Overcoming sorafenib evasion in hepatocellular carcinoma using CXCR4-targeted nanoparticles to co-deliver MEK-inhibitors

Scientific Reports

Volumn 7, Issue , 2017, Pages

  Chen, Yunching ^a,b   Liu, Ya Chi ^b   Sung, Yun Chieh ^b   Ramjiawan, Rakesh R ^a,c   Lin, Ts Ting ^b   Chang, Chih Chun ^b   Jeng, Kuo Shyang ^d   Chang, Chiung Fang ^d   Liu, Chun Hung ^b   Gao, Dong Yu ^b   Hsu, Fu Fei ^e   Duyverman, Annique M ^a,f   Kitahara, Shuji ^a   Huang, Peigen ^a   Dima, Simona ^g   Popescu, Irinel ^g   Flaherty, Keith T ^a   Zhu, Andrew X ^a   Bardeesy, Nabeel ^a   Jain, Rakesh K ^a   Benes, Cyril H ^a   Duda, Dan G ^a   more..

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b NATIONAL TSING HUA UNIVERSITY   (Taiwan)

^c VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^d FAR EASTERN MEMORIAL HOSPITAL   (Taiwan)

^e INSTITUTE OF BIOMEDICAL SCIENCES   (Taiwan)

^f UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^g FUNDENI CLINICAL INSTITUTE   (Romania)

Author keywords

[No Author keywords available]

Indexed keywords

BENZIMIDAZOLE DERIVATIVE; CARBANILAMIDE DERIVATIVE; CHEMOKINE RECEPTOR CXCR4; CXCR4 PROTEIN, HUMAN; CXCR4 PROTEIN, MOUSE; NANOPARTICLE; NICOTINAMIDE; PROTEIN KINASE INHIBITOR; SELUMETINIB; SORAFENIB; TUMOR PROTEIN;

ANALOGS AND DERIVATIVES; ANIMAL; CELL LINE; DRUG DELIVERY SYSTEM; HUMAN; IMMUNOLOGY; LIVER CELL CARCINOMA; LIVER TUMOR; MOUSE; PATHOLOGY; PROCEDURES;

ANIMALS; BENZIMIDAZOLES; CARCINOMA, HEPATOCELLULAR; CELL LINE; DRUG DELIVERY SYSTEMS; HUMANS; LIVER NEOPLASMS; MICE; NANOPARTICLES; NEOPLASM PROTEINS; NIACINAMIDE; PHENYLUREA COMPOUNDS; PROTEIN KINASE INHIBITORS; RECEPTORS, CXCR4;

EID: 85014835509     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep44123     Document Type: Article

References (35)

1. Duncan, J. S., et al. Dynamic reprogramming of the kinome in response to targeted MEK inhibition in triple-negative breast cancer. Cell 149, 307-321, doi: 10.1016/j.cell.2012.02.053 (2012).
2. Alcala, A. M., & Flaherty, K. T. BRAF inhibitors for the treatment of metastatic melanoma: clinical trials and mechanisms of resistance. Clin Cancer Res 18, 33-39, doi: 10.1158/1078-0432.CCR-11-0997 (2012).
3. Engelman, J. A., et al. MET amplification leads to gefitinib resistance in lung cancer by activating ERBB3 signaling. Science 316, 1039-1043, doi: 10.1126/science.1141478 (2007).
4. Poulikakos, P. I., Zhang, C., Bollag, G., Shokat, K. M., & Rosen, N. RAF inhibitors transactivate RAF dimers and ERK signalling in cells with wild-Type BRAF. Nature 464, 427-430, doi: 10.1038/nature08902 (2010).
5. Su, F., et al. RAS mutations in cutaneous squamous-cell carcinomas in patients treated with BRAF inhibitors. N Engl J Med 366, 207-215, doi: 10.1056/NEJMoa1105358 (2012).
6. Llovet, J. M., et al. Sorafenib in advanced hepatocellular carcinoma. N Engl J Med 359, 378-390, doi: 10.1056/NEJMoa0708857 (2008).
7. Cheng, A. L., et al. Efficacy and safety of sorafenib in patients in the Asia-Pacific region with advanced hepatocellular carcinoma: a phase III randomised, double-blind, placebo-controlled trial. Lancet Oncol 10, 25-34, doi: 10.1016/S1470-2045 (08)70285-7 (2009).
8. Chen, Y., et al. CXCR4 inhibition in tumor microenvironment facilitates anti-programmed death receptor-1 immunotherapy in sorafenib-Treated hepatocellular carcinoma in mice. Hepatol 61, 1591-1602, doi: 10.1002/hep.27665 (2015).
9. Chen, Y., et al. Differential effects of sorafenib on liver versus tumor fibrosis mediated by stromal-derived factor 1 alpha/C-X-C receptor type 4 axis and myeloid differentiation antigen-positive myeloid cell infiltration in mice. Hepatol 59, 1435-1447, doi: 10.1002/hep.26790 (2014).
10. Wilhelm, S. M., et al. BAY 43-9006 exhibits broad spectrum oral antitumor activity and targets the RAF/MEK/ERK pathway and receptor tyrosine kinases involved in tumor progression and angiogenesis. Cancer Res 64, 7099-7109, doi: 10.1158/0008-5472.CAN-04-1443 (2004).
11. Abou-Alfa, G. K., et al. Phase II study of sorafenib in patients with advanced hepatocellular carcinoma. J Clin Oncol 24, 4293-4300 (2006).
12. Farazi, P. A., & DePinho, R. A. Hepatocellular carcinoma pathogenesis: from genes to environment. Nat Rev Cancer 6, 674-687, doi: 10.1038/nrc1934 (2006).
13. Balmanno, K., & Cook, S. J. Tumour cell survival signalling by the ERK1/2 pathway. Cell Death Differ 16, 368-377, doi: 10.1038/cdd.2008.148 (2009).
14. Ota, K., et al. Induction of PD-L1 Expression by the EML4-ALK Oncoprotein and Downstream Signaling Pathways in Non-Small Cell Lung Cancer. Clin Cancer Res 21, 4014-4021, doi: 10.1158/1078-0432.CCR-15-0016 (2015).
15. Zhang, Y., et al. Myeloid cells are required for PD-1/PD-L1 checkpoint activation and the establishment of an immunosuppressive environment in pancreatic cancer. Gut, doi: 10.1136/gutjnl-2016-312078 (2016).
16. Flaherty, K. T., et al. Improved survival with MEK inhibition in BRAF-mutated melanoma. New Engl J Med 367, 107-114, doi: 10.1056/NEJMoa1203421 (2012).
17. Boussemart, L., et al. Prospective study of cutaneous side-effects associated with the BRAF inhibitor vemurafenib: a study of 42 patients. Ann Oncol 24, 1691-1697, doi: 10.1093/annonc/mdt015 (2013).
18. McDermott, U., et al. Identification of genotype-correlated sensitivity to selective kinase inhibitors by using high-Throughput tumor cell line profiling. Proc Natl Acad Sci USA 104, 19936-19941, doi: 10.1073/pnas.0707498104 (2007).
19. Zhu, A. X., Duda, D. G., Sahani, D. V., & Jain, R. K. HCC and angiogenesis: possible targets and future directions. Nat Rev Clin Oncol 8, 292-301, doi: 10.1038/nrclinonc.2011.30 (2011).
20. Wilhelm, S., et al. Discovery and development of sorafenib: a multikinase inhibitor for treating cancer. Nature reviews. Drug Discov 5, 835-844, doi: 10.1038/nrd2130 (2006).
21. Rudalska, R., et al. In vivo RNAi screening identifies a mechanism of sorafenib resistance in liver cancer. Nat Med 20, 1138-1146, doi: 10.1038/nm.3679 (2014).
22. Zhou, D., et al. Mst1 and Mst2 maintain hepatocyte quiescence and suppress hepatocellular carcinoma development through inactivation of the Yap1 oncogene. Cancer Cell 16, 425-438, doi: 10.1016/j.ccr.2009.09.026 (2009).
23. Reiberger, T., et al. An orthotopic mouse model of hepatocellular carcinoma with underlying liver cirrhosis. Nat Protoc 10, 1264-1274, doi: 10.1038/nprot.2015.080 (2015).
24. Smith, M. A., & Houghton, P. A proposal regarding reporting of in vitro testing results. Clin Cancer Res 19, 2828-2833, doi: 10.1158/1078-0432.CCR-13-0043 (2013).
25. Tan, T. T., et al. Key roles of BIM-driven apoptosis in epithelial tumors and rational chemotherapy. Cancer Cell 7, 227-238, doi: 10.1016/j.ccr.2005.02.008 (2005).
26. Wang, J., Zhou, J. Y., & Wu, G. S. Bim protein degradation contributes to cisplatin resistance. The Journal of biological chemistry 286, 22384-22392, doi: 10.1074/jbc.M111.239566 (2011).
27. Lin, T. T., et al. Development and characterization of sorafenib-loaded PLGA nanoparticles for the systemic treatment of liver fibrosis. J Control Release 221, 62-70, doi: 10.1016/j.jconrel.2015.11.003 (2015).
28. Gao, D. Y., et al. CXCR4-Targeted lipid-coated PLGA nanoparticles deliver sorafenib and overcome acquired drug resistance in liver cancer. Biomaterials 67, 194-203, doi: 10.1016/j.biomaterials.2015.07.035 (2015).
29. Richert, M. M., et al. Inhibition of CXCR4 by CTCE-9908 inhibits breast cancer metastasis to lung and bone. Oncol Rep 21, 761-767 (2009).
30. Wong, D., Kandagatla, P., Korz, W., & Chinni, S. R. Targeting CXCR4 with CTCE-9908 inhibits prostate tumor metastasis. BMC Urol 14, 12, doi: 10.1186/1471-2490-14-12 (2014).
31. Chen, Y., & Duda, D. G. Targeting immunosuppression after standard sorafenib treatment to facilitate immune checkpoint blockade in hepatocellular carcinoma-An auto-commentary on clinical potential and future development. Oncoimmunol 4, e1029703, doi: 10.1080/2162402X.2015.1029703 (2015).
32. Heidorn, S. J., et al. Kinase-dead BRAF and oncogenic RAS cooperate to drive tumor progression through CRAF. Cell 140, 209-221, doi: 10.1016/j.cell.2009.12.040 (2010).
33. Jiang, X., Zhou, J., Giobbie-Hurder, A., Wargo, J., & Hodi, F. S. The activation of MAPK in melanoma cells resistant to BRAF inhibition promotes PD-L1 expression that is reversible by MEK and PI3K inhibition. Clin Cancer Res 19, 598-609, doi: 10.1158/1078-0432.CCR-12-2731 (2013).
34. Jain, S., Singhal, S., Lee, P., & Xu, R. Molecular genetics of hepatocellular neoplasia. Am J Transl Res 2, 105-118 (2010).
35. Lim, H. Y., et al. A phase II study of the efficacy and safety of the combination therapy of the MEK inhibitor refametinib (BAY 86-9766) plus sorafenib for Asian patients with unresectable hepatocellular carcinoma. Clin Cancer Res 20, 5976-5985, doi: 10.1158/1078-0432.CCR-13-3445 (2014).