Synthesis of acid-stabilized iron oxide nanoparticles and comparison for targeting atherosclerotic plaques: Evaluation by MRI, quantitative MPS, and TEM alternative to ambiguous Prussian blue iron staining

Nanomedicine: Nanotechnology, Biology, and Medicine

Volumn 11, Issue 5, 2015, Pages 1085-1095

  Scharlach, Constantin ^a   Kratz, Harald ^a   Wiekhorst, Frank ^b   Warmuth, Carsten ^a   Schnorr, Jörg ^a   Genter, Gesche ^a   Ebert, Monika ^a   Mueller, Susanne ^a   Schellenberger, Eyk ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b PHYSIKALISCH TECHNISCHE BUNDESANSTALT   (Germany)

Author keywords

Atherosclerotic plaques; Ferumoxytol; Iron oxide particles; Magnetic particle spectroscopy; Magnetic resonance imaging

Indexed keywords

ANGIOGRAPHY; ENDOTHELIAL CELLS; IRON METALLOGRAPHY; MAGNETIC NANOPARTICLES; MAGNETIC RESONANCE IMAGING; MAGNETISM; MAMMALS; PARTICLE SPECTROMETERS; SYNTHESIS (CHEMICAL);

ATHEROSCLEROTIC PLAQUE; ELECTROSTATIC STABILIZATION; FERUMOXYTOL; IRON OXIDE NANOPARTICLE; IRON OXIDE PARTICLES; MAGNETIC PARTICLE; MAGNETIC PARTICLE SPECTROSCOPY (MPS); SUPERPARAMAGNETIC NANOPARTICLES;

IRON OXIDES;

CITRIC ACID; ETIDRONIC ACID; FERRIC FERROCYANIDE; IRON; MALIC ACID; SUCCIMER; SUPERPARAMAGNETIC IRON OXIDE NANOPARTICLE; TARTARIC ACID; APOLIPOPROTEIN E; FERRIC ION; FERRIC OXIDE; FERROCYANIDE; MAGNETITE NANOPARTICLE; MALIC ACID DERIVATIVE; TARTARIC ACID DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA; AORTA ROOT; ARTICLE; ARTIFACT; ATHEROSCLEROTIC PLAQUE; CAROTID ARTERY; CONTROLLED STUDY; ENDOTHELIUM CELL; EX VIVO STUDY; IN VIVO STUDY; MACROPHAGE; MAGNETIC FIELD; MAGNETIC PARTICLE SPECTROSCOPY; MOUSE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PH; PHAGOLYSOSOME; SPECTROSCOPY; TRANSMISSION ELECTRON MICROSCOPY; ZETA POTENTIAL; ANIMAL; C57BL MOUSE; CHEMISTRY; COMPARATIVE STUDY; GENETICS; MALE; PATHOLOGY; PLAQUE, ATHEROSCLEROTIC; STAINING;

MUS;

ANIMALS; AORTA; APOLIPOPROTEINS E; CAROTID ARTERIES; CITRIC ACID; ETIDRONIC ACID; FERRIC COMPOUNDS; FERROCYANIDES; MAGNETIC RESONANCE IMAGING; MAGNETITE NANOPARTICLES; MALATES; MALE; MICE; MICE, INBRED C57BL; MICROSCOPY, ELECTRON, TRANSMISSION; PLAQUE, ATHEROSCLEROTIC; SPECTRUM ANALYSIS; STAINING AND LABELING; TARTRATES;

EID: 84931074925     PISSN: 15499634     EISSN: 15499642     Source Type: Journal    
DOI: 10.1016/j.nano.2015.01.002     Document Type: Article

References (38)

1. Wagner M., Wagner S., Schnorr J., Schellenberger E., Kivelitz D., Krug L., et al. Coronary MR angiography using citrate-coated very small superparamagnetic iron oxide particles as blood-pool contrast agent: Initial experience in humans. J Magn Reson Imaging 2011, 34(4):816-823.
2. Warmuth C., Schnorr J., Kaufels N., Wagner S., Pilgrimm H., Hamm B., et al. Whole-heart coronary magnetic resonance angiography: contrast-enhanced high-resolution, time-resolved 3D imaging. Invest Radiol 2007, 42(8):550-557.
3. Schnorr J., Taupitz M., Schellenberger E.A., Warmuth C., Fahlenkamp U.L., Wagner S., et al. Cardiac magnetic resonance angiography using blood-pool contrast agents: comparison of citrate-coated very small superparamagnetic iron oxide particles with gadofosveset trisodium in pigs. Röfo 2012, 184(2):105-112.
4. Wagner S., Schnorr J., Ludwig A., Stangl V., Ebert M., Hamm B., et al. Contrast-enhanced MR imaging of atherosclerosis using citrate-coated superparamagnetic iron oxide nanoparticles: calcifying microvesicles as imaging target for plaque characterization. Int J Nanomedicine 2013, 8:767-779.
5. Tang T.Y., Patterson A.J., Miller S.R., Graves M.J., Howarth S.P., U-King-Im J.M., et al. Temporal dependence of in vivo USPIO-enhanced MRI signal changes in human carotid atheromatous plaques. Neuroradiology 2009, 51(7):457-465.
6. Trivedi R.A., U-King-Im J.M., Graves M.J., Cross J.J., Horsley J., Goddard M.J., et al. In vivo detection of macrophages in human carotid atheroma: temporal dependence of ultrasmall superparamagnetic particles of iron oxide-enhanced MRI. Stroke 2004, 35(7):1631-1635.
7. Kooi M.E., Cappendijk V.C., Cleutjens K.B., Kessels A.G., Kitslaar P.J., Borgers M., et al. Accumulation of ultrasmall superparamagnetic particles of iron oxide in human atherosclerotic plaques can be detected by in vivo magnetic resonance imaging. Circulation 2003, 107(19):2453-2458.
8. Schellenberger E.A., Reynolds F., Weissleder R., Josephson L. Surface-functionalized nanoparticle library yields probes for apoptotic cells. Chembiochem 2004, 5(3):275-279.
9. Snyder S.R., Heinen U. Characterization of magnetic nanoparticles for therapy and diagnostics 2010, Bruker BioSpin, Ettlingen, Germany.
10. Millward J.M., Schnorr J., Taupitz M., Wagner S., Wuerfel J.T., Infante-Duarte C. Iron oxide magnetic nanoparticles highlight early involvement of the choroid plexus in central nervous system inflammation. ASN Neuro 2013, 5(1):e00110.
11. Korosoglou G., Weiss R.G., Kedziorek D.A., Walczak P., Gilson W.D., Schär M., et al. Noninvasive detection of macrophage-rich atherosclerotic plaque in hyperlipidemic rabbits using "positive contrast" magnetic resonance imaging. J Am Coll Cardiol 2008, 52(6):483-491.
12. Sigovan M., Boussel L., Sulaiman A., Sappey-Marinier D., Alsaid H., Desbleds-Mansard C., et al. Rapid-clearance iron nanoparticles for inflammation imaging of atherosclerotic plaque: initial experience in animal model. Radiology 2009, 252(2):401-409.
13. von zur Muhlen C., Fink-Petri A., Salaklang J., Paul D., Neudorfer I., Berti V., et al. Imaging monocytes with iron oxide nanoparticles targeted towards the monocyte integrin MAC-1 (cd11b/CD18) does not result in improved atherosclerotic plaque detection by in vivo MRI. Contrast Media Mol Imaging 2010, 5(5):268-275.
14. Weissleder R., Kelly K., Sun E.Y., Shtatland T., Josephson L. Cell-specific targeting of nanoparticles by multivalent attachment of small molecules. Nat Biotechnol 2005, 23(11):1418-1423.
15. Litovsky S. Superparamagnetic iron oxide-based method for quantifying recruitment of monocytes to mouse atherosclerotic lesions in vivo: enhancement by tissue necrosis factor-alpha, interleukin-1beta, and interferon-gamma. Circulation 2003, 107(11):1545-1549.
16. Morris J.B., Olzinski A.R., Bernard R.E., Aravindhan K., Mirabile R.C., Boyce R., et al. P38 MAPK inhibition reduces aortic ultrasmall superparamagnetic iron oxide uptake in a mouse model of atherosclerosis: MRI assessment. Arterioscler Thromb Vasc Biol 2008, 28(2):265-271.
17. Klug G., Kampf T., Ziener C., Parczyk M., Bauer E., Herold V., et al. Murine atherosclerotic plaque imaging with the USPIO ferumoxtran-10. Front Biosci 2009, 14:2546-2552.
18. -/- mice by USPIO-enhanced magnetic resonance imaging. Invest Radiol 2010, 45(11):702-707.
19. Valois C.R., Braz J.M., Nunes E.S., Vinolo M.A., Lima E.C., Curi R., et al. The effect of DMSA-functionalized magnetic nanoparticles on transendothelial migration of monocytes in the murine lung via a beta2 integrin-dependent pathway. Biomaterials 2010, 31(2):366-374.
20. Mejías R., Gutiérrez L., Salas G., Pérez-Yagüe S., Zotes T.M., Lázaro F.J., et al. Long term biotransformation and toxicity of dimercaptosuccinic acid-coated magnetic nanoparticles support their use in biomedical applications. J Control Release 2013, 171(2):225-233.
21. Kolodgie F.D., Gold H.K., Burke A.P., Fowler D.R., Kruth H.S., Weber D.K., et al. Intraplaque hemorrhage and progression of coronary atheroma. N Engl J Med 2003, 349(24):2316-2325.
22. Michel J.B., Virmani R., Arbustini E., Pasterkamp G. Intraplaque haemorrhages as the trigger of plaque vulnerability. Eur Heart J 2011, 32(16):1977-1985.
23. Yuan X.M., Li W., Baird S.K., Carlsson M., Melefors O. Secretion of ferritin by iron-laden macrophages and influence of lipoproteins. Free Radic Res 2004, 38(10):1133-1142.
24. Lee F.Y., Lee T.S., Pan C.C., Huang A.L., Chau L.Y. Colocalization of iron and ceroid in human atherosclerotic lesions. Atherosclerosis 1998, 138(2):281-288.
25. Lee T.S., Shiao M.S., Pan C.C., Chau L.Y. Iron-deficient diet reduces atherosclerotic lesions in apoe-deficient mice. Circulation 1999, 99(9):1222-1229.
26. Lee H.T., Chiu L.L., Lee T.S., Tsai H.L., Chau L.Y. Dietary iron restriction increases plaque stability in apolipoprotein-e-deficient mice. J Biomed Sci 2003, 10(5):510-517.
27. -/-) double knockout mice. Invest Radiol 2007, 42(5):263-273.
28. Kockx M., De Meyer G.R.Y., Muhring J., Jacob W., Bult H., Herman G. Apoptosis and related proteins in different stages of human atherosclerotic plaques. Circulation 1998, 97(23):2307-2315.
29. Golub E.E. Biomineralization and matrix vesicles in biology and pathology. Semin Immunopathol 2011, 33(5):409-417.
30. Demer L.L., Tintut Y. Inflammatory, metabolic, and genetic mechanisms of vascular calcification. Arterioscler Thromb Vasc Biol 2014, 34(4):715-723.
31. Trivedi R.A., Mallawarachi C., U-King-Im J.M., Graves M.J., Horsley J., Goddard M.J., et al. Identifying inflamed carotid plaques using in vivo USPIO-enhanced MR imaging to label plaque macrophages. Arterioscler Thromb Vasc Biol 2006, 26(7):1601-1606.
32. Corot C., Robert P., Idee J.M., Port M. Recent advances in iron oxide nanocrystal technology for medical imaging. Adv Drug Deliv Rev 2006, 58(14):1471-1504.
33. -/- mice using susceptibility gradient mapping. Circ Cardiovasc Imaging 2011, 4(3):295-303.
34. Briley-Saebo K.C., Mulder W.J., Mani V., Hyafil F., Amirbekian V., Aguinaldo J.G., et al. Magnetic resonance imaging of vulnerable atherosclerotic plaques: current imaging strategies and molecular imaging probes. J Magn Reson Imaging 2007, 26(3):460-479.
35. Morishige K., Kacher D.F., Libby P., Josephson L., Ganz P., Weissleder R., et al. High-resolution magnetic resonance imaging enhanced with superparamagnetic nanoparticles measures macrophage burden in atherosclerosis. Circulation 2010, 122(17):1707-1715.
36. Meir K.S., Leitersdorf E. Atherosclerosis in the apolipoprotein-e-deficient mouse: a decade of progress. Arterioscler Thromb Vasc Biol 2004, 24(6):1006-1014.
37. Pendse A.A., Arbones-Mainar J.M., Johnson L.A., Altenburg M.K., Maeda N. Apolipoprotein E knock-out and knock-in mice: atherosclerosis, metabolic syndrome, and beyond. J Lipid Res 2009, 50:S178-S182. [Suppl.].
38. Harms C., Datwyler A.L., Wiekhorst F., Trahms L., Lindquist R., Schellenberger E., et al. Certain types of iron oxide nanoparticles are not suited to passively target inflammatory cells that infiltrate the brain in response to stroke. J Cereb Blood Flow Metab 2013, 33(5):e1-e9.