Comparative gene expression profiles of ABC transporters in brain microvessel endothelial cells and brain in five species including human

Pharmacological Research

Volumn 59, Issue 6, 2009, Pages 404-413

  Warren, Mark S ^a   Zerangue, Noa ^a   Woodford, Katie ^a   Roberts, Lori M ^a   Tate, Emily H ^a   Feng, Bo ^b   Li, Cheryl ^b   Feuerstein, Thomas J ^c   Gibbs, John ^b   Smith, Bill ^b   de Morais, Sonia M ^b   Dower, William J ^a   Koller, Kerry J ^a  

^a XenoPort Inc   (United States)

^b PFIZER INC   (United States)

^c UNIVERSITY OF FREIBURG   (Germany)

Author keywords

ABC Transporter; BBB; BMEC; Efflux; Multidrug resistance; P glycoprotein

Indexed keywords

ABC TRANSPORTER; ABC TRANSPORTER A2; ABC TRANSPORTER A3; ABC TRANSPORTER C1; ABC TRANSPORTER C10; ABC TRANSPORTER C2; ABC TRANSPORTER C3; ABC TRANSPORTER C4; ABC TRANSPORTER D3; ABC TRANSPORTER D4; ABC TRANSPORTER E1; ABC TRANSPORTER F1; ABC TRANSPORTER F2; ABC TRANSPORTER F3; ABC TRANSPORTER G1; BREAST CANCER RESISTANCE PROTEIN; MULTIDRUG RESISTANCE PROTEIN 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BLOOD BRAIN BARRIER; BRAIN CAPILLARY; CELL ISOLATION; CONTROLLED STUDY; COW; DRUG TRANSPORT; ENDOTHELIUM CELL; GENE EXPRESSION PROFILING; HUMAN; IMMUNOFLUORESCENCE MICROSCOPY; MOUSE; NONHUMAN; PRIORITY JOURNAL; RAT; REAL TIME POLYMERASE CHAIN REACTION; SPECIES DIFFERENCE; SWINE;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; BIOLOGICAL TRANSPORT; BLOOD-BRAIN BARRIER; BRAIN; CATTLE; ENDOTHELIAL CELLS; GENE EXPRESSION PROFILING; HUMANS; MICE; MICROVESSELS; RATS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SPECIES SPECIFICITY; SWINE;

EID: 65049090941     PISSN: 10436618     EISSN: 10961186     Source Type: Journal    
DOI: 10.1016/j.phrs.2009.02.007     Document Type: Article

References (65)

1. Miller D.S., Bauer B., and Hartz A.M. Modulation of P-glycoprotein at the blood-brain barrier: opportunities to improve central nervous system pharmacotherapy. Pharmacol Rev 60 (2008) 196-209
2. Ohtsuki S., and 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 24 (2007) 1745-1758
3. Nies A.T. The role of membrane transporters in drug delivery to brain tumors. Cancer Lett 254 (2007) 11-29
4. Obradovic T., Dobson G.G., Shingaki T., Kungu T., and Hidalgo I.J. Assessment of the first and second generation antihistamines brain penetration and role of P-glycoprotein. Pharm Res 24 (2007) 318-327
5. Lee Y.J., Kusuhara H., Jonker J.W., Schinkel A.H., and Sugiyama Y. Investigation of efflux transport of dehydroepiandrosterone sulfate and mitoxantrone at the mouse blood-brain barrier: a minor role of breast cancer resistance protein. J Pharmacol Exp Ther 312 (2005) 44-52
6. Kalvass J.C., Maurer T.S., and Pollack G.M. Use of plasma and brain unbound fractions to assess the extent of brain distribution of 34 drugs: comparison of unbound concentration ratios to in vivo P-glycoprotein efflux ratios. Drug Metab Dispos 35 (2007) 660-666
7. Dean M., Rzhetsky A., and Allikmets R. The human ATP-binding cassette (ABC) transporter superfamily. Genome Res 11 (2001) 1156-1166
8. Livak K.J., and Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods 25 (2001) 402-408
9. Yousif S., Marie-Claire C., Roux F., Scherrmann J.M., and Decleves X. Expression of drug transporters at the blood-brain barrier using an optimized isolated rat brain microvessel strategy. Brain Res 1134 (2007) 1-11
10. Roberts L.M., Black D.S., Raman C., Woodford K., Zhou M., Haggerty J.E., et al. Subcellular localization of transporters along the rat blood-brain barrier and blood-cerebral-spinal fluid barrier by in vivo biotinylation. Neuroscience 155 (2008) 423-438
11. Nies A.T., Jedlitschky G., Konig J., Herold-Mende C., Steiner H.H., Schmitt H.P., et al. Expression and immunolocalization of the multidrug resistance proteins, MRP1-MRP6 (ABCC1-ABCC6), in human brain. Neuroscience 129 (2004) 349-360
12. Eisenblatter T., Huwel S., and Galla H.J. Characterisation of the brain multidrug resistance protein (BMDP/ABCG2/BCRP) expressed at the blood-brain barrier. Brain Res 971 (2003) 221-231
13. Hori S., Ohtsuki S., Tachikawa M., Kimura N., Kondo T., Watanabe M., et al. Functional expression of rat ABCG2 on the luminal side of brain capillaries and its enhancement by astrocyte-derived soluble factor(s). J Neurochem 90 (2004) 526-536
14. Tachikawa M., Watanabe M., Hori S., Fukaya M., Ohtsuki S., Asashima T., et al. Distinct spatio-temporal expression of ABCA and ABCG transporters in the developing and adult mouse brain. J Neurochem 95 (2005) 294-304
15. Cooray H.C., Blackmore C.G., Maskell L., and Barrand M.A. Localisation of breast cancer resistance protein in microvessel endothelium of human brain. Neuroreport 13 (2002) 2059-2063
16. Kusuhara H., and Sugiyama Y. Efflux transport systems for drugs at the blood-brain barrier and blood-cerebrospinal fluid barrier (Part 1). Drug Discov Today 6 (2001) 150-156
17. Bronger H., Konig J., Kopplow K., Steiner H.H., Ahmadi R., Herold-Mende C., et al. ABCC drug efflux pumps and organic anion uptake transporters in human gliomas and the blood-tumor barrier. Cancer Res 65 (2005) 11419-11428
18. Borst P., de Wolf C., and van de Wetering K. Multidrug resistance-associated proteins 3, 4, and 5. Pflugers Arch 453 (2007) 661-673
19. Vulevic B., Chen Z., Boyd J.T., Davis Jr. W., Walsh E.S., Belinsky M.G., et al. Cloning and characterization of human adenosine 5'-triphosphate-binding cassette, sub-family A, transporter 2 (ABCA2). Cancer Res 61 (2001) 3339-3347
20. Mack J.T., Beljanski V., Tew K.D., and Townsend D.M. The ATP-binding cassette transporter ABCA2 as a mediator of intracellular trafficking. Biomed Pharmacother 60 (2006) 587-592
21. Chen Z.J., Vulevic B., Ile K.E., Soulika A., Davis Jr. W., Reiner P.B., et al. Association of ABCA2 expression with determinants of Alzheimer's disease. FASEB J 18 (2004) 1129-1131
22. Mace S., Cousin E., Ricard S., Genin E., Spanakis E., Lafargue-Soubigou C., et al. ABCA2 is a strong genetic risk factor for early-onset Alzheimer's disease. Neurobiol Dis 18 (2005) 119-125
23. Laing N.M., Belinsky M.G., Kruh G.D., Bell D.W., Boyd J.T., Barone L., et al. Amplification of the ATP-binding cassette 2 transporter gene is functionally linked with enhanced efflux of estramustine in ovarian carcinoma cells. Cancer Res 58 (1998) 1332-1337
24. Boonstra R., Timmer-Bosscha H., van Echten-Arends J., van der Kolk D.M., van den Berg A., de Jong B., et al. Mitoxantrone resistance in a small cell lung cancer cell line is associated with ABCA2 upregulation. Br J Cancer 90 (2004) 2411-2417
25. Steinbach D., Gillet J.P., Sauerbrey A., Gruhn B., Dawczynski K., Bertholet V., et al. ABCA3 as a possible cause of drug resistance in childhood acute myeloid leukemia. Clin Cancer Res 12 (2006) 4357-4363
26. Loscher W., and Potschka H. Role of drug efflux transporters in the brain for drug disposition and treatment of brain diseases. Prog Neurobiol 76 (2005) 22-76
27. Borst P., and Elferink R.O. Mammalian ABC transporters in health and disease. Annu Rev Biochem 71 (2002) 537-592
28. Lang T., Haberl M., Jung D., Drescher A., Schlagenhaufer R., Keil A., et al. Genetic variability, haplotype structures, and ethnic diversity of hepatic transporters MDR3 (ABCB4) and bile salt export pump (ABCB11). Drug Metab Dispos 34 (2006) 1582-1599
29. Cavadini P., Biasiotto G., Poli M., Levi S., Verardi R., Zanella I., et al. RNA silencing of the mitochondrial ABCB7 transporter in HeLa cells causes an iron-deficient phenotype with mitochondrial iron overload. Blood 109 (2007) 3552-3559
30. Pondarre C., Campagna D.R., Antiochos B., Sikorski L., Mulhern H., and Fleming M.D. Abcb7, the gene responsible for X-linked sideroblastic anemia with ataxia, is essential for hematopoiesis. Blood 109 (2007) 3567-3569
31. Bakos E., and Homolya L. Portrait of multifaceted transporter, the multidrug resistance-associated protein 1 (MRP1/ABCC1). Pflugers Arch 453 (2007) 621-641
32. Gazzin S., Strazielle N., Schmitt C., Fevre-Montange M., Ostrow J.D., Tiribelli C., et al. Differential expression of the multidrug resistance-related proteins ABCb1 and ABCc1 between blood-brain interfaces. J Comp Neurol 510 (2008) 497-507
33. Daood M., Tsai C., Ahdab-Barmada M., and Watchko J.F. ABC Transporter (P-gp/ABCB1, MRP1/ABCC1, BCRP/ABCG2) Expression in the Developing Human CNS. Neuropediatrics 39 (2008) 211-218
34. Soontornmalai A., Vlaming M.L., and Fritschy J.M. Differential, strain-specific cellular and subcellular distribution of multidrug transporters in murine choroid plexus and blood-brain barrier. Neuroscience 138 (2006) 159-169
35. van Vliet E.A., Redeker S., Aronica E., Edelbroek P.M., and Gorter J.A. Expression of multidrug transporters MRP1, MRP2, and BCRP shortly after status epilepticus, during the latent period, and in chronic epileptic rats. Epilepsia 46 (2005) 1569-1580
36. Sugiyama D., Kusuhara H., Lee Y.J., and Sugiyama Y. Involvement of multidrug resistance associated protein 1 (Mrp1) in the efflux transport of 17beta estradiol-D-17beta-glucuronide (E217betaG) across the blood-brain barrier. Pharm Res 20 (2003) 1394-1400
37. Rao V.V., Dahlheimer J.L., Bardgett M.E., Snyder A.Z., Finch R.A., Sartorelli A.C., et al. Choroid plexus epithelial expression of MDR1 P glycoprotein and multidrug resistance-associated protein contribute to the blood-cerebrospinal-fluid drug-permeability barrier. Proc Natl Acad Sci USA 96 (1999) 3900-3905
38. Wijnholds J., deLange E.C., Scheffer G.L., van den Berg D.J., Mol C.A., van der Valk M., et al. Multidrug resistance protein 1 protects the choroid plexus epithelium and contributes to the blood-cerebrospinal fluid barrier. J Clin Invest 105 (2000) 279-285
39. Cisternino S., Rousselle C., Lorico A., Rappa G., and Scherrmann J.M. Apparent lack of Mrp1-mediated efflux at the luminal side of mouse blood-brain barrier endothelial cells. Pharm Res 20 (2003) 904-909
40. Lee Y.J., Kusuhara H., and Sugiyama Y. Do multidrug resistance-associated protein-1 and -2 play any role in the elimination of estradiol-17 beta-glucuronide and 2, 4-dinitrophenyl-S-glutathione across the blood-cerebrospinal fluid barrier?. J Pharm Sci 93 (2004) 99-107
41. Kusuhara H., and Sugiyama Y. Efflux transport systems for drugs at the blood-brain barrier and blood-cerebrospinal fluid barrier (part 2). Drug Discov Today 6 (2001) 206-212
42. Miller D.S., Nobmann S.N., Gutmann H., Toeroek M., Drewe J., and Fricker G. Xenobiotic transport across isolated brain microvessels studied by confocal microscopy. Mol Pharmacol 58 (2000) 1357-1367
43. Johnson B.M., Zhang P., Schuetz J.D., and Brouwer K.L. Characterization of transport protein expression in multidrug resistance-associated protein (Mrp) 2-deficient rats. Drug Metab Dispos 34 (2006) 556-562
44. Xiong H., Turner K.C., Ward E.S., Jansen P.L., and Brouwer K.L. Altered hepatobiliary disposition of acetaminophen glucuronide in isolated perfused livers from multidrug resistance-associated protein 2-deficient TR(-) rats. J Pharmacol Exp Ther 295 (2000) 512-518
45. Zelcer N., van de Wetering K., Hillebrand M., Sarton E., Kuil A., Wielinga P.R., et al. Mice lacking multidrug resistance protein 3 show altered morphine pharmacokinetics and morphine-6-glucuronide antinociception. Proc Natl Acad Sci USA 102 (2005) 7274-7279
46. Belinsky M.G., Dawson P.A., Shchaveleva I., Bain L.J., Wang R., Ling V., et al. Analysis of the in vivo functions of Mrp3. Mol Pharmacol 68 (2005) 160-168
47. Russel F.G., Koenderink J.B., and Masereeuw R. Multidrug resistance protein 4 (MRP4/ABCC4): a versatile efflux transporter for drugs and signalling molecules. Trends Pharmacol Sci 29 (2008) 200-207
48. Madon J., Hagenbuch B., Landmann L., Meier P.J., and Stieger B. Transport function and hepatocellular localization of mrp6 in rat liver. Mol Pharmacol 57 (2000) 634-641
49. Belinsky M.G., Chen Z.S., Shchaveleva I., Zeng H., and Kruh G.D. Characterization of the drug resistance and transport properties of multidrug resistance protein 6 (MRP6, ABCC6). Cancer Res 62 (2002) 6172-6177
50. Chen Z.S., Hopper-Borge E., Belinsky M.G., Shchaveleva I., Kotova E., and Kruh G.D. Characterization of the transport properties of human multidrug resistance protein 7 (MRP7, ABCC10). Mol Pharmacol 63 (2003) 351-358
51. Hopper-Borge E., Chen Z.S., Shchaveleva I., Belinsky M.G., and Kruh G.D. Analysis of the drug resistance profile of multidrug resistance protein 7 (ABCC10): resistance to docetaxel. Cancer Res 64 (2004) 4927-4930
52. Berger J., Albet S., Bentejac M., Netik A., Holzinger A., Roscher A.A., et al. The four murine peroxisomal ABC-transporter genes differ in constitutive, inducible and developmental expression. Eur J Biochem 265 (1999) 719-727
53. Wanders R.J., Visser W.F., van Roermund C.W., Kemp S., and Waterham H.R. The peroxisomal ABC transporter family. Pflugers Arch 453 (2007) 719-734
54. Kerr I.D. Sequence analysis of twin ATP binding cassette proteins involved in translational control, antibiotic resistance, and ribonuclease L inhibition. Biochem Biophys Res Commun 315 (2004) 166-173
55. Chen Z.Q., Dong J., Ishimura A., Daar I., Hinnebusch A.G., and Dean M. The essential vertebrate ABCE1 protein interacts with eukaryotic initiation factors. J Biol Chem 281 (2006) 7452-7457
56. Dooher J.E., Schneider B.L., Reed J.C., and Lingappa J.R. Host ABCE1 is at plasma membrane HIV assembly sites and its dissociation from Gag is linked to subsequent events of virus production. Traffic 8 (2007) 195-211
57. Shichijo S., Ishihara Y., Azuma K., Komatsu N., Higashimoto N., Ito M., et al. ABCE1, a member of ATP-binding cassette transporter gene, encodes peptides capable of inducing HLA-A2-restricted and tumor-reactive cytotoxic T lymphocytes in colon cancer patients. Oncol Rep 13 (2005) 907-913
58. Yasui K., Mihara S., Zhao C., Okamoto H., Saito-Ohara F., Tomida A., et al. Alteration in copy numbers of genes as a mechanism for acquired drug resistance. Cancer Res 64 (2004) 1403-1410
59. Tyzack J.K., Wang X., Belsham G.J., and Proud C.G. ABC50 interacts with eukaryotic initiation factor 2 and associates with the ribosome in an ATP-dependent manner. J Biol Chem 275 (2000) 34131-34139
60. Richard M., Drouin R., and Beaulieu A.D. ABC50, a novel human ATP-binding cassette protein found in tumor necrosis factor-alpha-stimulated synoviocytes. Genomics 53 (1998) 137-145
61. Robey R.W., Polgar O., Deeken J., To K.W., and Bates S.E. ABCG2: determining its relevance in clinical drug resistance. Cancer Metastasis Rev 26 (2007) 39-57
62. Jonker J.W., Buitelaar M., Wagenaar E., Van Der Valk M.A., Scheffer G.L., Scheper R.J., et al. The breast cancer resistance protein protects against a major chlorophyll-derived dietary phototoxin and protoporphyria. Proc Natl Acad Sci USA 99 (2002) 15649-15654
63. Zaher H., Khan A.A., Palandra J., Brayman T.G., Yu L., and Ware J.A. Breast cancer resistance protein (Bcrp/abcg2) is a major determinant of sulfasalazine absorption and elimination in the mouse. Mol Pharm 3 (2006) 55-61
64. Merino G., Alvarez A.I., Pulido M.M., Molina A.J., Schinkel A.H., and Prieto J.G. Breast cancer resistance protein (BCRP/ABCG2) transports fluoroquinolone antibiotics and affects their oral availability, pharmacokinetics, and milk secretion. Drug Metab Dispos 34 (2006) 690-695
65. Breedveld P., Pluim D., Cipriani G., Wielinga P., van Tellingen O., Schinkel A.H., et al. The effect of Bcrp1 (Abcg2) on the in vivo pharmacokinetics and brain penetration of imatinib mesylate (Gleevec): implications for the use of breast cancer resistance protein and P-glycoprotein inhibitors to enable the brain penetration of imatinib in patients. Cancer Res 65 (2005) 2577-2582