Virulence-attenuated Salmonella engineered to secrete immunomodulators reduce tumour growth and increase survival in an autochthonous mouse model of breast cancer

References

• Kennedy LB, Salama AKS. A review of cancer immunotherapy toxicity. CA Cancer J Clin. 2020;70(2):86–104.
   PubMed Web of Science ®Google Scholar
• Nguyen KB, Spranger S. Modulation of the immune microenvironment by tumor-intrinsic oncogenic signaling. J Cell Biol. 2020;219(1):e201908224.
   PubMed Web of Science ®Google Scholar
• Alizadeh S, Esmaeili A, Barzegari A, et al. Bioengineered smart bacterial carriers for combinational targeted therapy of solid tumours. J Drug Target. 2020;28(7-8):700–713.
   PubMed Web of Science ®Google Scholar
• Sawant SS, Patil SM, Gupta V, et al. Microbes as medicines: harnessing the power of bacteria in advancing cancer treatment. Int J Mol Sci. 2020;21(20):7575.
   Web of Science ®Google Scholar
• Cao Z, Liu J. Bacteria and bacterial derivatives as drug carriers for cancer therapy. J Control Release. 2020;326:396–407.
   PubMed Web of Science ®Google Scholar
• Dróżdż M, Makuch S, Cieniuch G, et al. Obligate and facultative anaerobic bacteria in targeted cancer therapy: current strategies and clinical applications. Life Sci. 2020;261:118296.
   PubMed Web of Science ®Google Scholar
• Liang K, Liu Q, Kong Q. New technologies in developing recombinant attenuated bacteria for cancer therapy. Biotechnol Bioeng. 2020;1–18. doi:10.1002/bit.27596
   Web of Science ®Google Scholar
• Augustin LB, Milbauer L, Hastings SE, et al. Salmonella enterica Typhimurium engineered for nontoxic systemic colonization of autochthonous tumors. J Drug Target. 2020;10:1–6.
   Google Scholar
• Mortier E, Quemener A, Vusio P, et al. Soluble interleukin-15 receptor alpha (IL-15R alpha)-sushi as a selective and potent agonist of IL-15 action through IL-15R beta/gamma. Hyperagonist IL-15 x IL-15R alpha fusion proteins [Research Support, Non-U.S. J Biol Chem. 2006;281(3):1612–1619.
   PubMed Web of Science ®Google Scholar
• Guo Y, Luan L, Rabacal W, et al. IL-15 superagonist-mediated immunotoxicity: role of NK cells and IFN-γ. J Immunol. 2015;195(5):2353–2364.
   PubMed Web of Science ®Google Scholar
• Martins F, Sofiya L, Sykiotis GP, et al. Adverse effects of immune-checkpoint inhibitors: epidemiology, management and surveillance. Nat Rev Clin Oncol. 2019;16(9):563–580.
   PubMed Web of Science ®Google Scholar
• Drees JJ, Mertensotto MJ, Augustin LB, et al. Vasculature disruption enhances bacterial targeting of autochthonous tumors. J Cancer. 2015;6(9):843–848.
   PubMed Web of Science ®Google Scholar
• Solinas M, Massi P, Cantelmo AR, et al. Cannabidiol inhibits angiogenesis by multiple mechanisms. Br J Pharmacol. 2012;167(6):1218–1231.
   PubMed Web of Science ®Google Scholar
• Atalay S, Jarocka-Karpowicz I, Skrzydlewska E. Antioxidative and anti-inflammatory properties of cannabidiol. Antioxidants (Basel). 2019;9(1):21.
   PubMedGoogle Scholar
• Galan JE, Nakayama K, Curtiss R. 3rd. Cloning and characterization of the asd gene of Salmonella typhimurium: use in stable maintenance of recombinant plasmids in Salmonella vaccine strains. Gene. 1990;94(1):29–35.
   PubMed Web of Science ®Google Scholar
• Ryan RM, Green J, Williams PJ, et al. Bacterial delivery of a novel cytolysin to hypoxic areas of solid tumors [Evaluation Studies Research Support, Non-U.S]. Gene Ther. 2009;16(3):329–339.
   PubMed Web of Science ®Google Scholar
• Hess J, Gentschev I, Goebel W, et al. Analysis of the haemolysin secretion system by PhoA-HlyA fusion proteins. Mol Gen Genet. 1990;224(2):201–208.
   PubMedGoogle Scholar
• Finlay WJ, Bloom L, Cunningham O. Optimized generation of high-affinity, high-specificity single-chain Fv antibodies from multiantigen immunized chickens. Methods Mol Biol. 2011;681:383–401.
   PubMedGoogle Scholar
• Drees JJ, Augustin LB, Mertensotto MJ, et al. Soluble production of a biologically active single-chain antibody against murine PD-L1 in Escherichia coli. Protein Expr Purif. 2014;94:60–66.
   PubMed Web of Science ®Google Scholar
• Osorio M, Wu Y, Singh S, et al. Anthrax protective antigen delivered by Salmonella enterica serovar Typhi Ty21a protects mice from a lethal anthrax spore challenge [Research Support, N.I.H., Extramural Research Support, U.S. Gov't, P.H.S. Infect Immun. 2009;77(4):1475–1482.
   PubMed Web of Science ®Google Scholar
• Gilbert W. Starting and stopping sequences for the RNA polymerase. In: Losick R, Chamberlin M, editors. RNA Polymerase. Vol. 6. Cold Spring Harbor (NY): Cold Spring Harbor Laboratory Press; 1976. p. 193–205.
   Google Scholar
• Brosius J, Erfle M, Storella J. Spacing of the -10 and -35 regions in the tac promoter. Effect on its in vivo activity. J Biol Chem. 1985;260(6):3539–3541.
   PubMed Web of Science ®Google Scholar
• Drees J, Mertensotto M, Liu G, et al. Attenuated Salmonella enterica Typhimurium reduces tumor burden in an autochthonous breast cancer model. Anticancer Res. 2015;35(2):843–849.
   PubMed Web of Science ®Google Scholar
• Augustin L, Milbauer L, Hastings S, et al. Salmonella enterica Typhimurium engineered for nontoxic systemic colonization of autochthonous tumors. Manuscript submitted for publication. 2020.
   Google Scholar
• Gutierrez C, McEvoy C, Munshi L, et al. critical care management of toxicities associated with targeted agents and immunotherapies for cancer. Crit Care Med. 2020;48(1):10–21.
   PubMed Web of Science ®Google Scholar
• Oh DY, Kim TM, Han SW, et al. Phase I study of CKD-516, a novel vascular disrupting agent, in patients with advanced solid tumors. Cancer Res Treat. 2016;48(1):28–36.
   PubMed Web of Science ®Google Scholar
• Tome Y, Zhang Y, Momiyama M, et al. Primer dosing of S. typhimurium A1-R potentiates tumor-targeting and efficacy in immunocompetent mice. Anticancer Res. 2013;33(1):97–102.
   PubMed Web of Science ®Google Scholar
• Siemann DW, Chaplin DJ, Horsman MR. Realizing the potential of vascular targeted therapy: the rationale for combining vascular disrupting agents and anti-angiogenic agents to treat Cancer. Cancer Invest. 2017;35(8):519–534.
   PubMed Web of Science ®Google Scholar
• Bergamaschi MM, Queiroz RH, Zuardi AW, et al. Safety and side effects of cannabidiol, a Cannabis sativa constituent. Curr Drug Saf. 2011;6(4):237–249.
   PubMedGoogle Scholar
• Frahm M, Felgner S, Kocijancic D, et al. Efficiency of conditionally attenuated Salmonella enterica serovar Typhimurium in bacterium-mediated tumor therapy. mBio. 2015;6(2):1–11.
   Web of Science ®Google Scholar
• Chapman K, Sewell F, Allais L, et al. A global pharmaceutical company initiative: an evidence-based approach to define the upper limit of body weight loss in short term toxicity studies. Regul Toxicol Pharmacol. 2013;67(1):27–38.
   PubMed Web of Science ®Google Scholar
• Saltzman D, Augustin L, Leonard A, et al. Low dose chemotherapy combined with attenuated Salmonella decreases tumor burden and is less toxic than high dose chemotherapy in an autochthonous murine model of breast cancer. Surgery. 2018;163(3):509–514.
   PubMed Web of Science ®Google Scholar
• Toso JF, Gill VJ, Hwu P, et al. Phase I study of the intravenous administration of attenuated Salmonella typhimurium to patients with metastatic melanoma [Clinical Trial Clinical Trial, Phase I]. J Clin Oncol. 2002;20(1):142–152.
   PubMed Web of Science ®Google Scholar
• Leschner S, Westphal K, Dietrich N, et al. Tumor invasion of Salmonella enterica serovar Typhimurium is accompanied by strong hemorrhage promoted by TNF-alpha [Research Support, Non-U.S. PLoS One. 2009;4(8):e6692.
   PubMed Web of Science ®Google Scholar
• Guerin MV, Finisguerra V, Van den Eynde BJ, et al. Preclinical murine tumor models: a structural and functional perspective. Elife. 2020;9:e50740.
   PubMed Web of Science ®Google Scholar
• Tozer GM, Kanthou C, Baguley BC. Disrupting tumour blood vessels. Nat Rev Cancer. 2005;5(6):423–435.
   PubMed Web of Science ®Google Scholar
• Lee J, Kim SJ, Choi H, et al. Identification of CKD-516: a potent tubulin polymerization inhibitor with marked antitumor activity against murine and human solid tumors. J Med Chem. 2010;53(17):6337–6354.
   PubMed Web of Science ®Google Scholar
• Siemann DW. The unique characteristics of tumor vasculature and preclinical evidence for its selective disruption by Tumor-Vascular Disrupting Agents. Cancer Treat Rev. 2011;37(1):63–74.
   PubMed Web of Science ®Google Scholar
• Kim HK, Kang JW, Park YW, et al. Phase I and pharmacokinetic study of the vascular-disrupting agent CKD-516 (NOV120401) in patients with refractory solid tumors. Pharmacol Res Perspect. 2020;8(2):e00568.
   PubMed Web of Science ®Google Scholar
• Liang W, Ni Y, Chen F. Tumor resistance to vascular disrupting agents: mechanisms, imaging, and solutions. Oncotarget. 2016;7(13):15444–15459.
   PubMedGoogle Scholar
• Millar SA, Stone NL, Yates AS, et al. A systematic review on the pharmacokinetics of cannabidiol in humans. Front Pharmacol. 2018;9:1365.
   PubMed Web of Science ®Google Scholar
• Kovalchuk O, Kovalchuk I. Cannabinoids as anticancer therapeutic agents. Cell Cycle. 2020;19(9):961–989.
   PubMed Web of Science ®Google Scholar
• Zou W. Immunosuppressive networks in the tumour environment and their therapeutic relevance. Nat Rev Cancer. 2005;5(4):263–274.
   PubMed Web of Science ®Google Scholar
• Larkin J, Chiarion-Sileni V, Gonzalez R, et al. Combined Nivolumab and Ipilimumab or Monotherapy in Untreated Melanoma. N Engl J Med. 2015;373(1):23–34.
   PubMed Web of Science ®Google Scholar
• Parayath N, Padmakumar S, Nair SV, et al. Strategies for targeting cancer immunotherapy through modulation of the tumor microenvironment [Article]. Regen Eng Transl Med. 2020;6(1):29–49.
   Web of Science ®Google Scholar
• Marshall HT, Djamgoz MBA. Immuno-oncology: emerging targets and combination therapies. Front Oncol. 2018;8:315.
   PubMed Web of Science ®Google Scholar
• Waldmann TA, Dubois S, Miljkovic MD, et al. IL-15 in the combination immunotherapy of cancer. Front Immunol. 2020;11:868.
   PubMed Web of Science ®Google Scholar
• Schodel F, Kelly SM, Peterson DL, et al. Hybrid hepatitis B virus core-pre-S proteins synthesized in avirulent Salmonella typhimurium and Salmonella typhi for oral vaccination. Infect Immun. 1994;62(5):1669–1676.
   PubMed Web of Science ®Google Scholar
• Curtiss R. 3rd, inventor. University of Washington, St. Louis, MO, assignee. Functional balanced-lethal host-vector systems. United States of America patent 6872547; 2005.
   Google Scholar