Vascular smooth muscle cell senescence in atherosclerosis

GORENNE, I; KAVURMA, M; SCOTT, S; BENNETT, M

doi:10.1016/j.cardiores.2006.06.004

Cited by 196Telomeres, Telomerase, and SenescenceAtherosclerosis and Cardiovascular DiseasesNitric Oxide and Endothelin Effects

Vascular smooth muscle cell senescence in atherosclerosis

GORENNE, I, KAVURMA, M, SCOTT, S, BENNETT, M·2006·Cardiovascular Research

DOI 10.1016/j.cardiores.2006.06.004

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Abstract

Markers of cell senescence have been identified in both the blood and vessel wall of patients with atherosclerosis. In particular, vascular smooth muscle cells (VSMCs) derived from human plaques show numerous features of senescence both in culture and in vivo. This review summarises the evidence for VSMC senescence in atherosclerosis, and outlines the mechanisms and triggers leading to their senescence.

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Senescent endothelial and smooth muscle cells have been implicated in the genesis or promotion of age-related cardiovascular disease.
“In addition, senescent endothelial and smooth muscle cells have been implicated in the genesis or promotion of age-related cardiovascular disease (126, 127).”
From Aging, Cellular Senescence, and Cancer (2013) · cites this paper as [127]
Unstable mature plaques show low VSMC proliferation and clear evidence of VSMC senescence.
“Unstable mature plaques show low VSMC proliferation and clear evidence of VSMC senescence 191 .”
From Vascular smooth muscle cells in atherosclerosis (2019) · cites this paper as [191]

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Sorted by citations

Aging, Cellular Senescence, and Cancer
Campisi, J. (2013) · Annual Review of Physiology · doi:10.1146/annurev-physiol-030212-183653 · Cited by 2,954 · see citing works
“In addition, senescent endothelial and smooth muscle cells have been implicated in the genesis or promotion of age-related cardiovascular disease (126, 127).”
Background
Senescent intimal foam cells are deleterious at all stages of atherosclerosis
Childs, B. G., Baker, D. J., Wijshake, T., Conover, C. A., Campisi, J., & van Deursen, J. M. (2016) · Science · doi:10.1126/science.aaf6659 · Cited by 1,195 · see citing works
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Basatemur, G. L., Jørgensen, H. F., Clarke, M. C. H., Bennett, M. R., & Mallat, Z. (2019) · Nature Reviews Cardiology · doi:10.1038/s41569-019-0227-9 · Cited by 1,099 · see citing works
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Recapitulation of premature ageing with iPSCs from Hutchinson-Gilford progeria syndrome
Liu, G.-H., Barkho, B. Z., Ruiz, S., Diep, D., Qu, J., Yang, S.-L., Panopoulos, A. D., Suzuki, K., Kurian, L., Walsh, C., et al. (2011) · Nature · doi:10.1038/nature09879 · Cited by 575 · see citing works
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Cellular senescence: a link between cancer and age-related degenerative disease?
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“The proinflammatory SASP of senescent endothelial cells has also been proposed to contribute to cardiovascular disease by initiating and fueling the development of atherosclerotic lesions [35, 58].”
Background
Senescent vascular smooth muscle cells drive inflammation through an interleukin-1α-dependent senescence-associated secretory phenotype
Gardner, S. E., Humphry, M., Bennett, M. R., & Clarke, M. C. H. (2015) · Arteriosclerosis, Thrombosis, and Vascular Biology · doi:10.1161/atvbaha.115.305896 · Cited by 285 · see citing works
“However, unstable mature plaques show low levels of VSMC proliferation and clear evidence of VSMC senescence.(6) Similarly, restenotic neointimas also contain senescent VSMCs.”
BackgroundSelf-citation
Defective autophagy in vascular smooth muscle cells accelerates senescence and promotes neointima formation and atherogenesis
Grootaert, M. O., da Costa Martins, P. A., Bitsch, N., Pintelon, I., De Meyer, G. R., Martinet, W., & Schrijvers, D. M. (2015) · Autophagy · doi:10.1080/15548627.2015.1096485 · Cited by 267 · see citing works
“Different research groups have shown that VSMC senescence is present in atherosclerotic plaques and contributes to the pathogenesis of atherosclerosis.(21,32,53,54) Our observations confirm once more the dual role of VSMCs in atherosclerosis.”
Background
Impact of cellular senescence signature on ageing research
Sikora, E., Arendt, T., Bennett, M., & Narita, M. (2011) · Ageing Research Reviews · doi:10.1016/j.arr.2010.10.002 · Cited by 264 · see citing works
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Vascular Cell Senescence Contributes to Blood–Brain Barrier Breakdown
Yamazaki, Y., Baker, D. J., Tachibana, M., Liu, C.-C., van Deursen, J. M., Brott, T. G., Bu, G., & Kanekiyo, T. (2016) · Stroke · doi:10.1161/strokeaha.115.010835 · Cited by 263 · see citing works
Sirtuins, Cell Senescence, and Vascular Aging
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DNA Damage Links Mitochondrial Dysfunction to Atherosclerosis and the Metabolic Syndrome
Mercer, J. R., Cheng, K., Figg, N. L., Gorenne, I., Mahmoudi, M., Griffin, J. L., Vidal‐Puig, A., Logan, A., Murphy, M. P., & Bennett, M. R. (2010) · Circulation Research · doi:10.1161/circresaha.110.218966 · Cited by 240 · see citing works
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Signaling pathways involved in vascular smooth muscle cell calcification during hyperphosphatemia
Voelkl, J. G. J., Lang, F. J. W., Eckardt, K., Amann, K., Kuro‐o, M., Pasch, A., Pieske, B. M., & Alesutan, I. (2019) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-019-03054-z · Cited by 221 · see citing works
TRAP1 drives smooth muscle cell senescence and promotes atherosclerosis via HDAC3-primed histone H4 lysine 12 lactylation
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Telomeres and Telomerase in Cardiovascular Diseases
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“The senescent VSMCs in atherosclerotic plaque also exhibit limited capacity of proliferation with increased activity of matrix-degrading enzymes as well as promote the thinning of fibrous caps and plaque rupture, which may lead to subsequent thrombosis, MI, or stroke [30].”
Background
Generation of a p16 Reporter Mouse and Its Use to Characterize and Target p16high Cells In Vivo
Omori, S., Wang, T.-W., Johmura, Y., Kanai, T., Nakano, Y., Kido, T., Susaki, E. A., Nakajima, T., Shichino, S., Ueha, S., et al. (2020) · Cell Metabolism · doi:10.1016/j.cmet.2020.09.006 · Cited by 194 · see citing works
Telomere biology and age-related diseases
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Nucleotide Excision DNA Repair Is Associated With Age-Related Vascular Dysfunction
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Angiotensin II–Mediated Oxidative DNA Damage Accelerates Cellular Senescence in Cultured Human Vascular Smooth Muscle Cells via Telomere-Dependent and Independent Pathways
Herbert, K. E., Mistry, Y., Hastings, R., Poolman, T. M., Niklason, L. E., & Williams, B. (2007) · Circulation Research · doi:10.1161/circresaha.107.158626 · Cited by 191 · see citing works
Senescence as a therapeutic target in cancer and age-related diseases
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“…ageing but are also present in fibrotic 12,62 and many other diseased tissues and in diseases as diverse as type 2 diabetes 63 , atherosclerosis 64,65 , non-alcoholic fatty liver disease 66 , Alzheimer disease, retinopathy 67 , idiopathic pulmonary fibrosis (IPF) 62 or osteoarthritis 68,69…”
Cellular Senescence in Cardiovascular Diseases: A Systematic Review
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“Specifically, the occurrence of VSMCs senescence in atherosclerosis has been reviewed previously (as reviewed in Ref [70,72]).”
New insight into dyslipidemia‐induced cellular senescence in atherosclerosis
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Mitochondria in vascular disease
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“Importantly, the senescence of VSMCs could potentially contribute to inefficient plaque repair, with resulting plaque instability.(99)”
BackgroundSelf-citation
The multifaceted role of the SASP in atherosclerosis: from mechanisms to therapeutic opportunities
Sun, Y., Wang, X., Liu, T., Zhu, X., & Pan, X. (2022) · Cell & Bioscience · doi:10.1186/s13578-022-00815-5 · Cited by 151 · see citing works
Extracellular matrix alterations in senescent cells and their significance in tissue homeostasis
Mavrogonatou, E., Pratsinis, H., Papadopoulou, A., Karamanos, N. K., & Kletsas, D. (2019) · Matrix Biology · doi:10.1016/j.matbio.2017.10.004 · Cited by 153 · see citing works
A comparison of replicative senescence and doxorubicin-induced premature senescence of vascular smooth muscle cells isolated from human aorta
Bielak-Zmijewska, A., Wnuk, M., Przybylska, D., Grabowska, W., Lewinska, A., Alster, O., Korwek, Z., Cmoch, A., Myszka, A., Pikula, S., et al. (2014) · Biogerontology · doi:10.1007/s10522-013-9477-9 · Cited by 139 · see citing works
“…e-mail: g.mosieniak@nencki.gov.pl E. Sikora e-mail: e.sikora@nencki.gov.pl M. Wnuk A. Myszka Department of Genetics, University of Rzeszow, Rzeszow, Poland e-mail: mawnuk@gmail.com A. Myszka e-mail: amyszka@o2.pl Keywords Senescence VSMCs Doxorubicin Aging Cardiovascular diseases Calcification”
Background
The Role of Curcumin in the Modulation of Ageing
Bielak-Żmijewska, A., Grabowska, W., Ciolko, A., Bojko, A., Mosieniak, G., Bijoch, Ł., & Sikora, E. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20051239 · Cited by 143 · see citing works
Smooth Muscle Cells Healing Atherosclerotic Plaque Disruptions Are of Local, Not Blood, Origin in Apolipoprotein E Knockout Mice
Bentzon, J. F., Søndergaard, C. S., Kassem, M. S., & Falk, E. (2007) · Circulation · doi:10.1161/circulationaha.107.722355 · Cited by 136 · see citing works
Cellular senescence links aging and diabetes in cardiovascular disease
Shakeri, H., Lemmens, K., Gevaert, A. B., De Meyer, G. R. Y., & Segers, V. F. M. (2018) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00287.2018 · Cited by 134 · see citing works
“VSMCs in atherosclerotic plaques show signs of cellular senescence, such as increased SA- -Gal activity, upregulation of cell cycle regulators (p16 and p21), decreased telomerase activity, and telomere shortening (63, 121, 129).”
Background
Mitochondrial DNA damage and atherosclerosis
Yu, E. P. K., & Bennett, M. R. (2014) · Trends in Endocrinology & Metabolism · doi:10.1016/j.tem.2014.06.008 · Cited by 124 · see citing works
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Vascular Smooth Muscle Cells: Isolation, Culture, and Characterization
Metz, R. P., Patterson, J. L., & Wilson, E. (2011) · Methods in molecular biology · doi:10.1007/978-1-61779-523-7_16 · Cited by 115 · see citing works
Senescent Cells: A Therapeutic Target in Cardiovascular Diseases
Suda, M., Paul, K. H., Minamino, T., Miller, J. D., Lerman, A., Ellison, G. M., Tchkonia, T., & Kirkland, J. L. (2023) · Cells · doi:10.3390/cells12091296 · Cited by 116 · see citing works
“Accumulation of senescent VSMCs in atherosclerotic plaques is evidenced by reduced proliferation [114], larger and flatter cell morphology [115], increased expression of p16 INK4a and p21 CIP1/WAF1 [116], and shortened or dysfunctional telomeres [116].”
Background
Phenotypic switching of vascular smooth muscle cells in the ‘normal region’ of aorta from atherosclerosis patients is regulated by miR‐145
Zhang, Y., Xie, B., Sun, L., Chen, W., Jiang, S., Liu, W., Bian, F., Tian, H., & Li, R. (2016) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.12825 · Cited by 109 · see citing works
Metabolic syndrome, diabetes and atherosclerosis: Influence of gene–environment interaction
Andreassi, M. G. (2008) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2008.10.018 · Cited by 108 · see citing works
The Impact of Uremic Toxins on Vascular Smooth Muscle Cell Function
Hénaut, L., Mary, A., Chillon, J., Kamel, S., & Massy, Z. A. (2018) · Toxins · doi:10.3390/toxins10060218 · Cited by 106 · see citing works
“They have short telomeres, accumulate prelamin A, and contain elevated levels of senescence-associated markers (including senescence-associated β-galactosidase (SAβG) and cell cycle regulators (such as p16, p21, p53, and pRb) [119].”
Background
The TGF-β1/p53/PAI-1 Signaling Axis in Vascular Senescence: Role of Caveolin-1
Samarakoon, R., Higgins, S. P., Higgins, C. E., & Higgins, P. J. (2019) · Biomolecules · doi:10.3390/biom9080341 · Cited by 102 · see citing works
“, G1 stalling or arrest, reduced S phase cohort) and shortened life span [15].”
Background
Telomeres and Age-Related Diseases
Gruber, H., Semeraro, M. D., Renner, W., & Herrmann, M. (2021) · Biomedicines · doi:10.3390/biomedicines9101335 · Cited by 96 · see citing works
“Senescent VSMCs harbor a limited proliferative capacity and an increased amount of matrix-degrading enzymes, which stimulate the thinning of fibrous caps and plaque rupture [111].”
Background
Cellular senescence of renal tubular epithelial cells in acute kidney injury
Chen, J., Zhang, H., Yi, X., Dou, Q., Yang, X., Chen, J., Chen, J., & Chen, K. (2024) · Cell Death Discovery · doi:10.1038/s41420-024-01831-9 · Cited by 97 · see citing works
“Senescent smooth muscle cells, for instance, secrete IL-6 and IL-8, which in turn promote the proliferation and migration of adjacent smooth muscle cells, ultimately leading to pulmonary arterial hypertension [65].”
Background
Signaling mechanisms of angiotensin II in regulating vascular senescence
Min, L., Mogi, M., Iwai, M., & Horiuchi, M. (2009) · Ageing Research Reviews · doi:10.1016/j.arr.2008.12.002 · Cited by 93 · see citing works
Telomere biology in cardiovascular disease: the TERC-/- mouse as a model for heart failure and ageing
Wong, L. S. M., Oeseburg, H., de Boer, R. A., van Gilst, W. H., van Veldhuisen, D. J., & van der Harst, P. (2008) · Cardiovascular Research · doi:10.1093/cvr/cvn337 · Cited by 88 · see citing works
Age-related loss of SirT1 expression results in dysregulated human vascular smooth muscle cell function
Thompson, A. M., Wagner, R. J., & Rzucidlo, E. M. (2014) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00871.2013 · Cited by 91 · see citing works
Cellular Senescence in Ageing, Age-Related Disease and Longevity
Sikora, E., Bielak-Żmijewska, A., & Mosieniak, G. (2013) · Current Vascular Pharmacology · doi:10.2174/1570161111666131219094045 · Cited by 91 · see citing works
Arginase‐II Induces Vascular Smooth Muscle Cell Senescence and Apoptosis Through p66Shc and p53 Independently of Its l ‐Arginine Ureahydrolase Activity: Implications for Atherosclerotic Plaque Vulnerability
Xiong, Y., Yu, Y., Montani, J., Yang, Z., & Ming, X. (2013) · Journal of the American Heart Association · doi:10.1161/jaha.113.000096 · Cited by 91 · see citing works
“Senescence is characterized by the irreversible loss of the proliferative capability of the cells, which show typical morphological features such as large flattened shape accompanied by an increase in several senescent markers including enhanced senescence-associated b-galactosidase (SA-b-gal) activity, activation of…”
Background
Cellular Senescence in Age‐Related Macular Degeneration: Can Autophagy and DNA Damage Response Play a Role?
Błasiak, J., Piechota, M. J., Pawłowska, E., Szatkowska, M., Sikora, E., & Kaarniranta, K. (2017) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2017/5293258 · Cited by 92 · see citing works
“Senescence of human fibroblasts, described for the first time by Hayflick and Moorehead [10, 11] as a cell division limit in culture, affects not only fibroblasts but also other proliferating somatic human cells, such as keratinocytes and melanocytes [12], lymphocytes [13], epithelial [14] and endothelial [15] cells,…”
Epigenetic regulation of COL15A1 in smooth muscle cell replicative aging and atherosclerosis.
Connelly, J., Cherepanova, O., Doss, J., Karaoli, T., Lillard, T. S., Markunas, C. A., Nelson, S. C., Wang, T.-Y., Ellis, P., Langford, C., et al. (2013) · Human Molecular Genetics · doi:10.1093/hmg/ddt365 · Cited by 83 · see citing works
“The pre-senescent state can be achieved through multiple rounds of SMC replication in vitro (6) and comparison of early and late replicated cells has served as a model of SMC replicative aging (6,9,10).”
Background
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www.elsevier.com/locate/cardiores Review Vascular smooth muscle cell senescence in atherosclerosis
Gorenne, I., Kavurma, M. M., Scott, S., & Bennett, M. (2006)
Self-citation
Vascular Smooth Muscle Cells Undergo Telomere-Based Senescence in Human Atherosclerosis
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Senescence in Vascular Smooth Muscle Cells and Atherosclerosis
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Vascular smooth muscle cell senescence promotes atherosclerosis and features of plaque vulnerability
Uryga, A., Wang, J., Reinhold, J., Gray, K., Figg, N. L., Kumar, S., Baker, L. L., Finigan, A. J., Littlewood, T. D., Clarke, M. C. H., et al. (2015) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2015.04.071 · Cited by 2 · see citing works
Self-citation
Vascular smooth muscle cells undergo telomere-based senescence in human atherosclerosis: effects of telomerase and oxidative stress. Circ Res
Matthews, C., Gorenne, I., Scott, S., Figg, N., Kirkpatrick, P., Ritchie, A., Goddard, M., & Bennett, M. (2016)
Self-citation

Authors: GORENNE, I., KAVURMA, M., SCOTT, S., & BENNETT, M.
Affiliations: University of Cambridge (GB)
Corresponding author: BENNETT, M
ORCID: KAVURMA, M
BENNETT, M
Venue: Cardiovascular Research
Publisher: Oxford University Press (OUP)
Published: 2006-10-01
Volume: 72
Issue: 1
Pages: 9-17
ISSN: 0008-6363 (ISSN-L)
DOI: 10.1016/j.cardiores.2006.06.004
OpenAlex: W2155554546
Cited by: 196
References: 108
Citations by year: 2026: 4 · 2025: 8 · 2024: 11 · 2023: 7 · 2022: 14 · 2021: 15 · 2020: 13 · 2019: 14 · 2018: 9 · 2017: 16 · 2016: 11 · 2015: 12 · 2014: 11 · 2013: 12 · 2012: 8
FWCI: 0.62
Type: journal article
Language: en
Open access: closed
Locations: Cardiovascular Research (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Physiology › Telomeres, Telomerase, and Senescence
Life Sciences › Immunology and Microbiology › Immunology › Atherosclerosis and Cardiovascular Diseases
Health Sciences › Medicine › Physiology › Nitric Oxide and Endothelin Effects
Keywords: vascular smooth muscle cells, cellular senescence, atherosclerosis, atherosclerotic plaque, senescence markers, senescence mechanisms, plaque macrophages
MeSH terms: beta-Galactosidase, Cell Cycle, Humans, Muscle, Smooth, Vascular, Telomere, Cellular Senescence, Cell Proliferation, Atherosclerosis

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Vascular smooth muscle cell senescence in atherosclerosis

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