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Gut microbiota, inflammation and colorectal cancer
Open accessAbstract
Although genes contribute to colorectal cancer, the gut microbiota are an important player. Accumulating evidence suggests that chronic infection and the ensuing inflammation contributes to tumor initiation and tumor progression. A variety of bacterial species and tumor-promoting virulence mechanisms have been investigated. Significant advances have been made in understanding the composition and functional capabilities of the gut microbiota and its roles in cancer. In the current review, we discuss the novel roles of microbiota in the progression of colon cancer. Although microbiota technically include organisms other than bacteria e.g., viruses and fungi, this review will primarily focus on bacteria. We summarize epidemiological studies of human microbiome and colon cancer. We discuss the progress in the scientific understanding of the interplay between the gut microbiota, barrier function, and host responses in experimental models. Further, we discuss the potential application in prevention, diagnosis, and therapy of colon cancer by targeting microbiota. We discuss the challenges lie ahead and the future direction in studying gut microbiome in colon cancer to close the gap between the basic sciences and clinical application.
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“Strategies to detect specific bacteria or bacterial DNA sequences might be used in screening for early-stage colorectal adenomas or carcinomas.60, 61”
From Influence of the Gut Microbiome, Diet, and Environment on Risk of Colorectal Cancer (2020) · cites this paper as [60]
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“Recently, accumulating evidence by metagenome-wide association studies indicated an association between gut microbiota dysbiosis and CRC, and enteropathogenic microorganism plays a role in shaping the inflammatory environment and promoting tumor initiation and progression (4, 5).”
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BackgroundInfluentialEfficient inter-species conjugative transfer of a CRISPR nuclease for targeted bacterial killing
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“Several current studies that assessed beta diversity through 16S rRNA sequencing have illustrated structural differences amongst the gut microbiota, where samples belonging to different disease status (cancer, adenoma, or control/normal adjacent tissue) cluster in different two-dimensional spaces indicating the presen…”
BackgroundMicrobiome or Infections: Amyloid-Containing Biofilms as a Trigger for Complex Human Diseases
Miller, A. L., Bessho, S., Grando, K. C. M., & Tükel, Ç. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.638867 · Cited by 136
“Specific changes within the intestinal microbial community are observed in CRC patients, such as increased abundance of Fusobacteria, Alistipes, Porphyromonadaceae, Coriobacteridae, Staphylococcaceae, Akkermansia, and Methanobacteriales, while representation of Bifidobacterium, Lactobacillus, Ruminococcus, Faecalibact…”
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“Potentially, this reduces the generation of short-chain fatty acids such as butyrate which has also been reported to reduce the risk for cancer development (Sun and Kato, 2016).”
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“Similarly, other common bacteria of the human gut, such as Streptococcus gallolyticus and Helicobacter pylori, are believed to be involved in colorectal cancer [26].”
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“There are some recent reports on linkage between gut microbiome and colorectal cancer (Sun and Kato, 2016), including the role of E.”
BackgroundNovel Regulatory Roles of Wnt1 in Infection-Associated Colorectal Cancer
Wang, J., Lu, R., Fu, X., Dan, Z., Zhang, Y., Chang, X., Liu, Q., Xia, Y., Liu, X., & Sun, J. (2018) · Neoplasia · doi:10.1016/j.neo.2018.03.001 · Cited by 45
“001 Introduction Growing interest and accumulating data on human microbiota indicate that host-microbe interplay has an important role in the development of colorectal cancer (CRC) [1], which suggests that chronic infection and inflammation contribute to tumor initiation and tumor progression [2].”
BackgroundPotential biomarkers associated with oxidative stress for risk assessment of colorectal cancer
Mandal, P. (2017) · Naunyn-Schmiedeberg s Archives of Pharmacology · doi:10.1007/s00210-017-1352-9 · Cited by 44
“Cespedes Feliciano et al. (2016) reported that the effects of obesity and metabolic dysregulation on cancer survival are inconsistent with metabolic syndrome (MetSyn).”
BackgroundBile acids as carcinogens in the colon and at other sites in the gastrointestinal system
Bernstein, H., & Bernstein, C. (2022) · Experimental Biology and Medicine · doi:10.1177/15353702221131858 · Cited by 45
von Frieling, J., Fink, C., Hamm, J., Klischies, K., Förster, M., Bosch, T. C. G., Roeder, T., Rosenstiel, P. C., & Sommer, F. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.02020 · Cited by 45
“This topic is extensively covered by excellent recent publications to which we refer to for further reading (Shebl et al., 2012; Antonic et al., 2013; Cummins and Tangney, 2013; Sun and Kato, 2016; Pasquereau-Kotula et al., 2018).”
BackgroundEscherichia coli and Colorectal Cancer: Unfolding the Enigmatic Relationship
Rezaee, M. A., Nouri, R., Hasani, A., Shirazi, K. M., Alivand, M. R., Sepehri, B., Sotoodeh, S., & Hemmati, F. (2021) · Current Pharmaceutical Biotechnology · doi:10.2174/1389201022666210910094827 · Cited by 47
Microbiota and epigenetics: promising therapeutic approaches?
El-Sayed, A., Aleya, L., & Kamel, M. S. (2021) · Environmental Science and Pollution Research · doi:10.1007/s11356-021-15623-6 · Cited by 43
“In addition to breast cancer, a clear relationship between microbiota and other cancer types was described in the literature where the microbiome is involved directly/indirectly, completely/partially in the induction of different cancer types affecting the digestive tract (Borges-Canha et al. 2015; Dahiya and Renuka 2…”
BackgroundThe Effect of Microbiota on Colon Carcinogenesis
Yoon, K., & Kim, N. (2018) · Journal of Cancer Prevention · doi:10.15430/jcp.2018.23.3.117 · Cited by 43
“Adapted from Sun and Kato.(15) COLORECTAL NEOPLASM”
BackgroundInfluence of Iron on the Gut Microbiota in Colorectal Cancer
Phipps, O., Al-Hassi, H. O., Quraishi, M. N., Kumar, A., & Brookes, M. (2020) · Nutrients · doi:10.3390/nu12092512 · Cited by 41
“Cancer occurrence in the large intestines is approximately 12-fold higher than the small intestines [33].”
BackgroundXi, Y., Jing, Z., Wu, W., Zhang, C., Quan, Q., Zhou, Q., Jiamin, X., & Han, S. (2021) · BMC Cancer · doi:10.1186/s12885-021-07845-1 · Cited by 40
Huang, Z., Yang, W., Wang, X., Guo, F., Cheng, Y., Cao, L., Zhu, W., Sun, Y., & Xiong, H. (2022) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.2c00585 · Cited by 40
Xia, W., Liu, B., Tang, S., Yasir, M., & Khan, I. (2022) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2022.875513 · Cited by 40
“A balanced GM is key to host health, and any dysbiosis in gut microbial composition could put the host at a risk for obesity, inflammatory bowel disease, diabetes, autism, rheumatoid arthritis, and colorectal cancer (CRC) (Musso et al., 2010; Stefka et al., 2014; Sun and Kato, 2016; Maeda and Takeda, 2017).”
BackgroundColorectal cancer: The epigenetic role of microbiome
Sabit, H., Çevik, E., & Tombuloğlu, H. (2019) · World Journal of Clinical Cases · doi:10.12998/wjcc.v7.i22.3683 · Cited by 39
Oral–Gut Microbiome Axis in Gastrointestinal Disease and Cancer
Park, S.-Y., Hwang, B.-O., Lim, M., Ok, S. H., Lee, S., Chun, K., Park, K.-K., Hu, Y., Chung, W., & Song, N. (2021) · Cancers · doi:10.3390/cancers13071748 · Cited by 44
Molecular mechanistic pathway of colorectal carcinogenesis associated with intestinal microbiota
Mandal, P. (2017) · Anaerobe · doi:10.1016/j.anaerobe.2017.12.008 · Cited by 42
Influence of Gut Microbiota-Mediated Immune Regulation on Response to Chemotherapy
Deng, Y., Hou, X., Wang, H., Du, H., & Liu, Y. (2024) · Pharmaceuticals · doi:10.3390/ph17050604 · Cited by 39
“SCFAs also promote the differentiation of T-cells into effector T-cells (Th1 and Th17 cell) [94,104].”
BackgroundMudd, A. M., Gu, T., Munagala, R., Jeyabalan, J., Egilmez, N. K., & Gupta, R. C. (2019) · Cancer Prevention Research · doi:10.1158/1940-6207.capr-19-0362 · Cited by 37
“enterica), and enterotoxigenic Bacteriodes fragilis (ETBF) (9).”
Wang, T., Wang, P., Ge, W., Shi, C., Xiao, G., Wang, X., & Lü, X. (2021) · Food & Function · doi:10.1039/d1fo01531a · Cited by 37
Mechanism of Bile Acid-Induced Programmed Cell Death and Drug Discovery against Cancer: A Review
Jang, J. Y., Im, E., Choi, Y. H., & Kim, N. D. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23137184 · Cited by 36
“UDCA is the most hydrophilic bile acid, while DCA and LCA are the least polar and most toxic bile acids that can contribute to the development of colorectal cancer [45].”
BackgroundRole of preoperative gut microbiota on colorectal anastomotic leakage: preliminary results
Palmisano, S., Campisciano, G., Iacuzzo, C., Bonadio, L., Zucca, A., Cosola, D., Comar, M., & de Manzini, N. (2020) · Updates in Surgery · doi:10.1007/s13304-020-00720-x · Cited by 41
“Finally, as in the literature several studies show that the colorectal microbiota of individuals affected by cancer presents a decreased level of biodiversity [3, 6, 33], we analyzed the α-diversity.”
ResultRegulation of tissue-resident memory T cells by the Microbiota
Overacre-Delgoffe, A. E., & Hand, T. W. (2022) · Mucosal Immunology · doi:10.1038/s41385-022-00491-1 · Cited by 40
Huang, Q., Wei, X., Li, W., Ma, Y., Chen, G., Zhao, L., Jiang, Y., Xie, S., Chen, Q., & Chen, T. (2022) · Cancers · doi:10.3390/cancers14215178 · Cited by 36
“Accumulating evidence has shown that microbiota is viewed as an increasingly important factor in the initiation and progression of many diseases, including cancer [15–18].”
BackgroundConnect between gut microbiome and diseases of the human eye
Shivaji, S. (2019) · Journal of Biosciences · doi:10.1007/s12038-019-9931-1 · Cited by 34
Ibrahim, I. A. A., Alzahrani, A. R., Alanazi, I. M., Shahzad, N., Shahid, I., Falemban, A. H., Azlina, M. F. N., & Arulselvan, P. (2023) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2023.126581 · Cited by 35
Intestinal biofilms: pathophysiological relevance, host defense, and therapeutic opportunities
Jandl, B., Dighe, S. N., Gasché, C., Makristathis, A., & Muttenthaler, M. (2024) · Clinical Microbiology Reviews · doi:10.1128/cmr.00133-23 · Cited by 36
“Within the B. fragilis group, enterotoxigenic B. fragilis is of particular clinical relevance, representing the most common carcinogenic bacteria and a pivotal pathogen implicated in the initiation and progression of colorectal cancers (177–179).”
Andrade, A. I. C., Rivera-Bautista, C., Ruiz‐Cabrera, M. A., Guerra, R. E. S., Chávez, E. G., Ahumada, C. F., & Grajales‐Lagunes, A. (2019) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2019.06.045 · Cited by 34
Chou, Y.-C., Ho, P.-Y., Chen, W.-J., Wu, S.-H., & Pan, M. (2020) · PubMed Central · Cited by 34
Wang, T., Zheng, J., Dong, S., Ismael, M., Shan, Y., Wang, X., & Lü, X. (2022) · Probiotics and Antimicrobial Proteins · doi:10.1007/s12602-022-09967-9 · Cited by 34
“As the typical beneficial metabolites of intestinal microbiota, SCFAs (especially butyric acid) played important roles in ameliorating CRC [30], including inhibiting inflammation and histone deacetylases [31, 32], maintaining colonic epithelial health [33], inhibiting microbial pathogens [34], and regulating cell grow…”
BackgroundThe gastrointestinal microbiota in colorectal cancer cell migration and invasion
Henstra, C., van Praagh, J., Olinga, P., & Nagelkerke, A. (2021) · Clinical & Experimental Metastasis · doi:10.1007/s10585-021-10130-x · Cited by 32
“coli, as a commensal, coexists peacefully with its mammalian host, promoting healthy intestinal homeostasis and causing disease only rarely [112].”
BackgroundImpact of bacterial infection and intestinal microbiome on colorectal cancer development
Sun, J. (2022) · Chinese Medical Journal · doi:10.1097/cm9.0000000000001979 · Cited by 35
“Factors that affect the risk of CRC also affect the intestinal microbiome, including obesity; physical activity; and dietary intake of fiber, whole grains, and red and processed meat.([89,95]) These factors, including Salmonella infection,([96]) alter microbiome structure and function, along with the metabolic and imm…”
BackgroundIchim, T. E., Kesari, S., & Shafer, K. (2018) · Oncotarget · doi:10.18632/oncotarget.25778 · Cited by 36
Saha, B., Rithi, A. T., Adhikary, S., Banerjee, A., Radhakrishnan, A., Duttaroy, A. K., & Pathak, S. (2024) · Nutrition and Cancer · doi:10.1080/01635581.2024.2367266 · Cited by 39
The clinical application of fruquintinib on colorectal cancer
Chen, Z., & Jiang, L. (2019) · Expert Review of Clinical Pharmacology · doi:10.1080/17512433.2019.1630272 · Cited by 32
An age stratified analysis of the biomarkers in patients with colorectal cancer
Yao, H. Q., Li, C., & Tan, X. (2021) · Scientific Reports · doi:10.1038/s41598-021-01850-x · Cited by 33
Li, C., Gao, Y., Huan, Y., Ren, P., Zhi, J., Wu, A., Xu, J., Wei, Z., Xue, C., & Tang, Q. (2022) · Food Research International · doi:10.1016/j.foodres.2022.111324 · Cited by 32
Shen, J., Li, P., Liu, S., Liu, Q., Li, Y., Zhang, Z., Yang, C., Hu, M., Sun, Y., He, C., et al. (2020) · Food & Function · doi:10.1039/d0fo01731k · Cited by 31
Immunomodulatory Effect of Lactobacillus casei in a Murine Model of Colon Carcinogenesis
Casas‐Solís, J., Huizar-López, M. D. R., Irecta-Nájera, C. A., Pita‐López, M. L., & Santerre, A. (2019) · Probiotics and Antimicrobial Proteins · doi:10.1007/s12602-019-09611-z · Cited by 31
Microbial factors in inflammatory diseases and cancers
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Metadata
- Authors
- Sun, J., & Kato, I.
- Affiliations
- University of Illinois Chicago (US)
- Wayne State University (US)
- Corresponding author
- Sun, Jun
- ORCID
- Venue
- Genes & Diseases
- Publisher
- Elsevier BV
- Published
- 2016-06
- Volume
- 3
- Issue
- 2
- Pages
- 130-143
- ISSN
- 2352-3042 (ISSN-L)
- PMC
- PMC5221561
- OpenAlex
- W2338446464
- Cited by
- 257
- References
- 170
- Citations by year
- 2026: 14 · 2025: 19 · 2024: 25 · 2023: 27 · 2022: 34 · 2021: 29 · 2020: 39 · 2019: 29 · 2018: 27 · 2017: 14
- FWCI
- 12.06
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Genes & Diseases (publishedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Funders
- National Institute of Diabetes and Digestive and Kidney Diseases (R01 DK105118)
- Cancer Center, University of Illinois at Chicago
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Dentistry › Periodontics › Oral microbiology and periodontitis research
- Health Sciences › Medicine › Infectious Diseases › Clostridium difficile and Clostridium perfringens research
- Keywords
- gut microbiota, colorectal cancer, inflammation, tumor progression, chronic infection, bacterial virulence factors, host-microbe interactions, intestinal barrier function, cancer prevention, cancer diagnosis
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