Cited by 8Gut microbiota and healthBacteriophages and microbial interactionsProbiotics and Fermented Foods

Bacteriophages, Antibiotics and Probiotics: Exploring the Microbial Battlefield of Colorectal Cancer

Open access
Volovat, Cristian Constantin, Cosovanu, Mihai Andrei, Ostafe, Madalina-Raluca, Augustin, Iolanda Georgiana, Volovat, Constantin, Georgescu, Bogdan, Volovat, Simona Ruxandra·2025·International Journal of Molecular Sciences

Abstract

Colorectal cancer (CRC), a prevalent malignancy, is a significant global health concern. The intricate interplay of genetic mutations, inflammatory processes, and environmental factors underscores the complexity of CRC’s etiology. The human gut harbors a diverse microbial community that plays a key role in maintaining homeostasis and influencing various aspects of host physiology. Perturbations in the gut microbiome (GM) composition and function have been implicated in CRC carcinogenesis. This bidirectional relationship involves microbial contributions to inflammation, DNA damage, and immune modulation, shaping the tumor microenvironment (TME). Bacteriophages, viruses that infect bacteria, contribute to the microbiome’s diversity and function by influencing bacterial abundance and composition. These phages can impact host–microbiome interactions, potentially influencing CRC risk. Furthermore, they can be manipulated to transport targeted medication, without being metabolized. Antibiotics exert selective pressures on the gut microbiome, leading to shifts in bacterial populations and potential dysbiosis. Probiotics can modulate the composition and activity of the GM and could be considered adjunctive therapy in the treatment of CRC. Understanding the intricate balance between bacteriophages, antibiotics–probiotics, and the GM is essential for comprehending CRC etiology and progression.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.3390/ijms26167837

Cites

7 of 7 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Precision microbial interventions, including engineered probiotics and bacteriophage therapy, have emerged as next-generation tools to selectively deplete procarcinogenic bacteria while enriching protective microbial taxa.

    “More recently, precision microbial interventions, including engineered probiotics and bacteriophage therapy, have emerged as next-generation tools to selectively deplete procarcinogenic bacteria while enriching protective microbial taxa [71]”

    From Phage therapy in oncology: opportunities for cancer prevention and treatment (2026) · cites this paper as [71]

    Section 5.3 reports a phage-based approach that inhibited a pro-tumoral bacterium and promoted an anti-tumoral one. Sections 7 and 8 describe bioengineered probiotics as promising, but do not show that they selectively deplete procarcinogenic bacteria while enriching protective taxa. The Conclusions frame the combined approach as a future possibility, rather than an established intervention. (LLM, conf=0.84)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 108

  1. [1]Shin A.E. Giancotti F.G. Rustgi A.K. Metastatic colorectal cancer: Mechanisms and emerging therapeutics Trends Pharmacol. Sci. 2023 44 222 236 10.1016/j.tips.2023.01.003 36828759 PMC10365888 · DOI
  2. [2]Liu Y. Lau H.C.H. Cheng W.Y. Yu J. Gut Microbiome in Colorectal Cancer: Clinical Diagnosis and Treatment Genom. Proteom. Bioinform. 2023 21 84 96 10.1016/j.gpb.2022.07.002 PMC10372906 35914737 · DOI
  3. [3]Jerin S. Harvey A.J. Lewis A. Therapeutic Potential of Protein Tyrosine Kinase 6 in Colorectal Cancer Cancers 2023 15 3703 10.3390/cancers15143703 37509364 PMC10377740 · DOI
  4. [4]Ni J.J. Li X.S. Zhang H. Xu Q. Wei X.T. Feng G.J. Zhao M. Zhang Z.J. Zhang L. Shen G.H. Mendelian randomization study of causal link from gut microbiota to colorectal cancer BMC Cancer 2022 22 1371 10.1186/s12885-022-10483-w 36585646 PMC9804960 · DOI
  5. [5]Fong W. Li Q. Yu J. Gut microbiota modulation: A novel strategy for prevention and treatment of colorectal cancer Oncogene 2020 39 4925 4943 10.1038/s41388-020-1341-1 32514151 PMC7314664 · DOI
  6. [6]Song M. Chan A.T. Environmental Factors, Gut Microbiota, and Colorectal Cancer Prevention Clin. Gastroenterol. Hepatol. 2019 17 275 289 10.1016/j.cgh.2018.07.012 30031175 PMC6314893 · DOI · Paper page
  7. [7]Coker O.O. Liu C. Wu W.K.K. Wong S.H. Jia W. Sung J.J.Y. Yu J. Altered gut metabolites and microbiota interactions are implicated in colorectal carcinogenesis and can be non-invasive diagnostic biomarkers Microbiome 2022 10 35 10.1186/s40168-021-01208-5 35189961 PMC8862353 · DOI
  8. [8]Torres-Maravilla E. Boucard A.-S. Mohseni A.H. Taghinezhad-S S. Cortes-Perez N.G. Bermúdez-Humarán L.G. Role of Gut Microbiota and Probiotics in Colorectal Cancer: Onset and Progression Microorganisms 2021 9 1021 10.3390/microorganisms9051021 34068653 PMC8151957 · DOI
  9. [9]Saus E. Iraola-Guzmán S. Willis J.R. Brunet-Vega A. Gabaldón T. Microbiome and colorectal cancer: Roles in carcinogenesis and clinical potential Mol. Asp. Med. 2019 69 93 106 10.1016/j.mam.2019.05.001 31082399 PMC6856719 · DOI
  10. [10]Eslami M. Yousefi B. Kokhaei P. Hemati M. Nejad Z.R. Arabkari V. Namdar A. Importance of probiotics in the prevention and treatment of colorectal cancer J. Cell. Physiol. 2019 234 17127 17143 10.1002/jcp.28473 30912128 · DOI · Paper page
  11. [11]Milani C. Duranti S. Bottacini F. Casey E. Turroni F. Mahony J. Belzer C. Delgado Palacio S. Arboleya Montes S. Mancabelli L. The First Microbial Colonizers of the Human Gut: Composition, Activities, and Health Implications of the Infant Gut Microbiota Microbiol. Mol. Biol. Rev. 2017 81 e00036-17 10.1128/MMBR.00036-17 PMC5706746 29118049 · DOI · Paper page
  12. [12]Illiano P. Brambilla R. Parolini C. The mutual interplay of gut microbiota, diet and human disease FEBS J. 2020 287 833 855 10.1111/febs.15217 31955527 · DOI
  13. [13]Pant A. Maiti T.K. Mahajan D. Das B. Human Gut Microbiota and Drug Metabolism Microb. Ecol. 2023 86 97 111 10.1007/s00248-022-02081-x 35869999 PMC9308113 · DOI
  14. [14]Góralczyk-Bińkowska A. Szmajda-Krygier D. Kozłowska E. The Microbiota–Gut–Brain Axis in Psychiatric Disorders IJMS 2022 23 11245 10.3390/ijms231911245 36232548 PMC9570195 · DOI
  15. [15]Quigley E.M.M. Microbiota-Brain-Gut Axis and Neurodegenerative Diseases Curr. Neurol. Neurosci. Rep. 2017 17 94 10.1007/s11910-017-0802-6 29039142 · DOI · Paper page
  16. [16]Dang A.T. Marsland B.J. Microbes, metabolites, and the gut–lung axis Mucosal Immunol. 2019 12 843 850 10.1038/s41385-019-0160-6 30976087 · DOI · Paper page
  17. [17]Huang Y. Xin W. Xiong J. Yao M. Zhang B. Zhao J. The Intestinal Microbiota and Metabolites in the Gut-Kidney-Heart Axis of Chronic Kidney Disease Front. Pharmacol. 2022 13 837500 35370631 PMC8971625
  18. [18]Zhang T. Sun P. Geng Q. Fan H. Gong Y. Hu Y. Shan L. Sun Y. Shen W. Zhou Y. Disrupted spermatogenesis in a metabolic syndrome model: The role of vitamin A metabolism in the gut–testis axis Gut 2022 71 78 87 10.1136/gutjnl-2020-323347 33504491 PMC8666830 · DOI
  19. [19]Mauro D. Nakamura A. Haroon N. Ciccia F. The gut-enthesis axis and the pathogenesis of Spondyloarthritis Semin. Immunol. 2021 58 101607 10.1016/j.smim.2022.101607 35850909 · DOI
  20. [22]Xu J.Y. Liu M.T. Tao T. Zhu X. Fei F.Q. The role of gut microbiota in tumorigenesis and treatment Biomed. Pharmacother. 2021 138 111444 10.1016/j.biopha.2021.111444 33662679 · DOI
  21. [23]Yu A.I. Zhao L. Eaton K.A. Ho S. Chen J. Poe S. Becker J. Gonzalez A. McKinstry D. Hasso M. Gut Microbiota Modulate CD8 T Cell Responses to Influence Colitis-Associated Tumorigenesis Cell Rep. 2020 31 107471 10.1016/j.celrep.2020.03.035 32268087 PMC7934571 · DOI
  22. [24]Hu C. Xu B. Wang X. Wan W.H. Lu J. Kong D. Jin Y. You W. Sun H. Mu X. Gut microbiota–derived short-chain fatty acids regulate group 3 innate lymphoid cells in HCC Hepatology 2023 77 48 64 10.1002/hep.32449 35262957 PMC9970019 · DOI
  23. [25]De Vos W.M. Tilg H. Van Hul M. Cani P.D. Gut microbiome and health: Mechanistic insights Gut 2022 71 1020 1032 10.1136/gutjnl-2021-326789 35105664 PMC8995832 · DOI · Paper page
  24. [26]Morrison D.J. Preston T. Formation of short chain fatty acids by the gut microbiota and their impact on human metabolism Gut Microbes 2016 7 189 200 10.1080/19490976.2015.1134082 26963409 PMC4939913 · DOI · Paper page
  25. [28]Mirzaei R. Afaghi A. Babakhani S. Sohrabi M.R. Hosseini-Fard S.R. Babolhavaeji K. Khani Ali Akbari S. Yousefimashouf R. Karampoor S. Role of microbiota-derived short-chain fatty acids in cancer development and prevention Biomed. Pharmacother. 2021 139 111619 10.1016/j.biopha.2021.111619 33906079 · DOI
  26. [29]Binienda A. Owczarek K. Sałaga M. Fichna J. Synthetic free fatty acid receptor (FFAR) 2 agonist 4-CMTB and FFAR4 agonist GSK13764 inhibit colon cancer cell growth and migration and regulate FFARs expression in in vitro and in vivo models of colorectal cancer Pharmacol. Rep. 2024 76 1403 1414 10.1007/s43440-024-00667-5 39432182 PMC11582145 · DOI
  27. [30]Rivas-Domínguez A. Pastor N. Martínez-López L. Colón-Pérez J. Bermúdez B. Orta M.L. The Role of DNA Damage Response in Dysbiosis-Induced Colorectal Cancer Cells 2021 10 1934 10.3390/cells10081934 34440703 PMC8391204 · DOI
  28. [31]Artemev A. Naik S. Pougno A. Honnavar P. Shanbhag N.M. The Association of Microbiome Dysbiosis with Colorectal Cancer Cureus 2022 14 e22156 Available online: https://www.cureus.com/articles/86171-the-association-of-microbiome-dysbiosis-with-colorectal-cancer (accessed on 10 January 2025) 10.7759/cureus.22156 35174040 PMC8840808 · DOI
  29. [32]Yu L.C.H. Microbiota dysbiosis and barrier dysfunction in inflammatory bowel disease and colorectal cancers: Exploring a common ground hypothesis J. Biomed. Sci. 2018 25 79 10.1186/s12929-018-0483-8 30413188 PMC6234774 · DOI
  30. [33]Wang X. Huycke M.M. Colorectal cancer: Role of commensal bacteria and bystander effects Gut Microbes 2015 6 370 376 10.1080/19490976.2015.1103426 26727419 PMC4826092 · DOI
  31. [34]Clay S.L. Fonseca-Pereira D. Garrett W.S. Colorectal cancer: The facts in the case of the microbiota J. Clin. Investig. 2022 132 e155101 10.1172/JCI155101 35166235 PMC8843708 · DOI · Paper page
  32. [35]Debelius J.W. Engstrand L. Matussek A. Brusselaers N. Morton J.T. Stenmarker M. Olsen R.S. The Local Tumor Microbiome Is Associated with Survival in Late-Stage Colorectal Cancer Patients. Xu ZZ, editor Microbiol. Spectr. 2023 11 e05066-22 10.1128/spectrum.05066-22 37042765 PMC10269740 · DOI
  33. [36]Karpiński T.M. Ożarowski M. Stasiewicz M. Carcinogenic microbiota and its role in colorectal cancer development Semin. Cancer Biol. 2022 86 420 430 10.1016/j.semcancer.2022.01.004 35090978 · DOI
  34. [37]Tran H.N.H. Thu T.N.H. Nguyen P.H. Vo C.N. Doan K.V. Nguyen Ngoc Minh C. Nguyen N.T. Ta V.N.D. Vu K.A. Hua T.D. Tumour microbiomes and Fusobacterium genomics in Vietnamese colorectal cancer patients npj Biofilms Microbiomes 2022 8 87 10.1038/s41522-022-00351-7 36307484 PMC9616903 · DOI
  35. [38]Kim H.S. Kim C.G. Kim W.K. Kim K.A. Yoo J. Min B.S. Paik S. Shin S.J. Lee H. Lee K. Fusobacterium nucleatum induces a tumor microenvironment with diminished adaptive immunity against colorectal cancers Front. Cell. Infect. Microbiol. 2023 13 1101291 10.3389/fcimb.2023.1101291 36960042 PMC10028079 · DOI
  36. [39]Padma S. Patra R. Sen Gupta P.S. Panda S.K. Rana M.K. Mukherjee S. Cell Surface Fibroblast Activation Protein-2 (Fap2) of Fusobacterium nucleatum as a Vaccine Candidate for Therapeutic Intervention of Human Colorectal Cancer: An Immunoinformatics Approach Vaccines 2023 11 525 10.3390/vaccines11030525 36992108 PMC10056511 · DOI
  37. [40]Ma X. Sun T. Zhou J. Zhi M. Shen S. Wang Y. Gu X. Li Z. Gao H. Wang P. Pangenomic Study of Fusobacterium nucleatum Reveals the Distribution of Pathogenic Genes and Functional Clusters at the Subspecies and Strain Levels Microbiol. Spectr. 2023 11 e05184-22 10.1128/spectrum.05184-22 37042769 PMC10269558 · DOI
  38. [41]Baik J.E. Li L. Shah M.A. Freedberg D.E. Jin Z. Wang T.C. Han Y.W. Circulating IgA Antibodies Against Fusobacterium nucleatum Amyloid Adhesin FadA are a Potential Biomarker for Colorectal Neoplasia Cancer Res. Commun. 2022 2 1497 1503 10.1158/2767-9764.CRC-22-0248 36970057 PMC10035380 · DOI
  39. [42]Mármol I. Sánchez-de-Diego C. Pradilla Dieste A. Cerrada E. Rodriguez Yoldi M. Colorectal Carcinoma: A General Overview and Future Perspectives in Colorectal Cancer Int. J. Mol. Sci. 2017 18 197 10.3390/ijms18010197 28106826 PMC5297828 · DOI
  40. [43]Fan X. Jin Y. Chen G. Ma X. Zhang L. Gut Microbiota Dysbiosis Drives the Development of Colorectal Cancer Digestion 2021 102 508 515 10.1159/000508328 32932258 · DOI
  41. [44]Rashid M.H. Full-length recombinant antibodies from Escherichia coli: Production, characterization, effector function (Fc) engineering, and clinical evaluation mAbs 2022 14 2111748 10.1080/19420862.2022.2111748 36018829 PMC9423848 · DOI
  42. [45]Meng C. Bai C. Brown T.D. Hood L.E. Tian Q. Human Gut Microbiota and Gastrointestinal Cancer Genom. Proteom. Bioinform. 2018 16 33 49 10.1016/j.gpb.2017.06.002 PMC6000254 29474889 · DOI
  43. [46]Purcell R.V. Permain J. Keenan J.I. Enterotoxigenic Bacteroides fragilis activates IL-8 expression through Stat3 in colorectal cancer cells Gut Pathog. 2022 14 16 10.1186/s13099-022-00489-x 35468857 PMC9036718 · DOI
  44. [47]Butt J. Jenab M. Werner J. Fedirko V. Weiderpass E. Dahm C.C. Tjønneland A. Olsen A. Boutron-Ruault M.C. Rothwell J.A. Association of Pre-diagnostic Antibody Responses to Escherichia coli and Bacteroides fragilis Toxin Proteins with Colorectal Cancer in a European Cohort Gut Microbes 2021 13 1903825 10.1080/19490976.2021.1903825 33874856 PMC8078709 · DOI
  45. [48]De Almeida C.V. Taddei A. Amedei A. The controversial role of Enterococcus faecalis in colorectal cancer Ther. Adv. Gastroenterol. 2018 11 1756284818783606 10.1177/1756284818783606 30013618 PMC6044108 · DOI
  46. [49]Koliarakis I. Messaritakis I. Nikolouzakis T.K. Hamilos G. Souglakos J. Tsiaoussis J. Oral Bacteria and Intestinal Dysbiosis in Colorectal Cancer IJMS 2019 20 4146 10.3390/ijms20174146 31450675 PMC6747549 · DOI
  47. [50]Chen X. Mendes B.G. Alves B.S. Duan Y. Phage therapy in gut microbiome Progress in Molecular Biology and Translational Science Elsevier Amsterdam, The Netherlands 2023 93 118 Available online: https://linkinghub.elsevier.com/retrieve/pii/S1877117323001138 (accessed on 10 January 2025) 37770177
  48. [52]Mushegian A.R. Are There 1031 Virus Particles on Earth, or More, or Fewer? J. Bacteriol. 2020 202 e00052-20 10.1128/JB.00052-20 32071093 PMC7148134 · DOI
  49. [53]Cao Z. Sugimura N. Burgermeister E. Ebert M.P. Zuo T. Lan P. The gut virome: A new microbiome component in health and disease eBioMedicine 2022 81 104113 10.1016/j.ebiom.2022.104113 35753153 PMC9240800 · DOI
  50. [54]Tobin C.A. Hill C. Shkoporov A.N. Factors Affecting Variation of the Human Gut Phageome Annu. Rev. Microbiol. 2023 77 363 379 10.1146/annurev-micro-032421-105754 37307857 · DOI
  51. [55]Liu S. Lu H. Zhang S. Shi Y. Chen Q. Phages against Pathogenic Bacterial Biofilms and Biofilm-Based Infections: A Review Pharmaceutics 2022 14 427 10.3390/pharmaceutics14020427 35214158 PMC8875263 · DOI
  52. [56]El Haddad L. Mendoza J.F. Jobin C. Bacteriophage-mediated manipulations of microbiota in gastrointestinal diseases Front. Microbiol. 2022 13 1055427 10.3389/fmicb.2022.1055427 36466675 PMC9714271 · DOI
  53. [57]Marongiu L. Burkard M. Venturelli S. Allgayer H. Dietary Modulation of Bacteriophages as an Additional Player in Inflammation and Cancer Cancers 2021 13 2036 10.3390/cancers13092036 33922485 PMC8122878 · DOI
  54. [58]Murgas P. Bustamante N. Araya N. Cruz-Gómez S. Durán E. Gaete D. Oyarce C. López E. Herrada A.A. Ferreira N. A filamentous bacteriophage targeted to carcinoembryonic antigen induces tumor regression in mouse models of colorectal cancer Cancer Immunol. Immunother. 2018 67 183 193 10.1007/s00262-017-2076-x 29026949 PMC11028317 · DOI
  55. [59]Luo S. Ru J. Mirzaei M.K. Xue J. Peng X. Ralser A. Mejías-Luque R. Gerhard M. Deng L. Gut virome profiling identifies an association between temperate phages and colorectal cancer promoted by Helicobacter pylori infection Gut Microbes 2023 15 2257291 10.1080/19490976.2023.2257291 37747149 PMC10578192 · DOI
  56. [60]Marongiu L. Allgayer H. Viruses in colorectal cancer Mol. Oncol. 2022 16 1423 1450 10.1002/1878-0261.13100 34514694 PMC8978519 · DOI
  57. [61]Zheng D.W. Dong X. Pan P. Chen K.W. Fan J.X. Cheng S.X. Zhang X.Z. Phage-guided modulation of the gut microbiota of mouse models of colorectal cancer augments their responses to chemotherapy Nat. Biomed. Eng. 2019 3 717 728 10.1038/s41551-019-0423-2 31332342 · DOI
  58. [62]Dong X. Pan P. Zheng D.W. Bao P. Zeng X. Zhang X.Z. Bioinorganic hybrid bacteriophage for modulation of intestinal microbiota to remodel tumor-immune microenvironment against colorectal cancer Sci. Adv. 2020 6 eaba1590 10.1126/sciadv.aba1590 32440552 PMC7228756 · DOI
  59. [63]Huh H. Chen D.W. Foldvari M. Slavcev R. Blay J. EGFR-targeted bacteriophage lambda penetrates model stromal and colorectal carcinoma tissues, is taken up into carcinoma cells, and interferes with 3-dimensional tumor formation Front. Immunol. 2022 13 957233 10.3389/fimmu.2022.957233 36591314 PMC9800840 · DOI
  60. [64]Gabrielaitis D. Zitkute V. Saveikyte L. Labutyte G. Skapas M. Meskys R. Casaite V. Sasnauskiene A. Neniskyte U. Nanotubes from bacteriophage tail sheath proteins: Internalisation by cancer cells and macrophages Nanoscale Adv. 2023 5 3705 3716 10.1039/D3NA00166K 37441259 PMC10334369 · DOI
  61. [65]Rychahou P. Haque F. Shu Y. Zaytseva Y. Weiss H.L. Lee E.Y. Mustain W. Valentino J. Guo P. Evers B.M. Delivery of RNA Nanoparticles into Colorectal Cancer Metastases Following Systemic Administration ACS Nano 2015 9 1108 1116 10.1021/acsnano.5b00067 25652125 PMC4613746 · DOI
  62. [66]Kabwe M. Meehan-Andrews T. Ku H. Petrovski S. Batinovic S. Chan H.T. Tucci J. Lytic Bacteriophage EFA1 Modulates HCT116 Colon Cancer Cell Growth and Upregulates ROS Production in an Enterococcus faecalis Co-culture System Front. Microbiol. 2021 12 650849 10.3389/fmicb.2021.650849 33868210 PMC8044584 · DOI
  63. [67]Rama A.R. Hernandez R. Perazzoli G. Burgos M. Melguizo C. Vélez C. Prados J. Specific Colon Cancer Cell Cytotoxicity Induced by Bacteriophage E Gene Expression under Transcriptional Control of Carcinoembryonic Antigen Promoter IJMS 2015 16 12601 12615 10.3390/ijms160612601 26053394 PMC4490463 · DOI
  64. [68]Prados, E Phage gene transfection enhances sensitivity of lung and colon cancer cells to chemotherapeutic agents Int. J. Oncol. 2010 37 1503 1514 Available online: http://www.spandidos-publications.com/ijo/37/6/1503 (accessed on 10 January 2025) 21042719
  65. [69]Zhang W. Zhang J. Liu T. Xing J. Zhang H. Wang D. Tang D. Bidirectional effects of intestinal microbiota and antibiotics: A new strategy for colorectal cancer treatment and prevention J. Cancer Res. Clin. Oncol. 2022 148 2387 2404 10.1007/s00432-022-04081-3 35661254 PMC11800900 · DOI
  66. [70]Qu G. Sun C. Sharma M. Uy J.P. Song E.J. Bhan C. Shu L. Is antibiotics use really associated with increased risk of colorectal cancer? An updated systematic review and meta-analysis of observational studies Int. J. Color. Dis. 2020 35 1397 1412 10.1007/s00384-020-03658-z 32504337 · DOI
  67. [71]Weng L. Jin F. Shi J. Qiu Z. Chen L. Li Q. He C. Cheng Z. Antibiotics use and risk of colorectal neoplasia: An updated meta-analysis Int. J. Color. Dis. 2022 37 2291 2301 10.1007/s00384-022-04276-7 36329204 · DOI
  68. [72]Bullman S. Pedamallu C.S. Sicinska E. Clancy T.E. Zhang X. Cai D. Neuberg D. Huang K. Guevara F. Nelson T. Analysis of Fusobacterium persistence and antibiotic response in colorectal cancer Science 2017 358 1443 1448 10.1126/science.aal5240 29170280 PMC5823247 · DOI · Paper page
  69. [73]Stott K.J. Phillips B. Parry L. May S. Recent advancements in the exploitation of the gut microbiome in the diagnosis and treatment of colorectal cancer Biosci. Rep. 2021 41 BSR20204113 10.1042/BSR20204113 34236075 PMC8314433 · DOI
  70. [74]Lu S.S.M. Mohammed Z. Häggström C. Myte R. Lindquist E. Gylfe Å. Van Guelpen B. Harlid S. Antibiotics Use and Subsequent Risk of Colorectal Cancer: A Swedish Nationwide Population-Based Study JNCI J. Natl. Cancer Inst. 2022 114 38 46 10.1093/jnci/djab125 34467395 PMC8755503 · DOI
  71. [76]Derosa L. Routy B. Desilets A. Daillère R. Terrisse S. Kroemer G. Zitvogel L. Microbiota-Centered Interventions: The Next Breakthrough in Immuno-Oncology? Cancer Discov. 2021 11 2396 2412 10.1158/2159-8290.CD-21-0236 34400407 · DOI · Paper page
  72. [77]RoRoberti M.P. Yonekura S. Duong C.P.M. Picard M. Ferrere G. Tidjani Alou M. Rauber C. Iebba V. Lehmann C.H.K. Amon L. Chemotherapy-induced ileal crypt apoptosis and the ileal microbiome shape immunosurveillance and prognosis of proximal colon cancer Nat. Med. 2020 26 919 931 10.1038/s41591-020-0882-8 32451498 · DOI · Paper page
  73. [78]Bhatt A.P. Redinbo M.R. Bultman S.J. The role of the microbiome in cancer development and therapy CA A Cancer J. Clin. 2017 67 326 344 10.3322/caac.21398 28481406 PMC5530583 · DOI · Paper page
  74. [79]Zhou Y. Deng Y. Wang J. Yan Z. Wei Q. Ye J. Zhang J. He T.C. Qiao M. Effect of antibiotic monensin on cell proliferation and IGF1R signaling pathway in human colorectal cancer cells Ann. Med. 2023 55 954 964 10.1080/07853890.2023.2166980 36896461 PMC10795625 · DOI
  75. [80]Seçme M. Kocoglu S.S. Investigation of the TLR4 and IRF3 signaling pathway-mediated effects of monensin in colorectal cancer cells Med. Oncol. 2023 40 187 10.1007/s12032-023-02055-0 37219624 · DOI
  76. [81]Liu X.M. Zhu W.T. Jia M.L. Li Y.T. Hong Y. Liu Z.Q. Yan P.K. Rapamycin Liposomes Combined with 5-Fluorouracil Inhibits Angiogenesis and Tumor Growth of APC (Min/+) Mice and AOM/DSS-Induced Colorectal Cancer Mice Int. J. Nanomed. 2022 17 5049 5061 10.2147/IJN.S373777 36325149 PMC9621024 · DOI
  77. [82]Klose J. Trefz S. Wagner T. Steffen L. Preißendörfer Charrier A. Radhakrishnan P. Volz C. Schmidt T. Ulrich A. Dieter S.M. Salinomycin: Anti-tumor activity in a pre-clinical colorectal cancer model PLoS ONE 2019 14 e0211916 10.1371/journal.pone.0211916 30763370 PMC6375586 · DOI
  78. [83]Klose J. Kattner S. Borgström B. Volz C. Schmidt T. Schneider M. Oredsson S. Strand D. Ulrich A. Semi-synthetic salinomycin analogs exert cytotoxic activity against human colorectal cancer stem cells Biochem. Biophys. Res. Commun. 2018 495 53 59 10.1016/j.bbrc.2017.10.147 29107689 · DOI
  79. [84]Liu F. Lv R.B. Liu Y. Hao Q. Liu S.J. Zheng Y.Y. Li C. Zhu C. Wang M. Salinomycin and Sulforaphane Exerted Synergistic Antiproliferative and Proapoptotic Effects on Colorectal Cancer Cells by Inhibiting the PI3K/Akt Signaling Pathway in vitro and in vivo OncoTargets Ther. 2020 13 4957 4969 10.2147/OTT.S246706 PMC7276212 32581555 · DOI
  80. [85]Liu F. Li W. Hua S. Han Y. Xu Z. Wan D. Wang Y. Chen W. Kuang Y. Shi J. Nigericin Exerts Anticancer Effects on Human Colorectal Cancer Cells by Inhibiting Wnt/β-catenin Signaling Pathway Mol. Cancer Ther. 2018 17 952 965 10.1158/1535-7163.MCT-17-0906 29483216 · DOI
  81. [86]Garcia-Princival I.M.R. Princival J.L. Dias da Silva E. de Arruda Lima S.M. Carregosa J.C. Wisniewski A. Jr. de Lucena C.C.O. Halwass F. Alves Franca J.A. Ferreira L.F.G.R. Streptomyces hygroscopicus UFPEDA 3370: A valuable source of the potent cytotoxic agent nigericin and its evaluation against human colorectal cancer cells Chem. -Biol. Interact. 2021 333 109316 10.1016/j.cbi.2020.109316 33285127 · DOI
  82. [87]Ruiz-Malagón A.J. Hidalgo-García L. Rodríguez-Sojo M.J. Molina-Tijeras J.A. García F. Diez-Echave P. Vezza T. Becerra P. Marchal J.A. Redondo-Cerezo E. Tigecycline reduces tumorigenesis in colorectal cancer via inhibition of cell proliferation and modulation of immune response Biomed. Pharmacother. 2023 163 114760 10.1016/j.biopha.2023.114760 37119741 · DOI
  83. [88]Yang L. Yang J. Liu H. Lan J. Xu Y. Wu X. Mao Y. Wu D. Pan K. Zhang T. Minocycline binds and inhibits LYN activity to prevent STAT3-meditated metastasis of colorectal cancer Int. J. Biol. Sci. 2022 18 2540 2552 10.7150/ijbs.70708 35414768 PMC8990469 · DOI
  84. [89]Kabir S.R. Islam T. Antimycin A induced apoptosis in HCT-116 colorectal cancer cells through the up- and downregulation of multiple signaling pathways Med. Oncol. 2022 40 51 10.1007/s12032-022-01901-x 36527492 · DOI
  85. [90]Petroni G. Bagni G. Iorio J. Duranti C. Lottini T. Stefanini M. Kragol G. Becchetti A. Arcangeli A. Clarithromycin inhibits autophagy in colorectal cancer by regulating the hERG1 potassium channel interaction with PI3K Cell Death Dis. 2020 11 161 10.1038/s41419-020-2349-8 32123164 PMC7052256 · DOI
  86. [91]Kvakova M. Kamlarova A. Stofilova J. Benetinova V. Bertkova I. Probiotics and postbiotics in colorectal cancer: Prevention and complementary therapy World J. Gastroenterol. 2022 28 3370 3382 10.3748/wjg.v28.i27.3370 36158273 PMC9346452 · DOI
  87. [92]Lamichhane P. Maiolini M. Alnafoosi O. Hussein S. Alnafoosi H. Umbela S. Richardson T. Alla N. Lamichhane N. Subhadra B. Colorectal Cancer and Probiotics: Are Bugs Really Drugs? Cancers 2020 12 1162 10.3390/cancers12051162 32380712 PMC7281248 · DOI
  88. [93]Tang G. Zhang L. Update on Strategies of Probiotics for the Prevention and Treatment of Colorectal Cancer Nutr. Cancer 2022 74 27 38 10.1080/01635581.2020.1865420 33356609 · DOI
  89. [94]Zhao J. Liao Y. Wei C. Ma Y. Wang F. Chen Y. Zhao B. Ji H. Wang D. Tang D. Potential Ability of Probiotics in the Prevention and Treatment of Colorectal Cancer Clin. Med. Insights Oncol. 2023 17 11795549231188225 10.1177/11795549231188225 37601319 PMC10437046 · DOI
  90. [95]Zhao T. Wang H. Liu Z. Liu Y. DeJi Li B. Huang X. Recent Perspective of Lactobacillus in Reducing Oxidative Stress to Prevent Disease Antioxidants 2023 12 769 10.3390/antiox12030769 36979017 PMC10044891 · DOI
  91. [96]Shang F. Jiang X. Wang H. Chen S. Wang X. Liu Y. Guo S. Li D. Yu W. Zhao Z. The inhibitory effects of probiotics on colon cancer cells: In vitro and in vivo studies J. Gastrointest. Oncol. 2020 11 1224 1232 10.21037/jgo-20-573 33456995 PMC7807261 · DOI
  92. [97]Tripathy A. Dash J. Kancharla S. Kolli P. Mahajan D. Senapati S. Jena M.K. Probiotics: A Promising Candidate for Management of Colorectal Cancer Cancers 2021 13 3178 10.3390/cancers13133178 34202265 PMC8268640 · DOI
  93. [98]Zaharuddin L. Mokhtar N.M. Muhammad Nawawi K.N. Raja Ali R.A. A randomized double-blind placebo-controlled trial of probiotics in post-surgical colorectal cancer BMC Gastroenterol. 2019 19 131 10.1186/s12876-019-1047-4 31340751 PMC6657028 · DOI
  94. [99]Zamani F. Khalighfard S. Kalhori M.R. Poorkhani A. Amiriani T. Hosseinzadeh P. Esmati E. Alemrajabi M. Nikoofar A. Safarnezhad Tameshkel F. Expanding CYLD protein in NF-κβ/TNF-α signaling pathway in response to Lactobacillus acidophilus in non-metastatic rectal cancer patients Med. Oncol. 2023 40 302 10.1007/s12032-023-02170-y 37725175 · DOI
  95. [100]Khodaii Z. Mehrabani Natanzi M. Khalighfard S. Ghandian Zanjan M. Gharghi M. Khori V. Amiriani T. Rahimkhani M. Alizadeh A.M. Novel targets in rectal cancer by considering lncRNA–miRNA–mRNA network in response to Lactobacillus acidophilus consumption: A randomized clinical trial Sci. Rep. 2022 12 9168 10.1038/s41598-022-13297-9 35654932 PMC9163174 · DOI
  96. [101]Ha S. Zhang X. Yu J. Probiotics intervention in colorectal cancer: From traditional approaches to novel strategies Chin. Med. J. 2024 137 8 20 10.1097/CM9.0000000000002955 38031348 PMC10766304 · DOI
  97. [102]Stoeva M.K. Garcia-So J. Justice N. Myers J. Tyagi S. Nemchek M. McMurdie P.J. Kolterman O. Eid J. Butyrate-producing human gut symbiont, Clostridium butyricum, and its role in health and disease Gut Microbes 2021 13 1907272 10.1080/19490976.2021.1907272 33874858 PMC8078720 · DOI
  98. [103]Zhang K. Dong Y. Li M. Zhang W. Ding Y. Wang X. Chen D. Liu T. Wang B. Cao H. Clostridium butyricum inhibits epithelial–mesenchymal transition of intestinal carcinogenesis through downregulating METTL3 Cancer Sci. 2023 114 3114 3127 10.1111/cas.15839 37243376 PMC10394142 · DOI
  99. [104]Dikeocha I.J. Al-Kabsi A.M. Chiu H.T. Alshawsh M.A. Faecalibacterium prausnitzii Ameliorates Colorectal Tumorigenesis and Suppresses Proliferation of HCT116 Colorectal Cancer Cells Biomedicines 2022 10 1128 10.3390/biomedicines10051128 35625865 PMC9138996 · DOI · Paper page
  100. [105]Guo J. Meng F. Hu R. Chen L. Chang J. Zhao K. Ren H. Liu Z. Hu P. Wang G. Inhibition of the NF-κB/HIF-1α signaling pathway in colorectal cancer by tyrosol: A gut microbiota-derived metabolite J. Immunother. Cancer 2024 12 e008831 10.1136/jitc-2024-008831 39343509 PMC11440206 · DOI
  101. [106]Faghfuri E. Gholizadeh P. The role of Akkermansia muciniphila in colorectal cancer: A double-edged sword of treatment or disease progression? Biomed. Pharmacother. 2024 173 116416 10.1016/j.biopha.2024.116416 38471272 · DOI
  102. [108]Terrisse S. Goubet A.G. Ueda K. Thomas A.M. Quiniou V. Thelemaque C. Dunsmore G. Clave E. Gamat-Huber M. Yonekura S. Immune system and intestinal microbiota determine efficacy of androgen deprivation therapy against prostate cancer J. Immunother. Cancer 2022 10 e004191 10.1136/jitc-2021-004191 35296557 PMC8928383 · DOI · Paper page
  103. [110]Gurbatri C.R. Radford G.A. Vrbanac L. Im J. Thomas E.M. Coker C. Taylor S.R. Jang Y. Sivan A. Rhee K. Engineering tumor-colonizing E. coli Nissle 1917 for detection and treatment of colorectal neoplasia Nat. Commun. 2024 15 646 10.1038/s41467-024-44776-4 38245513 PMC10799955 · DOI
  104. [111]Huang F. Li S. Chen W. Han Y. Yao Y. Yang L. Li Q. Xiao Q. Wei J. Liu Z. Postoperative Probiotics Administration Attenuates Gastrointestinal Complications and Gut Microbiota Dysbiosis Caused by Chemotherapy in Colorectal Cancer Patients Nutrients 2023 15 356 10.3390/nu15020356 36678227 PMC9861237 · DOI
  105. [112]Lee J.Y. Chu S.H. Jeon J.Y. Lee M.K. Park J.H. Lee D.C. Lee J.W. Kim N.K. Effects of 12 weeks of probiotic supplementation on quality of life in colorectal cancer survivors: A double-blind, randomized, placebo-controlled trial Dig. Liver Dis. 2014 46 1126 1132 10.1016/j.dld.2014.09.004 25442120 · DOI
  106. [113]Golkhalkhali B. Rajandram R. Paliany A.S. Ho G.F. Wan Ishak W.Z. Johari C.S. Chin K.D. Strain-specific probiotic (microbial cell preparation) and omega-3 fatty acid in modulating quality of life and inflammatory markers in colorectal cancer patients: A randomized controlled trial Asia-Pac. J. Clin. Oncol. 2018 14 179 191 10.1111/ajco.12758 28857425 · DOI
  107. [114]Bajramagic S. Hodzic E. Mulabdic A. Holjan S. Smajlovic S. Rovcanin A. Usage of Probiotics and its Clinical Significance at Surgically Treated Patients Sufferig from Colorectal Carcinoma Med. Arch. 2019 73 316 10.5455/medarh.2019.73.316-320 31819304 PMC6885229 · DOI
  108. [115]Polakowski C.B. Kato M. Preti V.B. Schieferdecker M.E.M. Ligocki Campos A.C. Impact of the preoperative use of synbiotics in colorectal cancer patients: A prospective, randomized, double-blind, placebo-controlled study Nutrition 2019 58 40 48 10.1016/j.nut.2018.06.004 30278428 · DOI

Cited by

Sorted by citations

Authors
Volovat, C. C., Cosovanu, M. A., Ostafe, M.-R., Augustin, I. G., Volovat, C., Georgescu, B., & Volovat, S. R.
Affiliations
  • Department of Radiology, “Grigore T. Popa” University of Medicine and Pharmacy, 700115 Iasi, Romania
  • Center of Oncology Euroclinic, 700106 Iasi, Romania
  • Department of Medical Oncology-Radiotherapy, “Grigore T. Popa” University of Medicine and Pharmacy, 16 University Street, 700115 Iasi, Romania
  • Institutul Oncologic Bucuresti (RO)
  • Grigore T. Popa University of Medicine and Pharmacy (RO)
  • Carol Davila University of Medicine and Pharmacy (RO)
Corresponding author
  • Cosovanu, Mihai Andrei
  • Augustin, Iolanda Georgiana
Venue
International Journal of Molecular Sciences
Publisher
MDPI AG
Published
2025-08-13
Volume
26
Issue
16
Pages
7837
ISSN
1422-0067 (ISSN-L)
OpenAlex
W4413127654
Cited by
8
References
7
Citations by year
2026: 7 · 2025: 1
FWCI
0.70
Type
journal article
Language
en
Open access
Locations
  • International Journal of Molecular Sciences (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
  • Physical Sciences › Environmental Science › Ecology › Bacteriophages and microbial interactions
  • Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
Keywords
colorectal cancer, bacteriophages, antibiotics, probiotics, gut microbiota, tumor microenvironment, dysbiosis, host-microbiome interactions, carcinogenesis, inflammation, DNA damage, immunomodulation, targeted drug delivery
MeSH terms
Gastrointestinal Microbiome, Animals, Anti-Bacterial Agents, Bacteriophages, Humans, Colorectal Neoplasms, Probiotics, Tumor Microenvironment, Dysbiosis

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review