Co-targeting of EGF receptor and neuropilin-1 overcomes cetuximab resistance in pancreatic ductal adenocarcinoma with integrin β1-driven Src-Akt bypass signaling

Oncogene

Volumn 36, Issue 18, 2017, Pages 2543-2552

  Kim, Y J ^a   Jung, K ^a   Baek, D S ^a   Hong, S S ^b   Kim, Y S ^a  

^a Ajou University   (South Korea)

^b Inha University School of Medicine   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; 2,3 DIHYDRO 2 OXO 3 (4,5,6,7 TETRAHYDRO 1H INDOL 2 YLMETHYLENE) 1H INDOLE 5 SULFONIC ACID DIMETHYLAMIDE; BETA1 INTEGRIN; CETUXIMAB; EPIDERMAL GROWTH FACTOR RECEPTOR; NEUROPILIN 1; PROTEIN KINASE B; PROTEIN TYROSINE KINASE; EGFR PROTEIN, HUMAN; ONCOPROTEIN; PROTEIN KINASE P60;

ADENOCARCINOMA CELL LINE; ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; CANCER INHIBITION; CANCER RESISTANCE; CARBOXY TERMINAL SEQUENCE; CELL ADHESION; CELL MEMBRANE; CELL MOTILITY; CELL PROLIFERATION; CELL SURFACE; CONTROLLED STUDY; CYTOPLASM; DOWN REGULATION; ENZYME ACTIVATION; EXTRACELLULAR MATRIX; FEMALE; GENE OVEREXPRESSION; IN VITRO STUDY; IN VIVO STUDY; INTERNALIZATION; INTRACELLULAR SIGNALING; MOUSE; NONHUMAN; PANCREAS ADENOCARCINOMA; PANCREATIC CANCER CELL LINE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; RNA INTERFERENCE; SENSITIZATION; TUMOR XENOGRAFT; ADENOCARCINOMA; ANIMAL; ANTAGONISTS AND INHIBITORS; CARCINOMA, PANCREATIC DUCTAL; DRUG EFFECTS; DRUG RESISTANCE; DRUG SCREENING; GENETICS; HUMAN; PATHOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ADENOCARCINOMA; ANIMALS; ANTIGENS, CD29; CARCINOMA, PANCREATIC DUCTAL; CELL LINE, TUMOR; CETUXIMAB; DRUG RESISTANCE, NEOPLASM; HUMANS; MICE; NEUROPILIN-1; ONCOGENE PROTEIN PP60(V-SRC); ONCOGENE PROTEIN V-AKT; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84992751152     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2016.407     Document Type: Article

References (40)

1. Garrido-Laguna I, Hidalgo M. Pancreatic cancer: from state-of-the-art treatments to promising novel therapies. Nat Rev Clin Oncol 2015; 12: 319-334.
2. Philip PA, Benedetti J, Corless CL, Wong R, O'Reilly EM, Flynn PJ et al. Phase III study comparing gemcitabine plus cetuximab versus gemcitabine in patients with advanced pancreatic adenocarcinoma: Southwest Oncology Group-directed intergroup trial S0205. J Clin Oncol 2010; 28: 3605-3610.
3. Chong CR, Janne PA. The quest to overcome resistance to EGFR-targeted therapies in cancer. Nat Med 2013; 19: 1389-1400.
4. Oliveira-Cunha M, Newman WG, Siriwardena AK. Epidermal growth factor receptor in pancreatic cancer. Cancers (Basel) 2011; 3: 1513-1526.
5. Wong MH, Xue A, Julovi SM, Pavlakis N, Samra JS, Hugh TJ et al. Cotargeting of epidermal growth factor receptor and PI3K overcomes PI3K-Akt oncogenic dependence in pancreatic ductal adenocarcinoma. Clin Cancer Res 2014; 20: 4047-4058.
6. Wheeler DL, Dunn EF, Harari PM. Understanding resistance to EGFR inhibitorsimpact on future treatment strategies. Nat Rev Clin Oncol 2010; 7: 493-507.
7. Larbouret C, Gaborit N, Chardes T, Coelho M, Campigna E, Bascoul-Mollevi C et al. 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 2012; 14: 121-130.
8. Li B, Meng Y, Zheng L, Zhang X, Tong Q, Tan W et al. Bispecific antibody to ErbB2 overcomes trastuzumab resistance through comprehensive blockade of ErbB2 heterodimerization. Cancer Res 2013; 73: 6471-6483.
9. Prud'homme GJ, Glinka Y. Neuropilins are multifunctional coreceptors involved in tumor initiation, growth, metastasis and immunity. Oncotarget 2012; 3: 921-939.
10. Guo HF, Vander Kooi CW. Neuropilin functions as an essential cell surface receptor. J Biol Chem 2015; 290: 29120-29126.
11. Pan Q, Chanthery Y, Liang WC, Stawicki S, Mak J, Rathore N et al. Blocking neuropilin-1 function has an additive effect with anti-VEGF to inhibit tumor growth. Cancer Cell 2007; 11: 53-67.
12. Sugahara KN, Braun GB, de Mendoza TH, Kotamraju VR, French RP, Lowy AM et al. Tumor-penetrating iRGD peptide inhibits metastasis. Mol Cancer Ther 2015; 14: 120-128.
13. Jia H, Cheng L, Tickner M, Bagherzadeh A, Selwood D, Zachary I. Neuropilin-1 antagonism in human carcinoma cells inhibits migration and enhances chemosensitivity. Br J Cancer 2010; 102: 541-552.
14. Shin TH, Sung ES, Kim YJ, Kim KS, Kim SH, Kim SK et al. Enhancement of the tumor penetration of monoclonal antibody by fusion of a neuropilin-targeting peptide improves the antitumor efficacy. Mol Cancer Ther 2014; 13: 651-661.
15. Kim YJ, Bae J, Shin TH, Kang SH, Jeong M, Han Y et al. Immunoglobulin Fc-fused, neuropilin-1-specific peptide shows efficient tumor tissue penetration and inhibits tumor growth via anti-angiogenesis. J Control Release 2015; 216: 56-68.
16. Fukahi K, Fukasawa M, Neufeld G, Itakura J, Korc M. Aberrant expression of neuropilin-1 and-2 in human pancreatic cancer cells. Clin Cancer Res 2004; 10: 581-590.
17. Matsushita A, Gotze T, Korc M. Hepatocyte growth factor-mediated cell invasion in pancreatic cancer cells is dependent on neuropilin-1. Cancer Res 2007; 67: 10309-10316.
18. Wey JS, Gray MJ, Fan F, Belcheva A, McCarty MF, Stoeltzing O et al. Overexpression of neuropilin-1 promotes constitutive MAPK signalling and chemoresistance in pancreatic cancer cells. Br J Cancer 2005; 93: 233-241.
19. Zeng F, Luo F, Lv S, Zhang H, Cao C, Chen X et al. A monoclonal antibody targeting neuropilin-1 inhibits adhesion of MCF7 breast cancer cells to fibronectin by suppressing the FAK/p130cas signaling pathway. Anticancer Drugs 2014; 25: 663-672.
20. Valdembri D, Caswell PT, Anderson KI, Schwarz JP, Konig I, Astanina E et al. Neuropilin-1/GIPC1 signaling regulates alpha5beta1 integrin traffic and function in endothelial cells. PLoS Biol 2009; 7: e25.
21. Fukasawa M, Matsushita A, Korc M. Neuropilin-1 interacts with integrin beta1 and modulates pancreatic cancer cell growth, survival and invasion. Cancer Biol Ther 2007; 6: 1173-1180.
22. Kanda R, Kawahara A, Watari K, Murakami Y, Sonoda K, Maeda M et al. Erlotinib resistance in lung cancer cells mediated by integrin beta1/Src/Akt-driven bypass signaling. Cancer Res 2013; 73: 6243-6253.
23. Seguin L, Desgrosellier JS, Weis SM, Cheresh DA. Integrins and cancer: regulators of cancer stemness, metastasis, and drug resistance. Trends Cell Biol 2015; 25: 234-240.
24. Hou S, Isaji T, Hang Q, Im S, Fukuda T, Gu J. Distinct effects of beta1 integrin on cell proliferation and cellular signaling in MDA-MB-231 breast cancer cells. Sci Rep 2016; 6: 18430.
25. Arnoletti JP, Buchsbaum DJ, Huang ZQ, Hawkins AE, Khazaeli MB, Kraus MH et al. Mechanisms of resistance to Erbitux (anti-epidermal growth factor receptor) combination therapy in pancreatic adenocarcinoma cells. J Gastrointest Surg 2004; 8: 960-969 discussion 969-970.
26. Fotopoulou C, Baumunk D, Schmidt SC, Schumacher G. Additive growth inhibition after combined treatment of 2-methoxyestradiol and conventional chemotherapeutic agents in human pancreatic cancer cells. Anticancer Res 2010; 30: 4619-4624.
27. Iida M, Brand TM, Campbell DA, Li C, Wheeler DL. Yes and Lyn play a role in nuclear translocation of the epidermal growth factor receptor. Oncogene 2013; 32: 759-767.
28. Biscardi JS, Maa MC, Tice DA, Cox ME, Leu TH, Parsons SJ. c-Src-mediated phosphorylation of the epidermal growth factor receptor on Tyr845 and Tyr1101 is associated with modulation of receptor function. J Biol Chem 1999; 274: 8335-8343.
29. Sung ES, Park KJ, Lee SH, Jang YS, Park SK, Park YH et al. A novel agonistic antibody to human death receptor 4 induces apoptotic cell death in various tumor cells without cytotoxicity in hepatocytes. Mol Cancer Ther 2009; 8: 2276-2285.
30. Arjonen A, Alanko J, Veltel S, Ivaska J. Distinct recycling of active and inactive beta1 integrins. Traffic 2012; 13: 610-625.
31. De Franceschi N, Hamidi H, Alanko J, Sahgal P, Ivaska J. Integrin traffic-the update. J Cell Sci 2015; 128: 839-852.
32. Luque A, Gomez M, Puzon W, Takada Y, Sanchez-Madrid F, Cabanas C. Activated conformations of very late activation integrins detected by a group of antibodies (HUTS) specific for a novel regulatory region (355-425) of the common beta 1. chain. J Biol Chem 1996; 271: 11067-11075.
33. Tadokoro S, Shattil SJ, Eto K, Tai V, Liddington RC, de Pereda JM et al. Talin binding to integrin beta tails: a final common step in integrin activation. Science 2003; 302: 103-106.
34. Ye F, Kim C, Ginsberg MH. Reconstruction of integrin activation. Blood 2012; 119: 26-33.
35. Cox AD, Fesik SW, Kimmelman AC, Luo J, Der CJ. Drugging the undruggable RAS: mission possible? Nat Rev Drug Discov 2014; 13: 828-851.
36. Yaqoob U, Cao S, Shergill U, Jagavelu K, Geng Z, Yin M et al. Neuropilin-1 stimulates tumor growth by increasing fibronectin fibril assembly in the tumor microenvironment. Cancer Res 2012; 72: 4047-4059.
37. Okon IS, Coughlan KA, Zhang C, Moriasi C, Ding Y, Song P et al. Protein kinase LKB1 promotes RAB7-mediated neuropilin-1 degradation to inhibit angiogenesis. J Clin Invest 2014; 124: 4590-4602.
38. Choi DK, Bae J, Shin SM, Shin JY, Kim S, Kim YS. A general strategy for generating intact, full-length IgG antibodies that penetrate into the cytosol of living cells. MAbs 2014; 6: 1402-1414.
39. Choi HJ, Kim YJ, Lee S, Kim YS. A heterodimeric Fc-based bispecific antibody simultaneously targeting VEGFR-2 and Met exhibits potent antitumor activity. Mol Cancer Ther 2013; 12: 2748-2759.
40. Nguyen DH, Taub D. CXCR4 function requires membrane cholesterol: implications for HIV infection. J Immunol 2002; 168: 4121-4126.