Direct Comparison of Distinct Naive Pluripotent States in Human Embryonic Stem Cells

Overview

Journal Nat Commun

Specialty Biology

Date 2017 Apr 22

PMID 28429706

Citations 34

Authors

S Warrier

M Van der Jeught

G Duggal

L Tilleman

E Sutherland

J Taelman

M Popovic

S Lierman

S Chuva De Sousa Lopes

A Van Soom

L Peelman

F Van Nieuwerburgh

D I M De Coninck

B Menten

P Mestdagh

J Van de Sompele

D Deforce

P De Sutter

B Heindryckx

Affiliations

Soon will be listed here.

Abstract

Until recently, human embryonic stem cells (hESCs) were shown to exist in a state of primed pluripotency, while mouse embryonic stem cells (mESCs) display a naive or primed pluripotent state. Here we show the rapid conversion of in-house-derived primed hESCs on mouse embryonic feeder layer (MEF) to a naive state within 5-6 days in naive conversion media (NCM-MEF), 6-10 days in naive human stem cell media (NHSM-MEF) and 14-20 days using the reverse-toggle protocol (RT-MEF). We further observe enhanced unbiased lineage-specific differentiation potential of naive hESCs converted in NCM-MEF, however, all naive hESCs fail to differentiate towards functional cell types. RNA-seq analysis reveals a divergent role of PI3K/AKT/mTORC signalling, specifically of the mTORC2 subunit, in the different naive hESCs. Overall, we demonstrate a direct evaluation of several naive culture conditions performed in the same laboratory, thereby contributing to an unbiased, more in-depth understanding of different naive hESCs.

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References

Ware C, Nelson A, Mecham B, Hesson J, Zhou W, Jonlin E . Derivation of naive human embryonic stem cells. Proc Natl Acad Sci U S A. 2014; 111(12):4484-9. PMC: 3970494. DOI: 10.1073/pnas.1319738111. View

Honda A, Hatori M, Hirose M, Honda C, Izu H, Inoue K . Naive-like conversion overcomes the limited differentiation capacity of induced pluripotent stem cells. J Biol Chem. 2013; 288(36):26157-26166. PMC: 3764818. DOI: 10.1074/jbc.M113.502492. View

Luo W, Brouwer C . Pathview: an R/Bioconductor package for pathway-based data integration and visualization. Bioinformatics. 2013; 29(14):1830-1. PMC: 3702256. DOI: 10.1093/bioinformatics/btt285. View

Subramanian A, Tamayo P, Mootha V, Mukherjee S, Ebert B, Gillette M . Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A. 2005; 102(43):15545-50. PMC: 1239896. DOI: 10.1073/pnas.0506580102. View

Takashima Y, Guo G, Loos R, Nichols J, Ficz G, Krueger F . Resetting transcription factor control circuitry toward ground-state pluripotency in human. Cell. 2014; 158(6):1254-1269. PMC: 4162745. DOI: 10.1016/j.cell.2014.08.029. View

Luo W, Friedman M, Shedden K, Hankenson K, Woolf P . GAGE: generally applicable gene set enrichment for pathway analysis. BMC Bioinformatics. 2009; 10:161. PMC: 2696452. DOI: 10.1186/1471-2105-10-161. View

Liu Y, Liu H, Sauvey C, Yao L, Zarnowska E, Zhang S . Directed differentiation of forebrain GABA interneurons from human pluripotent stem cells. Nat Protoc. 2013; 8(9):1670-9. PMC: 4121169. DOI: 10.1038/nprot.2013.106. View

Robinson M, McCarthy D, Smyth G . edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2009; 26(1):139-40. PMC: 2796818. DOI: 10.1093/bioinformatics/btp616. View

Leitch H, McEwen K, Turp A, Encheva V, Carroll T, Grabole N . Naive pluripotency is associated with global DNA hypomethylation. Nat Struct Mol Biol. 2013; 20(3):311-6. PMC: 3591483. DOI: 10.1038/nsmb.2510. View

10.

Theunissen T, Powell B, Wang H, Mitalipova M, Faddah D, Reddy J . Systematic identification of culture conditions for induction and maintenance of naive human pluripotency. Cell Stem Cell. 2014; 15(4):471-487. PMC: 4184977. DOI: 10.1016/j.stem.2014.07.002. View

11.

Thomson J, Itskovitz-Eldor J, Shapiro S, Waknitz M, Swiergiel J, Marshall V . Embryonic stem cell lines derived from human blastocysts. Science. 1998; 282(5391):1145-7. DOI: 10.1126/science.282.5391.1145. View

12.

Grabole N, Tischler J, Hackett J, Kim S, Tang F, Leitch H . Prdm14 promotes germline fate and naive pluripotency by repressing FGF signalling and DNA methylation. EMBO Rep. 2013; 14(7):629-37. PMC: 3701237. DOI: 10.1038/embor.2013.67. View

13.

Nichols J, Smith A . The origin and identity of embryonic stem cells. Development. 2010; 138(1):3-8. DOI: 10.1242/dev.050831. View

14.

Maiese K . Stem cell guidance through the mechanistic target of rapamycin. World J Stem Cells. 2015; 7(7):999-1009. PMC: 4550632. DOI: 10.4252/wjsc.v7.i7.999. View

15.

Folmes C, Terzic A . Metabolic determinants of embryonic development and stem cell fate. Reprod Fertil Dev. 2014; 27(1):82-8. PMC: 4444364. DOI: 10.1071/RD14383. View

16.

Duggal G, Warrier S, Ghimire S, Broekaert D, van der Jeught M, Lierman S . Alternative Routes to Induce Naïve Pluripotency in Human Embryonic Stem Cells. Stem Cells. 2015; 33(9):2686-98. DOI: 10.1002/stem.2071. View

17.

Pekarsky Y, Koval A, Hallas C, Bichi R, Tresini M, Malstrom S . Tcl1 enhances Akt kinase activity and mediates its nuclear translocation. Proc Natl Acad Sci U S A. 2000; 97(7):3028-33. PMC: 16186. DOI: 10.1073/pnas.97.7.3028. View

18.

Nakaki F, Saitou M . PRDM14: a unique regulator for pluripotency and epigenetic reprogramming. Trends Biochem Sci. 2014; 39(6):289-98. DOI: 10.1016/j.tibs.2014.04.003. View

19.

Irie N, Weinberger L, Tang W, Kobayashi T, Viukov S, Manor Y . SOX17 is a critical specifier of human primordial germ cell fate. Cell. 2014; 160(1-2):253-68. PMC: 4310934. DOI: 10.1016/j.cell.2014.12.013. View

20.

Dalton S . Signaling networks in human pluripotent stem cells. Curr Opin Cell Biol. 2012; 25(2):241-6. PMC: 3570582. DOI: 10.1016/j.ceb.2012.09.005. View