Senescent cells suppress innate smooth muscle cell repair functions in atherosclerosis
Open accessAbstract
Senescent cells (SNCs) degenerate the fibrous cap that normally prevents atherogenic plaque rupture, a leading cause of myocardial infarction and stroke. Here we explored the underlying mechanism using pharmacological or transgenic approaches to clear SNCs in the Ldlr -/- mouse model of atherosclerosis. SNC clearance reinforced fully deteriorated fibrous caps in highly advanced lesions, as evidenced by restored vascular smooth muscle cell (VSMC) numbers, elastin content, and overall cap thickness. We found that SNCs inhibit VSMC promigratory phenotype switching in the first interfiber space of the arterial wall directly beneath atherosclerotic plaque, thereby limiting lesion entry of medial VSMCs for fibrous cap assembly or reinforcement. SNCs do so by antagonizing IGF-1 through the secretion of insulin-like growth factor-binding protein 3 (Igfbp3). These data indicate that the intermittent use of senolytic agents or IGFBP-3 inhibition in combination with lipid lowering drugs may provide therapeutic benefit in atherosclerosis.
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The findings are consistent with previous studies suggesting senescent cells contribute to fibrous cap thinning, although differences in other aspects could be due to different animal models, detection methods, traits examined, and time points.
“our findings are consistent with previous studies suggesting that senescent cells contribute to fibrous cap thinning, although differences in other aspects of these studies, such as gene expression changes, could be attributed to the use of different animal models, methods of detection, traits examined and time points studied48.”
From Single-cell and spatial transcriptomics map senescent vascular cells in arterial remodeling during atherosclerosis in mice (2025) · cites this paper as [48]
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Experimental — accuracy not yet measuredSenescent cells contribute to the initiation and progression of various aging-related chronic diseases.
“and contribute to the initiation and progression of various aging-related chronic diseases.9,10,11”
From Single-cell senescence identification reveals senescence heterogeneity, trajectory, and modulators (2024) · cites this paper as [10]
The Abstract links senescent cells at sites of age-related pathologies to tissue degeneration and dysfunction, and the Abstract and Discussion describe their harmful role in atherosclerosis. The paper does not establish that senescent cells contribute to both the initiation and progression of various chronic diseases; its mechanistic findings concern atherosclerosis in mice. (LLM, conf=0.82)
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BackgroundSenescent Cells: A Therapeutic Target in Cardiovascular Diseases
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“The senescent cells antagonize insulinlike growth factor (IGF)-1 through the secretion of IGF-binding protein-3, thereby inhibiting innate smoothmuscle cell repair (Childs et al., 2021).”
BackgroundRecent advances of traditional Chinese medicine for the prevention and treatment of atherosclerosis
Zhi, W., Liu, Y., Wang, X., & Zhang, H. (2022) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2022.115749 · Cited by 85 · see citing works
Cellular senescence links mitochondria-ER contacts and aging
Ziegler, D. V., Martin, N., & Bernard, D. (2021) · Communications Biology · doi:10.1038/s42003-021-02840-5 · Cited by 85 · see citing works
Mechanisms of fibrous cap formation in atherosclerosis
Alonso-Herranz, L., Albarrán-Juárez, J., & Bentzon, J. F. (2023) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2023.1254114 · Cited by 72 · see citing works
“Treatment with navitoclax in hyperlipidemic Ldlr-/- mice Mouse Anti-apoptotic BCL-2 pathways Clearance of senescent cells Enhanced fibrous cap thickness and more elastin and ACTA2 + cells in the fibrous cap Histological and immunohistochemical analysis (51) Alonso-Herranz et al.”
MethodCardiovascular aging: spotlight on mitochondria
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Cellular Senescence as a Targetable Risk Factor for Cardiovascular Diseases
Kumar, M., Yan, P., Kuchel, G. A., & Xu, M. (2024) · JACC Basic to Translational Science · doi:10.1016/j.jacbts.2023.12.003 · Cited by 56 · see citing works
Targeting cellular senescence as a novel treatment for osteoarthritis
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Endothelial IGFBP6 suppresses vascular inflammation and atherosclerosis
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“40).”
Association between dietary patterns and cardiovascular diseases: A review
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“In the context of health, immune cells facilitate the removal of senescent cells, while in disease they can instead amplify the proinflammatory SASP (Behmoaras & Gil, 2021; Sturmlechner et al., 2021).”
BackgroundSelf-citationMazan-Mamczarz, K., Tsitsipatis, D., Childs, B. G., Carr, A. E., Dos Santos, C. R., Anerillas, C., Romero, B., Gregg, J. M., Henry-Smith, C., Okereke, A. N., et al. (2025) · Nature Aging · doi:10.1038/s43587-025-00889-z · Cited by 37 · see citing works
“** P ≤ 0.01. changes, could be attributed to the use of different animal models, methods of detection, traits examined and time points studied 48 .”
InfluentialSelf-citationAnti-ageing interventions for the treatment of cardiovascular disease
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“167 Antiatherosclerotic effects were similarly reported in response to senolysis in male ApoE − / − mice.”
Potential Clinical Implications of Senotherapies for Cardiovascular Disease
Suda, M., Katsuumi, G., Tchkonia, T., Kirkland, J. L., & Minamino, T. (2023) · Circulation Journal · doi:10.1253/circj.cj-23-0657 · Cited by 37 · see citing works
Miscarriage syndrome: Linking early pregnancy loss to obstetric and age-related disorders
Bortoletto, P. E., Lucas, E. S., Melo, P., Gallos, I. D., Devall, A., Bourne, T., Quenby, S. M., Bennett, P. R., Coomarasamy, A., & Brosens, J. J. (2022) · EBioMedicine · doi:10.1016/j.ebiom.2022.104134 · Cited by 33 · see citing works
Gulej, R., Csík, B., Faakye, J., Tarantini, S., Shanmugarama, S., Chandragiri, S. S., Mukli, P., Conley, S. M., Csiszár, A., Ungvari, Z. I., et al. (2023) · Microcirculation · doi:10.1111/micc.12840 · Cited by 32 · see citing works
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Karnewar, S., Karnewar, V., Shankman, L. S., & Owens, G. K. (2024) · JCI Insight · doi:10.1172/jci.insight.173863 · Cited by 31 · see citing works
“…aortic arch lesions of Myh11-CreER T2 TdTomato Ldlr –/– male mice fed a WD for 14 weeks, followed by 9 weeks of a low-fat diet (LFD) and treatment with ABT-263, had a reduced proportion of tdTomato + cells that expressed the osteochondrogenic marker Runx1 as compared with vehicle-treated mice (26).”
BackgroundResultInfluentialTakaya, K., Asou, T., & Kishi, K. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24065857 · Cited by 29 · see citing works
“For example, the therapeutic potential of senescent cell removal has been demonstrated in mouse models of diverse diseases and disorders, including pulmonary fibrosis [2,3], atherosclerosis [4,5], diabetes [6,7], and neurodegeneration [8,9].”
BackgroundMas‐Bargues, C., Borrás, C., & Alique, M. (2022) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2022.854726 · Cited by 29 · see citing works
The role of cellular senescence in cardiovascular disease
Xu, C., Qiu, Z., Guo, Q., Huang, Y., Zhao, Y., & Zhao, R. (2025) · Cell Death Discovery · doi:10.1038/s41420-025-02720-5 · Cited by 31 · see citing works
“These data indicate that the intermittent use of senolytic agents or IGFBP-3 inhibition in combination with lipid-lowering drugs may provide therapeutic bene fi t in atherosclerosis [111].”
Cell non-autonomous regulation of cerebrovascular aging processes by the somatotropic axis
Bickel, M. A., Csík, B., Gulej, R., Ungvari, A., Nyúl‐Tóth, Á., & Conley, S. M. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1087053 · Cited by 28 · see citing works
Anti-senescence therapies: a new concept to address cardiovascular disease
Stojanović, S. D., Thum, T., & Bauersachs, J. K. (2025) · Cardiovascular Research · doi:10.1093/cvr/cvaf030 · Cited by 28 · see citing works
Kaistha, A., Oc, S., Garrido, A. M., Taylor, J. C. K., Imaz, M., Worssam, M. D., Uryga, A., Grootaert, M. O. J., Foote, K., Finigan, A. J., et al. (2025) · Cardiovascular Research · doi:10.1093/cvr/cvaf102 · Cited by 28 · see citing works
“Our findings also differ from other studies suggesting that senescent cells reduce VSMC migration through soluble growth factor inhibitors such as IGFBP3, 9 while we find similar numbers of VSMCs in fibrous caps, and IGFBP3 was not induced by senescent human VSMCs.”
From the divergence of senescent cell fates to mechanisms and selectivity of senolytic drugs
L’Hôte, V., Mann, C., & Thuret, J. (2022) · Open Biology · doi:10.1098/rsob.220171 · Cited by 26 · see citing works
Sutanto, H., Fetarayani, D., Narendra, M. R., & Nasution, S. A. (2025) · European Journal of Internal Medicine · doi:10.1016/j.ejim.2025.106488 · Cited by 30 · see citing works
Simoncini, S., Toupance, S., Labat, C., Gautier, S., Dumoulin, C., Arnaud, L., Stathopoulou, M. G., Visvikis‐Siest, S., Rossi, P. M., Bénétos, A., et al. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23168969 · Cited by 24 · see citing works
“The results reported in the present study agree with other studies demonstrating changes in senescence of endothelial and vascular smooth muscle cells in atherosclerotic lesions [38–42].”
ResultXin, Y., Yuan, Z., Wang, J., & Li, S. (2025) · The FASEB Journal · doi:10.1096/fj.202500244rrr · Cited by 27 · see citing works
“In the Ldlr − / − mouse model of AS, the removal of senescent cells augmented the fully degraded fibrous cap, which normally prevents rupture of atherogenic plaques [131, 132].”
Zhang, W., Wang, L., Wang, Y., Fang, Y., Cao, R., Fang, Z., Han, D. G., Huang, X., Gu, Z., Zhang, Y., et al. (2024) · Science China Life Sciences · doi:10.1007/s11427-024-2602-7 · Cited by 22 · see citing works
“Targeted clearance of senescent cells significantly reduces plaque number and area, increases fibrous cap thickness, and maintains plaque stability (Childs et al., 2016; Childs et al., 2021).”
Targeting vascular senescence in cardiovascular disease with aging
Hall, S. A., & Lesniewski, L. A. (2024) · The Journal of Cardiovascular Aging · doi:10.20517/jca.2023.45 · Cited by 25 · see citing works
“In studies using pharmacological or transgenic approaches to eliminate senescent cells in the Ldlr −/− mouse model of atherosclerosis, the removal of senescent cells protected deteriorated fibrous caps in atherosclerotic lesions, reduced inflammation, and improved vascular function [74] .”
BackgroundZhang, G., Cui, X., Qin, Z., Wang, Z., Lu, Y., Xu, Y., Xu, S., Tang, L., Zhang, L., Liu, G., et al. (2023) · iScience · doi:10.1016/j.isci.2023.107587 · Cited by 21 · see citing works
Cells in Atherosclerosis: Focus on Cellular Senescence from Basic Science to Clinical Practice
Molnár, A., Pásztor, D. T., Tarcza, Z., & Merkely, B. P. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms242417129 · Cited by 21 · see citing works
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“In the advanced phases of atherosclerosis, the proliferation of vascular smooth muscle cells (VSMCs) is crucial, which contributes to the formation and repair of the fibrous cap, thus maintaining plaque stability (Childs et al. 2021; Wang et al. 2015).”
Mahoney, S. A., Dey, A. K., Basisty, N., & Herman, A. B. (2023) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00352.2023 · Cited by 20 · see citing works
Role of vascular smooth muscle cell clonality in atherosclerosis
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Insulin-like Growth Factor-Binding Protein-1 (IGFBP-1) as a Biomarker of Cardiovascular Disease
LEWITT, M. S., & Boyd, G. W. (2024) · Biomolecules · doi:10.3390/biom14111475 · Cited by 17 · see citing works
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Lysosome Functions in Atherosclerosis: A Potential Therapeutic Target
Wang, Z., Li, X., Moura, A. K., Hu, J. Z., Wang, Y., & Zhang, Y. (2025) · Cells · doi:10.3390/cells14030183 · Cited by 13 · see citing works
“Indeed, defects in autophagy in VSMCs can promote their proliferation and migration, thereby contributing to the progression of atherosclerotic plaques [70].”
Mechanisms of cellular senescence-induced vascular aging: evidence of senotherapeutic strategies
Mahoney, S. A., Bloom, S. I., Seals, D. R., Donato, A. J., Rossman, M. J., & Clayton, Z. S. (2025) · The Journal of Cardiovascular Aging · doi:10.20517/jca.2024.31 · Cited by 15 · see citing works
“Although several studies found favorable effects of senolytic treatment on atherosclerotic plaques [36,85,188,194,195] , two studies found that senescent cell clearance worsened outcomes, including plaque instability and rupture in advanced stages of atherosclerosis [186,187] .”
Postmus, A. C., Kruit, J. K., Eilers, R. E., Havinga, R., Koster, M. H., Johmura, Y., Nakanishi, M., van de Sluis, B., & Jonker, J. W. (2023) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2023.116531 · Cited by 8 · see citing works
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“SMC and endothelial cell senescence may also affect lesion stability by amplifying inflammation and producing proteases against the fibrous cap [23,24].”
InfluentialThe senescent heart and atrial fibrillation
Pandey, A. C., Bidaoui, G., Younes, H., Tsakiris, E., & Marrouche, N. F. (2025) · Heart Rhythm · doi:10.1016/j.hrthm.2025.06.005 · Cited by 6 · see citing works
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“Moreover, reduced SPM synthesis and SMC senescence restrict collagen synthesis and fibrous cap repair [154].”
Lu, J., Wang, J., Liu, Y., Zhang, C., Zhang, G., Ge, Y., & Liu, L. (2025) · Cardiovascular Diabetology · doi:10.1186/s12933-025-02976-2 · Cited by 6 · see citing works
“Therapeutic strategies targeting senescent cells, including senomor-phic drugs that reduce senescence and senolytic drugs that eliminate these cells, have demonstrated protective effects against atherosclerosis in animal models [2, 4, 5].”
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Cellular senescence as a source of chronic microinflammation that promotes the aging process
Nakanishi, M. (2025) · Proceedings of the Japan Academy Series B · doi:10.2183/pjab.101.014 · Cited by 5 · see citing works
Nanotechnology for atherosclerotic plaque stabilisation: bridging innovation and clinical practice
Ren, Y., Zhou, Y., Xiang, B., Li, Q., & Zhou, X. (2026) · EBioMedicine · doi:10.1016/j.ebiom.2025.106102 · Cited by 3 · see citing works
“73 This represents a novel and interesting target for nano-intervention.”
Steegen, L., & Grootaert, M. O. J. (2026) · Cells · doi:10.3390/cells15020114 · Cited by 4 · see citing works
“Using SMC lineage-tracing techniques, the authors further showed that senolytic therapy enhances the number of vimentin+ SMC-derived cells—which are considered to be promigratory—in the SMC layer of the media underneath and closest to the plaque (which are called the first interfiber space) [9].”
InfluentialExploiting senescence as a therapeutic target in osteoarthritis
Larbie, C., & Raza, U. (2024) · Asia-Pacific Journal of Pharmacotherapy & Toxicology · doi:10.32948/ajpt.2024.11.19 · Cited by 3 · see citing works
The fat‐heart entanglement and the role of ‘osteopontin mechanics’ in cardiometabolic senescence
Michelauz, C., Montecucco, F., Liberale, L., & Carbone, F. (2026) · European Journal of Clinical Investigation · doi:10.1111/eci.70181 · Cited by 2 · see citing works
Epigenetic dynamics of cellular senescence: From mechanistic insights to precision senotherapy
Hu, X., Lai, W., Liu, M., & Wang, B. (2026) · Chinese Medical Journal · doi:10.1097/cm9.0000000000004042 · Cited by 2 · see citing works
“Although early studies have reported beneficial effects of navitoclax treatment in atherosclerotic mice, [156] subsequent research by Karnewar et al [157] reveals that navitoclax treatment in mice fed with a western diet (WD) with advanced atherosclerosis and persistent hyperlipidemia results in…”
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Aregs-IGFBP3-mediated SMC-like cells apoptosis impairs beige adipocytes formation in aged mice
Wang, S.-F., Cui, Y.-X., Wang, L., Feng, C., Sun, Y.-F., Huo, B., Jiang, H., Zhao, M., Tu, Y.-Y., Wang, Q.-Y., et al. (2025) · Molecular Metabolism · doi:10.1016/j.molmet.2025.102125 · Cited by 2 · see citing works
“Speci fi cally, IGFBP3 binds to IGFs, inhibiting its interaction with the IGFs receptors, thereby reducing IGFs signaling activity [20 e 23].”
Senescence in Aging, Within the Brain and Other Diseases: Mechanisms and Interventions
Chakrabarti, S. K., & Chattopadhyay, D. (2023) · Exploratory Research and Hypothesis in Medicine · doi:10.14218/erhm.2023.00018 · Cited by 2 · see citing works
Karnewar, S., Karnewar, V., Shankman, L. S., & Owens, G. K. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.07.12.548696 · Cited by 2 · see citing works
“First, they found that “presumed” selective clearance of senescent cells using a p16 driven thymidine kinase genetic approach similar to Childs et al.25 did not reduce Oil red O+ plaque burden, aortic root lesion size, fibrous cap thickness, or necrotic core area in Apoe-/- mice (males and females combined), but inste…”
InfluentialMazan-Mamczarz, K., Tsitsipatis, D., Carr, A. E., Childs, B. G., Santos, C. R. D., Anerillas, C., Romero, B., Gregg, J. M., Michel, M., Munk, R. B., et al. (2023) · Research Square · doi:10.21203/rs.3.rs-3235572/v1 · Cited by 2 · see citing works
Self-citationSNCs meet SMCs in the atherosclerotic plaque
Kabir, I., & Greif, D. M. (2021) · Nature Aging · doi:10.1038/s43587-021-00096-6 · Cited by 1 · see citing works
Siracusa, C., Canino, G., Scalise, M., Marino, F., Pagano, L., Santamaria, G., Torella, A., Rosa, S. D., Torella, D., & Cianflone, E. (2025) · Cells · doi:10.3390/cells14201641 · Cited by 1 · see citing works
“…growth arrest but may create a pro-inflammatory, matrix-remodeling milieu that could compromise long-term arterial stability—a working hypothesis that fits with reports showing that senescent VSMCs and their SASP drive features of plaque progression and fragility in atherosclerosis [28,39,40].”
Tang, H., Liu, Z., Qi, B., Huang, Y., Yuan, D., Cheng, X., Zhao, R., Zhang, B., & Liu, J. (2026) · Journal of King Saud University - Science · doi:10.25259/jksus_1072_2025 · Cited by 1 · see citing works
The Biological Mechanisms of Frailty: Focusing on Cellular Senescence
Erusalimsky, J. D. (2026) · European Cardiology Review · doi:10.15420/ecr.2025.81 · Cited by 1 · see citing works
“55,62”
Ma, D., Wang, Z., Ji, C., Wang, Y., Zhang, Y., Qu, L., Shi, L., & Mao, R. (2026) · Ageing Research Reviews · doi:10.1016/j.arr.2026.103215 · Cited by 1 · see citing works
Li, T., Niu, X., Lu, L., Liang, Y., & Zhang, L. (2026) · Reviews in Cardiovascular Medicine · doi:10.31083/rcm50363 · Cited by 1 · see citing works
“It may even serve as an intermediate state facilitating the transition of VSMCs into other pathological phenotypes, such as fibroblast-like or fibrochondrocyte-like cells [95,96].”
Application of senescence reporter mouse models in panvascular diseases
Li, H., Zhang, Y., Tian, Z., & Zhang, S. (2025) · Vessel Plus · doi:10.20517/2574-1209.2025.99
Self-citationSenolytic drug discovery and mechanisms of action in BRAF-V600E oncogene-induced senescence
L’Hôte, V. (2022) · theses.fr (ABES) · doi:10.70675/acd5f426zc1b2z446fz8404z0f8f121081f8
Zhao, H., Ren, W., Jiang, H., Zhou, R., Deng, Y., Huang, H., & Wang, P. (2026) · International Journal of General Medicine · doi:10.2147/ijgm.s599029
“22 In the ApoE −/− model, Wang et al 23 assessed plaque stability and reported an increase in collagen content accompanied by a reduction in MMP-9 positive area.”
Jianpi Qutan Formula attenuates vulnerable plaques by regulating IGFBP3
yang, M., Liu, Y., Yu, M., wang, T., Zhang, H., Fan, H., & Yang, Z. (2026) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2026.122035
Cellular senescence at the bidirectional interface between ageing and coronary artery disease
Li, X., Zhang, H., Chen, M., Wang, Y., Wang, K., Xu, X., Wang, J., Zhu, Q., Zhao, C., Wang, C., et al. (2026) · Ageing Research Reviews · doi:10.1016/j.arr.2026.103284
The senescence–immune axis as a target for combining immunotherapy and senotherapy
Saez‐Calazans, F., Grün, L. K., Stein, L. E., Barbé‐Tuana, F. M., & Filippi‐Chiela, E. C. (2026) · Ageing Research Reviews · doi:10.1016/j.arr.2026.103309
Li, H., Song, A., Zhang, J., Dong, H., Li, X., & Zhao, Y. (2026) · Cardiovascular Drugs and Therapy · doi:10.1007/s10557-026-07956-6
Self-citationLiu, Z., He, Y., & Zhu, W. (2026) · Integrative Biology · doi:10.1093/intbio/zyag022
- Authors
- Childs, B. G., Zhang, C., Shuja, F., Sturmlechner, I., Trewartha, S., Velasco, R. F., Baker, D. J., Li, H., & van Deursen, J. M.
- Affiliations
- Mayo Clinic (US)
- ORCID
- Venue
- Nature Aging
- Published
- 2021-08-02
- Volume
- 1
- Issue
- 8
- Pages
- 698-714
- ISSN
- 2662-8465 (ISSN-L)
- PMC
- PMC8570576
- OpenAlex
- W3187881836
- Cited by
- 76
- References
- 73
- Citations by year
- 2026: 15 · 2025: 18 · 2024: 12 · 2023: 18 · 2022: 10 · 2021: 3
- FWCI
- 4.01
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- Locations
- Nature Aging (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion, other-oa)
- Funders
- U.S. Department of Health & Human Services | National Institutes of Health (AG57493, AG049672)
- Keck Foundation Glenn Foundation for Medical Research
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Atherosclerosis and Cardiovascular Diseases
- Health Sciences › Medicine › Physiology › Telomeres, Telomerase, and Senescence
- Health Sciences › Medicine › Surgery › Cholesterol and Lipid Metabolism
- Keywords
- senescent cells, senolytics, atherosclerosis, vascular smooth muscle cells, IGF binding protein-3, insulin-like growth factor I, smooth muscle cell migration, plaque rupture, Ldlr-deficient mice, elastin, lipid-lowering therapy
- MeSH terms
- Animals, Myocardial Infarction, Cellular Senescence, Myocytes, Smooth Muscle, Atherosclerosis, Mice, Plaque, Atherosclerotic
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