Drug delivery to the central nervous system by polymeric nanoparticles: What do we know?

Advanced Drug Delivery Reviews

Volumn 71, Issue , 2014, Pages 2-14

  Kreuter, Jörg ^a  

^a GOETHE UNIVERSITY   (Germany)

Author keywords

Brain targeting; Brain tumours; Drug delivery; Glioblastomas; Nanoparticles

Indexed keywords

BIOCOMPATIBILITY; BRAIN; DRUG DELIVERY; DRUG PRODUCTS; ENDOTHELIAL CELLS; MACROMOLECULES; MOLECULAR BIOLOGY; NONINVASIVE MEDICAL PROCEDURES; PROTEINS; TUMORS;

BRAIN TARGETING; BRAIN TUMOURS; CENTRAL NERVOUS SYSTEMS; GLIOBLASTOMAS; INTRAVENOUS INJECTIONS; NANOPARTICLE SURFACE; POLYMERIC NANOPARTICLES; RECEPTOR-MEDIATED ENDOCYTOSIS;

NANOPARTICLES;

BETA CYCLODEXTRIN; CAMPTOTHECIN; CARMUSTINE; CURCUMIN; CYANOACRYLATE DERIVATIVE; DOXORUBICIN; ENHANCED GREEN FLUORESCENT PROTEIN; GEMCITABINE; HORSERADISH PEROXIDASE; NANOPARTICLE; PIPERINE; POLY(BUTYL CYANOACRYLATE) NANOPARTICLE; POLYCAPROLACTONE; POLYGLACTIN NANOPARTICLE; POLYSORBATE 80; QUINOLINE; RIVASTIGMINE; SOLID LIPID NANOPARTICLE; TACRINE; UNCLASSIFIED DRUG; POLYMER;

ALZHEIMER DISEASE; ANTINEOPLASTIC ACTIVITY; BIOCOMPATIBILITY; BIODEGRADABILITY; BLOOD BRAIN BARRIER; BRAIN TUMOR; CANCER SURVIVAL; CARDIOTOXICITY; CENTRAL NERVOUS SYSTEM DISEASE; CHEMICAL MODIFICATION; CONVECTION ENHANCED DELIVERY; COVALENT BOND; DRUG BRAIN LEVEL; DRUG COATING; DRUG DELIVERY SYSTEM; DRUG DISTRIBUTION; DRUG PENETRATION; DRUG RELEASE; DRUG SAFETY; DRUG TARGETING; DRUG TRANSPORT; DRUG UPTAKE; ENDOCYTOSIS; ENDOTHELIUM CELL; GLIOBLASTOMA; GLIOMA; HUMAN; LIVER TOXICITY; NONHUMAN; PARTICLE SIZE; PRIORITY JOURNAL; REVIEW; SURFACE CHARGE; SURFACE PROPERTY; SURVIVAL TIME; TRANSCYTOSIS; ANIMAL; BRAIN; CHEMISTRY; DRUG-RELATED SIDE EFFECTS AND ADVERSE REACTIONS; METABOLISM; PHYSIOLOGY; TIME; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; BIOLOGICAL TRANSPORT; BLOOD-BRAIN BARRIER; BRAIN; DRUG DELIVERY SYSTEMS; DRUG-RELATED SIDE EFFECTS AND ADVERSE REACTIONS; ENDOCYTOSIS; HUMANS; NANOPARTICLES; POLYMERS; TIME FACTORS; TRANSCYTOSIS;

EID: 84901473966     PISSN: 0169409X     EISSN: 18728294     Source Type: Journal    
DOI: 10.1016/j.addr.2013.08.008     Document Type: Review

References (152)

1. Kreuter J., Alyautdin R.N., Kharkevich D.A., Ivanov A.A. Passage of peptides through the blood-brain barrier with colloidal polymer particles (nanoparticles). Brain Res. 1995, 674:171-174.
2. Kreuter J. Nanoparticulate systems for brain delivery of drugs. Adv. Drug Deliv. Rev. 2001, 47:65-81.
3. Wohlfart S., Gelperina S., Kreuter J. Transport of drugs across the blood-brain barrier by nanoparticles. J. Control. Release 2012, 161:264-273.
4. Kurakhmaeva K.B., Djindjikashvili I.A., Petrov V.E., Balabanyan V.U., Voronina T.A., Trofimov S.S., Kreuter J., Gelperina S., Begley D., Alyautdin R.N. Brain targeting of nerve growth factor using poly(butyl cyanoacrylate) nanoparticles. J. Drug Target 2009, 17:564-574.
5. Patel T., Zhou J., Piepmeier J.M., Saltzman W.M. Polymeric nanoparticles for drug delivery to the central nervous system. Adv. Drug Deliv. Rev. 2012, 54:701-705.
6. Ramge R., Kreuter J., Lemmer B. Circadian phase-dependent antinociceptive reaction in mice after i. v. injection of dalargin-loaded nanoparticles determined by the hot-plate test and the tail-flick test. Chronobiol. Int. 1999, 17:767-777.
7. Steiniger S.C.J., Kreuter J., Khalansky A.S., Skidan I.N., Bobruskin A.I., Smirnova Z.S., Severin S.E., Uhl R., Kock M., Geiger K.D., Gelperina S.E. Chemotherapy of glioblastoma in rats using doxorubicin-loaded nanoparticles. Int. J. Cancer 2004, 109:759-767.
8. Alyautdin R.N., Petrov V.E., Langer K., Berthold A., Kharkevich D.A., Kreuter J. Delivery of loperamide across the blood-brain barrier with poly-sorbate 80-coated polybutylcyanoacrylate nanoparticles. Pharm. Res. 1997, 14:325-328.
9. Kreuter J., Petrov V.E., Kharkevich D.A., Alyautdin R.N. Influence of the type of surfactant on the analgesic effects induced by the peptide dalargin after its delivery across the blood-brain barrier using surfactant-coated nanoparticles. J. Control. Release 1997, 49:81-87.
10. Gelperina S., Maksimenko O., Khalansky A., Vanchugova L., Shipulo E., Abbasova K., Berdiev R., Wohlfart S., Chepurnova N., Kreuter J. Drug delivery to the brain using surfactant-coated poly(lactide-co-glycolide) nanoparticles: Influence of the formulation parameters. Eur. J. Pharm. Biopharm. 2010, 74:157-163.
11. Wohlfart S., Khalansky A.S., Gelperina S., Maksimenko O., Bernreuther C., Glatzel M., Kreuter J. Efficient chemotherapy of rat glioblastoma using doxorubicin-loaded PLGA nanoparticles with different stabilizers. PLoS One 2011, 6:e19121.
12. Michaelis K., Hoffmann M.M., Dreis S., Herbert E., Alyautdin R.N., Michaelis M., Kreuter J., Langer K. Covalent linkage of apolipoprotein E to albumin-nanoparticles strongly enhances drug transport into the brain. J. Pharmacol. Exp. Ther. 2006, 317:1246-1253.
13. Nagpal K., Singh S.K., Mishra D.N. Chitosan nanoparticles: a promising system in novel drug delivery. Chem. Pharm. Bull. 2010, 58:1423-1430.
14. Karatas H., Aktas Y., Gursoy-Ozdemir Y., Bodur E., Yemisci M., Caban S., Vural A., Pinarbasli O., Capan Y., Fernandez-Megia E., Novoa-Carballal R., Riguera R. A nanomedicine transports a peptide caspase-3 inhibitor across the blood-brain barrier and provides neuroprotection. J. Neurosci. 2009, 29:13761-13769.
15. Kreuter J. Nanoparticles. Encyclopedia of Pharmaceutical Technology 1994, vol. 10:165. Marcel Dekker, New York.
16. Kreuter J. Nanoparticles as drug delivery systems. Encyclopedia of Nanoscience and Nanotechnology 2004, vol. 7:161-180. American Scientific Publishers, Stevenson Ranch, U.S.A.
17. Kreuter J. Nanoparticles and nanocapsules - new dosage forms in the nanometer size range. Pharm. Acta Helv. 1978, 53:33-39.
18. Schäfer V., Briesen H.V., Rübsamen-Waigmann H., Steffan A.M., Royer C., Kreuter J. Phagocytosis and degradation of human serum albumin microspheres and nanoparticles in human macrophages. J. Microencapsul. 1994, 11:261-269.
19. Gao K., Jiang X. Influence of particle size on transport of methotrexate across blood brain barrier by polysorbate 80-coated polybutylcyanoacrylate nanoparticles. Int. J. Pharm. 2006, 310:213-219.
20. Yoshioka T., Hashida M., Muranishi S., Sezaki H. Specific delivery of mitomycin C to the liver, spleen and lung: nano- and microsperical carriers of gelatin. Int. J. Pharm. 1981, 8:131-141.
21. Kreuter J. Nanoparticulate systems for brain delivery of drugs. Adv. Drug Deliv. Rev. Suppl. 2012, 64:213-222.
22. Kreuter J. Mechanism of polymeric nanoparticle-based drug transport across the blood-brain barrier (BBB). J. Microencapsul. 2013, 30:49-54.
23. Kreuter J., Ramge P., Petrov V., Hamm S., Gelperina S.E., Engelhardt B., Alyautdin R., von Briesen H., Begley D.J. Direct evidence that polysorbate 80-coated poly(butyl cyanoacrylate) nanoparticles deliver drugs to the CNS via specific mechanisms requiring prior binding of drugs to the nanoparticles. Pharm. Res. 2003, 20:409-416.
24. Olivier J.-C., Fenart L., Chauvet R., Pariat C., Cecchelli R., Couet W. W Indirect evidence that drug brain targeting using polysorbate 80-coated polybutylcyanoacrylate nanoparticles is related to toxicity. Pharm. Res. 1999, 16:1836-1842.
25. Calvo P., Gouritin B., Chacun H., Desmaele D., D'Angelo J., Noel J.-P., Georgin D., Fatal E., Andreux P., Couvreur P. Long-circulating PEGylated polycyanoacrylate nanoparticles as new drug cariers for brain delivery. Pharm. Res. 2001, 18:1157-1166.
26. Zensi A., Begley D., Pontikis C., Legros C., Mihoreanu L., Wagner S., Büchel C., von Briesen H., Kreuter J. Albumin nanoparticles targeted with Apo E enter the CNS by transcytosis and are delivered to neurones. J. Control. Release 2009, 137:78-86.
27. Zensi A., Begley D., Charles Pontikis C., Legros C., Mihoreanu L., Büchel C., Kreuter J. Human serum albumin nanoparticles modified with apolipoprotein A-I cross the blood-brain barrier and enter the rodent brain. J. Drug Target 2010, 18:842-848.
28. Hekmatara T., Bernreuther C., Khalansky A.S., Theisen A., Weissenberger J., Gelperina S., Kreuter J., Glatzel M. Efficient systemic therapy of rat glioblastoma by nanoparticle-bound doxorubicin is due to antiangiogenic effects. Clin. Neuropathol. 2009, 28:153-164.
29. San W., Xie C., Wand H., Hu Y. Specific role of polysorbate 80 coating on the targeting of nanoparticles to the brain. Biomaterials 2004, 25:3065-3071.
30. Koziara M.J., Lockman P.R., Allen D.D., Mumper R.J. In situ blood-brain barrier transport of nanoparticles. Pharm. Res. 2003, 20:1772-1778.
31. Alyautdin R.N., Reichel A., Löbenberg R., Ramge P., Kreuter J., Begley D.J. Interaction of poly(butylcyanoacrylate) nanoparticles with the blood-brain-barrier in vivo and in vitro. J. Drug Target 2001, 9:209-221.
32. Borchard G., Audus K.L., Shi F., Kreuter J. Uptake of surfactant-coated poly(methyl methacrylate)-nanoparticles by bovine brain microvessel endothelial cell monolayers. Int. J. Pharm. 1994, 110:29-35.
33. Ramge P., Unger R.E., Oltrogge J.B., Zenker D., Begley D., Kreuter J., von Briesen H. Polysorbate 80-coating enhances uptake of polybutylcyanoacrylate (PBCA)-nanoparticles by human and bovine primary brain capillary endothelial cells. Eur. J. Neurosci. 2000, 12:1931-1940.
34. Wagner S., Kufleitner J., Zensi A., Dadparvar M., Wien S., Bungert J., Vogel T., Worek F., Kreuter J., von Briesen H. Nanoparticulate transport of oximes over an in vitro blood-brain barrier model. PLoS One 2010, 5:e14213.
35. Hasadsri L., Kreuter J., Hattori H., Iwasaki T., George J.M. Functional protein delivery into neurons using polymeric nanoparticles. J. Biol. Chem. 2009, 284:6972-6981.
36. Sanchez de Juan B., von Briesen H., Gelperina S.E., Kreuter J. Cytotoxicity of doxorubicin bound to poly(butyl cyanoacrylate) nanoparticles in rat glioma cell lines using different assays. J. Drug Target 2006, 14:614-622.
37. Tahara K., Kato Y., Yamamoto H., Kreuter J., Kawashima Y. Intracellular drug delivery using polysorbate 80-modified poly(d,l-lactide-co-glycolide) nanospheres to glioblastoma cells. J. Microencapsul. 2011, 28:29-36.M.
38. Lück M. Plasmaproteinadsorption als möglicher Schlüsselfaktor für eine kontrollierte Arzneistoffapplikation mit partikulären 1997, 14-24. Ph.D. Thesis, Freie Universität, Trägern, Berlin, (137-54).
39. Petri B., Bootz A., Khalansky A., Hekmatara T., Müller R., Uhl R., Kreuter J., Gelperina S. Chemotherapy of brain tumour using doxorubicin bound to surfactant-coated poly(butyl cyanoacrylate) nano-particles: revisiting the role of surfactants. J. Control. Release 2007, 117:51-58.
40. Kreuter J., Shamenkov D., Petrov V., Ramge P., Cychutek K., Koch-Brandt C., Alyautdin R.N. Apolipoprotein-mediated transport of nanoparticle-bound drugs across the blood-brain barrier. J. Drug Target 2002, 10:317-325.
41. Kreuter J., Hekmatara T., Dreis S., Vogel T., Gelperina S., Langer K. Covalent attachment of apolipoprotein A-I and apolipoprotein B-100 to albumin nanoparticles enables drug transport into the brain. J. Control. Release 2007, 118:54-58.
42. Panzenboeck U., Balazs Z., Sovic A., Hrzenjak A., Levak-Frank S., Wintersperger A., Malle E., Sattler W. 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. 2002, 277:42781-42789.
43. Balazs Z., Panzenboeck U., Hammer A., Sovic A., Quehenberger O., Malle E., Sattler W. Uptake and transport of high-density lipoprotein (HDL) and HDL-associated alpha-tocopherol by an in vitro blood-brain barrier model. J. Neurochem. 2004, 89:939-950.
44. Wagner S., Zensi A., Wien S.L., Tschickardt S.E., Maier W., Vogel T., Worek F., Pietrzik C.U., Kreuter J., von Briesen H. Uptake mechanism of apoE-modified nanoparticles on brain capillary endothelial cells as a blood-brain barrier model. PLoS One 2012, 7:e32568.
45. Wolburg H., Wolburg-Buchholz K., Sam H., Horvat S., Deli M.A., Mack A.F. Epithelial and endothelial barriers in the olfactory region of the nasal cavity of the rat. Histochem. Cell Biol. 2008, 130:127-140.
46. Thorne R.G., Nicholson C. In vivo diffusion analysis with quantum dots and dextrans predicts the width of brain extracellular space. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:5567-5572.
47. Begley D.J. Brain superhighways. Sci. Transl. Med. 2012, 4:1-3.
48. Reimold I., Domke D., Bender J., Seyfried C.A., Radunz H.-E., Fricker G. Delivery of nanoparticles to the brain detected by fluorescence microscopy. Eur. J. Pharm. Biopharm. 2008, 70:627-632.
49. Simionescu M., Gafencu A., Antohe F. Transcytosis of plasma macromolecules in endothelial cells: a cell biological survey. Microsc. Res. Tech. 2002, 57:269-288.
50. Simionescu M., Popov D., Sima A. Endothelial transcytosis in health and disease. Cell Tissue Res. 2009, 335:27-40.
51. Borchard G., Brandriss S., Kreuter J., Margel S. Body distribution of 75Se-radiolabeled silica nano-particles covalently coated with ω-functionalized surfactants after intravenous injection in rats. J. Drug Target 1994, 2:61-77.
52. Grislain L., Couvreur P., Lenaerts V., Roland M., Deprez-De Campenere D., Speiser P. Pharmacokinetics and distribution of a biodegradable drug-carrier. Int. J. Pharm. 1983, 15:335-345.
53. 14C]poly(butyl cyanoacrylate) nanoparticles after i.v. administration in rats. J. Drug Target 2005, 13:535-542.
54. 14C]-poly-(butyl cyanoacrylate) nanoparticles after intravenous administration to glioblastoma-bearing rats. J. Drug Target 2006, 14:103-111.
55. El-Egakey M.A., Bentele V., Kreuter J. Molecular weights of polycyanoacrylate nanoparticles. Int. J. Pharm. 1983, 13:349-352.
56. Vansnick L., Couvreur P., Christiaens-Leyh D., Roland M. Molecular weights of free and drug-loaded nanoparticles. Pharm. Res. 1985, 1:36-41.
57. Douglas S.J., Davis S.S., Holding S.R. Molecular weights of poly(butyl 2-cyanoacrylate) produced during nanoparticle formation. Br. Polym. J. 1986, 17:339-342.
58. Lenaerts V., Couvreur P., Christiaens-Leyh D., Joiris E., Rolland M., Rollman R., Speiser P. Degradation of poly(isobutyl cyanoacrylate) nanoparticles. Biomaterials 1985, 5:65-68.
59. Scherer D., Robinson J.R., Kreuter J. Influence of enzymes on the stability of polybutylcyanoacrylate nanoparticles. Int. J. Pharm. 1994, 101:165-168.
60. Lherm C.L., Müller R.H., Puisieux F., Couvreur P. Alkylcyanoacrylate drug carriers: II. Cytotoxicity of cyanoacrylate nanoparticles with different alkyl chain length. Int. J. Pharm. 1992, 84:13-22.
61. Efficacy and Safety Doxorubicin Transdrug Study in Patients Suffering From Advanced Hepatocellular Carcinoma (ReLive) 2012, (clinicaltrials.gov/show/NCT01655693).
62. Landry F.B., Bazile D.V., Spenlehauer G., Veillard M., Kreuter J. Degradation of poly(d,l-lactic acid) nanoparticles coated with albumin in model digestive fluids (USP XXII). Biomaterials 1996, 17:715-723.
63. Gref R., Minamitake Y., Peracchia M.T., Trubetskoy V., Torchilin V., Langer R. Biodegradable long-circulating polymeric particles. Science 1994, 263:1600-1603.
64. Bazile D., Prud'Homme C., Bassoullet M.-T., Marlard M., Spenlehauer G., Veillard M. Stealth Me.PEG-PLA nanoparticles avoid uptake by the mononuclear phagocytes system. J. Pharm. Sci. 1995, 84:493-498.
65. Illum L., Davis S.S., Müller R.H., Mak E., West P. The organ distribution and circulation time of intravenously injected colloidal carriers sterically stabilized with a blockcopolymer - poloxamine 908. Life Sci. 1987, 40:367-374.
66. Tröster S.D., Müller U., Kreuter J. Modification of the body distribution of poly(methyl methacrylate) nanoparticles in rats by coating with surfactants. Int. J. Pharm. 1990, 61:85-100.
67. 14C-poly(methyl methacrylate) nano-particles. J. Microencapsul. 1992, 9:19-28.
68. Araujo L., Löbenberg R., Kreuter J. Influence of the surfactant concentration on the body distribution of nanoparticles. J. Drug Target 1999, 5:373-385.
69. Brigger I., Morizet J., Aubert G., Chacun H., Terrier-Lacombe M.-J., Couvreur P., Vassal G. Poly(ethylene glycol)-coated hexadecylcyanoacrylate nanospheres display a combined effect for brain tumor targeting. J. Pharmacol. Exp. Ther. 2002, 303:928-936.
70. Brigger I., Morizet J., Laudani L., Aubert G., Appel M., Velasco V., Terrier-Lacombe M.-J., Desmaele D., d'Angelo J., Couvreur P., Vassal G. Negative preclinical results with stealth® nanosphere-encapsulated doxorubicin in an orthotropic murine brain tumor model. J. Control. Release 2004, 100:29-40.
71. Ambruosi A., Gelperina S., Khalansky A.S., Tanski S., Theisen A., Kreuter J. Influence of surfactants, polymer, and doxorubicin loading on the anti-tumour effect of poly(butyl cyanoacrylate) nanoparticles in a rat glioma model. J. Microencapsul. 2006, 23:582-592.
72. Huang M., Wu W., Qian J., Wan D.J., Wei X.L., Zhu J.H. Body distribution and in situ evading of phagocytic uptake by macrophages of long-circulating poly (ethylene glycol) cyanoacrylate-co-n-hexadecyl cyanoacrylate nanoparticles. Acta Pharmacol. Sin. 2005, 26:1512-1518.
73. Kulkarni S.A., Feng S.-S. Effects of surface modification on delivery efficiency of biodegradable nanoparticles across the blood-brain barrier. Nanomedicine 2011, 6:377-394.
74. Begley D.J. The blood-brain barrier: principles for targeting peptides and drugs to the central nervous system. J. Pharm. Pharmacol. 1996, 48:136-146.
75. Begley D.J. Understanding and circumventing the blood-brain barrier. Acta Paediatr. Suppl. 2003, 92:83-91.
76. Begley D.J. Delivery of therapeutic agents to the central nervous system: the problems and the possibilities. Pharmacol. Ther. 2004, 104:29-45.
77. Bickel U., Yoshikawa T., Landaw E.M., Faull K.F., Pardridge W.M. Pharmacologic effects in vivo in brain by vector-mediated peptide drug delivery. Proc. Natl. Acad. Sci. U. S. A. 1993, 90:2618-2622.
78. Bickel U., Yoshikawa T., Pardridge W.M. Delivery of peptides and proteins through the blood-brain barrier. Adv. Drug Deliv. Rev. 1993, 10:205-245.
79. Pardridge W.M., Boado R.J. Reengineering biopharmaceuticals for targeted delivery across the blood-brain barrier. Methods Enzymol. 2012, 503:269-292.
80. Ulbrich K., Hekmatara T., Herbert E., Kreuter J. Transferrin- and transferrin-receptor-antibody-modified nanoparticles enable drug delivery across the blood-brain barrier (BBB). Eur. J. Pharm. Biopharm. 2009, 71:251-256.
81. Chang J., Paillard A., Passirani C., Morille M., Benoit J.-P., Betbeder D., Garcion E. Transferrin adsorption onto PLGA nanoparticles governs their interaction with biological systems from blood circulation to brain cancer cells. Pharm. Res. 2012, 29:1495-1505.
82. Ulbrich K., Knobloch T., Kreuter J. Targeting the insulin receptor: nanoparticles for drug delivery across the blood-brain barrier (BBB). J. Drug Target 2011, 19:125-132.
83. Gabathuler R. Approaches to transport therapeutic drugs across the blood-brain barrier to treat brain diseases. Neurobiol. Dis. 2010, 37:48-57.
84. Costantino L., Gandolfi F., Tosi G., Rivasi F., Vandelli M.A., Forni F. Peptide-derivatized biodegradable nanoparticles able to cross the blood-brain barrier. J. Control. Release 2005, 108:84-96.
85. Xin H., Sha X., Jiang X., Zhang W., Chen L., Fang X. Anti-glioblastoma efficacy and safety of paclitaxel-loading Angiopep-conjugated dual targeting PEG-PCL nanoparticles. Biomaterials 2012, 33:8167-8176.
86. Tosi G., Costantino L., Rivasi F., Ruozi B., Leo E., Vergoni A.V., Tacchi R., Bertolini A., Vandelli M.A., Forni F. Targeting the central nervous system: In vivo experiments with peptide-derivatized nanoparticles loaded with loperamide and rhodamine-123. J. Control. Release 2007, 122:1-9.
87. Tosi G., Badiali L., Ruozi B., Vergoni A.V., Bondioli L., Ferrari A., Rivasi F., Forni F., Randelli M.A. Can leptin-derived sequence-modified nanoparticles be suitable tools for brain delivery?. Nanomedicine 2012, 7:365-382.
88. Prades R., Guerrero S., Araya E., Molina C., Salas E., Zurita E., Selva J., Egea G., López-Iglesias C., Teixidó M., Kogan M.J., Giralt E. Delivery of gold nanoparticles to the brain by conjugation with a peptide that recognizes the transferrin receptor. Biomaterials 2012, 33:7194-7205.
89. van Rooy I., Cakir-Tascioglu S., Hennink W.E., Storm G., Schiffelers R.M., Mastrobattista E. In vivo methods to study uptake of nanoparticles into the brain. Pharm. Res. 2011, 28:456-471.
90. Wohlfart S., Khalansky A.S., Gelperina S., Begley D., Kreuter J. Kinetics of transport of doxorubicin bound to nanoparticles across the blood-brain barrier. J. Control. Release 2011, 154:103-107.
91. Maincent P., Thouvenot P., Amicabile C., Hoffmann M., Kreuter J., Couvreur P., Devissaguet J.P. Lymphatic targeting of polymeric nanoparticles after intraperitoneal administration in rats. Pharm. Res. 1992, 9:1534-1539.
92. Geldenhuys W., Mbimba T., Bui T., Harrison K., Sutariya V. Brain-targeted delivery of paclitaxel using glutathione-coated nanoparticles for brain cancers. J. Drug Target 2011, 19:837-845.
93. Kreuter J. Solid dispersion and solid solution. Topics in Pharmaceutical Sciences 1983 1983, 359-370. Elsevier, Amsterdam, New York, Oxford. D.D. Breimer, P. Speiser (Eds.).
94. Ren T., Xu N., Cao C., Yuan W., Yu X., Chen J., Ren J. Preparation and therapeutic efficacy of polysorbate-80-coated amphotericin nanoparticles. J. Biomater. Sci. 2009, 20:1369-1380.
95. Han L., Ren Y., Long L., Zhong Y., Shen C., Pu P., Yuan X., Kang C. Inhibition of C6 glioma in vivo by combination chemotherapy of implantation of polymer wafer and intracarotid perfusion of transferrin-decorated nanoparticles. Oncol. Rep. 2012, 27:121-128.
96. Liu M., Li H., Luo G., Liu Q., Wang Y. Pharmacokinetics and biodistribution of surface modification polymeric nanoparticles. Arch. Pharm. Res. 2008, 31:547-554.
97. Çirpanli Y., Allard E., Passirani C., Bilensoy E., Lemaire L., Çaliş S., Benoit J.-P. Antitumoral activity of camptothecin-loaded nanoparticles in 9L rat glioma model. Int. J. Pharm. 2011, 403:201-206.
98. Chen Y.-C., Hsieh W.-Y., Lee W.-F., Zeng D.-T. Effects of surface modification of PLGA-PEG-PLGA nanoparticles on loperamide delivery efficiency across the blood-brain barrier. J. Biomater. Appl. 2013, 27:909-922.
99. Li J., Feng L., Fan L., Zha Y., Guo L., Zhang Q., Chen J., Pang Z., Wang Y., Jiang X., Yang V.C., Wen L. Targeting the brain with PEG-PLGA nanoparticles modified with phage-displayed peptides. Biomaterials 2011, 32:4943-4950.
100. Kim D.H., Martin D.C. Sustained release of dexamethasone from hydrophilic matrices using PLGA nanoparticles for neural drug delivery. Biomaterials 2006, 27:3031-3037.
101. Trapani A., Di Giglio E., Cafagna D., Denora N., Agrimi G., Cassano T., Gaetani S., Cuomo V., Trapani G. Characterisation and evaluation of chitosan nanoparticles for dopamine brain delivery. Int. J. Pharm. 2011, 419:296-307.
102. Gulyaev A.E., Gelperina S.E., Skidan I.N., Antropov A.S., Kivman G.Y., Kreuter J. Significant transport of doxorubicin into the brain with polysorbate 80-coated nanoparticles. Pharm. Res. 1999, 16:1564-1569.
103. Liu H., Ni J., Wang R. In vitro release performance and analgesic activity of endomorphin-1 loaded nanoparticles. Pharmazie 2006, 61:450-452.
104. Wang C.X., Huang L.S., Hou L.B., Jiang L., Yan Z.T., Wang Y.L., Chen Z.L. Antitumor effects of polysorbate-80 coated gemcitabine polybutylcyanoacrylate nanoparticles in vitro and its pharmacodynamics in vivo on C6 glioma cells of a brain tumor model. Brain Res. 2009, 1261:91-99.
105. Lin Y., Pan Y., Shi Y., Huang X., Jia N., Jiang J.Y. Delivery of large molecules via poly(butyl cyanoacrylate) nanoparticles into the injured rat brain. Nanotechnology 2012, 23:e165101.
106. Schroeder U., Sommerfeld P., Ulrich S., Sabel B.A. Nanoparticle technology for delivery of drugs across the blood-brain barrier. J. Pharm. Sci. 1998, 87:1305-1307.
107. Trapani A., Denora N., Iacobellis G., Sitterberg J., Bakowsky U., Kissel T. Methotrexate-loaded chitosan- and glycolchitosan-based nanoparticles: a promising strategy for the administration of the anticancer drug to brain tumors. AAPS Pharm. Sci. Technol. 2011, 12:1302-1311.
108. Friese A., Seiller E., Quack G., Lorenz B., Kreuter J. Increase of the duration of the anticonvulsive activity of a novel NMDA receptor antagonist using poly(butylcyanoacrylate) nanoparticles as a parenteral controlled release system. Eur. J. Pharm. Biopharm. 2000, 49:103-109.
109. Tosi G., Fano R.A., Bondioli L., Badiali L., Benassi R., Rivasi F., Ruozi B., Forni F., Vandelli M.A. Investigation on mechanism of glycopeptide nanoparticles for drug delivery across the blood-brain barrier. Nanomedicine 2011, 6:423-436.
110. Xin H.L., Jiang X.Y., Gu J.J., Sha X.Y., Chen L.C., Law K., Chen K.Y., Wang X., Jiang Y., Fang X. Angiopep-conjugated poly(ethylene glycol)-co-poly(ε-caprolactone) nanoparticles as dual-targeted drug delivery system for brain glioma. Biomaterials 2011, 32:4293-4305.
111. Guo J., Gao X., Su L., Xia H., Gu G., Pang Z., Jiang X., Yao L., Chen J., Chen H. Aptamer-functionalised PEG-PLGA nanoparticles for enhanced anti-glioma drug delivery. Biomaterials 2011, 32:8010-8020.
112. Xin H., Chen L., Gu J., Ren X., Wei Z., Luo J., Chen Y., Jiang X., Sha X., Fang X. Enhanced anti-glioblastoma efficacy by PTX-loaded PEGylated poly(ε-caprolactone) nanoparticles: in vitro and in vivo evaluation. Int. J. Pharm. 2010, 402:238-247.
113. Wilson B., Samanta M.K., Santhi K., Kumar K.P., Paramakrishnan N., Suresh B. Poly(n-butylcyanoacrylate) nanoparticles coated with polysorbate 80 for the targeted delivery of rivastigmine into the brain to treat Alzheimer's disease. Brain Res. 2008, 1200:159-168.
114. Wilson B., Samanta M.K., Muthu M.S., Vinothapooshan G. Design and evaluation of chitosan nanoparticles as novel drug carrier for the delivery of rivastigmine to treat Alzheimer's disease. Ther. Deliv. 2011, 2:599-609.
115. Rao K.S., Reddy M.K., Horning J.L., Labhasetwar V. TAT-conjugated nanoparticles for the CNS delivery of anti-HIV drugs. Biomaterials 2008, 29:4429-4438.
116. Kuo Y.C., Su F.L. Transport of stavudine, delavirdine, and saquinavir across the blood-brain barrier by polybutylcyanoacrylate, methylmethacrylate-sulfopropylmethacrylate, and solid lipid nanoparticles. Int. J. Pharm. 2007, 340:143-152.
117. Parikh T., Bommana M.M., Squillante E. Efficacy of surface charge in targeting pegylated nanoparticles of sulpiride to the brain. Eur. J. Pharm. Biopharm. 2010, 74:442-450.
118. Reddy M.K., Labhasetwar V. Nanoparticle-mediated delivery of superoxide dismutase to the brain: an effective strategy to reduce ischemia-reperfusion injury. FASEB J. 2009, 23:1384-1395.
119. Wilson B., Samanta M.K., Santhi K., Kumar K.P., Paramakrishnan N., Suresh B. Targeted delivery of tacrine into the brain with polysorbate 80-coated poly(n-butylcyanoacrylate) nanoparticles. Eur. J. Pharm. Biopharm. 2008, 70:75-84.
120. Wilson B., Samanta M.K., Santhi K., Kumar K.P.S., Ramasamy M., Suresh B. Chitosan nanoparticles as a new delivery system for the anti-Alzheimer drug tacrine. Nanomedicine 2011, 6:144-152.
121. Tian X., Lin X., Wei F., Feng W., Huang Z., Ren L., Diao Y. Enhanced brain targeting of temozolomide in polysorbate-80 coated polybutylcyanoacrylate nanoparticles. Int. J. Nanomedicine 2011, 6:445-452.
122. Alyautdin R.N., Tezikov E.B., Ramge P., Kharkevich D.A., Begley D.J., Kreuter J. Significant entry of tubocurarine into the brain of rats by adsorption to polysorbate 80-coated polybutylcyanoacrylate nanoparticles: an in situ brain perfusion study. J. Microencapsul. 1998, 15:67-74.
123. Schneider T., Becker A., Ringe K., Reinhold A., Firsching R., Sabel B.A. Brain tumor therapy by combined vaccination and antisense oligonucleotide delivery with nanoparticles. J. Neuroimmunol. 2008, 195:21-27.
124. Darius J., Meyer F.P., Sabel B.A., Schroeder U. Influence of nanoparticles on the brain-to-serum distribution and the metabolism of valproic acid in mice. J. Pharm. Pharmacol. 2000, 52:1043-1047.
125. Donelli M.G., Zucchetti M., D'Incalci M. Do anticancer agents reach the tumor target in the human brain?. Cancer Chemother. Pharmacol. 1992, 30:251-260.
126. Kreuter J. Nanoparticulate carriers for drug delivery to the brain. Nanoparticles as Drug Carriers 2006, 527-547. Imperial College Press, London. V.P. Torchilin (Ed.).
127. Maeda H. Tumor-selective delivery of macromolecular drugs via the EPR effect: background and future prospects. Bioconjug. Chem. 2010, 21:797-802.
128. Huynh N.T., Morille M., Bejaud J., Legras P., Vessieres A., Jaouen G., Benoit J.-P., Passirani C. Treatment of 9L gliosarcoma in rats by ferrociphenol-loaded lipid nanocapsules based on a passive targeting strategy via the EPR effect. Pharm. Res. 2011, 3189-3198.
129. Garcia-Garcia E., Andrieux K., Gil S., Couvreur P. Colloidal carriers and blood-brain barrier (BBB) translocation: a way to deliver drugs to the brain?. Int. J. Pharm. 2005, 298:274-292.
130. Wohlfart S., Bernreuther C., Khalansky A.S., Theisen A., Weissenberger J., Gelperina S., Glatzel M., Kreuter J. Increased numbers of injections of doxorubicin bound to nanoparticles lead to enhanced efficacy against rat glioblastoma 101/8. J. Nanoneurosci. 2009, 1:144-151.
131. Bobo R.H., Laske D.W., Akbasak A., Morrison P.F., Dedrick R.L., Oldfield E.H. Convection-enhanced delivery of macromolecules in the brain. Proc. Natl. Acad. Sci. U. S. A. 1994, 91:2076-2080.
132. Roney C., Kulkarni P., Arora V., Antich P., Bonte F., Wu A., Mallikarjuana N.N., Manohar S., Liang H.F., Kulkarni A.R., Sung H.W., Sairam M., Aminabhavi T.M. Targeted nanoparticles for drug delivery through the blood-brain barrier for Alzheimer's disease. J. Control. Release 2005, 108:193-214.
133. Andrieux K., Couvreur P. Nanomedicine as a promising approach for the treatment and diagnosis of brain diseases: the example of Alzheimer's disease. Ann. Pharm. Fr. 2013, 71:225-233.
134. Wilson B., Samanta M.K., Santhi K., Sampath Kumar K.P., Ramasamy M., Suresh B. Significant delivery of tacrine into the brain using magnetic chitosan microparticles for treating Alzheimer's disease. J. Neurosci. Methods 2009, 177:427-433.
135. Kulkarni P.V., Roney C.A., Antich P.P., Bonte F.J., Raghu A.V., Aminabhavi T.M. Quinoline-n-butylcyanoacrylate-based nanoparticles for brain targeting for the diagnosis of Alzheimer's disease. Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol. 2010, 2:35-47.
136. Yusuf M., Khan M., Khan R.A., Ahmed B. Preparation, characterization, in vivo and biochemical evaluation of brain targeted piperine solid lipid nanoparticles in an experimentally induced Alzheimer's disease model. J. Drug Target 2013, 21:300-311.
137. Mathew A., Fukuda T., Nagaoka Y., Hasumura T., Morimoto H., Yoshida Y., Maekawa T., Venugopal K., Kumar D.S. Curcumin loaded-PLGA nanoparticles conjugated with Tet-1 peptide for potential use in Alzheimer's disease. PLoS One 2012, 7:e32616.
138. Brasnjevic I., Steinbusch H.W.M., Schmitz C., Martinez-Martinez P. Delivery of peptide and protein drugs over the blood-brain barrier. Prog. Neurobiol. 2009, 87:212-251.
139. Yang C.S., Chang C.H., Tsai P.J., Chen W.Y., Tseng F.G., Lo L.W. Nanoparticle-based in vivo investigation on blood-brain barrier permeability following ischemia and reperfusion. Anal. Chem. 2004, 76:4465-4471.
140. Gelperina S.E., Khalansky A.S., Skidan I.N., Smirnova Z.S., Bobruskin A.I., Severin S.E., Turowski B., Zanella F., Kreuter J. Toxicological studies of doxorubicin bound to polysorbate 80-coated poly(butyl cyanoacrylate) nanoparticles in healthy rats and rats with intracranial glioblastoma. Toxicol. Lett. 2002, 126:131-141.
141. Pereverzeva E., Treschalin I., Bodyagin D., Maksimenko O., Langer K., Dreis S., Asmussen B., Kreuter J., Gelperina S. Influence of the formulation on the tolerance profile of nanoparticle-bound doxorubicin in healthy rats: focus on cardio- and testicular toxicity. Int. J. Pharm. 2007, 337:346-356.
142. Pereverzeva E., Treschalin I., Bodyagin D., Maksimenko O., Kreuter J., Gelperina S. Intravenous tolerance of a nanoparticle-based formulation of doxorubicin in healthy rats. Toxicol. Lett. 2008, 178:9-19.
143. Diehl K.-H., Hull R., Morton D., Pfister R., Rabemampianina Y., Smith D., Vidal J.-M., van de Vorstenbosch C. A good practice guide to the administration of substances and removal of blood, including routes and volumes. J. Appl. Toxicol. 2001, 21:15-23.
144. Couvreur P., Kante B., Grislain L., Roland M., Speiser P. Toxicity of polyalkylcyanoacrylate nanoparticles II: doxorubicin-loaded nanoparticles. J. Pharm. Sci. 1982, 71:790-792.
145. Couvreur P., Grislain L., Lenaerts V., Brasseur F., Guiot P., Biernacki A. A, Biodegradable polymeric nanoparticles as drug carrier for antitumor agents. Polymeric Nanoparticles and Microspheres 1986, 27-93. CRC Press, Boca Raton, FL. P. Guiot, P. Couvreur (Eds.).
146. Bawa R. FDA and nanotech: baby steps lead to regulatory uncertainty. Bio-Nanotechnology: A Revolution in Food, Biomedical and Health Sciences 2013, 720-732. Wiley, Bognor Regis, UK. 1st ed. D. Bagchi, M. Bagchi, H. Moriyama, F. Shahidi (Eds.).
147. Wohlfart S., Khalansky A.S., Bernreuther C., Michaelis M., Cinatl J., Glatzel M., Kreuter J. Treatment of glioblastoma with poly(isohexyl cyanoacrylate) nanoparticles. Int. J. Pharm. 2011, 415:244-251.
148. 3HH-labelled dalargin bound to poly(butyl cyanoacrylate) nanoparticles after I.V. injections to mice. Life Sci. 2000, 66:495-502.
149. Kreuter J. Nanoparticles. Colloidal Drug Delivery Systems 1994, 307-308. Marcel Dekker, New York. J. Kreuter (Ed.).
150. Bender A., Schäfer V., Steffan A.M., Royer C., Kreuter J., Rübsamen-Waigmann H., Briesen H.V. Inhibition of HIV in vitro by antiviral drug-targeting using nanoparticles. Res. Virol. 1994, 145:215-220.
151. Löbenberg R., Kreuter J. Macrophage targeting of azidothymidine: a promising strategy for AIDS therapy. AIDS Res. Hum. Retroviruses 1996, 12:1709-1715.
152. Petkov V.D., Mosharrof A.H., Petkov V.V. Comparative studies on the effects of the nootropic drugs adafenoxate, meclofenoxate and piracetam, and of citicholine on scopolamine-impaired memory, exploratory behavior and physical capabilities (experiments on rats and mice). Acta Physiol. Pharmacol. Bulg. 1988, 14:3-13.