Skip to main content
Top
Published in: Journal of Experimental & Clinical Cancer Research 1/2021

Open Access 01-12-2021 | Checkpoint Inhibitors | Review

The role of the tumor microbe microenvironment in the tumor immune microenvironment: bystander, activator, or inhibitor?

Authors: Jiayao Ma, Lingjuan Huang, Die Hu, Shan Zeng, Ying Han, Hong Shen

Published in: Journal of Experimental & Clinical Cancer Research | Issue 1/2021

Login to get access

Abstract

The efficacy of cancer immunotherapy largely depends on the tumor microenvironment, especially the tumor immune microenvironment. Emerging studies have claimed that microbes reside within tumor cells and immune cells, suggesting that these microbes can impact the state of the tumor immune microenvironment. For the first time, this review delineates the landscape of intra-tumoral microbes and their products, herein defined as the tumor microbe microenvironment. The role of the tumor microbe microenvironment in the tumor immune microenvironment is multifaceted: either as an immune activator, inhibitor, or bystander. The underlying mechanisms include: (I) the presentation of microbial antigens by cancer cells and immune cells, (II) microbial antigens mimicry shared with tumor antigens, (III) microbe-induced immunogenic cell death, (IV) microbial adjuvanticity mediated by pattern recognition receptors, (V) microbe-derived metabolites, and (VI) microbial stimulation of inhibitory checkpoints. The review further suggests the use of potential modulation strategies of the tumor microbe microenvironment to enhance the efficacy and reduce the adverse effects of checkpoint inhibitors. Lastly, the review highlights some critical questions awaiting to be answered in this field and provides possible solutions. Overall, the tumor microbe microenvironment modulates the tumor immune microenvironment, making it a potential target for improving immunotherapy. It is a novel field facing major challenges and deserves further exploration.
Literature
5.
go back to reference Coley WB. The treatment of inoperable sarcoma by bacterial toxins (the mixed toxins of the Streptococcus erysipelas and the Bacillus prodigiosus). Proc R Soc Med. 1910;3:1–48.PubMedPubMedCentral Coley WB. The treatment of inoperable sarcoma by bacterial toxins (the mixed toxins of the Streptococcus erysipelas and the Bacillus prodigiosus). Proc R Soc Med. 1910;3:1–48.PubMedPubMedCentral
6.
go back to reference Grabstald H. Unproved methods of cancer treatment: Coley’s mixed toxins. CA Cancer J Clin. 1965;15:139–40.PubMedCrossRef Grabstald H. Unproved methods of cancer treatment: Coley’s mixed toxins. CA Cancer J Clin. 1965;15:139–40.PubMedCrossRef
7.
go back to reference Eisenhofer R, Minich JJ, Marotz C, Cooper A, Knight R, Weyrich LS. Contamination in low microbial biomass microbiome studies: issues and recommendations. Trends Microbiol. 2019;27:105–17.PubMedCrossRef Eisenhofer R, Minich JJ, Marotz C, Cooper A, Knight R, Weyrich LS. Contamination in low microbial biomass microbiome studies: issues and recommendations. Trends Microbiol. 2019;27:105–17.PubMedCrossRef
8.
go back to reference Knight R, Vrbanac A, Taylor BC, Aksenov A, Callewaert C, Debelius J, et al. Best practices for analysing microbiomes. Nat Rev Microbiol. 2018;16:410–22.PubMedCrossRef Knight R, Vrbanac A, Taylor BC, Aksenov A, Callewaert C, Debelius J, et al. Best practices for analysing microbiomes. Nat Rev Microbiol. 2018;16:410–22.PubMedCrossRef
9.
go back to reference Relman DA, Schmidt TM, MacDermott RP, Falkow S. Identification of the uncultured bacillus of Whipple’s disease. N Engl J Med. 1992;327:293–301.PubMedCrossRef Relman DA, Schmidt TM, MacDermott RP, Falkow S. Identification of the uncultured bacillus of Whipple’s disease. N Engl J Med. 1992;327:293–301.PubMedCrossRef
10.
go back to reference Poore GD, Kopylova E, Zhu Q, Carpenter C, Fraraccio S, Wandro S, et al. Microbiome analyses of blood and tissues suggest cancer diagnostic approach. Nature. 2020;579:567–74.PubMedPubMedCentralCrossRef Poore GD, Kopylova E, Zhu Q, Carpenter C, Fraraccio S, Wandro S, et al. Microbiome analyses of blood and tissues suggest cancer diagnostic approach. Nature. 2020;579:567–74.PubMedPubMedCentralCrossRef
11.
go back to reference Nejman D, Livyatan I, Fuks G, Gavert N, Zwang Y, Geller LT, et al. The human tumor microbiome is composed of tumor type-specific intracellular bacteria. Science. 2020;368:973–80.PubMedPubMedCentralCrossRef Nejman D, Livyatan I, Fuks G, Gavert N, Zwang Y, Geller LT, et al. The human tumor microbiome is composed of tumor type-specific intracellular bacteria. Science. 2020;368:973–80.PubMedPubMedCentralCrossRef
12.
go back to reference Doroshow DB, Bhalla S, Beasley MB, Sholl LM, Kerr KM, Gnjatic S, et al. PD-L1 as a biomarker of response to immune-checkpoint inhibitors. Nat Rev Clin Oncol. 2021;18:345–62.PubMedCrossRef Doroshow DB, Bhalla S, Beasley MB, Sholl LM, Kerr KM, Gnjatic S, et al. PD-L1 as a biomarker of response to immune-checkpoint inhibitors. Nat Rev Clin Oncol. 2021;18:345–62.PubMedCrossRef
13.
go back to reference Tang T, Huang X, Zhang G, Hong Z, Bai X, Liang T. Advantages of targeting the tumor immune microenvironment over blocking immune checkpoint in cancer immunotherapy. Signal Transduct Target Ther. 2021;6:72.PubMedPubMedCentralCrossRef Tang T, Huang X, Zhang G, Hong Z, Bai X, Liang T. Advantages of targeting the tumor immune microenvironment over blocking immune checkpoint in cancer immunotherapy. Signal Transduct Target Ther. 2021;6:72.PubMedPubMedCentralCrossRef
14.
go back to reference Binnewies M, Roberts EW, Kersten K, Chan V, Fearon DF, Merad M, et al. Understanding the tumor immune microenvironment (TIME) for effective therapy. Nat Med. 2018;24:541–50.PubMedPubMedCentralCrossRef Binnewies M, Roberts EW, Kersten K, Chan V, Fearon DF, Merad M, et al. Understanding the tumor immune microenvironment (TIME) for effective therapy. Nat Med. 2018;24:541–50.PubMedPubMedCentralCrossRef
15.
go back to reference Ren D, Hua Y, Yu B, Ye X, He Z, Li C, et al. Predictive biomarkers and mechanisms underlying resistance to PD1/PD-L1 blockade cancer immunotherapy. Mol Cancer. 2020;19:19.PubMedPubMedCentralCrossRef Ren D, Hua Y, Yu B, Ye X, He Z, Li C, et al. Predictive biomarkers and mechanisms underlying resistance to PD1/PD-L1 blockade cancer immunotherapy. Mol Cancer. 2020;19:19.PubMedPubMedCentralCrossRef
16.
go back to reference Finlay BB, Goldszmid R, Honda K, Trinchieri G, Wargo J, Zitvogel L. Can we harness the microbiota to enhance the efficacy of cancer immunotherapy? Nat Rev Immunol. 2020;20:522–8.PubMedCrossRef Finlay BB, Goldszmid R, Honda K, Trinchieri G, Wargo J, Zitvogel L. Can we harness the microbiota to enhance the efficacy of cancer immunotherapy? Nat Rev Immunol. 2020;20:522–8.PubMedCrossRef
17.
go back to reference Fu Y, Liu S, Zeng S, Shen H. From bench to bed: the tumor immune microenvironment and current immunotherapeutic strategies for hepatocellular carcinoma. J Exp Clin Cancer Res. 2019;38:396.PubMedPubMedCentralCrossRef Fu Y, Liu S, Zeng S, Shen H. From bench to bed: the tumor immune microenvironment and current immunotherapeutic strategies for hepatocellular carcinoma. J Exp Clin Cancer Res. 2019;38:396.PubMedPubMedCentralCrossRef
18.
go back to reference Chevrier S, Levine JH, Zanotelli VRT, Silina K, Schulz D, Bacac M, et al. An immune atlas of clear cell renal cell carcinoma. Cell. 2017;169:736–749.e718.PubMedPubMedCentralCrossRef Chevrier S, Levine JH, Zanotelli VRT, Silina K, Schulz D, Bacac M, et al. An immune atlas of clear cell renal cell carcinoma. Cell. 2017;169:736–749.e718.PubMedPubMedCentralCrossRef
19.
go back to reference Wagner J, Rapsomaniki MA, Chevrier S, Anzeneder T, Langwieder C, Dykgers A, et al. A single-cell atlas of the tumor and immune ecosystem of human breast cancer. Cell. 2019;177:1330–1345.e1318.PubMedPubMedCentralCrossRef Wagner J, Rapsomaniki MA, Chevrier S, Anzeneder T, Langwieder C, Dykgers A, et al. A single-cell atlas of the tumor and immune ecosystem of human breast cancer. Cell. 2019;177:1330–1345.e1318.PubMedPubMedCentralCrossRef
20.
21.
go back to reference Chapman NM, Boothby MR, Chi H. Metabolic coordination of T cell quiescence and activation. Nat Rev Immunol. 2020;20:55–70.PubMedCrossRef Chapman NM, Boothby MR, Chi H. Metabolic coordination of T cell quiescence and activation. Nat Rev Immunol. 2020;20:55–70.PubMedCrossRef
22.
go back to reference Cheng S, Li Z, Gao R, Xing B, Gao Y, Yang Y, et al. A pan-cancer single-cell transcriptional atlas of tumor infiltrating myeloid cells. Cell. 2021;184:792–809.e723.PubMedCrossRef Cheng S, Li Z, Gao R, Xing B, Gao Y, Yang Y, et al. A pan-cancer single-cell transcriptional atlas of tumor infiltrating myeloid cells. Cell. 2021;184:792–809.e723.PubMedCrossRef
23.
24.
go back to reference Law AMK, Valdes-Mora F, Gallego-Ortega D. Myeloid-derived suppressor cells as a therapeutic target for cancer. Cells. 2020;9:561.PubMedCentralCrossRef Law AMK, Valdes-Mora F, Gallego-Ortega D. Myeloid-derived suppressor cells as a therapeutic target for cancer. Cells. 2020;9:561.PubMedCentralCrossRef
26.
27.
go back to reference Aykut B, Pushalkar S, Chen R, Li Q, Abengozar R, Kim JI, et al. The fungal mycobiome promotes pancreatic oncogenesis via activation of MBL. Nature. 2019;574:264–7.PubMedPubMedCentralCrossRef Aykut B, Pushalkar S, Chen R, Li Q, Abengozar R, Kim JI, et al. The fungal mycobiome promotes pancreatic oncogenesis via activation of MBL. Nature. 2019;574:264–7.PubMedPubMedCentralCrossRef
28.
go back to reference Torres HA, Shigle TL, Hammoudi N, Link JT, Samaniego F, Kaseb A, et al. The oncologic burden of hepatitis C virus infection: a clinical perspective. CA Cancer J Clin. 2017;67:411–31.PubMedPubMedCentralCrossRef Torres HA, Shigle TL, Hammoudi N, Link JT, Samaniego F, Kaseb A, et al. The oncologic burden of hepatitis C virus infection: a clinical perspective. CA Cancer J Clin. 2017;67:411–31.PubMedPubMedCentralCrossRef
29.
go back to reference Young LS, Yap LF, Murray PG. Epstein-Barr virus: more than 50 years old and still providing surprises. Nat Rev Cancer. 2016;16:789–802.PubMedCrossRef Young LS, Yap LF, Murray PG. Epstein-Barr virus: more than 50 years old and still providing surprises. Nat Rev Cancer. 2016;16:789–802.PubMedCrossRef
30.
go back to reference Geller LT, Barzily-Rokni M, Danino T, Jonas OH, Shental N, Nejman D, et al. Potential role of intratumor bacteria in mediating tumor resistance to the chemotherapeutic drug gemcitabine. Science. 2017;357:1156–60.PubMedPubMedCentralCrossRef Geller LT, Barzily-Rokni M, Danino T, Jonas OH, Shental N, Nejman D, et al. Potential role of intratumor bacteria in mediating tumor resistance to the chemotherapeutic drug gemcitabine. Science. 2017;357:1156–60.PubMedPubMedCentralCrossRef
31.
go back to reference Apostolou P, Tsantsaridou A, Papasotiriou I, Toloudi M, Chatziioannou M, Giamouzis G. Bacterial and fungal microflora in surgically removed lung cancer samples. J Cardiothorac Surg. 2011;6:137.PubMedPubMedCentralCrossRef Apostolou P, Tsantsaridou A, Papasotiriou I, Toloudi M, Chatziioannou M, Giamouzis G. Bacterial and fungal microflora in surgically removed lung cancer samples. J Cardiothorac Surg. 2011;6:137.PubMedPubMedCentralCrossRef
32.
go back to reference Zagato E, Pozzi C, Bertocchi A, Schioppa T, Saccheri F, Guglietta S, et al. Endogenous murine microbiota member Faecalibaculum rodentium and its human homologue protect from intestinal tumour growth. Nat Microbiol. 2020;5:511–24.PubMedPubMedCentralCrossRef Zagato E, Pozzi C, Bertocchi A, Schioppa T, Saccheri F, Guglietta S, et al. Endogenous murine microbiota member Faecalibaculum rodentium and its human homologue protect from intestinal tumour growth. Nat Microbiol. 2020;5:511–24.PubMedPubMedCentralCrossRef
33.
go back to reference Mager LF, Burkhard R, Pett N, Cooke NCA, Brown K, Ramay H, et al. Microbiome-derived inosine modulates response to checkpoint inhibitor immunotherapy. Science (New York, NY). 2020;369:1481–9.CrossRef Mager LF, Burkhard R, Pett N, Cooke NCA, Brown K, Ramay H, et al. Microbiome-derived inosine modulates response to checkpoint inhibitor immunotherapy. Science (New York, NY). 2020;369:1481–9.CrossRef
34.
go back to reference Wang T, Gnanaprakasam JNR, Chen X, Kang S, Xu X, Sun H, et al. Inosine is an alternative carbon source for CD8(+)-T-cell function under glucose restriction. Nat Metab. 2020;2:635–47.PubMedPubMedCentralCrossRef Wang T, Gnanaprakasam JNR, Chen X, Kang S, Xu X, Sun H, et al. Inosine is an alternative carbon source for CD8(+)-T-cell function under glucose restriction. Nat Metab. 2020;2:635–47.PubMedPubMedCentralCrossRef
35.
go back to reference Allen-Vercoe E, Coburn B. A microbiota-derived metabolite augments cancer immunotherapy responses in mice. Cancer Cell. 2020;38:452–3.PubMedCrossRef Allen-Vercoe E, Coburn B. A microbiota-derived metabolite augments cancer immunotherapy responses in mice. Cancer Cell. 2020;38:452–3.PubMedCrossRef
36.
go back to reference Bitto NJ, Cheng L, Johnston EL, Pathirana R, Phan TK, Poon IKH, et al. Staphylococcus aureus membrane vesicles contain immunostimulatory DNA, RNA and peptidoglycan that activate innate immune receptors and induce autophagy. J Extracell Vesicles. 2021;10:e12080.PubMedPubMedCentralCrossRef Bitto NJ, Cheng L, Johnston EL, Pathirana R, Phan TK, Poon IKH, et al. Staphylococcus aureus membrane vesicles contain immunostimulatory DNA, RNA and peptidoglycan that activate innate immune receptors and induce autophagy. J Extracell Vesicles. 2021;10:e12080.PubMedPubMedCentralCrossRef
37.
go back to reference Xuan C, Shamonki JM, Chung A, Dinome ML, Chung M, Sieling PA, et al. Microbial dysbiosis is associated with human breast cancer. PLoS One. 2014;9:e83744.PubMedPubMedCentralCrossRef Xuan C, Shamonki JM, Chung A, Dinome ML, Chung M, Sieling PA, et al. Microbial dysbiosis is associated with human breast cancer. PLoS One. 2014;9:e83744.PubMedPubMedCentralCrossRef
38.
go back to reference Thompson KJ, Ingle JN, Tang X, Chia N, Jeraldo PR, Walther-Antonio MR, et al. A comprehensive analysis of breast cancer microbiota and host gene expression. PLoS One. 2017;12:e0188873.PubMedPubMedCentralCrossRef Thompson KJ, Ingle JN, Tang X, Chia N, Jeraldo PR, Walther-Antonio MR, et al. A comprehensive analysis of breast cancer microbiota and host gene expression. PLoS One. 2017;12:e0188873.PubMedPubMedCentralCrossRef
39.
go back to reference Gao Z, Guo B, Gao R, Zhu Q, Qin H. Microbiota disbiosis is associated with colorectal cancer. Front Microbiol. 2015;6:20.PubMedPubMedCentral Gao Z, Guo B, Gao R, Zhu Q, Qin H. Microbiota disbiosis is associated with colorectal cancer. Front Microbiol. 2015;6:20.PubMedPubMedCentral
40.
go back to reference Richard ML, Liguori G, Lamas B, Brandi G, da Costa G, Hoffmann TW, et al. Mucosa-associated microbiota dysbiosis in colitis associated cancer. Gut Microbes. 2018;9:131–142.PubMedCrossRef Richard ML, Liguori G, Lamas B, Brandi G, da Costa G, Hoffmann TW, et al. Mucosa-associated microbiota dysbiosis in colitis associated cancer. Gut Microbes. 2018;9:131–142.PubMedCrossRef
41.
go back to reference So KA, Yang EJ, Kim NR, Hong SR, Lee JH, Hwang CS, et al. Changes of vaginal microbiota during cervical carcinogenesis in women with human papillomavirus infection. PLoS One. 2020;15:e0238705.PubMedPubMedCentralCrossRef So KA, Yang EJ, Kim NR, Hong SR, Lee JH, Hwang CS, et al. Changes of vaginal microbiota during cervical carcinogenesis in women with human papillomavirus infection. PLoS One. 2020;15:e0238705.PubMedPubMedCentralCrossRef
42.
go back to reference Lee SH, Sung JY, Yong D, Chun J, Kim SY, Song JH, et al. Characterization of microbiome in bronchoalveolar lavage fluid of patients with lung cancer comparing with benign mass like lesions. Lung Cancer. 2016;102:89–95.PubMedCrossRef Lee SH, Sung JY, Yong D, Chun J, Kim SY, Song JH, et al. Characterization of microbiome in bronchoalveolar lavage fluid of patients with lung cancer comparing with benign mass like lesions. Lung Cancer. 2016;102:89–95.PubMedCrossRef
43.
go back to reference Greathouse KL, White JR, Vargas AJ, Bliskovsky VV, Beck JA, von Muhlinen N, et al. Interaction between the microbiome and TP53 in human lung cancer. Genome Biol. 2018;19:123.PubMedPubMedCentralCrossRef Greathouse KL, White JR, Vargas AJ, Bliskovsky VV, Beck JA, von Muhlinen N, et al. Interaction between the microbiome and TP53 in human lung cancer. Genome Biol. 2018;19:123.PubMedPubMedCentralCrossRef
44.
go back to reference Gnanasekar A, Castaneda G, Iyangar A, Magesh S, Perez D, Chakladar J, et al. The intratumor microbiome predicts prognosis across gender and subtypes in papillary thyroid carcinoma. Comput Struct Biotechnol J. 2021;19:1986–97.PubMedPubMedCentralCrossRef Gnanasekar A, Castaneda G, Iyangar A, Magesh S, Perez D, Chakladar J, et al. The intratumor microbiome predicts prognosis across gender and subtypes in papillary thyroid carcinoma. Comput Struct Biotechnol J. 2021;19:1986–97.PubMedPubMedCentralCrossRef
45.
go back to reference Abed J, Emgård JE, Zamir G, Faroja M, Almogy G, Grenov A, et al. Fap2 mediates Fusobacterium nucleatum colorectal adenocarcinoma enrichment by binding to tumor-expressed gal-GalNAc. Cell Host Microbe. 2016;20:215–25.PubMedPubMedCentralCrossRef Abed J, Emgård JE, Zamir G, Faroja M, Almogy G, Grenov A, et al. Fap2 mediates Fusobacterium nucleatum colorectal adenocarcinoma enrichment by binding to tumor-expressed gal-GalNAc. Cell Host Microbe. 2016;20:215–25.PubMedPubMedCentralCrossRef
46.
go back to reference Parhi L, Alon-Maimon T, Sol A, Nejman D, Shhadeh A, Fainsod-Levi T, et al. Breast cancer colonization by Fusobacterium nucleatum accelerates tumor growth and metastatic progression. Nat Commun. 2020;11:3259.PubMedPubMedCentralCrossRef Parhi L, Alon-Maimon T, Sol A, Nejman D, Shhadeh A, Fainsod-Levi T, et al. Breast cancer colonization by Fusobacterium nucleatum accelerates tumor growth and metastatic progression. Nat Commun. 2020;11:3259.PubMedPubMedCentralCrossRef
47.
go back to reference Cronin M, Akin AR, Collins SA, Meganck J, Kim JB, Baban CK, et al. High resolution in vivo bioluminescent imaging for the study of bacterial tumour targeting. PLoS One. 2012;7:e30940.PubMedPubMedCentralCrossRef Cronin M, Akin AR, Collins SA, Meganck J, Kim JB, Baban CK, et al. High resolution in vivo bioluminescent imaging for the study of bacterial tumour targeting. PLoS One. 2012;7:e30940.PubMedPubMedCentralCrossRef
48.
go back to reference Riquelme E, Zhang Y, Zhang L, Montiel M, Zoltan M, Dong W, et al. Tumor microbiome diversity and composition influence pancreatic cancer outcomes. Cell. 2019;178:795–806.e712.PubMedPubMedCentralCrossRef Riquelme E, Zhang Y, Zhang L, Montiel M, Zoltan M, Dong W, et al. Tumor microbiome diversity and composition influence pancreatic cancer outcomes. Cell. 2019;178:795–806.e712.PubMedPubMedCentralCrossRef
49.
go back to reference McPherson AC, Pandey SP, Bender MJ, Meisel M. Systemic immunoregulatory consequences of gut commensal translocation. Trends Immunol. 2021;42:137–50.PubMedCrossRef McPherson AC, Pandey SP, Bender MJ, Meisel M. Systemic immunoregulatory consequences of gut commensal translocation. Trends Immunol. 2021;42:137–50.PubMedCrossRef
50.
go back to reference Bertocchi A, Carloni S, Ravenda PS, Bertalot G, Spadoni I, Lo Cascio A, et al. Gut vascular barrier impairment leads to intestinal bacteria dissemination and colorectal cancer metastasis to liver. Cancer Cell. 2021;39:708–724.e711.PubMedCrossRef Bertocchi A, Carloni S, Ravenda PS, Bertalot G, Spadoni I, Lo Cascio A, et al. Gut vascular barrier impairment leads to intestinal bacteria dissemination and colorectal cancer metastasis to liver. Cancer Cell. 2021;39:708–724.e711.PubMedCrossRef
51.
go back to reference Sommariva M, Le Noci V, Bianchi F, Camelliti S, Balsari A, Tagliabue E, et al. The lung microbiota: role in maintaining pulmonary immune homeostasis and its implications in cancer development and therapy. Cell Mol Life Sci. 2020;77:2739–49.PubMedPubMedCentralCrossRef Sommariva M, Le Noci V, Bianchi F, Camelliti S, Balsari A, Tagliabue E, et al. The lung microbiota: role in maintaining pulmonary immune homeostasis and its implications in cancer development and therapy. Cell Mol Life Sci. 2020;77:2739–49.PubMedPubMedCentralCrossRef
52.
go back to reference Abed J, Maalouf N, Manson AL, Earl AM, Parhi L, Emgård JEM, et al. Colon cancer-associated may originate from the oral cavity and reach colon tumors via the circulatory system. Front Cell Infect Microbiol. 2020;10:400.PubMedPubMedCentralCrossRef Abed J, Maalouf N, Manson AL, Earl AM, Parhi L, Emgård JEM, et al. Colon cancer-associated may originate from the oral cavity and reach colon tumors via the circulatory system. Front Cell Infect Microbiol. 2020;10:400.PubMedPubMedCentralCrossRef
53.
go back to reference Liu Y-X, Qin Y, Chen T, Lu M, Qian X, Guo X, et al. A practical guide to amplicon and metagenomic analysis of microbiome data. Protein Cell. 2021;12:315–30.PubMedCrossRef Liu Y-X, Qin Y, Chen T, Lu M, Qian X, Guo X, et al. A practical guide to amplicon and metagenomic analysis of microbiome data. Protein Cell. 2021;12:315–30.PubMedCrossRef
54.
go back to reference Johnson JS, Spakowicz DJ, Hong B-Y, Petersen LM, Demkowicz P, Chen L, et al. Evaluation of 16S rRNA gene sequencing for species and strain-level microbiome analysis. Nat Commun. 2019;10:5029.PubMedPubMedCentralCrossRef Johnson JS, Spakowicz DJ, Hong B-Y, Petersen LM, Demkowicz P, Chen L, et al. Evaluation of 16S rRNA gene sequencing for species and strain-level microbiome analysis. Nat Commun. 2019;10:5029.PubMedPubMedCentralCrossRef
56.
go back to reference Liu W, Zhang X, Xu H, Li S, Lau HC, Chen Q, et al. Microbial community heterogeneity within colorectal neoplasia and its correlation with colorectal carcinogenesis. Gastroenterology. 2021;160:2395–408.PubMedCrossRef Liu W, Zhang X, Xu H, Li S, Lau HC, Chen Q, et al. Microbial community heterogeneity within colorectal neoplasia and its correlation with colorectal carcinogenesis. Gastroenterology. 2021;160:2395–408.PubMedCrossRef
57.
go back to reference Mima K, Sukawa Y, Nishihara R, Qian ZR, Yamauchi M, Inamura K, et al. Fusobacterium nucleatum and T cells in colorectal carcinoma. JAMA Oncol. 2015;1:653–61.PubMedPubMedCentralCrossRef Mima K, Sukawa Y, Nishihara R, Qian ZR, Yamauchi M, Inamura K, et al. Fusobacterium nucleatum and T cells in colorectal carcinoma. JAMA Oncol. 2015;1:653–61.PubMedPubMedCentralCrossRef
58.
go back to reference Borowsky J, Haruki K, Lau MC, Dias Costa A, Vayrynen JP, Ugai T, et al. Association of Fusobacterium nucleatum with specific T-cell subsets in the colorectal carcinoma microenvironment. Clin Cancer Res. 2021;27:2816–26.PubMedCrossRefPubMedCentral Borowsky J, Haruki K, Lau MC, Dias Costa A, Vayrynen JP, Ugai T, et al. Association of Fusobacterium nucleatum with specific T-cell subsets in the colorectal carcinoma microenvironment. Clin Cancer Res. 2021;27:2816–26.PubMedCrossRefPubMedCentral
59.
go back to reference Chen T, Li Q, Zhang X, Long R, Wu Y, Wu J, et al. TOX expression decreases with progression of colorectal cancers and is associated with CD4 T-cell density and Fusobacterium nucleatum infection. Hum Pathol. 2018;79:93–101.PubMedCrossRef Chen T, Li Q, Zhang X, Long R, Wu Y, Wu J, et al. TOX expression decreases with progression of colorectal cancers and is associated with CD4 T-cell density and Fusobacterium nucleatum infection. Hum Pathol. 2018;79:93–101.PubMedCrossRef
60.
go back to reference Lopès A, Billard E, Casse AH, Villéger R, Veziant J, Roche G, et al. Colibactin-positive Escherichia coli induce a procarcinogenic immune environment leading to immunotherapy resistance in colorectal cancer. Int J Cancer. 2020;146:3147–59.PubMedCrossRef Lopès A, Billard E, Casse AH, Villéger R, Veziant J, Roche G, et al. Colibactin-positive Escherichia coli induce a procarcinogenic immune environment leading to immunotherapy resistance in colorectal cancer. Int J Cancer. 2020;146:3147–59.PubMedCrossRef
61.
go back to reference Bossuet-Greif N, Vignard J, Taieb F, Mirey G, Dubois D, Petit C, et al. The colibactin genotoxin generates DNA interstrand cross-links in infected cells. mBio. 2018;9:e02393–17.PubMedPubMedCentralCrossRef Bossuet-Greif N, Vignard J, Taieb F, Mirey G, Dubois D, Petit C, et al. The colibactin genotoxin generates DNA interstrand cross-links in infected cells. mBio. 2018;9:e02393–17.PubMedPubMedCentralCrossRef
62.
go back to reference Gagnière J, Bonnin V, Jarrousse AS, Cardamone E, Agus A, Uhrhammer N, et al. Interactions between microsatellite instability and human gut colonization by Escherichia coli in colorectal cancer. Clin Sci (Lond). 2017;131:471–85.CrossRef Gagnière J, Bonnin V, Jarrousse AS, Cardamone E, Agus A, Uhrhammer N, et al. Interactions between microsatellite instability and human gut colonization by Escherichia coli in colorectal cancer. Clin Sci (Lond). 2017;131:471–85.CrossRef
63.
go back to reference Bonnet M, Buc E, Sauvanet P, Darcha C, Dubois D, Pereira B, et al. Colonization of the human gut by E. coli and colorectal cancer risk. Clin Cancer Res. 2014;20:859–67.PubMedCrossRef Bonnet M, Buc E, Sauvanet P, Darcha C, Dubois D, Pereira B, et al. Colonization of the human gut by E. coli and colorectal cancer risk. Clin Cancer Res. 2014;20:859–67.PubMedCrossRef
64.
go back to reference Eklöf V, Löfgren-Burström A, Zingmark C, Edin S, Larsson P, Karling P, et al. Cancer-associated fecal microbial markers in colorectal cancer detection. Int J Cancer. 2017;141:2528–36.PubMedPubMedCentralCrossRef Eklöf V, Löfgren-Burström A, Zingmark C, Edin S, Larsson P, Karling P, et al. Cancer-associated fecal microbial markers in colorectal cancer detection. Int J Cancer. 2017;141:2528–36.PubMedPubMedCentralCrossRef
65.
go back to reference Lee JA, Yoo SY, Oh HJ, Jeong S, Cho NY, Kang GH, et al. Differential immune microenvironmental features of microsatellite-unstable colorectal cancers according to Fusobacterium nucleatum status. Cancer Immunol Immunother. 2021;70:47–59.PubMedCrossRef Lee JA, Yoo SY, Oh HJ, Jeong S, Cho NY, Kang GH, et al. Differential immune microenvironmental features of microsatellite-unstable colorectal cancers according to Fusobacterium nucleatum status. Cancer Immunol Immunother. 2021;70:47–59.PubMedCrossRef
66.
go back to reference Ling Z, Shao L, Liu X, Cheng Y, Yan C, Mei Y, et al. Regulatory T cells and plasmacytoid dendritic cells within the tumor microenvironment in gastric cancer are correlated with gastric microbiota dysbiosis: a preliminary study. Front Immunol. 2019;10:533.PubMedPubMedCentralCrossRef Ling Z, Shao L, Liu X, Cheng Y, Yan C, Mei Y, et al. Regulatory T cells and plasmacytoid dendritic cells within the tumor microenvironment in gastric cancer are correlated with gastric microbiota dysbiosis: a preliminary study. Front Immunol. 2019;10:533.PubMedPubMedCentralCrossRef
67.
go back to reference Kostic AD, Chun E, Robertson L, Glickman JN, Gallini CA, Michaud M, et al. Fusobacterium nucleatum potentiates intestinal tumorigenesis and modulates the tumor-immune microenvironment. Cell Host Microbe. 2013;14:207–15.PubMedPubMedCentralCrossRef Kostic AD, Chun E, Robertson L, Glickman JN, Gallini CA, Michaud M, et al. Fusobacterium nucleatum potentiates intestinal tumorigenesis and modulates the tumor-immune microenvironment. Cell Host Microbe. 2013;14:207–15.PubMedPubMedCentralCrossRef
68.
go back to reference Jin C, Lagoudas GK, Zhao C, Bullman S, Bhutkar A, Hu B, et al. Commensal microbiota promote lung cancer development via γδ T cells. Cell. 2019;176:998–1013.e1016.PubMedPubMedCentralCrossRef Jin C, Lagoudas GK, Zhao C, Bullman S, Bhutkar A, Hu B, et al. Commensal microbiota promote lung cancer development via γδ T cells. Cell. 2019;176:998–1013.e1016.PubMedPubMedCentralCrossRef
69.
go back to reference Grivennikov SI, Wang K, Mucida D, Stewart CA, Schnabl B, Jauch D, et al. Adenoma-linked barrier defects and microbial products drive IL-23/IL-17-mediated tumour growth. Nature. 2012;491:254–8.PubMedPubMedCentralCrossRef Grivennikov SI, Wang K, Mucida D, Stewart CA, Schnabl B, Jauch D, et al. Adenoma-linked barrier defects and microbial products drive IL-23/IL-17-mediated tumour growth. Nature. 2012;491:254–8.PubMedPubMedCentralCrossRef
70.
go back to reference Jhunjhunwala S, Hammer C, Delamarre L. Antigen presentation in cancer: insights into tumour immunogenicity and immune evasion. Nat Rev Cancer. 2021;21:298–312.PubMedCrossRef Jhunjhunwala S, Hammer C, Delamarre L. Antigen presentation in cancer: insights into tumour immunogenicity and immune evasion. Nat Rev Cancer. 2021;21:298–312.PubMedCrossRef
71.
go back to reference Kalaora S, Nagler A, Nejman D, Alon M, Barbolin C, Barnea E, et al. Identification of bacteria-derived HLA-bound peptides in melanoma. Nature. 2021;592:138–43.PubMedCrossRef Kalaora S, Nagler A, Nejman D, Alon M, Barbolin C, Barnea E, et al. Identification of bacteria-derived HLA-bound peptides in melanoma. Nature. 2021;592:138–43.PubMedCrossRef
72.
go back to reference Sepich-Poore GD, Carter H, Knight R. Intratumoral bacteria generate a new class of therapeutically relevant tumor antigens in melanoma. Cancer Cell. 2021;39:601–3.PubMedCrossRef Sepich-Poore GD, Carter H, Knight R. Intratumoral bacteria generate a new class of therapeutically relevant tumor antigens in melanoma. Cancer Cell. 2021;39:601–3.PubMedCrossRef
73.
go back to reference Zitvogel L, Ayyoub M, Routy B, Kroemer G. Microbiome and anticancer immunosurveillance. Cell. 2016;165:276–87.PubMedCrossRef Zitvogel L, Ayyoub M, Routy B, Kroemer G. Microbiome and anticancer immunosurveillance. Cell. 2016;165:276–87.PubMedCrossRef
74.
go back to reference Snyder A, Makarov V, Merghoub T, Yuan J, Zaretsky JM, Desrichard A, et al. Genetic basis for clinical response to CTLA-4 blockade in melanoma. N Engl J Med. 2014;371:2189–99.PubMedPubMedCentralCrossRef Snyder A, Makarov V, Merghoub T, Yuan J, Zaretsky JM, Desrichard A, et al. Genetic basis for clinical response to CTLA-4 blockade in melanoma. N Engl J Med. 2014;371:2189–99.PubMedPubMedCentralCrossRef
75.
go back to reference Fluckiger A, Daillère R, Sassi M, Sixt BS, Liu P, Loos F, et al. Cross-reactivity between tumor MHC class I-restricted antigens and an enterococcal bacteriophage. Science. 2020;369:936–42.PubMedCrossRef Fluckiger A, Daillère R, Sassi M, Sixt BS, Liu P, Loos F, et al. Cross-reactivity between tumor MHC class I-restricted antigens and an enterococcal bacteriophage. Science. 2020;369:936–42.PubMedCrossRef
76.
go back to reference Bessell CA, Isser A, Havel JJ, Lee S, Bell DR, Hickey JW, et al. Commensal bacteria stimulate antitumor responses via T cell cross-reactivity. JCI Insight. 2020;5:e135597.PubMedCentralCrossRef Bessell CA, Isser A, Havel JJ, Lee S, Bell DR, Hickey JW, et al. Commensal bacteria stimulate antitumor responses via T cell cross-reactivity. JCI Insight. 2020;5:e135597.PubMedCentralCrossRef
77.
go back to reference Chiou SH, Tseng D, Reuben A, Mallajosyula V, Molina IS, Conley S, et al. Global analysis of shared T cell specificities in human non-small cell lung cancer enables HLA inference and antigen discovery. Immunity. 2021;54:586–602.e588.PubMedPubMedCentralCrossRef Chiou SH, Tseng D, Reuben A, Mallajosyula V, Molina IS, Conley S, et al. Global analysis of shared T cell specificities in human non-small cell lung cancer enables HLA inference and antigen discovery. Immunity. 2021;54:586–602.e588.PubMedPubMedCentralCrossRef
78.
go back to reference Groza D, Gehrig S, Kudela P, Holcmann M, Pirker C, Dinhof C, et al. Bacterial ghosts as adjuvant to oxaliplatin chemotherapy in colorectal carcinomatosis. Oncoimmunology. 2018;7:e1424676.PubMedPubMedCentralCrossRef Groza D, Gehrig S, Kudela P, Holcmann M, Pirker C, Dinhof C, et al. Bacterial ghosts as adjuvant to oxaliplatin chemotherapy in colorectal carcinomatosis. Oncoimmunology. 2018;7:e1424676.PubMedPubMedCentralCrossRef
80.
go back to reference Wang Y, Guo W, Wu X, Zhang Y, Mannion C, Brouchkov A, et al. Oncolytic bacteria and their potential role in bacterium-mediated tumour therapy: a conceptual analysis. J Cancer. 2019;10:4442–54.PubMedPubMedCentralCrossRef Wang Y, Guo W, Wu X, Zhang Y, Mannion C, Brouchkov A, et al. Oncolytic bacteria and their potential role in bacterium-mediated tumour therapy: a conceptual analysis. J Cancer. 2019;10:4442–54.PubMedPubMedCentralCrossRef
81.
go back to reference Liwinski T, Zheng D, Elinav E. The microbiome and cytosolic innate immune receptors. Immunol Rev. 2020;297:207–24.PubMedCrossRef Liwinski T, Zheng D, Elinav E. The microbiome and cytosolic innate immune receptors. Immunol Rev. 2020;297:207–24.PubMedCrossRef
82.
go back to reference Di Lorenzo A, Bolli E, Tarone L, Cavallo F, Conti L. Toll-like receptor 2 at the crossroad between cancer cells, the immune system, and the microbiota. Int J Mol Sci. 2020;21:9418.PubMedCentralCrossRef Di Lorenzo A, Bolli E, Tarone L, Cavallo F, Conti L. Toll-like receptor 2 at the crossroad between cancer cells, the immune system, and the microbiota. Int J Mol Sci. 2020;21:9418.PubMedCentralCrossRef
83.
go back to reference Pushalkar S, Hundeyin M, Daley D, Zambirinis CP, Kurz E, Mishra A, et al. The pancreatic cancer microbiome promotes oncogenesis by induction of innate and adaptive immune suppression. Cancer Discov. 2018;8:403–16.PubMedPubMedCentralCrossRef Pushalkar S, Hundeyin M, Daley D, Zambirinis CP, Kurz E, Mishra A, et al. The pancreatic cancer microbiome promotes oncogenesis by induction of innate and adaptive immune suppression. Cancer Discov. 2018;8:403–16.PubMedPubMedCentralCrossRef
84.
go back to reference Zhang Q, Ma C, Duan Y, Heinrich B, Rosato U, Diggs LP, et al. Gut microbiome directs hepatocytes to recruit MDSCs and promote cholangiocarcinoma. Cancer Discov. 2021;11:1248–67.PubMedCrossRef Zhang Q, Ma C, Duan Y, Heinrich B, Rosato U, Diggs LP, et al. Gut microbiome directs hepatocytes to recruit MDSCs and promote cholangiocarcinoma. Cancer Discov. 2021;11:1248–67.PubMedCrossRef
85.
go back to reference Chen T, Li Q, Wu J, Wu Y, Peng W, Li H, et al. Fusobacterium nucleatum promotes M2 polarization of macrophages in the microenvironment of colorectal tumours via a TLR4-dependent mechanism. Cancer Immunol Immunother. 2018;67:1635–46.PubMedCrossRef Chen T, Li Q, Wu J, Wu Y, Peng W, Li H, et al. Fusobacterium nucleatum promotes M2 polarization of macrophages in the microenvironment of colorectal tumours via a TLR4-dependent mechanism. Cancer Immunol Immunother. 2018;67:1635–46.PubMedCrossRef
86.
go back to reference Deng Y, Yang J, Qian J, Liu R, Huang E, Wang Y, et al. TLR1/TLR2 signaling blocks the suppression of monocytic myeloid-derived suppressor cell by promoting its differentiation into M1-type macrophage. Mol Immunol. 2019;112:266–73.PubMedCrossRef Deng Y, Yang J, Qian J, Liu R, Huang E, Wang Y, et al. TLR1/TLR2 signaling blocks the suppression of monocytic myeloid-derived suppressor cell by promoting its differentiation into M1-type macrophage. Mol Immunol. 2019;112:266–73.PubMedCrossRef
87.
go back to reference Müller E, Christopoulos PF, Halder S, Lunde A, Beraki K, Speth M, et al. Toll-like receptor ligands and interferon-γ synergize for induction of antitumor M1 macrophages. Front Immunol. 2017;8:1383.PubMedPubMedCentralCrossRef Müller E, Christopoulos PF, Halder S, Lunde A, Beraki K, Speth M, et al. Toll-like receptor ligands and interferon-γ synergize for induction of antitumor M1 macrophages. Front Immunol. 2017;8:1383.PubMedPubMedCentralCrossRef
88.
go back to reference Hoste E, Arwert EN, Lal R, South AP, Salas-Alanis JC, Murrell DF, et al. Innate sensing of microbial products promotes wound-induced skin cancer. Nat Commun. 2015;6:5932.PubMedCrossRef Hoste E, Arwert EN, Lal R, South AP, Salas-Alanis JC, Murrell DF, et al. Innate sensing of microbial products promotes wound-induced skin cancer. Nat Commun. 2015;6:5932.PubMedCrossRef
89.
go back to reference Kim JH, Kordahi MC, Chac D, DePaolo RW. Toll-like receptor-6 signaling prevents inflammation and impacts composition of the microbiota during inflammation-induced colorectal cancer. Cancer Prev Res (Phila). 2020;13:25–40.CrossRef Kim JH, Kordahi MC, Chac D, DePaolo RW. Toll-like receptor-6 signaling prevents inflammation and impacts composition of the microbiota during inflammation-induced colorectal cancer. Cancer Prev Res (Phila). 2020;13:25–40.CrossRef
91.
go back to reference Maisonneuve C, Tsang DKL, Foerster EG, Robert LM, Mukherjee T, Prescott D, et al. Nod1 promotes colorectal carcinogenesis by regulating the immunosuppressive functions of tumor-infiltrating myeloid cells. Cell Rep. 2021;34:108677.PubMedCrossRef Maisonneuve C, Tsang DKL, Foerster EG, Robert LM, Mukherjee T, Prescott D, et al. Nod1 promotes colorectal carcinogenesis by regulating the immunosuppressive functions of tumor-infiltrating myeloid cells. Cell Rep. 2021;34:108677.PubMedCrossRef
92.
go back to reference Singh N, Gurav A, Sivaprakasam S, Brady E, Padia R, Shi H, et al. Activation of Gpr109a, receptor for niacin and the commensal metabolite butyrate, suppresses colonic inflammation and carcinogenesis. Immunity. 2014;40:128–39.PubMedPubMedCentralCrossRef Singh N, Gurav A, Sivaprakasam S, Brady E, Padia R, Shi H, et al. Activation of Gpr109a, receptor for niacin and the commensal metabolite butyrate, suppresses colonic inflammation and carcinogenesis. Immunity. 2014;40:128–39.PubMedPubMedCentralCrossRef
93.
go back to reference He Y, Fu L, Li Y, Wang W, Gong M, Zhang J, et al. Gut microbial metabolites facilitate anticancer therapy efficacy by modulating cytotoxic CD8(+) T cell immunity. Cell Metab. 2021;33:988–1000.e1007.PubMedCrossRef He Y, Fu L, Li Y, Wang W, Gong M, Zhang J, et al. Gut microbial metabolites facilitate anticancer therapy efficacy by modulating cytotoxic CD8(+) T cell immunity. Cell Metab. 2021;33:988–1000.e1007.PubMedCrossRef
94.
go back to reference Yang W, Feng Y, Zhou J, Cheung OK, Cao J, Wang J, et al. A selective HDAC8 inhibitor potentiates antitumor immunity and efficacy of immune checkpoint blockade in hepatocellular carcinoma. Sci Transl Med. 2021;13:eaaz6804.PubMedCrossRef Yang W, Feng Y, Zhou J, Cheung OK, Cao J, Wang J, et al. A selective HDAC8 inhibitor potentiates antitumor immunity and efficacy of immune checkpoint blockade in hepatocellular carcinoma. Sci Transl Med. 2021;13:eaaz6804.PubMedCrossRef
95.
go back to reference Woods DM, Sodré AL, Villagra A, Sarnaik A, Sotomayor EM, Weber J. HDAC inhibition upregulates PD-1 ligands in melanoma and augments immunotherapy with PD-1 blockade. Cancer Immunol Res. 2015;3:1375–85.PubMedPubMedCentralCrossRef Woods DM, Sodré AL, Villagra A, Sarnaik A, Sotomayor EM, Weber J. HDAC inhibition upregulates PD-1 ligands in melanoma and augments immunotherapy with PD-1 blockade. Cancer Immunol Res. 2015;3:1375–85.PubMedPubMedCentralCrossRef
96.
go back to reference Booth L, Roberts JL, Poklepovic A, Kirkwood J, Dent P. HDAC inhibitors enhance the immunotherapy response of melanoma cells. Oncotarget. 2017;8:83155–70.PubMedPubMedCentralCrossRef Booth L, Roberts JL, Poklepovic A, Kirkwood J, Dent P. HDAC inhibitors enhance the immunotherapy response of melanoma cells. Oncotarget. 2017;8:83155–70.PubMedPubMedCentralCrossRef
97.
go back to reference Luu M, Weigand K, Wedi F, Breidenbend C, Leister H, Pautz S, et al. Regulation of the effector function of CD8(+) T cells by gut microbiota-derived metabolite butyrate. Sci Rep. 2018;8:14430.PubMedPubMedCentralCrossRef Luu M, Weigand K, Wedi F, Breidenbend C, Leister H, Pautz S, et al. Regulation of the effector function of CD8(+) T cells by gut microbiota-derived metabolite butyrate. Sci Rep. 2018;8:14430.PubMedPubMedCentralCrossRef
98.
go back to reference Coutzac C, Jouniaux JM, Paci A, Schmidt J, Mallardo D, Seck A, et al. Systemic short chain fatty acids limit antitumor effect of CTLA-4 blockade in hosts with cancer. Nat Commun. 2020;11:2168.PubMedPubMedCentralCrossRef Coutzac C, Jouniaux JM, Paci A, Schmidt J, Mallardo D, Seck A, et al. Systemic short chain fatty acids limit antitumor effect of CTLA-4 blockade in hosts with cancer. Nat Commun. 2020;11:2168.PubMedPubMedCentralCrossRef
99.
go back to reference Sipe LM, Chaib M, Pingili AK, Pierre JF, Makowski L. Microbiome, bile acids, and obesity: how microbially modified metabolites shape anti-tumor immunity. Immunol Rev. 2020;295:220–39.PubMedPubMedCentralCrossRef Sipe LM, Chaib M, Pingili AK, Pierre JF, Makowski L. Microbiome, bile acids, and obesity: how microbially modified metabolites shape anti-tumor immunity. Immunol Rev. 2020;295:220–39.PubMedPubMedCentralCrossRef
100.
go back to reference Ma C, Han M, Heinrich B, Fu Q, Zhang Q, Sandhu M, et al. Gut microbiome-mediated bile acid metabolism regulates liver cancer via NKT cells. Science. 2018;360:eaan5931.PubMedPubMedCentralCrossRef Ma C, Han M, Heinrich B, Fu Q, Zhang Q, Sandhu M, et al. Gut microbiome-mediated bile acid metabolism regulates liver cancer via NKT cells. Science. 2018;360:eaan5931.PubMedPubMedCentralCrossRef
101.
go back to reference Mossanen JC, Kohlhepp M, Wehr A, Krenkel O, Liepelt A, Roeth AA, et al. CXCR6 inhibits hepatocarcinogenesis by promoting natural killer T- and CD4(+) T-cell-dependent control of senescence. Gastroenterology. 2019;156:1877–1889.e1874.PubMedCrossRef Mossanen JC, Kohlhepp M, Wehr A, Krenkel O, Liepelt A, Roeth AA, et al. CXCR6 inhibits hepatocarcinogenesis by promoting natural killer T- and CD4(+) T-cell-dependent control of senescence. Gastroenterology. 2019;156:1877–1889.e1874.PubMedCrossRef
102.
go back to reference Rojo D, Hevia A, Bargiela R, López P, Cuervo A, González S, et al. Ranking the impact of human health disorders on gut metabolism: systemic lupus erythematosus and obesity as study cases. Sci Rep. 2015;5:8310.PubMedPubMedCentralCrossRef Rojo D, Hevia A, Bargiela R, López P, Cuervo A, González S, et al. Ranking the impact of human health disorders on gut metabolism: systemic lupus erythematosus and obesity as study cases. Sci Rep. 2015;5:8310.PubMedPubMedCentralCrossRef
104.
go back to reference Gur C, Ibrahim Y, Isaacson B, Yamin R, Abed J, Gamliel M, et al. Binding of the Fap2 protein of Fusobacterium nucleatum to human inhibitory receptor TIGIT protects tumors from immune cell attack. Immunity. 2015;42:344–55.PubMedPubMedCentralCrossRef Gur C, Ibrahim Y, Isaacson B, Yamin R, Abed J, Gamliel M, et al. Binding of the Fap2 protein of Fusobacterium nucleatum to human inhibitory receptor TIGIT protects tumors from immune cell attack. Immunity. 2015;42:344–55.PubMedPubMedCentralCrossRef
105.
go back to reference Gur C, Maalouf N, Shhadeh A, Berhani O, Singer BB, Bachrach G, et al. Fusobacterium nucleatum supresses anti-tumor immunity by activating CEACAM1. Oncoimmunology. 2019;8:e1581531.PubMedPubMedCentralCrossRef Gur C, Maalouf N, Shhadeh A, Berhani O, Singer BB, Bachrach G, et al. Fusobacterium nucleatum supresses anti-tumor immunity by activating CEACAM1. Oncoimmunology. 2019;8:e1581531.PubMedPubMedCentralCrossRef
106.
go back to reference Gur C, Maalouf N, Gerhard M, Singer BB, Emgård J, Temper V, et al. The helicobacter pylori HopQ outermembrane protein inhibits immune cell activities. Oncoimmunology. 2019;8:e1553487.PubMedPubMedCentralCrossRef Gur C, Maalouf N, Gerhard M, Singer BB, Emgård J, Temper V, et al. The helicobacter pylori HopQ outermembrane protein inhibits immune cell activities. Oncoimmunology. 2019;8:e1553487.PubMedPubMedCentralCrossRef
107.
go back to reference Javaheri A, Kruse T, Moonens K, Mejias-Luque R, Debraekeleer A, Asche CI, et al. Helicobacter pylori adhesin HopQ engages in a virulence-enhancing interaction with human CEACAMs. Nat Microbiol. 2016;2:16189.PubMedCrossRef Javaheri A, Kruse T, Moonens K, Mejias-Luque R, Debraekeleer A, Asche CI, et al. Helicobacter pylori adhesin HopQ engages in a virulence-enhancing interaction with human CEACAMs. Nat Microbiol. 2016;2:16189.PubMedCrossRef
108.
go back to reference Feng R, Zhao H, Xu J, Shen C. CD47: the next checkpoint target for cancer immunotherapy. Crit Rev Oncol Hematol. 2020;152:103014.PubMedCrossRef Feng R, Zhao H, Xu J, Shen C. CD47: the next checkpoint target for cancer immunotherapy. Crit Rev Oncol Hematol. 2020;152:103014.PubMedCrossRef
109.
go back to reference Shi Y, Zheng W, Yang K, Harris KG, Ni K, Xue L, et al. Intratumoral accumulation of gut microbiota facilitates CD47-based immunotherapy via STING signaling. J Exp Med. 2020;217:e20192282.PubMedPubMedCentralCrossRef Shi Y, Zheng W, Yang K, Harris KG, Ni K, Xue L, et al. Intratumoral accumulation of gut microbiota facilitates CD47-based immunotherapy via STING signaling. J Exp Med. 2020;217:e20192282.PubMedPubMedCentralCrossRef
110.
go back to reference Kalia VC, Patel SKS, Cho BK, Wood TK, Lee JK. Emerging applications of bacteria as antitumor agents. Semin Cancer Biol. 2021;S1044-579X(21)00140-1. Kalia VC, Patel SKS, Cho BK, Wood TK, Lee JK. Emerging applications of bacteria as antitumor agents. Semin Cancer Biol. 2021;S1044-579X(21)00140-1.
111.
go back to reference Roy S, Trinchieri G. Microbiota: a key orchestrator of cancer therapy. Nat Rev Cancer. 2017;17:271–85.PubMedCrossRef Roy S, Trinchieri G. Microbiota: a key orchestrator of cancer therapy. Nat Rev Cancer. 2017;17:271–85.PubMedCrossRef
112.
113.
go back to reference Bommareddy PK, Shettigar M, Kaufman HL. Integrating oncolytic viruses in combination cancer immunotherapy. Nat Rev Immunol. 2018;18:498–513.PubMedCrossRef Bommareddy PK, Shettigar M, Kaufman HL. Integrating oncolytic viruses in combination cancer immunotherapy. Nat Rev Immunol. 2018;18:498–513.PubMedCrossRef
114.
go back to reference Harrington K, Freeman DJ, Kelly B, Harper J, Soria JC. Optimizing oncolytic virotherapy in cancer treatment. Nat Rev Drug Discov. 2019;18:689–706.PubMedCrossRef Harrington K, Freeman DJ, Kelly B, Harper J, Soria JC. Optimizing oncolytic virotherapy in cancer treatment. Nat Rev Drug Discov. 2019;18:689–706.PubMedCrossRef
115.
go back to reference Twumasi-Boateng K, Pettigrew JL, Kwok YYE, Bell JC, Nelson BH. Oncolytic viruses as engineering platforms for combination immunotherapy. Nat Rev Cancer. 2018;18:419–32.PubMedCrossRef Twumasi-Boateng K, Pettigrew JL, Kwok YYE, Bell JC, Nelson BH. Oncolytic viruses as engineering platforms for combination immunotherapy. Nat Rev Cancer. 2018;18:419–32.PubMedCrossRef
116.
117.
go back to reference Lawson CE, Harcombe WR, Hatzenpichler R, Lindemann SR, Löffler FE, O'Malley MA, et al. Common principles and best practices for engineering microbiomes. Nat Rev Microbiol. 2019;17:725–41.PubMedPubMedCentralCrossRef Lawson CE, Harcombe WR, Hatzenpichler R, Lindemann SR, Löffler FE, O'Malley MA, et al. Common principles and best practices for engineering microbiomes. Nat Rev Microbiol. 2019;17:725–41.PubMedPubMedCentralCrossRef
118.
go back to reference Chowdhury S, Castro S, Coker C, Hinchliffe TE, Arpaia N, Danino T. Programmable bacteria induce durable tumor regression and systemic antitumor immunity. Nat Med. 2019;25:1057–63.PubMedPubMedCentralCrossRef Chowdhury S, Castro S, Coker C, Hinchliffe TE, Arpaia N, Danino T. Programmable bacteria induce durable tumor regression and systemic antitumor immunity. Nat Med. 2019;25:1057–63.PubMedPubMedCentralCrossRef
119.
go back to reference Leventhal DS, Sokolovska A, Li N, Plescia C, Kolodziej SA, Gallant CW, et al. Immunotherapy with engineered bacteria by targeting the STING pathway for anti-tumor immunity. Nat Commun. 2020;11:2739.PubMedPubMedCentralCrossRef Leventhal DS, Sokolovska A, Li N, Plescia C, Kolodziej SA, Gallant CW, et al. Immunotherapy with engineered bacteria by targeting the STING pathway for anti-tumor immunity. Nat Commun. 2020;11:2739.PubMedPubMedCentralCrossRef
120.
go back to reference Dong X, Pan P, Zheng DW, Bao P, Zeng X, Zhang XZ. Bioinorganic hybrid bacteriophage for modulation of intestinal microbiota to remodel tumor-immune microenvironment against colorectal cancer. Sci Adv. 2020;6:eaba1590.PubMedPubMedCentralCrossRef Dong X, Pan P, Zheng DW, Bao P, Zeng X, Zhang XZ. Bioinorganic hybrid bacteriophage for modulation of intestinal microbiota to remodel tumor-immune microenvironment against colorectal cancer. Sci Adv. 2020;6:eaba1590.PubMedPubMedCentralCrossRef
121.
go back to reference Kulkarni AA, Ebadi M, Zhang S, Meybodi MA, Ali AM, DeFor T, et al. Comparative analysis of antibiotic exposure association with clinical outcomes of chemotherapy versus immunotherapy across three tumour types. ESMO Open. 2020;5:e000803.PubMedPubMedCentralCrossRef Kulkarni AA, Ebadi M, Zhang S, Meybodi MA, Ali AM, DeFor T, et al. Comparative analysis of antibiotic exposure association with clinical outcomes of chemotherapy versus immunotherapy across three tumour types. ESMO Open. 2020;5:e000803.PubMedPubMedCentralCrossRef
122.
go back to reference Xu H, Xu X, Wang H, Ge W, Cao D. The association between antibiotics use and outcome of cancer patients treated with immune checkpoint inhibitors: a systematic review and meta-analysis. Crit Rev Oncol Hematol. 2020;149:102909.PubMedCrossRef Xu H, Xu X, Wang H, Ge W, Cao D. The association between antibiotics use and outcome of cancer patients treated with immune checkpoint inhibitors: a systematic review and meta-analysis. Crit Rev Oncol Hematol. 2020;149:102909.PubMedCrossRef
123.
go back to reference Cortellini A, Di Maio M, Nigro O, Leonetti A, Cortinovis DL, Aerts JG, et al. Differential influence of antibiotic therapy and other medications on oncological outcomes of patients with non-small cell lung cancer treated with first-line pembrolizumab versus cytotoxic chemotherapy. J Immunother Cancer. 2021;9:e002421.PubMedPubMedCentralCrossRef Cortellini A, Di Maio M, Nigro O, Leonetti A, Cortinovis DL, Aerts JG, et al. Differential influence of antibiotic therapy and other medications on oncological outcomes of patients with non-small cell lung cancer treated with first-line pembrolizumab versus cytotoxic chemotherapy. J Immunother Cancer. 2021;9:e002421.PubMedPubMedCentralCrossRef
124.
go back to reference Cortellini A, Ricciuti B, Facchinetti F, Alessi JVM, Venkatraman D, Dall'Olio FG, et al. Antibiotic-exposed patients with non-small-cell lung cancer preserve efficacy outcomes following first-line chemo-immunotherapy. Ann Oncol. 2021;S0923-7534(21)03973-9. Cortellini A, Ricciuti B, Facchinetti F, Alessi JVM, Venkatraman D, Dall'Olio FG, et al. Antibiotic-exposed patients with non-small-cell lung cancer preserve efficacy outcomes following first-line chemo-immunotherapy. Ann Oncol. 2021;S0923-7534(21)03973-9.
125.
go back to reference Bullman S, Pedamallu CS, Sicinska E, Clancy TE, Zhang X, Cai D, et al. Analysis of Fusobacterium persistence and antibiotic response in colorectal cancer. Science. 2017;358:1443–8.PubMedPubMedCentralCrossRef Bullman S, Pedamallu CS, Sicinska E, Clancy TE, Zhang X, Cai D, et al. Analysis of Fusobacterium persistence and antibiotic response in colorectal cancer. Science. 2017;358:1443–8.PubMedPubMedCentralCrossRef
126.
go back to reference Goubet AG, Wheeler R, Fluckiger A, Qu B, Lemaitre F, Iribarren K, et al. Multifaceted modes of action of the anticancer probiotic enterococcus hirae. Cell Death Differ. 2021;28:2276–95.PubMedCrossRef Goubet AG, Wheeler R, Fluckiger A, Qu B, Lemaitre F, Iribarren K, et al. Multifaceted modes of action of the anticancer probiotic enterococcus hirae. Cell Death Differ. 2021;28:2276–95.PubMedCrossRef
127.
go back to reference Anker JF, Naseem AF, Mok H, Schaeffer AJ, Abdulkadir SA, Thumbikat P. Multi-faceted immunomodulatory and tissue-tropic clinical bacterial isolate potentiates prostate cancer immunotherapy. Nat Commun. 2018;9:1591.PubMedPubMedCentralCrossRef Anker JF, Naseem AF, Mok H, Schaeffer AJ, Abdulkadir SA, Thumbikat P. Multi-faceted immunomodulatory and tissue-tropic clinical bacterial isolate potentiates prostate cancer immunotherapy. Nat Commun. 2018;9:1591.PubMedPubMedCentralCrossRef
Metadata
Title
The role of the tumor microbe microenvironment in the tumor immune microenvironment: bystander, activator, or inhibitor?
Authors
Jiayao Ma
Lingjuan Huang
Die Hu
Shan Zeng
Ying Han
Hong Shen
Publication date
01-12-2021
Publisher
BioMed Central
Published in
Journal of Experimental & Clinical Cancer Research / Issue 1/2021
Electronic ISSN: 1756-9966
DOI
https://doi.org/10.1186/s13046-021-02128-w

Other articles of this Issue 1/2021

Journal of Experimental & Clinical Cancer Research 1/2021 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