Suppression of ERCC1 and Rad51 expression through ERK1/2 inactivation is essential in emodin-mediated cytotoxicity in human non-small cell lung cancer cells

Biochemical Pharmacology

Volumn 79, Issue 4, 2010, Pages 655-664

  Ko, Jen Chung ^a   Su, Ying Jhen ^b   Lin, Szu Ting ^b   Jhan, Jhih Yuan ^b   Ciou, Shih Ci ^b   Cheng, Chao Min ^b   Lin, Yun Wei ^b  

^a Hsinchu Hospital   (Taiwan)

^b NATIONAL CHIAYI UNIVERSITY   (Taiwan)

Author keywords

Emodin; ERCC1; ERK1 2; Non small cell lung cancer; Rad51

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; EMODIN; EXCISION REPAIR CROSS COMPLEMENTING PROTEIN 1; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE KINASE 2; RAD51 PROTEIN;

ARTICLE; CELL VIABILITY; CONTROLLED STUDY; DOWN REGULATION; DRUG CYTOTOXICITY; ENZYME INACTIVATION; HUMAN; HUMAN CELL; LUNG NON SMALL CELL CANCER; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY;

CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; DNA REPAIR; DNA-BINDING PROTEINS; DOSE-RESPONSE RELATIONSHIP, DRUG; EMODIN; ENDONUCLEASES; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LUNG NEOPLASMS; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; RAD51 RECOMBINASE;

EID: 71349083599     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcp.2009.09.024     Document Type: Article

References (51)

1. Demirezer L.O., Kuruuzum-Uz A., Bergere I., Schiewe H.J., and Zeeck A. The structures of antioxidant and cytotoxic agents from natural source: anthraquinones and tannins from roots of Rumex patientia. Phytochemistry 58 (2001) 1213-1217
2. Kuo Y.C., Tsai W.J., Meng H.C., Chen W.P., Yang L.Y., and Lin C.Y. Immune reponses in human mesangial cells regulated by emodin from Polygonum hypoleucum Ohwi. Life Sci 68 (2001) 1271-1286
3. Su Y.T., Chang H.L., Shyue S.K., and Hsu S.L. Emodin induces apoptosis in human lung adenocarcinoma cells through a reactive oxygen species-dependent mitochondrial signaling pathway. Biochem Pharmacol 70 (2005) 229-241
4. Zhang L., Lau Y.K., Xi L., Hong R.L., Kim D.S., Chen C.F., et al. Tyrosine kinase inhibitors, emodin and its derivative repress HER-2/neu-induced cellular transformation and metastasis-associated properties. Oncogene 16 (1998) 2855-2863
5. Zhang L., Lau Y.K., Xia W., Hortobagyi G.N., and Hung M.C. Tyrosine kinase inhibitor emodin suppresses growth of HER-2/neu-overexpressing breast cancer cells in athymic mice and sensitizes these cells to the inhibitory effect of paclitaxel. Clin Cancer Res 5 (1999) 343-353
6. Chen Y.C., Shen S.C., Lee W.R., Hsu F.L., Lin H.Y., Ko C.H., et al. Emodin induces apoptosis in human promyeloleukemic HL-60 cells accompanied by activation of caspase 3 cascade but independent of reactive oxygen species production. Biochem Pharmacol 64 (2002) 1713-1724
7. Shieh D.E., Chen Y.Y., Yen M.H., Chiang L.C., and Lin C.C. Emodin-induced apoptosis through p53-dependent pathway in human hepatoma cells. Life Sci 74 (2004) 2279-2290
8. Wang C., Wu X., Chen M., Duan W., Sun L., Yan M., et al. Emodin induces apoptosis through caspase 3-dependent pathway in HK-2 cells. Toxicology 231 (2007) 120-128
9. Zhang L., Chang C.J., Bacus S.S., and Hung M.C. Suppressed transformation and induced differentiation of HER-2/neu-overexpressing breast cancer cells by emodin. Cancer Res 55 (1995) 3890-3896
10. Battistutta R., Sarno S., De Moliner E., Papinutto E., Zanotti G., and Pinna L.A. The replacement of ATP by the competitive inhibitor emodin induces conformational modifications in the catalytic site of protein kinase CK2. J Biol Chem 275 (2000) 29618-29622
11. de Laat W.L., Appeldoorn E., Jaspers N.G., and Hoeijmakers J.H. DNA structural elements required for ERCC1-XPF endonuclease activity. J Biol Chem 273 (1998) 7835-7842
12. Evans E., Moggs J.G., Hwang J.R., Egly J.M., and Wood R.D. Mechanism of open complex and dual incision formation by human nucleotide excision repair factors. Embo J 16 (1997) 6559-6573
13. Vogel U., Dybdahl M., Frentz G., and Nexo B.A. DNA repair capacity: inconsistency between effect of over-expression of five NER genes and the correlation to mRNA levels in primary lymphocytes. Mutat Res 461 (2000) 197-210
14. Lord R.V., Brabender J., Gandara D., Alberola V., Camps C., Domine M., et al. Low ERCC1 expression correlates with prolonged survival after cisplatin plus gemcitabine chemotherapy in non-small cell lung cancer. Clin Cancer Res 8 (2002) 2286-2291
15. Olaussen K.A., Dunant A., Fouret P., Brambilla E., Andre F., Haddad V., et al. DNA repair by ERCC1 in non-small-cell lung cancer and cisplatin-based adjuvant chemotherapy. N Engl J Med 355 (2006) 983-991
16. West S.C. Molecular views of recombination proteins and their control. Nat Rev Mol Cell Biol 4 (2003) 435-445
17. Xia S.J., Shammas M.A., and Shmookler Reis R.J. Elevated recombination in immortal human cells is mediated by HsRAD51 recombinase. Mol Cell Biol 17 (1997) 7151-7158
18. Raderschall E., Stout K., Freier S., Suckow V., Schweiger S., and Haaf T. Elevated levels of Rad51 recombination protein in tumor cells. Cancer Res 62 (2002) 219-225
19. Slupianek A., Hoser G., Majsterek I., Bronisz A., Malecki M., Blasiak J., et al. Fusion tyrosine kinases induce drug resistance by stimulation of homology-dependent recombination repair, prolongation of G(2)/M phase, and protection from apoptosis. Mol Cell Biol 22 (2002) 4189-4201
20. Bello V.E., Aloyz R.S., Christodoulopoulos G., and Panasci L.C. Homologous recombinational repair vis-a-vis chlorambucil resistance in chronic lymphocytic leukemia. Biochem Pharmacol 63 (2002) 1585-1588
21. Qiao G.B., Wu Y.L., Yang X.N., Zhong W.Z., Xie D., Guan X.Y., et al. High-level expression of Rad51 is an independent prognostic marker of survival in non-small-cell lung cancer patients. Br J Cancer 93 (2005) 137-143
22. Takenaka T., Yoshino I., Kouso H., Ohba T., Yohena T., Osoegawa A., et al. Combined evaluation of Rad51 and ERCC1 expressions for sensitivity to platinum agents in non-small cell lung cancer. Int J Cancer 121 (2007) 895-900
23. Ko J.C., Ciou S.C., Cheng C.M., Wang L.H., Hong J.H., Jheng M.Y., et al. Involvement of Rad51 in cytotoxicity induced by epidermal growth factor receptor inhibitor (gefitinib, IressaR) and chemotherapeutic agents in human lung cancer cells. Carcinogenesis 29 (2008) 1448-1458
24. Ohnishi T., Taki T., Hiraga S., Arita N., and Morita T. In vitro and in vivo potentiation of radiosensitivity of malignant gliomas by antisense inhibition of the RAD51 gene. Biochem Biophys Res Commun 245 (1998) 319-324
25. Landis SH, Murray T, Bolden S, Wingo PA. Cancer statistics, 1999. CA Cancer J Clin 1999; 49:8-31, 1.
26. Wachters F.M., Wong L.S., Timens W., Kampinga H.H., and Groen H.J. ERCC1, hRad51, and BRCA1 protein expression in relation to tumour response and survival of stage III/IV NSCLC patients treated with chemotherapy. Lung Cancer 50 (2005) 211-219
27. Ko J.C., Hong J.H., Wang L.H., Cheng C.M., Ciou S.C., Lin S.T., et al. Role of repair protein Rad51 in regulating the response to gefitinib in human non-small cell lung cancer cells. Mol Cancer Ther 7 (2008) 3632-3641
28. Shi Y.Q., Fukai T., Sakagami H., Kuroda J., Miyaoka R., Tamura M., et al. Cytotoxic and DNA damage-inducing activities of low molecular weight phenols from rhubarb. Anticancer Res 21 (2001) 2847-2853
29. Lin C.C., Chang C.H., Yang J.J., Namba T., and Hattori M. Hepatoprotective effects of emodin from Ventilago leiocarpa. J Ethnopharmacol 52 (1996) 107-111
30. Lee N.J., Choi J.H., Koo B.S., Ryu S.Y., Han Y.H., Lee S.I., et al. Antimutagenicity and cytotoxicity of the constituents from the aerial parts of Rumex acetosa. Biol Pharm Bull 28 (2005) 2158-2161
31. Zhou X., Song B., Jin L., Hu D., Diao C., Xu G., et al. Isolation and inhibitory activity against ERK phosphorylation of hydroxyanthraquinones from rhubarb. Bioorg Med Chem Lett 16 (2006) 563-568
32. Huang Q., Shen H.M., and Ong C.N. Inhibitory effect of emodin on tumor invasion through suppression of activator protein-1 and nuclear factor-kappaB. Biochem Pharmacol 68 (2004) 361-371
33. Friedberg E.C. How nucleotide excision repair protects against cancer. Nat Rev Cancer 1 (2001) 22-33
34. Reardon J.T., Vaisman A., Chaney S.G., and Sancar A. Efficient nucleotide excision repair of cisplatin, oxaliplatin, and Bis-aceto-ammine-dichloro-cyclohexylamine-platinum(IV) (JM216) platinum intrastrand DNA diadducts. Cancer Res 59 (1999) 3968-3971
35. Altaha R., Liang X., Yu J.J., and Reed E. Excision repair cross complementing-group 1: gene expression and platinum resistance. Int J Mol Med 14 (2004) 959-970
36. Lee K.B., Parker R.J., Bohr V., Cornelison T., and Reed E. Cisplatin sensitivity/resistance in UV repair-deficient Chinese hamster ovary cells of complementation groups 1 and 3. Carcinogenesis 14 (1993) 2177-2180
37. Selvakumaran M., Pisarcik D.A., Bao R., Yeung A.T., and Hamilton T.C. Enhanced cisplatin cytotoxicity by disturbing the nucleotide excision repair pathway in ovarian cancer cell lines. Cancer Res 63 (2003) 1311-1316
38. Andrieux L.O., Fautrel A., Bessard A., Guillouzo A., Baffet G., and Langouet S. GATA-1 is essential in EGF-mediated induction of nucleotide excision repair activity and ERCC1 expression through ERK2 in human hepatoma cells. Cancer Res 67 (2007) 2114-2123
39. Youn C.K., Kim M.H., Cho H.J., Kim H.B., Chang I.Y., Chung M.H., et al. Oncogenic H-Ras up-regulates expression of ERCC1 to protect cells from platinum-based anticancer agents. Cancer Res 64 (2004) 4849-4857
40. Yacoub A., McKinstry R., Hinman D., Chung T., Dent P., and Hagan M.P. Epidermal growth factor and ionizing radiation up-regulate the DNA repair genes XRCC1 and ERCC1 in DU145 and LNCaP prostate carcinoma through MAPK signaling. Radiat Res 159 (2003) 439-452
41. Yacoub A., Park J.S., Qiao L., Dent P., and Hagan M.P. MAPK dependence of DNA damage repair: ionizing radiation and the induction of expression of the DNA repair genes XRCC1 and ERCC1 in DU145 human prostate carcinoma cells in a MEK1/2 dependent fashion. Int J Radiat Biol 77 (2001) 1067-1078
42. Fu Z.Y., Han J.X., and Huang H.Y. Effects of emodin on gene expression profile in small cell lung cancer NCI-H446 cells. Chin Med J (Engl) 120 (2007) 1710-1715
43. Yang J., Li H., Chen Y.Y., Wang X.J., Shi G.Y., Hu Q.S., et al. Anthraquinones sensitize tumor cells to arsenic cytotoxicity in vitro and in vivo via reactive oxygen species-mediated dual regulation of apoptosis. Free Radic Biol Med 37 (2004) 2027-2041
44. Yi J., Yang J., He R., Gao F., Sang H., Tang X., et al. Emodin enhances arsenic trioxide-induced apoptosis via generation of reactive oxygen species and inhibition of survival signaling. Cancer Res 64 (2004) 108-116
45. Ravi R., and Bedi A. Sensitization of tumor cells to Apo2 ligand/TRAIL-induced apoptosis by inhibition of casein kinase II. Cancer Res 62 (2002) 4180-4185
46. Bertrand P., Lambert S., Joubert C., and Lopez B.S. Overexpression of mammalian Rad51 does not stimulate tumorigenesis while a dominant-negative Rad51 affects centrosome fragmentation, ploidy and stimulates tumorigenesis, in p53-defective CHO cells. Oncogene 22 (2003) 7587-7592
47. Parsels L.A., Morgan M.A., Tanska D.M., Parsels J.D., Palmer B.D., Booth R.J., et al. Gemcitabine sensitization by checkpoint kinase 1 inhibition correlates with inhibition of a Rad51 DNA damage response in pancreatic cancer cells. Mol Cancer Ther 8 (2009) 45-54
48. Arias-Lopez C., Lazaro-Trueba I., Kerr P., Lord C.J., Dexter T., Iravani M., et al. p53 modulates homologous recombination by transcriptional regulation of the RAD51 gene. EMBO Rep 7 (2006) 219-224
49. Lazaro-Trueba I., Arias C., and Silva A. Double bolt regulation of Rad51 by p53: a role for transcriptional repression. Cell Cycle 5 (2006) 1062-1065
50. Shen W.H., Balajee A.S., Wang J., Wu H., Eng C., Pandolfi P.P., et al. Essential role for nuclear PTEN in maintaining chromosomal integrity. Cell 128 (2007) 157-170
51. Bindra R.S., and Glazer P.M. Repression of RAD51 gene expression by E2F4/p130 complexes in hypoxia. Oncogene 26 (2007) 2048-2057