Cellular localization and functional expression of P-glycoprotein in rat astrocyte cultures

Journal of Neurochemistry

Volumn 89, Issue 3, 2004, Pages 788-800

  Ronaldson, Patrick T ^a   Bendayan, Moise ^b   Gingras, Diane ^b   Piquette Miller, Micheline ^a   Bendayan, Reina ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Astrocytes; Brain parenchyma; Caveolin 1; Drug transport; Multidrug resistance; P glycoprotein

Indexed keywords

2,4 DINITROPHENOL; ADENOSINE TRIPHOSPHATE; CAVEOLIN 1; CYCLOSPORIN A; DIGOXIN; GLYCOPROTEIN P; INDINAVIR; MANNITOL; MESSENGER RNA; MONOCLONAL ANTIBODY; MULTIDRUG RESISTANCE PROTEIN 1; MULTIDRUG RESISTANCE PROTEIN 1B; QUINIDINE; RITONAVIR; SAQUINAVIR; UNCLASSIFIED DRUG; VALSPODAR; VERAPAMIL;

ANIMAL CELL; ARTICLE; ASTROCYTE; BRAIN CORTEX; CAVEOLA; CELL IMMORTALIZATION; CELL MEMBRANE; CELL NUCLEUS MEMBRANE; CELLULAR DISTRIBUTION; CHO CELL; COATED VESICLE; CONTROLLED STUDY; DRUG TRANSPORT; IMMUNOCYTOCHEMISTRY; IMMUNOPRECIPITATION; MULTIDRUG RESISTANCE; NEWBORN; NONHUMAN; PARENCHYMA; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ANIMALIA; RATTUS NORVEGICUS;

EID: 2042451616     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2004.02417.x     Document Type: Article

References (68)

1. Anderson C. M. and Swanson R. A. (2000) Astrocyte glutamate transport: review of properties, regulation, and physiological functions. Glia 32, 1-14.
2. Baldini N., Scotlandi K., Serra M., Shikita T., Zini N., Ognibene A., Santi S., Ferracini R. and Maraldi N. M. (1995) Nuclear immunolocalization of P-glycoprotein in multidrug-resistant cell lines showing similar mechanisms of doxorubicin distribution. Eur J. Cell Biol. 68, 226-239.
3. Ballerini P., Di Iorio P., Ciccarelli R., Nargi E., D'Alimonte I., Traversa U., Rathbone M. P. and Caciagli F. (2002) Glial cells express multiple ATP binding cassette proteins which are involved in ATP release. Neuroreport 13, 1789-1792.
4. Beaulieu E., Demeule M., Ghitescu L. and Beliveau R. (1997) P-glycoprotein is strongly expressed in the luminal membranes of the endothelium of blood vessels in the brain. Biochem. J. 326,539-544.
5. Bendayan M. (1995) Colloidal gold post-embedding immunocytochemistry. Prog. Histochem. Cytochem. 29, 1-159.
6. Bendayan R., Lee G. and Bendayan M. (2002) Functional expression and localization of P-glycoprotein at the blood brain barrier. Microsc. Res. Tech. 57, 365-380.
7. Bender A. S., Reichelt W. and Norenberg M. D. (2000) Characterization of cystine uptake in cultured astrocytes. Neurochem. Int. 37, 269-276.
8. Borst P. and Schinkel A. H. (1997) Genetic dissection of the function of mammalian P-glycoproteins. Trends Genet. 13, 217-222.
9. Bradford M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
10. Cameron P. L., Ruffin J. W., Bollag R., Rasmussen H. and Cameron R. S. (1997) Identification of caveolin and caveolin-related proteins in the brain. J. Neurosci. 17, 9520-9535.
11. Cameron P. L., Liu C., Smart D. K., Hantus S. T., Fick J. R. and Cameron R. S. (2002) Caveolin-1 expression is maintained in rat and human astroglioma cell lines. Glia 37, 275-290.
12. Chaillou S., Durant J., Garraffo R., Georgenthum E., Roptin C., Dunais B., Mondain Y., Roger P. M. and Dellamonica P. (2002) Intracellular concentration of protease inhibitors in HIV-1 infected patients: correlation with MDR-1 gene expression and low dose ritonavir. HIV Clin. Trials 3, 493-501.
13. Chiu F. C., Norton W. T. and Fields K. L. (1981) The cytoskeleton of primary astrocytes in culture contains actin, glial fibrillary acidic protein, and the fibroblast-type filament protein, vimentin. J. Neurochem. 37, 147-155.
14. Cole R. and de Vellis J. (2001) Preparation of astrocyte, oligodendrocytes, and microglia cultures from primary rat cerebral cultures, in Protocols for Neural Cell Culture (Fedoroff, S. and Richardson, A., eds), 3rd edn, pp. 117-128. Humana Press, Inc., Totowa.
15. Coley H. M., Amos W. B., Twentyman P. R. and Workman P. (1993) Examination by laser scanning confocal fluorescence imaging microscopy of the subcellular localization of anthracyclines in parent and multidrug resistant cell lines. Br J. Cancer 67, 1316-1323.
16. Conet J., Li S., Okamoto T., Ikezu T. and Lisanti M. P. (1997) Identification of peptide and protein ligands for the caveolin-scaffolding domain. Implications for the interaction of caveolin with caveolae-associated proteins. J. Biol. Chem. 272, 6525-6533.
17. Dallas S., Zhu X., Baruchel S., Schlichter L. and Bendayan R. (2003) Functional expression of the multidrug resistance protein 1 (MRP1) in microglia. J. Pharmacol. Exp. Ther. 307, 282-290.
18. De Lannoy I. A. and Silverman M. (1992) The MDR1 gene product, P-glycoprotein, mediates the transport of the cardiac glycoside, digoxin. Biochem. Biophys. Res. Commun. 189, 551-557.
19. Decleves X., Regina, A., Laplanche J. L., Roux F., Boval B., Launay J. M. and Scherrmann J. M. (2000) Functional expression of P-glycoprotein and multidrug resistance-associated protein (Mrp1) in primary cultures of rat astrocytes. J. Neurosci. Res. 60, 594-601.
20. Decleves X., Fajac A., Lehmann-Che J., Tardy M., Mercier C., Hurbain I., Lapanche J. L., Bemaudin J. F. and Scherrmann J. M. (2002) Molecular and functional MDR1-Pgp and MRPs expression in human glioblastoma multiforme cell lines. Int. J. Cancer 98, 173-180.
21. Demeule M., Jodoin J., Gingras D. and Beliveau R. (2000) P-glycoprotein is localized in caveolae in resistant cells and in brain capillaries. FEBS Lett. 466, 219-224.
22. Demeule M., Shedid D., Beaulieu E., Del Maestro R. F., Moghrali A., Ghosn P. B., Moumdijan R., Berthelet F. and Beliveau R. (2001) Expression of multidrug-resistance P-glycoprotein (MDR1) in human brain tumors. Int. J. Cancer 93, 62-66.
23. DiDiodato G. and Sharom F. J. (1997) Interaction of combinations of drugs, chemosensitizers, and peptides with the P-glycoprotein multidrug transporter. Biochem. Pharmacol. 53, 1789-1797.
24. Doige C. A. and Sharom F. J. (1992) Transport properties of P-glycoprotein in plasma membrane vesicles from multidrug-resistant Chinese hamster ovary cells. Biochim. Biophys. Acta 1109, 161-171.
25. Drion N., Risede P., Cholet N., Chanez C. and Scherrmann J. M. (1997) Role of P-170 glycoprotein in colchicine brain uptake. J. Neurosci. Res. 49, 80-88.
26. Fromm M. F. (2000) P-glycoprotein: a defense mechanism limiting oral bioavailability and CNS accumulation of drugs. Int. J. Clin. Pharmacol. Ther. 38, 69-74.
27. Fromm M. F., Kim R. B., Stein C. M., Wilkinson G. R. and Roden D. M. (1999) Inhibition of P-glycoprotein-mediated drug transport: a unifying mechanism to explain the reaction between digoxin and quinidine. Circulation 99, 552-557.
28. Georges E., Tsuruo T. and Ling V. (1993) Topology of P-glycoprotein as determined by epitope mapping of MRK-16 monoclonal antibody. J. Biol. Chem. 268, 1792-1798.
29. Golden P. L. and Pardridge W. M. (1999) P-glycoprotein on astrocyte foot processes of unfixed isolated human brain capillaries. Brain Res. 819, 143-146.
30. Gottesman M. M., Hrycyna C. A., Schoenlein P. V., Germann U. A. and Pastan I. (1995) Genetic analysis of the multidrug transporter. Annu. Rev. Genet. 29, 607-649.
31. Hirrlinger J., Konig J. and Dringen R. (2002) Expression of mRNAs of multidrug resistance proteins (Mrps) in cultured rat astrocytes, oligodendrocytes, microglial cells and neurones. J. Neurochem. 82, 716-719.
32. +-dependent nucleoside transporter in microglia. J. Pharmacol. Exp. Ther. 292, 366-374.
33. Hong M., Schlichter L. and Bendayan R. (2001) A novel zidovudine uptake system in microglia. J. Pharmacol. Exp. Ther. 296, 141-149.
34. Ikezu T., Ueda H., Trapp B. D. et al. (1998) Affinity-purification and characterization of caveolins from the brain: differential expression of caveolin-1,-2, and -3 in brain endothelial and astroglial cell types. Brain Res. 804, 177-192.
35. Jette L., Tetu B. and Beliveau R. (1993) High levels of P-glycoprotein detected in isolated brain capillaries. Biochim. Biophys. Acta 1150, 147-154.
36. Jodoin J., Demeule M., Fenart L., Cecchelli R., Farmer S., Linton K. J., Higgins C. F. and Beliveau R. (2003) P-glycoprotein in blood-brain barrier endothelial cells: interaction and oligomerization with caveolins. J. Neurochem. 87, 1010-1023.
37. Juliano R. L. and Ling V. (1976) A surface glycoprotein modulating drug permeability in Chinese hamster ovary cell mutants. Biochim. Biophys. Acta 455, 152-162.
38. Kim R. B., Fromm M. F., Wandel C., Leake B., Wood A. J., Roden D. M. and Wilkinson G. R. (1998) The drug transporter P-glycoprotein limits oral absorption and brain entry of HIV-1 protease inhibitors. J. Clin. Invest. 101, 289-294.
39. Lavie Y., Fiucci G. and Liscovitch M. (1998) Up-regulation of caveolae and caveolar constituents in Multidrug-resistant cancer cells. J. Biol. Chem. 273, 32380-32383.
40. Lavie Y., Fiucci G. and Liscovitch M. (2001) Upregulation of caveolin in multidrug resistant cancer cells: functional implications. Adv. Drug Deliv. Rev. 49, 317-323.
41. Lee G., Dallas S., Hong M. and Bendayan R. (2001a) Drug transporters in the central nervous system: brain barriers and brain parenchyma considerations. Pharmacol. Rev. 53, 569-596.
42. Lee G., Schlichter L., Bendayan M. and Bendayan R. (2001b) Functional expression of P-glycoprotein in rat brain microglia. J. Pharmacol. Exp. Ther. 299, 204-212.
43. Mayer U., Wagenaar E., Dorobek B., Beijnen J. H., Borst P. and Schinkel A. H. (1997) Full blockade of intestinal P-glycoprotein and extensive inhibition of blood-brain barrier P-glycoprotein by oral treatment of mice with PSC833. J. Clin. Invest. 100, 2430-2436.
44. Miller R. H., Ffrench-Constant C. and Raff M. C. (1989) The macroglial cells of the rat optic nerve. Ann. Rev. Neurosci. 12, 517-534.
45. Nutt C. L., Noble M., Chambers A. F. and Cairncross J. G. (2000) Differential expression of drug resistance genes and chemosensitivity in glial cell lineages correlate with differential response of oligodendrogliomas and astrocytomas to chemotherapy. Cancer Res. 60, 4812-4818.
46. Okochi E., Iwahashi T. and Tsuruo T. (1997) Monoclonal antibodies specific for P-glycoprotein. Leukemia 11, 1119-1123.
47. Pardridge W. M., Golden P. L., Kang Y. S. and Bickel U. (1997) Brain microvascular and astrocyte localization of P-glycoprotein. J. Neurochem. 68, 1278-1285.
48. Parkinson F. E., Sinclair C. J., Othman T., Haughey N. J. and Geiger J. D. (2002) Differences between rat primary cortical neurons and astrocytes in purine release evoked by ischemic conditions. Neuropharmacology 43, 836-846.
49. Perraud F., Labourdette G., Eclancher F. and Sensenbrenner M. (1990) Primary cultures of astrocytes from different brain areas of newborn rats and effects of basic fibroblast growth factor. Dev. Neurosci. 12, 11-21.
50. Radany E. H., Brenner M., Besnard F., Bigornia V., Bishop J. M. and Deschepper C. F. (1992) Directed establishment of rat brain cell lines with the phenotypic characteristics of type 1 astrocytes. Proc. Natl Acad. Sci. USA 89, 6467-6471.
51. Rao V. V., Dahlheimer J. L., Bardgett M. E., Snyder A. Z., Finch R. A., Sartorelli A. C. and Piwnica-Worms D. (1999) Choroid plexus epithelial expression of MDR1 P-glycoprotein and multidrug resistance-associated protein contribute to the blood-cerebrospinal fluid permeability barrier. Proc. Natl Acad. Sci. USA 96, 3900-3905.
52. Regina A., Koman A., Piciotti M., El Hafny B., Center M. S., Bergmann R., Couraud P. O. and Roux F. (1998) Mrp1 multidrug resistance-associated protein and P-glycoprotein expression in rat brain microvessel endothelial cells. J. Neurochem. 71, 705-715.
53. Robenek M. J., Schlattmann K., Zimmer K. P., Plenz G., Troyer D. and Robenek H. (2003) Cholesterol transporter caveolin-1 transits the lipid bilayer during intracellular cycling. FASEB J. 17, 1940-1942.
54. Roux F., Durieu-Trautmann O., Chaverot N., Claire M., Mailly P., Bourre J. M., Strosberg A. D. and Couraud P. O. (1994) Regulation of gamma-glutamyl transpeptidase and alkaline phosphatase activities in immortalized rat brain microvessel endothelial cells. J. Cell Physiol. 159, 101-113.
55. Schinkel A. H., Mayer U., Wagenaar E. et al. (1997) Normal viability and altered pharmacokinetics in mice lacking mdr1-type (drug-transporting) P-glycoproteins. Proc. Natl Acad. Sci. USA 94, 4028-4033.
56. Schlachetzki F. and Pardridge W. M. (2003) P-glycoprotein and caveolin-1α in endothelium and astrocytes of primate brain. Neuroreport 14, 2041-2046.
57. Schnitzer J. E., Oh P., Pinney E. and Allard J. (1994) Filipin-sensitive caveolae-mediated transport in endothelium: reduced transcytosis, scavenger endocytosis, and capillary permeability of select macromolecules. J. Cell Biol. 127, 1217-1232.
58. Shapiro A. B., Fox K., Lee P., Yang Y. D. and Ling V. (1998) Functional intracellular P-glycoprotein. Int. J. Cancer 76, 857-864.
59. Sinclair C. J., LaRiviere C. G., Young J. D., Cass C. E., Baldwin S. A. and Parkinson F. E. (2000) Purine uptake and release in rat C6 glioma cells: nucleoside transport and purine metabolism under ATP-depleting conditions. J. Neurochem. 75, 1528-1538.
60. Sisodiya S. M., Lin W. R., Harding B. R., Squier M. V. and Thom M. (2002) Drug resistance in epilepsy: expression of drug resistance proteins in common causes of refractory epilepsy. Brain 125, 22-31.
61. Smit J. J., Schinkel A. H., Oude Elferink R. P., Groen A. K., Wagenaar E., van Deemter L., Mol C. A., Ottenhoff R., van der Lugt N. M. and van Roon M. A. (1993) Homozygous disruption of the murine mdr2 P-glycoprotein expressed in a porcine kidney epithelial cell line LLC-PK1. Cell 75, 451-462.
62. Spiegl-Kreinecker S., Buchroithner J., Elbling L., Steiner E., Wurm G., Bodenteich A., Fischer J., Micksche M. and Berger W. (2002) Expression and functional activity of the ABC-transporter proteins P-glycoprotein and multidrug-resistance protein 1 in human brain tumor cells and astrocytes. J. Neurooncol. 57, 27-36.
63. Tanaka J. and Maeda N. (1996) Microglial ramification requires non-diffusible factors derived from astrocytes. Exp. Neurol. 137, 367-375.
64. Tishler D. M., Weinber K. I., Hinton D. R., Barbaro N., Annett G. M. and Raffel C. (1995) MDR1 gene expression in brain of patients with medically intractable epilepsy. Epilepsia 36, 1-6.
65. Ueda K., Cardarelli C., Gottesman M. M. and Pastan I. (1987) Expression of a full length cDNA for the human 'MDR1' gene confers resistance to colchicine, doxorubicin, and vinblastine. Proc. Natl Acad. Sci. USA 84, 3004-3008.
66. Van der Sandt I. C., Vos C. M., Nabulsi L., Blom-Roosemalen M. C., Voorwinden H. H., de Boer A. G. and Breimer D. D. (2001) Assessment of active transport of HIV protease inhibitors in various cell lines and the in vitro blood-brain barrier. AIDS 15, 483-491.
67. Virgintino D., Robertson D., Errede M., Benagiano V., Girolamo F., Maiorano E., Roncali L. and Bertossi M. (2002a) Expression of P-glycoprotein in human cerebral cortex microvessels. J. Histochem. Cytochem. 50, 1671-1676.
68. Virgintino D., Robertson D., Errede M., Benagiano V., Tauer U., Roncali L. and Bertossi M. (2002b) Expression of caveolin-1 in human brain microvessels. Neuroscience 115, 145-152.