Dextran-coated iron oxide nanoparticles: a versatile platform for targeted molecular imaging, molecular diagnostics, and therapy.

Advances in our understanding of the genetic basis of disease susceptibility coupled with prominent successes for molecular targeted therapies have resulted in an emerging strategy of personalized medicine. This approach envisions risk stratification and therapeutic selection based on an individual's genetic makeup and physiologic state (the latter assessed through cellular or molecular phenotypes). Molecularly targeted nanoparticles can play a key role in this vision through noninvasive assessments of molecular processes and specific cell populations in vivo, sensitive molecular diagnostics, and targeted delivery of therapeutics. A superparamagnetic iron oxide nanoparticle with a cross-linked dextran coating, or CLIO, is a powerful and illustrative nanoparticle platform for these applications. These structures and their derivatives support diagnostic imaging by magnetic resonance (MRI), optical, and positron emission tomography (PET) modalities and constitute a versatile platform for conjugation to targeting ligands. A variety of conjugation methods exist to couple the dextran surface to different functional groups; in addition, a robust bioorthogonal [4 + 2] cycloaddition reaction between 1,2,4,5-tetrazene (Tz) and trans-cyclooctene (TCO) can conjugate nanoparticles to targeting ligands or label pretargeted cells. The ready availability of conjugation methods has given rise to the synthesis of libraries of small molecule modified nanoparticles, which can then be screened for nanoparticles with specificity for a specific cell type. Since most nanoparticles display their targeting ligands in a multivalent manner, a detailed understanding of the kinetics and affinity of a nanoparticle's interaction with its target (as determined by surface plasmon resonance) can yield functionally important insights into nanoparticle design. In this Account, we review applications of the CLIO platform in several areas relevant to the mission of personalized medicine. We demonstrate rapid and highly sensitive molecular profiling of cancer markers ex vivo, as part of detailed, individualized molecular phenotyping. The CLIO platform also facilitates targeted magnetic resonance and combined modality imaging (such as MR/PET/fluorescence/CT) to enable multiplexed measurement of molecular phenotypes in vivo for early diagnosis and disease classification. Finally, the targeted delivery of a photodynamic therapy agent as part of a theranostic nanoparticle successfully increased local cell toxicity and minimized systemic side effects.

[1]  G. Dai,et al.  Abstract 593: Molecular MRI of Cardiomyocyte Apoptosis With Simultaneous Delayed Enhancement MRI Distinguishes Apoptotic and Necrotic Myocytes in vivo: Potential for Midmyocardial Salvage in Acute Ischemia , 2009 .

[2]  R. Weissleder,et al.  Tetrazine-based cycloadditions: application to pretargeted live cell imaging. , 2008, Bioconjugate chemistry.

[3]  P. Clemons,et al.  Unbiased discovery of in vivo imaging probes through in vitro profiling of nanoparticle libraries. , 2009, Integrative Biology.

[4]  R. Weissleder,et al.  Imaging inflammation of the pancreatic islets in type 1 diabetes. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[5]  Ralph Weissleder,et al.  Molecular imaging in the clinical arena. , 2005, JAMA.

[6]  R. DePinho,et al.  Targeted Nanoparticles for Imaging Incipient Pancreatic Ductal Adenocarcinoma , 2007, PLoS medicine.

[7]  Ralph Weissleder,et al.  High-Resolution Magnetic Resonance Imaging Enhanced With Superparamagnetic Nanoparticles Measures Macrophage Burden in Atherosclerosis , 2010, Circulation.

[8]  Taeghwan Hyeon,et al.  Synthesis of monodisperse spherical nanocrystals. , 2007, Angewandte Chemie.

[9]  D. Kraitchman,et al.  Noninvasive detection of macrophage-rich atherosclerotic plaque in hyperlipidemic rabbits using "positive contrast" magnetic resonance imaging. , 2008, Journal of the American College of Cardiology.

[10]  Hakho Lee,et al.  Micro-NMR for Rapid Molecular Analysis of Human Tumor Samples , 2011, Science Translational Medicine.

[11]  Ralph Weissleder,et al.  Magnetic nanoparticles for MR imaging: agents, techniques and cardiovascular applications , 2008, Basic Research in Cardiology.

[12]  Jan Grimm,et al.  Drug/dye-loaded, multifunctional iron oxide nanoparticles for combined targeted cancer therapy and dual optical/magnetic resonance imaging. , 2009, Small.

[13]  Hao Zeng,et al.  Monodisperse MFe 2 O 4 ( M ) Fe , Co , Mn ) Nanoparticles , 2022 .

[14]  R. Weissleder,et al.  Bioorthogonal Small‐Molecule Ligands for PARP1 Imaging in Living Cells , 2010, Chembiochem : a European journal of chemical biology.

[15]  C. Kaittanis,et al.  Rapid Nanoparticle-Mediated Monitoring of Bacterial Metabolic Activity and Assessment of Antimicrobial Susceptibility in Blood with Magnetic Relaxation , 2008, PloS one.

[16]  Hakho Lee,et al.  Magnetic nanoparticle biosensors. , 2010, Wiley interdisciplinary reviews. Nanomedicine and nanobiotechnology.

[17]  D. Kraitchman,et al.  Positive contrast MR‐lymphography using inversion recovery with ON‐resonant water suppression (IRON) , 2008, Journal of magnetic resonance imaging : JMRI.

[18]  Ralph Weissleder,et al.  A light-activated theranostic nanoagent for targeted macrophage ablation in inflammatory atherosclerosis. , 2010, Small.

[19]  Ralph Weissleder,et al.  Use of Magnetic Nanoparticles as Nanosensors to Probe for Molecular Interactions , 2004, Chembiochem : a European journal of chemical biology.

[20]  R. Weissleder,et al.  High‐Yielding, Two‐Step 18F Labeling Strategy for 18F‐PARP1 Inhibitors , 2011, ChemMedChem.

[21]  Ralph Weissleder,et al.  Crosslinked iron oxides (CLIO): a new platform for the development of targeted MR contrast agents. , 2002, Academic radiology.

[22]  S. Majetich,et al.  Magnetic nanoparticles , 2013, Handbook of Magnetism and Magnetic Materials.

[23]  R. Weissleder,et al.  Magnetic Resonance Imaging Monitors Physiological Changes With Antihedgehog Therapy in Pancreatic Adenocarcinoma Xenograft Model , 2008, Pancreas.

[24]  Hakho Lee,et al.  Ultrasensitive detection of bacteria using core-shell nanoparticles and an NMR-filter system. , 2009, Angewandte Chemie.

[25]  R. Weissleder,et al.  Utility of a new bolus-injectable nanoparticle for clinical cancer staging. , 2007, Neoplasia.

[26]  R. Weissleder,et al.  Hybrid PET-optical imaging using targeted probes , 2010, Proceedings of the National Academy of Sciences.

[27]  Hao Zeng,et al.  Monodisperse MFe2O4 (M = Fe, Co, Mn) nanoparticles. , 2004, Journal of the American Chemical Society.

[28]  Ralph Weissleder,et al.  Emerging concepts in molecular MRI. , 2007, Current opinion in biotechnology.

[29]  R. Weissleder Molecular Imaging in Cancer , 2006, Science.

[30]  Forrest M Kievit,et al.  Surface engineering of iron oxide nanoparticles for targeted cancer therapy. , 2011, Accounts of chemical research.

[31]  Vasilis Ntziachristos,et al.  High throughput magnetic resonance imaging for evaluating targeted nanoparticle probes. , 2002, Bioconjugate chemistry.

[32]  Greg M Thurber,et al.  18F labeled nanoparticles for in vivo PET-CT imaging. , 2009, Bioconjugate chemistry.

[33]  R. Weissleder,et al.  Detection of Macrophages in Aortic Aneurysms by Nanoparticle Positron Emission Tomography–Computed Tomography , 2011, Arteriosclerosis, thrombosis, and vascular biology.

[34]  S. Santra,et al.  Identification of molecular-mimicry-based ligands for cholera diagnostics using magnetic relaxation. , 2011, Bioconjugate chemistry.

[35]  Ralph Weissleder,et al.  Long-circulating iron oxides for MR imaging , 1995 .

[36]  Ravindra K. Pandey,et al.  The Role of Porphyrin Chemistry in Tumor Imaging and Photodynamic Therapy , 2011 .

[37]  Donhee Ham,et al.  Chip–NMR biosensor for detection and molecular analysis of cells , 2008, Nature Medicine.

[38]  R. Weissleder,et al.  Bioorthogonal turn-on probes for imaging small molecules inside living cells. , 2010, Angewandte Chemie.

[39]  Jan Grimm,et al.  Novel Nanosensors for Rapid Analysis of Telomerase Activity , 2004, Cancer Research.

[40]  R Weissleder,et al.  High-efficiency intracellular magnetic labeling with novel superparamagnetic-Tat peptide conjugates. , 1999, Bioconjugate chemistry.

[41]  Hakho Lee,et al.  Bioorthogonal chemistry amplifies nanoparticle binding and enhances the sensitivity of cell detection. , 2010, Nature nanotechnology.

[42]  R. Weissleder,et al.  Imaging pancreatic cancer with a peptide-nanoparticle conjugate targeted to normal pancreas. , 2006, Bioconjugate chemistry.

[43]  Ralph Weissleder,et al.  Noninvasive Vascular Cell Adhesion Molecule-1 Imaging Identifies Inflammatory Activation of Cells in Atherosclerosis , 2006, Circulation.

[44]  Hakho Lee,et al.  Rapid detection and profiling of cancer cells in fine-needle aspirates , 2009, Proceedings of the National Academy of Sciences.

[45]  Ralph Weissleder,et al.  Magneto/optical annexin V, a multimodal protein. , 2004, Bioconjugate chemistry.

[46]  Hakho Lee,et al.  Probing intracellular biomarkers and mediators of cell activation using nanosensors and bioorthogonal chemistry. , 2011, ACS nano.

[47]  R. Weissleder,et al.  Integrated nanosensors to determine levels and functional activity of human telomerase. , 2008, Neoplasia.

[48]  R. Weissleder,et al.  Synthesis and in vivo imaging of a 18F-labeled PARP1 inhibitor using a chemically orthogonal scavenger-assisted high-performance method. , 2011, Angewandte Chemie.

[49]  Hakho Lee,et al.  Carboxymethylated Polyvinyl Alcohol Stabilizes Doped Ferrofluids for Biological Applications , 2010, Advanced materials.

[50]  R. Weissleder,et al.  MRI with Magnetic Nanoparticles Monitors Downstream Anti-Angiogenic Effects of mTOR Inhibition , 2011, Molecular Imaging and Biology.

[51]  R. Weissleder,et al.  Development of a bioorthogonal and highly efficient conjugation method for quantum dots using tetrazine-norbornene cycloaddition. , 2010, Journal of the American Chemical Society.

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

[53]  Ralph Weissleder,et al.  Magnetic resonance imaging of cardiomyocyte apoptosis with a novel magneto‐optical nanoparticle , 2005, Magnetic resonance in medicine.

[54]  Ralph Weissleder,et al.  Noninvasive detection of clinically occult lymph-node metastases in prostate cancer. , 2003, The New England journal of medicine.

[55]  Joseph M. Fox,et al.  Tetrazine ligation: fast bioconjugation based on inverse-electron-demand Diels-Alder reactivity. , 2008, Journal of the American Chemical Society.

[56]  R. Weissleder,et al.  Cellular Imaging of Inflammation in Atherosclerosis Using Magnetofluorescent Nanomaterials , 2006, Molecular imaging.

[57]  Su Seong Lee,et al.  Synthesis of highly crystalline and monodisperse maghemite nanocrystallites without a size-selection process. , 2001, Journal of the American Chemical Society.

[58]  J. Spikes Chlorins as photosensitizers in biology and medicine. , 1990 .

[59]  R Weissleder,et al.  Superparamagnetic iron oxide: pharmacokinetics and toxicity. , 1989, AJR. American journal of roentgenology.

[60]  Michael M. Schmidt,et al.  Factors determining antibody distribution in tumors. , 2008, Trends in pharmacological sciences.

[61]  Ralph Weissleder,et al.  Binding affinity and kinetic analysis of targeted small molecule-modified nanoparticles. , 2010, Bioconjugate chemistry.

[62]  R. Weissleder,et al.  Noninvasive imaging of pancreatic inflammation and its reversal in type 1 diabetes. , 2005, The Journal of clinical investigation.

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

[64]  Ralph Weissleder,et al.  Behavior of endogenous tumor-associated macrophages assessed in vivo using a functionalized nanoparticle. , 2009, Neoplasia.

[65]  R Weissleder,et al.  Monocrystalline iron oxide nanocompounds (MION): Physicochemical properties , 1993, Magnetic resonance in medicine.

[66]  G. Dai,et al.  Molecular MRI Detects Low Levels of Cardiomyocyte Apoptosis in a Transgenic Model of Chronic Heart Failure , 2009, Circulation. Cardiovascular imaging.

[67]  Ralph Weissleder,et al.  A macrophage-targeted theranostic nanoparticle for biomedical applications. , 2006, Small.

[68]  S. Santra,et al.  Role of nanoparticle valency in the nondestructive magnetic-relaxation-mediated detection and magnetic isolation of cells in complex media. , 2009, Journal of the American Chemical Society.

[69]  Ralph Weissleder,et al.  Fast and sensitive pretargeted labeling of cancer cells through a tetrazine/trans-cyclooctene cycloaddition. , 2009, Angewandte Chemie.

[70]  Charalambos Kaittanis,et al.  One-step, nanoparticle-mediated bacterial detection with magnetic relaxation. , 2007, Nano letters.

[71]  R. Weissleder,et al.  Cell-specific targeting of nanoparticles by multivalent attachment of small molecules , 2005, Nature Biotechnology.

[72]  Anna Moore,et al.  In vivo magnetic resonance imaging of transgene expression , 2000, Nature Medicine.

[73]  Taeghwan Hyeon,et al.  Ultra-large-scale syntheses of monodisperse nanocrystals , 2004, Nature materials.

[74]  George M Whitesides,et al.  Polyvalent Interactions in Biological Systems: Implications for Design and Use of Multivalent Ligands and Inhibitors. , 1998, Angewandte Chemie.