Year 2015 / Volume 107 / Number 11
Original
Role of colonic microbiota in colorectal carcinogenesis: A systematic review

659-671

DOI: 10.17235/reed.2015.3830/2015

Marta Borges-Canha, José Pedro Portela-Cidade, Mário Dinis-Ribeiro, Adelino F. Leite-Moreira, Pedro Pimentel-Nunes,

Abstract
Background and aim: The human colonic mucosa is populated by a wide range of microorganisms, usually in a symbiotic relation with the host. Sometimes this balance is lost and a state of dysbiosis arises, exposing the colon to different metabolic and inflammatory stimuli (according to the microbiota’s changing profile). Recent findings lead to hypothesize that this unbalance may create a subclinical pro-inflammatory state that increases DNA mutations and, therefore, colorectal carcinogenesis. In this article we aim to systematically review the scientific evidence regarding colonic microbiota and its role in colorectal carcinogenesis. Methods: Systematic review of PubMed searching results for original articles studying microbiota and colorectal cancer until November 2014. Results: Thirty-one original articles studied the role of colon microbiota in colorectal carcinoma including both human and animal studies. Different and heterogeneous methods were used and different bacteria were considered. Nevertheless, some bacteria are consistently augmented (such as Fusobacteria, Alistipes, Porphyromonadaceae, Coriobacteridae, Staphylococcaceae, Akkermansia spp. and Methanobacteriales), while other are constantly diminished in colorectal cancer (such as Bifidobacterium, Lactobacillus, Ruminococcus, Faecalibacterium spp., Roseburia, and Treponema). Moreover, bacteria metabolites amino acids are increased and butyrate is decreased throughout colonic carcinogenesis. Conclusion: Conclusive evidence shows that colorectal carcinogenesis is associated with microbial dysbiosis. This information may be used to create new prophylactic, diagnostic and therapeutic strategies for colorectal cancer.
Share Button
New comment
Comments
No comments for this article
References
1. Candela M, Guidotti M, Fabbri A, et al. Human intestinal microbiota: cross-talk with the host and its potential role in colorectal cancer. Crit Rev Microbiol. 2011;37:1-14.
2. Gill SR, Pop M, Deboy RT, et al. Metagenomic analysis of the human distal gut microbiome. Science. 2006;312:1355-9.
3. Turnbaugh PJ, Ley RE, Hamady M, et al. The human microbiome project. Nature. 2007;449:804-10.
4. Shen XJ, Rawls JF, Randall T, et al. Molecular characterization of mucosal adherent bacteria and associations with colorectal adenomas. Gut Microbes. 2010;1:138-47.
5. Sobhani I, Tap J, Roudot-Thoraval F, et al. Microbial dysbiosis in colorectal cancer (CRC) patients. PLoS One. 2011;6:e16393.
6. Rustgi AK. The genetics of hereditary colon cancer. Genes & development. 2007;21:2525-38.
7. Watson AJ, Collins PD. Colon cancer: a civilization disorder. Dig Dis. 2011;29:222-8.
8. Riscuta G, Dumitrescu RG. Nutrigenomics: implications for breast and colon cancer prevention. Methods Mol Biol. 2012;863:343-58.
9. Le Chatelier E, Nielsen T, Qin J, et al. Richness of human gut microbiome correlates with metabolic markers. Nature. 2013;500:541-6.
10. Vogelstein B, Papadopoulos N, Velculescu VE, et al. Cancer genome landscapes. Science. 2013;339:1546-58.
11. Groden J, Thliveris A, Samowitz W, et al. Identification and characterization of the familial adenomatous polyposis coli gene. Cell. 1991;66:589-600.
12. Medema JP, Vermeulen L. Microenvironmental regulation of stem cells in intestinal homeostasis and cancer. Nature. 2011;474:318-26.
13. Cunningham D, Atkin W, Lenz HJ, et al. Colorectal cancer. Lancet. 2010;375:1030-47.
14. Poulogiannis G, Frayling IM, Arends MJ. DNA mismatch repair deficiency in sporadic colorectal cancer and Lynch syndrome. Histopathology. 2010;56:167-79.
15. Peltomaki P. Role of DNA mismatch repair defects in the pathogenesis of human cancer. J Clin Oncol. 2003;21:1174-9.
16. Pimentel-Nunes P, Goncalves N, Boal-Carvalho I, et al. Decreased Toll-interacting protein and peroxisome proliferator-activated receptor gamma are associated with increased expression of Toll-like receptors in colon carcinogenesis. Journal of clinical pathology. 2012;65:302-8.
17. Pimentel-Nunes P, Teixeira AL, Pereira C, et al. Functional polymorphisms of Toll-like receptors 2 and 4 alter the risk for colorectal carcinoma in Europeans. Digestive and liver disease : official journal of the Italian Society of Gastroenterology and the Italian Association for the Study of the Liver. 2013;45:63-9.
18. Uronis JM, Muhlbauer M, Herfarth HH, et al. Modulation of the intestinal microbiota alters colitis-associated colorectal cancer susceptibility. PLoS One. 2009;4:e6026.
19. Tyler AD, Smith MI, Silverberg MS. Analyzing the human microbiome: a "how to" guide for physicians. The American journal of gastroenterology. 2014;109:983-93.
20. Fierer N, Bradford MA, Jackson RB. Toward an ecological classification of soil bacteria. Ecology. 2007;88:1354-64.
21. Wang T, Cai G, Qiu Y, et al. Structural segregation of gut microbiota between colorectal cancer patients and healthy volunteers. The ISME Journal. 2012;6:320-9.
22. Wu N, Yang X, Zhang R, et al. Dysbiosis signature of fecal microbiota in colorectal cancer patients. Microb Ecol. 2013;66:462-70.
23. Zhu Q, Jin Z, Wu W, et al. Analysis of the intestinal lumen microbiota in an animal model of colorectal cancer. PLoS One. 2014;9:e90849.
24. Kostic AD, Chun E, Robertson L, et al. Fusobacterium nucleatum potentiates intestinal tumorigenesis and modulates the tumor-immune microenvironment. Cell Host Microbe. 2013;14:207-15.
25. McCoy AN, Araujo-Perez F, Azcarate-Peril A, et al. Fusobacterium is associated with colorectal adenomas. PLoS One. 2013;8:e53653.
26. Mira-Pascual L, Cabrera-Rubio R, Ocon S, et al. Microbial mucosal colonic shifts associated with the development of colorectal cancer reveal the presence of different bacterial and archaeal biomarkers. J Gastroenterol. 2014;10.1007/s00535-014-0963-x.
27. Marchesi JR, Dutilh BE, Hall N, et al. Towards the human colorectal cancer microbiome. PLoS One. 2011;6(5):e20447.
28. Zackular JP, Baxter NT, Iverson KD, et al. The gut microbiome modulates colon tumorigenesis. MBio. 2013;4:e00692-13.
29. Baxter NT, Zackular JP, Chen GY, et al. Structure of the gut microbiome following colonization with human feces determines colonic tumor burden. Microbiome. 2014;2:20.
30. Boleij A, Hechenbleikner EM, Goodwin AC, et al. The Bacteroides fragilis Toxin Gene Is Prevalent in the Colon Mucosa of Colorectal Cancer Patients. Clinical infectious diseases : an official publication of the Infectious Diseases Society of America. Clin Infect Dis. 2015;60:208-15.
31. Brim H, Yooseph S, Zoetendal EG, et al. Microbiome analysis of stool samples from African Americans with colon polyps. PLoS One. 2013;8:e81352.
32. Gueimonde M, Ouwehand A, Huhtinen H, et al. Qualitative and quantitative analyses of the bifidobacterial microbiota in the colonic mucosa of patients with colorectal cancer, diverticulitis and inflammatory bowel disease. World J Gastroenterol. 2007;13:3985-9.
33. Scanlan PD, Shanahan F, Clune Y, et al. Culture-independent analysis of the gut microbiota in colorectal cancer and polyposis. Environmental microbiology. 2008;10:789-98.
34. Bonnet M, Buc E, Sauvanet P, et al. Colonization of the human gut by E. coli and colorectal cancer risk. Clin Cancer Res. 2014;20:859-67.
35. Arthur JC, Gharaibeh RZ, Muhlbauer M, et al. Microbial genomic analysis reveals the essential role of inflammation in bacteria-induced colorectal cancer. Nat Commun. 2014 Sep 3;5:4724.
36. Weir TL, Manter DK, Sheflin AM, et al. Stool microbiome and metabolome differences between colorectal cancer patients and healthy adults. PLoS One. 2013;8:e70803.
37. Singh N, Gurav A, Sivaprakasam S, et al. Activation of Gpr109a, receptor for niacin and the commensal metabolite butyrate, suppresses colonic inflammation and carcinogenesis. Immunity. 2014;40:128-39.
38. Sato K, Tsuchihara K, Fujii S, et al. Autophagy is activated in colorectal cancer cells and contributes to the tolerance to nutrient deprivation. Cancer Res. 2007;67:9677-84.
39. Buc E, Dubois D, Sauvanet P, et al. High prevalence of mucosa-associated E. coli producing cyclomodulin and genotoxin in colon cancer. PLoS One. 2013;8:e56964.
40. Zackular JP, Rogers MA, Ruffin MTt, et al. The Human Gut Microbiome as a Screening Tool for Colorectal Cancer. Cancer Prev Res (Phila). Cancer Prev Res (Phila). 2014;10.1158/1940-6207.capr-14-0129.
41. Song X, Gao H, Lin Y, et al. Alterations in the microbiota drive interleukin-17C production from intestinal epithelial cells to promote tumorigenesis. Immunity. 2014;40:140-52.
42. Dennis KL, Wang Y, Blatner NR, et al. Adenomatous polyps are driven by microbe-instigated focal inflammation and are controlled by IL-10-producing T cells. Cancer Res. 2013;73:5905-13.
43. Klimesova K, Kverka M, Zakostelska Z, et al. Altered gut microbiota promotes colitis-associated cancer in IL-1 receptor-associated kinase M-deficient mice. Inflamm Bowel Dis. 2013;19:1266-77.
44. Szigeti R, Pangas SA, Nagy-Szakal D, et al. SMAD4 haploinsufficiency associates with augmented colonic inflammation in select humans and mice. Ann Clin Lab Sci. 2012;42:401-8.
45. Li Y, Kundu P, Seow SW, et al. Gut microbiota accelerate tumor growth via c-jun and STAT3 phosphorylation in APCMin/+ mice. Carcinogenesis. 2012;33:1231-8.
46. Hu B, Elinav E, Huber S, et al. Microbiota-induced activation of epithelial IL-6 signaling links inflammasome-driven inflammation with transmissible cancer. Proc Natl Acad Sci U S A. 2013;110:9862-7.
47. Irrazabal T, Belcheva A, Girardin SE, et al. The multifaceted role of the intestinal microbiota in colon cancer. Mol Cell. 2014;54:309-20.
48. Turner ND, Ritchie LE, Bresalier RS, et al. The microbiome and colorectal neoplasia: environmental modifiers of dysbiosis. Curr Gastroenterol Rep. 2013;15:346.
49. Sears CL, Garrett WS. Microbes, microbiota, and colon cancer. Cell Host Microbe. 2014;15:317-28.
50. Hagland HR, Soreide K. Cellular metabolism in colorectal carcinogenesis: Influence of lifestyle, gut microbiome and metabolic pathways. Cancer Lett. 2014 Mar 12;10.1016/j.canlet.2014.02.026.
Related articles

Digestive Diseases Image

Spontaneous regression of a rectal cancer

DOI: 10.17235/reed.2023.9486/2023

Letter

Vaginal lesion as first manifestation of colorectal disease

DOI: 10.17235/reed.2022.9270/2022

Review

Inflammatory bowel disease and solid organ transplantation

DOI: 10.17235/reed.2020.7361/2020

Review

New non-invasive biomarkers for colorectal cancer screening

DOI: 10.17235/reed.2020.7233/2020

Letter

Medullary colorectal carcinoma. Do we really know it?

DOI: 10.17235/reed.2020.6728/2019

Letter

The rectosigmoid junction: are limits important?

DOI: 10.17235/reed.2019.5983/2018

Editorial

Colorectal cancer screening and survival

DOI: 10.17235/reed.2018.5870/2018

Review

From the intestinal flora to the microbiome

DOI: 10.17235/reed.2017.4947/2017

Letter to the Editor

Liver metastasis from colorectal cancer 12 years after liver transplantation

DOI: 10.17235/reed.2017.4507/2016

Review

Serrated lesions and serrated polyposis syndrome

DOI: 10.17235/reed.2017.4065/2015

Letter to the Editor

Endobronchial metastases of colorectal cancer

DOI: 10.17235/reed.2016.4080/2015

Citation tools
Borges-Canha M, Portela-Cidade J, Dinis-Ribeiro M, Leite-Moreira A, Pimentel-Nunes P. Role of colonic microbiota in colorectal carcinogenesis: A systematic review. 3830/2015


Download to a citation manager

Download the citation for this article by clicking on one of the following citation managers:

Metrics
This article has received 2604 visits.
This article has been downloaded 254 times.

Statistics from Dimensions


Statistics from Plum Analytics

Publication history

Received: 29/04/2015

Accepted: 29/07/2015

Online First: 08/09/2015

Published: 30/10/2015

Article revision time: 72 days

Article Online First time: 132 days

Article editing time: 184 days


Share
This article hasn't been rated yet.
Reader rating:
Valora este artículo:




Asociación Española de Ecografía Digestiva Sociedad Española de Endoscopia Digestiva Sociedad Española de Patología Digestiva
The Spanish Journal of Gastroenterology is the official organ of the Sociedad Española de Patología Digestiva, the Sociedad Española de Endoscopia Digestiva and the Asociación Española de Ecografía Digestiva
Cookie policy Privacy Policy Legal Notice © Copyright 2023 y Creative Commons. The Spanish Journal of Gastroenterology