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A p53-mediated DNA damage response limits reprogramming to ensure iPS cell genomic integrity
Open accessAbstract
The reprogramming of differentiated cells to pluripotent cells (induced pluripotent stem (iPS) cells) is known to be an inefficient process. We recently reported that cells with short telomeres cannot be reprogrammed to iPS cells despite their normal proliferation rates, probably reflecting the existence of 'reprogramming barriers' that abort the reprogramming of cells with uncapped telomeres. Here we show that p53 (also known as Trp53 in mice and TP53 in humans) is critically involved in preventing the reprogramming of cells carrying various types of DNA damage, including short telomeres, DNA repair deficiencies, or exogenously inflicted DNA damage. Reprogramming in the presence of pre-existing, but tolerated, DNA damage is aborted by the activation of a DNA damage response and p53-dependent apoptosis. Abrogation of p53 allows efficient reprogramming in the face of DNA damage and the generation of iPS cells carrying persistent DNA damage and chromosomal aberrations. These observations indicate that during reprogramming cells increase their intolerance to different types of DNA damage and that p53 is critical in preventing the generation of human and mouse pluripotent cells from suboptimal parental cells.
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“In agreement with the negative role of prolonged p53 expression on stem cell potency, it was shown that p53 restricted the stem cell gene expression program [69].”
From Ultraviolet Radiation‐Induced Skin Aging: The Role of DNA Damage and Oxidative Stress in Epidermal Stem Cell Damage Mediated Skin Aging (2016) · cites this paper as [69]
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BackgroundBrief Report: Impaired Cell Reprogramming in Nonhomologous End Joining Deficient Cells
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“This is also supported by the fact that the efficiency of reprogramming is higher in a p53 null context [67-71].”
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Suvorova, I. I., Katolikova, N. V., & Pospelov, V. A. (2012) · International review of cytology · doi:10.1016/b978-0-12-394310-1.00004-7 · Cited by 14
Mlody, B., Wruck, W., Martins, S., Sperling, K., & Adjaye, J. (2017) · Scientific Reports · doi:10.1038/s41598-017-07905-2 · Cited by 13
Generation of Parthenogenetic Induced Pluripotent Stem Cells from Parthenogenetic Neural Stem Cells
Tae, J., Joo, J. Y., Han, D., Araúzo-Bravo, M. J., Kim, M. J., Greber, B., Zaehres, H., Sobek-Klocke, I., Chung, H., & Schöler, H. R. (2009) · Stem Cells · doi:10.1002/stem.233 · Cited by 13
Reprogramming somatic cells to pluripotency: A fresh look at Yamanaka’s model
Li, Y., Shen, Z., Shelat, H. S., & Geng, Y. (2013) · Cell Cycle · doi:10.4161/cc.26952 · Cited by 14
Lu, Y., Xu, D., Zhou, J., Ma, Y., Jiang, Y., Zeng, W., & Dai, W. H. (2013) · Journal of Hematology & Oncology · doi:10.1186/1756-8722-6-71 · Cited by 13
“Supporting this notion, p53 levels adversely affect reprogramming iPS cells from somatic cells [27].”
BackgroundA protocol to assess cell cycle and apoptosis in human and mouse pluripotent cells
Edel, M. J., Menchón, C., Vaquero, J. A., & Belmonte, J.-C. I. (2011) · Cell Communication and Signaling · doi:10.1186/1478-811x-9-8 · Cited by 14
“Recently, it has been shown that loss of p53 function can enhance the efficiency of reprogramming, suggesting that the cell cycle is a rate limiting step in the reprogramming process [4-10].”
BackgroundSrivastava, Y., Tan, D. S., Malik, V., Weng, M., Javed, A., Cojocaru, V., Wu, G., Veerapandian, V., Cheung, L. W. T., & Jauch, R. (2019) · FEBS Journal · doi:10.1111/febs.15076 · Cited by 12
Mechanism and Method for Generating Tumor-Free iPS Cells Using Intronic MicroRNA miR-302 Induction
Lin, S.-L., & Ying, S. (2018) · Methods in molecular biology · doi:10.1007/978-1-4939-7601-0_22 · Cited by 13
Helpers of the cellular gatekeeper—miRNAs dance in P53 network
Shi, M., Liu, D., Shen, B., & Guo, N. (2009) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2009.12.001 · Cited by 13
Noise Cancellation: Viral Fine Tuning of the Cellular Environment for Its Own Genome Replication
Sato, Y., & Tsurumi, T. (2010) · PLoS Pathogens · doi:10.1371/journal.ppat.1001158 · Cited by 12
“Interestingly, p53 serves as a negative regulator for reprogramming of somatic cells into induced pluripotent stem (iPS) cells [47,48,49,50,51].”
BackgroundMitochondria and mtDNA integrity in stem cell function and differentiation
Hämäläinen, R. H. (2016) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2016.04.008 · Cited by 13
Zhao, Q., Liu, K., Zhang, L., Li, Z., Wang, L., Cao, J., Xu, Y., Zheng, A., Chen, Q., & Zhao, T. (2022) · Cell Death and Disease · doi:10.1038/s41419-022-05413-4 · Cited by 12
Sharovskaya, Y. Y., Philonenko, E. S., Киселев, С. Л., & Lagarkova, M. A. (2012) · Stem Cells and Development · doi:10.1089/scd.2011.0707 · Cited by 12
Regulation of self-renewal and reprogramming by TCF factors
Ombrato, L., Lluı́s, F., & Cosma, M. P. (2012) · Cell Cycle · doi:10.4161/cc.11.1.18759 · Cited by 13
Efficient Cell Reprogramming Using Bioengineered Surfaces
Horna, D., Ramı́rez, J. C., Cifuentes‐Rius, A., Bernad, A., Borrós, S., & González, M. A. (2012) · Advanced Healthcare Materials · doi:10.1002/adhm.201200017 · Cited by 12
Telomere dynamics in induced pluripotent stem cells: Potentials for Human disease modeling
Ly, H. (2011) · World Journal of Stem Cells · doi:10.4252/wjsc.v3.i10.89 · Cited by 14
Mechanism and methods to induce pluripotency
Wang, P., & Na, J. (2011) · Protein & Cell · doi:10.1007/s13238-011-1107-1 · Cited by 13
“…a major barrier towards regaining pluripotency (Zhao et al., 2008b; Banito et al., 2009; Hong et al., 2009; Kawamura et al., 2009; Li et al., 2009; Marión et al., 2009; Utikal et al., 2009b), chemical compounds that alleviate the stress of DNA damage response may help cells to overcome this…”
BackgroundInfluentialXu, N., Li, X., Watanabe, M., Ueki, H., Hu, H., Li, N., Araki, M., Wada, K., Xu, A., Liu, C., et al. (2018) · Europe PMC (PubMed Central) · Cited by 11
Reyes, J., Priore, I. S. D., Chaikovsky, A. C., Pasnuri, N., Elhossiny, A. M., Park, J., Weiler, P., Krause, T., Moorman, A. R., Snopkowski, C., et al. (2026) · Cell · doi:10.1016/j.cell.2026.03.032 · Cited by 12
FANCA knockout in human embryonic stem cells causes a severe growth disadvantage
Vanuytsel, K., Cai, Q., Nair, N., Khurana, S., Shetty, S., Vermeesch, J. R., Ordovás, L., & Verfaillie, C. M. (2014) · Stem Cell Research · doi:10.1016/j.scr.2014.07.005 · Cited by 11
“…and in agreement with an exacerbated p53 stress response in FA cells (Ceccaldi et al., 2012) and the rate-limiting effect of p53 on reprogramming (Marion et al., 2009; Hong et al., 2009; Utikal et al., 2009), Liu et al. could only generate FA hiPSC when p53 shRNA was added to the reprogramming…”
BackgroundRetractedLu, W., Tseng, S. C. G., Chen, S., Tighe, S. P., Zhang, Y., Liu, X., Chen, S., Su, C., & Zhu, Y. (2016) · Scientific Reports · doi:10.1038/srep35166 · Cited by 11
Robertson, A., Mohamed, T., Maadawi, Z. E., Stafford, N., Bùi, T. A., Lim, D., Cartwright, E. J., & Oceandy, D. (2017) · Stem Cell Research · doi:10.1016/j.scr.2017.02.011 · Cited by 12
“In agreement with this, various observations have demonstrated that in less proliferative cells or in senescent cells the reprogramming efficiency is low (Banito et al., 2009; Kawamura et al., 2009; Li et al., 2009; Marion et al., 2009).”
BackgroundAn expedition in the jungle of pluripotent stem cells of non-human primates
Anwised, P., Moorawong, R., Samruan, W., Somredngan, S., Srisutush, J., Laowtammathron, C., Aksoy, I., Parnpai, R., & Savatier, P. (2023) · Stem Cell Reports · doi:10.1016/j.stemcr.2023.09.013 · Cited by 11
Towards New Anticancer Strategies by Targeting Cancer Stem Cells with Phytochemical Compounds
Sharif, T., Emhemmed, F., & Fuhrmann, G. (2011) · BiblioBoard Library Catalog (Open Research Library) · doi:10.5772/18695 · Cited by 11
“The Cutting Edge 448 production [Marion et al., 2009].”
BackgroundSwitching stem cell state through programmed germ cell reprogramming
Gillich, A., & Hayashi, K. (2011) · Differentiation · doi:10.1016/j.diff.2011.01.003 · Cited by 11
Concise Review: Methods and Cell Types Used to Generate Down Syndrome Induced Pluripotent Stem Cells
Hibaoui, Y., & Féki, A. (2015) · Journal of Clinical Medicine · doi:10.3390/jcm4040696 · Cited by 11
“Barriers such as the age and the differentiation status of the donor’s cells could explain this property [66–68].”
BackgroundCell fate, metabolic reprogramming and lncRNA of tumor-initiating stem-like cells induced by alcohol
Machida, K. (2020) · Chemico-Biological Interactions · doi:10.1016/j.cbi.2020.109055 · Cited by 11
Riggi, N., Suvà, M.-L., & Stamenkovic, I. (2011) · Expert Review of Anticancer Therapy · doi:10.1586/era.10.235 · Cited by 11
Novel Interplay between p53 and HO-1 in Embryonic Stem Cells
Toro, A. R., Anselmino, N., Solari, C., Francia, M. G., Oses, C., Sanchis, P., Bizzotto, J. A., Echegaray, C. V., Petrone, M. V., Levi, V., et al. (2020) · Cells · doi:10.3390/cells10010035 · Cited by 12
Yoshida, Y., & Yamanaka, S. (2012) · Circulation Research · doi:10.1161/circresaha.112.271445 · Cited by 11
Metadata
- Authors
- Marión, R. M., Strati, K., Li, H., Murga, M., Blanco, R., Ortega, S., Fernandez-Capetillo, O., Serrano, M., & Blasco, M. A.
- Affiliations
- Spanish National Cancer Research Centre (ES)
- Venue
- Nature
- Published
- 2009-08
- Volume
- 460
- Issue
- 7259
- Pages
- 1149-1153
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC3624089
- OpenAlex
- W2111920812
- Cited by
- 1,028
- References
- 29
- Citations by year
- 2026: 12 · 2025: 20 · 2024: 13 · 2023: 20 · 2022: 37 · 2021: 24 · 2020: 35 · 2019: 45 · 2018: 46 · 2017: 51 · 2016: 60 · 2015: 72 · 2014: 84 · 2013: 110 · 2012: 135
- FWCI
- 53.60
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- Ministerio de Ciencia e Innovación
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Pluripotent Stem Cells Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Telomeres, Telomerase, and Senescence
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
- Keywords
- p53, DNA damage response, induced pluripotent stem cells, cellular reprogramming, short telomeres, DNA repair deficiency, chromosomal abnormalities, genome stability, apoptosis, pluripotency
- MeSH terms
- Animals, Cells, Cultured, Chromosome Aberrations, DNA Damage, DNA Repair, Female, Fibroblasts, Humans, Male, Tumor Suppressor Protein p53, Telomere, Apoptosis, Pluripotent Stem Cells, Genomic Instability, Mice, Cellular Reprogramming
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