Microbiome—Stealth Regulator of Breast Homeostasis and Cancer Metastasis
Abstract
:Simple Summary
Abstract
1. Introduction
2. Breast Tissue Microbiota
3. Breast Milk Microbiota
4. Breast Tumor Microbiota
4.1. Breast Cancer Subtype-Specific Microbiota
4.2. Race-/Ethnicity-Specific Breast Cancer Microbiota
5. Origin of Breast Tissue Microbiota
5.1. Microbial Transfer from Breast Skin
5.2. Microbial Transfer from the Nipple
5.3. Microbial Transfer via the Gut–Breast Axis or the Oro–Breast Axis
6. Mechanisms of Bacterial Translocation
6.1. Internalization into Epithelial Cells
6.2. Sampling and Transportation by Immune Cells
7. Functions of Intracellular Microbiota
8. Bacterially Produced Metabolites
9. Breast-Tumor-Associated Bacteria
9.1. Origin of Breast-Tumor-Resident Bacteria
9.2. Major Breast-Tumor-Resident Bacterial Species
9.2.1. Fusobacterium nucleatum
9.2.2. Streptococcus
9.2.3. Staphylococcus and Enterobacteriaceae
9.3. Roles of Intracellular Microbes in Breast Tumor Initiation/Development
9.3.1. Genome Instability/Mutation
9.3.2. Tumor Metastasis
10. Discussion
11. Conclusions
Funding
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Normal Breast | Breast Cancer | ||||||
---|---|---|---|---|---|---|---|
Microbes | Levels | Functions | Ref. | Microbes | Levels | Functions | Ref. |
Sphingomonas | Higher | Degrades environmental carcinogens, aromatic hydrocarbons, and polycyclic aromatic hydrocarbons; protective against ER+ breast cancer | [24,28] | Fusobacterium nucleatum | Higher | Promotes breast cancer cell attachment, invasion, and colonization during metastasis; impairs immunity and therapy response; activates β-catenin-mediated oncogene transcription and cell proliferation; produces β-lactamase for resistance to β-lactam antibiotics (e.g., penicillin) | [24,29,30,31] |
Firmicutes, Actinobacteria | Higher | Negatively correlate with stromal fibrosis and breast cancer risk; enriched in breast milk | [32,33,34] | ||||
Lactobacillaceae, Acetobacterraceae, Leuconostocaceae Xanthomonadaceae | Higher | Induce fructose and mannose metabolism and immune-related genes; enriched in breast milk of healthy women | [35,36,37] | Enterobacteriaceae, Staphylococcus | Higher | Induce DNA double-strand breaks in host cells | [38,39] |
Ralstonia | Higher | Dysregulates genes involved in carbohydrate metabolism | [35] | ||||
Cyanobacteria | Higher | Produce anti-cancer molecules (e.g., Cryptophycin F) | [40] | Atopobium, Gluconacetobacter | Higher | Modulate immunological responses | [24,41,42] |
Proteobacteria, Synergistetes, Tenericutes | Higher | Regulate milk composition and production | [43,44] | Porphyromonadaceae, Ruminococcaceae | Higher | Participate in aberrant host metabolism | [40,45,46] |
Prevotellaceae, Butyricimonas | Higher | Produce short-chain fatty acids (SCFAs) (propionate and butyrate) that exert anti-tumor activities | [40,47,48,49] | Sutterella, Verrucomicrobiaceae | Higher | Also found in cecal microbiota | [40,50,51] |
Acinetobacter | Higher | Abundant in HR+ and HER2+ breast cancer | [40,52] | ||||
Flavobacterium, Hydrogenophaga | Higher | Abundant in metastatic breast cancer | [40,53,54] | ||||
Alcaligenaceae, Moraxellaceae, Parabacteroides | Higher | Enriched in breast milk | [40,55] | Akkermansia (phylum Verrucomicrobia), Thermia | Higher | Abundant in TNBC | [40,56] |
Cancer Types | Microbes | Levels | Pro-Tumor Mechanisms | Ref. |
---|---|---|---|---|
Breast | Fusobacterium nucleatum | Increased | Suppresses T cell infiltration into tumors; promotes tumor growth and metastatic progression | [29] |
Anaerococcus, Caulobacter Propionibacterium, Streptococcus, Staphylococcus | Decreased | Positively correlated with oncogenic immune features and T-cell activation-related genes | [9] | |
Bile duct | Bifidobacteriaceae, Enterobacteriaceae, Enterococcaceae | Increased | Increased production of bile acids and ammonia, leading to DNA damage in host cells and carcinogenesis | [88] |
Cervical | Fusobacterium spp. | Increased | Associated with increased IL-4 and TGF-β1 mRNA in cervical cells | [89] |
Anaerotruncus, Anaerostipes, Atopobium, Arthrospira, Bacteroides, Dialister, Peptoniphilus, Porphyromonas, Ruminococcus, Treponema | Increased | Elevates vaginal pH to weaken host defense against infection and promotes tumor formation | [90] | |
Colorectal | Bacteroides fragilis | Increased | Increased interleukin-17 in the colon and DNA damage in the colonic epithelium, accelerating tumor onset and elevating host mortality | [91] |
Fusobacterium | Increased | Cancer cell proliferation and distant metastasis | [80] | |
Esophageal | Lactobacillus fermentum | Increased | Establishes acidic environment for growth advantage | [92] |
Helicobacter pylori | Increased | Spread from gastric colonization | [92] | |
Campylobacter spp. | Increased | Causes inflammation that could contribute to carcinogenesis | [93] | |
Porphyromonas gingivalis | Increased | Accelerates cell cycle and promotes cellular migration and metabolism of potentially carcinogenic substances such as ethanol to the carcinogenic derivative acetaldehyde | [94] | |
Extrahepatic Bile duct | Helicobacter pylori | Increased | Increases abundance of the virulence genes cagA and vacA and promotes tumor formation | [89] |
Helicobacter bilis | Increased | Induces inflammation to contribute to tumor formation | [95] | |
Gallbladder | Fusobacterium nucleatum, Escherichia coli, Enterobacter spp. | Increased | Promotes gallstone development and chronic cholecystitis to contribute to tumor formation | [96] |
Gastric | Helicobacter pylori | Increased | CagA protein suppresses p53-mediated apoptosis of host cells while increasing cell motility and metastatic phenotypes | [97] |
Fusobacterium nucleatum | Increased | Induces epithelial-to-mesenchymal transition | [98] | |
Liver cancer | Helicobacter bifidus | Increased | Contributes to formation of chronic hepatitis that promotes tumor progression | [99] |
Lung | Acidovorax spp. | Increased | Associated with carcinomas with p53 mutations | [100] |
Thermus, Legionella | Increased | Associated with advanced-stage and metastatic cancer | [101] | |
Oral cancer | Fusobacterium nucleatum | Increased | Induces epithelial-to-mesenchymal transition | [98] |
Firmicutes (esp. Streptococcus), Actinobacteria (esp. Rothia) | Increased | Elevated in normal oral tissues | [102] | |
Ovarian | Mycoplasma | Increased | Prevalent in 60% of tumors | [103] |
Pancreatic | Enterobacteriaceae, Pseudomonas spp., Mycobacterium avium, Pseudoxanthomonas, Streptomyces, Bacillus cereus | Increased | Contributes to chemotherapy resistance and immune suppression | [104,105] |
Malassezia globosa | Increased | Induces the complement cascade through the activation of mannose-binding lectin C3 to promote tumorigenesis | [106] | |
Prostate | Pseudomonas, Escherichia, Immunobacterium, Propionibacterium spp. | Increased | Induces prostatitis and differentiation of prostate basal cells into ductal cells to promote tumor formation | [107] |
Propionibacterium acnes spp. | Increased | Induces prostatitis and promotes tumor formation | [108] | |
Staphylococcus | Increased | Induces inflammation of the prostate tissue and promotes tumor formation | [107] | |
Fusobacterium nucleatum, Streptococcus oligosporus | Increased | Induces chemoresistance by regulating autophagy | [109] |
Breast Cancer Subtypes | Microbes | Levels | Ref. |
---|---|---|---|
Luminal A | Proteobacteria (Xanthomonadale) | Increased | [83] |
Tenericutes, Proteobacteria, Planctomycetes | Increased | [110] | |
Luminal B | Firmicutes (Clostridium) | Increased | [83] |
Tenericutes, Proteobacteria, Planctomycetes | Increased | [110] | |
HER2+ | Thermi, Verrucomicrobia (Akkermasia) | Increased | [83] |
Firmicutes (Granulicatella:US31), Bacteroidetes (Dyadobacter) | Increased | [26] | |
Firmicutes (Filibacter, Anaerostipes), Bacteroides (Cloacibacterium, Alloprevotella), Proteobacteria (PRD01a011B, Stakelama Blastomonas) | Increased | [9] | |
Proteobacteria (Burkholderiales, Helicobacter pylori) | Increased | [85] | |
TNBC | Streptococcaceae, Ruminococcus | Increased | [83] |
Actinomycetaceae, Caulobacteriaceae, Sphingobacteriaceae, Enterobacteriaceae, Prevotellaceae, Brucellaceae, Bacillaceae, Peptostreptococcaceae, Flavobacteriaceae | Increased | [86] | |
Prevotella, Brevundimonas, Actinomyces, Aerococcus, Arcobacter, Geobacillus, Orientia, Rothia, Streptococcaceae, Ruminococcus, Euryarchaeota | Increased | [83,86] | |
Bartonella, Coxiella, Mobiluncus, Mycobacterium, Rickettsia, Sphingomonas, Azomonas, Alkanindiges, Proteus, Brevibacillus, Kocuria, Parasediminibacterium | Increased | [68] |
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Furuta, S. Microbiome—Stealth Regulator of Breast Homeostasis and Cancer Metastasis. Cancers 2024, 16, 3040. https://doi.org/10.3390/cancers16173040
Furuta S. Microbiome—Stealth Regulator of Breast Homeostasis and Cancer Metastasis. Cancers. 2024; 16(17):3040. https://doi.org/10.3390/cancers16173040
Chicago/Turabian StyleFuruta, Saori. 2024. "Microbiome—Stealth Regulator of Breast Homeostasis and Cancer Metastasis" Cancers 16, no. 17: 3040. https://doi.org/10.3390/cancers16173040
APA StyleFuruta, S. (2024). Microbiome—Stealth Regulator of Breast Homeostasis and Cancer Metastasis. Cancers, 16(17), 3040. https://doi.org/10.3390/cancers16173040