Nose-to-brain drug delivery by nanoparticles in the treatment of neurological disorders

Current Medicinal Chemistry

Volumn 21, Issue 37, 2014, Pages 4247-4256

  Ong, Wei Yi ^a,b   Shalini, Suku Maran ^a   Costantino, Luca ^c  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

Author keywords

Blood brain barrier (BBB); Nanomedicine; Nanoparticles; Neurological disorders; Nose to brain; Olfactory nerve

Indexed keywords

CHITOSAN; CLATHRIN; MACROGOL; NANOPARTICLE; POLYLACTIC ACID; DRUG; DRUG CARRIER;

ARTICLE; BLOOD BRAIN BARRIER; BRAIN CANCER; BRAIN REGION; CENTRAL NERVOUS SYSTEM; CEREBROVASCULAR ACCIDENT; DEGENERATIVE DISEASE; DRUG DELIVERY SYSTEM; DRUG FORMULATION; DRUG SAFETY; DRUG SOLUTION; EPILEPSY; GEL; HUMAN; INFECTION; MOLECULAR WEIGHT; MUCOADHESION; NEUROLOGIC DISEASE; NONHUMAN; NOSE MUCOSA; PAIN; SAFETY; TRAUMATIC BRAIN INJURY; ANIMAL; BRAIN; CHEMISTRY; METABOLISM; NERVOUS SYSTEM DISEASES; NOSE;

ANIMALS; BRAIN; DRUG CARRIERS; HUMANS; NANOPARTICLES; NERVOUS SYSTEM DISEASES; NOSE; PHARMACEUTICAL PREPARATIONS;

EID: 84921438595     PISSN: 09298673     EISSN: 1875533X     Source Type: Journal    
DOI: 10.2174/0929867321666140716103130     Document Type: Article

References (118)

1. Schulze, C.; Firth, J. A. Immunohistochemical localization of adherens junction components in blood-brain barrier microvessels of the rat. J. Cell Sci., 1993, 104(Pt 3), 773-782.
2. Pardridge, W. M. The blood-brain barrier: bottleneck in brain drug development. NeuroRx, 2005, 2(1), 3-14.
3. Pardridge, W. M. Blood-brain barrier biology and methodology. J. Neurovirol., 1999, 5(6), 556-569.
4. Pardridge, W. M. Blood-brain barrier drug targeting: the future of brain drug development. Mol. Interv., 2003, 3(2), 90-105, 151.
5. Banks, W. A. Delivery of peptides to the brain: emphasis on therapeutic development. Biopolymers, 2008, 90(5), 589-594.
6. Fisher, R. S.; Chen, D. K. New routes for delivery of anti-epileptic medications. Acta Neurologica Taiwanica, 2006, 15(4), 225-231.
7. Frey, W. H. Neurologic Agents for Nasal Administration to the Brain. 1991.
8. Seju, U.; Kumar, A.; Sawant, K. K. Development and evaluation of olanzapine-loaded PLGA nanoparticles for nose-to-brain delivery: in vitro and in vivo studies. Acta Biomaterialia, 2011, 7(12), 4169-4176.
9. Salama, H. A.; Mahmoud, A. A.; Kamel, A. O.; Abdel Hady, M.; Awad, G. A. Brain delivery of olanzapine by intranasal administration of transfersomal vesicles. J. Liposome Res., 2012, 22(4), 336-345.
10. Salama, H. A.; Mahmoud, A. A.; Kamel, A. O.; Abdel Hady, M.; Awad, G. A. Phospholipid based colloidal poloxamer-nanocubic vesicles for brain targeting via the nasal route. Colloids Surf B Biointerfaces., 2012, 100, 146-154.
11. Yang, Z. Z.; Zhang, Y. Q.; Wang, Z. Z.; Wu, K.; Lou, J. N.; Qi, X. R. Enhanced brain distribution and pharmacodynamics of rivastigmine by liposomes following intranasal administration. Int. J. Pharm., 2013, 452(1-2), 344-354.
12. Migliore, M. M.; Vyas, T. K.; Campbell, R. B.; Amiji, M. M.; Waszczak, B. L. Brain delivery of proteins by the intranasal route of administration: a comparison of cationic liposomes versus aqueous solution formulations. J. Pharm. Sci., 2010, 99(4), 1745-1761.
13. Arumugam, K.; Subramanian, G. S.; Mallayasamy, S. R.; Averineni, R. K.; Reddy, M. S.; Udupa, N. A study of rivastigmine liposomes for delivery into the brain through intranasal route. Acta Pharmaceutica, 2008, 58(3), 287-297.
14. Kumar, M.; Misra, A.; Mishra, A. K.; Mishra, P.; Pathak, K. Mucoadhesive nanoemulsion-based intranasal drug delivery system of olanzapine for brain targeting. J. Drug Target., 2008, 16(10), 806-814.
15. Dhuria, S. V.; Hanson, L. R.; Frey, W. H. 2nd, Intranasal delivery to the central nervous system: mechanisms and experimental considerations. J. Pharm. Sci., 2010, 99(4), 1654-1673.
16. Trapani, A.; De Giglio, E.; Cafagna, D.; Denora, N.; Agrimi, G.; Cassano, T.; Gaetani, S.; Cuomo, V.; Trapani, G. Characterization and evaluation of chitosan nanoparticles for dopamine brain delivery. Int. J. Pharm., 2011, 419(1-2), 296-307.
17. Abdelbary, G. A.; Tadros, M. I. Brain targeting of olanzapine via intranasal delivery of core-shell difunctional block copolymer mixed nanomicellar carriers: in vitro characterization, ex vivo estimation of nasal toxicity and in vivo biodistribution studies. Int. J. Pharm., 2013, 452(1-2), 300-310.
18. Md, S.; Khan, R. A.; Mustafa, G.; Chuttani, K.; Baboota, S.; Sahni, J. K.; Ali, J. Bromocriptine loaded chitosan nanoparticles intended for direct nose to brain delivery: Pharmacodynamic, Pharmacokinetic and Scintigraphy study in mice model. Eur. J. Pharm. Sci., 2012, 48(3), 393-405.
19. Patel, S.; Chavhan, S.; Soni, H.; Babbar, A. K.; Mathur, R.; Mishra, A. K.; Sawant, K. Brain targeting of risperidone-loaded solid lipid nanoparticles by intranasal route. J. Drug Target., 2011, 19(6), 468-474.
20. Jain, K.; Sood, S.; Gowthamarajan, K. Optimization of artemetherloaded NLC for intranasal delivery using central composite design. Drug Deliv., 2014(0), 1-15.
21. Pardeshi, C. V.; Rajput, P. V.; Belgamwar, V. S.; Tekade, A. R.; Surana, S. J. Novel surface modified solid lipid nanoparticles as intranasal carriers for ropinirole hydrochloride: application of factorial design approach. Drug Deliv., 2013, 20(1), 47-56.
22. Haque, S.; Md, S.; Sahni, J. K.; Ali, J.; Baboota, S. Development and evaluation of brain targeted intranasal alginate nanoparticles for treatment of depression. J. Psychiatr. Res., 2014, 48(1), 1-12.
23. Haque, S.; Md, S.; Fazil, M.; Kumar, M.; Sahni, J. K.; Ali, J.; Baboota, S. Venlafaxine loaded chitosan NPs for brain targeting: Pharmacokinetic and pharmacodynamic evaluation. Carbohydr. Polym., 2012, 89(1), 72-79.
24. Fazil, M.; Md, S.; Haque, S.; Kumar, M.; Baboota, S.; Sahni, J. K.; Ali, J. Development and evaluation of rivastigmine loaded chitosan nanoparticles for brain targeting. Eur. J. Pharm. Sci., 2012, 47(1), 6-15.
25. Piazza, J.; Hoare, T.; Molinaro, L.; Terpstra, K.; Bhandari, J.; Selvaganapathy, P. R.; Gupta, B.; Mishra, R. K. Haloperidol-loaded Intranasally administered lectin functionalized poly (ethylene glycol)-block-poly (d, l)-lactic-co-glycolic acid (PEG-PLGA) nanoparticles for the treatment of schizophrenia. Eur. J. Pharm. Biopharm., 2014, 87(1), 30-9.
26. Kumar, M.; Pandey, R. S.; Patra, K. C.; Jain, S. K.; Soni, M. L.; Dangi, J. S.; Madan, J. Evaluation of neuropeptide loaded trimethyl chitosan nanoparticles for nose to brain delivery. Int. J. Biol. Macromol., 2013, 61, 189-195.
27. Wen, Z.; Yan, Z.; Hu, K.; Pang, Z.; Cheng, X.; Guo, L.; Zhang, Q.; Jiang, X.; Fang, L.; Lai, R. Odorranalectin-conjugated nanoparticles: preparation, brain delivery and pharmacodynamic study on Parkinson's disease following intranasal administration. J. Control. Rel., 2011, 151(2), 131-138.
28. Wang, X.; Chi, N.; Tang, X. Preparation of estradiol chitosan nanoparticles for improving nasal absorption and brain targeting. Eur. J. Pharm. Biopharm., 2008, 70(3), 735-740.
29. Hans, M.; Lowman, A. Biodegradable nanoparticles for drug delivery and targeting. Curr. Opin. Solid State Mater. Sci., 2002, 6(4), 319-327.
30. Alcantar, N. A.; Aydil, E. S.; Israelachvili, J. N. Polyethylene glycolcoated biocompatible surfaces. J. Biomed. Mater. Res., 2000, 51(3), 343-351.
31. Cheng, Y.; A, C. S.; Meyers, J. D.; Panagopoulos, I.; Fei, B.; Burda, C. Highly efficient drug delivery with gold nanoparticle vectors for in vivo photodynamic therapy of cancer. J. Am. Chem. Soc., 2008, 130(32), 10643-10647.
32. Kim, C. K.; Ghosh, P.; Pagliuca, C.; Zhu, Z. J.; Menichetti, S.; Rotello, V. M. Entrapment of hydrophobic drugs in nanoparticle monolayers with efficient release into cancer cells. J. Am. Chem. Soc., 2009, 131(4), 1360-1361.
33. Onishi, H.; Machida, Y. Biodegradation and distribution of watersoluble chitosan in mice. Biomaterials, 1999, 20(2), 175-182.
34. Tan, W. B.; Zhang, Y. Surface modification of gold and quantum dot nanoparticles with chitosan for bioapplications. J. Biomed. Mater. Res. Part A, 2005, 75(1), 56-62.
35. Kumar, M.; Pathak, K.; Misra, A. Formulation and characterization of nanoemulsion-based drug delivery system of risperidone. Drug Dev. Ind. Pharm., 2009, 35(4), 387-395.
36. Gavini, E.; Rassu, G.; Haukvik, T.; Lanni, C.; Racchi, M.; Giunchedi, P. Mucoadhesive microspheres for nasal administration of cyclodextrins. J. Drug Target., 2009, 17(2), 168-179.
37. Dalpiaz, A.; Gavini, E.; Colombo, G.; Russo, P.; Bortolotti, F.; Ferraro, L.; Tanganelli, S.; Scatturin, A.; Menegatti, E.; Giunchedi, P. Brain uptake of an anti-ischemic agent by nasal administration of microparticles. J. Pharm. Sci., 2008, 97(11), 4889-4903.
38. Gao, X.; Tao, W.; Lu, W.; Zhang, Q.; Zhang, Y.; Jiang, X.; Fu, S. Lectin-conjugated PEG-PLA nanoparticles: preparation and brain delivery after intranasal administration. Biomaterials, 2006, 27(18), 3482-3490.
39. Gao, X.; Wu, B.; Zhang, Q.; Chen, J.; Zhu, J.; Zhang, W.; Rong, Z.; Chen, H.; Jiang, X. Brain delivery of vasoactive intestinal peptide enhanced with the nanoparticles conjugated with wheat germ agglutinin following intranasal administration. J. Control. Rel., 2007, 121(3), 156-167.
40. Kirby, B. P.; Pabari, R.; Chen, C. N.; Al Baharna, M.; Walsh, J.; Ramtoola, Z. Comparative evaluation of the degree of pegylation of poly (lactic-co-glycolic acid) nanoparticles in enhancing central nervous system delivery of loperamide. J. Pharm. Pharmacol., 2013, 65(10), 1473-1481.
41. Gao, X.; Chen, J.; Tao, W.; Zhu, J.; Zhang, Q.; Chen, H.; Jiang, X. UEA I-bearing nanoparticles for brain delivery following intranasal administration. Int. J. Pharm., 2007, 340(1-2), 207-215.
42. Kumar, M.; Misra, A.; Babbar, A. K.; Mishra, A. K.; Mishra, P.; Pathak, K. Intranasal nanoemulsion based brain targeting drug delivery system of risperidone. Int. J. Pharm., 2008, 358(1-2), 285-291.
43. Xia, H.; Gao, X.; Gu, G.; Liu, Z.; Zeng, N.; Hu, Q.; Song, Q.; Yao, L.; Pang, Z.; Jiang, X.; Chen, J.; Chen, H. Low molecular weight protamine-functionalized nanoparticles for drug delivery to the brain after intranasal administration. Biomaterials, 2011, 32(36), 9888-9898.
44. Liu, Z.; Jiang, M.; Kang, T.; Miao, D.; Gu, G.; Song, Q.; Yao, L.; Hu, Q.; Tu, Y.; Pang, Z.; Chen, H.; Jiang, X.; Gao, X.; Chen, J. Lactoferrin-modified PEG-co-PCL nanoparticles for enhanced brain delivery of NAP peptide following intranasal administration. Biomaterials, 2013, 34(15), 3870-3881.
45. Ahmad, N.; Warsi, M. H.; Iqbal, Z.; Samim, M.; Ahmad, F. J. Quantification of curcumin, demethoxycurcumin, and bisdemethoxycurcumin in rodent brain by UHPLC/ESI-Q-TOFMS/MS after intra-nasal administration of curcuminoids loaded PNIPAM nanoparticles. Drug testing and analysis, 2014, 6, 257-267.
46. Kumar, M.; Misra, A.; Pathak, K. Formulation and characterization of nanoemulsion of olanzapine for intranasal delivery. PDA J. Pharm. Sci. Technol., 2009, 63(6), 501-511.
47. Perez, A. P.; Mundina-Weilenmann, C.; Romero, E. L.; Morilla, M. J. Increased brain radioactivity by intranasal P-labeled siRNA dendriplexes within in situ-forming mucoadhesive gels. Int. J. Nanomed., 2012, 7, 1373-1385.
48. Malhotra, M.; Tomaro-Duchesneau, C.; Saha, S.; Prakash, S. Intranasal Delivery of Chitosan-siRNA Nanoparticle Formulation to the Brain. Method. Mol. Biol., 2014, 1141, 233-247.
49. Patel, D.; Naik, S.; Chuttani, K.; Mathur, R.; Mishra, A. K.; Misra, A. Intranasal delivery of cyclobenzaprine hydrochloride-loaded thiolated chitosan nanoparticles for pain relief. J. Drug Target., 2013, 21(8), 759-769.
50. Zhang, X.; Liu, L.; Chai, G.; Zhang, X.; Li, F. Brain pharmacokinetics of neurotoxin-loaded PLA nanoparticles modified with chitosan after intranasal administration in awake rats. Drug Dev. Ind. Pharm., 2013, 39(11), 1618-1624.
51. Vaka, S. R.; Shivakumar, H. N.; Repka, M. A.; Murthy, S. N. Formulation and evaluation of carnosic acid nanoparticulate system for upregulation of neurotrophins in the brain upon intranasal administration. J. Drug Target., 2013, 21(1), 44-53.
52. Vitaliano, G. D.; Vitaliano, F.; Rios, J. D.; Renshaw, P. F.; Teicher, M. H. New clathrin-based nanoplatforms for magnetic resonance imaging. PloS One, 2012, 7(5), e35821.
53. Mistry, A.; Stolnik, S.; Illum, L. Nanoparticles for direct nose-tobrain delivery of drugs. Int. J. Pharm., 2009, 379(1), 146-157.
54. Buck, L. B. In Principles of neural science. Kandel, E. R. Schwartz, J. H., Jessel, T. M., Ed.; McGraw-Hill: New York, 2000; Vol. 4, pp 625-652.
55. Tosi, G.; Vilella, A.; Chhabra, R.; Schmeisser, M. J.; Boeckers, T. M.; Ruozi, B.; Vandelli, M. A.; Forni, F.; Zoli, M.; Grabrucker, A. M. Insight on the fate of CNS-targeted nanoparticles. Part II: Intercellular neuronal cell-to-cell transport. J. Control. Rel., 2014, 177C, 96-107.
56. Clerico, D. M., To, W. C., Lanza, D. C. In Handbook of olfaction and gustation. Doty, R. L., Ed.; Marcel Dekker Inc.: New York, 2003, pp 1-16.
57. Gray, H. Gray's Anatomy. Classic Collector's Edition ed. Bounty Books: New York, 1978.
58. De Lorenzo, A. In Ciba Foundation Symposium-Taste and Smell in Vertebrates; Wiley Online Library, 1970, pp 151-176.
59. Oberdorster, G.; Sharp, Z.; Atudorei, V.; Elder, A.; Gelein, R.; Kreyling, W.; Cox, C. Translocation of inhaled ultrafine particles to the brain. Inhal. Toxicol., 2004, 16(6-7), 437-445.
60. Liu, Q.; Shen, Y.; Chen, J.; Gao, X.; Feng, C.; Wang, L.; Zhang, Q.; Jiang, X. Nose-to-brain transport pathways of wheat germ agglutinin conjugated PEG-PLA nanoparticles. Pharm. Res., 2012, 29(2), 546-558.
61. Wang, F.; Jiang, X.; Lu, W. Profiles of methotrexate in blood and CSF following intranasal and intravenous administration to rats. Int. J. Pharm., 2003, 263(1-2), 1-7.
62. Liu, Q.; Shao, X.; Chen, J.; Shen, Y.; Feng, C.; Gao, X.; Zhao, Y.; Li, J.; Zhang, Q.; Jiang, X. In vivo toxicity and immunogenicity of wheat germ agglutinin conjugated poly (ethylene glycol)-poly (lactic acid) nanoparticles for intranasal delivery to the brain. Toxicol. Appl. Pharmacol., 2011, 251(1), 79-84.
63. Shen, Y.; Chen, J.; Liu, Q.; Feng, C.; Gao, X.; Wang, L.; Zhang, Q.; Jiang, X. Effect of wheat germ agglutinin density on cellular uptake and toxicity of wheat germ agglutinin conjugated PEG-PLA nanoparticles in Calu-3 cells. Int. J. Pharm., 2011, 413(1-2), 184-193.
64. Wen, Z.; Yan, Z.; He, R.; Pang, Z.; Guo, L.; Qian, Y.; Jiang, X.; Fang, L. Brain targeting and toxicity study of odorranalectinconjugated nanoparticles following intranasal administration. Drug Deliv., 2011, 18(8), 555-561.
65. Oberdorster, G. Safety assessment for nanotechnology and nanomedicine: concepts of nanotoxicology. J. Intern. Med., 2010, 267(1), 89-105.
66. Ruan, Y.; Yao, L.; Zhang, B.; Zhang, S.; Guo, J. Nanoparticlemediated delivery of neurotoxin-II to the brain with intranasal administration: an effective strategy to improve antinociceptive activity of neurotoxin. Drug Dev. Ind. Pharm., 2012, 38(1), 123-128.
67. Ruan, Y.; Yao, L.; Zhang, B.; Zhang, S.; Guo, J. Antinociceptive properties of nasal delivery of neurotoxin-loaded nanoparticles coated with polysorbate-80. Peptides, 2011, 32(7), 1526-1529.
68. Jain, R.; Nabar, S.; Dandekar, P.; Patravale, V. Micellar nanocarriers: potential nose-to-brain delivery of zolmitriptan as novel migraine therapy. Pharm. Res., 2010, 27(4), 655-664.
69. Veronesi, M. C.; Aldouby, Y.; Domb, A. J.; Kubek, M. J. Thyrotropin-releasing hormone d, l polylactide nanoparticles (TRHNPs) protect against glutamate toxicity in vitro and kindling development in vivo. Brain Res., 2009, 1303, 151-160.
70. Kubek, M. J.; Domb, A. J.; Veronesi, M. C. Attenuation of kindled seizures by intranasal delivery of neuropeptide-loaded nanoparticles. Neurotherapeutics, 2009, 6(2), 359-371.
71. Pathan, S. A.; Alam, S.; Jain, G. K.; Zaidi, S. M.; Akhter, S.; Vohora, D.; Khar, R. K.; Ahmad, F. J. Quantitative analysis of safranal in saffron extract and nanoparticle formulation by a validated highperformance thin-layer chromatographic method. Phytochem. Anal., 2010, 21(3), 219-223.
72. Giordano, C.; Albani, D.; Gloria, A.; Tunesi, M.; Rodilossi, S.; Russo, T.; Forloni, G.; Ambrosio, L.; Cigada, A. Nanocomposites for neurodegenerative diseases: hydrogel-nanoparticle combinations for a challenging drug delivery. Int. J. Artificial Organs, 2011, 34(12), 1115-1127.
73. Zhang, C.; Chen, J.; Feng, C.; Shao, X.; Liu, Q.; Zhang, Q.; Pang, Z.; Jiang, X. Intranasal nanoparticles of basic fibroblast growth factor for brain delivery to treat Alzheimer's disease. Int. J. Pharm., 2014, 461(1-2), 192-202.
74. Zhao, Y. Z.; Li, X.; Lu, C. T.; Lin, M.; Chen, L. J.; Xiang, Q.; Zhang, M.; Jin, R. R.; Jiang, X.; Shen, X. T.; Li, X. K.; Cai, J. Gelatin nanostructured lipid carriers-mediated intranasal delivery of basic fibroblast growth factor enhances functional recovery in hemiparkinsonian rats. Nanomedicine, 2014, 10(4), 755-764.
75. Bhatt, R.; Singh, D.; Prakash, A.; Mishra, N. Development, characterization and nasal delivery of rosmarinic acid-loaded solid lipid nanoparticles for the effective management of Huntington's disease. Drug Deliv., 2014. [Epub ahead of print].
76. Liu, L.; Guo, K.; Lu, J.; Venkatraman, S. S.; Luo, D.; Ng, K. C.; Ling, E. A.; Moochhala, S.; Yang, Y. Y. Biologically active core/shell nanoparticles self-assembled from cholesterol-terminated PEG-TAT for drug delivery across the blood-brain barrier. Biomaterials, 2008, 29(10), 1509-1517.
77. Kepa, L.; Oczko-Grzesik, B.; Stolarz, W.; Sobala-Szczygiel, B. Drug-induced aseptic meningitis in suspected central nervous system infections. J. Clin. Neurosci., 2005, 12(5), 562-564.
78. Kumar, M.; Kakkar, V.; Mishra, A. K.; Chuttani, K.; Kaur, I. P. Intranasal delivery of streptomycin sulfate (STRS) loaded solid lipid nanoparticles to brain and blood. Int. J. Pharm., 2013, 461(1-2), 223-233.
79. Fisher, M.; Garcia, J. H. Evolving stroke and the ischemic penumbra. Neurology, 1996, 47(4), 884-888.
80. Mdzinarishvili, A.; Sutariya, V.; Talasila, P. K.; Geldenhuys, W. J.; Sadana, P. Engineering triiodothyronine (T3) nanoparticle for use in ischemic brain stroke. Drug Deliv. Transl. Res., 2013, 3(4), 309-317.
81. Ginsberg, M. D. Neuroprotection for ischemic stroke: past, present and future. Neuropharmacology, 2008, 55(3), 363-389.
82. Ehrenreich, H.; Weissenborn, K.; Prange, H.; Schneider, D.; Weimar, C.; Wartenberg, K.; Schellinger, P. D.; Bohn, M.; Becker, H.; Wegrzyn, M.; Jahnig, P.; Herrmann, M.; Knauth, M.; Bahr, M.; Heide, W.; Wagner, A.; Schwab, S.; Reichmann, H.; Schwendemann, G.; Dengler, R.; Kastrup, A.; Bartels, C.; Group, E. P. O. S. T. Recombinant human erythropoietin in the treatment of acute ischemic stroke. Stroke, 2009, 40(12), e647-656.
83. Jain, R.; Nabar, S.; Dandekar, P.; Hassan, P.; Aswal, V.; Talmon, Y.; Shet, T.; Borde, L.; Ray, K.; Patravale, V. Formulation and evaluation of novel micellar nanocarrier for nasal delivery of sumatriptan. Nanomedicine, 2010, 5(4), 575-587.
84. Digicaylioglu, M. Erythropoietin in stroke: quo vadis. Exp. Opin. Biol. Ther., 2010, 10(6), 937-949.
85. Topkoru, B. C.; Altay, O.; Duris, K.; Krafft, P. R.; Yan, J.; Zhang, J. H. Nasal administration of recombinant osteopontin attenuates early brain injury after subarachnoid hemorrhage. Stroke, 2013, 44(11), 3189-3194.
86. Ahmad, N.; Umar, S.; Ashafaq, M.; Akhtar, M.; Iqbal, Z.; Samim, M.; Ahmad, F. J. A comparative study of PNIPAM nanoparticles of curcumin, demethoxycurcumin, and bisdemethoxycurcumin and their effects on oxidative stress markers in experimental stroke. Protoplasma, 2013, 250(6), 1327-1338.
87. Draghia, R.; Caillaud, C.; Manicom, R.; Pavirani, A.; Kahn, A.; Poenaru, L. Gene delivery into the central nervous system by nasal instillation in rats. Gene Ther., 1995, 2(6), 418-423.
88. Kim, I. D.; Shin, J. H.; Kim, S. W.; Choi, S.; Ahn, J.; Han, P. L.; Park, J. S.; Lee, J. K. Intranasal delivery of HMGB1 siRNA confers target gene knockdown and robust neuroprotection in the postischemic brain. Mol. Ther., 2012, 20(4), 829-839.
89. Van Velthoven, C. T.; Sheldon, R. A.; Kavelaars, A.; Derugin, N.; Vexler, Z. S.; Willemen, H. L.; Maas, M.; Heijnen, C. J.; Ferriero, D. M. Mesenchymal stem cell transplantation attenuates brain injury after neonatal stroke. Stroke, 2013, 44(5), 1426-1432.
90. Liu, X. F.; Fawcett, J. R.; Hanson, L. R.; Frey, W. H. 2nd, The window of opportunity for treatment of focal cerebral ischemic damage with noninvasive intranasal insulin-like growth factor-I in rats. J. Stroke Cerebrovasc. Dis., 2004, 13(1), 16-23.
91. Doane, T.; Burda, C. Nanoparticle mediated non-covalent drug delivery. Adv. Drug Deliv. Rev., 2013, 65(5), 607-621.
92. Sarin, H.; Kanevsky, A. S.; Wu, H.; Brimacombe, K. R.; Fung, S. H.; Sousa, A. A.; Auh, S.; Wilson, C. M.; Sharma, K.; Aronova, M. A.; Leapman, R. D.; Griffiths, G. L.; Hall, M. D. Effective transvascular delivery of nanoparticles across the blood-brain tumor barrier into malignant glioma cells. J. Transl. Med., 2008, 6, 80.
93. Montet, X.; Funovics, M.; Montet-Abou, K.; Weissleder, R.; Josephson, L. Multivalent effects of RGD peptides obtained by nanoparticle display. J. Med. Chem., 2006, 49(20), 6087-6093.
94. Meyers, J. D.; Doane, T.; Burda, C.; Basilion, J. P. Nanoparticles for imaging and treating brain cancer. Nanomedicine, 2013, 8(1), 123-143.
95. Orringer, D. A.; Koo, Y. E.; Chen, T.; Kopelman, R.; Sagher, O.; Philbert, M. A. Small solutions for big problems: the application of nanoparticles to brain tumor diagnosis and therapy. Clin. Pharm. Ther., 2009, 85(5), 531-534.
96. Van Woensel, M.; Wauthoz, N.; Rosiere, R.; Amighi, K.; Mathieu, V.; Lefranc, F.; Van Gool, S. W.; De Vleeschouwer, S. Formulations for Intranasal Delivery of Pharmacological Agents to Combat Brain Disease: A New Opportunity to Tackle GBM? Cancers, 2013, 5(3), 1020-1048.
97. Hashizume, R.; Gupta, N. Telomerase inhibitors for the treatment of brain tumors and the potential of intranasal delivery. Curr. Opin. Mol. Ther., 2010, 12(2), 168-175.
98. Hashizume, R.; Ozawa, T.; Gryaznov, S. M.; Bollen, A. W.; Lamborn, K. R.; Frey, W. H. 2nd; Deen, D. F. New therapeutic approach for brain tumors: Intranasal delivery of telomerase inhibitor GRN163. Neuro Oncol., 2008, 10(2), 112-120.
99. Saw, M. M.; Chamberlain, J.; Barr, M.; Morgan, M. P.; Burnett, J. R.; Ho, K. M. Differential Disruption of Blood-Brain Barrier in Severe Traumatic Brain Injury. Neurocrit Care, 2014, 20(2), 209-216.
100. Bullock, M. R.; Lyeth, B. G.; Muizelaar, J. P. Current status of neuroprotection trials for traumatic brain injury: lessons from animal models and clinical studies. Neurosurgery, 1999, 45(2), 207-217; discussion 217-220.
101. Cohadon, F. Brain protection. Adv. Tech. Standard Neurosurg., 1994, 21, 77-152.
102. Faden, A. I.; Demediuk, P.; Panter, S. S.; Vink, R. The role of excitatory amino acids and NMDA receptors in traumatic brain injury. Science, 1989, 244(4906), 798-800.
103. Statler, K. D.; Jenkins, L. W.; Dixon, C. E.; Clark, R. S.; Marion, D. W.; Kochanek, P. M. The simple model versus the super model: translating experimental traumatic brain injury research to the bedside. J. Neurotrauma, 2001, 18(11), 1195-1206.
104. Lv, Q.; Fan, X.; Xu, G.; Liu, Q.; Tian, L.; Cai, X.; Sun, W.; Wang, X.; Cai, Q.; Bao, Y.; Zhou, L.; Zhang, Y.; Ge, L.; Guo, R.; Liu, X. Intranasal delivery of nerve growth factor attenuates aquaporins-4-induced edema following traumatic brain injury in rats. Brain Res., 2013, 1493, 80-89.
105. Tian, L.; Guo, R.; Yue, X.; Lv, Q.; Ye, X.; Wang, Z.; Chen, Z.; Wu, B.; Xu, G.; Liu, X. Intranasal administration of nerve growth factor ameliorate beta-amyloid deposition after traumatic brain injury in rats. Brain Res., 2012, 1440, 47-55.
106. Won, S. J.; Choi, B. Y.; Yoo, B. H.; Sohn, M.; Ying, W.; Swanson, R. A.; Suh, S. W. Prevention of traumatic brain injury-induced neuron death by intranasal delivery of nicotinamide adenine dinucleotide. J. Neurotrauma, 2012, 29(7), 1401-1409.
107. Hopkins, L.; Patchin, E. S.; Chiu, P. L.; Brandenberger, C.; Smiley-Jewell, S.; Pinkerton, K. E. Nose-to-Brain Transport of Aerosolized Quantum Dots Following Acute Exposure. Nanotoxicology, 2014, 8(8), 885-893.
108. Nune, S. K.; Gunda, P.; Thallapally, P. K.; Lin, Y. Y.; Forrest, M. L.; Berkland, C. J. Nanoparticles for biomedical imaging. Expert Opin. Drug Deliv., 2009, 6(11), 1175-1194.
109. Kumar, M.; Medarova, Z.; Pantazopoulos, P.; Dai, G.; Moore, A. Novel membrane-permeable contrast agent for brain tumor detection by MRI. Magn Reson Med., 2010, 63(3), 617-624.
110. Faucher, L.; Guay-Begin, A. A.; Lagueux, J.; Cote, M. F.; Petitclerc, E.; Fortin, M. A. Ultra-small gadolinium oxide nanoparticles to image brain cancer cells in vivo with MRI. Contrast Media Mol. Imaging, 2011, 6(4), 209-218.
111. Hadjipanayis, C. G.; Machaidze, R.; Kaluzova, M.; Wang, L.; Schuette, A. J.; Chen, H.; Wu, X.; Mao, H. EGFRvIII antibodyconjugated iron oxide nanoparticles for magnetic resonance imaging-guided convection-enhanced delivery and targeted therapy of glioblastoma. Cancer Res., 2010, 70(15), 6303-6312.
112. Vilella, A.; Tosi, G.; Grabrucker, A. M.; Ruozi, B.; Belletti, D.; Vandelli, M. A.; Boeckers, T. M.; Forni, F.; Zoli, M. Insight on the fate of CNS-targeted nanoparticles. Part I: Rab5-dependent cellspecific uptake and distribution. J. Control. Rel., 2014, 174, 195-201.
113. De Jong, W. H.; Borm, P. J. Drug delivery and nanoparticles: applications and hazards. Int. J. Nanomed., 2008, 3(2), 133-149.
114. Dahl, R.; Mygind, N. Anatomy, physiology and function of the nasal cavities in health and disease. Adv. Drug Deliv. Rev., 1998, 29(1-2), 3-12.
115. Jiang, L.; Gao, L.; Wang, X.; Tang, L.; Ma, J. The application of mucoadhesive polymers in nasal drug delivery. Drug Dev. Ind. Pharm., 2010, 36(3), 323-336.
116. Illum, L. Nanoparticulate systems for nasal delivery of drugs: a real improvement over simple systems? J. Pharm. Sci., 2007, 96(3), 473-483.
117. Cros, C. D.; Toth, I.; Blanchfield, J. T. Delivery of a lactose derivative of endomorphin 1 to the brain via the olfactory epithelial pathway. Bioorg. Med. Chem. Lett., 2014, 24(5), 1373-1375.
118. Lochhead, J. J.; Thorne, R. G. Intranasal delivery of biologics to the central nervous system. Adv. Drug Deliv. Rev., 2012, 64(7), 614-628.