Combination of dasatinib and gemcitabine reduces the ALDH1A1 expression and the proliferation of gemcitabine-resistant pancreatic cancer MIA PaCa-2 cells

International Journal of Oncology

Volumn 45, Issue 6, 2014, Pages 2132-2138

  Duong, Hong Quan ^a,b   Yi, Yong Weon ^a,c   Kang, Hyo Jin ^c   Bae, Insoo ^a,c,d   Jang, Young Joo ^a   Kwak, Sahng June ^a   Seong, Yeon Sun ^a  

^a Dankook University   (South Korea)

^b DUY TAN UNIVERSITY   (Viet Nam)

^c GEORGETOWN UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d GEORGETOWN UNIVERSITY   (United States)

Author keywords

ALDH1A1; Dasatinib; Gemcitabine; MIA PaCa 2; Pancreatic cancer cells; Resistance

Indexed keywords

ALDEHYDE DEHYDROGENASE; ALDEHYDE DEHYDROGENASE 1A1; CASPASE 3; CASPASE 7; DASATINIB; GEMCITABINE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; SMALL INTERFERING RNA; STAT3 PROTEIN; UNCLASSIFIED DRUG; ALPHA TUBULIN; ALDH1A1 PROTEIN, HUMAN; ANTINEOPLASTIC AGENT; DEOXYCYTIDINE; PYRIMIDINE DERIVATIVE; THIAZOLE DERIVATIVE;

ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; CANCER INHIBITION; CANCER SURVIVAL; CELL DEATH; CELL PROLIFERATION; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; DRUG POTENTIATION; ENZYME ACTIVITY; HUMAN; HUMAN CELL; PANCREATIC CANCER CELL LINE; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; ANTINEOPLASTIC ACTIVITY; CELL STRAIN MIA PACA 2; DRUG EFFICACY; PANCREAS CANCER; WESTERN BLOTTING; ANALOGS AND DERIVATIVES; DRUG EFFECTS; DRUG RESISTANCE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PANCREATIC NEOPLASMS; PATHOLOGY; TUMOR CELL LINE;

ALDEHYDE DEHYDROGENASE; ANTINEOPLASTIC AGENTS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; CELL LINE, TUMOR; CELL PROLIFERATION; DEOXYCYTIDINE; DRUG RESISTANCE, NEOPLASM; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; PANCREATIC NEOPLASMS; PYRIMIDINES; THIAZOLES;

EID: 84899579623     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo.2014.2357     Document Type: Article

References (47)

1. Hidalgo M: Pancreatic cancer. N Engl J Med 362: 1605-1617, 2010.
2. Long J, Zhang Y, Yu X, Yang J, LeBrun DG, Chen C, Yao Q and Li M: Overcoming drug resistance in pancreatic cancer. Expert Opin Ther Targets 15: 817-828, 2011.
3. Duffy JP, Eibl G, Reber HA and Hines OJ: Influence of hypoxia and neoangiogenesis on the growth of pancreatic cancer. Mol Cancer 2: 12, 2003.
4. Conroy T, Desseigne F, Ychou M, Bouché O, Guimbaud R, Bécouarn Y, Adenis A, Raoul JL, Gourgou-Bourgade S, de la Fouchardière C, Bennouna J, Bachet JB, Khemissa-Akouz F, Péré-Vergé D, Delbaldo C, Assenat E, et al: FOLFINOX versus gemcitabine for metastatic pancreatic cancer. N Engl J Med 364: 1817-1825, 2011.
5. Loehrer PJ Sr, Feng Y, Cardenes H, Wagner L, Brell JM, Cella D, Flynn P, Ramanathan RK, Crane CH, Alberts SR and Benson AB III: Gemcitabine alone versus gemcitabine plus radiotherapy in patients with locally advanced pancreatic cancer: an Eastern Cooperative Oncology Group trial. J Clin Oncol 29: 4105-4112, 2011.
6. Kim MP and Gallick GE: Gemcitabine resistance in pancreatic cancer: picking the key players. Clin Cancer Res 14: 1284-1285, 2008.
7. Marcato P, Dean CA, Giacomantonio CA and Lee PWK: Aldehyde dehydrogenase: its role as a cancer stem cell marker comes down to the speficic isoform. Cell Cycle 10: 1378-1384, 2011.
8. Dylla SJ, Beviglia L, Park IK, Chartier C, Raval J, Ngan L, Pickell K, Aguilar J, Lazetic S, Smith-Berdan S, Clarke MF, Hoey T, Lewicki J and Gurney AL: Colorectal cancer stem cells are enriched in xenogeneic tumors following chemotherapy. PLoS One 18: e2428, 2008.
9. Magni M, Shammah S, Schiró R, Mellado W, Dalla-Favera R and Gianni AM: Induction of cyclophosphamide-resistance by aldehyde-dehydrogenase gene transfer. Blood 87: 1097-1103. 1998.
10. Sládek NE, Kollander R, Sreerama L and Kiang DT: Cellular levels of aldehyde dehydrogeneases (ALDH1A1 and ALDH3A1) as predictors of therapeutic responses to cyclophosphamide-based chemotherapy of breast cancer: a retrospective study. Rational individualization of oxazaphosphorine-based cancer chemotherapeutic regimens. Cancer Chemother Pharmacol 49: 309-321, 2002.
11. Charafe-Jauffret E, Ginestier C, Iovino F, Tarpin C, Diebel M, Esterni B, Houvenaeghel G, Extra JM, Bertucci F, Jacquemier J, Xerri L, Dontu G, Stassi G, Xiao Y, Barsky SH, Birnbaum D, et al: Aldehyde dehydrogenase 1-positive cancer stem cells mediate metastasis and poor clinical outcome in inflammatory breast cancer. Clin Cancer Res 16: 45-55, 2010.
12. Huang EH, Hynes MJ, Zhang T, Ginestier C, Dontu G, Appelman H, Fields JZ, Wicha MS and Boman BM: Aldehyde dehydrogenase 1 is a marker for normal and malignant human colonic stem cells (SC) and tracks SC overpopulation during colon tumorigenesis. Cancer Res 69: 3382-3389, 2009.
13. Su Y, Qui Q, Zhang Z, Jiang Z, Leng Q, Liu Z, Stass SA and Jiang F: Aldehyde dehydrogenase 1 A1-positive cell population is enriched in tumor-initiating cells and associated with progression of bladder cancer. Cancer Epidemiol Biomarkers Prev 19: 327-337, 2010.
14. Dembinski JL and Krauss S: Characterization and functional analysis of a slow cycling stem cell-like subpopulation in pancreas adenocarcinoma. Clin Exp Metastasis 26: 611-623, 2009.
15. Clay MR, Tabor M, Owen JH, Carey TE, Bradford CR, Wolf GT, Wicha MS and Prince ME: Single-marker identification of head and neck squamous cell carcinoma cancer stem cells with aldehyde dehydrogenase. Head Neck 32: 1195-1201, 2010.
16. Jiang F, Qui Q, Khanna A, Todd NW, Deepak J, Xing L, Wang H, Liu Z, Su Y, Stass SA and Katz RL: Aldehyde dehydrogenase 1 is a tumor stem cell-associated marker in lung cancer. Mol Cancer Res 7: 330-338, 2009.
17. Ma S, Chan KW, Hu L, Lee TK, Wo JY, Ng IO, Zheng BJ and Guan XY: Identification and characterization of tumorigenic live cancer stem/progenitor cells. Gastroenterology 132: 2542-2556, 2007.
18. Landen CN Jr, Goodman B, Katre AA, Steg AD, Nick AM, Stone RL, Miller LD, Mejia PV, Jennings NB, Gershenson DM, Bast RC Jr, Coleman RL, Lopez-Berestein G and Sood AK: Targeting aldehyde dehydrogenase cancer stem cells in ovarian cancer. Mol Cancer Ther 9: 3186-3199, 2010.
19. Rasheed ZA, Yang J, Wang Q, Kowalski J, Freed I, Murter C, Hong SM, Koorstra JB, Rajeshkumar NV, He X, Goggins M, Iacobuzio-Donahue C, Berman DM, Laheru D, Jimeno A, Hidalgo M, Maitra A and Matsui W: Prognostic significance of tumorigenic cells with mesenchymal features in pancreatic adenocarcinoma. J Natl Cancer Inst 102: 340-351, 2010.
20. Duong HQ, Hwang JS, Kim HJ, Kang HJ, Seong YB and Bae I: Aldehyde dehydrogenase 1A1 confers intrinsic and acquired resistance to gemcitabine in human pancreatic adenocarcinoma MIA PaCa-2 cells. Int J Oncol 41: 855-861, 2012.
21. Araujo J and Logothetis C: Dasatinib: a potent SRC inhibitor in clinical development for the treatment of solid tumors. Cancer Treat Rev 36: 492-500, 2010.
22. Kim LC, Rix U and Haura EB: Dasatinib in solid tomors. Expert Opin Investig Drugs 19: 415-425, 2010.
23. Ceppi P, Papotti M, Monica V, Lolanono M, Saviozzi S, Pautasso M, Novello S, Mussino S, Bracco E, Volante M and Scagliotti GV: Effects of Src kinase inhibition induced by dasatinib in non-small cell lung cancer cell lines treated with cisplatin. Mol Cancer Ther 8: 3066-3074, 2009.
24. Kopetz S, Lesslie DP, Dallas NA, Park SI, Johnson M, Parikh NU, Kim MP, Abbruzzese JL, Ellis LM, Chandra J and Gallick GE: Synergistic activity of the SRC family kinase inhibitor dasatinib and oxaliplatin in colon carcinoma cells is mediated by oxidative stress. Cancer Res 69: 3842-3849, 2009.
25. Nagaraj NS, Washington MK and Merchant NB: Combined blockade of Src kinase and epidermal growth factor receptor with gemcitabine overcomes STAT3-mediated resistance of inhibition of pancreatic tumor growth. Clin Cancer Res 17: 483-493, 2011.
26. Kim YJ, Hong YB, Cho CH, Seong YS and Bae I: Exploring protein kinase inhibitors: unveiling gemcitabine resistance in pancreatic cancer. Pancreas 41: 804-805, 2012.
27. Hong DS, Choe JH, Naing A, Wheler JJ, Falchook GS, Piha-Paul S, Moulder SL, George GC, Choe JM, Strauss LC, Gallick GE and Kurzrock R: A phase 1 study of gemcitabine combinated with dasatinib in patients with advanced solid tumors. Invest New Drugs 31: 918-926, 2013.
28. Park BJ, Whichard ZL and Corey SJ: Dasatinib synergizes with both cytotoxic and signal transduction inhibitors in heterogeneous breast cancer cell lines - lessons for design of combination targeted therapy. Cancer Lett 320: 104-110, 2012.
29. Somlo G, Atzori F, Strauss LC, Geese WJ, Specht JM, Gradishar WJ, Rybicki A, Sy O, Vahdal LT and Cortes J: Dasatinib plus capecitabine for advanced breast cancer: safety and efficacy in phase I study CA180004. Clin Cancer Res 19: 1884-1893, 2013.
30. Araujo JC, Mathew P, Armstrong AJ, Braud EL, Posadas E, Lonberg M, Gallick GE, Trudel GC, Paliwal P, Agrawal S and Logothetic CJ: Dasatinib combined with docetaxel for castration-resistant prostate cancer: results from a phase 1-2 study. Cancer 118: 63-71, 2012.
31. Secord AA, Teoh DK, Barry WT, Yu M, Broadwater G, Havrilesky LJ, lee PS, Berchuck A, Lancaster J and Wenham RM: A phase I trial of dasatinib, an SRC-family kinase inhibitor, in combination with paclitaxel and carboplatin in patients with advanced or recurrent ovarian cancer. Clin Cancer Res 18: 5489-5498, 2012.
32. Algazi AP, Weber JS, Andrews SC, Urbas P, Munster PN, DeConti RC, Hwang J, Sondak VK, Messina JL, McCalmont T and Daud AI: Phase I clinical trial of the Src inhibitor dasatinib with dacarbazine in metastatic melanoma. Br J Cancer 106: 85-91, 2012.
33. Breccia M, Serrao A, Salaroli A, Loglisci G, Zacheo I and Alimena G: Dasatinib combined with weekly administration of vincristine as effective therapy in sudden or resistant Ph+ lymphoid blast crisis of chronic myeloid leukaemia. Br J Haematol 159: 612-613, 2012.
34. Kurebayashi J, Kanomata N, Moriya T, Kozuka Y, Watanabe M and Sonoo H: Preferential antitumor effect of the Src inhibitor dasatinib associated with a decreased proportion of aldehyde dehydrogenase 1-positive cells in breast cancer cells of the basal B subtype. BMC Cancer 10: 568, 2010.
35. Nautiyal J, Kanwar SS, Yu Y and Majumdar AP: Combination of dasatinib and curcumin eliminates chemo-resistant colon cancer cells. J Mol Signal 6: 7, 2011.
36. Duong HQ, Kim HJ, Kang HJ, Seong YS and Bae I: ZSTK474, a PI3K inhibitor, suppresses proliferation and sensitizes human pancreatic adenocarcinoma cells to gemcitabine. Oncol Rep 27: 182-188, 2012.
37. Duong HQ, Hong YB, Kim JS, Lee HS, Yi YW, Kim YJ, Wang A, Zhao W, Cho CH, Seong YS and Bae I: Inhibition of checkpoint kinase 2 (CHK2) enhances sensitivity of pancreatic adenocarcinoma cells to gemcitabine. J Cell Mol Med 17: 1261-1270, 2013.
38. Nagaraj NS, Smith JJ, Revetta F, Washington MK and Merchant NB: Targeted inhibition of SRC kinase signaling attenuates pancreatic tumorigenesis. Mol Cancer Ther 9: 2322-2332, 2010.
39. Dick JE: Stem cell concepts renew cancer research. Blood 112: 4793-4807, 2008.
40. Wang JC and Dick JE: Cancer stem cells: lesions from leukemia. Trends Cell Biol 15: 494-501, 2005.
41. Yin T, Wei H, Gou S, Shi P, Yang Z, Zhao G and Wang C: Cancer stem-like cells enriched in panc-1 spheres possess increased migration ability and resistance to gemcitabine. Int J Mol Sci 12: 1595-1604, 2011.
42. Hu G, Li F, Ouyang K, Xie F, Tang X, Wang K, Han S, Jiang Z, Zhu M, Wen D, Qin X and Zhang L: Intrinsic gemcitabine resistance in a novel pancreatic cancer cell line is associated with cancer stem cell-like phenotype. Int J Oncol 40: 798-806, 2012.
43. Hage C, Rausch V, Giese N, Giese T, Schonsiegel F, Labsch S, Nwaeburu C, Mattern J, Gladkich J and Herr I: The novel c-Met inhibitor cabozantinib overcomes gemcitabine resistance and stem cell signaling in pancreatic cancer. Cell Death Dis 4: e627, 2013.
44. Li C, Heidt DG, Dalerba P, Burant CF, Zhang L, Adsay V, Wicha M, Clarke MF and Simeone DM: Identification of pancreatic cancer stem cells. Cancer Res 67: 1030-1037, 2007.
45. Kim MP, Fleming JB, Wang H, Abbruzzese JL, Choi W, Kopetz S, McConkey DJ, Evans DB and Gallick GE: ALDH activity selectively defines an enhanced tumor-initiating cell population relative to CD133 expression in human pancreatic adenocarcinoma. PLoS One 6: e20636, 2011.
46. Koppaka V, Thompson DC, Chen Y, Ellermann M, Nicolaou KC, Juvonen RO, Petersen D, Deitrich RA, Hurley TD and Vasiliou V: Aldehyde dehydrogenase inhibitors: a comprehensive review on the pharmacology, mechanism of action, substrate specificity, and clinical application. Pharmacol Rev 64: 520-539, 2012.
47. + human breast cancer cells. Breast Cancer Res Treat 133: 75-87, 2012.