenzo-p-dioxin affects the number and function of murine splenic dendritic cells and their expression of accessory molecules. Toxicol Appl Pharmacol 2001, 171:117-125.
36. Lee JA, Hwang JA, Sung HN, Jeon CH, Gill BC, Youn HJ, Park JH: 2,3,7,8-Tetrachlorodibenzo-p-dioxin modulates functional differentiation of mouse bone marrow-derived dendritic cells Downregulation of RelB by 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicol Lett 2007, 173:31-40.
37. Ruby CE, Funatake CJ, Kerkvliet NI: 2,3,7,8 Tetrachlorodibenzo-p-Dioxin (TCDD) Directly Enhances the Maturation and Apoptosis of Dendritic Cells In Vitro. J Immunotoxicol 2005, 1:159-166.
38. Hao N, Whitelaw ML: The emerging roles of AhR in physiology and immunity. Biochem Pharmacol 2013, 86:561-570.
39. Nguyen NT, Kimura A, Nakahama T, Chinen I, Masuda K, Nohara K, Fujii-Kuriyama Y, Kishimoto T: Aryl hydrocarbon receptor negatively regulates dendritic cell immunogenicity via a kynurenine-dependent mechanism. Proc Natl Acad Sci U S A 2010, 107:19961-19966.
40. Klotz L, Dani I, Edenhofer F, Nolden L, Evert B, Paul B, Kolanus W, Klockgether T, Knolle P, Diehl L: Peroxisome proliferator-activated receptor gamma control of dendritic cell function contributes to development of CD4+ T cell anergy. J Immunol 2007, 178:2122-2131.
41. Szatmari I, Torocsik D, Agostini M, Nagy T, Gurnell M, Barta E, Chatterjee K, Nagy L: PPARgamma regulates the function of human dendritic cells primarily by altering lipid metabolism. Blood 2007, 110:3271-3280.
42. Majai G, Gogolak P, Ambrus C, Vereb G, Hodrea J, Fesus L, Rajnavolgyi E: PPARgamma modulated inflammatory response of human dendritic cell subsets to engulfed apoptotic neutrophils. J Leukoc Biol 2010, 88:981-991.
43. Szatmari I, Rajnavolgyi E, Nagy L: PPARgamma, a lipid-activated transcription factor as a regulator of dendritic cell function. Ann N Y Acad Sci 2006, 1088:207-218.
44. Park D, Lapteva N, Seethammagari M, Slawin KM, Spencer DM: An essential role for Akt1 in dendritic cell function and tumor immunotherapy. Nat Biotechnol 2006, 24:1581-1590.
45. Otterbein LE, Choi AM: Heme oxygenase: colors of defense against cellular stress. Am J Physiol Lung Cell Mol Physiol 2000, 279:L1029-L1037.
46. Chauveau C, Remy S, Royer PJ, Hill M, Tanguy-Royer S, Hubert FX, Tesson L, Brion R, Beriou G, Gregoire M, Josien R, Cuturi MC, Anegon I: Heme oxygenase-1 expression inhibits dendritic cell maturation and proinflammatory function but conserves IL-10 expression. Blood 2005, 106:1694-1702.
47. Tardif V, Riquelme SA, Remy S, Carreno LJ, Cortes CM, Simon T, Hill M, Louvet C, Riedel CA, Blancou P, Bach JM, Chauveau C, Bueno SM, Anegon I, Kalergis AM: Carbon monoxide decreases endosome-lysosome fusion and inhibits soluble antigen presentation by dendritic cells to T cells. Eur J Immunol 2013, 43:2832-2844.
48. Dhodapkar KM, Banerjee D, Connolly J, Kukreja A, Matayeva E, Veri MC, Ravetch JV, Steinman RM, Dhodapkar MV: Selective blockade of the inhibitory Fcgamma receptor (FcgammaRIIB) in human dendritic cells and monocytes induces a type I interferon response program. J Exp Med 2007, 204:1359-1369.
49. Heystek HC, Thierry AC, Soulard P, Moulon C: Phosphodiesterase 4 inhibitors reduce human dendritic cell inflammatory cytokine production and Th1-polarizing capacity. Int Immunol 2003, 15:827-835.
50. Clayton A, Harris CL, Court J, Mason MD, Morgan BP: Antigen-presenting cell exosomes are protected from complement-mediated lysis by expression of CD55 and CD59. Eur J Immunol 2003, 33:522-531.
51. Mezger M, Wozniok I, Blockhaus C, Kurzai O, Hebart H, Einsele H, Loeffler J: Impact of mycophenolic acid on the functionality of human polymorphonuclear neutrophils and dendritic cells during interaction with Aspergillus fumigatus. Antimicrob Agents Chemother 2008, 52:2644-2646.
52. Zheng Y, Manzotti CN, Liu M, Burke F, Mead KI, Sansom DM: CD86 and CD80 differentially modulate the suppressive function of human regulatory T cells. J Immunol 2004, 172:2778-2784.
53. Orabona C, Grohmann U, Belladonna ML, Fallarino F, Vacca C, Bianchi R, Bozza S, Volpi C, Salomon BL, Fioretti MC, Romani L, Puccetti P: CD28 induces immunostimulatory signals in dendritic cells via CD80 and CD86. Nat Immunol 2004, 5:1134-1142.
54. Schwarz AM, Banning-Eichenseer U, Seidel K, Mauz-Korholz C, Korholz D, Staege MS: Impact of interleukin-10 on phenotype and gene expression during early monocyte differentiation into dendritic cells. Anticancer Res 2013, 33:4791-4798.
55. De Smedt T, Van Mechelen M, De Becker G, Urbain J, Leo O, Moser M: Effect of interleukin-10 on dendritic cell maturation and function. Eur J Immunol 1997, 27:1229-1235.
56. Dieu MC, Vanbervliet B, Vicari A, Bridon JM, Oldham E, Ait-Yahia S, Briere F, Zlotnik A, Lebecque S, Caux C: Selective recruitment of immature and mature dendritic cells by distinct chemokines expressed in different anatomic sites. J Exp Med 1998, 188:373-386.
57. Sallusto F, Schaerli P, Loetscher P, Schaniel C, Lenig D, Mackay CR, Qin S, Lanzavecchia A: Rapid and coordinated switch in chemokine receptor expression during dendritic cell maturation. Eur J Immunol 1998, 28:2760-2769.
58. Riol-Blanco L, Sanchez-Sanchez N, Torres A, Tejedor A, Narumiya S, Corbi AL, Sanchez-Mateos P, Rodriguez-Fernandez JL: The chemokine receptor CCR7 activates in dendritic cells two signaling modules that independently regulate chemotaxis and migratory speed. J Immunol 2005, 174:4070-4080.
59. Li K, Fazekasova H, Wang N, Sagoo P, Peng Q, Khamri W, Gomes C, Sacks SH, Lombardi G, Zhou W: Expression of complement components, receptors and regulators by human dendritic cells. Mol Immunol 2011, 48:1121-1127.
60. Doi A, Park IH, Wen B, Murakami P, Aryee MJ, Irizarry R, Herb B, Ladd-Acosta C, Rho J, Loewer S, Miller J, Schlaeger T, Daley GQ, Feinberg AP: Differential methylation of tissue-and cancer-specific CpG island shores distinguishes human induced pluripotent stem cells, embryonic stem cells and fibroblasts. Nat Genet 2009, 41:1350-1353.
61. Irizarry RA, Ladd-Acosta C, Wen B, Wu Z, Montano C, Onyango P, Cui H, Gabo K, Rongione M, Webster M, Ji H, Potash JB, Sabunciyan S, Feinberg AP: The human colon cancer methylome shows similar hypo-and hypermethylation at conserved tissue-specific CpG island shores. Nat Genet 2009, 41:178-186.
62. Robbins SH, Walzer T, Dembele D, Thibault C, Defays A, Bessou G, Xu H, Vivier E, Sellars M, Pierre P, Sharp FR, Chan S, Kastner P, Dalod M: Novel insights into the relationships between dendritic cell subsets in human and mouse revealed by genome-wide expression profiling. Genome Biol 2008, 9:R17.
63. Fujiki K, Shinoda A, Kano F, Sato R, Shirahige K, Murata M: PPARgamma-induced PARylation promotes local DNA demethylation by production of 5-hydroxymethylcytosine. Nat Commun 2013, 4:2262.
64. D'Angelo R, Aresta S, Blangy A, Del Maestro L, Louvard D, Arpin M: Interaction of ezrin with the novel guanine nucleotide exchange factor PLEKHG6 promotes RhoG-dependent apical cytoskeleton rearrangements in epithelial cells. Mol Biol Cell 2007, 18:4780-4793.
65. Asiedu M, Wu D, Matsumura F, Wei Q: Centrosome/spindle pole-associated protein regulates cytokinesis via promoting the recruitment of MyoGEF to the central spindle. Mol Biol Cell 2009, 20:1428-1440.
66. Wu D, Asiedu M, Adelstein RS, Wei Q: A novel guanine nucleotide exchange factor MyoGEF is required for cytokinesis. Cell Cycle 2006, 5:1234-1239.
67. Chow A, Toomre D, Garrett W, Mellman I: Dendritic cell maturation triggers retrograde MHC class II transport from lysosomes to the plasma membrane. Nature 2002, 418:988-994.
68. Boes M, Bertho N, Cerny J, Op den Brouw M, Kirchhausen T, Ploegh H: T cells induce extended class II MHC compartments in dendritic cells in a Toll-like receptor-dependent manner. J Immunol 2003, 171:4081-4088.
69. Evans R, Patzak I, Svensson L, De Filippo K, Jones K, McDowall A, Hogg N: Integrins in immunity. J Cell Sci 2009, 122:215-225.
70. Katakai T, Habiro K, Kinashi T: Dendritic cells regulate high-speed interstitial T cell migration in the lymph node via LFA-1/ICAM-1. J Immunol 2013, 191:1188-1199.
71. Klug M, Schmidhofer S, Gebhard C, Andreesen R, Rehli M: 5-Hydroxymethylcytosine is an essential intermediate of active DNA demethylation processes in primary human monocytes. Genome Biol 2013, 14:R46.
72. Kallin EM, Rodriguez-Ubreva J, Christensen J, Cimmino L, Aifantis I, Helin K, Ballestar E, Graf T: Tet2 facilitates the derepression of myeloid target genes during CEBPalpha-induced transdifferentiation of pre-B cells. Mol Cell 2012, 48:266-276.
73. Kaneda M, Okano M, Hata K, Sado T, Tsujimoto N, Li E, Sasaki H: Essential role for de novo DNA methyltransferase Dnmt3a in paternal and maternal imprinting. Nature 2004, 429:900-903.
74. Trowbridge JJ, Orkin SH: Dnmt3a silences hematopoietic stem cell self-renewal. Nat Genet 2012, 44:13-14.
75. Challen GA, Sun D, Jeong M, Luo M, Jelinek J, Berg JS, Bock C, Vasanthakumar A, Gu H, Xi Y, Liang S, Lu Y, Darlington GJ, Meissner A, Issa JP, Godley LA, Li W, Goodell MA: Dnmt3a is essential for hematopoietic stem cell differentiation. Nat Genet 2012, 44:23-31.
76. Rhee I, Bachman KE, Park BH, Jair KW, Yen RW, Schuebel KE, Cui H, Feinberg AP, Lengauer C, Kinzler KW, Baylin SB, Vogelstein B: DNMT1 and DNMT3b cooperate to silence genes in human cancer cells. Nature 2002, 416:552-556.
77. Metivier R, Gallais R, Tiffoche C, Le Peron C, Jurkowska RZ, Carmouche RP, Ibberson D, Barath P, Demay F, Reid G, Benes V, Jeltsch A, Gannon F, Salbert G: Cyclical DNA methylation of a transcriptionally active promoter. Nature 2008, 452:45-50.
78. Chen CC, Wang KY, Shen CK: The mammalian de novo DNA methyltransferases DNMT3A and DNMT3B are also DNA 5-hydroxymethylcytosine dehydroxymethylases. J Biol Chem2012, 287:33116-33121.
79. Chen CC, Wang KY, Shen CK: DNA 5-methylcytosine demethylation activities of the mammalian DNA methyltransferases. J Biol Chem 2013, 288:9084-9091.
80. Frikeche J, Clavert A, Delaunay J, Brissot E, Gregoire M, Gaugler B, Mohty M: Impact of the hypomethylating agent 5-azacytidine on dendritic cells function. Exp Hematol 2011, 39:1056-1063.
81. Di Ruscio A, Ebralidze AK, Benoukraf T, Amabile G, Goff LA, Terragni J, Figueroa ME, De Figueiredo Pontes LL, Alberich-Jorda M, Zhang P, Wu M, D'Alò F, Melnick A, Leone G, Ebralidze KK, Pradhan S, Rinn JL, Tenen DG: DNMT1-interacting RNAs block gene-specific DNA methylation. Nature 2013, 503:371-376.
82. Thurner B, Roder C, Dieckmann D, Heuer M, Kruse M, Glaser A, Keikavoussi P, Kampgen E, Bender A, Schuler G: Generation of large numbers of fully mature and stable dendritic cells from leukapheresis products for clinical application. J Immunol Methods 1999, 223:1-15.
83. Bender A, Sapp M, Schuler G, Steinman RM, Bhardwaj N: Improved methods for the generation of dendritic cells from nonproliferating progenitors in human blood. J Immunol Methods 1996, 196:121-135.
84. Dauer M, Schad K, Herten J, Junkmann J, Bauer C, Kiefl R, Endres S, Eigler A: FastDC derived from human monocytes within 48 h effectively prime tumor antigen-specific cytotoxic T cells. J Immunol Methods 2005, 302:145-155.
85. Salcedo M, Bercovici N, Taylor R, Vereecken P, Massicard S, Duriau D, Vernel-Pauillac F, Boyer A, Baron-Bodo V, Mallard E, Bartholeyns J, Goxe B, Latour N, Leroy S, Prigent D, Martiat P, Sales F, Laporte M, Bruyns C, Romet-Lemonne JL, Abastado JP, Lehmann F, Velu T: Vaccination of melanoma patients using dendritic cells loaded with an allogeneic tumor cell lysate. Cancer Immunol Immunother 2006, 55:819-829.
86. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP: Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 2003, 4:249-264.
87. Welch BL: On the comparison of several mean values: an alternative approach. Biometrika 1951, 38:330-336.
88. Smyth GK: Limma: Linear Models for Microarray Data. In Bioinformatics and Computational Biology Solutions using R and Bioconductor. Edited by Gentleman R, Carey V, Dudoit S, Irizarry R, Huber W. New York: Springer; 2005:397-420.
89. Matys V, Kel-Margoulis OV, Fricke E, Liebich I, Land S, Barre-Dirrie A, Reuter I, Chekmenev D, Krull M, Hornischer K, Voss N, Stegmaier P, Lewicki-Potapov B, Saxel H, Kel AE, Wingender E: TRANSFAC and its module TRANSCompel: transcriptional gene regulation in eukaryotes. Nucleic Acids Res 2006, 34:D108-D110.
90. Mathelier A, Zhao X, Zhang AW, Parcy F, Worsley-Hunt R, Arenillas DJ, Buchman S, Chen CY, Chou A, Ienasescu H, Lim J, Shyr C, Tan G, Zhou M, Lenhard B, Sandelin A, Wasserman WW: JASPAR 2014: an extensively expanded and updated open-access database of transcription factor binding profiles. Nucleic Acids Res 2014, 42:D142-D147.
91. Robasky K, Bulyk ML: UniPROBE, update 2011: expanded content and search tools in the online database of protein-binding microarray data on protein-DNA interactions. Nucleic Acids Res 2011, 39:D124-D128.
92. Wang J, Zhuang J, Iyer S, Lin XY, Greven MC, Kim BH, Moore J, Pierce BG, Dong X, Virgil D, Birney E, Hung JH, Weng Z: Factorbook.org: a Wiki-based database for transcription factor-binding data generated by the ENCODE consortium. Nucleic Acids Res 2013, 41:D171-D176.
93. Jolma A, Yan J, Whitington T, Toivonen J, Nitta KR, Rastas P, Morgunova E, Enge M, Taipale M, Wei G, Palin K, Vaquerizas JM, Vincentelli R, Luscombe NM, Hughes TR, Lemaire P, Ukkonen E, Kivioja T, Taipale J: DNA-binding specificities of human transcription factors. Cell 2013, 152:327-339.
94. Weirauch MT, Cote A, Norel R, Annala M, Zhao Y, Riley TR, Saez-Rodriguez J, Cokelaer T, Vedenko A, Talukder S, DREAM5 Consortium, Bussemaker HJ, Morris QD, Bulyk ML, Stolovitzky G, Hughes TR: Evaluation of methods for modeling transcription factor sequence specificity. Nat Biotechnol 2013, 31:126-134.
95. Zambelli F, Pesole G, Pavesi G: Pscan: finding over-represented transcription factor binding site motifs in sequences from co-regulated or co-expressed genes. Nucleic Acids Res 2009, 37:W247-W252.
96. Heinz S, Benner C, Spann N, Bertolino E, Lin YC, Laslo P, Cheng JX, Murre C, Singh H, Glass CK: Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol Cell 2010, 38:576-589.