Systemic delivery of blood–brain barrier-targeted polymeric nanoparticles enhances delivery to brain tissue

References

• Mayberg M, Langer RS, Zervas NT, Moskowitz MA. Perivascular meningeal projections from cat trigeminal ganglia: possible pathway for vascular headaches in man. Science 1981;213:228–30
   PubMed Web of Science ®Google Scholar
• During MJ, Freese A, Sabel BA, et al. Controlled release of dopamine from a polymeric brain implant: in vivo characterization. Ann Neurol 1989;25:351–6
   PubMed Web of Science ®Google Scholar
• Freese A, Sabel BA, Saltzman WM, et al. Controlled release of dopamine from a polymeric brain implant: in vitro characterization. Exp Neurol 1989;103:234–8
   PubMed Web of Science ®Google Scholar
• Fung LK, Ewend MG, Sills A, et al. Pharmacokinetics of interstitial delivery of carmustine, 4-hydroperoxycyclophosphamide, and paclitaxel from a biodegradable polymer implant in the monkey brain. Cancer Res 1998;58:672–84
   PubMed Web of Science ®Google Scholar
• Zhou J, Patel TR, Sirianni RW, et al. Highly penetrative, drug-loaded nanocarriers improve treatment of glioblastoma. Proc Natl Acad Sci USA 2013;110:11751–6
   PubMed Web of Science ®Google Scholar
• Barchet TM, Amiji MM. Challenges and opportunities in CNS delivery of therapeutics for neurodegenerative diseases. Expert Opin Drug Deliv 2009;6:211–25
   PubMed Web of Science ®Google Scholar
• Institute NC. SEER Stat Fact Sheets: Brain and Other Nervous System Cancer 2015. Available from: http://seer.cancer.gov/statfacts/html/brain.html#risk [last accessed 10 Mar 2015]
   Google Scholar
• Weller M, Cloughesy T, Perry JR, Wick W. Standards of care for treatment of recurrent glioblastoma – are we there yet? Neuro Oncol 2013;15:4–27
   PubMed Web of Science ®Google Scholar
• Stupp R, Mason WP, van den Bent MJ, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 2005;352:987–96
   PubMed Web of Science ®Google Scholar
• Johnson DR, O'Neill BP. Glioblastoma survival in the United States before and during the temozolomide era. J Neurooncol 2012;107:359–64
   PubMed Web of Science ®Google Scholar
• Pardridge WM. Drug transport across the blood-brain barrier. J Cereb Blood Flow Metab 2012;32:1959–72
   PubMed Web of Science ®Google Scholar
• Abbott NJ, Patabendige AA, Dolman DE, et al. Structure and function of the blood-brain barrier. Neurobiol Dis 2010;37:13–25
   PubMed Web of Science ®Google Scholar
• van Tellingen O, Yetkin-Arik B, de Gooijer MC, et al. Overcoming the blood-brain tumor barrier for effective glioblastoma treatment. Drug Resist Updat 2015;19:1–12
   PubMed Web of Science ®Google Scholar
• Lockman PR, Mittapalli RK, Taskar KS, et al. Heterogeneous blood-tumor barrier permeability determines drug efficacy in experimental brain metastases of breast cancer. Clin Cancer Res 2010;16:5664–78
   PubMed Web of Science ®Google Scholar
• Li J, Feng L, Fan L, et al. Targeting the brain with PEG-PLGA nanoparticles modified with phage-displayed peptides. Biomaterials 2011;32:4943–50
   PubMed Web of Science ®Google Scholar
• Gao X, Qian J, Zheng S, et al. Overcoming the blood-brain barrier for delivering drugs into the brain by using adenosine receptor nanoagonist. ACS Nano 2014;8:3678–89
   PubMed Web of Science ®Google Scholar
• Jensen SA, Day ES, Ko CH, et al. Spherical nucleic acid nanoparticle conjugates as an RNAi-based therapy for glioblastoma. Sci Transl Med 2013;5:209ra152
   Google Scholar
• Cheng CJ, Tietjen GT, Saucier-Sawyer JK, Saltzman WM. A holistic approach to targeting disease with polymeric nanoparticles. Nat Rev Drug Discov 2015;14:239–47
   PubMed Web of Science ®Google Scholar
• Marin E, Briceno MI, Caballero-George C. Critical evaluation of biodegradable polymers used in nanodrugs. Int J Nanomed 2013;8:3071–91
   PubMed Web of Science ®Google Scholar
• Shive MS, Anderson JM. Biodegradation and biocompatibility of PLA and PLGA microspheres. Adv Drug Deliv Rev 1997;28:5–24
   PubMed Web of Science ®Google Scholar
• Woodrow KA, Cu Y, Booth CJ, et al. Intravaginal gene silencing using biodegradable polymer nanoparticles densely loaded with small-interfering RNA. Nat Mater 2009;8:526–33
   PubMed Web of Science ®Google Scholar
• Sawyer AJ, Saucier-Sawyer JK, Booth CJ, et al. Convection-enhanced delivery of camptothecin-loaded polymer nanoparticles for treatment of intracranial tumors. Drug Deliv Transl Res 2011;1:34–42
   PubMed Web of Science ®Google Scholar
• Ediriwickrema A, Zhou J, Deng Y, Saltzman WM. Multi-layered nanoparticles for combination gene and drug delivery to tumors. Biomaterials 2014;35:9343–54
   PubMed Web of Science ®Google Scholar
• Zhou J, Patel TR, Fu M, et al. Octa-functional PLGA nanoparticles for targeted and efficient siRNA delivery to tumors. Biomaterials 2012;33:583–91
   PubMed Web of Science ®Google Scholar
• Cheng J, Teply BA, Sherifi I, et al. Formulation of functionalized PLGA-PEG nanoparticles for in vivo targeted drug delivery. Biomaterials 2007;28:869–76
   PubMed Web of Science ®Google Scholar
• Park J, Fong PM, Lu J, et al. PEGylated PLGA nanoparticles for the improved delivery of doxorubicin. Nanomedicine 2009;5:410–18
   PubMed Web of Science ®Google Scholar
• Chan JM, Zhang L, Yuet KP, et al. PLGA-lecithin-PEG core-shell nanoparticles for controlled drug delivery. Biomaterials 2009;30:1627–34
   PubMed Web of Science ®Google Scholar
• Gref R, Minamitake Y, Peracchia MT, et al. Biodegradable long-circulating polymeric nanospheres. Science 1994;263:1600–3
   PubMed Web of Science ®Google Scholar
• Nance EA, Woodworth GF, Sailor KA, et al. A dense poly(ethylene glycol) coating improves penetration of large polymeric nanoparticles within brain tissue. Sci Transl Med 2012;4:149ra19
   Google Scholar
• Deng Y, Saucier-Sawyer JK, Hoimes CJ, et al. The effect of hyperbranched polyglycerol coatings on drug delivery using degradable polymer nanoparticles. Biomaterials 2014;35:6595–602
   PubMed Web of Science ®Google Scholar
• Xin HL, Sha XY, Jiang XY, et al. Anti-glioblastoma efficacy and safety of paclitaxel-loading angiopep-conjugated dual targeting PEG-PCL nanoparticles. Biomaterials 2012;33:8167–76
   PubMed Web of Science ®Google Scholar
• Ulbrich K, Knobloch T, Kreuter J. Targeting the insulin receptor: nanoparticles for drug delivery across the blood-brain barrier (BBB). J Drug Target 2011;19:125–32
   PubMed Web of Science ®Google Scholar
• Jain A, Chasoo G, Singh SK, et al. Transferrin-appended PEGylated nanoparticles for temozolomide delivery to brain: in vitro characterisation. J Microencapsul 2011;28:21–8
   PubMed Web of Science ®Google Scholar
• Bickel U, Yoshikawa T, Pardridge WM. Delivery of peptides and proteins through the blood-brain barrier. Adv Drug Deliv Rev 2001;46:247–79
   PubMed Web of Science ®Google Scholar
• Herve F, Ghinea N, Scherrmann JM. CNS delivery via adsorptive transcytosis. Aaps J 2008;10:455–72
   PubMed Web of Science ®Google Scholar
• Liu L, Guo K, Lu J, et al. Biologically active core/shell nanoparticles self-assembled from cholesterol-terminated PEG-TAT for drug delivery across the blood-brain barrier. Biomaterials 2008;29:1509–17
   PubMed Web of Science ®Google Scholar
• Smith MW, Gumbleton M. Endocytosis at the blood-brain barrier: from basic understanding to drug delivery strategies. J Drug Target 2006;14:191–214
   PubMed Web of Science ®Google Scholar
• Lafon M. Rabies virus receptors. J Neurovirol 2005;11:82–7
   PubMed Web of Science ®Google Scholar
• Lentz TL, Burrage TG, Smith AL, Tignor GH. The acetylcholine receptor as a cellular receptor for rabies virus. Yale J Biol Med 1983;56:315–22
   PubMed Web of Science ®Google Scholar
• Kumar P, Wu H, McBride JL, et al. Transvascular delivery of small interfering RNA to the central nervous system. Nature 2007;448:39–43
   PubMed Web of Science ®Google Scholar
• Liu Y, Huang R, Han L, et al. Brain-targeting gene delivery and cellular internalization mechanisms for modified rabies virus glycoprotein RVG29 nanoparticles. Biomaterials 2009;30:4195–202
   PubMed Web of Science ®Google Scholar
• Xiang L, Zhou R, Fu A, et al. Targeted delivery of large fusion protein into hippocampal neurons by systemic administration. J Drug Target 2011;19:632–6
   PubMed Web of Science ®Google Scholar
• Park TE, Singh B, Li H, et al. Enhanced BBB permeability of osmotically active poly(mannitol-co-PEI) modified with rabies virus glycoprotein via selective stimulation of caveolar endocytosis for RNAi therapeutics in Alzheimer's disease. Biomaterials 2015;38:61–71
   PubMed Web of Science ®Google Scholar
• Gaudin A, Yemisci M, Eroglu H, et al. Squalenoyl adenosine nanoparticles provide neuroprotection after stroke and spinal cord injury. Nat Nanotechnol 2014;9:1054–62
   PubMed Web of Science ®Google Scholar
• Carman AJ, Mills JH, Krenz A, et al. Adenosine receptor signaling modulates permeability of the blood-brain barrier. J Neurosci 2011;31:13272–80
   PubMed Web of Science ®Google Scholar
• Kim DG, Bynoe MS. A2A adenosine receptor regulates the human blood-brain barrier permeability. Mol Neurobiol 2015;52:664–78
   PubMed Web of Science ®Google Scholar
• Zhou J, Patel TR, Sirianni RW, et al. Highly penetrative, drug-loaded nanocarriers improve treatment of glioblastoma. Proc Natl Acad Sci USA 2013;110:11751–6
   PubMed Web of Science ®Google Scholar
• Thorne RG, Nicholson C. In vivo diffusion analysis with quantum dots and dextrans predicts the width of brain extracellular space. Proc Natl Acad Sci USA 2006;103:5567–72
   PubMed Web of Science ®Google Scholar
• Hobbs SK, Monsky WL, Yuan F, et al. Regulation of transport pathways in tumor vessels: role of tumor type and microenvironment. Proc Natl Acad Sci USA 1998;95:4607–12
   PubMed Web of Science ®Google Scholar
• Cheng CJ, Saltzman WM. Enhanced siRNA delivery into cells by exploiting the synergy between targeting ligands and cell-penetrating peptides. Biomaterials 2011;32:6194–203
   PubMed Web of Science ®Google Scholar
• Vauthier C, Schmidt C, Couvreur P. Measurement of the density of polymeric nanoparticulate drug carriers by isopycnic centrifugation. J Nanopart Res 1999;1:411–18
   Web of Science ®Google Scholar
• Householder KT, DiPerna DM, Chung EP, et al. Intravenous delivery of camptothecin-loaded PLGA nanoparticles for the treatment of intracranial glioma. Int J Pharm 2015;479:374–80
   PubMed Web of Science ®Google Scholar
• Xin HL, Sha XY, Jiang XY, et al. The brain targeting mechanism of Angiopep-conjugated poly(ethylene glycol)-co-poly(epsilon-caprolactone) nanoparticles. Biomaterials 2012;33:1673–81
   PubMed Web of Science ®Google Scholar
• Kreuter J. Drug delivery to the central nervous system by polymeric nanoparticles: what do we know? Adv Drug Deliv Rev 2014;71:2–14
   PubMed Web of Science ®Google Scholar
• Xin HL, Jiang XY, Gu JJ, et al. Angiopep-conjugated poly(ethylene glycol)-co-poly(epsilon-caprolactone) nanoparticles as dual-targeting drug delivery system for brain glioma. Biomaterials 2011;32:4293–305
   PubMed Web of Science ®Google Scholar
• Alavijeh MS, Palmer AM. Measurement of the pharmacokinetics and pharmacodynamics of neuroactive compounds. Neurobiol Dis 2010;37:38–47
   PubMed Web of Science ®Google Scholar
• Harris JM, Chess RB. Effect of pegylation on pharmaceuticals. Nat Rev Drug Discov 2003;2:214–21
   PubMed Web of Science ®Google Scholar
• Saadati R, Dadashzadeh S, Abbasian Z, Soleimanjahi H. Accelerated blood clearance of PEGylated PLGA nanoparticles following repeated injections: effects of polymer dose, PEG coating, and encapsulated anticancer drug. Pharm Res 2013;30:985–95
   PubMed Web of Science ®Google Scholar
• Huile G, Shuaiqi P, Zhi Y, et al. A cascade targeting strategy for brain neuroglial cells employing nanoparticles modified with angiopep-2 peptide and EGFP-EGF1 protein. Biomaterials 2011;32:8669–75
   PubMed Web of Science ®Google Scholar
• Gao H, Zhang S, Cao S, et al. Angiopep-2 and activatable cell-penetrating peptide dual-functionalized nanoparticles for systemic glioma-targeting delivery. Mol Pharm 2014;11:2755–63
   PubMed Web of Science ®Google Scholar
• Cui Y, Xu Q, Chow PK, et al. Transferrin-conjugated magnetic silica PLGA nanoparticles loaded with doxorubicin and paclitaxel for brain glioma treatment. Biomaterials 2013;34:8511–20
   PubMed Web of Science ®Google Scholar
• Gao H, Qian J, Cao S, et al. Precise glioma targeting of and penetration by aptamer and peptide dual-functioned nanoparticles. Biomaterials 2012;33:5115–23
   PubMed Web of Science ®Google Scholar
• Pardridge WM. The blood-brain barrier: bottleneck in brain drug development. NeuroRx 2005;2:3–14
   PubMedGoogle Scholar
• Li JY, Boado RJ, Pardridge WM. Cloned blood-brain barrier adenosine transporter is identical to the rat concentrative Na + nucleoside cotransporter CNT2. J Cereb Blood Flow Metab 2001;21:929–36
   PubMed Web of Science ®Google Scholar
• Jacobson KA, Gao ZG. Adenosine receptors as therapeutic targets. Nat Rev Drug Discov 2006;5:247–64
   PubMed Web of Science ®Google Scholar
• Brigger I, Morizet J, Aubert G, et al. Poly(ethylene glycol)-coated hexadecylcyanoacrylate nanospheres display a combined effect for brain tumor targeting. J Pharmacol Exp Ther 2002;303:928–36
   PubMed Web of Science ®Google Scholar
• Gu GZ, Gao XL, Hu QY, et al. The influence of the penetrating peptide iRGD on the effect of paclitaxel-loaded MT1-AF7p-conjugated nanoparticles on glioma cells. Biomaterials 2013;34:5138–48
   PubMed Web of Science ®Google Scholar
• Chevalier A, Dubois M, Le Joncour V, et al. Synthesis, biological evaluation, and in vivo imaging of the first camptothecin-fluorescein conjugate. Bioconjug Chem 2013;24:1119–33
   PubMed Web of Science ®Google Scholar
• Serwer L, Hashizume R, Ozawa T, James CD. Systemic and local drug delivery for treating diseases of the central nervous system in rodent models. J Vis Exp 2010;42:1992
   PubMedGoogle Scholar