Synthetic genistein glycosides inhibiting egfr phosphorylation enhance the effect of radiation in HCT 116 colon cancer cells

Molecules

Volumn 19, Issue 11, 2014, Pages 18558-18573

  Gruca, Aleksra ^a,b   Krawczyk, Zdzisław ^b   Szeja, Wiesław ^a   Grynkiewicz, Grzegorz ^c   Rusin, Aleksra ^b  

^a SILESIAN UNIVERSITY OF TECHNOLOGY   (Poland)

^b INSTITUTE OF ONCOLOGY   (Poland)

^c INDUSTRIAL CHEMISTRY RESEARCH INSTITUTE   (Poland)

Author keywords

Epidermal growth factor receptor inhibition; Genistein glycoconjugates; Radiosensitization; Radiotherapy

Indexed keywords

ANTINEOPLASTIC AGENT; EGFR PROTEIN, HUMAN; EPIDERMAL GROWTH FACTOR RECEPTOR; GENISTEIN; GLYCOSIDE; RADIOSENSITIZING AGENT; TUMOR PROTEIN;

CHEMISTRY; COLONIC NEOPLASMS; DOSE RESPONSE; DRUG EFFECTS; HUMAN; IONIZING RADIATION; METABOLISM; PATHOLOGY; PHOSPHORYLATION; RADIATION RESPONSE; SYNTHESIS; TUMOR CELL LINE;

ANTICARCINOGENIC AGENTS; CELL LINE, TUMOR; COLONIC NEOPLASMS; DOSE-RESPONSE RELATIONSHIP, DRUG; DOSE-RESPONSE RELATIONSHIP, RADIATION; GENISTEIN; GLYCOSIDES; HUMANS; NEOPLASM PROTEINS; PHOSPHORYLATION; RADIATION, IONIZING; RADIATION-SENSITIZING AGENTS; RECEPTOR, EPIDERMAL GROWTH FACTOR;

EID: 84911940791     PISSN: None     EISSN: 14203049     Source Type: Journal    
DOI: 10.3390/molecules191118558     Document Type: Article

References (55)

1. Ono, M.; Kuwano, M. Molecular mechanisms of epidermal growth factor receptor (EGFR) activation and response to gefitinib and other EGFR-targeting drugs. Clin. Cancer Res. 2006, 12, 7242-7251.
2. Thariat, J.; Milas, L.; Ang, K.K. Integrating radiotherapy with epidermal growth factor receptor antagonists and other molecular therapeutics for the treatment of head and neck cancer. Int. J. Rad. Oncol. Biol. Phys. 2007, 69, 974-984.
3. Nicholson, R.I.; Gee, J.M.; Harper, M.E. EGFR and cancer prognosis. Eur. J. Cancer 2001, 37 (Suppl. 4), S9-S15.
4. Baiocchi, G.; Lopes, A.; Coudry, R.A.; Rossi, B.M.; Soares, F.A.; Aguiar, S.; Guimaraes, G.C.; Ferreira, F.O.; Nakagawa, W.T. ErbB family immunohistochemical expression in colorectal cancer patients with higher risk of recurrence after radical surgery. Int. J. Colorectal Dis. 2009, 24, 1059-1068.
5. Gravalos, C.; Jimeno, A. HER2 in gastric cancer: A new prognostic factor and a novel therapeutic target. Ann. Oncol. 2008, 19, 1523-1529.
6. Bonner, J.A.; Harari, P.M.; Giralt, J.; Azarnia, N.; Shin, D.M.; Cohen, R.B.; Jones, C.U.; Sur, R.; Raben, D.; Jassem, J.; et al. Radiotherapy plus cetuximab for squamous-cell carcinoma of the head and neck. N. Engl. J. Med. 2006, 354, 567-578.
7. Cappuzzo, F.; Ciuleanu, T.; Stelmakh, L.; Cicenas, S.; Szczesna, A.; Juhasz, E.; Esteban, E.; Molinier, O.; Brugger, W.; Melezinek, I.; et al. Erlotinib as maintenance treatment in advanced non-small-cell lung cancer: A multicentre, randomised, placebo-controlled phase 3 study. Lancet Oncol. 2010, 11, 521-529.
8. Herbst, R.S.; Sun, Y.; Eberhardt, W.E.; Germonpre, P.; Saijo, N.; Zhou, C.; Wang, J.; Li, L.; Kabbinavar, F.; Ichinose, Y.; et al. Vandetanib plus docetaxel versus docetaxel as second-line treatment for patients with advanced non-small-cell lung cancer (ZODIAC): A double-blind, randomised, phase 3 trial. Lancet Oncol. 2010, 11, 619-626.
9. Krause, M.; Gurtner, K.; Deuse, Y.; Baumann, M. Heterogeneity of tumour response to combined radiotherapy and EGFR inhibitors: differences between antibodies and TK inhibitors. Int. J. Radiat. Biol. 2009, 85, 943-954.
10. Akiyama, T.; Ishida, J.; Nakagawa, S.; Ogawara, H.; Watanabe, S.; Itoh, N.; Shibuya, M.; Fukami, Y. Genistein, a specific inhibitor of tyrosine-specific protein kinases. J. Biol. Chem. 1987, 262, 5592-5595.
11. Yan, G.R.; Xiao, C.L.; He, G.W.; Yin, X.F.; Chen, N.P.; Cao, Y.; He, Q.Y. Global phosphoproteomic effects of natural tyrosine kinase inhibitor, genistein, on signaling pathways. Proteomics 2010, 10, 976-986.
12. Park, S.J.; Kim, M.J.; Kim, Y.K.; Kim, S.M.; Park, J.Y.; Myoung, H. Combined cetuximab and genistein treatment shows additive anti-cancer effect on oral squamous cell carcinoma. Cancer Lett. 2010, 292, 54-63.
13. Zhu, H.; Cheng, H.; Ren, Y.; Liu, Z.G.; Zhang, Y.F.; Luo, B.D. Synergistic inhibitory effects by the combination of gefitinib and genistein on NSCLC with acquired drug-resistance in vitro and in vivo. Mol. Biol. Rep. 2012, 39, 4971-4979.
14. Gadgeel, S.M.; Ali, S.; Philip, P.A.; Wozniak, A.; Sarkar, F.H. Genistein enhances the effect of epidermal growth factor receptor tyrosine kinase inhibitors and inhibits nuclear factor kappa B in nonsmall cell lung cancer cell lines. Cancer 2009, 115, 2165-2176.
15. Hillman, G.G.; Forman, J.D.; Kucuk, O.; Yudelev, M.; Maughan, R.L.; Rubio, J.; Layer, A.; Tekyi-Mensah, S.; Abrams, J.; Sarkar, F.H. Genistein potentiates the radiation effect on prostate carcinoma cells. Clin. Cancer Res. 2001, 7, 382-390.
16. Raffoul, J.J.; Wang, Y.; Kucuk, O.; Forman, J.D.; Sarkar, F.H.; Hillman, G.G. Genistein inhibits radiation-induced activation of NF-kappaB in prostate cancer cells promoting apoptosis and G2/M cell cycle arrest. BMC Cancer 2006, 6, doi:10.1186/1471-2407-6-107.
17. Raffoul, J.J.; Banerjee, S.; Che, M.; Knoll, Z.E.; Doerge, D.R.; Abrams, J.; Kucuk, O.; Sarkar, F.H.; Hillman, G.G. Soy isoflavones enhance radiotherapy in a metastatic prostate cancer model. Int. J. Cancer 2007, 120, 2491-2498.
18. Yashar, C.M.; Spanos, W.J.; Taylor, D.D.; Gercel-Taylor, C. Potentiation of the radiation effect with genistein in cervical cancer cells. Gynecol. Oncol. 2005, 99, 199-205.
19. Para, A.E.; Bezjak, A.; Yeung, I.W.; van Dyk, J.; Hill, R.P. Effects of genistein following fractionated lung irradiation in mice. Radiother. Oncol. 2009, 92, 500-510.
20. Day, R.M.; Barshishat-Kupper, M.; Mog, S.R.; Mccart, E.A.; Prasanna, P.G.; Davis, T.A.; Landauer, M.R. Genistein protects against biomarkers of delayed lung sequelae in mice surviving high-dose total body irradiation. J. Radiat. Res. 2008, 49, 361-372.
21. Singh, V.K.; Grace, M.B.; Parekh, V.I.; Whitnall, M.H.; Landauer, M.R. Effects of genistein administration on cytokine induction in whole-body gamma irradiated mice. Int. Immunopharmacol. 2009, 9, 1401-1410.
22. Booth, C.; Hargreaves, D.F.; Hadfield, J.A.; Mcgown, A.T.; Potten, C.S. Isoflavones inhibit intestinal epithelial cell proliferation and induce apoptosis in vitro. Br. J. Cancer 1999, 80, 1550-1557.
23. Gargala, G.; Baishanbo, A.; Favennec, L.; Francois, A.; Ballet, J.J.; Rossignol, J.F. Inhibitory activities of epidermal growth factor receptor tyrosine kinase-targeted dihydroxyisoflavone and trihydroxydeoxybenzoin derivatives on Sarcocystis neurona, Neospora caninum, and Cryptosporidium parvum development. Antimicrob. Agents Chemother. 2005, 49, 4628-4634.
24. Rusin, A.; Krawczyk, Z.; Grynkiewicz, G.; Gogler, A.; Zawisza-Puchalka, J.; Szeja, W. Synthetic derivatives of genistein, their properties and possible applications. Acta Biochem. Pol. 2010, 57, 23-34.
25. Rusin, A.; Gogler, A.; Glowala-Kosinska, M.; Bochenek, D.; Gruca, A.; Grynkiewicz, G.; Zawisza, J.; Szeja, W.; Krawczyk, Z. Unsaturated genistein disaccharide glycoside as a novel agent affecting microtubules. Bioorg. Med. Chem. Lett. 2009, 19, 4939-4943.
26. Rusin, A.; Zawisza-Puchalka, J.; Kujawa, K.; Gogler-Piglowska, A.; Wietrzyk, J.; Switalska, M.; Glowala-Kosinska, M.; Gruca, A.; Szeja, W.; Krawczyk, Z.; et al. Synthetic conjugates of genistein affecting proliferation and mitosis of cancer cells. Bioorg. Med. Chem. 2011, 19, 295-305.
27. Ahmed, A.A.; Goldsmith, J.; Fokt, I.; Le, X.F.; Krzysko, K.A.; Lesyng, B.; Bast, R.C.; Priebe, W. A genistein derivative, ITB-301, induces microtubule depolymerization and mitotic arrest in multidrug-resistant ovarian cancer. Cancer Chemother. Pharm. 2011, 68, 1033-1044.
28. Gogler-Piglowska, A.; Rusin, A.; Bochenek, D.; Krawczyk, Z. Aneugenic effects of the genistein glycosidic derivative substituted at C7 with the unsaturated disaccharide. Cell Biol. Toxicol. 2012, 28, 331-342.
29. Rusin, A.; Chrubasik, M.; Papaj, K.; Grynkiewicz, G.; Szeja, W. C-Glycosidic genistein conjugates and their antiproliferative activity. J. Chem. 2013, 2013, doi:10.1155/2013/951392.
30. Sawhney, R.S.; Zhou, G.H.K.; Humphrey, L.E.; Ghosh, P.; Kreisberg, J.I.; Brattain, M.G. Differences in sensitivity of biological functions mediated by epidermal growth factor receptor activation with respect to endogenous and exogenous ligands. J. Biol. Chem. 2002, 277, 75-86.
31. Akimoto, T.; Nonaka, T.; Ishikawa, H.; Sakurai, H.; Saitoh, J.; Takahashi, T.; Mitsuhashi, N. Genistein, a tyrosine kinase inhibitor, enhanced radiosensitivity in human esophageal cancer cell lines in vitro: Possible involvement of inhibition of survival signal transduction pathways. Int. J. Radiat. Oncol. 2001, 50, 195-201.
32. Toillon, R.A.; Magne, N.; Laios, I.; Lacroix, M.; Duvillier, H.; Lagneaux, L.; Devriendt, D.; van Houtte, P.; Leclercq, G. Interaction between estrogen receptor alpha, ionizing radiation and (anti-) estrogens in breast cancer cells. Breast Cancer Res. Treat. 2005, 93, 207-215.
33. st ed; Springer: New York, NY, USA, 2010; p. 494.
34. Donnem, T.; Al-Shibli, K.; Al-Saad, S.; Busund, L.T.; Bremnes, R.M. Prognostic impact of fibroblast growth factor 2 in non-small cell lung cancer coexpression with VEGFR-3 and PDGF-B predicts poor survival. J. Thorac. Oncol. 2009, 4, 578-585.
35. Jakobkiewicz-Banecka, J.; Piotrowska, E.; Narajczyk, M.; Baranska, S.; Wegrzyn, G. Genistein-mediated inhibition of glycosaminoglycan synthesis, which corrects storage in cells of patients suffering from mucopolysaccharidoses, acts by influencing an epidermal growth factor-dependent pathway. J. Biomed. Sci. 2009, 2, 16-26.
36. lck protein tyrosine kinase: A classical/quantum chemical approach. Quant. Struct.-Act. Relat. 1998, 17, 7-13.
37. Oblak, M.; Randic, M.; Solmajer, T. Quantitative structure-activity relationship of flavonoid analogues. 3. Inhibition of p56lck protein tyrosine kinase. J. Chem. Inf. Comput. Sci. 2000, 40, 994-1001.
38. Ogawara, H.; Akiyama, T.; Watanabe, S.; Ito, N.; Kobori, M.; Seoda, Y. Inhibition of tyrosine protein-kinase activity by synthetic isoflavones and flavones. J. Antibiot. 1989, 42, 340-343.
39. Batzer, A.G.; Rotin, D.; Urena, J.M.; Skolnik, E.Y.; Schlessinger, J. Hierarchy of binding-sites for Grb2 and Shc on the epidermal growth-factor receptor. Mol. Cell. Biol. 1994, 14, 5192-5201.
40. Rojas, M.; Yao, S.Y.; Lin, Y.Z. Controlling epidermal growth factor (EGF)-stimulated ras activation in intact cells by a cell-permeable peptide mimicking phosphorylated EGF receptor. J. Biol. Chem. 1996, 271, 27456-27461.
41. Blenis, J. Signal-transduction via the MAP kinases: Proceed at your own Rsk. Proc. Natl. Acad. Sci. USA 1993, 90, 5889-5892.
42. Ravichandran, K.S. Signaling via Shc family adapter proteins. Oncogene 2001, 20, 6322-6330.
43. Yacoub, A.; Miller, A.; Caron, R.W.; Qiao, L.; Curiel, D.A.; Fisher, P.B.; Hagan, M.P.; Grant, S.; Dent, P. Radiotherapy-induced signal transduction. Endocr.-Related Cancer 2006, 13, S99-S114.
44. Tai, C.J.; Chang, C.C.; Jiang, M.C.; Yeh, C.M.; Su, T.C.; Wu, P.R.; Chen, C.J.; Yeh, K.T.; Lin, S.H.; Chen, H.C. Clinical-pathological correlation of K-Ras mutation and ERK phosphorylation in colorectal cancer. Pol. J. Pathol. 2012, 63, 93-100.
45. Raponi, M.; Winkler, H.; Dracopoli, N.C. KRAS mutations predict response to EGFR inhibitors. Curr. Opin. Pharmacol. 2008, 8, 413-418.
46. Linardou, H.; Dahabreh, I.J.; Kanaloupiti, D.; Siannis, F.; Bafaloukos, D.; Kosmidis, P.; Papadimitriou, C.A.; Murray, S. Assessment of somatic k-RAS mutations as a mechanism associated with resistance to EGFR-targeted agents: a systematic review and meta-analysis of studies in advanced non-small-cell lung cancer and metastatic colorectal cancer. Lancet Oncol. 2008, 9, 962-972.
47. Jutten, B.; Dubois, L.; Li, Y.N.; Aerts, H.; Wouters, B.G.; Lambin, P.; Theys, J.; Lammering, G. Binding of cetuximab to the EGFRvIII deletion mutant and its biological consequences in malignant glioma cells. Radiother. Oncol. 2009, 92, 393-398.
48. Wheeler, S.E.; Suzuki, S.; Thomas, S.M.; Sen, M.; Leeman-Neill, R.J.; Chiosea, S.I.; Kuan, C.T.; Bigner, D.D.; Gooding, W.E.; Lai, S.Y.; et al . Epidermal growth factor receptor variant III mediates head and neck cancer cell invasion via STAT3 activation. Oncogene 2010, 29, 5135-5145.
49. Huang, S.; Armstrong, E.A.; Benavente, S.; Chinnaiyan, P.; Harari, P.M. Dual-agent molecular targeting of the epidermal growth factor receptor (EGFR): Combining anti-EGFR antibody with tyrosine kinase inhibitor. Cancer Res. 2004, 64, 5355-5362.
50. Huether, A.; Hopfner, M.; Baradari, V.; Schuppan, D.; Scherubl, H. EGFR blockade by cetuximab alone or as combination therapy for growth control of hepatocellular cancer. Biochem. Pharmacol. 2005, 70, 1568-1578.
51. Nakamura, H.; Takamori, S.; Fujii, T.; Ono, M.; Yamana, H.; Kuwano, M.; Shirouzu, K. Cooperative cell-growth inhibition by combination treatment with ZD1839 (Iressa) and trastuzumab (Herceptin) in non-small-cell lung cancer. Cancer Lett. 2005, 230, 33-46.
52. Ju, Y.H.; Allred, C.D.; Allred, K.F.; Karko, K.L.; Doerge, D.R.; Helferich, W.G. Physiological concentrations of dietary genistein dose-dependently stimulate growth of estrogen-dependent human breast cancer (MCF-7) tumors implanted in athymic nude mice. J. Nutr. 2001, 131, 2957-2962.
53. Nakamura, H.; Wang, Y.W.; Kurita, T.; Adomat, H.; Cunha, G.R.; Wang, Y.Z. Genistein increases epidermal growth factor receptor signaling and promotes tumor progression in advanced human prostate cancer. PLoS One 2011, 6, doi:10.1371/journal.pone.0020034.
54. Qi, W.T.; Weber, C.R.; Wasland, K.; Savkovic, S.D. Genistein inhibits proliferation of colon cancer cells by attenuating a negative effect of epidermal growth factor on tumor suppressor FOXO3 activity. BMC Cancer 2011, 11, doi:10.1186/1471-2407-11-219.
55. Chou, T.C.; Talalay, P. Analysis of combined drug effects: A new look at a very old problem. Trends Pharmacol. Sci. 1983, 4, 450-454.