Vascular smooth muscle cells in atherosclerosis
Open accessAbstract
The historical view of vascular smooth muscle cells (VSMCs) in atherosclerosis is that aberrant proliferation of VSMCs promotes plaque formation, but that VSMCs in advanced plaques are entirely beneficial, for example preventing rupture of the fibrous cap. However, this view has been based on ideas that there is a homogenous population of VSMCs within the plaque, that can be identified separate from other plaque cells (particularly macrophages) using standard VSMC and macrophage immunohistochemical markers. More recent genetic lineage tracing studies have shown that VSMC phenotypic switching results in less-differentiated forms that lack VSMC markers including macrophage-like cells, and this switching directly promotes atherosclerosis. In addition, VSMC proliferation may be beneficial throughout atherogenesis, and not just in advanced lesions, whereas VSMC apoptosis, cell senescence, and VSMC-derived macrophage-like cells may promote inflammation. We review the effect of embryological origin on VSMC behavior in atherosclerosis, the role, regulation and consequences of phenotypic switching, the evidence for different origins of VSMCs, and the role of individual processes that VSMCs undergo in atherosclerosis in regard to plaque formation and the structure of advanced lesions. We think there is now compelling evidence that a full understanding of VSMC behavior in atherosclerosis is critical to identify therapeutic targets to both prevent and treat atherosclerosis.
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Cellular senescence is observed in early stages of atherosclerosis, affecting different cell types in the arterial wall.
“Cellular senescence is observed in early stages of atherosclerosis,9 affecting different cell types in the arterial wall that have distinct roles in the pathogenesis of this disease: endothelial cells (ECs),96–98 vascular smooth muscle cells (VSMCs),45,99–101 macrophages, foam cells,9,102 monocytes,103 fibroblasts,104–106 and T cells.107,108”
From Senescence-induced inflammation: an important player and key therapeutic target in atherosclerosis (2020) · cites this paper as [99]
Cholesterol accumulation in intimal smooth muscle cells can drive their conversion into pro-inflammatory macrophage-like cells.
“Intimal smooth muscle cells not only accumulate cholesterol and turn into foam cells but the cholesterol accumulation in the cell can also drive their switching into pro-inflammatory, macrophage-like cells142,143.”
From Inflammation and its resolution in atherosclerosis: mediators and therapeutic opportunities (2019) · cites this paper as [143]
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Libby, P., Buring, J. E., Badimon, L., Hansson, G. K., Deanfield, J., Bittencourt, M. S., Tokgözoğlu, L., & Lewis, E. F. (2019) · Nature Reviews Disease Primers · doi:10.1038/s41572-019-0106-z · Cited by 3,211 · see citing works
The changing landscape of atherosclerosis
Libby, P. (2021) · Nature · doi:10.1038/s41586-021-03392-8 · Cited by 2,873 · see citing works
Inflammation and its resolution in atherosclerosis: mediators and therapeutic opportunities
Bäck, M., Yurdagul, A., Tabas, I., Öörni, K., & Kovanen, P. T. (2019) · Nature Reviews Cardiology · doi:10.1038/s41569-019-0169-2 · Cited by 1,341 · see citing works
Monocyte-macrophages and T cells in atherosclerosis
Tabas, I., & Lichtman, A. H. (2017) · Immunity · doi:10.1016/j.immuni.2017.09.008 · Cited by 646 · see citing works
Vascular smooth muscle cell death, autophagy and senescence in atherosclerosis
Grootaert, M. O. J., Moulis, M., Roth, L., Martinet, W., Vindis, C., Bennett, M. R., & De Meyer, G. R. Y. (2018) · Cardiovascular Research · doi:10.1093/cvr/cvy007 · Cited by 606 · see citing works
Self-citationChappell, J., Harman, J. L., Narasimhan, V. M., Yu, H., Foote, K., Simons, B. D., Bennett, M. R., & Jørgensen, H. F. (2016) · Circulation Research · doi:10.1161/circresaha.116.309799 · Cited by 437 · see citing works
Self-citationFate and state of vascular smooth muscle cells in atherosclerosis
Miano, J. M., Fisher, E. A., & Majesky, M. W. (2021) · Circulation · doi:10.1161/circulationaha.120.049922 · Cited by 318 · see citing works
KLF4-dependent perivascular cell plasticity mediates pre-metastatic niche formation and metastasis
Murgai, M., Ju, W., Eason, M., Kline, J., Beury, D. W., Kaczanowska, S., Miettinen, M. M., Kruhlak, M., Lei, H., Shern, J. F., et al. (2017) · Nature Medicine · doi:10.1038/nm.4400 · Cited by 263 · see citing works
Self-citationDavis, M. J., Earley, S., Li, Y.-S., & Chien, S. (2023) · Physiological Reviews · doi:10.1152/physrev.00053.2021 · Cited by 273 · see citing works
Gui, Y., Zheng, H., & Cao, R. Y. (2022) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2022.845942 · Cited by 258 · see citing works
Integrin beta3 regulates clonality and fate of smooth muscle-derived atherosclerotic plaque cells
Misra, A., Feng, Z., Chandran, R. R., Kabir, I., Rotllan, N., Aryal, B., Sheikh, A. Q., Ding, L., Qin, L., Fernández-Hernando, C., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-04447-7 · Cited by 207 · see citing works
Senescence-induced inflammation: an important player and key therapeutic target in atherosclerosis
Stojanović, S. D., Fiedler, J., Bauersachs, J., Thum, T., & Sedding, D. G. (2020) · European Heart Journal · doi:10.1093/eurheartj/ehz919 · Cited by 188 · see citing works
Vascular Smooth Muscle Cell Plasticity and Autophagy in Dissecting Aortic Aneurysms
Clément, M., Chappell, J., Raffort, J., Lareyre, F., Vandestienne, M., Taylor, A. L., Finigan, A., Harrison, J., Bennett, M. R., Bruneval, P., et al. (2019) · Arteriosclerosis, Thrombosis, and Vascular Biology · doi:10.1161/atvbaha.118.311727 · Cited by 184 · see citing works
Self-citationDefective autophagy in vascular smooth muscle cells enhances cell death and atherosclerosis
Osonoi, Y., Mita, T., Azuma, K., Nakajima, K., Masuyama, A., Goto, H., Nishida, Y., Miyatsuka, T., Fujitani, Y., Koike, M., et al. (2018) · Autophagy · doi:10.1080/15548627.2018.1501132 · Cited by 149 · see citing works
Das, S., Zhang, E., Senapati, P., Amaram, V., Reddy, M. A., Stapleton, K., Leung, A., Lanting, L., Wang, M., Chen, Z., et al. (2018) · Circulation Research · doi:10.1161/circresaha.118.313207 · Cited by 141 · 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
Lineage tracing of cells involved in atherosclerosis
Albarrán-Juárez, J., Kaur, H., Grimm, M., Offermanns, S., & Wettschureck, N. (2016) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2016.06.012 · Cited by 90 · see citing works
Monocytes and macrophages as protagonists in vascular complications of diabetes
Kanter, J. E., Hsu, C.-C., & Bornfeldt, K. E. (2020) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2020.00010 · Cited by 76 · see citing works
Uryga, A. K., Grootaert, M. O. J., Garrido, A. M., Oc, S., Foote, K., Chappell, J., Finigan, A., Rossiello, F., d’Adda di Fagagna, F., Aravani, D., et al. (2021) · Communications Biology · doi:10.1038/s42003-021-02123-z · Cited by 73 · see citing works
Self-citationModification of lipoprotein metabolism and function driving atherogenesis in diabetes
Luciani, L., Pedrelli, M., & Parini, P. (2024) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2024.117545 · Cited by 72 · see citing works
Animal Models of Neointimal Hyperplasia and Restenosis
Ebert, M. L. A., Schmidt, V. F., Pfaff, L., von Thaden, A., Kimm, M. A., & Wildgruber, M. (2021) · JACC: Basic to Translational Science · doi:10.1016/j.jacbts.2021.06.006 · Cited by 63 · see citing works
Incretin drugs as modulators of atherosclerosis
Gallego-Colon, E., Wojakowski, W., & Francuz, T. (2018) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2018.09.011 · Cited by 35 · see citing works
Telomeres and telomerase in risk assessment of cardiovascular diseases
Boniewska-Bernacka, E., Pańczyszyn, A., & Klinger, M. (2020) · Experimental Cell Research · doi:10.1016/j.yexcr.2020.112361 · Cited by 31 · see citing works
Target Sestrin2 to rescue the damaged organ: mechanistic insight into its function
Ala, M., & Eftekhar, S. P. (2021) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2021/8790369 · Cited by 27 · see citing works
RNA-binding proteins in vascular inflammation and atherosclerosis
Sachse, M., Tual-Chalot, S., Ciliberti, G., Amponsah-Offeh, M., Stamatelopoulos, K., Gatsiou, A., & Stellos, K. (2023) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2023.01.008 · Cited by 29 · see citing works
Transcriptome analysis of mouse aortae reveals multiple novel pathways regulated by aging
Gao, P., Gao, P., Choi, M., Chegireddy, K., Slivano, O. J., Zhao, J., Zhang, W., & Long, X. (2020) · Aging · doi:10.18632/aging.103652 · Cited by 21 · see citing works
Apelin is expressed in intimal smooth muscle cells and promotes their phenotypic transition
Cardoso Dos Santos, L. M., Azar, P., Brun, C., König, S., Roatti, A., Baertschi, A. J., Chaabane, C., & Bochaton-Piallat, M.-L. (2023) · Scientific Reports · doi:10.1038/s41598-023-45470-z · Cited by 9 · see citing works
- Authors
- Bennett, M. R., Sinha, S., & Owens, G. K.
- Affiliations
- Addenbrooke's Hospital (GB)
- Venue
- Circulation Research
- Published
- 2016-02-19
- Volume
- 118
- Issue
- 4
- Pages
- 692-702
- ISSN
- 0009-7330 (ISSN-L)
- 1524-4571
- PMC
- PMC4762053
- OpenAlex
- W2274924551
- Cited by
- 2,179
- References
- 93
- Citations by year
- 2026: 193 · 2025: 236 · 2024: 270 · 2023: 228 · 2022: 280 · 2021: 263 · 2020: 244 · 2019: 189 · 2018: 153 · 2017: 87 · 2016: 29 · 2015: 1 · 2012: 1
- FWCI
- 92.59
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Circulation Research (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Apollo (University of Cambridge) (submittedVersion)
- Apollo
- Funders
- British Heart Foundation (RG79079, PG/13/25/30014, RG71070, PG/16/11/32021, PG/19/6/34153, CH2000003, PG/16/63/32307, FS/18/19/33371, RG/13/14/30314, FS/13/29/30024, FS/15/38/31516, PG/17/9/32834, RG/16/8/32388)
- National Heart, Lung, and Blood Institute (HL057353, HL087867, HL098538, R01HL087867, R01HL057353, R37HL057353, R01HL098538, R01HL121008)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Atherosclerosis and Cardiovascular Diseases
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Cerebrovascular and Carotid Artery Diseases
- Health Sciences › Medicine › Surgery › Cholesterol and Lipid Metabolism
- Keywords
- vascular smooth muscle cells, atherosclerosis, vascular smooth muscle cell proliferation, phenotypic switching, cellular senescence, plaque formation, plaque rupture, fibrous cap, embryonic origin, lineage tracing, atherosclerosis treatment
- MeSH terms
- Animals, Cell Differentiation, Cell Movement, Humans, Muscle, Smooth, Vascular, Phenotype, Signal Transduction, Cellular Senescence, Apoptosis, Cell Lineage, Myocytes, Smooth Muscle, Cell Proliferation, Atherosclerosis, Plaque, Atherosclerotic
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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