Cited by 48Gut microbiota and healthCancer Research and TreatmentsCancer Immunotherapy and Biomarkers

The emerging tumor microbe microenvironment: From delineation to multidisciplinary approach-based interventions

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Fu, Yu, Li, Jia, Cai, Wenyun, Huang, Yulan, Liu, Xinlong, Ma, Zhongyi, Tang, Zhongjie, Bian, Xufei +3 more·2024·Acta Pharmaceutica Sinica B

Abstract

Intratumoral microbiota has become research hotspots, and emerges as a non-negligent new component of tumor microenvironments (TME), due to its powerful influence on tumor initiation, metastasis, immunosurveillance and prognosis despite in low-biomass. The accumulations of microbes, and their related components and metabolites within tumor tissues, endow TME with additional pluralistic features which are distinct from the conventional one. Therefore, it’s definitely necessary to comprehensively delineate the sophisticated landscapes of tumor microbe microenvironment, as well as their functions and related underlying mechanisms. Herein, in this review, we focused on the fields of tumor microbe microenvironment, including the heterogeneity of intratumor microbiota in different types of tumors, the controversial roles of intratumoral microbiota, the basic features of tumor microbe microenvironment (i.e., pathogen-associated molecular patterns (PAMPs), typical microbial metabolites, autophagy, inflammation, multi-faceted immunomodulation and chemoresistance), as well as the multidisciplinary approach-based intervention of tumor microbiome for cancer therapy by applying wild-type or engineered live microbes, microbiota metabolites, antibiotics, synthetic biology and rationally designed biomaterials. We hope our work will provide valuable insight to deeply understand the interplay of cancer-immune-microbial, and facilitate the development of microbes-based tumor-specific treatments.

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Crossref · 10.1016/j.apsb.2023.11.018

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  • Tumor microenvironment microbes produce pro-proliferative metabolites.

    “These microbes interact with both tumor and immune cells, influencing tumor dynamics by modulating immune responses, producing pro-proliferative metabolites, and reshaping the structural and biochemical landscape of the TME [38–40]”

    From Phage therapy in oncology: opportunities for cancer prevention and treatment (2026) · cites this paper as [38]

    The section on the pro-tumorigenic roles of intratumoral microbiota says that microbes secrete metabolites that promote tumorigenesis, and the section on microbial-metabolite interactions describes cancer-promoting examples (page numbers unavailable). These passages support production of pro-tumor metabolites, but do not specifically establish that the metabolites promote tumor-cell proliferation. (LLM, conf=0.79)

    Experimental — accuracy not yet measured
  • Tumor microenvironment microbes reshape the structural and biochemical landscape of the tumor microenvironment.

    “These microbes interact with both tumor and immune cells, influencing tumor dynamics by modulating immune responses, producing pro-proliferative metabolites, and reshaping the structural and biochemical landscape of the TME [38–40]”

    From Phage therapy in oncology: opportunities for cancer prevention and treatment (2026) · cites this paper as [38]

    The Introduction says that microbes, their residues, and metabolites give the TME additional features, supporting a changed biochemical landscape. It also describes organized, less-vascularized microbial niches as suggesting a potential contribution to TME heterogeneity, but does not establish that microbes reshape the TME’s structure. (LLM, conf=0.79)

    Experimental — accuracy not yet measured
  • Tumor microenvironment microbes influence tumor dynamics by modulating immune responses.

    “These microbes interact with both tumor and immune cells, influencing tumor dynamics by modulating immune responses, producing pro-proliferative metabolites, and reshaping the structural and biochemical landscape of the TME [38–40]”
  • Tumor microenvironment microbes interact with both tumor and immune cells.

    “These microbes interact with both tumor and immune cells, influencing tumor dynamics by modulating immune responses, producing pro-proliferative metabolites, and reshaping the structural and biochemical landscape of the TME [38–40]”

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  1. [1]Liu J.Y. Zhang Y. Intratumor microbiome in cancer progression: current developments, challenges and future trends Biomark Res 10 2022 1 18 35642013 PMC9153132
  2. [2]Xue C. Chu Q.F. Zheng Q.X. Yuan X. Su Y.S. Bao Z.Y. Current understanding of the intratumoral microbiome in various tumors Cell Rep Med 4 2023 100884 PMC9873978 36652905
  3. [3]Heymann C.J.F. Bard J.M. Heymann M.F. Heymann D. Bobin-Dubigeon C. The intratumoral microbiome: characterization methods and functional impact Cancer Lett 522 2021 63 79 34517085
  4. [4]Xie Y.F. Xie F. Zhou X.X. Zhang L. Yang B. Huang J. Microbiota in tumors: from understanding to application Adv Sci 9 2022 e2200470 PMC9313476 35603968
  5. [5]Chen J.W. Li T. Liang J.H. Huang Q.Q. Huang J.D. Ke Y.Q. Current status of intratumour microbiome in cancer and engineered exogenous microbiota as a promising therapeutic strategy Biomed Pharmacother 145 2022 112443 34847476
  6. [6]Zhang N. Kandalai S. Zhou X.Z. Hossain F. Zheng Q.F. Applying multi-omics toward tumor microbiome research iMeta 2 2023 e73 PMC10989946 38868335
  7. [8]Zhang J. Du Q.Q. Song X.W. Gao S.S. Pang X.C. Li Y. Evaluation of the tumor-targeting efficiency and intratumor heterogeneity of anticancer drugs using quantitative mass spectrometry imaging Theranostics 10 2020 2621 2630 32194824 PMC7052894
  8. [9]Galeano Nino J.L. Wu H.R. LaCourse K.D. Kempchinsky A.G. Baryiames A. Barber B. Effect of the intratumoral microbiota on spatial and cellular heterogeneity in cancer Nature 611 2022 810 817 36385528 PMC9684076
  9. [10]Gong Y.Y. Huang X.Q. Wang M.H. Liang X.Q. Intratumor microbiota: a novel tumor component J Cancer Res Clin Oncol 149 2023 6675 6691 36639531 PMC11798032
  10. [11]Ma J.Y. Huang L.J. 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 40 2021 327 34656142 PMC8520212
  11. [12]Zhou P. Hu Y.W. Wang X.Y. Shen L.X. Liao X.H. Zhu Y.J. Microbiome in cancer: an exploration of carcinogenesis, immune responses and immunotherapy Front Immunol 13 2022 877939 PMC9393638 36003378
  12. [13]Zhou X.Z. Kandalai S. Hossain F. Zheng Q.F. Tumor microbiome metabolism: a game changer in cancer development and therapy Front Oncol 12 2022 933407 PMC9351545 35936744
  13. [15]Yang L. Li A.T. Wang Y. Zhang Y. Intratumoral microbiota: roles in cancer initiation, development and therapeutic efficacy Signal Transduct Target Ther 8 2023 1 24 36646684 PMC9842669
  14. [18]Dhankhar R. Gupta V. Kumar S. Kapoor R.K. Gulati P. Microbial enzymes for deprivation of amino acid metabolism in malignant cells: biological strategy for cancer treatment Appl Microbiol Biot 104 2020 2857 2869 32037468
  15. [20]Fu A.K. Yao B.Q. Dong T.T. Chen Y.Y. Yao J. Liu Y. Tumor-resident intracellular microbiota promotes metastatic colonization in breast cancer Cell 185 2022 1356 1372 35395179
  16. [21]Azevedo M.M. Pina-Vaz C. Baltazar F. Microbes and cancer: friends or faux? Int J Mol Sci 21 2020 3115 32354115 PMC7247677
  17. [22]Bertocchi A. Carloni S. Ravenda P.S. Bertalot G. Spadoni I. Lo Cascio A. Gut vascular barrier impairment leads to intestinal bacteria dissemination and colorectal cancer metastasis to liver Cancer Cell 39 2021 708 724 33798472
  18. [23]Aykut B. Pushalkar S. Chen R. Li Q. Abengozar R. Kim J.I. The fungal mycobiome promotes pancreatic oncogenesis via activation of MBL Nature 574 2019 264 267 31578522 PMC6858566
  19. [24]Banerjee S. Alwine J.C. Wei Z. Tian T. Shih N. Sperling C. Microbiome signatures in prostate cancer Carcinogenesis 40 2019 749 764 30794288
  20. [25]Huang S. Li J.Y. Wu J. Meng L. Shou C.C. Mycoplasma infections and different human carcinomas World J Gastroenterol 7 2001 266 11819772 PMC4723534
  21. [26]Pehlivan M. Itirli G. Onay H. Bulut H. Koyuncuoglu M. Pehlivan S. Does Mycoplasma sp. play role in small cell lung cancer? Lung Cancer 45 2004 129 130 15196745
  22. [27]Nakatsu G. Zhou H.K. Wu W.K.K. Wong S.H. Coker O.O. Dai Z.W. Alterations in enteric virome are associated with colorectal cancer and survival outcomes Gastroenterology 155 2018 529 541 29689266
  23. [28]Agostinetto E. Gligorov J. Piccart M. Systemic therapy for early-stage breast cancer: learning from the past to build the future Nat Rev Clin Oncol 19 2022 763 774 36253451 PMC9575647
  24. [29]Zheng C. Zhang W. Wang J.M. Zhai Y.H. Xiong F.Q. Cai Y. Lenvatinib- and vadimezan-loaded synthetic high-density lipoprotein for combinational immunochemotherapy of metastatic triple-negative breast cancer Acta Pharm Sin B 12 2022 3726 3738 36176911 PMC9513558
  25. [30]Vitorino M. Costa D.A. Vicente R. Caleca T. Santos C. Local breast microbiota: a "new" player on the block Cancers 14 2022 3811 35954474 PMC9367283
  26. [31]Rao Malla R. Marni R. Kumari S. Chakraborty A. Lalitha P. Microbiome assisted tumor microenvironment: emerging target of breast cancer Clin Breast Cancer 22 2022 200 211 34625387
  27. [33]Velicer C.M. Heckbert S.R. Lampe J.W. Potter J.D. Robertson C.A. Taplin S.H. Antibiotic use in relation to the risk of breast cancer JAMA 291 2004 827 835 14970061
  28. [34]Rossini A. Rumio C. Sfondrini L. Tagliabue E. Morelli D. Miceli R. Influence of antibiotic treatment on breast carcinoma development in proto-neu transgenic mice Cancer Res 66 2006 6219 6224 16778196
  29. [36]Urbaniak C. Cummins J. Brackstone M. Macklaim J.M. Gloor G.B. Baban C.K. Microbiota of human breast tissue Appl Environ Microbiol 80 2014 3007 3014 24610844 PMC4018903
  30. [37]Tzeng A. Sangwan N. Jia M. Liu C.C. Keslar K.S. Downs-Kelly E. Human breast microbiome correlates with prognostic features and immunological signatures in breast cancer Genome Med 13 2021 60 33863341 PMC8052771
  31. [38]Parhi L. Alon-Maimon T. Sol A. Nejman D. Shhadeh A. Fainsod-Levi T. Breast cancer colonization by Fusobacterium nucleatum accelerates tumor growth and metastatic progression Nat Commun 11 2020 3259 32591509 PMC7320135
  32. [40]Ramirez-Labrada A.G. Isla D. Artal A. Arias M. Rezusta A. Pardo J. The influence of lung microbiota on lung carcinogenesis, immunity, and immunotherapy Trends Cancer 6 2020 86 97 32061309
  33. [41]Yu G.Q. Gail M.H. Consonni D. Carugno M. Humphrys M. Pesatori A.C. Characterizing human lung tissue microbiota and its relationship to epidemiological and clinical features Genome Biol 17 2016 163 27468850 PMC4964003
  34. [42]Sommariva M. Le Noci V. Bianchi F. Camelliti S. Balsari A. Tagliabue E. The lung microbiota: role in maintaining pulmonary immune homeostasis and its implications in cancer development and therapy Cell Mol Life Sci 77 2020 2739 2749 31974656 PMC7326824
  35. [43]Dickson R.P. Erb-Downward J.R. Martinez F.J. Huffnagle G.B. The microbiome and the respiratory tract Annu Rev Physiol 78 2016 481 504 26527186 PMC4751994
  36. [44]Mathieu E. Escribano-Vazquez U. Descamps D. Cherbuy C. Langella P. Riffault S. Paradigms of lung microbiota functions in health and disease Front Physiol 9 2018 1168 30246806 PMC6110890
  37. [45]Liu N.N. Yi C.X. Wei L.Q. Zhou J.A. Jiang T. Hu C.C. The intratumor mycobiome promotes lung cancer progression via myeloid-derived suppressor cells Cancer Cell 41 2023 1 18 37738973
  38. [47]Dumont-Leblond N. Veillette M. Racine C. Joubert P. Duchaine C. Non-small cell lung cancer microbiota characterization: prevalence of enteric and potentially pathogenic bacteria in cancer tissues PLoS One 16 2021 e0249832 PMC8064568 33891617
  39. [48]Cheng C. Wang Z.F. Wang J.Q. Ding C. Sun C. Liu P.L. Characterization of the lung microbiome and exploration of potential bacterial biomarkers for lung cancer Trans Lung Cancer Res 9 2020 693 704 PMC7354118 32676331
  40. [49]Zhang M. Zhang Y. Sun Y. Wang S. Liang H. Han Y.G. Intratumoral microbiota impacts the first-line treatment efficacy and survival in non-small cell lung cancer patients free of lung infection J Healthc Eng 2022 2022 5466853 PMC8844104 35178229
  41. [50]Najafi S. Abedini F. Jamalkandi S.A. Shariati P. Ahmadi A. Fesharaki M.G. The composition of lung microbiome in lung cancer: a systematic review and meta-analysis BMC Microbiol 21 2021 315 34763672 PMC8582175
  42. [51]Zhao Y.M. Yi J.Q. Xiang J.J. Jia W. Chen A.Q. Chen L.Y. Exploration of lung mycobiome in the patients with non-small-cell lung cancer BMC Microbiol 23 2023 81 36966280 PMC10039514
  43. [52]Lloyd C.M. Marsland B.J. Lung homeostasis: influence of age, microbes, and the immune system Immunity 46 2017 549 561 28423336
  44. [53]Jin C.C. Lagoudas G.K. Zhao C. Bullman S. Bhutkar A. Hu B. Commensal microbiota promote lung cancer development via gammadelta T cells Cell 176 2019 998 1013 30712876 PMC6691977
  45. [54]Peters B.A. Hayes R.B. Goparaju C. Reid C. Pass H.I. Ahn J.Y. The microbiome in lung cancer tissue and recurrence-free survival Cancer Epidemiol Biomarkers Prev 28 2019 731 740 30733306 PMC6449216
  46. [55]Gollwitzer E.S. Saglani S. Trompette A. Yadava K. Sherburn R. McCoy K.D. Lung microbiota promotes tolerance to allergens in neonates via PD-L1 Nat Med 20 2014 642 647 24813249
  47. [56]Hwang W.L. Jagadeesh K.A. Guo J.A. Hoffman H.I. Yadollahpour P. Reeves J.W. Single-nucleus and spatial transcriptome profiling of pancreatic cancer identifies multicellular dynamics associated with neoadjuvant treatment Nat Genet 54 2022 1178 1191 35902743 PMC10290535
  48. [57]Springfeld C. Ferrone C.R. Katz M.H.G. Philip P.A. Hong T.S. Hackert T. Neoadjuvant therapy for pancreatic cancer Nat Rev Clin Oncol 20 2023 318 337 36932224
  49. [58]Kiaie S.H. Sanaei M.J. Heshmati M. Asadzadeh Z. Azimi I. Hadidi S. Immune checkpoints in targeted-immunotherapy of pancreatic cancer: new hope for clinical development Acta Pharm Sin B 11 2021 1083 1097 34094821 PMC8144893
  50. [59]Wei M.Y. Shi S. Liang C. Meng Q.C. Hua J. Zhang Y.Y. The microbiota and microbiome in pancreatic cancer: more influential than expected Mol Cancer 18 2019 97 31109338 PMC6526613
  51. [60]Leinwand J. Miller G. Regulation and modulation of antitumor immunity in pancreatic cancer Nat Immunol 21 2020 1152 1159 32807942
  52. [61]Arsenijevic T. Nicolle R. Bouchart C. D’Haene N. Demetter P. Puleo F. Pancreatic cancer meets human microbiota: close encounters of the third kind Cancers 13 2021 1231 33799784 PMC7998494
  53. [62]Cohen J.R. Shannon A.B. McNEAL J.E. Shannon T. Garrett L.K. Propionibacterium acnes associated with inflammation in radical prostatectomy specimens: a possible link to cancer evolution? J Urology 173 2005 1969 1974 15879794
  54. [63]McAllister F. Khan M.A.W. Helmink B. Wargo J.A. The tumor microbiome in pancreatic cancer: bacteria and beyond Cancer Cell 36 2019 577 579 31951558
  55. [64]Geller L.T. Barzily-Rokni M. Danino T. Jonas O.H. Shental N. Nejman D. Potential role of intratumor bacteria in mediating tumor resistance to the chemotherapeutic drug gemcitabine Science 357 2017 1156 1160 28912244 PMC5727343
  56. [65]Capula M. Peran M. Xu G. Donati V. Yee D. Gregori A. Role of drug catabolism, modulation of oncogenic signaling and tumor microenvironment in microbe-mediated pancreatic cancer chemoresistance Drug Resist Updat 64 2022 100864 36115181
  57. [66]Guo W. Zhang Y.C. Guo S.W. Mei Z. Liao H.P. Dong H. Tumor microbiome contributes to an aggressive phenotype in the basal-like subtype of pancreatic cancer Commun Biol 4 2021 1019 34465850 PMC8408135
  58. [67]Driscoll J.A. Brody S.L. Kollef M.H. The epidemiology, pathogenesis and treatment of Pseudomonas aeruginosa infections Drugs 67 2007 351 368 17335295
  59. [69]Sun D.D. Zou Y.F. Song L. Han S.L. Yang H. Chu D. A cyclodextrin-based nanoformulation achieves co-delivery of ginsenoside Rg3 and quercetin for chemo-immunotherapy in colorectal cancer Acta Pharm Sin B 12 2022 378 393 35127393 PMC8799998
  60. [70]Wong S.H. Yu J. Gut microbiota in colorectal cancer: mechanisms of action and clinical applications Nat Rev Gastroenterol Hepatol 16 2019 690 704 31554963
  61. [72]Wu S.G. Rhee K.J. Albesiano E. Rabizadeh S. Wu X.Q. Yen H.R. A human colonic commensal promotes colon tumorigenesis via activation of T helper type 17 T cell responses Nat Med 15 2009 1016 1022 19701202 PMC3034219
  62. [74]Flemer B. Lynch D.B. Brown J.M. Jeffery I.B. Ryan F.J. Claesson M.J. Tumour-associated and non-tumour-associated microbiota in colorectal cancer Gut 66 2017 633 643 26992426 PMC5529966
  63. [75]Castellarin M. Warren R.L. Freeman J.D. Dreolini L. Krzywinski M. Strauss J. Fusobacterium nucleatum infection is prevalent in human colorectal carcinoma Genome Res 22 2012 299 306 22009989 PMC3266037
  64. [76]Kostic A.D. Gevers D. Pedamallu C.S. Michaud M. Duke F. Earl A.M. Genomic analysis identifies association of Fusobacterium with colorectal carcinoma Genome Res 22 2012 292 298 22009990 PMC3266036
  65. [77]Abed J. Emgard J.E. Zamir G. Faroja M. Almogy G. Grenov A. Fap2 mediates Fusobacterium nucleatum colorectal adenocarcinoma enrichment by binding to tumor-expressed Gal-GalNAc Cell Host Microbe 20 2016 215 225 27512904 PMC5465824
  66. [78]Bullman S. Pedamallu C.S. Sicinska E. Clancy T.E. Zhang X. Cai D.N. Analysis of Fusobacterium persistence and antibiotic response in colorectal cancer Science 358 2017 1443 1448 29170280 PMC5823247
  67. [79]LaCourse K.D. Johnston C.D. Bullman S. The relationship between gastrointestinal cancers and the microbiota Lancet Gastroenterol Hepatol 6 2021 498 509 33743198 PMC10773981
  68. [80]Peek R.M. Jr. Crabtree J.E. Helicobacter infection and gastric neoplasia J Pathol 208 2006 233 248 16362989
  69. [81]Aviles-Jimenez F. Vazquez-Jimenez F. Medrano-Guzman R. Mantilla A. Torres J. Stomach microbiota composition varies between patients with non-atrophic gastritis and patients with intestinal type of gastric cancer Sci Rep 4 2014 4202 24569566 PMC3935187
  70. [82]Dicksved J. Lindberg M. Rosenquist M. Enroth H. Jansson J.K. Engstrand L. Molecular characterization of the stomach microbiota in patients with gastric cancer and in controls J Med Microbiol 58 2009 509 516 19273648
  71. [83]Eun C.S. Kim B.K. Han D.S. Kim S.Y. Kim K.M. Choi BY, et al. Differences in gastric mucosal microbiota profiling in patients with chronic gastritis, intestinal metaplasia, and gastric cancer using pyrosequencing methods Helicobacter 19 2014 407 416 25052961
  72. [84]Coker O.O. Dai Z.W. Nie Y.Z. Zhao G.J. Cao L. Nakatsu G. Mucosal microbiome dysbiosis in gastric carcinogenesis Gut 67 2018 1024 1032 28765474 PMC5969346
  73. [85]Park C.H. Lee J.G. Lee A.R. Eun C.S. Han D.S. Network construction of gastric microbiome and organization of microbial modules associated with gastric carcinogenesis Sci Rep 9 2019 12444 PMC6712011 31455798
  74. [86]Ai B. Mei Y. Liang D. Wang T.J. Cai H. Yu D. Uncovering the special microbiota associated with occurrence and progression of gastric cancer by using RNA-sequencing Sci Rep 13 2023 5722 37029259 PMC10082026
  75. [87]Park J.Y. Seo H. Kang C.S. Shin T.S. Kim J.W. Park J.M. Dysbiotic change in gastric microbiome and its functional implication in gastric carcinogenesis Sci Rep 12 2022 4285 35277583 PMC8917121
  76. [88]Bast R.C. Hennessy B. Mills G.B. The biology of ovarian cancer: new opportunities for translation Nat Rev Cancer 9 2009 415 428 19461667 PMC2814299
  77. [89]Chang L.L. Hu Y. Fu Y.Y. Zhou T.Y. You J. Du J.M. Targeting slug-mediated non-canonical activation of c-Met to overcome chemo-resistance in metastatic ovarian cancer cells Acta Pharm Sin B 9 2019 484 495 31193822 PMC6543058
  78. [90]Carvalho J.P. Carvalho F.M. Is Chlamydia-infected tubal fimbria the origin of ovarian cancer? Med Hypotheses 71 2008 690 693 18703287
  79. [91]Hosseininasab-nodoushan S.A. Ghazvini K. Jamialahmadi T. Keikha M. Sahebkar A. Association of Chlamydia and Mycoplasma infections with susceptibility to ovarian cancer: a systematic review and meta-analysis Semin Cancer Biol 86 2022 923 928 34333041
  80. [92]Sipos A. Ujlaki G. Mikó E. Maka E. Szabó J. Uray K. The role of the microbiome in ovarian cancer: mechanistic insights into oncobiosis and to bacterial metabolite signaling Mol Med 27 2021 33 33794773 PMC8017782
  81. [93]Miles S.M. Hardy B.L. Merrell D.S. Investigation of the microbiota of the reproductive tract in women undergoing a total hysterectomy and bilateral salpingo-oopherectomy Fertil Steril 107 2017 813 820 28069180
  82. [94]Banerjee S. Tian T. Wei Z. Shih N. Feldman M.D. Alwine J.C. The ovarian cancer oncobiome Oncotarget 8 2017 36225 PMC5482651 28410234
  83. [95]Kumar P. Ranmale S. Tongaonkar H. Mehta S. Mania-Pramanik J. Human papillomavirus infection: is it associated with epithelial ovarian cancer? Indian J Med Microbi 39 2021 311 314 34016470
  84. [96]Al-Shabanah O.A. Hafez M.M. Hassan Z.K. Sayed-Ahmed M.M. Abozeed W.N. Al-Rejaie S.S. Human papillomavirus genotyping and integration in ovarian cancer Saudi patients Virol J 10 2013 343 24252426 PMC3842654
  85. [97]Zhou B. Sun C.Y. Huang J. Xia M. Guo E.S. Li N. The biodiversity composition of microbiome in ovarian carcinoma patients Sci Rep 9 2019 1691 30737418 PMC6368644
  86. [98]Omar M.I. MacLennan S. Ribal M.J. Roobol M.J. Dimitropoulos K. van den Broeck T. Unanswered questions in prostate cancer—findings of an international multi-stakeholder consensus by the PIONEER consortium Nat Rev Urol 20 2023 494 501 37012441
  87. [99]Liadi Y. Campbell T. Dike P. Harlemon M. Elliott B. Odero-Marah V. Prostate cancer metastasis and health disparities: a systematic review Prostate Cancer P D 1 2023 1 9 37046071
  88. [100]Anker J.F. Naseem A.F. Mok H. Schaeffer A.J. Abdulkadir S.A. Thumbikat P. Multi-faceted immunomodulatory and tissue-tropic clinical bacterial isolate potentiates prostate cancer immunotherapy Nat Commun 9 2018 1591 29686284 PMC5913311
  89. [101]Sfanos K.S. De Marzo A.M. Prostate cancer and inflammation: the evidence Histopathology 60 2012 199 215 22212087 PMC4029103
  90. [102]Kwon O.J. Zhang L. Ittmann M.M. Xin L. Prostatic inflammation enhances basal-to-luminal differentiation and accelerates initiation of prostate cancer with a basal cell origin Proc Natl Acad Sci U S A 111 2014 592 600 PMC3918789 24367088
  91. [103]Simons B.W. Durham N.M. Bruno T.C. Grosso J.F. Schaeffer A.J. Ross A.E. A human prostatic bacterial isolate alters the prostatic microenvironment and accelerates prostate cancer progression J Pathol 235 2015 478 489 25348195 PMC4352321
  92. [104]Davidsson S. Mölling P. Rider J.R. Unemo M. Karlsson M.G. Carlsson J. Frequency and typing of Propionibacterium acnes in prostate tissue obtained from men with and without prostate cancer Infect Agents Cancer 11 2016 26 PMC4899914 27284286
  93. [105]McDowell A. Valanne S. Ramage G. Tunney M.M. Glenn J.V. McLorinan G.C. Propionibacterium acnes types I and II represent phylogenetically distinct groups J Clin Microbiol 43 2005 326 334 15634990 PMC540145
  94. [106]Drott J.B. Alexeyev O. Bergström P. Elgh F. Olsson J. Propionibacterium acnes infection induces upregulation of inflammatory genes and cytokine secretion in prostate epithelial cells BMC Microbiol 10 2010 126 20420679 PMC2867951
  95. [107]Fehri L.F. Mak T.N. Laube B. Brinkmann V. Ogilvie L.A. Mollenkopf H. Prevalence of Propionibacterium acnes in diseased prostates and its inflammatory and transforming activity on prostate epithelial cells Int J Med Microbiol 301 2011 69 78 20943438
  96. [108]Bielecki R. Zdrodowska-Stefanow B. Ostaszewska-Puchalska I. Baltaziak M. Kozłowski B.M. Subclinical prostatic inflammation attributable to Chlamydia trachomatis in a patient with prostate cancer Med Wieku Rozwoj 9 2005 87 91 16082070
  97. [109]Cavarretta I. Ferrarese R. Cazzaniga W. Saita D. Luciano R. Ceresola E.R. The microbiome of the prostate tumor microenvironment Eur Urol 72 2017 625 631 28434677
  98. [110]Feng Y. Ramnarine V.R. Bell R. Volik S. Davicioni E. Hayes V.M. Metagenomic and metatranscriptomic analysis of human prostate microbiota from patients with prostate cancer BMC Genom 20 2019 146 PMC6379980 30777011
  99. [111]Grice E.A. Kong H.H. Conlan S. Deming C.B. Davis J. Young A.C. Topographical and temporal diversity of the human skin microbiome Science 324 2009 1190 1192 19478181 PMC2805064
  100. [112]Kalaora S. Nagler A. Nejman D. Alon M. Barbolin C. Barnea E. Identification of bacteria-derived HLA-bound peptides in melanoma Nature 592 2021 138 143 33731925 PMC9717498
  101. [113]Sepich-Poore G.D. Carter H. Knight R. Intratumoral bacteria generate a new class of therapeutically relevant tumor antigens in melanoma Cancer Cell 39 2021 601 603 33974857
  102. [115]Zhu G.J. Su H.X. Johnson C.H. Khan S.A. Kluger H. Lu L.G. Intratumour microbiome associated with the infiltration of cytotoxic CD8+ T cells and patient survival in cutaneous melanoma Eur J Cancer 151 2021 25 34 33962358 PMC8184628
  103. [116]Nakatsuji T. Chen T.H. Butcher A.M. Trzoss L.L. Nam S.J. Shirakawa K.T. A commensal strain of Staphylococcus epidermidis protects against skin neoplasia Sci Adv 4 2018 eaao4502 PMC5834004 29507878
  104. [117]Du D.Y. Liu C. Qin M.Y. Zhang X. Xi T. Yuan S.T. Metabolic dysregulation and emerging therapeutical targets for hepatocellular carcinoma Acta Pharm Sin B 12 2022 558 580 35256934 PMC8897153
  105. [118]Yuan J.M. Govindarajan S. Arakawa K. Yu M.C. Synergism of alcohol, diabetes, and viral hepatitis on the risk of hepatocellular carcinoma in blacks and whites in the U.S Cancer 101 2004 1009 1017 15329910
  106. [119]Chakladar J. Wong L.M. Kuo S.Z. Li W.T. Yu M.A. Chang E.Y. The liver microbiome is implicated in cancer prognosis and modulated by alcohol and hepatitis B Cancers 12 2020 1642 32575865 PMC7353057
  107. [120]Qu D.D. Wang Y. Xia Q.X. Chang J. Jiang X.N. Zhang H. Intratumoral microbiome of human primary liver cancer Hepatol Commun 6 2022 1741 1752 35191218 PMC9234634
  108. [121]Liao J.F. Han R.X. Wu Y.Z. Qian Z.Y. Review of a new bone tumor therapy strategy based on bifunctional biomaterials Bone Res 9 2021 18 33727543 PMC7966774
  109. [122]Nakagawa M. SuGIURA Y. OsHIMA T. Kajino G. Hirako H. Yamada Y. Urinary hydroxyproline excretion in orthopedic disease, with special reference to systemic bone disease and bone tumor (secondary report) Nagoya J Med Sci 29 1967 345 367 6066099
  110. [123]Huang Y. Fan X.G. Wang Z.M. Zhou J.H. Tian X.F. Li N. Identification of helicobacter species in human liver samples from patients with primary hepatocellular carcinoma J Clin Pathol 57 2004 1273 1277 15563667 PMC1770525
  111. [124]Klann E. Williamson J.M. Tagliamonte M.S. Ukhanova M. Asirvatham J.R. Chim H. Microbiota composition in bilateral healthy breast tissue and breast tumors Cancer Causes Control 31 2020 1027 1038 32844256
  112. [126]Thyagarajan S. Zhang Y. Thapa S. Allen M.S. Phillips N. Chaudhary P. Comparative analysis of racial differences in breast tumor microbiome Sci Rep 10 2020 14116 PMC7445256 32839514
  113. [127]Wong L.M. Shende N. Li W.T. Castaneda G. Apostol L. Chang E.Y. Comparative analysis of age- and gender-associated microbiome in lung adenocarcinoma and lung squamous cell carcinoma Cancers 12 2020 1447 32498338 PMC7352186
  114. [129]Tsay J.C.J. Wu B.G. Sulaiman I. Gershner K. Schluger R. Li Y.H. Lower airway dysbiosis affects lung cancer progression Cancer Discov 11 2021 293 307 33177060 PMC7858243
  115. [130]Greathouse K.L. White J.R. Vargas A.J. Bliskovsky V.V. Beck J.A. Muhlinen N.V. Interaction between the microbiome and TP53 in human lung cancer Genome Biol 19 2018 123 30143034 PMC6109311
  116. [131]Tsay J.C.J. Wu B.G. Badri M.H. Clemente J.C. Shen N. Meyn P. Airway microbiota is associated with upregulation of the PI3K pathway in lung cancer Am J Respir Crit Care Med 198 2018 1188 1198 29864375 PMC6221574
  117. [132]Burns M.B. Lynch J. Starr T.K. Knights D. Blekhman R. Virulence genes are a signature of the microbiome in the colorectal tumor microenvironment Genome Med 7 2015 55 26170900 PMC4499914
  118. [133]Gur C. Ibrahim Y. Isaacson B. Yamin R. Abed J. Gamliel M. Binding of the Fap2 protein of Fusobacterium nucleatum to human inhibitory receptor TIGIT protects tumors from immune cell attack Immunity 42 2015 344 355 25680274 PMC4361732
  119. [134]Kosumi K. Hamada T. Koh H. Borowsky J. Bullman S. Twombly T.S. The amount of Bifidobacterium genus in colorectal carcinoma tissue in relation to tumor characteristics and clinical outcome Am J Pathol 188 2018 2839 2852 30243655 PMC6284552
  120. [135]Liu W.X. Zhang X. Xu H.Z. Li S.M. Lau H.C.H. Chen Q.Y. Microbial community heterogeneity within colorectal neoplasia and its correlation with colorectal carcinogenesis Gastroenterology 160 2021 2395 2408 33581124
  121. [136]Yu G.Q. Torres J. Hu N. Medrano-Guzman R. Herrera-Goepfert R. Humphrys M.S. Molecular characterization of the human stomach microbiota in gastric cancer patients Front Cell Infect Microbiol 7 2017 302 28730144 PMC5498480
  122. [137]Shao D.T. Vogtmann E. Liu A.Q. Qin J.J. Chen W. Abnet C.C. Microbial characterization of esophageal squamous cell carcinoma and gastric cardia adenocarcinoma from a high-risk region of China Cancer 125 2019 3993 4002 31355925 PMC7285383
  123. [138]Mrazek J. Mekadim C. Kucerova P. Svejstil R. Salmonova H. Vlasakova J. Melanoma-related changes in skin microbiome Folia Microbiol 64 2019 435 442 30554379
  124. [139]Al-Shabanah O.A. Hafez M.M. Hassan Z.K. Sayed-Ahmed M.M. Abozeed W.N. Al-Rejaie S.S. Human papillomavirus genotyping and integration in ovarian cancer Saudi patients Virol J 10 2013 1 9 24252426 PMC3842654
  125. [140]Ma J.Y. Gnanasekar A. Lee A. Li W.T. Haas M. Wang-Rodriguez J. Influence of intratumor microbiome on clinical outcome and immune processes in prostate cancer Cancers 12 2020 2524 32899474 PMC7564876
  126. [141]Chakladar J. Kuo S.Z. Castaneda G. Li W.T. Gnanasekar A. Yu M.A. The pancreatic microbiome is associated with carcinogenesis and corse prognosis in males and smokers Cancers 12 2020 2672 32962112 PMC7565819
  127. [143]Li S. Fuhler G.M. Bn N. Jose T. Bruno M.J. Peppelenbosch M.P. Pancreatic cyst fluid harbors a unique microbiome Microbiome 5 2017 147 29122007 PMC5680603
  128. [144]Nalluri H. Jensen E. Staley C. Role of biliary stent and neoadjuvant chemotherapy in the pancreatic tumor microbiome BMC Microbiol 21 2021 280 34656097 PMC8520243
  129. [145]Pushalkar S. Hundeyin M. Daley D. Zambirinis C.P. Kurz E. Mishra A. The pancreatic cancer microbiome promotes oncogenesis by induction of innate and adaptive immune suppression Cancer Discov 8 2018 403 416 29567829 PMC6225783
  130. [146]Neuzillet C. Marchais M. Vacher S. Hilmi M. Schnitzler A. Meseure D. Prognostic value of intratumoral Fusobacterium nucleatum and association with immune-related gene expression in oral squamous cell carcinoma patients Sci Rep 11 2021 7870 33846399 PMC8041800
  131. [147]Al-Hebshi N.N. Nasher A.T. Maryoud M.Y. Homeida H.E. Chen T. Idris A.M. Inflammatory bacteriome featuring Fusobacterium nucleatum and Pseudomonas aeruginosa identified in association with oral squamous cell carcinoma Sci Rep 7 2017 1834 28500338 PMC5431832
  132. [148]Hooper S.J. Crean S.J. Lewis M.A. Spratt D.A. Wade W.G. Wilson M.J. Viable bacteria present within oral squamous cell carcinoma tissue J Clin Microbiol 44 2006 1719 1725 16672398 PMC1479175
  133. [149]Liu Y. Baba Y. Ishimoto T. Tsutsuki H. Zhang T.L. Nomoto D. Fusobacterium nucleatum confers chemoresistance by modulating autophagy in oesophageal squamous cell carcinoma Br J Cancer 124 2021 963 974 33299132 PMC7921654
  134. [150]Kaakoush N.O. Castano-Rodriguez N. Man S.M. Mitchell H.M. Is Campylobacter to esophageal adenocarcinoma as Helicobacter is to gastric adenocarcinoma? Trends Microbiol 23 2015 455 462 25937501
  135. [153]Andreeva N.V. Gabbasova R.R. Grivennikov S.I. Microbiome in cancer progression and therapy Curr Opin Microbiol 56 2020 118 126 33147555 PMC8404536
  136. [154]Peng M.F. Tabashsum Z. Patel P. Bernhardt C. Biswas D. Linoleic acids overproducing Lactobacillus casei limits growth, survival, and virulence of Salmonella Typhimurium and enterohaemorrhagic Escherichia coli Front Microbiol 9 2018 2663 30443248 PMC6223203
  137. [155]Litvak Y. Mon K.K.Z. Nguyen H. Chanthavixay G. Liou M. Velazquez E.M. Commensal Enterobacteriaceae protect against Salmonella colonization through oxygen competition Cell Host Microbe 25 2019 128 139 30629913 PMC12036633
  138. [156]Nauts H.C. Fowler G.A. BogatkoFH A review of the influence of bacterial infection and of bacterial products (Coley's toxins) on malignant tumors in man, a critical analysis of 30 inoperable cases treated by Coley's mixed toxins, in which diagnosis was confirmed by microscopic examination selected for special study Acta Med Scand Suppl 276 1953 1 103 13039964
  139. [157]Cheng M. Qian L.T. Shen G.D. Bian G. Xu T.J. Xu W.P. Microbiota modulate tumoral immune surveillance in lung through a δT17 immune cell-dependent mechanism Cancer Res 74 2014 4030 4041 24947042
  140. [158]Marinelli L. Tenore G.C. Novellino E. Probiotic species in the modulation of the anticancer immune response Semin Cancer Biol 46 2017 182 190 28844794
  141. [159]Furusawa Y. Obata Y. Fukuda S. Endo T.A. Nakato G. Takahashi D. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells Nature 504 2013 446 450 24226770
  142. [160]Galluzzi L. Vitale I. Senovilla L. Olaussen K.A. Pinna G. Eisenberg T. Prognostic impact of vitamin B6 metabolism in lung cancer Cell Rep 2 2012 257 269 22854025
  143. [161]Iida N. Dzutsev A. Stewart C.A. Smith L. Bouladoux N. Weingarten R.A. Commensal bacteria control cancer response to therapy by modulating the tumor microenvironment Science 342 2013 967 970 24264989 PMC6709532
  144. [162]Vétizou M. Pitt J.M. Daillère R. Lepage P. Waldschmitt N. Flament C. Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota Science 350 2015 1079 1084 26541610 PMC4721659
  145. [164]Gonzalez-Sanchez P. DeNicola G.M. The microbiome(s) and cancer: know thy neighbor(s) J Pathol 254 2021 332 343 33723873
  146. [165]Kostic A.D. Chun E.Y. Robertson L. Glickman J.N. Gallini C.A. Michaud M. Fusobacterium nucleatum potentiates intestinal tumorigenesis and modulates the tumor-immune microenvironment Cell Host Microbe 14 2013 207 215 23954159 PMC3772512
  147. [166]Grivennikov S.I. Wang K.P. Mucida D. Stewart C.A. Schnabl B. Jauch D. Adenoma-linked barrier defects and microbial products drive IL-23/IL-17-mediated tumour growth Nature 491 2012 254 258 23034650 PMC3601659
  148. [167]Dinges M.M. Orwin P.M. Schlievert P.M. Exotoxins of Staphylococcus aureus Clin Microbiol Rev 13 2000 16 34 10627489 PMC88931
  149. [168]Rossi T. Vergara D. Fanini F. Maffia M. Bravaccini S. Pirini F. Microbiota-derived metabolites in tumor progression and metastasis Int J Mol Sci 21 2020 5786 32806665 PMC7460823
  150. [169]Akira S. Hemmi H. Recognition of pathogen-associated molecular patterns by TLR family Immunol Lett 85 2003 85 95 12527213
  151. [170]Escamilla-Tilch M. Filio-Rodriguez G. Garcia-Rocha R. Mancilla-Herrera I. Mitchison N.A. Ruiz-Pacheco J.A. The interplay between pathogen-associated and danger-associated molecular patterns: an inflammatory code in cancer? Immunol Cell Biol 91 2013 601 610 24100386
  152. [171]Demento S.L. Siefert A.L. Bandyopadhyay A. Sharp F.A. Fahmy T.M. Pathogen-associated molecular patterns on biomaterials: a paradigm for engineering new vaccines Trends Biotechnol 29 2011 294 306 21459467 PMC7025712
  153. [172]Guo J.M. De May H. Franco S. Noureddine A. Tang L. Brinker C.J. Cancer vaccines from cryogenically silicified tumour cells functionalized with pathogen-associated molecular patterns Nat Biomed Eng 6 2022 19 31 34725505 PMC8792180
  154. [173]Zelechowska P. Brzezinska-Blaszczyk E. Agier J. Kozlowska E. Different effectiveness of fungal pathogen-associated molecular patterns (PAMPs) in activating rat peritoneal mast cells Immunol Lett 248 2022 7 15 35679972
  155. [174]Keller N.P. Fungal secondary metabolism: regulation, function and drug discovery Nat Rev Microbiol 17 2019 167 180 30531948 PMC6381595
  156. [175]Patel S. Seshadri S. Dalai S. Chapter seven-gut microbiome and type 2 diabetes Das B. Singh V. Progress in molecular biology and translational science 191 2022 Elsevier Amsterdam 175 185 36270677
  157. [176]Tan J. McKenzie C. Potamitis M. Thorburn A.N. Mackay C.R. Macia L. The role of short-chain fatty acids in health and disease Adv Immunol 121 2014 91 119 24388214
  158. [178]Hee B.V.D. Wells J.M. Microbial regulation of host physiology by short-chain fatty acids Trends Microbiol 29 2021 700 712 33674141
  159. [179]Guan B.Y. Tong J.L. Hao H.P. Yang Z.X. Chen K.J. Xu H. Bile acid coordinates microbiota homeostasis and systemic immunometabolism in cardiometabolic diseases Acta Pharm Sin B 12 2022 2129 2149 35646540 PMC9136572
  160. [181]Crowley-Weber C.L. Payne C.M. Gleason-Guzman M. Watts G.S. Futscher B. Waltmire C.N. Development and molecular characterization of HCT-116 cell lines resistant to the tumor promoter and multiple stress-inducer, deoxycholate Carcinogenesis 23 2002 2063 2080 12507930
  161. [182]Powolny A. Xu J. Loo G. Deoxycholate induces DNA damage and apoptosis in human colon epithelial cells expressing either mutant or wild-type p53 Int J Biochem Cell B 33 2001 193 203 11240376
  162. [183]Khan A.U. Mei Y.H. Wilson T. A proposed function for spermine and spermidine: protection of replicating DNA against damage by singlet oxygen Proc Natl Acad Sci U S A 89 1992 11426 11427 1454830 PMC50563
  163. [184]Smith R.C. Litwin M.S. Lu Y. Zetter B.R. Identification of an endogenous inhibitor of prostatic carcinoma cell growth Nat Med 1 1995 1040 1045 7489360
  164. [185]Wang X.J. Feith D.J. Welsh P. Coleman C.S. Lopez C. Woster P.M. Studies of the mechanism by which increased spermidine/spermine N1-acetyltransferase activity increases susceptibility to skin carcinogenesis Carcinogenesis 28 2007 2404 2411 17675337
  165. [186]Richarme G. Liu C. Mihoub M. Abdallah J. Leger T. Joly N. Guanine glycation repair by DJ-1/Park7 and its bacterial homologs Science 357 2017 208 211 28596309
  166. [187]Richarme G. Mihoub M. Dairou J. Bui L.C. Leger T. Lamouri A. Parkinsonism-associated protein DJ-1/Park7 is a major protein deglycase that repairs methylglyoxal- and glyoxal-glycated cysteine, arginine, and lysine residues J Biol Chem 290 2015 1885 1897 25416785 PMC4340429
  167. [188]Bollong M.J. Lee G. Coukos J.S. Yun H. Zambaldo C. Chang J.W. A metabolite-derived protein modification integrates glycolysis with KEAP1–NRF2 signalling Nature 562 2018 600 604 30323285 PMC6444936
  168. [189]Cuevas-Ramos G. Petit C.R. Marcq I. Boury M. Oswald E. Nougayrède J.P. Escherichia coli induces DNA damage in vivo and triggers genomic instability in mammalian cells Proc Natl Acad Sci U S A 107 2010 11537 11542 20534522 PMC2895108
  169. [191]Guo C.J. Chang F.Y. Wyche T.P. Backus K.M. Acker T.M. Funabashi M. Discovery of reactive microbiota-derived metabolites that inhibit host proteases Cell 168 2017 517 526 28111075 PMC5302092
  170. [192]Zheng Q.F. Wang Q.L. Wang S.F. Wu J.Q. Gao Q. Liu W. Thiopeptide antibiotics exhibit a dual mode of action against intracellular pathogens by affecting both host and microbe Chem Biol 22 2015 1002 1007 26211364
  171. [193]Vinogradov A.A. Suga H. Introduction to thiopeptides: biological activity, biosynthesis, and strategies for functional reprogramming Cell Chem Biol 27 2020 1032 1051 32698017
  172. [194]Xiang H.G. Zhou M. Li Y. Zhou L. Wang R.X. Drug discovery by targeting the protein‒protein interactions involved in autophagy Acta Pharm Sin B 13 2023 4373 4390 37969735 PMC10638514
  173. [195]Hu W. Chan H. Lu L. Wong K.T. Wong S.H. Li M.X. Autophagy in intracellular bacterial infection Semin Cell Dev Biol 101 2020 41 50 31408699
  174. [196]Huang J. Brumell J.H. Bacteria-autophagy interplay: a battle for survival Nat Rev Microbiol 12 2014 101 114 24384599 PMC7097477
  175. [197]Deretic V. Delgado M. Vergne I. Master S. Haro S.D. Ponpuak M. Autophagy in immunity against Mycobacterium tuberculosis: a model system to dissect immunological roles of autophagy Levine B. Yoshimori T. Deretic V. Autophagy in Infection and Immunity 2009 Springer Berlin Heidelberg Berlin 169 188 PMC2788935 19802565
  176. [198]Amano A. Nakagawa I. Yoshimori T. Autophagy in innate immunity against intracellular bacteria J Biochem 140 2006 161 166 16954534
  177. [199]Siqueira M.D.S. Ribeiro R.M. Travassos L.H. Autophagy and its interaction with intracellular bacterial pathogens Front Immunol 9 2018 935 29875765 PMC5974045
  178. [200]Singh S.B. Davis A.S. Taylor G.A. Deretic V. Human IRGM induces autophagy to eliminate intracellular Mycobacteria Science 313 2006 1438 1441 16888103
  179. [201]Ogawa M. Yoshimori T. Suzuki T. Sagara H. Mizushima N. Sasakawa C. Escape of intracellular Shigella from autophagy Science 307 2005 727 731 15576571
  180. [202]Py B.F. Lipinski M.M. Yuan J. Autophagy limits Listeria monocytogenes intracellular growth in the early phase of primary infection Autophagy 3 2007 117 125 17204850
  181. [203]Chavez-Dominguez R. Perez-Medina M. Lopez-Gonzalez J.S. Galicia-Velasco M. Aguilar-Cazares D. The double-edge sword of autophagy in cancer: from tumor suppression to pro-tumor activity Front Oncol 10 2020 578418 PMC7575731 33117715
  182. [204]Ferraresi A. Girone C. Esposito A. Vidoni C. Vallino L. Secomandi E. How autophagy shapes the tumor microenvironment in ovarian cancer Front Oncol 10 2020 599915 PMC7753622 33364196
  183. [205]Mukhopadhyay S. Mahapatra K.K. Praharaj P.P. Patil S. Bhutia S.K. Recent progress of autophagy signaling in tumor microenvironment and its targeting for possible cancer therapeutics Semin Cancer Biol 85 2022 196 208 34500075
  184. [207]Chen J. Pitmon E. Microbiome Wang K. Inflammation and colorectal cancer Semin Immunol 32 2017 43 53 28982615
  185. [208]Goodman B. Gardner H. The microbiome and cancer J Pathol 244 2018 667 676 29377130
  186. [209]Gagliani N. Hu B. Huber S. Elinav E. Flavell R.A. The fire within: microbes inflame tumors Cell 157 2014 776 783 24813605
  187. [210]Arthur J.C. Jobin C. The complex interplay between inflammation, the microbiota and colorectal cancer Gut Microb 4 2013 253 258 PMC3669172 23549517
  188. [211]Zhang Z.L. Liao Y.Q. Tang D. Intratumoral microbiota: new frontiers in tumor immunity Carcinogenesis 43 2022 719 727 35868230
  189. [212]Jiang X.T. Xu J. Liu M.F. Xing H. Wang Z.M. Huang L. Adoptive CD8+ T cell therapy against cancer: challenges and opportunities Cancer Lett 462 2019 23 32 31356845
  190. [213]Lam K.C. Araya R.E. Huang A. Chen Q. Modica M.D. Rodrigues R.R. Microbiota triggers STING-type I IFN-dependent monocyte reprogramming of the tumor microenvironment Cell 184 2021 5338 5356 34624222 PMC8650838
  191. [215]Davidsson S. Carlsson J. Greenberg L. Wijkander J. Söderquist B. Erlandsson A. Cutibacterium acnes induces the expression of immunosuppressive genes in macrophages and is associated with an increase of regulatory T-Cells in prostate cancer Microbiol Spectr 9 2021 e01497-21 PMC8694172 34937192
  192. [216]Weber R. Groth C. Lasser S. Arkhypov I. Petrova V. Altevogt P. IL-6 as a major regulator of MDSC activity and possible target for cancer immunotherapy Cell Immunol 359 2021 104254 33296753
  193. [217]Long D.L. Liu M. Li H.Y. Song J.H. Jiang X.H. Wang G. Dysbacteriosis induces abnormal neurogenesis via LPS in a pathway requiring NF-κB/IL-6 Pharmacol Res 167 2021 105543 33711435
  194. [218]Hezaveh K. Shinde R.S. Klotgen A. Halaby M.J. Lamorte S. Ciudad M.T. Tryptophan-derived microbial metabolites activate the aryl hydrocarbon receptor in tumor-associated macrophages to suppress anti-tumor immunity Immunity 55 2022 324 340 35139353 PMC8888129
  195. [219]Alexander J.L. Kohoutova D. Powell N. Science in focus: the microbiome and cancer therapy Clin Oncol 31 2019 1 4 30301591
  196. [220]Fu Y.J. Liu S.S. Zeng S. Shen H. From bench to bed: the tumor immune microenvironment and current immunotherapeutic strategies for hepatocellular carcinoma J Exp Clin Canc Res 38 2019 396 PMC6734524 31500650
  197. [221]Wagner J. Rapsomaniki M.A. Chevrier S. Anzeneder T. Langwieder C. Dykgers A. A single-cell atlas of the tumor and immune ecosystem of human breast cancer Cell 177 2019 1330 1345 30982598 PMC6526772
  198. [222]Alexander J.L. Wilson I.D. Teare J. Marchesi J.R. Nicholson J.K. Kinross J.M. Gut microbiota modulation of chemotherapy efficacy and toxicity Nat Rev Gastro Hepat 14 2017 356 365 28270698
  199. [225]Panebianco C. Adamberg K. Jaagura M. Copetti M. Fontana A. Adamberg S. Influence of gemcitabine chemotherapy on the microbiota of pancreatic cancer xenografted mice Cancer Chemoth Pharm 81 2018 773 782 29473096
  200. [226]LaCourse K.D. Zepeda-Rivera M. Kempchinsky A.G. Baryiames A. Minot S.S. Johnston C.D. The cancer chemotherapeutic 5-fluorouracil is a potent Fusobacterium nucleatum inhibitor and its activity is modified by intratumoral microbiota Cell Rep 41 2022 111625 PMC10790632 36384132

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Authors
Fu, Y., Li, J., Cai, W., Huang, Y., Liu, X., Ma, Z., Tang, Z., Bian, X., Zheng, J., Jiang, J., & Li, C.
Affiliations
  • Southwest University (CN)
  • Army Medical University (CN)
Corresponding author
  • Zheng, Ji
  • Jiang, Jiayun
  • Li, Chong
Venue
Acta Pharmaceutica Sinica B
Publisher
Elsevier BV
Published
2024-04
Volume
14
Issue
4
Pages
1560-1591
ISSN
2211-3835 (ISSN-L)
OpenAlex
W4388706621
Cited by
48
References
30
Citations by year
2026: 20 · 2025: 19 · 2024: 9
FWCI
1.27
Type
journal article
Language
en
Open access
Locations
  • Acta Pharmaceutica Sinica B (publishedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • National Natural Science Foundation of China (82204281, CX2019LC107)
  • Natural Science Foundation of Chongqing (cstc2021jcyj, cstc2021jcyj-msxmX0544)
  • Army Medical University (CX2019LC107)
  • Centre Scientifique et Technique du Bâtiment
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Biotechnology › Cancer Research and Treatments
  • Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
Keywords
intratumoral microbiota, tumor microenvironment, tumor microbiome, microbial metabolites, pathogen-associated molecular patterns, autophagy, inflammation, immunomodulation, chemoresistance, cancer immunotherapy, antibiotics, synthetic biology, biomaterials

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