Epidermal growth factor and ionizing radiation up-regulate the DNA repair genes XRCC1 and ERCC1 in DU145 and LNCaP prostate carcinoma through MAPK signaling

Radiation Research

Volumn 159, Issue 4, 2003, Pages 439-452

  Yacoub, Adly ^a   McKinstry, Robert ^a   Hinman, Darin ^a   Chung, Theodore ^a   Denta, Paul ^a   Hagan, Michael P ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COBALT 60; EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; TYRPHOSTIN;

ARTICLE; CANCER CELL; COBALT THERAPY; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; ENZYME ACTIVITY; GAMMA IRRADIATION; HUMAN; HUMAN CELL; IONIZING RADIATION; MALE; PRIORITY JOURNAL; PROSTATE CARCINOMA; SIGNAL TRANSDUCTION; UPREGULATION;

ADENOCARCINOMA; AUTOCRINE COMMUNICATION; COBALT RADIOISOTOPES; DNA DAMAGE; DNA REPAIR; DNA-BINDING PROTEINS; ENDONUCLEASES; ENZYME INHIBITORS; EPIDERMAL GROWTH FACTOR; FLAVONOIDS; GAMMA RAYS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MALE; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MITOGEN-ACTIVATED PROTEIN KINASES; NEOPLASM PROTEINS; PROSTATIC NEOPLASMS; PROTEIN BIOSYNTHESIS; PROTEINS; RECEPTOR, EPIDERMAL GROWTH FACTOR; TUMOR CELLS, CULTURED; TYRPHOSTINS;

EID: 0037382902     PISSN: 00337587     EISSN: None     Source Type: Journal    
DOI: 10.1667/0033-7587(2003)159[0439:EGFAIR]2.0.CO;2     Document Type: Article

References (71)

1. A. W. Grasso, D. Wen, C. M. Miller, J. S. Rhim, T. G. Pretlow and H. J. Kung, ErbB kinases and NDF signaling in human prostate cancer cells. Oncogene 15, 2705-2716 (1997).
2. S. H. Yuspa, The pathogenesis of squamous cell cancer: Lessons learned from studies of skin carcinogenesis - thirty-third G. H. A. Clowes Memorial Award Lecture. Cancer Res. 54, 1178-1189 (1994).
3. D. S. Salomon, R. Brandt, E Ciardiello and N. Normanno, Epidermal growth factor-related peptides and their receptors in human malignancies. Crit. Rev. Oncol. Hematol. 19, 183-232 (1995).
4. N. Bruchovsky, P. S. Rennie, A. J. Coldman, S. L. Goldenberg, M. To and D. Lawson, The effects of androgen withdrawal on the stem cell composition of Shionogi carcinoma. Cancer Res. 50, 2275-2282 (1990).
5. J. M. Kozlowski, W. J. Ellis and J. M. Grayhack, Advanced prostatic carcinoma: Early versus late endocrine therapy. Urol. Clin. N. Am. 18, 15-24 (1991).
6. Z. Culig, A. Hobisch, M. V. Cronauer, C. Radmayr, J. Trapman, A. Hittmair, G. Bartsch and H. Klocker, Androgen receptor activation in prostatic tumor cell lines by insulin-like growth factor-I, keratinocyte growth factor, and epidermal growth factor. Cancer Res. 54, 5474-5478 (1994).
7. H. Riedel, S. Massoglia, J. Schlessinger and A. Ullrich, Ligand activation of overexpressed epidermal growth factor receptors transforms NIH 3T3 mouse fibroblasts. Proc. Natl. Acad. Sci. USA 5, 1477-1481 (1988).
8. V. L. Bae, S. J. Maygarden, S. C. Strom, J. Chen and J. L. Ware, Selection of tumorigenic sublines of immortalized human prostate epithelial cells by growth in nude mice. Proc. Am. Assoc. Cancer Res. 34, 337 (1993). [Abstract]
9. V. L. Bae, C. K. Jackson-Cook, A. R. Brothman, S. J. Maygarden and J. L. Ware, Tumorigenicity of SV40 T antigen immortalized human prostate epithelial cells: Association with decreased epidermal growth factor receptor (EGFR) expression. Int. J. Cancer 58, 721-729 (1994).
10. V. L. Bae, C. K. Jackson-Cook, S. J. Maygarden, S. R. Plymate, J. Chen and J. L. Ware, Metastatic sublines of an SV40 large T antigen immortalized human prostate epithelial cell line. Prostate 34, 275-282 (1998).
11. P. O. Hackel, E. Zwick, N. Prenzel and A. Ullrich, Epidermal growth factor receptors: critical mediators of multiple receptor pathways. Curr. Opin. Cell Biol. 11, 184-189 (1999).
12. S. J. Taylor and D. Shalloway, Cell cycle-dependent activation of Ras. Curr. Biol. 6, 1621-1627 (1996).
13. 1 phase. Biochem. J. 326, 61-68 (1997).
14. T. H. Holmstrom, I. Schmitz, T. S. Soderstrom, M. Poukkula, V. L. Johnson, S. C. Chow, P. H. Krammer and J. E. Eriksson, MAPK/ERK signaling in activated T cells inhibits CD95/Fas-mediated apoptosis downstream of DISC assembly. EMBO J. 19, 5418-5428 (2000).
15. 1 cell cycle arrest and apoptosis in tumor cells in which the pathway is constitutively activated: up-regulation of p27(Kipl). J. Biol. Chem. 276, 2686-2692 (2001).
16. K. Kitta, R. M. Day, T. Ikeda and Y. J. Suzuki, Hepatocyte growth factor protects cardiac myocytes against oxidative stress-induced apoptosis. Free Radic. Biol. Med. 31, 902-910 (2001).
17. Z. Wang, C. Jiang, H. Ganther and J. Lu, Antimitogenic and proapoptotic activities of methylseleninic acid in vascular endothelial cells and associated effects on PI3K-AKT, ERK, JNK and p38 MAPK signaling. Cancer Res. 61, 7171-7178 (2001).
18. G. Pages, P. Lenormand, G. L'Allemain, J. C. Chambard, S. Meloche and J. Pouyssegur, Mitogen-activated protein kinases p42mapk and p44mapk are required for fibroblast proliferation. Proc. Natl. Acad. Sci. USA 90, 8319-8323 (1993).
19. A. Brunet, D. Roux, P. Lenormand, S. Dowd, S. Keyse and J. Pouyssegur, Nuclear translocation of p42/p44 mitogen-activated protein kinase is required for growth factor-induced gene expression and cell cycle entry. EMBO J. 18, 664-674 (1999).
20. J. I. Chao and J. L. Yang, Opposite roles of ERK and p38 mitogen-activated protein kinases in cadmium-induced genotoxicity and mitotic arrest. Chem. Res. Toxicol. 14, 1193-1202 (2001).
21. N. J. Holbrook, Y. Liu and A. J. Fornace, Jr., Signaling events controlling the molecular response to genotoxic stress. EXS 77, 273-288 (1996).
22. S. Kharbanda, P. Pandey, T. Yamauchi, S. Kumar, M. Kaneki, V. Kumar, A. Bharti, Z. M. Yuan, L. Ghanem and D. Kufe, Activation of MEK kinase 1 by the c-Ab1 protein tyrosine kinase in response to DNA damage. Mol. Cell. Biol. 20, 4979-4989 (2000).
23. J. T. Lett, Experimental models for cellular radiation targets: LET, RBE and radioprotectors. Adv. Space Res. 18, 31-40 (1996).
24. C. L. Limoli, B. Ponnaiya, J. J. Corcoran, E. Giedzinski, M. I. Kaplan, A. Hartmann and W. F. Morgan, Genomic instability induced by high and low LET ionizing radiation. Adv. Space Res. 25, 2107-2117 (2000).
25. S. A. Roberts and J. H. Hendry, A realistic closed-form radiobiological model of clinical tumor-control data incorporating intertumor heterogeneity. Int. J. Radiat. Oncol. Biol. Phys. 41, 689-699 (1998).
26. T Theron, J. Slabbert, A. Serafin and L. Bohm, The merits of cell kinetic parameters for the assessment of intrinsic cellular radiosensitivity to photon and high linear energy transfer neutron irradiation. Int. J. Radiat. Oncol. Biol. Phys. 37, 423-428 (1997).
27. N. Moghal and P. W. Sternberg, Multiple positive and negative regulators of signaling by the EGF-receptor. Curr. Opin. Cell. Biol. 2, 190-196 (1999).
28. P. Dent, D. B. Reardon, J. S. Park, G. Bowers, C. Logsdon, K. Valerie and R. Schmidt-Ullrich, Radiation-induced release of transforming growth factor alpha activates the epidermal growth factor receptor and mitogen-activated protein kinase pathway in carcinoma cells, leading to increased proliferation and protection from radiation-induced cell death. Mol. Biol. Cell. 10, 2493-2506 (1999).
29. V. L. Kumar, P. K. Majumder, S. Gujral and V. Kumar, Comparative analysis of epidermal growth factor receptor mRNA levels in normal, benign hyperplastic and carcinomatous prostate. Cancer Lett. 134, 177-180 (1998).
30. C. F. Yu, B. Roshan, Z. X. Liu and L. G. Cantley, Erk regulates the hepatocyte growth factor-mediated interaction of gab1 and the phosphatidylinositol 3-kinase. J. Biol. Chem. 276, 32552-32558 (2001).
31. X. Wu, Z. Fan, H. Masui, N. Rosen and J. Mendelsohn, Apoptosis induced by an anti-epidermal growth factor receptor monoclonal antibody in a human colorectal carcinoma cell line and its delay by insulin. J. Clin. Invest. 95, 1897-1905 (1995).
32. J. Baselga, L. Norton, H. Masui, A. Pandiella, K. Coplan, W. M. Miller, Jr. and J. Mendelsohn, Antitumor effects of doxorubicin in combination with anti-epidermal growth factor receptor monoclonal antibodies. J. Natl. Cancer Inst. 85, 1327-1333 (1993).
33. Z. Fan, Y. Lu, X. Wu, A. DeBlasio, A. Koff and J. Mendelsohn, Prolonged induction of p21Cip1/WAF1/CDK2/PCNA complex by epidermal growth factor receptor activation mediates ligand-induced A431 cell growth inhibition. J. Cell Biol. 1, 235-242 (1995).
34. Y. Tsukada, K. Miyazawa and N. Kitamura, High intensity ERK signal mediates hepatocyte growth factor-induced proliferation inhibition of the human hepatocellular carcinoma cell line HepG2. J. Biol. Chem. 276, 40968-40976 (2001).
35. J. Mendelsohn and Z. Fan, Epidermal growth factor receptor family and chemosensitization. J. Natl. Cancer Inst. 89, 341-343 (1997).
36. T. Akimoto, N. R. Hunter, L. Buchmiller, K. Mason, K. K. Ang and L. Milas, Inverse relationship between epidermal growth factor receptor expression and radiocurability of murine carcinomas. Clin. Cancer Res. 10, 2884-2984 (1999).
37. H. Xie, T. Turner, M. H. Wang, R. K. Singh, G. P. Siegal and A. Wells, In vitro invasiveness of DU-145 human prostate carcinoma cells is modulated by EGF receptor-mediated signals. Clin. Exp. Metastasis 6, 407-419 (1995).
38. R. K. Schmidt-Ullrich, P. Dent, S. Grant, R. B. Mikkelsen and K. Valerie, Signal transduction and cellular radiation responses. Radiat. Res. 153, 245-257 (2000).
39. G. Bowers, D. Reardon, T Hewitt, P. Dent, R. B. Mikkelsen, K. Valerie, G. Lammering, C. Amir and R. K. Schmidt-Ullrich, The relative role of ErbB 1-4 receptor tyrosine kinases in radiation signal transduction responses of human carcinoma cells. Oncogene 11, 1388-1397 (2001).
40. K. K. Khanna and S. P. Jackson, DNA double-strand breaks: Signaling, repair and the cancer connection. Nat. Genet. 27, 247-254 (2001).
41. L. Heron-Milhavet, M. Karas, C. M. Goldsmith, B. J. Baum and D. LeRoith, Insulin-like growth factor-I (IGF-I) receptor activation rescues UV-damaged cells through a p38 signaling pathway. Potential role of the IGF-I receptor in DNA repair. J. Biol. Chem. 276, 18185-18192 (2001).
42. X. L. You, L. Yen, N. Zeng-Rong, A. E. Al Moustafa and M. A. Alaoui-Jamali, Dual effect of erbB-2 depletion on the regulation of DNA repair and cell cycle mechanisms in non-small cell lung cancer cells. Oncogene 17, 3177-3186 (1998).
43. B. Gao, X. Shen, G. Kunos, Q. Meng, I. D. Goldberg, E. M. Rosen and S. Fan, Constitutive activation of JAK-STAT3 signaling by BRCA1 in human prostate cancer cells. FEBS Lett. 488, 179-184 (2001).
44. I. Boldogh, C. V. Ramana, Z. Chen, T. Biswas, T. K. Hazra, S. Grosch, T. Grombacher, S. Mitra and B. Kaina, Regulation of expression of the DNA repair gene O6-methylguanine-DNA methyltransferase via protein kinase C-mediated signaling. Cancer Res. 58, 3950-3956 (1998).
45. C. H. Lee, K. Sidik and K. V. Chin, Role of cAMP-dependent protein kinase in the regulation of DNA repair. Cancer Lett. 169, 51-58 (2001).
46. C. Petit-Frere, P. H. Clingen, M. Grewe, J. Krutmann, L. Roza, C. F. Arlett and M. H. Green, Induction of interleukin-6 production by ultraviolet radiation in normal human epidermal keratinocytes and in a human keratinocyte cell line is mediated by DNA damage. J. Invest. Dermatol. 111, 354-359 (1998).
47. 2/M-phase arrest. Radiat. Res. 153, 371-383 (2000).
48. A. Yacoub, J. S. Park, Q. Liang, P. Dent and M. P. Hagan, Ionizing radiation induces expression of the DNA repair XRCC1 and ERCC1 in DU-145 human prostate carcinoma cells in MEK1/2 dependent fashion. Int. J. Radiat. Biol. 77, 1067-1078 (2001).
49. O. Potapova, A. Haghighi, F. Bost, C. Liu, M. J. Birrer, R. Gjerset and D. Mercola, The Jun kinase/stress-activated protein kinase pathway functions to regulate DNA repair and inhibition of the pathway sensitizes tumor cells to cisplatin. J. Biol. Chem. 272, 14041-4044 (1997).
50. G. A. Ruiter, S. F. Zerp, H. Bartelink, W. J. van Blitterswijk and M. Verheij, Alkyl-lysophospholipids activate the SAPK/JNK pathway and enhance radiation-induced apoptosis. Cancer Res. 59, 2457-63 (1999).
51. 2/M transition and independently of increased signaling by the JNK/c-Jun pathway. Int. J. Oncol. 16, 413-22 (2000).
52. R. McKinstry, L. Qiao, A. Yacoub, Y. Dai, R. Decker, M. P. Hagan, S. Grant and P. Dent, Inhibitors of MEK1/2 interact synergistically with UCN-01 to induce apoptosis and reduce colony formation in mammary and prostate carcinoma cells. Cancer Biol. Ther., in press.
53. H. E. Jones, D. Barrow, C. M. Dutkowski, L. Goddard, C. Smith, M. E. Harper and R. I. Nicholson, Effect of an EGF-R selective tyrosine kinase inhibitor and an anti-androgen on LNCaP cells: Identification of divergent growth regulatory pathways. Prostate 49, 38-47 (2001).
54. S. A. Leadon, Repair of DNA damage produced by ionizing radiation: A minireview. Semin. Radiat. Oncol. 6, 295-305 (1996).
55. S. J. Whitaker, DNA damage by drugs and radiation. Eur. J. Cancer 28, 273-276 (1992).
56. W. Lee-Kwon, D. Park and M. Bernier, Involvement of the Ras/extracellular signal-regulated kinase signalling pathway in the regulation of ERCC-1 mRNA levels by insulin. Biochem. J. 331, 591-597 (1998).
57. D. L. Persons, E. M. Yazlovitskaya, W. Cui and J. C. Pelling, Cisplatin-induced activation of mitogen-activated protein kinases in ovarian carcinoma cells: Inhibition of extracellular signal-regulated kinase activity increases sensitivity to cisplatin. Clin. Cancer Res. 5, 1007-1014 (1999).
58. G. Dong, Z. Chen, Z. Y. Li, N. T. Yeh, C. C. Bancroft and C. Van Waes, Hepatocyte growth factor/scatter factor-induced activation of MEK and PI3K signal pathways contributes to expression of proangiogenic cytokines interleukin-8 and vascular endothelial growth factor in head and neck squamous cell carcinoma. Cancer Res. 61, 5911-5918 (2001).
59. T Putz, Z. Culig, I. E. Eder, C. Nessler-Menardi, G. Bartsch, H. Grunicke, F. Uberall and H. Klocker, Epidermal growth factor (EGF) receptor blockade inhibits the action of EGF, insulin-like growth factor I, and a protein kinase A activator on the mitogen-activated protein kinase pathway in prostate cancer cell lines. Cancer Res. 59, 227-233 (1999).
60. X. Zi, R. P. Singh and R. Agarwal, Impairment of erbB1 receptor and fluid-phase endocytosis and associated mitogenic signaling by inositol hexaphosphate in human prostate carcinoma DU145 cells. Carcinogenesis. 21, 2225-2235 (2000).
61. D. L. Lin, M. C. Whitney, Z. Yao and E. T. Keller, Interleukin-6 induces androgen responsiveness in prostate cancer cells through upregulation of androgen receptor expression. Clin. Cancer Res. 7, 1773-1781 (2001).
62. S. J. Rubin, D. E. Hallahan, C. R. Ashman, D. G. Brachman, M. A. Beckett, S. Virudachalam, D. W. Yandell and R. R. Weichselbaum, Two prostate carcinoma cell lines demonstrate abnormalities in tumor suppressor genes. J. Surg. Oncol. 46, 31-36 (1991).
63. K. Kubo, H. Ide, S. S. Wallace and Y. W. Kow, A novel, sensitive, and specific assay for abasic sites, the most commonly produced DNA lesion. Biochemistry 14, 3703-3708 (1992).
64. J. Nakamura, V. E. Walker, P. B. Upton, S. Y. Chiang, Y. W. Kow and J. A. Swenberg, Highly sensitive apurinic/apyrimidinic site assay can detect spontaneous and chemically induced depurination under physiological conditions. Cancer Res. 58, 222-225 (1998).
65. T. C. Somervaille, D. C. Linch and A. Khwaja, Growth factor withdrawal from primary human erythroid progenitors induces apoptosis through a pathway involving glycogen synthase kinase-3 and Bax. Blood 98, 1374-1381 (2001).
66. L. Wang, F. Liu and M. L. Adamo, Cyclic AMP inhibits extracellular signal-regulated kinase and phosphatidylinositol 3-kinase/AKT pathways by inhibiting rapl. J. Biol. Chem. 276, 37242-37249 (2001).
67. A. S. Yap, Initiation of cell locomotility is a morphogenetic checkpoint in thyroid epithelial cells regulated by ERK and PI3-kinase signals. Cell Motil. Cytoskeleton 49, 93-103 (2000).
68. J. B. Klein, A. Buridi, P. Y. Coxon, M. J. Rane, T. Manning, R. Kettritz and K. R. McLeish, Role of extracellular signal-regulated kinase and phosphatidylinositol-3 kinase in chemoattractant and LPS delay of constitutive neutrophil apoptosis. Cell Signal 13, 335-343 (2001).
69. J. Sun, M. Li, J. Han and J. Gu, Sensitization of differentiated PC12 cells to apoptosis by presenilin-2 is mediated by p38. Biochem. Biophys. Res. Commun. 287, 536-541 (2001).
70. O. J. Han, K. H. Joe, S. W. Kim, H. S. Lee, N. S. Kwon, K. J. Baek and H. Y. Yun, Involvement of p38 mitogen-activated protein kinase and apoptosis signal-regulating kinase-1 in nitric oxide-induced cell death in PC12 cells. Neurochem. Res. 26, 525-532 (2001).
71. L. H. Thompson, K. W. Brookman, N. J. Jones, S. A. Allen and A. V. Carrano, Molecular cloning of the human XRCC1 gene, which corrects defective DNA strand break repair and sister chromatid exchange. Mol. Cell Biol. 10, 6160-6171 (1990).