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The intersection between viral oncolysis, drug resistance, and autophagy

  • Vladimir Beljanski , Cindy Chiang and John Hiscott EMAIL logo
Published/Copyright: June 12, 2015

Abstract

Resistance to both cytotoxic and targeted therapies is a major problem facing cancer treatment. The mechanisms of resistance to unrelated drugs share many common features, including up-regulation of detoxifying pathways, activation of pro-survival mechanisms, and ineffective induction of cell death. Oncolytic viruses (OVs) are promising biotherapeutics for cancer treatment that specifically replicate in and lyse cancer cells. In addition to direct viral lysis, the anti-tumor effects of OVs are mediated via innate and adaptive immune responses, and several adaptation mechanisms such as autophagy appear to contribute to their anti-tumor properties. Autophagy is a versatile pathway that plays a key role in cancer survival during stressful conditions such as starvation or cytotoxic drug challenges. Autophagy also plays a role in mediating innate and adaptive immune responses by contributing to antigen presentation and cytokine secretion. This role of autophagy in regulation of immune responses can be utilized to design therapeutic combinations using approaches that either stimulate or block autophagy to potentiate therapeutic efficacy of OVs. Additional studies are needed to determine optimal multimodal combination approaches that will facilitate future successful clinical implementation of OV-based therapies.


Corresponding author: John Hiscott, Laboratorio Pasteur, Istituto Pasteur – Fondazione Cenci Bolognetti, Viale Regina Elena 291, I-00161 Rome, Italy, e-mail:

Acknowledgments

This work was supported in part by NIH grant CA192185 to J.H.

References

Alvarez-Breckenridge, C.A., Yu, J., Price, R., Wei, M., Wang, Y., Nowicki, M.O., Ha, Y.P., Bergin, S., Hwang, C., Fernandez, S.A., et al. (2012). The histone deacetylase inhibitor valproic acid lessens NK cell action against oncolytic virus-infected glioblastoma cells by inhibition of STAT5/ T-BET signaling and generation of γ interferon. J. Virol. 86, 4566–4577.10.1128/JVI.05545-11Search in Google Scholar PubMed PubMed Central

Baghdadi, M., Yoneda, A., Yamashina, T., Nagao, H., Komohara, Y., Nagai, S., Akiba, H., Foretz, M., Yoshiyama, H., Kinoshita, I., et al. (2013). TIM-4 glycoprotein-mediated degradation of dying tumor cells by autophagy leads to reduced antigen presentation and increased immune tolerance. Immunity 39, 1070–1081.10.1016/j.immuni.2013.09.014Search in Google Scholar PubMed

Behrends, C., Sowa, M.E., Gygi, S.P., and Harper, J.W. (2010). Network organization of the human autophagy system. Nature 466, 68–76.10.1038/nature09204Search in Google Scholar PubMed PubMed Central

Bird, S.W., Maynard, N.D., Covert, M.W., and Kirkegaard, K. (2014). Nonlytic viral spread enhanced by autophagy components. Proc. Natl. Acad. Sci. USA 111, 13081–13086.10.1073/pnas.1401437111Search in Google Scholar PubMed PubMed Central

Bonilla, D.L., Bhattacharya, A., Sha, Y., Xu, Y., Xiang, Q., Kan, A., Jagannath, C., Komatsu, M., and Eissa, N.T. (2013). Autophagy regulates phagocytosis by modulating the expression of scavenger receptors. Immunity 39, 537–547.10.1016/j.immuni.2013.08.026Search in Google Scholar PubMed PubMed Central

Botta, G., Passaro, C., Libertini, S., Abagnale, A., Barbato, S., Maione, A.S., Hallden, G., Beguinot, F., Formisano, P., and Portella, G. (2012). Inhibition of autophagy enhances the effects of E1A-defective oncolytic adenovirus dl922–947 against glioma cells in vitro and in vivo. Hum. Gene Ther. 23, 623–634.10.1089/hum.2011.120Search in Google Scholar PubMed

Boya, P., Reggiori, F., and Codogno, P. (2013). Emerging regulation and functions of autophagy. Nat. Cell Biol. 15, 713–720.10.1038/ncb2788Search in Google Scholar PubMed PubMed Central

Bramante, S., Kaufmann, J.K., Veckman, V., Liikanen, I., Nettelbeck, D.M., Hemminki, O., Vassilev, L., Cerullo, V., Oksanen, M., Heiskanen, R., et al. (2015). Treatment of melanoma with a serotype 5/3 chimeric oncolytic adenovirus coding for GM-CSF: Results in vitro, in rodents and in humans. Int. J. Cancer. doi: 10.1002/ijc.29536. [Epub ahead of print].10.1002/ijc.29536Search in Google Scholar PubMed

Breitbach, C.J., Burke, J., Jonker, D., Stephenson, J., Haas, A.R., Chow, L.Q., Nieva, J., Hwang, T.H., Moon, A., Patt, R., et al. (2011). Intravenous delivery of a multi-mechanistic cancer-targeted oncolytic poxvirus in humans. Nature 477, 99–102.10.1038/nature10358Search in Google Scholar PubMed

Buchberger, A., Bukau, B., and Sommer, T. (2010). Protein quality control in the cytosol and the endoplasmic reticulum: brothers in arms. Mol. Cell 40, 238–252.10.1016/j.molcel.2010.10.001Search in Google Scholar PubMed

Carew, J.S., Medina, E.C., Esquivel, J.A., 2nd, Mahalingam, D., Swords, R., Kelly, K., Zhang, H., Huang, P., Mita, A.C., Mita, M.M., et al. (2010). Autophagy inhibition enhances vorinostat-induced apoptosis via ubiquitinated protein accumulation. J. Cell Mol. Med. 14, 2448–2459.10.1111/j.1582-4934.2009.00832.xSearch in Google Scholar PubMed PubMed Central

Chan, K.S., Espinosa, I., Chao, M., Wong, D., Ailles, L., Diehn, M., Gill, H., Presti, J., Jr., Chang, H.Y., van de Rijn, M., et al. (2009). Identification, molecular characterization, clinical prognosis, and therapeutic targeting of human bladder tumor-initiating cells. Proc. Natl. Acad. Sci. USA 106, 14016–14021.10.1073/pnas.0906549106Search in Google Scholar PubMed PubMed Central

Cheng, P.H., Lian, S., Zhao, R., Rao, X.M., McMasters, K.M., and Zhou, H.S. (2013a). Combination of autophagy inducer rapamycin and oncolytic adenovirus improves antitumor effect in cancer cells. Virol. J. 10, 293.10.1186/1743-422X-10-293Search in Google Scholar PubMed PubMed Central

Cheng, Y., Ren, X., Hait, W.N., and Yang, J.M. (2013b). Therapeutic targeting of autophagy in disease: biology and pharmacology. Pharmacol. Rev. 65, 1162–1197.10.1124/pr.112.007120Search in Google Scholar PubMed PubMed Central

Choi, Y.H. and Yu, A.M. (2014). ABC transporters in multidrug resistance and pharmacokinetics, and strategies for drug development. Curr. Pharm. Des. 20, 793–807.10.2174/138161282005140214165212Search in Google Scholar PubMed PubMed Central

Comincini, S., Allavena, G., Palumbo, S., Morini, M., Durando, F., Angeletti, F., Pirtoli, L., and Miracco, C. (2013). microRNA-17 regulates the expression of ATG7 and modulates the autophagy process, improving the sensitivity to temozolomide and low-dose ionizing radiation treatments in human glioblastoma cells. Cancer Biol. Ther. 14, 574–586.10.4161/cbt.24597Search in Google Scholar PubMed PubMed Central

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., et al. (2015). Phase 1 Study of Intratumoral Pexa-Vec (JX-594), an Oncolytic and Immunotherapeutic Vaccinia Virus, in Pediatric Cancer Patients. Mol. Ther. 23, 602–608.10.1038/mt.2014.243Search in Google Scholar PubMed PubMed Central

Crotzer, V.L. and Blum, J.S. (2010). Autophagy and adaptive immunity. Immunology 131, 9–17.10.1111/j.1365-2567.2010.03321.xSearch in Google Scholar PubMed PubMed Central

Denton, D., Nicolson, S., and Kumar, S. (2012). Cell death by autophagy: facts and apparent artefacts. Cell. Death Differ. 19, 87–95.10.1038/cdd.2011.146Search in Google Scholar PubMed PubMed Central

Devereaux, K., Dall’Armi, C., Alcazar-Roman, A., Ogasawara, Y., Zhou, X., Wang, F., Yamamoto, A., De Camilli, P., and Di Paolo, G. (2013). Regulation of mammalian autophagy by class II and III PI 3-kinases through PI3P synthesis. PLoS One 8, e76405.10.1371/journal.pone.0076405Search in Google Scholar PubMed PubMed Central

Duffy, A., Le, J., Sausville, E., and Emadi, A. (2015). Autophagy modulation: a target for cancer treatment development. Cancer Chemother. Pharmacol. 75, 439–447.10.1007/s00280-014-2637-zSearch in Google Scholar PubMed

Fletcher, J.I., Gherardi, S., Murray, J., Burkhart, C.A., Russell, A., Valli, E., Smith, J., Oberthuer, A., Ashton, L.J., London, W.B., et al. (2012). N-Myc regulates expression of the detoxifying enzyme glutathione transferase GSTP1, a marker of poor outcome in neuroblastoma. Cancer Res. 72, 845–853.10.1158/0008-5472.CAN-11-1885Search in Google Scholar PubMed

Fung, A.S., Lee, C., Yu, M., and Tannock, I.F. (2015). The effect of chemotherapeutic agents on tumor vasculature in subcutaneous and orthotopic human tumor xenografts. BMC Cancer 15, 112.10.1186/s12885-015-1091-6Search in Google Scholar PubMed PubMed Central

Gomes, L.C. and Dikic, I. (2014). Autophagy in antimicrobial immunity. Mol Cell 54, 224–233.10.1016/j.molcel.2014.03.009Search in Google Scholar PubMed

Granato, M., Santarelli, R., Farina, A., Gonnella, R., Lotti, L.V., Faggioni, A., and Cirone, M. (2014). Epstein-barr virus blocks the autophagic flux and appropriates the autophagic machinery to enhance viral replication. J. Virol. 88, 12715–12726.10.1128/JVI.02199-14Search in Google Scholar PubMed PubMed Central

Hanada, T. and Ohsumi, Y. (2005). Structure-function relationship of Atg12, a ubiquitin-like modifier essential for autophagy. Autophagy 1, 110–118.10.4161/auto.1.2.1858Search in Google Scholar PubMed

Heo, J., Reid, T., Ruo, L., Breitbach, C.J., Rose, S., Bloomston, M., Cho, M., Lim, H.Y., Chung, H.C., Kim, C.W., et al. (2013). Randomized dose-finding clinical trial of oncolytic immunotherapeutic vaccinia JX-594 in liver cancer. Nat. Med. 19, 329–336.10.1038/nm.3089Search in Google Scholar PubMed PubMed Central

Hollville, E., Carroll, R.G., Cullen, S.P., and Martin, S.J. (2014). Bcl-2 family proteins participate in mitochondrial quality control by regulating Parkin/PINK1-dependent mitophagy. Mol. Cell 55, 451–466.10.1016/j.molcel.2014.06.001Search in Google Scholar PubMed

Huo, J., Du, X.L., Lairson, D.R., Chan, W., Jiang, J., Buchholz, T.A., and Guadagnolo, B.A. (2014). Utilization of surgery, chemotherapy, radiation therapy, and hospice at the end of life for patients diagnosed with metastatic melanoma. Am. J. Clin. Oncol. 38, 235–241.10.1097/COC.0b013e31829378f9Search in Google Scholar PubMed PubMed Central

Ito, H., Aoki, H., Kuhnel, F., Kondo, Y., Kubicka, S., Wirth, T., Iwado, E., Iwamaru, A., Fujiwara, K., Hess, K.R., et al. (2006). Autophagic cell death of malignant glioma cells induced by a conditionally replicating adenovirus. J. Natl. Cancer Inst. 98, 625–636.10.1093/jnci/djj161Search in Google Scholar PubMed

Jamal, M.H., Ch’ng, W.C., Yusoff, K., and Shafee, N. (2012). Reduced Newcastle disease virus-induced oncolysis in a subpopulation of cisplatin-resistant MCF7 cells is associated with survivin stabilization. Cancer Cell Int. 12, 35.10.1186/1475-2867-12-35Search in Google Scholar PubMed PubMed Central

Jaspers, J.E., Sol, W., Kersbergen, A., Schlicker, A., Guyader, C., Xu, G., Wessels, L., Borst, P., Jonkers, J., and Rottenberg, S. (2015). BRCA2-deficient sarcomatoid mammary tumors exhibit multidrug resistance. Cancer Res. 75, 732–741.10.1158/0008-5472.CAN-14-0839Search in Google Scholar PubMed

Joubert, P.E., Meiffren, G., Gregoire, I.P., Pontini, G., Richetta, C., Flacher, M., Azocar, O., Vidalain, P.O., Vidal, M., Lotteau, V., et al. (2009). Autophagy induction by the pathogen receptor CD46. Cell Host Microbe 6, 354–366.10.1016/j.chom.2009.09.006Search in Google Scholar PubMed

Kanayama, M., He, Y.W., and Shinohara, M.L. (2015). The Lung Is Protected from Spontaneous Inflammation by Autophagy in Myeloid Cells. J. Immunol. 194, 5465–5471.10.4049/jimmunol.1403249Search in Google Scholar PubMed PubMed Central

Klarquist, J., Hennies, C.M., Lehn, M.A., Reboulet, R.A., Feau, S., and Janssen, E.M. (2014). STING-mediated DNA sensing promotes antitumor and autoimmune responses to dying cells. J. Immunol. 193, 6124–6134.10.4049/jimmunol.1401869Search in Google Scholar PubMed PubMed Central

Lalaoui, N., Lindqvist, L.M., Sandow, J.J., and Ekert, P.G. (2015). The molecular relationships between apoptosis, autophagy and necroptosis. Semin. Cell Dev. Biol. 39, 63–69.10.1016/j.semcdb.2015.02.003Search in Google Scholar PubMed

Lamfers, M.L., Fulci, G., Gianni, D., Tang, Y., Kurozumi, K., Kaur, B., Moeniralm, S., Saeki, Y., Carette, J.E., Weissleder, R., et al. (2006). Cyclophosphamide increases transgene expression mediated by an oncolytic adenovirus in glioma-bearing mice monitored by bioluminescence imaging. Mol. Ther. 14, 779–788.10.1016/j.ymthe.2006.08.008Search in Google Scholar PubMed PubMed Central

Lamy, L., Ngo, V.N., Emre, N.C., Shaffer, A.L., 3rd, Yang, Y., Tian, E., Nair, V., Kruhlak, M.J., Zingone, A., Landgren, O., and Staudt, L.M. (2013). Control of autophagic cell death by caspase-10 in multiple myeloma. Cancer Cell 23, 435–449.10.1016/j.ccr.2013.02.017Search in Google Scholar PubMed PubMed Central

Lee, Y.R., Hu, H.Y., Kuo, S.H., Lei, H.Y., Lin, Y.S., Yeh, T.M., Liu, C.C., and Liu, H.S. (2013). Dengue virus infection induces autophagy: an in vivo study. J. Biomed. Sci. 20, 65.10.1186/1423-0127-20-65Search in Google Scholar PubMed PubMed Central

Levine, B. and Deretic, V. (2007). Unveiling the roles of autophagy in innate and adaptive immunity. Nat. Rev. Immunol. 7, 767–777.10.1038/nri2161Search in Google Scholar PubMed PubMed Central

Levine, B., Packer, M., and Codogno, P. (2015). Development of autophagy inducers in clinical medicine. J. Clin. Invest. 125, 14–24.10.1172/JCI73938Search in Google Scholar PubMed PubMed Central

Li, Y., Wang, L.X., Yang, G., Hao, F., Urba, W.J., and Hu, H.M. (2008). Efficient cross-presentation depends on autophagy in tumor cells. Cancer Res. 68, 6889–6895.10.1158/0008-5472.CAN-08-0161Search in Google Scholar PubMed PubMed Central

Lichty, B.D., Breitbach, C.J., Stojdl, D.F., and Bell, J.C. (2014). Going viral with cancer immunotherapy. Nat. Rev. Cancer 14, 559–567.10.1038/nrc3770Search in Google Scholar PubMed

Lindqvist, L.M., Heinlein, M., Huang, D.C., and Vaux, D.L. (2014). Prosurvival Bcl-2 family members affect autophagy only indirectly, by inhibiting Bax and Bak. Proc. Natl. Acad. Sci. USA 111, 8512–8517.10.1073/pnas.1406425111Search in Google Scholar PubMed PubMed Central

Lun, X., Chan, J., Zhou, H., Sun, B., Kelly, J.J., Stechishin, O.O., Bell, J.C., Parato, K., Hu, K., Vaillant, D., et al. (2010). Efficacy and safety/toxicity study of recombinant vaccinia virus JX-594 in two immunocompetent animal models of glioma. Mol. Ther. 18, 1927–1936.10.1038/mt.2010.183Search in Google Scholar PubMed PubMed Central

Luo, S., Garcia-Arencibia, M., Zhao, R., Puri, C., Toh, P.P., Sadiq, O., and Rubinsztein, D.C. (2012). Bim inhibits autophagy by recruiting Beclin 1 to microtubules. Mol. Cell 47, 359–370.10.1016/j.molcel.2012.05.040Search in Google Scholar PubMed PubMed Central

Meng, C., Zhou, Z., Jiang, K., Yu, S., Jia, L., Wu, Y., Liu, Y., Meng, S., and Ding, C. (2012a). Newcastle disease virus triggers autophagy in U251 glioma cells to enhance virus replication. Arch. Virol. 157, 1011–1018.10.1007/s00705-012-1270-6Search in Google Scholar PubMed PubMed Central

Meng, S., Zhou, Z., Chen, F., Kong, X., Liu, H., Jiang, K., Liu, W., Hu, M., Zhang, X., Ding, C., and Wu, Y. (2012b). Newcastle disease virus induces apoptosis in cisplatin-resistant human lung adenocarcinoma A549 cells in vitro and in vivo. Cancer Lett. 317, 56–64.10.1016/j.canlet.2011.11.008Search in Google Scholar PubMed

Meng, S., Xu, J., Wu, Y., and Ding, C. (2013). Targeting autophagy to enhance oncolytic virus-based cancer therapy. Expert. Opin. Biol. Ther. 13, 863–873.10.1517/14712598.2013.774365Search in Google Scholar PubMed

Merrick, A.E., Ilett, E.J., and Melcher, A.A. (2009). JX-594, a targeted oncolytic poxvirus for the treatment of cancer. Curr. Opin. Investig. Drugs 10, 1372–1382.Search in Google Scholar

Nelles, M.E., Moreau, J.M., Furlonger, C.L., Berger, A., Medin, J.A., and Paige, C.J. (2014). Murine splenic CD4+ T cells, induced by innate immune cell interactions and secreted factors, develop antileukemia cytotoxicity. Cancer Immunol. Res. 2, 1113–1124.10.1158/2326-6066.CIR-13-0208Search in Google Scholar PubMed

Nguyen, T.L., Abdelbary, H., Arguello, M., Breitbach, C., Leveille, S., Diallo, J.S., Yasmeen, A., Bismar, T.A., Kirn, D., Falls, T., et al. (2008). Chemical targeting of the innate antiviral response by histone deacetylase inhibitors renders refractory cancers sensitive to viral oncolysis. Proc. Natl. Acad. Sci. USA 105, 14981–14986.10.1073/pnas.0803988105Search in Google Scholar PubMed PubMed Central

Obeid, M., Tesniere, A., Ghiringhelli, F., Fimia, G.M., Apetoh, L., Perfettini, J.L., Castedo, M., Mignot, G., Panaretakis, T., Casares, N., et al. (2007). Calreticulin exposure dictates the immunogenicity of cancer cell death. Nat. Med. 13, 54–61.10.1038/nm1523Search in Google Scholar PubMed

Palikaras, K., Lionaki, E., and Tavernarakis, N. (2015). Coordination of mitophagy and mitochondrial biogenesis during ageing in C. elegans. Nature 521, 525–528.10.1038/nature14300Search in Google Scholar PubMed

Parato, K.A., Breitbach, C.J., Le Boeuf, F., Wang, J., Storbeck, C., Ilkow, C., Diallo, J.S., Falls, T., Burns, J., Garcia, V., et al. (2012). The oncolytic poxvirus JX-594 selectively replicates in and destroys cancer cells driven by genetic pathways commonly activated in cancers. Mol. Ther. 20, 749–758.10.1038/mt.2011.276Search in Google Scholar PubMed PubMed Central

Peral de Castro, C., Jones, S.A., Ni Cheallaigh, C., Hearnden, C.A., Williams, L., Winter, J., Lavelle, E.C., Mills, K.H., and Harris, J. (2012). Autophagy regulates IL-23 secretion and innate T cell responses through effects on IL-1 secretion. J. Immunol. 189, 4144–4153.10.4049/jimmunol.1201946Search in Google Scholar PubMed

Pietrocola, F., Izzo, V., Niso-Santano, M., Vacchelli, E., Galluzzi, L., Maiuri, M.C., and Kroemer, G. (2013). Regulation of autophagy by stress-responsive transcription factors. Semin. Cancer Biol. 23, 310–322.10.1016/j.semcancer.2013.05.008Search in Google Scholar PubMed

Pol, J.G., Zhang, L., Bridle, B.W., Stephenson, K.B., Resseguier, J., Hanson, S., Chen, L., Kazdhan, N., Bramson, J.L., Stojdl, D.F., et al. (2014). Maraba virus as a potent oncolytic vaccine vector. Mol. Ther. 22, 420–429.10.1038/mt.2013.249Search in Google Scholar PubMed PubMed Central

Puto, L.A., Brognard, J., and Hunter, T. (2015). Transcriptional Repressor DAXX Promotes Prostate Cancer Tumorigenicity via Suppression of Autophagy. J. Biol Chem. Apr 22. pii: jbc.M115.658765. [Epub ahead of print].Search in Google Scholar

Richetta, C. and Faure, M. (2013). Autophagy in antiviral innate immunity. Cell Microbiol. 15, 368–376.10.1111/cmi.12043Search in Google Scholar PubMed

Rouschop, K.M., van den Beucken, T., Dubois, L., Niessen, H., Bussink, J., Savelkouls, K., Keulers, T., Mujcic, H., Landuyt, W., Voncken, J.W., et al. (2010). The unfolded protein response protects human tumor cells during hypoxia through regulation of the autophagy genes MAP1LC3B and ATG5. J. Clin. Invest. 120, 127–141.10.1172/JCI40027Search in Google Scholar PubMed PubMed Central

Russell, R.C., Yuan, H.X., and Guan, K.L. (2014). Autophagy regulation by nutrient signaling. Cell Res. 24, 42–57.10.1038/cr.2013.166Search in Google Scholar PubMed PubMed Central

Sagnier, S., Daussy, C.F., Borel, S., Robert-Hebmann, V., Faure, M., Blanchet, F.P., Beaumelle, B., Biard-Piechaczyk, M., and Espert, L. (2015). Autophagy restricts HIV-1 infection by selectively degrading Tat in CD4+ T lymphocytes. J. Virol. 89, 615–625.10.1128/JVI.02174-14Search in Google Scholar PubMed PubMed Central

Saitoh, T., Fujita, N., Jang, M.H., Uematsu, S., Yang, B.G., Satoh, T., Omori, H., Noda, T., Yamamoto, N., Komatsu, M., et al. (2008). Loss of the autophagy protein Atg16L1 enhances endotoxin-induced IL-1beta production. Nature 456, 264–268.10.1038/nature07383Search in Google Scholar PubMed

Samuel, S., Beljanski, V., Van Grevenynghe, J., Richards, S., Ben Yebdri, F., He, Z., Nichols, C., Belgnaoui, S.M., Steel, C., Goulet, M.L., et al. (2013). BCL-2 inhibitors sensitize therapy-resistant chronic lymphocytic leukemia cells to VSV oncolysis. Mol. Ther. 21, 1413–1423.10.1038/mt.2013.91Search in Google Scholar PubMed PubMed Central

Schrag, D., Weiser, M.R., Goodman, K.A., Gonen, M., Hollywood, E., Cercek, A., Reidy-Lagunes, D.L., Gollub, M.J., Shia, J., Guillem, J.G., et al. (2014). Neoadjuvant chemotherapy without routine use of radiation therapy for patients with locally advanced rectal cancer: a pilot trial. J. Clin. Oncol. 32, 513–518.10.1200/JCO.2013.51.7904Search in Google Scholar PubMed PubMed Central

Sequist, L.V., Waltman, B.A., Dias-Santagata, D., Digumarthy, S., Turke, A.B., Fidias, P., Bergethon, K., Shaw, A.T., Gettinger, S., Cosper, A.K., et al. (2011). Genotypic and histological evolution of lung cancers acquiring resistance to EGFR inhibitors. Sci. Transl. Med. 3, 75ra26.10.1126/scitranslmed.3002003Search in Google Scholar PubMed PubMed Central

Shulak, L., Beljanski, V., Chiang, C., Dutta, S.M., Van Grevenynghe, J., Belgnaoui, S.M., Nguyen, T.L., Di Lenardo, T., Semmes, O.J., Lin, R., et al. (2014). Histone deacetylase inhibitors potentiate vesicular stomatitis virus oncolysis in prostate cancer cells by modulating NF-κB-dependent autophagy. J. Virol. 88, 2927–2940.10.1128/JVI.03406-13Search in Google Scholar PubMed PubMed Central

Siegel, R., Ma, J., Zou, Z., and Jemal, A. (2014). Cancer statistics, 2014. CA Cancer J. Clin. 64, 9–29.10.3322/caac.21208Search in Google Scholar PubMed

Sui, X., Chen, R., Wang, Z., Huang, Z., Kong, N., Zhang, M., Han, W., Lou, F., Yang, J., Zhang, Q., et al. (2013). Autophagy and chemotherapy resistance: a promising therapeutic target for cancer treatment. Cell Death Dis. 4, e838.10.1038/cddis.2013.350Search in Google Scholar PubMed PubMed Central

Suzuki, K., Noda, T., and Ohsumi, Y. (2004). Interrelationships among Atg proteins during autophagy in Saccharomyces cerevisiae. Yeast 21, 1057–1065.10.1002/yea.1152Search in Google Scholar PubMed

Trocoli, A., Bensadoun, P., Richard, E., Labrunie, G., Merhi, F., Schlafli, A.M., Brigger, D., Souquere, S., Pierron, G., Pasquet, J.M., et al. (2014). p62/SQSTM1 upregulation constitutes a survival mechanism that occurs during granulocytic differentiation of acute myeloid leukemia cells. Cell Death Differ. 21, 1852–1861.10.1038/cdd.2014.102Search in Google Scholar PubMed PubMed Central

Unger, F.T., Witte, I., and David, K.A. (2015). Prediction of individual response to anticancer therapy: historical and future perspectives. Cell Mol. Life Sci. 72, 729–757.10.1007/s00018-014-1772-3Search in Google Scholar PubMed PubMed Central

Vadlapatla, R.K., Vadlapudi, A.D., Pal, D., and Mitra, A.K. (2013). Mechanisms of drug resistance in cancer chemotherapy: coordinated role and regulation of efflux transporters and metabolizing enzymes. Curr. Pharm. Des. 19, 7126–7140.10.2174/13816128113199990493Search in Google Scholar PubMed

Van Brussel, J.P., Jan Van Steenbrugge, G., Van Krimpen, C., Bogdanowicz, J.F., Van Der Kwast, T.H., Schroder, F.H., and Mickisch, G.H. (2001). Expression of multidrug resistance related proteins and proliferative activity is increased in advanced clinical prostate cancer. J. Urol. 165, 130–135.10.1097/00005392-200101000-00032Search in Google Scholar PubMed

Viry, E., Paggetti, J., Baginska, J., Mgrditchian, T., Berchem, G., Moussay, E., and Janji, B. (2014). Autophagy: an adaptive metabolic response to stress shaping the antitumor immunity. Biochem. Pharmacol. 92, 31–42.10.1016/j.bcp.2014.07.006Search in Google Scholar PubMed

Walczak, M. and Martens, S. (2013). Dissecting the role of the Atg12-Atg5-Atg16 complex during autophagosome formation. Autophagy 9, 424–425.10.4161/auto.22931Search in Google Scholar PubMed PubMed Central

Xia, M., Gonzalez, P., Li, C., Meng, G., Jiang, A., Wang, H., Gao, Q., Debatin, K.M., Beltinger, C., and Wei, J. (2014). Mitophagy enhances oncolytic measles virus replication by mitigating DDX58/RIG-I-like receptor signaling. J. Virol. 88, 5152–5164.10.1128/JVI.03851-13Search in Google Scholar PubMed PubMed Central

Xu, D., Zhang, T., Xiao, J., Zhu, K., Wei, R., Wu, Z., Meng, H., Li, Y., and Yuan, J. (2015). Modification of BECN1 by ISG15 plays a crucial role in autophagy regulation by type I IFN/interferon. Autophagy 11, 617–628.10.1080/15548627.2015.1023982Search in Google Scholar PubMed PubMed Central

Yardley, D.A. (2013). Drug resistance and the role of combination chemotherapy in improving patient outcomes. Int. J. Breast Cancer 2013, 137414.10.1155/2013/137414Search in Google Scholar PubMed PubMed Central

Yip, N.C., Fombon, I.S., Liu, P., Brown, S., Kannappan, V., Armesilla, A.L., Xu, B., Cassidy, J., Darling, J.L., and Wang, W. (2011). Disulfiram modulated ROS-MAPK and NF-κB pathways and targeted breast cancer cells with cancer stem cell-like properties. Br. J. Cancer 104, 1564–1574.10.1038/bjc.2011.126Search in Google Scholar PubMed PubMed Central

Yokoyama, T., Iwado, E., Kondo, Y., Aoki, H., Hayashi, Y., Georgescu, M.M., Sawaya, R., Hess, K.R., Mills, G.B., Kawamura, H., et al. (2008). Autophagy-inducing agents augment the antitumor effect of telerase-selve oncolytic adenovirus OBP-405 on glioblastoma cells. Gene Ther. 15, 1233–1239.10.1038/gt.2008.98Search in Google Scholar PubMed

Zamarin, D., Holmgaard, R.B., Subudhi, S.K., Park, J.S., Mansour, M., Palese, P., Merghoub, T., Wolchok, J.D., and Allison, J.P. (2014). Localized oncolytic virotherapy overcomes systemic tumor resistance to immune checkpoint blockade immunotherapy. Sci. Transl. Med. 6, 226ra232.10.1126/scitranslmed.3008095Search in Google Scholar PubMed PubMed Central

Zamarron, B.F. and Chen, W. (2011). Dual roles of immune cells and their factors in cancer development and progression. Int. J. Biol. Sci. 7, 651–658.10.7150/ijbs.7.651Search in Google Scholar PubMed PubMed Central

Zheng, Y., Zhou, J., and Tong, Y. (2015). Gene signatures of drug resistance predict patient survival in colorectal cancer. Pharmacogenomics J. 15, 135–143.10.1038/tpj.2014.45Search in Google Scholar PubMed PubMed Central

Zhou, R., Tardivel, A., Thorens, B., Choi, I., and Tschopp, J. (2010). Thioredoxin-interacting protein links oxidative stress to inflammasome activation. Nat. Immunol. 11, 136–140.10.1038/ni.1831Search in Google Scholar PubMed

Zou, J., Li, W., Misra, A., Yue, F., Song, K., Chen, Q., Guo, G., Yi, J., Kimata, J.T., and Liu, L. (2015). The viral restriction factor tetherin prevents leucine-rich pentatricopeptide repeat-containing protein (LRPPRC) from association with beclin 1 and B-cell CLL/lymphoma 2 (Bcl-2) and enhances autophagy and mitophagy. J. Biol. Chem. 290, 7269–7279.10.1074/jbc.M114.627679Search in Google Scholar PubMed PubMed Central

Received: 2015-3-27
Accepted: 2015-6-9
Published Online: 2015-6-12
Published in Print: 2015-12-1

©2015 by De Gruyter

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