Strong and specific interaction of ultra small superparamagnetic iron oxide nanoparticles and human activated platelets mediated by fucoidan coating

Activated platelets play a pivotal role in cardiovascular diseases such as atherothrombosis. Therefore, strategies enabling activated platelet molecular imaging are of great interest. Herein, a chemical protocol was investigated for coating superparamagnetic iron oxide nanoparticles with low molecular weight fucoidan, a ligand of P-selectin expressed on the surface of activated platelets. The physico–chemical characterization of the obtained product demonstrated successful fucoidan coating and its potential as a T2 MRI contrast agent. The specificity and the strength of the interaction between fucoidan-coated iron oxide nanoparticles and human activated platelets was demonstrated by flow cytometry. Micromagnetophoresis experiments revealed that platelets experience magnetically-induced motion in the presence of a magnetic field gradient created by a micromagnet. Altogether, these results indicate that superparamagnetic iron oxide nanoparticles coated with low molecular weight fucoidan may represent a promising molecular imaging tool for activated platelets in human diseases.

[1]  L. Meng,et al.  Superparamagnetic submicro-megranates: Fe(3)O(4) nanoparticles coated with highly cross-linked organic/inorganic hybrids. , 2009, Chemical communications.

[2]  Aniruddh Solanki,et al.  Nanotechnology for regenerative medicine: nanomaterials for stem cell imaging. , 2008, Nanomedicine.

[3]  S. Corr,et al.  Magnetic-fluorescent nanocomposites for biomedical multitasking. , 2006, Chemical communications.

[4]  A. Varki,et al.  Selectin inhibition: synthesis and evaluation of novel sialylated, sulfated and fucosylated oligosaccharides, including the major capping group of GlyCAM-1. , 1997, Glycobiology.

[5]  J. Alsac,et al.  Radiolabeled Fucoidan as a P-Selectin Targeting Agent for In Vivo Imaging of Platelet-Rich Thrombus and Endothelial Activation , 2011, The Journal of Nuclear Medicine.

[6]  R. Molday,et al.  Immunospecific ferromagnetic iron-dextran reagents for the labeling and magnetic separation of cells. , 1982, Journal of immunological methods.

[7]  Didier Letourneur,et al.  Low Molecular Weight Fucoidan Increases VEGF165-induced Endothelial Cell Migration by Enhancing VEGF165 Binding to VEGFR-2 and NRP1* , 2006, Journal of Biological Chemistry.

[8]  Miqin Zhang,et al.  Design and fabrication of magnetic nanoparticles for targeted drug delivery and imaging. , 2010, Advanced drug delivery reviews.

[9]  Oliver T. Bruns,et al.  A highly effective, nontoxic T1 MR contrast agent based on ultrasmall PEGylated iron oxide nanoparticles. , 2009, Nano letters.

[10]  A. Masotti,et al.  Synthesis and characterization of polyethylenimine-based iron oxide composites as novel contrast agents for MRI , 2009, Magnetic Resonance Materials in Physics, Biology and Medicine.

[11]  Bing Xu,et al.  Biofunctional magnetic nanoparticles for protein separation and pathogen detection. , 2006, Chemical communications.

[12]  V. Kuban,et al.  Nitroprusside and methylene blue methods for silicone membrane differentiated flow injection determination of sulfide in water and wastewater. , 1992, Analytical chemistry.

[13]  Ralph Weissleder,et al.  Magnetic relaxation switches capable of sensing molecular interactions , 2002, Nature Biotechnology.

[14]  Alex M. Fichtenholtz,et al.  Methotrexate-immobilized poly(ethylene glycol) magnetic nanoparticles for MR imaging and drug delivery. , 2006, Small.

[15]  R P McEver,et al.  Adhesive Interactions of Leukocytes, Platelets, and the Vessel Wall during Hemostasis and Inflammation , 2001, Thrombosis and Haemostasis.

[16]  M. Olschewski,et al.  Magnetic Resonance Imaging Contrast Agent Targeted Toward Activated Platelets Allows In Vivo Detection of Thrombosis and Monitoring of Thrombolysis , 2008, Circulation.

[17]  Roy W. Chantrell,et al.  Measurements of particle size distribution parameters in ferrofluids , 1978 .

[18]  X. Ledoux,et al.  Deuteron stripping on beryllium target in the 100–2300 MeV energy range , 1999 .

[19]  Z. Dische,et al.  A specific color reaction of methylpentoses and a spectrophotometric micromethod for their determination. , 1948, The Journal of biological chemistry.

[20]  L. Gustafsson.  Determination of ultramicro amounts of sulphate as methylene blue—I: The colour reaction , 1960 .

[21]  J. Michel,et al.  Low-Molecular-Weight Fucoidan Promotes Therapeutic Revascularization in a Rat Model of Critical Hindlimb Ischemia , 2003, Journal of Pharmacology and Experimental Therapeutics.

[22]  A. Nurden,et al.  Cross-linking of alpha and gamma-thrombin to distinct binding sites on human platelets. , 1988, European journal of biochemistry.

[23]  A. Kondo,et al.  Improved method for fluorescence labeling of sugar chains with sialic acid residues. , 1990, Agricultural and biological chemistry.

[24]  Florence Gazeau,et al.  Magnetophoresis and ferromagnetic resonance of magnetically labeled cells , 2002, European Biophysics Journal.

[25]  Hea-Yeon Lee,et al.  Facile and rapid direct gold surface immobilization with controlled orientation for carbohydrates. , 2007, Bioconjugate chemistry.

[26]  Yuanyuan Cai,et al.  Pullulan acetate coated magnetite nanoparticles for hyper-thermia: Preparation, characterization and in vitro experiments , 2010 .

[27]  J. Bacri,et al.  Intracellular uptake of anionic superparamagnetic nanoparticles as a function of their surface coating. , 2003, Biomaterials.

[28]  A. Varki,et al.  Selectin ligands. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[29]  R. Weissleder,et al.  In vivo imaging of activated endothelium using an anti-VCAM-1 magnetooptical probe. , 2005, Bioconjugate chemistry.

[30]  R. Massart,et al.  Preparation of aqueous magnetic liquids in alkaline and acidic media , 1981 .

[31]  S. Neubauer,et al.  Magnetic Resonance Imaging of Endothelial Adhesion Molecules in Mouse Atherosclerosis Using Dual-Targeted Microparticles of Iron Oxide , 2007, Arteriosclerosis, thrombosis, and vascular biology.

[32]  Jin Y. Xie,et al.  Human serum albumin coated iron oxide nanoparticles for efficient cell labeling. , 2010, Chemical communications.

[33]  Philippe Robert,et al.  Recent advances in iron oxide nanocrystal technology for medical imaging. , 2006, Advanced drug delivery reviews.

[34]  Ivo Safarik,et al.  Magnetic techniques for the isolation and purification of proteins and peptides , 2004, Biomagnetic research and technology.

[35]  C. Robic,et al.  Magnetic iron oxide nanoparticles: synthesis, stabilization, vectorization, physicochemical characterizations, and biological applications. , 2008, Chemical reviews.

[36]  Amanda K. Andriola Silva,et al.  Magnetophoresis at the nanoscale: tracking the magnetic targeting efficiency of nanovectors. , 2012, Nanomedicine.

[37]  Forrest M Kievit,et al.  PEI–PEG–Chitosan‐Copolymer‐Coated Iron Oxide Nanoparticles for Safe Gene Delivery: Synthesis, Complexation, and Transfection , 2009, Advanced functional materials.

[38]  A. V. Sergeev,et al.  Evaluation of ferromagnetic fluids and suspensions for the site-specific radiofrequency-induced hyperthermia of MX11 sarcoma cells in vitro , 2001 .

[39]  Ralph Weissleder,et al.  Multifunctional magnetic nanoparticles for targeted imaging and therapy. , 2008, Advanced drug delivery reviews.

[40]  L. Motte,et al.  Bis-phosphonates-ultra small superparamagnetic iron oxide nanoparticles: a platform towards diagnosis and therapy. , 2008, Chemical communications.

[41]  Z. Fayad,et al.  Magnetic Resonance Molecular Imaging of Thrombosis in an Arachidonic Acid Mouse Model Using an Activated Platelet Targeted Probe , 2010, Arteriosclerosis, thrombosis, and vascular biology.

[42]  D. Letourneur,et al.  Biomarkers of atherosclerosis and the potential of MRI for the diagnosis of vulnerable plaque , 2007, Magnetic Resonance Materials in Physics, Biology and Medicine.

[43]  L. Jennings.  Role of platelets in atherothrombosis. , 2009, The American journal of cardiology.

[44]  J. Deux,et al.  Low Molecular Weight Fucoidan Prevents Neointimal Hyperplasia in Rabbit Iliac Artery In-Stent Restenosis Model , 2002, Arteriosclerosis, thrombosis, and vascular biology.

[45]  R. Taillefer,et al.  Imaging characteristics of a novel technetium Tc 99m-labeled platelet glycoprotein IIb/IIIa receptor antagonist in patients With acute deep vein thrombosis or a history of deep vein thrombosis. , 2003, Archives of internal medicine.

[46]  J. Bacri,et al.  Some biomedical applications of ferrofluids , 1999 .

[47]  T. V. van Berkel,et al.  P-selectin as a candidate target in atherosclerosis. , 2003, Biochemical pharmacology.

[48]  M. Roth.  Fluorescence reaction for amino acids. , 1971, Analytical chemistry.

[49]  A. Imberty,et al.  Uncharged P-selectin blockers , 2003, Glycoconjugate Journal.

[50]  L. Juillerat-Jeanneret,et al.  Development of functionalized superparamagnetic iron oxide nanoparticles for interaction with human cancer cells. , 2005, Biomaterials.

[51]  G. Pasterkamp,et al.  Targeting adhesion molecules in cardiovascular disorders. , 2008, Cardiovascular & hematological disorders drug targets.

[52]  F. Chaubet,et al.  Affinity of low molecular weight fucoidan for P-selectin triggers its binding to activated human platelets. , 2009, Biochimica et biophysica acta.

[53]  A. Lu,et al.  Magnetic nanoparticles: synthesis, protection, functionalization, and application. , 2007, Angewandte Chemie.

[54]  Bruno Brochet,et al.  Macrophage Imaging in Central Nervous System and in Carotid Atherosclerotic Plaque Using Ultrasmall Superparamagnetic Iron Oxide in Magnetic Resonance Imaging , 2004, Investigative radiology.

[55]  I. Y. Chen,et al.  Cardiovascular molecular imaging: focus on clinical translation. , 2011, Circulation.