Cited by 509Phagocytosis and Immune RegulationAtherosclerosis and Cardiovascular DiseasesCholesterol and Lipid Metabolism

The DOI matches its Crossref record; 43 of the 43 references it cites were found in a registry or an index.

Phagocytosis of Apoptotic Cells by Macrophages Is Impaired in Atherosclerosis

Schrijvers, Dorien M., De Meyer, Guido R.Y., Kockx, Mark M., Herman, Arnold G., Martinet, Wim·2005·Arteriosclerosis Thrombosis and Vascular Biology

DOI 10.1161/01.atv.0000166517.18801.a7

Open this paper in CoChat — free account

Abstract

OBJECTIVE: Apoptotic cell death has been demonstrated in advanced human atherosclerotic plaques. Apoptotic cells (ACs) should be rapidly removed by macrophages, otherwise secondary necrosis occurs, which in turn elicits inflammatory responses and plaque progression. Therefore, we investigated the efficiency of phagocytosis of ACs by macrophages in atherosclerosis. METHODS AND RESULTS: Human endarterectomy specimens and human tonsils were costained for CD68 (macrophages) and terminal deoxynucleotidyl transferase-mediated dUTP nick end-labeling (TUNEL) (apoptosis). Free and phagocytized ACs were counted in both tissues. The ratio of free versus phagocytized AC was 19-times higher in human atherosclerotic plaques as compared with human tonsils, indicating a severe defect in clearance of AC. Impaired phagocytosis of AC was also detected in plaques from cholesterol-fed rabbits and did not further change with plaque progression. In vitro experiments with J774 or peritoneal mouse macrophages showed that several factors caused impaired phagocytosis of AC including cytoplasmic overload of macrophages with indigestible material (beads), free radical attack, and competitive inhibition among oxidized red blood cells, oxidized low-density lipoprotein and ACs for the same receptor(s) on the macrophage. CONCLUSIONS: Our data demonstrate that phagocytosis of ACs is impaired in atherosclerotic plaques, which is at least partly attributed to oxidative stress and cytoplasmic saturation with indigestible material.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.1161/01.atv.0000166517.18801.a7

Cites

43 of 43 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Lessons From Sudden Coronary Death: A Comprehensive Morphological Classification Scheme for Atherosclerotic Lesions
Virmani, R., Kolodgie, F. D., Burke, A. P., Farb, A., & Schwartz, S. M. (2000) · Arteriosclerosis, Thrombosis, and Vascular Biology · doi:10.1161/01.atv.20.5.1262 · Cited by 4,084
Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/paracrine mechanisms involving TGF-beta, PGE2, and PAF.
Fadok, V. A., Bratton, D. L., Konowal, A., Freed, P. W., Westcott, J. Y., & Henson, P. M. (1998) · Journal of Clinical Investigation · doi:10.1172/jci1112 · Cited by 3,166
Mechanisms of phagocytosis in macrophages
Aderem, A., & Underhill, D. M. (1999) · Annual Review of Immunology · doi:10.1146/annurev.immunol.17.1.593 · Cited by 2,854
Immunol. Cell Biol.
Fitzgerald, M., Hayward, I. P., Thomas, A. C., Campbell, J. H., & CAMPBELL, G. R. (1995) · Cited by 2,552
Oxidative Stress and Vascular Disease
Madamanchi, N. R., Vendrov, A., & Runge, M. S. (2005) · Arteriosclerosis, Thrombosis, and Vascular Biology · doi:10.1161/01.atv.0000150649.39934.13 · Cited by 1,618
Corpse clearance defines the meaning of cell death
Savill, J., & Fadok, V. A. (2000) · Nature · doi:10.1038/35037722 · Cited by 1,572
Shed Membrane Microparticles With Procoagulant Potential in Human Atherosclerotic Plaques
Mallat, Z., Hugel, B., Ohan, J., Lesèche, G., Freyssinet, J., & Tedgui, A. (1999) · Circulation · doi:10.1161/01.cir.99.3.348 · Cited by 636
Phagocyte receptors for apoptotic cells: recognition, uptake, and consequences
Fadok, V. A., Bratton, D. L., & Henson, P. M. (2001) · Journal of Clinical Investigation · doi:10.1172/jci14122 · Cited by 474
Monoclonal antibodies against oxidized low-density lipoprotein bind to apoptotic cells and inhibit their phagocytosis by elicited macrophages: Evidence that oxidation-specific epitopes mediate macrophage recognition
Chang, M.-K., Bergmark, C., Laurila, A., Hörkkö, S., Han, K., Friedman, P., Dennis, E. A., & Witztum, J. L. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.11.6353 · Cited by 456
Elevated Levels of Oxidative DNA Damage and DNA Repair Enzymes in Human Atherosclerotic Plaques
Martinet, W., Knaapen, M., Meyer, G. R. Y. D., Herman, A. G., & Kockx, M. M. (2002) · Circulation · doi:10.1161/01.cir.0000026393.47805.21 · Cited by 448

Show all 42 references

Research works printed but not linked: 9

10.1161/circ.97.23.2307 · DOI
1996, Am J Pathol, 149, 911
10.1161/circ.99.3.348 · DOI
10.1161/atvb.20.5.1262 · DOI
10.1161/res.83.4.378 · DOI
1998, Am J Pathol, 152, 885
1996, Am J Pathol, 149, 367
2001, Am J Cardiol, 88, 3J
2004, Cell Death Differ, 1

Sorted by citations

Macrophages in the Pathogenesis of Atherosclerosis
Moore, K. J., & Tabas, I. (2011) · Cell · doi:10.1016/j.cell.2011.04.005 · Cited by 2,669
Mechanisms of plaque formation and rupture
Bentzon, J. F., Otsuka, F., Virmani, R., & Falk, E. (2014) · Circulation Research · doi:10.1161/circresaha.114.302721 · Cited by 2,391
Vascular smooth muscle cells in atherosclerosis
Bennett, M. R., Sinha, S., & Owens, G. K. (2016) · Circulation Research · doi:10.1161/circresaha.115.306361 · Cited by 2,179
Cytokines in Atherosclerosis: Pathogenic and Regulatory Pathways
Tedgui, A., & Mallat, Z. (2006) · Physiological Reviews · doi:10.1152/physrev.00024.2005 · Cited by 1,751
Role of cholesterol and lipid organization in disease
Maxfield, F. R., & Tabas, I. A. (2005) · Nature · doi:10.1038/nature04399 · Cited by 1,331
Apoptotic cell clearance: basic biology and therapeutic potential
Poon, I. K. H., Lucas, C. D., Rossi, A. G., & Ravichandran, K. S. (2014) · Nature Reviews Immunology · doi:10.1038/nri3607 · Cited by 1,223
Vascular smooth muscle cells in atherosclerosis
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
Macrophage death and defective inflammation resolution in atherosclerosis
Tabas, I. (2010) · Nature Reviews Immunology · doi:10.1038/nri2675 · Cited by 1,120
Apoptosis and Clearance of Apoptotic Cells
Nagata, S. (2018) · Annual Review of Immunology · doi:10.1146/annurev-immunol-042617-053010 · Cited by 1,135
Efferocytosis in health and disease
Doran, A. C., Yurdagul, A., & Tabas, I. (2020) · Nature Reviews Immunology · doi:10.1038/s41577-019-0240-6 · Cited by 1,066
Recent insights into the cellular biology of atherosclerosis
Tabas, I., García-Cardeña, G., & Owens, G. K. (2015) · Journal of Cell Biology · doi:10.1083/jcb.201412052 · Cited by 1,016
Apoptosis and apoptotic body: disease message and therapeutic target potentials
Xu, X., Lai, Y., & Hua, Z. (2018) · Bioscience Reports · doi:10.1042/bsr20180992 · Cited by 953
The clearance of dead cells by efferocytosis
Boada-Romero, E., Martinez, J., Heckmann, B. L., & Green, D. R. (2020) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-020-0232-1 · Cited by 924
Inflammation and plaque vulnerability
Hansson, G. K., Libby, P., & Tabas, I. A. (2015) · Journal of Internal Medicine · doi:10.1111/joim.12406 · Cited by 809
The CD47-SIRPα Immune Checkpoint
Logtenberg, M. E. W., Scheeren, F. A., & Schumacher, T. N. (2020) · Immunity · doi:10.1016/j.immuni.2020.04.011 · Cited by 760
CD47-blocking antibodies restore phagocytosis and prevent atherosclerosis
Kojima, Y., Volkmer, J.-P., McKenna, K., Civelek, M., Lusis, A. J., Miller, C. L., Direnzo, D., Nanda, V., Ye, J., Connolly, A. J., et al. (2016) · Nature · doi:10.1038/nature18935 · Cited by 683
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
Consequences and Therapeutic Implications of Macrophage Apoptosis in Atherosclerosis
Tabas, I. A. (2005) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000184783.04864.9f · Cited by 641
Macrophage Autophagy Plays a Protective Role in Advanced Atherosclerosis
Liao, X., Sluimer, J. C., Wang, Y., Subramanian, M., Brown, K., Pattison, J. S., Robbins, J., Martinez, J., & Tabas, I. (2012) · Cell Metabolism · doi:10.1016/j.cmet.2012.01.022 · Cited by 627
Neutrophils as protagonists and targets in chronic inflammation
Soehnlein, O., Steffens, S., Hidalgo, A., & Weber, C. (2017) · Nature reviews. Immunology · doi:10.1038/nri.2017.10 · Cited by 623
Regulation of macrophage immunometabolism in atherosclerosis
Koelwyn, G. J., Corr, E. M., Erbay, E., & Moore, K. J. (2018) · Nature Immunology · doi:10.1038/s41590-018-0113-3 · Cited by 569
Clearance of apoptotic cells: implications in health and disease
Elliott, M. R., & Ravichandran, K. S. (2010) · The Journal of Cell Biology · doi:10.1083/jcb.201004096 · Cited by 568
Physiology and diseases of tissue-resident macrophages
Lazarov, T., Juarez-Carreño, S., Cox, N., & Geissmann, F. (2023) · Nature · doi:10.1038/s41586-023-06002-x · Cited by 571
Inflammation and its Resolution as Determinants of Acute Coronary Syndromes
Libby, P., Tabas, I. A., Fredman, G., & Fisher, E. A. A. (2014) · Circulation Research · doi:10.1161/circresaha.114.302699 · Cited by 531
Macrophage-targeted nanomedicine for the diagnosis and treatment of atherosclerosis
Chen, W., Schilperoort, M., Cao, Y., Shi, J., Tabas, I. A., & Tao, W. (2021) · Nature Reviews Cardiology · doi:10.1038/s41569-021-00629-x · Cited by 544
Phagosome maturation: going through the acid test
Kinchen, J. M., & Ravichandran, K. S. (2008) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2515 · Cited by 555
Clearing the Dead: Apoptotic Cell Sensing, Recognition, Engulfment, and Digestion
Hochreiter-Hufford, A., & Ravichandran, K. S. (2013) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a008748 · Cited by 503
Has Our Understanding of Calcification in Human Coronary Atherosclerosis Progressed?
Otsuka, F., Sakakura, K., Yahagi, K., Joner, M., & Virmani, R. (2014) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.113.302642 · Cited by 500
The Role of Endoplasmic Reticulum Stress in the Progression of Atherosclerosis
Tabas, I. (2010) · Circulation Research · doi:10.1161/circresaha.110.224766 · Cited by 480
Regulatory T Cells Promote Macrophage Efferocytosis during Inflammation Resolution
Proto, J. D., Doran, A. C., Gusarova, G., Yurdagul, A., Sozen, E., Subramanian, M., Islam, M. N., Rymond, C. C., Du, J., Hook, J., et al. (2018) · Immunity · doi:10.1016/j.immuni.2018.07.015 · Cited by 441
Burying the Dead
Vandivier, R. W., Henson, P. M., & Douglas, I. S. (2006) · CHEST Journal · doi:10.1378/chest.129.6.1673 · Cited by 450
How macrophages deal with death
Lemke, G. (2019) · Nature reviews. Immunology · doi:10.1038/s41577-019-0167-y · Cited by 446
An imbalance between specialized pro-resolving lipid mediators and pro-inflammatory leukotrienes promotes instability of atherosclerotic plaques
Fredman, G., Hellmann, J., Proto, J. D., Kuriakose, G., Colas, R. A., Dorweiler, B., Connolly, E. S., Solomon, R., Jones, D. M., Heyer, E. J., et al. (2016) · Nature Communications · doi:10.1038/ncomms12859 · Cited by 411
Oxidative Stress-Mediated Atherosclerosis: Mechanisms and Therapies
Yang, X., Li, Y., Li, Y., Ren, X., Zhang, X., Hu, D., Gao, Y., Xing, Y., & Shang, H. (2017) · Frontiers in Physiology · doi:10.3389/fphys.2017.00600 · Cited by 418
Cytokines, macrophage lipid metabolism and foam cells: Implications for cardiovascular disease therapy
McLaren, J. E., Michael, D. R., Ashlin, T. G., & Ramji, D. P. (2011) · Progress in Lipid Research · doi:10.1016/j.plipres.2011.04.002 · Cited by 404
Chronic Apoptosis of Vascular Smooth Muscle Cells Accelerates Atherosclerosis and Promotes Calcification and Medial Degeneration
Clarke, M. C. H., Littlewood, T. D., Figg, N., Maguire, J. J., Davenport, A. P., Goddard, M., & Bennett, M. R. (2008) · Circulation Research · doi:10.1161/circresaha.108.175976 · Cited by 396
Cellular Origins and Thrombogenic Activity of Microparticles Isolated From Human Atherosclerotic Plaques
Leroyer, A. S., Isobe, H., Lesèche, G., Castier, Y., Wassef, M., Mallat, Z., Binder, B. R., Tedgui, A., & Boulanger, C. M. (2007) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2006.10.053 · Cited by 385
Enhanced Efferocytosis of Apoptotic Cardiomyocytes Through Myeloid-Epithelial-Reproductive Tyrosine Kinase Links Acute Inflammation Resolution to Cardiac Repair After Infarction
Wan, E. Y., Yeap, X. Y., Dehn, S., Terry, R. L., Novak, M. L., Zhang, S., Iwata, S., Han, X., Homma, S., Drosatos, K., et al. (2013) · Circulation Research · doi:10.1161/circresaha.113.301198 · Cited by 401
Mitochondrial fission promotes the continued clearance of apoptotic cells by macrophages
Wang, Y., Subramanian, M., Yurdagul, A., Barbosa-Lorenzi, V. C., Cai, B., de Juan-Sanz, J., Ryan, T. A., Nomura, M., Maxfield, F. R., & Tabas, I. (2017) · Cell · doi:10.1016/j.cell.2017.08.041 · Cited by 364
Macrophages in cardiovascular diseases: molecular mechanisms and therapeutic targets
Chen, R., Zhang, H., Tang, B., Luo, Y., Yang, Y., Zhong, X., Chen, S., Xu, X., Huang, S., & Liu, C. (2024) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-024-01840-1 · Cited by 418
Mertk Receptor Mutation Reduces Efferocytosis Efficiency and Promotes Apoptotic Cell Accumulation and Plaque Necrosis in Atherosclerotic Lesions of Apoe −/− Mice
Thorp, E., Cui, D., Schrijvers, D. M., Kuriakose, G., & Tabas, I. (2008) · Arteriosclerosis, Thrombosis, and Vascular Biology · doi:10.1161/atvbaha.108.167197 · Cited by 357
Self-citation
Reduced Apoptosis and Plaque Necrosis in Advanced Atherosclerotic Lesions of Apoe−/− and Ldlr−/− Mice Lacking CHOP
Thorp, E. B., Li, G., Seimon, T. A., Kuriakose, G., Ron, D., & Tabas, I. A. (2009) · Cell Metabolism · doi:10.1016/j.cmet.2009.03.003 · Cited by 345
Atherosclerotic Plaque Destabilization
Silvestre-Roig, C., de Winther, M. P. J., Weber, C., Daemen, M. J. A. P., Lutgens, E., & Soehnlein, O. (2014) · Circulation Research · doi:10.1161/circresaha.114.302355 · Cited by 346
Mechanisms and Consequences of Defective Efferocytosis in Atherosclerosis
Yurdagul, A., Doran, A. C., Cai, B., Fredman, G., & Tabas, I. A. (2018) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2017.00086 · Cited by 300
Vascular effects of adiponectin: molecular mechanisms and potential therapeutic intervention
Zhu, W., Cheng, K. K. Y., Vanhoutte, P. M., Lam, K. S. L., & Xu, A. (2008) · Clinical Science · doi:10.1042/cs20070347 · Cited by 291
The role of efferocytosis in atherosclerosis
Kojima, Y., Weissman, I. L., & Leeper, N. J. (2017) · Circulation · doi:10.1161/circulationaha.116.025684 · Cited by 289
A pathway for phagosome maturation during engulfment of apoptotic cells
Kinchen, J. M., Doukoumetzidis, K., Almendinger, J., Stergiou, L., Tosello-Trampont, A., Sifri, C. D., Hengartner, M. O., & Ravichandran, K. S. (2008) · Nature Cell Biology · doi:10.1038/ncb1718 · Cited by 284
Pro-efferocytic nanoparticles are specifically taken up by lesional macrophages and prevent atherosclerosis
Flores, A. M., Hosseini-Nassab, N., Jarr, K.-U., Ye, J., Zhu, X., Wirka, R. C., Koh, A. L., Tsantilas, P., Wang, Y., Nanda, V., et al. (2020) · Nature Nanotechnology · doi:10.1038/s41565-019-0619-3 · Cited by 289
Mitochondrial DNA Damage Can Promote Atherosclerosis Independently of Reactive Oxygen Species Through Effects on Smooth Muscle Cells and Monocytes and Correlates With Higher-Risk Plaques in Humans
Yu, E., Calvert, P. A., Mercer, J. R., Harrison, J. B., Baker, L. L., Figg, N. L., Kumar, S., Wang, J. C., Hurst, L. A., Obaid, D. R., et al. (2013) · Circulation · doi:10.1161/circulationaha.113.002271 · Cited by 288
Phagocytosis in atherosclerosis: Molecular mechanisms and implications for plaque progression and stability
Schrijvers, D. M., DEMEYER, G., HERMAN, A., & Martinet, W. (2006) · Cardiovascular Research · doi:10.1016/j.cardiores.2006.09.005 · Cited by 275
Endothelial cell apoptosis and the role of endothelial cell-derived extracellular vesicles in the progression of atherosclerosis
Paone, S., Baxter, A. A., Hulett, M. D., & Poon, I. K. H. (2018) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-018-2983-9 · Cited by 281
MerTK receptor cleavage promotes plaque necrosis and defective resolution in atherosclerosis
Cai, B., Thorp, E. B., Doran, A. C., Sansbury, B. E., Daemen, M. J. A. P., Dorweiler, B., Spite, M., Fredman, G., & Tabas, I. (2017) · Journal of Clinical Investigation · doi:10.1172/jci90520 · Cited by 262
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
“oxLDL was prepared as previously described.(64) In some experiments, cells were treated with 10 mmol/l puromycin (Sigma Aldrich, P8833) for 12 h or exposed to UV-irradiation for 10 min.”
Method
The role of non-resolving inflammation in atherosclerosis
Kasikara, C., Doran, A. C., Cai, B., & Tabas, I. (2018) · Journal of Clinical Investigation · doi:10.1172/jci97950 · Cited by 266
Macrophage Apoptosis Exerts Divergent Effects on Atherogenesis as a Function of Lesion Stage
Gautier, E. L., Huby, T., Witztum, J. L., Ouzilleau, B., Miller, E. R., Saint-Charles, F., Aucouturier, P., Chapman, M. J., & Lesnik, P. (2009) · Circulation · doi:10.1161/circulationaha.108.806158 · Cited by 246
Mechanisms and consequences of efferocytosis in advanced atherosclerosis
Thorp, E., & Tabas, I. (2009) · Journal of Leukocyte Biology · doi:10.1189/jlb.0209115 · Cited by 231
Atherosclerosis – A matter of unresolved inflammation
Viola, J. R., & Soehnlein, O. (2015) · Seminars in Immunology · doi:10.1016/j.smim.2015.03.013 · Cited by 229
Macrophage Apoptosis and Efferocytosis in the Pathogenesis of Atherosclerosis
Linton, M. F., Babaev, V. R., Huang, J., Linton, E. F., Tao, H., & Yancey, P. G. (2016) · Circulation Journal · doi:10.1253/circj.cj-16-0924 · Cited by 235
Macrophage Death as a Pharmacological Target in Atherosclerosis
Martinet, W., Coornaert, I., Puylaert, P., & Meyer, G. R. Y. D. (2019) · Frontiers in Pharmacology · doi:10.3389/fphar.2019.00306 · Cited by 232
Macrophage Trafficking, Inflammatory Resolution, and Genomics in Atherosclerosis
Moore, K. J., Koplev, S., Fisher, E. A. A., Tabas, I. A., Björkegren, J., Doran, A. C., & Kovacic, J. C. (2018) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2018.08.2147 · Cited by 229
Disassembly of the Dying: Mechanisms and Functions
Atkin‐Smith, G. K., & Poon, I. K. H. (2016) · Trends in Cell Biology · doi:10.1016/j.tcb.2016.08.011 · Cited by 214
Vascular Smooth Muscle Cell Apoptosis Induces Interleukin-1–Directed Inflammation: Effects of Hyperlipidemia-Mediated Inhibition of Phagocytosis
Clarke, M. C. H., Talib, S., Figg, N. L., & Bennett, M. R. (2010) · Circulation Research · doi:10.1161/circresaha.109.208389 · Cited by 216
The Endoplasmic Reticulum Stress-C/EBP Homologous Protein Pathway-Mediated Apoptosis in Macrophages Contributes to the Instability of Atherosclerotic Plaques
Tsukano, H., Gotoh, T., Endo, M., Miyata, K., Tazume, H., Kadomatsu, T., Yano, M., Iwawaki, T., Kohno, K., Araki, K., et al. (2010) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.110.206094 · Cited by 208
Programmed death of macrophages in atherosclerosis: mechanisms and therapeutic targets
Meyer, G. R. Y. D., Zurek, M., Puylaert, P., & Martinet, W. (2024) · Nature Reviews Cardiology · doi:10.1038/s41569-023-00957-0 · Cited by 221
Apoptotic Cell Death and Efferocytosis in Atherosclerosis
Vré, E. A. V., Ait‐Oufella, H., Tedgui, A., & Mallat, Z. (2012) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.111.224873 · Cited by 218
Natural progression of atherosclerosis from pathologic intimal thickening to late fibroatheroma in human coronary arteries: A pathology study
Otsuka, F., Kramer, M. C. A., Woudstra, P., Yahagi, K., Ladich, E. R., Finn, A. V., de Winter, R. J., Kolodgie, F. D., Wight, T. N., Davis, H. R., et al. (2015) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2015.05.011 · Cited by 202
Immune Clearance of Senescent Cells to Combat Ageing and Chronic Diseases
Song, P., An, J., & Zou, M.-H. (2020) · Cells · doi:10.3390/cells9030671 · Cited by 198
The roles of myeloperoxidase in coronary artery disease and its potential implication in plaque rupture
Teng, N., Maghzal, G. J., Talib, J., Rashid, I., Lau, A. K., & Stocker, R. (2016) · Redox Report · doi:10.1080/13510002.2016.1256119 · Cited by 198
Autophagy in Atherosclerosis
Schrijvers, D. M., Meyer, G. R. Y. D., & Martinet, W. (2011) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.111.224899 · Cited by 189
Defective Mer Receptor Tyrosine Kinase Signaling in Bone Marrow Cells Promotes Apoptotic Cell Accumulation and Accelerates Atherosclerosis
Ait-Oufella, H., Pouresmail, V., Simon, T., Blanc-Brude, O., Kinugawa, K., Merval, R., Offenstadt, G., Lesèche, G., Cohen, P. L., Tedgui, A., et al. (2008) · Arteriosclerosis, Thrombosis, and Vascular Biology · doi:10.1161/atvbaha.108.169078 · Cited by 187
Plaque angiogenesis and intraplaque hemorrhage in atherosclerosis
Parma, L., Baganha, F., Quax, P. H. A., & de Vries, M. R. (2017) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2017.04.028 · Cited by 186
Human Monocyte Heterogeneity as Revealed by High-Dimensional Mass Cytometry
Hamers, A. A. J., Dinh, H. Q., Thomas, G. D., Marcovecchio, P., Blatchley, A., Nakao, C., Kim, C., McSkimming, C. C., Taylor, A. M., Nguyen, A. T., et al. (2018) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.118.311022 · Cited by 183
Macrophage Apoptosis in Atherosclerosis: Consequences on Plaque Progression and the Role of Endoplasmic Reticulum Stress
Tabas, I. A. (2009) · Antioxidants and Redox Signaling · doi:10.1089/ars.2009.2469 · Cited by 186
Inflammation: a culprit for vascular calcification in atherosclerosis and diabetes
Bessueille, L., & Magne, D. (2015) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-015-1876-4 · Cited by 182
Vascular Macrophages in Atherosclerosis
Xu, H., Jiang, J., Chen, W., Li, W., & Chen, Z. (2019) · Journal of Immunology Research · doi:10.1155/2019/4354786 · Cited by 176
Distribution of Inflammation Within Carotid Atherosclerotic Plaques With High-Risk Morphological Features
Figueroa, A. L., Subramanian, S. S., Cury, R. C., Truong, Q. A., Gardecki, J. A., Tearney, G. J., Hoffmann, U., Brady, T. J., & Tawakol, A. A. (2011) · Circulation Cardiovascular Imaging · doi:10.1161/circimaging.110.959478 · Cited by 171
Macrophage LRP-1 Controls Plaque Cellularity by Regulating Efferocytosis and Akt Activation
Yancey, P. G., Blakemore, J., Ding, L., Fan, D., Overton, C. D., Zhang, Y., Linton, M. F., & Fazio, S. (2010) · Arteriosclerosis, Thrombosis, and Vascular Biology · doi:10.1161/atvbaha.109.202051 · Cited by 168
Defective Phagocytosis of Apoptotic Cells by Macrophages in Atherosclerotic Lesions of ob/ob Mice and Reversal by a Fish Oil Diet
Li, S., Sun, Y., Liang, C., Thorp, E. B., Han, S., Jehle, A. W., Saraswathi, V., Pridgen, B. C., Kanter, J. E., Li, R., et al. (2009) · Circulation Research · doi:10.1161/circresaha.109.199570 · Cited by 173
Efferocytosis in atherosclerosis
Adkar, S. S., & Leeper, N. J. (2024) · Nature Reviews Cardiology · doi:10.1038/s41569-024-01037-7 · Cited by 182
Proteomics Analysis of Human Coronary Atherosclerotic Plaque
Bagnato, C., Thumar, J. R., Mayya, V., Hwang, S., Zebroski, H. A., Claffey, K. P., Haudenschild, C. C., Eng, J. K., Lundgren, D. H., & Han, D. K. M. (2007) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m600259-mcp200 · Cited by 161
NLRP3 inflammasome activation in inflammaging
Latz, E., & Duewell, P. (2018) · Seminars in Immunology · doi:10.1016/j.smim.2018.09.001 · Cited by 174
Involvement of intraplaque hemorrhage in atherothrombosis evolution via neutrophil protease enrichment
Leclercq, A., Houard, X., Philippe, M., Ollivier, V., Sebbag, U., Meilhac, O., & Michel, J. (2007) · Journal of Leukocyte Biology · doi:10.1189/jlb.1106671 · Cited by 159
Macrophages: An elusive yet emerging therapeutic target of atherosclerosis
Tiwari, R. L., Singh, V., & Barthwal, M. K. (2007) · Medicinal Research Reviews · doi:10.1002/med.20118 · Cited by 155
Cyclin-dependent kinase inhibitor 2B regulates efferocytosis and atherosclerosis
Kojima, Y., Downing, K., Kundu, R., Miller, C., Dewey, F., Lancero, H., Raaz, U., Perisic, L., Hedin, U., Schadt, E., et al. (2014) · Journal of Clinical Investigation · doi:10.1172/jci70391 · Cited by 148
Suppression of Atherosclerotic Plaque Progression and Instability by Tissue Inhibitor of Metalloproteinase-2
Johnson, J. L., Baker, A. H., Oka, K., Chan, L., Newby, A. C., Jackson, C. L., & George, S. J. (2006) · Circulation · doi:10.1161/circulationaha.106.613281 · Cited by 148
The walking dead: macrophage inflammation and death in atherosclerosis
Kavurma, M. M., Rayner, K. J., & Karunakaran, D. (2017) · Current Opinion in Lipidology · doi:10.1097/mol.0000000000000394 · Cited by 146
The Macrophage at the Crossroads of Insulin Resistance and Atherosclerosis
Liang, C.-P., Han, S., Senokuchi, T., & Tall, A. R. (2007) · Circulation Research · doi:10.1161/circresaha.107.152165 · Cited by 143
Macrophage metabolism in atherosclerosis
Bories, G. F. P., & Leitinger, N. (2017) · FEBS Letters · doi:10.1002/1873-3468.12786 · Cited by 145
Necrotic cell death in atherosclerosis
Martinet, W., Schrijvers, D. M., & Meyer, G. R. Y. D. (2011) · Basic Research in Cardiology · doi:10.1007/s00395-011-0192-x · Cited by 139
SPION primes THP1 derived M2 macrophages towards M1-like macrophages
Laskar, A., Eilertsen, J., Li, W., & Yuan, X.-M. (2013) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2013.10.115 · Cited by 138
Atherosclerosis and interferon-γ: New insights and therapeutic targets
Voloshyna, I., Littlefield, M. J., & Reiss, A. B. (2013) · Trends in Cardiovascular Medicine · doi:10.1016/j.tcm.2013.06.003 · Cited by 139
Efferocytosis in atherosclerotic lesions: Malfunctioning regulatory pathways and control mechanisms
Tajbakhsh, A., Rezaee, M., Kovanen, P. T., & Sahebkar, A. (2018) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2018.02.003 · Cited by 134
Exploiting Oxidative Microenvironments in the Body as Triggers for Drug Delivery Systems
Joshi-Barr, S., Lux, C. D. G., Mahmoud, E., & Almutairi, A. (2013) · Antioxidants and Redox Signaling · doi:10.1089/ars.2013.5754 · Cited by 134
Inflammation: A Novel Therapeutic Target/Direction in Atherosclerosis
Li, B., Li, W., Li, X., & Zhou, H. (2017) · Current Pharmaceutical Design · doi:10.2174/1381612822666161230142931 · Cited by 130
Macrophage Apoptosis and Necrotic Core Development in Atherosclerosis: A Rapidly Advancing Field with Clinical Relevance to Imaging and Therapy
González, L., & Trigatti, B. L. (2016) · Canadian Journal of Cardiology · doi:10.1016/j.cjca.2016.12.010 · Cited by 136
Lipoprotein Retention—and Clues for Atheroma Regression
Williams, K. J., & Tabas, I. A. (2005) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000174795.62387.d3 · Cited by 132
Macrophages and Cardiovascular Health
Frodermann, V., & Nahrendorf, M. (2018) · Physiological Reviews · doi:10.1152/physrev.00068.2017 · Cited by 128
Macrophage ATP citrate lyase deficiency stabilizes atherosclerotic plaques
Baardman, J., Verberk, S. G. S., van der Velden, S., Gijbels, M. J., van Roomen, C. P. A. A., Sluimer, J. C., Broos, J. Y., Griffith, G. R., Prange, K. H. M., van Weeghel, M., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-20141-z · Cited by 134
Macrophage-Derived 25-Hydroxycholesterol Promotes Vascular Inflammation, Atherogenesis, and Lesion Remodeling
Canfrán‐Duque, A., Rotllán, N., Zhang, X., Andrés‐Blasco, I., Thompson, B. M., Sun, J., Price, N. L., Fernández‐Fuertes, M., Fowler, J. W., Gómez‐Coronado, D., et al. (2022) · Circulation · doi:10.1161/circulationaha.122.059062 · Cited by 130
The Impact of Macrophage Insulin Resistance on Advanced Atherosclerotic Plaque Progression
Tabas, I. A., Tall, A. R., & Accili, D. (2010) · Circulation Research · doi:10.1161/circresaha.109.208488 · Cited by 123

Authors: Schrijvers, D. M., De Meyer, G. R. Y., Kockx, M. M., Herman, A. G., & Martinet, W.
Affiliations: University of Antwerp (BE)
From the Division of Pharmacology (D.M.S., G.R.Y.D.M., M.M.K., A.G.H., W.M.), University of Antwerp, Wilrijk, Belgium; and the Department of Pathology (M.M.K.), AZ Middelheim, Antwerp, Belgium
ORCID: Schrijvers, Dorien M.
Kockx, Mark M.
Martinet, Wim
Venue: Arteriosclerosis Thrombosis and Vascular Biology
Publisher: Ovid Technologies (Wolters Kluwer Health)
Published: 2005-06
Volume: 25
Issue: 6
Pages: 1256-1261
ISSN: 1079-5642 (ISSN-L)
1524-4636
DOI: 10.1161/01.atv.0000166517.18801.a7
OpenAlex: W2163327518
Cited by: 509
References: 42
Citations by year: 2026: 13 · 2025: 32 · 2024: 34 · 2023: 31 · 2022: 34 · 2021: 33 · 2020: 21 · 2019: 24 · 2018: 29 · 2017: 32 · 2016: 20 · 2015: 25 · 2014: 21 · 2013: 24 · 2012: 16
FWCI: 6.74
Type: journal article
Language: en
Open access: closed
Locations: Arteriosclerosis Thrombosis and Vascular Biology (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Immunology and Microbiology › Immunology › Phagocytosis and Immune Regulation
Life Sciences › Immunology and Microbiology › Immunology › Atherosclerosis and Cardiovascular Diseases
Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Cholesterol and Lipid Metabolism
Keywords: phagocytosis of apoptotic cells, macrophages, atherosclerosis, atherosclerotic plaque, secondary necrosis, oxidative stress, oxidized LDL, plaque progression, cholesterol-fed rabbits, tonsil
MeSH terms: Aged, Animals, Carotid Artery Diseases, Cytoplasm, Erythrocytes, Female, Humans, Lipoproteins, LDL, Male, Necrosis, Phagocytosis, Rabbits, Palatine Tonsil, Apoptosis, Macrophages, Peritoneal, Oxidative Stress, U937 Cells, Mice

About these checks

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.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Phagocytosis of Apoptotic Cells by Macrophages Is Impaired in Atherosclerosis

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Self-check

Citations

Cites

Cited by

Related

Metadata

Record

About these checks