Cited by 314Gut microbiota and healthInflammatory Bowel DiseaseMitochondrial Function and Pathology

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Gut bacteria signaling to mitochondria in intestinal inflammation and cancer

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Jackson, Dakota N., Theiss, Arianne L.·2020·Gut Microbes

DOI 10.1080/19490976.2019.1592421PMC PMC7524274

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Abstract

The gastrointestinal microbiome plays a pivotal role in physiological homeostasis of the intestine as well as in the pathophysiology of diseases including inflammatory bowel diseases (IBD) and colorectal cancer (CRC). Emerging evidence suggests that gut microbiota signal to the mitochondria of mucosal cells, including epithelial cells and immune cells. Gut microbiota signaling to mitochondria has been shown to alter mitochondrial metabolism, activate immune cells, induce inflammasome signaling, and alter epithelial barrier function. Both dysbiosis of the gut microbiota and mitochondrial dysfunction are associated with chronic intestinal inflammation and CRC. This review discusses mitochondrial metabolism of gut mucosal cells, mitochondrial dysfunction, and known gut microbiota-mediated mitochondrial alterations during IBD and CRC.

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Figure 1. Mitochondrial dysfunction associated with IBD. Pro-inflammatory cytokines and bacterial toxins are implicated in mitochondrial alterations during IBD. Decreased activity of ETC complexes, decreased ATP levels, accumulation of mtROS, accumulation of misfolded or unfolded proteins in the matrix, and ultrastructural changes such as dissolved cristae have been reported in mitochondria of the epithelium of IBD patients. Subsequent loss of epithelial barrier integrity, epithelial cell apoptosis, and bacterial invasion have been demonstrated following mitochondrial dysfunction in the epithelium. mtDNA is released into the serum of IBD patients and serves as a DAMP for immune cell activation. Additionally, damaged mitochondria can signal inflammasome activation, leading to pro-inflammatory cytokine production.CC BY-NC-ND · PubMed Central

Figure 2. Mitochondrial alterations play a central role in CRC tumorigenesis. Cancer cells exhibit hybrid metabolism, utilizing both glycolysis and oxidative phosphorylation to drive ATP production and adapt to ever-changing microenvironments. Acetyl-CoA produced by glycolysis feeds the TCA cycle to produce cofactors NADH and FADH2 that donate electrons to the ETC and drive oxidative phosphorylation. Altered use of mitochondrial enzymes generate anabolic precursors necessary for rapid cell proliferation. Hypoxia is implicated as a driver of progression to CRC, with Hif-1α providing protection via enhanced D2HGDH production to inhibit the oncometabolite D2HG produced by the TCA cycle. Hif-2α directly targets STEAP4 which modulates mitochondrial iron balance and function. Although mtDNA mutations are demonstrated early in neoplasias, progression to malignancy selects for non-pathogenic mtDNA mutations and functioning mitochondria. These mitochondrial alterations enhance proliferation and metastatic potential and decrease apoptosis, driving CRC tumorigenesis.CC BY-NC-ND · PubMed Central

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Authors: Jackson, D. N., & Theiss, A. L.
Affiliations: Baylor University Medical Center (US)
Corresponding author: Theiss, Arianne L.
ORCID: Theiss, Arianne L.
Venue: Gut Microbes
Publisher: Informa UK Limited
Published: 2019-03-26
Volume: 11
Issue: 3
Pages: 285-304
ISSN: 1949-0976 (ISSN-L)
1949-0984
DOI: 10.1080/19490976.2019.1592421
PMC: PMC7524274
OpenAlex: W2923380089
Cited by: 312
References: 149
Citations by year: 2026: 44 · 2025: 51 · 2024: 47 · 2023: 43 · 2022: 71 · 2021: 33 · 2020: 20 · 2019: 3
FWCI: 2.83
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by-nc-nd
creativecommons.org/licenses/by-nc-nd/4.0/ (vor)
Locations: Gut Microbes (publishedVersion, cc-by-nc-nd)
PubMed Central (publishedVersion, cc-by-nc-nd)
PubMed (publishedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders: Crohn’s and Colitis Foundation (391869)
National Institute of Diabetes and Digestive and Kidney Diseases (R01-DK117001)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Health Sciences › Medicine › Gastroenterology › Inflammatory Bowel Disease
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
Keywords: gut microbiota, mitochondrial signaling, mitochondrial metabolism, mitochondrial dysfunction, intestinal inflammation, inflammatory bowel disease, colorectal cancer, mucosal epithelial cells, immune cells, inflammasome signaling, epithelial barrier function, dysbiosis
MeSH terms: Gastrointestinal Microbiome, Animals, Colitis, Humans, Inflammation, Intestinal Mucosa, Mitochondria, Colorectal Neoplasms, Inflammatory Bowel Diseases, Immunity, Mucosal

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