Folates provoke cellular efflux and drug resistance of substrates of the multidrug resistance protein 1 (MRP1)

Cancer Chemotherapy and Pharmacology

Volumn 73, Issue 5, 2014, Pages 911-917

  Hooijberg, Jan Hendrik ^a,b   Jansen, Gerrit ^b   Kathmann, Ietje ^b   Pieters, Rob ^c   Laan, Adrie C ^b   Van Zantwijk, Ina ^b   Kaspers, Gertjan J L ^b   Peters, Godefridus J ^b  

^a Department of Clinical Chemistry Slotervaartziekenhuis Amsterdam ^*  (Netherlands)

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^c SOPHIA CHILDREN S HOSPITAL   (Netherlands)

Author keywords

Anthracyclines; Calcein; Folate; Methotrexate; MRP1; Multidrug resistance

Indexed keywords

CALCEIN; DAUNORUBICIN; DOXORUBICIN; FOLIC ACID; METHOTREXATE;

ARTICLE; CELL CULTURE; CELL TYPE; CELLULAR EFFLUX; CONTROLLED STUDY; EFFUSION; FEMALE; HUMAN; HUMAN CELL; MULTIDRUG RESISTANCE; OVARIAN CANCER CELL LINE; OVARY CARCINOMA; PRIORITY JOURNAL; PROTEIN EXPRESSION;

BIOLOGICAL TRANSPORT; CELL LINE, TUMOR; DRUG RESISTANCE; FOLIC ACID; HUMANS; METHOTREXATE; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS;

EID: 84900799034     PISSN: 03445704     EISSN: 14320843     Source Type: Journal    
DOI: 10.1007/s00280-014-2421-0     Document Type: Article

References (44)

1. Bertino JR (1993) Ode to methotrexate. J Clin Oncol 11:5-14
2. Choi SW, Mason JB (2000) Folate and carcinogenesis: an integrated scheme. J Nutr 130:129-132
3. Molloy AM, Scott JM (2001) Folates and prevention of disease. Public Health Nutr 4(2B):601-609 (Pubitemid 32524580)
4. Kim YI (2003) Role of folate in colon cancer development and progression. J Nutr 133(Suppl 1):3731S-3739S
5. Mason JB (2011) Unraveling the complex relationship between folate and cancer risk. BioFactors 37:253-260
6. Weggemans RM, Schaafsma G, Kromhout D, Health Council of the Netherlands (2009) Toward an optimal use of folic acid: an advisory report of the Health Council of the Netherlands. Eur J Clin Nutr 63:1034-1036
7. Vollset SE, Clarke R, Lewington S, Ebbing M, Halsey J, Lonn E, Armitage J, Manson JE, Hankey GJ, Spence JD, Galan P, Bønaa KH, Jamison R, Gaziano JM, Guarino P, Baron JA, Logan RF, Giovannucci EL, den Heijer M, Ueland PM, Bennett D, Collins R, Peto R (2013) Effects of folic acid supplementation on overall and site-specific cancer incidence during the randomised trials: metaanalyses of data on 50.000 individuals. Lancet 381:1029-1036
8. Qin X, Cui Y, Shen L, Sun N, Zhang Y, Li J, Xu X, Wang B, Xu X, Huo Y, Wang X (2013) Folic acid supplementation and cancer risk: a meta-analysis of randomized controlled trials. Int J Cancer 133:1033-1041
9. Bertino JR (1977) "Rescue" techniques in cancer chemotherapy: use of leucovorin and other rescue agents after methotrexate treatment. Semin Oncol 4(sup2):203-216
10. Zervos PH, Allen RH, Thornton DE, Thiem PA (1997) Functional folate status as a prognostic indicator of toxicity in clinical trials of the multitargeted antifolate LY231514. Eur J Cancer (suppl) 33:S18
11. Vogelzang NJ, Rusthoven JJ, Symanowski J, Denham C, Kaukel E, Ruffie P, Gatzemeier U, Boyer M, Emri S, Manegold C, Niyikiza C, Paoletti P (2003) Phase III study of pemetrexed in combination with cisplatin versus cisplatin alone in patients with malignant pleural mesothelioma. J Clin Oncol 21:2636-2644 (Pubitemid 46606305)
12. Porcelli L, Assaraf YG, Azzariti A, Paradiso A, Jansen G, Peters GJ (2011) The impact of folate status on the efficacy of colorectal cancer treatment. Curr Drug Metab 12:975-984
13. Hooijberg JH, Jansen G, Assaraf YG, Kathmann I, Pieters R, Laan AC, Veerman AJP, Kaspers GJ, Peters GJ (2004) Folate concentration dependent transport activity of the Multidrug Resistance Protein 1 (ABCC1). Biochem Pharmacol 67:1541-1548 (Pubitemid 38388216)
14. Cole SP, Bhardwaj G, Gerlach J, 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 (Pubitemid 23012438)
15. Borst P, Evers R, Kool M, Wijnholds J (2000) A family of drug transporters: the multidrug resistance-associated proteins. J Natl Cancer Inst 92:1295-1302 (Pubitemid 30662093)
16. Borst P, Elferink RO (2002) Mammalian ABC transporters in health and disease. Annu Rev Biochem 71:537-592 (Pubitemid 34800230)
17. Scotto KW (2003) Transcriptional regulation of ABC drug transporters. Oncogene 20(22):7496-74511
18. Kruh GD, Belinsky MG (2003) The MRP family of drug efflux pumps. Oncogene 20(22):7537-7552 (Pubitemid 37487175)
19. Dean M, Allikmets R (2001) Complete characterization of the human ABC gene family. J Bioenerg Biomembr 33:475-479 (Pubitemid 34052573)
20. Hooijberg JH, Broxterman HJ, Kool M, Assaraf YG, Peters GJ, Noordhuis P, Scheper RJ, Borst P, Pinedo HM, Jansen G (1999) Antifolate resistance mediated by the multidrug resistance proteins MRP1 and MRP2. Cancer Res 59:2532-2535 (Pubitemid 29269093)
21. Chen ZS, Tiwari AK (2011) Multidrug resistance proteins (MRPs/ABCCs) in cancer chemotherapy and genetic diseases. FEBS J 278:3226-3245
22. Cole SP (2014) Targeting Multidrug Resistance Protein 1 (MRP1, ABCC1): past, present, and future. Annu Rev Pharmacol Toxicol 54:95-117
23. Kool M, Van der Linden M, De Haas M, Scheffer GL, De Vree ML, Smith AJ, Jansen G, Peters GJ, Ponne N, Scheper RJ, Oude Elferink RPV, Baas F, Borst P (1999) MRP3, a new organic anion transporter able to transport anti-cancer drugs. Proc Natl Acad Sci USA 96:6914-6918
24. Zeng H, Chen ZS, Belinsky MG, Rea PA, Kruh GD (2001) Transport of methotrexate (MTX) and folates by Multidrug Resistance Protein (MRP) 3 and MRP1: effect of poly-glutamylation on MTX transport. Cancer Res 61:7225-7232 (Pubitemid 32946519)
25. Lee K, Klein-Szanto AJ, Kruh GD (2000) Analysis of the MRP4 drug resistance profile in transfected NIH3T3 cells. J Natl Cancer Inst 92:1934-1940 (Pubitemid 32036924)
26. Chen ZS, Lee K, Walther S, Blanchard R, Kuwano M, Zeng H, Kruh GD (2002) Analysis of methotrexate and folate transport by Multidrug Resistance Protein 4 (ABCC4): MRP4 is a component of the methotrexate efflux system. Cancer Res 62:3144-3150 (Pubitemid 34602407)
27. Cronstein BN (1996) Methotrexate and its mechanism of action. Arthritis Rheum 39:1951-1960
28. Purcell WT, Ettinger DS (2003) Novel antifolate drugs. Curr Oncol Rep 5:114-125 (Pubitemid 38898774)
29. Zhao R, Goldman ID (2003) Resistance to antifolates. Oncogene 22:7431-7457 (Pubitemid 37487168)
30. Hooijberg JH, Peters GJ, Assaraf YG, Kathmann I, Priest DG, Bunni MA, Veerman AJ, Scheffer GL, Kaspers GJ, Jansen G (2003) The role of multidrug resistance proteins MRP1, MRP2 and MRP3 in cellular folate homeostasis. Biochem Pharmacol 65:765-771 (Pubitemid 36293693)
31. 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
32. Gekeler V, Ise W, Sanders KH, Ulrich WR, Beck J (1995) The leukotriene LT D4 receptor antagonist MK571 specifically modulates MRP associated multidrug resistance. Biochem Biophys Res Commun 208:345-352
33. Wielinga PR, Heijn M, Westerhoff HV, Lankelma J (1998) A method for studying plasma membrane transport with intact cells using computerized fluorometry. Anal Biochem 263:221-231 (Pubitemid 28480808)
34. Ruiz van Haperen VWT, Veerman G, Boven E, Noordhuis P, Vermorken JB, Peters GJ (1994) Schedule dependence of sensitivity to 2′,2- difluorocytidine (gemcitabine) in relation to accumulation and retention of its triphosphate in solid tumor cell lines and solid tumors. Biochem Pharmacol 48:1327-1339
35. Peters GJ, Kathmann I, Lemos C, Hooijberg JH, Losekoot N, Jansen G (2013) Folate homeostasis of cancer cells affects sensitivity to not only antifolates but also other non-folate drugs: effect of MRP expression. Pteridines 24:81-86
36. Loe DW, Deeley RG and Cole SP (1998) Characterization of vincristine transport by the Mw 190,000 kD Multidrug resistance protein (MRP): evidence for cotransport with reduced glutathione. Cancer Res 58:5130-5136 (Pubitemid 28521173)
37. Jedlitschky G, Leier I, Buchholz U, Barnouin K, Kurz G, Keppler D (1996) Transport of glutathione, glucuronate, and sulfate conjugates by the MRP gene-encoded conjugate export pump. Cancer Res 56:988-994 (Pubitemid 26065391)
38. Qian YM, Song WC, Cui H, Cole SP, Deeley RG (2001) Glutathione stimulates sulfated estrogen transport by Multidrug Resistance Protein 1. J Biol Chem 276:6404-6411
39. Borst P, Evers R, Kool M, Wijnholds J (1999) The Multidrug Resistance Protein Family. Biochem Biophys Acta 1461:347-357
40. Jhaveri MS, Wagner C, Trepel JB (2001) Impact of extracellular folate levels on global gene expression. Mol Pharmacol 60:1288-1295 (Pubitemid 33144900)
41. Zingg JM, Jones PA (1997) Genetic and epigenetic aspects of DNA methylation on genome expression, evolution, mutation and carcinogenesis. Carcinogenesis 18:869-882
42. Assaraf YG, Rothem L, Hooijberg JH, Stark M, Ifergan I, Kathmann I, Dijkmans BA, Peters GJ, Jansen G (2003) Loss of multidrug resistance protein 1 expression and folate efflux activity results in a highly concentrative folate transport in human leukemia cells. J Biol Chem 278:6680-6686 (Pubitemid 36800654)
43. Priest DG, Schmitz JC, Bunni MA, Stuart RK (1991) Pharmacokinetics of leucovorin metabolites in human plasma as a function of dose administered orally and intravenously. J Natl Cancer Inst 83:1806-1812
44. Choumenkovitch SF, Selhub J, Wilson PWF, Rader JI, Rosenberg IH, Jacques PF (2002) Folic acid intake from fortification in United States exceeds predictions. J Nutr 132:2792-2798 (Pubitemid 35013272)