Mrp1 multidrug resistance-associated protein and P-glycoprotein expression in rat brain microvessel endothelial cells

Journal of Neurochemistry

Volumn 71, Issue 2, 1998, Pages 705-715

  Regina, Anthony ^a   Koman, Ahmet ^b   Piciotti, Michèle ^a   El Hafny, Bouchra ^a   Center, Melvin S ^c   Bergmann, Ralf ^d   Couraud, Pierre Olivier ^b   Roux, Françoise ^a  

^a HÔPITAL FERNAND WIDAL   (France)

^b INSTITUT COCHIN   (France)

^c KANSAS STATE UNIVERSITY   (United States)

^d INSTITUTE OF ION BEAM PHYSICS AND MATERIALS RESEARCH   (Germany)

Author keywords

Blood brain barrier; Multidrug resistance associated protein; P glycoprotein; Primary cell culture; Rat brain microvessel endothelium; RBE4 cells

Indexed keywords

COLCHICINE; GLYCOPROTEIN P; ISOPROTEIN; MESSENGER RNA; MULTIDRUG RESISTANCE PROTEIN; VINBLASTINE; VINCRISTINE;

ANIMAL CELL; ARTICLE; ASTROCYTE; BLOOD BRAIN BARRIER; BRAIN BLOOD VESSEL; BRAIN CELL; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNOBLOTTING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VASCULAR ENDOTHELIUM;

ANIMALIA;

EID: 0031724003     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.1998.71020705.x     Document Type: Article

References (56)

1. Abbott N. J., Hughes C. C. W., Revest P. A., and Greenwood J. (1992) Development and characterisation of a rat brain capillary endothelial culture: towards an in vitro blood-brain barrier. J. Cell Sci. 103, 23-37.
2. Barrand M. A., Heppell-Parton A. C., Wright K. A., Rabbitts P. H., and Twentyman P. R. (1994) A 190-kilodalton protein overexpressed in non-P-glycoprotein-containing multidrug-resistant cells and its relationship to the MRP gene. J. Natl. Cancer Inst. 86, 110-117.
3. Barrand M. A., Robertson K. J., and von Weikersthal S. F. (1995) Comparisons of P-glycoprotein expression in isolated rat brain microvessels and in primary cultures of endothelial cells derived from microvasculature of rat brain, epididymal fat pad and from aorta. FEBS Lett. 374, 179-183.
4. Barrand M. A., Bagrij T., and Neo S.-Y. (1997) Multidrug resistance-associated protein: a protein distinct form P-glycoprotein involved in cytotoxic drug expulsion. Gen. Pharmacol. 28, 639-645.
5. Beaulieu E., Demeule M., Pouliot J.-F., Averill-Bates D. A., Murphy G. F., and Beliveau R. (1995) P-glycoprotein of blood-brain barrier: cross-reactivity of Mab C219 with a 190 kDa protein in bovine and rat isolated brain capillaries. Biochim. Biophys. Acta 1233, 27-32.
6. Begley D. J., Lechardeur D., Chen Z.-D., Rollinson C., Bardoul M., Roux F., Scherman D., and Abbott N. J. (1996) Functional expression of P-glycoprotein in an immortalised cell line of rat brain endothelial cells, RBE4. J. Neurochem. 67, 988-995.
7. Betz A. L., Csejtey J., and Golstein G. W. (1979) Hexose transport and phosphorylation by capillaries isolated from rat brain. Am. J. Physiol. 236, C96-C102.
8. 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.
9. Cole S. P. C., Bhardwaj G., Gerlach J. H., Mackie J. E., Grant C. E., Almquist K. C., Stewart A. J., Kurz E. U., Duncan A. M. V., and Deeley R. G. (1992) Overexpression of a transporter gene in a multidrug-resistant human lung cancer cell line. Science 258, 1650-1654.
10. Cole S. P. C., Sparks K. E., Fraser K., Loe D. W., Grant C. E., Wilson G. M., and Deeley R. G. (1994) Pharmacological characterization of multidrug resistant MRP-transfected human tumor cells. Cancer Res. 54, 5902-5910.
11. Coley H. M., Amos W. B., Twentyman P. R., and Workman P. (1993) Examination by laser scanning confocal fluorescence imaging microscopy of the subcellular localisation of anthracyclines in parent and multidrug resistant cell lines. Br. J. Cancer 67, 1316-1323.
12. Dehouck M.-P., Méresse S., Delorme P., Fruchart J.-C., and Cecchelli R. (1990) An easier, reproducible, and mass-production method to study the blood-brain barrier in vitro. J. Neurochem. 54, 1798-1801.
13. Dehouck B., Dehouck M.-P., Fruchart J.-C., and Cecchelli R. (1994) Upregulation of the low density lipoprotein receptor at the blood-brain barrier: intercommunications between brain capillary endothelial cells and astrocytes. J. Cell Biol. 126, 465-473.
14. Devault A. and Gros P. (1990) Two members of the mouse mdr gene family confer multidrug resistance with overlapping but distinct drug specificities. Mol. Cell. Biol. 10, 1652-1663.
15. Draper M. P., Martell R. L., and Levy S. B. (1997) Indomethacin-mediated reversal of multidrug resistance and drug efflux in human and murine cell lines overexpressing MRP, but not P-glycoprotein. Br. J. Cancer 75, 810-815.
16. Drion N., Lemaire M., Lefauconnier J.-M., and Scherrmann J.-M. (1996) Role of P-glycoprotein in the blood-brain transport of colchicine and vinblastine. J. Neurochem. 67, 1688-1693.
17. El Hafny B., Cano N., Piciotti M., Regina A., Scherrmann J.-M., and Roux F. (1997) Role of P-glycoprotein in colchicine and vinblastine cellular kinetics in an immortalized rat brain microvessel endothelial cell line. Biochem. Pharmacol. 53, 1735-1742.
18. Evers R., Zaman G. J. R., van Deemter L., Jansen H., Calafat J., Oomen L. C. J. M., Oude Elferink R. P. J., Borst P., and Schinkel S. (1996) Basolateral localization and export activity of the human multidrug resistance-associated protein in polarized pig kidney cells. J. Clin. Invest. 97, 1211-1218.
19. Flens M. J., Zaman G. J. R., van der Valk P., Izquierdo M. A., Schroeijers A. B., Scheffer G. L., van der Groep P., de Haas M., Meijer C. J. L. M., and Scheper R. J. (1996) Tissue distribution of the multidrug resistance protein. Am. J. Pathol. 148, 1237-1247.
20. Ford J. M. and Hait W. N. (1990) Pharmacology of drugs that alter multidrug resistance in cancer. Pharmacol. Rev. 42, 155-199.
21. Grant C. E., Valdimarsson G., Hipfner E., Almquist K. C., Cole S. P. C., and Deeley R. G. (1994) Overexpression of multidrug resistance-associated protein (MRP) increases resistance to natural product drugs. Cancer Res. 54, 357-361.
22. Holló Z., Homolya L., Hegedüs T., and Sarkadi B. (1996) Transport properties of the multidrug resistance-associated protein (MRP) in human tumour cells. FEBS Lett. 383, 99-104.
23. Jedlitschky G., Leier I., Buchholz U., Barnouin K., Kurz G., and Keppler D. (1996) Transport of glutathione, glucuronate and sulfate conjugates by the MRP gene-encoded conjugate export pump. Cancer Res. 56, 988-994.
24. Jetté L., Têtu B., and Béliveau R. (1993) High levels of P-glycoprotein detected in isolated brain capillaries. Biochim. Biophys. Acta 1150, 147-154.
25. Jetté L., Pouliot J.-F., Murphy G. F., and Béliveau R. (1995) Isoform I (mdr3) is the major form of P-glycoprotein expressed in mouse brain capillaries. Evidence for cross-reactivity of antibody C219 with an unrelated protein. Biochem. J. 305, 761-766.
26. Kavallaris M. (1997) The role of multidrug resistance-associated protein (MRP) expression in multidrug resistance. Anticancer Drugs 8, 17-25.
27. Keppler D., Leier I., Jedlitschky G., Mayer R., and Buchler M. (1996) The function of the multidrug resistance proteins (MRP and cMRP) in drug conjugate transport and hepatobiliary excretion. Adv. Enzyme Regul. 36, 17-29.
28. Keppler D., Konig J., and Buchler M. (1997) The canalicular multidrug resistance protein, cMRP/MRP2, a novel conjugate export pump expressed in the apical membrane of hepatocytes. Adv. Enzyme Regul. 37, 321-333.
29. Kool M., de Haas M., Scheffer G. L., Scheper R. J., van Eijk M. J. T., Juijn J. A., Baas F., and Borst P. (1997) Analysis of expression of cMOAT (MRP2), MRP3, MRP4, and MRP5, homologues of the multidrug resistance-associated protein gene (MRP1) in human cancer cell lines. Cancer Res. 57, 3537-3547.
30. Krishnamachary N. and Center M. S. (1993) The MRP gene associated with a non-P-glycoprotein multidrug resistance encodes a 190-kDa membrane bound glycoprotein. Cancer Res. 53, 3658-3661.
31. Krishnamachary N., Ma L., Zheng L., Safa A. R., and Center M. S. (1994) Analysis of MRP gene expression and function in HL60 cells isolated for resistance to adriamycin. Oncol Res. 6, 119-127.
32. Lautier D., Canitrot Y., Deeley R. G., and Cole S. P. C. (1996) Multidrug resistance mediated by the multidrug resistance protein (MRP) gene. Biochem. Pharmacol. 52, 967-977.
33. Lechardeur D. and Scherman D. (1995) Functional expression of the P-glycoprotein mdr in primary cultures of bovine cerebral capillary endothelial cells. Cell Biol. Toxicol. 11, 283-293.
34. Lee C. H., Bradley G., Zhang J.-T., and Ling V. (1993) Differential expression of P-glycoprotein genes in primary rat hepatocyte culture. J. Cell. Physiol. 157, 392-402.
35. 4 and structurally related conjugates. J. Biol. Chem. 269, 27807-27810.
36. Loe D. W., Almquist K. C., Cole S. P. C., and Deeley R. G. (1996) ATP-dependent 17β-estradiol 17-(β-D-glucuronide) transport by multidrug resistance protein (MRP). J. Biol. Chem. 272, 9683-9689.
37. Lowry O. H., Rosebrough N. J., Farr A. L., and Randall R. J. (1951) Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265-275.
38. Marquardt D. and Center M. S. (1992) Drug transport mechanisms in HL60 cells isolated for resistance to adriamycin: evidence for nuclear drug accumulation and redistribution in resistant cells. Cancer Res. 52, 3157-3163.
39. Mayer R., Kartenbeck J., Büchler M., Jedlitschky G., Leier I., and Keppler D. (1995) Expression of the MRP gene-encoded conjugate export pump in liver and its selective absence from the canalicular membrane in transport-deficient mutant hepatocytes. J. Cell Biol. 131, 137-150.
40. McCarthy K. D. and de Vellis J. (1980) Preparation of separate astroglial and oligodendroglial cultures from rat cerebral tissue. J. Cell Biol. 85, 890-902.
41. McGrath T. and Center M. S. (1987) Adriamycin resistance in HL-60 cells in the absence of detectable P-glycoprotein. Biochem. Biophys. Res. Commun. 145, 1171-1176.
42. Meyer J., Rauh J., and Galla H.-J. (1991) The susceptibility of cerebral endothelial cells to astroglial induction of blood-brain barrier enzymes depends on their proliferative state. J. Neurochem. 57, 1971-1977.
43. Müller M., Meijer C., Zaman G. J. R., Borst P., Scheper R. J., Mulder N. H., de Vries E. G. E., and Jansen P. L. (1994) Overexpression of the gene encoding the multidrug resistance associated protein results in increased ATP-dependent glutathione S-conjugate transport. Proc. Natl. Acad. Sci. USA 91, 13033-13037.
44. Ng W. F., Sarangi F., Zastawny R. K., Veinot-Drebot L., and Ling V. (1989) Identification of members of the P-glycoprotein multigene family. Mol. Cell. Biol. 98, 1224-1232.
45. 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.
46. Paul S., Belinsky M. G., Shen H., and Kruh G. D. (1996a) Structure and in vitro substrate specificity of the murine multidrug resistance-associated protein. Biochemistry 35, 13647-13655.
47. Paul S., Breuninger L. M., and Kruh G. D. (1996b) ATP-dependent transport of lipophilic cytotoxic drugs by membrane vesicles prepared from MRP-overexpressing HL60/ADR cells. Biochemistry 35, 14003-14011.
48. Paul S., Breuninger L. M., Tew K. D., Shen H., and Kruh G. D. (1996c) ATP-dependent uptake of natural product cytotoxic drugs by membrane vesicles establishes MRP as a broad specificity transporter. Proc. Natl. Acad. Sci. USA 93, 6929-6934.
49. 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.
50. Rubin L. L., Hall D. E., Porter S., Barbu K., Cannon C., Horner H. C., Janatpour M., Liaw C. W., Manning K., Morales J., Tanner L. I., Tomaselli K. J., and Bard F. (1991) A cell culture model of the blood-brain barrier. J. Cell Biol. 115, 1725-1735.
51. Sugawara I., Hamada H., Tsuruo T., and Mori S. (1990) Specialized localization of P-glycoprotein recognized by MRK 16 monoclonal antibody in endothelial cells of the brain and the spinal cord. Jpn. J. Cancer Res. 81, 727-730.
52. Tamai I. and Safa A. R. (1990) Competitive interactions of cyclosporins with the vinca alkaloid-binding site of the P-glycoprotein in multidrug-resistance cells. J. Biol. Chem. 265, 16509-16513.
53. Teeter L. D., Estes M., Chan J. Y., Atassi H., Sell S., Becker F. F., and Kuo M. T. (1993) Activation of distinct multidrug-resistance (P-glycoprotein genes) during rat liver regeneration and hepatocarcinogenesis. Mol. Carcinog. 8, 67-73.
54. Versantvoort C. H. M., Schuurhuis G. J., Pinedo H. M., Eekman C. A., Kuiper C. M., Lankelma J., and Broxterman H. J. (1993) Genistein modulates the decreased drug accumulation in non-P-glycoprotein mediated multidrug resistant tumour cells. Br. J. Cancer 68, 939-946.
55. Zaman G. J. R., Versantvoort C. H. M., Smit J. J. M., Eijdems E. W. H. M., de Haas M., Smith A. J., Broxterman H. J., Mulder N. H., de Vries E. G. E., Baas F., and Borst P. (1993) Analysis of the expression of MRP, the gene for a new putative trans-membrane drug transporter, in human multidrug resistant lung cancer cell lines. Cancer Res. 53, 1747-1750.
56. Zaman G. J. R., Flens M. J., van Leusden M. R., de Haas M., Mülder H. S., Lankelma J., Pinedo H. M., Scheper R. J., Baas F., Broxterman H. J., and Borst P. (1994) The human multidrug resistance-associated protein MRP is a plasma membrane drug-efflux pump. Proc. Natl. Acad. Sci. USA 91, 8822-8826.