White paper on microbial anti-cancer therapy and prevention

Journal for ImmunoTherapy of Cancer

Volumn 6, Issue 1, 2018, Pages

  Forbes, Neil S ^a   Coffin, Robert S ^b   Deng, Liang ^c   Evgin, Laura ^d   Fiering, Steve ^e   Giacalone, Matthew ^f   Gravekamp, Claudia ^g   Gulley, James L ^h   Gunn, Hal ⁱ   Hoffman, Robert M ^j,k   Kaur, Balveen ^l   Liu, Ke ^m   Lyerly, Herbert Kim ⁿ   Marciscano, Ariel E ^h   Moradian, Eddie ^o   Ruppel, Sheryl ^p   Saltzman, Daniel A ^q   Tattersall, Peter J ^r   Thorne, Steve ^s   Vile, Richard G ^d   Zhang, Halle Huihong ^t   Zhou, Shibin ^u   McFadden, Grant ^v   more..

^a University of Massachusetts   (United States)

^b Replimune Ltd   (United States)

^c MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^d MAYO CLINIC   (United States)

^e DARTMOUTH MEDICAL SCHOOL   (United States)

^f VaxiionTherapeutics   (United States)

^g ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^h NATIONAL CANCER INSTITUTE   (United States)

ⁱ Qu Biologics   (Canada)

^j UNIVERSITY OF CALIFORNIA   (United States)

^k ANTICANCER INC   (United States)

^l UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^m CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

ⁿ DUKE UNIVERSITY   (United States)

^o Salspera   (United States)

^p FREDERICK NATIONAL LABORATORY FOR CANCER RESEARCH   (United States)

^q UNIVERSITY OF MINNESOTA   (United States)

^r YALE UNIVERSITY   (United States)

^s UNIVERSITY OF PITTSBURGH   (United States)

^t BioMed Valley Discoveries Inc   (United States)

^u JOHNS HOPKINS UNIVERSITY   (United States)

^v ARIZONA STATE UNIVERSITY   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

CANCER VACCINE; IPILIMUMAB; ONCOLYTIC VIRUS; TUMOR ANTIGEN;

ADENOVIRIDAE; APOPTOSIS; ARTICLE; ASTROCYTOMA CELL LINE; BACTERIAL ANTICANCER THERAPY; BIFIDOBACTERIUM; BLADDER CANCER; BRAIN TUMOR; CANCER IMMUNIZATION; CANCER IMMUNOTHERAPY; CANCER PAIN; CANCER THERAPY; CARCINOGENESIS; CLOSTRIDIUM; COLORECTAL CARCINOMA; ESCHERICHIA; EUROPEAN MEDICINES AGENCY; GENE EXPRESSION; GENE SEQUENCE; GLIOBLASTOMA; HEAD AND NECK CANCER; HUMAN; IMMUNE RESPONSE; IMMUNOGENICITY; LACTOBACILLUS; LISTERIA; LIVER CANCER; LIVER CELL CARCINOMA; LUNG CANCER; MALIGNANT NEOPLASM; MELANOMA; METASTASIS; METASTATIC COLORECTAL CANCER; METASTATIC MELANOMA; MICROBIAL ANTICANCER THERAPY; MICROBIAL THERAPY; MORTALITY; MULTIPLE MYELOMA; NONHUMAN; ONCOLYTIC VIROTHERAPY; OROPHARYNX CANCER; OVARY CANCER; PANCREAS ADENOCARCINOMA; PANCREAS CANCER; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PLEURA MESOTHELIOMA; PRIORITY JOURNAL; PROSTATE CANCER; RANDOMIZED CONTROLLED TRIAL (TOPIC); SALMONELLA; SIGNAL TRANSDUCTION; SOLID MALIGNANT NEOPLASM; SQUAMOUS CELL CARCINOMA; TUMOR GROWTH; TUMOR INVASION; TUMOR MICROENVIRONMENT; TUMOR SPECIFIC INFECTIOUS MICROBE; TUMOR SUPPRESSOR GENE; UTERINE CERVIX CANCER; ANIMAL; BACTERIUM; BIOLOGICAL THERAPY; CLINICAL STUDY; GENE VECTOR; GENETIC ENGINEERING; GENETICS; IMMUNOLOGY; MULTIMODALITY CANCER THERAPY; NEOPLASM; PRECLINICAL STUDY; PROCEDURES; TREATMENT OUTCOME; VIRUS;

ANIMALS; BACTERIA; BIOLOGICAL THERAPY; CANCER VACCINES; CLINICAL STUDIES AS TOPIC; COMBINED MODALITY THERAPY; DRUG EVALUATION, PRECLINICAL; GENETIC ENGINEERING; GENETIC VECTORS; HUMANS; NEOPLASMS; ONCOLYTIC VIROTHERAPY; TREATMENT OUTCOME; VIRUSES;

EID: 85051295512     PISSN: None     EISSN: 20511426     Source Type: Journal    
DOI: 10.1186/s40425-018-0381-3     Document Type: Article

References (227)

1. Kocijancic D, Leschner S, Felgner S, Komoll RM, Frahm M, Pawar V, Weiss S. Therapeutic benefit of Salmonella attributed to LPS and TNF-alpha is exhaustible and dictated by tumor susceptibility. Oncotarget. 2017;8:36492-508.
2. Ganai S, Arenas RB, Sauer JP, Bentley B, Forbes NS. In tumors Salmonella migrate away from vasculature toward the transition zone and induce apoptosis. Cancer Gene Ther. 2011;18:457-66.
3. Brown JM, Wilson WR. Exploiting tumour hypoxia in cancer treatment. Nat Rev Cancer. 2004;4:437-47.
4. Hoffman RM. (ed.) Bacterial Therapy of Cancer: Methods and Protocols. Methods in Molecular Biology. Volume 1409. Totowa: Humana Press Inc; 2016. p. 1-186.
5. McCarthy EF. The toxins of William B. Coley and the treatment of bone and soft-tissue sarcomas. Iowa Orthop J. 2006;26:154-8.
6. Richardson MA, Ramirez T, Russell NC, Moye LA. Coley toxins immunotherapy: a retrospective review. Altern Ther Health Med. 1999;5:42-7.
7. Cann SAH, van Netten JP, van Netten C. Dr William Coley and tumour regression: a place in history or in the future. Postgraduate Medical Journal. 2003;79:672-80.
8. Zhao M, Yang M, Li XM, Jiang P, Baranov E, Li S, Xu M, Penman S, Hoffman RM. Tumor-targeting bacterial therapy with amino acid auxotrophs of GFP-expressing Salmonella typhimurium. Proc Natl Acad Sci U S A. 2005;102:755-60.
9. Moese JR, Moese G. Oncolysis by clostridia. I. Activity of clostridium butyricum (m-55) and other nonpathogenic clostridia against the Ehrlich carcinoma. Cancer Res. 1964;24:212-6.
10. Roberts NJ, Zhang L, Janku F, Collins A, Bai RY, Staedtke V, Rusk AW, Tung D, Miller M, Roix J, et al. Intratumoral injection of Clostridium novyi-NT spores induces antitumor responses. Sci Transl Med. 2014;6:249ra111.
11. Kelly E, Russell SJ. History of oncolytic viruses: genesis to genetic engineering. Mol Ther. 2007;15:651-9.
12. Miest TS, Cattaneo R. New viruses for cancer therapy: meeting clinical needs. Nat Rev Microbiol. 2014;12:23-34.
13. d'Herelle FH. Sur un microbe invisible antagoniste des bacilles dysenteriques. C R Hebd Seances Acad Sci Paris. 1917;165:373-90.
14. Dock G. The influence of complicating diseases upon leukemia. Am J Med Sci. 1904;127:563-92.
15. Pelner L, Fowler GA, Nauts HC. Effects of concurrent infections and their toxins on the course of leukemia. Acta Med Scand Suppl. 1958;338:1-47.
16. Hoster HA, Zanes RP Jr, Von Haam E. Studies in Hodgkin's syndrome; the association of viral hepatitis and Hodgkin's disease; a preliminary report. Cancer Res. 1949;9:473-80.
17. Martuza RL, Malick A, Markert JM, Ruffner KL, Coen DM. Experimental therapy of human glioma by means of a genetically engineered virus mutant. Science. 1991;252:854-6.
18. Forbes NS. Engineering the perfect (bacterial) cancer therapy. Nature Reviews Cancer. 2010;10:785-94.
19. Felgner S, Kocijancic D, Frahm M, Weiss S. Bacteria in Cancer Therapy: Renaissance of an Old Concept. Int J Microbiol. 2016;2016:8451728.
20. Andtbacka RH, Kaufman HL, Collichio F, Amatruda T, Senzer N, Chesney J, Delman KA, Spitler LE, Puzanov I, Agarwala SS, et al. Talimogene Laherparepvec Improves Durable Response Rate in Patients With Advanced Melanoma. J Clin Oncol. 2015;33:2780-8.
21. Breitbach CJ, Lichty BD, Bell JC. Oncolytic Viruses: Therapeutics With an Identity Crisis. EBioMedicine. 2016;9:31-6.
22. Ilkow CS, Swift SL, Bell JC, Diallo JS. From scourge to cure: tumour-selective viral pathogenesis as a new strategy against cancer. PLoS Pathog. 2014;10:e1003836.
23. Pol J, Buque A, Aranda F, Bloy N, Cremer I, Eggermont A, Erbs P, Fucikova J, Galon J, Limacher JM, et al. Trial Watch-Oncolytic viruses and cancer therapy. Oncoimmunology. 2016;5:e1117740.
24. Dang LH, Bettegowda C, Huso DL, Kinzler KW, Vogelstein B. Combination bacteriolytic therapy for the treatment of experimental tumors. Proc Natl Acad Sci U S A. 2001;98:15155-60.
25. Ganai S, Arenas RB, Forbes NS. Tumour-targeted delivery of TRAIL using Salmonella typhimurium enhances breast cancer survival in mice. Br J Cancer. 2009;101:1683-91.
26. Agrawal N, Bettegowda C, Cheong I, Geschwind JF, Drake CG, Hipkiss EL, Tatsumi M, Dang LH, Diaz LA Jr, Pomper M, et al. Bacteriolytic therapy can generate a potent immune response against experimental tumors. Proc Natl Acad Sci U S A. 2004;101:15172-7.
27. Thamm DH, Kurzman ID, King I, Li Z, Sznol M, Dubielzig RR, Vail DM, MacEwen EG. Systemic administration of an attenuated, tumor-targeting Salmonella typhimurium to dogs with spontaneous neoplasia: phase I evaluation. Clin Cancer Res. 2005;11:4827-34.
28. Clairmont C, Lee KC, Pike J, Ittensohn M, Low KB, Pawelek J, Bermudes D, Brecher SM, Margitich D, Turnier J, et al. Biodistribution and genetic stability of the novel antitumor agent VNP20009, a genetically modified strain of Salmonella typhimurium. J Infect Dis. 2000;181:1996-2002.
29. Diaz LA Jr, Cheong I, Foss CA, Zhang X, Peters BA, Agrawal N, Bettegowda C, Karim B, Liu G, Khan K, et al. Pharmacologic and toxicologic evaluation of C. novyi-NT spores. Toxicol Sci. 2005;88:562-75.
30. Wood LM, Paterson Y. Attenuated Listeria monocytogenes: a powerful and versatile vector for the future of tumor immunotherapy. Front Cell Infect Microbiol. 2014;4:51.
31. Le DT, Wang-Gillam A, Picozzi V, Greten TF, Crocenzi T, Springett G, Morse M, Zeh H, Cohen D, Fine RL, et al. Safety and survival with GVAX pancreas prime and Listeria Monocytogenes-expressing mesothelin (CRS-207) boost vaccines for metastatic pancreatic cancer. J Clin Oncol. 2015;33:1325-33.
32. Miles B, Safran HP, Monk BJ. Therapeutic options for treatment of human papillomavirus-associated cancers - novel immunologic vaccines: ADXS11-001. Gynecol Oncol Res Pract. 2017;4:10.
33. Maciag PC, Radulovic S, Rothman J. The first clinical use of a live-attenuated Listeria monocytogenes vaccine: a Phase I safety study of Lm-LLO-E7 in patients with advanced carcinoma of the cervix. Vaccine. 2009;27:3975-83.
34. Safran H, Leonard KL, Perez K, Vrees M, Klipfel A, Schechter S, Oldenburg N, Roth L, Shah N, Rosati K, et al. Tolerability of ADXS11-001 Lm-LLO Listeria Based Immunotherapy With Mitomycin, Fluorouracil and Radiation for Anal Cancer. Int J Radiat Oncol Biol Phys. 2018;100:1175-78.
35. Le DT, Brockstedt DG, Nir-Paz R, Hampl J, Mathur S, Nemunaitis J, Sterman DH, Hassan R, Lutz E, Moyer B, et al. A live-attenuated Listeria vaccine (ANZ-100) and a live-attenuated Listeria vaccine expressing mesothelin (CRS-207) for advanced cancers: phase I studies of safety and immune induction. Clin Cancer Res. 2012;18:858-68.
36. Kamat AM, Flaig TW, Grossman HB, Konety B, Lamm D, O'Donnell MA, Uchio E, Efstathiou JA, Taylor JA 3rd. Expert consensus document: Consensus statement on best practice management regarding the use of intravesical immunotherapy with BCG for bladder cancer. Nat Rev Urol. 2015;12:225-35.
37. Sharma P, Allison JP. The future of immune checkpoint therapy. Science. 2015;348:56-61.
38. Schildberg FA, Klein SR, Freeman GJ, Sharpe AH. Coinhibitory Pathways in the B7-CD28 Ligand-Receptor Family. Immunity. 2016;44:955-72.
39. Topalian SL, Drake CG, Pardoll DM. Immune checkpoint blockade: a common denominator approach to cancer therapy. Cancer Cell. 2015;27:450-61.
40. Zou W, Wolchok JD, Chen L. PD-L1 (B7-H1) and PD-1 pathway blockade for cancer therapy: Mechanisms, response biomarkers, and combinations. Sci Transl Med. 2016;8:328rv324.
41. Pitt JM, Vetizou M, Daillere R, Roberti MP, Yamazaki T, Routy B, Lepage P, Boneca IG, Chamaillard M, Kroemer G, Zitvogel L. Resistance Mechanisms to Immune-Checkpoint Blockade in Cancer: Tumor-Intrinsic and -Extrinsic Factors. Immunity. 2016;44:1255-69.
42. Shin DS, Zaretsky JM, Escuin-Ordinas H, Garcia-Diaz A, Hu-Lieskovan S, Kalbasi A, Grasso CS, Hugo W, Sandoval S, Torrejon DY, et al. Primary Resistance to PD-1 Blockade Mediated by JAK1/2 Mutations. Cancer Discov. 2017;7:188-201.
43. Myint ZW, Goel G. Role of modern immunotherapy in gastrointestinal malignancies: a review of current clinical progress. J Hematol Oncol. 2017;10:86.
44. Murphy AG, Kelly RJ. The Evolving Role of Checkpoint Inhibitors in the Management of Gastroesophageal Cancer. Hematol Oncol Clin North Am. 2017;31:485-98.
45. Laccetti AL, Subudhi SK. Immunotherapy for metastatic prostate cancer: immuno-cold or the tip of the iceberg? Curr Opin Urol. 2017;27:566-71.
46. Foley K, Kim V, Jaffee E, Zheng L. Current progress in immunotherapy for pancreatic cancer. Cancer Lett. 2016;381:244-51.
47. Prieto J, Melero I, Sangro B. Immunological landscape and immunotherapy of hepatocellular carcinoma. Nat Rev Gastroenterol Hepatol. 2015;12:681-700.
48. Yarchoan M, Hopkins A, Jaffee EM. Tumor Mutational Burden and Response Rate to PD-1 Inhibition. N Engl J Med. 2017;377:2500-1.
49. Anagnostou V, Smith KN, Forde PM, Niknafs N, Bhattacharya R, White J, Zhang T, Adleff V, Phallen J, Wali N, et al. Evolution of Neoantigen Landscape during Immune Checkpoint Blockade in Non-Small Cell Lung Cancer. Cancer Discov. 2017;7:264-76.
50. Gao J, Ward JF, Pettaway CA, Shi LZ, Subudhi SK, Vence LM, Zhao H, Chen J, Chen H, Efstathiou E, et al. VISTA is an inhibitory immune checkpoint that is increased after ipilimumab therapy in patients with prostate cancer. Nat Med. 2017;23:551-5.
51. George S, Miao D, Demetri GD, Adeegbe D, Rodig SJ, Shukla S, Lipschitz M, Amin-Mansour A, Raut CP, Carter SL, et al. Loss of PTEN Is Associated with Resistance to Anti-PD-1 Checkpoint Blockade Therapy in Metastatic Uterine Leiomyosarcoma. Immunity. 2017;46:197-204.
52. Spranger S, Bao R, Gajewski TF. Melanoma-intrinsic beta-catenin signalling prevents anti-tumour immunity. Nature. 2015;523:231-5.
53. Peng W, Chen JQ, Liu C, Malu S, Creasy C, Tetzlaff MT, Xu C, McKenzie JA, Zhang C, Liang X, et al. Loss of PTEN Promotes Resistance to T Cell-Mediated Immunotherapy. Cancer Discov. 2016;6:202-16.
54. Zaretsky JM, Garcia-Diaz A, Shin DS, Escuin-Ordinas H, Hugo W, Hu-Lieskovan S, Torrejon DY, Abril-Rodriguez G, Sandoval S, Barthly L, et al. Mutations Associated with Acquired Resistance to PD-1 Blockade in Melanoma. N Engl J Med. 2016;375:819-29.
55. Sade-Feldman M, Jiao YJ, Chen JH, Rooney MS, Barzily-Rokni M, Eliane JP, Bjorgaard SL, Hammond MR, Vitzthum H, Blackmon SM, et al. Resistance to checkpoint blockade therapy through inactivation of antigen presentation. Nat Commun. 2017;8:1136.
56. Chiocca EA, Aguilar LK, Bell SD, Kaur B, Hardcastle J, Cavaliere R, McGregor J, Lo S, Ray-Chaudhuri A, Chakravarti A, et al. Phase IB study of gene-mediated cytotoxic immunotherapy adjuvant to up-front surgery and intensive timing radiation for malignant glioma. J Clin Oncol. 2011;29:3611-9.
57. Sonawane P, Choi YA, Pandya H, Herpai DM, Fokt I, Priebe W, Debinski W. Novel Molecular Multilevel Targeted Antitumor Agents. Cancer Transl Med. 2017;3:69-79.
58. Assi H, Candolfi M, Baker G, Mineharu Y, Lowenstein PR, Castro MG. Gene therapy for brain tumors: basic developments and clinical implementation. Neurosci Lett. 2012;527:71-7.
59. Cattaneo R, Russell SJ. How to develop viruses into anticancer weapons. PLoS Pathog. 2017;13:e1006190.
60. Waehler R, Russell SJ, Curiel DT. Engineering targeted viral vectors for gene therapy. Nature Reviews Genetics. 2007;8:573-87.
61. Guo ZS, Thorne SH, Bartlett DL. Oncolytic virotherapy: Molecular targets in tumor-selective replication and carrier cell-mediated delivery of oncolytic viruses. Biochimica Et Biophysica Acta-Reviews on Cancer. 2008;1785:217-31.
62. Cattaneo R, Miest T, Shashkova EV, Barry MA. Reprogrammed viruses as cancer therapeutics: targeted, armed and shielded. Nature Reviews Microbiology. 2008;6:529-40.
63. Hartman ZC, Wei J, Glass OK, Guo H, Lei G, Yang XY, Osada T, Hobeika A, Delcayre A, Le Pecq JB, et al. Increasing vaccine potency through exosome antigen targeting. Vaccine. 2011;29:9361-7.
64. Nair SK, Boczkowski D, Morse M, Cumming RI, Lyerly HK, Gilboa E. Induction of primary carcinoembryonic antigen (CEA)-specific cytotoxic T lymphocytes in vitro using human dendritic cells transfected with RNA. Nat Biotechnol. 1998;16:364-9.
65. Ren J, Gwin WR, Zhou X, Wang X, Huang H, Jiang N, Zhou L, Agarwal P, Hobeika A, Crosby E, et al. Adaptive T cell responses induced by oncolytic Herpes Simplex Virus-granulocyte macrophage-colony-stimulating factor therapy expanded by dendritic cell and cytokine-induced killer cell adoptive therapy. Oncoimmunology. 2017;6:e1264563.
66. Hartman ZC, Osada T, Glass O, Yang XY, Lei GJ, Lyerly HK, Clay TM. Ligand-independent toll-like receptor signals generated by ectopic overexpression of MyD88 generate local and systemic antitumor immunity. Cancer Res. 2010;70:7209-20.
67. Hammerich L, Binder A, Brody JD. In situ vaccination: Cancer immunotherapy both personalized and off-the-shelf. Mol Oncol. 2015;9:1966-81.
68. Pierce RH, Campbell JS, Pai SI, Brody JD, Kohrt HE. In-situ tumor vaccination: Bringing the fight to the tumor. Hum Vaccin Immunother. 2015;11:1901-9.
69. Richman SP, Gutterman JU, Hersh EM. Cancer immunotherapy. Can Med Assoc J. 1979;120:322-4. 329
70. Rook AH, Gelfand JM, Wysocka M, Troxel AB, Benoit B, Surber C, Elenitsas R, Buchanan MA, Leahy DS, Watanabe R, et al. Topical resiquimod can induce disease regression and enhance T-cell effector functions in cutaneous T-cell lymphoma. Blood. 2015;126:1452-61.
71. Lizotte PH, Wen AM, Sheen MR, Fields J, Rojanasopondist P, Steinmetz NF, Fiering S. In situ vaccination with cowpea mosaic virus nanoparticles suppresses metastatic cancer. Nat Nanotechnol. 2016;11:295-303.
72. Yarchoan M, Johnson BA 3rd, Lutz ER, Laheru DA, Jaffee EM. Targeting neoantigens to augment antitumour immunity. Nat Rev Cancer. 2017;17:569.
73. Elsedawy NB, Russell SJ. Oncolytic vaccines. Expert Rev Vaccines. 2013;12:1155-72.
74. Perez OD, Logg CR, Hiraoka K, Diago O, Burnett R, Inagaki A, Jolson D, Amundson K, Buckley T, Lohse D, et al. Design and selection of Toca 511 for clinical use: modified retroviral replicating vector with improved stability and gene expression. Mol Ther. 2012;20:1689-98.
75. Lawler SE, Speranza MC, Cho CF, Chiocca EA. Oncolytic Viruses in Cancer Treatment: A Review. JAMA Oncol. 2017;3:841-9.
76. Middlebrook JL, Dorland RB. Bacterial toxins: cellular mechanisms of action. Microbiol Rev. 1984;48:199-221.
77. Uchugonova A, Zhang Y, Salz R, Liu F, Suetsugu A, Zhang L, Koenig K, Hoffman RM, Zhao M. Imaging the Different Mechanisms of Prostate Cancer Cell-killing by Tumor-targeting Salmonella typhimurium A1-R. Anticancer Res. 2015;35:5225-9.
78. Chang WW, Lee CH. Salmonella as an innovative therapeutic antitumor agent. Int J Mol Sci. 2014;15:14546-54.
79. Kasinskas RW, Forbes NS. Salmonella typhimurium lacking ribose chemoreceptors localize in tumor quiescence and induce apoptosis. Cancer research. 2007;67:3201-9.
80. Zhang M, Swofford CA, Forbes NS. Lipid A controls the robustness of intratumoral accumulation of attenuated Salmonella in mice. International journal of cancer. 2014;135:647-57.
81. St. Jean AT, Swofford CA, Brentzel ZJ, Forbes NS. Bacterial delivery of Staphylococcus aureus alpha-hemolysin causes tumor regression and necrosis in murine tumors. Molecular Therapy. 2014;22:1266-74.
82. Seavey MM, Maciag PC, Al-Rawi N, Sewell D, Paterson Y. An anti-vascular endothelial growth factor receptor 2/fetal liver kinase-1 Listeria monocytogenes anti-angiogenesis cancer vaccine for the treatment of primary and metastatic Her-2/neu+ breast tumors in a mouse model. J Immunol. 2009;182:5537-46.
83. Rankin EB, Giaccia AJ. Hypoxic control of metastasis. Science. 2016;352:175-80.
84. Jahangir A, Chandra D, Quispe-Tintaya W, Singh M, Selvanesan BC, Gravekamp C. Immunotherapy with Listeria reduces metastatic breast cancer in young and old mice through different mechanisms. Oncoimmunology. 2017;6:e1342025.
85. Sorenson BS, Banton KL, Frykman NL, Leonard AS, Saltzman DA. Attenuated Salmonella typhimurium with interleukin 2 gene prevents the establishment of pulmonary metastases in a model of osteosarcoma. J Pediatr Surg. 2008;43:1153-8.
86. Chen DS, Mellman I. Oncology meets immunology: the cancer-immunity cycle. Immunity. 2013;39:1-10.
87. Galluzzi L, Buque A, Kepp O, Zitvogel L, Kroemer G. Immunogenic cell death in cancer and infectious disease. Nat Rev Immunol. 2017;17:97-111.
88. Kepp O, Senovilla L, Vitale I, Vacchelli E, Adjemian S, Agostinis P, Apetoh L, Aranda F, Barnaba V, Bloy N, et al. Consensus guidelines for the detection of immunogenic cell death. Oncoimmunology. 2014;3:e955691.
89. Mogensen TH. Pathogen recognition and inflammatory signaling in innate immune defenses. Clin Microbiol Rev. 2009;22:240-73. Table of Contents
90. Lizotte PH, Baird JR, Stevens CA, Lauer P, Green WR, Brockstedt DG, Fiering SN. Attenuated Listeria monocytogenes reprograms M2-polarized tumor-associated macrophages in ovarian cancer leading to iNOS-mediated tumor cell lysis. Oncoimmunology. 2014;3:e28926.
91. Stern C, Kasnitz N, Kocijancic D, Trittel S, Riese P, Guzman CA, Leschner S, Weiss S. Induction of CD4(+) and CD8(+) anti-tumor effector T cell responses by bacteria mediated tumor therapy. Int J Cancer. 2015;137:2019-28.
92. Richer MJ, Nolz JC, Harty JT. Pathogen-specific inflammatory milieux tune the antigen sensitivity of CD8(+) T cells by enhancing T cell receptor signaling. Immunity. 2013;38:140-52.
93. Din MO, Danino T, Prindle A, Skalak M, Selimkhanov J, Allen K, Julio E, Atolia E, Tsimring LS, Bhatia SN, Hasty J. Synchronized cycles of bacterial lysis for in vivo delivery. Nature. 2016;536:81-5.
94. Shizuya H, Birren B, Kim UJ, Mancino V, Slepak T, Tachiiri Y, Simon M. Cloning and stable maintenance of 300-kilobase-pair fragments of human DNA in Escherichia coli using an F-factor-based vector. Proc Natl Acad Sci U S A. 1992;89:8794-7.
95. Forbes NS. Profile of a bacterial tumor killer. Nature biotechnology. 2006;24:1484-5.
96. Mengesha A, Dubois L, Lambin P, Landuyt W, Chiu RK, Wouters BG, Theys J. Development of a flexible and potent hypoxia-inducible promoter for tumor-targeted gene expression in attenuated Salmonella. Cancer Biology & Therapy. 2006;5:1120-8.
97. Arrach N, Zhao M, Porwollik S, Hoffman RM, McClelland M. Salmonella promoters preferentially activated inside tumors. Cancer research. 2008;68:4827-32.
98. Swofford CA, Van Dessel N, Forbes NS. Quorum-sensing Salmonella selectively trigger protein expression within tumors. Proc Natl Acad Sci U S A. 2015;112:3457-62.
99. Jiang SN, Phan TX, Nam TK, Nguyen VH, Kim HS, Bom HS, Choy HE, Hong Y, Min JJ. Inhibition of Tumor Growth and Metastasis by a Combination of Escherichia coli-mediated Cytolytic Therapy and Radiotherapy. Mol Ther. 2010;18(3):635-42.
100. Ryan RM, Green J, Williams PJ, Tazzyman S, Hunt S, Harmey JH, Kehoe SC, Lewis CE. Bacterial delivery of a novel cytolysin to hypoxic areas of solid tumors. Gene Ther. 2009;16:329-39.
101. St Jean AT, Swofford CA, Panteli JT, Brentzel ZJ, Forbes NS. Bacterial delivery of Staphylococcus aureus alpha-hemolysin causes regression and necrosis in murine tumors. Mol Ther. 2014;22:1266-74.
102. Swofford CA, St Jean AT, Panteli JT, Brentzel ZJ, Forbes NS. Identification of Staphylococcus aureus alpha-hemolysin as a protein drug that is secreted by anticancer bacteria and rapidly kills cancer cells. Biotechnology and bioengineering. 2014;111:1233-45.
103. Nguyen VH, Kim HS, Ha JM, Hong Y, Choy HE, Min JJ. Genetically engineered Salmonella typhimurium as an imageable therapeutic probe for cancer. Cancer Res. 2010;70:18-23.
104. Essmann F, Bantel H, Totzke G, Engels IH, Sinha B, Schulze-Osthoff K, Janicke RU. Staphylococcus aureus alpha-toxin-induced cell death: predominant necrosis despite apoptotic caspase activation. Cell Death Differ. 2003;10:1260-72.
105. Gouaux E. alpha-hemolysin from Staphylococcus aureus: An archetype of beta-barrel, channel-forming toxins. Journal of Structural Biology. 1998;121:110-22.
106. Song LZ, Hobaugh MR, Shustak C, Cheley S, Bayley H, Gouaux JE. Structure of staphylococcal alpha-hemolysin, a heptameric transmembrane pore. Science. 1996;274:1859-66.
107. Menestrina G, Dalla Serra M, Comai M, Coraiola M, Viero G, Werner S, Colin DA, Monteil H, Prevost G. Ion channels and bacterial infection: the case of beta-barrel pore-forming protein toxins of Staphylococcus aureus. FEBS Lett. 2003;552:54-60.
108. Loeffler M, Le'Negrate G, Krajewska M, Reed JC. Inhibition of tumor growth using salmonella expressing Fas ligand. J Natl Cancer Inst. 2008;100:1113-6.
109. Theys J, Nuyts S, Landuyt W, Van Mellaert L, Dillen C, Bohringer M, Durre P, Lambin P, Anne J. Stable Escherichia coli-Clostridium acetobutylicum shuttle vector for secretion of murine tumor necrosis factor alpha. Applied and Environmental Microbiology. 1999;65:4295-300.
110. Nuyts S, Theys J, Landuyt W, van Mellaert L, Lambin P, Anne J. Increasing specificity of anti-tumor therapy: cytotoxic protein delivery by non-pathogenic clostridia under regulation of radio-induced promoters. Anticancer Res. 2001;21:857-61.
111. Nuyts S, Van Mellaert L, Theys J, Landuyt W, Bosmans E, Anne J, Lambin P. Radio-responsive recA promoter significantly increases TNFalpha production in recombinant clostridia after 2 Gy irradiation. Gene Ther. 2001;8:1197-201.
112. Walczak H, Miller RE, Ariail K, Gliniak B, Griffith TS, Kubin M, Chin W, Jones J, Woodward A, Le T, et al. Tumoricidal activity of tumor necrosis factor-related apoptosis-inducing ligand in vivo. Nat Med. 1999;5:157-63.
113. Quispe-Tintaya W, Chandra D, Jahangir A, Harris M, Casadevall A, Dadachova E, Gravekamp C. Nontoxic radioactive Listeria(at) is a highly effective therapy against metastatic pancreatic cancer. Proc Natl Acad Sci U S A. 2013;110:8668-73.
114. Chandra D, Selvanesan BC, Yuan Z, Libutti SK, Koba W, Beck A, Zhu K, Casadevall A, Dadachova E, Gravekamp C. 32-Phosphorus selectively delivered by listeria to pancreatic cancer demonstrates a strong therapeutic effect. Oncotarget. 2017;8:20729-40.
115. Xiang S, Fruehauf J, Li CJ. Short hairpin RNA-expressing bacteria elicit RNA interference in mammals. Nat Biotechnol. 2006;24:697-702.
116. Kanai R, Rabkin SD, Yip S, Sgubin D, Zaupa CM, Hirose Y, Louis DN, Wakimoto H, Martuza RL. Oncolytic virus-mediated manipulation of DNA damage responses: synergy with chemotherapy in killing glioblastoma stem cells. J Natl Cancer Inst. 2012;104:42-55.
117. Waters AM, Johnston JM, Reddy AT, Fiveash J, Madan-Swain A, Kachurak K, Bag AK, Gillespie GY, Markert JM, Friedman GK. Rationale and Design of a Phase 1 Clinical Trial to Evaluate HSV G207 Alone or with a Single Radiation Dose in Children with Progressive or Recurrent Malignant Supratentorial Brain Tumors. Hum Gene Ther Clin Dev. 2017;28:7-16.
118. Heimberger AB, Sun W, Hussain SF, Dey M, Crutcher L, Aldape K, Gilbert M, Hassenbusch SJ, Sawaya R, Schmittling B, et al. Immunological responses in a patient with glioblastoma multiforme treated with sequential courses of temozolomide and immunotherapy: case study. Neuro Oncol. 2008;10:98-103.
119. Roulstone V, Khan K, Pandha HS, Rudman S, Coffey M, Gill GM, Melcher AA, Vile R, Harrington KJ, de Bono J, Spicer J. Phase I trial of cyclophosphamide as an immune modulator for optimizing oncolytic reovirus delivery to solid tumors. Clin Cancer Res. 2015;21:1305-12.
120. Durham NM, Mulgrew K, McGlinchey K, Monks NR, Ji H, Herbst R, Suzich J, Hammond SA, Kelly EJ. Oncolytic VSV Primes Differential Responses to Immuno-oncology Therapy. Mol Ther. 2017;25:1917-32.
121. Moesta AK, Cooke K, Piasecki J, Mitchell P, Rottman JB, Fitzgerald K, Zhan J, Yang B, Le T, Belmontes B, et al. Local Delivery of OncoVEX(mGM-CSF) Generates Systemic Antitumor Immune Responses Enhanced by Cytotoxic T-Lymphocyte-Associated Protein Blockade. Clin Cancer Res. 2017;23:6190-202.
122. Rajani K, Parrish C, Kottke T, Thompson J, Zaidi S, Ilett L, Shim KG, Diaz RM, Pandha H, Harrington K, et al. Combination Therapy With Reovirus and Anti-PD-1 Blockade Controls Tumor Growth Through Innate and Adaptive Immune Responses. Mol Ther. 2016;24:166-74.
123. Woller N, Gurlevik E, Fleischmann-Mundt B, Schumacher A, Knocke S, Kloos AM, Saborowski M, Geffers R, Manns MP, Wirth TC, et al. Viral Infection of Tumors Overcomes Resistance to PD-1-immunotherapy by Broadening Neoantigenome-directed T-cell Responses. Mol Ther. 2015;23:1630-40.
124. Zamarin D, Wolchok JD. Potentiation of immunomodulatory antibody therapy with oncolytic viruses for treatment of cancer. Mol Ther Oncolytics. 2014;1:14004.
125. Chesney J, Puzanov I, Collichio F, Singh P, Milhem MM, Glaspy J, Hamid O, Ross M, Friedlander P, Garbe C, et al. Randomized, Open-Label Phase II Study Evaluating the Efficacy and Safety of Talimogene Laherparepvec in Combination With Ipilimumab Versus Ipilimumab Alone in Patients With Advanced, Unresectable Melanoma. J Clin Oncol. 2018;36:1658.
126. Ribas A, Dummer R, Puzanov I, VanderWalde A, Andtbacka RHI, Michielin O, Olszanski AJ, Malvehy J, Cebon J, Fernandez E, et al. Oncolytic Virotherapy Promotes Intratumoral T Cell Infiltration and Improves Anti-PD-1 Immunotherapy. Cell. 2017;170:1109-19. e1110
127. Nishio N, Diaconu I, Liu H, Cerullo V, Caruana I, Hoyos V, Bouchier-Hayes L, Savoldo B, Dotti G. Armed oncolytic virus enhances immune functions of chimeric antigen receptor-modified T cells in solid tumors. Cancer Res. 2014;74:5195-205.
128. Rosewell Shaw A, Porter CE, Watanabe N, Tanoue K, Sikora A, Gottschalk S, Brenner MK, Suzuki M. Adenovirotherapy Delivering Cytokine and Checkpoint Inhibitor Augments CAR T Cells against Metastatic Head and Neck Cancer. Mol Ther. 2017;25:2440-51.
129. Tanoue K, Rosewell Shaw A, Watanabe N, Porter C, Rana B, Gottschalk S, Brenner M, Suzuki M. Armed Oncolytic Adenovirus-Expressing PD-L1 Mini-Body Enhances Antitumor Effects of Chimeric Antigen Receptor T Cells in Solid Tumors. Cancer Res. 2017;77:2040-51.
130. Lambin P, Theys J, Landuyt W, Rijken P, van der Kogel A, van der Schueren E, Hodgkiss R, Fowler J, Nuyts S, de Bruijn E, et al. Colonisation of Clostridium in the body is restricted to hypoxic and necrotic areas of tumours. Anaerobe. 1998;4:183-8.
131. Westphal K, Leschner S, Jablonska J, Loessner H, Weiss S. Containment of tumor-colonizing bacteria by host neutrophils. Cancer Res. 2008;68:2952-60.
132. Dang LH, Bettegowda C, Agrawal N, Cheong I, Huso D, Frost P, Loganzo F, Greenberger L, Barkoczy J, Pettit GR, et al. Targeting vascular and avascular compartments of tumors with C. novyi-NT and anti-microtubule agents. Cancer Biol Ther. 2004;3:326-37.
133. Bettegowda C, Dang LH, Abrams R, Huso DL, Dillehay L, Cheong I, Agrawal N, Borzillary S, McCaffery JM, Watson EL, et al. Overcoming the hypoxic barrier to radiation therapy with anaerobic bacteria. Proc Natl Acad Sci U S A. 2003;100:15083-8.
134. Hedley D, Ogilvie L, Springer C. Carboxypeptidase-G2-based gene-directed enzyme-prodrug therapy: a new weapon in the GDEPT armoury. Nat Rev Cancer. 2007;7:870-9.
135. Pawelek JM, Low KB, Bermudes D. Tumor-targeted Salmonella as a novel anticancer vector. Cancer Res. 1997;57:4537-44.
136. Stritzker J, Pilgrim S, Szalay AA, Goebel W. Prodrug converting enzyme gene delivery by L. monocytogenes. BMC Cancer. 2008;8:94.
137. Gulley JL, Madan RA, Pachynski R, Mulders P, Sheikh NA, Trager J, Drake CG. Role of Antigen Spread and Distinctive Characteristics of Immunotherapy in Cancer Treatment. J Natl Cancer Inst. 2017;109
138. Hodge JW, Sabzevari H, Yafal AG, Gritz L, Lorenz MG, Schlom J. A triad of costimulatory molecules synergize to amplify T-cell activation. Cancer Res. 1999;59:5800-7.
139. Madan RA, Arlen PM, Mohebtash M, Hodge JW, Gulley JL. Prostvac-VF: a vector-based vaccine targeting PSA in prostate cancer. Expert Opin Investig Drugs. 2009;18:1001-11.
140. Bazett M, Costa AM, Bosiljcic M, Anderson RM, Alexander MP, Wong SWY, Dhanji S, Chen JM, Pankovich J, Lam S, et al. Harnessing innate lung anti-cancer effector functions with a novel bacterial-derived immunotherapy. Oncoimmunology. 2018;7:e1398875.
141. You YN, Lakhani VT, Wells SA Jr. The role of prophylactic surgery in cancer prevention. World J Surg. 2007;31:450-64.
142. Bhatt AP, Redinbo MR, Bultman SJ. The role of the microbiome in cancer development and therapy. CA Cancer J Clin. 2017;67:326-44.
143. Frazer IH, Quinn M, Nicklin JL, Tan J, Perrin LC, Ng P, O'Connor VM, White O, Wendt N, Martin J, et al. Phase 1 study of HPV16-specific immunotherapy with E6E7 fusion protein and ISCOMATRIX adjuvant in women with cervical intraepithelial neoplasia. Vaccine. 2004;23:172-81.
144. Schiller JT, Lowy DR. Prospects for cervical cancer prevention by human papillomavirus vaccination. Cancer Res. 2006;66:10229-32.
145. Hilleman MR, Buynak EB, Roehm RR, Tytell AA, Bertland AU, Lampson GP. Purified and inactivated human hepatitis B vaccine: progress report. Am J Med Sci. 1975;270:401-4.
146. Gatti-Mays ME, Redman JM, Collins JM, Bilusic M. Cancer vaccines: Enhanced immunogenic modulation through therapeutic combinations. Hum Vaccin Immunother. 2017;13:2561-74.
147. Kaur B, Chiocca EA, Cripe TP. Oncolytic HSV-1 virotherapy: clinical experience and opportunities for progress. Curr Pharm Biotechnol. 2012;13:1842-51.
148. Bell J, McFadden G. Viruses for tumor therapy. Cell Host Microbe. 2014;15:260-5.
149. Cunningham C, Nemunaitis J. A phase I trial of genetically modified Salmonella typhimurium expressing cytosine deaminase (TAPET-CD, VNP20029) administered by intratumoral injection in combination with 5-fluorocytosine for patients with advanced or metastatic cancer. Protocol no: CL-017. Version: April 9, 2001. Hum Gene Ther. 2001;12:1594-6.
150. Toso JF, Gill VJ, Hwu P, Marincola FM, Restifo NP, Schwartzentruber DJ, Sherry RM, Topalian SL, Yang JC, Stock F, et al. Phase I study of the intravenous administration of attenuated Salmonella typhimurium to patients with metastatic melanoma. J Clin Oncol. 2002;20:142-52.
151. Heimann DM, Rosenberg SA. Continuous intravenous administration of live genetically modified salmonella typhimurium in patients with metastatic melanoma. J Immunother. 2003;26:179-80.
152. Nemunaitis J, Cunningham C, Senzer N, Kuhn J, Cramm J, Litz C, Cavagnolo R, Cahill A, Clairmont C, Sznol M. Pilot trial of genetically modified, attenuated Salmonella expressing the E. coli cytosine deaminase gene in refractory cancer patients. Cancer Gene Ther. 2003;10:737-44.
153. Fritz SE, Henson MS, Greengard E, Winter AL, Stuebner KM, Yoon U, Wilk VL, Borgatti A, Augustin LB, Modiano JF, Saltzman DA. A phase I clinical study to evaluate safety of orally administered, genetically engineered Salmonella enterica serovar Typhimurium for canine osteosarcoma. Vet Med Sci. 2016;2:179-90.
154. Krick EL, Sorenmo KU, Rankin SC, Cheong I, Kobrin B, Thornton K, Kinzler KW, Vogelstein B, Zhou S, Diaz LA Jr. Evaluation of Clostridium novyi-NT spores in dogs with naturally occurring tumors. Am J Vet Res. 2012;73:112-8.
155. Kashiwagi N, Nakanishi K, Kozuka T, Sato Y, Tanaka K, Tsukaguchi I, Uemura H, Fujii T, Yoshino K, Tomiyama N. Vascular supply with angio-CT for superselective intra-arterial chemotherapy in advanced maxillary sinus cancer. Br J Radiol. 2010;83:171-8.
156. Egeland TA, Gaustad JV, Galappathi K, Rofstad EK. Magnetic resonance imaging of tumor necrosis. Acta Oncol. 2011;50:427-34.
157. Fleming IN, Manavaki R, Blower PJ, West C, Williams KJ, Harris AL, Domarkas J, Lord S, Baldry C, Gilbert FJ. Imaging tumour hypoxia with positron emission tomography. Br J Cancer. 2015;112:238-50.
158. Tumeh PC, Harview CL, Yearley JH, Shintaku IP, Taylor EJ, Robert L, Chmielowski B, Spasic M, Henry G, Ciobanu V, et al. PD-1 blockade induces responses by inhibiting adaptive immune resistance. Nature. 2014;515:568-71.
159. Margolis SR, Wilson SC, Vance RE. Evolutionary Origins of cGAS-STING Signaling. Trends Immunol. 2017;38:733-43.
160. Hildner K, Edelson BT, Purtha WE, Diamond M, Matsushita H, Kohyama M, Calderon B, Schraml BU, Unanue ER, Diamond MS, et al. Batf3 deficiency reveals a critical role for CD8alpha+ dendritic cells in cytotoxic T cell immunity. Science. 2008;322:1097-100.
161. Ginhoux F, Liu K, Helft J, Bogunovic M, Greter M, Hashimoto D, Price J, Yin N, Bromberg J, Lira SA, et al. The origin and development of nonlymphoid tissue CD103+ DCs. J Exp Med. 2009;206:3115-30.
162. Zhang Y, Chen G, Liu Z, Tian S, Zhang J, Carey CD, Murphy KM, Storkus WJ, Falo LD Jr, You Z. Genetic Vaccines To Potentiate the Effective CD103+ Dendritic Cell-Mediated Cross-Priming of Antitumor Immunity. J Immunol. 2015;194:5937-47.
163. Callahan MK, Wolchok JD. At the bedside: CTLA-4- and PD-1-blocking antibodies in cancer immunotherapy. J Leukoc Biol. 2013;94:41-53.
164. Zhou S, Bettegowda C, Agrawal N. Combination bacteriolytic cancer therapy: Attacking cancer from inside out. Discov Med. 2004;4:33-7.
165. Minton NP. Clostridia in cancer therapy. Nature Reviews Microbiology. 2003;1:237-42.
166. Leschner S, Westphal K, Dietrich N, Viegas N, Jablonska J, Lyszkiewicz M, Lienenklaus S, Falk W, Gekara N, Loessner H, Weiss S. Tumor invasion of Salmonella enterica serovar Typhimurium is accompanied by strong hemorrhage promoted by TNF-alpha. PloS one. 2009;4:e6692.
167. Forbes NS, Munn LL, Fukumura D, Jain RK. Sparse initial entrapment of systemically injected Salmonella typhimurium leads to heterogeneous accumulation within tumors. Cancer Res. 2003;63:5188-93.
168. Kasinskas RW, Forbes NS. Salmonella typhimurium specifically chemotax and proliferate in heterogeneous tumor tissue in vitro. Biotechnology and Bioengineering. 2006;94:710-21.
169. Chandra D, Jahangir A, Quispe-Tintaya W, Einstein MH, Gravekamp C. Myeloid-derived suppressor cells have a central role in attenuated Listeria monocytogenes-based immunotherapy against metastatic breast cancer in young and old mice. British journal of cancer. 2013;108:2281-90.
170. Chandra D, Gravekamp C. Myeloid-derived suppressor cells: Cellular missiles to target tumors. Oncoimmunology. 2013;2:e26967.
171. Ostrand-Rosenberg S, Sinha P. Myeloid-derived suppressor cells: linking inflammation and cancer. Journal of immunology. 2009;182:4499-506.
172. Hiratsuka S, Watanabe A, Aburatani H, Maru Y. Tumour-mediated upregulation of chemoattractants and recruitment of myeloid cells predetermines lung metastasis. Nature cell biology. 2006;8:1369-75.
173. Tilney LG, Portnoy DA. Actin filaments and the growth, movement, and spread of the intracellular bacterial parasite, Listeria monocytogenes. J Cell Biol. 1989;109:1597-608.
174. Sznol M, Lin SL, Bermudes D, Zheng LM, King I. Use of preferentially replicating bacteria for the treatment of cancer. J Clin Invest. 2000;105:1027-30.
175. Thorne SH. Strategies to achieve systemic delivery of therapeutic cells and microbes to tumors. Expert Opin Biol Ther. 2007;7:41-51.
176. Kueberuwa G, Cawood R, Seymour LW. Blood compatibility of enveloped viruses. Current opinion in molecular therapeutics. 2010;12:412-20.
177. Fountzilas C, Patel S, Mahalingam D. Review: Oncolytic virotherapy, updates and future directions. Oncotarget. 2017;8:102617-39.
178. Morrison J, Briggs SS, Green N, Fisher K, Subr V, Ulbrich K, Kehoe S, Seymour LW. Virotherapy of ovarian cancer with polymer-cloaked adenovirus retargeted to the epidermal growth factor receptor. Mol Ther. 2008;16:244-51.
179. Kwon OJ, Kang E, Choi JW, Kim SW, Yun CO. Therapeutic targeting of chitosan-PEG-folate-complexed oncolytic adenovirus for active and systemic cancer gene therapy. J Control Release. 2013;169:257-65.
180. Tian J, Xu Z, Smith JS, Hofherr SE, Barry MA, Byrnes AP. Adenovirus activates complement by distinctly different mechanisms in vitro and in vivo: indirect complement activation by virions in vivo. J Virol. 2009;83:5648-58.
181. Carlisle R, Choi J, Bazan-Peregrino M, Laga R, Subr V, Kostka L, Ulbrich K, Coussios CC, Seymour LW. Enhanced tumor uptake and penetration of virotherapy using polymer stealthing and focused ultrasound. J Natl Cancer Inst. 2013;105:1701-10.
182. Zhang X, Huang Y, Ghazwani M, Zhang P, Li J, Thorne SH, Li S. Tunable pH-responsive polymeric micelle for cancer treatment. ACS Macro Letters. 2015;4:620-3.
183. Fisher KD, Stallwood Y, Green NK, Ulbrich K, Mautner V, Seymour LW. Polymer-coated adenovirus permits efficient retargeting and evades neutralising antibodies. Gene Ther. 2001;8:341-8.
184. Evgin L, Acuna SA, Tanese de Souza C, Marguerie M, Lemay CG, Ilkow CS, Findlay CS, Falls T, Parato KA, Hanwell D, et al. Complement inhibition prevents oncolytic vaccinia virus neutralization in immune humans and cynomolgus macaques. Mol Ther. 2015;23:1066-76.
185. Ilett E, Kottke T, Donnelly O, Thompson J, Willmon C, Diaz R, Zaidi S, Coffey M, Selby P, Harrington K, et al. Cytokine conditioning enhances systemic delivery and therapy of an oncolytic virus. Mol Ther. 2014;22:1851-63.
186. Rojas JJ, Sampath P, Bonilla B, Ashley A, Hou W, Byrd D, Thorne SH. Manipulating TLR Signaling Increases the Anti-tumor T Cell Response Induced by Viral Cancer Therapies. Cell Rep. 2016;15:264-73.
187. Kuhn I, Harden P, Bauzon M, Chartier C, Nye J, Thorne S, Reid T, Ni S, Lieber A, Fisher K, et al. Directed evolution generates a novel oncolytic virus for the treatment of colon cancer. PLoS One. 2008;3:e2409.
188. Thorne SH, Contag CH. Integrating the biological characteristics of oncolytic viruses and immune cells can optimize therapeutic benefits of cell-based delivery. Gene Ther. 2008;15(10):753-8.
189. Adair RA, Roulstone V, Scott KJ, Morgan R, Nuovo GJ, Fuller M, Beirne D, West EJ, Jennings VA, Rose A, et al. Cell carriage, delivery, and selective replication of an oncolytic virus in tumor in patients. Sci Transl Med. 2012;4:138ra177.
190. Carey RW, Holland JF, Whang HY, Neter E, Bryant B. Clostridial oncolysis in man. Europ J Cancer. 1967;3:37-46.
191. Bourquin C, von der Borch P, Zoglmeier C, Anz D, Sandholzer N, Suhartha N, Wurzenberger C, Denzel A, Kammerer R, Zimmermann W, Endres S. Efficient eradication of subcutaneous but not of autochthonous gastric tumors by adoptive T cell transfer in an SV40 T antigen mouse model. J Immunol. 2010;185:2580-8.
192. Kersten K, de Visser KE, van Miltenburg MH, Jonkers J. Genetically engineered mouse models in oncology research and cancer medicine. EMBO Mol Med. 2017;9:137-53.
193. Walrath JC, Hawes JJ, Van Dyke T, Reilly KM. Genetically engineered mouse models in cancer research. Adv Cancer Res. 2010;106:113-64.
194. Gengenbacher N, Singhal M, Augustin HG. Preclinical mouse solid tumour models: status quo, challenges and perspectives. Nat Rev Cancer. 2017;17:751-65.
195. Tschida BR, Largaespada DA, Keng VW. Mouse models of cancer: Sleeping Beauty transposons for insertional mutagenesis screens and reverse genetic studies. Semin Cell Dev Biol. 2014;27:86-95.
196. Tsoneva D, Minev B, Frentzen A, Zhang Q, Wege AK, Szalay AA. Humanized Mice with Subcutaneous Human Solid Tumors for Immune Response Analysis of Vaccinia Virus-Mediated Oncolysis. Mol Ther Oncolytics. 2017;5:41-61.
197. LeBlanc AK, Naik S, Galyon GD, Jenks N, Steele M, Peng KW, Federspiel MJ, Donnell R, Russell SJ. Safety studies on intravenous administration of oncolytic recombinant vesicular stomatitis virus in purpose-bred beagle dogs. Hum Gene Ther Clin Dev. 2013;24:174-81.
198. Hwang CC, Igase M, Sakurai M, Haraguchi T, Tani K, Itamoto K, Shimokawa T, Nakaichi M, Nemoto Y, Noguchi S, et al. Oncolytic reovirus therapy: Pilot study in dogs with spontaneously occurring tumours. Vet Comp Oncol. 2018;16:229-38.
199. Atherton MJ, Morris JS, McDermott MR, Lichty BD. Cancer immunology and canine malignant melanoma: A comparative review. Vet Immunol Immunopathol. 2016;169:15-26.
200. Panjwani MK, Smith JB, Schutsky K, Gnanandarajah J, O'Connor CM, Powell DJ Jr, Mason NJ. Feasibility and Safety of RNA-transfected CD20-specific Chimeric Antigen Receptor T Cells in Dogs with Spontaneous B Cell Lymphoma. Mol Ther. 2016;24:1602-14.
201. Pluhar GE, Grogan PT, Seiler C, Goulart M, Santacruz KS, Carlson C, Chen W, Olin MR, Lowenstein PR, Castro MG, et al. Anti-tumor immune response correlates with neurological symptoms in a dog with spontaneous astrocytoma treated by gene and vaccine therapy. Vaccine. 2010;28:3371-8.
202. Regan D, Guth A, Coy J, Dow S. Cancer immunotherapy in veterinary medicine: Current options and new developments. Vet J. 2016;207:20-8.
203. Anderson KL, Modiano JF. Progress in Adaptive Immunotherapy for Cancer in Companion Animals: Success on the Path to a Cure. Vet Sci. 2015;2:363-87.
204. Park JS, Withers SS, Modiano JF, Kent MS, Chen M, Luna JI, Culp WTN, Sparger EE, Rebhun RB, Monjazeb AM, et al. Canine cancer immunotherapy studies: linking mouse and human. J Immunother Cancer. 2016;4:97.
205. Sivan A, Corrales L, Hubert N, Williams JB, Aquino-Michaels K, Earley ZM, Benyamin FW, Lei YM, Jabri B, Alegre ML, et al. Commensal Bifidobacterium promotes antitumor immunity and facilitates anti-PD-L1 efficacy. Science. 2015;350:1084-9.
206. Song SJ, Lauber C, Costello EK, Lozupone CA, Humphrey G, Berg-Lyons D, Caporaso JG, Knights D, Clemente JC, Nakielny S, et al. Cohabiting family members share microbiota with one another and with their dogs. Elife. 2013;2:e00458.
207. Vetizou M, Pitt JM, Daillere R, Lepage P, Waldschmitt N, Flament C, Rusakiewicz S, Routy B, Roberti MP, Duong CP, et al. Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota. Science. 2015;350:1079-84.
208. Dunn GP, Old LJ, Schreiber RD. The immunobiology of cancer immunosurveillance and immunoediting. Immunity. 2004;21:137-48.
209. US FDA: Recommendations for Microbial Vectors used for Gene Therapy - Guidance for Industry (2016) [ https://www.fda.gov/downloads/biologicsbloodvaccines/guidancecomplianceregulatoryinformation/guidances/cellularandgenetherapy/ucm466625.pdf ]. Accessed 15 July 2018.
210. Cellular, Tissue and Gene Therapies & Oncologic Drug Advisory Committee Meeting: Talimogene Laherparepvec [ https://www.fda.gov/downloads/biologicsbloodvaccines/guidancecomplianceregulatoryinformation/guidances/cellularandgenetherapy/ucm404087.pdf ]. Accessed 15 July 2018.
211. Hu JC, Coffin RS, Davis CJ, Graham NJ, Groves N, Guest PJ, Harrington KJ, James ND, Love CA, McNeish I, et al. A phase I study of OncoVEXGM-CSF, a second-generation oncolytic herpes simplex virus expressing granulocyte macrophage colony-stimulating factor. Clin Cancer Res. 2006;12:6737-47.
212. Harrington KJ, Hingorani M, Tanay MA, Hickey J, Bhide SA, Clarke PM, Renouf LC, Thway K, Sibtain A, McNeish IA, et al. Phase I/II study of oncolytic HSV GM-CSF in combination with radiotherapy and cisplatin in untreated stage III/IV squamous cell cancer of the head and neck. Clin Cancer Res. 2010;16:4005-15.
213. Senzer NN, Kaufman HL, Amatruda T, Nemunaitis M, Reid T, Daniels G, Gonzalez R, Glaspy J, Whitman E, Harrington K, et al. Phase II clinical trial of a granulocyte-macrophage colony-stimulating factor-encoding, second-generation oncolytic herpesvirus in patients with unresectable metastatic melanoma. J Clin Oncol. 2009;27:5763-71.
214. Geletneky K, Hajda J, Angelova AL, Leuchs B, Capper D, Bartsch AJ, Neumann JO, Schoning T, Husing J, Beelte B, et al. Oncolytic H-1 Parvovirus Shows Safety and Signs of Immunogenic Activity in a First Phase I/IIa Glioblastoma Trial. Mol Ther. 2017;25:2620-34.
215. Angelova AL, Barf M, Geletneky K, Unterberg A, Rommelaere J. Immunotherapeutic Potential of Oncolytic H-1 Parvovirus: Hints of Glioblastoma Microenvironment Conversion towards Immunogenicity. Viruses. 2017;9:12.
216. Hajda J, Lehmann M, Krebs O, Kieser M, Geletneky K, Jager D, Dahm M, Huber B, Schoning T, Sedlaczek O, et al. A non-controlled, single arm, open label, phase II study of intravenous and intratumoral administration of ParvOryx in patients with metastatic, inoperable pancreatic cancer: ParvOryx02 protocol. BMC Cancer. 2017;17:576.
217. Leuchs B, Frehtman V, Riese M, Muller M, Rommelaere J. A novel scalable, robust downstream process for oncolytic rat parvovirus: isoelectric point-based elimination of empty particles. Appl Microbiol Biotechnol. 2017;101:3143-52.
218. Leuchs B, Roscher M, Muller M, Kurschner K, Rommelaere J. Standardized large-scale H-1PV production process with efficient quality and quantity monitoring. J Virol Methods. 2016;229:48-59.
219. Ungerechts G, Bossow S, Leuchs B, Holm PS, Rommelaere J, Coffey M, Coffin R, Bell J, Nettelbeck DM. Moving oncolytic viruses into the clinic: clinical-grade production, purification, and characterization of diverse oncolytic viruses. Mol Ther Methods Clin Dev. 2016;3:16018.
220. Angelova AL, Geletneky K, Nuesch JP, Rommelaere J. Tumor Selectivity of Oncolytic Parvoviruses: From in vitro and Animal Models to Cancer Patients. Front Bioeng Biotechnol. 2015;3:55.
221. Marchini A, Bonifati S, Scott EM, Angelova AL, Rommelaere J. Oncolytic parvoviruses: from basic virology to clinical applications. Virol J. 2015;12:6.
222. Marr M, D'Abramo A, Pittman N, Agbandje-McKenna M, Cotmore SF, Tattersall P. Optimizing the Targeting of Mouse Parvovirus 1 to Murine Melanoma Selects for Recombinant Genomes and Novel Mutations in the Viral Capsid Gene. Viruses. 2018;10
223. Kim SH, Castro F, Paterson Y, Gravekamp C. High Efficacy of a Listeria-Based Vaccine against Metastatic Breast Cancer Reveals a Dual Mode of Action. Cancer Research. 2009;69:5860-6.
224. Kono K, Mimura K, Kiessling R. Immunogenic tumor cell death induced by chemoradiotherapy: molecular mechanisms and a clinical translation. Cell death & disease. 2013;4:e688.
225. Singh M, Quispe-Tintaya W, Chandra D, Jahangir A, Venkataswamy MM, Ng TW, Sharma-Kharkwal S, Carreno LJ, Porcelli SA, Gravekamp C. Direct incorporation of the NKT-cell activator alpha-galactosylceramide into a recombinant Listeria monocytogenes improves breast cancer vaccine efficacy. Br J Cancer. 2014;111:1945-54.
226. Shahabi V, Seavey MM, Maciag PC, Rivera S, Wallecha A. Development of a live and highly attenuated Listeria monocytogenes-based vaccine for the treatment of Her2/neu-overexpressing cancers in human. Cancer Gene Ther. 2011;18:53-62.
227. Staedtke V, Bai RY, Sun W, Huang J, Kibler KK, Tyler BM, Gallia GL, Kinzler K, Vogelstein B, Zhou S, Riggins GJ. Clostridium novyi-NT can cause regression of orthotopically implanted glioblastomas in rats. Oncotarget. 2015;6:5536-46.