Human Naive Pluripotent Stem Cells Model X Chromosome Dampening and X Inactivation

Cell Stem Cell

Volumn 20, Issue 1, 2017, Pages 87-101

  Sahakyan, Anna ^a,b   Kim, Rachel ^b   Chronis, Constantinos ^a   Sabri, Shan ^a,b   Bonora, Giancarlo ^a,b   Theunissen, Thorold W ^c   Kuoy, Edward ^a   Langerman, Justin ^a   Clark, Amander T ^a,b   Jaenisch, Rudolf ^c,d   Plath, Kathrin ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^d MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

embryonic stem cells; human development; human stem cells; lncRNA; naive pluripotency; pluripotent stem cells; X chromosome; X chromosome dampening; X chromosome inactivation; XIST

Indexed keywords

GENOMIC DNA; HISTONE LYSINE METHYLTRANSFERASE; HISTONE LYSINE METHYLTRANSFERASE H3K27ME3; RNA; UNCLASSIFIED DRUG; XIST RNA; HISTONE; LONG UNTRANSLATED RNA; LYSINE; XIST NON-CODING RNA;

ALLELE; ARTICLE; BLASTOCYST; CELL DIFFERENTIATION; CHROMOSOMES AND CHROMOSOMAL PHENOMENA; CONTROLLED STUDY; DNA METHYLATION; EMBRYO CELL; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION; HISTONE MODIFICATION; HUMAN; HUMAN CELL; HUMAN DEVELOPMENT; HUMAN EMBRYONIC STEM CELL; NUCLEOTIDE SEQUENCE; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; STEM CELL CULTURE; STEM CELL RESEARCH; X CHROMOSOME DAMPENING; X CHROMOSOME INACTIVATION; CELL CULTURE; CYTOLOGY; GENETICS; METABOLISM; METHYLATION; X CHROMOSOME;

BASE SEQUENCE; BLASTOCYST; CELL DIFFERENTIATION; CELLS, CULTURED; CHROMOSOMES, HUMAN, X; DNA METHYLATION; FEMALE; HISTONES; HUMAN EMBRYONIC STEM CELLS; HUMANS; LYSINE; METHYLATION; PLURIPOTENT STEM CELLS; RNA, LONG NONCODING; X CHROMOSOME INACTIVATION;

EID: 85008418011     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2016.10.006     Document Type: Article

References (30)

1. Balaton, B.P., Cotton, A.M., Brown, C.J., Derivation of consensus inactivation status for X-linked genes from genome-wide studies. Biol. Sex Differ., 6, 2015, 35.
2. Chan, Y.-S., Göke, J., Ng, J.-H., Lu, X., Gonzales, K.A.U., Tan, C.-P., Tng, W.-Q., Hong, Z.-Z., Lim, Y.-S., Ng, H.-H., Induction of a human pluripotent state with distinct regulatory circuitry that resembles preimplantation epiblast. Cell Stem Cell 13 (2013), 663–675.
3. Davidson, K.C., Mason, E.A., Pera, M.F., The pluripotent state in mouse and human. Development 142 (2015), 3090–3099.
4. Gafni, O., Weinberger, L., Mansour, A.A., Manor, Y.S., Chomsky, E., Ben-Yosef, D., Kalma, Y., Viukov, S., Maza, I., Zviran, A., et al. Derivation of novel human ground state naive pluripotent stem cells. Nature 504 (2013), 282–286.
5. Hanna, J., Cheng, A.W., Saha, K., Kim, J., Lengner, C.J., Soldner, F., Cassady, J.P., Muffat, J., Carey, B.W., Jaenisch, R., Human embryonic stem cells with biological and epigenetic characteristics similar to those of mouse ESCs. Proc. Natl. Acad. Sci. USA 107 (2010), 9222–9227.
6. Huang, K., Maruyama, T., Fan, G., The naive state of human pluripotent stem cells: a synthesis of stem cell and preimplantation embryo transcriptome analyses. Cell Stem Cell 15 (2014), 410–415.
7. Lee, S.S., Wan, M., Francke, U., Spectrum of MECP2 mutations in Rett syndrome. Brain Dev. 23:Suppl 1 (2001), S138–S143.
8. Meissner, A., Gnirke, A., Bell, G.W., Ramsahoye, B., Lander, E.S., Jaenisch, R., Reduced representation bisulfite sequencing for comparative high-resolution DNA methylation analysis. Nucleic Acids Res. 33 (2005), 5868–5877.
9. Mekhoubad, S., Bock, C., de Boer, A.S., Kiskinis, E., Meissner, A., Eggan, K., Erosion of dosage compensation impacts human iPSC disease modeling. Cell Stem Cell 10 (2012), 595–609.
10. Minkovsky, A., Patel, S., Plath, K., Concise review: pluripotency and the transcriptional inactivation of the female Mammalian X chromosome. Stem Cells 30 (2012), 48–54.
11. Nazor, K.L., Altun, G., Lynch, C., Tran, H., Harness, J.V., Slavin, I., Garitaonandia, I., Müller, F.-J., Wang, Y.-C., Boscolo, F.S., et al. Recurrent variations in DNA methylation in human pluripotent stem cells and their differentiated derivatives. Cell Stem Cell 10 (2012), 620–634.
12. Nichols, J., Smith, A., Naive and primed pluripotent states. Cell Stem Cell 4 (2009), 487–492.
13. Okamoto, I., Patrat, C., Thépot, D., Peynot, N., Fauque, P., Daniel, N., Diabangouaya, P., Wolf, J.-P., Renard, J.-P., Duranthon, V., Heard, E., Eutherian mammals use diverse strategies to initiate X-chromosome inactivation during development. Nature 472 (2011), 370–374.
14. Pastor, W.A., Chen, D., Liu, W., Kim, R., Sahakyan, A., Lukianchikov, A., Plath, K., Jacobsen, S.E., Clark, A.T., Naive human pluripotent cells feature a methylation landscape devoid of blastocyst or germline memory. Cell Stem Cell 18 (2016), 323–329.
15. Patel, S., Bonora, G., Sahakyan, A., Kim, R., Chronis, C., Langerman, J., Fitz-Gibbon, S., Rubbi, L., Skelton, R.J.P., Ardehali, R., et al. Human embryonic stem cells do not change their X-inactivation status during differentiation. Cell Reports, 18, 2016, 10.1016/j.celrep.2016.11.054 in press. Published online December 15, 2016.
16. Petropoulos, S., Edsgärd, D., Reinius, B., Deng, Q., Panula, S.P., Codeluppi, S., Plaza Reyes, A., Linnarsson, S., Sandberg, R., Lanner, F., Single-cell RNA-seq reveals lineage and X chromosome dynamics in human preimplantation embryos. Cell 165 (2016), 1012–1026.
17. Plath, K., Fang, J., Mlynarczyk-Evans, S.K., Cao, R., Worringer, K.A., Wang, H., de la Cruz, C.C., Otte, A.P., Panning, B., Zhang, Y., Role of histone H3 lysine 27 methylation in X inactivation. Science 300 (2003), 131–135.
18. Sahakyan, A., Plath, K., Transcriptome encyclopedia of early human development. Cell 165 (2016), 777–779.
19. Schulz, E.G., Heard, E., Role and control of X chromosome dosage in mammalian development. Curr. Opin. Genet. Dev. 23 (2013), 109–115.
20. Sharp, A.J., Stathaki, E., Migliavacca, E., Brahmachary, M., Montgomery, S.B., Dupre, Y., Antonarakis, S.E., DNA methylation profiles of human active and inactive X chromosomes. Genome Res. 21 (2011), 1592–1600.
21. Shen, Y., Matsuno, Y., Fouse, S.D., Rao, N., Root, S., Xu, R., Pellegrini, M., Riggs, A.D., Fan, G., X-inactivation in female human embryonic stem cells is in a nonrandom pattern and prone to epigenetic alterations. Proc. Natl. Acad. Sci. USA 105 (2008), 4709–4714.
22. 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. USA 105 (2008), 4820–4825.
23. Smith, Z.D., Chan, M.M., Humm, K.C., Karnik, R., Mekhoubad, S., Regev, A., Eggan, K., Meissner, A., DNA methylation dynamics of the human preimplantation embryo. Nature 511 (2014), 611–615.
24. Takashima, Y., Guo, G., Loos, R., Nichols, J., Ficz, G., Krueger, F., Oxley, D., Santos, F., Clarke, J., Mansfield, W., et al. Resetting transcription factor control circuitry toward ground-state pluripotency in human. Cell 158 (2014), 1254–1269.
25. Tchieu, J., Kuoy, E., Chin, M.H., Trinh, H., Patterson, M., Sherman, S.P., Aimiuwu, O., Lindgren, A., Hakimian, S., Zack, J.A., et al. Female human iPSCs retain an inactive X chromosome. Cell Stem Cell 7 (2010), 329–342.
26. Theunissen, T.W., Powell, B.E., Wang, H., Mitalipova, M., Faddah, D.A., Reddy, J., Fan, Z.P., Maetzel, D., Ganz, K., Shi, L., et al. Systematic identification of culture conditions for induction and maintenance of naive human pluripotency. Cell Stem Cell 15 (2014), 471–487.
27. Theunissen, T.W., Friedli, M., He, Y., Planet, E., O'Neil, R.C., Markoulaki, S., Pontis, J., Wang, H., Iouranova, A., Imbeault, M., et al. Molecular criteria for defining the naive human pluripotent state. Cell Stem Cell 19 (2016), 502–515.
28. Vallot, C., Ouimette, J.-F., Makhlouf, M., Féraud, O., Pontis, J., Côme, J., Martinat, C., Bennaceur-Griscelli, A., Lalande, M., Rougeulle, C., Erosion of X chromosome inactivation in human pluripotent cells initiates with XACT coating and depends on a specific heterochromatin landscape. Cell Stem Cell 16 (2015), 533–546.
29. Ware, C.B., Nelson, A.M., Mecham, B., Hesson, J., Zhou, W., Jonlin, E.C., Jimenez-Caliani, A.J., Deng, X., Cavanaugh, C., Cook, S., et al. Derivation of naive human embryonic stem cells. Proc. Natl. Acad. Sci. USA 111 (2014), 4484–4489.
30. Yan, L., Yang, M., Guo, H., Yang, L., Wu, J., Li, R., Liu, P., Lian, Y., Zheng, X., Yan, J., et al. Single-cell RNA-seq profiling of human preimplantation embryos and embryonic stem cells. Nat. Struct. Mol. Biol. 20 (2013), 1131–1139.