Impact of tumoral structure and bacterial species on growth and biodistribution of live bacterial therapeutics in xenografted tumours

References

• Parker RC, Plummer HC, Siebenmann CO, et al. Effect of histolyticus infection and toxin on transplantable mouse tumors. Proc Soc Exp Biol Med. 1947;66(2):461–467.
   PubMed Web of Science ®Google Scholar
• Malmgren RA, Flanigan CC. Localization of the vegetative form of Clostridium tetani in mouse tumors following intravenous spore administration. Cancer Res. 1955;15(7):473–478.
   PubMed Web of Science ®Google Scholar
• Lambin P, Theys J, Landuyt W, et al. Colonisation of clostridium in the body is restricted to hypoxic and necrotic areas of tumours. Anaerobe. 1998;4(4):183–188.
   PubMed Web of Science ®Google Scholar
• Pawelek JM, Low KB, Bermudes D. Tumor-targeted Salmonella as a novel anticancer vector. Cancer Res. 1997;57(20):4537–4544.
   PubMed Web of Science ®Google Scholar
• Yazawa K, Fujimori M, Amano J, et al. Bifidobacterium longum as a delivery system for therapy: selective localization and growth in hypoxic tumors. Cancer Gene Ther. 2000;7(2):269–274.
   PubMed Web of Science ®Google Scholar
• Yazawa K, Fujimori M, Nakamura T, et al. Bifidobacterium longum as a delivery system for gene therapy of chemically induced rat mammary tumors. Breast Cancer Res Treat. 2001;66(2):165–170.
   PubMed Web of Science ®Google Scholar
• Yu YA, Timiryasova T, Zhang Q, et al. Optical imaging: Bacteria, viruses, and mammalian cells encoding light-emitting proteins reveal the locations of primary tumors and metastases in animals. Anal Bioanal Chem. 2003;377(6):964–972.
   PubMed Web of Science ®Google Scholar
• Yu YA, Shabahang S, Timiryasova TM, et al. Visualization of tumors and metastases in live animals with bacteria and vaccinia virus encoding light-emitting proteins. Nat Biotechnol. 2004;22(3):313–320.
   PubMed Web of Science ®Google Scholar
• Mowday AM, Guise CP, Ackerley DF, et al. Advancing clostridia to clinical trial: past lessons and recent progress. Cancers (Basel). 2016;8(7):63.
   PubMed Web of Science ®Google Scholar
• Zhou S, Gravekamp C, Bermudes D, et al. Tumour-targeting bacteria engineered to fight cancer. Nat Rev Cancer. 2018;18(12):727–743.
   PubMed Web of Science ®Google Scholar
• Dang LH, Bettegowda C, Huso DL, et al. Combination bacteriolytic therapy for the treatment of experimental tumors. Proc Natl Acad Sci U S A. 2001;98(26):15155–15160.
   PubMed Web of Science ®Google Scholar
• Clairmont C, Lee KC, Pike 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(6):1996–2002.
   PubMed Web of Science ®Google Scholar
• Kim SH, Castro F, Gonzalez D, et al. Mage-b vaccine delivered by recombinant Listeria monocytogenes is highly effective against breast cancer metastases. Br J Cancer. 2008;99(5):741–749.
   PubMed Web of Science ®Google Scholar
• Duong MTQ, Qin Y, You SH, et al. Bacteria-cancer interactions: bacteria-based cancer therapy. Exp Mol Med. 2019;51(12):1–15.
   PubMedGoogle 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. J Clin Oncol. 2002;20(1):142–152.
   PubMed Web of Science ®Google Scholar
• Heimann DM, Rosenberg SA. Continuous intravenous administration of live genetically modified Salmonella typhimurium in patients with metastatic melanoma. J Immunother. 2003;26(2):179–180.
   PubMed Web of Science ®Google Scholar
• Forbes NS. Engineering the perfect (bacterial) cancer therapy. Nat Rev Cancer. 2010;10(11):785–794.
   PubMed Web of Science ®Google Scholar
• Riglar DT, Silver PA. Engineering bacteria for diagnostic and therapeutic applications. Nat Rev Microbiol. 2018;16(4):214–225.
   PubMed Web of Science ®Google Scholar
• Cabral H, Matsumoto Y, Mizuno K, et al. Accumulation of sub-100 nm polymeric micelles in poorly permeable tumours depends on size. Nat Nanotechnol. 2011;6(12):815–823.
   PubMed Web of Science ®Google Scholar
• Forbes NS, Coffin RS, Deng L, et al. White paper on microbial anti-cancer therapy and prevention. J Immunother Cancer. 2018;6(1):78.
   PubMedGoogle Scholar
• Pangilinan CR, Lee CH. Salmonella-Based targeted cancer therapy: updates on a promising and innovative tumor immunotherapeutic strategy. Biomedicines. 2019;7(2):36.
   PubMed Web of Science ®Google Scholar
• Charbonneau MR, Isabella VM, Li N, et al. Developing a new class of engineered live bacterial therapeutics to treat human diseases. Nat Commun. 2020;11(1):1738.
   PubMed Web of Science ®Google Scholar
• Nemunaitis J, Cunningham C, Senzer N, et al. Pilot trial of genetically modified, attenuated Salmonella expressing the E. coli cytosine deaminase gene in refractory cancer patients. Cancer Gene Ther. 2003;10(10):737–744.
   PubMed Web of Science ®Google Scholar
• Afkhami-Poostchi A, Mashreghi M, Iranshahi M, et al. Use of a genetically engineered E. coli overexpressing β-glucuronidase accompanied by glycyrrhizic acid, a natural and anti-inflammatory agent, for directed treatment of Colon carcinoma in a mouse model. Int J Pharm. 2020;579:119159.
   PubMedGoogle Scholar
• Hosseini-Giv N, Bahrami AR, Matin MM. Application of bacterial directed enzyme prodrug therapy as a targeted chemotherapy approach in a mouse model of breast cancer. Int J Pharm. 2021;606:120931.
   PubMedGoogle Scholar
• Ryan RM, Green J, Lewis CE. Use of bacteria in anti-cancer therapies. Bioessays. 2006;28(1):84–94.
   PubMed Web of Science ®Google Scholar
• Nomura S, Takahashi M, Kato AH, et al. Biosorption-based 64Cu-labeling of bacteria for pharmacokinetic positron-emission tomography. Int J Pharm. 2020;590:119950.
   PubMedGoogle Scholar
• Cohen SN, Chang AC, Hsu L. Nonchromosomal antibiotic resistance in bacteria: genetic transformation of Escherichia coli by R-factor DNA. Proc Natl Acad Sci U S A. 1972;69(8):2110–2114.
   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. PLoS One. 2009;4(8):e6692.
   PubMed Web of Science ®Google Scholar
• Baker JHE, Kyle AH, Bartels KL, et al. Targeting the tumour vasculature: exploitation of low oxygenation and sensitivity to NOS inhibition by treatment with a hypoxic cytotoxin. PLoS One. 2013;8(10):e76832.
   PubMed Web of Science ®Google Scholar
• Smith NR, Baker D, Farren M, et al. Tumor stromal architecture can define the intrinsic tumor response to VEGF-targeted therapy. Clin Cancer Res. 2013;19(24):6943–6956.
   PubMed Web of Science ®Google Scholar
• Jiang Y, Allen D, Kersemans V, et al. Acute vascular response to cediranib treatment in human non-small-cell lung cancer xenografts with different tumour stromal architecture. Lung Cancer. 2015;90(2):191–198.
   PubMed Web of Science ®Google Scholar
• Wegner CS, Hauge A, Simonsen TG, et al. DCE-MRI of sunitinib-induced changes in tumor microvasculature and hypoxia: a study of pancreatic ductal adenocarcinoma xenografts. Neoplasia. 2018;20(7):734–744.
   PubMed Web of Science ®Google Scholar
• Park CR, Jo JH, Song MG, et al. Secreted protein acidic and rich in cysteine mediates active targeting of human serum albumin in U87MG xenograft mouse models. Theranostics. 2019;9(24):7447–7457.
   PubMed Web of Science ®Google Scholar
• Gao Q, Yang Z, Xu S, et al. Heterotypic CAF-tumor spheroids promote early peritoneal metastatis of ovarian cancer. J Exp Med. 2019;216(3):688–703.
   PubMed Web of Science ®Google Scholar
• Sato R, Imamura K, Semba T, et al. TGFβ signaling activated by cancer-associated fibroblasts determines the histological signature of lung adenocarcinoma. Cancer Res. 2021;81(18):4751–4765.
   PubMed Web of Science ®Google Scholar
• Weibel S, Stritzker J, Eck M, et al. Colonization of experimental murine breast tumours by Escherichia coli K-12 significantly alters the tumour microenvironment. Cell Microbiol. 2008;10(6):1235–1248.
   PubMed Web of Science ®Google Scholar
• Stern C, Kasnitz N, Kocijancic D, et al. Induction of CD4(+) and CD8(+) anti-tumor effector T cell responses by bacteria mediated tumor therapy. Int J Cancer. 2015;137(8):2019–2028.
   PubMed Web of Science ®Google Scholar
• Kocijancic D, Felgner S, Schauer T, et al. Local application of bacteria improves safety of Salmonella-mediated tumor therapy and retains advantages of systemic infection. Oncotarget. 2017;8(30):49988–50001.
   PubMedGoogle Scholar
• Kang SR, Jo EJ, Nguyen VH, et al. Imaging of tumor colonization by Escherichia coli using 18F-FDS PET. Theranostics. 2020;10(11):4958–4966.
   PubMed Web of Science ®Google Scholar
• Yu YA, Zhang Q, Szalay AA. Establishment and characterization of conditions required for tumor colonization by intravenously delivered bacteria. Biotechnol Bioeng. 2008;100(3):567–578.
   PubMed Web of Science ®Google Scholar
• Westphal K, Leschner S, Jablonska J, et al. Containment of tumor-colonizing bacteria by host neutrophils. Cancer Res. 2008;68(8):2952–2960.
   PubMed Web of Science ®Google Scholar
• Ganai S, Arenas RB, Sauer JP, et al. In tumors Salmonella migrate away from vasculature toward the transition zone and induce apoptosis. Cancer Gene Ther. 2011;18(7):457–466.
   PubMed Web of Science ®Google Scholar
• Matsumoto Y, Nichols JW, Toh K, et al. Vascular bursts enhance permeability of tumour blood vessels and improve nanoparticle delivery. Nat Nanotechnol. 2016;11(6):533–538.
   PubMed Web of Science ®Google Scholar
• Beuzón CR, Méresse S, Unsworth KE, et al. Salmonella maintains the integrity of its intracellular vacuole through the action of SifA. Embo J. 2000;19(13):3235–3249.
   PubMed Web of Science ®Google Scholar
• Raman V, Van Dessel N, Hall CL, et al. Intracellular delivery of protein drugs with an autonomously lysing bacterial system reduces tumor growth and metastases. Nat Commun. 2021;12(1):6116.
   PubMed Web of Science ®Google Scholar
• Kasinskas RW, Forbes NS. Salmonella typhimurium lacking ribose chemoreceptors localize in tumor quiescence and induce apoptosis. Cancer Res. 2007;67(7):3201–3209.
   PubMed Web of Science ®Google Scholar
• Hansen CH, Endres RG, Wingreen NS. Chemotaxis in Escherichia coli: a molecular model for robust precise adaptation. PLoS Comput Biol. 2008;4(1):e1.
   PubMed Web of Science ®Google Scholar
• Toley BJ, Forbes NS. Motility is critical for effective distribution and accumulation of bacteria in tumor tissue. Integr Biol (Camb). 2012;4(2):165–176.
   PubMed Web of Science ®Google Scholar
• Silva-Valenzuela CA, Desai PT, Molina-Quiroz RC, et al. Solid tumors provide niche-specific conditions that lead to preferential growth of Salmonella. Oncotarget. 2016;7(23):35169–35180.
   PubMedGoogle Scholar
• Raman V, Van Dessel N, O’Connor OM, et al. The motility regulator flhDC drives intracellular accumulation and tumor colonization of Salmonella. J Immunother Cancer. 2019;7(1):44.
   PubMedGoogle Scholar
• Kano MR, Komuta Y, Iwata C, et al. Comparison of the effects of the kinase inhibitors imatinib, sorafenib, and transforming growth factor-β receptor inhibitor on extravasation of nanoparticles from neovasculature. Cancer Sci. 2009;100(1):173–180.
   PubMed Web of Science ®Google Scholar
• Diop-Frimpong B, Chauhan VP, Krane S, et al. Losartan inhibits collagen I synthesis and improves the distribution and efficacy of nanotherapeutics in tumors. Proc Natl Acad Sci U S A. 2011;108(7):2909–2914.
   PubMed Web of Science ®Google Scholar
• Zhang L, Nishihara H, Kano MR. Pericyte-coverage of human tumor vasculature and nanoparticle permeability. Biol Pharm Bull. 2012;35(5):761–766.
   PubMed Web of Science ®Google Scholar
• Kohli AG, Kivimäe S, Tiffany MR, et al. Improving the distribution of doxil® in the tumormatrix by depletion of tumor hyaluronan. J Control Release. 2014;191:105–114.
   PubMed Web of Science ®Google Scholar
• Miao L, Huang L. Exploring the tumor microenvironment with nanoparticles. Cancer Treat Res. 2015;166:193–226.
   PubMedGoogle Scholar
• Dolor A, Szoka FC. Digesting a path forward: the utility of collagenase tumor treatment for improved drug delivery. Mol Pharm. 2018;15(6):2069–2083.
   PubMedGoogle Scholar
• Xu S, Xu H, Wang W, et al. The role of collagen in cancer: from bench to bedside. J Transl Med. 2019;17(1):309.
   PubMed Web of Science ®Google Scholar