Physiological oxygen prevents frequent silencing of the DLK1-DIO3 cluster during human embryonic stem cells culture

Stem Cells

Volumn 32, Issue 2, 2014, Pages 391-401

  Xie, Pingyuan ^a,b   Sun, Yi ^a,b,c   Ouyang, Qi ^a,b,c   Hu, Liang ^a,b,c   Tan, Yueqiu ^a,b   Zhou, Xiaoying ^c   Xiong, Bo ^c   Zhang, Qianjun ^a,b   Yuan, Ding ^c   Pan, Yi ^c   Liu, Tiancheng ^c   Liang, Ping ^a,d   Lu, Guangxiu ^a,b,c   Lin, Ge ^a,b,c  

^a CENTRAL SOUTH UNIVERSITY   (China)

^b BEIJING HOSPITAL   (China)

^c National Engineering and Research Center of Human Stem Cells   (China)

^d BROCK UNIVERSITY   (Canada)

Author keywords

Apoptosis; DLK1 DIO3; Epigenetics; Human embryonic stem cell; Physiological oxygen

Indexed keywords

APOPTOSIS; DLK1-DIO3; EPIGENETICS; HUMAN EMBRYONIC STEM CELL; PHYSIOLOGICAL OXYGEN;

BIOLOGICAL MARKERS; CELL DIFFERENTIATION; CELLS, CULTURED; DNA METHYLATION; EMBRYONIC STEM CELLS; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; IODIDE PEROXIDASE; MEMBRANE PROTEINS; OXYGEN; RNA, LONG NONCODING;

EID: 84894569297     PISSN: 10665099     EISSN: 15494918     Source Type: Journal    
DOI: 10.1002/stem.1558     Document Type: Article

References (60)

1. Baker DE, Harrison NJ, Maltby E et al. Adaptation to culture of human embryonic stem cells and oncogenesis in vivo. Nat Biotechnol 2007;25: 207-215.
2. Draper JS, Smith K, Gokhale P et al. Recurrent gain of chromosomes 17q and 12 in cultured human embryonic stem cells. Nat Biotechnol 2004;22: 53-54.
3. Spits C, Mateizel I, Geens M et al. Recurrent chromosomal abnormalities in human embryonic stem cells. Nat Biotechnol 2008;26: 1361-1363.
4. Maitra A, Arking DE, Shivapurkar N et al. Genomic alterations in cultured human embryonic stem cells. Nat Genet 2005;37: 1099-1103.
5. Yang S, Lin G, Tan YQ et al. Tumor progression of culture-adapted human embryonic stem cells during long-term culture. Gene Chromosome Cancer 2008;47: 665-679.
6. Werbowetski-Ogilvie TE, Bosse M, Stewart M et al. Characterization of human embryonic stem cells with features of neoplastic progression. Nat Biotechnol 2009;27: 91-97.
7. Amps K, Andrews PW, Anyfantis G et al. Screening ethnically diverse human embryonic stem cells identifies a chromosome 20 minimal amplicon conferring growth advantage. Nat Biotechnol 2011;29: 1132-1144.
8. Nazor KL, Altun G, Lynch C et al. Recurrent variations in DNA methylation in human pluripotent stem cells and their differentiated derivatives. Cell Stem Cell 2012;10: 620-634.
9. Calvanese V, Horrillo A, Hmadcha A. Cancer genes hypermethylated in human embryonic stem cells. PLoS One 2008;3: e3294.
10. Allegrucci C, Wu Y-Z, Thurston A. Restriction landmark genome scanning identifies culture-induced DNA methylation instability in the human embryonic stem cell epigenome. Hum Mol Genet 2007;16: 1253-1268.
11. Rugg-Gunn PJ, Ferguson-Smith AC, Pedersen RA. Status of genomic imprinting in human embryonic stem cells as revealed by a large cohort of independently derived and maintained lines. Hum Mol Genet 2007;16 Spec No. 2: R243-251.
12. Rugg-Gunn PJ, Ferguson-Smith AC, Pedersen RA. Epigenetic status of human embryonic stem cells. Nat Genet 2005;37: 585-587.
13. Kim KP, Thurston A, Mummery C et al. Gene-specific vulnerability to imprinting variability in human embryonic stem cell lines. Genome Res 2007;17: 1731-1742.
14. Tanasijevic B, Dai B, Ezashi T et al. Progressive accumulation of epigenetic heterogeneity during human ES cell culture. Epigenetics 2009;4: 330-338.
15. Silva SS, Rowntree RK, Mekhoubad S et al. X-chromosome inactivation and epigenetic fluidity in human embryonic stem cells. Proc Natl Acad Sci USA 2008;105: 4820-4825.
16. Shen Y, Matsuno Y, Fouse SD et al. Xinactivation in female human embryonic stem cells is in a nonrandom pattern and prone to epigenetic alterations. Proc Natl Acad Sci USA 2008;105: 4709-4714.
17. Hall LL, Byron M, Butler J et al. X-inactivation reveals epigenetic anomalies in most hESC but identifies sublines that initiate as expected. J Cell Physiol 2008;216: 445-452.
18. Jones PA, Baylin SB. The epigenomics of cancer. Cell 2007;128: 683-692.
19. Vucic EA, Brown CJ, Lam WL. Epigenetics of cancer progression. Pharmacogenomics 2008;9: 215-234.
20. Pannetier M, Feil R. Epigenetic stability of embryonic stem cells and developmental potential. Trends Biotechnol 2007;25: 556-562.
21. Lefort N, Perrier AL, Laabi Y et al. Human embryonic stem cells and genomic instability. Regen Med 2009;4: 899-909.
22. Buzzard JJ, Gough NM, Crook JM et al. Karyotype of human ES cells during extended culture. Nat Biotechnol 2004;22: 381-382, author reply 382.
23. Brimble SN, Zeng X, Weiler DA et al. Karyotypic stability, genotyping, differentiation, feeder-free maintenance, and gene expression sampling in three human embryonic stem cell lines derived prior to August 9, 2001. Stem Cells Dev 2004;13: 585-597.
24. Lengner CJ, Gimelbrant AA, Erwin JA et al. Derivation of Pre-X inactivation human embryonic stem cells under physiological oxygen concentrations. Cell 2010;141: 872-883.
25. Reijo Pera RA, DeJonge C, Bossert N et al. Gene expression profiles of human inner cell mass cells and embryonic stem cells. Differentiation 2009;78: 18-23.
26. Lin G, Xie YB, OuYang Q et al. HLAmatching potential of an established human embryonic stem cell bank in China. Cell Stem Cell 2009;5: 461-465.
27. Eisen MB, Spellman PT, Brown PO et al. Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 1998;95: 14863-14868.
28. Saeed AI, Bhagabati NK, Braisted JC et al. TM4 microarray software suite. Methods Enzymol 2006;411: 134-193.
29. Tusher VG, Tibshirani R, Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 2001;98: 5116-5121.
30. Li R, Li Y, Kristiansen K et al. SOAP: Short oligonucleotide alignment program. Bioinformatics 2008;24: 713-714.
31. Griffiths-Jones S. Annotating non-coding RNAs with Rfam. Curr Protoc Bioinformatics. 2005;Chapter 12: Unit 12 15.
32. Griffiths-Jones S, Moxon S, Marshall M et al. Rfam: Annotating non-coding RNAs in complete genomes. Nucleic Acids Res 2005; 33: D121-124.
33. Bock C, Kiskinis E, Verstappen G et al. Reference maps of human ES and iPS cell variation enable high-throughput characterization of pluripotent cell lines. Cell 2011;144: 439-452.
34. Soldner F, Hockemeyer D, Beard C et al. Parkinson's disease patient-derived induced pluripotent stem cells free of viral reprogramming factors. Cell 2009;136: 964-977.
35. Westfall SD, Sachdev S, Das P et al. Identification of oxygen-sensitive transcriptional programs in human embryonic stem cells. Stem Cells Dev 2008;17: 869-881.
36. Ebert AD, Yu J, Rose FF, Jr. et al. Induced pluripotent stem cells from a spinal muscular atrophy patient. Nature 2009;457: 277-280.
37. Maherali N, Ahfeldt T, Rigamonti A et al. A high-efficiency system for the generation and study of human induced pluripotent stem cells. Cell Stem Cell 2008;3: 340-345.
38. Fong CY, Chak LL, Biswas A et al. Human Wharton's jelly stem cells have unique transcriptome profiles compared to human embryonic stem cells and other mesenchymal stem cells. Stem Cell Rev 2011;7: 1-16.
39. Tchieu J, Kuoy E, Chin MH et al. Female human iPSCs retain an inactive X chromosome. Cell Stem Cell 2010;7: 329-342.
40. Hanna J, Cheng AW, Saha K et al. Human embryonic stem cells with biological and epigenetic characteristics similar to those of mouse ESCs. Proc Natl Acad Sci USA 2010; 107: 9222-9227.
41. Jia F, Wilson KD, Sun N et al. A nonviral minicircle vector for deriving human iPS cells. Nat Methods 2010;7: 197-199.
42. Yu J, Hu K, Smuga-Otto K et al. Human induced pluripotent stem cells free of vector and transgene sequences. Science 2009;324: 797-801.
43. Mayshar Y, Ben-David U, Lavon N et al. Identification and classification of chromosomal aberrations in human induced pluripotent stem cells. Cell Stem Cell 2010;7: 521-531.
44. Kim DS, Lee JS, Leem JW et al. Robust enhancement of neural differentiation from human ES and iPS cells regardless of their innate difference in differentiation propensity. Stem Cell Rev 2010;6: 270-281.
45. Sullivan GJ, Hay DC, Park IH et al. Generation of functional human hepatic endoderm from human induced pluripotent stem cells. Hepatology 2010;51: 329-335.
46. Sun Y, Yi H, Zhang PF et al. Identification of differential proteins in nasopharyngeal carcinoma cells with p53 silence by proteome analysis. FEBS Lett 2007;581: 131-139.
47. Zhou Y, Zhong Y, Wang Y et al. Activation of p53 by MEG3 non-coding RNA. J Biol Chem 2007;282: 24731-24742.
48. Cavaille J, Seitz H, Paulsen M et al. Identification of tandemly-repeated C/D snoRNA genes at the imprinted human 14q32 domain reminiscent of those at the Prader-Willi/Angelman syndrome region. Hum Mol Genet 2002;11: 1527-1538.
49. Seitz H, Royo H, Bortolin ML et al. A large imprinted microRNA gene cluster at the mouse Dlk1-Gtl2 domain. Genome Res 2004; 14: 1741-1748.
50. Kagami M, O'Sullivan MJ, Green AJ et al. The IG-DMR and the MEG3-DMR at human chromosome 14q32.2: Hierarchical interaction and distinct functional properties as imprinting control centers. PLoS Genet 2010; 6: e1000992.
51. Stadtfeld M, Apostolou E, Akutsu H et al. Aberrant silencing of imprinted genes on chromosome 12qF1 in mouse induced pluripotent stem cells. Nature 2010;465: 175-181.
52. Liu L, Luo GZ, Yang W et al. Activation of the imprinted Dlk1-Dio3 region correlates with pluripotency levels of mouse stem cells. J Biol Chem 2010;285: 19483-19490.
53. Hoffman LM, Carpenter MK. Characterization and culture of human embryonic stem cells. Nat Biotechnol 2005;23: 699-708.
54. Braconi C, Kogure T, Valeri N et al. microRNA-29 can regulate expression of the long non-coding RNA gene MEG3 in hepatocellular cancer. Oncogene 2011;30: 4750-4756.
55. Zhang X, Gejman R, Mahta A et al. Maternally expressed gene 3, an imprinted noncoding RNA gene, is associated with meningioma pathogenesis and progression. Cancer Res 2010;70: 2350-2358.
56. Pick M, Stelzer Y, Bar-Nur O et al. Cloneand gene-specific aberrations of parental imprinting in human induced pluripotent stem cells. Stem Cells 2009;27: 2686-2690.
57. Edwards CA, Mungall AJ, Matthews L et al. The evolution of the DLK1-DIO3 imprinted domain in mammals. PLoS Biol 2008;6: e135.
58. da Rocha ST, Edwards CA, Ito M et al. Genomic imprinting at the mammalian Dlk1-Dio3 domain. Trends Genet 2008; 24: 306-316.
59. Zhou Y, Zhang X, Klibanski A. MEG3 noncoding RNA: A tumor suppressor. J Mol Endocrinol 2012;48: R45-53.
60. Benetatos L, Vartholomatos G, Hatzimichael E. MEG3 imprinted gene contribution in tumorigenesis. Int J Cancer 2011;129: 773-779.