Skip to main content
Top
Published in: Discover Oncology 1/2023

Open Access 01-12-2023 | Review

Awareness of intratumoral bacteria and their potential application in cancer treatment

Authors: Yin Liang, Qiyan Li, Yulin Liu, Yajie Guo, Qingjiao Li

Published in: Discover Oncology | Issue 1/2023

Login to get access

Abstract

Hitherto, the recognition of the microbiota role in tumorigenesis and clinical studies mostly focused on the intestinal flora. In contrast to the gut microbiome, microorganisms resident in tumor tissue are in close contact with cancer cells and therefore have the potential to have similar or even different functional patterns to the gut flora. Some investigations have shown intratumoral bacteria, which might come from commensal microbiota in mucosal areas including the gastrointestinal tract and oral cavity, or from nearby normal tissues. The existence, origin, and interactions of intratumoral bacteria with the tumor microenvironment all contribute to intratumoral microorganism heterogeneity. Intratumoral bacteria have a significant role in tumor formation. They can contribute to cancer at the genetic level by secreting poisons that directly damage DNA and also intimately related to immune system response at the systemic level. Intratumoral bacteria have an impact on chemotherapy and immunotherapy in cancer. Importantly, various properties of bacteria such as targeting and ease of modification make them powerful candidates for precision therapy, and combining microbial therapies with other therapies is expected to improve the effectiveness of cancer treatment. In this review, we mainly described the heterogeneity and potential sources of intratumoral bacteria, overviewed the important mechanisms by which they were involved in tumor progression, and summarized their potential value in oncology therapy. At last, we highlight the problems of research in this field, and look forward to a new wave of studies using the various applications of intratumoral microorganisms in cancer therapy.
Literature
3.
go back to reference Cullin N, Azevedo Antunes C, Straussman R, Stein-Thoeringer CK, Elinav E. Microbiome and cancer. Cancer Cell. 2021;39:1317–41.PubMedCrossRef Cullin N, Azevedo Antunes C, Straussman R, Stein-Thoeringer CK, Elinav E. Microbiome and cancer. Cancer Cell. 2021;39:1317–41.PubMedCrossRef
4.
go back to reference Sadrekarimi H, Gardanova ZR, Bakhshesh M, Ebrahimzadeh F, Yaseri AF, Thangavelu L, Hasanpoor Z, Zadeh FA, Kahrizi MS. Emerging role of human microbiome in cancer development and response to therapy: special focus on intestinal microflora. J Transl Med. 2022;20:301.PubMedPubMedCentralCrossRef Sadrekarimi H, Gardanova ZR, Bakhshesh M, Ebrahimzadeh F, Yaseri AF, Thangavelu L, Hasanpoor Z, Zadeh FA, Kahrizi MS. Emerging role of human microbiome in cancer development and response to therapy: special focus on intestinal microflora. J Transl Med. 2022;20:301.PubMedPubMedCentralCrossRef
5.
go back to reference Fan X, Alekseyenko AV, Wu J, et al. Human oral microbiome and prospective risk for pancreatic cancer: a population-based nested case–control study. Gut. 2018;67:120–7.PubMedCrossRef Fan X, Alekseyenko AV, Wu J, et al. Human oral microbiome and prospective risk for pancreatic cancer: a population-based nested case–control study. Gut. 2018;67:120–7.PubMedCrossRef
6.
go back to reference Yang Y, Weng W, Peng J, et al. Fusobacterium nucleatum increases proliferation of colorectal cancer cells and tumor development in mice by activating toll-like receptor 4 signaling to nuclear factor – κB, and up-regulating expression of microRNA-21. Gastroenterology. 2017;152:851-866.e24.PubMedCrossRef Yang Y, Weng W, Peng J, et al. Fusobacterium nucleatum increases proliferation of colorectal cancer cells and tumor development in mice by activating toll-like receptor 4 signaling to nuclear factor – κB, and up-regulating expression of microRNA-21. Gastroenterology. 2017;152:851-866.e24.PubMedCrossRef
7.
go back to reference Gleeson FC, Jeraldo P, Levy MJ, et al. Composition, diversity and potential utility of intervention-naïve pancreatic cancer intratumoral microbiome signature profiling via endoscopic ultrasound. Gut. 2022;71:441–3.PubMedCrossRef Gleeson FC, Jeraldo P, Levy MJ, et al. Composition, diversity and potential utility of intervention-naïve pancreatic cancer intratumoral microbiome signature profiling via endoscopic ultrasound. Gut. 2022;71:441–3.PubMedCrossRef
8.
go back to reference Vannucci L, Stepankova R, Kozakova H, Fiserova A, Rossmann P, Tlaskalova-Hogenova H. Colorectal carcinogenesis in germ-free and conventionally reared rats: different intestinal environments affect the systemic immunity. Int J Oncol. 2008;32:609–17.PubMed Vannucci L, Stepankova R, Kozakova H, Fiserova A, Rossmann P, Tlaskalova-Hogenova H. Colorectal carcinogenesis in germ-free and conventionally reared rats: different intestinal environments affect the systemic immunity. Int J Oncol. 2008;32:609–17.PubMed
9.
go back to reference Mishra R, Rajsiglová L, Lukáč P, Tenti P, Šima P, Čaja F, Vannucci L. Spontaneous and induced tumors in germ-free animals: a general review. Med (Kaunas). 2021;57:260. Mishra R, Rajsiglová L, Lukáč P, Tenti P, Šima P, Čaja F, Vannucci L. Spontaneous and induced tumors in germ-free animals: a general review. Med (Kaunas). 2021;57:260.
10.
go back to reference Loman NJ, Constantinidou C, Christner M, et al. A culture-independent sequence-based metagenomics approach to the investigation of an outbreak of shiga-toxigenic Escherichia coli O104:H4. JAMA. 2013;309:1502.PubMedCrossRef Loman NJ, Constantinidou C, Christner M, et al. A culture-independent sequence-based metagenomics approach to the investigation of an outbreak of shiga-toxigenic Escherichia coli O104:H4. JAMA. 2013;309:1502.PubMedCrossRef
11.
go back to reference Kovács T, Mikó E, Ujlaki G, Sári Z, Bai P. The microbiome as a component of the tumor microenvironment. Adv Exp Med Biol. 2020;1225:137–53.PubMedCrossRef Kovács T, Mikó E, Ujlaki G, Sári Z, Bai P. The microbiome as a component of the tumor microenvironment. Adv Exp Med Biol. 2020;1225:137–53.PubMedCrossRef
12.
go back to reference Ma J, Huang L, Hu D, Zeng S, Han Y, Shen H. The role of the tumor microbe microenvironment in the tumor immune microenvironment: bystander, activator, or inhibitor? J Exp Clin Cancer Res. 2021;40:327.PubMedPubMedCentralCrossRef Ma J, Huang L, Hu D, Zeng S, Han Y, Shen H. The role of the tumor microbe microenvironment in the tumor immune microenvironment: bystander, activator, or inhibitor? J Exp Clin Cancer Res. 2021;40:327.PubMedPubMedCentralCrossRef
13.
go back to reference Nejman D, Livyatan I, Fuks G, 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, et al. The human tumor microbiome is composed of tumor type–specific intracellular bacteria. Science. 2020;368:973–80.PubMedPubMedCentralCrossRef
15.
go back to reference Matson V, Fessler J, Bao R, Chongsuwat T, Zha Y, Alegre M-L, Luke JJ, Gajewski TF. The commensal microbiome is associated with anti-PD-1 efficacy in metastatic melanoma patients. Science. 2018;359:104–8.PubMedPubMedCentralCrossRef Matson V, Fessler J, Bao R, Chongsuwat T, Zha Y, Alegre M-L, Luke JJ, Gajewski TF. The commensal microbiome is associated with anti-PD-1 efficacy in metastatic melanoma patients. Science. 2018;359:104–8.PubMedPubMedCentralCrossRef
17.
go back to reference Pushalkar S, Hundeyin M, Daley D, 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, et al. The pancreatic cancer microbiome promotes oncogenesis by induction of innate and adaptive immune suppression. Cancer Discov. 2018;8:403–16.PubMedPubMedCentralCrossRef
18.
go back to reference Bullman S, Pedamallu CS, Sicinska E, et al. Analysis of Fusobacterium persistence and antibiotic response in colorectal cancer. Science. 2017;358:1443–8.PubMedPubMedCentralCrossRef Bullman S, Pedamallu CS, Sicinska E, et al. Analysis of Fusobacterium persistence and antibiotic response in colorectal cancer. Science. 2017;358:1443–8.PubMedPubMedCentralCrossRef
19.
go back to reference Yuan L, Yang P, Wei G, Hu X, Chen S, Lu J, Yang L, He X, Bao G. Tumor microbiome diversity influences papillary thyroid cancer invasion. Commun Biol. 2022;5:864.PubMedPubMedCentralCrossRef Yuan L, Yang P, Wei G, Hu X, Chen S, Lu J, Yang L, He X, Bao G. Tumor microbiome diversity influences papillary thyroid cancer invasion. Commun Biol. 2022;5:864.PubMedPubMedCentralCrossRef
20.
go back to reference Estemalik J, Demko C, Bissada NF, Joshi N, Bodner D, Shankar E, Gupta S. Simultaneous detection of oral pathogens in subgingival plaque and prostatic fluid of men with periodontal and prostatic diseases. J Periodontol. 2017;88:823–9.PubMedCrossRef Estemalik J, Demko C, Bissada NF, Joshi N, Bodner D, Shankar E, Gupta S. Simultaneous detection of oral pathogens in subgingival plaque and prostatic fluid of men with periodontal and prostatic diseases. J Periodontol. 2017;88:823–9.PubMedCrossRef
21.
go back to reference Kostic AD, Chun E, Robertson L, 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, et al. Fusobacterium nucleatum potentiates intestinal tumorigenesis and modulates the tumor-immune microenvironment. Cell Host Microbe. 2013;14:207–15.PubMedPubMedCentralCrossRef
22.
go back to reference Abed J, Emgård JEM, Zamir G, 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 JEM, Zamir G, et al. Fap2 mediates Fusobacterium nucleatum colorectal adenocarcinoma enrichment by binding to tumor-expressed Gal-GalNAc. Cell Host Microbe. 2016;20:215–25.PubMedPubMedCentralCrossRef
23.
go back to reference Heymann CJF, Bard J-M, Heymann M-F, Heymann D, Bobin-Dubigeon C. The intratumoral microbiome: characterization methods and functional impact. Cancer Lett. 2021;522:63–79.PubMedCrossRef Heymann CJF, Bard J-M, Heymann M-F, Heymann D, Bobin-Dubigeon C. The intratumoral microbiome: characterization methods and functional impact. Cancer Lett. 2021;522:63–79.PubMedCrossRef
24.
go back to reference Andreassen A, Kure EH, Nielsen PS, Autrup H, Haugen A. Comparative synchronous fluorescence spectrophotometry and 32P-postlabelling analysis of PAH-DNA adducts in human lung and the relationship to TP53 mutations. Lung Cancer. 1997;2(16):265. Andreassen A, Kure EH, Nielsen PS, Autrup H, Haugen A. Comparative synchronous fluorescence spectrophotometry and 32P-postlabelling analysis of PAH-DNA adducts in human lung and the relationship to TP53 mutations. Lung Cancer. 1997;2(16):265.
25.
go back to reference Guo W, Zhang Y, Guo S, et al. Tumor microbiome contributes to an aggressive phenotype in the basal-like subtype of pancreatic cancer. Commun Biol. 2021;4:1019.PubMedPubMedCentralCrossRef Guo W, Zhang Y, Guo S, et al. Tumor microbiome contributes to an aggressive phenotype in the basal-like subtype of pancreatic cancer. Commun Biol. 2021;4:1019.PubMedPubMedCentralCrossRef
26.
go back to reference Liu W, Zhang X, Xu H, 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, et al. Microbial community heterogeneity within colorectal neoplasia and its correlation with colorectal carcinogenesis. Gastroenterology. 2021;160:2395–408.PubMedCrossRef
27.
go back to reference Galeano Niño JL, Wu H, LaCourse KD, et al. Effect of the intratumoral microbiota on spatial and cellular heterogeneity in cancer. Nature. 2022;611:810–7.PubMedPubMedCentralCrossRef Galeano Niño JL, Wu H, LaCourse KD, et al. Effect of the intratumoral microbiota on spatial and cellular heterogeneity in cancer. Nature. 2022;611:810–7.PubMedPubMedCentralCrossRef
30.
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
31.
go back to reference Sholl J, Sepich-Poore GD, Knight R, Pradeu T. Redrawing therapeutic boundaries: microbiota and cancer. Trends Cancer. 2022;8:87–97.PubMedCrossRef Sholl J, Sepich-Poore GD, Knight R, Pradeu T. Redrawing therapeutic boundaries: microbiota and cancer. Trends Cancer. 2022;8:87–97.PubMedCrossRef
33.
34.
go back to reference Baik SC, Youn HS, Chung MH, Lee WK, Cho MJ, Ko GH, Park CK, Kasai H, Rhee KH. Increased oxidative DNA damage in Helicobacter pylori-infected human gastric mucosa. Cancer Res. 1996;56:1279–82.PubMed Baik SC, Youn HS, Chung MH, Lee WK, Cho MJ, Ko GH, Park CK, Kasai H, Rhee KH. Increased oxidative DNA damage in Helicobacter pylori-infected human gastric mucosa. Cancer Res. 1996;56:1279–82.PubMed
35.
go back to reference Arthur JC, Gharaibeh RZ, Mühlbauer M, Perez-Chanona E, Uronis JM, McCafferty J, Fodor AA, Jobin C. Microbial genomic analysis reveals the essential role of inflammation in bacteria-induced colorectal cancer. Nat Commun. 2014;5:4724.PubMedCrossRef Arthur JC, Gharaibeh RZ, Mühlbauer M, Perez-Chanona E, Uronis JM, McCafferty J, Fodor AA, Jobin C. Microbial genomic analysis reveals the essential role of inflammation in bacteria-induced colorectal cancer. Nat Commun. 2014;5:4724.PubMedCrossRef
36.
go back to reference Valguarnera E, Wardenburg JB. Good gone bad: one toxin away from disease for Bacteroides fragilis. J Mol Biol. 2020;432:765–85.PubMedCrossRef Valguarnera E, Wardenburg JB. Good gone bad: one toxin away from disease for Bacteroides fragilis. J Mol Biol. 2020;432:765–85.PubMedCrossRef
38.
go back to reference Goodwin AC, Destefano Shields CE, Wu S, et al. Polyamine catabolism contributes to enterotoxigenic Bacteroides fragilis-induced colon tumorigenesis. Proc Natl Acad Sci USA. 2011;108:15354–9.PubMedPubMedCentralCrossRef Goodwin AC, Destefano Shields CE, Wu S, et al. Polyamine catabolism contributes to enterotoxigenic Bacteroides fragilis-induced colon tumorigenesis. Proc Natl Acad Sci USA. 2011;108:15354–9.PubMedPubMedCentralCrossRef
39.
go back to reference Lopez LR, Bleich RM, Arthur JC. Microbiota effects on carcinogenesis: initiation, promotion, and progression. Annu Rev Med. 2021;72:243–61.PubMedCrossRef Lopez LR, Bleich RM, Arthur JC. Microbiota effects on carcinogenesis: initiation, promotion, and progression. Annu Rev Med. 2021;72:243–61.PubMedCrossRef
40.
go back to reference Buti L, Spooner E, Van der Veen AG, Rappuoli R, Covacci A, Ploegh HL. Helicobacter pylori cytotoxin-associated gene A (CagA) subverts the apoptosis-stimulating protein of p53 (ASPP2) tumor suppressor pathway of the host. Proc Natl Acad Sci USA. 2011;108:9238–43.PubMedPubMedCentralCrossRef Buti L, Spooner E, Van der Veen AG, Rappuoli R, Covacci A, Ploegh HL. Helicobacter pylori cytotoxin-associated gene A (CagA) subverts the apoptosis-stimulating protein of p53 (ASPP2) tumor suppressor pathway of the host. Proc Natl Acad Sci USA. 2011;108:9238–43.PubMedPubMedCentralCrossRef
41.
go back to reference Alipour M. Molecular mechanism of Helicobacter pylori-induced gastric cancer. J Gastrointest Cancer. 2021;52:23–30.PubMedCrossRef Alipour M. Molecular mechanism of Helicobacter pylori-induced gastric cancer. J Gastrointest Cancer. 2021;52:23–30.PubMedCrossRef
42.
go back to reference Crusz SM, Balkwill FR. Inflammation and cancer: advances and new agents. Nat Rev Clin Oncol. 2015;12:584–96.PubMedCrossRef Crusz SM, Balkwill FR. Inflammation and cancer: advances and new agents. Nat Rev Clin Oncol. 2015;12:584–96.PubMedCrossRef
44.
go back to reference Rogovskii VS. The linkage between inflammation and immune tolerance: interfering with inflammation in cancer. Curr Cancer Drug Targets. 2017;17:325–32.PubMedCrossRef Rogovskii VS. The linkage between inflammation and immune tolerance: interfering with inflammation in cancer. Curr Cancer Drug Targets. 2017;17:325–32.PubMedCrossRef
45.
go back to reference Parkin DM, Hämmerl L, Ferlay J, Kantelhardt EJ. Cancer in Africa 2018: the role of infections. Int J Cancer. 2020;146:2089–103.PubMedCrossRef Parkin DM, Hämmerl L, Ferlay J, Kantelhardt EJ. Cancer in Africa 2018: the role of infections. Int J Cancer. 2020;146:2089–103.PubMedCrossRef
46.
go back to reference Hashimoto M, Kamphorst AO, Im SJ, Kissick HT, Pillai RN, Ramalingam SS, Araki K, Ahmed R. CD8 T cell exhaustion in chronic infection and cancer: opportunities for interventions. Annu Rev Med. 2018;69:301–18.PubMedCrossRef Hashimoto M, Kamphorst AO, Im SJ, Kissick HT, Pillai RN, Ramalingam SS, Araki K, Ahmed R. CD8 T cell exhaustion in chronic infection and cancer: opportunities for interventions. Annu Rev Med. 2018;69:301–18.PubMedCrossRef
47.
go back to reference Zhao H, Wu L, Yan G, Chen Y, Zhou M, Wu Y, Li Y. Inflammation and tumor progression: signaling pathways and targeted intervention. Sig Transduct Target Ther. 2021;6:1–46.CrossRef Zhao H, Wu L, Yan G, Chen Y, Zhou M, Wu Y, Li Y. Inflammation and tumor progression: signaling pathways and targeted intervention. Sig Transduct Target Ther. 2021;6:1–46.CrossRef
48.
go back to reference Tilg H, Adolph TE, Gerner RR, Moschen AR. The intestinal microbiota in colorectal cancer. Cancer Cell. 2018;33:954–64.PubMedCrossRef Tilg H, Adolph TE, Gerner RR, Moschen AR. The intestinal microbiota in colorectal cancer. Cancer Cell. 2018;33:954–64.PubMedCrossRef
49.
go back to reference Hoste E, Arwert EN, Lal R, South AP, Salas-Alanis JC, Murrell DF, Donati G, Watt FM. 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, Donati G, Watt FM. Innate sensing of microbial products promotes wound-induced skin cancer. Nat Commun. 2015;6:5932.PubMedCrossRef
50.
go back to reference Biswas SK, Mantovani A. Macrophage plasticity and interaction with lymphocyte subsets: cancer as a paradigm. Nat Immunol. 2010;11:889–96.PubMedCrossRef Biswas SK, Mantovani A. Macrophage plasticity and interaction with lymphocyte subsets: cancer as a paradigm. Nat Immunol. 2010;11:889–96.PubMedCrossRef
51.
go back to reference Udayasuryan B, Ahmad RN, Nguyen TTD, Umaña A, Monét Roberts L, Sobol P, Jones SD, Munson JM, Slade DJ, Verbridge SS. Fusobacterium nucleatum induces proliferation and migration in pancreatic cancer cells through host autocrine and paracrine signaling. Sci Signal. 2022;15:eabn4948.PubMedPubMedCentralCrossRef Udayasuryan B, Ahmad RN, Nguyen TTD, Umaña A, Monét Roberts L, Sobol P, Jones SD, Munson JM, Slade DJ, Verbridge SS. Fusobacterium nucleatum induces proliferation and migration in pancreatic cancer cells through host autocrine and paracrine signaling. Sci Signal. 2022;15:eabn4948.PubMedPubMedCentralCrossRef
52.
go back to reference Zhang Y, Weng Y, Gan H, Zhao X, Zhi F. Streptococcus gallolyticus conspires myeloid cells to promote tumorigenesis of inflammatory bowel disease. Biochem Biophys Res Commun. 2018;506:907–11.PubMedCrossRef Zhang Y, Weng Y, Gan H, Zhao X, Zhi F. Streptococcus gallolyticus conspires myeloid cells to promote tumorigenesis of inflammatory bowel disease. Biochem Biophys Res Commun. 2018;506:907–11.PubMedCrossRef
54.
go back to reference Gur C, Ibrahim Y, Isaacson B, 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, 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
55.
go back to reference Parhi L, Alon-Maimon T, Sol A, 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, et al. Breast cancer colonization by Fusobacterium nucleatum accelerates tumor growth and metastatic progression. Nat Commun. 2020;11:3259.PubMedPubMedCentralCrossRef
57.
go back to reference Malinowski B, Węsierska A, Zalewska K, Sokołowska MM, Bursiewicz W, Socha M, Ozorowski M, Pawlak-Osińska K, Wiciński M. The role of Tannerella forsythia and Porphyromonas gingivalis in pathogenesis of esophageal cancer. Infect Agent Cancer. 2019;14:3.PubMedPubMedCentralCrossRef Malinowski B, Węsierska A, Zalewska K, Sokołowska MM, Bursiewicz W, Socha M, Ozorowski M, Pawlak-Osińska K, Wiciński M. The role of Tannerella forsythia and Porphyromonas gingivalis in pathogenesis of esophageal cancer. Infect Agent Cancer. 2019;14:3.PubMedPubMedCentralCrossRef
58.
go back to reference Kong C, Yan X, Zhu Y, et al. Fusobacterium nucleatum promotes the development of colorectal cancer by activating a cytochrome P450/epoxyoctadecenoic acid axis via TLR4/Keap1/NRF2 signaling. Cancer Res. 2021;81:4485–98.PubMedCrossRef Kong C, Yan X, Zhu Y, et al. Fusobacterium nucleatum promotes the development of colorectal cancer by activating a cytochrome P450/epoxyoctadecenoic acid axis via TLR4/Keap1/NRF2 signaling. Cancer Res. 2021;81:4485–98.PubMedCrossRef
59.
go back to reference Zhang Y, Zhang L, Zheng S, et al. Fusobacterium nucleatum promotes colorectal cancer cells adhesion to endothelial cells and facilitates extravasation and metastasis by inducing ALPK1/NF-κB/ICAM1 axis. Gut Microbes. 2022;14:2038852.PubMedPubMedCentralCrossRef Zhang Y, Zhang L, Zheng S, et al. Fusobacterium nucleatum promotes colorectal cancer cells adhesion to endothelial cells and facilitates extravasation and metastasis by inducing ALPK1/NF-κB/ICAM1 axis. Gut Microbes. 2022;14:2038852.PubMedPubMedCentralCrossRef
60.
go back to reference Guo Y, Wang J, Zhou K, Lv J, Wang L, Gao S, Keller ET, Zhang Z-S, Wang Q, Yao Z. Cytotoxic necrotizing factor 1 promotes bladder cancer angiogenesis through activating RhoC. FASEB J. 2020;34:7927–40.PubMedCrossRef Guo Y, Wang J, Zhou K, Lv J, Wang L, Gao S, Keller ET, Zhang Z-S, Wang Q, Yao Z. Cytotoxic necrotizing factor 1 promotes bladder cancer angiogenesis through activating RhoC. FASEB J. 2020;34:7927–40.PubMedCrossRef
61.
go back to reference Guo Y, Zhang Z, Wei H, Wang J, Lv J, Zhang K, Keller ET, Yao Z, Wang Q. Cytotoxic necrotizing factor 1 promotes prostate cancer progression through activating the Cdc42-PAK1 axis. J Pathol. 2017;243:208–19.PubMedCrossRef Guo Y, Zhang Z, Wei H, Wang J, Lv J, Zhang K, Keller ET, Yao Z, Wang Q. Cytotoxic necrotizing factor 1 promotes prostate cancer progression through activating the Cdc42-PAK1 axis. J Pathol. 2017;243:208–19.PubMedCrossRef
62.
go back to reference Guo S, Chen J, Chen F, Zeng Q, Liu W-L, Zhang G. Exosomes derived from Fusobacterium nucleatum-infected colorectal cancer cells facilitate tumour metastasis by selectively carrying miR-1246/92b-3p/27a-3p and CXCL16. Gut. 2020;70(8):1507–19.CrossRef Guo S, Chen J, Chen F, Zeng Q, Liu W-L, Zhang G. Exosomes derived from Fusobacterium nucleatum-infected colorectal cancer cells facilitate tumour metastasis by selectively carrying miR-1246/92b-3p/27a-3p and CXCL16. Gut. 2020;70(8):1507–19.CrossRef
63.
go back to reference Domenis R, Cifù A, Marinò D, Fabris M, Niazi KR, Soon-Shiong P, Curcio F. Toll-like receptor-4 activation boosts the immunosuppressive properties of tumor cells-derived exosomes. Sci Rep. 2019;9:8457.PubMedPubMedCentralCrossRef Domenis R, Cifù A, Marinò D, Fabris M, Niazi KR, Soon-Shiong P, Curcio F. Toll-like receptor-4 activation boosts the immunosuppressive properties of tumor cells-derived exosomes. Sci Rep. 2019;9:8457.PubMedPubMedCentralCrossRef
64.
go back to reference He Y, Zhang Q, Yu X, Zhang S, Guo W. Overview of microbial profiles in human hepatocellular carcinoma and adjacent nontumor tissues. J Transl Med. 2023;21:68.PubMedPubMedCentralCrossRef He Y, Zhang Q, Yu X, Zhang S, Guo W. Overview of microbial profiles in human hepatocellular carcinoma and adjacent nontumor tissues. J Transl Med. 2023;21:68.PubMedPubMedCentralCrossRef
66.
go back to reference Holohan C, Van Schaeybroeck S, Longley DB, Johnston PG. Cancer drug resistance: an evolving paradigm. Nat Rev Cancer. 2013;13:714–26.PubMedCrossRef Holohan C, Van Schaeybroeck S, Longley DB, Johnston PG. Cancer drug resistance: an evolving paradigm. Nat Rev Cancer. 2013;13:714–26.PubMedCrossRef
67.
go back to reference McMillin DW, Negri JM, Mitsiades CS. The role of tumour-stromal interactions in modifying drug response: challenges and opportunities. Nat Rev Drug Discov. 2013;12:217–28.PubMedCrossRef McMillin DW, Negri JM, Mitsiades CS. The role of tumour-stromal interactions in modifying drug response: challenges and opportunities. Nat Rev Drug Discov. 2013;12:217–28.PubMedCrossRef
68.
69.
go back to reference Geller LT, Barzily-Rokni M, Danino T, 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, et al. Potential role of intratumor bacteria in mediating tumor resistance to the chemotherapeutic drug gemcitabine. Science. 2017;357:1156–60.PubMedPubMedCentralCrossRef
70.
go back to reference Lehouritis P, Cummins J, Stanton M, Murphy CT, McCarthy FO, Reid G, Urbaniak C, Byrne WL, Tangney M. Local bacteria affect the efficacy of chemotherapeutic drugs. Sci Rep. 2015;5:14554.PubMedPubMedCentralCrossRef Lehouritis P, Cummins J, Stanton M, Murphy CT, McCarthy FO, Reid G, Urbaniak C, Byrne WL, Tangney M. Local bacteria affect the efficacy of chemotherapeutic drugs. Sci Rep. 2015;5:14554.PubMedPubMedCentralCrossRef
71.
go back to reference Abbott M, Ustoyev Y. Cancer and the immune system: the history and background of immunotherapy. Semin Oncol Nurs. 2019;35:150923.PubMedCrossRef Abbott M, Ustoyev Y. Cancer and the immune system: the history and background of immunotherapy. Semin Oncol Nurs. 2019;35:150923.PubMedCrossRef
72.
go back to reference Alsaab HO, Sau S, Alzhrani R, Tatiparti K, Bhise K, Kashaw SK, Iyer AK. PD-1 and PD-L1 checkpoint signaling inhibition for cancer immunotherapy: mechanism, combinations, and clinical outcome. Front Pharmacol. 2017;8:561.PubMedPubMedCentralCrossRef Alsaab HO, Sau S, Alzhrani R, Tatiparti K, Bhise K, Kashaw SK, Iyer AK. PD-1 and PD-L1 checkpoint signaling inhibition for cancer immunotherapy: mechanism, combinations, and clinical outcome. Front Pharmacol. 2017;8:561.PubMedPubMedCentralCrossRef
73.
go back to reference Shi Y, Zheng W, Yang K, Harris KG, Ni K, Xue L, Lin W, Chang EB, Weichselbaum RR, Fu Y-X. 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, Lin W, Chang EB, Weichselbaum RR, Fu Y-X. Intratumoral accumulation of gut microbiota facilitates CD47-based immunotherapy via STING signaling. J Exp Med. 2020;217:e20192282.PubMedPubMedCentralCrossRef
74.
go back to reference Kalbasi A, Ribas A. Tumour-intrinsic resistance to immune checkpoint blockade. Nat Rev Immunol. 2020;20:25–39.PubMedCrossRef Kalbasi A, Ribas A. Tumour-intrinsic resistance to immune checkpoint blockade. Nat Rev Immunol. 2020;20:25–39.PubMedCrossRef
75.
go back to reference Shiao SL, Kershaw KM, Limon JJ, et al. Commensal bacteria and fungi differentially regulate tumor responses to radiation therapy. Cancer Cell. 2021;39:1202-1213.e6.PubMedPubMedCentralCrossRef Shiao SL, Kershaw KM, Limon JJ, et al. Commensal bacteria and fungi differentially regulate tumor responses to radiation therapy. Cancer Cell. 2021;39:1202-1213.e6.PubMedPubMedCentralCrossRef
76.
go back to reference Yoon WS, Kim S, Seo S, Park Y. Salmonella typhimurium with γ-radiation induced H2AX phosphorylation and apoptosis in melanoma. Biosci Biotechnol Biochem. 2014;78:1082–5.PubMedCrossRef Yoon WS, Kim S, Seo S, Park Y. Salmonella typhimurium with γ-radiation induced H2AX phosphorylation and apoptosis in melanoma. Biosci Biotechnol Biochem. 2014;78:1082–5.PubMedCrossRef
79.
go back to reference Thalmann GN, Sermier A, Rentsch C, Möhrle K, Cecchini MG, Studer UE. Urinary interleukin-8 and 18 predict the response of superficial bladder cancer to intravesical therapy with bacillus Calmette-Guerin. J Urol. 2000;164:2129–33.PubMedCrossRef Thalmann GN, Sermier A, Rentsch C, Möhrle K, Cecchini MG, Studer UE. Urinary interleukin-8 and 18 predict the response of superficial bladder cancer to intravesical therapy with bacillus Calmette-Guerin. J Urol. 2000;164:2129–33.PubMedCrossRef
80.
go back to reference Zhou S, Zhao Z, Lin Y, Gong S, Li F, Pan J, Li X, Gao Z, Zhao AZ. Suppression of pancreatic ductal adenocarcinoma growth by intratumoral delivery of attenuated Salmonella typhimurium using a dual fluorescent live tracking system. Cancer Biol Ther. 2016;17:732–40.PubMedPubMedCentralCrossRef Zhou S, Zhao Z, Lin Y, Gong S, Li F, Pan J, Li X, Gao Z, Zhao AZ. Suppression of pancreatic ductal adenocarcinoma growth by intratumoral delivery of attenuated Salmonella typhimurium using a dual fluorescent live tracking system. Cancer Biol Ther. 2016;17:732–40.PubMedPubMedCentralCrossRef
81.
go back to reference Chen J, Li T, Liang J, Huang Q, Huang J-D, Ke Y, Sun H. Current status of intratumour microbiome in cancer and engineered exogenous microbiota as a promising therapeutic strategy. Biomed Pharmacother. 2022;145:112443.PubMedCrossRef Chen J, Li T, Liang J, Huang Q, Huang J-D, Ke Y, Sun H. Current status of intratumour microbiome in cancer and engineered exogenous microbiota as a promising therapeutic strategy. Biomed Pharmacother. 2022;145:112443.PubMedCrossRef
82.
go back to reference Liang K, Liu Q, Li P, Luo H, Wang H, Kong Q. Genetically engineered Salmonella Typhimurium: recent advances in cancer therapy. Cancer Lett. 2019;448:168–81.PubMedCrossRef Liang K, Liu Q, Li P, Luo H, Wang H, Kong Q. Genetically engineered Salmonella Typhimurium: recent advances in cancer therapy. Cancer Lett. 2019;448:168–81.PubMedCrossRef
83.
go back to reference Chen Y, Du M, Yuan Z, Chen Z, Yan F. Spatiotemporal control of engineered bacteria to express interferon-γ by focused ultrasound for tumor immunotherapy. Nat Commun. 2022;13:4468.PubMedPubMedCentralCrossRef Chen Y, Du M, Yuan Z, Chen Z, Yan F. Spatiotemporal control of engineered bacteria to express interferon-γ by focused ultrasound for tumor immunotherapy. Nat Commun. 2022;13:4468.PubMedPubMedCentralCrossRef
84.
go back to reference Nelson MT, Pope CE, Marsh RL, et al. Human and extracellular DNA depletion for metagenomic analysis of complex clinical infection samples yields optimized viable microbiome profiles. Cell Rep. 2019;26:2227-2240.e5.PubMedPubMedCentralCrossRef Nelson MT, Pope CE, Marsh RL, et al. Human and extracellular DNA depletion for metagenomic analysis of complex clinical infection samples yields optimized viable microbiome profiles. Cell Rep. 2019;26:2227-2240.e5.PubMedPubMedCentralCrossRef
85.
go back to reference Chakladar J, Kuo SZ, Castaneda G, Li WT, Gnanasekar A, Yu MA, Chang EY, Wang XQ, Ongkeko WM. The pancreatic microbiome is associated with carcinogenesis and worse prognosis in males and smokers. Cancers. 2020;12:2672.PubMedPubMedCentralCrossRef Chakladar J, Kuo SZ, Castaneda G, Li WT, Gnanasekar A, Yu MA, Chang EY, Wang XQ, Ongkeko WM. The pancreatic microbiome is associated with carcinogenesis and worse prognosis in males and smokers. Cancers. 2020;12:2672.PubMedPubMedCentralCrossRef
86.
go back to reference Davis NM, Proctor DM, Holmes SP, Relman DA, Callahan BJ. Simple statistical identification and removal of contaminant sequences in marker-gene and metagenomics data. Microbiome. 2018;6:226.PubMedPubMedCentralCrossRef Davis NM, Proctor DM, Holmes SP, Relman DA, Callahan BJ. Simple statistical identification and removal of contaminant sequences in marker-gene and metagenomics data. Microbiome. 2018;6:226.PubMedPubMedCentralCrossRef
87.
go back to reference Finlay BB, Humans CIFAR, the Microbiome. Are noncommunicable diseases communicable? Science. 2020;367:250–1.PubMedCrossRef Finlay BB, Humans CIFAR, the Microbiome. Are noncommunicable diseases communicable? Science. 2020;367:250–1.PubMedCrossRef
88.
go back to reference Zheng W, Zhao S, Yin Y, Zhang H, Needham DM, Evans ED, Dai CL, Lu PJ, Alm EJ, Weitz DA. High-throughput, single-microbe genomics with strain resolution, applied to a human gut microbiome. Science. 2022;376:eabm1483.PubMedCrossRef Zheng W, Zhao S, Yin Y, Zhang H, Needham DM, Evans ED, Dai CL, Lu PJ, Alm EJ, Weitz DA. High-throughput, single-microbe genomics with strain resolution, applied to a human gut microbiome. Science. 2022;376:eabm1483.PubMedCrossRef
89.
go back to reference Ghaddar B, Biswas A, Harris C, Omary MB, Carpizo DR, Blaser MJ, De S. Tumor microbiome links cellular programs and immunity in pancreatic cancer. Cancer Cell. 2022;40:1240-1253.e5.PubMedCrossRef Ghaddar B, Biswas A, Harris C, Omary MB, Carpizo DR, Blaser MJ, De S. Tumor microbiome links cellular programs and immunity in pancreatic cancer. Cancer Cell. 2022;40:1240-1253.e5.PubMedCrossRef
90.
go back to reference Li Z, Fu R, Wen X, Wang Q, Huang X, Zhang L. The significant clinical correlation of the intratumor oral microbiome in oral squamous cell carcinoma based on tissue-derived sequencing. Front Physiol. 2023;13:1089539.PubMedPubMedCentralCrossRef Li Z, Fu R, Wen X, Wang Q, Huang X, Zhang L. The significant clinical correlation of the intratumor oral microbiome in oral squamous cell carcinoma based on tissue-derived sequencing. Front Physiol. 2023;13:1089539.PubMedPubMedCentralCrossRef
91.
go back to reference Ishaq HM, Mohammad IS, Sher Muhammad K, et al. Gut microbial dysbiosis and its association with esophageal cancer. J Appl Biomed. 2021;19:1–13.PubMedCrossRef Ishaq HM, Mohammad IS, Sher Muhammad K, et al. Gut microbial dysbiosis and its association with esophageal cancer. J Appl Biomed. 2021;19:1–13.PubMedCrossRef
92.
go back to reference Cass S, Hamilton C, Miller A, Jupiter D, Khanipov K, Booth A, Pyles R, Krill T, Reep G, Okereke I. Novel ex vivo model to examine the mechanism and relationship of esophageal microbiota and disease. Biomedicines. 2021;9:142.PubMedPubMedCentralCrossRef Cass S, Hamilton C, Miller A, Jupiter D, Khanipov K, Booth A, Pyles R, Krill T, Reep G, Okereke I. Novel ex vivo model to examine the mechanism and relationship of esophageal microbiota and disease. Biomedicines. 2021;9:142.PubMedPubMedCentralCrossRef
93.
go back to reference Deng Y, Tang D, Hou P, Shen W, Li H, Wang T, Liu R. Dysbiosis of gut microbiota in patients with esophageal cancer. Microb Pathog. 2021;150:104709.PubMedCrossRef Deng Y, Tang D, Hou P, Shen W, Li H, Wang T, Liu R. Dysbiosis of gut microbiota in patients with esophageal cancer. Microb Pathog. 2021;150:104709.PubMedCrossRef
94.
go back to reference Yamamura K, Baba Y, Nakagawa S, et al. Human microbiome Fusobacterium nucleatum in esophageal cancer tissue is associated with prognosis. Clin Cancer Res. 2016;22:5574–81.PubMedCrossRef Yamamura K, Baba Y, Nakagawa S, et al. Human microbiome Fusobacterium nucleatum in esophageal cancer tissue is associated with prognosis. Clin Cancer Res. 2016;22:5574–81.PubMedCrossRef
95.
96.
go back to reference Komiyama S, Yamada T, Takemura N, Kokudo N, Hase K, Kawamura YI. Profiling of tumour-associated microbiota in human hepatocellular carcinoma. Sci Rep. 2021;11:10589.PubMedPubMedCentralCrossRef Komiyama S, Yamada T, Takemura N, Kokudo N, Hase K, Kawamura YI. Profiling of tumour-associated microbiota in human hepatocellular carcinoma. Sci Rep. 2021;11:10589.PubMedPubMedCentralCrossRef
97.
go back to reference Huang H, Ren Z, Gao X, et al. Integrated analysis of microbiome and host transcriptome reveals correlations between gut microbiota and clinical outcomes in HBV-related hepatocellular carcinoma. Genome Med. 2020;12:102.PubMedPubMedCentralCrossRef Huang H, Ren Z, Gao X, et al. Integrated analysis of microbiome and host transcriptome reveals correlations between gut microbiota and clinical outcomes in HBV-related hepatocellular carcinoma. Genome Med. 2020;12:102.PubMedPubMedCentralCrossRef
98.
go back to reference Abate M, Vos E, Gonen M, et al. A novel microbiome signature in gastric cancer: a two independent cohort retrospective analysis. Ann Surg. 2022;276:605–15.PubMedCrossRef Abate M, Vos E, Gonen M, et al. A novel microbiome signature in gastric cancer: a two independent cohort retrospective analysis. Ann Surg. 2022;276:605–15.PubMedCrossRef
99.
go back to reference Peng R, Liu S, You W, Huang Y, Hu C, Gao Y, Jia X, Li G, Xu Z, Chen Y. Gastric microbiome alterations are associated with decreased CD8+ tissue-resident memory T cells in the tumor microenvironment of gastric cancer. Cancer Immunol Res. 2022;10:1224–40.PubMedCrossRef Peng R, Liu S, You W, Huang Y, Hu C, Gao Y, Jia X, Li G, Xu Z, Chen Y. Gastric microbiome alterations are associated with decreased CD8+ tissue-resident memory T cells in the tumor microenvironment of gastric cancer. Cancer Immunol Res. 2022;10:1224–40.PubMedCrossRef
100.
101.
go back to reference Kohi S, Macgregor-Das A, Dbouk M, et al. Alterations in the duodenal fluid microbiome of patients with pancreatic cancer. Clin Gastroenterol Hepatol. 2022;20:e196–227.PubMedCrossRef Kohi S, Macgregor-Das A, Dbouk M, et al. Alterations in the duodenal fluid microbiome of patients with pancreatic cancer. Clin Gastroenterol Hepatol. 2022;20:e196–227.PubMedCrossRef
103.
go back to reference Heidler S, Lusuardi L, Madersbacher S, Freibauer C. The microbiome in benign renal tissue and in renal cell carcinoma. Urol Int. 2020;104:247–52.PubMedCrossRef Heidler S, Lusuardi L, Madersbacher S, Freibauer C. The microbiome in benign renal tissue and in renal cell carcinoma. Urol Int. 2020;104:247–52.PubMedCrossRef
104.
go back to reference Fu A, Yao B, Dong T, et al. Tumor-resident intracellular microbiota promotes metastatic colonization in breast cancer. Cell. 2022;185:1356-1372.e26.PubMedCrossRef Fu A, Yao B, Dong T, et al. Tumor-resident intracellular microbiota promotes metastatic colonization in breast cancer. Cell. 2022;185:1356-1372.e26.PubMedCrossRef
105.
go back to reference Esposito MV, Fosso B, Nunziato M, Casaburi G, D’Argenio V, Calabrese A, D’Aiuto M, Botti G, Pesole G, Salvatore F. Microbiome composition indicate dysbiosis and lower richness in tumor breast tissues compared to healthy adjacent paired tissue, within the same women. BMC Cancer. 2022;22:30.PubMedPubMedCentralCrossRef Esposito MV, Fosso B, Nunziato M, Casaburi G, D’Argenio V, Calabrese A, D’Aiuto M, Botti G, Pesole G, Salvatore F. Microbiome composition indicate dysbiosis and lower richness in tumor breast tissues compared to healthy adjacent paired tissue, within the same women. BMC Cancer. 2022;22:30.PubMedPubMedCentralCrossRef
107.
go back to reference Salachan PV, Rasmussen M, Fredsøe J, Ulhøi B, Borre M, Sørensen KD. Microbiota of the prostate tumor environment investigated by whole-transcriptome profiling. Genome Med. 2022;14:9.PubMedPubMedCentralCrossRef Salachan PV, Rasmussen M, Fredsøe J, Ulhøi B, Borre M, Sørensen KD. Microbiota of the prostate tumor environment investigated by whole-transcriptome profiling. Genome Med. 2022;14:9.PubMedPubMedCentralCrossRef
108.
go back to reference Cavarretta I, Ferrarese R, Cazzaniga W, et al. The microbiome of the prostate tumor microenvironment. Eur Urol. 2017;72:625–31.PubMedCrossRef Cavarretta I, Ferrarese R, Cazzaniga W, et al. The microbiome of the prostate tumor microenvironment. Eur Urol. 2017;72:625–31.PubMedCrossRef
109.
go back to reference Wang Y, Wang Y, Wang J. A comprehensive analysis of intratumor microbiome in head and neck squamous cell carcinoma. Eur Arch Otorhinolaryngol. 2022;279:4127–36.PubMedCrossRef Wang Y, Wang Y, Wang J. A comprehensive analysis of intratumor microbiome in head and neck squamous cell carcinoma. Eur Arch Otorhinolaryngol. 2022;279:4127–36.PubMedCrossRef
Metadata
Title
Awareness of intratumoral bacteria and their potential application in cancer treatment
Authors
Yin Liang
Qiyan Li
Yulin Liu
Yajie Guo
Qingjiao Li
Publication date
01-12-2023
Publisher
Springer US
Published in
Discover Oncology / Issue 1/2023
Print ISSN: 1868-8497
Electronic ISSN: 2730-6011
DOI
https://doi.org/10.1007/s12672-023-00670-x

Other articles of this Issue 1/2023

Discover Oncology 1/2023 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine