Stacking the DEK: From chromatin topology to cancer stem cells

Cell Cycle

Volumn 12, Issue 1, 2013, Pages 51-66

  Privette Vinnedge, Lisa M ^a   Kappes, Ferdinand ^b   Nassar, Nicolas ^a   Wells, Susanne I ^a  

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

^b RWTH AACHEN UNIVERSITY   (Germany)

Author keywords

Cancer stem cells; Chromatin organization; DEK; Heterochromatin; Stem cells

Indexed keywords

ANTINEOPLASTIC AGENT; CELL MARKER; CISPLATIN; DOXORUBICIN; GAMMA SECRETASE INHIBITOR; MRK 003; NONHISTONE PROTEIN; NONHISTONE PROTEIN DEK; PROTEIN P53; RETINOIC ACID; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; CANCER CHEMOTHERAPY; CANCER RESISTANCE; CANCER STEM CELL; CELL POPULATION; CELL PROLIFERATION; CELL TRANSFORMATION; CHROMATIN; CHROMATIN STRUCTURE; EMBRYONIC STEM CELL; EPIGENETICS; GENE FUNCTION; HUMAN; MOLECULARLY TARGETED THERAPY; NONHUMAN; ONCOGENE; PROTEIN DEPLETION; PROTEIN LOCALIZATION; REGULATORY MECHANISM; REVIEW; STEM CELL;

EID: 84872318453     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.23121     Document Type: Review

References (160)

1. Grompe M. Tissue stem cells: new tools and functional diversity. Cell Stem Cell 2012; 10:685-9; PMID:22704508; http://dx.doi.org/10.1016/j.stem.2012. 04.006.
2. Seaberg RM, van der Kooy D. Stem and progenitor cells: the premature desertion of rigorous definitions. Trends Neurosci 2003; 26:125-31; PMID:12591214; http://dx.doi.org/10.1016/S0166-2236(03)00031-6.
3. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007; 131:861-72; PMID:18035408; http://dx.doi.org/10.1016/j.cell. 2007.11.019.
4. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006; 126:663-76; PMID:16904174; http://dx.doi.org/10.1016/j.cell.2006.07.024.
5. Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, Tian S, et al. Induced pluripotent stem cell lines derived from human somatic cells. Science 2007; 318:1917-20; PMID:18029452; http://dx.doi.org/10.1126/science. 1151526.
6. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A 2003; 100:3983-8; PMID:12629218; http://dx.doi.org/10.1073/pnas. 0530291100.
7. Bonnet D, Dick JE. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med 1997; 3:730-7; PMID:9212098; http://dx.doi.org/10.1038/nm0797-730.
8. Dreesen O, Brivanlou AH. Signaling pathways in cancer and embryonic stem cells. Stem Cell Rev 2007; 3:7-17; PMID:17873377; http://dx.doi.org/10.1007/ s12015-007-0004-8.
9. Okita K, Yamanaka S. Intracellular signaling pathways regulating pluripotency of embryonic stem cells. Curr Stem Cell Res Ther 2006; 1:103-11; PMID:18220859; http://dx.doi.org/10.2174/157488806775269061.
10. Sanges D, Cosma MP. Reprogramming cell fate to pluripotency: the decision-making signalling pathways. Int J Dev Biol 2010; 54:1575-87; PMID:21305473; http://dx.doi.org/10.1387/ijdb.103190ds.
11. Natarajan TG, FitzGerald KT. Markers in normal and cancer stem cells. Cancer Biomark 2007; 3:211-31; PMID:17917151.
12. Dontu G, Abdallah WM, Foley JM, Jackson KW, Clarke MF, Kawamura MJ, et al. In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes Dev 2003; 17:1253-70; PMID:12756227; http://dx.doi.org/10.1101/gad.1061803.
13. Osawa M, Hanada K, Hamada H, Nakauchi H. Long-term lymphohematopoietic reconstitution by a single CD34-low/negative hematopoietic stem cell. Science 1996; 273:242-5; PMID:8662508; http://dx.doi.org/10.1126/science.273.5272.242.
14. Woodward WA, Chen MS, Behbod F, Rosen JM. On mammary stem cells. J Cell Sci 2005; 118:3585-94; PMID:16105882; http://dx.doi.org/10.1242/jcs.02532.
15. Liu S, Dontu G, Wicha MS. Mammary stem cells, self-renewal pathways, and carcinogenesis. Breast Cancer Res 2005; 7:86-95; PMID:15987436; http://dx.doi.org/10.1186/bcr1021.
16. van der Flier LG, Clevers H. Stem cells, self-renewal, and differentiation in the intestinal epithelium. Annu Rev Physiol 2009; 71:241-60; PMID:18808327; http://dx.doi.org/10.1146/annurev.physiol.010908.163145.
17. Phinney DG, Prockop DJ. Concise review: mesenchymal stem/multipotent stromal cells: the state of transdifferentiation and modes of tissue repair - current views. Stem Cells 2007; 25:2896-902; PMID:17901396; http://dx.doi.org/ 10.1634/stemcells.2007-0637.
18. McKay R. Stem cells in the central nervous system. Science 1997; 276:66-71; PMID:9082987; http://dx.doi.org/10.1126/science.276.5309.66.
19. Braun KM, Prowse DM. Distinct epidermal stem cell compartments are maintained by independent niche microenvironments. Stem Cell Rev 2006; 2:221-31; PMID:17625258; http://dx.doi.org/10.1007/s12015-006-0050-7.
20. Cabarcas SM, Mathews LA, Farrar WL. The cancer stem cell niche - there goes the neighborhood? Int J Cancer 2011; 129:2315-27; PMID:21792897; http://dx.doi.org/10.1002/ijc.26312.
21. Jones DL, Wagers AJ. No place like home: anatomy and function of the stem cell niche. Nat Rev Mol Cell Biol 2008; 9:11-21; PMID:18097443; http://dx.doi.org/10.1038/nrm2319.
22. Takeda N, Jain R, LeBoeuf MR, Wang Q, Lu MM, Epstein JA. Interconversion between intestinal stem cell populations in distinct niches. Science 2011; 334:1420-4; PMID:22075725; http://dx.doi.org/10.1126/science.1213214.
23. Eckert RL, Adhikary G, Balasubramanian S, Rorke EA, Vemuri MC, Boucher SE, et al. Biochemistry of epidermal stem cells. Biochim Biophys Acta 2012; In press; PMID:22820019; http://dx.doi.org/10.1016/j.bbagen.2012.07.002.
24. Chen J, Li Y, Yu TS, McKay RM, Burns DK, Kernie SG, et al. A restricted cell population propagates glioblastoma growth after chemotherapy. Nature 2012; 488:522-6; PMID:22854781; http://dx.doi.org/10.1038/nature11287.
25. Driessens G, Beck B, Caauwe A, Simons BD, Blanpain C. Defining the mode of tumour growth by clonal analysis. Nature 2012; 488:527-30; PMID:22854777; http://dx.doi.org/10.1038/nature11344.
26. Schepers AG, Snippert HJ, Stange DE, van den Born M, van Es JH, van de Wetering M, et al. Lineage tracing reveals Lgr5+ stem cell activity in mouse intestinal adenomas. Science 2012; 337:730-5; PMID:22855427; http://dx.doi.org/10.1126/science.1224676.
27. Chen L, Kasai T, Li Y, Sugii Y, Jin G, Okada M, et al. A model of cancer stem cells derived from mouse induced pluripotent stem cells. PLoS One 2012; 7:e33544; PMID:22511923; http://dx.doi.org/10.1371/journal.pone.0033544.
28. Al-Hajj M, Clarke MF. Self-renewal and solid tumor stem cells. Oncogene 2004; 23:7274-82; PMID:15378087; http://dx.doi.org/10.1038/sj.onc.1207947.
29. Visvader JE, Lindeman GJ. Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat Rev Cancer 2008; 8:755-68; PMID:18784658; http://dx.doi.org/10.1038/nrc2499.
30. Ben-Porath I, Thomson MW, Carey VJ, Ge R, Bell GW, Regev A, et al. An embryonic stem cell-like gene expression signature in poorly differentiated aggressive human tumors. Nat Genet 2008; 40:499-507; PMID:18443585; http://dx.doi.org/10.1038/ng.127.
31. Dontu G, Liu S, Wicha MS. Stem cells in mammary development and carcinogenesis: implications for prevention and treatment. Stem Cell Rev 2005; 1:207-13; PMID:17142857; http://dx.doi.org/10.1385/SCR:1:3:207.
32. Phillips TM, McBride WH, Pajonk F. The response of CD24(-/low)/CD44+ breast cancer-initiating cells to radiation. J Natl Cancer Inst 2006; 98:1777-85; PMID:17179479; http://dx.doi.org/10.1093/jnci/djj495.
33. Sengupta A, Cancelas JA. Cancer stem cells: a stride towards cancer cure? J Cell Physiol 2010; 225:7-14; PMID:20458736; http://dx.doi.org/10.1002/jcp. 22213.
34. Schatton T, Frank NY, Frank MH. Identification and targeting of cancer stem cells. Bioessays 2009; 31:1038-49; PMID:19708024; http://dx.doi.org/10. 1002/bies.200900058.
35. Klonisch T, Wiechec E, Hombach-Klonisch S, Ande SR, Wesselborg S, Schulze-Osthoff K, et al. Cancer stem cell markers in common cancers - therapeutic implications. Trends Mol Med 2008; 14:450-60; PMID:18775674; http://dx.doi.org/10.1016/j.molmed.2008.08.003.
36. Alvi AJ, Clayton H, Joshi C, Enver T, Ashworth A, Vivanco MM, et al. Functional and molecular characterisation of mammary side population cells. Breast Cancer Res 2003; 5:R1-8; PMID:12559051; http://dx.doi.org/10.1186/bcr563.
37. Asakura A, Rudnicki MA. Side population cells from diverse adult tissues are capable of in vitro hematopoietic differentiation. Exp Hematol 2002; 30:1339-45; PMID:12423688; http://dx.doi.org/10.1016/S0301-472X(02)00954-2.
38. Hirschmann-Jax C, Foster AE, Wulf GG, Nuchtern JG, Jax TW, Gobel U, et al. A distinct "side population"of cells with high drug efflux capacity in human tumor cells. Proc Natl Acad Sci U S A 2004; 101:14228-33; PMID:15381773; http://dx.doi.org/10.1073/pnas.0400067101.
39. Goodell MA, Brose K, Paradis G, Conner AS, Mulligan RC. Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J Exp Med 1996; 183:1797-806; PMID:8666936; http://dx.doi.org/10.1084/ jem.183.4.1797.
40. Storms RW, Trujillo AP, Springer JB, Shah L, Colvin OM, Ludeman SM, et al. Isolation of primitive human hematopoietic progenitors on the basis of aldehyde dehydrogenase activity. Proc Natl Acad Sci U S A 1999; 96:9118-23; PMID:10430905; http://dx.doi.org/10.1073/pnas.96.16.9118.
41. Lin KK, Goodell MA. Detection of hematopoietic stem cells by flow cytometry. Methods Cell Biol 2011; 103:21-30; PMID:21722798; http://dx.doi.org/10.1016/B978-0-12-385493-3.00002-4.
42. Potten CS, Owen G, Booth D. Intestinal stem cells protect their genome by selective segregation of template DNA strands. J Cell Sci 2002; 115:2381-8; PMID:12006622.
43. Smith GH. Label-retaining epithelial cells in mouse mammary gland divide asymmetrically and retain their template DNA strands. Development 2005; 132:681-7; PMID:15647322; http://dx.doi.org/10.1242/dev.01609.
44. Sharma HW, Sokoloski JA, Perez JR, Maltese JY, Sartorelli AC, Stein CA, et al. Differentiation of immortal cells inhibits telomerase activity. Proc Natl Acad Sci U S A 1995; 92:12343-6; PMID:8618897; http://dx.doi.org/10.1073/pnas. 92.26.12343.
45. Morrison SJ, Prowse KR, Ho P, Weissman IL. Telomerase activity in hematopoietic cells is associated with self-renewal potential. Immunity 1996; 5:207-16; PMID:8808676; http://dx.doi.org/10.1016/S1074-7613(00)80316-7.
46. Reynolds BA, Weiss S. Clonal and population analyses demonstrate that an EGF-responsive mammalian embryonic CNS precursor is a stem cell. Dev Biol 1996; 175:1-13; PMID:8608856; http://dx.doi.org/10.1006/dbio.1996.0090.
47. O'Connor MD, Kardel MD, Eaves CJ. Functional assays for human embryonic stem cell pluripotency. Methods Mol Biol 2011; 690:67-80; PMID:21042985; http://dx.doi.org/10.1007/978-1-60761-962-8-4.
48. Perry JM, Li L. Functional assays for hematopoietic stem cell self-renewal. Methods Mol Biol 2010; 636:45-54; PMID:20336515; http://dx.doi.org/10.1007/978-1-60761-691-7-3.
49. Clarke MF, Dick JE, Dirks PB, Eaves CJ, Jamieson CH, Jones DL, et al. Cancer stem cells - perspectives on current status and future directions: AACR Workshop on cancer stem cells. Cancer Res 2006; 66:9339-44; PMID:16990346; http://dx.doi.org/10.1158/0008-5472.CAN-06-3126.
50. Santisteban M, Reiman JM, Asiedu MK, Behrens MD, Nassar A, Kalli KR, et al. Immune-induced epithelial to mesenchymal transition in vivo generates breast cancer stem cells. Cancer Res 2009; 69:2887-95; PMID:19276366; http://dx.doi.org/10.1158/0008-5472.CAN-08-3343.
51. Lowry WE, Richter L. Signaling in adult stem cells. Front Biosci 2007; 12:3911-27; PMID:17485347; http://dx.doi.org/10.2741/2360.
52. Wang MM. Notch signaling and Notch signaling modifiers. Int J Biochem Cell Biol 2011; 43:1550-62; PMID:21854867; http://dx.doi.org/10.1016/j.biocel. 2011.08.005.
53. Liu J, Sato C, Cerletti M, Wagers A. Notch signaling in the regulation of stem cell self-renewal and differentiation. Curr Top Dev Biol 2010; 92:367-409; PMID:20816402; http://dx.doi.org/10.1016/S0070-2153(10)92012-7.
54. Ninov N, Borius M, Stainier DY. Different levels of Notch signaling regulate quiescence, renewal and differentiation in pancreatic endocrine progenitors. Development 2012; 139:1557-67; PMID:22492351; http://dx.doi.org/10. 1242/dev.076000.
55. Kondratyev M, Kreso A, Hallett RM, Girgis-Gabardo A, Barcelon ME, Ilieva D, et al. Gamma-secretase inhibitors target tumor-initiating cells in a mouse model of ERBB2 breast cancer. Oncogene 2012; 31:93-103; PMID:21666715; http://dx.doi.org/10.1038/onc.2011.212.
56. Ying M, Wang S, Sang Y, Sun P, Lal B, Goodwin CR, et al. Regulation of glioblastoma stem cells by retinoic acid: role for Notch pathway inhibition. Oncogene 2011; 30:3454-67; PMID:21383690; http://dx.doi.org/10.1038/onc.2011.58.
57. Tatarek J, Cullion K, Ashworth T, Gerstein R, Aster JC, Kelliher MA. Notch1 inhibition targets the leukemia-initiating cells in a Tal1/Lmo2 mouse model of T-ALL. Blood 2011; 118:1579-90; PMID:21670468; http://dx.doi.org/10. 1182/blood-2010-08-300343.
58. Yang C, Atkinson SP, Vilella F, Lloret M, Armstrong L, Mann DA, et al. Opposing putative roles for canonical and noncanonical NFêB signaling on the survival, proliferation, and differentiation potential of human embryonic stem cells. Stem Cells 2010; 28:1970-80; PMID:20882529; http://dx.doi.org/10. 1002/stem.528.
59. Armstrong L, Hughes O, Yung S, Hyslop L, Stewart R, Wappler I, et al. The role of PI3K/AKT, MAPK/ERK and NFkappabeta signalling in the maintenance of human embryonic stem cell pluripotency and viability highlighted by transcriptional profiling and functional analysis. Hum Mol Genet 2006; 15:1894-913; PMID:16644866; http://dx.doi.org/10.1093/hmg/ddl112.
60. Zhang Y, Liu J, Yao S, Li F, Xin L, Lai M, et al. Nuclear factor kappa B signaling initiates early differentiation of neural stem cells. Stem Cells 2012; 30:510-24; PMID:22134901; http://dx.doi.org/10.1002/stem.1006.
61. Scheel C, Eaton EN, Li SH, Chaffer CL, Reinhardt F, Kah KJ, et al. Paracrine and autocrine signals induce and maintain mesenchymal and stem cell states in the breast. Cell 2011; 145:926-40; PMID:21663795; http://dx.doi.org/ 10.1016/j.cell.2011.04.029.
62. Zeng YA, Nusse R. Wnt proteins are self-renewal factors for mammary stem cells and promote their long-term expansion in culture. Cell Stem Cell 2010; 6:568-77; PMID:20569694; http://dx.doi.org/10.1016/j.stem.2010.03.020.
63. Sato N, Meijer L, Skaltsounis L, Greengard P, Brivanlou AH. Maintenance of pluripotency in human and mouse embryonic stem cells through activation of Wnt signaling by a pharmacological GSK-3-specific inhibitor. Nat Med 2004; 10:55-63; PMID:14702635; http://dx.doi.org/10.1038/nm979.
64. Lluis F, Pedone E, Pepe S, Cosma MP. Periodic activation of Wnt/beta-catenin signaling enhances somatic cell reprogramming mediated by cell fusion. Cell Stem Cell 2008; 3:493-507; PMID:18983965; http://dx.doi.org/10. 1016/j.stem.2008.08.017.
65. Yang A, McKeon F. P63 and P73: P53 mimics, menaces and more. Nat Rev Mol Cell Biol 2000; 1:199-207; PMID:11252895; http://dx.doi.org/10.1038/35043127.
66. Deyoung MP, Ellisen LW. p63 and p73 in human cancer: defining the network. Oncogene 2007; 26:5169-83; PMID:17334395; http://dx.doi.org/10.1038/sj. onc.1210337.
67. Talos F, Abraham A, Vaseva AV, Holembowski L, Tsirka SE, Scheel A, et al. p73 is an essential regulator of neural stem cell maintenance in embryonal and adult CNS neurogenesis. Cell Death Differ 2010; 17:1816-29; PMID:21076477; http://dx.doi.org/10.1038/cdd.2010.131.
68. Gonzalez-Cano L, Herreros-Villanueva M, Fernandez-Alonso R, Ayuso-Sacido A, Meyer G, Garcia-Verdugo JM, et al. p73 deficiency results in impaired self renewal and premature neuronal differentiation of mouse neural progenitors independently of p53. Cell Death Dis 2010; 1:e109; PMID:21368881; http://dx.doi.org/10.1038/cddis.2010.87.
69. Agostini M, Tucci P, Chen H, Knight RA, Bano D, Nicotera P, et al. p73 regulates maintenance of neural stem cell. Biochem Biophys Res Commun 2010; 403:13-7; PMID:20977890; http://dx.doi.org/10.1016/j.bbrc.2010.10.087.
70. Mills AA, Zheng B, Wang XJ, Vogel H, Roop DR, Bradley A. p63 is a p53 homologue required for limb and epidermal morphogenesis. Nature 1999; 398:708-13; PMID:10227293; http://dx.doi.org/10.1038/19531.
71. Yang A, Schweitzer R, Sun D, Kaghad M, Walker N, Bronson RT, et al. p63 is essential for regenerative proliferation in limb, craniofacial and epithelial development. Nature 1999; 398:714-8; PMID:10227294; http://dx.doi.org/10.1038/ 19539.
72. Nekulova M, Holcakova J, Coates P, Vojtesek B. The role of p63 in cancer, stem cells and cancer stem cells. Cell Mol Biol Lett 2011; 16:296-327; PMID:21442444; http://dx.doi.org/10.2478/s11658-011-0009-9.
73. Dotto GP. Crosstalk of Notch with p53 and p63 in cancer growth control. Nat Rev Cancer 2009; 9:587-95; PMID:19609265; http://dx.doi.org/10.1038/nrc2675.
74. Boldrup L, Coates PJ, Gu X, Nylander K. DeltaNp63 isoforms regulate CD44 and keratins 4, 6, 14 and 19 in squamous cell carcinoma of head and neck. J Pathol 2007; 213:384-91; PMID:17935121; http://dx.doi.org/10.1002/path.2237.
75. Du Z, Li J, Wang L, Bian C, Wang Q, Liao L, et al. Overexpression of ΔNp63α induces a stem cell phenotype in MCF7 breast carcinoma cell line through the Notch pathway. Cancer Sci 2010; 101:2417-24; PMID:20950370; http://dx.doi.org/10.1111/j.1349-7006.2010.01700.x.
76. Tichy ED. Mechanisms maintaining genomic integrity in embryonic stem cells and induced pluripotent stem cells. Exp Biol Med (Maywood) 2011; 236:987-96; PMID:21768163; http://dx.doi.org/10.1258/ebm.2011.011107.
77. Tichy ED, Pillai R, Deng L, Liang L, Tischfield J, Schwemberger SJ, et al. Mouse embryonic stem cells, but not somatic cells, predominantly use homologous recombination to repair double-strand DNA breaks. Stem Cells Dev 2010; 19:1699-711; PMID:20446816; http://dx.doi.org/10.1089/scd.2010.0058.
78. Marión RM, Strati K, Li H, Murga M, Blanco R, Ortega S, et al. A p53-mediated DNA damage response limits reprogramming to ensure iPS cell genomic integrity. Nature 2009; 460:1149-53; PMID:19668189; http://dx.doi.org/10.1038/ nature08287.
79. Kawamura T, Suzuki J, Wang YV, Menendez S, Morera LB, Raya A, et al. Linking the p53 tumour suppressor pathway to somatic cell reprogramming. Nature 2009; 460:1140-4; PMID:19668186; http://dx.doi.org/10.1038/nature08311.
80. Menendez S, Camus S, Izpisua Belmonte JC. p53: guardian of reprogramming. Cell Cycle 2010; 9:3887-91; PMID:20948296; http://dx.doi.org/10.4161/cc.9.19. 13301.
81. Jain AK, Allton K, Iacovino M, Mahen E, Milczarek RJ, Zwaka TP, et al. p53 regulates cell cycle and microRNAs to promote differentiation of human embryonic stem cells. PLoS Biol 2012; 10:e1001268; PMID:22389628; http://dx.doi.org/10.1371/journal.pbio.1001268.
82. Lee KH, Li M, Michalowski AM, Zhang X, Liao H, Chen L, et al. A genomewide study identifies the Wnt signaling pathway as a major target of p53 in murine embryonic stem cells. Proc Natl Acad Sci U S A 2010; 107:69-74; PMID:20018659; http://dx.doi.org/10.1073/pnas.0909734107.
83. Cicalese A, Bonizzi G, Pasi CE, Faretta M, Ronzoni S, Giulini B, et al. The tumor suppressor p53 regulates polarity of self-renewing divisions in mammary stem cells. Cell 2009; 138:1083-95; PMID:19766563; http://dx.doi.org/10. 1016/j.cell.2009.06.048.
84. Kouzarides T. Chromatin modifications and their function. Cell 2007; 128:693-705; PMID:17320507; http://dx.doi.org/10.1016/j.cell.2007.02.005.
85. Chi P, Allis CD, Wang GG. Covalent histone modi-fications - miswritten, misinterpreted and mis-erased in human cancers. Nat Rev Cancer 2010; 10:457-69; PMID:20574448; http://dx.doi.org/10.1038/nrc2876.
86. Robertson KD. DNA methylation and human disease. Nat Rev Genet 2005; 6:597-610; PMID:16136652; http://dx.doi.org/10.1038/nrg1655.
87. Filion GJ, van Bemmel JG, Braunschweig U, Talhout W, Kind J, Ward LD, et al. Systematic protein location mapping reveals five principal chromatin types in Drosophila cells. Cell 2010; 143:212-24; PMID:20888037; http://dx.doi.org/10. 1016/j.cell.2010.09.009.
88. Gaspar-Maia A, Alajem A, Meshorer E, Ramalho-Santos M. Open chromatin in pluripotency and reprogramming. Nat Rev Mol Cell Biol 2011; 12:36-47; PMID:21179060; http://dx.doi.org/10.1038/nrm3036.
89. Lister R, Pelizzola M, Dowen RH, Hawkins RD, Hon G, Tonti-Filippini J, et al. Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 2009; 462:315-22; PMID:19829295; http://dx.doi.org/10.1038/ nature08514.
90. Zlatanova J, Seebart C, Tomschik M. The linker-protein network: control of nucleosomal DNA accessibility. Trends Biochem Sci 2008; 33:247-53; PMID:18468442; http://dx.doi.org/10.1016/j.tibs.2008.04.001.
91. Bártová E, Krejcí J, Harnicarová A, Kozubek S. Differentiation of human embryonic stem cells induces condensation of chromosome territories and formation of heterochromatin protein 1 foci. Differentiation 2008; 76:24-32; PMID:17573914.
92. Waldmann T, Scholten I, Kappes F, Hu HG, Knippers R. The DEK protein - an abundant and ubiquitous constituent of mammalian chromatin. Gene 2004; 343:1-9; PMID:15563827; http://dx.doi.org/10.1016/j.gene.2004.08.029.
93. Aravind L, Koonin EV. SAP - a putative DNA-binding motif involved in chromosomal organization. Trends Biochem Sci 2000; 25:112-4; PMID:10694879; http://dx.doi.org/10.1016/S0968-0004(99)01537-6.
94. Kipp M, Göhring F, Ostendorp T, van Drunen CM, van Driel R, Przybylski M, et al. SAF-Box, a conserved protein domain that specifically recognizes scaffold attachment region DNA. Mol Cell Biol 2000; 20:7480-9; PMID:11003645; http://dx.doi.org/10.1128/MCB.20.20.7480-7489.2000.
95. Waldmann T, Baack M, Richter N, Gruss C. Structure-specific binding of the proto-oncogene protein DEK to DNA. Nucleic Acids Res 2003; 31:7003-10; PMID:14627833; http://dx.doi.org/10.1093/nar/gkg864.
96. Böhm F, Kappes F, Scholten I, Richter N, Matsuo H, Knippers R, et al. The SAF-box domain of chromatin protein DEK. Nucleic Acids Res 2005; 33:1101-10; PMID:15722484; http://dx.doi.org/10.1093/nar/gki258.
97. Waldmann T, Eckerich C, Baack M, Gruss C. The ubiquitous chromatin protein DEK alters the structure of DNA by introducing positive supercoils. J Biol Chem 2002; 277:24988-94; PMID:11997399; http://dx.doi.org/10.1074/jbc. M204045200.
98. Devany M, Kotharu NP, Matsuo H. Expression and isotopic labeling of structural domains of the human protein DEK. Protein Expr Purif 2005; 40:244-7; PMID:15766865; http://dx.doi.org/10.1016/j.pep.2004.07.008.
99. Devany M, Kappes F, Chen KM, Markovitz DM, Matsuo H. Solution NMR structure of the N-terminal domain of the human DEK protein. Protein Sci 2008; 17:205-15; PMID:18227428; http://dx.doi.org/10.1110/ps.073244108.
100. Devany M, Matsuo H. NMR resonance assignments for the DNA-supercoiling domain of the human protein DEK. J Biomol NMR 2005; 31:65; PMID:15692740; http://dx.doi.org/10.1007/s10858-004-6889-5.
101. Holm L, Park J. DaliLite workbench for protein structure comparison. Bioinformatics 2000; 16:566-7; PMID:10980157; http://dx.doi.org/10.1093/ bioinformatics/16.6.566.
102. Okubo S, Hara F, Tsuchida Y, Shimotakahara S, Suzuki S, Hatanaka H, et al. NMR structure of the N-terminal domain of SUMO ligase PIAS1 and its interaction with tumor suppressor p53 and A/T-rich DNA oligomers. J Biol Chem 2004; 279:31455-61; PMID:15133049; http://dx.doi.org/10.1074/jbc.M403561200.
103. Gajiwala KS, Burley SK. Winged helix proteins. Curr Opin Struct Biol 2000; 10:110-6; PMID:10679470; http://dx.doi.org/10.1016/S0959-440X(99)00057-3.
104. Devany M, Kotharu NP, Matsuo H. Solution NMR structure of the C-terminal domain of the human protein DEK. Protein Sci 2004; 13:2252-9; PMID:15238633; http://dx.doi.org/10.1110/ps.04797104.
105. Meyn MS, Lu-Kuo JM, Herzing LB. Expression cloning of multiple human cDNAs that complement the phenotypic defects of ataxia-telangiectasia group D fibroblasts. Am J Hum Genet 1993; 53:1206-16; PMID:7504406.
106. Kappes F, Damoc C, Knippers R, Przybylski M, Pinna LA, Gruss C. Phosphorylation by protein kinase CK2 changes the DNA binding properties of the human chromatin protein DEK. Mol Cell Biol 2004; 24:6011-20; PMID:15199154; http://dx.doi.org/10.1128/MCB.24.13.6011-6020.2004.
107. Kappes F, Scholten I, Richter N, Gruss C, Waldmann T. Functional domains of the ubiquitous chromatin protein DEK. Mol Cell Biol 2004; 24:6000-10; PMID:15199153; http://dx.doi.org/10.1128/MCB.24.13.6000-6010.2004.
108. Mor-Vaknin N, Kappes F, Dick AE, Legendre M, Damoc C, Teitz-Tennenbaum S, et al. DEK in the synovium of patients with juvenile idiopathic arthritis: characterization of DEK antibodies and posttranslational modification of the DEK autoantigen. Arthritis Rheum 2011; 63:556-67; PMID:21280010; http://dx.doi.org/10.1002/art.30138.
109. Fahrer J, Popp O, Malanga M, Beneke S, Markovitz DM, Ferrando-May E, et al. High-affinity interaction of poly(ADP-ribose) and the human DEK oncoprotein depends upon chain length. Biochemistry 2010; 49:7119-30; PMID:20669926; http://dx.doi.org/10.1021/bi1004365.
110. Gamble MJ, Fisher RP. SET and PARP1 remove DEK from chromatin to permit access by the transcription machinery. Nat Struct Mol Biol 2007; 14:548-55; PMID:17529993; http://dx.doi.org/10.1038/nsmb1248.
111. Kappes F, Fahrer J, Khodadoust MS, Tabbert A, Strasser C, Mor-Vaknin N, et al. DEK is a poly(ADP-ribose) acceptor in apoptosis and mediates resistance to genotoxic stress. Mol Cell Biol 2008; 28:3245-57; PMID:18332104; http://dx.doi.org/10.1128/MCB.01921-07.
112. Tabbert A, Kappes F, Knippers R, Kellermann J, Lottspeich F, Ferrando-May E. Hypophosphorylation of the architectural chromatin protein DEK in death-receptor-induced apoptosis revealed by the isotope coded protein label proteomic platform. Proteomics 2006; 6:5758-72; PMID:17001602; http://dx.doi.org/10.1002/pmic.200600197.
113. Cleary J, Sitwala KV, Khodadoust MS, Kwok RP, Mor-Vaknin N, Cebrat M, et al. p300/CBP-associated factor drives DEK into interchromatin granule clusters. J Biol Chem 2005; 280:31760-7; PMID:15987677; http://dx.doi.org/10.1074/jbc. M500884200.
114. Cronican JJ, Beier KT, Davis TN, Tseng JC, Li W, Thompson DB, et al. A class of human proteins that deliver functional proteins into mammalian cells in vitro and in vivo. Chem Biol 2011; 18:833-8; PMID:21802004; http://dx.doi.org/10.1016/j.chembiol.2011.07.003.
115. Mor-Vaknin N, Punturieri A, Sitwala K, Faulkner N, Legendre M, Khodadoust MS, et al. The DEK nuclear autoantigen is a secreted chemotactic factor. Mol Cell Biol 2006; 26:9484-96; PMID:17030615; http://dx.doi.org/10.1128/MCB.01030- 06.
116. Carro MS, Spiga FM, Quarto M, Di Ninni V, Volorio S, Alcalay M, et al. DEK Expression is controlled by E2F and deregulated in diverse tumor types. Cell Cycle 2006; 5:1202-7; PMID:16721057; http://dx.doi.org/10.4161/cc.5.11.2801.
117. Wise-Draper TM, Allen HV, Thobe MN, Jones EE, Habash KB, Münger K, et al. The human DEK protooncogene is a senescence inhibitor and an upregulated target of high-risk human papillomavirus E7. J Virol 2005; 79:14309-17; PMID:16254365; http://dx.doi.org/10.1128/JVI.79.22.14309-14317.2005.
118. Soares LM, Zanier K, Mackereth C, Sattler M, Valcárcel J. Intron removal requires proofreading of U2AF/3′ splice site recognition by DEK. Science 2006; 312:1961-5; PMID:16809543; http://dx.doi.org/10.1126/science. 1128659.
119. Kappes F, Burger K, Baack M, Fackelmayer FO, Gruss C. Subcellular localization of the human proto-oncogene protein DEK. J Biol Chem 2001; 276:26317-23; PMID:11333257; http://dx.doi.org/10.1074/jbc.M100162200.
120. Takata H, Nishijima H, Ogura S, Sakaguchi T, Bubulya PA, Mochizuki T, et al. Proteome analysis of human nuclear insoluble fractions. Genes Cells 2009; 14:975-90; PMID:19695025; http://dx.doi.org/10.1111/j.1365-2443.2009.01324.x.
121. Hu HG, Illges H, Gruss C, Knippers R. Distribution of the chromatin protein DEK distinguishes active and inactive CD21/CR2 gene in pre- and mature B lymphocytes. Int Immunol 2005; 17:789-96; PMID:15908448; http://dx.doi.org/10. 1093/intimm/dxh261.
122. Torrente MP, Zee BM, Young NL, Baliban RC, LeRoy G, Floudas CA, et al. Proteomic interrogation of human chromatin. PLoS One 2011; 6:e24747; PMID:21935452; http://dx.doi.org/10.1371/journal.pone.0024747.
123. Brázda V, Laister RC, Jagelská EB, Arrowsmith C. Cruciform structures are a common DNA feature important for regulating biological processes. BMC Mol Biol 2011; 12:33; PMID:21816114; http://dx.doi.org/10.1186/ 1471-2199-12-33.
124. Datta A, Adelson ME, Mogilevkin Y, Mordechai E, Sidi AA, Trama JP. Oncoprotein DEK as a tissue and urinary biomarker for bladder cancer. BMC Cancer 2011; 11:234; PMID:21663673; http://dx.doi.org/10.1186/1471-2407-11-234.
125. Kappes F, Waldmann T, Mathew V, Yu J, Zhang L, Khodadoust MS, et al. The DEK oncoprotein is a Su(var) that is essential to heterochromatin integrity. Genes Dev 2011; 25:673-8; PMID:21460035; http://dx.doi.org/10.1101/gad.2036411.
126. Sawatsubashi S, Murata T, Lim J, Fujiki R, Ito S, Suzuki E, et al. A histone chaperone, DEK, transcriptionally coactivates a nuclear receptor. Genes Dev 2010; 24:159-70; PMID:20040570; http://dx.doi.org/10.1101/gad.1857410.
127. Fu GK, Grosveld G, Markovitz DM. DEK, an autoantigen involved in a chromosomal translocation in acute myelogenous leukemia, binds to the HIV-2 enhancer. Proc Natl Acad Sci U S A 1997; 94:1811-5; PMID:9050861; http://dx.doi.org/10.1073/pnas.94.5.1811.
128. Alexiadis V, Waldmann T, Andersen J, Mann M, Knippers R, Gruss C. The protein encoded by the proto-oncogene DEK changes the topology of chromatin and reduces the efficiency of DNA replication in a chromatin-specific manner. Genes Dev 2000; 14:1308-12; PMID:10837023.
129. Campillos M, García MA, Valdivieso F, Vázquez J. Transcriptional activation by AP-2alpha is modulated by the oncogene DEK. Nucleic Acids Res 2003; 31:1571-5; PMID:12595566; http://dx.doi.org/10.1093/nar/ gkg247.
130. Kavanaugh GM, Wise-Draper TM, Morreale RJ, Morrison MA, Gole B, Schwemberger S, et al. The human DEK oncogene regulates DNA damage response signaling and repair. Nucleic Acids Res 2011; 39:7465-76; PMID:21653549; http://dx.doi.org/10.1093/nar/gkr454.
131. Le Hir H, Gatfield D, Izaurralde E, Moore MJ. The exon-exon junction complex provides a binding platform for factors involved in mRNA export and nonsense-mediated mRNA decay. EMBO J 2001; 20:4987-97; PMID:11532962; http://dx.doi.org/10.1093/emboj/20.17.4987.
132. McGarvey T, Rosonina E, McCracken S, Li Q, Arnaout R, Mientjes E, et al. The acute myeloid leukemia-associated protein, DEK, forms a splicing-dependent interaction with exon-product complexes. J Cell Biol 2000; 150:309-20; PMID:10908574; http://dx.doi.org/10.1083/jcb.150.2.309.
133. Sammons M, Wan SS, Vogel NL, Mientjes EJ, Grosveld G, Ashburner BP. Negative regulation of the RelA/p65 transactivation function by the product of the DEK proto-oncogene. J Biol Chem 2006; 281:26802-12; PMID:16829531; http://dx.doi.org/10.1074/jbc.M600915200.
134. Khodadoust MS, Verhaegen M, Kappes F, Riveiro-Falkenbach E, Cigudosa JC, Kim DS, et al. Melanoma proliferation and chemoresistance controlled by the DEK oncogene. Cancer Res 2009; 69:6405-13; PMID:19679545; http://dx.doi.org/10.1158/ 0008-5472.CAN-09-1063.
135. Kim DW, Chae JI, Kim JY, Pak JH, Koo DB, Bahk YY, et al. Proteomic analysis of apoptosis related proteins regulated by proto-oncogene protein DEK. J Cell Biochem 2009; 106:1048-59; PMID:19229864; http://dx.doi.org/10.1002/jcb. 22083.
136. Privette Vinnedge LM, McClaine R, Wagh PK, Wikenheiser-Brokamp KA, Waltz SE, Wells SI. The human DEK oncogene stimulates β-catenin signaling, invasion and mammosphere formation in breast cancer. Oncogene 2011; 30:2741-52; PMID:21317931; http://dx.doi.org/10.1038/onc.2011.2.
137. Wise-Draper TM, Allen HV, Jones EE, Habash KB, Matsuo H, Wells SI. Apoptosis inhibition by the human DEK oncoprotein involves interference with p53 functions. Mol Cell Biol 2006; 26:7506-19; PMID:16894028; http://dx.doi.org/10. 1128/MCB.00430-06.
138. Wise-Draper TM, Mintz-Cole RA, Morris TA, Simpson DS, Wikenheiser-Brokamp KA, Currier MA, et al. Overexpression of the cellular DEK protein promotes epithelial transformation in vitro and in vivo. Cancer Res 2009; 69:1792-9; PMID:19223548; http://dx.doi.org/10.1158/0008-5472.CAN-08-2304.
139. Cheung TH, Quach NL, Charville GW, Liu L, Park L, Edalati A, et al. Maintenance of muscle stem-cell quiescence by microRNA-489. Nature 2012; 482:524-8; PMID:22358842; http://dx.doi.org/10.1038/nature10834.
140. Liu K, Feng T, Liu J, Zhong M, Zhang S. Silencing of the DEK gene induces apoptosis and senescence in CaSki cervical carcinoma cells via the up-regulation of NFêB p65. Biosci Rep 2012; 32:323-32; PMID:22390170; http://dx.doi.org/10.1042/BSR20100141.
141. Lee KS, Kim DW, Kim JY, Choo JK, Yu K, Seo SB. Caspase-dependent apoptosis induction by targeted expression of DEK in Drosophila involves histone acetylation inhibition. J Cell Biochem 2008; 103:1283-93; PMID:17685435; http://dx.doi.org/10.1002/jcb.21511.
142. Shibata T, Kokubu A, Miyamoto M, Hosoda F, Gotoh M, Tsuta K, et al. DEK oncoprotein regulates transcriptional modifiers and sustains tumor initiation activity in high-grade neuroendocrine carcinoma of the lung. Oncogene 2010; 29:4671-81; PMID:20543864; http://dx.doi.org/10.1038/onc.2010.217.
143. Kim DW, Kim JY, Choi S, Rhee S, Hahn Y, Seo SB. Transcriptional regulation of 1-cys peroxiredoxin by the proto-oncogene protein DEK. Mol Med Report 2010; 3:877-81; PMID:21472329.
144. Babaei-Jadidi R, Li N, Saadeddin A, Spencer-Dene B, Jandke A, Muhammad B, et al. FBXW7 influences murine intestinal homeostasis and cancer, targeting Notch, Jun, and DEK for degradation. J Exp Med 2011; 208:295-312; PMID:21282377; http://dx.doi.org/10.1084/jem.20100830.
145. Espinosa L, Inglés-Esteve J, Aguilera C, Bigas A. Phosphorylation by glycogen synthase kinase-3 beta down-regulates Notch activity, a link for Notch and Wnt pathways. J Biol Chem 2003; 278:32227-35; PMID:12794074; http://dx.doi.org/10.1074/jbc.M304001200.
146. Wise-Draper TM, Morreale RJ, Morris TA, Mintz-Cole RA, Hoskins EE, Balsitis SJ, et al. DEK proto-oncogene expression interferes with the normal epithelial differentiation program. Am J Pathol 2009; 174:71-81; PMID:19036808; http://dx.doi.org/10.2353/ajpath.2009.080330.
147. Opferman JT, Iwasaki H, Ong CC, Suh H, Mizuno S, Akashi K, et al. Obligate role of anti-apoptotic MCL-1 in the survival of hematopoietic stem cells. Science 2005; 307:1101-4; PMID:15718471; http://dx.doi.org/10.1126/ science.1106114.
148. Campbell CJ, Lee JB, Levadoux-Martin M, Wynder T, Xenocostas A, Leber B, et al. The human stem cell hierarchy is defined by a functional dependence on Mcl-1 for self-renewal capacity. Blood 2010; 116:1433-42; PMID:20525924; http://dx.doi.org/10.1182/blood-2009-12-258095.
149. Secchiero P, Voltan R, di Iasio MG, Melloni E, Tiribelli M, Zauli G. The oncogene DEK promotes leukemic cell survival and is downregulated by both Nutlin-3 and chlorambucil in B-chronic lymphocytic leukemic cells. Clin Cancer Res 2010; 16:1824-33; PMID:20215548; http://dx.doi.org/10.1158/1078-0432.CCR-09- 3031.
150. Chai W, Ford LP, Lenertz L, Wright WE, Shay JW. Human Ku70/80 associates physically with telomerase through interaction with hTERT. J Biol Chem 2002; 277:47242-7; PMID:12377759; http://dx.doi.org/10.1074/jbc.M208542200.
151. Ting NS, Yu Y, Pohorelic B, Lees-Miller SP, Beattie TL. Human Ku70/80 interacts directly with hTR, the RNA component of human telomerase. Nucleic Acids Res 2005; 33:2090-8; PMID:15824061; http://dx.doi.org/10.1093/nar/gki342.
152. Antão JM, Mason JM, Déjardin J, Kingston RE. Protein landscape at Drosophila melanogaster telomere-associated sequence repeats. Mol Cell Biol 2012; 32:2170-82; PMID:22493064; http://dx.doi.org/10.1128/MCB.00010- 12.
153. Broxmeyer HE, Kappes F, Mor-Vaknin N, Legendre M, Kinzfogl J, Cooper S, et al. DEK Regulates Hematopoietic Stem Engraftment and Progenitor Cell Proliferation. Stem Cells Dev 2011; 21:1449-54; PMID:21943234.
154. Tondeur S, Pangault C, Le Carrour T, Lannay Y, Benmahdi R, Cubizolle A, et al. Expression map of the human exome in CD34+ cells and blood cells: increased alternative splicing in cell motility and immune response genes. PLoS One 2010; 5:e8990; PMID:20126548; http://dx.doi.org/10.1371/journal.pone. 0008990.
155. Oancea C, Rüster B, Henschler R, Puccetti E, Ruthardt M. The t(6;9) associated DEK/CAN fusion protein targets a population of long-term repopulating hematopoietic stem cells for leukemogenic transformation. Leukemia 2010; 24:1910-9; PMID:20827285; http://dx.doi.org/10.1038/leu.2010.180.
156. von Lindern M, Fornerod M, van Baal S, Jaegle M, de Wit T, Buijs A, et al. The translocation (6;9), associated with a specific subtype of acute myeloid leukemia, results in the fusion of two genes, dek and can, and the expression of a chimeric, leukemia-specific dek-can mRNA. Mol Cell Biol 1992; 12:1687-97; PMID:1549122.
157. Ko SI, Lee IS, Kim JY, Kim SM, Kim DW, Lee KS, et al. Regulation of histone acetyltransferase activity of p300 and PCAF by proto-oncogene protein DEK. FEBS Lett 2006; 580:3217-22; PMID:16696975; http://dx.doi.org/10.1016/j. febslet.2006.04.081.
158. Hu HG, Scholten I, Gruss C, Knippers R. The distribution of the DEK protein in mammalian chromatin. Biochem Biophys Res Commun 2007; 358:1008-14; PMID:17524367; http://dx.doi.org/10.1016/j.bbrc.2007.05.019.
159. Carone DM, Lawrence JB. Heterochromatin instability in cancer: From the Barr body to satellites and the nuclear periphery. Semin Cancer Biol 2012; PMID:22722067; http://dx.doi.org/10.1016/j.semcancer.2012.06.008.
160. Dephoure N, Zhou C, Villén J, Beausoleil SA, Bakalarski CE, Elledge SJ, et al. A quantitative atlas of mitotic phosphorylation. Proc Natl Acad Sci U S A 2008; 105:10762-7; PMID:18669648; http://dx.doi.org/10.1073/pnas. 0805139105.