In pancreatic carcinoma, dual EGFR/HER2 targeting with cetuximab/trastuzumab is more effective than treatment with trastuzumab/ erlotinib or lapatinib alone: Implication of receptors' down-regulation and dimers' disruption

Neoplasia

Volumn 14, Issue 2, 2012, Pages 121-130

  Larbouret, Christel ^a,b,c   Gaborit, Nadège ^a,b,c   Chardès, Thierry ^a,b,c   Coelho, Mickaël ^a,b,c   Campigna, Emmanuelle ^a,b,c   Bascoul Mollevi, Caroline ^c   Mach, Jean Pierre ^d   Azria, David ^a,b,c   Robert, Bruno ^a,b,c   Pèlegrin, André ^a,b,c  

^a INSTITUT DE RECHERCHE EN CANCÉROLOGIE DE MONTPELLIER   (France)

^b UNIV MONTPELLIER   (France)

^c CENTRE VAL D AURELLE   (France)

^d UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CETUXIMAB; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; ERLOTINIB; LAPATINIB; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE B; TRASTUZUMAB;

ANIMAL EXPERIMENT; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ARTICLE; BODY WEIGHT; CANCER CELL CULTURE; CANCER INHIBITION; CELL PROLIFERATION; CONTROLLED STUDY; DRUG EFFICACY; DRUG MEGADOSE; FEMALE; FLUORESCENCE RESONANCE ENERGY TRANSFER; IC 50; MOUSE; NONHUMAN; PANCREAS CARCINOMA; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR DOWN REGULATION; SURVIVAL; TUMOR GROWTH; TUMOR VOLUME; TUMOR XENOGRAFT; WESTERN BLOTTING;

EID: 84858013723     PISSN: 15228002     EISSN: 14765586     Source Type: Journal    
DOI: 10.1593/neo.111602     Document Type: Article

References (39)

1. Azria D, Ychou M, Jacot W, Thezenas S, Lemanski C, Senesse P, Prost P, Delard R, Masson B, and Dubois JB (2002). Treatment of unresectable, locally advanced pancreatic adenocarcinoma with combined radiochemotherapy with 5-fluorouracil and cisplatin. Pancreas 25, 360-365.
2. Nelson NJ (2007). Pancreatic cancer research matures. J Natl Cancer Inst 99, 1432-1434.
3. Jones S, Zhang X, Parsons DW, Lin JCH, Leary RJ, Angenendt P, Mankoo P, Carter H, Kamiyama H, Jimeno A, et al. (2008). Core signaling pathways in human pancreatic cancers revealed by global genomic analyses. Science 321, 1801-1806.
4. Wong HH and Lemoine NR (2009). Pancreatic cancer: molecular pathogenesis and new therapeutic targets. Nat Rev Gastroenterol Hepatol 6, 412-422.
5. Huang ZQ and Buchsbaum DJ (2009). Monoclonal antibodies in the treatment of pancreatic cancer. Immunotherapy 1, 223-239.
6. Larbouret C, Robert B, Navarro-Teulon I, Thèzenas S, Ladjemi MZ, Morisseau S, Campigna E, Bibeau F, Mach JP, Pèlegrin A, et al. (2007). In vivo therapeutic synergism of anti-epidermal growth factor receptor and anti-HER2 monoclonal antibodies against pancreatic carcinomas. Clin Cancer Res 13, 3356-3362.
7. Yamanaka Y, Friess H, Kobrin MS, Buchler M, Beger HG, and Korc M (1993). Coexpression of epidermal growth factor receptor and ligands in human pancreatic cancer is associated with enhanced tumor aggressiveness. Anticancer Res 13, 565-569.
8. Safran H, Steinhoff M, Mangray S, Rathore R, King TC, Chai L, Berzein K, Moore T, Iannitti D, Reiss P, et al. (2001). Overexpression of the HER-2/neu oncogene in pancreatic adenocarcinoma. Am J Clin Oncol 24, 496-499.
9. Yarden Y and Sliwkowski MX (2001). Untangling the ErbB signalling network. Nat Rev Mol Cell Biol 2, 127-137.
10. Moore MJ, Goldstein D, Hamm J, Figer A, Hecht JR, Gallinger S, Au HJ, Murawa P, Walde D, Wolff RA, et al. (2007). Erlotinib plus gemcitabine compared with gemcitabine alone in patients with advanced pancreatic cancer: a phase III trial of the National Cancer Institute of Canada Clinical Trials Group. J Clin Oncol 25, 1960-1966.
11. Safran H, Miner T, Resnick M, Dipetrillo T, McNulty B, Evans D, Joseph P, Plette A, Millis R, Sears D, et al. (2008). Lapatinib/gemcitabine and lapatinib/ gemcitabine/oxaliplatin: a phase I study for advanced pancreaticobiliary cancer. Am J Clin Oncol 31, 140-144.
12. Larbouret C, Robert B, Bascoul-Mollevi C, Penault-Llorca F, Ho-Pun-Cheung A, Morisseau S, Navarro-Teulon I, Mach JP, Pèlegrin A, and Azria D (2010). Combined cetuximab and trastuzumab are superior to gemcitabine in the treatment of human pancreatic carcinoma xenografts. Ann Oncol 21, 98-103.
13. Germain C, Larbouret C, Cesson V, Donda A, Held W, Mach JP, Pèlegrin A, and Robert B (2005). MHC class I-related chain A conjugated to antitumor antibodies can sensitize tumor cells to specific lysis by natural killer cells. Clin Cancer Res 11, 7516-7522.
14. Gaborit N, Larbouret C, Vallaghe J, Peyrusson F, Bascoul-Mollevi C, Crapez E, Azria D, Chardès T, Poul MA, Mathis G, et al. (2011). Time-resolved fluorescence resonance energy transfer (TR-FRET) to analyze the disruption of EGFR/ HER2 dimers: a new method to evaluate the efficiency of targeted therapy using monoclonal antibodies. J Biol Chem 286, 11337-11345.
15. Vogel CA, Bischof-Delaloye A, Mach JP, Pèlegrin A, Hardman N, Delaloye B, and Buchegger F (1993). Direct comparison of a radioiodinated intact chimeric anti-CEA MAb with its F(ab')2 fragment in nude mice bearing different human colon cancer xenografts. Br J Cancer 68, 684-690.
16. Clynes RA, Towers TL, Presta LG, and Ravetch JV (2000). Inhibitory Fc receptors modulate in vivo cytotoxicity against tumor targets. Nat Med 6, 443-446.
17. Roopenian DC and Akilesh S (2007). FcRn: the neonatal Fc receptor comes of age. Nat Rev Immunol 7, 715-725.
18. Karapetis CS, Khambata-Ford S, Jonker DJ, O'Callaghan CJ, Tu D, Tebbutt NC, Simes RJ, Chalchal H, Shapiro JD, Robitaille S, et al. (2008). K-ras mutations and benefit from cetuximab in advanced colorectal cancer. N Engl J Med 359, 1757-1765.
19. da Cunha Santos G, Dhani N, Tu D, Chin K, Ludkovski O, Kamel-Reid S, Squire J, Parulekar W, Moore MJ, and Tsao MS (2010). Molecular predictors of outcome in a phase 3 study of gemcitabine and erlotinib therapy in patients with advanced pancreatic cancer: National Cancer Institute of Canada Clinical Trials Group Study PA.3. Cancer 116, 5599-5607.
20. Normanno N, Campiglio M, de LA, Somenzi G, Maiello M, Ciardiello F, Gianni L, Salomon DS, and Menard S (2002). Cooperative inhibitory effect of ZD1839 (Iressa) in combination with trastuzumab (Herceptin) on human breast cancer cell growth. Ann Oncol 13, 65-72.
21. Huang S, Armstrong EA, Benavente S, Chinnaiyan P, and Harari PM (2004). Dual-agent molecular targeting of the epidermal growth factor receptor (EGFR): combining anti-EGFR antibody with tyrosine kinase inhibitor. Cancer Res 64, 5355-5362.
22. Karaman MW, Herrgard S, Treiber DK, Gallant P, Atteridge CE, Campbell BT, Chan KW, Ciceri P, Davis MI, Edeen PT, et al. (2008). A quantitative analysis of kinase inhibitor selectivity. Nat Biotechnol 26, 127-132.
23. Frolov A, Schuller K, Tzeng CWD, Cannon EE, Ku BC, Howard JH, Vickers SM, Heslin MJ, Buchsbaum DJ, and Arnoletti JP (2007). ErbB3 expression and dimerization with EGFR influence pancreatic cancer cell sensitivity to erlotinib. Cancer Biol Ther 6, 548-554.
24. Buck E, Eyzaguirre A, Haley JD, Gibson NW, Cagnoni P, and Iwata KK (2006). Inactivation of Akt by the epidermal growth factor receptor inhibitor erlotinib is mediated by HER-3 in pancreatic and colorectal tumor cell lines and contributes to erlotinib sensitivity. Mol Cancer Ther 5, 2051-2059.
25. Komoto M, Nakata B, Nishii T, Kawajiri H, Shinto O, Amano R, Yamada N, Yashiro M, and Hirakawa K (2010). In vitro and in vivo evidence that a combination of lapatinib plus S-1 is a promising treatment for pancreatic cancer. Cancer Sci 101, 468-473.
26. Kimple RJ, Vaseva AV, Cox AD, Baerman KM, Calvo BF, Tepper JE, Shields JM, and Sartor CI (2010). Radiosensitization of epidermal growth factor receptor/ HER2-positive pancreatic cancer is mediated by inhibition of Akt independent of ras mutational status. Clin Cancer Res 16, 912-923.
27. Rusnak DW, Alligood KJ, Mullin RJ, Spehar GM, Arenas-Elliott C, Martin AM, Degenhardt Y, Rudolph SK, Haws TF Jr, Hudson-Curtis BL, et al. (2007). Assessment of epidermal growth factor receptor (EGFR, ErbB1) and HER2 (ErbB2) protein expression levels and response to lapatinib (Tykerb, GW572016) in an expanded panel of human normal and tumour cell lines. Cell Prolif 40, 580-594.
28. Wainberg ZA, Anghel A, Desai AJ, Ayala R, Luo T, Safran B, Fejzo MS, Hecht JR, Slamon DJ, and Finn RS (2010). Lapatinib, a dual EGFR and HER2 kinase inhibitor, selectively inhibits HER2-amplified human gastric cancer cells and is synergistic with trastuzumab in vitro and in vivo. Clin Cancer Res 16, 1509-1519.
29. Scaltriti M, Verma C, Guzman M, Jimenez J, Parra JL, Pedersen K, Smith DJ, Landolfi S, Ramon y Cajal S, Arribas J, et al. (2009). Lapatinib, a HER2 tyrosine kinase inhibitor, induces stabilization and accumulation of HER2 and potentiates trastuzumab-dependent cell cytotoxicity. Oncogene 28, 803-814.
30. Ben-Kasus T, Schechter B, Lavi S, Yarden Y, and Sela M (2009). Persistent elimination of ErbB-2/HER2-overexpressing tumors using combinations of monoclonal antibodies: relevance of receptor endocytosis. Proc Natl Acad Sci USA 106, 3294-3299.
31. Ji Z, Mei FC, Xie J, and Cheng X (2007). Oncogenic KRAS activates hedgehog signaling pathway in pancreatic cancer cells. J Biol Chem 282, 14048-14055.
32. Rinehart J, Adjei AA, Lorusso PM, Waterhouse D, Hecht JR, Natale RB, Hamid O, Varterasian M, Asbury P, Kaldjian EP, et al. (2004). Multicenter phase II study of the oral MEK inhibitor, CI-1040, in patients with advanced non-small-cell lung, breast, colon, and pancreatic cancer. J Clin Oncol 22, 4456-4462.
33. Jimeno A, Rubio-Viqueira B, Amador ML, Grunwald V, Maitra A, Iacobuzio-Donahue C, and Hidalgo M (2007). Dual mitogen-activated protein kinase and epidermal growth factor receptor inhibition in biliary and pancreatic cancer. Mol Cancer Ther 6, 1079-1088.
34. Meira DD, de Almeida VH, Mororó JS, Nóbrega I, Bardella L, Silva RLA, Albano RM, and Ferreira CG (2009). Combination of cetuximab with chemo-radiation, trastuzumab or MAPK inhibitors: mechanisms of sensitisation of cervical cancer cells. Br J Cancer 101, 782-791.
35. Ghosh R, Narasanna A, Wang SE, Liu S, Chakrabarty A, Balko JM, González-Angulo AM, Mills GB, Penuel E, Winslow J, et al. (2011). Trastuzumab has preferential activity against breast cancers driven by HER2 homodimers. Cancer Res 71, 1871-1882.
36. Carpentier JL, White MF, Orci L, and Kahn RC (1987). Direct visualization of the phosphorylated epidermal growth factor receptor during its internalization in A-431 cells. J Cell Biol 105, 2751-2762.
37. Baulida J, Kraus MH, Alimandi M, Di Fiore PP, and Carpenter G (1996). All ErbB receptors other than the epidermal growth factor receptor are endocytosis impaired. J Biol Chem 271, 5251-5257.
38. Wang Z, Zhang L, Yeung TK, and Chen X (1999). Endocytosis deficiency of epidermal growth factor (EGF) receptor-ErbB2 heterodimers in response to EGF stimulation. Mol Biol Cell 10, 1621-1636.
39. Wilkinson JC and Staros JV (2002). Effect of ErbB2 coexpression on the kinetic interactions of epidermal growth factor with its receptor in intact cells. Biochemistry 41, 8-14.