Synergistic antitumor activity of regorafenib and lapatinib in preclinical models of human colorectal cancer

Cancer Letters

Volumn 386, Issue , 2017, Pages 100-109

  Zhang, Wen Ji ^a   Li, Yong ^b   Wei, Meng Ning ^a   Chen, Yao ^a   Qiu, Jian Ge ^a   Jiang, Qi Wei ^a   Yang, Yang ^a   Zheng, Di Wei ^a   Qin, Wu Ming ^a   Huang, Jia Rong ^a   Wang, Kun ^a   Zhang, Wen Juan ^c   Wang, Yi Jun ^d   Yang, Dong Hua ^d   Chen, Zhe Sheng ^a,d   Shi, Zhi ^a  

^a JINAN UNIVERSITY   (China)

^b GUANGDONG PROVINCIAL PEOPLE'S HOSPITAL   (China)

^c MEDICAL COLLEGE OF JINAN UNIVERSITY   (China)

^d ST JOHN'S UNIVERSITY   (United States)

Author keywords

Colorectal cancer; Combination chemotherapy; Lapatinib; Regorafenib; Targeted therapy

Indexed keywords

LAPATINIB; REGORAFENIB; ANGIOGENESIS INHIBITOR; ANTINEOPLASTIC AGENT; CARBANILAMIDE DERIVATIVE; PROTEIN KINASE INHIBITOR; PYRIDINE DERIVATIVE; QUINAZOLINE DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CACO2 CELL LINE; CANCER INHIBITION; CANCER MODEL; CELL CYCLE ARREST; CELL LINE; COLORECTAL CANCER; COLORECTAL CANCER CELL LINE; COMBINATION CHEMOTHERAPY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG BLOOD LEVEL; DRUG EFFICACY; DRUG POTENTIATION; HCT116 CELL LINE; HCT8 CELL LINE; HT 29 CELL LINE; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NCM460 CELL LINE; NONHUMAN; PRECLINICAL STUDY; PRIORITY JOURNAL; SW480 CELL LINE; SW620 CELL LINE; TUMOR VOLUME; TUMOR XENOGRAFT; ANIMAL; BAGG ALBINO MOUSE; BLOOD; CELL CYCLE CHECKPOINT; CELL PROLIFERATION; COLORECTAL NEOPLASMS; DOSE RESPONSE; DRUG EFFECTS; DRUG SCREENING; FEMALE; HCT 116 CELL LINE; HT-29 CELL LINE; IC50; MOLECULARLY TARGETED THERAPY; NEOVASCULARIZATION (PATHOLOGY); NUDE MOUSE; PATHOLOGY;

ANGIOGENESIS INHIBITORS; ANIMALS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; APOPTOSIS; CELL CYCLE CHECKPOINTS; CELL PROLIFERATION; COLORECTAL NEOPLASMS; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG SYNERGISM; FEMALE; HCT116 CELLS; HT29 CELLS; HUMANS; INHIBITORY CONCENTRATION 50; MICE, INBRED BALB C; MICE, NUDE; MOLECULAR TARGETED THERAPY; NEOVASCULARIZATION, PATHOLOGIC; PHENYLUREA COMPOUNDS; PROTEIN KINASE INHIBITORS; PYRIDINES; QUINAZOLINES; TUMOR BURDEN; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84999040174     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2016.11.011     Document Type: Article

References (47)

1. [1] Sanz-Garcia, E., Grasselli, J., Argiles, G., Elez, M.E., Tabernero, J., Current and advancing treatments for metastatic colorectal cancer. Expert Opin. Biol. Ther., 2015, 1–18.
2. [2] Ciombor, K.K., Wu, C., Goldberg, R.M., Recent therapeutic advances in the treatment of colorectal cancer. Annu. Rev. Med. 66 (2015), 83–95.
3. [3] Demetri, G.D., Reichardt, P., Kang, Y.K., Blay, J.Y., Rutkowski, P., Gelderblom, H., et al. Efficacy and safety of regorafenib for advanced gastrointestinal stromal tumours after failure of imatinib and sunitinib (GRID): an international, multicentre, randomised, placebo-controlled, phase 3 trial. Lancet 381 (2013), 295–302.
4. [4] Grothey, A., Van Cutsem, E., Sobrero, A., Siena, S., Falcone, A., Ychou, M., et al. Regorafenib monotherapy for previously treated metastatic colorectal cancer (CORRECT): an international, multicentre, randomised, placebo-controlled, phase 3 trial. Lancet 381 (2013), 303–312.
5. [5] Wilhelm, S.M., Dumas, J., Adnane, L., Lynch, M., Carter, C.A., Schutz, G., et al. Regorafenib (BAY 73-4506): a new oral multikinase inhibitor of angiogenic, stromal and oncogenic receptor tyrosine kinases with potent preclinical antitumor activity. Int. J. Cancer 129 (2011), 245–255.
6. [6] Abou-Elkacem, L., Arns, S., Brix, G., Gremse, F., Zopf, D., Kiessling, F., et al. Regorafenib inhibits growth, angiogenesis, and metastasis in a highly aggressive, orthotopic colon cancer model. Mol. Cancer Ther. 12 (2013), 1322–1331.
7. [7] Mirone, G., Perna, S., Shukla, A., Marfe, G., Involvement of Notch-1 in resistance to regorafenib in colon Cancer cells. J. Cell Physiol. 231:5 (2015), 1097–1105.
8. [8] Lippolis, C., Refolo, M.G., D'Alessandro, R., Carella, N., Messa, C., Cavallini, A., et al. Resistance to multikinase inhibitor actions mediated by insulin like growth factor-1. J. Exp. Clin. Cancer Res., 34, 2015, 90.
9. [9] Bozic, I., Reiter, J.G., Allen, B., Antal, T., Chatterjee, K., Shah, P., et al. Evolutionary dynamics of cancer in response to targeted combination therapy. Elife, 2, 2013, e00747.
10. [10] Jiang, Q.W., Cheng, K.J., Mei, X.L., Qiu, J.G., Zhang, W.J., Xue, Y.Q., et al. Synergistic anticancer effects of triptolide and celastrol, two main compounds from thunder god vine. Oncotarget 6 (2015), 32790–32804.
11. [11] Diyabalanage, H.V., Granda, M.L., Hooker, J.M., Combination therapy: histone deacetylase inhibitors and platinum-based chemotherapeutics for cancer. Cancer Lett. 329 (2013), 1–8.
12. [12] Geyer, C.E., Forster, J., Lindquist, D., Chan, S., Romieu, C.G., Pienkowski, T., et al. Lapatinib plus capecitabine for HER2-positive advanced breast cancer. N. Engl. J. Med. 355 (2006), 2733–2743.
13. [13] Schwartzberg, L.S., Franco, S.X., Florance, A., O'Rourke, L., Maltzman, J., Johnston, S., Lapatinib plus letrozole as first-line therapy for HER-2+ hormone receptor-positive metastatic breast cancer. Oncologist 15 (2010), 122–129.
14. [14] Patil, A., Sherbet, G.V., Therapeutic approach to the management of HER2-positive breast cancer metastatic to the brain. Cancer Lett. 358 (2015), 93–99.
15. [15] Zhang, H., Wang, Y.J., Zhang, Y.K., Wang, D.S., Kathawala, R.J., Patel, A., et al. AST1306, a potent EGFR inhibitor, antagonizes ATP-binding cassette subfamily G member 2-mediated multidrug resistance. Cancer Lett. 350 (2014), 61–68.
16. [16] Chou, T.C., Talalay, P., Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Adv. Enzyme Regul. 22 (1984), 27–55.
17. [17] Chen, X.X., Xie, F.F., Zhu, X.J., Lin, F., Pan, S.S., Gong, L.H., et al. Cyclin-dependent kinase inhibitor dinaciclib potently synergizes with cisplatin in preclinical models of ovarian cancer. Oncotarget 6 (2015), 14926–14939.
18. [18] Mei, X.L., Yang, Y., Zhang, Y.J., Li, Y., Zhao, J.M., Qiu, J.G., et al. Sildenafil inhibits the growth of human colorectal cancer in vitro and in vivo. Am. J. Cancer Res. 5 (2015), 3311–3324.
19. [19] Shi, Z., Park, H.R., Du, Y., Li, Z., Cheng, K., Sun, S.Y., et al. Cables1 complex couples survival signaling to the cell death machinery. Cancer Res. 75 (2015), 147–158.
20. [20] Xie, F.F., Pan, S.S., Ou, R.Y., Zheng, Z.Z., Huang, X.X., Jian, M.T., et al. Volasertib suppresses tumor growth and potentiates the activity of cisplatin in cervical cancer. Am. J. Cancer Res. 5 (2015), 3548–3559.
21. [21] Luo, Y., Jiang, Q.W., Wu, J.Y., Qiu, J.G., Zhang, W.J., Mei, X.L., et al. Regulation of migration and invasion by Toll-like receptor-9 signaling network in prostate cancer. Oncotarget 6 (2015), 22564–22574.
22. [22] Gong, L.H., Chen, X.X., Wang, H., Jiang, Q.W., Pan, S.S., Qiu, J.G., et al. Piperlongumine induces apoptosis and synergizes with cisplatin or paclitaxel in human ovarian cancer cells. Oxid. Med. Cell Longev., 2014, 2014, 906804.
23. [23] Qiu, J.G., Zhang, Y.J., Li, Y., Zhao, J.M., Zhang, W.J., Jiang, Q.W., et al. Trametinib modulates cancer multidrug resistance by targeting ABCB1 transporter. Oncotarget 6 (2015), 15494–15509.
24. [24] Tiwari, A.K., Sodani, K., Dai, C.L., Abuznait, A.H., Singh, S., Xiao, Z.J., et al. Nilotinib potentiates anticancer drug sensitivity in murine ABCB1-, ABCG2-, and ABCC10-multidrug resistance xenograft models. Cancer Lett. 328 (2013), 307–317.
25. [25] Shi, Z., Li, Z., Li, Z.J., Cheng, K., Du, Y., Fu, H., et al. Cables1 controls p21/Cip1 protein stability by antagonizing proteasome subunit alpha type 3. Oncogene 34 (2015), 2538–2545.
26. [26] Lankheet, N.A., Hillebrand, M.J., Rosing, H., Schellens, J.H., Beijnen, J.H., Huitema, A.D., Method development and validation for the quantification of dasatinib, erlotinib, gefitinib, imatinib, lapatinib, nilotinib, sorafenib and sunitinib in human plasma by liquid chromatography coupled with tandem mass spectrometry. Biomed. Chromatogr. 27 (2013), 466–476.
27. [27] Shukla, S., Chen, Z.S., Ambudkar, S.V., Tyrosine kinase inhibitors as modulators of ABC transporter-mediated drug resistance. Drug Resist Updat 15 (2012), 70–80.
28. [28] Shi, Z., Tiwari, A.K., Patel, A.S., Fu, L.W., Chen, Z.S., Roles of sildenafil in enhancing drug sensitivity in cancer. Cancer Res. 71 (2011), 3735–3738.
29. [29] Chen, D., Wei, L., Yu, J., Zhang, L., Regorafenib inhibits colorectal tumor growth through PUMA-mediated apoptosis. Clin. Cancer Res. 20 (2014), 3472–3484.
30. [30] Zhou, Y., Li, S., Hu, Y.P., Wang, J., Hauser, J., Conway, A.N., et al. Blockade of EGFR and ErbB2 by the novel dual EGFR and ErbB2 tyrosine kinase inhibitor GW572016 sensitizes human colon carcinoma GEO cells to apoptosis. Cancer Res. 66 (2006), 404–411.
31. [31] Schmieder, R., Hoffmann, J., Becker, M., Bhargava, A., Muller, T., Kahmann, N., et al. Regorafenib (BAY 73-4506): antitumor and antimetastatic activities in preclinical models of colorectal cancer. Int. J. Cancer 135 (2014), 1487–1496.
32. [32] Takigawa, H., Kitadai, Y., Shinagawa, K., Yuge, R., Higashi, Y., Tanaka, S., et al. Multikinase inhibitor regorafenib inhibits the growth and metastasis of colon cancer with abundant stroma. Cancer Sci. 107:5 (2016), 601–618.
33. [33] Sajithlal, G.B., Hamed, H.A., Cruickshanks, N., Booth, L., Tavallai, S., Syed, J., et al. Sorafenib/regorafenib and phosphatidyl inositol 3 kinase/thymoma viral proto-oncogene inhibition interact to kill tumor cells. Mol. Pharmacol. 84 (2013), 562–571.
34. [34] Wei, N., Chu, E., Wu, S.Y., Wipf, P., Schmitz, J.C., The cytotoxic effects of regorafenib in combination with protein kinase D inhibition in human colorectal cancer cells. Oncotarget 6 (2015), 4745–4756.
35. [35] Napolitano, S., Martini, G., Rinaldi, B., Martinelli, E., Donniacuo, M., Berrino, L., et al. Of colorectal Cancer to anti-EGFR monoclonal antibody can Be overcome by combined treatment of regorafenib with cetuximab. Clin. Cancer Res. 21 (2015), 2975–2983.
36. [36] Schultheis, B., Folprecht, G., Kuhlmann, J., Ehrenberg, R., Hacker, U.T., Kohne, C.H., et al. Regorafenib in combination with FOLFOX or FOLFIRI as first- or second-line treatment of colorectal cancer: results of a multicenter, phase Ib study. Ann. Oncol. 24 (2013), 1560–1567.
37. [37] Argiles, G., Saunders, M.P., Rivera, F., Sobrero, A., Benson, A. 3rd, Guillen Ponce, C., et al. Regorafenib plus modified FOLFOX6 as first-line treatment of metastatic colorectal cancer: a phase II trial. Eur. J. Cancer 51 (2015), 942–949.
38. [38] LaBonte, M.J., Manegold, P.C., Wilson, P.M., Fazzone, W., Louie, S.G., Lenz, H.J., et al. The dual EGFR/HER-2 tyrosine kinase inhibitor lapatinib sensitizes colon and gastric cancer cells to the irinotecan active metabolite SN-38. Int. J. Cancer 125 (2009), 2957–2969.
39. [39] Dolloff, N.G., Mayes, P.A., Hart, L.S., Dicker, D.T., Humphreys, R., El-Deiry, W.S., Off-target lapatinib activity sensitizes colon cancer cells through TRAIL death receptor up-regulation. Sci. Transl. Med., 3, 2011, 86ra50.
40. [40] Chu, C., Noel-Hudson, M.S., Boige, V., Goere, D., Marion, S., Polrot, M., et al. Therapeutic efficiency of everolimus and lapatinib in xenograft model of human colorectal carcinoma with KRAS mutation. Fundam. Clin. Pharmacol. 27 (2013), 434–442.
41. [41] Frank, D., Jumonville, A., Loconte, N.K., Schelman, W.R., Mulkerin, D., Lubner, S., et al. A phase II study of capecitabine and lapatinib in advanced refractory colorectal adenocarcinoma: a Wisconsin Oncology Network study. J. Gastrointest. Oncol. 3 (2012), 90–96.
42. [42] Hamed, H.A., Tavallai, S., Grant, S., Poklepovic, A., Dent, P., Sorafenib/regorafenib and lapatinib interact to kill CNS tumor cells. J. Cell Physiol. 230 (2015), 131–139.
43. [43] Kort, A., Durmus, S., Sparidans, R.W., Wagenaar, E., Beijnen, J.H., Schinkel, A.H., et al. Of regorafenib is restricted by breast Cancer resistance protein (BCRP/ABCG2) and P-glycoprotein (P-GP/ABCB1). Pharm. Res. 32 (2015), 2205–2216.
44. [44] Ohya, H., Shibayama, Y., Ogura, J., Narumi, K., Kobayashi, M., Iseki, K., Regorafenib is transported by the organic anion transporter 1B1 and the multidrug resistance protein 2. Biol. Pharm. Bull. 38 (2015), 582–586.
45. [45] Kuang, Y.H., Shen, T., Chen, X., Sodani, K., Hopper-Borge, E., Tiwari, A.K., et al. Lapatinib and erlotinib are potent reversal agents for MRP7 (ABCC10)-mediated multidrug resistance. Biochem. Pharmacol. 79 (2010), 154–161.
46. [46] Dai, C.L., Tiwari, A.K., Wu, C.P., Su, X.D., Wang, S.R., Liu, D.G., et al. Lapatinib (Tykerb, GW572016) reverses multidrug resistance in cancer cells by inhibiting the activity of ATP-binding cassette subfamily B member 1 and G member 2. Cancer Res. 68 (2008), 7905–7914.
47. [47] Ma, S.L., Hu, Y.P., Wang, F., Huang, Z.C., Chen, Y.F., Wang, X.K., et al. Lapatinib antagonizes multidrug resistance-associated protein 1-mediated multidrug resistance by inhibiting its transport function. Mol. Med. 20 (2014), 390–399.