Preclinical validation of AXL receptor as a target for antibody-based pancreatic cancer immunotherapy

Oncogene

Volumn 33, Issue 47, 2014, Pages 5405-5414

  Leconet, W ^a   Larbouret, C ^a   Chardes T ^a   Thomas, G ^a   Neiveyans, M ^a   Busson, M ^a   Jarlier, M ^b   Radosevic Robin, N ^c,d   Pugniere M ^a   Bernex, F ^a   Penault Llorca, F ^c,d   Pasquet, J M ^a   Pelegrin A ^a   Robert, B ^a  

^a INSERM   (France)

^b CENTRE VAL D AURELLE   (France)

^c CENTRE JEAN PERRIN   (France)

^d UNIVERSITÉ CLERMONT AUVERGNE   (France)

Author keywords

monoclonal antibodies; pancreatic cancer; RTK; targeted therapy

Indexed keywords

AXL RECEPTOR TYROSINE KINASE; GROWTH ARREST-SPECIFIC PROTEIN 6; KRAS PROTEIN, HUMAN; MONOCLONAL ANTIBODY; ONCOPROTEIN; PROTEIN KINASE B; PROTEIN TYROSINE KINASE; RAS PROTEIN; SIGNAL PEPTIDE;

ANIMAL; CELL MOTION; CELL SURVIVAL; DRUG EFFECTS; DRUG SCREENING; FEMALE; GENETICS; HUMAN; IMMUNOLOGY; IMMUNOTHERAPY; METABOLISM; MOLECULARLY TARGETED THERAPY; NUDE MOUSE; PANCREAS CARCINOMA; PANCREATIC NEOPLASMS; PHOSPHORYLATION; PROCEDURES;

ANIMALS; ANTIBODIES, MONOCLONAL; CARCINOMA, PANCREATIC DUCTAL; CELL MOVEMENT; CELL SURVIVAL; FEMALE; HUMANS; IMMUNOTHERAPY; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE, NUDE; MOLECULAR TARGETED THERAPY; PANCREATIC NEOPLASMS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; RAS PROTEINS; RECEPTOR PROTEIN-TYROSINE KINASES; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84887514966     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2013.487     Document Type: Article

References (40)

1. Nelson NJ. Pancreatic Cancer Research Matures. J Natl Cancer Inst 2007; 99: 1432-1434.
2. Beck A, Wurch T, Bailly C, Corvaia N. Strategies and challenges for the next generation of therapeutic antibodies. Nat Rev Immunol 2010; 10: 345-352.
3. Vanneman M, Dranoff G. Combining immunotherapy and targeted therapies in cancer treatment. Nat Rev Cancer 2012; 12: 237-251.
4. Kim EJ, Simeone DM. Advances in pancreatic cancer. Curr Opin Gastroenterol 2011; 27: 460-466.
5. Jones S, Zhang X, Parsons DW, Lin JC, Leary RJ, Angenendt P et al. Core signaling pathways in human pancreatic cancers revealed by global genomic analyses. Science 2008; 321: 1801-1806.
6. Wong HH, Lemoine NR. Pancreatic cancer: molecular pathogenesis and new therapeutic targets. Nat Rev Gastroenterol Hepatol 2009; 6: 412-422.
7. Linger RMA, Keating AK, Earp HS, Graham DK. TAM receptor tyrosine kinases: biologic functions, signaling, and potential therapeutic targeting in human cancer. Adv Cancer Res 2008; 100: 35-83.
8. Verma A, Warner SL, Vankayalapati H, Bearss DJ, Sharma S. Targeting axl and mer kinases in cancer. Mol Cancer Ther 2011; 10: 1763-1773.
9. Liu E, Hjelle B, Bishop JM. Transforming genes in chronic myelogenous leukemia. Proc Natl Acad Sci USA 1988; 85: 1952-1956.
10. Linger RM, Keating AK, Earp HS, Graham DK. Taking aim at Mer and Axl receptor tyrosine kinases as novel therapeutic targets in solid tumors. Expert Opin Ther Targets 2010; 14: 1073-1090.
11. Koorstra JBM, Karikari CA, Feldmann G, Bisht S, Rojas PL, Offerhaus GJA et al. The Axl receptor tyrosine kinase confers an adverse prognostic influence in pancreatic cancer and represents a new therapeutic target. Cancer Biol Ther 2009; 8: 618-626.
12. Song X, Wang H, Logsdon CD, Rashid A, Fleming JB, Abbruzzese JL et al. Overexpression of receptor tyrosine kinase Axl promotes tumor cell invasion and survival in pancreatic ductal adenocarcinoma. Cancer 2011; 117: 734-743.
13. Gjerdrum C, Tiron C, Hoiby T, Stefansson I, Haugen H, Sandal T et al. Axl is an essential epithelial-to-mesenchymal transition-induced regulator of breast cancer metastasis and patient survival. Proc Natl Acad Sci USA 2010; 107: 1124-1129.
14. Vuoriluoto K, Haugen H, Kiviluoto S, Mpindi J-P, Nevo J, Gjerdrum C et al. Vimentin regulates EMT induction by Slug and oncogenic H-Ras and migration by governing Axl expression in breast cancer. Oncogene 2011; 30: 1436-1448.
15. Hong C-C, Lay J-D, Huang J-S, Cheng A-L, Tang J-L, Lin M-T et al. Receptor tyrosine kinase AXL is induced by chemotherapy drugs and overexpression of AXL confers drug resistance in acute myeloid leukemia. Cancer Lett 2008; 268: 314-324.
16. Gioia R, Leroy C, Drullion C, Lagarde V, Etienne G, Dulucq S et al. Quantitative phosphoproteomics revealed interplay between Syk and Lyn in the resistance to nilotinib in chronic myeloid leukemia cells. Blood 2011; 118: 2211-2221.
17. Mahadevan D, Cooke L, Riley C, Swart R, Simons B, Croce KD et al. A novel tyrosine kinase switch is a mechanism of imatinib resistance in gastrointestinal stromal tumors. Oncogene 2007; 26: 3909-3919.
18. Liu L, Greger J, Shi H, Liu Y, Greshock J, Annan R et al. Novel mechanism of lapatinib resistance in HER2-positive breast tumor cells: activation of AXL. Cancer Res 2009; 69: 6871-6878.
19. Macleod K, Mullen P, Sewell J, Rabiasz G, Lawrie S, Miller E et al. Altered ErbB receptor signaling and gene expression in cisplatin-resistant ovarian cancer. Cancer Res 2005; 65: 6789-6800.
20. Lay J-D, Hong C-C, Huang J-S, Yang Y-Y, Pao C-Y, Liu C-H et al. Sulfasalazine suppresses drug resistance and invasiveness of lung adenocarcinoma cells expressing AXL. Cancer Res 2007; 67: 3878-3887.
21. Li Y, Ye X, Tan C, Hongo J-A, Zha J, Liu J et al. Axl as a potential therapeutic target in cancer: role of Axl in tumor growth, metastasis and angiogenesis. Oncogene 2009; 28: 3442-3455.
22. Larbouret C, Robert B, Navarro-Teulon I, Thèzenas S, Ladjemi M-Z, Morisseau S et al. In vivo therapeutic synergism of anti-epidermal growth factor receptor and anti-HER2 monoclonal antibodies against pancreatic carcinomas. Clin Cancer Res 2007; 13: 3356-3362.
23. Trédan O, Galmarini CM, Patel K, Tannock IF. Drug resistance and the solid tumor microenvironment. J Natl Cancer Inst 2007; 99: 1441-1454.
24. Troiani T, Martinelli E, Capasso A, Morgillo F, Orditura M, De Vita F et al. Targeting EGFR in pancreatic cancer treatment. Curr Drug Targets 2012; 13: 802-810.
25. Byers LA, Diao L, Wang J, Saintigny P, Girard L, Peyton M et al. An epithelial- mesenchymal transition gene signature predicts resistance to EGFR and PI3K inhibitors and identifies axl as a therapeutic target for overcoming EGFR inhibitor resistance. Clin Cancer Res 2013; 19: 279-290.
26. Thiery JP, Acloque H, Huang RYJ, Nieto MA. Epithelial-mesenchymal transitions in development and disease. Cell 2009; 139: 871-890.
27. Krantz SB, Shields MA, Dangi-Garimella S, Munshi HG, Bentrem DJ. Contribution of epithelial-to-mesenchymal transition and cancer stem cells to pancreatic cancer progression. J Surg Res 2012; 173: 105-112.
28. Tai K-Y, Shieh Y-S, Lee C-S, Shiah S-G, Wu C-W. Axl promotes cell invasion by inducing MMP-9 activity through activation of NF-kB and Brg-1. Oncogene 2008; 27: 4044-4055.
29. Rankin EB, Fuh KC, Taylor TE, Krieg AJ, Musser M, Yuan J et al. AXL is an essential factor and therapeutic target for metastatic ovarian cancer. Cancer Res 2010; 70: 7570-7579.
30. Clynes RA, Towers TL, Presta LG, Ravetch JV. Inhibitory Fc receptors modulate in vivo cytoxicity against tumor targets. Nat Med 2000; 6: 443-446.
31. Cartron G, Dacheux L, Salles G, Solal-Celigny P, Bardos P, Colombat P et al. Therapeutic activity of humanized anti-CD20 monoclonal antibody and polymorphism in IgG Fc receptor FcgRIIIa gene. Blood 2002; 99: 754-758.
32. Musolino A, Naldi N, Bortesi B, Pezzuolo D, Capelletti M, Missale G et al. Immunoglobulin G fragment C receptor polymorphisms and clinical efficacy of trastuzumab- based therapy in patients with HER-2/neu-positive metastatic breast cancer. J Clin Oncol 2008; 26: 1789-1796.
33. Bibeau F, Lopez-Crapez E, Fiore FD, Thezenas S, Ychou M, Blanchard F et al. Impact of FcgRIIa-FcgRIIIa polymorphisms and KRAS mutations on the clinical outcome of patients with metastatic colorectal cancer treated with cetuximab plus irinotecan. J Clin Oncol 2009; 27: 1122-1129.
34. Mishra A, Wang J, Shiozawa Y, McGee S, Kim J, Jung Y et al. Hypoxia stabilizes GAS6/Axl signaling in metastatic prostate cancer. Mol Cancer Res 2012; 10: 703-712.
35. Ye X, Li Y, Stawicki S, Couto S, Eastham-Anderson J, Kallop D et al. An anti-Axl monoclonal antibody attenuates xenograft tumor growth and enhances the effect of multiple anticancer therapies. Oncogene 2010; 29: 5254-5264.
36. Linger RMA, Cohen RA, Cummings CT, Sather S, Migdall-Wilson J, Middleton DHG et al. Mer or Axl receptor tyrosine kinase inhibition promotes apoptosis, blocks growth and enhances chemosensitivity of human non-small cell lung cancer. Oncogene 2012; 32: 3420-3431.
37. Zhang Z, Lee JC, Lin L, Olivas V, Au V, Laframboise T et al. Activation of the AXL kinase causes resistance to EGFR-targeted therapy in lung cancer. Nat genet 2012; 44: 852-860.
38. Gaborit N, Larbouret C, Vallaghe J, Peyrusson F, Bascoul-Mollevi C, Crapez E et al. Time-resolved fluorescence resonance energy transfer (TR-FRET) to analyze the disruption of EGFR/HER2 dimers. J Biol Chem 2011; 286: 11337-11345.
39. Robert B, Mach J-P, Mani J-C, Ychou M, Folli S, Artus J-C et al. Cytokine targeting in tumors using a bispecific antibody directed against carcinoembryonic antigen and tumor necrosis factor a. Cancer Res 1996; 56: 4758-4765.
40. Bossard C, Busson M, Vindrieux D, Gaudin F, Machelon V, Brigitte M et al. Potential role of estrogen receptor beta as a tumor suppressor of epithelial ovarian cancer. PLoS One 2012; 7: e44787.