MicroRNA-31 induced by Fusobacterium nucleatum infection promotes colorectal cancer tumorigenesis

Tang, Bin; Lu, Xiaoxue; Tong, Yanan; Feng, Yuyang; Mao, Yilan; Dun, Guodong; Li, Jing; Xu, Qiao-Lin; Tang, Jie; Zhang, Tao; Deng, Lei; Xiao, He; Lan, Yuanzhi; Luo, Hua-xing; Zeng, Linghai; Xiang, Yuanyuan; Li, Qian; Zeng, Da‐Wu; Mao, Xuhu

doi:10.1016/j.isci.2023.106770

Cited by 6 publications

(5 citation statements)

References 66 publications

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“…Similarly, Ito et al (2015) also showed that there was no significant correlation between miR-31 expression and F. nucleatum status. However, Tang et al (2023) demonstrated that the upregulation of miR-31 was significantly correlated with the presence of F. nucleatum in CRC tissues and resulted in the promotion of tumorigenesis. Furthermore, they reported that miR-31-mediated inhibition of autophagic flux via suppression of syntaxin-12 (STX12) was linked to enhanced intracellular survival of F. nucleatum infection (Tang et al, 2023).…”

Section: Discussionmentioning

confidence: 98%

“…However, Tang et al (2023) demonstrated that the upregulation of miR-31 was significantly correlated with the presence of F. nucleatum in CRC tissues and resulted in the promotion of tumorigenesis. Furthermore, they reported that miR-31-mediated inhibition of autophagic flux via suppression of syntaxin-12 (STX12) was linked to enhanced intracellular survival of F. nucleatum infection (Tang et al, 2023). The investigation of the relationship between F. nucleatum and miRNAs expression has been very limited.…”

Section: Discussionmentioning

confidence: 98%

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Exploring the interplay between Fusobacterium nucleatum with the expression of microRNA, and inflammatory mediators in colorectal cancer

Bostanghadiri,

Razavi,

Shariati

et al. 2023

Front. Microbiol.

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BackgroundFusobacterium nucleatum has been recognized as an important key bacterium in the cause and spread of colorectal carcinogenesis. Nevertheless, the clinical relevance of F. nucleatum in colorectal cancer (CRC) and its effect on immune factors and the tumor microenvironment have not been fully elucidated.Materials and methodsThe frequency of F. nucleatum was measured in 100 paired tumor and normal tissue specimens by TaqMan quantification Real-Time Polymerase Chain Reaction (qPCR). The mRNA expression levels of cytokines (IL-6, IL-10, IL-12β, IL-17, TNF-α, TLR-2, and TLR-4), and miRNAs (miR-21, miR-31) were examined. Eventually, any potential correlations between the molecular and clinicopathological features of the neoplastic samples and the abundance of F. nucleatum were analyzed.ResultsThe relative frequency of F. nucleatum was significantly increased in cancerous tissue compared to adjacent non-tumor tissues. Furthermore, the high level of F. nucleatum was significantly associated with histological grade III and IV CRC tissues (P = 0.027 and P = 0.022, respectively) and perineural invasion-positive patients (P = 0.037). In addition, the expression levels of IL-6, IL-17, TNF-α,IL-12β, TLR-2, and TLR-4 as well as miR-21 and miR-31 showed a significant increase in the cancer group. A notable correlation was also observed between the high status of F. nucleatum and the expression of IL-6, TNF-α and miR-21.ConclusionOur results emphasize the importance of F. nucleatum and changes in the expression of genes involved in CRC. Studying the microbial profile and gene expression changes in CRC patients may be a promising approach to improve screening methods and provide therapeutic strategies.

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Section: Discussionmentioning

confidence: 98%

Section: Discussionmentioning

confidence: 98%

Exploring the interplay between Fusobacterium nucleatum with the expression of microRNA, and inflammatory mediators in colorectal cancer

Bostanghadiri,

Razavi,

Shariati

et al. 2023

Front. Microbiol.

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“…Moreover, activation of the NF-kB signaling pathway induced the expression of miRNA-31, which directly acted upon eukaryotic initiation factor 4f-binding protein 1/2 to promote CRC cell proliferation by inhibiting its expression. On the other hand, miRNA-31 enhanced the inhibitory effect of F. nucleatum on autophagic flux by targeting SYNTAXIN-12 and increased the intracellular survival of F. nucleatum resulting in continuous infection of CRC cells and enhanced tumorigenicity[ 32 ].…”

Section: Mechanisms Of Carcinogenesis Of F Nucleatummentioning

confidence: 99%

Application of Fusobacterium nucleatum as a biomarker in gastrointestinal malignancies

Yu,

Li,

Xin

et al. 2024

World J Gastrointest Oncol

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The morbidity and mortality of gastrointestinal (GI) malignancies are among the highest in the world, posing a serious threat to human health. Because of the insidious onset of the cancer, it is difficult for patients to be diagnosed at an early stage, and it rapidly progresses to an advanced stage, resulting in poor treatment and prognosis. Fusobacterium nucleatum (F. nucleatum ) is a gram-negative, spore-free anaerobic bacterium that primarily colonizes the oral cavity and is implicated in the development of colorectal, esophageal, gastric, and pancreatic cancers via various intricate mechanisms. Recent development in novel research suggests that F. nucleatum may function as a biomarker in GI malignancies. Detecting the abundance of F. nucleatum in stool, saliva, and serum samples of patients may aid in the diagnosis, risk assessment, and prognosis monitoring of GI malignancies. This editorial systematically describes the biological roles and mechanisms of F. nucleatum in GI malignancies focusing on the application of F. nucleatum as a biomarker in the diagnosis and prognosis of GI malignancies to promote the clinical translation of F. nucleatum and GI tumors-related research.

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“…These pathogens utilize the host cell actin network to form protrusions into adjacent cells, leading to a double-membrane vacuole forming in the new host cell, composed of the membrane of the previous and the new host 47 . Other bacteria may inhibit autophagy, a degradation and recycling process that is effective against invading bacteria 48 . Similar invasion, evasion, and survival mechanisms may be used by intracellular bacteria in the cancer setting, and merit future studies.…”

Section: Lifestyles Of Intracellular Bacteriamentioning

confidence: 99%

“…Autophagy is modulated by various intracellular bacteria, affecting their niche and enabling intracellular survival. F. nucleatum , for example, may promote initiation of autophagy through downregulation of miR-18a* and miR-4802 43 , while autophagosome fusion with the lysosome may be inhibited via intracellular F. nucleatum -mediated upregulation of miR-31 48 , 153 . An expansion of myeloid-derived immune cells including tumor-associated macrophages (TAMs), tumor-associated neutrophils (TANs) and myeloid-derived suppressor cells (MDSCs) in a F. nucleatum -inoculated CRC mouse model was accompanied by T-cell suppression and increased expression of immunosuppressive molecules such as CTLA4 and arginase-1 17 , 154 .…”

Section: Potential Impacts Of Intracellular Bacteria On Cancer Phenot...mentioning

confidence: 99%

Intracellular bacteria in cancer—prospects and debates

Schorr,

Mathies,

Elinav

et al. 2023

npj Biofilms Microbiomes

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Recent evidence suggests that some human cancers may harbor low-biomass microbial ecosystems, spanning bacteria, viruses, and fungi. Bacteria, the most-studied kingdom in this context, are suggested by these studies to localize within cancer cells, immune cells and other tumor microenvironment cell types, where they are postulated to impact multiple cancer-related functions. Herein, we provide an overview of intratumoral bacteria, while focusing on intracellular bacteria, their suggested molecular activities, communication networks, host invasion and evasion strategies, and long-term colonization capacity. We highlight how the integration of sequencing-based and spatial techniques may enable the recognition of bacterial tumor niches. We discuss pitfalls, debates and challenges in decisively proving the existence and function of intratumoral microbes, while reaching a mechanistic elucidation of their impacts on tumor behavior and treatment responses. Together, a causative understanding of possible roles played by intracellular bacteria in cancer may enable their future utilization in diagnosis, patient stratification, and treatment.

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MicroRNA-31 induced by Fusobacterium nucleatum infection promotes colorectal cancer tumorigenesis

Cited by 6 publications

References 66 publications

Exploring the interplay between Fusobacterium nucleatum with the expression of microRNA, and inflammatory mediators in colorectal cancer

Exploring the interplay between Fusobacterium nucleatum with the expression of microRNA, and inflammatory mediators in colorectal cancer

Application of Fusobacterium nucleatum as a biomarker in gastrointestinal malignancies

Intracellular bacteria in cancer—prospects and debates

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