Visualization of multidrug resistance in vivo

European Journal of Nuclear Medicine

Volumn 26, Issue 3, 1999, Pages 283-293

  Hendrikse, N H ^a   Franssen, E J F ^a   Van Der Graaf, W T A ^a   Vaalburg, W ^a   De Vries, E G E ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

Multidrug resistance; Multidrug resistance associated protein; P glycoprotein; Positron emission tomography; Single photon emission tomography

Indexed keywords

CARBON 11; COLCHICINE; DAUNORUBICIN; GLYCOPROTEIN P; METHOXY ISOBUTYL ISONITRILE TECHNETIUM TC 99M; MULTIDRUG RESISTANCE PROTEIN; TETROFOSMIN TC 99M; VERAPAMIL;

ARTICLE; DRUG TRANSPORT; IMAGE ANALYSIS; MULTIDRUG RESISTANCE; POSITRON EMISSION TOMOGRAPHY; PROTEIN TRANSPORT; SINGLE PHOTON EMISSION COMPUTER TOMOGRAPHY;

ANIMALS; ANTINEOPLASTIC AGENTS; ATP-BINDING CASSETTE TRANSPORTERS; DRUG RESISTANCE, MULTIPLE; GENES, MDR; HUMANS; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; NEOPLASM PROTEINS; P-GLYCOPROTEIN; RADIOPHARMACEUTICALS; TOMOGRAPHY, EMISSION-COMPUTED; TOMOGRAPHY, EMISSION-COMPUTED, SINGLE-PHOTON;

EID: 0033061153     PISSN: 03406997     EISSN: None     Source Type: Journal    
DOI: 10.1007/s002590050390     Document Type: Article

References (91)

1. 1. Fojo AT, Ueda K, Slamon DJ, Poplack DG, Gottesman MM, Pastan I. Expression of a multidrug-resistance gene in human tumours and tissues. Proc Natl Acad Sci USA 1987; 84: 265-269.
2. 2. Goldstein LJ, Galski H, Fojo A, Willingham M, Lai SL, Gazdar A, Pirker R, Green A, Crist W, Brodeur GM, Lieber GM, Cossman J, Gottesman MM, Pastan I. Expression of a multidrug resistance gene in human cancers. J Natl Cancer Inst 1989; 81: 116-124.
3. 3. Bourhis J, Goldstein LJ, Riou G, Pastan I, Gottesman MM, Benard J. Expression of a human multidrug resistance gene in ovarian carcinomas. Cancer Res 1989; 49: 5062-5065.
4. 4. Dalton WS, Grogan TM, Meltzer PS, Scheper RJ, Durie BGM, Taylor CW, Miller TP, Salmon SE. Drug-resistance in multiple myeloma and non-Hodgkin's lymphoma: detection of P-glycoprotein and potential circumvention by addition of verapamil to chemotherapy. J Clin Oncol 1989; 7: 415-424.
5. 5. Goldie JH, Goldman AJ. The genetic origin of drug resistance in neoplasms: implications for systemic therapy. Cancer Res 1984; 44: 3643-3653.
6. 6. Gottesman MM, Pastan I. Biochemistry of multidrug resistance mediated by the multidrug transporter. Annu Rev Biochem 1993; 62: 385-427.
7. 7. Wood L, Palmer M, Hewitt J, Urtasun R, Bruera E, Rapp E, Thaell JF. Results of a phase III, double-blind, placebo-controlled trial of megestrol acetate modulation of P-glycoprotein-mediated drug resistance in the first-line management of small-cell lung carcinoma. Br J Cancer 1998; 77: 627-631.
8. 8. Zijlstra JG, de Vries EGE, Mulder NH. Multifactorial drug resistance in an adriamycin-resistant human small cell lung carcinoma cell line. Cancer Res 1987; 47: 1780-1784.
9. 9. Roninson IB, Abelson HT, Housman DE, Howell N, Varshavsky A. Amplification of specific DNA sequences correlates with multi-drug resistance in Chinese hamster cells. Nature 1984; 309: 626-628.
10. 10. Ueda K, Cornwell MM, Gottesman MM, Pastan I, Roninson IB, Ling V, Riordan JR. The mdr1 gene, responsible for multidrug-resistance, codes for P-glycoprotein. Biochem Biophys Res Commun 1986; 141: 856-862.
11. 11. Callen DF, Baker E, Simmers RN, Seshadri R, Roninson IB. Localization of the human multiple drug resistance gene, MDR1, to 7q21.1. Hum Genet 1987; 77: 122-126.
12. 12. Gros P, Croop J. Housman D. Mammalian multidrug resistance gene: complete cDNA sequence indicates strong homology to bacterial transport proteins. Cell 1986; 47: 371-380.
13. 13. Higgins CF. ABC transporters: from microorganisms to man. Annu Rev Cell Biol 1992; 8: 67-113.
14. 14. Tsuruo T, Lida H, Tsukagoshi S, Sakuray Y. Increased accumulation of vincristine and adriamycin in drug-resistant P388 tumour cells following incubation with calcium antagonists and calmodulin inhibitors. Cancer Res 1982; 42: 4730-4733.
15. 15. Herzog CE, Tsokos M, Bates SE, Fojo AT. Increased mdr-1/P-glycoprotein expression after treatment of human colon carcinoma cells with P-glycoprotein antagonists. J Biol Chem 1993; 268: 2946-2952.
16. 16. Nooter K, Oostrum R, Jonker R, Van Dekken H, Stokdijk W, Van den Engh G. Effect of cyclosporin A on daunomycin accumulation in multi-drug resistant P388 leukemia cells measured by real-time flow cytometry. Cancer Chemother Pharmacol 1989; 23: 296-300.
17. 17. Gavériaux C, Boesch D, Boelsterli JJ, Bollinger P, Eberle MK, Hiestand P, Payne T, Traber R, Wenger R, Loor F. Overcoming multidrug resistance in Chinese hamster ovary cells in vitro by cyclosporin A (Sandimmune) and non-immunosuppressive derivates. Br J Cancer 1989; 60: 867-871.
18. 18. Valverde MA, Diaz M, Sepulveda FV, Gill DR, Hyde SC, Higgins CF. Volume-regulated chloride channels associated with the human multidrug-resistance P-glycoprotein. Nature 1992; 355: 830-833.
19. 19. Abraham EH, Prat AG, Gerweck L, Seneveratne T, Arceci RJ, Kramer R, Guidotti G, Cantiello HF. The multidrug resistance (mdr1) gene product functions as an ATP channel. Proc Natl Acad Sci USA 1994; 90: 312-316.
20. 20. Van Asperen J, Schinkel AH, Beijnen JH, Nooijen WJ, Borst P, van Tellingen O. Altered pharmacokinetics of vinblastine in Mdr1a P-glycoprotein-deficient mice. J Natl Cancer Inst 1996; 88: 994-999.
21. 21. Cordon-Cardo C, O'Brien JP, Boccia J, Casals D, Bertino JR, Melamed MR. Expression of the multidrug resistance gene product (P-glycoprotein) in human normal and tumour tissues. J Histochem Cytochem 1990; 38: 1277-1287.
22. 22. Tsuij A, Terasaki T, Takabatake Y, Tenda Y, Yamashima T, Moritani S, Turuo T, Yamashita J. P-glycoprotein as drug efflux pump in primary cultured bovine brain capillary endothelial cells. Life Sci 1992; 51: 1427-1437.
23. 23. Zaman GJR, Versantvoort CH, Smit JJM, Eijdems EWHM, de Haas M, Smith AJ, Broxterman HJ, Mulder NH, de Vries EGE, 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 1993; 53: 1747-1750.
24. 24. Loe DW, Deeley RG, Cole SP. Biology of the multidrug resistance-associated protein, MRP. Eur J Cancer 1996; 32A: 945-957.
25. 25. Cole SP, Bhardwaj G, Gerlach JH, Mackie JE, Grant CE, Almquist KC, Stewart AJ, Kurz EU, Duncan AM, Deeley RG. Overexpression of a transporter gene in a multidrug-resistant human lung cancer cell line. Science 1992; 258: 1650-1654.
26. 26. Slovak ML, Ho JP, Bhardwaj G, Kurz EU, Deeley RG, Cole SP. Localization of a novel multidrug resistance-associated gene in the HT1080/DR4 and H69AR human tumour cell lines. Cancer Res 1993; 53: 3221-3225.
27. 27. Almquist KC, Loe DW, Hipfner DR, Mackie JE, Cole SP, Deeley SP. Characterization of the M(r) 190 000 multidrug resistance protein (MRP) in drug-selected and transfected human tumour cell. Cancer Res 1995; 55: 102-110.
28. 28. Flens MJ, Izquierdo MA, Schaffer GL, Fritz JM, Meijer CJ, Scheper RJ, Zaman GJR. Immunochemical detection of the multidrug resistance-associated protein MRP in human multidrug-resistant tumour cells by monoclonal antibodies. Cancer Res 1994; 54: 4556-4563.
29. 29. Marquardt D, Center MS. Drug transport mechanisms in HL60 cells isolated for resistance to adriamycin: evidence for nuclear drug accumulation and redistribution in resistant cells. Cancer Res 1992; 52: 3157-3163.
30. 30. Van Luyn MJA, Müller M, Renes J. Meijer C, Scheper RJ, Nienhuis EF, Mulder NH, Jansen PLM, De Vries EGE. Transport of glutathione conjugates into secretory vesicles is mediated by the multidrug-resistance protein 1. Int J Cancer 1998; 76: 55-62.
31. 31. Zaman GJR, Flens MJ, van Leusden MR, de Haas M, Mulder HS, Lankelma J. Pinedo HM, Scheper RJ, Boas F, Broxterman HJ, Borst P. The human multidrug resistance-associated protein MRP is a plasma membrane drug-efflux pump. Proc Natl Acad Sci USA 1994; 91: 8822-8826.
32. 32. Leier I, Jedlitschky G, Bucholz U, Cole SP, Deeley RG, Keppler D. The MRP gene encodes an ATP-dependent export pump for leukotriene C4 and structurally related conjugates. J Biochem Chem 1994; 269: 27807-27810.
33. 33. Müller M, Meijer C, Zaman GJ, Borst P, Scheper RJ, Mulder NH, de Vries EGE, Jansen PLM. Overexpression of the gene encoding the multidrug resistance-associated protein results in increased ATP-dependent glutathione S-conjugate transport. Proc Natl Acad Sci USA 1994; 91: 13033-13037.
34. 34. Versantvoort CHM, Broxterman HJ, Bagrij T, Scheper RJ, Twentyman PR. Regulation by glutathione of drug transport in multidrug-resistant human lung cell lines overexpressing multidrug resistance-associated protein. Br J Cancer 1995; 72: 82-89.
35. 35. Loe DW, Almquist KC, Deeley RG, Cole SPC. Multidrug resistance protein (MRP)-mediated transport of leukotriene C4 and chemotherapeutic agents in membrane vesicles. Demonstration of glutathione-dependent vincristine transport. J Biol Chem 1996; 271: 9675-9682.
36. 99mTc-sestamibi is a substrate for P-glycoprotein and the multidrug resistance associated protein. Br J Cancer 1998; 77: 353-358.
37. 37. Oude Elferink RPJ, Jansen PLM. The role of the canalicular multispecific organic anion transporter in the disposal of endo-and xenobiotics. Pharmacol Ther 1994; 64: 77-97.
38. 38. Evers R, Zaman GJR, Van Deemster L, Jansen H, Calafat J, Oomen LC, Oude Elferink RP, Borst P, Schinkel AH. Basolateral localization and export activity of the human multidrug resistance associated protein in polarized pig kidney cells. J Clin Invest 1996; 97: 1211-1218.
39. 39. Nishida T, Gatmaitan Z, Roy-Chowdhry J, Arias IM. Two distinct mechanisms for bilirubin glucuronide transport by rat bile canalicular membrane vesicles. Demonstration of defective ATP-dependent transport in rats (TR-) with inherited conjugated hyperbilirubinemia. J Clin Invest 1992; 90: 2130-2135.
40. 40. Ishikawa T, Müller M, Klünemann C, Schaub T, Keppler D. ATP-dependent primary active transport of cysteinyl leukotrienes across liver canalicular membranes. J Biol Chem 1990; 265: 19279-19286.
41. 41. Kuipers F, Enserink M, Havinga R, Van der Steen AB, Hardonk Mj, Vonk RJ. Separate transport systems for biliary secretion of sulfated and unsulfated bile acids in the rat. J Clin Invest 1988; 81: 1593-1599.
42. 42. Paulusma CC, Bosma PJ, Zaman GJR, Bakker CTM, Otter M, Schaffer GL, Scheper RJ, Borst P, Oude Elferink RPJ. Congenital jaundice in rats with a mutation in a multidrug resistance-associated protein gene. Science 1996; 271: 1126-1128.
43. 43. Büchler M, König J. Brom M, Kartenbeck J. Spring H, Horie T, Keppler D. cDNA cloning of the hepatocyte canalicular isoform of the multidrug resistance protein, CMRP, reveals a novel conjugate export pump deficient in hyperbilirubinemic mutant rats. J Biol Chem 1996; 271: 15091-15098.
44. 44. Kartenbeck J, Leuschner U, Mayer R, Keppler D. Absence of the canalicular isoform of the MRP gene-encoded conjugate export pump from the hepatocytes in Dubin-Johnson syndrome. Hepatology 1996; 23: 1061-1066.
45. 45. Paulusma CC, Kool M, Bosma PJ, Schaffer GL, Ter Borg, Scheper RJ, Tytgat GN, Borst P, Baas F, Oude Elferink RP. A mutation in the human canalicular multispecific organic anion transporter gene causes the Dubin-Johnson syndrome, Hepatology 1997; 25: 1539-1542.
46. 46. Kool M, de Haas M, Scheffer GL, Scheper RJ, van Eijk MJT, Juijn JA, 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 1997; 57: 3537-3547.
47. 47. Meijer C, Mulder NH, de Vries EGE. The role of detoxifying systems in resistance of tumour cells to cisplatin and adriamycin. Cancer Treat Rev 1990; 17: 389-407.
48. 48. Scheper RJ, Broxterman HJ, Schaffer GL, Kaaijk P, Dalton WS, van Heijningen THM, van Kalken CK, Slovak ML, de Vries EGE, van der Valk P, Meijer CJLM, Pinedo HM. Overexpression of a M(r) 110,000 vesicular protein in non-P-glycoprotein-mediated multidrug resistance. Cancer Res 1993; 53: 1475-1479.
49. 49. Scheffer GL, Wijngaard PL, Flens MJ, Izquierdo MA, Slovak ML, Pinedo HM, Meijer CJ, Clevers HC, Scheper RJ. The drug resistance-related protein LRP is the human major vault protein. Nature Med 1995; 6: 578-582.
50. 50. Noonan KE, Beck C, Holzmayer TA, Chin JE, Wunder JS, Andrulis IL, Gazdar AF, Willman CL, Griffith B, Von Hoff DD, Roninson IB. Quantitative analysis of MDRI (multidrug resistance) gene expression in human tumours by polymerase chain reaction. Proc Natl Acad Sci USA 1990; 87: 7160-7164.
51. 51. Bailly JD, Muller C, Jaffrezou JP, Demur C, Gassar G, Bordier C, Laurnt G. Lack of correlation between expression and function of P-glycoprotein in acute myeloid leukemia cell lines. Leukemia 1995; 9: 799-807.
52. 99mTc-sestamibi by GF120918. Proc Am Assoc Cancer Res 1996; 37: 2271.
53. 99mTechnetium-hexakis 2-methoxyisobutyl isonitrile: human biodistribution, dosimetry, safety, and preliminary comparison to thallium-201 for myocardial perfusion imaging. J Nucl Med 1989; 30: 301-311.
54. 54. Piwnica Worms D, Chiu ML, Budding M, Kronauge JF, Kramer RA, Croop JM. Functional imaging of multidrug-resistant P-glycoprotein with an organotechnetium complex. Cancer Res 1993; 53: 977-984.
55. 99mTc-hexakis 2-methoxy isobutyl isonitrile in benign and malignant lesions in the lungs. Clin Nucl Med 1989; 14: 333-340.
56. 99mtechnetium-MIBI with expression of P-glycoprotein in lung cancer. J Nucl Med 1998; 39: 228-234.
57. 57. Caner B, Kitapci M, Aras T, Erbengi G, Ugur O, Bekdik C. Increased accumulation of hexakis (2-methoxyisobutylisonitrile)technetium(I) in osteosarcoma and its metastatic lymph nodes. J Nucl Med 1991; 32: 1977-1978.
58. 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 1995; 16: 253-257.
59. 59. Barbaris E, Kronauge JF, Cohen D, Davison A, Jones AG, Croop JM. Characterization of P-glycoprotein transport and inhibition in vivo. Cancer Res 1998; 58: 276-282.
60. 99mtechnetium-sestamibi scan in untreated breast patients. Eur J Nucl Med 1997; 24: 150-159.
61. 99mtechnetium-sestamibi as a predictor of response to neoadjuvant chemotherapy for locally advanced breast cancer. J Clin Oncol 1998; 16: 1677-1683.
62. 62. Linn SC, Pinedo HM, van Ark-Otte J, van der Valk P, Hoekman K, Honkoop AH, Vermorken JB, Giaccone G. Expression of drug resistance proteins in breast cancer, in relationship to chemotherapy. Int J Cancer 1997; 71: 787-795.
63. 63. Dimitrakopoulou-Strauss A, Strauss LS, Goldschmidt H, Lorenz WJ, Maier Borst W, van Kaick G. Evaluation of tumour metabolism and multidrug resistance in patients with treated malignant lymphomas. Eur J Nucl Med 1995; 22: 434-442.
64. 99mtechnetium-sestamibi uptake in malignant tumours. J Nucl Med 1997; 38: 1003-1008.
65. 99mTc-tetrofosmin in breast tumour cells in vitro: role of multidrug resistance P-glycoprotein. J Nucl Med 1995; 36: 202P.
66. 99mTechnetium-tetrofosmin as a substrate for P-glycoprotein: in vitro studies in multidrug-resistant breast tumour cells. J Nucl Med 1996; 37: 1578-1582.
67. 99mTc-tetrofosmin accumulation in sensitive and multidrug resistant tumour cells with and without verapamil. Eur J Nucl Med 1096; 23: 1095.
68. 99mTc-tetrofosmin uptake in anaplastic thyroid carcinoma. Eur J Nucl Med 1996; 23: 1142.
69. 69. Crankshaw CL, Marmion M, Luker GD, Rao V, Dahlheimer J, Burleigh D, Webb E, Deutsch KF, Piwnica-Worms D. Novel technetium (III)-Q complexes for functional imaging of myltidrug resistance (MDR1) P-glycoprotein. J Nucl Med 1998; 39: 77-86.
70. 70. Luker GD, Rao VV, Crankshew CL, 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 1997; 36: 14218-14227.
71. 99mTechnetium-tetrofosmin as a substrate for P-glycoprotein: in vitro studies in multidrug-resistant breast tumour cells. J Nucl Med 1996; 37: 1578-1582.
72. 72. Miller TP, Graogan TS, Dalton WS, Spier CM, Scheper RJ, Salmon SE. P-glycoprotein expression in malignant lymphoma and reversal of clinical drug resistance with chemotherapy plus high dose verapamil. J Clin Oncol 1991; 9: 17-24.
73. 73. Hendrick AM, Harris AL, Cantwell BMJ. Verapamil with mitoxantrone for advanced ovarian cancer: a negative phase II trial Ann Oncol 1991; 2: 71-72.
74. 74. Rodenburg CJ, Nooter K, Herweijer H, Seynaeve C, Oosterom R, Stoter G, Verweij J. Phase II study of combining vinblastine and cyclosporin A to circumvent multidrug resistance in renal cell cancer. Ann Oncol 1991; 2: 305-306.
75. 99mtechnetium-sestamibi in vivo. J Nucl Med 1997; 38: 369-372.
76. 99mTc-sestamibi. Clin Cancer Res 1997; 3: 545-552.
77. 99mTc-MIBI in cells with P-glycoprotein-mediated and MRP-associated multidrug resistance phenotypes. Eur J Biochem 1998; 252: 140-146.
78. 99mTc-sestamibi is a substrate for MRP and its uptake is enhanced by the resistance modulator PAK-200S. Proc Am Assoc Cancer Res 1997; 38: 2942.
79. 99mTechnetium-sestamibi uptake in human breast carcinoma cell lines displaying glutathione-associated drug-resistance. Eur J Nucl Med 1996; 23: 568-570.
80. 99mTc-HIDA cholescintigraphy in Dubin-Johnson and Rotor syndromes. Radiology 1982; 142: 743-746.
81. 99mTc-HIDA cholescintigraphy in children with Dubin-Johnson syndrome. J Pediatr Gastroenterol Nutr 1983; 2: 311-312.
82. 82. Pinos T, Figueras C, Herranz R. Scintigraphic diagnosis of Dubin-Johnson syndrome: DISIDA is also useful. Am J Gastroenterol 1991; 86: 1687-1688.
83. 83. Ford JM, Hait WN. Pharmacology of drugs that alter multidrug resistance in cancer. Pharmacol Rev 1990; 42: 155-199.
84. 3H]colchicine. J Nucl Med 1992; 33: 1373-1377.
85. 85. Hunter AL, Klaassen CD. Biliary excretion of colchicine. J Pharmacol Exp Ther 1975; 192: 605-617.
86. 14C]-colchicine for identification of tumour multidrug resistance. J Nucl Med 1994; 35: 1179-1184.
87. 14C]-colchicine biodistribution with whole body quantitative autoradiography in colchicine-sensitive and -resistant xenografts. J Nucl Med 1996; 37: 312-314.
88. 11C]-labeled daunorubicin and verapamil for probing P-glycoprotein in tumours with PET. J Nucl Med 1996; 37: 1571-1575.
89. 11C]daunorubicin and positron emission tomography. Proc Am Assoc Cancer Res 1998; 39: 488.
90. 90. Denzlinger C, Guhlmann A, Scheuber PH, Wilker D, Hammer DK, Keppler D. Metabolism and analysis of cysteinyl leukotrienes in the monkey. J Biol Chem 1986; 261: 15601-15606.
91. 91. Guhlman A, Krauss K, Oberdorfer F, Siegel T, Scheuber PH, Müller J, Csuk-Glänzer B, Ziegler S, Ostertag H, Keppler D. Noninvasive assessment of hepatobiliary and renal elimination of cysteinyl leukotrienes by positron emission tomography. Hepatology 1995; 21: 1568-1575.