Ribonucleotide reductase subunit M1 assessed by quantitative double-fluorescence immunohistochemistry predicts the efficacy of gemcitabine in biliary tract carcinoma

International Journal of Oncology

Volumn 37, Issue 4, 2010, Pages 845-852

  Nakamura, Jun ^a   Kohya, Naohiko ^a   Kai, Keita ^a   Ohtaka, Kazuma ^a   Hashiguchi, Kazuyoshi ^a   Hiraki, Masatsugu ^a   Kitajima, Yoshihiko ^a   Tokunaga, Osamu ^a   Noshiro, Hirokazu ^a   Miyazaki, Kohji ^a  

^a SAGA UNIVERSITY   (Japan)

Author keywords

Biliary tract carcinoma; Chemoresistance; Gemcitabine; Quantitative double fluorescence immunohistochemistry; Ribonucleotide reductase subunit M1

Indexed keywords

BETA ACTIN; BIOLOGICAL MARKER; DEOXYCYTIDINE KINASE; EQUILIBRATIVE NUCLEOSIDE TRANSPORTER 1; GEMCITABINE; RIBONUCLEOTIDE REDUCTASE; RIBONUCLEOTIDE REDUCTASE SUBUNIT 1; RIBONUCLEOTIDE REDUCTASE SUBUNIT 2; UNCLASSIFIED DRUG;

ADULT; AGED; ARTICLE; BILE DUCT CARCINOMA; CANCER CELL CULTURE; CANCER SURVIVAL; CLINICAL ARTICLE; CONTROLLED STUDY; DRUG EFFICACY; DRUG METABOLISM; DRUG RESISTANCE; DRUG SENSITIVITY; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IC 50; IMMUNOHISTOCHEMISTRY; MALE; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; QUANTITATIVE DOUBLE FLUORESCENCE IMMUNOHISTOCHEMISTRY;

AGED; ANTIMETABOLITES, ANTINEOPLASTIC; BILIARY TRACT NEOPLASMS; BLOTTING, WESTERN; CARCINOMA; CELL LINE, TUMOR; CELL PROLIFERATION; DEOXYCYTIDINE; DEOXYCYTIDINE KINASE; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG RESISTANCE, NEOPLASM; EQUILIBRATIVE NUCLEOSIDE TRANSPORTER 1; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; INHIBITORY CONCENTRATION 50; JAPAN; KAPLAN-MEIER ESTIMATE; MALE; MIDDLE AGED; PATIENT SELECTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RIBONUCLEOSIDE DIPHOSPHATE REDUCTASE; RNA, MESSENGER; TREATMENT OUTCOME; TUMOR MARKERS, BIOLOGICAL; TUMOR SUPPRESSOR PROTEINS;

EID: 77956506292     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo_00000735     Document Type: Article

References (55)

1. Ministry of Health, Labour and Welfare. Statistics and Information Department, Minister's Secretariat, Ministry of Health, Labour and Welfare: Vital Statistics in Japan, 2000 (in Japanese).
2. Pichlmayr R, Lamesch P, Weimann A, Tusch G and Ringe B: Surgical treatment of cholangiocellular carcinoma. World J Surg 19: 83-88, 1995.
3. Valverde A, Bonhomme N, Farges O, Sauvanet A, Flejou JF and Belghiti J: Resection of intrahepatic cholangiocarcinoma: a Western experience. J Hepatobiliary Pancreat Surg 6: 122-127, 1999.
4. de Groen PC, Gores GJ, LaRusso NF, Gunderson LL and Nagorney DM: Biliary tract cancers. N Engl J Med 341: 1368-1378, 1999.
5. Glimelius B, Hoffman K, Sjödén PO, Jacobsson G, Sellström H, Enander LK, Linné T and Svensson C: Chemotherapy improves survival and quality of life in advanced pancreatic and biliary cancer. Ann Oncol 7: 593-600, 1996.
6. Gebbia V, Giuliani F, Maiello E, Colucci G, Verderame F, Borsellino N, Mauceri G, Caruso M, Tirrito ML and Valdesi M: Treatment of inoperable and/or metastatic biliary tree carcinomas with single-agent gemcitabine or in combination with levofolinic acid and infusional fluorouracil: results of a multicenter phase II study. J Clin Oncol 19: 4089-4091, 2001.
7. Penz M, Kornek GV, Raderer M, Ulrich-Pur H, Fiebiger W, Lenauer A, Depisch D, Krauss G, Schneeweiss B and Scheithauer W: Phase II trial of two-weekly gemcitabine in patients with advanced biliary tract cancer. Ann Oncol 12: 183-186, 2001.
8. Park JS, Oh SY, Kim SH, Kwon HC, Kim JS, Jin-Kim H and Kim YH: Single-agent gemcitabine in the treatment of advanced biliary tract cancers: a phase II study. Jpn J Clin Oncol 35: 68-73, 2005. (Pubitemid 40567871)
9. Okusaka T, Ishii H, Funakoshi A, Yamao K, Ohkawa S, Saito S, Saito H and Tsuyuguchi T: Phase II study of single-agent gemcitabine in patients with advanced biliary tract cancer. Cancer Chemother Pharmacol 57: 647-653, 2006.
10. Valle JW, Wasan H, Johnson P, Jones E, Dixon L, Swindell R, Baka S, Maraveyas A, Corrie P, Falk S, Gollins S, Lofts F, Evans L, Meyer T, Anthoney A, Iveson T, Highley M, Osborne R and Bridgewater J: Gemcitabine alone or in combination with cisplatin in patients with advanced or metastatic cholangiocarcinomas or other biliary tract tumours: a multicentre randomised phase II study - The UK ABC-01 Study. Br J Cancer 101: 621-627, 2009.
11. Patt YZ, Hassan MM, Aguayo A, Nooka AK, Lozano RD, Curley SA, Vauthey JN, Ellis LM, Schnirer II, Wolff RA, Charnsangavej C and Brown TD: Oral capecitabine for the treatment of hepatocellular carcinoma, cholangiocarcinoma, and gallbladder carcinoma. Cancer 101: 578-586, 2004.
12. Androulakis N, Aravantinos G, Syrigos K, Polyzos A, Ziras N, Tselepatiotis E, Samonis G, Kentepozidis N, Giassas S, Vamvakas L and Georgoulias V: Oxaliplatin as first-line treatment in inoperable biliary tract carcinoma: a multicenter phase II study. Oncology 70: 280-284, 2006.
13. Ueno H, Okusaka T, Ikeda M, Takezako Y and Morizane C: Phase II study of S-1 in patients with advanced biliary tract cancer. Br J Cancer 91: 1769-1774, 2004.
14. Furuse J, Okusaka T, Boku N, Ohkawa S, Sawaki A, Masumoto T and Funakoshi A: S-1 monotherapy as first-line treatment in patients with advanced biliary tract cancer: a multicenter phase II study. Cancer Chemother Pharmacol 62: 849-855, 2008.
15. Knox JJ, Hedley D, Oza A, Feld R, Siu LL, Chen E, Nematollahi M, Pond GR, Zhang J and Moore MJ: Combining gemcitabine and capecitabine in patients with advanced biliary cancer: a phase II trial. J Clin Oncol 23: 2332-2338, 2005.
16. Riechelmann RP, Townsley CA, Chin SN, Pond GR and Knox JJ: Expanded phase II trial of gemcitabine and capecitabine for advanced biliary cancer. Cancer 110: 1307-1312, 2007. (Pubitemid 47435603)
17. Koeberle D, Saletti P, Borner M, Gerber D, Dietrich D, Caspar CB, Mingrone W, Beretta K, Strasser F, Ruhstaller T, Mora O and Herrmann R; Swiss Group for Clinical Cancer Research: Patient-reported outcomes of patients with advanced biliary tract cancers receiving gemcitabine plus capecitabine: a multicenter, phase II trial of the Swiss Group for Clinical Cancer Research. J Clin Oncol 26: 3702-3708, 2008.
18. André T, Tournigand C, Rosmorduc O, Provent S, Maindrault-Goebel F, Avenin D, Selle F, Paye F, Hannoun L, Houry S, Gayet B, Lotz JP, de Gramont A and Louvet C; GERCOR Group: Gemcitabine combined with oxaliplatin (GEMOX) in advanced biliary tract adenocarcinoma: a GERCOR study. Ann Oncol 15: 1339-1343, 2004.
19. Harder J, Riecken B, Kummer O, Lohrmann C, Otto F, Usadel H, Geissler M, Opitz O and Henss H: Outpatient chemotherapy with gemcitabine and oxaliplatin in patients with biliary tract cancer. Br J Cancer 95: 848-852, 2006.
20. Wagner AD, Buechner-Steudel P, Moehler M, Schmalenberg H, Behrens R, Fahlke J, Wein A, Behl S, Kuss O, Kleber G and Fleig WE: Gemcitabine, oxaliplatin and 5-FU in advanced bile duct and gallbladder carcinoma: two parallel, multicentre phase-II trials. Br J Cancer 101: 1846-1852, 2009.
21. Nehls O, Oettle H, Hartmann JT, Hofheinz RD, Hass HG, Horger MS, Koppenhöfer U, Hochhaus A, Stieler J, Trojan J, Gregor M and Klump B: Capecitabine plus oxaliplatin as first-line treatment in patients with advanced biliary system adenocarcinoma: a prospective multicentre phase II trial. Br J Cancer 98: 309-315, 2008.
22. Park SH, Park YH, Lee JN, Bang SM, Cho EK, Shin DB and Lee JH: Phase II study of epirubicin, cisplatin, and capecitabine for advanced biliary tract adenocarcinoma. Cancer 106: 361-365, 2006. (Pubitemid 43100445)
23. Kim YJ, Im SA, Kim HG, Oh SY, Lee KW, Choi IS, Oh DY, Lee SH, Kim JH, Kim DW, Kim TY, Kim SW, Heo DS, Yoon YB and Bang YJ: A phase II trial of S-1 and cisplatin in patients with metastatic or relapsed biliary tract cancer. Ann Oncol 19: 99-103, 2008.
24. Sasaki T, Isayama H, Nakai Y, Ito Y, Kogure H, Togawa O, Toda N, Yasuda I, Hasebe O, Maetani I, Sasahira N, Hirano K, Tsujino T, Tada M and Omata M: Multicenter, phase II study of gemcitabine and S-1 combination chemotherapy in patients with advanced biliary tract cancer. Cancer Chemother Pharmacol 65: 1101-1107, 2010.
25. Kaye SB: Gemcitabine: current status of phase I and II trials. J Clin Oncol 12: 1527-1531, 1994.
26. Galmarini CM, Mackey JR and Dumontet C: Nucleoside analogues and nucleobases in cancer treatment. Lancet Oncol 3: 415-424, 2002.
27. Schiller JH, Harrington D, Belani CP, Langer C, Sandler A, Krook J, Zhu J and Johnson DH; Eastern Cooperative Oncology Group: Comparison of four chemotherapy regimens for advanced non-small-cell lung cancer. N Engl J Med 346: 92-98, 2002.
28. Burris HA III, Moore MJ, Andersen J, Green MR, Rothenberg ML, Modiano MR, Cripps MC, Portenoy RK, Storniolo AM, Tarassoff P, Nelson R, Dorr FA, Stephens CD and Von Hoff DD: 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, 1997.
29. Albain KS, Nag SM, Calderillo-Ruiz G, Jordaan JP, Llombart AC, Pluzanska A, Rolski J, Melemed AS, Reyes-Vidal JM, Sekhon JS, Simms L and O'Shaughnessy J: Gemcitabine plus Paclitaxel versus Paclitaxel monotherapy in patients with metastatic breast cancer and prior anthracycline treatment. J Clin Oncol 26: 3950-3957, 2008.
30. Damaraju VL, Damaraju S, Young JD, Baldwin SA, Mackey J, Sawyer MB and Cass CE: Nucleoside anticancer drugs: the role of nucleoside transporters in resistance to cancer chemotherapy. Oncogene 22: 7524-7536, 2003.
31. Bergman AM, Pinedo HM and Peters GJ: Determinants of resistance to 2′,2′-difluorodeoxycytidine (gemcitabine). Drug Resist Updat 5: 19-33, 2002.
32. Huang P, Chubb S, Hertel LW, Grindey GB and Plunkett W: Action of 2′,2′-difluorodeoxycytidine on DNA synthesis. Cancer Res 51: 6110-6117, 1991.
33. Heinemann V, Schulz L, Issels RD and Plunkett W: Gemcitabine: a modulator of intracellular nucleotide and deoxynucleotide metabolism. Semin Oncol 22 (Suppl 11): 11-18, 1995.
34. Heinemann V, Xu YZ, Chubb S, Sen A, Hertel LW, Grindey GB and Plunkett W: Inhibition of ribonucleotide reduction in CCRF-CEM cells by 2′,2′-difluorodeoxycytidine. Mol Pharmacol 38: 567-572, 1990.
35. Bergman AM, Pinedo HM, Jongsma AP, Brouwer M, Ruiz van Haperen VW, Veerman G, Leyva A, Eriksson S and Peters GJ: Decreased resistance to gemcitabine (2′,2′-difluorodeoxycitidine) of cytosine arabinoside-resistant myeloblastic murine and rat leukemia cell lines: role of altered activity and substrate specificity of deoxycytidine kinase. Biochem Pharmacol 57: 397-406, 1999.
36. Mackey JR, Mani RS, Selner M, Mowles D, Young JD, Belt JA, Crawford CR and Cass CE: Functional nucleoside transporters are required for gemcitabine influx and manifestation of toxicity in cancer cell lines. Cancer Res 58: 4349-4357, 1998.
37. Achiwa H, Oguri T, Sato S, Maeda H, Niimi T and Ueda R: Determinants of sensitivity and resistance to gemcitabine: the roles of human equilibrative nucleoside transporter 1 and deoxycytidine kinase in non-small cell lung cancer. Cancer Sci 95: 753-757, 2004.
38. Spratlin J, Sangha R, Glubrecht D, Dabbagh L, Young JD, Dumontet C, Cass C, Lai R and Mackey JR: 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, 2004.
39. Johansson M, Brismar S and Karlsson A: Human deoxycytidine kinase is located in the cell nucleus. Proc Natl Acad Sci USA 94: 11941-11945, 1997.
40. Sabini E, Ort S, Monnerjahn C, Konrad M and Lavie A: Structure of human dCK suggests strategies to improve anticancer and antiviral therapy. Nat Struct Biol 10: 513-519, 2003. (Pubitemid 36792901)
41. Kroep JR, Loves WJ, van der Wilt CL, Alvarez E, Talianidis I, Boven E, Braakhuis BJ, van Groeningen CJ, Pinedo HM and Peters GJ: Pretreatment deoxycytidine kinase levels predict in vivo gemcitabine sensitivity. Mol Cancer Ther 1: 371-376, 2002.
42. Ruiz van Haperen VW, Veerman G, Eriksson S, Boven E, Stegmann AP, Hermsen M, Vermorken JB, Pinedo HM and Peters GJ: Development and molecular characterization of a 2′,2′-difluorodeoxycytidine-resistant variant of the human ovarian carcinoma cell line A2780. Cancer Res 54: 4138-4143, 1994.
43. Cory JG and Sato A: Regulation of ribonucleotide reductase activity in mammalian cells. Mol Cell Biochem 53-4: 257-266, 1983.
44. Goan YG, Zhou B, Hu E, Mi S and Yen Y: Overexpression of ribonucleotide reductase as a mechanism of resistance to 2,2-difluorodeoxycytidine in the human KB cancer cell line. Cancer Res 59: 4204-4207, 1999.
45. Davidson JD, Ma L, Flagella M, Geeganage S, Gelbert LM and Slapak CA: An increase in the expression of ribonucleotide reductase large subunit 1 is associated with gemcitabine resistance in non-small cell lung cancer cell lines. Cancer Res 64: 3761-3776, 2004.
46. Kai K, Kitajima Y, Hiraki M, Satoh S, Tanaka M, Nakafusa Y, Tokunaga O and Miyazaki K: Quantitative double-fluorescence immunohistochemistry (qDFIHC), a novel technology to assess protein expression: a pilot study analyzing 5-FU sensitive markers thymidylate synthase, dihydropyrimidine dehydrogenase and orotate phosphoribosyl transferases in gastric cancer tissue specimens. Cancer Lett 258: 45-54, 2007.
47. Jiao W, Yakushiji H, Kitajima Y, Ogawa A and Miyazaki K: Establishment and characterization of human hilar bile duct carcinoma cell line and cell strain. J Hepatobiliary Pancreat Surg 7: 417-425, 2000.
48. Ohtaka K, Kohya N, Sato K, Kitajima Y, Ide T, Mitsuno M and Miyazaki K: Ribonucleotide reductase subunit M1 is a possible chemoresistance marker to gemcitabine in biliary tract carcinoma. Oncol Rep 20: 279-286, 2008.
49. Oguri T, Achiwa H, Sato S, Bessho Y, Takano Y, Miyazaki M, Muramatsu H, Maeda H, Niimi T and Ueda R: 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, 2006.
50. Duxbury MS, Ito H, Zinner MJ, Ashley SW and Whang EE: Inhibition of SRC tyrosine kinase impairs inherent and acquired gemcitabine resistance in human pancreatic adenocarcinoma cells. Clin Cancer Res 10: 2307-2318, 2004.
51. Akada M, Crnogorac-Jurcevic T, Lattimore S, Mahon P, Lopes R, Sunamura M, Matsuno S and Lemoine NR: Intrinsic chemoresistance to gemcitabine is associated with decreased expression of BNIP3 in pancreatic cancer. Clin Cancer Res 11: 3094-3101, 2005.
52. Duxbury MS, Ito H, Benoit E, Zinner MJ, Ashley SW and Whang EE: RNA interference targeting focal adhesion kinase enhances pancreatic adenocarcinoma gemcitabine chemosensitivity. Biochem Biophys Res Commun 311: 786-792, 2003. (Pubitemid 37377726)
53. Rosell R, Felip E, Taron M, Majo J, Mendez P, Sanchez-Ronco M, Queralt C, Sanchez JJ and Maestre J: Gene expression as a predictive marker of outcome in stage IIB-IIIA-IIIB non-small cell lung cancer after induction gemcitabine-based chemotherapy followed by resectional surgery. Clin Cancer Res 10: S4215-S4219, 2004.
54. García-Manteiga J, Molina-Arcas M, Casado FJ, Mazo A and Pastor-Anglada M: Nucleoside transporter profiles in human pancreatic cancer cells: role of hCNT1 in 2′,2′-difluorodeoxycytidine- induced cytotoxicity. Clin Cancer Res 9: 5000-5008, 2003.
55. Nakano Y, Tanno S, Koizumi K, Nishikawa T, Nakamura K, Minoguchi M, Izawa T, Mizukami Y, Okumura T and Kohgo Y: Gemcitabine chemoresistance and molecular markers associated with gemcitabine transport and metabolism in human pancreatic cancer cells. Br J Cancer 96: 457-463, 2007.