Mass spectrometry-based targeted proteomics as a tool to elucidate the expression and function of intestinal drug transporters

AAPS Journal

Volumn 15, Issue 4, 2013, Pages 1128-1140

  Oswald, Stefan ^a   Gröer, Christian ^a   Drozdzik, Marek ^b   Siegmund, Werner ^a  

^a UNIVERSITY MEDICINE GREIFSWALD   (Germany)

^b POMERANIAN MEDICAL UNIVERSITY   (Poland)

Author keywords

drug transporters; intestinal; mass spectrometry; quantification; targeted proteomics

Indexed keywords

MESSENGER RNA; MULTIDRUG RESISTANCE ASSOCIATED PROTEIN 2; MULTIDRUG RESISTANCE PROTEIN; MULTIDRUG RESISTANCE PROTEIN 1; SOLUTE CARRIER ORGANIC ANION TRANSPORTER 1B1; SOLUTE CARRIER ORGANIC ANION TRANSPORTER 1B3;

ALGORITHM; COLON; DRUG ABSORPTION; DRUG TRANSPORT; DUODENUM; HUMAN; ILEUM; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; INTESTINE ABSORPTION; JEJUNUM; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; NONHUMAN; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEOMICS; REVIEW; VALIDITY; WESTERN BLOTTING;

AMINO ACID SEQUENCE; ANIMALS; GENE EXPRESSION REGULATION; GENE TARGETING; HUMANS; INTESTINES; MASS SPECTROMETRY; MEMBRANE TRANSPORT PROTEINS; MOLECULAR SEQUENCE DATA; PROTEOMICS;

EID: 84887994085     PISSN: 15507416     EISSN: None     Source Type: Journal    
DOI: 10.1208/s12248-013-9521-3     Document Type: Review

References (101)

1. Fisher MB, Labissiere G. The role of the intestine in drug metabolism and pharmacokinetics: an industry perspective. Curr Drug Metab. 2007;8(7):694-9.
2. Darwich AS, Neuhoff S, Jamei M, Rostami-Hodjegan A. Interplay of metabolism and transport in determining oral drug absorption and gut wall metabolism: a simulation assessment using the "Advanced Dissolution, Absorption, Metabolism (ADAM)" model. Curr Drug Metab. 2010;11(9):716-29.
3. Konig J, Muller F, Fromm MF. Transporters and drug-drug interactions: important determinants of drug disposition and effects. Pharmacol Rev. 2013;65(3):944-66.
4. Zhang Y, Benet LZ. The gut as a barrier to drug absorption: combined role of cytochrome P450 3A and P-glycoprotein. Clin Pharmacokinet. 2001;40(3):159-68.
5. Harwood MD, Neuhoff S, Carlson GL, Warhurst G, Rostami-Hodjegan A. Absolute abundance and function of intestinal drug transporters: a prerequisite for fully mechanistic in vitro-in vivo extrapolation of oral drug absorption. Biopharm Drug Dispos. 2013;34(1):2-28.
6. Bruyere A, Decleves X, Bouzom F, Ball K, Marques C, Treton X, et al. Effect of variations in the amounts of P-glycoprotein (ABCB1), BCRP (ABCG2) and CYP3A4 along the human small intestine on PBPK models for predicting intestinal first pass. Mol Pharm. 2010;7(5):1596-607.
7. Giacomini KM, Huang SM, Tweedie DJ, Benet LZ, Brouwer KL, Chu X, et al. Membrane transporters in drug development. Nat Rev Drug Discov. 2010;9(3):215-36.
8. Dresser GK, Bailey DG, Leake BF, Schwarz UI, Dawson PA, Freeman DJ, et al. Fruit juices inhibit organic anion transporting polypeptide-mediated drug uptake to decrease the oral availability of fexofenadine. Clin Pharmacol Ther. 2002;71(1):11-20.
9. Hamman MA, Bruce MA, Haehner-Daniels BD, Hall SD. The effect of rifampin administration on the disposition of fexofenadine. Clin Pharmacol Ther. 2001;69(3):114-21.
10. Kusuhara H, Miura M, Yasui-Furukori N, Yoshida K, Akamine Y, Yokochi M, et al. Effect of coadministration of single and multiple doses of rifampicin on the pharmacokinetics of fexofenadine enantiomers in healthy subjects. Drug Metab Dispos. 2013;41(1):206-13.
11. Oswald S, Haenisch S, Fricke C, Sudhop T, Remmler C, Giessmann T, et al. Intestinal expression of P-glycoprotein (ABCB1), multidrug resistance associated protein 2 (ABCC2), and uridine diphosphate-glucuronosyltransferase 1A1 predicts the disposition and modulates the effects of the cholesterol absorption inhibitor ezetimibe in humans. Clin Pharmacol Ther. 2006;79(3):206-17.
12. Oswald S, Giessmann T, Luetjohann D, Wegner D, Rosskopf D, Weitschies W, et al. Disposition and sterol-lowering effect of ezetimibe are influenced by single-dose coadministration of rifampin, an inhibitor of multidrug transport proteins. Clin Pharmacol Ther. 2006;80(5):477-85.
13. Rengelshausen J, Goggelmann C, Burhenne J, Riedel KD, Ludwig J, Weiss J, et al. Contribution of increased oral bioavailability and reduced nonglomerular renal clearance of digoxin to the digoxin-clarithromycin interaction. Br J Clin Pharmacol. 2003;56(1):32-8.
14. Schwarz UI, Gramatte T, Krappweis J, Oertel R, Kirch W. P-glycoprotein inhibitor erythromycin increases oral bioavailability of talinolol in humans. Int J Clin Pharmacol Ther. 2000;38(4):161-7.
15. Schwarz UI, Seemann D, Oertel R, Miehlke S, Kuhlisch E, Fromm MF, et al. Grapefruit juice ingestion significantly reduces talinolol bioavailability. Clin Pharmacol Ther. 2005;77(4):291-301.
16. Westphal K, Weinbrenner A, Zschiesche M, Franke G, Knoke M, Oertel R, et al. Induction of P-glycoprotein by rifampin increases intestinal secretion of talinolol in human beings: a new type of drug/drug interaction. Clin Pharmacol Ther. 2000;68(4):345-55.
17. Greiner B, Eichelbaum M, Fritz P, Kreichgauer HP, Von RO, Zundler J, et al. The role of intestinal P-glycoprotein in the interaction of digoxin and rifampin. J Clin Invest. 1999;104(2):147-53.
18. Hediger MA, Romero MF, Peng JB, Rolfs A, Takanaga H, Bruford EA. The ABCs of solute carriers: physiological, pathological and therapeutic implications of human membrane transport proteinsIntroduction. Pflugers Arch. 2004;447(5):465-8.
19. Tamai I. Oral drug delivery utilizing intestinal OATP transporters. Adv Drug Deliv Rev. 2012;64(6):508-14.
20. Paine MF, Hart HL, Ludington SS, Haining RL, Rettie AE, Zeldin DC. The human intestinal cytochrome P450 "pie". Drug Metab Dispos. 2006;34(5):880-6.
21. Riches Z, Stanley EL, Bloomer JC, Coughtrie MW. Quantitative evaluation of the expression and activity of five major sulfotransferases (SULTs) in human tissues: the SULT "pie". Drug Metab Dispos. 2009;37(11):2255-61.
22. Harbourt DE, Fallon JK, Ito S, Baba T, Ritter JK, Glish GL, et al. Quantification of human uridine-diphosphate glucuronosyl transferase 1A isoforms in liver, intestine, and kidney using nanobore liquid chromatography-tandem mass spectrometry. Anal Chem. 2012;84(1):98-105.
23. Barr WH, Zola EM, Candler EL, Hwang SM, Tendolkar AV, Shamburek R, et al. Differential absorption of amoxicillin from the human small and large intestine. Clin Pharmacol Ther. 1994;56(3):279-85.
24. Chan KK, Buch A, Glazer RD, John VA, Barr WH. Site-differential gastrointestinal absorption of benazepril hydrochloride in healthy volunteers. Pharm Res. 1994;11(3):432-7.
25. Gramatte T, Oertel R, Terhaag B, Kirch W. Direct demonstration of small intestinal secretion and site-dependent absorption of the beta-blocker talinolol in humans. Clin Pharmacol Ther. 1996;59(5):541-9.
26. Weitschies W, Bernsdorf A, Giessmann T, Zschiesche M, Modess C, Hartmann V, et al. The talinolol double-peak phenomenon is likely caused by presystemic processing after uptake from gut lumen. Pharm Res. 2005;22(5):728-35.
27. Mouly S, Paine MF. P-glycoprotein increases from proximal to distal regions of human small intestine. Pharm Res. 2003;20(10):1595-9.
28. Tachibana T, Kato M, Takano J, Sugiyama Y. Predicting drug-drug interactions involving the inhibition of intestinal CYP3A4 and P-glycoprotein. Curr Drug Metab. 2010;11(9):762-77.
29. Varma MV, Ambler CM, Ullah M, Rotter CJ, Sun H, Litchfield J, et al. Targeting intestinal transporters for optimizing oral drug absorption. Curr Drug Metab. 2010;11(9):730-42.
30. Englund G, Rorsman F, Ronnblom A, Karlbom U, Lazorova L, Grasjo J, 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 Pharm Sci. 2006;29(3-4):269-77.
31. Gutmann H, Hruz P, Zimmermann C, Beglinger C, Drewe J. Distribution of breast cancer resistance protein (BCRP/ABCG2) mRNA expression along the human GI tract. Biochem Pharmacol. 2005;70(5):695-9.
32. Hilgendorf C, Ahlin G, Seithel A, Artursson P, Ungell AL, Karlsson J. Expression of thirty-six drug transporter genes in human intestine, liver, kidney, and organotypic cell lines. Drug Metab Dispos. 2007;35(8):1333-40.
33. Meier Y, Eloranta JJ, Darimont J, Ismair MG, Hiller C, Fried M, et al. Regional distribution of solute carrier mRNA expression along the human intestinal tract. Drug Metab Dispos. 2007;35(4):590-4.
34. Nakamura T, Sakaeda T, Ohmoto N, Tamura T, Aoyama N, Shirakawa T, et al. Real-time quantitative polymerase chain reaction for MDR1, MRP1, MRP2, and CYP3A-mRNA levels in Caco-2 cell lines, human duodenal enterocytes, normal colorectal tissues, and colorectal adenocarcinomas. Drug Metab Dispos. 2002;30(1):4-6.
35. Nishimura M, Naito S. Tissue-specific mRNA expression profiles of human ATP-binding cassette and solute carrier transporter superfamilies. Drug Metab Pharmacokinet. 2005;20(6):452-77.
36. Seithel A, Karlsson J, Hilgendorf C, Bjorquist A, Ungell AL. Variability in mRNA expression of ABC- and SLC-transporters in human intestinal cells: comparison between human segments and Caco-2 cells. Eur J Pharm Sci. 2006;28(4):291-9.
37. Taipalensuu J, Tornblom H, Lindberg G, Einarsson C, Sjoqvist F, Melhus H, 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. 2001;299(1):164-70.
38. Thorn M, Finnstrom N, Lundgren S, Rane A, Loof L. Cytochromes P450 and MDR1 mRNA expression along the human gastrointestinal tract. Br J Clin Pharmacol. 2005;60(1):54-60.
39. Zimmermann C, Gutmann H, Hruz P, Gutzwiller JP, Beglinger C, Drewe J. Mapping of multidrug resistance gene 1 and multidrug resistance-associated protein isoform 1 to 5 mRNA expression along the human intestinal tract. Drug Metab Dispos. 2005;33(2):219-24.
40. Terada T, Shimada Y, Pan X, Kishimoto K, Sakurai T, Doi R, et al. Expression profiles of various transporters for oligopeptides, amino acids and organic ions along the human digestive tract. Biochem Pharmacol. 2005;70(12):1756-63.
41. Berggren S, Gall C, Wollnitz N, Ekelund M, Karlbom U, Hoogstraate J, et al. Gene and protein expression of P-glycoprotein, MRP1, MRP2, and CYP3A4 in the small and large human intestine. Mol Pharm. 2007;4(2):252-7.
42. Tucker TG, Milne AM, Fournel-Gigleux S, Fenner KS, Coughtrie MW. Absolute immunoquantification of the expression of ABC transporters P-glycoprotein, breast cancer resistance protein and multidrug resistance-associated protein 2 in human liver and duodenum. Biochem Pharmacol. 2012;83(2):279-85.
43. Tweedie D, Polli JW, Gil BE, Huang SM, Zhang L, Poirier A, et al. Transporter studies in drug development: experience to date and follow up on decision trees from the international transporter consortium. Clin Pharmacol Ther 2013; 94(1): 113-25.
44. Picotti P, Aebersold R. Selected reaction monitoring-based proteomics: workflows, potential, pitfalls and future directions. Nat Methods. 2012;9(6):555-66.
45. Gallien S, Duriez E, Domon B. Selected reaction monitoring applied to proteomics. J Mass Spectrom. 2011;46(3):298-312.
46. Balogh L, Kimoto E, Chupka J, Zhang H, Lai Y. Membrane protein quantification by peptide-based mass spectrometry approaches: studies on the organic anion-transporting polypeptide family. J Proteomics Bioinform 2012.
47. Deo AK, Prasad B, Balogh L, Lai Y, Unadkat JD. Interindividual variability in hepatic expression of the multidrug resistance-associated protein 2 (MRP2/ABCC2): quantification by liquid chromatography/tandem mass spectrometry. Drug Metab Dispos. 2012;40(5):852-5.
48. Ji C, Tschantz WR, Pfeifer ND, Ullah M, Sadagopan N. Development of a multiplex UPLC-MRM MS method for quantification of human membrane transport proteins OATP1B1, OATP1B3 and OATP2B1 in in vitro systems and tissues. Anal Chim Acta. 2012;717:67-76.
49. Kamiie J, Ohtsuki S, Iwase R, Ohmine K, Katsukura Y, Yanai K, et al. Quantitative atlas of membrane transporter proteins: development and application of a highly sensitive simultaneous LC/MS/MS method combined with novel in-silico peptide selection criteria. Pharm Res. 2008;25(6):1469-83.
50. Kawakami H, Ohtsuki S, Kamiie J, Suzuki T, Abe T, Terasaki T. Simultaneous absolute quantification of 11 cytochrome P450 isoforms in human liver microsomes by liquid chromatography tandem mass spectrometry with In silico target peptide selection. J Pharm Sci 2011; 100(1):341-52.
51. Li N, Nemirovskiy OV, Zhang Y, Yuan H, Mo J, Ji C, et al. Absolute quantification of multidrug resistance-associated protein 2 (MRP2/ABCC2) using liquid chromatography tandem mass spectrometry. Anal Biochem. 2008;380(2):211-22.
52. Li N, Palandra J, Nemirovskiy OV, Lai Y. LC-MS/MS mediated absolute quantification and comparison of bile salt export pump and breast cancer resistance protein in livers and hepatocytes across species. Anal Chem. 2009;81(6):2251-9.
53. Miliotis T, Ali L, Palm JE, Lundqvist AJ, Ahnoff M, Andersson TB, et al. Development of a highly sensitive method using liquid chromatography-multiple reaction monitoring to quantify membrane P-glycoprotein in biological matrices and relationship to transport function. Drug Metab Dispos. 2011;39(12):2440-9.
54. Niessen J, Jedlitschky G, Grube M, Bien S, Schwertz H, Ohtsuki S, et al. Human platelets express organic anion-transporting peptide 2B1, an uptake transporter for atorvastatin. Drug Metab Dispos. 2009;37(5):1129-37.
55. Ohtsuki S, Uchida Y, Kubo Y, Terasaki T. Quantitative targeted absolute proteomics-based ADME research as a new path to drug discovery and development: methodology, advantages, strategy, and prospects. J Pharm Sci. 2011;100(9):3547-59.
56. Ohtsuki S, Schaefer O, Kawakami H, Inoue T, Liehner S, Saito A, et al. Simultaneous absolute protein quantification of transporters, cytochromes P450, and UDP-glucuronosyltransferases as a novel approach for the characterization of individual human liver: comparison with mRNA levels and activities. Drug Metab Dispos. 2012;40(1):83-92.
57. Ohtsuki S, Ikeda C, Uchida Y, Sakamoto Y, Miller F, Glacial F, et al. Quantitative targeted absolute proteomic analysis of transporters, receptors and junction proteins for validation of human cerebral microvascular endothelial cell line hCMEC/D3 as a human blood-brain barrier model. Mol Pharm. 2013;10(1):289-96.
58. Prasad B, Lai Y, Lin Y, Unadkat JD. Interindividual variability in the hepatic expression of the human breast cancer resistance protein (BCRP/ABCG2): Effect of age, sex, and genotype. J Pharm Sci. 2013;102(3):787-93.
59. Qiu X, Bi YA, Balogh LM, Lai Y. Absolute measurement of species differences in sodium taurocholate cotransporting polypeptide (NTCP/Ntcp) and its modulation in cultured hepatocytes. J Pharm Sci 2013. doi: 10.1002/jps.23582.
60. Sakamoto A, Matsumaru T, Ishiguro N, Schaefer O, Ohtsuki S, Inoue T, et al. Reliability and robustness of simultaneous absolute quantification of drug transporters, cytochrome P450 enzymes, and Udp-glucuronosyltransferases in human liver tissue by multiplexed MRM/selected reaction monitoring mode tandem mass spectrometry with nano-liquid chromatography. J Pharm Sci. 2011;100(9):4037-43.
61. Sakamoto A, Matsumaru T, Yamamura N, Uchida Y, Tachikawa M, Ohtsuki S, et al. Quantitative expression of human drug transporter proteins in lung tissues: Analysis of regional, gender, and interindividual differences by liquid chromatography-tandem mass spectrometry. J Pharm Sci 2013 May 13. doi: 10.1002/jps.23606
62. Schaefer O, Ohtsuki S, Kawakami H, Inoue T, Liehner S, Saito A, et al. Absolute quantification and differential expression of drug transporters, cytochrome P450 enzymes, and UDP-glucuronosyltransferases in cultured primary human hepatocytes. Drug Metab Dispos. 2012;40(1):93-103.
63. Uchida Y, Ohtsuki S, Katsukura Y, Ikeda C, Suzuki T, Kamiie J, et al. Quantitative targeted absolute proteomics of human blood-brain barrier transporters and receptors. J Neurochem. 2011;117(2):333-45.
64. Zhang Y, Li N, Brown PW, Ozer JS, Lai Y. Liquid chromatography/tandem mass spectrometry based targeted proteomics quantification of P-glycoprotein in various biological samples. Rapid Commun Mass Spectrom. 2011;25(12):1715-24.
65. Englund G, Jacobson A, Rorsman F, Artursson P, Kindmark A, Ronnblom A. Efflux transporters in ulcerative colitis: decreased expression of BCRP (ABCG2) and Pgp (ABCB1). Inflamm Bowel Dis. 2007;13(3):291-7.
66. Wojtal KA, Eloranta JJ, Hruz P, Gutmann H, Drewe J, Staumann A, et al. Changes in mRNA expression levels of solute carrier transporters in inflammatory bowel disease patients. Drug Metab Dispos. 2009;37(9):1871-7.
67. von RO, Burk O, Fromm MF, Thon KP, Eichelbaum M, Kivisto KT. Cytochrome P450 3A4 and P-glycoprotein expression in human small intestinal enterocytes and hepatocytes: a comparative analysis in paired tissue specimens. Clin Pharmacol Ther. 2004;75(3):172-83.
68. Gygi SP, Rochon Y, Franza BR, Aebersold R. Correlation between protein and mRNA abundance in yeast. Mol Cell Biol. 1999;19(3):1720-30.
69. Giessmann T, May K, Modess C, Wegner D, Hecker U, Zschiesche M, et al. Carbamazepine regulates intestinal P-glycoprotein and multidrug resistance protein MRP2 and influences disposition of talinolol in humans. Clin Pharmacol Ther. 2004;76(3):192-200.
70. Giessmann T, Modess C, Hecker U, Zschiesche M, Dazert P, Kunert-Keil C, et al. CYP2D6 genotype and induction of intestinal drug transporters by rifampin predict presystemic clearance of carvedilol in healthy subjects. Clin Pharmacol Ther. 2004;75(3):213-22.
71. Haenisch S, May K, Wegner D, Caliebe A, Cascorbi I, Siegmund W. Influence of genetic polymorphisms on intestinal expression and rifampicin-type induction of ABCC2 and on bioavailability of talinolol. Pharmacogenet Genomics. 2008;18(4):357-65.
72. Glaeser H, Bailey DG, Dresser GK, Gregor JC, Schwarz UI, McGrath JS, et al. Intestinal drug transporter expression and the impact of grapefruit juice in humans. Clin Pharmacol Ther. 2007;81(3):362-70.
73. Haller S, Schuler F, Lazic SE, Bachir-Cherif D, Kramer SD, Parrott NJ, et al. Expression profiles of metabolic enzymes and drug transporters in the liver and along the intestine of beagle dogs. Drug Metab Dispos 2012; 40(8): 1603-10.
74. MacLean C, Moenning U, Reichel A, Fricker G. Closing the gaps: a full scan of the intestinal expression of p-glycoprotein, breast cancer resistance protein, and multidrug resistance-associated protein 2 in male and female rats. Drug Metab Dispos. 2008;36(7):1249-54.
75. Cao X, Gibbs ST, Fang L, Miller HA, Landowski CP, Shin HC, et al. Why is it challenging to predict intestinal drug absorption and oral bioavailability in human using rat model. Pharm Res. 2006;23(8):1675-86.
76. Alegria-Schaffer A, Lodge A, Vattem K. Performing and optimizing Western blots with an emphasis on chemiluminescent detection. Methods Enzymol. 2009;463:573-99.
77. MacPhee DJ. Methodological considerations for improving Western blot analysis. J Pharmacol Toxicol Methods. 2010;61(2):171-7.
78. Oswald S, Hintze D, Peter A, Keiser M, Siegmund W. Comparison of absolute protein quantification by Western blot and MRM-based mass spectrometric analysis. Proteomic Forum. 2011 (Abstract).
79. Charette SJ, Lambert H, Nadeau PJ, Landry J. Protein quantification by chemiluminescent Western blotting: elimination of the antibody factor by dilution series and calibration curve. J Immunol Methods. 2010;353(1-2):148-50.
80. Barr JR, Maggio VL, Patterson Jr DG, Cooper GR, Henderson LO, Turner WE, et al. Isotope dilution-mass spectrometric quantification of specific proteins: model application with apolipoprotein A-I. Clin Chem. 1996;42(10):1676-82.
81. Dass C, Kusmierz JJ, Desiderio DM. Mass spectrometric quantification of endogenous beta-endorphin. Biol Mass Spectrom. 1991;20(3):130-8.
82. Anderson L, Hunter CL. Quantitative mass spectrometric multiple reaction monitoring assays for major plasma proteins. Mol Cell Proteomics. 2006;5(4):573-88.
83. Barnidge DR, Dratz EA, Martin T, Bonilla LE, Moran LB, Lindall A. Absolute quantification of the G protein-coupled receptor rhodopsin by LC/MS/MS using proteolysis product peptides and synthetic peptide standards. Anal Chem. 2003;75(3):445-51.
84. Barnidge DR, Goodmanson MK, Klee GG, Muddiman DC. Absolute quantification of the model biomarker prostate-specific antigen in serum by LC-Ms/MS using protein cleavage and isotope dilution mass spectrometry. J Proteome Res. 2004;3(3):644-52.
85. Nesvizhskii AI, Aebersold R. Interpretation of shotgun proteomic data: the protein inference problem. Mol Cell Proteomics. 2005;4(10):1419-40.
86. Mead JA, Shadforth IP, Bessant C. Public proteomic MS repositories and pipelines: available tools and biological applications. Proteomics. 2007;7(16):2769-86.
87. Picotti P, Bodenmiller B, Mueller LN, Domon B, Aebersold R. Full dynamic range proteome analysis of S. cerevisiae by targeted proteomics. Cell. 2009;138(4):795-806.
88. Lange V, Picotti P, Domon B, Aebersold R. Selected reaction monitoring for quantitative proteomics: a tutorial. Mol Syst Biol. 2008;4:222.
89. Gröer C, Brück S, Balogh LM, Lai Y, Paulick A, Busemann A, et al. LC-MS/MS-based quantification of clinically relevant intestinal uptake and efflux transporter proteins. submitted 2013. doi: 10.1016/j.jpba.2013.07.031.
90. Drozdzik M, Penski J, Lapczuk I, Ostrowski M, Balogh LM, Lai Y, et al. Expression of clinically relevant drug transporter proteins along the entire human intestine. Clin Pharmacol Ther. 2013;93:S65.
91. Hubatsch I, Ragnarsson EG, Artursson P. Determination of drug permeability and prediction of drug absorption in Caco-2 monolayers. Nat Protoc. 2007;2(9):2111-9.
92. Hayeshi R, Hilgendorf C, Artursson P, Augustijns P, Brodin B, Dehertogh P, et al. Comparison of drug transporter gene expression and functionality in Caco-2 cells from 10 different laboratories. Eur J Pharm Sci. 2008;35(5):383-96.
93. Oswald S, Terhaag B, Siegmund W. In vivo probes of drug transport: commonly used probe drugs to assess function of intestinal P-glycoprotein (ABCB1) in humans. Handb Exp Pharmacol. 2011;201:403-47.
94. Bailey DG. Fruit juice inhibition of uptake transport: a new type of food-drug interaction. Br J Clin Pharmacol. 2010;70(5):645-55.
95. Shirasaka Y, Shichiri M, Mori T, Nakanishi T, Tamai I. Major active components in grapefruit, orange, and apple juices responsible for OATP2B1-mediated drug interactions. J Pharm Sci. 2013;102(1):280-8.
96. Sjoberg A, Lutz M, Tannergren C, Wingolf C, Borde A, Ungell AL. Comprehensive study on regional human intestinal permeability and prediction of fraction absorbed of drugs using the Ussing chamber technique. Eur J Pharm Sci. 2013;48(1-2):166-80.
97. Andreose JS, Fumagalli G, Sigworth FJ, Caplan MJ. Real-time detection of the surface delivery of newly synthesized membrane proteins. Proc Natl Acad Sci U S A. 1996;93(15):7661-6.
98. Hua W, Sheff D, Toomre D, Mellman I. Vectorial insertion of apical and basolateral membrane proteins in polarized epithelial cells revealed by quantitative 3D live cell imaging. J Cell Biol. 2006;172(7):1035-44.
99. Drozdzik M, Penski J, Lapczuk J, Ostrowski M, Siegmund W, Oswald S. Expression of drug metabolizing enzymes and transporter proteins along the entire human gastrointestinal tract. Clin Pharmacol Ther. 2012;91:S50.
100. Nishimura M, Yaguti H, Yoshitsugu H, Naito S, Satoh T. Tissue distribution of mRNA expression of human cytochrome P450 isoforms assessed by high-sensitivity real-time reverse transcription PCR. Yakugaku Zasshi. 2003;123(5):369-75.
101. Nishimura M, Naito S. Tissue-specific mRNA expression profiles of human phase I metabolizing enzymes except for cytochrome P450 and phase II metabolizing enzymes. Drug Metab Pharmacokinet. 2006;21(5):357-74.