Synergistic Antiproliferative Effects of a New Cucurbitacin B Derivative and Chemotherapy Drugs on Lung Cancer Cell Line A549

Chemical Research in Toxicology

Volumn 28, Issue 10, 2015, Pages 1949-1960

  Marostica, Lucas Lourenço ^a   Silva, Izabella Thaís ^a   Kratz, Jadel Müller ^a   Persich, Lara ^a   Geller, Fabiana Cristina ^a   Lang, Karen Luise ^a   Caro, Miguel Soriano Balparda ^a   Durán, Fernando Javier ^b   Schenkel, Eloir Paulo ^a   Simões, Cláudia Maria Oliveira ^a  

^a FEDERAL UNIVERSITY OF SANTA CATARINA   (Brazil)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

2 DEOXY 2 AMINE CUCURBITACIN E; ACETYLCYSTEINE; BUTHIONINE SULFOXIMINE; CASPASE; CISPLATIN; CUCURBITACIN; F ACTIN; IRINOTECAN; PACLITAXEL; PROTEIN P53; REACTIVE OXYGEN METABOLITE; SURVIVIN; UNCLASSIFIED DRUG; ACTIN; ANTINEOPLASTIC AGENT; BIRC5 PROTEIN, HUMAN; CAMPTOTHECIN; CUCURBITACIN B; INHIBITOR OF APOPTOSIS PROTEIN; TP53 PROTEIN, HUMAN; TRITERPENE;

A549 CELL LINE; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; CANCER INHIBITION; CELL PROLIFERATION; COMPARATIVE EFFECTIVENESS; COMPUTER MODEL; CONTROLLED STUDY; CYTOSKELETON; DRUG MECHANISM; DRUG POTENCY; DRUG POTENTIATION; DRUG STRUCTURE; ENZYME ACTIVITY; ENZYME INHIBITION; FLOW CYTOMETRY; G2 PHASE CELL CYCLE CHECKPOINT; HUMAN; HUMAN CELL; IC50; METASTASIS INHIBITION; MIGRATION INHIBITION; PROTEIN EXPRESSION; ANALOGS AND DERIVATIVES; CELL MOTION; CHEMISTRY; DRUG EFFECTS; LUNG NEOPLASMS; M PHASE CELL CYCLE CHECKPOINT; METABOLISM; PATHOLOGY; TUMOR CELL LINE;

ACTINS; ANTINEOPLASTIC AGENTS; APOPTOSIS; CAMPTOTHECIN; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; CISPLATIN; DRUG SYNERGISM; G2 PHASE CELL CYCLE CHECKPOINTS; HUMANS; INHIBITOR OF APOPTOSIS PROTEINS; LUNG NEOPLASMS; M PHASE CELL CYCLE CHECKPOINTS; PACLITAXEL; REACTIVE OXYGEN SPECIES; TRITERPENES; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84944754711     PISSN: 0893228X     EISSN: 15205010     Source Type: Journal    
DOI: 10.1021/acs.chemrestox.5b00153     Document Type: Article

References (55)

1. Chen, Z., Fillmore, C. M., Hammerman, P. S., Kim, C. F., and Wong, K.-K. (2014) Non-small cell lung cancers: a heterogeneous set of diseases Nat. Rev. Cancer 14, 535-546 10.1038/nrc3775
2. Siegel, R. L., Miller, K. D., and Jemal, A. (2015) Cancer Statistics, 2015 Ca-Cancer J. Clin. 65, 5-29 10.3322/caac.21254
3. Koh, P. K., Faivre-Finn, C., Blackhall, F. H., and De Ruysscher, D. (2012) Targeted agents in non-small cell lung cancer (NSCLC): Clinical developments and rationale for the combination with thoracic radiotherapy Cancer Treat. Rev. 38, 626-640 10.1016/j.ctrv.2011.11.003
4. Ríos, I., Andújar, J. M., Escandell, R. M., and Recio, M. C. (2012) Cucurbitacins as inducers of cell death and a rich source of potential cancer compounds Curr. Pharm. Des. 18, 1663-1676 10.2174/138161212799958549
5. Chen, X., Bao, J., Guo, J., Ding, Q., Lu, J., Huang, M., and Wang, Y. (2012) Biological activities and potential molecular targets of cucurbitacins: a focus on cancer Anti-Cancer Drugs 23, 777-787 10.1097/CAD.0b013e3283541384
6. Silva, I. T., Carvalho, A., Lang, K. L., Dudek, S. E., Durán, F. J., Caro, M. S. B., Rapp, U. R., Wixler, V., Schenkel, E. P., Simões, C. M. O., and Ludwig, S. (2015) In vitro and in vivo antitumor activity of a novel semisynthetic derivative of cucurbitacin B PLoS One 10, 1-19 10.1371/journal.pone.0117794
7. Lang, K. L., Guimarães, T., Machado, V. R., Zimmermann, L., Silva, I. T., Teixeira, M. R., Durán, F. J., Palermo, J. A., Simões, C. M. O., Caro, M. B. C., and Schenkel, E. P. (2011) New cytotoxic cucurbutacins from Wilbrandia ebracteata Cogn Planta Med. 77, 1648-1651 10.1055/s-0030-1270962
8. Lang, K., Silva, I. T., Zimmermann, L., Machado, V. R., Teixeira, M. R., Lapuh, M. I., Galleti, M. A., Palermo, J. A., Cabrera, G. M., Bernardes, L. S. C., Simões, C. M. O., Schenkel, E. P., Caro, M. S. B., and Durán, F. J. (2012) Synthesis and cytotoxic activity evaluation of dihydrocucurbitacin B and cucurbitacin B derivatives Bioorg. Med. Chem. 20, 3016-3030 10.1016/j.bmc.2012.03.001
9. Lang, K. L., Silva, I. T., Machado, V. R., Zimmermann, L., Caro, M. S. B., Simões, C. M. O., Schenkel, E. P., Durán, F. J., Bernardes, L. S. C., and Melo, E. B. (2014) Multivariate SAR and QSAR of cucurbitacin derivatives as cytotoxic compounds in a human lung adenocarcinoma cell line J. Mol. Graphics Modell. 48, 70-79 10.1016/j.jmgm.2013.12.004
10. Silva, I. T., Teixeira, M. R., Lang, K., Guimarães, T. R., Dudek, S. E., Durán, F. J., Ludwig, S., Caro, M. S. B., Schenkel, E. P., and Simões, C. M. O. (2013) Proliferative inhibition and apoptotic mechanism on human non-small-cell lung cancer (A549 cells) of a novel cucurbitacin from Wilbrandia ebracteata Cogn Int. J. Cancer Res. 9, 54-68 10.3923/ijcr.2013.54.68
11. Thoennissen, N. H., Iwanski, G. B., Doan, N. B., Okamoto, R., Lin, P., Abbassi, S., Song, J. H., Yin, D., Toh, M., Xie, W. D., Said, J. W., and Koeffler, P. (2009) Cucurbitacin B Induces Apoptosis by Inhibition of the JAK/STAT Pathway and Potentiates Antiproliferative Effects of Gemcitabine on Pancreatic Cancer Cells Cancer Res. 69, 5876-5884 10.1158/0008-5472.CAN-09-0536
12. Liu, T., Peng, H., Zhang, M., Deng, Y., and Wu, Z. (2010) Cucurbitacin B, a small molecule inhibitor of the Stat3 signaling pathway, enhances the chemosensitivity of laryngeal squamous cell carcinoma cells to cisplatin Eur. J. Pharmacol. 641, 15-22 10.1016/j.ejphar.2010.04.062
13. Chen, W., Leiter, A., Yin, D., Meiring, M., Louw, V., and Koeffler, H. P. (2010) Cucurbitacin B inhibits growth, arrest the cell cycle, and potentiates antiproliferative efficacy of cisplatin in cutaneous squamous cell carcinoma cell lines Int. J. Oncol. 37, 737-743 10.3892/ijo-00000723
14. Iwanski, G. B., Lee, D., En-Gal, S., Doan, N. B., Castor, B., Vogt, M., Toh, M., Bokemeyer, C., Said, J. W., Thoennissen, N. H., and Koeffler, P. (2010) Cucurbitacin B, a novel in vivo potentiator of gemcitabine with low toxicity in the treatment of pancreatic cancer Br. J. Pharmacol. 160, 998-1007 10.1111/j.1476-5381.2010.00741.x
15. Martinelli, E., Troiani, T., Morgillo, F., Rodolico, G., Vitagliano, D., Pia Morelli, M., Tuccillo, C., Vecchione, L., Capasso, A., Orditura, M., De Vita, F., Eckhardt, S. G., Santoro, M., Berrino, L., and Ciardiello, F. (2010) Synergistic antitumor activity of Sorafenib in combination with Epidermal Growth Factor Receptor inhibitors in colorectal and lung cancer cells Clin. Cancer Res. 16, 4990-5001 10.1158/1078-0432.CCR-10-0923
16. Li, C. J., Chu, C., Huang, L., Wang, M., Sheu, L., Yeh, J., and Hsu, H. (2012) Synergistic anticancer activity of triptolide combined with cisplatin enhances apoptosis in gastric cancer in vitro and in vivo Cancer Lett. 319, 203-213 10.1016/j.canlet.2012.01.006
17. Hatakeyama, Y., Kobayashi, K., Nagano, T., Tamura, D., Yamamoto, M., Tachihara, M., Kotani, Y., and Nishimura, Y. (2014) Synergistic effects of pemetrexed and amrubicin in non-small cell lung cancer cell lines Cancer Lett. 343, 74-79 10.1016/j.canlet.2013.09.019
18. Duangmano, S., Sae-lim, P., Suksamrarn, A., Patmasiriwat, P., and Domman, F. E. (2012) Cucurbitacin B causes increased radiation sensitivity of human breast cancer cells via G2/M cell cycle arrest J. Oncol. 2012, 1-8 10.1155/2012/601682
19. Chang, C.-J., Chiang, C.-H., Song, W.-S., Tsai, S.-K., Woung, L.-C., Chang, C.-H., Jeng, S.-Y., Tsay, C.-Y., Hsu, C.-C., Lee, H.-F., Huang, C.-S., Yung, M.-C., Liu, J.-H., and Lu, K.-H. (2012) Inhibition of phosphorylated STAT3 by cucurbitacin I enhances chemoradiosensitivity in medulloblastoma-derived cancer stem cells Childs Nerv. Syst. 28, 363-373 10.1007/s00381-011-1672-x
20. Aribi, A., Gery, S., Lee, D. H., Thoennissen, N. H., Thoennissen, G. B., Alvarez, R., Ho, Q., Lee, K., Doan, N. B., Chan, K. T., Toh, M., Said, J. W., and Koeffler, H. P. (2013) The triterpenoid cucurbitacin B augments the antiproliferative activity of chemotherapy in human breast cancer Int. J. Cancer 132, 2730-2737 10.1002/ijc.27950
21. Qu, Y., Wu, X., Yin, Y., Yang, Y., Ma, D., and Li, H. (2014) Antitumor activity of selective MEK 1/2 inhibitor AZD6244 in combination with PI3K/mTOR inhibitor BEZ235 in gefitinib-resistant NSCLC xenograft models J. Exp. Clin. Cancer Res. 33, 52 10.1186/1756-9966-33-52
22. Vichai, V. and Kirtikara, K. (2006) Sulforhodamine B colorimetric assay for cytotoxicity screening Nat. Protoc. 1, 1112-1116 10.1038/nprot.2006.179
23. Larsson, J., Gottfries, J., Muresan, S., and Backlund, A. (2007) ChemGPS-NP: Tuned for navigation in biologically relevant chemical space J. Nat. Prod. 70, 789-794 10.1021/np070002y
24. Felth, J., Rickardson, L., Rosén, J., Wickstrom, M., Fryknas, M., Lindskog, M., Bohlin, L., and Gullbo, J. (2009) Cytotoxic Effects of Cardiac Glycosides in Colon Cancer Cells, Alone and in Combination with Standard Chemotherapeutic Drugs J. Nat. Prod. 72, 1969-1974 10.1021/np900210m
25. Chou, T. C. (2006) Theoretical Basis, Experimental Design, and Computerized Simulation of Synergism and Antagonism in Drug Combination Studies Pharmacol. Rev. 58 (3) 621-681 10.1124/pr.58.3.10
26. Franken, N. A. P., Rodermond, H. M., Stap, J., Haveman, J., and Van Bree, C. (2006) Clonogenic assay of cells in vitro Nat. Protoc. 1, 2315-2319 10.1038/nprot.2006.339
27. Riccardi, C. and Nicoletti, I. (2006) Analysis of apoptosis by propidium iodide staining and flow cytometry Nat. Protoc. 1, 1458-1461 10.1038/nprot.2006.238
28. Selinummi, J., Seppala, J., Yli-Harja, O., and Puhakka, J. A. (2005) Software for quantification of labeled bacteria from digital microscope images by automated image analysis BioTechniques 39, 859-862 10.2144/000112018
29. Custodio, A., Méndez, M., and Provencio, M. (2012) Targeted therapies for advanced non-small-cell lung cancer: current status and future implications Cancer Treat. Rev. 38, 36-53 10.1016/j.ctrv.2011.04.001
30. Rosén, J., Lövgren, A., Kogej, T., Muresan, S., Gottfries, J., and Backlund, A. (2009) ChemGPS NPWeb: chemical space navigation online J. Comput.-Aided Mol. Des. 23, 253-259 10.1007/s10822-008-9255-y
31. Rosén, J., Rickardson, L., Backlund, A., Gullbo, J., Bohlin, L., Larsson, R., and Gottfries, J. (2009) ChemGPS-NP mapping of chemical compounds for prediction of anticancer mode of action QSAR Comb. Sci. 28, 436-446 10.1002/qsar.200810162
32. Lee, C., Lin, Y., Chang, F., Chen, G., Backlund, A., Yang, J., Chen, Y., and Wu, Y. (2012) Synthesis and biological evaluation of phenanthrenes as cytotoxic agents with pharmacophore modeling and ChemGPS-NP prediction as topo II inhibitors PLoS One 7, 1-14 10.1371/journal.pone.0037897
33. Kausar, H., Munagala, R., Bansal, S. S., Aqil, F., Vadhanan, M. V., and Gupta, R. C. (2013) Cucurbitacin B potently suppresses non-small-cell lung cancer growth: Identification of intracellular thiols as critical targets Cancer Lett. 332, 35-45 10.1016/j.canlet.2013.01.008
34. Guo, J., Wu, G., Bao, J., Hao, W., Lu, J., and Chen, X. (2014) Cucurbitacin B Induced ATM-Mediated DNA Damage Causes G2/M Cell Cycle Arrest in a ROS-Dependent Manner PLoS One 9, 1-12 10.1371/journal.pone.0088140
35. Andriani, F., Perego, P., and Roz, L. (2006) Increased sensitivity to cisplatin in non-small cell lung cancer cell lines after FHIT gene transfer Neoplasia 8, 9-17 10.1593/neo.05517
36. Kaufmann, S. H., Peereboom, D., Buckwalter, C. A., Swingen, P. A., Grochow, L. B., Donehower, R. C., and Rowinsky, E. K. (1996) Cytotoxic effects of topotecan combined with various anticancer agents in human cancer cell lines J. Natl. Cancer Inst. 88, 734-741 10.1093/jnci/88.11.734
37. Odonkor, C. A. and Achilefu, S. (2008) Differential activity of caspase-3 regulates susceptibility of lung and breast tumor cell lines to paclitaxel Open Biochem. J. 2, 121-128 10.2174/1874091X00802010121
38. Zhu, J. S., Ouyang, D. Y., Shi, Z. J., Xu, L. H., Zhang, Y. T., and He, X. H. (2012) Cucurbitacin B Induces Cell Cycle Arrest, Apoptosis and Autophagy Associated with G Actin Reduction and Persistent Activation of Cofilin in Jurkat Cells Pharmacology 89, 348-356 10.1159/000338757
39. Duangmano, S., Sae-lim, P., Suksamrarn, A., Patmasiriwat, P., and Domman, F. E. (2012) Cucurbitacin B causes increased radiation sensitivity of human breast cancer cells via G2/M cell cycle arrest J. Oncol. 2012, 1-8 10.1155/2012/601682
40. Yasuda, S., Yogosawa, S., Izutani, Y., Nakamura, Y., Watanabe, H., and Sakai, T. (2010) Cucurbitacin B induces G2 arrest and apoptosis via a reactive oxygen species-dependent mechanism in human colon adenocarcinoma SW480 cells Mol. Nutr. Food Res. 54, 559-565 10.1002/mnfr.200900165
41. Huang, W., Yang, J., Lin, M., Chen, P., Chiou, S., Chueh, F., Lan, Y., Pai, S., Tsuzuki, M., Ho, W., and Chung, J. (2012) Cucurbitacin E Induces G2/M Phase Arrest through STAT3/p53/p21 Signaling and Provokes Apoptosis via Fas/CD95 and Mitochondria-Dependent Pathways in Human Bladder Cancer T24 Cells Evid-Based Compl. Alt. 2012, 1-11 10.1155/2012/952762
42. Zhu, J. S., Ouyang, D. Y., Shi, Z. J., Xu, L. H., Zhang, Y. T., and He, X. H. (2012) Cucurbitacin B Induces Cell Cycle Arrest, Apoptosis and Autophagy Associated with G Actin Reduction and Persistent Activation of Cofilin in Jurkat Cells Pharmacology 89, 348-356 10.1159/000338757
43. Haritunians, T., Gueller, S., Zhang, L., Badr, R., Yin, D., Xing, H., Fung, M. C., and Koeffler, P. (2008) Cucurbitacin B induces differentiation, cell cycle arrest, and actin cytoskeletal alterations in myeloid leukemia cells Leuk. Res. 32, 1366-1373 10.1016/j.leukres.2008.01.019
44. Knecht, D. A., LaFleur, R. A., Kahsai, A. W., Argueta, C. E., Beshir, A. B., and Fenteany, G. (2010) Cucurbitacin I Inhibits Cell Motility by Indirectly Interfering with Actin Dynamics PLoS One 5, 1-11 10.1371/journal.pone.0014039
45. Zhang, T., Li, Y., Park, K. A., Byun, H. S., Won, M., Jeon, J., Lee, Y., Seok, J. H., Choi, S., Lee, S., Kim, J. M., Lee, J. H., Son, C. G., Lee, Z., Shen, H., and Hur, G. M. (2012) Cucurbitacin induces autophagy through mitochondrial ROS production which counteracts to limit caspase-dependent apoptosis Autophagy 8, 559-576 10.4161/auto.18867
46. Park, S., Kim, J., Chi, G., Kim, G., Chang, Y., Moon, S., Nam, S., Kim, W., Yoo, Y., and Choi, Y. (2012) Induction of apoptosis and autophagy by sodium selenite in A549 human lung carcinoma cells through generation of reactive oxygen species Toxicol. Lett. 212, 252-261 10.1016/j.toxlet.2012.06.007
47. Gabrielsen, M., Schuldt, M., Munro, J., Borucka, D., Cameron, J., Baugh, M., Mleczak, A., Lilla, S., Morrice, N., and Olson, M. (2013) Cucurbitacin covalent bonding to cysteine thiols: the filamentous-actin severing protein Cofilin1 as an exemplary target Cell Commun. Signaling 11, 58 10.1186/1478-811X-11-58
48. Blaschuk, O. W. and Devemy, E. (2009) Cadherins as novel targets for anticancer therapy Eur. J. Pharmacol. 625, 195-198 10.1016/j.ejphar.2009.05.033
49. Shanmugam, M. K., Nguyen, A. H., Kumar, A. P., Tan, B. K. H., and Sethi, G. (2012) Targeted inhibition of tumor proliferation, survival, and metastasis by pentacyclic triterpenoids: Potential role in prevention and therapy of cancer Cancer Lett. 320, 158-170 10.1016/j.canlet.2012.02.037
50. Zhang, T., Li, J., Dong, Y., Zhai, D., Lai, L., Dai, F., Deng, H., Chen, Y., Liu, M., and Yi, M. (2012) Cucurbitacin E inhibits breast tumor metastasis by suppressing cell migration and invasion Breast Cancer Res. Treat. 135, 445-458 10.1007/s10549-012-2175-5
51. Deryugina, E. I. and Quigley, J. P. (2006) Matrix Metalloproteinases and tumor metastasis Cancer Metastasis Rev. 25, 9-34 10.1007/s10555-006-7886-9
52. Muller, C. B., Barros, R. L. S., Castro, M. A. A., Lopes, F. M., Meurer, R. T., Roehe, A., Mazzini, G., Ulbrich-Kulczynski, J. N., Dal-Pizzol, F., Fernandes, M. C., Moreira, J. C. F., Xavier, L. L., and Klamt, F. (2011) Validation of cofilin-1 as a biomarker in non-small cell lung cancer: application of quantitative method in a retrospective cohort J. Cancer Res. Clin. Oncol. 137, 1309-1316 10.1007/s00432-011-1001-5
53. Nakashima, S., Matsuda, H., Kurume, A., Oda, Y., Nakamura, S., Yamashita, M., and Yoshikawa, M. (2010) Cucurbitacin E as a new inhibitor of cofilin phosphorylation in human leukemia U937 cells Bioorg. Med. Chem. Lett. 20, 2994-2997 10.1016/j.bmcl.2010.02.062
54. Zhang, Y.-T., Ouyang, D.-Y., Xu, L.-H., Zha, Q.-B., and He, X.-H. (2013) Formation of Cofilin-Actin rods following cucurbitacin-B-induced aggregation depends on slingshot Homolog1-Mediated Cofilin Hyperactivation J. Cell. Biochem. 114, 2415-2429 10.1002/jcb.24587
55. Siveen, K. S., Sikka, S., Surana, R., Dai, X., Zhang, J., Kumar, A. P., Tan, B. K. H., Sethi, G., and Bishayee, A. (2014) Targeting the Stat3 signaling pathway in cancer: Role of synthetic and natural inhibitors Biochim. Biophys. Acta, Rev. Cancer 1845, 136-154 10.1016/j.bbcan.2013.12.005