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A Molecular Roadmap of Reprogramming Somatic Cells into iPS Cells
Open accessAbstract
Factor-induced reprogramming of somatic cells into induced pluripotent stem cells (iPSCs) is inefficient, complicating mechanistic studies. Here, we examined defined intermediate cell populations poised to becoming iPSCs by genome-wide analyses. We show that induced pluripotency elicits two transcriptional waves, which are driven by c-Myc/Klf4 (first wave) and Oct4/Sox2/Klf4 (second wave). Cells that become refractory to reprogramming activate the first but fail to initiate the second transcriptional wave and can be rescued by elevated expression of all four factors. The establishment of bivalent domains occurs gradually after the first wave, whereas changes in DNA methylation take place after the second wave when cells acquire stable pluripotency. This integrative analysis allowed us to identify genes that act as roadblocks during reprogramming and surface markers that further enrich for cells prone to forming iPSCs. Collectively, our data offer new mechanistic insights into the nature and sequence of molecular events inherent to cellular reprogramming.
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“Taken together, these two attributes may act as the source of memory for initial cell identity during a time when the somatic transcriptional program is otherwise mostly repressed and somatic proteins such as CD13 are lost (Polo et al., 2012; David and Polo, 2014).”
From Multi-omic rejuvenation of human cells by maturation phase transient reprogramming (2022) · cites this paper as Polo et al., 2012
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“Importantly, we must note that all of the transcriptional remodeling studies utilizing OSKM occupancy data are limited to the events that occur in the beginning (fibroblasts) or end points (pluripotent stem cells), with everything in between still up for interpretation 80,83,85 .”
From Mechanisms, pathways and strategies for rejuvenation through epigenetic reprogramming (2023) · cites this paper as [83]
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“It is worth noting, however, that full reprogramming is relatively inefficient, with ~3% of cells reaching full reprogramming in the first round 83 .”
From Mechanisms, pathways and strategies for rejuvenation through epigenetic reprogramming (2023) · cites this paper as [83]
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“The distinct mechanisms observed among combinations of OCT4 and SOX2 (without KLF4) versus OSK may explain the controversy regarding whether OSK mainly function as the pioneer factors or bind readily open chromatin in early reprogramming, or both 80,82,83,85 .”
From Mechanisms, pathways and strategies for rejuvenation through epigenetic reprogramming (2023) · cites this paper as [83]
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“Cellular reprogramming to pluripotency by forced expression of the Yamanaka factors (Oct4, Sox2, Klf4, and c-Myc [OSKM]) occurs through the global remodeling of epigenetic marks”
From In Vivo Amelioration of Age-Associated Hallmarks by Partial Reprogramming. (2016) · cites this paper as Polo et al., 2012
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“Interestingly, cellular reprogramming to pluripotency occurs through a stepwise global epigenetic remodeling (Benayoun et al., 2015;Liu et al., 2013b;Polo et al., 2012).”
From In Vivo Amelioration of Age-Associated Hallmarks by Partial Reprogramming. (2016) · cites this paper as Polo et al., 2012
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“First, MYC primarily facilitates early gene induction for proliferation, whereas OCT4 and SOX2 induce chromatin opening while also binding readily open chromatin enriched with KLF4 motifs, supporting the notion that KLF4 recruits OCT4 and SOX2 to somatic chromatin that later becomes closed 83 .”
From Mechanisms, pathways and strategies for rejuvenation through epigenetic reprogramming (2023) · cites this paper as [83]
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“Genes associated with cell proliferation, metabolism and cytoskeleton organization were activated first, with developmental genes temporarily downregulated.”
From Mechanisms, pathways and strategies for rejuvenation through epigenetic reprogramming (2023) · cites this paper as [83]
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“It was initially reported in MEFs that transcriptional remodeling occurs in two waves, the first driven by MYC and KLF4 in the first 3 days and the second by OSK (ref.83).”
From Mechanisms, pathways and strategies for rejuvenation through epigenetic reprogramming (2023) · cites this paper as [83]
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“Changes in DNA methylation were initially thought to happen in the late stages of reprogramming 83 , but a recent study revealed that loci near Oct4, Klf4 and Nanog are demethylated earlier and de novo DNA methylation occurs in late reprogramming 85 .”
From Mechanisms, pathways and strategies for rejuvenation through epigenetic reprogramming (2023) · cites this paper as [83]
In the citing paper
“OSKM induction triggers complex cellular changes1–3.”
From In vivo partial reprogramming of myofibers promotes muscle regeneration by remodeling the stem cell niche (2021) · cites this paper as [3]
In the citing paper
“whereas OCT4 and SOX2 induce chromatin opening while also binding readily open chromatin enriched with KLF4 motifs, supporting the notion that KLF4 recruits OCT4 and SOX2 to somatic chromatin that later becomes closed 83 .”
From Mechanisms, pathways and strategies for rejuvenation through epigenetic reprogramming (2023) · cites this paper as [83]
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Metadata
- Authors
- Polo, J. M., Anderssen, E., Walsh, R. M., Schwarz, B. A., Nefzger, C. M., Lim, S. M., Borkent, M., Apostolou, E., Alaei, S., Cloutier, J., Bar-Nur, O., Cheloufi, S., Stadtfeld, M., Figueroa, M. E., Robinton, D., Natesan, S., Melnick, A., Zhu, J., Ramaswamy, S., & Hochedlinger, K.
- Affiliations
- Harvard University (US)
- Broad Institute (US)
- Monash University (AU)
- Weill Cornell Medicine (US)
- National Institutes of Health (US)
- Howard Hughes Medical Institute (US)
- Corresponding author
- Ramaswamy, Sridhar
- Hochedlinger, Konrad
- ORCID
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2012-12
- Volume
- 151
- Issue
- 7
- Pages
- 1617-1632
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC3608203
- OpenAlex
- W2060613703
- Cited by
- 861
- References
- 38
- Citations by year
- 2026: 30 · 2025: 20 · 2024: 37 · 2023: 51 · 2022: 48 · 2021: 47 · 2020: 61 · 2019: 69 · 2018: 63 · 2017: 79 · 2016: 90 · 2015: 83 · 2014: 105 · 2013: 76 · 2012: 1
- FWCI
- 34.04
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 385 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Adelaide Research & Scholarship (AR&S) (University of Adelaide) (submittedVersion)
- Funders
- Howard Hughes Medical Institute
- National Institutes of Health (1dp2od003266-01)
- National Cancer Institute (T32CA009216)
- National Institute of General Medical Sciences (P01GM099117)
- National Institute of Allergy and Infectious Diseases (ZIAAI001169)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01HD058013)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Pluripotent Stem Cells Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- induced pluripotent stem cells, cellular reprogramming, c-Myc, KLF4, Oct4, SOX2, bivalent domains, DNA methylation, cell surface markers, pluripotency
- MeSH terms
- Kruppel-Like Factor 4, Animals, Cytological Techniques, Humans, Transcription Factors, Mice, Genome-Wide Association Study, Induced Pluripotent Stem Cells, Cellular Reprogramming
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