Involvement of multidrug resistance proteins (MDR) in the modulation of glucocorticoid response

Journal of Steroid Biochemistry and Molecular Biology

Volumn 82, Issue 4-5, 2002, Pages 277-288

  Webster, Jeanette I ^a,b   Carlstedt Duke, Jan ^a  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^b NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

Author keywords

ABC transporter proteins; Glucocorticoid response; Multidrug resistance; P glycoprotein; Receptor modulation

Indexed keywords

CALCEIN; GLUCOCORTICOID; MESSENGER RNA; MULTIDRUG RESISTANCE PROTEIN; PROBENECID; PROTEIN INHIBITOR; RHODAMINE;

ANIMAL CELL; ARTICLE; CELL ASSAY; CELL LINE; CELL TRANSPORT; CONTROLLED STUDY; HORMONE DETERMINATION; HORMONE RESPONSE; HORMONE TRANSPORT; MOUSE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN TRANSPORT; RNA ANALYSIS;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; BIOLOGICAL TRANSPORT; CELLS, CULTURED; CHLORAMPHENICOL O-ACETYLTRANSFERASE; DEXAMETHASONE; DNA PRIMERS; DRUG RESISTANCE, MULTIPLE; FLUORESCEINS; GLUCOCORTICOIDS; MICE; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; P-GLYCOPROTEIN; P-GLYCOPROTEINS; PROBENECID; PROMOTER REGIONS (GENETICS); REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RHODAMINES; TRANS-ACTIVATION (GENETICS);

EID: 0036877355     PISSN: 09600760     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0960-0760(02)00227-3     Document Type: Article

References (83)

1. Ray D.W. Molecular mechanisms of glucocorticoid resistance. J. Endocrinol. 149:1996;1-5.
2. Werner S., Brönnegård M. Molecular basis of glucocorticoid-resistant syndromes. Steroids. 61:1996;216-221.
3. Farrell R.J., Murphy A., Long A., Donnelly S., Cherikuri A., O'Toole D., Mahmud N., Keeling P.W.N., Weir D.G., Kelleher D. High multidrug resistance (P-glycoprotein 170) expression in inflammatory bowel disease patients who fail medical therapy. Gastroenterology. 118:2000;279-288.
4. Higgins C.F. ABC transporters: from microganisms to man. Annu. Rev. Cell Biol. 8:1992;67-113.
5. Higgins C.F., Callaghan R., Linton K.J., Rosenberg M.F., Ford R.C. Structure of the multidrug resistance P-glycoprotein. Semin. Cancer Biol. 8:1997;135-142.
6. Gottesman M.M., Pastan I. Biochemistry of multidrug resistance mediated by the multidrug transporter. Annu. Rev. Biochem. 62:1993;385-427.
7. Borst P., Schinkel A.H., Smit J.J.M., Wagenaar E., Van Deemter L., Smith A.J., Eijdems E.W., Baas F., Zaman G.J.R. Classical and novel forms of multidrug resistance and the physiological functions of P-glycoproteins in mammals. Pharmacol. Ther. 60:1993;289-299.
8. Bosch I., Croop J. P-glycoprotein multidrug resistance and cancer. Biochim. Biophys. Acta. 1288:1996;F37-F54.
9. Thiebaut F., Tsurua T., Hamada H., Gottesman M.M., Pastan I., Willingham M.C. Cellular localization of the multidrug resistance gene product P-glycoprotein in normal human tissues. Proc. Natl. Acad. Sci. U.S.A. 84:1987;7735-7738.
10. Sugawara I., Kataoka I., Morishita Y., Hamada H., Tsuruo T., Itoyama S., Mori S. Tissue distribution of P-glycoprotein encoded by a multidrug resistant gene as revealed by a monoclonal antibody, MRK16. Cancer Res. 48:1988;1926-1929.
11. van Helvoort A., Smith A.J., Sprong H., Fritzsche I., Schinkel A.H., Borst P., van Meer G. MDR1 P-glycoprotein is a lipid translocase of broad specificity, while MDR3 P-glycoprotein specifically translocates phosphatidylcholine. Cell. 87:1996;507-517.
12. 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., Deeley R.G. Overexpression of a transporter gene in a multidrug resistant human lung cancer cell line. Science. 258:1992;1650-1654.
13. Deeley R.G., Cole S.P.C. Function, evolution and structure of multidrug resistance protein (MRP). Semin. Cancer Biol. 8:1997;193-204.
14. Borst P., Kool M., Evers R. Do cMOAT (MRP2), other MRP homologues, and LRP play a role in MDR? Semin. Cancer Biol. 8:1997;205-213.
15. Kool M., de Haas M., Scheffer G.L., Scheper R.J., van Eijk M.J.T., Juijn J.A., Baas F., Borst P. 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. 57:1997;3537-3547.
16. Devault A., Gros P. Two members of the mouse mdr gene family confer multidrug resistance with overlapping but distinct drug specificities. Mol. Cell. Biol. 10:1990;1652-1663.
17. Gros P., Croop J., Housman D. Mammalian multidrug resistance gene: complete cDNA sequence indicates strong homology to bacterial transport proteins. Cell. 47:1986;371-380.
18. Hsu S.-I., Lothstein L., Horwitz S.B. Differential overexpression of three mdr gene family members in multidrug resistant J774.2 mouse cells. J. Biol. Chem. 264:1989;12053-12062.
19. Gros P., Raymond M., Bell J., Housman D. Cloning and characterization of a second member of the mouse mdr gene family. Mol. Cell. Biol. 8:1988;2770-2778.
20. Yang C.-P.H., Cohen D., Greenberger L.M., Hsu S.I.-H., Horwitz S.B. Differential transport properties of two mdr gene products are distinguished by progesterone. J. Biol. Chem. 265:1990;10282-10288.
21. Gross S.R., Aronow L., Pratt W.B. The active transport of cortisol by mouse fibroblasts growing in vitro. Biochem. Biophys. Res. Commun. 32:1968;66-72.
22. Barnes K.M., Dickstein B., Cutler G.B. Jr., Fojo T., Bates S.E. Steroid transport, accumulation, and antagonism of P-glycoprotein in multidrug resistant cells. Biochemistry. 35:1996;4820-4827.
23. Ueda K., Okamura N., Hirai M., Tanigawara Y., Saeki T., Kioka N., Komano T., Hori R. Human P-glycoprotein transports cortisol, aldosterone, and dexamethasone, but not progesterone. J. Biol. Chem. 267:1992;24248-24252.
24. van Kalken C.K., Broxterman H.J., Pinedo H.M., Feller N., Dekker H., Lankelma J., Giaccone G. Cortisol is transported by the multidrug resistance gene product P-glycoprotein. Br. J. Cancer. 67:1993;284-289.
25. Schinkel A.H., Waganaar E., van Deemter L., Mol C.A.A.M., Borst P. Absence of the mdr1 a P-glycoprotein in mice affects tissue distribution and pharmokinetics of dexamethasone, digoxin, and cyclosporin A. J. Clin. Invest. 96:1995;1698-1705.
26. Bourgeois S., Gruol D.J., Newby R.F., Rajah F.M. Expression of an mdr gene is associated with a new form of resistance to a dexamethasone-induced apoptosis. Mol. Endocrinol. 7:1993;840-851.
27. Gruol D.J., Bourgeois S. Expression of the mdr1 P-glycoprotein gene: a mechanism of escape from glucocorticoid-induced apoptosis. Biochem. Cell Biol. 72:1994;561-571.
28. Meijer O.C., de Lange C.M., Breimer D.D., de Boer A.G., Workel J.O., de Kloet E.R. Penetration of dexamethasone into brain glucocorticoid targets is enhanced in mdr1a P-glycoprotein knockout mice. Endocrinology. 139:1998;1789-1793.
29. Gruol D.J., Vo Q.D., Zee M.C. Profound differences in the transport of steroids by two mouse P-glycoproteins. Biochem. Pharmacol. 58:1999;1191-1199.
30. Daoud S.S., Juliano R.L. Modulation of doxorubicin resistance by valinomycin (NSC 122023) and liposomal valinomycin in Chinese hamster ovary cells. Cancer Res. 49:1989;2661-2667.
31. Tsuruo T., Iida H., Naganuma K., Tsukagoshi S., Sakurai Y. Promotion by verapamil of vincristine responsiveness in tumor cell lines inherently resistant to the drug. Cancer Res. 43:1983;808-813.
32. Tsuruo T., Iida H., Nojiri M., Tsukagoshi S., Sakurai Y. Circumvention of vincrisitine and adriamycin resistance in vitro and in vivo by calcium influx blockers. Cancer Res. 43:1983;2905-2910.
33. Safa A.R. Photoaffinity labeling of the multidrug resistance-related P-glycoprotein with photoactive analogs of verapamil. Proc. Natl. Acad. Sci. U.S.A. 85:1988;7187-7191.
34. Cole S.P.C., Sparks K.E., Fraser K., Loe D.W., Grant C.E., Wilson G.M., Deeley R.G. Pharmacological characterization of multidrug resistance MRP-transfected human tumor cells. Cancer Res. 54:1994;5902-5910.
35. Arceci R.J., Stieglitz K., Bierer B.E. Immunosuppressants FK506 and rapamycin function as reversal agents of the multidrug resistance phenotype. Blood. 80:1992;1528-1536.
36. Mizuno K., Furuhashi Y., Misawa T., Iwata M., Kawai M., Kikkawa F., Kano T., Tomoda Y. Modulation of multidrug resistance by immunosuppressive agents: cyclosporin analogues, FK506 and mizoribine. Anticancer Res. 12:1992;21-26.
37. Naito M., Oh-hara T., Yamazaki A., Danki T., Tsuruo T. Reversal of multidrug resistance by an immunosuppressive agent FK-506. Cancer Chemother. Pharmacol. 29:1992;195-200.
38. Feller N., Broxterman H.J., Währer D.C.R., Pinedo H.M. ATP-dependent efflux of calcein by the multidrug resistance protein (MRP): no inhibition by intracellular glutathione depletion. FEBS Lett. 368:1995;385-388.
39. Gollapudi S., Kim C.H., Tran B.-N., Sanga S., Gupta S. Probenecid reverses multidrug resistance in multidrug resistance-associated protein-overexpressing HL60/AR and H69/AR cells but not in P-glycoprotein-overexpressing HL60/Tax and P388/ADR cells. Cancer Chemother. Pharmacol. 40:1997;150-158.
40. Hooijberg J.H., Broxterman H.J., Kool M., Assaraf Y.G., Peters G.F., Noordhuis P., Scheper R.J., Borst P., Pinedo H.M., Jansen G. Antifolate resistance mediated by the multidrug resistance proteins MRP1 and MRP2. Cancer Res. 59:1999;2532-2535.
41. Payen L., Courtois A., Campion J.-P., Guillouzo A., Fardel O. Characterization and inhibition by a wide range of xenobiotics of organic anion excretion by primary human hepatocytes. Biochem. Pharmacol. 60:2000;1967-1975.
42. Kolaczkowski M., van der Rest M., Cybularz-Kolaczkowska A., Soumillion J.-P., Konings W.N., Goffeau A. Anticancer drugs, ionophoric peptides and steroids as substrates of the yeast multidrug transporter Pdr5p. J. Biol. Chem. 271:1996;31543-31548.
43. Kralli A., Yamamoto K.R. An FK506-sensitive transporter selectively decreases intracellular levels and potency of steroid hormones. J. Biol. Chem. 271:1996;17152-17156.
44. Kolaczkowski M., Goffeau A. Active efflux by multidrug transporters as one of the strategies to evade chemotherapy and novel practical implications of yeast pleiotropic drug resistance. Pharmacol. Therap. 76:1997;219-242.
45. Marsaud V., Mercier-Bodard C., Fortin D., Le Bihan S., Renoir J.-M. Dexamethasone and triamcinolone acetonide accumulation in mouse fibroblasts is differently modulated by the immunosuppressants cyclosporin A, FK506, rapamycin and their analogues, as well as by other P-glycoprotein ligands. J. Steroid Biochem. Mol. Biol. 66:1998;11-25.
46. Medh R.D., Lay R.H., Schmidt T.J. Agonist-specific modulation of glucocorticoid receptor-mediated transcription by immunosuppressants. Mol. Cell. Endocrinol. 138:1998;11-23.
47. Wood T.J.J., Sliva D., Lobie P.E., Pircher T.J., Gouilleux F., Wakao H., Gustafsson J.-Å., Groner B., Norstedt G., Haldosen L.-A. Mediation of growth hormone-dependent transcriptional activation by mammary gland factor/Stat 5. J. Biol. Chem. 270:1995;9448-9453.
48. Nadakavukaren K.K., Nadakavukaren J.J., Chen L.B. Increased rhodamine 123 uptake by carcinoma cells. Cancer Res. 45:1985;6093-6099.
49. Chomcynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:1987;156-159.
50. Lacave R., Coulet F., Ricci S., Touboul E., Flahault A., Rateau J.G., Cesari D., Lefranc J.P., Bernaudin J.F. Comparative evaluation by semiquantitative reverse transcriptase polymerase chain reaction of MDR1, MRP and GSTp gene expression in breast carcinomas. Br. J. Cancer. 77:1998;694-702.
51. Ning Y.-M., Sanchez E.R. Potentiation of glucocorticoid receptor-mediated gene expression by the immunophilin ligands FK506 and rapamycin. J. Biol. Chem. 268:1993;6073-6076.
52. Petriz J., Garcia-Lopez J. Flow cytometric analysis of P-glycoprotein function using rhodamine 123. Leukemia. 11:1997;1124-1130.
53. Eisenbraun M.D., Miller R.A. mdr1a-encoded P-glycoprotein is not required for peripheral T Cell proliferation, cytokine release, or cytotoxic effector function in mice. J. Immunol. 163:1999;2621-2627.
54. Santoni-Rugiu E., Silverman J.A. Functional characterization of the rat mdr1b encoded P-glycoprotein: not all inducing agents are substrates. Carcinogenesis. 18:1997;2255-2263.
55. Homolya L., Hollo Z., Germann U.A., Pastan I., Gottesman M.M., Sarkadi B. Fluorescent cellular indicators are extruded by the multidrug resistance protein. J. Biol. Chem. 268:1993;21493-21496.
56. Hollo Z., Homolya L., Davis C.W., Sarkadi B. Calcein accumulation as a fluorometric functional assay of the multidrug transporter. Biochim. Biophys. Acta. 1191:1994;384-388.
57. Essadaigui M., Broxterman H.J., Garnier-Suillerat A. Kinetic analysis of calcein and calcein-acetoxymethylester efflux mediated by the multidrug resistance protein and P-glycoprotein. Biochemistry. 37:1998;2243-2250.
58. Alvarez M., Robey R., Sandor V., Nishiyama K., Matsumoto Y., Paull K., Bates S., Fojo T. Using the national cancer institute anticancer drug screen to assess the effect of MRP expression on drug sensitivity profiles. Mol. Pharmacol. 54:1998;802-814.
59. Legrand O., Simonin G., Perrot J.-Y., Zittoun R., Marie J.-P. Pgp and MRP activities using calcein-AM are prognostic factors in adult acute myeloid leukemia patients. Blood. 91:1998;4480-4488.
60. Ueda K., Clark D.P., Chen C.-J., Roninson I.B., Gottesman M.M., Pastan I. The human multidrug resistance (mdr1) gene. J. Biol. Chem. 262:1987;505-508.
61. Gerloff T., Stieger B., Hagenbuch B., Madon J., Landmann L., Roth J., Hofmann A.F., Meier P.J. The sister of P-glycoprotein represents the canalicular bile salt export pump of mammalian liver. J. Biol. Chem. 273:1998;10046-10050.
62. Tai P.K., Chang H., Albers M.W., Schreiber S.L., Toft D.O., Faber L.E. P59 (FK506 binding protein 59) interaction with heat shock proteins is highly conserved and may involve proteins other than steroid receptors. Biochemistry. 32:1993;8842-8847.
63. Milad M., Sullivan W., Diehl E., Altmann M., Nordeen S., Edwards D.P., Toft D.O. Interaction of the progesterone receptor with binding proteins for FK506 and cyclosporin A. Mol. Endocrinol. 9:1995;838-847.
64. Renoir J.M., Le Bihan S., Mercier-Bodard C., Gold A., Arjomandi M., Radanyi C., Baulieu E.E. Effects of immunosuppressants FK506 and rapamycin on the heterooligomeric form of the progesterone receptor. J. Steroid Biochem. Mol. Biol. 48:1994;101-110.
65. Kunz J., Hall M.N. Cyclosporin A, FK506 and rapamycin: more than just immunosuppression. Trends Biochem. Sci. 18:1993;334-338.
66. Harding M.W., Galat A., Uehling D.E., Schreiber S.L. A receptor for the immunosuppressant FK506 is a cis-trans peptidyl-prolyl isomerase. Nature. 341:1989;758-760.
67. Wolf D.C., Horwitz S.B. P-glycoprotein transports corticosterone and is photoaffinity-labeled by the steroid. Int. J. Cancer. 52:1992;141-146.
68. Vo Q.D., Groul D.J. Identification of P-glycoprotein mutations causing a loss of steroid recognition and transport. J. Biol. Chem. 274:1999;20318-20327.
69. Yang C.-P.H., DePinho S.G., Greenberger L.M., Arceci R.J., Horwitz S.B. Progesterone interacts with P-glycoprotein in multidrug resistant cells and in the endometrium of gravid uterus. J. Biol. Chem. 264:1989;782-788.
70. Gruol D.J., Bourgeois S. Chemosensitizing steroids: glucocorticoid receptor agonists capable of inhibiting P-glycoprotein function. Cancer Res. 54:1997;720-727.
71. Qian X.-D., Beck W.T. Progesterone photoaffinity labels P-glycoprotein in multidrug resistant human leukemic lymphoblasts. J. Biol. Chem. 265:1990;18753-18756.
72. Vottero A., Chrousos G.P. Glucocorticoid receptor beta: view I. Trends Endocrinol. Metab. 10:1999;333-338.
73. Oakley R.H., Sar M., Cidlowski J.A. The human glucocorticoid receptor beta isoform. Expression, biochemical properties, and putative function. J. Biol. Chem. 271:1996;9550-9559.
74. Oakley R.H., Jewell C.M., Yudt M.R., Bofetiado D.M., Cidlowski J.A. The dominant negative activity of the human glucocorticoid receptor beta isoform. Specificity and mechanisms of action. J. Biol. Chem. 274:1999;27857-27866.
75. Brogan I.J., Murray I.A., Cerillo G., Needham M., White A., Davis J.R. Interaction of glucocorticoid receptor isoforms with transcription factors AP-1 and NF-kappaB: lack of effect of glucocorticoid receptor beta. Mol. Cell. Endocrinol. 157:1999;95-104.
76. Carlstedt-Duke J. Glucocorticoid receptor beta: view II. Trends Endocrinol. Metab. 10:1999;339-342.
77. Hecht K., Carlstedt-Duke J., Stierna P., Gustafsson J., Bronnegard M., Wikstrom A.C. Evidence that the beta-isoform of the human glucocorticoid receptor does not act as a physiologically significant repressor. J. Biol. Chem. 272:1997;26659-26664.
78. Leung D.Y., Hamid Q., Vottero A., Szefler S.J., Surs W., Minshall E., Chrousos G.P., Klemm D.J. Association of glucocorticoid insensitivity with increased expression of glucocorticoid receptor beta. J. Exp. Med. 186:1997;1567-1574.
79. Hamid Q.A., Wenzel S.E., Hauk P.J., Tsicopoulos A., Wallaert B., Lafitte J.J., Chrousos G.P., Szefler S.J., Leung D.Y. Increased glucocorticoid receptor beta in airway cells of glucocorticoid-insensitive asthma. Am. J. Respir. Crit. Care Med. 159:1999;1600-1604.
80. Sousa A.R., Lane S.J., Cidlowski J.A., Staynov D.Z., Lee T.H. Glucocorticoid resistance in asthma is associated with elevated in vivo expression of the glucocorticoid receptor beta-isoform. J. Allergy Clin. Immunol. 105:2000;943-950.
81. Honda M., Orii F., Ayabe T., Imai S., Ashida T., Obara T., Kohgo Y. Expression of glucocorticoid receptor beta in lymphocytes of patients with glucocorticoid-resistant ulcerative colitis. Gastroenterology. 118:2000;859-866.
82. Derijk R.H., Schaaf M.J., Turner G., Datson N.A., Vreugdenhil E., Cidlowski J., de Kloet E.R., Emery P., Sternberg E.M., Detera-Wadleigh S.D. A human glucocorticoid receptor gene variant that increases the stability of the glucocorticoid receptor beta-isoform mRNA is associated with rheumatoid arthritis. J. Rheumatol. 28:2001;2383-2388.
83. Bello-Reuss E., Ernest S., Holland O.B., Hellmich M.R. Role of multidrug resistance P-glycoprotein in the secretion of aldosterone by human adrenal NCI-H295 cells. Am. J. Physiol. Cell Physiol. 278:2000;C1256-C1265.