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Cancers
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Microbiota in Colorectal Cancer
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Microbiota in Colorectal Cancer

A special issue of Cancers (ISSN 2072-6694).

Deadline for manuscript submissions: closed (31 January 2021) | Viewed by 41883

Special Issue Editors

Prof. Dr. John Tsiaoussis

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Guest Editor
Associate Professor of Anatomy, Laboratory of Anatomy-Histology-Embryology, Medical School, University of Crete, Voutes Campus, GR-71003, Heraklion, Crete, Greece
Interests: cancer biology; colorectal cancer; microbiota; surgical anatomy; cancer immunology; cancer treatment
Prof. Dr. John Souglakos

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Guest Editor
Associate Professor of Medical Oncology, Laboratory of Translational Oncology, Medical School, University of Crete, Voutes Campus, GR-71110, Heraklion, Crete, Greece
Interests: cancer biology; gastrointestinal cancer; cancer treatment

Special Issue Information

Dear colleagues,

The role of the microbiota in health and disease is widely accepted, and there is growing evidence that the microbiota mediates various functions, such as regulating host metabolism, immune homeostasis, and the pathogenesis and progression of numerous malignancies. Colorectal cancer (CRC) constitutes one of the leading causes of mortality and morbidity related to cancer, being the third most commonly diagnosed tumor, which is strongly associated with environmental and genetic risk factors. It has been reported by human and animal studies that the microbiota, especially in the large intestine, is altered in patients with CRC. Interestingly, changes in the microbiota ecosystem, known as dysbiosis, are able to promote intestinal carcinogenesis and progression through various factors, either locally by forming biofilms, causing dysmetabolism, and impairing the intestinal epithelial barrier or systemically by aberrant immunity and secretion of several cytokines and other mediators. Recently, it was also reported that the microbiota affects the efficacy of chemotherapy and immunotherapy for CRC among other cancers. These facts combined suggest that the microbiota could serve as a possible biomarker for the diagnosis, prognosis, and treatment of CRC. In this Special Issue, we aim to further elucidate the role of the microbiota in CRC pathogenesis and how the microbiota could serve as a novel biomarker for CRC.

Prof. Dr. John Tsiaoussis
Prof. Dr. John Souglakos
Guest Editors

Manuscript Submission Information

Manuscripts should be submitted online at www.mdpi.com by registering and logging in to this website. Once you are registered, click here to go to the submission form. Manuscripts can be submitted until the deadline. All submissions that pass pre-check are peer-reviewed. Accepted papers will be published continuously in the journal (as soon as accepted) and will be listed together on the special issue website. Research articles, review articles as well as short communications are invited. For planned papers, a title and short abstract (about 100 words) can be sent to the Editorial Office for announcement on this website.

Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Cancers is an international peer-reviewed open access semimonthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2900 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

  • microbiota
  • colorectal cancer
  • cancer pathogenesis
  • tumor progression
  • chemotherapy
  • immunotherapy
  • dysbiosis
  • immunity
  • biomarker
  • inflammation

Published Papers (11 papers)

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Editorial

Jump to: Research, Review, Other

3 pages, 164 KiB  
Editorial
Microbiota: An Emerging Biomarker in Colorectal Cancer
by John Tsiaoussis and John Souglakos
Cancers 2021, 13(21), 5530; https://doi.org/10.3390/cancers13215530 - 04 Nov 2021
Cited by 1 | Viewed by 1160
Abstract
This series of 10 articles (four original articles, five literature reviews, and one systematic review) is presented by international experts in the study of microbiota and its relation to colorectal cancer (CRC) [...] Full article
(This article belongs to the Special Issue Microbiota in Colorectal Cancer)

Research

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13 pages, 9004 KiB  
Article
Oral and Intravenous Iron Therapy Differentially Alter the On- and Off-Tumor Microbiota in Anemic Colorectal Cancer Patients
by Oliver Phipps, Hafid O. Al-Hassi, Mohammed N. Quraishi, Edward A. Dickson, Jonathan Segal, Helen Steed, Aditi Kumar, Austin G. Acheson, Andrew D. Beggs and Matthew J. Brookes
Cancers 2021, 13(6), 1341; https://doi.org/10.3390/cancers13061341 - 16 Mar 2021
Cited by 12 | Viewed by 3296
Abstract
Iron deficiency anemia is a common complication of colorectal cancer and may require iron therapy. Oral iron can increase the iron available to gut bacteria and may alter the colonic microbiota. We performed an intervention study to compare oral and intravenous iron therapy [...] Read more.
Iron deficiency anemia is a common complication of colorectal cancer and may require iron therapy. Oral iron can increase the iron available to gut bacteria and may alter the colonic microbiota. We performed an intervention study to compare oral and intravenous iron therapy on the colonic tumor-associated (on-tumor) and paired non-tumor-associated adjacent (off-tumor) microbiota. Anemic patients with colorectal adenocarcinoma received either oral ferrous sulphate (n = 16) or intravenous ferric carboxymaltose (n = 24). On- and off-tumor biopsies were obtained post-surgery and microbial profiling was performed using 16S ribosomal RNA analysis. Off-tumor α- and β-diversity were significantly different between iron treatment groups. No differences in on-tumor diversity were observed. Off-tumor microbiota of oral iron-treated patients showed higher abundances of the orders Clostridiales, Cytophagales, and Anaeroplasmatales compared to intravenous iron-treated patients. The on-tumor microbiota was enriched with the orders Lactobacillales and Alteromonadales in the oral and intravenous iron groups, respectively. The on- and off-tumor microbiota associated with intravenous iron-treated patients infers increased abundances of enzymes involved in iron sequestration and anti-inflammatory/oncogenic metabolite production, compared to oral iron-treated patients. Collectively, this suggests that intravenous iron may be a more appropriate therapy to limit adverse microbial outcomes compared to oral iron. Full article
(This article belongs to the Special Issue Microbiota in Colorectal Cancer)
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21 pages, 2596 KiB  
Article
Dysbiosis Triggers ACF Development in Genetically Predisposed Subjects
by Stefania De Santis, Marina Liso, Mirco Vacca, Giulio Verna, Elisabetta Cavalcanti, Sergio Coletta, Francesco Maria Calabrese, Rajaraman Eri, Antonio Lippolis, Raffaele Armentano, Mauro Mastronardi, Maria De Angelis and Marcello Chieppa
Cancers 2021, 13(2), 283; https://doi.org/10.3390/cancers13020283 - 14 Jan 2021
Cited by 8 | Viewed by 2473
Abstract
Background: Colorectal cancer (CRC) is the third most common cancer worldwide, characterized by a multifactorial etiology including genetics, lifestyle, and environmental factors including microbiota composition. To address the role of microbial modulation in CRC, we used our recently established mouse model (the Winnie-APC [...] Read more.
Background: Colorectal cancer (CRC) is the third most common cancer worldwide, characterized by a multifactorial etiology including genetics, lifestyle, and environmental factors including microbiota composition. To address the role of microbial modulation in CRC, we used our recently established mouse model (the Winnie-APCMin/+) combining inflammation and genetics. Methods: Gut microbiota profiling was performed on 8-week-old Winnie-APCMin/+ mice and their littermates by 16S rDNA gene amplicon sequencing. Moreover, to study the impact of dysbiosis induced by the mother’s genetics in ACF development, the large intestines of APCMin/+ mice born from wild type mice were investigated by histological analysis at 8 weeks. Results: ACF development in 8-week-old Winnie-APCMin/+ mice was triggered by dysbiosis. Specifically, the onset of ACF in genetically predisposed mice may result from dysbiotic signatures in the gastrointestinal tract of the breeders. Additionally, fecal transplant from Winnie donors to APCMin/+ hosts leads to an increased rate of ACF development. Conclusions: The characterization of microbiota profiling supporting CRC development in genetically predisposed mice could help to design therapeutic strategies to prevent dysbiosis. The application of these strategies in mothers during pregnancy and lactation could also reduce the CRC risk in the offspring. Full article
(This article belongs to the Special Issue Microbiota in Colorectal Cancer)
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15 pages, 2813 KiB  
Article
Microbiome Analysis from Paired Mucosal and Fecal Samples of a Colorectal Cancer Biobank
by Ulrich Wirth, Debora Garzetti, Lara M. Jochum, Stefanie Spriewald, Florian Kühn, Matthias Ilmer, Serene M. L. Lee, Hanno Niess, Alexandr V. Bazhin, Joachim Andrassy, Jens Werner, Barbara Stecher and Tobias S. Schiergens
Cancers 2020, 12(12), 3702; https://doi.org/10.3390/cancers12123702 - 09 Dec 2020
Cited by 14 | Viewed by 3045
Abstract
The role of gut microbiota in colorectal cancer is subject to extensive research. Before usage of biorepositories for microbiome studies, it is crucial to evaluate technical feasibility of microbiome profiling from various biospecimens. The aim of this study was to assess the feasibility [...] Read more.
The role of gut microbiota in colorectal cancer is subject to extensive research. Before usage of biorepositories for microbiome studies, it is crucial to evaluate technical feasibility of microbiome profiling from various biospecimens. The aim of this study was to assess the feasibility of DNA-extraction and microbiome profiling of samples from different sample sites, tissue sites and storage duration of a colorectal cancer biobank. Mucosa samples, mucosal scrapings and feces as well as different tissue sites (tumor, normal mucosa) were analyzed. 16S rRNA gene-based microbiome profiling with taxonomic assignment was performed on the Illumina MiSeq (Illumina, San Diego, USA) platform from stored snap frozen samples. For statistical analysis, α- and β-diversity measures, PCoA, permutational multivariate analysis of variance and graphical representation were performed. Microbiome analysis could be successfully performed in most of the samples (overall 93.3%) with sufficient numbers of high-quality reads. There were no differences between sample sites, while in some measures significant differences were found between tumor and normal mucosa (α-diversity, Shannon/Simpson Indices p = 0.028/0.027, respectively). Samples stored for up to eight years were used and storage conditions had no significant influence on the results. Tumor and tissue samples of a biobank stored long term can be successfully used for microbiome analysis. As large sample sizes are needed for association studies to evaluate microbial impact on tumorigenesis or progression of colorectal cancer, an already established biorepository may be a useful alternative to prospective clinical studies. Full article
(This article belongs to the Special Issue Microbiota in Colorectal Cancer)
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Graphical abstract

14 pages, 2384 KiB  
Article
The Prognostic Value of the Detection of Microbial Translocation in the Blood of Colorectal Cancer Patients
by Ippokratis Messaritakis, Konstantinos Vogiatzoglou, Konstantina Tsantaki, Agapi Ntretaki, Maria Sfakianaki, Asimina Koulouridi, John Tsiaoussis, Dimitrios Mavroudis and John Souglakos
Cancers 2020, 12(4), 1058; https://doi.org/10.3390/cancers12041058 - 24 Apr 2020
Cited by 19 | Viewed by 3220
Abstract
Dysbiosis has been associated with various diseases and is of major health importance. Dysbiosis leads to microbial translocation, which is the passage of microorganisms, their fragments, or their metabolites from the intestinal lumen into the blood circulation and other sites. The aim of [...] Read more.
Dysbiosis has been associated with various diseases and is of major health importance. Dysbiosis leads to microbial translocation, which is the passage of microorganisms, their fragments, or their metabolites from the intestinal lumen into the blood circulation and other sites. The aim of the study was to determine whether microbial translocation occurs in stage II/III-IV colorectal cancer (CRC) patients. The aim was also to evaluate the usefulness of blood PCR for diagnosis of such translocation and correlate the presence of toll-like receptor/vitamin D receptor (TLR/VDR) gene polymorphisms with microbial DNA fragments detected in the blood of CRC patients. Three hundred and ninety-seven CRC patients enrolled in the study. Peripheral blood DNA was analyzed using PCR for the amplification of genomic DNA encoding 16S rRNA, the β-galactosidase gene of Escherichia coli, glutamine synthase gene of Bacteroides fragilis, and 5.8S rRNA of Candida albicans. Significantly higher rates of all microbial fragments, but E. coli, detected were observed in the CRC patients (p < 0.001); such detection of all four microbial fragments was also significantly associated with the metastatic disease (p < 0.001), leading to shorter survival rates (p < 0.001). Tumor location in the right colon also significantly correlated with shorter survival (p = 0.016). Individuals with homozygous mutant alleles of TLR/VDR polymorphisms had significantly higher detection rates of microbial DNA fragments. The detection of microbial DNA fragments in CRC patients highlighted the role of these microbes in cancer development, progression, and patients’ survival. Full article
(This article belongs to the Special Issue Microbiota in Colorectal Cancer)
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Review

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25 pages, 2016 KiB  
Review
Stem Cell Impairment at the Host-Microbiota Interface in Colorectal Cancer
by Marinella Marzano, Bruno Fosso, Elisabetta Piancone, Giuseppe Defazio, Graziano Pesole and Mariangela De Robertis
Cancers 2021, 13(5), 996; https://doi.org/10.3390/cancers13050996 - 27 Feb 2021
Cited by 20 | Viewed by 4127
Abstract
Colorectal cancer (CRC) initiation is believed to result from the conversion of normal intestinal stem cells (ISCs) into cancer stem cells (CSCs), also known as tumor-initiating cells (TICs). Hence, CRC evolves through the multiple acquisition of well-established genetic and epigenetic alterations with an [...] Read more.
Colorectal cancer (CRC) initiation is believed to result from the conversion of normal intestinal stem cells (ISCs) into cancer stem cells (CSCs), also known as tumor-initiating cells (TICs). Hence, CRC evolves through the multiple acquisition of well-established genetic and epigenetic alterations with an adenoma-carcinoma sequence progression. Unlike other stem cells elsewhere in the body, ISCs cohabit with the intestinal microbiota, which consists of a diverse community of microorganisms, including bacteria, fungi, and viruses. The gut microbiota communicates closely with ISCs and mounting evidence suggests that there is significant crosstalk between host and microbiota at the ISC niche level. Metagenomic analyses have demonstrated that the host-microbiota mutually beneficial symbiosis existing under physiologic conditions is lost during a state of pathological microbial imbalance due to the alteration of microbiota composition (dysbiosis) and/or the genetic susceptibility of the host. The complex interaction between CRC and microbiota is at the forefront of the current CRC research, and there is growing attention on a possible role of the gut microbiome in the pathogenesis of CRC through ISC niche impairment. Here we primarily review the most recent findings on the molecular mechanism underlying the complex interplay between gut microbiota and ISCs, revealing a possible key role of microbiota in the aberrant reprogramming of CSCs in the initiation of CRC. We also discuss recent advances in OMICS approaches and single-cell analyses to explore the relationship between gut microbiota and ISC/CSC niche biology leading to a desirable implementation of the current precision medicine approaches. Full article
(This article belongs to the Special Issue Microbiota in Colorectal Cancer)
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17 pages, 1321 KiB  
Review
Interplay between the Gut Microbiota and Inflammatory Mediators in the Development of Colorectal Cancer
by Gwangbeom Heo, Yunna Lee and Eunok Im
Cancers 2021, 13(4), 734; https://doi.org/10.3390/cancers13040734 - 10 Feb 2021
Cited by 14 | Viewed by 3733
Abstract
Inflammatory mediators modulate inflammatory pathways during the development of colorectal cancer. Inflammatory mediators secreted by both immune and tumor cells can influence carcinogenesis, progression, and tumor metastasis. The gut microbiota, which colonize the entire intestinal tract, especially the colon, are closely linked to [...] Read more.
Inflammatory mediators modulate inflammatory pathways during the development of colorectal cancer. Inflammatory mediators secreted by both immune and tumor cells can influence carcinogenesis, progression, and tumor metastasis. The gut microbiota, which colonize the entire intestinal tract, especially the colon, are closely linked to colorectal cancer through an association with inflammatory mediators such as tumor necrosis factor, nuclear factor kappa B, interleukins, and interferons. This association may be a potential therapeutic target, since therapeutic interventions targeting the gut microbiota have been actively investigated in both the laboratory and in clinics and include fecal microbiota transplantation and probiotics. Full article
(This article belongs to the Special Issue Microbiota in Colorectal Cancer)
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18 pages, 1080 KiB  
Review
Microbe–Mucus Interface in the Pathogenesis of Colorectal Cancer
by Olivia I. Coleman and Dirk Haller
Cancers 2021, 13(4), 616; https://doi.org/10.3390/cancers13040616 - 04 Feb 2021
Cited by 22 | Viewed by 5691
Abstract
Overlying gastrointestinal epithelial cells is the transparent mucus layer that separates the lumen from the host. The dynamic mucus layer serves to lubricate the mucosal surface, to protect underlying epithelial cells, and as a transport medium between luminal contents and epithelial cells. Furthermore, [...] Read more.
Overlying gastrointestinal epithelial cells is the transparent mucus layer that separates the lumen from the host. The dynamic mucus layer serves to lubricate the mucosal surface, to protect underlying epithelial cells, and as a transport medium between luminal contents and epithelial cells. Furthermore, it provides a habitat for commensal bacteria and signals to the underlying immune system. Mucins are highly glycosylated proteins, and their glycocode is tissue-specific and closely linked to the resident microbiota. Aberrant mucin expression and glycosylation are linked to chronic inflammation and gastrointestinal cancers, including colorectal cancer (CRC). Aberrant mucus production compromises the mucus layer and allows bacteria to come into close contact with the intestinal epithelium, potentially triggering unfavorable host responses and the subsequent development of tumors. Here, we review our current understanding of the interaction between the intestinal microbiota and mucus in healthy and CRC subjects. Deep knowledge of the intricate mechanisms of microbe–mucus interactions may contribute to the development of novel treatment strategies for CRC, in which a dysfunctional mucus layer is observed. Full article
(This article belongs to the Special Issue Microbiota in Colorectal Cancer)
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Graphical abstract

23 pages, 1648 KiB  
Review
Intestinal Microbiota in Colorectal Cancer Surgery
by Ioannis Koliarakis, Elias Athanasakis, Markos Sgantzos, Theodoros Mariolis-Sapsakos, Evangelos Xynos, Emmanuel Chrysos, John Souglakos and John Tsiaoussis
Cancers 2020, 12(10), 3011; https://doi.org/10.3390/cancers12103011 - 16 Oct 2020
Cited by 32 | Viewed by 3941
Abstract
The intestinal microbiota consists of numerous microbial species that collectively interact with the host, playing a crucial role in health and disease. Colorectal cancer is well-known to be related to dysbiotic alterations in intestinal microbiota. It is evident that the microbiota is significantly [...] Read more.
The intestinal microbiota consists of numerous microbial species that collectively interact with the host, playing a crucial role in health and disease. Colorectal cancer is well-known to be related to dysbiotic alterations in intestinal microbiota. It is evident that the microbiota is significantly affected by colorectal surgery in combination with the various perioperative interventions, mainly mechanical bowel preparation and antibiotic prophylaxis. The altered postoperative composition of intestinal microbiota could lead to an enhanced virulence, proliferation of pathogens, and diminishment of beneficial microorganisms resulting in severe complications including anastomotic leakage and surgical site infections. Moreover, the intestinal microbiota could be utilized as a possible biomarker in predicting long-term outcomes after surgical CRC treatment. Understanding the underlying mechanisms of these interactions will further support the establishment of genomic mapping of intestinal microbiota in the management of patients undergoing CRC surgery. Full article
(This article belongs to the Special Issue Microbiota in Colorectal Cancer)
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23 pages, 1257 KiB  
Review
Targeting Gut Microbial Biofilms—A Key to Hinder Colon Carcinogenesis?
by Siang-Siang Chew, Loh Teng-Hern Tan, Jodi Woan-Fei Law, Priyia Pusparajah, Bey-Hing Goh, Nurul Syakima Ab Mutalib and Learn-Han Lee
Cancers 2020, 12(8), 2272; https://doi.org/10.3390/cancers12082272 - 13 Aug 2020
Cited by 29 | Viewed by 7038
Abstract
Colorectal cancer (CRC) is a global public health issue which poses a substantial humanistic and economic burden on patients, healthcare systems and society. In recent years, intestinal dysbiosis has been suggested to be involved in the pathogenesis of CRC, with specific pathogens exhibiting [...] Read more.
Colorectal cancer (CRC) is a global public health issue which poses a substantial humanistic and economic burden on patients, healthcare systems and society. In recent years, intestinal dysbiosis has been suggested to be involved in the pathogenesis of CRC, with specific pathogens exhibiting oncogenic potentials such as Fusobacterium nucleatum, Escherichia coli and enterotoxigenic Bacteroides fragilis having been found to contribute to CRC development. More recently, it has been shown that initiation of CRC development by these microorganisms requires the formation of biofilms. Gut microbial biofilm forms in the inner colonic mucus layer and is composed of polymicrobial communities. Biofilm results in the redistribution of colonic epithelial cell E-cadherin, increases permeability of the gut and causes a loss of function of the intestinal barrier, all of which enhance intestinal dysbiosis. This literature review aims to compile the various strategies that target these pathogenic biofilms and could potentially play a role in the prevention of CRC. We explore the potential use of natural products, silver nanoparticles, upconverting nanoparticles, thiosalicylate complexes, anti-rheumatic agent (Auranofin), probiotics and quorum-sensing inhibitors as strategies to hinder colon carcinogenesis via targeting colon-associated biofilms. Full article
(This article belongs to the Special Issue Microbiota in Colorectal Cancer)
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Other

14 pages, 601 KiB  
Systematic Review
Microbiota Alterations in Precancerous Colon Lesions: A Systematic Review
by Francesca Aprile, Giovanni Bruno, Rossella Palma, Maria Teresa Mascellino, Cristina Panetta, Giulia Scalese, Alessandra Oliva, Carola Severi and Stefano Pontone
Cancers 2021, 13(12), 3061; https://doi.org/10.3390/cancers13123061 - 19 Jun 2021
Cited by 18 | Viewed by 2614
Abstract
Gut microbiota plays an important role in human health. It may promote carcinogenesis and is related to several diseases of the gastrointestinal tract. This study of microbial dysbiosis in the etiology of colorectal adenoma aimed to investigate the possible causative role of microbiota [...] Read more.
Gut microbiota plays an important role in human health. It may promote carcinogenesis and is related to several diseases of the gastrointestinal tract. This study of microbial dysbiosis in the etiology of colorectal adenoma aimed to investigate the possible causative role of microbiota in the adenoma–carcinoma sequence and its possible preventive role. A systematic, PRISMA-guided review was performed. The PubMed database was searched using “adenoma microbiota” and selecting original articles between January 2010 and May 2020 independently screened. A higher prevalence of Proteobacteria, Fusobacteria, and Bacteroidetes phyla was observed in the fecal luminal and mucosa-associated microbiota of patients with adenoma. However, other studies provided evidence of depletion of Clostridium, Faecalibacterium, Bacteroides and Romboutsia. Results on the relationship between adenoma endoscopic resection and microbiota were inconsistent. In conclusion, none of the analyzed studies developed a predictive model that could differentiate adenoma from non-adenoma patients, and therefore, to prevent cancer progression. The impact of adenoma’s endoscopic resection on microbiota was investigated, but the results were inconclusive. Further research in the field is required. Full article
(This article belongs to the Special Issue Microbiota in Colorectal Cancer)
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