Induction of Atherosclerotic Plaque Rupture in Apolipoprotein E −/− Mice After Adenovirus-Mediated Transfer of p53
Abstract
Background — The presence of the tumor-suppressor gene p53 in advanced atherosclerotic plaques and the sensitivity to p53-induced cell death of smooth muscle cells isolated from these plaques have fueled speculation about the role of p53 in lesion destabilization and plaque rupture. In this study, we describe a strategy to promote (thrombotic) rupture of preexisting atherosclerotic lesions using p53-induced lesion remodeling. Methods and Results — Carotid atherogenesis was initiated in apolipoprotein E knockout mice by placement of a perivascular silastic collar. The resulting plaques were incubated transluminally with recombinant adenovirus carrying either a p53 or β-galactosidase ( lacZ ) transgene. p53 transfection was restricted to the smooth muscle cell-rich cap of the plaque and led to an increase in cap cell apoptosis 1 day after transfer. p53 overexpression resulted in a marked decrease in the cellular and extracellular content of the cap, reflected by a markedly reduced cap/intima ratio (0.21±0.04 versus 0.46±0.03, P <0.001). The latter is a characteristic feature of plaque vulnerability to rupture, and whereas spontaneous rupture of p53-treated lesions was rare, it was found in 40% of cases after treatment with the vasopressor compound phenylephrine ( P =0.003). Conclusions — We have demonstrated a potential role of p53-induced remodeling in atherosclerotic plaque destabilization. Being the first example of inducible rupture at a predefined location, this model offers a unique opportunity to delineate the processes that precede rupture and to evaluate plaque-stabilizing therapies.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
Early work with adenoviral p53 expression in plaques led to VSMC apoptosis and cap thinning.
“Early work with adenoviral p53 expression in plaques led to VSMC apoptosis and cap thinning 182 .”
From Vascular smooth muscle cells in atherosclerosis (2019) · cites this paper as [182]
Cites
Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation.
Gavrieli, Y., Sherman, Y., & Ben-Sasson, S. A. (1992) · The Journal of cell biology · doi:10.1083/jcb.119.3.493 · Cited by 9,444 · see citing works
p53: puzzle and paradigm.Preprint
Ko, L. J., & Prives, C. L. (1996) · Genes & Development · doi:10.1101/gad.10.9.1054 · Cited by 2,338 · see citing works
Bennett, M. R., Evan, G. I., & Schwartz, S. M. (1995) · Journal of Clinical Investigation · doi:10.1172/jci117917 · Cited by 707 · see citing works
Kolodgie, F. D., BURKE, A. P., Farb, A. A., Gold, H. K., Yuan, J., Narula, J., Finn, A. V., & Virmani, R. (2001) · Current Opinion in Cardiology · doi:10.1097/00001573-200109000-00006 · Cited by 686 · see citing works
Apoptosis in Human Atherosclerosis and Restenosis
Isner, J. M., Kearney, M., Bortman, S., & Passeri, J. J. (1995) · Circulation · doi:10.1161/01.cir.91.11.2703 · Cited by 673 · see citing works
McGrory, W. J., Bautista, D., & Graham, F. L. (1988) · Virology · doi:10.1016/0042-6822(88)90302-9 · Cited by 590 · see citing works
Fallaux, F. J., Bout, A., van der Velde, I., van den Wollenberg, D. J. M., Hehir, K. M., Keegan, J., Auger, C., Cramer, S. J., van Ormondt, H., van der Eb, A. J., et al. (1998) · Human Gene Therapy · doi:10.1089/hum.1998.9.13-1909 · Cited by 480 · see citing works
Self-citationBjörkerud, S., & Björkerud, B. (1996) · PubMed · Cited by 419 · see citing works
The p53 Tumor Suppressor Gene: From Molecular Biology to Clinical Investigation
Soussi, T. (2000) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2000.tb06705.x · Cited by 330 · see citing works
Apoptosis in atherosclerosis: beneficial or detrimental?
Kockx, M. M. (2000) · Cardiovascular Research · doi:10.1016/s0008-6363(99)00235-7 · Cited by 314 · see citing works
Self-citationThe absence of p53 accelerates atherosclerosis by increasing cell proliferation in vivo
Guevara, J., Kim, H.-S., Antonova, E. I., & Chan, L. (1999) · Nature Medicine · doi:10.1038/6585 · Cited by 286 · see citing works
Geng, Y., Henderson, L. E., Levesque, E. B., Muszynski, M., & Libby, P. (1997) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.17.10.2200 · Cited by 266 · see citing works
Apoptosis in the Atherosclerotic Plaque
Kockx, M. M. (1998) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.18.10.1519 · Cited by 235 · see citing works
Self-citationAtherosclerotic plaque rupture in the apolipoprotein E knockout mouse
Johnson, J. L., & Jackson, C. L. (2001) · Atherosclerosis · doi:10.1016/s0021-9150(00)00515-3 · Cited by 221 · see citing works
Bennett, M. R., Gibson, D. F., Schwartz, S. M., & Tait, J. F. (1995) · Circulation Research · doi:10.1161/01.res.77.6.1136 · Cited by 206 · see citing works
Bennett, M. R., Evan, G. I., & Newby, A. C. (1994) · Circulation Research · doi:10.1161/01.res.74.3.525 · Cited by 201 · see citing works
Apoptosis of endothelial cells. Contribution to the pathophysiology of atherosclerosis?
Dimmeler, S., Hermann, C., & Zeiher, A. M. (1998) · PubMed · Cited by 181 · see citing works
Macrophage p53 Deficiency Leads to Enhanced Atherosclerosis in APOE*3-Leiden Transgenic Mice
van Vlijmen, B. J. M., Gerritsen, G., Franken, A. L., Boesten, L. S. M., Kockx, M. M., Gijbels, M. J., Vierboom, M., Eck, M. V., van de Water, B., van Berkel, T. J. C., et al. (2001) · Circulation Research · doi:10.1161/hh0801.089261 · Cited by 170 · see citing works
Self-citationCalara, F. B., Silvestre, M., Casanada, F., Yuan, N., Claudio Napoli, A., & Palinski, W. (2001) · The Journal of Pathology · doi:10.1002/path.915 · Cited by 167 · see citing works
Bennett, M. R., Littlewood, T. D., Schwartz, S. M., & Weissberg, P. L. (1997) · Circulation Research · doi:10.1161/01.res.81.4.591 · Cited by 132 · see citing works
Ihling, C. H., Menzel, G., Wellens, E., Mönting, J. S., Schaefer, H. E., & Zeiher, A. M. (1997) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.17.10.2218 · Cited by 99 · see citing works
Apoptosis of vascular smooth muscle cells in atherosclerosis
Bennett, M. R., & Boyle, J. J. (1998) · Atherosclerosis · doi:10.1016/s0021-9150(98)00013-6 · Cited by 98 · see citing works
Distinct Regulation of p53 and p73 Activity by Adenovirus E1A, E1B, and E4orf6 Proteins
Steegenga, W. T., Shvarts, A., Riteco, N., Bos, J. L., & Jochemsen, A. G. (1999) · Molecular and Cellular Biology · doi:10.1128/mcb.19.5.3885 · Cited by 93 · see citing works
Specific tumor-cell killing with adenovirus vectors containing the apoptin gene
Pietersen, A. M., van der Eb, M. M., Rademaker, H. J., van den Wollenberg, D. J. M., Rabelink, M. J. W. E., Kuppen, P. J. K., van Dierendonck, J. H., van Ormondt, H., Masman, D., van de Velde, C. J. �., et al. (1999) · Gene Therapy · doi:10.1038/sj.gt.3300876 · Cited by 91 · see citing works
Self-citationColocalization of CPP-32 With Apoptotic Cells in Human Atherosclerotic Plaques
Mallat, Z., Ohan, J., Lesèche, G., & Tedgui, A. (1997) · Circulation · doi:10.1161/01.cir.96.2.424 · Cited by 86 · see citing works
Apoptosis in human atherosclerosis and restenosis.
Kockx, M. M., & G, D. M. (1996) · PubMed · Cited by 74 · see citing works
Self-citationAnti-hepatocyte growth factor antibody inhibits hepatocyte proliferation during liver regeneration
Burr, A. W., Toole, K., Chapman, C., Hines, J. E., & Burt, A. D. (1998) · The Journal of Pathology · doi:10.1002/(sici)1096-9896(199807)185:3 · Cited by 67 · see citing works
Apoptosis in inflammatory–fibroproliferative disorders of the vessel wall
Walsh, K. (2000) · Cardiovascular Research · doi:10.1016/s0008-6363(99)00270-9 · Cited by 51 · see citing works
Smith, R. L., Geller, A. I., Escudero, K. W., & Wilcox, C. L. (1995) · Journal of Virology · doi:10.1128/jvi.69.8.4593-4599.1995 · Cited by 51 · see citing works
Drazan, K. E., Xd, S., Me, C., Ww, Z., Roth, J. A., Rw, B., & Shaked, A. A. (1994) · PubMed · Cited by 36 · see citing works
Tumor suppressor proteins as regulators of cell differentiation.
Li, Z., Hromchak, R., Mudipalli, A., & Bloch, A. (1998) · PubMed · Cited by 28 · see citing works
Pathophysiology of ischaemia-reperfusion injury
Carden, D. L., & Granger, D. N. (2000) · The Journal of Pathology · doi:10.1002/(sici)1096-9896(200002)190:3 · Cited by 5 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
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 · see citing works
Atherosclerotic Lesion Size and Vulnerability Are Determined by Patterns of Fluid Shear Stress
Cheng, C., Tempel, D., van Haperen, R., van der Baan, A., Grosveld, F. G., Daemen, M. J. A. P., Krams, R., & de Crom, R. (2006) · Circulation · doi:10.1161/circulationaha.105.590018 · Cited by 1,002 · see citing works
Animal models of atherosclerosis
Emini Veseli, B., Perrotta, P., De Meyer, G. R. A., Roth, L., Van der Donckt, C., Martinet, W., & De Meyer, G. R. Y. (2017) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2017.05.010 · Cited by 548 · see citing works
Vascular Cell Senescence: Contribution to Atherosclerosis
Minamino, T., & Komuro, I. (2007) · Circulation Research · doi:10.1161/01.res.0000256837.40544.4a · Cited by 542 · see citing works
Mechanisms of plaque vulnerability and rupture
Shah, P. K. (2003) · Journal of the American College of Cardiology · doi:10.1016/s0735-1097(02)02834-6 · Cited by 541 · see citing works
Atherosclerosis in the Apolipoprotein E–Deficient Mouse
Meir, K. S., & Leitersdorf, E. (2004) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000128849.12617.f4 · Cited by 498 · see citing works
Molecular Biology of Atherosclerosis
Hopkins, P. N. (2013) · Physiological Reviews · doi:10.1152/physrev.00004.2012 · Cited by 456 · see citing works
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 334 · see citing works
Pathology of the Thin‐Cap Fibroatheroma:
Virmani, R., BURKE, A. P., Kolodgie, F. D., & Farb, A. A. (2003) · Journal of Interventional Cardiology · doi:10.1034/j.1600-0854.2003.8042.x · Cited by 330 · see citing works
Kunieda, T., Minamino, T., Nishi, J.-I., Tateno, K., Oyama, T., Katsuno, T., Miyauchi, H., Orimo, M., Okada, S., Takamura, M., et al. (2006) · Circulation · doi:10.1161/circulationaha.106.626606 · Cited by 302 · see citing works
Bot, I., de Jager, S. C. A., Zernecke, A., Lindstedt, K. A., van Berkel, T. J. C., Weber, C., & Biessen, E. A. L. (2007) · Circulation · doi:10.1161/circulationaha.106.660472 · Cited by 282 · see citing works
Self-citationPlaque Rupture in Humans and Mice
Schwartz, S. M., Galis, Z. S., Rosenfeld, M. E., & Falk, E. (2007) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000261709.34878.20 · Cited by 253 · see citing works
p53 is a suppressor of inflammatory response in mice
Komarova, E. A., Krivokrysenko, V. I., Wang, K., Neznanov, N. S., Chernov, M. V., Komarov, P. G., Brennan, M., Golovkina, T. V., Rokhlin, O. W., Kuprash, D. V., et al. (2005) · The FASEB Journal · doi:10.1096/fj.04-3213fje · Cited by 243 · see citing works
Redox signaling in cardiovascular health and disease
Madamanchi, N. R., & Runge, M. S. (2013) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2013.04.001 · Cited by 223 · see citing works
Role of apoptosis in atherosclerosis and its therapeutic implications
Stoneman, V. E. A., & Bennett, M. R. (2004) · Clinical Science · doi:10.1042/cs20040086 · Cited by 219 · see citing works
de Nooijer, R., Verkleij, C. J. N., von der Thüsen, J. H., Jukema, J. W., van der Wall, E. E., van Berkel, T. J. C., Baker, A. H., & Biessen, E. A. L. (2005) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000197795.56960.64 · Cited by 220 · see citing works
Self-citationInflammation and p53: A Tale of Two Stresses
Gudkov, A. V., Gurova, K. V., & Komarova, E. A. (2011) · Genes & Cancer · doi:10.1177/1947601911409747 · Cited by 204 · see citing works
Chen, Y., Bui, A. V., Diesch, J., Manasseh, R., Hausding, C., Rivera, J., Haviv, I., Agrotis, A., Htun, N., Jowett, J. B. M., et al. (2013) · Circulation Research · doi:10.1161/circresaha.113.301562 · Cited by 206 · see citing works
Apoptotic cell death in atherosclerosis
Littlewood, T. D., & Bennett, M. R. (2003) · Current Opinion in Lipidology · doi:10.1097/00041433-200310000-00007 · Cited by 194 · see citing works
Murine Models of Vascular Thrombosis
Westrick, R. J., Winn, M. E., & Eitzman, D. T. (2007) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.107.142810 · Cited by 184 · see citing works
Mercer, J. R., Figg, N. L., Stoneman, V. E. A., Braganza, D. M., & Bennett, M. R. (2005) · Circulation Research · doi:10.1161/01.res.0000161069.15577.ca · Cited by 181 · see citing works
Matrix metalloproteinases: influence on smooth muscle cells and atherosclerotic plaque stability
Johnson, J. L. (2007) · Expert Review of Cardiovascular Therapy · doi:10.1586/14779072.5.2.265 · Cited by 172 · see citing works
The ubiquitin–proteasome system in cardiovascular diseases—a hypothesis extended
Herrmann, S. M. (2003) · Cardiovascular Research · doi:10.1016/j.cardiores.2003.09.033 · Cited by 163 · see citing works
Shear stress–induced changes in atherosclerotic plaque composition are modulated by chemokines
Cheng, C., Tempel, D., van Haperen, R., de Boer, H. C., Segers, D., Huisman, M., van Zonneveld, A. J., Leenen, P. J. M., van der Steen, A. F. W., Serruys, P. W. J. C., et al. (2007) · Journal of Clinical Investigation · doi:10.1172/jci28180 · Cited by 155 · see citing works
Atherosclerotic Plaque Rupture
Lutgens, E., van Suylen, R. J., Faber, B. C. G., Gijbels, M. J., Eurlings, P. M. H., Bijnens, A. P., Cleutjens, K. B. J. M., Heeneman, S., & Daemen, M. J. A. P. (2003) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000097783.01596.e2 · Cited by 154 · see citing works
Vascular cell senescence and vascular aging
Minamino, T., Miyauchi, H., Yoshida, T., Tateno, K., Kunieda, T., & Komuro, I. (2003) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2003.11.010 · Cited by 149 · see citing works
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 · see citing works
DNA damage and repair in atherosclerosis
Mahmoudi, M., MERCER, J., & Bennett, M. R. (2006) · Cardiovascular Research · doi:10.1016/j.cardiores.2006.03.002 · Cited by 137 · see citing works
Merched, A. J., Williams, E. M., & Chan, L. (2003) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000084825.88022.53 · Cited by 125 · see citing works
Platelet Adhesion Receptors and Their Ligands in Mouse Models of Thrombosis
Denis, C. V., & Wagner, D. D. (2007) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000259359.52265.62 · Cited by 123 · see citing works
A Simple Method of Plaque Rupture Induction in Apolipoprotein E–Deficient Mice
Sasaki, T., Kuzuya, M., Nakamura, K., Cheng, X. W., Shibata, T., Sato, K., & Iguchi, A. (2006) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000219687.71607.f7 · Cited by 120 · see citing works
p53 and the Carcinogenicity of Chronic InflammationPreprint
Gudkov, A. V., & Komarova, E. A. (2016) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a026161 · Cited by 122 · see citing works
Inflammation and Plaque Vulnerability
Shah, P. K. (2008) · Cardiovascular Drugs and Therapy · doi:10.1007/s10557-008-6147-2 · Cited by 119 · see citing works
Assessment of Unstable Atherosclerosis in Mice
Jackson, C. L., Bennett, M. R., Biessen, E. A. L., Johnson, J. L., & Krams, R. (2007) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000261873.86623.e1 · Cited by 119 · see citing works
Self-citationGranzyme B Induces Smooth Muscle Cell Apoptosis in the Absence of Perforin
Choy, J. C., Hung, V. H. Y., Hunter, A. L., Cheung, P., Motyka, B., Goping, I. S., Sawchuk, T., Bleackley, R. C., Podor, T. J., McManus, B. M., et al. (2004) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000147162.51930.b7 · Cited by 117 · see citing works
The Emerging Role of Vascular Smooth Muscle Cell Apoptosis in Atherosclerosis and Plaque Stability
Clarke, M. C. H., & Bennett, M. R. (2006) · American Journal of Nephrology · doi:10.1159/000097815 · Cited by 115 · see citing works
Pathologies Associated with the p53 ResponsePreprint
Gudkov, A. V., & Komarova, E. A. (2010) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a001180 · Cited by 116 · see citing works
MMP-7 mediates cleavage of N-cadherin and promotes smooth muscle cell apoptosis
Williams, H. J., Johnson, J. L., Jackson, C. L., White, S. J., & George, S. J. (2010) · Cardiovascular Research · doi:10.1093/cvr/cvq042 · Cited by 114 · see citing works
Rupture of the Atherosclerotic Plaque
Cullen, P., Baetta, R., Bellosta, S., Bernini, F., Chinetti, G., Cignarella, A., von Eckardstein, A., Exley, A., Goddard, M. J., Hofker, M. H., et al. (2003) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000060200.73623.f8 · Cited by 114 · see citing works
Kuijpers, M. J. E., Gilio, K., Reitsma, S., Nergiz‐Unal, R., Prinzen, L., Heeneman, S., Lutgens, E., van Zandvoort, M. A. M. J., Nieswandt, B., Egbrink, M. G. A. O., et al. (2008) · Journal of Thrombosis and Haemostasis · doi:10.1111/j.1538-7836.2008.03186.x · Cited by 113 · see citing works
Intramural Plasminogen Activator Inhibitor Type-1 and Coronary Atherosclerosis
Sobel, B. E., Taatjes, D. J., & Schneider, D. J. (2003) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000091250.53231.4d · Cited by 112 · see citing works
Molecular mechanisms of plaque instability
Shah, P. K. (2007) · Current Opinion in Lipidology · doi:10.1097/mol.0b013e3282efa326 · Cited by 109 · see citing works
Development of experimental designs for atherosclerosis studies in mice
Daugherty, A., & Rateri, D. L. (2005) · Methods · doi:10.1016/j.ymeth.2004.11.008 · Cited by 103 · see citing works
Overstreet, J. M., Samarakoon, R., Meldrum, K. K., & Higgins, P. J. (2014) · Cellular Signalling · doi:10.1016/j.cellsig.2014.02.017 · Cited by 103 · see citing works
Control of cell proliferation in atherosclerosis: insights from animal models and human studies
Fuster, J. J., Fernandez, P., Navarro, H. G., Silvestre, C., Nabah, Y. N. A., & Andrés, V. (2009) · Cardiovascular Research · doi:10.1093/cvr/cvp363 · Cited by 101 · see citing works
Oxidation of LDL, Atherogenesis, and Apoptosis
Claudio Napoli, A. (2003) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1299.127 · Cited by 99 · see citing works
DNA damage, p53, apoptosis and vascular disease
Mercer, J. R., Mahmoudi, M., & Bennett, M. R. (2007) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2007.02.011 · Cited by 97 · see citing works
de Nooijer, R., von der Thüsen, J. H., Verkleij, C. J. N., Kuiper, J., Jukema, J. W., van der Wall, E. E., van Berkel, T. J. C., & Biessen, E. A. L. (2004) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000147126.99529.0a · Cited by 97 · see citing works
Self-citationThe Pathogenesis of Atherosclerosis
Cullen, P., Rauterberg, J., & Stefan Lorkowski, A. (2005) · Handbook of experimental pharmacology · doi:10.1007/3-540-27661-0_1 · Cited by 96 · see citing works
Emotional stressors trigger cardiovascular events
Schwartz, B. G., French, W. J., Mayeda, G. S., Burstein, S., Economides, C., Bhandari, A. K., Cannom, D. S., & Kloner, R. A. (2012) · International Journal of Clinical Practice · doi:10.1111/j.1742-1241.2012.02920.x · Cited by 94 · see citing works
Choy, J. C., McDonald, P. C., Suarez, A., Hung, V. H. Y., Wilson, J. E., McManus, B. M., & Granville, D. J. (2003) · Modern Pathology · doi:10.1097/01.mp.0000067424.12280.bc · Cited by 93 · see citing works
Rosner, D., Stoneman, V. E. A., Littlewood, T. D., McCarthy, N. J., Figg, N. L., Wang, Y., Tellides, G., & Bennett, M. R. (2006) · American Journal Of Pathology · doi:10.2353/ajpath.2006.050473 · Cited by 93 · see citing works
van der Meer, F. J., Faber, D. J., Aalders, M. C. G., Poot, A. A., Vermes, I., & van Leeuwen, T. G. J. M. (2009) · Lasers in Medical Science · doi:10.1007/s10103-009-0723-y · Cited by 84 · see citing works
von der Thüsen, J. H., Borensztajn, K., Moimas, S., van Heiningen, S., Teeling, P., van Berkel, T. J. C., & Biessen, E. A. L. (2011) · American Journal Of Pathology · doi:10.1016/j.ajpath.2010.10.007 · Cited by 87 · see citing works
Self-citationAkhtar, S., Gremse, F., Kiessling, F. M., Weber, C., & Schober, A. (2013) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.112.301162 · Cited by 86 · see citing works
DNA damage, vascular senescence and atherosclerosis
Andreassi, M. G. (2008) · Journal of Molecular Medicine · doi:10.1007/s00109-008-0358-7 · Cited by 86 · see citing works
The Role of p53 in Atherosclerosis
Mercer, J. R., & Bennett, M. R. (2006) · Cell Cycle · doi:10.4161/cc.5.17.3166 · Cited by 82 · see citing works
Unraveling Pleiotropic Effects of Statins on Plaque Rupture
Palinski, W., & Claudio Napoli, A. (2002) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000038754.39483.cd · Cited by 82 · see citing works
Pathophysiology of plaque rupture and the concept of plaque stabilization
Shah, P. K. (2003) · Cardiology Clinics · doi:10.1016/s0733-8651(03)00058-4 · Cited by 79 · see citing works
Animal Models of Atherosclerosis
Fuster, J. J., Castillo, A. I., Zaragoza, C., Ibáñez, B., & Andrés, V. (2011) · Progress in molecular biology and translational science · doi:10.1016/b978-0-12-394596-9.00001-9 · Cited by 75 · see citing works
Cell death in the cardiovascular system
Clarke, M. C. H., Bennett, M. R., & Littlewood, T. D. (2006) · Heart · doi:10.1136/hrt.2006.088203 · Cited by 70 · see citing works
Merched, A. J., & Chan, L. (2004) · Circulation · doi:10.1161/01.cir.0000148681.01282.89 · Cited by 70 · see citing works
Marfella, R., Amico, M. D., Filippo, C. D., Siniscalchi, M., Sasso, F. C., Ferraraccio, F., Rossi, F., & Paolisso, G. (2007) · Cardiovascular Diabetology · doi:10.1186/1475-2840-6-35 · Cited by 69 · see citing works
Models to Study Atherosclerosis: A Mechanistic Insight
Singh, V., Tiwari, R. L., Dikshit, M., & Barthwal, M. K. (2009) · Current Vascular Pharmacology · doi:10.2174/157016109787354097 · Cited by 63 · see citing works
The Pre-Clinical Animal Model in the Translational Research of Interventional Cardiology
Suzuki, Y., Yeung, A. C., & Ikeno, F. (2009) · JACC: Cardiovascular Interventions · doi:10.1016/j.jcin.2009.03.004 · Cited by 63 · see citing works
Cheng, C., Tempel, D., van Haperen, R., van Damme, L., Algür, M., Krams, R., & de Crom, R. (2009) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2009.01.025 · Cited by 62 · see citing works
N-Cadherin–Dependent Cell–Cell Contacts Promote Human Saphenous Vein Smooth Muscle Cell Survival
Koutsouki, E., Beeching, C. A., Slater, S. C., Blaschuk, O. W., Sala‐Newby, G. B., & George, S. J. (2005) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000163183.27658.4b · Cited by 62 · see citing works
Vessel wall apoptosis and atherosclerotic plaque instability
Kavurma, M. M., Bhindi, R., Lowe, H. C., Chesterman, C. N., & Khachigian, L. M. (2005) · Journal of Thrombosis and Haemostasis · doi:10.1111/j.1538-7836.2005.01120.x · Cited by 62 · see citing works
Bond, A., & Jackson, C. L. (2010) · BioMed Research International · doi:10.1155/2011/379069 · Cited by 59 · see citing works
Comparison of two murine models of thrombosis induced by atherosclerotic plaque injury
Hechler, B., & Gachet, C. (2011) · Thrombosis and Haemostasis · doi:10.1160/ths10-11-0730 · Cited by 59 · see citing works
Kumar, S., Chen, M., Li, Y., Wong, F. H. S., Thiam, C. H., Hossain, M. Z., Poh, K. K., Hirohata, S., Ogawa, H., Angéli, V., et al. (2016) · Scientific Reports · doi:10.1038/srep31130 · Cited by 59 · see citing works
Jin, S., Shen, L., Nie, P., Yuan, W., Hu, L., Li, D., Chen, X., Zhang, X.-K., & He, B. (2012) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.111.236158 · Cited by 57 · see citing works
Artwohl, M., Lindenmair, A., Roden, M., Waldhäusl, W., Freudenthaler, A., Klosner, G., İlhan, A., Luger, A., & Baumgartner-Parzer, S. M. (2008) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2008.05.030 · Cited by 56 · see citing works
Tsirpanlis, G. I. (2008) · American Journal of Kidney Diseases · doi:10.1053/j.ajkd.2007.07.035 · Cited by 54 · see citing works
Madeddu, P. R., Emanueli, C., Spillmann, F., Meloni, M., Bouby, N., Richer, C., Alhenc‐Gelas, F., van Weel, V., Eefting, D., Quax, P. H. A., et al. (2006) · Vascular Pharmacology · doi:10.1016/j.vph.2006.08.008 · Cited by 56 · see citing works
Cadherin:catenin complex: A novel regulator of vascular smooth muscle cell behaviour
George, S. J., & Beeching, C. A. (2006) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2005.12.017 · Cited by 54 · see citing works
The role of p53 in the alternation of vascular functions
Chan, G. H. H., Chan, E., Kwok, C. T., Leung, G., Lee, S. M., & Seto, S. W. (2022) · Frontiers in Pharmacology · doi:10.3389/fphar.2022.981152 · Cited by 53 · see citing works
Zadelaar, A. S. M., von der Thüsen, J. H., MBOESTEN, L., Hoeben, R. C., KOCKX, M., Versnel, M. A., VANBERKEL, T., Havekes, L. M., LBIESSEN, E., & VANVLIJMEN, B. (2005) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2005.03.044 · Cited by 52 · see citing works
Self-citationSoluble N-Cadherin Overexpression Reduces Features of Atherosclerotic Plaque Instability
Lyon, C. A., Johnson, J. L., Williams, H., Sala-Newby, G. B., & George, S. J. (2009) · Arteriosclerosis, Thrombosis, and Vascular Biology · doi:10.1161/atvbaha.108.178087 · Cited by 51 · see citing works
Mill, C., Monk, B. A., Williams, H. J., Simmonds, S. J., Jeremy, J. Y., Johnson, J. L., & George, S. J. (2014) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.114.303922 · Cited by 51 · see citing works
Complement factor C5a induces atherosclerotic plaque disruptions
Wezel, A., de Vries, M. R., Lagraauw, H. M., Foks, A. C., Kuiper, J., Quax, P. H. A., & Bot, I. (2014) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.12357 · Cited by 51 · see citing works
Golshiri, K., Ataabadi, E. A., Portilla-Fernández, E., Danser, A. H. J., & Roks, A. J. M. (2019) · Basic & Clinical Pharmacology & Toxicology · doi:10.1111/bcpt.13319 · Cited by 51 · see citing works
Zhang, K., Huang, X., Li, X., Feng, M., Li, L., Cai, X., Zhang, C., Liu, X., Zhang, M., Zhang, Y., et al. (2012) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2012.09.007 · Cited by 50 · see citing works
Ling, M., Ma, Z.-Y., Wang, Y., Qi, J., Liu, L., Li, L., & Zhang, Y. (2012) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2012.11.016 · Cited by 50 · see citing works
Winkel, L. C. J., Hoogendoorn, A., Xing, R., Wentzel, J. J., & der Heiden, K. V. (2015) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2015.04.796 · Cited by 49 · see citing works
Using Mice to Dissect Genetic Factors in Atherosclerosis
Allayee, H., Ghazalpour, A., & Lusis, A. J. (2003) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000090886.40027.dc · Cited by 49 · see citing works
Wan, S., George, S. J., Nicklin, S. A., Yim, A. P. C., & Baker, A. H. (2004) · Molecular Therapy · doi:10.1016/j.ymthe.2004.02.005 · Cited by 48 · see citing works
Chen, W. Q., Zhang, L., Liu, Y., Chen, L., Ji, X. P., Zhang, M., Zhao, Y. X., Yao, G., Zhang, C., Wang, X. L., et al. (2007) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00472.2007 · Cited by 47 · see citing works
Ni, M., Wang, Y., Zhang, M., Zhang, P. F., Ding, S. F., Liu, C. X., Liu, X. L., Zhao, Y. X., & Zhang, Y. (2009) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.01202.2008 · Cited by 46 · see citing works
Cbx3 inhibits vascular smooth muscle cell proliferation, migration, and neointima formation
Zhang, C., Chen, D., Maguire, E. M., He, S., Chen, J., An, W., Yang, M., Afzal, T. A., Luong, L. A., Zhang, L., et al. (2017) · Cardiovascular Research · doi:10.1093/cvr/cvx236 · Cited by 45 · see citing works
apoB and apobec1, two genes key to lipid metabolism, are transcriptionally regulated by p53
Ashur‐Fabian, O., Har‐Zahav, A., Shaish, A., Amram, H. W., Margalit, O., Weizer‐Stern, O., Dominissini, D., Harats, D., Amariglio, N., & Rechavi, G. (2010) · Cell Cycle · doi:10.4161/cc.9.18.12993 · Cited by 43 · see citing works
DNA damage response signaling: A common link between cancer and cardiovascular diseases
Nikfarjam, S., & Singh, K. K. (2022) · Cancer Medicine · doi:10.1002/cam4.5274 · Cited by 43 · see citing works
Acute and persistent platelet and coagulant activities in atherothrombosis
Mastenbroek, T. G., van Geffen, J. P., Heemskerk, J. W. M., & Cosemans, J. M. E. M. (2015) · Journal of Thrombosis and Haemostasis · doi:10.1111/jth.12972 · Cited by 41 · see citing works
Ma, T., Gao, Q., Zhu, F., Guo, C., Wang, Q., Gao, F., & Zhang, L. (2013) · Cellular and Molecular Immunology · doi:10.1038/cmi.2013.4 · Cited by 41 · see citing works
Sanz-Gonzalez, S. M., BARQUIN, L., Garcı́a-Cao, I., Roqué, M., GONZALEZ, J., Fuster, J. J., CASTELLS, M., FLORES, J., Serrano, M., & Andrés, V. (2007) · Cardiovascular Research · doi:10.1016/j.cardiores.2007.05.002 · Cited by 41 · see citing works
Overexpression of Lysosomal Acid Lipase and Other Proteins in Atherosclerosis
Zschenker, O., Illies, T., & Ameis, D. (2006) · The Journal of Biochemistry · doi:10.1093/jb/mvj137 · Cited by 40 · see citing works
Reduced Immunoregulatory CD31 + T Cells in the Blood of Atherosclerotic Mice With Plaque Thrombosis
Caligiuri, G., Groyer, É., Khallou‐Laschet, J., Zen, A. A. H., Sainz, J., Urbain, D., Gaston, A., Lemitre, M., Nicoletti, A., & Lafont, A. M. (2005) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000172660.24580.b4 · Cited by 40 · see citing works
Aparicio-Vergara, M., Shiri‐Sverdlov, R., de Haan, G., & Hofker, M. H. (2010) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2010.05.030 · Cited by 40 · see citing works
Hashimoto, T., Ichiki, T., Ikeda, J., Narabayashi, E., Matsuura, H., Miyazaki, R., Inanaga, K., Takeda, K., & Sunagawa, K. (2011) · Cardiovascular Research · doi:10.1093/cvr/cvr108 · Cited by 38 · see citing works
Luo, Y., Guo, Y., Wang, H. H., Yu, M., Hong, K. W., Li, D., Li, R., Wen, B., Hu, D., Chang, L., et al. (2021) · EBioMedicine · doi:10.1016/j.ebiom.2021.103725 · Cited by 39 · see citing works
- Authors
- von der Thüsen, J. H., van Vlijmen, B. J. M., Hoeben, R. C., Kockx, M. M., Havekes, L. M., van Berkel, T. J. C., & Biessen, E. A. L.
- Affiliations
- From the Division of Biopharmaceutics (J.H.v.d.T., T.J.C.v.B., E.A.L.B.), Leiden/Amsterdam Center for Drug Research; Molecular Virology Group, Department of Molecular Cell Biology (R.C.H.) and Department of Cardiology (J.H.v.d.T.), Leiden University Medical Center; and TNO-PG (B.J.M.v.V., L.M.H.), Leiden, the Netherlands; and Department of Pathology (M.M.K.), Middelheim Academic Hospital, Antwerp, Belgium.
- Leiden University (NL)
- Venue
- Circulation
- Published
- 2002-04-30
- Volume
- 105
- Issue
- 17
- Pages
- 2064-2070
- ISSN
- 0009-7322 (ISSN-L)
- 1524-4539
- OpenAlex
- W2122574397
- Cited by
- 203
- References
- 32
- Citations by year
- 2026: 2 · 2025: 3 · 2024: 2 · 2023: 1 · 2022: 3 · 2021: 6 · 2020: 3 · 2019: 6 · 2018: 5 · 2017: 5 · 2016: 4 · 2015: 7 · 2014: 8 · 2013: 10 · 2012: 8
- FWCI
- 5.80
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Circulation (publishedVersion)
- PubMed (publishedVersion)
- TNO Repository (submittedVersion)
- Repository hosted by TU Delft Library (TU Delft) (submittedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Funders
- Koninklijke Nederlandse Akademie van Wetenschappen
- 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 › Coronary Interventions and Diagnostics
- Keywords
- atherosclerotic plaque rupture, p53, plaque destabilization, plaque remodeling, smooth muscle cell apoptosis, ApoE-deficient mice, adenoviral gene transfer, phenylephrine, plaque vulnerability
- MeSH terms
- Adenoviridae, Animals, Apolipoproteins E, Arteriosclerosis, beta-Galactosidase, Carotid Artery Diseases, Cell Division, Genetic Vectors, Immunohistochemistry, Muscle, Smooth, Vascular, Transfection, Biomarkers, Tumor Suppressor Protein p53, Apoptosis, Mice, Knockout, 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