Evaluation of layers of the rat airway epithelial cell line RL-65 for permeability screening of inhaled drug candidates

European Journal of Pharmaceutical Sciences

Volumn 47, Issue 2, 2012, Pages 481-489

  Hutter, V ^a   Hilgendorf, C ^b   Cooper, A ^c   Zann, V ^c   Pritchard, D I ^a   Bosquillon, C ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^b ASTRAZENECA R AND D   (Sweden)

^c ASTRAZENECA   (United Kingdom)

Author keywords

Absorption prediction; Drug inhalation; Drug transporters; In vitro models; In vitro in vivo correlation; Pulmonary delivery

Indexed keywords

DIGOXIN; GLYCOPROTEIN P; MANNITOL; PROTEIN ZO1; RHODAMINE 123;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL STRUCTURE; DRUG ABSORPTION; DRUG PENETRATION; ELECTRIC RESISTANCE; EPITHELIUM CELL; EX VIVO STUDY; GENETIC ANALYSIS; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PHARMACOKINETICS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RESPIRATORY EPITHELIUM;

ADMINISTRATION, INHALATION; ANIMALS; BRONCHI; CELL LINE; CELL MEMBRANE PERMEABILITY; DIGOXIN; EPITHELIAL CELLS; FLUORESCENT DYES; GENE EXPRESSION; HUMANS; MANNITOL; MEMBRANE TRANSPORT PROTEINS; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, SCANNING; PHARMACEUTICAL PREPARATIONS; RATS; RHODAMINE 123; RNA, MESSENGER;

EID: 84864496479     PISSN: 09280987     EISSN: 18790720     Source Type: Journal    
DOI: 10.1016/j.ejps.2012.07.007     Document Type: Article

References (57)

1. A. Ayrton, and P. Morgan Role of transport proteins in drug discovery and development: a pharmaceutical perspective Xenobiotica 38 2008 676 708
2. D. Balharry, K. Sexton, and K.A. BéruBé An in vitro approach to assess the toxicity of inhaled tobacco smoke components: nicotine, cadmium, formaldehyde and urethane Toxicology 244 2008 66 76
3. P.J. Barnes Targeting the epigenome in the treatment of asthma and chronic obstructive pulmonary disease Proc. Am. Thorac. Soc. 6 2009 693 696
4. S.A. Blaine, M. Wick, C. Dessev, and R.A. Nemenoff Induction of cPLA2 in lung epithelial cells and non-small cell lung cancer is mediated by Sp1 and c-Jun J. Biol. Chem. 276 2001 42737 42743
5. K. Bleasby, J.C. Castle, C.J. Roberts, C. Cheng, W.J. Bailey, J.F. Sina, A.V. Kulkarni, M.J. Hafey, R. Evers, J.M. Johnson, R.G. Ulrich, and J.G. Slatter Expression profiles of 50 xenobiotic transporter genes in humans and pre-clinical species: a resource for investigations into drug disposition Xenobiotica 36 2006 963 988
6. Y. Bren-Mattison, V. Van Putten, D. Chan, R. Winn, M.W. Geraci, and R.A. Nemenoff Peroxisome proliferator-activated receptor-c (PPARc) inhibits tumorigenesis by reversing the undifferentiated phenotype of metastatic non-small-cell lung cancer cells (NSCLC) Oncogene 24 2005 1412 1422
7. P.C. Brown, S.S. Thorgeirsson, and J.A. Silverman Cloning and regulation of the rat mdr2 gene Nucl. Acids Res. 21 1993 3885 3891
8. G. Borchard, M.L. Cassará, P.E. Roemelé, B.I. Florea, and H.E. Junginger Transport and local metabolism of budesonide and fluticasone propionate in a human bronchial epithelial cell line (Calu-3) J. Pharm. Sci. 91 2002 1561 1567
9. C. Bosquillon Drug transporters in the lung - do they play a role in the biopharmaceutics of inhaled drugs? J. Pharm. Sci. 99 2010 2240 2255
10. J.M. Brady, N.J. Cherrington, D.P. Hartley, S.C. Buist, N. Li, and C.D. Klaassen Tissue distribution and chemical induction of multiple drug resistance genes in rats Drug Metab. Dispos. 30 2002 838 844
11. J. Brillault, W.V. De Castro, T. Harnois, A. Kitzis, J.C. Olivier, and W. Couet P-glycoprotein-mediated transport of moxifloxacin in a Calu-3 lung epithelial cell model Antimicrob. Agents Chemother. 53 2009 1457 1462
12. L. Campbell, A.N. Abulrob, L.E. Kandalaft, S. Plummer, A.J. Hollins, A. Gibbs, and M. Gumbleton Constitutive expression of p-glycoprotein in normal lung alveolar epithelium and functionality in primary alveolar epithelial cultures J. Pharmacol. Exp. Ther. 304 2003 441 452
13. M.E. Cavet, M. West, and N.L. Simmons Transepithelial transport of the fluoroquinolone ciprofloxacin by human airway epithelial Calu-3 cells Antimicrob. Agents Chemother. 41 1997 2693 2698
14. L.A. Doyle, W. Yang, L.V. Abruzzo, T. Krogmann, Y. Gao, A.K. Rishi, and D.D. Ross A multidrug resistance transporter from human MCF-7 breast cancer cells Proc. Natl. Acad. Sci. USA 95 1998 15665 15670
15. C. Ehrhardt, C. Kneuer, J. Fiegel, J. Hanes, U.F. Schaefer, K.J. Kim, and C.M. Lehr 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 2002 391 400
16. C. Ehrhardt, C. Kneuer, M. Laue, U.F. Schaefer, K.J. Kim, and C.M. Lehr 16HBE14o - human bronchial epithelial cell layers express P-glycoprotein, lung resistance-related protein, and caveolin-1 Pharm. Res. 20 2003 545 551
17. C. Ehrhardt, C. Kneuer, C. Bies, C.M. Lehr, K.J. Kim, and U. Bakowsky Salbutamol is actively absorbed across human bronchial epithelial cell layers Pulm. Pharmacol. Ther. 18 2005 165 170
18. C. Ehrhardt, B. Forbes, and K. Kim In vitro models of the tracheo-bronchial epithelium C. Ehrhardt, K. Kim, Drug Absorption Studies 2008 Springer New York 235 257
19. V.M. Felton, L.J. Inge, B.C. Willis, R.M. Bremner, and M.A. Smith Immunosuppression induced bronchial epithelial-mesenchymal transition: a potential contributor to obliterative bronchiolitis J. Thorac. Cardiovasc. Surg. 141 2011 523 530
20. J. Fiegel, C. Ehrhardt, U.F. Schaefer, C.M. Lehr, and J. Hanes Large porous particle impingement on lung epithelial cell monolayers - toward improved particle characterization in the lung Pharm. Res. 20 2003 788 796
21. B. Forbes, A. Shah, G.P. Martin, and A.B. Lansley The human bronchial epithelial cell line 16HBE14o- as a model system of the airways for studying drug transport Int. J. Pharm. 257 2003 161 167
22. B. Forbes, and C. Ehrhardt Human respiratory epithelial cell culture for drug delivery applications Eur. J. Pharm. Biopharm. 60 2005 193 205
23. K.A. Foster, M.L. Avery, M. Yazdanian, and K.L. Audus Characterization of the Calu-3 cell line as a tool to screen pulmonary drug delivery Int. J. Pharm. 208 2000 1 11
24. D. Francombe, G. Taylor, S. Taylor, G. Somers, C.D. Edwards, and M. Gumbleton Functional role of P-gp efflux in limiting pulmonary drug absorption within an intact lung: application of an isolated perfused rat lung model Proc. Respir. Drug Del. II 2008 461 464
25. C.I. Grainger, L.L. Greenwell, D.J. Lockley, G.P. Martin, and B. Forbes Culture of Calu-3 cells at the air interface provides a representative model of the airway epithelial barrier Pharm. Res. 23 2006 1482 1490
26. M. Haghi, P.M. Young, D. Traini, R. Jaiswal, J. Gong, and M. Bebawy Time- and passage-dependent characteristics of a Calu-3 respiratory epithelial cell model Drug Dev. Ind. Pharm. 36 2010 1207 1214
27. K.O. Hamilton, G. Backstrom, M.A. Yazdanian, and K.L. Audus P-glycoprotein efflux pump expression and activity in Calu-3 cells J. Pharm. Sci. 90 5 2001 647 658
28. G. Horvath, N. Schmid, M.A. Fragoso, A. Schmid, G.E. Conner, M. Salathe, and A. Wanner Epithelial organic cation transporters ensure pH-dependent drug absorption in the airway Am. J. Resp. Cell Mol. Biol. 36 2007 53 60
29. S.-M. Huang, R. Temple, D.C. Throckmorton, and L.J. Lesko Drug interaction studies: study design, data analysis, and implications for dosing and labeling Clin. Pharmacol. Ther. 81 2007 298 304
30. V. Hutter, C. Hilgendorf, A. Brown, A. Cooper, V. Zann, D. Pritchard, and C. Bosquillon Evaluation of P-glycoprotein in drug trafficking across human bronchial epithelial cell culture models J. Aero. Med. Pulm. Drug Del. 24 2011 22
31. G.A. Kullak-Ublick, M.G. Ismair, B. Stieger, L. Landmann, R. Huber, F. Pizzagalli, K. Fattinger, P.J. Meier, and B. Hagenbuch Organic anion-transporting polypeptide B (OATP-B) and its functional comparison with three other OATPs of human liver Gastroenterology 120 2001 525 533
32. H. Lin, H. Li, H.J. Cho, S. Bian, H.J. Roh, M.K. Lee, J.S. Kim, S.J. Chung, C.K. Shim, and D.D. Kim 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 2007 341 350
33. M. Madlova, C. Bosquillon, D. Asker, P. Dolezal, and B. Forbes In-vitro respiratory drug absorption models possess nominal functional P-glycoprotein activity J. Pharm. Pharmacol. 61 2009 293 301
34. F. Manford, A. Tronde, A.B. Jeppsson, N. Patel, F. Johansson, and B. Forbes Drug permeability in 16HBE14o- airway cell layers correlates with absorption from the isolated perfused rat lung Eur. J. Pharm. Sci. 26 2005 414 420
35. R. Masereeuw, M.M. Moons, and F.G. Russel Rhodamine 123 accumulates extensively in the isolated perfused rat kidney and is secreted by the organic cation system Eur. J. Pharmacol. 321 1997 315 323
36. N.R. Mathias, J. Timoszyk, P.I. Stetsko, J.R. Megill, R.L. Smith, and D.A. Wall Permeability characteristics of Calu-3 human bronchial epithelial cells: in vitro-in vivo correlation to predict lung absorption in rats J. Drug Target. 10 2002 31 40
37. C. Meaney, B.I. Florea, G. Borchard, and H.E. Junginger Characterisation of a human submucosal gland cell line (Calu-3) as an in vitro model of the airway epithelium Proc. Int. Symp. Control. Rel. Bioact. Mater. 26 1999 198 199
38. T. Mikkaichi, T. Suzuki, T. Onogawa, M. Tanemoto, H. Mizutamari, M. Okada, T. Chaki, S. Masuda, T. Tokui, N. Eto, M. Abe, F. Satoh, M. Unno, T. Hishinuma, K. Inui, S. Ito, J. Goto, and T. Abe Isolation and characterization of a digoxin transporter and its rat homologue expressed in the kidney Proc. Natl. Acad. Sci. USA 101 2004 3569 3574
39. M. Mukherjee, D.I. Pritchard, and C. Bosquillon Evaluation of air-interfaced Calu-3 cell layers for investigation of inhaled drug interactions with organic cation transporters in vitro Int. J. Pharm. 426 2012 7 14
40. T. Nakamura, T. Nakanishi, T. Haruta, Y. Shirasaka, J.P. Keogh, and I. Tamai Transport of ipratropium, an anti-chronic obstructive pulmonary disease drug, is mediated by organic cation/carnitine transporters in human bronchial epithelial cells: implications for carrier-mediated pulmonary absorption Mol. Pharm. 7 2010 187 195
41. R. Nemenoff, M. Weiser-Evans, and R. Winn Activation and molecular targets of peroxisome proliferator-activated receptor-gamma ligands in lung cancer PPAR Res. 75 2008 196 207
42. J. Patel, D. Pal, V. Vangal, M. Gandhi, and A.L. Mitra Transport of HIV-protease inhibitors across 1 alpha,25di-hydroxy vitamin D3-treated Calu-3 cell monolayers: modulation of P-glycoprotein activity Pharm. Res. 19 2002 1696 1703
43. J. Rautio, J.E. Humphreys, L.O. Webster, A. Balakrishnan, J.P. Keogh, J.R. Kunta, C.J. Serabjit-Singh, and J.W. Polli In vitro p-glycoprotein inhibition assays for assessment of clinical drug interaction potential of new drug candidates: a recommendation for probe substrates Drug Metab. Dispos. 34 2006 786 792
44. P.E. Roberts, D.M. Phillips, and J.P. Mather A novel epithelial cell from neonatal rat lung: isolation and differentiated phenotype Am. J. Physiol. 259 1990 415 425
45. M. Sakagami In vivo, in vitro and ex vivo models to assess pulmonary absorption and disposition of inhaled therapeutics for systemic delivery Adv. Drug Deliv. Rev. 58 2006 1030 1060
46. A.H. Schinkel, U. Mayer, E. Wagenaar, C.A. Mol, L. van Deemter, J.J. Smit, M.A. van der Valk, A.C. Voordouw, H. Spits, O. van Tellingen, J.M. Zijlmans, W.E. Fibbe, and P. Borst Normal viability and altered pharmacokinetics in mice lacking mdr1-type (drug-transporting) P-glycoproteins Proc. Natl. Acad. Sci. USA 94 1997 4028 4033
47. J.L. Sporty, L. Horálková, and C. Ehrhardt In vitro cell culture models for the assessment of pulmonary drug disposition Expert Opin. Drug Metab. Toxicol. 4 2008 333 345
48. N. Suzuyama, M. Katoh, T. Takeuchi, S. Yoshitomi, T. Higuchi, S. Asashi, and T. Yokoi Species differences of inhibitory effects on P-glycoprotein- mediated drug transport J. Pharm. Sci. 96 2007 1609 1618
49. T. Takeuchi, S. Yoshitomi, T. Higuchi, K. Ikemoto, S. Niwa, T. Ebihara, M. Katoh, T. Yokoi, and S. Asahi Establishment and characterization of the transformants stablyexpressing MDR1 derived from various animal species in LLC-PK1 Pharm. Res. 23 2006 1460 1472
50. M.E. Taub, K.M. Mease, R.S. Sane, C.A. Watson, L. Chen, H. Ellens, B.P. Hirakawa, E.L. Reyner, M. Jani, and C.A. Lee Digoxin is not a substrate for organic anion transporting polypeptide transporters OATP1A2, OATP1B1, OATP1B3, and OATP2B1 but is a substrate for a sodium dependent transporter expressed in HEK293 cells Drug Metab. Dispos. 39 2011 2093 2102
51. A. Tronde, B. Nordén, A.B. Jeppsson, P. Brunmark, E. Nilsson, H. Lennernäs, and U.H. Bengtsson Drug absorption from the isolated perfused rat lung-correlations with drug physicochemical properties and epithelial permeability J. Drug Target. 11 2003 61 74
52. I.C. van der Sandt, M.C. Blom-Roosemalen, A.G. de Boer, and D.D. Breimer Specificity of doxorubicin versus rhodamine-123 in assessing P-glycoprotein functionality in the LLC-PK1, LLC-PK1:MDR1 and Caco-2 cell lines Eur. J. Pharm. Sci. 11 3 2000 207 214
53. V. Van Putten, Z. Refaat, C. Dessev, S. Blaine, M. Wick, L. Butterfield, S.-Y. Han, L.E. Heasley, and R.A. Nemenoff Induction of cytosolic phospholipase A2 by oncogenic RAS is mediated through the JNK and ERK pathways in rat epithelial cells J. Biol. Chem. 276 2001 1226 1232
54. X.Q. Wang, H. Li, V. Van Putten, R.A. Winn, L.E. Heasley, and R.A. Nemenoff Oncogenic K-Ras regulates proliferation and cell junctions in lung epithelial cells through induction of cyclooxygenase-2 and activation of metalloproteinase-9 Mol. Biol. Cell 20 2009 791 800
55. J.H. Widdicombe, L.A. Sachs, J.L. Morrow, and W.E. Finkbeiner Expansion of cultures of human tracheal epithelium with maintenance of differentiated structure and function Biotechniques 39 2005 249 255
56. M.J. Wick, S. Blaine, V. Van Putten, M. Saavedra, and R.A. Nemenoff Lung Krüppel-like factor (LKLF) is a transcriptional activator of the cytosolic phospholipase A2 alpha promoter Biochem. J. 387 2005 239 246
57. H. Yamaguchi, M. Sugie, M. Okada, T. Mikkaichi, T. Toyohara, T. Abe, J. Goto, T. Hishinuma, M. Shimada, and N. Mano Transport of estrone 3-sulfate mediated by organic anion transporter OATP4C1: estrone 3-sulfate binds to the different recognition site for digoxin in OATP4C1 Drug Metab. Pharmacokinet. 25 2010 314 317