The dynamic changes of X chromosome inactivation during early culture of human embryonic stem cells

Stem Cell Research

Volumn 17, Issue 1, 2016, Pages 84-92

  Xie, Pingyuan ^a,b,c   Ouyang, Qi ^a,b,c   Leng, Lizhi ^a,c   Hu, Liang ^a,b,c   Cheng, Dehua ^a,b,c   Tan, Yueqiu ^a,b,c   Lu, Guangxiu ^b,c   Lin, Ge ^a,b,c  

^a CENTRAL SOUTH UNIVERSITY   (China)

^b National Center of Human Stem Cell Research and Engineering   (China)

^c BEIJING HOSPITAL   (China)

Author keywords

Culture alteration; Epigenetics; Gene expression regulation; Human embryonic stem cells; X chromosome inactivation

Indexed keywords

RNA; HISTONE; LONG UNTRANSLATED RNA; OXYGEN; XIST NON-CODING RNA;

ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; EMBRYO; EPIGENETICS; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN EMBRYONIC STEM CELL; IN VITRO STUDY; MALE; PRIORITY JOURNAL; STEM CELL CULTURE; TUMOR GENE; UPREGULATION; X CHROMOSOME INACTIVATION; XIST GENE; CELL CULTURE; CYTOLOGY; DNA METHYLATION; FLUORESCENCE MICROSCOPY; GENETICS; METABOLISM; PROMOTER REGION;

CELL DIFFERENTIATION; CELLS, CULTURED; DNA METHYLATION; FEMALE; HISTONES; HUMAN EMBRYONIC STEM CELLS; HUMANS; MICROSCOPY, FLUORESCENCE; OXYGEN; PROMOTER REGIONS, GENETIC; RNA, LONG NONCODING; X CHROMOSOME INACTIVATION;

EID: 84973364230     PISSN: 18735061     EISSN: 18767753     Source Type: Journal    
DOI: 10.1016/j.scr.2016.05.011     Document Type: Article

References (38)

1. Adewumi O., Aflatoonian B., Ahrlund-Richter L., Amit M., Andrews P.W., Beighton G., Bello P.A., Benvenisty N., Berry L.S., Bevan S., Blum B., Brooking J., Chen K.G., Choo A.B.H., Churchill G.A., Corbel M., Damjanov I., Draper J.S., Dvorak P., Emanuelsson K., Fleck R.A., Ford A., Gertow K., Gertsenstein M., Gokhale P.J., Hamilton R.S., Hampl A., Healy L.E., Hovatta O., Hyllner J., Imreh M.P., Itskovitz-Eldor J., Jackson J., Johnson J.L., Jones M., Kee K., King B.L., Knowles B.B., Lako M., Lebrin F., Mallon B.S., Manning D., Mayshar Y., McKay R.D.G., Michalska A.E., Mikkola M., Mileikovsky M., Minger S.L., Moore H.D., Mummery C.L., Nagy A., Nakatsuji N., O'Brien C.M., Oh S.K.W., Olsson C., Otonkoski T., Park K.Y., Passier R., Patel H., Patel M., Pedersen R., Pera M.F., Piekarczyk M.S., Pera R.A.R., Reubinoff B.E., Robins A.J., Rossant J., Rugg-Gunn P., Schulz T.C., Semb H., Sherrer E.S., Siemen H., Stacey G.N., Stojkovic M., Suemori H., Szatkiewicz J., Turetsky T., Tuuri T., van den Brink S., Vintersten K., Vuoristo S., Ward D., Weaver T.A., Young L.A., Zhang W.D., I.Int Stem Cell Characterization of human embryonic stem cell lines by the International Stem Cell Initiative. Nature Biotechnology 2007, 25:803-816.
2. Berry N.B., Bapat S.A. Ovarian cancer plasticity and epigenomics in the acquisition of a stem-like phenotype. J Ovarian Res 2008, 1:8.
3. Brown C.J., Ballabio A., Rupert J.L., Lafreniere R.G., Grompe M., Tonlorenzi R., Willard H.F. A gene from the region of the human X inactivation centre is expressed exclusively from the inactive X chromosome. Nature 1991, 349:38-44.
4. Buller R.E., Sood A.K., Lallas T., Buekers T., Skilling J.S. Association between nonrandom X-chromosome inactivation and BRCA1 mutation in germline DNA of patients with ovarian cancer. J. Natl. Cancer Inst. 1999, 91:339-346.
5. Carrel L., Willard H.F. X-inactivation profile reveals extensive variability in X-linked gene expression in females. Nature 2005, 434:400-404.
6. Cerase A., Pintacuda G., Tattermusch A., Avner P. Xist localization and function: new insights from multiple levels. Genome Biol. 2015, 16:166.
7. Chen M., Li G., Yan J., Lu X., Cui J., Ni Z., Cheng W., Qian G., Zhang J., Tu H. Reevaluation of glypican-3 as a serological marker for hepatocellular carcinoma. Clin. Chim. Acta 2013, 423:105-111.
8. Draper J.S., Smith K., Gokhale P., Moore H.D., Maltby E., Johnson J., Meisner L., Zwaka T.P., Thomson J.A., Andrews P.W. Recurrent gain of chromosomes 17q and 12 in cultured human embryonic stem cells. Nat. Biotechnol. 2004, 22:53-54.
9. Dvash T., Lavon N., Fan G. Variations of X chromosome inactivation occur in early passages of female human embryonic stem cells. PLoS One 2010, 5.
10. Guo Z., Yuan J., Tang W., Chen X., Gu X., Luo K., Wang Y., Wan B., Yu L. Cloning and characterization of the human gene RAP2C, a novel member of Ras family, which activates transcriptional activities of SRE. Mol. Biol. Rep. 2007, 34:137-144.
11. Hall L.L., Byron M., Butler J., Becker K.A., Nelson A., Amit M., Itskovitz-Eldor J., Stein J., Stein G., Ware C., Lawrence J.B. X-inactivation reveals epigenetic anomalies in most hESC but identifies sublines that initiate as expected. J. Cell. Physiol. 2008, 216:445-452.
12. Hoffman L.M., Hall L., Batten J.L., Young H., Pardasani D., Baetge E.E., Lawrence J., Carpenter M.K. X-inactivation status varies in human embryonic stem cell lines. Stem Cells 2005, 23:1468-1478.
13. Hu C., Chen L., Jiang Y., Li Y., Wang S. The effect of fatty acid-CoA ligase 4 on the growth of hepatic cancer cells. Cancer Biol Ther 2008, 7:131-134.
14. Jeon B.G., Coppola G., Perrault S.D., Rho G.J., Betts D.H., King W.A. S-adenosylhomocysteine treatment of adult female fibroblasts alters X-chromosome inactivation and improves in vitro embryo development after somatic cell nuclear transfer. Reproduction 2008, 135:815-828.
15. Kim Y.H., Kim J.H., Choi Y.W., Lim S.K., Yim H., Kang S.Y., Chung Y.S., Lee G.Y., Park T.J. Gankyrin is frequently overexpressed in breast cancer and is associated with ErbB2 expression. Exp. Mol. Pathol. 2012, 94:360-365.
16. Lengner C.J., Gimelbrant A.A., Erwin J.A., Cheng A.W., Guenther M.G., Welstead G.G., Alagappan R., Frampton G.M., Xu P., Muffat J., Santagata S., Powers D., Barrett C.B., Young R.A., Lee J.T., Jaenisch R., Mitalipova M. Derivation of pre-X inactivation human embryonic stem cells under physiological oxygen concentrations. Cell 2010, 141:872-883.
17. Li G., Jin T., Liang H., Tu Y., Zhang W., Gong L., Su Q., Gao G. Skewed X-chromosome inactivation in patients with esophageal carcinoma. Diagn. Pathol. 2013, 8:55.
18. Li G., Su Q., Liu G.Q., Gong L., Zhang W., Zhu S.J., Zhang H.L., Feng Y.M. Skewed X chromosome inactivation of blood cells is associated with early development of lung cancer in females. Oncol. Rep. 2006, 16:859-864.
19. Liao H., Zhang S., Cheng D., Ouyang Q., Lin G., Gu Y., Lu C., Gong F., Lu G. Cytogenetic analysis of human embryos and embryonic stem cells derived from monopronuclear zygotes. J. Assist. Reprod. Genet. 2009, 26:583-589.
20. Lin G., Xie Y.B., OuYang Q., Qian X.B., Xie P.Y., Zhou X.Y., Xiong B., Tan Y.Q., Li W., Deng L.Y., Zhou J., Zhou D., Du L.L., Cheng D.H., Liao Y., Gu Y.F., Zhang S.P., Liu T.C., Sun Y., Lu G.X. HLA-matching potential of an established human embryonic stem cell bank in China. Cell Stem Cell 2009, 5:461-465.
21. Lyon M.F. Gene action in X-chromosome of mouse (Mus musculus L). Nature 1961, 190:372.
22. Meng Y., He L., Guo X., Tang S., Zhao X., Du R., Jin J., Bi Q., Li H., Nie Y., Liu J., Fan D. Gankyrin promotes the proliferation of human pancreatic cancer. Cancer Lett. 2010, 297:9-17.
23. Miyazaki I., Simizu S., Okumura H., Takagi S., Osada H. A small-molecule inhibitor shows that pirin regulates migration of melanoma cells. Nat. Chem. Biol. 2010, 6:667-673.
24. Morishima A., Grumbach M.M., Taylor J.H. Asynchronous duplication of human chromosomes and the origin of sex chromatin. Proc. Natl. Acad. Sci. U. S. A. 1962, 48:756-763.
25. Nichols J., Smith A. Naive and primed pluripotent states. Cell Stem Cell 2009, 4:487-492.
26. Penny G.D., Kay G.F., Sheardown S.A., Rastan S., Brockdorff N. Requirement for Xist in X chromosome inactivation. Nature 1996, 379:131-137.
27. Plath K., Fang J., Mlynarczyk-Evans S.K., Cao R., Worringer K.A., Wang H.B., de la Cruz C.C., Otte A.P., Panning B., Zhang Y. Role of histone H3 lysine 27 methylation in X inactivation. Science 2003, 300:131-135.
28. Richardson A.L., Wang Z.C., De Nicolo A., Lu X., Brown M., Miron A., Liao X., Iglehart J.D., Livingston D.M., Ganesan S. X chromosomal abnormalities in basal-like human breast cancer. Cancer Cell 2006, 9:121-132.
29. Rugg-Gunn P.J., Ferguson-Smith A.C., Pedersen R.A. 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-R251.
30. Shen Y., Matsuno Y., Fouse S.D., Rao N., Root S., Xu R.H., Pellegrini M., Riggs A.D., Fan G.P. X-inactivation 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.
31. Silva S.S., Rowntree R.K., Mekhoubad S., Lee J.T. X-chromosome inactivation and epigenetic fluidity in human embryonic stem cells. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:4820-4825.
32. Song K., Li Q., Peng Y.B., Li J., Ding K., Chen L.J., Shao C.H., Zhang L.J., Li P. Silencing of hHS6ST2 inhibits progression of pancreatic cancer through inhibition of Notch signalling. Biochem. J. 2011, 436:271-282.
33. Spits C., Mateizel I., Geens M., Mertzanidou A., Staessen C., Vandeskelde Y., Van der Elst J., Liebaers I., Sermon K. Recurrent chromosomal abnormalities in human embryonic stem cells. Nat. Biotechnol. 2008, 26:1361-1363.
34. Talebizadeh Z., Bittel D.C., Veatch O.J., Kibiryeva N., Butler M.G. Brief report: non-random X chromosome inactivation in females with autism. J. Autism Dev. Disord. 2005, 35:675-681.
35. Tesar P.J., Chenoweth J.G., Brook F.A., Davies T.J., Evans E.P., Mack D.L., Gardner R.L., McKay R.D. New cell lines from mouse epiblast share defining features with human embryonic stem cells. Nature 2007, 448:196-199.
36. Thomson J.A., Itskovitz-Eldor J., Shapiro S.S., Waknitz M.A., Swiergiel J.J., Marshall V.S., Jones J.M. Embryonic stem cell lines derived from human blastocysts. Science 1998, 282:1145-1147.
37. Vincenzo Calvanese A.H., Hmadcha A. Cancer genes hypermethylated in human embryonic stem cells. PLoS One 2008, 3.
38. Xie P., Sun Y., Ouyang Q., Hu L., Tan Y., Zhou X., Xiong B., Zhang Q., Yuan D., Pan Y., Liu T., Liang P., Lu G., Lin G. Physiological oxygen prevents frequent silencing of the DLK1-DIO3 cluster during human embryonic stem cells culture. Stem Cells 2014, 32:391-401.