Synergistic activity of the Src family kinase inhibitor dasatinib and oxaliplatin in colon carcinoma cells is mediated by oxidative stress

Cancer Research

Volumn 69, Issue 9, 2009, Pages 3842-3849

  Kopetz, Scott ^a   Lesslie, Donald P ^a   Dallas, Nikolas A ^a   Park, Serk I ^a   Johnson, Marjorie ^a   Parikh, Nila U ^a   Kim, Michael P ^a   Abbruzzese, James L ^a   Ellis, Lee M ^a   Chandra, Joya ^b   Gallick, Gary E ^a,c  

^a UNIVERSITY OF TEXAS   (United States)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^c UNIVERSITY OF TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCYSTEINE; DASATINIB; OXALIPLATIN; PROTEIN TYROSINE KINASE; REACTIVE OXYGEN METABOLITE; TIRON;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ARTICLE; CANCER COMBINATION CHEMOTHERAPY; CANCER REGRESSION; CANCER RESISTANCE; CANCER SIZE; CANCER SUSCEPTIBILITY; CARCINOMA CELL; COLORECTAL CARCINOMA; CONTROLLED STUDY; DRUG EFFICACY; DRUG POTENCY; DRUG POTENTIATION; DRUG SENSITIVITY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INACTIVATION; ENZYME INHIBITION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LIVER METASTASIS; MALE; METASTASIS INHIBITION; MOUSE; NONHUMAN; NUDE MOUSE; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; THERAPY EFFECT; TREATMENT OUTCOME; TREATMENT RESPONSE;

ANIMALS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; APOPTOSIS; CELL GROWTH PROCESSES; COLONIC NEOPLASMS; DOWN-REGULATION; DRUG SYNERGISM; HCT116 CELLS; HT29 CELLS; HUMANS; LIVER NEOPLASMS, EXPERIMENTAL; MALE; MICE; MICE, NUDE; NEOVASCULARIZATION, PATHOLOGIC; ORGANOPLATINUM COMPOUNDS; OXIDATIVE STRESS; PROTEIN KINASE INHIBITORS; PYRIMIDINES; RANDOM ALLOCATION; REACTIVE OXYGEN SPECIES; SRC-FAMILY KINASES; THIAZOLES; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 65949102791     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-08-2246     Document Type: Article

References (48)

1. Kelland Kelland. The resurgence of platinum-based cancer chemotherapy. Nat Rev Cancer 2007; 7: 573-84.
2. Miyajima Miyajima. Nakashima Nakashima. Yoshioka Yoshioka. Tachibana Tachibana. Tazaki Tazaki. Murai Murai. Role of reactive oxygen species in cis-dichlorodiammineplatinum-induced cytotoxicity on bladder cancer cells. Br J Cancer 1997; 76: 206-10.
3. Laurent Laurent. Nicco Nicco. Chereau Chereau. et al. Controlling tumor growthby modulating endogenous production of reactive oxygen species. Cancer Res 2005; 65: 948-56.
4. Godwin Godwin. Meister Meister. O'Dwyer PJ. Huang Huang. Hamilton Hamilton. Anderson Anderson. Highresistance to cisplatin in human ovarian cancer cell lines is associated with marked increase of glutathione synthesis. Proc Natl Acad Sci U S A 1992; 89: 3070-4.
5. Masuda Masuda. Tanaka Tanaka. Takahama Takahama. Cisplatin generates superoxide anion by interaction withDNA in a cell-free system. Biochem Biophys Res Commun 1994; 203: 1175-80.
6. Kruidering Kruidering. Van de Water B. de Heer E. Mulder Mulder. Nagelkerke Nagelkerke. Cisplatin-induced nephrotoxicity in porcine proximal tubular cells: mitochondrial dysfunction by inhibition of complexes I to IV of the respiratory chain. J Pharmacol Exp Ther 1997; 280: 638-49.
7. Kopetz Kopetz. Shah Shah. Gallick Gallick. SRC continues aging: current and future clinical directions. Clin Cancer Res 2007; 13: 7232-6.
8. Summy Summy. Gallick Gallick. Treatment for advanced tumors: SRC reclaims center stage. Clin Cancer Res 2006; 12: 1398-401.
9. Termuhlen Termuhlen. Curley Curley. Talamonti Talamonti. Saboorian Saboorian. Gallick Gallick. Site-specific differences in pp60c-src activity in human colorectal metastases. J Surg Res 1993; 54: 293-8.
10. Talamonti Talamonti. Roh MS. Curley Curley. Gallick Gallick. Increase in activity and level of pp60c-src in progressive stages of human colorectal cancer. J Clin Invest 1993; 91: 53-60.
11. Allgayer Allgayer. Boyd Boyd. Heiss Heiss. Abdalla Abdalla. Curley Curley. Gallick Gallick. Activation of Src kinase in primary colorectal carcinoma: an indicator of poor clinical prognosis. Cancer 2002; 94: 344-51.
12. Schlessinger Schlessinger. New roles for Src kinases in control of cell survival and angiogenesis. Cell 2000; 100: 293-6.
13. Ellis Ellis. Staley Staley. Liu Liu. et al. Down-regulation of vascular endothelial growth factor in a human colon carcinoma cell line transfected withan antisense expression vector specific for c-src. J Biol Chem 1998; 273: 1052-7.
14. Gray Gray. Zhang Zhang. Ellis Ellis. et al. HIF-1a, STAT3, CBP/p300 and Ref-1/APE are components of a transcriptional complex that regulates Src-dependent hypoxia-induced expression of VEGF in pancreatic and prostate carcinomas. Oncogene 2005; 24: 3110-20.
15. Griffiths Griffiths. Koh Koh. Brunton Brunton. et al. Expression of kinase-defective mutants of c-Src in human metastatic colon cancer cells decreases Bcl-xL and increases oxaliplatin- and Fas-induced apoptosis. J Biol Chem 2004; 279: 46113-21.
16. Duxbury Duxbury. Ito Ito. Zinner Zinner. Ashley Ashley. Whang Whang. Inhibition of SRC tyrosine kinase impairs inherent and acquired gemcitabine resistance in human pancreatic adenocarcinoma cells. Clin Cancer Res 2004; 10: 2307-18.
17. George George. Chen Chen. Taylor Taylor. SRC tyrosine kinase and multidrug resistance protein-1 inhibitions act independently but cooperatively to restore paclitaxel sensitivity to paclitaxel-resistant ovarian cancer cells. Cancer Res 2005; 65: 10381-8.
18. Pengetnze Pengetnze. Steed Steed. Roby Roby. Terranova Terranova. Taylor Taylor. Src tyrosine kinase promotes survival and resistance to chemotherapeutics in a mouse ovarian cancer cell line. Biochem Biophys Res Commun 2003; 309: 377-83.
19. Lombardo Lombardo. Lee Lee. Chen Chen. et al. Discovery of N- (2-chloro-6-methyl-phenyl) -2- (6- (4- (2-hydroxyethyl) - piperazin-1-yl) -2-methylpyrimidin-4-ylamino) thiazole-5- carboxamide (BMS-354825), a dual Src/Abl kinase inhibitor with potent antitumor activity in preclinical assays. J Med Chem 2004; 47: 6658-61.
20. Yang Yang. Fan Fan. Camp Camp. et al. Chronic oxaliplatin resistance induces epithelial-to-mesenchymal transition in colorectal cancer cell lines. Clin Cancer Res 2006; 12: 4147-53.
21. Lesslie Lesslie. Summy Summy. Parikh NU. et al. Vascular endothelial growth factor receptor-1 mediates migration of human colorectal carcinoma cells by activation of Src family kinases. Br J Cancer 2006; 94: 1710-7.
22. Chou Chou. Talalay Talalay. Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Adv Enzyme Regul 1984; 22: 27-55.
23. Chou T-C. Theoretical basis, experimental design, and computerized simulation of synergism and antagonism in drug combination studies. Pharmacol Rev 2006; 58: 621-81.
24. Trevino Trevino. Summy Summy. Gray Gray. et al. Expression and activity of SRC regulate interleukin-8 expression in pancreatic adenocarcinoma cells: implications for angiogenesis. Cancer Res 2005; 65: 7214-22.
25. LeBel LeBel. Ischiropoulos Ischiropoulos. Bondy Bondy. Evaluation of the probe 2', 7'-dichlorofluorescein as an indicator of reactive oxygen species formation and oxidative stress. Chem Res Toxicol 1992; 5: 227-31.
26. Smith AD. Morris Morris. Levander Levander. Rapid determination of glutathione peroxidase and thioredoxin reductase activities using a 96-well microplate format: comparison to standard cuvette-based assays. Int J Vitam Nutr Res 2001; 71: 87-92.
27. Gray Gray. Van Buren G. Dallas Dallas. et al. Therapeutic targeting of neuropilin-2 on colorectal carcinoma cells implanted in the murine liver. J Natl Cancer Inst 2008; 100: 109-20.
28. O'Reilly MS. Holmgren Holmgren. Chen Chen. Folkman Folkman. Angiostatin induces and sustains dormancy of human primary tumors in mice. Nat Med 1996; 2: 689-92.
29. Reinmuth N. Fan Fan. Liu Liu. et al. Impact of insulinlike growthfactor receptor-I function on angiogenesis, growth, and metastasis of colon cancer. Lab Invest 2009; 82: 1377-89.
30. Takahashi Takahashi. Tucker Tucker. Kitadai Kitadai. et al. Vessel counts and expression of vascular endothelial growth factor as prognostic factors in node-negative colon cancer. Arch Surg 1997; 132: 541-6.
31. Benhar Benhar. Engelberg Engelberg. Levitzki Levitzki. Cisplatininduced activation of the EGF receptor. Oncogene 2002; 21: 8723-31.
32. Windham Windham. Parikh Parikh. Siwak Siwak. et al. Src activation regulates anoikis in human colon tumor cell lines. Oncogene 2002; 21: 7797-807.
33. Palmer Palmer. Zimmer Zimmer. Erdmann Erdmann. et al. Ephrin Bphosphorylation and reverse signaling: regulation by Src kinases and PTP-BL phosphatase. Mol Cell 2002; 9: 725-37.
34. 2+/calmodulin. Biochim Biophys Acta 1998; 1405: 171-9.
35. Lei Lei. Townsend Townsend. Tew Tew. Protein cysteine sulfinic acid reductase (sulfiredoxin) as a regulator of cell proliferation and drug response. Oncogene 2008; 27: 4877-87.
36. Witte Witte. Anestal Anestal. Jerremalm Jerremalm. Ehrsson Ehrsson. Arner Arner. Inhibition of thioredoxin reductase but not of glutathione reductase by the major classes of alkylating and platinum-containing anticancer compounds. Free Radic Biol Med 2005; 39: 696-703.
37. Han Han. Curley Curley. Gallick Gallick. Differential activation of pp60 (c-src) and pp62 (c-yes) in human colorectal carcinoma liver metastases. Clin Cancer Res 1996; 2: 1397-404.
38. Sasada Sasada. Iwata Iwata. Sato Sato. et al. Redox control of resistance to cis-diamminedichloroplatinum (II) (CDDP): protective effect of human thioredoxin against CDDP- induced cytotoxicity. J Clin Invest 1996; 97: 2268-76.
39. Gourdier Gourdier. Crabbe Crabbe. Andreau Andreau. Pau Pau. Kroemer Kroemer. Oxaliplatin-induced mitochondrial apoptotic response of colon carcinoma cells does not require nuclear DNA. Oncogene 2004; 23: 7449-57.
40. Pu Pu. Akhand Akhand. Kato Kato. et al. Evidence of a novel redox-linked activation mechanism for the Src kinase which is independent of tyrosine 527-mediated regulation. Oncogene 1996; 13: 2615-22.
41. Giannoni Giannoni. Buricchi Buricchi. Raugei Raugei. Ramponi Ramponi. Chiarugi Chiarugi. Intracellular reactive oxygen species activate Src tyrosine kinase during cell adhesion and anchorage-dependent cell growth. Mol Cell Biol 2005; 25: 6391-403.
42. Krasnowska Krasnowska. Pittaluga Pittaluga. Brunati Brunati. et al. N-acetyl- L-cysteine fosters inactivation and transfer to endolysosomes of c-Src. Free Radic Biol Med 2008; 45: 1566-72.
43. Chinery Chinery. Brockman Brockman. Peeler Peeler. Shyr Shyr. Beauchamp Beauchamp. Coffey Coffey. Antioxidants enhance the cytotoxicity of chemotherapeutic agents in colorectal cancer: a p53-independent induction of p21WAF1/CIP1 via C/EBPβ. Nat Med 1997; 3: 1233-41.
44. Alexandre Alexandre. Nicco Nicco. Chereau Chereau. et al. Improvement of the therapeutic index of anticancer drugs by the superoxide dismutase mimic mangafodipir. J Natl Cancer Inst 2006; 98: 236-44.
45. Pelicano Pelicano. Carney Carney. Huang Huang. ROS stress in cancer cells and therapeutic implications. Drug Resist Updat 2004; 7: 97-110.
46. Eng Eng. Kopetz Kopetz. Morris Morris. et al. Phase II study of the novel oral Src-kinase inhibitor, AZD0530, in previously treated advanced colorectal cancer patients. Proceedings of the 98th Annual Meeting of the AACR; 2008. San Diego, CA. LB-76.
47. Kopetz Kopetz. Wolff Wolff. C. C. et al. Phase IB study of Src inhibition with dasatinib in combination with 5-fluorouracil, leucovorin, oxaliplatin (FOLFOX) and cetuximab in metastatic colorectal cancer. Proceedings of the 98th Annual Meeting of the AACR; 2008 Apr. 12-16; San Diego, CA. LB-69.
48. Lu Lu. Li Li. Liang Liang. et al. Epidermal growthfactor receptor (EGFR) ubiquitination as a mechanism of acquired resistance escaping treatment by the anti-EGFR monoclonal antibody cetuximab. Cancer Res 2007; 67: 8240-7.