Sage Journals: Discover world-class research

Abstract

The mechanisms of nuclear reprogramming following somatic cell nuclear transfer (SCNT) to enucleated oocytes or factor-based reprogramming are poorly understood. In this study global transcriptional analysis was performed on a number of different rhesus monkey (Macaca mulatta) cell and tissue samples, including rhesus-induced pluripotent stem cells (IPSCs) and rhesus SCNT-derived embryonic stem cells (SCNT-ESCs). Global transcriptional cluster analysis and stem cell-specific gene expression analysis both suggested that the oocyte-reprogrammed SCNT-ESCs were transcriptionally closer to the control fertilized ESCs than IPSCs. These results, combined with previous epigenetic analysis studies in the mouse, reinforce the hypothesis that oocyte-reprogrammed cell nuclei are more completely reprogrammed to an ESC state than IPSCs. Transcriptional analysis of rhesus oocytes detected over 500 ESC-specific genes, including OCT3/4, NR5A2, and DNMT3B. These results, combined with previously published reprogramming research, were used as the basis for a general model to explain the mechanisms of nuclear reprogramming.

Get full access to this article

View all access options for this article.

References

Anokye-Danso

, Trivedi

C.M.

, Juhr

et al. 2011. Highly efficient miRNA-mediated reprogramming of mouse and human somatic cells to pluripotency. Cell Stem Cell, 8:376–388.

Bhutani

, Brady

J.J.

, Damian

et al. 2010. Reprogramming towards pluripotency requires AID-dependent DNA demethylation. Nature, 463:1042–1047.

Boland

M.J.

, Hazen

J.L.

, Nazor

K.L.

et al. 2009. Adult mice generated from induced pluripotent stem cells. Nature, 461:91–94.

Boyer

L.A.

, Lee

T.I.

, Cole

M.F.

et al. 2005. Core transcriptional regulatory circuitry in human embryonic stem cells. Cell, 122:947–956.

Byrne

J.A.

2008. Generation of isogenic pluripotent stem cells. Hum. Mol. Genet., 17:R37–R41.

Byrne

J.A.

, Pedersen

D.A.

, Clepper

L.L.

et al. 2007. Producing primate embryonic stem cells by somatic cell nuclear transfer. Nature, 450:497–502.

Card

D.A.

, Hebbar

P.B.

, Li

et al. 2008. Oct4/Sox2-regulated miR-302 targets cyclin D1 in human embryonic stem cells. Mol. Cell. Biol., 28:6426–6438.

Chin

M.H.

, Pellegrini

, Plath

et al. 2010. Molecular analyses of human induced pluripotent stem cells and embryonic stem cells. Cell Stem Cell, 7:263–269.

Cowan

C.A.

, Atienza

, Melton

D.A.

et al. 2005. Nuclear reprogramming of somatic cells after fusion with human embryonic stem cells. Science, 309:1369–1373.

10.

Ding

, Guo

, Liu

et al. 2009. Embryonic stem cells derived from somatic cloned and fertilized blastocysts are post-transcriptionally indistinguishable: a MicroRNA and protein profile comparison. Proteomics, 9:2711–2721.

11.

Duan

, Pauley

M.A.

, Spindel

E.R.

et al. 2010. Large scale analysis of positional effects of single-base mismatches on microarray gene expression data. BioData Min., 3:2.

12.

French

A.J.

, Adams

C.A.

, Anderson

L.S.

et al. 2008. Development of human cloned blastocysts following somatic cell nuclear transfer with adult fibroblasts. Stem Cells, 26:485–493.

13.

Gurdon

J.B.

1962. The developmental capacity of nuclei taken from intestinal epithelium cells of feeding tadpoles. J. Embryol. Exp. Morphol., 10:622–640.

14.

Hanna

, Saha

, Pando

et al. 2009. Direct cell reprogramming is a stochastic process amenable to acceleration. Nature, 462:595–601.

15.

Harvey

A.J.

, Armant

D.R.

, Bavister

et al. 2009. Inner cell mass localization of NANOG precedes OCT3/4 in rhesus monkey blastocysts. Stem Cells Dev., 18:1451–1458.

16.

Heng

J.C.

, Feng

, Han

et al. 2010. The nuclear receptor Nr5a2 can replace Oct4 in the reprogramming of murine somatic cells to pluripotent cells. Cell Stem Cell, 6:167–174.

17.

Kim

, Doi

, Wen

et al. 2010. Epigenetic memory in induced pluripotent stem cells. Nature, 467:285–290.

18.

Krek

, Grun

, Poy

M.N.

et al. 2005. Combinatorial microRNA target predictions. Nat. Genet., 37:495–500.

19.

Kuroda

, Tada

, Kubota

et al. 2005. Octamer and Sox elements are required for transcriptional cis regulation of Nanog gene expression. Mol. Cell. Biol., 25:2475–2485.

20.

Lee

Y.S.

, Latham

K.E.

, Vandevoort

C.A.

2008. Effects of in vitro maturation on gene expression in rhesus monkey oocytes. Physiol. Genomics, 35:145–158.

21.

Lin

S.L.

, Chang

D.C.

, Lin

C.H.

et al. 2011. Regulation of somatic cell reprogramming through inducible mir-302 expression. Nucleic Acids Res., 39:1054–1065.

22.

Liu

, Zhu

, Yong

et al. 2008. Generation of induced pluripotent stem cells from adult rhesus monkey fibroblasts. Cell Stem Cell, 3:587–590.

23.

Loh

Y.H.

, Wu

, Chew

J.L.

et al. 2006. The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells. Nat. Genet., 38:431–440.

24.

Loh

Y.H.

, Zhang

, Chen

et al. 2007. Jmjd1a and Jmjd2c histone H3 Lys 9 demethylases regulate self-renewal in embryonic stem cells. Genes Dev., 21:2545–2557.

25.

Marson

, Levine

S.S.

, Cole

M.F.

et al. 2008. Connecting microRNA genes to the core transcriptional regulatory circuitry of embryonic stem cells. Cell, 134:521–533.

26.

Mikkelsen

T.S.

, Hanna

, Zhang

et al. 2008. Dissecting direct reprogramming through integrative genomic analysis. Nature, 454:49–55.

27.

Mitalipov

, Kuo

H.C.

, Byrne

et al. 2006. Isolation and characterization of novel rhesus monkey embryonic stem cell lines. Stem Cells, 24:2177–2186.

28.

Mitalipov

S.M.

, Zhou

, Byrne

J.A.

et al. 2007. Reprogramming following somatic cell nuclear transfer in primates is dependent upon nuclear remodeling. Hum. Reprod., 22:2232–2242.

29.

Okumura-Nakanishi

, Saito

, Niwa

et al. 2005. Oct-3/4 and Sox2 regulate Oct-3/4 gene in embryonic stem cells. J. Biol. Chem., 280:5307–5317.

30.

Santos

, Hendrich

, Reik

et al. 2002. Dynamic reprogramming of DNA methylation in the early mouse embryo. Dev. Biol., 241:172–182.

31.

Stojkovic

, Stojkovic

, Leary

et al. 2005. Derivation of a human blastocyst after heterologous nuclear transfer to donated oocytes. Reprod. Biomed. Online, 11:226–231.

32.

Tabar

, Tomishima

, Panagiotakos

et al. 2008. Therapeutic cloning in individual parkinsonian mice. Nat. Med., 14:379–381.

33.

Takahashi

, Yamanaka

2006. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell, 126:663–676.

34.

Takahashi

, Tanabe

, Ohnuki

et al. 2007. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell, 131:861–872.

35.

Wilmut

, Schnieke

A.E.

, McWhir

et al. 1997. Viable offspring derived from fetal and adult mammalian cells. Nature, 385:810–813.

36.

Yuan

, Wan

, Zhao

et al. 2011. Combined chemical treatment enables Oct4-induced reprogramming from mouse embryonic fibroblasts. Stem Cells, 29:549–553.

37.

Zhao

, Zhang

Z.-N.

, Rong

et al. 2011. Immunogenicity of induced pluripotent stem cells. Nature, 474:212–215.

38.

Zhao

X.Y.

, Li

, Lv

et al. 2009. iPS cells produce viable mice through tetraploid complementation. Nature, 461:86–90.

Supplementary Material

Please find the following supplemental material available below.

For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.

For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.

0.00 MB

5.72 MB

Global Transcriptional Analysis of Oocyte-Based and Factor-Based Nuclear Reprogramming in the Nonhuman Primate

Abstract

Abstract

Get full access to this article

References

Supplementary Material