Undifferentiated hematopoietic cells are characterized by a genome-wide undermethylation dip around the transcription start site and a hierarchical epigenetic plasticity

Blood

Volumn 114, Issue 24, 2009, Pages 4968-4978

  Chung, Yun Shin ^a   Kim, Hye Joung ^a   Kim, Tae Min ^a   Hong, Sung Hyun ^a   Kwon, Kyung Rim ^a   An, Sungwhan ^b   Park, Jung Hoon ^a   Lee, Suman ^c   Oh, Il Hoan ^a  

^a The Catholic University of Korea College of Medicine   (South Korea)

^b Genomictree Inc   (South Korea)

^c CHA University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

AZACITIDINE; CD34 ANTIGEN; HISTONE; TRICHOSTATIN A;

ACETYLATION; ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; BONE MARROW; CELL DEDIFFERENTIATION; CELL DIFFERENTIATION; CELL RENEWAL; CELL STIMULATION; CHROMATIN; CHROMATIN CONDENSATION; CHROMATIN STRUCTURE; CONTROLLED STUDY; CORRELATION ANALYSIS; CPG ISLAND; EPIGENETICS; GENOME; HEMATOPOIETIC CELL; HUMAN; HUMAN CELL; METHYLATION; MOUSE; NONHUMAN; PHENOTYPE; PLASTICITY; PRIORITY JOURNAL; STEADY STATE; TRANSCRIPTION INITIATION SITE; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CYTOLOGY; DNA METHYLATION; GENETIC EPIGENESIS; GENETICS; HEMATOPOIETIC STEM CELL; METABOLISM; PROMOTER REGION; WESTERN BLOTTING;

ACETYLATION; ANIMALS; ANTIGENS, CD34; BLOTTING, WESTERN; CELL DIFFERENTIATION; CPG ISLANDS; DNA METHYLATION; EPIGENESIS, GENETIC; HEMATOPOIETIC STEM CELLS; HUMANS; MICE; MICE, INBRED C57BL; PROMOTER REGIONS, GENETIC; TRANSCRIPTION INITIATION SITE;

EID: 73949136873     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2009-01-197780     Document Type: Article

References (50)

1. Eaves C, Miller C, Cashman J, et al. Hematopoietic stem cells: inferences from in vivo assays. Stem Cells. 1997;15(suppl 1):1-5.
2. Stein MI, Zhu J, Emerson SG. Molecular pathways regulating the self-renewal of hematopoietic stem cells. Exp Hematol. 2004;32(12): 1129-1136.
3. Ramalho-Santos M, Yoon S, Matsuzaki Y, Mulligan RC, Melton DA. "Stemness": transcriptional profiling of embryonic and adult stem cells. Science. 2002;298(5593):597-600.
4. Ivanova NB, Dimos JT, Schaniel C, Hackney JA, Moore KA, Lemischka IR. A stem cell molecular signature. Science. 2002;298(5593):601-604.
5. Reik W, Dean W, Walter J. Epigenetic reprogramming in mammalian development. Science. 2001; 293(5532):1089-1093.
6. Jaenisch R, Bird A. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet. 2003; 33[suppl]:245-254.
7. Eberharter A, Becker PB. Histone acetylation: a switch between repressive and permissive chromatin [second in review series on chromatin dynamics]. EMBO Rep. 2002;3(3):224-229.
8. Bird A. DNA methylation patterns and epigenetic memory. Genes Dev. 2002;16(1):6-21.
9. Nan X, Campoy FJ, Bird A. MeCP2 is a transcriptional repressor with abundant binding sites in genomic chromatin. Cell. 1997;88(4): 471-481.
10. Azuara V, Perry P, Sauer S, et al. Chromatin signatures of pluripotent cell lines. Nat Cell Biol. 2006;8(5):532-538.
11. Spivakov M, Fisher AG. Epigenetic signatures of stem-cell identity. Nat Rev Genet. 2007;8(4):263-271.
12. Bernstein BE, Mikkelsen TS, Xie X, et al. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell. 2006; 125(2):315-326.
13. Bonifer C. Epigenetic plasticity of hematopoietic cells. Cell Cycle. 2005;4(2):211-214.
14. Cerny J, Quesenberry PJ. Chromatin remodeling and stem cell theory of relativity. J Cell Physiol. 2004;201(1):1-16.
15. Rice KL, Hormaeche I, Licht JD. Epigenetic regulation of normal and malignant hematopoiesis. Oncogene. 2007;26(47):6697-6714.
16. Hu M, Krause D, Greaves M, et al. Multilineage gene expression precedes commitment in the hemopoietic system. Genes Dev. 1997;11(6):774-785.
17. Miyamoto T, Iwasaki H, Reizis B, et al. Myeloid or lymphoid promiscuity as a critical step in hematopoietic lineage commitment. Dev Cell. 2002;3(1): 137-147.
18. Akashi K, He X, Chen J, et al. Transcriptional accessibility for genes of multiple tissues and hematopoietic lineages is hierarchically controlled during early hematopoiesis. Blood. 2003;101(2):383-389.
19. Tagoh H, Himes R, Clarke D, et al. Transcription factor complex formation and chromatin fine structure alterations at the murine c-fms (CSF-1 receptor) locus during maturation of myeloid precursor cells. Genes Dev. 2002; 16(13):1721-1737.
20. Bruno L, Hoffmann R, McBlane F, et al. Molecular signatures of self-renewal, differentiation, and lineage choice in multipotential hemopoietic progenitor cells in vitro. Mol Cell Biol. 2004;24(2): 741-756.
21. Attema JL, Papathanasiou P, Forsberg EC, Xu J, Smale ST, Weissman IL. Epigenetic characterization of hematopoietic stem cell differentiation using miniChIP and bisulfite sequencing analysis. Proc Natl Acad Sci U S A. 2007;104(30):12371-12376.
22. Kang YJ, Yang SJ, Park G, et al. A novel function of interleukin-10 promoting self-renewal of hematopoietic stem cells. Stem Cells. 2007;25(7): 1814-1822.
23. Boyer LA, Lee TI, Cole MF, et al. Core transcriptional regulatory circuitry in human embryonic stem cells. Cell. 2005;122(6):947-956.
24. Huang da W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2009;4(1):44-57.
25. Moon N, Yang SJ, Park BB, Chung YS, Lee JW, Oh IH. Efficient bone marrow transduction by gene transfer with allogeneic umbilical cord blood serum and plasma: an implication for clinical trials. Hum Gene Ther. 2008;19(7):744-752.
26. Petzer AL, Hogge DE, Landsdorp PM, Reid DS, Eaves CJ. Self-renewal of primitive human hematopoietic cells (long-term-culture-initiating cells) in vitro and their expansion in defined medium. Proc Natl Acad Sci U S A. 1996;93(4): 1470-1474.
27. Chung YJ, Park BB, Kang YJ, Kim TM, Eaves CJ, Oh IH. Unique effects of Stat3 on the early phase of hematopoietic stem cell regeneration. Blood. 2006;108(4):1208-1215.
28. Szilvassy SJ, Humphries RK, Lansdorp PM, Eaves AC, Eaves CJ. Quantitative assay for totipotent reconstituting hematopoietic stem cells by a competitive repopulation strategy. Proc Natl Acad Sci U S A. 1990;87(22):8736-8740.
29. Rauch T, Li H, Wu X, Pfeifer GP. MIRA-assisted microarray analysis, a new technology for the determination of DNA methylation patterns, identifies frequent methylation of homeodomain-containing genes in lung cancer cells. Cancer Res. 2006;66(16):7939-7947.
30. Ben-Porath I, Thomson MW, Carey VJ, et al. An embryonic stem cell-like gene expression signature in poorly differentiated aggressive human tumors. Nat Genet. 2008;40(5):499-507.
31. Kim SY, Volsky DJ. PAGE: parametric analysis of gene set enrichment. BMC Bioinformatics. 2005; 6:144.
32. Lee TI, Jenner RG, Boyer LA, et al. Control of developmental regulators by Polycomb in human embryonic stem cells. Cell. 2006;125(2): 301-313.
33. Orford K, Kharchenko P, Lai W, et al. Differential H3K4 methylation identifies developmentally poised hematopoietic genes. Dev Cell. 2008; 14(5):798-809.
34. Kang YK, Koo DB, Park JS, et al. Aberrant methylation of donor genome in cloned bovine embryos. Nat Genet. 2001;28(2):173-177.
35. Kim SH, Kang YK, Koo DB, et al. Differential DNA methylation reprogramming of various repetitive sequences in mouse preimplantation embryos. Biochem Biophys Res Commun. 2004;324(1):58-63.
36. Yang AS, Estecio MR, Doshi K, Kondo Y, Tajara EH, Issa JP. A simple method for estimating global DNA methylation using bisulfite PCR of repetitive DNA elements. Nucleic Acids Res. 2004;32(3):e38.
37. Oh IH, Lau A, Eaves CJ. During ontogeny primitive (CD34(+)CD38(-)) hematopoietic cells show altered expression of a subset of genes associated with early cytokine and differentiation responses of their adult counterparts. Blood. 2000; 96(13):4160-4168.
38. Santos-Rosa H, Schneider R, Bannister AJ, et al. Active genes are tri-methylated at K4 of histone H3. Nature. 2002;419(6905):407-411.
39. Kouzarides T. Histone methylation in transcriptional control. Curr Opin Genet Dev. 2002;12(2): 198-209.
40. Tadokoro Y, Ema H, Okano M, Li E, Nakauchi H. De novo DNA methyltransferase is essential for self-renewal, but not for differentiation, in hematopoietic stem cells. J Exp Med. 2007;204(4):715-722.
41. Georgantas RW 3rd, Hildreth R, Morisot S, et al. CD34+ hematopoietic stem-progenitor cell microRNA expression and function: a circuit diagram of differentiation control. Proc Natl Acad Sci U S A. 2007;104(8):2750-2755.
42. Bernstein BE, Kamal M, Lindblad-Toh K, et al. Genomic maps and comparative analysis of histone modifications in human and mouse. Cell. 2005;120(2):169-181.
43. Tanay A, O'Donnell AH, Damelin M, Bestor TH. Hyperconserved CpG domains underlie Polycomb-binding sites. Proc Natl Acad Sci U S A. 2007;104(13):5521- 5526.
44. Kingston RE, Narlikar GJ. ATP-dependent remodeling and acetylation as regulators of chromatin fluidity. Genes Dev. 1999;13(18):2339-2352.
45. Eberharter A, Ferreira R, Becker P. Dynamic chromatin: concerted nucleosome remodelling and acetylation. Biol Chem. 2005;386(8):745-751.
46. Araki H, Mahmud N, Milhem M, et al. Expansion of human umbilical cord blood SCID-repopulating cells using chromatin-modifying agents. Exp Hematol. 2006;34(2):140-149.
47. Araki H, Yoshinaga K, Boccuni P, Zhao Y, Hoffman R, Mahmud N. Chromatin-modifying agents permit human hematopoietic stem cells to undergo multiple cell divisions while retaining their repopulating potential. Blood. 2007;109(8): 3570-3578.
48. Milhem M, Mahmud N, Lavelle D, et al. Modification of hematopoietic stem cell fate by 5aza 2′ deoxycytidine and trichostatin A. Blood. 2004; 103(11):4102-4110.
49. Jost JP, Oakeley EJ, Zhu B, et al. 5-Methylcytosine DNA glycosylase participates in the genome-wide loss of DNA methylation occurring during mouse myoblast differentiation. Nucleic Acids Res. 2001; 29(21):4452-4461.
50. Meshorer E, Yellajoshula D, George E, Scambler PJ, Brown DT, Misteli T. Hyperdynamic plasticity of chromatin proteins in pluripotent embryonic stem cells. Dev Cell. 2006;10(1): 105-116.