Constitutively active Harvey Ras confers resistance to epidermal growth factor receptor-targeted therapy with cetuximab and gefitinib

Cancer Letters

Volumn 306, Issue 1, 2011, Pages 85-91

  Luwor, Rodney B ^a   Lu, Yang ^a   Li, Xinqun ^a   Liang, Ke ^a   Fan, Zhen ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

Cetuximab; EGFR; Gefitinib; H Ras; Resistance

Indexed keywords

CETUXIMAB; GEFITINIB; HARVEY RAS PROTEIN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE B; RAS PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER RESISTANCE; CARCINOMA CELL; CONTROLLED STUDY; DRUG EFFICACY; DRUG TARGETING; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; FEMALE; GENE ACTIVITY; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE MUTATION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MALIGNANT NEOPLASTIC DISEASE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SQUAMOUS CELL CARCINOMA; TRANSCRIPTION REGULATION; VULVA CARCINOMA;

ANTIBODIES, MONOCLONAL; ANTINEOPLASTIC AGENTS; CARCINOMA, SQUAMOUS CELL; CELL LINE, TUMOR; DRUG RESISTANCE, NEOPLASM; EPIDERMAL GROWTH FACTOR; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; GENES, RAS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MODELS, BIOLOGICAL; PHOSPHORYLATION; QUINAZOLINES; RAS PROTEINS; RECEPTOR, EPIDERMAL GROWTH FACTOR; VULVAR NEOPLASMS;

EID: 79955463114     PISSN: 03043835     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.canlet.2011.02.035     Document Type: Article

References (51)

1. Lemmon M.A., Schlessinger J. Cell signaling by receptor tyrosine kinases. Cell 2010, 141:1117-1134.
2. Ciardiello F., Tortora G. EGFR antagonists in cancer treatment. N. Engl. J. Med. 2008, 358:1160-1174.
3. Olayioye M.A., Neve R.M., Lane H.A., Hynes N.E. The ErbB signaling network: receptor heterodimerization in development and cancer. EMBO J. 2000, 19:3159-3167.
4. Blancher C., Moore J.W., Robertson N., Harris A.L. Effects of ras and von Hippel-Lindau (VHL) gene mutations on hypoxia-inducible factor (HIF)-1alpha, HIF-2alpha, and vascular endothelial growth factor expression and their regulation by the phosphatidylinositol 3'-kinase/Akt signaling pathway. Cancer Res. 2001, 61:7349-7355.
5. Fukuda R., Hirota K., Fan F., Jung Y.D., Ellis L.M., Semenza G.L. Insulin-like growth factor 1 induces hypoxia-inducible factor 1-mediated vascular endothelial growth factor expression, which is dependent on MAP kinase and phosphatidylinositol 3-kinase signaling in colon cancer cells. J. Biol. Chem. 2002, 277:38205-38211.
6. Minet E., Arnould T., Michel G., Roland I., Mottet D., Raes M., Remacle J., Michiels C. ERK activation upon hypoxia: involvement in HIF-1 activation. FEBS Lett. 2000, 468:53-58.
7. Treins C., Giorgetti-Peraldi S., Murdaca J., Semenza G.L., Van Obberghen E. Insulin stimulates hypoxia-inducible factor 1 through a phosphatidylinositol 3-kinase/target of rapamycin-dependent signaling pathway. J. Biol. Chem. 2002, 277:27975-27981.
8. Zhong H., Chiles K., Feldser D., Laughner E., Hanrahan C., Georgescu M.M., Simons J.W., Semenza G.L. Modulation of hypoxia-inducible factor 1alpha expression by the epidermal growth factor/phosphatidylinositol 3-kinase/PTEN/AKT/FRAP pathway in human prostate cancer cells: implications for tumor angiogenesis and therapeutics. Cancer Res. 2000, 60:1541-1545.
9. Semenza G.L. HIF-1 inhibitors for cancer therapy: from gene expression to drug discovery. Curr. Pharm. Des. 2009, 15:3839-3843.
10. Semenza G.L. HIF-1: upstream and downstream of cancer metabolism. Curr. Opin. Genet. Dev. 2010, 20:51-56.
11. Harvey J.J. An unidentified virus which causes the rapid production of tumours in mice. Nature 1964, 204:1104-1105.
12. Kirsten W.H., Schauf V., McCoy J. Properties of a murine sarcoma virus. Bibl. Haematol. 1970, 246-249.
13. Cooper G.M. Cellular transforming genes. Science 1982, 217:801-806.
14. Taparowsky E., Shimizu K., Goldfarb M., Wigler M. Structure and activation of the human N-ras gene. Cell 1983, 34:581-586.
15. Buday L., Downward J. Many faces of Ras activation. Biochim. Biophys. Acta 2008, 1786:178-187.
16. Shaw R.J., Cantley L.C. Ras, PI(3)K and mTOR signalling controls tumour cell growth. Nature 2006, 441:424-430.
17. Lievre A., Bachet J.B., Le C.D., Boige V., Landi B., Emile J.F., Cote J.F., Tomasic G., Penna C., Ducreux M., Rougier P., Penault-Llorca F., Laurent-Puig P. KRAS mutation status is predictive of response to cetuximab therapy in colorectal cancer. Cancer Res. 2006, 66:3992-3995.
18. Di F.F., Blanchard F., Charbonnier F., Le P.F., Lamy A., Galais M.P., Bastit L., Killian A., Sesboue R., Tuech J.J., Queuniet A.M., Paillot B., Sabourin J.C., Michot F., Michel P., Frebourg T. Clinical relevance of KRAS mutation detection in metastatic colorectal cancer treated by cetuximab plus chemotherapy. Br. J. Cancer 2007, 96:1166-1169.
19. Khambata-Ford S., Garrett C.R., Meropol N.J., Basik M., Harbison C.T., Wu S., Wong T.W., Huang X., Takimoto C.H., Godwin A.K., Tan B.R., Krishnamurthi S.S., Burris H.A., Poplin E.A., Hidalgo M., Baselga J., Clark E.A., Mauro D.J. Expression of epiregulin and amphiregulin and K-ras mutation status predict disease control in metastatic colorectal cancer patients treated with cetuximab. J. Clin. Oncol. 2007, 25:3230-3237.
20. Karapetis C.S., Khambata-Ford S., Jonker D.J., O'Callaghan C.J., Tu D., Tebbutt N.C., Simes R.J., Chalchal H., Shapiro J.D., Robitaille S., Price T.J., Shepherd L., Au H.J., Langer C., Moore M.J., Zalcberg J.R. K-ras mutations and benefit from cetuximab in advanced colorectal cancer. N. Engl. J. Med. 2008, 359:1757-1765.
21. Amado R.G., Wolf M., Peeters M., Van C.E., Siena S., Freeman D.J., Juan T., Sikorski R., Suggs S., Radinsky R., Patterson S.D., Chang D.D. Wild-type KRAS is required for panitumumab efficacy in patients with metastatic colorectal cancer. J. Clin. Oncol. 2008, 26:1626-1634.
22. Lievre A., Bachet J.B., Boige V., Cayre A., Le C.D., Buc E., Ychou M., Bouche O., Landi B., Louvet C., Andre T., Bibeau F., Diebold M.D., Rougier P., Ducreux M., Tomasic G., Emile J.F., Penault-Llorca F., Laurent-Puig P. KRAS mutations as an independent prognostic factor in patients with advanced colorectal cancer treated with cetuximab. J. Clin. Oncol. 2008, 26:374-379.
23. Freeman D.J., Juan T., Reiner M., Hecht J.R., Meropol N.J., Berlin J., Mitchell E., Sarosi I., Radinsky R., Amado R.G. Association of K-ras mutational status and clinical outcomes in patients with metastatic colorectal cancer receiving panitumumab alone. Clin. Colorectal Cancer 2008, 7:184-190.
24. Van C.E., Kohne C.H., Hitre E., Zaluski J., Chang Chien C.R., Makhson A., D'Haens G., Pinter T., Lim R., Bodoky G., Roh J.K., Folprecht G., Ruff P., Stroh C., Tejpar S., Schlichting M., Nippgen J., Rougier P. Cetuximab and chemotherapy as initial treatment for metastatic colorectal cancer. N. Engl. J. Med. 2009, 360:1408-1417.
25. Jimeno A., Messersmith W.A., Hirsch F.R., Franklin W.A., Eckhardt S.G. KRAS mutations and sensitivity to epidermal growth factor receptor inhibitors in colorectal cancer: practical application of patient selection. J. Clin. Oncol. 2009, 27:1130-1136.
26. Allegra C.J., Jessup J.M., Somerfield M.R., Hamilton S.R., Hammond E.H., Hayes D.F., McAllister P.K., Morton R.F., Schilsky R.L. American Society of Clinical Oncology provisional clinical opinion: testing for KRAS gene mutations in patients with metastatic colorectal carcinoma to predict response to anti-epidermal growth factor receptor monoclonal antibody therapy. J. Clin. Oncol. 2009, 27:2091-2096.
27. Leon J., Guerrero I., Pellicer A. Differential expression of the ras gene family in mice. Mol. Cell. Biol. 1987, 7:1535-1540.
28. Fiorucci G., Hall A. All three human ras genes are expressed in a wide range of tissues. Biochim. Biophys. Acta 1988, 950:81-83.
29. Lea I.A., Jackson M.A., Li X., Bailey S., Peddada S.D., Dunnick J.K. Genetic pathways and mutation profiles of human cancers: site- and exposure-specific patterns. Carcinogenesis 2007, 28:1851-1858.
30. Anderson J.A., Irish J.C., McLachlin C.M., Ngan B.Y. H-ras oncogene mutation and human papillomavirus infection in oral carcinomas. Arch. Otolaryngol. Head Neck Surg. 1994, 120:755-760.
31. Boguski M.S., McCormick F. Proteins regulating Ras and its relatives. Nature 1993, 366:643-654.
32. Lu Y., Liang K., Li X., Fan Z. Responses of cancer cells with wild-type or tyrosine kinase domain-mutated epidermal growth factor receptor (EGFR) to EGFR-targeted therapy are linked to downregulation of hypoxia-inducible factor-1alpha. Mol. Cancer 2007, 6:63.
33. Fan Z., Baselga J., Masui H., Mendelsohn J. Antitumor effect of anti-epidermal growth factor receptor monoclonal antibodies plus cis-diamminedichloroplatinum on well established A431 cell xenografts. Cancer Res. 1993, 53:4637-4642.
34. Jin W., Wu L., Liang K., Liu B., Lu Y., Fan Z. Roles of the PI-3K and MEK pathways in Ras-mediated chemoresistance in breast cancer cells. Br. J. Cancer 2003, 89:185-191.
35. Post D.E., Van Meir E.G. Generation of bidirectional hypoxia/HIF-responsive expression vectors to target gene expression to hypoxic cells. Gene Ther. 2001, 8:1801-1807.
36. Luwor R.B., Lu Y., Li X., Mendelsohn J., Fan Z. The antiepidermal growth factor receptor monoclonal antibody cetuximab/C225 reduces hypoxia-inducible factor-1 alpha, leading to transcriptional inhibition of vascular endothelial growth factor expression. Oncogene 2005, 24:4433-4441.
37. Luwor R.B., Johns T.G., Murone C., Huang H.J., Cavenee W.K., Ritter G., Old L.J., Burgess A.W., Scott A.M. Monoclonal antibody 806 inhibits the growth of tumor xenografts expressing either the de2-7 or amplified epidermal growth factor receptor (EGFR) but not wild-type EGFR. Cancer Res. 2001, 61:5355-5361.
38. Liang K., Ang K.K., Milas L., Hunter N., Fan Z. The epidermal growth factor receptor mediates radioresistance. Int. J. Radiat. Oncol. Biol. Phys. 2003, 57:246-254.
39. Liu B., Fang M., Lu Y., Mendelsohn J., Fan Z. Fibroblast growth factor and insulin-like growth factor differentially modulate the apoptosis and G1 arrest induced by anti-epidermal growth factor receptor monoclonal antibody. Oncogene 2001, 20:1913-1922.
40. Li X., Lu Y., Liang K., Pan T., Mendelsohn J., Fan Z. Requirement of hypoxia-inducible factor-1alpha down-regulation in mediating the antitumor activity of the anti-epidermal growth factor receptor monoclonal antibody cetuximab. Mol. Cancer Ther. 2008, 7:1207-1217.
41. Baselga J., Norton L., Masui H., Pandiella A., Coplan K., Miller W.H., Mendelsohn J. Antitumor effects of doxorubicin in combination with anti-epidermal growth factor receptor monoclonal antibodies. J. Natl. Cancer Inst. 1993, 85:1327-1333.
42. Ciardiello F., Caputo R., Bianco R., Damiano V., Pomatico G., De Placido S., Bianco A.R., Tortora G. Antitumor effect and potentiation of cytotoxic drugs activity in human cancer cells by ZD-1839 (Iressa), an epidermal growth factor receptor-selective tyrosine kinase inhibitor. Clin. Cancer Res. 2000, 6:2053-2063.
43. Sirotnak F.M., Zakowski M.F., Miller V.A., Scher H.I., Kris M.G. Efficacy of cytotoxic agents against human tumor xenografts is markedly enhanced by coadministration of ZD1839 (Iressa), an inhibitor of EGFR tyrosine kinase. Clin. Cancer Res. 2000, 6:4885-4892.
44. Hasui M., Saikawa Y., Miura M., Takano N., Ueno Y., Yachie A., Miyawaki T., Taniguchi N. Effector and precursor phenotypes of lymphokine-activated killer cells in mice with severe combined immunodeficiency (scid) and athymic (nude) mice. Cell. Immunol. 1989, 120:230-239.
45. Bleeker W.K., Lammerts van Bueren J.J., van Ojik H.H., Gerritsen A.F., Pluyter M., Houtkamp M., Halk E., Goldstein J., Schuurman J., van Dijk M.A., van de Winkel J.G., Parren P.W. Dual mode of action of a human anti-epidermal growth factor receptor monoclonal antibody for cancer therapy. J. Immunol. 2004, 173:4699-4707.
46. Bos J.L. The ras gene family and human carcinogenesis. Mutat. Res. 1988, 195:255-271.
47. Downward J. Targeting RAS signalling pathways in cancer therapy. Nat. Rev. Cancer 2003, 3:11-22.
48. Cunningham D., Humblet Y., Siena S., Khayat D., Bleiberg H., Santoro A., Bets D., Mueser M., Harstrick A., Verslype C., Chau I., Van Cutsem E. Cetuximab monotherapy and cetuximab plus irinotecan in irinotecan-refractory metastatic colorectal cancer. N. Engl. J Med. 2004, 351:337-345.
49. Vakiani E., Solit D.B. KRAS and BRAF: drug targets and predictive biomarkers. J. Pathol. 2011, 223:219-229.
50. Zoppoli G., Moran E., Soncini D., Cea M., Garuti A., Rocco I., Cirmena G., Grillo V., Bagnasco L., Icardi G., Ansaldi F., Parodi S., Patrone F., Ballestrero A., Nencioni A. Ras-induced resistance to lapatinib is overcome by MEK inhibition. Curr. Cancer Drug Targets 2010, 10:168-175.
51. Lu Y., Li X., Lu H., Fan Z. 1, 9-Pyrazoloanthrones downregulate HIF-1alpha and sensitize cancer cells to cetuximab-mediated anti-EGFR therapy. PLoS One 2010, 5:e15823.