Effects of MDR1 and MDR3 P-glycoproteins, MRP1, and BCRP/MXR/ABCP on the transport of 99mTc-Tetrofosmin

Biochemical Pharmacology

Volumn 60, Issue 3, 2000, Pages 413-426

  Chen, Wendy S ^a   Luker, Kathryn E ^a   Dahlheimer, Julie L ^a   Pica, Christina M ^a   Luker, Gary D ^a   Piwnica Worms, David ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

99mTc Tetrofosmin; 99mTc Sestamibi; ABC transporters; Blood brain barrier; Cancer; Gene therapy; MDR modulators; Multidrug resistance; P glycoprotein; Radiopharmaceuticals; Technetium

Indexed keywords

ELACRIDAR; GLYCOPROTEIN P; METHOXY ISOBUTYL ISONITRILE TECHNETIUM TC 99M; MULTIDRUG RESISTANCE PROTEIN; TETROFOSMIN TC 99M; VALSPODAR;

ARTICLE; BLOOD BRAIN BARRIER; CANCER THERAPY; DRUG DISTRIBUTION; DRUG TRANSPORT; GENE THERAPY; HUMAN; HUMAN CELL; ION TRANSPORT; MEMBRANE POTENTIAL; MEMBRANE TRANSPORT; MULTIDRUG RESISTANCE; PRIORITY JOURNAL; PROTEIN EXPRESSION;

3T3 CELLS; ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; BACULOVIRIDAE; BIOLOGICAL TRANSPORT; BLOOD-BRAIN BARRIER; CROSS REACTIONS; HUMANS; KB CELLS; MICE; NEOPLASM PROTEINS; ORGANOPHOSPHORUS COMPOUNDS; ORGANOTECHNETIUM COMPOUNDS; P-GLYCOPROTEIN; RADIOPHARMACEUTICALS; REPRODUCIBILITY OF RESULTS; SUBCELLULAR FRACTIONS; TUMOR CELLS, CULTURED;

EID: 0034257083     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-2952(00)00341-5     Document Type: Article

References (85)

1. Juliano R.L., Ling V. A surface glycoprotein modulating drug permeability in Chinese hamster ovary cell mutants. Biochim Biophys Acta. 455:1976;152-162.
2. Gros P. Ben Neriah Y, Croop JM and Housman DE, Isolation and expression of a complementary DNA that confers multidrug resistance. Nature. 323:1986;728-731.
3. Shen D.W., Fojo A., Chin J.E., Roninson I.B., Richert N., Pastan I., Gottesman M.M. Human multidrug-resistant cell lines Increased mdr1 expression can precede gene amplification. Science. 232:1986;643-645.
4. Gottesman M.M., Pastan I. Biochemistry of multidrug resistance mediated by the multidrug transporter. Annu Rev Biochem. 62:1993;385-427.
5. Bosch I and Croop J, P-glycoprotein multidrug resistance and cancer. Biochim Biophys Acta 1288: F37-F54, 1996.
6. 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.
7. 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., Scheper R.J. Tissue distribution of multidrug resistance protein. Am J Pathol. 148:1996;1237-1247.
8. Keppler D., Leier I., Jedlitschky G. Transport of glutathione conjugates and glucuronides by the multidrug resistance proteins MRP1 and MRP2. Biol Chem. 378:1997;787-791.
9. Lautier D., Canitrot Y., Deeley R.G., Cole S.P.C. Multidrug resistance mediated by the multidrug resistance protein (MRP) gene. Biochem Pharmacol. 52:1996;967-977.
10. Doyle L., Yang W., Abruzzo L., Drogmann T., Gao Y., Rishi A. A multidrug resistance transporter from human MCF-7 breast cancer cells. Proc Natl Acad Sci USA. 95:1998;15665-15670.
11. Miyake K., Mickley L., Litman T., Zhan Z., Robey R., Cristensen B., Brangi M., Greenberger L., Dean M., Fojo T., Bates S. Molecular cloning of cDNAs which are highly overexpressed in mitoxantrone-resistant cells Demonstration of homology to ABC transport genes. Cancer Res. 59:1999;8-13.
12. Allikmets R., Schriml L.M., Hutchinson A., Romano-Spica V., Dean M. A human placenta-specific ATP-binding cassette gene (ABCP) on chromosome 4q22 that is involved in multidrug resistance. Cancer Res. 58:1998;5337-5339.
13. Ford J.M., Hait W.N. Pharmacology of drugs that alter multidrug resistance in cancer. Pharmacol Rev. 42:1990;155-199.
14. Stein W.D., Cardarelli C., Pastan I., Gottesman M.M. Kinetic evidence suggesting that the multidrug transporter differentially handles influx and efflux of its substrates. Mol Pharmacol. 45:1994;763-772.
15. Marquardt D., McCrone S., Center M.S. Mechanisms of multidrug resistance in HL60 cells Detection of resistance-associated proteins with antibodies against synthetic peptides that correspond to the deduced sequence of P-glycoprotein. Cancer Res. 50:1990;1426-1430.
16. Robinson L., Roberts W., Ling T., Lamming D., Sternberg S., Roepe P. Human MDR1 protein overexpression delays the apoptotic cascade in Chinese hamster ovary fibroblasts. Biochemistry. 36:1997;11169-11178.
17. Smyth M.J., Krasovskis E., Sutton V.R., Johnstone R.W. The drug efflux protein P-glycoprotein additionally protects drug-resistant tumor cells from multiple forms of caspase-dependent apoptosis. Proc Natl Acad Sci USA. 95:1998;7024-7029.
18. Twentyman P.R., Bleehen N.M. Resistance modification by PSC-833, a novel non-immunosuppressive cyclosporin. Eur J Cancer. 27:1991;1639-1642.
19. Hyafil F., Vergely C., Du Vignaud P., Grand-Perret T. In vitro and in vivo reversal of multidrug resistance by GF120918, an acridonecarboxamide derivative. Cancer Res. 53:1993;4595-4602.
20. Dantzig A.H., Shepard R.L., Cao J., Law K.L., Ehlhardt W.J., Baughman T.M., Bumol T.F., Starling J.J. Reversal of P-glycoprotein-mediated multidrug resistance by a potent cyclopropyldibenzosuberane modulator, LY335979. Cancer Res. 56:1996;4171-4179.
21. Germann U., Ford P., Schlakhter D., Mason V., Harding M. Chemosensitization and drug accumulation effects of VX-710, verapamil, cyclosporin A, MS-209, and GF120918 in multidrug resistant HL60/ADR cells expressing the multidrug resistance-associated protein MRP. Anticancer Drugs. 8:1997;141-155.
22. Rabindran S., He H., Singh M., Brown E., Collins K., Annable T., Greenberger L. Reversal of a novel multidrug resistance mechanism in human colon carcinoma cells by fumitremorgin C. Cancer Res. 58:1998;5850-5858.
23. Sorrentino B.P., Brandt S.J., Bodine D., Gottesman M., Pastan I., Cline A., Nienhuis A.W. Selection of drug-resistant bone marrow cells in vivo after retroviral transfer of human MDR1. Science. 257:1992;99-103.
24. Podda S., Ward M., Himelstein A., Richardson C., de la Flor-Weiss E., Smith L., Gottesman M., Pastan I., Bank A. Transfer and expression of the human multiple drug resistance gene into live mice. Proc Natl Acad Sci USA. 89:1992;9676-9680.
25. Hanania E.G., Fu S., Roninson I., Zu Z., Gottesman M.M., Deisseroth A.B. Resistance to taxol chemotherapy produced in mouse marrow cells by safety-modified retroviruses containing a human MDR-1 transcription unit. Gene Ther. 2:1995;279-284.
26. Moscow J.A., Huang H., Carter C., Hines K., Zujewski J., Cusack G., Chow C., Venzon D., Sorrentino B., Chiang Y., Goldspiel B., Leitman S., Read E.J., Abati A., Gottesman M.M., Pastan I., Sellers S., Dunbar C., Cowan K.H. Engraftment of MDR1 and NeoR gene-transduced hematopoietic cells after breast cancer chemotherapy. Blood. 94:1999;52-61.
27. Piwnica-Worms D., Chiu M., Budding M., Kronauge J., Kramer R., Croop J. Functional imaging of multidrug-resistant P-glycoprotein with an organotechnetium complex. Cancer Res. 53:1993;977-984.
28. Piwnica-Worms D., Rao V., Kronauge J., Croop J. Characterization of multidrug-resistance P-glycoprotein transport function with an organotechnetium cation. Biochemistry. 34:1995;12210-12220.
29. 99mTc-Sestamibi as an agent for imaging P-glycoprotein-mediated multi-drug resistance In vitro and in vivo studies in a rat breast tumour cell line and its doxorubicin-resistant variant. Nucl Med Commun. 16:1995;253-257.
30. Ballinger J.R., Sheldon K.M., Boxen I., Erlichman C., Ling V. Differences between accumulation of Tc-99m-MIBI and Tl-201-thallous chloride in tumor cells Role of P-glycoprotein. Q J Nucl Med. 39:1995;122-128.
31. Cordobes M.D., Starzec A., Delmon-Moingeon L., Blanchot C., Kouyoumdjian J.-C., Prévost G., Caglar M., Moretti J.-L. Technetium-99m-sestamibi uptake by human benign and malignant breast tumor cells Correlation with mdr gene expression. J Nucl Med. 37:1996;286-289.
32. Del Vecchio S., Ciarmiello A., Potena M.I., Carriero M.V., Mainolfi C., Botti G., Thomas R., Cerra M., D'Aiuto G., Tsuruo T., Salvatore M. In vivo detection of multidrug resistance (MDR1) phenotype by technetium-99m sestamibi scan in untreated breast cancer patients. Eur J Nucl Med. 24:1997;150-159.
33. Del Vecchio S., Ciarmiello A., Pace L., Potena M.I., Carriero M.V., Mainolfi C., Thomas R., D'Aiuto G., Tsuruo T., Salvatore M. Fractional retention of technetium-99m-sestamibi as an index of P-glycoprotein expression in untreated breast cancer patients. J Nucl Med. 38:1997;1348-1351.
34. Chen C.C., Meadows B., Regis J., Kalafsky G., Fojo T., Carrasquillo J.A., Bates S.E. Detection of. in vivo P-glycoprotein inhibition by PSC 833 using Tc-99m sestamibi, Clin Cancer Res. 3:1997;545-552.
35. Luker G.D., Fracasso P.M., Dobkin J., Piwnica-Worms D. Modulation of the multidrug resistance P-glycoprotein Detection with technetium-99m-sestamibi in vivo. J Nucl Med. 38:1997;369-372.
36. Bom HS, Kim YC, Lim SC and Park KO, Dipyridamole modulated Tc-99m sestamibi (MIBI) scintigraphy, A predictor of response to chemotherapy in patients with small cell lung cancer (SCLC). J Nucl Med 38: 240P, 1997.
37. Kostakoglu L., Elahi N., Kïratlï P., Ruacan S., Sayek S., Baltalï E., Sungur A., Hayran M., Bekdik C.F. Clinical validation of the influence of P-glycoprotein on technetium-99m-sestamibi uptake in malignant tumors. J Nucl Med. 38:1994;1003-1008.
38. Barbarics E., Kronauge J., Cohen D., Davison A., Jones A., Croop J. Characterization of P-glycoprotein transport and inhibition in vivo. Cancer Res. 58:1998;276-282.
39. Kostakoglu L., Kirath P., Ruacan S., Hayran M., Emri S., Ergün E.L., Bekdik C.F. Association of tumor washout rates and accumulation of technetium-99m-MIBI with expression of P-glycoprotein in lung cancer. J Nucl Med. 39:1998;228-234.
40. Ciarmiello A., Del Vecchio S., Silvestro P., Potena M.I., Carriero M.V., Thomas R., Botti G., D'Aiuto G., Salvatore M. Tumor clearance of technetium 99m-sestamibi as a predictor of response to neoadjuvant chemotherapy for locally advanced breast cancer. J Clin Oncol. 16:1998;1677-1683.
41. Herman L.W., Sharma V., Kronauge J.F., Barbarics E., Herman L.A., Piwnica-Worms D. Novel hexakis(areneisonitrile)technetium(I) complexes as radioligands targeted to the multidrug resistance P-glycoprotein. J Med Chem. 38:1995;2955-2963.
42. Luker G.D., Rao V.V., Crankshaw C.L., Dahlheimer J., Piwnica-Worms D. Characterization of phosphine complexes of technetium(III) as transport substrates of the multidrug resistance P-glycoprotein and functional markers of P-glycoprotein at the blood-brain barrier. Biochemistry. 36:1997;14218-14227.
43. Ballinger J., Muzzammil T., Moore M. Technetium-99m-Furifosmin as an agent for functional imaging of multidrug resistance in tumors. J Nucl Med. 38:1997;1915-1919.
44. Crankshaw C.L., Marmion M., Luker G.D., Rao V., Dahlheimer J., Burleigh B.D., Webb E., Deutsch K.F., Piwnica-Worms D. Novel technetium (III)-Q complexes for functional imaging of the multidrug resistance (MDR1) P-glycoprotein. J Nucl Med. 39:1998;77-86.
45. Sharma V., Piwnica-Worms D. Metal complexes for therapy and diagnosis of drug resistance. Chem Rev. 99:1999;2545-2560.
46. Hendrikse N., Franssen E., van der Graaf W., Vaalburg W., de Vries E. Visualization of multidrug resistance in vivo. Eur J Nucl Med. 26:1999;283-293.
47. Kelly J.D., Forster A.M., Higley B., Archer C.M., Booker F.S., Canning L.R., Chiu K.W., Edwards B., Gill H.K., McPartlin M., Nagle K.R., Latham I.A., Pickett R.D., Storey A.E., Webbon P.M. Technetium-99m-tetrofosmin as a new radiopharmaceutical for myocardial perfusion imaging. J Nucl Med. 34:1993;222-227.
48. Münch G., Neverve J., Matsunari I., Schröter G., Schwaiger M. Myocardial technetium-99m-tetrofosmin and technetium-99m-sestamibi kinetics in normal subjects and patients with coronary artery disease. J Nucl Med. 38:1997;428-432.
49. Ballinger J.R., Bannerman J., Boxen I., Firby P., Hartman N.G., Moore M.J. Technetium-99m-tetrofosmin as a substrate for P-glycoprotein In vitro studies in multidrug-resistant breast tumor cells. J Nucl Med. 37:1996;1578-1582.
50. Piwnica-Worms D., Kronauge J.F., Chiu M.L. Uptake and retention of hexakis (2-methoxyisobutyl isonitrile) technetium(I) in cultured chick myocardial cells. Mitochondrial and plasma membrane potential dependence. Circulation. 82:1990;1826-1838.
51. Akiyama S.I., Fojo A., Hanover J.A., Pastan I., Gottesman M.M. Isolation and genetic characterization of human KB cell lines resistant to multiple drugs. Somat Cell Mol Genet. 11:1985;117-126.
52. Bosch I., Crankshaw C.L., Piwnica-Worms D., Croop J.M. Characterization of functional assays of multidrug resistance P-glycoprotein transport activity. Leukemia. 11:1997;1131-1137.
53. Luker G.D., Nilsson K.R., Covey D.F., Piwnica-Worms D. Multidrug resistance (MDR1) P-glycoprotein enhances esterification of plasma membrane cholesterol. J Biol Chem. 274:1999;6979-6991.
54. Rao V.V., Chiu M.L., Kronauge J.F., Piwnica-Worms D. Expression of recombinant human multidrug resistance P-glycoprotein in insect cells confers decreased accumulation of technetium-99m-sestamibi. J Nucl Med. 35:1994;510-515.
55. - Carrier free? J Nucl Med. 16:1975;639-641.
56. Sedlak J., Lindsay R.H. Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman's reagent. Anal Biochem. 25:1968;192-205.
57. Rao V.V., Dahlheimer J.L., Bardgett M.E., Snyder A.Z., Finch R.A., Sartorelli A.C., Piwnica-Worms D. 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.
58. 2) (ethylenediamine)bis[propyl(R-benzylimino)]metal(III) cations. J Med Chem. 39:1996;3483-3490.
59. Younes A. Mechanism of uptake of Tc-tetrofosmin II Uptake into isolated adult rat heart mitochondria. J Nucl Cardiol. 2:1995;327-333.
60. Ritchie R.J., A critical assessment of the use of lipophilic cations as membrane potential probes. Prog Biophys Mol Biol. 43:1984;1-32.
61. Piwnica-Worms D., Kronauge J.F., Chiu M.L. Enhancement by tetraphenylborate of technetium-99m-MIBI uptake kinetics and accumulation in cultured chick myocardial cells. J Nucl Med. 32:1991;1992-1999.
62. Chernoff D.M., Strichartz G.R., Piwnica-Worms D. Membrane potential determination in large unilamellar vesicles with hexakis(2-methoxyisobutylisonitrile) technetium(I). Biochim Biophys Acta. 1147:1993;262-266.
63. Backus M, Piwnica-Worms D, Hockett D, Kronauge J, Lieberman M, Ingram P and LeFurgey A, Microprobe analysis of Tc-MIBI in heart cells: Calculation of mitochondrial membrane potential. Am J Physiol 265: C178-C187, 1993.
64. 99Tc-NMR spectroscopy. Magn Reson Imaging. 12:1994;641-652.
65. Ruetz S., Gros P. Functional expression of P-glycoproteins in secretory vesicles. J Biol Chem. 269:1994;12277-12284.
66. 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.
67. Lemasters J, Necrapoptosis and the mitochondrial permeability transition: Shared pathways to necrosis and apoptosis. Am J Physiol 276: G1-G6, 1999.
68. r 190,000 multidrug resistance protein (MRP) Evidence for cotransport with reduced glutathione. Cancer Res. 58:1998;5130-5136.
69. Lorico A., Rappa G., Finch R.A., Yang D., Flavell R.A., Sartorelli A.C. Disruption of the murine MRP (multidrug resistance protein) gene leads to increased sensitivity to etoposide (VP-16) and increased levels of glutathione. Cancer Res. 57:1997;5238-5242.
70. Rappa G., Lorico A., Flavell R.A., Sartorelli A.C. Evidence that the multidrug resistance protein (MRP) functions as a co-transporter of glutathione and natural product toxins. Cancer Res. 57:1997;5232-5237.
71. Schinkel AH, Mol CAAM, Wagenaar E, van Deemter L, Smit JJM and Borst P, Multidrug resistance and the role of P-glycoprotein knockout mice. Eur J Cancer 31A: 1295-1298, 1995.
72. Franssen E, Hendrikse N, Elsinga P, Fluks E, Schinkel A, van der Graaf W, van Loenen-Weemaes A, de Vries E and Vaalburg W, P-glycoprotein monitoring of carbon-11 daunorubicin and verapamil in P-glycoprotein gene knock-out and wild type mice with PET. J Nucl Med 37: 355P, 1996.
73. Hendrikse N.H., Schinkel A.H., de Vries E.G., Fluks E., Van der Graaf W.T., Willemsen A.T., Vaalburg W., Franssen E.J. Complete in vivo reversal of P-glycoprotein pump function in the blood-brain barrier visualized with positron emission tomography. Br J Pharmacol. 124:1998;1413-1418.
74. Delmon-Moingeon L.I., Piwnica-Worms D., Van den Abbeele A.D., Holman B.L., Davison A., Jones A.G. Uptake of the cation hexakis (2-methoxyisobutylisonitrile) technetium-99m by human carcinoma cell lines in vitro. Cancer Res. 50:1990;2198-2202.
75. Platts E.A., North T.L., Pickett R.D., Kelly J.D. Mechanism of uptake of technetium-tetrofosmin. I Uptake into isolated adult rat ventricular myocytes and subcellular localization. J Nucl Cardiol. 2:1995;317-326.
76. 99mTc-sestamibi is a substrate for P-glycoprotein and the multidrug resistance-associated protein. Br J Cancer. 77:1998;353-358.
77. Hoffman M.M., Roepe P.D. Analysis of ion transport perturbations caused by hu MDR 1 protein overexpression. Biochemistry. 36:1997;11153-11168.
78. 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., Borst P. Analysis of the expression of MRP, the gene for a new putative transmembrane drug transporter, in human multidrug resistant lung cancer cell lines. Cancer Res. 53:1993;1747-1750.
79. Breuninger L.M., Paul S., Gaughan K., Miki T., Chan A., Aaronson S.A., Kruh G.D. Expression of multidrug resistance-associated protein in NIH/3T3 cells confers multidrug resistance associated with increased drug efflux and altered intracellular drug distribution. Cancer Res. 55:1995;5342-5347.
80. Evers R., Zaman G.J.R., van Deemter L., Jansen H., Calafat J., Oomen L.C.J.M. Oude Elferink RPJ, Borst P and Schinkel AH, Basolateral localization and export activity of the human multidrug resistance-associated protein in polarized pig kidney cells. J Clin Invest. 97:1996;1211-1218.
81. Crankshaw C., Piwnica-Worms D. Tc-99m-Sestamibi may be a transport substrate of the human multidrug resistance-associated protein (MRP). J Nucl Med. 37:1996;247P.
82. Moretti J.-L., Cordobes M.D., Starzec A., de Beco V., Vergote J., Benazzouz F., Boissier B., Cohen H., Safi N., Piperno-Neumann S., Kouyoumdjian J.-C. Involvement of glutathione in loss of technetium-99m-MIBI accumulation related to membrane MDR protein expression in tumor cells. J Nucl Med. 39:1998;1214-1218.
83. Schinkel A.H., Smit J.J.M., van Tellingen O., Beijnen J.H., Wagenaar E., van Deemter L., Mol C.A.A.M., van der Valk M.A., Robanus-Maandag E.C., te Riele H.P.G., Berns A.J.M., Borst P. Disruption of the mouse mdr1a P-glycoprotein gene leads to a deficiency in the blood-brain barrier and to increased sensitivity to drugs. Cell. 77:1994;491-502.
84. Schinkel A.H., Mayer U., Wagenaar E., Mol C.A.A.M., van Deemter L., Smit J.J.M., van der Valk M.A., Voordouw A.C., Spits H., van Tellingen O., Zijlmans J.M.J.M., Fibbe W.E., Borst P. Normal viability and altered pharmacokinetics in mice lacking mdr1-type (drug-transporting) P-glycoproteins. Proc Natl Acad Sci USA. 94:1997;4028-4033.
85. Kostakoglu L., Guc D., Canpinar H., Kars A., Alper E., Kiratli P., Hayran M., Gündüz U., Kansu E. P-glycoprotein expression by technetium-99m-MIBI scintigraphy in hematologic malignancy. J Nucl Med. 39:1998;1191-1197.