DOI QR코드

DOI QR Code

In vitro Nasal Cell Culture Systems for Drug Transport Studies

  • Received : 2010.11.21
  • Accepted : 2010.12.14
  • Published : 2010.12.20

Abstract

Growing interest in the nasal route as a drug delivery system calls for a reliable in vitro model which is crucial for efficiently evaluating drug transport through the nasal cells. Various in vitro cell culture systems has thus been developed to displace the ex vivo excised nasal tissue and in vivo animal models. Due to species difference, results from animal studies are not sufficient for estimating the drug absorption kinetics in humans. However, the difficulty in obtaining reliable human tissue source limits the use of primary culture of human nasal epithelial cells. This shortage of human nasal tissue has therefore prompted studies on the "passage" culture of nasal epithelial cells. A serially passaged primary human nasal epithelial cell monolayer system developed by the air-liquid interface (ALI) culture is known to promote the differentiation of cilia and mucin gene and maintain high TEER values. Recent studies on the in vitro nasal cell culture systems for drug transport studies are reviewed in this article.

Keywords

References

  1. Agu, R.U., Jorissen, M., Willems, T., Augustijns, P., Kinget, R., Verbeke, N., 2001. In-vitro nasal drug delivery studies: comparison of derivatised, fibrillar and polymerised collagen matrix-based human nasal primary culture systems for nasal drug delivery studies. J. Pharm. Pharmacol. 53, 1447-1456. https://doi.org/10.1211/0022357011777981
  2. Agu, R.U., Jorissen, M., Willems, T., Van den Mooter, G., Kinget, R., Verbeke, N., Augustijns, P., 2000. Safety assessment of selected cyclodextrins - effect on ciliary activity using a human cell suspension culture model exhibiting in vitro ciliogenesis. Int. J. Pharm. 193, 219-226. https://doi.org/10.1016/S0378-5173(99)00342-7
  3. Agu, R.U., Obimah, D., Lyzenga, W., Jorissen, M., Massoud, E., Verbeke, N., 2009. Specific aminopeptidases of excised human nasal epithelium and primary culture: a comparison of functional characteristics and gene transcripts expression. J. Pharm. Pharmacol. 61, 599-606. https://doi.org/10.1211/jpp.61.05.0008
  4. Agu, R.U., Vu Dang, H., Jorissen, M., Kinget, R., Verbeke, N., 2004. Metabolism and absorption enhancement of methionine enkephalin in human nasal epithelium. Peptides 25, 563-569. https://doi.org/10.1016/j.peptides.2004.02.019
  5. Agu, R.U., Vu Dang, H., Jorissen, M., Willems, T., Kinget, R., Verbeke, N., 2002. Nasal absorption enhancement stratigies for therapeutic peptides: an in vitro study using cultured human nasal epithelium. Int. J. Pharm. 237, 179-191. https://doi.org/10.1016/S0378-5173(02)00039-X
  6. Alford, B.R., Douglas Jr., R.G., Couch, R.B., 1969. Atraumatic biopsy of nasal mucosa. Arch. Otolaryngol. 90, 180-184. https://doi.org/10.1001/archotol.1969.00770030182018
  7. Amidi, M., Romeijn, S.G., Borchard, G., Junginger, H.E., Hennink, W.E., Jiskoot, W., 2006. Preparation and characterization of protein-loaded N-trimethyl chitosan nanoparticles as nasal delivery system. J. Control. Release 111, 107-116. https://doi.org/10.1016/j.jconrel.2005.11.014
  8. Amoako-Tuffour, M., Yeung, P.K., Agu, R.U., 2009. Permeation of losartan across human respiratory epithelium: an in vitro study with Calu-3 cells. Arch. Pharm. 59, 395-405.
  9. Arora, P., Sharma, S., Garg, S., 2002. Permeability issues in nasal drug delivery. Drug Discov. Today 7, 967-975. https://doi.org/10.1016/S1359-6446(02)02452-2
  10. Bai, S., Yang, T., Abbruscato, T.J., Ahsan, F., 2008. Evaluation of human nasal RPMI 2650 cells grown at an air-liquid interface as a model for nasal drug transport studies. J. Pharm. Sci. 97, 1165-1178. https://doi.org/10.1002/jps.21031
  11. Berger, J.T., Voynow, J.A., Peters, K.W., Rose, M.C., 1999. Respiratory carcinoma cell lines. MUC genes and glycoconjugates. Am. J. Respir. Cell Mol. Biol. 20, 500-510. https://doi.org/10.1165/ajrcmb.20.3.3383
  12. Bernstein, J.M., Yankaskas, J.R., 1994. Increased ion transport in cultured nasal polyp epithelial cells. Arch. Otolaryngol. Head Neck Surg. 120, 993-996. https://doi.org/10.1001/archotol.1994.01880330071013
  13. Bitko, V., Barik, S., 2008. Nasal delivery of siRNA. Methods Mol. Biol. 442, 75-82. https://doi.org/10.1007/978-1-59745-191-8_6
  14. Boucher, R.C., Cotton, C.U., Gatzy, J.T., Knowles, M.R., 1988. Evidence for reduced $Cl^-$ and increased $Na^+$ permeability in cystic fibrosis human primary cell cultures. J. Physiol. 405, 77-103. https://doi.org/10.1113/jphysiol.1988.sp017322
  15. Boucher, R.C., Yankaskas, J.R., Cotton, C.U., Knowles, M.R., Stutts, M.J., 1987. Cell culture approaches to the investigation of human airway ion transport. Eur. J. Respir. Dis. Suppl. 153, 59-67.
  16. Bremer, S., Hoof, T., Wilke, M., Busche, R., Scholte, B., Riordan, J.R., Maass, G., Tummler, B., 1992. Quantitative expression patterns of multidrug resistance P-glycoprotein (MDR1) and differentially spliced cyctic-fibrosis transmembrane-conductance regulator mRNA transcripts in human epithelia. Eur. J. Biochem. 206, 137-149. https://doi.org/10.1111/j.1432-1033.1992.tb16911.x
  17. Brouillard, F., Tondelier, D., Edelman, A., Baudouin-Legros, M., 2001. Drug resistance induced by ouabain via the stimulation of MDR1 gene expression in human carcinomatous pulmonary cells. Cancer Res. 61, 1693-1698.
  18. Bur, M., Huwer, H., Muys, L., Lehr, C.M., 2010. Drug transport across pulmonary epithelial cell monolayers: effects of particle size, apical liquid volume, and deposition technique. J. Aerosol. Med. Pulm. Drug Deliv. 23, 119-127. https://doi.org/10.1089/jamp.2009.0757
  19. Chemuturi, N.V., Donovan, M.D., 2007. Role of organic cation transporters in dopamine uptake across olfactory and nasal respiratory tissues. Mol. Pharm. 4, 936-942. https://doi.org/10.1021/mp070032u
  20. Chen, M., Li, X.R., Zhou, Y.X., Yang, K.W., Chen, X.W., Deng, Q., Liu, Y., Ren, L.J., 2009. Improved absorption of salmon calcitonin by ultraflexible liposomes through intranasal delivery. Peptides. 30, 1288-1295. https://doi.org/10.1016/j.peptides.2009.03.018
  21. Chen, Y., Zhao, Y.H., Wu, R., 2001. Differential regulation of airway mucin gene expression and mucin secretion by extracellular nucleotide triphosphates. Am. J. Respir. Cell Mol. Biol. 25, 409-417. https://doi.org/10.1165/ajrcmb.25.4.4413
  22. Cho, E., Gwak, H., Chun, I., 2008. Formulation and evaluation of ondansetron nasal delivery systems. Int. J. Pharm. 349, 101-107. https://doi.org/10.1016/j.ijpharm.2007.07.028
  23. Cho, H.J., Balakrishnan, P., Shim, W.S., Chung, S.J., Shim, C.K., Kim, D.D. 2010. Characterization and in vitro evaluation of freeze-dried microparticles composed of granisetron-cyclodextrin complex and carboxymethylcellulose for intranasal delivery. Int. J. Pharm. 400, 59-65. https://doi.org/10.1016/j.ijpharm.2010.08.030
  24. Cho, H.J., Balakrishnan, P., Park, E.K., Song, K.W., Hong, S.S., Jang, T.Y., Kim, K.S., Chung, S.J., Shim, C.K., Kim, D.D. 2011a. Poloxamer/cyclodextrin/chitosan-based thermoreversible gel for intranasal delivery of fexofenadine hydrochloride. J. Pharm. Sci. in press.
  25. Cho, H.J., Choi, M.K., Lin, H., Kim, J.S., Chung, S.J., Shim, C.K., Kim, D.D. 2011. Expression and functional activity of P-glycoprotein (P-gp) in passaged primary human nasal epithelial (HNE) cell monolayers cultured by the air-liquid interface (ALI) method for nasal drug transport study. J. Pharm. Pharmacol.
  26. Christensen, D., Foged, C., Rosenkrands, I., Lundberg, C.V., Andersen, P., Agger, E.M., Nielsen, H.M., 2010. CAF01 liposomes as a mucosal vaccine adjuvant: In vitro and in vivo investigations. Int. J. Pharm. 390, 19-24. https://doi.org/10.1016/j.ijpharm.2009.10.043
  27. Cornaz, A.L., Buri, P., 1994. Nasal mucosa as an absorption barrier. Eur. J. Pharm. Biopharm. 40, 261-270.
  28. Costantino, H.R., Illum, L., Brandt, G., Johnson, P.H., Quay, S.C., 2007. Intranasal delivery: physicochemical and therapeutic aspects. Int. J. Pharm. 337, 1-24. https://doi.org/10.1016/j.ijpharm.2007.03.025
  29. Coste, A., Rateau, J., Roudot-Thoraval, F., Chapelin, C., Gilain, L., Poron, F., Peynegre, R., Bernaudin, J., Escudier, E., 1996. Increased epithelial cell proliferation in nasal polyps. Arch. Otolaryngol. Head Neck Surg. 122, 432. https://doi.org/10.1001/archotol.1996.01890160072013
  30. Cozens, A.L., Yezzi, M.J., Kunzelmann, K., Ohrui, T., Chin, L., Eng, K., Finkbeiner, W.E., Widdicombe, J.H., Gruenert, D.C., 1994. CFTR expression and chloride secretion in polarized immortal human bronchial epithelial cells. Am. J. Respir. Cell. Mol. Biol. 10, 38-47. https://doi.org/10.1165/ajrcmb.10.1.7507342
  31. De Fraissinette, A., Brun, R., Felix, H., Vonderscher, J., Rummelt, A., 1995. Evaluation of the human cell line RPMI 2650 as an in vitro nasal model. Rhinology. 33, 194-198.
  32. Dimova, S., Vlaeminck, V., Brewster, M.E., Noppe, M., Jorissen, M., Augustijns, P., 2005. Stable ciliary activity in human nasal epithelial cells grown in a perfusion system. Int. J. Pharm. 292, 157-168. https://doi.org/10.1016/j.ijpharm.2004.11.030
  33. Ehrhardt, C., Kneuer, C., Fiegel, J., Hanes, J., Schaefer, U.F., Kim, K.J., Lehr, C.M., 2002. Influence of apical fluid volume on the development of functional intercellular junctions in the human epithelial cell line 16HBE14o-: implications for the use of this cell line as an in vitro model for bronchial drug absorption studies. Cell. Tissue. Res. 308, 391-400. https://doi.org/10.1007/s00441-002-0548-5
  34. Ehrhadt, C., Kneuer, C., Laue, M., Schaefer, U.F., Kim, K.J., Lehr, C.M., 2003. 16HBE14o- human bronchial epithelial cell layers express P-glycoprotein, lung resistance-related protein, and caveolin-1. Pharm. Res. 20, 545-551. https://doi.org/10.1023/A:1023230328687
  35. Endter, S., Francombe, D., Ehrhardt, C., Gumbleton, M., 2009. RTPCR analysis of ABC, SLC and SLCO drug transporters in human lung epithelial cell models. J. Pharm. Pharmacol. 61, 583-591. https://doi.org/10.1211/jpp.61.05.0006
  36. Florea, B.I., van der Sandt, I.C., Schrier, S.M., Kooiman, K., Deryckere, K., de Boer, A.G., Junginger, H.E., Borchard, G., 2001. Evidence of P-glycoprotein mediated apical to basolateral transport of flunisolide in human broncho-tracheal epithelial cells (Calu-3). Br. J. Pharmacol. 134, 1555-1563. https://doi.org/10.1038/sj.bjp.0704390
  37. Foster, K.A., Avery, M.L., Yazdanian, M., Audus, K.L., 2000. Characterization of the Calu-3 cell line as a tool to screen pulmonary drug delivery. Int. J. Pharm. 208, 1-11. https://doi.org/10.1016/S0378-5173(00)00452-X
  38. Genter, M.B., Krishan, M., Augustine, L.M., Cherrington, N.J., 2010. Drug transporter expression and localization in rat nasal respiratory and olfactory mucosa and olfactory bulb. Drug Metab. Dispos. 38, 1644-1647. https://doi.org/10.1124/dmd.110.034611
  39. Gervasi, P., Longo, V., Naldi, F., Panattoni, G., Ursino, F., 1991. Xenobiotic-metabolizing enzymes in human respiratory nasal mucosa. Biochem. Pharmacol. 41, 177-184. https://doi.org/10.1016/0006-2952(91)90474-J
  40. Getchell, M.L., Chen, Y., Ding, X., Sparks, D.L., Getchell, T.V., 1993. Immunohistochemical localization of a cytochrome P-450 isozyme in human nasal mucosa: age-related trends. Ann. Otol. Rhinol. Laryngol. 102, 368-374. https://doi.org/10.1177/000348949310200509
  41. Gray, T.E., Guzman, K., Davis, C.W., Abdullah, L.H., Nettesheim, P., 1996. Mucociliary differentiation of serially passaged normal human tracheobronchial epithelial cells. Am. J. Respir. Cell Mol. Biol. 14, 104-112. https://doi.org/10.1165/ajrcmb.14.1.8534481
  42. Gray, T., Koo, J.S., Nettesheim, P., 2001. Regulation of mucous differentiation and mucin gene expression in the tracheobronchial epithelium. Toxicology 160, 35-46. https://doi.org/10.1016/S0300-483X(00)00455-8
  43. Gruenert, D.C., Basbaum, C.B., Widdicombe, J.H., 1990. Long-term culture of normal and cystic fibrosis epithelial cells grown under serum-free conditions. In Vitro Cell. Dev. Biol. 26, 411-418. https://doi.org/10.1007/BF02623833
  44. Han, D., Wang, N., Zhang, L., 2009. The effect of myrtol standardized on human nasal ciliary beat frequency and mucociliary transport time. Am. J. Rhinol. Allergy 23, 610-614. https://doi.org/10.2500/ajra.2009.23.3401
  45. Hanamure, Y., Deguchi, K., Ohyama, M., 1994. Ciliogenesis and mucus synthesis in cultured human respiratory epithelial cells. Ann. Otol. Rhinol. Laryngol. 103, 889-895. https://doi.org/10.1177/000348949410301111
  46. Harikarnpakdee, S., Lipipun, V., Sutanthavibul, N., Ritthidej, G.C., 2008. Spray-dried mucoadhesive microspheres: preparation and transport through nasal cell monolayer. AAPS Pharm-SciTech. 7, 12.
  47. Henriksson, G., Norlander, T., Zheng, X., Stierna, P., Westrin, K.M., 1997. Expression of P-glycoprotein 170 in nasal mucosa may be increased with topical steroids. Am. J. Rhinol. 11, 317-321. https://doi.org/10.2500/105065897781446603
  48. Hofmann, T., Reinisch, S., Gerstenberger, C., Koele, W., Gugatschka, M., Wolf, G., 2010. Influence of topical antifungal drugs on ciliary beat frequency of human nasal mucosa: an in vitro study. Laryngoscope. 120, 1444-1448. https://doi.org/10.1002/lary.20965
  49. Hoang, V.D., Uchenna, A.R., Mark, J., Renaat, K., Norbert, V., 2002. Characterization of human nasal primary culture systems to investigate peptide metabolism. Int. J. Pharm. 238, 247-256. https://doi.org/10.1016/S0378-5173(02)00077-7
  50. Hood, A.T., Currie, D., Garte, S.J., 1987. Establishment of a rat nasal epithelial tumor cell line. In Vitro Cell. Dev. Biol. 23, 274-278. https://doi.org/10.1007/BF02623710
  51. Hosoya, K., Kubo, H., Natsume, H., Sugibayashi, K., Morimoto, Y., 1994. Evaluation of enhancers to increase nasal absorption using Ussing chamber technique. Biol. Pharm. Bull. 17, 316-322. https://doi.org/10.1248/bpb.17.316
  52. Howard, K.A., Rahbek, U.L., Liu, X., Damgaard, C.K., Glud, S.Z., Andersen, M.O., Hovgaard, M.B., Schmitz, A., Nyengaard, J.R., Besenbacher, F., Kjems, J., 2006. RNA interference in vitro and in vivo using a novel chitosan/siRNA nanoparticle system. Mol. Ther. 14, 476-484. https://doi.org/10.1016/j.ymthe.2006.04.010
  53. Huh, Y., Cho, H.J., Yoon, I.S., Choi, M.K., Kim, J.S., Oh, E., Chung, S.J., Shim, C.K., Kim, D.D., 2010. Preparation and evaluation of spary-dried hyaluronic acid microspheres intranasal delivery of fexofenadine hydrochloride. Eur. J. Pharm. Sci. 40, 9-15. https://doi.org/10.1016/j.ejps.2010.02.002
  54. Hull, J., Harris, A., 1994. Limitations of cell culture of airway epithelium collected by a nasal brushing technique. In Vitro Cell. Dev. Biol. 30A, 488-489.
  55. Jintapattanakit, A., Peungvicha, P., Sailasuta, A., Kissel, T., Junyaprasert, V.B., 2010. Nasal absorption and local tissue reaction of insulin nanocomplexes of trimethyl chitosan derivatives in rats. J. Pharm. Pharmacol. 62, 583-591. https://doi.org/10.1211/jpp.62.05.0004
  56. Kaler, G., Truong, D.M., Sweeney, D.E., Logan, D.W., Nagle, M., Wu, W., Eraly, S.A., Nigam, S.K., 2006. Olfactory mucosa-expressed organic anion transporter, Oat6, manifests high affinity interactions with odorant organic anions. Biochem. Biophys. Res. Commun. 351, 872-876. https://doi.org/10.1016/j.bbrc.2006.10.136
  57. Kandimallar, K.K., Donovan, M.D., 2005. Localization and differential activity of P-glycoprotein in the bovine olfactory nasal respiratory mucosae. Pharm. Res. 22, 1121-1128. https://doi.org/10.1007/s11095-005-5420-3
  58. Kienast, K., Riechelmann, H., Knorst, M., Schlegel, J., Muller-Quernheim, J., Schellenberg, J., Ferlinz, R. 1994. An experimental model for the exposure of human ciliated cells to sulfur dioxide at different concentrations. Clin. Investig. 72, 215-219.
  59. Kissel, T., Werner, U., 1998. Nasal delivery of peptides: an in vitro cell culture model for the investigation of transport and metabolism in human nasal epithelium. J. Control. Release 53, 195-203. https://doi.org/10.1016/S0168-3659(97)00253-8
  60. Koizumi, J., Kojima, T., Ogasawara, N., Kamekura, R., Kurose, M., Go, M., Harimaya, A., Murata, M., Osanai, M., Chiba, H., Himi, T., Sawada, N., 2008. Protein kinase C enhances tight junction barrier function of human nasal epithelial cells in primary culture by transcriptional regulation. Mol. Pharmacol. 74, 432-442. https://doi.org/10.1124/mol.107.043711
  61. Lang, S., Langguth, P., Oschmann, R., Traving, B., Merkle, H.P., 1996. Transport and metabolic pathway of thymocartin (TP4) in excised bovine nasal mucosa. J. Pharm. Pharmacol. 48, 1190-1196. https://doi.org/10.1111/j.2042-7158.1996.tb03919.x
  62. Lazard, D.S., Moore, A., Hupertan, V., Martin, C., Escabasse, V., Dreyfus, P., Burgel, P.R., Amselem, S., Escudier, E., Coste, A., 2009. Muco-ciliary differentiation of nasal epithelial cells is decreased after wound healing in vitro. Allergy 64, 1136-1143. https://doi.org/10.1111/j.1398-9995.2009.02003.x
  63. Lee, M.K., Yoo, J.W., Lin, H., Kim, Y.S., Kim, D.D., Choi, Y.M., Park, S.K., Lee, C.H., Roh, H.J., 2005. Air-liquid interface culture of serially passaged human nasal epithelial cell monolayer for in vitro drug transport studies. Drug Deliv. 12, 305-311. https://doi.org/10.1080/10717540500177009
  64. Leitner, V.M., Guggi, D., Krauland, A.H., Bernkop-Schnurch, A., 2004. Nasal delivery of human growth hormone: in vitro and in vivo evaluation of a thiomer/glutathione microparticulate delivery system. J. Control. Release 100, 87-95. https://doi.org/10.1016/j.jconrel.2004.08.001
  65. Li, L., Mathias, N.R., Heran, C.L., Moench, P., Wall, D.A., Smith, R.L., 2006. Carbopol-mediated paracellular transport enhancement in Calu-3 cell layers. J. Pharm. Sci. 95, 326-335. https://doi.org/10.1002/jps.20541
  66. Lin, H., Gebhardt, M., Bian, S., Kwon, K.A., Shim, C.K., Chung, S.J., Kim, D.D., 2007. Enhancing effect of surfactants on fexofenadine.HCl transport across the human nasal epithelial cell monolayer. Int. J. Pharm. 330, 23-31. https://doi.org/10.1016/j.ijpharm.2006.08.043
  67. Lin, H., Li, H., Cho, H.J., Bian, S., Roh, H.J., Lee, M.K., Kim, J.S., Chung, S.J., Shim, C.K., Kim, D.D., 2007b. Air-liquid interface (ALI) culture of human bronchial epithelial cell monolayers as an in vitro model for airway drug transport studies. J. Pharm. Sci. 96, 341-350. https://doi.org/10.1002/jps.20803
  68. Lin, H., Yoo, J.W., Roh, H.J., Lee, M.K., Chung, S.J., Shim, C.K., Kim, D.D., 2005. Transport of anti-allergic drugs across the passage cultured human nasal epithelial cell monolayer. Eur. J. Pharm. Sci. 26, 203-210. https://doi.org/10.1016/j.ejps.2005.06.003
  69. Mallant, R., Jorissen, M., Augustijns, P., 2008. Beneficial effect of antibiotics on ciliary beat frequency of human nasal epithelial cells exposed to bacterial toxins. J. Pharm. Pharmacol. 60, 437-443. https://doi.org/10.1211/jpp.60.4.0005
  70. Mallant, R., Vlaeminck, V., Jorissen, M., Augustijns, P., 2009. An improved primary human nasal cell culture for the simultaneous determination of transepithelial transport and ciliary beat frequency. J. Pharm. Pharmacol. 61, 883-890. https://doi.org/10.1211/jpp.61.07.0007
  71. Manford, F., Tronde, A., Jeppsson A.B., Patel, N., Johansson, F., Forbes, B., 2005. Drug permeability in 16HBE14o- airway cell layers correlates with absorption from the isolated perfused rat lung. Eur. J. Pharm. Sci. 26, 414-420. https://doi.org/10.1016/j.ejps.2005.07.010
  72. Marttin, E., Verhoef, J.C., Merkus, F.W., 1998. Efficacy, safety and mechanism of cyclodextrins as absorption enhancers in nasal delivery of peptide and protein drugs. J. Drug Target. 6, 17-36. https://doi.org/10.3109/10611869808997878
  73. Mathia, N.R., Timoszyk, J., Stetsko, P.I., Megill, J.R., Smith R.L., Wall, D.A., 2002. Permeability characteristics of calu-3 human bronchial epithelial cells: in vitro-in vivo correlation to predict lung absorption in rats. J. Drug Target. 10, 31-40. https://doi.org/10.1080/10611860290007504
  74. Minn, A., Leclerc, S., Heydel, J.M., Denizot, C., Cattarelli, M., Netter, P., Gradinaru, D., 2002. Drug transport into the mammalian brain: the nasal pathway and its specific metabolic barrier. J. Drug Target. 10, 285-296. https://doi.org/10.1080/713714452
  75. Noruddin, N.A.A., Saim, A.B., Chua, K.H., Idrus, R., 2007. Human nasal turbinates as a viable source of respiratory epithelial cells using co-culture system versus dispase-dissociation technique. Laryngoscope 117, 2139-2145. https://doi.org/10.1097/MLG.0b013e3181453a1e
  76. Otsuka, H., Dolovich, J., Richardson, M., Bienenstock, J., Denburg, J.A., 1987. Metachromatic cell progenitors and specific growth and differentiation factors in human nasal mucosa and polyps. Am. Rev. Respir. Dis. 136, 710-717. https://doi.org/10.1164/ajrccm/136.3.710
  77. Pipkorn, U., Karlsson, G., Enerback, L., 1988. A brush method to harvest cells from the nasal mucosa for microscopic and biochemical analysis. J. Immunol. Methods 112, 37-42. https://doi.org/10.1016/0022-1759(88)90030-0
  78. Pipkorn, U., Karlsson, G., 1988. Methods for obtaining specimens from the nasal mucosa for morphological and biochemical analysis. Eur. Respir. J. 1, 856-862.
  79. Pires, A., Fortuna, A., Alves, G., Falcao, A., 2009. Intranasal drug delivery: how, why and what for? J. Pharm. Pharm. Sci. 12, 288-311. https://doi.org/10.18433/J3NC79
  80. Robinson, C.B., Wu, R., 1993. Mucin synthesis and secretion by cultured tracheal cells: effects of collagen substratum thickness. In Vitro Cell. Dev. Biol. Anim. 29A, 469-477.
  81. Roh, H.J., Goh, E.K., Wang, S.G., Chon, K.M., Yoon, J.H., Kim, Y.S., 1999. Serially passaged normal human nasal epithelial cells: morphology and mucous secretory differentiation. Korean. J. Rhinol. 6, 107-112.
  82. Sarkar, M.A., 1992. Drug metabolism in the nasal mucosa. Pharm Res. 9, 1-9. https://doi.org/10.1023/A:1018911206646
  83. Merkle, H.P., Ditzinger, G., Lang, S.R., Peter, H., Schmidt, M.C., 1998. In vitro cell models to study nasal mucosal permeability and metabolism. Adv. Drug Deliv. Rev. 29, 51-79. https://doi.org/10.1016/S0169-409X(97)00061-6
  84. Seki, T., Kanbayashi, H., Chono, S., Tabata, Y., Morimoto, K., 2007. Effects of sperminated gelatin on the nasal absorption of insulin. Int. J. Pharm. 338, 213-218. https://doi.org/10.1016/j.ijpharm.2007.02.004
  85. Slutter, B., Bal, S., Keijzer, C., Mallants, R., Hagenaars, N., Que, I., Kaijzel, E., van Eden, W., Augustijns, P., Lowik, C., Bouwstra, J., Broere, F., Jiskoot, W., 2010. Nasal vaccination with N-trimethyl chitosan and PLGA based nanoparticles: nano-particle characteristics determine quality and strength of the antibody response in mice against the encapsulated antigen. Vaccine 28, 6282-6291. https://doi.org/10.1016/j.vaccine.2010.06.121
  86. Steele, V.E., Arnold, J.T., 1985. Isolation and long-term culture of rat, rabbit, and human nasal terbinate epithelial cells. In Vitro Cell. Dev. Biol. 21, 681-687. https://doi.org/10.1007/BF02620922
  87. Suptawiwat, O., Tantilipikorn, P., Boonarkart, C., Lumyongsatien, J., Uiprasertkul, M., Puthavathana, P., Auewarakul, P., Brown, J., 2010. Enhanced susceptibility of nasal polyp tissues to avian and human influenza viruses. PLoS One 5: e12973 https://doi.org/10.1371/journal.pone.0012973
  88. Teijeiro-Osorio, D., Remunan-Lopez, C., Alonso, M.J., 2009. New generation of hybrid poly/oligosaccharide nanoparticles as carriers for the nasal delivery of macromolecules. Biomacromolecules 10, 243-249. https://doi.org/10.1021/bm800975j
  89. Usui, S., Shimizu, T., Kishioka, C., Fujita, K., Sakakura, Y., 2000. Secretory cell differentiation and mucus secretion in cultures of human nasal epithelial cells: use of a monoclonal antibody to study human nasal mucin. Ann. Otol. Rhinol. Laryngol. 109, 271-277. https://doi.org/10.1177/000348940010900307
  90. Vetter, A., Martien, R., Bernkop-Schnurch, A., 2010. Thiolated polycarbophil as an adjuvant for permeation enhancement in nasal delivery of antisense nucleotides. J. Pharm. Sci. 99, 1427-1439. https://doi.org/10.1002/jps.21887
  91. Vu Dang, H., Agu, R.U., Jorissen, M., Kinget, R., Verbeke, N., 2002. Characterization of human nasal primary culture systems to investigate peptide metabolism. Int. J. Pharm. 238. 247-256. https://doi.org/10.1016/S0378-5173(02)00077-7
  92. Wadell, C., Bjork, E., Camber, O., 1999. Nasal drug delivery-evaluation of an in vitro model using porcine nasal mucosa. Eur. J. Pharm. Sci. 7, 197-206. https://doi.org/10.1016/S0928-0987(98)00023-2
  93. Wadell, C., Bjork, E., Camber, O., 2003. Permeability of porcine nasal mucosa correlated with human nasal absorption. Eur. J. Pharm. Sci. 18, 47-53. https://doi.org/10.1016/S0928-0987(02)00240-3
  94. Wengst, A., Reichl, S., 2010. RPMI 2650 epithelial model and three-dimensional reconstructed human nasal mucosa as in vitro models for nasal permeation studies. Eur. J. Pharm. Biopharm. 74, 290-297. https://doi.org/10.1016/j.ejpb.2009.08.008
  95. Werner, U., Kissel, T., 1995. Development of a human nasal epithelial cell culture model and its suitability for transport and metabolism studies under in vitro conditions. Pharm. Res. 12, 565-571. https://doi.org/10.1023/A:1016210231121
  96. Werner, U., Kissel, T., 1996. In-vitro cell culture models of the nasal epithelium: a comparative histochemical investigation of their suitability for drug transport studies. Pharm. Res. 13, 978-988. https://doi.org/10.1023/A:1016038119909
  97. Wilk-Blaszczak, M.A., French, A.S., Man, S.F., 1992. Halide permeation through 10 pS and 20 pS anion channels in human airway epithelial cells. Biochim. Biophys. Acta. 1104, 160-166. https://doi.org/10.1016/0005-2736(92)90145-C
  98. Wioland, M.A., Fleury-Feith, J., Corlieu, P., Commo, F., Monceaux, G., Lacau-St-Guily, J., Bernaudin, J.F., 2000. CFTR, MDR1, and MRP1 immunolocalization in normal human nasal respiratory mucosa. J. Histochem. Cytochem. 48, 1215-1222. https://doi.org/10.1177/002215540004800905
  99. Witschi, C., Mrsny, R.J., 1999. In vitro evaluation of microparticles and polymer gels for use as nasal platforms for protein delivery. Pharm. Res. 16, 382-390. https://doi.org/10.1023/A:1018869601502
  100. Wu, R., Yankaskas, J., Cheng, E., Knowles, M.R., Boucher, R., 1985. Growth and differentiation of human nasal epithelial cells in culture. Serum-free, hormone-supplemented medium and proteoglycan synthesis. Am. Rev. Respir. Dis. 132, 311-320.
  101. Wuthrich, P., Buri, P., 1989. The transnasal route of drug administration. Aspects of nasal anatomy and physiology. Pharm. Acta. Helv. 64, 322-331.
  102. Yang, T., Hussain, A., Paulson, J., Abbruscato, T.J., Ahsan, F., 2004. Cyclodextrins in nasal delivery of low-molecular-weight heparins: in vivo and in vitro studies. Pharm. Res. 21, 1127-1136. https://doi.org/10.1023/B:PHAM.0000032998.84488.7a
  103. Yankaskas, J.R., Cotton, C.U., Knowles, M.R., Gatzy, J.T., Boucher, R.C., 1985. Culture of human nasal epithelial cells on collagen matrix supports. A comparison of bioelectric properties of normal and cystic fibrosis epithelia. Am. Rev. Respir. Dis. 132, 1281-1287.
  104. Yeo, N.K., Jang, Y.J., 2010. Rhinovirus infection-induced alteration of tight junction and adherens junction components in human nasal epithelial cells. Laryngoscope 120, 346-352.
  105. Yoo, J.W., Kim, Y.S., Lee, S.H., Lee, M.K., Roh, H.J., Jhun, B.H., Lee, C.H., Kim, D.D., 2003. Serially passaged human nasal epithelial cell monolayer for in vitro drug transport studies. Pharm. Res. 20, 1690-1696. https://doi.org/10.1023/A:1026112107100
  106. Yoon, J.H., Kim, K.S., Kim, S.S., Lee, J.G., Park, I.Y., 2000. Secretory differentiation of serially passaged normal human nasal epithelial cells by retinoic acid: expression of mucin and lysozyme. Ann. Otol. Rhinol. Laryngol. 109, 594-601. https://doi.org/10.1177/000348940010900612
  107. Yu, H., Kim, K., 2009. Direct nose-to-brain transfer of a growth hormone releasing neuropeptide, hexarelin after intranasal administration to rabbits. Int. J. Pharm. 378, 73-79. https://doi.org/10.1016/j.ijpharm.2009.05.057
  108. Zhou, H., Wang, X., Brighton, L., Hazucha, M., Jaspers, I., Carson, J.L., 2009. Increased nasal epithelial ciliary beat frequency associated with lifestyle tobacco smoke exposure. Inhal. Toxicol. 21, 875-881. https://doi.org/10.1080/08958370802555898
  109. Zuckerman, J.D., Lee, W.Y., DelGaudio, J.M., Moore, C.E., Nava, P., Nusrat, A., Parkos, C.A., 2008. Pathophysiology of nasal polyposis: the role of desmosomal junctions. Am. J. Rhinol. 22, 589-597. https://doi.org/10.2500/ajr.2008.22.3235

Cited by

  1. Primary Air–Liquid Interface Culture of Nasal Epithelium for Nasal Drug Delivery vol.13, pp.7, 2016, https://doi.org/10.1021/acs.molpharmaceut.5b00852
  2. Is RPMI 2650 a Suitable In Vitro Nasal Model for Drug Transport Studies? pp.2107-0180, 2017, https://doi.org/10.1007/s13318-017-0426-x