Exploiting the Powerful Anti-tumor Effects of Salmonella Typhimurium: Systematic Review
Article Sidebar
PDF downloads: 117
XML-PubMed downloads: 10
XML-DOAJ downloads: 9
XML-Crossref downloads: 9
Crossref Citations: 0
Main Article Content
Abstract
Introduction: Salmonella typhimurium (S. typhimurium) has emerged as a promising agent for cancer therapy. This systematic review aims to comprehensively analyze the existing literature regarding the utilization of S. typhimurium as a therapeutic strategy against cancer. The present systematic review aimed to evaluate the current state of knowledge regarding the anti-tumor properties of S. typhimurium, encompassing its tumor-targeting mechanisms, impact on tumor growth, modulation of the tumor microenvironment, and potential for combination therapies.
Materials and methods: A systematic literature search was conducted across major scientific databases, including PubMed, Web of Science, and Scopus, using predefined search terms. Studies published between 2000 and 2023 were included if they investigated the anti-tumor effects of S. typhimurium in vivo. Studies were independently screened, selected, and evaluated for quality by two reviewers.
Results: The systematic review identified 152 relevant studies that met the inclusion criteria. These studies collectively demonstrated the ability of S. typhimurium to selectively target and colonize tumors, resulting in significant tumor growth inhibition in various cancer types. Mechanistic insights revealed that S. typhimurium can induce direct cytotoxicity, modulate the tumor microenvironment, and activate anti-tumor immune responses. Additionally, studies highlighted the potential of combining S. typhimurium with conventional therapies or immune checkpoint inhibitors to enhance therapeutic efficacy.
Conclusion: This systematic review underscores the promising potential of S. typhimurium as a novel and multifaceted approach to cancer therapy. The accumulated evidence suggests that S. Typhimurium possesses inherent tumor-targeting capabilities, exerts direct anti-tumor effects, and can synergize with other treatment modalities.
Article Details
This work is licensed under a Creative Commons Attribution 4.0 International License.
References
Aganja RP, Sivasankar C, Senevirathne A and Lee JH. Salmonella as a Promising Curative Tool against Cancer. Pharmaceutics. 2022; 14(10). DOI: https://doi.org/10.3390/pharmaceutics14102100
Minchinton AI and Tannock IF. Drug penetration in solid tumours. Nat Rev Ca. 2006; 6(8): 583-592. DOI: https://doi.org/10.1038/nrc1893
St Jean AT, Zhang M and Forbes NS. Bacterial therapies: completing the cancer treatment toolbox. Curr Opin Biotechnol. 2008; 19(5): 511-517. DOI: https://doi.org/10.1016/j.copbio.2008.08.004
Keung EZ, Fairweather M and Raut CP. Surgical Management of Metastatic Disease. Surg Clin North Am. 2016; 96(5): 1175-1192. DOI: https://doi.org/10.1016/j.suc.2016.05.010
Dutt S, Ahmed MM, Loo BW Jr. and Strober S. Novel Radiation Therapy Paradigms and Immunomodulation: Heresies and Hope. Semin Radiat Oncol. 2020; 30(2): 194-200. DOI: https://doi.org/10.1016/j.semradonc.2019.12.006
Kocakavuk E, Anderson KJ, Varn FS, Johnson KC, Amin SB, Sulman EP, Lolkema MP, Barthel FP and Vehaak RGW. Radiotherapy is associated with a deletion signature that contributes to poor outcomes in patients with cancer. Nat Genet. 2021; 53(7): 1088-1096. DOI: https://doi.org/10.1038/s41588-021-00874-3
Saeed M, Sadr S, Gharib A, Lotfalizadeh N, Hajjafari A, Ahmadi Simab P and Borji H. Phytosomes: A Promising Nanocarrier for Enhanced Delivery of Herbal Compounds in Cancer Therapy. J Lab Anim Res. 2022; 1(1): 26-32. DOI: https://doi.org/10.58803/jlar.v1i1.8
Jing X, Yang F, Shao C, Wei K, Xie M, Shen H and Shu Y. Role of hypoxia in cancer therapy by regulating the tumor microenvironment. Mol Can. 2019; 18(1): 157. DOI: https://doi.org/10.1186/s12943-019-1089-9
Rohwer N and Cramer T. Hypoxia-mediated drug resistance: novel insights on the functional interaction of HIFs and cell death pathways. Drug Resist Updat. 2011; 14(3): 191-201. DOI: https://doi.org/10.1016/j.drup.2011.03.001
Asouli A, Sadr S, Mohebalian H and Borji H. Anti-Tumor Effect of Protoscolex Hydatid Cyst Somatic Antigen on Inhibition Cell Growth of K562. Acta Parasitol. 2023; 68(2): 385-392. DOI: https://doi.org/10.1007/s11686-023-00680-3
Sadr S, Yousefsani Z, Ahmadi Simab P, Jafari Rahbar Alizadeh A, Lotfalizadeh N and Borji H. Trichinella spiralis as a potential antitumor agent: An update. World Vet J. 2023; 13(1): 65-74. DOI: https://doi.org/10.54203/scil.2023.wvj7
Sadr S, Ghiassi S, Lotfalizadeh N, Simab PA, Hajjafari A and Borji H. Antitumor mechanisms of molecules secreted by Trypanosoma cruzi in colon and breast cancer: A review. Anticancer Agt Med Chem. 2023; 23(15): 1710-1721 DOI: https://doi.org/10.2174/1871520623666230529141544
Asouli A, Sadr S, Mohebalian H and Borji H. Anti-Tumor Effect of Protoscolex Hydatid Cyst Somatic Antigen on Inhibition Cell Growth of K562. Acta Parasit. 2023; 68: 385–392. DOI: https://doi.org/10.1007/s11686-023-00680-3
Sadr S and Borji H. Echinococcus granulosus as a Promising Therapeutic Agent against Triplenegative Breast Cancer. Curr Cancer Ther Rev. 2023; 19(4): 292-297. DOI: https://doi.org/10.2174/1573394719666230427094247
Dang LH, Bettegowda C, Huso DL, Kinzler KW and Vogelstein B. Combination bacteriolytic therapy for the treatment of experimental tumors. Proc Natl Acad Sci U S A. 2001; 98(26): 15155-15160. DOI: https://doi.org/10.1073/pnas.251543698
Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson MA, Roy SL, Jones JL and Griffin PM. Foodborne illness acquired in the United States--major pathogens. Emerg Infect Dis. 2011; 17(1): 7-15. DOI: https://doi.org/10.3201/eid1701.P11101
Akoachere JF, Tanih NF, Ndip LM and Ndip RN. Phenotypic characterization of Salmonella typhimurium isolates from food-animals and abattoir drains in Buea, Cameroon. J H Popul Nutr. 2009; 27(5): 612-618. DOI: https://doi.org/10.3329/jhpn.v27i5.3637
Liang K, Liu Q, Li P, Luo H, Wang H and Kong Q. Genetically engineered Salmonella Typhimurium: Recent advances in cancer therapy. Can Lett. 2019; 448: 168-181. DOI: https://doi.org/10.1016/j.canlet.2019.01.037
Chen F, Zang Z, Chen Z, Cui L, Chang Z, Ma A, Yin T, Liang R, Han Y, Wu Z, Zheng M, Lui C and Cai L. Nanophotosensitizer-engineered Salmonella bacteria with hypoxia targeting and photothermal-assisted mutual bioaccumulation for solid tumor therapy. Biomaterials. 2019; 214: 119226. DOI: https://doi.org/10.1016/j.biomaterials.2019.119226
Wei MQ, Ellem KA, Dunn P, West MJ, Bai CX and Vogelstein B. Facultative or obligate anaerobic bacteria have the potential for multimodality therapy of solid tumours. Eur J Cancer. 2007; 43(3): 490-496. DOI: https://doi.org/10.1016/j.ejca.2006.10.005
Jalal K, Khan K, Hassam M, Abbas MN, Uddin R, Khusro A, Sahibzade MUK and Gajdács M. Identification of a novel therapeutic target against XDR Salmonella typhi H58 using genomics driven approach followed up by natural products virtual screening. Microorganisms. 2021; 9(12): 2512. DOI: https://doi.org/10.3390/microorganisms9122512
Mi Z, Guo L, Liu P, Qi Y, Feng Z, Liu J, He Z, Yang X, Jiang S, Wu J, Ding J, Zhiu W and Rong P. “Trojan horse” Salmonella enabling tumor homing of silver nanoparticles via neutrophil infiltration for synergistic tumor therapy and enhanced biosafety. Nano Lett. 2020; 21(1): 414-423. DOI: https://doi.org/10.1021/acs.nanolett.0c03811
Zhang Q, Feng Y and Kennedy D. Multidrug-resistant cancer cells and cancer stem cells hijack cellular systems to circumvent systemic therapies, can natural products reverse this? Cell Mol Life Sci. 2017; 74: 777-801. DOI: https://doi.org/10.1007/s00018-016-2362-3
Zheng JH and Min J-J. Targeted cancer therapy using engineered Salmonella typhimurium. Chonnam Med J. 2016; 52(3): 173-184. DOI: https://doi.org/10.4068/cmj.2016.52.3.173
Yong L, Tang S, Yu H, Zhang H, Zhang Y, Wan Y and Cai F. The role of hypoxia-inducible factor-1 alpha in multidrug-resistant breast cancer. Front Oncol. 2022; 12: 964934. DOI: https://doi.org/10.3389/fonc.2022.964934
Aganja RP, Sivasankar C, Senevirathne A and Lee JH. Salmonella as a Promising Curative Tool against Cancer. Pharmaceutics. 2022; 14(10): 2100. DOI: https://doi.org/10.3390/pharmaceutics14102100
Semenov AV, van Overbeek L, Termorshuizen AJ and van Bruggen AH. Influence of aerobic and anaerobic conditions on survival of Escherichia coli O157:H7 and Salmonella enterica serovar Typhimurium in Luria-Bertani broth, farm-yard manure and slurry. J Environ Manage. 2011; 92(3): 780-787. DOI: https://doi.org/10.1016/j.jenvman.2010.10.031
Nguyen VH and Min J-J. Salmonella-mediated cancer therapy: roles and potential. NMMI. 2017; 51: 118-126. DOI: https://doi.org/10.1007/s13139-016-0415-z
Lowerison MR, Huang C, Lucien F, Chen S and Song P. Ultrasound localization microscopy of renal tumor xenografts in chicken embryo is correlated to hypoxia. Sci Rep. 2020; 10(1): 2478. DOI: https://doi.org/10.1038/s41598-020-59338-z
Hayek I, Schatz V, Bogdan C, Jantsch J and Lührmann A. Mechanisms controlling bacterial infection in myeloid cells under hypoxic conditions. Cell Mol Life Sci. 2021; 78: 1887-1907. DOI: https://doi.org/10.1007/s00018-020-03684-8
Viallard C and Larrivee B. Tumor angiogenesis and vascular normalization: alternative therapeutic targets. Angiogenesis. 2017; 20(4): 409-426. DOI: https://doi.org/10.1007/s10456-017-9562-9
Murakami T, Hiroshima Y, Matsuyama R, Homma Y, Hoffman RM and Endo I. Role of the tumor microenvironment in pancreatic cancer. Ann gastroenterol surg. 2019; 3(2): 130-137. DOI: https://doi.org/10.1002/ags3.12225
Camacho EM, Mesa-Pereira B, Medina C, Flores A and Santero E. Engineering Salmonella as intracellular factory for effective killing of tumour cells. Sci Rep. 2016; 6(1): 30591. DOI: https://doi.org/10.1038/srep30591
Liu F, Zhang L, Hoffman RM and Zhao M. Vessel destruction by tumor-targeting Salmonella typhimurium A1-R is enhanced by high tumor vascularity. CC. 2010; 9(22): 4518-4524. DOI: https://doi.org/10.4161/cc.9.22.13744
Das R and Fernandez JG. Biomaterials for mimicking and modelling tumor microenvironment. Microfluidics and Biosensors in Cancer Research: Applications in Cancer Modeling and Theranostics. Microfluidics Biosensors Cancer Res. 2022;139-170. DOI: https://doi.org/10.1007/978-3-031-04039-9_6
Sullivan MR, Danai LV, Lewis CA, Chan SH, Gui DY, Kunchok T, Dennstedt EA, Vander Heiden MG and Muir A. Quantification of microenvironmental metabolites in murine cancers reveals determinants of tumor nutrient availability. Elife. 2019; 16: 8:e44235. DOI: https://doi.org/10.7554/eLife.44235
Pavlova NN, Zhu J and Thompson CB. The hallmarks of cancer metabolism: Still emerging. Cell Metab. 2022; 34(3): 355-377. DOI: https://doi.org/10.1016/j.cmet.2022.01.007
Felgner S, Kocijancic D, Frahm M and Weiss S. Bacteria in cancer therapy: renaissance of an old concept. Int J Microbiol. 2016; 8451728. DOI: https://doi.org/10.1155/2016/8451728
Jawalagatti V, Kirthika P and Lee JH. Targeting primary and metastatic tumor growth in an aggressive breast cancer by engineered tryptophan auxotrophic Salmonella Typhimurium. Mol Ther Oncolytics. 2022; 25: 350-363. DOI: https://doi.org/10.1016/j.omto.2022.05.004
Nguyen VH and Min JJ. Salmonella-Mediated Cancer Therapy: Roles and Potential. Nucl Med Mol Imaging. 2017; 51(2): 118-126. DOI: https://doi.org/10.1007/s13139-016-0415-z
Ganai S, Arenas RB, Sauer JP, Bentley B and Forbes NS. In tumors Salmonella migrate away from vasculature toward the transition zone and induce apoptosis. Cancer Gene Ther. 2011; 18(7): 457-466. DOI: https://doi.org/10.1038/cgt.2011.10
Toley BJ and Forbes NS. Motility is critical for effective distribution and accumulation of bacteria in tumor tissue. Integr Biol (Camb). 2012; 4(2): 165-176. DOI: https://doi.org/10.1039/c2ib00091a
Stritzker J, Weibel S, Seubert C, Gotz A, Tresch A, van Rooijen N, Oelschleager TA, Hill PJ, Gentschev I and Szalay AA. Enterobacterial tumor colonization in mice depends on bacterial metabolism and macrophages but is independent of chemotaxis and motility. Int J Med Microbiol. 2010; 300(7): 449-456. DOI: https://doi.org/10.1016/j.ijmm.2010.02.004
Zhang X, Yu D, Wu D, Gao X, Shao F, Zhao M, Wang J, Ma J, Wang W, Qin X, Chen Y, Xia P and Wang S. Tissue-resident Lachnospiraceae family bacteria protect against colorectal carcinogenesis by promoting tumor immune surveillance. Cell Host Microbe. 2023; 31(3): 418-432 e8. DOI: https://doi.org/10.1016/j.chom.2023.01.013
Mi Z, Feng ZC, Li C, Yang X, Ma MT and Rong PF. Salmonella-Mediated Cancer Therapy: An Innovative Therapeutic Strategy. J Cancer. 2019; 10(20): 4765-4776. DOI: https://doi.org/10.7150/jca.32650
Badie F, Ghandali M, Tabatabaei SA, Safari M, Khorshidi A, Shayestehpour M, Mahjoubin M, Morshedi K, Jalili A, Tajiknia V, Hamblin MR and Mirzaei H. Use of Salmonella Bacteria in Cancer Therapy: Direct, Drug Delivery and Combination Approaches. Front Oncol. 2021; 11: 624759. DOI: https://doi.org/10.3389/fonc.2021.624759
Hoffman RM and Zhao M. Methods for the development of tumor-targeting bacteria. Expert OPIN. 2014; 9(7): 741-750. DOI: https://doi.org/10.1517/17460441.2014.916270
Chang WW and Lee CH. Salmonella as an innovative therapeutic antitumor agent. Int J Mol Sci. 2014; 15(8): 14546-14554. DOI: https://doi.org/10.3390/ijms150814546
Lee C, Lin S, Liu J, Chang W, Hsieh J and Wang W. Salmonella induce autophagy in melanoma by the downregulation of AKT/mTOR pathway. Gene Ther. 2014; 21(3): 309-316. DOI: https://doi.org/10.1038/gt.2013.86
Lee CH, Lin ST, Liu JJ, Chang WW, Hsieh JL and Wang WK. Salmonella induce autophagy in melanoma by the downregulation of AKT/mTOR pathway. Gene Ther. 2014; 21(3): 309-316. DOI: https://doi.org/10.1038/gt.2013.86
Tsao YT, Kuo CY, Cheng SP and Lee CH. Downregulations of AKT/mTOR Signaling Pathway for Salmonella-Mediated Suppression of Matrix Metalloproteinases-9 Expression in Mouse Tumor Models. Int J Mol Sci. 2018; 19(6): 1630. DOI: https://doi.org/10.3390/ijms19061630
Jiang X, Wang J, Deng X, Xiong F, Zhang S, Gong Z, Li X, Cao K, Deng H, He Y, Liao K, Xiang B, Zhou M, Guo C, Zeng Z, Li G, Li X and Xiong W. The role of microenvironment in tumor angiogenesis. J Exp Clin Cancer Res. 2020; 39(1): 1-19. DOI: https://doi.org/10.1186/s13046-020-01709-5
Tu DG, Chang WW, Lin ST, Kuo CY, Tsao YT and Lee CH. Salmonella inhibits tumor angiogenesis by downregulation of vascular endothelial growth factor. Oncotarget. 2016; 7(25): 37513-37523. DOI: https://doi.org/10.18632/oncotarget.7038
Wang WK, Chen MC, Leong HF, Kuo YL, Kuo CY and Lee CH. Connexin 43 suppresses tumor angiogenesis by down-regulation of vascular endothelial growth factor via hypoxic-induced factor-1alpha. Int J Mol Sci. 2014; 16(1): 439-451. DOI: https://doi.org/10.3390/ijms16010439
Kiyuna T, Tome Y, Uehara F, Murakami T, Zhang Y, Zhao M, Kanaya F and Hoffman RM. Tumor-targeting Salmonella typhimurium A1-R Inhibits Osteosarcoma Angiogenesis in the In Vivo Gelfoam(R) Assay Visualized by Color-coded Imaging. Anticancer Res. 2018; 38(1): 159-164. DOI: https://doi.org/10.21873/anticanres.12203
Li S, Yue H, Wang S, Li X, Wang X, Guo P, Ma G and Wei W. Advances of bacteria-based delivery systems for modulating tumor microenvironment. Adv Drug Deliv Rev. 2022; 188: 114444. DOI: https://doi.org/10.1016/j.addr.2022.114444
Kaimala S, Al-Sbiei A, Cabral-Marques O, Fernandez-Cabezudo MJ and Al-Ramadi BK. Attenuated Bacteria as Immunotherapeutic Tools for Cancer Treatment. Front Oncol. 2018; 8: 136. DOI: https://doi.org/10.3389/fonc.2018.00136
Lee CH, Hsieh JL, Wu CL, Hsu HC and Shiau AL. B cells are required for tumor-targeting Salmonella in host. Appl Microbiol Biotechnol. 2011; 92(6): 1251-1260. DOI: https://doi.org/10.1007/s00253-011-3386-0
Grille S, Moreno M, Bascuas T, Marques JM, Munoz N, Lens D and Chabalgoity JA. Salmonella enterica serovar Typhimurium immunotherapy for B-cell lymphoma induces broad anti-tumour immunity with therapeutic effect. Immunology. 2014; 143(3): 428-437. DOI: https://doi.org/10.1111/imm.12320
Galdiero MR, Bonavita E, Barajon I, Garlanda C, Mantovani A and Jaillon S. Tumor associated macrophages and neutrophils in cancer. Immunobiol. 2013; 218(11): 1402-1410. DOI: https://doi.org/10.1016/j.imbio.2013.06.003
Duan B, Shao L, Liu R, Msuthwana P, Hu J and Wang C. Lactobacillus rhamnosus GG defense against Salmonella enterica serovar Typhimurium infection through modulation of M1 macrophage polarization. Microb Pathog. 2021; 156: 104939. DOI: https://doi.org/10.1016/j.micpath.2021.104939
Mantovani A, Sica A, Sozzani S, Allavena P, Vecchi A and Locati M. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 2004; 25(12): 677-686. DOI: https://doi.org/10.1016/j.it.2004.09.015
Kaimala S, Mohamed YA, Nader N, Issac J, Elkord E, Chouaib S, Fernandez-Cabezudo MJ and al-Ramadi BK. Salmonella-mediated tumor regression involves targeting of tumor myeloid suppressor cells causing a shift to M1-like phenotype and reduction in suppressive capacity. Cancer Immunology, IO. 2014; 63: 587-399. DOI: https://doi.org/10.1007/s00262-014-1543-x
Josefowicz SZ, Lu LF and Rudensky AY. Regulatory T cells: mechanisms of differentiation and function. Annu Rev Immunol. 2012; 30: 531-564. DOI: https://doi.org/10.1146/annurev.immunol.25.022106.141623
Hong EH, Chang SY, Lee BR, Pyun AR, Kim JW, Kweon MN and Ko HJ. Intratumoral injection of attenuated Salmonella vaccine can induce tumor microenvironmental shift from immune suppressive to immunogenic. Vaccine. 2013; 31(10): 1377-1384. DOI: https://doi.org/10.1016/j.vaccine.2013.01.006
Liu T and Chopra AK. An enteric pathogen Salmonella enterica serovar Typhimurium suppresses tumor growth by downregulating CD44high and CD4T regulatory (Treg) cell expression in mice: the critical role of lipopolysaccharide and Braun lipoprotein in modulating tumor growth. Cancer Gene Ther. 2010; 17(2): 97-108. DOI: https://doi.org/10.1038/cgt.2009.58
Varela-Vazquez A, Guitian-Caamano A, Carpintero-Fernandez P, Fonseca E, Sayedyahossein S, Aasen T, Penuela S and Mayán MD. Emerging functions and clinical prospects of connexins and pannexins in melanoma. Biochim Biophys Acta Rev Cancer. 2020; 1874(1): 188380. DOI: https://doi.org/10.1016/j.bbcan.2020.188380
Saccheri F, Pozzi C, Avogadri F, Barozzi S, Faretta M, Fusi P and Rescingo M. Bacteria-induced gap junctions in tumors favor antigen cross-presentation and antitumor immunity. Sci Transl Med. 2010; 2(44): 44-57. DOI: https://doi.org/10.1126/scitranslmed.3000739
DeNardo DG and Ruffell B. Macrophages as regulators of tumour immunity and immunotherapy. Nat Rev Immunol. 2019; 19(6): 369-382. DOI: https://doi.org/10.1038/s41577-019-0127-6
Biswas SK, Gangi L, Paul S, Schioppa T, Saccani A, Sironi M, Bottazzi B, Doni A, Vincenzo B, Pasqualini F, Vago L, Nebuloni M, Mantovani A and Sica A. A distinct and unique transcriptional program expressed by tumor-associated macrophages (defective NF-kappaB and enhanced IRF-3/STAT1 activation). Blood. 2006; 107(5): 2112-2122. DOI: https://doi.org/10.1182/blood-2005-01-0428
Boutilier AJ and Elsawa SF. Macrophage Polarization States in the Tumor Microenvironment. Int J Mol Sci. 2021; 22(13): 6995. DOI: https://doi.org/10.3390/ijms22136995
Jorgovanovic D, Song M, Wang L and Zhang Y. Roles of IFN-γ in tumor progression and regression: a review. Biomark Res. 2020; 8: 1-16. DOI: https://doi.org/10.1186/s40364-020-00228-x
Chen G, Xiong W, Gu Z, Gao Y, Hou J, Long L, WangH, Asrorov AM, Muhitdinov B, Xu Q and Huang Y. Mannosylated engineered trichosanthin-legumain protein vaccine hydrogel for breast cancer immunotherapy. Int J Biol Macromol. 2022; 223: 1485-1494. DOI: https://doi.org/10.1016/j.ijbiomac.2022.11.045
Luo Y, Zhou H, Krueger J, Kaplan C, Lee SH, Dolman C, Marowitz D, Wu W, Liu C, Reisfeld RA and Xiang R. Targeting tumor-associated macrophages as a novel strategy against breast cancer. J Clin Invest. 2006; 116(8): 2132-2141. DOI: https://doi.org/10.1172/JCI27648
Kong Q and Zhang Z. Cancer-associated pyroptosis: A new license to kill tumor. Front Immunol. 2023; 14: 1082165. DOI: https://doi.org/10.3389/fimmu.2023.1082165
Deng W, Marshall NC, Rowland JL, McCoy JM, Worrall LJ, Santos AS, Strynadka NCJ and Finlay BB. Assembly, structure, function and regulation of type III secretion systems. Nat Rev Microbiol. 2017; 15(6): 323-337. DOI: https://doi.org/10.1038/nrmicro.2017.20
Sorenson BS, Banton KL, Frykman NL, Leonard AS and Saltzman DA. Attenuated Salmonella typhimurium with IL-2 gene reduces pulmonary metastases in murine osteosarcoma. Clin Orthop Relat Res. 2008; 466(6): 1285-1291. DOI: https://doi.org/10.1007/s11999-008-0243-2
Loeffler M, Le'Negrate G, Krajewska M and Reed JC. IL-18-producing Salmonella inhibit tumor growth. Cancer Gene Ther. 2008; 15(12): 787-794. DOI: https://doi.org/10.1038/cgt.2008.48
Ganai S, Arenas RB and Forbes NS. Tumour-targeted delivery of TRAIL using Salmonella typhimurium enhances breast cancer survival in mice. Br J Cancer. 2009; 101(10): 1683-1691. DOI: https://doi.org/10.1038/sj.bjc.6605403
Loeffler M, Le'Negrate G, Krajewska M and Reed JC. Inhibition of tumor growth using salmonella expressing Fas ligand. J Natl Cancer Inst. 2008; 100(15): 1113-1116. DOI: https://doi.org/10.1093/jnci/djn205
Loeffler M, Le’Negrate G, Krajewska M and Reed JC. Inhibition of tumor growth using salmonella expressing Fas ligand. J Natl Cancer Inst. 2008; 100(15): 1113-1116. DOI: https://doi.org/10.1093/jnci/djn205
Chen W, Zhu Y, Zhang Z and Sun X. Advances in Salmonella Typhimurium-based drug delivery system for cancer therapy. Adv Drug Deliv. 2022; 185: 114295. DOI: https://doi.org/10.1016/j.addr.2022.114295
Nallar SC and Xu D-Q, Kalvakolanu DV. Bacteria and genetically modified bacteria as cancer therapeutics: Current advances and challenges. Cytokine. 2017; 89: 160-172. DOI: https://doi.org/10.1016/j.cyto.2016.01.002
Yang M, Yang F, Chen W, Liu S, Qiu L and Chen J. Bacteria-mediated cancer therapies: opportunities and challenges. Biomater Sci. 2021; 9(17): 5732-5744. DOI: https://doi.org/10.1039/D1BM00634G
Ganai S, Arenas R and Forbes N. Tumour-targeted delivery of TRAIL using Salmonella typhimurium enhances breast cancer survival in mice. Br J Cancer. 2009; 101(10): 1683-1691. DOI: https://doi.org/10.1038/sj.bjc.6605403
Broadway KM and Scharf BE. Salmonella typhimurium as an anticancer therapy: recent advances and perspectives. Curr Clin Microbiol. 2019; 6: 225-239. DOI: https://doi.org/10.1007/s40588-019-00132-5
Chen J, Yang B, Cheng X, Qiao Y, Tang B, Chen G, Wei J, Liu X, Cheng W, Du P, Huang X, Jiang W Hu Q, Hu Y, Li J and Hua Z. Salmonella-mediated tumor-targeting TRAIL gene therapy significantly suppresses melanoma growth in mouse model. Cancer Sci. 2012; 103(2): 325-333. DOI: https://doi.org/10.1111/j.1349-7006.2011.02147.x
Kim SI, Kim S, Kim E, Hwang SY and Yoon H. Secretion of Salmonella pathogenicity island 1-encoded type III secretion system effectors by outer membrane vesicles in Salmonella enterica serovar typhimurium. Front Microbiol. 2018; 9: 2810. DOI: https://doi.org/10.3389/fmicb.2018.02810
Galan JE, Wolf-Watz H. Protein delivery into eukaryotic cells by type III secretion machines. Nature. 2006; 444(7119): 567-573. DOI: https://doi.org/10.1038/nature05272
Lou L, Zhang P, Piao R and Wang Y. Salmonella pathogenicity island 1 (SPI-1) and its complex regulatory network. Front Cell Infect Microbiol. 2019; 9: 270. DOI: https://doi.org/10.3389/fcimb.2019.00270
Liss V, Swart AL, Kehl A, Hermanns N, Zhang Y, Chikkaballi D, Böhles N, Deiwick J and Hensel M. Salmonella enterica Remodels the Host Cell Endosomal System for Efficient Intravacuolar Nutrition. Cell Host Microbe. 2017; 21(3): 390-402. DOI: https://doi.org/10.1016/j.chom.2017.02.005
Rajashekar R, Liebl D, Seitz A and Hensel M. Dynamic remodeling of the endosomal system during formation of Salmonella-induced filaments by intracellular Salmonella enterica. Traffic. 2008; 9(12): 2100-2116. DOI: https://doi.org/10.1111/j.1600-0854.2008.00821.x
Zhang K, Riba A, Nietschke M, Torow N, Repnik U, Pütz A, Fulde M, Dupont A, Hensel M and Hornef M. Minimal SPI1-T3SS effector requirement for Salmonella enterocyte invasion and intracellular proliferation in vivo. PLoS Patho. 2018; 14(3): e1006925. DOI: https://doi.org/10.1371/journal.ppat.1006925
Lin H-H, Chen H-L, Weng C-C, Janapatla RP, Chen C-L and Chiu C-H. Activation of apoptosis by Salmonella pathogenicity island-1 effectors through both intrinsic and extrinsic pathways in Salmonella-infected macrophages. Journal of Microbiology, Immun Infect. 2021; 54(4): 616-626. DOI: https://doi.org/10.1016/j.jmii.2020.02.008
Al-Saafeen BH, Fernandez-Cabezudo MJ and Al-Ramadi BK. Integration of Salmonella into combination cancer therapy. Cancers. 2021; 13(13): 3228. DOI: https://doi.org/10.3390/cancers13133228
Mercado-Lubo R, Zhang Y, Zhao L, Rossi K, Wu X, Zou Y, Castillo A, Leonard J, Bortell R, Greiner DL, Shultz LD, Han G and McCormick B. A Salmonella nanoparticle mimic overcomes multidrug resistance in tumours. Nat Commun. 2016; 7: 12225. DOI: https://doi.org/10.1038/ncomms12225
Siccardi D, Mumy KL, Wall DM, Bien JD and McCormick BA. Salmonella enterica serovar Typhimurium modulates P-glycoprotein in the intestinal epithelium. Am J Physiol Gastrointest Liver Physiol. 2008; 294(6): G1392-1400. DOI: https://doi.org/10.1152/ajpgi.00599.2007
Sundaram B and Kanneganti T-D. Advances in understanding activation and function of the NLRC4 inflammasome. Int J Mol Sci. 2021; 22(3): 1048. DOI: https://doi.org/10.3390/ijms22031048
Yang J, Liu Z and Xiao TS. Post-translational regulation of inflammasomes. Cell mol immun. 2017; 14(1): 65-79. DOI: https://doi.org/10.1038/cmi.2016.29
Sundaram B and Kanneganti TD. Advances in Understanding Activation and Function of the NLRC4 Inflammasome. Int J Mol Sci. 2021; 22(3): 1048. DOI: https://doi.org/10.3390/ijms22031048
Christgen S, Zheng M, Kesavardhana S, Karki R, Malireddi RKS, Banoth B, Place DE, Briard B, Sharma BR, Tuladhar S, Samir P, Burton A and Kanneganti TD. Identification of the PANoptosome: A Molecular Platform Triggering Pyroptosis, Apoptosis, and Necroptosis (PANoptosis). Front Cell Infect Microbiol. 2020; 10: 237. DOI: https://doi.org/10.3389/fcimb.2020.00237
Liu X, Zhang Z, Ruan J, Pan Y, Magupalli VG, Wu H and Lieberman J. Inflammasome-activated gasdermin D causes pyroptosis by forming membrane pores. Nature. 2016; 535(7610): 153-158. DOI: https://doi.org/10.1038/nature18629
Raymond B, Young JC, Pallett M, Endres RG, Clements A and Frankel G. Subversion of trafficking, apoptosis, and innate immunity by type III secretion system effectors. Trends Microbiol. 2013; 21(8): 430-441. DOI: https://doi.org/10.1016/j.tim.2013.06.008
Nishikawa H, Sato E, Briones G, Chen LM, Matsuo M, Nagata Y, Ritter G, Jäger E, Nomura H, Konda S, Tawara I, Kato T, Shiku H, Old LJ, Galán JE and Gnjatic S. In vivo antigen delivery by a Salmonella typhimurium type III secretion system for therapeutic cancer vaccines. J Clin Invest. 2006; 116(7): 1946-1954. DOI: https://doi.org/10.1172/JCI28045
Roider E, Jellbauer S, Kohn B, Berchtold C, Partilla M, Busch DH, Rüssmann H and Panthel K. Invasion and destruction of a murine fibrosarcoma by Salmonella-induced effector CD8 T cells as a therapeutic intervention against cancer. Cancer Immunol Immunother. 2011; 60(3): 371-380. DOI: https://doi.org/10.1007/s00262-010-0950-x
Xiong G, Husseiny MI, Song L, Erdreich-Epstein A, Shackleford GM, Seeger RC, Jäckel D, Hensel M and Metelista LS. Novel cancer vaccine based on genes of Salmonella pathogenicity island 2. Int J Cancer. 2010; 126(11): 2622-2634. DOI: https://doi.org/10.1002/ijc.24957
Panthel K, Meinel KM, Sevil Domenech VE, Trulzsch K and Russmann H. Salmonella type III-mediated heterologous antigen delivery: a versatile oral vaccination strategy to induce cellular immunity against infectious agents and tumors. Int J Med Microbiol. 2008; 298(1-2): 99-103. DOI: https://doi.org/10.1016/j.ijmm.2007.07.002
Liang K, Liu Q, Li P, Luo H, Wang H and Kong Q. Genetically engineered Salmonella Typhimurium: Recent advances in cancer therapy. Cancer lett. 2019; 448: 168-181. DOI: https://doi.org/10.1016/j.canlet.2019.01.037
Kung Y-J, Lam B, Tseng S-H, MacDonald A, Tu H-F, Wang S, Lin J, Tsai YC and Hung CF. Localization of Salmonella and albumin-IL-2 to the tumor microenvironment augments anticancer T cell immunity. J Biomed Sci. 2022; 29(1): 57. DOI: https://doi.org/10.1186/s12929-022-00841-y
Sun X, Ni N, Ma Y, Wang Y and Leong DT. Retooling cancer nanotherapeutics’ entry into tumors to alleviate tumoral hypoxia. Small. 2020; 16(41): 2003000. DOI: https://doi.org/10.1002/smll.202003000
Frutos-Grilo E, Marsal M, Irazoki O, Barbé J and Campoy S. The interaction of RecA with both CheA and CheW is required for Chemotaxis. Front Microbiol. 2020; 7(11): 583. DOI: https://doi.org/10.3389/fmicb.2020.00583
Wang L, Li Y, Liu Y, Zuo L, Li Y, Wu S and Huang R. Salmonella spv locus affects type I interferon response and the chemotaxis of neutrophils via suppressing autophagy. Fish Shellfish Immunol. 2019; 87: 721-729. DOI: https://doi.org/10.1016/j.fsi.2019.02.009
Singleton DC, Macann A and Wilson WR. Therapeutic targeting of the hypoxic tumour microenvironment. Nature Rev Clinical Oncology. 2021; 18(12): 751-772. DOI: https://doi.org/10.1038/s41571-021-00539-4
Ma J, Sun X, Wang Y, Chen B, Qian L and Wang Y. Fibroblast-derived CXCL12 regulates PTEN expression and is associated with the proliferation and invasion of colon cancer cells via PI3k/Akt signaling. Cell Commun Signal. 2019; 17(1): 119. DOI: https://doi.org/10.1186/s12964-019-0432-5
Kalia VC, Patel SK, Cho B-K, Wood TK and Lee J-K. Emerging applications of bacteria as antitumor agents. Semin Cancer Biol. Elsevier. 2022; DOI: https://doi.org/10.1016/j.semcancer.2021.05.012
Jimenez-Jimenez C, Moreno VM and Vallet-Regi M. Bacteria-Assisted Transport of Nanomaterials to Improve Drug Delivery in Cancer Therapy. Nanomaterials (Basel). 2022; 12(2): 288. DOI: https://doi.org/10.3390/nano12020288
Guo Y, Chen Y, Liu X, Min JJ, Tan W and Zheng JH. Targeted cancer immunotherapy with genetically engineered oncolytic Salmonella typhimurium. Cancer Lett. 2020; 469: 102-110. DOI: https://doi.org/10.1016/j.canlet.2019.10.033
Dos Santos AMP, Ferrari RG and Conte-Junior CA. Virulence Factors in Salmonella Typhimurium: The Sagacity of a Bacterium. Curr Microbiol. 2019; 76(6): 762-773. DOI: https://doi.org/10.1007/s00284-018-1510-4
Wang W, Xu H, Ye Q, Tao F, Wheeldon I, Yuan A, Hu Y and Wy J. Systemic immune responses to irradiated tumours via the transport of antigens to the tumour periphery by injected flagellate bacteria. Nat Biomed Eng. 2022; 6(1): 44-53. DOI: https://doi.org/10.1038/s41551-021-00834-6
Kiani AA, Elyasi H, Ghoreyshi S, Nouri N, Safarzadeh A and Nafari A. Study on hypoxia-inducible factor and its roles in immune system. Immunol Med. 2021; 44(4): 223-236. DOI: https://doi.org/10.1080/25785826.2021.1910187
Chiu H-M, Chiou W-Y, Hsu W-J, Wu L-H, Yang M-H, Tyan Y-C and Lee C-H. Salmonella alters heparanase expression and reduces tumor metastasis. Int J Med Sci. 2021; 18(13): 2981. DOI: https://doi.org/10.7150/ijms.60281
Leschner S and Weiss S. Salmonella—allies in the fight against cancer. J Mol Med. 2010; 88(8): 763-773. DOI: https://doi.org/10.1007/s00109-010-0636-z
Zhao M, Yang M, Ma H, Li X, Tan X, Li S, Yang Z and Hoffman RM. 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: https://doi.org/10.1158/0008-5472.CAN-06-0716
Nguyen VH, Kim H-S, Ha J-M, Hong Y, Choy HE and Min J-J. Genetically engineered Salmonella typhimurium as an imageable therapeutic probe for cancer. Cancer Res. 2010; 70(1): 18-23. DOI: https://doi.org/10.1158/0008-5472.CAN-09-3453
Zheng JH, Nguyen VH, Jiang S-N, Park S-H, Tan W, Hong SH, Shin MG, Chung J-J, Hong Y, Bom H-S, Choy HE, Lee SE, Rhee JH and Min J-J. Two-step enhanced cancer immunotherapy with engineered Salmonella typhimurium secreting heterologous flagellin. Sci Trans Med. 2017; 9(376): eaak9537. DOI: https://doi.org/10.1126/scitranslmed.aak9537
Al-Ramadi BK, Fernandez-Cabezudo MJ, El-Hasasna H, Al-Salam S, Bashir G and Chouaib S. Potent anti-tumor activity of systemically-administered IL2-expressing Salmonella correlates with decreased angiogenesis and enhanced tumor apoptosis. Clin Immunol. 2009; 130(1): 89-97. DOI: https://doi.org/10.1016/j.clim.2008.08.021
Zhang Y, Tome Y, Suetsugu A, Zhang L, Zhang N, Hoffman RM and Zhao M. Determination of the optimal route of administration of Salmonella typhimurium A1-R to target breast cancer in nude mice. Anticancer Res. 2012; 32(7): 2501-2508.
Li X, Li Y, Wang B, Ji K, Liang Z, Guo B, Hu j, Du Y, Kopecko DJ, Kalvalolanu DV, Zhao X, Xu D and Zhang L. Delivery of the co-expression plasmid pEndo-Si-Stat3 by attenuated Salmonella serovar typhimurium for prostate cancer treatment. J Cancer Res Clin Oncol. 2013; 139(6): 971-980. DOI: https://doi.org/10.1007/s00432-013-1398-0
Schatten H. Immunodiagnostics and immunotherapy possibilities for prostate cancer. Molecular & Diagnostic Imaging in Prostate Cancer: Clin App Treat Strateg. 2018: 185-94. DOI: https://doi.org/10.1007/978-3-319-99286-0_10
Wang C-Z, Kazmierczak RA and Eisenstark A. Strains, mechanism, and perspective: Salmonella-based cancer therapy. Int J Microbiol. 2016; 5678702. DOI: https://doi.org/10.1155/2016/5678702
Pangilinan CR and Lee CH. Salmonella-Based Targeted Cancer Therapy: Updates on A Promising and Innovative Tumor Immunotherapeutic Strategy. Biomed. 2019; 7(2): 36. DOI: https://doi.org/10.3390/biomedicines7020036
Ebrahimzadeh S, Ahangari H, Soleimanian A, Hosseini K, Ebrahimi V, Ghasemnejad T, Razi Soofiyan S, Tarhiz V and Eyvazi S. Colorectal cancer treatment using bacteria: focus on molecular mechanisms. BMC Microbiol. 2021; 21(1): 218. DOI: https://doi.org/10.1186/s12866-021-02274-3
Deng J, Guo Y, Jiang Z, Yang M, Li H and Wang J. Enhancement of ovarian cancer chemotherapy by delivery of multidrug-resistance gene small interfering RNA using tumor targeting Salmonella. J Obstet Gynaecol Res. 2015; 41(4): 615-622. DOI: https://doi.org/10.1111/jog.12598
Fu W, Lan H, Li S, Han X, Gao T and Ren D. Synergistic antitumor efficacy of suicide/ePNP gene and 6-methylpurine 2′-deoxyriboside via Salmonella against murine tumors. Cancer Gene Ther. 2008; 15(7): 474-484. DOI: https://doi.org/10.1038/cgt.2008.19
Phan T, Nguyen VH, D’Alincourt MS, Manuel ER, Kaltcheva T, Tsai W, Blazer BR, Diamond DJ and Melstrom LG. Salmonella-mediated therapy targeting indoleamine 2, 3-dioxygenase 1 (IDO) activates innate immunity and mitigates colorectal cancer growth. Cancer gene Ther. 2020; 27(3-4): 235-245. DOI: https://doi.org/10.1038/s41417-019-0089-7
Pangilinan CR, Wu L-H and Lee C-H. Salmonella Impacts Tumor-Induced Macrophage Polarization, and Inhibits SNAI1-Mediated Metastasis in Melanoma. Cancers. 2021; 13(12): 2894. DOI: https://doi.org/10.3390/cancers13122894
Yoon W, Park YC, Kim J, Chae YS, Byeon JH, Min S-H, Park S, Yoo Y, Park YK and Kim BM. Application of genetically engineered Salmonella typhimurium for interferon-gamma–induced therapy against melanoma. Eur J Cancer. 2017; 70: 48-61. DOI: https://doi.org/10.1016/j.ejca.2016.10.010
Oladejo M, Paulishak W and Wood L. Synergistic potential of immune checkpoint inhibitors and therapeutic cancer vaccines. Semin Cancer Biol. Elsevier. 2022; DOI: https://doi.org/10.1016/j.semcancer.2022.12.003
Chen Y, Liu X, Guo Y, Wang J, Zhang D, Mei Y, Shi J, Tan W and Zheng JH. Genetically engineered oncolytic bacteria as drug delivery systems for targeted cancer theranostics. Acta biomaterialia. 2021; 124: 72-87. DOI: https://doi.org/10.1016/j.actbio.2021.02.006
Zhang Y, Sun X, Wang Q, Xu J, Dong F, Yang S, Yang J, Zhang Z, Qian Y, Chen J, Zhang J, Liu Y, Tao R, Jiang Y, Yang J and Yang S. Multicopy chromosomal integration using CRISPR-associated transposases. ACS Synth Biol. 2020; 9(8): 1998-2008. DOI: https://doi.org/10.1021/acssynbio.0c00073
Zhou S, Gravekamp C, Bermudes D and Liu K. Tumour-targeting bacteria engineered to fight cancer. Nat Rev Cancer. 2018; 18(12): 727-743. DOI: https://doi.org/10.1038/s41568-018-0070-z
Sedighi M, Zahedi Bialvaei A, Hamblin MR, Ohadi E, Asadi A, Halajzadeh M, Lohrasbi V, Mohammadzadeh N, Amiriani T, Krutova M, Amini A and Kousari E. Therapeutic bacteria to combat cancer; current advances, challenges, and opportunities. Cancer Med. 2019; 8(6): 3167-3181. DOI: https://doi.org/10.1002/cam4.2148
Forbes NS, Coffin RS, Deng L, Evgin L, Fiering S, Giacalone M, Gravecamp C, Gulley JL, Gunn H, Hoffman RM, Kaur B, Liuu K, Lyerly HK, Marciscano AE, Moradain E, Ruppel S, Saltzman DA, Tattersall PJ, Thorne S, Vile RG, Zhang HH, Zhou S and McFadden G. White paper on microbial anti-cancer therapy and prevention. J Immunother Cancer. 2018; 6(1): 78. DOI: https://doi.org/10.1186/s40425-018-0381-3
Geller LT, Barzily-Rokni M, Danino T, Jonas OH, Shental N, Nejman D, Gavert N, Zwang Y, Cooper ZA, Shee K, Thaiss CA, et al. Potential role of intratumor bacteria in mediating tumor resistance to the chemotherapeutic drug gemcitabine. Sci. 2017;357(6356):1156-1160. DOI: https://doi.org/10.1126/science.aah5043
Sharma P and Allison JP. The future of immune checkpoint therapy. Sci. 2015; 348(6230): 56-61. DOI: https://doi.org/10.1126/science.aaa8172
Zou W, Wolchok JD and Chen L. PD-L1 (B7-H1) and PD-1 pathway blockade for cancer therapy: Mechanisms, response biomarkers, and combinations. Sci Trans Med. 2016; 8(328): 328rv4-328rv4. DOI: https://doi.org/10.1126/scitranslmed.aad7118
Rock CL, Thomson C, Gansler T, Gapstur SM, McCullough ML, Patel AV, Andrews KS, Bandera EV, Spees CK, Robien K, Hartman S, Sullivan K, Grant BL, Hamilton KK, Kushi LH, Caan BJ, Kibbe D, Black JD, Wiedt TL, McMahon C, Sloan K and Doyle C. American Cancer Society guideline for diet and physical activity for cancer prevention. CA Cancer J Clin. 2020; 70(4): 245-271. DOI: https://doi.org/10.3322/caac.21591