Cancer-Associated Microbiota: From Mechanisms of Disease Causation to Microbiota-Centric Anti-Cancer Approaches
Abstract
:Simple Summary
Abstract
1. Introduction
2. Epidemiology of Infection-Associated Cancers
3. Commensal Overgrowth in Cancer Patients
4. Disrupted Microbiota in Cancer
5. Association of Tissue-Resident Microbiota with Different Types of Cancer
5.1. Colorectal Cancer
5.2. Liver Cancer
5.3. Lung Cancer
5.4. Hematological Cancer
5.5. Pancreatic Cancer
5.6. Breast Cancer
5.7. Oral Cancer
5.8. Other Types of Cancers
6. The Classical Case of H. pylori Infection, Gut Microbiota, and Gastric Cancer
7. Microbiota Changes in Patients with Cancer-Causing Viral Infections
8. Cancer-Promoting Role of Microbiota
8.1. Microbiota Promotes Cancer by Modulation of Bile Acid Metabolism
8.2. Microbiota Promotes Cancer by Modulating Hormonal Effects
8.3. Cancer Promoting Roles of Bacterial Toxins
8.4. Microbiota Cause DNA Damage and Hinders DNA Repair
8.5. Microbiota Influence Chemotherapeutic Efficiency
8.6. Other Cancer-Promoting Roles of Microbiota
9. The Microbiota, Immunity, Cancer Axis
10. Pathoadaptive Mutations and Improved Colonization Efficiency of Microbiota
11. Microbiota-Centric Strategies against Cancer
11.1. Dietary Strategies
11.2. Prebiotics
11.3. Probiotics
11.4. Synbiotics
11.5. Antibiotics
11.6. Fecal Microbiota Transplantation
12. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
Abbreviations
References
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Infection | Study Population | Study Characteristics | Observed Microbial Changes | Reference |
---|---|---|---|---|
Pulmonary Tuberculosis | 31 healthy controls vs. 46 patients from China | Patients with active Mycobacterium tuberculosis infection; gut microbial signatures using shotgun sequencing | Depletion of SCFA producing microbes (Roseburia inulinivorans, R. hominis, R. intestinalis, Eubacterium rectale, and Coprococcus comes, Bifidobacterium adolescentis and B. longum, Ruminococcus obeum, and Akkermansia muciniphila); lower microbial metabolic functions related to SCFA production; decrease in alpha diversity. | [128] |
Hepatitis B virus (HBV) | 30 Asymptomatic HBV carriers, 31 chronic hepatitis B, 31 decompensated HBV cirrhosis, and 32 health controls from China | 16S rRNA sequencing of fecal microbiota and qPCR-based analysis of bacterial virulence genes | Depletion of Lactobacillus, Pediococcus, Leuconostoc, and Weissella in symptomatic patients; variation in F. prausnitzii, E. faecalis, and Enterobacteriaceae in asymptomatic carriers; lower Bifidobacteria-to-Enterobacteriaceae ratio in subjects with infections; lower abundance of Clostridium clusters XI and XIVab in decompensated HBV cirrhotic patients. | [129] |
Urinary tract infection | 168 kidney transplant patients, with 30% developing Enterobacteriaceae bacteremia within 6-mo of transplantation from USA | 16S rRNA sequencing; fecal samples | Increased abundance of Faecalibacterium and Romboutsia, and lower Lactobacillus; decreased microbial diversity. | [130] |
Human immunodeficiency virus (HIV) | 31 HIV patients (18 with antiretroviral treatment) vs. 27 healthy controls from France | 16S rRNA sequencing; fecal samples | Lower microbial diversity in HIV patients; Lower Clostridia, Subdoligranulum, Ruminococcus, Blautia, Faecalibacterium, Bifidobacterium, and increased gamma-proteobacteria, Enterococcus in HIV patients; systemic inflammatory markers were inversely correlated with R. bromii and F. prausnitzii, whereas associated with E. coli, Enterobacter aerogenes, E. faecalis and E. faecium. | [131] |
Human papillomavirus (HPV) | 345 women having infection with 27 different HPV types Sweden | 16S rRNA sequencing; vaginal fluid samples | Prevalence of Lactobacillus crispatus and L. iners; infected subjects had higher microbial diversity; abundance of Sneathia, Prevotella, and Megasphaera were associated with HPV infection. | [132] |
Hepatitis C virus (HCV) | 166 HCV infected patients vs. 23 healthy subjects from Japan | 16S rRNA sequencing from fecal samples | Less abundance of Lachnospiraceae and Ruminococcaceae in the patients; a decrease of Streptococcus salivarius and increase of Lactobacillus spp. with disease progression. | [62] |
Chlamydia trachomatis | 42 infected and 35 non-infected subjects from Malaysia | 16S rRNA sequencing; endocervical swab samples | Lower abundance of Tenericutes and Proteobacteria, and increased abundance of Delftia, Streptococcus, Pseudomonas, Cloacibacterium, Prevotella, Veillonella, Megasphaera, Ureaplasma, and Ralstonia in infected subjects | [133] |
Opisthorchis viverrini | 30 infected and 26 non-infected subjects from Russia; all 54 were diagnosed with cholelithiasis | 16S rRNA sequencing of samples from gall bladder | Increased abundance of Spirochaetes, Planctomycetes, Synergistetes, Verrucomicrobia, and Saccharibacteria (TM7) in infected patients; detection of Veillonella dispar, Paracoccus aminovorans, Parabacteroides distasonis, Sphingomonas changbaiensis, Cellulosimicrobium sp., Phycicoccus spp. only in infected patients, whereas Flectobacillus sp., Xanthobacter sp., Burkholderia sp., Streptomyces sp., Jeotgalicoccus psychrophilus, and Treponema socranskii present only in un-infected subjects. | [134] |
Urogenital schistosomiasis | 116 pre-school children with infection from UK | 16S rRNA sequencing from fecal samples | The most abundant genera were Prevotella, Bacteroides, Alistipes, Eubacterium, Faecalibacterium, Clostridium, Roseburia; Pseudomonas, Azospirillum, Stenotrophomonas, Derxia, and Thalassospira were associated with infection. | [135] |
Kaposi’s sarcoma (KS)-associated herpesvirus | 29 subjects from USA with pathology-confirmed KS who were serologically positive for KS-associated herpesvirusand HIV infection | 16S rRNA gene sequencing of samples from an oral swab | Lower microbial diversity and observed species and distinctly altered microbial taxonomic signatures in subjects with oral KS without any oral cell-associated HIV infection; the abundance of Aggregibacter and Lautropia were higher, but Corynebacterium and Shuttleworthia were lower in subjects with no oral KS. | [136] |
Study Characteristic | Observations | References |
---|---|---|
Dietary fiber intake was assessed in patients diagnosed with advanced colorectal adenoma to colorectal cancer (n = 344) and healthy controls (n = 47) from China. | Patients had reduced dietary fiber-intake patterns and consistently decreased SCFA production, less prevalence of Clostridium, Roseburia, and Eubacterium spp, and low abundance of Enterococcus and Streptococcus spp.; Fecal butyrate levels and butyrate-producing bacteria were high in a subset of cancer patients with comparatively higher fiber intake. | [244] |
A meta-analysis of 24 studies to define how effective dietary fiber consumption is at lowering the risk of breast cancer | Dietary fiber consumption was found to reduce the incidence of breast cancer by 12%; Based on the type of studies and menopausal status, the link between dietary fiber consumption and breast cancer risk was substantial. A dose-response study revealed that every 10 g/d increase in dietary fiber consumption was linked to a 4% reduction in the incidence of breast cancer. | [245] |
Dietary questionary-based examination of 519,978 people (25–70 y age) to link dietary fiber intake with colorectal cancer incidence in Europe. | The amount of dietary fiber in meals was inversely associated with the occurrence of large bowel cancer; However, there was no evidence that one kind of fiber was significantly more protective than another. | [246] |
The association of dietary fiber intake with colon and rectal cancer was assessed in 1168 cancer patients out of a cohort of 108,081 persons from the Scandinavian population | There was an inverse relationship between total fiber intake and the risk of colon cancer with each additional increase of 10 g/d and 2 g/d fiber consumption for males and females, respectively. | [247] |
Investigation of the links between whole grain and dietary fiber consumption and the risk of liver cancer and death from chronic liver disease in 485,717 subjects from the USA. | Higher grain intake was linked to a decreased incidence of liver cancer and death from chronic liver disease; Dietary fiber was also linked to a reduced incidence of liver cancer. | [248] |
Dietary questionary-based analysis of the association of fiber intake with renal cancer risk in 491,841 subjects in the USA. | Total dietary fiber consumption was linked to a 16–20% decreased incidence of kidney carcinoma; The negative relationship between fiber consumption and renal cancer was seen in people who had never smoked, had a low BMI and had no history of diabetes or hypertension. | [249] |
A meta-analysis of 24 studies (580,064 subjects) was performed to study the effects of dietary fiber consumption on the risk of gastric cancer. | Dietary fiber consumption is linked to a lower risk of gastric cancer, and this impact is likely independent of other risk variables; A dose-response study found that increasing fiber consumption by 10 g per day reduced the incidence of stomach cancer by 44%. | [250] |
Dietary fiber intake was evaluated in a US-based cohort study, including 463 head and neck cancer patients. | Increasing dietary fiber consumption before starting treatment can help patients longer; No statistically significant links between whole grains and prognostic outcomes were identified. | [251] |
A dose-response meta-analysis of dietary fiber intake in 13 studies (142,189 participants) consisting of 5777 ovarian cancer patients | Dietary fiber intake and the risk of ovarian cancer have a substantial inverse dose-response relationship. | [252] |
Study Characteristic | Observations | References |
---|---|---|
Milk fermented by Lactobacillus casei CRL 431 supplementation for 80-d. Female BALB/c mice of 6-wk age were challenged with 4T1 breast cancer cells. | Attenuated tumor growth, vasculature, extravasation, and metastasis; lower macrophage infiltration within the tumor microenvironment and lungs; increased CD8+ T-cell mediated tumor cytotoxicity; improved CD4+ T-cell populations. | [269] |
Lactobacillus plantarum YYC-3 isolated from fermented rose. C57BL/6-APCMin/+ mice with colon cancer supplemented with a high-fat diet were treated with either 109 CFU of L. plantarum YYC-3 or cell-free bacterial supernatant. | Reduced mucosal injury and tumor incidents; lowered the populations of inflammatory lymphocytes and the levels of IL-6, IL-17, IL-22; attenuated NFκB activation and Wnt signaling pathway; restored altered microbiota composition with increased abundance of gut commensals. | [270] |
Lactobacillus reuteri GMNL-89 and Lactobacillus paracasei GMNL-133 in 1:1 ratio administered 5-d per wk for 4 wk. Mice models of pancreatic cancer (LSL-K-rasG12D; Pdx-1-cre) were orally treated with 109 viable P. gingivalis | Decrease body weight; tissue expression of Snail-1, ZEB-1, collagen fibers, Galectin-3, and PD-L1 were attenuated; attenuated expression of total Smad3 and phosphorylated Smad3; Reduced cancer cell proliferation, viability, pancreatic intraepithelial neoplasia, and metastasis likely by affecting transforming growth factor-β signaling pathway. | [271] |
Supplementation of 108 CFU/d of Lactobacillus rhamnosus R0011 to NMRI inbreed mice for 2-wk, followed by grafting of human gastric cancer tissue, then 4-wk treatment of L. rhamnosus. | Resulted in tumor regression; an increase in WBC populations, Bax/BCL2 ratio; inflammatory reaction around tumor tissue, cell necrosis, and apoptosis are increased. | [272] |
Female BALB/C mice were pre-treated for 14-d with 108 CFU Lactobacillus acidophilus NCFM followed by inoculation of CT-26 colon carcinoma cells. | Suppression of tumor growth; reduction of micro-tumor size and initiation of apoptosis in tumor cells; Bcl2 expression was lower whereas caspase-9 and caspase-3 expressions were higher; CXCR4 and MHC class I expression colon and mesenteric lymph nodes. | [273] |
Lactobacillus casei KK378 at 104–108 CFU was injected into tumor site in male BALB/cSlc-nu/nu mice inoculated with head and neck squamous cell carcinoma cell (SAS, HSC2, and HSQ89) | Regression of tumor size; increase levels of TNF-α, IFN-γ, IL-5, IL-10, and IL-12. | [274] |
Lactobacillus salivarius REN was supplemented at 105–1010 CFU per day for 32 wk or 23 wk to Male F344 rats treated for 8-wk with 4-nitroquioline 1-oxide to induce oral cancer. | Reduced incidence of tongue tumors and preneoplastic lesions; decreased level of 8-hydroxydeoxyguanosine (a marker of oxidative stress) in the tongue mucosa; lower expression of COX-2 and proliferating cell nuclear antigen; Degradation of carcinogen. | [275] |
C57BL/6 mice were orally supplemented with 2 × 108 CFU of Lactobacillus rhamnosus GG for 2-wk | Lowered colonic tumor counts; Increased expression of IL-2, IFN-γ, CXCL9, CXCL10; increased population of CD8+ CD3+ T-cell, granzyme B+ CD8 T-cells, dendritic cells. | [276] |
Lactobacillus acidophilus cell lysate + anti-CTL antigen-4 blocking antibody treatment for 34-d | Prevents loss of body weight and development of colorectal cancer; tumor microenvironment had higher CD8+ T cells, CD44+ CD8+ CD62L+ effector T-cells, and lower CD4+ CD25+ Foxp3+ T-reg and F4/80+ CD206+ M2 macrophages; reduced macrophage M2 polarization and IL-10 expression in LPS-treated macrophage; reduce the fecal abundance of proteobacteria. | [277] |
Supplementation of Bifidobacterium lactis at 1011 CFU/g with or without resistant starch (100 g/kg diet) for 22-wk to Sparge-Dawley rats treated with azoxymethane for induction of colon cancer. | Reduction of frequency and development of colonic neoplasm; increased SCFA production; increased crypt column length, and decreased PCNA+ cells. | [278] |
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Dey, P.; Ray Chaudhuri, S. Cancer-Associated Microbiota: From Mechanisms of Disease Causation to Microbiota-Centric Anti-Cancer Approaches. Biology 2022, 11, 757. https://doi.org/10.3390/biology11050757
Dey P, Ray Chaudhuri S. Cancer-Associated Microbiota: From Mechanisms of Disease Causation to Microbiota-Centric Anti-Cancer Approaches. Biology. 2022; 11(5):757. https://doi.org/10.3390/biology11050757
Chicago/Turabian StyleDey, Priyankar, and Saumya Ray Chaudhuri. 2022. "Cancer-Associated Microbiota: From Mechanisms of Disease Causation to Microbiota-Centric Anti-Cancer Approaches" Biology 11, no. 5: 757. https://doi.org/10.3390/biology11050757
APA StyleDey, P., & Ray Chaudhuri, S. (2022). Cancer-Associated Microbiota: From Mechanisms of Disease Causation to Microbiota-Centric Anti-Cancer Approaches. Biology, 11(5), 757. https://doi.org/10.3390/biology11050757