Skip to main content
Top
Published in: Clinical and Translational Oncology 2/2018

01-02-2018 | Review Article

The potential roles of bacteria to improve radiation treatment outcome

Authors: E. Kouhsari, A. Ghadimi-Daresajini, H. Abdollahi, N. Amirmozafari, S. R. Mahdavi, S. Abbasian, S. H. Mousavi, H. F. Yaseri, M. Moghaderi

Published in: Clinical and Translational Oncology | Issue 2/2018

Login to get access

Abstract

Many combined therapies have been proposed to enhance radiotherapy outcome, but they have several limitations. As a new feasible strategy, combination of radiotherapy with bacteria showed a significant positive impact on the tumor treatment and metastasis inhibition. Although probiotic bacteria and radiotherapy alone can be effective in the treatment of different cancers, the combination of these two therapies seems to enhance therapeutic outcome and is cost-effective. Bacterial cells can act as therapeutic/gene/drug delivery vehicles as well as theranostic agents. In this communication, we reviewed current evidences, studies, suggestions, and future-based directions on combination of radiotherapy and bacteria. In another sections, an overview on tumor hypoxia, bacteria in cancer therapy, and combination of radiotherapy and bacteria is presented. A brief overview on trials and animal studies which used bacteria to protect normal tissues against radiotherapy-induced complications is also included.
Literature
1.
go back to reference Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A. Global cancer statistics 2012. CA Cancer J Clin. 2015;65(2):87–108.CrossRefPubMed Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A. Global cancer statistics 2012. CA Cancer J Clin. 2015;65(2):87–108.CrossRefPubMed
2.
go back to reference Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 2015;136(5):E359–86.CrossRefPubMed Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 2015;136(5):E359–86.CrossRefPubMed
3.
go back to reference Bentzen SM, Heeren G, Cottier B, Slotman B, Glimelius B, Lievens Y, et al. Towards evidence-based guidelines for radiotherapy infrastructure and staffing needs in Europe: the ESTRO QUARTS project. Radiother Oncol. 2005;75(3):355–65.CrossRefPubMed Bentzen SM, Heeren G, Cottier B, Slotman B, Glimelius B, Lievens Y, et al. Towards evidence-based guidelines for radiotherapy infrastructure and staffing needs in Europe: the ESTRO QUARTS project. Radiother Oncol. 2005;75(3):355–65.CrossRefPubMed
4.
go back to reference Liauw SL, Connell PP, Weichselbaum RR. New paradigms and future challenges in radiation oncology: an update of biological targets and technology. Sci Tansl Med. 2013;5(173):1732sr2-sr2. Liauw SL, Connell PP, Weichselbaum RR. New paradigms and future challenges in radiation oncology: an update of biological targets and technology. Sci Tansl Med. 2013;5(173):1732sr2-sr2.
5.
go back to reference Datta N, Ordóñez SG, Gaipl U, Paulides M, Crezee H, Gellermann J, et al. Local hyperthermia combined with radiotherapy and-/or chemotherapy: recent advances and promises for the future. Cancer Treat Rev. 2015;41(9):742–53.CrossRefPubMed Datta N, Ordóñez SG, Gaipl U, Paulides M, Crezee H, Gellermann J, et al. Local hyperthermia combined with radiotherapy and-/or chemotherapy: recent advances and promises for the future. Cancer Treat Rev. 2015;41(9):742–53.CrossRefPubMed
6.
go back to reference Hainfeld JF, Slatkin DN, Smilowitz HM. The use of gold nanoparticles to enhance radiotherapy in mice. Phys Med Biol. 2004;49(18):N309.CrossRefPubMed Hainfeld JF, Slatkin DN, Smilowitz HM. The use of gold nanoparticles to enhance radiotherapy in mice. Phys Med Biol. 2004;49(18):N309.CrossRefPubMed
7.
go back to reference Hood JD, Bednarski M, Frausto R, Guccione S, Reisfeld RA, Xiang R, et al. Tumor regression by targeted gene delivery to the neovasculature. Science. 2002;296(5577):2404–7.CrossRefPubMed Hood JD, Bednarski M, Frausto R, Guccione S, Reisfeld RA, Xiang R, et al. Tumor regression by targeted gene delivery to the neovasculature. Science. 2002;296(5577):2404–7.CrossRefPubMed
8.
go back to reference Higgins GS, O’Cathail SM, Muschel RJ, McKenna WG. Drug radiotherapy combinations: review of previous failures and reasons for future optimism. Cancer Treat Rev. 2015;41(2):105–13.CrossRefPubMed Higgins GS, O’Cathail SM, Muschel RJ, McKenna WG. Drug radiotherapy combinations: review of previous failures and reasons for future optimism. Cancer Treat Rev. 2015;41(2):105–13.CrossRefPubMed
9.
go back to reference Winczura P, Jassem J. Combined treatment with cytoprotective agents and radiotherapy. Cancer Treat Rev. 2010;36(3):268–75.CrossRefPubMed Winczura P, Jassem J. Combined treatment with cytoprotective agents and radiotherapy. Cancer Treat Rev. 2010;36(3):268–75.CrossRefPubMed
10.
go back to reference Formenti SC, Demaria S. Combining radiotherapy and cancer immunotherapy: a paradigm shift. J Natl Cancer Inst. 2013;105(4):256–65. Formenti SC, Demaria S. Combining radiotherapy and cancer immunotherapy: a paradigm shift. J Natl Cancer Inst. 2013;105(4):256–65.
11.
go back to reference Begg AC, Stewart FA, Vens C. Strategies to improve radiotherapy with targeted drugs. Nat Rev Cancer. 2011;11(4):239–53.CrossRefPubMed Begg AC, Stewart FA, Vens C. Strategies to improve radiotherapy with targeted drugs. Nat Rev Cancer. 2011;11(4):239–53.CrossRefPubMed
12.
go back to reference Richardson RB, Harper M-E. Mitochondrial stress controls the radiosensitivity of the oxygen effect: implications for radiotherapy. Oncotarget. 2016;7(16):21469.CrossRefPubMedPubMedCentral Richardson RB, Harper M-E. Mitochondrial stress controls the radiosensitivity of the oxygen effect: implications for radiotherapy. Oncotarget. 2016;7(16):21469.CrossRefPubMedPubMedCentral
13.
go back to reference Hill RP, Bristow RG, Fyles A, Koritzinsky M, Milosevic M, Wouters BG. Hypoxia and predicting radiation response. Semin Radiat Oncol. 2015;25(4):260–72.CrossRefPubMed Hill RP, Bristow RG, Fyles A, Koritzinsky M, Milosevic M, Wouters BG. Hypoxia and predicting radiation response. Semin Radiat Oncol. 2015;25(4):260–72.CrossRefPubMed
14.
go back to reference Chouaib S, Messai Y, Couve S, Escudier B, Hasmim M, Noman MZ. Hypoxia promotes tumor growth in linking angiogenesis to immune escape. Front Immunol. 2012;3:21.CrossRefPubMedPubMedCentral Chouaib S, Messai Y, Couve S, Escudier B, Hasmim M, Noman MZ. Hypoxia promotes tumor growth in linking angiogenesis to immune escape. Front Immunol. 2012;3:21.CrossRefPubMedPubMedCentral
15.
go back to reference Wang W-M, Zhao Z-L, Ma S-R, Yu G-T, Liu B, Zhang L, et al. Epidermal growth factor receptor inhibition reduces angiogenesis via hypoxia-inducible factor-1α and notch1 in head neck squamous cell carcinoma. PLoS One. 2015;10(2):e0119723.CrossRefPubMedPubMedCentral Wang W-M, Zhao Z-L, Ma S-R, Yu G-T, Liu B, Zhang L, et al. Epidermal growth factor receptor inhibition reduces angiogenesis via hypoxia-inducible factor-1α and notch1 in head neck squamous cell carcinoma. PLoS One. 2015;10(2):e0119723.CrossRefPubMedPubMedCentral
16.
18.
go back to reference Feng H, Wang J, Chen W, Shan B, Guo Y, Xu J, et al. Hypoxia-induced autophagy as an additional mechanism in human osteosarcoma radioresistance. J Bone Oncol. 2016;5(2):67–73.CrossRefPubMedPubMedCentral Feng H, Wang J, Chen W, Shan B, Guo Y, Xu J, et al. Hypoxia-induced autophagy as an additional mechanism in human osteosarcoma radioresistance. J Bone Oncol. 2016;5(2):67–73.CrossRefPubMedPubMedCentral
19.
go back to reference Corry J, Rischin D. Strategies to overcome accelerated repopulation and hypoxia—What have we learned from clinical trials? Semin Oncol. 2004;31(6):802–8.CrossRefPubMed Corry J, Rischin D. Strategies to overcome accelerated repopulation and hypoxia—What have we learned from clinical trials? Semin Oncol. 2004;31(6):802–8.CrossRefPubMed
20.
go back to reference Peters LJ. Targeting hypoxia in head and neck cancer. Act Oncol. 2001;40(8):937–40.CrossRef Peters LJ. Targeting hypoxia in head and neck cancer. Act Oncol. 2001;40(8):937–40.CrossRef
21.
go back to reference Moeller BJ, Richardson RA, Dewhirst MW. Hypoxia and radiotherapy: opportunities for improved outcomes in cancer treatment. Cancer Metastasis Rev. 2007;26(2):241–8.CrossRefPubMed Moeller BJ, Richardson RA, Dewhirst MW. Hypoxia and radiotherapy: opportunities for improved outcomes in cancer treatment. Cancer Metastasis Rev. 2007;26(2):241–8.CrossRefPubMed
22.
go back to reference Overgaard J, Horsman MR. Modification of hypoxia-induced radioresistance in tumors by the use of oxygen and sensitizers. Semin Radiat Oncol. 1996;6(1):10–21.CrossRefPubMed Overgaard J, Horsman MR. Modification of hypoxia-induced radioresistance in tumors by the use of oxygen and sensitizers. Semin Radiat Oncol. 1996;6(1):10–21.CrossRefPubMed
23.
go back to reference Rockwell S, Dobrucki IT, Kim EY, Marrison ST, Vu VT. Hypoxia and radiation therapy: past history, ongoing research, and future promise. Curr Mol Med. 2009;9(4):442–58.CrossRefPubMedPubMedCentral Rockwell S, Dobrucki IT, Kim EY, Marrison ST, Vu VT. Hypoxia and radiation therapy: past history, ongoing research, and future promise. Curr Mol Med. 2009;9(4):442–58.CrossRefPubMedPubMedCentral
24.
go back to reference Machtay M, Pajak TF, Suntharalingam M, Shenouda G, Hershock D, Stripp DC, et al. Radiotherapy with or without erythropoietin for anemic patients with head and neck cancer: a randomized trial of the Radiation Therapy Oncology Group (RTOG 99-03). Int J Radiat Oncol Biol Phys. 2007;69(4):1008–17.CrossRefPubMed Machtay M, Pajak TF, Suntharalingam M, Shenouda G, Hershock D, Stripp DC, et al. Radiotherapy with or without erythropoietin for anemic patients with head and neck cancer: a randomized trial of the Radiation Therapy Oncology Group (RTOG 99-03). Int J Radiat Oncol Biol Phys. 2007;69(4):1008–17.CrossRefPubMed
25.
go back to reference Varlotto J, Stevenson MA. Anemia, tumor hypoxemia, and the cancer patient. Int J Radiat Oncol Biol Phys. 2005;63(1):25–36.CrossRefPubMed Varlotto J, Stevenson MA. Anemia, tumor hypoxemia, and the cancer patient. Int J Radiat Oncol Biol Phys. 2005;63(1):25–36.CrossRefPubMed
26.
go back to reference Wardman P. Chemical radiosensitizers for use in radiotherapy. Clin Oncol. 2007;19(6):397–417.CrossRef Wardman P. Chemical radiosensitizers for use in radiotherapy. Clin Oncol. 2007;19(6):397–417.CrossRef
27.
go back to reference Denny WA, Wilson WR. Tirapazamine: a bioreductive anticancer drug that exploits tumour hypoxia. Exp Opin Invest Drugs. 2000;9(12):2889–901.CrossRef Denny WA, Wilson WR. Tirapazamine: a bioreductive anticancer drug that exploits tumour hypoxia. Exp Opin Invest Drugs. 2000;9(12):2889–901.CrossRef
28.
go back to reference Barnett GC, West CM, Dunning AM, Elliott RM, Coles CE, Pharoah PD, et al. Normal tissue reactions to radiotherapy: towards tailoring treatment dose by genotype. Nat Rev Cancer. 2009;9(2):134–42.CrossRefPubMedPubMedCentral Barnett GC, West CM, Dunning AM, Elliott RM, Coles CE, Pharoah PD, et al. Normal tissue reactions to radiotherapy: towards tailoring treatment dose by genotype. Nat Rev Cancer. 2009;9(2):134–42.CrossRefPubMedPubMedCentral
29.
go back to reference Rodemann HP, Blaese MA. Responses of normal cells to ionizing radiation. Semin Radiat Oncol. 2007;17(2):81–8.CrossRefPubMed Rodemann HP, Blaese MA. Responses of normal cells to ionizing radiation. Semin Radiat Oncol. 2007;17(2):81–8.CrossRefPubMed
30.
go back to reference Khanna KK, Jackson SP. DNA double-strand breaks: signaling, repair and the cancer connection. Nat Genet. 2001;27(3):247–54.CrossRefPubMed Khanna KK, Jackson SP. DNA double-strand breaks: signaling, repair and the cancer connection. Nat Genet. 2001;27(3):247–54.CrossRefPubMed
32.
33.
go back to reference Felgner S, Kocijancic D, Frahm M, Weiss S. Bacteria in cancer therapy: renaissance of an old concept. Int J Microbiol. 2016;8(45):17–28. Felgner S, Kocijancic D, Frahm M, Weiss S. Bacteria in cancer therapy: renaissance of an old concept. Int J Microbiol. 2016;8(45):17–28.
34.
go back to reference Nallar SC, Xu D-Q, Kalvakolanu DV. Bacteria and genetically modified bacteria as cancer therapeutics: current advances and challenges. Cytokine. 2017;89:160–72.CrossRefPubMed Nallar SC, Xu D-Q, Kalvakolanu DV. Bacteria and genetically modified bacteria as cancer therapeutics: current advances and challenges. Cytokine. 2017;89:160–72.CrossRefPubMed
36.
go back to reference Carswell E, Old LJ, Kassel R, Green S, Fiore N, Williamson B. An endotoxin-induced serum factor that causes necrosis of tumors. Proc Nat Acad Sci. 1975;72(9):3666–70.CrossRefPubMedPubMedCentral Carswell E, Old LJ, Kassel R, Green S, Fiore N, Williamson B. An endotoxin-induced serum factor that causes necrosis of tumors. Proc Nat Acad Sci. 1975;72(9):3666–70.CrossRefPubMedPubMedCentral
37.
go back to reference Nougayrède J-P, Taieb F, De Rycke J, Oswald E. Cyclomodulins: bacterial effectors that modulate the eukaryotic cell cycle. Trend Microbiol. 2005;13(3):103–10.CrossRef Nougayrède J-P, Taieb F, De Rycke J, Oswald E. Cyclomodulins: bacterial effectors that modulate the eukaryotic cell cycle. Trend Microbiol. 2005;13(3):103–10.CrossRef
38.
go back to reference Oswald E, Sugai M, Labigne A, Wu HC, Fiorentini C, Boquet P, et al. Cytotoxic necrotizing factor type 2 produced by virulent Escherichia coli modifies the small GTP-binding proteins Rho involved in assembly of actin stress fibers. Proc Nat Acad Sci. 1994;91(9):3814–8.CrossRefPubMedPubMedCentral Oswald E, Sugai M, Labigne A, Wu HC, Fiorentini C, Boquet P, et al. Cytotoxic necrotizing factor type 2 produced by virulent Escherichia coli modifies the small GTP-binding proteins Rho involved in assembly of actin stress fibers. Proc Nat Acad Sci. 1994;91(9):3814–8.CrossRefPubMedPubMedCentral
39.
41.
go back to reference Wei MQ, Ellem KA, Dunn P, West MJ, Bai CX, Vogelstein B. Facultative or obligate anaerobic bacteria have the potential for multimodality therapy of solid tumours. Eur J Cancer. 2007;43(3):490–6.CrossRefPubMed Wei MQ, Ellem KA, Dunn P, West MJ, Bai CX, Vogelstein B. Facultative or obligate anaerobic bacteria have the potential for multimodality therapy of solid tumours. Eur J Cancer. 2007;43(3):490–6.CrossRefPubMed
42.
go back to reference Ryan RM, Green J, Lewis CE. Use of bacteria in anti-cancer therapies. BioEssays. 2006;28(1):84–94.CrossRefPubMed Ryan RM, Green J, Lewis CE. Use of bacteria in anti-cancer therapies. BioEssays. 2006;28(1):84–94.CrossRefPubMed
43.
go back to reference Van Mellaert L, Barbé S, Anné J. Clostridium spores as anti-tumour agents. Trend Microbiol. 2006;14(4):190–6.CrossRef Van Mellaert L, Barbé S, Anné J. Clostridium spores as anti-tumour agents. Trend Microbiol. 2006;14(4):190–6.CrossRef
44.
45.
go back to reference Fensterle J, Bergmann B, Yone C, Hotz C, Meyer S, Spreng S, et al. Cancer immunotherapy based on recombinant Salmonella enterica serovar Typhimurium aroA strains secreting prostate-specific antigen and cholera toxin subunit B. Cancer Gene Ther. 2008;15(2):85–93.CrossRefPubMed Fensterle J, Bergmann B, Yone C, Hotz C, Meyer S, Spreng S, et al. Cancer immunotherapy based on recombinant Salmonella enterica serovar Typhimurium aroA strains secreting prostate-specific antigen and cholera toxin subunit B. Cancer Gene Ther. 2008;15(2):85–93.CrossRefPubMed
46.
go back to reference Zhao M, Yang M, Ma H, Li X, Tan X, Li S, et al. Targeted therapy with a Salmonella typhimurium leucine-arginine auxotroph cures orthotopic human breast tumors in nude mice. Cancer Res. 2006;66(15):7647–52.CrossRefPubMed Zhao M, Yang M, Ma H, Li X, Tan X, Li S, et al. Targeted therapy with a Salmonella typhimurium leucine-arginine auxotroph cures orthotopic human breast tumors in nude mice. Cancer Res. 2006;66(15):7647–52.CrossRefPubMed
47.
go back to reference Avogadri F, Martinoli C, Petrovska L, Chiodoni C, Transidico P, Bronte V, et al. Cancer immunotherapy based on killing of Salmonella-infected tumor cells. Cancer Res. 2005;65(9):3920–7.CrossRefPubMed Avogadri F, Martinoli C, Petrovska L, Chiodoni C, Transidico P, Bronte V, et al. Cancer immunotherapy based on killing of Salmonella-infected tumor cells. Cancer Res. 2005;65(9):3920–7.CrossRefPubMed
48.
go back to reference Frankel AE, Rossi P, Kuzel TM, Foss F. Diphtheria fusion protein therapy of chemoresistant malignancies. Curr Cancer Drug Targets. 2002;2(1):19–36.CrossRefPubMed Frankel AE, Rossi P, Kuzel TM, Foss F. Diphtheria fusion protein therapy of chemoresistant malignancies. Curr Cancer Drug Targets. 2002;2(1):19–36.CrossRefPubMed
49.
go back to reference Hagihara N, Walbridge S, Olson AW, Oldfield EH, Youle RJ. Vascular protection by chloroquine during brain tumor therapy with Tf-CRM107. Cancer Res. 2000;60(2):230–4.PubMed Hagihara N, Walbridge S, Olson AW, Oldfield EH, Youle RJ. Vascular protection by chloroquine during brain tumor therapy with Tf-CRM107. Cancer Res. 2000;60(2):230–4.PubMed
50.
go back to reference Xu J, Liu XS, Zhou S-F, Wei MQ. Combination of immunotherapy with anaerobic bacteria for immunogene therapy of solid tumours. Gene Ther Mol Biol. 2009;13:36–52. Xu J, Liu XS, Zhou S-F, Wei MQ. Combination of immunotherapy with anaerobic bacteria for immunogene therapy of solid tumours. Gene Ther Mol Biol. 2009;13:36–52.
51.
go back to reference Sznol M, Lin SL, Bermudes D, Zheng L-M, King I. Use of preferentially replicating bacteria for the treatment of cancer. J Clin Invest. 2000;105(8):1027–30.CrossRefPubMedPubMedCentral Sznol M, Lin SL, Bermudes D, Zheng L-M, King I. Use of preferentially replicating bacteria for the treatment of cancer. J Clin Invest. 2000;105(8):1027–30.CrossRefPubMedPubMedCentral
53.
go back to reference Parvez S, Malik KA, Ah Kang S, Kim HY. Probiotics and their fermented food products are beneficial for health. J Appl Microbiol. 2006;100(6):1171–85.CrossRefPubMed Parvez S, Malik KA, Ah Kang S, Kim HY. Probiotics and their fermented food products are beneficial for health. J Appl Microbiol. 2006;100(6):1171–85.CrossRefPubMed
54.
go back to reference Wollowski I, Rechkemmer G, Pool-Zobel BL. Protective role of probiotics and prebiotics in colon cancer. Am J Clin Nutr. 2001;73(2):451s–5s.PubMed Wollowski I, Rechkemmer G, Pool-Zobel BL. Protective role of probiotics and prebiotics in colon cancer. Am J Clin Nutr. 2001;73(2):451s–5s.PubMed
55.
go back to reference Bettegowda C, Dang LH, Abrams R, Huso DL, Dillehay L, Cheong I, et al. Overcoming the hypoxic barrier to radiation therapy with anaerobic bacteria. Proc Nat Acad Sci. 2003;100(25):15083–8.CrossRefPubMedPubMedCentral Bettegowda C, Dang LH, Abrams R, Huso DL, Dillehay L, Cheong I, et al. Overcoming the hypoxic barrier to radiation therapy with anaerobic bacteria. Proc Nat Acad Sci. 2003;100(25):15083–8.CrossRefPubMedPubMedCentral
56.
go back to reference Nuyts S, Van Mellaert L, Theys J, Landuyt W, Lambin P, Anné J. The use of radiation-induced bacterial promoters in anaerobic conditions: a means to control gene expression in clostridium-mediated therapy for cancer. Radiat Res. 2001;155(5):716–23.CrossRefPubMed Nuyts S, Van Mellaert L, Theys J, Landuyt W, Lambin P, Anné J. The use of radiation-induced bacterial promoters in anaerobic conditions: a means to control gene expression in clostridium-mediated therapy for cancer. Radiat Res. 2001;155(5):716–23.CrossRefPubMed
57.
go back to reference Nuyts S, Van Mellaert L, Theys J, Landuyt W, Bosmans E, Anné J, et al. Radio-responsive recA promoter significantly increases TNF [alpha] production in recombinant clostridia after 2 Gy irradiation. Gene Ther. 2001;8(15):1197.CrossRefPubMed Nuyts S, Van Mellaert L, Theys J, Landuyt W, Bosmans E, Anné J, et al. Radio-responsive recA promoter significantly increases TNF [alpha] production in recombinant clostridia after 2 Gy irradiation. Gene Ther. 2001;8(15):1197.CrossRefPubMed
58.
go back to reference Jiang S-N, Phan TX, Nam T-K, Nguyen VH, Kim H-S, Bom H-S, et al. Inhibition of tumor growth and metastasis by a combination of Escherichia coli–mediated cytolytic therapy and radiotherapy. Mol Ther. 2010;18(3):635–42.CrossRefPubMedPubMedCentral Jiang S-N, Phan TX, Nam T-K, Nguyen VH, Kim H-S, Bom H-S, et al. Inhibition of tumor growth and metastasis by a combination of Escherichia coli–mediated cytolytic therapy and radiotherapy. Mol Ther. 2010;18(3):635–42.CrossRefPubMedPubMedCentral
59.
go back to reference Platt J, Sodi S, Kelley M, Rockwell S, Bermudes D, Low K, et al. Antitumour effects of genetically engineered Salmonella in combination with radiation. Euro J Cancer. 2000;36(18):2397–402.CrossRef Platt J, Sodi S, Kelley M, Rockwell S, Bermudes D, Low K, et al. Antitumour effects of genetically engineered Salmonella in combination with radiation. Euro J Cancer. 2000;36(18):2397–402.CrossRef
60.
go back to reference Liu X, Jiang S, Piao L, Yuan F. Radiotherapy combined with an engineered Salmonella typhimurium inhibits tumor growth in a mouse model of colon cancer. Exp Anim. 2016;65(4):413–8.CrossRefPubMedPubMedCentral Liu X, Jiang S, Piao L, Yuan F. Radiotherapy combined with an engineered Salmonella typhimurium inhibits tumor growth in a mouse model of colon cancer. Exp Anim. 2016;65(4):413–8.CrossRefPubMedPubMedCentral
61.
go back to reference Abdollahi H. Beneficial effects of cellular autofluorescence following ionization radiation: hypothetical approaches for radiation protection and enhancing radiotherapy effectiveness. Med Hypotheses. 2015;84(3):194–8.CrossRefPubMed Abdollahi H. Beneficial effects of cellular autofluorescence following ionization radiation: hypothetical approaches for radiation protection and enhancing radiotherapy effectiveness. Med Hypotheses. 2015;84(3):194–8.CrossRefPubMed
62.
go back to reference Brizel DM, Wasserman TH, Henke M, Strnad V, Rudat V, Monnier A, et al. Phase III randomized trial of amifostine as a radioprotector in head and neck cancer. J Clin Oncol. 2000;18(19):3339–45.CrossRefPubMed Brizel DM, Wasserman TH, Henke M, Strnad V, Rudat V, Monnier A, et al. Phase III randomized trial of amifostine as a radioprotector in head and neck cancer. J Clin Oncol. 2000;18(19):3339–45.CrossRefPubMed
63.
go back to reference Abdollahi H. Probiotic-based protection of normal tissues during radiotherapy. Nutrition. 2014;30(4):495.CrossRefPubMed Abdollahi H. Probiotic-based protection of normal tissues during radiotherapy. Nutrition. 2014;30(4):495.CrossRefPubMed
64.
go back to reference Khademi S, Abdollahi H. Application of hydrogen producing microorganisms in radiotherapy: an idea. Iran J Public Health. 2014;43:1018–9.PubMedPubMedCentral Khademi S, Abdollahi H. Application of hydrogen producing microorganisms in radiotherapy: an idea. Iran J Public Health. 2014;43:1018–9.PubMedPubMedCentral
65.
go back to reference Abdollahi H, Shiri I, Atashzar M, Sarebani M, Moloudi K, Samadian H. Radiation protection and secondary cancer prevention using biological radioprotectors in radiotherapy. Int J Cancer Ther Oncol. 2015;3(3):1–9. Abdollahi H, Shiri I, Atashzar M, Sarebani M, Moloudi K, Samadian H. Radiation protection and secondary cancer prevention using biological radioprotectors in radiotherapy. Int J Cancer Ther Oncol. 2015;3(3):1–9.
66.
go back to reference Abdollahi H, Atashzar M, Amini M. The potential use of biogas producing microorganisms in radiation protection. J Med Hypotheses Ideas. 2015;9(2):67–71.CrossRef Abdollahi H, Atashzar M, Amini M. The potential use of biogas producing microorganisms in radiation protection. J Med Hypotheses Ideas. 2015;9(2):67–71.CrossRef
67.
go back to reference Group JFWW, Group JFWW. Guidelines for the evaluation of probiotics in food. London: World Health Organization, ON, Canada: Food and Agriculture Organization. 2002. Group JFWW, Group JFWW. Guidelines for the evaluation of probiotics in food. London: World Health Organization, ON, Canada: Food and Agriculture Organization. 2002.
68.
go back to reference Ciorba MA, Riehl TE, Rao MS, Moon C, Ee X, Nava GM, et al. Lactobacillus probiotic protects intestinal epithelium from radiation injury in a TLR-2/cyclo-oxygenase-2-dependent manner. Gut. 2012;61(6):829–38.CrossRefPubMed Ciorba MA, Riehl TE, Rao MS, Moon C, Ee X, Nava GM, et al. Lactobacillus probiotic protects intestinal epithelium from radiation injury in a TLR-2/cyclo-oxygenase-2-dependent manner. Gut. 2012;61(6):829–38.CrossRefPubMed
69.
go back to reference Demirer S, Aydıntug S, Aslım B, Kepenekci I, Sengül N, Evirgen O, et al. Effects of probiotics on radiation-induced intestinal injury in rats. Nutrition. 2006;22(2):179–86.CrossRefPubMed Demirer S, Aydıntug S, Aslım B, Kepenekci I, Sengül N, Evirgen O, et al. Effects of probiotics on radiation-induced intestinal injury in rats. Nutrition. 2006;22(2):179–86.CrossRefPubMed
70.
go back to reference Seal M, Naito Y, Barreto R, Lorenzetti A, Safran P, Marotta F. Experimental radiotherapy-induced enteritis: a probiotic interventional study. J Dig Dis. 2007;8(3):143–7.CrossRefPubMed Seal M, Naito Y, Barreto R, Lorenzetti A, Safran P, Marotta F. Experimental radiotherapy-induced enteritis: a probiotic interventional study. J Dig Dis. 2007;8(3):143–7.CrossRefPubMed
71.
go back to reference Mego M, Holec V, Drgona L, Hainova K, Ciernikova S, Zajac V. Probiotic bacteria in cancer patients undergoing chemotherapy and radiation therapy. Complement Ther Med. 2013;21(6):712–23.CrossRefPubMed Mego M, Holec V, Drgona L, Hainova K, Ciernikova S, Zajac V. Probiotic bacteria in cancer patients undergoing chemotherapy and radiation therapy. Complement Ther Med. 2013;21(6):712–23.CrossRefPubMed
72.
go back to reference Delia P, Sansotta G, Donato V, Frosina P, Messina G, De Renzis C, et al. Use of probiotics for prevention of radiation-induced diarrhea. World J Gastroenterol. 2007;13(6):912.CrossRefPubMedPubMedCentral Delia P, Sansotta G, Donato V, Frosina P, Messina G, De Renzis C, et al. Use of probiotics for prevention of radiation-induced diarrhea. World J Gastroenterol. 2007;13(6):912.CrossRefPubMedPubMedCentral
73.
go back to reference Sharma A, Rath G, Chaudhary S, Thakar A, Mohanti BK, Bahadur S. Lactobacillus brevis CD2 lozenges reduce radiation-and chemotherapy-induced mucositis in patients with head and neck cancer: a randomized double-blind placebo-controlled study. Eur J Cancer. 2012;48(6):875–81.CrossRefPubMed Sharma A, Rath G, Chaudhary S, Thakar A, Mohanti BK, Bahadur S. Lactobacillus brevis CD2 lozenges reduce radiation-and chemotherapy-induced mucositis in patients with head and neck cancer: a randomized double-blind placebo-controlled study. Eur J Cancer. 2012;48(6):875–81.CrossRefPubMed
74.
go back to reference Demers M, Dagnault A, Desjardins J. A randomized double-blind controlled trial: impact of probiotics on diarrhea in patients treated with pelvic radiation. Clin Nutr. 2014;33(5):761–7.CrossRefPubMed Demers M, Dagnault A, Desjardins J. A randomized double-blind controlled trial: impact of probiotics on diarrhea in patients treated with pelvic radiation. Clin Nutr. 2014;33(5):761–7.CrossRefPubMed
75.
go back to reference Österlund P, Ruotsalainen T, Korpela R, Saxelin M, Ollus A, Valta P, et al. Lactobacillus supplementation for diarrhoea related to chemotherapy of colorectal cancer: a randomised study. Br J Cancer. 2007;97(8):1028–34.CrossRefPubMedPubMedCentral Österlund P, Ruotsalainen T, Korpela R, Saxelin M, Ollus A, Valta P, et al. Lactobacillus supplementation for diarrhoea related to chemotherapy of colorectal cancer: a randomised study. Br J Cancer. 2007;97(8):1028–34.CrossRefPubMedPubMedCentral
76.
go back to reference Giralt J, Regadera JP, Verges R, Romero J, de la Fuente I, Biete A, et al. Effects of probiotic Lactobacillus casei DN-114 001 in prevention of radiation-induced diarrhea: results from multicenter, randomized, placebo-controlled nutritional trial. Int J Radiat Oncol Biol Phys. 2008;71(4):1213–9.CrossRefPubMed Giralt J, Regadera JP, Verges R, Romero J, de la Fuente I, Biete A, et al. Effects of probiotic Lactobacillus casei DN-114 001 in prevention of radiation-induced diarrhea: results from multicenter, randomized, placebo-controlled nutritional trial. Int J Radiat Oncol Biol Phys. 2008;71(4):1213–9.CrossRefPubMed
77.
go back to reference Delia P, Sansotta G, Donato V, Messina G, Frosina P, Pergolizzi S, et al. Prevention of radiation-induced diarrhea with the use of VSL# 3, a new high-potency probiotic preparation. Am J Gastroenterol. 2002;97(8):2150.CrossRefPubMed Delia P, Sansotta G, Donato V, Messina G, Frosina P, Pergolizzi S, et al. Prevention of radiation-induced diarrhea with the use of VSL# 3, a new high-potency probiotic preparation. Am J Gastroenterol. 2002;97(8):2150.CrossRefPubMed
81.
go back to reference Miladi I, Alric C, Dufort S, Mowat P, Dutour A, Mandon C, et al. The in vivo radiosensitizing effect of gold nanoparticles based MRI contrast agents. Small. 2014;10(6):1116–24.CrossRefPubMed Miladi I, Alric C, Dufort S, Mowat P, Dutour A, Mandon C, et al. The in vivo radiosensitizing effect of gold nanoparticles based MRI contrast agents. Small. 2014;10(6):1116–24.CrossRefPubMed
82.
go back to reference Detappe A, Lux F, Tillement O. Pushing radiation therapy limitations with theranostic nanoparticles. Nanomed. 2016;11(9):997–9.CrossRef Detappe A, Lux F, Tillement O. Pushing radiation therapy limitations with theranostic nanoparticles. Nanomed. 2016;11(9):997–9.CrossRef
83.
go back to reference Sancey L, Lux F, Kotb S, Roux S, Dufort S, Bianchi A, et al. The use of theranostic gadolinium-based nanoprobes to improve radiotherapy efficacy. Br J Radiol. 1041;2014(87):20140134. Sancey L, Lux F, Kotb S, Roux S, Dufort S, Bianchi A, et al. The use of theranostic gadolinium-based nanoprobes to improve radiotherapy efficacy. Br J Radiol. 1041;2014(87):20140134.
84.
go back to reference Park SJ, Park S-H, Cho S, Kim D-M, Lee Y, Ko SY, et al. New paradigm for tumor theranostic methodology using bacteria-based microrobot. Sci Rep. 2013;3:3394.CrossRefPubMedPubMedCentral Park SJ, Park S-H, Cho S, Kim D-M, Lee Y, Ko SY, et al. New paradigm for tumor theranostic methodology using bacteria-based microrobot. Sci Rep. 2013;3:3394.CrossRefPubMedPubMedCentral
85.
go back to reference Kojima R, Aubel D, Fussenegger M. Toward a world of theranostic medication: programming biological sentinel systems for therapeutic intervention. Adv Drug Deliv Rev. 2016;105:66–76.CrossRefPubMed Kojima R, Aubel D, Fussenegger M. Toward a world of theranostic medication: programming biological sentinel systems for therapeutic intervention. Adv Drug Deliv Rev. 2016;105:66–76.CrossRefPubMed
86.
go back to reference Wu HC, Tsao CY, Quan DN, Cheng Y, Servinsky MD, Carter KK, et al. Autonomous bacterial localization and gene expression based on nearby cell receptor density. Mol Syst Biol. 2013;9(1):636.CrossRefPubMedPubMedCentral Wu HC, Tsao CY, Quan DN, Cheng Y, Servinsky MD, Carter KK, et al. Autonomous bacterial localization and gene expression based on nearby cell receptor density. Mol Syst Biol. 2013;9(1):636.CrossRefPubMedPubMedCentral
87.
go back to reference Quispe-Tintaya W, Chandra D, Jahangir A, Harris M, Casadevall A, Dadachova E, et al. Nontoxic radioactive Listeriaat is a highly effective therapy against metastatic pancreatic cancer. Proc Nat Acad Sci. 2013;110(21):8668–73.CrossRefPubMedPubMedCentral Quispe-Tintaya W, Chandra D, Jahangir A, Harris M, Casadevall A, Dadachova E, et al. Nontoxic radioactive Listeriaat is a highly effective therapy against metastatic pancreatic cancer. Proc Nat Acad Sci. 2013;110(21):8668–73.CrossRefPubMedPubMedCentral
88.
go back to reference Luo C-H, Huang C-T, Su C-H, Yeh C-S. Bacteria-mediated hypoxia-specific delivery of nanoparticles for tumors imaging and therapy. Nano Lett. 2016;16(6):3493–9.CrossRefPubMed Luo C-H, Huang C-T, Su C-H, Yeh C-S. Bacteria-mediated hypoxia-specific delivery of nanoparticles for tumors imaging and therapy. Nano Lett. 2016;16(6):3493–9.CrossRefPubMed
89.
go back to reference Martel S, Mohammadi M, Felfoul O, Lu Z, Pouponneau P. Flagellated magnetotactic bacteria as controlled MRI-trackable propulsion and steering systems for medical nanorobots operating in the human microvasculature. Int J Robot Res. 2009;28(4):571–82.CrossRef Martel S, Mohammadi M, Felfoul O, Lu Z, Pouponneau P. Flagellated magnetotactic bacteria as controlled MRI-trackable propulsion and steering systems for medical nanorobots operating in the human microvasculature. Int J Robot Res. 2009;28(4):571–82.CrossRef
90.
go back to reference Zurkiya O, Chan AW, Hu X. MagA is sufficient for producing magnetic nanoparticles in mammalian cells, making it an MRI reporter. Mag Resonan Med. 2008;59(6):1225–31.CrossRef Zurkiya O, Chan AW, Hu X. MagA is sufficient for producing magnetic nanoparticles in mammalian cells, making it an MRI reporter. Mag Resonan Med. 2008;59(6):1225–31.CrossRef
91.
go back to reference Pfeifer F. Distribution, formation and regulation of gas vesicles. Nat Rev Microbiol. 2012;10(10):705–15.CrossRefPubMed Pfeifer F. Distribution, formation and regulation of gas vesicles. Nat Rev Microbiol. 2012;10(10):705–15.CrossRefPubMed
93.
go back to reference Shapiro MG, Goodwill PW, Neogy A, Yin M, Foster FS, Schaffer DV, et al. Biogenic gas nanostructures as ultrasonic molecular reporters. Nat Nanotechnol. 2014;9(4):311–6.CrossRefPubMedPubMedCentral Shapiro MG, Goodwill PW, Neogy A, Yin M, Foster FS, Schaffer DV, et al. Biogenic gas nanostructures as ultrasonic molecular reporters. Nat Nanotechnol. 2014;9(4):311–6.CrossRefPubMedPubMedCentral
94.
go back to reference Ibsen S, Schutt CE, Esener S. Microbubble-mediated ultrasound therapy: a review of its potential in cancer treatment. Drug Des Dev Ther. 2013;7:375–88.CrossRef Ibsen S, Schutt CE, Esener S. Microbubble-mediated ultrasound therapy: a review of its potential in cancer treatment. Drug Des Dev Ther. 2013;7:375–88.CrossRef
95.
go back to reference Kiessling F, Fokong S, Koczera P, Lederle W, Lammers T. Ultrasound microbubbles for molecular diagnosis, therapy, and theranostics. J Nucl Med. 2012;53(3):345–8.CrossRefPubMed Kiessling F, Fokong S, Koczera P, Lederle W, Lammers T. Ultrasound microbubbles for molecular diagnosis, therapy, and theranostics. J Nucl Med. 2012;53(3):345–8.CrossRefPubMed
96.
go back to reference Wang X, Gkanatsas Y, Palasubramaniam J, Hohmann JD, Chen YC, Lim B, et al. Thrombus-targeted theranostic microbubbles: a new technology towards concurrent rapid ultrasound diagnosis and bleeding-free fibrinolytic treatment of thrombosis. Theranostics. 2016;6(5):726.CrossRefPubMedPubMedCentral Wang X, Gkanatsas Y, Palasubramaniam J, Hohmann JD, Chen YC, Lim B, et al. Thrombus-targeted theranostic microbubbles: a new technology towards concurrent rapid ultrasound diagnosis and bleeding-free fibrinolytic treatment of thrombosis. Theranostics. 2016;6(5):726.CrossRefPubMedPubMedCentral
97.
go back to reference Jibu T, Ando K, Matsumoto T, Koike S, Kobori O, Morioka Y, et al. Active components of intestinal bacteria for abdominal irradiation-induced inhibition of lung metastases. Clin Exp Metastasis. 1991;9(6):529–40.CrossRefPubMed Jibu T, Ando K, Matsumoto T, Koike S, Kobori O, Morioka Y, et al. Active components of intestinal bacteria for abdominal irradiation-induced inhibition of lung metastases. Clin Exp Metastasis. 1991;9(6):529–40.CrossRefPubMed
98.
go back to reference Fang J, Liao L, Yin H, Nakamura H, Shin T, Maeda H. Enhanced bacterial tumor delivery by modulating the EPR effect and therapeutic potential of Lactobacillus casei. J Pharm Sci. 2014;103(10):3235–43.CrossRefPubMed Fang J, Liao L, Yin H, Nakamura H, Shin T, Maeda H. Enhanced bacterial tumor delivery by modulating the EPR effect and therapeutic potential of Lactobacillus casei. J Pharm Sci. 2014;103(10):3235–43.CrossRefPubMed
99.
go back to reference Dietzel F, Gericke D, König W. Tumor hyperthermia using high frequency for increase of oncolysis by Clostridium butyricum (M 55). Strahlentherapie. 1976;152(6):537–41.PubMed Dietzel F, Gericke D, König W. Tumor hyperthermia using high frequency for increase of oncolysis by Clostridium butyricum (M 55). Strahlentherapie. 1976;152(6):537–41.PubMed
100.
go back to reference Dietzel F, Gericke D. Intensification of the oncolysis by clostridia by means of radio-frequency hyperthermy in experiments on animals–dependence on dosage and on intervals (author’s transl). Strahlentherapie. 1977;153(4):263–6.PubMed Dietzel F, Gericke D. Intensification of the oncolysis by clostridia by means of radio-frequency hyperthermy in experiments on animals–dependence on dosage and on intervals (author’s transl). Strahlentherapie. 1977;153(4):263–6.PubMed
102.
go back to reference Kainthola A, Gupta N, Agrawala PK. Gastrointestinal microflora in radiation injury and countermeasure. Ann Res Rev Biol. 2016;10(1):1–22. Kainthola A, Gupta N, Agrawala PK. Gastrointestinal microflora in radiation injury and countermeasure. Ann Res Rev Biol. 2016;10(1):1–22.
103.
go back to reference Liu Q, Nobaek S, Adawi D, Mao Y, Wang M, Molin G, et al. Administration of Lactobacillus plantarum 299v reduces side‐effects of external radiation on colon anastomotic healing in an experimental model. Colorectal Dis. 2001;3(4):245–52. Liu Q, Nobaek S, Adawi D, Mao Y, Wang M, Molin G, et al. Administration of Lactobacillus plantarum 299v reduces side‐effects of external radiation on colon anastomotic healing in an experimental model. Colorectal Dis. 2001;3(4):245–52.
104.
go back to reference Chitapanarux I, Chitapanarux T, Traisathit P, Kudumpee S, Tharavichitkul E, Lorvidhaya V. Randomized controlled trial of live lactobacillus acidophilus plus bifidobacterium bifidum in prophylaxis of diarrhea during radiotherapy in cervical cancer patients. Radiat Oncol. 2010;5(1):31. Chitapanarux I, Chitapanarux T, Traisathit P, Kudumpee S, Tharavichitkul E, Lorvidhaya V. Randomized controlled trial of live lactobacillus acidophilus plus bifidobacterium bifidum in prophylaxis of diarrhea during radiotherapy in cervical cancer patients. Radiat Oncol. 2010;5(1):31.
105.
go back to reference Tanaka I, Tanaka M, Satoh A, Kurematsu A, Ishiwata A, Suzuki K, et al. Alteration of radioprotective effects of heat-killed Lactobacillus casei in X-irradiated C3H/He mouse related to blood level of proinflammatory cytokines by corticoids. J Radiat Res. 2010;51(1):81–6. Tanaka I, Tanaka M, Satoh A, Kurematsu A, Ishiwata A, Suzuki K, et al. Alteration of radioprotective effects of heat-killed Lactobacillus casei in X-irradiated C3H/He mouse related to blood level of proinflammatory cytokines by corticoids. J Radiat Res. 2010;51(1):81–6.
106.
go back to reference García-Peris P, Gimeno CV, Lozano M, Moreno Y, Paron L, de la Cuerda Compés C, et al. Effect of a mixture of inulin and fructo-oligosaccharide on lactobacillus and bifidobacterium intestinal microbiota of patients receiving radiotherapy; a randomised, double-blind, placebo-controlled trial. Nutr Hosp. 2012;27(6):1908–15. García-Peris P, Gimeno CV, Lozano M, Moreno Y, Paron L, de la Cuerda Compés C, et al. Effect of a mixture of inulin and fructo-oligosaccharide on lactobacillus and bifidobacterium intestinal microbiota of patients receiving radiotherapy; a randomised, double-blind, placebo-controlled trial. Nutr Hosp. 2012;27(6):1908–15.
107.
go back to reference Ki Y, Kim W, Cho H, Ahn K, Choi Y, Kim D. The effect of probiotics for preventing radiation-induced morphological changes in intestinal mucosa of rats. J Korean Med Sci. 2014;29(10):1372–8. Ki Y, Kim W, Cho H, Ahn K, Choi Y, Kim D. The effect of probiotics for preventing radiation-induced morphological changes in intestinal mucosa of rats. J Korean Med Sci. 2014;29(10):1372–8.
108.
go back to reference Nomoto K, Yokokura T, Tsuneoka K, Shikita M. Radioprotection of mice by a single subcutaneous injection of heat-killed Lactobacillus casei after irradiation. Radiation Res. 1991;125(3):293–7. Nomoto K, Yokokura T, Tsuneoka K, Shikita M. Radioprotection of mice by a single subcutaneous injection of heat-killed Lactobacillus casei after irradiation. Radiation Res. 1991;125(3):293–7.
Metadata
Title
The potential roles of bacteria to improve radiation treatment outcome
Authors
E. Kouhsari
A. Ghadimi-Daresajini
H. Abdollahi
N. Amirmozafari
S. R. Mahdavi
S. Abbasian
S. H. Mousavi
H. F. Yaseri
M. Moghaderi
Publication date
01-02-2018
Publisher
Springer International Publishing
Published in
Clinical and Translational Oncology / Issue 2/2018
Print ISSN: 1699-048X
Electronic ISSN: 1699-3055
DOI
https://doi.org/10.1007/s12094-017-1701-7

Other articles of this Issue 2/2018

Clinical and Translational Oncology 2/2018 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine