Epidermal growth factor receptor inhibitors for radiotherapy: Biological rationale and preclinical results

Journal of Pharmacy and Pharmacology

Volumn 60, Issue 8, 2008, Pages 1019-1028

  Zips, Daniel ^a,b   Krause, Mechthild ^a   Yaromina, Ala ^a   Dörfler, Annegret ^a   Eicheler, Wolfgang ^a   Schütze, Christina ^a   Gurtner, Kristin ^a   Baumann, Michael ^a  

^a DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^b UNIVERSITY HOSPITAL CARL GUSTAV CARUS   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BIBX 1382BS; CETUXIMAB; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR KINASE INHIBITOR; MONOCLONAL ANTIBODY;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; APOPTOSIS; CANCER INHIBITION; CANCER RADIOTHERAPY; CONTROLLED STUDY; DNA REPAIR; DRUG CYTOTOXICITY; MOUSE; NONHUMAN; NUDE MOUSE; RADIATION DOSE; RADIATION DOSE FRACTIONATION; RADIOSENSITIVITY; REVIEW; SIGNAL TRANSDUCTION; SQUAMOUS CELL CARCINOMA; TUMOR XENOGRAFT;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; CHEMOTHERAPY, ADJUVANT; DOSE FRACTIONATION; HUMANS; MICE; MICE, NUDE; NEOPLASMS, EXPERIMENTAL; ORGANIC CHEMICALS; PROTEIN KINASE INHIBITORS; RADIATION TOLERANCE; RECEPTOR, EPIDERMAL GROWTH FACTOR; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 47949102297     PISSN: 00223573     EISSN: None     Source Type: Journal    
DOI: 10.1211/jpp.60.8.0008     Document Type: Review

References (64)

1. Ang, K. K., Berkey, B. A., Tu, X., Zhang, H. Z., Kate, R., Hammond, E. H., Fu, K. K., Milas, L. (2002) Impact of epidermal growth factor receptor expression on survival and pattern of relapse in patients with advanced head and neck carcinoma. Cancer Res. 62: 7350-7356
2. Bamberg, M., Budach, W., Belka, C. (1996) Radioonkologie 2000. Der Onkologe 2: 5-9
3. Baumann, M. (2006) Keynote comment: radiotherapy in the age of molecular oncology. Lancet Oncol. 7: 786-787
4. Baumann, M., Dubois, W., Suit, H. D. (1990) Response of human squamous cell carcinoma xenografts of different sizes to irradiation: relationship of clonogenic cells, cellular radiation sensitivity in vivo, and tumor rescuing units. Radiat. Res. 123: 325-330
5. Baumann, M., Dorr, W., Petersen, C., Krause, M. (2003a) Repopulation during fractionated radiotherapy: much has been learned, even more is open. Int. J. Radiat. Biol. 79: 465-467
6. Baumann, M., Krause, M., Zips, D., Eicheler, W., Dorfler, A., Ahrens, J., Petersen, C., Bruchner, K., Hilberg, F. (2003b) Selective inhibition of the epidermal growth factor receptor tyrosine kinase by BIBX1382BS and the improvement of growth delay, but not local control, after fractionated irradiation in human FaDu squamous cell carcinoma in the nude mouse. Int. J. Radiat. Biol. 79: 547-559
7. Baumann, M., Krause, M., Dikomey, E., Dittmann, K., Dorr, W., Kasten-Pisula, U., Rodemann, H. P. (2007) EGFR-targeted anti-cancer drugs in radiotherapy: preclinical evaluation of mechanisms. Radiother. Oncol. 83: 238-248
8. Bentzen, S. M., Atasoy, B. M., Daley, F. M., Dische, S., Richman, P. I., Saunders, M. I., Trott, K. R., Wilson, G. D. (2005) Epidermal growth factor receptor expression in pretreatment biopsies from head and neck squamous cell carcinoma as a predictive factor for a benefit from accelerated radiation therapy in a randomized controlled trial. J. Clin. Oncol. 23: 5560-5567
9. Bernier, J., Schneider, D. (2007) Cetuximab combined with radiotherapy: an alternative to chemoradiotherapy for patients with locally advanced squamous cell carcinomas of the head and neck? Eur. J. Cancer 43: 35-45
10. 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., Ove, R., Kies, M. S., Baselga, J., Youssoufian, H., Amellal, N., Rowinsky, E. K., Ang, K. K. (2006) Radiotherapy plus cetuximab for squamous-cell carcinoma of the head and neck. N. Engl. J. Med. 354: 567-578
11. Bourhis, J., Overgaard, J., Audry, H., Ang, K. K., Saunders, M., Bernier, J., Horiot, J. C., Le Maitre, A., Pajak, T. F., Poulsen, M. G., O'Sullivan, B., Dobrowsky, W., Hliniak, A., Skladowski, K., Hay, J. H., Pinto, L. H., Fallai, C., Fu, K. K., Sylvester, R., Pignon, J. P. (2006) Hyperfractionated or accelerated radiotherapy in head and neck cancer: a meta-analysis. Lancet 368: 843-854
12. Boyle, P., Ferlay, J. (2005) Cancer incidence and mortality in Europe, 2004. Ann. Oncol. 16: 481-488
13. Carter, P., Presta, L., Gorman, C. M., Ridgway, J. B., Henner, D., Wong, W. L., Rowland, A. M., Kotts, C., Carver, M. E., Shepard, H. M. (1992) Humanization of an anti-p185HER2 antibody for human cancer therapy. Proc. Natl Acad. Sci. USA 89: 4285-4289
14. Chakravarti, A., Dicker, A., Mehta, M. (2004) The contribution of epidermal growth factor receptor (EGFR) signaling pathway to radioresistance in human gliomas: a review of preclinical and correlative clinical data. Int. J. Radiat. Oncol. Biol. Phys. 58: 927-931
15. Chinnaiyan, P., Huang, S., Vallabhaneni, G., Armstrong, E., Varambally, S., Tomlins, S. A., Chinnaiyan, A. M., Harari, P. M. (2005) Mechanisms of enhanced radiation response following epidermal growth factor receptor signaling inhibition by erlotinib (Tarceva). Cancer Res. 65: 3328-3335
16. Chua, D. T., Nicholls, J. M., Sham, J. S., Au, G. K. (2004) Prognostic value of epidermal growth factor receptor expression in patients with advanced stage nasopharyngeal carcinoma treated with induction chemotherapy and radiotherapy. Int. J. Radiat. Oncol. Biol. Phys. 59: 11-20
17. Dittmann, K., Mayer, C., Fehrenbacher, B., Schaller, M., Raju, U., Milas, L., Chen, D. J., Kehlbach, R., Rodemann, H. P. (2005) Radiation-induced epidermal growth factor receptor nuclear import is linked to activation of DNA-dependent protein kinase. J. Biol. Chem. 280: 31 182-31 189
18. Eicheler, W., Krause, M., Hessel, F., Zips, D., Baumann, M. (2005) Kinetics of EGFR expression during fractionated irradiation varies between different human squamous cell carcinoma lines in nude mice. Radiother. Oncol. 76: 151-156
19. Eriksen, J. G., Steiniche, T., Overgaard, J. (2005) The influence of epidermal growth factor receptor and tumor differentiation on the response to accelerated radiotherapy of squamous cell carcinomas of the head and neck in the randomized DAHANCA 6 and 7 study. Radiother. Oncol. 74: 93-100
20. Feng, F. Y., Lopez, C. A., Normolle, D. P., Varambally, S., Li, X., Chun, P. Y., Davis, M. A., Lawrence, T. S., Nyati, M. K. (2007) Effect of epidermal growth factor receptor inhibitor class in the treatment of head and neck cancer with concurrent radiochemotherapy in vivo. Clin. Cancer Res. 13: 2512-2518
21. Gibson, M. K., Abraham, S. C., Wu, T. T., Burtness, B., Heitmiller, R. F., Heath, E., Forastiere, A. (2003) Epidermal growth factor receptor, p53 mutation, and pathological response predict survival in patients with locally advanced esophageal cancer treated with preoperative chemoradiotherapy. Clin. Cancer Res. 9: 6461-6468
22. Giralt, J., de las Heras, M., Cerezo, L., Eraso, A., Hermosilla, E., Velez, D., Lujan, J., Espin, E., Rosello, J., Majo, J., Benavente, S., Armengol, M., de Torres, I. (2005) The expression of epidermal growth factor receptor results in a worse prognosis for patients with rectal cancer treated with preoperative radiotherapy: a multicenter, retrospective analysis. Radiother. Oncol. 74: 101-108
23. Hanahan, D., Weinberg, R. A. (2000) The hallmarks of cancer. Cell 100: 57-70
24. Harari, P. M., Allen, G. W., Bonner, J. A. (2007) Biology of interactions: antiepidermal growth factor receptor agents. J. Clin. Oncol. 25: 4057-4065
25. Hessel, F., Petersen, C., Zips, D., Krause, M., Pfitzmann, D., Thames, H. D., Baumann, M. (2003) Impact of increased cell loss on the repopulation rate during fractionated irradiation in human FaDu squamous cell carcinoma growing in nude mice. Int. J. Radiat. Biol. 79: 479-486
26. Huang, S. M., Bock, J. M., Harari, P. M. (1999) Epidermal growth factor receptor blockade with C225 modulates proliferation, apoptosis, and radiosensitivity in squamous cell carcinomas of the head and neck. Cancer Res. 59: 1935-1940
27. Kawaguchi, Y., Kono, K., Mimura, K., Sugai, H., Akaike, H., Fujii, H. (2007) Cetuximab induce antibody-dependent cellular cytotoxicity against EGFR-expressing esophageal squamous cell carcinoma. Int. J. Cancer 120: 781-787
28. Krause, M., Baumann, M. (2008) Clinical biomarkers of kinase activity: examples from EGFR inhibition trials. Cancer Metastasis Rev. 27: Apr 22 [Epub ahead of print]
29. Krause, M., Baumann, M., Thames, H. D. (2003) In regard to Solomon etal.: EGFR blockade with ZD1839 ("Iressa") potentiates the antitumor effects of single and multiple fractions of ionizing radiation in human A431 squamous cell carcinoma. IJROBP 2003;55:713-723. Int. J. Radiat. Oncol. Biol. Phys. 57: 300-301
30. Krause, M., Hessel, F., Zips, D., Hilberg, F., Baumann, M. (2004) Adjuvant inhibition of the epidermal growth factor receptor after fractionated irradiation of FaDu human squamous cell carcinoma. Radiother. Oncol. 72: 95-101
31. Krause, M., Schutze, C., Petersen, C., Pimentel, N., Hessel, F., Harstrick, A., Baumann, M. (2005a) Different classes of EGFR inhibitors may have different potential to improve local tumour control after fractionated irradiation: a study on C225 in FaDu hSCC. Radiother. Oncol. 74: 109-115
32. Krause, M., Ostermann, G., Petersen, C., Yaromina, A., Hessel, F., Harstrick, A., van der Kogel, A. J., Thames, H. D., Baumann, M. (2005b) Decreased repopulation as well as increased reoxygenation contribute to the improvement in local control after targeting of the EGFR by C225 during fractionated irradiation. Radiother. Oncol. 76: 162-167
33. Krause, M., Zips, D., Thames, H. D., Kummermehr, J., Baumann, M. (2006) Preclinical evaluation of molecular-targeted anticancer agents for radiotherapy. Radiother. Oncol. 80: 112-122
34. Krause, M., Prager, J., Zhou, X., Yaromina, A., Dorfler, A., Eicheler, W., Baumann, M. (2007) EGFR-TK inhibition before radiotherapy reduces tumour volume but does not improve local control: differential response of cancer stem cells and nontumourigenic cells? Radiother. Oncol. 83: 316-325
35. Kurai, J., Chikumi, H., Hashimoto, K., Yamaguchi, K., Yamasaki, A., Sako, T., Touge, H., Makino, H., Takata, M., Miyata, M., Nakamoto, M., Burioka, N., Shimizu, E. (2007) Antibody-dependent cellular cytotoxicity mediated by cetuximab against lung cancer cell lines. Clin. Cancer Res. 13: 1552-1561
36. Lammering, G., Valerie, K., Lin, P. S., Hewit, T. H., Schmidt-Ullrich, R. K. (2004) Radiation-induced activation of a common variant of EGFR confers enhanced radioresistance. Radiother. Oncol. 72: 267-273
37. Li, S., Schmitz, K. R., Jeffrey, P. D., Wiltzius, J. J., Kussie, P., Ferguson, K. M. (2005) Structural basis for inhibition of the epidermal growth factor receptor by cetuximab. Cancer Cell 7: 301-311
38. Lo, H. W., Hung, M. C. (2006) Nuclear EGFR signalling network in cancers: linking EGFR pathway to cell cycle progression, nitric oxide pathway and patient survival. Br. J. Cancer 94: 184-188
39. Mendelsohn, J., Baselga, J. (2006) Epidermal growth factor receptor targeting in cancer. Semin. Oncol. 33: 369-385
40. Milas, L., Mason, K., Hunter, N., Petersen, S., Yamakawa, M., Ang, K., Mendelsohn, J., Fan, Z. (2000) In vivo enhancement of tumor radioresponse by C225 antiepidermal growth factor receptor antibody. Clin. Cancer Res. 6: 701-708
41. Milas, L., Fang, F. M., Mason, K. A., Valdecanas, D., Hunter, N., Koto, M., Ang, K. K. (2007) Importance of maintenance therapy in C225-induced enhancement of tumor control by fractionated radiation. Int. J. Radiat. Oncol. Biol. Phys. 67: 568-572
42. Nasu, S., Ang, K. K., Fan, Z., Milas, L. (2001) C225 antiepidermal growth factor receptor antibody enhances tumor radiocurability. Int. J. Radiat. Oncol. Biol. Phys. 51: 474-477
43. Overgaard, M., Hansen, P. S., Overgaard, J., Rose, C., Andersson, M., Bach, F., Kjaer, M., Gadeberg, C. C., Mouridsen, H. T., Jensen, M. B., Zedeler, K. (1997) Postoperative radiotherapy in high-risk premenopausal women with breast cancer who receive adjuvant chemotherapy. Danish Breast Cancer Cooperative Group 82b Trial. N. Engl. J. Med. 337: 949-955
44. Petersen, C., Zips, D., Krause, M., Schone, K., Eicheler, W., Hoinkis, C., Thames, H. D., Baumann, M. (2001) Repopulation of FaDu human squamous cell carcinoma during fractionated radiotherapy correlates with reoxygenation. Int. J. Radiat. Oncol. Biol. Phys. 51: 483-493
45. Petersen, C., Eicheler, W., Frommel, A., Krause, M., Balschukat, S., Zips, D., Baumann, M. (2003) Proliferation and micromilieu during fractionated irradiation of human FaDu squamous cell carcinoma in nude mice. Int. J. Radiat. Biol. 79: 469-477
46. Pignon, J. P., Bourhis, J., Domenge, C., Designe, L. (2000) Chemotherapy added to locoregional treatment for head and neck squamous-cell carcinoma: three meta-analyses of updated individual data. MACH-NC Collaborative Group. Meta-Analysis of Chemotherapy on Head and Neck Cancer. Lancet 355: 949-955
47. Pillai, M. R., Jayaprakash, P. G., Nair, M. K. (1998) Tumour-proliferative fraction and growth factor expression as markers of tumour response to radiotherapy in cancer of the uterine cervix. J. Cancer Res. Clin. Oncol. 124: 456-461
48. Ragaz, J., Jackson, S. M., Le, N., Plenderleith, I. H., Spinelli, J. J., Basco, V. E., Wilson, K. S., Knowling, M. A., Coppin, C. M., Paradis, M., Coldman, A. J., Olivotto, I. A. (1997) Adjuvant radiotherapy and chemotherapy in node-positive premenopausal women with breast cancer. N. Engl. J. Med. 337: 956-962
49. Reff, M. E., Carner, K., Chambers, K. S., Chinn, P. C., Leonard, J. E., Raab, R., Newman, R. A., Hanna, N., Anderson, D. R. (1994) Depletion of B cells in vivo by a chimeric mouse human monoclonal antibody to CD20. Blood 83: 435-445
50. Sarkaria, J. N., Carlson, B. L., Schroeder, M. A., Grogan, P., Brown, P. D., Giannini, C., Ballman, K. V., Kitange, G. J., Guha, A., Pandita, A., James, C. D. (2006) Use of an orthotopic xenograft model for assessing the effect of epidermal growth factor receptor amplification on glioblastoma radiation response. Clin. Cancer Res. 12: 2264-2271
51. Saunders, M., Dische, S., Barrett, A., Harvey, A., Griffiths, G., Palmar, M. (1999) Continuous, hyperfractionated, accelerated radiotherapy (CHART) versus conventional radiotherapy in non-small cell lung cancer: mature data from the randomised multicentre trial. CHART Steering committee. Radiother. Oncol. 52: 137-148
52. Schlee, J., Dorfler, A., Zips, D., Petersen, C., Krause, M., Hilberg, F., Baumann, M. (2003) Einfluss der EGFR-rezeptorhemmung mit BIBX1382BS auf FaDu-zellen während fraktionierter bestrahlung in vitro: erste ergebnisse. Exp. Strahlenther. Klin. Strahlenhiol. 12: 4-8
53. Schmidt-Ullrich, R. K., Contessa, J. N., Dent, P., Mikkelsen, R. B., Valerie, K., Reardon, D. B., Bowers, G., Lin, P. S. (1999) Molecular mechanisms of radiation-induced accelerated repopulation. Radiat. Oncol. Investig. 7: 321-330
54. Schutze, C., Dorfler, A., Eicheler, W., Zips, D., Hering, S., Solca, F., Baumann, M., Krause, M. (2007) Combination of EGFR/HER2 tyrosine kinase inhibition by BIBW 2992 and BIBW 2669 with irradiation in FaDu human squamous cell carcinoma. Strahlenther Onkol. 183: 256-264
55. Solomon, B., Hagekyriakou, J., Trivett, M. K., Stacker, S. A., McArthur, G. A., Cullinane, C. (2003) EGFR blockade with ZD1839 ("Iressa") potentiates the antitumor effects of single and multiple fractions of ionizing radiation in human A431 squamous cell carcinoma. Epidermal growth factor receptor. Int. J. Radiat. Oncol. Biol. Phys. 55: 713-723
56. Steel, G. G. (ed.) (2002) The radiobiology of tumours. In: Basic clinical radiobiology, 3rd edn. Arnold, London, pp 182-191
57. Thomas, S. M., Grandis, J. R. (2004) Pharmacokinetic and pharmacodynamic properties of EGFR inhibitors under clinical investigation. Cancer Treat. Rev. 30: 255-268
58. Toulany, M., Dittmann, K., Baumann, M., Rodemann, H. P. (2005a) Radiosensitization of Ras-mutated human tumor cells in vitro by the specific EGF receptor antagonist BIBX1382BS. Radiother. Oncol. 74: 117-129
59. Toulany, M., Dittmann, K., Kruger, M., Baumann, M., Rodemann, H. P. (2005b) Radioresistance of K-Ras mutated human tumor cells is mediated through EGFR-dependent activation of PI3K-AKT pathway. Radiother. Oncol. 76: 143-150
60. Toulany, M., Kasten-Pisula, U., Brammer, I., Wang, S., Chen, J., Dittmann, K., Baumann, M., Dikomey, E., Rodemann, H. P. (2006) Blockage of epidermal growth factor receptor-phosphatidylinositol 3-kinase-AKT signaling increases radiosensitivity of K-RAS mutated human tumor cells in vitro by affecting DNA repair. Clin. Cancer Res. 12: 4119-4126
61. Turrisi, A. T., 3rd, Kim, K., Blum, R., Sause, W. T., Livingston, R. B., Komaki, R., Wagner, H., Aisner, S., Johnson, D. H. (1999) Twice-daily compared with once-daily thoracic radiotherapy in limited small-cell lung cancer treated concurrently with cisplatin and etoposide. N. Engl. J. Med. 340: 265-271
62. Williams, K. J., Telfer, B. A., Stratford, I. J., Wedge, S. R. (2002) ZD1839 ('Iressa'), a specific oral epidermal growth factor receptor-tyrosine kinase inhibitor, potentiates radiotherapy in a human colorectal cancer xenograft model. Br. J. Cancer 86: 1157-1161
63. Williams, K. J., Telfer, B. A., Brave, S., Kendrew, J., Whittaker, L., Stratford, I. J., Wedge, S. R. (2004) ZD6474, a potent inhibitor of vascular endothelial growth factor signaling, combined with radiotherapy: schedule-dependent enhancement of antitumor activity. Clin. Cancer Res. 10: 8587-8593
64. Yarden, Y., Sliwkowski, M. X. (2001) Untangling the ErbB signalling network. Nat. Rev. Mol. Cell Biol. 2: 127-137