Molecular Imaging of Matrix Metalloproteinase in Atherosclerotic Lesions
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Objectives This study sought to evaluate the feasibility of noninvasive detection of matrix metalloproteinase (MMP) activity in experimental atherosclerosis using technetium-99m-labeled broad matrix metalloproteinase inhibitor (MPI) and to determine the effect of dietary modification and statin treatment on MMP activity.Background The MMP activity in atherosclerotic lesions contributes to the vulnerability of atherosclerotic plaques to rupture.Methods Atherosclerosis was produced in 34 New Zealand White rabbits by balloon de-endotheliazation of the abdominal aorta and a high-cholesterol diet. In addition, 12 unmanipulated rabbits were used as controls and 3 for blood clearance characteristics. In vivo micro-single-photon emission computed tomography (SPECT) imaging was performed after radiolabeled MPI administration. Subsequently, aortas were explanted to quantitatively measure percent injected dose per gram (%ID/g) MPI uptake. Histological and immunohistochemical characterization was performed and the extent of MMP activity was determined by gel zymography or enzyme-linked immunosorbent assays.Results The MPI uptake in atherosclerotic lesions (n = 18) was clearly visualized by micro-SPECT imaging; MPI uptake was markedly reduced by administration of unlabeled MPI before the radiotracer (n = 4). The MPI uptake was also significantly reduced after diet withdrawal (n = 6) and fluvastatin treatment (n = 6); no uptake was observed in normal control rabbits (n = 12). The %ID/g MPI uptake (0.10 +/- 0.03%) in the atherosclerotic lesions was significantly higher than the uptake in control aorta (0.016 +/- 0.004%, p < 0.0001). Uptake in fluvastatin (0.056 +/- 0.011%, p < 0.0005) and diet withdrawal groups (0.043 +/- 0.011%, p < 0.0001) was lower than the untreated group. The MPI uptake correlated with immunohistochemically verified macrophage infiltration (r = 0.643, p < 0.0001), and MMP-2 (r = 0.542, p < 0.0001) or MMP-9 (r = 0.578, p < 0.0001) expression in plaques.Conclusions The present data show the feasibility of noninvasive detection of MMP activity in atherosclerotic plaques, and confirm that dietary modification and statin therapy reduce MMP activity.
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Various radioactive tracers have been developed to detect different aspects of atherosclerotic disease more specifically.
“To detect different aspects of atherosclerotic disease more specifically, various radioactive tracers have been developed145–147.”
From Perspectives and opportunities for nanomedicine in the management of atherosclerosis (2011) · cites this paper as [145]
Cites
Visse, R., & Nagase, H. (2003) · Circulation Research · doi:10.1161/01.res.0000070112.80711.3d · Cited by 4,575 · see citing works
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 · see citing works
Galis, Z. S., Sukhova, G. K., Lark, M. W., & Libby, P. (1994) · Journal of Clinical Investigation · doi:10.1172/jci117619 · Cited by 2,537 · see citing works
Pathology of the Vulnerable Plaque
Virmani, R., BURKE, A. P., Farb, A. A., & Kolodgie, F. D. (2006) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2005.10.065 · Cited by 2,358 · see citing works
Davies, M. J., & Thomas, A. C. (1985) · Heart · doi:10.1136/hrt.53.4.363 · Cited by 1,985 · see citing works
van der Wal, A. C., Becker, A. E., van der Loos, C. M., & Das, P. K. (1994) · Circulation · doi:10.1161/01.cir.89.1.36 · Cited by 1,906 · see citing works
Matrix metalloproteinases in vascular remodeling and atherogenesis: the good, the bad, and the ugly.
Galis, Z. S., & Khatri, J. J. (2002) · PubMed · Cited by 1,787 · see citing works
Matrix Metalloproteinases in Vascular Remodeling and Atherogenesis
Galis, Z. S., & Khatri, J. J. (2002) · Circulation Research · doi:10.1161/res.90.3.251 · Cited by 1,550 · see citing works
Coronary Plaque Erosion Without Rupture Into a Lipid Core
Farb, A. A., BURKE, A. P., Tang, A. L., Liang, Y.-H., Mannan, P., Smialek, J. E., & Virmani, R. (1996) · Circulation · doi:10.1161/01.cir.93.7.1354 · Cited by 1,274 · see citing works
Macrophage infiltration in acute coronary syndromes. Implications for plaque rupture.
Moreno, P., Falk, E., Palacios, I. F., Newell, J. B., Fuster, V., & Fallon, J. T. (1994) · Circulation · doi:10.1161/01.cir.90.2.775 · Cited by 1,105 · see citing works
Crisby, M., Fredrikson, G. N., Shah, P. K., Yano, J., Zhu, J., & Nilsson, J. Å. (2001) · Circulation · doi:10.1161/01.cir.103.7.926 · Cited by 999 · see citing works
Blankenberg, S., Rupprecht, H. J., Poirier, O., Bickel, C., Smieja, M., Hafner, G., Meyer, J., Cambien, F., & Tiret, L. (2003) · Circulation · doi:10.1161/01.cir.0000058700.41738.12 · Cited by 755 · see citing works
Shah, P. K., Falk, E., Badimón, J. J., Fernández‐Ortíz, A., Mailhac, A. C., Villareal-Levy, G., Fallon, J. T., Regnström, J., & Fuster, V. (1995) · PubMed · Cited by 722 · see citing works
Sukhova, G. K., Schönbeck, U., Aikawa, E. R., Schöen, F. J., Poole, A. R., Billinghurst, R. C., & Libby, P. (1999) · Circulation · doi:10.1161/01.cir.99.19.2503 · Cited by 657 · see citing works
Simvastatin Attenuates Plaque Inflammation
Tahara, N., Kai, H., Ishibashi, M., Nakaura, H., Kaida, H., Baba, K., Hayabuchi, N., & Imaizumi, T. (2006) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2006.03.069 · Cited by 649 · see citing works
Kai, H., Ikeda, H., Yasukawa, H., Kai, M., Seki, Y., Kuwahara, F., Ueno, T., Sugi, K., & Imaizumi, T. (1998) · Journal of the American College of Cardiology · doi:10.1016/s0735-1097(98)00250-2 · Cited by 591 · see citing works
Aikawa, M., Aikawa, E. R., Sugiyama, S., Voglic, S. J., Fukumoto, Y., Furukawa, Y., Shiomi, M., Schöen, F. J., & Libby, P. (2001) · Circulation · doi:10.1161/01.cir.103.2.276 · Cited by 587 · see citing works
Relationship Between Coronary Artery Remodeling and Plaque Vulnerability
Varnava, A. M., Mills, P. G., & Davies, M. J. (2002) · Circulation · doi:10.1161/hc0802.104327 · Cited by 557 · see citing works
Galis, Z. S., Sukhova, G. K., Kranzhöfer, R., Clark, S. C., & Libby, P. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.2.402 · Cited by 557 · see citing works
Aikawa, M., Aikawa, E. R., Okada, Y., Voglic, S. J., Clinton, S. K., Brinckerhoff, C., Sukhova, G. K., & Libby, P. (1998) · Circulation · doi:10.1161/01.cir.97.24.2433 · Cited by 552 · see citing works
Atherosclerotic plaque caps are locally weakened when macrophages density is increased
Lendon, C. L., Davies, M. J., Born, G. V. R., & Richardson, P. D. (1991) · Atherosclerosis · doi:10.1016/0021-9150(91)90235-u · Cited by 547 · see citing works
HMG-CoA Reductase Inhibitors Reduce MMP-9 Secretion by Macrophages
Bellosta, S., Via, D. P., Canavesi, M., Pfister, P., Fumagalli, R., Paoletti, R., & Bernini, F. (1998) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.18.11.1671 · Cited by 512 · see citing works
Identification of 92-kD Gelatinase in Human Coronary Atherosclerotic Lesions
Brown, D., Hibbs, M. S., Kearney, M., Loushin, C., & Isner, J. M. (1995) · Circulation · doi:10.1161/01.cir.91.8.2125 · Cited by 487 · see citing works
Macrophage expression of active MMP-9 induces acute plaque disruption in apoE-deficient mice
Gough, P. J. (2005) · Journal of Clinical Investigation · doi:10.1172/jci25074 · Cited by 453 · see citing works
Welgus, H. G., Campbell, E. J., Cury, J., Eisen, A. Z., Senior, R. M., Wilhelm, S. M., & Goldberg, G. I. (1990) · Journal of Clinical Investigation · doi:10.1172/jci114867 · Cited by 446 · see citing works
Increased Matrix Metalloproteinase-9 Activity in Unstable Carotid Plaques
Loftus, I. M., Naylor, A. R., Goodall, S., Crowther, M., Jones, L., Bell, P. R. F., & Thompson, M. M. (2000) · Stroke · doi:10.1161/01.str.31.1.40 · Cited by 419 · see citing works
Inflammation in Atherosclerosis
Deguchi, J., Aikawa, M., Tung, C., Aikawa, E. R., Kim, D., Ntziachristos, V., Weissleder, R., & Libby, P. (2006) · Circulation · doi:10.1161/circulationaha.106.619056 · Cited by 418 · see citing works
Galis, Z. S., Johnson, C., Godin, D., Magid, R., Shipley, J. M., Senior, R. M., & Ivan, E. (2002) · Circulation Research · doi:10.1161/01.res.0000041036.86977.14 · Cited by 417 · see citing works
Interstitial Collagenase (MMP-1) Expression in Human Carotid Atherosclerosis
Nikkari, S. T., O’Brien, K. D., Ferguson, M. S., Hatsukami, T. S., Welgus, H. G., Alpers, C. E., & Clowes, A. W. (1995) · Circulation · doi:10.1161/01.cir.92.6.1393 · Cited by 395 · see citing works
Fukumoto, Y., Libby, P., Aikawa, E. R., Hill, C. C., Enomoto, M., Hirouchi, Y., Shiomi, M., & Aikawa, M. (2001) · Circulation · doi:10.1161/01.cir.103.7.993 · Cited by 383 · see citing works
Luan, Z.-X., Chase, A. J., & Newby, A. C. (2003) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000068646.76823.ae · Cited by 341 · see citing works
Pasterkamp, G., Schoneveld, A. H., van der Wal, A. C., Haudenschild, C. C., Clarijs, R., Becker, A. E., Hillen, B., & Borst, C. (1998) · Journal of the American College of Cardiology · doi:10.1016/s0735-1097(98)00304-0 · Cited by 339 · see citing works
Pasterkamp, G., Schoneveld, A. H., Hijnen, D., de Kleijn, D. P. V., Teepen, H. L. J. M., van der Wal, A. C., & Borst, C. (2000) · Atherosclerosis · doi:10.1016/s0021-9150(99)00371-8 · Cited by 298 · see citing works
Targeting of Apoptotic Macrophages and Experimental Atheroma With Radiolabeled Annexin V
Kolodgie, F. D., Petrov, A. D., Virmani, R., Narula, N., Verjans, J. W. H., Weber, D. K., Hartung, D., Steinmetz, N. D., Vanderheyden, J. L., Vannan, M. A., et al. (2003) · Circulation · doi:10.1161/01.cir.0000105761.00573.50 · Cited by 249 · see citing works
Self-citationIncreased expression of 72-kd type IV collagenase (MMP-2) in human aortic atherosclerotic lesions.
Li, Z., Li, L., Zielke, H. R., Cheng, L., Xiao, R., Crow, M. T., Stetler‐Stevenson, W. G., Froehlich, J. P., & Lakatta, E. G. (1996) · Europe PMC (PubMed Central) · Cited by 243 · see citing works
Scintigraphic Imaging of Matrix Metalloproteinase Activity in the Arterial Wall In Vivo
Schäfers, M. A., Riemann, B., Kopka, K., Breyholz, H., Wagner, S., Schäfers, K. P., Law, M. P., Schober, O., & Levkau, B. (2004) · Circulation · doi:10.1161/01.cir.0000129088.49276.83 · Cited by 215 · see citing works
Su, H., Spinale, F. G., Dobrucki, L. W., Song, J., Hua, J., Sweterlitsch, S. E., Dione, D. P., Cavaliere, P., Chow, C., Bourke, B. N., et al. (2005) · Circulation · doi:10.1161/circulationaha.105.583021 · Cited by 203 · see citing works
Self-citationN -Acetyl-Cysteine Decreases the Matrix-Degrading Capacity of Macrophage-Derived Foam Cells
Galis, Z. S., Asanuma, K., Godin, D., & Meng, X. (1998) · Circulation · doi:10.1161/01.cir.97.24.2445 · Cited by 160 · see citing works
PRESCOTT, M. F., Sawyer, W. K., LINDEN‐REED, J. V., Jeune, M. R., Chou, M., Caplan, S. L., & Jeng, A. Y. (1999) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1999.tb07683.x · Cited by 143 · see citing works
Eldrup, N., Grønholdt, M.-L. M., Sillesen, H. H., & Nordestgaard, B. G. (2006) · Circulation · doi:10.1161/circulationaha.105.593483 · Cited by 80 · see citing works
Xue, C., Voss, M. E., Nelson, D. J., Duan, J. J. ‐., Cherney, R. J., Jacobson, I. C., He, X., Roderick, J. J., Chen, L., Corbett, R. L., et al. (2001) · Journal of Medicinal Chemistry · doi:10.1021/jm010127e · Cited by 79 · see citing works
Hartung, D., Schäfers, M. A., Fujimoto, S., Levkau, B., Narula, N., Kopka, K., Virmani, R., Reutelingsperger, C. P. M., Hofstra, L., Kolodgie, F. D., et al. (2007) · European Journal of Nuclear Medicine and Molecular Imaging · doi:10.1007/s00259-007-0435-0 · Cited by 33 · see citing works
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Pleiotropic Effects of Statins - Basic Research and Clinical Perspectives -
Zhou, Q., & Liao, J. K. (2010) · Circulation Journal · doi:10.1253/circj.cj-10-0110 · Cited by 567 · see citing works
Perspectives and opportunities for nanomedicine in the management of atherosclerosis
Lobatto, M. E., Fuster, V., Fayad, Z. A., & Mulder, W. J. M. (2011) · Nature Reviews Drug Discovery · doi:10.1038/nrd3578 · Cited by 423 · see citing works
Serial Coronary CT Angiography–Verified Changes in Plaque Characteristics as an End Point
Inoue, K., Motoyama, S., Sarai, M., Sato, T., Harigaya, H., Hara, T., Sanda, Y., Anno, H., Kondo, T., Wong, N. D., et al. (2010) · JACC. Cardiovascular imaging · doi:10.1016/j.jcmg.2010.04.011 · Cited by 179 · see citing works
Self-citation2-deoxy-2-[18F]fluoro-d-mannose positron emission tomography imaging in atherosclerosis
Tahara, N., Mukherjee, J., de Haas, H. J., Petrov, A. D., Tawakol, A. A., Haider, N., Tahara, A., Constantinescu, C. C., Zhou, J. F., Boersma, H. H., et al. (2014) · Nature Medicine · doi:10.1038/nm.3437 · Cited by 177 · see citing works
Self-citationVancraeynest, D., Pasquet, A., Roelants, V., Gerber, B. L., & Vanoverschelde, J. (2011) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2011.02.018 · Cited by 174 · see citing works
Arithmetic of vulnerable plaques for noninvasive imaging
Narula, J., Garg, P. K., Achenbach, S. S., Motoyama, S., Virmani, R., & Strausś, H. W. (2008) · Nature Clinical Practice Cardiovascular Medicine · doi:10.1038/ncpcardio1247 · Cited by 167 · see citing works
Self-citationLDL oxidation by platelets propagates platelet activation via an oxidative stress-mediated mechanism
Carnevale, R., Bartimoccia, S., Nocella, C., Santo, S. D., Loffredo, L., Illuminati, G., Lombardi, E., Boz, V., Ben, M. D., Marco, L. D., et al. (2014) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2014.08.041 · Cited by 116 · see citing works
Vascular Extracellular Matrix in Atherosclerosis
Chistiakov, D. A., Sobenin, I. A., & Orekhov, A. N. (2013) · Cardiology in Review · doi:10.1097/crd.0b013e31828c5ced · Cited by 114 · see citing works
Non-invasive anatomic and functional imaging of vascular inflammation and unstable plaque
Camici, P. G., Rimoldi, O. E., Gaemperli, O., & Libby, P. (2012) · European Heart Journal · doi:10.1093/eurheartj/ehs067 · Cited by 104 · see citing works
Molecular imaging of inflammation - Current and emerging technologies for diagnosis and treatment
MacRitchie, N. A., Frleta‐Gilchrist, M., Sugiyama, A., Lawton, T., McInnes, I. B., & Maffia, P. (2020) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2020.107550 · Cited by 104 · see citing works
Molecular Imaging of the Cardiac Extracellular Matrix
de Haas, H. J., Arbustini, E., Fuster, V., Kramer, C. M., & Narula, J. (2014) · Circulation Research · doi:10.1161/circresaha.113.302680 · Cited by 101 · see citing works
Self-citationImaging Atherosclerosis and Vulnerable Plaque
Sadeghi, M. M., Glover, D. K., Lanza, G. M., Fayad, Z. A., & Johnson, L. L. (2010) · Journal of Nuclear Medicine · doi:10.2967/jnumed.109.068163 · Cited by 99 · see citing works
Maruf, A., Wang, Y., Yin, T., Huang, J., Wang, N., Durkan, C., Tan, Y., Wu, W., & Wang, G. (2019) · Advanced Healthcare Materials · doi:10.1002/adhm.201900036 · Cited by 84 · see citing works
Ohshima, S., Petrov, A. D., Fujimoto, S., Zhou, J. F., Azure, M. T., Edwards, D. S., Murohara, T., Narula, N., Tsimikas, S., & Narula, J. (2009) · Journal of Nuclear Medicine · doi:10.2967/jnumed.108.055889 · Cited by 70 · see citing works
Self-citationLi, X., Bauer, W. R., Israel, I., Kreissl, M. C., Weirather, J., Richter, D., Bauer, E., Herold, V., Jakob, P. M., Buck, A. K., et al. (2014) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.114.303485 · Cited by 70 · see citing works
Molecular imaging of macrophage protease activity in cardiovascular inflammation in vivo
Quillard, T., Croce, K., Jaffer, F. A., Weissleder, R., & Libby, P. (2011) · Thrombosis and Haemostasis · doi:10.1160/th10-09-0589 · Cited by 67 · see citing works
Advanced Carotid Plaque Imaging
Hermus, L., van Dam, G. M., & Zeebregts, C. J. (2009) · European Journal of Vascular and Endovascular Surgery · doi:10.1016/j.ejvs.2009.11.020 · Cited by 67 · see citing works
Razavian, M., Tavakoli, S., Zhang, J., Nie, L., Dobrucki, L. W., Sinusas, A. J., Azure, M. T., Robinson, S. P., & Sadeghi, M. M. (2011) · Journal of Nuclear Medicine · doi:10.2967/jnumed.111.092379 · Cited by 67 · see citing works
Self-citationMolecular Imaging of Atherothrombotic Diseases
Wang, X., & Peter, K. (2017) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.116.306483 · Cited by 67 · see citing works
Imaging Biomarkers in Atherosclerosis Trials
Tardif, J., Lesage, F., Harel, F., Roméo, P., & Pressacco, J. (2011) · Circulation Cardiovascular Imaging · doi:10.1161/circimaging.110.962001 · Cited by 66 · see citing works
The Effect of Statins through Mast Cells in the Pathophysiology of Atherosclerosis: a Review
Kouhpeikar, H., Delbari, Z., Sathyapalan, T., Simental‐Mendía, L. E., Jamialahmadi, T., & Sahebkar, A. (2020) · Current Atherosclerosis Reports · doi:10.1007/s11883-020-00837-9 · Cited by 66 · see citing works
Matrix-Metalloproteinases as Imaging Targets for Inflammatory Activity in Atherosclerotic Plaques
Schäfers, M. A., Schober, O., & Hermann, S. (2010) · Journal of Nuclear Medicine · doi:10.2967/jnumed.109.065698 · Cited by 61 · see citing works
Ma, B., Xiao, Y., Lv, Q., Li, G., Wang, Y., & Fu, G. (2022) · Advanced Materials · doi:10.1002/adma.202206129 · Cited by 59 · see citing works
Qin, H., Zhao, Y., Zhang, J., Xiao, P., Yang, S., & Xing, D. (2016) · Nanomedicine Nanotechnology Biology and Medicine · doi:10.1016/j.nano.2016.02.016 · Cited by 59 · see citing works
Spronk, H. M. H., Padró, T., Siland, J. E., Prochaska, J. H., Winters, J., van der Wal, A. C., Posthuma, J. J., Lowe, G. D. O., D’Alessandro, E., Wenzel, P., et al. (2018) · Thrombosis and Haemostasis · doi:10.1160/th17-07-0492 · Cited by 61 · see citing works
Coronary CT angiography and high-risk plaque morphology
Motoyama, S., Sarai, M., Narula, J., & Ozaki, Y. (2012) · Cardiovascular Intervention and Therapeutics · doi:10.1007/s12928-012-0140-1 · Cited by 58 · see citing works
Self-citationHaider, N., Hartung, D., Fujimoto, S., Petrov, A. D., Kolodgie, F. D., Virmani, R., Ohshima, S., Liu, H., Zhou, J. F., Fujimoto, A., et al. (2009) · Journal of Nuclear Cardiology · doi:10.1007/s12350-009-9107-8 · Cited by 57 · see citing works
Self-citationMolecular Probes for Imaging Fibrosis and Fibrogenesis
Désogère, P. A., Montesi, S. B., & Caravan, P. D. (2018) · Chemistry - A European Journal · doi:10.1002/chem.201801578 · Cited by 57 · see citing works
Hyafil, F., Vucic, E., Cornily, J., Sharma, R., Amirbekian, V., Blackwell, F., Lancelot, E., Corot, C., Fuster, V., Galis, Z. S., et al. (2010) · European Heart Journal · doi:10.1093/eurheartj/ehq413 · Cited by 55 · see citing works
Cardiovascular Molecular Imaging: The Road Ahead
Majmudar, M. D., & Nahrendorf, M. (2012) · Journal of Nuclear Medicine · doi:10.2967/jnumed.111.099838 · Cited by 51 · see citing works
Razavian, M., Zhang, J., Nie, L., Tavakoli, S., Razavian, N. B., Dobrucki, L. W., Sinusas, A. J., Edwards, D. S., Azure, M. T., & Sadeghi, M. M. (2010) · Journal of Nuclear Medicine · doi:10.2967/jnumed.110.075259 · Cited by 50 · see citing works
Self-citationSmall-animal SPECT and SPECT/CT: application in cardiovascular research
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Self-citationMatrix Metalloproteinase-9 is a Diagnostic Marker of Heterotopic Ossification in a Murine Model
Rodenberg, E. J., Azhdarinia, A., Lazard, Z. W., Hall, M. A., Kwon, S. K., Wilganowski, N. L., Salisbury, E. A., Merched-Sauvage, M., Olmsted‐Davis, E. A., Sevick-Muraca, E. M., et al. (2011) · Tissue Engineering Part A · doi:10.1089/ten.tea.2011.0007 · Cited by 49 · see citing works
Herde, A. M., Krämer, S. D., Meletta, R., Beck, K. R., Selivanova, S. V., Rančić, Z., Kaufmann, P. A., Vos, B., Meding, J., Stellfeld, T., et al. (2014) · Nuclear Medicine and Biology · doi:10.1016/j.nucmedbio.2014.04.085 · Cited by 50 · see citing works
Khanicheh, E., Mitterhuber, M., Xu, L., Häuselmann, S. P., Kuster, G. M., & Kaufmann, B. A. (2013) · PLoS ONE · doi:10.1371/journal.pone.0058761 · Cited by 45 · see citing works
Vulnerable atherosclerotic plaque - a review of current concepts and advanced imaging
Špaček, M., Zemánek, D., Hutyra, M., Sluka, M., & Táborský, M. (2018) · Biomedical Papers · doi:10.5507/bp.2018.004 · Cited by 46 · see citing works
Oláh, M., Koncz, Á., Fehér, J., Kálmánczhey, J., Oláh, C., Balogh, S., Nagy, G., & Bender, T. (2009) · International Journal of Biometeorology · doi:10.1007/s00484-009-0276-6 · Cited by 43 · see citing works
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Kuge, Y., Takai, N., Ogawa, Y., Temma, T., Zhao, Y., Nishigori, K., Ishino, S., Kamihashi, J., Kiyono, Y., Shiomi, M., et al. (2010) · European Journal of Nuclear Medicine and Molecular Imaging · doi:10.1007/s00259-010-1521-2 · Cited by 39 · see citing works
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Molecular imaging of the extracellular matrix in the context of atherosclerosis
Reimann, C., Brangsch, J., Collettini, F., Walter, T., Hamm, B., Botnar, R. M., & Makowski, M. R. (2016) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2016.09.005 · Cited by 35 · see citing works
The vulnerable coronary plaque: update on imaging technologies
Rosa, G. M., Bauckneht, M., Masoero, G., Mach, F., Quercioli, A., Seitun, S., Balbi, M., Brunelli, C., Parodi, A., Nencioni, A., et al. (2013) · Thrombosis and Haemostasis · doi:10.1160/th13-02-0121 · Cited by 34 · see citing works
Moustardas, P., Kadoglou, N. P. E., Katsimpoulas, M., Kapelouzou, A., Kostomitsopoulos, N. G., Karayannacos, P. E., Kostakis, A. I., & Liapis, C. D. (2014) · PLoS ONE · doi:10.1371/journal.pone.0108240 · Cited by 34 · see citing works
Non-FDG imaging of atherosclerosis: Will imaging of MMPs assess plaque vulnerability?
Hermann, S., Staršíchová, A., Waschkau, B., Kuhlmann, M. T., Wenning, C., Schober, O., & Schäfers, M. A. (2012) · Journal of Nuclear Cardiology · doi:10.1007/s12350-012-9553-6 · Cited by 33 · see citing works
Lin, S.-A., Patel, M. R., Suresch, D. L., Connolly, B., Bao, B., Groves, K., Rajopadhye, M., Peterson, J. D., Klimas, M. T., Sur, C., et al. (2012) · International Journal of Molecular Imaging · doi:10.1155/2012/189254 · Cited by 32 · see citing works
Preclinical Evaluation of RYM1, a Matrix Metalloproteinase–Targeted Tracer for Imaging Aneurysm
Toczek, J., Ye, Y., Gona, K. B., Kim, H.-Y., Han, J., Razavian, M., Golestani, R., Zhang, J., WU, T. L., Jung, J., et al. (2017) · Journal of Nuclear Medicine · doi:10.2967/jnumed.116.188656 · Cited by 32 · see citing works
Novel Imaging-Based Biomarkers for Identifying Carotid Plaque Vulnerability
Fernández‐Álvarez, V., Linares-Sánchez, M., Suárez, C., López, F., Guntinas‐Lichius, O., Mäkitie, A. A., Bradley, P. J., & Ferlito, A. (2023) · Biomolecules · doi:10.3390/biom13081236 · Cited by 29 · see citing works
Osborn, E. A., & Jaffer, F. A. (2012) · JACC. Cardiovascular imaging · doi:10.1016/j.jcmg.2011.12.011 · Cited by 29 · see citing works
Progress in atherosclerotic plaque imaging
Soloperto, G. (2012) · World Journal of Radiology · doi:10.4329/wjr.v4.i7.353 · Cited by 28 · see citing works
Molecular imaging of matrix metalloproteinases in atherosclerotic plaques
Lenglet, S., Thomas, A., Chaurand, P., Galan, K., Mach, F., & Montecucco, F. (2012) · Thrombosis and Haemostasis · doi:10.1160/th11-10-0717 · Cited by 28 · see citing works
Molecular Imaging of Vulnerable Coronary Plaque: A Pathophysiologic Perspective
Krishnan, S. K., Otaki, Y., Doris, M. K., Slipczuk, L. N., Arnson, Y., Rubeaux, M., Dey, D., Slomka, P. J., Berman, D. S., & Tamarappoo, B. K. (2017) · Journal of Nuclear Medicine · doi:10.2967/jnumed.116.187906 · Cited by 28 · see citing works
A comprehensive review on controls in molecular imaging: lessons from MMP‐2 imaging
Lebel, R., & Lepage, M. (2014) · Contrast Media & Molecular Imaging · doi:10.1002/cmmi.1555 · Cited by 27 · see citing works
Heidt, T., Deininger, F., Peter, K., Goldschmidt, J., Pethe, A., Hagemeyer, C. E., Neudorfer, I., Zirlik, A., Weber, W., Bode, C., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0018446 · Cited by 27 · see citing works
Tavakoli, S., Razavian, M., Zhang, J., Nie, L., Marfatia, R., Dobrucki, L. W., Sinusas, A. J., Robinson, S. P., Edwards, D. S., & Sadeghi, M. M. (2010) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.110.216036 · Cited by 27 · see citing works
Self-citationGolestani, R., & Sadeghi, M. M. (2013) · Journal of Nuclear Cardiology · doi:10.1007/s12350-013-9845-5 · Cited by 26 · see citing works
Basiak, M., Kosowski, M., Hachuła, M., & Okopień, B. (2022) · Pharmaceuticals · doi:10.3390/ph15070802 · Cited by 26 · see citing works
Gao, S., Xue, X., Yin, J., Gao, L., Zhu, L., Li, L., Gao, S., Wang, S., Liang, R., Xu, Y., et al. (2020) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2020.113158 · Cited by 26 · see citing works
Stendahl, J. C., Kwan, J. M., Pucar, D., & Sadeghi, M. M. (2022) · Journal of Nuclear Medicine · doi:10.2967/jnumed.121.263507 · Cited by 25 · see citing works
Lipid lowering and imaging protease activation in atherosclerosis
Razavian, M., Nie, L., Challa, A. A., Zhang, J., Golestani, R., Jung, J., Robinson, S. P., & Sadeghi, M. M. (2013) · Journal of Nuclear Cardiology · doi:10.1007/s12350-013-9843-7 · Cited by 24 · see citing works
Yu, S. S., Ortega, R. A., Reagan, B. W., McPherson, J., Sung, H., & Giorgio, T. D. (2011) · Wiley Interdisciplinary Reviews Nanomedicine and Nanobiotechnology · doi:10.1002/wnan.158 · Cited by 24 · see citing works
Molecular Imaging of Vulnerable Plaque
Nakahara, T., Narula, J., & Strausś, H. W. (2018) · Seminars in Nuclear Medicine · doi:10.1053/j.semnuclmed.2018.02.004 · Cited by 22 · see citing works
Self-citationImaging Inflammation in Patients and Animals: Focus on PET Imaging the Vulnerable Plaque
Bartlett, B., Ludewick, H. P., Lee, S., Verma, S., Francis, R. J., & Dwivedi, G. (2021) · Cells · doi:10.3390/cells10102573 · Cited by 21 · see citing works
Stacy, M. R., Naito, Y., Maxfield, M. W., Kurobe, H., Tara, S., Chan, C., Rocco, K. A., Shinoka, T., Sinusas, A. J., & Breuer, C. K. (2014) · Journal of Thoracic and Cardiovascular Surgery · doi:10.1016/j.jtcvs.2014.05.037 · Cited by 20 · see citing works
Molecular imaging of atrial myopathy: Towards early AF detection and non-invasive disease management
Ezeani, M., Hagemeyer, C. E., Lal, S., & Niego, B. (2020) · Trends in Cardiovascular Medicine · doi:10.1016/j.tcm.2020.12.002 · Cited by 20 · see citing works
Tekabe, Y., Li, Q., Luma, J., Weisenberger, D., Sedlar, M., Harja, E., Narula, J., & Johnson, L. L. (2010) · Journal of Nuclear Cardiology · doi:10.1007/s12350-010-9276-5 · Cited by 20 · see citing works
Self-citationLin, X., Jo, H., Ishii, T. M., Fujita, M., Fu, M. L. X., Tambara, K., Yamamoto, M., Tabata, Y., Komeda, M., & Matsuoka, S. (2009) · Circulation Journal · doi:10.1253/circj.cj-09-0379 · Cited by 20 · see citing works
Bourantas, C. V., García‐García, H. M., Diletti, R., Muramatsu, T., & Serruys, P. W. J. C. (2013) · American Heart Journal · doi:10.1016/j.ahj.2013.02.015 · Cited by 19 · see citing works
Recent advances and future trends in multimodality cardiac imaging
Beller, G. (2010) · Heart Lung and Circulation · doi:10.1016/j.hlc.2009.11.003 · Cited by 18 · see citing works
Multi-Scale Imaging of Vascular Pathologies in Cardiovascular Disease
Tiwari, A., Elgrably, B., Saar, G., & Vandoorne, K. (2022) · Frontiers in Medicine · doi:10.3389/fmed.2021.754369 · Cited by 17 · see citing works
Degnan, A. J., Young, V. E. L., & Gillard, J. H. (2011) · Expert Review of Cardiovascular Therapy · doi:10.1586/erc.11.168 · Cited by 17 · see citing works
Molecular imaging of atherosclerosis in translational medicine
Filardi, P. P., Dellegrottaglie, S., Rudd, J. H. F., Costanzo, P., Marciano, C., Vassallo, E., Marsico, F., Ruggiero, D., Petretta, M. P., Massimo Chiariello, A., et al. (2010) · European Journal of Nuclear Medicine and Molecular Imaging · doi:10.1007/s00259-010-1697-5 · Cited by 16 · see citing works
Kiugel, M., Hellberg, S., Käkelä, M., Liljenbäck, H., Saanijoki, T., Li, X., Tuomela, J. M., Knuuti, J. M., Saraste, A., & Roivainen, A. (2018) · Molecules · doi:10.3390/molecules23123168 · Cited by 16 · see citing works
Nuclear Molecular Imaging for Vulnerable Atherosclerotic Plaques
Lee, S. J., & Paeng, J. C. (2015) · Korean Journal of Radiology · doi:10.3348/kjr.2015.16.5.955 · Cited by 15 · see citing works
Grodin, J. L., Powell‐Wiley, T. M., Ayers, C. R., Kumar, D. S., Rohatgi, A. K., Khera, A., McGuire, D. K., de Lemos, J. A., & Das, S. R. (2011) · Vascular Medicine · doi:10.1177/1358863x11422110 · Cited by 14 · see citing works
Tan, H., Zhou, J., Yang, X., Abudupataer, M., Li, X., Hu, Y., Xiao, J., Shi, H., & Cheng, D. (2017) · Scientific Reports · doi:10.1038/s41598-017-03276-w · Cited by 14 · see citing works
Self-citationNovel Arginine-containing Macrocyclic MMP Inhibitors: Synthesis, 99mTc-labeling, and Evaluation
Ye, Y., Toczek, J., Gona, K. B., Kim, H.-Y., Han, J., Razavian, M., Golestani, R., Zhang, J., WU, T. L., Ghosh, M., et al. (2018) · Scientific Reports · doi:10.1038/s41598-018-29941-2 · Cited by 13 · see citing works
Osborn, E. A., & Jaffer, F. A. (2010) · JACC. Cardiovascular imaging · doi:10.1016/j.jcmg.2010.09.009 · Cited by 13 · see citing works
Okubo, R., Nakanishi, R., Toda, M., Saito, D., Watanabe, I., Yabe, T., Amano, H., Hirai, T., & Ikeda, T. (2017) · Heart and Vessels · doi:10.1007/s00380-017-0943-1 · Cited by 12 · see citing works
Sanz, J., Moreno, P., & Fuster, V. (2010) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2009.12.027 · Cited by 12 · see citing works
Toczek, J., Gona, K., Liu, Y., Ahmad, A., Ghim, M., Ojha, D., Kukreja, G., Salarian, M., Luehmann, H., Heo, G. S., et al. (2023) · Circulation: Cardiovascular Imaging · doi:10.1161/circimaging.122.014615 · Cited by 12 · see citing works
Imaging the Extracellular Matrix in Prevalent Cardiovascular Diseases
Chaher, N., Hajhosseiny, R., Phinikaridou, A., & Botnar, R. M. (2020) · Applied Sciences · doi:10.3390/app10114001 · Cited by 12 · see citing works
Buchler, A., Munch, M., Farber, G., Zhao, X., Haddad, R., Farber, E., & Rotstein, B. H. (2021) · Molecular Imaging and Biology · doi:10.1007/s11307-021-01626-9 · Cited by 12 · see citing works
Fan, D., Zheng, C., Wu, W., Chen, Y., Chen, D., Hu, X., Shen, C., Chen, M., Li, R., & Chen, Y. (2022) · Brain and Behavior · doi:10.1002/brb3.2473 · Cited by 11 · see citing works
Functional and molecular imaging techniques in aortic aneurysm disease
Hope, M. D., & Hope, T. A. (2013) · Current Opinion in Cardiology · doi:10.1097/hco.0b013e3283644beb · Cited by 11 · see citing works
Nakahara, T., Strausś, H. W., Narula, J., & Jinzaki, M. (2022) · Seminars in Nuclear Medicine · doi:10.1053/j.semnuclmed.2022.08.009 · Cited by 10 · see citing works
Self-citationNuevas herramientas en la estratificación del riesgo cardiovascular
Badimón, J. J., Santos‐Gallego, C. G., Torres, F., Castillo, J., & Kaski, J. C. (2011) · Revista Española de Cardiología Suplementos · doi:10.1016/s1131-3587(11)70011-5 · Cited by 10 · see citing works
Kosowski, M., Basiak, M., Hachuła, M., & Okopień, B. (2022) · Medicina · doi:10.3390/medicina58070969 · Cited by 9 · see citing works
Molecular targets in aortic aneurysm for establishing novel management paradigms
Hu, C., Zhu, K., Li, J., Wang, C., & Lai, L. (2017) · Journal of Thoracic Disease · doi:10.21037/jtd.2017.10.63 · Cited by 8 · see citing works
High-Resolution Small Animal Imaging
Schäfers, K. P., Bolwin, K., Büther, F., Hermann, S., Jacobs, A. H., Kösters, T., Kuhlmann, M. T., Schäfers, M. A., & Viel, T. (2014) · Elsevier eBooks · doi:10.1016/b978-0-444-53632-7.00110-6 · Cited by 8 · see citing works
Molecular imaging of cardiovascular disease: Current status and future perspective
Nakahara, T., Fujimoto, S., & Jinzaki, M. (2025) · Journal of Cardiology · doi:10.1016/j.jjcc.2025.01.017 · Cited by 7 · see citing works
Self-citationEmerging Nuclear Medicine Imaging of Atherosclerotic Plaque Formation
Кондаков, А. К., Berdalin, A. B., Beregov, M. M., & Lelyuk, V. G. (2022) · Journal of Imaging · doi:10.3390/jimaging8100261 · Cited by 6 · see citing works
Improved Risk Assessment for Abdominal Aortic Aneurysm Rupture
Hope, T. A., & Hope, M. D. (2011) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2011.09.016 · Cited by 5 · see citing works
Who gets the heart attack: noninvasive imaging markers of plaque instability
Narula, J. (2009) · Journal of Nuclear Cardiology · doi:10.1007/s12350-009-9141-6 · Cited by 5 · see citing works
Self-citationPu, Z., Wang, Y., Zhang, Y., Huang, J., Hong, Y., He, H., Liu, C., Chen, S., Grayburn, P. A., & Huang, P. (2015) · Scientific Reports · doi:10.1038/srep08956 · Cited by 4 · see citing works
Kapelouzou, A., Katsimpoulas, M., Kontogiannis, C., Lidoriki, I., Georgiopoulos, G. A., Kourek, C., Papageorgiou, C., Mylonas, K. S., Dritsas, S., Charalabopoulos, A., et al. (2021) · Current Issues in Molecular Biology · doi:10.3390/cimb43020059 · Cited by 4 · see citing works
Tu, Z., Wei, Y., Liao, Y., Wan, Z., Zhou, Z., & Guo, J. (2026) · Frontiers in Immunology · doi:10.3389/fimmu.2026.1816199 · Cited by 2 · see citing works
Wang, Z., Deng, G., Zhang, Z., Huang, H., & Zhao, Y. (2017) · Nuclear Medicine Communications · doi:10.1097/mnm.0000000000000651 · Cited by 2 · see citing works
Špaček, M., Vacha, J., Přeček, J., Hutyra, M., Nykl, R., Sluka, M., & Táborský, M. (2022) · Biomedical Papers · doi:10.5507/bp.2022.024 · Cited by 2 · see citing works
- Authors
- Fujimoto, S., Hartung, D., Ohshima, S., Edwards, D. S., Zhou, J., Yalamanchili, P., Azure, M., Fujimoto, A., Isobe, S., Matsumoto, Y., Boersma, H., Wong, N., Yamazaki, J., Narula, N., Petrov, A., & Narula, J.
- Affiliations
- University of California, Irvine (US)
- Bristol-Myers Squibb (United States) (US)
- Toho University (JP)
- Corresponding author
- Petrov, Artiom
- Venue
- Journal of the American College of Cardiology
- Publisher
- Elsevier BV
- Published
- 2008-12
- Volume
- 52
- Issue
- 23
- Pages
- 1847-1857
- ISSN
- 0735-1097 (ISSN-L)
- OpenAlex
- W2141910805
- Cited by
- 133
- References
- 42
- Citations by year
- 2026: 2 · 2025: 3 · 2024: 1 · 2023: 2 · 2022: 10 · 2021: 4 · 2020: 6 · 2019: 2 · 2018: 6 · 2017: 10 · 2016: 2 · 2015: 6 · 2014: 16 · 2013: 8 · 2012: 11
- FWCI
- 5.00
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Journal of the American College of Cardiology (publishedVersion)
- PubMed (publishedVersion)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion, other-oa)
- Funders
- National Heart, Lung, and Blood Institute (R01HL078681)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Protease and Inhibitor Mechanisms
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Cardiac Imaging and Diagnostics
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Cerebrovascular and Carotid Artery Diseases
- Keywords
- matrix metalloproteinases, atherosclerosis, MMP-2, MMP-9, plaque vulnerability, macrophage infiltration, fluvastatin, statin therapy, high-cholesterol diet, rabbit model, atherosclerotic plaque imaging, radiotracer clearance
- MeSH terms
- Animals, Aorta, Abdominal, Combined Modality Therapy, Immunohistochemistry, Macrophages, Male, Models, Chemical, Rabbits, Technetium, Tomography, Emission-Computed, Single-Photon, Hydroxymethylglutaryl-CoA Reductase Inhibitors, Matrix Metalloproteinase 2, Matrix Metalloproteinase 9, Atherosclerosis, Matrix Metalloproteinase Inhibitors
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