Small RNA changes en route to distinct cellular states of induced pluripotency

Jennifer L. Clancy; Hardip R. Patel; Samer M.I. Hussein; Peter D. Tonge; Nicole Cloonan; Andrew J. Corso; Mira Li; Dong Sung Lee; Jong Yeon Shin; Justin J.L. Wong; Charles G. Bailey; Marco Benevento; Javier Munoz; Aaron Chuah; David Wood; John E.J. Rasko; Albert J.R. Heck; Sean M. Grimmond; Ian M. Rogers; Jeong Sun Seo; Christine A. Wells; Mira C. Puri; Andras Nagy; Thomas Preiss

doi:10.1038/ncomms6522

Small RNA changes en route to distinct cellular states of induced pluripotency

Jennifer L. Clancy, Hardip R. Patel, Samer M.I. Hussein, Peter D. Tonge, Nicole Cloonan, Andrew J. Corso, Mira Li, Dong Sung Lee, Jong Yeon Shin, Justin J.L. Wong, Charles G. Bailey, Marco Benevento, Javier Munoz, Aaron Chuah, David Wood, John E.J. Rasko, Albert J.R. Heck, Sean M. Grimmond, Ian M. Rogers, Jeong Sun SeoChristine A. Wells, Mira C. Puri, Andras Nagy, Thomas Preiss^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

50 Citations (Scopus)

Abstract

MicroRNAs (miRNAs) are critical to somatic cell reprogramming into induced pluripotent stem cells (iPSCs), however, exactly how miRNA expression changes support the transition to pluripotency requires further investigation. Here we use a murine secondary reprogramming system to sample cellular trajectories towards iPSCs or a novel pluripotent 'F-class' state and perform small RNA sequencing. We detect sweeping changes in an early and a late wave, revealing that distinct miRNA milieus characterize alternate states of pluripotency. miRNA isoform expression is common but surprisingly varies little between cell states. Referencing other omic data sets generated in parallel, we find that miRNA expression is changed through transcriptional and post-transcriptional mechanisms. miRNA transcription is commonly regulated by dynamic histone modification, while DNA methylation/demethylation consolidates these changes at multiple loci. Importantly, our results suggest that a novel subset of distinctly expressed miRNAs supports pluripotency in the F-class state, substituting for miRNAs that serve such roles in iPSCs.

Original language	English
Article number	5522
Journal	Nature Communications
Volume	5
DOIs	https://doi.org/10.1038/ncomms6522
Publication status	Published - 2014

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Clancy, J. L., Patel, H. R., Hussein, S. M. I., Tonge, P. D., Cloonan, N., Corso, A. J., Li, M., Lee, D. S., Shin, J. Y., Wong, J. J. L., Bailey, C. G., Benevento, M., Munoz, J., Chuah, A., Wood, D., Rasko, J. E. J., Heck, A. J. R., Grimmond, S. M., Rogers, I. M., ... Preiss, T. (2014). Small RNA changes en route to distinct cellular states of induced pluripotency. Nature Communications, 5, Article 5522. https://doi.org/10.1038/ncomms6522

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title = "Small RNA changes en route to distinct cellular states of induced pluripotency",

abstract = "MicroRNAs (miRNAs) are critical to somatic cell reprogramming into induced pluripotent stem cells (iPSCs), however, exactly how miRNA expression changes support the transition to pluripotency requires further investigation. Here we use a murine secondary reprogramming system to sample cellular trajectories towards iPSCs or a novel pluripotent 'F-class' state and perform small RNA sequencing. We detect sweeping changes in an early and a late wave, revealing that distinct miRNA milieus characterize alternate states of pluripotency. miRNA isoform expression is common but surprisingly varies little between cell states. Referencing other omic data sets generated in parallel, we find that miRNA expression is changed through transcriptional and post-transcriptional mechanisms. miRNA transcription is commonly regulated by dynamic histone modification, while DNA methylation/demethylation consolidates these changes at multiple loci. Importantly, our results suggest that a novel subset of distinctly expressed miRNAs supports pluripotency in the F-class state, substituting for miRNAs that serve such roles in iPSCs.",

author = "Clancy, {Jennifer L.} and Patel, {Hardip R.} and Hussein, {Samer M.I.} and Tonge, {Peter D.} and Nicole Cloonan and Corso, {Andrew J.} and Mira Li and Lee, {Dong Sung} and Shin, {Jong Yeon} and Wong, {Justin J.L.} and Bailey, {Charles G.} and Marco Benevento and Javier Munoz and Aaron Chuah and David Wood and Rasko, {John E.J.} and Heck, {Albert J.R.} and Grimmond, {Sean M.} and Rogers, {Ian M.} and Seo, {Jeong Sun} and Wells, {Christine A.} and Puri, {Mira C.} and Andras Nagy and Thomas Preiss",

year = "2014",

doi = "10.1038/ncomms6522",

language = "English",

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journal = "Nature Communications",

issn = "2041-1723",

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Clancy, JL, Patel, HR, Hussein, SMI, Tonge, PD, Cloonan, N, Corso, AJ, Li, M, Lee, DS, Shin, JY, Wong, JJL, Bailey, CG, Benevento, M, Munoz, J, Chuah, A, Wood, D, Rasko, JEJ, Heck, AJR, Grimmond, SM, Rogers, IM, Seo, JS, Wells, CA, Puri, MC, Nagy, A & Preiss, T 2014, 'Small RNA changes en route to distinct cellular states of induced pluripotency', Nature Communications, vol. 5, 5522. https://doi.org/10.1038/ncomms6522

TY - JOUR

T1 - Small RNA changes en route to distinct cellular states of induced pluripotency

AU - Clancy, Jennifer L.

AU - Patel, Hardip R.

AU - Hussein, Samer M.I.

AU - Tonge, Peter D.

AU - Cloonan, Nicole

AU - Corso, Andrew J.

AU - Li, Mira

AU - Lee, Dong Sung

AU - Shin, Jong Yeon

AU - Wong, Justin J.L.

AU - Bailey, Charles G.

AU - Benevento, Marco

AU - Munoz, Javier

AU - Chuah, Aaron

AU - Wood, David

AU - Rasko, John E.J.

AU - Heck, Albert J.R.

AU - Grimmond, Sean M.

AU - Rogers, Ian M.

AU - Seo, Jeong Sun

AU - Wells, Christine A.

AU - Puri, Mira C.

AU - Nagy, Andras

AU - Preiss, Thomas

PY - 2014

Y1 - 2014

N2 - MicroRNAs (miRNAs) are critical to somatic cell reprogramming into induced pluripotent stem cells (iPSCs), however, exactly how miRNA expression changes support the transition to pluripotency requires further investigation. Here we use a murine secondary reprogramming system to sample cellular trajectories towards iPSCs or a novel pluripotent 'F-class' state and perform small RNA sequencing. We detect sweeping changes in an early and a late wave, revealing that distinct miRNA milieus characterize alternate states of pluripotency. miRNA isoform expression is common but surprisingly varies little between cell states. Referencing other omic data sets generated in parallel, we find that miRNA expression is changed through transcriptional and post-transcriptional mechanisms. miRNA transcription is commonly regulated by dynamic histone modification, while DNA methylation/demethylation consolidates these changes at multiple loci. Importantly, our results suggest that a novel subset of distinctly expressed miRNAs supports pluripotency in the F-class state, substituting for miRNAs that serve such roles in iPSCs.

AB - MicroRNAs (miRNAs) are critical to somatic cell reprogramming into induced pluripotent stem cells (iPSCs), however, exactly how miRNA expression changes support the transition to pluripotency requires further investigation. Here we use a murine secondary reprogramming system to sample cellular trajectories towards iPSCs or a novel pluripotent 'F-class' state and perform small RNA sequencing. We detect sweeping changes in an early and a late wave, revealing that distinct miRNA milieus characterize alternate states of pluripotency. miRNA isoform expression is common but surprisingly varies little between cell states. Referencing other omic data sets generated in parallel, we find that miRNA expression is changed through transcriptional and post-transcriptional mechanisms. miRNA transcription is commonly regulated by dynamic histone modification, while DNA methylation/demethylation consolidates these changes at multiple loci. Importantly, our results suggest that a novel subset of distinctly expressed miRNAs supports pluripotency in the F-class state, substituting for miRNAs that serve such roles in iPSCs.

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U2 - 10.1038/ncomms6522

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M3 - Article

SN - 2041-1723

VL - 5

JO - Nature Communications

JF - Nature Communications

M1 - 5522

ER -

Small RNA changes en route to distinct cellular states of induced pluripotency

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