6-Mercaptopurine and 9-(2-phosphonyl-methoxyethyl) adenine (PMEA) transport altered by two missense mutations in the drug transporter gene ABCC4

Human Mutation

Volumn 29, Issue 5, 2008, Pages 659-669

  Janke, Daniel ^a   Mehralivand, Sherif ^a   Strand, Dennis ^a   Gödtel Armbrust, Ute ^a   Habermeier, Alice ^a   Gradhand, Ulrike ^b   Fischer, Christine ^c   Toliat, Mohammad R ^e   Fritz, Peter ^c   Zanger, Ulrich M ^c   Schwab, Matthias ^c,d   Fromm, Martin F ^b   Nürnberg, Peter ^e   Wojnowski, Leszek ^a   Closs, Ellen L ^a   Lang, Thomas ^a  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

^b UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^c UNIVERSITY OF TÜBINGEN   (Germany)

^d UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^e UNIVERSITY OF COLOGNE   (Germany)

Author keywords

ABC transporter; ABCC4; Human hepatic expression; MRP4; Multidrug resistance protein 4; Protein variants; Xenopus laevis oocytes

Indexed keywords

ABC TRANSPORTER; ADEFOVIR; GREEN FLUORESCENT PROTEIN; MERCAPTOPURINE; MULTIPLE DRUG RESISTANCE PROTEIN 4;

ARTICLE; CAUCASIAN; DRUG TRANSPORT; EFFUSION; FEMALE; GENE EXPRESSION; GENE FUNCTION; GENE LOCATION; GENETIC VARIABILITY; HUMAN; HUMAN TISSUE; ISOTOPE LABELING; MAJOR CLINICAL STUDY; MISSENSE MUTATION; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN VARIANT; SINGLE NUCLEOTIDE POLYMORPHISM; WILD TYPE; XENOPUS LAEVIS;

6-MERCAPTOPURINE; ADENINE; ANIMALS; BASE SEQUENCE; DNA PRIMERS; GREEN FLUORESCENT PROTEINS; HUMANS; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; MUTAGENESIS, SITE-DIRECTED; MUTATION, MISSENSE; PHOSPHONIC ACIDS; RECOMBINANT FUSION PROTEINS; XENOPUS LAEVIS;

XENOPUS LAEVIS;

EID: 42949168885     PISSN: 10597794     EISSN: None     Source Type: Journal    
DOI: 10.1002/humu.20694     Document Type: Article

References (42)

1. Adachi M, Sampath J, Lan LB, Sun D, Hargrove P, Flatley R, Tatum A, Edwards MZ, Wezeman M, Matherly L, Drake R, Schuetz J. 2002. Expression of MRP4 confers resistance to ganciclovir and compromises bystander cell killing. J Biol Chem 277:38998-39004.
2. Belinsky MG, Guo P, Lee K, Zhou F, Kotova E, Grinberg A, Westphal H, Shchaveleva I, Klein-Szanto A, Gallo JM, Kruh GD. 2007. Multidrug resistance protein 4 protects bone marrow, thymus, spleen, and intestine from nucleotide analogue-induced damage. Cancer Res 67:262-268.
3. Borst P, de Wolf C, van de Wetering K. 2007. Multidrug resistance-associated proteins 3, 4, and 5. Pflugers Arch 453:661-673.
4. Castillo G, Vera JC, Yang CPH, Horwitz SB. 1990. Functional expression of murine multidrug resistance in Xenopus laevis oocytes. Proc Natl Acad Sci USA 87:4737-4741.
5. Chen ZS, Lee K, Kruh GD. 2001. Transport of cyclic nucleotides and estradiol 17-b-D-glucuronide by multidrug resistance protein 4. Resistance to 6-mercaptopurine and 6-thioguanine. J Biol Chem 276:33747-33754.
6. Chen ZS, Lee K, Walther S, Raftogianis RB, 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.
7. Frelet A, Klein M. 2006. Insight in eukaryotic ABC transporter function by mutation analysis. FEBS Lett 580:1064-1084.
8. Gao M, Cui HR, Loe DW, Grant CE, Almquist KC, Cole SP, Deeley RG. 2000. Comparison of the functional characteristics of the nucleotide binding domains of multidrug resistance protein 1. J Biol Chem 17:13098-13108.
9. Gerloff T, Stieger B, Hagenbuch B, Madon J, Landmann L, Roth J, Hofmann AF, Meier PJ. 1998. The sister of P-glycoprotein represents the canalicular bile salt export pump of mammalian liver. J Biol Chem 16:1046-1050.
10. Gradhand U, Lang T, Schaeffeler E, Glaeser H, Tegude H, Klein K, Fritz P, Jedlitschky G, Kroemer HK, Bachmakov I, Anwald B, Kerb R, Zanger UM, Eichelbaum M, Schwab M, Fromm MF. Variability in human hepatic MRP4 expression: influence of cholestasis and genotype. Pharmacogenomics J (in press). [Epub ahead of print].
11. Grantham R. 1974. Amino acid difference formula to help explain protein evolution. Science 185:862-864.
12. Haimeur A, Conseil G, Deeley RG, Cole SPC. 2004. The MRP-related and BCRP/ABCG2 multidrug resistance proteins: biology, substrate specificity and regulation. Curr Drug Metab 5:21-53.
13. Herrlinger KR, Kreisel W, Schwab M, Schoelmerich J, Fleig WE, Ruhl A, Reinshagen M, Deibert P, Fellermann K, Greinwald R, Stange EF. 2003. 6-thioguanine-efficacy and safety in chronic active Crohn's disease. Aliment Pharmacol Ther 17:503-508.
14. Hitzl M, Klein K, Zanger UM, Fritz P, Nussler AK, Neuhaus P, Fromm MF. 2003. Influence of omeprazole on multidrug resistance protein 3 expression in human liver. J Pharmacol Exp Ther 304:524-530.
15. - cotransporter. J Am Soc Nephrol 14:271-282.
16. Jedlitschky G, Tirschmann K, Lubenow LE, Nieuwenhuis HK, Akkerman JW, Greinacher A, Kroemer HK. 2004. The nucleotide transporter MRP4 (ABCC4) is highly expressed in human platelets and present in dense granules, indicating a role in mediator storage. Blood 12:3603-3610.
17. Keitel V, Burdelski M, Warskulat U, Kuhlkamp T, Keppler D, Haussinger D, Kubitz R. 2005. Expression and localization of hepatobiliary transport proteins in progressive familial intrahepatic cholestasis. Hepatology 41:1160-1172.
18. Kerb R, Brinkmann U, Chatskaia N, Gorbunov D, Gorboulev V, Mornhinweg E, Keil A, Eichelbaum M, Koepsell H. 2002. Identification of genetic variations of the human organic cation transporter hOCT1 and their functional consequences. Pharmacogenetics 12:591-595.
19. Lang T, Klein K, Fischer J, Nussler AK, Neuhaus P, Hofmann U, Eichelbaum M, Schwab M, Zanger UM. 2001. Extensive genetic polymorphism in the human CYP2B6 gene with impact on expression and function in human liver. Pharmacogenetics 11:399-415.
20. Lee K, Klein-Szanto AJP, Kruh GD. 2000. Analysis of the MRP4 drug resistance proÆle in transfected NIH3T3 cells. J Natl Cancer Inst 92:1934-1940.
21. Leggas M, Adachi M, Scheffer GL, Sun D, Wielinga P, Du G, Mercer KE, Zhuang Y, Panetta JC, Johnston B, Scheper RJ, Stewart CF, Schuetz JD. 2004. Mrp4 confers resistance to topotecan and protects the brain from chemotherapy. Mol Cell Biol 17:7612-7621.
22. Li WH, Wu CI, Luo CC. 1984- Nonrandomness of point mutation as reflected in nucleotide substitutions in pseudogenes and its evolutionary implications. J Mol Evol 2:58-71.
23. Madon J, Eckhardt U, Gerloff T, Stieger B, Meier PJ. 1997. Functional expression of the rat liver canalicular isoform of the multidrug resistance-associated protein. FEBS Lett 406:75-78.
24. Marschall HU, Wagner M, Bodin K, Zollner G, Fickert P, Gumhold J, Silbert D, Fuchsbichler A, Sjovall J, Trauner M. 2005. Fxr-/- mice adapt to biliary obstruction by enhanced phase I detoxification and renal elimination of bile acids. J Lipid Res 47:582-592.
25. Nakanishi T, Doyle LA, Hassel B, Wei Y, Bauer KS, Wu S, Pumplin DW, Fang HB, Ross DD. 2003. Functional characterization of human breast cancer resistance protein (BCRP, ABCG2) expressed in the oocytes of Xenopus laevis. Mol Pharmacol 6:1452-1462.
26. Neurath MF, Kiesslich R, Teichgraber U, Fischer C, Hofmann U, Eichelbaum M, Galle PR, Schwab M. 2005. 6-thioguanosine diphosphate and triphosphate levels in red blood cells and response to azathioprine therapy in Crohn's disease. Clin Gastroenterol Hepatol 3:1007-1014.
27. Ng PC, Henikoff S. 2003. SIFT: predicting amino acid changes that affect protein function. Nucleic Acids Res 31:3812-3814.
28. Nozawa T, Minami H, Sugiura S, Tsuji A, Tamai I. 2005. Role of organic anion transporter OATP1B1 (OATP-C) in hepatic uptake of irinotecan and its active metabolite, 7-ethyl-10-hydroxycamptothecin: in vitro evidence and effect of single nucleotide polymorphisms. Drug Metab Dispos 3:434-439.
29. Ramensky V, Bork P, Sunyaev S. 2002. Human non-synonymous SNPs: server and survey. Nucleic Acids Res 30:3894-3900.
30. Reid G, Wielinga P, Zelcer N, van der Heijden I, Kuil A, de Haas M, Wijnholds J, Borst P. 2003a. 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.
31. Reid G, Wielinga P, Zelcer N, de Haas M, van Deemter L, Wijnholds J, Balzarini J, Borst P. 2003b. Characterization of the transport of nucleoside analog drugs by the human multidrug resistance proteins MRP4 and MRP5. Mol Pharmacol 63:1094-1103.
32. Rius M, Nies AT, Hummel-Eisenbeiss J, Jedlitschky G, Keppler D. 2003. Cotransport of reduced glutathione with bile salts by MRP4 ABCC4 localized to the basolateral hepatocyte membrane. Hepatology 38:374-384.
33. Sampath J, Adachi M, Hatse S, Naesens L, Balzarini J, Flatley RM, Matherly LH, Schuetz JD. 2002. Role of MRP4 and MRP5 in biology and chemotherapy. AAPS PharmSci 4:E14.
34. Schuetz JD, Connelly MC, Sun D, Paibir SG, Flynn PM, Srinivas RV, Kumar A, Fridland A. 1999. MRP4: a previously unidentified factor in resistance to nucleoside-based antiviral drugs. Nat Med 5:1048-1051.
35. Shu Y, Leabman MK, Feng B, Mangravite LM, Huang CC, Stryke D. 2003. Evolutionary conservation predicts function of variants of the human organic cation transporter, OCT1. Proc Natl Acad Sci USA 100:5902-5907.
36. Tian Q, Zhang J, Tan TM, Chan E, Duan W, Chan SY, Boelsterli UA, Ho PC, Yang H, Bian JS, Huang M, Zhu YZ, Xiong W, Li X, Zhou S. 2005. Human multidrug resistance associated protein 4 confers resistance to camptothecins. Pharm Res 22:1837-1853.
37. Van Aubel RA, Smeets PH, Peters JG, Bindels RJ, Russel FG. 2002. The MRP4/ABCC4 gene encodes a novel apical organic anion transporter in human kidney proximal tubules: putative efflux pump for urinary cAMP and cGMP. J Am Soc Nephrol 13:595-603.
38. Van Aubel RA, Smeets PH, van den Heuvel JJ, Russel FG. 2005. Human organic anion transporter MRP4 (ABCC4) is an efflux pump for the purine end metabolite urate with multiple allosteric substrate binding sites. Am J Physiol Renal Physiol 288:327-333.
39. Wagner CA, Friedrich B, Setiawan I, Lang F, Broer S. 2000. The use of Xenopus laevis oocytes for the functional characterization of heterologously expressed membrane proteins. Cell Physiol Biochem 10:1-12.
40. Wang HC, Beer B, Sassano D, Blume AJ, Ziai MR. 1991. Gene expression in Xenopus oocyte. J Biochem 23:271-276.
41. Wielinga PR, Reid G, Challa EE, van der Heijden I, van Deemter L, de Haas M, Mol C, Kuil AJ, Groeneveld E, Schuetz JD, Brouwer C, De Abreu RA, Wijnholds J, Beijnen JH, Borst P. 2002. Thiopurine metabolism and identification of the thiopurine metabolites transported by MRP4 and MRP5 overexpressed in human embryonic kidney cells. Mol Pharmacol 62:1321-1331.
42. Zelcer N, Reid G, Wielinga P, Kuil A, van der Heijden I, Schuetz JD, Borst P. 2003. Steroid and bile acid conjugates are substrates of human multidrug-resistance protein MRP 4 ABC C4. Biochem J 371:361-367.