Initial gut microbiota composition is a determining factor in the promotion of colorectal cancer by oral iron supplementation: evidence from a murine model.

IF 13.8 1区生物学 Q1 MICROBIOLOGY

Microbiome Pub Date : 2025-04-21 DOI:10.1186/s40168-025-02101-1

Thibault Cuisiniere, Roy Hajjar, Manon Oliero, Annie Calvé, Gabriela Fragoso, Hervé Vennin Rendos, Claire Gerkins, Nassima Taleb, Marianne Gagnon-Konamna, François Dagbert, Rasmy Loungnarath, Herawaty Sebajang, Frank Schwenter, Ramses Wassef, Richard Ratelle, Éric De Broux, Carole Richard, Manuela M Santos

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引用次数: 0

Abstract

Background: Colorectal cancer (CRC) development is influenced by both iron and gut microbiota composition. While iron supplementation is routinely used to manage anemia in CRC patients, it may also impact gut microbiota and promote tumorigenesis. In this study, we investigated the impact of initial gut microbiota composition on iron-promoted tumorigenesis. We performed fecal microbiota transplantation (FMT) in Apc^Min/+ mice using samples from healthy controls, CRC patients, and mice, followed by exposure to iron sufficient or iron excess diets.

Results: We found that iron supplementation promoted CRC and resulted in distinct gut microbiota changes in Apc^Min/+ mice receiving FMT from CRC patients (FMT-CRC), but not from healthy controls or mice. Oral treatment with identified bacterial strains, namely Faecalibaculum rodentium, Holdemanella biformis, Bifidobacterium pseudolongum, and Alistipes inops, protected FMT-CRC mice against iron-promoted tumorigenesis.

Conclusions: Our findings suggest that microbiota-targeted interventions may mitigate tumorigenic effects of iron supplementation in anemic patients with CRC.

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初始肠道菌群组成是口服补铁促进结直肠癌的决定性因素：来自小鼠模型的证据。

背景：结直肠癌（CRC）的发展受铁和肠道菌群组成的影响。虽然铁补充剂通常用于治疗结直肠癌患者的贫血，但它也可能影响肠道微生物群并促进肿瘤发生。在这项研究中，我们研究了初始肠道微生物群组成对铁促进肿瘤发生的影响。我们使用来自健康对照、结直肠癌患者和小鼠的样本对ApcMin/+小鼠进行粪便微生物群移植（FMT），然后暴露于铁充足或铁过量的饮食中。结果：我们发现，在接受结直肠癌患者（FMT-CRC） FMT的ApcMin/+小鼠中，铁补充剂促进结直肠癌，并导致明显的肠道微生物群变化，而不是来自健康对照或小鼠。经鉴定的细菌菌株，即Faecalibaculum rodentium， Holdemanella biformis， pseudolongum双歧杆菌和Alistipes inops，口服治疗可保护FMT-CRC小鼠免受铁促进的肿瘤发生。结论：我们的研究结果表明，针对微生物群的干预可能会减轻铁补充剂对结直肠癌贫血患者的致瘤作用。

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来源期刊

Microbiome MICROBIOLOGY-

CiteScore

21.90

自引率

2.60%

发文量

198

审稿时长

4 weeks

期刊介绍： Microbiome is a journal that focuses on studies of microbiomes in humans, animals, plants, and the environment. It covers both natural and manipulated microbiomes, such as those in agriculture. The journal is interested in research that uses meta-omics approaches or novel bioinformatics tools and emphasizes the community/host interaction and structure-function relationship within the microbiome. Studies that go beyond descriptive omics surveys and include experimental or theoretical approaches will be considered for publication. The journal also encourages research that establishes cause and effect relationships and supports proposed microbiome functions. However, studies of individual microbial isolates/species without exploring their impact on the host or the complex microbiome structures and functions will not be considered for publication. Microbiome is indexed in BIOSIS, Current Contents, DOAJ, Embase, MEDLINE, PubMed, PubMed Central, and Science Citations Index Expanded.