Low-density lipoprotein nanoparticles as magnetic resonance imaging contrast agents.

Low-density lipoproteins (LDLs) are a naturally occurring endogenous nanoplatform in mammalian systems. These nanoparticles (22 nm) specifically transport cholesterol to cells expressing the LDL receptor (LDLR). Several tumors overexpress LDLRs presumably to provide cholesterol to sustain a high rate of membrane synthesis. Amphiphilic gadolinium (Gd)-diethylenetriaminepentaacetic acid chelates have been incorporated into the LDL to produce a novel LDLR-targeted magnetic resonance imaging (MRI) contrast agent. The number of Gd chelates per LDL particle ranged between 150 and 496 Gd(III). In vitro studies demonstrated that Gd-labeled LDL retained a similar diameter and surface charge as the native LDL particle. In addition, Gd-labeled LDL retained selective cellular binding and uptake through LDLR-mediated endocytosis. Finally, Gd-labeled LDLs exhibited significant contrast enhancement 24 hours after administration in nude mice with human hepatoblastoma G2 xenografts. Thus, Gd-labeled LDL demonstrates potential use as a targeted MRI contrast agent for in vivo tumor detection.

[1]  J. Pinotti,et al.  Uptake of a cholesterol-rich emulsion by breast cancer. , 2002, Gynecologic oncology.

[2]  R. Firestone,et al.  Low-density lipoprotein as a vehicle for targeting antitumor compounds to cancer cells. , 1994, Bioconjugate chemistry.

[3]  M. Bednarski,et al.  Tumor Regression by Targeted Gene Delivery to the Neovasculature , 2002, Science.

[4]  M. Knopp,et al.  Estimating kinetic parameters from dynamic contrast‐enhanced t1‐weighted MRI of a diffusable tracer: Standardized quantities and symbols , 1999, Journal of magnetic resonance imaging : JMRI.

[5]  M. Piccinini,et al.  Towards MRI contrast agents of improved efficacy. NMR relaxometric investigations of the binding interaction to HSA of a novel heptadentate macrocyclic triphosphonate Gd(III)-complex , 1997, JBIC Journal of Biological Inorganic Chemistry.

[6]  S. Vitols,et al.  Low-density lipoprotein as a carrier of antitumoral drugs: in vivo fate of drug-human low-density lipoprotein complexes in mice. , 1986, Cancer research.

[7]  M C Phillips,et al.  A 13C NMR characterization of lysine residues in apolipoprotein B and their role in binding to the low density lipoprotein receptor. , 1988, The Journal of biological chemistry.

[8]  S. Gambhir,et al.  Molecular imaging in living subjects: seeing fundamental biological processes in a new light. , 2003, Genes & development.

[9]  A. Hasso,et al.  Efficacy evaluation of gadoteridol for MR angiography of intracranial vascular lesions , 1994, Journal of magnetic resonance imaging : JMRI.

[10]  T. Vo‐Dinh,et al.  Optical sensor for the detection of caspase-9 activity in a single cell. , 2004, Journal of the American Chemical Society.

[11]  E. De Clercq,et al.  Carrier-mediated delivery improves the efficacy of 9-(2-phosphonylmethoxyethyl)adenine against hepatitis B virus. , 2001, Molecular pharmacology.

[12]  T. Laudański,et al.  Treatment of cancer patients with a low-density-lipoprotein delivery vehicle containing a cytotoxic drug , 2004, Cancer Chemotherapy and Pharmacology.

[13]  Enzo Terreno,et al.  Contrast agents for magnetic resonance angiographic applications: 1H and 17O NMR relaxometric investigations on two gadolinium(III) DTPA-like chelates endowed with high binding affinity to human serum albumin , 1999, JBIC Journal of Biological Inorganic Chemistry.

[14]  Jo Klaveness,et al.  Liposomes as carriers of amphiphilic gadolinium chelates: the effect of membrane composition on incorporation efficacy and in vitro relaxivity. , 2002, International journal of pharmaceutics.

[15]  J. Segrest,et al.  Structure of apolipoprotein B-100 in low density lipoproteins. , 2001, Journal of lipid research.

[16]  Helen H. Hobbs,et al.  Identification of Scavenger Receptor SR-BI as a High Density Lipoprotein Receptor , 1996, Science.

[17]  Shelton D Caruthers,et al.  Molecular imaging of angiogenesis in early-stage atherosclerosis with alpha(v)beta3-integrin-targeted nanoparticles. , 2003, Circulation.

[18]  P. Urizzi,et al.  Indium-111 labeling of low density lipoproteins with the DTPA-bis(stearylamide): evaluation as a potential radiopharmaceutical for tumor localization. , 1996, Bioconjugate chemistry.

[19]  A. Bjørnerud,et al.  A targeted contrast agent for magnetic resonance imaging of thrombus: Implications of spatial resolution , 2001, Journal of magnetic resonance imaging : JMRI.

[20]  Zahi A Fayad,et al.  Recombinant HDL-like nanoparticles: a specific contrast agent for MRI of atherosclerotic plaques. , 2004, Journal of the American Chemical Society.

[21]  Stasia A. Anderson,et al.  Magnetic resonance contrast enhancement of neovasculature with αvβ3‐targeted nanoparticles , 2000 .

[22]  R. Lees,et al.  Adrenal imaging with technetium-99m-labelled low density lipoproteins. , 1986, Metabolism: clinical and experimental.

[23]  T. Murakami,et al.  Hepatic malignancies: usefulness of acquisition of multiple arterial and portal venous phase images at dynamic gadolinium-enhanced MR imaging. , 1996, Radiology.

[24]  Alan Pater,et al.  Loading anticancer drugs into HDL as well as LDL has little affect on properties of complexes and enhances cytotoxicity to human carcinoma cells. , 2002, Journal of controlled release : official journal of the Controlled Release Society.

[25]  H R Hoogenboom,et al.  Design and application of diabodies, triabodies and tetrabodies for cancer targeting. , 2001, Journal of immunological methods.

[26]  R. Lees,et al.  99mTechnetium-labeled low density lipoprotein: receptor recognition and intracellular sequestration of radiolabel. , 1991, Journal of lipid research.

[27]  Sheng-Kwei Song,et al.  Improved molecular imaging contrast agent for detection of human thrombus , 2003, Magnetic resonance in medicine.

[28]  Hui Li,et al.  Rerouting lipoprotein nanoparticles to selected alternate receptors for the targeted delivery of cancer diagnostic and therapeutic agents. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[29]  J. Bulte,et al.  Magnetic resonance imaging of cell surface receptors using targeted contrast agents. , 2004, Current pharmaceutical biotechnology.

[30]  Indrajit Roy,et al.  Ceramic-based nanoparticles entrapping water-insoluble photosensitizing anticancer drugs: a novel drug-carrier system for photodynamic therapy. , 2003, Journal of the American Chemical Society.

[31]  S A Wickline,et al.  Magnetic resonance contrast enhancement of neovasculature with alpha(v)beta(3)-targeted nanoparticles. , 2000, Magnetic resonance in medicine.

[32]  Leif Østergaard,et al.  Cerebral Perfusion Imaging by Bolus Tracking , 2004, Topics in magnetic resonance imaging : TMRI.

[33]  H. Blomgren,et al.  Hypocholesterolemia in cancer patients may be caused by elevated LDL receptor activities in malignant cells , 1985, Medical oncology and tumor pharmacotherapy.

[34]  N. Tarasova,et al.  Small molecule toxins targeting tumor receptors. , 2004, Current pharmaceutical design.

[35]  S. Yanovich,et al.  Characteristics of uptake and cytotoxicity of a low-density lipoprotein-daunomycin complex in P388 leukemic cells. , 1984, Cancer research.

[36]  S. H. Koenig,et al.  The design of liposomal paramagnetic mr agents: effect of vesicle size upon the relaxivity of surface‐incorporated lipophilic chelates , 1992, Magnetic resonance in medicine.

[37]  R. Zhou,et al.  MR and fluorescent imaging of low-density lipoprotein receptors. , 2004, Academic radiology.

[38]  W. Lautt,et al.  Hepatic circulation and toxicology. , 1997, Drug metabolism reviews.

[39]  D. Gómez-Coronado,et al.  Human CD36 is a high affinity receptor for the native lipoproteins HDL, LDL, and VLDL. , 1998, Journal of lipid research.

[40]  Plasma stability and cytotoxicity of lipophilic daunorubicin derivatives incorporated into low density lipoproteins. , 2000, European journal of medicinal chemistry.

[41]  J. Klaveness,et al.  Preparation and in vitro evaluation of a novel amphiphilic GdPCTA-[12] derivative; a micellar MRI contrast agent. , 2003, Organic & biomolecular chemistry.

[42]  R. Mahley,et al.  Uptake of chemically modified low density lipoproteins in vivo is mediated by specific endothelial cells , 1985, The Journal of cell biology.

[43]  S. Laurent,et al.  Physicochemical Characterization of MS‐325, a New Gadolinium Complex, by Multinuclear Relaxometry , 1999 .

[44]  E. Gianolio,et al.  Targeting cells with MR imaging probes based on paramagnetic Gd(III) chelates. , 2004, Current pharmaceutical biotechnology.

[45]  C. Yuan,et al.  Development of a lipoprotein based molecular imaging MR contrast agent for the noninvasive detection of early atherosclerotic disease , 2004, The International Journal of Cardiovascular Imaging.

[46]  S. Yamashita,et al.  Marked hypocholesterolemia in a case with adrenal adenoma--enhanced catabolism of low density lipoprotein (LDL) via the LDL receptors of tumor cells. , 1995, The Journal of clinical endocrinology and metabolism.

[47]  M. Krieger,et al.  Reconstitution of the hydrophobic core of low-density lipoprotein. , 1986, Methods in enzymology.

[48]  S. Caruthers,et al.  Novel paramagnetic contrast agents for molecular imaging and targeted drug delivery. , 2004, Current pharmaceutical biotechnology.

[49]  M. Brown,et al.  Receptor-mediated endocytosis: insights from the lipoprotein receptor system. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[50]  P. Urizzi,et al.  Internalization of indium‐labeled LDL through a lipid chelating anchor in human pancreatic‐cancer cells as a potential radiopharmaceutical for tumor localization , 1997, International journal of cancer.

[51]  D. Rhainds,et al.  Low density lipoprotein uptake: holoparticle and cholesteryl ester selective uptake. , 1999, The international journal of biochemistry & cell biology.

[52]  S. Vitols,et al.  Elevated uptake of low density lipoprotein by drug resistant human leukemic cell lines. , 2002, Biochemical pharmacology.

[53]  Y. Chen,et al.  Human prostate cancer cells lack feedback regulation of low‐density lipoprotein receptor and its regulator, SREBP2 , 2001, International journal of cancer.

[54]  H. Lodish,et al.  Expression cloning of SR-BI, a CD36-related class B scavenger receptor. , 1994, The Journal of biological chemistry.

[55]  J. Goldstein,et al.  Regulation of the activity of the low density lipoprotein receptor in human fibroblasts , 1975, Cell.

[56]  Hui Li,et al.  High payload delivery of optical imaging and photodynamic therapy agents to tumors using phthalocyanine-reconstituted low-density lipoprotein nanoparticles. , 2005, Journal of biomedical optics.

[57]  E. Koivunen,et al.  Peptide-mediated delivery of therapeutic and imaging agents into mammalian cells. , 2004, Current pharmaceutical design.

[58]  M. Phillips,et al.  Apolipoprotein B-100 conformation and particle surface charge in human LDL subspecies: implication for LDL receptor interaction. , 1998, Biochemistry.

[59]  Britton Chance,et al.  Tricarbocyanine cholesteryl laurates labeled LDL: new near infrared fluorescent probes (NIRFs) for monitoring tumors and gene therapy of familial hypercholesterolemia. , 2002, Bioorganic & medicinal chemistry letters.

[60]  G. Soula,et al.  Biodistribution study of 99mTc‐labeled LDL in B16‐melanoma‐bearing mice. Visualization of a preferential uptake by the tumor , 1993, International journal of cancer.

[61]  E. Ruoslahti Antiangiogenics meet nanotechnology. , 2002, Cancer cell.

[62]  Britton Chance,et al.  Carbocyanine labeled LDL for optical imaging of tumors1 , 2004 .

[63]  M. Krieger [34] Reconstitution of the hydrophobic core of low-density lipoprotein , 1986 .

[64]  Thommey P. Thomas,et al.  Design and Function of a Dendrimer-Based Therapeutic Nanodevice Targeted to Tumor Cells Through the Folate Receptor , 2002, Pharmaceutical Research.

[65]  S A Wickline,et al.  Novel MRI Contrast Agent for Molecular Imaging of Fibrin: Implications for Detecting Vulnerable Plaques , 2001, Circulation.

[66]  Samuel A. Wickline,et al.  Molecular Imaging of Angiogenesis in Early-Stage Atherosclerosis With &agr;v&bgr;3-Integrin–Targeted Nanoparticles , 2003 .

[67]  Alexander Petrovsky,et al.  Magnetic resonance imaging of inducible E-selectin expression in human endothelial cell culture. , 2002, Bioconjugate chemistry.

[68]  M J Welch,et al.  Metabolic imaging with gallium-68- and indium-111-labeled low-density lipoprotein. , 1991, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[69]  A. Leo,et al.  Low density lipoprotein receptor and mRNA expression in human colorectal cancer. , 2001, Anticancer Research.

[70]  Grace Hu,et al.  Molecular MR imaging of melanoma angiogenesis with ανβ3‐targeted paramagnetic nanoparticles , 2005, Magnetic resonance in medicine.

[71]  E. Simpson,et al.  Low-density lipoprotein as a potential vehicle for chemotherapeutic agents and radionucleotides in the management of gynecologic neoplasms. , 1981, American journal of obstetrics and gynecology.

[72]  V. Runge,et al.  Central Nervous System: Review of Clinical Use of Contrast Media , 2001, Topics in magnetic resonance imaging : TMRI.

[73]  A. Niendorf,et al.  Increased LDL receptor mRNA expression in colon cancer is correlated with a rise in plasma cholesterol levels after curative surgery , 1995, International journal of cancer.

[74]  T. V. van Berkel,et al.  Specific targeting of a lipophilic prodrug of iododeoxyuridine to parenchymal liver cells using lactosylated reconstituted high density lipoprotein particles. , 1996, Biochemical pharmacology.

[75]  H. Schmidt,et al.  Low-density lipoprotein receptor mRNA in human breast cancer cells: Influence by PKC modulators , 1997, Breast Cancer Research and Treatment.

[76]  S. Vitols,et al.  Low Density Lipoprotein as a Carrier of Cytostatics in Cancer Chemotherapy: Study of Stability of Drug-carrier Complexes in Blood , 2000, Journal of drug targeting.

[77]  L. Chan,et al.  Reversal of Hypercholesterolemia in Low Density Lipoprotein Receptor Knockout Mice by Adenovirus-mediated Gene Transfer of the Very Low Density Lipoprotein Receptor (*) , 1996, The Journal of Biological Chemistry.