983
Views
0
CrossRef citations to date
0
Altmetric
Original Research

Salmonella immunotherapy engineered with highly efficient tumor antigen coating establishes antigen-specific CD8+ T cell immunity and increases in antitumor efficacy with type I interferon combination therapy

, , , , , , , & show all
Article: 2298444 | Received 18 Oct 2023, Accepted 19 Dec 2023, Published online: 27 Dec 2023

References

  • Gupta KH, Nowicki C, Giurini EF, Marzo AL, Zloza A. Bacterial-based cancer therapy (BBCT): recent advances, Current challenges, and future prospects for cancer immunotherapy. Vaccines (Basel). 2021;9(12):1497. doi: 10.3390/vaccines9121497.
  • Liang S, Wang C, Shao Y, Wang Y, Xing D, Geng Z. Recent advances in bacteria-mediated cancer therapy. Front Bioeng Biotechnol. 2022;10:1026248. doi: 10.3389/fbioe.2022.1026248.
  • Phan TX, Nguyen VH, Duong MT, Hong Y, Choy HE, Min JJ. Activation of inflammasome by attenuated salmonella typhimurium in bacteria-mediated cancer therapy. Microbiol Immunol. 2015;59(11):664–9. doi: 10.1111/1348-0421.12333.
  • Xiao S, Shi H, Zhang Y, Fan Y, Wang L, Xiang L, Liu Y, Zhao L, Fu S. Bacteria-driven hypoxia targeting delivery of chemotherapeutic drug proving outcome of breast cancer. J Nanobiotechnology. 2022;20(1):178. doi: 10.1186/s12951-022-01373-1.
  • Yu B, Yang M, Shi L, Yao Y, Jiang Q, Li X, Tang L-H, Zheng B-J, Yuen K-Y, Smith DK, et al. Explicit hypoxia targeting with tumor suppression by creating an “obligate” anaerobic salmonella typhimurium strain. Sci Rep. 2012;2(1):436. doi: 10.1038/srep00436.
  • Gurbatri CR, Arpaia N, Danino T. Engineering bacteria as interactive cancer therapies. Sci. 2022;378(6622):858–64. doi: 10.1126/science.add9667.
  • Chandra D, Selvanesan BC, Yuan Z, Libutti SK, Koba W, Beck A, Zhu K, Casadevall A, Dadachova E, Gravekamp C, et al. 32-phosphorus selectively delivered by listeria to pancreatic cancer demonstrates a strong therapeutic effect. Oncotarget. 2017;8(13):20729–40. doi: 10.18632/oncotarget.15117.
  • Aganja RP, Sivasankar C, Senevirathne A, Lee JH. Salmonella as a promising curative tool against cancer. Pharmaceutics. 2022;14(10):2100. doi: 10.3390/pharmaceutics14102100.
  • Al-Ramadi BK, Fernandez-Cabezudo MJ, El-Hasasna H, Al-Salam S, Bashir G, 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: 10.1016/j.clim.2008.08.021.
  • Kung YJ, Lam B, Tseng SH, MacDonald A, Tu HF, Wang S, Lin J, Tsai YC, Wu TC, Hung C-F, et al. Localization of Salmonella and albumin-IL-2 to the tumor microenvironment augments anticancer T cell immunity. J Biomed Sci. 2022;29(1):57. doi: 10.1186/s12929-022-00841-y.
  • Nishikawa H, Sato E, Briones G, Chen LM, Matsuo M, Nagata Y, et al. 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: 10.1172/JCI28045.
  • Ylösmäki E, Fusciello M, Martins B, Feola S, Hamdan F, Chiaro J, Ylösmäki L, Vaughan MJ, Viitala T, Kulkarni PS, et al. Novel personalized cancer vaccine platform based on Bacillus Calmette-Guèrin. J Immunother Cancer. 2021;9(7):e002707. doi: 10.1136/jitc-2021-002707.
  • Bayat Mokhtari R, Homayouni TS, Baluch N, Morgatskaya E, Kumar S, Das B, Yeger H. Combination therapy in combating cancer. Oncotarget. 2017;8(23):38022–38043. doi: 10.18632/oncotarget.16723.
  • Dunn GP, Old LJ, Schreiber RD. The immunobiology of cancer immunosurveillance and immunoediting. Immunity. 2004;21(2):137–48. doi: 10.1016/j.immuni.2004.07.017.
  • Guillot B, Portalès P, Thanh AD, Merlet S, Dereure O, Clot J, Corbeau P. The expression of cytotoxic mediators is altered in mononuclear cells of patients with melanoma and increased by interferon-alpha treatment. Br J Dermatol. 2005;152(4):690–696. doi: 10.1111/j.1365-2133.2005.06512.x.
  • Zitvogel L, Galluzzi L, Kepp O, Smyth MJ, Kroemer G. Type I interferons in anticancer immunity. Nat Rev Immunol. 2015;15(7):405–14. doi: 10.1038/nri3845.
  • Tarhini AA, Cherian J, Moschos SJ, Tawbi HA, Shuai Y, Gooding WE, Sander C, Kirkwood JM. Safety and efficacy of combination immunotherapy with interferon alfa-2b and tremelimumab in patients with stage IV melanoma. J Clin Oncol. 2012;30(3):322–328. doi: 10.1200/JCO.2011.37.5394.
  • Preudhomme C, Guilhot J, Nicolini FE, Guerci-Bresler A, Rigal-Huguet F, Maloisel F, Coiteux V, Gardembas M, Berthou C, Vekhoff A, et al. Imatinib plus peginterferon alfa-2a in chronic myeloid leukemia. N Engl J Med. 2010;363(26):2511–21. doi: 10.1056/NEJMoa1004095.
  • Burchert A, Müller MC, Kostrewa P, Erben P, Bostel T, Liebler S, Hehlmann R, Neubauer A, Hochhaus A. Sustained molecular response with interferon alfa maintenance after induction therapy with imatinib plus interferon alfa in patients with chronic myeloid leukemia. J Clin Oncol. 2010;28(8):1429–1435. doi: 10.1200/JCO.2009.25.5075.
  • Tseng SH, Cheng MA, Farmer E, Ferrall L, Kung YJ, Lam B, Lim L, Wu T-C, Hung C-F. Albumin and interferon-β fusion protein serves as an effective vaccine adjuvant to enhance antigen-specific CD8+ T cell-mediated antitumor immunity. J Immunother Cancer. 2022;10(4):e004342. doi: 10.1136/jitc-2021-004342.
  • Cutrona KJ, Kaufman BA, Figueroa DM, Elmore DE. Role of arginine and lysine in the antimicrobial mechanism of histone-derived antimicrobial peptides. FEBS Lett. 2015;589(24PartB):3915–20. doi: 10.1016/j.febslet.2015.11.002.
  • Wang TL, Ling M, Shih IM, Pham T, Pai SI, Lu Z, Kurman RJ, Pardoll DM, Wu T-C. Intramuscular administration of E7-transfected dendritic cells generates the most potent E7-specific anti-tumor immunity. Gene Ther. 2000;7(9):726–733. doi: 10.1038/sj.gt.3301160.
  • Shen Z, Reznikoff G, Dranoff G, Rock KL. Cloned dendritic cells can present exogenous antigens on both MHC class I and class II molecules. J Immunol. 1997;158(6):2723–30. doi: 10.4049/jimmunol.158.6.2723.
  • Ma Y, Yang A, Peng S, Qiu J, Farmer E, Hung CF, Wu T-C. Characterization of HPV18 E6-specific T cell responses and establishment of HPV18 E6-expressing tumor model. Vaccine. 2017;35(31):3850–3858. doi: 10.1016/j.vaccine.2017.05.081.
  • Ebrahimi A, Csonka LN, Alam MA. Analyzing thermal stability of cell membrane of salmonella using time-multiplexed impedance sensing. Biophys J. 2018;114(3):609–18. doi: 10.1016/j.bpj.2017.10.032.
  • Fuchs SM, Raines RT. Polyarginine as a multifunctional fusion tag. Protein Sci. 2005;14(6):1538–44. doi: 10.1110/ps.051393805.
  • Lentini G, De Gaetano GV, Famà A, Galbo R, Coppolino F, Mancuso G, Teti G, Beninati C. Neutrophils discriminate live from dead bacteria by integrating signals initiated by Fprs and TLRs. EMBO J. 2022;41(5):e109386. doi: 10.15252/embj.2021109386.
  • Met O, Buus S, Claesson MH. Peptide-loaded dendritic cells prime and activate MHC-class I-restricted T cells more efficiently than protein-loaded cross-presenting DC. Cellular Immunology. 2003;222(2):126–133. doi: 10.1016/S0008-8749(03)00128-X.
  • Romani N, Flacher V, Tripp CH, Sparber F, Ebner S, Stoitzner P. Targeting skin dendritic cells to improve intradermal vaccination. Curr Top Microbiol Immunol. 2012;351:113–138.
  • van Pul KM, Fransen MF, van de Ven R, de Gruijl TD, van Pul KM. Immunotherapy goes local: the central role of lymph nodes in driving tumor infiltration and efficacy. Front Immunol. 2021;12:643291. doi: 10.3389/fimmu.2021.643291.
  • Marion Pitorre GB, Bastiat G, Dit Chatel EM, Benoit J-P. Elodie Marie dit Chatel, Jean-Pierre Benoit. Passive and specific targeting of lymph nodes: the influence of the administration route. Eur J Nanomed. 2015;7(2). doi: 10.1515/ejnm-2015-0003.
  • Koukourakis MI, Giatromanolaki A. Tumor draining lymph nodes, immune response, and radiotherapy: towards a revisal of therapeutic principles. Biochim Biophys Acta Rev Cancer. 2022;1877(3):188704. doi: 10.1016/j.bbcan.2022.188704.
  • Hong WX, Haebe S, Lee AS, Westphalen CB, Norton JA, Jiang W, Levy R. Intratumoral immunotherapy for early-stage solid tumors. Clin Cancer Res. 2020;26(13):3091–3099. doi: 10.1158/1078-0432.CCR-19-3642.
  • Wu W, Pu Y, Gao S, Shen Y, Zhou M, Yao H, Shi J. Bacterial metabolism-initiated nanocatalytic tumor immunotherapy. Nanomicro Lett. 2022;14(1):220. doi: 10.1007/s40820-022-00951-0.
  • Yi X, Zhou H, Chao Y, Xiong S, Zhong J, Chai Z, Yang K, Liu Z. Bacteria-triggered tumor-specific thrombosis to enable potent photothermal immunotherapy of cancer. Sci Adv. 2020;6(33):eaba3546. doi: 10.1126/sciadv.aba3546.
  • Welsh RM, Bahl K, Marshall HD, Urban SL, Rall GF. Type 1 interferons and antiviral CD8 T-cell responses. PLoS Pathog. 2012;8(1):e1002352. doi: 10.1371/journal.ppat.1002352.
  • McSorley SJ, Cookson BT, Jenkins MK. Characterization of CD4+ T cell responses during natural infection with salmonella typhimurium. J Immunol. 2000;164(2):986–93. doi: 10.4049/jimmunol.164.2.986.
  • Antonelli AC, Binyamin A, Hohl TM, Glickman MS, Redelman-Sidi G. Bacterial immunotherapy for cancer induces CD4-dependent tumor-specific immunity through tumor-intrinsic interferon-γ signaling. Proc Natl Acad Sci U S A. 2020;117(31):18627–37. doi: 10.1073/pnas.2004421117.
  • Hess J, Ladel C, Miko D, Kaufmann SH. Salmonella typhimurium aroA- infection in gene-targeted immunodeficient mice: major role of CD4+ TCR-alpha beta cells and IFN-gamma in bacterial clearance independent of intracellular location. J Immunol. 1996;156(9):3321–6. doi: 10.4049/jimmunol.156.9.3321.
  • Ravindran R, McSorley SJ. Tracking the dynamics of T-cell activation in response to Salmonella infection. Immunology. 2005;114(4):450–8. doi: 10.1111/j.1365-2567.2005.02140.x.
  • Cao X, Liang Y, Hu Z, Li H, Yang J, Hsu EJ, Zhu J, Zhou J, Fu Y-X. Next generation of tumor-activating type I IFN enhances anti-tumor immune responses to overcome therapy resistance. Nat Commun. 2021;12(1):5866. doi: 10.1038/s41467-021-26112-2.