Detection of vulnerable atherosclerosis plaques with a dual-modal single-photon-emission computed tomography/magnetic resonance imaging probe targeting apoptotic macrophages

ACS Applied Materials and Interfaces

Volumn 7, Issue 4, 2015, Pages 2847-2855

  Cheng, Dengfeng ^a,b   Li, Xiao ^a,b   Zhang, Chunfu ^c   Tan, Hui ^a,b   Wang, Cong ^a   Pang, Lifang ^a,b   Shi, Hongcheng ^a,b  

^a FUDAN UNIVERSITY   (China)

^b SHANGHAI INSTITUTE OF MEDICAL IMAGING   (China)

^c SHANGHAI JIAO TONG UNIVERSITY   (China)

Author keywords

Annexin V; apoptotic macrophage; atherosclerosis; hybrid nanoparticle system; SPECT MRI; vulnerable plaque

Indexed keywords

ANTIBIOTICS; DISEASES; IRON OXIDES; MACROPHAGES; MAGNETIC RESONANCE IMAGING; NANOPARTICLES; PARTICLE BEAMS; PHOTONS; POLYETHYLENE GLYCOLS; PROBES;

ANNEXINS; APOPTOTIC; ATHEROSCLEROSIS; HYBRID NANOPARTICLE; SPECT/MRI; VULNERABLE PLAQUES;

SINGLE PHOTON EMISSION COMPUTED TOMOGRAPHY;

DEXTRAN; FERUMOXTRAN-10; LIPOCORTIN 5; MAGNETITE NANOPARTICLE;

ANIMAL; APOPTOSIS; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; C57BL MOUSE; CHEMISTRY; COMPUTER ASSISTED EMISSION TOMOGRAPHY; CYTOLOGY; DEVICES; HUMAN; KNOCKOUT MOUSE; MACROPHAGE; METABOLISM; MOUSE; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOLOGY; PATHOPHYSIOLOGY; PROCEDURES; RADIOGRAPHY;

ANIMALS; ANNEXIN A5; APOPTOSIS; ATHEROSCLEROSIS; DEXTRANS; HUMANS; MACROPHAGES; MAGNETIC RESONANCE IMAGING; MAGNETITE NANOPARTICLES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PLAQUE, ATHEROSCLEROTIC; TOMOGRAPHY, EMISSION-COMPUTED;

EID: 84922461830     PISSN: 19448244     EISSN: 19448252     Source Type: Journal    
DOI: 10.1021/am508118x     Document Type: Article

References (42)

1. Lee, W. W.; Marinelli, B.; van der Laan, A. M.; Sena, B. F.; Gorbatov, R.; Leuschner, F.; Dutta, P.; Iwamoto, Y.; Ueno, T.; Begieneman, M. P. V; Niessen, H. W. M.; Piek, J. J.; Vinegoni, C.; Pittet, M. J.; Swirski, F. K.; Tawakol, A.; Di Carli, M.; Weissleder, R.; Nahrendorf, M. PET/MRI of Inflammation in Myocardial Infarction J. Am. Coll. Cardiol. 2012, 59, 153-163
2. Xing, H.; Bu, W.; Zhang, S.; Zheng, X.; Li, M.; Chen, F.; He, Q.; Zhou, L.; Peng, W.; Hua, Y.; Shi, J. Multifunctional Nanoprobes for Upconversion Fluorescence, MR and CT Trimodal Imaging Biomaterials 2012, 33, 1079-1089
3. Ni, D.; Zhang, J.; Bu, W.; Xing, H.; Han, F.; Xiao, Q.; Yao, Z.; Chen, F.; He, Q.; Liu, J.; Zhang, S.; Fan, W.; Zhou, L.; Peng, W.; Shi, J. Dual-targeting Upconversion Nanoprobes across the Blood-brain Barrier for Magnetic Resonance/Fluorescence Imaging of Intracranial Glioblastoma ACS Nano 2014, 8, 1231-1242
4. 4 Nanodots for Efficient MR Angiography and Atherosclerotic Plaque Imaging Adv. Mater. 2014, 26, 3867-3872
5. 99mTc-labeled Anti-LOX-1 Antibody: Potential Agent for Imaging of Vulnerable Plaque J. Nucl. Med. 2008, 49, 1677-1685
6. Li, D.; Patel, A. R.; Klibanov, A. L.; Kramer, C. M.; Ruiz, M.; Kang, B.-Y.; Mehta, J. L.; Beller, G. a; Glover, D. K.; Meyer, C. H. Molecular Imaging of Atherosclerotic Plaques Targeted to Oxidized LDL Receptor LOX-1 by SPECT/CT and Magnetic Resonance Circ. Cardiovasc. Imaging 2010, 3, 464-472
7. Rudd, J. H. F.; Hyafil, F.; Fayad, Z. A. Inflammation Imaging in Atherosclerosis Arterioscler. Thromb. Vasc. Biol. 2009, 29, 1009-1016
8. 3-antisense Oligonucleotide to PCNA and Effect on Gene Expression in Vascular Smooth Muscle Cells J. Nucl. Med. 2005, 46, 1052-1058
9. Kolodgie, F. D.; Petrov, A.; Virmani, R.; Narula, N.; Verjans, J. W.; Weber, D. K.; Hartung, D.; Steinmetz, N.; Vanderheyden, J. L.; Vannan, M. A.; Gold, H. K.; Reutelingsperger, C. P. M.; Hofstra, L.; Narula, J. Targeting of Apoptotic Macrophages and Experimental Atheroma with Radiolabeled Annexin V: a Technique with Potential for Noninvasive Imaging of Vulnerable Plaque Circulation 2003, 108, 3134-3139
10. Britz-Cunningham, S. H.; Adelstein, S. J. Molecular Targeting with Radionuclides: State of the Science J. Nucl. Med. 2003, 44, 1945-1961
11. 99mTc-HYNIC-Annexin V, a Novel Human Recombinant Annexin V for Human Application J. Nucl. Med. 2003, 44, 947-952
12. -/- mice Eur. J. Nucl. Med. Mol. Imaging 2007, 34, 1747-1755
13. Boersma, H. H.; Kietselaer, B. L. J. H.; Stolk, L. M. L.; Bennaghmouch, A.; Hofstra, L.; Narula, J.; Heidendal, G. a. K.; Reutelingsperger, C. P. M. Past, Present, and Future of Annexin A5: from Protein Discovery to Clinical Applications J. Nucl. Med. 2005, 46, 2035-2050
14. Ito, A.; Shinkai, M.; Honda, H.; Kobayashi, T. Medical Application of Functionalized Magnetic Nanoparticles J. Biosci. Bioeng. 2005, 100, 1-11
15. Hao, R.; Xing, R.; Xu, Z.; Hou, Y.; Gao, S.; Sun, S. Synthesis, Functionalization, and Biomedical Applications of Multifunctional Magnetic Nanoparticles Adv. Mater. 2010, 22, 2729-2742
16. He, W.; Cheng, L.; Zhang, L.; Liu, Z.; Cheng, Z.; Zhu, X. Facile Fabrication of Biocompatible and Tunable Multifunctional Nanomaterials via Iron-mediated Atom Transfer Radical Polymerization with Activators Generated by Electron Transfer ACS Appl. Mater. Interfaces 2013, 5, 9663-9669
17. Figge, L.; Appler, F.; Chen, H. H.; Sosnovik, D. E.; Schnorr, J.; Seitz, O.; Taupitz, M.; Hamm, B.; Schellenberger, E. Direct Coupling of Annexin A5 to VSOP Yields Small, Protein-covered Nanoprobes for MR Imaging of Apoptosis Contrast Media Mol. Imaging 2014, 9, 291-299
18. Dash, R.; Chung, J.; Chan, T.; Yamada, M.; Barral, J.; Nishimura, D.; Yang, P. C.; Simpson, P. C. A Molecular MRI Probe to Detect Treatment of Cardiac Apoptosis In Vivo Magn. Reson. Med. 2011, 66, 1152-1162
19. Van Tilborg, G. A. F.; Mulder, W. J. M.; Deckers, N.; Storm, G.; Reutelingsperger, C. P. M.; Strijkers, G. J.; Nicolay, K. Annexin A5-functionalized Bimodal Lipid-based Contrast Agents for the Detection of Apoptosis Bioconjugate Chem. 2006, 17, 741-749
20. Schellenberger, E. A.; Bogdanov, A.; Högemann, D.; Tait, J.; Weissleder, R.; Josephson, L. Annexin V-CLIO: a Nanoparticle for Detecting Apoptosis by MRI Mol. Imaging 2002, 1, 102-107
21. 99mTc-bisphosphonate-iron Oxide Nanoparticle Conjugates for Dual-modality Biomedical Imaging Bioconjugate Chem. 2011, 22, 455-465
22. Chen, T.-J.; Cheng, T.-H.; Hung, Y.-C.; Lin, K.-T.; Liu, G.-C.; Wang, Y.-M. Targeted Folic Acid-PEG Nanoparticles for Noninvasive Imaging of Folate Receptor by MRI J. Biomed. Mater. Res., Part A 2008, 87, 165-175
23. Lee, H.-Y.; Li, Z.; Chen, K.; Hsu, A. R.; Xu, C.; Xie, J.; Sun, S.; Chen, X. PET/MRI Dual-modality Tumor Imaging using Arginine-glycine-aspartic (RGD)-conjugated Radiolabeled Iron Oxide Nanoparticles J. Nucl. Med. 2008, 49, 1371-1379
24. Lijnen, H. R.; Stassen, J. M.; Vanlinthout, I.; Fukao, H.; Okada, K.; Matsuo, O.; Collen, D. Comparative Fibrinolytic Properties of Staphylokinase and Streptokinase in Animal Models of Venous Thrombosis Thromb. Haemostasis 1991, 66, 468-473
25. Hans, C. P.; Zerfaoui, M.; Naura, A. S.; Troxclair, D.; Strong, J. P.; Matrougui, K.; Boulares, A. H. Thieno[2,3- c ]isoquinolin-5-one, a Potent Poly(ADP-ribose) Polymerase Inhibitor, Promotes Atherosclerotic Plaque Regression in High-fat Diet-fed Apolipoprotein E-deficient Mice: Effects on Inflammatory Markers and Lipid Content J. Pharmacol. Exp. Ther. 2009, 329, 150-158
26. 3 Expression Theranostics 2011, 1, 135-148
27. 99mTc Labeled to a Peptide by 4 Methods J. Nucl. Med. 2001, 42, 1870-1877
28. Mattson, G.; Conklin, E.; Desai, S.; Nielander, G.; Savage, M. D.; Morgensen, S. A Practical Approach to Crosslinking Mol. Biol. Rep. 1993, 17, 167-183
29. Brinkley, M. A Brief Survey of Methods for Preparing Protein Conjugates with Dyes, Haptens, and Cross-linking Reagents Bioconjugate Chem. 1992, 3, 2-13
30. Lahorte, C. M. M.; Vanderheyden, J.-L.; Steinmetz, N.; Van de Wiele, C.; Dierckx, R. A.; Slegers, G. Apoptosis-Detecting Radioligands: Current State of the Art and Future Perspectives Eur. J. Nucl. Med. Mol. Imaging 2004, 31, 887-919
31. 3 for Technetium-99m Labeling of DNA Nucl. Med. Biol. 1997, 24, 425-432
32. Abrams, M. J.; Juweid, M.; TenKate, C. I.; Schwartz, D. A.; Hauser, M. M.; Gaul, F. E.; Fuccello, A. J.; Rubin, R. H.; Strauss, H. W.; Fischman, A. J. Technetium-99m-human Polyclonal IgG Radiolabeled via the Hydrazino Nicotinamide Derivative for Imaging Focal Sites of Infection in Rats J. Nucl. Med. 1990, 31, 2022-2028
33. 3-annexin V: Influence of the Chelate on In Vitro and In Vivo Properties in Mice Nucl. Med. Biol. 2006, 33, 135-144
34. 99mTc-annexin V and its Biologic Evaluation for In Vivo Imaging of Apoptosis after Photodynamic Therapy J. Nucl. Med. 2003, 44, 650-656
35. Grierson, J. R.; Yagle, K. J.; Eary, J. F.; Tait, J. F.; Gibson, D. F.; Lewellen, B.; Link, J. M.; Krohn, K. A. Production of [F-18]fluoroannexin for Imaging Apoptosis with PET Bioconjugate Chem. 2004, 15, 373-379
36. Williams, H. Characteristics of Intact and Ruptured Atherosclerotic Plaques in Brachiocephalic Arteries of Apolipoprotein E Knockout Mice Arterioscler. Thromb. Vasc. Biol. 2002, 22, 788-792
37. Coleman, R.; Hayek, T.; Keidar, S.; Aviram, M. A Mouse Model for Human Atherosclerosis: Long-term Histopathological Study of Lesion Development in the Aortic Arch of Apolipoprotein E-deficient (E0) Mice Acta Histochem. 2006, 108, 415-424
38. Schellenberger, E. A.; Sosnovik, D.; Weissleder, R.; Josephson, L. Magneto/Optical Annexin V, a Multimodal Protein Bioconjugate Chem. 2004, 15, 1062-1067
39. Van Tilborg, G. A. F.; Mulder, W. J. M.; Chin, P. T. K.; Storm, G.; Reutelingsperger, C. P.; Nicolay, K.; Strijkers, G. J. Annexin A5-conjugated Quantum Dots with a Paramagnetic Lipidic Coating for the Multimodal Detection of Apoptotic Cells Bioconjugate Chem. 2006, 17, 865-868
40. Van Tilborg, G. A. F.; Vucic, E.; Strijkers, G. J.; Cormode, D. P.; Mani, V.; Skajaa, T.; Reutelingsperger, C. P. M.; Fayad, Z. A.; Mulder, W. J. M.; Nicolay, K. Annexin A5-functionalized Bimodal Nanoparticles for MRI and Fluorescence Imaging of Atherosclerotic Plaques Bioconjugate Chem. 2010, 21, 1794-1803
41. Judenhofer, M. S.; Cherry, S. R. Applications for Preclinical PET/MRI Semin. Nucl. Med. 2013, 43, 19-29
42. Nensa, F.; Schlosser, T. Cardiovascular Hybrid Imaging using PET/MRI RoFo 2014, 186, 1094-1101