Nose-to-Brain Delivery: Investigation of the Transport of Nanoparticles with Different Surface Characteristics and Sizes in Excised Porcine Olfactory Epithelium

Molecular Pharmaceutics

Volumn 12, Issue 8, 2015, Pages 2755-2766

  Mistry, Alpesh ^a   Stolnik, Snjezana ^a   Illum, Lisbeth ^b  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^b IDentity   (United Kingdom)

Author keywords

chitosan; excised tissue; nose to brain delivery; olfactory epithelium; polysorbate 80; transepithelial transport

Indexed keywords

CHITOSAN; CITRIC ACID; NANOPARTICLE; POLYSORBATE 80; POLYSTYRENE;

ANIMAL TISSUE; ARTICLE; BIOENERGY; BRAIN; DIFFUSION CHAMBER; DRUG DELIVERY SYSTEM; DRUG FORMULATION; DRUG PENETRATION; DRUG TRANSPORT; ELECTROPHYSIOLOGY; FLUORESCENCE MICROSCOPY; HISTOLOGY; HYDROPHILICITY; MUCUS; NONHUMAN; NOSE; OLFACTORY EPITHELIUM; OXYGENATION; PARTICLE SIZE; PH; PIG; PRIORITY JOURNAL; RESAZURIN ASSAY; SURFACE PROPERTY; TEMPERATURE; TISSUE INJURY; TISSUE METABOLISM; ANIMAL; BIOAVAILABILITY; BLOOD BRAIN BARRIER; CELL SURVIVAL; DRUG EFFECTS; FEMALE; IN VITRO STUDY; INTRANASAL DRUG ADMINISTRATION; METABOLISM; TRANSPORT AT THE CELLULAR LEVEL;

ADMINISTRATION, INTRANASAL; ANIMALS; BIOLOGICAL AVAILABILITY; BIOLOGICAL TRANSPORT; BLOOD-BRAIN BARRIER; BRAIN; CELL SURVIVAL; DRUG DELIVERY SYSTEMS; FEMALE; IN VITRO TECHNIQUES; NANOPARTICLES; NOSE; OLFACTORY MUCOSA; PARTICLE SIZE; SURFACE PROPERTIES; SWINE;

EID: 84938377218     PISSN: 15438384     EISSN: 15438392     Source Type: Journal    
DOI: 10.1021/acs.molpharmaceut.5b00088     Document Type: Article

References (67)

1. 3 particles into the brain: microdistribution, chemical states, and histopathological observation Biol. Trace Elem. Res. 2007, 118, 233-243
2. 2 nanoparticles Toxicology 2008, 254, 82-90
3. Wang, Y.-Y.; Lai, S. K.; Suk, J. S.; Pace, A.; Cone, R.; Hanes, J. Addressing the peg mucoadhesivity paradox to engineer nanoparticles that "slip" through the human mucus barrier Angew. Chem., Int. Ed. 2008, 4, 9726-9729
4. Wang, X.; Chi, N.; Tang, X. Preparation of estradiol chitosan nanoparticles for improving nasal absorption and brain targeting Eur. J. Pharm. Biopharm. 2008, 70, 735-740
5. Illum, L. Transport of drugs from the nasal cavity to the central nervous system Eur. J. Pharm. Sci. 2000, 11, 1-18
6. Illum, L. Nasal drug delivery-recent developments and future prospects J. Controlled Release 2012, 161, 254-263
7. Lochhead, J. J.; Thorne, R. G. Intranasal delivery of biologics to the central nervous system Adv. Drug Delivery Rev. 2012, 64, 614-628
8. Alam, M. I.; Baboota, S.; Ahuja, A.; Ali, M.; Ali, J.; Sahni, J. K.; Bhatnagar, A. Pharmacoscintigraphic evaluation of potential lipid nanocarriers for nose-to-brain delivery of antidepressant drug Int. J. Pharm. 2014, 470, 88-106
9. Illum, L. Is nose to brain transport of drugs in man a reality? J. Pharm. Pharmacol. 2004, 56, 3-17
10. Elder, A.; Gelein, R.; Silva, V.; Feikert, T.; Opanashuk, L.; Carter, J.; Potter, R.; Maynard, A.; Finkelstein, J.; Oberdörster, G. Translocation of inhaled ultrafine manganese oxide particles to the central nervous system Environ. Health Perspect. 2006, 114, 1172-11178
11. Oberdörster, G.; Sharp, Z.; Atudorei, V.; Elder, A.; Gelein, R.; Kreyling, W.; Cox, C. Translocarion of inhaled ultrafine particles to the brain Inhalation Toxicol. 2004, 16, 437-445
12. Oberdörster, G.; Oberdörster, E.; Oberdörster, J. Nanotoxicology: an emerging discipline evolving from studies of ultrafine particles Environ. Health. Perspect. 2005, 113, 823-839
13. De Lorenzo, A. J. Electron microscopy of the olfactory and gustatory pathways Ann. Otol., Rhinol., Laryngol. 1960, 69, 410-420
14. Illum, L. The potential for nose-to-brain delivery of drugs. In Nanoparticles in the Lung: Environmental Exposure and Drug Delivery; Tsuda, A.; Gehr, P., Eds.; CRC Press/Taylor & Francis Group: Boca Raton, FL, 2015; pp 295-321.
15. 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, 3482-3490
16. 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, 184-193
17. 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-functionalised nanoparticles for drug delivery to the brain after intranasal administration Biomaterials 2011, 32, 9888-9898
18. Lui, 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 brains delivery of NAP peptide following intranasal administration Biomaterials 2013, 34, 3870-3881
19. Zhang, Q.; Jiang, X.; Jiang, W.; Lu, W.; Su, L.; Shi, Z. Preparation of nimodipine-loaded microemulsion for intranasal delivery and evaluation on the targeting efficiency to the brain Int. J. Pharm. 2004, 275, 85-96
20. Gao, X.; Wu, Z.; 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. Controlled Release 2007, 121, 156-167
21. 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, 6-15
22. Kumar, M.; Pandey, R. S.; Patra, K. C.; Jain, S. K.; Soni, M. L.; Dang, J. S.; Madan, J. Evaluation of neuropeptide loaded trimethyl chitosan nanoparticles for nose to brain delivery Int. J. Biol. Macromol. 2013, 61, 189-195
23. Dalpiaz, A.; Ferraro, L.; Perrone, D.; Leo, E.; Iannuccelli, V.; Pavan, B.; Paganetto, G.; Beggiato, G.; Beggiato, S.; Scalia, S. Brain uptake of a zidovudine prodrug after nasal administration of solid lipid microparticles Mol. Pharmaceutics 2014, 11, 1550-1561
24. Stevenson, B. R.; Anderson, M. J.; Bullivant, S. The epithelial tight junction: structure, function and preliminary biochemical characterisation Mol. Cell. Biochem. 1988, 83, 129-145
25. Costantino, H. R.; Illum, L.; Brandt, G.; Johnson, P.; Quay, S. C. Intanasal delivery: physiochemical and therapeutic aspects Int. J. Pharm. 2007, 337, 1-24
26. Morrison, R. H.; Costanzo, R. M. Morphology of olfactory epithelium in humans and other vertebrates Microsc. Res. Technol. 1992, 23, 49-61
27. Rejman, J.; Oberle, V.; Zuhorn, I. S.; Hoekstra, D. Size dependent internalisation of particles via the pathway of clathrin- and caveolae-mediated endocytosis Biochem. J. 2004, 377, 159-169
28. Jones, A. T. Gateways and tools for drug delivery: endocytic pathways and the cellular dynamics of cell penetrating peptides Int. J. Pharm. 2008, 354, 34-38
29. Harush-Frenkel, O.; Rozentur, E.; Benita, S.; Altschuler, Y. Surface charge of nanoparticles determines their their endocytotic and transcytotic pathway in polarized MDCK cells Biomacromolecules 2008, 9, 435-443
30. Larochelle, R.; Martineaudoize, B. Distribution and histochemical characterisation of goblet cells in the nasal cavity of piglets Am. J. Anat. 1991, 191, 103-111
31. Fransen, N.; Westin, U. E.; Nystrom, C.; Bjork, E. The in vitro transport of dihydroergotamine across porcine nasal respiratory and olfactory mucosa and the effect of a novel powder formulation J. Drug Delivery Sci. Technol. 2007, 17, 267-271
32. Jansson, B. Models for the transfer of drugs from the nasal cavity to the central nervous system. Ph.D. Thesis, Uppsala University, 2004; pp 24-27.
33. Brooking, J.; Davis, S. S.; Illum, L. Transport of nanoparticles across the rat nasal mucosa J. Drug Targeting 2001, 9, 267-279
34. Mistry, A.; Glud, S. Z.; Kjems, J.; Randel, J.; Howard, K. A.; Stolnik, S.; Illum, L. Effect of physicochemical properties on intranasal nanoparticle transit into murine olfactory epithelium J. Drug Targeting 2009, 17, 543-52
35. Östh, K.; Grasjo, J.; Bjork, E. A new method for drug transport studies on pig nasal mucosa using a horizontal Ussing chamber J. Pharm. Sci. 2002, 91, 1259-1273
36. Jones, T. R. General Outline of the Organisation of the Animal Kingdom and Manual of Comparative Anatomy; John Van Voorst: London, 1861.
37. Kock, A. M.; Schmidt, M. C.; Merkle, H. P. In vitro methodologies to study nasal delivery using excised mucosa. In Cell Culture Models of Biological Barriers; Lehr, C. M., Ed.; Taylor & Francis Group: London, 2002; pp 228-252.
38. Maitani, Y.; Ishigaki, K.; Takayama, K.; Nagai, T. In vitro nasal transport across rabbit mucosa: effect of oxygen bubbling, pH and hypertonic pressure on permeability of Lucifer yellow, diazepam and 17-beta-estradiol Int. J. Pharm. 1997, 146, 11-19
39. Wadell, C.; Björk, E.; Camber, O. Permeability of porcine nasal mucosa correlated with human nasal absorption Eur. J. Pharm. Sci. 2003, 18, 47-53
40. Grizzle, W. E.; Fredenburgh, J. L.; Myers, R. B. Fixation of tissues. In Theory and Practice of Histological Techniques, 6 th ed.; Bancroft, J.; Gamble, M., Eds.; Churchill Livingstone: Edinburgh, 2007; pp 53-74.
41. Wang, Q. Z.; Chen, X. G.; Liu, N.; Wang, S. X.; Liu, C. S.; Meng, X. H.; Liu, C. G. Protonation constants of chitosan with different molecular weight and degree of deacetylation Carbohydr. Polym. 2006, 65, 194-201
42. 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. 2013, 48, 393-405
43. Wadell, C.; Björk, E.; Camber, O. Nasal drug delivery-evaluation of an in vitro model using porcine nasal mucosa Eur. J. Pharm. Sci. 1999, 7, 197-206
44. Östh, K.; Strindelius, L.; Larhed, A.; Ahlander, A.; Roomans, G. M.; Sjöholm, I.; Björk, E. Uptake of ovalbumin-conjugated starch microparticles by pig respiratory nasal mucosa in vitro J. Drug Targeting 2003, 11, 75-82
45. Östh, K.; Paulsson, M.; Björk, E.; Edsman, K. Evaluation of drug release from gels on pig nasal mucosa in a horizontal Ussing chamber J. Controlled Release 2002, 83, 377-388
46. Lai, S. K.; O'Hanlon, D. E.; Harrold, S.; Man, S. T.; Wang, Y.-Y.; Cone, R.; Hanes, J. Rapid transport of large polymeric nanoparticles in fresh undiluted human mucus Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 1482-1487
47. Lai, S. K.; Wang, Y.-Y.; Hanes, J. Mucus-penetrating nanoparticles for drug and gene delivery to mucosal tissues Adv. Drug Delivery Rev. 2009, 61, 158-171
48. Scherer, D.; Mooren, F. C.; Kinne, R. K. H.; Kreuter, J. In vitro permeability of PBCA nanoparticles through porcine small intestine J. Drug Targeting 1993, 1, 21-27
49. De Campos, A. M.; Diebold, Y.; Carvalho, E. L. S.; Sanchez, A.; Alonso, M. J. Chitosan nanoparticles as new ocular drug delivery systems: in vitro stability, in vivo fate and cellular toxicity Pharm. Res. 2004, 21, 803-810
50. Vllasaliu, D.; Casettari, L.; Fowler, R.; Exposito-Harris, R.; Illum, L.; Garnett, M.; Stolnik, S. Absorption-promoting effects of chitosan in airway and intestinal cell lines: a comparison Int. J. Pharm. 2012, 430, 151-160
51. Kawashima, Y.; Yamamoto, H.; Takeuchi, H.; Kuno, Y. Mucoadhesive dl-lactide/glycolide copolymer nanospheres coated with chitosan to improve oral delivery of elcatonin Pharm. Dev. Technol. 2000, 5, 77-85
52. Leung, S.; Robinson, J. Polyanionic polymers in bio- and mucoadhesive drug delivery. Polyelectrolyte gels-properties, preparations and applications ACS Symp. Ser. 1992, 480, 269-284
53. Kristensson, K.; Olsson, Y. Uptake of exogenous proteins in mouse olfactory cells Acta Neuropathol. 1971, 19, 145-154
54. Hunter, D. D.; Castranova, V.; Stanley, C.; Dey, R. D. Effects of silica exposure on substance P immunoreactivity and preprotachykinin mRNA expression in trigeminal sensory neurons in Fischer 344 rats J. Toxicol. Environ. Health, Part A 1998, 53, 593-605
55. 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, 1-12
56. 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, 1526-1529
57. 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 Biomater. 2011, 7, 4169-4176
58. 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 pharmacodynamics study on Parkinson's disease following intranasal administration J. Controlled Release 2011, 151, 131-138
59. Xia, T.; Kovochich, M.; Brant, J.; Hotze, M.; Sempf, J.; Oberley, T.; Sioutas, C.; Yeh, J.; Wiesner, M. R.; Nel, A. E. Comparison of the abilities of ambient and manufactured nanoparticles to induce cellular toxicity according to an oxidative stress paradigm Nano Lett. 2006, 6, 1794-1807
60. Bannunah, A.; Vvlasaliu, D.; Lord, J.; Stolnik, S. Mechanisms of nanoparticle internalization and transport across an intestinal epithelial cell model: Effect of size and surface charge Mol. Pharmaceutics 2014, 11, 4363-4373
61. Casettari, L.; Illum, L. Chitosan in nasal delivery systems for therapeutic drugs J. Controlled Release 2014, 190, 189-200
62. Carreno-Gomez, B.; Duncan, R. Evaluation of the biological properties of soluble chitosan and chitosan microspheres Int. J. Pharm. 1997, 148, 231-240
63. Huang, M.; Khor, E.; Lim, L. Y. Uptake and cytotoxicity of chitosan molecules and nanoparticles: effects of molecular weight and degree of deacetylation Pharm. Res. 2004, 21, 344-353
64. Casettari, L.; Vllasaliu, D.; Mantovani, G.; Howdle, S. M.; Stolnik, S.; L Effect of PEGylation on the toxicity and permeability enhancement of chitosan Biomacromolecules. 2010, 11, 2854-2865
65. Vllasaliu, D.; Exposito-Harris, R.; Heras, A.; Casettari, L.; Garnett, M.; Illum, L.; Stolnik, S. Tight junction modulation by chitosan nanoparticles: comparison with chitosan solution Int. J. Pharm. 2010, 400, 183-93
66. Behrens, I.; Pena, A. I. V.; Alonso, M. J.; Kissel, T. Comparative uptake studies of bioadhesive and non-bioadhesive nanoparticles in human intestinal cell lines and rats: the effect of mucus on particle adsorption and transport Pharm. Res. 2002, 19, 1185-1193
67. Brown, D. M.; Wilson, M. R.; MacNee, W.; Stone, V.; Donaldson, K. Size-dependent proinflammatory effects of ultrafine polystyrene particles: a role for surface area and oxidative stress in the enhanced activity of ultrafines Toxicol. Appl. Pharmacol. 2001, 175, 191-199