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

Molecular Pharmaceutics

Volumn 10, Issue 1, 2013, Pages 289-296

  Ohtsuki, Sumio ^a,b   Ikeda, Chiemi ^a   Uchida, Yasuo ^a   Sakamoto, Yumi ^a   Miller, Florence ^c,d,e   Glacial, Fabienne ^c,d,e   Decleves, Xavier ^d,f   Scherrmann, Jean Michel ^d,f   Couraud, Pierre Olivier ^c,d,e   Kubo, Yoshiyuki ^a   Tachikawa, Masanori ^a   Terasaki, Tetsuya ^a  

^a TOHOKU UNIVERSITY   (Japan)

^b KUMAMOTO UNIVERSITY   (Japan)

^c INSTITUT COCHIN   (France)

^d CNRS   (France)

^e UNIVERSITÉ PARIS DESCARTES   (France)

^f INSERM   (France)

Author keywords

ATP binding cassette transporter; breast cancer resistant protein; claudin 5; human blood brain barrier; multidrug resistant protein 1; protein quantification; quantitative targeted absolute proteomics; receptor, junction protein; transporter

Indexed keywords

ABC TRANSPORTER A2; ABC TRANSPORTER A3; ABC TRANSPORTER A6; ABC TRANSPORTER A8; ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); ATA1 PROTEIN; BREAST CANCER RESISTANCE PROTEIN; CLAUDIN 5; EQUILIBRATIVE NUCLEOSIDE TRANSPORTER 1; GLUCOSE TRANSPORTER 1; GUANOSINE TRIPHOSPHATASE; INSULIN RECEPTOR; LAT1 PROTEIN; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; MEMBRANE PROTEIN; MONOCARBOXYLATE TRANSPORTER 1; MULTIDRUG RESISTANCE PROTEIN 1; MULTIDRUG RESISTANCE PROTEIN 4; TRANSFERRIN; UNCLASSIFIED DRUG;

ARTICLE; BLOOD BRAIN BARRIER; BRAIN BLOOD VESSEL; CELL MEMBRANE; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN TISSUE; LIMIT OF QUANTITATION; MICROVASCULAR ENDOTHELIAL CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEOMICS; UMBILICAL VEIN ENDOTHELIAL CELL;

BIOLOGICAL TRANSPORT; BLOOD-BRAIN BARRIER; CELL LINE; CELL MEMBRANE; CEREBROVASCULAR CIRCULATION; CEREBRUM; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MEMBRANE PROTEINS; MEMBRANE TRANSPORT PROTEINS; MICROVESSELS; MODELS, BIOLOGICAL; PROTEOME; PROTEOMICS;

EID: 84872159164     PISSN: 15438384     EISSN: 15438392     Source Type: Journal    
DOI: 10.1021/mp3004308     Document Type: Article

References (41)

1. Ohtsuki, S.; Terasaki, T. Contribution of carrier-mediated transport systems to the blood-brain barrier as a supporting and protecting interface for the brain; importance for CNS drug discovery and development Pharm. Res. 2007, 24 (9) 1745-1758
2. Kusuhara, H.; Sugiyama, Y. Active efflux across the blood-brain barrier: role of the solute carrier family NeuroRx 2005, 2 (1) 73-85
3. Mayerl, S.; Visser, T. J.; Darras, V. M.; Horn, S.; Heuer, H. Impact of Oatp1c1 deficiency on thyroid hormone metabolism and action in the mouse brain Endocrinology 2012, 153 (3) 1528-1537
4. Ohtsuki, S.; Yamaguchi, H.; Asashima, T.; Terasaki, T. Establishing a method to isolate rat brain capillary endothelial cells by magnetic cell sorting and dominant mRNA expression of multidrug resistance-associated protein 1 and 4 in highly purified rat brain capillary endothelial cells Pharm. Res. 2007, 24 (4) 688-694
5. Leino, R. L.; Gerhart, D. Z.; Drewes, L. R. Monocarboxylate transporter (MCT1) abundance in brains of suckling and adult rats: a quantitative electron microscopic immunogold study Brain Res. Dev. Brain Res. 1999, 113 (1-2) 47-54
6. Ohtsuki, S.; Kikkawa, T.; Hori, S.; Terasaki, T. Modulation and compensation of the mRNA expression of energy related transporters in the brain of glucose transporter 1-deficient mice Biol. Pharm. Bull. 2006, 29 (8) 1587-1591
7. Ohtsuki, S.; Yamaguchi, H.; Kang, Y. S.; Hori, S.; Terasaki, T. Reduction of L-type amino acid transporter 1 mRNA expression in brain capillaries in a mouse model of Parkinson's disease Biol. Pharm. Bull. 2010, 33 (7) 1250-1252
8. Che, C.; Yang, G.; Thiot, C.; Lacoste, M. C.; Currie, J. C.; Demeule, M.; Regina, A.; Beliveau, R.; Castaigne, J. P. New Angiopep-modified doxorubicin (ANG1007) and etoposide (ANG1009) chemotherapeutics with increased brain penetration J. Med. Chem. 2010, 53 (7) 2814-2824
9. Pardridge, W. M. Tyrosine hydroxylase replacement in experimental Parkinson's disease with transvascular gene therapy NeuroRx 2005, 2 (1) 129-138
10. Ito, S.; Ohtsuki, S.; Katsukura, Y.; Funaki, M.; Koitabashi, Y.; Sugino, A.; Murata, S.; Terasaki, T. Atrial natriuretic peptide is eliminated from the brain by natriuretic peptide receptor-C-mediated brain-to-blood efflux transport at the blood-brain barrier J. Cereb. Blood Flow Metab. 2011, 31 (2) 457-466
11. Warren, M. S.; Zerangue, N.; Woodford, K.; Roberts, L. M.; Tate, E. H.; Feng, B.; Li, C.; Feuerstein, T. J.; Gibbs, J.; Smith, B.; de Morais, S. M.; Dower, W. J.; Koller, K. J. Comparative gene expression profiles of ABC transporters in brain microvessel endothelial cells and brain in five species including human Pharmacol. Res. 2009, 59 (6) 404-413
12. 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) 3547-3559
13. Shawahna, R.; Uchida, Y.; Decleves, X.; Ohtsuki, S.; Yousif, S.; Dauchy, S.; Jacob, A.; Chassoux, F.; Daumas-Duport, C.; Couraud, P. O.; Terasaki, T.; Scherrmann, J. M. Transcriptomic and quantitative proteomic analysis of transporters and drug metabolizing enzymes in freshly isolated human brain microvessels Mol. Pharmaceutics 2011, 8 (4) 1332-1341
14. Uchida, Y.; Ohtsuki, S.; Katsukura, Y.; Ikeda, C.; Suzuki, T.; Kamiie, J.; Terasaki, T. Quantitative targeted absolute proteomics of human blood-brain barrier transporters and receptors J. Neurochem. 2011, 117 (2) 333-345
15. Carl, S. M.; Lindley, D. J.; Couraud, P. O.; Weksler, B. B.; Romero, I.; Mowery, S. A.; Knipp, G. T. ABC and SLC transporter expression and pot substrate characterization across the human CMEC/D3 blood-brain barrier cell line Mol. Pharmaceutics 2010, 7 (4) 1057-1068
16. Dauchy, S.; Miller, F.; Couraud, P. O.; Weaver, R. J.; Weksler, B.; Romero, I. A.; Scherrmann, J. M.; De Waziers, I.; Decleves, X. Expression and transcriptional regulation of ABC transporters and cytochromes P450 in hCMEC/D3 human cerebral microvascular endothelial cells Biochem. Pharmacol. 2009, 77 (5) 897-909
17. Poller, B.; Gutmann, H.; Krahenbuhl, S.; Weksler, B.; Romero, I.; Couraud, P. O.; Tuffin, G.; Drewe, J.; Huwyler, J. The human brain endothelial cell line hCMEC/D3 as a human blood-brain barrier model for drug transport studies J. Neurochem. 2008, 107 (5) 1358-1368
18. Weksler, B. B.; Subileau, E. A.; Perriere, N.; Charneau, P.; Holloway, K.; Leveque, M.; Tricoire-Leignel, H.; Nicotra, A.; Bourdoulous, S.; Turowski, P.; Male, D. K.; Roux, F.; Greenwood, J.; Romero, I. A.; Couraud, P. O. Blood-brain barrier-specific properties of a human adult brain endothelial cell line FASEB J. 2005, 19 (13) 1872-1874
19. Fasler-Kan, E.; Suenderhauf, C.; Barteneva, N.; Poller, B.; Gygax, D.; Huwyler, J. Cytokine signaling in the human brain capillary endothelial cell line hCMEC/D3 Brain Res. 2010, 1354, 15-22
20. Hurst, L. A.; Bunning, R. A.; Couraud, P. O.; Romero, I. A.; Weksler, B. B.; Sharrack, B.; Woodroofe, M. N. Expression of ADAM-17, TIMP-3 and fractalkine in the human adult brain endothelial cell line, hCMEC/D3, following pro-inflammatory cytokine treatment J. Neuroimmunol. 2009, 210 (1-2) 108-112
21. Joice, S. L.; Mydeen, F.; Couraud, P. O.; Weksler, B. B.; Romero, I. A.; Fraser, P. A.; Easton, A. S. Modulation of blood-brain barrier permeability by neutrophils: in vitro and in vivo studies Brain Res. 2009, 1298, 13-23
22. Lim, J. C.; Kania, K. D.; Wijesuriya, H.; Chawla, S.; Sethi, J. K.; Pulaski, L.; Romero, I. A.; Couraud, P. O.; Weksler, B. B.; Hladky, S. B.; Barrand, M. A. Activation of beta-catenin signalling by GSK-3 inhibition increases p-glycoprotein expression in brain endothelial cells J. Neurochem. 2008, 106 (4) 1855-1865
23. Luissint, A. C.; Federici, C.; Guillonneau, F.; Chretien, F.; Camoin, L.; Glacial, F.; Ganeshamoorthy, K.; Couraud, P. O. Guanine nucleotide-binding protein Galphai2: a new partner of claudin-5 that regulates tight junction integrity in human brain endothelial cells J. Cereb. Blood Flow Metab. 2012, 32 (5) 860-873
24. Schwanhausser, B.; Busse, D.; Li, N.; Dittmar, G.; Schuchhardt, J.; Wolf, J.; Chen, W.; Selbach, M. Global quantification of mammalian gene expression control Nature 2011, 473 (7347) 337-342
25. Ohtsuki, S.; Schaefer, O.; Kawakami, H.; Inoue, T.; Liehner, S.; Saito, A.; Ishiguro, N.; Kishimoto, W.; Ludwig-Schwellinger, E.; Ebner, T.; Terasaki, T. 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
26. Kamiie, J.; Ohtsuki, S.; Iwase, R.; Ohmine, K.; Katsukura, Y.; Yanai, K.; Sekine, Y.; Uchida, Y.; Ito, S.; Terasaki, T. 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) 1469-1483
27. Ito, S.; Ohtsuki, S.; Terasaki, T. Functional characterization of the brain-to-blood efflux clearance of human amyloid-beta peptide (1-40) across the rat blood-brain barrier Neurosci. Res. 2006, 56 (3) 246-252
28. Tamaki, C.; Ohtsuki, S.; Terasaki, T. Insulin facilitates the hepatic clearance of plasma amyloid beta-peptide (1 40) by intracellular translocation of low-density lipoprotein receptor-related protein 1 (LRP-1) to the plasma membrane in hepatocytes Mol. Pharmacol. 2007, 72 (4) 850-855
29. Cornford, E. M.; Hyman, S. Localization of brain endothelial luminal and abluminal transporters with immunogold electron microscopy NeuroRx 2005, 2 (1) 27-43
30. Pardridge, W. M. The blood-brain barrier: bottleneck in brain drug development NeuroRx 2005, 2 (1) 3-14
31. Seetharaman, S.; Barrand, M. A.; Maskell, L.; Scheper, R. J. Multidrug resistance-related transport proteins in isolated human brain microvessels and in cells cultured from these isolates J. Neurochem. 1998, 70 (3) 1151-1159
32. Kageyama, T.; Nakamura, M.; Matsuo, A.; Yamasaki, Y.; Takakura, Y.; Hashida, M.; Kanai, Y.; Naito, M.; Tsuruo, T.; Minato, N.; Shimohama, S. The 4F2hc/LAT1 complex transports L-DOPA across the blood-brain barrier Brain Res. 2000, 879 (1-2) 115-121
33. Leong, H. X.; Simkevich, C.; Lesieur-Brooks, A.; Lau, B. W.; Fugere, C.; Sabo, E.; Thompson, N. L. Short-term arginine deprivation results in large-scale modulation of hepatic gene expression in both normal and tumor cells: microarray bioinformatic analysis Nutr. Metab. 2006, 3, 37
34. Liu, X. M.; Reyna, S. V.; Ensenat, D.; Peyton, K. J.; Wang, H.; Schafer, A. I.; Durante, W. Platelet-derived growth factor stimulates LAT1 gene expression in vascular smooth muscle: role in cell growth FASEB J. 2004, 18 (6) 768-770
35. Boado, R. J.; Li, J. Y.; Tsukamoto, H.; Pardridge, W. M. Hypoxia induces de-stabilization of the LAT1 large neutral amino acid transporter mRNA in brain capillary endothelial cells J. Neurochem. 2003, 85 (4) 1037-1042
36. Piehler, A. P.; Ozcurumez, M.; Kaminski, W. E. A-Subclass ATP-Binding Cassette Proteins in Brain Lipid Homeostasis and Neurodegeneration Front. Psychiatry 2012, 3, 17
37. Yoshida, I.; Ban, N.; Inagaki, N. Expression of ABCA3, a causative gene for fatal surfactant deficiency, is up-regulated by glucocorticoids in lung alveolar type II cells Biochem. Biophys. Res. Commun. 2004, 323 (2) 547-555
38. Kim, W. S.; Guillemin, G. J.; Glaros, E. N.; Lim, C. K.; Garner, B. Quantitation of ATP-binding cassette subfamily-A transporter gene expression in primary human brain cells NeuroReport 2006, 17 (9) 891-896
39. Ito, K.; Uchida, Y.; Ohtsuki, S.; Aizawa, S.; Kawakami, H.; Katsukura, Y.; Kamiie, J.; Terasaki, T. Quantitative membrane protein expression at the blood-brain barrier of adult and younger cynomolgus monkeys J. Pharm. Sci. 2011, 100 (9) 3939-3950
40. Ciccimaro, E.; Hanks, S. K.; Yu, K. H.; Blair, I. A. Absolute quantification of phosphorylation on the kinase activation loop of cellular focal adhesion kinase by stable isotope dilution liquid chromatography/mass spectrometry Anal. Chem. 2009, 81 (9) 3304-3313
41. Domanski, D.; Murphy, L. C.; Borchers, C. H. Assay development for the determination of phosphorylation stoichiometry using multiple reaction monitoring methods with and without phosphatase treatment: application to breast cancer signaling pathways Anal. Chem. 2010, 82 (13) 5610-5620