Functional and molecular characterization of the role of CTCF in human embryonic stem cell biology

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Balakrishnan, Sri Kripa ^a   Witcher, Michael ^a,b   Berggren, Travis W ^a   Emerson, Beverly M ^a  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN 4; COHESIN; GROWTH DIFFERENTIATION FACTOR 3; TRANSCRIPTION FACTOR CTCF; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2;

ARTICLE; BINDING SITE; CELL DIFFERENTIATION; CONTROLLED STUDY; DPPA3 GENE; EMBRYO; EMBRYONIC STEM CELL; GDF3 GENE; GENE; GENE EXPRESSION; GENE LOCUS; HUMAN; HUMAN CELL; LIN28 GENE; NANOG GENE; ONCOGENE C MYC; PLURIPOTENT STEM CELL; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SOX2 GENE;

BINDING SITES; BIOLOGICAL MARKERS; CELL DIFFERENTIATION; CELL LINE; EMBRYONIC STEM CELLS; ENHANCER ELEMENTS, GENETIC; GENE EXPRESSION REGULATION; GENETIC LOCI; GROWTH DIFFERENTIATION FACTOR 3; HOMEODOMAIN PROTEINS; HUMANS; MODELS, BIOLOGICAL; PLURIPOTENT STEM CELLS; POLY ADENOSINE DIPHOSPHATE RIBOSE; PROTEIN BINDING; PROTEINS; REPRESSOR PROTEINS;

VERTEBRATA;

EID: 84864535173     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0042424     Document Type: Article

References (50)

1. Orkin SH, Wang J, Kim J, Chu J, Rao S, et al. (2008) The transcriptional network controlling pluripotency in ES cells. Cold Spring Harbor symposia on quantitative biology 73: 195-202.
2. Kim J, Chu J, Shen X, Wang J, Orkin SH, (2008) An extended transcriptional network for pluripotency of embryonic stem cells. Cell 132: 1049-1061.
3. Jaenisch R, Young R, (2008) Stem cells, the molecular circuitry of pluripotency and nuclear reprogramming. Cell 132: 567-582.
4. Chia NY, Chan YS, Feng B, Lu X, Orlov YL, et al. (2010) A genome-wide RNAi screen reveals determinants of human embryonic stem cell identity. Nature 468: 316-320.
5. Tutter AV, Kowalski MP, Baltus GA, Iourgenko V, Labow M, et al. (2009) Role for Med12 in regulation of Nanog and Nanog target genes. J Biol Chem 284: 3709-3718.
6. Phillips JE, Corces VG, (2009) CTCF: master weaver of the genome. Cell 137: 1194-1211.
7. Filippova GN, (2008) Genetics and epigenetics of the multifunctional protein CTCF. Curr Top Dev Biol 80: 337-360.
8. Wan LB, Pan H, Hannenhalli S, Cheng Y, Ma J, et al. (2008) Maternal depletion of CTCF reveals multiple functions during oocyte and preimplantation embryo development. Development 135: 2729-2738.
9. Fedoriw AM, Stein P, Svoboda P, Schultz RM, Bartolomei MS, (2004) Transgenic RNAi reveals essential function for CTCF in H19 gene imprinting. Science 303: 238-240.
10. Bell AC, Felsenfeld G, (2000) Methylation of a CTCF-dependent boundary controls imprinted expression of the Igf2 gene. Nature 405: 482-485.
11. Bell AC, West AG, Felsenfeld G, (1999) The protein CTCF is required for the enhancer blocking activity of vertebrate insulators. Cell 98: 387-396.
12. Hark AT, Schoenherr CJ, Katz DJ, Ingram RS, Levorse JM, et al. (2000) CTCF mediates methylation-sensitive enhancer-blocking activity at the H19/Igf2 locus. Nature 405: 486-489.
13. Kanduri C, Pant V, Loukinov D, Pugacheva E, Qi CF, et al. (2000) Functional association of CTCF with the insulator upstream of the H19 gene is parent of origin-specific and methylation-sensitive. Curr Biol 10: 853-856.
14. Murrell A, Heeson S, Reik W, (2004) Interaction between differentially methylated regions partitions the imprinted genes Igf2 and H19 into parent-specific chromatin loops. Nat Genet 36: 889-893.
15. Kurukuti S, Tiwari VK, Tavoosidana G, Pugacheva E, Murrell A, et al. (2006) CTCF binding at the H19 imprinting control region mediates maternally inherited higher-order chromatin conformation to restrict enhancer access to Igf2. Proc Natl Acad Sci U S A 103: 10684-10689.
16. Cuddapah S, Jothi R, Schones DE, Roh TY, Cui K, et al. (2009) Global analysis of the insulator binding protein CTCF in chromatin barrier regions reveals demarcation of active and repressive domains. Genome Res 19: 24-32.
17. Witcher M, Emerson BM, (2009) Epigenetic silencing of the p16(INK4a) tumor suppressor is associated with loss of CTCF binding and a chromatin boundary. Mol Cell 34: 271-284.
18. Kunarso G, Chia NY, Jeyakani J, Hwang C, Lu X, et al. (2010) Transposable elements have rewired the core regulatory network of human embryonic stem cells. Nat Genet 42: 631-634.
19. Heintzman ND, Hon GC, Hawkins RD, Kheradpour P, Stark A, et al. (2009) Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 459: 108-112.
20. Ludwig TE, Bergendahl V, Levenstein ME, Yu J, Probasco MD, et al. (2006) Feeder-independent culture of human embryonic stem cells. Nat Methods 3: 637-646.
21. Xu RH, Chen X, Li DS, Li R, Addicks GC, et al. (2002) BMP4 initiates human embryonic stem cell differentiation to trophoblast. Nat Biotechnol 20: 1261-1264.
22. Richards M, Tan SP, Tan JH, Chan WK, Bongso A, (2004) The transcriptome profile of human embryonic stem cells as defined by SAGE. Stem Cells 22: 51-64.
23. Cartwright P, McLean C, Sheppard A, Rivett D, Jones K, et al. (2005) LIF/STAT3 controls ES cell self-renewal and pluripotency by a Myc-dependent mechanism. Development 132: 885-896.
24. Xu RH, Peck RM, Li DS, Feng X, Ludwig T, et al. (2005) Basic FGF and suppression of BMP signaling sustain undifferentiated proliferation of human ES cells. Nat Methods 2: 185-190.
25. Strumpf D, Mao CA, Yamanaka Y, Ralston A, Chawengsaksophak K, et al. (2005) Cdx2 is required for correct cell fate specification and differentiation of trophectoderm in the mouse blastocyst. Development 132: 2093-2102.
26. Ng YK, George KM, Engel JD, Linzer DI, (1994) GATA factor activity is required for the trophoblast-specific transcriptional regulation of the mouse placental lactogen I gene. Development 120: 3257-3266.
27. Lister R, Pelizzola M, Dowen RH, Hawkins RD, Hon G, et al. (2009) Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 462: 315-322.
28. Chen X, Xu H, Yuan P, Fang F, Huss M, et al. (2008) Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell 133: 1106-1117.
29. Chen G, Gulbranson DR, Hou Z, Bolin JM, Ruotti V, et al. (2011) Chemically defined conditions for human iPSC derivation and culture. Nature methods 8: 424-429.
30. Phanstiel D, Brumbaugh J, Berggren WT, Conard K, Feng X, et al. (2008) Mass spectrometry identifies and quantifies 74 unique histone H4 isoforms in differentiating human embryonic stem cells. Proc Natl Acad Sci U S A 105: 4093-4098.
31. Barski A, Cuddapah S, Cui K, Roh TY, Schones DE, et al. (2007) High-resolution profiling of histone methylations in the human genome. Cell 129: 823-837.
32. Bao L, Zhou M, Cui Y, (2008) CTCFBSDB: a CTCF-binding site database for characterization of vertebrate genomic insulators. Nucleic acids research 36: D83-87.
33. Kim TH, Abdullaev ZK, Smith AD, Ching KA, Loukinov DI, et al. (2007) Analysis of the vertebrate insulator protein CTCF-binding sites in the human genome. Cell 128: 1231-1245.
34. Recillas-Targa F, Bell AC, Felsenfeld G, (1999) Positional enhancer-blocking activity of the chicken beta-globin insulator in transiently transfected cells. Proc Natl Acad Sci U S A 96: 14354-14359.
35. Yusufzai TM, Tagami H, Nakatani Y, Felsenfeld G, (2004) CTCF tethers an insulator to subnuclear sites, suggesting shared insulator mechanisms across species. Mol Cell 13: 291-298.
36. Parelho V, Hadjur S, Spivakov M, Leleu M, Sauer S, et al. (2008) Cohesins functionally associate with CTCF on mammalian chromosome arms. Cell 132: 422-433.
37. Rubio ED, Reiss DJ, Welcsh PL, Disteche CM, Filippova GN, et al. (2008) CTCF physically links cohesin to chromatin. Proc Natl Acad Sci U S A 105: 8309-8314.
38. Wendt KS, Yoshida K, Itoh T, Bando M, Koch B, et al. (2008) Cohesin mediates transcriptional insulation by CCCTC-binding factor. Nature 451: 796-801.
39. Yu W, Ginjala V, Pant V, Chernukhin I, Whitehead J, et al. (2004) Poly(ADP-ribosyl)ation regulates CTCF-dependent chromatin insulation. Nat Genet 36: 1105-1110.
40. Xiao T, Wallace J, Felsenfeld G, (2011) Specific sites in the C terminus of CTCF interact with the SA2 subunit of the cohesin complex and are required for cohesin-dependent insulation activity. Mol Cell Biol 31: 2174-2183.
41. Filippova GN, Fagerlie S, Klenova EM, Myers C, Dehner Y, et al. (1996) An exceptionally conserved transcriptional repressor, CTCF, employs different combinations of zinc fingers to bind diverged promoter sequences of avian and mammalian c-myc oncogenes. Mol Cell Biol 16: 2802-2813.
42. Gombert WM, Farris SD, Rubio ED, Morey-Rosler KM, Schubach WH, et al. (2003) The c-myc insulator element and matrix attachment regions define the c-myc chromosomal domain. Mol Cell Biol 23: 9338-9348.
43. Heath H, Ribeiro de Almeida C, Sleutels F, Dingjan G, van de Nobelen S, et al. (2008) CTCF regulates cell cycle progression of alphabeta T cells in the thymus. The EMBO journal 27: 2839-2850.
44. Korkola JE, Houldsworth J, Chadalavada RS, Olshen AB, Dobrzynski D, et al. (2006) Down-regulation of stem cell genes, including those in a 200-kb gene cluster at 12p13.31, is associated with in vivo differentiation of human male germ cell tumors. Cancer Res 66: 820-827.
45. Ezeh UI, Turek PJ, Reijo RA, Clark AT, (2005) Human embryonic stem cell genes OCT4, NANOG, STELLAR, and GDF3 are expressed in both seminoma and breast carcinoma. Cancer 104: 2255-2265.
46. Clark AT, Rodriguez RT, Bodnar MS, Abeyta MJ, Cedars MI, et al. (2004) Human STELLAR, NANOG, and GDF3 genes are expressed in pluripotent cells and map to chromosome 12p13, a hotspot for teratocarcinoma. Stem Cells 22: 169-179.
47. Tolhuis B, Palstra RJ, Splinter E, Grosveld F, de Laat W, (2002) Looping and interaction between hypersensitive sites in the active beta-globin locus. Mol Cell 10: 1453-1465.
48. Levasseur DN, Wang J, Dorschner MO, Stamatoyannopoulos JA, Orkin SH, (2008) Oct4 dependence of chromatin structure within the extended Nanog locus in ES cells. Genes Dev 22: 575-580.
49. Gombert WM, Krumm A, (2009) Targeted deletion of multiple CTCF-binding elements in the human C-MYC gene reveals a requirement for CTCF in C-MYC expression. PLoS One 4: e6109.
50. Lunyak VV, Prefontaine GG, Nunez E, Cramer T, Ju BG, et al. (2007) Developmentally regulated activation of a SINE B2 repeat as a domain boundary in organogenesis. Science 317: 248-251.