A small-molecule induces apoptosis and suppresses metastasis in pancreatic cancer cells

European Journal of Pharmaceutical Sciences

Volumn 48, Issue 4-5, 2013, Pages 658-667

  Li, Dan ^a   Liu, Zuojia ^a   Zhao, Wenjing ^a   Zheng, Xiliang ^a   Wang, Jin ^a,b   Wang, Erkang ^a  

^a CHANGCHUN INSTITUTE OF APPLIED CHEMISTRY   (China)

^b STONY BROOK UNIVERSITY   (United States)

Author keywords

Apoptosis; Metastasis; Mitochondrial pathway; Pancreatic cancer

Indexed keywords

4 TERT BUTYL 2 [(CYCLOHEXYLAMINO) METHYL] 6 METHYLPHENOL; ANTINEOPLASTIC AGENT; CASPASE 3; CASPASE 9; CYTOCHROME C; PROTEIN BAX; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER INHIBITION; CANCER INVASION; CELL INVASION; CELL VIABILITY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; DRUG SELECTIVITY; ENZYME ACTIVATION; HUMAN; HUMAN CELL; IC 50; IN VITRO STUDY; METASTASIS; MITOCHONDRIAL MEMBRANE POTENTIAL; PANCREAS CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; WOUND HEALING;

ANTINEOPLASTIC AGENTS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; BENZYLAMINES; CELL LINE, TUMOR; CELL SURVIVAL; CYCLOHEXYLAMINES; CYTOCHROMES C; HEK293 CELLS; HUMANS; MEMBRANE POTENTIAL, MITOCHONDRIAL; NEOPLASM METASTASIS; PANCREATIC NEOPLASMS; REACTIVE OXYGEN SPECIES; WOUND HEALING;

EID: 84875203212     PISSN: 09280987     EISSN: 18790720     Source Type: Journal    
DOI: 10.1016/j.ejps.2012.12.023     Document Type: Article

References (58)

1. M. Akada, T. Crnogorac-Jurcevic, S. Lattimore, P. Mahon, R. Lopes, M. Sunamura, S. Matsuno, and N.R. Lemoine Intrinsic chemoresistance to gemcitabine is associated with decreased expression of BNIP3 in pancreatic cancer Clin. Cancer Res. 11 2005 3094 3101
2. M.N. Balak, Y. Gong, G.J. Riely, R. Somwar, A.R. Li, M.F. Zakowski, A. Chiang, G. Yang, O. Ouerfelli, M.G. Kris, M. Ladanyi, V.A. Miller, and W. Pao Novel D761Y and common secondary T790M mutations in epidermal growth factor receptor-mutant lung adenocarcinomas with acquired resistance to kinase inhibitors Clin. Cancer Res. 12 2006 6494 6501
3. S. Banerjee, A.O. Kaseb, Z. Wang, D. Kong, M. Mohammad, S. Padhye, F.H. Sarkar, and R.M. Mohammad Antitumor activity of gemcitabine and oxaliplatin is augmented by thymoquinone in pancreatic cancer Cancer Res. 69 2009 5575 5583
4. C.D. Blanke, J. Shultz, J. Cox, M. Modiano, R. Isaacs, B. Kasimis, R. Schilsky, J. Fleagle, M. Moore, N. Kemeny, D. Carlin, L. Hammershaimb, D. Haller, and P. Investigators A double-blind placebo-controlled randomized phase III trial of 5-fluorouracil and leucovorin, plus or minus trimetrexate, in previously untreated patients with advanced colorectal cancer Ann. Oncol. 13 2002 87 91
5. J.L. Bos ras Oncogenes in Human Cancer: A Review Cancer Res. 49 1989 4682 4689
6. C.J. Bruns, C.C. Solorzano, M.T. Harbison, S. Ozawa, R. Tsan, D. Fan, J. Abbruzzese, P. Traxler, E. Buchdunger, R. Radinsky, and I.J. Fidler Blockade of the epidermal growth factor receptor signaling by a novel tyrosine kinase inhibitor leads to apoptosis of endothelial cells and therapy of human pancreatic carcinoma Cancer Res. 60 2000 2926 2935
7. E. Buck, A. Eyzaguirre, J.D. Haley, N.W. Gibson, P. Cagnoni, and K.K. Iwata Inactivation of Akt by the epidermal growth factor receptor inhibitor erlotinib is mediated by HER-3 in pancreatic and colorectal tumor cell lines and contributes to erlotinib sensitivity Mol. Cancer Ther. 5 2006 2051 2059
8. I. Budihardjo, H. Oliver, M. Lutter, X. Luo, and X. Wang Biochemical pathways of caspase activation during apoptosis Annu. Rev. Cell Dev. Biol. 15 1999 269 290
9. H.A. Burris, M.J. Moore, J. Andersen, M.R. Green, M.L. Rothenberg, M.R. Modiano, M.C. Cripps, R.K. Portenoy, A.M. Storniolo, P. Tarassoff, R. Nelson, F.A. Dorr, C.D.Von. Stephens, and D.D. Hoff 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 1997 2403 2413
10. A. Carracedo, M. Gironella, M. Lorente, S. Garcia, M. Guzmán, G. Velasco, and J.L. Iovanna Cannabinoids induce apoptosis of pancreatic tumor cells via endoplasmic reticulum stress related genes Cancer Res. 66 2006 6748 6755
11. V. Cryns, and J. Yuan Proteases to die for Gene. Dev. 12 1998 1551 1570
12. T.P. Devasagayam, J.C. Tilak, K.K. Boloor, K.S. Sane, S.S. Ghaskadbi, and R.D. Lele Free radicals and antioxidants in human health: current status and future prospects J. Assoc. Phys. India 52 2004 794 804
13. J. Downward Targeting Ras signalling pathways in cancer therapy Nat. Rev. Cancer 3 2003 11 22
14. M. Ducreux, V. Boige, D. Goéré, E. Deutsch, P. Ezra, D. Elias, and D. Malka Pancreatic cancer: from pathogenesis to cure Res. Clin. Gastroenterol. 21 2007 997 1014
15. J.-H. Egberts, V. Cloosters, A. Noack, B. Schniewind, L. Thon, S. Klose, B. Kettler, C. von Forstner, C. Kneitz, J. Tepel, D. Adam, H. Wajant, H. Kalthoff, and A. Trauzold Anti-tumor necrosis factor therapy inhibits pancreatic tumor growth and metastasis Cancer Res. 68 2008 1443 1450
16. S. Elmore Apoptosis: a review of programmed cell death Toxicol. Pathol. 35 2007 495 516
17. B. Ford, V. Hornak, H. Kleinman, and N. Nassar Structure of a transient intermediate for GTP hydrolysis by Ras Structure 14 2006 427 436
18. S. Fulda, and K.M. Debatin Extrinsic versus intrinsic apoptosis pathways in anticancer chemotherapy Oncogene. 25 2006 4798 4811
19. J.C. Goldstein, N.J. Waterhouse, P. Juin, G.I. Evan, and D.R. Green The coordinate release of cytochrome c during apoptosis is rapid, complete and kinetically invariant Nat. Cell Biol. 2 2000 156 162
20. W. Guo, and B.L. Fang Dominant negative Ras as an anticancer agent Cancer Biol. Ther. 5 2006 1492 1493
21. B.E. Hall, D. Bar-Sagi, and N. Nassar The structural basis for the transition from Ras-GTP to Ras-GDP Proc. Natl. Acad. Sci. USA 99 2002 12138 12142
22. D. Hanahan, and R.A. Weinberg The Hallmarks of Cancer Cell 100 2000 57 70
23. D. Hariharan, A. Saied, and H.M. Kocher Analysis of mortality rates for pancreatic cancer across the world HPB 10 2008 58 62
24. S.P. Hong, J. Wen, S. Bang, S. Park, and S.Y. Song CD44-positive cells are responsible for gemcitabine resistance in pancreatic cancer cells Int. J. Cancer 125 2009 2323 2331
25. Y. Hu, M.A. Benedict, L. Ding, and G. Nunez Role of cytochrome c and dATP/ATP hydrolysis in Apaf-1-mediated caspase-9 activation and apoptosis EMBO J. 18 1999 3586 3595
26. M. Humbert, N. Casteran, S. Letard, K. Hanssens, J. Iovanna, P. Finetti, F. Bertucci, T. Bader, C.D. Mansfield, A. Moussy, O. Hermine, and P. Dubreuil Masitinib combined with standard gemcitabine chemotherapy: in vitro and in vivo studies in human pancreatic tumour cell lines and ectopic mouse model PLoS ONE 5 2010 e9430
27. W. Jin, W. Aibin, X. Yufang, L. Jianwen, and Q. Xuhong M2-A induces apoptosis and G2-M arrest via inhibiting PI3K/Akt pathway in HL60 cells Cancer Lett. 283 2009 193 202
28. D.C. Joshi, and J.C. Bakowska Determination of mitochondrial membrane potential and reactive oxygen species in live rat cortical neurons J. Vis. Exp. 51 2011 e2704
29. S. Keleg, P. Buchler, R. Ludwig, M. Buchler, and H. Friess Invasion and metastasis in pancreatic cancer Mol. Cancer. 2 2003 14
30. J.F. Kerr, A.H. Wyllie, and A.R. Currie Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics Br. J. Cancer. 26 1972 239 257
31. H.L. Kindler, G. Friberg, D.A. Singh, G. Locker, S. Nattam, M. Kozloff, D.A. Taber, T. Karrison, A. Dachman, W.M. Stadler, and E.E. Vokes Phase II trial of bevacizurnab plus gemcitabine in patients with advanced pancreatic cancer J. Clin. Oncol. 23 2005 8033 8040
32. S. Kothakota, T. Azuma, C. Reinhard, A. Klippel, J. Tang, K. Chu, T.J. McGarry, M.W. Kirschner, K. Koths, D.J. Kwiatkowski, and L.T. Williams Caspase-3-generated fragment of gelsolin: effector of morphological change in apoptosis Science 278 1997 294 298
33. S.D. Lahiri, G.F. Zhang, D. Dunaway-Mariano, and K.N. Allen The pentacovalent phosphorus intermediate of a phosphoryl transfer reaction Science 299 2003 2067 2071
34. D. Li, K. Xie, R. Wolff, and J.L. Abbruzzese Pancreatic cancer The Lancet. 363 2004 1049 1057
35. L. Li, B.B. Aggarwal, S. Shishodia, J. Abbruzzese, and R. Kurzrock Nuclear factor-κB and IκB kinase are constitutively active in human pancreatic cells, and their down-regulation by curcumin (diferuloylmethane) is associated with the suppression of proliferation and the induction of apoptosis Cancer 101 2004 2351 2362
36. P. Li, D. Nijhawan, I. Budihardjo, S.M. Srinivasula, M. Ahmad, E.S. Alnemri, and X. Wang Cytochrome c and dATP-dependent formation of Apaf-1/Caspase-9 complex initiates an apoptotic protease cascade Cell 91 1997 479 489
37. Q. Li, M. Wu, H. Wang, G. Xu, T. Zhu, Y. Zhang, P. Liu, A. Song, C. Gang, Z. Han, J. Zhou, L. Meng, Y. Lu, S. Wang, and D. Ma Ezrin silencing by small hairpin RNA reverses metastatic behaviors of human breast cancer cells Cancer Lett. 261 2008 55 63
38. J. Ma, and M. Karplus Molecular switch in signal transduction: reaction paths of the conformational changes in Ras P21 Proc. Natl. Acad. Sci. USA 94 1997 11905 11910
39. M. Mimeault, R. Hauke, and S.K. Batra Recent advances on the molecular mechanisms involved in the drug resistance of cancer cells and novel targeting therapies Clin. Pharmacol. Ther. 83 2007 673 691
40. M.J. Moore, D. Goldstein, J. Hamm, A. Figer, J.R. Hecht, S. Gallinger, H.J. Au, P. Murawa, D. Walde, R.A. Wolff, D. Campos, R. Lim, K. Ding, G. Clark, T. Voskoglou-Nomikos, M. Ptasynski, and W. Parulekar Erlotinib plus gemcitabine compared with gemcitabine alone in patients with advanced pancreatic cancer: a phase III trial of the National Cancer Institute of Canada Clinical Trials Group J. Clin. Oncol. 25 2007 1960 1966
41. I. Murtaza, M. Saleem, V.M. Adhami, B.B. Hafeez, and H. Mukhtar Suppression of cFLIP by Lupeol, a Dietary Triterpene, is sufficient to overcome resistance to TRAIL-mediated apoptosis in chemoresistant human pancreatic cancer cells Cancer Res. 69 2009 1156 1165
42. J. Neuzil, X.F. Wang, L.F. Dong, P. Low, and S.J. Ralph Molecular mechanism of 'mitocan'-induced apoptosis in cancer cells epitomizes the multiple roles of reactive oxygen species and Bcl-2 family proteins FEBS Lett. 580 2006 5125 5129
43. Oberstein, P.E., Saif, M.W., 2011. First-line treatment for advanced pancreatic cancer. Highlights from the "2011 ASCO Gastrointestinal Cancers Symposium". San Francisco, CA, USA. January 20-22, 2011. JOP: J. Pancreas. vol. 2, pp. 96-100.
44. M. Parreno, I. Casanova, M.V. Cespedes, J.P. Vaque, M.A. Pavon, J. Leon, and R. Mangues Bobel-24 and derivatives induce caspase-independent death in pancreatic cancer regardless of apoptotic resistance Cancer Res. 68 2008 6313 6323
45. W. Plunkett, P. Huang, and V. Gandhi Preclinical characteristics of gemcitabine Anticancer Drugs 6 1995 7 13
46. N.K. Rai, K. Tripathi, D. Sharma, and V.K. Shukla Apoptosis: a basic physiologic process in wound healing Inter. J. Lower Extremity Wounds 4 2005 138 144
47. Raymond, E., Faivre, S., Armand, J.P., 2000. Epidermal growth factor receptor tyrosine kinase as a target for anticancer therapy. Drugs. vol. 60 Suppl. 1, pp. 15-23; discussion 41-12.
48. J.C. Reed, and D.R. Green Remodeling for demolition: changes in mitochrondrial ultrastructure during apoptosis Mol. Cell. 9 2002 1 3
49. S. Rejiba, C. Bigand, C. Parmentier, and A. Hajri Gemcitabine-based chemogene therapy for pancreatic cancer using Ad-dCK: UMK GDEPT and TS/RR siRNA strategies Neoplasia 11 2009 637 650
50. G. Schneider, J.T. Siveke, F. Eckel, and R.M. Schmid Pancreatic cancer: basic and clinical aspects Gastroenterology 128 2005 1606 1625
51. K. Stahnke, A. Mohr, J. Liu, L.H. Meyer, L. Karawajew, and K.M. Debatin Identification of deficient mitochondrial signaling in apoptosis resistant leukemia cells by flow cytometric analysis of intracellular cytochrome c, caspase-3 and apoptosis Apoptosis 9 2004 457 465
52. Y. Tsujimoto, and S. Shimizu Bcl-2 family: life-or-death switch FEBS Lett. 466 2000 6 10
53. B. Turk, V. Stoka, J. Rozman-Pungercar, T. Cirman, G. Droga-Mazovec, K. Oreic, and V. Turk Apoptotic pathways: involvement of lysosomal proteases Biol. Chem. 383 2002 1035 1044
54. M. Vogler, H. Walczak, D. Stadel, T.L. Haas, F. Genze, M. Jovanovic, U. Bhanot, C. Hasel, P. Moller, J.E. Gschwend, T. Simmet, K.-M. Debatin, and S. Fulda Small molecule XIAP inhibitors enhance TRAIL-induced apoptosis and antitumor activity in preclinical models of pancreatic carcinoma Cancer Res. 69 2009 2425 2434
55. W. von Bernstorff, M. Voss, S. Freichel, A. Schmid, I. Vogel, C. Johnk, D. Henne-Bruns, B. Kremer, and H. Kalthoff Systemic and local immunosuppression in pancreatic cancer patients Clin. Cancer Res. 7 2001 925s 932s
56. Z. Wang, A.S. Azmi, A. Ahmad, S. Banerjee, S. Wang, F.H. Sarkar, and R.M. Mohammad TW-37, a small-molecule inhibitor of Bcl-2, inhibits cell growth and induces apoptosis in pancreatic cancer: involvement of notch-1 signaling pathway Cancer Res. 69 2009 2757 2765
57. S. Westphal, and H. Kalthoff Apoptosis: targets in pancreatic cancer Mol. Cancer. 2 2003 6
58. Y.-j. Zhou, S.-p. Zhang, C.-w. Liu, and Y.-q. Cai The protection of selenium on ROS mediated-apoptosis by mitochondria dysfunction in cadmium-induced LLC-PK1 cells Toxicol. in Vitro. 23 2009 288 294