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Rejuvenating senescent and centenarian human cells by reprogramming through the pluripotent state
Open accessAbstract
Direct reprogramming of somatic cells into induced pluripotent stem cells (iPSCs) provides a unique opportunity to derive patient-specific stem cells with potential applications in tissue replacement therapies and without the ethical concerns of human embryonic stem cells (hESCs). However, cellular senescence, which contributes to aging and restricted longevity, has been described as a barrier to the derivation of iPSCs. Here we demonstrate, using an optimized protocol, that cellular senescence is not a limit to reprogramming and that age-related cellular physiology is reversible. Thus, we show that our iPSCs generated from senescent and centenarian cells have reset telomere size, gene expression profiles, oxidative stress, and mitochondrial metabolism, and are indistinguishable from hESCs. Finally, we show that senescent and centenarian-derived pluripotent stem cells are able to redifferentiate into fully rejuvenated cells. These results provide new insights into iPSC technology and pave the way for regenerative medicine for aged patients.
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“However, induction of pluripotency in iPSCs resets the age signatures of the donor cells to a fetal stage (7–9).”
From Modeling late-onset Alzheimer’s disease neuropathology via direct neuronal reprogramming (2024) · cites this paper as [7]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“Telomere length decreases with age due to cell proliferation in the absence of telomerase enzymes and is restored upon complete iPSC reprogramming (Lapasset et al., 2011).”
From Multi-omic rejuvenation of human cells by maturation phase transient reprogramming (2022) · cites this paper as Lapasset et al., 2011
Experimental — accuracy not yet measuredThe cited source says what the claim attributes to it.
In the citing paper
“The rejuvenation of aging hallmarks has been extensively described during cellular reprogramming to pluripotency in vitro (Lapasset et al., 2011;Liu et al., 2011;Mahmoudi and Brunet, 2012;Rando and Chang, 2012), but the dynamics of this process remain poorly understood.”
From In Vivo Amelioration of Age-Associated Hallmarks by Partial Reprogramming. (2016) · cites this paper as Lapasset et al., 2011
The cited source says what the claim attributes to it.
In the citing paper
“Several groups, including ours, have observed an amelioration of age-associated cellular phenotypes during in vitro cellular reprogramming”
From In Vivo Amelioration of Age-Associated Hallmarks by Partial Reprogramming. (2016) · cites this paper as Lapasset et al., 2011
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In the citing paper
“iPSC reprogramming reverses many age-associated changes, including telomere attrition and oxidative stress (Lapasset et al., 2011).”
From Multi-omic rejuvenation of human cells by maturation phase transient reprogramming (2022) · cites this paper as Lapasset et al., 2011
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“Early reports using cells derived from old donors to generate iPS cells demonstrated beneficial effects on senescence phenotypes and telomere length [26][27][28] .”
From Mechanisms, pathways and strategies for rejuvenation through epigenetic reprogramming (2023) · cites this paper as [26]
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In the citing paper
“but protocols relied upon rejuvenation through re-differentiation after iPS cell formation 20,26,28 .”
From Mechanisms, pathways and strategies for rejuvenation through epigenetic reprogramming (2023) · cites this paper as [26]
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“Early experiments in human cells were somewhat encouraging as they provide evidence that some of the biomarkers of aging (that is telomere lengths) were responding to the epigenetic reprogramming”
From Mechanisms, pathways and strategies for rejuvenation through epigenetic reprogramming (2023) · cites this paper as [26]
In the citing paper
“Of note, senescent cells from elderly people could be reverted to a pluripotent state only by the additional over-expression of NANOG and LIN2 in addition to Oct3/4, Sox2, c-Myc, and KLF4.196”
From Senescence-induced inflammation: an important player and key therapeutic target in atherosclerosis (2020) · cites this paper as [196]
In the citing paper
“A growing body of evidence, including the present study and a prior report of reprogramming of senescent human fibroblasts into induced pluripotent stem cells (iPSCs; ref. 48), suggests that near-senescent or senescent cells can be induced back into a proliferative state.”
From p53 isoforms regulate aging- and tumor-associated replicative senescence in T lymphocytes (2013) · cites this paper as [48]
In the citing paper
“Reprogramming cells from elderly humans (as old as 101 years of age) into pluripotent cells erases many of the hallmarks of aging and restores a youthful gene expression profile that is maintained during differentiation (Lapasset et al., 2011; Mertens et al., 2015).”
From The Aging Epigenome (2016) · cites this paper as Lapasset et al., 2011
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Citations
Cites
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“It has been reported by several groups that cellular senescence is a barrier to reprogramming due to upregulation of p53, p16, and p21, which are also induced by some of the iPSC reprogramming factors (Banito et al. 2009; Kawamura et al. 2009; Li et al. 2009; Marion et al. 2009a; Utikal et al. 2009).”
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BackgroundSingle short reprogramming early in life increases healthspan
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“One important issue is that iPSC reprogramming largely resets cellular age [85].”
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Shorokhova, M. (2024) · Cell and Tissue Biology · doi:10.1134/s1990519x23700104 · Cited by 1
Linking Aging to Cancer: The Role of Chromatin Biology
Corveleyn, L., Sen, P., Adams, P. D., & Sidoli, S. (2024) · The Journals of Gerontology Series A · doi:10.1093/gerona/glae133 · Cited by 2
Niculescu, V. F. (2025) · Academia molecular biology and genomics. · doi:10.20935/acadmolbiogen7755 · Cited by 2
Genodermatoses with Premature Aging/Syndromes
Chedraoui, A., Kibbi, A. G., & Kurban, M. (2015) · Springer eBooks · doi:10.1007/978-3-642-27814-3_132-1 · Cited by 1
Longevity Pathways in Mammalian Stem Cells
Brunet, A., Mahmoudi, S., Mancini, E., Rafalski, V. A., & Webb, A. E. (2014) · Annual Review of Gerontology and Geriatrics · doi:10.1891/0198-8794.34.1 · Cited by 1
“Indeed, some aspects of aged cells, such as telomere lengths and gene expression changes, are reversed to young states by the process of reprogramming followed by redifferentiation (Lapasset et al., 2011).”
BackgroundRejuvenation on the Road to Pluripotency
Sarkar, T. J., & Sebastiano, V. (2016) · InTech eBooks · doi:10.5772/63219 · Cited by 1
“iPSC reprogramming has been achieved on completely senescent populations, propagated for 51 population doublings then maintained for 2 months, and show revived proliferation in the pluripotent state as well as upon redifferentiation [39].”
BackgroundConsiderable Life Extension and the Deprivation View
Rantanen, R. (2012) · Thanatos · Cited by 1
Helm, P. J., Lifshin, U., Greenberg, J., & Pyszczynski, T. (2021) · Psychological Reports · doi:10.1177/0033294121988997 · Cited by 1
“technologies that range in their scope and goals such as regenerative medicine, nanotechnology, research on telomeres, brain preservation, and even mind upload technology (e.g., Boichenko et al., 2020; Cerullo, 2016; Kenyon, 2010; Laakasuo et al., 2020; Lapasset et al., 2011; Peters, 2018; Rattan & Singh, 2009).”
BackgroundKardeh, S., Mazloomrezaei, M., Jalouli, M., & Faezi-Marian, S. (2021) · Burns · doi:10.1016/j.burns.2021.04.008 · Cited by 1
Editorial: Mechanisms and Implications of the Aging of Cardiovascular Regenerative Cells
Beltrami, A. P., & Spinetti, G. (2018) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2018.00093 · Cited by 1
“Somehow surprisingly, the reprogramming capabilities of somatic cells, although decreased with age, appears to be maintained as iPSC from centenarians indicate (3, 4).”
BackgroundMolecular Mechanisms Underlying Cardiometabolic Disease in Aging
Fanjul, V. (2019) · doi:10.4321/repisalud.8343 · Cited by 1
Jalnapurkar, B., Le, D., Shainin, W., Zarcone, R., Bhatnagar, R., Chin, J., Corbin, C. K., Curt, C., Hodge, B. A., Martinez, F., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.11.21.568079 · Cited by 1
“One potential reason for the lack of disease signature in iPSC-derived neurons is that they appear to have an embryonic age signature regardless of the age of the original donor 27,28 .”
BackgroundComparative analysis of mouse strains for in vivo reprogrammingPreprint
Picó, S., Vílchez-Acosta, A., de Sousa, J. A., Maza, M. D. C. L., Parras, A., Desdín-Micó, G., Mrabti, C., Maroun, C. Y., Branchina, C., von Meyenn, F., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.03.08.584074 · Cited by 1
Luo, Y., Zhu, X., Le, Q.-R., Chen, W., Xu, Y., Chen, X., Yang, X., Yuan, H., Xu, J., Zhong, J., et al. (2025) · Research Square · doi:10.21203/rs.3.rs-5848058/v1 · Cited by 1
Induced pluripotent stem-cell re-programming in the elderly prostate
Pal, D. (2014) · Cited by 1
T Cells Seen from the Metabolic and Aging Perspective
Camous, X., & Larbi, A. (2013) · Springer eBooks · doi:10.1007/978-3-642-39495-9_12
Past, Present, and Future: The Behavioral Sciences.
Darley, J. G. (1971) · Contemporary Psychology · doi:10.1037/014015
Use of Induced Pluripotent Stem Cells in Aging Research
Isobe, K. (2015) · Springer eBooks · doi:10.1007/978-4-431-55763-0_4
Stem cells for all ages, yet hostage to aging
Finch, C. E., & McMahon, A. P. (2016) · Stem Cell Investigation · doi:10.21037/sci.2016.04.02
“The potential for FB rejuvenation extends to ‘senescent cells’: from the same 74 years old, iPSCs were derived from either primary FBs or replicatively senescent FBs after serial in vitro passaging: both differentiated into normal embryonic lineages (2).”
BackgroundCited2 in mouse embryonic fibroblasts reprogramming
Alves, A. (2014) · Portuguese National Funding Agency for Science, Research and Technology (RCAAP Project by FCT)
Respuela, P., & Rada-Iglesias, Á. (2016) · Current Stem Cell Reports · doi:10.1007/s40778-016-0050-8
Les cellules souches pluripotentes induites : un nouveau paradigme pour l’étude des tissus humains
Sansac, C., Assou, S., Bouckenheimer, J., Lemaı̂tre, J.-M., & Vos, J. D. (2016) · Biologie Aujourd hui · doi:10.1051/jbio/2016013
“Certaines variations dans le nombre et la nature de ces facteurs ont permis de g´en´eraliser cette technologie en la ren-dant applicable `a partir de nombreux types cellulaires y compris ceux issus de personnes tr`es ˆag´ees et mˆeme centenaires (Lapasset et al. , 2011).”
Stem Cell Applications in Rejuvenation
Almadori, A., & Kalaskar, D. M. (2017) · Stem cells in clinical applications · doi:10.1007/978-3-319-55687-1_13
Neuromuscular Tissue Engineering
Avin, K. G., Badylak, S. F., & Ambrosio, F. (2014) · Orthopaedic Section, APTA, Inc. eBooks · doi:10.17832/isc.2014.23.2.2
Langer, S. K., Horn, P., & Heinrichs, S. (2017) · Cellular Reprogramming · doi:10.1089/cell.2017.0037
“However, at the same time, such models have revealed stark limitations in the reflection of the cellular age of their origin, as the reprogramming process reliably erases the aging memory from old cells (Lapasset et al., 2011; Miller et al., 2013).”
Gene Therapy and Immunosenescence
Hsu, H., Chen, J., & Mountz, J. D. (2017) · Springer eBooks · doi:10.1007/978-3-319-64597-1_76-1
The Relevance of Induced Pluripotent Stem Cells for the Study of Physiological and Premature Aging
Carrero, D., & López-Otı́n, C. (2018) · Springer eBooks · doi:10.1007/978-3-319-90695-9_13
Novel Approaches for Pluripotent Reprogramming
Weltner, J. (2018) · Työväentutkimus Vuosikirja
How to Treat or Prevent, or Slow Down, Cellular Ageing and Senescence?
Swynghedauw, B. (2019) · Practical issues in geriatrics · doi:10.1007/978-3-030-15111-9_7
Attaining Epigenetic Rejuvenation: Challenges Ahead
Purohit, J. S., Singh, N., Hussain, S. S., & Chaturvedi, M. M. (2020) · Springer eBooks · doi:10.1007/978-981-32-9005-1_9 · Cited by 1
Steg, L. C., Shireby, G. L., Imm, J. L., Davies, J. P., Flynn, R. J., Namboori, S. C., Bhinge, A., Jeffries, A. R., Burrage, J., Neilson, G., et al. (2020) · doi:10.21203/rs.3.rs-94490/v1
Marsellach, X. (2021) · Preprints.org · doi:10.20944/preprints202012.0506.v2
Deconstructing Stepwise Fate Conversion of Human Fibroblasts to Neurons by MicroRNAsPreprint
McCoy, M. J., Cates, K., Liu, Y., Abernathy, D. G., Zhang, B., Liu, S., Gontarz, P. M., Kim, W. K., Chen, S., Kong, W., et al. (2019) · SSRN Electronic Journal · doi:10.2139/ssrn.3485473 · Cited by 1
“to a fetal stage and therefore erases age- or pathology-dependent epigenetic information (Horvath, 2013; Lapasset et al., 2011; Miller et al., 2013; Patterson et al., 2012), direct conversion propagates age-associated signatures in reprogrammed neurons (Huh et al.”
BackgroundModelling late-onset diseases with induced pluripotent stem cells: a matter of time management
Cossins, C., & Fairchild, P. J. (2021) · Cell and Gene Therapy Insights · doi:10.18609/cgti.2021.015
“However, accumulating 188 evidence suggests that the age signature of iPSC is erased upon reprogramming to pluripotency, 189 resulting in restoration of telomere length, mitochondrial function and nuclear morphology, as 190 well as reversal of cellular senescence [47].”
Background
Metadata
- Authors
- Lapasset, L., Milhavet, O., Prieur, A., Besnard, E., Babled, A., Aït-Hamou, N., Leschik, J., Pellestor, F., Ramirez, J.-M., De Vos, J., Lehmann, S., & Lemaitre, J.-M.
- Affiliations
- Institut de Génomique Fonctionnelle (FR)
- Hôpital Arnaud de Villeneuve (FR)
- Hôpital Saint Eloi (FR)
- Institut de Génétique Humaine (FR)
- ORCID
- Venue
- Genes & Development
- Publisher
- Cold Spring Harbor Laboratory
- Published
- 2011-11-01
- Volume
- 25
- Issue
- 21
- Pages
- 2248-2253
- ISSN
- 0890-9369 (ISSN-L)
- 1549-5477
- PMC
- PMC3219229
- OpenAlex
- W2114840727
- Cited by
- 570
- References
- 31
- Citations by year
- 2026: 30 · 2025: 41 · 2024: 46 · 2023: 49 · 2022: 53 · 2021: 49 · 2020: 38 · 2019: 40 · 2018: 49 · 2017: 33 · 2016: 33 · 2015: 30 · 2014: 29 · 2013: 25 · 2012: 23
- Type
- posted content
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Genes & Development (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- Funders
- Agence Nationale de la Recherche (ANR-07-BLAN-0076)
- Institut National de la Santé et de la Recherche Médicale
- Institut National Du Cancer
- 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 › Cell Biology › Mesenchymal stem cell research
- Keywords
- cellular senescence, induced pluripotent stem cells, direct reprogramming, aging, telomere length, oxidative stress, mitochondrial metabolism, gene expression profiles, redifferentiation, rejuvenation, regenerative medicine
- MeSH terms
- Aged, Aged, 80 and over, Animals, Cell Differentiation, Cell Line, Cells, Cultured, Humans, Mitochondria, Rejuvenation, Transcription Factors, Mice, SCID, Telomere, Mice, Inbred NOD, Cellular Senescence, Mice, Induced Pluripotent Stem Cells, Cellular Reprogramming
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