Cited by 440Atherosclerosis and Cardiovascular DiseasesCardiovascular, Neuropeptides, and Oxidative Stress ResearchCerebrovascular and Carotid Artery Diseases

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Extensive Proliferation of a Subset of Differentiated, yet Plastic, Medial Vascular Smooth Muscle Cells Contributes to Neointimal Formation in Mouse Injury and Atherosclerosis Models

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Chappell, Joel, Harman, Jennifer L., Narasimhan, Vagheesh M., Yu, Haixiang, Foote, Kirsty, Simons, Benjamin D., Bennett, Martin R., Jørgensen, Helle F.·2016·Circulation Research

DOI 10.1161/circresaha.116.309799PMC PMC5149073

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Abstract

Rationale: Vascular smooth muscle cell (VSMC) accumulation is a hallmark of atherosclerosis and vascular injury. However, fundamental aspects of proliferation and the phenotypic changes within individual VSMCs, which underlie vascular disease, remain unresolved. In particular, it is not known whether all VSMCs proliferate and display plasticity or whether individual cells can switch to multiple phenotypes. Objective: To assess whether proliferation and plasticity in disease is a general characteristic of VSMCs or a feature of a subset of cells. Methods and Results: Using multicolor lineage labeling, we demonstrate that VSMCs in injury-induced neointimal lesions and in atherosclerotic plaques are oligoclonal, derived from few expanding cells. Lineage tracing also revealed that the progeny of individual VSMCs contributes to both alpha smooth muscle actin (aSma)–positive fibrous cap and Mac3-expressing macrophage-like plaque core cells. Costaining for phenotypic markers further identified a double-positive aSma+ Mac3+ cell population, which is specific to VSMC-derived plaque cells. In contrast, VSMC-derived cells generating the neointima after vascular injury generally retained the expression of VSMC markers and the upregulation of Mac3 was less pronounced. Monochromatic regions in atherosclerotic plaques and injury-induced neointima did not contain VSMC-derived cells expressing a different fluorescent reporter protein, suggesting that proliferation-independent VSMC migration does not make a major contribution to VSMC accumulation in vascular disease. Conclusions: We demonstrate that extensive proliferation of a low proportion of highly plastic VSMCs results in the observed VSMC accumulation after injury and in atherosclerotic plaques. Therapeutic targeting of these hyperproliferating VSMCs might effectively reduce vascular disease without affecting vascular integrity.

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Authors: Chappell, J., Harman, J. L., Narasimhan, V. M., Yu, H., Foote, K., Simons, B. D., Bennett, M. R., & Jørgensen, H. F.
Affiliations: Wellcome/MRC Cambridge Stem Cell Institute (GB)
From the Cardiovascular Medicine Division, Department of Medicine (J.C., J.L.H., H.Y., K.F., M.R.B., H.F.J.), Cavendish Laboratory, Department of Physics (B.D.S.), The Wellcome Trust/Cancer Research UK Gurdon Institute (B.D.S.), and Wellcome Trust-Medical Research Council Stem Cell Institute (B.D.S.), University of Cambridge, United Kingdom; and The Wellcome Trust Sanger Institute, Hinxton, Cambridge, United Kingdom (V.M.N.).
Corresponding author: Jørgensen, Helle F.
ORCID: Chappell, Joel
Narasimhan, Vagheesh M.
Yu, Haixiang
Foote, Kirsty
Simons, Benjamin D.
Bennett, Martin R.
Jørgensen, Helle F.
Venue: Circulation Research
Publisher: Ovid Technologies (Wolters Kluwer Health)
Published: 2016-12-09
Volume: 119
Issue: 12
Pages: 1313-1323
ISSN: 0009-7330 (ISSN-L)
1524-4571
DOI: 10.1161/circresaha.116.309799
PMC: PMC5149073
OpenAlex: W2525459565
Cited by: 437
References: 32
Citations by year: 2026: 39 · 2025: 38 · 2024: 45 · 2023: 56 · 2022: 62 · 2021: 62 · 2020: 39 · 2019: 45 · 2018: 29 · 2017: 17 · 2016: 3
FWCI: 18.96
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by
Locations: Circulation Research (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
Apollo (University of Cambridge) (submittedVersion, cc-by)
Apollo (cc-by)
Funders: Wellcome Trust (098357/Z/12/Z, 100574/Z/12/Z)
British Heart Foundation (PG/13/25/30014, PG/16/11/32021, PG/12/86/29930, RM/13/3/30159, RG/13/14/30314, FS/15/38/31516, RE/13/6/30180)
Topics: Life Sciences › Immunology and Microbiology › Immunology › Atherosclerosis and Cardiovascular Diseases
Health Sciences › Medicine › Surgery › Cardiovascular, Neuropeptides, and Oxidative Stress Research
Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cerebrovascular and Carotid Artery Diseases
Keywords: vascular smooth muscle cells, vascular smooth muscle cell proliferation, phenotypic plasticity, intimal hyperplasia, atherosclerosis, atherosclerotic plaque, lineage tracing, alpha-smooth muscle actin, VSMC migration, vascular injury
MeSH terms: Animals, Disease Models, Animal, Mice, Inbred BALB C, Mice, Inbred C57BL, Mice, Transgenic, Muscle, Smooth, Vascular, Mice, Knockout, Myocytes, Smooth Muscle, Cell Proliferation, Atherosclerosis, Mice, Vascular System Injuries, Neointima

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Extensive Proliferation of a Subset of Differentiated, yet Plastic, Medial Vascular Smooth Muscle Cells Contributes to Neointimal Formation in Mouse Injury and Atherosclerosis Models

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