Cited by 206Nuclear Structure and FunctionTelomeres, Telomerase, and SenescenceGenetics, Aging, and Longevity in Model Organisms

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Oxidative stress induces an ATM‐independent senescence pathway through p38 MAPK‐mediated lamin B1 accumulation

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Barascu, Aurelia, Le Chalony, Catherine, Pennarun, Gaëlle, Genet, Diane, Imam, Naima, Lopez, Bernard, Bertrand, Pascale·2012·The EMBO Journal

DOI 10.1038/emboj.2011.492PMC PMC3297999

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Abstract

We report crosstalk between three senescence-inducing conditions, DNA damage response (DDR) defects, oxidative stress (OS) and nuclear shape alterations. The recessive autosomal genetic disorder Ataxia telangiectasia (A-T) is associated with DDR defects, endogenous OS and premature ageing. Here, we find frequent nuclear shape alterations in A-T cells, as well as accumulation of the key nuclear architecture component lamin B1. Lamin B1 overexpression is sufficient to induce nuclear shape alterations and senescence in wild-type cells, and normalizing lamin B1 levels in A-T cells reciprocally reduces both nuclear shape alterations and senescence. We further show that OS increases lamin B1 levels through p38 Mitogen Activated Protein kinase activation. Lamin B1 accumulation and nuclear shape alterations also occur during stress-induced senescence and oncogene-induced senescence (OIS), two canonical senescence situations. These data reveal lamin B1 as a general molecular mediator that controls OS-induced senescence, independent of established Ataxia Telangiectasia Mutated (ATM) roles in OIS.

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WITHDRAWN: Oxidative stress in aging: Theoretical outcomes and clinical evidences in humans
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Persistent DNA damage signalling triggers senescence-associated inflammatory cytokine secretion
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“Elevated levels of lamins B1 have been also reported in the Werner syndrome (51), and by our team, in the Ataxia-Telangiectasia disorder (AT) and we showed that increased lamin B1 expression accounts for nuclear shape alterations and senescence in this condition (52).”
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“Finally, for the biological activity of oxidative stress, the most contributing Cell Health phenotype (level 3) was the average nucleus roundness, which is consistent with the significant crosstalk between DNA damage, oxidative stress, and nuclear shape alterations (Barascu et al. , 2012).”
Background
The Methyl Xanthine Caffeine Inhibits DNA Damage Signaling and Reactive Species and Reduces Atherosclerosis in ApoE −/− Mice
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“However, given that high lamin B1 levels have been linked to ROS induction and cellular senescence [28], a synergistic effect of lamin B1 up-regulation and altered Oct-1 nuclear import, leading to improper regulation of response factors, could induce oxidative stress-triggered cell death [29].”
Background
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“T patients, and knocking down the MAPK14 gene encoding p38 prevented their premature senescence (52).”
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Individual Cytokines Modulate the Neurological Symptoms ofATMDeficiency in a Region Specific Manner
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“…control cell-cycle checkpoint for DNA repair and promote survival in normal or A-T cells (Panta et al., 2004; Kani et al., 2007; Kim et al., 2007; Barascu et al., 2012) while the ATM-Akt pathway maintains homeostasis and survival by regulating glucose transporter 4 translocation in response to…”
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Pan-senescence transcriptome analysis identified RRAD as a marker and negative regulator of cellular senescence
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“Mechanistically ROS have been implied in persistent DDR signaling [4] and activation of the p38 mitogen activated protein kinase (p38 MAPK); inducing proliferation arrests both in ATM dependent and independent fashion [5, 6].”
Background
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“(Barascu et al. 2012).”
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Background
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BackgroundInfluential
ATM-deficient human fibroblast cells are resistant to low levels of DNA double-strand break induced apoptosis and subsequently undergo drug-induced premature senescence
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Background
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Background
Human dermal fibroblast senescence in response to single and recurring oxidative stress
McCarty, T. Y., & Kearney, C. J. (2025) · Frontiers in Aging · doi:10.3389/fragi.2025.1504977 · Cited by 8
Mitochondrial Reactive Oxygen Species in Cellular Senescence
Nacarelli, T., Torres, C. A., & Sell, C. (2016) · Healthy ageing and longevity · doi:10.1007/978-3-319-26239-0_10 · Cited by 9
High copper levels induce premature senescence in 3T3-L1 preadipocytes
de Oliveira, R. F., Salazar, M., Matos, L., Almeida, H., Rodrigues, A. R., & Gouveia, A. (2024) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2024.119734 · Cited by 8
Drosophila p38 MAPK interacts with BAG‐3/starvin to regulate age‐dependent protein homeostasis
Ryan, S. M., Almassey, M., Burch, A. M., Ngo, G., Martin, J. M., Myers, D., Compton, D., Archie, S., Cross, M., Naeger, L., et al. (2021) · Aging Cell · doi:10.1111/acel.13481 · Cited by 6
“We find that Lamin, which is mutated to an aggregation prone protein form in Hutchinson- Gilford progeria (Barascu et al., 2012; Burke & Stewart, 2013; Cao et al., 2007; Chandran et al., 2019; Eriksson et al., 2003), is a target of p38Kb and stv. Interestingly, p38Kb and Lamin mutants share similar…”
Background
An update on healthspan and lifespan enhancing attributes of tea amidst the emerging understanding of aging biology
Sharma, R., & Diwan, B. (2022) · Human Nutrition & Metabolism · doi:10.1016/j.hnm.2022.200149 · Cited by 8
Regulatory mechanisms of transforming growth factor-β in senescence of fibroblast associated with refractory skin diseases
Zheng, Y., Lei, J., Zhang, A., Cao, C., Xu, A., Zhou, M., & Lin, F. (2025) · Experimental Gerontology · doi:10.1016/j.exger.2025.112900 · Cited by 7
GREG—studying transcriptional regulation using integrative graph databases
Mei, S., Huang, X., Xie, C., & Mora, A. (2020) · Database · doi:10.1093/database/baz162 · Cited by 6
In Situ Detection of Interactions Between Nuclear Envelope Proteins and Partners
Barateau, A., & Buendia, B. (2016) · Methods in molecular biology · doi:10.1007/978-1-4939-3530-7_9 · Cited by 6
A high throughput, high content screen for non-toxic small molecules that reduce levels of the nuclear lamina protein, Lamin B1
Vollmer, L. L., Liu, F., Nmezi, B., Bey, G. R., Herdman, N., Shun, T. Y., Gough, A., Liu, R., Wipf, P., Lezon, T. R., et al. (2025) · Scientific Reports · doi:10.1038/s41598-025-91546-3 · Cited by 5
“Because published reports had suggested an involvement of MAPKs in LMNB1 regulation (Barascu et al., 2012), we confirmed the activity of SB202190 and SP600125 in Western blots as non-fluorescent orthogonal assays ( Fig.”
Entwined processes in Alzheimer's disease: Brain cellular senescence and Alzheimer's disease pathology
Li, W., Han, Y., Wang, P., & Qiao, S. (2025) · Alzheimer s & Dementia · doi:10.1002/alz.70803 · Cited by 6
EZH2 inhibition induces senescence via ERK1/2 signaling pathway in multiple myeloma
Guo, S., Tang, Q., Gao, X., Hu, L., Hu, K., Zhang, H., Zhang, Q., Lai, Y., Liu, Y., Wang, Z., et al. (2024) · Acta Biochimica et Biophysica Sinica · doi:10.3724/abbs.2024077 · Cited by 5
“High level of Lamin B1 in Ataxia telangiectasia cells results in altered nuclei and senescence [8], which is parallel to what we have demonstrated in OCI-MY5 and RPMI-8226 cells.”
BackgroundMethodResult
Surface Acoustic Wave‐Enhanced Multi‐View Acoustofluidic Rotation Cytometry (MARC) for Pre‐Cytopathological Screening
Zhang, X., Dumčius, P., Mikhaylov, R., Qi, J., Stringer, M., Sun, C., Nguyen, V. D., Zhou, Y., Sun, X., Liang, D., et al. (2024) · Advanced Science · doi:10.1002/advs.202403574 · Cited by 4
Beneficial Antioxidant Effects of Coenzyme Q10 in In Vitro and In Vivo Models of CDKL5 Deficiency Disorder
Loi, M., Valenti, F., Trazzi, S., Mottolese, N., Candini, G., Bove, A. M., Trebbi, F., Pincigher, L., Fato, R., Bergamini, C., et al. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26052204 · Cited by 7
“Our finding is in agreement with the recently proposed role of lamin B1 as a general marker and mediator of ROS-induced cell senescence [46,56].”
Tumor Dormancy, Quiescence, and Senescence, Volume 1
Hayat, M. A. (2013) · Springer eBooks · doi:10.1007/978-94-007-5958-9 · Cited by 6
Sprouty1 is a broad mediator of cellular senescence
Anerillas, C., Perramon‐Güell, A., Altés, G., Cuesta, S., Vaquero, M., Olomí, A., Barrueco, R. R., Llobet‐Navàs, D., Egea, J., Dolcet, X., et al. (2024) · Cell Death and Disease · doi:10.1038/s41419-024-06689-4 · Cited by 4
“Transgenic p16-3MR mice [Tg(Cdkn2a/luc/RFP/TK)1Cmps] were a generous gift of Dr. Judith Campisi (Buck Institute for Research on Aging, Novato, California), and were generated as described [31].”
Background
Le vieillissement
Fontanilla-Ramirez, P., Willaume, S., Thezé, B., Moussa, A., Pennarun, G., & Bertrand, P. (2020) · médecine/sciences · doi:10.1051/medsci/2020241 · Cited by 6
Self-citation
The relationship of lamins with epigenetic factors during aging
Mustafin, R. N., & Хуснутдинова, Э. К. (2022) · Vavilov Journal of Genetics and Breeding · doi:10.18699/vjgb-22-06 · Cited by 3
“Using the PLA method (proximity ligation assay), it was proved that p38 MAPK interacts with lamin B1, causing its phosphorylation (Barascu et al., 2012).”
Method
Life and Death without Telomerase: The Saccharomyces cerevisiae ModelPreprint
Martinez-Fernandez, V., Barascu, A., & Teixeira, M. T. (2024) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a041699 · Cited by 5
Self-citation
Effect of Regular Exercise and Resveratrol on Hypertension-Induced Cellular Stress Response and Senescence in Renal and Vascular Tissues of Rats
Bal, N. B., Sadı, G., Bostancı, A., Kiremitçi, S., Adanir, I., Uludağ, M. O., & Demirel-Yılmaz, E. (2025) · Journal of Cardiovascular Pharmacology · doi:10.1097/fjc.0000000000001744 · Cited by 3
Mechanisms Enhancing the Cytotoxic Effects of Bleomycin plus Suicide or Interferon-β Gene Lipofection in Metastatic Human Melanoma Cells
Fondello, C., Agnetti, L., Glikin, G. C., & Finocchiaro, L. M. E. (2018) · Anti-Cancer Agents in Medicinal Chemistry · doi:10.2174/1871520618666180604084849 · Cited by 3
Radiation symptoms resemble laminopathies and the physical underlying cause may sit at the lamin A C-terminus
Waldherr, A., & Fogtman, A. (2025) · Molecular Medicine · doi:10.1186/s10020-025-01081-0 · Cited by 2
“The pathway causes nuclear alterations and eventually leads to senescence via p38 and MAPK (Barascu et al. 2012; Wang et al. 2020).”
Aging and Cardiovascular Diseases: The Role of Cellular Senescence
Bozaykut, P. (2019) · Springer eBooks · doi:10.1007/978-981-13-8273-4_10 · Cited by 3
Higher-Order Unfolding of Peri/Centric Satellite Heterochromatin is an Early and Consistent Event in Cell Senescence: A Dissertation
Swanson, E. C. (2014) · The Journal of the American Medical Association (JAMA) Network (American Medical Association) · doi:10.13028/m2k30f · Cited by 1
“Additionally, it has recently been shown that cells can senesce in an ATM-independent manner (Barascu et al., 2012; Takahashi et al., 2006), suggesting that oxidative stresses can also cause senescence independent of DNA”
Background
Cdk1-dependent lamin aggregation underlies oxidative stress-induced nuclear shape abnormalities
Ahn, J.-H., Cho, M.-G., Basit, A., Song, I.-K., Lee, K., & Lee, J. (2025) · BMB Reports · doi:10.5483/bmbrep.2024-0164 · Cited by 1
“In this study, we elucidated a novel mechanism by which ROS, specifically hydrogen peroxide (H 2 O 2 ), could modulate Cdk1 activity during mitotic entry, resulting in aberrant lamin phosphorylation and formation of aggregated lamin.”
Influential
Alginate Oligosaccharides Attenuate Ochratoxin A‐Induced Liver Injury through Regulating the Interaction of Nrf2 and NF‐κB Signaling Pathways
Zhao, Y., Ye, X.-Q., Guo, Y., Zhao, Z., Yao, Q., Wang, Y., Liu, H., Lin, Z., & Liu, W. (2025) · Food Frontiers · doi:10.1002/fft2.70177 · Cited by 1
Neuron-specific increase in lamin B1 disrupts nuclear function in Huntington’s diseasePreprint
Alcalá‐Vida, R., García-Forn, M., Creus‐Muncunill, J., Ito, Y., Blanco, E., Castany‐Pladevall, C., Crespí-Vázquez, K., Parry, A., Slater, G., Samarajiwa, S., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.03.06.979674 · Cited by 1
The Glial Aging & Senescence Hypothesis of Late-onset Alzheimer’sPreprint
Lau, V. Z., Ramer, L. M., & Tremblay, M. (2022) · Preprints.org · doi:10.20944/preprints202109.0437.v2 · Cited by 1
Identification of Markers for Cellular Stress and Senescence in Laminopathic Cells by Proteomic Analysis
Sinha, K., Swamy, C. V. B., Muralikrishna, B., Idris, M. M., Nagaraj, R., & Parnaik, V. K. (2014) · Revista de Fomento Social · doi:10.16943/ptinsa/2014/v80i5/47977
Generation Of Humanized Models For The Understanding Of Health And Aging
Kraus, M. (2015) · INFM-OAR (INFN Catania) · doi:10.5281/zenodo.32656
THE ROLE OF DENDRITIC BDNF TRANSCRIPTS ON ALTERED INHIBITORY CIRCUITRY IN AGING AND DEPRESSION
Oh, H. (2015) · D-Scholarship@Pitt (University of Pittsburgh)
Die Rolle der Metalloprotease ADAM17 während der zellulären Seneszenz
Effenberger, T. (2014) · Multimedialen Archiv und Publikationsserver der Christian-Albrechts-Universität zu Kiel (Christian-Albrechts-Universität zu Kiel)
The Role of p38 MAPK in Protein Homeostasis and Aging
Ryan, S. M. (2016) · Digital Commons - DU (University of Denver)
An in vivo and in vitro study of stress-induced senescence in neurones and its role in neurodegeneration
Vázquez-Villaseñor, I. (2018) · White Rose eTheses Online (University of Leeds, The University of Sheffield, University of York)
Aberrant DNA Methylation Patterns in Gynecologic Cancers
Beetch, M., Bai, Y., Lubecka, K., Stefañska, B., & Lelièvre, S. A. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-812215-0.00024-8
Role of Nuclear Lamins in the Regulation of the Genome: Focus on CardioLaminopathy
Kervella, M., & Muchir, A. (2025) · Sub-cellular biochemistry/Subcellular biochemistry · doi:10.1007/978-3-032-00537-3_1
Etude du rôle du gène suppresseur de tumeur WWOX et de ses partenaires dans la voie de signalisation Wnt/β-caténine et dans la carcinogenèse mammaire
Hage, P. E. (2012) · theses.fr (ABES) · doi:10.70675/ccc1dd98z7231z4049z820bz0b737c38ec44 · Cited by 1
Caractérisation de la sénescence des cardiomyocytes et identification de marqueurs associés
Maggiorani, D. (2017) · theses.fr (ABES) · doi:10.70675/a58747bczd60bz4482za3b2z7ae33d26ffa4
“Toutefois, dans certains modèle de sénescence induite in vitro, une augmentation paradoxale de la lamine B1 est observée remettant alors en question cette caractéristique comme marqueur de sénescence (Barascu et al., 2012).”
Background
Role of Lamin B1 dysregulation in two Enabling Forces of Cancer : Genome Instability and Inflammation
Fontanilla-Ramirez, P. (2020) · theses.fr (ABES) · doi:10.70675/55998d2az7ba5z4d1ez9adezd5b9861cf0fe
Implications de la lamine B1 dans la stabilité des télomères et la mitose
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Tiki2 restrains Wnt5a/Ror signaling to limit inflammation in acute kidney injury
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“Given that Lmnb1 is typically reduced at the protein level in senescent cells, the increased Lmnb1 mRNA observed here does not provide suf ﬁ cient evidence for cellular senescence and may instead re ﬂ ect nuclear lamina remodeling or cell-cycle – related changes following injury 39,40 .”
Nox4 mediates chondrocyte senescence and cartilage degradation in post-traumatic osteoarthritis via the ROS/p38MAPK signaling pathway
Wu, Q., Qin, H., Shen, K., Huang, D., Chen, J., Jiang, G., Chen, H., Yu, B., & Wang, S.-H. (2026) · International Immunopharmacology · doi:10.1016/j.intimp.2026.116924
Profilin-1 Deficiency Activates STING to Drive T Cell-Mediated Anti-Tumor Immunity in Breast CancerPreprint
Eder, I., Baghaei, M., Maurya, S. K., Yu, V., Wilson, E., Kashkoush, A., Liu, J.-J., Liu, S., Luo, J., Storkus, W. J., et al. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.06.05.730362

Authors: Barascu, A., Le Chalony, C., Pennarun, G., Genet, D., Imam, N., Lopez, B., & Bertrand, P.
Affiliations: Centre National de la Recherche Scientifique (FR)
Corresponding author: Bertrand, Pascale
ORCID: Pennarun, Gaëlle
Genet, Diane
Bertrand, Pascale
Venue: The EMBO Journal
Publisher: Springer Science and Business Media LLC
Published: 2012-01-13
Volume: 31
Issue: 5
Pages: 1080-1094
ISSN: 0261-4189 (ISSN-L)
1460-2075
DOI: 10.1038/emboj.2011.492
PMC: PMC3297999
OpenAlex: W2160703969
Cited by: 206
References: 84
Citations by year: 2026: 6 · 2025: 14 · 2024: 12 · 2023: 8 · 2022: 11 · 2021: 16 · 2020: 17 · 2019: 9 · 2018: 12 · 2017: 12 · 2016: 17 · 2015: 15 · 2014: 24 · 2013: 15 · 2012: 18
FWCI: 9.25
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.springernature.com/gp/researchers/text-and-data-mining (tdm)
www.springernature.com/gp/researchers/text-and-data-mining (vor)
Locations: The EMBO Journal (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nuclear Structure and Function
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Telomeres, Telomerase, and Senescence
Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
Keywords: oxidative stress, cellular senescence, ATM, lamin B1, p38 MAPK, ataxia telangiectasia, DNA damage response, stress-induced senescence, oncogene-induced senescence, nuclear organization, premature aging
MeSH terms: Aging, Cells, Cultured, Humans, Signal Transduction, Oxidative Stress, Lamin Type B, p38 Mitogen-Activated Protein Kinases

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Oxidative stress induces an ATM‐independent senescence pathway through p38 MAPK‐mediated lamin B1 accumulation

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