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REVIEW

Bacteria-Based Nanoprobes for Cancer Therapy

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Pages 759-785 | Received 05 Sep 2023, Accepted 04 Jan 2024, Published online: 23 Jan 2024

References

  • Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68(6):394–424. doi:10.3322/caac.21492
  • Yock TI, Yeap BY, Ebb DH, et al. Long-term toxic effects of proton radiotherapy for paediatric medulloblastoma: a Phase 2 single-arm study. Lancet Oncol. 2016;17(3):287–298. doi:10.1016/S1470-2045(15)00167-9
  • Li H, Jin H, Wan W, Wu C, Wei L. Cancer nanomedicine: mechanisms, obstacles and strategies. Nanomedicine. 2018;13(13):1639–1656. doi:10.2217/nnm-2018-0007
  • Schiller JH, Harrington D, Belani CP, et al. Comparison of Four Chemotherapy Regimens for Advanced Non–Small-Cell Lung Cancer. N Engl J Med. 2002;346(2):92–98. doi:10.1056/NEJMoa011954
  • Sharma R, Tobin P, Clarke SJ. Management of chemotherapy-induced nausea, vomiting, oral mucositis, and diarrhoea. Lancet Oncol. 2005;6(2):93–102. doi:10.1016/S1470-2045(05)01735-3
  • Matsumura Y, Maeda H. A New Concept for Macromolecular Therapeutics in Cancer Chemotherapy: mechanism of Tumoritropic Accumulation of Proteins and the Antitumor Agent Smancs. Cancer Res. 1986;46(12 Pt 1):6387–6392.
  • Maeda H. Tumor-selective delivery of macromolecular drugs via the EPR effect: background and future prospects. Bioconjug Chem. 2010;21(5):797–802. doi:10.1021/bc100070g
  • Kobayashi H, Turkbey B, Watanabe R, Choyke PL. Cancer drug delivery: considerations in the rational design of nanosized bioconjugates. Bioconjug Chem. 2014;25(12):2093–2100. doi:10.1021/bc500481x
  • Wu C, Li H, Zhao H, et al. Potentiating antilymphoma efficacy of chemotherapy using a liposome for integration of CD20 targeting, ultra-violet irradiation polymerizing, and controlled drug delivery. Nanoscale Res Lett. 2014;9(1):9–12. doi:10.1186/1556-276X-9-447
  • Bar-Zeev M, Livney YD, Assaraf YG. Targeted nanomedicine for cancer therapeutics: towards precision medicine overcoming drug resistance. Drug Resist Updat. 2017;31:15–30. doi:10.1016/j.drup.2017.05.002
  • Choi JH, Ha T, Shin M, Lee SN, Choi JW. Nanomaterial-based fluorescence resonance energy transfer (Fret) and metal-enhanced fluorescence (mef) to detect nucleic acid in cancer diagnosis. Biomedicines. 2021;9(8):928. doi:10.3390/biomedicines9080928
  • Li M, Zhao G, Su WK, Shuai Q. Enzyme-Responsive Nanoparticles for Anti-tumor Drug Delivery. Front Chem. 2020;8:1–20. doi:10.3389/fchem.2020.00001
  • Guo X, Shi C, Wang J, Di S, Zhou S. PH-triggered intracellular release from actively targeting polymer micelles. Biomaterials. 2013;34(18):4544–4554. doi:10.1016/j.biomaterials.2013.02.071
  • Gordon AN, Fleagle JT, Guthrie D, Parkin DE, Gore ME, Lacave AJ. Recurrent epithelial ovarian carcinoma: a randomized Phase III study of pegylated liposomal doxorubicin versus topotecan. J Clin Oncol. 2001;19(14):3312–3322. doi:10.1200/JCO.2001.19.14.3312
  • Gradishar WJ, Tjulandin S, Davidson N, et al. Phase III trial of nanoparticle albumin-bound paclitaxel compared with polyethylated castor oil-based paclitaxel in women with breast cancer. J Clin Oncol. 2005;23(31):7794–7803. doi:10.1200/JCO.2005.04.937
  • Wilhelm S, Tavares AJ, Dai Q, et al. Analysis of nanoparticle delivery to tumours. Nat Rev Mater. 2016;1(5):1–12. doi:10.1038/natrevmats.2016.14
  • Christopher AMLS M. Principles of nanoparticle design for overcoming biological barriers to drug delivery. Physiol Behav. 2016;176:100–106.
  • Jain RK, Stylianopoulos T. Delivering nanomedicine to solid tumors. Nat Rev Clin Oncol. 2010;7(11):653–664. doi:10.1038/nrclinonc.2010.139
  • Li C, Zhang J, Zu YJ, et al. Biocompatible and biodegradable nanoparticles for enhancement of anti-cancer activities of phytochemicals. Chin J Nat Med. 2015;13(9):641–652. doi:10.1016/S1875-5364(15)30061-3
  • Zhao X, Xie N, Zhang H, Zhou W, Ding J. Bacterial Drug Delivery Systems for Cancer Therapy: “Why” and “How”. Pharmaceutics. 2023;15(9):2214. doi:10.3390/pharmaceutics15092214
  • Yue Y, Xu J, Li Y, et al. Antigen-bearing outer membrane vesicles as tumour vaccines produced in situ by ingested genetically engineered bacteria. Nat Biomed Eng. 2022;6(7):898–909. doi:10.1038/s41551-022-00886-2
  • Harimoto T, Hahn J, Chen YY, et al. A programmable encapsulation system improves delivery of therapeutic bacteria in mice. Nat Biotechnol. 2022;40(8):1259–1269. doi:10.1038/s41587-022-01244-y
  • Thomas SC, Madaan T, Kamble NS, Siddiqui NA, Pauletti GM, Kotagiri N. Engineered Bacteria Enhance Immunotherapy and Targeted Therapy through Stromal Remodeling of Tumors. Adv Healthc Mater. 2022;11(2):e2101487. doi:10.1002/adhm.202101487
  • Van Mellaert L, Barbé S, Anné J. Clostridium spores as anti-tumour agents. Trends Microbiol. 2006;14(4):190–196. doi:10.1016/j.tim.2006.02.002
  • Coley WB. Contribution to the Knowledge of Sarcoma. Ann Surg. 1891;14:199–220. doi:10.1097/00000658-189112000-00015
  • Loughlin KR, William B. Coley: his Hypothesis, His Toxin, and the Birth of Immunotherapy. Urol Clin North Am. 2020;47(4):413–417. doi:10.1016/j.ucl.2020.07.001
  • Tsung K, Norton JA. Lessons from Coley’s Toxin. Surg Oncol. 2006;15(1):25–28. doi:10.1016/j.suronc.2006.05.002
  • Pearl R. Cancer and Tuberculosis. Am J Hyg. 1929;9:97–159.
  • Lj OLD, Clarke DA, Benacerraf B. Effect of Bacillus Calmette-Guerin infection on transplanted tumours in the mouse. Nature. 1959;184(4682):291–292. doi:10.1038/184291a0
  • Zbar B, Bernstein ID, Rapp HJ, Branch B. Suppression of tumor growth at the site of infection with living Bacillus Calmette-Guérin. J Natl Cancer Inst. 1971;46(4):831–839.
  • Lamm DL, Thor DE, Harris SC, Reyna JA, Stogdill VD, Radwin HM. Bacillus Calmette-Guerin immunotherapy of superficial bladder cancer. J Urol. 1980;124(1):38–42. doi:10.1016/S0022-5347(17)55282-9
  • DeKernion JB, Huang MY, Lindner A, Smith RB, Kaufman JJ. The management of superficial bladder tumors and carcinoma in situ with intravesical bacillus Calmette-Guerin. J Urol. 1985;133(4):598–600. doi:10.1016/S0022-5347(17)49104-X
  • Martinez-Outschoorn UE, Peiris-Pagés M, Pestell RG, Sotgia F, Lisanti MP. Cancer metabolism: a therapeutic perspective. Nat Rev Clin Oncol. 2017;14(1):11–31. doi:10.1038/nrclinonc.2016.60
  • Sambasivarao SV. Engineering the perfect (bacterial) cancer therapy. Nat Rev Cancer. 2013;18:1199–1216.
  • Chouaib S, Noman MZ, Kosmatopoulos K, Curran MA. Hypoxic stress: obstacles and opportunities for innovative immunotherapy of cancer. Oncogene. 2017;36(4):439–445. doi:10.1038/onc.2016.225
  • Vaupel P, Multhoff G, Vaupel P, Multhoff G. Hypoxia-/HIF-1α-Driven Factors of the Tumor Microenvironment Impeding Antitumor Immune Responses and Promoting Malignant Progression. Oxyg Transp Tissue XL. 2018;171–175.
  • Heldin CH, Rubin K, Pietras K, Östman A. High interstitial fluid pressure - An obstacle in cancer therapy. Nat Rev Cancer. 2004;4(10):806–813. doi:10.1038/nrc1456
  • Leschner S, Westphal K, Dietrich N, et al. Tumor invasion of Salmonella enterica serovar Typhimurium is accompanied by strong hemorrhage promoted by TNF-α. PLoS One. 2009;4(8):e6692. doi:10.1371/journal.pone.0006692
  • 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(17):5188–5193.
  • Jivrajani M, Nivsarkar M. Ligand-targeted bacterial minicells: futuristic nano-sized drug delivery system for the efficient and cost effective delivery of shRNA to cancer cells. Nanomedicine. 2016;12(8):2485–2498. doi:10.1016/j.nano.2016.06.004
  • Granato ET, Meiller-Legrand TA, Foster KR. The Evolution and Ecology of Bacterial Warfare. Curr Biol. 2019;29(11):R521–37. doi:10.1016/j.cub.2019.04.024
  • Baindara P, Mandal SM. Bacteria and bacterial anticancer agents as a promising alternative for cancer therapeutics. Biochimie. 2020;177:164–189. doi:10.1016/j.biochi.2020.07.020
  • Kang SR, Nguyen DH, Yoo SW, Min JJ. Bacteria and bacterial derivatives as delivery carriers for immunotherapy. Adv Drug Deliv Rev. 2022;181:114085. doi:10.1016/j.addr.2021.114085
  • Farkas-Himsley H, Hill R, Rosen B, Arab S, Lingwood CA. The bacterial colicin active against tumor cells in vitro and in vivo is verotoxin 1. Proc Natl Acad Sci U S A. 1995;92(15):6996–7000. doi:10.1073/pnas.92.15.6996
  • Lancaster LE, Wintermeyer W, Rodnina MV. Colicins and their potential in cancer treatment. Blood Cells Mol Dis. 2007;38(1):15–18. doi:10.1016/j.bcmd.2006.10.006
  • Stachowiak R, Lyzniak M, Budziszewska BK, et al. Cytotoxicity of bacterial metabolic products, including listeriolysin O, on leukocyte targets. J Biomed Biotechnol. 2012;2012:1–9. doi:10.1155/2012/954375
  • Lai XH, Arencibia I, Johansson A, et al. Cytocidal and Apoptotic Effects of the ClyA Protein from Escherichia coli on Primary and Cultured Monocytes and Macrophages. Infect Immun. 2000;68(7):4363–4367. doi:10.1128/IAI.68.7.4363-4367.2000
  • Barak Y, Schreiber F, Thorne SH, Contag CH, deBeer D, Matin A. Role of nitric oxide in Salmonella typhimurium-mediated cancer cell killing. BMC Cancer. 2010;10(1). doi:10.1186/1471-2407-10-146
  • Williams EL, Djamgoz MBA. Nitric oxide and metastatic cell behaviour. BioEssays. 2005;27(12):1228–1238. doi:10.1002/bies.20324
  • Liu X, Yin S, Chen Y, et al. LPS-induced proinflammatory cytokine expression in human airway epithelial cells and macrophages via NF-κB, STAT3 or AP-1 activation. Mol Med Rep. 2018;17:5484–5491.
  • Sivan A, Corrales L, Hubert N, et al. Commensal Bifidobacterium promotes antitumor immunity and facilitates anti–PD-L1 efficacy. Science. 2015;350(6264):1084–1089. doi:10.1126/science.aac4255
  • Huang X, Pan J, Xu F, et al. Bacteria-Based Cancer Immunotherapy. Adv Sci. 2021;8:1–22.
  • Bouzari S, Bakhtiari R, Ajoudanifar H, Sadat Shandiz SA. Review of the Effects of Probiotics and Their Metabolites in the Treatment of Liver Cancer: an Update on Probiotics as a New Treatment. Erciyes Med J. 2023;45:8–18.
  • Li Z, Wang Y, Liu J, et al. Chemically and Biologically Engineered Bacteria-Based Delivery Systems for Emerging Diagnosis and Advanced Therapy. Adv Mater. 2021;33(38):e2102580. doi:10.1002/adma.202102580
  • Kuehn MJ, Kesty NC. Bacterial outer membrane vesicles and the host-pathogen interaction. Genes Dev. 2005;19(22):2645–2655. doi:10.1101/gad.1299905
  • Feng Q, Ma X, Cheng K, et al. Engineered Bacterial Outer Membrane Vesicles as Controllable Two-Way Adaptors to Activate Macrophage Phagocytosis for Improved Tumor Immunotherapy. Adv Mater. 2022;34:e2206200. doi:10.1002/adma.202206200
  • Hajam IA, Dar PA, Won G, Lee JH. Bacterial Ghosts as Adjuvants: mechanisms and Potential. Vet Res. 2017;48(1):37. doi:10.1186/s13567-017-0442-5
  • Jiménez-Jiménez C, Moreno VM, Vallet-Regí M. Bacteria-Assisted Transport of Nanomaterials to Improve Drug Delivery in Cancer Therapy. Nanomaterials. 2022;12(2):288. doi:10.3390/nano12020288
  • Yin T, Diao Z, Blum NT, Qiu L, Ma A, Huang P. Engineering Bacteria and Bionic Bacterial Derivatives with Nanoparticles for Cancer Therapy. Small. 2022;18(12):e2104643. doi:10.1002/smll.202104643
  • Germanier R, Fuerer E. Isolation and characterization of Gal E mutant Ty 21a of Salmonella typhi: a candidate strain for a live, oral typhoid vaccine. J Infect Dis. 1975;131(5):553–558. doi:10.1093/infdis/131.5.553
  • Lin IYC, Van TTH, Smooker PM. Live-attenuated bacterial vectors: tools for vaccine and therapeutic agent delivery. Vaccines. 2015;3(4):940–972. doi:10.3390/vaccines3040940
  • Low KB, Ittensohn M, Le T, et al. Lipid A mutant Salmonella with suppressed virulence and TNFa induction retain tumor-targeting in vivo. Nat Biotechnol. 1999;17(1):37–41. doi:10.1038/5205
  • Zhao M, Yang M, Ma H, et al. Targeted Therapy with a Salmonella Typhimurium Leucine-Arginine Auxotroph Cures Orthotopic Human Breast Tumors in Nude Mice. Cancer Res. 2006;66(15):7647–7652. doi:10.1158/0008-5472.CAN-06-0716
  • Fàbrega A, Vila J. Salmonella enterica serovar Typhimurium skills to succeed in the host: virulence and regulation. Clin Microbiol Rev. 2013;26(2):308–341. doi:10.1128/CMR.00066-12
  • Li CX, Yu B, Shi L, et al. ‘obligate‘anaerobic Salmonella strain YB1 suppresses liver tumor growth and metastasis in nude mice. Oncol Lett. 2017;13(1):177–183. doi:10.3892/ol.2016.5453
  • 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. doi:10.1086/315497
  • Zhao M, Yang M, Li XM, et al. Tumor-targeting bacterial therapy with amino acid auxotrophs of GFP-expressing Salmonella typhimurium. Proc Natl Acad Sci U S A. 2005;102(3):755–760. doi:10.1073/pnas.0408422102
  • Kimura H, Zhang L, Zhao M, et al. Targeted therapy of spinal cord glioma with a genetically modified Salmonella typhimurium. Cell Prolif. 2010;43(1):41–48. doi:10.1111/j.1365-2184.2009.00652.x
  • Nagakura C, Hayashi K, Zhao M, et al. Efficacy of a genetically-modified Salmonella typhimurium in an orthotopic human pancreatic cancer in nude mice. Anticancer Res. 2009;29(6):1873–1878.
  • Hayashi K, Zhao M, Yamauchi K, et al. Cancer metastasis directly eradicated by targeted therapy with a modified Salmonella typhimurium. J Cell Biochem. 2009;106(6):992–998. doi:10.1002/jcb.22078
  • Hayashi K, Zhao M, Yamauchi K, et al. Systemic targeting of primary bone tumor and lung metastasis of high-grade osteosarcoma in nude mice with a tumor-selective strain of Salmonella typhimurium. Cell Cycle. 2009;8(6):870–875. doi:10.4161/cc.8.6.7891
  • Zhao M, Geller J, Ma H, Yang M, Penman S, Hoffman RM. Monotherapy with a tumor-targeting mutant of Salmonella typhimurium cures orthotopic metastatic mouse models of human prostate cancer. Proc Natl Acad Sci U S A. 2007;104(24):10170–10174. doi:10.1073/pnas.0703867104
  • Yu B, Yang M, Shi L, et al. Explicit hypoxia targeting with tumor suppression by creating an ‘obligate’ anaerobic Salmonella Typhimurium strain. Sci Rep. 2012;2(1):1–10. doi:10.1038/srep00436
  • Ning BT, Yu B, Chan S, Chan JL, Huang JD, Chan GCF. Treatment of Neuroblastoma with an Engineered “Obligate” Anaerobic Salmonella typhimurium Strain YB1. J Cancer. 2017;8(9):1609–1618. doi:10.7150/jca.18776
  • Toley BJ, Forbes NS. Motility is critical for effective distribution and accumulation of bacteria in tumor tissue. Integr Biol. 2012;4(2):165–176. doi:10.1039/c2ib00091a
  • Kasinskas RW, Forbes NS. Salmonella typhimurium Lacking Ribose Chemoreceptors Localize in Tumor Quiescence and Induce Apoptosis. Cancer Res. 2007;67(7):3201–3209. doi:10.1158/0008-5472.CAN-06-2618
  • Sznol M, Lin SL, Bermudes D, Zheng L, King I. Perspective. Use of preferentially replicating bacteria for the treatment of cancer. J Clin Invest. 2000;105(8):1027–1030. doi:10.1172/JCI9818
  • Uchugonova A, Zhao M, Zhang Y, Weinigel M, König K, Hoffman RM. Cancer-cell killing by engineered Salmonella imaged by multiphoton tomography in live mice. Anticancer Res. 2012;32(10):4331–4338.
  • Tu DG, Chang WW, Lin ST, Kuo CY, Tsao YT, Lee CH. Salmonella inhibits tumor angiogenesis by downregulation of vascular endothelial growth factor. Oncotarget. 2016;7(25):37513–37523. doi:10.18632/oncotarget.7038
  • Liu F, Zhang L, Hoffman RM, Zhao M. Vessel destruction by tumor-targeting Salmonella typhimurium A1-R is enhanced by high tumor vascularity. Cell Cycle. 2010;9(22):4518–4524. doi:10.4161/cc.9.22.13744
  • Kuan YD, Lee CH. Salmonella overcomes tumor immune tolerance by inhibition of tumor indoleamine 2, 3-dioxygenase 1 expression. Oncotarget. 2016;7(1):374–385. doi:10.18632/oncotarget.6258
  • Wang WK, Lu MF, Kuan YD, Lee CH. The treatment of mouse colorectal cancer by oral delivery tumor-targeting Salmonella. Am J Cancer Res. 2015;5(7):2222–2228.
  • Pizarro-Cerdá J, Cossart P. Microbe profile: listeria monocytogenes: a paradigm among intracellular bacterial pathogens. Microbiol. 2019;165(7):719–721. doi:10.1099/mic.0.000800
  • Radoshevich L, Cossart P. Listeria monocytogenes: towards a complete picture of its physiology and pathogenesis. Nat Rev Microbiol. 2018;16(1):32–46. doi:10.1038/nrmicro.2017.126
  • Pizarro-Cerdá J, Kühbacher A, Cossart P. Entry of listeria monocytogenes in mammalian epithelial cells: an updated view. Cold Spring Harb Perspect Med. 2012;2(11):a010009–a010009. doi:10.1101/cshperspect.a010009
  • Lambrechts A, Gevaert K, Cossart P, Vandekerckhove J, Van Troys M. Listeria comet tails: the actin-based motility machinery at work. Trends Cell Biol. 2008;18(5):220–227. doi:10.1016/j.tcb.2008.03.001
  • Flickinger JC, Rodeck U, Snook AE. Listeria monocytogenes as a vector for cancer immunotherapy: current understanding and progress. Vaccines. 2018;6(3):48. doi:10.3390/vaccines6030048
  • Brocksted DG, Giedlin MA, Leong ML, et al. Listeria-based cancer vaccines that segregate immunogenicity from toxicity. Proc Natl Acad Sci U S A. 2004;101(38):13832–13837. doi:10.1073/pnas.0406035101
  • Thompson RJ, Bouwer HGA, Portnoy DA, Frankel FR. Pathogenicity and Immunogenicity of a Listeria monocytogenes Strain That Requires d-Alanine for Growth. Infect Immun. 1998;66(8):3552–3561. doi:10.1128/IAI.66.8.3552-3561.1998
  • Verch T, Pan ZK, Paterson Y. Listeria monocytogenes -Based Antibiotic Resistance Gene-Free Antigen Delivery System Applicable to Other Bacterial Vectors and DNA Vaccines. Infect Immun. 2004;72(11):6418–6425. doi:10.1128/IAI.72.11.6418-6425.2004
  • Rayevskaya MV, Frankel FR. Systemic Immunity and Mucosal Immunity Are Induced against Human Immunodeficiency Virus Gag Protein in Mice by a New Hyperattenuated Strain of Listeria monocytogenes. J Virol. 2001;75(6):2786–2791. doi:10.1128/JVI.75.6.2786-2791.2001
  • Wallecha A, Maciag PC, Rivera S, Paterson Y, Shahabi V. Construction and Characterization of an Attenuated Listeria monocytogenes Strain for Clinical Use in Cancer Immunotherapy. Clin Vaccine Immunol. 2009;16(1):96–103. doi:10.1128/CVI.00274-08
  • Li Z, Zhao X, Higgins DE, Frankel FR. Conditional Lethality Yields a New Vaccine Strain of Listeria monocytogenes for the Induction of Cell-Mediated Immunity. Infect Immun. 2005;73(8):5065–5073. doi:10.1128/IAI.73.8.5065-5073.2005
  • Brockstedt DG, Bahjat KS, Giedlin MA, et al. Killed but metabolically active microbes: a new vaccine paradigm for eliciting effector T-cell responses and protective immunity. Nat Med. 2005;11(8):853–860. doi:10.1038/nm1276
  • Lauer P, Hanson B, Lemmens EE, et al. Constitutive Activation of the PrfA Regulon Enhances the Potency of Vaccines Based on Live-Attenuated and Killed but Metabolically Active Listeria monocytogenes Strains. Infect Immun. 2008;76(8):3742–3753. doi:10.1128/IAI.00390-08
  • Ikonomidis G, Paterson Y, Kos FJ, Portnoy DA. Delivery of a viral antigen to the class i processing and presentation pathway by listeria monocytogenes. J Exp Med. 1994;180(6):2209–2218. doi:10.1084/jem.180.6.2209
  • Shahabi V, Reyes-Reyes M, Wallecha A, Rivera S, Paterson Y, MacIag P. Development of a Listeria monocytogenes based vaccine against prostate cancer. Cancer Immunol Immunother. 2008;57(9):1301–1313. doi:10.1007/s00262-008-0463-z
  • Gunn GR, Zubair A, Peters C, Pan Z-K, Wu T-C, Paterson Y. Two Listeria monocytogenes Vaccine Vectors That Express Different Molecular Forms of Human Papilloma Virus-16 (HPV-16) E7 Induce Qualitatively Different T Cell Immunity That Correlates with Their Ability to Induce Regression of Established Tumors Immortalized by HPV-16. J Immunol. 2001;167(11):6471–6479. doi:10.4049/jimmunol.167.11.6471
  • Sewell DA, Shahabi V, Gunn GR, Pan ZK, Dominiecki ME, Paterson Y. Recombinant Listeria Vaccines Containing PEST Sequences Are Potent Immune Adjuvants for the Tumor-Associated Antigen Human Papillomavirus-16 E7. Cancer Res. 2004;64(24):8821–8825. doi:10.1158/0008-5472.CAN-04-1958
  • Schnupf P, Zhou J, Varshavsky A, Portnoy DA. Listeriolysin O Secreted by Listeria monocytogenes into the Host Cell Cytosol Is Degraded by the N-End Rule Pathway. Infect Immun. 2007;75(11):5135–5147. doi:10.1128/IAI.00164-07
  • Jin MP, Ng VH, Maeda S, Rest RF, Karin M. Anthrolysin O and other gram-positive cytolysins are toll-like receptor 4 agonists. J Exp Med. 2004;200(12):1647–1655. doi:10.1084/jem.20041215
  • Wallecha A, Wood L, Pan ZK, Maciag PC, Shahabi V, Paterson Y. Listeria monocytogenes-derived listeriolysin O has pathogen-associated molecular pattern-like properties independent of its hemolytic ability. Clin Vaccine Immunol. 2013;20(1):77–84. doi:10.1128/CVI.00488-12
  • Hussain SF, Paterson Y. CD4+CD25+ regulatory T cells that secrete TGFβ and IL-10 are preferentially induced by a vaccine vector. J Immunother. 2004;27(5):339–346. doi:10.1097/00002371-200409000-00002
  • Chen Z, Ozbun L, Chong N, Wallecha A, Berzofsky JA, Khleif SN. Episomal expression of truncated listeriolysin O in LmddA-LLO- E7 vaccine enhances antitumor efficacy by preferentially inducing expansions of CD4+ FoxP3− and CD8+ T cells Zhisong. Cancer Immunol Res. 2014;2(9):911–922. doi:10.1158/2326-6066.CIR-13-0197
  • Sewell DA, Pan ZK, Paterson Y. Listeria-based HPV-16 E7 vaccines limit autochthonous tumor growth in a transgenic mouse model for HPV-16 transformed tumors. Vaccine. 2008;26(41):5315–5320. doi:10.1016/j.vaccine.2008.07.036
  • Wood LM, Pan ZK, Shahabi V, Paterson Y. Listeria-derived ActA is an effective adjuvant for primary and metastatic tumor immunotherapy. Cancer Immunol Immunother. 2010;59(7):1049–1058. doi:10.1007/s00262-010-0830-4
  • Moors MA, Auerbuch V, Portnoy DA. Stability of the Listeria monocytogenes ActA protein in mammalian cells is regulated by the N-end rule pathway. Cell Microbiol. 1999;1(3):249–257. doi:10.1046/j.1462-5822.1999.00020.x
  • Parker RC, Plummer HC, Siebenmann CO, Chapman MG. Effect of Histolyticus Infection and Toxin on Transplantable Mouse Tumors. Proc Soc Exp Biol Med. 1947;66(2):461–467. doi:10.3181/00379727-66-16124
  • Barbé S, Van Mellaert L, Theys J, et al. Secretory production of biologically active rat interleukin-2 by Clostridium acetobutylicum DSM792 as a tool for anti-tumor treatment. FEMS Microbiol Lett. 2005;246(1):67–73. doi:10.1016/j.femsle.2005.03.037
  • Liu S, Xu X, Zeng X, Li L, Chen Q, Li J. Tumor-targeting bacterial therapy: a potential treatment for oral cancer. Oncol Lett. 2014;8(6):2359–2366. doi:10.3892/ol.2014.2525
  • 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(26):15155–15160. doi:10.1073/pnas.251543698
  • Bettegowda C, Huang X, Lin J, et al. The genome and transcriptomes of the anti-tumor agent Clostridium novyi-NT. Nat Biotechnol. 2006;24(12):1573–1580. doi:10.1038/nbt1256
  • Agrawal N, Bettegowda C, Cheong I, et al. Bacteriolytic therapy can generate a potent immune response against experimental tumors. Proc Natl Acad Sci U S A. 2004;101(42):15172–15177. doi:10.1073/pnas.0406242101
  • Zhang YL, Lü R, Chang ZS, et al. Clostridium sporogenes delivers interleukin-12 to hypoxic tumours, producing antitumour activity without significant toxicity. Lett Appl Microbiol. 2014;59(6):580–586. doi:10.1111/lam.12322
  • Kaper JB, Nataro JP, Mobley HLT. Pathogenic Escherichia coli. Nat Rev Microbiol. 2004;2(2):123–140. doi:10.1038/nrmicro818
  • Acs Y, Loo JFC, Yu S, Kong SK, Chan TF. Monitoring bacterial growth using tunable resistive pulse sensing with a pore-based technique. Appl Microbiol Biotechnol. 2014;98(2):855–862. doi:10.1007/s00253-013-5377-9
  • Kubitschek HE. Cell volume increase in Escherichia coli after shifts to richer media. J Bacteriol. 1990;172(1):94–101. doi:10.1128/jb.172.1.94-101.1990
  • Liu Q, Gai Y, Chen Y, Lan X, Jiang D. Escherichia coli nissle 1917 as a novel microrobot for tumor-targeted imaging and therapy. Pharmaceutics. 2021;13(8):1226. doi:10.3390/pharmaceutics13081226
  • Henker J, Laass M, Blokhin BM, et al. The probiotic Escherichia coli strain Nissle 1917 (EcN) stops acute diarrhoea in infants and toddlers. Eur J Pediatr. 2007;166(4):311–318. doi:10.1007/s00431-007-0419-x
  • Stritzker J, Weibel S, Hill PJ, Oelschlaeger TA, Goebel W, Szalay AA. Tumor-specific colonization, tissue distribution, and gene induction by probiotic Escherichia coli Nissle 1917 in live mice. Int J Med Microbiol. 2007;297(3):151–162. doi:10.1016/j.ijmm.2007.01.008
  • He L, Yang H, Liu F, et al. Escherichia coli Nissle 1917 engineered to express Tum-5 can restrain murine melanoma growth. Oncotarget. 2017;8(49):85772–85782. doi:10.18632/oncotarget.20486
  • Zhang Y, Zhang Y, Xia L, et al. Escherichia coli Nissle 1917 targets and restrains mouse b16 melanoma and 4T1 breast tumors through expression of azurin protein. Appl Environ Microbiol. 2012;78(21):7603–7610. doi:10.1128/AEM.01390-12
  • Zschüttig A, Auerbach C, Meltke S, et al. Complete Sequence of Probiotic Symbioflor 2 Escherichia coli Strain G3/10 and Draft Sequences of Symbioflor 2 E. coli Strains G1/2, G4/9, G5, G6/7, and G8. Genome Announc. 2015;3(2):9–10. doi:10.1128/genomeA.01330-14
  • Kocijancic D, Felgner S, Frahm M, et al. Therapy of solid tumors using probiotic Symbioflor-2-restraints and potential. Oncotarget. 2016;7(16):22605–22622. doi:10.18632/oncotarget.8027
  • Zhu J, Ke Y, Liu Q, et al. Engineered Lactococcus lactis secreting Flt3L and OX40 ligand for in situ vaccination-based cancer immunotherapy. Nat Commun. 2022;13(1):7466. doi:10.1038/s41467-022-35130-7
  • Kaczmarek K, Więckiewicz J, Węglarczyk K, Siedlar M, Baran J. The Anti-Tumor Effect of Lactococcus lactis Bacteria-Secreting Human Soluble TRAIL Can Be Enhanced by Metformin Both In Vitro and In Vivo in a Mouse Model of Human Colorectal Cancer. Cancers. 2021;13(12):3004. doi:10.3390/cancers13123004
  • Heydari Z, Rahaie M, Alizadeh AM, Agah S, Khalighfard S, Bahmani S. Effects of Lactobacillus acidophilus and Bifidobacterium bifidum Probiotics on the Expression of MicroRNAs 135b, 26b, 18a and 155, and Their Involving Genes in Mice Colon Cancer. Probiotics Antimicrob Proteins. 2019;11(4):1155–1162. doi:10.1007/s12602-018-9478-8
  • Huter V, Szostak MP, Gampfer J, et al. Bacterial ghosts as drug carrier and targeting vehicles. J Control Release. 1999;61(1–2):51–63. doi:10.1016/S0168-3659(99)00099-1
  • Langemann T, Koller VJ, Muhammad A, Kudela P, Mayr UB, Lubitz W. The bacterial ghost platform system: production and applications. Bioeng Bugs. 2010;1(5):326–336. doi:10.4161/bbug.1.5.12540
  • Hajam IA, Dar PA, Appavoo E, Kishore S, Bhanuprakash V, Ganesh K. Bacterial ghosts of Escherichia coli drive efficient maturation of bovine monocyte-derived dendritic cells. PLoS One. 2015;10(12):1–15. doi:10.1371/journal.pone.0144397
  • Kraśko JA, Źilionyte K, Darinskas A, et al. Bacterial ghosts as adjuvants in syngeneic tumour cell lysate-based anticancer vaccination in a murine lung carcinoma model. Oncol Rep. 2017;37(1):171–178. doi:10.3892/or.2016.5252
  • Parti RP, Biswas D, Wang M, Liao M, Dillon JAR. A MinD mutant of enterohemorrhagic E. coli O157:H7 has reduced adherence to human epithelial cells. Microb Pathog. 2011;51(5):378–383. doi:10.1016/j.micpath.2011.07.003
  • MacDiarmid JA, Brahmbhatt H. Minicells: versatile vectors for targeted drug or si/shRNA cancer therapy. Curr Opin Biotechnol. 2011;22(6):909–916. doi:10.1016/j.copbio.2011.04.008
  • Farley MM, Hu B, Margolin W, Liu J, de Boer P. Minicells, back in fashion. J Bacteriol. 2016;198(8):1186–1195. doi:10.1128/JB.00901-15
  • MacDiarmid JA, Amaro-Mugridge NB, Madrid-Weiss J, et al. Sequential treatment of drug-resistant tumors with targeted minicells containing siRNA or a cytotoxic drug. Nat Biotechnol. 2009;27(7):643–651. doi:10.1038/nbt.1547
  • Shubhika K. Nanotechnology and medicine - The upside and the downside. Int J Drug Dev Res. 2013;5:1–10.
  • Nguyen HN, Romero Jovel S, Nguyen THK. Nanosized Minicells Generated by Lactic Acid Bacteria for Drug Delivery. J Nanomater. 2017;2017:1–10. doi:10.1155/2017/6847297
  • Park JW. Liposome-based drug delivery in breast cancer treatment. Breast Cancer Res. 2002;4(3):95–99. doi:10.1186/bcr432
  • Solomon BJ, Desai J, Rosenthal M, et al. A First-Time-In-Human Phase i Clinical Trial of Bispecific Antibody-Targeted, Paclitaxel-Packaged Bacterial Minicells. PLoS One. 2015;10(12):1–17. doi:10.1371/journal.pone.0144559
  • MacDiarmid JA, Langova V, Bailey D, et al. Targeted doxorubicin delivery to brain tumors via minicells: proof of principle using dogs with spontaneously occurring tumors as a model. PLoS One. 2016;11(4):1–23. doi:10.1371/journal.pone.0151832
  • Zhang Y, Ji W, He L, et al. E. coli Nissle 1917-Derived Minicells for Targeted Delivery of Chemotherapeutic Drug to Hypoxic Regions for Cancer Therapy. Theranostics. 2018;8(6):1690–1705. doi:10.7150/thno.21575
  • Chatterjee SN, Das J. Electron Microscopic Observations on the Excretion of Cell-wall Material. J Gen Microbiol. 1967;49(1):1–11. doi:10.1099/00221287-49-1-1
  • Toyofuku M, Nomura N, Eberl L. Types and origins of bacterial membrane vesicles. Nat Rev Microbiol. 2019;17(1):13–24. doi:10.1038/s41579-018-0112-2
  • Gujrati V, Kim S, Kim SH, et al. Bioengineered bacterial outer membrane vesicles as cell-specific drug-delivery vehicles for cancer therapy. ACS Nano. 2014;8(2):1525–1537. doi:10.1021/nn405724x
  • Li Y, Zhao R, Cheng K, et al. Bacterial Outer Membrane Vesicles Presenting Programmed Death 1 for Improved Cancer Immunotherapy via Immune Activation and Checkpoint Inhibition. ACS Nano. 2020;14(12):16698–16711. doi:10.1021/acsnano.0c03776
  • Santos JC, Dick MS, Lagrange B, et al. LPS targets host guanylate-binding proteins to the bacterial outer membrane for non-canonical inflammasome activation. EMBO J. 2018;37(6):1–19. doi:10.15252/embj.201798089
  • Dorward DW, Garon CF. DNA is packaged within membrane-derived vesicles of gram-negative but not gram-positive bacteria. Appl Environ Microbiol. 1990;56(6):1960–1962. doi:10.1128/aem.56.6.1960-1962.1990
  • Zhang Y, Fang Z, Li R, Huang X, Liu Q. Design of outer membrane vesicles as cancer vaccines: a new toolkit for cancer therapy. Cancers. 2019;11(9):1–24. doi:10.3390/cancers11091314
  • Blakemore R. Magnetotactic bacteria. Science. 1975;190(4212):377–379. doi:10.1126/science.170679
  • Dieudonné A, Pignol D, Prévéral S. Magnetosomes: biogenic iron nanoparticles produced by environmental bacteria. Appl Microbiol Biotechnol. 2019;103(9):3637–3649. doi:10.1007/s00253-019-09728-9
  • Farina M, Esquivel DMS, de Barros HGPL. Magnetic iron-sulphur crystals from a magnetotactic microorganism. Nature. 1990;343(6255):256–258. doi:10.1038/343256a0
  • Frankel RB, Blakemore RP, Wolfe RS. Magnetite in freshwater magnetotactic bacteria. Science. 1979;203(4387):1355–1356. doi:10.1126/science.203.4387.1355
  • Lisjak D, Mertelj A. Anisotropic magnetic nanoparticles: a review of their properties, syntheses and potential applications. Prog Mater Sci. 2018;95:286–328.
  • Yang W, Bai Y, Wang X, Dong X, Li Y, Fang M. Attaching biosynthesized bacterial magnetic particles to polyethylenimine enhances gene delivery into mammalian cells. J Biomed Nanotechnol. 2016;12(4):789–799. doi:10.1166/jbn.2016.2213
  • Mériaux S, Boucher M, Marty B, et al. Magnetosomes, Biogenic Magnetic Nanomaterials for Brain Molecular Imaging with 17.2 T MRI Scanner. Adv Healthc Mater. 2015;4(7):1076–1083. doi:10.1002/adhm.201400756
  • Orlando T, Mannucci S, Fantechi E, et al. Characterization of magnetic nanoparticles from Magnetospirillum Gryphiswaldense as potential theranostics tools. Contrast Media Mol Imaging. 2016;11(2):139–145. doi:10.1002/cmmi.1673
  • Erdal E, Demirbilek M, Yeh Y, et al. A Comparative Study of Receptor-Targeted Magnetosome and HSA-Coated Iron Oxide Nanoparticles as MRI Contrast-Enhancing Agent in Animal Cancer Model. Appl Biochem Biotechnol. 2018;185(1):91–113. doi:10.1007/s12010-017-2642-x
  • Alphandéry E, Idbaih A, Adam C, et al. Chains of magnetosomes with controlled endotoxin release and partial tumor occupation induce full destruction of intracranial U87-Luc glioma in mice under the application of an alternating magnetic field. J Control Release. 2017;262:259–272. doi:10.1016/j.jconrel.2017.07.020
  • Long R, Liu Y, Dai Q, Wang S, Deng Q, Zhou X. A natural bacterium-produced membrane-bound nanocarrier for drug combination therapy. Materials. 2016;9(11):1–10. doi:10.3390/ma9110889
  • Wang X, Wang J, Geng Y, et al. An enhanced anti-tumor effect of apoptin-cecropin B on human hepatoma cells by using bacterial magnetic particle gene delivery system. Biochem Biophys Res Commun. 2018;496(2):719–725. doi:10.1016/j.bbrc.2018.01.108
  • Dai Q, Long R, Wang S, et al. Bacterial magnetosomes as an efficient gene delivery platform for cancer theranostics. Microb Cell Fact. 2017;16(1):1–9. doi:10.1186/s12934-017-0830-6
  • Pum D, Toca-Herrera JL, Sleytr UB. S-Layer protein self-assembly. Int J Mol Sci. 2013;14(2):2484–2501. doi:10.3390/ijms14022484
  • Stel B, Cometto F, Rad B, De Yoreo JJ, Lingenfelder M. Dynamically resolved self-assembly of S-layer proteins on solid surfaces. Chem Commun. 2018;54(73):10264–10267. doi:10.1039/C8CC04597F
  • Ilk N, Egelseer EM, Sleytr UB. S-layer fusion proteins-construction principles and applications. Curr Opin Biotechnol. 2011;22(6):824–831. doi:10.1016/j.copbio.2011.05.510
  • Wetzer B, Pum D, Sleytr UB. S-layer stabilized solid supported lipid bilayers. J Struct Biol. 1997;119(2):123–128. doi:10.1006/jsbi.1997.3867
  • Farjadian F, Moghoofei M, Mirkiani S, et al. Bacterial components as naturally inspired nano-carriers for drug/gene delivery and immunization: set the bugs to work? Biotechnol Adv. 2018;36(4):968–985. doi:10.1016/j.biotechadv.2018.02.016
  • Shi H, Chen L, Liu Y, et al. Bacteria-Driven Tumor Microenvironment-Sensitive Nanoparticles Targeting Hypoxic Regions Enhances the Chemotherapy Outcome of Lung Cancer. International Journal of Nanomedicine. 2023;18:1299–1315. doi:10.2147/IJN.S396863
  • Li J, Dai J, Zhao L, et al. Bioactive Bacteria/MOF Hybrids Can Achieve Targeted Synergistic Chemotherapy and Chemodynamic Therapy against Breast Tumors. Adv Funct Mater. 2023;33(42):2303254. doi:10.1002/adfm.202303254
  • Xiao S, Shi H, Zhang Y, et al. Bacteria-driven hypoxia targeting delivery of chemotherapeutic drug proving outcome of breast cancer. J Nanobiotechnol. 2022;20(1):178. doi:10.1186/s12951-022-01373-1
  • Li Y, Leng Q, Zhang Y, et al. Anaerobic bacteria mediated ‘smart missile’ targeting tumor hypoxic area enhances the therapeutic outcome of lung cancer. Chem Eng J. 2022;438:135566. doi:10.1016/j.cej.2022.135566
  • Chen Q, Bai H, Wu W, et al. Bioengineering Bacterial Vesicle-Coated Polymeric Nanomedicine for Enhanced Cancer Immunotherapy and Metastasis Prevention. Nano Lett. 2020;20(1):11–21. doi:10.1021/acs.nanolett.9b02182
  • Kuerban K, Gao X, Zhang H, et al. Doxorubicin-loaded bacterial outer-membrane vesicles exert enhanced anti-tumor efficacy in non-small-cell lung cancer. Acta Pharm Sin B. 2020;10(8):1534–1548. doi:10.1016/j.apsb.2020.02.002
  • Patyar S, Joshi R, Byrav DSP, Prakash A, Medhi B, Das BK. Bacteria in cancer therapy: a novel experimental strategy. J Biomed Sci. 2010;17(1):1–9. doi:10.1186/1423-0127-17-21
  • Xie S, Zhao L, Song X, Tang M, Mo C, Li X. Doxorubicin-conjugated Escherichia coli Nissle 1917 swimmers to achieve tumor targeting and responsive drug release. J Control Release. 2017;268:390–399. doi:10.1016/j.jconrel.2017.10.041
  • Quispe-Tintaya W, Chandra D, Jahangir A, et al. Nontoxic radioactive Listeria at is a highly effective therapy against metastatic pancreatic cancer. Proc Natl Acad Sci U S A. 2013;110(21):8668–8673. doi:10.1073/pnas.1211287110
  • Chandra D, Selvanesan BC, Yuan Z, et al. 32-Phosphorus selectively delivered by listeria to pancreatic cancer demonstrates a strong therapeutic effect. Oncotarget. 2017;8(13):20729–20740. doi:10.18632/oncotarget.15117
  • Li X, Lovell JF, Yoon J, Chen X. Clinical development and potential of photothermal and photodynamic therapies for cancer. Nat Rev Clin Oncol. 2020;17(11):657–674. doi:10.1038/s41571-020-0410-2
  • Qing S, Lyu C, Zhu L, et al. Biomineralized Bacterial Outer Membrane Vesicles Potentiate Safe and Efficient Tumor Microenvironment Reprogramming for Anticancer Therapy. Adv Mater. 2020;32:1–14.
  • Chen W, Wang Y, Qin M, et al. Bacteria-Driven Hypoxia Targeting for Combined Biotherapy and Photothermal Therapy. ACS Nano. 2018;12(6):5995–6005. doi:10.1021/acsnano.8b02235
  • Gujrati V, Prakash J, Malekzadeh-Najafabadi J, et al. Bioengineered bacterial vesicles as biological nano-heaters for optoacoustic imaging. Nat Commun. 2019;10(1):1–10. doi:10.1038/s41467-019-09034-y
  • Chen QW, Liu XH, Fan JX, et al. Self-Mineralized Photothermal Bacteria Hybridizing with Mitochondria-Targeted Metal–Organic Frameworks for Augmenting Photothermal Tumor Therapy. Adv Funct Mater. 2020;30. doi:10.1002/adfm.201909806
  • Zhuang Q, Xu J, Deng D, et al. Bacteria-derived membrane vesicles to advance targeted photothermal tumor ablation. Biomaterials. 2021;268:120550. doi:10.1016/j.biomaterials.2020.120550
  • Zheng DW, Chen Y, Li ZH, et al. Optically-controlled bacterial metabolite for cancer therapy. Nat Commun. 2018;9(1):1–12. doi:10.1038/s41467-018-03233-9
  • Luo Y, Xu D, Gao X, et al. Nanoparticles conjugated with bacteria targeting tumors for precision imaging and therapy. Biochem Biophys Res Commun. 2019;514(4):1147–1153. doi:10.1016/j.bbrc.2019.05.074
  • Wang H, Chen T, Wan L, et al. Attenuated Salmonella engineered with an apoptosis-inducing factor (AIF) eukaryotic expressing system enhances its anti-tumor effect in melanoma in vitro and in vivo. Appl Microbiol Biotechnol. 2020;104(8):3517–3528. doi:10.1007/s00253-020-10485-3
  • Mateos-Chávez AA, Muñoz-López P, Becerra-Báez EI, et al. Live Attenuated Salmonella enterica Expressing and Releasing Cell-Permeable Bax BH3 Peptide Through the MisL Autotransporter System Elicits Antitumor Activity in a Murine Xenograft Model of Human B Non-hodgkin’s Lymphoma. Front Immunol. 2019;10:1–22. doi:10.3389/fimmu.2019.02562
  • Samadi M, Majidzadeh-a K, Salehi M, et al. Engineered hypoxia-responding Escherichia coli carrying cardiac peptide genes, suppresses tumor growth, angiogenesis and metastasis in vivo. J Biol Eng. 2021;2:1–15.
  • Huang W, Shu C, Hua L, et al. Modified bacterial outer membrane vesicles induce autoantibodies for tumor therapy. Acta Biomater. 2020;108:300–312. doi:10.1016/j.actbio.2020.03.030
  • Swofford CA, Van Dessel N, Forbes NS. Quorum-sensing Salmonella selectively trigger protein expression within tumors. Proc Natl Acad Sci USA. 2015;112(11):3457–3462. doi:10.1073/pnas.1414558112
  • Chowdhury S, Castro S, Coker C, Hinchliffe TE, Arpaia N, Danino T. Programmable Bacteria Induce Durable Tumor Regression and Systemic Antitumor Immunity. Nat Med. 2019;25(7):1057–1063. doi:10.1038/s41591-019-0498-z
  • Yaghoubi A, Khazaei M, Jalili S, et al. Bacteria as a Double-Action Sword in Cancer. Biochim Biophys Acta Rev Cancer. 2020;1874:188388.
  • Li J, Zakariah M, Malik A, et al. Analysis of Salmonella Typhimurium Protein-Targeting in the Nucleus of Host Cells and the Implications in Colon Cancer: an in-Silico Approach. Infect Drug Resist. 2020;13:2433–2442.
  • Shi Y, Zheng W, Yang K. Intratumoral accumulation of gut microbiota facilitates CD47-based immunotherapy via STING signaling. J Exp Med. 2020;217(5):e20192282. doi:10.1084/jem.20192282
  • Lee SH, Cho SY, Yoon Y, et al. Bifidobacterium bifidum strains synergize with immune checkpoint inhibitors to reduce tumour burden in mice. Nat Microbiol. 2021;6(3):277–288. doi:10.1038/s41564-020-00831-6
  • Xie S, Zhang P, Zhang Z, et al. Bacterial navigation for tumor targeting and photothermally-triggered bacterial ghost transformation for spatiotemporal drug release. Acta Biomater. 2021;131:172–184. doi:10.1016/j.actbio.2021.06.030
  • 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. doi:10.1200/JCO.2002.20.1.142
  • Gniadek TJ, Augustin L, Schottel J, et al. A Phase I, dose escalation, single dose trial of oral attenuated salmonella typhimurium containing human IL-2 in patients with metastatic gastrointestinal cancers. J Immunother. 2020;43(7):217–221. doi:10.1097/CJI.0000000000000325
  • Le DT, Brockstedt DG, Nir-Paz R, et al. A Live-attenuated Listeria Vaccine (ANZ-100) and a Live- attenuated Listeria Vaccine Expressing Mesothelin (CRS-207) for Advanced Cancers: Phase 1 Studies of Safety and Immune Induction. Clin Cancer Res. 2012;18:858–868.
  • Le DT, Wang-Gillam A, Picozzi V, 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(12):1325–1333. doi:10.1200/JCO.2014.57.4244
  • Le DT, Picozzi VJ, Ko AH, et al. Results from a Phase IIb, Randomized, Multicenter Study of GVAX Pancreas and CRS-207 Compared with Chemotherapy in Adults with Previously Treated Metastatic Pancreatic Adenocarcinoma (ECLIPSE Study). Clin Cancer Res. 2019;25(18):5493–5502. doi:10.1158/1078-0432.CCR-18-2992
  • Hassan R, Alley E, Kindler H, et al. Clinical Response of Live-Attenuated, Listeria monocytogenes Expressing Mesothelin (CRS-207) with Chemotherapy in Patients with Malignant Pleural Mesothelioma. Clin Cancer Res. 2019;25(19):5787–5798. doi:10.1158/1078-0432.CCR-19-0070
  • Karbach J, Neumann A, Brand K, et al. Phase I Clinical Trial of Mixed Bacterial Vaccine (Coley’s Toxins) in Patients with NY-ESO-1 Expressing Cancers: immunological Effects and Clinical ActivityEffects of Mixed Bacterial Vaccine. Clin Cancer Res. 2012;18(19):5449–5459. doi:10.1158/1078-0432.CCR-12-1116
  • Steinberg GD, Shore ND, Karsh LI. Immune response results from vesigenurtacel-l (HS-410) in combination with BCG from a randomized phase 2 trial in patients with non-muscle invasive bladder cancer (NMIBC). J Clin Oncol. 2017;35(15_suppl):4531. doi:10.1200/JCO.2017.35.15_suppl.4531
  • Drake CG, Pachynski RK, Subudhi SK, et al. Safety and preliminary immunogenicity of JNJ-64041809, a live-attenuated, double-deleted Listeria monocytogenes-based immunotherapy, in metastatic castration-resistant prostate cancer. Prostate Cancer Prostatic Dis. 2022;25(2):219–228. doi:10.1038/s41391-021-00402-8
  • Janku F, Zhang HH, Pezeshki A, et al. Intratumoral Injection of Clostridium novyi-NT Spores in Patients with Treatment-refractory Advanced Solid Tumors. Clin Cancer Res. 2021;27(1):96–106. doi:10.1158/1078-0432.CCR-20-2065
  • Lucca I, Derré L, Cesson V, et al. Intravesical Ty21a Treatment of Non-muscle-invasive Bladder Cancer Shows a Good Safety Profile. Eur Urol Open Sci. 2022;45:55–58. doi:10.1016/j.euros.2022.09.004
  • Zhao AZ, Li F, Mai J, et al. Effects of oncolytic bacteria, SGN1, against a broad spectrum of malignancies in pre-clinical and clinical studies. J Clin Oncol. 2023;41(16_suppl):e15184. doi:10.1200/JCO.2023.41.16_suppl.e15184
  • Liu C, Han Y, Kankala R, Wang S, Chen A. Subcellular Performance of Nanoparticles in Cancer Therapy. Int J Nanomed. 2020;15:675–704. doi:10.2147/IJN.S226186
  • Forbes NS, Coffin RS, Deng L, et al. White paper on microbial anti-cancer therapy and prevention. J Immunother Cancer. 2018;6(1):1–24. doi:10.1186/s40425-018-0381-3
  • Gurbatri CR, Lia I, Vincent R, et al. Engineered probiotics for local tumor delivery of checkpoint blockade nanobodies. Sci Transl Med. 2020;12(530). doi:10.1126/scitranslmed.aax0876
  • Kim OY, Dinh NTH, Park HT, Choi SJ, Hong K, Gho YS. Bacterial protoplast-derived nanovesicles for tumor targeted delivery of chemotherapeutics. Biomaterials. 2017;113:68–79. doi:10.1016/j.biomaterials.2016.10.037
  • Aly RG, El-Enbaawy MI, Abd El-Rahman SS, Ata NS. Antineoplastic activity of Salmonella Typhimurium outer membrane nanovesicles. Exp Cell Res. 2021;399(1):112423. doi:10.1016/j.yexcr.2020.112423
  • Gao J, Wang S, Dong X, Wang Z. RGD-expressed bacterial membrane-derived nanovesicles enhance cancer therapy via multiple tumorous targeting. Theranostics. 2021;11(7):3301–3316. doi:10.7150/thno.51988
  • Kaczmarek K, Więckiewicz J, Węglarczyk K, Siedlar M, Baran J. The anti-tumor effect of Lactococcus lactis bacteria-secreting human soluble trail can be enhanced by metformin both in vitro and in vivo in a mouse model of human colorectal cancer. Cancers. 2021;13(12):1–25.
  • Boucher M, Geffroy F, Prévéral S, et al. Genetically tailored magnetosomes used as MRI probe for molecular imaging of brain tumor. Biomaterials. 2017;121:167–178. doi:10.1016/j.biomaterials.2016.12.013