The Proteome of Filter-Grown Caco-2 Cells with a Focus on Proteins Involved in Drug Disposition

Journal of Pharmaceutical Sciences

Volumn 105, Issue 2, 2016, Pages 817-827

  Ölander, Magnus ^a   Wiśniewski, Jacek R ^b   Matsson, Pär ^a   Lundquist, Patrik ^a   Artursson, Per ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

Author keywords

ABC transporters; caco 2 cells; epithelial delivery permeability; oral absorption; permeability; proteomics; solute transporters; tight junction in vitro in vivo correlations; transporters

Indexed keywords

ABC TRANSPORTER; HYDROLASE; INTEGRIN; ORGANIC ANION TRANSPORTER B; PITAVASTATIN; PROTEOME; TIGHT JUNCTION PROTEIN; DRUG; MEMBRANE PROTEIN; POLYCARBONATE; POLYCARBOXYLATE CEMENT;

ACTIVE TRANSPORT; ADHERENS JUNCTION; ARTICLE; BRUSH BORDER; CACO 2 CELL LINE; CELL DIFFERENTIATION; CELL GROWTH; DIFFUSION; DRUG ABSORPTION; DRUG DISPOSITION; DRUG DISTRIBUTION; DRUG EXCRETION; DRUG METABOLISM; DRUG PENETRATION; FILTER; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INTESTINE CELL; JEJUNUM; MEMBRANE TRANSPORT; MONOLAYER CULTURE; NORMAL HUMAN; PROTEIN ANALYSIS; PROTEIN EXPRESSION; TIGHT JUNCTION; CACO-2 CELL LINE; CELL MEMBRANE PERMEABILITY; COLON; DRUG EFFECTS; METABOLISM; MICROPORE FILTER; PHYSIOLOGY;

CACO-2 CELLS; CELL MEMBRANE PERMEABILITY; COLON; HUMANS; JEJUNUM; MEMBRANE PROTEINS; MICROPORE FILTERS; PHARMACEUTICAL PREPARATIONS; POLYCARBOXYLATE CEMENT; PROTEOME;

EID: 84964461819     PISSN: 00223549     EISSN: 15206017     Source Type: Journal    
DOI: 10.1016/j.xphs.2015.10.030     Document Type: Article

References (90)

1. J. Fogh, J.M. Fogh, and T. Orfeo One hundred and twenty-seven cultured human tumor cell lines producing tumors in nude mice J Natl Cancer Inst 59 1 1977 221 226
2. M. Pinto, S. Robineleon, M.D. Appay, and et al. Enterocyte-like differentiation and polarization of the human colon carcinoma cell line Caco-2 in culture Biol Cell 47 3 1983 323 330
3. E. Grasset, M. Pinto, E. Dussaulx, A. Zweibaum, and J. Desjeux Epithelial properties of human colonic carcinoma cell line Caco-2: electrical parameters Am J Physiol 247 3 1984 C260 C267
4. I.J. Hidalgo, T.J. Raub, and R.T. Borchardt Characterization of the human colon carcinoma cell line (Caco-2) as a model system for intestinal epithelial permeability Gastroenterology 96 3 1989 736 749
5. P. Artursson Epithelial transport of drugs in cell culture. I: a model for studying the passive diffusion of drugs over intestinal absorbtive (Caco-2) cells J Pharm Sci 79 6 1990 476 482
6. G. Wilson, I. Hassan, C. Dix, and et al. Transport and permeability properties of human Caco-2 cells: an in vitro model of the intestinal epithelial cell barrier J Control Release 11 1 1990 25 40
7. A.R. Hilgers, R.A. Conradi, and P.S. Burton Caco-2 cell monolayers as a model for drug transport across the intestinal mucosa Pharm Res 7 9 1990 902 910
8. K.L. Audus, R.L. Bartel, I.J. Hidalgo, and R.T. Borchardt The use of cultured epithelial and endothelial cells for drug transport and metabolism studies Pharm Res 7 5 1990 435 451
9. I.J. Hidalgo, and R.T. Borchardt Transport of bile acids in a human intestinal epithelial cell line, Caco-2 Biochim Biophys Acta 1035 1 1990 97 103
10. D.C. Kim, A. Harrison, M. Ruwart, and et al. Evaluation of the bile acid transporter in enhancing intestinal permeability to renin-inhibitory peptides J Drug Target 1 4 1993 347 359
11. J.R. Wiśniewski, K. Dus-Szachniewicz, P. Ostasiewicz, P. Ziolkowski, D. Rakus, and M. Mann Absolute proteome analysis of colorectal mucosa, adenoma and cancer reveals drastic changes in fatty acid metabolism and plasma membrane transporters J Proteome Res 14 9 2015 4005 4018
12. Y. Uchida, S. Ohtsuki, J. Kamiie, K. Ohmine, R. Iwase, and T. Terasaki Quantitative targeted absolute proteomics for 28 human transporters in plasma membrane of Caco-2 cell monolayer cultured for 2, 3, and 4 weeks Drug Metab Pharmacokinet 30 2 2015 205 208
13. I. Simoff, M. Karlgren, M. Backlund, and et al. Complete knockout of endogenous Mdr1 (Abcb1) in MDCK cells by CRISPR-Cas9 J Pharm Sci 105 2016 1017 1021
14. P. Matsson, L.A. Fenu, P. Lundquist, J.R. Wiśniewski, M. Kansy, and P. Artursson Quantifying the impact of transporters on cellular drug permeability Trends Pharmacol Sci 36 5 2015 255 262
15. A. Kalliokoski, and M. Niemi Impact of OATP transporters on pharmacokinetics Br J Pharmacol 158 3 2009 693 705
16. K. Takeuchi, T. Sugiura, S. Umeda, and et al. Pharmacokinetics and hepatic uptake of eltrombopag, a novel platelet-increasing agent Drug Metab Dispos 39 6 2011 1088 1096
17. P. Annaert, Z. Ye, B. Stieger, and P. Augustijns Interaction of HIV protease inhibitors with OATP1B1, 1B3, and 2B1 Xenobiotica 40 3 2010 163 176
18. S. Tavelin, J. Gråsjö, J. Taipalensuu, G. Ocklind, and P. Artursson Applications of epithelial cell culture in studies of drug transport Methods Mol Biol 188 2002 233 272
19. J.R. Wiśniewski, and M. Mann Consecutive proteolytic digestion in an enzyme reactor increases depth of proteomic and phosphoproteomic analysis Anal Chem 84 6 2012 2631 2637
20. J.R. Wisniewski, A. Zougman, and M. Mann Combination of FASP and StageTip-based fractionation allows in-depth analysis of the hippocampal membrane proteome J Proteome Res 8 12 2009 5674 5678
21. J.R. Wiśniewski, and F.Z. Gaugaz Fast and sensitive total protein and peptide assays for proteomic analysis Anal Chem 87 8 2015 4110 4116
22. J.R. Wiśniewski, K. Duś, and M. Mann Proteomic workflow for analysis of archival formalin-fixed and paraffin-embedded clinical samples to a depth of 10,000 proteins Proteomics Clin Appl 7 3-4 2013 225 233
23. J. Cox, and M. Mann MaxQuant enables high peptide identification rates, individualized ppb-range mass accuracies and proteome-wide protein quantification Nat Biotechnol 26 12 2008 1367 1372
24. J.R. Wiśniewski, and D. Rakus Multi-enzyme digestion FASP and the 'Total Protein Approach'-based absolute quantification of the Escherichia coli proteome J Proteomics 109 2014 322 331
25. M. Ashburner, C.A. Ball, J.A. Blake, and et al. Gene Ontology: tool for the unification of biology Nat Genet 25 1 2000 25 29
26. S. Bauer, S. Grossmann, M. Vingron, and P.N. Robinson Ontologizer 2.0 - a multifunctional tool for GO term enrichment analysis and data exploration Bioinformatics 24 14 2008 1650 1651
27. H. Mi, A. Muruganujan, and P.D. Thomas PANTHER in 2013: modeling the evolution of gene function, and other gene attributes, in the context of phylogenetic trees Nucleic Acids Res 41 D1 2013 D377 D386
28. G. Englund, F. Rorsman, A. Rönnblom, and et al. Regional levels of drug transporters along the human intestinal tract: co-expression of ABC and SLC transporters and comparison with Caco-2 cells Eur J Pharml Sci 29 3 2006 269 277
29. G. Ahlin, C. Hilgendorf, J. Karlsson, C.A. Szigyarto, M. Uhlén, and P. Artursson Endogenous gene and protein expression of drug-transporting proteins in cell lines routinely used in drug discovery programs Drug Metab Dispos 37 12 2009 2275 2283
30. J. Taipalensuu, H. Törnblom, G. Lindberg, and et al. Correlation of gene expression of ten drug efflux proteins of the ATP-binding cassette transporter family in normal human jejunum and in human intestinal epithelial Caco-2 cell monolayers J Pharmacol Exp Ther 299 1 2001 164 170
31. A. Vildhede, M. Karlgren, E.K. Svedberg, and et al. Hepatic uptake of atorvastatin: influence of variability in transporter expression on uptake clearance and drug-drug interactions Drug Metab Dispos 42 7 2014 1210 1218
32. K. Sotaert, and T. Petzoldt Solving differential equations in R: Package deSolve J Stat Softw 33 2010 1 25
33. H. Lennernäs, Ö. Ahrenstedt, R. Hällgren, L. Knutson, M. Ryde, and L.K. Paalzow Regional jejunal perfusion, a new in vivo approach to study oral drug absorption in man Pharm Res 9 10 1992 1243 1251
34. H.F. Helander, and L. Fändriks Surface area of the digestive tract - revisited Scand J Gastroenterol 49 6 2014 681 689
35. S. Davis, J. Hardy, and J. Fara Transit of pharmaceutical dosage forms through the small intestine Gut 27 8 1986 886 892
36. M. Karlgren, A. Vildhede, U. Norinder, and et al. Classification of inhibitors of hepatic organic anion transporting polypeptides (OATPs): influence of protein expression on drug-drug interactions J Med Chem 55 10 2012 4740 4763
37. J.R. Wiśniewski, P. Ostasiewicz, K. Duś, D.F. Zielińska, F. Gnad, and M. Mann Extensive quantitative remodeling of the proteome between normal colon tissue and adenocarcinoma Mol Syst Biol 8 1 2012 611
38. N.M. Hooper Ectopeptidases K.L. Audus, T.J. Raub, Biological Barriers to Protein Delivery 1993 Plenum Press New York, NY 23 50
39. R. Holmes, and R. Lobley Intestinal brush border revisited Gut 30 12 1989 1667 1678
40. M. Takeichi Dynamic contacts: rearranging adherens junctions to drive epithelial remodelling Nat Rev Mol Cell Biol 15 6 2014 397 410
41. P. Artursson, and S.D. Knight Breaking the intestinal barrier to deliver drugs Science 347 6223 2015 716 717
42. P. Artursson, A.L. Ungell, and J.E. Löfroth Selective paracellular permeability in two models of intestinal absorption: cultured monolayers of human intestinal epithelial cells and rat intestinal segments Pharm Res 10 8 1993 1123 1129
43. J. Linnankoski, J. Mäkelä, J. Palmgren, and et al. Paracellular porosity and pore size of the human intestinal epithelium in tissue and cell culture models J Pharm Sci 99 4 2010 2166 2175
44. J.R. Turner, M.M. Buschmann, I. Romero-Calvo, A. Sailer, and L. Shen The role of molecular remodeling in differential regulation of tight junction permeability Semin Cell Dev Biol 36 2014 204 212
45. A. Tamura, and S. Tsukita Paracellular barrier and channel functions of TJ claudins in organizing biological systems: advances in the field of barriology revealed in knockout mice Semin Cell Dev Biol 36 2014 177 185
46. S. Maher, D.J. Brayden, L. Feighery, and S. McClean Cracking the junction: update on the progress of gastrointestinal absorption enhancement in the delivery of poorly absorbed drugs Crit Rev Ther Drug Carrier Syst 25 2 2008 117 168
47. A.G. Markov, A. Veshnyakova, M. Fromm, M. Amasheh, and S. Amasheh Segmental expression of claudin proteins correlates with tight junction barrier properties in rat intestine J Comp Physiol B 180 4 2010 591 598
48. M. Barczyk, S. Carracedo, and D. Gullberg Integrins Cell Tissue Res 339 1 2010 269 280
49. C. Lussier, N. Basora, Y. Bouatrouss, and J.F. Beaulieu Integrins as mediators of epithelial cell-matrix interactions in the human small intestinal mucosa Microsc Res Tech 51 2 2000 169 178
50. A. Bianchi-Smiraglia, S. Paesante, and A.V. Bakin Integrin β5 contributes to the tumorigenic potential of breast cancer cells through the Src-FAK and MEK-ERK signaling pathways Oncogene 32 25 2013 3049 3058
51. R.C. Bates, D.I. Bellovin, C. Brown, and et al. Transcriptional activation of integrin β6 during the epithelial-mesenchymal transition defines a novel prognostic indicator of aggressive colon carcinoma J Clin Invest 115 2 2005 339 347
52. A. Schrφder, K. Klein, S. Winter, and et al. Genomics of ADME gene expression: mapping expression quantitative trait loci relevant for absorption, distribution, metabolism and excretion of drugs in human liver Pharmacogenomics J 13 1 2013 12 20
53. L. Lin, S.W. Yee, R.B. Kim, and K.M. Giacomini SLC transporters as therapeutic targets: emerging opportunities Nat Rev Drug Discov 14 8 2015 543 560
54. V. Vasiliou, K. Vasiliou, and D.W. Nebert Human ATP-binding cassette (ABC) transporter family Hum Genomics 3 3 2009 281
55. A. Cιsar-Razquin, B. Snijder, T. Frappier-Brinton, and et al. A call for systematic research on solute carriers Cell 162 3 2015 478 487
56. P. Schmiedlin-Ren, K.E. Thummel, J.M. Fisher, M.F. Paine, K.S. Lown, and P.B. Watkins Expression of enzymatically active CYP3A4 by Caco-2 cells grown on extracellular matrix-coated permeable supports in the presence of 1α, 25-dihydroxyvitamin D3 Mol Pharmacol 51 5 1997 741 754
57. H.A. Engman, H. Lennernäs, J. Taipalensuu, C. Otter, B. Leidvik, and P. Artursson CYP3A4, CYP3A5, and MDR1 in human small and large intestinal cell lines suitable for drug transport studies J Pharm Sci 90 11 2001 1736 1751
58. K.E. Thummel, C. Brimer, K. Yasuda, and et al. Transcriptional control of intestinal cytochrome P-4503A by 1α, 25-dihydroxy vitamin D3 Mol Pharma 60 6 2001 1399 1406
59. J.Y. Chiang Bile acids: regulation of synthesis J Lipid Res 50 10 2009 1955 1966
60. M. Kumarakulasingham, P.H. Rooney, S.R. Dundas, and et al. Cytochrome p450 profile of colorectal cancer: identification of markers of prognosis Clin Cancer Res 11 10 2005 3758 3765
61. K. Stenstedt, M. Hallstrom, I. Johansson, M. Ingelman-Sundberg, P. Ragnhammar, and D. Edler The expression of CYP2W1: a prognostic marker in colon cancer Anticancer Res 32 9 2012 3869 3874
62. K.M. Giacomini, S.M. Huang, D.J. Tweedie, and et al. Membrane transporters in drug development Nat Rev Drug Discov 9 3 2010 215 236
63. K.M. Hillgren, D. Keppler, A. Zur, and et al. Emerging transporters of clinical importance: an update from the International Transporter Consortium Clin Pharmacol Ther 94 1 2013 52 63
64. Y. Sai, Y. Kaneko, S. Ito, and et al. Predominant contribution of organic anion transporting polypeptide OATP-B (OATP2B1) to apical uptake of estrone-3-sulfate by human intestinal Caco-2 cells Drug Metab Dispos 34 8 2006 1423 1431
65. R. Hayeshi, C. Hilgendorf, P. Artursson, and et al. Comparison of drug transporter gene expression and functionality in Caco-2 cells from 10 different laboratories Eur J Pharm Sci 35 5 2008 383 396
66. C. Vogel, and E.M. Marcotte Insights into the regulation of protein abundance from proteomic and transcriptomic analyses Nat Rev Genet 13 4 2012 227 232
67. N. Nagaraj, J.R. Wisniewski, T. Geiger, and et al. Deep proteome and transcriptome mapping of a human cancer cell line Mol Syst Biol 7 1 2011 548
68. M. Drozdzik, C. Groer, J. Penski, and et al. Protein abundance of clinically relevant multidrug transporters along the entire length of the human intestine Mol Pharma 11 10 2014 3547 3555
69. A. Vildhede, J.R. Wiśniewski, A. Norén, M. Karlgren, and P. Artursson Comparative proteomic analysis of human liver tissue and isolated hepatocytes with a focus on proteins determining drug exposure J Proteome Res 14 8 2015 3305 3314
70. Y. Saito Pitavastatin: an overview Atheroscler Suppl 12 3 2011 271 276
71. M.D. Harwood, M.R. Russell, S. Neuhoff, G. Warhurst, and A. Rostami-Hodjegan Lost in centrifugation: accounting for transporter protein losses in quantitative targeted absolute proteomics Drug Metab Dispos 42 10 2014 1766 1772
72. M. Uhlén, L. Fagerberg, B.M. Hallström, and et al. Tissue-based map of the human proteome Science 347 6220 2015 1260419
73. A. Uzozie, P. Nanni, T. Staiano, and et al. Sorbitol dehydrogenase overexpression and other aspects of dysregulated protein expression in human precancerous colorectal neoplasms: a quantitative proteomics study Mol Cell Proteomics 13 5 2014 1198 1218
74. T. Lindmark, Y. Kimura, and P. Artursson Absorption enhancement through intracellular regulation of tight junction permeability by medium chain fatty acids in Caco-2 cells J Pharmacol Exp Ther 284 1 1998 362 369
75. S. Tavelin, K. Hashimoto, J. Malkinson, L. Lazorova, I. Toth, and P. Artursson A new principle for tight junction modulation based on occludin peptides Mol Pharmacol 64 6 2003 1530 1540
76. R.J. Mrsny, G.T. Brown, K. Gerner-Smidt, and et al. A key claudin extracellular loop domain is critical for epithelial barrier integrity Am J Pathol 172 4 2008 905 915
77. L.M. Feighery, S.W. Cochrane, T. Quinn, and et al. Myosin light chain kinase inhibition: correction of increased intestinal epithelial permeability in vitro Pharma Res 25 6 2008 1377 1386
78. I.C. Teller, and J.-F. Beaulieu Interactions between laminin and epithelial cells in intestinal health and disease Expert Rev Mol Med 3 24 2001 1 18
79. F. Palmieri The mitochondrial transporter family SLC25: identification, properties and physiopathology Mol Aspects Med 34 2 2013 465 484
80. A. Chevrollier, D. Loiseau, P. Reynier, and G. Stepien Adenine nucleotide translocase 2 is a key mitochondrial protein in cancer metabolism Biochim Biophys Acta 1807 6 2011 562 567
81. V.A. van der Mark, D.R. de Waart, K.S. Ho-Mok, and et al. The lipid flippase heterodimer ATP8B1-CDC50A is essential for surface expression of the apical sodium-dependent bile acid transporter (SLC10A2/ASBT) in intestinal Caco-2 cells Biochim Biophys Acta 1842 12 2014 2378 2386
82. S. Hallén, A. Björquist, A. Östlund-Lindqvist, and G. Sachs Identification of a region of the ileal-type sodium/bile acid cotransporter interacting with a competitive bile acid transport inhibitor Biochemistry 41 50 2002 14916 14924
83. A. Dantzig, J. Hoskins, L. Tabas, and et al. Association of intestinal peptide transport with a protein related to the cadherin superfamily Science 264 5157 1994 430 433
84. T. Terada, K. Sawada, H. Saito, Y. Hashimoto, and K.I. Inui Functional characteristics of basolateral peptide transporter in the human intestinal cell line Caco-2 Am J Physiol 276 6 1999 G1435 G1441
85. A. Kunze, J. Huwyler, G. Camenisch, and B. Poller Prediction of organic anion-transporting polypeptide 1B1-and 1B3-mediated hepatic uptake of statins based on transporter protein expression and activity data Drug Metab Dispos 42 9 2014 1514 1521
86. B. Williamson, A. Soars, A. Owen, P. White, R. Riley, and M. Soars Dissecting the relative contribution of OATP1B1-mediated uptake of xenobiotics into human hepatocytes using siRNA Xenobiotica 43 10 2013 920 931
87. Y. Shirasaka, K. Suzuki, M. Shichiri, T. Nakanishi, and I. Tamai Intestinal absorption of HMG-CoA reductase inhibitor pitavastatin mediated by organic anion transporting polypeptide and P-glycoprotein/multidrug resistance 1 Drug Metab Pharmacokinet 26 2 2011 171 179
88. M. Hirano, K. Maeda, S. Matsushima, Y. Nozaki, H. Kusuhara, and Y. Sugiyama Involvement of BCRP (ABCG2) in the biliary excretion of pitavastatin Mol Pharmacol 68 3 2005 800 807
89. R. Elsby, C. Hilgendorf, and K. Fenner Understanding the critical disposition pathways of statins to assess drug-drug interaction risk during drug development: it's not just about OATP1B1 Clin Pharmacol Ther 92 5 2012 584 598
90. M. Mueckler, and B. Thorens The SLC2 (GLUT) family of membrane transporters Mol Aspects Med 34 2 2013 121 138