Preclinical modeling of EGFR-specific antibody resistance: Oncogenic and immune-associated escape mechanisms

Oncogene

Volumn 33, Issue 24, 2014, Pages 3129-3139

  Garrido, G ^a   Rabasa, A ^a   Garrido, C ^b,c   Lopez A ^a   Chao, L ^a   Garcia Lora A M ^b   Garrido, F ^b,c   Fernandez L E ^a   Sanchez B ^a  

^a CENTER OF MOLECULAR IMMUNOLOGY   (Cuba)

^b Department of Analisis Clinicos and Inmunologia Hospital Universitario VirgenNieves   (Spain)

^c UNIVERSITY OF GRANADA   (Spain)

Author keywords

EGFR; MHC I alterations; monoclonal antibodies; resistance

Indexed keywords

4 (3 CHLOROANILINO) 6,7 DIMETHOXYQUINAZOLINE; 7A7; ANTINEOPLASTIC AGENT; BETA 2 MICROGLOBULIN; EPIDERMAL GROWTH FACTOR RECEPTOR; GAMMA INTERFERON; HER3 PROTEIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN; PROTEIN KINASE B; STAT3 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTATION; APOPTOSIS; ARTICLE; CANCER RESISTANCE; CELL CYCLE PROGRESSION; CELL INVASION; CELL VIABILITY; CONTROLLED STUDY; FEMALE; GENETIC VARIABILITY; HEAVY CHAIN; IN VITRO STUDY; IN VIVO STUDY; MAJOR HISTOCOMPATIBILITY COMPLEX; METASTASIS; MOUSE; NONHUMAN; OVERALL SURVIVAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

MURINAE; MUS;

ANIMALS; ANTIBODIES, MONOCLONAL; APOPTOSIS; BLOTTING, WESTERN; CARCINOMA, LEWIS LUNG; CELL MOVEMENT; CELL PROLIFERATION; DRUG RESISTANCE, NEOPLASM; FEMALE; FLOW CYTOMETRY; IMMUNOENZYME TECHNIQUES; INTERFERON-GAMMA; LUNG NEOPLASMS; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED C57BL; MICE, NUDE; NEOPLASM INVASIVENESS; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTOR, EPIDERMAL GROWTH FACTOR; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; T-LYMPHOCYTES, CYTOTOXIC; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84902518844     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2013.288     Document Type: Article

References (48)

1. Yarden Y, Pines G. The ERBB network: at last, cancer therapy meets systems biology. Nat Rev Cancer 2012; 12: 553-563.
2. Reichert JM, Dhimolea E. The future of antibodies as cancer drugs. Drug Discov Today 2012; 17: 954-963.
3. Perez R, Moreno E, Garrido G, Crombet T. EGFR-targeting as a biological therapy: understanding nimotuzumab's clinical effects. Cancers 2011; 3: 2014-2031.
4. Amado RG, Wolf M, Peeters M, Van Cutsem E, Siena S, Freeman DJ et al. Wild-type KRAS is required for panitumumab efficacy in patients with metastatic colorectal cancer. J Clin Oncol 2008; 26: 1626-1634.
5. Karapetis CS, Khambata-Ford S, Jonker DJ, O'Callaghan CJ, Tu D, Tebbutt NC et al. K-ras mutations and benefit from cetuximab in advanced colorectal cancer. N Engl J Med 2008; 359: 1757-1765.
6. Van Cutsem E, Kohne CH, Hitre E, Zaluski J, Chang Chien CR, Makhson A et al. Cetuximab and chemotherapy as initial treatment for metastatic colorectal cancer. N Engl J Med 2009; 360: 1408-1417.
7. Bokemeyer C, Bondarenko I, Makhson A, Hartmann JT, Aparicio J, de Braud F et al. Fluorouracil, leucovorin, and oxaliplatin with and without cetuximab in the firstline treatment of metastatic colorectal cancer. J Clin Oncol 2009; 27: 663-671.
8. Douillard JY, Siena S, Cassidy J, Tabernero J, Burkes R, Barugel M et al. Randomized, phase III trial of panitumumab with infusional fluorouracil, leucovorin, and oxaliplatin (FOLFOX4) versus FOLFOX4 alone as first-line treatment in patients with previously untreated metastatic colorectal cancer: the PRIME study. J Clin Oncol 2010; 28: 4697-4705.
9. Peeters M, Price TJ, Cervantes A, Sobrero AF, Ducreux M, Hotko Y et al. Randomized phase III study of panitumumab with fluorouracil, leucovorin, and irinotecan (FOLFIRI) compared with FOLFIRI alone as s-line treatment in patients with metastatic colorectal cancer. J Clin Oncol 2010; 28: 4706-4713.
10. Brand TM, Iida M, Wheeler DL. Molecular mechanisms of resistance to the EGFR monoclonal antibody cetuximab. Cancer Biol Ther 2011; 11: 777-792.
11. Correale P, Botta C, Cusi MG, Del Vecchio MT, De Santi MM, Gori Savellini G et al. Cetuximab /- chemotherapy enhances dendritic cell-mediated phagocytosis of colon cancer cells and ignites a highly efficient colon cancer antigen-specific cytotoxic T-cell response in vitro. Int J Cancer 2012; 130: 1577-1589.
12. Yang X, Zhang X, Mortenson ED, Radkevich-Brown O, Wang Y, Fu YX. Cetuximabmediated tumor regression depends on innate and adaptive immune responses. Mol Ther 2012; 21: 91-100.
13. Srivastava RM, Lee SC, Andrade Filho PA, Lord CA, Jie HB, Davidson C et al. Cetuximab-activated natural killer (NK) and dendritic cells (DC) collaborate to trigger tumor antigen-specific T cell immunity in head and neck cancer patients. Clin Cancer Res 2013; 19: 1858-1872.
14. Garrido G, Sanchez B, Rodriguez HM, Lorenzano P, Alonso D, Fernandez LE. 7A7 MAb: a new tool for the pre-clinical evaluation of EGFR-based therapies. Hybrid Hybridomics 2004; 23: 168-175.
15. Talavera A, Mackenzie J, Garrido G, Friemann R, Lopez-Requena A, Moreno E et al. Structure of the Fab fragment of the anti-murine EGFR antibody 7A7 and exploration of its receptor binding site. Mol Immunol 2011; 48: 1578-1585.
16. Garrido G, Lorenzano P, Sanchez B, Beausoleil I, Alonso DF, Perez R et al. T cells are crucial for the anti-metastatic effect of anti-epidermal growth factor receptor antibodies. Cancer Immunol Immunother 2007; 56: 1701-1710.
17. Garrido G, Rabasa A, Sanchez B, Lopez MV, Blanco R, Lopez A et al. Induction of immunogenic apoptosis by blockade of epidermal growth factor receptor activation with a specific antibody. J Immunol 2011; 187: 4954-4966.
18. Kelly-Spratt KS, Philipp-Staheli J, Gurley KE, Hoon-Kim K, Knoblaugh S, Kemp CJ. Inhibition of PI-3K restores nuclear p27Kip1 expression in a mouse model of Kras-driven lung cancer. Oncogene 2009; 28: 3652-3662.
19. Chu IM, Hengst L, Slingerland JM. The Cdk inhibitor p27 in human cancer: prognostic potential and relevance to anticancer therapy. Nat Rev Cancer 2008; 8: 253-267.
20. Ishizawar RC, Miyake T, Parsons SJ. c-Src modulates ErbB2 and ErbB3 heterocomplex formation and function. Oncogene 2007; 26: 3503-3510.
21. Akiyama T, Matsuda S, Namba Y, Saito T, Toyoshima K, Yamamoto T. The transforming potential of the c-erbB-2 protein is regulated by its autophosphorylation at the carboxyl-terminal domain. Mol Cell Biol 1991; 11: 833-842.
22. Wheeler DL, Iida M, Dunn EF. The role of Src in solid tumors. Oncologist 2009; 14: 667-678.
23. Rabinovich GA, Gabrilovich D, Sotomayor EM. Immunosuppressive strategies that are mediated by tumor cells. Annu Rev Immunol 2007; 25: 267-296.
24. Seliger B, Ruiz-Cabello F, Garrido F. IFN inducibility of major histocompatibility antigens in tumors. Adv Cancer Res 2008; 101: 249-276.
25. Erjala K, Sundvall M, Junttila TT, Zhang N, Savisalo M, Mali P et al. Signaling via ErbB2 and ErbB3 associates with resistance and epidermal growth factor receptor (EGFR) amplification with sensitivity to EGFR inhibitor gefitinib in head and neck squamous cell carcinoma cells. Clin Cancer Res 2006; 12: 4103-4111.
26. Engelman JA, Zejnullahu K, Mitsudomi T, Song Y, Hyland C, Park JO et al. MET amplification leads to gefitinib resistance in lung cancer by activating ERBB3 signaling. Science 2007; 316: 1039-1043.
27. Wheeler DL, Huang S, Kruser TJ, Nechrebecki MM, Armstrong EA, Benavente S et al. Mechanisms of acquired resistance to cetuximab: role of HER (ErbB) family members. Oncogene 2008; 27: 3944-3956.
28. Sergina NV, Rausch M, Wang D, Blair J, Hann B, Shokat KM et al. Escape from HER-family tyrosine kinase inhibitor therapy by the kinase-inactive HER3. Nature 2007; 445: 437-441.
29. Yarden Y, Sliwkowski MX. Untangling the ErbB signalling network. Nat Rev Mol Cell Biol 2001; 2: 127-137.
30. Kim SM, Kim JS, Kim JH, Yun CO, Kim EM, Kim HK et al. Acquired resistance to cetuximab is mediated by increased PTEN instability and leads cross-resistance to gefitinib in HCC827 NSCLC cells. Cancer Lett 2010; 296: 150-159.
31. Garrido F, Ruiz-Cabello F, Cabrera T, Perez-Villar JJ, Lopez-Botet M, Duggan-Keen M et al. Implications for immunosurveillance of altered HLA class I phenotypes in human tumours. Immunol Today 1997; 18: 89-95.
32. Aptsiauri N, Cabrera T, Garcia-Lora A, Lopez-Nevot MA, Ruiz-Cabello F, Garrido F. MHC class I antigens and immune surveillance in transformed cells. Int Rev Cytol 2007; 256: 139-189.
33. Garrido F, Cabrera T, Aptsiauri N. 'Hard' and 'soft' lesions underlying the HLA class I alterations in cancer cells: implications for immunotherapy. Int J Cancer 2010; 127: 249-256.
34. Garcia-Lora A, Martinez M, Algarra I, Gaforio JJ, Garrido F. MHC class I-deficient metastatic tumor variants immunoselected by T lymphocytes originate from the coordinated downregulation of APM components. Int J Cancer 2003; 106: 521-527.
35. Meissner M, Reichert TE, Kunkel M, Gooding W, Whiteside TL, Ferrone S et al. Defects in the human leukocyte antigen class I antigen processing machinery in head and neck squamous cell carcinoma: association with clinical outcome. Clin Cancer Res 2005; 11: 2552-2560.
36. Romero JM, Jimenez P, Cabrera T, Cozar JM, Pedrinaci S, Tallada M et al. Coordinated downregulation of the antigen presentation machinery and HLA class I/beta2-microglobulin complex is responsible for HLA-ABC loss in bladder cancer. Int J Cancer 2005; 113: 605-610.
37. Duncan TJ, Rolland P, Deen S, Scott IV, Liu DT, Spendlove I et al. Loss of IFN gamma receptor is an independent prognostic factor in ovarian cancer. Clin Cancer Res 2007; 13: 4139-4145.
38. Abril E, Real LM, Serrano A, Jimenez P, Garcia A, Canton J et al. Unresponsiveness to interferon associated with STAT1 protein deficiency in a gastric adenocarcinoma cell line. Cancer Immunol Immunother 1998; 47: 113-120.
39. Xi S, Dyer KF, Kimak M, Zhang Q, Gooding WE, Chaillet JR et al. Decreased STAT1 expression by promoter methylation in squamous cell carcinogenesis. J Natl Cancer Inst 2006; 98: 181-189.
40. Groettrup M, Standera S, Stohwasser R, Kloetzel PM. The subunits MECL-1 and LMP2 are mutually required for incorporation into the 20S proteasome. Proc Natl Acad Sci USA 1997; 94: 8970-8975.
41. Herrmann F, Lehr HA, Drexler I, Sutter G, Hengstler J, Wollscheid U et al. HER-2/ neu-mediated regulation of components of the MHC class I antigen-processing pathway. Cancer Res 2004; 64: 215-220.
42. Romero I, Martinez M, Garrido C, Collado A, Algarra I, Garrido F et al. The tumour suppressor Fhit positively regulates MHC class I expression on cancer cells. J Pathol 2012; 227: 367-379.
43. Bianchi F, Magnifico A, Olgiati C, Zanesi N, Pekarsky Y, Tagliabue E et al. FHIT-proteasome degradation caused by mitogenic stimulation of the EGF receptor family in cancer cells. Proc Natl Acad Sci USA 2006; 103: 18981-18986.
44. Garrido C, Paco L, Romero I, Berruguilla E, Stefansky J, Collado A et al. MHC class I molecules act as tumor suppressor genes regulating the cell cycle gene expression, invasion and intrinsic tumorigenicity of melanoma cells. Carcinogenesis 2012; 33: 687-693.
45. 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.
46. Eisenbach L, Hollander N, Greenfeld L, Yakor H, Segal S, Feldman M. The differential expression of H-2K versus H-2D antigens, distinguishing high-metastatic from low-metastatic clones, is correlated with the immunogenic properties of the tumor cells. Int J Cancer 1984; 34: 567-573.
47. Porgador A, Brenner B, Vadai E, Feldman M, Eisenbach L. Immunization by gamma-IFN-treated B16-F10.9 melanoma cells protects against metastatic spread of the parental tumor. Int J Cancer Suppl 1991; 6: 54-60.
48. Garrido C, Algarra I, Maleno I, Stefanski J, Collado A, Garrido F et al. Alterations of HLA class I expression in human melanoma xenografts in immunodeficient mice occur frequently and are associated with higher tumorigenicity. Cancer Immunol Immunother 2010; 59: 13-26.