Localized delivery of low-density lipoprotein docosahexaenoic acid nanoparticles to the rat brain using focused ultrasound

Pardridge, 2012, Drug transport across the blood-brain barrier, J. Cereb. Blood Flow Metab. Off. J. Int. Soc. Cereb. Blood Flow Metab., 32, 1959, 10.1038/jcbfm.2012.126 Rubin, 1999, The cell biology of the blood-brain barrier, Annu. Rev. Neurosci., 22, 11, 10.1146/annurev.neuro.22.1.11 Stewart, 1987, Interendothelial junctional changes underlie the developmental ‛tightening’ of the blood-brain barrier, Brain Res., 429, 271, 10.1016/0165-3806(87)90107-6 Wolburg, 2002, Tight junctions of the blood-brain barrier: development, composition and regulation, Vasc. Pharmacol., 38, 323, 10.1016/S1537-1891(02)00200-8 Pardridge, 2003, Blood-brain barrier drug targeting: the future of brain drug development, Mol. Interv., 3, 90, 10.1124/mi.3.2.90 Cosolo, 1989, Blood-brain barrier disruption using mannitol: time course and electron microscopy studies, Am. J. Physiol., 256, R443 Zou, 2013, Cell-penetrating peptide-mediated therapeutic molecule delivery into the central nervous system, Curr. Neuropharmacol., 11, 197, 10.2174/1570159X11311020006 Bobo, 1994, Convection-enhanced delivery of macromolecules in the brain, Proc. Natl. Acad. Sci., 91, 2076, 10.1073/pnas.91.6.2076 Fresta, 1997, Survival rate improvement in a rat ischemia model by long circulating liposomes containing cytidine-5I-diphosphate choline, Life Sci., 61, 1227, 10.1016/S0024-3205(97)00667-X Korkusuz, 2013, Transferrin-coated gadolinium nanoparticles as MRI contrast agent, Mol. imaging Biol. MIB Off. Publ. Acad. Mol. Imaging, 15, 148, 10.1007/s11307-012-0579-6 Kreuter, 2015, Influence of chronobiology on the nanoparticle-mediated drug uptake into the brain, Pharmaceutics, 7, 3, 10.3390/pharmaceutics7010003 Cosco, 2014, Colloidal supramolecular aggregates for therapeutic application in neuromedicine, Curr. Med. Chem., 21, 4132, 10.2174/0929867321666140826113933 Hynynen, 2001, Noninvasive MR imaging-guided focal opening of the blood-brain barrier in rabbits, Radiology, 220, 640, 10.1148/radiol.2202001804 Sheikov, 2004, Cellular mechanisms of the blood-brain barrier opening induced by ultrasound in presence of microbubbles, Ultrasound Med. Biol., 30, 979, 10.1016/j.ultrasmedbio.2004.04.010 Marty, 2012, Dynamic study of blood-brain barrier closure after its disruption using ultrasound: a quantitative analysis, J. Cereb. Blood Flow Metab. Off. J. Int. Soc. Cereb. Blood Flow Metab., 32, 1948, 10.1038/jcbfm.2012.100 Cho, 2011, Two-photon fluorescence microscopy study of cerebrovascular dynamics in ultrasound-induced blood-brain barrier opening, J. Cereb. Blood Flow Metab. Off. J. Int. Soc. Cereb. Blood Flow Metab., 31, 1852, 10.1038/jcbfm.2011.59 Park, 2012, The kinetics of blood brain barrier permeability and targeted doxorubicin delivery into brain induced by focused ultrasound, J. Control Release, 162, 134, 10.1016/j.jconrel.2012.06.012 Hynynen, 2003, Non-invasive opening of BBB by focused ultrasound, Acta Neurochir. Suppl., 86, 555 Chen, 2014, The size of blood-brain barrier opening induced by focused ultrasound is dictated by the acoustic pressure, J. Cereb. Blood Flow Metab. Off. J. Int. Soc. Cereb. Blood Flow Metab., 34, 1197, 10.1038/jcbfm.2014.71 De Jong, 2008, Drug delivery and nanoparticles: applications and hazards, Int. J. Nanomed., 3, 133, 10.2147/IJN.S596 Palombo, 2014, Pharmaceutical and toxicological properties of engineered nanomaterials for drug delivery, Annu. Rev. Pharmacol. Toxicol., 54, 581, 10.1146/annurev-pharmtox-010611-134615 Masserini, 2013, Nanoparticles for brain drug delivery, ISRN Biochem., 2013, 18, 10.1155/2013/238428 Corbin, 2006, Low-density lipoprotein nanoparticles as magnetic resonance imaging contrast agents, Neoplasia, 8, 488, 10.1593/neo.05835 Duivenvoorden, 2014, A statin-loaded reconstituted high-density lipoprotein nanoparticle inhibits atherosclerotic plaque inflammation, Nat. Commun., 5 Ng, 2011, Lipoprotein-inspired nanoparticles for cancer theranostics, Acc. Chem. Res., 44, 1105, 10.1021/ar200017e Allijn, 2013, Gold nanocrystal labeling allows low-density lipoprotein imaging from the subcellular to macroscopic level, ACS Nano, 7, 9761, 10.1021/nn403258w Bing, 2014, Trans-cranial opening of the blood-brain barrier in targeted regions using a stereotaxic brain atlas and focused ultrasound energy, J. Ther. Ultrasound, 2, 13, 10.1186/2050-5736-2-13 Lund-Katz, 1998, Apolipoprotein B-100 conformation and particle surface charge in human LDL subspecies: implication for LDL receptor interaction, Biochemistry, 37, 12867, 10.1021/bi980828m Reynolds, 2014, Low-density lipoprotein-mediated delivery of docosahexaenoic acid selectively kills murine liver cancer cells, Nanomedicine UK, 1 Li, 2004, Carbocyanine labeled LDL for optical imaging of tumors, Acad. Radiol., 11, 669, 10.1016/j.acra.2004.01.016 Stewart, 1980, Colorimetric determination of phospholipids with ammonium ferrothiocyanate, Anal. Biochem., 104, 10, 10.1016/0003-2697(80)90269-9 Mehta, 1998, Rapid quantitation of free fatty acids in human plasma by high-performance liquid chromatography, J. Chromatogr. B Biomed. Sci. Appl., 719, 9, 10.1016/S0378-4347(98)00403-4 Zhang, 2013, Optimized negative-staining electron microscopy for lipoprotein studies, Biochim. Biophys. Acta, 1830, 2150, 10.1016/j.bbagen.2012.09.016 O'Reilly MA, Muller A, Hynynen K. Ultrasound Insertion Loss of Rat Parietal Bone Appears to Be Proportional to Animal Mass at Submegahertz Frequencies. Ultrasound in Medicine and Biology.37:1930-7. Aslan, 2013, LC-MS/MS analysis of plasma polyunsaturated fatty acids in type 2 diabetic patients after insulin analog initiation therapy, Lipids Health Dis., 12, 169, 10.1186/1476-511X-12-169 Zhao, 2010, An extremely simple method for extraction of lysophospholipids and phospholipids from blood samples, J. Lipid Res., 51, 652, 10.1194/jlr.D001503 Erdahl, 1991, A comparison of phospholipid degradation by oxidation and hydrolysis during the mitochondrial permeability transition, Arch. Biochem. Biophys., 285, 252, 10.1016/0003-9861(91)90357-O Aggerbeck, 1976, Enzymatic probes of lipoprotein structure. Hydrolysis of human serum low density lipoprotein-2 by phospholipase A2, J. Biol. Chem., 251, 3823, 10.1016/S0021-9258(17)33418-X Krieger, 1979, Replacement of neutral lipids of low density lipoprotein with esters of long chain unsaturated fatty acids, J. Biol. Chem., 254, 3845, 10.1016/S0021-9258(18)50664-5 Shen, 1977, Structure of human serum lipoproteins inferred from compositional analysis, Proc. Natl. Acad. Sci. U. S. A., 74, 837, 10.1073/pnas.74.3.837 Choi, 2010, Molecules of various pharmacologically-relevant sizes can cross the ultrasound-induced blood-brain barrier opening in vivo, Ultrasound Med. Biol., 36, 58, 10.1016/j.ultrasmedbio.2009.08.006 Panzenboeck, 2002, ABCA1 and scavenger receptor class B, type I, are modulators of reverse sterol transport at an in vitro blood-brain barrier constituted of porcine brain capillary endothelial cells, J. Biol. Chem., 277, 42781, 10.1074/jbc.M207601200 Dehouck, 1997, A new function for the LDL receptor: transcytosis of LDL across the blood-brain barrier, J. Cell Biol., 138, 877, 10.1083/jcb.138.4.877 Spady, 1987, Role of receptor-independent low density lipoprotein transport in the maintenance of tissue cholesterol balance in the normal and WHHL rabbit, J. Lipid Res., 28, 32, 10.1016/S0022-2275(20)38731-9 Osono, 1995, Role of the low density lipoprotein receptor in the flux of cholesterol through the plasma and across the tissues of the mouse, J. Clin. Investig., 95, 1124, 10.1172/JCI117760 Dietschy, 2004, Thematic review series: brain Lipids. Cholesterol metabolism in the central nervous system during early development and in the mature animal, J. Lipid Res., 45, 1375, 10.1194/jlr.R400004-JLR200 Spady, 1983, Rates of receptor-dependent and -independent low density lipoprotein uptake in the hamster, Proc. Natl. Acad. Sci. U. S. A., 80, 3499, 10.1073/pnas.80.11.3499 Goppert, 2005, Polysorbate-stabilized solid lipid nanoparticles as colloidal carriers for intravenous targeting of drugs to the brain: comparison of plasma protein adsorption patterns, J. Drug Target, 13, 179, 10.1080/10611860500071292 Kreuter, 2007, Covalent attachment of apolipoprotein A-I and apolipoprotein B-100 to albumin nanoparticles enables drug transport into the brain, J. Control Release, 118, 54, 10.1016/j.jconrel.2006.12.012 Lemke, 2010, Delivery of amphotericin B nanosuspensions to the brain and determination of activity against Balamuthia mandrillaris amebas, Nanomedicine UK, 6, 597, 10.1016/j.nano.2009.12.004 Herz, 2000, Apolipoprotein E receptors: linking brain development and Alzheimer's disease, Nat. Rev. Neurosci., 1, 51, 10.1038/35036221 Jung-Testas, 1992, Low density lipoprotein-receptors in primary cultures of rat glial cells, J. Steroid Biochem. Mol. Biol., 42, 597, 10.1016/0960-0760(92)90450-W Bazinet, 2014, Polyunsaturated fatty acids and their metabolites in brain function and disease, Nat. Rev. Neurosci., 15, 771, 10.1038/nrn3820 Domenichiello, 2014, Whole body synthesis rates of DHA from alpha-linolenic acid are greater than brain DHA accretion and uptake rates in adult rats, J. Lipid Res., 55, 62, 10.1194/jlr.M042275 Crawford, 1999, Evidence for the unique function of docosahexaenoic acid during the evolution of the modern hominid brain, Lipids, 34, S39, 10.1007/BF02562227 Singh, 2005, Essential fatty acids, DHA and human brain, Indian J. Pediatr., 72, 239, 10.1007/BF02859265 Hong, 2003, Novel docosatrienes and 17S-resolvins generated from docosahexaenoic acid in murine brain, human blood, and glial cells. Autacoids in anti-inflammation, J. Biol. Chem., 278, 14677, 10.1074/jbc.M300218200 Serhan, 2007, Resolution of inflammation: state of the art, definitions and terms, FASEB J., 21, 325, 10.1096/fj.06-7227rev Serhan, 2007, Resolution phase of inflammation: novel endogenous anti-inflammatory and proresolving lipid mediators and pathways, Annu. Rev. Immunol., 25, 101, 10.1146/annurev.immunol.25.022106.141647 Tassoni, 2008, The role of eicosanoids in the brain, Asia Pac. J. Clin. Nutr., 17, 220 Niemoller, 2010, Docosahexaenoic acid neurolipidomics, Prostagl. Other Lipid Mediat., 91, 85, 10.1016/j.prostaglandins.2009.09.005 Esterbauer, 1991, Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes, Free Radic. Biol. Med., 11, 81, 10.1016/0891-5849(91)90192-6 Dyall, 2008, Neurological benefits of omega-3 fatty acids, Neuromolecular Med., 10, 219, 10.1007/s12017-008-8036-z Rapoport, 2007, Brain metabolism of nutritionally essential polyunsaturated fatty acids depends on both the diet and the liver, Prostagl. Leukot. Essent. Fat. Acids, 77, 251, 10.1016/j.plefa.2007.10.023 Barberger-Gateau, 2002, Fish, meat, and risk of dementia: cohort study, BMJ, 325, 932, 10.1136/bmj.325.7370.932 Orr, 2013, Unesterified docosahexaenoic acid is protective in neuroinflammation, J. Neurochem., 127, 378, 10.1111/jnc.12392 Trepanier, 2012, Increases in seizure latencies induced by subcutaneous docosahexaenoic acid are lost at higher doses, Epilepsy Res., 99, 225, 10.1016/j.eplepsyres.2011.12.001 Bazan, 2011, Docosahexaenoic acid signalolipidomics in nutrition: significance in aging, neuroinflammation, macular degeneration, Alzheimer's, and other neurodegenerative diseases, Annu. Rev. Nutr., 31, 321, 10.1146/annurev.nutr.012809.104635 Gleissman, 2010, Docosahexaenoic acid metabolome in neural tumors: identification of cytotoxic intermediates, FASEB J., 24, 906, 10.1096/fj.09-137919 Lindskog, 2006, Neuroblastoma cell death in response to docosahexaenoic acid: sensitization to chemotherapy and arsenic-induced oxidative stress, Int. J. Cancer, 118, 2584, 10.1002/ijc.21555 Downs, 2015, Long-term safety of repeated blood-brain Barrier opening via focused ultrasound with microbubbles in non-human primates performing a cognitive task, PLoS One, 10, e0125911, 10.1371/journal.pone.0125911 Belayev, 2005, Docosahexaenoic acid complexed to albumin elicits high-grade ischemic neuroprotection, Stroke J. Cereb. Circ., 36, 118, 10.1161/01.STR.0000149620.74770.2e