Competition between innate multidrug resistance and intracellular binding of rhodamine dyes

FEBS Journal

Volumn 276, Issue 3, 2009, Pages 637-648

  Yeheskely Hayon, Daniella ^a   Regev, Ronit ^a   Katzir, Hagar ^a   Eytan, Gera D ^a  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

Innate multidrug resistance; MDR; MRP1; Multidrug resistance; Rhodamines

Indexed keywords

4 CHLORO 7 NITROBENZOFURAZAN; ABC TRANSPORTER; CARBONYL CYANIDE CHLOROPHENYLHYDRAZONE; CHLOROMERCURIBENZENESULFONIC ACID; CONCANAMYCIN A; CYCLOSPORIN A; DICYCLOHEXYLCARBODIIMIDE; DOXORUBICIN; GLUTATHIONE; INDOMETACIN; MULTIDRUG RESISTANCE PROTEIN; N ETHYLMALEIMIDE; PROBENECID; RHODAMINE; VANADIC ACID; VERLUKAST;

ARTICLE; CELL STRAIN K 562; CONTROLLED STUDY; CYTOPLASM; FLUORESCENCE; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; MITOCHONDRION; MULTIDRUG RESISTANCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RADIOASSAY;

DRUG RESISTANCE, MULTIPLE; FLUORESCENT DYES; HUMANS; K562 CELLS; KINETICS; RHODAMINES;

EID: 58449111035     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2008.06812.x     Document Type: Article

References (49)

1. Juliano RL Ling V (1976) A surface glycoprotein modulating drug permeability in Chinese hamster ovary cell mutants. Biochim Biophys Acta 455, 152 162.
2. Chen CJ, Chin JE, Ueda K, Clark DP, Pastan I, Gottesman MM Roninson IB (1986) Internal duplication and homology with bacterial transport proteins in the mdr1 (P-glycoprotein) gene from multidrug-resistant human cells. Cell 47, 381 389.
3. Gros P, Croop J Housman D (1986) Mammalian multidrug resistance gene: complete cDNA sequence indicates strong homology to bacterial transport proteins. Cell 47, 371 380.
4. Borst P Elferink RO (2002) Mammalian ABC transporters in health and disease. Annu Rev Biochem 71, 537 592.
5. Szakacs G, Paterson JK, Ludwig JA, Booth-Genthe C Gottesman MM (2006) Targeting multidrug resistance in cancer. Nat Rev Drug Discov 5, 219 234.
6. Cole SP, Bhardwaj G, Gerlach JH, Mackie JE, Grant CE, Almquist KC, Stewart AJ, Kurz EU, Duncan AM Deeley RG (1992) Overexpression of a transporter gene in a multidrug-resistant human lung cancer cell line. Science 258, 1650 1654.
7. Doyle LA, Yang W, Abruzzo LV, Krogmann T, Gao Y, Rishi AK Ross DD (1998) A multidrug resistance transporter from human MCF-7 breast cancer cells Published erratum appears in Proc Natl Acad Sci USA 1999; 96: 2569 Proc Natl Acad Sci USA 95, 15665 15670.
8. Miyake K, Mickley L, Litman T, Zhan Z, Robey R, Cristensen B, Brangi M, Greenberger L, Dean M, Fojo T et al. (1999) Molecular cloning of cDNAs which are highly overexpressed in mitoxantrone-resistant cells: demonstration of homology to ABC transport genes. Cancer Res 59, 8 13.
9. Allikmets R, Schriml LM, Hutchinson A, Romano-Spica V Dean M (1998) A human placenta-specific ATP-binding cassette gene (ABCP) on chromosome 4q22 that is involved in multidrug resistance. Cancer Res 58, 5337 5339.
10. Eytan GD Kuchel PW (1999) Mechanism of action of P-glycoprotein in relation to passive membrane permeation. Int Rev Cytol 190, 175 250.
11. Stein WD (1997) Kinetics of the multidrug transporter (P-glycoprotein) and its reversal. Physiol Rev 77, 545 590.
12. Wielinga PR, Westerhoff HV Lankelma J (2000) The relative importance of passive and P-glycoprotein mediated anthracycline efflux from multidrug-resistant cells. Eur J Biochem 267, 649 657.
13. Mankhetkorn S, Dubru F, Hesschenbrouck J, Fiallo M Garnier-Suillerot A (1996) Relation among the resistance factor, kinetics of uptake, and kinetics of the P-glycoprotein-mediated efflux of doxorubicin, daunorubicin, 8-(S)-fluoroidarubicin, and idarubicin in multidrug-resistant K562 cells. Mol Pharmacol 49, 532 539.
14. Loetchutinat C, Saengkhae C, Marbeuf-Gueye C Garnier-Suillerot A (2003) New insights into the P-glycoprotein-mediated effluxes of rhodamines. Eur J Biochem 270, 476 485.
15. Schinkel AH, Smit JJ, van Tellingen O, Beijnen JH, Wagenaar E, van Deemter L, Mol CA, van der Valk MA, Robanus-Maandag EC, te Riele HP et al. (1994) 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, 491 502.
16. Lankas GR, Wise LD, Cartwright ME, Pippert T Umbenhauer DR (1998) Placental P-glycoprotein deficiency enhances susceptibility to chemically induced birth defects in mice. Reprod Toxicol 12, 457 463.
17. Sparreboom A, van Asperen J, Mayer U, Schinkel AH, Smit JW, Meijer DK, Borst P, Nooijen WJ, Beijnen JH van Tellingen O (1997) Limited oral bioavailability and active epithelial excretion of paclitaxel (Taxol) caused by P-glycoprotein in the intestine. Proc Natl Acad Sci USA 94, 2031 2035.
18. Kamimoto Y, Gatmaitan Z, Hsu J Arias IM (1989) The function of Gp170, the multidrug resistance gene product, in rat liver canalicular membrane vesicles. J Biol Chem 264, 11693 11698.
19. Johnson DR, Finch RA, Lin ZP, Zeiss CJ Sartorelli AC (2001) The pharmacological phenotype of combined multidrug-resistance mdr1a/1b- and mrp1-deficient mice. Cancer Res 61, 1469 1476.
20. Schinkel AH, Mayer U, Wagenaar E, Mol CA, van Deemter L, Smit JJ, van der Valk MA, Voordouw AC, Spits H, van Tellingen O 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.
21. Lorico A, Rappa G, Finch RA, Yang D, Flavell RA Sartorelli AC (1997) 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, 5238 5242.
22. Maliepaard M, Scheffer GL, Faneyte IF, van Gastelen MA, Pijnenborg AC, Schinkel AH, van De Vijver MJ, Scheper RJ Schellens JH (2001) Subcellular localization and distribution of the breast cancer resistance protein transporter in normal human tissues. Cancer Res 61, 3458 3464.
23. Chen LB (1989) Fluorescent labeling of mitochondria. Methods Cell Biol 29, 103 123.
24. Marbeuf-Gueye C, Broxterman HJ, Dubru F, Priebe W Garnier-Suillerot A (1998) Kinetics of anthracycline efflux from multidrug resistance protein-expressing cancer cells compared with P-glycoprotein-expressing cancer cells. Mol Pharmacol 53, 141 147.
25. al-Shawi MK Senior AE (1993) Characterization of the adenosine triphosphatase activity of Chinese hamster P-glycoprotein. J Biol Chem 268, 4197 4206.
26. Chen ZS, Hopper-Borge E, Belinsky MG, Shchaveleva I, Kotova E Kruh GD (2003) Characterization of the transport properties of human multidrug resistance protein 7 (MRP7, ABCC10). Mol Pharmacol 63, 351 358.
27. Gekeler V, Ise W, Sanders KH, Ulrich WR Beck J (1995) The leukotriene LTD4 receptor antagonist MK571 specifically modulates MRP associated multidrug resistance. Biochem Biophys Res Commun 208, 345 352.
28. van Aubel RA, van Kuijck MA, Koenderink JB, Deen PM, van Os CH Russel FG (1998) Adenosine triphosphate-dependent transport of anionic conjugates by the rabbit multidrug resistance-associated protein Mrp2 expressed in insect cells. Mol Pharmacol 53, 1062 1067.
29. Feller N, Broxterman HJ, Wahrer DC Pinedo HM (1995) ATP-dependent efflux of calcein by the multidrug resistance protein (MRP): no inhibition by intracellular glutathione depletion. FEBS Lett 368, 385 388.
30. Rabindran SK, He H, Singh M, Brown E, Collins KI, Annable T Greenberger LM (1998) Reversal of a novel multidrug resistance mechanism in human colon carcinoma cells by fumitremorgin C. Cancer Res 58, 5850 5858.
31. Eytan GD, Regev R, Oren G Assaraf YG (1996) The role of passive transbilayer drug movement in multidrug resistance and its modulation. J Biol Chem 271, 12897 12902.
32. Horio M, Gottesman MM Pastan I (1988) ATP-dependent transport of vinblastine in vesicles from human multidrug-resistant cells. Proc Natl Acad Sci USA 85, 3580 3584.
33. Qian YM, Qiu W, Gao M, Westlake CJ, Cole SPC Deeley RG (2001) Characterization of binding of leukotriene C4 by human multidrug resistance protein 1. Evidence of differential interactions with NH2-and COOH-proximal halves of the protein. J Biol Chem 276, 38636 38644.
34. Bakos E, Evers R, Sinko E, Varadi A, Borst P Sarkadi B (2000) Interactions of the human multidrug resistance proteins MRP1 and MRP2 with organic anions. Mol Pharmacol 57, 760.
35. Aubel R, Kuijck MA, Koenderink JB, Deen PMT, Os CH Russel FGM (1998) Adenosine triphosphate-dependent transport of anionic conjugates by the rabbit multidrug resistance-associated protein Mrp2 expressed in insect cells. Mol Pharmacol 53, 1062.
36. Reid G, Wielinga P, Zelcer N, De Haas M, Van Deemter L, Wijnholds J, Balzarini J Borst P (2003) Characterization of the transport of nucleoside analog drugs by the human multidrug resistance proteins MRP4 and MRP5. Mol Pharmacol 63, 1094 1103.
37. Evers R, de Haas M, Sparidans R, Beijnen J, Wielinga PR, Lankelma J Borst P (2000) Vinblastine and sulfinpyrazone export by the multidrug resistance protein MRP2 is associated with glutathione export. Br J Cancer 83, 375 383.
38. Bodo A, Bakos E, Szeri F, Varadi A Sarkadi B (2003) Differential modulation of the human liver conjugate transporters MRP2 and MRP3 by bile acids and organic anions. J Biol Chem 278, 23529 23537.
39. Reid G, Wielinga P, Zelcer N, van der Heijden I, Kuil A, de Haas M, Wijnholds J Borst P (2003) The human multidrug resistance protein MRP4 functions as a prostaglandin efflux transporter and is inhibited by nonsteroidal antiinflammatory drugs. Proc Natl Acad Sci USA 100, 9244 9249.
40. Ilias A, Urban Z, Seidl TL, Le Saux O, Sinko E, Boyd CD, Sarkadi B Varadi A (2002) Loss of ATP-dependent transport activity in pseudoxanthoma elasticum-associated mutants of human ABCC6 (MRP6). J Biol Chem 277, 16860 16867.
41. Lozzio CB Lozzio BB (1975) Human chronic myelogenous leukemia cell-line with positive Philadelphia chromosome. Blood 45, 321 334.
42. Adachi M, Sampath J, Lan LB, Sun D, Hargrove P, Flatley R, Tatum A, Edwards MZ, Wezeman M, Matherly L et al. (2002) Expression of MRP4 confers resistance to ganciclovir and compromises bystander cell killing. J Biol Chem 277, 38998 39004.
43. Wijnholds J, Mol CA, van Deemter L, de Haas M, Scheffer GL, Baas F, Beijnen JH, Scheper RJ, Hatse S, De Clercq E et al. (2000) Multidrug-resistance protein 5 is a multispecific organic anion transporter able to transport nucleotide analogs. Proc Natl Acad Sci USA 97, 7476 7481.
44. Storkus WJ, Alexander J, Payne JA, Dawson JR Cresswell P (1989) Reversal of natural killing susceptibility in target cells expressing transfected class I HLA genes. Proc Natl Acad Sci USA 86, 2361 2364.
45. McCarthy RE, Junius V, Farber S, Lazarus H Foley GE (1965) Cytogenetic analysis of human lymphoblasts in continuous culture. Exp Cell Res 40, 197 200.
46. Weiss A, Wiskocil RL Stobo JD (1984) The role of T3 surface molecules in the activation of human T cells: a two-stimulus requirement for IL 2 production reflects events occurring at a pre-translational level. J Immunol 133, 123 128.
47. Zijlstra JG, de Vries EG Mulder NH (1987) Multifactorial drug resistance in an adriamycin-resistant human small cell lung carcinoma cell line. Cancer Res 47, 1780 1784.
48. Davey RA, Longhurst TJ, Davey MW, Belov L, Harvie RM, Hancox D Wheeler H (1995) Drug resistance mechanisms and MRP expression in response to epirubicin treatment in a human leukaemia cell line. Leuk Res 19, 275 282.
49. Beckmann R, Smythe JS, Anstee DJ Tanner MJ (1998) Functional cell surface expression of band 3, the human red blood cell anion exchange protein (AE1), in K562 erythroleukemia cells: band 3 enhances the cell surface reactivity of Rh antigens. Blood 92, 4428 4438.