The epidermal growth factor receptor in squamous cell carcinoma: An emerging drug target

Australasian Journal of Dermatology

Volumn 55, Issue 1, 2014, Pages 24-34

  Gaffney, Daniel C ^a,b   Soyer, H Peter ^a,b   Simpson, Fiona ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b PRINCESS ALEXANDRA HOSPITAL   (Australia)

Author keywords

cetuximab; epidermal growth factor; erlotinib; gefitinib; panitumumab; squamous cell carcinoma

Indexed keywords

BIOLOGICAL MARKER; CELECOXIB; CETUXIMAB; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR KINASE INHIBITOR; ERLOTINIB; FLUOROURACIL; FOLINIC ACID; GEFITINIB; GEMCITABINE; IRINOTECAN; LAPATINIB; OXALIPLATIN; PANITUMUMAB; PLATINUM DERIVATIVE; TRASTUZUMAB; ANTINEOPLASTIC AGENT; MONOCLONAL ANTIBODY; PROTEIN TYROSINE KINASE; QUINAZOLINE DERIVATIVE;

ACNE; ADVANCED CANCER; ALOPECIA; BREAST METASTASIS; CANCER PATIENT; CANCER RESISTANCE; CARDIOTOXICITY; CONTINUOUS INFUSION; DIARRHEA; DRUG EFFICACY; DRUG MECHANISM; DRUG TARGETING; DRUG TOLERABILITY; DRUG WITHDRAWAL; ECZEMA; FATIGUE; GASTROINTESTINAL SYMPTOM; HEAD AND NECK SQUAMOUS CELL CARCINOMA; HUMAN; IMMUNOHISTOCHEMISTRY; LUNG NON SMALL CELL CANCER; METASTASIS; METASTATIC COLORECTAL CANCER; MOLECULARLY TARGETED THERAPY; MORBIDITY; NAUSEA; PANCREAS CANCER; PARONYCHIA; PRECANCER; RASH; REVIEW; SKIN CARCINOMA; SKIN SQUAMOUS CELL CARCINOMA; TREATMENT OUTCOME; TREATMENT RESPONSE; XERODERMA PIGMENTOSUM; XEROSIS; ANTAGONISTS AND INHIBITORS; CARCINOMA, SQUAMOUS CELL; CHEMISTRY; DRUG EFFECTS; SIGNAL TRANSDUCTION; SKIN NEOPLASMS;

ANTIBODIES, MONOCLONAL; ANTIBODIES, MONOCLONAL, HUMANIZED; ANTINEOPLASTIC AGENTS; CARCINOMA, SQUAMOUS CELL; HUMANS; MOLECULAR TARGETED THERAPY; PROTEIN-TYROSINE KINASES; QUINAZOLINES; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION; SKIN NEOPLASMS;

EID: 84892783142     PISSN: 00048380     EISSN: 14400960     Source Type: Journal    
DOI: 10.1111/ajd.12025     Document Type: Review

References (91)

1. Cancer Australia and AIHW (Australian Institute of Health and Welfare). Non-Melanoma Skin Cancer: General Practice Consultations, Hospitalisation and Mortality. Cat. no. CAN 39. Canberra: AIHW, 2008.
2. AIHW. Health System Expenditures on Cancer and Other Neoplasms in Australia, 2000-01. Health and Welfare Expenditure Series No. 22. Cat. no. HWE 29. Canberra: AIHW, 2005.
3. Staples MP, Elwood M, Burton RC, et al. Non-melanoma skin cancer in Australia: the 2002 national survey and trends since 1985. Med. J. Aust. 2006; 184: 6-10.
4. Housman TS, Williford PM, Feldman SR, et al. Nonmelanoma skin cancer: an episode of care management approach. Dermatol. Surg. 2003; 29: 700-711.
5. Soyer HP, Rigel DS, Wurm EMT,. Actinic keratosis, basal cell carcinoma and squamous cell carcinoma. In, Bolognia JL, Jorizzo JL, Schaffer JV, (eds). Dermatology, 3rd edn. Edinburgh: Elsevier, 2012; 1773-1793.
6. Ackerman AB, Mones JM,. Solar (actinic) keratosis is squamous cell carcinoma. Brit. J. Dermatol. 2006; 155: 9-22.
7. Cohn BA,. From sunlight to actinic keratosis to squamous cell carcinoma. J. Am. Acad. Dermatol. 2000; 42: 143-144.
8. Marks R,. Who benefits from calling a solar keratosis a squamous cell carcinoma? Br. J. Dermatol. 2006; 155: 23-26.
9. de Zwaan SE, Haass NK,. Genetics of basal cell carcinoma. Australas. J. Dermatol. 2010; 51: 81-92.
10. Leffell DJ,. The scientific basis of skin cancer. J. Am. Acad. Dermatol. 2000; 42: 18-22.
11. Ke H, Harris R, Coloff JL, et al. The c-Jun NH2-terminal kinase 2 plays a dominant role in human epidermal neoplasia. Cancer Res. 2010; 70: 3080-3088.
12. El-Abaseri TB, Hansen LA,. EGFR activation and ultraviolet light-induced skin carcinogenesis. J. Biomed. Biotechnol. 2007; 2007: doi: 10.1155/2007/97939. (Accessed 1 January 2013).
13. Hansen LA, Woodson RL 2nd, Holbus S, et al. The epidermal growth factor receptor is required to maintain the proliferative population in the basal compartment of epidermal tumors. Cancer Res. 2000; 60: 3328-3332.
14. El-Abaseri TB, Fuhrman J, Trempus C, et al. Chemoprevention of UV light-induced skin tumorigenesis by inhibition of the epidermal growth factor receptor. Cancer Res. 2005; 65: 3958-3965.
15. Schlessinger J,. Cell signaling by receptor tyrosine kinases. Cell 2000; 103: 211-225.
16. Jorissen RN, Walker F, Pouliot N, et al. Epidermal growth factor receptor: mechanisms of activation and signalling. Exp. Cell Res. 2003; 284: 31-53.
17. Hu JC, Sadeghi P, Pinter-Brown LC, et al. Cutaneous side effects of epidermal growth factor receptor inhibitors: clinical presentation, pathogenesis, and management. J. Am. Acad. Dermatol. 2007; 56: 317-326.
18. Avraham R, Yarden Y,. Feedback regulation of EGFR signalling: decision making by early and delayed loops. Nat. Rev. Mol. Cell Biol. 2011; 12: 104-117.
19. Nazmi MN, Dykes PJ, Marks R,. Epidermal growth factor receptors in human epidermal tumours. Br. J. Dermatol. 1990; 123: 153-161.
20. Nanney LB, Magid M, Stoscheck CM, et al. Comparison of epidermal growth factor binding and receptor distribution in normal human epidermis and epidermal appendages. J. Invest. Dermatol. 1984; 83: 385-393.
21. Nanney LB, McKanna JA, Stoscheck CM, et al. Visualization of epidermal growth factor receptors in human epidermis. J. Invest. Dermatol. 1984; 82: 165-169.
22. Groves RW, Allen MH, MacDonald DM,. Abnormal expression of epidermal growth factor receptor in cutaneous epithelial tumours. J. Cutan. Pathol. 1992; 19: 66-72.
23. Kikuchi A, Amagai M, Hayakawa K, et al. Association of EGF receptor expression with proliferating cells and of ras p21 expression with differentiating cells in various skin tumours. Br. J. Dermatol. 1990; 123: 49-58.
24. Bauknecht T, Gross G, Hagedorn M,. Epidermal growth factor receptors in different skin tumours. Dermatologica 1985; 171: 16-20.
25. Lavrijsen AP, Tieben LM, Ponec M, et al. Expression of EGF receptor, involucrin, and cytokeratins in basal cell carcinomas and squamous cell carcinomas of the skin. Arch. Dermatol. Res. 1989; 281: 83-88.
26. Tucci MG, Offidani A, Lucarini G, et al. Advances in the understanding of malignant transformation of keratinocytes: an immunohistochemical study. J. Eur. Acad. Dermatol. Venereol. 1998; 10: 118-124.
27. Fogarty GB, Conus NM, Chu J, et al. Characterization of the expression and activation of the epidermal growth factor receptor in squamous cell carcinoma of the skin. Br. J. Dermatol. 2007; 156: 92-98.
28. Ikeuchi T, Urano Y, Fukuhara K, et al. Light microscopic autoradiographical analysis of [125I]epidermal growth factor binding in basal cell epithelioma and squamous cell carcinoma of the skin. J. Dermatol. 1993; 20: 219-225.
29. Toll A, Salgado R, Yebenes M, et al. Epidermal growth factor receptor gene numerical aberrations are frequent events in actinic keratoses and invasive cutaneous squamous cell carcinomas. Exp. Dermatol. 2010; 19: 151-153.
30. Krahn G, Leiter U, Kaskel P, et al. Coexpression patterns of EGFR, HER2, HER3 and HER4 in non-melanoma skin cancer. Eur. J. Cancer 2001; 37: 251-259.
31. Ch'ng S, Low I, Ng D, et al. Epidermal growth factor receptor: a novel biomarker for aggressive head and neck cutaneous squamous cell carcinoma. Hum. Pathol. 2008; 39: 344-349.
32. Shimizu T, Izumi H, Oga A, et al. Epidermal growth factor receptor overexpression and genetic aberrations in metastatic squamous-cell carcinoma of the skin. Dermatology 2001; 202: 203-206.
33. Maubec E, Duvillard P, Velasco V, et al. Immunohistochemical analysis of EGFR and HER-2 in patients with metastatic squamous cell carcinoma of the skin. Anticancer Res. 2005; 25: 1205-1210.
34. Jost M, Kari C, Rodeck U,. The EGF receptor-an essential regulator of multiple epidermal functions. Eur. J. Dermatol. 2000; 10: 505-510.
35. Liu B, Zhang H, Li S, et al. The expression of c-erbB-1 and c-erbB-2 oncogenes in basal cell carcinoma and squamous cell carcinoma of skin. Chin. Med. Sci. J. 1996; 11: 106-109.
36. Hama T, Yuza Y, Saito Y, et al. Prognostic significance of epidermal growth factor receptor phosphorylation and mutation in head and neck squamous cell carcinoma. Oncologist 2009; 14: 900-908.
37. Chung KY, Shia J, Kemeny NE, et al. Cetuximab shows activity in colorectal cancer patients with tumors that do not express the epidermal growth factor receptor by immunohistochemistry. J. Clin. Oncol. 2005; 23: 1803-1810.
38. Bell DW, Lynch TJ, Haserlat SM, et al. Epidermal growth factor receptor mutations and gene amplification in non-small-cell lung cancer: molecular analysis of the IDEAL/INTACT gefitinib trials. J. Clin. Oncol. 2005; 23: 8081-8092.
39. Ridd K, Bastian BC,. Somatic mutation of epidermal growth factor receptor in a small subset of cutaneous squamous cell carcinoma. J. Invest. Dermatol. 2010; 130: 901-903.
40. Lewis CM, Glisson BS, Feng L, et al. A phase II study of gefitinib for aggressive cutaneous squamous cell carcinoma of the head and neck. Clin. Cancer Res. 2012; 18: 1435-1446.
41. Abella JV, Park M,. Breakdown of endocytosis in the oncogenic activation of receptor tyrosine kinases. Am. J. Physiol. Endocrinol. Metab. 2009; 296: E973-984.
42. Ceresa BP, Schmid SL,. Regulation of signal transduction by endocytosis. Curr. Opin. Cell Biol. 2000; 12: 204-210.
43. Haslekas C, Breen K, Pedersen KW, et al. The inhibitory effect of ErbB2 on epidermal growth factor-induced formation of clathrin-coated pits correlates with retention of epidermal growth factor receptor-ErbB2 oligomeric complexes at the plasma membrane. Mol. Biol. Cell 2005; 16: 5832-5842.
44. Irwin ME, Mueller KL, Bohin N, et al. Lipid raft localization of EGFR alters the response of cancer cells to the EGFR tyrosine kinase inhibitor gefitinib. J. Cell. Physiol. 2011; 226: 2316-2328.
45. Arnold AW, Bruckner-Tuderman L, Zuger C, et al. Cetuximab therapy of metastasizing cutaneous squamous cell carcinoma in a patient with severe recessive dystrophic epidermolysis bullosa. Dermatology 2009; 219: 80-83.
46. Bauman JE, Eaton KD, Martins RG,. Treatment of recurrent squamous cell carcinoma of the skin with cetuximab. Arch. Dermatol. 2007; 143: 889-892.
47. Kim S, Eleff M, Nicolaou N,. Cetuximab as primary treatment for cutaneous squamous cell carcinoma to the neck. Head Neck 2011; 33: 286-288.
48. Miller K, Sherman W, Ratner D,. Complete clinical response to cetuximab in a patient with metastatic cutaneous squamous cell carcinoma. Dermatol. Surg. 2010; 36: 2069-2074.
49. Rubio Casadevall J, Grana-Suarez B, Hernandez-Yague X, et al. Xeroderma pigmentosum: neck lymph node metastasis of a squamous cell carcinoma of the skin treated with cetuximab. Eur. J. Dermatol. 2009; 19: 163-165.
50. Suen JK, Bressler L, Shord SS, et al. Cutaneous squamous cell carcinoma responding serially to single-agent cetuximab. Anticancer Drugs 2007; 18: 827-829.
51. Wollina U, Schreiber A, Merla K, et al. Combined cetuximab and volumetric modulated arc-radiotherapy in advanced recurrent squamous cell carcinoma of the scalp. Dermatol. Rep. 2011; 3: 130-134.
52. Giacchero D, Barriere J, Benezery K, et al. Efficacy of cetuximab for unresectable or advanced cutaneous squamous cell carcinoma-a report of eight cases. Clin. Oncol. (R. Coll. Radiol.) 2011; 23: 716-718.
53. Kanakamedala MR, Packianathan S, Vijayakumar S,. Lack of cetuximab induced skin toxicity in a previously irradiated field: case report and review of the literature. Radiat. Oncol. 2010; 5: 38.
54. Goppner D, Nekwasil S, Franke I, et al. Successful combination therapy of a locally advanced squamous cell carcinoma of the skin with cetuximab and gamma-irradiation. J. Dtsch. Dermatol. Ges. 2010; 8: 826-828.
55. Jalili A, Pinc A, Pieczkowski F, et al. Combination of an EGFR blocker and a COX-2 inhibitor for the treatment of advanced cutaneous squamous cell carcinoma. J. Dtsch. Dermatol. Ges. 2008; 6: 1066-1069.
56. Bonner JA, Harari PM, Giralt J, et al. Radiotherapy plus cetuximab for squamous-cell carcinoma of the head and neck. N. Engl. J. Med. 2006; 354: 567-578.
57. Maubec E, Petrow P, Scheer-Senyarich I, et al. Phase II study of cetuximab as first-line single-drug therapy in patients with unresectable squamous cell carcinoma of the skin. J. Clin. Oncol. 2011; 29: 3419-3426.
58. Necchi A, Nicolai N, Colecchia M, et al. Proof of activity of anti-epidermal growth factor receptor-targeted therapy for relapsed squamous cell carcinoma of the penis. J. Clin. Oncol. 2011; 29: e650-652.
59. Clinical Trials Org. An Open Label Multicentric Phase II Study of Panitumumab (Vectibix®) in Cutaneous Squamous Cell Carcinoma (SCC) 2010. Updated August 2010. Available from URL: http://www.clinicaltrialsfeeds.org/ clinical-trials/show/NCT01129154. (Accessed 1 January 2013).
60. Machiels JP, Subramanian S, Ruzsa A, et al. Zalutumumab plus best supportive care versus best supportive care alone in patients with recurrent or metastatic squamous-cell carcinoma of the head and neck after failure of platinum-based chemotherapy: an open-label, randomised phase 3 trial. Lancet Oncol. 2011; 12: 333-343.
61. Baltaci M, Fritsch P, Weber F, et al. Treatment with gefitinib (ZD 1839) in a patient with advanced cutaneous squamous cell carcinoma. Br. J. Dermatol. 2005; 153: 234-236.
62. Clinical Trials.Org. A Phase I/II Pilot Study Of Bioimmunotherapy With IRESSA (Gefitinib) And Pegylated Interferon Alpha-2a For Patients With Unresectable/Metastatic Squamous Cell Carcinoma Of The Skin. 2007 Updated 6 February 2006. Available from URL: http://www.clinicaltrialsfeeds.org/clinical- trials/show/NCT00423397. (Accessed 1 January 2013).
63. Read WL,. Squamous carcinoma of the skin responding to erlotinib: three cases. J. Clin. Oncol. 2007; 25: 16519.
64. Macripo G, Caliendo V, Grassi M, et al. Squamous cell carcinoma of the umbilicus: management of an unusual localization. Tumori 2011; 97: 236-238.
65. Engelhardt C, Curiel-Lewandrowski C, Warneke J, et al. Metastatic cutaneous squamous cell carcinoma responding to erlotinib therapy. J. Am. Acad. Dermatol. 2011; 65: 237-238.
66. Clinical Trials.Org. Phase II Study of Erlotinib, an Epidermal Growth Factor Receptor (EGFR) Tyrosine Kinase Inhibitor, in the Treatment of Recurrent or Metastatic Squamous Cell Carcinoma of the Skin 2010. Updated 20 December 2012. Available from URL: http://www.clinicaltrialsfeeds.org/clinical-trials/ show/NCT01198028. (Accessed 1 January 2013).
67. Clinical Trials.Org. Phase II Trial of Erlotinib, Prior to Surgery or Radiation in Patients with Squamous Cell Cancers (SCC) of the Skin. 2010. Updated 28 September 2012. Available from URL: http://www.clinicaltrials.gov/ ct2/show/NCT01059305. (Accessed 1 January 2013).
68. Wheeler DL, Dunn EF, Harari PM,. Understanding resistance to EGFR inhibitors-impact on future treatment strategies. Nat. Rev. Clin. Oncol. 2010; 7: 493-507.
69. Hidaka T, Fujimura T, Watabe A, et al. Successful treatment of HER-2-positive metastatic apocrine carcinoma of the skin with lapatinib and capecitabine. Acta Derm. Venereol. 2012; 92: 654-655.
70. Yamazaki M, Yamashita Y, Kubo N, et al. Concurrent biological targeting therapy of squamous cell carcinoma of the esophagus with cetuximab and trastuzumab. Oncol. Rep. 2012; 28: 49-54.
71. Nemunaitis J, Eiseman I, Cunningham C, et al. Phase 1 clinical and pharmacokinetics evaluation of oral CI-1033 in patients with refractory cancer. Clin. Cancer Res. 2005; 11: 3846-3853.
72. Clayburgh DR, Gross ND, Proby C, et al. Effects of epidermal growth factor receptor and insulin-like growth factor 1 receptor inhibition on proliferation and intracellular signaling in cutaneous SCCHN: potential for dual inhibition as a therapeutic modality. Head Neck 2012; 35: 86-93.
73. Weickhardt AJ, Price TJ, Chong G, et al. Dual targeting of the epidermal growth factor receptor using the combination of cetuximab and erlotinib: preclinical evaluation and results of the phase II DUX study in chemotherapy-refractory, advanced colorectal cancer. J. Clin. Oncol. 2012; 30: 1505-1512.
74. Albanell J, Rojo F, Averbuch S, et al. Pharmacodynamic studies of the epidermal growth factor receptor inhibitor ZD1839 in skin from cancer patients: histopathologic and molecular consequences of receptor inhibition. J. Clin. Oncol. 2002; 20: 110-124.
75. Pollack BP, Sapkota B, Cartee TV,. Epidermal growth factor receptor inhibition augments the expression of MHC class I and II genes. Clin. Cancer Res. 2011; 17: 4400-4413.
76. Lievre A, Bachet JB, Le Corre D, et al. KRAS mutation status is predictive of response to cetuximab therapy in colorectal cancer. Cancer Res. 2006; 66: 3992-3995.
77. Montagut C, Dalmases A, Bellosillo B, et al. Identification of a mutation in the extracellular domain of the epidermal growth factor receptor conferring cetuximab resistance in colorectal cancer. Nat. Med. 2012; 18: 221-223.
78. Wnorowski AM, de Souza A, Chachoua A, et al. The management of EGFR inhibitor adverse events: a case series and treatment paradigm. Int. J. Dermatol. 2012; 51: 223-232.
79. Soulieres D, Senzer NN, Vokes EE, et al. Multicenter phase II study of erlotinib, an oral epidermal growth factor receptor tyrosine kinase inhibitor, in patients with recurrent or metastatic squamous cell cancer of the head and neck. J. Clin. Oncol. 2004; 22: 77-85.
80. DeWitt CA, Siroy AE, Stone SP,. Acneiform eruptions associated with epidermal growth factor receptor-targeted chemotherapy. J. Am. Acad. Dermatol. 2007; 56: 500-505.
81. Orditura M, De Vita F, Galizia G, et al. Correlation between efficacy and skin rash occurrence following treatment with the epidermal growth factor receptor inhibitor cetuximab: a single institution retrospective analysis. Oncol. Rep. 2009; 21: 1023-1028.
82. Mohamed MK, Ramalingam S, Lin Y, et al. Skin rash and good performance status predict improved survival with gefitinib in patients with advanced non-small cell lung cancer. Ann. Oncol. 2005; 16: 780-785.
83. Wollina U,. Cetuximab in non-melanoma skin cancer. Expert Opin. Biol. Ther. 2012; 12: 949-956.
84. Pryor DI, Porceddu SV, Burmeister BH, et al. Enhanced toxicity with concurrent cetuximab and radiotherapy in head and neck cancer. Radiother. Oncol. 2009; 90: 172-176.
85. Potthoff K, Hofheinz R, Hassel JC, et al. Interdisciplinary management of EGFR-inhibitor-induced skin reactions: a German expert opinion. Ann. Oncol. 2011; 22: 524-535.
86. Lacouture ME, Anadkat MJ, Bensadoun RJ, et al. Clinical practice guidelines for the prevention and treatment of EGFR inhibitor-associated dermatologic toxicities. Support. Care Cancer 2011; 19: 1079-1095.
87. Hermanns JF, Pierard GE, Quatresooz P,. Erlotinib-responsive actinic keratoses. Oncol. Rep. 2007; 18: 581-584.
88. Reid DC, Guitart J, Agulnik M, et al. Treatment of multiple keratoacanthomas with erlotinib. Int. J. Clin. Oncol. 2010; 15: 413-415.
89. Kenner-Bell BM, Paller AS, Lacouture ME,. Epidermal growth factor receptor inhibition with erlotinib for palmoplantar keratoderma. J. Am. Acad. Dermatol. 2010; 63: e58-59.
90. Cranmer LD, Engelhardt C, Morgan SS,. Treatment of unresectable and metastatic cutaneous squamous cell carcinoma. Oncologist 2010; 15: 1320-1328.
91. Brantsch KD, Meisner C, Schonfisch B, et al. Analysis of risk factors determining prognosis of cutaneous squamous-cell carcinoma: a prospective study. Lancet Oncol. 2008; 9: 713-720.