Oncolytic virotherapy versus cancer stem cells: A review of approaches and mechanisms

Cancers

Volumn 10, Issue 4, 2018, Pages

  Chaurasiya, Shyambabu ^a   Chen, Nanhai G ^a   Warner, Susanne G ^a  

^a CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

Author keywords

Cancer stem cells; Oncolytic virus; Viral therapy

Indexed keywords

ANTINEOPLASTIC AGENT; ONCOLYTIC VIRUS;

ACUTE MYELOID LEUKEMIA; BREAST CANCER; CANCER CHEMOTHERAPY; CANCER PROGNOSIS; CANCER RESISTANCE; CANCER STEM CELL; CARCINOGENICITY; CELL POPULATION; CELL PROLIFERATION; CELL SELF-RENEWAL; CELL SURVIVAL; CHRONIC MYELOID LEUKEMIA; COLON CANCER; COLORECTAL CANCER; DNA REPAIR; DRUG EFFECT; DRUG TARGETING; EPITHELIAL MESENCHYMAL TRANSITION; GLIOBLASTOMA; HUMAN; INNATE IMMUNITY; LEUKEMIA; LIVER CANCER; LUNG CANCER; MALIGNANT NEOPLASM; NONHUMAN; ONCOLYTIC VIROTHERAPY; REVIEW; STEM CELL NICHE; STOMACH CANCER; TREATMENT PLANNING; TUMOR MICROENVIRONMENT;

EID: 85047551871     PISSN: None     EISSN: 20726694     Source Type: Journal    
DOI: 10.3390/cancers10040124     Document Type: Review

References (127)

1. Hanahan, D.; Weinberg, R.A. The hallmarks of cancer. Cell 2000, 100, 57-70
2. Feinberg, A.P.; Ohlsson, R.; Henikoff, S. The epigenetic progenitor origin of human cancer. Nat. Rev. Genet. 2006, 7, 21-33
3. Greaves, M.; Maley, C.C. Clonal evolution in cancer. Nature 2012, 481, 306-313
4. Shackleton, M.; Quintana, E.; Fearon, E.R.; Morrison, S.J. Heterogeneity in cancer: Cancer stem cells versus clonal evolution. Cell 2009, 138, 822-829
5. Clarke, M.F.; Dick, J.E.; Dirks, P.B.; Eaves, C.J.; Jamieson, C.H.; Jones, D.L.; Visvader, J.; Weissman, I.L.; Wahl, G.M. Cancer stem cells—Perspectives on current status and future directions: AACR Workshop on cancer stem cells. Cancer Res.2006, 66, 9339-9344
6. Campbell, L.L.; Polyak, K. Breast tumor heterogeneity: Cancer stem cells or clonal evolution? Cell Cycle 2007, 6, 2332-2338
7. Chaffer, C.L.; Brueckmann, I.; Scheel, C.; Kaestli, A.J.; Wiggins, P.A.; Rodrigues, L.O.; Brooks, M.; Reinhardt, F.; Su, Y.; Polyak, K.; et al. Normal and neoplastic nonstem cells can spontaneously convert to a stem-like state. Proc. Natl. Acad. Sci. USA 2011, 108, 7950-7955
8. Lapidot, T.; Sirard, C.; Vormoor, J.; Murdoch, B.; Hoang, T.; Caceres-Cortes, J.; Minden, M.; Paterson, B.; Caligiuri, M.A.; Dick, J.E. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 1994, 367, 645-648
9. Bonnet, D.; Dick, J.E. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat. Med. 1997, 3, 730-737
10. Al-Hajj, M.; Wicha, M.S.; Benito-Hernandez, A.; Morrison, S.J.; Clarke, M.F. Prospective identification of tumorigenic breast cancer cells. Proc. Natl. Acad. Sci. USA 2003, 100, 3983-3988
11. Klonisch, T.; Wiechec, E.; Hombach-Klonisch, S.; Ande, S.R.; Wesselborg, S.; Schulze-Osthoff, K.; Los, M. Cancer stem cell markers in common cancers—Therapeutic implications. Trends Mol. Med. 2008, 14, 450-460
12. Hiraga, T.; Ito, S.; Nakamura, H. Side population in MDA-MB-231 human breast cancer cells exhibits cancer stem cell-like properties without higher bone-metastatic potential. Oncol. Rep. 2011, 25, 289-296
13. Xiong, B.; Ma, L.; Hu, X.; Zhang, C.; Cheng, Y. Characterization of side population cells isolated from the colon cancer cell line SW480. Int. J. Oncol. 2014, 45, 1175-1183
14. Ebben, J.D.; Treisman, D.M.; Zorniak, M.; Kutty, R.G.; Clark, P.A.; Kuo, J.S. The cancer stem cell paradigm: A new understanding of tumor development and treatment. Expert Opin. Ther. Targets 2010, 14, 621-632
15. Kirn, D. Replication-selective oncolytic adenoviruses: Virotherapy aimed at genetic targets in cancer. Oncogene 2000, 19, 6660-6669
16. Dean, M.; Fojo, T.; Bates, S. Tumour stem cells and drug resistance. Nat. Rev. Cancer 2005, 5, 275-284
17. Blagosklonny, M.V. Target for cancer therapy: Proliferating cells or stem cells. Leukemia 2006, 20, 385-391
18. Kruger, G.M.; Morrison, S.J. Brain repair by endogenous progenitors. Cell 2002, 110, 399-402
19. Lou, H.; Dean, M. Targeted therapy for cancer stem cells: The patched pathway and ABC transporters. Oncogene 2007, 26, 1357-1360
20. Diehn, M.; Cho, R.W.; Lobo, N.A.; Kalisky, T.; Dorie, M.J.; Kulp, A.N.; Qian, D.; Lam, J.S.; Ailles, L.E.; Wong, M.; et al. Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature 2009, 458, 780-783
21. Bao, S.; Wu, Q.; McLendon, R.E.; Hao, Y.; Shi, Q.; Hjelmeland, A.B.; Dewhirst, M.W.; Bigner, D.D.; Rich, J.N. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 2006, 444, 756-760
22. Dalerba, P.; Cho, R.W.; Clarke, M.F. Cancer stem cells: Models and concepts. Annu. Rev. Med. 2007, 58, 267-284
23. Creighton, C.J.; Li, X.; Landis, M.; Dixon, J.M.; Neumeister, V.M.; Sjolund, A.; Rimm, D.L.; Wong, H.; Rodriguez, A.; Herschkowitz, J.I.; et al. Residual breast cancers after conventional therapy display mesenchymal as well as tumor-initiating features. Proc. Natl. Acad. Sci. USA 2009, 106, 13820-13825
24. Phillips, T.M.; McBride, W.H.; Pajonk, F. The response of CD24(−/low)/CD44+ breast cancer-initiating cells to radiation. J. Natl. Cancer Inst. 2006, 98, 1777-1785
25. McDermott, S.P.; Wicha, M.S. Targeting breast cancer stem cells. Mol. Oncol. 2010, 4, 404-419
26. Li, X.; Lewis, M.T.; Huang, J.; Gutierrez, C.; Osborne, C.K.; Wu, M.F.; Hilsenbeck, S.G.; Pavlick, A.; Zhang, X.; Chamness, G.C.; et al. Intrinsic resistance of tumorigenic breast cancer cells to chemotherapy. J. Natl. Cancer Inst. 2008, 100, 672-679
27. Stojdl, D.F.; Lichty, B.; Knowles, S.; Marius, R.; Atkins, H.; Sonenberg, N.; Bell, J.C. Exploiting tumor-specific defects in the interferon pathway with a previously unknown oncolytic virus. Nat. Med. 2000, 6, 821-825
28. Everts, B.; van der Poel, H.G. Replication-selective oncolytic viruses in the treatment of cancer. Cancer Gene Ther. 2005, 12, 141-161
29. Evgin, L.; Vaha-Koskela, M.; Rintoul, J.; Falls, T.; Le Boeuf, F.; Barrett, J.W.; Bell, J.C.; Stanford, M.M. Potent oncolytic activity of raccoonpox virus in the absence of natural pathogenicity. Mol. Ther. 2010, 18, 896-902
30. Russell, S.J.; Peng, K.W.; Bell, J.C. Oncolytic virotherapy. Nat. Biotechnol. 2012, 30, 658-670
31. Martin, T.A.; Watkins, G.; Jiang, W.G. The Coxsackie-adenovirus receptor has elevated expression in human breast cancer. Clin. Exp. Med. 2005, 5, 122-128
32. Sanjuan, X.; Fernandez, P.L.; Miquel, R.; Munoz, J.; Castronovo, V.; Menard, S.; Palacin, A.; Cardesa, A.; Campo, E. Overexpression of the 67-kD laminin receptor correlates with tumour progression in human colorectal carcinoma. J. Pathol. 1996, 179, 376-380
33. Masson, D.; Jarry, A.; Baury, B.; Blanchardie, P.; Laboisse, C.; Lustenberger, P.; Denis, M.G. Overexpression of the CD155 gene in human colorectal carcinoma. Gut 2001, 49, 236-240
34. Anderson, B.D.; Nakamura, T.; Russell, S.J.; Peng, K.W. High CD46 receptor density determines preferential killing of tumor cells by oncolytic measles virus. Cancer Res.2004, 64, 4919-4926
35. Kim, J.S.; Lee, S.H.; Cho, Y.S.; Choi, J.J.; Kim, Y.H.; Lee, J.H. Enhancement of the adenoviral sensitivity of human ovarian cancer cells by transient expression of coxsackievirus and adenovirus receptor (CAR). Gynecol. Oncol. 2002, 85, 260-265
36. Tseng, J.C.; Levin, B.; Hirano, T.; Yee, H.; Pampeno, C.; Meruelo, D. In vivo antitumor activity of Sindbis viral vectors. J. Natl. Cancer Inst. 2002, 94, 1790-1802
37. Ohka, S.; Matsuda, N.; Tohyama, K.; Oda, T.; Morikawa, M.; Kuge, S.; Nomoto, A. Receptor (CD155)-dependent endocytosis of poliovirus and retrograde axonal transport of the endosome. J. Virol. 2004, 78, 7186-7198
38. Dorig, R.E.; Marcil, A.; Chopra, A.; Richardson, C.D. The human CD46 molecule is a receptor for measles virus (Edmonston strain). Cell 1993, 75, 295-305
39. Mullen, J.T.; Tanabe, K.K. Viral oncolysis. Oncologist 2002, 7, 106-119
40. Liu, T.C.; Thorne, S.H.; Kirn, D.H. Oncolytic adenoviruses for cancer gene therapy. Methods Mol. Biol. 2008, 433, 243-258
41. Kaufman, H.L.; Kohlhapp, F.J.; Zloza, A. Oncolytic viruses: A new class of immunotherapy drugs. Nat. Rev. Drug Discov. 2015, 14, 642-662
42. Chaurasiya, S.; Hew, P.; Crosley, P.; Sharon, D.; Potts, K.; Agopsowicz, K.; Long, M.; Shi, C.; Hitt, M.M. Breast cancer gene therapy using an adenovirus encoding human IL-2 under control of mammaglobin promoter/enhancer sequences. Cancer Gene Ther. 2016, 23, 178-187
43. Andreansky, S.; He, B.; van Cott, J.; McGhee, J.; Markert, J.M.; Gillespie, G.Y.; Roizman, B.; Whitley, R.J. Treatment of intracranial gliomas in immunocompetent mice using herpes simplex viruses that express murine interleukins. Gene Ther.1998, 5, 121-130
44. Parker, J.N.; Gillespie, G.Y.; Love, C.E.; Randall, S.; Whitley, R.J.; Markert, J.M. Engineered herpes simplex virus expressing IL-12 in the treatment of experimental murine brain tumors. Proc. Natl. Acad. Sci. USA 2000, 97, 2208-2213
45. Kim, J.H.; Oh, J.Y.; Park, B.H.; Lee, D.E.; Kim, J.S.; Park, H.E.; Roh, M.S.; Je, J.E.; Yoon, J.H.; Thorne, S.H.; et al. Systemic armed oncolytic and immunologic therapy for cancer with JX-594, a targeted poxvirus expressing GM-CSF. Mol. Ther. 2006, 14, 361-370
46. Han, Z.Q.; Assenberg, M.; Liu, B.L.; Wang, Y.B.; Simpson, G.; Thomas, S.; Coffin, R.S. Development of a second-generation oncolytic Herpes simplex virus expressing TNFalpha for cancer therapy. J. Gene Med. 2007, 9, 99-106
47. Heiber, J.F.; Barber, G.N. Vesicular stomatitis virus expressing tumor suppressor p53 is a highly attenuated, potent oncolytic agent. J. Virol. 2011, 85, 10440-10450
48. Bai, F.L.; Yu, Y.H.; Tian, H.; Ren, G.P.; Wang, H.; Zhou, B.; Han, X.H.; Yu, Q.Z.; Li, D.S. Genetically engineered Newcastle disease virus expressing interleukin-2 and TNF-related apoptosis-inducing ligand for cancer therapy. Cancer Biol. Ther. 2014, 15, 1226-1238
49. Breitbach, C.J.; Arulanandam, R.; De Silva, N.; Thorne, S.H.; Patt, R.; Daneshmand, M.; Moon, A.; Ilkow, C.; Burke, J.; Hwang, T.H.; et al. Oncolytic vaccinia virus disrupts tumor-associated vasculature in humans. Cancer Res. 2013, 73, 1265-1275
50. Angarita, F.A.; Acuna, S.A.; Ottolino-Perry, K.; Zerhouni, S.; McCart, J.A. Mounting a strategic offense: Fighting tumor vasculature with oncolytic viruses. Trends Mol. Med. 2013, 19, 378-392
51. Vaha-Koskela, M.J.; Heikkila, J.E.; Hinkkanen, A.E. Oncolytic viruses in cancer therapy. Cancer Lett. 2007, 254, 178-216
52. Tong, Y.; You, L.; Liu, H.; Li, L.; Meng, H.; Qian, Q.; Qian, W. Potent antitumor activity of oncolytic adenovirus expressing Beclin-1 via induction of autophagic cell death in leukemia. Oncotarget 2013, 4, 860-874
53. Kim, M.; Madlambayan, G.J.; Rahman, M.M.; Smallwood, S.E.; Meacham, A.M.; Hosaka, K.; Scott, E.W.; Cogle, C.R.; McFadden, G. Myxoma virus targets primary human leukemic stem and progenitor cells while sparing normal hematopoietic stem and progenitor cells. Leukemia 2009, 23, 2313-2317
54. Eriksson, M.; Guse, K.; Bauerschmitz, G.; Virkkunen, P.; Tarkkanen, M.; Tanner, M.; Hakkarainen, T.; Kanerva, A.; Desmond, R.A.; Pesonen, S.; et al. Oncolytic adenoviruses kill breast cancer initiating CD44+CD24−/low cells. Mol. Ther. 2007, 15, 2088-2093
55. Bauerschmitz, G.J.; Ranki, T.; Kangasniemi, L.; Ribacka, C.; Eriksson, M.; Porten, M.; Herrmann, I.; Ristimaki, A.; Virkkunen, P.; Tarkkanen, M.; et al. Tissue-specific promoters active in CD44+CD24-/low breast cancer cells. Cancer Res. 2008, 68, 5533-5539
56. Li, J.; Zeng, W.; Huang, Y.; Zhang, Q.; Hu, P.; Rabkin, S.D.; Liu, R. Treatment of breast cancer stem cells with oncolytic herpes simplex virus. Cancer Gene Ther. 2012, 19, 707-714
57. Marcato, P.; Dean, C.A.; Giacomantonio, C.A.; Lee, P.W. Oncolytic reovirus effectively targets breast cancer stem cells. Mol. Ther. 2009, 17, 972-979
58. Warner, S.G.; Haddad, D.; Au, J.; Carson, J.S.; O’Leary, M.P.; Lewis, C.; Monette, S.; Fong, Y. Oncolytic herpes simplex virus kills stem-like tumor-initiating colon cancer cells. Mol. Ther. Oncolytics 2016, 3, 16013
59. Jiang, H.; Gomez-Manzano, C.; Aoki, H.; Alonso, M.M.; Kondo, S.; McCormick, F.; Xu, J.; Kondo, Y.; Bekele, B.N.; Colman, H.; et al. Examination of the therapeutic potential of Delta-24-RGD in brain tumor stem cells: Role of autophagic cell death. J. Natl. Cancer Inst. 2007, 99, 1410-1414
60. Wakimoto, H.; Kesari, S.; Farrell, C.J.; Curry, W.T., Jr.; Zaupa, C.; Aghi, M.; Kuroda, T.; Stemmer-Rachamimov, A.; Shah, K.; Liu, T.C.; et al. Human glioblastoma-derived cancer stem cells: Establishment of invasive glioma models and treatment with oncolytic herpes simplex virus vectors. Cancer Res. 2009, 69, 3472-3481
61. Zhu, G.; Su, W.; Jin, G.; Xu, F.; Hao, S.; Guan, F.; Jia, W.; Liu, F. Glioma stem cells targeted by oncolytic virus carrying endostatin-angiostatin fusion gene and the expression of its exogenous gene in vitro. Brain Res. 2011, 1390, 59-69
62. Zhang, X.; Meng, S.; Zhang, R.; Ma, B.; Liu, T.; Yang, Y.; Xie, W.; Liu, X.; Huang, F.; Liu, T.; et al. GP73-regulated oncolytic adenoviruses possess potent killing effect on human liver cancer stem-like cells. Oncotarget 2016, 7, 29346-29358
63. Bach, P.; Abel, T.; Hoffmann, C.; Gal, Z.; Braun, G.; Voelker, I.; Ball, C.R.; Johnston, I.C.; Lauer, U.M.; Herold-Mende, C.; et al. Specific elimination of CD133+ tumor cells with targeted oncolytic measles virus. Cancer Res. 2013, 73, 865-874
64. Yang, Y.; Xu, H.; Huang, W.; Ding, M.; Xiao, J.; Yang, D.; Li, H.; Liu, X.Y.; Chu, L. Targeting lung cancer stem-like cells with TRAIL gene armed oncolytic adenovirus. J. Cell. Mol. Med. 2015, 19, 915-923
65. Yano, S.; Tazawa, H.; Hashimoto, Y.; Shirakawa, Y.; Kuroda, S.; Nishizaki, M.; Kishimoto, H.; Uno, F.; Nagasaka, T.; Urata, Y.; et al. A genetically engineered oncolytic adenovirus decoys and lethally traps quiescent cancer stem-like cells in S/G2/M phases. Clin. Cancer Res. 2013, 19, 6495-6505
66. Plaks, V.; Kong, N.; Werb, Z. The cancer stem cell niche: How essential is the niche in regulating stemness of tumor cells? Cell Stem Cell 2015, 16, 225-238
67. Seguin, L.; Desgrosellier, J.S.; Weis, S.M.; Cheresh, D.A. Integrins and cancer: Regulators of cancer stemness, metastasis, and drug resistance. Trends Cell Biol.2015, 25, 234-240
68. Vinogradov, S.; Wei, X. Cancer stem cells and drug resistance: The potential of nanomedicine. Nanomedicine 2012, 7, 597-615
69. Yang, Y.; Xu, H.; Shen, J.; Yang, Y.; Wu, S.; Xiao, J.; Xu, Y.; Liu, X.Y.; Chu, L. RGD-modifided oncolytic adenovirus exhibited potent cytotoxic effect on CAR-negative bladder cancer-initiating cells. Cell Death Dis. 2015, 6, e1760
70. Ammayappan, A.; Peng, K.W.; Russell, S.J. Characteristics of oncolytic vesicular stomatitis virus displaying tumor-targeting ligands. J. Virol. 2013, 87, 13543-13555
71. Zhao, Y.; Bao, Q.; Renner, A.; Camaj, P.; Eichhorn, M.; Ischenko, I.; Angele, M.; Kleespies, A.; Jauch, K.W.; Bruns, C. Cancer stem cells and angiogenesis. Int. J. Dev. Biol. 2011, 55, 477-482
72. Adini, A.; Adini, I.; Ghosh, K.; Benny, O.; Pravda, E.; Hu, R.; Luyindula, D.; D’Amato, R.J. The stem cell marker prominin-1/CD133 interacts with vascular endothelial growth factor and potentiates its action. Angiogenesis 2013, 16, 405-416
73. Lai, C.Y.; Schwartz, B.E.; Hsu, M.Y. CD133+ melanoma subpopulations contribute to perivascular niche morphogenesis and tumorigenicity through vasculogenic mimicry. Cancer Res. 2012, 72, 5111-5118
74. Mak, A.B.; Schnegg, C.; Lai, C.Y.; Ghosh, S.; Yang, M.H.; Moffat, J.; Hsu, M.Y. CD133-targeted niche-dependent therapy in cancer: A multipronged approach. Am. J. Pathol. 2014, 184, 1256-1262
75. Folkins, C.; Man, S.; Xu, P.; Shaked, Y.; Hicklin, D.J.; Kerbel, R.S. Anticancer therapies combining antiangiogenic and tumor cell cytotoxic effects reduce the tumor stem-like cell fraction in glioma xenograft tumors. Cancer Res. 2007, 67, 3560-3564
76. Hou, W.; Chen, H.; Rojas, J.; Sampath, P.; Thorne, S.H. Oncolytic vaccinia virus demonstrates antiangiogenic effects mediated by targeting of VEGF. Int. J. Cancer 2014, 135, 1238-1246
77. Kim, Y.; Joo, K.M.; Jin, J.; Nam, D.H. Cancer stem cells and their mechanism of chemo-radiation resistance. Int. J. Stem Cells 2009, 2, 109-114
78. McAuliffe, S.M.; Morgan, S.L.; Wyant, G.A.; Tran, L.T.; Muto, K.W.; Chen, Y.S.; Chin, K.T.; Partridge, J.C.; Poole, B.B.; Cheng, K.H.; et al. Targeting Notch, a key pathway for ovarian cancer stem cells, sensitizes tumors to platinum therapy. Proc. Natl. Acad. Sci. USA 2012, 109, E2939-E2948
79. Mato-Berciano, A.; Raimondi, G.; Maliandi, M.V.; Alemany, R.; Montoliu, L.; Fillat, C. A NOTCH-sensitive uPAR-regulated oncolytic adenovirus effectively suppresses pancreatic tumor growth and triggers synergistic anticancer effects with gemcitabine and nab-paclitaxel. Oncotarget 2017, 8, 22700-22715
80. Easwaran, H.; Tsai, H.C.; Baylin, S.B. Cancer epigenetics: Tumor heterogeneity, plasticity of stem-like states, and drug resistance. Mol. Cell 2014, 54, 716-727
81. Goldman, A.; Majumder, B.; Dhawan, A.; Ravi, S.; Goldman, D.; Kohandel, M.; Majumder, P.K.; Sengupta, S. Temporally sequenced anticancer drugs overcome adaptive resistance by targeting a vulnerable chemotherapy-induced phenotypic transition. Nat. Commun. 2015, 6, 6139
82. Safa, A.R.; Saadatzadeh, M.R.; Cohen-Gadol, A.A.; Pollok, K.E.; Bijangi-Vishehsaraei, K. Glioblastoma stem cells (GSCs) epigenetic plasticity and interconversion between differentiated non-GSCs and GSCs. Genes Dis. 2015, 2, 152-163
83. O’Brien-Ball, C.; Biddle, A. Reprogramming to developmental plasticity in cancer stem cells. Dev. Biol. 2017, 430, 266-274
84. Deheeger, M.; Lesniak, M.S.; Ahmed, A.U. Cellular plasticity regulated cancer stem cell niche: A possible new mechanism of chemoresistance. Cancer Cell. Microenviron. 2014, 1
85. Blick, T.; Hugo, H.; Widodo, E.; Waltham, M.; Pinto, C.; Mani, S.A.; Weinberg, R.A.; Neve, R.M.; Lenburg, M.E.; Thompson, E.W. Epithelial mesenchymal transition traits in human breast cancer cell lines parallel the CD44(hi)/CD24 (lo)/-stem cell phenotype in human breast cancer. J. Mammary Gland Biol. Neoplasia 2010, 15, 235-252
86. Mani, S.A.; Guo, W.; Liao, M.J.; Eaton, E.N.; Ayyanan, A.; Zhou, A.Y.; Brooks, M.; Reinhard, F.; Zhang, C.C.; Shipitsin, M.; et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008, 133, 704-715
87. Singh, A.; Settleman, J. EMT, cancer stem cells and drug resistance: An emerging axis of evil in the war on cancer. Oncogene 2010, 29, 4741-4751
88. Chen, C.H.; Chen, W.Y.; Lin, S.F.; Wong, R.J. Epithelial-mesenchymal transition enhances response to oncolytic herpesviral therapy through nectin-1. Hum. Gene Ther. 2014, 25, 539-551
89. Trumpp, A.; Wiestler, O.D. Mechanisms of Disease: Cancer stem cells--targeting the evil twin. Nat. Clin. Pract. Oncol. 2008, 5, 337-347
90. Eyler, C.E.; Rich, J.N. Survival of the fittest: Cancer stem cells in therapeutic resistance and angiogenesis. J. Clin. Oncol. 2008, 26, 2839-2845
91. Pantelidou, C.; Cherubini, G.; Lemoine, N.R.; Hallden, G. The E1B19K-deleted oncolytic adenovirus mutant AdDelta19K sensitizes pancreatic cancer cells to drug-induced DNA-damage by down-regulating Claspin and Mre11. Oncotarget 2016, 7, 15703-15724
92. Cherubini, G.; Kallin, C.; Mozetic, A.; Hammaren-Busch, K.; Muller, H.; Lemoine, N.R.; Hallden, G. The oncolytic adenovirus AdDeltaDelta enhances selective cancer cell killing in combination with DNA-damaging drugs in pancreatic cancer models. Gene Ther. 2011, 18, 1157-1165
93. Aghi, M.; Rabkin, S.; Martuza, R.L. Effect of chemotherapy-induced DNA repair on oncolytic herpes simplex viral replication. J. Natl. Cancer Inst. 2006, 98, 38-50
94. Xie, A.; Scully, R. Hijacking the DNA damage response to enhance viral replication: Gamma-herpesvirus 68 orf36 phosphorylates histone H2AX. Mol. Cell 2007, 27, 178-179
95. Cohen, M.H.; Shen, Y.L.; Keegan, P.; Pazdur, R. FDA drug approval summary: Bevacizumab (Avastin®) as treatment of recurrent glioblastoma multiforme. Oncologist 2009, 14, 1131-1138
96. Kane, R.C.; Farrell, A.T.; Madabushi, R.; Booth, B.; Chattopadhyay, S.; Sridhara, R.; Justice, R.; Pazdur, R. Sorafenib for the treatment of unresectable hepatocellular carcinoma. Oncologist 2009, 14, 95-100
97. Ma, J.; Waxman, D.J. Combination of antiangiogenesis with chemotherapy for more effective cancer treatment. Mol. Cancer Ther. 2008, 7, 3670-3684
98. Rockwell, S.; Dobrucki, I.T.; Kim, E.Y.; Marrison, S.T.; Vu, V.T. Hypoxia and radiation therapy: Past history, ongoing research, and future promise. Curr. Mol. Med. 2009, 9, 442-458
99. Teicher, B.A. Hypoxia and drug resistance. Cancer Metastasis Rev. 1994, 13, 139-168
100. Benencia, F.; Courreges, M.C.; Conejo-Garcia, J.R.; Buckanovich, R.J.; Zhang, L.; Carroll, R.H.; Morgan, M.A.; Coukos, G. Oncolytic HSV exerts direct antiangiogenic activity in ovarian carcinoma. Hum. Gene Ther. 2005, 16, 765-778
101. Saito, Y.; Sunamura, M.; Motoi, F.; Abe, H.; Egawa, S.; Duda, D.G.; Hoshida, T.; Fukuyama, S.; Hamada, H.; Matsuno, S. Oncolytic replication-competent adenovirus suppresses tumor angiogenesis through preserved E1A region. Cancer Gene Ther. 2006, 13, 242-252
102. Breitbach, C.J.; Paterson, J.M.; Lemay, C.G.; Falls, T.J.; McGuire, A.; Parato, K.A.; Stojdl, D.F.; Daneshmand, M.; Speth, K.; Kirn, D.; et al. Targeted inflammation during oncolytic virus therapy severely compromises tumor blood flow. Mol. Ther.2007, 15, 1686-1693
103. Fasullo, M.; Burch, A.D.; Britton, A. Hypoxia enhances the replication of oncolytic herpes simplex virus in p53breast cancer cells. Cell Cycle 2009, 8, 2194-2197
104. Hay, J.G. The potential impact of hypoxia on the success of oncolytic virotherapy. Curr. Opin. Mol. Ther. 2005, 7, 353-358
105. Hiley, C.T.; Yuan, M.; Lemoine, N.R.; Wang, Y. Lister strain vaccinia virus, a potential therapeutic vector targeting hypoxic tumours. Gene Ther. 2010, 17, 281-287
106. Reinblatt, M.; Pin, R.H.; Federoff, H.J.; Fong, Y. Utilizing tumor hypoxia to enhance oncolytic viral therapy in colorectal metastases. Ann. Surg. 2004, 239, 892-902
107. Pajonk, F.; Vlashi, E.; McBride, W.H. Radiation resistance of cancer stem cells: The 4 R’s of radiobiology revisited. Stem Cells 2010, 28, 639-648
108. Holtz, M.; Forman, S.J.; Bhatia, R. Growth factor stimulation reduces residual quiescent chronic myelogenous leukemia progenitors remaining after imatinib treatment. Cancer Res. 2007, 67, 1113-1120
109. Lechman, E.R.; Gentner, B.; Ng, S.W.K.; Schoof, E.M.; van Galen, P.; Kennedy, J.A.; Nucera, S.; Ciceri, F.; Kaufmann, K.B.; Takayama, N.; et al. miR-126 Regulates Distinct Self-Renewal Outcomes in Normal and Malignant Hematopoietic Stem Cells. Cancer Cell 2016, 29, 602-606
110. Wang, H.; Chen, N.G.; Minev, B.R.; Szalay, A.A. Oncolytic vaccinia virus GLV-1h68 strain shows enhanced replication in human breast cancer stem-like cells in comparison to breast cancer cells. J. Transl. Med. 2012, 10, 167
111. Chaurasiya, S.; Favis, N.; Umer, B.; Potts, K.; Noyce, R.; Irwin, C.; Evans, D.H.; Hitt, M.M. F4L-deleted Vaccinia Virus Exhibits Oncolytic Activity in Breast Cancer Models. Sci. Rep. (under revision).
112. Levine, P.H.; Steinhorn, S.C.; Ries, L.G.; Aron, J.L. Inflammatory breast cancer: The experience of the surveillance, epidemiology, and end results (SEER) program. J. Natl. Cancer Inst. 1985, 74, 291-297
113. Gupta, P.B.; Fillmore, C.M.; Jiang, G.; Shapira, S.D.; Tao, K.; Kuperwasser, C.; Lander, E.S. Stochastic state transitions give rise to phenotypic equilibrium in populations of cancer cells. Cell 2011, 146, 633-644
114. Hoffmeyer, M.R.; Wall, K.M.; Dharmawardhane, S.F. In vitro analysis of the invasive phenotype of SUM 149, an inflammatory breast cancer cell line. Cancer Cell Int. 2005, 5, 11
115. Butler, M.C.; Ehrlich, S.B. Positional influences on job satisfaction and job performance: A multivariate, predictive approach. Psychol. Rep. 1991, 69, 855-865
116. Skog, J.; Edlund, K.; Bergenheim, A.T.; Wadell, G. Adenoviruses 16 and CV23 efficiently transduce human low-passage brain tumor and cancer stem cells. Mol. Ther. 2007, 15, 2140-2145
117. Yoo, S.Y.; Bang, S.Y.; Jeong, S.N.; Kang, D.H.; Heo, J. A cancer-favoring oncolytic vaccinia virus shows enhanced suppression of stem-cell like colon cancer. Oncotarget 2016, 7, 16479-16489
118. Ma, S.; Chan, K.W.; Hu, L.; Lee, T.K.; Wo, J.Y.; Ng, I.O.; Zheng, B.J.; Guan, X.Y. Identification and characterization of tumorigenic liver cancer stem/progenitor cells. Gastroenterology 2007, 132, 2542-2556
119. Sagara, M.; Inoue, H.; Miyamoto, S.; Sakamoto, C.; Nakano, Y.; Takayama, K.; Shimizu, H.; Nakanishi, Y.; Tani, K. CVB3 Infection Elicits Potent Oncolytic Activity Against Lung Cancer Stem Cells. Mol. Ther. 2013, 21, S170
120. Chaurasiya, S.; Chen, N.G.; Fong, Y.; City of Hope National Medical Center, Duarte, CA 91010, USA. Personal observation, 2017.
121. Zhang, X.; Komaki, R.; Wang, L.; Fang, B.; Chang, J.Y. Treatment of radioresistant stem-like esophageal cancer cells by an apoptotic gene-armed, telomerase-specific oncolytic adenovirus. Clin. Cancer Res. 2008, 14, 2813-2823
122. Schatton, T.; Frank, M.H. The in vitro spheroid melanoma cell culture assay: Cues on tumor initiation? J. Investig. Dermatol. 2010, 130, 1769-1771
123. Frank, N.Y.; Schatton, T.; Frank, M.H. The therapeutic promise of the cancer stem cell concept. J. Clin. Investig. 2010, 120, 41-50
124. Adusumilli, P.S.; Stiles, B.M.; Chan, M.K.; Chou, T.C.; Wong, R.J.; Rusch, V.W.; Fong, Y. Radiation therapy potentiates effective oncolytic viral therapy in the treatment of lung cancer. Ann. Thorac. Surg. 2005, 80, 409-416
125. Dai, M.H.; Zamarin, D.; Gao, S.P.; Chou, T.C.; Gonzalez, L.; Lin, S.F.; Fong, Y. Synergistic action of oncolytic herpes simplex virus and radiotherapy in pancreatic cancer cell lines. Br. J. Surg 2010, 97, 1385-1394
126. Huang, B.; Sikorski, R.; Kirn, D.H.; Thorne, S.H. Synergistic anti-tumor effects between oncolytic vaccinia virus and paclitaxel are mediated by the IFN response and HMGB1. Gene Ther. 2011, 18, 164-172
127. Heinemann, L.; Simpson, G.R.; Boxall, A.; Kottke, T.; Relph, K.L.; Vile, R.; Melcher, A.; Prestwich, R.; Harrington, K.J.; Morgan, R.; et al. Synergistic effects of oncolytic reovirus and docetaxel chemotherapy in prostate cancer. BMC Cancer 2011, 11, 221.