Interdependence of gemcitabine treatment, transporter expression, and resistance in human pancreatic carcinoma cells

Neoplasia

Volumn 12, Issue 9, 2010, Pages 740-747

  Hagmann, Wolfgang ^a   Jesnowski, Ralf ^a   Löhr, Johannes Matthias ^a,b  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

EQUILIBRATIVE NUCLEOSIDE TRANSPORTER 1; FLUOROURACIL; GEMCITABINE; MESSENGER RNA; MULTIDRUG RESISTANCE PROTEIN 1; MULTIDRUG RESISTANCE PROTEIN 3; MULTIDRUG RESISTANCE PROTEIN 5;

ARTICLE; CANCER CELL CULTURE; CELL PROLIFERATION; CHEMOSENSITIVITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOTOXICITY; DRUG TRANSPORT; DRUG UPTAKE; EMBRYO; GENE OVEREXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNOBLOTTING; NUCLEOTIDE SEQUENCE; PANCREAS CARCINOMA; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION;

EID: 77956868652     PISSN: 15228002     EISSN: 14765586     Source Type: Journal    
DOI: 10.1593/neo.10576     Document Type: Article

References (60)

1. Jemal A, Siegel R, Ward E, Hao Y, Xu J, and Thun MJ (2009). Cancer statistics. CA Cancer J Clin 59, 225-249.
2. Löhr M (2006). Is it possible to survive pancreatic cancer? Nat Clin Pract 3, 236-237.
3. Burris HA III, Moore MJ, Andersen J, Green MR, Rothenberg ML, Modiano MR, Cripps MC, Portenoy RK, Storniolo AM, Tarassoff P, et al. (1997). Improvements in survival and clinical benefit with gemcitabine as first-line therapy for patients with advanced pancreas cancer: a randomized trial. J Clin Oncol 15, 2403-2413.
4. O'Reilly EM and Abou-Alfa GK (2007). Cytotoxic therapy for advanced pancreatic adenocarcinoma. Semin Oncol 34, 347-353.
5. O'Reilly EM (2009). Pancreatic adenocarcinoma: new strategies for success. Gastrointest Cancer Res 3, S11-S15.
6. Nakano Y, Tanno S, Koizumi K, Nishikawa T, Nakamura K, Minoguchi M, Izawa T, Mizukami Y, Okumura T, and Kohgo Y (2007). Gemcitabine chemoresistance and molecular markers associated with gemcitabine transport and metabolism in human pancreatic cancer cells. Br J Cancer 96, 457-463.
7. Liau SS and Whang E (2008). HMGA1 is a molecular determinant of chemoresistance to gemcitabine in pancreatic adenocarcinoma. Clin Cancer Res 14, 1470-1477.
8. Liu WS, Yan HJ, Qin RY, Tian R, Wang M, Jiang JX, Shen M, and Shi CJ (2009). siRNA directed against survivin enhances pancreatic cancer cell gemcitabine chemosensitivity. Dig Dis Sci 54, 89-96.
9. Guillermet-Guibert J, Davenne L, Pchejetski D, Saint-Laurent N, Brizuela L, Guilbeau-Frugier C, Delisle MB, Cuvillier O, Susini C, and Bousquet C (2009). Targeting the sphingolipid metabolism to defeat pancreatic cancer cell resistance to the chemotherapeutic gemcitabine drug. Mol Cancer Ther 8, 809-820.
10. Andersson R, Aho U, Nilsson BI, Peters GJ, Pastor-Anglada M, Rasch W, and Sandvold ML (2009). Gemcitabine chemoresistance in pancreatic cancer: molecular mechanisms and potential solutions. Scand J Gastroenterol 44, 782-786.
11. Park JK, Lee EJ, Esau C, and Schmittgen TD (2009). Antisense inhibition of microRNA-21 or -221 arrests cell cycle, induces apoptosis, and sensitizes the effects of gemcitabine in pancreatic adenocarcinoma. Pancreas 38, e190-e199.
12. Logan-Collins J, Thomas RM, Yu P, Jaquish D, Mose E, French R, Stuart W, McClaine R, Aronow B, Hoffman RM, et al. (2010). Silencing of RON receptor signaling promotes apoptosis and gemcitabine sensitivity in pancreatic cancers. Cancer Res 70, 1130-1140.
13. Zhang J, Visser F, King KM, Baldwin SA, Young JD, and Cass CE (2007). The role of nucleoside transporters in cancer chemotherapy with nucleoside drugs. Cancer Metastasis Rev 26, 85-110.
14. Mackey JR, Mani RS, Selner M, Mowles D, Young J D, Belt J A, Crawford C R, and Cass C E (1998). Functional nucleoside transporters are required for gemcitabine influx and manifestation of toxicity in cancer cell lines. Cancer Res 58, 4349-4357.
15. +-nucleoside cotransporter proteins (hCNT3 and mCNT3) broadly selective for purine and pyrimidine nucleosides (system cib). J Biol Chem 276, 2914-2927.
16. Mackey JR, Yao SY, Smith KM, Karpinski E, Baldwin SA, Cass CE, and Young JD (1999). Gemcitabine transport in xenopus oocytes expressing recombinant plasma membrane mammalian nucleoside transporters. J Natl Cancer Inst 91,1876-1881.
17. Garcia-Manteiga J, Molina-Arcas M, Casado FJ, Mazo A, and Pastor-Anglada M (2003). Nucleoside transporter profiles in human pancreatic cancer cells: role of hCNT1 in 2′,2′-difluorodeoxycytidine-induced cytotoxicity. Clin Cancer Res 9, 5000-5008.
18. Rauchwerger DR, Firby PS, Hedley DW, and Moore MJ (2000). Equilibrativesensitive nucleoside transporter and its role in gemcitabine sensitivity. Cancer Res 60, 6075-6079.
19. Paproski RJ, Young JD, and Cass CE (2010). Predicting gemcitabine transport and toxicity in human pancreatic cancer cell lines with the positron emission tomography tracer 3′-deoxy-3′-fluorothymidine. Biochem Pharmacol 79, 587-595.
20. Davidson JD, Ma L, Iverson PW, Lesoon A, Jin S, Horwitz L, Gallery M, and Slapak CA (2002). Human multi-drug resistance protein 5 (MRP5) confers resistance to gemcitabine. Proc Am Assoc Cancer Res 43, 3868.
21. Kiuchi Y, Suzuki H, Hirohashi T, Tyson CA, and Sugiyama Y (1998). cDNA cloning and inducible expression of human multidrug resistance associated protein 3 (MRP3). FEBS Lett 433, 149-152.
22. König J, Rost D, Cui Y, and Keppler D (1999). Characterization of the human multidrug resistance protein isoform MRP3 localized to the basolateral hepatocyte membrane. Hepatology 29, 1156-1163.
23. Kool M, van der Linden M, de Haas M, Scheffer GL, de Vree JM, Smith AJ, Jansen G, Peters GJ, Ponne N, Scheper RJ, et al. (1999). MRP3, an organic anion transporter able to transport anti-cancer drugs. Proc Natl Acad Sci USA 96, 6914-6919.
24. Scheffer GL, Kool M, de Haas M, de Vree JM, Pijnenborg AC, Bosman DK, Elferink RP, van der Valk P, Borst P, and Scheper RJ (2002). Tissue distribution and induction of human multidrug resistant protein 3. Lab Invest 82, 193-201.
25. König J, Hartel M, Nies AT, Martignoni ME, Guo J, Büchler MW, Friess H, and Keppler D (2005). Expression and localization of human multidrug resistance protein (ABCC) family members in pancreatic carcinoma. Int J Cancer 115, 359-367.
26. Hagmann W, Jesnowski R, Faissner R, Guo C, and Löhr J M (2009). ATP-binding cassette C transporters in human pancreatic carcinoma cell lines. Upregulation in 5-fluorouracil-resistant cells. Pancreatology 9, 136-144.
27. Zelcer N, Saeki T, Reid G, Beijnen JH, and Borst P (2001). Characterization of drug transport by the human multidrug resistance protein 3 (ABCC3). J Biol Chem 276, 46400-46407.
28. Pratt S, Shepard RL, Kandasamy RA, Johnston PA, Perry W III, and Dantzig AH (2005). The multidrug resistance protein 5 (ABCC5) confers resistance to 5-fluorouracil and transports its monophosphorylated metabolites. Mol Cancer Ther 4, 855-863.
29. Oguri T, Achiwa H, Sato S, Bessho Y, Takano Y, Miyazaki M, Muramatsu H, Maeda H, Niimi T, and Ueda R (2006). The determinants of sensitivity and acquired resistance to gemcitabine differ in non-small cell lung cancer: a role of ABCC5 in gemcitabine sensitivity. Mol Cancer Ther 5, 1800-1806.
30. Spratlin J, Sangha R, Glubrecht D, Dabbagh L, Young JD, Dumontet C, Cass C, Lai R, and Mackey JR (2004). The absence of human equilibrative nucleoside transporter 1 is associated with reduced survival in patients with gemcitabine-treated pancreas adenocarcinoma. Clin Cancer Res 10, 6956-6961.
31. Giovannetti E, Del Tacca M, Mey V, Funel N, Nannizzi S, Ricci S, Orlandini C, Boggi U, Campani D, Del Chiaro M, et al. (2006). Transcription analysis of human equilibrative nucleoside transporter-1 predicts survival in pancreas cancer patients treated with gemcitabine. Cancer Res 66, 3928-3935.
32. Farrell JJ, Elsaleh H, Garcia M, Lai R, Ammar A, Regine WF, Abrams R, Benson AB, Macdonald J, Cass CE, et al. (2009). Human equilibrative nucleoside transporter 1 levels predict response to gemcitabine in patients with pancreatic cancer. Gastroenterology 136, 187-195.
33. Marechal R, Mackey JR, Lai R, Demetter P, Peeters M, Polus M, Cass CE, Young J, Salmon I, Deviere J, et al. (2009). Human equilibrative nucleoside transporter 1 and human concentrative nucleoside transporter 3 predict survival after adjuvant gemcitabine therapy in resected pancreatic adenocarcinoma. Clin Cancer Res 15, 2913-2919.
34. Hong SP, Wen J, Bang S, Park S, and Song SY (2009). CD44-positive cells are responsible for gemcitabine resistance in pancreatic cancer cells. Int J Cancer 125, 2323-2331.
35. Haraguchi N, Utsunomiya T, Inoue H, Tanaka F, Mimori K, Barnard GF, and Mori M(2006). Characterization of a side population of cancer cells from human gastrointestinal system. Stem Cells 24, 506-513.
36. Löhr M, Schmidt C, Ringel J, Kluth M, Müller P, Nizze H, and Jesnowski R (2001). Transforming growth factor-beta1 induces desmoplasia in an experimental model of human pancreatic carcinoma. Cancer Res 61, 550-555.
37. Jedlitschky G, Burchell B, and Keppler D (2000). The multidrug resistance protein 5 functions as an ATP-dependent export pump for cyclic nucleotides. J Biol Chem 275, 30069-30074.
38. Hagmann W, Nies AT, König J, Frey M, Zentgraf H, and Keppler D (1999). Purification of the human apical conjugate export pump MRP2. Reconstitution and functional characterization as substrate-stimulated ATPase. Eur J Biochem 265, 281-289.
39. Bradford MM (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72, 248-254.
40. Grunewald R, Abbruzzese JL, Tarassoff P, and Plunkett W (1991). Saturation of 2′,2′-difluorodeoxycytidine 5′-triphosphate accumulation by mononuclear cells during a phase I trial of gemcitabine. Cancer Chemother Pharmacol 27, 258-262.
41. Shi X, Liu S, Kleeff J, Friess H, and Büchler MW (2002). Acquired resistance of pancreatic cancer cells towards 5-Fluorouracil and gemcitabine is associated with altered expression of apoptosis-regulating genes. Oncology 62, 354-362.
42. Duxbury MS, Ito H, Zinner MJ, Ashley SW, and Whang EE (2004). Inhibition of SRC tyrosine kinase impairs inherent and acquired gemcitabine resistance in human pancreatic adenocarcinoma cells. Clin Cancer Res 10, 2307-2318.
43. Giovannetti E, Mey V, Danesi R, Mosca I, and Del Tacca M (2004). Synergistic cytotoxicity and pharmacogenetics of gemcitabine and pemetrexed combination in pancreatic cancer cell lines. Clin Cancer Res 10, 2936-2943.
44. Mori R, Ishikawa T, Ichikawa Y, Taniguchi K, Matsuyama R, Ueda M, Fujii Y, Endo I, Togo S, Danenberg PV, et al. (2007). Human equilibrative nucleoside transporter 1 is associated with the chemosensitivity of gemcitabine in human pancreatic adenocarcinoma and biliary tract carcinoma cells. Oncol Rep 17, 1201-1205.
45. Tsujie M, Nakamori S, Nakahira S, Takeda S, Takahashi Y, Hayashi N, Okami J, Nagano H, Dono K, Umeshita K, et al. (2006). Schedule-dependent therapeutic effects of gemcitabine combined with uracil-tegafur in a human pancreatic cancer xenograft model. Pancreas 33, 142-147.
46. Carmichael J, Fink U, Russell RC, Spittle MF, Harris AL, Spiessi G, and Blatter J (1996). Phase II study of gemcitabine in patients with advanced pancreatic cancer. Br J Cancer 73, 101-105.
47. Li D, Xie K, Wolff R, and Abbruzzese JL (2004). Pancreatic cancer. Lancet 363, 1049-1057.
48. El-Rayes BF and Philip PA (2002). Systemic therapy for advanced pancreatic cancer. Expert Rev Anticancer Ther 2, 426-436.
49. Kulke MH (2003). Advanced pancreatic cancer: is there a role for combination therapy? Expert Rev Anticancer Ther 3, 729-739.
50. Heinemann V, Boeck S, Hinke A, Labianca R, and Louvet C (2008). Metaanalysis of randomized trials: evaluation of benefit from gemcitabine-based combination chemotherapy applied in advanced pancreatic cancer. BMC Cancer 8, 82.
51. Pressacco J, Wiley JS, Jamieson GP, Erlichman C, and Hedley DW (1995). Modulation of the equilibrative nucleoside transporter by inhibitors of DNA synthesis. Br J Cancer 72, 939-942.
52. Pratt S, Chen V, Perry WI III, Starling JJ, and Dantzig AH (2006). Kinetic validation of the use of carboxydichlorofluorescein as a drug surrogate for MRP5-mediated transport. Eur J Pharm Sci 27, 524-532.
53. Perez-Torras S, Garcia-Manteiga J, Mercade E, Casado FJ, Carbo N, Pastor- Anglada M, and Mazo A (2008). Adenoviral-mediated overexpression of human equilibrative nucleoside transporter 1 (hENT1) enhances gemcitabine response in human pancreatic cancer. Biochem Pharmacol 76, 322-329.
54. Kantharidis P, El-Osta A, de Silva M, Wall DM, Hu XF, Slater A, Nadalin G, Parkin JD, and Zalcberg JR (1997). Altered methylation of the human MDR1 promoter is associated with acquired multidrug resistance. Clin Cancer Res 3, 2025-2032.
55. Hauswald S, Duque-Afonso J, Wagner M M, Schertl FM, Lubbert M, Peschel C, Keller U, and Licht T (2009). Histone deacetylase inhibitors induce a very broad, pleiotropic anticancer drug resistance phenotype in acute myeloid leukemia cells by modulation of multiple ABC transporter genes. Clin Cancer Res 15, 3705-3715.
56. König J, Nies AT, Cui Y, Leier I, and Keppler D (1999). Conjugate export pumps of the multidrug resistance protein (MRP) family: localization, substrate specificity, and MRP2-mediated drug resistance. Biochim Biophys Acta 1461, 377-394.
57. Borst P, de Wolf C, and van de Wetering K (2007).Multidrug resistance-associated proteins 3, 4, and 5. Pflügers Arch 453, 661-673.
58. Cui Y, König J, Buchholz JK, Spring H, Leier I, and Keppler D (1999). Drug resistance and ATP-dependent conjugate transport mediated by the apical multidrug resistance protein, MRP2, permanently expressed in human and canine cells. Mol Pharmacol 55, 929-937.
59. Reid G, Wielinga P, Zelcer N, De Haas M, Van Deemter L,Wijnholds J, Balzarini J, and 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.
60. Pan X, Arumugam T, Yamamoto T, Levin PA, Ramachandran V, Ji B, Lopez-Berestein G, Vivas-Mejia PE, Sood AK, McConkey DJ, et al. (2008). Nuclear factor-kappaB p65/relA silencing induces apoptosis and increases gemcitabine effectiveness in a subset of pancreatic cancer cells. Clin Cancer Res 14, 8143-8151.