Progress on attenuated <i>Salmonella typhimurium</i> in the treatment of tumors_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

YIN Yanmei ¹ , LI Junfeng ¹ , PENG Lei ¹ , RUAN Wanbai ¹ ,  ZHU Kexiang ²

1. The First Clinical Medical College of Lanzhou University, Lanzhou 730000, P. R. China;
2. Department of General Surgery, The First Hospital of Lanzhou University, Lanzhou 730000, P. R. China;

Corresponding author：

ZHU Kexiang, Email: flexzhu6910@163.com

Keywords：

Salmonella typhimurium; antitumor therapy; clinical trial

DOI：

10.7507/1007-9424.202304004

Video：

Export PDF Favorites Scan Get Citation

Abstract Full text Figures/Tables Video References Cited by

Objective To provide an overview of the main anti-tumor mechanisms of attenuated Salmonella typhimurium（ST） and explore potential reasons for the limited clinical application of attenuated ST. Methods The literatures related to clinical and basic research on attenuated ST tumor treatment and virulence at home and abroad in recent years were reviewed and the relevant mechanisms of attenuated ST tumor treatment were summarized. And then, analyses were made regarding the failure of clinical application experiments of attenuated ST based on the characteristics of attenuated ST and the human immune microenvironment. Results Attenuated ST could inhibit the growth of primary tumors and reduce the metastasis of secondary tumor due to its effect of tumor-targeting, its property of facultative anaerobic and its characteristic of being able to carry plasmids. On the other hand, the toxicity of wild strains to hosts had been reduced through biotechnology. In terms of clinical application, the anti-tumor effect of attenuated ST was far lower than expected due to excessive detoxification of ST, the elimination effect of foreign substances by the human immune system, and the inactivation effect of various proteases in the body. Conclusion As an emerging bacterial mediated anti-tumor therapy, attenuated ST will provide a new treatment option for precise treatment of cancer patients once its clinical application problems are solved.

Citation： YIN Yanmei, LI Junfeng, PENG Lei, RUAN Wanbai, ZHU Kexiang. Progress on attenuated Salmonella typhimurium in the treatment of tumors. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2023, 30(8): 988-994. doi: 10.7507/1007-9424.202304004 Copy

1.	Sung H, Ferlay J, Siegel RL, et al. Global Cancer Statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin, 2021, 71(3): 209-249.
2.	Phan T, Nguyen VH, D’Alincourt MS, et al. 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.
3.	Feltis BA, Miller JS, Sahar DA, et al. Liver and circulating NK1.1⁺CD3^- cells are increased in infection with attenuated Salmonella typhimurium and are associated with reduced tumor in murine liver cancer. J Surg Res, 2002, 107(1): 101-107.
4.	Pawelek JM, Low KB, Bermudes D. Tumor-targeted Salmonella as a novel anticancer vector. Cancer Res, 1997, 57(20): 4537-4544.
5.	Rabea S, Alanazi FK, Ashour AE, et al. Salmonella-innovative targeting carrier: loading with doxorubicin for cancer treatment. Saudi Pharm J, 2020, 28(10): 1253-1262.
6.	Liang K, Tian Z, Chen X, et al. Attenuated Salmonella typhimurium with truncated LPS and outer membrane-displayed RGD peptide for cancer therapy. Biomed Pharmacother, 2022, 155: 113682.
7.	Crull K, Bumann D, Weiss S. Influence of infection route and virulence factors on colonization of solid tumors by Salmonella enterica serovar Typhimurium. FEMS Immunol Med Microbiol, 2011, 62(1): 75-83.
8.	Hu M, Yang Y, Meng C, et al. Responses of macrophages against Salmonella infection compared with phagocytosis. In Vitro Cell Dev Biol Anim, 2013, 49(10): 778-784.
9.	Saltzman D, Augustin L, Leonard A, et al. Low dose chemotherapy combined with attenuated Salmonella decreases tumor burden and is less toxic than high dose chemotherapy in an autochthonous murine model of breast cancer. Surgery, 2018, 163(3): 509-514.
10.	Jawalagatti V, Kirthika P, 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.
11.	Ebelt ND, Zuniga E, Passi KB, et al. Hyaluronidase-expressing Salmonella effectively targets tumor-associated hyaluronic acid in pancreatic ductal adenocarcinoma. Mol Cancer Ther, 2020, 19(2): 706-716.
12.	Tan W, Duong MT, Zuo C, et al. Targeting of pancreatic cancer cells and stromal cells using engineered oncolytic Salmonella typhimurium. Mol Ther, 2022, 30(2): 662-671.
13.	Liang K, Zhang R, Luo H, et al. Optimized attenuated Salmonella typhimurium suppressed tumor growth and improved survival in mice. Front Microbiol, 2021, 12: 774490.
14.	Mónaco A, Plata MC, Chilibroste S, et al. Salmonella-induced immune response reduces recurrence and tumor dissemination in preclinical melanoma model. Curr Res Immunol, 2022, 3: 159-166.
15.	Johnson SA, Ormsby MJ, Wessel HM, et al. Monocytes mediate Salmonella typhimurium-induced tumor growth inhibition in a mouse melanoma model. Eur J Immunol, 2021, 51(12): 3228-3238.
16.	Chen J, Qiao Y, Chen G, et al. Salmonella flagella confer anti-tumor immunological effect via activating Flagellin/TLR5 signalling within tumor microenvironment. Acta Pharm Sin B, 2021, 11(10): 3165-3177.
17.	Zheng JH, Nguyen VH, Jiang SN, et al. Two-step enhanced cancer immunotherapy with engineered Salmonella typhimurium secreting heterologous flagellin. Sci Transl Med, 2017, 9(376): eaak9537.
18.	Yang S, Zhao W, Zhu M, et al. Tumor temporal proteome profiling reveals the immunological triple offensive induced by synthetic anti-cancer Salmonella. Front Immunol, 2021, 12: 712936.
19.	Miyake K, Murata T, Murakami T, et al. Tumor-targeting Salmonella typhimurium A1-R overcomes nab-paclitaxel resistance in a cervical cancer PDOX mouse model. Arch Gynecol Obstet, 2019, 299(6): 1683-1690.
20.	Trebichavský I. Cytokines in Salmonella infection. Folia Microbiol (Praha), 1999, 44(4): 457-460.
21.	Kiyuna T, Tome Y, Uehara F, et al. Tumor-targeting Salmonella typhimurium A1-R inhibits osteosarcoma angiogenesis in the in vivo Gelfoam^® assay visualized by color-coded imaging. Anticancer Res, 2018, 38(1): 159-164.
22.	Chen J, Qiao Y, Tang B, et al. Modulation of Salmonella tumor-colonization and intratumoral anti-angiogenesis by triptolide and its mechanism. Theranostics, 2017, 7(8): 2250-2260.
23.	Fan Y, Bai T, Tian Y, et al. H₂O₂-inactivated Salmonella typhimurium RE88 strain as a new cancer vaccine carrier: evaluation in a mouse model of cancer. Drug Des Devel Ther, 2021, 15: 209-222.
24.	Becerra-Báez EI, Meza-Toledo SE, Muñoz-López P, et al. Recombinant attenuated Salmonella enterica as a delivery system of heterologous molecules in cancer therapy. Cancers (Basel), 2022, 14(17): 4224.
25.	de Lima Fragelli BD, Camillo L, de Almeida Rodolpho JM, et al. Antitumor effect of IL-2 and TRAIL proteins expressed by recombinant Salmonella in murine bladder cancer cells. Cell Physiol Biochem, 2021, 55(4): 460-476.
26.	Ahmed SG, Oliva G, Shao M, et al. Intratumoral injection of schwannoma with attenuated Salmonella typhimurium induces antitumor immunity and controls tumor growth. Proc Natl Acad Sci U S A, 2022, 119(24): e2202719119.
27.	Pinkert J, Boehm HH, Trautwein M, et al. T cell-mediated elimination of cancer cells by blocking CEACAM6-CEACAM1 interaction. Oncoimmunology, 2021, 11(1): 2008110.
28.	Fujiwara Y, Kato S, Nesline MK, et al. Indoleamine 2, 3-dioxygenase (IDO) inhibitors and cancer immunotherapy. Cancer Treat Rev, 2022, 110: 102461.
29.	Chen J, Zhao S, Tan W, et al. Attenuated Salmonella carrying plasmid co-expressing HPV16 L1 and siRNA-E6 for cervical cancer therapy. Sci Rep, 2021, 11(1): 20083.
30.	Lu S, Gao J, Jia H, et al. PD-1-siRNA delivered by attenuated salmonella enhances the antitumor effect of chloroquine in colon cancer. Front Immunol, 2021, 12: 707991.
31.	Liang K, Liu Q, Li P, et al. Endostatin gene therapy delivered by attenuated Salmonella typhimurium in murine tumor models. Cancer Gene Ther, 2018, 25(7-8): 167-183.
32.	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.
33.	Zhao T, Feng Y, Guo M, et al. Combination of attenuated Salmonella carrying PD-1 siRNA with nifuroxazide for colon cancer therapy. J Cell Biochem, 2020, 121(2): 1973-1985.
34.	Zhao T, Wei T, Guo J, et al. PD-1-siRNA delivered by attenuated Salmonella enhances the antimelanoma effect of pimozide. Cell Death Dis, 2019, 10(3): 164.
35.	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: 2562.
36.	Yoon W, Yoo Y, Chae YS, et al. Therapeutic advantage of genetically engineered Salmonella typhimurium carrying short hairpin RNA against inhibin alpha subunit in cancer treatment. Ann Oncol, 2018, 29(9): 2010-2017.
37.	Chen F, Zang Z, Chen Z, et al. Nanophotosensitizer-engineered Salmonella bacteria with hypoxia targeting and photothermal-assisted mutual bioaccumulation for solid tumor therapy. Biomaterials, 2019, 214: 119226.
38.	Gu J, Li Y, Zeng J, et al. Knockdown of HIF-1α by siRNA-expressing plasmid delivered by attenuated Salmonella enhances the antitumor effects of cisplatin on prostate cancer. Sci Rep, 2017, 7(1): 7546.
39.	Jin C, Duan X, Liu Y, et al. T cell immunity induced by a bivalent Salmonella-based CEACAM6 and 4-1BBL vaccines in a rat colorectal cancer model. Oncol Lett, 2017, 13(5): 3753-3759.
40.	Jin C, Liu Y, Zhu J, et al. Recombinant Salmonella-based CEACAM6 and 4-1BBL vaccine enhances T-cell immunity and inhibits the development of colorectal cancer in rats: in vivo effects of vaccine containing 4-1BBL and CEACAM6. Oncol Rep, 2015, 33(6): 2837-2844.
41.	Chen P, Li Y, Wei P, et al. siRNA targeting PD-L1 delivered with attenuated Salmonella enhanced the anti-tumor effect of lenvatinib on mice bearing hepatocellular carcinoma. Int Immunopharmacol, 2022, 111: 109127.
42.	Zhang Y, Cao W, Toneri M, et al. Toxicology and efficacy of tumor-targeting Salmonella typhimurium A1-R compared to VNP 20009 in a syngeneic mouse tumor model in immunocompetent mice. Oncotarget, 2017, 8(33): 54616-54628.
43.	Huang H, Brekken RA. The next wave of stroma-targeting therapy in pancreatic cancer. Cancer Res, 2019, 79(2): 328-330.
44.	Yang CJ, Chang WW, Lin ST, et al. Salmonella overcomes drug resistance in tumor through P-glycoprotein downregulation. Int J Med Sci, 2018, 15(6): 574-579.
45.	Kawaguchi K, Higuchi T, Li S, et al. Combination therapy of tumor-targeting Salmonella typhimurium A1-R and oral recombinant methioninase regresses a BRAF-V600E-negative melanoma. Biochem Biophys Res Commun, 2018, 503(4): 3086-3092.
46.	Kawaguchi K, Miyake K, Zhao M, et al. Tumor targeting Salmonella typhimurium A1-R in combination with gemcitabine (GEM) regresses partially GEM-resistant pancreatic cancer patient-derived orthotopic xenograft (PDOX) nude mouse models. Cell Cycle, 2018, 17(16): 2019-2026.
47.	Igarashi K, Kawaguchi K, Kiyuna T, et al. Tumor-targeting Salmonella typhimurium A1-R combined with recombinant methioninase and cisplatinum eradicates an osteosarcoma cisplatinum-resistant lung metastasis in a patient-derived orthotopic xenograft (PDOX) mouse model: decoy, trap and kill chemotherapy moves toward the clinic. Cell Cycle, 2018, 17(6): 801-809.
48.	Igarashi K, Kawaguchi K, Zhao M, et al. Recombinant methioninase combined with tumor-targeting Salmonella typhimurium A1-R induced regression in a PDOX mouse model of doxorubicin-resistant dedifferentiated liposarcoma. Anticancer Res, 2020, 40(5): 2515-2523.
49.	Pangilinan CR, Lee CH. Salmonella-based targeted cancer therapy: updates on a promising and innovative tumor immunotherapeutic strategy. Biomedicines, 2019, 7(2): 36.
50.	Zhao Q, Wang Y, Li WT. Synergistic effects of arsenic trioxide combined with Salmonella typhimurium in treating the advanced hepatocellular carcinoma in rat models. J Gastrointest Oncol, 2021, 12(4): 1732-1742.
51.	Gao S, Jung JH, Lin SM, et al. Development of oxytolerant Salmonella typhimurium using radiation mutation technology (RMT) for cancer therapy. Sci Rep, 2020, 10(1): 3764.
52.	Kung YJ, Lam B, Tseng SH, 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.
53.	Bascuas T, Moreno M, Grille S, et al. Salmonella immunotherapy improves the outcome of CHOP chemotherapy in non-hodgkin lymphoma-bearing mice. Front Immunol, 2018, 9: 7.
54.	Aly RG, El-Enbaawy MI, Abd El-Rahman SS, et al. Antineoplastic activity of Salmonella typhimurium outer membrane nanovesicles. Exp Cell Res, 2021, 399(1): 112423.
55.	Tsao YT, Kuo CY, Cheng SP, et al. 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.
56.	Chiu HM, Chiou WY, Hsu WJ, et al. Salmonella alters heparanase expression and reduces tumor metastasis. Int J Med Sci, 2021, 18(13): 2981-2989.
57.	Lee TH, Lin GY, Yang MH, et al. Salmonella reduces tumor metastasis by downregulation C-X-C chemokine receptor type 4. Int J Med Sci, 2021, 18(13): 2835-2841.
58.	Pangilinan CR, Wu LH, Lee CH. Salmonella impacts tumor-induced macrophage polarization, and inhibits SNAI1-mediated metastasis in melanoma. Cancers (Basel), 2021, 13(12): 2894.
59.	Nemunaitis J, Cunningham C, Senzer N, et al. Pilot trial of genetically modified, attenuated Salmonella expressing the E. coli cytosine deaminase gene in refractory cancer patients. Cancer Gene Ther, 2003, 10(10): 737-744.
60.	Zhou S, Gravekamp C, Bermudes D, et al. Tumour-targeting bacteria engineered to fight cancer. Nat Rev Cancer, 2018, 18(12): 727-743.
61.	Mackie GM, Copland A, Takahashi M, et al. Bacterial cancer therapy in autochthonous colorectal cancer affects tumor growth and metabolic landscape. JCI Insight, 2021, 6(23): e139900.
62.	Mi Z, Guo L, Liu P, et al. “Trojan Horse” Salmonella enabling tumor homing of silver nanoparticles via neutrophil infiltration for synergistic tumor therapy and enhanced biosafety. Nano Lett, 2021, 21(1): 414-423.
63.	Tian S, Lin G, Piao L, et al. Del-1 enhances therapeutic efficacy of bacterial cancer immunotherapy by blocking recruitment of tumor-infiltrating neutrophils. Clin Transl Oncol, 2022, 24(2): 244-253.
64.	Chen T, Zhao X, Ren Y, et al. Triptolide modulates tumour-colonisation and anti-tumour effect of attenuated Salmonella encoding DNase Ⅰ. Appl Microbiol Biotechnol, 2019, 103(2): 929-939.
65.	Wang Y, Zhou Z, Chen W, et al. Potentiating bacterial cancer therapy using hydroxychloroquine liposomes. J Control Release, 2018, 280: 39-50.
66.	Quintero D, Carrafa J, Vincent L, et al. Co-expression of a chimeric protease inhibitor secreted by a tumor-targeted Salmonella protects therapeutic proteins from proteolytic degradation. J Microbiol Biotechnol, 2018, 28(12): 2079-2094.

1. Sung H, Ferlay J, Siegel RL, et al. Global Cancer Statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin, 2021, 71(3): 209-249.
2. Phan T, Nguyen VH, D’Alincourt MS, et al. 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.
3. Feltis BA, Miller JS, Sahar DA, et al. Liver and circulating NK1.1⁺CD3^- cells are increased in infection with attenuated Salmonella typhimurium and are associated with reduced tumor in murine liver cancer. J Surg Res, 2002, 107(1): 101-107.
4. Pawelek JM, Low KB, Bermudes D. Tumor-targeted Salmonella as a novel anticancer vector. Cancer Res, 1997, 57(20): 4537-4544.
5. Rabea S, Alanazi FK, Ashour AE, et al. Salmonella-innovative targeting carrier: loading with doxorubicin for cancer treatment. Saudi Pharm J, 2020, 28(10): 1253-1262.
6. Liang K, Tian Z, Chen X, et al. Attenuated Salmonella typhimurium with truncated LPS and outer membrane-displayed RGD peptide for cancer therapy. Biomed Pharmacother, 2022, 155: 113682.
7. Crull K, Bumann D, Weiss S. Influence of infection route and virulence factors on colonization of solid tumors by Salmonella enterica serovar Typhimurium. FEMS Immunol Med Microbiol, 2011, 62(1): 75-83.
8. Hu M, Yang Y, Meng C, et al. Responses of macrophages against Salmonella infection compared with phagocytosis. In Vitro Cell Dev Biol Anim, 2013, 49(10): 778-784.
9. Saltzman D, Augustin L, Leonard A, et al. Low dose chemotherapy combined with attenuated Salmonella decreases tumor burden and is less toxic than high dose chemotherapy in an autochthonous murine model of breast cancer. Surgery, 2018, 163(3): 509-514.
10. Jawalagatti V, Kirthika P, 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.
11. Ebelt ND, Zuniga E, Passi KB, et al. Hyaluronidase-expressing Salmonella effectively targets tumor-associated hyaluronic acid in pancreatic ductal adenocarcinoma. Mol Cancer Ther, 2020, 19(2): 706-716.
12. Tan W, Duong MT, Zuo C, et al. Targeting of pancreatic cancer cells and stromal cells using engineered oncolytic Salmonella typhimurium. Mol Ther, 2022, 30(2): 662-671.
13. Liang K, Zhang R, Luo H, et al. Optimized attenuated Salmonella typhimurium suppressed tumor growth and improved survival in mice. Front Microbiol, 2021, 12: 774490.
14. Mónaco A, Plata MC, Chilibroste S, et al. Salmonella-induced immune response reduces recurrence and tumor dissemination in preclinical melanoma model. Curr Res Immunol, 2022, 3: 159-166.
15. Johnson SA, Ormsby MJ, Wessel HM, et al. Monocytes mediate Salmonella typhimurium-induced tumor growth inhibition in a mouse melanoma model. Eur J Immunol, 2021, 51(12): 3228-3238.
16. Chen J, Qiao Y, Chen G, et al. Salmonella flagella confer anti-tumor immunological effect via activating Flagellin/TLR5 signalling within tumor microenvironment. Acta Pharm Sin B, 2021, 11(10): 3165-3177.
17. Zheng JH, Nguyen VH, Jiang SN, et al. Two-step enhanced cancer immunotherapy with engineered Salmonella typhimurium secreting heterologous flagellin. Sci Transl Med, 2017, 9(376): eaak9537.
18. Yang S, Zhao W, Zhu M, et al. Tumor temporal proteome profiling reveals the immunological triple offensive induced by synthetic anti-cancer Salmonella. Front Immunol, 2021, 12: 712936.
19. Miyake K, Murata T, Murakami T, et al. Tumor-targeting Salmonella typhimurium A1-R overcomes nab-paclitaxel resistance in a cervical cancer PDOX mouse model. Arch Gynecol Obstet, 2019, 299(6): 1683-1690.
20. Trebichavský I. Cytokines in Salmonella infection. Folia Microbiol (Praha), 1999, 44(4): 457-460.
21. Kiyuna T, Tome Y, Uehara F, et al. Tumor-targeting Salmonella typhimurium A1-R inhibits osteosarcoma angiogenesis in the in vivo Gelfoam^® assay visualized by color-coded imaging. Anticancer Res, 2018, 38(1): 159-164.
22. Chen J, Qiao Y, Tang B, et al. Modulation of Salmonella tumor-colonization and intratumoral anti-angiogenesis by triptolide and its mechanism. Theranostics, 2017, 7(8): 2250-2260.
23. Fan Y, Bai T, Tian Y, et al. H₂O₂-inactivated Salmonella typhimurium RE88 strain as a new cancer vaccine carrier: evaluation in a mouse model of cancer. Drug Des Devel Ther, 2021, 15: 209-222.
24. Becerra-Báez EI, Meza-Toledo SE, Muñoz-López P, et al. Recombinant attenuated Salmonella enterica as a delivery system of heterologous molecules in cancer therapy. Cancers (Basel), 2022, 14(17): 4224.
25. de Lima Fragelli BD, Camillo L, de Almeida Rodolpho JM, et al. Antitumor effect of IL-2 and TRAIL proteins expressed by recombinant Salmonella in murine bladder cancer cells. Cell Physiol Biochem, 2021, 55(4): 460-476.
26. Ahmed SG, Oliva G, Shao M, et al. Intratumoral injection of schwannoma with attenuated Salmonella typhimurium induces antitumor immunity and controls tumor growth. Proc Natl Acad Sci U S A, 2022, 119(24): e2202719119.
27. Pinkert J, Boehm HH, Trautwein M, et al. T cell-mediated elimination of cancer cells by blocking CEACAM6-CEACAM1 interaction. Oncoimmunology, 2021, 11(1): 2008110.
28. Fujiwara Y, Kato S, Nesline MK, et al. Indoleamine 2, 3-dioxygenase (IDO) inhibitors and cancer immunotherapy. Cancer Treat Rev, 2022, 110: 102461.
29. Chen J, Zhao S, Tan W, et al. Attenuated Salmonella carrying plasmid co-expressing HPV16 L1 and siRNA-E6 for cervical cancer therapy. Sci Rep, 2021, 11(1): 20083.
30. Lu S, Gao J, Jia H, et al. PD-1-siRNA delivered by attenuated salmonella enhances the antitumor effect of chloroquine in colon cancer. Front Immunol, 2021, 12: 707991.
31. Liang K, Liu Q, Li P, et al. Endostatin gene therapy delivered by attenuated Salmonella typhimurium in murine tumor models. Cancer Gene Ther, 2018, 25(7-8): 167-183.
32. 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.
33. Zhao T, Feng Y, Guo M, et al. Combination of attenuated Salmonella carrying PD-1 siRNA with nifuroxazide for colon cancer therapy. J Cell Biochem, 2020, 121(2): 1973-1985.
34. Zhao T, Wei T, Guo J, et al. PD-1-siRNA delivered by attenuated Salmonella enhances the antimelanoma effect of pimozide. Cell Death Dis, 2019, 10(3): 164.
35. 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: 2562.
36. Yoon W, Yoo Y, Chae YS, et al. Therapeutic advantage of genetically engineered Salmonella typhimurium carrying short hairpin RNA against inhibin alpha subunit in cancer treatment. Ann Oncol, 2018, 29(9): 2010-2017.
37. Chen F, Zang Z, Chen Z, et al. Nanophotosensitizer-engineered Salmonella bacteria with hypoxia targeting and photothermal-assisted mutual bioaccumulation for solid tumor therapy. Biomaterials, 2019, 214: 119226.
38. Gu J, Li Y, Zeng J, et al. Knockdown of HIF-1α by siRNA-expressing plasmid delivered by attenuated Salmonella enhances the antitumor effects of cisplatin on prostate cancer. Sci Rep, 2017, 7(1): 7546.
39. Jin C, Duan X, Liu Y, et al. T cell immunity induced by a bivalent Salmonella-based CEACAM6 and 4-1BBL vaccines in a rat colorectal cancer model. Oncol Lett, 2017, 13(5): 3753-3759.
40. Jin C, Liu Y, Zhu J, et al. Recombinant Salmonella-based CEACAM6 and 4-1BBL vaccine enhances T-cell immunity and inhibits the development of colorectal cancer in rats: in vivo effects of vaccine containing 4-1BBL and CEACAM6. Oncol Rep, 2015, 33(6): 2837-2844.
41. Chen P, Li Y, Wei P, et al. siRNA targeting PD-L1 delivered with attenuated Salmonella enhanced the anti-tumor effect of lenvatinib on mice bearing hepatocellular carcinoma. Int Immunopharmacol, 2022, 111: 109127.
42. Zhang Y, Cao W, Toneri M, et al. Toxicology and efficacy of tumor-targeting Salmonella typhimurium A1-R compared to VNP 20009 in a syngeneic mouse tumor model in immunocompetent mice. Oncotarget, 2017, 8(33): 54616-54628.
43. Huang H, Brekken RA. The next wave of stroma-targeting therapy in pancreatic cancer. Cancer Res, 2019, 79(2): 328-330.
44. Yang CJ, Chang WW, Lin ST, et al. Salmonella overcomes drug resistance in tumor through P-glycoprotein downregulation. Int J Med Sci, 2018, 15(6): 574-579.
45. Kawaguchi K, Higuchi T, Li S, et al. Combination therapy of tumor-targeting Salmonella typhimurium A1-R and oral recombinant methioninase regresses a BRAF-V600E-negative melanoma. Biochem Biophys Res Commun, 2018, 503(4): 3086-3092.
46. Kawaguchi K, Miyake K, Zhao M, et al. Tumor targeting Salmonella typhimurium A1-R in combination with gemcitabine (GEM) regresses partially GEM-resistant pancreatic cancer patient-derived orthotopic xenograft (PDOX) nude mouse models. Cell Cycle, 2018, 17(16): 2019-2026.
47. Igarashi K, Kawaguchi K, Kiyuna T, et al. Tumor-targeting Salmonella typhimurium A1-R combined with recombinant methioninase and cisplatinum eradicates an osteosarcoma cisplatinum-resistant lung metastasis in a patient-derived orthotopic xenograft (PDOX) mouse model: decoy, trap and kill chemotherapy moves toward the clinic. Cell Cycle, 2018, 17(6): 801-809.
48. Igarashi K, Kawaguchi K, Zhao M, et al. Recombinant methioninase combined with tumor-targeting Salmonella typhimurium A1-R induced regression in a PDOX mouse model of doxorubicin-resistant dedifferentiated liposarcoma. Anticancer Res, 2020, 40(5): 2515-2523.
49. Pangilinan CR, Lee CH. Salmonella-based targeted cancer therapy: updates on a promising and innovative tumor immunotherapeutic strategy. Biomedicines, 2019, 7(2): 36.
50. Zhao Q, Wang Y, Li WT. Synergistic effects of arsenic trioxide combined with Salmonella typhimurium in treating the advanced hepatocellular carcinoma in rat models. J Gastrointest Oncol, 2021, 12(4): 1732-1742.
51. Gao S, Jung JH, Lin SM, et al. Development of oxytolerant Salmonella typhimurium using radiation mutation technology (RMT) for cancer therapy. Sci Rep, 2020, 10(1): 3764.
52. Kung YJ, Lam B, Tseng SH, 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.
53. Bascuas T, Moreno M, Grille S, et al. Salmonella immunotherapy improves the outcome of CHOP chemotherapy in non-hodgkin lymphoma-bearing mice. Front Immunol, 2018, 9: 7.
54. Aly RG, El-Enbaawy MI, Abd El-Rahman SS, et al. Antineoplastic activity of Salmonella typhimurium outer membrane nanovesicles. Exp Cell Res, 2021, 399(1): 112423.
55. Tsao YT, Kuo CY, Cheng SP, et al. 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.
56. Chiu HM, Chiou WY, Hsu WJ, et al. Salmonella alters heparanase expression and reduces tumor metastasis. Int J Med Sci, 2021, 18(13): 2981-2989.
57. Lee TH, Lin GY, Yang MH, et al. Salmonella reduces tumor metastasis by downregulation C-X-C chemokine receptor type 4. Int J Med Sci, 2021, 18(13): 2835-2841.
58. Pangilinan CR, Wu LH, Lee CH. Salmonella impacts tumor-induced macrophage polarization, and inhibits SNAI1-mediated metastasis in melanoma. Cancers (Basel), 2021, 13(12): 2894.
59. Nemunaitis J, Cunningham C, Senzer N, et al. Pilot trial of genetically modified, attenuated Salmonella expressing the E. coli cytosine deaminase gene in refractory cancer patients. Cancer Gene Ther, 2003, 10(10): 737-744.
60. Zhou S, Gravekamp C, Bermudes D, et al. Tumour-targeting bacteria engineered to fight cancer. Nat Rev Cancer, 2018, 18(12): 727-743.
61. Mackie GM, Copland A, Takahashi M, et al. Bacterial cancer therapy in autochthonous colorectal cancer affects tumor growth and metabolic landscape. JCI Insight, 2021, 6(23): e139900.
62. Mi Z, Guo L, Liu P, et al. “Trojan Horse” Salmonella enabling tumor homing of silver nanoparticles via neutrophil infiltration for synergistic tumor therapy and enhanced biosafety. Nano Lett, 2021, 21(1): 414-423.
63. Tian S, Lin G, Piao L, et al. Del-1 enhances therapeutic efficacy of bacterial cancer immunotherapy by blocking recruitment of tumor-infiltrating neutrophils. Clin Transl Oncol, 2022, 24(2): 244-253.
64. Chen T, Zhao X, Ren Y, et al. Triptolide modulates tumour-colonisation and anti-tumour effect of attenuated Salmonella encoding DNase Ⅰ. Appl Microbiol Biotechnol, 2019, 103(2): 929-939.
65. Wang Y, Zhou Z, Chen W, et al. Potentiating bacterial cancer therapy using hydroxychloroquine liposomes. J Control Release, 2018, 280: 39-50.
66. Quintero D, Carrafa J, Vincent L, et al. Co-expression of a chimeric protease inhibitor secreted by a tumor-targeted Salmonella protects therapeutic proteins from proteolytic degradation. J Microbiol Biotechnol, 2018, 28(12): 2079-2094.

Previous Article
Anti-inflammatory effects of caloric restriction and caloric restriction mimetics
Next Article
Application of artificial intelligence in risk assessment and diagnosis of pancreatic cancer

CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Progress on attenuated Salmonella typhimurium in the treatment of tumors

Abstract Full text Figures/Tables Video References Cited by

Previous Article

Next Article

Format

Content