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http://dx.doi.org/10.5352/JLS.2016.26.7.835

In vitro Anti-tumor Effect of an Engineered Vaccinia Virus in Multiple Cancer Cells and ABCG2 Expressing Drug Resistant Cancer Cells  

Park, Ji Hye (Lab. of Regenerative Medicine & Stem Cell Biology, Department of Physiology, Medical Research Institute, School of Medicine, Pusan National University)
Yun, Jisoo (Lab. of Regenerative Medicine & Stem Cell Biology, Department of Physiology, Medical Research Institute, School of Medicine, Pusan National University)
Heo, Jeong (Department of Internal Medicine, Pusan National University and Medical Research Institute, Pusan National University Hospital)
Hwang, Tae Ho (Department of Pharmacology, School of Medicine, Pusan National University)
Kwon, Sang Mo (Lab. of Regenerative Medicine & Stem Cell Biology, Department of Physiology, Medical Research Institute, School of Medicine, Pusan National University)
Publication Information
Journal of Life Science / v.26, no.7, 2016 , pp. 835-846 More about this Journal
Abstract
Chemo-resistance is the biggest issue of effective cancer therapy. ABCG2 is highly correlated with multi-drug resistance, and represent a typical phenotype of multiple cancer stem-like cells. Accumulating evidence recently reported that oncolytic viruses represent a new strategy for multiple aggressive cancers and drug resistant cancers including cancer stem cell-like cells and ABCG2 expressing cells. In this study, we generated an evolutionally engineered vaccinia virus, SLJ-496, for drug-resistant cancer therapy. We first showed that SLJ-496 treatment enhanced tumor affinity using cytopathic effect assay, plaque assay, as well as cell viability assay. Next, we clearly demonstrated that in vitro SLJ-496 treatment represents significant cytotoxic effect in multiple cancers including colorectal cancer cells (HT-29, HCT-116, HCT-8), gastric cancer cells (AGS, NCI-N87, MKN-28), Hepatocellular carcinoma cells (SNU-449, SNU-423, SNU-475, HepG2), as well as mesothelioma cell (NCI-H226, NCI-H28, MSTO-221h). Highly ABCG2 expressing HT-29 cells represent cancer stem like phenotype including stem cell marker expression, and self-renewal bioactivities. Interestingly, we demonstrated that in vitro treatment of SLJ-496 showed significant cytotoxicity effect, as well as viral replication capacity in ABCG2 overexpressing cell. In addition, we also demonstrated the cytotoxic effect of SLJ-496 in Adriamycin-resistant cell lines, SNU-620 and ADR-300. Taken together, these findings provide us a pivotal clue that cancer therapy using SLJ-496 vaccinia virus might be new therapeutic strategy to overcome ABCG2 expressing cancer stem-like cell and multiple chemo-resistance cancer cells.
Keywords
ABCG2; drug-resistance cells; oncolytic vaccinia virus; SLJ-496GFP; vaccinia virus;
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1 Alemany, R. 2013. Viruses in cancer treatment. Clin. Transl. Oncol. 15, 182-188.   DOI
2 Ambudkar, S. V., Dey, S., Hrycyna, C. A., Ramachandra, M., Pastan, I. and Gottesman, M. M. 1999. Biochemical, cellular, and pharmacological aspects of the multidrug transporter. Annu. Rev. Pharmacol. Toxicol. 39, 361-398.   DOI
3 An, Y. and Ongkeko, W. M. 2009. ABCG2: the key to chemoresistance in cancer stem cells? Expert Opin. Drug Metab. Toxicol. 5, 1529-1542.   DOI
4 Bartlett, D. L., Liu, Z., Sathaiah, M., Ravindranathan, R., Guo, Z., He, Y. and Guo, Z. S. 2013. Oncolytic viruses as therapeutic cancer vaccines. Mol. Cancer 12, 103.   DOI
5 Bell, J. and McFadden, G. 2014. Viruses for tumor therapy. Cell Host Microbe. 15, 260-265.   DOI
6 Breitbach, C. J., Arulanandam, R., De Silva, N., Thorne, S. H., Patt, R., Daneshmand, M., Moon, A., Ilkow, C., Burke, J., Hwang, T. H., Heo, J., Cho, M., Chen, H., Angarita, F. A., Addison, C., McCart, J. A., Bell, J. C. and Kirn, D. H. 2013. Oncolytic vaccinia virus disrupts tumor-associated vasculature in humans. Cancer Res. 73, 1265-1275.   DOI
7 Breitbach, C. J., Moon, A., Burke, J., Hwang, T. H. and Kirn, D. H. 2015. A Phase 2, Open-label, randomized study of Pexa-Vec (JX-594) administered by intratumoral injection in patients with unresectable primary hepatocellular carcinoma. Methods Mol. Biol. 1317, 343-357.   DOI
8 Burke, M. J., Ahern, C., Weigel, B. J., Poirier, J. T., Rudin, C. M., Chen, Y., Cripe, T. P., Bernhardt, M. B. and Blaney, S. M. 2015. Phase I trial of Seneca Valley Virus (NTX-010) in children with relapsed/refractory solid tumors: a report of the Children′s Oncology Group. Pediatr Blood Cancer 62, 743-750.   DOI
9 Candeil, L., Gourdier, I., Peyron, D., Vezzio, N., Copois, V., Bibeau, F., Orsetti, B., Scheffer, G. L., Ychou, M., Khan, Q. A., Pommier, Y., Pau, B., Martineau, P. and Del Rio, M. 2004. ABCG2 overexpression in colon cancer cells resistant to SN38 and in irinotecan-treated metastases. Int. J. Cancer 109, 848-854.   DOI
10 Chernichenko, N., Linkov, G., Li, P., Bakst, R. L., Chen, C. H., He, S., Yu, Y. A., Chen, N. G., Szalay, A. A., Fong, Y. and Wong, R. J. 2013. Oncolytic vaccinia virus therapy of salivary gland carcinoma. JAMA Otolaryngol. Head Neck Surg. 139, 173-182.   DOI
11 Choi, J. W., Lee, J. S., Kim, S. W. and Yun, C. O. 2012. Evolution of oncolytic adenovirus for cancer treatment. Adv. Drug Deliv. Rev. 64, 720-729.   DOI
12 Cripe, T. P., Ngo, M. C., Geller, J. I., Louis, C. U., Currier, M. A., Racadio, J. M., Towbin, A. J., Rooney, C. M., Pelusio, A., Moon, A., Hwang, T. H., Burke, J. M., Bell, J. C., Kirn, D. H. and Breitbach, C. J. 2015. Phase 1 study of intratumoral Pexa-Vec (JX-594), an oncolytic and immunotherapeutic vaccinia virus, in pediatric cancer patients. Mol. Ther. 23, 602-608.   DOI
13 Dean, M., Fojo, T. and Bates, S. 2005. Tumour stem cells and drug resistance. Nat. Rev. Cancer 5, 275-284.   DOI
14 Ding, X. W., Wu, J. H. and Jiang, C. P. 2010. ABCG2: a potential marker of stem cells and novel target in stem cell and cancer therapy. Life Sci. 86, 631-637.   DOI
15 Hu, L. L., Wang, X. X., Chen, X., Chang, J., Li, C., Zhang, Y., Yang, J., Jiang, W. and Zhuang, S. M. 2007. BCRP gene polymorphisms are associated with susceptibility and survival of diffuse large B-cell lymphoma. Carcinogenesis 28, 1740-1744.   DOI
16 Doyle, L. A., Yang, W., Abruzzo, L. V., Krogmann, T., Gao, Y., Rishi, A. K. and Ross, D. D. 1998. A multidrug resistance transporter from human MCF-7 breast cancer cells. Proc. Natl. Acad. Sci. USA 95, 15665-15670.   DOI
17 Freytag, S. O., Barton, K. N. and Zhang, Y. 2013. Efficacy of oncolytic adenovirus expressing suicide genes and interleukin-12 in preclinical model of prostate cancer. Gene Ther. 20, 1131-1139.   DOI
18 Heo, J., Reid, T., Ruo, L., Breitbach, C. J., Rose, S., Bloomston, M., Cho, M., Lim, H. Y., Chung, H. C., Kim, C. W., Burke, J., Lencioni, R., Hickman, T., Moon, A., Lee, Y. S., Kim, M. K., Daneshmand, M., Dubois, K., Longpre, L., Ngo, M., Rooney, C., Bell, J. C., Rhee, B. G., Patt, R., Hwang, T. H. and Kirn, D. H. 2013. Randomized dose-finding clinical trial of oncolytic immunotherapeutic vaccinia JX-594 in liver cancer. Nat. Med. 19, 329-336.   DOI
19 Hwang, T. H., Moon, A., Burke, J., Ribas, A., Stephenson, J., Breitbach, C. J., Daneshmand, M., De Silva, N., Parato, K., Diallo, J. S., Lee, Y. S., Liu, T. C., Bell, J. C. and Kirn, D. H. 2011. A mechanistic proof-of-concept clinical trial with JX-594, a targeted multi-mechanistic oncolytic poxvirus, in patients with metastatic melanoma. Mol. Ther. 19, 1913-1922.   DOI
20 Ichihashi, Y. 1996. Extracellular enveloped vaccinia virus escapes neutralization. Virology 217, 478-485.   DOI
21 Jiang, Y., He, Y., Li, H., Li, H. N., Zhang, L., Hu, W., Sun, Y. M., Chen, F. L. and Jin, X. M. 2012. Expressions of putative cancer stem cell markers ABCB1, ABCG2, and CD133 are correlated with the degree of differentiation of gastric cancer. Gastric Cancer 15, 440-450.   DOI
22 Marchesi, V. 2013. Immunotherapy: Oncolytic vaccinia virus shows promise in liver cancer. Nat. Rev. Clin. Oncol. 10, 182.
23 Kirn, D., Martuza, R. L. and Zwiebel, J. 2001. Replication-selective virotherapy for cancer: Biological principles, risk management and future directions. Nat. Med. 7, 781-787.   DOI
24 Kirn, D. H. and Thorne, S. H. 2009. Targeted and armed oncolytic poxviruses: a novel multi-mechanistic therapeutic class for cancer. Nat. Rev. Cancer 9, 64-71.   DOI
25 Liu, H. G., Pan, Y. F., You, J., Wang, O. C., Huang, K. T. and Zhang, X. H. 2010. Expression of ABCG2 and its significance in colorectal cancer. Asian Pac. J. Cancer Prev. 11, 845-848.
26 Miyake, K., Mickley, L., Litman, T., Zhan, Z., Robey, R., Cristensen, B., Brangi, M., Greenberger, L., Dean, M., Fojo, T. and Bates, S. E. 1999. Molecular cloning of cDNAs which are highly overexpressed in mitoxantrone-resistant cells: demonstration of homology to ABC transport genes. Cancer Res. 59, 8-13.
27 Noguchi, K., Katayama, K. and Sugimoto, Y. 2014. Human ABC transporter ABCG2/BCRP expression in chemoresistance: basic and clinical perspectives for molecular cancer therapeutics. Pharmgenomics Pers Med. 7, 53-64.
28 Ortiz, R., Melguizo, C., Prados, J., Alvarez, P. J., Caba, O., Rodriguez-Serrano, F., Hita, F. and Aranega, A. 2012. New gene therapy strategies for cancer treatment: a review of recent patents. Recent Pat Anticancer Drug Discov. 7, 297-312.   DOI
29 Parato, K. A., Breitbach, C. J., Le Boeuf, F., Wang, J., Storbeck, C., Ilkow, C., Diallo, J. S., Falls, T., Burns, J., Garcia, V., Kanji, F., Evgin, L., Hu, K., Paradis, F., Knowles, S., Hwang, T. H., Vanderhyden, B. C., Auer, R., Kirn, D. H. and Bell, J. C. 2012. The oncolytic poxvirus JX-594 selectively replicates in and destroys cancer cells driven by genetic pathways commonly activated in cancers. Mol. Ther. 20, 749-758.   DOI
30 Park, B. H., Hwang, T., Liu, T. C., Sze, D. Y., Kim, J. S., Kwon, H. C., Oh, S. Y., Han, S. Y., Yoon, J. H., Hong, S. H., Moon, A., Speth, K., Park, C., Ahn, Y. J., Daneshmand, M., Rhee, B. G., Pinedo, H. M., Bell, J. C. and Kirn, D. H. 2008. Use of a targeted oncolytic poxvirus, JX-594, in patients with refractory primary or metastatic liver cancer: a phase I trial. Lancet Oncol. 9, 533-542   DOI
31 Park, S. H., Breitbach, C. J., Lee, J., Park, J. O., Lim, H. Y., Kang, W. K., Moon, A., Mun, J. H., Sommermann, E. M., Maruri Avidal, L., Patt, R., Pelusio, A., Burke, J., Hwang, T. H., Kirn, D. and Park, Y. S. 2015. Phase 1b trial of biweekly intravenous Pexa-Vec (JX-594), an oncolytic and immunotherapeutic vaccinia virus in colorectal cancer. Mol. Ther. 23, 1532-1540.   DOI
32 Raaijmakers, M. H., de Grouw, E. P., Heuver, L. H., van der Reijden, B. A., Jansen, J. H., Scheffer, G., Scheper, R. J., de Witte, T. J. and Raymakers, R. A. 2005. Impaired breast cancer resistance protein mediated drug transport in plasma cells in multiple myeloma. Leuk Res. 29, 1455-1458.   DOI
33 Roth, J. C., Cassady, K. A., Cody, J. J., Parker, J. N., Price, K. H., Coleman, J. M., Peggins, J. O., Noker, P. E., Powers, N. W., Grimes, S. D., Carroll, S. L., Gillespie, G. Y., Whitley, R. J. and Markert, J. M. 2014. Evaluation of the safety and biodistribution of M032, an attenuated herpes simplex virus type 1 expressing hIL-12, after intracerebral administration to aotus nonhuman primates. Hum. Gene Ther. Clin. Dev. 25, 16-27.   DOI
34 Sargent, J. M., Williamson, C. J., Maliepaard, M., Elgie, A. W., Scheper, R. J. and Taylor, C. G. 2001. Breast cancer resistance protein expression and resistance to daunorubicin in blast cells from patients with acute myeloid leukaemia. Br. J. Haematol. 115, 257-262.   DOI
35 Schinkel, A. H. and Jonker, J. W. 2003. Mammalian drug efflux transporters of the ATP binding cassette (ABC) family: an overview. Adv. Drug Deliv. Rev. 55, 3-29.   DOI
36 Zhou, S., Morris, J. J., Barnes, Y., Lan, L., Schuetz, J. D. and Sorrentino, B. P. 2002. Bcrp1 gene expression is required for normal numbers of side population stem cells in mice, and confers relative protection to mitoxantrone in hematopoietic cells in vivo. Proc. Natl. Acad. Sci. USA 99, 12339-12344.   DOI
37 Stanziale, S. F. and Fong, Y. 2003. Novel approaches to cancer therapy using oncolytic viruses. Curr. Mol. Med. 3, 61-71.   DOI
38 Valdespino-Gomez, V. M. and Valdespino-Castillo, V. E. 2012. [Targeted epigenetic therapy of cancer. Achievements and perspectives]. Cir. Cir. 80, 470-480.
39 Yoh, K., Ishii, G., Yokose, T., Minegishi, Y., Tsuta, K., Goto, K., Nishiwaki, Y., Kodama, T., Suga, M. and Ochiai, A. 2004. Breast cancer resistance protein impacts clinical outcome in platinum-based chemotherapy for advanced non-small cell lung cancer. Clin. Cancer Res. 10, 1691-1697.   DOI
40 Zhou, S., Schuetz, J. D., Bunting, K. D., Colapietro, A. M., Sampath, J., Morris, J. J., Lagutina, I., Grosveld, G. C., Osawa, M., Nakauchi, H. and Sorrentino, B. P. 2001. The ABC transporter Bcrp1/ABCG2 is expressed in a wide variety of stem cells and is a molecular determinant of the side-population phenotype. Nat. Med. 7, 1028-1034.   DOI