Ultrasmall superparamagnetic iron oxide nanoparticles coated with fucoidan for molecular MRI of intraluminal thrombus

Nanomedicine

Volumn 10, Issue 1, 2015, Pages 73-87

  Suzuki, Michimasa ^a   Bachelet Violette, Laure ^a,b   Rouzet, François ^a,c   Beilvert, Anne ^a,b   Autret, Gwennhael ^d   Maire, Murielle ^a,b   Menager, Christine ^d   Louedec, Liliane ^a   Choqueux, Christine ^a   Saboural, Pierre ^a,b   Haddad, Oualid ^a,b   Chauvierre, Cédric ^a,b   Chaubet, Frédéric ^a,b   Michel, Jean Baptiste ^a   Serfaty, Jean Michel ^a,c   Letourneur, Didier ^a,b  

^a INSERM   (France)

^b Site Xavier Bichat and Département Hospitalo Universitaire Fibrosis Inflammation and Remodeling   (France)

^c ASSISTANCE PUBLIQUE HÔPITAUX DE PARIS   (France)

^d CNRS   (France)

Author keywords

aneurysm; iron oxide nanoparticle; MRI; P selectin; thrombus

Indexed keywords

ELASTASE; FUCOIDIN; NANOPARTICLE; PADGEM PROTEIN; TECHNETIUM 99M; ULTRASMALL SUPERPARAMAGNETIC IRON OXIDE; CONTRAST MEDIUM; FERRIC ION; FERRIC OXIDE; MAGNETITE NANOPARTICLE; POLYSACCHARIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTRON MICROSCOPY; HISTOLOGY; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; INTRALUMINAL THROMBUS; MALE; MOLECULAR DIAGNOSTICS; MOLECULAR IMAGING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; RAT; SURFACE PLASMON RESONANCE; THROMBUS; WISTAR RAT; ZETA POTENTIAL; ANIMAL; CHEMISTRY; DIAGNOSTIC USE; HUMAN; MAGNETIC RESONANCE ANGIOGRAPHY; PATHOLOGY; RADIOGRAPHY; THROMBOSIS;

ANIMALS; CONTRAST MEDIA; FERRIC COMPOUNDS; HUMANS; MAGNETIC RESONANCE ANGIOGRAPHY; MAGNETITE NANOPARTICLES; POLYSACCHARIDES; RATS; RATS, WISTAR; THROMBOSIS;

EID: 84921522243     PISSN: 17435889     EISSN: 17486963     Source Type: Journal    
DOI: 10.2217/nnm.14.51     Document Type: Article

References (47)

1. Ramaswamy AK, Hamilton M, Joshi RV et al. Molecular imaging of experimental abdominal aortic aneurysms. Sci. World J. 2013, 973150 (2013).
2. Buxton DB. Molecular imaging of aortic aneurysms. Circ. Cardiovasc. Imaging 5(3), 392-399 (2012).
3. Klink A, Hyafil F, Rudd J et al. Diagnostic and therapeutic strategies for small abdominal aortic aneurysms. Nat. Rev. Cardiol. 8(6), 338-347 (2011).
4. Touat Z, Ollivier V, Dai J et al. Renewal of mural thrombus releases plasma markers and is involved in aortic abdominal aneurysm evolution. Am. J. Pathol. 168(3), 1022-1030 (2006).
5. Fontaine V, Touat Z, Mtairag El M et al. Role of leukocyte elastase in preventing cellular re-colonization of the mural thrombus. Am. J. Pathol. 164(6), 2077-2087 (2004).
6. Delbosc S, Alsac JM, Journe C et al. Porphyromonas gingivalis participates in pathogenesis of human abdominal aortic aneurysm by neutrophil activation. Proof of concept in rats. PLoS ONE 6(4), e18679 (2011).
7. Michel JB, Virmani R, Arbustini E, Pasterkamp G. Intraplaque haemorrhages as the trigger of plaque vulnerability. Eur. Heart J. 32(16), 1977-1985 (2011).
8. Michel JB, Martin-Ventura JL, Egido J et al. Novel aspects of the pathogenesis of aneurysms of the abdominal aorta in humans. Cardiovasc Res. 90(1), 18-27 (2011).
9. Flacke S, Fischer S, Scott MJ et al. Novel MRI contrast agent for molecular imaging of fibrin: implications for detecting vulnerable plaques. Circulation 104(11), 1280-1285 (2001).
10. Klink A, Heynens J, Herranz B et al. In vivo characterization of a new abdominal aortic aneurysm mouse model with conventional and molecular magnetic resonance imaging. J. Am. Coll. Cardiol. 58(24), 2522-2530 (2011).
11. Klink A, Lancelot E, Ballet S et al. Magnetic resonance molecular imaging of thrombosis in an arachidonic acid mouse model using an activated platelet targeted probe. Arterioscler. Thromb. Vasc. Biol. 30(3), 403-410 (2010).
12. Sirol M, Fuster V, Badimon JJ et al. Chronic thrombus detection with in vivo magnetic resonance imaging and a fibrin-targeted contrast agent. Circulation 112(11), 1594-1600 (2005).
13. Spuentrup E, Fausten B, Kinzel S et al. Molecular magnetic resonance imaging of atrial clots in a swine model. Circulation 112(3), 396-399 (2005).
14. Mcateer MA, Schneider JE, Ali ZA et al. Magnetic resonance imaging of endothelial adhesion molecules in mouse atherosclerosis using dual-targeted microparticles of iron oxide. Arterioscler. Thromb. Vasc. Biol. 28(1), 77-83 (2008).
15. Sarda-Mantel L, Coutard M, Rouzet F et al. 99mTc-annexin-V functional imaging of luminal thrombus activity in abdominal aortic aneurysms. Arterioscler. Thromb. Vasc. Biol. 26(9), 2153-2159 (2006).
16. Nchimi A, Defawe O, Brisbois D et al. MR imaging of iron phagocytosis in intraluminal thrombi of abdominal aortic aneurysms in humans. Radiology 254(3), 973-981 (2010).
17. Richards JM, Semple SI, Macgillivray TJ et al. Abdominal aortic aneurysm growth predicted by uptake of ultrasmall superparamagnetic particles of iron oxide: a pilot study. Circ. Cardiovasc. Imaging 4(3), 274-281 (2011).
18. Anidjar S, Salzmann JL, Gentric D, Lagneau P, Camilleri JP, Michel JB. Elastase-induced experimental aneurysms in rats. Circulation 82(3), 973-981 (1990).
19. Coutard M, Touat Z, Houard X, Leclercq A, Michel JB. Thrombus versus wall biological activities in experimental aortic aneurysms. J. Vasc. Res. 47(4), 355-366 (2009).
20. Yokoyama S, Ikeda H, Haramaki N, Yasukawa H, Murohara T, Imaizumi T. Platelet P-selectin plays an important role in arterial thrombogenesis by forming large stable platelet-leukocyte aggregates. J. Am. Coll. Cardiol. 45(8), 1280-1286 (2005).
21. Huo Y, Xia L. P-selectin glycoprotein ligand-1 plays a crucial role in the selective recruitment of leukocytes into the atherosclerotic arterial wall. Trends Cardiovasc. Med. 19(4), 140-145 (2009).
22. Semple JW, Freedman J. Platelets and innate immunity. Cell Mol. Life Sci. 67(4), 499-511 (2010).
23. Haverslag R, Pasterkamp G, Hoefer IE. Targeting adhesion molecules in cardiovascular disorders. Cardiovasc. Hematol. Disord. Drug Targets 8(4), 252-260 (2008).
24. Varki A. Selectin ligands. Proc. Natl Acad. Sci. USA 91(16), 7390-7397 (1994).
25. Kusaykin M, Bakunina I, Sova V et al. Structure, biological activity, and enzymatic transformation of fucoidans from the brown seaweeds. Biotechnol. J. 3(7), 904-915 (2008).
26. Li B, Lu F, Wei X, Zhao R. Fucoidan: structure and bioactivity. Molecules 13(8), 1671-1695 (2008).
27. Bachelet L, Bertholon I, Lavigne D et al. Affinity of low molecular weight fucoidan for P-selectin triggers its binding to activated human platelets. Biochim. Biophys. Acta 1790(2), 141-146 (2009).
28. Rouzet F, Bachelet-Violette L, Alsac JM et al. Radiolabeled fucoidan as a P-selectin targeting agent for in vivo imaging of platelet-rich thrombus and endothelial activation. J. Nucl. Med. 52, 1433-1440 (2011).
29. Riviere C, Boudghene FP, Gazeau F et al. Iron oxide nanoparticle-labeled rat smooth muscle cells: cardiac MR imaging for cell graft monitoring and quantitation. Radiology 235(3), 959-967 (2005).
30. Kondo A, Suzuki J, Kuraya N, Hase S, Kato I, Ikenaka T. Improved method for fluorescence labeling of sugar chains with sialic acid residues. Agric. Biol. Chem. 54(8), 2169-2170 (1990).
31. Hyafil F, Laissy JP, Mazighi M et al. Ferumoxtran-10-enhanced MRI of the hypercholesterolemic rabbit aorta: relationship between signal loss and macrophage infiltration. Arterioscler. Thromb. Vasc. Biol. 26(1), 176-181 (2006).
32. Botnar RM, Buecker A, Wiethoff AJ et al. In vivo magnetic resonance imaging of coronary thrombosis using a fibrin-binding molecular magnetic resonance contrast agent. Circulation 110(11), 1463-1466 (2004).
33. Vandendries ER, Furie BC, Furie B. Role of P-selectin and PSGL-1 in coagulation and thrombosis. Thromb. Haemost. 92(3), 459-466 (2004).
34. Jacobin-Valat MJ, Deramchia K, Mornet S et al. MRI of inducible P-selectin expression in human activated platelets involved in the early stages of atherosclerosis. NMR Biomed. 24(4), 413-424 (2011).
35. Van Kasteren SI, Campbell SJ, Serres S, Anthony DC, Sibson NR, Davis BG. Glyconanoparticles allow pre-symptomatic in vivo imaging of brain disease. Proc. Natl Acad. Sci. USA 106(1), 18-23 (2009).
36. Tang TY, Howarth SP, Miller SR et al. The ATHEROMA (Atorvastatin Therapy: Effects on Reduction of Macrophage Activity) study. Evaluation using ultrasmall superparamagnetic iron oxide-enhanced magnetic resonance imaging in carotid disease. J. Am. Coll. Cardiol. 53(22), 2039-2050 (2009).
37. Chambon C, Clement O, Le Blanche A, Schouman-Claeys E, Frija G. Superparamagnetic iron oxides as positive MR contrast agents: in vitro and in vivo evidence. Magn. Reson. Imaging 11(4), 509-519 (1993).
38. Canet E, Revel D, Forrat R et al. Superparamagnetic iron oxide particles and positive enhancement for myocardial perfusion studies assessed by subsecond T1-weighted MRI. Magn. Reson. Imaging 11(8), 1139-1145 (1993).
39. Ruehm SG, Corot C, Vogt P, Kolb S, Debatin JF. Magnetic resonance imaging of atherosclerotic plaque with ultrasmall superparamagnetic particles of iron oxide in hyperlipidemic rabbits. Circulation 103(3), 415-422 (2001).
40. Chung HJ, Jeun J, Houng SJ, Jun HJ, Kweon DK, Lee SJ. Toxicological evaluation of fucoidan from Undaria pinnatifida in vitro and in vivo. Phytother. Res. 24(7), 1078-1083 (2010).
41. Luyt CE, Meddahi-Pelle A, Ho-Tin-Noe B et al. Low-molecular-weight fucoidan promotes therapeutic revascularization in a rat model of critical hindlimb ischemia. J. Pharmacol. Exp. Ther. 305(1), 24-30 (2003).
42. Deux JF, Meddahi-Pelle A, Le Blanche AF et al. Low molecular weight fucoidan prevents neointimal hyperplasia in rabbit iliac artery in-stent restenosis model. Arterioscler. Thromb. Vasc. Biol. 22(10), 1604-1609 (2002).
43. Thomsen HS. Recent hot topics in contrast media. Eur. Radiol. 21(3), 492-495 (2011).
44. Schlorf T, Meincke M, Kossel E, Gluer CC, Jansen O, Mentlein R. Biological properties of iron oxide nanoparticles for cellular and molecular magnetic resonance imaging. Int. J. Mol. Sci. 12(1), 12-23 (2010).
45. Takaya N, Yuan C, Chu B et al. Presence of intraplaque hemorrhage stimulates progression of carotid atherosclerotic plaques: a high-resolution magnetic resonance imaging study. Circulation 111(21), 2768-2775 (2005).
46. Foster-Gareau P, Heyn C, Alejski A, Rutt BK. Imaging single mammalian cells with a 1.5 T clinical MRI scanner. Magn. Reson. Med. 49(5), 968-971 (2003).
47. Corot C, Robert P, Idee JM, Port M. Recent advances in iron oxide nanocrystal technology for medical imaging. Adv. Drug Deliv. Rev. 58(14), 1471-1504 (2006).